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Volume and Caloric Density of Human Milk
B. Volum e an d Calori c Densit y of Huma n Mil k MARGARET C. NEVILLE I. Introductio n A detaile d knowledg e o f mil k volum e productio n and/o r transfe r t o th e offspring i s important in assessing the metabolic impact of lactation on th e mother, materna l factor s tha t impac t mil k yield, an d th e rol e o f mother' s milk i n nutritio n o f th e young . I n thi s discussion w e will focus mainl y o n human lactatio n bu t th e methodologie s an d principle s ar e generall y ap plicable t o othe r mammals . On e importan t differenc e i s that , unlik e women, th e rat e o f mil k productio n fo r thos e anima l specie s tha t hav e received th e mos t study , namel y dair y animal s an d laborator y rodents , is limited b y the amoun t o f mammar y tissu e and th e rat e a t which nutrient s can be delivered t o the mammary gland . Maximal production i s stimulated by consisten t milkin g i n dair y specie s an d b y th e ofte n massiv e mil k demands o f a larg e litte r i n rodents . I n thes e animals , th e rat e o f mil k production is, as expected, highly dependent on maternal factors includin g genetic heritag e an d nutrition . O n th e othe r hand , lactatin g women , an d probably many other species in the wild, produce milk at a rate determine d largely b y infan t deman d (Prentic e et a/., 1986 ; Dewe y an d Lonnerdal , 1986), a poin t w e wil l retur n t o severa l time s i n thi s discussion . Th e maximal huma n capacit y fo r mil k productio n ma y hav e bee n achieve d by the wet nurses studied i n the 1920 s by Macy et al. (1930) who produce d up t o 350 0 m l o f mil k pe r day , abou t fou r time s th e volum e produce d by wome n breast-feedin g a singl e infant . Mother s o f twin s an d triplet s produced 2 o r 3 liter s o f mil k pe r da y i n a stud y b y Hartman n an d hi s colleagues (Sain t et ai, 1986) . I t i s especiall y importan t t o kee p thi s distinction i n min d whe n materna l factor s tha t ma y influenc e lactatio n capacity ar e unde r consideration . It i s als o importan t t o remembe r tha t partia l rathe r tha n exclusiv e breast-feeding i s th e rul e i n mos t huma n societie s afte r 3 t o 6 month s postpartum (Prentice etai, 1986 ; Creed de Kanashiro etai, 1990) , yet most studies have focussed o n volume transfer i n the exclusively breast-feedin g mother-infant dyad . I n this chapter, followin g a discussion of methods of measurement of milk volume transfer, we will summarize the available data for th e exclusively breast-feeding dya d followe d b y a shorter discussio n of partial breast-feeding an d weaning . A brief sectio n o n calori c density wil l complete th e chapter . H A N D B O O K O F MJL K COMPOSITIO N Copyright O 199 5 b y Academi c Press , Inc. All light s reserved . N o reproduaio n withou t permission .
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II. Method s for Measuremen t of Milk Volum e In th e measuremen t o f mil k volum e i t is important t o distinguish betwee n milk yield an d mil k transfer to the infant. I n dair y animal s mil k yield , th e amount o f mil k tha t i s transferre d fro m th e mammar y glan d t o th e mil k pail o r milkin g machine , i s th e appropriat e measure . I n general , thi s quantity represent s th e productiv e capacit y o f th e glan d whe n i t is milke d empty a t least twic e a day. I n humans , mil k transfe r t o the infan t i s almos t always th e valu e sought . Becaus e th e breas t i s no t usuall y emptie d com pletely a t a feed, thi s valu e i s somewhat lowe r tha n th e mil k yiel d tha t ca n be obtained b y expression o f mil k with a good electri c breas t pump severa l times durin g a 24-h r perio d (Nevill e et ai, 1987 ; Dewe y et al., 1991a) . Several method s ar e availabl e fo r measuremen t o f mil k volum e pro duction. Th e first, expressio n o f th e content s o f th e breas t b y pum p o r manually, is , a s mentione d above , th e metho d almos t universall y use d t o obtain mil k volum e i n dair y animals . O f th e othe r availabl e method s test weighing the young before an d after each feed fo r a specified perio d of tim e is conceptuall y th e simplest . Isotope dilution, virtuall y th e onl y accurat e method availabl e fo r th e measuremen t o f mil k productio n i n smal l labo ratory mammals, has recently been applied usin g stable isotopes t o human s (Butte et al., 1988) . The Doppler ultrasound human milk flowmeter (Woolridge et al, 1985) , whic h use s ultrasoun d t o measur e mil k velocit y a s i t travel s from mothe r t o infant , ha s no t bee n foun d t o b e particularl y reliabl e fo r any bu t ver y short-ter m measurement s o f mil k flow an d wil l no t b e examined furthe r here . A ne w metho d base d o n topographical computer imaging o f th e breas t ha s recentl y becom e availabl e fo r short-ter m mea surement o f mil k productio n i n wome n (Arthu r et al, 1989 ) an d wil l b e discussed briefl y althoug h i t ha s no t ye t receive d extensiv e evaluation . A. Extraction of Milk Extraction o f mil k b y pump , milkin g machine , o r manuall y ca n achiev e nearly complet e emptyin g o f th e mammar y glan d i f a n adequat e let-dow n is accomplished . Moder n breedin g practice s hav e produce d dair y catd e that le t dow n t o th e milkin g machine , s o tha t extractio n efficienc y i s excellent. Nevertheless , t o achiev e complet e extractio n i n goats , Linzel l (1967) gave an iv dose of oxytocin just prior to milking. LinzelP s technique , used t o measur e hourl y mil k yield , wa s adapte d t o wome n b y Nevill e et al. (1988). Briefly, a n electric breast pum p with dual heads was used t o extract milk fro m th e breasts ; afte r 1 0 mi n o f pumpin g on e dro p o f syntheti c oxytocin wa s administere d intranasall y an d pumpin g continue d fo r a further 5 min . Th e volume s obtaine d durin g th e first an d secon d hour s were higher than the average milk production due to extraction of residua l
3. Determinant s o f Mil k Volum e an d Compositio n 10
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milk (mea n tota l exces s 20 0 ± 25 ml) . After th e thir d pumpin g episod e th e mean hourly milk extraction in five women did not differ significantl y fro m the mil k volum e measure d b y tes t weighin g durin g a precedin g 24-h r period. Suc h a pumpin g regime n ma y b e usefu l whe n mil k yiel d i s t o b e assessed o n a short-ter m basis . Others hav e use d mil k extractio n t o measur e 24-h r mil k yield . Brow n et al. (1982 ) extracte d al l mil k b y breas t pum p fo r 2 4 h r an d compare d extracted volume s wit h mea n volume s obtaine d b y 6 days of tes t weighing . Pumped volume s exceede d test-weig h volume s b y 5 0 g/da y o r abou t 7% , again reflectin g residua l milk . Dewe y et al. (1991a) , usin g a breast pum p t o extract milk fro m alternat e breasts at each fee d ove r a 24-hr period , foun d residual volume s o f abou t 11 0 ml/day . Al l investigator s have , therefore , found tha t mil k volum e transfe r i s overestimate d whe n measure d b y th e extraction technique . Th e amoun t o f th e overestimat e varie s fro m 5 0 t o 200 ml/da y dependin g o n th e populatio n an d techniqu e used . B. Test Weighing
In mos t studie s fo r whic h value s ar e give n i n Tabl e I , th e infan t wa s tes t weighed befor e an d afte r ever y fee d fo r a t leas t 2 4 hr . Thi s procedur e i s usually carrie d ou t b y th e mothe r i n th e hom e afte r a brie f perio d o f training, althoug h traine d worker s hav e bee n use d i n th e field o r clinic i n some studies , particularl y i n developin g nation s (Brow n et al, 1982 ; Pren tice et al.y 1983) . Becaus e th e day-to-da y coefficien t o f variatio n fo r mil k transfer i n a singl e mother-infan t pai r i s quit e hig h [15 % i n on e stud y (Butte et aly 1985) , 8.9 % i n anothe r (Dewe y et al, 1991a)] , curren t rec ommendations sugges t tha t tes t weighin g b e continue d fo r 4 day s whe n accurate measurement s ar e neede d fo r a singl e individua l (Stuf f et a/. , 1986). However , 24-h r o r eve n properl y standardize d 12-h r tes t weight s appear to give equivalent populatio n mean s (Prentice et a/., 1981 ; Creed d e Kanashiro et a/., 1990) . An integratin g electronic balance provides the mos t accurate data , particularl y i f th e infan t i s moving (Nevill e et a/., 1988) . Fo r older children it is possible to suspend a swing from th e balance (Woolridg e et a/., 1985) . I f th e balanc e print s ou t th e weight , error s i n recordin g ar e minimized. Tes t weighin g result s i n a systemati c underestimatio n o f th e volume o f mil k produce d becaus e o f insensibl e wate r los s throug h respi ration an d sweatin g durin g th e feed . Thi s los s fro m th e infan t amounte d to 0.03 g/kg/mi n i n on e stud y (Hendrikso n et a/., 1985 ) an d 0.0 5 g/kg/mi n in anothe r (Nommse n et a/., 1991) . Thi s numbe r i s multiplied b y th e tota l nursing tim e pe r 2 4 hour s an d th e weigh t o f th e infan t t o obtai n th e correction whic h usuall y amount s t o 3 to 5 % of th e measure d dail y intake . It is possibl e t o obtai n satisfactor y mil k yield s b y weighing th e mothe r rather tha n th e infan t befor e an d afte r th e fee d i f a sufficientl y sensitiv e balance i s available (Arthu r et a/., 1987) . However , th e result s obtaine d ar e less reliabl e tha n tes t weighin g th e infan t becaus e th e amoun t o f mil k
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TABLE I Volume of Milk Transferred from Mother t o Infan t i n the Exclusivel y Breast-Feeding Dyad
Months ]postpartumI Reference/Country Neville et aL (1988) / United State s (Denver, CO) mean SD n Pao et aL (1980)/United States (Ohio) mean SD n van Steenbergen et at. (1981)/Kenya mean SD n Hofvander et aL (1982) / Uppsala, Sweden mean Range n Butte and Calloway, (1981)/United State s (Navajo) mean SD n
