Am J Clin Nutr 1978 Jelliffe 492 515

perspectives
in nutrition
The volume and composition poorly nourished communities A review1

Derrick B. Jelliffe and E. F. Patrice Jelliffe
of human
milk
in
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How is it that poor mens wives, who have no cold fowl or port wine on coshered up, nurse their children without difficulty, whereas the wives of rich and drink everything that is good, cannot do so, we will for the present leave and mothers to settle between them. Anthony
which to be men, who eat to the doctors
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, hydifferent 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, mainly in the subtropics and tropics (77). in resource-poor countries. Fundamentally, ultimate concerns are the Considerations of the volume and comnutritional adequacy of such milk for young position of breast milk in poorly nourished infants in relation to calories, proteins, vicommunities 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, paper attempts to draw together the maternal on infant diets, when or if neces- this main relevant information from different sary. 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, butcircumstances prevail. Differences, when rather in an ecological context. For exam- they exist, may be related mainly to nutriple , with regard to breast feeding in lesstion, to physical overwork and/or to enpsychosocial stress. Other vandeveloped countries, the nutritional andvironmental abbes such as maternal parasitic diseases health consequences of the prevention of diarnheab disease , the lactation contracepand genetic physiological differences may relevant than presently appnecitive phenomenon, and the economic andbe more Variations in results in different studagnonomic considerations have to be borne ated. ies are difficult to interpret, especially those in mind at the same time (77). degree, because of dissimilarities Conversely, for the majority of the world, of minor and methods of sampling and analbreast feeding cannot only be compared in times and levels of maternal underwith adequate feeding with cows milk ysis, in types 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, psyshosocial Methods
and
in stress.
degrees
of environmental
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). ri;u ProcIs.ocin The actual obtaining of representative samples of Alveokts human milk poses unique problems as the normal destination is the babys stomach and not a test-tube or laboratory container. The ejection of breast milk is mediated by the psychosomatic let-down reflex (Fig. reflex . Sucking stimulation on 1). Milk production is proportional to the secretion of FIG . 2 . Prolactin breast generates nerve impulses which pass to the ananterior pituitary hormone , prolactin , resulting from tenor pituitary, which secretes prolactin. This is carnipple stimulation (prolactin reflex) (Fig. 2), and to to the breast where , it acts in the degree of intra-alveolar tension, related to empty- ried in the bloodstream the alveoli causing milk secretion . The prolactin proing. Methods used must, therefore , avoid interfering is proportional to the amount of sucking stimwith normal mechanisms as much as possible, but duced in fact, all do so considerably. As Hytten (48) noted, ulus. the sucking of a baby has, for the mother, psychological 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 compleof 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 day-time on estimations. In fact, in traditional cultures, considerable difference in fat content between fore-the baby sleeps by the mothers side and must obtain and hind-milk (1 to 2 g/100 ml) means that the time considerable of quantities as night feedings . Omo(A 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 (test weighing) (130). Such seasonal changes have long been recog- Test feeding 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 demandas under nonexperimental conditions at homeExpensive, . accurate scales are required to measure relatively small weight increases in an uncooperative infantThere . is
considerable lldk
Alveoko,
likelihood
of
interference
with
the
emo-
tionally-sensitive iety-producing
itably created
let-down circumstances
by the
reflex in the unnatural, and embarrassment

