infant feeding and childhood cognition.pdf

8/22/2019 Infant Feeding and Childhood Cognition.pdf

1/9

Infant Feedingand Childhood Cognition atAges3 and 7 Years

Effects of Breastfeeding Duration and Exclusivity

Mandy B. Belfort,MD, MPH; SherylL. Rifas-Shiman, MPH; Ken P. Kleinman,ScD;Lauren B.Guthrie,MPH;

David C. Bellinger, PhD; Elsie M.Taveras, MD, MPH; Matthew W. Gillman, MD, SM;Emily Oken,MD,MPH

IMPORTANCE Breastfeeding may benefit child cognitive development, but few studies have

quantified breastfeeding durationor exclusivity, norhas anystudyto date examined therole

of maternal diet duringlactation on child cognition.

OBJECTIVES To examine relationships of breastfeeding duration and exclusivity with child

cognition at ages 3 and7 years and to evaluate theextent to which maternal fish intake

during lactation modifies associations of infant feeding with later cognition.

DESIGN, SETTING, AND PARTICIPANTS Prospective cohort study (Project Viva), a US prebirth

cohort that enrolled mothers from April 22, 1999,to July 31,2002, andfollowedup children

to age7 years,including 1312 Project Viva mothers and children.

MAINEXPOSURE Duration of anybreastfeedingto age12 months.

MAINOUTCOMES AND MEASURES Child receptive language assessed with the Peabody

Picture Vocabulary Testat age 3 years, Wide RangeAssessment of VisualMotor Abilitiesat

ages 3 and 7 years, and Kaufman Brief IntelligenceTest andWide RangeAssessment of

Memory andLearningat age7 years.

RESULTS Adjusting for sociodemographics, maternal intelligence, and home environment in

linear regression, longer breastfeeding duration was associated with higher Peabody Picture

Vocabulary Testscoreat age3 years (0.21; 95%CI, 0.03-0.38points per month breastfed)

and with higher intelligenceon theKaufman Brief Intelligence Testat age 7 years (0.35;

0.16-0.53 verbal points per month breastfed; and 0.29; 0.05-0.54 nonverbal points per

month breastfed). Breastfeeding duration was not associated with Wide Range Assessmentof Memory andLearning scores. Beneficial effects of breastfeedingon theWide Range

Assessment of VisualMotor Abilities at age3 years seemed greater forwomenwho

consumed 2 or more servings of fish per week (0.24; 0.00-0.47 pointsper monthbreastfed)

compared with less than 2 servings of fish per week (0.01;0.22 to 0.20 points per month

breastfed) (P= .16 for interaction).

CONCLUSIONS AND RELEVANCE Our results support a causal relationship of breastfeeding

duration with receptive language and verbal and nonverbal intelligence later in life.

JAMAPediatr. doi:10.1001/jamapediatrics.2013.455

Published onlineJuly 29,2013.

Editorial

Author Affiliations: Division of

Newborn Medicine,Boston Childrens

Hospital, Harvard Medical School,

Boston, Massachusetts (Belfort);

Departmentof PopulationMedicine,

HarvardMedical Schooland Harvard

PilgrimHealth Care Institute,Boston,

Massachusetts (Rifas-Shiman,

Kleinman, Guthrie, Taveras,Gillman,

Oken); Departmentof Neurology,

BostonChildrens Hospital, Harvard

Medical School, Boston,

Massachusetts (Bellinger);Departments of Epidemiology and

Nutrition, Harvard Schoolof Public

Health, Boston, Massachusetts

(Gillman).

Corresponding Author: Mandy B.

Belfort, MD, MPH, Division of

Newborn Medicine,Boston Childrens

Hospital, Harvard Medical School,

HunnewellRoom 438,300

Longwood Ave, Boston, MA 02115

([email protected]

.edu).

Research

Original Investigation

E1

wnloaded From: http://archpedi.jamanetwork.com/ by a World Health Organization User on 08/01/2013


2/9

Strong evidencesupports therelationship betweenbreast-

feeding andhealth benefits in infancy, includingpreven-

tionof gastrointestinaltract infections andotitismedia.1

Theextent to which breastfeeding leads to bettercognitive de-

velopment is less certain. While observational studies1-4 have

reported positiveassociationsof breastfeeding with laterintel-

ligence, breastfeeding is stronglyrelatedto determinantsof child

intelligence, such as maternal intelligence, and developmen-

tal stimulation received by the child; residual confounding by

suchshareddeterminantsmayhaveledobservationalstudies1,2,5

to overestimate the effect of breastfeeding on child intelli-

gence.Another limitation of prior investigations is theclassifi-

cation of infant feeding as ever vs never breastfed.4 Failure to

account for partial vs exclusivebreastfeedingor breastfeeding

duration could lead to underestimation of the true effect of

breastfeeding on child intelligence. Detailed data regarding

breastfeedingexposure and adequate control for confounding

factorsare necessary forvalid estimatesof therelationshipbe-

tweenbreastfeedingand laterintelligence,but no studyto date

has fulfilled these requirements.