1
668 117 12
3
4
5
6
7
8
694 98 12
734 114 10
711 100 12
838 134 12
820 79 9
848 63 6
818 158 3
755 113 111
741 103 26
818 166 8
875 142 8
834 99 8
600 159 11
833
778** 180 7
619** 197 13
656 360860 25
2
773 575985 25
776 600937 25
725 129 40
723* 114 37
634 113 10
Butte et aL (1991a) / United State s (Texas) mean 738* SD 157 64 n De^ey etaL (1984) / United State s (California ) mean SD n Dewey and LSnnerda l (1983)/United State s (California) mean SD n
2
672 192 16
756 170 19
782 172 16
810 142 13
805 117 11
896 122 11
103
3. Determinant s o f Mil k Volum e an d Compositio n TABLE I (continued) Months p>ostpartum Reference/Country
1
2
3
Salmenpera et al. (1985) / Finland mean SD n
4
790 140 12
800 120 31
747 19 48
740** 16 26
Walgren (1944 ) Sweden (girls ) mean Variance n
576** 80 65
Walgren (1944 ) Sweden (Boys ) mean Variance n
645*** 750*** 798*** 821** * 97 107 122 113 58 42 49 72
704* 98 72
733* 113 43
7
6
5
8
817*** 133 33
Whitehead an d Pau l (1981) Unite d Kingdo m (girls) mean SD n
677 87 20
742 119 17
775 138 14
814 113 6
838
854
786
1
1
1
Whitehead an d Pau l (1981) Unite d Kingdo m (boys) mean SD n
791*** 820 187 116 27 23
829 168 18
790 113 5
922
Stuff et al. (1986)/Unite d States (Houston , TX ) mean SD n
735 85 9
Chandra (1981)/Canad a mean SD n van Raai j et ai (1991) / The Netherland s mean SD n Nommsen et al. (1991) / United State s (California ) mean SD n
1
793 71 33
692 122 16
745 131 40
811* 133 58
856 99 31
925** 112 28
872* 126 27
815 97 24
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T A B L E I (continued) ]Vfonths
Reference/Country Frigerio ^ f fl/. (1991)/ The Gambi a mean SD n Butte et al. (1992)/ Mexico (rural ) (^HgO t o mothers ) mean SD n Goldberg ^ ^ a/. (1991) / Cambridge, Englan d (H2*»0 to mother ) mean SD n Weighted mea n (test weigh only) mean SD n
1
2
3
f)ostpartu m
4
5
6
7
8
809 120 42
819 100 36
738 47 16
885** 146 15
792 177 10
802** 179 10
657 121 284
869* 150 15
735 111 343
767 111 293
773 112 313
802 109 100
827 102 148
*p < 0.0 5 with respec t t o weighted mean . **p < 0.0 1 with respec t t o weighted mean . ***Significantly differen t fro m girls , p < 0.05 .
transferred compare d t o th e mother' s bod y weigh t i s smal l an d th e correction fo r insensibl e weigh t los s i s substantial . Mil k volume s obtaine d using thi s procedur e i n Australi a wer e usuall y considerabl y greate r tha n the value s give n i n Tabl e I (Rattiga n et al, 1981) ; however , thes e earl y values wer e no t correcte d fo r insensibl e wate r loss . Whe n th e correctio n was made, mil k volumes within th e rang e of othe r reporte d studie s were obtained (Arthu r et al, 1987) . The advantag e o f tes t weighin g i s tha t i t i s a reliabl e an d relativel y inexpensive wa y t o measur e mil k transfe r fro m mothe r t o infant . Th e major disadvantag e i s tha t th e techniqu e require s a certai n degre e o f education and dedication on the part of the mother or the presence in the home of a trained field worker. It can disrupt the feeding routine especially if frequen t nighttim e feed s ar e th e norm .
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C. Isotope Dilution Isotope dilution was used first in animals and is the only technique availabl e for smal l animal s suc h a s rat s an d mice . Th e mothe r i s give n a dos e o f tritiated wate r an d th e passag e o f isotop e t o th e youn g i s tracked b y whol e body analysi s o f pup s a t intervals (Thornbur n et al, 1983) . I n human s i t is not possibl e t o use radioactiv e isotopes ; fortunately, wate r can be obtaine d labeled wit h stabl e isotopes , namely , deuteriu m o r ^^O . Deuterium oxid e was firs t use d b y Cowar d an d colleagues . I n thei r earlies t studie s (Cowar d et al., 1979 , 1982a ) th e isotop e wa s administered t o th e infan t an d th e rat e of dilutio n ove r a perio d o f severa l day s wa s determine d b y mas s spec trometry. I n thi s form th e techniqu e ha s been show n t o be usefu l bu t onl y if a correctio n i s mad e fo r exchang e o f wate r a t th e integumenta l an d respiratory surface s a s wel l a s intak e o f wate r fro m source s othe r tha n breast mil k (Fjeld et ai, 1988 ; Butt e et ai, 1991b) . I n late r studie s Cowar d et al. (1982b ) an d other s (Butt e et al., 1988 ) administere d th e isotope t o th e mother an d measure d deuteriu m enrichmen t i n th e mother' s mil k an d infant's urin e t o calculate mil k transfer . I t is necessary t o know th e infant' s total bod y wate r whe n usin g thi s method ; thi s paramete r ca n bes t b e estimated by administering a separate dose of 2H2O or H2^®0 to the infant . Careful evaluatio n o f isotop e dilutio n agains t th e test-weighin g metho d (Butte et ai, 1988 ) i n nine wome n gav e a mean differenc e betwee n th e tw o methods o f 2% , no t statisticall y significan t whe n metaboli c wate r produc tion wa s take n int o account . Isotop e dilutio n ha s th e advantag e o f eas e o f sampling and require s litde cooperation o n th e par t of th e mother. I t gives mean mil k intak e ove r severa l days . I t ha s th e disadvantag e o f requirin g sophisticated an d expensiv e analytica l techniques . Nevertheless , th e tech nique is finding increasin g us e fo r studies in developing countries (Cowar d et al., 1982b ; Butt e et al., 1992 ; Goldber g et al., 1991) . D. Topographical Computer Imaging Hartmann an d hi s colleague s (Arthu r et al, 1989 ) hav e develope d a technique i n whic h moir e pattern s ar e projecte d ont o th e lactatin g breast . Video image s obtaine d ove r a perio d o f tim e ar e store d i n th e compute r for late r analysis . A s th e breas t expand s wit h increasin g store d mil k th e moire pattern s chang e i n a way tha t ca n b e relate d t o th e volum e o f mil k produced. Thi s promisin g techniqu e ha s the potentia l o f measurin g short term rate s o f mil k synthesi s betwee n breas t feed s an d fo r tha t reaso n should b e mor e completel y evaluated . Wit h th e increasin g availabilit y o f computers suitabl e fo r thi s typ e o f task , th e cos t o f thi s metho d ma y become quit e reasonable , particularl y i n th e clinica l setting .
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III. Mil k Volumes in Exclusively Breast Feeding Women Table I is a compilation of worldwide values for milk transfer in exclusively breast-feeding women . Whe n mea n values , weighte d fo r th e numbe r o f subjects in each study, are calculated breast milk transfer is seen to increase gradually from about 650 g/day at 1 mont h to about 800 g/day at 6 months when it appears to level off (Figur e 1) . The variatio n between individual s is large wit h mea n SD s about 10 0 g/da y a t all tim e points . Mil k volume s from tw o underprivilege d groups , Navaj o Indian s an d wome n i n Th e Gambia, did no t differ fro m th e overall mea n in early lactation an d milk volumes from Kenya at 1 mont h were actually significantly higher than the mean (Tabl e I) . The consistenc y betwee n th e variou s populatio n group s suggest tha t nutritiona l an d cultura l factor s hav e littl e effec t o n mil k transfer i n the exclusivel y breast-feedin g dyad . Milk volume s obtaine d b y isotop e dilutio n i n Cambridge , Englan d were significantly higher than the overall mean at 1 mont h postpartum but not significandy differen t thereafte r fro m value s obtained usin g th e test weighing method. The mil k volumes measured in a group of undernour ished Mesoamerindian s usin g th e isotope dilutio n techniqu e wer e signifi candy highe r a t 4 an d 6 month s tha n th e mea n value s i n the table . Thi s finding was attribute d b y th e author s t o th e lowe r calori c densit y o f th e milk in this group (se e below). The rang e of mil k volumes among individuals varies from abou t 50 0 to 110 0 g/da y (Figur e 1) . I n a well-nourishe d populatio n n o materna l characteristics wer e foun d t o correlat e wit h breas t mil k transfe r t o th e infant leading Dewe y and he r colleagues t o propose tha t "infant deman d is the main determinant of lactation performance" in affluent population s (Dewey et al., 1991a). A similar study in malnourished populations has not been published, but Butte et al, (1992) proposed that milk production may be subject to maternal limitations on the basis of he r study of Mesoamer indians i n whic h mil k transfe r appeare d t o b e insufficien t t o suppor t optimal infant growth after 3 months postpartum. Infant factors related to milk production include d infan t weigh t (Nevill e et al., 1988 ; Dewey et al, 1991a) an d tota l tim e nursin g (Dewe y et ai, 1991a) . Th e differenc e between boy s and girl s disappear s whe n thei r weigh t differenc e i s taken into account . I n general , althoug h earlie r author s suggeste d tha t infan t morbidity would alter milk volume transfer (Prentice et ai, 1981) , this has not prove n t o b e th e case . I n a careful stud y b y Brow n an d co-worker s (Brown et al, 1990) diarrhea or fever were associated with no changes in the frequency o f breast-feeding, tota l suckling time, or amount of breast milk consumed. Dat a supportin g thi s conclusio n hav e bee n obtaine d b y Rowland et ai (1988 ) an d Butt e et al. (1992). The caloric density of milk may be a factor in determining the volume of milk transferred t o the infant. Butte et al, (1992) suggested that the low
3. Determinant s o f Mil k Volum e an d Compositio n
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1200
Months Postpartu m Figure I Mil k transfe r t o exclusivel y breast-fe d infants . Heav y lin e represent s weighte d mean from al l studies using test weighing in Table I and shaded area represents one standard deviation fro m th e mean . Are a betwee n ligh t line s represents th e 95 % confidence interval .
