Context It has been suggested that breastfeeding is protective against children
becoming overweight, and that there is a dose-dependent effect of its duration.
Objective To determine whether breastfeeding and its duration are associated with
a reduced risk of being overweight among young children in the United States.
Design and Setting Data on infant feeding and child overweight status were taken from the
third National Health and Nutrition Examination Survey (NHANES III), a cross-sectional
health examination survey conducted from 1988-1994.
Subjects Sample of 2685 US-born children between the ages of 3 and 5 years, with
birth certificates, height and weight measures, and information on infant
feeding.
Main Outcome Measures A body mass index (BMI) between the 85th and 94th percentile was considered
at risk of overweight and a BMI in the 95th percentile or higher was considered
being overweight.
Results After adjusting for potential confounders, there was a reduced risk
of being at risk of overweight for ever breastfed children (adjusted odds
ratio [AOR], 0.63; 95% confidence interval [CI], 0.41-0.96) compared with
those never breastfed. There was no reduced risk of being overweight (AOR,
0.84; 95% CI, 0.62-1.13). There was no clear dose-dependent effect of the
duration of full breastfeeding on being at risk of overweight or overweight
and no threshold effect. The strongest predictor of child overweight status
was the mother's concurrent weight. The rate of children being overweight
nearly tripled with maternal overweight status (BMI, 25.0-29.9 kg/m2; AOR, 2.95; 95% CI, 1.35-6.42) and more than quadrupled with maternal
obesity status (BMI ≥30.0 kg/m2; AOR, 4.34; 95% CI, 2.50-7.54).
Conclusions There are inconsistent associations among breastfeeding, its duration,
and the risk of being overweight in young children. Breastfeeding continues
to be strongly recommended, but may not be as effective as moderating familial
factors, such as dietary habits and physical activity, in preventing children
from becoming overweight.
With rare exceptions, breast milk is the preferred feeding for infants
and confers unique immunologic, growth, and developmental benefits.1,2 Immunologic benefit and reduction in
risk for or severity of many acute and chronic diseases, including diarrhea,
lower respiratory tract infections, urinary tract infections, otitis media,
and asthma, have been associated with exclusive breastfeeding for at least
4 months.1-3 Shorter
and less intensive periods of breastfeeding may be less protective. Cognitive
developmental scores for infants who were fully breastfed for 6 months or
more are increased in comparison with those scores of infants who were never
breastfed.4
There is some suggestion that breastfeeding is also protective against
the development of overweight in young children and adolescents.5,6
If breastfeeding is protective against overweight in early childhood, the
explanation may lie less in inherent obesity-preventing properties of breast
milk than in the fact that breastfeeding displaces potentially more energy-dense
formula-feeding. In addition, the higher protein/nitrogen content of infant
formula compared with breast milk may cause a metabolic response of increased
insulin and insulin-like growth factor-1 secretion in formula-fed infants
leading to excessive weight gain, or there may be differences in the regulation
of intake of formula-fed infants compared with breastfed infants.
Any protective mechanism of breastfeeding is difficult to identify because
many of the same factors related to child growth and the development of overweight,
such as race/ethnicity, maternal education, maternal size, and birth weight,
are also related to the initiation and duration of breastfeeding or the decision
to formula-feed.7-11
Our objective was to determine if breastfeeding and its duration are associated
with a reduced risk of overweight in a nationally representative sample of
young US-born children.
Information on infant feeding and child overweight status were taken
from the National Health and Nutrition Examination Survey III (NHANES III),
a cross-sectional survey conducted by the National Center for Health Statistics/Centers
for Disease Control and Prevention (NCHS/CDC) from 1988-1994.12
As part of the stratified, multistage probability design, infants and children
from ages 2 to 71 months at interview, blacks, and Mexican-Americans were
oversampled. These analyses focus on young children, 3 to 5 years (36-71 months)
at interview, for whom retrospective information on infant feeding was obtained.
NHANES III included 3461 children, ages 3 to 5 years, and 94.1% (n = 3257)
were measured for height and weight.
Birth certificates were sought for US-born children ages 6 years or
younger.13-15
For these analyses, 2879 birth certificates (94% of US-born children ages
3-5 years) were linked to the NHANES III file. Variables taken from the birth
certificates included sex, birth plurality (singleton or twin), birth order,
birth weight (grams), and length of gestation (weeks). As in previous studies
using the linked file,10,13-15
gestational length from the mother's last menstrual period was examined for
completeness and validity16-18;
235 subjects (8.2%) were found to have missing or invalid length of gestation.