Nutrients in breast milk, such as n-3 fatty acid docosa-

hexaenoicacid (DHA),maybenefit thedevelopingbrain. A ma-

jor determinant of breast milk DHA content is the mothers

diet,6 and fish is a rich source of DHA. In pregnancy, greater

maternal fish intake (particularlyfish lowin mercurycontami-

nation) is associated with better childhood cognitive

outcomes,7but the extent to which maternal fish intake dur-

ing lactation accounts for the relationship between breast-

feeding and cognitionhas notbeen reported.The aims of our

study were 2-fold: (1) to examine relationships of breastfeed-

ingdurationand exclusivitywith child cognitionat ages3 and

7 years and (2) to evaluate the extent to which maternal fish

intake during lactation modifies associations of infant feed-

ing with later cognition.

Methods

Participants

Westudied participantsin Project Viva, a prospective,longitu-

dinal cohort study designed to examine prenatal factors in re-

lationtopregnancy andchildhealth.FromApril22,1999,to July

31,2002,Project Viva enrolled pregnantwomenattending pre-

natal care at8 obstetrical offices of a multispecialty groupprac-

tice in eastern Massachusetts.Exclusioncriteria included mul-

tiple gestation, inability to answer questions in English,

gestational age of at least 22 weeks at the initial prenatal care

appointment,and plans to move away fromthe area beforede-livery. Recruitment andfollow-up detailsat birth,8at6 months,9

and at3 years10 have beenreported. Follow-up data collection

at age7 years wascompletedin December2010. Humaninves-

tigation committees of the Harvard Pilgrim Health Care Insti-

tute, Brigham and Womens Hospital, and BethIsrael Deacon-

ess Medical Center approved the study, and mothers of all

participating children gave written informed consent.

Of2128 womenwho delivered a live infant,we excluded45

childrenbornat a gestationalageof less than 34weeks, 325chil-

drenwho weremissingbreastfeedingstatus atage 6 monthsand

breastfeeding durationat age12 months, and446children who

were missing cognitive measures at ages 3 and 7 years. There-

fore, our sample for this analysis comprised 1312 Project Viva

mothersandchildren(1224atage3yearsand1037atage7years).

Measurements

Breastfeeding

When the participating child was ages 6 and 12 months, we

asked the mother the questions listed in Table 1. To deter-

mine breastfeeding exclusivity at ages 6 and 12 months, we

asked detailed questions about the age at which solid foods

and nonbreast milk liquids were introduced.

Cognition

Whenchildren wereage 3 years, trained researchstaff admin-

istered the Peabody Picture Vocabulary TestThird Edition(PPVT-III),11 a test of receptive language correlated (Pearson

R = 0.90) with intelligence tests, such as the Wechsler Intelli-

gence Scale for Children III. We also administered the Wide

Range Assessmentof VisualMotor Abilities(WRAVMA)12peg-

board (fine motor), matching (visual spatial), and drawing(vi-

sualmotor) subtests. Subtest scores are reportedindividually

and combined as a visual motor composite score.

Atage7years,weadministeredtheWRAVMAdrawingsub-

test and the Kaufman Brief Intelligence TestSecond Edition

(KBIT-II), which measures verbal and nonverbal intelligence

and is correlated (Pearson R = 0.89) with the Wechsler Intel-

ligenceScale forChildrenIII.13Inaddition, weassessed memory

andlearning withthe WideRangeAssessment of Memory andLearning (WRAML)14 design memory and picture memory

tests. Scores were summed to yield a visual memory com-

bined score.

Study staff administeringcognitivetests wereunaware of

the childrens breastfeeding status. The PPVT-III, WRAVMA,

and KBIT-II are scaled to a mean (SD) score of 100 (15).

