The Volume And Composition Of Human Milk In Poorly Nourished Communities A Review

perspectives in nutrition The volume and composition of human milk in poorly nourished communities A review1 Derrick B. Jelliffe and E. F. Patrice Jelliffe “How is it that poor men’s wives, who have no cold fowl or port wine on which to be Downloaded from www.ajcn.org by on August 22, 2009 coshered up, nurse their children without difficulty, whereas the wives of rich men, who eat and drink everything that is good, cannot do so, we will for the present leave to the doctors and mothers to settle between them.” Anthony Trollope (1847) The question of the composition and vol- comparison of breast feeding and formula ume of breast milk produced by mothers on feeding as they exist in the nutritional, hy- different planes of nutrition at different gienic, and economic circumstances usually phases of lactation is a major issue in pedi- found in villages and urban shanty towns in atnic public health in the world, especially resource-poor, less developed countries, in resource-poor countries. mainly in the subtropics and tropics (77). Fundamentally, ultimate concerns are the Considerations of the volume and com- nutritional adequacy of such milk for young position of breast milk in poorly nourished infants in relation to calories, proteins, vi- communities can only be made in relation tamins, and minerals, and the physiological to other ecological circumstances affecting and practical efficacy of supplementing the both mother and baby (66, 77). However, maternal on infant diets, when or if neces- this paper attempts to draw together the sary. main relevant information from different However, it must be stressed that infant parts of the world, in which widely varying feeding cannot be considered in relation to cultural, genetic, economic, and nutritional the dietary supply of nutrients alone, but circumstances prevail. Differences, when rather in an ecological context. For exam- they exist, may be related mainly to nutri- ple , with regard to breast feeding in less tion, to physical overwork and/or to en- developed countries, the nutritional and vironmental psychosocial stress. Other van- health consequences of the prevention of abbes such as maternal parasitic diseases diarnheab disease , the lactation contracep- and genetic physiological differences may tive phenomenon, and the economic and be more relevant than presently appneci- agnonomic considerations have to be borne ated. Variations in results in different stud- in mind at the same time (77). ies are difficult to interpret, especially those Conversely, for the majority of the world, of minor degree, because of dissimilarities breast feeding cannot only be compared in times and methods of sampling and anal- with adequate feeding with cow’s milk - ysis, in types and levels of maternal under- that is with sufficient formula available and with reasonable home hygiene. From a ‘From the School of Public Health, University of practical point-of-view, it is more usually a California, Los Angeles, California 90024. 492 The American Journal of Clinical Nutrition 31: MARCH 1978, pp. 492-515. Printed in U.S.A.

VOLUME AND COMPOSITION OF HUMAN MILK 493 nutrition, and in degrees of environmental psyshosocial stress. Methods Recent work has reemphasized the possibility of very considerable variations in findings as a result of using different biochemical methods . This is particularly so with regard to protein (91). The actual obtaining of representative samples of ri;u ProcIs.ocin human milk poses unique problems as the normal Alveokts destination is the baby’s stomach and not a test-tube or laboratory container. The ejection of breast milk is mediated by the psychosomatic let-down reflex (Fig. 1). Milk production is proportional to the secretion of FIG . 2 . Prolactin reflex . Sucking stimulation on anterior pituitary hormone , prolactin , resulting from breast generates nerve impulses which pass to the an- nipple stimulation (“prolactin reflex”) (Fig. 2), and to tenor pituitary, which secretes prolactin. This is car- the degree of intra-alveolar tension, related to empty- ried in the bloodstream to the breast , where it acts in ing. Methods used must , therefore , avoid interfering the alveoli causing milk secretion . The prolactin pro- with normal mechanisms as much as possible, but in duced is proportional to the amount of sucking stim- fact, all do so considerably. As Hytten (48) noted, ulus. Downloaded from www.ajcn.org by on August 22, 2009 “the sucking of a baby has, for the mother, psycholog- ical overtones beyond the mere local stimulation of nipple stimulation (and reflex prolactin secretion). the areola and nipple; and the mechanical replacement Important reducers of such stimulation are comple- of this local stimulus cannot hope to be an entirely mentary bottle feeds (allaitement mixte) and the early effective substitute for the baby”. introduction of semisolid foods. Diurnal variations in milk volume and composition Likewise , questions of total ouptut are often based have been noted (50, 104, 105). The invariable and on day-time estimations. In fact, in traditional cultures, considerable difference in fat content between fore- the baby sleeps by the mother’s side and must obtain and hind-milk (1 to 2 g/100 ml) means that the time of considerable quantities as “night feedings” (A . Omo- sampling during a feeding can be significant. lulu, personal communication). In addition, in some areas of the world, seasonal Two methods can be used to try to measure the variation has been noted - for example, lower levels of volume produced - test feeding and expression (48): ascorbic acid in the “hungry season” in parts of Africa (130). Such seasonal changes have long been recog- Test feeding (test weighing) nized by dairy farmers. The stage of lactation is another In this venerable technique, the baby is weighed variable, as is frequency, intensity and duration of before and after each feeding. Difficulties are numerous and obvious. Results depend on the vigor of the infant and the success of the mother-baby interaction. To ensure larger, more measurable samples, it may be considered preferable for mothers to nurse their babies at prescribed intervals rather than on demand - as under nonexperimental conditions at home . Expensive, accurate scales are required to measure relatively small weight increases in an uncooperative infant . There is considerable likelihood of interference with the emo- tionally-sensitive let-down reflex in the unnatural, anx- lldk iety-producing circumstances and embarrassment inev- Alveoko, itably created by the investigation, which often have been carried out in hospitals. Practically, there may be a need for continuous surveillance to ensure that no feeding takes place between weighings, and, as noted earlier, ideally this should be on a 24-hr basis, which is almost never possible. FIG. 1 . Letdown reflex: the key to successful lac- Expression tation. Sucking stimulation on the breast generates nerve impulses that pass to the posterior pituitary Milk may be expressed from the breast manually that secretes oxytocin . This passes via the bloodstream and by some form of mechanical or electrical pump. to the breast, where it acts on the myoepithelial cells, These methods can be used to estimate total output, surrounding the milk-containing alveoli, causing their and, of course, are required if samples are to be contraction. This expresses the milk from the alveoli obtained for analysis. into the lacteals. The sequence is also known as the The same difficulties exist as with test feeding. “milk ejection reflex.” Importantly, it can be inhibited Indeed , anxiety can be greater with expression , espe- by anxiety (Fig. 3) and enhanced by confidence. cially with an unfamiliar, uncomfortable apparatus,

494 JELLIFFE AND JELLIFFE possibly combined with concern over feeding the baby poorly nourished women (4) Recent . stud- later with the expressed milk. Also, the influence of ies in Guatemala have suggested that fat expression on prolactin secretion , compared with suckling by the baby, is unknown. loss may be the main mechanism by which such mothers can continue to lactate (124a). Results Many accounts from different parts of the world suggest that malnourished women Comparative results have varied in differ- often lactate with unexpectedly little clini- ent studies. In some, expression has given cabby obvious deterioration of their nutri- greater volumes; in others, test weighing. tional status. However, in recent years there Sometimes daily outputs have been calcu- may be increasing evidence of shorter pe- bated from the amount obtained at one nods of satisfactory lactation then previ- feeding only. In all cases, it is apparent that ously, at least in some parts of the world. results are only approximations. The effect of maternal malnutrition may be partly hormonal, with decreased secretion Maternal nutrition of cortisol and possibly prolactin (55a) Cer- . Comparisons are also made more difficult tainby the cumulative effects of sequential by variables in the nutritional status of reproductive cycles, including prolonged mothers, both between mothers in a partic- lactation, can bead to general “maternal Downloaded from www.ajcn.org by on August 22, 2009 ubar group and between various communi- depletion,” as shown by progressive weight ties, and by the possibilities of different loss and a prematurely aged appearance degrees of adaptation (53). The nutrients (78 , 1 24a) More specific . nutrient deficien- involved, the degree and duration of depri- cies may occur with repeated reproductive vation, methods of nutritional assessment, cycles for example - , an increasingly large and the previous nutritional situation and goiter, anemia, osteomalacia, or nutritional stores can have many and varying combina- edema (78). tions. There may, for example, be consid- enable difference between the nutritional Environmental psychosocial stress past and present histories in poorer women Under-appreciated in the past has been in Sao Paobo, Brazil, (106a) in Ibadan, Ni- the effect of environmental psychosocial genia (8-12), and in Southern India (37). stress from poverty and unemployment, An aspect of the situation about which from poor housing and crime , from ilbegiti- nothing is known is the effect of the nutri- macy and family instability, and from cub- tional status of the pregnant mothers to- tural confusion and uncertainty on lactation wards the end of gestation on the sensitive, performance, probably manifested through developing mammary glands of the female the effect of anxiety on the bet-down fetus (89). reflex and possibly - on the secretion of More directly, the physiological weight various hormones, such as contisob. This is gain in pregnancy, about one-third due to mainly of concern in urban slums and shanty deposition of subcutaneous fat (“lactation towns. Despite these differences, certain stores”2) ; can vary considerably from the general findings seem to be usual and enable 1 2 .5 kg suggested for Western women to 5 principles to be suggested on which practical kg (or even weight boss) reported in poorly action can be based. These can be consid- fed communities (53) . Dietary inadequacy ered under three headings-volume, com- in pregnancy may sometimes be compli- position, and adequacy of breast milk in cated by associated hard work and by re- poorly nourished communities. stnictive food customs. However, culturally defined customs or physiological adjust- Volume ments may bead to less energy expenditure Well-nourished mothers. To interpret the in pregnancy and lactation. adequacy of yields of breast milk in mothers Likewise, in all communities, lactation itself leads to weight loss. In very ill-fed 2 An estimated average increase in body fat of 4 kg mothers, this can sometimes be as much as (9 Ib) represents an energy store of some 35,000 kcal, 7 kg after a year-even leading to the enough to subsidize lactation by nearly 300 kcal daily development of nutritional edema in very for 3 to 4 months (53).

