J. Nutr.-1968-Buss-421-6
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Gross Composition and Variation of the Components of Baboon Milk during Natural Lactation' DAVID H. BUSS Division of Biological Growth and Development, Southwest for Research and Education, San Antonio, Texas Foundation ABSTRACT The characterization of natural baboon milk was undertaken to pro vide information on the dietary requirements of infant and lactating female baboons (Papio anubis, P. cynocephalus and P. papio). The gross composition of the mature milk (days 36 to 279) was as follows: (in grams per 100 ml) total solids, 14.4; lipids, 5.0; crude protein, 1.6; lactose, 7.3; and ash, 0.26. The specific gravity and pH were 1.027 and 7.18, respectively. The mammary secretion obtained during the first 5 days of lactation was richer in crude protein and poorer in carbohydrates than the mature milk, but the lipid and ash concentrations were not appreciably different. Variations in those components with each other, with length of lactation and with milk yield were also determined; as lactation progressed, the only significant change in composition was the increase in lipid concentration. Downloaded from jn.nutrition.org by guest on July 13, 2011 Adequate lactation is of critical impor tance to the maintenance of any mam malian species. The quantity and compo sition of the milk not only determine all the nutriments which the infant receives, but also reflect the nutritional status of the mother at a time when her requirements are especially stringent. Human lactation has been studied in detail (1), but, despite the extent to which subhuman primates are now being used as models for man in health research (2), very little is known about lactation in any other primate. A few reports of the gross composition of primate milk have been published (3—8); of these, two were concerned with baboon milk. Van Zyl (5) determined the choles terol, lipid phosphorus, lipid and iodine contents, and Vice et al. (7) determined only the lipid content. Baboons are among the most used of laboratory primates, because of their many physiological similarities to man (9, 10). It is, therefore, important that their nutri tional requirements be known. To better elucidate the requirements of both infant and lactating baboons, we have analyzed baboon milk more completely. This paper reports the gross chemical composition of the milk obtained when lactation was maintained by the suckling of the infant. The variations of the components with the length of lactation, with the size of the sample and with each other are also preJ. NUTRITION, 421-426. 96: sented, together with an indication of the changes occurring in the gross composi tion of the milk in the final stages of lactation. MATERIALS AND METHODS Animals. The 26 lactating baboons {Papio anubis, P. cynocephalus and P. papio) used in this study were fed a diet of a standard biscuit (11) and water, ad libitum. Their infants were all born naturally. MiZfesamples. At approximately week ly intervals the baboon to be milked was sedated with 0.75 mg/kg l-(l-phenylcyclohexyl)piperidine hydrochloride,2 and the infant was removed. The nipples were prepared as described elsewhere (12) and, approximately 20 minutes later, 20 IU of a purified oxytocic preparation 3 were in jected intravenously. The milk flow began almost immediately, and the samples were obtained by gentle manual massage of the mammary tissue and stripping of the teat in one motion with the thumb and fore finger. More than 85% of the samples con tained between 3 and 12 ml of milk. To prevent its rejection, the infant was reReceived for publication May 9, 1968. 1Supported by Public Health Service Research Grant no. GM-13252 from the Division of General Medical Sciences. Parke, Davis and Company, Dallas, 2 Sernylan, Texas. 3P.O.P., Armour-Baldwin Labs., Omaha, Nebraska. 