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JAMA Vol.
287 No. 18, The
Association Between Duration of Breastfeeding and Adult Intelligence
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
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. METHODS
The
Copenhagen Perinatal Cohort
Wechsler
Adult Intelligence Scale Sample 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 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). Subject
Selection 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.
Data
Analysis 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.
RESULTS 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
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. COMMENTThe 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. Author/Article Information Author
Contributions: Study concept and design:
Mortensen, Sanders, Reinisch. Acquisition
of data: Mortensen, Sanders, Reinisch. Analysis
and interpretation of data: Mortensen,
Michaelsen, Sanders, Reinisch. Drafting
of the manuscript: Mortensen. Critical
revision of the manuscript for important intellectual content:
Mortensen, Michaelsen, Sanders, Reinisch. Statistical
expertise: Mortensen. Obtained
funding: Mortensen, Sanders, Reinisch. Administrative,
technical, or material support: Mortensen,
Sanders, Reinisch. Study
supervision: Reinisch. Funding/Support:
This study was supported by United States Public Health Service (USPHS) grants
HD17655 and HD20263 from the National Institute of Child Health and Human
Development to Dr Reinisch, USPHS grant DA05056 from the National Institute on
Drug Abuse to Drs Reinisch and Sanders, and grant 9700093 from The Danish
Research Councils as well as grant 1400/2-4-1997 from the Danish National Board
of Health to Dr Mortensen. Acknowledgment:
We thank Vibeke Munk, BA, for help with the manuscript and critical comments. REFERENCES
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JW, Johnstone BM, Remley DT. 2. 3. 4. 5. 6. 7. 8. 9. 10. 11. 12. 13. 14. 15. 16. 17. 18. 19. 20. 21. 22. |