VOLUME AND COMPOSITION OF HUMAN MILK 495 in communities with defective nutrition, it TABLE 1 is plainly important to compare results with Mean intake of breast milk in Swedish babies (1945). those from well-nourished communities. Volume (mean) Age Unfortunately, such data are scanty, out- Girls Boy’. of-date , and difficult to compare because of inc ml differences in technique and sampling, and 1 576 645 because of recent back of interest in the 2 704 750 whole subject of lactation. 3 733 798 In scientific and international literature, 6 740 817 the figure of 850 mb/day is usually quoted for the volume of milk produced in the first TABLE 2 6 months. However, review of the literature Daily volume of breast milk in Swedish women (1975) of 20 to 25 years ago shows that this was an (91). arbitrary estimate and selected as an easy- Month No. of Breast milk to-remember round number based on an postpartum mothers volume “assumption” in 1950 in the United Nations - ml Committee on Calorie Requirements (34a). 0-’/2 15 558±83 /2- l/2 11 724 ± 117 It has become sanctified by repetition in Downloaded from www.ajcn.org by on August 22, 2009 1’/2-3’/2 12 752 ± 177 subsequent international reports (34b, 3’/2-6’/2 12 756 ± 140 150a) and in the United States, where the first (1953) recommended dietary allowances for babies were based on the assump- the intakes of 26 healthy totally breast fed tion that 850 ml of breast milk would be babies in lllinois, with the following results produced from 1 to 3 months and 1400 (in mb/day) (lila). from 4 to 6 months (139a). Typical daily outputs of mature breast Month Mean Mm. Max. milk in well-nourished women in the first 6 1 606.3 294.5 996.1 months of life can often be less than antici- 2 601.4 322.0 892.4 pated - between 600 to 700 mb/day rather 3 625.5 400.2 899.9 than the 850 mb/day often quoted, according to a recent interpretation by Thomson In Sweden, test weighing by mothers gave and Black (138) of the data collected by daily volumes which were higher, with a Morrison up to 1952 (101). However, much mean of 838 mb/day (134a). variation occurred between the results of Various studies have been undertaken different investigations, depending on the which have sometimes shown minor varia- methods used and the type of subjects. For tions between the volume produced by each example, a Detroit series of studies and breast, and on different days or times of other early investigations contained profes- nursing. Diurnal variation in the amount sional wet-nurses (104, 105), whose “con- secreted has also been noted, often with ditioned” lactation performance can be par- maximal yields in the early morning and ticulanly impressive. lowest yields towards evening. Carefully conducted investigation of 363 Results concerning variation with age or babies of normal Swedish mothers was un- parity of mother have been rightly termed dertaken 30 years ago by Wallgren (145), “confused and inconclusive.” Variation in using test-weighing at home for 2 consecu- volume of milk secreted between individual tive days (Table 1 Recently, ). L#{246}nnerdal et women is recognized as being considerable, al. (91) estimated the yield of 53 mothers although difficulties in making comparisons in the same country by test-weighing (Table are great, including variation in the weight 2) . Despite different detailed techniques and sucking vigor of the baby Breast size . and the intervening time between the stud- does not appear to be related to yield, being ies, the results are quite similar. more an indication of mammary fat. How- Very recent studies show the difficulty in ever, the influence of emotional factors on interpreting variation in results. For exam- milk yield has recently been reendorsed by ple, Picciano determined by test weighing Lindbbad et al. (88b) who found that hospi-

496 JELLIFFE AND JELLIFFE talization of healthy Swedish mothers limits by the mother has no physiological merely to collect samples of milk, blood effect on the volume of milk secreted. This and feces caused a significant drop of 210 seems endocrinobogicalby explicable in light mb/24 hr. of the renal antidiunetic, water-sparing ef- Variation in yield with “later” lactation fect of pnolactin (77). The common belief is difficult to judge in webb-nourished corn- that fluid intake affects milk yield probably rnunities as, until the resurgence of interest operates more through a “sympathetic in breast feeding of recent years, nursing magic” effect on confidence (“fluid in = into the second semester of life or longer fluid out”), and hence on the psychosomatic has not been usual in Western industrialized “let-down reflex.” Conversely, in what has countries. Also, there seems little doubt been termed a “low solute , continuous con- that the main stimulus responsible for the tract species”, such as man, human milk volume of milk produced is the amount of with an approximately 87% water content sucking at the breast, and hence of prolactin is also the young baby’s source of fluid, as secreted. This is shown by “induced bacta- well as nourishment, even in solely breast tion” in some traditional societies and by fed infants, including such a hot climate as recently introduced “adoptive lactation” or Jamaica (la). nelactation in nonbactating American women, Dominating considerations of the “nor- Downloaded from www.ajcn.org by on August 22, 2009 who wish to breast feed their adopted ba- mab range” of milk volume secreted by well- bies. (143a) In both, frequent sucking at the nourished mothers are difficult questions of breast is the main factor in initiating and sampling, very great differences in tech- continuing milk secretion. Likewise, 24% of nique and timing of collection of specimens, a series of twins have been shown to be and individual variation between women solely breast-fed adequately for 3 to 6 and in the same woman , both from day to months (1). Also, the “perpetual,” on at day and as lactation progresses . As a gener- beast very prolonged, high output by tnadi- abization, technique and method of calcuba- tional wet-nurses is in part a reflection of tion often appear to play a major robe in continuing vigorous sucking stimulus by suc- the final figure brought forward. cessive hungry customers. In fact, the vol- Poorly nourished mothers. Estimations of ume of milk secreted has to be viewed the volume of breast milk produced have against the pattern of infant feeding in the also been undertaken in a variety of coun- particular family (or culture) and the con- tries in Asia and Africa, and in New sequent degree of sucking stimulus and its Guinea . The results have been extracted effect on the pnolactin secretion. from published information and these ap- The common concept of the “normal pat- proximations are presented in Table 3 De- . tern” in Western-type cultures is of rise in spite differences in methods of collection, output in the first month or so , followed by sampling, and analysis, and bevels and forms a decline thereafter to a plateau lasting of maternal undernutrition, it seems that approximately until the baby is about 6 the volumes produced were usually some- months old, followed by a slow decline what below those reported from well-noun- thereafter. Consideration of lactation pat- ished countries in Europe and North Amer- terns elsewhere and the previously men- ica. tioned results in twins, in wet-nurses, in Volumes reported varied greatly and induced lactation, and in nelactation, sug- seem to be lowest in communities with poor gest that the Western pattern may not be a levels of nutrition and with inadequate liv- biological inevitable, but rather a response ing conditions, whether urban (Cobombo, to a particular pattern of sucking stimula- Sri Lanka (30)) or rural (New Guinea High- tion. lands (5)) . However, working approxima- Very few studies have been undertaken tions in round figures can be suggested: on dietary effects on the volume of milk between 500 to 700 mb/day in the first 6 produced in well-nourished women. By con- months of life,400 to 600 mb/day in the trast, numerous investigations have shown second 6 months and 300 to 500 mb/day in that variation in water intake between wide the second year. The few studies under-