which often
anxinevhave
investigation,
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 tation. Sucking stimulation on nerve impulses that pass to that secretes oxytocin . This passes to the breast, where it acts on surrounding the milk-containing contraction. This expresses the into the lacteals. The sequence milk ejection reflex. Importantly, by anxiety (Fig. 3) and enhanced
key the to successful lacExpression breast generates
the posterior pituitary Milk may be expressed from the breast manually via the bloodstream and by some form of mechanical or electrical pump. the myoepithelial cells,These methods can be used to estimate total output, alveoli, causing their and, of course, are required if samples are to be milk from the alveoli obtained for analysis. is also known as the The same difficulties exist as with test feeding. it can be inhibited Indeed , anxiety can be greater with expression , especially with an unfamiliar, uncomfortable apparatus, by confidence.
494 possibly combined with concern later with the expressed milk. expression on prolactin secretion ling by the baby, is unknown. over Also,
JELLIFFE
feeding the the influence
AND
JELLIFFE
.
nourished women (4)Recent studies in Guatemala have suggested that fat compared with suckloss may be the main mechanism by which such mothers can continue to lactate (124a). Many accounts from different parts of Results the world suggest that malnourished women lactate with unexpectedly little cliniComparative results have varied in differ- often deterioration of their nutrient studies. In some, expression has given cabby obvious status. However, in recent years there greater volumes; in others, test weighing. tional be increasing evidence of shorter peSometimes daily outputs have been calcu- may nods of satisfactory lactation then previbated from the amount obtained at one ously, at least in some parts of the world. feeding only. In all cases, it is apparent that The effect of maternal malnutrition may be results are only approximations. partly hormonal, with decreased secretion Maternal nutrition of cortisol and possibly prolactin (55a) CerComparisons 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 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 deficieninvolved, 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 considpsychosocial stress enable difference between the nutritional Environmental past and present histories in poorer women Under-appreciated in the past has been in Sao Paobo, Brazil, (106a) in Ibadan, Nithe effect of environmental psychosocial genia (8-12), and in Southern India (37). stress from poverty and unemployment, An aspect of the situation about whichfrom poor housing and crime from , ilbegitinothing is known is the effect of the nutri-macy and family instability, and from cubtional status of the pregnant mothers totural 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 mainly to of concern in urban slums and shanty deposition of subcutaneous fat (lactation towns. Despite these differences, certain stores2) can vary considerably from the general findings seem to be usual and enable 1 2 .5 kg suggested for Western women 5 to principles to be suggested on which practical kg (or even weight boss) reported in poorly action can be based. These can be considfed communities (53) Dietary inadequacy ered under three headings-volume, comin pregnancy may sometimes be compli- position, and adequacy of breast milk in cated by associated hard work and by repoorly 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 kg 4 of 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 enough the to subsidize lactation by nearly 00 3 kcal daily development of nutritional edema in very 3 to 4 months for (53).
, . . ; .
baby poorly of
VOLUME
AND
COMPOSITION
OF
HUMAN
MILK
495
TABLE 1 in communities with defective nutrition, it babies (1945). is plainly important to compare results with Mean intake of breast milk in Swedish those from well-nourished communities. Volume (mean) Age Unfortunately, such data are scanty, outBoy. Girls of-date , and difficult to compare because of ml inc differences in technique and sampling, and 645 1 576 because of recent back of interest in the 704 750 2 whole subject of lactation. 3 733 798 817 740 6 In scientific and international literature, 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 easyMonth No. of Breast milk to-remember round number based on an postpartum mothers volume assumption in 1950 in the United Nations ml 0-/2 15 55883 Committee on Calorie Requirements (34a). 11 724 117 /2l/2 It has become sanctified by repetition in 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 antici2 601.4 322.0 892.4 400.2 899.9 3 625.5 pated between 600 to 700 mb/day rather than the 850 mb/day often quoted, accordIn Sweden, test weighing by mothers gave ing to a recent interpretation by Thomson daily volumes which were higher, with a and Black (138) of the data collected by of 838 mb/day (134a). Morrison up to 1952 (101). However, much mean variation occurred between the results of Various studies have been undertaken which have sometimes shown minor variadifferent investigations, depending on the 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 lowest yields towards evening. ticulanly impressive. Carefully conducted investigation of 363 Results concerning variation with age or parity of mother have been rightly termed babies of normal Swedish mothers was unand inconclusive. Variation in dertaken 30 years ago by Wallgren (145), confused of milk secreted between individual using test-weighing at home for 2 consecu- volume 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. HowVery 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 210seems endocrinobogicalby explicable in light of the renal antidiunetic, water-sparing efmb/24 hr. Variation in yield with later lactation fect of pnolactin (77). The common belief intake affects milk yield probably is difficult to judge in webb-nourished corn- that fluid 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 let-down reflex. Conversely, in what has has not been usual in Western industrialized termed a low solute, continuous concountries. Also, there seems little doubt been tract species, such as man, human milk that the main stimulus responsible for the 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 babys source of fluid, as even in solely breast secreted. This is shown by induced bacta-well as nourishment, fed infants, including such a hot climate as tion in some traditional societies and by Jamaica (la). recently introduced adoptive lactation or Dominating considerations of the nornelactation in nonbactating American women, mab range of milk volume secreted by wellwho wish to breast feed their adopted bamothers are difficult questions of bies. (143a) In both, frequent sucking at thenourished breast is the main factor in initiating and sampling, very great differences in techcontinuing milk secretion. Likewise, 24% of nique and timing of collection of specimens, and individual variation between women a series of twins have been shown to be woman , both from day to solely breast-fed adequately for 3 to and in the same 6 months (1). Also, the perpetual, on day and as lactation at progresses As a generbeast very prolonged, high output by tnadi- abization, technique and method of calcubation often appear to play a major robe in tional wet-nurses is in part a reflection of brought forward. continuing vigorous sucking stimulus by suc- the final figure 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 counparticular family (or culture) and the con-tries in Asia and Africa, and in New Guinea The results have been extracted sequent degree of sucking stimulus and its from published information and thesepa effect on the pnolactin secretion. The common concept of the normal pat- proximations are presented in Table De3 tern in Western-type cultures is of rise spite in 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 somemonths old, followed by a slow decline what below those reported from well-nounthereafter. Consideration of lactation pat-ished countries in Europe and North Amerterns elsewhere and the previously men- ica. reported varied greatly and tioned results in twins, in wet-nurses, in Volumes induced lactation, and in nelactation, sug-seem to be lowest in communities with poor gest that the Western pattern may not be levels a of nutrition and with inadequate livbiological inevitable, but rather a response ing conditions, whether urban (Cobombo, to a particular pattern of sucking stimula- Sri Lanka (30)) or rural (New Guinea Highlands (5)) . However, working approximation. 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 of life,00 4 to 600 mb/day in the produced in well-nourished women. By con- months 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 TABLE
Approximate communities0
Country reference 1-6
AND
COMPOSITION
OF
HUMAN
MILK
497
3
quantities of milk produced daily at different periods of lactation in some poorly nourished
months
6-12
months
12-24
months
24 months
and above
India(15,16)
India (Baroda)
.
600ml
(116, 117) 600 (3 mo) (350-1100) 735 (3 mo)
SOOml
350ml
New
Guinea
(Chimbu)
(142)
Biak Island (60) New Guinea (14) New Guinea (5)

Chimbu and Maprik
(540-1100) 525 ml 427 ml 720 ml 400 ml 600 ml
525 ml 390-430 660 ml 400 ml 600 ml
ml
343 ml 127-338 705 ml 400 ml 600 ml
ml
343-142 243 ml 488 ml
ml
New
Guinea
(5)
Baiyer River New Guinea (108) Ajamaru
350-480
ml
270-360 200-210 250-340

