PEDIATRICS (ISSN 0031 4005). Copyright © 1984 by the American Academy of Pediatrics.
Infant
Feeding
and Infant
Growth
Jane F. Seward, MBBS, and Mary K. Serdula, MD
Growth in infancy is a complex process affected
directly or indirectly by numerous interrelated
fac-tors. The predominant factors include diet, the
nutritional status and health of the mother, and
the occurrence of infections. In addition, social
factors (family structure and cohesiveness),
eco-nomic status, cultural practices, and biologic
fac-tons-such as the sex of the infant, birth weight,
birth order, birth interval, and genetics-may also
play a significant role in growth.
Nutritional factors may affect growth in infancy
both before and after birth. Maternal and infant
nutrition are intimately related. For breast-fed
in-fants, nutrition of the mother and that of her young
are interrelated from conception until weaning;
therefore, dietary intake of pregnant and lactating women is very important.#{176}7 Underweight mothers with poor weight gain in the last trimester of
preg-nancy bear infants with lower mean birth
weights.11’ Although there are ethnic differences in
low birth weight in the United States, the incidence is relatively low.45 In contrast, in developing
coun-tries, low birth weight (2,5OO g), mainly caused by
the high proportion of growth-retarded newborns,
is a major public health problem.’26”38 Infants who
have suffered from intrauterine growth retardation
remain smaller, on average, than normal babies
throughout infancy and early childhood.Co,39,44
In developing countries, many nondietary factors
also play an important role in determining growth.
Infections, particularly gastroentenitis, are among
the most important of these factors.91”24
Case-con-trol studies examining factors that differ between
malnourished (weight-for-age less than Harvard
third or tenth percentile) and adequately nourished children in the second 6 months of life have found
significant associations between the following
non-dietary factors and growth failure: high birth order
(greater than six or seven), lower mean maternal
age, low maternal weight, children from families in
which one or more siblings had died, greater mean
number of children less than 5 years old in the
home, birth weight less than 2.4 kg, twinning,
in-fections (measles, whooping cough, severe or
ne-peated diarrhea), death of either parent, on a broken marniage.4’#{176}
The association of both dietary and nondietary
factors with growth and their complex interactions
make interpretation of growth studies difficult. It
is likely that these factors ultimately affect growth
through inadequate dietary intake, increased
infec-tions, or both; and the best use of such factors may
thus be to determine infants at high risk of poor
growth. The similar rate of growth in infants from
groups with high socioeconomic status in
develop-ing countries and infants in developed countries is
undoubtedly because of adequate nutrition, better
environmental conditions, and fewer
growth-re-tarding infections.
Unfortunately, the pattern of growth seen in
developed countries is the exception rather than
the rule in developing countries, where
malnutni-tion is a chronic problem. As mentioned, this often
begins at conception because poorly nourished
women tend to bear babies of low birth weight. The
most severe faltering in growth usually occurs in
the transitional weaning period in the second half
of infancy, when the interaction of inadequate diet,
infections, and growth retardation combines to
pro-duce a malnourished child at higher risk of death.
Kielmann and McCond78 showed that for every 10%
decline in weight-for-age below 80% weight-for-age
compared with the Harvard median there was a
twofold increase in the risk of death.78 Similarly,
Chen et al24 found that children categorized as
severely malnourished (weight-for-age <60%
Han-yard median) between 13 and 23 months of age
experienced a threefold higher mortality during a
2-year follow-up period than normally nourished
or mildly to moderately malnourished children
(weight-for-age >60% Harvard median).
The primary concern of this section is to review
current knowledge on the effects of feeding method
(breast v alternative methods v a combination) on
infant growth and nutritional status in the
devel-oping world. Because the nutritional requirements
of the infant increase as it grows, the optimal
method of feeding will change with age from an
mod-ified adult diet. Breast milk alone cannot be
ex-pected to support normal growth during the second
half of infancy. This leads to an important related
issue that is addressed first; namely, the length of
time that an infant who is exclusively breast-fed
can grow normally.
HOW LONG INFANTS WHO ARE
EXCLUSIVELY BREAST-FED HAVE NORMAL
GROWTH
As long as a satisfactory growth rate is
main-tamed, there is little disagreement that exclusive
breast-feeding is the preferred mode of feeding for
healthy babies.3 Obviously, however, for every
in-fant, breast-feeding alone at some point becomes
inadequate to fully provide the energy and nutrient needs for growth; a food supplement is then needed.
The age when additional food is needed depends on
many interrelated factors, including the mother’s
health and nutritional status, the quality and quan-tity of milk produced, and the infant’s birth weight,
gestational age, and health (particularly burden of
infection). Because of the number of factors
in-volved, the age when breast milk alone becomes
inadequate to meet the nutritional requirements for
satisfactory growth may vary between populations
and between individuals within a population. A
recent review on the appropriate timing for
com-plementary feeding of the breast-fed infant has
been done by Underwood and Hofvander.’31
Two approaches have been used to evaluate the
adequacy of breast milk for infant growth:
theoret-ical calculations of infant energy and protein
re-quirements for growth compared with breast milk
produced; and actual growth performance of infants
compared with growth references.
The following topics will be discussed in this
section: (1) growth references; measurements of
nutritional status and issues in interpretation; (2)
theoretical calculations; (3) measurement of breast
milk output; problems and issues; (4) studies on
growth performance of breast-fed infants in devel-oped and developing countries.
Growth References
Measurements
of Nutritional
Status
Most studies on the effect of feeding practices on
infant growth and nutrition use anthropometnic
measurements to determine the adequacy of infant
nutrition. The measurements most frequently used
in studies reviewed for this report were weight-for-age and height-for-age.
Weight-for-age is the most commonly used
an-thropometnic measurement. It is easily measured
by relatively untrained personnel and reflects
pres-ent nutritional status. Weight curves for individual
infants, especially in developing countries, show
wide variability, with many short-term
fluctua-tions. A single weight-for-age measurement should
therefore be interpreted cautiously. The nutritional
status of groups of infants or children has been
most frequently assessed via a classification system based on a deficit in weight-for-age.49’#{176} More
re-cently, a combination of weight-for-height as an
indicator of present state of nutrition and
height-for-age as an indicator of past nutrition has been
advocated.’45 Weight-for-height is nearly independ-ent of age between 1 and 10 years.145 At ages of less
than 1 year, at a given height or length the older
infant tends to be heavier. This source of error
coupled with the difficulty of performing accurate
length measurements in children less than 1 year
of age limits the use of weight-for-height as an
indicator of nutritional status in infants less than 12 months of age.
Height- or length-for-age is an indicator of
long-term nutritional status. Accurate, reproducible
measurements require two trained personnel.
Stat-ure is considered to be one of the more hereditary
morphologic characteristics.’ In well-nourished
populations, in which infants are presumably
ful-filling their genetic growth potential, changes in
rate of linear growth (height) occur frequently dur-ing infancy. Although birth length (which is related
predominantly to maternal size) correlates poorly
with eventual height, by 2 years of age, length
correlates best with mean parental height.’25 This
means that infants frequently shift in length
per-centiles (catch-up growth or “lag-down” growth)
during the first 2 years of life. Thus, an otherwise
healthy infant whose birth length is near the 50th
percentile and decelerates toward the third
per-centile during infancy may be growing normally,
adjusting to his or her genetic potential for growth
in stature-not faltering in growth.’25 On an
mdi-vidual basis, therefore, even serial measurement of
height may be difficult to interpret.