VOLUME AND COMPOSITION OF HUMAN MILK 497 TABLE 3 Approximate quantities of milk produced daily at different periods of lactation in some poorly nourished communities0 Country 24 months 1-6 months 6-12 months 12-24 months reference and above India(15,16) 600ml SOOml 350ml India (Baroda) (116, 117) 600 (3 mo) . (350-1100) 735 (3 mo) (540-1100) New Guinea (Chimbu) (142) 525 ml 525 ml 343 ml 343-142 ml Biak Island (60) 427 ml 390-430 ml 127-338 ml 243 ml New Guinea (14) 720 ml 660 ml 705 ml 488 ml New Guinea (5) 400 ml 400 ml 400 ml Chimbu and Maprik New Guinea (5) 600 ml 600 ml 600 ml Baiyer River New Guinea (108) 350-480 ml 270-360 ml (12-18 mo) 230-300 ml 200-210 ml (12-24 mo) Ajamaru Nubuai 310-410 ml 250-340 ml (12-18 mo) Downloaded from www.ajcn.org by on August 22, 2009 150-210 ml (18-24 mo) Egypt (45) Healthy 922 ml Malnourished 733 ml Sri Lanka (30) 475 ml 495 ml 506 ml Nigeria (Benin) (81) 555 ml (2-3 mo) 590 ml (6-9 mo) 606 ml (13-18 mo) Uganda (122a) 660 ml (2-12 mo) a Results not strictly comparable as varying collection techniques and methods of sampling used. taken in the third year of lactation show palan showed an increase in volume se- very considerable differences, varying from creted, from 420 to 540 ml in poorly nour- 230 to 488 mb/day. ished Indian women after protein supple- Also, it is well recognized in practice that mentation (from 61 g/day to 90 g/day (36)). the output of extremely malnourished moth- Similar results were obtained in Western ers in families declines and ultimately Nigeria by Bassir using a vegetable protein ceases, with fatal consequences for the nurs- supplement-30 g of soya flour daily (10). ing baby (71). The nutritional point at Another study in India, where inadequately which human lactation becomes seriously nourished mothers were fed with milk bis- inhibited or ceases in famine circumstances cuits, showed a rise in serum albumen par- is not known , but early marasmus (in the abbebed by increase in albumen in the breast first 9 months of life) a solely breast fed milk, presumably by “spill-oven” (26b). babies may be occurring increasingly in the Also , an early investigation in 1 93 1 , showed babies of very poorly nourished women that an increase in output could be achieved living in conditions of severe psychosocial in New Zealand women by increasing the stress - for example , in Karachi , Pakistan calorie and/on the protein intake (27). Re- (89). Sometimes in some countries this may cently, a study in England seemed to sug- be partly “contraceptive manasmus,” from gest that poor lactation could be rebated to further interference with breast milk secre- inadequate energy reserves in the form of - tions by oral estrogen-containing contracep- subcutaneous fat laid down in pregnancy, tive pills. In pants of the world with seasonal and calorie intakes in lactation. In the food shortages (“hungry seasons”), as in United Kingdom, slimming diets in lactating Central Africa, the daily output may drop mothers lead to “an immediate reduction in by 100 to 200 ml (l43a). milk supply” (148). Supplementation. Limited studies have A recent detailed investigation was re- been carried out on the effect of supplemen- ported by Edozien and co-workers from tation of the mother’s diet on output. Go- Nigeria, (31b) when they showed that pro-

498 JELLIFFE AND JELLIFFE tein supplementation of the lactating less than in dairy cows, but it should be mother’s diet increased the milk produced remembered that such farm animals have and weight in the baby, but not the protein been bred to produce much greater yields content of the milk (Table 4). Similarly, than are required by the offspring (138). Sosa et al. (128a) demonstrated a rapid Composition increase in milk production in a malnourished Guatemalan woman following an im- The biochemical composition of human proved diet, particularly calories and pro- milk has been examined in different parts tein. of the world . Approximate comparisons can As usual , those concerned with the pro- be made between various communities, and duction of cow’s milk as a business, the with well-nourished mothers, for protein, dairy farmers, have infinitely more practical fat, lactose, vitamins, and calcium, keeping knowledge than those concerned with hu- in mind previously mentioned difficulties man milk and breast feeding. Thus, Lind- posed by variations with sampling (period blad and colleagues quoted the following in lactation cycle , time of day ; single , re- aphorism from Morrison’s 1948 Handbook peated or 24 hr; seasons; one subject or of Stockmen (101) which may not be com- pooled specimens, etc.), with laboratory techniques and with bevels of difficulties in Downloaded from www.ajcn.org by on August 22, 2009 pleteby correct for the human, but is cer- tainby generally so: maternal nutrition (Table 5) . Interpretation “Any inadequacy in the ration or fault in of such comparisons is made much greaten the methods of care or management will by recent realizations of the physiological generally manifest itself in the yield of milk, variations that occur in well-fed healthy rather than by a change in its chemical women successfully breast feeding their ba- composition” bies. However, the effect of increasing the ma- Protein. The protein content of human ternal diet on human milk output may be milk has been described as varying between 1 .0 to 1 .6 g/100 ml in well-nourished TABLE 4 women. In 1952, Morrison reported the Effect of maternal dietary supplementation with mean of European analyses to be 1 .6 g/l00 protein on the volume and protein content of breast ml and American 1 .2 g/lOO ml (101). He milkand weight gained by baby (Nigeria) 31b.0 suggested that differences in methods of Daily protein intake estimation may be mainly responsible, and Variable’ . 50g lOOg 25g bOg that 1 .2 g/100 ml probably represented an nitially initially overall mean . A study in Britain showed No. of subjects 7 7 3 3 1 .3 g/100 ml (29a). There seems little evi- Totalmilksolids 13.8d 13.4 12.0 11.9 dence for significant diurnal variation or (g/lOOml) ±1.3 ±0.9 ±0.6 ±0.5 fluctuation with age on parity. Milk protein 1 .61 1 .57 1 .20 1.25 (g/lOOml) ±0.15 ±0.19 ±0.21 ±0.23 However, very recent Swedish studies Milklactose 8.1 7.9 7.3 8.0 (1975) have shown the “true protein con- (g/lOOml) ±0.9 ±1.0 ±1.4 ±1.8 tent” to be only 0.8 to 0.9% in apparently Milkproduced 742 872 817 1059 well-nourished women in that country, (g/day) ±16 ±32 ±59 ±63 when determined by amino acid analysis Milkconsumed 617 719 777 996 (g/day) ±15 ±10 ±38 ±74 (91). These investigators pointed out that Weightgainedby 30.4 45#{149}7e 10.5 32.2e earlier analyses of breast milk were made baby(g/day) ±3.6 ±2.0 ±3.6 ±10.1 with the same methods as used for cow’s 0 Subjects were fed the initial diets for the first 14 milk. In fact, it is now recognized that the days and then a diet providing 100 g protein per day relatively low protein, low solute character- for the next 14 days. Results for each subject represent istics of breast milk place the human as a the mean values for milk samples collected during continuous contact, frequent suckling spe- days 8 to 14 (for initial diet) and days 21 to 28 (for diet providing 100 g protein per day). b Duration cies in infancy, with rather slow growth, of lactation for all subjects was between 30 and 90 and also permits breast milk to be the only days. C Duration of lactation was over 100 supply of water as well as nutrients. days. ii Results are mean values + SD. e Signifi- Retrospective examination of analyses cantly different at the 0.05 level from the unsupplemented subjects. undertaken with similar methods in Brus-