150-210
ml (12-18 ml (12-24 ml (12-18

ml
mo) 230-300 mo) mo)
ml
Nubuai Egypt (45) Healthy

Malnourished
310-410
ml
(18-24 mo)
922
733
ml
ml
Sri Lanka
Nigeria
(30)
(Benin) (81)
475
555
ml ml (2-3
Uganda
a
(122a)
not strictly comparable
495 ml mo) 590 ml (6-9 660 ml (2-12 mo)

collection
506 mo) 606
ml ml (13-18
and methods
mo)
of sampling used.
Results
as varying
techniques
taken in the third year of lactation show palan showed an increase in volume severy considerable differences, varying from creted, from 420 to 540 ml in poorly nour230 to 488 mb/day. ished Indian women after protein suppleAlso, 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 bisinhibited or ceases in famine circumstances cuits, showed a rise in serum albumen paris 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, showed 1 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 sugbe 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 contracepsubcutaneous 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 rebeen carried out on the effect of supplemenported by Edozien and co-workers from tation of the mothers diet on output. Go-Nigeria, (31b) when they showed that pro-
498
JELLIFFE
AND
JELLIFFE
less than in dairy cows, but it should be tein supplementation of the lactating remembered that such farm animals have mothers diet increased the milk produced bred to produce much greater yields and weight in the baby, but not the protein been by the offspring (138). content of the milk (Table 4). Similarly, than are required Sosa et al. (128a) demonstrated a rapid Composition increase in milk production in a malnourbiochemical composition of human ished Guatemalan woman following an im- The has been examined in different parts proved diet, particularly calories and pro- milk of the world Approximate comparisons can tein. between various communities, and As usual , those concerned with the pro- be made with well-nourished mothers, for protein, duction of cows milk as a business, the vitamins, and calcium, keeping dairy farmers, have infinitely more practical fat, lactose, previously mentioned difficulties knowledge than those concerned with hu-in mind by variations with sampling (period man milk and breast feeding. Thus, Lind- posed cycle , time of day ; single , reblad and colleagues quoted the following in lactation peated or 24 hr; seasons; one subject or aphorism from Morrisons 1948 Handbook specimens, etc.), with laboratory of Stockmen (101) which may not be com- pooled and with bevels of difficulties in pleteby correct for the human, but is cer-techniques maternal nutrition (Table 5) . Interpretation tainby generally so: of is made much greaten Any inadequacy in the ration or fault in such comparisons by recent realizations of the physiological the methods of care or management will that occur in well-fed healthy generally manifest itself in the yield of milk, variations successfully breast feeding their barather than by a change in its chemical women bies. composition The protein content of human However, the effect of increasing the ma- Protein. milk has been described as varying between ternal diet on human milk output may be 1 .0 to 1 .6 g/100 ml in well-nourished women. In 1952, Morrison reported the TABLE 4 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 that 1 .2 g/100 ml probably represented an 50g lOOg 25g bOg nitially initially overall mean A study in Britain showed 1 .3 g/100 ml (29a). There seems little eviNo. of subjects 7 7 3 3 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 However, very recent Swedish studies (g/lOOml) 0.15 0.19 0.21 0.23 have shown the true protein conMilklactose 8.1 7.9 7.3 8.0 (1975) (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 (91). These investigators pointed out that (g/day) 15 10 38 74 analyses of breast milk were made Weightgainedby 30.4 45#{149}7e 10.5 32.2e earlier baby(g/day) 3.6 2.0 3.6 10.1 with the same methods as used for cows 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 characterfor 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 spedays 8 to 14 (for initial diet) and days to 28 (for 21 cies in infancy, with rather slow growth, diet providing 100 g protein per day). b Duration also permits breast milk to be the only of lactation for all subjects was between 30 and and 90 days. Duration of lactation was over 100 supply of water as well as nutrients. days. ii Results are mean values + SD. e SignifiRetrospective examination of analyses cantly different at the 0.05 level from the unsuppleundertaken with similar methods in Brusmented subjects.
. . . 0 C
VOLUME TABLE 5 Fat, lactose,

nourished
AND
COMPOSITION
OF
HUMAN
MILK
499
protein,
communities
Country
and
calcium
content
of mature
human
milk
from
some
well-nourished
and
poorly
(reference)
Fat
Lactose g/IOO ml
Protein
Calcium mgIlOO ml
Well-Nourished American(92) British(87) Australian (150) British (29a) Poorly-Nourished Indian(17) BantuS.Africa(144) Chimbu, New New Hebrides 4.5 4.78 6.8 6.95 7.4 1.1 1.16 1.3 34.0 29.9 28.6-30.7
4.2
3.42 3.90 2.36 3.8
Guinea (111)
Highlands
(142)
7.51 7.10 7.34 5.0
1.06 1.35 1.01 1.40
34.2 28.7 25.8
Wuppertal,
(Immediately Nauru(19)
Germany
Post World War II) (42)
3.59
1.20
1.60
Ibadan,
New
Nigeria
Guinea
(88
(Biak)
months)
(60)
(62)
1 .20
(0.59-1.79)
0.83-0.9
Alexandria, Healthy Malnourished
Egypt
(45) 4.43 4.01

2.3 2.8 3.9
6.65 6.48
6.48 6.8 6.8
1.09 0.93
0.93 1.5 1.3 20.8
New Guinea (14) Sri Lanka (30) Brazil (21) Higheconomic
Loweconomic Pakistan (139) Tanzania (25)

