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Unidad de Investigación Médica en Nutrición, Hospital de Pediatría, Centro Médico Nacional Siglo XXI, Instituto Mexicano del Seguro Social, Mexico, D.F.
1To whom correspondence should be addressed.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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KEY WORDS: • breast-feeding • weight • length • infection infant
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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, Howie et al. 1990
, Launer et al. 1990
, López-Alarcón et al. 1997
).
Other infections, such as otitis, urinary tract infection and
giardiasis, are also less frequent in infants fed human milk.
The role of breast-feeding in the growth of the recipient infants
has also been addressed widely. The growth pattern of infants fed human
milk differs from that of infants fed formula. BF infants are generally
leaner than formula-fed (FF) infants at 6 mo of age, mainly because
their weight gain is slower but their linear growth is not, as reported
by some authors (Dewey et al. 1992
, Roche et al. 1993
, Shepherd et al. 1988
). However, some other
authors have reported that linear growth is also slower in BF infants
than in FF infants (Hernández Beltran et al. 1996
, Nelson et al. 1989
, Owen et al.
1984, Salmenpera et al. 1985
, Vis et al. 1987
). Most of the studies failing to find negative
differences in linear growth have been conducted in developed
countries. Therefore, assessing the effect of environmental
determinants of growth, such as acute infections, was not pertinent in
those studies. Although studies conducted in BF infants born in less
favorable environments (Hernández Beltran et al. 1996
, Vis et al. 1987
) found length gain to be
significantly lower than WHO-NCHS references, which were
constructed basically with FF infants, the effect of infections was not
analyzed.
This study was conducted to test the hypothesis that breast-feeding prevents the negative effects of infections on the weight and length growth of the recipient infant reared in underprivileged environments. To reach this aim, we followed a sample of healthy, BF and FF infants from birth through 6 mo. A very close record of episodes of diarrhea and acute respiratory infections was included. Episodes were then related to the infants’ weight and length growth. The sample herein presented was selected from the same urban neighborhood in Mexico City aiming for a similar level of environmental microbial contamination among groups.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Subjects.
All infants recruited were born in a maternal and child care facility
(CIMIGen) serving a community located in a slum neighborhood in Mexico
City. Health care is provided in this center by practicing nurses under
the supervision of a physician. Well-child clinics are conducted on
the same basis. The general characteristics of the community have been
described previously (López-Alarcón et al. 1997
). Infants were enrolled consecutively at birth if they
were term, singleton, birth weight between 2500 to 4000 g
inclusive, and whose mothers were literate and agreed to participate in
the study. Infants with congenital malformations or neonatal diseases
were excluded from the study.
Study design.
All delivering women whose infants met the selection criteria completed a questionnaire concerning socioeconomic characteristics. Data about pregnancy outcome and parturition were collected from the hospital records before discharge. Thereafter, infants were examined and mothers were interviewed at 2-wk intervals, alternately at the clinic and at home for as long as 6 mo postpartum. Mothers missing one clinic appointment were visited at home. Three field nurses, previously trained, conducted the physical examinations, interviews and data recording.
Anthropometry.
The weight and length of the infants were obtained at 15-d intervals in
the clinic and at home visits, alternately. An electronic balance
(model 3862MP8; Sartorius, Gottingen, Germany) and a portable
length board (Holtain Limited, Crymych, United Kingdom) were used for
anthropometry following standard techniques. Intra- and interobserver
variability were assessed as recommended by Habicht (1974)
. The
assessment of birth weight and length was performed by the same trained
anthropometrists.
Morbidity.