VOLUME AND COMPOSITION OF HUMAN MILK 499 TABLE 5 Fat, lactose, protein, and calcium content of mature human milk from some well-nourished and poorly nourished communities” Country (reference) Fat Lactose Protein Calcium g/IOO ml mgIlOO ml Well-Nourished American(92) 4.5 6.8 1.1 34.0 British(87) 4.78 6.95 1.16 29.9 Australian (150) 28.6-30.7 British (29a) 4.2 7.4 1.3 Poorly-Nourished Indian(17) 3.42 7.51 1.06 34.2 BantuS.Africa(144) 3.90 7.10 1.35 28.7 Chimbu, New Guinea Highlands (142) 2.36 7.34 1.01 New Hebrides (111) 3.8 5.0 1.40 25.8 Wuppertal, Germany 3.59 1.20 (Immediately Post World War II) (42) Nauru(19) 1.60 Ibadan, Nigeria (88 months) (62) 1 .20 (0.59-1.79) New Guinea (Biak) (60) 0.83-0.9 Downloaded from www.ajcn.org by on August 22, 2009 Alexandria, Egypt (45) Healthy 4.43 6.65 1.09 Malnourished 4.01 6.48 0.93 New Guinea (14) 2.3 6.48 0.93 Sri Lanka (30) 2.8 6.8 1.5 Brazil (21) Higheconomic 3.9 6.8 1.3 20.8 Loweconomic 4.2 6.5 1.3 25.7 Pakistan (139) 1.2 Tanzania (25) Often below 2% Nigeria(Ibadan)(102) 4.05 7.67 1.22 a Modified from Gopalan and Belavady (37), with added data. sels, Belgium (129) in 1954 and in Tokyo, although the lysine and methionine levels Japan (1 23) shows similar “low” levels for were lower. “true protein content” as with recent Swed- Varying results have been obtained with ish figures. estimations of the protein content with what In poorer, technically developing coun- is termed by modern Western cultural defi- tries, the average protein content of the nition “prolonged lactation” that is into - milk of inadequately nourished mothers, the second year of life and later. Some have based on previously used methods of total found a decline, some a rise, and others no nitrogen assessment, is usually surprisingly material change. high-in fact, a low normal (1 .0 to 1 .1 g/ The effect of maternal dietary suppbemen- 100 ml), although the range may be quite tation on protein content does not appear wide (Table 5). to have been investigated adequately. How- In some places with probably poorer flu- ever, in the protein supplementation study trition, analyses with older methods have carried out by Gopaban, the increased out- sometimes shown the protein content to be put of milk was associated with a come- lower (0.8 to 0.9%). However, in a care- sponding fall in protein concentration, with fully carried out study of poorly nourished the result that the total protein output in 24 women in Karachi, Pakistan, the “true pro- hr was not significantly altered (36, 37). tein content,” determined by an exchange Also, modern laboratory methods such as chromatography after acid hydrolysis and immunoelectrophoresis, which enables ac- adding up the calculated amino acid resi- curate quantities and measurement of the dues, was 0.8 ± 0.1 g/100 ml (89). These individual proteins of milk to be made were results are similar to those obtained by like not available at the time of earlier studies. techniques in Sweden, Belgium, and Japan, Recent investigations by L#{246}nnendal et al.

500 JELLIFFE AND JELLIFFE (91) have shown many unexplained vania- breast milk (or cow’s milk based formula) tions in healthy, well-fed women-for ex- appears to be reflected in the fatty acids in ample, in “milk-specific proteins,” those the infant’s subcutaneous fat. synthesized by the mammary gland, no- The relevance of the fatty acid (and cho- tabby ct-lactalbumin and lactoferrin . The lestenol) contents of human milk is currently decrease in total nitrogen in the first period under consideration in relation to the deveb- of lactation, for example in the first month, opment of the central nervous system and was mainly due to a dramatic drop in secre- atheroma in adults in industrialized coun- tory IgA bevel. tries. In developing regions, the pobyenoic Fat (lipid) . The significance of the fat con- fatty acids may be diminished in the breast tent of milk has been under-emphasized. It milk of malnourished mothers, with possible is the main source of calories; it contains ill-consequences in relation to brain growth fat soluble vitamins, especially vitamin A; (25). it is also the source of essential fatty acids Lactose. The third “proximate principle,” needed for the growth and development of lactose, is generally recognized as being the central nervous system (24b). Lastly, most constant in concentration and shows the higher fat in the after-milk may act as a no diurnal variation. Morrison’s (101) fig- physicochemical appetite control for the une based on 1010 samples examined in Downloaded from www.ajcn.org by on August 22, 2009 suckling baby (44). various American and European studies Earlier estimations of the fat content of showed a mean of 7.2 g/100 ml, while Kon milk in webb-nourished communities in the and Mawson found 6.9 g/100 ml in 586 United States and Britain showed means of samples of mature milk (87). In poorly 4.5 (93) and 4.78 g/100 ml (87), respec- nourished mothers, lactose also does not lively. A more recent 1977 study showed a seem to vary very much (Table 5) (range mean of 4.2 g/100 ml (29a). 6.43 to 7.51 g/l00 ml), except in one study Results from poorly fed women in devel- in the New Hebrides where 5.0 g/100 ml oping countries have demonstrated consid- was reported (111). enable variation (Table 5). However, some Calories. The calorie intake from breast recent work has suggested that the fat may milk is a product of the volume (as taken sometimes be considerably reduced, even by the baby) and its caloric content, which down to 1 g/100 ml (24b). Under these is primarily derived from fat. In well-fed circumstances , the calorie content of the communities, the caloric content varies milk may be much decreased with signifi- greatly. Macy and Kelly (92) give a mean cant lessening of energy intake (24a). The figure of 75 kcab/100 ml (range 45 to 119). significance of a bower fat content has to be The recent United Kingdom report showed related to inadequate energy intake in pneg- a mean of 70 kcab/100 ml (29a). nancy, with an inadequate subcutaneous In poorly nourished communities, both “fat bank” (53), as well as to the diet in the volume secreted and the fat, the main lactation itself. calorie-containing constituent, (and other The fatty acid pattern of breast milk can nutrients) may be less than in well-fed moth- be altered to some extent without affecting ens. milk volume or milk fat output by variation Vitamins in the types of dietary fat (especially if these are extreme) (25a) on by changes in the Vitamin A . The concentration is influ- calorie intake (57, 147). During energy enced by the adequacy of the diet of the equilibrium, milk fat resembles the fatty mother in pregnancy and lactation. The acid pattern of dietary fat, but when inade- vitamin A content of breast milk is often quate calories are eaten, the fat in human much lower in poorer populations of some milk follows the composition of human sub- developing countries (India , Ceylon , Indo- cutaneous depot fat. The major factor influ- nesia, Jordan), where this nutrient is mar- encing the fatty acid composition of milk is ginal, than in Europe and North America. the carbohydrate supply in the diet. Ulti- Maternal serum bevels are also low. The mately, the fatty acid composition of the intake is generally higher in the spring and

VOLUME AND COMPOSITiON OF HUMAN MILK 501 summer months due to greaten supplies of Niacin. Although human milk is bow in dark green leafy and yellow vegetables. actual niacin, it has a high potential niacin Particularly high levels of netinob (vitamin value because this vitamin may be synthe- A) have been noted in Western Nigeria, sized from the amino acid, tryptophan. presumably because of the widespread use Vitamin B12. Low bevels of vitamin B12 of palm oil in cooking (102). have been found in the milk of poorer In a recent comparative investigation , the vegetarian women in Bombay. Also, in var- vitamin A content of breast milk was signifi- ious parts of India the “syndrome of cantly higher in normal Swedish mothers tremors” have been described in solely than in nonpnivileged Ethiopian mothers, breast fed babies, and has been ascribed to whose milk showed greater concentrations deficient B12 in the mother’s milk (59). of f3-carotene (35). Vitamin C. The level of ascorbic acid in Kcn and Mawson (87) found that supple- breast milk is subject to variations in dietary mentation with vitamin A, before and after intake in developing countries, particularly partunition or later during lactation, bed to with the seasonal availability of fresh fruits the secretion of milk richer in vitamin A and vegetables. In webb-nourished mothers, than normally produced. In Central Amer- human milk contains an average of 4 mg/ ica, Arroyave et al. (3) observed a rise in 100 ml of vitamin C. In Botswana (formerly Downloaded from www.ajcn.org by on August 22, 2009 the breast milk vitamin A levels after the Bechuanaband), Squires (130) found the introduction of vitamin A fortified sugar. content to be 1 .7 mg/100 ml in the dry Vitamin D. As well-known, levels of fat- season and 2.7 mg/100 ml in the wet sea- soluble vitamin D are low in both human sons. The subjects were poorly nourished and bovine milks. However, the recent dis- Tswana women. covery that breast milk contains a water- Since the ascorbic acid contant of breast soluble conjugate of vitamin D with sub- milk is greater than that of blood plasma, phate (87a) producing the same anti-nachitic which is generally below 2.5 mg/100 ml, potential as milk formulas fortified with secretory activity in the mammary glands conventional vitamin D explains the clini- must play a part in determining the bevel of cally well-recognized rarity of rickets in the vitamin C in milk. Apparent adaptation to breast fed. low maternal intakes of vitamin C has been Thiamine. The thiamine content of breast noted in Banoda, India (117) and the Phil- milk in areas with a high incidence of infan- ippines (132). The possibility of placental tile beriberi has been found to be low, due synthesis in pregnancy has been suggested. to insufficient maternal stores and intake in Certainly both the placenta and the breasts communities with diets largely based on may be abbe to actively secrete ascorbic polished rice (66) . Under these circum- acid for the offspring. Levels of fobic acid stances, a specific form of malnutrition - and vitamin B6 seem to reflect maternal infantile beriberi - occurs exclusively in nor- nutritional status (106a, 85). mab-seeming breast fed babies, and is due to a thiamine-deficient diet in the mother Vitamin supplementation during pregnancy and lactation . It is so characteristic in time of onset that the 2 to Deodhar and Ramakrishnan (28) carried 5 month mortality has been suggested as an out a dietary survey among women in South age-specific rate for this condition in the India with special reference to pantothenic regions at risk. acid, riboflavin, nicotinic acid, ascorbic acid Riboflavin. Human milk is a good source and thiamin. Subsequently, the breast milk of riboflavin, provided the maternal diet is was analyzed for the concentrations of the adequate. However, in South India, Gopa- same vitamins. A positive and significant ban and Belavady (37) found an average of correlation was found between dietary in- only 17.2 pg/100 ml of riboflavin in breast take and vitamin content of the milk for the milk, as compared with a value of about 25 vitamins investigated, which underlines the g/100 ml found by Kon and Mawson in need for an adequate diet for the lactating Britain (87). women. The content of all the vitamins

