Effects of Environmental Change on Emerging Parasitic Diseases

International Journal for Parasitology (2000) 1±11www.parasitology-online.com Effects of environmental change on emerging parasitic diseases Jonathan A. Patz a,*, Thaddeus K. Graczyk b, Nina Geller a, Amy Y. Vittor c Department of Environmental Health Sciences, Johns Hopkins University School of Hygiene and Public Health, 615 N. Wolfe Street, Baltimore, MD 21205-2179, USA. b Department of Molecular Microbiology and Immunology, Johns Hopkins University School of Hygiene and Public Health, 615 N. Wolfe Street, Baltimore, MD 21205-2179, USA c Department of International Health, Johns Hopkins University School of Hygiene and Public Health, 615 N. Wolfe Street, Baltimore, MD 21205-2179, USA Received 18 September 2000; received in revised form 19 September 2000; accepted 19 September 2000 a Abstract Ecological disturbances exert an in¯uence on the emergence and proliferation of malaria and zoonotic parasitic diseases, including, Leishmaniasis, cryptosporidiosis, giardiasis, trypanosomiasis, schistosomiasis, ®lariasis, onchocerciasis, and loiasis. Each environmental change, whether occurring as a natural phenomenon or through human intervention, changes the ecological balance and context within which disease hosts or vectors and parasites breed, develop, and transmit disease. Each species occupies a particular ecological niche and vector species sub-populations are distinct behaviourally and genetically as they adapt to man-made environments. Most zoonotic parasites display three distinct life cycles: sylvatic, zoonotic, and anthroponotic. In adapting to changed environmental conditions, including reduced nonhuman population and increased human population, some vectors display conversion from a primarily zoophyllic to primarily anthrophyllic orientation. Deforestation and ensuing changes in landuse, human settlement, commercial development, road construction, water control systems (dams, canals, irrigation systems, reservoirs), and climate, singly, and in combination have been accompanied by global increases in morbidity and mortality from emergent parasitic disease. The replacement of forests with crop farming, ranching, and raising small animals can create supportive habitats for parasites and their host vectors. When the landuse of deforested areas changes, the pattern of human settlement is altered and habitat fragmentation may provide opportunities for exchange and transmission of parasites to the heretofore uninfected humans. Construction of water control projects can lead to shifts in such vector populations as snails and mosquitoes and their parasites. Construction of roads in previously inaccessible forested areas can lead to erosion, and stagnant ponds by blocking the ¯ow of streams when the water rises during the rainy season. The combined effects of environmentally detrimental changes in local landuse and alterations in global climate disrupt the natural ecosystem and can increase the risk of transmission of parasitic diseases to the human population. q 2000 Australian Society for Parasitology Inc. Published by Elsevier Science Ltd. All rights reserved. Ä o; Global warning; Landuse Keywords: Biodiversity; Cryptosporidiosis; Deforestation; El Nin 1. Introduction Environmental changes and ecological disturbances, due to both natural phenomena and human intervention, have exerted and can be expected to continue to exert a marked in¯uence on the emergence and proliferation of zoonotic parasitic diseases. The ®rst section of this article presents the types of environmental conditions and changes that contribute to proliferation of emerging parasitic diseases. The effects of changes in landuse, especially deforestation and its sequelae, water control projects, road construction, and climatic changes on vectors and their parasites are discussed. The second section focuses on malaria and the zoonotic * Corresponding author. Tel.: 11-410-955-4195; fax: 11-410-955-1811. E-mail address: [email protected] (J.A. Patz). parasitic diseases most commonly affected by environmental changes and which constitute the greatest threats to human populations. The effects of ecological disruption on each of the diseases are discussed within the context of their local environments. 2. Environmental changes affecting transmission of zoonotic parasitic diseases Each environmental change natural phenomenon or through human intervention, alters the ecological balance and context within which vectors and their parasites breed, develop, and transmit disease. The mix of vectors, their biodiversity, abundance, vector competence and human biting behaviour can be affected by any one of the multifactoral changes occurring as ecological stability is 0020-7519/00/$20.00 q 2000 Australian Society for Parasitology Inc. Published by Elsevier Science Ltd. All rights reserved. PII: S 0020-751 9(00)00141-7 formerly forested areas to more densely populated deforested areas with parasite dense human reservoirs for vectors to feed upon and increased interactions. are particularly vulnerable as they lack immunity to the zoonotic parasitic diseases endemic to the area. Bodies of water in disrupted areas Soil type and elevation contribute to determining the type of bodies of water formed in disrupted areas. changes in climate. and raising small animals can create a supportive habitat for parasites and their host vectors. During the processes of landscape fragmentation and urbanization. They may well lack familiarity with self-protective habits that would limit their availability as feed sources to vectors. pH. Puddles with clear water (H . 2. As human settlements move from sparsely settled. the migrants become a reservoir for transmission of parasitic disease endemic to their former home grounds. human. thereby providing changed ecological niches and conditions for proliferation of newly arriving and/ or adaptive existing vectors and their parasites. pigs.5±5.3. using bed nets and remaining indoors during peak biting hours. so too. and climate singly and in combination have been accompanied by global increases in morbidity and mortality from a number of emergent parasitic diseases. canals. small-scale agricultural plots. migrants may come. With the larger reservoirs of infection. ¯ow.5) form in areas with red clay [6]. Vector competence Levels of vector competence vary among species. the vectors may reduce feeding on humans or.5. Each species occupies a particular ecological niche and sub- . Human movement When deforested areas are replaced by crop agriculture.5). commercial development. As the ecology of an area changes. Terrain affects the manner in which water collects in deforested areas: on steep inclines. becomes deforested. Replacement of forests with crop farming. during the process of deforestation. Patz et al.A. conversely. streams are more common than large pools. shape. but also further increase the parasite reservoirs. 2. In addition to an in¯ux of settlers. irrigation systems. enhancing the transmission of their parasite [7]. 5.2. new settlers who are drawn to the edge of the forest for agricultural activities. it is permitted and able to regenerate. changes in type of soil and its degree of water absorption. feed sources [2]. ranching. and if a suitable anthrophyllic vector is present. variously. Introduction of new to-thearea animal species. However. the pattern of human settlement usually changes. Expansion of existing human settlements and movement of human populations create a need for increased food supply.1. water control systems (dams. with the plethora of livestock blood resources. sedimentation and proximity to vegetation and. construction of roads. for example. in either increased or decreased transmission of parasitic disease to humans [1]. e.4. their size. Their resulting increased vulnerability to resident vectors can serve as the kindling for an outbreak of disease. When the forest is cleared and erosion of the soil strips away the thin layer of nutrients. mean precipitation. and latitude. if indeed. and in turn. vectors may multiply and seek additional. 