Nutritional Components of Human Milk

8/14/2019 Nutritional Components of Human Milk

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Nutrient Requirements and InteractionsAmino Acid Composition of Human M ilkIs Not unique1'2'3

TERESA A. DAVIS,4 HANH V. NGUYEN, ROSELINA GARCIA-BRAVO,MARTA L FIOROTTO, EVELYN M. JACKSON,* DOUGLAS S. LEWIS,*D . RICK LEEr AND PETER J. REEDSUSDA-A gricultural R esearch Service C hildren's N utrition R esearch C enter, D epartm ent ofP ediatrics, B aylor C ollege of M edicine, H ouston, T X 77030; *Southw est F oundationfor Biomedicai Research, San Antonio, TX 78228; and nhe university of TexasM . D . Anderson Cancer Center, D epartm ent of Veterinary Resources, Bastrop, TX 78602

ABSTRACT To determine whether the amino acidpattern of hum an m ilk is unique, w e com pared the am inoacid pattern of hum an m ilk w ith the am ino acid patternsof the milks of great apes (chimpanzee and gorilla),low er prim ates (baboon and rhesus m onkey) and nonpri-m ates (cow , goat, sheep, llam a, pig, horse, elephant, catand rat). A mino acid pattern w as defined as the relativep ro po rtio n o f each am in o acid (pro tein -b oun d p lu s free)(in m g) to the total am ino acids (in g). Total am ino acidconcentration was lower in primate milk than in non-prim ate m ilk. There were com monalities in the overallam ino acid pattern of the m ilks of all species sam pled:the most abundant amino acids were glutamate (plusglutam ine, 20% ), proline (10% ) and leucine (10% ). Essential am ino acids were 40% , branched-chain am inoacids 20% , and sulfur am ino acids 4% of the total am inoacids. The amino acid pattern of human milk was moresimilar to those of great apes than to those of lowerprimates. For example, cystine was higher andmethionine was lower in primate milks than in non-prim ate m ilks, and in great ape and hum an m ilks than inlower prim ate m ilks. Because the m ilk am ino acid patterns of the human and elephant, both slow-growingspecies, were dissim ilar, the amino acid pattern ofhuman milk seems unrelated to growth rate. J. Nutr.124: 1126-1132, 1994.IN DEX IN G K EY W OR DS:am ino a dds m ilk prim ateshuman s e le ph an ts

Neonatal mammals rely on a single food source,m ilk, to meet their nutrient needs. The molecularcomposition of m ilk can vary widely among differentspecies, and it seems reasonable, ideologically, thatthese differences in milk composition may representan evolutionary phenomenon associated with thespecific nutrient needs of the young of each species(Jenness 1986, Jenness and Sloan 1970). D ifferences

among species in the nutrient requirements of theiryoung m ay arise from differences in postnatal growthrate, stage of maturity at birth, body composition atbirth , and environm ental peculiarities of their naturalhabitats. In addition, constraints imposed on the lac-tating female, such as litter size and lactation load,maternal diet consumed and nursing schedule, couldpotentially influence m ilk com position.The protein concentration of m ilk varies m ore than10-fold among species, w ith that of human milk atthe low end of the range (~8 g protein/L, Jenness andSloan 1970). A lthough the milk protein concentrations of num erous species have been well established,there has been little systematic study of the total (i.e.,protein-bound as w ell as free) am ino acid com position

'P resented in part at E xperim ental B iology 93, M arch 28-A pril1, 1993, N ew O rleans, L A [D avis, T . A ., N guyen, H . V ., F ioretto, M .L. & Reeds, P . ]. (1993) Primate and nonprimate milks havedifferent am ino acid patterns. F ASEB J. 7: A 158 (abs.)j.2This work is a publication of the U.S. Department ofA gricu ltu re /A gricu ltu ral R esea rch S erv ice C hild re n's N utritio n R esearch Center, Department of Pediatrics, Baylor College ofM edicine and T exas C hildren's H ospital, H ouston, T X. T his projecthas been funded in part with federal funds from the U.S.D epartm ent of A griculture, A gricultural R esearch S ervice underCooperative A greem ent no. 58-6250-1-003. The contents of thispublication do not necessarily reflect the view s or policies of theU .S. D epartm ent of A griculture, nor does m ention of trade nam es,com mercial products or organizations im ply endorsem ent by theU nited S tates governm ent. P artial support for baboons and rhesusm onkeys at the S outhw est F oundation for B iom edicai R esearch w asprovided by A nim al M odels C ontract H V-53030 from the N ationalH eart, L ung and B lood Institute.3The costs of publication of this article w ere defrayed in part bythe paym ent of page charges. T his article m ust therefore be herebym arked "advertisem ent" in accordance w ith 18 U SC section 1734solely to indicate this fact.4To w hom correspondence should be addressed.