On a population basis or in a survey situation,
weight-for-age and height-for-age are used as
mea-sures of immediate and long-term nutritional status
in infants and children. Weight-for-age has a
num-ben of advantages: it is easier to measure and
inter-pret; children can lose weight but not height; and
significant increments can be measured over short
periods so that in the first weeks or months of life
significant growth failure can be detected earlier by changes in velocity of weight gain than by any other
measurement.95 Accurate age, which may be
diffi-cult to obtain in some developing countries, is nec-essary for interpreting weight-for-age and height-for-age growth data.
may be another, more subtle, indicator of nutni-tional status.21”#{176}”2#{176}Reports on supplemental
feed-ing programs for children have noted an apparent
disparity between the net increase in energy intake
and the observed growth response. The most logical
explanation for the apparent disparity between
in-take and the responding growth is that a substantial
part of the additional energy intake is applied to a
“de-adaptation” process, such as restoration of
basal metabolic rates toward normal and/or an
increase in physical activity probably expressed as
play.’2 Because physical activity was rarely
dis-cussed in the articles we reviewed that examined
infant-feeding practices, anthropometric
measure-ments of nutritional status (namely, weight-for-age,
sometimes height-for-age) were examined in this
report.
Issues in Interpretation
Although the techniques of growth
measure-ments for height and weight are relatively
straight-forward, interpreting adequate infant growth is
complex, depending on the growth reference and
the cutoffs that are chosen. For proper
interpreta-tion of infant growth data, a number of issues must
be considered, including: (1) choice of growth
ref-erences, (2) appropriateness of currently used
growth references for exclusively breast-fed infants, (3) growth of infants who are small for gestational
age, and (4) measurement of attained weight v
incremental weight gain.
Choice of References. Because growth in the first
few years of life under good environmental
circum-stances is very similar in different population
groups, comparing the growth of infants from
var-ious populations according to an international
ref-erence seems appropriate,53#{176} though there is not general agreement on this issue.
The Harvard references#{176} have been used by the
World Health Organization since 1966. However,
since the National Center for Health Statistics
(NCHS) references became available, WHO has
recommended the use of this reference population
for international growth comparisons.’TM The
growth chart prepared by WHO contains three
weight channels below the NCHS third percentile;
this makes it easier to evaluate growth performance
in infants who have low birth weight and those who
falter in growth to levels below the third percentile.
Specific advantages of the widely used NCHS
references are that they are based on recently
col-lected growth data (1960 to 1970), have large
num-bers of children (1,000 for each age group), and
more accurately define outer percentiles. However,
for the birth to 23-month age group, data were
provided by the Fels Institute and only 200 to 300
infants per age group were measured from 1929 to
1972; therefore, the advantages of the NCHS ref-erences do not apply to this age group.
The advantage of a single international reference is that it allows comparisons of data from different countries and different populations. Unfortunately,
comparing growth to a single reference was not
possible from data provided in the articles. The
Harvard, Iowa, 1959 United Kingdom,94 Denver,59
Tanner,’ and NCHS references were used in the
articles discussed in this report. The difference in
medians between these growth references can be
considerable; for example, weights for male infants
at 3 and at 6 months are 0.5 kg higher in the Iowa
references than in the NCHS weights.
Appropriateness of Available Growth References
for Breast-Fed Infants. All currently available
growth references are based on predominantly
for-mula-fed infants given early supplements. The
ear-lien references used for growth in the United
States-the Harvard references (longitudinal) and
the Iowa references (cross sectional) were based on
small numbers (<100) of healthy children from
upper social classes who were predominantly fed
cow’s milk or formula with the addition of solid
foods. The study population for the currently used
NCHS reference (Fels Institute growth data) for
infants was white, predominantly middle class, and
predominantly artificially fed in the early months. Bottle-fed infants who are introduced early to solid foods grow fasten than exclusively breast-fed
in-fants1#{176}#{176},127Neuman&#{176}#{176}found that bottle-fed
in-fants (who as a group had solid foods introduced at
1.9 months v 3.9 months for breast-fed infants)
doubled their birth weight earlier than breast-fed
infants. When their birth weight doubled, they had
gained disproportionately more weight than length
compared with breast-fed infants. However, when
low-solute formulas were used and solid foods were
introduced later, one study demonstrated similar
weight gains in breast-fed infants and formula-fed infants but higher weight gains in infants fed cow’s milk.’22
In 1974, Jelliffe and Gurney7’ stated that “until
recently it was widely considered that ‘the larger
the better’ or ‘the greater the growth, the healthier
the child.” This has been questioned by
many.48’#{176}”71”23”27”4’ Bottle-fed infants may be big-ger; it is not known whether this is “better.”
Because all currently available growth references
are based on predominantly bottle-fed infants who
were introduced early to solid foods, the use of
currently available charts for exclusively breast-fed
infants may not be appropriate.20’6’ No growth
charts are available for exclusively breast-fed
in-fants in the first 6 months. This is an extremely
in developing countries are still exclusively or
pre-dominantly breast-fed during these months.
Appropriateness of Growth References for Infants Who Are Small for Gestational Age. Infants who are
small for gestational age (SGA) (birth weight less
than tenth percentile for gestational age), which
implies intrauterine growth retardation, do not
at-tam the same weight-for-age as babies who have
the appropriate weight for gestational age. As
Mata9’ states, “As a group, young children tend to
remain in a track defined by birthweight and
ges-tational age: without knowledge of birthweight any
interpretation of growth in developing countries
becomes difficult.” This is particularly true in
de-veloping countries, where the percentage of
growth-retarded babies has been reported to be as high as
41%.138 Villar and Belizau’38 analyzed data on birth
weight and gestational age from 25 areas in
devel-oping countries and found a high correlation
be-tween the overall incidence of low birth weight
(2,500 g) and the incidence of intrauterine growth
retardation (r = .95, P < .001). Therefore, when the
incidence of low birth weight was greater than 10%,
it was almost exclusively caused by the increase in
intrauterine growth retardation, low birth weight;
the incidence of prematurity remained almost
un-changed. Because intrauterine growth retardation
is considerably underdiagnosed when only the
cri-tenon of weight for gestational age is used, it is
undoubtedly more common in developing countries
than is reported now.93
Studies30’39’87”#{176}5in developed countries indicate
that, as a group, SGA infants do not achieve
ex-pected weight and height even by 6 years. There
are two types of SGA infants described, however.