Nigeria(Ibadan)(102)
a
4.2
Often below 4.05
6.5 2%
7.67
1.3 1.2
1.22
25.7
Modified
from
Gopalan
and
Belavady
(37),
with
added
data.
Belgium (129) in 1954 and in Tokyo, although the lysine and methionine levels (1 23) shows similar low levels for were lower. true protein content as with recent SwedVarying 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 defitries, 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 totalfound 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 suppbemen100 ml), although the range may be quite tation on protein content does not appear wide (Table 5). to have been investigated adequately. HowIn some places with probably poorer flu-ever, in the protein supplementation study trition, analyses with older methods have carried out by Gopaban, the increased outsometimes shown the protein content to be put of milk was associated with a comelower (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 acadding 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 likenot available at the time of earlier studies. techniques in Sweden, Belgium, and Japan, Recent investigations by L#{246}nnendal et al.
-
sels, Japan
500
JELLIFFE
AND
JELLIFFE
(91) have shown many unexplained vania- breast milk (or cows milk based formula) tions in healthy, well-fed women-for exappears to be reflected in the fatty acids in ample, in milk-specific proteins, those the infants subcutaneous fat. synthesized by the mammary gland,noThe relevance of the fatty acid (and cholestenol) contents of human milk is currently tabby ct-lactalbumin and lactoferrin The decrease in total nitrogen in the first period under consideration in relation to the devebof the central nervous system and of lactation, for example in the first month, opment was mainly due to a dramatic drop in secre- atheroma in adults in industrialized countory 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 no diurnal a variation. Morrisons (101) figphysicochemical appetite control for theune based on 1010 samples examined in 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 theand Mawson found 6.9 g/100 ml in 586 samples of mature milk (87). In poorly United States and Britain showed means of 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 (111). oping countries have demonstrated consid- was reported enable variation (Table 5). However, some Calories. The calorie intake from breast is a product of the volume (as taken recent work has suggested that the fat maymilk sometimes be considerably reduced, even by the baby) and its caloric content, which is derived from fat. In well-fed down to 1 g/100 ml (24b). Under these primarily 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). Thefigure of 75 kcab/100 ml (range 45 to 119). The recent United Kingdom report showed significance of a bower fat content has to be related to inadequate energy intake in pneg- a mean of 70 kcab/100 ml (29a). In poorly nourished communities, both nancy, with an inadequate subcutaneous secreted and the fat, the ain m fat bank (53), as well as to the diet the volume in lactation itself. calorie-containing constituent, (and other The fatty acid pattern of breast milk cannutrients) may be less than in well-fed mothbe 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 A . The concentration is influare extreme) (25a) on by changes in the Vitamin by the adequacy of the diet of the calorie intake (57, 147). During energy enced in pregnancy and lactation. The equilibrium, milk fat resembles the fattymother A content of breast milk is often acid pattern of dietary fat, but when inade- vitamin lower in poorer populations of some quate calories are eaten, the fat in human much countries (India , Ceylon , Indomilk follows the composition of human sub-developing Jordan), where this nutrient is marcutaneous depot fat. The major factor influ- nesia, than in Europe and North America. encing the fatty acid composition of milk ginal, is Maternal serum bevels are also low. The the carbohydrate supply in the diet. Ultiintake is generally higher in the spring and mately, the fatty acid composition of the
. .
VOLUME
AND
COMPOSITiON
OF
HUMAN
MILK
501
Although human milk is bow in summer months due to greaten supplies of Niacin. actual niacin, it has a high potential niacin dark green leafy and yellow vegetables. because this vitamin may be syntheParticularly high levels of netinob (vitamin value the amino acid, tryptophan. A) have been noted in Western Nigeria, sized from B12. Low bevels of vitamin B12 presumably because of the widespread use Vitamin have been found in the milk of poorer of palm oil in cooking (102). vegetarian women in Bombay. Also, in varIn a recent comparative investigation , the parts of India the syndrome of vitamin A content of breast milk was signifi- ious have been described in solely cantly higher in normal Swedish mothers tremors fed babies, and has been ascribed to than in nonpnivileged Ethiopian mothers, breast deficient B12 in the mothers milk (59). whose milk showed greater concentrations Vitamin C. The level of ascorbic acid in of f3-carotene (35). milk is subject to variations in dietary Kcn and Mawson (87) found that supple- breast in developing countries, particularly mentation with vitamin A, before and after intake with the seasonal availability of fresh fruits partunition or later during lactation, bed to and vegetables. In webb-nourished mothers, the secretion of milk richer in vitamin A milk contains an average of 4 mg/ than normally produced. In Central Amer- human 100 ml of vitamin C. In Botswana (formerly ica, Arroyave et al. (3) observed a rise in Bechuanaband), Squires (130) found the the breast milk vitamin A levels after the content to be 1 .7 mg/100 ml in the dry introduction of vitamin A fortified sugar. and 2.7 mg/100 ml in the wet seaVitamin D. As well-known, levels of fat- season The subjects were poorly nourished soluble vitamin D are low in both human sons. women. and bovine milks. However, the recent dis-Tswana Since the ascorbic acid contant of breast covery that breast milk contains a watermilk is greater than that of blood plasma, soluble conjugate of vitamin D with subwhich is generally below 2.5 mg/100 ml, phate (87a) producing the same anti-nachitic activity in the mammary glands potential as milk formulas fortified withsecretory play a part in determining the bevel of conventional vitamin D explains the clini- must C in milk. Apparent adaptation to cally well-recognized rarity of rickets in thevitamin low