00 22 -3 16 6/94 $ 3.0 0 1 99 4 Ame ric an Ins titu te o f N utritio n.M anuscript received 14 D ecem ber 1993. Initial review com pleted 21 January 1994. R evision accepted 15 February 1994.1126


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A M INO A CID PA TTERN OF HUMA N M ILK IS N OT UN IQUE 1127of the m ilk s secreted by dif ferent species. Hum anm ilk is generally recogniz ed as being distinct in itsam ino acid com position (Heine et al. 1991); how ev er,this conclusion has arisen principally f rom comparison of hum an m ilk w ith bov ine m ilk , its com monsubstitute for hum an infant feeding. T he m ost distinct dif ference betw een hum an and bov ine m ilkseem s to be the greater concentrations of cy stine andtryptophan relativ e to the total am ino acid concentration and low er concentration of m ethioninerelativ e to the total am ino acid concentration inhum an m ilk . T his has been ascribed to the greater a-lactalbum in content. W e do not k now , how ever, ifthe am ino acid com position of the hum an m ilk isindeed unique or w hether it is characteristic of them am mals w ithin the sam e phy logenetic group (i.e.,the great apes in particular and prim ates in general) orof slow ly grow ing species, w hich w ould include notonly the great apes but also such species as the elephant (M cCullagh and W iddow son 1970). T herefore,it w as our objectiv e to determ ine the am ino acid(protein-bound plus f ree) com position of hum an m ilkand to com pare it w ith the am ino acid com positionsof m ilk s of great apes, low er prim ates and nonprim atespecies.

M ATER IALS AND M ETHODSMilk collection. M ilk was obtained from fivespecies of prim ate: hum an (Hom o sapiens, n = 6),chim panz ee (Pan troglody tes, n = 5), gorilla (Gorillagorilla, n = 3), baboon (Papio cynocephalus anubis

and Papio cy nocephalus anubis/Papio cy nocephalus,n = 5) and rhesus monkey (Macaca mulatta, n = 6).M ilk w as also obtained from the follow ing rum inantand nonrum inant nonprim ate species: cow (B ostaurus, n = 4), goat (Capra hircus, n = 2), sheep (Ovisaries, n = 6), llama (Lama glama, n = 3), pig (Susscrofa, n = 3), horse (Equus caballus, n = 8), elephant(Elephas maximus, n = 3), cat (Felis catus, n = 4) andrat (R attus norv giens, n = 3). S om e of the prim atem ilk s w ere purchased from Y e rk es R egional Prim ateR esearch Center, Em ory Univ ersity (A tlanta, GA ).S om e of the sheep m ilk w as donated by W . G. Pond(C hildren's N utrition R esearch Center, H ouston, T X ).Horse and cat m ilk s w ere donated by S . C . Z ick er andQ. R . R ogers, respectiv ely (Univ ersity of California,Dav is, CA ). Horse, sheep and goat m ilk s w ere alsodonated by G . S . Sm ith (N ew M ex ico S tateUniv ersity , L as Cruces, N M). Elephant m ilk w as donated by E. M iller (S t. L ouis Z oological Park , S t.L ouis, M O ), C . L . W allace (B urnet Park Z oo, S yracuse,N Y ) and J. Glaz ier (Dick erson Park Z oo, S pringf ield,M O). L lam a m ilk w as donated by E. Dom atti (S unshine A cres L lam as, S im onton, TX ). Pig and bov inem ilk w as purchased from Texas A &M Univ ersity(College S tation, TX ). R ats w ere purchased fromCharles R iv er L aboratories (W ilm ington, M A ).