5.5) form in sandy soils when the soil is saturated. Indigenous forest dwellers generally have developed immunity to forest-dwelling parasites. Whereas the forest ¯oor in primary growth tends to be heavily shaded and littered with a thick layer of organic matter that absorbs water and renders it quite acidic (pH 4. / International Journal for Parasitology (2000) 1±11 disrupted. Reduction in water salinity and conversion from acidic to alkaline condition increase fecundity and growth of freshwater vectors such as snails. the incidence and prevalence of parasitic disease. cleared lands are generally more sunlit and prone to the formation of puddles with more neutral pH [3±5] which can favour speci®c anopheline larvae development (described below). the humans not only become ill. that is. the time interval from one landuse to another/others. With livestock to feed up on. or enter the remaining forest for commercial activity such as logging. movement. but foreign to the non-immune resident settlers. and muddy puddles (pH . small animals The replacement of forests with crop farming. ranching. changes in the types and amounts of bodies of water. The new settlement is frequently environmentally different from the settlers' previous home areas and populated with unfamiliar vectors and parasites to which they have not developed protective immunity. reservoirs). and chickens can result. Deforestation and ensuing changes in landuse. 2.2 J. The nature and extent of change in the incidence of parasitic disease are affected by changes in landuse and settlement. 2. human settlements or. Cleared tropical forests are typically converted into grazing land for cattle. All affect parasite and insect vectors. as the forest recedes. Deforestation Deforestation is one of the most disruptive changes affecting parasitic vector populations. there is increased parasite transmission and. left as open areas. elevation. the opportunities for exchange and transmission of parasites increase. such as cattle. changes in vegetation characteristics. temperature. human settlement. there are changes of the species in the area. Crops such as sugar cane or rice may be surrounded by a network of irrigation ditches and arti®cial bodies of water may be formed for small ®sh farms and wells. The response of tropical forests to pertubation is affected by soil type. 2.g. both animals and humans are exposed to new contacts in new environments. it may take up to 50 years or more before the area resembles its former state. leading to changes in the types and amounts of vegetation. through anthelmintic programs. others thrive in irrigation and hydroelectric reservoirs with their frequent changes in water level. Zoophyllic to anthrophyllic orientation In adapting to changed environmental conditions. some vectors display a conversion from a primarily zoophyllic to primarily anthrophyllic orientation. national parks and wildlife reserves.16]. ¯ight range of the vector.A.29. the wide variety of conditions under which at least a few species are able to thrive ensures that parasitic disease is ubiquitous. By providing access to forested and newly deforested areas. In earlier times. There are species which require extensive vegetation cover and inhabit swamps and relatively permanent waterbodies with organic material. Construction of reservoirs and canals can lead to a shift in vector populations. Road construction The construction of new roads provides access for new human. sanitation standards are not aggressively enforced. with all their attendant disruption of the ecological balance. Roads facilitate acceleration of crop farming. increases the association between humans and animals [20±23]. ¯ourishing throughout many regions of the world. building of dams and hydroelectric plants and new settlements.8. having no air tube. whether internal or from external forcings. ¯oat just beneath the water's surface. and biting times in relation to human habits. and is related to the intensity of disease transmission [9±12]. aquaria.34]. Some larvae prefer clear water. Deeply shaded pools. Today. seepages in forests. and new vector species from their far ¯ung points origin. (i. Further. livestock. changes in climate occurred solely through natural processes resulting from phenomena such as changes in the output of the sun or slowing of ocean circulation.9. vector and parasite populations. during construction of dams and canals.7. nontraditional agriculture [21. Riverine pools. and land features. vertical shorelines. others inhabit coastal areas with high salinity. the oceans. and disease control activities are often inadequate or unavailable [17] 2. Establishment of animal conservation and rehabilitation centres. such as snails and mosquitoes.30]. sea ice. and impounded water and seepage. industrial animal production. are exposed to indigenous and newly arrived vectors and their parasites. non-protected populations. mining. Most zoonotic parasites display three distinctive life cycles: sylvatic. freeranging/farmed game species and hunting [13. This interchange is exacerbated by most of the animal conservation operations being localised in developing or underdeveloped countries where public health policies are not well executed. zoonotic. tourists and conservationists. humidity. subsequently. these visiting human populations bring with them and introduce to existing vectors and settlers along the forested/deforested interface. short term ± hours to days ± ¯uctuation). and excavated depressions in the open sunlight all provide areas for mosquitoes to deposit their eggs [18]. In the tropics. conversely. mining pits and irrigation ditches. including reduction of non-human population and increased human population.32. as do zoos. 2. The aggregate effect of temperature. parasitic infections. provide breeding in shallow. The human biting behaviour of vectors are affected by human availability. and dams are closely associated with parasitic disease.J. stagnant surface water exposed to sunlight. Unfortunately. with differences by geographic region and in frequency of chromosomal inversion. Additional breeding sites are provided by creation of basin irrigation for rice. ranching. logging. The parasite eradicated from human and domestic animal populations. 2. their larvae and their parasites.15. its biting frequency. can cause climatic variation and change. 2. tourism and. irrigation canals. for example. and anthroponotic [13±16]. and seaworlds [24±28]. Patz et al. especially in tropical areas. Climate involves variations in interactions among different components of the climate system: the atmosphere. suggesting population adaptation to man-made environments [8].33. Climate and parasitic disease Climate is usually de®ned as the average weather. Some species prefer sunlit pools with turbid water. inhabiting the edges of clean. Changes in any of the climate system components. re-invade human and domestic animal reservoirs [13. solar radiation and wind which are re¯ected in the type of vegetation in plant communities contribute to determining the nature of vector populations [35]. Water control projects Reservoirs. Different mosquito species vary in their habitat requirements. which is facilitated by new access roads. over a period of years and in a particular geographic region. aquaculture [31]. human activities also contribute to . The ponds then serve as breeding grounds. by poor drainage. and emergent vegetation without organic material or salinity. clear. with little or no emergent vegetation. such as construction workers. can survive in sylvatic habitats of national parks or wildlife refuges and then. Construction of roads in previously inaccessible forested areas can lead to erosion [19] and may create ponds by blocking the ¯ow of streams when the water rises during the rainy season. loggers.e. commercial development. The larvae. created by diversion of ¯ow out of river beds. footprints. The degree of a parasite's genetic diversity may also vary among endemic geographic regions. excavation pits provide breeding sites for mosquitoes where they lay buoyant egg masses. miners.6. non-immune. precipitation. in both the larval and adult stages. / International Journal for Parasitology (2000) 1±11 3 populations of vector species are distinct behaviourally. Tropical reservoirs and irrigation systems provide ideal aquaria for rapid reproduction and growth of ¯uke-transmitting aquatic snails. gently moving streams or. However. giardiasis. leading to both more droughts and more ¯oods. Patz et al. Recent mathematical simulations. 