One group is disproportionately small, with normal
length (more than tenth percentile) and low weight (less than tenth percentile); this probably reflects growth retardation during the later weeks of intra-uterine life. The other group is proportionately
small (weight and length less than tenth
percent-ile), implying a genetically small individual or
chronic retardation during the entire last trimester,
as would occur, for example, in chronic maternal
undernutrition. The latter type of SGA has even
less potential for catch-up growth. Tables for
dis-tance and velocity growth (quarterly increments)
from birth through 3 years for 65 SGA infants
followed longitudinally in the United States are
available.30 From birth to 1 year, these SGA infants
had the same weight gain as infants whose size was
appropriate for gestational age (AGA), thus the
infants maintained their mean 1-kg weight
differ-ence at 12 months.3#{176}
No international growth references are available
for evaluating growth of SGA infants. Most studies
reviewed in developing countries were from
popu-lations of infants with low mean birth weights,
which have, undoubtedly, a high proportion of SGA
infants. Villar et al’39 describe proportionately
grown SGA infants as being twice as common as
disproportionately grown SGA infants in a study in
Guatemala. Because their weight cannot be
ex-pected to “catch up” to weight of AGA infants, the
use of currently available growth reference charts
to follow SGA infants’ attained weight-for-age is
cleanly inadequate.
Measurement of Attained Weight Versus
Incre-mental Weight Gain. Monthly incremental weight
gain (velocity) rather than attained weight has been
used to evaluate growth in the first 6 months.
Incremental weight gain has been advocated as a
more sensitive indicator of weight gain and as more
independent of birth weight than attained
weight.”3 A major problem in interpreting monthly
incremental weight gain, however, is that references
for monthly gains in weight are not available. The
NCHS references are based on measurements at
birth, and at 1, 3, and 6 months; values for other
months must be obtained by interpolation.
Incre-mental growth references must be derived from
longitudinal measurements, and they are presently
available only for 6-month increments for weight
and height”6 on yearly increments.’29
Roche and Himes”6 caution that incremental
charts are more sensitive than charts measuring
attained weight or length gain. For example, the
range from the 25th to the 75th percentile for
stature on the NCHS growth charts for 10-year-old
boys is about 16 cm; the corresponding range for
incremental stature is about 1.5 cm. Thus,
measur-ing weight or length accurately is more important.
In addition, children change “channels” for growth
increments much more commonly. Changing
chan-nels would be even more of a problem with monthly
increments. As Whitehead and Paul’49 aptly
com-ment, “Even if monthly incremental weight
refer-ences were available it may be difficult to interpret small deviations in growth velocity.”
In summary, although current growth references
are available for international comparisons of
growth in infancy, there are many unresolved issues
with their use. These include choice of appropriate
references, what is optimal as opposed to maximal
growth, and whether currently used references are appropriate for infants who are exclusively breast-fed and SGA infants.
Theoretical Calculations
Calculations based on estimated production or
consumption of human milk and energy and protein
requirements for normal infant growth are one way
TABLE 1. Theoretical Calculations: Age When Breast for Infants with Normal Birth Weight
Milk Provides Inadequate Energy
Author Volume in Energy
24-h (mL) Content (kcal/kg)
Growth Reference
Weight/Age When Breast Milk Provides Inadequate Energy
Thomson and Black’3#{176}(1965) 700 70
Naismith97 (1975) 970 71
Whitehead’ (1976) 850 78
Waterlow and Thomson146 752 70
(1979)
Zhi-chien’ (1981) 850 NS
Average* Normal* Average*
NCHSt 25%
NCHSt5O% NCHSnormal*
5.5 kg/4 mo 4 mo 5.0 kg/3 mo 5.65 kg/3-4 mo 2mo
3-4 mo
* Growth reference not further specified.
t NCHS, National Center for Health StatisticsY suffice as the infant’s sole source of food. Because
these calculations are based on numerous
assump-tions and do not take into account population or
individual variability, their validity must be
con-firmed by direct observation of infant growth
per-formance. However theoretical, these calculations
do provide useful supporting information.
Calcula-tions done for both normal and SGA infants are
discussed below.
Infants
with Normal
Birth Weight
Several authors have calculated the age when
breast-feeding alone becomes inadequate to meet
the theoretical requirements of the infant with
nor-mal birth weight. For most calculations, this age
varies between 3 and 4 months, depending on the
assumptions about breast milk volume, growth
ref-erence used, and desired percentile for growth;
es-timated energy content of milk; and estimated
re-quirements for protein and calories (Table 1).
Infants
Who Are Small for Gestational
Age
Villar and Belizan’37 calculated protein and
en-engy requirements for SGA infants of poorly
nour-ished mothers.’37 They estimated that breast milk
output provided only 69% of calculated protein
requirements at birth and 51% at 3 months. An
estimated 123% of energy requirements were
pro-vided at birth, decreasing to 55% at 3 months. The
reasons for the early inadequate energy and protein
requirements lie in the assumptions of the rapid
growth (30 g/d) of SGA infants and the relatively
poor breast milk volume (600 mL/d) and quality
(57 kcal/dL; 0.8 g of protein per deciliter).
The validity of the above calculations for infants
with normal birth weight and for SGA infants
depends on the validity of the assumptions. There
are problems with the assumptions used in these
calculations, however.
Estimates of Normal Protein Energy Needs.
World Health Organization/Food and Agricultural
Organization (WHO/FAO) estimates of energy and
protein needs for “normal” growth in infancy may
be too high.52”5#{176}These estimates were derived from observed intakes of bottle-fed infants in the United
States.4’ The 1973 WHO/FAO estimates of energy
and protein requirements have been used by all
authors with one exception: Zhi-chien Ho’58 used
lower estimates of 95 kcal/kg/d and 1.87 g protein! kg/d.
The WHO/FAO estimates for breast-fed infants
have recently been challenged by Whitehead and
Paul,’#{176}who studied energy intake from breast milk
and complementary foods in Cambridge infants
who had good growth performances as measured by
mean weight NCHS 50th percentile in the first
6 months. From these data, a multiple regression
analysis was used to predict human milk volumes
required for 5th, 50th, and 95th percentile growth.
The energy requirements predicted for the infant
in the 50th percentile were consistently 15% to 20%
lower than those recommended by WHO/FAO.
Daily predicted energy requirements per kilogram
of body weight for a male infant in the 50th
pen-centile were 104 kcal/kg at 2 months, compared
with the recommended 120 kcal/kg by WHO/FAO,
and 87 kcal/kg at 6 months, compared with the
recommended 110 kcal/kg.
When these energy predictions and a mean peak
volume of 720 mL as observed in The Gambia are
used, exclusive breast-feeding would be predicted
as adequate for the average-sized rural Gambian
boy and girl for 10 and 12 weeks, respectively.
Because these are the ages when decreasing growth
velocities are actually observed in these children,
Whitehead and Paul suggest that these predicted
human milk requirements for young infants may
prove a better guideline for evaluating adequacy. In
other words, WHO/FAO energy requirements for
growth in infancy may be 15% to 20% too high, at
least for infants in developed countries. Energy and
protein requirements for growth in infants living in
poor environmental conditions in developing
coun-tries with higher infection rates may be different
from those for infants studied in developed
coun-tries.
Individ-ual Requirements. The calculations assumed that
breast milk intake and individual requirements
were independent. It is possible that breast milk
intake may be influenced by the demands of the
infant; prolonged, vigorous sucking by a hungry
infant may lead to higher breast milk output.
Al-though this relationship seems intuitively
appeal-ing, the evidence for such a relationship is lacking.
As Waterlow and Thomson’46 phrased it,
“Unfon-tunately, since it is not feasible to measure the
requirements of an individual infant, objective
evi-dence on the relationship between requirement and
intake does not exist.”