caloric density of the milk (see below) was a factor in the high milk volumes noted i n Mesoamerindians . Nommse n et al. (1991 ) foun d a significan t inverse relationshi p betwee n mil k intak e an d mil k energ y densit y i n a group o f affluen t America n women . Th e effec t o f othe r compositio n variables on milk transfer has been incompletely investigated. Nommsen et al, (1991 ) foun d a significan t (p < 0.05 ) invers e relatio n betwee n mil k volume and milk protein concentrations at 6 and 9 months postpartum in an affluen t population . The y als o foun d a positive correlatio n wit h mil k lactose concentratio n a t th e sam e stages . However , bot h thes e change s could hav e bee n th e resul t o f th e inclusio n o f wome n i n th e earl y stage s of weanin g i n thei r stud y population . I n thei r stud y wome n wer e onl y considered to be weaning, and therefore excluded from the analysis if their milk volume s wer e belo w 20 0 m l pe r day . Nevill e et al. (1991) foun d a n increase i n protei n concentratio n an d a decrease i n lactose concentratio n when mil k volume fel l belo w 400 ml/da y i n affluent America n women. I t would b e o f interes t t o kno w whethe r th e invers e relatio n observe d b y Nommsen et a/. (1991) persists when women transferring between 200 and 400 g of milk per day are excluded from statistical analysis. The correlation between mil k volume an d the rat e of transfe r o f othe r mil k components, such as calcium, magnesium, or other minerals, to the infant has not been investigated systematicall y althoug h th e relevan t dat a ar e probabl y avail able i n som e studies . I n on e stud y (Alle n et al., 1991) , fo r example , th e amounts of lactose, magnesium, and ionized calcium transferred t o a given infant o n Da y 2 1 o f lactatio n wer e highl y correlate d wit h th e amount s transferred a t 6 months postpartum although the concentrations o f thes e substances varied significantl y throug h lactation . The numbe r o f subject s in thi s stud y (13 ) wa s no t sufficien t t o mak e meaningfu l correlation s between th e rat e of mil k transfer an d productio n o f thes e nutrients .
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IV. Breas t Mil k Volume s Transferre d t o Partially Breast-Fe d infant s It i s difficul t t o giv e universa l value s o f breas t mil k volume s i n partiall y breast-fed infants because the pattern of supplementation differs from one cultural grou p t o another . However , tw o circumstances ar e o f particula r interest. On e is the infant who is breast-fed severa l time s a day, receivin g supplemental foo d o n a meal-by-mea l basis , bu t breast-feed s ar e no t replaced b y supplementa l feeding s o r bottles. A smal l grou p o f Wester n women who fed accordin g to this pattern transferred abou t 600 g of milk per day to their infants at 1 year of age (Neville et al., 1991). This patter n is prevalent in developing countries where breast-feeding o f longer duration is the norm. The second pattern is the infant who is gradually weaned by replacing feeds with meals containing milk or formula and other foods. This i s the patter n ofte n note d durin g weanin g i n affluent societies . A stud y b y Cree d d e Kanoshir a et al. (1990 ) i n Per u provide s a n excellent exampl e o f th e first pattern . Th e infant s wer e supplemente d from a n earl y ag e ( < 3 months ) wit h a variety o f food s includin g dair y products and, as time progressed, cereals. Breast milk consumed remaine d at a high level (> 55 0 ml per day) throughout the first year in 89% of the infants. Th e actua l dail y volume s o f breas t mil k consume d ar e give n i n Table II . Thes e volume s wer e abou t 93 % of th e volume s transferre d t o exclusively breast-fe d infant s a t 2 months (Tabl e I ) and decrease d slowl y to about 75% at 6 months. By 10-12 months the infants were still receiving about 45 % o f thei r tota l energ y fro m breas t milk . Thus , thes e infant s continued to obtain a substantial proportion of their nutrition from breast milk at 1 year and after. Dat a from The Gambia and Papua, New Guinea gave similar volume estimates. Note that the variability between individuals is about twic e tha t seen i n th e exclusivel y breast-feedin g group . In contrast. Figure 2A shows the volumes of breast milk consumed by five American infants whose mother s deliberately bega n gradua l weanin g at about 6 month s o f ag e b y substitutin g formul a feed s fo r breas t feeds . Milk volumes gradually decreased, reaching zero by 17 months postpartum or earlier. When milk transfer was plotted as a function of number of feeds per day for each mother-infant pai r (Figure 2B), it became clear that milk volume was linearly relate d t o the number of feeds , fallin g t o zero at one feed pe r day . Th e dat a i n Figur e 2 als o mak e i t clea r tha t o n a crosssectional basis little correlation between numbe r of fed s pe r day and milk volume woul d b e expecte d sinc e subject s producin g ove r 60 0 g/da y fe d between 4 and 1 2 times pe r day, depending o n th e individual . V. Calori c Densit y o f Huma n Mil k The caloric density of human milk is best determined by bomb calorimetry (Garza et al., 1985) . However , man y investigator s calculat e thi s quantit y
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TABLE I I Breast Milk Transfer i n Partially Breast-Fe d Infant s Milk volume :t S D (n )
Duration o f lactatio n (Months)
Creed d e Kanashir o et al (1990) / Peru (12-h r tes t weig h extrapolate d to 2 4 hr )
685 ±245 (128 ) 6 9 0 ± 2 4 0 (121 ) 655 ± 2 26 (108 ) 624±219(103) 565 ±20 8 (89)
1.0-2.9 3.0-4.9 5.0-6.9 7.0-9.9 10.0-12.5
Prentice et al (1986)/Keneba , Th e Gambia (24-h r tes t weigh )
582 ±16 9 643 ± 1 4 9 607±131 594 ±20 0 633 ± 2 0 0
(10) (17) (16) (16) (15)
3-3.99 4-5.99 5-8.99 9-11.99 12-18
Prentice et al. (1986)/Cambridge , England (96-h r tes t weigh/4 )
783 ±17 6 717±207 588 ±20 6 493 ±21 6 342 ±22 8 328 ±29 2
(48) (42) (45) (38) (31) (19)
3-3.99 4-5.99 5-5.99 6-7.99 7-8.99 9-10.99
Dewey et al (1991b)/Davis , C A (4-day tes t weigh )
769±171 646±217 448 ±25 1
(60) (50) (42)
6 9 12
Coward et al (1982b)/Th e Gambi a (^HgO t o mother )
752± 3 6 757± 4 4 728 ±17 0
(4) (4) (5)
0-4 5-9 >9
Coward et al (1982b)/Papua , Ne w Guinea (^Hg O t o mother )
670 ±18 4 (17) 936 ± 1 8 3 (8)
0-4 5-9
Reference
from th e proximate composition o f the milk using the following factor s i n kcal/gm: 5.6 5 protein , 9.2 5 fat , 3.9 5 lactose , 5.6 5 nonprotei n nitrogen . Other author s hav e use d th e factor s 4 , 9, an d 4 kcal/g m fo r protein , fat , and lactose , respectivel y (Cree d d e Kanashir o et al., 1990) . Because lipid s are th e larges t contributo r t o th e calori c density , i t is important tha t car e be taken t o obtain a representative mil k sample. If thi s is not done, or th e milk sampl e i s store d i n suc h a wa y tha t a representativ e aliquo t i s no t assayed, erroneou s value s ca n result . A secon d cautio n i s tha t som e methods fo r lactos e measurements, notabl y th e automate d enzym e proce dure on the Yellow Springs Instrument Analyzer , probably do not include the oligosaccharide s o f huma n mil k tha t compris e abou t 1 % of th e tota l weight of mil k i n normal circumstance s an d ma y contribute eve n mor e in conditions suc h a s diabete s (Ferris , persona l communication) . Us e o f th e standard factor s in these circumstances may result in a small but systematic underestimation o f th e calori c conten t o f th e milk . Representative value s fo r calori c density ar e give n i n Tabl e III . Not e that th e value s fo r undernourishe d Mesoamerindian s ar e abou t 10 0 cal/g
Margaret C . Nevill e
110 1000 rN
•d *^ 60 Sm/
u 0
750 500 250 0
(H M
59
a«
^ 1000 •^
S
1
31
7
Months Postpartum •
750 500 250
"B
0
03
6
9
1
2
Feeds pe r Da y Figure 2 Mil k volume s durin g gradua l weaning . Mil k transfe r wa s measure d b y tes t weighing i n five breast-feedin g dyad s wh o weane d graduall y betwee n 6 an d 1 7 month s lactation. (A) Milk volume transfer as a function o f time postpartum. (B) Relation between the numbers of feeds pe r day and the milk volume. Each set of symbols represents an individua l dyad. Fro m Nevill e et al. (1991). Used b y permission of Am. J. Clin. Nutr.