502 JELLIFFE AND JELLIFFE increased steadily with the dose of supple- In this regard, it is often insufficiently mentation. appreciated that the RDA’s given for in- In a more recent investigation, supple- fants are themselves derived from estimated mentation with ascorbic acid, nicotinic acid, intakes of breast fed babies, with an addi- riboflavin, thiamin, pantothenic acid, cyan- tional safety factor added for the less certain ocobalamin, biotin, pyridoxine, and folic situation of infants fed on cow’s milk for- acid was undertaken. As a result, the vi- mulas (70). This is the case, for example, tamin content of the milk increased steadily with the very high RDA of iron (1 0 mg/ with the dose used in supplementation (29). day) for the first 6 months of life , which Calcium . Levels of calcium reported in can not be attained with human milk. the milk of webb-fed mothers vary consider- The derivation of RDA’s for infants are ably. The calcium content in poorly nour- often not understood by pediatricians or ished mothers has been reported to range nutritionists, so that the advertising of corn- from “normal” levels to somewhat bow con- mercial baby foods can issue the following centrations (Table 5). Again, differences in appeal to “logic”: sampling and technique may be in part responsible. “A stimulating exercise for professionals would Levels of other minerals will not be con- be sorting one’s beliefs about breast feeding into Downloaded from www.ajcn.org by on August 22, 2009 those based on scientific fact and those stemming sidered here, but are presented elsewhere from hearsay and emotion. One could thus more (77). Early analyses are given by Morrison objectively counsel that growing membership in and others (101). The question of the con- lay organizations dedicated to breast feeding. tent of trace minerals will be much under Many sincerely believe that breast milk is all sufficient without any supplementation for at least investigation in coming years, in relation six months if not the full duration of breast feed- both to nutritional need and to possible ing. The fallacy of this concept is obvious if one effects of environmental pollution. compares the nutrient content of breast milk with recommended RDA for infants.” Adequacy The nutritional adequacy of breast milk The inanity of this comment is apparent for the infant can be roughly assessed by especially in view of the biological adapta- measuring 24-hr output and chemical corn- tion that has occurred over hundreds of position , or by the recording of satisfactory mibbenia. Carried to extremes, this argument growth, “good health” and absence of clini- would mean that breast milk was unfit for cab malnutrition. consumption by human babies, without ad- Adequacy of nutrients. The “nutrient ditional iron and vitamins. needs” of the baby during the exterogestate The RDA’s of protein and calories sug- fetal stage are not derived only from the gested for infants have been derived from diet, but also from fetal stores acquired in breast milk estimations, feeding with cow’s utero, from the placental transfusion (iron) milk based formulas and from the impon- and, to a limited and variable extent from tant, but special, studies by Fomon and ultraviolet irradiation of the skin (vitamin May (1958) on babies bottle fed ad bibiturn D). The recommended daily dietary allow- with pasteurized breast milk (33). Based on ances (RDA) for babies are estimated their findings, it has been suggested that mainly “by analogy with breast fed infants,” infants need: 1 st month 836 mb/day - (pro- and yet it is agreed increasingly that pres- tein 2.6 g/kg; cab 143kg); 6th month-990 entby available data on the composition of ml/day (protein 1 .7 g/kg; cal 90k). human milk is incomplete and out-of-date. However, as noted earlier, outputs in Fomon (34) rightly notes the need for more well-nourished women actually nursing their modern studies, and remarks that “until babies often supply less than this, a common such data are available, many of our calcu- range being 600-700 mb/day for the first 6 lations rebating to nutrients in human milk months (138). Among poorly nourished will be likely to be misleading”. Recent tropical communities estimated volumes Swedish studies (91) on the protein content often seem to range from 500-700 mb/day of breast milk give urgency to this comment. during the first six months (Table 4).

VOLUME AND COMPOSITION OF HUMAN MILK 503 As noted earlier, many of the constituents protein recommended, are probably high. of breast milk can be affected by inadequate As noted earlier, the reported consumption maternal nutrition, depending upon its Se- of milk in direct breast feeding studies are verity, length and the mother’s previous often lower with apparently well-nourished nutritional status. Water soluble vitamins babies. are particularly influenced, including ascor- Also, the difficulties with understanding bic acid and riboflavin. Likewise, levels of the nutritional and biochemical meaning of vitamin A and the pattern of fatty acids results obtained by analyses of single sam- reflect maternal diet and stores. The fat ples are increased by recent increased may be reduced in some malnourished awareness of the physiological variation in countries. The protein content of human human milk composition and by the need milk in poorly nourished women is usually to recognize breast milk as a biological within “normal” limits (1 .0 to 1 .1 g/100 system with interacting nutrients, which ml) or sometimes below this (0.7 to 0.9 g/ modify each other’s absorption and utibiza- 100 ml) (Table 5). tion, rather than as a solution of indepen- By comparison with estimates of volume dent chemicals. Recent work on the supe- and composition in well-fed mothers, infor- nor absorption of zinc from human milk mation derived from poorly nourished may be noted in this respect (31a). In other Downloaded from www.ajcn.org by on August 22, 2009 women suggests that their babies may some- words, the nutrients and their physiological times receive lesser intakes of nutrients. effects in the human baby vary greatly in However, five factors need to be taken into the breast fed and the bottle fed. account before making too sweeping conclu- Physiological variations in the constitu- sions: ents of milk from webb-nourished healthy First, the figures on volume gained in mothers with babies who are being success- general studies are often those obtained by fully breast fed can be between individuals expression or following test-feeding with the and/or in the same individual at different errors implicit, and often having a risk of times. Similar differences are to be found underestimations because of interference with other aspects of body physiology - for with the psychosomatic “bet-down reflex” example , serum biochemistry. and inadequate stimulation of prolactin pro- Genetic variations in the composition of duction. cow’s milk have been recognized for dec- Second, such investigations are usually ades-fon example, the high fat content of based on daytime output, when in most Jerseys. Also, in the last 10 years on so, traditional cultures, babies sleep by the genetic variations in the milk of different mothers side with frequent night feedings breeds of cattle has been demonstrated in the normol practice. their “milk protein systems,” notably in the Third, there is a possibility of lower cab- forms of a SI casein and the /3-lactogbobulin ne intakes being needed by infants in truly (120). Despite the very barge amount of tropical areas. new scientific information that has become Fourth, smaller babies have a lesser need available recently, these authorities main- of nutrients, but also may have less sucking tam that “we have barely scratched the potential. surface of the complex behavior and prop- Fifth, the data on which the RDA are erties of the (cow’s) milk system” and other based are inadequate and approximate for “fundamentals of dairy chemistry.” There infants. The babies in the Fomon and May are even fewer analyses of the detailed investigation (33) were receiving pasteur- structure of the protein systems in human ized breast milk from a feeding bottle, with milk (120). No information seems to be an easier rate of flow and without the pos- available concerning possible genetic differ- sibly appetite-controlling function of high ence in milk composition on lactationab abil- fat found in the hind-milk (44), and other ity in varying ethnic groups. “powerful self-regulatory controls within The level of some nutrients varies with the infant” (110). In other words, the intake breast feeding itself on possibly in relation of milk noted, and hence of calories and to the stage of maternal digestion. The fat