Reference Standards for Growth. Reference
standards for growth that are based on bottle-fed
infants may be too high at 3 to 6 months for
breast-fed babies. This has been discussed previously
un-den “Growth References.”
Estimation of Milk Volume and Composition.
Ac-curate estimation of milk volume and composition
is difficult. Measurements of average, peak, 24-hour
breast milk volumes vary substantially both within
and between populations-from 500 mL in poor
Indian mothers5#{176}to 1,200 mL in healthy Australian
115
Problems with measurement of breast milk
out-put and issues in interpretation of these data,
es-pecially as they relate to maternal nutritional sta-tus, are discussed in the next section.
In summary, theoretical calculations generally
suggest that breast milk alone cannot supply
suffi-cient energy to provide for the normal growth of
infants with normal birth weight and size
appro-pniate for gestational age beyond 3 to 4 months of
age. However, the wide variations in measured
24-hour milk volumes make generalizations across
en-tire populations inappropriate. Most theoretical
calculations would indicate that a well-nourished
mother who produces 1,000 mL of milk per day can
fully breast-feed for 6 months, whereas another
mother with a maximum output of 600 mL can only
provide enough energy nutrients for growth for the
first 2 to 3 months. Because of the number of
assumptions used in these theoretical calculations,
many of which may be inaccurate, validation by
direct observation of the actual growth of the
breast-fed infant within a described setting is nec-essary.
Measurement of Breast Milk Output: Problems
and Issues
Many studies have measured milk volume, on
composition, or both among women in developed
and developing countries. Although these studies
provide useful supportive information, particularly
on the effect of maternal nutritional deprivation on
lactation, they cannot, by themselves, be used to
determine adequacy of breast-feeding. According to
Jelliffe and Jelliffe,
considerations of the volume and composition of breast milk in poorly nourished communities can only be made in relation to other ecological circumstances affecting both mother and infant. Differences, when they exist, may be related mainly to nutrition, to physical overwork and/or to environmental psychosocial stress [as well as other factors]. Variations in results in different studies are difficult to interpret, especially those of minor degree, because of dissimilarities in times and methods of sam-pling and analysis; in types and level of maternal under-nutrition; and in degrees of environmental psychosocial stress.
The volume of milk measured by different studies
varies widely between populations as well as
be-tween and within individuals of the same
popula-tion. Most studies report mean peak volumes of
milk during the first 6 months between 500 to 900
mL/24 h, although both higher and lower volumes
have been rtl7M.ms91o7l32l421s1 Recently,
mean values of 1,212 mL of milk per 24 hours (range
680 to 1,637 mL) have been reported in a select
group of highly motivated women who were fully
and partially breast-feeding; the women were
mem-bers of the Nursing Mothers Association of
Aus-tralia.”5 Many factors affect breast milk output
and its measurement. These include measurement
factors, infant and maternal ones, and external
conditions.
Measurement
Factors
Many factors relating to the method of
measure-ment can affect the assessment of volume and
composition of breast milk. The measurement of
milk output itself can affect milk volume by
stress-ing the mother and interfering with her let-down
reflex. The decrease in output can be dramatic. For
example, when Swedish mothers were hospitalized
to collect milk and other laboratory specimens,
their 24-hour milk output decreased 210 mL. In
some cases, investigators have interrupted the
in-fant’s normal feeding schedule from a
demand-feeding program to feeding at scheduled
inter-vals.7Co
Several methods have been used to measure
vol-ume: weighing the infant (or mother) before and
after each feeding, mechanical extraction, and
heavy water isotope dilution.2#{176} Differences exist
among the milk volumes measured by these
methods’#{176}”#{176};in addition, test-weighing infants after
ingestion of a known quantity of milk from a bottle
has demonstrated error, particularly in
demand-feeding situations, in which small quantities of
breast milk are delivered.’6”53 Some investigators
pe-nods, whereas others have estimated 24-hour vol-ume from a 12-hour observation peniod.#{176}”#{176}3”2’
Both composition and volume can be affected by
diurnal variation and stage of lactation.la22,m76bo3 In addition to diurnal variation, fat concentration is higher at the end of a feeding.42
The choice of laboratory test can also result in
different levels of some measured constituents. For
example, earlier laboratory methodology
overesti-mated protein content.ac
Infant and Maternal
Factors
Besides methods of measurement, many other
conditions influence the quality and quantity of
milk. Factors that influence the level of stimulation
needed to produce breast milk include the type of
feeding schedule (demand v rigid), infant health,
and gestational age (including birth weight, ability
to suck, and supplementation). Maternal
consider-ations include nutritional, health, and pregnancy
status; level of psychosocial stress; and drug inges-tion (particularly oral contraceptives). Only mater-nal nutritional status, because of its
interrelation-ship with infant nutrition and its importance in
developing countries, is discussed here.
The effect of maternal nutritional status on the
adequacy of lactation is well recognized as an
im-portant issue and has been the subject of several
comprehensive reviews.57’”55 Milk volume, and in
some cases milk composition (chiefly fat levels),
decrease with severe maternal undernutrition. The
effect of maternal nutritional status on
micronutni-ents varies depending on the micronutnient.69 The
threshold at which lactation is affected, the effects of specific types of nutritional deprivation, and the
effect of maternal dietary supplementation on milk
output, however, have not been determined.
The effect of maternal nutritional deprivation on
the adequacy of breast milk is probably a function
of both the past and present maternal nutritional
situation and the degree of deprivation. Wray’55
points out that the “failure to define or distinguish
clearly between maternal nutritional status and the
nutritional adequacy of the mother’s current diet is
characteristic of the literature.” The mother’s
abil-ity to lactate may depend on her nutritional status
before and during pregnancy, as well as during
lactation.’8”#{176}4”55 Longitudinal studies from The
Gambia suggest that dietary intake during
preg-nancy may affect lactation through the build-up of
fat stores.’#{176}”#{176}Milk fat concentration was found
to be correlated with subcutaneous fat deposits (P
< .01) rather than current dietary energy intake.’#{176}
Studies of maternal dietary supplementation
dur-ing pregnancy, lactation, or both have yielded
in-consistent results: milk volume increased with no
change in protein levels”36; milk volume increased,
but total protein content did not increase
commensurably22’51; no change in milk volume on
composition occurred after supplementation.51”#{176}
Conflicting conclusions may be the results of
sev-eral factors including difference in the timing of
supplementation (lactation, pregnancy, or both)
and level of supplementation of the mother, infant,
or both; base-line nutritional status and dietary
consumption of the population studied; and
differ-ences in study design. Because breast milk intake
is positively correlated with birth weight, it is
pos-sible that supplementation during pregnancy may
also increase breast milk intake through increasing birth weight.’52
External
Factors
Dramatic seasonal differences in milk volume
have been demonstrated in both The Gambia and
Kenya. In a longitudinal study1#{176}of 80 infants aged
1 to 18 months in The Gambia, the volume of milk
(2 to 6 months post partum) dropped from a peak
output of 850 g/d in the dry season to a minimum
value of 550 g/d in the wet season. During this time,
maternal food intake dropped from 1,736 kcal/d in
the dry season to 1,351 kcal/d in the wet season. In
addition, agriculturally related physical activity
in-creased. Similar seasonal differences have been
de-scnibed in Kenya.’32”33
In summary, because of methodologic differences
in collection and analysis, studies of milk obtained
from undernourished mothers in developing
coun-tries cannot be directly compared with studies from
well-nourished women in developed countries. In
addition, any differences observed in milk output
and composition between populations cannot be
attributed to differences in maternal nutritional
status without consideration of other factors known
to affect volume, such as differences in feeding
patterns (demand v scheduled feeding), infant
sup-plementation, birth weight, and level of maternal
psychosocial stress.