lower than values obtained by the same investigators for affluent America n women. This difference is due to a difference i n the fat content of the milk (Butte et aL, 1992), probably, as mentioned above , related t o a lower body fat content . Th e value s give n b y Dewe y et al (1991b ) fo r a grou p o f California women are about 10 % higher than the values given by Butte et al fo r th e Texa s women . Althoug h thi s differenc e coul d b e relate d t o calculation from the proximate composition rathe r than actual analysis by bomb calorimetry, i t is more likel y relate d t o the fact tha t the percentag e fat obtained by the California grou p was systematically higher . Because of the systematic variation i n the currendy reporte d values , it is not possibl e at this time to give a single representative valu e fo r th e caloric density o f human milk .
V I . Conclusion s The mean volume of milk transfer in exclusively breast-feeding dyad s can now b e considere d t o b e establishe d fo r most , i f no t all , population s a s about 770 g/day at 3 months postpartum. I n exclusively breast-fed infant s milk transfer varies significantly fro m on e mother-infan t pai r to another with ranges fro m abou t 50 0 t o 120 0 g/day . Th e factor s tha t gover n mil k consumption b y breast-fe d infant s ar e imperfectl y understoo d althoug h most of the variability can be ascribed to infant factors. The weight of the
III
3. Determinant s o f Mil k Volum e an d Compositio n TABLE il l Caloric Density of Human Mil k
Reference
Energy Densit y (cal/g)
Butte etal (1985) / Caucasians (U.S.A. ) (bomb calorimetry)
680 ± 7 1 (37 ) 643 ± 8 3 (40) 625 ± 9 3 (37) 644 ±102 (41 ) 560± 6 0 (15) 530± 70(15 )
1 2 3 4 4 6
697 ± 6 7 (67) 707 ± 9 2 (45) 709 ± 7 4 (28) 796±110(21)
3 6 9 12
Butte^^ a/. (1992) / Mesoamerindians (Mexico) (bomb calorimetry) Nommsen et al. (1991)/ Caucasians (U.S.A.) (calculate d from proximat e composition)
Time postpartu m (months)
Sampling method Expression o f alternate breasts over 24 hr Pumped content s of one breast thre e times daily Expression o f alternate breasts over 24 hr
infant i s the mos t significan t variabl e bu t ca n accoun t a t mos t fo r 30 % of the variation. Further , th e rat e o f mil k consumption pe r kil o decreases as the infan t become s olde r s o ag e mus t als o be take n int o account . Differ ences in energy densit y of the mil k produced b y different wome n accoun t for perhap s 10 % of the variability. I t is possible that mil k volume transfe r is regulate d o n th e basi s o f mil k component s othe r tha n energy . Th e question boil s dow n ultimatel y t o determinatio n o f thos e factor s tha t control infan t appetite , a n are a tha t stil l require s substantia l research . References Allen, J. C, Keller , R. P., Neville, M. C, an d Archer, P . (1991). Studies in human lactation: 6. Mil k compositio n an d dail y secretio n rate s o f macronutrient s i n th e first year o f lactation. Am. J. Clin. Nutr. 54, 69-80. Arthur, P . G., Hartmann , P . E., and Smith , M . (1987). Measuremen t o f th e mil k intak e o f breast-fed infants . J. Fed. Gastroenterol. Nutr. 6 , 758-768 . Arthur, P . G., Jones, T.J. , Spruce , J., an d Hartmann , P . E. (1989) . Measurin g short-ter m rates of mil k synthesis in breast-feeding mothers . Q . /. Exp. Physiol. 74 , 419-428. Brown, K . H., Black , R . E., Robertson , A . D., Akhtar , N . A., Ahmed , G. , an d Becker , S . (1982). Clinical and field trials of huma n lactation: Methodological consideradons . Am. J. Clin. Nutr. 35, 745-756 . Brown, K . H., Stallings , R . Y., Cree d d e Kanashiro , H. , Lope z d e Romafta , G. , an d Black , R. E. (1990). Effects of common illnesses on infants' energy intakes from breast milk and other foods during longitudinal community-based studies in Huascar (Lima), Peru. Am. J. Clin. Nutr. 52, 1005-1013 . Butte, N . F., an d Calloway , D . H. (1981) . Evaluatio n o f lactationa l performanc e o f Navaj o women. Am. J. Clin. Nutr. 34, 2210-2215. Butte, N. P., and Garza, C. (1985). Energy and protein intakes of exclusively brestfed infant s during the first four month s of life . In "Nutritional Need s and Assessmen t o f Norma l
i l 2 Margare
t C. Neville
Growth" (M . Gracey an d F . Falkner , eds.) , pp . 63-81 . Nestl e Nutrition , Vevey/Rave n Press, Ne w York . Butte, N. F., Wong, W. W., Petterson, B. W., Garza, C, an d Klein , P. D. (1988). Human-milk intake measure d b y administratio n o f deuteriu m oxid e t o th e mother : A compariso n with th e test-weighin g technique . Am. J. Clin. NiUr. 47 , 815-821 . Butte, N. F., Wong, W. W., Garza, C., Stuff, J. E., O'Brian Smith, E., Klein, P. D., and Nichols, B.L. (1991a). Energy requirements of breast-fed infants./ . Am. Colloq. NiUr. 10,190-195. Butte, N. F., Wong, W. W., Klein, P. D., and Garza, C. (1991b). Measurement of milk intake: Tracer-to-infant deuteriu m dilutio n method . Br. J. Nutr. 65, 3-14 . Butte, N . F., Villalpando , S. , Wong , W . W., Flores-Huerta , S. , d e Hernandez-Beltran , M. , O'Brian, Smith , E. , and Garza , C . (1992) . Human mil k intak e an d growt h falterin g o f rural Mesoamerindia n infants . Am.J. Clin. Nutr. 55, 1109-1116 . Chandra, R . K. (1981). Breast feeding , growt h an d morbidity . NtUr. Res. 1, 25-31 . Coward, W. A., Whitehead, R . G., Sawyer, M. B., Prentice, A. M., and Evans , J. (1979) . New method fo r measurin g mil k intake s i n breast-fe d babies . Lancet, July 7 , 13-14 . Coward, W. A., Cole, T. J., Gerber , H. , Roberts , S. B., and Fleet , I. (1982a). Water turnove r and th e measuremen t o f mil k intake . Pfluger's Archiv 393, 344-347. Coward, W . A., Cole , T. J., Sawyer , M . B., Prentice , A . M., an d Orr-Ewing , A . K. (1982b) . Breast-milk intak e measuremen t i n mixed-fed s infant s b y administration o f deuteriu m oxide t o their mothers . Hum. Nutr. Clin. Nutr. 36C, 141-148 . Creed d e Kanashiro , H. , Brown , K . H., Lope z d e Romana , G. , Lopez , T. , an d Black , R . E. (1990). Consumption o f foo d an d nutrient s b y infants i n Huasca r (Lima) , Peru. Am. J. Clin. Nutr. 52, 995-1004. Dewey, K. G., and Lonnerdal , B. (1983). Milk and nutrien t intak e of breast-fed infant s fro m 1 to 6 months: Relatio n t o growth an d fatness . /. Ped. Gastroenterol. Nutr. 2, 497-506. Dewey, K . G., an d Lonnerdal , B . (1986) . Infan t self-regulatio n o f breas t mil k intake . Acta Paediatr. Scand. 75 , 893-898. Dewey, K. G., Finley, D. A., and Lonnerdal , B . (1984). Breast mil k volume and compositio n during lat e lactatio n (7-2 0 months) . /. Ped. Gastroenterol. Nutr. 3, 713-720. Dewey, K . G., Heinig , M.J. , Nommsen , L . A., an d Lonnerdal , B . (1991a). Materna l versu s infant factor s relate d t o breast mil k intak e an d residua l mil k volume : Th e DARLIN G study. Pediatrics 87 , 829-837. Dewey, K . G., Heinig , M.J. , Nommsen , L . A., an d Lonnerdal , B . (1991b) . Adequac y o f energy intake among breast-fed infant s in the DARLING study: Relationships to growth velocity, morbidit y an d activit y levels. / Pediatr. 119 , 538-547. Fjeld, C . R., Brown , K . H., an d Schoeller , D . A. (1988) . Validation o f th e deuteriu m oxid e method fo r measurin g averag e dail y mil k intak e i n infants . Am. J. Clin. Nutr. 48 , 671-679. Frigerio, C, Schutz , Y., Whitehead, R., and Jequier, E. (1991). A new procedure to assess the energy requirement s o f lactatio n i n Gambia n women . Am.J. Clin. Nutr. 54, 526-533. Garza, C , Butte , N . F., and Dewey , K . G. (1985) . Determinatio n o f th e energ y conten t o f human milk . In "Huma n Lactatio n 1 : Mil k Component s an d Methodologies " (R . G. Jensen an d M . C. Neville, eds.), pp. 121-125 . Plenum Press , Ne w York . Goldberg, G . R., Prentice , A . M., Coward , W . A., Daries , H . L., Murgatroyd , P . R., Sawyer , M. B., Ashford, J., an d Black , A. E. (1991). Longitudinal assessment of the components of energ y balanc e i n well-nourished lactatin g women. Am.J. Clin. Nutr. 54, 788-798. Hendrikson, E . C, Seacat , J. M., and Neville , M. C. (1985). Insensible weight loss in children under on e yea r o f age . Acta Paediatr. Scand. 74(5) , 678-680. Hofvander, Y. , Hagman , U. , Hillervik , C , an d Sjolin , S . (1982) . Th e amoun t o f mil k consumed b y 1- 3 month s ol d breast - o r botde-fe d infants . Acta Paediatr. Scand. 71 , 953-958. Linzell, J . L. (1967) . Th e effec t o f frequen t milkin g an d o f oxytoci n o n th e yiel d an d composition o f mil k in fe d an d faste d goats . /. Physiol. 190 , 333-346. Macy, I. G., Hunscher , H . A., Donelson , E. , and Nims , B. (1930). Human mil k flow. Am. J. Dis. Child. 6 , 492-515.