maternal intakes of vitamin C has been breast fed. in Banoda, India (117) and the PhilThiamine. The thiamine content of breast noted (132). The possibility of placental milk in areas with a high incidence of infan- ippines in pregnancy has been suggested. tile beriberi has been found to be low, duesynthesis Certainly both the placenta and the breasts to insufficient maternal stores and intake in may be abbe to actively secrete ascorbic communities with diets largely based on acid for the offspring. Levels of fobic acid polished rice (66) Under these circumstances, 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 supplementation during pregnancy and lactation It is so Vitamin characteristic in time of onset that the 2 to Deodhar and Ramakrishnan (28) carried 5 month mortality has been suggested as anout 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 was analyzed is for the concentrations of the adequate. However, in South India, Gopasame vitamins. A positive and significant ban and Belavady (37) found an average of correlation was found between dietary inonly 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 suppleIn this regard, it is often insufficiently mentation. appreciated that the RDAs given for inIn a more recent investigation, supple- fants are themselves derived from estimated mentation with ascorbic acid, nicotinic acid, intakes of breast fed babies, with an addiriboflavin, thiamin, pantothenic acid, cyan- tional safety factor added for the less certain of infants fed on cows milk forocobalamin, biotin, pyridoxine, and folic situation mulas (70). This is the case, for example, acid was undertaken. As a result, the vithe very high RDA of iron (1 0 mg/ tamin content of the milk increased steadily with for the first 6 months of , life which with the dose used in supplementation (29). day) with human milk. Calcium Levels of calcium reported in can not be attained the milk of webb-fed mothers vary considerThe derivation of RDAs for infants are not understood by pediatricians or ably. The calcium content in poorly nour- often so that the advertising of cornished mothers has been reported to range nutritionists, baby foods can issue the following from normal levels to somewhat bow con- mercial to logic: centrations (Table 5). Again, differences in appeal sampling and technique may be in part A stimulating exercise for professionals would responsible. ones beliefs about breast feeding into Levels of other minerals will not be con- be sorting 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. sincerely believe that breast milk is all tent of trace minerals will be much under Many sufficient without any supplementation for at least investigation in coming years, in relation six months if not the full duration of breast feedboth 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
inanity of this comment is apparent The nutritional adequacy of breast milk The especially in view of the biological adaptafor the infant can be roughly assessed by that has occurred over hundreds of measuring 24-hr output and chemical corn- tion mibbenia. Carried to extremes, this argument position , or by the recording of satisfactory mean that breast milk was unfit for growth, good health and absence of clini- would consumption by human babies, without adcab malnutrition. Adequacy of nutrients. The nutrient ditional iron and vitamins. needs of the baby during the exterogestate The RDAs of protein and calories sugfetal stage are not derived only from the gested for infants have been derived from diet, but also from fetal stores acquired breast in milk estimations, feeding with cows utero, from the placental transfusion (iron) milk based formulas and from the imponand, to a limited and variable extent fromtant, 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 (procab 143kg); 6th month-990 and yet it is agreed increasingly that pres-tein 2.6 g/kg; ml/day (protein 1 .7 g/kg; cal 90k). entby available data on the composition of human milk is incomplete and out-of-date. However, as noted earlier, outputs in women actually nursing their Fomon (34) rightly notes the need for more well-nourished 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 milkmonths (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 the first six months (Table 4). of breast milk give urgency to this comment. during
-
VOLUME
AND
COMPOSITION
OF
HUMAN
MILK
503
protein recommended, are probably high. As noted earlier, many of the constituents As noted earlier, the reported consumption of breast milk can be affected by inadequate maternal nutrition, depending upon its Se- milk of in direct breast feeding studies are verity, length and the mothers previous often lower with apparently well-nourished nutritional status. Water soluble vitamins babies. Also, the difficulties with understanding are particularly influenced, including ascorthe nutritional and biochemical meaning of bic acid and riboflavin. Likewise, levels of vitamin A and the pattern of fatty acidsresults obtained by analyses of single samples are increased by recent increased reflect maternal diet and stores. The fat awareness of the physiological variation in may be reduced in some malnourished milk composition and by the need countries. The protein content of human human breast milk as a biological milk in poorly nourished women is usually to recognize 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 others absorption and utibiza100 ml) (Table 5). tion, rather than as a solution of indepenBy comparison with estimates of volume dent chemicals. Recent work on the supeand 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 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 intothe breast fed and the bottle fed. account before making too sweeping concluPhysiological variations in the constitusions: ents of milk from webb-nourished healthy First, the figures on volume gained in mothers with babies who are being successfully breast fed can be between individuals general studies are often those obtained by expression or following test-feeding with the and/or in the same individual at different times. Similar differences are to be found errors implicit, and often having a risk of 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. cows milk have been recognized for decSecond, 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 mainof nutrients, but also may have less sucking tam that we have barely scratched the potential. surface of the complex behavior and propFifth, the data on which the RDA are erties of the (cows) milk system and other based are inadequate and approximate forfundamentals of dairy chemistry. There infants. The babies in the Fomon and Mayare 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 differsibly appetite-controlling function of high ence in milk composition on lactationab abilfat 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 andto the stage of maternal digestion. The fat