Studies on Growth Performance
The growth ofbreast-fed infants has been studied
in both developed and developing countries.
Infon-mation from the former is important in determining
how long exclusive breast-feeding can support
ad-equate growth under optimal conditions, ie,
healthy, well-nourished mothers and infants living
in a comparatively clean environment.
Developed
Countries
Waligren’s prospective studies”2 of healthy,
progress of their full-term, healthy, exclusively
breast-fed infants (n = 363) and found that
ade-quate growth was maintained for 6 months. Male
and female infants had mean weight at or above
the NCHS median from birth until 6 months of
age. No infants were studied after 6 months because
weaning usually started soon after that age.
Jackson et al did a retrospective longitudinal
study on diet and growth of “well born” American
infants. The group (n = 89) that was fed only breast
milk for 6 months, without additional solid foods,
had adequate gain in length compared with the
Iowa growth references. However, the gain in
weight was somewhat lower after 2 months for male
infants, and after 3 months for female infants. The
long-term growth implications of the lower weight
gain seen between 3 to 6 months is unclear, because
by 1 1 months the median weights of both sexes
were back to Iowa norms. In addition, the pattern
of lower weight gain between 3 to 6 months was
also seen in artificially fed infant boys. Therefore,
Jackson questioned the use of the Iowa references
for breast-fed and formula-fed babies because the
majority of infants used to construct these
refer-ences were artificially fed before low-solute infant
formulas were available and at a time when solid
foods were introduced early. He, therefore, inferred that the mean growth progress of the totally
breast-fed infants was adequate up to 6 months.
More recent studies of middle and upper
socio-economic status populations have also found
ade-quate growth in weight and length until 6 months
in most infants receiving breast milk alone.”920’6’ In a retrospective longitudinal study of 96 infants
of mothers in the La Leche League, mean weight
and length curves of exclusively breast-fed male
and female infants remained above the 50th
pen-centile of the NCHS reference through the sixth
month. The study population was highly select:
infants had a higher birth weight and length than
the NCHS population, and few experienced serious
illness; mothers were generally white, well
edu-cated, enthusiastic, and highly motivated. From 6
to 9 months, the height and length growth
perform-ance of exclusively breast-fed female infants was
not significantly different from the NCHS 50th
percentile (n = 10); but for exclusively breast-fed male infants, the growth in weight but not in length
was significantly slower (n = 8, P = .002). The
authors of that study, Ahn and MacLean’
acknowl-edge that the fact that weight-for-age curves crossed
successively lower percentile lines toward the end
of the 10-month period may indicate growing
in-sufficiency of human milk as the sole source of
nutrients.
Hitchcock et al6’ reported a prospective
longitu-dinal study of growth in selected low-risk infants
from middle-class families in Western Australia.
Weight gains in predominantly breast-fed infants
(n = 105) with no formula intake and a mean energy
intake of 150 kcal/24 h from other sources at 6
months were similar to United Kingdom growth
references (1959) from birth to 3 months. However,
from 3 to 6 months, the mean weight gain in both
sexes was 0.43 kg less than United Kingdom
refer-ences. Hitchcock et al attribute these differences to
a normal physiologic phenomenon rather than
growth faltering because both the infants and
mothers appeared healthy and well nourished.
In a prospective longitudinal study of 222 infants
who were exclusively breast-fed (white, middle and
upper socioeconomic status) from birth to 9
months, Chandra2#{176} found weight gain comparable
to the NCHS reference until 3 months but lower
from 3 to 6 months and from 6 to 9 months.
Although median birth weights were essentially the
same as those in the NCHS population, median
weights for these infants at 6 months were 0.44 kg
less for males and 0.41 kg less for females; at 9
months, they were 0.67 kg less for males and 0.58
kg less for females. Length was comparable at 9
months (median length 0.4 cm less for males, 0.1
cm more for females); statistical significance could not be calculated because insufficient information was provided.
Because breast-fed infants had significantly
fewer episodes of illness than bottle-fed infants and
because “reduction in illness was also seen in the
lower centiles of NCHS references,” Chandra
con-cluded that physical growth slightly less than the
NCHS references may be optimal for the
exclu-sively breast-fed infant. Unfortunately, important details about the study design (method of selection
of breast-feeding mothers and bottle-feeding
moth-ens, definition of exclusive breast-feeding and
bot-tle-feeding, and definition of some illnesses) were
not provided in this synopsis article. In addition, the “lower centile” levels at which breast-feeding
remains advantageous, the type of illness and the
degree of protection, and the temporal relation
be-tween illness and growth were not provided.
In an earlier study of a small number of infants
who were exclusively breast-fed (n = 36), Chandra’
reported that “growth faltering,” as defined by
weight-for-age at or below the tenth percentile
NCHS reference, occurred in three (8%) infants at
4 months, five (13%) at 5 months (P = .24), and
eight (22%) at 6 months (P = .01). Growth faltering was considered clinically significant because respi-ratory illness (P < .01) and otitis media (P < .01)
occurred more frequently (at statistically
signifi-cant levels) in infants who fell below the tenth
percentile for weight. The growth faltering was
versa because, in the majority of infants, growth faltering was stated to have occurred before clinical
infections; however, criteria for determining the
temporal relationship were not discussed. Birth
order and birth interval were similar in the two
groups of infants. The average volume of milk
in-gested at each month from ages 3 to 8 months was
similar in those with adequate and faltered growth,
implying differences in individual requirements.
Chandra concluded that a small proportion of
in-fants who were exclusively breast-fed may not
achieve adequate growth and should be given
sup-plementation after 4 months of age.
In summary, most studies from developed
coun-tries indicate that under optimal conditions, most
infants who are exclusively breast-fed grow
ade-quately for 6 months, although a somewhat lower
weight gain compared with some growth references
may be expected from 3 to 6 months. Successful
exclusive breast-feeding for more than 12 months
has also been reported.”5
Any group of infants shows variability in growth
rate. There will always be those at the upper and
lower centiles whose growth needs to be observed
more carefully and who may need dietary
modifi-cation. Case reports of serious failure to thrive
occurring in breast-fed infants less than 3 months
of age exist in the literature (especially from
pni-migravid mothers).31’47”#{176}’”7 The health
signifi-cance of mild growth faltering is uncertain. In a
small study of 36 infants, Chandra’9 found an
as-sociation with minor infections and growth less
than the tenth percentile of the NCHS growth
reference. In his study2#{176}of 222 breast-fed infants,
breast-fed infants had lower rates of illness than
bottle-fed infants. The reduction in illness was also
seen in the “lower centiles” of NCHS references;
however, “lower centiles” was not defined.