3. Determinant s o f Mil k Volum e an d Compositio n 11
3
Neville, M . C, an d Oliva-Rasbach , J. (1987) . I s materna l mil k productio n limitin g fo r infan t growth durin g th e first yea r o f lif e i n breast-fe d infants ? In "Huma n Lactation : Effec t of Huma n Mil k o n th e Recipien t Infant " (A . Goldma n an d S . A. Atkinson , eds.) , pp . 123-133. Plenu m Press , Ne w York . Neville, M. C, Keller , R., Seacat , J., Lutes , V., Neifert , M. , Casey, C, Allen , J. A., and Archer , P. (1988). Studies in human lactation : Mil k volumes i n lactating women durin g the onse t of lactatio n an d ful l lactation . Am. J. Clin. Ntur. 48 , 1375-1386 . Neville, M . C, Allen , J. C, Archer , P . G., Seacat , J., Casey , C , Sawicki , V. , Oliva-Rasbach , J., and Neifert , M . (1991) . Studie s i n huma n lactation : 7 . Mil k volum e an d nutrien t composition durin g weanin g an d lactogenesis . Am. J. Clin. Nutr. 54 , 81-93 . Nommsen, L . A., Lovelady , C . A., Heinig , M . U., Lonnerdal , B. , an d Dewey , K . G. (1991) . Determinants o f energy , protein , lactos e concentration s i n huma n mil k durin g th e first 12 m o o f lactation : Th e DARLIN G study . Am. J. Clin. Nutr. 53 , 457-465 . Pao, E . M., Himes , J . M. , an d Roche , A . F . (1980) . Mil k intake s an d feedin g pattern s o f breast-fed infants . J. Am. Diet. Assoc. 77, 540-545 . Prentice, A . M., Whitehead , R . G., Roberts , S . B., an d Paul , A . A. (1981) . Long-ter m energ y balance i n child-bearin g Gambia n women . Am. J. Clin. Nutr. 34 , 2790-2799 . Prentice, A. M., Roberts, S. B., Prentice A., Paul, A. A., Watkinson, M., Watkinson, A. A., an d Whitehead, R . G. (1983) . Dietar y supplementatio n o f lactatin g Gambia n women . I . Effect o n breas t mil k volum e an d quality . Hum. Nutr. Clin. Nutr. 37C , 53-64 . Prentice, A.M. , Paul , A. , Prentice , A. , Black , A. , Cole , T. , an d Whitehead , R . (1986) . Cross-cultural difference s i n lactationa l performance . In "Huma n Lactation : Maternal and Environmenta l Factors " (M. Hamos h an d A . S. Goldman, eds.) , pp . 13-50 . Plenu m Press, Ne w York . Rattigan, S. , Ghisalberti , A . V., an d Hartmann , P . E. (1981) . Breast-mil k productio n i n Australian women . Br. J. Nutr. 45 , 243-249 . Rowland, M . G. M., Go h Rowland , S . G. I. , an d Cole , T.J . (1988) . Impac t o f infectio n o n th e growth o f childre n fro m 0 t o 2 year s i n a n urba n Wes t Africa n community . Am. J. Clin. Nutr. 47 , 134-138 . Saint, L. , Maggiore , P. , an d Hartmann , P . E. (1986) . Yiel d an d nutrien t conten t o f mil k i n eight women breast-feedin g twin s and on e woma n breast-feedin g triplets . Br. J. Nutr. 56 , 49-58. Salmenpera, L. , Perheentupa, J., and Siimes , M. (1985). Exclusivel y breast-fe d health y infant s grow slowe r tha n referenc e infants . Pediatr. Res. 19 , 307-312 . Stuff, J. E. , Garza , C , Boutte , C , Fraley , J. K. , Smith , E . O., Klien , E . R., an d Nichols , B . L. (1986). Sources of varianc e in milk and caloric intakes in breast-fed infants : Implication s for lactatio n stud y desig n an d interpretation . Am. J. Clin. Nutr. 43 , 361-366 . Thornburn, C . C, an d Bailey , C.J . (1983) . Us e o f a T - or har d P-emittin g radioisotop e t o assess mil k intak e i n sucklin g mous e pups./ . Nutr. 113 , 805-812 . van Raaij , J. M . A., Schonk , C . M., Vermaat-Miedema , S . H., Peek , M . E. M., an d Hautvast , J. G. A.J. (1991) . Energ y cos t o f lactatio n an d energ y balance s o f well-nourishe d Dutc h lactating women : Reappraisa l o f th e extr a energ y requiremen t o f lactation . Am. J. Clin. Nutr. 53 , 612-619 . van Steenbergen, W . M., Kusin , J. A., an d Va n Reus , M. M. (1981). Lactatio n performanc e o f Akamba mothers , Kenya . Breas t feedin g behaviour , breas t mil k yiel d an d composition . y. Trop. Fed. 27 , 155-161 . Walgren, A . (1944) . Breast-mil k consumptio n o f health y full-ter m infants . Acta Paediatr. Scand. 32, 778-790 . Whitehead, R . G., an d Paul , A . A. (1981) . Infan t growt h an d huma n mil k requirements : A fresh approach . Lancet 2, 161-163 . Woolridge, M . W., Butte , N. , Dewey , K . G., Ferris , A. M. , Garza , C , an d Keller , R . P. (1985). Methods fo r th e measuremen t o f mil k volum e intak e o f th e breast-fe d infant . In "Human Lactation : Mil k Component s an d Methodologies " (R . G. Jense n an d M . C. Neville, eds.) , pp . 5-20 . Plenu m Press , Ne w York .