3. Altitude can serve as a proxy for temperature. weakening of easterly trade the world [58]. particularly affecting waterborne disease vectors. including parasites. Although global distribution of these changes are expected to be unequal. onchocerciasis. drought [59]. Surveillance systems need to be developed in order to identify association between climatic phenomena and locally appropriate indicators of outbreaks of parasitic disease. in addition to their destructive effect on the stratospheric ozone layer [38].4 J. During El Nin winds causes warm equatorial Paci®c water to migrate from the western to the eastern Paci®c. total precipitation [43]. . Small changes in the mean climate can produce relatively large changes in the frequency of extreme weather events and frequency and severity of heat waves. and gas) increasing the concentration of CO2. there is concern for increased transmission of same tropical diseases and potential for their expansion (of debatable extent) [52] into temperate regions [49±51]. in the East African highlands. because warmer air can hold more moisture than cooler air. during the last ®fty years. Plasmodium falciparum and P. the incubation time of the parasite within the mosquito. there was a rise in average daily temperatures. Halogenated compounds that do not exist naturally are now present in substantial amounts in the atmosphere. S. haematobium in very dry regions with long dry seasons and. calculated the altitudes (which vary by latitude) at which these temperatures occur. the rate with which parasites are acquired and. Temperature and rainfall During the twentieth century. absorbing capacity of forested areas. at an intensity of more than two inches per day [44± 46]. S. ironically. the excess wastewater may be discharged directly into surface water bodies [55. shistosomiasis. resulting in drought in some regions of the world and ¯ooding in others. These in¯uences must be compared with the opposing effects that high temperatures exert in reducing adult mosquito survival. and their capacity to transmit disease are discussed. Examples of parasitic diseases affected by environmental change The primary types of environmental changes that affect the breeding. El Nin excessive rainfall and in southern Africa. deforestation reducing CO2.10.56]. propane) that undergo photo-oxidation in the presence of nitrogen oxides to form tropospheric ozone. Extreme weather has deleterious effects on the population: drought resulting in poor hygiene and reduced food supplies. Äo 2.5 m or less. development. and prolonged recovery of the ozone hole [47]. there will be a 28C rise in temperatures with accompanying indirect effects: a 49 cm. / International Journal for Parasitology (2000) 1±11 climate change: fossil-fuel combustion (coal. The distribution of snails and their Schistoma parasite species are also sensitive to the amount of rainfall and length of the dry season. There were also increases in cloud cover [42]. doubling of atmospheric methane (CH4) from pre-industrial levels [36] with current levels at the highest ever [37].11. temperature determines the rate at which mosquitoes develop into adults. is second only to seasonal variability as the strongest driver of weather variability in many regions of Ä o. ¯oods in contamination. rise in sea level. the hydrologic cycle has changed. El Nin Ä o phenomenon. and proliferation of speci®c parasite species and their hosts. vivax. With a threshold temperature of greater than 208C required to spark an epidemic [54]. Illustrative examples citing malaria. such as malaria. Rainfall intensity is considered a key determinant of the transport of pathogenic micro-organisms. As global warming continues. an increase in hydrologic extremes [38] and enhanced evaporation. surface temperatures appear to have been warmer than any similar period in the last 600 years. oil. higher mean temperatures may also lead to reduced soil moisture due to enhanced evaporation [40]. and frequency in extreme precipitation events. they are expected to result in signi®cant wideranging effect on ecosystems [48]. trypanosomiasis. and loiasis are brie¯y presented. It is expected that by the year 2100. which are sensitive to changes in the hydrological cycles. S.mansoni in regions of medium rainfall and medium-length dry seasons [57].g. Warmer temperatures are expected to lead to a more vigorous hydrological cycle. the frequency of their blood feeding. cryptosporidiosis. During periods of heavy rainfall or melting snow. The length of rainy and dry seasons and the interval between seasons affects larvae and adult vector development and abundance. leishmaniasis. cycling with a frequency of The El Nin every 2±7 years. And. butane. industrial activity and biomass burning resulting in emissions of gases such as carbon monoxide (CO) and volatile organic compounds (e. ®lariasis. respectively. the average temperature decrease with height is 100 m in free atmosphere [53]. 2. causing increased precipitation intensity and more rainfall events. which prolongs the life of vectors. using. and have high greenhouse warming properties. as an example. For example. areas in Africa above 1000±1500 m are considered safe from the spread of malaria. For Ä o results in instance. With an annual rainfall of 2. [39]. japonicum is present only in very wet regions with short dry seasons. Rain provides the breeding sites for mosquitoes and helps create a humid environment.A. the minimum temperatures of approximately 18 and 158C for the development of the malaria parasites. [41]. Transmission of many parasitic diseases is con®ned to the rainy season. when the capacity of a sewer system and/or treatment plant can be overwhelmed. which support large numbers of bromeliads on their branches. falciparum due to limited contact with an infected population. the highly competent malaria vector. malaria [64. wind. thriving in irrigation and hydroelectric reservoirs with their frequent changes in water level. ®nding the newly formed habitat congenial to their survival and proliferation. vivax. Lacking familiarity in dealing with the newly deforested region's environment. darlingi with P. culcifacies. irrigation systems harbour A. inhabits swamps and relatively permanent waterbodies with organic material. contrary to popular belief. cattle herding.61]. in Trinidad.A. during a 50-year period of repeated resowing of rubber plants. balabacensis deposits its eggs in deeply shaded pools and seepages in the rain forests. gently moving streams. maculatus. A. The characteristics of bodies of water. in footprints. A secondary effect of deforestation and initiation of crop agriculture. to a deforested area. minimus larvae inhabit the edges of clean. balabacensis are the major malaria vectors in the hilly regions of Burma. Climatic conditions. and human settlement. suggesting that. were planted to provide shade for growing cocoa. bodies of water and their locations and climate. Each Anopheles species occupies a unique