Epidemiology of diarrhea and acute respiratory infections of the
infants in this sample and an ample description of the methods used to
collect that information were already described
(López-Alarcón et al. 1997
). In brief, all
the mothers were instructed to keep a 1-d grid for the 6-mo
follow-up period on which they recorded whether the infant was
healthy or ill on a daily basis. The mother checked, on a separate
grid, symptoms related to diarrhea and acute respiratory tract
infections whenever an infant became ill in her judgment. These records
were discussed with mothers at each interview. A physician blinded to
the feeding mode established the final diagnosis according to
preestablished definitions. Diarrhea was defined as the presence of
three or more liquid or semiliquid stools per day accompanied or not by
blood, mucus or fever. The total number had to exceed the usual number
of daily bowel movements. Acute respiratory infection was defined as
the presence of runny nose or cough for at least two consecutive days
plus one or more of the following signs: erythematous mucosa,
hoarse-cry, respiratory distress or fever. Personnel related to the
study did not treat, prescribe medicines or give any recommendations
regarding feeding practices to any member of the family.
Feeding practices.
The types of milk, other liquids and solids fed to the infant were
recorded at each interview. At the end of the 6-mo follow-up,
infants were classified as BF or FF, depending upon if from birth to 6
mo, they receive solely breast-milk or commercially available
infant formula, respectively, and as partially BF to those receiving
other sources of milk in addition to breast milk. To analyze duration
of lactation, infants were also classified according to the time they
received breast milk. Four categories were considered: those who never
received breast milk, infants who were BF from birth to 2 mo, infants
who were BF for 3 to 4 mo, and those who were BF for 5–6 mo. A 24-h
recall questionnaire was given to the mother by a trained nutritionist
1 mo after solid food was introduced, most of them at 4 mo of age. The
daily intake of energy and macronutrients from sources other than milk
was calculated by comparisons from local food composition tables
(Hernández et al. 1977
). Practicing nurses and
supervising pediatricians prescribed formula only when a mother freely
decided to do so, and after a careful explanation of the advantages of
breast-feeding. The prescription of formulas followed the policy of
the Hospital to recommend a daily intake of 410 kJ/kg body weight, but
compliance was not assessed. Commercially available infant formulas
were prescribed in all cases, and no powdered dry milk or other milk
was used as a breast-milk substitute.
Analytic design.
Comparisons of weight or length at birth and weight and length
increments at 6 mo of fully BF, partially BF and FF infants, were made
in those infants who completed the 6-mo follow-up and had at least
one anthropometric evaluation in every month. The effect of duration of
breast-feeding on the weight and length growth was assessed. For
that purpose, a multiple regression model was fixed by introducing the
cumulated 6-mo weight or length increments, alternately, as dependent
variables. The number and duration of episodes of diarrhea and acute
respiratory infections; the maternal and socioeconomic characteristics;
and the duration of lactation, as a dummy variable, were the
predictors. Interactions between breast-feeding and infections were
examined. Then, the effect of breast-feeding on growth was
dissected from the effect of diarrhea by stratifying infants into two
categories: those who never were ill with diarrhea and those who had
suffered at least one episode. Finally, the overall growth pattern of
these infants was compared to the WHO Working Group reference
(WHO 1994
), using NCHS Z-scores for weight- and
length-for-age.
To avoid the potential selectivity bias related to loss to follow-up, a second set of analysis was performed. Data from all the enrolled infants, including those who eventually dropped the study, were analyzed. Available body weight or length increments measured at 15-d intervals were regressed on age, feeding mode at the beginning of the interval, incidence and duration of diarrhea and acute respiratory infection, and the introduction of solid food recorded for that particular interval.
Statistical analysis.
Data were analyzed with Minitab Statistical Software, release 10 (Minitab 1994, State College, PA).
