Health and development outcomes in 6.

5-y-old children breastfed

exclusively for 3 or 6 mo13
Michael S Kramer, Lidia Matush, Natalia Bogdanovich, Frances Aboud, Bruce Mazer, Eric Fombonne, Jean-Paul Collet,
Ellen Hodnett, Elena Mironova, Sergei Igumnov, Beverley Chalmers, Mourad Dahhou, and Robert W Platt

INTRODUCTION

In May 2001, the World Health Assembly passed a resolution

recommending exclusive breastfeeding for 6 mo (1). That decision was based, in part, on a systematic review of the evidence
available at that time, which suggested that exclusive breastfeeding for 6 mo provided additional protection against gastrointestinal infection and prolonged the period of postpartum
amenorrhea and was not associated with any detectable health
risks compared with shorter durations of exclusive breastfeeding
with continued partial breastfeeding (2). Many countries and
pediatric and other health organizations have issued guidelines
consistent with the World Health Organization (WHO) recommendation. Nonetheless, exclusive breastfeeding for 6 mo

1070

remains unusual in most settings, including both developed and

developing countries (38).
In the mid-1990s, we initiated the Promotion of Breastfeeding
Intervention Trial (PROBIT), a cluster-randomized trial of
a breastfeeding promotion intervention modeled on the WHO/
UNICEF Baby-Friendly Hospital Initiative (BFHI) (9). Although
most of the publications emanating from this trial have used an
intention-to-treat analysis based on randomized treatment allocation, we have also published several observational analyses of the
PROBIT cohort, including a previous summary of infant outcomes
during the first year of life in which we compared PROBIT children
who had been breastfed exclusively for 3 mo with continued partial
breastfeeding to 6 mo with those who were breastfed exclusively
for 6 mo (10). We found that the group exclusively breastfed for
6 mo had a significantly lower incidence of gastrointestinal infection during the period 36 mo (10). We have continued to
follow the PROBIT cohort since that time and have reported on
health and development outcomes at 6.5 y, according to the randomized treatment allocation (1115). In this article, we extend
our previous comparison of 3 with 6 mo of exclusive breastfeeding
to include the outcomes measured at 6.5 y of age.
SUBJECTS AND METHODS

PROBIT is registered as ISRCTN-37687716; a detailed description of the methods is provided in previous publications
(9, 1115). In summary, 31 maternity hospitals and 1 of their
1

From the Departments of Pediatrics (MSK, BM, EF, J-PC, MD, and
RWP), Epidemiology and Biostatistics (MSK, J-PC, and RWP), Psychology
(FA), and Psychiatry (EF), McGill University Faculty of Medicine, Montreal, Canada; the Republican Scientific and Practical Center Mother and
Child, Minsk, Belarus (LM, NB, IM, and SI); the Faculty of Nursing,
University of Toronto, Toronto, Canada (EH); and the Department of Obstetrics and Gynecology and Ontario Health Research Institute, University of
Ottawa, Ottawa, Canada (BC).
2
Supported by a grant from the Canadian Institutes of Health Research.
RWP is a career investigator (Chercheur-boursier) and BM a Chercheur
national, of the fonds de la recherche en sante du Quebec (FRSQ). EF is
a Tier 1 Canada Research Chair in Child Psychiatry. MSK, RWP, EF, BM,
and MD are members of the Research Institute of the McGill University
Health Centre, which is supported in part by the FRSQ.
3
Address correspondence to MS Kramer, The Montreal Childrens
Hospital 2300 Tupper Street (Les Tourelles) Montreal, Quebec H3H 1P3,
Canada. E-mail: michael.kramer@mcgill.ca.
Received May 1, 2009. Accepted for publication July 12, 2009.
First published online August 26, 2009; doi: 10.3945/ajcn.2009.28021.

Am J Clin Nutr 2009;90:10704. Printed in USA. 2009 American Society for Nutrition

