Context A number of studies suggest a positive association between breastfeeding
and cognitive development in early and middle childhood. However, the only
previous study that investigated the relationship between breastfeeding and
intelligence in adults had several methodological shortcomings.
Objective To determine the association between duration of infant breastfeeding
and intelligence in young adulthood.
Design, Setting, and Participants Prospective longitudinal birth cohort study conducted in a sample of
973 men and women and a sample of 2280 men, all of whom were born in Copenhagen,
Denmark, between October 1959 and December 1961. The samples were divided
into 5 categories based on duration of breastfeeding, as assessed by physician
interview with mothers at a 1-year examination.
Main Outcome Measures Intelligence, assessed using the Wechsler Adult Intelligence Scale (WAIS)
at a mean age of 27.2 years in the mixed-sex sample and the Børge Priens
Prøve (BPP) test at a mean age of 18.7 years in the all-male sample.
Thirteen potential confounders were included as covariates: parental social
status and education; single mother status; mother's height, age, and weight
gain during pregnancy and cigarette consumption during the third trimester;
number of pregnancies; estimated gestational age; birth weight; birth length;
and indexes of pregnancy and delivery complications.
Results Duration of breastfeeding was associated with significantly higher scores
on the Verbal, Performance, and Full Scale WAIS IQs. With regression adjustment
for potential confounding factors, the mean Full Scale WAIS IQs were 99.4,
101.7, 102.3, 106.0, and 104.0 for breastfeeding durations of less than 1
month, 2 to 3 months, 4 to 6 months, 7 to 9 months, and more than 9 months,
respectively (P = .003 for overall F test). The corresponding
mean scores on the BPP were 38.0, 39.2, 39.9, 40.1, and 40.1 (P = .01 for overall F test).
Conclusion Independent of a wide range of possible confounding factors, a significant
positive association between duration of breastfeeding and intelligence was
observed in 2 independent samples of young adults, assessed with 2 different
intelligence tests.
A number of studies have suggested a positive association between breastfeeding
and cognitive and intellectual development in early and middle childhood.1,2 However, studies of correlations between
childhood and adult intelligence show that intelligence is quite unstable
during the first decade of life, particularly in early childhood.3 Consequently, it is possible that exclusively or predominantly
bottlefed children may catch up and ultimately achieve the same intelligence
level as children who were breastfed.
Few studies have examined the relationship between breastfeeding and
intellectual development in older children and adolescents. One study observed
significantly higher scores in breastfed children at 15 years of age on tests
of nonverbal ability, mathematics, and reading ability,4
and another study demonstrated a positive association between breastfeeding
and high school attainment at 18 years of age.5
The latter study also demonstrated an apparent dose-response relationship
between duration of breastfeeding and scores on intelligence tests (at ages
8 and 9 years) and on standardized tests of reading and mathematics (at ages
8, 10, 12, and 13 years). These studies—and most others assessing cognitive
ability in childhood—included a number of demographic, family, and perinatal
factors as covariates. Despite the fact that controlling for these factors
generally resulted in diminution of the effect, the positive association of
breastfeeding with various measures of cognitive function remained significant
and thus appeared robust.
There has only been one investigation of the relationship between breastfeeding
and intelligence in adults.6 In that study,
a significant association between breastfeeding and scores on a computerized
test of logical, verbal, and arithmetic reasoning was observed. However, when
family and perinatal factors were included in a regression model, the association
lost significance. This finding has been interpreted as strong evidence against
a causal relationship between breastfeeding and long-term intellectual development7 despite the study's methodological weaknesses, which
included the following: (1) feeding methods were assessed roughly in 3 categories
(breastfed, bottlefed, and combined feeding, with 658 breastfed infants and
only 53 bottlefed infants); (2) family information, including data on father's
occupational class, was collected retrospectively from participants born between
1920 and 1930 (ie, 60-70 years later); (3) neither mean age nor variation
in age at the time of intelligence testing was reported, but apparently the
majority of participants were in their 60s or 70s. This means that the results
may have been affected by individual differences in age-related decline in
cognitive function or neurological diseases,8
thus weakening the possible association between breastfeeding and adult intelligence.