The appropriateness of current growth references
for infants who are exclusively breast-fed has been
questioned.20’6”#{176}’ Interpretation of growth in the
3-to 6-month period depends on many issues,
includ-ing choice of references and whether growth of
healthy breast-fed babies should be considered
op-timal. Many authors have advocated that growth
patterns of healthy, breast-fed infants should be
used for reference purposes for the period from
birth to 6 months for all infants.20’40’61”27
How applicable findings from these studies of
advantaged women in developed countries are to
the general population in developed
countries-much less to populations in developing
countries-is debatable. Apart from Hitchcock’s study,6’ the
infants studied were from a self-selected group of
highly motivated, healthy mothers who were able
to breast-feed successfully. The mother and infant
situation in developing countries is very different
from that in developed countries. Many women in
developing countries have been malnourished since
birth, have a much lower mean weight gain in
pregnancy, and produce lower-birth-weight babies.
Infants live in poor, crowded environments, often
without clean water or sanitary facilities. Unlike
breast-fed infants in developed countries, once
growth faltering occurs, catch-up growth is much
less likely to occur.
Developing
Countries
There are few reliable studies on growth
perform-ance of infants who are exclusively breast-fed
through the first 6 months in developing countries.
Although exclusive breast-feeding may be the
as-sumed practice, it is customary in most of these
communities to give small amounts of some
com-plementary foods, usually thin gruels. In some com-munities, prelacteal feedings rather than colostrum
are given before lactation is fully established.
Al-though these foods contribute negligible amounts
to the infant’s total energy intake, any foods given are certainly potential sources of infection through
contamination.9 Because the infant’s growth
pen-formance may also be affected by infection,
inter-pretation of the nutritional adequacy as measured
by growth performance of infants who are
exclu-sively breast-fed is difficult.
Study design may also limit interpretation. Many
studies follow a small number of infants, or do not
have representative samples of the populations for
which they provide inferences. The method for
selecting the sample may not be discussed. Most
studies do not provide information on birth weight,
which is a serious limitation; however, in developing
countries birth weight may be difficult to obtain.
Growth of SGA infants is not analyzed separately,
and the effect of the low mean birth weights on
attained mean weight-for-age is not addressed. To
study the temporal adequacy of breast milk requires
longitudinal studies; deaths should be studied
con-currently. Few longitudinal studies discussed
whether growth data on infants who died were
included up until the age of death.
Longitudinal Studies. Few longitudinal studies
were available for examining the growth pattern of
infants who were exclusively breast-fed for more
than 3 months; most examined the growth of
in-fants who were predominantly breast-fed who
ne-ceived complementary feedings. Lauber and
Reinhardt prospectively followed 19 infants
start-ing from age 1 to 3 months until 16 months in an
Ivory Coast rural community. Unlike infants in
other studies that we reviewed, most infants in this
community were exclusively breast-fed until 6
Mean weight-for-age was at or above 100% of the
Harvard median initially; it then slowly declined
from the fifth month onward and leveled off at 85%
of the Harvard Median at 10 months. Mean
height-for-age remained at 94% of the Harvard median
from 0 to 16 months. These researchers concluded
that satisfactory growth was achieved in these
in-fants until 5 to 6 months without supplementary
feeding.
In a longitudinal study from India, Gopalan#{176}
followed the growth of 14 infants who were
exclu-sively breast-fed for the first 6 months. Mothers
belonged to the poor socioeconomic group, and their
total daily calorie intake ranged from 1,500 to 1,850
calories between the fourth and sixth month of
lactation. The mean weight of the infants at 1 week
of age was 2,778 g and although the body weights
for age in the first 6 months were lower than the
Harvard median, Gopalan considered growth rates
satisfactory, as judged by the criterion of average
time to doubling of birth weight (on average at 20
weeks). But he observed that growth was
progres-sively more inadequate beyond the sixth month. He
concluded that breast milk alone was not able to
support growth at an adequate level beyond about
20 weeks.
Asha Bai et al5 described a longitudinal study in
Vellone, India, of 155 infants who were exclusively
breast-fed and were attending the “well infant”
clinic in the hospital where they had been born.
The mean weights of exclusively breast-fed male
infants remained at or above the Harvard median
until 28 weeks; then growth faltered relative to the
Harvard median. At 9 and 12 months, mean weights
were approximately 1 kg less. Starting with a larger
deficit at birth, the weights of female infants who
were exclusively breast-fed paralleled the Harvard
median only up to 16 weeks. In both sexes, heights
paralleled the Harvard median until approximately 28 weeks. The low percentage of follow-up (only
46% of the 155 breast-fed infants were measured at
6 months, 30% at 9 months, and 22% at 12 months)
limited the conclusions of this study.
Dempsey3’ analyzed data from a longitudinal
study done in Lahore, Pakistan, from 1962 to 1966.
The sample consisted of 300 births in a low-income
population in a defined urban and semiurban area.
Anthropometnic measurements were collected
within 1 week of birth and at 3, 6, 9, and 12 months
of age. Morbidity data were recorded by local
mid-wives who visited the homes every 2 weeks. Dietary
interviews in the form of 24-hour recalls were
con-ducted every ‘3 months on a selected group of
moth-ens with infants aged 6 months or older. (This is
not further defined.)
Infants were classified by method of feeding at
ages 3 and 6 months. Infants who were exclusively
breast-fed were those who relied solely on breast
milk for nourishment. Of the 176 infants for whom
adequate feeding histories were available, 92.6%
were breast-feeding at 6 months (though only 19.3%
exclusively), and at least 78% were still
breast-feeding at 9 months (though only 8% exclusively).
“Growth faltering” was defined as a decline over
a given 3-month period to a lower weight or length
percentile channel of the WHO growth curve. The
WHO standardized growth curve consists of NCHS
growth reference data adapted to enable classifica-tion of infants into three percentile categories below the tenth percentile, ten percentile categories up to
the 90th, and three categories above the 90th
pen-centile. This is the only study that reports growth
performance for infants who were exclusively
breast-fed by percentile channels at 3, 6, and 9
months relative to their birth percentiles.
For infants with birth weights greater than 2,500
g, mean weights-for-age and mean lengths-for-age
and their corresponding percentile channels were
presented by sex and method of feeding. Starting
with a mean birth weight of 3. 1 kg (30th percentile),
exclusively breast-fed male infants had mean
weights of 5.5 kg at 3 months (30th percentile) and
6.9 kg at 6 months (tenth to 20th percentile).
Ex-clusively breast-fed female infants with a mean
birth weight of 3.0 kg (30th percentile) had mean
weights of 5.2 kg at 3 months (40th percentile) and
6.1 kg at 6 months (tenth percentile). Thus, there
was faltering in weight gain between 3 and 6 months
in male and female infants who were exclusively
breast-fed, although at 6 months the number of
infants who were exclusively breast-fed was
small-16 males and nine females. There was a similar
faltering in length in both sexes from mean birth
lengths between the 40th and 50th percentiles,
which declined to the 20th to 30th percentiles at 6
months.
Data on growth for infants aged 9 and 12 months
were by classification of feeding at 6 months of age.