A ll sam ples w ere obtained from anim als 10 orm ore day s af ter parturition and therefore w ere considered "m ature" m ilk sam ples. N one of the sam plesw as obtained during the late stage of lactation w henof f spring obtain a large proportion of their nutrientsf rom foods other than m ilk . Each of the three pigm ilk sam ples w as pooled from sev eral pigs, but allother m ilk sam ples w ere obtained from indiv idualanim als. W hen possible, nipples of the anim als w erecleaned prior to m ilk ing. R ats and m ost nonhum anprim ates w ere anesthetiz ed prior to m ilk collection.Oxy tocin w as adm inistered to som e but not all non-hum an prim ates and to pigs, rats and cats. T he of fspring had suck led just before the m ilk sam ples w ereobtained from som e anim als. Com plete evacuation ofthe glands w as not possible in som e instances. In allspecies ex cept the hum an, single sam ples w ere obtained at one m ilk ing. Hum an m ilk sam ples w ereobtained from alternate breasts during a 24-h periodw hile the infant suck led on the contralateral breast,and then the sam ples w ere pooled. A ll m ilk sam plesw ere frozen, shipped to the laboratory on dry ice, andthen frozen at -20 C until analy z ed. Hum an m ilksam ples w ere obtained af ter approval by the Institutional R ev iew Comm ittees on Hum an R esearch ofB ay lor College of M edicine and T exas Children'sHospital. A nim al care w as in com pliance w ith theGuide for the Use and Care of Laboratory Animals(N R C 1985).M ilk analysis. M ilk samples were warmed to 37Cand inv erted sev eral tim es to m ix . Duplicate aliquots(-0.20 m L ) w ere w eighed and an equal volum e ofw ater w as added. S am ples w ere centrifuged at 3000 xg for 15 m in and frozen for 10 m in at -70 C, and theupper fat lay er w as sk im med from the low er frozenaqueous lay er. T he sk im med m ilk w as hy droly z ed in4 m L of 6 m ol/L HC1 under a blanket of nitrogen at110 Cfor 24 h. T he protein hydroly sates w ere driedunder vacuum (S peedvac, S av ant Instrum ents, Far-m ingdale, N J), 1 m L of w ater w as added and evaporated tw o tim es, and 1 m L of 4.0 m mol/L m ethioninesulfone w as added as an internal standard. T heprotein hydroly sates w ere f iltered through a 0.2-/m if ilter, and the am ino acid com positions w ere determined.Amino acid chromatography. Am ino acids in them ilk protein hydroly sates w ere pre-colum n deriva-tiz ed w ith pheny lisothiocyanate and separated on aPICOT AG reverse-phase colum n (W aters, M ilford,M A ). Deriv atiz ed am ino acids w ere detected on-linespectrophotom etrically and quantif ied by com paringthe area under the sam ple peak against that of anam ino acid standard solution (Pierce H standard,S igm a Chem ical, S t. L ouis, M O) of know n concentration.T ryptophan is destroy ed by acid hy droly sis(M cK enz ie 1970); theref ore try ptophan v alues are notreported. B ecause glutam ine w as converted to


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1128 DA V IS ET A L .glutam ate and asparagine w as conv erted to aspartateduring the hydroly sis, the values reported asglutam ate include both glutam ate and glutam ine andthose for aspartate include both aspartate andasparagine. W e prev iously reported (D av is et al. 1993)that the recov ery of am ino acids, as determ ined bythe total am ino acids (corrected for the w ater ofhydroly sis) in relation to the protein (using the assayof L ow ry et al. 1951), w as 97 % . T he recovery ratesof indiv idual am ino acids from hum an recom binantinsulin (>98% pure; B oehringer M annheim , Indianapolis, IN ) and bov ine serum album in (>98% pure;S igm a C hem ical) w ere 97% f or ly sine, pheny lalanineand proline, 98% for histidine and isoleucine, 100%for valine, threonine and ty rosine, 101% form ethionine and leucine, 102% for cy stine, gly cine,arginine and serine, 103% for aspartate and alanine,and 104% for glutam ate.Ca lcula tions. Tota l a mino a cid concentr a tion (g/Lof w hole m ilk ) w as the sum of all indiv idual am inoacids analy zed. T ryptophan w as not included in thetotal am ino acid concentration. T he am ino acidpattern of m ilk w as def ined as the am ount of eachindiv idual am ino acid (in m g) div ided by the totalam ino acids (in g).Sta tistics. Da ta a re presented a s means SD. Totest for dif ferences am ong species, one-w ay A N OV Aw as conducted, beginning w ith com parisons across allspecies. T his w as follow ed by com parison of prim atesv s. nonprim ates and then specif ic com parisons w ithinthese groups (such as hum ans and great apes v s. low erprim ates, and hum ans v s. great apes) using tw o-tailedt tests (S nedecor and Cochran 1967). B ecause of them ultiple com parisons, w e used a B onferroni correction ,- only pro bability lev els