Downloaded from ajcn.nutrition.org by guest on May 18, 2016

ABSTRACT
Background: Despite the current World Health Organization
recommendation that infants be exclusively breastfed for 6 mo,
this practice remains unusual in both developed and developing
countries.
Objective: The objective was to compare health and development
outcomes at age 6.5 y in children who were exclusively breastfed
for 3 mo (EBF3) or for 6 mo (EBF6); in the EBF3 group, the
children continued partial breastfeeding for 6 mo.
Design: This was a prospective cohort study nested within a large,
cluster-randomized trial of a breastfeeding promotion intervention
in the Republic of Belarus. Outcomes compared at 6.5 y included
anthropometric measurements, systolic and diastolic blood pressure,
intelligence quotient, teachers ratings of academic performance,
parent- and teacher-rated behavior, atopic symptoms, allergen
skin-prick tests, and dental caries. All statistical analyses were adjusted for cluster- and individual-level covariates and for clustering
of outcomes within the clinics at which the children were examined.
Results: The 2427 EBF3 and 524 EBF6 children who were followed up represented 84.7% and 89.4%, respectively, of those followed for the first year of life. The only significant differences
observed between the 2 groups were in mean body mass index,
triceps skinfold thickness, and hip circumference, all of which were
higher in the EBF6 group.
Conclusions: We observed no demonstrable beneficial or adverse
long-term effects on child health of exclusive breastfeeding for
6 mo. Higher adiposity measures in the EBF6 group probably reflect
reverse causality rather than a causal effect of prolonged exclusive
breastfeeding. Established benefits appear to be limited to the period
of exclusive breastfeeding.
Am J Clin Nutr 2009;90:10704.

1071

EXCLUSIVE BREASTFEEDING FOR 3 OR 6 MO

TABLE 1
Baseline characteristics of the mothers and of the infants exclusively
breastfed for 3 mo (EBF3) or for 6 mo (EBF6)
Variable

EBF6
(n = 524)

313 (12.9)
2021 (83.3)
93 (3.8)

65 (12.4)
437 (83.4)
22 (4.2)

93 (3.8)
737 (30.4)
1199 (49.4)

21 (4.0)
166 (31.7)
261 (49.8)

398 (16.4)
96 (4.0)

76 (14.5)
41 (7.8)1

1387
840
200
33
278

(57.1)
(34.6)
(8.2)
(1.4)
(11.5)

1229 (50.6)
39.4 6 1.03
3447 6 416
52.0 6 2.1
35.2 6 1.4
8.6 6 0.7
6.2 6 0.6
61.0 6 2.4
40.6 6 1.4

266 (50.8)
212 (40.5)
46 (8.8)
5 (1.0)
54 (10.3)
255 (48.7)
39.5 6 0.9
3442 6 404
51.7 6 2.21
34.8 6 1.71
8.5 6 0.64
6.2 6 0.7
60.9 6 2.5
40.5 6 1.6

Significantly different from EBF3: 1P , 0.001, 4P , 0.01.

Significant difference between EBF3 and EBF6, P , 0.05.
Mean 6 SD (all such values).

1,4
2
3

affiliated polyclinics (ie, the outpatient clinics where children are

followed for routine health care) were randomly assigned to
receive a breastfeeding promotion intervention modeled on the
WHO/UNICEF Baby-Friendly Hospital Initiative (experimental
group) or to continue the maternity hospital and polyclinic
practices in effect at the time of randomization (control group).
Healthy term newborns weighing 2500 g at birth were enrolled
during their postpartum hospital stay. Detailed information on
infant feeding and on infant outcomes was obtained during the
polyclinic study visits at 1, 2, 3, 6, 9, and 12 mo of age.
The classification of degree of breastfeeding was based on
WHO definitions (16). We classified infants as exclusively
breastfed at 3 mo if the cross-sectional feeding information
obtained at 1, 2, and 3 mo indicated that no liquid or solid foods
other than breast milk were administered to the infant. They were
considered to be exclusively breastfed at 6 mo if, in addition to
the above criteria, the child was not receiving any other liquid or
solid foods at the time of the 6-mo visit. The 2 groups compared
were 1) EBF3, those who were exclusively breastfed for 3 mo
with continued partial breastfeeding to 6 mo, and 2) EBF6,
those who were exclusively breastfed for 6 mo. Feeding beyond 6 mo did not affect these group assignments.
At the age of 6.5 y, children were followed up by their
polyclinic pediatricians. At that visit, the pediatricians obtained

Outcome
Height (cm)
Leg length (cm)
Head circumference
(cm)
BMI (kg/m2)
Triceps skinfold
thickness (mm)
Subscapular skinfold
thickness (mm)
Waist circumference
(cm)
Hip circumference
(cm)
Systolic blood
pressure (mm Hg)
Diastolic blood
pressure (mg Hg)
1
2

EBF31
(n = 2427)

EBF61
(n = 524)

Adjusted
difference,
EBF6 EBF3
(95% CI)2

120.6 6 5.0
54.9 6 4.1
51.9 6 1.5

120.7 6 5.3
55.1 6 3.5
52.0 6 1.5

0.1 (20.4, 0.6)

0.1 (20.4, 0.5)
0.1 (20.1, 0.3)

15.6 6 1.7
10.2 6 3.8

15.8 6 1.9
11.1 6 4.2

0.3 (0.1, 0.4)

0.4 (0.03, 0.8)

5.9 6 2.2

6.4 6 2.7

0.2 (20.02, 0.5)

54.5 6 4.2

54.5 6 4.5

0.4 (20.01, 0.9)

63.0 6 4.7

63.5 6 4.8

0.6 (0.1, 1.1)

97.8 6 9.1

99.1 6 9.7

0.0 (21.0, 0.9)

57.3 6 7.6

58.3 6 7.5

20.3 (21.2, 0.5)

All values are means 6 SDs.