In an effort to overcome difficulties of interpreting previous studies,
we describe the association between duration of breastfeeding and adult intelligence,
applying 2 different intelligence measures, in 2 nonoverlapping samples from
a perinatal cohort with a wide range of potentially confounding variables
collected prospectively. In both samples, intelligence was assessed in young
adulthood, an age when cognitive functioning is optimal and intelligence test
scores are highly stable.
The Copenhagen Perinatal Cohort
The Copenhagen Perinatal Cohort comprises 9125 individuals born at the
Copenhagen University Hospital between October 1959 and December 1961. When
the cohort was established, demographic, socioeconomic, prenatal, and postnatal
medical data were recorded prospectively during pregnancy, at delivery, and
at a 1-year examination.9 Information on duration
of breastfeeding was collected by a physician who interviewed the mothers
at the 1-year examination. The mothers were asked both about duration of exclusive
breastfeeding and about total duration of breastfeeding, but 2 out of 3 mothers
in the cohort gave the same answer to these 2 questions. It is possible that
the mothers distinctly remembered when they completely stopped breastfeeding,
but less clearly when they started to supplement breast milk. It was not possible
therefore to make a detailed analysis of exclusive breastfeeding vs total
duration of breastfeeding, but a preliminary analysis showed no significant
intelligence differences between subsamples of infants who were exclusively
breastfed vs partially breastfed. Consequently, unless otherwise specified,
duration of breastfeeding refers to total duration of any breastfeeding.
Wechsler Adult Intelligence Scale Sample
A subsample from the Perinatal Cohort participated in an ongoing research
program between 1982-1994 that focused on the developmental effects of prenatal
and perinatal factors, in particular the effects of prenatal exposure to prescribed
maternal medications.10 On the basis of perinatal
records, 1575 potential subjects were contacted, and 1155 (73%) completed
the Danish version of the Wechsler Adult Intelligence Scale (WAIS).11 Information on duration of breastfeeding was available
for 1001 (87%) potential subjects, but 28 twins were excluded (see below).
The final sample included 973 singletons (490 males and 483 females), with
a mean assessment age of 27.2 years (SD = 4.4; range, 20-34 years). Of the
remaining 602 contacted individuals, information on duration of breastfeeding
was only available for 399 potential subjects. The distribution of duration
of breastfeeding was nearly identical in these 399 subjects and in the 973
subjects included in the final sample. The mean parental social status score
of the final WAIS sample was slightly, but significantly, higher than the
score of the remaining contacted subjects, but otherwise there were no significant
differences with respect to the covariates included in the study (Table 1).
The WAIS generates 3 IQ scores: Verbal, Performance, and Full Scale
IQs (in this study, derived from Danish test norms). It was individually administered
by 3 psychologists who were all completely blind to the subjects' breastfeeding
status and other prenatal and perinatal information.
