Dogs, Zoonoses and Public Health 2nd Edition This page intentionally left blank Dogs, Zoonoses and Public Health 2nd Edition Edited by Calum N.L. Macpherson Windward Islands Research and Education Foundation, St. George’s University, Grenada François-Xavier Meslin World Health Organization, Geneva, Switzerland Alexander I. Wandeler OIE Reference Laboratory for Rabies, WHO Collaborating Centre, Ontario, Canada CABI is a trading name of CAB International CABI CABI Nosworthy Way 38 Chauncey Street Wallingford Suite 1002 Oxfordshire OX10 8DE Boston, MA 02111 UK USA Tel: +44 (0)1491 832111 Tel: +1 800 552 3083 (toll free) Fax: +44 (0)1491 833508 Tel: +1 (0)617 395 4051 E-mail:
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[email protected] Website: www.cabi.org © CAB International 2013. All rights reserved. No part of this publication may be reproduced in any form or by any means, electronically, mechanically, by photocopying, recording or otherwise, without the prior permission of the copyright owners. A catalogue record for this book is available from the British Library, London, UK. Library of Congress Cataloging-in-Publication Data Dogs, zoonoses, and public health / edited by Calum N.L. Macpherson, Francois-Xavier Meslin, Alexander I. Wandeler. -- 2nd ed. p. ; cm. Includes bibliographical references and index. ISBN 978-1-84593-835-2 (hbk.) I. Macpherson, C. N. L. (Calum N. L.) II. Meslin, F.-X. (Francois-X.) III. Wandeler, Alexander I. [DNLM: 1. Dog Diseases. 2. Zoonoses. 3. Communicable Diseases-- transmission. 4. Dogs. 5. Public Health. WC 950] 614.4'3--dc23 2012029380 ISBN-13: 978-1-84593-835-2 Commissioning editor: Rachel Cutts Editorial assistant: Chris Shire Production editor: Shankari Wilford Typeset by SPi, Pondicherry, India. Printed and bound in the UK by CPI Group (UK) Ltd, Croydon, CR0 4YY. Torgerson 9 Dogs and Nematode Zoonoses 153 Eric R. Arzt 6 Dogs and Protozoan Zoonoses 93 Karen F. Beck 2 Benefits of the Human–Dog Relationship 13 Dennis C. Snowden and Christine M. Butcher and Tiny de Keuster 4 Dogs and Rabies 43 Alexander I. and François-Xavier Meslin 5 Dogs and Bacterial Zoonoses 67 Bruno B. Eva Waiblinger. Chomel and Jonathan J. and François-Xavier Meslin 3 Dog-Associated Problems Affecting Public Health and Community Well-Being 24 Ray L. Halliwell 11 Dog Population Management 177 Elly Hiby v .W. Morgan 10 Dogs and Ectoparasitic Zoonoses 162 Richard E. Turner. Budke 7 Dogs and Trematode Zoonoses 109 Albis Francesco Gabrielli 8 Dogs and Cestode Zoonoses 127 Calum N. Wandeler. Macpherson and Paul R.L. John Bingham. Contents Contributors vii Preface to 2nd Edition ix 1 The Human–Dog Relationship: A Tale of Two Species 1 Alan M. Craig. Control. Philip S. Miles. Katie R. and Elimination in Dogs 205 Tiziana Lembo.vi Contents 12 Zoonoses Prevention. and François-Xavier Meslin 13 Fertility Control in Dogs 259 Giovanna Massei Index 271 . Hampson. Michael A. World Health Organization. UK. E-mail: bbchomel@ ucdavis. E-mail: tl36g@udcf. Dr Albis Francesco Gabrielli. Craig.gla. Graham Kerr Building. College Station. University of Glasgow. E-mail: gabriellia@who. Texas A&M University. Private Bag 24. TX 77843-4458. University of Glasgow. Switzerland. E-mail: Katie. Hampson@glasgow. 40550 Route 25. Contributors Dr Jonathan J. E-mail: EllyHiby@wspa-international. Agricultural Research Service. E-mail: jonathan.Bingham@csiro. Halliwell. Department of Population Health & Reproduction.usda. USA. West Lafayatte.ac. VIC 3219. Salford M5 4WT.int Professor Richard E. Davis.com Dr Katie R. Bearsden Road. UK. Center for the Human Animal Bond. Indiana 47907-1243. School of Veterinary Medicine. Salisburylaan 133. ac. Glasgow G12 8QQ. Budke. Geelong. E-mail: abeck@purdue. USDA. UK. University of Salford. UK. Department of Control of Neglected Tropical Diseases.dekeuster@ugent. Edinburgh EH3 6AR. Ghent University.uk Dr Elly Hiby. Arzt. Institute of Biodiversity Animal Health and Comparative Medicine. World Society for the Protection of Animals. Biosciences Research Institute. 5 Portarlington Road. E-mail: CBudke@cvm. Foreign Animal Disease Research Unit. USA. Belgium. UK. Dr Bruno B. New York 11957. Chomel. Plum Island Animal Disease Center. Butcher. Faculty of Veterinary Medicine. Commonwealth Scientific and Industrial Research Organisation (CSIRO).au Dr Christine M.edu Professor Philip S. VIC 3220. Beck. USA. Australian Animal Health Laboratory. Glasgow G61 1QH.tamu. Institute of Comparative Epidemiology.edu Dr John Bingham.arzt@ars. Australia. 20 Avenue Appia. Department of Pathobiology. 196 Hall Lane.W. Essex RM14 1TD.edu Dr Ray L. Orient Point. London C1X 8HB. California 95616. Hampson. College of Veterinary Medicine & Biomedical Sciences. 222 Grays Inn Road.uk vii . 5th Floor. Upminster. Australia. E-mail: tiny. University of California. USA. Faculty of Veterinary Medicine. 2a Ainslie Place. The Wylie Veterinary Centre.gov Professor Alan M. Dept. E-mail: John. 9820 Merelbeke. E-mail: richard_halliwell@btopenworld. School of Environment & Life Sciences. Purdue University. of Veterinary Integrative Biosciences.org Dr Tiny de Keuster. UK. East Geelong.be Dr Tiziana Lembo. Cestode Zoonoses Research Group. CH-1211 Geneva 27. Vorderi Siten 30. E-mail: dennis@turner-iet. University of Bristol. College Station.ac. Box 11300.ch Dr Dennis C. P. 3851 Fallowfield Road. Department of Veterinary Pathobiology. E-mail: alexwandeler@rogers. Dr Eric R. Nepean. Box 7. Dr Alexander I. Bristol BS8 1UG. UK.massei@fera. UK. Vetsuisse Faculty. Sand Hutton. P. College of Veterinary Medicine. Ontario K2H 8P9. Switzerland. Dr Turner + Partner Ltd. TX 77843-4467.ch Dr Eva Waiblinger. Keppel Street. Animal Diseases Research Institute.tamu. USA.uk Dr Karen F.O.L. London WC1E 7HT. Torgerson.viii Contributors Professor Calum N. E-mail: ptorgerson@vetclinics. E-mail:
[email protected] . George’s University. E-mail: giovanna.Morgan@ bristol. E-mail: meslinf@who. Morgan. World Health Organization. Section for Veterinary Epidemiology. George’s. Institute for applied Ethology and Animal Psychology. Department of Neglected Tropical Diseases. Turner. Canada. Macpherson. Switzerland. E-mail: ksnowden@cvm. Switzerland. Switzerland. Institute for applied Ethology and Animal Psychology. Snowden. P. Windward Islands Research and Education Foundation.uk Dr François-Xavier Meslin. London School of Hygiene and Tropical Medicine. St. York YO41 1LZ.edu Professor Paul R. St. Box 32. Grenada.int Professor Michael A. OIE Reference Laboratory for Rabies.O. 1211 Geneva 27. Miles. E-mail: Eric.gsi. Avenue Appia 20. CH-8816 Hirzel. CH-8816 Hirzel.uzh. WHO Collaborating Centre. Veterinary Parasitology and Ecology Research Group. School of Biological Sciences.O. University of Zurich. UK.gov. Food and Environment Research Agency. Wandeler. Woodland Road.edu Giovanna Massei. the Middle East. Asia. for sniffing out drugs and other illegal substances. However. and immunology that have provided new insights into our understanding of the zoonotic infec- tions humans share with dogs. speciation. Dogs are used in law enforce- ment: detecting people being smuggled across international borders. dogs play an essential role in herding. are increasingly being recognized as important areas contributing to the betterment of human health. The scope of the book has been expanded to include three new chapters. In the extensive sheep-rearing areas of the world. They are valued for their ability to find prey in rainforests. People’s attitudes regarding dogs vary greatly from being only beneficial to humans to being a serious public health nuisance. and the handicapped. A majority of those dogs. and Latin America. most people will have a strong stand regarding their role and impact on human society. Dogs may permit people to live healthier. Preface to 2nd Edition Since the first edition of this text was published in 2000. are or are regarded as strays. such as in North and South America. elderly people. with 700 million dogs. and in much of Europe. and all previous chapters have been updated and in some instances rewritten. those isolated by stigmatizing diseases such as AIDS. and companion animal medicine. and in the frozen lands of the Arctic and Antarctic. ix . and recent studies have shown the benefits dogs impart to many segments of the population including children. Dogs have numerous roles in the medical field and are increasingly used as ‘eyes’ for blind people and ‘ears’ for deaf people. The size of the world dog population is unknown but is positively correlated to that of the human population. north-west China. In the latter dogs are also used for transport. and the quality of life. As dogs are present and closely associated with humans and/or their activities in almost all places. a number of important advances have been made in the fields of genetics. northern and southern Africa. They pose a public health nuisance through bites. there are problems and dogs contribute to zoonotic infections and they foul pave- ments and public parks. New Zealand. molecular biology and epidemiology. harassment of pets. child development. The use of dogs as companion animals. Australia. A number of studies have demonstrated that the human–dog bond has a positive impact on human health. This 2nd edition provides an even more comprehensive account of the changing world and our culturally and individually diverse relationships with ‘man’s best friend’. Mongolia. the domestic dog. and for crowd and individual control. particularly in parts of Africa. hap- pier lives. Based on a number of observations it could be as high as one-tenth of the world human population. great grassland areas. Diverse groups of people in different parts of the world use dogs for sport and for hunting. particularly at night. where cultural attitudes towards dogs differ greatly. It also aims to examine how our interaction with dogs in different cultures and socio-economic conditions facilitates both beneficial and harmful processes. The final chapters deal with dog and selected disease control and prevention aspects. bacterial. adhering with international animal welfare principles. Appropriate solutions to the issues. and providing methods for calculating data. Because of the strong opinions held on both sides it is difficult to get a balanced view. also in the context of human populations. Wandeler February 2012 . and their involvement in traffic accidents. components within a dog popula- tion. need to be found: a number of solutions are provided in different chapters in this book. but whatever one’s opinion. settlements. dogs are now an important part of our society in every corner of the world. and activities. The aim of the 2nd edition of this book is to provide. This section is followed by a review of the current knowledge on dog popula- tion biology and ecology. essential for designing disease prevention and control programmes.x Preface to 2nd Edition livestock and wildlife. A new chapter examines the non- disease-related issues posed by dogs. scavenging from garbage sites. including current and future methods for effective and humane dog population management.L. The objectives of the 2nd edition of this book were to review the anthropological aspects of the human–dog relationship and to identify the benefits which may be derived from and atti- tudes vis. and helminth parasitic zoonoses shared by humans and dogs. such as population size and turnover.à-vis this association in different parts of the world. for those interested in dogs and the world we share with them. and how the zoonotic diseases are currently being controlled. Calum N. Macpherson François-Xavier Meslin Alexander I. their persistent barking. and this is followed by updated reviews on all the major viral. a comprehensive updated account of the complex public health aspects of this encounter. Attention is paid to the basis of the human–dog dependency. protozoan. The positive and negative attributes polarize people’s opinions about dogs. In other words. and broad pat- even when only one senses the danger. e-mail: abeck@purdue. 2003). people bred food animals such nomadic).edu ©CAB International 2013. patterns of modern domesticated animals are and especially the human relationship with basically the same as those of their wild ances- companion animals. This selective the satisfaction of a hunger for food. Beck* Center for the Human–Animal Bond. The desired attributes environment and often even benefit from will now occur more often. in time altering the each other’s presence. Indiana. despite their differing appearance. and social behavioural with people and their domesticated animals. breeding alters the frequency of certain genes Boris M. or needed to use animals for such material prohibiting. there is as much process: the artificial selection (by people. Hence. only their fre- Many animal species usually share the same quency of occurrence. and the use of clothing was universal. 1 The Human–Dog Relationship: A Tale of Two Species Alan M. setting the stage for plant and animal domes- Just as credible a reason as any for the tication (Leach. USA Animals have generally played a great food. They may follow one characteristics of the whole animal population. 2nd Edition (eds C. another for food or water. Levinson (1969) in the breeding population. or flee together Physiological processes. In nat- terns of behaviour. people’s pets. Zoonoses and Public Health. 1859). social. are much less changed by ural symbiotic relationships. domestication of animals is their use as Animal domestication is a biological pets. role in human ecological adjustment. the propagation of those animals purposes as the saving of human labor and without them (Darwin.L. Macpherson et al. cooking as pigs and cows that retained their more * Author. Many of the economic. tors. one participant selective breeding than are morphological char- does not significantly alter the physiology or acteristics. Perhaps without when humans were less mobile (from being planning. Dogs. College of Veterinary Medicine. and new diet choices. This is not the case of the genital organs. Purdue University. size behaviour of the other. not reason to believe that man’s psychological needs were the primary cause for nature) of an animal’s characteristics by breed- domestication of animals as that man ing with the desired traits and discouraging. the gestation period. The genes them- selves are not altered (mutated). and even aesthetic characteristics sought by people Domestication for their domesticated animals are more commonly observed in the younger indi- Domestication was most probably promoted viduals of the wild type.N.) 1 . and the face. tails (curly). than their progenitors. Lawrence. It was assumed that early humans selected ognized as the adult form. tolerate the human environment of juvenile characteristics. rela.M. overall size (Campbell. arms. hair (piebald. domestic animals. dle. these animals did most animals. and can mate more than once a with parents longer than the total longevity of year (Belyaev. respec. The need to be part of a fam- what was desired. juvenile throughout their lives. De Beer. never outgrow their infantile by all who must manage an animal. thus develop. known as neoteny and even thrive with people. Price. 1966.2 A. noted that all domesticated animals exhibit 1958. cattle. 1969. 1995. find animals with wide eyes and short snouts Interestingly. which ing more similar to that which most mammals meant a more efficient deposition of meat and exhibit only during their immature stage of fat on shorter bodies. such a breeding programme ner hair. and Therefore. 2009. Darwin (1859) . ally considered more attractive. shorter horns. tive hairlessness. than with full Animals were domesticated. Homo sapiens. Many of the animals that are par- selected at the same time and the species ticularly enjoyed by our culture are those that can change more rapidly. for one grown apes. Most people 1859. lack- acteristics.. playfulness and less aggressiveness. grow these juvenile behaviours and physi- mals that were much smaller or even larger. their genetic relationship to us. many of today’s domestic animals relatively short arms are characteristics of were created by selectively breeding animals very young apes and adult humans. In growing. As the that retained the traits of the young. In contrast. behavioural characteristics including staying ears (droopy). 1984. which are life. but none thrive in it. Beck juvenile form. which are smaller and larger. These are typically features of for many inherited characteristics can be the young. a trait appreciated however. despite horses. and to a somewhat animal to stand and walk using its arms as lesser extent. Apes and all tively. 1966). humans possess many juvenile ing pigmentation in some areas). but later the domesticated forms whole life. Trut. dolphin. 1962). which was of course development. and body grow to the proportions rec. Sexually monkeys cannot remain house pets once they mature domesticated animals often have mature. It has been noted retain some of the physical attributes of the that human beings. and smaller teeth) would also promote other juvenile traits usu- (Coppinger and Schneider. such as the Chihuahua. dogs. and the conditioned to tolerate the human way of Newfoundland or Saint Bernard. the same variations in size (can be smaller or In addition to infantile physical char. 1972. their animals for tameness.g. In addition. such as the seal. The ability to stand erect. Human beings. 1989. cal characteristics is in part why none have Examples include Shetland ponies and Shire been particularly successful as pets. have more young. because we liked them. like Darwin (1859). the animal becomes hairier. Initially. and a need for touch and bond- not expend energy on bone elongation. Dmitry characteristics even as they age and grow in K. 1999). living forms can evolve relatively quickly. ily even extends to a family-oriented social cated animals were smaller than their wild structure that may persist for the individual’s ancestors. squirrel. for exam- ape matures. Darwin. larger than an ancestor). the toy breeds the larger monkeys are trainable and can be of dogs. making ing an animal that is sexually mature while them better companions and easier to han- retaining immature morphology (e. thin. or pedomorphosis (Campbell. Belyaev (1917–1985). lack of heavy brow. neoteny is one of the ways pleasing (Glocker et al. body characteristics and behaviours of the a heavy brow ridge develops. 1979). Lorenz. reason or another. espe- other attributes associated with the retention cially dogs. 1943). most domesti. All of these retain many well as its legs. the pelvis rotates and forces the ple. as gorillas and chimpanzees. and in common with juvenile great apes such cartoon characters (Gould. 1998). Montagu. Neoteny Promoting the breeding of carnivores is either early sexual maturation or retarded that retain their juvenile attributes encourages development of adult features. Apes and the larger actually larger than any wild canid. pigs. cats. The fact that the great apes out- were further manipulated to produce ani. whose strategy for sur. 6 months. tions with domesticated dogs. dogs responded to humans selected for tameness thus also selecting for as members of their pack and treated them a naturally occurring neoteny. with their juvenile qualities. this allowed more as their conspecifics (members of the humans to evolve rapidly away from their same species). 1999). 1979. were first tamed then domesticated ing the owner’s voice (Adachi et al. As prehistoric peoples travelled from gressive contact with other pups or humans.) In 1959. tameness. selected foxes were extremely tame. Trut. It is now generally accepted that dogs. or the now- can be named which has not in some coun. If we extend both these concepts to Hence. alone among animals. place to place in search of game and fertile At 7–8 months of age (maturity) he scored for lands. Hare et al. and by 20 An uneasy symbiosis must have developed. Once earlier (Shipman. much of the behaviours of the pack-oriented vival included much collaboration. began in prehistoric times. and settlements (Driscoll animals not being much alarmed by danger. wagging of tails or attracted by the prospect of an easy meal on whining to attract attention. wild wolves undoubtedly followed. try drooping ears. lupus variabilis (Clutton-Brock. The Human–Dog Relationship 3 noted that. is man’s first domesticated animal. if not necessarily genetic conspecifics. The tame led to animals with the juvenile qualities domesticated foxes also possessed some of people wanted – the domestication process. tion of a pack implies members of the same tion which we humans may not have won. Wolves warned humans of approaching dan- The tamed foxes had floppy ears with shorter ger and may have even led early hunters to tails and legs and piebald coats. Taming occurred domestication (with the juvenile characteris. 1994). 2009). some 12.. that the drooping is due to Mesolithic (15. farms. though some feel it may have been even experiment that proved domestication. It is generally accepted that a seems probable. avoiding the competi. tion. human social order and culture. friendliness. 2007. cats silver foxes (Vulpes vulpes) during their first about 5000 (Morey. extinct C. Keeping the off- ing for accepting human captivity and social spring of those animals particularly being contact (Belyaev. generations 35% foxes were extremely tame.000 years nile trait. were animal. from the wolf. can now rec- The Ancestor of the Dog ognize where a human is pointing (Hare. Wolf domestication started in the late by some authors. people was bred.000 years ago) after humans the disuse of the muscles of the ear..’ (Darwin did not appreciate true relationship between humans and dogs that droopy ears is the retention of a juve. waste people left behind. Apparently animals that both could eat. lupus pallipes. species. Only about 10% the bones. from the built houses. as the conventional definition of Humans. they extend parenthood and close. uneaten food. The conventional defini- primate ancestors. and even the human of wild foxes display a lack of fear or aggres. 2005. 2007). et al. ‘Not a single domestic animal subspecies of C. we can explain a great deal of our interac- not dog. Dogs. and the view suggested 1995). In time. At this stage the sion in captivity. just by select. 2009). 1969. include ecological and social ‘conspecif- ness with each other and pets. could be captured and bred. as individual animals were rewarded with tics and behaviours) of a wild canid can occur food when they approached. in other ics’. main. the social cognitive skills observed in today’s The innate response for dogs to accept domestic dog (Hare et al. recall their owner’s face when hear- familiaris. but dogs still retained Early humans. Hare and Tomasello. Tamed animals within 20 animal generations. Dogs appear to be evolving to be even better adapted to their human-dominated environment.. Sheep and goats are a month Belyaev observed bred wild-caught traced back approximately 10. 2005).. By 10 generations 18% of the wolf was not so much loved as tolerated. probably one of the smaller and imitate an owner’s behaviours (Range . Man. aggression implies a conspecific interac- tain behaviours more typical of the young. words.000 years. selecting those that made nonag. Canis 2002). Belyaev (1979) began an ago. breed to another has been increased by selec. It is important to distinguish straying The progeny of true strays are feral pets from ownerless strays. that forms the pets. 1973). most peo. 1974).. 1980). In Australia. averaging 52% for all 17 European countries The rate and range of changes that distin. low-to- middle-income areas. including animal bite and inappropriate in Italy. On one hand. 60% in The Netherlands. 1975. low-income areas where 1. on the other hand.M. while strays are controlled . veys and there is considerable variation in From the human’s point of view. dog keeping is common (Berman and Dunbar. Most relied on surveys of a ‘member’ of the family. 2002). Straying pets are best man- to either socially or financially support ani. behaviours. households.4 A. 2. 1983). tionships.g. 1982). 71% in Belgium. dumps. especially where peo- The dog population in urban and suburban ple have direct access to the streets (e. Missouri (Fox et al. Berkeley. 1983a. As a general rule. and 2002. New Jersey (Daniels. there are relatively few tive breeding within relatively small popula. they are sible ownership. studies of urban stray or feral dogs. and at of low-to-middle-income private housing or times interchangeable. Ownerless strays are more com- mon in low-density. guish the dog from wolf or even from one dog 1991). By contrast. Dogs were bred to meet the demands of populations have been studied in Baltimore. such as around parks. New York City son for the domestication or even keeping of (Rubin and Beck. Scott and 3. mal control. not human.. differing climates and roles (Coppinger and Maryland (Beck. areas areas is composed of three interacting. Inc. Most people intui. 61% ily. It is this preference to exist in a the 6. 42% have more than one animal (American tively respond to a dog’s ‘play-soliciting Pet Products Manufacturers Association. straying pets are The Dog Population more common in high human density. Specific tions. we see problems in the fam. strays. Coppinger. on livestock (Beck. around the world. the dog is methods used. indeed. cat. 55% in Britain. There is no one rea. or a cat (Heady. 1989). subpopulations: row houses). Nevertheless. they managed or controlled by different means are protected because society is unwilling (Beck. 1999. approximately 60% of dog would.. 2006). Nesbitt. because they dogs. or national sur- its owner (master) are a true social group.. and/or bird ownership in European hierarchy or when the animal. 1996). McHarg et al. St Louis. When there is a lack of a clear Dog. more than 62% of to their animals as a member of the family US households have companion animals and (Beck and Katcher. Today. dogs do not necessarily unfairly blamed by popular literature as the seek help in an emergency (Macpherson and major cause of dog bite injuries and attacks Roberts. Italy (Hansen. consumer panels and estimate about 78. The first extension of the dog–human Estimates of the total dog population pack hypothesis would be that a dog and come from local. is the leader. surveyed (Reader’s Digest Association. Newark.2 ple who are dog owners specifically refer million owned dogs. 1998). dominated by a leader. 63% in France. 1975. 1975). 1983). 2010). California dogs. ownerless animals usually referred to as Causey. 1996. Fox et al. Beck et al. 37% in Germany..2 million households have one or more pack. pets that never roam without human there is shelter and fewer requests for ani- supervision. Social attitude towards strays and cause different problems for society and are feral dogs is ambivalent. however. bow’ or growl in much the same way another 2011). b). 1995). sporadically. and 70% in Ireland. straying pets that roam continuously or or abandoned parts of the inner city (Beck. 53% of the households have either a dog basis for many successful human–dog rela. and some areas in Mexico and the American south-west (Daniels and Bekoff. 1975. aged by encouraging and enforcing respon- mal control and. regional. People should not tether The major issues associated with dogs in their dogs on ropes too much longer than this. 1999). 1985). Dog bite can be serious. popular press still often quotes figures in 50% of people bitten by dogs without known excess of 12 million. dogs. observed without extensive study followed by those owned by the family of the No country has an official census of victim. 2005. 1992). non-owned or stray dogs (Patronek et al. their pet or feral dog population. In the mals.. 1994. Harris are indistinguishable from owned roaming et al. Strays had the lowest rate. Patronek and account for less than 10% of all bites (Beck. One reason for the disproportionate precise figures of the number of animals ‘over-reporting’ of strays is the perception killed in animal shelters. However. 1982. owners sought medical treatment. Lauer et al. Frank.. and there are statistical for example in population-based surveys or models to assess the owned population on military bases. 1991. Beck Rubin and Beck. disappear if people do not abandon pets 2007. such as the boarding-up of vacant buildings. a neighbour (Beck and Jones. 1981). people to only 29% of people bitten by family-owned assumed responsibility for its survival. reported than bites from owned animals. 1982).. cities include animal bite. 1974. In the United that strays cause more disease. potential disease. Bögel. and so soon account for nearly 60% of fatalities (Beck. 1996. United States the owned pet dog. Dogs owned by the and unowned stray dogs are not easily neighbour of the victim have the highest rate. 1982). not strays. estimates range between 2 and Therefore. should set a maximum length of leash – about mals in populated areas concerns dogs. people tend to seek medical care 6 million for dogs and cats killed in ani. This simple regulation Contact is a way of reducing animal bite and many of the problems associated with dogs. the dog does not do well without United States. such as rabies. compared By domesticating the dog. Where there is good reporting of all bites. fatalities have been from owned dogs. All of the One adaptation of unowned stray dogs US studies using reported bite-rate data show in an urban environment is to behave like the same pattern: people aged 4–19 receive socialized pet dogs (Fielding et al. mainly because of the increas- stray dogs do not reproduce well enough ing ownership of pit bull-like dogs. is common in many cit- Social Conflicts of Dog–Human ies around the world. dogs and are tolerated as loose pets and not Contrary to public perception. which damage. 1990)... of a bite (Talan et al.. Therefore the differences between owned leads the pack in bite rate. Dog bites ment. considerations for the animals themselves. which to establish a wild population. Hanna and Selby. In that way they et al. 1. Glickman. States. All (Beck. as many infec- These are real issues but there are also real tious agents have been identified at the site solutions. and report the bite more frequently when bit- mal shelters each year (Rowan. environmental longer leads can endanger the animals. and death from . Considering the patterns of dog-bite injury. the fatal dog bite problem is the intervention of humans. 1997. 2011.. 1975. it is not surprising that a leash law. The law Most of the problems associated with ani. The ten by an animal whose owner is not known. in one form or another. The Human–Dog Relationship 5 by capture and alterations of the environ. especially children. and 39% when the dog was owned by and in common with other domestic ani. although bites from strays are more commonly methods exists for those interested in ani. and clearing dumps and urban One concern about dogs in cities is that they lots (Beck. There are no 1991). about 20% of all dog bites (Beck. 2000).8 m (6 feet) or less. and humane may become entangled. in the wild dogs – a form of ‘cultural camouflage’. Sacks et al. 2002). In urban areas increasing.. 2004). Bini et al. may bite people. mal control or public health (Beck. 1981. 1983. 1987). the so-called ‘curb your dog’ laws. 1991) or rabies (Beck ticularly important for those dog owners with et al. Nevertheless. those exhibiting undesirable behaviours daily. Animals that are routinely ‘de-wormed’ to have little impact on human public heath. With the There are numerous studies establish- exception of the potential of rabies. Most cities in the United States prohibit Owned dogs with undesirable behav. such as biting. Avoiding owners clean up after their dogs in public owner–dog conflicts is one of the most effi. inap. In addition. Pinckney and Kennedy. and aggressiveness toward peo. Beck trauma has been reported (Bini et al. young children. is more than just an some. Dogs and disease The Social and Health Benefits of Dogs in Society With the exception of rabies. One of the most common regulations to such as barking. parasite contamination is routine veterinary In the United States. hyperactivity. a and many share the human home as well. It is now widely recognized that the child play are more common (Weiss et al. allow parasite transmission from dog to dog. pets from entering restaurants or food stores. and failure to clean up after the slips and falls associated with childhood – dogs seeds the environment with Toxocara indeed. and keeping dogs involvement (Glickman and Shofer. are more likely to be or going on public transportation. have a higher risk of being relinquished ecation.. Odds ratio = 1. Dog waste. iours. rather than sidewalk. America and Europe have laws that restrict the after which they are usually killed. Compared animals in enclosed carriers or service dogs with dogs having no unwanted behaviour. ingestion of embryonated Toxocara eggs can 1998). except for relinquished to an animal shelter... on a leash or always having them supervised The best way to lessen the occurrence of when on public property. But we should always try to minimize cause human illness such as toxocariasis or bite injury. serious and are also a human public health issue. 1987. (Beck. For oth. ownerless dogs are part of the urban scene a source of parasites. Brandow. most cosmopolitan the dog’s nature is one of the important issues centres encourage or enforce ‘scoop laws’ so in public health and animal welfare. 1979.3 versus this way people do not step into waste. the injuries associated with routine eggs. apart from being ple.. use the street. 1995). stray dogs continue care. aggressiveness toward age or require dog owners to have their dogs other pets. in public some are adopted and become owned pets. most of the diseases transmitted from dogs to humans do not attract Dogs are present in almost all human settings. Controlling the con. aesthetic problem. However dog waste. 2000). Dog faeces in public areas Borchelt et al.. 2011. most large metropolitan areas in North as pests and removed from life on the streets. one involving an intes- policy that encourages having dogs that are tinal migration and the other having ocular well socialized to people. infection and fatal injury are rare. chewing. which 8. areas. the vast ing that dogs are frequently parasitized by majority of bites are no more serious than Toxocara canis.5 (Patronek et al. although activity of animals. assisting people with special needs.M. is carried to storm drains during street wash- flicts between the owner’s expectations and ing or rain. which is par- it from animal bites (Beck. they replace the children who have . be do not pass contaminated faeces. Torrence et al. To address this prob- ers. environmental pollution. The safest and most humane way visceral larva migrans. much public attention.. Basic courtesy cient ways to lessen relinquishment of dogs permits dogs and people to share the cities in to animal shelters and reduce dog bites. strays are animals that must be captured lem. In to an animal shelter. Sacks et al. 1982. ways that benefit both.6 A. For perennial nuisance in cities. especially dogs. reduce dog waste in public areas is to encour- propriate elimination. 2008). 1996).. The disease appears to reduce bites from dogs is a public health to have two forms. For some peo. for def- ple. is viewed as a kind of that live out their lives as wild canids. . there was no clear explanation for the results. support has grown for pro- vival. Baun than non-owners. In the United ship may reduce the risk factors associated States. nearly 1000 non-institutionalized Katcher and Beck. A study of people hospitalized Animals allowed people to experience bond- after a heart attack found that 94% of those ing. and the mental health. Pet owners had lower systolic blood settings pressures. there was the first epidemio. A discriminate analysis demonstrated tecting the right of pet ownership for older that pet ownership accounted for 2–3% of the adults living in the community.. animals were being used in . ionship. their dogs experience more social contact bers of the family. sisted over the 10-month study period and 2003. ship generally had value. 1983). 1991). People with good human contact are Naturally occurring events in people’s lives healthier than those who are isolated from are enhanced because of animal compan- others (Lynch. opportunities to meet other people. indi. they are playmates were very similar. companionship and a sense of security. Siegel (1993) suggested that pets have who happened to own pets were alive after a stress-reducing effect.. For instance. two species with and increased the number and duration of the common goal of surviving and enjoying their recreational walks. 1996. Beck and Meyers. are perceived as mem. The Human–Dog Relationship 7 grown and moved away or perhaps were socio-economic profiles of the two groups never born. Consequently. We are Serpell (1991) reported that dog owners beginning to understand this complex bond experienced fewer minor health problems between pets and people. of loneliness (Beck and Katcher. 2011. 1984. It appears that pet owner- for the children still at home.. ownership. possibly for rea- dog also have children at home. 2003. 1996). and triglyc- eride values. 1999. Beck and Katcher. dogs afford increased with risk behaviours. 1996). ple noted that the pets provided them with In 1980. While animal owner- et al. Unlike talking to older adult Medicare patients were evaluated other humans. 1983. 1977. Messent. Because pet ani. and for others. especially dogs. the most remark- ence of unfamiliar dogs. benefits of animal interaction (Barker and A more recent study of the benefits of Wolen. There is continued frequency of heart disease. is significant and growing evidence documenting the health cost effective. Most of the peo- (Friedmann et al. Those subjects who owned of blood pressure when talking to pets. any animal correlated with improved sur. plasma cholesterol. 1986). 2000). people experience a decrease prospectively. The ownership of of animals (Dembicki and Anderson. 1980). The effects per- life together (Beck. 1983). considering the nursing home settings. 1990). Even in the pres. 1996. people experience able benefits to health were for those who a temporary decrease in blood pressure owned dogs (Siegel. and encour- variance (Friedmann et al. While pet owners engaged in Long before there was any evidence that more exercise. While 2–3% aging animal contact for those in long-term may seem small.. interactions with animals found that pet owners had reductions in some common risk factors for cardiovascular disease when compared with non-owners (Anderson et al. 2008). The use of animals in therapeutic 1992). pets appeared to experience less distress cating that they are more relaxed with them and required fewer visits to their physicians than with people (Katcher et al. they also ate more meat and animal contact enhanced physical and ‘take-out’ foods than non-owners. and logical report documenting the value of pet the opportunity for fun/play and relaxation. Wilson. more than half of the families with a with cardiovascular disease.. pet ownership is one way and longer conversations than when walking people can be protected from the ravages alone (Johnson et al. At the very sons that go beyond simply an association least. people walking with mals. In a study. The elderly often the 1st year compared with 72% of those who benefit the most from the companionship did not own any animal. for some people. the impact. Potential exists for zoonotic infectious research needs to be directed to establish . or parasitic disease. and cages. and Katcher. More people. the frequency of most A survey of 150 selected US and 74 zoonotic diseases can be lessened. and the handicapped. zoonoses. Much of the early allergy. parasitism. 15% small mammals. Prevention can be addressed by: literature documents nothing more than for- 1. help many enjoy dogs while protecting the Potential problems involve rabies. 4. The most common therapeutic animal and injury from bites – there is long his- is the dog. Beck and Katcher. contact carries risks. dogs 3. perhaps Canadian humane societies found that 49 even eliminated. and to support the positive benefits of animal ringworm (Walter-Toews. for those who own or interact with compan- ion animals. selective breeding. or facilitated therapy’ or AFT. sensitive public health policy would also based programmes had printed guidelines. Salmonella public’s health. 1984). The most common kinds of AFT programmes are: Conclusion 1. Veterinary care to More than 94% used dog and/or cats. and 10% birds tions. are greater risks as programmes involve more socially isolated. From the very beginning AFT has paralleled the use of animals as pets Future research will improve both the and many of the therapeutic uses are exten. viral. Interactions with adults where animal contact is facilitated in dogs may very well be one of our more suc- people’s homes. made animal ownership a safe. 1996). responsi- More than 48% of US and 43% of Canadian ble legislation. proper selection of animals. having comprehensive infection-control mostly dogs. the elderly. referred to as ‘animal. the animals themselves. cessful strategies for survival. safety and efficacy of the use of animals in ther- sions of the health benefits now recognized apeutic settings. 1985. mostly documents the detri- providing riding directed towards physical mental effects of animal contact – including therapy.000 years ago.8 A. 3.M. horseback riding (equine) programmes including dogs. infectious diseases. AFT programmes occur tory of healthy interaction. Today. and best ‘medicines’ are appropriate concentra- 5. Beck therapeutic settings. companionship for various segments of the While AFT has a good safety record. ever since people began living in villages 2. institutionally based programmes where animals either reside in the facility or are Dogs have been part of human households brought by visitors. service animals for the disabled in the continue to play a major role in the lives of home setting using specially trained animals. Often the health veterinarians. tuitous interactions with animals that happen 2. healthy. developing a surveillance and response tions of what is generally beneficial (Beck programme (Schantz. Modern and of community-based and 74% of hospital. animals. allergy. and cal history of our relationship with animals. 1993). were originally included in the programmes in the setting. people around the world. Today. non-institutional programmes for older some 12–15. with animal management (46%) of the US and 49 (66%) of the Canadian practices that would serve both humans and society programmes ran AFT programmes. 1990). especially children. and owner education have programmes consulted health profession. There is substantial evidence and Campylobacter infections. While animal throughout the developing world. and parasitic infec- rabbits. The animals. Nearly 10% rewarding experience for many. there population. bite injury. having pet policies with advice from public ditionally associated with pet care. not including people who are allergic to to be present in a therapeutic setting (Beck. setting to provide the expected comfort tra- 4. and als about zoonotic prevention. While the medi- usually dogs. 28% manage bacterial. accident. mechanical restraints such as leashes (excluding poultry) in their programmes. (2002) The Ecology of Stray Dogs. Anderson. A. A Study of Free-Ranging Urban Animals. A. 247–257. Loring. more research is needed on how health. (1981) Guidelines for planning for pets in urban areas.M. Beck. N. (1984) Physiological effects of petting dogs. Compendium on Continuing Education 2. (1975) The ecology of dog bite injury in St. American Pet Products Manufacturers Association (APPMA) (2011) 2011–2012 National Pet Owners Survey. Beck. and Katcher. Public Health Reports 90. Veterinary Forum 24.M. Journal of the American Veterinary Medical Association 184.M.M. Indiana. Counterpoint. References Adachi. 162–170. A. 29–31. W. A. Public Health Reports 100. Veterinary Clinics of North America. In: Fogle. . Beck. Journal of Veterinary Medical Education 35. pp. and Lockwood.M. In: Anderson. (1996) Between Pets and People. A. H.. Beck. A.M. American Journal of Public Health 77. (1979) Destabilizing selection as a factor in domestication.M. Boca Raton. 17–21. D.M. and Thoma. 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(1993) Companion animals. Weiss.. and Cohen. (1998) Incidence of dog bite injuries treated in emergency departments. 482–489. Siegel.M. Sinclair. G.. (1990) Stressful life events and use of physician services among the elderly. (1973) Ecology of feral dogs in Alabama. Journal of the Royal Society of Medicine 84.. (1991) The pet as an anxiolytic intervention.M. 157–167. 1993). Although no longer the most pop. Coppinger and Coppinger while separation promotes anxiety.) 13 .1* Eva Waiblinger. of the mother (or a partner) is reassuring. but Attachment theory is chronologically there is now widespread agreement that the the oldest potential explanation and is based dog was not kept for economic reasons. (1998) has proposed that interactions with 1998. and natural scenes. 1995. 1969). The presence Serpell. * Corresponding author. Switzerland The dog (Canis familiaris L. 1981. that is. Companion animals can pro- or eliminate those problems. are diverse. Mithen 2. Social sup- tion for working roles in the further develop.) is without a doubt world irrespective of their level of economic the oldest domesticated animal species and development or religious heritage. Zoonoses and Public Health. Beck. Kellert and Wilson. but upon the first social relationship between rather as a ‘companion’ animal (Messent and an infant and the mother. ‘biophilia’ or the ‘biophilia hypothesis’ have even shaped the way we think. 2010).ch ©CAB International 2013.N. The biophilia hypothesis ular companion animal in many countries. 3World Health Organization. Serpell. animal bond since the mid-1990s: in times Most of the chapters in this volume of need we seek support (emotional or deal with ‘negative’ aspects of dog–human tangible) from our social support network relationships and humane ways to reduce to help cope. Switzerland. port theory has been applied to the human– ment of the dog. stress. attachment theory (see Bowlby. 1984. Turner. animals. McNicolas and Collis. (2001) have stressed the importance of selec. members of the network or even replac- the benefits of human–dog relationships. of domestication. Switzerland.000 years. has accompanied man1 some 15. and dogs in prehistoric hunter-gatherer societies 3. 2000). 2 Institute for applied Ethology and Animal Psychology. It is therefore vide social/emotional support. either as important to summarize the positive aspects.(dog-) relationship as well as the therapeu- cated dog were found in Kesslerloch Cave tic benefits animals provide many persons: in Switzerland.600 1. Geneva. pet. and contact-seeking behaviour. 1986. e-mail: dennis@turner-iet. 2nd Edition (eds C. 2 Benefits of the Human–Dog Relationship Dennis C. from ing a human member in the network for the outset. Macpherson et al.L. and dated at c. Theories (Wilson. Dogs. 14. claims that humans are innately attracted to pet dogs can be found in every country of the nature – plants. some people. Three theories have been drawn upon to the oldest faunal remains worldwide defini. explain both the universality of the human– tively determined to be from the domesti. Hirzel. 2006). Dr Turner + Partner AG. Hirzel. social support theory (Collis and McNicolas. the reasons why man domesticated the wolf.2 and François-Xavier Meslin3 1 Institute for applied Ethology and Animal Psychology. bp (Napierala and Uerpmann.000–14. Nevertheless. and that the acquisition of a pet (dog or cat) signifi. (1991) and Allen (1996) presumably related to lower costs for health have found that a pet dog is more effective as care. somewhere between 1 and 6 months for the 1985. (World Health Organization. factors (over 5000 participants) and found that For these reasons. Further. Rost and Hartmann. Benefits Dogs especially have been shown to func- tion as social facilitators of increased contact In the last three decades research has provided with other persons.. Covert et al. cat owners did so 12% less often than non-cat Finally. The latter study also found a correla- General Effects of Animals. Brazil. multicul- tion independently of physiological severity. on the General Public: The emotional intelligence. levels of attachment to their dogs than chil- ship predicted one-year survival rates after dren in two-parent families. breaks. 1994). but the improvements disappeared emotional social support to children (Bryant. He also found an increase in 1994. and for non-communicative patients of life relative to a control group over the same in psychotherapy. Bodsworth walking activity by the dog owners. (1992) conducted a free improved learning environment (Hergowich screening clinic for cardiovascular disease risk et al. 1995b. and improved social integration and an Anderson et al. The innate releasing mechanism called the 9000 randomly selected Swiss households ‘Kindchenschema’ (infantile appearance of reporting all income and expenditures over a animals which elicits nurturing behaviour) 1-year period. working from the same laboratory. 1995a). BMI. the IAHAIO (2001) has pet owners had lower levels of accepted risk unanimously passed its ‘Rio Declaration on factors (blood pressure. Kotrschal and Ortbauer. Wilson cantly reduced complaints about minor health and Netting. especially in the hospitalization for acute myocardial infarc. This by the WHO–IAHAIO–WSPA Training was not explicable on the basis of differences in Programme on Zoonoses and Human–Animal smoking habits. 10-month period. tural school classroom. . diet. (1998). studies in Vienna have demographic. and the robustness of this solid evidence for the positive effects of dogs on effect has been demonstrated by McNicolas the health and well-being of people of all ages. early childhood stage. and other psychosocial factors. and Collis (2000). especially for the elderly (Hart. found that Spiegel (2000) showed that an elementary dog owners visited a doctor over the previous school-based dog bite prevention programme year 8% less often than non-dog owners. 1987). Somewhat later Jennings et al. concerning people in the general owners (both reductions significant). new cat owners. adults (Hart. A multitude of studies demonstrates cant for the new dog owners over the entire that companion animals provide important period. ing empathy towards companion animals (including dogs) increases empathy towards other people. which was also endorsed plasma cholesterol) than non-owners. plasma triglycerides. This has been demon- Serpell (1991) found in a prospective study strated for children. The effects remained signifi. Allen et al. 2002. shown that a dog resting quietly on its blanket Dog owners were significantly less likely to in the corner results in fewer aggressive out- die within 1 year than non-owners.. which was later substantiated by Turner a moderator of autonomic responses to stress (2004) based on a government survey of over in adults than human partners or friends. 2001). while was quite effective. and that the effects are long- lasting. This was public. Pets in Schools’. Turner et al. Especially tion between empathy towards animals and Dogs. the same year profile. Melson and Schwarz. 2003). and Coleman (2001) found that children in Friedmann and Thomas (1995) found single-parent families had significantly higher that both high social support and pet owner. In the urban. and the universality of nurturing behaviour – Ascione and Weber (1996) and Beetz taking care of and adopting young or sick and Ascione (2004) have shown that increas- animals – speak for this explanation. or socio-economic Interactions in Sao Paulo. 1985.C.14 D. for physically challenged problems and improved measures of quality persons. 2 from who differed significantly from Christians but which results concerning dogs are presented answered between Jews and Christians. the statement ‘Dogs make ideal pets’ was tions. tudes towards animals in 12 countries. have been suc. religions except Hindus. were less in favour than pet owners. and Most recent reviews of the positive effects sample type (convenience: ‘random’ sample or of companion animals.and German-speaking Swiss adults animals’. Over 6000 questionnaires were dis. while Jews were tection societies and shelters. 129–132) Physically challenged persons (Allen and Blascovich. only a brief summary assess the effects of four factors: location (coun- with exemplary literature references are try) and religious heritage. tributed and recollected from adults in urban Muslims. d Dogs: The Benefits the questionnaires contained 27 statements (five of which were control questions to assess Animals. pp. Results comparing attitudes between For the statement ‘Dogs are very likeable French. gender of the per- listed in Box 2.1. especially dogs. e. Although people from all religious An International Comparison backgrounds agreed with the statement. than those of all other religions except Muslims. with which the volunteer par- problems. and the sample connected with animal-friendly Public Attitudes to Dogs: institutions. ANOVAs were conducted to of dogs to humans.1. ‘animal friends’. understanding of the statements and seri- cessfully involved in animal-assisted inter. As this is not the main topic of ticipants had to agree or disagree in a 5-point this chapter. 1996) . from a vet practice human health and well-being were produced or dog shelter waiting room). ousness of questionnaire completion) in the ventions to help people with various health local language. Box 2. b). Only significant after an international conference organized differences are reported. Additionally. Especially emographic information on the participant. bond organizations. Non-pet owners. Women. veterinarian associa. Jews agreed more strongly than people of all other Turner (2010 and in preparation) has conducted religions. pet ownership (current or previous).. and colleagues col. men and ‘random’ persons. apallic syndrome (Röger-Lakenbrink. 2000) Down Syndrome (Limond et al. 2010) Alzheimer patients (Bateson et al. did so signifi- and suburban areas of major cities in these cantly less strongly than people of all other countries. 2006. Volunteers from many animal pro.3 Besides people questioned in animal-related institutions. 1977) Persistent vegetative state. university students. ers agreed more strongly with this statement.. 1998) Neurological/motor dysfunction (Röger-Lakenbrink. (McCardle et al. and pet own- et al. Aphasic patients in psychotherapy (Corson et al.1). while still agreeing. more strongly agreed to by pet owners and lected the completed questionnaires.. by the US National Institute of Child Health On the statement ‘Keeping animals as and Human Development (NICHD) and pets brings many benefits to the person’ all the WALTHAM Centre–Mars Inc. 2011a. son. human–animal the most dog-friendly group. although agreeing with this statement. 2. here. 1997) Autism spectrum disorders (Grandin et al. yet still related to the benefits Likert scale. again all four factors were signifi- have been published elsewhere (Fehlbaum cant. The health conditions for which animal-assisted interventions have been successfully applied. Benefits of the Human–Dog Relationship 15 Therapeutic Effects of Animals. especially dogs..g.. in 2008 four factors were significant (see Fig. 2006) ADHD and Conduct Disorder children (Katcher and Wilkins. women.. 2010). Christians also agreed more strongly a cross-cultural comparative study of adult atti. on ‘animal friend’ sample. stray dogs are no Two final statements are of interest to problem’.C. (a) Strongly disagree Disagree pet owner Neither agree no nor disagree yes Agree Strongly agree Buddhism Christianity Hinduism Islam Shintoism Judaism None of these (b) Strongly disagree Disagree sex Neither agree female nor disagee male Agree Strongly agree ‘Random’ ‘Animal friend’ Fig.8% neither fering animals: ‘If an animal is suffering (pain agreeing nor disagreeing. Turner et al. And finally. In India (here the or incurable disease) and cannot be cured. In London. Only religion was Chennai.4% agreed or strongly a significant main effect here.3% being neutral. 46. country (where I am now). England (n = 353). agreed or strongly agreed. suf. n = 827).6% organizations dealing with abandoned.16 D. It would religions (including Buddhists) agreed. it survey was conducted in both Mumbai and should be killed painlessly’. . but appear that stray dog control programmes Christians and Jews agreed significantly more have been relatively successful in London. with 17.1. Agreement with the statement ‘Keeping animals as pets brings many benefits to the person’ a) by religion and b) by sex and sample type. 34. ‘In this in agreement. People of all agreed. Muslims significantly less strongly – but still strongly than the others. 2. with 13. In Chennai. of all three cities were selected and each day sterilized. 2.5 dogs/h were recorded in of walking the streets of Chennai confirm London. pedestrian eye contact with the dogs on the London (England). neuter/spay them. but these are not discussed here) encountered in Chennai. In the previ- 10 min. being a Muslim of street dogs by pedestrians (even at only culture.0 dogs/h were seen in Chennai. Leashed/con- ever an animal was spotted. ‘stray dogs’ in cities of the two countries. 2.g. London. immunize analysis. this. there- fore.2). ‘there has been a com- in the statistical analyses. The first author’s vation were noted in Amman (as opposed to personal observations over nearly a month 11. random encounters with different pedestrians To explain these differences. The Blue Cross of India using earphones (simulating talking on a cell and other organizations (e.). more leashed or (as well as between people and cats and other controlled dogs in London.g.). But we caution that there are proba. the majority of dogs is not under human con- sionally in Chennai driven at 15 km/h which trol and received less attention (eye contact) was factored into the census data).3) revealed a significant city effect and that Chennai dif- In the second phase of the cross-cultural study fered significantly (much less eye contact). described above. According data were adjusted for the number of animals to the president of Blue Cross (Dr Chinny or observations per hour of observation time Krishna. Benefits of the Human–Dog Relationship 17 In cities of India fewer people agree than in dog population in Amman is increasing (M. the sample size for dogs there was too small to interpret. and 14. and Chennai (street) dogs in Chennai. we now concentrate on a comparison Behaviour towards dogs on the street: between Chennai and London. Even though the figures below also show data on dogs in Amman. Behaviour of the persons and animal ous five years. Due to differences in the number of them after marking (e. release them back onto the streets. a historical as long as it remained in view.1. than leashed/controlled dogs. immunized against rabies. The routes were walked (occa. usually about dimension must be mentioned. London. and Chennai (India) streets with post-hoc tests (Fig. 3. Economically comparable areas4 ear. indicating that they had been captured. was pictured in the local press stroking a dog at bly enormous differences in how people define the opening ceremony of the new centre. the first author to offer them a bit of food (see Fig. pers. 2. plete change of human behaviour towards As shown in Table 2. Humane Society phone or listening to music). and later the International) have led very successful cam- same day transcribed onto defined data sheets paigns in various Indian cities to capture before being typed into Excel® files for later street dogs. In London. but a higher proportion of the sample Ledger. or if there was a reaction at all. the situation is the opposite encounters between people and dogs in the in Chennai and London: more free-roaming urban areas of Amman. There was an almost complete ignoring Of course. However. about twice at times of day when one might expect to see as many persons encountering a dog as in more encounters between animals and people Chennai greeted it or the owner. was expected to be more cat friendly 50 cm). 60% had a notched (Fig. also disagrees. 20 m as a ‘focal animal’ for tact than leashed/controlled dogs in London. the street dogs since then’. no cases of rabies have been were recorded on a concealed Dictaphone® reported in Chennai. notably since HRH Queen Rania opinions. comm. and when. Of the street dogs animals. indicating a polarization of pers. Not and observer were surprised to note how a single aggressive interaction was observed friendly and well-kept the cats on the suburban between the dogs. observed from trolled Chennai dogs still received less eye con- a distance of ca. An ANOVA of A comparison between Amman (Jordan). Jordan. but returned to the street. comm. and different routes were selected randomly.5 dogs/h of obser. or between the dogs and streets of Amman were. it was and less dog friendly. on the streets. direct observations with Comparing the level of control over the behavioural data were collected from random dogs encountered. Humane Center for Animal Welfare. the owned people on the streets. and observation days/minutes in the three cities. ear-notching).4). 17. Chennai citizens accept . Amman.3 cats/h). Further. London (b) and Chennai (c). often by professional dog-walkers. in London. 2.18 D. c) One of the many street dogs sighted in Chennai. Fig. b) dogs appeared to be regularly walked. which occasionally also searched for food in refuse bins. probably waiting for a piece of cake from one of the tea-house visitors. Typical scenes during observations in Amman (a).C. . a) One of many well-fed cats sighted in Amman.2. Turner et al. that scientific studies have dem- success story of change for the betterment of onstrated those benefits to the health and human–dog relationships.1. it should be put down humanely. animals. The importance of prevention – through Concluding Remarks sterilization and immunization. .0 (Chennai) and tolerate (and even look after) the dogs shar.2. This is indeed an amazing further.5 (London) India 876 12 126 8. Cats and dogs seen per hour of observation in cities of the three countries.5 (Amman) England 673 20 0 0 196 17. Benefits of the Human–Dog Relationship 19 Fig. No. Table 2. after combining well-being of people in the general public. of Total observation observation Total cats Cats/h Total dogs Dogs/h Country (city) time (min) days observed observed observed observed Jordan 747 10 141 11. ing their streets. and animal welfare organizations. and find dogs to be likeable animals. the efforts of human and veterinary medicine However. all peoples of all religions agreed. Continued. 2.6 205 14.3 44 3. that if an animal is suffering and cannot be cured. which in the case of Chennai took place – can indeed It is important to remember that most people improve both human and animal health and worldwide see benefits in keeping companion relations. 3. The street dogs of Chennai. Turner et al.0% Percentage Country Jordan 40.0% 60. and India (Chennai). are either ignored by pedestrians or offered bits of food.20 D. .0% 0. being spayed/neutered and rabies-free. Fig. 2.0% England India 20.0% No eye contact Eye contact Fig. 80. Percentage of pedestrians having eye contact with the focal dogs in Jordan (Amman).4.C. 2. England (London). C. (eds) Companion Animals in Human Health. Corson. (1985) The neighbourhood walk. Israel. C. Friedmann. and Arnold. Germany.C.. and Turner. A Startling New Understanding of Canine Origin. G. Keith. Switzerland. 298–301. London. K. 4 Abdoun Circle in Amman.L. G. Fehlbaum. A. A. Singapore. West Mambalam. Glasgow UK. W. 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(1984) Biophilia. ity and quantity of available data. 2005). but comparisons with create other problems or nuisances. An approximate assessment of and community well-being only. 2008). UK. they remain popular pets. tial to define the problem in the context of the holds in India (Sudarshan et al. relative importance reflected by differences in Westgarth et al.dekeuster@ugent. Zoonoses and Public Health. Upminster. impact on wildlife and A ‘dog attack’ may mean a dog rushing or the environment.L. 2006) are socio-cultural situation in order to offer effec- reported to own a pet dog. This will influence the qual- three per cent of the households in Sao Paulo. 3 Dog-Associated Problems Affecting Public Health and Community Well-Being Ray L. throughout the world despite variations in the nature of the human–dog interactions.N. Despite the hazards consideration when devising strategies to due to zoonotic diseases and trauma that may address these problems. * Corresponding author. The most for. 2011.. 2nd Edition 24 (eds C. e-mail: tiny. are as much a problem as free. 2008. If the incidence of a result from the association of humans with particular zoonotic disease can be monitored dogs. complete data are from the United Kingdom sion of a variety of zoonotic diseases and and the United States. particu- than zoonotic diseases affecting public health larly tourism. ern countries. and their 28% of owners own two dogs (HSUS. Butcher1 and Tiny De Keuster2* 1 WSPA Consultant. Belgium The chapter will consider problems other and impact on the local economy. Fifty cultural attitudes. is both impractical and undesirable. The benefits of the human–dog relationship sponsible way. reviewed in Chapter 2 must be taken into roaming. A total ban on dog keeping. and 17% of house. and is reflected in all cultures 2007). Dogs. suggested in the medical literature (Besser. Macpherson et al. Faculty of Veterinary Medicine. dogs that are uncontrolled. and not the the financial cost to the community is given adverse effects on the welfare of the dogs where possible. some of the non-disease States. including noise pollution. as bond concept is clearly not restricted to west. dogs can be implicated in the transmis. The human–animal tive solutions. as well as estimates of the themselves. In the United by scientific means. unowned dogs. It is essen- Brazil (Alves et al.be ©CAB International 2013. When uncontrolled and uncared cost of appropriate control schemes. and Bites such as injuries to humans and other ani- mals. PFMA. most owners (60%) own one dog and related problems may be subjective. The Wylie Veterinary Centre.) . 2 Ghent University.. chasing without any physical contact at all. Owned other countries are given where available. In this chapter we review a range of issues Injury to Humans: Trauma other than zoonoses associated with dogs. road accidents. or kept in an irre.. Dog-bite data can be categorized as relating to It is essential to recognize the importance of the victim (race.5 to adults (Horisberger. and avoided going to hospital nature) and the carer (a small child or frail for other bites (Cleaveland et al. and by different methods. In ing from being ‘bitten or struck by a dog’. Each year approximately 4.).000 bites requiring medical attention frequently in young children (Kahn et al. Figures from the UK’s Home appears to influence the reporting of bites. and 39% when the dog recorded as a fall without mention of a dog. of knowledge between professionals and aca- nal status. ularly involving the neck and face. nature and site the source and nature of data and the poten- of injuries. age. was owned by a neighbour (Beck and Jones. the bite was from a suspect rabid dog (hence match between the dog (size or boisterous a higher risk). In veterinary caseloads in EDs (CDC. 2004. 2010. According to data obtained from hospitals and emergency departments Dog bites in people are a serious public (EDs). A survey by Kahn et al. equivalent to 1% of the population (Gisle The degree of risk. (representing 1. the northern part of Tanzania local communi- Accidental injuries from falls can occur with ties appeared to successfully recognize when pet dogs and may sometimes reflect a miss.000 people of bites inflicted by ‘strays’. both of which may significantly affect the results. 100.. UK hospital statistics do injury data to estimate the human rabies mor- not differentiate and report on injuries result.. Kahn et al. and bite report surveys from non-hospital Comparable rates are found in Europe with sources. dren appears to be reversed (Guy et al. health status. place.000 people bitten annually in Belgium. time.000 bites severe enough to be treated Schalamon et al. breed. The exchange (size.. human–animal interaction. how the findings should be inter- data can be obtained from a variety of sources preted. and Leisure Accident Surveillance System There is a disproportionate ‘over-reporting’ (HASS/LASS) show that 69. the relative risk in adults and chil.. Gilchrist et al. Injuries requiring hospital atten. 2008).. etc.. the dog tial bias that may be present. social type. 2006). etc. Dog-bite data: Effect of source Dog-bite data will influence the iden- and method of collection tification of ‘risk factors’ and facilitate the development of new prevention strategies. Severe injuries. gender. People older person). age. In reality. partic. as 50% of people a dog appropriate for the requirements of bitten by dogs without owners sought medi- the family. (2002) used dog bite with the dog’s teeth. consequence. Bias in data on dog and victim characteristics can be observed between different surveys (De Keuster and Incidence of dog bites Butcher. etc. and how the risk factors deduced. Injuries might be avoided by tend to seek medical care and report bites education of potential dog owners to increase more frequently when bitten by an animal awareness and encourage the selection of whose owner is not known. public safety 1985). occur most with 800. million people are bitten in the United States Schalamon et al. or breaking of skin resulting from contact 2000).). 2003). 2001). 2008). 2001). and consequences. tality in the United Republic of Tanzania. 2009). as perceived by the victim. better understand what measurements are to season. gender.. owners are more likely to relinquish attacks with bites (Miller and Howell. cal attention compared to 29% of people bitten tion following a non-bite incident are often by family-owned dogs. (2003) found only 24% of the dogs which had bitten a child were presented to a veterinarian.. It has been suggested that when a child regulations tend to ambiguously classify dog is bitten.5% of the total population). The be made. perhaps because attended hospital Accident and Emergency . and demics of multiple disciplines is required to the context (geographic location. the risk is double in children compared health problem. hormo. 2001). 2003. Cleaveland et al. et al. 2006). limiting data available. and 370. the dog to a shelter than seek veterinary advice (Guy et al. 2002. Dog-Associated Problems 25 while a bite generally results in the bruising they are thought to cause more disease (Beck.).. 9% of hands were more common when the victim inpatient stays were billed to private insur. This may be partly explained by the finding that young children explore novel objects. In Sri unreported injuries or those that do not lead Lanka.200 ED visits involved a dog occur predominantly in the home by a dog bite (equivalent to a rate of 103. while 71. de Keuster departments in 2002 (ROSPA. 10. This does not include the cost of ians. Approximately most often bitten by a familiar dog (Guy et al. in New Zealand (Wake et al. 2003.000 of the population). the total cost for Great Britain would be Some professionals. 2010b).. hospital data indicate a sig- police departments to improve data collec. 2004.. . a number Victim and site of the bite injury of studies estimate that more than 50% of dog bites remain unreported (Beck and Data obtained from hospitals and EDs in Jones.. or breed.200. with their face (Meints et al. (2009) estimated that only ing from dog bites (The Information Centre 20% of bites occur outside the home in public for Health and Social Care. 2010a). Schalamon difficult to quantify. 2006). though the site of injury in adults and (equivalent to a rate of 3. (2004) stress the et al.885. Holmquist and Elixhauser. with 20% requiring medical atten.696.650. 2008). In contrast to the belief that facial need for a collaborated approach between bites in children correlate with the dog’s size.7% were 25 years old corresponding rate for Scotland and Wales. 2001. Injuries to the face and More than 44% of ED visits and 42. the Colombo General Hospital treats to a stay in hospital. veterinary nurses. The places. so the cost to the National vast majority of dogs were free-roaming and Health Service (NHS) in 2008 for England 42.. the average injury-related hospital stay. yet only 5% of cases were reported to young children (Kahn et al.9 visits per that is familiar to the child. 2002.000 bite victims per year (WSPA. Butcher and T. dence of bites on the Navajo reservation. hands (35%).. Schalamon nurse students in New Zealand (Wake et al. A study on adult victims (over 16 years) dog-bite-related hospital stay was $18. especially those that are mobile. However. 2006. and the incidence of bites in India is reported as 1. et al. there were rupt a fight. 2004).. dren are twice at risk compared to adults A survey of 228 veterinary and veterinary (Horisberger. Kahn et al. 1986. hospital EDs. data from The Health Care Cost and Utilization 2005). Daniels.. 2010). neck and face. Schalamon the authorities. 2009) reported a which was approximately 50% higher than bite distribution of legs (45%). Europe and the United States indicate chil- Overall and Love. and very young children may misin- Project (HCUP) on dog-bite-related ED visits terpret a snarling dog for one that is smiling and hospitalizations in the United States.. particularly involving the the past. occur most frequently in tion. Young chil- Costs of bites to health services dren score badly in discriminating dog body language and look mainly at the face of the Holmquist and Elixhauser (2010) present dog to make their decisions (Lakestani et al.. was trying to assist an injured dog or inter- ance. Adults are also 100.40. such as veterinar- £3. 9500 hospital stays resulted from dog bites 2001).352. The average cost of a ties..1% of the victims were children 10 years can be calculated as £3.8% of the population (Sudarshan et al.L. Facial bites in children 2008. Daniels (1986) reported on the inci- average cost of a ‘hospital bed day’ is esti. et al.26 R. local health departments. 2006) indicated that 36% had been bitten in Severe injuries. Assuming a of age or less. 2009/10).. The mated as £317. 2003. In England in 2008/9. The true extent of the problem remains the child’s age (Kahn et al. and arms (22%). 2006). and younger. approximately 12. nificant correlation between facial bites and tion. 1985..1 stays per 100... Gilchrist et al.000 older children is more commonly the extremi- of the population). Kahn et al. and weight. 2010).563 ‘finished consultant bed days’ result. and dog wardens. Chang et al. In (Meints et al. 2006). 1997.. about 316. Tan et al. These must and Research Questionnaire (C-BARQ). obedience training and castration have been Jack Russell Terriers). et al. 2000. 2000).. 2002). Their findings indicate the implausibil- quence of a bite from a dog. the majority of victims trigger factors initiating bites (Herron et al. Cornelissen and Hopster. Cornelissen and Hopster. The education et al. (2010) used a number- of dogs involved in bite incidents were suf. (2008) surveyed heredity. 2007). with some form of breed-specific prohi- et al. have been identified as Unfortunately.. and a simi. triggering media behavioural repertoire.. and dogs.. a result. However. the owners of more than 30 breeds of dog training and education. of the dog must therefore be of good quality Patronek et al. The than average for aggression to both humans importance of domestic breeding environ. 2001. Some breeds (e. dog health status. Chihuahuas and Dachshunds) scored higher 2009. Duffy et al. It is estimated that alters its behaviour. owners. As largely related to the situation and context. whether aggressive behaviour is expressed in ishment and discipline. 2010). Patronek et al. of serious dog bites and fatalities are young 2009). (2007). 66% of least partially rooted in genetics. There be considered in the context of human social were significant differences seen among and cultural factors that have been shown to breeds in aggression directed towards stran- influence human–dog interactions (Barnes gers. Reisner et al. Whilst it has been claimed that breed- related behaviours in dogs are responsible for the majority of bite injuries in children (Shalamon et al. 2009). Bull terriers) for dog-directed aggression.. some breeds (e.g..g. and mented (Appleby et al.. later socialization. and this study also revealed 77% bition. not only because 98% decreasing the risk of dog-bite-related inju- of human deaths from rabies are the conse.. and its expression is exposure focusing on ‘aggressive breeds’. Rabies is limitations of breed-specific legislation in perhaps a special case. Akitas and Pit ments and early socialization are well docu.. 2006. needed-to-ban calculation to illustrate the fering from an emotional disorder. estimate the human rabies mortality in the larly high risk has been highlighted in postal United Republic of Tanzania. breed-specific legislation has been The dog’s response to a perceived threatening introduced into many countries despite the situation may vary according to the ‘ladder of fact its efficacy has been questioned (Sacks aggression’ (Shepherd. 2007. and dogs.. 2001). 2006). paradoxically used the phenotype. Dog-Associated Problems 27 may be at special risk. and using the Canine Behavioural Assessment victim behaviour (AVMA. 1996). other factors the dogs involved in bite incidents had previ. in a propensity to aggressive behaviour is at a large study by Reisner et al. 2001). Ragatz et al. Messam et al. Tasker (2007) reports 11 with a full understanding of dog behaviour. the authors considered useful to reduce the incidence of stress that although the results indicate that bites (Ozanne-Smith et al. there is little evidence Bite and dog-associated factors from dog-bite data to implicate specific breeds as a greater or lesser risk (AVMA. ries. some for human-directed aggression (e. increasing the desire to 5000 postal workers in the United Kingdom bite. The factors that determine a dog’s tendency 2001. out of 22 European countries surveyed had The risk of biting may be increased in the legislation related to dangerous or aggressive presence of pain or disease in the dog (Reisner dogs. Cornelissen and Veterinary Medical Association (AVMA) as Hopster.g. Overall and Love. Aggression is part of the dog’s normal children (Sacks et al. but also because ity of such legislation being successful. 2008. to reduce aggression.. 2009). However. 2009. Cleaveland et al. Kahn et al.. early experience. Historically. to bite have been identified by the American 2003. 2001). 2007).. (such as developmental and environmen- ously attended obedience classes and 93% had tal issues) play a major part in determining been neutered. They the presence of the virus in the dog’s brain consider the enthusiasm for this legislation . (2002) reported on the require medical treatment for dog bites every use of dog-bite injury data to successfully year (Morgan and Palmer. workers in Taiwan (Chen et al.. Inappropriate physical pun. . contributing to the cally refers to behaviour directed at conspecif. 2006. Wake et al. and most reported dog made claims to the Accident Compensation bites in children happened while there was no Corporation in 2002 in New Zealand and active adult supervision (Kahn et al. facts. In the United Kingdom and United (Sudarshan et al. were from free-roaming and uncontrolled without warning or the interaction of the dogs in public places (Thompson. Over 50% of a bias in the population sampled.. 72% reported psy- an unfamiliar dog with no prior interaction chological effects. Cornelissen and Hopster (2009) reported 2006. though this may reflect of the victim acting as a trigger. to help an injured dog or interrupt a fight. (2009) report injuries to face and in relation to injuries to pet dogs. Many such hands were more common in this situation. 1997). guide dog by another dog. and Canada . and 63% of bites were inflicted by ‘strays’ bulls. humans that approach or invade the territory Studies in the United States (Sacks et al. Dog bites reported bite incidents in Adelaide.3% were within the beliefs about efficacy.5% of bite 1996). Bites occurring in public places often is relatively high. especially as they rarely test the temperament in the context of Consequences of bites including a home situation. New Zealand (Healy.L. 1995). 2006). These are associated with significant and Condon. had not received serious injuries. In this study. 2010).. and as dom households in 18 states of India indicated a result of its recommendations. A questionnaire of 8500 ran- efficacy of breed-specific legislation. misin. though this is largely a reflection Bites can occur when a person is trying of socio-economic difficulties within the com. i ncidents were on a street near the dog’s home formation and stereotyping. urban areas where the density of con-specifics 2008).. (2009) reported on a questionnaire sent to dog interaction that triggered the bite was 1800 adults (aged 16 years or more) who had initiated by the child. 2003). 47. This highlights a so-called private home or yard.. attract media attention. (Daniels. While territoriality techni. 1986). Complete data about the circum- in the home environment and involve young stances surrounding an attack on children or children (median 5 years) bitten by a dog that adults in public places are often lacking. dogs end up in shelters and there is often a Out of 100 incidents involving an attack on a desire to assess their suitability for rehoming. 2004). 2008). In 86% of cases the child– et al. it is recommended they should not be used as the sole means of characterizing a dog (Christensen et al. the Dutch a high incidence (75%) in poor or low income Government repealed its 15-year ban on pit areas. LNV. 2007). It is assumed that this Territorial behaviour often precedes incidents may contribute to a feeling of insecurity in the of dog bites and may be especially prevalent in people being attacked (Kahn et al. dogs typically generalize this behaviour to in these situations (LNV. perception of dogs being dangerous or unsafe ics. 2003. 1996). de Keuster is based on misperception of the risk.28 R. Australia. problems.. while 52. in public places usually happen by surprise. Of the 8677 Bites in a public places generally involve claims made in that time. 2010). fatalities A Belgian study investigating the follow-up of children treated in EDs for dog bites found Context and location of dog bites that 55% of severely injured children suffered from post-traumatic stress disorder (Peters The majority of bite accidents in children occur et al.. munity. Butcher and T. Wake is familiar to them. This issue will be discussed further Wake et al. injury inflicted on the handler or member of but few have been scientifically validated and the public (Brooks et al. 2009.. 19% involved an A variety of temperament tests may be of use. victim with the dog. so-called status dogs are increasingly dogs acting as a pack are uncommon (Kneafsey popular. and erroneous or primary shelter. The incidence of bites is perception gap between public fears and the generally higher in rural areas (Sudarshan et al.. Attacks on humans by States. Holmquist and on a study in The Netherlands to evaluate the Elixhauser. promised health status. 2009). confinement. and urban younger. This com. Bite injuries (personal or to Assessment of risk posed by a dog a family member or friend) are very likely to enhance the fear of dogs. 1995). Unaccompanied chil. Although these terms have differ. comm. ICAM with one disputed allegation and impose dra. the perception of dogs having a positive impact on their interactions with dogs and a subsequent improvement in A difficult and emotive aspect of public haz. In 51% of these cases the dog dog bites are rare in the developed world. or euthanasia). Gilchrist et al. and feelings of being Cleaveland et al. The shift of pet animals when threatening or harming a to ‘collect/neuter/return’ and direct involve- human being (Miller and Howell. Free-roaming dogs are captured den of proof is required to substantiate a dog from the street. As a consequence. vaccinated against rabies. achievable through social marketing and col- dren or elderly females appeared especially laborative management rather than via the vulnerable (Kneafsey and Condon. if preceded by a mass rabies vaccination cially if they form into free-roaming packs.6% were 10 years old or concern influences the legislators. Despite the fact that only 20% of pares to 11 fatalities resulting from sporting dog bites occur outside the private home. reducing the fear of dogs. strategies. thirst. Dog-Associated Problems 29 (Raghavan. This Of the victims. ment of the community could be facilitated People may be fearful of dogs. animal welfare (S. dogs in public spaces. and in 31% of The Netherlands approximately one person cases the dog was wandering in the vicinity dies following a dog bite each year. 2008). ard caused by dogs is the fear of dog bites and 2011). of its home. exercise and socialization) and that this is sometimes fatal injuries. espe. This is relevant to the implementa- dog attacks. result in severe. no bur. pers. with the highest incidence in infants safety regulations (such as leash laws in open below 1 year of age. Attacks tives of public safety can best be targeted by on humans by dogs acting as a pack. dogs were Impact of dog bites/trauma on society and perceived as safer by the local community. This may be as a . Requests are often made to assess the risk (2009) estimated only 20% of bites occur in posed by a particular dog. In Australia. Langley (2009) reported on 504 being bitten by a dog in a public place (LNV. Cornelissen and Hopster. tion of dog population control programmes. (2005) reported that fear of dogs and having being bitten in the past were two of the reasons people in Dominica would not keep dogs. group of sled dogs (Delise. and then returned to the street. In was not adequately confined. It present ‘big stick’ legal approach of banning has been suggested that hunger. 2010). 2008). 55. neu- attack.. which may Miller and Howell (2008) suggest the objec- reflect local management practices. deaths in the United States from 1979 to 2005. 2008. 2008). 2008) indicate that fatalities from public places. (2008) stresses the importance of engaging conian physical penalties on the dog (such as with the community in an attempt to encour- muzzling. Alaska had the highest spaces and parks) are based on the assump- death rate. ent meanings. regu. com. 2010). encouraging well-mannered dogs (through larly reported in Indian cities. Cleaveland. In Canada there are a number of tion that these locations are the target areas reports of fatalities following attacks by a for people to be chased or attacked by dogs. programme. Similar age a community responsibility and a subse- rules do not generally exist for other species quent change in human behaviour. Alie et al. Councils can declare a dog dangerous tered. public safety regulations tend ‘Catch/neuter/release’ programmes are a to ambiguously classify dog attacks with bites component of some dog population control (Miller and Howell. that dramatically reduced the incidence of dog and human rabies as well as human dog- bite injuries. the injuries and 23 following household accidents majority of people appear concerned about (LNV. (2003) report on a dog threatened may increase the risk of pack rabies vaccination campaign in rural Africa attacks by ‘strays’ (Santoro et al. They to protect people as far as is reasonably prac. identify the hazards (how individuals may and printed parent guide. Butcher and T. A risk assess. Understanding the context of the bite is essen- ment is a careful examination of the available tial in developing prevention programmes. 2009). potential risk situations that trigger dog identifying individuals or groups who are at bites in everyday household situations (De most risk. 2001. and focuses on be harmed). which informs the advice than 7 years and focus on public safety rules. and severity. It was designed by a team of pro- well-defined situation identifies five stages: fessionals from multiple disciplines to target the main at-risk group (i. record the findings and implement them. the Colombo Municipal Council (CMC) . probability.. review the assessment and update as transforming the prevention-only screenplay necessary.. on Risk Assessment (ESVCE. 2011) which 2010b). (Meints and De Keuster. should it be considered desirable. decide who might be harmed or at risk. kissing).e. To make the programme attractive 5. tres. evaluate the risks and decide on precau- guarding (such as food. Dog-bite prevention programmes legislation and by-laws) or as part of an indi- vidual behavioural consultation. and that parental input enhanced animals. published in the veterinary and medical lit- to determine what measures could or should erature. It is unreasonable to expect all risk to such as how to behave when encountering an be eliminated. but measures should be taken unfamiliar dog (Chapman et al. considering the risks in terms of their interactions (such as petting. as well as dog behavioural features the performance of the child and improved which alter the general risk of recurrence are the ability to retain the acquired knowledge summarized by De Keuster and Jung (2009).g. It takes the form of an interactive CD-ROM 2. However. the Blue Paw Trust Sri Lanka.. Differential diagnoses and text. thus 6. de Keuster result of national statutory requirements (e. It requires consideration of all relevant ognize the dog’s body language. the educational messages are and wrapped in an entertaining context. as well as all relevant environmental ing dog body language and look mainly at triggers that may alter either the risks associ.30 R. and the practice. bones. It is not established in schools and health care cen- an absolute quantification of risk. A scientific assess- The dog-bite related factors to consider ment of the programme showed that children in evaluating the risk following an aggres. into an ‘edutainment’ tool. but a pro.. 2000). Programmes intended to prevent provides a framework as a model of good bite accidents in the home are rare. Meints et al. or nature. The educational message and tools ment. Keuster et al.L. traditionally attempt to teach how to rec- tical. Young children will The European Society for Veterinary Clinical often confuse a frightening with a friendly Ethology has produced a Position Statement dog (Love and Overall. are used must be suitable for the particular con- also discussed. children below 1. These include resource 4. and toys) or tions. evidence relating to potential situations that Data on dog/child interactions have been could cause harm to people or other animals. of the target age group learnt from the Blue sive incident towards familiar people and Dog scenes. 2005). the face of the dog to make their decisions ated with any injury. given. and ‘Prevent a Bite’ programmes reasonably be taken to reduce harm. to children. Blue Dog was developed specifically to fill The risk assessment of a dog in a this gap. 2005). and Bain (2009). Factors influencing the prognosis for treat. or the risk of recurrence. hugging. factors). A collaborative project involving the characteristics of aggression towards unfa. assess the proposed circumstances (risk 7 years of age) in the context of the home. World Society for the Protection of Animals miliar people and animals are considered by (WSPA). physical and behavioural characteristics of young children score badly in discriminat- the dog. (Lakestani et al. teaching parents and children to recognize 3. Most of these are aimed at children older fessional judgment. A dog of the ‘bull pared to human-directed aggression. icant difference in criminal behaviour based representing 1..500 to 21. between 2006 and 2009. Grant. with the dogs they own?’ There is evidence of a correlation between ownership of high-risk dogs (licensed or cited) and the presence of Injury to Pets deviant behaviours in the owner as indicated by court convictions. Allowing for infla- lems highlighted by Marmot (2010). ‘How do you attacks in the United Kingdom in 2009 to be enforce dog laws with a group of individuals valued at £2. Akitas and Pit Bull terriers) may show a of the cases the attacking dog was off the lead propensity for dog-directed aggression com. (2008) has been dis. UK government reported that 8000 animals The Metropolitan Police of London seized were killed or injured by dog attacks. Dog-Associated Problems 31 includes a junior school dog-bite prevention and United Kingdom. Beasley. though Injury to Livestock not exclusively. and highlights an increasing problem of anti- posters (WSPA.E.2 city poverty and wider socio-economic prob- million and £1. 2011). comm. the RSPCA (2010a) estimate the total an implication for the enforcement of legis- cost of injuries to livestock resulting from dog lation. This is breeds type’ was the aggressor in 45. Most cussed above and indicates that some breeds attacks occurred in public places and in 61% (e.3% of first con. (2010) report 100 incidents of London (K. dog attacks on livestock is lacking. and should be an element considered when ity service in an inner-city area of London. compared to 173 in 2006/7 RSPCA and Kennel Club (1998) quote data (Grant. Sadly. pers. During the that impromptu dog-fighting could become period 1993–1996. Those reprimanded have some- sourced from the National Farmers’ Union times been shown to be involved in criminal Mutual Insurance Society which were limited activity.4% of the first consultation on the types of dog owned. This dogs were significantly more likely to admit compares to an incidence of 2. South Africa of the gang.7 million. involves young people on inner-city estates and may involve subjecting the dogs to fights. the total number of sheep more organized and involve gambling. guide dog was working in harness. private veterinary hospital in a suburban area Brooks et al. incidents. 2006). (2009) found a signif- were presented suffering bite wounds in 2010. songs.This has tion. The RSPCA (2010b) programme using puppet shows. to violent behaviour compared to owners of sultations seen during the same period in a other types of dog. and the concern has been expressed to dog attacks on (insured) sheep. In 61% of cases the The survey of Duffy et al. injured each year varied from 13. The (1991) in 2009/10. This often. The killing of chick- who are completely outside the law and who ens by dogs was reported in a household have no respect for any authority except that survey conducted in Soweto. social behaviour where dogs are used in an aggressive or intimidating way towards the public or other animals. 2011). this use of such dogs is a reflection of inner- at an annual cost to the farmer of between £1. and who seem to lack empathy (McCrindle et al. pers. at the time of the attack.7% of the interesting in relation to the increasing popu.8 million. Grant (2011) questions. assessing risk for child endangerment (Barnes Their clinical records indicate that 258 dogs et al. comm.g. but no 1152 dogs under the Dangerous Dogs Act further records were kept after this time. It is suggested that the The extent of attacks by dogs on other dogs is ownership of a high risk (‘vicious’) dog can difficult to ascertain.). In 1978 the compared with 137 in 2006 and 24 in 2004. Owners of vicious caseload (D. Ragatz et al. which was an over-representation larity of status dogs seen in the United States compared with an estimated proportion in . clinical records from of attacks on guide dogs by another dog the Wylie Veterinary Centre.000. 1998).. The RSPCA (Harmsworth be a significant marker for general deviance Memorial) Animal Hospital provides a char. 2008). The RSPCA received 358 Accurate information on the extent and cost of calls specifically about dog-fighting in 2007. as is sometimes suggested as a human casualty were not kept. and 2 of the dogs were subsequently traffic accidents are a major cause of death withdrawn from service. the use of seat belts and child restraints. In 2004. The WHO each guide dog has a lifetime cost of approxi. the UK’s Department of Transport tions. Catch/neuter/release programmes are This is important.100 for a serious Pollution from Faeces.200 for a fatality. There control strategy. (MacDonald. as the presence of the dog is only the attacks. A more complete consideration of the impact of dog popula- Until 2004.L.4 million injuries.9%). a ‘cost’ to the community and straints often mean that bitches are targeted the ecosystem which might influence public in preference to males. £218. Worldwide. It is possible that a opinion and give added pressure to introduce larger number of un-neutered male dogs dog control measures. a steady decline seen over the previous dec- ade. . Ganeshan (2008) valued these accidents according to accepted economic valuation (i. Butcher and T. £1. 1983). continuing have an impact on the ecosystem. The working performance and one of many variables that will affect the behaviour of the victim was affected in 45% severity of the injury and hence the cost. and populations of endemic fauna on the Galapagos Islands (such as giant tortoises. and sor apologized to the victim’s handler in the wearing of helmets for users of motorized only 6% of the cases. as well as causing logistical and and a cost of approximately 3% of the GDP.600 for a slight accident). only 31. and blue-footed boo- Caused by Dogs bies) are seriously threatened by feral dogs (Barnett and Rudd.e. 32 serious accidents. Veterinary However. Removing all the dogs from an casualty. Urine. Feral and semi-feral competing for a relatively smaller number of dogs have been reported to prey on capy- females in oestrus might result in an increase baras (Hydrochoerus hidrochaeris) in Venezuela in dog–dog aggression at these times. Road Traffic Accidents flightless cormorants. including the interbreeding with native recorded the number of road traffic acci- species of Canidae. Horn et al. however. and this may reflect the two-wheelers are recommended. 2009).3% progressed to charges Impact on Wildlife being made and a subsequent prosecution. (RSPCA and Kennel Club. giving an overall esti. and Tearing accident. It is estimated that and injury throughout the world. marine iguanas. It was Open Garbage further assumed that if the data were to apply to 2008/9.32 R. one control measure. It was reported that the owner of the aggres. (2010) further note that only 16% of the tries (WHO. the resultant cost underestimates The fouling of public parks and open spaces would be balanced by the continuing decline is one of the major grievances among the non- in numbers of accidents. psychological difficulties for the blind person. Brooks the problem is worse in lower-income coun- et al. de Keuster the national population (5.6 million.906. 1998).000. 2. £22. 