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A M INO A CID PA TTERN OF HUM A N M ILK IS NOT UN IQUE 112

T ABL EAminoa cid s o f g rea test a bun da nce in p rima tendnonprimatemilks1-2Species

n Glutam ate L eucinerolinemgaminocid/gtotalaminocidPrimateHuman

6 190 8 104 1 95 Chimpanzee 5 221 3 104 2 104 Gorilla 3 203 8 102 3 99 Baboon 5 194 6 105 3 107 Rhesus 6 191 5 111 3 112 NonprimateCow4 208 2 99 1 100 Goat 2 209 15 96 3 106 Sheep 6 203 4 90 4 102 Llama 3 220 1 99 1 102 Pig 3 208 5 89 4 117 Horse 8 217 8 93 3 91 Elephant 3 195 8 98 3 102 Cat4 208 1 118 1 94 Rat 3 221 8 92 2 75 'Values

are m eans so calculated from the com ent ofachindividualam ino acid (in m g| div ided by the total am inocidcontent(in g, ex clu din gryptophan).^Primatesdif fered f rom nonprim ates f or glutam ate andeucine(P

< 0.001), huma ns a nd gr ea t a pes differ ed fr om lower pr ima tesorproline[P < 0.001), and hum ans dif fered from great apesorglutamate (P


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1130 DA V IS ET A L .

T ABL E 4Su lfur am ino acids in prim ate and nonprim ate m ilks1'2

SpeciesPrimateHum anChimpanzeeGorillaBaboonRhesusNonprimateCowG oatSheepLlamaPigHorseElephantCatRatn65356426338343Methioninemg16.1

.917.0 .219.8 .721.2 .824.8 .026.3 .925.5 .228.7 .731.1 .021.7 .422.0 .721.8 .732.0 .625.0 0.5Cy stineamino

ac id /g t ot almino20.2 .616.2 .715.5 .210.1 .711.7 .58.9 .88.6 .17.5 .57.3 .915.6 .311.3 .310.6 .912.1 .825.7 0.3To tal

sulfuraminocidsacid36.3

.333.2 .635.3 .731.2 .236.5 .135.2 .934.1 .336.3 .838.4 .337.3 .433.4 .532.4 .644.0 .250.7 0.6M ethionine

tocystineatio0.81

.091.06 .111.28 .202.13 .292.18 .392.97 .302.97 .143.82 .284.29 .661.40 .112.03 .462.36 .282.650.170.97 0.02'V alues f or m ethionine and cy stine are m eans o calculated from the sum of each am ino acid (in m g| div ided by the total am ino acids (in

g, excluding try ptophan). T otal sulfur am ino acids are m eans so of the sum of m ethionine and cy stine v alues.^M ethionine dif fered in prim ates vs. nonprim ates, hum ans and great apes vs. low er prim ates, and hum ans vs. elephants |P < 0.001 ).C ystine dif fered in prim ates v s. nonprim ates (P < 0.01), hum ans and great apes v s. low er prim ates (P < 0 .001], hum ans v s. great apes (P < 0 .01),and hum ans v s. elephants (P < 0.01). T he m ethionine to cy stine ratio dif f ered in prim ates v s. nonprim ates, hum ans and great apes v s. low erprim ates, hum ans v s. great apes, and hum ans v s. elephants (P < 0.001).

taxonom ic relationships of interest (Jenness 1986,lenness and S loan 1970). W e chose species born atsim ilar stages of m aturity (such as the cow , llam a,horse and pig), species that share sim ilar ecologicalniches (such as the cow and horse), species that nurseon dem and (such as prim ates and the horse), speciesthat vary in litter siz e (hum an and cow v s. rat andpig), species that as adults hav e radically dif ferentdietary am ino acid patterns (om niv ores, herbiv oresand carnivores), and species that dif fer in site andex tent of digestion (rum inants, nonrum inant herbivores and nonrum inants). W e further questionedw hether the unique am ino acid needs of a speciesm ight be ref lected in the am ino acid pattern of them ilk of that species. T hese unique needs include thecat's essential requirem ent for arginine and thesheep's, llam a's and rat's need to sy nthesiz e largeam ounts of a tissue (i.e., hair or w ool) w ith a radicallydif ferent am ino acid pattern from that of othertissues.To deter m in e th e am ino acid p a t ter n of m ilksam ples from a large num ber of species, dif ferentsam pling techniques had to be used. How ever, itseem s unlik ely that the use of dif ferent sam plingtechniques inf luenced the results. For exam ple,w ithin one species (baboon), tw o of the f iv e indiv idualanim als suck led their young just prior to sam plingand three did not. A lthough the total am ino acid

concentration tended to be higher in the m ilk of thoseallow ed to suck le their y oung before sam pling (13.9 0.4 v s. 10.0 1.6 g/L ), the am ino acid pattern of them ilk w as the sam e for all baboons (data not show n).T he lack of ef fect of sam pling technique on am inoacid pattern is also ref lected in the sm all CV for eachspecies (