Covariates

We collected data from mothers regarding parental and child

demographic, social, economic, and health information

Table 1.Questions AboutBreastfeedingatAges6 and12Months

Question About Breastfeeding

At Age 6 mo

For all infants

(1) Have you ever breastfed your baby? By breastfeeding, we mean thatyou have put your baby to your breast, whether or not your baby actuallyreceived breast milk, or that you have fed your baby your breast milk.

(2) Are you now feeding your baby any infant formula?

(3) Are you now feeding your baby any breast milk?

For weaned infants

How old was your baby when you stopped breastfeeding?

At Age 12 mo

For all infants

Have you ever breastfed your child?

Are you still breastfeeding at all?

For weaned infants

How old was your child when you stopped breastfeeding?

Research Original Investigation Infant Feeding and Childhood Cognition

E 2 JA MA P ed ia tric s Published online July 29, 2013 jamapediatrics.com



3/9

through self-administered questionnaires and interviews in

pregnancy and shortly afterdelivery.15 At6 months post par-

tum, we administered a brief, validated food frequency

questionnaire,16 including questions about the mothers mean

weekly fishintake(canned tunafish, shellfish, and darkmeat

fish [eg, mackerel, salmon, sardines, bluefish, or swordfish],

as well as other fish [eg, cod, haddock, or halibut]) since the

infantsbirth. To measure maternal intelligence,we adminis-

tered to mothers the PPVT-III when the child was age 3 years

and the KBIT-II when the child was age 7 years. We also ad-

ministered the Home Observation Measurement of the Envi-

ronment short form (HOME-SF),17 which measures cognitive

stimulation and emotional support in the childs environ-

ment. Higher scores (range, 0-22) indicate more favorable

environments.

DataAnalysis

Our main exposures were the following: (1) duration of any

breastfeeding in months;(2) durationof exclusive breastfeed-

ingin months, defined asfeeding breastmilkbut nosolidfoods

or nonbreast milkliquids(exceptwater)to age6 months;and

(3) breastfeeding status at age 6 months, categorized as for-

mulaonly,never breast fed, formulaonly, weaned, mixed

formula and breast milk, and breast milk only, no formula.

Our outcome measures werethe PPVT-IIIandWRAVMAscores

at age 3 years and theKBIT-II, WRAVMA, and WRAML scores

atage 7 years.To examine theeffect of potentialconfounders

on estimatedrelationships of breastfeedingmeasureswith cog-

nitive outcome measures, we adjusted for 4 models in linear

regression.Model0 adjustedfor child ageand sex.Model1 ad-

justed for covariatesin model 0 plus gestational age and birth

weightzscore.18Model2 adjustedfor covariates inmodel1 plus

childrace/ethnicity and maternalage, parity, smoking status,

depression at 6 months post partum, and employment and

child care at age 6 months, as well as primary language, an-nual household income, and parental educational level and

marital status.Model 3 adjusted for covariatesin model2 plus

HOME-SFscore.Model4 adjustedfor covariates in model3 plus

maternal PPVT-III or KBIT-II score.

Tocompareourresultswith thoseof other studies,we es-

timated the difference in cognitive test scores between chil-

dren ever vs never breastfed. Toexaminethe extentto which

maternal fish intake modified relationships of breastfeeding

with outcome measures, we stratified by fish intake (


4/9

Table2. IncludedandExcludedProjectVivaMothersand Children

VariableIncluded at Age 3 y

(n = 1224)Included at Age 7 y

(n = 1037)Excluded at Ages 3 and 7 ya

(n = 771)

Mother

Age, mean (SE), y 32.5 (0.1) 32.3 (0.2) 31.0 (0.2)

PPVT-III score, mean (SE) 106.0 (0.4) 105.4 (0.5) 100.8 (0.8)

KBIT-II score, mean (SE) 107.9 (0.5) 107.2 (0.5) 102.5 (0.7)

2 Servings of fish per wk, % 55.0 52.8 50.1

Parity, %

0 47.5 47.3 47.6

1 36.3 36.4 35.4

2 16.2 16.4 17.0

Smoking status, %

Never 68.8 70.1 64.5

Former 21.0 20.1 17.4

During pregnancy 10.2 9.8 18.1

Depression at 6 mo post partum, % 8.8 9.1 11.0

Educational level, %

High school diploma 7.2 8.6 18.8

Some college 20.2 21.3 26.9

Bachelors degree 37.7 34.9 32.7

Graduate degree 34.9 35.2 21.6

Employment at 6 mopost partum, %

Employed 66.0 66.7 56.0

Employed, on maternity leave 6.0 6.8 6.2

Not employed, looking 4.6 5.3 10.1

Not employed, not looking 23.3 21.3 27.7

Child

Gestational age, mean (SE), wk 39.6 (0.0) 39.7 (0.0) 39.6 (0.1)