100 Margare
t C . Nevill e
II. Method s for Measuremen t of Milk Volum e In th e measuremen t o f mil k volum e i t is important t o distinguish betwee n milk yield an d mil k transfer to the infant. I n dair y animal s mil k yield , th e amount o f mil k tha t i s transferre d fro m th e mammar y glan d t o th e mil k pail o r milkin g machine , i s th e appropriat e measure . I n general , thi s quantity represent s th e productiv e capacit y o f th e glan d whe n i t is milke d empty a t least twic e a day. I n humans , mil k transfe r t o the infan t i s almos t always th e valu e sought . Becaus e th e breas t i s no t usuall y emptie d com pletely a t a feed, thi s valu e i s somewhat lowe r tha n th e mil k yiel d tha t ca n be obtained b y expression o f mil k with a good electri c breas t pump severa l times durin g a 24-h r perio d (Nevill e et ai, 1987 ; Dewe y et al., 1991a) . Several method s ar e availabl e fo r measuremen t o f mil k volum e pro duction. Th e first, expressio n o f th e content s o f th e breas t b y pum p o r manually, is , a s mentione d above , th e metho d almos t universall y use d t o obtain mil k volum e i n dair y animals . O f th e othe r availabl e method s test weighing the young before an d after each feed fo r a specified perio d of tim e is conceptuall y th e simplest . Isotope dilution, virtuall y th e onl y accurat e method availabl e fo r th e measuremen t o f mil k productio n i n smal l labo ratory mammals, has recently been applied usin g stable isotopes t o human s (Butte et al., 1988) . The Doppler ultrasound human milk flowmeter (Woolridge et al, 1985) , whic h use s ultrasoun d t o measur e mil k velocit y a s i t travel s from mothe r t o infant , ha s no t bee n foun d t o b e particularl y reliabl e fo r any bu t ver y short-ter m measurement s o f mil k flow an d wil l no t b e examined furthe r here . A ne w metho d base d o n topographical computer imaging o f th e breas t ha s recentl y becom e availabl e fo r short-ter m mea surement o f mil k productio n i n wome n (Arthu r et al, 1989 ) an d wil l b e discussed briefl y althoug h i t ha s no t ye t receive d extensiv e evaluation . A. Extraction of Milk Extraction o f mil k b y pump , milkin g machine , o r manuall y ca n achiev e nearly complet e emptyin g o f th e mammar y glan d i f a n adequat e let-dow n is accomplished . Moder n breedin g practice s hav e produce d dair y catd e that le t dow n t o th e milkin g machine , s o tha t extractio n efficienc y i s excellent. Nevertheless , t o achiev e complet e extractio n i n goats , Linzel l (1967) gave an iv dose of oxytocin just prior to milking. LinzelP s technique , used t o measur e hourl y mil k yield , wa s adapte d t o wome n b y Nevill e et al. (1988). Briefly, a n electric breast pum p with dual heads was used t o extract milk fro m th e breasts ; afte r 1 0 mi n o f pumpin g on e dro p o f syntheti c oxytocin wa s administere d intranasall y an d pumpin g continue d fo r a further 5 min . Th e volume s obtaine d durin g th e first an d secon d hour s were higher than the average milk production due to extraction of residua l
3. Determinant s o f Mil k Volum e an d Compositio n 10
1
milk (mea n tota l exces s 20 0 ± 25 ml) . After th e thir d pumpin g episod e th e mean hourly milk extraction in five women did not differ significantl y fro m the mil k volum e measure d b y tes t weighin g durin g a precedin g 24-h r period. Suc h a pumpin g regime n ma y b e usefu l whe n mil k yiel d i s t o b e assessed o n a short-ter m basis . Others hav e use d mil k extractio n t o measur e 24-h r mil k yield . Brow n et al. (1982 ) extracte d al l mil k b y breas t pum p fo r 2 4 h r an d compare d extracted volume s wit h mea n volume s obtaine d b y 6 days of tes t weighing . Pumped volume s exceede d test-weig h volume s b y 5 0 g/da y o r abou t 7% , again reflectin g residua l milk . Dewe y et al. (1991a) , usin g a breast pum p t o extract milk fro m alternat e breasts at each fee d ove r a 24-hr period , foun d residual volume s o f abou t 11 0 ml/day . Al l investigator s have , therefore , found tha t mil k volum e transfe r i s overestimate d whe n measure d b y th e extraction technique . Th e amoun t o f th e overestimat e varie s fro m 5 0 t o 200 ml/da y dependin g o n th e populatio n an d techniqu e used . B. Test Weighing
In mos t studie s fo r whic h value s ar e give n i n Tabl e I , th e infan t wa s tes t weighed befor e an d afte r ever y fee d fo r a t leas t 2 4 hr . Thi s procedur e i s usually carrie d ou t b y th e mothe r i n th e hom e afte r a brie f perio d o f training, althoug h traine d worker s hav e bee n use d i n th e field o r clinic i n some studies , particularl y i n developin g nation s (Brow n et al, 1982 ; Pren tice et al.y 1983) . Becaus e th e day-to-da y coefficien t o f variatio n fo r mil k transfer i n a singl e mother-infan t pai r i s quit e hig h [15 % i n on e stud y (Butte et aly 1985) , 8.9 % i n anothe r (Dewe y et al, 1991a)] , curren t rec ommendations sugges t tha t tes t weighin g b e continue d fo r 4 day s whe n accurate measurement s ar e neede d fo r a singl e individua l (Stuf f et a/. , 1986). However , 24-h r o r eve n properl y standardize d 12-h r tes t weight s appear to give equivalent populatio n mean s (Prentice et a/., 1981 ; Creed d e Kanashiro et a/., 1990) . An integratin g electronic balance provides the mos t accurate data , particularl y i f th e infan t i s moving (Nevill e et a/., 1988) . Fo r older children it is possible to suspend a swing from th e balance (Woolridg e et a/., 1985) . I f th e balanc e print s ou t th e weight , error s i n recordin g ar e minimized. Tes t weighin g result s i n a systemati c underestimatio n o f th e volume o f mil k produce d becaus e o f insensibl e wate r los s throug h respi ration an d sweatin g durin g th e feed . Thi s los s fro m th e infan t amounte d to 0.03 g/kg/mi n i n on e stud y (Hendrikso n et a/., 1985 ) an d 0.0 5 g/kg/mi n in anothe r (Nommse n et a/., 1991) . Thi s numbe r i s multiplied b y th e tota l nursing tim e pe r 2 4 hour s an d th e weigh t o f th e infan t t o obtai n th e correction whic h usuall y amount s t o 3 to 5 % of th e measure d dail y intake . It is possibl e t o obtai n satisfactor y mil k yield s b y weighing th e mothe r rather tha n th e infan t befor e an d afte r th e fee d i f a sufficientl y sensitiv e balance i s available (Arthu r et a/., 1987) . However , th e result s obtaine d ar e less reliabl e tha n tes t weighin g th e infan t becaus e th e amoun t o f mil k
102
Margaret C . Nevill e
TABLE I Volume of Milk Transferred from Mother t o Infan t i n the Exclusivel y Breast-Feeding Dyad
Months ]postpartumI Reference/Country Neville et aL (1988) / United State s (Denver, CO) mean SD n Pao et aL (1980)/United States (Ohio) mean SD n van Steenbergen et at. (1981)/Kenya mean SD n Hofvander et aL (1982) / Uppsala, Sweden mean Range n Butte and Calloway, (1981)/United State s (Navajo) mean SD n
1
668 117 12
3
4
5
6
7
8
694 98 12
734 114 10
711 100 12
838 134 12
820 79 9
848 63 6
818 158 3
755 113 111
741 103 26
818 166 8
875 142 8
834 99 8
600 159 11
833
778** 180 7
619** 197 13
656 360860 25
2
773 575985 25
776 600937 25
725 129 40
723* 114 37
634 113 10
Butte et aL (1991a) / United State s (Texas) mean 738* SD 157 64 n De^ey etaL (1984) / United State s (California ) mean SD n Dewey and LSnnerda l (1983)/United State s (California) mean SD n
2
672 192 16
756 170 19
782 172 16
810 142 13
805 117 11
896 122 11
103
3. Determinant s o f Mil k Volum e an d Compositio n TABLE I (continued) Months p>ostpartum Reference/Country
1
2
3
Salmenpera et al. (1985) / Finland mean SD n
4
790 140 12
800 120 31
747 19 48
740** 16 26
Walgren (1944 ) Sweden (girls ) mean Variance n
576** 80 65
Walgren (1944 ) Sweden (Boys ) mean Variance n
645*** 750*** 798*** 821** * 97 107 122 113 58 42 49 72
704* 98 72
733* 113 43
7
6
5
8
817*** 133 33
Whitehead an d Pau l (1981) Unite d Kingdo m (girls) mean SD n
677 87 20
742 119 17
775 138 14
814 113 6
838
854
786
1
1
1
Whitehead an d Pau l (1981) Unite d Kingdo m (boys) mean SD n
791*** 820 187 116 27 23
829 168 18
790 113 5
922
Stuff et al. (1986)/Unite d States (Houston , TX ) mean SD n
735 85 9
Chandra (1981)/Canad a mean SD n van Raai j et ai (1991) / The Netherland s mean SD n Nommsen et al. (1991) / United State s (California ) mean SD n
1
793 71 33
692 122 16
745 131 40
811* 133 58
856 99 31
925** 112 28
872* 126 27
815 97 24
104
Margaret C. Neville
T A B L E I (continued) ]Vfonths
Reference/Country Frigerio ^ f fl/. (1991)/ The Gambi a mean SD n Butte et al. (1992)/ Mexico (rural ) (^HgO t o mothers ) mean SD n Goldberg ^ ^ a/. (1991) / Cambridge, Englan d (H2*»0 to mother ) mean SD n Weighted mea n (test weigh only) mean SD n
1
2
3
f)ostpartu m
4
5
6
7
8
809 120 42
819 100 36
738 47 16
885** 146 15
792 177 10
802** 179 10
657 121 284
869* 150 15
735 111 343
767 111 293
773 112 313
802 109 100
827 102 148
*p < 0.0 5 with respec t t o weighted mean . **p < 0.0 1 with respec t t o weighted mean . ***Significantly differen t fro m girls , p < 0.05 .
transferred compare d t o th e mother' s bod y weigh t i s smal l an d th e correction fo r insensibl e weigh t los s i s substantial . Mil k volume s obtaine d using thi s procedur e i n Australi a wer e usuall y considerabl y greate r tha n the value s give n i n Tabl e I (Rattiga n et al, 1981) ; however , thes e earl y values wer e no t correcte d fo r insensibl e wate r loss . Whe n th e correctio n was made, mil k volumes within th e rang e of othe r reporte d studie s were obtained (Arthu r et al, 1987) . The advantag e o f tes t weighin g i s tha t i t i s a reliabl e an d relativel y inexpensive wa y t o measur e mil k transfe r fro m mothe r t o infant . Th e major disadvantag e i s tha t th e techniqu e require s a certai n degre e o f education and dedication on the part of the mother or the presence in the home of a trained field worker. It can disrupt the feeding routine especially if frequen t nighttim e feed s ar e th e norm .