ecological niche. A. there were cyclic malaria epidemics transmitted by A. between and within de®ned geographical areas [9±12]. falciparum. after the construction of a hydroelectric dam in Tucurui in Brazil. between 1971 and 1986. including their vegetation. nuneztovari transmits vivax malaria. falciparum increasing disproportionately to vivax [65. play a role in determining which mosquito species inhabits an area. However. Äo rainfall. temperature. activity. the coastal areas with high salinity. stagnant surface water exposed to sunlight. funestus larvae prefer clear water. melas. Malaria Malaria is ubiquitous in Africa and is ¯ourishing in much of South America and other tropical regions. and A. braziliensis 5 years later [64]. and construction is the in¯ux of new populations from other regions. It has not been determined whether the absence of P. resettled populations may inadvertently engage in practices leading to their becoming infected. In western Venezuela. Some vectors. rapidly leading to an increased incidence of malaria.64]. A. In Sri Lanka.1. Many of the malarial parasite species and their vectors respond sharply to changes in the ecology of their habitat: deforestation. but rather. becoming reservoirs of infection. the type of landuse. Different degrees of genetic diversity in the parasite. in turn. and operates at a different level of vector competence. the A. and. gambiae. mining pits and irrigation ditches. Patz et al. When an environment is altered. a succession of species may occupy the area. mining. altitude. and in excavated depressions in the open sunlight [18]. Following deforestation. are the preferred breeding sites of A. breeding primarily in shallow. A. to be replaced by a different. which collect water. the prevalence of P. Unfortunately. A. the prevalence of P. and Latin America [63. it will disappear. Small increases in existing low temperatures have been shown to exert a disproportionately strong effect on . but not P.68]. / International Journal for Parasitology (2000) 1±11 5 3. falciparum malaria. and the ecological context created determines which indigenous species of mosquito are able to adapt and remain. gambiae in villages close to forest. where malaria is hyperendemic. A. there was a 76% increase in malaria transmitted by A. falciparum may not have been transmitted in the forest [60]. When the bromeliads were removed. humidity. if the indigenous anophelines are not able to successfully adapt to the changed ecology. P. opportunist species that moves into the vacated niche. As the new environment undergoes the process of stabilisation. in the riverine pools created by diversion of ¯ow out of river beds. the vectors are not found in the irrigated ®elds or drains. subsequent to development of mining and migration following deforestation. around shorelines with vertical. which disappear. malaria prevalence returned to its previous level [69]. Thailand and Indo-China. For example. for example. Erythrina trees. related to the intensity of disease (malaria) transmission have been reported from various endemic regions [12] and. requiring extensive vegetation cover. A. For example. A. and which new species arrive. P.66]. falciparum antibodies in the blood samples was attributable to a sparse presence of the vector or a low rate of vector infection with P. deforestation and irrigation have been followed by an increase in P. upsurges of malaria have been co-incident with changes in land-use and human settlement subsequent to deforestation in Africa [60. In Brazil. falciparum malaria transmitted by A. arabiensis in urban and peri-urban areas. malariae malaria were found higher in the Waorani Indians of Ecuador living in permanent settlements with greater ecological alteration than in those maintaining their traditional nomadic lifestyle: indeed. In western Africa.J. density of human population. Pharaoensis. The A. emergent vegetation without organic material or salinity. falciparum. mediopunctatus transmit simian. falciparum antibodies in blood samples of the nomadic group was zero. P. vegetation. The vegetation that supplants the previously forested area frequently promotes an increase in malaria prevalence. Asia [62]. A malaria epidemic ensued because the bromeliads. ¯ooding. minimus and A. only to be succeeded by A. and P. argyritarsis appeared. In an interesting investigation [63].67. gambie prefers sunlit pools with turbid water with little or no emergent vegetation. in the 1940's following deforestation. In Africa. but not human. such as A. clear. bellator. In sub-Saharan Africa. the wide variety of conditions under which at least one mosquito species with a malaria causing parasite can be found to thrive ensures that malaria remains endemic throughout Africa. proliferates. In Malaysia. A. funestus in the savannah. In rural India. and phenomena such as El Nin mitigate toward or against increase in the malaria infection. or refugees. associated with domestic livestock and readily transmitted to humans. there are phlebotomine sand¯ies and leishmaniasis has become a serious problem [88]. 3. 3. However. It is possible that. Most malaria deaths.81]. human populations. In the United Kingdom [93]. the ent parts of the world [73. Wisconsin. serving to increase the prevalence of leishmaniasis [86]. in deaths. Kala-Azar has increased and the sylvatic leishmaniasis vector sand¯ies have become peridomestic. Contamination from leaking septic tanks or agricultural runoff increases the risk for Cryptosporidium contamination of drinking water. for example. As the human population remains in the area.vivax malaria each year between 1934 and 1936. in Milwaukee. in the highlands and lowland fringes). to a combination of the introduction of the parasite to a non-immune population by a large wave of immigrants from an area with endemic leishmaniasis and ecological changes favourable to the sand¯y [90]. New exposure can result in serious outbreaks. the parasite causing Cryptosporidiosis. The 1997/98 El Nin largest in recorded history.3. and are dif®cult to remove from water.80. Increases in temperature have been linked to malaria epidemics in Pakistan [73] and in Zimbabwe [74] where incidence and prevalence of malaria have been closely associated with altitude [75]. Tajikistan. accompanied by their infected dogs. and transmitted by phlebotomine sand¯ies. falciparum and P.2. enter the area. did not occur in El Nin some areas. such as Cryptosporidiosis. in 1993. such as construction workers. / International Journal for Parasitology (2000) 1±11 increased transmission of malaria [70±72]. Twelve years after large areas of forest in Para State in Brazil were cleared and pines and gmelina planted for a paper industry. as the oocyst is resistant to chlorine treatment during periods of heavy precipitation when there is ¯ooding. where there are large shade trees among the coffee plants. In the Caucasus and Volga river basin. had adapted to the changed environment and become infected with leishmanial parasites [87]. In some parts of Latin America. where there were 9 million cases of P. (e. El Nin responsible for all epidemics. the reservoir host of cutaneous leishmaniasis parasite. When non-immune populations. Areas considered vulnerable to a shift in malaria transmission are those above 1000 m where. In a site situated at 2000 m in Western Kenya. an area in which KalaAzar had not been endemic. the ratio of precipitation to potential evapotranspiration is more than 0. during the ®ve wettest consecutive months of the year. Increases in rainfall and run-off intensity leads to heavily contaminated source waters. resulted in torrential rain in parts of East Africa and a malaria epidemic in the southwestern Ä o is certainly not Uganda highlands [82].A. In Rwanda. an excellent reservoir host of visceral leishmaniasis. The Highlands of Africa. the spiny rat. in part. [84]. indicating passage