Birth weight, mean (SE), kg 3.5 (0.0) 3.5 (0.0) 3.5 (0.0)

Birth weight for gestational agez score, mean (SE)

0.22 (0.03) 0.20 (0.00) 0.14 (0.04)

Female sex, % 50.4 50.5 47.7

Race/ethnicity, %

Asian 2.7 3.0 5.8

Black 11.9 15.1 21.0

Hispanic 3.5 3.7 8.0

White 70.1 66.1 55.4

Other 11.8 12.2 9.8

Primary English speaker, % 96.2 98.7 92.7

Child care at age 6 mo, %

Center 16.8 17.2 17.4

Other home 26.1 27.3 24.8

At own home 14.3 13.6 14.9

None 42.8 42.0 43.0

Breastfeeding status at age 6 mo, %Formula only, never breastfed 10.6 10.1 15.0

Formula only, weaned 34.7 35.1 46.3

Mixed formula and breast milk 26.4 26.8 19.5

Breast milk only, no formula 28.2 28.0 19.2

Duration of breastfeeding,mean (SE), mo

Exclusive to age 6 mo 2.4 (0.1) 2.4 (0.1) 1.9 (0.1)

Any to age 12 mo 6.4 (0.1) 6.5 (0.1) 4.9 (0.2)

(continued)


E 4 JA MA P ed iat ri cs Published online July 29, 2013 jamapediatrics.com



5/9

We found a similar trend forthe KBIT-IIverbal andnonverbal

scoresat age 7 yearsbutobserved noappreciabletrend forthe

WRAVMA or WRAML scores.Compared with children who were never breastfed, the

fully adjusted PPVT-III score at age 3 years was 1.45 (95% CI,

0.98 to 3.87) points higher forchildren whowere ever breast-

fed, and the KBIT-II verbal score at age 7 years was 3.75 (1.17-

6.33) points higher.The WRAVMAand WRAML scores werenot

statistically different (data not shown).

Stratifying by maternal postpartum fish intake (


6/9

4.2 points, or almost one-third of an SD during 12 months,

whereas the effect size of 0.80 verbal IQ points per month of

exclusive breastfeeding translates to almost 5 points over 6

months.Effects weresimilarin directionbut somewhatweaker

in magnitude for nonverbal IQ and receptive language at age

3 years. We found no important main association of breast-

feeding with visual motor skills or visual memory.While numerous investigations have demonstrated asso-

ciations of breastfeedingwith latercognition,some studies1,4,5

have had methodological flaws. In particular, adequate con-

trol for confounding factors is critical because breastfeeding

and child cognition share many determinants, including ma-

ternal characteristics and environmental factors. A 2007

meta-analysis1 identifiedmaternal intelligence and the home

environment as key confounders that are frequently over-

looked and found only 1 prior study5 withappropriate adjust-

ment, an analysis of data from the US National Longitudinal

Survey of Youth(NSLY) in which theassociation of breastfeed-

ing(ever vsnever) withachievement scoresat ages5 to14 years

was attenuated from4.7 to 1.3points after adjustment for ma-ternal intelligence and diminished to only 0.5points afterad-

justment for sociodemographic and other variables, includ-

ing the HOME-SF score. We also adjusted for maternal

intelligence andtheHOME-SFscore, as wellas numerous other

potential confounders, and nevertheless found a substan-

tially stronger association(3.75points)of evervs never breast-

fed with verbal IQ at age 7 years.

It is possible that differences in the degree of breastfeed-

ing exclusivity explain why we observed a stronger associa-

tionof breastfeedingwith cognitionthan wasseen in theNSLY.5

By classifying breastfeeding as ever vs never, the NSLY may

have included in their breastfed group a substantial number

of infants who received formula and breast milk, biasing re-

sults toward the null, but the authors did not report the de-

gree of mixed feedings.Differences in breastfeeding duration

mayalso explain our discrepant results.In a secondaryanaly-

sis, the NSLY found that the achievement scores of children

breastfedfor at least29 weekswere 1.5points higher thanthose

of children never breastfed (P= .01), but the authors consid-

eredtheirdataaboutbreastfeeding durationlessreliable thandata about whether a child was ever breastfed. Finally, vari-

able outcome measures (achievement test score in the NSLY

vs IQ in our study) may explain our different results.