For those with valid gestational ages, preterm delivery was defined as less than 37 weeks and term
as 37 weeks or more.
Birth-weight categories were defined as low birth weight (<2500 g),
normal (2500-3999 g), and high birth weight (≥4000 g). Children with valid
gestational ages were categorized as small (<10th percentile of birth weight
for gestation), appropriate (10th-89th percentile), and large for gestational
age (≥90th percentile), using reference percentiles derived separately
for non-Hispanic white, non-Hispanic black, and Mexican-American singleton
infants.18 Infants of "other" races/ethnicities
were categorized using the reference for non-Hispanic whites.
Demographic and Maternal Characteristics
Race/ethnicity and region of residence were based on US Bureau of the
Census categories and definitions.12 The education
of the family reference person in NHANES III was used to represent household
education level. The following were taken from the questionnaire administered
to the child's parent or other adult caretaker in the home: mother's age at
the time of the child's birth, smoking during pregnancy, reported current
weight and height, and whether the infant received special neonatal care and
duration of that care. Sex was taken from NHANES III and checked for discrepancies
with the birth certificate. Mother's weight and height were converted into
a body mass index (BMI, kg/m2), except for 145 subjects who had
missing information. Maternal BMI was classified as underweight (< 18.5
kg/m2), normal weight (18.5-24.9 kg/m2), overweight
(25.0-29.9 kg/m2), and obese (≥30.0 kg/m2).19 In multivariate analyses, the underweight and normal
weight women were combined as the reference because only 88 women were classified
as underweight.
Questions on infant feeding practices included whether the child was
ever breastfed and the age (converted into months) when the child completely
stopped breastfeeding, was first fed formula daily, completely stopped drinking
formula, was first fed milk daily, and started eating solid foods daily.12 Infant feeding was defined based on the duration
(in months) that the children were fully breastfed (no liquids daily other
than breast milk or water). Infants who were partially breastfed (supplemented
daily with formula or milk) were no longer considered fully breastfed once
daily supplementation with formula or milk began. Feeding groups were classified
as never breastfed and fully breastfed for 2 months or less, 3 to 5 months,
6 to 8 months, and 9 months or more. Timing (in months) of the introduction
of solid foods was considered separately because timing of the introduction
of solids does not appear to alter growth and body composition in the first
year of life.20,21
Body weight and height were measured using standard anthropometric techniques.22,23 Body mass index was calculated, and
weight status was defined using BMI-for-age percentiles from the revised NCHS/CDC
growth charts.24 Body mass index and weight
status based on BMI-for-age were chosen as the primary dependent variables
because BMI is the worldwide standard for screening for overweight in children,
it is based on highly reliable measurements (height and weight), and even
in early childhood BMI is highly correlated with fatness.24-26
Twenty-nine children had missing heights or weights. Following current guidelines
for children and adolescents, a BMI between the 85th through 94th percentile
was considered "at risk of overweight" and at or above the 95th percentile
as overweight.24-26
Young children generally are not designated "obese," even at or above the
95th percentile of BMI-for-age, in the absence of clinical evaluation. The
95th percentile corresponds to a BMI of 30.0 or grade 2 obesity in adults.19
From the base sample of 2879 subjects with interview, examination, and
birth certificate data, 76 twins and triplets were excluded, as were cases
missing birth weight (n = 5), sex (n = 4), and infant feeding (n = 5). Twenty-nine
children born very low birth weight (<1500 g) were excluded because they
were not sufficiently mature at birth to initiate breastfeeding, and they
remained small through childhood. For the same reason, 75 children with extended
periods (≥2 weeks) of special neonatal care were excluded. The final analytic
sample was 2685 subjects.
Following NCHS/CDC analytic guidelines, statistical sample weights for
examined children were used (weighted) to account both for the oversampling
and unit nonresponse.27 Both nonresponse and
poststratification adjustments impose a great deal of heterogeneity into the
weights, and thus ignoring the sample weights in this case would have imposed
a bias in both the prevalence estimates and in the estimates of sampling error.