Børge Priens Prøve Sample
As part of the same research program,10
draft records were located for 3773 male members of the cohort. With the exception
of individuals with disqualifying diseases (eg, epilepsy and diabetes) and
individuals who volunteer for military service at an earlier age, all Danish
males are required to appear before the draft board at 18 years of age. (Only
a little over 5% of Danish males do not appear.)12
The Danish military draft board administers an intelligence test, the
Børge Priens Prøve (BPP), a 45-minute group test with 4 subtests
(letter matrices, verbal analogies, number series, and geometric figures)
and a total score ranging from 0 to 78. This total score has a correlation
of 0.82 with the Full Scale WAIS IQ, indicating that the BPP is closely related
to standard measures of general intelligence.13
Of the 4668 males in the Perinatal Cohort, 77% (4279) survived the first
4 weeks of life. The BPP scores were available for 3306 of these, but 501
singletons were excluded to avoid overlap with the WAIS sample; in addition,
76 twins were excluded. Information on duration of breastfeeding was available
for 2280 (84%) of the remaining 2729 individuals. Thus, the final BPP sample
comprised 2280 singleton males who appeared before the draft board at the
mean age of 18.7 years (SD, 1.2; range, 17-26 years). The sample represents
69% of the 3306 males with BPP scores. The distribution of duration of breastfeeding
was almost identical for this sample and for the 1283 males for whom information
on duration of breastfeeding was available, but who because of lack of a BPP
score, overlap with the WAIS sample, or twin status were excluded. However,
on several of the covariates in this study, the BPP sample differed significantly
from the excluded males of the Perinatal Cohort who survived the first 4 weeks
of life. The BPP sample had higher mean scores on gestational age, birth weight,
and birth length and lower mean scores on parental social status and the indexes
of pregnancy and delivery complications. In general, these differences were
small: eg, for gestational age, 0.2 week; for birth weight, 55 g; and for
birth length, 0.3 cm (Table 1).
Twins were excluded because relationships between some of the covariates
and adult intelligence may be different in twins and singletons (eg, associations
between adult intelligence and birth weight and length) and because data for
twin pairs are not statistically independent. Twin pairs only comprised a
small fraction of the 2 samples, and when analyses were conducted on samples
that included twins, the results are essentially the same as those presented
in Table 3.
Exclusive breastfeeding beyond 6 months may be associated with nutrient
deficiencies and suboptimal growth.14 In a
preliminary analysis, we investigated this potential risk to intellectual
development. In the WAIS and BPP samples, the 40 and 83 subjects who were
exclusively breastfed for 7 months or longer obtained essentially the same
adjusted mean test scores as the 87 and 180 subjects who were partially breastfed
for 7 months or longer. Consequently, we decided to include subjects who were
exclusively breastfed for 7 months or longer in the analyses presented here.
Duration of breastfeeding was originally recorded on a 1- to 11-point
scale (from ≤1-2 weeks to >12 months). On the basis of this scale, the
subjects in both samples were classified into 5 categories according to duration
of breastfeeding: (1) 1 month or less (in the 2 samples, 67% and 72% of this
category were originally coded ≤1-2 weeks); (2) 2 to 3 months; (3) 4 to
6 months; (4) 7 to 9 months; and (5) more than 9 months. It was not possible
to include a separate category for children who were never breastfed since
they were coded as 1 to 2 weeks or less. For both samples, the number of subjects
in each breastfeeding category is shown in Table 2. Unadjusted and adjusted mean differences in intelligence
test scores among the 5 breastfeeding categories were analyzed statistically
for both samples, using the SPSS linear regression and analysis of variance
routines (SPSS Inc, Chicago, Ill, version 10.0). The level of significance
was set at .05.
Based on preliminary regression analyses, the following variables were
considered potential confounders and included as covariates in analyses of
both the 3 WAIS IQs and the BPP scores: (1) marital status; (2) social status;
(3) breadwinner's education; (4) mother's height; (5) mother's age; (6) mother's
weight gain during pregnancy; (7) mother's cigarette consumption during the
third trimester; (8) number of pregnancies; (9) estimated gestational age;
(10) birth weight; (11) birth length; (12) a previously described index of
pregnancy complications15; and (13) a previously
described index of delivery complications.15
Preliminary analyses of both the BPP and the WAIS samples showed no
significant 2-factor interaction between any covariate and duration of breastfeeding.