We identified 4 additional observational studies20-23 that

adjusted for maternal intelligence and the HOME-SF score.

Whilewe founda modest associationof breastfeedingwith ver-

bal intelligenceat age 3 years, neither of the other 2 preschool

studies found an important association with cognitive out-

c omes ( M c Ca rt h y G enera l Cognit iv e Index21 ,22 an d

PPVT-Revised22atage 4 years). Of thestudiesreporting school-

age outcomes, one study21 found a 1.3-point (95% CI, 2.3 to

4.9) advantage of ever vs never breastfeeding on the Wechs-

ler Full-Scale IQ at age 7 years; another study

23

found a 0.7-point (0.2-1.3)advantageon thesame outcome at age11 years;

andtheotherstudy22 found no association withverbal or per-

formance IQ at age 11 years(effect estimate not reported). All

those effect estimates are smaller than ours, but none of the

studies accounted for breastfeeding duration or exclusivity.

Studiesof cohortswith different confounding patterns are

alsoinformative. Brionet al24analyzedassociations of breast-

feeding durationwith IQ atage 8 years in 2 cohorts.In oneco-

hort(the British Avon LongitudinalStudy of Parents and Chil-

dren), breastfeeding duration and child IQ were strongly

Table4.AdjustedAssociationsof Durationof Breastfeeding

WithCognitiveTestScoresa

Score

Points (95% CI) per Month Breastfed

Any Breastfeedingto Age 12 mo

Exclusive Breastfeedingto Age 6 mob

At Age 3 y

PPVT-III 0.21 (0.03 to 0.38) 0.50 (0.11 to 0.89)

WRAVMA drawing 0.01 (0.15 to 0.16) 0.12 (0.47 to 0.22)WRAVMA pegboard 0.09 (0.06 to 0.24) 0.03 (0.37 to 0.31)

WRAVMA matching 0.09 (0.10 to 0.27) 0.00 (0.42 to 0.41)

WRAVMA total 0.08 (0.07 to 0.23) 0.07 (0.40 to 0.27)

At Age 7 y

KBIT-II verbal 0.35 (0.16 to 0.53) 0.80 (0.38 to 1.22)

KBIT-II nonverbal 0.29 (0.05 to 0.54) 0.58 (0.01 to 1.14)

WRAVMA drawing 0.08 (0.33 to 0.18) 0.05 (0.62 to 0.53)

WRAML visualmemory

0.04 (0.02 to 0.11) 0.12 (0.03 to 0.27)

Abbreviations: HOME-SF, HomeObservation Measurement of the Environment

shortform; KBIT-II,Kaufman BriefIntelligence TestSecond Edition;

PPVT-III,Peabody Picture VocabularyTestThirdEdition;WRAML, WideRange

Assessmentof Memory and Learning;WRAVMA,Wide RangeAssessment of

VisualMotor Abilities.a Estimatesare adjusted for childage, sex,fetal growth, gestational age,

race/ethnicity, and primarylanguageand for maternal age,parity,smoking

status, IQ,depression, employment, andchildcareat 6 months post partum,

as well as forparental educational level,annual householdincome,and

HOME-SF score.

b Nosolid foods or nonbreast milk liquids(exceptwater).

Figure.Differences inKaufmanBrief IntelligenceTestSecondEdition

Verbal Scoresat Age7 Years AccordingtoDurationof Any

Breastfeeding,WithLinearTrendLine

0

1-3 4-6 7-9 10-11 12

7

5

6

VerbalIQ

Difference

Duration of Any Breastfeeding, mo

4

2

3

1


7/9

predictedby measuresof socioeconomic position, whereasin

theother cohort(Pelotas,Brazil) childIQ waspredicted byso-

cioeconomic factors, but breastfeeding duration was not. In

both cohorts, child IQ was strongly associated with breast-

feeding duration, suggesting that confounding alone did not

explain the relationship.Theresultsofourstudyarealsoconsistentwithalargeclus-

terrandomizedtrial25of breastfeedingpromotionin whichver-

bal IQ at age 6.5 years was 7.5points (one-halfof an SD) higher

in the breastfeeding promotion group. By design, that study

minimized confounding by measured and unmeasured fac-

tors; however, nonblinding of clinicians assessing the cogni-

tive outcomesto participantbreastfeeding statussuggests the

potential for bias. Together, the results of the well-controlled

observational studies20-23 (including ours), the analysis of co-

hortswithoutsocialpatterningof breastfeeding(eg, inthePelo-

tas cohort),24andthelargerandomized trial25suggest thatcon-

founding does notaccount fully for the observed association

of breastfeeding with later cognition.