SUDAAN software, which incorporates the heterogeneity in survey weight
along with the clustering effects in survey design, was used for statistical
analysis and to estimate standard errors (SEs).28
The effect of duration of full breastfeeding (in months) on child BMI was
examined by multiple regression. The likelihood of being at risk of overweight
and overweight among fully breastfed as compared with never breastfed children
was estimated using the SUDAAN MULTILOG procedure. MULTILOG is an extension
of traditional logistic regression with the capability to model multiple level
outcomes. Using the MULTILOG procedure, odds and adjusted odds ratios for
at risk of overweight and overweight were estimated in the same model with
the normal BMI group (< 85th percentile) as the reference. Possible confounding
variables were selected for inclusion based on both forward selection and
backward deletion, with the decision to include or delete based on changes
in the significance and β values of the exposure effects (duration of
breastfeeding).29 In parallel, most analyses
were performed unweighted to confirm that the significance of the findings
was not affected by the variance estimates used to account for the sample
design. The unweighted results were not different and are not shown.
Characteristics of the Sample
Sample sizes and characteristics of the sample are given in Table 1. In terms of infant feeding, 46%
were never breastfed, nearly 25% were fully breastfed for 2 months or less,
and then approximately 10% were fully breastfed for 3 to 5 months, for 6 to
8 months, and for 9 months or more. The timing of introduction of solid foods
was consistent with the American Academy of Pediatrics recommendations for
infant feeding1 for 4 to 6 months for only
about half the sample.
BMI and Childhood Weight Status
Using weighted estimates, 11% of the US-born children were classified
as being at risk of overweight and 8.2% as overweight (Table 2). For females, but not for males, there was a trend toward
increasing overweight from ages 3 to 5 years.
Risk of Overweight by Duration of Full Breastfeeding
There were differences in full breastfeeding and its duration by key
demographic, maternal, and perinatal characteristics that were likely to be
associated with child BMI, and these were tested for inclusion in the multivariable
models (Table 3). Non-Hispanic
black infants were less likely to have been ever breastfed, while non-Hispanic
white and infants of "other" race/ethnicity were more likely to have been
breastfed longer. Only about 10% of non-Hispanic blacks continued full breastfeeding
for 3 months or longer, compared with 37% of non-Hispanic whites.
There were no differences in the duration of full breastfeeding by infant
sex. Moderately low birth weight infants (1500-2499 g) were less likely and
high birth weight infants more likely to have been breastfed. Infants who
were introduced to solids at the recommended age (4-6 months) were more likely
to have been breastfed, but infants for whom the introduction of solids was
delayed beyond 6 months were breastfed longer. Mother's concurrent BMI was
strongly related to infant feeding. Underweight mothers breastfed for a shorter
duration compared with normal weight mothers. Over 50% of overweight and obese
mothers did not breastfeed at all (Table
3).
There was a reduction in the prevalence of being at risk of overweight
if ever breastfed, although the reduction did not appear dose-dependent (Table 4). The reduction in risk was not
significant in unadjusted analyses (odds ratio [OR], 0.66; 95% confidence
interval [CI], 0.44-1.00), but there was a significant reduction in being
at risk of overweight associated with having ever been breastfed (AOR, 0.63;
95% CI, 0.41-0.96), adjusting for birth weight status, race/ethnicity, sex,
age group, mother's BMI status, and the timing of introduction of solid foods.
However, there was no clear dose-dependent effect of duration of full breastfeeding
(Table 4) nor was there a recognizable
threshold effect of breastfeeding. The AOR for being at risk of overweight
with full breastfeeding for 3 months or more was 0.67 (95% CI, 0.39-1.14),
indistinguishable from the AOR of 0.66 (95% CI, 0.34-1.29) for being at risk
of overweight with full breastfeeding for 6 months or more.
For overweight, there was no significant reduction in being overweight
with being ever breastfed either in unadjusted (OR, 0.81; 95% CI, 0.61-1.09)
or in adjusted analyses (AOR, 0.84; 95% CI, 0.62-1.13). As in the case of
being at risk of overweight, for overweight status there was neither a clear
dose-dependent effect with duration (Table
4) nor a threshold effect. The AOR of being overweight with full
breastfeeding for 3 months or more was 0.70 (95% CI, 0.39-1.25), again indistinguishable
from the AOR of 0.70 (95% CI, 0.37-1.32) for full breastfeeding for 6 months
or more.
The lack of strong association between duration of full breastfeeding
and child BMI was confirmed in a linear multiple regression model using duration
of full breastfeeding (in months) to predict child BMI, adjusting for the
race/ethnicity, sex, age group, birth weight status, mother's BMI, and timing
(in months) of introduction of solid foods. There was a slight reduction in
child BMI with duration of full breastfeeding (−0.02 ± 0.01 kg/m2 per month full breastfeeding), but it was not statistically significant
(P = .20).