of microorganisms from their source to treated drinking water. Wet and humid environments provide the breeding sites and prolong the life of malaria mosquitoes [72]. Cryptosporidium. It is speculated that the sugar of the ripe coffee fruit may facilitate the development of Leishmania parasites in the vectors [89]. a progressive rise in temperature and heavy rainfall in 1987 and 1988 was correlated with a steep rise in malaria cases. where the largest reported water- . especially in the light of the recent spate of malaria in the Eastern European countries of Azerbaijan.6 J. the Phlebotomus sand¯y transmit the disease to them and they develop large open sores on their faces and arms. In southern Sudan. In the Upper Nile province in southern Sudan. over the years they develop limited immunity and parasite trasmissing results in milder symptoms [57]. Patz et al. Leishmaniasis Leishmaniasis (Kala-Azar) is caused by Leishmania spp. malaria outbreaks have occurred when mean monthly temperature exceeds 188C [77] and rainfall is greater than 150 mm per month. Concentrations of Cryptosporidium oocysts are very small (~5 mm). completing its life cycle within the intestine of the animal that sheds high numbers of infectious oocysts dispersed in their faeces [91]. resulting in reduced malaria [76].g. deforestation has led to an increase in leishmaniasis. With growth of the fox population. represent an ecological zone of special concern [54]. Climate change may increase the risk of reintroduction of malaria unless programs to control vectors are maintained or increased [83]. exceptionally heavy rains may wash larvae from their breeding sites. interspersed with patches of forest. have immigrated. and Turkey [85]. about reintroduction of malaria to these areas and the republics of the former Soviet Union because of their deteriorating health care systems. the extreme Ethiopian epidemics in 1953 and 1958. there is now concern. which resulted in thousands of Ä o years. However. and. usually occur at the end of the rainy season [78]. Ä o-affected areas have recently provided evidence El Nin Ä o years may precipitate malaria outbreaks in differthat El Nin Ä o. where the population has developed little or no immunity. Environmental monitoring in these `transitional' zones is a priority for detecting any change in disease driven by warming trends. Cryptosporidiosis Spread of waterborne zoonotic parasitic diseases. is highly prevalent in ruminants. The former forest has been replaced by areas of farmland. In the Amazon region. resettled populations. it has been suggested that an outbreak of leishmaniasis may have been attributable. affecting both adults and children in areas at extremes of the temperature range.5. Montana [94]. especially at higher altitudes [79]. malaria has been eradicated. and the minimum temperature is 158C or higher [76]. In mountainous coffee-growing regions of Latin America. the sand¯y circulates the Leishmania parasite among small mammals. where malaria incidence is on the rise. a recent US study found 13% of ®nished treated water still contained Cryptosporidium oocysts [92]. Gorilla gorilla beringei. cysts which settle rapidly in the slow moving waters [99]. called Ngana in parts of Africa) and T. In late spring and early fall.A. Trypanosomiasis Trypanosomiasis is caused by Trypanosoma spp. construction of an improved irrigation system and a new canal system resulted in an upsurge in the prevalence of bilharzia. shedding the parasite cysts in their faeces. 3. had become habituated to humans through growing ecotourism and conservation activities. in cattle. Macoma balthica clams. opossums. and rodents serve as host reservoirs for Triatoma.. as described above (under `Temperature and Rainfall'). In the Nile Delta below Cairo and in the Sudan. a Chesapeake Bay. where raw sewage has been used to irrigate a variety of vegetable crops. and migration of infected human population and their domestic reservoir hosts [102] 3. The prevalence of Giardia sp. The abundance of the parasite is in direct proportion to that of the snail population. When there is deforestation. and in the Mekong River area of IndoChina. managed program [101]. in the African Sahel zone they inhabit the river banks. so cattle ranching is often con®ned to dry areas where tsetse ¯ies cannot survive. in some instances leading to afforestation.J. oil palms and mangoes. who come to work the land and tend the herds. contaminating the sediment [22]. adaptation of reservoir hosts and wild vectors to peripheral and living areas as the sole feeding source. The overstocking results in poor quality cattle and causes land degradation. before escaping into water. year-round irrigation became possible and snail populations swelled. cysts settle to the bottom. infections in the gorillas habituated to humans was considerably greater than that of the nonhabituated gorillas [23]. japonicum. as the snail is pumped along with the water [57]. which provide comfortable habitats for tsetse colonisation. altering the ecological balance between reservoir hosts and wild vectors. Similarly. coffee. beaver (Castor canadensis) and muskrats (Ondatra zibethicus) serve as ampli®cation hosts for Giardia sp. Areas were enclosed so that natural vegetation could recover. In Africa. The larvae dwell in their intermediate host. primarily S. S. burrow in the mud or sandy-mud substrata.6. the prevalence of bilharzia parallels the degree of irrigation intensity. Maryland subestuary. The African forms are transmitted by the tsetse ¯y (Glossina) and Chagas' disease by contamination of the Triatoma bug with infected insect faeces and by transfusion of contaminated blood. In Colorado.1. for about 1 month. In Iran. feeding on the surface sediment layer. with temporal variations. and S. moving into drier areas during the rainy seasons and returning to the forests during dry seasons [57]. As the tsetse ¯y requires the protection of vegetation or forests.97]. not only seasonal rain variation and changes in water temperature and ¯ow.: T bruci varieties gamiense and rhodesiense cause Gambian and Rhodesian trypanosomiasis (African sleeping sickness). cysts [100]. the snail. but also by the abundance of snails. armadillos. mansoni. domestic and peridomestic animals such as dogs. In the Salta area of Argentina. compromising the ef®ciency of the drinking water treatment plant [96. cysts. It has been predicted that the Brazilian Amazon is at risk for Chagas disease becoming endemic due to the con¯uence of a number of factors-uncontrolled deforestation and colonisation. . / International Journal for Parasitology (2000) 1±11 7 borne disease outbreak occurred. when a storage dam was added to the original Gezira irrigation system of the central Sudan [103]. in the Delaware River. which harbour Giardia sp. The intestinal form of bilharzia has prevailed throughout the Gezira irrigation system since 1970. especially among those working and living within the immediate area [57]. Human populations. an association was found between the amount of rainfall and the number of Cryptosporidium oocysts [98]. it is not economically feasible to raise cattle on large areas of land due to high prevalence of tsetse ¯ies. throughout the year.5. these effects are exacerbated if the forest is replaced by tall crops such as cocoa. In Central and South America. length of the rainy and dry seasons. As the waters are slow moving. An example of the introduction of a parasitic disease to an animal species by a human population occurred in Uganda. Patz et al. compatible with the environment. Shistosomiasis (Bilharzia) Shistosomiasis (Bilharzia) is caused by the Shistosoma blood ¯ukes. In Marrakech. The Ugandan mountain gorilla population.6. With the construction of the Roseires and Aswan Dams in Egypt. S. haematobium.4. and hence that of the parasite changes in the type and quantity of vegetation. and cattle grazing was conducted under a controlled. seeking a human host. Giardiasis Giardiasis is caused by Giardia lamblia. cruzi causes South American trypanosomiasis (Chagas' disease). japonicum. Shistosoma species vary considerably in their preferences for amount of rainfall. the waterborne Giardia sp. mekongi which closely resembles S. Trematode 3. The severity of the Milwaukee outbreak has been attributed to the heavy spring rainfall and runoff from melting snow with a subsequent turbidity load. which is harboured by a variety of animals and crops. Snails egg laying is dependent on the type of vegetation in the habitat. potatoes irrigated with raw waste water were contaminated with Giardia sp. and interval between rainy and dry seasons. cats. are vulnerable to infection. 