In analyses stratified by fish intake, the beneficial effects

of breastfeeding on visual motor ability at age 3 years seemed

greater for women who consumed 2 or more servings com-pared with less than 2 servings per week, although the inter-

actionwas not statisticallysignificant. Thisobservationis con-

sistent with the hypothesis that 1 or more nutrients in fish

transfer to breast milk and account for some of the observed

beneficial effectand is relevant to optimizingthe maternaldiet

during lactation.Docosahexaenoicacid is incorporated in large

amounts into cell membranes of the developing retina and

brain. Its content in breast milk is variable26 and depends on

DHAsourcesinthematernaldiet, 6,27 includingfish; infant DHA

status in turn depends on theDHA content of ingested breast

Table5.AdjustedCognitive TestScoreDifferencesat Ages3 and7 YearsAccording toBreastfeeding Status at Age6 Monthsa

Score

Difference in Points (95% CI)PValue

for TrenddNever Breastfed Weaned Mixed Feedingsb Breast Milk Onlyc

At Age 3 y

PPVT-III 3.17 (5.92 to 0.41) 2.26 (4.22 to 0.29) 2.27 (4.24 to 0.30) 0.00 [Reference] .01

WRAVMA drawing 0.63 (3.03 to 1.78) 0.01 (1.74 to 1.72) 0.52 (2.27 to 1.22) 0.00 [Reference] .80

WRAVMA pegboard 1.96 (4.31 to 0.39) 0.36 (2.05 to 1.34) 0.04 (1.66 to 1.74) 0.00 [Reference] .18

WRAVMA matching 1.93 (4.82 to 0.96) 0.62 (2.65 to 1.41) 1.13 (3.21 to 0.96) 0.00 [Reference] .29

WRAVMA total 2.04 (4.39 to 0.30) 0.47 (2.13 to 1.19) 0.75 (2.42 to 0.93) 0.00 [Reference] .19

At Age 7 y

KBIT-II verbal 5.59 (8.52 to 2.67) 2.96 (5.05 to 0.88) 1.40 (3.49 to 0.68) 0.00 [Reference]


8/9

milk.27Randomized trialsof DHA supplementationduringlac-

tation have found beneficial effects of DHA on early motor

skills28 and sustained attention29but not v isual motor func-

tion or general cognition.28,30 Our observation may be ex-

plainedby DHAor nutrients in fish other than DHA.It mayalso

be a chance finding.

Strengths of our study include a prospective design, de-

tailed contemporaneous measurement of duration and exclu-

sivity of breastfeeding,and measurement of numerous poten-

tialconfoundingvariables, includingthehome environmentand

maternalIQ. As in allobservationalstudies,confoundingby un-

measured factors is possible and may have led us to overesti-

mate the true effect of breastfeeding, although our results are

consistent with data from a randomized trial25 of breastfeed-

ingpromotionthat eliminatesconfoundingby design. We mea-

sured cognitionat schoolage,whichtendsto be stablethrough

adulthood31 comparedwith measurement in preschool or ear-

lier. The elevated socioeconomic status and high breastfeed-

ingrateof ourcohortmaylimitgeneralizabilityofthestudyfind-

ings. In addition, we followed up only a subset of the original

Project Viva cohort to ages 3 and 7 years. The children we ob-

served tended to be of higher socioeconomic status and were

less likely to be of minority race/ethnicity than thechildrenwe

did not follow up,whichcould have led to overestimates if the

effect of breastfeedingon cognitionwas much weakeror in the

oppositedirectionin those whodroppedout,situationswe find

unlikely. Finally, for the statisticallysignificant associations of

breastfeeding withlatercognition, 95%CIs werenarrowand ex-

clude a null result, butthe lower confidencelimitsinclude val-

ues with little clinical importance.

In summary, our results support a causal relationship of

breastfeeding in infancy with receptive language at age 3 and

with verbaland nonverbalIQ atschool age. Thesefindingssup-

port national and international recommendations to pro-

mote exclusive breastfeeding through age 6 months and con-

tinuation of breastfeeding through at least age 1 year.