421 This ono RWQX-7UD-P6ZR Mallinckrodt Chemical Works. Chicago. (18). the samples were allowed to reach room temperature and were well mixed before portions were re ti*IHO)IH^IOrHti0rHetv^coIOr-lciCOIHital tis0rt^§oti00 moved for analysis. days of lactation) was investigated by a -tÃ-"rO modification of one of the methods of «li5NSo•iljjn Jenness et al. lipids.org by guest on July 13.. total solids. Missouri.'C ooC. carbohydrate and ash. The supernatant solution was di QProperty luted with an equal volume of water and deionized by passage through a column of mixed ion-exchange resins5 and elution osi °II*' with water. For determinations of the gross chemical composition. specific grav ity. The total solids and ash were deter mined by AOAC methods (14). ' ! constituentgO0+1fHCOO«HÃŽ^~sCOOootigM E.1 ml with 0. Louis. The eluate was separated by (dir«i^otirH1><n\^s00o+1cot-iH^^t^Oti^c-CN•*^<NCOCDg/100 ethyl acelactose baboons H. Illinois.|HCNCOCNg/100 (16) and calculated as N X 6.nutrition. computer. . v/v/v (19) as develop ing solvents.9 ml 10% tungstic acid. The car bohydrate content was measured by the IH0+ Nelson-Somogyi method (17) modified for 1£*•^*^^COr-lOti1-H*"coIOrH use with milk by deproteinizing 0. «Amberlite IR 120 (H+) and IR 4B (OH-). the milk was centri0tit»gIHlecific Oti00m(ONHai—ir-lf|o>2?v^coIH fuged.•aMIO0+11-HfHC7v^COOIIco^rH^ *Miniature combination electrode and model LS pH meter. Carbohydrates were detected 1IO*f«\mS00rHtioIOcirHV-'CNrHtico•*CN00IOCNrHIOpids. Macy. prior to storage at — 20°. Some suckling infants were killed for ¿4â„¢SörtiH(N^^01t>I«0H«2ÕH« other purposes. After precipitation of the protein by addition of 5 volumes of 95% v/v ethanol. pH. H. 5:2:7. . k»SS1-Hr-tia*>V)¿(Aa UU•0^tÕli11-1 Downloaded from jn. and lipids were determined by the Rose-Gottlieb method (15).38. G. crude protein. The specific grav ity of the milk was determined at 24° with a micropycnometer (13) and the pH * was measured. v/v/v (18) and the upper layer of ethyl acetate-pyrimi3o?CDXzC'S g/100 gravitygìMIHr-?si*r-4CNOtiCOr-lt»rH^•^O5 mi3i!<yfiyrtPi5g1s g/100 Mean mis~\Hihydrous SD. Crude protein was deter mined by the micro-Kjeldahl procedure IH5S§0tigrt«^^i0otioIH'tCDOO —CIotiIOIH<Nf. diluting <NOci"J to 10 ml with water.COCOCOOJm1s". 2011 SE. BUSS turned to the mother before she recovered from the sedation. tate-pyridine-water. weight of sample. 10:4:3. E. Analytical methods. Numbers I.422 DAVID H. Correlation coefficients were calculated between the values obtained for day of lactation. or using ml(HOrH+ g/100 solids.•öSO The carbohydrate composition of two samples of mature milk (after 22 and 211 . Sargent and Company. ofFromdetermina paper chromatography NumbersFrom 194 of Modde. centrifuging and per forming the analysis on 1 ml of the super natant solution. milking of their mothers was continued at approximately weekly intervals until the milk supply dried up.o1^8Ì•5 •+• 1 mlr-lO0tioCNO§O50o dine-water. St. using an IBM 1130 SìoCigjoh.. specific gravity. New from various lactation periods. total solids.9813. lipids. The samples were then combined and lyo.90.41.7113.. (editor) Tables.24C9331.001. p.34B1641.38).92.90. mlAsh.85.36.0225. ard deviations and the number of deter Geigy Pharmaceuticals. New TABLE 2 Downloaded from jn.0 . The melt crude protein. mlCrudeg/100 protein (N X 6. Mean values for mature human milk (21.63. and the melting point and infra the day of lactation. red spectrum were determined. the total length of hydrate. with silver nitrate and ammonia (20).58D9731.12. Table 3 shows the individual analyses of mined. 61. 6. 