3. on its way to infecting humans. has restored the original productivity of the ecosystem. good livestock management. they contaminate surface waters downstream from their dams with Giardia sp. In the Rhode River. with an estimated 403 000 cases of intestinal illness and 54 deaths [95]. subsequent to the construction of the Three Gorges high dam on the Yangtze River. West. with more infective parasites at the beginning and end of rain [107]. In the Orient. British Guinea. polluted by faeces of domestic animals.58:195±203. aquasalis transmitted on the Demerara River estuary. Packer MJ.7. Science 1995. changes in soil moisture have preceded changes in prevalence of Bancroftian ®lariasis [105]. In Central and West Africa.8 J.15:468±74. Spp.2. Parasitol Today 1997. Amazonia: fundamentos da ecologia da maior regiao de ¯orestas tropicais. [8] Conn JE. 3. Ecological change as a factor in renewed malaria transmission in an eradicated area: a localized outbreak of A. the vector's natural habitat is dense forest and the forest edge with the forest swamp serving as the breeding ground. 3. In India.Y. and the social and physical sciences holds out the best hope for developing comprehensive risk assessment to aid local. annual rainfall.3:166±70. it has also adapted to rubber plantations [108]. The examples cited in this brief review demonstrate the close relationships among landuse. Further investigation and exploration are needed in order to gain a better understanding and control of these forces so as to prevent increasing damage to our ecosystem and reverse the rising morbidity and mortality from parasitic disease. Freitas-Sibajev MGR. Mali and future prospects. Central and East Africa.A. Guatemala and Mexico. and in the Nile delta. Culex and Anopheles mosquitoes. and human behaviour that are associated with disease transmission. In each of the areas in which it occurs. Transmission intensity and Plasmodium falciparum diversity on the northwestern border of Thailand. and wandering pigs and cows destroy the banks of unlined drains. Population structure of Plasmodium falciparum in villages with different malaria endemicity in East Africa.71(2):125±32. [9] Babiker HA. creating shallow larval habitats [106]. the vectors breed during the wet season and peak biting density occurs at the height of the rainy season.7. Hackford I. the snail distribution and annual prevalence of human schistosomiasis varied signi®cantly in accordance with water levels in the Yangzte River. darlingi and malaria eradication. El bosque y las formaciones vegetales en la llanura amazonica del Peru. river blindness is most common along the main river valleys. climate variability and human disease. 4. Loiasis Loiasis (calabar swellings). 1985. their hosts and vectors. [5] Marques AC. Ind J Malariolog 1951.6:95±114. Mating patterns in malaria parasite populations of Papua New Guinea. Deforestation and epidemic malaria in the wet and intermediate zones of Ceylon. Momen H. national and international governments and decision makers. Improved surveillance and monitoring is needed so as to detect changes resulting from global climate and ecological change. et al. Onchocerca volvulus. transmitted by Aedes.1. Walmsley M. Although deforestation reduces its prevalence. genetic and behavioural characteristics of vectors and parasites. Molecular population genetics of the primary malaria vector Anopheles darlingi using mtDNA. [6] Encarnacion F. [12] Babiker HA. Am J Trop Med Hyg 1997. [2] Giglioli G. . Bull World Health Org 1963. Hill WG. it is transmitted by a different species of Simuliidae. [11] Paul REL.5(1):135±61. [3] Tyssul Jones TW. Alma Mater 1993. Ecuador. rice cultivation and ¯ooding are associated with increased prevalence of ®lariasis [57]. they can provide insight into associations among ecological factors. [10] Paul REL. provide breeding grounds. Walliker D. Simuliidae. Patz et al. Filariasis Filariasis is most commonly caused in humans by the Wuchereria bancrofti parasite. [4] Sioli H. Acknowledgements Funding for A. Patz was provided through a grant from the New York Community Trust. Human migration and the spread of malaria in Brazil.7. Luz SLB. [7] Southgate VR.56(1):41±147.3. Shistosomiasis in the Senegal River Basin: before and after the construction of dams at Diama Senegal and Manantali. In the Plateau State in Nigeria. Am J Trop Med Hyg 1998. Current views on the population structure of Plasmodium falciparum: implications for control. rapids or white water on spillways and water control structures provide breeding sites for the black¯y. Rev Saude Publica 1991. References [1] Service MW. Walliker D.25:165±78.269:1709. Lines J. In Nigeria. Parasitol Today 1987. is caused by Loa loa and transmitted to humans by the bite of the Chrysops ¯y. J Helminthol 1997. 3. Multidisciplinary co-operation among workers in public health. entomological. In Africa. standing water. in the ®fteenth year of A. the water table.7. yearly evaporation and ground altitude [104]. Agricultural development and arthropod-borne diseases: a review. and transmitted by the bite of the black¯y. both for identi®cation of immediately required action and to serve as the basis for developing predictive models. and poor husbanding of natural resources has modi®ed the distribution and behaviour of parasites. J Am Mosquito Contrl Assoc 1999. Onchocerciasis (river blindness) Onchocerciasis is caused by the parasite.A. Tissue Nematodes 3. / International Journal for Parasitology (2000) 1±11 In China. Petropolis: Vozes Ltda. especially deforestation. Vittor and partial funding for J. Brockman A. Coping with the future The continued disturbance of natural ecosystems by destructive changes in landuse. in a direct association with density of the snails.29:131±45. Such models can serve as effective aids in developing strategies and mechanisms for minimising parasitic disease consequent to expected changes in the environment.13:262±7. ecology. Gockowski J. Cambridge: Cambridge University Press.78(6):1107±19. Boca Raton. Am J Trop Med Hyg 1998. Lowenstine LJ. Knight RW. Emerg Infect Dis 1998. Grassl H. [20] Fowler ME. J Climate 1994. Ropelewski CF. Harris N. [22] Graczyk TK. Seattle. Korotkevich YS. Calitz EM. Health and climate change. World Meteorological Organisation/United Nations Environment Programme. Graczyk TK..392:589±92. B Am Meteor Soc 1996. Advances in Trematode Biology.15:91±114. pp. Am J Trop Med Hyg 1997. Global Change & Human Health 2000. Husbandry and disease of camelids. The effect of climate change on ozone depletion through changes in stratospheric water vapour. Wrangham RW. Manual on environmental management for mosquito control. Environmental Change and Human Health. Karl TR. Nature 1999. Special challenges of maintaining wild animals in captivity in North America. with special emphasis on the black-footed ferret (Mustellla nigripes). Rev Sci Technol 1996. Patz et al. From pan to pandemic. 