504 JELLIFFE AND JELLIFFE content increases with an uninhibited bet- Also, it is possible that stimuli from the down reflex (with a possible appetite-con- nursing baby may affect the milk composi- trolling significance (44), and the prolactin tion, by as yet unappreciated mechanisms, produced as a result of sucking appear to such as alteration in the details of suckling have a controlling effect on mammary fat or even the weight of the baby. These synthesis (44). Periprandiab variation in suggestions are speculative and seem fanci- constituents secreted may also occur. Blood ful. However, the ability of the female kan- bevels of sugar, fat, amino acids, and other garoo simultaneously to secrete milks of nutrients will rise at different times after quite different compositions from two nip- the mother’s meals according to their speed ples in response to differing stimulation of of digestion and absorption, and this may the young of varying stages of development make supplies to the breast’s secretory cells may be noted (77). fluctuate also. The physiological variation in composi- Cyclical chronobiobogicab changes are tion of human milk is unsurprising. Genetic continually occurring in all living organisms, variations and cyclical changes occur in the from plankton to flowers to vertebrates. In milks of other mammals, and, as men- man , well-recognized cycles include those tioned, in other body fluids in man. The Downloaded from www.ajcn.org by on August 22, 2009 that occur each 24 hr (circadian rythms), expectation that breast milk will be stan- each month (notably menstruation) and dandized entity reflects a common fallacy each lifetime, as manifest by aging. Circa- based on “medical education, thought and dian changes in humans involved many as- practice , for the past 1 00 years (which has pects of body physiology, including for ex- placed emphasis on the constancy of physi- ample, the secretion of steroids, body tem- ological systems, (and) inter alia that con- peratune , the rate of cell division and levels stancy is a characteristic of life .“ Rather of brain electrical activity. the normal healthy human being is an “os- Some chronobiobogical variations in the cillating system” that is fluctuating chrono- constituents of breast milk are well-known, biologically (127). particularly the diurnal fluctuation in fat In the solely breast fed infants of webb content (50). It also seems that, as with nourished mothers with established lacta- pregnancy, lactation can be considered as a tion and unimpaired let-down reflexes, “free-running biological cycle ,“ although growth is excellent in the first 4 to 6 months open-ended and without a clean-cut end- of life and nutritional deficiency is virtually point. During this cycle, marked changes in nonexistent, despite variation in milk corn- composition of human milk occur between position between individuals and in any one the cobostrurn , with its high protein (protec- individual. Breast feeding does not consist tive immunogbobulins, etc., high zinc and of ingesting milk obtained at a single time, pattern of fatty acids, and subsequent ma- but over a continuing period of time . Hu- tune milk. Later, chnonobiobogical changes man milk can, therefore, be considered as in the lactation cycle are unclean and need physiologically variable in composition , me- investigation. sponding to various factors suggested earlier Lastly, the needs of individuals for all and doubtless to others, but uniformly nutrients varies, and this is certainly the adapted to supply the nutrients required for case for infants. This individuality can be the infant, both as an individual and at the partly taken cane of by the “demand and particular stage of growth and development. supply” nature of the volume of milk pro- Finally, the question of possible disadvan- duced in breast feeding, with greaten suck- tages of rigidly constant formula composi- ing stimulus beading to greaten secretion. In tion needs consideration. Such is the case addition, the composition may vary with with regard to absence of a cobostrum-sur- the individual need of the baby, possibly on rogate, but whether inability to match the a genetic basis or as a result of feedback flexible variability of breast milk is signifi- mechanisms acquired transplacentally by cant on not will only become more apparent the mother while the fetus was in utero. when more detailed investigations are un-

VOLUME AND COMPOSITION OF HUMAN MILK 505 dertaken into the mechanisms and purpose milk (and the prolactin-mediated “supply of physiological chronobiological changes in and demand” nature of breast feeding) is human milk. indicated by a recent investigation of 173 One conclusion seems inescapable - that pains of twins in Southern California (1). is that the present RDA for young babies 23 .7% pains were breast fed, and, of these, in the “exteno-gestate fetal” stage are in 59.5% received no food other than human urgent need of reconsideration . In view of milk for three months or more, and 21.9% the unique biochemical components of hu- for 6 months on more (1). Growth is being man milk (and their interactions), the investigated in detail, but in general seemed dyadic nature of nutrition in early infancy comparable to those bottle fed. and the difficulties of obtaining valid breast With the babies of poorly nourished milk samples, it would appear that these mothers in resource-poor, technically deveb- revisions will pose considerable , perhaps oping countries, difficulties in interpreting insuperable, difficulties in practice. growth curves exist in relation to the preva- Adequacy by growth. It is apparent that bence and significance of low birth weights the ultimate test of the adequacy of human in the particular community, in the selection milk output in breast feeding is not reflected of reference standards thought to be the Downloaded from www.ajcn.org by on August 22, 2009 by estimates of volume produced or by the most appropriate genetically for the partic- composition, but rather by assessment of ular group, the significance of infections physical growth, metabolic equilibrium, and (including diarrhea with fluid loss) and the “good health and nutrition.” From an im- usual problem of sorting out weight gain in mediate and rough point-of-view, adequate relation to increases in fat, muscle on water- growth is normally assessed anthropornetni- electrolyte retention. cabby, usually judged approximately by serial Earlier evidence from various pants of weight gain, and by the absence of necogniz- Africa and India in the 1950’s indicated able nutritional deficiency, as the main prac- that breast feeding, with little or no supple- tical yardsticks. Laboratory tests for specific mentation, resulted in excellent growth for nutrients may rarely be possible , but in any about the first 5 to 6 months of life (36, 66, case, are often difficult to evaluate. Clinical 146). impressions concerning “good health,” However, as a generalization, more me- vigor and well-being are helpful, but impos- cent studies from such varied, but poorly sible to measure objectively. Indeed, even nourished, parts of the world as New the weight “standards of reference” used in Guinea (5), Ethiopia (32), and Tanzania the assessment of growth may be inappro- ( 1 1 3), often show comparable weight curves priate in that they were collected in the to those of Western standards of reference United States and Europe in mainly bottle- only up to about 4 months of age. However, fed babies. Biologically, standards are in some studies growth has continued to be needed derived from breast-fed infants. similar up to 5 months of age as in Malaysia There is sufficient evidence from widely (31), while in other investigations in Jordan scattered areas, including such diverse (84), in northeastern Tanzania (1 13), and sources as the United States (58), and the in Mexico (23 , 94) the weight gain in some People’s Republic of China (125), that babies was reported to have become made- solely breast fed infants do well and show quate after only 3 months. It seems possi- satisfactory gains in weight during the first ble , then , that decreasing lengths of satisfac- 6 months on so of life when the lactating tory lactation are becoming evident in mothers are well nourished. From about 6 poorer communities in some less developed months, flattening of the weight curve usu- countries, perhaps especially in slum areas. ally indicates that the intake of calories and An additional problem is related to the protein are no longer adequate - in other effect of oral contraceptives on reducing words, that the baby has outgrown the milk secretion (especially with the earlier breast as a sole source of food. higher dose of estrogens, and on the com- The adequacy of unsupplemented human position. The possible range of significance