-
504
JELLIFFE
AND
JELLIFFE
Also, it is possible that stimuli from the content increases with an uninhibited betdown reflex (with a possible appetite-connursing baby may affect the milk compositrolling significance (44), and the prolactin tion, by as yet unappreciated mechanisms, produced as a result of sucking appear such to 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 fanciconstituents secreted may also occur. Blood ful. However, the ability of the female kanbevels of sugar, fat, amino acids, and other garoo simultaneously to secrete milks of nutrients will rise at different times afterquite different compositions from two nipthe mothers 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 breasts secretory cellsmay be noted (77). fluctuate also. The physiological variation in composimilk is unsurprising. Genetic Cyclical chronobiobogicab changes aretion of human variations and cyclical changes occur in the continually occurring in all living organisms, from plankton to flowers to vertebrates. In milks of other mammals, and, as menman , well-recognized cycles include those tioned, in other body fluids in man. The that occur each 24 hr (circadian rythms), expectation that breast milk will be staneach 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 aspractice , for the past 1 00 years (which has placed emphasis on the constancy of physipects of body physiology, including for example, the secretion of steroids, body tem-ological systems, (and) inter alia that conperatune , the rate of cell division and levels stancy is a characteristic of life Rather the normal healthy human being is an osof brain electrical activity. Some chronobiobogical variations in thecillating system that is fluctuating chronoconstituents 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 lactapregnancy, lactation can be considered as tion a 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 cornbetween individuals and in any one composition of human milk occur between position the cobostrurn , with its high protein (protecindividual. Breast feeding does not consist tive immunogbobulins, etc., high zinc and ingesting of milk obtained at a single time, pattern of fatty acids, and subsequent mabut over a continuing period of time Hutune milk. Later, chnonobiobogical changes man milk can, therefore, be considered as in the lactation cycle are unclean and needphysiologically variable in composition , mesponding to various factors suggested earlier investigation. 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 stage of growth and development. partly taken cane of by the demand and particular the question of possible disadvansupply nature of the volume of milk pro- Finally, duced in breast feeding, with greaten suck- tages of rigidly constant formula composiing stimulus beading to greaten secretion. In tion needs consideration. Such is the case regard to absence of a cobostrum-suraddition, the composition may vary with with the individual need of the baby, possibly on rogate, but whether inability to match the a genetic basis oras a result of feedback flexible variability of breast milk is signifimechanisms acquired transplacentally by cant on not will only become more apparent more detailed investigations are unthe mother while the fetus was in utero. when
. , .
VOLUME
AND
COMPOSITION
OF
HUMAN
MILK
505
dertaken into the mechanisms and purpose milk (and the prolactin-mediated supply of physiological chronobiological changes inand 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). breast fed, and, of these, is that the present RDA for young babies 23 .7% pains were 59.5% received no food other than human in the exteno-gestate fetal stage are in milk for three months or more, and 21.9% urgent need of reconsideration In view of on more (1). Growth is being the unique biochemical components of hu-for 6 months investigated in detail, but in general seemed man milk (and their interactions), the to those bottle fed. dyadic nature of nutrition in early infancy comparable With the babies of poorly nourished and the difficulties of obtaining valid breast in resource-poor, technically devebmilk samples, it would appear that these mothers oping countries, difficulties in interpreting revisions will pose considerable , perhaps growth curves exist in relation to the prevainsuperable, difficulties in practice. and significance of low birth weights Adequacy by growth. It is apparent that bence community, in the selection the ultimate test of the adequacy of human in the particular standards thought to be the milk output in breast feeding is not reflected of reference appropriate genetically for the particby estimates of volume produced or by themost ular group, the significance of infections composition, but rather by assessment of diarrhea with fluid loss) and the physical growth, metabolic equilibrium, and (including usual problem of sorting out weight gain in good health and nutrition. From an immediate and rough point-of-view, adequate relation to increases in fat, muscle on waterelectrolyte retention. growth is normally assessed anthropornetnicabby, usually judged approximately by serial Earlier evidence from various pants of weight gain, and by the absence of necogniz- Africa and India in the 1950s indicated able nutritional deficiency, as the main prac- that breast feeding, with little or no suppletical 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 mevigor 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 those to 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 some in 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 Mexico in (23 , 94) the weight gain in some Peoples Republic of China (125), that babies was reported to have become madesolely breast fed infants do well and show quate after only 3 months. It seems possisatisfactory gains in weight during the firstble , then , that decreasing lengths of satisfac6 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 theweight 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 comThe adequacy of unsupplemented human position. The possible range of significance