Based on linear mixed models.

detailed anthropometric measurements and systolic and diastolic

blood pressure, all in duplicate with average of the 2 measurements made (13). Atopic symptoms and diagnoses were elicited
by using the International Study of Asthma and Allergy in
Childhood questionnaire, and skin-prick tests were performed by
using standard techniques with allergens to house dust mite, cat
dander, birch pollen, mixed northern grasses, and Alternaria (11).
Cognitive ability was assessed by using the Wechsler Abbreviated Scales for Intelligence, which comprises 4 subtests of the
well-known Wechsler scales, which were translated from English
to Russian and back-translated from Russian to English (15). The
training and monitoring of the pediatricians who administered
the intelligence quotient (IQ) tests were assured by child psychologists and psychiatrists at a week-long training workshop
before study implementation, using a convenience sample of
children who lived in a residential facility in Minsk, the capital of
Belarus.
In addition, teachers, who were blind to the feeding history and
the randomized treatment allocation, rated children in reading,
writing, mathematics, and other subjects for those children who
had begun school by the time of the follow-up visit (15). The
children were rated on a 5-point scale as far below, somewhat
below, at, somewhat above, or far above grade level. Parents
(usually the mother) and teachers both completed the Strength
and Difficulties Questionnaire, which contains 25 items and
provides quantitative assessments of total difficulties as well as
the following 5 subscales: conduct problems, hyperactivity/inattention, emotional symptoms, peer problems, and prosocial
behavior (14). Finally, a dental examination was carried out by
a public health dentist at age 6 y; the total number of teeth and of
incisors and the number of decayed, missing and filled teeth
overall and for incisors were recorded. The recorded dental

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Mothers
Maternal age at delivery [n (%)]
,20 y
2034 y
35 y
Maternal education [n (%)]
Incomplete secondary
Complete secondary
Advanced secondary or
partial university
Completed university
Positive atopic family
history [n (%)]
Older siblings [n (%)]2
0
1
2
Smoking during pregnancy [n (%)]
Cesarean delivery [n (%)]
Infants
Male [n (%)]
Gestational age (wk)
Birth weight (g)
Birth length (cm)
Birth head circumference (cm)
5-min Apgar score
Weight at 3 mo (g)
Length at 3 mo (cm)
Head circumference at 3 mo (cm)

EBF3
(n = 2427)

TABLE 2
Comparison of anthropometric and blood pressure outcomes in the
children who had been exclusively breastfed for 3 mo (EBF3) or for
6 mo (EBF6)

1072

KRAMER ET AL

TABLE 3
Comparison of cognitive and academic outcomes in children who had been
exclusively breastfed for 3 mo (EBF3) or for 6 mo (EBF6)1

Outcome

EBF3

EBF6

20.3
20.1
20.5
20.7
20.3
21.2
20.8

(21.4,
(21.0,
(21.5,
(21.6,
(21.7,
(22.6,
(22.2,

20.07
20.07
0.00
20.07

(20.17,
(20.17,
(20.09,
(20.15,

0.8)
0.9)
0.4)
0.3)
1.2)
0.3)
0.6)

0.03)
0.02)
0.09)
0.01)

WASI, Wechsler Abbreviated Scales of Intelligence; IQ, intelligence

quotient.
2
Based on linear mixed models.
3
Mean 6 SD (all such values).

examination was extracted from the childs polyclinic chart by

the pediatrician.
We used t tests for continuous variables and chi-square tests
for categorical variables to compare the baseline variables in the
2 study groups seen at 6.5 y. The comparison of 6.5-y study
outcomes was based on linear mixed models (PROC MIXED)
for continuous outcomes and generalized linear mixed models
(PROC GLIMMIX) for dichotomous outcomes, accounting both
for cluster-level (geographic region and urban compared with
rural location) and individual-level (birth weight, maternal education, and child age at the follow-up visit) covariates. Additional covariates for the cognitive and behavioral outcomes
included the fathers educational attainment; mothers and fathers BMI for the anthropometric outcomes and blood pressure;
and maternal prenatal smoking, maternal postnatal smoking,
paternal postnatal smoking, number of older and younger siblings in the household, and atopic family history for atopic
outcomes. Within-polyclinic clustering was also accounted for
in all analyses. The results of the linear mixed models are reported as adjusted differences (EBF6 mean EBF3 mean) with
their 95% CIs, whereas the results of the generalized linear
mixed models (dichotomous outcomes) are reported as adjusted
odds ratios for EBF6 compared with EBF3 (with EBF3 as the
reference group) with their 95% CIs. All statistical analyses
were carried out with the use of SAS software (version 9; SAS
Institute Inc, Cary, NC).