506 JELLIFFE AND JELLIFFE of the latter is emphasized by recent reviews pling methods and analytic techniques. which reveal the complexity of oral contra- These would include preferably more than ceptive interactions with vitamin metabo- one 24 hr sample, and include investigations lism in general and difficulties in their inter- covering the volume and major nutrients as pretation (22, 73, 88). well as more recently recognized biochemi- cab components and physio-chemical ele- Conclusions ments (such as the forms of casein present) in different communities with various levels The investigations summarized in the of maternal oven- and under-nutrition, in- present account of knowledge concerning cluding women using oral contraceptives. the quantity and quality of human milk in These should also include longitudinal sam- both well and poorly nourished communi- ples to investigate the dimensions (and pun- ties in different ecological circumstances are pose) of physiological variation. very far from satisfactory . Understandably, studies have, on the whole, been piecemeal Generalizations with different emphases and techniques used in various investigations. Nevertheless, present-day incomplete Although not usually appreciated, until knowledge appears to warrant the following Downloaded from www.ajcn.org by on August 22, 2009 the 1975 studies in Sweden (89, 91), New generalizations for practical action: Zealand (100), and the 1977 report from 1 ) Unsupplemented human milk is all the United Kingdom (29a), the most recent that is required to sustain growth and good investigations in well-nourished communi- nutrition for the first six months of life in ties were made about a quarter of a century the babies of well-nourished mothers, who ago. have, therefore, produced fetuses with op- Likewise , the technical difficulties of ob- timal stores, who have themselves laid down taming representative samples, especially adequate nutritional reserves, including on a 24 hr basis, can be almost insuperable, subcutaneous fat, in pregnancy, and who especially in the field. Also the degrees of are well-fed during lactation (69). severity, chronicity and specificity of mater- 2) The volume and composition of human nab malnutrition (and of maternal depletion milk in poorly nourished women is sumpnis- from numerous previous reproductive cy- ingly good, possibly due to some metabolic des) are rarely indicated, and indeed, with adaptations, but probably usually to their many of these variables are difficult to cate- cumulative nutritional detriment (“maternal gomize. Lastly, the questions of genetic dif- depletion”). However, it is often subopti- fenences in lactation ability in different hu- mal in quantity and in quality with lower man groups has never been explored ade- values of fat (calories), water soluble vita- quately (138) and would be difficult to mins, vitamin A, and somewhat lower cab- undertake, because of variation in diet and cium and protein, than in webb-nourished forms of environmental psychosocial stress. women. At another level altogether is the fact 3) Limited studies with supplementary that most research undertaken has been feeding of poorly nourished lactating concerned with gross analyses of occasional women (and common sense probability) samples, with no recognition of the degree have suggested improvement in volume of of variation seen normally of the more output and in nutritional quality of breast newly recognized considerations mentioned milk to be feasible. elsewhere, such as the pattern of amino 4) The adequacy of breast milk as the acids, the different protein components, po- sole food for the baby is related to the lyenoic fatty acids, pobyamines, and nucbeo- mother’s diet in pregnancy; to maternal tides, and the presence of anti-infective sub- puempenal calorie reserves in the form of stances. subcutaneous fat; to fetal stores, mainly There is, in fact, a need for coordinated hepatic; to birth weight; and to the iron comparative modern studies into all aspects obtained from the placental transfusion. of human lactation in webb-fed and in poorly 5) Breast milk produced in so-called “late nourished communities, using similar sam- lactation” (e.g., 7 months to 2 years or

VOLUME AND COMPOSITION OF HUMAN MILK 507 more) is insufficient by itself for the rising TABLE 6 nutrient needs (and declining stones) of the Puerperal practices in orthodox Western maternity ward, which interfere with lactation, via the prolactin rapidly growing infant, and forms a decreas- and let-down reflexes. In other cultural circumstances, ing, but, valuable supplementary source of an analysis for practices facilitating or interfering with “complete” protein, and of fat, calcium and these lactation reflexes needs to be undertaken (77). vitamins.3 Practice Effect Delaying first breast feed Practical approaches Sedated newborn (excess maternal anesthesia) If growth, as evidenced by the weight Supplying prelacteal and comple- curve, becomes inadequate in solely breast mentary feeds fed babies at 4 months or earlier in poor Regularly, limited feeds (4 hr) Limitation of communities in less developed countries, it (with no night feeds) sucking and prolactin se- is necessary to consider why this “failure to cretion thrive” should be the case. Maternal nutri- Separation of mother and infant tion is often considered as though it was (“nurseries”) occurring in isolation, with the mother as a Automatic free supply of formula and infant food industry litera- tempemamentless, disease-free “breast ma- Downloaded from www.ajcn.org by on August 22, 2009 ture chine” (88b). As Lindblad et al. (88b) Uninformed, confused mother noted: Tired mother (no food or drink) “The most important variable behind lac- Routine episiotomy (pain) tation failure in poor women, namely milk Weighing before and after (test feeds) volume, does not seem to be primarily de- Restricting visitors Anxiety and in- pendent on food intake, but the combined terference with stress of maternal disease , undernutrition let-down re- and the increasingly difficult living condi- Unsympathetic health staff (“an- tions in rapidly developing city slum areas” tidoula effect”) Automatic free supply of formula It follows, therefore, that diagnosis of an and infant food industry litera- individual in a community in relation to ture lactation failure must be concerned with factors considered to be responsible in some baby in the maternity unit on the taboo on measure, including maternal infections and breast feeding in public), and/on create un- environmental psychosocial stress. Never- certainty and anxiety and thus inhibit the theless, the two main forms of interference bet-down reflex (Fig. 3). Conversely, minor with lactation performance appear to be changes in regimen can be introduced with- through’ the maternal reflexes and through out cost and make the initiation of lactation hem nutrition, so that the relative significance of these two requires consideration in easier (Table 7). There is little doubt that disturbed reflex any individual woman on community. behavior is often more important in the Interference with reflexes causation of lactation failure than maternal subnutmition, unless severe. In devising an Present-day infant feeding practices in the appropriate program to improve breast particular area should be scrutinized to feeding, both aspects need consideration. identify possible practices which may be Conversely, failure to gain weight in the affecting the two main maternal reflexes breast fed extemo-gestate fetus needs inves- responsible for the production and ejection tigation into the effects of the techniques of milk -the prolactin and the bet-down employed on lactation reflexes. reflexes (76a). Various customs may be found in the traditional culture on, more often, in im- 3 Rohde in Indonesia comments that, in domestic ported Westernized practices in maternity terms, the output in the second year means that the child is receiving at least one 8 oz glass of milk daily, units (Table 6) which reduce sucking stimu- with 3 to 5 g of protein (supplementary to the usual bus and, hence, diminish the pnolactin secre- vegetable protein weaning diet), essential fatty acids tion (such as the separation of mother and and 200 to 500 IU ofvitamin A (121).

508 JELLIFFE AND JELLIFFE Inadequate maternal nutrition proach (allaitement mixte) usually needs to If the infant is judged to be receiving be avoided. It introduces the danger of breast milk, which is insufficient in volume weanbing diarrhea at an early and vulnerable and/or composition because of poor mater- age It decreases . the secretion of breast nal nutrition, three approaches need to be milk, as it interferes with sucking stimula- considered: tion and proportional secretion of pituitary Cow’s milk supplementation. A “logical” prolactin. It interferes with lactation amen- possible solution may seem to be the intro- orrhea. It is an additional endorsement by duction of bottle feeds with cow’s milk the pediatric nutritionist of the unfortunate based formulas from just prior to the usual and unaffordable trend away from breast age of flattening of the weight curve. feeding. Lastly, if viewed on a family or on In the circumstances of most resource- a large-scale community basis, it has eco- poor, less developed countries, this ap- nomic, agmonomic and food production consequences of very considerable dimensions. Early introduction of semisolids. Again, under majority circumstances in the world, the risks of weanbing diarrhea are great if unavoidably unclean semisolid foods are Downloaded from www.ajcn.org by on August 22, 2009 introduced. Also, in average kitchen cm- cumstances in tropical countries and with the foods most often available, it is usually very difficult to prepare digestible, well-tol- emated and nutritionally adequate supple- mentany semisolid foods for an infant in the first semester of life. However, the introduction of semisobids by cup on by spoon would have less effect on the prolactin reflex FIG. 3. The anxiety-nursing failure s)ndrome. Anx- and hence on lactation performance than iety, uncertainty or lack of interest can inhibit the let- cow’s milk by bottle and can be based on down reflex, often leading to failure of lactation. the use of mixtures of locally available TABLE 7 Possible modifications in health services designed to promote breastfeeding in a community (77). (1978.) Health service Modifications Prenatal care Information on breastfeeding (preferably from breastfeeding mothers). Breast preparation. Maternal diet. Emotional preparation for labor. Puerperal care Avoid maternal fatigue/anxiety/pain (e.g. , allow to eat in early labor; avoid unnecessary episiotomy; relatives and visitors allowed; privacy and relaxed atmosphere; organization of day with breastfeeding in mind). Stimulate lactation (e.g., no prelacteal feeds; first breast feeding as soon as possible; avoid unnecessary maternal anesthesia; permissive schedule; rooming in). Lactation “consultants” (advisers-preferably women who have breast fed); adequate “lying-in-period.” In hot weather, extra water to baby by dropper or spoon. Premature unit Use of expressed breast milk (preferably fresh). Contact between mother and baby with earliest return to direct breastfeeding. Children’s wards Accommodation in hospital (or nearby) for mothers of breast fed babies. Home visiting Encourage, motivate, support. Health center Supplementary food distribution (e.g., formula and wearning foods) according to defined, locally relevant policy. General Supportive atmosphere from all staff. Avoid promotion of unwanted commercial infant foods (e.g. , samples, posters, calendars, brochures, etc.). Adopt minimal bottle feeding policy and practical health education concerning “biological breastfeeding.”