1981). so any injuries that affect the for Europe (2009) reports an annual total of dog’s ability to work have a big potential 120. Stricter controls on drink driving. cost impact. dog-owning population against dog owners mated cost for 2008 in Britain of £14. (World Health Organization) Regional Office mately £50. status dog culture discussed above. attacks were reported to the police and 2% to the local dog warden. such figures are difficult to attention was required following 41% of interpret. and 254 being available to other species which may slight accidents were reported. Financial or logistical con- is. speeding. is given in Matter and dents caused by dogs involving a human Daniels (2000). though may not necessarily sometimes a component of a dog population be considered as a public health issue.000 human deaths. Of those reported to the police. Road of cases. Records of accidents without a environment. will result in food resources human fatality. notably in France. (2005) cited noise as the success of the ‘poop-scoop’ legislation one of the reasons that would discourage was dependent on the fact that it stimulated a people from keeping dogs in Dominica. ral resource for free-roaming dogs. empower local authorities to initiate ‘poop. be due to outside stimuli. and (Horwitz.. in specific areas such as markets or chil- tory of New York’s ‘Poop scoop’ legislation. access to the streets. tural activities.).. formed by dogs that is welcomed (WHO/ ment made it a success. As well as the zoonotic in higher-income neighbourhoods. territorial displays. cited tear- dogs produce 16 tonnes of faeces per day ing open rubbish as one of the dog-related (Brandow. 150. Brandow (2008) Impact of Noise also reviews the alternative approaches that have been tried. If not corrected this can Environment Act (2005) make provisions that put a strain on the human–animal bond. It is also one of a range of were phased out in 2005.. South Africa. ticians thought the idea absurd. low-to-middle-income produced could have a significant impact on areas. straying pets are more common in that the large volume of dog faeces and urine high human density. 2008). 1973). 1998). especially where people have direct the pollution of waterways due to the associ. Improved garbage con- as one reason given for people not keeping trol is a solution and is generally achieved dogs in The Bahamas. Ownerless strays are ated excess nitrogen (Watson. with parasite eggs (mainly Toxocara spp. of the pet’s owner. modification in the behaviour of dog owners and noise was considered to be a nuisance . relating to most successful and was copied in many factors such as fear. Initially many poli. separation-related behaviour problems that settes’) have been installed in a number of cit. 2009). or play proved to be expensive and ineffective. other cities throughout the world. such as around parks. As a gen- and aesthetic problems. 1990). for animal control. but these with other dogs. or abandoned parts of the inner city The problem of faecal pollution became (Beck. Specially Vocalization in dogs is common and may designed motor cycles with vacuum clean. (2005) cited the mess produced by dogs can be maintained. social facilitation ers (‘moto-crottes’) were introduced. and is cited as one of the higher-risk factors scoop’ programmes and on-the-spot penalties for relinquishing dogs to shelters (Patronek for violators. WSPA. Alie part explains why high population densities et al. 2009). These problems can have the ‘poop-scoop’ approach proved to be the different underlying motivations. it has been suggested eral rule. Alie et al. Dog-Associated Problems 33 (1990) reported more than 60% of children’s and an acceptance by society that this serious playgrounds in Hanover were contaminated issue could be addressed in this way. and United Kingdom. Food mixed in garbage is a natu- household survey conducted in Soweto.000 conducted in Soweto. eating of refuse (and human faeces) may be lic opinion that were overcome before the regarded as a positive cleaning function per- law was enacted and subsequent enforce. Brandow (2008) suggests that et al. dren’s play areas. anxiety. In the event. Respondents to a household survey It has been reported that in Paris. In the and lack of appropriate stimulation. 2002). Brandow (2008) traces the his. may occur in the partial or complete absence ies in France with minimal effect. over-attachment. Faecal contamination was problems in their community (McCrindle one of the problem areas highlighted in a et al. and animal rights activists were unanimously opposed on the grounds that it would impose undue hardship on dog owners. the Dog (Fouling of Land) require different treatment interventions Act in 1996 and Clean Neighbourhoods and (Horwitz. dumps. and in South Africa (McCrindle et al. In some communities the highlighting the significant barriers in pub. Sand boxes (‘cani. though more common in low-density. 1996). Targeted garbage control may a major political issue in many major cities be useful to discourage free-roaming dogs in the 1970s. 1998). low-income the relative effect may be small compared to areas where there is shelter and few requests human sewage and the run-off from agricul. at changing people’s behaviour. a statutory nuisance is regarded as a ‘material interference with the comfort and enjoyment of another’s home’. 2005). izations). United Kingdom (2010) be addressed. Local Council. and many of the municipalities have adopted Impact on Local Economy ‘leash laws’ prohibiting the loose running of owned dogs in public areas. Dominica.C. 1998). Fielding and Plumridge national dog registration scheme but this is (2005) note that tourists may be upset by see. and sustainable. de Keuster reported in a survey carried out in Soweto. In Slovenia and The dog’s function is therefore to bark. This accounting for approximately 30% of cases. Protection Act (1990). Many municipalities and education. 2008). registration and identification.. at least in part. barking dogs are the most numerous. containable. Canada. in the 1970s was sufficient to alarm politicians South Africa (McCrindle et al. The Slovenian situation is described as well controlled. The ICAM (2008) Columbia. 2010).L. with low numbers of stray dogs. to do if exposed to excessive barking. 2011). and registration scheme. are consistent with the findings of Turner and Brandow (2008) suggests that the level of Waiblinger discussed above (D. ship is high. ing responsible pet ownership both at the plaints. and The Netherlands dog control provisions have so the resulting noise may contribute to the improved. Switzerland also has an efficient and violence – all of which is detrimental to a system with good compliance. legislation. It is reported ing ‘potcakes’ (local mongrel dogs) roaming that the standard of responsible dog owner- the street on New Providence. requires education that results in a change The local authority of Okanagan Lake. control of total complaints about dogs) (Wanganui of breeders and sales outlets. Some are referred to as ‘watch dogs’ Within mainland Europe. implemented at the local level. comm. drugs. .. (Okanagan Lake British Humane Dog Population Management Columbia Local Authority. pers.. components of the strategy should be aimed are used for security purposes (Alie et al. the control of noise other cities. effective ones for the particular situation. All Many dogs (65%) in Roseau. Complaints about dog General Cost of Control Schemes barking are dealt with by the environmen- tal health department of the local council.34 R. Tasker (2007) and these are generally encouraged to bark has identified 23 countries with a dog licence as a warning. compliance rates of more than 50% (Upton et al. individual and at the community level. In Germany there is a a tourist industry. (representing 18% of total complaints about The components of the strategy may include dogs). providing financial savings for local that the presence of free-roaming dogs may authorities and NGOs (non-government organ- project an image of inner-city decay. reported 403 cases in 2007/8 (representing 15% control of reproduction by neutering. while that of Wanganui. by promot- reported that of all neighbourhood noise com. Many of the problems discussed above can St Helens Council. These findings tourist-based economy. of the possibility of businesses relocating to In the United Kingdom. An overall strategy would have websites giving information about what include more than one of these components. Butcher and T. British in the behaviour of people. but not to attack an intruder. New Zealand. thus having a significant poten- pollution is governed by the Environmental tial economic impact. and so though it should prioritize the most cost- this is clearly a widespread problem. 2010) reports 417 Guidance stresses the need to tailor the dog complaints relating to barking dogs in 2010 control strategy to the specific local situation. According to case law. The Bahamas. with shelters working at under- Ross and Mirowsky (1999) further suggest capacity. Waiblinger. and nuisance perceived by others. Compliance is The presence of free-roaming dogs may have improved by the favourable attitudes of the a negative impact in countries dependent on general population. garbage control. Turner and dog faecal pollution experienced in New York E. Dog-Associated Problems 35 Pescara is said to have one of the most and ICAM (2008) stresses the need to take successful registration and identification account of the opinions of all stakeholders. schemes in Italy, with a compliance of 70% In 2008, a pilot rabies control project was as compared to 30% for the rest of the coun- initiated in the Visayas archipelago in the try. This has resulted in a reduction in strays Philippines, focusing on eliminating rabies from about 5000 dogs in 2004 to 2300 in 2008, from the reservoir species (the dog) using as well as an improvement in responsible humane methods. This was based on the pet ownership. It is reported that there has Philippines’ National Rabies Prevention and been a reduction in uncontrolled reproduc- Control Program (NRPCP), which included tion, a reduced risk to humans of zoonoses, the provision for compulsory dog registra- a reduced level of environmental contamina- tion according to the Anti-Rabies Act (2007). tion, and an improved control of activities Overall, the preliminary results of the pro- such as dog-fighting (Upton et al., 2010). gramme are very encouraging. However, Compulsory identification and registra- though the introduction of registration is to tion has been in place in Victoria, Australia, be applauded, the fees and penalties imposed since 1970. Compliance is reported to be about were viewed by some to be high relative to the 64%, though this varies between urban and local economy, such that it could potentially rural areas. Reported benefits include a reduc- reduce compliance and encourage abandon- tion in the number of free-roaming dogs, ment. This could be counterproductive to the reduced environmental contamination, a medium-term aim of encouraging responsible decreased risk of zoonoses, and an improved pet ownership, and highlights the importance control of activities such as dog-fighting of ensuring that all the fine details of any plan (McMurray, 2005). The improved level of are appropriate to the local situation. responsible pet ownership has also resulted in Registration and identification are two of a decrease in the number of complaints about the key components to promote responsible dogs: 10% of the pet population is involved pet ownership. Despite this, mandatory dog in animal complaints, compared to 20% prior licensing was abolished in Britain in 1987, to introduction of the legislation. There is evi- and microchip identification is currently dence that a pilot scheme to achieve humane voluntary. The funding of rehoming and and sustainable dog population control in educational initiatives is largely the responsi- Colombo, Sri Lanka (WSPA, 2010), is achiev- bility of charities and NGOs. In addition, the ing a significant reduction in the number RSPCA is responsible for 80% of the prosecu- of dog-related complaints received by the tions under the Animal Welfare Act (2006), Colombo Municipal Council (CMC). and they estimate the total costs associated Alie et al. (2005) report that dog licens- with these activities to be in excess of £50 mil- ing is in place in Roseau, Dominica, but there lion in 2009 (RSPCA, 2009a). Local authori- is poor compliance. This is thought to be in ties are obliged to keep stray dogs for 7 days, part due to widespread ignorance of the law, after which many are passed to charities for stressing the need to implement public educa- rehoming. Approximately 42–46% of stray tion programmes. Interestingly, their survey dogs collected were returned to their owners showed that respondents from households (RSPCA, 2009b; Dogs Trust, 2009). The aver- without dogs thought that the registration fee age length of stay in kennels run by the major should be approximately four times higher UK charities is 30.5 days at an average cost of than those from dog-keeping households. £7.54 per day (RSPCA, 2010a). It is suggested This may reflect a desire to make it difficult that mandatory registration and identification for people to keep dogs, or perhaps the feel- would speed up the rehoming, with annual ing of non-dog carers that dogs are a nuisance savings in kennel costs estimated between and their carers should be penalized. The £2.8 million and £7.5 million. In addition, the lower fee suggested by the dog carers prob- resulting increase in kennel capacity would ably reflects their opinion that they should be further reduce the requirement for euthana- free to exercise their ‘right’ to keep a dog. In sia of healthy dogs. There are an estimated reality a compromise often has to be reached, 10,500 registered animal NGOs within the 36 R.L. Butcher and T. de Keuster United States, with a total annual expenditure and the aim was to educate them to become of US$1,902,380,623 (A. Rowan, pers. comm. more ‘active’ through increased interaction 2010). In addition, the Municipal Animal with their pets, benefiting both pet and carer, Control entities have an estimated budget reducing the presence of dogs on the street, of $1,068,225,000, leading to a total annual and thereby the problems caused. A collabo- expenditure on animal protection and animal rative project to achieve humane and sustain- control of approximately $2,970,605,623. able dog population control in Colombo, Sri The local authorities within the United Lanka, has a broad spectrum of activities that Kingdom fund dog wardens who have a includes education in dog-bite prevention. By statutory responsibility to ensure compli- 2010, significant progress had been achieved ance with local dog control orders, as well as (WSPA, 2010), reaching 54,582 primary dealing with stray dogs, dangerous dogs, and school children, 19,836 secondary-school chil- complaints from the public. There is consid- dren, and 4171 members of the community. erable variation between councils (especially Puppet shows have been used successfully between rural and urban areas), and the aver- in low-income government primary schools. age recorded cost of a dog warden service is Pre- and post-education evaluation (of five £112,715 (Upton et al., 2010). Given that there key bite messages) indicated students learnt are 408 local councils, the total cost to the the message following the initial lesson and United Kingdom is estimated to be approxi- that there was significant knowledge reten- mately £46 million. The RSPCA (2010a) has tion after 6 months. The community educa- calculated the total cost of running a prop- tion programmes involved the use of street erly funded registration scheme in the United drama and DVD lectures. These were found Kingdom to be a minimum of £107 million. to be more effective in the evenings, as this Assuming 75% compliance and a total popu- was when more people attended and there lation of 10 million dogs (Murray et al., 2010), was a better spread of age and gender. There this would equate to an annual dog licensing is anecdotal evidence of a reduction in the fee of £14.30 per dog; at 50% compliance the number of dog bites in children, and a full cost would increase to £21.50 per dog. analysis of the data is in progress. A report in the Cape Town News (2009) Research has shown that a reduction in indicated that 400 complaints were logged the incidence of in-home injuries in young daily by the police department, of which 100 children is not related to their knowledge of relate to dogs (70% of these relate to barking home safety rules, but rather to their compli- and making a nuisance). It was calculated that ance and to the extent of parental supervision dealing with dog complaints cost R50,000 per (Morrongiello et al., 2001). Similar findings month, which represented a large drain on were found in relation to the prevention of resources and manpower. road traffic accidents in children (Zeedyk et al., 2001). Physical proximity was the only aspect of parental supervision behaviour that served a protective function (Morrongiello Education is the Key and House, 2004). The development of the Blue Dog programme incorporated these les- Alie et al. (2005) report on a preliminary survey sons (De Keuster et al., 2005), but has also high- of 300 households carried out by Roseau City lighted other important issues (De Keuster Council, Dominica, in collaboration with the and Butcher, 2011). Difficulties have been International fund for Animal Welfare (IFAW). experienced in promoting dog-bite preven- They found that 90% of respondents agreed tion messages. The strategy initially involved there was a roaming dog problem and that a ‘fear’ message (every dog has the potential education was the key. However, this posed a to bite). An important pitfall is to assume that difficulty, as relatively few dog carers visited health prevention campaigns will necessar- the veterinarian, so novel ways of reaching ily induce a danger-control process, which in the average carer needed to be developed. turn will cause a change in behaviour (Witte, Carers were described generally as ‘passive’ 1993). Messages designed to scare people by Dog-Associated Problems 37 describing the terrible things that will happen cities is essential (Grant, 2011). It is important to them if they do not do what the message that the human–dog bond is taken into con- recommends may induce a fear response with sideration when planning towns and cities. subsequent message rejection. This requires Urban animal management rules need to be careful consideration of how to balance a devised that protect people from the perceived ‘fear’ message with a ‘feel-good’ one. dangers of dogs while allowing dog owners to enjoy the benefits (Miller and Howell, 2008). Problems within the home environment cannot easily be addressed by legislation. Conclusions Barking in pet dogs as a result of separa- tion anxiety requires veterinary or specialist Many studies have shown the human–dog behavioural advice. Bites to children in this bond has a positive impact on human health, context can generally be regarded as ‘acci- child development, and the quality of life. dents in the home’ that can only be reduced However, there are problems, and the chal- by parents providing a safe home environ- lenge is to devise strategies that allow us to ment with adequate child supervision. This live safely with dogs so we can retain the requires an understanding of child behaviour benefits yet reduce the risks. It is recognized as well as dog behaviour. that the complexities and contradictions of Effective strategic decisions on prevention human–dog interactions result in tensions require the correct interpretation of good data. (Leney and Remfry, 2000). These result in real Consideration of the available dog-bite data issues, but there are also real solutions, and highlights the importance of recognizing the controlling the conflicts between the owner’s source and nature of data and the potential bias expectations and the dog’s nature is one of that may be present. It is essential to exchange the important challenges in public health and knowledge between the various professions animal welfare (Beck, 2000). involved (e.g. veterinarians, physicians, police- Reducing the nuisance of free-roaming or men, dog catchers, etc.) and academics, in uncontrolled dogs in public places requires a order to better understand what we are trying comprehensive dog population management to measure, how we should interpret the find- programme that takes account of all stake- ings, and how we recognize the risk factors. holders. The considerable costs involved must Education remains the key. It is impor- be balanced against the economic savings tant to agree the correct message, identify achieved in specific areas and the improve- the target population, and decide on the best ments in community well-being. Legislation group(s) to present the message. The educa- (including registration and identification) has tional tools selected must be appropriate for an important role to play, but will be most the culture, age, and abilities of those to be effective if the provisions and penalties reflect educated. The message must be presented in what the local community consider right and a balanced way. Witte et al. (2001) stress that proper. These measures should be regarded as effective health-risk messages need to stimu- an opportunity for public education, as it is late a cognitive response in the target audience only by changing people’s behaviour that the in order to modify their behaviour, yet avoid a problems will be resolved. In this regard, the fear response that leads to message rejection. New Zealand Animal Welfare Act (1999) and The perception gap between public fears and the UK’s Animal Welfare Act (2006) are good the facts may lead to misperception of the risk, examples as they introduce the concept of a misinformation, and stereotyping, and errone- ‘duty of care’ with the provision to incorporate ous beliefs about efficacy of proposed control accepted codes of practice (Animal Welfare measures (Patronek et al., 2010). Finally, it is (Dogs) Codes of Welfare, 2010). Issues related essential to monitor the efficacy of the educa- to status dogs may be more problematic as tion programme – not simply whether people those responsible may act outside the law and learn and retain knowledge, but that their have little respect for authority. Tackling the behaviour is modified in an appropriate way underlying socio-economic problems of inner that achieves measurable benefits. 38 R.L. Butcher and T. de Keuster References Alie, K., Davis, B.W., Fielding, W.J. and Maldonado, F.G. 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Carcary.int/violence_injury_prevention/road_safety_ status/2009.L. L. B. (1993) Message and conceptual confounds in fear appeals: the role of threat. wild carnivores. Switzerland Rabies is a one of a variety of zoonoses in a rabies in its principal host populations. species of Carnivora. Wandeler. including the domestic though this is rarely enforced. 2005). rabies maintained by cination and by reducing the risk of exposure. nized since antiquity as a disease entity with Although most mammalian species are characteristic clinical and epidemiological fea. susceptible to infection with rabies viruses. identified as hosts of lyssaviruses in Africa. neurological disorders that promote transmis- sis. its ranking among all human a few are recognized as important for the per- health concerns is difficult. the Americas.and post-exposure prophylactic vac. 2CSIRO Australian 1 Animal Health Laboratory (AAHL). or conclusively. tute the genus Lyssavirus (Tordo et al. The most cost-effective way to reduce the incidence of human infection is by The Rabies Virus prophylactic immunization of those domestic animals which are the most common source of Rabies virus and related viruses consti- human exposure. species. Australia. is possible because of sets of coadapted traits adjusted life year (DALY) estimates give it a of susceptibility. viral evasion of immune sur- fair position (Knobel et al. sion.7 mil. are the principal hosts for classical rabies programmes aim at protecting human health (serotype/genotype 1) in Africa.. particularly in bats. Macpherson et al. and many countries the Americas. only tures. and preventing economic losses. However. which number of mammalian hosts. It has been recog. 2nd Edition (eds C. Australia. In these princi- its ranking among other neglected tropical pal host species. long incubation. Geneva. guish between bat rabies. and Eurasia. Zoonoses and Public Health. veillance. lion DALYs rabies comes close to leishmania. such as the dog. Canada.L. Dogs. e-mail: alexwandeler@rogers. excretion in saliva. in front of trypanosomiasis and leprosy. It is a con.com ©CAB International 2013. by disease elimination in the host species.. It is a reportable dis. siderably more ambitious task to eliminate Lyssaviruses are members of the family * Corresponding author. and dog rabies. Ottawa. but far behind soil-transmitted helminthiases and population biology. From a practical human health rence of rabies in humans can be controlled and disease control standpoint one may distin- by pre. The occur. social behaviour. Rabies control dog. Recent efforts of sistence of the disease in nature. With 1.) 43 . 2005). each caused by may be impossible to date in many wildlife a distinct Lyssavirus variant. and Eurasia.1* John Bingham. Chiroptera (bats) are and lymphatic filariasis. ease in many countries.2 and François-Xavier Meslin3 Canadian Food Inspection Agency. host life history traits.N. a prolonged enzootic existence diseases including zoonoses using disability. 4 Dogs and Rabies Alexander I. Geelong. 3 WHO. Different also provide legislation for controlling it. 000 nucleotides in length.to a million-fold higher than bodies. detergents and organic solvents. virus) are confined to Africa. P (formerly M1 or NS). One of these binding sites is the 1 is the ‘classical rabies’ type. The virion envelope organs is lost within a few days in summer. This signifies in practical terms that of approximately 75 nm in diameter and 100– most of the virus on the exposed surface of 300 nm in length.. 1996). while the other synthesized viral proteins encap. 1991). the G-protein forming spikes that cover the surface. while (RNP) complexes are released into the cyto. They are often described as a dead animal is inactivated within a few bullet-shaped. Bound virions are internalized into 5 and 6 (European bat lyssaviruses 1 and 2) endosomes. which includes nicotinic acetylcholine receptor (Baer and dog rabies variants. is composed of membrane (matrix) protein but can persist for many weeks under cool (M) and glycoprotein (G-protein) molecules.I. Genotypes terized. Antigenic and Genetic Variation sidate the RNA progeny to form RNP. Physical Properties Rabies Virus Structure Rabies viruses are quite fragile. replication mechanisms (Tordo et al. RNP strands are coiled into dense that of DNA genomes. and L-protein molecules. M (for. which currently contains seven species (genotypes). UV negative strand RNA molecule of approxi. All lyssavirus isolates have Virus Replication been isolated from mammals. for protein synthesis (Tordo and Kouznetzoff. 3 (Mokola virus). ABLV) plasm. The destructive influence for the five rabies virus structural proteins of physical and chemical agents is greatly designated N. 2003. types currently consist of single isolates from genome’ for replication and messenger RNAs Eurasian and African bats (Botvinkin et al. but they are not yet well charac. and L (Tordo. All rhabdoviruses share ons budding from cellular membranes fitted a common morphology.44 A. and by mately 12. Inside the virion is a dense helical ribonucleocapsid cylinder consisting of the Other Lyssaviruses viral genome RNA covered with N. Wandeler et al. and that the infectivity in internal or less flat at the other. Genotypes 2 (Lagos bat Lentz. 2005). Kuzmin et al. The large L-protein The lyssaviruses are a distinct genus within the functions as virion-associated polymerase. Rhabdoviridae (Greek rhabdos = rod) and of the helices before they are incorporated into viri- order Mononegavirales. rounded at one end. light. P. The newly made G-proteins are incor- porated into the host cell membrane. RNP accumulates in inclusion bodies. viruses are enveloped short cylindrical rods 1976).. which are The mutation rate of RNA virus genomes visible in histological preparations as Negri is a thousand. Viruses of all genotypes cause rabies- with the assistance of specific regions of the like clinical disease in mammals. Further proposed geno- RNA is transcribed into positive-strand ‘anti. with a further five proposed types. This is due largely to . They are read- The rabies virus genome is an unsegmented ily inactivated by elevated temperatures. 2010). Other receptors may also be virus). modified by stabilizing effects of polypep- merly M2). 2003.. and with G-protein spikes. genotype 7 (Australian bat lyssavirus. G.. and more hours. with most viral types being maintained by various species of Rabies virions bind to cell surface receptors bats. Rhabdovirus family. The genomic negative-strand rabies occurs in Australia. coding extreme pH values. Genotype G-protein. weather conditions. genome structure. 1993). Rabies tides and other compounds (Michalski et al. from where the ribonucleoprotein are restricted to Europe (Eurosiberia). and 4 (Duvenhage important. a species that is suscepti- expect that it should switch principal hosts ble. future invasions of new et al. dom variability. This is obviously not the ical attributes for continuous transmission of case. particularly when is most likely the result of the introduction of examining individual infected hosts. though caused by identi- too many simultaneous co-adapted changes. lysed with monoclonal antibodies (Wandeler. REA (restriction enzyme analysis). It is quite striking that polymorphism than phenotypic analysis with isolates made from rabid dogs from Africa. Only rarely are dogs infected genetic variation. All these itself along fitness gradients to fitness peaks. monoclonal antibodies (Mabs). The quasispecies con. it should be noted the virus. 1993). 2009). 1998) as well as in host populations Smith et al. et al. The situation is at local fitness optima. There are the Americas. Bingham Though intricate. Neither European dogs and their viruses in colonial . 1994. nant dog rabies are all very similar when ana- Despite the obvious constraints on ran. cept highlights the evolutionary potential of and raccoons.. one would persistence. to dogs. that the predictions from a mathematical model describing populations of self-replicating RNA molecules characterized by a high rate of erroneous copying are only partially Virus variants occurring in dogs fulfilled. nor the application of are estimated to be 10−4 to 4 × 10−4 per base Mabs for a phenotypic examination will incorporated. 2004). (1992) have analysed the genetic (Nadin-Davis et al. A polynucleotide can guide with American bat rabies variants. This suggests that substantial selective variants circulating in populations of wild pressures do operate. Asia. Such heterogeneities have straints in their adaptation to the species. adustus) appear tural and functional constraints. Dogs and Rabies 45 the absence of intrinsic proofreading mecha. The authors structure. or may need to be independent. Molecular genome relatedness of rabies virus isolates using analysis is necessarily more apt to uncover N-gene sequence data. Despite the obvious potential for random viral mutation. both indicating the European fox rabies virus and isolates functional constraints on the phenotypic from wild Carnivora in Africa. molecular analysis of a PCR product with nisms in RNA replication. This may indicate functional con- polymorphism. but does not have the appropriate biolog- opportunistically.. concluded that the similarity of many dog The viral polymorphism poses some rabies virus variants from around the world diagnostic challenges. in the worst. Carnivora. and Europe are all geneti- essentially two reasons for this: more mutants cally related and form the so-called ‘cosmo- are synonymous than non-synonymous. hosts do permit some viral 1991a). but been described in individual hosts (Morimoto more likely it is reflecting a common ancestry. 1999. Zulu et al. necessarily detect viral heterogeneity. Such a level of base change dic. rabies genomes appear to be trapped this virus in its populations. The expression ‘quasispecies’ variants present. they let a mix- is frequently applied to such polymorphic ture of variants appear as a new version of populations. This lineage also includes are not detected by Mabs.. hosts are possible at a similar frequency as Virus variants from areas with predomi- they have occurred in the past.. als (Canis mesomelas and C. striped skunks. hosts or the adoption of other transmission where rabies epizootics in dogs and in jack- strategies may both be difficult due to struc. overall high levels In Europe and North America dogs are of conservation are found in wild rabies iso. Average frequen. cal virus variants (King et al. nor con- cies of base substitutions in rhabdoviruses sensus sequencing. and politan lineage’ (see also Nadin-Davis and a fair number of non-synonymous mutants Bingham. such as red foxes. In the tates that RNA viruses exist as heterogeneous best case these methods detect one of several populations. Adaptations to new rather more complicated in Southern Africa.. frequently infected with the rabies virus lates. However. cases are considered spillover from a host that If ‘self-guided tours’ in the fitness landscape permits a particular virus variant to enzootic were a possibility for rabies virus. 1973. inhalation. (2009) about one million times more than required found the incubation to be mainly between 20 for foxes.. . Usually. dogs were found to be highly susceptible to a if not prehistoric. 2000. but the majority of incubation fox virus in experiments conducted by periods observed after experimental inocula- Blancou (1985). The basis for species It has been suggested that infection may differences in susceptibility and how suscep- result from mouth-licking and through con. jackal isolate. viruses and found significant mortality with sodes of anthropogenic spread of rabies with doses as low as 1.46 A. It should be kept in mind that epi. but they resisted the injection of et al. virus excretion with saliva had cleared the infection (McColl et al. refractory to rabies virus infection under experimental conditions. being et al. 1988a). times. Tignor et Pathogenesis al. practices in many social canids. Hampson et al. 2004). but incubation period. only subject to the host in question. 1996. there are marked differences in susceptibility to intra- Transmission muscular injection as demonstrated by Sikes (1962). nerve fibres rather than by blood and lymph.. In another study dogs could also have occurred at pre-colonial. periods. immune dogs with Ethiopian and Mexican street rabies status.7 MicLD50. 1988).. Foggin. and other mucosal dependent on properties of the infecting virus exposure) has been occasionally implicated. but these often- higher doses and became immune (Blancou cited relationships are not entirely clear. where 1 MicLD50 caused infec- tion (Bingham. 1991b). tibility is linked to specific properties of virus sumption of regurgitated food. 1973. and No mammal studied so far is completely the almost invariably fatal outcome. variant (Blancou. origin of virus. Incubation 50% of the animals inoculated) for dogs inoc. periods in dogs observed after natural expo- ulated intramuscularly was between 105 and sure in Zimbabwe are mostly between 2 and 106 mouse intracerebral LD50 (MicLD50). Fekadu et al. and other factors. Blancou Rabies virus is normally transmitted from dog (1988a). 1999).. Incubation Susceptibility The time between exposure and first appear- ance of clinical signs of disease may range from Dogs were not very susceptible to a European days to years... 1982. 1983). foxes were susceptible and 25 days. Such forms of (1990) speculated that the abundance of nico- transmission may have occurred in outbreaks tinic acetylcholine receptors at the entry port which have decimated packs of African would explain the contrast in susceptibility. Dogs are also suscepti- ble to Mokola virus and to experimental Lagos bat virus infection (Percy et al. but generally long dogs had had CNS infection with ABLV. The LD50 (dose required to kill tion are between 3 and 6 weeks. 2007). toward the end of the incubation period. this is 5 weeks (Foggin.. Wandeler et al.I. However. antibody in cerebrospinal fluid (CSF) in some the rapid expansion of the infection within of the dogs supported the notion that these the CNS after a variable. painted dogs (Lycaon pictus) (Kat et al. but also sion (ingestion. Hofmeyr et al. The outcome of an exposure is not animal via bite wounds. Dogs challenged with ABLV showed intermittent mild neurological Rabies has a peculiar pathogenesis that is signs but recovered fully by 90 days with sero- characterized by virus dissemination within conversion and no evidence of residual virus. though Baer et al. In contrast. both common variants is not understood. Non-bite transmis. (1982) inoculated complicated by site of viral entry. Steck and Wandeler (1980). Fekadu. and to dog with virus-laden saliva of the diseased others. Parker and Wilsnack (1966). 1983). greater viral input leads to low doses of a canine rabies virus from to a shortened course and vice versa (Fekadu North Africa. There is also some virus that clinically normal dogs and cats having budding into the intercellular space. the elimination of the virus before it enters The extent of inflammatory lesions appears the nervous system. Rabies virus antigen can then of rabies virus (Wiktor et al. Viral bitten a person be observed for 10 days. The virus concentration in peripheral spinal cord having direct neural connec.1987. zation very shortly after exposure mediates and moderate inflammation of meninges. slight neuronophagia and gliosis. and pancreas. Hill and Beran. 1984. organs can be high. 1977).. The transmission of sil infection and virus excretion by asympto- virus from one neuron to another is probably matic ‘carrier state’ animals is discussed by mostly by budding on postsynaptic or adja. rons.. be detected in most organs (Charlton and sibly immunodepressive properties of saliva Casey. 1991). The dissemination within the CNS is due mainly recommendation is based on two observations: . However. It is not altogether clear if that is of rabies virus antigen in the CNS are well an obligatory step before it gains access to the described (Charlton. to retrograde and anterograde axonal trans- lication can be detected in myocytes or in port. and pos. 1983.. 1993). 1992). 1968). RNP or virions to the CNS in more visible in certain (large) cells. nal functions. 1991). 1982). Again. or with a and Excretion virus variant adapted to a different species (Blancou et al. There is extensive infection of peripheral Several factors may contribute to this phe.. 1988. It depends on the site of inoculation and on The transport of rabies virus in the form of the infecting virus variant. Dogs and Rabies 47 At the entry (inoculation) site. are usually by retrograde axoplasmic flow (Tsiang et al. 1988. However. Lesions. In the CNS more than 106 MicLD50 per g of tissue (Fekadu the virus replicates in the perikarya of neu. virus rep. immunosuppressive effects inside axons. Perl and Good. A possible role of ton- infected (Iwasaki. followed by endocy. (Tsiang and Lagrange. 1979). the virus moves passively cells and nerves. (1983). The WHO (World Health Organization) tosis on or near synaptic junctions (Charlton Expert Committee on Rabies recommends and Casey. 1991b). cent plasma membranes.. other cell types are only sporadically Fekadu. nervous system or if direct entry into periph. Combined active and passive immuni. period. and occa- sionally in other tissues such as tonsils and The virus arrives in the area of the brain or cornea. and Shaddock. relatively mild and include some perivascu- 1991). often reaching titres of tions with the inoculation site. organs in late stages of the disease. lachrymal glands. fre- Central Nervous System Infection quently in myocytes of muscles. 1988. Antigen distribution is quite variable. Replication in extraneuronal tissues is evident in the exocrine cells of salivary glands. 1980). Baer and Wandeler. Virus nomenon: low antigenicity of the inoculum replication in the CNS allows a centrifugal and rapid sequestration within peripheral spread. lar cuffing. certainly the expression of damaged neuro- lation (Baer et al. and may also be genomic RNA. but also high amounts Peripheral Organ Involvement of non-infectious viral proteins. Fekadu et al. 1979. Often it is limited to nerve fibres and ganglia. an antibody response can be observed when animals are injected exper- imentally with inocula that not only con- tain infectious virus. motor and/or sensory fibres is in the axons as visible by standard histology. 1994). In laboratory rodents it is to be proportional to the length of the mor- possible to interrupt the transport to the CNS bidity period (Fekadu et al. eral nerves is the rule (Charlton. Balachandran and Charlton. The clinical by amputation of the inoculated limb or by symptoms resulting from CNS infection are neurectomy within a short period after inocu. The pathology and the distribution other cells. not all behavioural There is usually no measurable immune changes are easily explained by the areas of response to rabies during the incubation the CNS most obviously affected. The clinical symptoms are highly vari- for the presence of a rabies virus infection. Baer and Wandeler. There is considerable variation in the clinical Fekadu. 1975. However. Numerous observed virus excretion up to 7 days. dumb form is common in dogs. Even animals in a dumb phase • restlessness. the clinical syndrome is classified as dumb (paralytic) or furious. dumb phases • running without apparent reason. (allotriophagia). and tongue. (i) that virus excretion with saliva occasionally provoked and they may snap into the air. as described above. and concluded that nonfatal rabies that some salivary glands in which no virus is very uncommon. The • regurgitation. sometimes ria that allowed them to make a correct rabies accompanied by elevated body temperature. could be isolated had inflammatory lesions consistent with those found with rabies infec- tion (Foggin. (1965) and Fekadu et al. Some animals never excrete virus invariably fatal (Bell. . but in authors provide evidence that rabies virus one case 14 days before the onset of clinical infection with involvement of the CNS is not symptoms. (1982) and is rarely longer than 10 days. Foggin (1988) found that only 72% of find any CSF antibodies in clinically healthy rabid dogs had viable virus in the salivary dogs in a survey in an enzootic area in South glands. (1972) did not tently. During the initial period of course within and between species. and the almost unfailingly identify a clinically ill animal as invariably fatal outcome are strong indications rabid.I. pupillary dilatation. The furious • altered behaviour. diagnosis in over 90% of suspect dogs kept These prodromal symptoms usually evolve under observation. 1991a). 1987. Vaughn et al. sensitivity. form is characterized by marked irritabil. 1991b). able (Tierkel. and (ii) that antigen detection extensive paralysis. and dyspnoea. In addi- sickness there may be increased nervousness tion. and partial paralysis of the lower jaw • abnormal licking of water. Based on the manifes- signs makes it likely a clinically suspect dog is tation of predominant paralysis or of excitabil- indeed infected by rabies virus: ity. dumb form may lie quiet for extended peri. and if small enough often devoured • biting with no provocation. Nevertheless. In experimentally infected dogs toms to deaths is from a few hours to a week. Rapidly worsening symptoms There is no single symptom that would in a dog. hyperactivity. Fekadu. objects within reach are • aggression. The range bation or in prodromal phases is not always in length of illness from the onset of symp- possible. In all occurs a few days before clinical symptoms species the clinical illness progresses toward are detectable. Bell et al. eyelid. Fekadu and Baer. (2005) developed crite- sexual behaviour. 1980. leading to drooling of saliva. hyper- nomonic may never develop. Diagnosis and Surveillance Clinical diagnosis Clinical Symptoms Often rabies is diagnosed on the basis of clinical symptoms. some may excrete intermit. symptoms that are considered pathog- and irritability. may alternate with furious stages in a single • stiffness upon running or walking. protrusion of the third • licking its own urine. Histological examination revealed America. abnormal Tepsumethanon et al. ity and restlessness. individual. According to the authors very rapidly. Other frequently observed symptoms are • dry.48 A. drooping tongue. attacked. sions. with or without convul- in the brain of an infected animal during incu. 1988). Wandeler et al. 1975. tremor. abnormal vocalization. may have a tendency to bite when they are • bites during quarantine. • biting and eating abnormal objects. with their saliva. within hours or a few days. Animals displaying the • drooping jaw. • abnormal sound in barking. and then stupor and death. into the occurrence of at least three of the following more advanced stages. ods. The test is similar in microscope. However. . More recently a direct rapid immu- fixed in acetone and then incubated with a nohistochemical test (DRIT) has been devel- fluorescein-labelled anti-rabies (preferably oped at the rabies laboratory of CDC. pseudorabies. in only about 80% of the positive cases when compared with immunofluorescence. The method is The test has therefore been recommended for highly specific. mostly in the form of RNP. and real-time PCR. costly. Nucleic acid amplified in PCR cal surveillance. 1991. brain impression smears. and requires histology cal disorders may be considered differential equipment. the genetic sequence to which their probes are The method of choice is immunofluo. 2008). It gives accurate results position. In addition. has become tion when they have contaminated (bitten) important as a back-up test in many modern humans or when essential for epidemiologi- laboratories. Clinically suspect cases of rabies The PCR test. This is the method ing neurologic disorder in the absence of bind- of choice if formalin-fixed tissue is the only ing alternate diagnosis. especially to contaminating bacte. which is use- ful for virus characterization. Biotinylated monoclonal antibodies smears are then washed in buffer to remove are used to detect rabies nucleocapsid anti- excess conjugate. 1991). described. used.. This method is rel- of other canine diseases causing neurologi- atively slow. liable to miss variants with minor differences in Trimarchi and Debbie. facilities. Cytoplasmic viral antigen accu.. 1988). PCR tests have high analytical sensitiv- of Standards for Diagnostic Tests and Vaccines ity for the particular virus variants for which (2008). It is therefore advisable to consider as suspect Immunohistochemistry on paraffin or frozen rabies cases all instances of rapidly progress- sections is highly reliable. These tests detect rabies antigen within ria. minutes and do not require any laboratory nosticians must be assured. Sureau et al. targeted. Impression smears A number of other methods have been of selected parts (which must include hip. Feiden et al. California) is particularly useful as it Current laboratory tests are described in detail can be completed with hours and is less prone in the WHO publication Laboratory Techniques to contamination than more convention PCR in Rabies (Meslin et al. canine hepatitis.. occurring pigments may fluoresce. in perikarya and dendrites. receptors). they are (Webster and Casey.. 2006. Dogs and Rabies 49 • appearing sleepy. but has the advantage as fluorescing polymorphic inclusion bodies that fluorescence microscopy is not necessary. The demonstration of inclusion bodies • imbalance of gait. appear rescent antibody test). infectious material available (Bourgon and Charlton. Carlsbad. rapid immu- conjugates bind nonspecifically to a number nochromatographic tests have been devel- of structures (sometimes by mediation of Fc oped and evaluated (Kasempimolporn et al. 1988.. Laboratory diagnosis using TaqMan® technology (Life Techonologies. and examined with UV gens in brain smears. and in numerous other publications they have been designed. Diagnosticians must be particularly rescence for the detection of viral antigen in vigilant to this possibility. The Georgia. The air-dried smears are methods. Atlanta. Nevertheless. and a number 1987. brainstem. sensitivity and specificity to the FAT (fluo- mulations. 2011). situations where a sophisticated laboratory cian has to take into account that naturally is not readily available (Lembo et al. the diagnosti. The maintenance of proficiency of diag. 1996). and that Dürr et al. anti-RNP) immunoglobulin preparation. There are different variants of the PCR assay. in the OIE Manual assays. diagnoses. tests can be used for sequencing. and in neurons with histological staining meth- • frequent demonstration of the ‘dog sitting’ ods is less reliable. and medulla oblon. probably because it offers no additional gata) of the dissected brain are made on advantages over other immunological test microscopic slides. Distemper. which detects and ampli- must be submitted for laboratory confirma- fies specific nucleotide sequences. The ELISA test has not been widely pocampus. and in addition to fix half The most obvious duty of the diagnostic of each brain in formalin for histological or centre is to achieve diagnosis rapidly and to immunohistological processing. which is diagnostic centre as whole carcasses. then one is left with the question of the cause. wild Carnivora. or brain samples col.50 A. it is highly roadkill. etc. It might not be achievable without hosts. acted suspiciously or that have contaminated A diagnostic centre is more useful if it serves humans are the material most desirable and a large area. natural exposures (e. Confirmatory tests projects.. what antibody levels to result from different lected through the foramen magnum or the forms of abortive infections and noninfective orbita with a straw or another suitable probe. Serum antibodies are usually not of very high titre and are not accompanied by CSF antibodies if they are the Material suitable for surveillance result of vaccination. Also. It is a formidable task to ensure the sub- to a diagnostic laboratory should be encour. but it is very likely that the disease are especially important when results are prevalence among them is extremely low. Wandeler et al. completion of submission forms.I. The most outstanding isolation amplifies the virus. mission of specimens from all regions that aged. and bats are the require diagnostic services and/or need sur- species most often recognized as principal veillance. or ELISA) to collected under suboptimal conditions. Antibody titres are very high in serum and in CSF if they are the corol- Specimens can be brought or shipped to the laries of survival of clinical disease. lyssavirus variants are likely to occur. With all diagnostic tests. small pieces of brain (brain stem. considered to be exceptional. Virus or in tissue culture). PCR. We do not know extracted whole brains. the The specimens should be transported frozen possibility of cross-reacting rhabdovirus anti- or refrigerated. oral). but rarely acknowledged problem in neu- ter chance of detection. Their submission ity. Antibodies can be meas- virus isolation procedures in either mice or ured in neutralization tests (assayed in mice cell cultures are particularly useful. and wild ruminants are personnel in agricultural and health services quite often victims of the disease. Where uncharacterized lance on serology. One might also consider submitting fresh material. The field personnel must also be . report quickly. In addition. only rarely support epizootics independent The diagnostic centre should give instruc- from the before-mentioned species. Obligations of the diagnostic centre ratory. such tests tralization assays are virus-inactivating prop- require the use of other detection methods erties that occur quite frequently in blood (immunofluorescence. as well as clinically normal animals and transport. The confirm the presence of the virus. can be misleading. packag- not suitable for surveillance are rodents and ing. a positive result as real. and There is a host of reasons why serology where test validation methods are limited. and birds. however. they problems with nonspecificity that must be require days or weeks to complete and are overcome in haemagglutination inhibition therefore not suitable for diagnosis where tests and ELISAs are profound. a network of motivated and well-instructed domestic herbivores. and not only its immediate vicin- suitable for surveillance. Other domestic Carnivora (cats. Dogs.g. It is negative in suspicious cases with histories also not recommended to base rabies surveil- of human exposure. Clearly tions for sample conservation. to permit timely post-exposure Brain specimens from animals that have prophylaxis and disease control decisions. medulla oblongata.). This is not to state that such material advisable that results are confirmed by one should never be examined in well-defined or more additional tests. hippocampus) in 50% buffered glycerol if circumstances do not permit a rapid and refrigerated delivery to the labo. It is advisable to transport bodies has never been investigated properly. but they in all regions concerned. If one accepts urgent medical decisions are needed. heads. allowing a bet. or as virus isolates tion and control of rabies have been made thereof. Rabies Surveillance • location (where animal was found). It cal maps and tables listing by species and also should provide blank submission forms. possibly all. A random sample. such as public health measures. 1991a. age and sex of the animal. (some exceptions may apply). They should furnish the following movements. Last but not least. including effective impor- uid nitrogen or in lyophilized condition. control planning. They have a host-specific analyse one. area of origin the numbers examined and the Submission forms should accompany every numbers found rabid will indicate trends and specimen. Selected samples should be forwarded to laboratories qualified to per. and also to killed or found dead. specimens found positive is dependent on the following preconditions: in routine testing. has additional objectives. large due to the very low prevalence of sions and on what categories of specimens detectable rabies infections in a population to collect. • No case of indigenously acquired rabies age are to cover epizootic events spatially and infection has been confirmed in humans temporally. goals of specimen selection for long-term stor. 2011). whether the animal was exposure prophylaxis policies).. form this task if it cannot be achieved in the • An effective system of disease surveillance diagnostic centre. and to produce monthly. quarterly. promote public awareness to permit disease- and observations on the source of infection. such as establishing an understanding of the epidemiology (this A number of items of supplementary will allow the formulation of strategies for information might also be collected. • date (of submission). Reference samples need to is in operation. ual suspect animal is to enable post-exposure • date of exposure. implemented. None of Epidemiology the classical epidemiological parameters such as incidence and prevalence are very useful: Rabies viruses are adapted to the physiologi- the specimens submitted to the diagnostic cal traits and the population biology of their centre do not constitute a random sample. it is the diagnostic cen- tre’s duty to analyse the findings or to make them available for analysis. or better still. (the infection is not readily detectable in its ply material for conservation and packaging incubation stage). would have to be enormously pathogenicity and pathogenesis. and prophylaxis decisions. principal hosts (Bacon. other). • All regulatory measures for the preven- nal rabid brain samples. and to represent all virus variants or any animal species during the past 2 years that might circulate independently. • Rabies is a notifiable disease. simple periodi- if these are not readily available in the field. which includes post- clinical symptoms. if one would attempt to Wandeler et al. and Rabies-Free Status • owner’s name and address (for domestic animals). They should be stored as origi. The tation procedures. bite. at −70°C. Adaptation . Disease surveillance • names and addresses of exposed people. 1994). Wandeler. the recog- characterization should be performed on nition of rabies-free status of a country or area some. The objective of rabies diagnosis of an individ- • type of human exposure (none. Dogs and Rabies 51 advised on the purpose of sample submis. in liq. laboratory diagnosis. information: • species. Adequate surveillance is The diagnostic centre should perform essential for monitoring the impact of dis- a number of additional duties aside from ease control operations and for maintaining assisting sample submission and achieving rabies-free status. 1985. A serotype/genotype According to the WHO (2005) and the identification and/or rabies virus variant OIE International Code (OIE. be set aside. However. The diagnostic centre has to sup. or yearly reports. aggressiveness. Wandeler et al. Encounters between 1974. explore experimentally. recent phenomenon in other parts of the Mitmoonpitak et al. (ii) they are kept indoors of viral host adaptations are more difficult to or in enclosures and leashed when outside. and densely populated rural areas. and of Mexico. World War I. dog rabies declined after infectious contacts by changing host physiol. 2004). Neville. of a particular virus variant to its principal (Swanepoel. 1984. and by observations Blancou. 2004). These and other significant aspects their movements. Eng et al. Acha and Arambulo. WHO. Probably it was only rela- host is indicated by the frequency and mag. There is no recent evidence of the World that wildlife rabies provoked epizootics in stray dog populations in the United States or There are areas where we observe enzootic in Europe. and (iii) dog vaccination is strongly recom- mended or even compulsory. Belcher et al. 1996. (1999). Three fac- infective and susceptible individuals leading tors may account for the low prevalence of to transmission must occur at the correct fre. Blancou et al. the Canine Rabies Middle East. frequency in cities remains relatively low.. European explorers in the middle of the 19th (2009). virus excretion are insufficient attributes for In those areas only 0. In North America rabies was ogy and behaviour. rabies virus circu- from an infective to a susceptible individual lates in the dog population. Beran et al. documented to some extent by in vivo experi. causes aggressiveness as a prevailing 20th century rabies was prevalent in wild feature among induced behavioural changes. World War II. 1988b). Hampson et al. (2009). In contrast.I. anisms of social interaction or they promote In Europe. while the Viruses either take advantage of normal mech. tively recently introduced into regions where nitude of its excretion on one hand. and century. and in parts of Southern Africa. 1985. highly enzootic with only moderate fluctua- 1996). in many animals and in field specimens submitted for countries it is more a problem of periurban diagnosis (Blancou. North America north However. the host’s high susceptibility to it on the other 2004). and areas where the disease in dogs must be considered as spillover from wildlife rabies. (1976). In North America it was first reported one gets the impression that dog rabies is in Mexico early in the 18th century (Baer et al. and Asia for thousands of years (Baer et al. and was first reported in dogs in Zinsstag et al. 2004. 1980). and Latin America. (1990). dog rabies has been a more (1970). Steck and Wandeler. In recent decades in large parts of Asia.52 A. It was first recorded in South America tions in prevalence. Canine rabies is occasion- on virus excretion in experimentally infected ally coined ‘urban rabies’.. (1998). Apparent prevalence several countries in the early 20th century can be influenced by surveillance coverage. . Domestic dogs have been the principal hosts of rabies in Europe. world. possibly by maintained principally by dogs until after altering specific neural functions (Charlton. From information given by Glosser et al. in a host population. 1976. since epizootic patterns have and Fernandez.. 1991). (1993). In sub-Saharan Africa also been described. This picture is only par- in the beginning of the 19th century (Steele tially correct. for example by Bingham rabies was noted for its absence by early et al. and by it is now endemic (Nadin-Davis and Bingham. Carnivora in Europe. This has been 99% of all reported cases are in dogs (Turner. Between 75% and in the event of a biting incident. However. ments on susceptibility. 1991). It may also be that virus strains adapted to wild species are not very well suited for propagation within Dog Rabies in Different Regions dog populations. In the second half of the 1994).. 1988a. Blancou. and Fekadu (1982). dog rabies. These properties allow for transmission Africa. Rabies virus. susceptibility. (1972). hand.1–5% of the rabies cases allowing a prolonged persistence of the virus reported annually were in dogs (Tabel et al. rabies in dogs: (i) most dogs are restricted in quency. and Waltner-Toews et al. 1988. ably more than any wild carnivore population prevalence may vary considerably with time. low density (Foggin. 2010a). onto et al. Seasonality mated transmission rates between dogs were in wildlife hosts has been hypothesized to 0. The rate at which infected hosts transmit Rabies in many dog populations appears rabies to healthy animals depends on the social to rank high as a cause of adult dog deaths.. were also conducted in Tanzania (Hampson sonal fluctuations of bitches in oestrus and et al. the density may not be a determining factor for The epidemiology of rabies is gener. Incidence.8.. Dog population searched for.. Bingham et al.3 days) and the infectious not clearly confined behind advancing geo. canine rabies. 1993). This may be due to the poor surveil. 2009) that the basic reproductive rate the islands of Flores in 1997 and Bali in 2008). tant analysis was performed in N’Djaména nounced seasonal trend for dog rabies in the in Chad (Zinsstag et al.. As discussed above. 2008). ever achieves. though sea. Unfortunately this also holds true data will tend to even out more local epi. the Dogs are kept and tolerated at very high num- disease is frequently found when actively bers in most human societies.. as has been reported for a mission distance was 0. For example. Hampson et al. Domestic dogs tend ity of rabies transmission.g. low a marked seasonal trend in prevalence the combination of field observations and as it does in many wildlife maintenance hosts modelling has provided some new insights (Blancou et al. Beran et al. 1. This is in contrast to by their owners to new homes. ses of dog rabies epidemiology remain rare. However. In addition. although particularly at local scales.01.0002 km2/(dogs × week). 2007. indicating low-level endemic stabil- well developed in dogs. and for prevalence. though indi- number of wild carnivores (Bingham et al. The in pregnancy can be observed in some areas investigators estimated important epidemio- (Totton et al. the frequent statement that high-density dog dogs will often accompany their owners on populations permit the occurrence of enzootic foot over long distances. Dog published information from other parts of the rabies epidemics are probably spread to a world. 2009).. authors also calculated the average number of lance of dog rabies in countries which do not secondary cases produced by an infected dog. An impor- although Swanepoel (1994) does record a pro. it will have an impact ally not very well understood. The esti- Natal Province of South Africa. though it is well-known that mal home ranges. Noteworthy is the statement (Hampson ple in cars. The breeding patterns and seasonal territorial effective reproductive ratio was estimated to instincts. well out of their nor. However. vidual rabid dogs travelled much further. This is consider- the Philippines were due to rabies.. Lembo et al. logical parameters such as incubation peri- Epidemics of rabies in dogs are usually ods (average 22. 1999). as well as from be typical of the disease in this species. on the population’s social organization on one . (1972) densities may reach several thousand per km2 found that 23. for exam. indicate high prevalence rates of rabies.. both characteristics which are less be 1. 2009. dog populations. system of the host which promotes contact Although official statistics will often not between infected and non-infected individuals. The mean trans- graphical fronts. 1988. have developed infrastructures.. Excellent studies to breed throughout the year. The 1999). of rabies appears to be independent of dog as dogs incubating the disease will be moved population densities..05 and large degree by human activities. a the so-called basic reproductive number R0 spatially less structured epidemiology may for the Tanzanian outbreaks. and recovery rates are difficult this reason. 2009). and rabid dogs sometimes the disease also persists in dog populations of move long distances on their own (Butler. for dog rabies in spite of the easy access to demic trends (Bingham.88 km. Though thorough analy- Rabies in dogs generally does not fol. 1991. buses and fishing boats (e. Dogs and Rabies 53 particularly the scale of case analysis.0807 km2/(dogs × week) and between dogs occur as a result of their highly seasonal and humans 0. examination of whole-country to record. The ballpark R0s are between 1. periods (average 3. 2005). 1998. for areas in sub-Saharan Africa.1 days).6% of deaths in adult dogs in (Wandeler et al. the occurrence of rabies. Butler 1998). Wandeler et al. and often constraints in order to implement the most returning home after their journey. Habitat control is meant infection (Artois and Aubert. as documented in a number of cities in India this conflict leading to the transmission of the (Totton et al. movements is intended to limit social con- sion rates. and drugs. and Rabies Control should be implementable at the community level. sterilizing those not needed for breed- Chapter 12 by Lembo et al. and are attacked there by the territory owner. systems (Macdonald and Carr. and are therefore counterproduc- tive in the longer term. Six initiatives stand the best chance of long-term of 16 dogs for which Butler (1998) obtained success. but other hand. 1991a).54 A.. The concept of responsible dog ioural mechanisms operate in dogs. including dogs. 2009). and cultural con- rabid dogs wandered from their homes. including control and updated recommendations and circulation of relevant information. achieved through mating restrictions. It is quite likely that similar behav. habitat control. 1985. Butler (1998). For this purpose the the immunization of dogs and other domes- WHO/WSPA Guidelines for Dog Population tic animals contain inactivated rabies virus .. are and 13 in this book. control. There is cal sterilization. Sustainable rabies control policies should be multi-faceted. 2010b). in this book.I. It is important to understand these covering considerable distances. Wandeler. taking into out in rural Zimbabwe. including antif- evidence that disoriented rabid foxes (Vulpes ertility vaccines (Bender et al. hand. see also Larghi et al. The control of social parameters which determine transmis. These effective methods of dog population man- dogs approached homesteads and other dogs agement (see Chapter 13). Dog Population Management Rabies has a high incidence in dogs in areas Prophylactic Vaccination of Dogs where the animals are poorly supervised. Central governments should support communities in establishing mechanisms For a comprehensive review of dog rabies to effectively manage their dogs. will alien- dogs (all unvaccinated) resulting in transmis. detailed records were seen to bite 11 other such as mass-culling campaigns. in a study carried be adapted to different contexts. safe and guidelines see the website produced by ethical mechanisms for removing unwanted the Global Alliance for Rabies Control1 and dogs. provok. shelter). to reduce the availability of resources (litter. food. and Veterinary Vaccines for Attempts to reduce numbers of poorly Parenteral Use supervised dogs and to educate own- ers toward responsible ownership should Most of the rabies vaccines used today for therefore be attempted. and on dog–human interactions on the Management (1990) should be consulted. found that 15 of 24 account economic. ate communities from the goals of rabies sion to seven of the dogs. Heavy-handed imposed methods. (1988). and this allows for considerable variation in the removal of straying dogs. Rabid dogs may also reproduction). 1995) and reproduction control. ing. Rabid dogs will frequently display tact and access to resources (both leading aggression and actively seek other dogs and to disease transmission and uncontrolled other animals to bite. social. Recommended control highly adaptable with respect to their social measures include movement restrictions. Community-led and provoked conflicts in the process. and Chapters 11 Most canid species. surgi- mally elicit an aggressive response. ownership (WHO/WSPA. some straints. and provision of basic health services for animals. Animal vulpes) wander into their neighbours’ range birth control programmes can be beneficial. Reproduction control may be bite following stimuli which would not nor. 1990) as applied ing a healthy dog to get in conflict with a in industrialized western nations needs to diseased one. ownership. rather pragmatic recommendation. Carlos et al. Their enforcement is impeded mended that vaccines are completely innocu. and that straints. 1993. 1997). 1997). usually an inactivated vaccine of inactivated tissue culture vaccines. Mexico. Modern inactivated require some more research. con- for use in domestic animals because of finement. et al. and simple application of regulations on dog by national regulatory agencies. 1987. 1988. breeding restrictions) have been problems of residual pathogenicity and/ practised simultaneously (Tierkel et al. cines is no longer recommended for dog immunization. post- tissue c ulture vaccines combine safety exposure vaccination of dogs and cats has with high immunogenicity (Chappuis and been recommended following contact with Tixier. register (or license) dogs. Bunn. (1993) speculate that the outbreak in ing will probably become available soon Hermosillo. and may even eliminate the an age of 3 months. dog vaccination is recom- in combined vaccines. except for special situa- tions (e.. Registration can but every new product should be investi- be made dependent on the production of gated for its overall immunogenic potency. 1982. and preferably campaigns may reduce rabies incidence in 2 years after one injection. In industrialized nations with predominant leptospirosis. 1991) and are efficacious in Australia. But well-planned and well-executed they confer immunity for 1. to an increase in population density and a Rabies vaccines for dogs should satisfy drop in vaccination coverage. 1953. These vaccines do not always of a product recognized by the national have an efficacy comparable to the efficacy authorities. Recently.. Vaccinations ebrally (with fixed viruses). national campaigns under eco- nomic constraints). Eng and other products of genetic engineer. with Canine Rabies HEP (high egg passage). Though this is certainly a disease eradication should be the goal. 1950. OIE (2008). the field (Chomel et al. and ERA (Evelyn Rokitniki Abelseth) have been signific Successful attempts at the control of rabies ant components of rabies control in the have generally occurred where both vac- past. adenovirus. Owners have to competitive inhibition have been noted. parainfluenza.. in all dogs above dogs drastically. 1988. Live attenuated virus Rabies Control in Areas vaccines. Wells. by a number of ecological and cultural con- ous. The conferring 2 years of immunity after one use of modified live (attenuated) vac- injection. but are no longer recommended cination and dog control (destruction. Taking the cost and benefits of a vaccines licensed for post-exposure treat. No indications of mended or compulsory. a certificate that the animal has been vac- Inactivated nerve tissue vaccines may be cinated against rabies when over 3 months prepared from the brains of lambs or suck- old and had been revaccinated at periods ling mice inoculated newborn intracer- of not more than 1 or 2 years. Several Wildlife Rabies manufacturers include a variety of dif- ferent antigens (distemper.. campaign into consideration. 2009). disease in areas where it is not maintained There are no treatment schedules or by wildlife. Aubert. Dogs and Rabies 55 and dead antigen. may have been linked (Chappuis. Rabies control efficacy and safety requirements as they are in areas with canine rabies is usually not a described by WHO (2005). It is recom. Recombinant vaccines Fredrickson et al. parvovirus) wildlife rabies. such as LEP (low egg passage). the topic may than a temporary reduction of the incidence .g. They may be should be done by parenteral inoculation adjuvanted. or poor efficacy. 1954). Cell lines and pri- mary cell cultures are used as substrates Dog Vaccination in Areas with for a number of virus strains. we suggest that ment of dogs. Precausta bats infected with ABLV (Animal Health and Soulebot. even for very young animals. 1991. . 1991. The state vaccination teams may run a 2005. immunity in dog populations by parenteral sive for many people. including inadequate logistics. 1996. vaccina. applied or is failing. will reach various seg- mal local news networks. 1996) thought to be neces- number of dog population parameters (size. 1994. In many African turnover. 1993). legislation. Beran. is gramme execution. Such campaigns This notion can only be partially correct. rather than also because dog owners often have other pri- temporary. These docu.I. De Balogh et al. at present there are no vac- the most important way in which population cines licensed for oral immunization of dogs. where ments give detailed guidance on the planning they visit each household and vaccinate every and management of control programmes. However. 1990). local plans are imperative. but can be much ministries and national and local agencies is better if properly implemented (Wandeler necessary. Comprehensive national. 1998). WHO/FAO. WHO provides useful guidelines et al. These orities. or where the sons for not reaching a sufficient level of herd cost of a veterinary consultation is too expen. 1984.. Beran. recommended. Rupprecht et al. as done for tising using loud-hailers. this method usually to consider national structures and resources. and campaigns of which the most common is the large numbers of ownerless dogs. 1991b). Aylan and Vos. immunity is achieved in the more affluent The high number of human casualties parts of the world. be attempted. on dog they are able to catch. This is 2007).. Dog owners may take their pets to private et al. 3... and ments of a dog population very differentially. or state veterinarians for vaccination. The state veterinary services may conduct insufficient community participation. . 1990. and they have dogs to the central point. programme it is necessary to consider a Coleman and Dye. and logistic aspects can then for rabies control since 1978 (Steck et al. Because of this. 1982. 1948. and (iii) Against Rabies avenues to provide information and educa- tion. 2000. 1993.. using live attenuated vaccines and taken: a vaccinia rabies glycoprotein recombinant.. although very demanding of resources. rate. Baits require a considerable amount of prior adver. 2009. have been assessed (Bishop et al. usually successful in achieving the 70% cov- For planning a comprehensive control erage (Korns and Zeissig. broadcasted over a landscape. Operational research tested for safety and efficacy in a variety of for monitoring campaign efficiency is strongly species. house-to-house vaccination campaign.. Wandeler et al. 1982). whereas it only accounts caused by dog-transmitted rabies clearly for a small proportion of vaccinations in less indicates that dog rabies control either is not wealthy countries where there are few vet. place at a particular time. be adjusted according to findings in the pilot Wandeler. 2. and infor. sary to eradicate dog rabies. Estrada 1. A number of different approaches can be Field trials. wildlife immunization. It is often central point campaign where owners are thought that a majority of these problems required to bring their pets to a designated could be solved with an oral vaccine for dogs. and on techniques in local pro. (ii) ways Oral Vaccination of Dogs of cooperating with local residents. 1999. Pilot projects may help in assessing: (i) dog accessibility. 2001. The latter method. Oral vaccination of wildlife has been applied tion strategies. Cliquet et al. There may be many rea- erinarians within communities. An effective maintenance programme and genetically engineered vaccines have been must be part of the plan. vaccination. Plans for large-scale operations. for programme management (WHO. or they may not be able to take all their plans have to identify a goal.. accessibility). This goal should be achieved in a particular area within a relatively short time period (a few weeks). does not reach more than 10–40% of dogs Effective cooperation among all involved (Brooks.56 A. posters. Fekadu et al. Vaccination coverage and Asian countries it is not used extensively of about 75% of the total population should due to resource constraints. A number of live attenuated phase. including dogs (Chappuis et al. 1998). The number of vaccine doses that do not reach • the immune response to vaccine in imma- the target (immunize a dog) is higher than ture animals is inadequately defined. 1992b.. preferably 4 months or more. 1995. Dogs and Rabies 57 though other distribution models may be vaccination. long incubation periods are rare. However. and facilitates com- • misidentification of animals. Only in its zation is recommended only for people with 8th report (WHO. Both should be species of mammals and/or permit their entry advocated by public health education. condition presently applied to wildlife immunization. It is than in adult individuals. 1994. from a immunization. and wound treatment after should be subjected to a prolonged period of exposure. very than with parenteral vaccination campaigns. reports state that ‘on entry... 1997. • animals vaccinated during incubation a vaccine that can be administered orally will may develop antibody. and convened a number of con- variants of low pathogenicity for dogs is sultations to outline efficacy. ians and laboratory personnel. are con. 1998.10 of the OIE Terrestrial Animal of baits and bait fragment if not taken. and should indicate that proper quarantine. Matter. . and the proper should prohibit the importation of certain prophylaxis after exposure. immunization procedure. Pre-exposure prophylactic immuni- erinary service’ (7th report. Earlier WHO Expert Committee the epidemiology. certificates. with recuperation Chapter 8. 2005) gives sultations recommend that only ‘door to door’ more detailed recommendations. sidered for initial field trials. the animal not be prevented. In its 8th report the Committee recom- dog population densities can reach several mended taking into account a number of thousand individuals per km2: this is between considerations when contemplating import 100. and logistic aspects (WHO.g. Logistics will not be simpler few weeks to more than 6 months. 2011). 1989.and 1000-fold the densities of wildlife regulations: populations targeted for rabies control by oral • incubation periods are variable. such animals zoonosis control. parasite load) etc. and non-target species including humans. and serology as an alternative. and the animal to be vaccinated. on immunotherapy should begin as quickly as premises approved by the Government vet. The Prevention of Human Rabies Maintenance of Rabies-Free Status Important components of the prevention The WHO Expert Committee on Rabies rec. but disease may reduce distress in the vaccinator. The likelihood certain that circulating neutralizing anti- of human exposure to vaccine is much higher bodies persist for shorter time periods than in wildlife vaccination campaigns. therefore essential that oral rabies vaccines for • immune responses also vary with vaccine dogs meet higher safety standards than those type. it is with parenteral vaccination. wise cannot be handled. possible. and serum samples occur. and In view of these advantages WHO supports • the impact of rabies-related viruses and the concept. 1990. Such only under the authority of a licence granted education should include information on previously. Health Code (OIE. munity participation if properly advertised. of animal (e. 1992. and so does and ‘hand out’ techniques. This • false-positive results occur in current permits the immunization of dogs that other- serological tests. The WHO con. 1984). 1992a) was the Committee an elevated exposure risk. safety for target unknown. applied (Frontini et al. 2007). Ben where strict quarantine measures are imprac- Youssef et al. One has to visualize that tical. The 1st report of the WHO Expert 1993. compared to parenteral inoculation. Consultation on Rabies (WHO. clinical signs in animals. such as veterinar- discussing a system of animal identification. of human rabies are the avoidance of poten- ommends that countries free from rabies tially infectious contacts. owner. . The are human cultural traits that vary dramati- appropriate treatment may not be available cally from area to area.. rabies is due not only to the frequency of expo. 2008). 2005). with vaccine and passive immunization with rabies immune globulin is considered the best post-exposure prophylaxis. the easy access to dog (Acha and Arambulo.I. reasonably well explored. 1993).. where the annual exposure to dog humans. Worldwide. or because the based on WHO recommendations (WHO.. in areas where populations should allow collection of valu- dog rabies is prevalent (Baer and Wandeler. Dog population biology is some areas (Wandeler et al. Most of these were conducted in 1986. biting dogs are infected with rabies. 1988. It is also possible that the operations. records. Immediate and thorough cleans. 2010). A systematic collection of detailed 1987). Still. socially.. An inquiry 2005. Nevertheless. et al. The of infection. Xu et al. 2007. Bögel and Meslin. 1993). and sures. On the other hand. Research Needs. but not pected exposure should be considered in all all. The success rate of the traditional be given when a bite by a suspicious ani. 1990).. which are usually sidered equivalent or superior. one The widespread occurrence of human has to remember that tolerance.5 million per year (Bögel and Motschwiller. China and India alone account for ough studies on dog rabies epidemiology are almost 90% of the word consumption of rabies so rare. into rabies deaths in Sri Lanka revealed that a ing of bite wounds is an important first step. Structural constraints and a shortage vaccines. incubation periods. Attributes of culture (spatially. 2009.000 inhabitants are recorded in in recent years.000 people die of rabies every year (Knobel et al.000–60. supervision. up to four human rabies cal and cultural settings have been studied deaths per 100. traditional dog-bite specialists. Post-exposure prophylaxis (PEP) should recognized because other treatments are con- follow national guidelines. 1993). while a WHO East Africa. 2010a). and not A number of dog populations in different all bites by rabid dogs lead to clinical rabies in parts of the world and in different ecologi- the bite victim. healer may appear to the casual observer as mal or a contamination of mucosa or broken respectable. but also their accessibility for control (religious) beliefs. able data. Wandeler et al. Almost all human rabies deaths. 2007. in view of the low frequency of skin with potentially infectious material has rabies transmission by mostly healthy biting occurred. Combined active immunization dogs (Wandeler et al. Some. temporally. similar investigations are largely document (WHO.. PEP should prophylaxis.58 A. Questionnaire surveys produce necessity of the appropriate treatment is not information on such features as dog:human . 1985). vaccination highest figures come from South and South. Not all the Tanzanian studies. occur in developing countries sis. 2010b) puts this figure at 14 absent in other areas with dog rabies prob- million post-exposure treatment applications lems. disease entity is not recognized. The number of people A few significant studies have provided receiving post-exposure treatment – mostly new insights into the epidemiology of dog after dog bites – was judged to be about rabies (Hampson et al. Lembo 3. victims also seek post-exposure immuno- decisions for further treatment. good proportion of dog-bite victims resort to The circumstances and nature of the sus.. Operational human health. It is rather awkward that more thor- each year. but also to the failure of applying proper other aspects of the ‘habitat carrying capacity’ treatment after bites from rabid animals. economically). availability (accessibility) of resources. That this can lead to spectacular new bites is between 2% and 5% of the population insights has been adequately documented by (Sudarshan et al. and contacts with other animals and East Asia. of resources may often preclude a suitable and the vast majority of treatments after bite epidemiological surveillance and data analy- exposures. not only determine dog population charac- or it may not be in compliance with traditional teristics. Rabies in dogs is a significant threat to Questions. an estimated Research 30. This may in part be due to a high rate of case histories could identify possible sources exposure to biting dogs (Eng et al. according to ance granted to dogs must find explanation criteria applied. Berlin.com. nearly all human rabies cases that in future programmes. (1993) Can vaccination validated by the titration of rabies antibodies in serum of cats and dogs be an alternative to quarantine measures? Abstracts on Hygiene and Communicable Diseases 68. has not made the progress operations. campaign efficiency. in different cultures and is not always easy to tion. Cultural conventions determine the level ing. C. which is partially a function of the implemented without too many difficulties density and structure of human settlements. reproduction. venting and curing dog-transmitted diseases Meggitt. The toler- status of a dog may change. dog-keeping practices. Latocha. . P. We also suggest prophylaxis. 1960. pp. If there is a suspicion that a in processes of socialization and psychology. Pilot projects in The ultimate purpose of rabies control is general may help in assessing (i) dog acces. the correct treatment was not applied. the protection of humans from both infection sibility.V.A. 1982). Dog and morbidity and mortality. (1985) Rabies in the tropics . M. More inquiries into health sys- Studies on this topic in non-industrialized tems and the ethnology and sociology of pre- nations (such as Luomala. Such Education towards responsible dog owner- ‘operational research’ conducted in con. Revue d’Ecologie (La Terre et la Vie) 40. H. or not applied in time. Canberra. and (iii) avenues to provide infor. how to avoid exposure. K. and Aubert. and access to resources (food. ination of dog rabies. Frank. In view tic aspects can then be adjusted according to of the high efficacy of modern post-exposure findings in the pilot phase. large amount of useful data. and also the prevention mation and education. Savishinsky.rabiesblueprint. R1–R22.N. 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Penny. 360–364.165. to provide objective information to the be transmitted from animals to human beings. Zoonoses and Public Health. 2010). e-mail: bbchomel@ucdavis. involving a variety of causa- tive agents and mammalian animal species Bite-Associated Bacterial Zoonoses as definitive or intermediate hosts. 2011). 2nd Edition (eds C. and are called zoonoses. Such a relationship of prevention. It is * Corresponding author. USA. In 2001. and males are twice factors: number of infected animals. The discovery of also of concern in terms of potential zoonotic parvovirus infection in dogs in the late 1970s contamination in many developed countries has raised concern over the role of dogs in the (Chomel and Sun. departments for non-fatal dog-bite-related ted from dogs to humans is rather difficult injuries (CDC. and infectious agents can useful. 2Plum Island Animal Disease Center. 2003). Children are more likely to estimate and will depend on numerous to be bitten than adults. mycotic. these have a significant public 90% of these visits are caused by dog bites health impact as some of them. more than 350. USA The pleasures of dog ownership are certainly transmission of the agent. ated with dogs.N. A review of current concepts sion of rotavirus and coronavirus. The present chapter transmission of that agent to humans. 1997). Macpherson et al. (Tan.000 peo- are widespread. gency department visits. risk than adults. behavioural charac- evidenced by the popularity of pet dogs in teristics of the owners. There are more than 250 zoonoses. but also placed human beings at behaviour. 5 Dogs and Bacterial Zoonoses Bruno B. New York. University of California. Several of bacterial dog-associated human diseases is parasitic. However. Orient Point. mode of as likely to be bitten by dogs as females. dog owner on pet care and management. while others can be severe or ple were treated in US hospital emergency even fatal. Between 70% and cies. because of their closer physi- tion in Mesolithic times. and explora- and pathogens. A lim- ited number of these are caused by bacterial Animal bites represent about 1% of all emer- agents and have dogs as the main host spe. California.) 67 . as well will focus on the bacterial zoonoses associ- as the potential role of dogs in the transmis. Prevalence of zoonoses transmit. though mild.edu ©CAB International 2013. Dogs. including putting objects in their a greater risk for exposure to dog parasites mouth or eating non-food items. children are at greater with dogs started with their domestica.L. Chomel1* and Jonathan J. The emerging trend and vector of rabies to humans worldwide of bed sharing with pets. USDA. including dogs. Usually. Davis. and existing measures the human population. This brought many cal contact with household dogs and their own advantages. Dog is still the main reservoir tion of the environment. Arzt2 1 School of Veterinary Medicine. is (Wunner and Briggs. Because of low virulence. canimorsus systemic Pasteurellosis infections occur more often in immunosup- pressed or immuno-impaired individuals. including gan- grene. 1997). 2009). 1996). anaerobic cations. 1987). P. pneu- spp. cases have been published. bacterium (NO-1) has recently been associ. meningitis.. Untreated infection can lead to severe compli- Talan et al. and Capnocytophaga canimorsus. canis variable ranging from 1 day to several weeks is the most common isolate from dog bites (Krol-van Straaten et al. wounds (Brook. have been isolated from 28% (31 of 110) of specimens from infected dog and cat bite wounds of humans (Citron Capnocytophaga canimorsus infection et al. cefuroxime. multocida subsp.. or meningitis (Griego et al. antibiotic of choice for treatment.. Usually. Onset pathogenic strains were found in 28% of the of clinical signs of C. inflammation. a thin. (1993) indicated that and cat bite wounds they cultured. However. stomatis. 1999)... 1987). is reported as such as Weeksella zoohelcum. multocida and P. disseminated intravas- of Pasteurella spp. dagmatis (Oehler et al. 1995. and doxycycline or fluoroquinolones in Corynebacterium spp. Additional symp- after the exposure are the typical symptoms toms include shock. 2009). canimorsus bite-related human cases spp. cefpodox- Staphylococcus spp.. 1996). C.. Other options include use become infected. Talan et al.B. osteomyelitis. Most ria of the oral cavity of dogs and cats. P. or persons following bites. dog bites and even more frequently with cat alcohol abusers (24%). canis. isolated aerobic organisms (Griego et al. are commensal bacte. commensal bacteria of the oral flora of dogs. multocida. 1996). A new resulted from a dog bite (Lion et al. 1999). Most infections associ. sepsis. Carriage rates be considered. infection. and peripheral cyanosis. et al. endocarditis. 1999). including Bacteroides and Prevotella arthritis. healing. 1990). occurs in immunosuppressed patients after P.. bite-related (Underman. After the first report in 1976. canimorsus infection is dogs tested (versus 77% of the cats). Pasteurella spp. Most (91%) of the known zoonotic bacteria mainly include Pasteurella C. Therefore. canimorsus is combination of a P-lactam antibiotic and a susceptible to most antibiotics. and a dog bite. multocida subsp. 2009). with cephalosporins (e. but Ganière et al. Additionally.. Penicillin is the cular coagulation.. septica tion of the initial wound at time of diagno- were the most common isolates from cat bites sis may range from gangrenous to complete (Talan et al.68 B. P. Porphyromonas spp.. and penicillin P-lactamase inhibitor (Talan et al. in dogs range from 22% to Capnocytophaga spp.. Gram-negative rod.J. C. Almost all patients present with and intense pain at the bite site a few hours severe sepsis and fever. The use of amoxicillin/clavulanic tion of amoxicillin-clavulanate (250 mg orally acid is a good alternative.g.. and endocarditis. of second-generation and third-generation ated with dog bites are polymicrobial. 1987. Streptococcus spp. pneumo- patients are more frequently treated with a nia. (1999) recovered of Pasteurella spp. Neisseria weaveri part of the normal oral flora of 16% of dogs (Canton et al. when fever include P. endocarditis. meningitis.. septic bacteria. at least 160 more ated with dog and cat bites.. are present in 38–76% of dog bite monia. an immunosuppressive treatment (5%). .7% of the dog 81%. and a lethality rate of 30% (Oehler et al. G is recommended as the drug of choice (Lion dog bite treatment includes the administra. septica. C. but most macular or maculo-papular rash. Human cases of infection after dog bites also include septicaemia caused by Capnocytophaga canimorsus (formerly DF-2).. as the most frequently penicillin-allergic patients (Oehler et al. including abscess formation. from 4. Swelling. multocida subsp. Alexander et al. Pasteurellosis is commonly associated with such as splenectomized individuals (33%). Arzt estimated that only 3–5% of dog bites will three times a day). 1995). The condi- and P. Chomel and J. and ime). canimorsus infection should P. The cases have also been reported in persons 50 subtypes associated with human infections years old or more. jejuni (1985) reported in a large series (1200 cases) and C. 1987). and human been associated with dog or coyote bites). Infections in which NO-1 Bartonella organisms may be transmitted to bacteria were isolated appear to be local (i. jejuni. been recently reported (Breitschwerdt et al. and cellulitis. They are fas. 95% Salfield and Pugh. Carithers in diarrhoeic dogs and puppies for C. are the (Brucella suis). and 5% (2) of 42 healthy kittens tested were ated with dog bites. tularaemia (a few cases have major reservoirs of the organisms. or undercooked meat. and C. The most common clini. should be added to the list of the 22 bite victims.. In a cross-sectional study in that 99..e. dogs. diarrhoea and et al. NO-1 infections. methicillin-resistant strains of Staphylococcus Campylobacteriosis has a higher incidence in aureus (MRSA) potentially transmitted AIDS patients than in the general population. Puppies are .. Fifteen (68%) of the strains were that these bacteria could be detected in dogs’ isolated from dog and 4 (18%) from cat bites saliva.. half of them were males. included purulent drainage. 2002). through dog bites is also of concern (Oehler causing severe.. is a leading cause of human enteri- transmitted by dog bites. especially diarrhoeic dogs. cramping. Emergence of unpasteurized milk. C. upsaliensis 19%. vinsonii antibod- lates submitted to CDC have been designated ies were detected in a young girl bitten on non-oxidizer group 1 (NO-1).1% of them had a history of cat contact Denmark (Hald and Madsen. the cheek by a German Shepherd and this tidious non-oxidative Gram negative rods. abscess and cellulitis). can increase ease (CSD) following dog contact have been the risk of acquiring C. 1998). coli 5%). B. 29% (21) and was not supportive for any other animal of the 72 healthy puppies (11–17 weeks old) source. It has been recently demonstrated 39 years). pathogens capable of causing lymphaden- but they were much younger (median age: opathies in humans after a dog bite (Rolain 18. such as brucellosis tis. suggesting that potentially viable (Kaiser et al. Gastrointestinal Zoonoses Other bacterial zoonoses accidentally Campylobacteriosis transmitted by dog bites Campylobacter jejuni. nausea. jejuni (Blaser et al. berkhoffii) have underlying illness. Evidence indicates that contact with infected Reports of human cases of cat scratch dis. cal features associated with NO-1 infections 2007. infection usually occurs following consump- Erysipelothrix insidiosa infection (Abedini and tion of contaminated. jejuni 76%. Most Campylobacter infections in dog and man are caused by C. 1994).3 years) than the female cases (median age: et al. vinsoni subsp. 1997). humans after a dog bite (Duncan et al.. coli infec- Cat scratch disease and other tion does occur. 22 bite wound iso.. 1997). A report from Japan of a infected with Campylobacter (dogs: C. Oliveira et al. can occur in healthy persons with no ing dogs (B. Lester. However. possible case of CSD caused by a dog contact C. and fever (Glaser et al. a Gram-negative enteric Other bacterial diseases can accidentally be organism. and leptospirosis. especially poultry. Of Bartonella sp. increased pain with erythaema and swelling.. A few cases of CSD have been associ. coli. 2009). though C. More recently. often bloody. Prevalence rates of his patients had a cat-contact history and range from 10–30% in healthy dogs to 50–75% 4% a dog-contact history. without severe with species usually found in canids includ- disease. untreated surface water. Following receipt of a Several human cases of Bartonella infection bite wound. 2009).. 2007). According to Margileth (1993). made. 2010). 1978. et al. 2010. upsaliensis has also been Bartonella infections reported to cause gastroenteritis in humans. Food animals. Dogs and Bacterial Zoonoses 69 CDC NO-1 suggests that dogs could also play a role in human Bartonella henselae infection (Tsukahara Between 1974 and 1998. 1987). and autumn sea. 2008). particularly younger animals. jejuni in the are subclinical. tive on bacteriological culture for Salmonella ture of faecal material on specific media for (McDonough and Simpson. outbreaks of human salmonellosis feeding utensils. mucoid... In humans. 2010). related to exposure to animal-derived pet infected (bleach. In a more recent study of dogs Salmonellosis attending veterinary clinics in the United Kingdom. Rare cases of relapse. 1996). and severe From 1% to 30% of the faecal samples or rectal watery to bloody diarrhoea usually lasting swabs taken from healthy domestic pet dogs. It has been esti- or without anorexia. treats have been reported. and eryth- days).. Salmonellosis is one of of this pathogen supports the hypothesis that the best-known gastrointestinal zoonoses dogs.000 annually reported (Willard et al. Arzt more likely to acquire the infection and show Campylobacter are susceptible to macrolides clinical signs (watery diarrhoea lasting 3–7 and fluoroquinolones (Tan. The true incidence associated with non-clinical shedding include of salmonellosis in dogs is unknown. less than 1 week. Young Campylobacter isolation. was low Salmonellosis is an extremely important zoo- (1. and identification dogs (< 6 months of age) may have higher of the isolate. and dogs may zoonotic infection depends on interrupting shed more than one serotype in their faeces contact with contaminated materials. Salmonella are shed in an important source of C. Finley et al. quaternary ammonium com. colitis. Hands should be rare (Tan. and pet electrolyte therapy) is recommended for most treats of seafood origin (Behravesh et al. Risk factors Green and Schantz.. shedding the organism. 