. -
506
JELLIFFE
AND
JELLIFFE
pling methods and analytic techniques. These would include preferably more than one 24 hr sample, and include investigations covering the volume and major nutrients as well as more recently recognized biochemicab components and physio-chemical eleConclusions ments (such as the forms of casein present) in different communities with various levels The investigations summarized in the of maternal ovenand under-nutrition, inpresent account of knowledge concerning cluding women using oral contraceptives. the quantity and quality of human milk These in should also include longitudinal samboth well and poorly nourished communiples to investigate the dimensions (and punties 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 the 1975 studies in Sweden (89, 91), Newgeneralizations 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 opLikewise , 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 materof 2) The volume and composition of human nab malnutrition (and of maternal depletion milk in poorly nourished women is sumpnisfrom numerous previous reproductive cyingly good, possibly due to some metabolic des) are rarely indicated, and indeed, withadaptations, 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 suboptifenences 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 vitaquately (138) and would be difficult to mins, vitamin A, and somewhat lower cabundertake, because of variation in diet andcium 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 moreoutput 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- mothers 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
.
of the latter is emphasized by recent reviews which reveal the complexity of oral contraceptive interactions with vitamin metabolism in general and difficulties in their interpretation (22, 73, 88).
VOLUME
AND
COMPOSITION
OF
HUMAN
MILK
507
more) is insufficient by itself for the rising TABLE 6 practices in orthodox Western maternity nutrient needs (and declining stones) of thePuerperal ward, which interfere with lactation, via the prolactin rapidly growing infant, and forms a decreasand let-down reflexes. In other cultural circumstances, ing, but, valuable supplementary source of analysis an 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 Practical approaches
Delaying first breast feed
If growth, as evidenced by the weight Supplying prelacteal and complecurve, becomes inadequate in solely breast mentary feeds limited feeds (4 hr) Limitation of fed babies at 4 months or earlier in poorRegularly, sucking and communities in less developed countries, it (with no night feeds) prolactin seis 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) free supply of formula occurring in isolation, with the mother as Automatic a food industry literatempemamentless, disease-free breast ma- and infant 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) before and after (test tation failure in poor women, namely milk Weighing volume, does not seem to be primarily de- feeds) Restricting visitors Anxiety and inpendent on food intake, but the combined terference with stress of maternal disease , undernutrition let-down rehealth staff (anand the increasingly difficult living condi- Unsympathetic tidoula effect) tions in rapidly developing city slum areas Automatic free supply of formula It follows, therefore, that diagnosis of an and infant food industry literaindividual 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 unenvironmental psychosocial stress. Nevercertainty 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 withthrough the maternal reflexes and through out cost and make the initiation of lactation hem nutrition, so that the relative signifieasier (Table 7). cance of these two requires consideration in There is little doubt that disturbed reflex any individual woman on community. behavior is often more important in the causation of lactation failure than maternal Interference with reflexes 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 invesresponsible 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 in Indonesia comments that, in domestic traditional culture on, more often, in im- 3 Rohde the output in the second year means that the ported Westernized practices in maternity terms, child is receiving at least one 8 oz glass of milk daily, units (Table 6) which reduce sucking stimuwith 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 andand 200 to 500 IU ofvitamin A (121).
-
Sedated newborn ternal anesthesia)
(excess
ma-
508
JELLIFFE
AND
JELLIFFE
proach (allaitement mixte) usually needs to be avoided. It introduces the danger of If the infant is judged to be receiving weanbing diarrhea at an early and vulnerable breast milk, which is insufficient in volume It decreases the secretion of breast and/or composition because of poor mater- age milk, as it interferes with sucking stimulanal nutrition, three approaches need to be tion and proportional secretion of pituitary considered: prolactin. It interferes with lactation amenCows milk supplementation. A logical It is an additional endorsement by possible solution may seem to be the intro- orrhea. the pediatric nutritionist of the unfortunate duction of bottle feeds with cows milk unaffordable trend away from breast based formulas from just prior to the usual and feeding. Lastly, if viewed on a family or on age of flattening of the weight curve. community basis, it has ecoIn the circumstances of most resource- a large-scale nomic, agmonomic and food production conpoor, less developed countries, this apsequences 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 introduced. Also, in average kitchen cmcumstances in tropical countries and with the foods most often available, it is usually very difficult to prepare digestible, well-tolemated and nutritionally adequate supplementany 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 and hence on lactation performance than FIG. 3. The anxiety-nursing failure s)ndrome. Anxcows milk by bottle and can be based on iety, uncertainty or lack of interest can inhibit the letdown reflex, often leading to failure of lactation. the use of mixtures of locally available
.
Inadequate
maternal
nutrition
TABLE Possible
Health
7 modifications
service
in health
services
designed
to promote
breastfeeding
in a community
(77).
(1978.)
Modifications
Prenatal
care
Information Maternal
on breastfeeding diet. Emotional