VOLUME AND COMPOSITION OF HUMAN MILK 509 foods, nutritionally blended as “multi- tion of breast milk, to avoid the economic, mixes,” particularly based on cereal-legume infective and distributive complexities of blends (79). introducing cow’s milk and bottle feeding Supplementation of maternal diet.4 Cur- unnecessarily, and also to avoid assisting rent knowledge suggests that the most eco- still further a decline in breast feeding on a nomical, safe , physiological, and practicable community basis. method of approaching the situation is by In addition, and at risk of oven-repetition, laying maximum emphasis on feeding the it must be emphasized again that those mother during both pregnancy and lacta- concerned with infant feeding often do not tion . Some nutrient stones may be neplen- give adequate appreciation to the associated ished rapidly (e .g , vitamin . C); some may effects of great nutritional significance of take months, particularly calories (subcuta- the anti-infective, child spacing and eco- neous fat) and protein (muscle). An optimal nomic significance of human milk and breast diet in pregnancy leads to improved fetal feeding. stores and a higher birth weight and more A quarter of a century ago in 1952, Mom- vigorous baby. nison (101) concluded his painstakingly de- Adequate feeding, again based on “multi- tailed analysis of available evidence con- mixes” of locally available foods (79) or cemning the “yield, proximate principles and Downloaded from www.ajcn.org by on August 22, 2009 sometimes on maternal dietary supple- inorganic constituents” of human milk by ments, during pregnancy (as well as lacta- commenting: tion) can assist in insuring adequate mater- “It is clear that there is plenty of room for nab weight gain and sufficient nutrient work on every constituent. This review may serve stones, including calorie reserves in the form to show where special care is needed in sampling I, of subcutaneous fat, as well as a newborn technique and the spacing of samples.” of good weight and with optimal nutritional reserves. Similarly, an appropriate maternal The need for further investigations is diet, again based on locally available food greaten at the present-day in view of the mixtures, should be the emphasis during increasing realization of the significance of lactation , with semisolids slowly introduced human milk on a world basis, but especially to the baby, probably from about the age in resource-poor, less developed countries. of 4 to 6 months onwards, depending on Such studies need to take into account mod- local circumstances, particularly the usual ern knowledge of the psychophysiology and weight curve in infancy in the community endocrinology of lactation, and, if feasible, concerned. Recent studies have shown that should be undertaken on a collaborative the main additional nutrients needed during and comparative basis in various represent- lactation are less than previously thought ative ecobogies in different pants of the (137), and that they can usually be obtained from economical, every-day foods (77). 4 In the still relatively affluent Western world, with Evidence for the adequacy of human milk food increasing greatly in cost but still abundant, as the sole food for young infants up to 6 probably most mothers obtain their extra calories (and months is available, at beast in well-noun- probably most other nutrients also) with little extra expense by taking somewhat larger portions of the ished communities. Theme is evidence of dishes in their everyday diet. However, guidance may improvement in lactation performance, es- be needed in widening this diet, and one wonders pecially the volume of milk produced, with whether the Nutrition Section, Ministry of Agriculture, dietary supplementation in less well-fed cm- or other appropriate body, could suggest economical cumstances, and deterioration with calorie and culturally acceptable additions to the diet during lactation (and pregnancy). In other words, by advising restriction (148). the mother not only that she needs more calories and The message seems clean. As with so protein but also that these can be obtained by eating much else concerning the health and nutri- more mashed potato (with milk) or bread-and-cheese tion of young children, the emphasis should or similar low-cost everyday foods, rather than by be in large measure on the mother.5 By consuming large volumes of milk or other relatively costly animal products. feeding hem with locally available foods dur- The title of a recent paper by Sosa et al. (128a) ing pregnancy and lactation, it will be pos- encapsulates this approach: “Feed the Nursing Mother: sible to optimize the volume and composi- Thereby the Infant”.

510 JELLIFFE AND JELLIFFE world Priority . should be given to practical References issues of immediate application , particularly the effect of improved maternal diet on 1 . ADDY, H. A. The breast feeding of twins: an lactation and, conversely, the breast’s abib- exploratory study . J . Trop . Pediat . Environ. ity to biosynthesize nutrients and to supply Child Health 21: 231, 1975. these to cover the infant’s needs on a contin- la.ALMR0rH, S. G. Water requirements of breast uing basis. fed infants in a warm climate. J. Trop. Pediat. Environ. Child Health, in press, 1978. At the same time , within the labyrinth of 2. APPLEBAUM, R. M. The Modern Management available data, sufficient knowledge already of Successful Breast Feeding. Pediat. Clin. North exists to permit a rational practical approach Am. 17: 203, 1970. to be suggested, based on the important 3. ARROYAVE, G., I. BEGHIN, M. FLORES, C. S. DE Gurno AND J. M. TICAS. Efectos del consumo information available , on probability and de azucar fortificada con retinol, en la madre on an understanding of the biological back- embarazada y lactancte cuya dicta habitual es ground of man’s mammalian needs. As baja en vitamina A. Estudio de la madre y del Ounsted and Sleigh (1 10) comment in a nino. Arch. Latinamer. Nutr. 24: 485, 1974. recent paper on “the infant’s self-regulation 4. BAILEY, K. V. Field surveys on lactating women. Trop. Geogr. Med. 14: 11, 1962. of food intake and weight gain” in the 5 . BAILEY, K . V. Quantity and composition of offspring of presumably well-nourished Downloaded from www.ajcn.org by on August 22, 2009 breast milk in some New Guinean populations. women: “The mange of optimal intake and J. Trop. Pediat. 11: 35, 1965. growth mate varies widely, and the individual 6. BARRIE, H. Modified milk for babies. J. Mat. Child Health 1 : 30, 1976. infant’s needs would best be met, if he is 7. BARRIE, H., E. MARTIN AND C. ANSELL. Milk allowed to take what he wishes, preferably for babies. Lancet 2: 1330, 1975. from his mother only.” 8. BASSIR, 0. Breast milk in Nigeria. J. Trop. Med. Infant feeding is a dyadic phenomenon Hyg. 59: 138, 1956. from many points of view. Nutritionally, an 9. BASSIR, 0 . Nutritional studies on breast milk of Nigerian women (3). Variation in output of milk adequate diet in pregnancy, including atten- with the stage of lactation. West Afr. Med. J. 5: tion to calories, leads to sufficient fetal 88, 1956. stones, an optimal maternal fat bank 10 . BASSIR, 0 . Nutritional studies on breast milk of ( needed to cater for a sufficient volume of Nigerian women. Determination of the output of breast milk. West Afr. J. Biol. Chem. 1: 15, milk with a “normal” calorie content de- 1957. mived from fat), and a vigorous full-sized 11 . BASSIR, 0. Nutritional studies on breast milk of neonate (88a) capable of inducing appnopni- Nigerian women. J. Trop. Pediat. 4: 3, 1958. ate prolactin secretion . Psychophysiobogi- 12 . BASSIR, 0 . Nutritional studies on breast milk of Nigerian women. Trans. Roy. Soc. Trop. Med. cabby, the key moles of the maternal lactation Hyg. 53: 256, 1959. reflexes are also vital to success. 13. BEAL, V. Breast and formula feeding of infants. In practice , it may be that Western pedi- J. Am. Dietet. Assoc. 55: 31, 1969. atnc nutritionists find themselves in a maze 14. BECROFT, C. T. A longitudinal study of breast of often conjectural mathematical biochem- feeding in the Highlands of New Guinea. Med. J. Australia 2: 598, 1967. istry full of circular logic and doubtful data. 15. BELAvADY, B. Special report series no. 45. Stud- (The recent halving of the RDA for calories ies on lactation. Indian Coun. Med. Res. 1963. for lactating women seems to give expres- 16 . BELAVADY, B . Nutrition in pregnancy and lacta- sion to the fundamental uncertainties.) tion. Indian J. Med. Res. 57: 63, 1969. Theme is a need for new factual informa- 17. BELAvADY, B., AND C. GOPALAN. The effect of dietary supplementation on the composition of tion, although difficulties in obtaining it will breast milk. Indian J. Med. Res. 48: 518, 1960. be very great. In the well-fed, non-stressed 18. BOSTOCK, J. Evolutionary approaches to infant mother it seems increasingly clean that care. Lancet 1: 1033, 1962. breast feeding represents an unique titration 19. Bay, G. W. Vitamin deficiency in infants. Trans. Roy. Soc. Trop. Med. Hyg. 22: 9, 1928. between the mother and baby - a truly 20. CAMERON, M., AND Y. HOFVANDER. Manual on dyadic adaptation. Feeding Infants and Young Children. New York: Protein Advisory Group of the United Nations, 1971. Thanks are due to Ms. Indira Yalamanchili for 21. CARNIERO, T. A., AND J. E. DULTA DE OLIv- assistance with library research. ERIA. Nutritional studies on human lactation in

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