However, growth data were available for the small
number of male infants (n = 1 1) who were
exclu-sively breast-fed for 9 months. Starting with a mean
birth weight of 2.9 kg (20th percentile), these
in-fants showed more severe faltering in growth from
6 months (tenth to 20th percentile) to 9 months
(third percentile). The author concluded that in
this cohort of Pakistani infants, exclusive
breast-feeding beyond 3 months did not support growth
parallel to the WHO growth reference.
The follow-up of the 300 infants initially enrolled
in the study revealed that: (1) only 153 infants
(51%) had both relatively complete records on
feed-ing histories and birth anthropometry available; (2)
of the 137 infants with normal birth weight,
14
13
12
11
10
9
8
7
6
5
4
3
2
1
.
a)
g > 3000
2501 - 3000
2001 - 2500
K 2001
_t I
90% at 6 months, but only 66% at 9 months and
52% at 12 months. Whether the infants who
re-mained in the study were representative of the
sample or the community at each age group is not
discussed. The low follow-up, especially at later
ages, and the small numbers of infants who were
exclusively breast-fed at 6 months make
interpre-tation of the results of this study difficult.
Mata9’ collected longitudinal data on all 430
sin-gleton live births in the Guatemalan village of
Santa Maria Cauque from 1964 to 1972.
Breast-feeding was universal, and weaning usually began
at about 6 months. Supplementary foods
contnib-uted negligible amounts of energy or protein to the
diet before 6 months. However, small amounts were
introduced in some infants starting at 2 months of
age. The mean birth weight was 2,550 g; 32% of
infants were small for their gestational age. Iowa
15
standards were used for comparison of attained
weight and height. Overall weight-for-age
measure-ments paralleled the Iowa references until 3 to 4
months, but cohorts of infants by birth weight
showed varying levels of growth (Figure). Mata
interpreted these data as indicating that weight
faltering began from 3 months onward; however, if
he had used other growth references, the
interpre-tation may have been altered.
Progressively severe growth faltering occurred
from 6 months onward: weights-for-age for most
infants 18 months of age fell so far below the
Denver percentiles that at 18 months the majority
of children were below the 16th percentile (Table
2). The Denver references may be more appropriate
than the Iowa ones because Santa Maria Cauque is
situated 6,000 feet above sea level, similar to Den-yen’s altitude of 5,000 feet.
0 3 6 9 12 15 18 21 24 27 30 33 36
Age, months
Figure. Mean values and standard deviations of weights for cohorts of children defined
TABLE 2. Standards,
Cohort Children by Age and 1964_1972*
Percentiles of Denver Weight and Height
Age (mo) No. of
Cases
Denver Weight Percentiles
<3rd 3rd-lSth l6th-49th SOth-S3rd S4th-99th 100th
Birth 3 6 12 18 24 30 36 408 375 374 332 276 249 207 204 25 19 33 78 85 88 87 83 44 27 37 17 13 10 11 15 27 4 36 13 23 6 4 1 2 0 2 0 2 0 2 0 0 5 1 0 0 0 0 0 0 0 0 0 0 0 0 0
Denver Height Percentiles
<3rd 3rd-l5th l6th-49th 5Oth-S3rd S4th-99th 100th Birth 3 6 12 18 24 30 36 407 186 184 166 130 141 109 129 44 65 77 94 97 97 99 98 32 21 18 5 2 3 1 2 22 2 11 3 4 1 1 0 1 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0
* Adapted from Math.9’ Values shown are
and height percentiles.
Whitehead et al’5’ presented prospective
longi-tudinal data from infants born in a village in rural
Gambia whose mean birth weight ws 2.87 kg (85%
of the Harvard median). These infants
demon-strated an increase in percentile of weight-for-age
relative to the Harvard Median in the first 2 to 3
months; they returned at 5 to 6 months to
approx-imately the same percentage weight-for-age as at
birth (85%). By 12 months, weight-for-age was 75%
of the Harvard Median. In The Gambia,
breast-feeding is universal, but small amounts of
supple-mentary foods are introduced from 3 months on-ward.
One interpretation of this observed weight gain
in the first 6 months is that growth faltering occurs
at 3 months. Another is that the 3-month “normal,
expected” weight from the growth reference is too
low with respect to birth weight and the 6-month
target data. As Rowland et al”8 state, “If the
3-month growth reference figure were higher, the
Gambian children would follow, but not cross, a
lower percentile. For any individual, this could be
interpreted as normal growth rather than growth
faltering from 3 to 6 months.”
Zhichien1M studied all infants less than 1 year
old in a rural area in South China in a longitudinal
study. Although most infants were predominantly
breast-fed, half were receiving some complementary
food at 3 months. Mean birth weight for male
infants was 3.20 kg and for female infants 3.12 kg,
very similar to the NCHS references. Compared
with the NCHS reference, the Chinese infants had
a more rapid weight gain in the first 3 months. The
percentages under the specific Denver weight
mean weights for male and female infants crossed
below the respective NCHS medians at 4 months
for male infants and at 5#{189}months for female
infants. At 6 months, the mean weights for both
the male and female Chinese infants were 7.31 kg
and 7.01 kg, respectively, compared with NCHS
median weights of 7.85 kg for male infants and 7.21
kg for female infants.
Zhi-chien concluded that weight gain reaches a
plateau in the third month in this population and
that breast milk alone is not sufficient for growth after the first 4 months. It appears, though, that
the trajectories of weight gain are different from
those of the NCHS population; weight gains are
higher in the first 3 to 4 months. Therefore, another
interpretation is that breast milk supports normal
growth for 4 to 5 months in boys and up to 6 months in girls in this population. Other studies”#{176} have
noted that female infants who are exclusively or
predominantly breast-fed can grow adequately for
a longer period than male infants receiving breast
milk alone because of their lower growth velocity.
Khan77 studied infant-feeding practices
longitu-dinally in rural areas of Bangladesh (n = 401);
100% of the mothers breast-fed their babies at
birth, 98% at 12 months, and 85% at 2 years. The
median birth weight of these infants was 74% of
the Harvard median (ie, 2.5 kg) but at 1 year, their
median weight had decreased to 67% ofthe Harvard
reference. No weight-for-age data are provided at 3
to 6 months except those provided graphically.
Khan interpreted the growth pattern of those
months and deviating from the fourth month. He
concluded that breast-feeding alone was not
ade-quate to provide required nutrition to the children
after the third month of age without proper
supple-ments.
However, as discussed previously, it may not be
appropriate to expect the growth of a group of
infants with a median birth weight of 2.5 kg to
parallel the Harvard median when they start with
a birth weight less than the third percentile. It is
likely that a high percentage of these infants are
small for their gestational age. Khan’s findings that
the weight of children of heavier mothers was
higher at birth and that weight continued to be
higher through age 5 years (significance testing
could not be done on data provided) corroborates
this and highlights the interrelationship of
mater-nal and infant nutrition.
Supplementation in these infants, studied
monthly, was poor in quality and quantity. Khan
thus concluded that prolonged breast-feeding was
important in this community and that mothers
should be taught the nutritional values of locally
available food items and the proper time for
sup-plementation.