Thus, analyses of the WAIS sample showed no significant interactions between
sex and duration of breastfeeding. Consequently, the analysis of the WAIS
sample only included the main effect of sex. The WAIS sample consisted of
433 subjects who were prenatally exposed to maternal medication and 540 control
subjects. (Among the exposed subjects, 106 were exposed to hormones and 323
were exposed to barbiturates.) There were no significant interactions between
duration of breastfeeding and being either a medication-exposed or a control
subject, but the main effect of being exposed to medication was significant
and this factor was included as a covariate. Control subjects obtained significantly
higher WAIS IQs than subjects exposed to maternal medication, and this finding
was not unexpected since we have previously observed effects of prenatal exposure
to phenobarbital on adult intelligence.16
Preliminary analyses revealed significant nonlinear associations between
some of the intelligence test scores and mother's height, mother's age, and
delivery complications. To reflect possible nonlinearity, the final regression
models included squared deviations from the mean for these 3 variables.
For most covariates, the missing data rate was less than 1%, but the
missing data rates for maternal weight gain, gestational age, social status,
and breadwinner's education were 23%, 10%, 6%, and 7%, respectively, in the
WAIS sample, and 44%, 21%, 13%, and 14%, respectively, in the BPP sample.
Since about 38% and 63% of the 2 samples had missing data on 1 or more predictor
variables, we decided to present analyses based on overall mean substitution
for missing values and to include dummy variables for missing data on weight
increase in pregnancy, gestational age, social status, and breadwinner's education.17 (Essentially the same results were obtained with
alternative methods of imputing missing values.) Univariate analyses showed
that missing data were not significantly related to WAIS scores, but that
missing data on maternal weight gain were significantly associated with lower
BPP scores. In the regression analyses with all covariates included, missing
data on maternal weight gain, gestational age, social status, and breadwinner's
education were not significantly associated with any intelligence test score.
In general, correlations between the included covariates were low (<0.20),
but a few covariates showed relatively high intercorrelations. In the BPP
sample, the largest squared multiple correlations between an individual covariate
and all other variables in the regression model were 0.71 (for both birth
weight and length) while they were 0.64 for these 2 variables in the WAIS
sample (here the squared multiple correlation for social status was 0.69).
The purpose of the study was not to estimate effects associated with the individual
covariates, but to obtain unbiased estimates of the effects associated with
duration of breastfeeding. Consequently, collinearity among the covariates
was not considered a serious problem.
In summary, the BPP means are adjusted for marital status, social status,
breadwinner's education, mother's height, mother's age, mother's weight gain
during pregnancy, mother's cigarette consumption during the third trimester,
number of pregnancies, estimated gestational age, birth weight, birth length,
an index of pregnancy complications, and an index of delivery complications.
The adjusted WAIS means are also adjusted for effects of sex and medication
exposure, and for both samples, the linear regression model included variables
coding possible nonlinear effects of mother's height, mother's age, and delivery
complications and missing data for maternal weight gain, gestational age,
social status, and breadwinner's education.
Contrasts were calculated to evaluate the significance of differences
between pairs of means, in particular the differences between the 7- to 9-months
and the more than 9-months breastfeeding categories. For tests of trend, interval
midpoints were used to code duration of breastfeeding (0.5, 2.5, 5.0, 8.0,
and 11.0 months) and power polynomials were calculated.17
Tests of trend using the original 1- to 11-point scale essentially showed
the same results as those reported for the 5-category classification.
The study was approved by the institutional review board of the Institute
of Preventive Medicine and the Danish Public Scientific Ethics Committee.
Informed consent was obtained for the WAIS sample, but according to Danish
rules, was not necessary for the BPP sample, which is purely register-based.
Table 2 shows the relation
between the covariates and breastfeeding categories. Duration of breastfeeding
was positively associated with mother's age, social status, education, birth
weight, birth length, and negatively associated with single mother status
and cigarette consumption. In addition, further significant associations with
breastfeeding categories were observed in the BPP sample for gestational age,
weight increase during pregnancy, and pregnancy complications.
In both samples, the positive association between duration of breastfeeding
and parental demographic characteristics (social status and education) and
between breastfeeding and physical development at birth (birth weight and
length) was observed in 4 of the 5 breastfeeding categories. However, breastfeeding
for more than 9 months was associated with lower means than those of the 7-
to 9-months category, and thus the association with duration of breastfeeding
appears to be nonlinear.