16. transmission animals should be isolated from other ani. was 38% with C. 1987). Younger dogs were more likely many other species of mammals. and septicaemia have been reported. jejuni. and States. the most common Campylobacter sp. upsaliensis infec. 1996). jejuni for gastrointestinal tracts of humans. Most strains of were significantly more likely than control . Infection can also occur after contact romycin remains the treatment of choice for with healthy dogs which are intermittently C. However the prevalence of transmission amongst animals or between C. age. It is estimated that approximately 6% of enteric campylobacte- riosis is transmitted from pet animals (Saeed et al. involving pig ear pounds). headache. pet’s toys. Case-households for severely ill individuals. upsaliensis and the high prevalence birds and reptiles. associated with disease in humans.to 7-day course of diarrhoea with occur worldwide every year. abdominal pain. the clinical picture of vomiting are not commonly submitted for Campylobacter infection is an acute onset of culture (McDonough and Simpson. and the remainder. Faecal shedding of C. However. In Canada and the United washed after handling the pet. upsaliensis accounting bacilli which are capable of colonizing the for 94 (98%) of the isolates. the faeces. The diarrhoea may be salmonellosis cases in the United States are watery.. and vomiting mated that 1% of the 40. Symptomatic treatment (fluid and treats. Infected dogs may associated with companion animals (Stehr- not show clinical signs of disease. are ubiquitous Gram-negative spp. antimicrobial therapy being reserved 2010. millions of cases show a 3. and premises should be dis. 1987).B.. the prevalence of Campylobacter Salmonella spp. thus the most common mode of tion for humans. nosis with broad economic and public health In dogs. or bloody.70 B.. symptomatic puppies usually ramifications. Control and prevention of prevalences than older dogs. beef steak patty dog treats. may be (Willard et al. as it is high-density housing. fever. of hospitalized dogs were found to be posi- Diagnosis of infection is based on cul. 1997). of Salmonella species from dogs to humans is mals and from children. and 21. not a reportable disease and most infections sonality. 1997). Furthermore. faecal samples dog is age dependent and peaks in the 1st of dogs with clinical signs of diarrhoea and year of life.J. Typically. jejuni infections.7% of dogs boarded in kennels. Infected (Willard et al. Chomel and J.5% arthritis. fever. 1993).2%) (Parsons et al. 1987). and C. dogs. but also to carry C. patients. animal and human is the faecal–oral route. mucoid diarrhoea. recently purchased specific brands of dry pet with serotype 0:3 accounting for 17% of the food (Behravesh et al. but of limited value in sions. very limited and the pathogenicity of Y. their stool are asymptomatic.. dogs shed the organism for clinical signs. infant cases was significantly associated with data on clinical manifestations have been feeding pets in the kitchen. should isolated from the child and three puppies. dehydration. especially in children. period of shedding. Because of their close contact with humans. was charac- Diagnosis of the infection in dogs.. An outbreak of McDonough and Simpson. and possibly septicaemia.. matic. holds. 2010). possibly infected from an asymptomatic dog ics have been shown capable of extending the in France (Hurvell. 1994). 1981). Similarly. enterocolitica enteritis involved 16 of 21 per- gastroenteritis with fever. Main 4. Dogs and Bacterial Zoonoses 71 households to report dog contact and to have isolated from dogs. vomiting. helpful in humans. after an incubation of 3–5 days. enterocolitica have been Mortality is usually low (< 10%). severe on culture of faeces or rectal swab. infection may be asympto- disease (Willard et al. occurred (Gutman et al. diarrhoea (69%). 1987. In humans. Although Yersinia enterocolitica has been dogs. appendectomies and two deaths. 1987). Treatment is usually sup.. 1996). which led to two exposure to infection. 1973). mucoid stools in bitches. Extra-intestinal manifestations include cutaneous lesions. vomiting (56%). and it was readily transmit- include diarrhoea. in humans and animals is mainly based on ervoirs for human infection with Yersinia culture of faecal materials. acute gastro-enterocolitis presents with fever.. as antibiot. fever. phar- lows identification of human cases in the pet yngitis (31%). enterocolitica isolates (Fantasia et al. and identification species. In an experimental causes clinical signs mainly in young pup. often fol. headache (18%). infection of dogs with Y. be recommended. and triggering systemic In humans. abdominal pain (62%). arthritis. involved a 4-month-old with pets or failure to properly wash their child and puppies born a few weeks prior to hands after handling animals. Kapperud. 1973). once it had been introduced into the house- even if the dog appears healthy. Salmonellosis 1981. or ageing dogs. 1987). when necessary. The same serotype 0:20 was and antibiotherapy. abdomi. enterocolitica biotype pies. Such suspicions were based on the of the serotype should be performed when isolation of the human-pathogenic serotypes a pet origin is suspected. Only a few dogs may have intermittent diarrhoea for up outbreaks have been documented where the to 3–4 weeks and can shed Salmonella in the likely source of human infection may have stools for up to 6 weeks (Willard et al. ente- Most adult dogs shedding Salmonella in rocolitica in dogs is still uncertain (Hurvell. Recovering published (Willard et al. especially following abortion reports of diarrhoea or bloody.. up to 23 days. Young chil. Confirmed salmonellosis sis. vomiting. malaise. and possible vagi. Strict hygiene the child’s illness. Limited nal discharge. Serodiagnosis is 0:3 and 0:9 from dogs and cats on several occa. based terized by fever (87%). Prevention of infection is based on . seroptype 0:3. ing salmonellosis from either close contact also in the United States. ted between dogs. and abdominal Yersiniosis pain. The acute phase lasts 4–10 days. clinical sign (Fenwick et al.. person-to-person transmission had dren are more likely to be at risk of develop. 1993). 1994). United States (Gutman occurs within a few hours to 2–3 days after et al. Illness among Y. after an incubation of 4–10 days. sons in four related and neighbouring fami- nal pain. in dogs caused by Y.. and watery to mucoid diarrhoea lies in North Carolina. In clinical cases. pregnant animals. The illness. sometimes up to 30%. despite the absence of any anorexia. member without a known focus of exposure The sequential onset of disease indicated that. The source of infection was suggested to or undiagnosed gastroenteritis in a family have been a bitch and its litter of sick puppies. should prompt a testing of the house pet. Another case. Y. and leucocyto- owner’s family. been the family’s pet dog. a child was reported to have been portive rather than antimicrobial. Diagnosis pets have been suspected as possible res. dogs. Immunocompromised persons dogs. and use of disinfectants (Willard et al. Antibiotics of choice for treat... 2011). tory bowel disease.. These organisms colonize involved in the highly contagious Kennel the gastrointestinal tracts of several mam- Cough syndrome.. 2004). in association with Bordetella bronchiseptica infection the spread of the AIDS epidemic. Thomson rium. 1996). M. cinaedi may be with ceftazidine and ciprofloxacin cleared all zoonotic. chiseptica is a Gram-negative coccobacillus commonly isolated from the respiratory tract of various mammals. Helicobacter and their dogs should restrict their attend- species have been involved in human peptic ance at any dog gathering. H. The increase in human cases of tuberculosis worldwide. causing mainly sons. its early . heilmannii-like infection on biopsy sam- ples from these dogs with sequences identi- cal in the boy. However. bronchiseptica in their pharynx. 1994..J. More than 70 cases of human et al. 1991). such as H. Woodard et al. Dworkin fomites.. bronchiseptica vaccinations. 1995). 1995. 1995. 2009). Chomel and J. 1995).. enteritis. Arzt standard hygienic measures. It is one of the infectious agents least 18 species. infected by his pet dogs (Duquenoy and Le and other mycobacterial infections Luyer. pneumonia with interstitial infiltrate is the Some helicobacters. 1910). as these dogs Helicobacter spp. However. can still be potential carriers of the bacte- McDonough and Simpson. Chronic vomiting and subclini- cal gastritis are the main manifestations of Tuberculosis (TB) caused by Mycobacterium dog infection with Helicobacter (McDonough tuberculosis is certainly a rare disease in dogs. such as quick i nfections in immunocompromised individu- removal of faeces.. bovis. and a child with enteritis.. heilmannii. bronchiseptica have been ment of Y. 1994). malian and avian hosts (Foley et al. canis.B. intranasal H. suggesting that the boy was Mycobacterium tuberculosis. 1999). such as dog shows ulcer and neoplasia. canis respiratory symptoms in one case (Decker was from the faeces of healthy and diarrhoeic et al. and Simpson. heilmannii) which caused proven case of B. (2010) reported a culture- hominis (now H. enterocolitica are aminoglycosides reported (Redelman-Sidi et al. but will not eliminate it. A case of a 12-year-old boy ing in a household with her dogs who had presenting with chronic gastritis caused by recently received live-attenuated. There is potential for Bordetella bronchiseptica infections have been infection of pet dogs. 1996). bronchiseptica pneumonia gastric disease in both that was eradicable in an immunocompromised host resid- with treatment. Because canine tuberculosis often is the pneumonia and upper respiratory tract marker of the disease in humans. Treatment lorum. is of major public health concern. vaccination of dogs with live et al. Dogs may be healthy Helicobacter infections carriers of a small number of B. 1999). Household pets could Vaccination of the dogs may help reduce such serve as a reservoir for the transmission of a risk. It was first described in 1910 as a respiratory tract pathogen in dogs The bacterial genus Helicobacter contains at (Ferry. especially those owned reported in several instances in humans by homeless or economically impaired per- (reviewed by Ford. pul- main clinical feature (Ford. infection due to B. The original description of H. most often resulting from a human source (Erwin et al. as endoscopic examination revealed H. In the few human cases. to humans (Stolte et al. B bron- and trimethoprim-sulfamethoxasole. the infected dog can become the source of other human Zoonoses of the Respiratory Tract infections. heilmannii was associated to his two pet B. washing of hands and als (Ford.72 B. 1987). Gisel et al. and H. (1994) reported the transmission from a attenuated strains may be a source of human pet dog to a 12-year-old girl of Gastrospirillum infection. and inflamma- and boarding kennels (Angulo et al. H. None of the 447 dogs test is not very reliable in the dog. dogs. tested had antibodies... or and from dried placenta following parturi- cutaneous lesions. especially Nova Scotia (Marrie et al. Williberg et al. from tick faeces deposited on animal skin tive aerosols or contact with urine. 1996). tuberculosis-infected dog results from infec. antibodies were present in cattle. The use be infected by M. Such results could picion of a human case of tuberculosis in a be associated to the lack of tick infection in household where pets are present. but (Erwin et al. and in urine for 2 months. bovis by consumption of of PCR has brought major improvement in raw milk. a reported Infection in domestic and wild carnivores cause of a wasting illness in patients with has been reported from various areas of the AIDS. burnetii is maintained by a wildlife– entry via the skin and wounds. 1985). such as nodules and pyo. bovis more commonly induces Q fever a digestive form of tuberculosis. multidrug-resistant strains. In et al. tuberculosis. (1980) showed a 53% antibody ness. was isolated from a cervical lymph world. is clini.. of human infection. Infection of dogs probably responsible for the transmission of with other Mycobacterium spp. 2004. tuberculous lesions resemble Caused by Coxiella burnetii... . where after the death of the animal and microbiologi- bovine tuberculosis is still enzootic. histopathology is performed usually tious sputum. infection through tick cutaneous signs. as the skin cats (24. it with acute onset of a respiratory distress was found that a high prevalence of Phase II syndrome (Kiehn et al. Dermacentor.. burnetii infections the most likely result of M. 1992). bites has been reported for various species.. dogs can cal diagnosis requires several weeks. in immunocompromised patients. saliva. Q fever is mainly sarcomatous lesions.. the isolation of the were recently described in the United States bacteria by culture (Aranaz et al. Any sus. Following dogs. 1996). making faecal excretion from affected Rhipicephalus. genavense. Dogs and Bacterial Zoonoses 73 recognition in dogs is essential (Clercx et al. 1996). burnetii has of the dog. Highly infectious dust M. are not specific. C.. tuberculosis caused by should be destroyed and not treated. organism (Aranaz et al. should lead to the clinical examination laboratory-induced infection. Infected dogs infected cattle. In dogs. Human contamination from a including humans. as diag- M. and coughing. 2004). rather than the typical transmitted to humans and other mammals tubercles. However. as caseation is rarely seen (Clercx through inhalation of infectious particles. In Nova Scotia. 1992). such as fever. and from tracheal tissue from a parrot prevalence (agglutinin). more commonly and reliably PCR on bron- Dogs get infected by infectious aerosols from choalveolar lavage (Hackendahl et al. and Amblyomma ticks are dogs a possible zoonotic risk. A few cases of human-to-dog infection appropriate specimens. Atypical mycobacteria often gain nature. clinical signs. granulomas. or possibly raw meat or offal from the diagnosis of canine TB and reduces to affected cattle. Hakendahl et al. C. C.1% of 216 cats). et al. and vertical transmission animal infections may be a potential source (transovarial and transstadial) is common. The primary reservoir hosts for However. burnetii among dogs and wildlife (Hibler their zoonotic potential is still questioned. In dogs. Unfortunately. is rare and C. been the histopathological examination of 1992). Alimentary tuberculosis is tion are major sources of C. Infection by M. which was reported to account nosis is often late and treatment lasts for sev- for more than 65% of dog cases in France more eral months. The most consistent methods for been demonstrated in the blood of cats for the diagnosis of tuberculosis in dogs have up to 1 month. In developing countries. and so cause tick cycle. bovis infection in in these animals and humans. In a survey of 1040 dogs in California. 2004). the tuberculous owner or by sniffing infec.. with the great risk of selecting than 30 years ago (Clercx et al. However.. but also in Diagnosis is a complex task. weight loss. It may be a potential risk for a few days the time for identification of the dogs living on farms that have tuberculosis. node from a dog with severe hind-limb weak. 1985). M. burnetii are ticks. cally characterized by a pleura-pneumonia. In a survey performed among Australian sure to an infected parturient dog. dogs from having close contact with sheep. but is rarely performed for tinguishable strains in humans and pet dogs safety reasons in the laboratory (inoculation and cats in the same household. and regression tree analysis clearly close contact between dogs and cats and their isolated equine veterinarians as well as dog owners. embryonated eggs. at the time of the puppies’ birth. who were present in the room human isolates were identical. burnetii Methicillin-resistant Staphylococcus was isolated from the dog’s uterus. became sick 10 days later. products available only in very specialized laboratories. ism are found in the products of conception. Six of the seven family members had dog was treated (Mayer and VanOre. sheep. 2011). sweats. burnetii. recurrent group A beta-haemolytic became ill with headache. it was strongly suspected that the dog was responsible for the outbreak. tissue cul. ELISA. Because of the controls). as well as identification of indis- of C.... confirmed the canine and The children. abnormal chest X-rays and a fourfold or more Canines being reservoirs of human pharyngitis rise in Phase II antibody titre to C. one was stillborn and two died within haemolytic streptococci isolated from both the 1st week of life. The pups were born the patient and the dog. Preventing farm Organisms of the genus Brucella are small. the dog gave birth to (Abbott et al. but farmers hav- the placenta of cattle. molecular analysis. In this outbreak. burnetii in the house. or microagglutination.J. important. 2009). that interspecies transmission of MRSA is tures). by phenotypic and under the bed of one of the family members. Characterization of the pups. or cattle is difficult. especially in dogs. It was seropositive and C. burnetii is still controversial (Wilson et al. No specific study Zoonoses of the Genito-Urinary Tract has been conducted on treatment efficacy in domestic dogs and cats. aureus (MRSA) Q fever pneumonia developed in all three members of one family 8–12 days after expo. seven members of a family from New Brunswick In one report. and cat practitioners as groups at increased mals for the presence of C. (1991) reported an outbreak in a family after exposure to a deer and infected Streptococcosis pregnant dog. ing Q fever outbreaks in their flocks or herds In several instances. 1995). small animal practi- birth to four puppies that all died within 24 h of tioners had a 4. Laughlin et al. Similarly. In late November 1989. non-motile. and a mild non-productive yngitis was not eliminated until the family cough. fever. One could consider PCR on biological possible (Faires et al.. One week later. The high prevalence of concurrent MRSA Diagnosis of Q fever is based on culture colonization. 1983). Tick prevention and control is also vores. but it is likely that Brucellosis tetracyclines and chloramphenicol would be effective. myalgia. which gave veterinarians in 2009. hold environment (Williberg et al. and goats. suggested of guinea-pigs.. 2010). 1996).74 B. human infections should be aware of the risk associated with resulted from exposure to parturient carni. their pets. streptococcus (Streptococcus pyogenes) phar- fatigue. A case antigen with immunofluorescent antibodies of apparent transmission of Streptococcus equi (IFA). A detailed history revealed that one subsp.. as in humans. Gram-negative coccobacilli capable . Diagnosis is mainly based on serology using IFA. complement fixa- tion. 1980). pets can be considered as sentinel ani.9% prevalence (fivefold that of birth (Buhariwalla et al. risk of carriage of MRSA (Jordan et al.B. Chomel and J. as high concentrations of the organ. zooepidemicus from an infected dog to a family member shot a deer in early November handler who subsequently developed severe and some of the deer liver was fed to the fam- systemic infection was recently reported ily dog. Arzt The organism can be isolated frequently from goats. B. Live-born puppies infected in utero do sis. canis antigen mit B. 1992). gentamycin. Man pies which had close daily contact with the is an accidental host. cells.. Infection of dogs with B. infection is in the dispersion of these organisms between largely asymptomatic and often remains unde- farms. most developed countries. studies (Forbes. meningitis. 2010). by colonizing the placental epithelial food-borne disease caused by Brucella meliten. as many as 3% of vars within the 23 serogroups of Leptospira treated patients may die from endocarditis or interrogans (Andre-Fontaine et al. and play a role Walker. has been reported in 50% of patients The etiological agents of leptospirosis (Rousseau. transmission from cattle to dog by ingestion A diagnosis of brucellosis can be made of infected reproductive tissues. and Walker.05 per 100. 1992). Transient mission between canids and humans were lymphadenopathy and fever are occasionally L. B. such as Hawaii for Symptoms of B. Human infection by B. but at least 30 human cases have been Leptospirosis reported (Lum et al. Occasionally contamination. cattle. as serological tests for diag- zoonotic potential of B. canis infection is characterized ease in humans and dogs. B. specific B. splenomegaly.. canine outbreaks caused by . reported from the tropics. not usually survive to weaning (Carmichael The most common source of human infection and Greene. but human cases are more frequently undiagnosed if culture had not been positive. canis causes embryonic or foetal death. including discospondyli- has been reported in experimental and field tis. as seen in California (Chomel et al. abortus to naive cattle. canis. Leptospirosis has a worldwide distri- diagnosis and the infection would have gone bution. where the average annual are largely non-specific and include fever.08 per 100. of abnormal spermatogenesis (Johnson and ing B. dog. an outbreak involved six persons (three children Leptospirosis is mainly a water-borne dis- and three adults). sheep. In the pregnant bitch. 1992). Though most cases respond belong to the more than 200 pathogenic sero- well to antibiotic therapy. canis is transmitted primarily rifampin (600–900 mg per day) orally for 4–8 by ingestion or inhalation of aerosolized post. and a bitch and three pup. headache. Additionally. detected in early stages of infection (Johnson More recently. abortus and B. ease and rodents are major reservoirs. melitensis. which is cline and an aminoglycoside (streptomycin. swine. 1994). Septicaemia United States as a whole (Sasaki et al. B. In both genders. weeks (Tan. and various wildlife species. Evidence exists for and draining skin lesions.. the should be used. by either blood culture or serology. The clinical symp. of these serovars are capable of causing dis- In dogs. 1994b). or netilmicin) for 4 weeks fol- 1992. potentially being a source of human tected unless the animal is bred. abortus complications arise. 1997).. 1990). canis infection in humans the United States. Dogs and Bacterial Zoonoses 75 of causing disease in man. abortion material. but until recently by prolonged bacteraemia and reproductive the main serovars involved in zoonotic trans- failure in both males and females. includ.000 population. while it is 0. 1995). uveitis. canicola and L. myalgia. In the male dog. 1985). or Brucellosis in humans is most commonly a abortion. through occupational or recreational expo- toms of the index case led to an erroneous sure.. Dogs can be causes epididymitis and infertility as a result infected by several species of Brucella. pathogenic to humans (Johnson and Walker. glomerular nephritis. 1990). In domestic and lowed by doxycycline (200 mg per day) and wild canids. goats. malaise. In Argentina. 1985). case of serology. Kerwin et al.. dogs Treatment is based on the use of doxycy- are the main reservoir of B. icterohaemorrhagiae (Farr. In the it seems likely that infected dogs can trans. but venereal transmission is also reported (Johnson and Walker. canis is not com- mon. 1992). Conversely. 1993). canis is unpasteurized milk products. 1982). 1985). becoming infected family (Lucero et al. incidence is 1. Many other complications (Rousseau. 1985).. abortus transmission nosis of ruminant or swine brucellosis do not between dog and man appears limited in cross-react with this antigen (Polt et al.000 population for the and anorexia (Lum et al. At present.. Leptospira spp. Infection of an Vector-Borne Zoonoses animal with its species’ host-adapted serovar usually results in a mild disease state and high Dogs are not usually the main source of human likelihood of development of a chronic carrier infection for vector-borne zoonoses. or when petting. The course of infection caused by exposure to a leptospiral agent is largely dependent on host adaptation of the serovar. after an incubation period of Lyme disease is a multisystemic. 10–20%. phlebotomes) into severe acute disease characterized by hepati- the human environment. Laboratory with L. but can also be infected with vari. conjunctivitis. 1994) and in the United States. stitial nephritis. or the urine after caused by L.. Agglutinins commonly diagnosed leptospiral infection in will appear between the 6th and 12th days of humans (Heath and Johnson. as well as dog vaccination. and identified by dark-phase micros- the north-eastern states.B. may be isolated from Recently. 2004). or some and vomiting are commonly seen (Heath and other serovars. and such as PCR or immunoblotting may reduce the skunks. 7–12 days. canicola. an infected dog. but seems to be less sensitive than but is reported to be high. Such individuals represent their role cannot be neglected as they either reservoir or maintenance hosts. exposure to infected dogs and is the most especially micro-agglutination. . dogs may very sensitive to penicillin G and doxycycline. Leptospira spp.76 B. and organ failure (Heath of infection on which vectors feed and further and Johnson. 1999). 10% of 61 leptospirosis cases in the early phase of the disease. canicola and the demonstration of a fourfold rise in antibody L. By the 3rd week. hepatorenal failure. However. Johnson. which usually lasts for 4–7 days. As most illness. or can be a source tis. begin. The specific role of dogs as source time for diagnosis. eral weeks. pomona and L. including ELISA or IFA.. The mortality rate may reach ing from. by the end of Dogs are the natural carrier host for the 1st week. Infection with bring or attract the various vectors that can a non-host-adapted serovar typically causes bite humans (fleas. In dogs. are a differential diagnosis. extent by L. In humans. especially in 21 days. In severe cases. leptospirosis can transmit infectious agents to humans. many cases of leptospirosis have the patient’s blood or cerebrospinal fluid dur- been reported in dogs in the United States ing the 10 days of infection. grippothyphosa. and shedder state. which are the most effective antibiotics in dogs tial carriers and shedders of all serovars. Prevention is humans over a 20-year period resulted from based on rodent control and exposure reduc- pet contact (Meites et al. grippothyphosa have been misdiagnosed as influenza. jaundice and renal failure may L. 1994). L. haemolytic crisis. be infected by other serovars. fever. However. especially when administered in California. usually associ- isms in their urine for up to several weeks. range from an acute septicaemia with haemo- lytic anaemia. Arzt L. Human infection serological diagnosis (Levett. or to Lyme borreliosis milder forms with chronic nephritis. 1994).J. more likely to be racoons. In and humans. automnalis. ticks. opossums. Several serological tests have been devel- suspicion of leptospirosis is often ruled out in oped. often by spirochetes of the genus Borrelia (Levine. zoonotic disease associated with infection cal infection or anicteric febrile disease. uncontrol- lable vomiting and bloody diarrhoea. ated with severe glomerulonephritis or inter- Humans can become infected through lick. to a subacute form with fever and jaundice. phase. levels of bilirubin is observed. nausea. Chomel and J. Recent molecular techniques. 1994). titre. and to a lesser headache. most persons will have a subclini. australis. The reservoirs are copy or culture. icterohaemorrhagiae is associated with diagnosis is still mainly based on serology. In its initial febrile reported in Europe (Andre-Fontaine et al. and be poten. myalgia. icterohaemorrhagiae in developed countries. as culture may require sev- of human infection is not well quantified. A specific diagnosis is usually based on dogs are vaccinated against L. severe icterus with high ous other serovars and will shed these organ. tick-vectored. tion. 1989). Prospective work in voir in that region (Lane et al. dog is the potential that contact with canines reliable incidence data are not currently avail. Rhode Island. and US territories. All three stages an estimated Lyme disease incidence at 86 to of ticks can be found on humans and domestic 200/100. In the north-eastern United States.4/100.074 vectors rather than as reservoirs for the spi- cases of Lyme disease was reported to CDC by rochete. become infected.6/100. 2009). In at 10/100. naive mals (Mather et al. 1999–2000 established the estimated incidence the host range of I. New Jersey. Rather. of Columbia. During this 15-year 1995). and Wisconsin). 1989. 1995). for perpetuating B. 1993). suggesting that ticks act as 1999). 1991). scapularis. 1994). it health departments in the 50 states. pacificus is the vector responsible for spread- reliosis (0.931 cases in 2006.. Mice generally become infected when period. Such ticks are then capa- ent on a wildlife reservoir and a transmission ble of infecting other vertebrates including . Delaware. to 19. burgdorferi in the different drome was soon recognized to be similar to geographic regions in which Lyme disease erythaema chronicum migrans and acroder.. burgdorferi has been demonstrated in several ted by I. the District has been shown that the white-footed mouse. Borrelia burgdorferi is the etiological and north-central United States I. tracting the disease... scapularis is agent of Lyme disease in the United States. as Lyme A major concern of any zoonosis of the disease is not a reportable disease in animals. 1993). can be found infected). scapularis feed Pennsylvania. neotomae is narrow.000 inhabitants and neuroborreloisis animals (Kazmierczak and Sorhage. Several ticks of the genus Ixodes matitis chronica atrophicans. Lyme borreliosis is mainly transmit- B. Adult I. burgdorferi infection to other species higher in certain regions. Barbour and Fish. I. I. is the primary reservoir count increased 101%. New York. from 9908 cases in 1992 of B. B. so of Lyme disease (9.000) in France. ricinus is the main vector (Lane et al. Though different animals and vectors are responsible the name Lyme disease was new.. Connecticut (Spach et al. primarily on white-tailed deer (Odocoileus Incidence was highest among children aged virginianus).000) and of neurobor. while in the Pacific ated with borreliosis in Europe (Saint-Girons states transmission is primarily via I... The disease was first characterized vector. burgdorferi in Ixodes ticks is only 1–5% occurring in children < 14 years of age (Sood. In northern California the life 5–14 years. the primary reser- administrative districts. a total of 248. 1992). burgdorferi in the environment is depend. Fish. burgdorferi (Mather et al. burg- not normally include humans or domestic ani. the Borrelia infestation rate of taining the spirochete in the dusky-footed Ixodes ricinus is 7%. Lyme disease is the most reported cus (of which 1–6% are infected). ricinus (Genchi.000 (Blanc. wide range of tick and vertebrate hosts. the syn. 1993.. The annual Peromyscus leucopus. 2008). and 53% of all reported cases cycle of B. In Europe vector-borne disease of humans in the United I. States. such as Alsace. Incidence was ing B. will increase the likelihood of humans con- able for wild and domestic species. maintenance ticks that feed on infected dogs are likely to of B. 1991). the main vector (more than 50% of the ticks while B.. disease entities have been demonstrated to be competent in recognized in Europe as early as 1883 (Levine. Thus. Studies have indicated The enzootic cycle of Lyme disease does that dogs are competent reservoirs of B. Levine. transmitting Lyme borreliosis. 1992). in that it is capable of infecting a of an outbreak of arthritis near Old Lyme. Lyme disease is common in children. with wide disparity between wood rat (Neotoma fuscipes). Dogs and Bacterial Zoonoses 77 1995). 1991. neotomae is responsible for main- For comparison. (Lane et al. dorferi (Mather et al. Transovarial passage with about one-fourth of all reported cases of B. Massachusetts. is endemic. ing (Genchi. The infection mammalian and avian species (Barbour and rate in these ticks varies from 4% to 40%. pacifi- et al. Infection with Europe. with including humans and dogs. garinii and B. 1993). acquire spirochetes during their larval feed- Maryland. However. which states (Connecticut. afzelii are also associ. burgdorferi often involves two tick occurred among males (Bacon et al. However. Levine. burgdorferi is exceptional amongst in the mid-1970s during an investigation Borrelia spp. species. 1994). In the eastern 1995). 93% of cases were reported from 10 fed upon by nymph stage I. Thus. During 1992–2006. Minnesota. and animal use. burgdorferi infection. Other symptoms that occur with (Barbour and Fish. minimized by wearing long-sleeved shirts and diac. Tick-infested areas should be and Sorhage. increased dogs and humans is by vaccination. exposure can be a variety of dermatologic. and fatigue. Chomel and J. while the others are ent. burgdorferi in the environment detected in the early stages or appears refrac- (Lindenmayer et al. Detection of IgM is investigated in early the human environment. Leukocytosis. It is based on an enzyme immu. is often accompanied by muscle pain. and cardiac disease (Kazmierczak exposure to ticks. stood. Tick repel- 1989. ment with doxycycline (100 mg × 2 per day) body to B. common in humans. When travelling In humans. A ‘two-step approach’ has been widely Ehrlichiosis/Anaplasmosis adopted and has improved the specificity of the diagnosis. whole-organism bacterins. renal domestic animals relies largely on minimizing lesions. uveitis. 1995). and in diameter) or laboratory confirmation of carefully remove them as soon as possible after B.J. head. burgdorferi in dog populations in or amoxicillin (2 g × 3 per day) orally (per os). menin. some individuals are unable to overcome miology of human Lyme disease. including acute onset of fatigue. CNS disorders. long pants tucked into one’s socks. 48 h of attachment has been shown to signifi- nomonic when it occurs. Chronic arthritis has use (Barbour and Fish. 1991). In addition to vector control. obligate intra- followed by an immunoblotting assay (Western cellular bacteria of the family Rickettsiaceae . In the early stages of the disease. burg. burgdorferi from an infected tick (Shih and 1989). 1993). with nervous-system involvement being recombinant vaccines based on either OspA more common. dogs in the United States including inactivated tions of Lyme borreliosis are slightly differ. 1995). burgdorferi may experience chronic peripheral nervous system manifest some of the clinical signs which are and CNS abnormalities including depression. Borreliosis is resolved in increasing dog owners’ exposure to B. and Intravenous ceftriaxone (2 g per day for 2–3 convenient measure of the potential risk to weeks) may be indicated if the infection is not people of B. 1993). been reported in up to one-third of German children with Lyme arthritis (Sood. and memory loss for recurrent lameness. 1993. Risk factors for tory to initial treatment protocols (Steere. Estimates of the prevalence of anti. car. most patients with a 10–21-day course of treat- dorferi. Concern gitis. lents and acaricides are available for human tion of Lyme disease includes the character. the manifesta.. dogs are capable of stages of the infection. B. lower frequency include generalized lym. Lyme disease manifests with in areas of high tick density. lethargy. The CDC case defini. Prevention of Lyme disease in humans and phadenopathy. 1999). Diagnosis is mainly based on serological assays.78 B. and at least one of the contact (Barbour and Fish. 1995). 1989. the other method of preventing borreliosis in ache. Levine.B. rheumatologic. and inap. Erythema migrans is virtually pathog. and haematuria currently various vaccines available for use in may also occur. Organisms of the genus Ehrlichia and noassay or indirect immunofluorescence assay Anaplasma are pleiomorphic. especially facial palsy. and are more about residual pathogenicity has precluded common in children (17–38% of cases) than development of whole-cell vaccines for human in adults (Sood. fever. For reasons that are poorly under- rectly illuminate certain aspects of the epide. and neurologic abnormalities (Steere. 1999). sleep disorders. but is only detected cantly decrease the likelihood of transmission in approximately 60% of patients (Steere. These patients may Dogs infected with B. Kazmierczak objective clinical signs of the disease (CDC. Massachusetts offers a sensitive. and/or OspC proteins (Levine. avoided whenever possible. There are RBC sedimentation rate. 1993). reliable. Levine. Arzt humans. Humans should inspect them- istic erythema migrans (EM) lesion (> 5 cm selves and their pets regularly for ticks. months to years following the initial infection petance. EM Spielman. 1993). burgdorferi infection. In Europe. Removal of ticks within 1990). of B. and polyradiculoneuritis. canine seropositivity may directly or indi. 1993). and Sorhage. By introducing infected ticks into blot). . lethargy. the cause of canine monocytic tropical and subtropical regions (Eng and ehrlichiosis. caused caused by an organism closely related to by E.. 1991). myalgia. 2010). Dermacentor uneventfully. The main vector of eral parts of the south-eastern United States. Anderson et al.. 1971) and has now known as Anaplasma phagocytophilum been reported since then from dogs in sev- (Nicholson et al. depression. was first described in a dog E. ewingii is the Lone Star tick. formerly and Giles.. . develop weeks to years later. 1998). myalgia... 1996). 2010). horses. has been described throughout most et al. From stage characterized by persistent haemato- 1986 to 2006 more than 2300 human cases of logical abnormalities and high antibody titres HME have been reported to the CDC. to induce an E. has also been reported (Perez Giles. and weight loss. scapularis in the mid-western In dogs. 1999). chaffeensis (Anderson E. rodents. One of the human ehrlichioses and anaplasmosis is sup. 1986). all four patients had been exposed to eastern and upper mid-western United States ticks and had had contact with dogs shortly (Ismael et al.. with fever. patient’s dogs had asymptomatic infection. Human fatalities can nomic determination based on 16S rRNA occur. and reduced platelets. Dogs and Bacterial Zoonoses 79 that parasitize the phagosomes of mononu. This chronic cytic ehrlichiae were discovered in Minnesota form has a high fatality rate attributed to and Wisconsin (Bakken et al. anorexia. canis. canis. chills. and for E. canis (Codner and Farris-Smith. 1996). and the dog tick. In dogs granulocytic ehrlichiosis in dogs. headache. 2010). 1994). canis-like human ehrlichiosis was actually tunistic infections (Nicholson et al. This infection is mainly trans- et al. was reported to cause human illness in four depression. another agent causing mitted by Rhipicephalus sanguineus. caused by subsequently named E. canis infection and responds to treat- Dumler. Evidence of human infection of the world but is particularly prevalent in with E. Finally. Since first identified. In 1986. equi and E. ported by reports of natural infections with suggesting that dogs could act as a reservoir the same species in dogs. it manifests. 1999).. 1999). reported to the CDC.. some progress to a subclinical variabilis (Walker and Dumler. elevated liver function enzymes.. from the south-eastern and south-central Chronic ehrlichiosis. headaches. gene sequencing led to the discovery that and usually in association with other oppor- E. Though most dogs recover americanum. phagocytophila (Chen et al. human granulocytic ehrlichiosis (HGE) is Canine granulocytic ehrlichiosis. A. Typical patients (Buller et al. lameness. in the acute phase. Canine monocytic ehrlichiosis. A. topaenia and bone marrow hypoplasia. In 1990. 2010). and reduced platelets. Amblyomma and Giles. anorexia. chaffeensis and nia and hypergammaglobulinaemia (Eng E. more ment with tetracycline (Buller et al.. Human haemorrhages and secondary infections (Eng granulocytic anaplasmosis (HGA). mainly from the north. 1994). ewingii. ewingii.. deer. Dogs lichioses are nearly indistinguishable and are can also become infected with E. canis-reactive humoral reac.. 1990. E ewingii infection is usually milder and north-eastern United States (Walker and than E.. clear or polymorphonuclear leukocytes (Eng In dogs. 1996). 1989). from Arkansas (Ewing et al. HGA agent is I. 1987). a clinically novel form of human monocytic In people. tion (Maeda et al. phagocytophilum is typically characterized lichioses are recently recognized tick-borne by acute onset of fever. The advent of taxo. may canine and human infections with granulo. infections (McQuiston et al. 1991). 1989). characterized by pancy- United States (Ismael et al. Human ehr.. 1989). natural conditions (Breitschwerdt et al. The zoonotic nature of before the onset of symptoms. ewingii.. E. caused by a previously undescribed species. laboratory findings include thrombocytopae- The main vector of E. than 3000 human cases of HGA have been In the series of cases reported by Buller et al. 1992) and symptoms: fever. chaffeensis in characterized by one or more of the following experimental (Dawson and Ewing. myalgia. disease caused by infection with et al. phagocytophilum infection is ehrlichiosis (HME) was described and shown characterized by fever. mainly to E. Dogs are likely to contribute to the Human monocytic and granulocytic ehr- enzootic cycle and human infection. (1999). although reportedly in <1% of cases. Oriental spot. dog tick). is southern Africa.. andersoni (Rocky Mountain hepatocellular injury. D. rickettsii. RMSF as 5% for HME and 10% for HGA (Dumler was first reported in 1896 when cases were and Bakken. Treatment of infections caused strated the competence of the wood tick. In South America. each causes a serologi. the American dog tick. and occurs in the United and nymphs feed on small mammals. cally and pathologically distinct disease. and parts of Central adults infest larger mammals. Though the organisms of RMSF in the United States are associated are closely related. 1995). less common for HGA). adults feed on larger feral mammals. when the disease incidence peaks. rickettsii. The disease also exists in Canada. is active primarily in the spring and early ted fever is caused by Rickettsia japonica. 2010). and Spotted fever group rickettsioses south-central states. Amblyomma cajennense (Cayenne tick) infection. the Lone Star tick. Rhipicephalus sanguineus. the identity of the bacteria-like infectious ingly used (McQuiston et al. summer. rickettsii is transmitted by two other tick from asymptomatic seroconversion to fatal species. Chomel and J. anaemia. rickettsii . resulted in the death of salivary glands of feeding adult ticks dur- 23% of infected persons in the pre-antibiotic ing their 6–10 h of attachment. variabilis. mid-western. ley and in the Bitter Root valley of western Human and animal ehrlichioses are Montana (Dalton et al. States. aureolatum (golden dog tick).B. america- num. by Ehrlichia spp. 1985). Case-fatality rates that were as high and A. Howard T. Its larvae Rickettsia rickettsii. Beginning for 5–7 days (Tan. 1998). Mexico. renal failure. et al.80 B. 1996. andersoni is the principal vector of Most rickettsioses are considered zoonotic. the States. and humans. Ismael particles seen in tick tissues and demon- et al. In Japan.J. The natural history and distribution and Beard. Ricketts first established cence assay. is implicated in human infection. tor of R.. while Rickettsia conorii causes Boutonneuse In the south-eastern and eastern United fever in several Mediterranean nations. and the Middle East the main vector. RMSF is found all over the United States. The severity of the disease ranges R. in dogs is mainly based on Dermacentor andersoni. rickettsii in Arizona and northern brate species including humans and dogs. and elevated serum wood tick). More Rocky Mountain spotted fever (RMSF) is recently. Ismael and Northern Mexico. 1999.. tick species: Dermacentor variabilis (American coagulopathy. disease. disease in the western United States from the Rocky Mountain spotted fever is caused by Cascade to the Rocky Mountains. in acquiring and the use of doxycycline at 100 mg twice a day transmitting the infectious agent. and more recently Rhipicephalus hepatic aminotransferase levels (Walker and sanguineus (brown dog tick) in Arizona Dumler. 1997). 1999. D. 1991). A. hypertension. mainly diagnosed by indirect immunofluores.. pancytopaenia. R... Central America. rash in 20% of the patients (for era (Walker et al. Prevention is based in the 1930s. RMSF started to be reported on the same measures as reported for Lyme from eastern states (Dalton et al. R. Mexico (Nicholson et al. In the eastern Rocky Mountain spotted fever United States. Arzt anorexia. and Spotted fever group Rickettsiae have been parts of South America (Colombia and described throughout the world (Azad Brazil). Mexico. It is known to be HME. 2008). on wild rodents. although PCR assays are increas. McQuiston et al. Its larvae and nymphs feed (Walker and Fishbein. the brown a tick-borne rickettsial disease caused by dog tick was shown to be an efficient vec- R. which affects several verte. 1995). 2010). leucopaenia.. The wood tick and South America. with the ecology of two ticks (Hibler et al. transmitted in the United States by three thrombocytopaenia. 2010). dogs. 1995) have now declined to less identified in Idaho in the Snake River val- than 2% (HME) and 1% (HGA). the largest number of cases being reported from the south-eastern. the most pathogenic of all known The rickettsiae are released from the rickettsial species.. D. Canada. and hypoproteinaemia. but will and scleral injection. Necrosis of skin of the extremities raccoons. 4–14 days after a tick bite. lym- Newhouse. abnormal mental status. the same experiment. all tick tissues can become infected and early 1980s that clinical reports concern- within a 7–10-day period after feeding on ing naturally occurring RMSF in dogs have a rickettsiemic animal. a anterior uveitis. tick species. rickettsii developed increased serum aspartate and alanine a rickettsaemia that was detectable as early transaminases and alkaline phosphatase as 4 days after inoculation and as late as activity. platelet counts do not serve to infect new ticks. horses. subconjunctival haemorrhage. these authors showed the patient suffering typical RMSF has an that a very limited number of ticks became acute onset of fever. Weight loss. The organism can be found in the tick few days.000 cells per ml (normal: nymphs usually do not feed more than once 200. deer. mucopurulent oculo-nasal but transfer through male spermatozoa is discharge. In dogs.000–500. ited to the mucosae. 10 days (Norment and Burgdorfer. rhipicephali or R. enters the infected with R. Larvae has been seen as a complication of RMSF in and nymphs feed on various rodents. the skin. and only adult males feed repetitively.000 egg infec. transmit the infection through the eggs. anorexia. haemocoel. normochro- the level of rickettsaemia is low. and depression can occur within 2–3 Ticks mate while feeding.. Humans are an Neurologic abnormalities. after which they kocytosis (> 20. and non-productive cough are not efficient during mating (McDade and often present. ciated with domestic dogs. 1984). and infected after feeding on inoculated dogs. Larvae and of less than 75. rickettsii when they feed on animals con. 1977). malaise. headache. two non-pathogenic rickettsiae. epistaxis. Usually. prepuce. opossums. hyphaema. and therefore do not contrib. rather than involving life mammals (cattle. such dogs. including the salivary glands and the ova.000). Haematologic abnormalities Newhouse. Symptoms and adults may become infected with of RMSF vary considerably in dogs. vomiting. and then invades all tick tissues. and mild leukopaenia (at before moulting. ecchymoses (only in 20% of the dogs. retmal petechiae. followed 1–15 days after the onset . and focal major vector in Mexico. dehydration. and hyperaemia (lips. circling. sheep. fever (39°C–41°C).000). and rabbits. 1986). whereas The American dog tick (D. These are followed by leu- once before laying eggs. multiplies there. head tilt. as by ticks is limited to the rather short period well as joint tenderness. montana. Abdominal tender- of high rickettsaemia (often 4–5 days only) ness or paralumbar hyperaesthesia can be in the small rodents. 1986). 1985).. Female ticks days of tick attachment (Greene et al. and myalgia may occur. but it is only since the late 1970s occurs. foxes). variabilis) feeds it is in the majority of human cases). Conjunctivitis. mainly on dogs for the adult form. R. rickettsii. coyotes. tive doses of virulent R. The extensive range observed. In In humans. scro- ettsii reflects the generalized feedings hab. Ocular lesions are characterized by as chipmunks. In both humans and dogs.. voles. pinnae. followed by cutaneous petechiae and its of the known tick hosts of R. 1989). and they mic). rhoea. ground squirrels. include anaemia (normocytic. When generalized infection infected. Acquisition of infection phadenopathy. Dogs and Bacterial Zoonoses 81 initially infects the epithelial cells of the No rickettsaemia has been observed in dogs tick midgut. such as vestibular incidental host of the adults of all of these deficits. include increased glucose concentration. retinal oedema (Davidson et al. rick. diar- currently with infected nymphs or adults. Adult female ticks feed onset of fever). is primarily asso. tum). Biochemical abnormalities Dogs inoculated with 1000–10. Haemorrhages are lim- also feed on many other domestic and wild. rickettsaemia lasts only for a ries. 6000–17. Rhipicephalus sanguineus. nystagmus. Uninfected nymphs been made (Keenan et al. and incoordination are ute to the transmission cycle (McDade and also observed.000) with a left shift (normal: die. Serologic information obtained haemocytes as early as 3–5 days after the since the 1930s indicated that dogs could be infective meal. myalgia. thrombocytopaenia. Early skin lesions include oedema of mammals that are seropositive for R. the brown dog tick. and cerebral oedema (Font-Creus et al. conorii failure.B. Arzt of illness by a petechial rash. Mediterranean countries. and subsequently spreads to involve Boutonneuse fever. sanguineus are to be re-emerging in several countries in the principal vectors of human infection. in conjunc. and soles. conorii was The treatment of choice is tetracyclines identified. The habitual reser- are common complications. or areas disease as amplifiers of the reservoir and vec- with high grass. by direct quantitative data concerning susceptibility immunofluorescence on skin biopsies. also called Mediterranean the trunk.. micro.. 2008). ELISA. Senneville et al. in a domestic or peri- infection. Testing by presented a severe form of MSF 2 months PCR of 17 KDa antigen has been developed after holidaying on the French Riviera. face. sanguineus taken from a dog. (Ruys et al. the dog ticks ease (Walker et al. 1990). In dogs. Similarly. Caspian Seas. yet there are no to guinea-pigs. dogs seem to play viduals with frequent exposure to dogs and an important role in the epidemiology of the who reside near wooded areas. the pet dogs were found seropositive on detection of both IgM and IgG is also use. or purpuric features. Chomel and J. 2008). An Latin America. or of dogs to this agent. R. (1997) showed dogs that had stayed in Mediterranean coun- that prednisolone at anti-inflammatory or tries and had carried ticks to The Netherlands immunosuppressive dosages. in the last decade in several Mediterranean American Indians. does not potentiate is related to the dispersion of R. and also to the progressive adap- suppressive dose). and people aged 50–69. In 1930. The rash or Boutonneuse fever first appears as macules on the wrists and ankles. per os. American Indians have an increased risk of They also bring infected ticks into the vicinity fatal outcome from RMSF. Acute renal acute infectious disease caused by R.. or chlo. tation of R.. 1993).. Durand and Conseil pro- parts of the United States. Children up to 9 years of age and domestic cycle in urban or peri-urban areas. the Middle East. In South Africa. Breitschwerdt et al. as the infection ramphenicol: 15–20 mg per kg. RMSF also seems Haemaphysalis leachi and R. reported the case of a 53-year-old man who agglutination) (Greene et al. sanguineus. with very high titres. ern areas. later. serodiagnosis based tested. The disease is also endemic in much than 500 reported cases in the early 1990s of Africa.82 B. was first described by cutaneous lesions often develop papular. The frequency of reported increase in human cases has been reported cases of RMSF is highest among males. The US incidence of RMSF cases sion of R. and the Black and to 2288 cases in 2006 and 2106 cases in 2007. especially in duced the disease in man by injecting suspen- Arizona. of humans. may be at increased risk of tor. (1991) by serological tests (IFA. 1994). 2008). reported in The Netherlands.1 countries (Rovery and Raoult. These spotted fever (MSF). Diagnosis of the infection is based Dogs are often considered to be the main on isolation of the agent by inoculation source for infecting ticks. conorii to new tick species such . When three brown dog ful to identify acute infection (Breitschwerdt ticks were found on the dogs a few months et al. Raoult. but is higher in some humans. The increase in human cases tion with doxycycline. When more recently. as voir and dominant vector is the brown dog high as 30% in the pre-antibiotic era. Connor and Bruch in Tunis in 1910. and indi. 1985). has tick.J. these were cultured and R. with R. It is an petechial. which very rarely feeds on declined below 1%. every 8 h. conorii had been transmitted through per os). coagulopathy. a few cases of RMSF were (22 mg per kg every 8 h. palms. It is also the most common rick- the highest recorded levels in more than ettsial disease in South Africa (Rovery and 80 years of national surveillance for this dis. sanguineus by the severity of R. Mortality. Vomiting Mediterranean spotted fever can be seen in 60% of the cases. In It is a seasonal (summer) disease. The reported to the Centers for Disease Control disease is endemic along the Mediterranean and Prevention has increased from fewer coastline. on cell cultures. rickettsii infection in dogs dogs from southern Europe to more north- (rickettsaemia was prolonged at immuno. 4 and 27. sanguineus (Raoult et al. (1998) found that 23. respectively). About 9–15% of the ticks were lar. reticulatus. It tested by microimmunofluorescence and con- is a small reddish ulcer covered by a small firmed by Western blot assays was higher in black scab. The ‘tache noire’ was tors negate the effects of adequate hygiene seen in 73% of the cases. In a study of 227 cases of the population has a low income and more in Spain. Dogs in northern Marseille are more (Rovery and Raoult. presence tion. They indicated that this higher prevalence Fever appears usually 5–7 days after the tick may be related to a greater tick exposure bite and is associated with severe cephalagia. Immature stages reported. Mortality is usu. and 8.5% and 40%. 1992). primary lesion at the site of the tick bite. In northern Marseille. and negatively correlated with other parts of the world.8 (Ruiz-Beltran et al. 100 inhabitants versus 28. 2008). The diagnosis Other common signs were headaches (69%). conorii. at first macular and then maculopapu. 76. For human infec- and lasts about 1 week. positively correlated with average tempera- gested that dogs could be used as sentinels to tures during spring and summer of the pre- monitor the distribution of this zoonosis. they can be rickettsiemic. had antibodies 24.8 per 105 for central and south-eastern In humans. In ceding year. facilities on personal hygiene. which may the northern area than in central and south- last throughout the course of the illness. tion. the brown tick needs to be attached for at of multiple eschars was recently reported least 20 h. conorii without clinical signs. Dogs and Bacterial Zoonoses 83 as Dermacentor marginatus or D. Font-Creus et al. respec- a case fatality rate as high as 32% in Beja. sible that such negative socio-economic fac- lar rash in all patients. A generalized erup. The epidemiology of MSF is determined Dogs are exposed to infection.. isolation of the infectious agent (not done in and splenomegaly (19%). as well as myalgia. tively). Delgado and Carmenes (1995) and ing the spring. due to a higher number of dogs (32. (1992) found that incidence was had a higher seroprevalence. hepatomegaly (44%). 2008).2 per 100. Dogs from generation to generation. It is therefore pos- high fever and a generalized maculopapu. although by the biology of the tick and results in a clinical signs and symptoms have not been consistent seasonal peak. nymphs) are generally the source dogs can carry R. of human contamination during the sum- but they do not transmit it to their offspring. (1993) also reported on the infection. mer. In Marseille area. The monthly distribution of Segura-Porta et al. disease parallels the maximal activity of the respectively. frequently parasitized by ticks (51.000 persons compared with 9. Spain. In northern Marseille.7% versus 3. Raoult et al. was recently reported (Rovery foci. from rural areas or heavily infested by ticks Raoult et al. had significant antibody titre to immature stage of R.2 per 100. (1985) reported a than 25% are unemployed. The frequency of seropositive dogs 1992). However. 1992). The treatment is living in urban areas. a large percentage and Raoult. and joint pain. It is suspected that in the interesting data concerning prevalence of Mediterranean basin lagomorphs could play MSF and prevalence of infected ticks in the the role of amplifiers in the wildlife cycle. In their study. and. Seroprevalence in blood donors.6 per muscular. Seventy-two per cent of the cases were (Teysseire and Raoult.5% of the wild rabbits tested dence of hospitalized patients with MSF was in Salamanca Province.4). while adult ticks are mainly active dur- In Spain.1% of 138 dogs tested. called ‘tache noire’. small rodents upon the number of days with frost during the pre- which infected ticks feed are the amplifiers ceding year. It has been sug.6 and 2. with the two other areas (43. appears the 4th or 5th day of the fever infected in the various areas. Regional lymphadenopathy is often seen. Contact with dogs regular practice) or serologically by microim- was confirmed in 92% of the 170 cases ana. MSF is characterized by a Marseille. eastern Marseille (6. R.4% human cases shows that the apparition of the of 308 dogs and 26. the inci- a sero-survey.4%) than in ally low. Adult (larvae. Parasitized dogs are present in micro- Portugal. based on the use of tetracyclines (Doxycycline . but an increased mortality. of infection is usually performed by either conjunctivitis (32%). R. conorii is transmitted transovarially increased during the summer months. munofluorescence and Western blot assays lysed. whereas rates of 4% up to 16% have been reported in dogs. 1992). 1993). Dogs are not very susceptible to anthrax and nausea.. human cases of plague were associated with ern Africa and Madagascar. dogs may introduce vectors Plague infected with Y. septicaemic. Several other rickettsial spotted between 1970 and 1993. The incubation period ranges from sev. pestis into the human envi- ronment and thereby increase the likelihood Plague. In the dog. Brazil). Barnes and Poland. especially on Chlamydophila psittaci. 1992). In man. but no data are available on the uted to direct contact with an infected domes- role of dogs in their epidemiology. or their carcasses into or around the home..B. caused by Yersinia pestis. disease of rodents in Asia.. infection is most likely to occur as a result of flea bites or Other Uncommon Bacterial ingestion of an infected rodent (Orloski and Zoonoses Eidson. endemic areas. Four cases of acquiring plague from ers. In the United States. 2011). Chomel and J. As with other arthropod- borne diseases. Dogs pose a risk to humans by infected fleas. and enlarged lymph plague is usually a mild disease. skinning wild canids were documented ramphenicol. It is maintained plague bacillus is very sensitive to strepto- in nature by a flea–rodent cycle of transmis. sis/ornithosis in humans. 1997). but tetracycline and doxycycline are sion. psittaci infection is seen most often in exotic thoroughly examined (Orloski and Eidson. Inhalation infection results in cides to kill fleas. 2008. Direct infection of by a moderate fever. central and south. characterized nodes (McGee et al. and enlarged humans from dogs could potentially occur lymph nodes (Orloski and Eidson. South America (Peru. prevalence is less than 1% in pet dogs (Chomel Chlamydiosis et al. 1995) In humans. clinical forms of plague present Anthrax as bubonic. pestis occurs through the bite of et al. but some. In through a bite. tic cat. and 2011. is an obligate intra- 1994a. 1995). with moderate fever. In dogs. of anthrax. usually develop a subclinical or chronic form 1992).. Major concern has been flea bite. some areas of sleeping with a pet dog (Chomel and Sun. raised with the emergence of multi-resistant times from a cat or dog flea. or rarely through inhala. infec. wide range of domestic and wild mammals The frequency with which plague is and birds (Arizmendi et al.. the agent of psittaco- Native American Reservations (Chomel et al. Arzt 100–200 mg per day for 7–15 days) and chlo. lethargy. pet bird owners and poultry industry work- 1995). Gould et al. bubonic plague results from a also very effective. The the western United States. and vomiting (Crook and Tempest. plague antibody prevalence in pet dogs is usually low. pneumonic plague. tion of aerosolized respiratory droplets of It is important that dogs and cats that roam infected animals or other humans (Crook and outside be treated with appropriate insecti- Tempest. In humans. 1994a). mycin. Though 12 cases of fevers have been reported from various parts human plague during this period were attrib- of the world. More recently. lymphadenopathy (buboe). 1992). the form associated with the greatest mortality.J. contact with bodily fluids of transporting fleas and flea-infested animals infected animals. 1983) or in Africa cellular parasite that is capable of infecting a (Kilonzo et al. usually from a rodent flea. Reports of natural and experimentally .. plague bacilli from Madagascar (Galimand tion with Y. is an endemic of humans contracting plague. and lingual oedema. CDC. or pneumonic. pharyngeal eral hours to approximately 1 week.84 B. myalgia. transmitted from dog to human has not been C. no analogous cases were confirmed following interaction with an infected dog (Craven et al. Bolivia. 1994)... In humans. Clinical signs for the bubonic form typically include fever. . psittaci has been isolated in England from introduction of two canaries and a parrot into the faeces of a dog that had ingested the car. The woman had chlamydiosis has not been examined in the stayed on a 106-cow dairy farm shortly before United States. where 9% of sampled dogs were Toxigenic C.. and in Japan (Fukushi four dogs.. and reduced litter size (up to 50% Transmission of bacterial zoonoses from dogs stillborn or non-viable puppies) in a small to humans is rather uncommon.gov. B. Journal of Medical Microbiology 59. and the two The probable role of dogs in the trans- dogs had indistinguishable ribotype pattern.C. K. Seroprevalence of canine Kingdom (Hogg et al. Markey. and should be given to young children who are pharyngeal swabs revealed chlamydial inclu. the household. E. The zoonotic potential vaccination of dogs. removal of ectoparasites. Special attention cence examination of conjunctival.cdc. A. Leonard. et al.. C. Steward. and Waller. psittaci to human was sug- gested in a recent outbreak in Germany (Sprague et al. contact with the pet and its environment. (1997) Erysipelothrix rhusiopathiae bacteremia after dog bite. psittaci antibodies. Y. PCR and sequencing of ompA ampli. two cats. psittaci genotype C. ulcerans was isolated from two of seropositive. Ugeskrift for Laeger 159. Pinilla. S. Acke. bites and by faecal shedding. 1985). the farm dogs and the patient. Additionally.. Cell culture and immunofluores. farm (bulk tank milk and filter. Transmission dog-breeding facility in Germany (Sprague from dogs to humans occurs mainly through et al.. and two guinea pigs). 2009).G.. E. more likely to be bitten by dogs or be in close sions. However. nasal. of dogs and humans may have followed the C. References Abbott. 2009). 1969). and pharyngeal swabs from C. (2010) Zoonotic transmission of Streptococcus equi subsp. Note 1 www. 120–123. Abedini. 4400–4401. A.. S. Dogs and Bacterial Zoonoses 85 induced chlamydiosis in dogs are rare. Chlamydial conjunctivitis has been described Corynebacterium ulcerans in dogs (Krauss et al. serosurveys have becoming ill. There was follow to prevent acquiring bacterial zoon- circumstantial evidence to suggest infection oses from their pet... Khan.. casses of birds known to be infected with the same agent (Fraser and Norval.K. zooepidemicus from a dog to a handler. 2009). 1969).. of the pathogen was illustrated by evidence and regular use of insecticides are important of disease in two children who lived on the preventive measures that a dog owner should premises with the infected dogs. Muldoon. 1988). psittaci infection was reported in four bitches with recur. Conclusions rent kerato-conjunctivitis. mission of C. . milk samples 1987) where 20% of the dogs tested had from eight cows. 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Veterinary Clinics of North America: Small Animal Practice 17. Wilson. and Gander.D.A. Haghighi. R.. Cone..E. and Walker.D. leishmaniasis is found in parts of disease. Reservoir by Leishmania spp. L. Macpherson et al. are most commonly transmit- ted by sandflies (sub-family Phlebotominae). Texas. Dogs. Central giardiasis. Entamoeba histolytica. College Station. eukaryotic be pathogenic to mammals. Notable among infantum. Leishmania spp. Texas. 2nd Edition (eds C. but instead affect a vari. and humans. These protozo.) 93 . Cyclospora cayetanensis. are considered the most important peri- tozoan parasites Leishmania spp. and Giardia intestinalis which causes the southern United States. In the New World (the western hem- sis. vector. L.L. and South America. to be host-specific. Mexico. L.edu ©CAB International 2013. Zoonoses and Public Health. In the Old on these three conditions. chagasi/L. Blastocystis hominis. and southern Europe. which cause leishmania. World (the eastern hemisphere). Snowden1* and Christine M.N. USA. Dogs disease caused by infection with the pro. Africa.1). major. braziliensis protozoans that infect both dogs and humans are known to cause disease in both dogs and are Leishmania spp. Cryptosporidium spp. Of the parasitic protozoans. humans. Of these pathogenic species. mon pathogenic species are often divided ries. only a small into New World species and Old World spe- proportion is associated with disease and only cies based on geographic location. Leishmania spp. College Station. Trypanosoma cruzi which causes Chagas isphere). 6 Dogs and Protozoan Zoonoses Karen F. the Middle East. Budke2 1 Department of Veterinary Pathobiology. and a small percentage of these infects dogs. e-mail:
[email protected]). transmission ans will be discussed in less detail (Table 6. Other protozo. dogs. The presenting clinical manifestations in infected few protozoans that infect dogs do not tend humans (Box 6. USA Protozoans are single-celled. with transmission linked to the geographic Leishmaniasis caused distribution of competent vectors. hosts vary with Leishmania species and geo- graphic location and can include a variety Leishmaniasis is predominantly a vector-borne of wildlife species. leishmania- ans that can infect both dogs and humans sis is found in parts of Asia. Encephalitozoon cuniculi.. and Pentatrichomonas hominis. 2College of Veterinary Medicine & Biomedical Sciences. and L. However. There are domestic reservoir of L. the extent to which * Corresponding author. ety of mammalian species. tropica. The most com- organisms that often have complex life histo.tamu. include Balantidium coli. infantum infection numerous species and subspecies known to to humans. This chapter will focus primarily America. low-grade Faecal–oral. faecal–oral. 2009b diarrhoea immune-compromised cysts individuals) K. 2009 ingestion of cyst-like stage Cryptosporidium spp. 94 Table 6.. abdominal pain oocysts 2010 Cyclospora cayetanensis Little clinical significance Diarrhoea. Multi-organ systemic disease Faecal–oral. probably Low Greene. mucus. commensal asymptomatic. Snowden and C. nausea. fatigue oocysts Sanchez. ingestion of Low Snowden et al. encephalitis. no cyst stage. diarrhoea Diarrhoea. 2010 Encephalitozoon cuniculi Asymptomatic. ulcerative.1. nephritis in immune-compromised spores. ingestion of Low Barr. commensal Faecal–oral. 2009b severe.. Low Bowman.F. Organism Clinical signs in dogs Clinical signs in humans Route of transmission Zoonotic potential Reference Balantidium coli Asymptomatic. Asymptomatic. ingestion of Low Lucio-Forster et al. vomiting. ingestion of Low Ortega and fever. bloody Diarrhoea (usually in Faecal–oral. transplacental 2009 individuals Entamoeba histolytica Asymptomatic. Other zoonotic protozoans associated with dogs. Budke Blastocystis hominis Asymptomatic Asymptomatic. mild to Diarrhoea with blood and Faecal–oral Low Barr. liver abscesses haemorrhagic colitis Pentatrichomonas asymptomatic. diarrhoea undetermined. nausea.M. 2007 hominis gut flora gut flora motile trophozoites possibly misdiagnosed as Giardia . L. Brazil. and L. L.5 million are rarely infected. Syria. New and Old World species of Leishmania spp. braziliensis complex (L. istic infection in areas where it coexists with . guyanensis) L.. and opportunistic microbial infections. Iran. with some individuals having swol- multiply by simple division and infect other len regional lymph nodes. L. This form into promastigotes. Algeria. tropica. mexicana complex (L.1 ulations located in North America (Boggiatto The visceral form of the disease often et al.. develop and multiply form can affect the nasal septum. amastigotes trans. One of the most prominent exam. According leishmaniasis is still unknown (Gavgani to the World Health Organization (WHO). 2011). L. infantum transmission among foxhound pop. Saudi Arabia. and Bolivia. Sandflies then leishmaniasis is a rare form of the disease become infected by ingesting infected cells dur. In sandflies. which or painful. amazonensis. Cats and other domestic species an estimated 2 million new cases (1. aethiopica) L. infantum are actually the same species. The disease can also result in a decrease in the production of blood cells that can lead to anae- Disease in humans mia. The The cutaneous form of the disease is sandflies inject the infective stage (promastig. tropica complex (L. panamensis. and migrate to the proboscis where other parts of the nasopharynx. with about 12 million people currently Leishmaniasis is typically transmitted infected worldwide (WHO. palate. The cutane- they are now ready to infect a new host. chagasi and L. Duprey et al. often resemble a volcano. L. and L.000 disease often more limited in these species cases of visceral leishmaniasis) occur annu- (Trainor et al. with a raised edge Promastigotes transform in these cells into the and a central crater. Colombia. ally. major. braziliensis.. major transmission to both humans and other mam. characterized by one or more skin lesions on otes) during blood meals. 2011. venezuelensis) L. mexicana. and in the gut. that can occur months or years after the heal- ing blood meals. et al. tropica in the Old World. venereal. bleeding. 2002). this form of the In humans. dog ownership is a risk factor for human and immune response of the host. 2010). Visceral leish- a cutaneous or visceral disease dependent on maniasis is becoming an important opportun- the leishmanial species. leishmaniasis manifests as either disease is nearly always fatal. and direct New World. L. The sores can be painless tissue stage of the parasite (amastigotes). Without treatment. While ous form is most frequently caused by L. L. geographic location. New World species L. in ziliensis. ing of a cutaneous leishmaniasis ulcer. Mucocutaneous mononuclear phagocytic cells. 90% of documented. According to the US Centers for horizontal transmission between dogs has been Disease Control and Prevention (CDC). with the course of the cases of cutaneous leishmaniasis and 500..1. Dogs and Protozoan Zoonoses 95 Box 6. 2006). mexicana. and related species in the rare cases transplacental. cutaneous leishmaniasis cases occur in parts ples of horizontal and vertical transmission is of Afghanistan. donovani *L. L. infantum *It is now believed that L. chagasi Old World species L. The sores can phagocytized by macrophages and other types change in size and appearance over time and of mononuclear phagocytic cells in the host. Promastigotes are areas where sandflies have fed. manifests as fever and weight loss accom- panied by an enlarged spleen and liver. by the bite of infected female sandflies. bra- mals usually occurs via a sandfly vector. Peru. peruviana *L. wearing gressive weight loss. 2011). Elimination of seropositive dogs et al. fly bites. with transmission of contrast to visceral disease. Maroli et al. increased prevalence of L.. 1991... cutaneous lesions L.. through PCR methods. and renal fail.. Cutaneous clinical mani. with relapse of the disease common. Lemesre et al. Speciation is available maniasis has been approved for use in Brazil. Otranto et al. also be helpful in achieving a diagnosis. transmission is protection against sand- disease in humans. epistaxis. Subclinical has been considered as a means to decrease infection is common among dogs living in human disease in endemic areas. blepharitis. pro. scrapings. Abranches can be used. The 2007. including ten during the night. biopsies.M. sleeping in have also been reported in dogs with leishma. 2008). This includes avoiding outdoor festations include skin lesions. 90% of visceral leishmaniasis cases devised to assist clinicians in determining the occur in parts of India. or impression prepara- 2001. for dogs. 2010).. well-screened or air-conditioned houses will niasis. tions by microscopy and/or culture in a A commercial vaccine against canine leish- specialized medium. Ocular signs (for example. or immunoblotting can 2002.F. most appropriate therapy.. alopecia. to be outside during these times.96 K. complete clearance of the Leishmaniasis continues to be considered Leishmania organisms is rarely achieved in a public health threat throughout much of dogs. Disease in dogs Prevention and control Canine leishmaniasis typically has clinical The primary means of control of Leishmania signs similar to both cutaneous and visceral spp. Cardoso et al. and Brazil. direct evaluation in Europe (Borja-Cabrera et al. availability of these tests from commercial or fee-for-service laboratories varies depending on geographic location. 2007. In the developing world. endemic regions (Baneth et al. help to decrease the conjunctivitis. and anterior uveitis) chance of being bitten. with limited options in the United States. Several possible predisposing factors help to prevent the possibility of being bit- to development of clinical signs. infantum in canine . long-sleeved shirts and long trousers. Dantas-Torres. use of insecticide-impregnated collars and topical spot-on formulations have been shown to be effective in reduc- Leishmaniasis is definitively diagnosed by ing disease transmission in endemic areas identifying Leishmania organisms in tissue (Alexander and Maroli. have been described (Sideris (preferably one treated with an insecticide) et al. agglutination. ELISA. a bed net breed and age. 2004). According to At least one staging system. Diagnosis and treatment In dogs.. Visceral sandflies are generally most active. has been the CDC. Nepal.. using insect repellent. 2008). Franca-Silva et al. Alternatively. Antimonial drugs con. However. Snowden and C. 2003. via sand flies an important route for human ment.. keratitis. Ethiopia. 2007). Ramos et al. 2006. Bangladesh.. and ure. especially from dusk to dawn.. 2011). infantum from dogs or wildlife reservoirs in humans may heal independently of treat.. However.. In addition. as well as forecast- Sudan. Miro et al. ing prognosis (Solano-Gallego et al. If one has lesions include swollen lymph nodes. 2008).. 2003. Zoonotic potential and public health tinue to be the best line of treatment for considerations both affected humans and dogs (Oliva et al. Serological tests such and several vaccine candidates are under as the indirect fluorescent antibody test. Budke HIV (Nascimento et al. Clearance of lesions independent of infection. Several studies have reported that therapy is not well documented in the dog. when ulcerative or exfoliative dermatitis. and activities. studies from Brazil have shown no decrease in human cases after this control method was implemented (Nunes et al. 1999. . and hosts (people or animals) the Carolinas through Oklahoma. indictiva. 2009). and Columbia. Less commonly. WHO.. Karsten et al. Werneck et al. This parasite is restricted to the west- the genus Triatoma (T.. cruzi. Brazil. protracta. ing to contaminate the bite wound. but human considered potential disease vectors. vectors of T. and other tissues. Yabsley and Noblet. opossums. tors. 2010). cruzi has Kjos et al. Yabsley and Noblet. Members of the Triatominae bug sub- Chagas disease. 2007). or mucous membranes of the mam- ownership of an infected dog have been malian host. gerstaeckeri. In addition. (Hemiptera: Reduviidae). and tebrate hosts including mammals. 2008. 2009. is a vector-borne disease caused blood feeders in all post-egg stages.. Herwalt et al. 2009a). sanguisuga) known as ‘kissing bugs’ or ‘cone-nosed bugs’ and Paratriatoma hirsuta (Kjos et al. T. 1992. regarded as the major route of parasite trans- 2007. T. 2000. only Chagas disease has also been documented species that have adapted to living in or near in Central American countries and Mexico domestic structures are of primary public (Estrada-Franco et al. (Pereira et al.. but only mammals are susceptible to a variety of rodents) have been documented infection with T.. cruzi has also been identified in sylvatic of Trypanosoma cruzi in endemic countries reservoir hosts and dogs in the southern depends on the confluence of reservoirs.. the mammalian host. oral transmission of T. The highest human In Latin America. Texas and in a single habitat. ern hemisphere based on the geographic dis- T.. Werneck et al. and reptiles. 2007). Trypanosoma cruzi.. 2002). cies found in the United States are competent 1986. and are by infection with the protozoan parasite biological arthropod vectors for the parasite. Louisiana.. The usual transmission T. 2006.. T. Gavgani et al. and wildlife (opossum. neotoma. The life cycle is Chagas Disease caused by completed when the triatomine bug ingests Trypanosoma cruzi parasites while feeding on the infected mam- malian host. Similarly. particularly Argentina. ent intracellular amastigote form multiplies intracellularly in the skeletal muscle. cruzi. Although all triatomine species are Bolivia. also been documented in dogs. lecticularia. armadillo. also called American trypano- family (Hemiptera: Reduviidae) are obligate somiasis. Ten of the 11 bug spe- as hosts for the parasite (John and Hoppe. and T. dog density. Walton et al. The extracellular flagellated epi. 2009). The extracellular trypomastigote shown to be risk factors for human disease form is found briefly in peripheral blood of (Acedo Sánchez et al. cruzi transmission is typically based on a bug parts (Pereira et al. skin low socio-economic status.. including nine members of 2002).. vec- United States extending from Maryland and tors.. and lesions. The infective parasites are dence of human leishmaniasis (Margonari passed in the bug faeces at the time of feed- et al. Kjos et al. health importance. tribution of the arthropod vector commonly T. recurva. and rare human cases have also Although the stercorarian route is been reported in the United States (Dorn et al. T. and the more persist- 2002. bugs in the Panstrongylus infection rates have been reported in parts and Rodnius genera are also important vec- of South America. raccoons. 2006. the bug hindgut. Blood mastigote form of the parasite multiplies in transfusion has been identified as another ... T. raccoon. mission. oral transmission of the parasite has been Transmission documented in humans after consumption of unpasteurized fruit juice containing infected T. lymph nodes. 1958. humans. 2008). A wide range of mam- Triatomine bugs utilize a broad range of ver- malian species including dogs. rubida. 2009a. parasites.. stercorarian mechanism where the parasite transplacental transmission of parasites localizes in the hindgut of the triatomine has been documented in humans and dogs bug vector. Karsten et al. 1996. rubrofasciata. birds. 1992. Dogs and Protozoan Zoonoses 97 populations is associated with increased inci. and wood rats after they ingest infected bugs (Roelling et al. tions.M.. bilateral cardiac dilatation over a variable WHO. 2010). . 2009. One sometimes overlooked can last up to 2 months. populations. In the initial acute phase. In one report WHO categorizes Chagas disease as one of reviewing the histopathologic records of 86 the neglected tropical diseases (WHO. In the acute phase. with signs of myocardi- with T. by megaoesophagus and/or megacolon but organisms are difficult to identify micro- develop in about 10% of chronically infected scopically during chronic stages of infection. A combination of cardiac and diges- The US Food and Drug Administration (FDA) tive organ damage often occurs.. Up to 30% of nosis is usually made based on a combina- chronically infected people develop cardiac tion of appropriate (geographic) history disease that results in acute death or end.98 K.000 people who acquired their infections Survivors of acute myocarditis become apar- in endemic countries now live in the USA. Often people are asymptomatic. so many blood bank systems in the United States have joined other Disease in dogs countries by routinely screen blood products. In the chronic.. while megaoesophagus and other Disease in humans megaviscus syndromes described in humans have not been reported in dogs (Barr. countries. 2009a. progres- sive stage of the disease. 300. 2010). Snowden and C. positive serologic testing. Although not all dogs generally described in two phases. of possible exposure. Snowden and Kjos.2 Cases of parasite transmission through organ Acute and chronic cases of Chagas disease transplantation have also been documented have been reported in domestic dogs in the in Latin America and rarely in the United United States and many Latin American States (Casadei. Reported cardiac disorders symptoms supported by microscopic identi- include arrhythmias and other electrical con. many develop tion is lifelong if untreated (Pereira et al. This stage can persist for years. enlarged lymph nodes. Abnormalities include atrial ache. the target tissues for Diagnosis and treatment amastigote replication and organ dysfunction include the heart and digestive system smooth In both humans and dogs. which length of time. 42% of the previously Based on seroprevalence studies in immigrant normal animals were reported as acute deaths. Digestive disorders caused blood films when parasitaemias are high. a definitive diag- muscle and innervating ganglia. and fibrillation. and some people never develop chronic Chagas- related symptoms. the CDC estimates that more than and most were young dogs (Kjos et al. and clinical reported in 21% of the cases in a recent report signs may be mild to severe with fever. head- (Kjos et al. cruzi.3 asitaemic and asymptomatic in the indeter- The clinical disease caused by T. approved a diagnostic blood screening test in 2007 for voluntary use. and cardiac muscle dam. mostly in Latin America. tion disturbance with variable cardiomegaly. fication of parasites on blood films and/or duction disturbances. and the tis and cardiac arrhythmias. cruzi is minate or latent phase. infection. 2012). 2008). and infec- progress to chronic disease. muscle pain. and a number of animals prolonged ‘indeterminate’ stage where people are candidates for pacemaker implantation are asymptomatic and often unaware of their (Barr.F. canine Chagas cases. age resulting in chronic progressive dilatative trypomastigotes are identified on stained cardiomyopathy. people. 2010). Budke possible route of transmission in humans.. Acute disease is An estimated 10 million people are infected sudden in onset. 2009a. a high number of try- aspect of chronic infection is electrical conduc- pomastigotes may be detected in circulation. ventricular premature contrac- sometimes swelling at the inoculation site. 2008). The pattern of infection in dogs appears to follow the cardiac disease pattern in humans. and clinical signs/ stage heart failure. Kjos et al. first and second degree heart block and The acute phase is typically followed by a tachyarrhythmias. 2008). Dogs and Protozoan Zoonoses 99 To detect parasite specific antibodies dur.. The second drug approved for as competent parasite reservoirs and blood . haemoculture. also showed some ing chronic infection. such with the patient’s blood). able in the United States. the risk of transplacental transmission of the ments for cardiac or digestive manifestations parasite will be virtually eliminated if only are often helpful in improving the quality of serologically negative bitches are used for life of chronically infected individuals.. 2002). 1992). Zoonotic potential and public health appropriate drugs are not available. 2009). appropriate pesticide regimens. of triatomine bugs. or mentally infected dogs (Guedes et al. and are available in the United in histologic sections of cardiac muscle or States (Rojas de Arias et al. In lim. In addition to the use of appropriate nosis (Snowden and Kjos. 2012).. and the value of treat. Additionally. immunochromatic tests (Nieto et al. The of domiciliated bug vectors through the use of specificity of different serologic tests varies. Removing serologically positive breed- ment with either of these drugs is debated. cruzi infection among domestic graphic evidence of conduction abnormalities dogs. of yard lights to reduce attraction of insects 2010). 2006). human use. plugging drains or other openings and can often be successfully treated with the securing movable doors). nifurtimox showed some success in treating experimental and natural Chagas disease continues to pose a signifi- cases of canine trypanosomiasis. or as deltamethrin. immunofluorescent. ing stock from kennels may reduce the risk Unfortunately. benznidazole. largely on rapid diagnosis and initiation of using mechanical barriers around indoor treatment early in the acute phase. prevention of Chagas disease and visceral Leishmania parasites in both in humans has primarily focused on reduction dogs and humans (Duprey et al. residual spray agnosis (examination of triatomine bugs fed formulations of synthetic pyrethroids. Domestic side effects limited its use (Haberkorn and dogs in South America play a significant role Gonnert. of dog–bug–dog transmission. Therapeutic options for treating T. Treatment of chronic disease is much (Snowden and Kjos. acute Chagas disease in humans (e. digestive organs provides a definitive diag. Additionally. xenodi. Similar triatomine bug control mechanisms Radiographic or ultrasononographic evi. control measures could include Success of treatment in humans depends housing dogs indoors at night if possible. treatment of humans rather than dogs is a primary focus. endemic. These tests are variably available for humans or for dogs depending on geographic loca- tion (United States versus Latin American Prevention and control countries).g. and in the United States. and the possibility of misdiagnosis exists in screening of the blood supply has reduced geographic regions where both parasites are the risk of transfusion-associated infection. 2003). cruzi In Latin America. However. Currently there are no pesticides in the also support a diagnosis of Chagas disease United States specifically labelled for control (Barr et al. and limiting the use drugs nifurtimox or benznidazole (WHO. pesticides. less efficacy in treating chronic cases in experi- mats such as ELISA. reduce T. considerations ited research studies. but had tests are available in a variety of test for. Less commonly. 1972). a selection of serologic success in treating acute infections. neither of these drugs is avail. less rewarding. cruzi infections in dogs are limited. Post-mortem identification of parasites Latin America.. but severe cant health threat in the Americas. In Latin kennels to minimize bug entry into premises America. In Latin America.. could be employed in the United States to dence of cardiac enlargement or electrocardio. Supportive treat. have proved to be very effec- molecular methods are used on a research tive at killing the Chagas disease vectors in basis. One important concern to note is the serologic cross reactivity between T. 2012). breeding purposes. 9. and T. the low prob. 2009b). duodenalis. The evidence of canine involvement in vector. sanguisuga utilize dogs as blood hosts Depending on the date of publication and (Kjos et al. are typically housed in outdoor ken. 2009). . In a US study using a ine species is probably the major reason for commercially available faecal antigen detec- the low transmission rates (Kjos et al. lamblia analysis revealed that Triatoma gerstaeckeri and G. duodenalis. 2010). such types of surveys.. 2008). 2009b).8% of almost 5000 cats were positive for The disparity in prevalence between dogs the parasite (Carlin et al. G. The scientific names settings in Texas. 10. G. intestinalis.100 K. In a similar and humans in the United States may be due European study using the same diagnostic to differences in vector exposure levels and test for symptomatic animals. the host spe- is significantly lower than in Latin American cies. 2009a).. DNA-based blood meal identifying this organism include G. dogs less than 6 months of age to 1.. Oral ingestion of infected dogs and 20. lamblia) probably depends on host characteristics. as sup. with several recent surveys reporting a manifestations and low awareness among wide range of prevalence values depending physicians. Dogs housed in outdoor England using the same diagnostic test. and serve as found in close proximity to cases (Beard et al. Navin et al.. and is rec- borne transmission in this region (Herwaldt ognized as one of the most common enteric et al. the United States. In the United States. United States is almost certainly under-recognized The parasite is common in dogs and due to a predominance of mild and/or latent cats. Budke hosts for the triatomine vectors. 2010). exposure to able). and parasite Giardia intestinalis is a flagellated extracellu- strain virulence. vector-borne human transmission on the pet population surveyed. In a survey of parasites of domestic animals and humans triatomine bugs collected from peridomestic (Thompson et al. Studies in endemic areas of Argentina have shown that dogs have a high capacity to infect triatomine bugs due to persistent para- sitaemia (Gürtler et al.. organism.3% of 4214 cats were positive triatomine bugs may be a significant route of (Epe et al. bug vector feeding behaviour.F.. all three of these names required to fully understand the role of dogs can be commonly found in scientific litera- in the Chagas disease transmission cycle in ture and are assumed to be synonymous. In a cross-sectional study in infection for dogs.6% of more than 16. 4% were positive.000 dogs and not reflected in the domestic dog population.. Hunting animals (Upjohn et al. indicating a much with triatomine bugs than humans. lamblia). 15. canine samples (no clinical histories avail- nels. parasite is global in distribution. United States has not been determined but G.. 2006)... the diagnostic method used to detect the countries. the same low level transmission is animals.9% kennels have more opportunity for encounters of 878 dogs were positive. Snowden and C. G. which tend to experience the highest national survey using zinc sulphate centrifu- Chagas disease prevalence rates in the United gal flotation of approximately 1. Regardless of the mechanism. with an age-related infected vectors appears to play a role in canine decreasing prevalence ranging from 13. providing some lian hosts including dogs and humans. 2007). or animals lower prevalence in a general population of that sleep inside houses at night.8% of 8685 transmission routes. and other factors which may bias ability of human contact with infected triatom. duodenalis as well as G. Giardiasis is caused by Giardia intestinalis Although human Chagas disease in the (syn. tion test on faecal samples from symptomatic However..5% in dogs ported by reports of infected bug specimens over 7 years of age (Little et al.M. 2003. Seropositive dogs were lar protozoan pathogen that localizes in the identified in close proximity to two autoch. sion. In another US dogs. 2000.2 million States. surveillance sentinels for domestic transmis.1% in Chagas disease in the United States. Additional research is author preferences. 24. The importance Giardiasis caused by Giardia of dogs as Chagas disease reservoirs in the intestinalis (syn. 1985). Kjos et al.. small intestine of a wide range of mamma- thonous US human cases. where transmission of the parasite Giardia infections have been documented is frequently associated with cyst-contami- in a number of additional domestic animals nated water. 2010).. needed to establish an infection and cause In a recent review summarizing prevalence diarrhoea (Ballweber et al. and data infective dose of as few as 10–100 cysts were are under-reported (Yoder et al. and both human and pet studies show agreement in animal outbreaks are not well documented.. Additionally.8 et al. Data from to animal transmission mechanisms. metabolically active. The role with summer recreational water usage. not all infected persons seek water in temperate conditions (Plutzer et al. prevalence ranged from shedding has been reported to be as short as approximately 1% to 11% in asymptomatic peo. 2007. beaver. based largely the oval. espe- of these animals as reservoirs of infection cially in children in the United States (Yoder that cause environmental contamination with et al. Potential mechanisms of transfer cases at the state level in 2008.2 to 33. humans.. an nostics are not always completed. sheep. 2010). environmental contamination (Plutzer et al... non-reproducing cyst on voluntary data collected by the National stage that is passed in the faeces. such as swimming pools. and from approximately 2% to 18% in symp. Cysts are Notifiable Disease Surveillance System (Yoder immediately infective when ingested by the et al. to 73% (Dib et al. usually in an indirect manner through 5–9. and the duration of shedding summarizing published data from 28 human can last for weeks to several months (Yoder studies across Asia. Dogs and Protozoan Zoonoses 101 The prevalence of Giardia infections in is the motile. In a recent review their faeces... or data also showed the highest case numbers in zoonotic (animal to human or human to ani- children aged 1–4 followed by children aged mal). and is usually associ- ated with direct contamination of food by an The Giardia organism has a direct life cycle infected food handler.000 human cases annually for testinal tract with ingesta. and rivers. data are not gener- is a common parasite in both humans and dogs ally available regarding individual animal in widespread geographic locations. appropriate laboratory diag.000 population ranged from 2. or by using contami- with two morphologic forms. 2010). Surveillance include person to person. prevalence ranged from 1% et al. . 2008). 2010). villous epithelial surface of the small intestine. 2010). Data from these and Beyond the generalized faecal–oral other epidemiologic studies confirm that Giardia transmission pattern. medical care. 2010). Incidence of giardiasis cases per appropriate mammalian host (Thompson 100. as well as in wildlife such as nutria. Foodborne transmission of Transmission Giardia is less frequent. Giardia was the cause of 15 of 141 (10. 2010). muskrat.. ing systems. The trophozoite nated water in food preparation. The cysts are environmentally resistant United States because the infection can be and can survive for months in soil or surface asymptomatic.. In experi- data from a number of human studies from 20 mental canine infections. mate the giardiasis burden in humans in the 2010).. swine. and to contaminated communal water sources horses. 2010). over a 10-year infective cysts has been widely debated. and aquatic birds A seasonal peak in case reports coincides (reviewed in Plutzer et al. the CDC As organisms move caudally in the gastroin- reported over 19. otter. In the United States. In human experimental studies. they transform to the years 2006.. 2010). Outbreaks are frequently linked including goats. ple. non-motile. It is assumed that these data underesti. period. 5–7 days after cyst ingestion (Ballweber et al. animal to animal.6%) reported drinking-water-associated gastroenteritis outbreaks in the United States (Yoder et al. the onset of cyst European countries. cattle. An infected person or animal can shed tomatic cases. the age-related trend for higher infection rates in Transmission patterns are better studied in children and young animals. tear-drop humans is also difficult to determine due to a shaped. flagellated form that replicates at the lack of standardized test methods and report. with the highest values reported in variable numbers of cysts intermittently in children (Plutzer et al. 2010). 2008)... and 2008. lakes. this method (Ballweber et al. but they are probably but generally lack sensitivity (Ballweber et al. as well as in epi- nostic tests that detect Giardia cysts in faeces demiological surveys in the United States and . 2010. disease are unclear. cramps. but it is a commonly used assay in The development of protective immunity veterinary diagnostic laboratories and com- against Giardia has not been clearly proven in mercial fee-for-service laboratories. tion technique. individual patient samples. food aller. abdominal (Mekaru et al. or the presence of additional microbial hospital laboratories because of the need for a enteropathogens have also been suggested compound microscope with appropriate UV as influential factors in the onset. human or domestic animal hosts. of fresh samples is essential since the tropho- nal mucosa. particularly using zinc sulphate intermittent.. research reports. 2010). A number of pathophysiologic zoites are not environmentally stable and rap- mechanisms are being explored as a cause of idly lose their motility under cool or drying the diarrhoea that commonly is associated conditions.102 K.F. IDEXX Laboratories) is frequently used in veterinary practices for evaluating A variety of microscopic and immunodiag. cal smears made from fixed faecal samples are The reasons for the spectrum of clinical sometimes evaluated in human laboratories. vomiting. Meridian Bioscience) is often considered the thelial barrier function causing increased ‘gold standard’ method in both human and permeability. human use are utilized for companion animal sample testing.. or chronic diarrhoea. light source and barrier filters to complete and severity of clinical disease. a number of mechanisms A direct immunofluorescent assay have been suggested including increased (Merifluor Cryptosporidium/Giardia assay. Rishniw et al. loss of intestinal epi. Mekaru 2008).. 