However, there were factors that were significantly associated with
child overweight in the multiple logistic regression models. Compared with
non-Hispanic white children, Mexican-American children were at significantly
increased risk of overweight (AOR, 1.76; 95% CI, 1.05-2.94). The timing of
introduction of solid foods was associated with a 0.1% reduction in risk of
overweight (AOR, 0.9994; 95% CI, 0.9990-0.9997) for each month that the introduction
of solids was delayed (P<.001).
By far the strongest predictor of child BMI status was mother's concurrent
BMI (Table 5). Children were at
moderately increased risk for being at risk of overweight with an overweight
mother (AOR, 1.54; 95% CI, 0.93-2.57) but nearly 3 times more likely to be
at risk of overweight with maternal obesity (AOR, 2.97; 95% CI, 1.88-4.69).
Furthermore, overweight in early childhood was nearly 3-fold greater (AOR,
2.95; 95% CI, 1.35-6.42) with maternal overweight and more than 4-fold greater
(AOR, 4.34; 95% CI, 2.50-7.54) with maternal obesity.
We found a significant 37% reduction in being at risk of overweight
(BMI 85th-94th percentile) among children ever breastfed compared with those
who were never breastfed but only a 16% reduction in overweight (≥95th
percentile). There was no strong dose-dependent effect of the duration of
full breastfeeding on overweight status in early childhood, nor was there
an apparent threshold effect, that is, a reduction in risk with full breastfeeding
for 3 months or more or for 6 months or more. Children fully breastfed for
3 months or longer were at about a 30% decreased risk for overweight, but
the CIs for the estimates were wide and included unity. Duration of full breastfeeding
as an independent variable showed only a weak linear association with child
BMI.
Our results are in contrast to the findings of von Kries et al,5 who reported a clear dose-dependent effect for duration
of exclusive breastfeeding (defined as the child having been fed "no food"
other than breast milk) on the prevalence of "obesity" (>97th percentile for
BMI) in Bavarian children at ages 5 to 6 years. However, the current recommendation
is to allow supplementation with solids by 4 to 6 months, while continuing
full breastfeeding for 12 months or more. The findings of von Kries et al5 may be attributed to reverse causality, that is, the
Bavarian children who were exclusively breastfed for 6 months or longer were
smaller as infants, able to be nutritionally supported on breast milk alone
longer, and were therefore less likely to be at risk of overweight or to be
overweight in early childhood.
Our findings are less likely to be attributable to such reverse causality,
and the study has additional strengths. The nationally representative sample
of US-born young children is ethnically diverse, and the findings for breastfeeding
are consistent both with prevalence data and with demographic associations
reported in other national studies.7-9
Our conclusions therefore are less likely due to chance or sample bias, although
neither explanation can be totally ruled out. Having excluded infants born
weighing less than 1500 g or with extended periods (≥ 2 weeks) of special
neonatal care, we were able to adjust for the effects of both moderately low
(1500-2499 g) and high birth weight, since both have been shown to be associated
with early childhood growth in NHANES III.10,13-15
By not limiting our definition of breastfeeding to those exclusively breastfed
and allowing the introduction of solids at the recommended ages, we were better
able to determine if there were inherent overweight-preventing properties
of breastfeeding, as compared with lesser weight gain from a lower energy
intake.
Basing the duration of breastfeeding on mother's recall is a limitation
of this study. However, studies of the reliability of recalling infant feeding
mode and duration have shown that, if anything, more highly educated mothers
tend to overestimate the duration of full breastfeeding.2,30
This would have the effect of exaggerating the beneficial effects of breastfeeding
on child overweight since children born to more highly educated parents tend
to be healthier, better nourished, and leaner. It is unlikely, therefore,
that recall bias is masking an association between breastfeeding and early
childhood overweight.
We did find that factors other than infant feeding were associated with
child overweight, implying that the association between breastfeeding and
being at risk of overweight may be confounded by unmeasured sociodemographic
or intervening familial factors. Compared with non-Hispanic white children,
young Mexican-American children were at significantly increased risk of overweight,
a finding that has been reported previously for NHANES III.11,15
The timing of the introduction of solid foods was associated significantly
with a 0.1% reduction in risk of overweight for each month that introduction
of solids was delayed. For half of the sample, timing of introduction of solid
foods was consistent with American Academy of Pediatrics recommendations of
4 to 6 months.1 A further delay in introduction
of solid foods in infancy would appear to provide a statistically significant
but relatively minor reduction in risk for overweight at ages 3 to 5 years.