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A M INO A CID PA TTERN OF HUMA N M ILK IS N OT UN IQUE 1131

T ABL E 5U nique differences in milk amino acid patterns among species^

SpeciesPrimateHum anChimpanzeeGorillaBaboonRhesusNonprimateCowG oatSheepLlamaPigHorseElephantCatRatn6S356426338343Glycine22

20 22 14 14 18 18 18 14 32 16 13 10 15 1Serinemg61

41 47 53 48 56 49 52 41 51 52 68 44 85 2Cy stineamino

acid/gotal20 16 16 10 12 9

9 8 71611 11 12 26 1Prolineamino

acid95 10 4 99 10 7 112 100 106 102 102 117 91 102 94 75 3A rginine36

35 35 56 +47 342934364460 48 64 33 1

'V alues are m eans so of each am ino acid { in m g) div ided by the total am ino acids (in g, ex cluding try ptophan

and, to a lesser degree, sim ilar to those of the m ilk s oflow er prim ates. T he m ilk of the cow w as m ostsim ilar to those of the goat and sheep (w hich are ofthe sam e phy logenetic suborder) and, to a lesserdegree, w as sim ilar to the m ilk of the llam a, w hich isof the sam e order (A rtiodacty la) but dif ferent suborder.T he relationship betw een phy logenetic order andam ino acid pattern of m ilk is m ost apparent for theam ino acids cy stine and m ethionine. T he prim ates asa w hole had low er m ethionine and higher cy stinecontents in their m ilk com pared w ith the artiodacty les. T he hum an and the great apes had low erm ethionine and higher cy stine in their m ilk s than didthe low er prim ates, and indeed the low er prim ateshad m ethionine and cy stine contents in their m ilk sthat w ere m ore sim ilar to those of the nonprim atesthan to those of the great apes. Hum an m ilk had thehighest cy stine content of all the prim ate m ilk s. B ecause the requirem ent for cy stine, as a proportion oftotal am ino acids, is higher for m aintenance than forgrow th (Fuller et al. 1989), and because m aintenancecontributes a greater proportion of the nutrient requirem ents of slow -grow ing species, w e questionedw hether the high cy stine content in the m ilk s of thehum an and the great apes m ight be related to theslow grow th of these species. How ev er, com parison ofthe cy stine content of m ilk s f rom the hum an and theelephant, another slow -grow ing species (M cC ullaghand W iddow son 1970), suggests that the am ino acidpattern of hum an m ilk is unrelated to grow th rate.T his conclusion is supported by the lack of closesim ilarity betw een hum an and elephant m ilk for

other indiv idual am ino acids, as w ell as the observation that m ilk f rom the rat, a rapidly grow ingspecies, had the highest cy stine content in its m ilk ofall species surv ey ed.A lthough com parison of m ilk am ino acid patternsam ong species by specif ic classif ications such as stageof m aturity at birth, litter siz e and nursing schedulerev ealed little relationship, there did seem to be som erelationship betw een m ilk am ino acid content andthe unique am ino acid needs of som e species. T hehigh content of arginine that w e found in cat m ilkand that others have found in the m ilk of the tiger(B ock 1984) m ay be related to the high arginine requirem ent of felines (M orris 1985). How ever, m ilkf rom the horse w as also relativ ely high in arginine.B ecause w e (Dav is et al. 1993) had prev iously foundthe serine content of rat m ilk to be higher thanavailable literature values for the m ilk s of otherspecies ex cept the sheep (US DA 1976), w e speculatedthat a high serine content in m ilk m ight be related tothe need to synthesiz e large quantities of hair orw ool; serine is required for the synthesis of cy stine,and there is a proportionally high abundance ofcy stine in hair and w ool proteins. How ev er, in thecurrent study w e found that sheep and llam a m ilk sw ere not serine rich, and thus the rat w as uniqueam ong species sam pled in its high serine content inm ilk . T his high serine and cy stine but low prolinecontent in rat m ilk is in agreem ent w ith a prev iouslypublished description of the am ino acid com positionof rat casein (W oodw ard and M esser 1976). A dditionally , pig m ilk w as unique in its high gly cinecontent, consistent w ith prev iously reported valuesfor sow m ilk (Elliott et al. 1971).