relatives and
(preferably preparation
visitors
from for (e.g.allow ,
breastfeeding
mothers).
Breast
preparation.
labor. to eat
privacy
Puerperal
care
Avoid
maternal
fatigue/anxiety/pain in mind). as possible;

Lactation
in early
and relaxed
labor; no
avoid
atmosphere;
unnecessary
organization
episiotomy;
allowed;
of day with breastfeeding breast feeding as soon

schedule; rooming in).
Stimulate lactation avoid unnecessary

consultants
(e.g., maternal extra
prelacteal anesthesia;
who
feeds; first permissive

have
(advisers-preferably
women
breast fed); or spoon.

Premature unit
adequate
lying-in-period.
In hot
weather,
water
to baby
by dropper
Use
of expressed earliest return
breast
milk
(preferably
fresh).
Contact
between
mother
and
baby
with
to direct breastfeeding. in hospital (or nearby) for mothers of breast fed babies.
Childrens
wards
Accommodation
Home Health
visiting center
Encourage, Supplementary
locally
motivate, food
relevant
atmosphere
support. distribution (e.g., formula and wearning foods) according to defined,
policy.
General
Supportive
foods
policy
(e.g. , samples, and practical
all staff. Avoid promotion of posters, calendars, brochures, etc.). health education concerning biological
from
unwanted commercial Adopt minimal bottle breastfeeding.
infant feeding
VOLUME
AND
COMPOSITION
OF
HUMAN
MILK
509
I,
blended as multi- tion of breast milk, to avoid the economic, infective and distributive complexities of based on cereal-legume introducing cows milk and bottle feeding Supplementation of maternal diet.4 Curunnecessarily, and also to avoid assisting a decline in breast feeding on a rent knowledge suggests that the most eco- still further nomical, safe , physiological, and practicable community basis. and at risk of oven-repetition, method of approaching the situation is by In addition, be emphasized again that those laying maximum emphasis on feeding the it must 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 (subcutathe anti-infective, child spacing and ecosignificance of human milk and breast neous fat) and protein (muscle). An optimal nomic diet in pregnancy leads to improved fetal feeding. of a century ago in 1952, Momstores and a higher birth weight and more A quarter nison (101) concluded his painstakingly devigorous baby. analysis of available evidence conAdequate feeding, again based on multi- tailed cemning the yield, proximate principles and mixes of locally available foods (79) or constituents of human milk by sometimes on maternal dietary supple- inorganic ments, during pregnancy (as well as lacta- commenting: tion) can assist in insuring adequate materIt 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 of subcutaneous fat, as well as a newborn technique and the spacing of samples. of good weight and with optimal nutritional The need for further investigations is reserves. Similarly, an appropriate maternal at the present-day in view of the diet, again based on locally available food greaten realization of the significance of mixtures, should be the emphasis during increasing human milk on a world basis, but especially lactation , with semisolids slowly introduced in less developed countries. to the baby, probably from about the age resource-poor, Such studies need to take into account modof 4 to 6 months onwards, depending on of the psychophysiology and local circumstances, particularly the usual ern knowledge endocrinology of lactation, and, if feasible, weight curve in infancy in the community be undertaken on a collaborative concerned. Recent studies have shown that should basis in various representthe main additional nutrients needed during and comparative ative ecobogies in different pants of the lactation are less than previously thought
. .
foods, mixes, blends
nutritionally particularly (79).
(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 probably 6 most mothers obtain their extra calories (and most other nutrients also) with little extra months is available, at beast in well-noun- probably 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 acceptable additions to the diet during cumstances, and deterioration with calorie and culturally 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 low-cost everyday foods, rather than by tion of young children, the emphasis should or similar consuming large volumes of milk or other relatively be in large measure on the mother.5 By costly animal products. feeding hem with locally available foods durThe 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 breasts abibexploratory study J Trop Pediat Environ. ity to biosynthesize nutrients and to supply Child Health 21: 231, 1975. la.ALMR0rH, S. G. Water requirements of breast these to cover the infants needs on a continfed infants in a warm climate. J. Trop. Pediat. uing basis. 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 Am. 17: 203, 1970. exists to permit a rational practical approach 3. ARROYAVE, G., I. BEGHIN, M. FLORES, C. S. to be suggested, based on the important 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 backembarazada y lactancte cuya dicta habitual es ground of mans mammalian needs. As baja en vitamina A. Estudio de la madre y del Nutr. 24: 485, 1974. Ounsted and Sleigh (1 10) comment in a nino. Arch. Latinamer. 4. BAILEY, K. V. Field surveys on lactating women. recent paper on the infants self-regulation 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 breast milk in some New Guinean populations. women: The mange of optimal intake and J. Trop. Pediat. 11: 35, 1965. 6. BARRIE, H. Modified milk for babies. J. Mat. growth mate varies widely, and the individual 1 : 30, 1976. infants needs would best be met, if he is Child Health 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. Hyg. 59: 138, 1956. Infant feeding is a dyadic phenomenon 0 Nutritional studies on breast milk of from many points of view. Nutritionally, an 9 BASSIR, Nigerian women (3). Variation in output of milk adequate diet in pregnancy, including attenwith the stage of lactation. West Afr. Med. J. 5: tion to calories, leads to sufficient fetal 88, 1956. 0 Nutritional studies on breast milk of stones, an optimal maternal fat bank 1 0 BASSIR, Nigerian women. Determination of the output of ( needed to cater for a sufficient volume of breast milk. West Afr. J. Biol. Chem. 1: 15, milk with a normal calorie content de1957. mived from fat), and a vigorous full-sized 1 1 BASSIR, 0. Nutritional studies on breast milk of neonate (88a) capable of inducing appnopniNigerian women. J. Trop. Pediat. 4: 3, 1958. 1 2 BASSIR, 0 Nutritional studies on breast milk of ate prolactin secretion PsychophysiobogiNigerian 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 pediJ. Am. Dietet. Assoc. 55: 31, 1969. C. T. A longitudinal study of breast atnc nutritionists find themselves in a maze 14. BECROFT, feeding in the Highlands of New Guinea. Med. of often conjectural mathematical biochemJ. 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 lactation. Indian J. Med. Res. 57: 63, 1969. sion to the fundamental uncertainties.) 17. BELAvADY, B., AND C. GOPALAN. The effect of Theme is a need for new factual informadietary 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 care. Lancet 1: 1033, 1962. mother it seems increasingly clean that 19. Bay, G. W. Vitamin deficiency in infants. breast feeding represents an unique titration 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:
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perspectives

The volume and composition poorly nourished communities A review1

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which to be men, who eat to the doctors

nutrition, psyshosocial Methods

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reflex in the unnatural, and embarrassment

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Biak Island (60) New Guinea (14) New Guinea (5)

(540-1100) 525 ml 427 ml 720 ml 400 ml 600 ml

525 ml 390-430 660 ml 400 ml 600 ml

343 ml 127-338 705 ml 400 ml 600 ml

343-142 243 ml 488 ml

Baiyer River New Guinea (108) Ajamaru

270-360 200-210 250-340

ml (12-18 ml (12-24 ml (12-18

mo) 230-300 mo) mo)

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Nubuai Egypt (45) Healthy

495 ml mo) 590 ml (6-9 660 ml (2-12 mo)

506 mo) 606

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VOLUME TABLE 5 Fat, lactose,

7.51 7.10 7.34 5.0

1.06 1.35 1.01 1.40

34.2 28.7 25.8

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Alexandria, Healthy Malnourished

(45) 4.43 4.01

New Guinea (14) Sri Lanka (30) Brazil (21) Higheconomic

Loweconomic Pakistan (139) Tanzania (25)

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Sedated newborn ternal anesthesia)

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on breastfeeding diet. Emotional

from for (e.g.allow ,

fatigue/anxiety/pain in mind). as possible;

of day with breastfeeding breast feeding as soon

Stimulate lactation avoid unnecessary

(e.g., maternal extra

feeds; first permissive

breast fed); or spoon.

of expressed earliest return

support. distribution (e.g., formula and wearning foods) according to defined,

(e.g. , samples, and practical

unwanted commercial Adopt minimal bottle breastfeeding.

foods, mixes, blends

nutritionally particularly (79).

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Advisory T. Nutritional A.,

VOLUME Brazil. J. Trop. 19: 384, 1974.

COMPOSITION Child Health

in a pre-industrial 56: 71, 1967.