Mehta et al20 have reported that early (3-4
months), as compared with late (≥6 months), introduction of solid foods
did not affect infant growth or body composition in the first year of life
and concluded that early introduction of solid foods in infancy simply displaced
energy intake from liquid sources (breast milk or formula), rather than supplying
additional energy that would contribute to overweight.
By far the strongest predictor of BMI status in young children was mother's
concurrent BMI. Risk of overweight among young children was nearly tripled
with maternal overweight and more than quadrupled with mothers' obesity. The
overwhelming significance of the association between parental obesity and
overweight status in children younger than 5 years has also been demonstrated.31 It was shown that risk among children ages 3 to 5
years of subsequently becoming obese as adults was nearly tripled for those
with obese mothers compared with risk among children whose mothers were not
obese, although overweight in early childhood is not by itself a strong predictor
of adult obesity. The extent to which familial tendencies to obesity are genetic
or associated with shared dietary and activity habits has yet to be determined,
but it is unlikely that breastfeeding alone would be sufficient to prevent
the development of overweight in such a situation.
Our findings therefore agree with previous studies that have failed
to find an association between mode of infant feeding and body composition
in early childhood10,21 or overweight,
but have implicated maternal or parental obesity.32-35
For example, Baranowski et al32 reported for
246 children from 3 ethnic groups that no measure of infant feeding (breastfeeding
or duration) was associated with adiposity at 3 to 4 years of age. Likewise,
Zive et al33 found no relationship between
duration of breastfeeding and adiposity, as measured by BMI, for 331 children
at 4 years of age. However, as we found in this study, Zive et al33 found that mother's BMI explained the largest portion
of the variance in child fatness.
Our study is best compared with that of O'Callaghan et al34
who reported in a large study of 4062 children at age 5 years that birth weight,
paternal BMI, and sleeplessness at 6 months predicted risk of being at risk
of overweight (BMI 85th-94th percentile), while birth weight, being female,
and maternal and paternal BMI predicted increased risk of overweight (≥95th
percentile). On the other hand, whereas birth weight and parental BMI were
strongly associated with risk of overweight, breastfeeding and its duration
were not.34 We also found that a high birth
weight (≥4000 g) was associated with an increased risk of having a high
BMI in early childhood (>85th percentile), but the effect was diminished when
maternal BMI was considered.
Between infancy and ages 3 to 5 years, patterns of food consumption
and physical activity probably have more impact on weight status in early
childhood than infant feeding. Because the NHANES III is a cross-sectional
survey, no data are available to describe relevant behaviors during this intervening
period or to characterize the timing or relative weight level at which the
adiposity rebound may be occurring. Children who reach the nadir of their
BMI at ages younger than 6 years before it once again increases tend to be
at increased risk for overweight.36,37
A limitation of cross-sectional survey data is that the contribution of these
time-dependent patterns to the development of overweight cannot be evaluated.
Overweight in early childhood is a growing problem in the United States.
Recent findings from NHANES III (1988-1994), compared with earlier national
surveys,11,15 demonstrated that
children as young as 4 or 5 years, and especially females and Mexican-Americans,
show an increased prevalence of overweight. Mei et al38
have documented an increasing trend in overweight among low-income children
aged 5 years or younger who were included in the CDC Pediatric Nutrition Surveillance
System from 1983 to 1995. Consistent with our findings, Mei et al38 also observed that overweight prevalence was higher
for young females than for males, a trend that emerges as early as the preschool
years and persists into adulthood. In this context, the suggestion that breastfeeding
may be protective against the development of overweight in children5,6 has raised expectations that promoting
breastfeeding might help reverse this trend.
The findings from our analyses of US national survey data do not support
the contention that breastfeeding and its duration are necessarily protective
against early childhood overweight, although there is some conferred protection
from being at risk of overweight. However, maternal obesity (suggesting shared
familial dietary habits and activity patterns) far supersedes infant feeding
as a risk factor for being at risk of overweight or overweight in early childhood,
and the dose-dependent effect for duration of breastfeeding and risk for overweight
is inconsistent compared with that for maternal obesity. The finding that
overweight and obese mothers were less likely to have breastfed at all may
suggest a synergistic effect of maternal overweight status, combined with
the absence of breastfeeding, that results in increased risk for overweight
in the children of these mothers.
It cannot be too strongly emphasized that breastfeeding has numerous
attributes that render it the preferred feeding choice for almost all infants.
However, duration of full breastfeeding does not appear to be predictive of
or necessarily have preventive properties for overweight in early childhood,
and encouraging breastfeeding for overweight prevention would not be as effective
as moderating familial factors in preventing early childhood overweight.
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