1993..85(6):1168±70. Cryptosporidium sp. Kattenberg A.1(1):10±25. pp. Bretsky PM. subarctic and temperate regions: Greenland.50(6 Suppl):134±44.57(4):457±63. Climate change 1995. J Parasitol 1999.76(1):33±45. Van Kruiningen HJ. Boardman W. Kattenberg A. Geneva: World Health Organisation.213:1559±60. Randolph SE. Perciasepe R. Increased cloudiness in the United States during the ®rst half of the twentieth century: fact or ®ction? Geophys Res Lett 1990. and Giardia sp. Department of Natural Resources. 285±357. Maskell K. editors. Secular trends of precipitation amount. Patz JA. 383±404. the Scandinavian countries and the Baltic States. Banoita S. [26] Williams ES. Engelberg D. London. The effects of changing weather on public health. pp. Karl TR. in Earthscan. Easterling DR. Development of Fasciola hepatica in the intermediate host. 1999.402:399±401. Trichinella in Arctic. 1998. [28] Michalak K. Science 2000. [19] Geoecologia y desarollo Amazonico: estudio integrado en la zona de Iquitos. Groisman PY. Infectious and parasitic diseases of captive carnivores. Jouzel J. 1998. Rev Sci Technol 1996. Indices of climate change for the United States. semi-ranging and captive cervids. Rogers DJ. Chappellaz J. Parker DE. J Vet Med Assoc 1998. Martens WJM. Karl TR. and irrigation systems. Arthropods as disease vectors in a changing environment. Keith DW. Karl TR. Variability and trends of precipitation and snowfall over the United States and Canada. Barnola JM. Am J Trop Med Hyg 1994. editors.A. Knight RW.377(6546):217±20. Knight RW. Annual Rev Public Health 2000.67:151±4.58:501±4. pp. Cambridge: Cambridge University Press. Barry RG. editors. London: Routledge.289:1763±65.15:155±69. Deforestation hunting and the ecology of microbial emergence.7:184±205. Offset Publication Number 66. 1998. 1996. [33] Weiss RA. Easterling DR. Epidemiologic aspects of 42 cases of human brucellosis in the Republic of Djibouti. [18] World Health Organisation. [25] Schultz DJ. editors. Flores Paitan S. Larsen JL. The science of climate change. Husbandry practices as related to infectious and parasitic diseases of farmed ratites. Rankuwa Hospital. Diesel S. infections in mountain gorillas (Gorilla gorilla beringei) of the Bwindi Impenetrable National Park.345:127±31. Shane SM. [30] Gavazzi G. The 1995 Chicago heat wave: how likely is a recurrence? Bull Am Meteorol Soc 1997. Alves D. [21] Hunter DL. Giorgi F. Sulkava: Finnreklama Oy. London: E&F.15:251±66. Cambridge: Cambridge University Press. [23] Nizeyi JB. Maskell K. Hintsa EJ. Dalsgaard I. [27] Hannah HW. Global Ozone Research and Monitoring Project Report No. In: Houghton JT.17:1925±8. Meira-Filho LG. In: Kalliola R. Cartter ML. Quayle RG. Simonds J. Climate models projections of future climate. Combined sewer over¯ows: where are we four years after adoption of the CSO control policy? Washington (DC): EPA Of®ce of Wastewater Management. Gruza GV. Vibrio damsela associated with diseased ®sh in Denmark. 1996. WA: Water and Land Resources Division. pp. Chichester: Wiley. [14] Graczyk TK. Thorne ET. 1998. Emergence of raccoon rabies on Connecticut 1991±1994: spatial and temporal characteristics of animal infection and human contact. 65±131. Hay IT. and intensity in the USA. Rev Sci Technol 1996. 1998. Geneva: World Meteorological Organisation. Bacon MJ. Nature 1995.N. J Parasitol 1999. An investigation of the relative morbidity of zoonoses in paediatric patients admitted to G. Raynaud D. canals. Plummer N. Karl TR. Sutherst RW. Callander BA. Schimel D. Uganda. pp. Cran®eld MR.79:231±41. Fried B. 1982. King County water quality assessment: assessment of public health impacts associated with pathogens and combined sewer over¯ows. Tuberculosis in free-ranging. Martens P. Wood BL. Buick WW. [32] Wilson ML.15:171±81. Baudet JM. Nanteza A. Special challenge of maintaining wild animals in captivity in Australia and New Zealand. Callander BA. Harris N. Bull Amer Meteor Soc 1998. In: Dalton JP. Odendaal JS. Zoos and veterinarians. 1996. editors.28(Suppl 1):14±19. The science of climate change. Bull World Health Org 1998. Jobin W. 25. Nature 1999. Scienti®c assessment of ozone depletion: 1994.15:73±89. Fasciolosis. Application of remote sensing to arthropod 9 [36] [37] [38] [39] [40] [41] [42] [43] [44] [45] [46] [47] [48] [49] [50] [51] [52] [53] [54] [55] [56] [57] [58] vector surveillance and control. Eitel MN. Egberson SH. New York: CAB International.77:279±303. Austin C. Anderson NG. Mwebe R. Rose JB. some legal issues. Callander BA.63(9):3711±5. Steurer PM. Fried B. [16] Graczyk TK. Karl TR. Increased polar stratospheric ozone losses and delayed eventual recovery owing to increasing greenhouse-gas concentrations. [24] Cambre RC. [15] Graczyk TK. 133±92. present and future. The global spread of malaria in a future. Knight RW. Malaria in the African highlands: past. Cran®eld MR. Halpert MS. Nature 1990. Zimmerman P. et al. Nicholls N. et al. Lorius C.289:1763±65. [17] McCrindle CM.A.J. Ogallo LA. 124±45. 31±46. Appl Environ Microbiol 1997. editor. 1992. Peru. Kattenberg A. Lindsay SW. Ecological design and health impacts of large dams. Last J. Capillaria hepatica (Nematoda) infections in human-habituated Mountain gorillas (Gorilla gorilla beringei) of the Parc National de Volcans Rwanda. Maskell K. Mycobacterium tuberculosis infection as a zoonotic disease: transmission between humans and elephants. Rind D. In: Houghton JT. Kirk-Davidoff DB. Global and regional scale precipitation . Trends in high-frequency climate variability in the twentieth century. Ice-core record of atmospheric methane over the past 160 000 years. Kattenberg A. Climate change 1995. Rev Sci Technol 1996. Shindell DT. Lonergan P. Cooper GH.85(6):1084±8. warmer world. et al. et al. Immunobiology of trematodes in vertebrate hosts. 1995. Nature 1998.15:289±308. [29] Tully TN. Rev Sci Technol 1996. Prigent D. Southeast Asian J Trop Med Public Health 1997. [34] Wolfe ND. Maslow JN. Climate change 1995. [35] Washino RK. Kalema GRNN. / International Journal for Parasitology (2000) 1±11 [13] Kapel CM. In: Houghton JT. Graczyk TK. [31] Pedersen K. In: Fried B. Observed climate variability and change. MeiraFilho LG.57:365±8. 1997. Rev Sci Technol 1996. Radiative forcing of climate change. FL: CRC Press. Harris N. Meira-Filho LG. Hough IJ. Enting I. frequency.397:385±6. Daoud W. The science of climate change. Echniostomiasis: a common but forgotten food-borne disease. Mountain weather and climate. Med Tropicale 1997. Spon. et al. J South African Vet Assoc 1996.4(2):283±7. Tadei WP. Am J Public Health 1997. some of their habits and relation to malaria in endemic areas of Rondonia state. 1988 (mimeographed document). Climate change and malaria risk: an integrated modelling approach. DC. 1999. Davis JP. new tools: the impact of climate change on infectious diseases.25:82±88. pp. editor. Phinichpongse S. War in Tajikistan and re-emergence of Plasmodium falciparum. Yost J. / International Journal for Parasitology (2000) 1±11 Ä o southern oscillation. Prevalence of Giardia sp. Birley MH. 1±42. Bouhoum K.84(4):501±14. Emerg Infect Dis 1998. Malakooti MA. Kilian AHD.331(3):161-7. 1979. Di Deco. West Africa. el-Hassan AM. braziliensis guyanensis). Taylor P. Banatvala N. Trop Med Int Health 1997. Kala-azar in displaced people from southern Sudan: epidemiological. 1993. Bilthoven. Scorza JV.45(1):1±33. Mutambu SL. Monzingo Jr.93:22±23. Montoya-Lerma J. Monthly patterns associated with the El Nin Weather Rev 1987. Boca Raton. Bromeliade malaria in Trinidad. and apparent absence of 'pian bois' (Le. Harinasuta C. Stevens RH. Lindsay SW. Trans R Soc Trop Med Hyg 1993. 