ANOVA was used to compare the body weight and length at birth, the increments of body weight and length at given ages and the Z-scores among groups, with an alpha level of 0.05. Multiple regression analyses were fixed for the association analysis. First, measurements of weight and length by age were fitted to a second-degree polynomial equation (Y = b0 + b1 age in months + b2 age2 in months) to describe individual growth patterns; predictions of weight and length at fixed ages were used for subsequent analyses. The 6-mo increments of weight and length were regressed on incidence and prevalence of diarrhea and acute respiratory infection; maternal age education, and previous parity; the number of people sleeping in the same room (crowding); and two levels of socioeconomic status: those who had availability of refrigerator, paved floor, sewage and piped water at individual households, and those who did not have all these assets. Duration of lactation was introduced to the model as a dummy variable with three levels: i) those who never received breast milk, ii) those BF from birth to 2 mo and iii) those BF for 3 to 4 mo. To avoid collinearity, the number of episodes and the number of days ill with diarrhea or acute respiratory infection were analyzed separately.
Two models were fitted for the stratified analysis. In the first model, the 6-mo weight or length increments of subjects who never experienced diarrhea were regressed on birth weight or length, the type of feeding, the maternal and household characteristics and the number of days ill with acute respiratory infection. In the second model, the weight or length increments of infants who presented at least one episode of diarrhea were regressed on the predictors mentioned above plus the number of episodes with diarrhea.
For the second model, body weight and length increments measured at each 15-d interval were regressed on the incidence and duration of diarrhea and acute respiratory infections, and the feeding pattern at the beginning of the interval. The introduction of solids at that interval was analyzed as a covariate.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Characteristics of the mothers and households of the infants,
stratified by feeding mode, are presented in Table 1
; data from infants who did not complete the follow-up are included.
Basically, formula-feeding mothers were older, and a higher
percentage of their households had sewage removal, than those of women
who BF their infants. Except for the lower percentage of households
with paved floors, the characteristics of the subjects who abandoned
the study were not different from those who completed the follow-up.
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The infants (90%) were fully BF at hospital discharge which occurs, at
the latest, 24 h after delivering. At the first interview (15 d
postpartum), 31% of the infants were already receiving formula, but
the maternal decision to switch to formula was not based on the
perception of poor growth of their infants. Further, at age 15 d
the mean body weight was similar in breast-fed and solely FF
infants, and increments were significantly higher in infants fed
formula (105.9 ± 51.5 g/15 d) than in BF infants (17.7 ± 21.5 g/15 d, P < 0.02). The prevalence of
breast-feeding fell to 25% at 6 mo, in such a way that only 41
infants were BF, and 53 were FF for the entire 6-mo period. None of
these FF infants received cow’s milk or powdered dry milk. An estimate
of the daily energy intake from sources other than milk was made 1 mo
after the onset of solids in the diet of each individual infant. The
mean energy and protein intake from sources other than milk were not
different between feeding groups. Fifty percentage of the FF and 40%
of the BF infants (P = 0.63) who were introduced to
complementary foods consumed at least 15 g/d of food from animal
sources (mostly chicken meat, chicken liver and egg yolk). By 2 mo of
age, a small number of infants had been exposed to solid food, but at 4
mo 86% of them were consuming variable amounts of solids (Fig. 1
). From those infants who did not receive solids at that age, 43% were
BF, and 43% FF.
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BF infants had a lower frequency of diarrhea and acute respiratory
infections (ARI), and shorter episodes of both diarrhea and ARI
than FF infants. Partially BF infants had intermediate frequencies and
duration of episodes of disease (Table 2
). Further details about the relationships among feeding mode and
incidence and prevalence of acute infections in this sample were
published elsewhere (López-Alarcón et al. 1997
).
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The mean birth weight and length of the three feeding mode categories
were not different. However, fully BF infants were heavier at 6 mo than
infants fed formula. Attained length at 6 mo was not different among
groups, but a trend for infants to be taller (P
= 0.1) in the BF group was observed (Table 2)
.