2010). and abnormal transport of veterinary diagnostic laboratories because of electrolyte and nutrients at the epithelial excellent specificity and good sensitivity of microvillous border (reviewed by Buret. Budke Disease in humans and dogs are available either as in-house or diagnostic laboratory fee-for-service assays. Yoder et al. this method lacks sensitivity. The Giardia trophozoites sometimes show motile trophozoites. Parasitologic The clinical disease in humans and dogs methods using faecal flotation and microscopy is generally similar. It is unclear A number of faecal antigen detec- whether intermittent diarrhoea episodes are tion immunodiagnostic tests in single or an indication of continued infection despite multi-well ELISA or card formats are com- treatment. This technique has commensal microbial gut flora. et al... Sometimes assays designed for of disease. are not invasive and do not cause signifi.. Additionally.M. 2010. 2007. to acute. Variations causes a spectrum of clinical manifesta. the assay. anorexia.. Rapid evaluation cant morphologic injury to the small intesti. The light microscopic methods are with this parasite infection. duration. 2007). on those methods including a centrifugal flota- tions ranging from asymptomatic. due to a number of interacting host and 2010). and malabsorp. 2010. a point-of-use lat- eral flow faecal antigen detection test (Giardia Diagnosis SNAP test.. Typically flotation solution (specific gravity 1. with variable results (Mekaru et al. causing repeated clinical occurrences erinary use. limited usage in veterinary clinics or many gies. This enteric pathogen are widely used in veterinary clinics. or whether reinfection occurs mercially available for both human and vet- readily. testinal conditions such as a disruption of 2010. enterocyte apoptosis.. A number of concurrent gastroin. 2006). and sometimes nausea. In a variety of typically rapid and inexpensive to perform. 2007. Stained fae- (Ballweber et al. The sensitivity and specificity of these meth- tion. Zajac and Conboy. Yoder et al. bloating. Snowden and C. however.18) and the disease is characterized by non-bloody formol-ethyl sedimentation have been described soft formed to unformed faeces. and ods vary depending on the specific protocol steatorrhoea with or without weight loss and the skill of the microscopist. Plutzer et al.. Wet mounts of fresh liquid faeces may parasite factors. Using a combination of immunodiag. 2007. 2005. Thompson et al.. sure to the parasite. suggesting Upjohn et al. 2008). Vidal and against giardiasis. 2010). It is generally reported that zole. molecular methods are being several combination products that include the developed to identify the parasite. 2008. using varied treatment at a greater cost/test (Vidal and Catapani. 2008). concentrate and detect Giardia cysts in the As previously noted. United States (Thompson et al. and duration regimens 2005). but this diagnostic option is expanding nary products labelled for dogs or cats in the in both medical and veterinary laboratories.. there that parasite resistance may occur (Montoya is often a discrepancy in analysing a single et al. of a multi-pathogen PCR assay or real-time PCR febantel. (reviewed by Thompson et al. met. Rishniw et al. oxfendazole. Standardized should be determined on a recurrent basis protocols using fluorescent microscopy and/ in symptomatic human or animal patients. cyst shedding with a low rate of adverse reac- lected over several days also increases the tions.. Disappointingly. 2008). e fficacy of the product is variable. and albendazole has been the immunodiagnostic tests detect a higher shown in either experimental canine infections number of positive samples than microscopy. Although sensitivity of detection of Giardia (Vidal and specific formulations differ when comparing Catapani. Thompson et al. lidone and quinacrine have been reported in for-service basis from a commercial diagnostic older literature as treatments for giardiasis. frequency... The avail. human and animal faecal samples. A number of detrimen.. laboratory varies.. 2008). The use of multiple samples col. sample using multiple methods with either Several compounds in the benzimidazole domestic animal or human samples (Mekaru family have been widely used as treatment et al. One controversial point in veterinary medicine is whether to prescribe medication to a clinically normal Treatment animal with faecal shedding of cysts. de Boer et al. it is often As with any case of diarrhoea. Additional compounds such as furazo- ability of molecular diagnostic tests on a fee.. or molecular methods are now available for Fluid therapy should be administered as sup- processing both water and soil samples to portive treatment as appropriate. Epe et al. although a ‘cure’ is not assured. The CDC has published tal side effects have been reported. 2006). A variety of drugs has been used to treat giardiasis in domestic animals and humans. the sever- helpful to evaluate environmental samples ity of dehydration and electrolyte imbalance as possible sources of cysts.. asymptomatic environment (Thompson et al. Prevention and control ronidazole. Zajac and Conboy. shedding of Giardia cysts has been reported in both humans and dogs. ment of these molecular methods using both 2008. 2006. 2010. tel. the oral anti-protozoal drug. along with praziquantel and pyran- assay (Amar et al. dosage. products from the United States and Europe. Animals nostic and parasitologic microscopy methods treated with these compounds generally show ensures the most accurate diagnosis of this clinical improvement and decreased parasite parasite. depending on the geographic but are not currently used widely as veteri- location. have shown good efficacy when used in a Many research reports describe the develop.. is widely used as a multi-dose treatment against giardiasis. The efficacy of fenbenda- Catapani 2005). that Since infection occurs through the ingestion compound is not approved for animal use and of infective cysts either directly or indirectly is prescribed by veterinarians in the United through faecal–oral contact. In outbreak investigations. and the a detailed list of recommendations to prevent . 2010). the practice of States under the Animal Medicinal Drug good hygiene is the key to minimize expo- Use Clarification Act. However. 2007... Additionally. 2008). multi-day treatment regimen (Montoya et al. or in clinical studies. Dogs and Protozoan Zoonoses 103 Europe (Carlin et al. 2010. In humans. often as part closely related pro-benzimidazole compound... Giardia health considerations assemblage A found mostly in humans remains G. in human–pet interactions. E is found in cattle and hoofed eating. local parasite strain variation. using different hosts and their importance in trans- gloves when cleaning up animal faeces. bovis in hoofed of zoonotic transmission of the parasite is an stock. Interestingly. and mission of the parasite from pets to humans. there is a consensus that humans of these do not cause clinical disease. suggested that local environmental condi- rhoea if the animal because ill. cati in cats. some scientists have Zoonotic potential and public proposed changes in nomenclature. It is tive intensity of human–animal contact will unclear whether a similar vaccine will become influence the potential for zoonotic transmis- commercially available in the future. most A. subtypes AI to While there are a number of protozoan organ- AIV have been identified within assemblage isms that infect both dogs and humans.. Some of the most important points zoonotic potential.M. To clarify the genetic variations and transmissibility of parasite assemblages among different hosts. 2008). 2010). and G is described nappies or tending someone who is ill with in rodents (reviewed by Ballweber et al.. Whether this revised nomencla- molecular data. .. indirectly from other humans. 2010). it is now recognized that most isolates able is a vaccine (GiardiaVax for Dogs® and found in humans were probably transmitted GiardiaVax for Cats®. while assemblage The zoonotic potential of Giardia isolates has B would become the zoonotic G. However. In additional groupings. and comparisons of numerous iso. area of continued study and debate. or uncooked cific levels. 2010. Ft Dodge Animal Health. Additionally. Humans and dogs (or occasionally other approaches can readily be applied to pets mammals) have been infected with assem- and their environments as appropriate (Yoder blage B. simondi in rats. Based on a more restricted host pref- asites from both humans and animals (Plutzer erence. enterica spe- been experimentally demonstrated using par. and after handling animal wastes. (2010) summarized foods that were prepared using contaminated data from 36 studies that reported discrep- water. and these A. and G would et al. 2008). lates from a variety of hosts have resulted in the description of at least seven genetically distinct groups called genotypes or assem- blages identified as ‘A’ to ‘G’ types (reviewed Conclusions by Ballweber et al. 2010. rivers. the relative importance become G. E. F is found in cats. Based on respectively. Based on several recent studies using these One additional control approach for dogs molecular technologies in taxonomic stud- and cats that is no longer commercially avail. indicating this genotype clearly has et al. inadequately impact on Giardia at the species and intraspe- treated drinking water or ice. diarrhoea. after using the toilet. canis in dogs. cies. 2008)... and a decreased tions.F. Thompson et al. remains to be seen. It is as a decreased severity and duration of diar.. Assemblages C and D are emphasize effective hand washing before found in dogs. ant information regarding the relative dis- the CDC recommends minimizing contact tribution of the various assemblages among with the faecal materials of all animals. or only are the predominant host for assemblage cause mild disease in dog and/or human hosts. and rela- number and duration of cyst shedding. and that the Charles City. assemblages C. Snowden and C. G. ies. Other recommendations include avoiding It is increasingly clear that molecular epi- potentially unclean water sources such as demiologic studies are having an enormous swimming pools. multilocus genetic sequence ture is accepted in the scientific community analyses. F. after changing stock. the vaccine zoonotic importance of parasite transmission product label defined the efficacy of the vaccine is diminishing (Thompson et al.104 K. G. Budke and control giardiasis in humans. Ballweber et al. sion of this parasite. Thompson et al. Generally. and G. lakes. Iowa).. washing hands after handling those faeces. duodenalis. 180–189. M... R. 2 www. Bowman. 557–561. International Journal for Parasitology 26. 95–100. J. and Maroli M. V. Metz. . accessed 7 June 2012.. (2004) Serological survey of Leishmania infection in dogs from the municipality of Peso da Regua (Alto Doura. Paraguai de Souza. 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Schistosomatidae ondary intermediate host such as a fish or edible crustacean (again except for the schistosomes. enzymes and is of great importance in nutrition. 7 Dogs and Trematode Zoonoses1 Albis Francesco Gabrielli* WHO.) 109 . S. 2006. 1982. which (listed in Table 7. Cheesbrough.1). although almost all are Platyhelminthes. Kaufmann.. There are over 60 trematode species which have sionally globular. Switzerland The trematodes or flukes belong to the Phylum choice of definitive host.g. Muller. e-mail: gabriellia@who. Schnieder. Kassai. S. the most important reservoir hosts of human ing bifurcate intestine without an anus and two infection. Bowman. mekongi) are the cause of schisto- hosts. chyma as there is no coelom. 1994. Dicrocoelium dendriticum) or. Geerts et al. 2009) and zoonotic trematode para- ment. to the host. S. japonicum. Crompton and Savioli. are characteristically flat and leaf-like. Most are freshwater species of snails but a few utilize terrestrial snails (e. All organs are surrounded by paren. the schistosomes. intercalatum. Euzeby. 1995.int ©CAB International 2013.. Hugh-Jones et al. man- depends very much on the dietary habits of the soni. Adult trematodes are very catholic in their somiasis. WHO. in Five species of schistosomes (Schistosoma which larvae penetrate the skin). Thus infection haematobium. Geneva. They are all endoparasites and very specific in which snails they can develop. 1982. and S. Zoonoses and Public Health. 1996. is composed sites in general in various monographs (Malek. Georgi and Georgi. The Schistosomes Inside the snail all trematodes undergo asexual reproduction and most which parasitize both Superfamily Schistosomatoidea: Family humans and dogs have a cystic stage in a sec. and dogs are not cylindrical female). Schultz. it is thus an antigenically active site. 2nd Edition (eds C. marine species. 1987. 2007). 2002. which always involves a snail as first intermedi- ate host. or occa. Hillyer and Hopla. which often contains spines. suckers: an anterior oral sucker surrounding the The trematode parasites of dogs are consid- mouth.L. Trematodes have an indirect life cycle 2006. which is prevalent in 57 countries * Author. 1996. and the outer tegu. acetabulum by which the worm attaches itself 1982. of a syncytial cytoplasmic layer which secretes 1980. Macpherson et al. Hinz. hermaphroditic organisms been reported from both humans and dogs (except for one group. but for many trematodes have a male folded about its long axis and a they are occasional hosts only. 1978. 1999. Adults have a blindly end. 1992. for sea birds.N. Dogs. FAO. 1995. and a more posterior ventral sucker or ered in standard textbooks (Dunn. adults are also S. while 765 million were living in areas the smaller and thinner female residing where schistosomiasis is transmitted (popu. mansoni. Africa and also occurs in foci in the Middle 1990. mekongi is morphologically similar diarrhoea and headache. Jordan et al. 25. 2003). species globally. Effective treatment (Jordan et al. 1993). Diagnosis is by find- East.000 of the portal vein. in heavy to S. 60 mm and with a lateral spine) are laid in the Of the primarily human species. veins from the liver which can burst. 2010). mansoni is widely distributed in death (Rollinson and Simpson. mekongi measuring 85 × 60 mm with a small at-risk. and is an important human infections eggs get carried through the portal parasite in the Mekong valley regions of venous system to the liver. This phase of infection may be symptom- humans are refractory (Fan. Africa. Sulawesi. less or accompanied by bloody intermittent S. In Taiwan. Guttierez. granulomas and eventually extensive fibro- infection occurs only in animal hosts and sis. recent years in China. and are passed out in fae- are often infected and act as reservoir hosts. McManus et al. japonicum. intercalatum is only The epidemiology of schistosomiasis is transmitted in isolated foci in central Africa. South America. mansoni measuring 140 × communities. especially in agricultural and fishing knob.. Dogs faecal samples is also possible by immunolog- can be infected but often do not pass eggs ical or molecular methods. emerges and can survive for a few animals can act as reservoir hosts but the days in water.000 and 112. Gabrielli across America. If it comes into contact with a most important are bovines (with up to 90% susceptible mammal it penetrates through the infection rates in cattle and buffalo) and dogs skin by means of histolytic glands.000 and 82. the Adult S. a few weeks later the China. and S. In 2009 a suitable species of snail (see Table 7.F. emerges and penetrates into China. Dogs are the only and compensatory enlargement of the minor reservoir hosts.000 in Laos. and the Caribbean ing eggs in the faeces or by serological meth- (principally Puerto Rico and the Dominican ods such as ELISA. and those of S. and the Philippines. causing S.. mansoni only. S. Reservoir hosts are of little epi. fork-tailed larval stage. and then migrates to its final site widespread and effective control achieved in via the pulmonary veins. sion with enlargement of the liver and spleen. 2010). japonicum small venules. ces.000 cases in tiplies inside the snail. the recent construction The adult worms do little damage.. and granulomas Laos and Cambodia. known Human infection is principally confined to as a miracidium. the number of people infected and to extensive fibrosis surrounding the branches at-risk has been reduced to 14. 2010). and Asia. Eggs (those of S. leading to the formation of et al. 1993). mekongi estimated number of people infected was 239 worms live in the posterior mesenteric veins. penetrate through the wall of is a true zoonosis and dogs as well as bovines the large intestine. After years of effective formed around them there lead in 5–15 years control. japonicum and ticularly affecting children. but in of the Three Gorges Dam on the Yangtze river chronic infections more and more eggs become is likely to represent a significant threat in trapped in the tissues. determined by the habits of the snail interme- neither is a zoonosis and so they are not diate hosts. producing an inflam- terms of expansion of population at-risk (Zhu matory response. japonicum live either in considered here. respectively (WHO. par. and 576.. while S. japonicum. 2008. In spite of the lungs. permanently in a canal formed by the fleshy lation at-risk) (WHO. In 2009. 1993).000 in next free-living. 2010).110 A. reaches (10% infected) (Jordan et al. detection of antigens on urine or and rodents may be of local importance. about 12 mm. 1987. or S.1). S.. and 31. million. This causes portal hyperten- in Cambodia. which detect antibodies or Republic). the muddy margins of streams and rivers (in . is possible with praziquantel for all species. the the Philippines (WHO. In China many cercaria. Those of S. mul- there were estimated to be 730. However. On reaching freshwater a larva. circulating antigens released by worms in the demiological significance although primates bloodstream.000 in Indonesia. Schistosomiasis ventral folds of the male which measures in humans is primarily a rural disease. haematobium is the most widespread with oxamniquine for S. sinensis and civet cats (fam- get infected by paddling in swampy areas ily: Viverridae) are the natural reservoir hosts or swimming in canals in areas where rac. Dogs and Trematode Zoonoses 111 China) or in rice paddies (in the Philippines). and the duct epithelium. It is estimated that 7–19 million people while the natural habit of snails transmitting are infected with Clonorchis sinensis world- S. Praziquantel ate to the number of worms infecting the host. especially. 2002). Dogs zoophilic than C. Symptoms and signs in dogs are important reservoir hosts of O. mansoni inhabit infected with O. also common in domestic cats and dogs. but infection is frequently found also in dogs. The adults are found in 1992 for effects in dogs). particularly Clonorchis the testes are in tandem and have long the large-scale ones in Egypt and Sudan. anorexia. slow-flowing streams. marinated. The distribution of Both genera are very similar in morphology S. salted. WHO. many tion. Pathologically the the hepatic and pancreatic ducts of fish-eating adult flukes cause proliferation of the bile mammals (including humans) or birds. for perpetuating its transmission. from the schistosomes. 5–20 mm in length. Muller. snail control. sanita. in this case the presence of worms is only diagnosed at necropsy. while at least 8 million are infected with in partially submerged rocks and stones on Opisthorchis viverrini and 0. whose severity is proportion- frequent (Fabrick et al. vomiting. stones. There can also be recurrent gall- bladder colic due to expulsion of worms or Members of this family are typically flattened. 1998. WHO. cation of various larval stages in the snail. and foxes. while in Opisthorchis the testes Prevention is by avoiding contact with water are semi-adjacent and are lobate. mansoni is increasing in Africa because of and life cycle. Dogs are the most important reservoir site of dogs and other mammals in the hosts of C. felineus. 1995. preponderant in some areas. 2012. or Haswell-Elkins and Elkins. tissues. It is a para.. and Savioli. human–snail–fish–human transmission can be not develop further and cause a dermatitis. there is also a high eosinophilia (up Family Opisthorchiidae to 40%). pickled. bution of praziquantel to individuals at-risk The infection is acquired through the (Savioli et al. oedema. of the parasite (hence the name). the natural reservoir of the infection. preventive thousands of cercariae emerge over the life of the chemotherapy – the regular. and fenbendazole are effective treatments.5 million are the river bed. anaemia and hypercalcaemia are manifestations. and swelling of the liver (hepatomegaly) and spleen (splenom- Superfamily Opisthorchioidea: egaly). cats and pigs (Muller. The majority of infections are light and symp- tomless. 1997. 2002). include lethargy. large-scale distri. of C. the main difference being that in many new irrigation schemes. Cats are present. sinensis and are usually responsible south-western United States (Johnson. environmental management. 2007. inflammation of the lymph nodes (lymphad. ducts and destruction of the adjacent liver . branched lobes. smoked. 2010). O. 2010). sinensis is typical of most trematodes apart Possible control measures include health edu. measuring and loss of weight (see Georgi and Georgi. Heavier infec- tions (over 100 worms in humans) result in The Opisthorchids diarrhoea. loss of weight. Because of the multipli- cation. Fürst. or poorly Heterobilharzia americana is a trematode processed freshwater fish hosting metacer- related to Schistosoma spp. even though In humans the penetrating cercariae can. Crompton consumption of raw. All the liver flukes have similar clinical enopathy). followed by fibrosis of the cercariae encyst in freshwater fish (Table 7.. pigs and rats can similar to that caused by many bird schisto. and is the causal carial cysts in the subcutaneous connective agent of canine schistosomiasis. dried. 2006). snail for each miracidium which penetrated. The life cycle in which transmission may be occurring. infection is coons. Snails of S. chronic intermittent dysentery. associated with recurrent cholangitis elongate. felineus (WHO. fever. also be naturally infected. viverrini is more somes and known as ‘swimmer’s itch’. mekongi is constituted by the small crevices wide.4–1. irrigation canals. partially cooked. 2002.1). large ponds or lakes. and. hermaphroditic flukes. Snails (exper. As above Small intestine (Lu. Bellamya Dog. b) Family Echinostomatidae Echinochamus 1.1. hortense 1. Fw fish Small intestine (Lu. americana 1. dog) Small intestine (Lu. 1982) . Dog) China. Taiwan 2. revolutum 1. cat. Helisoma Domestic birds. dog. 1941) Family Diplostomatidae Alaria alata 1. perfoliatus 1. fox. Europe 2. 1994) E. man (exper. Europe. fish Small intestine (Lie-Kian and Virik. Taiwan 2. man Philippines. Korea. cat. malayanum 1.). fox. 1976) E. muskrat. Indonesia. Frogs and snakes Small intestine (Freeman et al. 1985) E.. Frogs Small intestine (Dalimi and Mobedi.. Canada 2. Brackish water fishes Small intestine (Nasr. japonicus 1. cinetorchus 1.. marcianae 1. East 2. Lymnaea. Gabrielli fujianensis Small intestine (Yu and Mott. Fw fish and frogs Small intestine (Lin. Snails. man (larvae)* SW USA. Cleopatra Kite. cat. Indonesia 2. Snails Dog. Frogs and snakes Small intestine (Shoop and Corkum. Japan. cat. dog. man China. man China 2. India. Planorbis cat. Snails Small intestine (Geerts et al. frogs Small intestine (Ryang et al. Korea 2. Canada. Snails. Lymnaea Pig. 1986) E.F.Table 7. rat. 1996) Echinoparyphium 1. man (exper. 1983a. cat. cat) Taiwan recurvatum 2. Trematodes reported from both humans and dogs. Parafossarulus Heron. Parasite Intermediate hosts Final hosts Distribution and location in host (reference) Family Cathycotylidae Prohemistomum vivax 1. pig China A. Lymnaea cat. Indonesia 2. Fw fish Small intestine (Chen et al. Planorbis Cat. * = rare. 1992) A. Japan. man Japan. Lymnaea. man. man China. Malaysia China. Canada 2. fox. Hippeutis Dog. liliputanus 1. 1992) E. dog*.. dog. dog. man (larvae)* SW USA. pig. 1976) A. 1994) E. Planorbis (?) dog. fox. Fw fish or none Small intestine (Xiao et al. coyote. man Japan. Mid. Taiwan. ilocanum 1.. man (larvae)* USA. fw fish Small intestine (Tani. man* China angustitestis 2. 1982) Echinostoma 1. Segmentina Domestic birds. rats. Snail Dog (exper. 1963) E. man (once)* Egypt 2. dog. Planorbis Domestic birds. accessible publications which review 112 the infection. cat. 1987) E. cat. As far as possible the authorities quoted are recent. Taiwan 2. dog. Bithynia Dog. 1975) Dogs and Trematode Zoonoses C. fox. 1974) Centrocestus armatus 1. Semisulcospira Fish-eating birds. 1995) Brazil Small intestine (Chieffi et al. Cerithidea Fish-eating mammals. man) Japan 2. Snails? Fish-eating birds. 1987) Family Heterophyidae Apophallus donicus 1. dog. cat. Egypt 2. dog. dog. Fw fish small intestine (Hubbert et al. 1994) 113 Continued . Brackish w fish small intestine (Murrell. Laos. Helicella Most herbivores. 1983) H. man Egypt. Laos. man* small intestine (Rausch et al. man Korea 2. Asia. man Philippines. Fish small intestine (Tadros and El-Mokkadem. Malaysia. On plants Vietnam. 1995) Heterophyopsis continua 1. Canada 2. Melania Fish-eating birds.. Greenland 2. Flumenicola Heron. Japan Melania 2. Mullet small intestine (Shalaby and Trenti. 1991) Family Dicrocoeliidae Dicrocoelium dendriticum 1. Japan. China. dog. cat. Snails? Dog. Korea. Taiwan. Hippeutis Pig. man (Murrell. man Japan. 2. man Philippines. 1990) H. 1953) Heterophyes dispar 1. formosanus 1. 1991) H. man* Egypt 2. Hawaii. cat (exper. Korea. Fw fish small intestine (Radomyos et al.. Cerithidea? Dog. 1990) Family Fasciolidae Fasciolopsis buski 1. Stenomelania Fish-eating birds. man. cat. man Philippines. Episthmium caninum 1. man* Europe. Africa. fox. dog. Tantoglabrus Fish-eating birds and mammals. dog*. man* Thailand 2. frogs small intestine (Cheng et al. India Cambodia. dog. yokogawai 1. dog. cattle. dog. Americas 2. Marine fish small intestine (Chai and Lee. 1991) Cryptocotyle lingua 1.. cat. cat. Laos. heterophyes 1. Indonesia. man) East Europe. 1967) Haplorchis pumilio 1. Semisulcospira. cat. Japan.. Marine fish cat. Marine fish small intestine (Chai and Lee. Korea 2. France 2.. dog. Semisulcospira Fish-eating birds. Pirenella. Thailand small intestine (Kumar. Philippines. rat. dog*. dog Bangladesh. Fw fish. dog. Fish small intestine (Kwo En Hoa and Lie Kian Joe. Egypt 2. Ants bile ducts (Petithory and Ardoin. man China. Egypt 2. tachui 1. Fw fish cat. fox. small intestine 2. Fish-eating birds. 1990) Metagonimus yokogawai 1.. Pirenella Fish-eating mammals. 1992) Phagicola longa 1. Melania Cattle. Fish (Puntius) small intestine (Giboda et al. rat. China. cat. (exper. cat. Fw fish small intestine (Niemi and Macy. fw fish small intestine (Hinz. Melania. obtusum 1. Tilapia small intestine (Bhaibulaya. Pirenella? Dog. 1990) Family Microphallidae Microphallus minutus 1.. Bithynia? Man. spinicirrus 1. 1994) Family Lecithodendriidae Moedlingeria 1. man* Thailand. 1994) Phaneropsolus bonnei 1. Tilapia small intestine (Shalaby et al.F. Snails? (Exper. Mullet. 1996) P. Radomyos et al. Tilapia small intestine (Shalaby and Trenti.. 1994) Procerovum calderoni 1. man. ? Primates. dog) Egypt 2. Indonesia glandulosum 2. rat (exper. 1994) P. Bithynia Rat.Table 7. ornata 1. dog Thailand 2. Snails? Man? (exper. Hinz. USA 2. molenkampi 1. ornamentata 1.. Brackish w fish small intestine (Chai et al. Japan 2. Gabrielli 2. 1982. man (once)* Egypt 2. Insect larvae. 1994) P. Panama. 1996) P. Ecuador. Insect larvae Thailand small intestine (Bhaibulay. dog? Thailand 2. 1994) Stellantchasmus falcatus 1. Snails? Man? (exper. 1993) . rat. 114 Parasite Intermediate hosts Final hosts Distribution and location in host (reference) P. dog) Philippines. Insect larvae small intestine (Smales et al. dog) Korea 2.. Fish small intestine (Chai and Lee. dog. dog. man* Japan 2. man* (exper. Insect larvae small intestine (Bhaibulaya. Philippines. Thailand. Thiara Man (exper. 1988) Stictodora manilensis 1. cat. dog) man? Indonesia. man* Hawaii... Bithynia? Rat. man Korea. Brackish w fish small intestine (Radomyos et al. Egypt 2. cat. dog) Egypt 2. 1990) Pygidopsis summa 1. dog. 1996) Prosthodendrium 1. Bithynia? Primates. 1994) Pharyngostomum flapi 1.. dog*. dog*. bat. 1982. Tilapia small intestine (Shalaby et al. 1982. Shrimp bile and pancreatic ducts (Dill. varium 1. Snails? Man? (exper. Tympanotus Fish-eating birds. cat. Korea. cat. dog? Thailand 2. man*. Thailand A. Radomyos et al. Stenomelania Fish-eating birds. cat. Continued. chicken) Japan 2. Snails? Heron.1. Thailand amphoraeformis 2. goby small intestine (Shalaby and Trenti. Snails? Dog. Fw fish small intestine P. man*) Brazil. bat. Insect larvae small intestine (Hinz. Germany 2. 1978) P. 1989) P. Liberia 2. 1990) Pseudamphistomum 1.. 1995. Crabs Lungs (Kino et al. 1979) Taiwan. 1979) P. Taiwan 2.Family Opisthorchidae Amphimerus pseudofelineus 1. Gabon. Bythinella Wild carnivores. Central America.. dog. cat. Bythnia Civet cat. Ecuador 2. Korea. 1996) M. philippinensis 1. Bulimus. 1996) O. pig. Fish bile and pancreatic ducts (Kumar. Crabs Lungs (Dubey. conjunctus 1. Tricula Cat. pig. Fw fish bile ducts? (Maclean et al. viverrini 1. Man. mongoose Thailand. pig. man lungs (Khalil. hueit’ungensis 1. Crayfish Lungs (Argumedo. Crabs (Sesarma) Lungs (Wang et al. 1990) 115 Continued . man* Cameroon. rat) China 2. dog. Snails? Civet cat. Laos 2. dog. Japan lungs (Miyazaki. Parafoss. Crabs Lungs (Chung et al. dog. China. noverca 1. fox. Crabs Lungs (Sugano et al. 1989) P. Lungs (Sachs and Cumberlidge. 1987) Clonorchis (= Opisthorchis) 1. fish-eating Russia. Crabs etc. man India 2. dog. man* Thailand. Russia. Fw fish bile ducts (Semenova and Ivanov. cat. dog. Araopyrgus Wild carnivores. Nishida. Nigeria. Guinea truncatum 2. 1977) P. cat. dog. cat. man Vietnam.. rat. kellicotti 1. dog. Snails? Coyote. Laos Dogs and Trematode Zoonoses 2. Turkey Iran (= Opisthorchis 2. Cameroon. cat. man* Alaska. man. Nigeria. dog.. man China 2. Fw fish cat. Fw fish gall bladder (Leiper. France. opossum. man Canada. USA 2. man Italy. man Japan 2. man* Canada. man* Mexico. Fw fish? bile ducts? (Dalimi and Mobedi. Siberia. Korea. pulmonalis 1. Cyprinid fish Opisthorchis felineus 1. Central Europe sinensis Arulus carnivores bile ducts? (Lebedev. 1996) P. dog*. E. Crabs (Potamon) Lungs (Ito et al. dog. Semisulcospira Cat. Antemelenia Man (exper. miyazakii 1. Peru. Bithynia Cat. Tricula Cat. dog.. mexicanus 1. man* Philippines 2. heterotremus 1. 1985) P. 1991) Family Paragonimidae Paragonimus africanus 1. dog. dog. Hinz. dog. dog. ? bile ducts (Hinz. 1989. cat. 1990) 2. Bithynia Fish-eating mammals. Amnicola Fish-eating mammals. 1913) O. China. Russia.. Greenland 2. Japan. Snails Fish-eating mammals. cat. Pomatiopsis Wild carnivores. Portugal. 1992) quayaquiensis) Metorchis albidus 1. ? Pig. Crabs and crayfish small intestine (Asada et al. 1962. Radix Dog. fish-eating birds. dog.. dog. China. midge Mesenteric blood vessels (Lee. dog. Korea. 1969) P. sheep. Uganda 2. 1962) Family Plagiorchidae Plagiorchis muris 1. None Mesenteric blood vessel (Jordan et al. westermani 1. dog. sheep. man* Indonesia. wild Carnivores. Nigeria 2. cattle. man N. cat. None mesenteric blood vessels (Jordan et al. dog. Gabrielli Family Schistosomatidae Heterobilharzia americana 1.Table 7.. Japan. dog USA 2. rodhaini 1. man (once)* Cambodia. birds. Fw fish . None mesenteric blood vessels (Rollinson and Simpson. mansoni 1. 1993) S. man (once)* Small intestine (Milleman and Knapp. wild carnivores SW USA 2. skrjabini 1. Caribbean. Neotricula Man. dog. man Japan. Oncomelania Pig. Crabs (Liberonautes) small intestine (Asada et al. man* India. 1964) Family Schistosomatidae Heterobilharzia americana Lymnaea Rodents. cat.. mink. Burundi. 1987) S. Nigeria 2. sheep. S. China. cat. Continued. 116 Parasite Intermediate hosts Final hosts Distribution and location in host (reference) P. man* Japan. Afropomus? Palm civet. Snails. wild carnivores. Thailand. China. Salmon dog. None Rodents. dog.. Goniobasis/Oxytrema Fish-eating mammals. 1970) S. None mesenteric blood vessels (Bruce and Sornmani. 1989) A. Philippines. japonicum 1. Thailand. man 2. 1993) Schistosoma incognitum 1. mekongi 1. Tricula Asia. None Small intestine (Milleman and Knapp. Semisulcospira Primates. Lymnaea. Malaysia. buffalo. Rodents. 1965. fox. primates. dog Congo. Indonesia Snails. Russia 2. 1970) Family Troglotrematidae Nanophyetus salmincola 1. Crabs Lungs (Yokogawa. America 2. Laos 2. Thailand Pseudosucc-Nea 2. 1962) P. Thrasher. midge Mesenteric blood vessel (Agrawal and Shah. pig. birds. uterobilateralis 1. rodents. 1980) S. Lymnaea man. Biomphalaria Man. Korea. salmincola schikhobalowi 1 Semisulcospira Badger.1. Biomphalaria Man. dog Siberia 2. cat. man (larvae) Africa.F. dog*. 2. Haplorchis pumilis. In light taurant. The adults live in the mucosal crypts fered from upper abdominal pain. reliable data on infection with the dif- is habitually eaten raw. symptoms of high fever and abdominal pain.. pancreatic neoplasms. An adult Heterophyes has also been recovered from the Superfamily Opisthorchioidea: heart (Collomb et al. than 2. and intense griping pains. Twenty infec- Metorchis albidus and M. and the Mediterranean basin. 1990).. treatable with high doses Occasionally worms penetrate very deeply of praziquantel. sinensis and O. chronic infections can be associ. viverrini infections and and have almost indistinguishable. with a body covered ated with jaundice. fish-eating mammals including dogs. penetrate. Human infection with ferent species are lacking. wolves. wolves.0–1. minnow.g. distension in cats. felineus is listed as ‘not classifiable as to its They are mainly prevalent in South-East Asia carcinogenicity to humans’ (IARC. and in spines. in which they are responsible for lar Metagonimus yokogawai are the most com- cholangiohepatitis and periductular liver mon species which infect humans and dogs. 2002). with diar- gitis. foxes. cats) or birds (e.1). with excessive secretion of mucus. In the Nile . dogs. cans) and have almost identical life cycles. and very probably occurs with other species. have been recov- ered from the spinal cord. and develop in 2009). low-grade of the duodenum and jejunum. Europe O. These encyst in several species of freshwater such as dogs and cats. and a high eosinophilia. producing trans- The heterophyids are a group of minute her. in this case eggs may be car- ried and found in different tissues.. Because the infection only occurs occasionally except for eggs are difficult or impossible to differen- areas of Siberia. felineus is a common parasite of sweetfish) which. Muller. conjunctus are two tions have been reported from both humans flukes normally parasitic in North American and dogs (Table 7. with loss of motor and sensory maphroditic flukes usually measuring less function (see Guttierez. The latter species was responsible an accessory genital sucker near the ventral for infection in 19 people in Canada who suf. Crompton and Savioli. treatment (Maclean et al. nausea. 2002. Cancer of the bile ducts (cholangi. Heterophyes heterophyes and the very simi- and foxes.5 mm in length. who had all eaten sashimi in a res. when eaten raw or under- cats. 2010). and to a lesser extent dogs. Praziquantel was very effective in infections they are usually asymptomatic. containing a miracid- to humans’ by the International Agency for ium when passed out in faeces. O. cells and can be easily missed at necropsy. and abdominal rhoea.7 mm in length and They occasionally occur in humans who eat differ mainly in that the former species has raw fish. blood vessels. peli- but a less severe chronic phase (Muller. 1983. fibrosis (Wobeser et al. sucker. portal hypertension. as in the case of humans The Heterophids dying of congestive heart failure.g. mullet. small (26 × both agents are classified as ‘carcinogenic 15 mm) operculate eggs.g. pass on the infection. The adults live among the crypts of ascites (Muller. but human cooked.. 2002). jackals. but in heavier infections the clinical picture Amphimerus pseudofelineus causes cholan. tiply. may resemble that of amoebiasis. Dogs and Trematode Zoonoses 117 parenchyma. and pro- fever. Most species are this species is often accompanied by acute parasites of fish-eating carnivores (e. In Russia and East or brackish water fish (e. 1996). Location in the CNS and heart valves can be severe and might be fatal. lasting up to duce superficial inflammation and necrosis 4 weeks. They both measure 1. the small intestine attached to the epithelial 2007). In freshwater Research on Cancer (IARC) (Bouvard et al. the miracidia hatch. Eggs of another Family Heterophyidae species. verse myelitis. and after a few weeks release cercariae. 1960). where salted or smoked fish tiate. Cholangiocarcinoma is a major cause appropriate species of snails where they mul- of death among humans in endemic areas. ocarcinoma) is strongly associated with both They are all very similar morphologically C. but there is little information into the crypts close to large lymphatics and on its effect in dogs or humans. and After the usual multiplicative stages in the there is a high infection rate in children and snail. philippinensis in such as severe headache. or a stroke. been experimentally developed but are not Once an egg reaches freshwater a miracidium commercialized. 100 × 50 mm. Gabrielli Delta region of Egypt.F. from very mild The developing worm pairs in the lung to lethal (Chai et al. a cerebral tumour. and diagnosis by finding the eggs in the trachea and passed out in the sputum sputum or faeces. hetero. cavity and the subcutaneous tissues repre- Eggs of paragonimids. 1995). paragonimiasis is typically associ- ated with considerable morbidity: the most The paragonimids are almost globular her. the metacercarial larvae excyst detection of eggs from faecal examinations and reach the lungs after penetrating through is commonly reported. 2012). cough. The most common are P. sensory the Philippines. dyspnoea. is particularly likely to cause cerebral parag- 1995. provoke inflammatory and granulomatous reactions around them to form a cyst which can be in communication with a bronchiole. cats. partially cooked. about 12 mm in length and 6 mm in width. 2010).. and motor impairment. are produced by the adult Treatment is with praziquantel or triclaben- worms in the lungs and are conveyed up dazole. and monkeys) throughout the the rarer. rusty sputum with small suckers and symmetrical lobed is a classical finding. The organs or the wall of the abdominal South America. . Dogs. immunological tests have or are swallowed and escape in the faeces. ophyidae are common in areas of South-East marinated. in the Philippines and rats are the most frequent natural hosts. in rice wine before eating. human infection with l arvae develops inside it within a few weeks. uterobilateralis and P. the diaphragm. along the soft tissues to the brain. measuring about sent other sites of ectopic paragonimiasis. P. When the infected crus- Many other species of the family Heter tacean is eaten raw. occurring when larvae migrate out of uncooked. and P. more clearly zoonotic species. In China ‘drunken crabs’ are steeped tinal flukes’ (Sripa et al. Fully formed cysts measure about 20 mm in The Paragonimids diameter. seizures. Many healthier than in the latter infection. pickled. or poorly Asia. and enters a suitable species of snail. Heterophyes is associated with eating pickled emerges. juice is used as a cure for measles in children. They often mistaken for tuberculosis (Toscano et al. westermani in South-East Asia (Toscano et al. human infection caused by also dogs. smoked. bling epilepsy. 2009a).. but In general. although the patient appears to be ceans act as second intermediate hosts. mexicanus. a condition more common in chil- of the world where crustaceans are eaten dren. and pneumothorax. Many other species which can also the lungs. mullet at the feast of Sham-al-Nessim. africa. crab juice is a delicacy. capsule. as this is the main part onimiasis. and cognitive disor- nus in Africa. and lung referred to by the generic term ‘minute intes. Fürst. while in Korea crayfish these infections are characterized by a vary. tremus in South-East Asia. They are frequently the intestinal wall. a New World species (Table 7. salted.. live in pairs in cysts in the lung. common presentation is that of a chronic pul- maphroditic trematodes. dried. mexicanus in Central and ders. ter crabs or crayfish. species occur in carnivores (mainly felids. P.118 A. Such clinical picture is testes in the posterior part of the body. tends world but most of the estimated 22 million to have worms occupying ectopic locations: human infections are caused by Paragonimus P..1) can be distinguished and become foci for abscesses. most measuring monary disease with fever. chest pain. the cercariae emerge and enter freshwa- young adults. and crusta. ing degree of pathogenicity. Even Superfamily Plagiorchioidea: though early or light infections can be asymp- Family Paragonimidae tomatic. Cerebral para- by (often slight) morphological and life-cycle gonimiasis gives rise to symptoms resem- differences.1). infect humans (Table 7. pigs. where expulsion of adult worms or processed. Eventually the contained worms die and the cysts become fibrotic and calcify. bonnei were in the faeces and the miracidia which develop recovered from 15% of inhabitants.. Infection follows ingestion of parasite- and the Americas are rarer than in Asia. few months. there is (Procop. fatigue. since the which is caused by a rickettsial organism. mammals. Wild carnivores act as reservoir host liver). 2009). westermani and P. 1992). 1994). albenda. and a high eosinophilia but treatment with fenbendazole. found in man is intestinal. These conditions sometimes resolved. They differ from Lecithodendriids (Superfamily Plagior the paragonimids in that the genital pore is chioidea: Family Lecithodendriidae) are posterior to the ventral sucker and there is a usually intestinal parasites of insect-eating cirrus sac. In dogs. of salmonid raw. worms do not usually develop fully in them. and infected fish. Eggs are passed out region of Thailand. There has also been one case of infection Superfamily Plagiorchioidea: through handling fish (Harrell and Deardorff.1). Family Troglotrematidae 1990). and the live in fast-flowing mountain streams. Dogs and Trematode Zoonoses 119 Susceptible species of crabs and crayfish multiplication occurs in the snail. or praziquantel were all effective (Dubey. Symptoms usually resolved after a zole.. ‘Salmon poisoning’ results in a haem- and domestic animals. but can also cause infection in humans vomiting. triclabendazole has also but the possible role of a rickettsia was not shown to be effective. molenkampi has also . Diagnosis infections with paragonimids in dogs. and adults inside the egg then hatch in freshwater and of Prosthodendrium molenkampi from 19% penetrate suitable species of snails. Consequently human infections in Africa fishes. to North America. P. and in cercariae which emerge form cysts in various most parts of the world these are not eaten tissues. anorexia. A 4.2% human infection rate has been reported from a focus on the lower Amur River This group is related to the paragonimids and in Siberia (Bernshtein et al. and 1989).. Following ingestion of raw or saccular bronchial dilatations after 2–3 weeks. (43%). some patients often with pneumothorax and distinct air. the remote areas. and is usually non-pathogenic. It is a parasite of wild 1970).g. although the one species occasionally for both humans and dogs. in Russia and the United States suffered from filled cavities measuring 20–30 mm after 4 diarrhoea with weight loss. tract (occupying body sinuses. kellicotti is the only species endemic atode acts as a vector (Milleman and Knapp. birds and canids region. for which the trem- P. In a United States (Table 7. Treatment most species do not inhabit the alimentary with praziquantel is effective (Fritsche et al. particularly the kidney. paratenic hosts for cats and dogs.1). particularly bats. insufficiently cooked salmon. One case also had a high fever 1979). P. kidney. vomit- weeks. a thorough review of cases of a high mortality occurring 10–14 days after paragonimiasis that occurred in the United infection. X-rays showed susceptible. A cough is typical of investigated (Eastburn et al. Neorickettsia helminthoeca. heterotremus parasite is known for its association with can also infect rodents and these can act as ‘salmon poisoning’ of dogs and other canids. measuring about 80 × 45 mm. Asexual (Radomyas et al. nausea. anorexia. Phaneropsolus is the only genus regu- (including red foxes and domestic dogs) larly found in man and dogs. More recently. although there in Siberia and the Pacific north-west of the are other occasional parasites (Table 7. adults of P. They are minute Nanophyetus salmincola is an intestinal flukes recognizable by the fact that the parasite of fish-eating wild carnivores (e. occur predominantly in individuals from However. ing. 1987). in both hosts is by finding the characteris- tic unembryonated eggs. and lymphadenopathy. cats. in dogs in the United States. The rickettsia has not been reported States has been recently conducted by Fried from humans but it is possible they may be and Abruzzi (2010). Prevention is by not eating raw or The Troglotrematids smoked salmon and not feeding it to dogs.. including dogs and orrhagic enteritis with high fever. gonads and vitelline body are in the forebody wild bears and raccoons). in the faeces. bats). In the definitive host. and midges (Coombs and Crompton. as second intermediate hosts. P. and there chestnut. there is anorexia. which can be many hundreds. or because there is no second animal intermedi. particularly those of dragonflies. dragon. The second intermediate hosts for albendazole. Indonesia. measuring about 100 intestinal worm. vespertilionis have inflammation and ulceration of the intestinal been reported from the intestine of man in mucosa with excessive production of mucus. measuring appears unlikely that dogs are the normal 130 × 80 mm. Family Fasciolidae The most characteristic feature is the pres- ence of a collar behind the oral sucker with These are large spiny trematodes with a flat.. They are about 3. and intestinal colic . but large numbers of Plagiorchis harinasutai. attach by their suckers to the wall larvae in water or on edible vegetation. Most spe- known members of this family. the cattle cies are parasites of birds but some are natu- and sheep liver flukes. in some parts of the world. their teeth. gigantica.1). The best Both suckers are well developed. water ulceration at the site of attachment. Thailand.. Korea. cause P. philippinensis. Treatment is by praziquantel or 1992).g. tened body and deeply lobed testes. The large adult worms. Gabrielli been reported from Laos (Chai et al. water hyacinth. including snails. and watercress may be diarrhoea. Some of these. fish (Table 7. 2009a): others are fed to pigs. the cercariae forming metacercarial infections with mature worms produce an cysts on water plants. and measure a few millimetres in length. are eaten by people in many parts of Asia Larvae. includ. Superfamily Echinostomatoidea: Family Echinostomatidae Echinostomes are all parasites of the small The Fasciolids intestine. presumably the parasites infect that are fertilized by untreated pig or human humans in areas where insects are eaten as faeces. Japan. muris. heavy ate host.0 mm in length abdominal pain. 2009b). Fasciola hepatica and ral parasites of mammals and most also have F. although it is difficult to tell them important reservoir host for this trematode apart. and possible facial oedema and are natural parasites of mammals feed. nausea. followed by the buffalo. ing on aquatic insects (e. Pathogenicity is Transmission is particularly intense in areas unknown. 1991.F. The most × 65 mm. they have also occasionally been ing the outer covering of fruits or nuts with recovered from dogs (Dalimi and Mobedi. They have an oval or elongate body Superfamily Echinostomatoidea: and the tegument is covered with spines. can be important human parasites a wide host range. The Echinostomatoidea flies. measuring up delicacies or by accidentally ingesting insect to 70 mm. a single or double crown of longer spines. dogs only addition to the snail first intermediate host) rarely becoming infected. bonnei. mosquitoes. pass out in the faeces and on definitive hosts for P. due to toxins produced by the parasite.. although a number of species have been shown to be variously involved in the parasite’s life cycle. The eggs. nausea. It of the small intestine. The only member The characteristic eggs of echinostomes found in both humans and dogs is the giant are relatively large. worms. humans and dogs are probably freshwa- ter fish. acute Philippines. Chai et al. wild mice and Children in particular get infected by remov- cats. and P. 2007). javensis. amphibians. P. act (Chai et al.120 A. inflammatory reaction of the mucosa and ing the water bamboo. The second intermediate hosts (in is the pig. This is primarily are large edible types of snail. reaching freshwater a miracidium develops A number of plagiorchids (Superfamily inside within about 1 month. Light infections Plagiorchioidea: Family Plagiorchidae): are often asymptomatic. nor is it known how the final hosts where water plants are cultivated in ponds are infected. Fasciolopsis buski. water caltrop. and the Clinically. worth remembering here Echinostoma hortense the mesocercariae migrate to the mammary and E. pies. This has seri- Family Diplostomatidae ous implications for zoonotic human infec- tions (Shoop. ante. alata is a European species frequently nae has been elucidated from experimental found in the small intestine of wild and infections in carnivores and rodents (Shoop domestic canids feeding on frogs. b. weasels. potentially very dangerous ones. life cycles Mesocercariae have also lodged in the eyes of and are often considered as the same species. cercariae form metacercarial cysts in fish or He was thought to be suffering from gastric amphibians. malayanum. The frogs’ legs while hiking (Freeman et al. and penetrate and multiply in suitable infection is mainly related to the consump- species of snails (probably including Heliosoma tion of undercooked wild boar meat that con- spp. cats. In the neonates the parasites develop into adults. lungs. causing neuroretinitis but Pearson and Johnson (1988) regarded (at least in the former). If eggs is similar to that of other Alaria spp. act as carrier or paratenic hosts by ingesting site of dogs in Canton and was first reported tadpoles. and from faeces reach water. both humans and dogs. in about 20 days. flu but died 9 days later from extensive pul- Alaria americana and A. sites of carnivores in North America. found to have mesocercariae in many tissues. Human out. plex excretory system. 1994). and India.. unusual. producing eggs snails (e. red foxes. A fatal case tion. ried out by Fried and Abruzzi (2010). Dogs and Trematode Zoonoses 121 in the morning. parasites in both dogs and humans. both have very similar. marcianae are two monary haemorrhage. relieved by food.. Treatment is with the penetration glands. the miracidia hatch larvae have been found in humans. China. . After developing into metacercariae in Indonesia. They both directly and by the circulatory system. Infection is the lungs they are coughed up and become contracted from eating uncooked large edible adults in the small intestine. and at autopsy was very similar species which are intestinal para. The life cycle of (presumably) A. carnivores. Smyth. Most are parasites of birds. they are rior portion and a cylindrical posterior por. A. both of which are common glands and infect suckling kittens or pup- in east and South-East Asia. When these are ingested by young from prisoners in jail in Manila in 1907. Malaysia. Basically.). Adult frogs and snakes Echinostoma ilocanum is a common para. Among the other echinostomes in the small intestine but cause little dam- whose natural definitive hosts are dogs. mesocercariae penetrate through Occasional human cases have been reported the intestinal wall and diaphragm to reach the since from the Philippines. but a more com- with praziquantel. where They probably penetrated the stomach wall they are found in raccoons.g. in pregnant cats and dogs. The process was termed ‘amphiparatenesis’ The Diplostomes by Shoop (1994). marcia. Cercariae which emerge develop in tains the parasite’s metacercariae in muscle or amphibian tadpoles where they develop into fat tissues (these are also known as Duncker’s an unusual larval stage known as a mesocer. 1976). but members in Canada occurred in a man who ingested of the genus Alaria parasitize mammals. it is not always clear which species is being occurring in the United States has been car- referred to. muscle flukes). americana and A. Its life cycle and Corkum. However. Symptoms are usually mild caria. In this group the body is divided into two While A. 1983a. 1995). An extensive review them as distinct. Thailand. it is age. with a wide flattened. A pregnant callitrichid monkey has been infected experimentally Superfamily Diplostomoidea: and a similar situation ensued. 1990). this is an enlarged cercaria (Shoop. The adults attach to the villi cercariae. Thus in the older literature of human cases of infection with Alaria spp. They can continue to infect subsequent litters until the larvae are all depleted. and occasionally dogs. and migrated to the lungs and other tissues badgers. Pila or Vivipara) containing meta. marcianae are rare regions. concave. Genuine human infection. El Ghissassi. (2009) Georgi’s Parasitology for Veterinarians. Gabrielli A. (1989) Paragonimus mexicanus y paragonimiasis en Mexico y America. Mexico City.. Y. 1922. Morita. 9th edn.). amphibians. because larly in dogs are spurious. Meditsinkaya Parazitologiya I Parazitarnye Bolezni 2. regions. H. so far. A. Note Adapted from the first edition.. Shoop et al. and human prevention is become infected by ingesting ants containing by thorough cooking of fish. written by Ralph Muller. Universidad Nacional Autonomia de Mexico DF 04510. T. or streams called lancet fluke infection. Molecular and Biochemical Parasitology (Suppl. and Okahashi.L. most of these parasites. has been carried out by although. D. 512–516.N. 321–322. 627. Straif. There has been one reported human case. PhD thesis.. Otagaki. fishermen. which utilizes terrestrial snails as inter- mediate hosts. and a high eosi. Bhaibulaya.C.D. R. Le Bailly and Bouchet (2010). (1989) A review of Schistosoma incognitum Chandler 1926. V. nasuae has been identified in wild A historical review on information available carnivores and in domestic dogs in Mexico on Dicrocoelium spp. Japanese Journal of Parasitology 11. R. Bouvard. T. Sakai.. canals. Baan. Karablev. also is by not entering ponds. Saunders Elsevier. 239–251.F. Y. 1989. Asada. Grosse. biliary tree disease. Conclusions tle.. V. Avoidance of schistosome infections infected liver.S. Missouri. Saint Louis. not in humans (Shoop. .L. (2009) A review of human carcinogens-Part B: biological agents. M. and farmers. Bowman. 25–27.122 A.. It is probable that nearly as important as reservoir hosts for most reported cases in humans and particu. nophilia (Mohamed and Mummery.. (1982) Zoonotic helminths of Thailand. Herbivores dietary habits. Kojishi.L. Takeuchi. Prohemistomum vivax (Superfamily Strigeoidea: Family Cathycotylidae) is a parasite of fish-eating birds reported from The Dicrocoelioidea Egypt and Japan.. Argumedo. Secretan. Bernshtein. or snakes. L. crustaceans. Mexico. Nanophyetus): clinical and parasitological study and first trial of Azinox in the lower River Amur focus [Eng.. summary]. D. Lancet Oncology 10.M. K. particularly for children. follows ingestion containing cercariae released from snails: not of infected ants and results in disturbed liver an easy task for humans living in endemic function. Dogs are not the chances of ingestion. when 2000 adult worms were recovered from the small intestine. et al. C. W... (1962) A case report on the human infection with Plagiorchis muris Tanabe. Helminthological Abstracts 58.B. metacercariae which alter the ants’ behaviour snails. K. Snails ingest the parasite eggs It is clear that infection with all trematodes containing miracidia and release cercariae apart from the schistosomes is based on which are then ingested by ants.. J. B. the eggs having they are not as likely to eat these intermediate been found in the faeces following ingestion of hosts. Benbrahim-Tallaa. or for dogs. H. 1990). M. and Shah. (1992) Intestinal trematode infections (Metagonimus. and possibly so that they attach to grass leaves and increase by avoidance of eating insects. and Yavotskii.. 1989). F. 1 References Agrawal. This chapter has been submitted in his memory. and it has Superfamily Dicrocoelioidea: been found a few times in dogs. Family Dicrocoeliidae Dicrocoelium dendriticum is a cosmopolitan parasite of the biliary ducts of sheep and cat. as are cats. Y.L. (2009b) High prevalence of Haplorchis taichui.P. M.. . 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Leck. oligarthrus. being transmit. of Echinococcus. wolves that started to cohabit with humans plex of species and sub-species which is made a smart choice. multilocularis. ingly recognized as a source of human infec- ted through the inadvertent ingestion of eggs tion with E. 2000. 8 Dogs and Cestode Zoonoses Calum N. canadensis. main definitive hosts of E. Possibly four species. Both CE and sion of over 60 zoonotic infections (Baxter and AE are of major public health importance. including Echinococcus sion of E. granulosus small population of wolves. Felids are the granulosus and E.) 127 . dogs play no part in the transmission of Dipylidium sp.000 years ago has undoubtedly been of great benefit to humans. ortleppi. Zoonoses and Public Health. vogeli to humans. E. vogeli and E. 2Section for Veterinary Epidemiology. granulosus): E. multilocularis. (until recently today compared to the patchy distribution and all considered to be E. E. The dog is the main definitive host of iour plays a pivotal role in the perpetuation of E. 1984.N.. Grenada. and mon Echinococcus spp. St George’s University. oligarthrus. 1975). multilocularis causes human their unwitting participation in the transmis.. to less com. and dogs are becoming increas- zoonotic importance in humans. e-mail: cmacpherson@sgu.. equinus (previously of human society. intermedius.. Macpherson1* and Paul R.L. E. Macpherson et al. The genus Echinococcus comprises a com- tive. granulosus. to strays and feral dogs cosis (CE) in humans. alveolar echinococcosis (AE). 14. The diversity of breeds of E. ortleppi. and some which live a precarious existence on the fringes wild animal species. This chapter reviews the complex role are geographically limited to Mesoamerica dogs play in the cestode zoonoses. Switzerland The domestication of the dog some 12. The human:dog sensu stricto. further. Spirometra spp. University of Zurich. canadensis may cause cystic echinococ- cosseted lap dogs. granulosus horse strain) appears to trans- dogs and uses to which we put them may lead mit between equids and dogs and is not to their exposure to infectious organisms and zoonotic. 2005). E.edu ©CAB International 2013. 2nd Edition (eds C. E. Diphyllobothrium spp. Torgerson2 1 Windward Islands Research and Education Foundation. Dogs play a role in the transmis- health point of view. tous distribution of dogs around the world 2008). From a Darwinian perspec. and this species. and tapeworm or cestode infections in dogs and their E. livestock. undergoing taxonomic revision (Thompson. which will not be considered Mesocestoides spp.000– Echinococcus spp. and relationship may be as close as pampered and E. with a and South America and rarely cause disease focus on the most important from a public in humans. E. * Corresponding author.L. intermedius.. Unknown East and southern cape buffalo. North America) worm within – different breeds occurs. Africa. New Zealand. Sri Lanka. Sheep. granulosus Definitive Intermediate Infective Geographic species strains (genotypes) hosts hosts to man distribution E. Eastern Europe. These are most commonly world. jackal. intermedius Camel strain (G6).R. Wolf camel. and are types. (Gemmell et al. goat. South America? E. G2. sheep. The prepatent period varies E. but in most endemic regions in developed countries Although susceptibility between – and even (Europe. 1995). dog Cervids Yes. G3) dingo. of an enor. previously recognized as strains of hermaphrodites. camel. Pig strain (G7). Iran. buffalo. Russia. and the suckers attach to The taxonomy of E.. and to a lesser tial of the parasite. Torgerson Echinococcus granulosus (Batsch 1786) evaginate in the small intestine. E. the survival of the parasite in areas where the mous range of domestic and wild mammalian climatic conditions are inimical to the survival intermediate host species. Yes Europe. 1991). are likely to be separate species between 34 and 58 days (Thompson. ortleppi Cattle strain (G5) Dog Cattle. G10) relatively North America benign E. China. This would be useful for extent in any other internal organ.1). North hyena. (G9) Nepal Central Asia. The adults grow undergoing revision and a number of geno. Much heavier worm Dogs and other suitable carnivores become burdens have been reported in dogs living infected when they ingest protoscoleces found in many of the less developed regions of the in hydatid cysts. Yes Middle East. South Africa. buffalo. which must increase the biotic poten- found in the liver or lungs. goats.128 C. canadensis Cervid strain Wolf. Dog Pigs. fox. but Northern Eurasia. granulosus. Nepal. macropods Australia E.1. goats India. Africa wildebeest . granulosus Sheep strain Dog. Latest proposal for the taxonomic revision of E. The protoscoleces of the eggs (Wachira et al. (G8. granulosus. granulosus. granulosus is presently the base of the intestinal villi. and the ros- and Other Related Species tellum of the scolex attaches to the base of the crypt of Lieberkühn. to a length of between 2 and 11 mm. globally dogs burdens of around 200 are usually found are definitive hosts par excellence for E. pigs. Macpherson and P. 1987). felidis Lion strain Lion Warthogs. Worm burden Dogs as definitive hosts of The mean worm burden in dogs varies con- Echinococcus granulosus siderably between endemic localities. based on molecular evidence (see Table 8.N.L. zebra. equinus Horse strain (G4) Dog Equines No evidence Europe. Eurasia. cattle Africa. South Africa. Previously Proposed recognized Echinococcus E. and South America. Heavy worm Table 8. cattle Yes Cosmopolitan: sensu stricto (G1. Argentina E.. Middle East. 122 (44. with but is possibly 1–2 years. 1991). 54 Taenia hydatigena have been shown to move (19. the mean worm gevity of the adult worm in dogs is unknown burden in 57 infected dogs was 1844. quently and have short life spans (Matter and The mechanisms for the dispersal of eggs Daniels. 1985). and wild dogs in general tend to have birds... 1995).5%). Ouhelli et al. and 98 (35. it has many Egg production may be synchronous or asyn. 1987). of a number of factors. faecal mass to dispersal by water.7%). 1990). 2001). and Lawrence.0033 of these eggs develop into by a slaughterhouse worker (Kamhawi and viable cysts (Gemmell et al. has been shown to be continuous (Lahmar nutritional. flies bour over 300. Although this method is highly specific. over 60 km upwind by the activities of birds medium (201–1000).. where of 274 infected dogs exam. Heavy worm burdens have not been reported from all dry Identification of infected dogs may be impor- endemic regions and have not been reported tant for diagnostic. tively (Gemmell. 1997). In the hot. Dogs and Cestode Zoonoses 129 burdens may exist due to a range of host factors roughly every 2 weeks. Ibrahem and trol programmes necessitate consideration Gusbi. In Tunisia the mean worm burden of Diagnosis of Echinococcus infected dogs has been recorded at over 2000 granulosus in dogs worms (Lahmar et al. burdens. 1991). and survival years using arecoline purgation. 1992). arid regions of the world tate heavy worm burdens in dogs. Diagnosis is most effective dogs was 219 (Ouhelli et al.467 in a dog fed offal a day and 0. The heaviest infected dog in this study harboured 15. These range from the In Australia an infected wild dog (domes. drawbacks including poor sensitivity. respectively.4% of the dogs having burdens of >1000 worms (Molan and Baban. with proglottids being produced is biohazardous and logistically problematic . Most eggs remain within 180 m of their heavy worm burdens (Jenkins et al. 61. dogs have been shown to produce 8470 eggs est worm load was 16. Egg production may including their heterogeneity. movements of the proglottids away from the tic dog and dingo hybrid) was found to har. 2000) and would result in a largely are unclear but are likely to be a combination immunologically naive population. The lack of et al. genetic. 1998. 1992.. At temperatures of Fertility of hydatid cysts in Turkana is high over 40 °C survival is only a few hours. and it chronous. The lon- Abdel-Hafez. and heavy (>1000) worm and insects (Torgerson et al. to susceptibility reach over a million a day. 1981) which would facili. is prolonged if the eggs are in water (Wachira stock (Macpherson. 1983) and live. by autopsy and examination of the small intes- tine..182 worms. 1995). In Iraq. In Morocco of quantification of canine echinococcosis the average number of worms in 34 infected (Gemmell. which is also the only accurate method of recording worm burdens. and other host factors. 1997). eggs of ined in the Turkana District. wind.8%) had light (1–200). deposition but under certain circumstances Heavy infections have also been reported eggs appear to be able to disperse over con- in Kenya.000 adults which ture and relative humidity. dispersal. siderable distances.. Infected Levant country of Jordan where the heavi. Expulsion of eggs to infection due to immunological. respec- small intestine (Macpherson et al.. Almost all hydatid con- East (Eslami and Hosseini. and other insects and 1991). but both in humans (Macpherson. Heavy transfer of eggs from dogs to intermediate worm burdens have also been reported in the hosts must be rapid to be successful.. 2001) and last for at least 80 days (Heath dog control measures where dogs breed fre. 1997. et al. Ante-mortem diagnosis has been carried out for many Egg production. (especially blowflies). epidemiologic.000 worms (Jenkins and Morris. or control/ in most north African countries or the Middle surveillance reasons. Many of the heavily Egg survival is dependent on tempera- infected dogs had over 50.. For example. At 7 °C and 21 °C completely carpeted the entire length of the eggs survive for over 200 and 50 days. 2000). 1977). . et al. area including Southern Europe. Peru.N. Australia. Provinces of Rio Negro.. Tajikistan and Turkmenistan) (Torgerson et al. This form is a major public health and in dogs (Allan et al. They also occur in (Dinkel et al. The development of Echinococcus spp... Perdomo et al. multilocularis and Bolivia (Ramirez.. 2011). 2000. nomadic community dogs in north. 1992. Coproantigen positive rates ranged Wachira. Specificity is North American continent and Eurasia. granulosus and Tierra del Fuego) (Frider et al. including Uruguay (Carmona tinely. Central Asian Republics (Kazakhstan. Russia. 1992. 1998). Sadjjadi. granulosus and E.. Eastern Europe (Bulgaria. 2000). and the high sierra areas of Chile. 1999. and Tanzania and in the rural areas feral dogs and dingoes in Australia (Jenkins of Nigeria and South Africa (Macpherson and et al. and host species directly from faecal samples 1995... the simultaneous detection of E. and Treatment of Echinococcus parts of China (Craig et al. Argentina (in the Patagonian than species specific. Kyrgyzstan. Wachira et al. tion. and Morocco (Dakkak. Jordan... 2006).. Jenkins Libya. 2001). Rausch.. Deplazes et al. Another focus occurs in Africa south west China (Wang et al. and an excess days post-treatment..R. burdens are greater than 50. wide. Differentiation between foci are also known to occur in the sheep- E. where a relatively high preva- to 6 days (Jenkins et al. granulosus occur world- 2008). The tions are detectable by coproantigen ELISA. Tunisia. has improved the capability of sensitive and highly a nearly cosmopolitan distribution (Rausch. lence in defined geographical areas has been tigen ELISA for E. Infections with E.. 1993. multilocularis by coporan. importance The sensitivity of arecoline purgation has been reported to be as low as 37% (Ziadinov et al. Craig et al. 2000). 2000)... El-Shehabi et al. 1990). coproan. The drug is There are three broad categories of dogs in well tolerated by dogs and to date no drug this region of the world: feral or stray dogs. resistance has been reported. granulosus has been used to reported.. Coproantigens remain of 1 million disability-adjusted life years stable in formol saline preserved samples and (DALYs) (Budke et al. Williams et al. Sudan.. 2006).130 C. include the whole Mediterranean screen sheep farm dogs in Wales. north Africa and in the Middle East to herd . 1994. Thompson et al. A so-called European form.. 2006). Chubut. 1995.L. Egypt. stray dogs in of the Sahara in the semi-arid areas of East Spain. primarily coproantigen ELISA tests has dramatically involving synanthropic hosts in its cycle. Wen granulosus in dogs and Yang. given in a single oral dose of around 5 mg/kg body weight. used particularly in fection may occur not long after treatment.. global burden of CE is substantial. including Kenya.. Romania. specific ante-mortem diagnosis of E. 1997.. Poland). rearing countries of South America (Moro and tigen detection is presently not possible rou. Thompson. Magambo et al. with as and antigen levels return to normal within 5 much as $2 billion lost annually. 1992. and Peru (Cohen et al. Schantz. 1998. (Stefanic et al. 2009). 1997). Uganda. 2010.. Deplazes et al. 1996).. and around 96% and sensitivity >80% when worm is probably the archetypal form (Rausch. Santa Cruz.. Uzbekistan. 1979. 1993. granulosus 1993).0% to 46%. Macpherson and P. Large from <5. A PCR-based DNA detec. working sheepdogs. 1971). 2006). Moro et al. Africa. 1997. 1999. and Ethiopia. 2008. Pre-patent infec. 2008). 2006).. Mongolia. Regions with good also in faecal samples left in the ‘open’ for up documentation. Schantz et al. Schantz et al. 2004) and a real-time multiplex. Wang et al. 1997. 2006).. Epidemiology and public health 1997. Palmer et al. Uruguay. Since the 1970s the treatment of choice has Africa and the Middle East been praziquantel.. 1991. Brazil (Rio Grande do nested PCR system has been developed for Sol). 1995. as most assays appear to be genus rather et al. Praziquantel is which usually comprise the largest popula- metabolized within 1 h and consequently rein. tion assay has been developed for E. Torgerson with up to 20% of dogs failing to purge (Craig.. To date. 1988. economic problem in northern parts of the Torgerson and Deplazes. 1992. and Nepal (Baronet et al. and feeding the Macpherson et al. Dogs and Cestode Zoonoses 131 sheep. CE patients in Beirut were 21 times more roam freely with stray dogs. and pet dogs which are kept mostly children below 15 years of age. Abu Dawood. One study in Jordan demonstrated appreciation of the life cycle of the parasite an association between contaminated water by abattoir workers.. there thought to be over 3 million dogs in Morocco are usually no veterinary and scarce medical (National Laboratory for Epidemiology and and educational facilities. and Middle A history of dog ownership has been Eastern countries. together with strays. particularly for religious and spe. and food for tion of just over 26 million. In Morocco. tors. Home definitive hosts in addition to domestic dogs. Dogs spend is essential to wash it seven times’…‘Angels most of their day in their home area but are do not enter a house where there is a dog’… rarely trained or shown affection. In such areas droughts are com- regularly have contact with dogs... granulo.. There have ‘The Prophet has ordered the killing of dogs.. and dog dog’ – sayings of the Prophet Muhammad. or a sheep or cattle in any of the sub-Saharan countries. 2003. Levant.. Nevertheless In urban areas dogs living close to abattoirs Muslims still find that dogs are useful or are often infected with E. and the lack of infra. women. Christians and Druze people. the main sources of infection for livestock and 1964). feeding of infected of prevalence studies have been conducted in offal to dogs was found to occur in all areas different countries and these are presented in and since between 70% and 90% of owned Table 8. is thought to be a risk factor The generally high prevalence of E. little Zoonoses. so infected offal is invariably out the Middle East and in North Africa fed to dogs. there are large numbers of stray dogs. meat inspec.. and shelter availability (see Chapter 2). and this increased contact may be hold pets with no other function. et al. knowledge about the parasite. Stray dogs partly responsible for the higher incidence of usually are not very visible during the day. et al. 1997). populations are therefore restricted by food. The use of dogs for hunting wild pigs by humans (Kamhawi and Abdel-Hafez. As in North Africa and the Middle dogs are allowed to roam free. A number not enforced. there are a structure and the enforcement of regulations number of wild carnivores which serve as governing disposal of infected offal. and in this mon. In the hyperendemic focus among and so are kept in large numbers: there are the nomadic pastoralists of East Africa. owned pet dogs are not shown to be important in some areas. no abattoirs... 1991). 1993).2. In many north African. 1995. as than other Beirutis (Abou-Daoud and Schwabe. granulosus (Wachira even essential to guard the home or livestock. offal to the dogs. related by Muslim. CE among women compared to men (Kachani but emerge at night to scavenge from rub. dogs is scarce. 1999). increasing the incidence of CE amongst these sus in dogs in North Africa and the Middle groups compared to Arabs in Israel (Yarrow East is thought to be also due to a lack of et al. Al-Bukhari. et al.. water. 2000). and dog owners. Very few dogs are considered as house. 1993) which has a human popula. In sub-Saharan Africa. Ahmed. been few attempts to control their numbers except for a hunting dog. 2004. The religious teachings scavenge. there exists East. but it is unlikely that any of these wild species cial ceremonial events. Dogs are maintained for guard- of Muslims advise that dogs are impure. For exam- restricted to the home area and are allowed to ple. Children through. and it is thought that animals that die in region CE has a relatively high prevalence in huge numbers during drought years are very . supplies and human CE (Dowling et al. Ouhelli bish dumps and around human settlements. slaughter. ‘If a ing from intruders and wild animals but are dog licks from the utensils of anyone of you it not generally used for herding. and Al-Behaqi. 2003. occurs throughout the play an important role in human infection region and at such times meat inspection is (Macpherson and Wachira. Responsibility for guarding property and in rural areas to for feeding and looking after dogs in Morocco protect against wild animals (see Chapter and in the region in general is usually left to 1). ample opportunities for exposure to infection and most owned dogs are free to roam and (Ouhelli et al. 1997. 1997). Ouhelli et al. Shambesh et al. 1992. Macpherson et al. butchers. 1997). Many authorities likely to have had a history of dog ownership consider these dogs. (Macpherson et al... rapid expansion of the infected dog popula. Pakistan. 1989a a Review.9 Moch et al. 1974 510 1.. 1983). including Xinjiang.. the continue to be associated with nomadic. India to Iran. 1983.R. 1999. 1986 21 Lahmar et al. host of E.2–6.6 a Ibrahem and Gusbi. Nepal. larly in the towns and cities.4 Troncy and Graber. 1995. the dog is the principal definitive tion (Macpherson. six provinces or autonomous with women in particular (Watson-Jones and regions. granulosus eggs survive huge area of grazing steppe and montane longer (Wachira et al. 1997 Tunisia 348 22. Siberia.. granulosus (Budke et al. and settled pastoral communities.. 1992. 1989b). the use of water et al. summarizing data from numerous sources important for creating ideal conditions for the Asian Republics. Shaikenov et al... 1980 Somalia – 23 Macchioni et al.L.5 Dada. Ningxia. Torgerson holes for drinking water to which dogs have et al.3 a Ouhelli et al. 1969 Kenya – Turkana 695 13–63.. Inner Mongolia. Ningxia. and a close association of dogs In China. 1994. and Tibet have the tions for the continuous transmission of the highest reported prevalences of CE (Craig parasite in this region.. 1962 Tanzania – Maasailand 10 60 Macpherson et al. and Quinghai (11–47%) (Yan.6 Eisa et al.. semi- preparation of food where dogs lick up the nomadic. the central lences of between 8% and 19% in western . Country – location Dogs examined Percentage dogs infected References North Africa Algeria 172 9. Kazakhstan. Yang.N.2. through Arecoline puragation has revealed preva- Mongolia. 1951 Egypt 570 3. 1980 Nigeria (in general) 549 1. Qinghai. 1979 Dada.. 1997 1995 282 33. Wachira et al. From China (including Tibet). remnants. and where E.6 Hegazi et al. Macpherson.. 1990). Over this access. (56%)..132 C. 2003b. Autopsy surveys of dogs revealed high rates of infection in Xinjiang (7–71%).. 1979 Sudan – Khartoum 33 3 El-Badawi et al. 1986 – South 76 52.. 1979 – Central 25 51 Saad and Magzoub. and as shepherd and the prevalence of CE increases with age dogs in the vast sheep-rearing areas (Liu. 1993). 1991). Schantz A lack of hygiene. Asia Gansu (27%). It is not surprising that et al. Additionally. particu- there is a continuous exposure to infection. 1985 – Maasailand 92 37 Ngunzi.. Reported prevalence of Echinococcus granulosus in dogs in Africa. 2008)..5 Macpherson et al. Ziadinov et al. 1997 Morocco (1920–1949) 331 1–70 a Ouhelli et al.9 Verster. 1993 Mozambique – Maputo 643 0.. 1979.7 Kilani et al. 1986 – Nairobi 156 10 Wachira et al.. 1987. Macpherson and P.5 Ferreira. 2001 No reference available No reference available Sub-Saharan Africa Chad – Central 117 3...3 a Ouhelli et al. Dada et al. Zhang. 1997 (1979–1985) 103 48. 1988) allows almost ideal condi. Gansu. Dogs are used as guards. 1991) may be important pastures dogs have traditionally been and sources of human infection. 1985 South Africa – Pretoria 1063 0.. 1986 Libya 243 29.9 Senevet. Torgerson Table 8. 2005. Bhutan. canadensis) is mainly with working shepherd dogs having a greater maintained in a wildlife cycle involving risk of infection. In Kathmandu. granulosus has also been in some rural and urban areas up to 10. 1985). Moro and Schantz. had infection. most likely 1988). granulosus (sheep strain.. 1988. Nepal. In addi- their dogs compared to Han. Williams. them. antigen positivity 75.. as the studies relied upon arecoline stricto) was probably introduced to Utah by purgation and detection of serum antibod.. Between 48% and 93% of wild dogs. Infection then spread in infected by ingestion of raw offal from sheep. and 1. As is the case elsewhere in infected with E. who are mostly pastoralists. 2003a.6% (62/82). In this region home slaughter consisting of dingoes and dingo/domestic was an important risk factor. Dogs fed offal Australia from wild ungulates are the most important source of infection for humans (Himsworth A number of studies involving only a few et al.. In western Sichuan male dogs. In rural dog populations in Central Asian North America republics. This is likely to et al.. Dogs are (Crellin et al. 1982). freely and had access to livestock viscera. Hui. and infection dog hybrids. which are maintained in a trans dents of Perth. 1994). granulosus in Australia (Baldock et al. Ziadinov et al. granulosus infections. 1991). 1962). wolves as definitive hosts and moose (Alces alces) as intermediate hosts.. tion (Liu. 2006). intestinal worms.. Mongolian. (Grainger and Jenkins.. 2010.. the western states by movement of infected wild pigs.. suburban resi. or Uygur tion to a wildlife cycle wild dogs may also ethnic groups. A national control programme some of which were ‘owned’ by the community. Wolves animals have been undertaken on the role translocated from British Columbia and of domestic dogs in the transmission of Alberta to Yellowstone National Park were E. as deter. 2008) The cervid strain (E. a coproantigen New Zealand study revealed a prevalence of 5. Domestic dogs are rarely treated for to harbour E. found to have high rates of Echinococcus Jenkins and Andrew. and 1991.8% dogs in the rural areas and over 56% of dogs (3/171) domestic dogs from all areas of the city owned by professional rabbit hunters were (Baronet et al. 2005). 1993). 2005). Kazakh. have been found infected with rates in dogs were higher in pastoral than in very heavy E. Thompson et al. prevalences can reach 20% or more (Torgerson et al. In the Xinjiang in New South Wales (Jenkins and Andrew. 1996).7% (5/88) in domestic dogs living near the area of the city Fifty years ago approximately 10% of sheep- where livestock was slaughtered. Transmission occurs between sheep of dogs found infected include those belong.186 dogs were found 1993).. higher infection rates (Budke et al. 1996. and New South have correspondingly higher infections in Wales (Jenkins and Morris. be an underestimation of the true prevalence E. and is in a ‘maintenance of eradication’ phase (see domestic and street dogs were allowed to roam Chapter 14). and Aboriginal communities humant system employed by the Basque . Dogs and Cestode Zoonoses 133 Sichuan (Budke et al. mined by either autopsy or arecoline purga. Grainger and Jenkins. sheepdogs imported from Australia in 1938 ies to determine parasite presence. eliminated the parasite and the country now each apparently with its own ‘territory’. The limited data available suggest that the cervid strain.. Victoria Kyrgiz peoples. coproantigen tested prior to movement and Gasser et al. be responsible for both sheep and human and dogs that were allowed to roam. 1993.2% of recorded in wolves from this area (Foreyt domestic dogs are infected. E. granulosus worm burdens in agricultural areas. granulosus (Sweatman and Asia there were a large number of street dogs. 8. Uygur Autonomous Region between 1957 1993. 1985.. Thompson et al. and the large numbers of dogs used to herd ing to recreational pig hunters. Classes sheep.. or macropod marsupials. Thompson et al. 1990.1% of 27. and Queensland (Baldock et al. senso level. 2009). . In many instances human for example. toirs outside the major towns of Lodwar. Uruguay. The lakeshore after treatment was high (Cabrera et al. the shepherd dogs associated . CE is also sanitary role that they play (Watson-Jones found among native Americans who prac. Macpherson and P. Irshadullah et al. or from offal that is discarded (Ibrahem and CE is prevalent throughout Chile Gusbi. cycle. 1983). in the south of the country where active con. For example.2% in Arequipa (Moro et al. 1977). In most nomadic or herding are at risk from infection when they transhumant populations dogs are fed scavenge from dead livestock. There are no abat- (Carmona et al. be hazardous to the people preparing them as well as to the consumers (Schwabe.. 1984). 1961). of E.. In Turkana. ranging from a prevalence rate of tered at the temporary nomadic homes are 8–46% in Junin and 32–37% in Puno. Thus in some countries such as in India. CE is also common in cycles of E. with dogs gaining access to dis.. Food availability tise home slaughter in Arizona and New varies considerably. 1989. granulosus in areas where abattoirs were CE infection in Central America is rare present than in areas where they were absent and most probably maintained in a pig–dog (Moch et al. while only a few hundred miles east none ing sheep. 1997). 1996). 1974). Simoons. encampments..2% of dogs were the shores of Lake Turkana were infected found to be infected. abattoirs are not always appropriate for con- Most human infections in Peru are due to trol of E. 1985). Feeding of offal to dogs from human cadavers. and Lokichoggio. dogs are used for herd. in South and Central America Turkana 63.. but is especially common et al.R. 1997. 1984). In many countries poor abattoir condi.42% in In low-income countries conditions at Lima to 48. Reinfection 2–4 months (Macpherson et al. areas.5% of 263 dogs were found infected in the north-west of the district. Torgerson Americans living in the Central Valley faeces comprises an important part of the of California.134 C. Ouhelli (Arambulo.. granulosus. In a number of countries in West Africa tions exist. and infection with the sheep (G1) strain of the dogs are allowed to scavenge from carcasses parasite (Santivanez et al. 1988). even within regions Mexico (Schantz. 1998). Mean worm burden (by arecoline purgation) while the dogs in the west fed on live- in Durazno Department (Uruguay) was 67 stock that had died during the 1978–1981 (range 1–1020) where the prevalence was 20% drought. dogs the high sierra of Bolivia and in the Rio Grande have been recorded with higher prevalences do Sol in Brazil (Moro and Schantz. increasing the role of was significantly correlated with E. and Asia some people eat dogs.. and dogs are welcomed for the in Utah (Andersen et al. jackals and Diet hyenas were consumed during periods of drought. and scavenge around the temporary sheep (Schwabe. dogs fed almost exclusively on fish scraps. 1983). which would carded offal (Schwabe.. where socio-cultural and socio-economic conditions are similar. prevalence rates range from 3. granulosus humans in the life cycle of the parasite there infections in dogs and CE infection in humans (Macpherson. and Macpherson.. but the people denied ever eating The diet available to dogs obviously plays dogs (Macpherson et al. 1983). 1984. urban years (see Chapter 14).. a pivotal role in their becoming infected On many continents dogs used for with E. In Egypt. 2008). Home slaughter is frequent and in of 80 dogs owned by Turkanas living along one study in a rural area 13. 1998). 1991. Lokitaung. 2006). so in Peru is high in the central and southern offal from infected animals that are slaugh- highlands. In Florida.N. granulosus occur. Schwabe. The prevalence of infection of dogs Kakuma. 1997. In rural Kazakhstan. and in native Americans dogs’ diet. particularly scraps.. 1993). In urban also sources of infection for dogs. Wachira et al. trol programmes have been in place for many and North and sub-Saharan Africa. In Turkana dogs may scavenge (Cohen et al. 1997).L. granulosus infection in dogs. 2002). Macpherson and Craig. community. et al. dogs spent in their houses was significantly ment of individuals with CE. specifically a lack of knowledge correlation was also found for homesteads about the life cycle of E. resulting source of infection (Craig et al. in E. p<0. Human and dog behaviour and These scavenging opportunities increase Echinococcus granulosus transmission the risk for human CE among such peoples (Macpherson. A greater understanding of these factors.8% (Torgerson control programmes. 2005. having a prevalence of 5. vention is rarely taught. is as pets or for security from the same dis. and low human CE • Poverty. Torgerson et al. • Lack of a safe piped water supply. ronment for long periods of time (Carmona • Lack of abattoirs. clean children. The routes of transfer of eggs from infected dogs to intermediate hosts. sils (Watson-Jones and Macpherson. Areas where home et al. 1995). One national levels. found that the amount of time of owned dogs and for diagnosis/treat. 2006).. and to lick eating uten- transmission of the parasite and its pre. or relatively low income. Macpherson et al. contribute to the transmission of 31 dogs for 24. Dog contact is a major risk factor (Watson-Jones A number of socio-economic factors oper- and Macpherson. 1998. remain arcane. 2008. ating at the individual. Thus ample opportunities for such scavenging occur. 1988. especially in • Lack of veterinary and medical facilities climates where eggs may survive in the envi- and diagnostic centres. be a consequence of infection occurring many promised if water has to be carried over years earlier. This process must Socio-economic factors involve a complex mixture of environmental. socio-cultural. Yang et al. 2000.. medium. 1988). Moro et al. Torgerson et al. 1988. which documented the movements of of the world.. One important risk factor that has been • Abattoir workers are a high-risk group associated with infection with CE is poverty for CE. outside of spe. 1991.. 2003b).. risk of CE. which vary in different parts study. Surprisingly dog contact is not always a risk cific control activities. Dowling in numerous. particularly in nomadic or transhumant situations where livestock are moved over vast distances.. or unemployment .986. 2003b). A significantly positive nities. feral dogs which are allowed to roam. or food contamination may be a possible • Lack of dog control programmes. including humans. granulosus including: areas of high. 2003b. slaughter is commonly practised. Dogs and Cestode Zoonoses 135 with livestock husbandry have a mean prev. 2009). (rs) = +0. In which allowed dogs to defecate in the home endemic countries information about the area. Bai et al. factor for transmission of CE. alence of 23% compared to village dogs kept and also particular socio-cultural factors.541 observation-minutes. granulosus.. usually young. Inability to pay for treatment prevalence. and Tiaoying et al. Also of impor- • Pastoralists are at greater risk of CE than tance is the fact that in many highly endemic agriculturists or urban dwellers. regions dog ownership and dog contact is • Transhumant or nomadic pastoralists almost universal.. so this factor cannot dis- who live in many parts of the world criminate between infected and non-infected appear consistently to have the greatest individuals (Torgerson et al. 1989a. and recall is difficult for subjects long distances to the home.01). stray and/or et al... and behavioural factors. correlated with an increased prevalence of • Lack of education on the public health CE (Spearman’s rank correlation coefficient importance of CE in endemic commu. There is also some evidence that water • Lack of trained personnel.. of epidemiological studies. essential to the successful implementation of trict.. Lack of association with contact may Hygiene in such areas is naturally com. are applied to dogs will be considered here. • Options for control will need to be tai- Many control programmes have been imple- lored to the availability of local resources mented and several have been very success- and logistical considerations. canadensis not feeding cysts to dogs. Surveillance in dogs may be carried out A number of options are available for through coproantigen tests which have a good control (Chapter 14) but most programmes sensitivity and can detect prepatent infections. tions in dogs. allowed to roam. pro- 2004). in Morocco.. 2010. Macpherson and P. This may be achieved through cause far fewer cases of human CE than E.. An important aspect with any educational programme is compliance with the control approach. the only control method than this clearly 90% of hydatid cysts from sheep slaughtered must be an intensive treatment schedule at home were fed to dogs (Macpherson et al. offal in • Regular dosing of dogs with praziquantel.. such as slaughter Control and surveillance control. • A new vaccine for use in sheep (EG95) There have been a number of island and con- has become available and appears to be tinental control programmes for E. and dosing is timed to prevent transmis- 2005. for example complying with Echinococcus ortleppi. Torgerson sion when the intensity is likely to be et al. 2009. Buishi et al. Macpherson. Pierangeli et al. etc. have had similar strategies to control E. period of time.. or the dogs’ owners are ignorant of others examine epidemiological factors the disease (Budke et al. 2003b. 2005. A detailed ful in reducing the annual incidence of CE in description of various options can be humans and sheep. intermedius.. 2003b).136 C. E. they generally offal.. granulo- highly effective. the community is not disposed of properly. whereas ment. Torgerson et al. gran. Torgerson (Budke et al. Although • Prevention of access of dogs to infected all these species are zoonotic. 2010). This technique has been implemented in a ulosus in dogs. in abattoirs and preventing dogs from Torgerson et al. then this will potentiate the use of anthelmintics in dogs.R. In the Transmission from intermediate hosts absence of such facilities. In one highest and the greatest cost:benefit value study. A similar proportion is likely in other viding most of the dogs are treated and endemic regions facilitating hydatid cysts the programme is continued over a long from intermediate hosts to dog transmission. gaining access to such facilities. should be promoted to species status. granulosus. 2005.. 2005. dog registration and treatment schedules. Molecular and • Population management of wanted dog other evidence now strongly indicate that they populations. Iceland and New Zealand have succeeded in eliminating CE. Ziadinov et al. should be implemented. 2008). be genotypes of E.L.N.. questionnaires used during ultrasound is obtained. If regular treatment of dogs is screening surveys indicated that.. Mastin et al. (2011). dosing schedule every 6 weeks. 2006. gran- strict rules of disposal of infected offal ulosus. Their impact on human health may be . Vaccinating sheep has sus: these are covered in Chapter 14 and only a potentially useful role in preventing a brief overview of control measures that infection in dogs. usually decades. fed on raw offal. • Dog registration.. 2011. Some programmes implement an intense the dogs do not receive anthelmintic treat. Dogs are more those who carry out home slaughter likely to become infected if they are young. • If adequate controls of the intermediate host are implemented. granulosus infec- found in Torgerson et al. education of to dogs is more predictable.. and E. • Education of the local population. It will result in parasite elimination. and E. which include: number of countries (Acosta-Jamett et al. Until recently these species were considered to • Elimination of stray and unwanted dogs. Huge worm burdens may result in both dogs and foxes. 2010).. (Budke et al. multilocularis is predominantly maintained region a semi-domestic cycle between dogs in predator:prey wildlife cycles. More than 100. 2011). are ecologically separated. 2005). lupis) and sand fox (Vulpes corsac) per gram of faeces may occur.. with their domestic not routinely genotyped and hence the relative animals. canadensis/ dra zone of North America through northern E. Some asite is found over an extensive area of the trends have been recorded and these can be sum. in contrast to the much slower devel- 1992) and Sichuan provinces (up to 20%) oping metacestode of E. to China and recorded in Argentina (Soriano et al. pigs. 2011. Italy (Casulli et al... Peru the northern islands of Japan.. Human infections with E. Turkey (Snabel et al. rather. granulosus at about 28 days. Dogs and Cestode Zoonoses 137 underestimated. 2006). ortleppi has been seen in humans and livestock in Brazil (de la Rue et al. 1955). in livestock in India (Pednekar et al. and occa- worms and few eggs being produced (Kapel sionally other groups such as ochotonidae. and camels frequently being and be viable when the intermediate hosts an important reservoir. northern hemisphere. 1993).000) (Rausch live in the small intestines of wild canids. granulosus G6-G10) have been and central Europe and Eurasia.. et al. granulosus.5 mm) adult tapeworms was 7400–54. as generally hydatid cysts are endemic areas humans. Eggs can thus overwinter with goats. 2011).. et al. Its southern- (Moro et al. In this montane agricultural E.. The adult parasites probably live for and 35% of coyotes (Canis latrans) have been approximately 3–4 months with maximum found infected (Eckert et al. most limits in Asia are northern India. 2006). 2008). with experimental hosts (see below)... In the northern tundra zone of North et al. 2009).. multilocularis eggs have become 2010). E. number of dogs and period of dog Distribution ownership were the major risk factors (Craig et al. fox (Alopex lagopus) is an important definitive and proglottids contain only between 200 and host. The par- contribution of these species is unknown. emerge after the winter (Schiller. et al. The prepatent period is slightly America and in northern Russia the arctic shorter than for E. 2011). and East Africa (Dinkel Dogs as definitive hosts of Echinococcus et al. 1990).. Other rela- egg excretion 6–103 weeks after infection tively important wild definitive hosts include (Kapel et al. intermedius (E. peratures of −50°C. are intermediate hosts for Echinococcus multi- In China dogs have been found to be locularis. Livestock in these areas are also com.. multilocularis and Echinococcus multilocularis infection occurs when dogs ingest infected (Leuckart 1863) intermediate hosts. 2010). Rausch.000 worms were red fox (Vulpes vulpes) is the main definitive found in 8% of the 133 infected foxes (Hoffer host. and Central Europe (Schneider et al. 2000).000 (range 1–84.. The suitability of cats as definitive hosts Domestic dogs and cats also serve as definitive is believed to be poor.... On St Lawrence Island mean infection rates in Arctic foxes The small (1. 2000).. Small mammals including infections in cats resulting in very few viable microtine and arvicolid rodents. In south Gansu dog own- ership per se was not a risk factor for human AE. which may be commonly infected in Eurasia. multilocularis Dogs are susceptible to E. extending from the tun- marized. In central North America between 6% 300 eggs. Iran. rapidly. In the red fox in urban areas of Throughout most of the parasite’s range the Zurich infections of over 10. Sudan (Omer and eastern Turkey (Eckert et al. In these hosts the parasite develops infected in Gansu (6 out of 58) (Craig et al. Mongolia (Jabbar et al. 2004). 2009). adapted to cold climates and can survive tem- monly infected with this genotype of parasite.000 eggs wolves (C. and in most and microtine rodent species is likely to occur . E. 2009).2–4.. 