2011 Sign and significance1 of the correlation coefficients between constituents of natural baboon milk * «H p±1 — ns 4_ _*** * the properties Crude + and gravity protein— Yiold IleIQ Total solids + "* _ *** _(_ ns 1_ n« TiniHa Llpia °*** Ash_ _+ »• +_ " —+"» **_ lactationSpecific Day of gravityYieldpHTotal solidsLipidsCrude proteinLactoseSpecific us +_ *** _j_ ns nsus# ns+ _* ** _(. gPHTotal solids. ** = P < 0. New York. *+ + ""Lactose "»• _** nns _|_ i ** i »« = not significant.4916. Inc. mlAnhydrous g/100 lactose (direct).87. * From 56 to 63 pairs of values. Ardsley. The sign and significance level7 of the philized. the resultant solid was twice recrystallized from water to give colorless correlation coefficients calculated between prisms.02611. g/100mlLipids.26.60. g/100 g/100 mlSample TABLE 3 of baboon milk as the supply was allowed to dry up by removal of infant designationA141. pH. ed.org by guest on July 13.05.27.0325.22) have been included for comparison.nutrition. erties and constituents of baboon milk • Mann Research Laboratories. K.01. and * = P < 0. 1962 Scientific York. weight of sample.37.26.NATURAL BABOON MILK 423 by spraying the developed chromatograms minations made are shown in table 1. their stand York.the milk samples obtained after final re moval of the infants. as was the melting point of a mix ture of the milk sugar and lactose mono. lactose and ash are shown ing point and infrared spectrum of authen tic lactose monohydrate 6 were also deter in table 2.83. Composition Property or constituentDays after removal infantTotal of days of lactationSpecific gravityYield. *** = P < 0. 'Diem. lactation and the number of days after RESULTS the suckling stimulus was removed are The mean values for the major prop both shown. Of correlations were found between the car the 64 samples analyzed. Tokyo. anesthesia lowered the milk yield. because of the probabil ity of rejection of the infant after too early Zyl " has milked unsedated baboons with a sedation of the mother. (4) could obtain only simi colostrum was produced for similar pe lar quantities from rhesus monkeys. cantly change as lactation progressed. and some but the yield could be returned to normal color change also occurs. Samples of ba by the use of oxytocin (25. but neither the fat nor • Saito.. Noguchi and S.05) between the sample size and point of 210 to 213° (uncorrected). BUSS As lactation progressed. Snow Brand Milk Products Company Ltd. in breast for several hours. despite the necessity of se samples. and a mixture of the two sample size and lipid content of human melted at 210 to 214°. Six samples found in a detailed study of the milk of from each of these animals were analyzed Japanese women. or by centration was considerably higher. and considerably in these. and during the less oxytocin was also used. protein and ash. The pH was also correlated with the lipid and DISCUSSION carbohydrate contents. The riods in the two species. this is characteristic of • footnote 6. with both solvent systems used. No differences were form of lipoprotein. Nishikawa. ash concentrations changed appreciably.org by guest on July 13. Un during the first 5 days after parturition is considered as colostrum. T. Reports of Research Laboratory. Y. rapidly through this period. 11Van Zyl. The lack of correlation between more crude protein and ash than human the lipids and protein indicated that only milk. Au the lipid concentration. would be unphysthis early milk. See human colostrum. both the sam The only carbohydrate detected in ma ture baboon milk had a Chromatographie ple size and the lipid concentration in mobility identical with that of lactose. the pH. white. but did not signifi hydrate were also identical. No The milk used in the present study was other baboon contributed more than three assumed to be representative of normal baboon milk. but there was a sig found between the values from milk ob nificant positive correlation between the tained from baboons classified as Papio protein and the ash. H. the effect on the milk composition was not. Downloaded from jn. papio. The pH decreased markedly tra of the milk sugar and lactose mono. Doi.10 in the 36. A. Japan. Kondo. 