3. Determinant s o f Mil k Volum e an d Compositio n 10
5
C. Isotope Dilution Isotope dilution was used first in animals and is the only technique availabl e for smal l animal s suc h a s rat s an d mice . Th e mothe r i s give n a dos e o f tritiated wate r an d th e passag e o f isotop e t o th e youn g i s tracked b y whol e body analysi s o f pup s a t intervals (Thornbur n et al, 1983) . I n human s i t is not possibl e t o use radioactiv e isotopes ; fortunately, wate r can be obtaine d labeled wit h stabl e isotopes , namely , deuteriu m o r ^^O . Deuterium oxid e was firs t use d b y Cowar d an d colleagues . I n thei r earlies t studie s (Cowar d et al., 1979 , 1982a ) th e isotop e wa s administered t o th e infan t an d th e rat e of dilutio n ove r a perio d o f severa l day s wa s determine d b y mas s spec trometry. I n thi s form th e techniqu e ha s been show n t o be usefu l bu t onl y if a correctio n i s mad e fo r exchang e o f wate r a t th e integumenta l an d respiratory surface s a s wel l a s intak e o f wate r fro m source s othe r tha n breast mil k (Fjeld et ai, 1988 ; Butt e et ai, 1991b) . I n late r studie s Cowar d et al. (1982b ) an d other s (Butt e et al., 1988 ) administere d th e isotope t o th e mother an d measure d deuteriu m enrichmen t i n th e mother' s mil k an d infant's urin e t o calculate mil k transfer . I t is necessary t o know th e infant' s total bod y wate r whe n usin g thi s method ; thi s paramete r ca n bes t b e estimated by administering a separate dose of 2H2O or H2^®0 to the infant . Careful evaluatio n o f isotop e dilutio n agains t th e test-weighin g metho d (Butte et ai, 1988 ) i n nine wome n gav e a mean differenc e betwee n th e tw o methods o f 2% , no t statisticall y significan t whe n metaboli c wate r produc tion wa s take n int o account . Isotop e dilutio n ha s th e advantag e o f eas e o f sampling and require s litde cooperation o n th e par t of th e mother. I t gives mean mil k intak e ove r severa l days . I t ha s th e disadvantag e o f requirin g sophisticated an d expensiv e analytica l techniques . Nevertheless , th e tech nique is finding increasin g us e fo r studies in developing countries (Cowar d et al., 1982b ; Butt e et al., 1992 ; Goldber g et al., 1991) . D. Topographical Computer Imaging Hartmann an d hi s colleague s (Arthu r et al, 1989 ) hav e develope d a technique i n whic h moir e pattern s ar e projecte d ont o th e lactatin g breast . Video image s obtaine d ove r a perio d o f tim e ar e store d i n th e compute r for late r analysis . A s th e breas t expand s wit h increasin g store d mil k th e moire pattern s chang e i n a way tha t ca n b e relate d t o th e volum e o f mil k produced. Thi s promisin g techniqu e ha s the potentia l o f measurin g short term rate s o f mil k synthesi s betwee n breas t feed s an d fo r tha t reaso n should b e mor e completel y evaluated . Wit h th e increasin g availabilit y o f computers suitabl e fo r thi s typ e o f task , th e cos t o f thi s metho d ma y become quit e reasonable , particularl y i n th e clinica l setting .
106 Margare
t C . Nevill e
III. Mil k Volumes in Exclusively Breast Feeding Women Table I is a compilation of worldwide values for milk transfer in exclusively breast-feeding women . Whe n mea n values , weighte d fo r th e numbe r o f subjects in each study, are calculated breast milk transfer is seen to increase gradually from about 650 g/day at 1 mont h to about 800 g/day at 6 months when it appears to level off (Figur e 1) . The variatio n between individual s is large wit h mea n SD s about 10 0 g/da y a t all tim e points . Mil k volume s from tw o underprivilege d groups , Navaj o Indian s an d wome n i n Th e Gambia, did no t differ fro m th e overall mea n in early lactation an d milk volumes from Kenya at 1 mont h were actually significantly higher than the mean (Tabl e I) . The consistenc y betwee n th e variou s populatio n group s suggest tha t nutritiona l an d cultura l factor s hav e littl e effec t o n mil k transfer i n the exclusivel y breast-feedin g dyad . Milk volume s obtaine d b y isotop e dilutio n i n Cambridge , Englan d were significantly higher than the overall mean at 1 mont h postpartum but not significandy differen t thereafte r fro m value s obtained usin g th e test weighing method. The mil k volumes measured in a group of undernour ished Mesoamerindian s usin g th e isotope dilutio n techniqu e wer e signifi candy highe r a t 4 an d 6 month s tha n th e mea n value s i n the table . Thi s finding was attribute d b y th e author s t o th e lowe r calori c densit y o f th e milk in this group (se e below). The rang e of mil k volumes among individuals varies from abou t 50 0 to 110 0 g/da y (Figur e 1) . I n a well-nourishe d populatio n n o materna l characteristics wer e foun d t o correlat e wit h breas t mil k transfe r t o th e infant leading Dewe y and he r colleagues t o propose tha t "infant deman d is the main determinant of lactation performance" in affluent population s (Dewey et al., 1991a). A similar study in malnourished populations has not been published, but Butte et al, (1992) proposed that milk production may be subject to maternal limitations on the basis of he r study of Mesoamer indians i n whic h mil k transfe r appeare d t o b e insufficien t t o suppor t optimal infant growth after 3 months postpartum. Infant factors related to milk production include d infan t weigh t (Nevill e et al., 1988 ; Dewey et al, 1991a) an d tota l tim e nursin g (Dewe y et ai, 1991a) . Th e differenc e between boy s and girl s disappear s whe n thei r weigh t differenc e i s taken into account . I n general , althoug h earlie r author s suggeste d tha t infan t morbidity would alter milk volume transfer (Prentice et ai, 1981) , this has not prove n t o b e th e case . I n a careful stud y b y Brow n an d co-worker s (Brown et al, 1990) diarrhea or fever were associated with no changes in the frequency o f breast-feeding, tota l suckling time, or amount of breast milk consumed. Dat a supportin g thi s conclusio n hav e bee n obtaine d b y Rowland et ai (1988 ) an d Butt e et al. (1992). The caloric density of milk may be a factor in determining the volume of milk transferred t o the infant. Butte et al, (1992) suggested that the low
3. Determinant s o f Mil k Volum e an d Compositio n
107
1200
Months Postpartu m Figure I Mil k transfe r t o exclusivel y breast-fe d infants . Heav y lin e represent s weighte d mean from al l studies using test weighing in Table I and shaded area represents one standard deviation fro m th e mean . Are a betwee n ligh t line s represents th e 95 % confidence interval .
caloric density of the milk (see below) was a factor in the high milk volumes noted i n Mesoamerindians . Nommse n et al. (1991 ) foun d a significan t inverse relationshi p betwee n mil k intak e an d mil k energ y densit y i n a group o f affluen t America n women . Th e effec t o f othe r compositio n variables on milk transfer has been incompletely investigated. Nommsen et al, (1991 ) foun d a significan t (p < 0.05 ) invers e relatio n betwee n mil k volume and milk protein concentrations at 6 and 9 months postpartum in an affluen t population . The y als o foun d a positive correlatio n wit h mil k lactose concentratio n a t th e sam e stages . However , bot h thes e change s could hav e bee n th e resul t o f th e inclusio n o f wome n i n th e earl y stage s of weanin g i n thei r stud y population . I n thei r stud y wome n wer e onl y considered to be weaning, and therefore excluded from the analysis if their milk volume s wer e belo w 20 0 m l pe r day . Nevill e et al. (1991) foun d a n increase i n protei n concentratio n an d a decrease i n lactose concentratio n when mil k volume fel l belo w 400 ml/da y i n affluent America n women. I t would b e o f interes t t o kno w whethe r th e invers e relatio n observe d b y Nommsen et a/. (1991) persists when women transferring between 200 and 400 g of milk per day are excluded from statistical analysis. The correlation between mil k volume an d the rat e of transfe r o f othe r mil k components, such as calcium, magnesium, or other minerals, to the infant has not been investigated systematicall y althoug h th e relevan t dat a ar e probabl y avail able i n som e studies . I n on e stud y (Alle n et al., 1991) , fo r example , th e amounts of lactose, magnesium, and ionized calcium transferred t o a given infant o n Da y 2 1 o f lactatio n wer e highl y correlate d wit h th e amount s transferred a t 6 months postpartum although the concentrations o f thes e substances varied significantl y throug h lactation . The numbe r o f subject s in thi s stud y (13 ) wa s no t sufficien t t o mak e meaningfu l correlation s between th e rat e of mil k transfer an d productio n o f thes e nutrients .