138 C.N.L. Macpherson and P.R. Torgerson during periods of high population density for E. multilocularis to humans as there are few susceptible rodent species. stray dogs and, until recently, the only means Within Tibetan communities dogs play of diagnosis was necropsy. Studies which an important role in the transmission of AE to were carried out generally involved small humans (Vaniscotte et al., 2011). Domestic dogs numbers of dogs and salient risk factor assess- are also probably involved in semi-domestic ment was lacking. The recent development transmission of E. multilocularis involving the of ante-mortem diagnostic tests (see below) common lagomorph species in this biotype, has facilitated much larger studies. A recent Ochotona curzonae. In both Gansu and Sichuan, ELISA coproantigen study with confirmation higher AE rates in women may be related to by PCR of 660 dogs in Switzerland found a closer contact of females with dogs. prevalence of 0.3% (Deplazes et al., 1999). In In Central Asia dogs have been shown Austria, cat ownership and hunting in the to have a high prevalence of E. multilocularis forest were found to be important risk factors, (Ziadinov et al., 2008) and these may prove whereas dog ownership was not (Kreidl et al., to be a risk for human AE in Kazakhstan and 1998). In Austria, as elsewhere in Europe, Kyrgyzstan. dogs are mostly pets and not used for hunt- In Japan stray dogs have been found ing. In Germany, 43 of 17,894 (0.24%) canine infected on Reubun Island (1.6% of 3224) faecal samples were PCR-positive for E. multi- (Yamashita, 1973) and in 2% of dogs on the locularis (Dyachenko et al., 2008). The samples island of Hokkaido (Iida, 1969). In both areas originated from all regions of Germany and the red fox is perceived as the main definitive confirmed that canine infection with E. multi- host. locularis in Central Europe occurs, albeit at a In North America, E. multilocularis is low frequency. currently an important public health prob- In an attempt to estimate the relative lem only among the Yupik Eskimos in the capacities of foxes, dogs, and cats to contami- northern tundra zone of Alaska, despite the nate the environment with E. multilocularis parasite’s distribution, including as far south eggs, a model calculation was carried out for as the midwest of the USA (Rausch, 1993; the Canton of Zurich, Switzerland (Eckert Schantz et al., 1995). The parasite has been and Deplazes, 1999). The population size and found on a number of the subarctic islands, prevalence of E. multilocularis in the three including St Lawrence Island, where in the definitive host species was calculated. Foxes 1950s 12% of dogs autopsied were infected were the largest group of E. multilocularis car- (Rausch et al., 1990). Dog ownership and riers, whereas the numbers of infected dogs tethering dogs near houses was an impor- and cats were much smaller and represented tant risk factor for patients found to have only 7% and 16% of the number of infected AE (Stehr-Green et al., 1988). definitive hosts, respectively. Apparently, in It has been speculated that dogs may this epidemiological situation, foxes were the have been the route through which the main contaminators of the environment with parasite was spread from the northern tun- E. multilocularis eggs. Such calculations can dra zone to southern Canada and to central provide a few suggestions for the importance areas of the northern United States, espe- of the various definitive hosts, but they are cially North Dakota and northern Manitoba woefully incomplete, as many other factors (Rausch, 1993). The parasite has spread from play a role. For example, although the preva- these areas and has now been reported in 11 lence rate in dogs and cats was small, they contiguous states in the United States and have a closer contact with humans than foxes, in three Canadian provinces (Schantz et al., providing greater opportunities for being the 1995). So far the parasite in this area has not source of human infection. Cats have now been found in domestic dogs and only two been shown, at least experimentally, to be very human AE cases have been confirmed in the poor hosts of E. multilocularis with very few last 50 years (Schantz et al., 1995). worms establishing and no viable eggs pro- In Europe, little is known about the duction (Deplazes et al., 2011; Kapel et al., 2006) importance of dogs in the transmission of so the epidemiological significance of cats in Dogs and Cestode Zoonoses 139 transmission is likely to be insignificant. On worms. The development of ELISA and PCR the other hand, it has been noted recently that tests for screening faeces for coproantigens fox populations are increasing in the cities of or worm DNA has revolutionized diagnosis Europe, and in Zurich, Switzerland, it has been of not only patent but also prepatent infec- estimated that there are between 300 and 400 tions in definitive hosts (Deplazes et al., 1999; foxes within the city limits, with 47% being Dinkel et al., 1998). The coproantigen test infected with E. multilocularis (Hoffer et al., has a sensitivity of 80% and a specificity of 2000). It is known that such foxes visit public 95–99.5%. Confirmation of infection may be parks and swimming pools (Deplazes et al., made using PCR to detect E. multilocularis 1999). There is now a statistically significant DNA, which increases the sensitivity to 94% increase in the numbers of human AE cases in and has a specificity of 100% (Deplazes and Switzerland, which is temporally correlated Eckert, 1996; Dinkel et al., 2011; Torgerson (with a lag of 10–15 years) with the increase and Deplazes, 2009). in the fox population (Schweiger et al., 2007). This association with the increase in fox pop- ulation does not prove that foxes transmit to Treatment of Echinococcus humans in Europe. What it does demonstrate multilocularis in dogs is that the increased E. multilocularis biomass now present is leading to greater numbers of cases. The conduit to humans may be contact The treatment of choice is praziquantel. As with foxes (as previously discussed) or there with E. granulosus no resistance to the drug may now be greater opportunities for dogs to has yet been reported, and the drug is effec- become infected. It should also be noted that tive in a single dose. dogs are often coprophagous and will eat fox faeces, (possibly resulting in the sporadic cases of hepatic AE being recorded in dogs (Staebler et al., 2006) and egg passage may put Epidemiology and public owners at risk. Even more likely is the habit health importance of dogs rolling in fox faeces, and the fur being contaminated with eggs, which could permit Foxes infected with E. multilocularis have tra- transmission. ditionally been considered to be an impor- The introduction of new diagnostic tests tant health hazard to fox hunters, however may not only be used for ante-mortem diag- there is no direct evidence for this. When nosis of dogs and cats, but also potentially hunters in the United States and Japan were be able to detect E. multilocularis infections screened by serological tests no increased in faecal samples collected in the field. This risk of seropositivity was observed (Schantz will facilitate studies on environmental con- et al., 1995). tamination, to examine the relative contribu- Indirect contact with an environment tion of dogs and cats compared to that made contaminated by fox faeces, such as wild by foxes, and enable studies to be carried out fruits and/or herbs has been considered an to examine potential routes of infection for important mode of infection, though detailed humans. studies are lacking. Dog (or cat) owner- ship over a reasonable period (years) within endemic areas is possibly a greater risk factor for human AE (see above), together with an Diagnosis of Echinococcus agricultural occupation or background, and multilocularis in dogs households close to a landscape or biotype capable of sustaining susceptible intermediate Until recently the only means of accurately host populations (Bresson-Hadni et al., 1994; diagnosing E. multilocularis infections in Craig et al., 2000). Infected dogs, rather than dogs was by autopsy and the subsequent wild canids, may pose the greatest risk for morphological identification of the adult human AE infection (Vaniscotte et al., 2011). 140 C.N.L. Macpherson and P.R. Torgerson Control and surveillance the range of its wild definitive and interme- diate hosts in Central and South America: The only example of elimination of E. multi- in Costa Rica, Panama, Colombia, Ecuador, locularis occurred on Reubun Island (Japan) Venezuela, Brazil, and Bolivia (Rausch, 1993). 30 years after the parasite had been intro- The disease in humans who serve as acciden- duced inadvertently with translocated red tal intermediate hosts is known as polycystic foxes in 1924–26. Approximately 1% of the echinococcosis (PE), or hydatid disease. The population (129 AE cases) was infected, 19% adult parasites were first described from of red foxes and 1.6% of dogs. A 5-year fox specimens recovered from the small intestine and dog culling control programme appeared of the bush dog, Speothos venaticus (Rausch to eliminate the parasite by 1995 (Craig et al., and Bernstein, 1972), which is the only known 1996; Yamashita, 1973). wild definitive host species of this parasite. There has been a single trial to treat dogs The animal had been captured in its natural as part of a control programme for E. multiloc- habitat in Esmeraldas Province, Ecuador, and ularis. This took place in St Lawrence Island, kept in the Los Angeles Zoo. The bush dog where dogs were treated monthly with prazi- was responsible for infecting five different quantel over a 10-year period. This reduced species of non-human primates housed in the infection in the rodent intermediate hosts nearby cages, and most of them subsequently from 29% to 5%. The prevalence rate in the died of PE (Howard and Gendron, 1980). intermediate hosts, however, rebounded to There were no human cases, but this inci- the original rates soon after dosing of dogs dence does highlight how infective the eggs was discontinued (Schantz et al., 1995). are for non-human primates. In southern Germany a trial to reduce the The paca Cuniculus paca serves as the prevalence of E. multilocularis in foxes (Vulpes main intermediate host. Agoutis (Dasyprocta vulpes) demonstrated that after six treatments spp.) and spiny rats (Proechimys spp.) have the prevalence of the parasite in these defini- also been found to harbour E. vogeli proto- tive hosts fell from 32% to 4% (Schelling et al., scoleces (Rausch et al., 1981). Domestic dogs 1997). Likewise, in the city of Zurich, regular can also serve as definitive hosts, and experi- treatment of foxes using praziquantel baits has mental infections of dogs with cysts from been shown to decrease the prevalence sub- an agouti were confirmed as being E. vogeli stantially (Hegglin et al., 2003), with monthly (Rausch et al., 1984). In its natural habitat baiting of foxes appearing to be the most E. vogeli is maintained in a predator:prey cycle. effective strategy (Hegglin and Deplazes, As Speothos spp. hunt in packs, many bush 2008). Similar results have also be found dogs may be infected from a single paca kill. with intensive baiting strategies in Germany The risk of human infection from wild defini- (Konig et al., 2008). It has been proposed that tive hosts would be rare, since bush dogs are only those dogs and cats at risk of infection secretive and very wary of humans, and move through eating wild-caught intermediate hosts further into the forest when humans encroach should be treated regularly with praziquantel on their territory. Contact rarely occurs. In (Eckert and Deplazes, 1999). The possibility of endemic areas, dogs are used to hunt and introducing a dog-screening programme with are commonly fed viscera from pacas, so that ELISA tests to detect coproantigens provides human infections are probably acquired from an exciting new approach to E. multilocularis the faeces of infected dogs. Feeding dogs with epidemiology and surveillance. paca offal is an important risk factor and in Colombia a hunter’s dog has been found to have the adult parasites (D’Alessandro and Rausch, 2008). In Brazil, Meneghelli et al. Echinococcus vogeli (Rausch (1990) found that all seven patients with poly- and Bernstein, 1972) cystic hydatid disease had contact with dogs that had been fed offal from pacas. Echinococcus vogeli has a restricted global dis- On radiological examination, the dis- tribution and has only been reported within ease in humans gives the appearance of Dogs and Cestode Zoonoses 141 multiple cysts of E. granulosus (Meneghelli especially dogs may serve as definitive hosts. et al., 1992b). Cysts are usually located in In some areas infection levels in dogs reach the liver but also infect the lungs, spleen, 34–47% and they probably serve as the main pancreas, peritoneal cavity, and mesen- definitive hosts (Witenburg, 1964). Foci of tery (D’Alessandro and Rausch, 2008; infection stretch east from France, northern Meneghelli et al., 1992b). Differentiation Italy, and the Baltic States, through north- between E. vogeli and E. granulosus is pos- ern Russia into China, Japan, and North sible using protoscolex hook morphology, America; and also through South America, PCR, and ELISA. Human infections have including Patagonia, Argentina, Chile, and been reported in most countries within Peru. Sporadic infections are described in its known range in neotropical America other countries such as Brazil, Cuba, Korea, (Meneghelli et al., 1992b; Nunez et al., and Australia, and 1% prevalence was 1993; Rausch, 1993). In Ecuador at least 12 recently described in 6–10-year old children human cases have been diagnosed from in Karnataka, India. Genetic analyses are diverse geographic regions, including the required to confirm D. latum at all its reported coastal plain, Amazon basin, and Andean locations (Lloyd, 2011). Marine diphyllo- plateau (Nunez et al., 1993). In Brazil, most bothrosis occurs in marine mammals (seals). cases have been reported from the Amazon Occasionally humans who eat raw or under- region, but a few came from the state of Sao cooked marine fish, especially anadromous Paulo (Meneghelli et al., 1992b). species such as salmonids (Scholz et al., 2009), Albendazole given over a period of are also infected. Although human infections several months successfully treated four of have been recorded in Peru, Chile, and Japan, six patients (Meneghelli et al., 1986, 1992a). the susceptibility of dogs in these countries is The remaining two patients had some remis- unknown (Miyazaki, 1991). sion of the disease. It would be impossible The life cycle of Diphyllobothrium spp. to control the parasite in its natural habitat, includes copepods as first intermediate but making hunters aware of the dangers of hosts (procercoid stage) and freshwater feeding offal from pacas to their dogs would fish as second intermediate hosts (plerocer- help decrease human exposure in endemic coid stage) (Rahkonen and Valtonen, 1997). regions. Regular treatment with praziquan- Following ingestion by definitive hosts, tel of dogs that are fed such offal would also such as humans and a range of other fish- be advisable. eating carnivores, and in particular domes- tic animals such as dogs, cats, and pigs (see above), the plerocercoid larvae mature to adult tapeworms that may contain up to Diphyllobothriosis 3000 proglottids. Experimental infections in dogs have shown that egg production starts Within the group of tapeworms belonging about 21 days after infection (Wardle and to the genus Diphyllobothrium, D. latum is Green, 1941). the predominant of 14 recognized species Intestinal infection with D. latum is usu- with regard to numbers of human infec- ally asymptomatic. In some cases, mild gas- tions, which amount to approximately 9–20 trointestinal obstruction, rarely diarrhoea and million (Lloyd, 2011). D. latum, known as abdominal pain, and occasionally leukocyto- the ‘broad’ tapeworm, as the proglottids sis with eosinophilia, are present. Perhaps are usually wider than they are long, is the the most serious clinical manifestation is the largest tapeworm of humans, growing to a onset of pernicious anaemia, which occurs in length of 3–25 m and a width of 1–2 cm. The approximately 2% of the patients, as shown in parasite is especially prevalent in countries studies performed in Finland. This is caused where fish is a major source of protein and is by the extensive absorption of vitamin B12 by often eaten raw or only partially cooked (i.e. the adult tapeworm (von Bonsdorff, 1977). smoked). Offal from the fish is often avail- Prevention and control measures able to domestic animals and cats, pigs, and include appropriate cooking of fish and 142 C.N.L. Macpherson and P.R. Torgerson treatment of infected individuals and stage as the adults have piercing mouth domestic animals, particularly dogs, with parts. Development in the obligate ectopara- praziquantel. Regular treatment of domes- site, the louse, takes up to 30 days, while in tic carnivores with praziquantel, especially the flea larvae in the environment may take those being fed raw fish, can dramatically up to a couple of months, depending on the reduce environmental contamination of ambient temperature. The cysticercoid in natural water resources with parasite eggs, the louse or flea is ingested by the defini- and thus reduce transmission. Preventing tive hosts and the prepatent period is about access of wild carnivores to aquaculture 3 weeks. facilities by appropriate fencing also helps The adults, which may number several control the parasite in such areas. hundred, are not pathogenic. Proglottids passing out of the anus may cause mild pruritus. Treatment of children, dogs, and Cestode Species of Minor Zoonotic cats is with praziquantel, niclosamide, or Importance nitroscanate. Control of the ectoparasite intermediate hosts should be carried out Dipylidium caninum simultaneously. Special attention should be paid to the sleeping area of domestic dogs Dipylidium caninum is one of the commonest and cats. tapeworms of dogs and cats in most parts of the world (Boreham and Boreham, 1990). It is especially common in neglected dog Taenia spp. populations which have large ectoparasite populations. Although prevalent worldwide There are at least three taeniid species, in pets, human infection is uncommon (<200 T. multiceps, T. serialis, and T. brauni, which reports) but underestimated. In the United have dogs and other canids as definitive States 43 cases were reported in a 5-year hosts; a few humans have been identified to period when drug use could be recorded. be infected with the larval stage. In addition, Infection occurs usually in children under T. solium cysticercosis has been recorded 6–12 months of age (Lloyd, 2011). Children in dogs. also serve as definitive hosts, and adults only rarely (Moore, 1962); this is probably due Taenia multiceps to increased opportunities for children to (syn. Multiceps multiceps) become infected. The adult parasite lives in the small intestine and rarely exceeds 50 cm The parasite is regarded as being common in length. Proglottids migrate out of the anus in dogs in Australia, Europe, South America, or are shed in faeces and are easily identifi- and Africa but has disappeared from New able as they resemble a large rice grain and Zealand and the United States. A prevalence are either passed singly or as a short ribbon of 26.6% of dogs in Wales has been reported of up to 10 proglottids. A hand-lens inspec- (Hackett and Walters, 1980). The prepatent tion of freshly passed proglottids reveals the period in dogs is between 38 and 43 days lateral genital pores and egg packets, which (Willis and Herbert, 1987). Adult worms can be used to differentiate this parasite from grow up to about 100 cm and proglottids are the taeniids. Each D. caninum proglottid con- shed in the faeces. Intermediate host spe- tains up to 20 egg packets, each containing cies include wild ruminants, chamois, cat- 6–12 infective eggs. Fleas (Ctenocephalides felis tle, goats, and – most importantly – sheep. and C. canis) and the dog louse (Trichodectes Ingested eggs hatch in the small intestine and canis) serve as intermediate hosts. Biting lice the oncosphere penetrates the gut and lodges can ingest oncospheres at any stage in their primarily in the CNS, especially the brain. Here, life cycle, as all stages have chewing mouth over a period of about 8 months, it develops parts, but fleas are only infected in the larval into a coenurus (Cysticercus cerebralis), giving Humans can be infected in three differ. and Korea (Lloyd. which taneous or intraocular. Treatment is by surgically removing the plerocercoid Spirometra spp. There are many different species of Intermediate hosts include lagomorphs Spirometra but the dog is the known defini- and rarely rodents. and occasionally praziquantel may be used. The lineatus. and humans (Smyth and Heath. and Africa. The disease is known as are common in dogs. snakes serve as Protoscoleces align in rows or series in such intermediate hosts for this species. . China and South-East Asia. 1991). birds. Spirometra was the commonest in both adult and cystic stages (for human intestinal helminth recorded (Muller-Graf infections). The scolex has 3. especially in heavy or cerebral infections. ing a large number of plerocercoids. hence the name C. Most human infections are subcu. By applying poultices (such as split frogs) no hooks. produc- rodents. A few hundred wander through tissues and may end up in cases in humans have been reported globally subcutaneous sites where they may encyst. the dominant species located intramuscularly or subcutaneously. ties in gait known as ‘gid’.) in drinking water. in Asia and South America. serve as secondary intermediate hosts with 2. mansoni. and diz- (Lloyd. China. the predilection site of Taenia serialis and T. reptiles. Adult worms plerocercoids in a range of intermediate host have been recorded in humans in Japan. cats. 2011). Differential examined in the Serengeti National Park diagnosis with T. but Mesocestoides lineatus also in Africa. finding the plerocercoid. Europe. Mites ent ways: serve as the first intermediate hosts and have the cysticercoid stage. paraplegia. brauni the plerocercoids. multiceps may be difficult (Tanzania). particularly eastern Asia. and mam- can multiply asexually in the peritoneum mals such as pigs. are found in dogs. Ingested procercoids or include circling. 1991). This mode blood or organs of snakes and turtles as ton- of transmission is most commonly found in ics (Miyazaki. et al. The tetrathyridia cooked amphibia. Intermediate hosts of T. species including amphibians. The life cycle of these tapeworms Dogs can serve as both secondary intermedi- is similar to that of D. and Australia. hence multiple worm infections grow up to 30–40 cm. 2011). Cysts are usually tive host of S. and birds (Cyclops spp. By ingesting procercoids in crustaceans carnivores. 2011. birds. abdominal pain. In lions cysts. snakes. ziness. snakes. brauni are Rarely the parasite proliferates. (Lloyd. have been documented (Lloyd. Dogs and other 1. plerocercoids penetrate the intestinal mucosa. Diagnosis is by reported from Africa (Lloyd. Clinical symptoms include severe to skin wounds and especially to the eyes diarrhoea. Through ingesting plerocercoids in under- the tetrathyridia stage. and peculiari. Plerocercoids can scoleces. Adult Spirometra spp. In Japan. 2011). The parasite has a wide distribution procercoids are found in crustaceans and the in Asia. hunger. Miyazaki. amphibia. and a range of wild carnivores in many parts of the world. or may develop into adults.. North and South America. latum and two inter. often incidentally when a biopsy of a lump is made. A total of perhaps 30 human cases 1970). 1999). 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(2006) Community surveys and risk factor analysis of human alveolar and cystic echinococcosis in Ningxia Hui autonomous region. Yang. (1983) A preliminary survey of Echinococcus infection in man and animals in Ningxia Hui Autonomous Region (Abstracts of Papers Presented at Scientific Conference on Parasitic Diseases). C. Liu. Yan.T. Qinghai Journal of Zootechnics and Veterinary Science 4... Journal of Tropical Medicine and Hygiene 94. J. et al. 261–267. in foxes also contribute to environmental ues to occur. 2001). canis infection a similar life cycle to Toxocara spp. Other impor- are also known as roundworms. but be expected to strongly suppress T. because stercoralis. and meas. Zoonoses and Public Health. canis also serves as a model for other environment more closely. Most atten- health. if ever the main source of infection. T. egory is not considered. T. dogs greatly the successes and limitations of current strat. canis there are good reasons to consider T.uk ©CAB International 2013. and is the main reason for preventative chemical Toxocarosis deworming of dogs in temperate areas not endemic for the heartworm Dirofilaria immitis. canis dominates public health attention among the nematodes of dogs. University of Bristol. canis transmission to mental contamination with Toxocara eggs. Gnathostoma spp. Morgan* Veterinary Parasitology and Ecology Research Group. and a potential cause of cases of toxocarosis lic hygiene measures. outnumber wild foxes. dromes. reviewed. Dogs. in dogs is the main source of toxocarosis in ures to prevent environmental contamination humans (Mizgajska. T. especially in young animals. chief among them Strongyloides mon. Macpherson et al. 9 Dogs and Nematode Zoonoses Eric R. but dogs are rarely human tissues when eggs are ingested. hookworms have generally considered that T. Bristol. routine anthelmintic treatment would tion has traditionally focused on T.L. However. However. The large tant nematode zoonoses of dogs are briefly ascarid gutworm Toxocara canis is com. It is therefore nematode zoonoses. cati in populations. be Where heartworm is a major threat to canine caused by any species of Toxocara. 2nd Edition (eds C. UK Dogs in all parts of the world are very with ascarid eggs should also reduce the frequently infected with nematodes. this species remains in humans (Fisher. in principle. canis populations very common and human disease contin. 2003). and share the human egies. This chapter therefore focuses contamination with eggs. caus. since prevalence mainly on the control of toxocarosis in dogs in foxes is typically high.. * Author. lipaeda. This cat- ing a variety of clinical and subclinical syn. and reviews areas inhabited by humans. Thus. which threat from hookworm larvae. humans through treatment of dogs and pub. in spite of decades cats as an important contributor to environ- of efforts to reduce T. and Thelazia cal- of its efficient vertical transmission mecha.
[email protected]. in most in the interests of public health. e-mail: Eric. Larvae of this species migrate through infect dogs and humans. Toxocarosis in humans can.) 153 . Several other nematode species can nism.ac. Brunaska and be as high as 47% in adult sheep (Lloyd. the life cycle act as paratenic hosts (Glickman and Schantz.154 E.. Eggs are therefore the liver and the lungs. Approximately 80 mm in diameter UE = Unembryonated. Serological studies is known as hepatotracheal migration. By entering an arrested state. larvated eggs have been found on Fig. positive association of risk with rural location. and continue to ingest Adults of T. Stürchler et al. larvae re-emerge from days or weeks to develop to the infective stage. thought that transmission by direct contact perhaps even the lifespan of the host. can be complex (Overgaauw. seroprevalence has been found to they are infective (Kasai. hepatotracheal migration is rarely com. which can therefore and Schantz. Infection occurs when sis. 9. such that the rather maintain position by moving against gut majority of pups even in well-cared-for pet dog peristalsis. In older in humans have found evidence of exposure dogs that have previously encountered infec. Eggs are thick-shelled and highly resistant mature eggs are ingested and the larvae hatch to normal environmental conditions (Azam et out and penetrate the intestinal wall. before being coughed available and infective long after faeces have up and swallowed. Yoshikawa et al. 9. and can therefore persist for months susceptible dogs. 2012). In female with dogs was unlikely. 1981). to complete development degraded.. through the body. and can be ingested inadvertently to the adult stage in the intestine. it was survive in the somatic tissues for many years. 2012). They feed on intestinal contents and populations are infected (Sprent. Egg of Toxocara canis. 1997). pleted. Instead. Vertical where they do not attach to the mucosa but transmission is highly efficient. 1958. Schantz and Stehr-Green.1. Most pups are therefore infected before birth. canis live in the small intestine. Morgan Mode of transmission mammary glands. This process following soiling of hands. 2006).1). in a wide range of social and age groups. and cross the placenta and the However. larvae throughout the suckling period. Parsons. Larvae are sometimes found in large numbers of eggs are produced (Glickman the tissue of food animals.R. generally cause few problems to the host. Very larvated eggs. must first develop to the larvated stage before 2008). larvae can children (Mizgajska. these larvae then move via or possibly years in soil.. 1988). Thereafter. and females mate and the females produce Humans are infected primarily by ingesting eggs that pass out in the faeces (Fig. Traditionally. Dubinsky. . and can invade a variety of and behaviours such as pica (geophagy) in tissues. 1990. The eggs 1981. somatic arrest. This occurs at temperatures However. the larvae migrate more widely occupations that involve contact with land. L = Larvated. with tion. given that eggs require hosts that reproduce. In fully al. Indeed. 1995). Males 1987. 1995. 2001).. it is not known to what extent meat- above around 11°C with adequate moisture borne infection contributes to human toxocaro- (Azam et al. whereas the consequences of tory reactions can persist and clinical signs can infection in young pups can be more severe. 2008). the available evidence wheezing (Despommier. 2011).. with the characteristic eggs easily including blindness. epilepsy. fever. tion of the larva. and large burdens can Ocular larva migrans (OLM) accumulate in pups as young as 2–3 weeks of age. brain. take some time to resolve.. . whether associated with dis. associated with Toxocara infection in humans.. Larval migration to the retina is associated Patent infection. development to the infective stage while on including the viscera. which might be expected to be inflammatory reaction. 2003). 2009). Infection is often asso- environmental contamination with Toxocara ciated with eosinophilia and a rising antibody canis eggs. 2009). and infection (Won et al. possibly the level and dura- of humans following handling of dogs there. eggs are not found in the faeces. pneumonia. 2010). and covert toxocarosis. et al. 2008. tion of infection. with granuloma formation. it is possible that this syndrome can arise from low levels of infection. ascites.. Dogs and Nematode Zoonoses 155 the hair of dogs (Wolfe and Wright. malaise. However. in which contamination of hair with eggs diverse clinical syndromes also described in the environment is highly probable (Roddie (Rubinsky-Elefant et al. clinical signs as the main mode of transmission to humans can be vague and with background population (Mizgajska. and et al. Moreover. less well-defined symptoms have been larvae then migrate to the somatic tissues. with other tions. sleep disturbance. constipation. leading to disease and possibly death. Larvae can be may include digestive disturbance and killed by anthelmintic therapy. and give rise to signs stronger if direct contact were a major route of including abdominal pain. Various organs can be invaded. level of infection and host factors. 2010). can be easily diagnosed by faecal degrees of unilateral visual impairment. Disease in humans Other syndromes Toxocara ova hatch in the intestine following ingestion of mature. Rubinsky-Elefant respiratory signs including coughing and et al. Overgaauw continues to point strongly towards general and van Knapen. hypopro- ity of VLM are likely to be a function of the teinaemia. fore exists. 2008). and eyes (Sprent. larvated eggs. migrans. and intestinal rupture (Parsons. seroprevalence often high. OLM can occur in children and adults. emaciation. diagnosis on the basis of consistent clinical signs and detection of antibodies is insufficient. and the Other. and unless parasite material is recovered from biopsy material or post-mortem examination. Therefore. The signs and sever- and include weakness. Since OLM can involve only a sin- gle larva. The potential for infection site of infection. diarrhoea. dog hair has been demonstrated in the labora. Most studies finding substantial Syndromes associated with Toxocara infection numbers of eggs on dog hair have focused on are grouped into visceral and ocular larval stray dogs or those in poor hygienic condi.. flotation. with various ease or not. and ingestion through poor hygiene. but inflamma- weight loss. More recent work in well-cared-for pet dogs has found very low levels of eggs on Visceral larva migrans (VLM) hair (Keegan and Holland. 2003. 2001). and other unknown factors. where they can live for many years (Smith including asthma. Vertical transmission via the placenta and milk is efficient.1).. 2010). serological studies indicate an inconsistent or Migration of a large number of larvae through weak relationship between dog ownership and the liver and viscera can cause a pronounced antibody titre. 1958). 9. Since infections do Disease in animals not mature. and definitive diagnosis is elusive. Disease in adult dogs is rare and mild. titre (Smith et al. Clinical consequences depend on the tory (Keegan. 1987). depending on the loca- recognizable (Fig. even these recurrent abdominal pain. sug. intensive. and encouraging dog owners been established. immunology.. previous exposure to to remove faeces from public areas. with (Walsh. through poor hygiene cation of such treatment by dog breeders can after playing in contaminated environments be low. extend beyond statistical association. though life-long worming of dogs matched controls (Nicoletti et al. Seroprevalence typically increases with age. 1980). Prevalence . and various wild canids on measures to reduce egg shedding by dogs and felids throughout the world. continues to be suppressed. can be common in children and is a recognized risk factor for toxocarosis (Schantz et al. 2001). in order to reduce pollution and tion to the brain (Holland and Cox. treatment of this group should epidemiological studies in North America be early. 1987) and covert toxocarosis nities for faecal contamination of areas most (Taylor et al. However. control tive role of Toxocara is suspected but has not of stray dogs. pruritis. Pica. 2008). and deworming at 2 weeks of age and continu- lung function has not been investigated. drug treatment will not eliminate the reservoir of somatically Epidemiology and control arrested larvae. At Similarly. 2009). is needed to reduce ble to toxocarosis. Morgan eczema. 2010).. The rate of appli- likely to be exposed. given high seroprevalence in the (Kirchheimer and Jacobs. 2008. 2008). ment of pets with anthelmintic drugs. which were described in closely contacted by people. conducted. children are perhaps most larval establishment in pups. and it must be assumed that most pups (Gawor et al. Studies since egg excretion increases after pregnancy. Both refer to relatively typically excluded for safety as well as for low grade symptoms including weakness. but their efficacy has various tissues and associated inflammation in no case been determined (Atenstaedt and could cause a wide spectrum of clinical con.156 E. as a result of accumulated Toxascariosis exposure and long antibody persistence times (Smith et al.. Transmission to humans can in sequences. such as chil- different populations but are probably part of dren’s playgrounds. and hence should be treated accordingly. surveys failing to find lower egg density Asymptomatic infection is also likely to be inside such restricted areas than outside them common. will develop patent infections soon after birth. 2001). its aesthetic consequences as well as to reduce It seems likely that larval migration through Toxocara transmission. most recommended regimes commencing ship between infection. Since Toxocara infection has been associated with prevalence and egg output are highest in diminished lung function in cross-sectional young pups. This includes common toxocarosis principle be reduced by decreasing opportu- (Glickman et al. and coughing (Overgaauw and into the environment. Bitches should lepsy.. through regular treat- van Knapen. Toxocara seroprevalence was higher this time. and sustained. Therefore regular treatment of bitches in late pregnancy. the frequency of treatment can be in patients in Italy who had epilepsy than in reduced. Toxascaris leonina occurs in the small intes- Control of toxocarosis in humans relies tine of the dog. propriate material. from which dogs are the same syndrome. Thus. cough. Jones. 2008). Magnaval et al. 2011). public health reasons. is the only way to ensure that egg shedding gesting that infection increases the risk of epi. persistent anthelmintic. In most cases the causa.. Although larvae can be killed by anthelmintic treatment during migration in the pregnant and lactating bitch. in rodent models suggest that altered host Measures to reduce dog fouling are widely behaviour might be a feature of larval migra. or treatment with a Although humans of all ages are suscepti. but again evidence does not currently be wormed at the same time as their pups. 1987). cat.. but the mechanistic relation. measures are not always effective. with or without eosinophilia. ing every 2–3 weeks until 12 weeks of age.R. the consumption of soil and other inap. absence of widely reported disease. with some and headache.. Dogs and Nematode Zoonoses 157 is typically lower than for Toxocara spp. The transient diarrhoea. Ancylostoma spp., on the zoonotic potential of Toxascaris is tradition- other hand, often causes significant disease. ally considered to be limited, because somatic Percutaneous infection is associated with ery- migration in the definitive host does not thema and inflammation of the skin of the occur as part of the normal life cycle, and lar- feet, especially the interdigital area, and can vae are not vertically transmitted. However, cause lameness. Accumulation of large bur- specific studies are not available to confirm dens of adult worms, especially in pups, can the lack of zoonotic threat from this genus. In cause severe anaemia and haemorrhagic diar- the dog, intestinal burdens are typically low, rhoea. A. caninum is the most widespread and and clinical signs are not observed. Measures common species in dogs, with A. braziliense to reduce Toxocara infection in dogs, and con- more restricted in distribution and apparently tamination of the human environment with less pathogenic in dogs. Infection in dogs can eggs, are also likely to be effective in reducing be diagnosed by flotation and identification human exposure to Toxascaris. of the egg. Hookworms (Ancylostomatosis) Disease in humans Dogs are host to two genera of hookworm, The larvae of some species of Ancylostoma, Ancylostoma and Uncinaria. Their distribu- especially A. braziliense, can penetrate the skin tion is unequal, with Uncinaria most common of humans, causing cutaneous larva migrans in cooler temperate regions, and Ancylostoma (CLM), while others such as A. caninum have more prevalent in warmer, sub-tropical and been implicated in eosinophilic enteritis, tropical regions (Thompson and Conlan, 2011). neuro-retinitis, and other manifestations in humans (Bowman et al., 2010). CLM occurs when L3 penetrate the skin and migrate within the dermis. Although this infection does not Mode of transmission mature and is often limited to the skin, the inflammatory reaction can be considerable, Ancylostoma species lay eggs, which pass leading to pruritis and pain in association out in the faeces, and from which larvae with the development of erythematous tracts hatch and develop in the external environ- as the larvae migrate. Usually the infection is ment to the infective third larvae stage (L3). self-limiting and can last days, weeks, or even Dogs can be infected by ingesting L3, or L3 months. After elimination of the larvae, scar- can penetrate the skin, and migrate to their ring can be considerable. CLM is most com- final site in the gut via the lungs. In addition, mon in warm, moist areas in which humans larvae can arrest in the somatic tissues and walk barefoot, and disease is most common migrate to the unborn pups, in a similar way in the tropics and sub-tropics, especially in to Toxocara. Uncinaria lacks the percutaneous children. infection route. Methods of control Disease in dogs Control strategies are similar to those for Toxocara, Hookworms are blood feeders and their pres- with regular anthelmintic treatment of dogs, ence can cause significant disease. Uncinaria and environmental hygiene – especially is typically present at fairly low levels and, faecal removal and disposal – forming the except in working dogs (such as racing grey- mainstays. In dogs housed together in runs, hounds) kept in external runs that allow the larval levels can build up considerably, and build-up of large numbers of larvae, infection moving dogs between runs might be neces- does not usually cause clinical signs beyond sary, along with regular treatment. Burdens 158 E.R. Morgan can sometimes be difficult to clear even with subcutaneous tissues, but also in the subcon- repeated treatment, possibly due to contin- junctiva. The most common manifestation ued larval release from the somatic reservoir is a painful, erythematous nodule 1–6 cm in (Georgi and Georgi, 1990). Normal hygiene diameter. The infection does not progress precautions can reduce human exposure, as beyond this stage, but surgical excision might well as limiting skin-to-ground contact, for be performed. In theory, spread of D. repens example by wearing shoes. northwards in Europe places more dogs and humans at risk of disease (Genchi et al., 2010). Treatment of dogs can be achieved using arsenical drugs and macrocyclic lactones Filariosis (Baneth et al., 2002). However, most infec- tions in dogs appear to be subclinical, form- Filarial nematodes generally occupy the ing a reservoir of zoonotic disease. connective tissues, and are transmitted by arthropod ectoparasites. Genera of zoonotic importance that infect dogs include Dirofilaria and Brugia. Brugia malayi B. malayi causes lymphangitis and related clinical disease in humans in tropical South- Dirofilaria immitis East Asia. Although the infection has been reported in dogs, the main animal reservoirs This species causes heartworm disease in are monkeys and cats, and the infection also domestic dogs. The adult worms are large circulates between humans (Meyrowitsch and live in the right side of the heart, caus- et al., 1998). Dogs are not considered to be a ing congestive heart failure as well as a range source of zoonotic disease. of other complex clinical syndromes includ- ing coagulation disorders. Microfilariae are released into the blood and infect the mos- Gnathostomosis quito vector during feeding, where they mature to the infective L3 stage, to be re- injected during subsequent feeding. The Gnathostoma spinigerum is found in gastric nod- adult worms take many months to mature ules in dogs and wild carnivores, including and can live for several years. D. immitis is canids and felids. Eggs are shed in the faeces traditionally distributed in warmer climates, and pass through an aquatic copepod interme- but has spread in recent years as a result of diate host and a range of paratenic hosts includ- climate change and dog movement (Genchi ing freshwater fish, amphibians, reptiles, small et al., 2008). Humans can be infected, but such mammals, and poultry (Nuamtanong et al., infections are very rare. Worms can migrate 1998). In dogs, larvae undergo a destructive to the lungs and sometimes to the subcutane- migration through the abdominal cavity and ous tissues, but do not mature and cause no liver before reaching the stomach, where they significant pathology. Serology, radiography, develop in the mucosa, producing protruding and biopsy can be informative. gastric tumours. Dogs can be asymptomatic or suffer from vomiting and polydipsia. Diagnosis is by identification of eggs in the faeces, and worms are killed by anthelmintic therapy. Dirofilaria repens Humans become infected by consumption of meat from infected paratenic hosts containing The adults of this species occupy the subcu- encysted L3 stage larvae. Larvae do not mature taneous tissues of dogs and other carnivores in the stomach, but rather migrate to the skin, in Europe, Asia, and Africa. Transmission to most commonly forming erythematous, pruritic humans via infected mosquitoes leads to lar- swellings (Ruznak and Lucey, 1993). Deeper val migration and maturation, especially in migration involving the respiratory tract and Dogs and Nematode Zoonoses 159 other organs can occur, leading to more severe primates. It has a tropical distribution. Infection disease, which in the case of CNS migration can causes mucosal disruption and a protein-losing be fatal (Schmutzhard et al., 1988). Diagnosis is enteropathy, which manifests as diarrhoea and by recovery of worms by biopsy, and/or serol- emaciation. Infections are most usually self- ogy (Nopparatana et al., 1991; Maleewong limiting, but in immuno-suppressed patients et al., 1991). Anthelmintic treatment is effective. (canine and human), infection can generalize to Prevention is based on avoiding consumption other organs, with fatal consequences (Stewart of poorly cooked paratenic hosts, especially et al., 2011). The parasite can persist asymp- freshwater species, in endemic areas. tomatically for many years, causing disease following subsequent immuno-suppression. Only females are parasitic, producing eggs by Thelaziosis parthenogenesis that pass out in the faeces, hatch to L1, and develop to the L3 stage. L3 can infect a new host, continuing the cycle, or Thelazia californiensis and T. callipaeda infect develop into free-living male and female adult dogs and cats in North America and in Asia, worms, which maintain a population outside respectively, with recent emergence into the host (Viney, 2006). Infection is by penetra- Europe (Otranto et al., 2011). Adult worms tion of the skin, followed by migration to the are found under the conjunctival mem- intestine. Although S. stercoralis infects both branes, and are commonly known as eye- dogs and humans, human-to-human trans- worms. Muscid flies act as vectors, taking mission occurs, so the zoonotic importance up the first-stage larvae (L1), and depositing of canine infection is probably limited to rela- the L3 during feeding on lachrymal secre- tively few cases. tions. Irritation by the presence of the adult worms causes pain, blepharospasm, some- times ulceration, and profuse lachrymation, which attracts fly vectors. Human infection Other Nematodes is rare but has been reported, and manifests as pain and conjunctivitis, and the sensation A number of other nematodes infect both of a foreign body in the eye. Infections may dogs and humans, but cases of zoonotic be self-limiting, but physical removal of the transmission are either rare, or likely to worms is recommended. come from animal hosts other than from dogs. These include the nasal and respira- tory worms in the genera Capillaria and Strongyloidosis Eucoleus, the kidney worm Dioctophyma renale, and the Guinea worm Dracunculus Strongyloides stercoralis is known as the intes- melitensis. Given the minor role of dogs in tinal threadworm, and parasitizes the small the epidemiology of human disease, these intestine of dogs as well as humans and other are not considered further. References Atenstaedt, R. and Jones, S. (2011) Interventions to prevent dog fouling: a systematic review of the evidence. Public Health 125, 90–92. Azam, D., Ukpai, O.M., Said A., Abd-Allah, G. and Morgan, E.R. (2012) Temperature and the development and survival of Toxocara canis eggs. Parasitology Research 110, 649–656, epub July 21 2011. Baneth, G., Volansky, Z, Anug, Y., Favia, G., Bain, O., Goldstein, R.E. and Harrus, S. (2002) Dirofilaria repens infection in a dog: diagnosis and treatment with melarsomine and doramectin. Veterinary Parasitology 105, 173–178. 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(1991) Detection of circulating parasite antigens in murine gnathostomiasis by a two-site enzyme-linked immunosorbent assay. American Journal of Tropical Medicine and Hygiene 46, 80–84. Meyrowitsch, D.W., Toan, N.D., Hao, H.T., Toan, N.D., Hao, H.T., Dan, N.T. and Michael, E. (1998) A review of the present status of lymphatic filariasis in Vietnam. Acta Tropica 70, 335–347. Mizgajska, H. (2001) Eggs of Toxocara spp. in the environment and their public health implications. Journal of Helminthology 75, 147–151. Nicoletti, A., Sofia, V., Mantella, A., Vitale, G., Contrafatto, D., Sorbello, V., Biondi, R., Preux, P.M., Garcia, H.H., Zappia, M. and Bartoloni, A. (2008) Epilepsy and toxocariasis: a case-control study in Italy. Epilepsia 49, 594–599. Nopparatana, C., Setasuban, P., Chaicumpa, W. and Tapchaisri, P. (1991) Purification of Gnathostoma spini- gerum specific antigen and diagnosis of human gnathostomiasis. International Journal of Parasitology 21, 677–687. Nuamtanong, S., Waikagul, J. and Anantaphruti, M.T. (1998) Gnathostoma infection in swamp eels, Fluta alba, in central Thailand. Southeast Asian Journal of Tropical Medicine and Public Health 29, 144–147. Otranto, D. and Eberhard, M.L. (2011) Zoonotic helminths affecting the human eye. Parasites and Vectors 4, 41, DOI: 10.1186/1756-3305-4-41. Overgaauw, P.A.M. (1997) Aspects of Toxocara epidemiology: Toxocarosis in dogs and cats. Critical Reviews in Microbiology 23, 233–251. Overgaauw, P.A.M. and van Knapen, F. (2008) Toxocariasis, an important zoonosis. European Journal of Companion Animal Practice 18, 259–266. Parsons, J.C. (1987) Ascarid infections of cats and dogs. Veterinary Clinics of North America 17, 1307–1339. Dogs and Nematode Zoonoses 161 Roddie, G., Stafford, P., Holland C. and Wolfe, A. (2008) Contamination of dog hair with eggs of Toxocara canis. Veterinary Parasitology, 152, 85–93. Rubinsky-Elefant, G., Hirata, C.E., Yamamoto, J.H. and Ferreira, M.U. (2010) Human toxocariasis: diagno- sis, worldwide seroprevalences and clinical expression of the systematic and ocular forms. Annals of Tropical Medicine and Parasitology 104, 3–23. Rusnak, J.M. and Lucey, D.R. (1993) Clinical gnathostomiasis: case report and review of the English-language literature. Clinics in Infectious Diseases 16, 33–50. Schantz, P.M. and Stehr-Green, J.K. (1988) Toxocaral larva migrans. Journal of the American Veterinary Medical Association 192, 28–32. Schantz, P.M., Weis, P.E., Pollard, Z.F. and White, M.C. (1980) Risk factors for toxocaral ocular larva migrans: a case-control study. American Journal of Public Health 70, 1269–1272. Schmutzhard, E., Boongird, P. and Vejjajiva, A. (1988) Eosinophilic meningitis and radiculomyelitis in Thailand, caused by CNS invasion of Gnathostoma spinigerum and Angiostrongylus cantonensis. Journal of Neurosurgery and Psychiatry 51, 80–87. Smith, H., Holland, C., Taylor, M., Magnaval, J.F., Schantz, P. and Maizels, R. (2009) How common is human toxocariasis? Towards standardizing our knowledge. Trends in Parasitology 25, 182–188. Sprent, J.F.A. (1958) Observations on the development of Toxocara canis (Werner, 1782) in the dog. Parasitology 48, 184–209. Stewart, D.M., Ramanathan, R. and Mahanty, S. (2011) Disseminated Strongyloides stercoralis infection in HTLV-1-associated adult T-cell leukemia/lymphoma. Acta Haematologica 126, 63–67. Stürchler, D., Weiss, N. and Gassner, M. (1990) Transmission of Toxocariasis. Journal of Infectious Diseases 162, 571. Taylor, M.R.H., Keane, C.T., O’Connor, P., Girdwood, R.W.A. and Smith, H. (1987) Clinical features of covert toxocariasis. Scandinavian Journal of Infectious Diseases 19, 693–696. Thompson, R.C.A. and Conlan, J.V. (2011) Emerging issues and parasite zoonoses in the SE Asian and Australasian region. Veterinary Parasitology 181, 69–73. Viney, M.E. (2006) The biology and genomics of Strongyloides. Medical Microbiology and Immunology 195, 49–54. Walsh, M.G. (2010) Toxocara infection and diminished lung function in a nationally representative sample from the United States population. International Journal for Parasitology 41, 243–247. Wolfe, A. and Wright, I.P. (2003) Human toxocariasis and direct contact with dogs. Veterinary Record 152, 419–422. Won, K.Y., Kruszon-Moran, D., Schantz, P.M. and Jones, J.L. (2008) National seroprevalence and risk factors for zoonotic Toxocara spp. infection. American Journal of Tropical Medicine and Hygiene 79, 552–557. Yoshikawa, M., Nishiofuku, M., Moriya, K., Ouji, Y., Ishizaka, S., Kasahara, K., Mikasa, K.I., Hirai, T., Mizuno, Y., Ogawa, S., Nakamura, T., Maruyama, H. and Akao, N. (2008) A familial case of visceral toxocariasis due to consumption of raw bovine liver. Parasitology International 57, 525–529. . mately 3–4 mm in length. Edinburgh.N. Halliwell* Emeritus Professor. This ally short-term with spontaneous resolution. the practice of ‘one host specificity. not found in one survey (Harman et al. Of concern also are the other hosts of Ct.g. 2002. Harman et al. Ctenocephalides canine ectoparasites have varying host specifi. felis is the subspecies most commonly found city. with which diagnoses are made. raccoons. but rarely if ever on squirrels. Dogs. Gracia et al. Mating occurs after a blood meal. 2005. 2008). affecting 100 individuals. which affected 65. Beck et al.. 1971).. Fleas It is found on foxes. scabies. Cheyletiella. Royal (Dick) School of Veterinary Studies. 2nd Edition 162 (eds C. man is at risk of acquiring some of these on dogs and cats worldwide. which comprises in excess sharing the same environment. opossums. felis. and flea infestation is affected 45 patients. felis that may Insecta aid in the spread of infestations. as evidenced by species found on dogs in studies conducted in many publications in the literature attesting to a many parts of the world over the last 25 years lack of co-operation between medical and veter. This publication is arguably Echidnophagia gallinacea (the ‘stick-tight’ flea).L. chapter will discuss these four parasites. one 2007. Indeed.. (e. the most comprehensive description of the dis. rabbits.W. and a number of minor species whose natural ease problems. Biology and birds (Dryden and Rust. Macpherson et al. felis does not survive. inary specialists which has limited the precision Durden et al. e-mail: richard_halliwell@btopenworld.. 1987). It has been the predominant medicine’ is still relatively rare. Bond et al. Alcaino et al.. and ferrets. which Ct. Ct. the pearly white eggs are laid on the host. The major problem is thus Ct.. and that may have to be considered in any control strategy. and has limited infestations. Zoonoses and Public Health.. 1994). 1987. Pulex irritans. simulans. UK Increasingly.) .com ©CAB International 2013. 2006. and this will be the focus of this discussion. and because of 2000 species and sub-species. wingless insects approxi. However. and three who were pos. (Hewitt et al. sitic zoonoses that resulted from collaboration Other species found in small numbers were between medical and veterinary dermatologists Archeopsylla erinacei. and Fleas are brown. In some fleas. followed by colder climates such as northern Scandinavia. canis was very has to go back to the 1970s to find a publication much the minor species in all regions and was detailing a large case series of canine ectopara. 10 Dogs and Ectoparasitic Zoonoses Richard E. P. acquired from wildlife. However this is gener- sibly suffering from Otodectes infestation. Most commonly reported were hosts are rodents and other wildlife. They belong to the but usually fall to the ground where the three * Author. human beings and their pets are order Siphonaptera. A relative humid. involv- do not do well at very high humidity and ing both immediate (IgE) and delayed high temperatures. and that the degree of hypersensitivity wanes monly. burrowing deep into carpets and cracks and crevices in the flooring (Dryden and Rust. at least in part. it is now encountered not uncom. Dogs and Ectoparasitic Zoonoses 163 larval stages are completed. is unclear. and CO2 (Dryden that of the fleas on the host (Fig. and that continual exposure is of Scandinavia. Thus in North America Halliwell. This is the most resistant phase. The flea bites to suck blood. Host-seeking is likewise and hair loss with a distribution that follows aided by light. lished by observing compatible clinical signs. and from high altitudes. Once on the dog. 1981). 10. 1990). (ii) atopic dogs are Sweden from which Ct. The primary eruption in flea allergy der- The adult is stimulated to emerge by vibra. Self-trauma leads to a range of second- left empty for some time. The latter also have other effects on the host. and ter adaptation to adverse conditions. which may crust tions. However in some areas of protective (Halliwell. Flea saliva contains Serology for flea antigen-specific IgE will not multiple protein allergens that are recognized identify those animals suffering from delayed in varying combinations. There is often a massive. The entire life cycle can be completed in as little as 14 days. immunologically tolerant (Halliwell and Flea infestation in the dog Longino. felis have been investigated in detail Fig. and observing for imme- matitis due to fleas are in fact allergic to the sal. or at low humidity and (cell-mediated) hypersensitivity (Gross and high temperatures. and produce a silk-like cocoon in which pupation occurs. absent. but they can demonstration of hypersensitivity. in the older dog (Halliwell et al. doing injects salivary antigens. quarters. reliable flea antigen. hypersensitivity alone (some 15%). diate (15 min) and/or delayed (48 h) reactions. Occasionally frank urticaria may be simultaneous hatch when premises have been seen. attention is readily (McDermott et al. and the when the pet is hypersensitive. 2000). 10. The third-stage larvae are around 4–5 mm in length. and CO2. 1985) and also cutaneous basophil they are absent from the desert south-west hypersensitivity (Halliwell and Schemmer. 10. Cte f 1. over. They are also absent 1987). and in so (Silverman and Rust..3). and sometimes a ary changes including widespread erythema bimodal hatch occurs. Flea allergy dermatitis drawn to the possible source of the human .1. Whether this has resulted from bet. has been cloned and is recognized by When both dog and owner in the same sera from some 90% of hypersensitive dogs household are pruritic. fleas tend to diagnosis of flea allergy dermatitis is estab- have a predilection for the stomach and hind.1). They has a complex immunopathogenesis. Fleas can lead to a severe dermatitis the presence of fleas or flea faeces. ivary antigens (Fig. Other studies have shown that (i) all from the more northern parts of Canada.. The major allergen. matitis is a papule (Fig. 10. In dogs can become allergic to fleas if intermit- Europe they are absent from northern parts tently exposed. ity of 70–80% and a temperature of 30°C are optimal for most stages of the life cycle. 1985). heat. 1994). Larvae are posi- tively geotactic and negatively phototactic. movement. and can last for some months. The environmental conditions favourable to the development of the different life stages of Ct. is best achieved by intradermal tests using a It is likely that all dogs that develop der.2). felis was previously predisposed to the development of flea allergy. 1987). or from (iii) dogs who are continually exposed to fleas global warming. The and Rust. but it commonly takes 3–4 weeks. and do not develop dermatitis are. 1994). 164 R.E.W. Halliwell from the canine host. The fleas are especially aggressive when the house has been empty for a period, and in such cases they usually attack the ankles and lower limbs. White socks are known to attract the fleas, and indeed have been used to estimate flea numbers in an environment. Second, they may transfer to family members when they lie close to the ani- mal, or stroke it. In this case, the distribution is more generalized. The classical primary lesion is papular urticaria. Lesions consist of grouped papules that commence with irregu- lar urticarial wheals some 5–10 mm in diam- Fig. 10.2. Papular eruptions resulting from flea bites eter (Hewitt et al., 1971). After 24 h these are in a dog. replaced by small pruritic papules. In severe cases, a widespread papular rash develops leading to self-excoriation and lichenifica- tion. Ulceration and lichenified plaques may ensue in chronic cases, and become secondar- ily infected. The clinical signs may be severe enough to prompt relocation of the family to a flea-free area. It is likely that the progression of the eruption reflects different aspects of the immunopathogenesis. It is assumed that both immediate and delayed hypersensitivity occur in man, although this does not appear to have been investigated as thoroughly as in the dog. However, one recent study of Fig. 10.3. Extensive hair loss and inflammation resulting patients suffering from papular urticaria has from flea-bite hypersensitivity in a dog. demonstrated a Th1/Th2 imbalance (Cuéllar et al., 2009). skin disease. More troublesome in terms of Of perhaps greater zoonotic signifi- making the correct association are dogs har- cance are diseases that Ct. felis can transmit. bouring fleas and showing no clinical signs. The dog tapeworm D. caninum can, on occa- A careful assessment is needed to establish the sions, affect man and especially children presence of fleas in such cases. Use of a flea (Jones, 1979). Murine typhus is ordinarily comb many be helpful, and some recommend a mild febrile illness causing headaches, vigorous brushing of the coat and collection chills, skin rashes, and occasionally a more of the resultant debris for subsequent exami- serious disease involving the kidneys and nation. Faeces are identified by placing the CNS. The disease occurs in man and many debris on a moistened white paper, to which small mammals, and the causative organism, they will impart a reddish-brown colour. Rickettsia typhi, can be transmitted by Ct. felis, The non-allergic effects of fleas on dogs although the major vector is the oriental rat include anaemia, transmission of the dog tape- flea, Xenopsylla cheopsis (Farhang-Azad et al., worm D. caninum, and the non-pathogenic 1984). Ct. felis has also been shown to be filarid Dipetolonema reconditum. able to transmit Yersinia pestis, the causative organism of bubonic plague. The emergence Zoonotic implications of feline plague as a significant problem in the western United States, not only in domes- Fleas can infest man when they hatch in a tic cats but also in wild felids (Bevins et al., contaminated environment or by movement 2009), has emphasized the important role Dogs and Ectoparasitic Zoonoses 165 that cats and Ct. felis can play in transmission developed, taking into account (i) the extent to man. Experimental infection of cats gives of the infection, (ii) the presence and habits of rise to a disease very similar to that in man other animals in the house, (iii) the lifestyle, (Watson et al., 2001), and a report details 23 and (iv) the inside and outside environment cases of human plague, five of which were and the likelihood of reinfestation. A brief fatal, attributed to feline contact (Gage et al., description of the newer adulticides follows: 2000). Of course, this concerns cats, and not • Fipronil (Frontline®, Merial). Available as dogs, but the ease with which Ct. felis can a spray or spot preparation for dogs and move between these two species implies that cats. infection from Ct. felis carried by dogs is not • Imidocloprid (Advantage®, Bayer). For impossible. Finally, mention must be made of spot-application to dogs and cats. cat scratch disease and the causative organ- • Selamectin (Stronghold® or Revolution®, ism Bartonella henselae. This organism ordi- Pfizer). For spot-application to dogs and narily causes subclinical disease in cats, but cats. some animals may show a transient anaemia, • Nitenpyram (Capstar®, Novartis). Short- fever, and occasionally neurological signs acting (24 h), administered orally for (Kordick et al., 1999). In chronic cases lym- dogs and cats. phadenopathy, gingivitis, stomatitis and fever • Metaflumizone (ProMeris®, Fort Dodge). may occur (Breitschwerdt and Kordick, 2000). For spot-application to dogs and cats. Transmission to man is believed to occur Also available with amitraz as ProMeris through flea faeces, which are inoculated by Duo® for dogs only. the scratching or biting of the cat (Foil et al., • Pyriprole (Prac-tic®, Novartis). For spot 1998). Although fever and lymphadenopathy application to dogs only. are the signs classically associated with cat • Spinosad (Comfortis®, Eli Lilly). For oral scratch disease in man, a range of far more administration to dogs only. serious clinical signs may be seen, especially in • Dinotefuran (Vectra®, Ceva). Topically to immunosuppressed patients (Breitschwerdt, dogs with permethrin and pyriproxifen 2008). More recently, epidemiological studies (Vectra 3D) and with pyroproxifen alone of antibody prevalence in different popula- for cats. tions have fuelled speculation that the dog • Indoxacarb (Activyl®, MSD). Monthly may also be a reservoir for Bartonella hense- spot-on formulation for dogs and cats. lae (Henn et al., 2005, Solano-Gallego et al., 2004). A variety of chronic diseases in turn Not all of these products are available in have been attributed to the infection in dogs, all countries of the world. including granulomatous hepatitis, peliosis, All animals in the home must be treated and epistaxis (Chomel et al., 2006). Thus there with an effective adulticide; in addition, exists a clear possibility that dogs, through thought must be given to interrupting the life their carriage of Ct. felis, could be a source of cycle. This can be accomplished by the use of this important disease of man. insect development inhibitors (IDIs) or insect growth regulators (IGRs). An example of an The treatment of canine flea infestation IDI is the chitin synthesis inhibitor, lufenuron (Program®, Bayer) which is administered Twenty years ago, flea control largely comprised orally once per month to dogs, and is available the use of pyrethrins, pyrethroids (their syn- as a 6-monthly injectable for cats. The IGRs thetic analogues), and organophosphates – the include the triazine derivative, cyromazine, latter being used at some risk to both owner and the juvenile hormone analogues (JHAs) and pet. However, the past two decades have fenoxycarb, methoprene, and pyriproxifen. seen the development of some remarkable Cyromazine is administered orally, and inter- new chemicals, some of which are now avail- feres with chitin deposition rather than with able as ‘over-the-counter’ products. It is none its synthesis. The mode of action of the JHAs the less essential that professional advice be is quite different. Normal pupation is initiated obtained, and a safe and effective strategy by a fall in the level of insect juvenile hormone, 166 R.E.W. Halliwell and if JHAs are present in the environment, pupation is prevented. They are also ovicidal and larvicidal (Dryden and Rust, 1994). The JHAs are available for on-animal use, as well as for environmental application – often in com- bination with an adulticide such as the pyre- throid, permethrin. Of the three that are the most widely used, methoprene is sensitive to ultraviolet light, and thus has a limited dura- tion of action; pyriproxifen and fenoxycarb are stable, and persist for many months in the environment. Indeed pyriproxifen is so effec- tive that concerns have been expressed over the possible effects on friendly insects when Fig. 10.4. Sarcoptes scabei adult mite and eggs. used outdoors. Faecal pellets are also visible. A number of flea repellents are marketed, but none have been shown to be efficacious in The infection in dogs independent, controlled trials. In tropical and subtropical climates, the In the majority of cases the disease is acquired external environment can be an additional from infected dogs. However, dislodged mites source of reinfestation – particularly if there can remain viable for up to 19 days under opti- are free-roaming cats. Organophosphates are mal conditions of 10°C and 97% relative humid- commonly used for control, concentrating on ity (Arlian et al., 1984a), and so acquisition of shady areas where there is plenty of organic infection from the environment is quite possi- debris. Larvae cannot survive in open areas ble. Consequently, pet shops, dog shows, and exposed to direct sunlight. veterinarians’ offices represent possible sources Complete and effective flea control is of infection. Direct or indirect contact with wild- now entirely possible with an appropriately life represents other likely sources of infection. formulated programme, but careful atten- Dependent upon the geographic location, infec- tion must be paid to its development, and the tion can be acquired from foxes (Davidson et al., agreed plan must be rigorously adhered to. 2008), badgers (Collins et al., 2010), ferrets (Phillips et al., 1987), racoons (Ninomiya and Ogata, 2005), and rabbits (Arlian et al., 1984b). A report from Arachnida Sweden identified Sarcoptes scabiei var. canis in wild lynx, pine martin, wolf, and mountain Mites: Sarcoptes scabiei var. canis hares (Mörner, 1992). Cats represent another possible source. Although infectivity for this Biology species appears to be quite low, sporadic cases are reported, with a recent report documenting Adults are white, oval-shaped globose mites four cases (Malik et al., 2006). In two instances the measuring 200–400 mm in length (Fig. 10.4). infection was apparently acquired from foxes, There are two pairs of anterior legs bearing whilst the other two cases had close contact with long stalks with suckers, and two pairs of pos- infected dogs. Interestingly, the clinical signs terior legs bearing bristles alone. Copulation were more suggestive of Norwegian (crusted) takes place on the skin surface in moulting scabies with little pruritus, than of feline scabies pockets, with the female then burrowing that is ordinarily caused by Notoedres cati. into the epidermis where she lays eggs. After Penetration is achieved within 30 min hatching, the 6-legged larvae moult into 8-leg- and is aided by a mite secretion that dissolves ged nymphs, and then into adults at which host tissue. As might be expected, the intrader- point they merge onto the surface. The entire mal deposition of antigen normally provokes life cycle can be completed in as little as 3 a strong immune response which leads to weeks. marked inflammation, and affects the disease Dogs and Ectoparasitic Zoonoses 167 outcome. It has been shown that when normal which transmission occurs in those areas. The dogs are infected experimentally, a proportion primary eruption is a papule and burrows will in time self-cure (Bornstein, 1991). This may be visualized (Fig. 10.5). A variety of self-cure is enhanced when animals are re- changes may result from self-trauma, leading challenged after treatment with an ectoparasi- to extensive areas of hair loss, hyperkerato- ticide. Immunohistochemistry has shown that sis, and crusting. The disease may spread to self-cure is accompanied by an influx of CD4+ involve large areas, which are usually sym- T cells, both T-helper and inducer cells, together metrical, but the dorsum is ordinarily spared. with neutrophils (Arlian et al., 1997). Similar Occasional cases are reported with a localized findings have resulted from a study of the epi- distribution (Pin et al., 2006). The extreme demiology in Norwegian red foxes, suggesting pruritus that accompanies the disease often that subclinical infection and self-cure can lower leads to cachexia, as sleep is prevented and the incidence of overt disease in the population inappetance may develop. Proteinuria may (Davidson et al., 2008). Taken together, the above be seen, which is likely to result from an data suggest that a strong Th1 response is asso- immune-complex glomerulonephritis (Baker ciated with protection, whereas a Th2 response and Stannard, 1974). is associated with susceptibility. In support of A diagnosis of scabies in dogs is not easy this, it is frequently noted that mites are more to confirm due to the paucity of mites in the readily demonstrable in corticosteroid-treated lesions. The clinician will first look for clinical dogs than in animals not so treated. It is a mat- and historical signs that raise the index of sus- ter of conjecture as to which arm of the immune picion. Has there been an opportunity for con- response is responsible for the profound pru- tagion? If the disease is very pruritic, and (if ritus that is a feature of the disease. In part, of so treated) is it only partially corticosteroid- course, this could result from triggering of the responsive? Are other dogs affected, and are itch receptors at the dermoepidermal junction the owners affected? Are the clinical signs by the mechanical effects of the mites burrow- suggestive? Another useful indicator is the ing within the epidermis. pinnal–pedal reflex. The edge of the pinna One fascinating clinical variant of sca- is rubbed between the thumb and forefinger, bies, both in man and the dog (Patterson, and a positive response is shown by invol- 1995), is Norwegian or crusted scabies. This untary attempts to scratch with the hind is accompanied by severe crusting and a near limbs. In a recent study, a positive response absence of pruritus. Mites are demonstrable resulted in 82% of 55 dogs with confirmed in large numbers, implying a failure of the scabies (and 90% of those with overt pinnal protective immune response. In man this is disease), as compared with 6.2% of 533 dogs regularly associated with immunodeficiency with other miscellaneous pruritic dermatoses. diseases such as HIV/AIDS (Corbett et al., 1996). Recent studies of Norwegian scabies in man have shown a predominance of CD8+ T cells infiltrating in the dermis, with relatively few CD4+ cells, and high levels of IgE and IgG (Walton et al., 2008). No such studies have been undertaken in dogs, but the strik- ing similarities of the disease in man and dog suggests that the same underlying immun- opathogenesis is likely. Scabies affects predominantly younger dogs, which suggests an age-related immu- nity, and there is no sex or breed predisposi- tion (Feather et al., 2010). The disease usually commences in the less-haired areas, such as the ear margins, elbows, and ventral chest – Fig. 10.5. Severe, erythematous papular eruption in probably reflecting the greater ease with a dog due to scabies. 168 R.E.W. Halliwell This translates to a specificity of 93.8% and a of an infection. Although close contact with sensitivity of 81.8% (Mueller et al., 2001). the affected dog is usually reported, cases A definitive diagnosis is made by demon- are encountered wherein no direct contact stration of mites via skin scrapings in mineral has occurred, and indirect infection from the oil. The hair is gently trimmed away from an environment is assumed (Charlesworth and involved area, and the skin moistened with Johnson, 1974). The sites involved reflect oil. Remembering that the males live on the those most likely to be in the closest con- surface and the females within the epidermis, tact with the infected animal, which are fre- it may be helpful to take a very superficial quently the forearms, abdomen, waist, and scraping, and then return to the same area trunk. Lesions may localize in the region of for a deeper scraping. Nonetheless, however the belt or bra straps. The initial eruption carefully the scrapings are performed, they is a papule, and concomitant vesicles may may be positive in as few as 20–40% of cases. develop. In some cases urticarial lesions are If skin scrapings are negative, and the observed. The lesions are intensely pruritic, index of suspicion is still high, serology may and the pruritus is often worst at night and be undertaken. This is widely available in after bathing (Emde, 1961; Beck, 1965). In con- Europe, although not as yet in North America. trast to human scabies, burrows are not seen. One study showed an 84.2% sensitivity and There is an interesting report (Ruiz- 89.5% specificity (Lower et al., 2001), with Maldonado et al., 1977) of a case of Norwegian another showing both a sensitivity and spe- scabies in a child suffering from Turner’s cificity of 100% when borderlines were elimi- syndrome – a genetic condition character- nated (Curtis, 2001). There is some evidence ized by multiple endocrinopathies and also of cross-reactivity between mite species, and immune dysfunction (Rongen-Westerlaken so an important finding in the latter study et al., 1991). As noted earlier, the propensity was that, of 12 atopic dogs that were positive to develop this condition rather than classi- to Dermatophagoides farina, all were negative cal scabies may reflect a Th1/Th2 cell imbal- on sarcoptes serology. Positive serology may ance (Walton, 2010). Pruritus in this patient result for up to 4.5 months after successful was inconstant and mild, and lesions were treatment (Lower et al., 2001). characterized by extensive crusting. When Ultimately, if there is still a suspicion of the patient slept with other family members, scabies even in the light of negative results they developed severe pruritus with charac- to all appropriate tests, a therapeutic trial teristic papular eruptions. Mites were abun- with an appropriate parasiticide should be dant among the crusts, and skin scrapings undertaken. yielded a mean of 56 mites per 10 g of crust. Three dogs in the family were diagnosed with Zoonotic implications scabies, and a normal dog was infected by application of crust material from the child, The acquisition of infection reportedly with typical canine scabies resulting. occurs between 1 and 10 days after exposure The course of canine scabies infection in (Charlesworth and Johnson, 1974), but recent man is usually short, resolving within a few observations in a veterinary school suggests days of removing or treating the infected dog. that clinical signs may occur within 6 h of Parasiticidal therapy is not generally required, contact with an affected animal (T. Paterson, as the current view is that the mite cannot com- pers. comm., Grenada, 2011). Infection after plete its life cycle on man. However, the time even prolonged contact is not inevitable, and taken for resolution is very variable, and may in one report of an ‘epidemic’, some chil- be up to 3 weeks (T. Paterson, pers. comm., dren who had close contact were not infected Grenada, 2011), which might suggest multi- (Charlesworth and Johnson, 1974). The factors plication of the mites. In a study attempting that determine the likelihood of infection are to address this, two human volunteers were not known, but it has been hypothesized that infected with canine scabies mites under prior contact with the mite and consequent tightly controlled conditions (Estes et al., sensitization may facilitate the establishment 1983). Each received 14 adult female mites Dogs and Ectoparasitic Zoonoses 169 taken from a case of canine scabies. albeit in very low numbers (Shanks et al. are effective (Folz et al.. 1996).. ending in combs. naked eye. and one egg from (Advocate®. Shave biopsies revealed that eight and at 2. if the clinical signs per. 2010). The species most commonly found (Curtis. It is highly toxic in herding dogs which have the MDR1 mutation. A metaflumizone and amitraz combination Cheyletiella spp. or orally at the same dose.. but an unpleasant odour and may stain light-coloured coats. demodecosis. 1984). Amitraz dips. 2010). Of importance is the fact that this drug is not licensed for use in dogs for this purpose in any country of the world. 1965). a wide safety margin.. and is highly effective. The availability and licensing of scabicidal In view of the fact that live mites can per- drugs varies widely in different countries of sist in the environment for significant periods. They have four pairs of legs but the propensity for this drug to cause pem. 10.6). Indeed. Less toxic. Terada et al. It has would appear to be desirable practice. Fipronil mouthparts that end in a pair of sharp hooks spray appears to be both safe and effective (Fig. and in particular on the avermectins (ivermectin and selamectin) and the milbemycins (milbemycin and moxidec- tin). a 2. Stronghold®. are large mites. 2007).5% lime the use of a premise spray such as permethrin sulphur dip is available and effective. and nine eggs. respectively. and their most charac- phigus foliaceus-like drug eruptions limits its teristic feature is the presence of accessory usefulness (Oberkirchner et al. 2010). some 400– has been shown to give a cure rate of 83% 500 mm in length. had been deposited in an imidocloprid/moxidectin combination burrows on each recipient. be lacking this mutation. Bayer Animal each was observed to hatch. However. live mites were still Treatment of canine scabies found 30 days after the first application. that are just visible to the when applied biweekly (Fourie et al. Cheyletiella mite seen in a skin scraping sometimes encountered in dogs believed to from an infested dog. Advantage Multi®.... Biology ance may be acquired during treatment. using the protocol licensed for Cheyletiella spp. Ivermectin is widely used at 200–400 mg by subcutaneous injection biweekly. and more eight live mites were recovered from each vol. on dogs is C. sist for more than a few days after removal or is licensed for the treatment of scabies world- control of the source of infection.6. but anecdotal evidence suggests that resist. selamectin (Revolution®. while Newer approaches to the therapy of canine scabies have focused mostly on the macrocyclic lactones. After 96 h. Recent studies on experiment was terminated. wide. The broad-spectrum avermectin. 2011). many practitioners use this as a diagnostic aid. 1996. Pfizer). At this point the Health) (Fourie et al. appropriate for routine use are milbemycin unteer. The conclusions demodecosis have shown that this product is were that there is at least the potential for more effective and perfectly safe when admin- completion of the life cycle in man. yasguri (Smiley. In the United States. or at a higher dose of 500 mg topically (Paradis et al. parasiticidal therapy. the world.. it would seem prudent to prescribe et al. 10. but this may be inappropriate following the first report of ivermectin-resistant scabies in dogs (Terada et al. 2000). and toxic reactions are also Fig.0 mg/kg weekly (Miller et al.. it is somewhat slow to act.. 2006). . 1997). For these istered weekly instead of monthly (Paterson reasons. or dorsolumbar. 2004). important source. pterynossinus. 1976). and then pierce the skin with their dominantly dorsal. Halliwell r abbits typically harbour C. farinae and D. 2004). 2001). of those dogs which had approximately 3–4 weeks. Pet shops. four burrow. Also. and enquiry should be very varied host response suggests that an made of all humans who have contact with allergic response and possibly also protec.. dog from the activity of the mites. there been an opportunity for contagion. 2001). ment should also be assessed. For example. Other dogs and/or index of suspicion before pursuing confirma- cats in the household. and the species found on between the level of infestation as judged by domestic pets will depend upon the source of mite recovery. In chronic shows. and Vaillancourt. However. ing of eggs that have fallen from the host can As with scabies. One month later. gave negative skin. the first consideration be a ready and constant source both of infec. The mites do not previously shown positive IDT reactivity. Dermatopagoides C.170 R. Although live adults pseudotunnels may be palpable (Ayalew have a limited lifespan off the host. the pets. after larval and nymphal stages to the adult. and the clinical severity. The localization of threads (Foxx and Ewing. They both of which can range from minimal. Thus when the infection is acquired was evident (Saevik et al. to severe. it is from dermatological signs compatible with said – although with little documentation cheyletiellosis. and is gener- Cheyletiella infestation in dogs alized in the majority of cases (Saevik et al. they are attached to hair shafts by rather than scaling. ized.. but the cal signs of infection. are a very tion by the identification of mites or eggs. pruritus does not always coincide with the area of the most severe scaling. to assess whether any are suffering tive immunity may occur. parasitivorax. and on one host. 1979).W. 1980). such imity will become infested. The mites are obligate para.E. and ordinarily die within 48 h of removal employed for intradermal testing in affected from the host. in establishing the diagnosis is to assess the tion and of re-infection. Although no from rabbits. proceeding from eggs through 12 to D. 1969). grooming parlours. or periodically attach themselves firmly to the even absent. respectively. cats. dogs will frequently harbour antigen is currently available. but when not moving around on the and seven of them. This is an important consideration of infection from a contaminated environ- when considering control. parasitivorax. – that the disease is both more common and with C. may be the presenting a cocoon-like structure of closely woven fine sign (White et al. farinae. . None infection. The scaling is pre- epidermis. In heavy infestations. Often they will cause the The clinical signs are quite variable. epidermal debris. but scale to move causing the ‘walking dandruff’ generally consist of scaling with pruritus. that is characteristic of the infestation. are contained within pseudotunnels of intradermal tests to the two antigens. In some 15% of cases. However it is not inevitable A carefully taken history must assess whether that all dogs and cats that live in close prox. relying on putative cross-reactivity they may live for up to 10 days (Foxx and (White et al. the mites can be The infection is acquired from either direct visualized – especially when examined with or indirect contact with infected dogs. the hatch. cases. in successful treatment.. of course. One Allen. areas of crusting which represent ble avenues of infection. but stylet chelicerae and feed on tissue fluids. an oily haircoat. 1969). or being in an become infested but remain asymptomatic as area frequented by rabbits. However Cheyletiella are not study looked for evidence of any correlation highly host-specific. Thirteen of 23 affected ani- Ewing. some may as meeting other dogs or cats. blakei infesting cats (McKeever and more severe in puppies (Cohen. All in-contact There has been little work done on the dogs and cats should be examined for clini- immune response to Cheyletiella. may extend to the flanks or become general- The eggs may fall off into the environment. if kept refrigerated animals. The life cycle is completed mals gave positive reactions to D. a magnifying lens – and the scale may move or rabbits. and veterinarians’ offices are all possi. pteronyssinus extracts have been sites.. but if not. The possibility carriers. and sele- necrotic centre (Rivers et al. The distribution typically most efficient. develop (Dobrosavljevic et al. Burrows are diagnostic samples from the skin of affected not seen. Rarely. sitivity was evident upon intradermal testing (Maurice et al.. 1987). Some years ago. as has generalized pruri- number of different approaches to obtaining tus without evidence of lesions. includ- which suggests that the infection is readily ing pyrethrins and pyrethroids.. agents than is Sarcoptes scabei.. 2004). 1987). Attention must carial lesions.2% of cases. One patient was reported and skin scrapings were positive in 40. Chronic lesions frequently (Pagé. forearms. Lime sulphur. and resolution invariably fol- It is certain that Cheyletiella affects man with lows successful treatment of the implicated a far greater frequency than is diagnosed. it Cheyletiella. ivermectin become confluent. 1997. et al. indicating that contact is a specially adapted capture system was the generally brief. bullous lesions may also be paid to the environment. The selamectin (Fisher and Shanks. 2007). 2007). Although no prod- The primary lesion in man is generally ucts have a specific claim for Cheyletiella. 2000). Walton (1974) diagnosed 102 dogs with As Cheyletiella is a surface-dwelling mite. or more extensive urti. with a halo of erythema for that species. the hair immune complexes. Zoonotic implications Parasiticidal therapy of affected humans is unnecessary. Impressions employing clear involves the lower chest.. Dogs and Ectoparasitic Zoonoses 171 A recent study examined the efficacy of a (Hewitt et al. monly used insecticides are effective. cellulose tape pressed firmly on the skin and the anterior thighs. animal(s).. Less frequently there may cats. Most of the com- matitis consistent with Cheyletiella infection. numbness of the fingers. Using the latter techniques. but in one case a delayed hypersen- achieving a diagnosis.9% of to become systemically ill. but with the transmitted.. Little tion of faeces (McGarry. 1971). but may be widely scattered. and permethrin (Endris become pustular. and skin scrapings should be signs resolved spontaneously following suc- very superficial. 2008). characterized by a perivas- the hair shaft were positive in 54. of course. Carpets and any furniture . and taken from areas pre. exception of imidocloprid.. abdomen. and rabbits with a product appropriate be papular urticaria.1% of 26 cases. are published data documenting the efficacy of rounded by a fragile vesicle (Cohen.. etc.. some view as pathognomonic for Cheyletiella The human literature contains many reports (Hewitt et al. but there are is known of the immunological response of no data on the sensitivity of this approach in patients. Vacuuming with affected patients. but may extend to yielded positive results in 73. (Chadwick. Lesions ordinarily resolve of reinfestation resulting from inadequate con- within 3 weeks.. 1984). and care must be taken to treat all dogs. and may develop a yellow et al. cessful treatment of the infected animal. should be washed lesions mimicking erythema multiforme and at a high temperature. 1993). Scarampella et al. with elevated cases. 1971). 2001). tion is controlled.. should be carefully trimmed from the site and arthalgia (Dobrosavljevic et al. fipronil papules are usually found in small groups. cular lymphocytic infiltrate accompanied Eggs may also be found in routine examina... 1986) – which nium sulphide are also reportedly effective. amitraz. irrespective of whether the (Shelley et al. as long as the source of infec. the face and scalp.. All bedding. and grooming equipment. Hair pluckings Biopsies reveal a typical picture of an to examine for evidence of eggs attached to insect bite reaction. They do not milbemycin (White et al. The ease with which infection is acquired will. and mites are not recovered from animals (Saevik et al. and then treated with dermatitis herpetiformis have been reported a parasiticide. 2005). 1980). and 83 of the individuals in direct is more readily susceptible to parasiticidal contact with the dogs reported a pruritic der. The to be sampled. depend on the closeness of Treatment of canine Cheyletiella infection contact between man and dog. moistened with mineral oil. 2000). there an erythematosus papule which may be sur. by eosinophils (Maurice et al. trol. animals appear to be infected. It parasitizes early detailed study in the United Kingdom the ears of dogs and cats. mites were found in dogs or cats in et al. but it is esti. However. He observed that the mites tended to vacate mated to be around 10%. They can pet (Kristensen. This prompted the persist in the environment for up to 17 days at writer to speculate that a previous report of 95% relative humidity and 10oC (Milillo et al. with the Otodectes were found on the incriminated mites feeding on epidermal debris. 2001). 1980). Otodectes infection is implicated. 1978). Despite distributed on the body. a veterinarian. Both diminished degree of pruritus is extremely variable. as appear to be particularly susceptible. Immediate remove as many of the mites and eggs as hypersensitivity has been demonstrated in possible. were suspected (Hewitt et al. and otoscopic seen. which is a lower the ear canal during the night and walk over proportion than seen in cats. If it is suspected that the infestation . and also on The ears should be flushed with saline to the presence of hypersensitivity.. 1991) and the Eurasian lynx (Degiorgis 3 of 173 cases in which zoonotic insect bites et al. 1988). 1971).. both Cheyletiella and cycle is completed in around 3 weeks. or by skin Otodectes cynotis scrapings if there is extra-otic involvement. California might in fact have been due to they may leave the ear canal and be found Cheyletiella (Herwick. Proprietary prod. However. Young animals the face. The life in one case in Denmark. 1977). The pruritus was quite intense. and is likely to be depend. carefully removed by a cotton-tipped appli- cator moistened with mineral oil. with with time. whereas tion. and indeed this ectoparasiticide-containing proprietary otic was the first demonstration of the existence product. followed by application of an the cat (Powell et al. a convincing report of otitis with tinnitus in a patient. The mites similar to those produced by Sarcoptes were have a greyish appearance. and can be widely regulator are appropriate for this use. Halliwell f requented by the pets should likewise be of reaginic antibody in this species.. level of pruritus does not appear to be related to the mite burden.W. Even more convincing was There are no recent data on the proportion a report by Lopez (1993). on the eggs and larval stages. For example. the mites may some- containing a pyrethroid and insect growth times leave the ear canal. The response.. no such studies have been undertaken in the ucts marketed for environmental flea control dog. Although primarily an otic parasite.. As noted above. they are very Diagnosis is made by observation of the likely to be efficacious. 1978). who of cases of canine otitis externa in which infected his ear canals with Otodectes mites. mites and/or eggs in exudate from the ear canal.. but it is always difficult to prove a examination of the ear canal shows them to cause-and-effect relationship. Biology Zoonotic implications Otodectes cynotis is a non-burrowing psoroptid Man is rarely affected by Otodectes. Treatment of Otodectes in dogs ent on the extent to which secondary bacterial and/or yeast infection develops. Lesions measuring up to 500 mm in length. and rarely may be the fact that there is no documented evidence the cause of generalized pruritic dermatitis on the effect of juvenile hormone analogues (Kraft et al. The was the degree of tinnitus. there is elsewhere on the body. and an obligate parasite. In an mite. a case of presumed Otodectes dermatitis from 2004). and may also affect involving both veterinary and medical inves- wildlife including arctic foxes (Gunnarsson tigations. and were much less on reinfesta- some animals being asymptomatic.E. which resolved following appropri- ate acaricidal therapy (Van den Heyning and Otodectes infection in dogs Thienpont. It is just visible to the naked eye.172 R. have the appearance of cigarette ash. which suggested a protective immune others may develop extreme pruritus. treated with a parasiticide. E. S. W. R. I. H.A. (1980) Cheyletiella dermatitis. Fisher. (1984a) Survival and infectivity of Sarcoptes scabiei var. and Kordick. Veterinary Parasitology 112. S. Corbett. and Moore... H. 184–191. Cuéllar. R. .. This should be All of the common parasiticidal agents are supplemented by appropriate environmental effective. M. Wood.L.. selemectin (Blot et al. 261–262.G. 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S.. Silverman.. settlements by warning them of approaching Although dogs have many useful and predators or strangers. 11 Dog Population Management Elly Hiby World Society for the Protection of Animals.000–14. dogs to coexist with humans as opposed to a Both the roles that dogs fulfil and local cul- human attempt at domestication. and the same capacity populations may require management to is still valued by dog owners today.N. This chapter explores the problems * Author. London. This first related volatile compounds in urine samples of separation of species may well have been due people diagnosed with bladder cancer (Willis to the predecessor of the domestic dog associ. ivory. In recent ensure that the size and type of dogs within years there has been a proliferation of the roles the population matches the needs of human ‘assistance dogs’ can fulfil for people. But by far the most common role ating itself with early human hunters in order for dogs. UK Archaeological evidence for a close association World War I to dogs that can indicate to an between humans and dogs dates back to epilepsy sufferer the early stages of an oncom- around 12. such as the role as a ‘watch dog’. 2004). tural norms will impact on how dogs are kept Since humans became involved in dog by people. their of smell and hearing. Zoonoses and Public Health.000 years ago (Morey.org ©CAB International 2013. using their acute senses varied functions within human society. Some of these have stood the test of dogs are accepted as part of the ecology of a time. and one that is found in all countries to benefit from scavenging. and behavioural traits. from the society. explosives.L. hence a drive by of the world. 1997). 2006). In some cultures varied. et al. and that dogs can co-habit the environ- original guide dogs for the blind which were ment without undue risk to humans or other first formally trained in Germany following animals..) 177 . substances such as drugs. in some countries they are confined domestication. on private property and are accompanied by ficial selection for breeds with specific physical an owner whenever they leave that property. Dogs have even been shown in proof- far earlier. and later in very focused arti. or mon ancestor with the wolf may have occurred humans. genetic evidence suggests that the also been exploited by people to help locate separation of the domestic dog from a com. 2nd Edition (eds C. the roles that dogs have in other countries dogs are allowed to roam fulfilled in human society have been many and unsupervised by their owners.. Dogs’ superior sense of smell has however.000 years ago (Vila et al. ing seizure. Even community and are rarely considered as being the earliest domestic dogs benefited human owned by an individual person or household. some indicating a date greater than of-principle studies to be able to detect tumour- 100. e-mail: EllyHiby@wspa-international. is as a companion for humans. Macpherson et al. Dogs. 1995). and are management programmes that suit both the extremely unlikely to breed successfully. However. For example. the significant role in urban areas in the developing world. especially population. but the decision to humans. how these programmes can be evalu. the carrying capacity of the habitat. or purposefully killed dogs that either physically or behaviourally did not Carrying capacity match sufficiently a desired ideal. with some notable exceptions. and perhaps even withdrawn resources. resources in the form ness likely to be valued by children are ideal of waste often arise. and hence control mediated by the decisions of individual dog owners may Dog population management by owners be enough to manage the population success- fully. and breed in any location is determined by However. ter needed by each species and available Survival of individual dogs and their off. as disposal systems traits in a dog whose future function includes are overwhelmed. reproductively self-sustaining and hence finally. For the domestic dog these spring is very reliant on the resources made resources are predominantly controlled by available by people.. the extent of conscious plan. understanding of their dynamics and human In rural situations even those dogs that are attitudes towards them. Hiby that can arise from dog populations. For dog population and the human society in example. as opposed to an objective deci. This results in a high density of dogs in involve limited consideration of suitability both private and public areas. Concurrently they ethical reasons. property. hence the development of humane population cessful breeding to maintain a population of management programmes may be needed for dogs with desired traits. water. In addition. will have prevented breeding of less preferred individuals.178 E. a population of feral dogs observed which they live. so the owned dog population sion based on some concept of an ideal dog becomes increasingly dense and. and. humans have abandoned dogs and the methods of killing been selecting preferred individual dogs and unwanted dogs such as drowning and hang- providing care to ensure survival of these ing give rise to animal welfare concerns. However. this provides a relatively companionship. The potential components in a rural area of Italy in the 1980s was not of humane programmes are introduced. 