26). only 1 to 2 ml next 5 days as transitional milk (23). nent in the total solids. the mammary secretion dating the animals to remove the infant from the breast and obtain the milk. was similar in the a small portion of either could be in the two types of milk. these samples increased considerably. Nakazato. Natural lactation produced mature ba The total solids were extremely depend boon milk which was more concentrated ent on the lipid content.to 279-day lactation period. with a very reported. no. and allowing the milk to accumulate in the the lactose concentration was lower. in contrast to the thentic lactose monohydrate ' melted at negative correlation reported between the 210 to 214°. E. ing the relative amounts of each compo 10See footnote 9. A. In the cat and The composition of the milk changes most rabbit. The protein con trauma caused by such a procedure. boon milk taken 1 day after parturition were the same color. personal communication. as those taken several was to be expected from a primate whose infants suckle almost continuously. It contained gravity was in turn lowered by increases more lipids and lactose. That it There resulted a small positive correlation was lactose was confirmed by its melting (P < 0. The low yield of baboon milk slight yellow cast. S. tained from one baboon. 2011 . cynocephalus and P.with a larger sample. Shingo 1965 Studies on human No clarification was achieved by consider milk.. van months later and. nine were ob bohydrates and the lipid. of milk could be expressed. and van tained for analysis to indicate whether Wagenen et al. however. G.nutrition. Significant negative anubis. an insufficient out the use of oxytocin and was able to number of early milk samples was ob obtain only about 6 ml of milk. Fumichi.. and eight from Somewhat different correlations were each of two other animals. however. P.424 DAVID H.The infrared spec milk9 (24). In the human. K. 69. Kawanishi. Noguchi. I. and the specific than mature human milk. vol. Care. G. Anim... Papio J. creased very rapidly thereafter. Miller.. eds. LITERATURE CITED and only increased gradually as lactation 1. 2011 The author thanks Dr. Van Wagenen. T. The concentrations of these other com press. Biol. of infant baboons away from their 16. A. The milk national Zoo Year Book. Folia Primatologica. The values obtained not only serve as a Washington. Kon. ed. University of Texas Press. cynocephalus and P. Austin. J. however. Himwich and H.nutrition. Chem. Milk Dairy tute milks for the more successful raising J. the lipid content could of the milk of wild animals. New primates (3. Kalter 1966 Care and raising of new primates. of the monkey (M. S.. 1966 The feeding of ba With a total solids content of nearly 11. Composition of milk from Galago crassicaudatus. (editor) 1965 The Baboon complete removal of the infant.17%) (6). 9. quickly the longer the previous lactation. Pilson. 1960 Official Methods of Analysis. a concentration not normally found with Biol. M. Exp. . M. Britton.1 ± g/100 ml). was found to be approximately 5 g/100 ml. viscous. 333. and V. Van Zyl. D.. A. and H. John Wiley and Sons. and F. 153: 375. tained during the first 3 months of lacta 56: 415. Ratner and reported for the human (21) and other S. Biol. 1934 Die chemische ± 2.5%) (3). vol.org by guest on July 13. prerequisite for the preparation of substi The Rose-Gottlieb method.(editor) 1966 Some Recent Developments in Comparative Medi The baboon milk obtained by van Zyl (5). Lab.. 17.. Academic Press. London. in J. As the milk supply dried up after the 9... 4. Lab.. cine. Hutchinson and Com study was also much closer to the values pany Ltd. H. p. S. (editor) 1967 The Baboon in composition appeared to occur more in Medical Research. had a lipid concentration of 10. Vice. Tiennes. 16: 12. L. Chem. ACKNOWLEDGMENTS Downloaded from jn. In: The Inter rise as high as 20 g/100 ml. 4. and R. N. base line for studies of the nutrition of 15. except for the prosimYork. H. Inc. 12. chimpanzee 8. H. but are also fat content of milk and milk products. born baboons. 