This document reviews the volume and composition of human milk produced by mothers with poor nutrition. It discusses 3 main topics:
1) Volume of breast milk produced is often adequate for infant nutrition despite maternal malnutrition. Poor mothers can continue lactating through mechanisms like fat loss.
2) Maternal nutritional status can impact lactation through hormonal effects and cumulative impacts of repeated reproductive cycles and prolonged lactation leading to depletion.
3) Environmental and psychosocial stressors like poverty, poor housing, and cultural changes can negatively impact lactation through increased anxiety levels affecting the let-down reflex and hormone secretion.
The Volume And Composition Of Human Milk In Poorly Nourished Communities A Review
1. 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
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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.
2. 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 particu-
larly 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.
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“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 numer-
ous 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,
3. 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 suck-
ling 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
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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).
4. 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
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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 allow-
ances 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, accord-
ing 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-
5. 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-
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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-
6. 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)
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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-
7. 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 malnour-
ished 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
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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 unsupple-
mented subjects.
undertaken with similar methods in Brus-
8. 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
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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.
9. 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
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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
10. 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
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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
11. 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
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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).