When Waterlow et al’44 pooled data from
longi-tudinal on semilongitudinal studies on growth in
the first 6 months of life in developing countries,
they reported that the monthly incremental weight
gain, which is considered to be independent of birth
weight, falls off substantially compared with 1959
United Kingdom references (obtained
longitudi-nally) between 3 and 4 months (Table 3). These
researchers suggested that the growth faltering in
these populations may be caused by inadequate
breast-feeding, infection, or both. They
acknowl-edged problems with the design of many of the
studies (small numbers and nonrepresentative
sam-ples) used in their report. In addition, exclusive
breast-feeding was not documented in most of the
studies.
That report has been the subject of much
discus-sion. It centers around interpreting the significance
of growth faltering, as measured by monthly
incne-TABLE 3. Monthly Increments in Weigh t in Firs t 6 Months of Life*
No. of
Children
Increments (kg/mo)
0-1 mo 1-2 mo 2-3 mo 3-4 mo 4-5 mo 5-6 mo Boys
Uganda 19 . . . 1.09 0.82 0.50 0.27
Tanzania 148 . . . 0.92 0.79 0.58 0.47 0.33
Egypt 6,738 0.78 0.82 0.69 0.71 0.39 0.52
India 32 0.52 0.65 0.55 0.61 0.45 0.44
New Guinea 189 0.80 1.02 0.94 0.67 0.43 0.37
St. Kitts 273 1.23 0.72 0.64 0.50 0.36 0.50
Nevis 82 . . . 0.78 0.63 0.55 0.45 0.68
Anguilla 47 . . . 0.68 0.64 0.59 0.41 0.64
Aborigines 212 0.96 1.11 0.84 0.65 0.48 0.40
Eskimos 84 . . . 0.70 1.10 0.80 0.50 0.50
Mean 0.86 0.82 0.79 0.65 0.44 0.46
UK mean’8 0.72 0.96 0.91 0.79 0.73 0.58
%ofUKmean 119% 86% 87% 82% 61% 80%
Boys and girls
Tanzania 90 1.13 0.79 0.88 0.48 0.27 0.32
South Africa 1,303 . . . 1.06 0.86 0.67 0.54 0.46
Nigeria 304 1.11 0.87 0.70 0.58 0.37 0.31
Gambia 68 0.83 0.89 0.88 0.41 0.27 0.42
India 14 . . . 0.70 0.45 0.53 0.51 ...
New Guinea
Western Highlands 30 . . . 0.82 0.63 0.31 0.17
Eastern Highlands(1963) 499 . . . 0.97 0.81 0.61 0.39 0.16
Eastern Highlands(1964) 101 . . . 0.63 0.61 0.63 0.32 0.39
Singapore 47 0.99 0.98 0.76 0.58 0.42 0.31
Mean 1.01 0.86 0.75 0.57 0.38 0.32
UK mean 0.67 0.91 0.84 0.76 0.70 0.59
%ofUKmean 151% 95% 89% 75% 54% 54%
* Data from Waterlow et al.’44 Data are from longitudinal or semilongitudinal surveys. In
mental weight gains, and the appropriateness of the 1959 United Kingdom references for predominantly
breast-fed infants and for monthly incremental
weights.27’6”23”49 Although birth weight data are
not given in the pooled studies of Waterlow et al,
the highest weight gain in the first month may
reflect “catch-up” growth in SGA infants. As
Cooper27 noted, at 4 months, when compared with
the United Kingdom growth reference, these
in-fants from developing countries had achieved the
same mean weight gain but had arrived there by a
different trajectory; their most rapid increase
oc-curred during the first month of life. The United
Kingdom references used by Waterlow as a
com-parison are higher than other references, especially in the first 4 months.’49
Interestingly, Whitehead and Paul combined
data from male infants who were exclusively or
predominantly breast-fed from four studies in
de-veloped countries; their growth was similar to that
of male infants in the pooled data of Waterlow et
al. These male infants gained 2.66 kg in the first 3
months and 1.61 kg from 3 to 6 months, compared
with 2.47 kg and 1.55 kg for the same quarters for
Waterlow’s combined male infants from low
socio-economic groups in developing countries.’49
The conclusion, therefore, must be either that (1)
this represents inadequate growth from 3 to 6
months in breast-fed infants in both developed and
developing countries or (2) current growth
refer-ences are too high; normal growth for breast-fed
babies may be somewhat lower.
Mean 3-month incremental weight data for
in-fants who were exclusively or predominantly
breast-fed were calculated, when possible, for
com-bined sexes from the longitudinal studies discussed
from developed and developing countries (Table 4).
It is notable that infants from low-income
Paki-stani families in Dempsey’s study had incremental
weight gains that were nearly identical with those
of Canadian infants from middle and upper
socio-economic levels in Chandra’s study and that, in
general, the incremental weight gained from birth
to 6 months was similar in breast-fed infants in
developed and developing countries (though infants
from developing countries often gain more weight
in the first 3 months).
Cross-sectional Studies. Cross-sectional studies to assess the association of breast-feeding with growth
have been common. These have been done in
Kenya,’33 China,’58 Iran,46 Uganda,’2’
Egypt, West Indies,6 Jordan,79 New Guinea,8”4
India,”4 Trinidad,70 Mexico,2’ and Indonesia.75
Be-cause cross-sectional studies examine cohorts of
survivors at each age-group at one point in time,
rather than a single cohort over a period of time,
conclusions about the temporal adequacy of breast
milk are limited. Often samples are nonrandom and
not community based. Secular trends and seasonal
variations are missed. Some studies determine the
method of feeding for each individual at the time
of the survey; others assume that the feeding
pat-tern of the study population is the same as that of
the community. Data on infant-feeding practices
may be ascertained by recall and may therefore be
inaccurate.
With these limitations in mind, the common
theme of most cross-sectional studies is progressive
deviation from growth references from 3, 4, 5, or 6
months onward but most marked in the second half
of the first year of life; inadequate supplementary foods are associated with this deviation.
Summary. From available studies, it is difficult
to assess when breast-feeding alone becomes
mad-equate to support normal growth in developing
countries. There are no published
community-based longitudinal studies evaluating growth in
in-fants who were exclusively breast-fed for the first
6 months of life. In Pakistan, infants who were
exclusively breast-fed and had birth weight greater
than 2,500 g showed mild faltering in growth
be-tween 3 and 6 months and more severe growth
faltering between 6 and 9 months in the small
subgroup of infants who were exclusively
breast-fed until age 9 months.33 In Guatemala,9’ The
Gam-bia,’5’ and Bangladesh,77 supplements may be
in-TABLE 4. Mean 3-Month Increments in Weight of Infants Who Were Predominantly
Breast-Fed Infants in First 6 Months of Life: Combined Sexes*
Study N <3 mo
(kg)
3 to <6 mo (kg)
Total for 6 mo (kg) Developed countries
Hitchcock et al6’ 105 2.35 1.71 4.06
Chandra’#{176}t 222 2.26 1.27 3.53
Developing countries
Mata9’ 432 2.65 1.23 3.88
Zhi-chien” 218 2.94 1.09 4.03
Waterlow et al’44 2,456 2.62 1.27 3.89
Dempsey3’ 71 2.31 1.24 3.55