2. and J. Houghton 1945 The micro-Kjeldahl determination of the nitrogen mothers. C. 188.7%) (6) and gorilla (2. Anim. and the lactose decreased. Nelson.. days of lactation was 6. Cowie (editors) 1961 progressed (the lipid concentration of the Milk: The Mammary Gland and Its Secre seven samples taken after more than 200 tion. E. Vagtborg. Academic Press. 6). H. Kinderheilk. 2. The mean of the values he ob Zusammensetzung der Milch eines anthro poiden Affen (Orang-Utan). p.9% ) (4). Cooper 1967 (3. Afr. D. 7. 16: 178. Sci. New York. Several Catchpole 1941 Composition of the milk samples contained more than 15% lipids. K. namely orangutan (3. I. Association of Official Agricultural Chemists ian Galago crassicaudatus (8). boons.. Austin. A. H. 1963 The composition allowed to dry up. B. O. 1955 The lipid and iodine content in blood and milk of the lactating probable that the infants of those baboons baboon. the computer program and for his assist The concentration of lipids in the milk ance with the analyses. E. T. Z.NATURAL BABOON MILK 425 iological and might also cause changes in also indebted to Earl Gradley for devising the milk composition. 16: 172. tion was 3. 30 g/100 ml. He is content of amino acids and proteins. species which nurse frequently (6). 159: 373. Care..1 2. H. Med. These changes 10.8%.-W. T. H. study were also close to those of human cromethods of Quantitative Organic Analy milk (21). Neth. University of Texas tein and ash concentrations also increased Press. 14. p. doguera.0%.. J. 48: 133.C. Mulder 1962 Gravi metric methods for the determination of the infant and female baboons. Jarlipid concentration found in the present vis and D.. P. E. Q. D. Walstra. It is 5. 5: 88. J. the pro in Medical Research. Koehn. Niederl 1942 MiNiederl. R. Vagtborg. Buss. 6. Care. Kriewaldt 1968 A machine for milking baboons. Anim. Proc. R. Ben Shaul. Morris. 39. 1944 A spectrophotometric adap tation of the Somogyi method for the deter mination of glucose. N. M. ponents of the baboon milk used in this 13. table 3 show that as the milk supply was 20: 119. rhesus macaque (3.. C. F. W.. Schumacher. New York. H.. and to those reported for other sis. the milk became extremely Lab. their influence on the serum lipids were partially weaned. since the results in of the suckling infant. II. ed. A. Soc. Med. Kriewaldt and his staff for their invaluable assistance With the handling of the baboons.6 3. S. but the concentration in 4. 2. and A. mulatta).. Zacharias 1961 Hydrogen-ion concentration of fresh human milk. Macy. K.. J. and rat milk using paper chromatography. Méd. Pettinati and W. Endocrinology. Macy.. H. Trevelyan. Sawyer 1963 Milk ejection reflex and maintenance of lactation in the rabbit. Washington. 2011 . Comp. H. Estud. Mena 1965 Effect of ovariectomy and barbiturate administration on lactation in the cat and rabbit. Biochem. G. D. P.org by guest on July 13. 7: 136. A.nutrition. Dis. 23: Downloaded from jn. 72: 720. Harrison 1950 Detection of sugars on paper chromatograms. Dairy Sci. Modde.. J. T. Amer. E. 89. S. Jenness... Wedler and O. Dialyzable carbohydrates... Lindner. J. 22. 37: 538. and F.. Roberts. I. 78: 589. 13: 339. II. Dworschák 1965 The effect of different factors on the composition of human milk. C. Dieta. 26. The composition of hu man milk during lactation. S... BUSS 18. C. H. W. Szöke. Szarvas and E. 23. Beyer and C. Sloan 1953 The composition of milks. Nutr. Nature. Gynaekol. Biol. 20.. Beyer. Physiol. 254. K. I. 196: 343. pubi. J. cow. H. Méx. D. 24. II. Kelly and R. R. sow. 166: 444. Bucek 1954 A comparative study of human. E. E. Bol. J. D. E. Tarjan. R. 25. C. Procter and J. Arch. M. Regehr and R. 1949 Composition of human colostrum and milk. G. R. National Academy of Sciences —National Research Council.. 21.. Inst. E. Kramer. Children. Tindal.426 DAVID H. 19. Sloan 1964 Comparative biochemical studies of milk. Documents Similar To J. 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