Relative to NCHS values, weight for age of FF infants fell from -0.22
Z-score at birth to almost -1 Z-score at 6 mo of age. On the
contrary, fully BF infants improved from -0.15 at birth to 0.23 at 3
mo, but fell again to -0.20 at 6 mo of age. Differences between FF and
BF infants were significant at 3 and 6 mo (P = 0.007 and 0.02, respectively) (Fig. 2A
). Similarly, the mean length for age Z-score of
fully BF and FF infants was not different at birth, but a trend to
improve was evident for fully BF infants. In contrast, infants fed
formula declined to a Z-score of -0.94 at 3 mo, and to -1.3 at 6,
but differences were not significant (P = 0.17)
(Fig. 2B
). The growth pattern of these Mexican infants
was also compared to a sample of healthy BF infants reared in better
socioeconomic conditions in the United States and Europe (WHO 1994
). The mean weight for age at birth of the American and
European infants was 0.5 Z-scores of NCHS, well above the mean
weight for age of the Mexican BF and FF infants. At 6 mo, they fell to
the 0.10 Z-score of NCHS, very close to the weight for age attained
by the Mexican BF infants, but far above the weight for age of the
Mexican infants fed formula. The mean length for age of the American
and European BF infants at 1 mo was 0.2 Z-scores of the NCHS
reference. At 6 mo of age, there was no difference between the mean
length for age Z-scores of the WHO Working Group and the Mexican BF
infants (-0.10). The difference between the length-for-age of
the latter groups and that of the Mexican infants fed formula was about
-1 Z-score (Fig. 1A
and B
).
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).
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. Weight and length of both, some-time-ill with diarrhea and
never-ill with diarrhea infants were not different at birth, but
the cumulated 6-mo increments were higher for those infants who never
were ill, resulting in heavier and taller infants. Weight and length
Z-scores of never ill and some-time-ill infants were not different
at birth, but at 6 mo of age Z-scores of weight and length were
significantly higher for those infants who never were ill.
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). Although breast-feeding was not associated with length gain of
those some-time-ill infants, removing this variable from the model
importantly diminished the value of the
R2.
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. Fifteen-day weight increments were positively related to age and
breast-feeding, and negatively to the introduction of solids, but
reverse causality can not be ruled out. The presence of diarrhea was
negatively associated to increments in weight only in FF infants.
Therefore, if an infant suffered one episode of diarrhea and received
formula, it lost 100 g more than a BF infant that suffered
diarrhea (P < 0.05). Length increments were also
positively related to age and breast-feeding. This was not due to
the introduction of solids or to the presence of diarrhea or acute
respiratory infection. Interaction between breast-feeding and
infections was not related to length gain (P = 0.55).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Based on the fact that mean weight and length and their associated variances for the two feeding mode groups were not different at birth, we inferred that factors negatively affecting their prenatal growth were homogeneously distributed. Therefore, the difference in postnatal growth between groups is assumed to be due to environmental factors: nutrition and acute infections.
Attained lengths of BF, partially breast-fed and formula-fed infants were not significantly different at 6 mo. The power available to find differences between the three groups was of 65%; to detect differences with a power of 80%, the sample size should be of 71 infants per group.
Compared to a set of BF infants reared in the United States and Europe, these two groups of Mexican BF and FF infants had lower weights at birth. The BF infants grew more rapidly than their American and European counterparts during the first 3 mo, so that, by the age of 6 mo, neither weight nor length was different than those of the American infants. In contrast, the Mexican FF infants grew more slowly, particularly during the first 3 mo of life and did not recover by 6 mo. At this age, they were clearly faltering, since 32% of them were below two standard deviations relative to NCHS reference values, compared to only 8% of their BF counterparts.
The difference between the growth patterns of BF and FF infants is likely due to either different energy intake or different energy expenditure. We did not find differences between feeding groups in the timing of introduction of solids, the energy and protein intakes from food other than milk or in the percentage of infants consuming food from animal sources. We did not assess the energy intake from milk, so that the possibility of mothers or caregivers diluting formula inappropriately, or limiting intake by presenting infants with inadequately low volumes of milk can not be ruled out. However, the growth of never-ill, FF infants was comparable to that of never-ill BF infants, suggesting that the quantity of formula consumed did not determine the differences in the overall growth.