108 Margare
t C . Nevill e
IV. Breas t Mil k Volume s Transferre d t o Partially Breast-Fe d infant s It i s difficul t t o giv e universa l value s o f breas t mil k volume s i n partiall y breast-fed infants because the pattern of supplementation differs from one cultural grou p t o another . However , tw o circumstances ar e o f particula r interest. On e is the infant who is breast-fed severa l time s a day, receivin g supplemental foo d o n a meal-by-mea l basis , bu t breast-feed s ar e no t replaced b y supplementa l feeding s o r bottles. A smal l grou p o f Wester n women who fed accordin g to this pattern transferred abou t 600 g of milk per day to their infants at 1 year of age (Neville et al., 1991). This patter n is prevalent in developing countries where breast-feeding o f longer duration is the norm. The second pattern is the infant who is gradually weaned by replacing feeds with meals containing milk or formula and other foods. This i s the patter n ofte n note d durin g weanin g i n affluent societies . A stud y b y Cree d d e Kanoshir a et al. (1990 ) i n Per u provide s a n excellent exampl e o f th e first pattern . Th e infant s wer e supplemente d from a n earl y ag e ( < 3 months ) wit h a variety o f food s includin g dair y products and, as time progressed, cereals. Breast milk consumed remaine d at a high level (> 55 0 ml per day) throughout the first year in 89% of the infants. Th e actua l dail y volume s o f breas t mil k consume d ar e give n i n Table II . Thes e volume s wer e abou t 93 % of th e volume s transferre d t o exclusively breast-fe d infant s a t 2 months (Tabl e I ) and decrease d slowl y to about 75% at 6 months. By 10-12 months the infants were still receiving about 45 % o f thei r tota l energ y fro m breas t milk . Thus , thes e infant s continued to obtain a substantial proportion of their nutrition from breast milk at 1 year and after. Dat a from The Gambia and Papua, New Guinea gave similar volume estimates. Note that the variability between individuals is about twic e tha t seen i n th e exclusivel y breast-feedin g group . In contrast. Figure 2A shows the volumes of breast milk consumed by five American infants whose mother s deliberately bega n gradua l weanin g at about 6 month s o f ag e b y substitutin g formul a feed s fo r breas t feeds . Milk volumes gradually decreased, reaching zero by 17 months postpartum or earlier. When milk transfer was plotted as a function of number of feeds per day for each mother-infant pai r (Figure 2B), it became clear that milk volume was linearly relate d t o the number of feeds , fallin g t o zero at one feed pe r day . Th e dat a i n Figur e 2 als o mak e i t clea r tha t o n a crosssectional basis little correlation between numbe r of fed s pe r day and milk volume woul d b e expecte d sinc e subject s producin g ove r 60 0 g/da y fe d between 4 and 1 2 times pe r day, depending o n th e individual . V. Calori c Densit y o f Huma n Mil k The caloric density of human milk is best determined by bomb calorimetry (Garza et al., 1985) . However , man y investigator s calculat e thi s quantit y
3. Determinant s o f Mil k Volum e an d Compositio n 10
9
TABLE I I Breast Milk Transfer i n Partially Breast-Fe d Infant s Milk volume :t S D (n )
Duration o f lactatio n (Months)
Creed d e Kanashir o et al (1990) / Peru (12-h r tes t weig h extrapolate d to 2 4 hr )
685 ±245 (128 ) 6 9 0 ± 2 4 0 (121 ) 655 ± 2 26 (108 ) 624±219(103) 565 ±20 8 (89)
1.0-2.9 3.0-4.9 5.0-6.9 7.0-9.9 10.0-12.5
Prentice et al (1986)/Keneba , Th e Gambia (24-h r tes t weigh )
582 ±16 9 643 ± 1 4 9 607±131 594 ±20 0 633 ± 2 0 0
(10) (17) (16) (16) (15)
3-3.99 4-5.99 5-8.99 9-11.99 12-18
Prentice et al. (1986)/Cambridge , England (96-h r tes t weigh/4 )
783 ±17 6 717±207 588 ±20 6 493 ±21 6 342 ±22 8 328 ±29 2
(48) (42) (45) (38) (31) (19)
3-3.99 4-5.99 5-5.99 6-7.99 7-8.99 9-10.99
Dewey et al (1991b)/Davis , C A (4-day tes t weigh )
769±171 646±217 448 ±25 1
(60) (50) (42)
6 9 12
Coward et al (1982b)/Th e Gambi a (^HgO t o mother )
752± 3 6 757± 4 4 728 ±17 0
(4) (4) (5)
0-4 5-9 >9
Coward et al (1982b)/Papua , Ne w Guinea (^Hg O t o mother )
670 ±18 4 (17) 936 ± 1 8 3 (8)
0-4 5-9
Reference
from th e proximate composition o f the milk using the following factor s i n kcal/gm: 5.6 5 protein , 9.2 5 fat , 3.9 5 lactose , 5.6 5 nonprotei n nitrogen . Other author s hav e use d th e factor s 4 , 9, an d 4 kcal/g m fo r protein , fat , and lactose , respectivel y (Cree d d e Kanashir o et al., 1990) . Because lipid s are th e larges t contributo r t o th e calori c density , i t is important tha t car e be taken t o obtain a representative mil k sample. If thi s is not done, or th e milk sampl e i s store d i n suc h a wa y tha t a representativ e aliquo t i s no t assayed, erroneou s value s ca n result . A secon d cautio n i s tha t som e methods fo r lactos e measurements, notabl y th e automate d enzym e proce dure on the Yellow Springs Instrument Analyzer , probably do not include the oligosaccharide s o f huma n mil k tha t compris e abou t 1 % of th e tota l weight of mil k i n normal circumstance s an d ma y contribute eve n mor e in conditions suc h a s diabete s (Ferris , persona l communication) . Us e o f th e standard factor s in these circumstances may result in a small but systematic underestimation o f th e calori c conten t o f th e milk . Representative value s fo r calori c density ar e give n i n Tabl e III . Not e that th e value s fo r undernourishe d Mesoamerindian s ar e abou t 10 0 cal/g
Margaret C . Nevill e
110 1000 rN
•d *^ 60 Sm/
u 0
750 500 250 0
(H M
59
a«
^ 1000 •^
S
1
31
7
Months Postpartum •
750 500 250
"B
0
03
6
9
1
2
Feeds pe r Da y Figure 2 Mil k volume s durin g gradua l weaning . Mil k transfe r wa s measure d b y tes t weighing i n five breast-feedin g dyad s wh o weane d graduall y betwee n 6 an d 1 7 month s lactation. (A) Milk volume transfer as a function o f time postpartum. (B) Relation between the numbers of feeds pe r day and the milk volume. Each set of symbols represents an individua l dyad. Fro m Nevill e et al. (1991). Used b y permission of Am. J. Clin. Nutr.
lower than values obtained by the same investigators for affluent America n women. This difference is due to a difference i n the fat content of the milk (Butte et aL, 1992), probably, as mentioned above , related t o a lower body fat content . Th e value s give n b y Dewe y et al (1991b ) fo r a grou p o f California women are about 10 % higher than the values given by Butte et al fo r th e Texa s women . Althoug h thi s differenc e coul d b e relate d t o calculation from the proximate composition rathe r than actual analysis by bomb calorimetry, i t is more likel y relate d t o the fact tha t the percentag e fat obtained by the California grou p was systematically higher . Because of the systematic variation i n the currendy reporte d values , it is not possibl e at this time to give a single representative valu e fo r th e caloric density o f human milk .
V I . Conclusion s The mean volume of milk transfer in exclusively breast-feeding dyad s can now b e considere d t o b e establishe d fo r most , i f no t all , population s a s about 770 g/day at 3 months postpartum. I n exclusively breast-fed infant s milk transfer varies significantly fro m on e mother-infan t pai r to another with ranges fro m abou t 50 0 t o 120 0 g/day . Th e factor s tha t gover n mil k consumption b y breast-fe d infant s ar e imperfectl y understoo d althoug h most of the variability can be ascribed to infant factors. The weight of the
III
3. Determinant s o f Mil k Volum e an d Compositio n TABLE il l Caloric Density of Human Mil k
Reference
Energy Densit y (cal/g)
Butte etal (1985) / Caucasians (U.S.A. ) (bomb calorimetry)
680 ± 7 1 (37 ) 643 ± 8 3 (40) 625 ± 9 3 (37) 644 ±102 (41 ) 560± 6 0 (15) 530± 70(15 )
1 2 3 4 4 6
697 ± 6 7 (67) 707 ± 9 2 (45) 709 ± 7 4 (28) 796±110(21)
3 6 9 12
Butte^^ a/. (1992) / Mesoamerindians (Mexico) (bomb calorimetry) Nommsen et al. (1991)/ Caucasians (U.S.A.) (calculate d from proximat e composition)
Time postpartu m (months)
Sampling method Expression o f alternate breasts over 24 hr Pumped content s of one breast thre e times daily Expression o f alternate breasts over 24 hr
infant i s the mos t significan t variabl e bu t ca n accoun t a t mos t fo r 30 % of the variation. Further , th e rat e o f mil k consumption pe r kil o decreases as the infan t become s olde r s o ag e mus t als o be take n int o account . Differ ences in energy densit y of the mil k produced b y different wome n accoun t for perhap s 10 % of the variability. I t is possible that mil k volume transfe r is regulate d o n th e basi s o f mil k component s othe r tha n energy . Th e question boil s dow n ultimatel y t o determinatio n o f thos e factor s tha t control infan t appetite , a n are a tha t stil l require s substantia l research . References Allen, J. C, Keller , R. P., Neville, M. C, an d Archer, P . (1991). Studies in human lactation: 6. Mil k compositio n an d dail y secretio n rate s o f macronutrient s i n th e first year o f lactation. Am. J. Clin. Nutr. 54, 69-80. Arthur, P . G., Hartmann , P . E., and Smith , M . (1987). Measuremen t o f th e mil k intak e o f breast-fed infants . J. Fed. Gastroenterol. Nutr. 6 , 758-768 . Arthur, P . G., Jones, T.J. , Spruce , J., an d Hartmann , P . E. (1989) . Measurin g short-ter m rates of mil k synthesis in breast-feeding mothers . Q . /. Exp. Physiol. 74 , 419-428. Brown, K . H., Black , R . E., Robertson , A . D., Akhtar , N . A., Ahmed , G. , an d Becker , S . (1982). Clinical and field trials of huma n lactation: Methodological consideradons . Am. J. Clin. Nutr. 35, 745-756 . Brown, K . H., Stallings , R . Y., Cree d d e Kanashiro , H. , Lope z d e Romafta , G. , an d Black , R. E. (1990). Effects of common illnesses on infants' energy intakes from breast milk and other foods during longitudinal community-based studies in Huascar (Lima), Peru. Am. J. Clin. Nutr. 52, 1005-1013 . Butte, N . F., an d Calloway , D . H. (1981) . Evaluatio n o f lactationa l performanc e o f Navaj o women. Am. J. Clin. Nutr. 34, 2210-2215. Butte, N. P., and Garza, C. (1985). Energy and protein intakes of exclusively brestfed infant s during the first four month s of life . In "Nutritional Need s and Assessmen t o f Norma l
i l 2 Margare
t C. Neville
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