ARTICLE INFORMATION

Accepted for Publication: February 6, 2013.

Published Online: July 29,2013.

doi:10.1001/jamapediatrics.2013.455.

Author Contributions:Study concept and design:

Belfort,Kleinman,Gillman,Oken.

Acquisition of data: Bellinger, Gillman, Oken.

Analysis and interpretation of data: Belfort,

Rifas-Shiman,Kleinman,Guthrie,Bellinger, Taveras,

Oken.

Drafting of themanuscript:Belfort.

Critical revision of themanuscriptfor important

intellectual content: All authors.

Statistical analysis: Belfort, Rifas-Shiman, Kleinman,

Guthrie.

Obtained funding:Belfort, Gillman, Oken.

Administrative, technical, andmaterial support:

Gillman.Study supervision: Bellinger, Taveras, Gillman, Oken.

Conflict of Interest Disclosures: None.

Funding/Support: This workwassupported by

grants K23 DK083817 (Dr Belfort), K24HL68041

(Dr Gillman), K24 HD069408(Dr Oken),

R01 ES016314,R01 HD34568, and R01 HL64925

from theNational Institutesof Health.

REFERENCES

1. Ip S,ChungM, Raman G,et al.Breastfeeding and

maternal and infant health outcomes in developed

countries. EvidRep TechnolAssess (Full Rep).

2007;(153):1-186.

2. Jain A, Concato J,Leventhal JM.How goodis the

evidence linking breastfeeding and intelligence?

Pediatrics. 2002;109(6):1044-1053.

3. Anderson JW, JohnstoneBM, Remley DT.

Breast-feeding and cognitivedevelopment: a

meta-analysis.Am J Clin Nutr. 1999;70(4):525-535.

4. DraneDL, LogemannJA. A critical evaluationof

theevidence onthe association between type of

infant feeding and cognitive development. Paediatr

Perinat Epidemiol. 2000;14(4):349-356.

5. Der G, BattyGD, Deary IJ. Effectof breast

feeding on intelligence in children: prospective

study, sibling pairs analysis, and meta-analysis.BMJ.

2006;333(7575):e945. http://

www.ncbi.nlm.nih.gov/pmc/articles/PMC1633819/.

Accessed June15, 2013.

6. JensenCL, MaudeM, Anderson RE,HeirdWC.

Effect of docosahexaenoic acid supplementationof

lactatingwomen onthe fattyacid composition of

breastmilklipidsand maternal andinfant plasma

phospholipids.Am J Clin Nutr. 2000;71(1)(suppl):

292S-299S.

7. OkenE, Radesky JS,WrightRO, etal. Maternal

fish intake duringpregnancy, bloodmercury levels,

andchildcognition at age3 years in a UScohort.

Am J Epidemiol. 2008;167(10):1171-1181.

8. OkenE, Kleinman KP, OlsenSF, Rich-Edwards

JW, GillmanMW. Associationsof seafoodand

elongatedn-3 fatty acid intake withfetal growth

andlength of gestation: results froma US

pregnancycohort.Am J Epidemiol. 2004;160(8):

774-783.

9. GillmanMW, Rifas-Shiman SL, Kleinman KP,

Rich-Edwards JW, Lipshultz SE. Maternal calcium

intake and offspring blood pressure.Circulation.

2004;110(14):1990-1995.

10. Taveras EM, Rifas-ShimanSL, Scanlon KS,

Grummer-Strawn LM, SherryB, GillmanMW. To

what extent is theprotectiveeffectof

breastfeeding on futureoverweight explained by

decreasedmaternal feeding restriction? Pediatrics.

2006;118(6):2341-2348.

11. WilliamsKT, Wang J-J.TechnicalReferences to

the Peabody Picture VocabularyTestThirdEdition

(PPVT-III). CirclePines, MN:American Guidance

Service Inc;1997.

12. Adams W, SheslowD.WRAVMA (WideRange

Assessment of Visual Motor Abilities). Wilmington,

DE:WideRangeInc;1995.

13. GradosJJ,Russo-GarciaKA. Comparisonof the

Kaufman BriefIntelligence Test and the Wechsler

Intelligence Scalefor ChildrenThirdEdition in

economicallydisadvantaged AfricanAmerican

youth.J Clin Psychol. 1999;55(9):1063-1071.

14. Adams W, SheslowD.WideRange Assessment

ofMemoryand LearningAdministrationand

TechnicalManual. 2nd ed. Lutz,FL: Psychological

AssessmentResourcesInc; 2001.