The incidence and prevalence of diarrhea were greater in FF infants
than in BF infants: almost doubled that of BF infants. The overall
growth performance was negatively associated with the number of
episodes with diarrhea, but it was less negative in BF infants.
Moreover, duration of breast-feeding offset the detrimental effect
of infections on growth in a dose-response fashion: i.e., infants
who never received breast milk for the entire 6-mo period were 549 g lighter and 1.10 cm shorter than infants fed formula for the same
period (Table 3)
. Besides, breast-feeding protected the weight gain
of those infants who became ill but had no effect on those who never
were ill. Similarly, socioeconomic status was related to the growth of
some-time-ill infants, but not those who never suffered diarrhea (Table 5)
. We believe that the intake of nutrients from formula of these
infants was barely sufficient to support their growth if they were
healthy. However, when facing higher nutrient demands because of acute
infections, an increase due in milk intake might be blunted by
infection-induced anorexia and the lack of perception of caregivers
of the need for more milk. Furthermore, in these societies, formula may
be intentionally diluted when an episode of infection is present
(Mata et al. 1977
). It has also been suggested that
illness-induced anorexia is lower in BF infants than in FF infants
(Brown et al. 1990
, Hoyle et al. 1980
.
According to Lutter and coworkers (1992), there is a synergistic effect of infections and inadequate energy intake on the nutritional status of infants. We found a multiplicative effect between breast-feeding and infection on 15-d weight increments, but not on the cumulative 6-mo weight gain. The latter suggests that the intake of energy might be inadequate during infections but not in the long term.
The negative effect of diarrhea on length increments seen in the
analysis of cumulative 6-mo growth is in apparent contradiction to the
analysis of the growth by 15-d increments where length was not affected
by diarrhea. The lack of effect of infections on length gain at 15-d
intervals may be explained by the observation of Lampl et al. (1992)
on
the episodic pattern of linear growth. Linear growth remains static for
days, but eventually it will present a "saltation." Saltation
periods are less frequent when infections or shortage of energy occur.
Therefore, these 15-d periods of observation may be an insufficient
window to identify them, but in the long term, a reduction in the
expected stature is easier to detect (Frongillo 1999
).
In the stratified analysis, we compared the growth of infants who were
BF or FF for the entire 6-mo period. The selected FF infants were not
switched from breast-feeding to formula-feeding because they
were not growing well, avoiding reverse causality (Victora et al. 1998
). In addition, the potential selectivity bias related
to loss to follow-up was avoided by relating the available 15-d
growth increments of all the infants included in the study to several
potential confounders. This analysis included infants until the last
moment they remained in the study, and none of them abandoned the study
because of death, illness or because they were not growing well.
Birth length was a strong negative predictor of the 6-mo length gain in
such a way that those infants who were born smaller presented higher
increments in length, suggesting an effect of regression to the mean.
Therefore, in a separate analysis (not shown) we regressed the
residuals of length-for-age as the dependent variable on the predictors
included in the analysis described in this study, to control for the
effects of the birth length (Esrey et al. 1990
).
Conclusions were not different from those herein presented.
In summary, we present evidence that BF infants reared in underprivileged environments grow better than those infants fed with formula. Such a difference in growth may be related to the preventive effect of breast milk against acute infections which, in turn, impacts negatively on growth performance. We speculate that this effect of breast-feeding on growth may result not only from less frequent episodes of infection, but also from a more adequate energy intake because infection-induced anorexia is lower in BF infants. Further studies of differences in appetite and food consumption through episodes of acute infections compared by feeding mode are in order, placing particular emphasis on the degree of exclusivity of breast-feeding.
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FOOTNOTES |
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Manuscript received June 23, 1999. Initial review completed July 2, 1999. Revision accepted November 3, 1999.
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