Table 3 shows significant
differences among breastfeeding categories for all 3 WAIS IQs. Both the unadjusted
and adjusted IQ means showed a dose-response relationship with duration of
breastfeeding up to 9 months, but a lower mean IQ in the more than 9-months
category. However, the differences between the 7- to 9-months category and
the more than 9-months category were not significant for any WAIS IQ, and
with covariate adjustment, tests of linear and quadratic trend showed only
a significant linear trend (P = .001 for the Verbal
and Performance IQs and P<.001 for the Full Scale
IQ). Although covariate adjustment somewhat reduced the effects associated
with duration of breastfeeding, the differences between the less than 1 month
and the 7- to 9-months categories remained substantial. The unadjusted and
adjusted differences in mean Full Scale IQ between these 2 breastfeeding categories
were 10.1 and 6.6, respectively. Since the theoretical SD is 15, the unadjusted
difference corresponds to about two thirds of the theoretical SD, while the
adjusted difference is approaching half an SD. The patterns of differences
for the Verbal and Performance IQs were strikingly similar, as the adjusted
difference between the less than 1 month and the 7- to 9-months categories
was 6.0 for both IQs.
The observed percentages of subjects with Full Scale IQ scores below
90 were 28, 20, 18, 9, and 4 in the 5 breastfeeding categories, respectively.
A χ2 test showed that these percentages were significantly
different among the 5 breastfeeding categories (P<.001),
and they remained significant when a logistic regression model was used to
adjust for all covariates included in the linear regression analyses of IQ
(P<.001).
Table 3 shows a similar
pattern of mean test scores for the BPP sample. Thus, analyses of the BPP
sample also revealed a positive dose-response relationship for the first 4
breastfeeding categories. While the unadjusted difference between the BPP
mean for the 7- to 9-months and the more than 9-months categories approached
significance, the adjusted means were identical, and for the model with covariates,
tests of linear and quadratic trend only showed significant linear trend (P = .002). However, the effect associated with breastfeeding
appeared smaller for the BPP than for the WAIS, as the difference between
the lowest and the highest adjusted means was 2.1 BPP points, which is less
than one fifth of an SD.
The current study demonstrates a robust association between the duration
of breastfeeding and adult intelligence in 2 nonoverlapping samples assessed
with 2 different measures of intelligence. The results suggest larger effects
associated with breastfeeding for the WAIS sample. A likely explanation is
that the WAIS is a more sensitive measure than the BPP because the 11 subtests
of the WAIS assess a broader range of cognitive functions than the 4 subtests
of the BPP. In addition, the WAIS was administered individually by trained
psychologists, while the BPP is a group test administered as part of the military
preinduction procedures.
The unadjusted test scores were lower for individuals who were breastfed
for more than 9 months compared with those breastfed for 7 to 9 months. However,
the adjusted means for the 2 categories were not significantly different for
any of the test scores. Thus, the overall pattern of results suggests that
no additional positive effects are associated with breastfeeding after 9 months.
Three types of explanations may be considered for the observed positive
association between breastfeeding and cognitive development4:
(1) differences between human milk and infant formula or other complementary
foods (ie, breast milk may contain nutrients that stimulate brain development);
(2) factors associated with the feeding situation, ie, physical and psychological
contact between mother and child; and (3) unidentified factors that correlate
with both infant feeding methods and development of cognitive and intellectual
ability, or relevant and identified factors that cannot be fully controlled
in statistical analyses (residual confounding). The first 2 types of explanations
consider the association with intellectual development as a direct effect
of breastfeeding, whereas the third type of explanation focuses on factors
that are associated with the choice of feeding method.
Most studies in industrialized countries have found a positive association
between breastfeeding and parental education as well as social class.18 This was also the case in our samples since duration
of breastfeeding was associated with a number of demographic factors (mother's
age, single mother status, social status, and education). Although we were
able to statistically control these and other social and perinatal factors,
the question remains whether duration of breastfeeding in our samples was
associated with unregistered factors that correlate with offspring intellectual
development.