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1132 DA V IS ET A L .W e conclude that hum an m ilk is not unique in itsam ino acid pattern but is sim ilar to the m ilk s of otherprim ates, particularly the great apes. B ecause the v astm ajority of m ilk am ino acids are deriv ed from m ilkproteins, our results support a recent study thatshow ed that the protein com positions of rhesusm onkey m ilk and hum an m ilk are sim ilar (K unz andLonnerdal 1993). On the sam e basis, how ever, w e

w ould predict that the sim ilarity in the protein composition of the m ilk s of the great apes and that ofhum an m ilk w ould be ev en closer.

ACKNOWLEDGMENTSW e thank E. O. Sm ith for assistance in thestatistical analy ses and L . L oddeke for editorialreview.

L IT ER AT UR E C IT EDB ock , V . H., W unsche, J., K reienbring, F., L ink e, K . & Frick e, G.(1984) ber die A m inosaurenzusam mensetzung der M ilchproteine einiger Z ootierspez ies. Z ool. G art. 54: 349-353.Dav is, T . A ., Fioretto, M . L . & R eeds, P. J. (1993) A m ino acidcom position of body and m ilk protein change during thesuck ling period in rats. J. N utr. 123: 947-956.Elliott, R . F., N oot, G .W .V ., Gilbreath, R . L . & Fisher, H. (1971)Ef fect of dietary protein lev el on com position changes in sowcolostrum and m ilk . J. A nim . S ci. 32: 1128-1137.Fuller, M . F., M e W illiam , R ., W ang, T . C . & G iles, L . R . (1989) T heoptim um dietary am ino acid pattern for grow ing pigs. 2. R equirem ents f or m aintenance and f or tissue protein accretion. B r.J. N utr. 62: 255-267.H eine, W . E., K lein, P. D . & R eeds, P. J. (1991) T he im portance of a-

lactalbum in in inf ant nutrition. J. N utr. 121: 277-283.Jen nes s, R . (1 98 6) L actatio nal pe rf orm an ce of v ario us m ammalianspecies. J. D airy S ci. 69: 869-885.lenness, R . & . S loan, R . E. (1970) T he com position of m ilk s ofv arious species. D airy S ci. A b str. 32: 599-612.K unz , C. & L onnerdal, B . (1993) Protein com position of rhesusm onk ey m ilk : com parison to hum an m ilk . Com p. B iochem .Ph ysiol. 1 04 A : 7 93 -7 97 .L ow ry , O . H ., R osebrough, N . J., Farr, A . L . & R andall, R . ]. (1951)Protein m easurem ent w ith the Folin phenol reagent. J. B iol.C hem . 193: 265-275.M cCullagh, K . G. & W iddow son, E. M . (1970) The m ilk of theA f rican elephant. B r. J. N utr. 24: 109-117.M cK enz ie, H. A . (1970) A m ino acid, peptide, and function groupanaly ses. In: M ilk Proteins: C hem istry and M olecular B iology(M cK enz ie, H . A ., d.),p. 181-192. A c adem ic Press, N ew Y o rk ,N Y .M o rris, J. G . (1 985 ) N u trition al an d m e tab olic re sp on se s to arg in in edef iciency in carniv ores. J. N utr. 115: 524-531.N ational R esearch Council (1985) Guide for the Care and Use ofL ab oratory A n im als. Pu blicatio n no . 8 5-2 3 (re v.), N atio nal Ins titutes of Health, B ethesda, M D.R enner, E. (1983) M ilk and D airy Products in H um an N utrition.V o l ksw irt sc haf tl ic he r V e rlag , M nc he n,G e rman y.S nedecor, G . W . & C ochran, W . G . (1967) S tatistical M ethods. Iow aS tate Univ ersity Press, A m es, IA .U .S . D ep artm e nt o f A g ricu ltu re (1 976 ) C om p ositio n o f Fo od s: D airyand E gg Products, R aw , Processed, Prepared. A griculturalHandbook no. 8-1, US D A , W ashington, DC.W o odw ard, D . R . & M esser, M . (1976) C hem ical com position of ratcasein. C om p. B iochem . Phy siol. 55B : 141-143.

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Nutritional Components of Human Milk

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