1. Petrarca V. Mac Kenzie WR. Surveillance for waterborne-disease outbreaks-United States 19931994. Dubey JP. Bouma MJ. A review of the malaria situation in Zimbabwe with special reference to the period 1972-1981. Am J Public Health 1983. Santos JMM. Martens WJM. Lourenco-de-Oliveira R.111:517±28. Nin Freeman T. Marquez M. Warburg A. Lindsay SW. Malaria: principles and practise of malariology.73(5):483±97. Monograph on water resources and human health in Europe.26:47±66. Hoxie NJ. Castillo L. Demography and vector-borne diseases. Human tropical diseases in a changing environment. Coluzzi M.87(12):2032±5. McGregor I. London: Department of the Environment. El papel d cafeto en la endemicidad de la leishmaniasis cutanea en Venezuela. Calderon RL. New challenges. Demographic changes and their in¯uence on the epidemiology of the American leishmaniasis. Lainson R. Di Deco MA. Cryptosporidium and Cryptosporidiosis. The effect of waste water reuse in irrigation on the contamination level of food crops by Giar- [59] [60] [81] [82] [83] [84] [61] [62] [85] [86] [63] [64] [65] [66] [67 [68] [87] [88] [89] [90] [91] [92] [93] [94] [69] [70] [71] [72] [73] [74] [75] [76] [77] [78] [95] [96] [97] [98] [99] [100] [79] [80] . Temperature is predictive of severe malaria years in Zimbabwe. Anonymous. Kabagambe G. pp. Rezzano S.87(Suppl 2):3±11. Hibler CP.1:86±96. Craun GF.21:1 21. Giardia and Cryptosporidium in raw and ®nished water. Frontier malaria in the amazon region of brazil: types of malaria situations and some implications for control. Speer CA.A. Med Vet Ent 1990. FL: CRC Press. Fayer R. 146±70. Boca Raton. In: Fayer R. Variation of the vectorial capacity of some anophelines in western Venezuela. History of malaria from prehistory to eradication. Trans R Soc Trop Med Hyg 1979. Pickering H. Bunnag T. Sharipov A. J Am Water Works Assoc 1995. Anopheline Species. A malaria control trial using insecticide-treated bed nets and targeted chemoprophylaxis in a rural area of The Gambia West Africa. Lancet 1994. et al. Pan American Health Organization. Ann Trop Med Parasitol 1996.87(9):54±68. van der Kaay HJ. 21st SEAMEO-TROPMED Seminar: environmental impact on human health in southeast and east Asia. Dutary Thatcher B. Am J Trop Med Hyg 1946. Effect of rainfall on giardia and crypto.115:1606±26. Bol Direcc Malar Saneam amb 1985.90:573±88. Rojas W.344:1638±9. World Health Organisation. LeChevallier MW. Leishmaniasis vector potential Lutzomyiaspp. Am J Trop Med Hyg 1980. In: Environmental change in human health. Pearcy BE.2:445±51. et al. et al.90(9):66±80. Bradley M. Cruz-Ruiz AL.10 J. Ostrovska K. Lippy EC. Bruce-Chwatt LJ.29(2):298±312. British West Indies. Mor Mortal Wkly Rep CDC Surveill Summ 1996. Zijlstra EE. FL: CRC Press. Bradley DJ. Lancet 1998.85(3):365±9. Ecological observations on Anopheline vectors of malaria in the Brazilian Amazon. European Centre for Environment and Health/European Environment Agency. Department of Health 1990. Chromosomal inversion intergradation and incipient speciation in Anopheles gambiae. Sao Paulo 1988. p. Kaplan JE. Asmama S. Presented to the symposio sobre a malaria. A review of the epidemiology and control of malaria in The Gambia.90:232. Trans R Soc Trop Med Hyg 1986. in plantations of introduced tree species and in other non-climax forests in eastern Amazonia. Poveda G.4:671±6. Arle M. 1±59. The general biology of Cryptosporidium. et al. Cryptosporidium in water supplies. Chromosomal differentiation and adaptation to human environments in the Anopheles gambiaecomplex. Halpert MS. Jaramillo C. Alterholt TB. pp. Pittendrigh CS. Weniger BG. Chichester: Wiley. LeChevallier MS. Epidemic malaria in India and the El Ä o southern oscillation. editors. Blair KA. Am J Trop Med Hyg 1994. Da Gama AE.50(4):420±4. Patz JA. Global and regional scale precipitation Ä o southern oscillation Monthly patterns associated with the El Nin Weather Rev 1987. 1989.73(8):868±72. In: Wernsdorfer WH. Greenwood BM.2(12):1122±7. Sabatini A. 1994. Nashold RD. Norton WD. Langi P. Rotmans J. editor. Talisuna A. Juranek DD. et al. Larrick JW. Hoxie NJ. Rubio-Palis Y.5:9±16. Report CD33/INF2. Rome: WHO. Trans R Soc Trop Med Hyg Nin 1999. Norton WD. an isolated Amerindian population. Trans R Soc Trop Med Hyg 1991. Climatic warming and increased malaria incidence in Rwanda. van der Kaay HJ. A massive outbreak in Milwaukee of cryptosporidium infection transmitted through the public water supply. clinical and therapeutic ®ndings. Am J Trop Med Hyg 1998. Biomndo K. Sawyer D. N Engl J Med 1994. Pitt S.343:714±8.77(6):775±85. Downs WG. Shaw JJ. Sornmani S. 1997. Tokyo: Tsukuba. Satarov K. An outbreak of waterborne giardiasis associated with heavy water runoff due to warm weather and volcanic ashfall. Surveillance of water-borne parasitic infections and studies on the impact of ecological changes on vector mosquitoes of malaria after dam construction. in a beaver colony and the resulting environmental contamination. Shanks DG. Lancet 1994. Edinburgh: Churchill Livingstone. Gedrose J. 1988. Vergeront JM. Washington. Amazon region of Brazil. Cryptosporidiosis-associated mortality following a massive waterborne outbreak in Milwaukee Wisconsin. Predicting high-risk years for Ä o southern oscillamalaria in Columbia using parameters of El Nin tion. Kramer MH.23(4):576±85. Rainfall pattern El Ä o and malaria in Uganda. Infectious disease patterns in the Waorani. Lainson R. Ali MA. J Wildl Dis 1987. Blaser MJ. In: Service MW. Bouma MJ. Ropelewski CF. Climate change and malaria transmission. Amahmid O. et al. Niessen LW. 85. Ä o southern oscillation and Bouma MJ. Coluzzi M. Herwaldt BL. Leishmaniasis in Brazil: XX Prevalence of `enzootic rodent leishmaniasis' (Leishmania mexicana amazonensis). J Am Water Works Assoc 1998. DL. M.A.52:45±63. Bull Zool 1985. Trans R Soc Trop Med Hyg 1996. in Colombian coffee plantation. Patz et al. Ready PD.59(2):325±35. Mem Inst Oswaldo Cruz 1989. Loevinsohn M. Juranek DD. Trans R Soc Trop Med Hyg 1983. Proctor ME. Status of malaria programs in the Americas. Curr Opin Microbiol 1999.352:1279. The El Nin the historic malaria epidemics on the Indian subcontinent and Sri Lanka: an early warning system for future epidemics? Trop Med Int Health 1996. Petrarca V. Marquez C. Re-emergence of epidemic malaria in the highlands of western Kenya. Rosen JS. The Netherlands: Rijksinstituut voor Volksgezondheid en Milieuhygiene.80:12±19. Xu XJ.76:557±80. Giordano CM. 1 Zoological Journal of the Linnean Society 51. 1990. Chen LY. Bucher EH. McLaren M. London: Academic Press. Rao DR. .3(3):234±5. Malone JB. Behavioural aspects of parasitic transmission. editor. O. In: Canning EU. Bancroftian ®lariasis distribution in the southern Nile delta: correlation with diurnal temperature differences from satellite imagery. local disease perception & treatment. The assessment of a 3 year snail control programme in the Gezira irrigated area Sudan. Emerg Infect Dis 1996. pp. Reuben R. Yang XX.36(2):153±60.13:79±82. [108] Duke BOL. Funatsu RK. PEEM/WP/10/90. [106] Rajagopalan PK. Ann Trop Med Hygiene Parasitol 1982. pp. Amin M. Int J Food Microbiol 1999. and vector/parasite dynamics. Toledo C. Harb M. Chagas. Solbrig. Behavioral aspects of the life cycle of loa. I±A short review. disease in the Brazilian Amazon. Junqueira AC. / International Journal for Parasitology (2000) 1±11 dia cysts and Ascaris eggs. Onchocerciasis in Plateau State Nigeria: ecological background. Lines JD. J Hyg Epidemol Microbiol Immunol 1992. 121±38. Dai YH. Ufomadu GO. Self LS. 11 [101] [102] [103] [104] [105] Thompson DF. 1972. Appropriate technology in vector control. Supplement No. Wright CA. In: Curtis CF. Environmental and water management for mosquito control.30(3):549±55. FL: CRC Press. Livestock management and disease vector control 1990.mimeographed. Coura JR. Teesdale C. Fenwick A. editors. et al.A.49(1-2):19± 26. Das PK. 97±107.6 . Interciencia 1998. Destruccion o transformacion de paisaje tropical sudamericano?. Yu GY. Southeast Asian J Trop Med Public Health 1999. [107] Nwoke BE. Boca Raton. Impact of environmental change and schistosomiasis transmission in the middle reaches of the Yangtze River following the Three Gorges construction project. Revista do Instituto de Medicina Tropical de Sao Paulo 1994(4):363±8. Patz et al.J. Paniker KN. Onwuliri CO. Su ZM.