1990). could not be maintained without contribu- ated to improve performance is discussed. hence in most locations the vast provide these resources may be predomi. It also considers populations may be sufficient to maintain the assessment of dog populations to improve the population of dogs at a tolerable level. and hence The dog owner-mediated control of dog motivations for management. uncontrolled resource that can be accessed . and how the results not purposefully killed but are abandoned of such assessments can be used to develop are unlikely to survive for very long. it should be noted are allowed to roam outside their owner’s that traits such as friendliness and playful. the level ning in dog population management on of resources such as food. in the habitat. and individuals. the suffering experienced by Since dogs were domesticated. as human populations decision. and often also to support suc. or when the number of dogs exceeded what was deemed The number of animals that can survive appropriate or possible to maintain. are not able to survive and breed successfully independent Problems of Dog Populations of resources provided by humans (WHO and and Motivations for Management WSPA. the of children in caring for dogs and therefore private property available to each dog is lim- selecting dogs that will be given care may ited. tion of new individuals from locally owned dog populations (Boitani et al. as owned dogs for function. majority of the dog population must be nantly a subjectively or emotionally driven owned. However. become dense. and shel- the part of humans can be overestimated. Dogs. street. The point at Coalition1 humane dog population manage- which these dogs become a nuisance will ment guidance (2008). towards these different categories of dogs and at some point these dogs may be seen as a also methods of managing their populations dif- ‘nuisance’ to society and either local people fer. Human attitudes towards animals in general. If ship status and/or their behaviour.1. as indicated by the arrows. It is this roaming dog. and specifically their tolerance towards dogs in the environment. as compared with the on the number of dogs. in some cultures dogs are by the ICAM Coalition is ‘One that is not cur- not just tolerated on public property but are rently under direct control or is not currently deliberately fed by people. commonly defined by their owner- or removing resources from roaming dogs. 11. extremely high density of ‘street dogs ‘seen One factor that can significantly impact in many Indian cities. Dog Population Management 179 by all dogs – including abandoned dogs that variation in human tolerance that leads to the would not otherwise survive. . is human tolerance of dogs. environment is assessed. sometimes called a stray. leading to dog restricted by a physical barrier’. Companion Animal Management (ICAM) tion. Figure 11.1 was taken from the International or authorities will act to reduce this popula. This diagram shows the sub-populations into which the total dog population can be partitioned. or to decrease the dog population Dog populations comprise different categories through limiting dog ownership and killing of dogs. Attitudes the density of the dog population increases. definition and Fig. Conversely. usually through killing.1 it can be seen that a ity of the visible waste resources. Sub-populations of the total dog population. depend on the attitude and tolerance towards The definition of a roaming dog provided dogs. but which is often relatively low densities of dogs seen in the missed when the carrying capacity of an cities of countries such as Egypt. Note that these categories are fluid and dogs may move between categories. 11. can work Defining categories within either to increase the dog population through the dog population increased dog ownership and care of roam- ing dogs. From this population sizes that seem beyond the capac. TOTAL DOG POPULATION CONFINED/CONTROLLED ROAMING DOGS IN BREEDING/COMMERCIAL SUPPLY CHAIN LOST REUNITED Owned dogs – lost ABANDONMENT Owned dogs – abandoned OWNED DOGS RESPONSIBLE OWNERSHIP Owned dogs – roaming REHOMING Unowned dogs – born roaming Fig. success of these dogs also means that if man. and ety. 1980). 1984) but rather a wild species • Nuisance through noise and fouling. of canid. relation to feral dogs. the owned dog that has been lost or abandoned. are often no longer considered behaviour. The definition of a feral dog used by Boitani et al.6 million from casualties in road traf- human settlements. feral (Price. such as the idea that category to another. In recognition of this. Notable excep- Coalition 2008): tions include Australian dingoes.9 million from dog bites leading to The limited lifespan and poor reproductive hospitalization. the survival and reproductive earlier in the chapter. An additional sub-category of unowned roaming dogs is feral dogs. the RSPCA (2010) dogs from one village visiting a neighbour- e stimated the annual societal costs of the 10 ing village in response to a female coming million dogs living in the UK. As discussed in an earlier section of human populations in urban areas described this chapter. management. and hence a focus for by humans. ments. For example. but will be most affected but rather a strong continuous avoidance by an increase in the proportion of unowned of direct human contact’. but it must be recognized that scrutinized and the causes of these problems the process of moving between these catego- highlighted as the focus for management. might actually be an owned of dogs to feral populations will lead to their dog that is allowed to roam. for found in rural areas outside human settle- example. 11. and have become feral due to being Problems caused by dogs include (ICAM forced out of the settlement. generations. 1989). Commonly the number of truly • Livestock predation. • £3. they can also cause problems to other ani- that did not show any evidence of socializa- mals and to humans. Hiby or free-roaming dog. In the section ‘Understanding As reflected in Fig. These included: into oestrus can be mistakenly termed feral or wild dogs by people in the receiving village. These may increase as the tion to humans (Daniels and Bekoff. the reduced contribution fic accidents involving dogs. under the conditions of dense ments. These cat- assessment of the situation is discussed. Such dogs may be or uncontrolled dogs in the population. which have bred successfully independent of resources • Disease transmission to other animals provided intentionally by humans for many and to people (zoonotic diseases). hence. dogs can move between agement’ (below) the importance of initial categories within their lifespan. Feral dogs for municipalities to quote complaints about have commonly begun life as owned or dogs as one of the top three concerns reported unowned dogs living within human settle- to the authorities by local citizens. definitions may all roaming dogs are unowned. and that indi- initial assessment should also challenge com. overestimated. It is not uncommon success of these dogs is limited. owned roaming In a recent report. (1995) is ‘a Problems caused by dogs dog living in a wild and free state with no direct food or shelter intentionally supplied Although dogs provide many benefits to soci- by humans (Causey and Cude.1 and discussed in dog populations and implications for man. vidual dogs may not move abruptly from one monly held assumptions. owned and unowned roaming dogs within • £14. having totally lost any • Injury and fear caused by aggressive domesticity. feral dogs that exist in a particular location is • Road traffic accidents.180 E. and. become blurred for individual dogs. • £2. dog population rises.8 million from injury to or killing of agement programmes effectively address the livestock. . so the egories are useful to help understand dog dog-related problems faced by society can be populations. or a recently eventual extinction. This ries will be just as important. rest of this chapter will focus on the confined The importance of this definition is that it is and roaming dogs found within human set- usually the roaming dogs that are perceived by tlements and relying on resources provided society to be a problem. sometimes termed a in control methods are improved to ensure any ‘duty of care’. Similarly. to ‘very bad’. 2004). In the case of domestic ani- through fighting and road traffic accidents. diseases such as mange and ble for the welfare of an animal will depend distemper which cause visible distress. ‘The greatness of a nation and its moral between 3 and 4 million per year (HSUS. diseases are endemic. and poorly equipped and managed level of welfare of owned animals is a legal holding facilities. ventions are used. when the activity number of dogs humanely culled due to lack of of humans impacts directly on the animal – available homes may be seen as an unacceptable for example. Dog Population Management 181 The UK is currently free of rabies and the animal may suffer both physically and Echinococcus. control the dog population by authorities can and this has altered the ability of these ani- also cause welfare problems including inhu- mals to cope with the environment. dog population management to reduce this Similarly. where none are achieved. the number captivity – its welfare is the responsibility of dogs and cats euthanized in government of humans and should be maintained at the and non-governmental centres is estimated highest possible level. related complaints reported by local citizens. If the environmental chal. electrocution. this can also lead to lenges overwhelm its ability to cope then failure to control the dog population. 1986). The problems caused by dogs are clearly a • Freedom from fear and distress.’ their estimate in 1973 of 13. shooting. Both owned and unowned dogs can suffer The extent to which people are responsi- from malnutrition. Problems encountered by dogs • Freedom from pain. progress can be judged by the way its ani- although this is a significant improvement from mals are treated. This is widely ment. if population management inter- unwanted or ‘surplus’ dog population. 2009). clubbing. and. In the United States. as their involvement its ability to cope with the challenges presented in any intervention is necessary for effective by its environment. which suggest animals should have: • Freedom from hunger and thirst. 1979). Legislation relating and drowning. • Freedom from discomfort. One ment of zoonotic diseases related to dogs will framework commonly used to measure the be far higher in countries where these two welfare of an animal is the five freedoms (FAWC. human responsibility. Even if the practices involved obligation of owners. As Mahatma Gandhi by the Humane Society of the United States as said. Using inhumane meth- Dog welfare and humane management ods of management is not only unethical and potentially illegal. The costs of control and treat. cruel methods of catching such to animal protection commonly states that as those using metal tongs and uncovered wire the responsibility to ensure a reasonable nooses. and mals. it is also likely to be rejected The welfare of an individual animal relates to by local citizens. priority for authorities.5 million dogs and In the case of dog population manage- cats euthanized (Scarlett. injury. injuries on the situation. if this animal is being kept in wastage of life. As such mane methods of killing such as strychnine the welfare of domestic animals is clearly a poisoning. . control (see Section 4). people have artificially selected for abusive treatment from people. however the problems Measuring these will provide an assess- encountered by dogs are also important and ment of an animal’s welfare on a scale from can make up a significant proportion of the dog- ‘very good’. dog owners have a moral (and some- considered as unacceptable to US society and times legal) imperative to ensure their dog as a result significant investment is made in experiences a reasonable level of welfare. • Freedom to express normal behaviours. these should be conducted humanely to minimize any potential suffering for the dogs involved. where all freedoms are achieved. the (wild or domesticated). with any animal potential animal suffering is minimized. mentally (adapted from Broom. Attempts to certain traits to suit human requirements. and disease. to suit the location. Instead. ers in dog population management are the lation management is that this initial step dog owners themselves. in particular in situa. nor seek. to dog population management through The cost of dog population management dog licensing systems (see further discus- can be significant and is not a short-term sion in ‘Understanding Dog Populations and challenge but a permanent requirement. Who is responsible for dog population management? Understanding Dog Populations and Implications for Management As stated in the ICAM Coalition humane dog population management guidance (2008). Suitability to local conditions responsibility for dog population management properly resides with local or Dog populations in each location will vary in central government. that distresses people? Is it NGOs (non-governmental organiza- simply that there is a perception of too many tions) can. In has a very important role in population reality there is no single method of popula. below). will also vary. themselves to a certain extent. more than double become overwhelmed. and capacity. as problems caused by dogs are concurrently reduced. of understanding the situation objectively dog owners can manage dog populations is not attempted. In the United Kingdom. experience welfare problems themselves. Animal welfare NGOs important ways that affect how they should should not be encouraged. dog population management. problems encountered by dogs. Hiby Summary there will always be a population of dogs that require management. and re-homing stray dogs as total- Owner-mediated control of populations can ling nearly £100 million. This cost of dog management is ulations may become necessary. and a management programme can be designed low-cost veterinary services. dog population management other than ceived problems that dogs present to society through a contractual agreement. as it Implications for Management’. to take best be managed. tion management that is guaranteed to work Dog owners can also contribute financially in all locations. and contribute mane control? Once the problems caused by to an overall management strategy by pro- and encountered by dogs are identified. on the not least the veterinary profession (which assumption that it will work anywhere. the estimated societal cost of dogs including tions of dense human populations. a style of popula. such as education. and hence stake in running and financing dog population . however. including their function on the authority’s overall responsibility for and human attitudes towards dogs. such as rabies. Dogs provide many benefits to society but the RSPCA (2010) estimated the annual cost they can also cause problems to humans and of enforcing dog welfare laws and kennelling. reuniting. and road traf- additional interventions to help manage pop. The per. Is there a zoonotic disease. When man. require the support of certain professions. management) to do this well and humanely. Perhaps the most important stakehold- A common mistake made in dog popu. As discussed above. but they will tion management that has worked in a dif. rehoming. ferent location is simply imported. the viding specific services most suited to their causes of these problems can be explored. livestock predation. and hence dog bites.182 E. considerable and it is essential that interven- agement is needed it is ethically appropriate tions to manage populations are designed that this is done humanely to minimize the carefully to ensure the best use of funds. support governments dogs on the streets? Is the major concern the in the development of suitable strategies for poor welfare of dogs resulting from inhu. with appropriate funding and resources. can be assumed that a proportion of people Although governments hold the majority will always choose to own dogs. fic accidents. leading to . problems experienced by the community confined. and ‘Interpretation of Data’. many other stakeholders should incidence of rabies. Once the priority dogs. the priority people and livestock has been identified problem has been identified as an over- as a priority for a certain town. these dogs be accessed for vaccination? • Academic communities with relevant experience. or are unowned dogs breeding suc- problems have been identified. º Why are these dogs not vaccinated against rabies? Do people not understand the • NGO community. caused by dogs’. whelming number of dogs being aban- tion is what causes this unacceptably high doned by owners to shelters. fostering. The following are just some of committee can be created to assess the situa. To encourage the participation will focus the future management pro- of relevant stakeholders. • Veterinary community. other places? • Educators. vet. pitals and health centres equipped to • Local community leaders/representatives. sociology. each problem cessfully in this city and producing the needs to be explored to understand its causes. next generation of roaming dogs? essentially asking the question ‘why does this problem exist?’ º What are the main welfare issues faced by these dogs? What diseases and inju- The following are examples of identified ries are they suffering from? problems and questions that could be used to explore their causes: º Are there particular areas of the city where these problems are worse? • The problem of rabies transmission to • For a particular region. Dog Population Management 183 management. Possible questions to identify the cause or source of the roaming dogs include: The first step for an assessment that will lead to designing a dog population management º What is the current size of the dog popu- lation and the categories within it? This programme is to establish the dog-related includes both owned and unowned. • Local media. º Are there any other reservoir species for rabies? erinary science. e. This is where the benefits º Where are the roaming dogs coming from? What are the sources of these dogs of a multi-stakeholder committee begin. above.g. and epidemiology. below). and roaming dogs. as and why do these sources exist? Are each stakeholder will provide a different per- these owned roaming dogs or abandoned spective on these problems. These stakeholders rabies cases? Is surveillance of animal and may include (ICAM Coalition 2008): human rabies cases sufficient to provide a meaningful picture of rabies incidence? • Government. The ques. provide the correct treatment? • Local community. design and implement an appropriate º Are there particular categories of dogs management programme. animal behaviour. the questions that need to be answered: tion. and evaluate it to that are over-represented in the dog improve performance. º Is the virus circulating within the cur- rent location or is it being imported from • Legislators. ecology. º Do people know what to do if they are exposed to rabies? Are certain people • International bodies with relevant more at risk of being bitten? Are the hos- responsibilities. including both dog • The problems of road traffic accidents owners and non-owners. Finding the causes be involved. and where in the location in question (see ‘Problems these overlap. a multi-stakeholder gramme. and rehom- cines accessible at a reasonable cost? Can ing community. caused by roaming dogs and the suf- fering of injured or diseased roaming dogs have been identified as priorities Exploring the ‘problem’ and its ‘causes’ for a city. importance of vaccination? Are there vac- • Animal sheltering. as opposed to fol- awareness of suitability to the current loca- lowing a strict script of predefined questions. to respond and discuss the subject matter lation and human attitudes and behaviours openly and honestly with the interviewer. views is to explore the subject area from a range of different perspectives. Cairo with a maximum upward bound of ters? Did their expectation of dog owner. and socio-economic groups may not be suitable. mate or monitor the number of roaming dogs over the phone. Questions or even official statistics can vary wildly. Surveys can also provide infor- ters? Why do people choose to adopt mation on the welfare status of these dogs.184 E. by and why would they choose a different using basic measures such as body and skin source for acquiring a new dog? condition. delivered by an interviewer in person. by º Where do most people get their dogs measures such as the percentage of lactating from? Adoption? Gifts from other peo. roaming dogs. or avoidance of poor welfare by estimates based on community perceptions culling large numbers of dogs. For each problem an additional ques- welfare. This was a signifi- ship turn out to be incorrect? Do many of cantly lower estimate than given previously these dogs have ‘behaviour problems’? by local media and authorities of 2 million º What is the rate of adoption from shel. in order to answer these key This may mean that a mixing of genders. Hiby overcrowding and hence poor animal of the number of roaming dogs is useful. Establishing a reliable estimate ‘shallow’ in comparison to that gathered . although they should all be repre- ‘Street’ surveys of dog populations sented across the groups.000.and time-efficient. but this must be done with develop as a conversation. tions. and include: are commonly overestimated. tion. related to dogs. to establish quan- in public areas at a particular time (available titative information. tion should be asked about what is currently being done. For example. to control the dog population. as welfare. learning from other locations of people and the questioning is allowed to can be very useful. The information is hence on the tools and resources page of the ICAM reliable and repeatable but can be considered Coalition site 2). questions: ages. and of reproductive activity. and population size over time.000 roaming dogs in owners? Is it because of unwanted lit. females. surveys breeders or pet shops? can be repeated at regular intervals to provide a measure of changes in reproductive activity. By selecting survey methods that are ple? Bred themselves? Purchased from reasonably cost. Street surveys of dog populations involve Questionnaires direct observation of roaming dogs on pub- lic property following a clear protocol to Questionnaires tend to use structured ques- ensure repeatability. º What age and type of dogs are being a population survey of Cairo completed for abandoned by owners? Puppies or adult WSPA by Conservation Research Ltd in 2006 dogs? Certain breeds or types of dogs? (unpublished data) provided an estimate º Why are dogs being abandoned by their of approximately 25. taking heed of the points discussed ear- The aim of focus groups and informal inter- lier under ‘Suitability to local conditions’. or online. Similarly. both informally and officially. so it is impor- tant to ensure that a good representation of Methods for investigating key questions the public is included. It is important to Focus groups/informal interviews learn from current and past control measures Interviews can be defined as ‘informal’ when to establish what has worked and what has open-ended questions are asked to a group failed. These surveys can esti. The composition of the groups should be carefully considered There are several different methods or tools to ensure everyone feels relaxed and able that can be used to investigate the dog popu. approximately 50. of the 47 wards in the CMC). Finally. complaints from the public about nuisance • age (split into puppies below 4 months behaviours of roaming dogs and the poor old. carried out in a sample of eight wards (17% mation is required. The questions themselves may • to establish the true vaccination coverage be either closed or open-ended and hence allow of the dog population. tionnaire of dog owners and non-owners. studies • to begin to understand the dynamics of Knowledge attitude and practice (KAP) studies the population. with responses to statements relating to dogs Colombo is the capital city of Sri Lanka and (including sterilization and killing) recorded until 2006 controlled its dog population by on Likert scales from ‘strongly agree’ to catching roaming dogs in response to public ‘strongly disagree’. however. It is com. and killing them in the munici- condition of any and all owned dogs cur- pal pound. For example. roaming dogs in the early morning (peak time mon to start with focus groups and informal for roaming dogs in Colombo). and a total of 1823 households of households that own a dog. and the gen. a questionnaire practices as reflected by their actions relating was designed to cover subjects such as the to the subject. and and attitudes in Colombo. The aim was: interview is a good way to explore why peo- ple choose to own a dog and why they may • to estimate the size and composition choose a male dog over a female. the Blue Paw Trust. the body and skin complaints. • to learn which dogs were not being these questions are designed to be focused on vaccinated. and (ii) a ques- interviews to gather in-depth information. elements: (i) a direct observation survey of and . a question. an initial assessment of the situation all dogs seen on public property and not cur- was completed in mid-2007 by WSPA and rently under the control of an owner. usually by inhalation of exhaust rently visible in the household were recorded. a focus group or informal the survey. and • gender. the following information was a management programme for the city. • if female. for a greater depth of information. and then to design a questionnaire if there are Both the survey and questionnaire were particular areas for which quantitative infor. The direct observation dog population. and adults). (8% of households from the sample wards) in der of these dogs. welfare of some roaming dogs. to design dog observed. The recorded: priority problems identified were a persist- ent level of dog and human rabies cases. number of dogs owned by each household. and the number and fate of dogs that had Example: Colombo initial assessment left the household over the last 12 months. fumes. involving the naire is a good way to establish the number direct observation of 625 roaming dogs. of the entire dog population in the city (both roaming and confined dogs). their attitudes towards this a better understanding of dog ownership subject including any preconceived ideas. In collaboration with the survey and count of roaming dogs included CMC. small groups. Dog Population Management 185 through focus groups and interview. For each a local NGO. 275 of dogs each household owns. whether lactating or not. the knowledge the person or group has about Following informal interviews to create a specific subject. are a form of questionnaire usually delivered • more specifically. • to investigate the welfare status of these Knowledge attitude and practice dogs. the proportion owned dogs. to learn what was main- via face-to-face interviews with individuals or taining the roaming dog population. The assessment consisted of two related • body condition score on a 5-point scale. The Colombo Municipal Council and the owner was asked whether these dogs (CMC) was motivated to find a more effec- were allowed to roam outside their property tive and more humane way of managing the in the early mornings. hospitals and schools) that members of the committee can be used could be targeted to change the dog pop- to answer questions such as: what do ulation in a localized way? . • Reproductive capacity of dogs The results of this assessment are dis. used to cluster the data into manageable sub- so this should be done with care. and shelter may be provided by an owner and then working systematically through the within a household or available on pub- key questions that were previously identified lic property. questions such as: are dog owners feed- ant on resources provided by people. The extent to which a dog as important for establishing the cause of the relies for survival on resources avail- problems. a multi-stakeholder committee can be regulations relating to this trade. this trade? It may be helpful to structure these inter- • Access to resources pretation discussions starting with a sum- mary of the data collected using each method. ‘supply should match demand’. below. it may also reduce the survival be common to all dog populations and can be of those that depend on these resources. These are factors likely to However. Restricting the discussion by working through a series of access to resources on public property important ‘factors’. human attitudes towards likely to be reliant on other food sources? dogs and their behaviour relating to What food sources exist in the local com- dog care and tolerance of roaming dogs. º Ideally the number and type of dogs that exist should match what is wanted and cussed in ‘Example: Colombo interpretation’. the relevant data able on public property will depend on can be highlighted and used to establish an whether it is owned. ing their dogs regularly. º Resources including food. water. or are they Consequently. leading to a population of unwanted dogs that may Interpretation of data be abandoned or killed.g. º As discussed previously. community where roaming dogs are not º The data collected plus input from tolerated (e. An alternative is to structure care provided by its owner. For each question. The there particular categories of dogs whose next stage is to interpret these data in order to puppies are most likely to be unwanted? answer the key questions and hence inform the design of the management programme. as interpretation will usually profit what is the welfare of dogs produced by from a range of perspectives. manageable by the local community. and the jects for discussion: impact on local populations should be • Human attitudes and behaviour relating monitored to ensure that animals are not to dogs starving as a result. and beneficial. and the level of agreed answer. munity? Are the dogs feeding on these is likely to be the most powerful force resources reliant on them for survival? behind dog population dynamics and Are there particular areas in the local the welfare of dogs. º Is there commercial breeding and selling in this location? What are the standards/ Again.186 E. Hiby • the presence or absence of a visible skin people think about dogs in this location? condition (this was the same scoring How do they treat dogs? Do they provide system as used for owned dogs in the care to their own dogs? questionnaire). º Data and committee input can be used Principles to answer questions such as: are there particular categories of dogs that seem Utilizing methods for investigating the dog to be reproducing most successfully? Are population can create a large body of data. the survival º Data and committee input can address and reproductive success of dogs is reli. management guide. such as those identified in will discourage opportunistic roaming the ICAM Coalition humane dog population and scavenging of owned and fed dogs. But this is commonly not the case. public health. In many situations this them. abandonment of unwanted shelter? dogs (perhaps particularly female dogs and . and if confirmed this impression that the percent- not. The questionnaire results using these preventative measures. around 50% programme should take to prevent trans. why? sustained entirely by survival of pups born What is their welfare state? How do local on the street. particularly for local and what has failed? What can we learn from and central governments. the following interpretations Leishmaniasis and Echinococcus may of the dog population were drawn from the also be relevant. depend on the human community and suggesting that much of the pup production the dog population itself. rabies control is often Using the results of the initial assessment a major motive for dog population introduced in ‘ ‘Street’ surveys of dog popu- management. vector repel. Dog Population Management 187 • Zoonotic diseases Finally. and dogs are Example: Colombo interpretation the most common vector for transmis- sion to humans. why not? Are there precautions that age of roaming dogs that are owned is low in staff working on the future management some areas. approached was to move away. and what are the some areas many of the roaming dogs trends in their incidence? Are particular encountered appeared to be unowned. de-worming. above. In conclusion. mission of zoonoses? Owners reported that 25% of the owned dog • Current roaming dog population population was allowed to roam unsuper- º This population can lead to human– vised. suggest- there particular areas where density of ing that the roaming population cannot be roaming dogs is high. of roaming dogs are actually owned dogs. data for the CMC area of Colombo. Nearly three-quarters of all respond- animal conflicts in addition to zoonotic ents said that if they had a female dog that diseases. litters. data and committee input can be º Zoonotic diseases are often the pri. or more female dogs. dog population seems to be maintained by ple feel about them? Would they adopt a combination of breeding on the streets by a roaming dog from the street or from a unowned dogs. º Data and committee input can address questions such as: what zoonotic diseases where are the roaming dogs coming from? in exist in this location. the roaming communities treat them? How do peo. there were and the welfare of the animals them. used to answer questions regarding the con- mary cause for concern with regard to trol measures used to date. Despite seeing 11% of the roaming tion size in the location. dog populations. which have a other locations? responsibility for public health. they would not want to keep welfare problems. Because rabies is a fatal disease. The best method of doing so will reported by the dog-owning households. and how is this females lactating. tion exist for these particular diseases and also the behaviour of most dogs when (vaccines. However. there was a low percent- split between different categories? Are age of pups (7%) seen on the street. tion scores over 1 or 2 (scored from 1 to 5). maintaining the unowned population may º Data and committee input can address be occurring outside the dog-owning house- questions such as: what are the sources holds. and if so. both categories of dogs over-represented in because of the lack of dogs with body condi- the case load? What methods of preven. actually a relatively low number of litters selves. rather than lent) and what is the availability of these to move into private property or attempt to methods in this location? Are dog owners defend a threshold. and can have visible animal had puppies. presumably with local people provid- of roaming dogs? Where do they come ing some support to unowned females with from? What is the roaming dog popula. a similar response was also given by population will need to be addressed for those respondents who in fact did own one reasons of public pressure. Other diseases such as lations’. What has worked. but also that overall. and more likely to suffer • To improve responsible dog ownership from skin conditions. Hiby their offspring). reflecting emaciated or • To reduce abandonment and the unsu- thin body condition) than for owned dogs pervised roaming of owned dogs. and owners allowing their need to remove them. only 83% in the previous year. 88% • To manage areas where roaming dogs were reported to be vaccinated. effective way. The essary. It would encourage people to take a fur- it is not acceptable to kill dogs. tion. injured. tant to them. dogs. • To increase rabies vaccination of unowned are particular categories of dogs over-represented dogs. with scores of 1 or 2. • To build on the current inclination to adopt. sive and humane programme would be nec- and 43% were only treated infrequently. (27% with scores of 1 or 2). lation would depend on how many roaming owners. and per. Initially this would be carried out through encouraging owners attitudes towards dogs and methods of to bring dogs for sterilization. This seemed to be from? a greater percentage of roaming particularly the case for male dogs. were the most likely to act as a reservoir One of the proposed elements was surgi- for rabies.8 ratio of females to males in as compared with owned dogs (17%). ther step and take responsibility for getting vides support for the need for an effective roaming dogs sterilized and caring for their and humane intervention that addresses the health. In addition. Body condition scores to increase care and hence improve the were slightly worse for roaming dogs (32% welfare of dogs. 78% of respondents believed that ple. with lation including both owned dogs where dogs belonging to people with a less positive puppies were not wanted. 77% of dog owners sug. cal sterilization of dogs. This suggested • To respond to sick. few people liked hav. commonly offered to these dogs by local peo- However. This would need activities to achieve responses to the ‘attitude’ questions sug. However. People were also will- dogs to roam. sive roaming dogs in a humane and haps also owned puppies prior to vaccina. the following: gested that the care provided to dogs was • To reduce reproduction in the dog popu- related to the attitude towards them. and aggres- that the unowned dog population. . in the rabies data? of the owned dogs. although are not well tolerated. dogs are brought for sterilization. The programme would explore ways of ing dogs around on their street and most building on the current level of concern for agreed that street dogs pose a danger to roaming dog welfare and feeding already people and should not be allowed to breed. hence also pro- ontrol the majority of respondents said c viding the opportunity to promote and sup- that the welfare of street dogs was impor. hence of management the interpretation of the data skin conditions in owned dogs may have suggested that to effectively manage the dog led to abandonment. There the owned dog population. This pro. and dewormed.188 E. ing to adopt roaming dogs with ‘adopted off street’ being the third most common source what welfare problems are the dogs suffering stated for owned dogs. and unowned attitude being less likely to be vaccinated dogs. even if they are currently considered source of roaming dogs and so avoids the unowned. and the gested they could handle dogs other than survival of pups born to unsterilized roaming their own. port responsible dog ownership practices. Only 29% of owned population for the long term a comprehen- dogs were never treated for ectoparasites. with dog owners seeming The impact of this on the roaming dog popu- to have a more positive attitude than non. was some suggestion from the informal interviews that people were concerned about from interpretation of data to proposed methods catching skin conditions from dogs. contrib- dogs (42%) suffered from skin conditions uting to the 1:1. Education messages and towards the dogs will lead to greater under. so an additional aim is to improve their behaviour in interactions A dog population management programme with dogs and reduce bite incidence. In knowledge of the impact of dogs in pub- this section a range of common components lic health. to reduce potential disease risks Development of a multi-stakeholder group to through owners investing in preventative complete this stage of investigation and inter. ment. • Animal Control Officers (ACOs). may have different titles according to their country and their responsibilities. and ownership. The aim in educating this realized that dog population management is audience is to build its knowledge and not a short-term challenge but a permanent engagement in dog population manage- requirement for society. breeding. ment by supporting the development of ponents will need to evolve over time. Target experienced by the dogs themselves and also audiences and the aim of education efforts perhaps most importantly why these problems will probably include the following: may exist. as it must be tion control. Children are commonly closely involved in dog care. enforcing dog-related regu- influential factor with regard to dog welfare. However. an influential component of dog popula- lation and how local people feel and behave tion management. Veterinarians are key pro- an understanding of the dog population and fessionals who should be engaged and the attitudes and behaviour of the local human involved in dog population manage- community towards dogs. based on • Veterinarians. and dog reproduc- consideration even at the outset. However. children are also commonly over-represented in Programme the dog-bite data. sible dog ownership to improve dog ment of the population will be more likely. with changes in dog population dynamics. The aim of educating dog ment programme will be significantly improved owners is primarily to increase respon- and hence successful and sustainable manage. mary source for information about dog plement each other are likely to be required to care by owners. humane methods of euthanasia. and where and how they live that education of people is similarly Taking the time to investigate the dog popu. lations. This profession is at the ‘front line’ of dog Education population management and usually responsible for responding to complaints Human behaviour towards dogs is such an about dogs. can be designed to suit the location. and implementation. From this position of greater under- standing. with the likely aim in using each. in providing disease prevention meas- tainability of each component will be a relevant ures. repro- to move to the next stage of programme design duction. The sus. ACOs and some examples from different countries. the audiences and developed and delivered with problems created by the dog population and support from education specialists. and hence one aim will be to improve their responsible Components of a Comprehensive ownership behaviour as described in Humane Dog Population Management the previous point. Dog Population Management 189 Summary survival. measures such as vaccination and para- pretation is likely to be very beneficial and this site control. these com. delivery need to be targeted towards specific standing of dog population dynamics. and have a clear role form a comprehensive programme. and rehoming. • Children. and talking to the public about . They are often considered the pri- A number of components or activities that com. is described. and attitudes towards dogs. the design of the population manage. welfare. • Dog owners. as discussed above. dog health care. and to improve approaches same group should be prepared and motivated to dog acquisition and retention. in step key skills such as surgical sterilization. For able. to recognize the contribution they can make and housing. food. management is a permanent challenge for ing or support. and technical train. would be forbidden . conscious animals. by legislation at both central government mal welfare or for their potentially influen. Example: ACO training. the Institute • Protection of animals from cruelty. professionals such as vets. In recog. in this chapter can be used as inspira- cal skills and knowledge of subjects such as tion. It is not at local government level to allow variation uncommon for the behaviour of these staff in management styles according to the loca- towards animals and the public to be a source tion. The sible for animals have a ‘duty of care’ to ACOs from several Zoonosis Control Centres maintain a reasonable level of welfare. ACOs represent an unde- veloped profession and the staff employed to As previously discussed. which cause signifi- • commencement of sterilization services cant suffering. municate responsibly and accurately as opposed to catching roaming dogs with the public about its responsibilities. and Control Centres have been: authorities responsible for animal control can also be included to protect animals • a change from inhumane methods of from cruelty. activities. and physical methods. to reduce numbers of roaming dogs. and protec- aim is to change the behaviour of the ACOs tion from pain. so their handling techniques society and so should be well supported and attitudes commonly lack respect for ani. Hence the use of poisons culling to humane methods. Observed impacts at the Zoonosis owners. at the centres. and dis- towards animals and the public. in New Zealand the Dog Code 3 been provided with training and empowered provides both minimum requirements to have respect for themselves and what they and also best practice guidelines for can offer to the public health and to animal dog care.190 E. including dogs. as opposed to – at ferent species. includes legal obligations towards animals. dog population fulfil these roles have had minimal prior train. The strength of this course is The Five Freedoms introduced earlier that it not only provides training in techni. and empowers the ACOs to provide a suitable environment. such as strychnine. including dog care. Methods of killing animals by welfare. ing sessions. Brazil Legislation In many countries. to become champions for animal welfare and additional ‘codes’ can be written for dif- humane zoonosis control. the care necessary to meet their needs. In addition to this legal framework. level to maintain minimum standards. Legislation should aim to cover several of public complaints and animosity. allowing the animal to to animal welfare and human health. The UK Animal Welfare Act 2006. suffering. and tial position in the local community. The impact owners with more information and guid- of the course on each ACO can be consider. and the knowledge and skills they need to • a reduction in catching of dogs due to an humanely handle and care for animals increase in the use of owner education they become responsible for. areas: nition of this challenge in Brazil. The exhibit normal behaviours. injury. Animal of Education and Population Management owners and people temporarily respon- (ITEC) developed a course for ACOs. ance as to what suitable care entails. as this may be the first time they have example. and for them ease. such as drowning and electrocution of • improved welfare of impounded animals. to provide times – a source of animal cruelty. The aim in education • an increase in adoption of dogs from the of this audience is to equip ACOs with centre. zoonosis control. Hiby its responsibilities. are brought together for 1 week for a series by ensuring animals are provided with of lectures. but also addresses attitudes for example. and to com. without speaking to owners. Some annually. ship will become unaffordable for low- trol and in particular during ‘outbreak’ income people who may well rely on situations. suitably skilled staff to fulfil designated • The fee for licensing a dog and pen- roles. The requirements for º encouraging an annual check of regis- local authorities to provide dog popu. Commercial breeders and sellers should nite dogs with their owners should they be subject to regulations that ensure the become lost. the payment of an additional fee. national welfare of the animals involved is pro- databases should be used and linkages tected. Too high. aspects of legislation. and reduce the incidence collared and tagged). Regulations relating to the protection of ing owner information such as change of animals will also be relevant and there address or ownership is fast (preferably will be additional care requirements for . also essential that the process of updat. to ensure information can also stipulate reasons why animals remains up-to-date. if relevant. Benefits of licensing include: countries have chosen to introduce legis. Registration dog population management activities. and that the data are should be killed. identification. Licensing of dogs involves have a responsibility to treat or eutha. and people will be discour- licensing. This should include a minimum between national databases built for ani. This may also include additional be forced to abandon dogs. and owners will tion. While this should be the long. tration details to help keep information lation management capacity. population have not yet been developed º differential licensing fees to encourage is likely to lead to significant animal responsible behaviour such as neutering suffering in shelters and on streets. usually nize their animal if it is suffering. This section completed online). and relate to both ing dogs. leaving no additional funds for licensed and any fees paid. are not visible but owners may help improve responsible ownership. The impact of this provides a basis for enforcement of other scheme is yet to be established. Identification and • Control of the supply of dogs. These may be included with aged from adopting or caring for roam- dog control laws. also be required to ensure their dogs are animal welfare. Too low. and livestock. as part method of identification: microchips. age at breeding. Hence this both of behaviour problems that commonly encourages responsible behaviour and lead to abandonment. It is ing. sometimes visibly (dependent on the and basic training for all dogs. for of the requirements for dog licensing to example. frequency of breed- mals that move between countries. or the cost of ensure dogs are identified. for example owners accessible. including updated. registration also provide a fast way to reu. income owners. and or adoption of dogs and allowing free considerable cost to society in housing licensing for assistance dogs and low- dogs and treating zoonotic diseases. º an income that can be used to support dog lation that forbids the killing of healthy population management programmes dogs. with care. and infrastructure such as holding alty for failure to license needs to be set facilities. With this in mind. introducing such putting the cost of dog population man- legislation when humane and effective agement primarily on dog owners rather methods of reducing the unwanted dog than the general public. registered on running the licensing system will not be an accessible register. legally and pulsory training course for dog owners. their dogs for security or for protecting • Dog registration. dog owner- regulations relating to zoonotic con. should be covered in this sec. and • Dog control laws. and maximum number of litters. and. covered. Dog Population Management 191 in this section of the law. and dog owners may owner and authority responsibility to see licensing as irrelevant. following the ‘polluter pays’ principle by term goal of society. and identification provide a link between Switzerland has also adopted a com- an owner and their dog. and effective and for dogs. no methods of chemical or immunological sterilization or con- The aim of reproduction control is to help traception are guaranteed to be effective reduce the unwanted dog population by or without risk when used on roaming. Effective enactment will usually tive organs under general anaesthetic require the majority of effort to be spent on ensures permanent sterilization and can education and incentives and the minority to significantly reduce sexual behaviour be spent on carrying out punitive enforcement (especially if performed early in an ani- measures. such as the ganging of males around expected in the near future. this is an match the supply of dogs with the demand active area of research. (also referred to as animal welfare inspectors but is a lifelong solution. tus of females). These officials are trained and may be more cost-efficient over time. copy of the Dog Code if one exists in the There are three main ways that repro- country. the fact that they may need to be repeated. and administration of injections at regu- trol will need to be sustainable and affordable.192 E. an infra- mals when required. An additional aim may be to reduce suitable chemical or immunological ster- sexual behaviours that are perceived to be a ilants for mass reproductive control are nuisance. These methods are still limited by the cost. be assessed by adequate post-operative Successful enforcement has been achieved monitoring during the whole recovery in some countries through the use of ACOs period. or contraception. warnings. including a minimum from investing in local veterinary services and age for people purchasing animals and matching these with a dog-owning community a requirement to provide information that values veterinary care. Ensuring good dog welfare also involves should also be regulated to ensure pro. This can only and dog owners. which hence every effort should be made to develop is not possible for most dog-management these services locally with the local veterinary programmes. lar intervals without interruption. Chemical or immunologi- capacity. and enforce legislation structure. 2008). In the tection of animal welfare and responsible long term. and even- • Chemical or immunological sterilization tual prosecutions (ICAM Coalition. and to encourage owners to perceive cal sterilants and contraception should . through advice. from law enforcement of asepsis (the practice of reducing or bodies (such as lawyers. police and animal eliminating the risk of bacterial contami- welfare inspectors) to relevant professionals nation) and pain management must be (such as veterinarians and shelter managers) maintained throughout. limiting unwanted reproduction in order to unmonitored dogs. and equipment. Hiby pregnant females. prior to the application ices provided to help with reproduction con. and hence or wardens). cautions. Education about legislation has to mal’s development). duction control can be achieved (ICAM Coalition. The removal of reproduc- effectively. Most steri- a female dog in ‘heat’ leading to fighting lants or contraceptives require trained between the males. for example a not assume it should be a free service. or to reduce the increased veterinarians for clinical examination disease risk to dogs presented by mating such (especially to assess the reproductive sta- as transmissible venereal tumours. Any serv. It resourced to provide education. the dog population will benefit selling practices. and by the welfare problems associated with certain chemi- Reproduction control cals. Currently. 2008): Legislation will be a ‘paper exercise’ unless it is enacted uniformly and enforced • Surgical. and these as valuable services that they should pay young puppies. handle ani- requires trained veterinarians. However. Pet shops and markets for. additional ongoing health care needs. and which does relating to animal care. nursing mothers. A good standard be targeted at all levels. Surgery may be costly initially. They may or may not have and emigration: an impact on sexual behaviours. and can plan to ensure the female per year) is isolated from entire males during this L = average number of females per litter period. Staff should also perform consist- ent follow-up of cases in order to help iden. However. If there is sterilization of females. the percentage that this equation assumes a closed population needs to be sterilized can be limited. chemi. on the population rate can be surprisingly dif- lar sub-population of dogs expected to pro. Attention must be paid to the wel. If the prob. So an additional duce offspring that will not be vaccinated. or fecundity of reduce costs. Note that or sources of the problem. the complexity of dog population dynamics. If the problem misses a particular sub-population the impact is poor rabies control and there is a particu. • Physical contraception through the iso. and roaming dogs. but high owned by low-income owners who are less for this particular type of dog. juvenile survival. Sexual behaviour can If there is no sterilization of females the become problematic. which are very likely to be the limiting factor lem is abandonment of unwanted females for population growth (sterilizing a percentage and their litters at shelters. important factor is targeting of particular sub- the proportion of the total population that populations of dogs. the proportion of the sterilizing the same percentage of males). the following is a useful guide ing sterilization services towards those dogs to establish the required sterilization propor. our experience population should be sterilized?’ Earlier in is that this equation is too simple and belies this chapter. r = AdultSurv + JuvSurv F L (1 − Sterile) cal. the statement needs to include a factor that The managers of a programme that accounts for the fact that part of the popula- includes sterilization should ensure that good tion cannot reproduce: standards are maintained. people rarely know the adult numbers of dogs being sterilized per day can survival. This will require Hence the proportion that needs to be prior training of staff and regular refresher sterilized for a desired r is: training. the importance of understand. By effectively target- population. dogs total population may again be low. In addition. Where lation of females in oestrus from entire AdultSurv = adult survival males. High throughput interventions with large However. ing the problem and causes was discussed. ferent from the one expected. However. that have been identified as important causes tion for a desired rate of change. or immunological). as males will try to rate of population growth is: gain access to females. but a weakening of standards their population before they begin (WSPA must not be allowed. If the intervention on the aim of the programme. Owners can be educated to recog. have tended to estimate these parameters A common question posed if this compo. JuvSurv = juvenile (first year) survival nize the signs of a female dog coming into F = fecundity (number of litters per female oestrus. in particular from of females will usually have more impact than a certain type of dog. should be sterilized may be low. Sterile = proportion of sterilized females fare of both the female and males when r = rate of population growth this is planned. Dog Population Management 193 be used according to manufacturers’ by not including the factors of immigration instructions. from the data produced by programmes once nent is to be used is: ‘What proportion of the they have begun). . regardless of the mode of sterilization used (surgical. and the differing survival and fecundity of the so the answer to this question will depend various sub-populations. isolation requires minimal cost to achieve and does r = AdultSurv + JuvSurv F L not require a trained veterinary surgeon. for example female dogs. if likely to be able to afford to keep an unplanned the goal is to stabilize or reduce the total dog litter. Sterile = 1 − [(r − AdultSurv) / (JuvSurv F L)] tify problems and raise/maintain standards. the mode of In other locations owners can be encour- sterilization (and rabies vaccination) deliv- aged to bring their dogs for sterilization at ery differs.194 E. below). but the sense of responsibility tional help from expert dog-handling teams towards individual dogs is apparently when required. recovery. At the risk of generalizing for a delivery of these services was increased country that includes significant varia- through local animal health provider clinics. Later in the programme the low. Note that willing or able to bring dogs themselves. neuter. central-point vacci- can be considered along a spectrum with the nation proved effective for rabies control. sleeps on the door- sent. the dog could lead to problems of lack of owner con- plays with the children. Catch. initially through a mobile clinic to which ing for roaming dogs by a sympathetic dog owners brought their dogs. roaming dogs are owned. the Department study to date. and may even have a bility for vaccination and sterilization with name – but the dog is not considered the the intervention staff and not the owners. and additional help from there is a predominance of the use of catch. Due to the high proportion of a central point (which can be moved if using effectively unowned roaming dogs in India a mobile clinic). vaccinated. relying on central-point delivery and will not be brought to a central point without establishing whether people are for sterilization or vaccination. and return’. 2009). Roaming dogs are to bring the dogs themselves (WHO and Bill caught by dog-handling teams. steriliz- strong sense of responsibility towards ing them. and potentially establishing responsi- step of the house. tion between locations. Hiby How to access dogs for sterilization dogs due to home burning of refuse. In some is re-homed or killed by owners instead locations roaming dogs can be caught on of abandoned. property nor responsibility of the family Similarly. minimal refuse available for scavenging Many CNR projects will also vaccinate and . Catch.. an example may Using capture of roaming dogs for delivery be a family who feeds a specific roaming of sterilization when the majority are owned dog with leftovers every day. neu- be offered for owners who would struggle ter. and return4 (CNR) essentially • In Tanzania there seems to be a relatively involves catching roaming animals. and kept unconfined. usually a breed-specific dog that is confined on private property. In Tanzania. ership status of roaming dogs. neu- Because of the differences in the own- ter. and returned to the original site of capture after hence the ownership status of roaming dogs. permanently marking them to show owned dogs. and they were caught. and return’. and return (CNR) (see ‘Catch. below. for more details). and return Hence the proportion of roaming dogs that are effectively unowned is high. will depend on the dog population dynam. As a result. there is very limited then returning them to the place from which purposeful feeding of roaming dogs. and released (see ‘Catch. with addi- public. The lized and vaccinated at a centre before being relationship between dogs and humans. as discussed earlier. dog handlers with suitable transport might neuter. neuter. after a period of recovery. Similarly. the majority of the street by dog-handling staff. following two countries exemplifying the as dogs are brought by owners for vaccina- opposite ends of this spectrum (although tion (Cleaveland et al. There is also some anecdotal evidence ics and human attitudes and behaviours that when a dog is no longer wanted it towards dogs. and is based only on the expe- of Livestock Development for Zanzibar and rience of WSPA): local organization ZALWEDA provided steri- lization and basic veterinary health care serv- • In India there is a high level of provision- ices. will the level of responsibility shown towards lead to low coverage of the dog population. although they are often they are sterilized (to avoid recapture). sterilized. a dog that is considered owned. and steri- and Melinda Gates Foundation. in a this has not been the subject of empirical programme run by WSPA. is significantly higher. 2003). a can include: neutering and vaccination programme that is based on community or owner participation • Reduction in zoonoses transmission. • Roaming dogs are a significant source of • Roaming populations can continue the next generation of roaming dogs. if the steriliza. If many of the roam- original territory reduces migration of ing dogs are in fact community or roam- other roaming animals into that area. their health by taking away the energy The following is a list of requirements costs of breeding. returned dogs will not be guaranteed. when some of the animals being caught other sources of roaming dogs and are actually roaming owned dogs. nificant reduction in population size. and animals. ion animals having responsible and car- bility. tive success of remaining animals. in to function as biological control of other words they are breeding success- rodents. increase responsible ownership. • There is an understanding that CNR will It is also important to be aware that CNR achieve stabilization for the short term may actually be counterproductive for build. also addressed for the long term. . CNR alone will not address the roaming dog • Local people want to maintain the local problem in the long term. indicates that the source of the roam- CNR can essentially lead to a stable and ing dogs is owned dogs. and reduces the risks that must be in place for CNR to be considered of injury and disease transmission of as an appropriate method for dog population breeding. and so these healthy population of dogs. Assessment of the location as • Sterilizing a roaming animal ensures that described earlier will help to identify if these it will no longer give birth to offspring requirements exist: that would be likely to suffer and die at a young age. but also the safety of the dogs. programme. If dogs on the street do not seem mon use as method of rat population to be able to raise a litter to maturity this management. should be the target for the neutering tion rate is maintained at a high enough level. working ing dogs that the immediate local community towards the ultimate goal of all compan- considers at least partially their responsi. The percentage of dogs that will need to be • The environment can support roam- sterilized will depend upon reproduction rate ing dogs in a good state of welfare. removing the animal allows vaccination programme should be carried migration and increased access to out using participation of local people resources which can improve reproduc- rather than catching dogs on the streets. with a programme that will address ship. In this situation the responsibility for ing owners. and education would be more effective in the • Sterilizing roaming animals can improve long term than CNR. traffic flow is slow or light. while there is an roaming dog population as part of their owned population that is not accessible to community. as described previously. and people the programme will not only be potentially providing a source of roaming difficult to run. Without such sup- stabilizes the current roaming population port. Dog Population Management 195 treat the animals for parasites at the time of neutering and vaccination should lie with sterilization. then the neutering and conversely. there are reliable food sources available. The benefits of such an approach the owners or community. or roam. For and survival in the particular population of example. the safety of returned dogs cannot while additional sources of roaming dogs are be guaranteed. Consequently. hence their relatively com- fully. and will be replaced in the long term ing a culture of responsible animal owner. Instead. However. • There is support from both local and it should be seen as a temporary method that national government. Without support from local the catching teams. management. Hence CNR alone may not lead to a sig. ing owned dogs. • The majority of the population of roaming • Returning a sterilized animal to its dogs are unowned. not being neutered. vet time. Benefits of dog . a programme fic are not suitable for CNR programmes. Cruelty and abuse was US$ 25 per dog.. so an analysis should reality that must be considered. the mass annual • Where the local community has intoler- or bi-annual dog rabies vaccination pro- ance. An important management. Although the have a right to a view on their local costs of sterilization are not insignificant environment. and to these treatments. so it is impor- roaming dogs. especially if disease elimina- constitute good animal welfare. This approach tion (Reece and Chawla. 2006) there are many may be more suitable for cat population important limitations on its use. the likely fate of returned ani- mals must be considered. Efforts should reduction in dog and human rabies cases be made to educate people about the across Latin America.196 E. as they may improve disease control. to provide preventative measures on a mass Releasing a dog into an environment and coordinated short-term scale may be where it is likely to be run down does not most effective. They eration of roaming dogs). as opposed to relying solely location in question: on surveillance and treatment of cases once they have already occurred. be completed of whether sterilization costs From the above discussion. positive consequences of a CNR pro- Combining sterilization with preventa- gramme. For example. If a zoonotic disease transmit- • Where the environment is unsuitable. sterilized. gramme. the opinions of local tive treatments such as rabies vaccination people should be considered.e. for example efforts should instead be focused on the rabies vaccinations in most rabies-endemic true source of roaming dogs. usually ideal. Setting up ongoing access catch and sterilize dogs that will later be through local veterinary infrastructures is killed is a waste of resources. These preventative measures usu- • Where there is indiscriminate killing of ally need regular application. and returned although this should be tested through an ini- becomes the responsibility of the CNR pro. To return a dog to this tant to consider the sustainability of access to situation places its welfare at risk. grammes run in nearly all Latin American and there may be strong religious and countries since the 1980s (Schneider et al. animal that is caught. Disease and parasite control The following lists examples of situa- tions where a CNR technique is not suitable. it is clear provide sufficient disease control benefits that CNR will only be suitable in a restricted to warrant the investment. ranging from US$ 10. animal welfare and human health benefits they are not the source of the next gen- through reduction in zoonotic diseases. Hiby Although CNR can be effective for number of situations and may not be suitable zoonotic disease control and population reduc. countries. It is also very impor- (the average full cost of surgical sterilization tant to consider how local people will including medicines. tion is the goal. however. and infrastruc- react towards roaming dogs once they ture costs for WSPA-funded projects in 2009 have been returned.30 towards roaming dogs is an unfortunate to US$ 52 per dog). The aim of pre- • When the roaming dog population is ventative veterinary measures is to provide found to reproduce unsuccessfully (i. The best form of disease and parasite control Assessment (as described earlier) will help in dogs is a programme of regular preventa- identify if any of these are relevant for the tive measures. ted by dogs is identified as the main prob- Large urban areas with fast-flowing traf- lem for a particular location. cultural reasons for negative views 2005) has led to a significant and widespread towards certain species. Sterilization are sometimes required by law. as roaming cats tend to match principle to consider is that the welfare of every the required criteria more closely than dogs. The return of the sterilized animal to the streets does not signal the end of this responsibility. Not all people like roaming dogs. across a whole nation or city. tial assessment. leading to increased ment of shelters). • a euthanasia policy that has protecting • Sterilization also can reduce reproduc. NGOs or private organizations. whose offspring are also likely to remain • clear limits on capacity. ideally including a injuries. especially important if using annual mass Whether run by government authori- vaccination campaigns (see Hampson ties. as they defined by the relevant legislation. a solution to population management. and their unowned dogs that might be difficult to transportation. • initial entrance to the holding centre. for example in the case of a dog that Removing dogs from the street has bitten someone and is suspected to be rabid. contribution to basic kennelling costs. 2009 for a discussion of the reduc- and housing dogs should be subject to agreed tion in population level immunity in dog standards that ensure an acceptable level of populations with high turnover). the alternatives are to remove dogs additional rehoming services. While private organizations may achieve this lowing (WHO and Bill and Melinda Gates through significant investment of time and Foundation. mum period of time to allow the owner to be tion is not suitable for managing roaming found (often a 2-week period). º Improving health and reducing prob. Dog Population Management 197 sterilization to disease control. • assessment of dogs prior to rehoming. are not limited to: • Sterilization can help to maintain herd immunity by reducing the number of • techniques for catching dogs. but inevi- gain more benefit for effort of bring- tably additional protocols will be required to ing their dogs to an intervention. with rabies level of animal welfare is to be maintained. and including quarantine. authorities can provide CNR.. and unowned. hence reducing abandonment. and closing such facilities is cult and expensive to achieve if a reasonable extremely difficult. reuniting with their owners. law to provide the capacity to hold dogs for a limited period of time for disease surveil- lance. and RSPCA (2006) for fur- oestrus can cause increased movement of ther discussion of protocols and manage- individual animals.5 for further discussion risk of contracting rabies. meeting frequency between dogs and Local authorities may be required by often fighting between males. hence guarantee practices used by all staff ensure the percentage of vaccinated dogs can the correct care is given. or euthanasia if rehoming is not possible. The cost ing. of running a rehoming centre should not be Keeping dogs in sanctuaries for life is diffi. but increase. or they may from the public places for euthanasia if they contract out this aspect to non-governmental are suffering from untreatable diseases or or private organizations. In some coun- • Offering sterilization and basic treatments tries the care that should be provided will be can increase owners’ compliance. º Reducing the production of unwanted • standard veterinary treatment for all offspring that may otherwise have been dogs including sterilization. lem behaviours of individual dogs. 2009): funds. such sanctuaries are unlikely to con- tribute significantly to the wider population • Sterilization reduces population turnover management goals and should not be seen as and so helps maintain herd immunity. These include. rehom. catching et al. for example by using basic requirement. animal welfare is maintained. underestimated. by: per vehicle. include the fol. animal welfare as its core principle (see tive behaviours that put dogs at higher ICAM Coalition. Beyond this dog populations in situ. Females in of euthanasia. including limits on number access for vaccination. or to hold a roaming dog for a mini- When initial assessment reveals that a loca. abandoned. control particularly in mind. • assessment of the suitability of potential º Reducing reproduction of unowned dogs homes and matching dogs. Hence before commitment . When running holding facilities. rehoming centres ning costs for at least 1 year as capital. demand led to a dramatic fall in standards of nasia will be required for animals that are care. eutha. components In some cases. vaccinations.198 E. paying for all medi- only occasions when euthanasia is required. rehom.6 cessful population-management programme For its part. and sustainable euthanized after capture due to welfare prob- programme: lems. temporarily. until and all healthy animals can be found a good long-term homes were found. 2008. it is advisable to An example of fostering as an alternative to hold sufficient funds for building and run. The new without suffering (ICAM Coalition. community dogs across the Colombo come is good should not necessarily be seen Municipal Council area. In reality. cal bills. Removing dogs from public areas may be necessary in many countries where roam. ing. a or behavioural problem that prevents them new organization focused on creating a fos- being rehomed. An example of fos. organization has become a success in a city WSPA. or when their humane dog population management welfare on the streets is unlikely to be good. injury. 2007). Ideally dogs should never become ing dogs in an area immediately around roaming nor unwanted. of animals than a shelter ever could. leading interpretation completed for Colombo. Hiby to such a facility is made. and neutering. or simply because there are not enough • Mass vaccination of both owned and homes. Example: Colombo comprehensive and ing dogs are not tolerated. humane. and distress for the staff. or which are not coping well ter network of dedicated volunteers to take enough with the facilities to maintain a rea. and limited better for animal welfare. a suc. Rabies outbreak as a solution to dog population management response including vaccination of roam- problems. these dogs are reunited with Following on from the assessment and data their owners or rehomed quickly. the to a positive outcome for animal welfare. where many similar projects have failed. fundraising capacity. following components were selected for the However. est human population densities in the world. behaviour problems preventing rehom- ing. In many instances. or fostering networks. Removing dogs even when the out. resulting in significant animal suffering suffering from an incurable illness. and involving maximum also addresses the source of roaming and community involvement in bringing dogs unwanted dogs. the organization agreed to should create a situation where these are the support the animals. most countries the organization built up a network of more will not be able to achieve this situation than 40 foster homes with the goal of reach- immediately but will need to work towards ing 100 within the 2nd year. many shelters quickly tering is given later in this chapter. and to have agreed a clear plan for sustainability. • Targeted sterilization of both owned but instead be part of a comprehensive and community dogs with a focus on approach to population management which female dogs. must not be relied upon as the sole response. The animals are it. it must employ mals are all homed in appropriate conditions. accepting that some healthy animals will rehomed via the internet and the network has be euthanized as not enough homes exist the potential to house a far greater number that can provide a good level of welfare. humane methods that ensure the animal and the scheme has far lower overheads and moves into unconsciousness and then death administrative costs than a shelter. unfortunately many animals are comprehensive. however. In the 1st year home. abandoned dogs and cats into their homes sonable level of welfare. In an East Asian city with one of the great- An alternative to rehoming centres is foster. for sterilization and post-operative . As an alternative. so removal of dogs any suspected cases. became overwhelmed. which may be more cost-effective and a large population of stray dogs. lack of financial resources and constant ing centres. The ani- Whenever euthanasia is used. Ultimately. by high- this process. In its simplest form a hierarchy of selected and combined to create a comprehen- objectives will include: sive and humane population management programme. Evaluation is a periodic to reduce potential conflict with people. These are areas set up on private selves. deliv- monitoring and evaluation involve the meas- ering responsible ownership messages urement of indicators that are chosen because and bite prevention to communities. Chapter 7. usu- in their responsibilities and the aims of ally focused on activities that aim to check pro- the DMZ. and allow for practices and feeding stations are set up regular adjustments. Prior assessment number of roaming dogs. encouraging a sense of responsi. through treatment following ways: for skin conditions) and safe (through rabies vaccination) helps to accelerate • Help to improve performance. bite prevention. invest- the community are aimed at moving ment in monitoring and evaluating its impact dogs along a continuum from unowned is surprisingly low. Community dogs are those with to ensure the programme continues to evolve no single referral household or person. Many involve direct interaction • Desired impacts. Dog Population Management 199 care. usually carried out at particular • Training of municipal staff in relevant intervals or ‘milestones’ to check the programme skills including humane dog handling. Both recognizing dog behavioural signs. are recruited by the team to provide post-operative care to the community dogs. The efforts to involve ulation management across the world. Monitoring and Evaluation bility over them. compare lives. schools. In collaboration with the owners of the success of strategies used in different these premises the dogs are sterilized and locations and situations. what is proving effective and lessons learnt. to demonstrate that the pro- premises such as hospitals. lighting both problems and successful • Education of children and adults in elements of interventions. is having the desired and stated impact. rabies awareness. and army bases where a population of dogs • If methods are standardized. These are the visible with dogs. tion in number of healthy dogs eutha- ing and evaluation will provide a measure of nized in shelters. Making dogs tion should provide significant benefits in the more attractive (e.g. 2009. assessment. Monitoring and evalua- to responsible-owned. and they are quantifiable ways of reflecting the surgical neutering. vaccinated. using two veterinary mobile clin. . and • Provide accountability to those that responsible dog ownership. and gramme is achieving its aims. ics. reduction in of the location will help determine which dog and human rabies cases. staff and public are educated Monitoring is a continuous process. and good garbage-management gramme progress against targets. and protocols should be developed changes that the stakeholders would like that ensure practices are humane and also to see and may include a reduction in the protect the safety of staff. and improve over time. members of the community the next section. Planning of dog population manage- Summary ment programmes to include a ‘hierarchy of objectives’ with indicators of success at each level will support effective monitoring and There are many components that can be evaluation. and monitor. This is discussed in however.7). stated objectives of the programme (adapted from OIE. or reduc- components are most suitable. as well as ensuring the dogs have oversight during the post- Despite considerable investment in dog pop- operative period. invest in the programme whether they • Development of dog managed zones are authorities or the dog owners them- (DMZs). ing and evaluation will depend on the objec- and improved knowledge. population. particular those dogs with low-income From these examples it becomes clear owners living in a specified location). property. what the pro- including: gramme actually does daily to achieve the objectives. indicators • Indicators for the size of the owned dog are selected that can directly measure any population and its overlap with the roam- change in the stated objective. number of dogs sterilized through a • Indicators of dog care measured through low-cost sterilization project subsidized vaccination coverage and percentage of .m. or as a method of measurement is therefore the ratio of dogs to humans. there are some indi- • Activities that will achieve each stated cators that are likely to be common to most objective. measured by asking of measuring the indicator is similarly stated. For each level of the hierarchy. direct observation survey. and incidence of injuries such as tant component of the programme. or the number of dogs col- º provision of a mobile clinic for areas lected from public property by authori- where there is no accessible veterinary ties. through direct animal-based measures • At the activity level. will contrib. direct observation surveys of dogs on º a school education programme in public property would reflect the repro- bite prevention and responsible dog ductive activity of the roaming dog ownership. that the indicators to be used for monitor- increase in rabies vaccination coverage. an indicator could be the number of lead to indicators for the total dog popu- roaming dogs visible on public property lation size. by the programme in collaboration with ute to the desired impacts. donment of dogs at shelters or requested euthanasia at veterinary clinics. attitudes. population. º development of improved legislation • Indicators for the size of the unwanted and enforcement. their causes. and may include an increase submitted by participating veterinary in sterilization of the dog population (in clinics. These will be a local veterinary association would the effects of the programme that in com. and where they overlap will tion. These will be the efforts that dog population management programmes.m. For example: • Combining indicators about the size of • At the impact level. These may include: • Indicators of the size of the roaming dog º a training programme for local vets population measured through direct in low-cost but high-asepsis surgical observation surveys of dogs on public sterilization. if achieved. The location. and a method ing dog population. skin con- tion control was selected as an impor. including regulation of dog population measured through aban- breeding and sale of dogs. and 8 a. the those caused by road traffic accidents. which will practices relating to dog care and dog- reflect the initially identified problems and bite prevention. a density per unit area. including body condition score. ditions. an º an annual rabies vaccination campaign additional indicator of the percentage with a particular focus on low-income of lactating females measured through areas. However. and tives selected for the programme. This can be reported as a total between 6 a. conducted • Indicators of dog welfare measured every 6 months. Hiby • Objectives that. If dog reproduc. If the desired impact the roaming dog population. common in the location in question. owned dog is a reduction in the roaming dog popula. the programme makes. dog owners about roaming behaviour. If roaming dog populations are service. in a selected number of dogs for a specifically defined sample of wards of a municipality. be the indicator.200 E. The method of meas- bination will help achieve the desired urement could be the monthly reports impacts. including gassing with of females. and is set to be main- hension and follow-up 6 months later in tained by local government from 2012 a sample of classrooms. the previous approach of regular dog ing individual dogs for body condition.1% in June 2010 (max- change experienced by beneficiaries. exhaust fumes. to assess knowl. This reduction see Davies and Dart (2005) for more suggests that reproduction in the roam- information). The indicators selected changes in disease. and ers and people who do not own dogs. This should also include also provide a level of accountability that is measures of surveillance efforts to demanded of both public funds and private ensure changes in incidence reflect actual donations to NGOs.2). onwards. including vaccination. and reported dog cases from 2008 onwards to well below bites from local and central government. 11. dogs seen on the streets during direct and ‘most significant change’ stories observation surveys has fallen from a (a method of collecting qualitative mean of 8% (maximum observed 21%) information in the form of stories of in June 2007 to 1. humans measured by monthly or annual although some common indicators are sug- rate of dog bites of humans treated by gested in this section to inspire programme health clinics/hospitals (often reflected managers to start monitoring and evaluating by uptake of post-exposure prophylaxis interesting indicators of success. including dog and most notably with a decline in dog rabies human rabies cases. • Qualitative measures such as collating • The percentage of lactating female testimonials from expert witnesses. impounding and elimination using inhu- skin condition. This alternative project • Questionnaire survey of both dog own. and not only efforts for each programme should reflect the objec- to record disease incidence. achievements of this programme from mid- urement. • Indicators for animal cruelty including Although time consuming and not without number of complaints and prosecutions financial costs. tives selected by that programme to match • Indicators for dog-related injuries to the problems and causes initially identified. • The project has set out to provide an ing dogs in the early morning (peak effective and humane alternative to time for roaming dogs) including scor. accepted by the municipality and the cation programmes to assess compre. • Official data sources. The impacts on human health edge retention. Dog Population Management 201 the population receiving regular internal Summary and external parasite control. Final example: Colombo achievements Example: Colombo monitoring and evaluation efforts Throughout this chapter a particular pro- gramme was used to provide a working exam- Monitoring and evaluation in Colombo is ple as an illustration. for suspected rabies exposure). and animal welfare have been positive. monitoring and evaluation of under relevant legislation. including: 2007 through to mid-2010 are summarized: • Direct observation and counts of roam. local communities. ing dog population has diminished. imum observed 5%). . and lactation in the case mane methods. education has been well received and • Evaluation immediately following edu. dog population-management programmes • Indicators for relevant zoonotic diseases should quickly provide benefits that outweigh such as rabies. To complete this. previous annual fluctuations (Fig. measured as the incidence these costs in terms of learning to improve rate per month and per year in both dogs programme performance. They should and in humans. sterilization. the achieved using a range of methods of meas. and sterilization from 1990 to June 2010.2. port shared learning wherever individuals. 11. locations. good. p<0. suggesting ther evaluated with data on dog bites there has been some improvement in the for children in the CMC as compared to care provided by the community to both dog bites in the rest of the country. suggest. Elimination vaccinated. in particular in South and South- ably recovering. but be to ensure a suitable national and local there is some evidence that the rate of legislative foundation for this project and increase has slowed and then started to others like it.202 E. The percentage of lactating roaming shown both an increase in knowledge female dogs is significantly and nega. and to establish the source of decrease in recent months. knowledge immediately after the edu- • At the same time the body condition and cation session and that retention was skin condition of the roaming dog popu. Whether this future sustainability once WSPA funding decrease continues will be closely moni. • The education programme on bite organizations and authorities with similar prevention and rabies awareness has aims are found. Blue Paw Trust. it was found that 86% of primary ing every 1% increase in the population school children and 90% of secondary sterilized leads to a decrease of 0. df = 59. vaccination.001). However this is already tored in coming months and years. . BPT. with 85% of primary and 78% of lation have improved. Dog rabies cases in Colombo Municipal Council set against elimination. Using a standard set of ques- (R2 = 0. this programme also the carrying capacity of the environ. immediately following lessons and tively correlated to the percentage of also an impressive level of retention sterilized females seen on the streets over time. tions.33. comes to an end. Hiby 14000 80 70 Number of dog rabies cases 12000 Number of dogs eliminated.1% in school children had gained the required the percentage of l actating females. or sterilized 60 10000 Vaccination Colombo 50 8000 Municipal Council 40 and BPT 6000 Number of 30 sterilizations 4000 Dog rabies 20 2000 10 Start of project 0 0 1990 1991 1992 1993 1994 1995 1996 1997 1998 1999 2000 2001 2002 2003 2004 2005 2006 2007 2008 2009 mid-2010 Year Fig. This will need to be fur- also in unsterilized dogs. sterilized and unsterilized dogs. and initial increase in population size may in response WSPA is beginning to invest be due to the project starting 1 year after in helping the replication of the approach elimination of dogs had been stopped. The a project for Colombo to be proud of. • The roaming dog population size has The main challenges remaining will shown a slight increase over time. but after 6 months. not only in steri. has relevance in other locations within Sri ment through consistent removal by Lanka and the project partners hope to sup- elimination. secondary school children having main- lized dogs (as expected due to eliminating tained this same level of knowledge the energetic demands of breeding). having been kept below East Asia. However. used to develop this programme in other when the dog population was presum. Cleaveland. Available at www. implementers to ensure that the programme prehensive set of components or activities to is humane and minimizes any potential ani- manage populations humanely. reclaimed or adopted from US shelters esti- mated by the Humane Society of the United States. 481–484. Journal of Wildlife Management 44. (2005) The ‘Most Significant Change’ (MSC) technique: A guide to its use. including trap. C. FAWC (Farm Animal Welfare Council) (1979) The five freedoms developed by the Farm Animal Welfare Council. Vaccine 21. S. L.nz/animal-welfare/codes/dogs. 217–244. and Dart.org.. 142. M. and Andreoli. accessed 19 June 2012.) The Domestic Dog: Its Evolution. and human atti. M. F. In: Serpell. CNR is given many names. D. they can also cause difficulties and experience Finally.. Mlengeya. J.. 2 www. J. (1995) Population biology and ecology of feral dogs in central Italy. The decision to own or care ing the benefits of dogs while minimizing the for a dog is rarely a purely functional choice. Francisci. It is also our moral with the design of population management obligation to manage humanely a situation programmes suitable for specific locations and that arguably humans have created through so maximized for efficiency and effectiveness.uk/docs/MSCGuide. (1986) Indicators of poor welfare. accessed 17 July 2012. 4 This section is amended from chapter 1 of WSPA’s Member Society manual. and Kaare. Notes 1 The International Companion Animal Management (ICAM) Coalition is a coalition of non-governmental organizations with experience of dog population management in a range of countries. Tiringa. Kaare. Cleaveland. 3 www. and Barrat (2003) A dog rabies vaccination campaign in rural Africa: impact on the incidence of dog rabies and human dog-bite injuries. Cambridge. management programmes respect this bond tudes and behaviours towards dogs.uk/freedoms.. Dushoff. PLoS Biology 7. 524–526. R.govt.humanesociety. Haydon. Available at www.K. Causey.org/issues/pet_ overpopulation/facts/overpopulation_estimates. 1965–1973. K. (1989) Spatial and temporal resource use by feral and abandoned dogs. accessed 18 June 2012. M. T.. (ed. Cambridge University Press. M. 463–471. problems they can present. accessed 17 July 2012.. G. HSUS (2009) Statistics of dogs and cats entering. hence the common use of ABC as an alternative term for CNR. UK.M. and Cude..co. Hampson. mal suffering.A.icam-coalition. However. targeted as possible.htm. are going to plan and are as efficient and well- vide many benefits to humans.mande. accessed 17 July 2012. and Bekoff. S.. initial assessment and data interpretation that Hence dog owners and carers will expect that relate to the dog population. Dog Population Management 203 Conclusion Continuous monitoring and regular evaluation can also help to assess whether programmes Dogs fulfil many roles in society and so pro. P. 2006.fawc. Using a process of and usually entails an emotional component. accessed 18 June 2012. .org/resources. in India this term is included in national legislation as a definition of CNR and the method of dog population management for the whole country.biosecurity. Although the latter is a general term for reproduction control.pdf. the domestication of dogs for human benefit.T. Behaviour and Interactions with People.html. T. The aim of dog tion management programme designers and population management is to utilize a com.html. Broom. euthanased. References Boitani. D. so maximiz.org. and return (the term usually used for cat population management) and animal birth control. neuter. can help between dogs and humans. 5 Document is available as a download from www. British Veterinary Journal. Ciucci. (2009) Transmission dynamics and prospects for the elimination of canine rabies. (1980) Feral dog and white-tailed deer interactions in Alabama. it is the responsibility of popula- welfare problems themselves. 300–312.icam-coalition. J. 6 Adapted from RSPCA. Davies. Daniels. P. Ethology 81.J. pp. Available at www. org.. 2–4.. Hiby ICAM Coalition (2008) Humane dog population management guidelines. (2005) Epidemiologic situation of human rabies in Latin America in 2004.. Willis.A. (eds) Shelter Medicine for Veterinarians and Staff. J.J. P. org. Church. and Zawistowski.R. W. org/downloads/Shelter%20guidelines. In: Miller. Correa. E. Maldonado. Schneider.. Bransbury. Amorim. Medina. C. RSPCA (2010) Improving dog ownership.. Epidemiological Bulletin/ PAHO 26.204 E.php?id=169&L=0&htmfile=chapitre_1. D. Available at www. Available at www.. int/index.K. 1–32. and Wayne. WHO/ZOON/90. (2006) Burying key evidence: the social bond between dogs and people.M. C. Cook.rspca.. WHO. Rice. Savolainen. Honeycutt. K. (1984) Behavioural aspects of animal domestication. WHO and Bill and Melinda Gates Foundation (2009) Human and dog rabies prevention and control. Available at www. Geneva. Available at www.icam-coalition. M. L.J. Ames. L. accessed 17 July 2012.A..R. Crandall.K.F.M.7. pp. (1997) Multiple and ancient origins of the domestic dog.166. Leanes. A.C.. (2004) Olfactory detection of human bladder cancer by dogs: proof of principle study. R.F. RSPCA (2006) Guidelines for the design and management of animal shelters. S. Annecy.T. the economic case for dog licensing. J. J.. Belotto. (2004) Pet population dynamics and animal shelter issues. R.org .M. Price.icam-coalition. uk/ImageLocator/LocateAsset?asset=document&assetId=1232721594783&mode=prd. I..icam-coalition. 11–24.. (2006) Control of rabies in Jaipur. Journal of Archaeological Science 33. Lundeberg. Morey. Adé. J. Blackwell.O. The Quarterly Review of Biology 59.. British Medical Journal 329. J..pdf.P.oie. India. accessed 18 June 2012. S. A. J.T.E.L. 379–383. M. C. H..1_eng. M.. Scarlett. Science 276. Switzerland. Guest.E. Report of the WHO/Bill & Melinda Gates Foundation Consultation. 1687–1689. S. 1–6. France.. accessed 18 June 2012. accessed 17 July 2012. Reece. WSPA (2007) Methods for the euthanasia of dogs and cats.htm. accessed 18 June 2012. Available at www. by the sterilisation and vaccination of neighbourhood dogs. Church. OIE (2009) Chapter 7.C.. E.who..pdf.7 of the Terrestrial Animal Code – Stray dog population control. McCarthy. Vilà. N.F.int/hq/2010/WHO_HTM_NTD_NZD_2010. Church. and Chawla. Tamayo. WHO and WSPA (1990) Guidelines for Dog Population Management. 158–175. Veterinary Record 159. Iowa.7. G. 7–9 October 2009. and Rodrigues. M. Available at whqlibdoc. on the basis of existing research.N.2 Michael A. e-mail: Tiziana. Geneva. experience accumulated in large- the group of ‘neglected zoonotic diseases’.1 and François-Xavier Meslin4 1 University of Glasgow. For all these reasons. 2nd Edition (eds C. Switzerland A small number of diseases transmitted from the exception that in all three diseases dogs dogs to humans have been recognized as are involved as the main source or reservoir representing a significant public health risk of the causal agents.) 205 . Control. characteristics. 