15. Gillman MW, Rich-Edwards JW, Rifas-Shiman

SL, Lieberman ES, Kleinman KP, Lipshultz SE.Maternal ageand other predictorsof newborn

blood pressure.J Pediatr. 2004;144(2):240-245.

16. Fawzi WW, Rifas-ShimanSL, Rich-Edwards JW,

Willett WC,GillmanMW.Calibrationof a

semi-quantitative food frequency questionnaire in

early pregnancy.Ann Epidemiol. 2004;14(10):

754-762.

17. Frankenburg WK, CoonsCE. HomeScreening

Questionnaire: its validity in assessing home

environment.J Pediatr. 1986;108(4):624-626.

18. OkenE, Kleinman KP, Rich-Edwards J, Gillman

MW. A nearlycontinuous measureof birth weight

forgestationalage using a UnitedStates national

reference.BMCPediatr. 2003;3:e6.

http://www.biomedcentral.com/1471-2431/3/6.


19. HortonNJ,Kleinman KP. Much adoabout

nothing:a comparisonof missing data methods and

software to fit incompletedata regression models.

Am Stat. 2007;61(1):79-90.

20. Morrow-Tlucak M, HaudeRH, ErnhartCB.

Breastfeeding and cognitivedevelopment in the

first 2 years of life.Soc Sci Med. 1988;26(6):

635-639.

21. Wigg NR,Tong S,McMichael AJ, BaghurstPA,

Vimpani G,Roberts R. Does breastfeeding at six

months predict cognitivedevelopment?Aust N Z J

Public Health. 1998;22(2):232-236.

22. Jacobson SW, ChiodoLM, Jacobson JL.

Breastfeeding effects on intelligence quotient in

4- and 11-year-old children.Pediatrics. 1999;103(5):

e71. http://www.biomedcentral.com/1471-2431/3/6.


23. Hay DF, PawlbyS, Sharp D,Asten P, Mills A,

KumarR. Intellectual problems shownby

11-year-old children whosemothers had postnatal

depression.J Child Psychol Psychiatry. 2001;42(7):

871-889.

24. BrionMJ,LawlorDA, MatijasevichA, etal.

What arethe causaleffects of breastfeeding on IQ,

obesity and blood pressure? evidence from

comparing high-income withmiddle-income

cohorts. Int J Epidemiol. 2011;40(3):670-680.


E 8 JA MA P ed iat ri cs Published online July 29, 2013 jamapediatrics.com



9/9

25. Kramer MS, Aboud F, MironovaE, etal;

Promotion of Breastfeeding Intervention Trial

(PROBIT) StudyGroup. Breastfeeding and child

cognitive development: new evidence from a large

randomizedtrial.Arch Gen Psychiatry. 2008;65(5):

578-584.

26. BrennaJT, VaraminiB, JensenRG,

Diersen-SchadeDA, BoettcherJA, Arterburn LM.

Docosahexaenoic and arachidonicacid

concentrations in humanbreast milk worldwide.Am J Clin Nutr. 2007;85(6):1457-1464.

27. Sanders TA, ReddyS. Theinfluence of a

vegetariandieton thefatty acid composition of

human milk andthe essentialfattyacidstatus of the

infant.J Pediatr. 1992;120(4, pt 2):S71-S77.

28. JensenCL, VoigtRG, PragerTC, etal. Effects of

maternal docosahexaenoic acid intake on visual

function and neurodevelopmentin breastfed term

infants.Am J Clin Nutr. 2005;82(1):125-132.

29. Cheatham CL,Nerhammer AS,AsserhjM,

MichaelsenKF, Lauritzen L. Fishoil

supplementationduring lactation: effects on

cognitionand behavior at 7 yearsof age. Lipids.

2011;46(7):637-645.

30. CampoyC, Escolano-Margarit MV, AnjosT,

SzajewskaH, Uauy R. Omega3 fattyacidson child

growth, visualacuity and neurodevelopment. Br J

Nutr. 2012;107(suppl 2):S85-S106.

31. Sattler JM.Assessment of Children: Cognitive

Applications. 4thed. SanDiego,CA: JeromeM.

Sattler Inc;2001.

Infant Feeding and Childhood Cognition Original Investigation Research

jamapediatrics.com JAMA Pediatrics Published onlineJuly 29,2013 E9

infant feeding and childhood cognition.pdf

Documents