The most obvious factor is maternal intelligence, since studies have
observed either nonsignificant or much smaller effects of breastfeeding on
offspring intellectual development when maternal intelligence was included
as a covariate.19,20 However,
in a recent study, the association between duration of breastfeeding and intelligence
at 5 years persisted after controlling for maternal intelligence.21 In our study, the multiple correlations between parental
education and social status (both of which are highly correlated with IQ)
and the 4 offspring IQs were high (0.43, 0.46, 0.28, and 0.41, for the BPP
and the WAIS Verbal, Performance, and Full Scale IQs, respectively). It is
likely that correlations between education, social status, and parental IQs
would be even higher. Consequently, including parental education and social
status as covariates in the current study removed a substantial part of the
variance in offspring IQ associated with parental IQ (the average correlation
between parent IQ and offspring IQ has been reported to be 0.42).22 In addition, the current study does not focus on
bottlefeeding vs breastfeeding, but on the relationship between duration of
breastfeeding and offspring intelligence. Consequently, maternal intelligence
could only explain our results if it correlated systematically with duration
of breastfeeding even within educational and social classes (since the latter
variables were controlled as covariates). It is possible that general awareness
of potential benefits from breastfeeding was less prevalent and more strongly
associated with maternal intelligence among low social status mothers than
among high social status mothers. Counter to this hypothesis, when the 2 samples
were split into low social status (codes 1-5) and high social status subsamples
(codes 6-8), the patterns of mean test scores for the 5 breastfeeding categories
were remarkably similar in the 2 social status subsamples, and formal statistical
tests showed no interaction between duration of breastfeeding and social status.
The extra mother-child physical and psychological contact associated
with duration of breastfeeding may affect the intellectual development of
the child during the first year of life, but seems an unlikely explanation
of long-term effects of breastfeeding on intellectual development into adulthood.
Perhaps a more viable hypothesis is to consider duration of breastfeeding
as an indicator of the interest, time, and energy that the mother is able
to invest in the child during the whole upbringing period. Behavior predicts
behavior, and even within each different social class and educational level,
it may be that mothers who spend more time breastfeeding during the first
year of life also spend more time later interacting with the child. The influence
of family environment on long-term intellectual development has, however,
been questioned by some twin studies,22 and
it is an open question whether associations between duration of breastfeeding
and particular aspects of parental behavior can explain the effects.
A randomized trial demonstrated that early diet may affect childhood
intelligence,23 and the hypothesis that breast
milk contains nutrients that stimulate brain development was supported by
a study comparing developmental scores at the age of 18 months of infants
fed solely standard formula and infants fed donor breast milk.24
A possible explanation of the influence of breastfeeding on cognitive development
is an effect of long-chain polyunsaturated fatty acids, especially docosahexaenoic
acid (DHA), which is present in human milk but not in infant formula or cow's
milk. Docosahexaenoic acid is a main constituent of cell membranes in the
central nervous system, including the retina, and it has been suggested that
it has a role in signal transmission both within and between neurons.25 Randomized controlled trials in both preterm and
term infants have demonstrated improved visual and mental development in those
receiving a formula supplemented with DHA.25-27
To some degree, DHA may be converted from the precursor alfa-linolenic acid
(ALA), and the content of ALA in modern infant formula is high compared with
the content in cow's milk and infant formula used in the early 1960s. According
to the DHA hypothesis, the effect of breastfeeding would therefore be expected
to be somewhat larger in a cohort born in the early 1960s compared with cohorts
of infants receiving modern infant formula.
In conclusion, we observed a positive significant association between
duration of breastfeeding and intelligence in young adults in 2 independent
samples assessed with 2 different intelligence tests. These results indicate
that breastfeeding may have long-term positive effects on cognitive and intellectual
development. The nutrients in breast milk, behavioral factors, and factors
associated with choice of feeding method may all contribute to the positive
association.
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