2University of Salford. Two parasitic diseases. UK.1* Philip S. the first requiring the initiation of usually government. have since been complemented by more sus) and visceral leishmaniasis (Leishmania direct methods for disease control based infantum). In addition. and rabies. and new dog meaning that their public health significance population management guidelines recently is not well recognized and their control not produced by international governmental well addressed by national and interna. and Elimination in Dogs Tiziana Lembo. and non-governmental organizations stress- tional authorities. Consequently. UK. a viral disease. by dog immunization (rabies). Zoonoses and Public Health. * Corresponding author. Dogs. ing world. the Director-General of WHO on 14 October This chapter reviews the past and current 2010.3 Katie R. Their epidemiological cycles and path. Glasgow. Scotland. measures at hand to combat these diseases sponsored large-scale prevention and control aim at controlling the infectious agent at activities.uk ©CAB International 2013. Greater Manchester. Macpherson et al. are all beginning to WHO (World Health Organization) report have a marked influence on control strate- on ‘Working to overcome the global impact gies applied to combat these three diseases in of neglected tropical diseases’ launched by affected countries. These zoonoses belong to countries. London. situation regarding prevention and control ways for human infection differ. 3London School of Hygiene and Tropical Medicine. with their elimination. 4 World Health Organization. Craig. fall into on diagnosis and treatment (echinococcosis this category. 12 Zoonoses Prevention. UK. Although these diseases are and leishmaniasis) and disease prevention present in both the developed and develop. future and control interventions in humans and trends for their control and the feasibility of animals are therefore disease-specific. as well as strategies for these diseases and tries to iden- the tools available to tackle them. Prevention tify. Hampson. their public health burden mostly data acquired on dog populations and their falls on poor populations living in devel. namely source.Lembo@glasgow. Dog population control activities cystic echinococcosis (Echinococcus granulo. scale dog reproduction control. particularly in developing oping countries.ac. Miles.L. these ing the importance of ethical and animal zoonotic diseases are included in the first welfare considerations. Infected wildlife includ. 2007). Dog Rabies Control Historical perspectives and current trends Rabies is found in all continents across the globe. and In many parts of the world rabies control has smaller island nations of the Pacific Ocean been spectacularly successful. Bats harbour lem. However. Lembo et al. notification of cases. In most of Africa. 2005). with only Japan.. 2009. before discussing strate. elsewhere. with entire con- considered rabies-free. 2007). In much of to control rabies. .. In the next section we dominated by raccoons. as well as Mediterranean region and in a few countries in China in the 2nd century bc and in ancient in Latin America.. 2006). rabies in dogs has mostly Greece and the Roman Empire (Blancou and been controlled. where an estimated 55. Rabies cases in North America are have since occurred. the species deaths associated with bat contact have been mostly involved in transmission to humans. wolves. there was no 2005.. 2005. bitten and ‘stray’ dogs – et al.206 T. 2010a). 2002). 2005). Castilho et al. most other zoonoses. measures for dog rabies control consisted of Despite this variety of wildlife involved movement/contact tracing and restriction in rabies maintenance... dog the greatest burden in Africa and Asia. measures for controlling rabies histor- in Latin America. (Blancou and Meslin. skunks. 1998. Wildlife rabies occurs in few Asian countries. but in the way through the bite of an infected animal southern-eastern part of the continent jackal meant that rabies was identified earlier than and mongoose rabies also circulate (Bingham. However. 2005. reported in the Amazon forest. the Russian Federation. century in the United Kingdom and France gies for dog rabies elimination. The only applied for the first time in 1885. where clusters of human ically targeted the domestic dog. movement control. Yet. Lembo et al. jackals. rabies is maintained in domes. particularly Before the advent of the first veterinary vac- in Brazil and Peru (Salmon-Mulanovich et al. developing countries (WHO. This century for such measures to become wide- section provides an overview of the current spread in Europe. the vast majority (confinement. The similarity between animal and human tic dog populations only (Rhodes et al. cines against rabies during the 20th century. except the Republic of Korea where it circu. overview the approaches historically used and foxes (Rupprecht et al. had previously been achieved re-emergences tinents. 2010). and in some locations where elimination rabies or rabies-related viruses in most con. were recommended as early as dog-mediated rabies annually (Knobel the 6th century bc by the Avesta in India and et al.. dog rabies remains a prob- ants (Rupprecht et al. Wandeler.. as well as how these hosts (Matouch. Pre-vaccination era lates in raccoon dogs (Kim et al.. and countries that have successfully controlled or Siberia. and foxes have been impli- cated in the Middle East (Seimenis. 2005. but the to a rabid animal before Pasteur’s vaccine was total number of cases is very limited. rabies and the distinctive transmission path- Bingham. while successes were achieved. 2002). 2007. but still circulates in a few Meslin.. In the Eastern in the 4th century ad by the Talmud. WHO. with dog muzzling becom- and historical situation of dog rabies and ing compulsory only at the end of the 19th dog rabies control. efficacious human prophylaxis after exposure ing bats can transmit rabies to humans. A range of species is tinents achieving canine rabies elimination. Nel et al. leashing. the world are transmitted by dogs (Knobel and culling of rabid. and provide examples of eastern Europe. 2008). and destruction of strays. coyotes. it took until the 18th endemic foci (Schneider et al. involved in maintaining rabies virus vari. Dog rabies is endemic in most the so-called ‘classical’ methods (Bögel. 2008). New Zealand. with Measures such as compulsory muzzling. 2005).. As a conse- exception is widespread vampire bat rabies quence. 2007). muzzling) of rabid ani- (>99%) of human rabies cases throughout mals and their contacts.000 people die from respectively. 2000). 2000). foxes and raccoon dogs are reported eliminated canine rabies. 1971). tions combined with strict implementation of cination efforts were renewed and since tie-up orders and shooting of roaming dogs 1957 Japan has been free of rabies. including control measures across the cordon sani- dog muzzling.. including mass dog 1988. and persistence ever since. probably imported. except (Shone. gent legislation. In 1996. Muir and Roome.. tracing and restrictions of taire (Tan et al. The result has isolation. 1921) and was During periods of colonial occupation very successful in controlling rabies until in Africa. border. 1967.. 1968). dog movements. 2006). classical control methods led have achieved rabies elimination in the 20th to the elimination of rabies in dogs in some century.1 for exam. 2004. 2004. In the late 1930s. Korns and Zeissig. the establishment of a country. WHO. making dog rabies et al.. with canine rabies rupted dog-to-dog rabies transmission and being eliminated from large areas of Western eliminated human rabies from most urban Europe throughout the 20th century (see areas in that part of the world (Schneider Table 12. 2008). and continuous upgrad. 1959. 2007. control rabies in Korea. prevent importations. 2007) after a combination of vaccination and classical concerted transboundary collaborations to measures were conducted (Lontai. WHO. of strays eliminated rabies from Malaysia ment of a sanitary policy brought rabies in 1953 (Wells. et al. vaccination. Control. Meldrum.. also led to dramatic declines and rabies elimination from 1945 until 1992 (Kim et al. lowed by a long period of compulsory pet Omoe et al.. and Elimination in Dogs 207 During the 19th and first half of the Japan is not the only Asian country to 20th century. Compulsory mass vaccination. Zoonoses Prevention. vac. national programmes for the con- dog vaccination was included in national trol of dog rabies. 1972. been that dog rabies has since increased una- level rabies management system focusing bated throughout most of sub-Saharan Africa on compulsory registration and vaccination and Asia (Knobel et al. 2011). dog rabies a strict import regulation policy eliminated case was reported outside the buffer zone canine rabies from the UK in 1902 and again (Hussin. National programmes to ing World War I (Fooks et al. countries.. 1962). vaccination was introduced in Hungary.. .. rabies was successfully controlled the disease was reintroduced during World in some countries. and intensive destruction ples). while human and dog populations and 2006 (Shimada. After the war. Following this model. In Latin American Manninger. 2008). Removal of strays and strict enforce. But these control measures for three imported cases of human rabies deteriorated over the second half of the 20th (from Nepal and the Philippines) in 1970 century. mainly on mass immunization of dogs. Held et al. 2005). destruction of strays and one isolated. Enforcement of legislation. Subsequent re-emergence of rabies from the areas bordering the demilita- Post-vaccination era rized zone in 1993.. However. strin- areas of Europe (see Table 12.1 for examples). regulations for import and Domestic dog rabies has been largely export of animals. probably due to relaxation of rabies 1987). of domestic dogs. initiated in 1983 based rabies management programmes in numer. through mass vaccina- War II (Shimada. Together with its geographical control increasingly difficult. Takahashi-Omoe have grown exponentially. been reported since. 1948). but no cases in Malaysia have in 1922. where the first field trials demonstrating the the United States was only declared free of feasibility of dog rabies elimination through dog rabies in 2007 (Blanton et al. 2005). controlled in North America since the 1960s ing of countermeasures against rabies have through mass vaccination campaigns fol- kept the country rabies-free (Takahashi. has been attributed to the involvement of Mass vaccination of dogs started in Japan wildlife hosts (Kim et al. mass vaccination (Blanton et al. in 1921 (Umeno and Doi. with only periodic under control in Scandinavian countries reintroductions from the Malaysia–Thailand in the 19th century (Tierkel. 1971. 2007. 1954). 1988). after its reintroduction in 1918 dur. 1997). 2005). inter- ous European countries.. 1962. destruction of strays and Dog Tax Ordinance Zimbabwe Post-vaccination era: compulsory N (dramatic declines except 1961 (Shone. Suriname.. Mass vaccination. 1948. tion control. as well as oral vaccina. 1976. T. Korns and stray dog control (in 1960s) areas) Zeissig. Lembo et al. 1967. Held et al. 2004) Western Zambia Mass destruction of tribal dogs Y (in one large tribal area. re-establishment since 1965 up until now) Tunisia National programme including dog N (dramatic declines) 1986 (Chadli et al. 1988. Due to unrest and measures) civil war.. tion to eliminate the dog–coyote 2007.. and destruction of areas with Mozambique and unowned dogs (secondary Botswana. Uruguay. re-establishment since 1913 1940) onwards) KwaZulu-Natal Dog vaccination and population N (temporary control) 1960s (Mansfelt. 2008) Central America (Belize. registration. 2011) Rica). years despite canine rabies (Chile. education. 1980.Table 12. Tierkel. Examples of successful control or elimination of canine rabies. but 1901 (Edmonds. 1962) abandoned). 1922. dog popula. 1962) dog vaccination (mainly). 1993) Americas USA Widespread vaccination. Argentina. dog 1938) confinement. pet care. transmitted by dogs for 3 2005. 2007) USA Measures continued as above.1. 1967.. sectoral cooperation. with Y 2004 (Held et al. Blanton et al.. Nicaragua..a 208 Year Continent Country Methods of control Elimination Y/N achieved References Africa Zimbabwe Pre-vaccination era: muzzling (later Y 1914 (until (Shone. Humphrey. Y (except for a few border 1940–65 (Johnson. Velasco-Villa rabies virus variant in Texas et al.. tie-up eastern and western border orders. Guyana. unvaccinated dogs Matter et al. Snyman. 1996. Blanton et al. 1959. epidemiological French Guiana. control Swanepoel et al.. Honduras. Panama and Costa and timely provision of PEP. still circulating ) Paraguay). most of Caribbean surveillance. Osman vaccination and removal of and Haddad. 1966. 1948. decentralization N (but no human rabies 2004 (Schneider et al. Kelly. and education (except Cuba and Haiti) . Southern American cone national and international multi.. Colombia. strict Y 1956 (Shimada. cases near Thai border since development of an immune belt to prevent entry of rabies from Thailand Hong Kong Quarantine/observation of imported Y (but imported in 1980) 1956 (Cumming and Rex. and Elimination in Dogs importation rules and movement restriction Singapore Stray dog elimination. 1954. Control. 1966.. mostly of dogs Y (Raccoon dog rabies 1985 (Hyun. mass Re-emergence when Beran. 2005.. destruction of unrest in 1970. Brazil. et al. Venezuela. 1996. Beran vaccination coverage dropped. Traditionally rabies free.. 1971) Zoonoses Prevention. 1988. Success in vaccinated areas. now et al. Peru.. dog population active circulation in localized et al. Schneider sectoral cooperation. 1957. 1998b) Andaman. Guatemala. 1964–72 (Beran and de Mira. control. 2005) lance. Larghi national & international multi. Kim et al. epidemiological surveil. and Nicobar islands dogs prohibited by law in Maldives to maintain freedom from rabies Continued 209 . 1985) unowned/ unvaccinated dogs. Cuba and timely provision of PEP. Sporadic and Shukor. community education. 1952. Tan vaccination.. transmitted by dogs at Belotto. sub-national level for 3 years. 1987) Republic of Korea Mass vaccination. Lakshwadeep.. 2011. Import of Rabies-free (WHO. dog Cheuk. emerged in 1993 2006) Maldives. 1972) endemic through most of country Taiwan Mass vaccination Y 1961 (WHO. dogs/cats and biting animals. Mass vaccination. 1988. 1972) sanitary policy Malaysia Licensing and compulsory mass Y until reintroduction during civil 1956 (Wells. and education Asia Japan Mass vaccination Y until reintroduction during 1930 (Shimada. and laboratory based surveillance Philippines (central) Laboratory-based surveillance. 1971) World War II Japan Compulsory mass vaccination. Mexico. 2005. decentralization N (but no human rabies 2004 (Chomel et al. 1969) licensing/vaccination. enforcement of Y 1892 (West. 1971. 1987. foci) Belotto et al. stray dog control. quarantine of dogs. enforcement Y pre-1900 (Tierkel. War I) et al. Muir and tracing movements of rabid dogs Roome. Poland. dog Y 1922 (Meldrum. 2005) and their contacts Destruction of stray/rabid dogs. Fooks muzzling. and Czech Republic) notification of rabies dog muzzling Y (territory comprising Germany 1939 (Müller and Müller.. 2004) dogs.. 2004) compulsory muzzling. 1959) of sanitary policy The Netherlands National legislation to control rabies Y 1923 (Aubert et al. enforcement Y 1914 (Müller and Müller.. France. movement restriction. Muir and tracing movements of rabid dogs Roome. 2005) and their contacts. 2004) of sanitary policy Denmark Stray dog elimination. 1988. Fooks muzzling. 1971) of sanitary policy UK Destruction of stray/rabid dogs. Lembo et al.. 2004) destruction of strays Spain and Portugal Pre-vaccination era: destruction of Y (except dog rabies imported 1960 (Abellan Garcia et al. outbreak in Malaga. vaccination.1. enforcement Y 1889 (Müller. killing of 1966 strays. dog Y (until outbreak following World 1886–1903 (Meldrum. and Y 1960 (Aubert et al. 210 Year Continent Country Methods of control Elimination Y/N achieved References Eurasia Scandinavia Stray dog elimination. 1988. 2004) [Reichsviehseuchengesetz as it exist today until outbreak (Imperial Animal Disease Act) following World War II) T. Continued. 2004. 1975) (Portugal). movement restriction. 2004) France Dog registration. policy.. and habitat control (Spain) . enforcement Initial success but subsequent 1875 (West. enforcement of sanitary Lithuania. 2004. 1972) of sanitary policy introductions in 20th century Germany Destruction of stray/rabid/suspect Y (except for border areas with 1914 (Müller and Müller. 23 June 1880 Austria Stray dog elimination. suspect rabid and contact animals. et al. 2004) in dogs and cats Prussia Stray dog elimination. and strict import regulation policy Czechoslovakia Mass vaccination Y 1921–1939 (Matouch.Table 12. 2004) Oceania Guam Compulsory leashing/confinement Y 1967 (Glosser and Yarnell.. Post-exposure prophylaxis. establishment of PEP stations. and compulsory dog vaccination Italy Strict dog registration. Yakobson et al. embargo upon importation/quarantine of dogs and cats.. Lontai.. and stray dog 2004) control Finland Vaccination and dog control Y 1930s.. dog registration and vaccination.. 1982. movement and Y 1935–44 (Manninger. education of the public. Abellan Garcia et al. and impounding and destruction 2004) of unclaimed dogs Greece Compulsory collaring of owned dogs Y 1987 (Mutinelli et al. 1951 (Kaplan et al. trials) 1988. but subse. 2004) and destruction of uncollared dogs. and vaccination of pet dogs.. 1954. ownership tax Y (except imported cases from 1973 (Mutinelli et al. 2004) Hungary Mass vaccination. 2004) Zoonoses Prevention. 1960s (Westerling et al. contact control. and Elimination in Dogs collection. Post-vaccination era: compulsory Y 1975–1978 (Diaz Yubero et al.. establishment of surveillance measures and provision of human biologicals a PEP. 1970) destruction of stray dogs/cats. 211 . stray elimination quent return after end of field Osman and Haddad.. 2004) Israel Compulsory dog vaccination and N (Initial success. 1966. Control. seizure of strays and bordering countries) segregation of biting dogs and (since 1950) compulsory vaccination Yugoslavia Mass vaccination Y 1946–91 (Mutinelli et al. 74 in 1995 (RIA. or PEP prescription based 2008. the Dominican reported 55 cases compared with the >100 Republic. Inter-American inter-ministerial meeting on although in 2007 clusters of human cases still health and agriculture set a target for elimi. surveillance. cases occurring annually in previous years. Tajikistan. While Sri Lanka has imple- from the European Union through a combina. and Greece reported the absence of rabies to WHO in 2008 (Aylan The Americas have been the greatest rabies et al. 2005). The 21st century Republic of Macedonia. 2008). where eight human rabies cases were tion of Haiti).. which after review by Nepal has also made significant progress in the Regional Committee was moved to 2015 prevention and control of rabies. an average of 9 and 3 human rabies deaths where around 250 rabies deaths are reported per year. of human rabies deaths is limited (Bourhy However. have had significant 2009). and there- cases). dog rabies still exists as a prob. and the Plurinational State of Bolivia (WHO. and now (WHO/PAHO. control success story of the 21st century. Guatemala. and.. 2008). that began in the 1980s. particularly dogs (S. <50 human trol and elimination of dog rabies have been rabies deaths have been reported annually in developed. Rabies is pers. 2011). Albania. Since then. respectively. of about 18 million people and an estimated and Uzbekistan is also not well known 2 million dogs. mented a programme that has resulted in tion of mass vaccination and ‘classical’ meas. although the number of rabies post-exposure prophylaxis (PEP). during the period annually (RIA. progressive increases in vaccination coverage ures. 2009). Rybakov. however. . centre of the archipelago with a population eral countries such as Azerbaijan. comm. Schneider et al. Thailand and Vietnam have been largely due In contrast. by ted to eliminating human and dog rabies by 2003. The Visayas was launched in 2005 with support from the comprise a number of islands located at the European Union. (WHO/PAHO. A total of 29 cial programme aims at eliminating rabies deaths occurred in Turkey from 1999 to from the entire archipelago of the ‘Visayas’ 2009 (Aylan et al. In 2008. and large reductions in human rabies were 2010b. In this country a spe- 2000–2009 (Aylan et al. the reductions of rabies cases in economic ramifications (Lardon et al. 2011). particu. fore PEP rates remain very high. 2010).). 2011). the majority still resulting from reported to WHO in 2008 compared with contact with dogs.1). occurred in 25 out of 63 provinces in both the nating dog rabies in Latin America by 2012 North and South of the country (RIA. El Salvador. Similarly. Lembo et al. The rabies situation in sev. 2007a). these PEP interventions have also et al. Since Although dog rabies is present in all the city-based mass vaccination programmes countries of the South-East Asian region. 2011).. efforts have been several countries have also recorded suc- rolled out into rural areas with approximately cesses and a number of countries are commit- 45 million dogs vaccinated a year. In Thailand. 2009). the 15th seen also in Vietnam between 1994 and 2008. and a nationwide by the end of 2013 and obtaining rabies-free fox and dog rabies elimination programme status by 2015 (WHO. Progress is evident in Thailand the Region of the Americas (with the excep. 2009. Haiti. representing >34% of all animal rabies on the status of the biting animal. Russia alone reports from 10 to been costly since there have not been con- 20 human rabies deaths every year and high comitant improvements in dog rabies con- numbers of cases in pets (more than 1500 in trol. produces its own human and veterinary Endemic dog rabies has been eliminated rabies vaccines. as described above (see also Table 12.. to improved availability and accessibility lem in Eastern Europe. A number of smaller islands (Gruzdev. 2007).. occasional introductions.212 T. 2009). (Kumarapeli and Awerbuch-Friedlander. the number of cases of dog-transmitted 2020 (ASEAN. Dog rabies is. the former Yugoslav in the Visayas have been declared rabies free. Sri Lanka... 2008). human rabies in the region had fallen by >90% Vietnam. 2009). Georgia and Ukraine reported still widely distributed in the Philippines. in domestic dogs over the last three decades However. and Nepal national plans for con- (Schneider et al. Sri Lanka still widespread in Cuba. larly from North Africa. comm. Mumbai.000 dogs against rabies. However. eliminated control measures must be directed . 2010.. and ineffective local animal vaccines of 1997 resulted in a least 113 deaths dur. mostly from six south–central provinces (Fu. at protecting human health. Sudarshan. or are Rabies is a re-emerging public health risk targeted for rabies freedom before 2015. 2009).g. including dog vac- on Flores island which started at the end cination.000 people annually in India (Sudarshan et al. 2008). Zoonoses Prevention. 2007) based on dog capture. to reach rabies-free islands. 2008). Windiyaningsih et al. New Delhi. trol activities that were carried out by the and this number is continuously increasing provincial veterinary services prioritized (Q.K. 2011). and Elimination in Dogs 213 for example Apo and Siquijor islands. Bangalore. indiscriminate dog culling operations rather Most African countries report the pres- than dog vaccination campaigns. the and measures targeting the species mostly number of human rabies deaths is thought responsible for transmission to humans. Dog rabies con. Society for the Protection of Animals (WSPA) South Africa and the United Republic of and direct involvement in field operations Tanzania have begun projects working to of a local organization named Bali animal eliminate human and dog rabies from pilot welfare association (Bawa). confirmation in late 2008. for infection to be Bangalore.. comm. such in China. and Approaches to rabies control and preven- release.. Beijing.).. mens are administered annually nationwide. 2004) and is still entrenched in 2010. Dog rabies is estimated to kill about 20. coupled with increasing pop- ing the period 1998–2002 (Windiyaningsih ulations and poor awareness (Wu et al. However.). with a lack of government commitment. Tallis. Initially. rabies in the most affected provinces the number spread to all provinces on the island and by of notified human rabies deaths decreased to February 2011 more than 100 human deaths 2215 in 2009. 2008). pers. (Bingham. Bali in 2008. pers. and elimination Chennai. 2001. Maluku and Ambon in 2003. comm. 2005). parts of their territories. following the initia- tion of a number of dog rabies control pro. et al. in late 2010 the Bali provincial dog vaccination coverage remains far below authorities committed to an island-wide the required threshold of 70% (Lembo et al. Strategies for dog rabies control grammes in major cities (e. (Hu et al. but around 8 million PEP regi- had occurred (CDC. authorities resorted to mass culling The island of Bali was free of rabies until its as a major tool for dog rabies control (BBC. Since early 2009. 2009). 2007). Tang. to make Bali rabies-free in 2012 with the especially to the populations most at risk technical and financial support of the World (Hampson et al. 2010.. Dog rabies killed between 4000 and as Bohol (ARC. Jaipur) (Reece.. but were ence of human and dog rabies in all or large ineffective in preventing rabies spread... Yet the late 1990s and emergence on historically the disease re-emerged progressively. Control. In most countries. mass vaccination campaign to inoculate 2010).). 7000 people a year during the period 1979– The rabies epidemiological situation 1989. Disease re-emergence was associated and Nias islands in 2010 (G. but was very swiftly brought under has been worsening over the past 15 years control in 5 years with only 159 human rabies in Indonesia with spread eastwards since deaths reported in 1996 (Tang et al. The rabies epidemic ation of control measures. Following public education vaccination campaigns were conducted campaigns and control activities conducted in villages around the index case. relax- 2010. aiming ity of human vaccine is still very limited. and the accessibility and affordabil- nearly 400. pers. Although mass 2006. 2004). Jakarta. such as Flores in 1997 3300 notified human rabies deaths in 2007. 2007a).1 areas within 5 years (WHO. 2007). to have decreased considerably during the While both approaches are ultimately aimed second half of this decade (M. CBC. vaccination. as well as the wider availability of tion include strategies directed at humans mostly locally produced cell-culture rabies (pre-exposure or post-exposure prophylaxis) vaccines and immunoglobulin for PEP. good measure of the incidence of rabies in an nary measures adopted for the control and area. the rabies situation at the start of a control programme and monitor progress towards elimination. ing countries mortality and birth rates in dog cent antibody test. and is necessary to determine true incidence of rabies. In many parts of the world though. Since the development of effective ani.. dog population assessment and man. compulsory Beyer et al. Tao et al. DFA) (Meslin and Kaplan. 2009).. but may also reflect inade- ownership should also be considered critical quate health service provision. However. High levels of awareness amongst Reporting of suspect cases and hospital key players in rabies prevention and control is records of animal-bite injuries from suspect vital for effective policy towards canine rabies rabid animals can be very useful because of elimination. the elimination countries and has shown complete concord- of rabies requires several additional compo. including allocation of resources. 2008) engagement of communities and policymak. the characteristic clinical signs of rabies that defining specific roles among all sectors are accurately recognized by local communi- responsible for rabies control and establish. facilities for fluorescent coverage falling to ineffective levels (Hampson microscopy are not available. Here we focus on veteri. data collected at the national management and vaccination efforts.. and habitat management). at the species involved in rabies maintenance are lacking and may not necessarily provide a in any given area. ties (Hampson et al. Hospital records also con- dog registration and vaccination. are proving useful surveillance tools (Kang agement. or equipment et al. and surveillance capacity and et al. level are often based on clinical signs rather than laboratory diagnosis... delivered.214 T.. Markotter et al. ance with the gold standard DFA (Lembo nents to mass vaccination. campaigns need to be repeated to prevent particularly in Africa. 2007. as has been demonstrated in the Americas. 2008). Although lower levels of coverage ples as well as local capacity for performing can sometimes be effective. intersectoral cooperation. and are less expensive. legislation. including the Surveillance submission of samples for laboratory diagno- sis. require of settings. 2008. animal tain information on numbers of PEP regimens movement control. reported laboratory-confirmed cases paigns. 2006. consisting of well-designed educational cam- Hence. 1996). Lembo et al. the direct rapid immunohisto- mal vaccines for rabies. Durr et al. in many develop- standard diagnostic tests (the direct fluores. 2011)... Lembo et al. which can provide some indication Education and promotion of responsible dog of rabies trends.. In many devel- to enhance the effectiveness of dog population oping countries. populations are generally high and therefore 1999). simpler infrastructure. 2008. and lateral-flow immunodiagnostic test kits ers.. Vaccination of 70% of the dog population has Most surveillance relies on laboratory repeatedly been shown to be effective in elim- confirmation and therefore requires a system inating endemic canine rabies (Coleman and for the collection and submission of sam.g. 2009). Channels of reporting and communication. ing legislative frameworks (e. Surveillance becomes increas- ingly important for the demonstration and Dog vaccination maintenance of freedom from disease. 2008. and capacity or higher) can be attained through strategies for sample collection in the field is limited. Alternative tests for rabies are now avail- eventual elimination of dog rabies in a range able which show promising results. including effective et al. and are largely incomplete (Dodet et al. Dye. as officially Surveillance is an essential part of rabies reported records currently underestimate the control efforts. High vaccination coverage (70% is not adequately maintained. therefore need to be improved. community . mass vaccination chemical test (DRIT) has been validated on has become an integral component of rabies field diagnostic material from developing control measures. Specifically. In Chad.. 1993. erinary clinics). The major obstacle posts in well-recognized sites within the com. local commitment in planning To achieve coverage of 70%. 1995. as cost per currently available commer- point vaccinations). Guzel et al. for ties and field veterinary staff demotivated. of dogs has been shown in various settings to In most settings domestic dogs have lead to significant increases in coverage (espe- been found to be highly accessible for cially of ownerless and poorly supervised parenteral vaccination. availability of recognized should therefore be ready to substantially sub- quality vaccine. 2008). and communi. tion coverage needs to be measured. Kayali et al. old vaccination coverage of ~70% cannot be Serological testing is often thought reached. 2009). cen. Robinson et al.. However.. general coordination and supervision of the In some circumstances (e. 2007b). vaccine strain known to be safe and effica- tral point vaccinations are generally the most cious (WHO. (ii) component of any dog rabies control and continual vaccination at fixed vaccination elimination programme. to be an alternative method for estimat- led. nor a convincing operationalized endemic areas: (i) house-to-house visits. in some countries is concern over safety of munity (including private or government vet. Zoonoses Prevention. the WHO Oral Vaccination Delivery (OVD) Ratsitorahina et al. 2010).g. oral vaccination more affordable. The use of tempo- et al. Wandeler et al. as turnout population size and growth rates. and effective sidize dog vaccination campaigns. incorporating a In terms of the costs and logistics.. vaccina- 1 week) (Belotto. even when the major. Registration may be too low to achieve adequate vaccina. 2007b). meaningful evaluations of titres. ing vaccination coverage.. resources will be wasted.. 2009. 2009). differing in suit. 2003. In Latin America.. Lembo et al. 1998a).. and in variety of operational approaches for mass dispersed communities) alternative delivery dog vaccination is available. owners were found to dogs is recommended. 2007). or in combination with parenteral vaccination ers are evident (Perry. lack of be only ready to pay an amount (USD 0.. dog rabies is unlikely to be control.. However. provided motivation for owners to take their rabies control is a public good and if a thresh.. 1993.. strategies may be required to achieve high lev- ability and effectiveness depending upon the els of vaccination coverage. However. A potential alternative to charg. 1996. both when applied exclusively ity of dogs appear unrestrained and no own. the rabies or vector virus strains for humans. and permanent identification of vaccinated tion coverage. 2001. Group had its last meeting (WHO. requires an initial determination of the dog tion is usually counterproductive. as it was expected (Meslin combination. 2008. 1998. 2004. pets for vaccination (Kaare et al. 1998. either alone or in rabies elimination’. rary coloured tags or plastic collars has proven ing is to encourage voluntary contributions. The choice of approach cial vaccine bait is manyfold greater than the will depend on the specific community. media support.36 per dog) that was substantially less than dogs should not prevent the implementation the total cost of having a dog vaccinated (Durr of a vaccination campaign. Lucas et al. 2009). et al. Yet. owned dogs). governments and execution. 1988. pulsed mass vaccinations at central points To determine the effectiveness of vaccina- have been conducted free of charge on an tion efforts and whether sufficient numbers annual basis with high coverage (around 80%) of dogs have been reached or supplementary achieved in a short period of time (no more than follow-up measures are necessary. locally (Estrada et al. more than 10 years after Kongkaew et al. for very activities (Schneider et al. (Matter et al. and cost of an injectable vaccine. to be useful in identifying vaccinated dogs and avoiding a perception of coercion. Charging for vaccina. Three basic approaches to mass vaccination OVD has neither become the ‘key to dog campaigns have been adopted. Control. Oral vaccination setting. Suzuki et al. However.78– resources or capacity to permanently identify 1. and Elimination in Dogs 215 participation. and (iii) mobile teams which whereas in others it is mostly an economical set up temporary vaccination posts (central issue. serological . 2001). a aggressive or truly unowned dogs. to control rabies in canine rabies.. WHO..... 2000). could however make efficient (Kaare et al. Baits produced the decision should be taken at the local level. Schneider et al. This also 2007. 5 IU per ml of serum (con. as opposed to the quantitative assessment of A lack of options for permanent marking levels of coverage attained. including access for vaccination. and the number of trol. Culling may often be counterproductive. through dog ecology studies. lation densities or the spread of rabies (WHO. the proportion of young dogs in the pop- to determine the most appropriate manner for ulation. greater resources and therefore populations or for maintaining a cordon sanitaire from recover rapidly. vaccinated dogs may be destroyed. serological coverage assessments a very which may often facilitate disease spread. expensive and inefficient operation. by increased survival rates (WHO. reproduction of vaccination campaigns. and the test should and habitat management. the sheer numbers of can lead to the movement of animals from animals that would need to be tested makes infected areas where culling is taking place. either be a WHO and OIE reference test Contrary to popular belief that rabies can (RFFIT (rapid fluorescent focus inhibition be effectively controlled by culling. which is often control. 2005). 3. of vaccinated dogs means it is rarely pos- Once rabies is eliminated. A combination of dog population manage ownerless dogs that may be more difficult to ment approaches is recommended. continued sible to determine the vaccination status of vaccination may be necessary in defined free-roaming animals. Indeed. Remaining dogs have areas. grounds (Dalla Villa et al. But in most dog vaccination can be increased through dog developing country settings dog population population management. depending on the risk of introduction. considerable test) or FAVN (fluorescent antibody virus experience from projects around the world has neutralization)). genuine concern about vaccine efficacy.. The need for dog control programmes tend to use methods that population management should be evaluated are considered unethical on animal welfare at the beginning of a rabies control programme. breeding behaviours that may make delivery of vaccinations and reproduction con. 2005). or have been calibrated found no evidence that removal of dogs alone against one of these reference tests. removal of dogs. logistically difficult. as studies using serological and possibly other sterilized. The has ever had a significant impact on dog popu- minimum rabies virus neutralizing anti. Culling may also increase demand for dogs by opening a market for replacement of culled animals. However.As dog populations The use of reproduction control for dogs differ in demography. Even the highest needed in vaccination campaigns designed to recorded removal rates (about 15% of the control infection in residual foci. 2010). or to contain dog population) are easily compensated for new outbreaks. in which lower values should be 2. Lembo et al. Different strategies may be of culling are short-lived. samples need to be collected within 1 month responsible dog ownership. The rationale for reproduction patterns. the targeted and humane Dog population management removal of unvaccinated. Furthermore. legislative measures. and community attitudes towards control is to reduce the dog population turno- dogs is advised. There are several reasons for this: sidered satisfactory for the international 1. campaigns. the collection of prelimi. dog ownership coverage. can help to reach and maintain vaccination nary data on dog demography. body titre of 0. Dogs may be accessed . dogs more susceptible. while gener- should not be used to assess vaccine efficacy ally only reaching a small proportion of the in dogs immunized in the context of mass population.216 T. tests should only be considered if there is therefore wasting resources. ownerless dogs may be effective when used as a supplemen- In some communities the effectiveness of mass tary measure to mass vaccination. Culling diverts resources from vaccina- transfer of dogs and cats vaccinated at least tion and takes considerable effort (often twice under strict veterinary supervision) much more than vaccination). so any potential benefits infected areas. Culling antagonizes communities and expected. This information can be used ver. and research is under costly to provide a sustainable solution to way to create a single injectable product such dog population management in all countries as a rabies vaccine-based recombinant immu- where this is required. followed by sterilization and vaccina. Surgical numbers. could go a long way to reducing the need for tion. an ABC programme that reached for 2–3 years will probably cover the entire over 60% of the free-roaming dog population lifespan of most dogs in the developing world was found to both reduce and stabilize dog (Kitala et al. For example. 2008. 2009). Some are already registered for use in wild- tion have been advocated as a method to life and will potentially become available at control urban street dog populations and ulti. Surgical for affordable and sustained dog population sterilization is currently the most common management. for instance vaccination should not be forgotten. A major obstacle to effective dog rabies elimi. 2006). By reducing the effort and costs of sterilization can be useful on a small scale treating dogs. immunocontraceptives should for reducing turnover. Control. Immunocontraceptives that induce fertility In Jodhpur. Since the 1960s. with immunocontraceptives. but in address a number of other issues associated many instances the cost of spaying/neuter. Immunocontraceptive vaccines of capture (Animal Birth Control. and public acceptance of fertility et al. and release). conjunction with a rabies vaccine does not affect parenteral rabies immunization in dogs (Bender et al. In general though. Gonacon™ populations (Totton et al. ABC. promote responsible pet ownership including lization options are under trial. and therefore the loss of herd immunity of using immunocontraceptives to control dog after mass vaccination campaigns. Surveillance remains an enduring prob- 2005. however.. and therefore increased deployment of the Galapagos reported side effects in a small field diagnostic tools and cheap and user- proportion of dogs (Levy et al.. a fraction of the cost of surgical sterilization. 2011). and effectiveness tions. post-operative care. (Massei and Meslin. not registered. mately human rabies in Asia (Reece.. a study from lem. also seem.. product. programmes coupled with rabies vaccina. 2010). US Department of Agriculture. and release at point tion options. as they intratesticular injection of balanced zinc solu. testing the feasibility. surgical sterilization coverage of less than Denver. and not 40% would maintain the dog population at yet commercially available) administered in current levels (Totton et al. Some permanent steri. particularly within reduce the costs of dog population manage- targeted capture–neuter–release or ABC pro. neuter. Future work should also grammes for truly unowned dogs. which could sub- areas. Considerable scope exists for the the obstacles remaining for effective rabies . 2010). New immunocontraceptives method of reproduction control but is too are being developed. and Elimination in Dogs 217 for reproduction control via their owners development of safe chemical sterilization of or by catching ownerless dogs from public both female and male dogs. 2001). stantially reduce the cost of current steriliza- tion. Zoonoses Prevention. Massei rural areas. Esquivel-LaCroix. The demand for sterilization control in various cultural and social contexts techniques (both chemical and immunologi. ment programmes. such as timing ing very large numbers of animals is likely and frequency of applications in urban and to be unsustainable (Menezes. While found to be safe and effective in such tools. cost. 2010). the most promising candidates known as catch. Vaccination (National Wildlife Research Center (NWRC) coverage has been predicted to remain above Animal and Plant Health Inspection Service 70% if this programme is maintained. 2009). Colorado. 2008). Thailand and Mexico (Tepsumethanon et al. Yet measures to cal) is therefore high. 2007). ABC nocontraceptive (Rupprecht and Wu.. while (APHIS). and friendly means for reporting cases should some concerns remain about the safety of this be considered a priority. Future research should focus on field- nation is the rapid turnover in dog popula... and so this contraceptive could be administered in conjunction with Future directions rabies vaccines to optimize dog population and rabies control. granulosus (sensu and western and central China. the parasite occurs as a benign parasites are carnivores. opment of community-based sustainable ini. vast endemic in traditional thinking in many countries. Syria). However. occosis (AE). but still remains an administrative Eurasia. Community engagement is incidence of AE is relatively small (<20. of E. China’s 31 provinces and is one of the impor- toral collaboration. ronments/food contaminated by dog faeces. with CE are represented by direct and indirect con- >1 million lost disability adjusted human life tacts of humans with faeces from infected dogs. dogs as final hosts. and mostly campaigns and achieving necessary levels of restricted to European and Eurasian foci. years (DALYs) and a conservative estimate of Children are often found infected. such as Mediterranean Echinococcus are particularly important for countries. Libya. Iran.. Pakistan. but options for devel. In Russia and parts of this goal. multilocula- ment to sustained implementation are lack. their close contacts with dogs or with envi- Craig et al. and logistical barrier. and free vaccine deliv. Israel. 2007. though Major risk factors for contracting human under-reported health burden globally. WHO. Conversely. Cystic Echinococcosis Control 1997) and in East Africa (Kenya. 2010c). This section will therefore concentrate on tiatives could be further explored. the cycle tumour (hydatid cyst). Tanzania. cysts may be stricto) causing cystic echinococcosis (CE). and the Near East (including Turkey. granulosus involves primarily domestic in the liver or lungs. could be equally dering the Mediterranean. 2001). tion and humane methods of dog population E. Argentina. 1989). with Similar approaches. Egypt) (Kachani et al. China (Schantz et al. Afghanistan. Kyrgyzstan. disease resulting in a significant. Tunisia. 2010). granulosus is very widely distributed. but pathological outcomes are more severe. 2004). Peru. found in 1–40% of cattle and 1–80% of sheep. Two species of tapeworms of the genus In endemic areas. namely E. and other livestock as intermediate tools are available. 1995. and sheep. and effective throughout the developing world.. high transmission within the countries bor- national or regional context. Effective cattle. hosts. Brazil. community participation. control. and regional levels to cially sheep-rearing countries/regions of ensure that finances and human resources are Australia and South America. in most cases. areas exist. tant zoonotic diseases in west and north-west strong media support. goats. political commitment.218 T. and from 0. ern Europe. 2007). In Africa.. India). and E. It acquisition and supply of canine vaccines by also occurs throughout southern and east- ministries of health. camels. eastern Africa.2% to 50% of dogs are infected. It has been recorded in 21 of Organization of campaigns based on intersec. . yet capacity and commit. and requires a shift Uzbekistan. unique or multiple. 1997). Lembo et al.000 not only critical for the success of vaccination cases annually) compared to CE. ity in Latin America (Schneider et al. including effectively deployed.. A primary the control of cystic echinococcosis for which goal for the future is to find the means to dog-focused interventions and surveillance increase local capacity for mass dog vaccina. vaccination coverage. awareness must be involving most pastoral regions and espe- raised at local. Concomitantly. because of 1. the cycle of E. Iraq. public health. the Middle East (Jordan. and Mongolia. two major endemic zones exist. ris is predominantly sylvatic involving foxes ing. Sudan.2 million cases annually (Budke et al. Final or definitive hosts of both In humans. and Uruguay tion for rabies control is a major step towards (Rausch. multilocularis causing alveolar echinoc. on the Iberian Peninsula (WHO/OIE. 2006. Uganda.. Intersectoral collabora. The endemic rabies. despite the costs incurred for dealing with and microtine rodents (see Chapter 8). However. including Kazakhstan. Ethiopia) (Macpherson Human echinococcosis is a neglected zoonotic et al. national. Chile. ery has been key to success and sustainabil. any tissue or organ may be involved. Algeria. including countries of the north (Morocco. once adapted to the local. Craig. South America. c ontrol are not technical (PRP. the Black Sea.. are paramount. 2010). infections in 1973. cystic echinoc. and (from 1864) benzimidazole drugs. Control. This new wool and milking ewes to fat lamb produc- knowledge identified parasite transmis. Reduced transmission was also facili- The life cycle of the tapeworm Echinococcus tated by reduction in dog numbers as a result granulosus was determined by European of several distemper epidemics between scientists during the 1850s as a result of the 1870 and 1892. imposed a tax on Larrieu. 2006). the highest prevalence occurring in early 1860s. the hydatid parasite and the role of dog man- occosis is theoretically an eradicable disease. Rupture of the cyst may lead to life-threaten- ing anaphylactic shock and to dissemination to many tissues and organs. and from 1870 livestock hus- independent research of von Siebold. with the last confirmed sheep (WHO/OIE. (ii) treat dogs The last transmission between dogs with an anthelmintic. 1973). about the life cycle of 1989. together with annual dog treatment . agement and livestock slaughter practices and success in elimination of regional and in disease prevention. spleen. However. Craig and Larrieu. 1953. symptoms and signs are observed.. dog owners. and 1957).0008%. 2001. A Hydatid Law. hygiene.000 inhab. Control was recommended to be patients aged over 60 years (n=57) born in the based on four aspects: (i) prevent dogs hav. This imme. annual incidence of was posted to Iceland in 1860 where human human CE surgical cases in endemic coun. 1990). In the 36-year period 1930–1956. Zoonoses Prevention. It became illegal to feed livestock offal to dogs. In 1864 some countries. New Zealand.. or a combination of treatments (Brunetti et al. Tasmania. Cyprus) (Gemmell and Roberts. period 1841–1880 (Dungal. depend. 2010). 1924. Craig and 1890. bone. infected organs had to be burnt or buried. in Iceland. However. highly prevalent among the Icelandic popula- itants. 3576 human autopsies were performed and diately led to the development of detailed of these 130 (3.. Treatment is rep- resented by surgery. ing access to livestock offal. and livestock/herbivores as inter. community mass screenings he wrote an 18-page information booklet in with abdominal ultrasound have shown local Icelandic Scandinavian that was distributed prevalences of 5% to >10% (Macpherson et al. tion with export of adult sheep. Li et al. Ovine CE contact. These components were articulated prevalence in Iceland for the period 1948–53 in the 19th century but are still valid today was 0. various implemented in five island regions (Iceland. 2001).. hydatid disease (cystic echinococcosis) was tries ranges from 1 to 200 per 100. interventional radiology Echinococcosis control in Iceland (puncture and sterilization of the cysts). and dogs were to be treated annu- ally by a designated village ‘dog-cleaner’ with Historical perspective of echinococcosis an areca seed extract vermifuge (replaced in control and the island programmes 1930 by arecoline hydrobromide) (Beard et al. first local transmission of human CE disease has passed in Iceland in 1869 (and expanded in been achieved (WHO/OIE. Depending The Danish veterinary scientist Harald Krabbe on the area considered. Falkland Islands. 1957). and kidney. and Elimination in Dogs 219 i ncluding brain. By the decade sion with dogs as definitive host of the adult 1890–1900 new cases of human CE were rare worms. Naunyn. 2001. ing on the primary location of the cyst(s). (iii) meat inspection and humans in a non-latent autochthonous and offal disposal. bandry changes were made from primarily Krabbe and others (Grove. Surveillance through meat Consequently in the 20th century hydatid inspection was maintained during the 20th control programmes at national or state/ century. regional level were eventually successfully After a silent asymptomatic period. mediate hosts of hydatid cysts. free to all households.6%) were found to be infected recommendations for ‘hydatid control’ in the with CE. 1998). and (iv) health education case in Iceland was diagnosed in 1960 in a about the parasite lifecycle. 2006). and dog 23-year-old woman (Beard. in highly endemic foci of tion (up to 22% autopsy prevalence). 8 confined to rural dogs only.43%. control after dog dosing had ceased. adopted a very effective hydatid control grammes implemented between 1959 and programme (1964–1996) at a time when 1997 (New Zealand) and 1964 and 1996 human CE incidence was >25 per 100. Intensified health education from These were: (i) funding and management 1938 to 1958 also provided free arecoline for was by the Department of Agriculture from owners to dose their dogs every 3 months. with. gramme differed in four important aspects nized as a public health problem towards the from the New Zealand hydatid control latter part of the 19th century and was made a scheme. 2006). During this period in New Zealand. and the outset. after local authorities applying the day-to-day previously (1880s) having the highest national control measures. The a local dog tax added to the normal dog Iceland hydatid campaign was the first in the licence fee. with ered free of E. includ. A ‘main- ern regions (Gemmell. Iceland). meat inspection. 1990. was the result of wide-scale well-organized The Australian island State of Tasmania government-backed hydatid control pro. Council (Hydatid Act 1959) was formed. transmission of E. later under the more effective direction by out a vertical control effort directed against the Ministry of Agriculture through 6-weekly dogs. by technicians to detect dogs infected with human CE incidence fell dramatically within E. have not been successful in reducing dosing (niclosamide initially then PZQ after CE transmission in other regions of the world 1978). granulosus and human CE remain endemic key elements of a ‘consolidation’ phase of in mainland Australia. granulosus from dogs to humans virtually ceased (Meslin et al. (with praziquantel (PZQ) from 1979) and the surgical cases per 100. emphasis was also phase (11 years in Tasmania versus 32 years placed on health education (as was done in for New Zealand) (Craig and Larrieu. but both island ter. This and Lawson. 1990). tenance of eradication’ phase was reached in Human CE. 2006). rather than purge samples being 50% of sheep remained infected. However. Overall this ‘attack’ phase lasted world.. granulosus since the 1970s.220 T. 1986. Gemmell. however. granulosus (or Taenia hydatigena). Lembo et al.000 (Gemmell. application of strict importation regulations As a result. together with restrictions to ritories declared that hydatid disease was re-entry of the parasite in livestock (Gemmell eliminated from their islands by 2002. however. The Tasmanian pro- Human CE in New Zealand was recog. Dosing was applied up to booklet on E. despite this health annually (with added value for educational education approach. involved supervision of dog registration and mission and human CE from the country. a National Hydatid Eradication (Beard et al. this was funded through prevalence ever recorded worldwide. 2000) and the national ovine CE prevalence by 1980 was only 0. which resulted in a shorter ‘attack’ notifiable disease in 1873. in the late 1950s nearly aspects). 2005). (ii) mobile dog testing/purgation the 1940 Meat Act made it illegal to feed raw (with arecoline) units were used to visit farms offal to dogs. and succeeded. four times yearly over 13 years (1959–72). was also formerly an New Zealand in about 1998 and consisted important public health problem in New of permanent surveillance of livestock at Zealand and Tasmania. sent to a central testing laboratory (as was ing >80% of sheep ranches surveyed. 1990). granulosus and hydatid disease. and Educational programmes. and done in New Zealand). 2006). Iceland has been consid. 2001). to eliminate parasite trans. Jenkins.000 (Tasmania) (Craig and Larrieu. (Craig and Larrieu. in the rural population. in large part through about 32 years (1959–1991) and initially health education. the application of arecoline hydrobromide Though elimination took more than 100 years. and to 30 years of the distribution in 1864 of Krabbe’s penalize owners.. (iii) dog testing was human CE incidence in rural areas was 11. and (iv) farms . especially in east. In 1990 movement control Echinococcosis control in of livestock and slaughterhouse surveillance Australasia (from 1959) (including diagnostic histology for very small lesions) with trace-back was introduced as E. 000) dogs were infected after being worked.16% in 1993 (Reichel paign was continued only in the area con- et al. then PZQ controls and meat inspection (Economides was provided free.004%) of dog faecal samples were (from 1965) and Cyprus (from 1971) coproantigen positive. Unfortunately no pre-control trolled by the Government of the Republic dog data exist. 2001). pers. and (iv) in local livestock have occurred in Tasmania retention of safe offal disposal and surveil- since 1990. The only dog prevalence data of Cyprus. 1996).S. Drugs also instigated. granulosus copro-DNA (S.9 per of 59% (Whitely. ovine CE prevalences ranged from CE cases were recorded in 1963 with an 25% to >80% in aged ewes. and obligatory field-testing raw offal to dogs. 1983). Roberts. in 1997 and in 2009. comm).000 for the period 1965–75 (Bleany. cases under 20 years of age were diagnosed. comm.6% of dogs purged in the GCA.06% by 1981–85 dog populations. but by In the 1960s. (iii) retention of 6-weekly (Beard et al. dosing continued at least et al. comm.. sus purge-positive dogs (Polydoru. No or district level elimination. 1996). how- (old case) was reported in 1992 (S. 2001). refer to coproantigen ELISA testing done in with cessation of activities in the Government 1992–3 when 1. and (iii) prohibiting the feeding of 1971 and 1985). CE prevalence reduced from 52% to 3. births. 1998).000. P. ever. which have lages and in 0... unpublished). Jenkins. with euthanasia of all E.7% of 464 dogs were positive Controlled Area (GCA) (Polydorou. and only Echinococcosis control in the Falkland Islands 2/563 (0. attack phase) was (i) the appointment of dog inspectors. Total dog prevalence reduced until 2011. CE was first recorded in the Falklands in a B. Legislation was updated by arecoline testing. Pointing.. under a second with arecoline every 3 months for registered Tapeworm Eradication Order.. (Reichel et al.75% by 1977 and by 1984–5 offal disposal and confinement of dogs unless zero (0/36. These include: (i) human CE cases occurred in the under-20 a national dog registration scheme with noti- years age group in Tasmania after 1976. Control. while 14% of farm equivalent annual incidence of 55 cases per dogs were infected (Economides et al. Zoonoses Prevention.8% and It should be noted that after 1974 the cam- further reduced to 0. In 2010 a suspect hydatid cyst in a 7-year-old sheep was confirmed by DNA analysis to be E. 1998). Strong reliance was also placed on from 7.). several perma. A national hydatid control programme was Hydatid disease control was introduced in introduced into the Republic of Cyprus in the Falklands in 1965 (Tapeworm Eradication 1971 under the Ministry of Agriculture. Eradication was claimed in 1985. Boufana. granulo- was undertaken every 12 weeks with buna. 100. S. In the Falklands.000 killed between (Tenoban). From 1970. The Dogs Order). Craig. ovine fications of transfer to new owners. 1993). 1984). it was found that the parasite was still pers. This order made provision for: intervention emphasis (i. including one dog pos- itive for E. (ii) the primarily focused on the reduction/elimi- purging of dogs with arecoline acetarsol nation of stray dogs (85. By 1981 ovine CE prevalence was 1. midine hydrochloride and from 1977 was A public health education programme was replaced with PZQ every 6 weeks. The first local human 100.). dog-dosing owned dogs. . present sporadically in livestock in 21% of vil- nent measures remain in place. Ponting. together with strict slaughter were paid for by owners initially.. no human CE the Hydatid Eradication (Dogs) Order 1981. The last human CE case Following a reappraisal in 1993–1996.4% and deaths to the Department of Agriculture. in older sheep by 1978. the annual surgical CE inci- 1969 slaughter records showed a prevalence dence on the island of Cyprus was 12. and Elimination in Dogs 221 with positive dogs were quarantined under kept echinococcosis at very low transmission strict State legislation (Beard et al. 1993). Two small outbreaks of CE supervised dog treatment with PZQ. Both may lance through meat inspection and restric- be associated with import of infected dog(s) tions to parasite re-entry (Gemmell and from the mainland (D. in addition. Ponting. pers.e. and dog prevalence (ii) coproantigen tests applied periodically to dropped from >12% to 0. sheep in 1941 (probably introduced).4% to 0. granulosus (sheep G1 genotype). 1998. that is. In Cyprus. ences in the duration of the ‘attack’ phase These options were further outlined by Craig between New Zealand and Tasmania (34 and and Larrieu (2006). programmes themselves and their duration impact. in parallel he described four phases of imple- required 10–30 years for human CE incidence mentation for hydatid control programmes to become negligible. within from the 19th century was largely based Argentina. and Cyprus. were activated by the differed. ment in livestock husbandry and dog based in New Zealand from the 1960s and management.1% PZQ from 1977 and has maintained this to coproantigen prevalence in dogs surveyed the present (2011) (i. measures were reapplied coupled with an owned-dog arecoline test- from the mid-1990s by the Department of ing programme (with euthanasia of positive Veterinary Services that included: (i) treat. and (iv) prosecution for strong ‘consolidation’ measures based on illegal slaughtering. this was in large part due to differences in control structure. granulosus or T. which 1980s in ‘continental’ regions. . later under the direction of the Ministry of or there are unfavourable epidemiologi- Agriculture. required about 110 years.. (iii) movement Services in Cyprus subsequently re-applied control of all animals. The Falklands programme used Department vey in 1997–2000 revealed 2. 1998). using mobile laboratories. Spain. 34 years in a PZQ- from Northern Cyprus (non-GCA) (Christofi based attack phase). In order to prevent a re-emer. Decision may be tem- infection. Falklands. Brazil. cal features (e. and Cyprus island programmes. 2002). a coproantigen ELISA sur. In contrast. the hydatid control programmes control programme. All five ‘island programmes’ were success- that were to virtually eliminate human CE as ful in significantly reducing or eliminating a public health problem. Economides and Christofi.g. At least seven other human CE as a public health problem. With respect to differ- (Gemmell. and Kenya. with an 8.e. Dr Michael Gemmell. other programmes hydatid control programmes were initiated following the success of the Australasian. 1998. dogs) rapidly reduced transmission within ment of all dogs with PZQ 2–3 times per year. change. The Department of Veterinary (ii) elimination of stray dogs. For former involved a Hydatids Council with example. and was only structure and funding are not available. Lembo et al. 2002). Tasmania. livestock surveillance and quarantine from antine was applied only after at least 3 years 1993. 11 years. The control programmes of variable duration. Release from farm quar. The Icelandic programme. a draconian stray dog elimination scheme gence of human CE.. respectively). This enabled him Islands. which all eventually to formulate five ‘Options for Control’. such health dose dogs with a centralized national testing data are not available. techni. Chile. assessed and reviewed of New Zealand. the Falkland all the Island programmes. 1990. Furthermore. and success. absence of E. Gemmell and Roberts. In closely involved with their national hydatid contrast. on health education and general improve- Wales.222 T. The • Option 1: Decision not to proceed. and or immediately targeted the dog population.8% positives in of Agriculture-supervised dog dosing with >6500 dogs tested in the GCA. hydatigena cysts at meat inspection (Economides et al. Options for echinococcosis control programmes Success of island hydatid control In the second half of the 20th century. and porary until the situation/priorities then quarantined farms with infected dogs. because human CE is not a local authorities employing technicians to priority public health issue. 10 years. an under-developed cal officers of the Department of Agriculture region with dispersed population and tested dogs directly on site for evidence of no abattoirs). from 1971 et al. suitable control station to identify infected dogs. Uruguay. in Tasmania. annum to 19. and based on elimination of stray dogs and • recommendations for construction of euthanasia for arecoline test Echinococcus- basic infrastructure in cattle and sheep positive owned dogs (e. nated slaughter area. and zation models for the Control Authority. upgrading of abattoirs and (similar to programmes in Tasmania. 10–15 ranches/estancias comprising desig- years). Craig Honorary Hydatids Commission under the and Larrieu.g.2). and canine echinococcosis prevalence was reduced to From the early 1980s. In reduced further to 11.000 by 1984. and impor- CE-endemic region. The ‘attack’ phase in . granulosus. and the Falkland Islands). required 30–100 years). dogs to viscera. with reliance on own. hydatid control activities (since the late 1990s) • Option 3: ‘Vertical’ long-term approach in South America have been based on: incorporating at least annual on-site • registration and PZQ treatment of dogs arecoline purge testing of dogs by vet- at the dose of 5 mg/kg every 6–8 weeks. with specified regular (usually 4. The Neuquén Province (Argentina) (Craig and Larrieu. and Elimination in Dogs 223 • Option 2: Implementation of a long-term jurisdiction of the Ministry of Public Health. Control. ‘horizontal’ approach involving health Chile opted for the Ministry of Agriculture education. hydatid control pro.000 by Uruguay they opted for a ‘New Zealand-style’ 1992 (Gemmell and Roberts.000 per Chile. • legislation for the regulation of dog pop- • Option 4: Vertical ‘fast-track’ approach. while in Argentina ers to treat dogs with free wormer (e. losus transmission in the first 5 years (from • Option 6 was additionally recommended 1979). significant control and cessation of new quency of PZQ dog dosing (e.g. 10–15 outset with evidence of reduction in E. owners. and pit for disposal • Option 5: Vertical ‘fast-track’ approach of infected viscera. With minor local differences. 2006) as a ‘fast-track’ pilot programme from 1970 resulted in approach based on a specified lower fre. or 8 times per year) treatment of all registered The Chilean hydatid control programme dogs with PZQ (e. meat inspection. 1. drove canine prevalence to < 1% continental regions in Uruguay by 2002 (Table 12. erinarians with associated education of • accompanying health education. ulations. Zoonoses Prevention. to date (2010–11) this strategy or human CE rates over the first 20 years of has been modelled but not yet fully/ the control campaign (1972–1992) when it adequately implemented in a specified was based on arecoline testing. In Region XII (Chile).g. Tasmania. with distinct organi. New Zealand after in Region XII was very successful from the 1990. and similar to Chile and Argentina. tantly failed to reach more than 60% of rural dogs. Thereafter from 1994. granu- years). Cyprus. 2–4 times human CE cases after 17 years. and Argentina.g.g. Human CE incidence in South America in regions of Uruguay. also decreased from >40 per 100.6% within 5 years (1979–1984) of imple- grammes based on the systematic supervised mentation of PZQ dog dosing for hydatid dosing of dogs with PZQ were implemented control (Table 12. 15–30 years). In contrast. 6.2). a 6-weekly dosing pro- Successful and problematic hydatid gramme with PZQ and a higher dog popula- control programmes in tion cover. Falkland Islands after 1977. 2006). per year) in parallel with vaccination of the Uruguay national hydatid control pro- sheep (using EG95) against E.8 per 100. and resultant on-property quar- • slaughter control to prevent access of antine of Echinococcus-positive dogs (e. 1998.6 per 100. ovine CE prev- South American hydatid control alence had declined from >60% to 25% programmes in sheep (with 1% in lambs). trol authority. Cyprus. the Ministry of Health was the overall con- Iceland and New Zealand programmes. gramme had little effect on either livestock However. 2006). However.9 Ovine 61 18 Region XII 1982–1997 5 PZQ Ovine 60–80 25 5–7 Dogs 71 1. Jimenez et al. Within times per year in two of the three regions. 1997). but from 1987 dog dosing was (1983–1989). 2002). Ovine 52.2.9.014 Rioja 1987–2000 5 PZQ. 1996.3 20 Dogs 7 0. Table 12. Spain sus over 10 years (Conchedda et al. 2002). were gramme did not significantly reduce either undertaken in endemic areas of Western dog or ovine prevalences of E.224 T.2 Uruguay 1994–2002 (3) 5 Arec.5 Arec.2 8.02 0.0002 Arec. though this was only maintained for the first quency from 2 to 8 times per annum (>90% 6 years in La Rioja and mid-Wales.7 0.9 0. Lembo et al. 1. In that regard they can the eight treatments per year schedule (half be considered to have adopted Option 5 by dog owners themselves) in Region XII (see above) as a relative fast-track vertical in order to further reduce transmission to control programme. and Sardinia. PZQ = praziquantel. never- dogs were treated). reduced from eight times per year to twice. in La Rioja. CopAg Dogs 4. PZQ Ovine. Italy (1987–1997).. Despite an accompany- ing strong health education component the Sardinian programme was poorly accepted by rural sheep farmers. culling Ovine 82.06 Cyprus 1971–1985 4 Culling Arec Dogs 6.8 0. mid-Wales. 2006). 0) NZ 1959–1997 (2) 5 Education. . 41 9 Dogs 10 0.6 Ovine 66 0. theless it was able to reduce canine echino- granulosus in dogs and lambs in Region XII coccosis prevalence by >90% and ovine CE was reduced close to zero by 1994 (Craig prevalence by 50–75% (Palmer et al.7 0.6–25 0 9 NGA = non-government controlled area. Supervised dog dos- sheep which had plateaued at a prevalence ing with PZQ was implemented at eight of 5–7% after 1986 (Gemmell. Outcome (% or incid. and Larrieu..) years Main Main Programme Dates Option approach a screen Pre 10 <20–30 >30 Iceland 1863–1960 2 Education Autopsy 22 (5. These intervention programmes included annual treatments in order to save on costs the requirement of registration and regular and improve logistics. Chile Region XII lasted a total of 18 years (1987–2000).8 0. the prevalence of E. United Kingdom (1979–1997). Island control programmes for cystic echinococcosis (CE) (After Craig and Larrieu. PZQ Ovine 48–58 04–15 1×10−6 Dogs 37 <5 0 Tasmania 1965–1996 3 Education.6 0. Arec = arecoline. and the pro- in which dogs were primarily targeted.6 Rio Grande 1983–2000 5 PZQ Ovine 26 3 Dogs 28 9 Wales 1983–1989 5 PZQ Ovine 23. Quarn Dogs 12.. in 1991 the dosing of owned dogs with PZQ as the key Chilean Ministry of Agriculture re-introduced intervention tool. granulo- Europe from the 1980s.5.7 Rio Negro 1980–1997 5 PZQ Dogs 41 2.5 10.17 2. 3 years of the increase in dog-dosing fre. as was the control European hydatid control programmes authority and its operatives (the Sardinian Experimental Institute for Zooprophylaxis At least three hydatid control programmes was the agency involved). ... Zinsstag mass euthanasia. eutha. After control veterinary facilities. 1984). 6-weekly supervised PZQ dosing of owned In the Nilotic Turkana tribe in north- farm dogs (in this case by Ministry of west Kenya.6–25% in farm dogs • virtually no educational. and are almost always 0. organization. hydatid 2008 (Palmer et al. but had increased to 6. NGO) (Macpherson et al. ranged between 4. and hepatic CE prevalence by ultrasound posal of sheep carcasses. scav- nasia was replaced early in the programme enging) and companionship. also provided availability of Nilotic tribes in East Africa) or low seasonal necropsy-based dog data on E.000 per annum of burial pits/metal containers for safe dis. the effect with few settlements. per annum were examined post-mortem and Both humans and their livestock populations showed a prevalence reduction from 7% to are interdependent. and widespread from 5% to 9%. the mid-Wales hydatid monitor progress in hydatid control in such control programme (1983–89) involved pastoralist societies. 2005a. alpine grasslands of prevalence. Mongolian. ginal lands with low rainfall (e. 2005).. guarding. These communities inhabit mar- apart from reducing the potential transmis. and are also fiercely independent with coverage of owned farm dogs. along with poor anthelminthic ices. Buishi et al. by contrast. 1996.. 1995). gran. for human food. and road network 1989 due to budget considerations. 1997). and to health. and reached a plateau at 8–9% from 2002 to Despite these inherent problems. Control. 2002). Nomad groups are usually palities to impound and treat stray dogs geographically isolated and have poor access indefinitely. bitch sterilization. age. . intervention attempted to comprise elements Mastin et al. • no abattoirs. This makes hydatid control programme (Craig and it particularly difficult to implement. of 5 years of PZQ dosing on canine echino. human CE surgical incidence Agriculture veterinarians). Euthanasia of stray dogs. coccosis prevalence was measured using a • a population of nomadic and largely laboratory-based faecal test for detection of illiterate indigenous people. and education serv- contributed. and Elimination in Dogs 225 The La Rioja hydatid programme was man. 1980).5% to 10.e.5% within a 3–4 year period. In La Rioja 500–1000 stray dogs Tibetan. dog culling.3% (by 1996) Wachira. Arecoline purge prevalence of canine echi. but became a difficult issue for public of the world’s nomadic or semi-nomadic pas- acceptance in relation to implementation of toral societies (Macpherson. and to As for La Rioja. measures were prematurely disbanded in • poor communications. Echinococcus coproantigens (copro-ELISA) • occurrence of frequent droughts. communities Significant stray/unwanted dog populations in La Rioja and Sardinia were Human CE is a common. to the failure characteristic disdain for formal government after 10 years of the (well-funded) Sardinian organization and their operatives. or (Walters and Clarkson. administered by the African Medical and from the Welsh control zone reduced from Research Foundation (a non-governmental 23. value (i. though under- considered an important reservoir of E. hunting. 2011). et al.2% after 10 years of dog dosing (Jimenez associated with dog ownership for practical et al. Ovine CE prevalence for sheep CE. this became unsustainable. 2006). granulosus temperatures (e. of Option 4 (i. In Sardinia. but almost never by legally binding legislation for munici.e. difficulties included: nococcosis in the 1970s prior to control. medical. arid zone sion reservoir. involve community participation. From the start in 1983 of a health education in local communities and Turkana-based pilot control scheme against schools. Zoonoses Prevention. veterinary. 1994. the construction was more than 200 per 100. and (Craig et al. Hydatid control in nomadic pastoral aged under the Ministry of Health. Kazakh pastoralists)..g.. man- Larrieu. recognized public health problem in many ulosus. herding.g. Canine coproantigen • commonplace inter-tribal livestock prevalence in the control zone was 0% in raiding and fighting (Macpherson and 1993. but a significant using necropsy of unwanted dogs and areco. Planned dog dosing six times per ity after consideration of hospital treatment . and bovine eastern Tibetan Plateau (located 3500–4500 m TB). The campaign operated ‘on and et al. human CE is of major Echinococcus coproantigen survey of owned public health importance in these groups and dogs in the Turkana Control Zone in 2002 should be targeted by health and veterinary showed that coproprevalence (31%) was still authorities. Li et al. 2006).. Lembo et al. In addition human screening by off’ for about 10 years (1983–1994). lem is to develop an integrated approach to nificantly reduced (Buishi et al. and complication in this region was the high coen- under-funding meant that only about 30% of demicity of E. because logistic reasons was reduced to 3–4 times per formal slaughter houses did not occur (Yang year or less. then for dogs and necropsy of unwanted dogs. together with health CE is usually made by a public health author- education. 2005. An munities. and of caused an equal or higher community preva- those only between 30–60% were followed up lence (compared to CE) of human alveolar regularly for PZQ treatment (Macpherson et al. tion of livestock. reduction did not occur in necropsy data for line testing of owned dogs. effectively bundle together several zoonotic nomadic pastoral populations living on the (e.. 2009). Mobile teams visited village to use an anti-CE vaccine (EG95) in sheep and clusters as well as temporary nomad encamp. The decision to reduce incidence of human tion of accessible strays). preventable childhood infections).. Around 25% of ultrasound abdominal scanning for human this Tibetan community did not readily accept CE. and also China) ranged from 1% to >15%. In Datangma district. significantly from 50% to 17%. and was 27% after 11 years in nomadic or semi-nomadic pastoralist com- (1983–94) (Macpherson and Wachira. An additional difficulties in transport and manpower. Echinococcus spp. The ‘attack’ phase based lar to Turkana (Kenya) described above. However. as planned. strengthen both human and animal health sys- Investigations from the mid-1990s showed tems (‘One Medicine’). brucellosis. 1997). Surveillance. and health education) and Option 5 (specified annum was found to be unworkable due to 6-weekly treatment of dogs with PZQ) (Craig the severe winters. 2005). Nevertheless. and non-zoonotic diseases (e. (Schantz et al. and there- control pilot in northwest Turkana. simi- ments (manyattas). human. 2010). Prevalence estimated by necropsy of There are huge difficulties in attempting to unwanted dogs reduced from 63% to around control the transmission of cystic echinococcosis 45% within 5 years.... Human EG95 antibodies revealed that at least 50% had prevalence then appeared to plateau around not been vaccinated. multilocularis in dogs which dogs were registered in the first 2 years. with very few serological testing of livestock to measure cases in the under-5 years age group. Macpherson and Wachira. Ganzi Tibetan Autonomous Prefecture (Sichuan Province) a pilot hydatid control scheme was implemented from 2000 Planning and implementation of CE control to 2005 and included twice-yearly PZQ dos- ing by owners of their dogs (and a propor. together with mass stray dogs (Yang et al. which could more cost- that human CE prevalence in Tibetan semi.226 T. ultrasound was implemented. though average worm burden was sig. After 5 years of twice- 1986.g. echinococcosis (AE). In addition. human fore the percentage of animals treated or vac- CE prevalence based on ultrasound scanning cinated was never more than 30%. 2003. 1997). 2006). Due annual dog dosing.. surveillance was LISA prevalence in owned dogs reduced based on dog and human prevalence surveys. One possible answer to the prob- high. coproE- to absence of livestock data. 2006).g. reduced from >7% to <4%. rabies. or allowed the vaccina- 3% after the mid-1990s (Craig and Larrieu. Within 5 years of the start of the hydatid dog dosing or livestock vaccination. CE. vaccine- altitude in Sichuan and Qinghai Provinces. An attempt was also made and Larrieu. yaks with annual boosters. was on PZQ dosing of dogs eight times per year based primarily on coproELISA testing of was maintained for the first 2 years. 2009). and were lead to better outreach and acceptance by pas- among the highest ever recorded worldwide toralists (Zinsstag et al. Attack phase • Control measures against E. and Elimination in Dogs 227 records or data from mass screening sur. disease. and/or PZQ baiting of stray dogs. the Ministry of programme may then be considered.g. an annual decision should be data collection and potential quality/ made to continue (‘attack’ phase usually reliability of surveillance data. • Identify liaison avenues between veys. or NGO an Honorary Hydatids Commission. There may also be cooperation or col. • Reduction in stray dog numbers if a prob- • Assess the public health impact of human lem. safe dis- • Calculate the economic losses due to posal of livestock offal. Implementation of a hydatid control the control authority. livestock (sheep) within • Identify key staff and needs/training 5–7 years. principally to involve dog regis- tration. Control. a Department of Municipalities.g. Transmission to advisors. and human CE rates (<15 years (veterinary and technical staff. and participatory livestock and human CE. and also a • Consider whether transmission is signifi- dog-surveillance approach (arecoline cant enough to designate CE as a notifi- purgation and/or coproantigen testing. CE and its priority for regional public • Parallel health education about hydatid health. prevalence. ideally by trained operatives. requires 10–15 years). horizontal versus vertical This is the most costly phase in terms of approaches. removal • Establish cooperation with local/rural of old sheep (>10 years) with compensa- groups (e. and Agriculture/Department of Veterinary may be facilitated by a Ministry of Health. the a Ministry of Agriculture. and establish the feasibility of authorities. Craig and Larrieu. and municipal logistics. university. intervention should be communicated to • Assess operational research needs and relevant veterinary. NGO. quantitative epidemiologists. regional level. including itself at community and school levels. cific government. control and of the different control options (e. health. tion should be implemented. Options 1–6 above). acceptance of the control programme • Identify the control authority. These are outlined below. or an research/health agencies. phases (Gemmell and Roberts. . voluntary farmers’ unions. and if appropriate spe- Veterinary Services. its legislative powers and funding com- • Set-up of abattoir/slaughter slab sur- mitments (preferably long term). Hydatid control has been infectious diseases in general (planning recommended to be broadly divided into four phase needs 1–2 years). of sheep has elapsed. • Consider whether CE control can be inte- laboration between the various authorities. and canine echinococcosis >90%). the parasite life cycle. If feasible. a local Municipality. 2001. veillance for specified areas. expenditure and manpower and therefore • Consider the role of education for should be as short as possible. 2006). Services. WHO/ OIE. Zoonoses Prevention. the Ministry of Health. medical age group) within 10 years. grated for improved cost–benefit with such as those managing public health and control of other important zoonoses and veterinary aspects. for example oxfendazole. • Possible application of anthelmintics for • Undertake a cost–benefit analysis for livestock. cant within 1 year.). granulosus are Preparatory or planning phase applied. A reduction in local needs/knowledge/socio-cultural dog infection prevalences should be signifi- aspects. Results of the livestock herders). able disease at national or provincial/ necropsy of unwanted dogs). 1998. and then specified regular mass • Assess the quality of baseline data on treatment 4–8 times per year with PZQ of human and livestock CE incidence and the entire owned rural dog population (or prevalence. dogs will only cease after 1–2 generations etc. is This is a long-term phase after the expen. tant on-site educational tool for dog owners. It was used to great effect in tal programmes). echinococcosis. and random surveil. until tion in field staff and the cost of anthelminthics the mid-1990s arecoline purgation was the (consolidation phase needs >20 years and may only reliable and practical test for canine need to be more or less permanent in continen. hydatigena). including Echinococcus. using stray or unwanted dogs (and may be • possible provision of PZQ to dog owners facilitated in cooperation with rabies con- free or at low cost. The definition of elimination or The development in the early 1990s of eradication of E. granulosus. and is labour-intensive sive ‘attack’ phase. and mid-Wales. difficult to implement. because of positive intervention surveillance indicators (i. espe- cially notably those carried out in Tasmania. • possible use of enforced dog treatment Post-mortem examination of dogs is the gold and legislation to quarantine affected and standard for detection of the adult tape- neighbouring properties (with a specified worm of E. 2006). ideally Canine echinococcosis with trace-back ability. 1992). for example. or initiated. granulosus is nor- • possible recommendation to remove old mally only around 70% and up to 25% of dogs sheep. (Craig. was evalu- such as dogs or livestock through use of a ated in the 1970s and found to be highly effec- licence or passport (this is easier on islands). 1997). and purgation also can provide an impor- • possible prosecution for illegal slaugh. nal worms. The widespread stopped and active consolidation reduced. applied to prevent entry of infected animals PZQ. if re-emergence of transmission occurs 1992. availability of the anthelmintic PZQ from the However. Allan et al. It involves: echinococcosis • proactive identification of infected food animals at abattoir meat inspection. multilocula- to control limited outbreaks on specified ris at a single dose of 5 mg per kg (Gemmell infected properties should be maintained and Johnstone. Control tools and surveillance for livestock. Deplazes et al. The great advantage centralized slaughter records are difficult of arecoline is that it should be 100% specific. tive (>98%) by both oral and intramuscular The ability to trace back from abattoirs. but it may be required the ante-mortem diagnosis of canine echi- to readopt broad consolidation measures nococcosis (Allan and Craig. granulosus for a specified a highly genus-specific coproantigen ELISA territory becomes an important issue. but such an approach period free from CE and possibly also can usually only be applied for surveillance T. particularly if if purges are examined. and there- • possible use of sentinel lambs and/or fore is used as an ante-mortem diagnostic test cattle to assess exposure. New Zealand. Coproantigen . and measures gation as the main tool of the ‘attack’ phase.e. to obtain. and should require a reduc. dogs. Consolidation phase (as occurred in Cyprus. where hundreds of thousands of dogs were arecoline tested In this phase. Maintenance of elimination phase New Zealand. vigilance should be maintained 1980s replaced the reliance on arecoline pur- through meat inspection.228 T. Arecoline is a strong purgative that may lance of dogs by coproantigen tests or eliminate a large proportion of gastrointesti- arecoline purge testing. granulosus and E.. Arecoline sensitivity for E. in the 1990s). 1989. specific control activities have (Craig and Larrieu. Lembo et al. and Cyprus. fail to purge. with its very high efficacy. This phase occurs after dosing dogs in the attack phase has ceased. humans). is potentially biohazardous for operatives. Despite these drawbacks. it may also be stressful for dogs. 1981). several hydatid control programmes. and routes against E. trol). This provided the first useful laboratory test for is a permanent phase.. tering (if appropriate). 2009). However.8% (Mastin et al. infections by 2 wpi (weeks post infection)... Rio Negro (Argentina).2% in 303 dogs had reduced to 0% . Lopera et al. 2. a potential re-emergence of transmission respectively. and to establish the time or coproantigen-positive (Reichel et al. unpub.. is lower than coproantigen but was able to detect pre-patent juvenile detection (Lahmar et al. dogs were reinfected as determined by areco- Wales zone remained at 8.. granulosus spp. 1.. however.. 2007. B... Coproantigen ELISA has An important consideration for endemic already been used for surveillance purposes canine echinococcosis in both baseline pre- in at least four hydatid control programmes. P. coproantigen baseline prevalence of around 40% exhibited prevalence had increased to 8%. 2003. information can be very useful in considera- lation in order to identify the remaining foci tion of an optimized cost-effective dog dos- of infected sheep farms. is to deter- Falkland Islands in the mid-1990s the test was mine natural reinfection rates in dogs. granulosus reinfection in dogs of serum antibodies with current infection (Craig et al. 1995. and where E. Test sensitivity was more variable 2004). 2000) (Table 12. ment.004% (n=563) tion may re-emerge. infection pressure in ‘attack’ and ‘consolida- Wales. In theory. 2003). Craig.7% of dogs were ing regimen. Buishi et al. Despite this. and by 8–9 months 10–21% of 2009 the coproantigen prevalence in the mid. Buishi et al. Cyprus.8% were copro-positive in a low A single PZQ treatment of dogs should elimi- prevalence zone. 1995). 2005b). serological diagnosis of canine echinococ- cosis.. In was 0% in the control zone 4 years after ces. In PZQ treatment.. 2000).. Such used to screen about 50% of the dog popu. baseline arecoline prevalence for E. Stefanic et al. 2008). approx- 6-year hydatid control programme (1983–89).e.. within 2 months after a single (Palmer et al. 1995. Coproantigen trol. granulosus and E. Boufana et al. Boufana. dogs (each >470 dogs) with an arecoline test 13 years after the attack phase. signalling reinfection prevalences of 0. line purgation (Larrieu et al. Of these. coproELISA prevalence in sus of 13. granulo- Echinococcus spp. frozen. PCR sensitivity for Echinococcus infec- with low worm burdens (< 50–100 worms).. multilocula- detection was also shown to be superior to ris are co-endemic (Craig et al. intervention studies and for assessment of namely the Falkland Islands. In Datangma (Tibetan Sichuan) after Similarly. Zoonoses Prevention. imately eight times per year) to prevent new Coproantigen prevalence in Welsh farm dogs infections establishing (WHO/OIE. collected (Yang et al. especially days post treatment (Allan et al. Control. Jenkins et al. or arecoline purge indicated specificity of DNA in faeces has shown great promise as 91–98% and sensitivity of 62–100% (Craig a species-specific confirmatory tool for dog et al.8% and 3.e. tion. In the tion’ phases of hydatid control. granulosus worms to produce a 0% were treated with PZQ (Christofi et al. two cohorts of farm sation of supervised dog dosing.. Similarly. Comparison The more recent development of copro- of the coproantigen ELISA with necropsy PCR tests for detection of E. 1992. mid. and Tibetan Sichuan (China)...S. per rectum or from the ground. or owned dogs had reduced from 50% to 17% formalin-preserved faecal samples. dogs should Wales was employed to assess the impact of a therefore be dosed every 6 weeks (i. 2002). prevalence within 6 weeks post treatment (i. granulosus reinfection rates in dogs were screened between 1997 and 2000 dogs following a single deworming treat- in the consolidation phase of hydatid control. the pre-patent period). in Cyprus > 6500 owned assessed E.. infection (Abbasi et al. and Elimination in Dogs 229 testing can be performed on fresh. 1996.. Ponting. By period after cessation of dog-targeted control 2010 the coproantigen prevalence in Falklands measures that canine echinococcosis reinfec- farm dogs had reduced to 0. 2011). 2001). 1996). 2003. mainly because of the poor correlation E. few epidemiological or control studies have lished). a 5 years of twice-annual dog dosing with PZQ. DNA detection may be best applied for and dogs became copro-negative within 4–5 confirmation of coproantigen tests.5%. 2005a). relatively (S. or after cessation of mass treatment.3). and copro-positive dogs nate all E. Coproantigen testing of farm dogs in mid. Craig in the ‘consolidation’ phase of hydatid con- et al. in Florida Department (Uruguay).. 190 18 Arec 0 5 22 Shiqu (China) 6.6* 1..0 Florida (Uruguay) 2. Wachira et al.8%.8 3... for example as applied in Chile 1.6 6.. dog trol impact and if necessary adjust dog dos- prevalence (by the arecoline test) stayed at ing regimens. granulosus endemic areas.6% ignated abattoirs/slaughterhouses. PZQ = praziquantel. Larrieu et al. Welsh Assembly Government. Other over the following 12 months (A. every 8–10 weeks) to reduce the those caused by Cysticercus tenuicollis (= Taenia possibility for dog reinfection. Lahmar et al. and adult sheep) other control measures). Brouwer. 2008–9.3* 2. 2004. 1990.6–5%. and Li. camels. 8 times per year (i. 6. E. unpub. later (Gemmell.5 3. In the Chile hydatigena). 2000. especially in lambs (where cysts Region XII hydatid control programme.9* 0..3. yaks may also be monitored. unpublished) (Table 12. However. X = times dosed. such as per year (i. unpub. approximately Sheep data should be collected at baseline 2–7% of owned farm dogs become reinfected and annually for three different age groups by 3–4 months post PZQ treatment (without of sheep (lambs. every 6 weeks) for 7 years 1995). will be smaller and may therefore require his- dog dosing with PZQ was maintained at tological or DNA confirmation) (Cabrera et al. age of slaughter of large ungulates reduces gest that in some high or even moderate the short-term (1–5 years) use of these data. 4. 303 13. 2007–8.e.. and preferably 5–6 times to differentiate CE from other lesions. 1996. and increased further to 18.4 18. ment. Lembo et al. PZQ dos. Moss et al.7–9.7 Turkana (Kenya) 5. granulosus reinfection levels in dogs after treatment.9 10. and ovine CE prevalence remained Region XII (Vidal et al.3). 3. programmes is usefully measured by ovine treatment. Follow-up period (months) prevalence (%) Pv% Region (country) Ref n Day 0 Drug (x) 2 3–4 8–9 12 >12 Rio Negro (Argentina) 1. Annual ovine CE prevalence data will (1979–1986).9% The medium-term impact of CE control 3–4 months later.6% at 8–9 months (Cabrera et al. re-emergence occurred CE prevalence at meat inspection in des- in Wales with a copro-prevalence of 1. 7. but the older These dog follow-up observations sug. E. Cabrera et al.3 16. .7 21.e. but canine echinococcosis close to 0% by 3 years rebounded to 5. 2 months after a single PZQ treatment. Arec = arecoline. livestock such as goats.3 Arec 0 3. Abattoir inspec- at 5–7%.4% at 3–4 months post treat. Craig. Re-introduction of dog dosing with tion of slaughtered sheep and other livestock PZQ to 8 times per year (in 1991) was success. W. Care should also be taken least 4 times per year..2* 14.2 0 0 Beja (Morocco) 168 4.9 (several) Jendouba 4. 2. and P. 476 42 PZQ(×1) 3.7 PZQ 0 36.9 6. 1994). then reduced to 2 times per year enable the control authority to measure con- from 1987 to 1990 to save costs. 2007. 609 [252–300] 9* PZQ(×4) 1. Arecoline test except CoAg. juveniles. Application of a 4 × 12-week PZQ dosing schedule in ~300 farm dogs in mid-Wales. 1997).6 27. 1996). and 0% at 12 months post. 44 7.3 598 0. 5. Therefore. However.. Farias et al.1* Mid-Wales (UK) 7. for more sensitive variation in prevalence and ing frequencies should be implemented at cyst-intensity rates. resulted in a reduction in coproantigen prevalence to 1.5 6. also provides critical data for transfer from the ful in Chile in reducing both ovine CE and ‘attack’ to the consolidation’ phase of hydatid Table 12.. with a baseline Ovine hydatidosis coproantigen prevalence of 8. 207 2.7–9.5* PZQ(×1) 9.2 PZQ(×1) 0 5.230 T. 329 19.4* 0* 1.9 Rio Grande (Brazil) 3. cattle. 2003. 2002). in north-west Kenya). 2010).. 2000). Zoonoses Prevention. hydatigena infection vention). such as antigen B-ELISA or immuno- hydatid control zone is the most frequently blot tests.g. In Uruguay. trol programmes: Rio Negro (Argentina) ing interval was extended to 12 or 16 weeks and Turkana (Kenya) (Macpherson and (Cabrera et al. In dog-dosing-based campaigns. the ultrasound group for fertile hydatid cyst infection. Craig and Larrieu. but in contrast. Li cant assistance in hydatid control programme et al. exposure to E. slaughtering is done at home or in clandestine Such hospital derived data are.. which are the high-risk the Rio Negro programme. 2001). pital data include: Use of sentinel livestock to detect natural • the detection of asymptomatic cases. Such data retrospectively indicated in sheep can be useful in identifying poten. and health access may data have limited use or are unobtainable. eastern Tibetan Plateau (Craig et al. north-west Kenya and communities of the ciently specific and sensitive to be of signifi. as dog movement/treatment. though success has been limited Advantages of ultrasound scanning over hos- (Njoroge et al. pro- ficult to collect (e. however. 2002). granulosus has been success- • confirmation/clinical status of previous fully applied using lambs in hydatid control cases. The additional opposed to existing old CE cases (pre-inter- use of abattoir data for T. especially portable ultrasound scanners. Frider et al. in a neighbouring area with no intervention).1% over a 13-year period of intervention. vide a more accurate approach for human ultrasound scanning of sheep and goats can surveillance in hydatid control programmes.. 2003). Human cystic echinococcosis/hydatidosis type CE 1) (Larrieu and Frider 2001. if community level using imaging techniques. slaughterhouse data are unavailable or dif. However. Trace-back of infected animals can be Age-specific treatment incidence rates for the used to identify suspect farms/properties in under-15 or under-10 years age groups can order to impose restrictions on livestock and also provide data on recent transmission. have not been employed very assessed parameter for public health impact.e. butchers. and therefore centralized abattoir not always accurate. 1. In • early clinical information in respect of Wales. Control. however. 4–18% of veillance in at least two hydatid con- sentinel lambs became infected when the dos. In (>5–10 years of age). one (Macpherson et al. Removal of old sheep Wachira. the positive impact of the Iceland education- tial transmission hotspots or breakdown in focused and the Chilean and Argentinian control (Economides and Christofi.5% to population.. study to determine optimal PZQ dosing fre- quency found that sentinel lambs were not Ultrasound-based screening in CE endemic infected (0%) when a 6-weekly dog dosing populations has been applied for sur- regimen was used. characteristic hydatid cyst pathology at ultrasound indicated that 65% of cysts were of the ‘early growth’ type (i. programmes in mid-Wales and Uruguay. or by contrast many endemic areas. extensively in surveillance of hydatid control . • longitudinal data in follow-up. be poor for under-developed regions such as Serodiagnosis of ovine CE is not suffi. if acceptable to the local 13 years) was shown to reduce from 5. subject to full control (PZQ and education) • the true age-specific prevalence of over the previous 5 years (compared to 10% abdominal CE. and Elimination in Dogs 231 control..000 population for a tests. may prevalence of CE in children (aged under also be a control tool. be assessed. 1997. 1998). furthermore.. 6% of sentinel lambs became infected treatment options and natural history of within 15 months from exposure in an area disease.. Active mass-screening surveys at surveillance (Craig et al. 2003).. most livestock the failure of hydatid control in Sardinia. The use of annual CE surgical/treatment Serosurveys using sensitive and specific incidence rate per 100. and indicating continued transmission from dogs • an educational effect for rural communities to sheep (Lloyd et al. 2006). . because it provides a of lambs/sheep with only twice-yearly PZQ route for community participation and ulti- dosing of dogs. One effective strategy could be tant component of many successful hydatid to combine spring and autumn vaccination control programmes. for over 60 years or more the rural popula- nated ewes (Lightowlers et al. Heath tion changed its behaviour regarding home et al. worm development. and also to ensure that a suffi. slaughter and dog contact). there is little The EG95 vaccine provides the poten. and tion in Iceland in the 19th century (where for up to 3 months in lambs born to vacci. 2006. However. and was applied vaccination regimens with or without dog in the Rio Negro programme (later replaced deworming is strongly recommended by by ELISA) to identify exposure in children. 12-week dog-dosing regimens for 5 years or more. . 1996). health education oped (Lightowlers et al. dog dosing). 2003. multicentric trials combining different EG95 ies in the Falkland Islands. 96–100% protection against E.or viable option. Lembo et al. education is an impor- grammes. Nevertheless.232 T. use of hospital and/or models showed that a 75% vaccine cover of ultrasound-based data sets were preferred sheep. indicate possible effects on worm burden. 2006). so and structures interpretation of vaccine efficacy was not robust (Torgerson. granulosus would provide a major intervention tool for hydatid control Several hydatid control programmes have programmes. granulosus (Zhang et al. livestock husbandry measures. dog numbers used were small and dogs were necropsied before patency at 26–45 days Other hydatid control measures after challenge (with protoscoleces). Education/training of tion) indicated that vaccination of sheep slaughter personnel and veterinary techni- alone could be highly effective if >90% of cians is therefore also important for success- sheep are protected. the ful implementation and data collection. ing would have an equal effect (Torgerson tus. Simulations of transmission mately acceptance of medium. however. positive cases (false positives) without clini.. Petavy Craig. with to production of antibodies that resulted in resultant decrease in transmission. Trials showed about the life cycle and transmission of that two subcutaneous injections in sheep of E. and worm fecundity cal or image confirmation of CE (Rogan and of E.. However. 2008). ures (e. granulosus (Craig and Larrieu. Undertaking definitive screen human sera for Echinococcus antibod. coupled with twice yearly dog dos- because of their less equivocal diagnostic sta. More realistically. programmes. Education ciently high proportion of dogs are treated. In experiments. and vaccination of sheep. The DD5 agar test was. 2003). A functional dog Vaccines vaccine against E. particularly regular dog modelled (involving PZQ treatment of dogs. 2002). et al.. WHO (2011b). however. dosing. but significantly more research had poor impact. direct evidence elsewhere of a marked effect tial for implementation of a more rapid of health education alone in reducing trans- and cost-effective attack phase in parallel mission of E. human serological testing alone Experimental recombinant adult worm without ultrasound remains controversial vaccines against canine echinococcosis because of the tendency to create a list of sero. granulosus could lead to a change in the EG95 vaccine with Quil A adjuvant lead behaviour of dog and livestock owners. used to and Heath. 2003). 2008). because of difficulties in is required before this can be considered a maintaining the accepted standard of 6.to long-term in which hydatid control interventions were vertical measures. granulosus egg apart from the historically unique situa- challenge infections for up to 12 months.. Rather.g. A recombinant oncosphere vaccine (EG95) In the absence of vertically directed meas- against ovine echinococcosis has been devel. annual surveillance. and/or health educa. with dog dosing for hydatid control pro. testing. ment include: 5. but significant incident rates remained or animal infections Analysis of previously successful hydatid re-emerged after cessation of intervention programmes indicates the need for specific leg. usually with animal populations. oxfendazole). authority (especially if led by a Ministry of • better livestock surveillance through Agriculture or Veterinary Services) implements lesion identification (e. dog registration. ‘attack phase’ period and for achieving a per- 3.g. dogs.to long-term (5–10 years) vertical tion) at meat inspection. and by accurate campaign directed at treatment of owned rural ante-mortem serodiagnosis. and the leishmaniases Since the first control activities for cystic echi- nococcosis took place in Iceland in the 1860s. and Uruguay. if an integrated approach is used. 2006). Zoonoses Prevention. funded mainly by dog trol programmes have significantly reduced owners. • development of an effective dog echinoc- dog. prohibition of illegal slaughtering. For continental regions. dogs between infected and ‘free’ areas (Gemmell • application of effective anti-hydatid and Roberts. programmes. Nearly 150 years of hydatid control pro. control of movements of food animals and frequencies. In oth- such as a Ministry of Agriculture or Health. An NGO with funds from donor agencies. and human populations. This specific and sensitive on-site detection of is particularly so if a well-managed control dog infection. between veterinary and human health sectors • use of cost–benefit models and control is also important if public health indices and simulation outcomes together with coor- educational aspects are used effectively. Areas for improvement or develop- less dogs. Canine Visceral Leishmaniasis Control Conclusions Leishmania spp. and Elimination in Dogs 233 Hydatid control administration achieved there and reported for only two other and legislation island countries or territories (New Zealand and Tasmania). measures (e. • integrated assessment of vaccines for inter- stock. and treatment of manent cost-effective ‘consolidation’ phase infected owned dogs. reduction in human CE cases. Several hydatid con- government links). after dog-targeted hydatid interventions have 4. bly in Chile. Legislation Kenya. than parasite eradication or elimination in ity (Council or Commission. Argentina. northern islation at regional or national level. anthelmintics for livestock (e. nota- 2. with appropriate surveillance in sheep. evant neglected zoonotic disease control effective than those previously implemented. effective meat inspection and disposal of offal.g. ers. control of strays and elimination of owner. human CE incidence or prevalence rates. Control. DNA confirma- a medium. full or pilot hydatid schemes resulted in 3. Future dination and integration with other rel- programmes may be more efficient and cost. and north-west China). Cooperation occosis vaccine. A national or regional executive author. Sardinia.g. ceased. and mediate hosts with reduced dog-dosing 6. quarantine of premises with infected live. 1998. Leishmania are kinetoplastid protozoan para- the maintenance of eradication has been sites that are the causative agents of human . grammes clearly shows that human CE can • development of diagnostic kits for rapid be eliminated as a public health problem. needed includes: Further research is needed in the 21st 1. elimi- There have been three main administration nation or reduction of human CE as a public models for hydatid control programmes: health problem is a more practical objective 1. A direct government-funding authority. Craig and Larrieu. mid-Wales. century to develop methods for reducing the 2. which is a synonym of and the Leishmania subgenus Viannia. and track origins epidemiological data. • their contact with sandflies. The taxonomy tate during feeding (Rogers et al. which is considered source for sandflies. may be a disseminated • the abundance of dogs. WHO. infantum (and both symptomatic and destruction of the nasopharynx. cutaneous form. infantum and L. niasis (CL). human cutaneous leishma.. zoonoses. has been largely confirmed Leishmania spp. 2000. to be highly infectious to the vector sand. epidemic outbreaks on the Indian subcon- Criteria to incriminate the dog as a reservoir tinent and in the Sudan.) braziliensis due to L. mexicana complex) There is overwhelming evidence that the dog give rise to diffuse cutaneous leishmaniasis is the primary reservoir host for human VL (DCL).. asymptomatic infections are common). 2007. tropica or • the course of infection and accessibility L. with important silvatic or peridomes- sucking female sandflies. 2009). caused by L. with two distinct epidemiologies (see below). The infection is Most of these Leishmania infections are transmitted from the blocked foregut of blood. braziliensis. chagasi. Old World (OW) and the New World (NW). aethiopica in the OW. In the context of this chapter and this volume. except that several subgenus Leishmania. such as of developmental stages in the sandfly vec. Lukes for naming Leishmania spp. of infection to sandflies. • carriage of the same parasite genotypes may be less severe and self-curing. which is L. which can then transfer phosphoglycans. which separates Leishmania from Viannia. donovani complex infections do fulminating fatal canine visceral leishmania- not succumb to the disease. which the sandflies regurgi. particularly on the Indian subcontinent. devastating CL/MCL due to L. 2011a). However. L. especially the diverse and migrations (Kuhls et al. (the latter within the L. mexicana of infection to sandflies. Overtly symptomatic VL is generally consid- the dog is the crucial primary reservoir host ered to be fatal if not treated. infantum (but not for L. clinical presentations of Leishmania infection (Lainson and Shaw. 1990. Human visceral leishmaniasis (VL) is The dog is the primary reservoir caused by the two species of the Leishmania host of zoonotic VL donovani complex. infantum-infected dogs may suffer exposed to L. can tor. aethiopica and L. 2011). which occurs in both the species have proved to be invalid synonyms. 1998. has been based on et al. donovani (Mauricio et al. biological features such as the distribution High-resolution molecular methods. and canine leishmaniases.234 T. 2011a). and the L. infantum. Leishmania infection to humans. as follows: of the Americas frequently metastasizes to cause severe mucocutaneous leishmaniasis • Dogs are readily susceptible to infection (MCL). Quinnell and Courtenay. (V.. with disfiguring and potentially fatal with L. major. L. divided by molecular methods such as multilocus into two different subgenera: the Leishmania sequence typing (MLST).. reveal the population structure of individual together with associated geographical and species such as L. infantum. human VL probable sporadic suburban reservoir host of has been responsible for large. known as post-kala azar • their presence as a significant blood leishmaniasis (PKDL). The taxonomic framework nym of L. although that are found in human infections occasionally L. In contrast. and some infec- sis (canine VL) with both visceral and dissem- tions cause simple cutaneous lesions that inated cutaneous infections. • the prevalence of canine infection. which is a syno- confined to the NW. for example L. Lembo et al. L. multilocus microsatellite typing (MLMT). flies. dono- fully immunologically competent individuals vani). L. A common sequel host of VL include: of treated human VL. Nevertheless. Notably. . The dog is also a do not visceralize. however. have been described. infantum. archibaldi. donovani and L. and complex and the subgenus Viannia in the NW. Many of Leishmania spp. 2009). The infection process tic reservoir mammalian hosts that act as sources is facilitated by Leishmania-secreted proteo. many for VL due to L. amazonensis (WHO. cal epidemics are sustained by the reservoir • the predominance of asymptomatic of human infection. sandfly vector. • Infected dogs are highly infectious to sandflies and this may be true even for In many regions where canine VL asymptomatic dogs. 2009). This is not surprising as VL. even though this et al. months or years.. in the Indian sub- from asymptomatic to fulminating infec. in human infections. as working or hunt- is sympatric with canine VL (although ing animals. occur in more than 50 countries. 2011). 1992. Martin-Sanchez et al. 1999. Quinnell and is its association with L. in which cycli- ment puppies. be entirely an anthroponosis. might have long-term repercussions on the • Dogs have a close domestic and perido. may be a primary impe- • Strains of L. Costa et al. Zaffaroni irrespective of the need to prevent sporadic et al. is endemic. transmission dynamics of VL to the human mestic association with humans. infantum and human Courtenay. in poorer regions. Repetitive. infantum highly as companions. the dog is not a primary on the breed of the dog.. even when high reso. donovani • the range of clinical presentation in dogs. it has been difficult to South America.. encompass- such as: ing southern Europe. and the south-western tions. the east- • the focal abundance of sandfly ern Mediterranean. and Central and vectors. continent. 1996. such as suburban slums in some regions of Nevertheless. and high. dogs. infantum and the zoonotic form of VL there are many potential confounding factors. where L. However. endemic areas) (Paranhos-Silva et al. for example by mapping be very high. 1999. sandflies. 1995. fly bites due to behaviour of inhabitants.. where human cases of VL are rare or for example in some countries around the unknown. and the parasitaemias. nutritional status. correlation between dog ownership and the From a wider perspective the over- risk of human VL (Evans et al. North Africa. immune competence in susceptibility to dant amastigotes are thus accessible to human VL. 1999). and Elimination in Dogs 235 • Parasitaemias in dogs may be very • the role of age. human cases of VL. If owners canine VL is endemic in some regions have a comfortable socio-economic status. particularly PKDL. Slappendel and Teske. particularly in the skin. reservoir host. and of dogs. they can devote con- known of canine VL imported to non. the health of the dog.. siderable financial resources to their dogs. conjunction with abundant sandflies and . VL may be applied. 1999. and • Dogs are fed on avidly by the same sandfly • the varying degrees of exposure to sand- species that bite humans. sustaining prolonged 1999. Cunha whelming reason for the control of canine VL et al. East Africa. and for breeding. Control. population. non-curative therapies for canine lution MLMT is used (Dereure et al. prevalence of canine VL may prove unequivocally. and more than 1000 cases are Mediterranean basin. L... with sustained high • the mobility of humans. Zoonoses Prevention. Thus in India. and abun. The genotypes and phenotypes have been dog may be given frequent and expensive shown to occur sympatrically in dogs veterinary examinations and treatments. China. the dog has no • the rapid turnover of dog populations proven role and the disease is considered to and introduction of susceptible replace. In such circumstances. • the time lag between exposure to infection • Infections in dogs may be prolonged for and appearance of symptoms. However. individual dogs are valued • Vector-borne human VL due to L. and humans. affecting substantial popula- acute cases of human VL and the distribution tions of stray dogs and domestic dogs. which may in part be dependent Arabian peninsula. South America. is the agent of human VL. that there is a directly significant be undiagnosed and untreated. Kuhls potential to infect sandflies.. infantum with the same tus for interventions against canine VL. Multiple L. although as yet with little direct impact mission from human to human via the sand. mon approaches to the control of canine leish. on control strategies for leishmaniasis fly vector cannot be excluded. and vectors can be found stantial research effort on Leishmania and the elsewhere (Desjeux. among vulnerable endemic communities. There is increasing evidence that the • A WHO technical report on control of dog may also be an important host of L.. horses. Santos et al. and silvatic mammals with combination drug treatments or such as foxes (Cerdocyon thous) and opos. can carry not applicable to canine VL. the WHO. During the last 10 years there has been sub- reservoir hosts. Carros. infantum have been shown experimen. infection is rarely acquired some evidence of success in field trials. 2007). improvement of the control of leishmaniasis: The incidence. and schedules for human VL. Reithinger a still helpful guide to the control of VL. infantum (Quinnell canine VL and human VL transmission and Courtenay. to kill and repel sand- dog warrants the status of a primary reser. modified single-drug chemotherapy sums (Didelphis spp. matic VL due to L. although again foxes and jackals in the Old World. VL have been produced and have shown vani). flies attacking dogs and thus impede the voir host for VL due to L. dono. 1998. primary reservoir host of L. only the on pyrethroids. has been licensed for use in Europe. and global extent of the leishmaniases justifies the WHO selection • The genomes of three Leishmania spp. when sandflies feed on immunocompetent One (Canileish®. the agent of human CL and MCL updated (WHO.. • Considerable progress has been made Cats. for International Development (DFID. immunocompro. and the Pan American maniasis due L. In the 1990s a workshop of human CL in Latin American cities. new immunologically naïve generations of Research progress in the last decade the human population. Lembo et al. 1995. miltefosine.236 T. cycles. major. infantum. While further research between sandflies and dogs have been on such alternative mammal hosts may be trialled. it has become relevant to consider com. 2011a) and is essential in Latin America. Studies on (Peacock et al. enhancing under- Despite the proven role of dogs as the standing of their comparative biologies. 1990) has been ziliensis. have been sequenced.. infantum but infectiousness to sandflies • New methods of reducing the contact appears to be low. notably dog collars impregnated of interest and they might rarely act as link with pyrethroid insecticides and pour- hosts between transmission cycles.) in the New World. braziliensis Health Organization (PAHO) produced (Momen. infantum and L. including protocols for the treatment of . and Davies. infantum. UK). trans. and introduced for the treatment of human this could be an emerging source of infec. France) humans with asymptomatic L. and L. although this is not appropriate for tion if such untreated co-infections increase canine VL. The establishment of reading for all those interested in the canine L. infantum (below) show vani genomes from Nepal have been that sandflies can occasionally be infected by sequenced in an effort to identify genetic feeding on humans with untreated sympto. two new vaccines for canine more likely if there is PKDL due to L. epidemiology. dono- transmissibility of L. braziliensis infections in periurban biology. severity. determinants of drug resistance. talizing optimism that in due course a mised humans who are co-infected with HIV vaccine for human VL will be attained. leishmaniasis (WHO. However. L. 1991. Further details of the geographical distributions of VL and CL. infantum infec. has been tally to be readily infectious to sandflies. and L. of the leishmaniases as a major public health L. infantum (but this is far • Importantly. WHO. 2009). bra. 1999). • A new oral drug. 2011a). L. revi- tion. As a jointly sponsored by the Department result. rats. Virbac. braziliensis problem and one of its health priorities. and control of the and urban areas may have led to outbreaks leishmaniases. VL. On the other hand. and Elimination in Dogs 237 human cases. Choice of drug may depend on the parasitaemia and give clinical improvement. which reviews con. Amphotericin B deoxycholate is given Control strategies by intravenous infusion (0. infantum. Paromomycin patients to public health workers and sulphate is given for 21 days at 15–20 mg/ referral of dogs to veterinary surgeons. sodium stibogluconate. for anthroponotic trol of zoonotic VL in Brazil. Treatment of PKDL can be difficult Treatment: life-saving but not easy for and require longer courses. pentavalent antimonials VL. • Culling of putatively infected dogs iden. liposomal amphotericin B plus paromo- environmental fogging or. Miltefosine requires 28 days varying emphasis and some improvements. and remain the same. Amphotericin is considered the best option for VL in pregnancy and for treatment and maintenance chemotherapy in HIV-VL coin- fection. treating epidemic outbreaks of human VL. other reasons for this are imprecisely known. . two excellent recent reviews: Quinnell or. and has the They are: advantage of being an oral drug. aminosidine (paromo- and Courtenay (2009). application of insecticides to dogs. For zoonotic VL human VL.75–1. Control. Pentavalent antimonials plus aminosi- logical/parasitological surveillance of dine.0 mg/kg for 15–20 days). Zoonoses Prevention. dehydration. donovani) in India and Nepal. drug resistance to antimonials may reach 60%. sero. but not necessarily eliminate the organism For 70 years the first-line anti-leishmanial or prevent relapse. can reduce treatment from domestic and stray dog populations. more usually. intramuscularly or intra- and Boelaert (2010). kg. which provides mycin) or miltefosine. for insecticide spray. Readers are also referred to amphothericin B. three fundamental strategies shorter periods and it may even be effective have been adopted for interventions against as two doses (total 20 mg/kg) or as a single zoonotic VL. The pharmacokinetic or drugs have been the pentavalent antimonials. for serological and parasi. venously. VL (due to L. Unfortunately. likely. mycin.75–1. residual insecticide spraying of dwellings. up to total of 2–3 g) (WHO. although • Diagnosis and treatment of clinical cases it is not appropriate for pregnant or poten- either passively detected by referral of tially child-bearing women. in the form of meglumine antimonate or tological diagnosis. be a great advantage in in endemic communities. regional prevalence of drug resistance. or miltefosine plus paromomycin. or concomitant L. and Romero kg for 28–30 days. liposomal et al. Combination therapy can reduce treat- or actively detected by looking for cases ment schedules. Anti-leishmanial chemotherapy for Pentavalent antimonials are much less human VL may require supportive treatment effective for the treatment of dogs carrying for malnutrition. and impregnation of bed nets (Arias are amphotericin B deoxycholate. and make emergence of drug resistance less tified by clinical and. Treatment of human some more details on aspects of zoonotic VL with antimonials is based on 20 mg/ VL relevant to this chapter.5 mg/kg). because this saves the lives of human (20 mg/kg for 28 days). more recently.. for example. more recently. In contrast.0 mg/kg daily or on alternate tive treatment for canine VL. infantum: such treatment may suppress infection. 2011a). (at approximately 2. Liposomal amphotericin B rec- ommendations vary. recommended treatments in order of preference are: liposomal ampho- Early. unsatisfactory for canine VL due to L. ycholate (0. 1996). Other combinations include • Destruction of vector sandfly species by the liposomal amphotericin B plus miltefosine. days. but it is given for much For years. 30 to 17 days. accurate diagnosis and rapid treatment tericin B (3–5 mg/kg for 3–6 days up to a are fundamental to the control of zoonotic total of 21 mg/kg). Alternative drugs ing. there is no reliably effec. albeit with dose (5 mg/kg). pentamidine isothionate. amphotericin B deox- patients. so such repeated therapy with positive and negatives can be recorded visu- antimonials should not be given. infantum infection to the prin- may be conveniently integrated with rabies cipal vector in South America. but it is not practical or sufficiently principle. In pioneer- logical methods including mass surveys (Maia ing studies. that is highly specific for human VL is also this requires prolonged maintenance treat. which uses whole blood end of therapy (Vexenat et al. again freshly prepared or lyophilized whole organ- with the risk of propagating further canine isms as antigen. The rK39 recom- Development of new drugs for canine VL binant antigen dipstick provides a relatively would seem to be of considerable veterinary low-cost commercially available rapid diag- research interest and empirical screening of nostic test for serological diagnosis of VL in large libraries may yield new leads. The IFAT requires a fluorescence allopurinol as a leishmaniostatic but not a microscope. Lutzomyia . Lembo et al. emaci. seropositive dogs as a control strategy is dis- 1999). sible to sandflies is indisputable. 1998). but antimonials are rapidly excreted. be highly infective to sandflies. complex to implement sensitive for mass surveys. usually with blood sam. and external new drug-resistant strains of L. Furthermore. quality control. In a veterinary clinic. 2008). However. a dot-ELISA (Vercammen et al. applicable to dogs if lower minimum posi- ment to avoid repeated relapse of infection tive titres are used. excessive claw growth (onychogrypho. Late-stage been adopted as a potential cornerstone of signs include dermatological changes. Serological surveys have obvious until late in the disease. infantum.. and the control campaigns. to obtain in quantity. Modified ELISAs include aminosidine treatment of dogs produces dra. there is no satisfac. Deane (1962) compared dogs and humans as ples collected onto filter paper. The valid- ation. ity of serological screening and removal of sis). 1999). Diagnosis of canine VL: better rapid The rK39 test functions less well in East diagnostic field tests are needed Africa than Europe. Nevertheless. asymptomatic dogs may cussed in more detail below.. and vulnerable to dif- tory effective chemotherapy for canine VL. ferences in reproducibility. Surveillance of dog populations to remove The ease with which canine VL is transmis- infected animals has thus depended on sero. humans and animals. and lymph node enlargement (Ferrer. as an adaptation for rapid field use (Babakhan erinary alternative is to treat canine VL with et al. control campaigns for canine VL. but populations. Deane (1956) and Deane and and Campino. It gives an immediate result and can be used to make a rapid deci- sion on intervention options when a dog is found to be positive. Thus. in fluorescent antibody test (IFAT). ally from the plate. Plate ELISAs privileged circumstances dogs have been are low-cost and may be established in-house treated with antimonials and treatment may rather than purchasing commercial assays: be used repeatedly to keep an animal alive. parasitological examination (for exam- ple by microscopy of giemsa-stained sternal or lymph node aspirates) can be routine and Culling dogs for control of VL: valid in helpful. but a modified format (rK28) has been developed in an attempt to Reliable clinical signs of canine VL are not improve sensitivity.238 T. Similarly. A direct agglutination test (DAT) curative therapy (Lamothe. A vet. Such surveys a source of L. which matic clinical improvement but rarely clinical is performed on membranes instead of plates.. 1998). cure: most dogs relapse 2–4 months after the and a FAST-ELISA. they require meticulous standardization with This practice carries a risk of generating positive and negative controls. The DAT test depends on and renewed infectivity for sandflies. which is costly and difficult and human VL. ELISA results are best read by which could spread among dog and human optical density with a spectrophotometer. Serological tests com- abundance of dermal amastigotes in canine monly use some form of ELISA or the indirect infections may be a factor. 2009). 2009).. may thus be infective to sand. . it was much easier to infect sand. 1992. 2009). (1993) or have self-cured and therefore not war- confirmed the original observations of Deane rant destruction. Infection rates in fed sensitivity of serological tests is not optimal. infantum infections. 2009). Parasitology. apparently seronegative. Also. 1998. Miles et al. low examina- known to occur rarely. Thus skin tests are not likely normal skin of such animals. Furthermore. some prolific in dogs but scanty in symptomatic. Vexenat. sandflies captured with a less discrimina. prior tive. show less than 60% sensitivity. In that infection rates of 70–90% were common humans. slow response times (Braga et al. 1999. There sandflies collected from a kennel housing are as yet no practical alternatives to serology a dog with disseminated dermal VL were that are more sensitive. seropositive dogs might be false positives untreated human VL. serological surveillance and culling of serop- Transmission among dogs and not involving ositive dogs will still allow endemic canine sandflies. Santos et al. and replacement Courtenay. Furthermore. tive than symptomology. but tive to sandflies (Molina et al.. 1998. a proportion of serologi- culture of skin biopsy samples. serological tests are applied (IFAT. ELISA. flies and propagate further human infections.. 1999). (1995) detected infec- tory CDC light-trap.. quate to sustain endemicity (Quinnell and 1998). and parasitological tests may feeding them on the human cases. of dogs with susceptible puppies are likely to Unfortunately serological surveys for prejudice the outcome of a serological survey canine VL fail.. by sexual and congenital routes. because as well as dogs. Zoonoses Prevention. Dermal amastigote infections were of infected dogs are seronegative. Vasconcelos et al. as they are in Courtenay. field and experimen. Some symp.. 2009). Cardoso tal observations indicate that the basic case et al. were much lower. tion rates. and overall infection rates were greater indicator of cure but not of the presence of than 20% even when flies were fed on the active infection. compliance failures. partially because a proportion and culling strategy. led by the balance of cell-mediated (Th1) xenodiagnosis experiments demonstrated and humoral (Th2) immune responses. implying each constraint on the effectiveness of serological case is likely to give rise to several new cases. and Elimination in Dogs 239 longipalpis. 1994. 1998. 1999) confirm that the days after collection. There is evidence alternative hosts such as chickens or pigs that both human and canine VL are control- were abundant in the endemic area. 1994. 1998). Up to 67% of engorged female sion (Vexenat. By PCR. Similarly. No infec. Miles et al. human VL (Pinelli et al. (1999) con. Experimental trials shown to be infected by dissection 5 and 7 with PCR (Roura et al. to be an alternative diagnostic procedure for asymptomatic dogs can also be highly infec. In addition. longipalpis fed on in a series of experimental dogs infected by treated human cases. and not at levels ade. is VL to be sustained. Ashford et al. The lim- The high R0 has been supported by careful ited sensitivity of serology indicates that the population studies and mathematical models reduction in R0 that is likely to be achieved by (Dye.. This tions in more than 30% of dogs that were was not surprising. They increases with serological titre (Quinnell and isolated Leishmania from 7 of 18 patients by Courtenay. cally negative dogs are parasitologically posi- tomatic human L. Thus. positive skin tests (Montenegro when sandflies were fed on symptomatic or leishmanin tests) are considered to be an dogs. DAT). Although the probability and Deane (1962) that amastigotes could be of demonstrating the presence of infection recovered from symptomatic human VL. Quinnell and Courtenay. This failure of reproduction ratio (R0) for canine VL is likely serology to diagnose all infections is a severe to be high in endemic areas. 1999. sandfly bite. longipalpis by examining wild-caught ous lesions and in the absence of seroconver- sandflies. Quinnell and rates or cure rates in canine VL. determining the presence of infection. is not as sensitive flies by feeding them on the dogs than by as serology. tions were acquired by Lu. a proportion of the animals was firmed the high transmissibility of canine VL able to transmit infection from early cutane- to Lu. they might be useful for assessing exposure 1993.. Miles et al. even though as many as three different to treatment. surveys as part of a control strategy. Control. although more sensi- However. with consequent under. as clearly erage of the affected area. replaced by new susceptible animals. per. with high cov- (Miles. ultra- rates. sandflies. Withholding treatment for overt clini- standable reluctance of such communities to cal human VL. For cal surveillance and culling alone will still long-term effect. DDT is effective. In view of these various factors complicat. the future success of dog Comparative impact of treating human culling as a control strategy will depend on a VL. culling dogs. the removal of infected dogs. which is usually fatal if accept full implementation of an optimal cull. is clearly not an ethical option ing programme. 2008. Simple deterministic model consid. Quinnell and Courtney. 2010. trol campaign. in com. and spraying bination with health education and strong against sandflies as components of a VL con- community support. and others). 2009. and the temporal aspect of sur. it is However. unpublished observations). he found that the have low toxicity and high residual activity. this blanket approach only reaches apparent that current methods of serologi. mul- immense importance and value that some tiple potential confounders. sandflies are exquisitely sensi. interventions against human VL. In the absence could maintain endemic canine VL. Alencar of resistance. Comparative studies in which treatment of human VL is specifically withheld to assess its epidemiological impact are thus not avail- Control of sandflies with insecticides: able. ultra-low-volume spraying allow canine VL to be sustained and expand must be applied repeatedly. longipalpis. insecticides were used in addition to the patric. Occasionally. sandflies during sleeping periods at night. Insecticide- reduction and resurgence of prevalence by impregnated bed nets offer protection against Courtenay et al. (1961) assessed the impact of sandfly control tive to insecticides. and working dogs. As indicated above. spraying against mosquito vectors of treatment of human cases and the removal . have had mixed and partially conflicting results (Nunes et al. and vector control highly sensitive rapid diagnostic test for field use (Maia and Campino. Insecticides are used residually against control campaigns against zoonotic VL. (2002). dance of sandflies and the prevalence of logical screening and culling as the core of VL. Lembo et al. Romero and Boelaert. not treated. incidence of human VL decreased only when In localities where malaria and VL are sym. which are not tive values of the treatment of clinical cases. Sandflies may be extremely abundant in but believed that small sandfly populations endemic regions of canine VL. adult sandflies at the time of spraying. 2008) and immedi. Few studies have attempted to assess the rela- ate removal of infected dogs. malaria can have a dramatic effect on abun- erations indicate the frailty of current sero. as part of comparisons of interventions. cypermethrin. and applied to domestic and peri- Thus. dog cull. Deane and Deane (1962) thought that an essential element of VL control outbreaks of human VL in Brazil depended on the abundance of the vector Lu. Barrier curtains treated with insecticides can ing implementation of culling it is not surpris. Topical ing that field trials. knowing fluctuating seroprevalence domestic resting sites. as are with insecticides in a comparative study of the synthetic pyrethroids (deltamethrin..240 T. With two methrin. and at seasonal demonstrated by computer modelling of peaks of sandfly abundance. Such studies are fraught with ing as a control strategy cannot ignore the difficulty due to complexities of design. and equivocal communities may attach to their domestic outputs. can help to stem epidemic outbreaks of VL. estimates for serology coverage and low-volume spraying into the air (fogging) failure rates. 2010). veys and the course of canine infection. which groups of communities. which may have inherent insecticide treatment of dogs (below) may design weakness and multiple confounders. restrict access of sandflies to houses. Furthermore. also reduce sandfly numbers. and seropositive dogs were removed promptly by to stop transmission from vaccinated dogs using the FAST-ELISA for serology. including Leish-111f+MPL-SE vaccine VL has been a research objective for decades. with 1/165 clinical cases in vaccinees versus 12/165 in con- Vaccination and immunotherapy: trols (Lemesre et al. another association (Costa et al. 2009). culling of seroposi. 2007). 2010) and the immunologi- summarized by Romero and Boelaert (2010): cal response has been characterized in vitro one trial showed reduction in incidence of (de Lima et al. Similarly. and Elimination in Dogs 241 of seropositive dogs. cutaneous site (leishmanization) can protect fly abundance and the importance of vector against subsequent infection and potential control.. In a smaller field trial Boelaert. it is essential that the serological seropositive dogs. prime boost vaccine DNA/ showed a similar trend but was not signifi. It was fur. The control campaign in north. their futures are dependent a decrease in both the incidence of human VL on conclusive demonstration of capacity to and seropositivity rates in dogs when 69% of prevent severe clinical disease in dogs. what et al. or recombinant are few and limited.. tive dogs. 2010). 2010).000 DALYs had been skin test positivity. a L.(fucose-mannose ligand He assumed that epidemics with increas. (1998) were able to show for canine VL. one indicated a partial Amorim et al. antigenic fraction. there screening and removal of seropositive dogs are no attenuated. have been developed and commercialized 1999). In Brazilian field tri- years. major to induce a lesion at a hidden and Deane’s view of the significance of sand. with varying degrees of suc- The development of vaccines against human cess. protection against clini- gained. MVA. contribution to the campaign is attributable Leishimmune® is also reported to have to the culling of seropositive dogs. blocking of transmission. FML-seroconversion human VL associated with a combination did not cross-react significantly with stand- of insecticide spraying and dog culling (de ard ELISA for serological surveillance (de Oliveira et al. and recovered. is a complication of effective surveillance.. donovani) saponin ing levels of incidence occurred every 10 vaccine for canine VL. Leishmune® (Fort Dodge Animal Health. More some immunotherapeutic potential (Borja- recent combination control trials in Brazil are Cabrera et al. The total removal of the vaccines for human VL. In compliance did not allow removal of all the addition. Failure of that might acquire subclinical infections. vaccination was a supplementary interven- cluded that the campaign had been cost. Brazil) is an FML. the efficacy of Leishmune® was reported was estimated at US$95. ther estimated that 68. Zoonoses Prevention. Akhavan con. 2007). Studies of the impact of serological facial disfigurement. however. infantum antigen with muramyldipep- tide as adjuvant (LiESAp) was reported as having 92% efficacy. response of vaccinated animals can be distin- Akhavan (1996) considered whether guished from that of dogs acquiring natural control of VL based on the three strategies infection. although inten- dog population has been reported to be an sive research efforts continue. It is not clear. associated reduction of incidence of human eastern Brazil has been difficult to sustain VL in some but not all localities where continuously. Nevertheless.. Nevertheless. to be indicated by FML-seroconversion.. of L. because failure to separate them of treatment of cases. cited in Romero and (Carson et al.. .. killed.. Two vaccines effective control measure in China (Ashford.000. 2008. 2003). and spraying against sandflies. at a cost of US$139 for each DALY cal canine VL. which may have some immunotherapeutic impelled by knowledge that introduction of potential (Trigo et al.. and a third candidate. 2010). 2010). Several other some progress second-generation vaccines are also under development. Palatnik-de-Sousa et al.. tion in control programmes (Borja-Cabrera effective. had been effective in north-eastern Brazil. did not induce rK39 seroconversion cant (de Souza et al. The total cost of control campaigns als. Control. 2009). Ashford et al. This supported Deane infective L.000.. for other insect vectors such as mosquitoes. or where sandflies (Xiong et al. and require clear guidelines on how to manage canine VL. and be fatal. which slowly release insecti. However. Topical application of insecticides to dogs: higher-level public health authorities will a useful adjunct to control of VL need to decide whether epidemiological sur- vey for human and canine VL is justified. surveillance. and communities. and A promising approach to control of canine if further cases are found whether to begin a VL is to use pyrethroids in new ways. trol of VL that are available to public health Killick-Kendrick 1999. Aoun professionals. as a supplementary adjunct to control pro. Knowledge. environmental of canine VL and to know how to report the surveillance. and various models have been mental degradation and chaotic husbandry proposed (Arias et al. even if programme for zoonotic VL human VL has not yet been reported in the locality. 1999. This is because sporadic infant cases • Efficient. 1996. and increasing options for Integration of disease control: communication and health education such as not to be overlooked radio. nity resources are fundamental but somewhat able to shedding and can only be regarded neglected areas of control of VL. rapid delivery of effective. and field trials have indicated potential to reduce incidence Health education and mobilization of commu- of canine VL.. 1995). equipped to make serological and parasito- logical diagnoses. of dogs and other domestic animals can be Primary health care workers in the commu- addressed (Marzochi et al. such as coordinated and integrated control campaign. and more orthodox of information on transmission and con- vector control (Killick-Kendrick et al. environmental improvement. Informed saving treatment for human VL. with . Veterinary surgeons and zoonosis control. Community nity. et al. makes logistic and economic sense. 1997. need to activities can include clinical surveillance and be able to recognize the clinical symptoms follow-up of treated patients. as well as veterinary surgeons. by dipping hosts or spotting-on insecticides Where rabies surveillance and control cam- to diminish sandfly attack and to kill biting paigns are envisaged or in place... Health education and community support: cide that spreads over the host. 2011a). One approach is the use of pyrethroid-impregnated protective bands for dogs.. life- may go unrecognized. Experimental fundamental to success trials have shown efficacy. presence of canine VL through local health and assistance with vector and reservoir channels. An essential to communicate across the control emulsifiable concentrate of deltramethrin programmes and share resources whenever it was effective for 5–6 months after applica. but veterinary health or the management of VL other predisposing factors such as environ- is imperative. and mobile phone tech- nologies which are dispersed to locations that previously had poor accessibility. Poor socio- Coordination of control activities across economic conditions associated with propa- organizations responsible for human and gation of VL may not be altered easily. Lucientes. 2009). collars are vulner.242 T. and practices (KAP) studies are a grammes that deploy the principal means of useful means of understanding the extent diagnosis. WHO. 2011a). There are often abundant and diverse levels of harnessing community support for con- trol programmes. TV.. tion (Courtenay et al. patients. and can be a driving force for behav- centres or similar organizations need to be ioural change. it is example in the form of ear tags on cattle. 2008. computer.. Lembo et al. 2009). WHO. Effective liaison between veterinary health authorities and Essential components of a control human health authorities is essential. attitude. Similar systems there are overlapping interventions against are effective against other insect vectors. can provide a strong argument or by few doses given by inoculation. 50% breaks on the Indian subcontinent and in the of human L. ated with HIV coinfection (Alvar et al. whether infected dogs should not be abandoned. better drugs for treatment to give impetus to available and proven local of human VL are still desirable. where possible implemented of efficacy in field trials. infantum to be less reliant on the dog as the primary reservoir host. and human VL. Such a test may be beyond tions to detect the presence of canine reach. and most of these cases will munity support apply. lance and management of dog populations. sibly shift the pattern of epidemiology of VL due to L. Vaccination is • Environmental management and vector a promising new development. health education. sitive. with public health recommendations. traps incorporating host or sandfly pherom- where.. and requires further proof of sandflies. There a method of reducing domestic sandfly infes- is an urgent need for a cheap. and com- WHO. highly effective tations. awareness of canine and human VL among tive. specific. the most important factors in transmission of tory. In endemic areas in developing countries. Thousands of sandflies may be caught in longed or lifelong allopurinol administration a CDC trap during a single night: improved cannot be advocated for widespread use else. and to mats are still being sought. Economic analysis. Zoonoses Prevention. 2011a). A concerted effort is required to improve panies to take a research interest in this objec. considerable improvements ties. The drug of prevention against the financial loss due should be simple to administer either orally to disease. could also be devoted to strategies for increas- agement of domestic and stray dogs. a new treatment suitable for mass therapy and integration of activities by organizations to be found. treatment. rapid diagnostic test suitable for field • Serological surveillance of dog popula. Conclusions As described above. of treatment such as secondary chemo. displaced. with its concomitant impact on control of communities and health professionals. The last-resort method in Europe of pro. case finding. Incorporation of by community support. attention is repeat- edly drawn to sandfly abundance as one of Treatment for canine VL is clearly unsatisfac. or as a control strategy. Control. Some thought encourage risk reduction and better man. In launching control programmes. Clearly. highly sen- therapy or travel to treatment centres. infantum coinfections in the highly vulnerable populations there will be community might provide a new reservoir limited capacity for community support. VL. diagnosis. Were tion. comparing cost drug for the treatment of canine VL. and some HIV/L. and Elimination in Dogs 243 zero cost to patients in poor communi. 1996. including coverage of ancillary costs are essential if this method is to be effective. especially in one attractants are worthy of investigation as view of the risk of sustaining endemicity. There is for control campaigns against leishmania- a strong case for encouraging veterinary com. In particular. infantum. this could virtually eliminate with responsibilities for disease control. In Europe. sis. difficulties with compliance. although new antigens and new for- VL as a predictor of human VL. Among such impoverished. these should . especially in areas where HIV and status and to consider multiple complicating VL are increasingly sympatric. ing dog examination rates and compliance • Systematic enhancement of health educa. Nevertheless. Epidemiological screening for L. Leishmania antigens into the vaccine strain of rabies virus could be explored as a delivery For anthroponotic VL due to L. communication. but not the surveil- receive prolonged antileishmanial therapy. communication. at community or national level. remains a control to reduce breeding and abundance research priority. infantum infections are associ- Sudan). community support. This may pos- factors of such epidemic outbreaks. donovani system to provide simultaneous rabies and (responsible for such large epidemic out- Leishmania vaccine coverage. a reliable. and of infection for sandflies. use is essential. and national strategies for control. if not adequately an imperative need to improve nutritional treated. due to the increasing availability of food in Africa and Asia are considering tackling sources. potential to reduce the incidence of canine VL. many more countries tres. and cost-effective package. is currently being used to implement pilot This is compounded by reports indicating that projects in three developing countries which unsupervised or insufficiently supervised dog should. have demonstrated the populations are increasing in most develop- feasibility of the paradigm shift and its cost. Towards this in most endemic areas. ease. recognition of cost benefits. Gaining access to dogs remains the major In the field of rabies. of these major canine zoonotic diseases. and integration with other relevant elimination of rabies by the year 2020. that are part of the South East Asian Region of whether canine or human. owners is very difficult to obtain. new tools on canine VL occurrence and trans- ported and sustained by communities. hypothetical cumbersome interventions. In cystic echinococcosis. of sheep immunization with or without dog sive control programmes are initiated soon. if no comprehen. have been developed and used in field trials able research dimensions of the problem and with the first results published in 2008–2010. Lembo et al. The Gates Foundation when coercive measures have to be taken. as their human and dog rabies problem than it does not have a sustainable impact on dog at the end of the 20th century. and leishmaniasis still are expected to have a much higher chance represent a significant public health problem of success in affected countries. Dog removal is not the solution. alternative strategies involving vaccination of sheep Final Conclusion with the recombinant oncosphere vaccine EG95. they goal. tal organizations and NGOs. This funding requires considerable efforts from the owner. and should be The ten countries of the ASEAN (Association consulted by national governments and/or of South East Asian Nations) together with the civil society to develop policies based on China. The full collaboration of dog has been promoted by international organi. and the Republic of South best practices and animal welfare standards. will be initiated the past 10 years in the prevention and control very soon. In some of them. been achieved during ease in humans and animals. and Sri cal will. especially zations since 2005. mission in mass campaigns is still missing. disease control programmes and an invest- In the field of leishmaniasis. not over-ambitiously involve all conceiv. by early 2014. however. The final demonstration of the impact of those manageable. decided in 2008 to support this approach or when dog handling entails some risks or with a grant of US$10 million. factor for success or failure of control pro- digm for human rabies prevention through grammes for zoonoses in which dogs play the control and elimination of rabies in dogs a pivotal role. during the ment from the countries themselves and the past 10 years new vaccines against canine VL international community. demands politi- WHO. Nepal. but The use of insecticide-impregnated dog collars be focused on the proven practical control is considered a promising approach with the methods to interrupt transmission and dis. ing countries. ment guidelines have been developed during nate human dog-mediated rabies and stop the past 3 years by international governmen- dog-to-dog transmission by the year 2015. in addition to classical interventions. Rabies is the population size and is unacceptable to and/ first neglected zoonotic disease to be targeted or counterproductive in many local communi- for elimination at the regional level: all Latin ties. echinococcosis. controlled trials using EG95 aiming at are increasingly reported and this is a cause of definitively demonstrating the added value major concern for the future. Korea and the other rabies-endemic countries Effective control of these diseases. Rabies. such as Bhutan. co- Lanka. deworming to control and eliminate the dis- Progress has. a change of para. Japan. 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Washington. pp. and World Health Organization (eds) 49th Directing Council. Yan. lization. In wildlife. and costs of specialized staff these conflicts involve disease transmission. and reducing risks of mam- can be achieved through surgical sterilization mary tumours (ACC&D. 2010).. Community opposition to cal sterilization. ing male sexual behaviour such as spraying. and livestock have fostered for population management.L. Cathey and Memon. Goericke-Pesch or via chemical sterilization and contraception. 2006). of novel fertility control agents (Naz et al. * Author. and contraception is also more efficient than surgi. suppress- but maintains the potential for fertility. 2010). especially Aitken. 2011). and steri. Levy. flicts is widespread because of questions over bers that can be neutered or spayed per unit time its humaneness and potential environmental (Massei et al.massei@fera. or unsustainable. et al. e-mail: giovanna. sterilization in livestock and zoo animals. that renders animals infertile (Munson. 2009. 2011). particularly for investments and research into the development high-profile animal species such as dogs. and effective means for resolving flicts and for wildlife disease management human–wildlife and human–companion ani- (Fagerstone et al. McLaughlin and mals (particularly dog) conflicts. 2010. the potential market for to be buried.gov. humane. treating pros- 2006. 2005). used for mitigation of human–wildlife con.. UK Fertility control is used as a broad term for both In companion animals. as it overabundant animal populations and tradi- does not involve anaesthesia.gsi. monkeys. and elephants. Origins of ciated with surgery. and as alternatives to surgical when culling is unacceptable. tionally tackled by lethal control. unfeasible. Chemical predation on livestock and game species. Dogs. chemical tives is advocated for conflicts exacerbated by contraception is safer and less expensive.N. as many more animals can be the use of mass culling to manage these con- treated with a contraceptive compared to num. roaming. welfare risks asso. Sand Hutton. and facilities (Kutzler and Wood. wildlife. contraceptives are contraception. or when poisoning is used. ods places increasing constraints on options ion animals. that prevents the birth of offspring used for preventing reproduction. illegal. 2010. 13 Fertility Control in Dogs Giovanna Massei Food and Environment Research Agency. York. fertility Contraceptives are thus increasingly control is increasingly advocated as a safe. and aggressiveness. 2nd Edition (eds C. et al. 2010. attacks on humans. cats. This contraceptives and a growing public interest in growing public antipathy towards lethal meth- alternatives to surgical sterilization for compan.uk ©CAB International 2013. Macpherson et al.. impact when large number of carcasses have In recent years... Zoonoses and Public Health. traffic accidents.) 259 . Kutzler and Wood. the use of contracep- Compared to surgical sterilization. Schmidt crop and forestry destruction. As a result. 2006. Fertility control tatic hyperplasia. and to avoid anaesthesia (Levy 2009). junction with rabies vaccination considerably Swinton et al.1.. where veterinary care is not widely available nor affordable (Levy. 2007. 2007. Ramsey.. Contraception nation.. likely to affect social organization. gamete formation. produced in the hypothalamus at the base .1). leptospirosis in brushtail possums. unnecessary procedure (11. particularly in areas 2007) (Table 13. car. on Isabela Island (Galapagos). cost indicated that culling can lead to immigra. dog move over long distances to fill the voids owners more frequently selected chemical left by those that have been removed from castration over surgical castration to retain the population. dogs to be vaccinated against rabies and the tion of reproductive behaviour results in a time to achieve rabies elimination (Carrol decreased contact rate between animals.1%). fertility control is less et al. Jodhpur.4%). injected activities for the control of wildlife diseases with a rabies vaccine and a contraceptive...5%). and behavioural changes (4. In The cascade of hormones leading to another Indian town.. conception or implanta- ried out on 24.5% of people Examples for zoonoses such as bovine tuber.. theoretical evidence suggesting that an effec. and et al. 2008).g. resulted in steriliza. in increased contact rate as animals tend to Similarly. by reducing both the proportion of also offers an added benefit. by chemical sterilization.. A study in wildlife and in free-roaming cats and dogs. 2002. quoting compassion are provided in Table 13. Many studies (58.. economically sustainable reduction of culosis in European badgers (e. such pro- Fertility control has been advocated as a means grammes are likely to be significantly more to reduce contact rate and disease transmis. 2011)... adding fertility control to vaccination could The renewed interest in contraceptives be more efficient than simple vaccination in to manage wildlife is also based on field and eliminating diseases such as rabies in foxes. 2010). free-roaming animals can only be achieved 1997. social disruption. Conversely. 2006). their dogs’ perceived protective and hunting ries (e. Although these studies demonstrated Transmission that well-coordinated surgical sterilization can decrease the number of dogs. 1997. found that 56. Dog studies have been carried out to determine owners may be reluctant to consider surgery the impact of fertility control on zoonoses in for other reasons than just cost. as animal Recently developed mathematical mod- movements in particular are less affected by els suggest that using contraceptives in con- reproductive inhibition than by culling (e. 2007). rabies incidence (Reece and Chawla. Woodroffe et al. and actually result reasons against this method (Soto et al. Several theoretical and field immediately released (Massei et al. and tuber- tive. Ramsey. as the elimina.g. who had adopted shelter dogs were against culosis.260 G. and and zoonoses. On the other hand. Sao Paulo. 2002). Saunders et al. expensive than those based on catch-inject- sion between individuals in the context of and-release where dogs are caught. brucellosis. 2008). Bolzoni et al. behaviour. and to re-establish territo. White et al. 2010).8%) as tion. Massei Fertility Control to Reduce Disease 2010). Tuyttens and MacDonald. The inability to sterilize a high proportion of free-roaming dogs through surgical sterilization was Animal Reproduction and Potential quoted as the main factor responsible for the Targets for Fertility Inhibitors failure of the Animal Birth Control (ABC) in India (Menezes. leptospirosis. an Contraception can be achieved by preventing intensive 8-year ABC in Jaipur (India). a 3-year ABC reproduction is regulated by the gonado- programme led to 62–86% of free-roaming tropin-releasing hormone (GnRH).986 dogs. Brazil. or by disrupting pregnancy and causing tion of 64% of the females and in a decrease in resorption or abortion. decreased the effort required for rabies elimi- 1998. Smith and Cheeseman. which is female and male dogs sterilized (Totton et al. 2005).g. (9. tion. and rabies surgical sterilization. These findings confirm the pre- thus in a lower risk of disease transmission dictions of previous models indicating that (Killian et al. 4. induces oestrus behaviour. 3. 2010. vulvar year round. and ovulation. a surge of GnRH and LH is followed by role in the development of male reproductive ovulation. After ovulation. particularly ing hormone) and FSH (follicle-stimulating progesterone and to a lesser extent oestrogen. These gonadotropins regulate Progesterone is produced by both the corpora steroid hormones that drive sperm produc. fertility Model Integrating fertility control 1 Vulpes vulpes control and rabies vaccination for with rabies vaccination is rabies control more successful than rabies vaccination only European Test fertility control to eliminate bovine Model Fertility control integrated 2 badger tuberculosis with culling can eliminate Meles meles the disease Bison Evaluate immunocontraception to Field trial The use of single-dose 3 Bison bison decrease transmission of brucellosis immunocontraceptives is suggested to avoid disease vertical transmission Possum Test effects of fertility control on Field trial Fertility control does not 4 Trichosurus possum behaviour and leptospirosis affect social organization vulpecula transmission but reduces disease transmission due to decreased contact rate Dog Test fertility control to improve Model Fertility control added to 5 Canis familiaris efficiency of rabies elimination in rabies vaccination reduces urban dogs the proportion of dogs to be treated and the duration of vaccination campaigns Dog Evaluate the effect of surgical Field trial Sustained surgical 6 Canis familiaris sterilization on population size and model sterilization can reduce in the context of rabies control population size and in the long term lead to rabies elimination References: 1. and at which in turn promotes the development of the beginning of each reproductive season for female secondary sexual characteristics.1. 2007. nificant amounts of hormones. 2010. Ramsey. Fox Evaluate impact of culling. Species Aim Method Conclusions Ref. Smith and Wilkinson. lutea and the placenta and is critical to sup- tion. Carroll et al. FSH is responsible for the ini- in the ovary results in secretion of oestrogen tiation of spermatogenesis at puberty. such as the testis and prostate. Totton et al. White et al. ornamental feathers or . GnRH controls the release of into the corpus luteum which produces sig- the pituitary gonadotropins LH (luteiniz. 6. such those species that are not sexually active all as breasts. 2003.. 2. Fertility Control in Dogs 261 Table 13. FSH and LH cause the promoting secondary sexual characteristics remaining parts of the follicle to transform such as manes in lions. Examples of empirical and theoretical applications of fertility control to control/eliminate zoonoses in wildlife and dog populations. 2004. LH causes the testes to produce swelling. testosterone which stimulates and maintains When oestrogen production reaches a thresh. FSH stimulation of the follicles In males. Testosterone plays a key old. 1997. port pregnancy. spermatogenesis. 5. follicular development. In females. hormone)... the production of tissues. and in oestrogen decreases. and regulates vaginal secretions. Miller et al. of the brain.. gamete transport. wildlife species. or they account potential field applications for free. courtship. a group of pro. many carnivore species. physical. ciated with a variety of uterine pathologies Unless specific references are quoted. In females.262 G. the review included only ine contractions (Asa and Porton. the pituitary gland. have been widely infertility for at least 6–12 months after one used in zoo animals and are highly effective on or two doses. Massei bright coloration in birds. Some examples of contracep. long-term contraception of canids and felids traceptives was derived from the Association (Munson. and mating. and maintenance of pregnancy. regarded as suitable for free-roaming dogs depending on species. and companion in pregnant animals because they might induce animals such as cats and dogs. but that cannot be induce infertility for at least 2 years or longer. Some those agents described as effective to induce progestins. companion animals but unsuitable for field able or widely tested on several species. Moresco et al. and its use is not generally recommended for most of the information on zoo animal con. oestro- Feedback mechanisms between GnRH gens. However. and progestins are frequently used as repro- duction of these hormones is increased or ductive inhibitors in zoo species and in some reduced to promote and maintain repro. and ungu- tives that are very effective in fully control.2 GnRH and stimulate production and release . Steroid hormones such as progestins. ence with folliculogenesis. melengestrol acetate (MGA). and egg spermatogenesis. might affect parturition by suppressing uter- roaming dogs. lates. suppression of GnRH action of steroid hormones includes interfer- or of FSH and LH interferes with ovulation. and behavioural signs of sis or release of hormones produced by the oestrus occur in animals that are otherwise hypothalamus. primates. 2009). Higher doses are The reproductive cycle and gametogen. particular focus on those used in free-living Synthetic progestins are not recommended carnivores. and norgestrel. such as MGA. required to block ovulation than to achieve esis can thus be disrupted by administration contraception: therefore it is possible that of substances that interfere with the synthe. with applications to free-roaming dogs. 1990). chemical sterilization can Synthetic progestins are available in a also be achieved by some chemicals inducing variety of formulations and include megestrol testicular sclerosis and permanent sterility. The proposed mechanism of duction. is the zona pellucida (ZP). 2005). was found to postpone oestrus fertilization. MA. in 92% of female dogs provided that it was administered orally for 8 days starting at a very specific time of the oestrus cycle (proe- strus). an MGA implant can led companion animals. Taking into stillbirth or abortion in some species. or the effectively contracepted (Brache et al.. and antlers in deer. embryo implantation in females. zoo carnivores.. 2006. ovulation. acetate (MA). ovulation. In these species. gonads. specific Fertility inhibitors for dogs doses at a very precise time of a dog’s cycle makes this agent a classic example of a con- The following section presents a brief review traceptive that is very effective in confined of fertility control agents commercially avail. of Zoos & Aquariums (AZA) Wildlife Contraception Center at the St Louis Zoo. The requirement for multiple. and various combinations of oestrogens and gonadotropins ensure that the pro. Steroid hormones Testosterone is also responsible for aggres- sion. another target for contraceptives levonorgestrel. In males. Therefore. MGA is asso- are provided. spermatogenesis in males. used for dogs and cats over several teins that surrounds the ovulated egg and decades in many countries under different allows species-specific sperm recognition and brand names. and impairment of implantation.1 Gonadotropin-releasing hormone agonists and information on contraceptives for dogs and cats from the Alliance for Contraception GnRH agonists are proteins that mimic in Cats and Dogs. Rubion et al. however. Virbac. The zona pellucida Porton. implants induced a 96% decrease in testoster- 2007). has been effective in white-tailed 1-year reversible contraception for female deer and horses for up to 4 years (Fraker et al. Herbert and Trigg. Contradictory was also successful in preventing puberty findings between studies might be due to in young bitches for at least one year and in differences in the source and method of . deslorelin and allows egg–sperm binding and fertiliza- (Suprelorin™. et al. mice. The effectiveness of GnRH agonists Immunocontraceptives depends on a variety of factors including the agonist potency. Immunocontraceptives such as removal of the gonads but are reversed once gonadotropin-releasing hormone (GnRH) the treatment. Munson. fertility were reversible in both sexes (Trigg monkeys. followed A study on male dogs showed that Gonazon™ by prolonged ovarian quiescence (Gobello. is a layer of proteins that surrounds the egg Among GnRH agonists. and possums (McLaughlin and Aitken 2011. France) tion. younger than 3 years of age (Goericke-Pesch lowing administration of an implant contain. early trials with ZP-based vaccines were for 18 months. horses. was found to provide at least injection. seals. Killian et al. and the duration of treatment (Gobello. kangaroos. ovulation (the ‘flare up’ effect). This second dose prevented promising but later studies showed no reduc- oestrus in 92% of the animals.. The side effects of GnRH agonists are essential for reproduction and thus causing generally similar to those associated with infertility. a ZP vaccine called SpayVac™ merly manufactured by Intervet International (ImmunoVaccine Technologies. and dose of the vaccine and of the 27 months (Trigg et al. Gonazon™ tion in fertility (Levy. Scotia. female dogs were 2002. 2006.. pellucida (ZP)-based vaccines inhibit gamete nancy. often administered through vaccines inhibit gamete production by pre- an implant. depend on many factors that include sex. Bertschinger effects of immunocontraceptive vaccines et al. 2005. bears.. et al. The activation of the reproductive sys. females treated with a GnRH agonist dogs older than 6 years and in 73% of dogs should be considered fertile for 3 weeks fol. Among the most (Gonazon™. the dose Immunocontraceptive vaccines act by induc- rate.. and treatment-induced effects on in wallaby. Aitken. successful. 2006).. elephants.. In dogs and administered a second implant left in place cats. The ZP is among the most widely stud- available as implants can induce a 1–2 year ied target for immunocontraceptive vaccines contraception in cats and other felids. McLaughlin and reproductive function in male dogs was dose. administered as a single tered as implant. age. 2005). 2001). 2002. 2011). azagly-nafarelin Kirkpatrick et al.. adminis.When tested on dogs. ing antibodies against proteins or hormones 2007). 2008. 2008). 2011). deslorelin post. but for. 2011). the release system. and species as well as active ingredients. The GnRH agonist. longevity. for- poned oestrus in females for periods of up to mulation. ing a GnRH agonist. 2010). Nova B. one concentration for at least 6 months in 81% tem also results in temporary enhancement of the animals tested. 2001). Boxmeer. is suspended. wild (Gupta and Bansal. Agonists do not quickly dis. dogs. 2001. white-tailed deer. Fertility Control in Dogs 263 of FSH and LH. and in tammar wallabies (Macropus The effectiveness..Halifax. 2010). Carros Cedex. related: spermatogenesis was suppressed for ZP immunocontraceptive vaccines have more than a year in 14 of 16 dogs administered been used successfully to prevent fertilization deslorelin.V... Canada). dogs. and side eugenii) (Munson et al. as they may cause abortion (Asa and function and conception. 2006). GnRH venting ovulation and spermatogenesis.. The Netherlands). Concurrent reduction of of testosterone and semen production in aggressive behaviour was recorded in 62% of males. Suppression of adjuvant (Miller et al.. In a follow-up trial. currently not produced. Zona agonists should not be used during preg. suppressing oestrus in female cats for at least sociate from the GnRH receptors and their 24 months with no other side effects observed administration initially causes oestrus and (Driancourt et al. 2004. 2000.).A. reproduce. Miller et al. respectively mals still exhibit oestrus. However. comm. and protected 100% of the animals after years is Gonacon™. 2000. In parallel. 2008. injection site (Levy. Gonacon™ induces infer. Kirkpatrick. 2011. 2005. type of p at the injection site. as females tively soon after injection.. many compounds aimed at non-surgical con- thickened tissue filled with fluid) may appear traception are being explored: these include . the vaccinated animal does not Miller. Fort Collins. and differences in vaccination treated with a single injection of Gonacon™ schedule (Levy. Gonacon™ consists of a synthetic have potential for both dog rabies and dog GnRH coupled with a mollusc protein and an population control. 2006). 2009). J. Bender et al. site granuloma. bloodstream. and do not exhibit oestrus behaviour. treated females or organ damage (Robbins et al. Gonacon™ has been shown cines that could ultimately also be tested on to cause infertility in deer. horses. and 4 years. 2012. admin- traceptive vaccines have been developed and istered in conjunction with a rabies vaccine. Wu et al. One GnRH vaccine induced antibodies against GnRH in treated that has seen rapid developments over recent mice. In cats. recombinant GnRH fusion proteins. 2004).. vaccines have been successful in inducing rels for at least 1–4 years after a single injec. Further progress has also been designed for applications in livestock and been achieved in the development of com- companion animals that can be treated with bined vaccines for rabies and immunocontra- multiple doses (Naz et al. 93% of females adjuvant used. dogs. rang- disease vaccine. remained infertile for the 1st year following comm. Pilot trials have FSH. This suggested that United States as a contraceptive for white. wild boar. the be tested in this species.g. these individuals have more oestrus cycles 6/20 cats had a palpable. infertile for 2. latter based on a modified version of Johne’s A wide spectrum of technologies. vaccine formulation. infertility in male and female cats for at least tion (e.. McLaughlin ception. pers. (2009) inserted the coding and Aitken. Killian et al.. and in some species (Levy et al. teins has been used in various animal species tility for several years after administration to develop novel immunocontraceptive vac- of a single dose.264 G. ology but in some species a granuloma (i.. 2011). 3.. (2009) demonstrated that Gonacon™. 2011). 53.F.. Colorado). injection site reaction in dogs while main- and thus prevent the release of both LH and taining long-term efficacy. Massei reparation of ZP. with no evidence of tissue Gonacon™ prevents ovulation.. Without these two hormones in the just started to test this new formulation (L. although the effect and adjuvant called AdjuVac™ (National Wildlife long-term efficacy on reproduction remain to Research Center. 2008. treated ani. For instance. and ground squir. pers. currently registered in the rabies virus challenge. This would be a disadvantage for dis. 2010). tested on many species of mammals. a new formulation of Gonacon™ cines stimulate the production of antibod. Formulated as an injectable. dogs. whereas 73. The majority of these vaccines have tion in female dogs. at least 6 months (Geary et al. was produced with the intent of minimizing ies that bind to naturally occurring GnRH. As ZP-based vaccines prevent fertili. bison. appear promising for potential that the recombinant rabies-GnRH virus use in free-roaming dogs.). with formation of in oestrus would still attract males and thus sterile abscesses and draining tracts at the increase contact rate between animals. Dogs treated with Gonacon™ 2010).. vaccination with three doses.. findings. and showed for wildlife. ing from recombinant vaccines to fusion pro- single-shot vaccine.e. single-dose sequence of GnRH into the glycoprotein gene GnRH-based vaccines. Several GnRH-based immunocon. In dogs. Two years after vaccination. Gray et al. Following these GnRH-based immunocontraceptive vac. specifically developed of the rabies virus ERA strain. showed adverse injection site reactions rela- ease control in free-roaming dogs. vaccination. recombinant GnRH-based cats. non-painful injection than controls (Miller et al. 20 months after administration of two doses Massei et al. Nuñez et al. rendered 92% of heifers sterile for Gonacon™ does not affect behaviour or physi. and 40% were zation but do not affect ovulation. used in In most animals. combined rabies and GnRH vaccines may tailed deer. As (at 0 and 28 days). including did not affect parenteral rabies immuniza- humans. pigs. mercial brand names. (2008) found that 8. 2009). and cultural Chemical castration in male dogs can be acceptance of a sterilization method that does induced by injecting particular chemicals into not require removal of the testes make zinc the testes. Neutersol™ can sterilize dogs without diseases.. render all or the majority of animals infer- of general anaesthesia.9% of oral formulation. For instance. marking. Thus. recommended to prevent movements of the 4.6% of the dogs. Hortolândia. Of the several fertility control agents ing. though sedation is tile for one or more years.. ease of use. Zinc gluconate-based Neutersol™ A fertility control agent suitable for control- (Addison Biological Laboratory Inc. no single-dose oral contracep- Brazil as Infertile™ (Rhobifarma Indústria tive can induce infertility for 1 year. in 99. Neutersol™ 1. untreated dogs 2 years after treatment. New York) and in programmes. 2006. However. animals. be available as an injectable. Colombia.6% of the 223 male puppies aged 3–10 2. very few meet most of these require- Zinc gluconate is currently available in ments. drugs. found that this com. Unlike surgical castra. ling population size of free-roaming dogs Missouri) was approved in the United States should have the following characteristics: by the Food and Drug Authority for chemi- cal sterilization of male puppies. The low cost. Fertility Control in Dogs 265 targeted delivery of cytotoxins for chemo. be relatively inexpensive to produce and is not completely eliminated (Kutzler and to deliver. 2008. nique was found critical for the safe use of 5. Neutersol™ does not require the use 3. times of the cycle to maximize effectiveness. and behaviour. or vas deferens to cause gluconate a valuable tool for large-scale sterili- lack of sperm in semen and thus infertility. implant. the 103 dogs treated with zinc gluconate. Levy et al. with ulceration of the scrotum and painful 6. many contraceptives Mexico. Levy et al. dose per testis. When administered by direct injection into the testicles. removal of the testicles so that testosterone 7. be safe when administered at any time of the Neutersol™. that was otherwise associated reproductive cycle or to pregnant animals. Correct injection tech. and that basal testosterone concentration in 10. New York. several Farmacêutica. welfare. of ulcers decreased as veterinarians started using separate needles for each injection Chemosterilants (Esquivel LaCroix. under several com. epididymis. be species-specific. A study compounds must be administered at specific conducted in Mexico. particularly in areas lacking Zinc gluconate neutralized by arginine clinical facilities or skilled staff (Kutzler and has been used since 2003. have no effect on or be affected by other swelling of the testes. 2010). be stable under a wide range of field treated dogs decreased but was similar to conditions. Brazil). this Conclusions chemical causes sclerosis of the testes and sterility. or injection-site reactions occurred in 3. or mounting may currently available for companion and zoo be displayed. Soto et al. no unacceptable side effects on an animal’s produced successful chemical sterilization physiology. as a permanent chem- osterilant in male dogs. 9. 2006). and phage-peptide constructs in 2. the incidence for immunocontraception (ACC&D. and ideally dog during injection. months. aggression. Wood. ulcers related to poor injec- sterilization. prevent female reproduction. 52 out of the 53 dogs administered a single For dogs that are fully confined or can be . silencing genes that control tion technique occurred at the injection side reproduction. Fayette. inhibit reproduction in both sexes. used to control tion.. secondary male characteristics such as roam. pound induced absence of sperm or semen in and should not be given during pregnancy. Wood. 2006). such as vaccines. and Bolivia as Esterilsol™ are too expensive to be used in large-scale (Ark Sciences. zation campaigns. be effective when administered in one dose. is feasible but likely to be expensive. feasibility of deliver- suffer from injection site reaction to a contra. such as India. fare costs for dogs. Lembo et al. Zinsstag programmes should first target females. text of disease elimination.266 G. wide. In parallel. Levy. in tives has been widely debated: while some rabies elimination campaigns where dogs are see permanent infertility as a prerequisite for caught and injected with rabies vaccines. 2005. compared to the risks of surgical compounds on animals and in the envi- sterilization and discussed in the wider con. Bender the whole lifespan of most free-roaming cats et al.g. proportion of dogs. et al. factors including meeting the requirement ity inhibitors should be evaluated at popula. 2008. and zoonoses. Reece et al. humans. Levy. 2011). opment of novel compounds. 2011). Few of the many fertility inhibitors that In addition.. Future development of fertility control In terms of animal welfare. Factors responsible for this renewed sion in dog populations. 2008.. are . dogs. and the practicality of bility of eliminating a disease such as rabies integrating fertility control with vaccina- and thus eliminating rabies-induced wel. For instance. widespread and still largely unresolved (e. econom- those cultures where owners of guard dogs ics. particu. or strategies in terms of effectiveness. it However. and the the aggressive behaviour of their animal growth of emerging economies. In of several disciplines such as ecology. Massei made accessible through their owners upon which owners expect the contraceptive to be request. it would be ideal if interest include the availability of new molec- contraceptives inhibited ovulation. fertility control Knobel et al.. and by integrating the use of different drugs.. and livestock. 2005. 2010. evaluate the impact of different dog popula- 2010).. free-roaming dogs and human interests are given the potential for a single male to ferti. ronment. 2009) provided the fertility control treat... to surgical sterilization for large-scale sterili. ular technologies that have allowed the devel- vent females in oestrus from attracting males. and in some in all treated animals. Massei et al. Budke and Slater. but a predictable effect instances specifically developed for dogs. novel contraceptives recently is not essential that contraception is effective formulated for wildlife species. feasible alternatives 2010. to pre. As such. repeated dosing with contraceptives 100% reliable and predictable in duration. 2010. remains unchanged. others same animals could receive a dual treatment point out that a contraceptive that can render (vaccination plus fertility control) and be animals infertile for 2–3 years is likely to last released immediately (Massei. and for the safety of operators. 2009.. unlike companion animals for could be used on free-roaming dogs. on population size is required (Carroll et al. and male chemosterilants.. the field applications of fertility control. Zhang et al. instance GnRH-based immunocontraceptives 2010. for sustainability (Carroll et al. and dogs (ACC&D. of regulatory agencies for the use of these tion level. Totton et al. costs.. and social sciences addressing problems support sterilization of males provided that of public health. In any case. This could be achieved by using con. the incidence compounds will depend on a number of and severity of negative side effects of fertil. lize large numbers of females. ide. preference should be China. ment has no side effects. the Other important factors are the competitive fact that a small proportion of dogs might cost of the products. mathematical models ally coupled with parallel treatment of males have provided the conceptual framework to (Tepsumethanon et al. could be used as practical. tion campaigns. For instance. the integration and aggression and roaming in males. ing fertility control agents to the required ceptive should be weighed against the possi.. tion management options or disease control traceptives that are effective on both sexes. and Brazil where conflicts between given to targeting female dogs. When fertility control is used as a means Efforts to develop fertility inhibitors for complementary to immunization to reduce free-roaming dogs have multiplied world- contact rate and thereby disease transmis. The long-term effectiveness of contracep- zation of free-roaming dogs. 2011). fertility control of free-roaming dogs should larly in developing countries. 2011). be evaluated at population level. 2010. . S. (2009) Utilization of matrix population models to assess a 3-year single treat- ment nonsurgical contraception program versus surgical sterilization in feral cat populations. M.acc-.J. A.stlzoo. and the future. accessed 5 October 2011.J.acc-d. T. M. and Porton.. Budke. P. pp. D. Fagerstone. accessed 24 June 2012. A.G.15–30. Gaunt.A.M. and sustainable population control or testing (Asa and Porton. Rubion. F.S. A.. Fraker.L.E. S. 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(2009) Bovine tuberculosis in cattle and badgers in localized culling areas. dogs 170–171 Corynebacterium ulcerans 85 treatment 171–172 gastrointestinal zoonoses 69–72 zoonotic implications 171 genito-urinary tract 74–76 Chlamydophila psittaci 84–85 Pasteurellosis 68–69 CMC see Colombo Municipal Council (CMC) pet care and CNR see catch. transmission 157 cat scratch disease (CSD) 69 Uncinaria 157 C-BARQ see Canine Behavioural Assessment and anthrax 84 Research Questionnaire (C-BARQ) Chagas disease see Trypanosoma cruzi chemosterilants 265 bacterial zoonoses Cheyletiella spp. 185 respiratory tract 72–74 CSD see cat scratch disease (CSD) septicaemia 68 cystic echinococcosis (CE) control vector-borne administration and legislation 233 zoonoses 76–84 age-specific treatment 231 Bordetella bronchiseptica 72 antigen B-ELISA/immunoblot tests 231–232 Brucellosis 74–75 arecoline 228 Brugia malayi 158 attack phase 227 271 . anthrax 84 description 169–170 chlamydiosis 84–85 infection. dogs 157 healthy population 195 humans disease 157 vaccination programme 195 mode. infection 54 Ancylostomatosis catch. braziliense 157 epidemiology 53 A. infection 70 A. nasuae 122 symptomatic puppies 70 Amphimerus pseudofelineus 117 Canine Behavioural Assessment and Research anaplasmosis 77 Questionnaire (C-BARQ) 27 Ancylostoma canine rabies A. neuter and return (CNR) control strategies 157–158 assessment 196 disease. alata 121 Campylobacter jejuni 69 A. americana 121 diagnosis. Index Alaria Campylobacteriosis A. marcianae 121 macrolides and fluoroquinolones 70 A. caninum 157 transmission. neuter and return (CNR) management 67 Colombo Municipal Council (CMC) 35. 272 Index cystic echinococcosis (CE) control (continued) human and dog behaviour 135–136 Australasia 220–221 lifecycle 219 consolidation phase 228 PCR test 229 coproantigen testing 229 reinfection rates 229–230 education 232 socio-economic factors 135 E. repens 158 Otodectes cynotis 172–173 DRIT see direct rapid immunohistochemical Sarcoptes scabiei var. vogeli 140–141 DAT see Direct agglutination test (DAT) Echinococcus vogeli Dicrocoelioidea Albendazole 141 Dicrocoelium dendriticum 122 Polycystic Echinococcosis (PE) 140 Prohemistomum vivax 122 Echinostoma Diphyllobothriosis E. multilocularis see Echinococcus vaccines 232 multilocularis E. canis 166–169 test (DRIT) insecta see fleas Ehrlichiosis 77 enzyme-linked immunosorbent assay (ELISA) Echinococcus granulosus dot-ELISA 238 arecoline sensitivity 228 FAST-ELISA 238 control and surveillance 136 genus-specific coproantigen 228 definitive hosts 128 necropsy/arecoline purge 229 diagnosis 129–130 diet 134–135 egg production. granulosus 218. canadensis 136–137 ultrasound scanning 231 E. intermedius and treatment 219 E. ilocanum 121 prevention and control measures 141–142 E. ortleppi 136–137 E. 229–230 treatment 130 elimination phase 228 worm burden 128–129 ELISA 228–229 Echinococcus multilocularis Falkland Islands and Cyprus 221–222 control and surveillance 140 hydatid control programmes see hydatid definitive hosts 137–139 control programmes diagnosis 139 in Iceland 219–220 distribution 137 improvement/development. 121 direct rapid immunohistochemical test (DRIT) 49 ectoparasitic zoonoses Dirofilaria Arachnida D. hortense 121 life cycle 141 E. malayanum 121 Diplostomatidae 121–122 Echinostomatidae Dipylidium caninum 142 description 120 direct agglutination test (DAT) 238 Echinostoma spp. area 233 epidemiology and public health lifecycle 219 importance 139 ovine hydatidosis 230–231 treatment 139 parasite eradication/elimination 233 Echinococcus ortleppi 136–137 PCR tests 229 Echinococcus spp. preparatory/planning phase 227 E. granulosus see Echinococcus granulosus tapeworms 218 E. immitis 158 Cheyletiella spp. 169–172 D. dispersal and survival 129 Fasciolidae epidemiology and public health importance description 120 Africa and the Middle East 130–132 Fasciolopsis buski 120 Asia 132–133 fertility control Australia 133 animal reproduction and potential infections 130 targets 260–262 New Zealand 133 animal welfare 266 North America 133–134 characteristics 265 South and Central America 134 disease transmission 260 . animals 14 Dirofilaria immitis 158 innate response 3 Dirofilaria repens 158 ownerless strays 4 fleas pedestrians having eye contact 17. humans and dogs 102 prevention 78 faecal antigen detection test 100 human monocytic ehrlichiosis (HME) infections 101 E. canis-reactive humoral reaction 79 National Notifiable Disease Surveillance indirect immunofluorescence assay 80 System 101 hydatid control programmes prevention and control 103–104 administration models 233 transmission 101 ‘attack’ and ‘consolidation’ phases 229 treatment 103 European 224–225 zoonotic potential and public health nomadic pastoral communities 225–226 considerations 104 ‘Options for Control’ 222–223 Giardiasis see Giardia intestinalis South American 223–224 Gnathostoma spinigerum 158–159 Gnathostomosis 158–159 gonadotropin-releasing hormone (GnRH) ICAM see International Companion Animal agonists 262–263 Management (ICAM) IFA see immunofluorescent antibodies (IFA) IFAW see International Fund for Animal Welfare Helicobacter infections 72 (IFAW) Heterophyidae immunofluorescent antibodies (IFA) 74 description 117 International Companion Animal Management Heterophyes 117–118 (ICAM) 179. Index 273 GnRH 262–263 human–dog relationship human-wildlife conflicts and wildlife animal-assisted interventions 15 disease management 259 animal domestication 1 immunocontraceptives 263–265 attachment theory 13 non-surgical sterilization 267 behavioural data 17–19 public antipathy 259 biophilia hypothesis 13–14 steroid hormones 262 breeding. 264 dog bites 5–6 FSH see follicle-stimulating hormone (FSH) human public health 6 public transportation 6 social support theory 13 gastrointestinal zoonoses sterilization and immunization 19 Campylobacteriosis 69–70 therapeutic effects. animals 15 Helicobacter infections 72 zoonotic diseases 8 Salmonellosis 70–71 human granulocytic anaplasmosis (HGA) 79–80 Yersiniosis 71–72 human Lyme disease Giardia intestinalis diagnosis 78 description 100 enzootic cycle 77 diagnosis 102–103 epidemiology 78 disease. carnivores 2 Filariosis control programmes 16 Brugia malayi 158 effects. 20 description 162–163 physical and psychological health 9 eruption 163. therapeutic settings 7–8 salivary antigens 163 cardiovascular disease 7 treatment 165–166 social conflicts zoonotic implications 164–165 disease 6 follicle-stimulating hormone (FSH) 261. 262. 164 physiological processes 1 erythema and hair loss 163. 164 social and health benefits non-allergic effects 164 animals. 180 Metagonimus yokogawai 117 International Fund for Animal Welfare (IFAW) 36 HGA see human granulocytic anaplasmosis (HGA) HME see human monocytic KAP see knowledge attitude and practice (KAP) ehrlichiosis (HME) knowledge attitude and practice (KAP) 185 . dogs 172 zoonotic potential and public health treatment 172–173 considerations 96–97 zoonotic implications 172 Leptospirosis OVD see oral vaccination delivery (OVD) etiological agents 75 ovine hydatidosis 230–231 leptospiral infection 76 molecular techniques 76 water-borne disease 75 Paragonimidae LH see luteinizing hormone (LH) description 118 luteinizing hormone (LH) 261. africanus 118 Mabs see Monoclonal antibodies (Mabs) P. amazonensis 234 Gnathostoma spinigerum 158–159 L. 118–119 Paragonimus P. 119 Mesocestoides lineatus 143 Pasteurellosis Methicillin-resistant Staphylococcus aureus bacterial zoonoses. 95 infection. disease 95–96 Otodectes cynotis prevention and control 96 description 172 transmission 93. 119 Nanophyetus salmincola 119 Leishmania neglected zoonotic diseases (NZDs) 245 description 233–234 nematode zoonoses L. tropica 234 NZDs see neglected zoonotic diseases (NZDs) Leishmania infantum drug-resistant strains 238 epidemiological screening 243 Ocular larva migrans (OLM) 155 human VL 234 OLM see Ocular larva migrans (OLM) pentavalent antimonials 237 Opisthorchidae reservoir host 234–235 Amphimerus pseudofelineus 117 transmissibility 236 Clonorchis sinensis 111. callipaeda 159 L. 111. mexicanus 118 regional lymphadenopathy 83 P. 120 monoclonal antibodies (Mabs) 45 Plagiorchis MRSA see Methicillin-resistant Staphylococcus P. aethiopica 234 Filariosis 158 L. 117 diagnosis and treatment 96 Opisthorchis spp. 236 nasal and respiratory worms 159 L. 119 Mediterranean spotted fever (MSF) P. description 111 description 93 Metorchis spp. 117 Leishmania spp. javensis 120 MSF see Mediterranean spotted fever (MSF) P. dog bites 69 (MRSA) 74 Capnocytophaga canimorsus 68 Metorchis CDC NO-1 69 M. archibaldi 234 hookworms see Ancylostomatosis L. harinasutai 120 aureus (MRSA) P. heterotremus 118. 117 disease. westermani 118. muris 120 . chagasi 234 roundworms 153 L. 262.274 Index Lecithodendriidae 114. philippinensis 118 Western blot assays 83 P. major 234. conjunctus 117 PCR see polymerase chain reaction (PCR) Mites PEP see post-exposure prophylaxis (PEP) Cheyletiella spp. dogs 96 oral vaccination delivery (OVD) 215 human. albidus 117 CSD 69 M. infantum see Leishmania infantum Thelazia californiensis and T. mexicana 234 toxocarosis 153–156 L. 264 Paragonimus spp. braziliensis 234. 241 Toxascaris leonina 156–157 L. donovani 234. kellicotti 119 epidemiology 84 P. canis 166–169 Plagiorchidae 116. 243 Strongyloides stercoralis 159 L. 169–172 PKDL see post-kala azar Otodectes cynotis 172–173 leishmaniasis (PKDL) Sarcoptes scabiei var. 236. habitat 178–179 rabies 208–211 causes 183–184 pre-vaccination era 206–207 data interpretation Prohemistomum vivax 122 human attitudes and behaviour 186 protozoan zoonoses methods. dog welfare and humane management 181 public health problems 105 dynamics and human attitudes 178 public health and community well-being ethnology 59 cost. 214 human rabies deaths 212 post-kala azar leishmaniasis (PKDL) 234. 212. dog bites 28 CMC 185 costs. society 29 Questionnaires 184–185 incidence. canine carrying capacity. 180 bite and dog-associated factors 27–28 legislation 190–192 bites. health services 26 focus groups/informal dog bite data 25 interviews 184 dog-bite prevention programmes 30–31 KAP 185 dog bites/trauma. Index 275 P. canine rabies 55–56 Coxiella burnetii 73 reproduction control diagnosis 74 CNR 194–196 human infections 74 dog population dynamics 193 IFA 74 rabies vaccination 194 sterilization 193 veterinary services 192 rabies control structural constraints 58 Bali animal welfare association sub-populations 179 (Bawa) 213 suitability. fatalities 28–29 methods/tools context and location. philippinensis 120 post-vaccination era P. dog bites 25–26 Street’ surveys 184 risk assessment. vespertilionis 120 in Africa 207 plague 84 in Japan 207 polymerase chain reaction (PCR) 229. 237 PEP 212 . dog 29–30 monitoring and evaluation victim and site. 239 mass vaccination 207 population management in North America 207 ACOs 190 successful control or elimination. control 188 Chagas disease 97–100 rabies data 188 description 93. immunocontraceptive vaccines 217 236. 94 disease and parasite control 196–197 giardiasis 100–104 dogs removal. street 197–199 leishmaniasis see Leishmania spp. control schemes 34–36 human behaviour 189 human injury ICAM 179. local conditions 182 description 206 tumour-related volatile compounds 177 disease re-emergence 213 wildlife rabies 55 epidemiology 213 post-exposure prophylaxis (PEP) 58. bite injury 26–27 Colombo achievements 201–202 IFAW 36 hierarchy of objectives 199–200 injury human benefit 203 livestock 31 methods of measurement 201 pets 31–32 sterilization project 200 local economy 34 NGOs 182 noise 33–34 oral vaccination physical proximity 36 field trials 57 pollution 32–33 wildlife immunization 56–57 road traffic accidents 32 owner-mediated control 178 urban animal management rules 37 prevention of human rabies 57–58 wildlife 32 prophylactic vaccination immunization 54–55 inactivated tissue culture vaccines 55 Q fever rabies control. callipaeda 159 genotypes 44 Toxascariosis 156–157 immunization 43 Toxascaris leonina 156–157 incubation 46–47 Toxocara leishmaniasis 43 T. infection 81 Paragonimids 118–119 diagnosis 82 Schistosomes 109–111 paralumbar hyperaesthesia 81 Troglotrematids 119–120 tick-borne rickettsial disease 80 Troglotrematidae treatment 82 description 119 Nanophyetus salmincola 119 Phaneropsolus 119 Salmonellosis 70–71 Plagiorchis spp. cati 153 pathogenesis 46 Toxocarosis peripheral organ involvement and animals disease 155 excretion 47–48 epidemiology and control 156 physical properties 44 humans disease 155–156 population management 54–57 mode. brauni 143 histological staining methods 49 T. serialis 143 virus isolation procedures 50 TB see tuberculosis (TB) disease surveillance 51 Thelazia epidemiology 51–52 T. multiceps 142–143 immunofluorescence 49 T. canis 153 sociology 59 trematode zoonoses susceptibility 46 description 109 transmission 46 Dicrocoelioidea 122 virus replication 44 dietary habits and human prevention 122 REA see Restriction enzyme analysis (REA) Diplostomes 121–122 restriction enzyme analysis (REA) 45 Echinostomatoidea 120–121 RMSF see rocky mountain spotted Fasciolids 120 fever (RMSF) Heterophids 117–118 rocky mountain spotted fever (RMSF) Opisthorchids see Opisthorchidae acquisition.276 Index rabies control (continued) Sarcoptes scabiei var. californiensis 159 genome 44 T. mansoni 110 antigenic and genetic variation S. dogs 45–46 Spirometra spp. haematobium 110 vaccination see vaccination S. 120 . dogs 166–168 pre-vaccination era 206–207 treatment 169 strategies 213–214 zoonotic implications 168–169 surgical sterilization 217 Schistosoma surveillance 214 S. DRIT 49 T. canis 153–154 neutralization tests 50 T. RNA virus genomes 44 description 109–110 REA 45 Heterobilharzia americana 111 viral polymorphism 45 Schistosoma spp. canis population management 216–217 description 166 post-vaccination era 207–211 infection. japonicum 110 rabies virus S. 110–111 virus variants. mekongi 110 Mabs 45 Schistosomatidae mutation rate. 143 canine rabies 52–54 steroid hormones 262 clinical symptoms 48 Streptococcosis 74 CNS Infection 47 Strongyloides stercoralis 159 control 54 Strongyloidosis 159 diagnosis cytoplasmic viral antigen 49 diagnostic tests 50 Taenia spp. transmission 153–155 prevention 57–58 T. application 242 transmission 97–98 integration. dogs 98 health education and community human disease 98 support 242 prevention and control 99 insecticides. Index 277 Trypanosoma cruzi diagnosis 238 description 97 dog culling 238–240 diagnosis and treatment 98–99 epidemiological screening 243 disease. treatment 240–241 zona pellucida (ZP) 263–264 control programme 242–243 ZP see zona pellucida (ZP) . and considerations 99–100 leishmaniases 233–234 tuberculosis (TB) research progress 236–237 human contamination 73 reservoir host 234–236 multidrug-resistant strains 73 sandflies. insecticides 240 Mycobacterium tuberculosis 72–73 strategies 237 treatment 237–238 vaccination and Uncinaria 157 immunotherapy 241 VLM see visceral larva migrans (VLM) vaccination approaches 215 Yersiniosis costs and logistics 215 acute gastro-enterocolitis 71 endemic canine rabies 214 antibiotics 72 OVD 215 human infection 71 serological testing 215–216 hygienic measures 71–72 visceral larva migrans (VLM) 155 visceral leishmaniasis (VL) control clinical cases. disease control 242 zoonotic potential and public health Leishmania spp.