RESULTS

Of the 2862 infants in the EBF3 group and 621 in the EBF6
group who were followed for the first year of life, 2427 (84.7%)
and 524 (89.4%), respectively, were seen at the 6.5-y follow-up.

DISCUSSION

We found few statistically significant differences between the

EBF3 and EBF6 groups. The findings with respect to dental
health, behavior, and atopy were not unexpected, given our
previously reported results of intention-to-treat analyses based on
the randomized intervention. The absence of significant differences in the cognitive and academic outcomes, however, contrasts with the improved cognitive outcomes observed in the
experimental group (15). The absence of additional benefit of

TABLE 4
Comparison of parent and teacher Strengths and Difficulties Questionnaire
(SDQ) results in children who had been exclusively breastfed for 3 mo
(EBF3) or for 6 mo (EBF6)

Outcome
Parent SDQ
n
Total difficulties
Emotional symptoms
Conduct problems
Hyperactivity/
inattention
Peer problems
Prosocial behavior
Teacher SDQ
n
Total difficulties
Emotional symptoms
Conduct problems
Hyperactivity/
inattention
Peer problems
Prosocial behavior
1
2

Adjusted
difference,
EBF6 EBF3
(95% CI)1

EBF3

EBF6

2419
11.2 6 5.02
2.5 6 2.0
1.6 6 1.5
4.6 6 2.3

522
11.5 6 4.8
2.6 6 2.0
1.6 6 1.4
4.8 6 2.2

2.5 6 1.6
8.3 6 1.7

2.6 6 1.6
8.4 6 1.6

2061
9.2 6 5.6
1.9 6 1.9
1.3 6 1.7
3.9 6 2.7

464
9.3 6 5.5
1.9 6 1.8
1.3 6 1.7
3.8 6 2.7

0.0
0.0
0.0
20.1

2.2 6 1.7
7.6 6 2.2

2.3 6 1.8
7.5 6 2.3

0.1 (20.1, 0.3)

20.1 (20.3, 0.2)

Based on linear mixed models.

Mean 6 SD (all such values).

0.5
0.1
0.1
0.2

(20.05, 1.0)
(20.1, 0.3)
(20.1, 0.2)
(20.02, 0.4)

0.1 (20.04, 0.3)

0.0 (20.2, 0.2)

(20.6,
(20.2,
(20.2,
(20.4,

0.6)
0.2)
0.2)
0.2)

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WASI
n
2421
523
Vocabulary
52.3 6 11.63 52.8 6 11.3
Similarities
56.1 6 9.7
56.4 6 9.0
Matrices
52.4 6 9.9
52.2 6 9.1
Block designs
56.7 6 9.3
58.0 6 9.6
Verbal IQ
107.3 6 16.1 107.8 6 15.2
Performance IQ
107.7 6 14.9 108.5 6 14.1
Full-scale IQ
108.4 6 15.0 109.2 6 14.5
Teacher
academic ratings
n
1796
400
Reading
3.26 6 0.84 3.16 6 0.85
Writing
3.21 6 0.77 3.09 6 0.78
Mathematics
3.25 6 0.79 3.21 6 0.74
Other subjects
3.32 6 0.67 3.22 6 0.65

Adjusted
difference,
EBF6 EBF3
(95% CI)2

Baseline data for the 3-mo and 6-mo study groups followed up at
6.5 y are compared in Table 1. Except for a higher prevalence of
atopic family history in the EBF6 group, differences between the
2 groups were small and few were statistically significant.
The results of the comparison of anthropometric and blood
pressure outcomes are summarized in Table 2. Children who had
been breastfed exclusively for 6 mo had slightly but statistically
significantly higher mean values for BMI, triceps skinfold
thickness, and hip circumference, but no statistically significant
differences in height or blood pressure were observed.
The results for the Wechsler Abbreviated Scales for Intelligence (IQ) outcomes and teachers ratings of academic
performance for children who had begun school at the time of
their follow-up visit are shown in Table 3. No statistically significant differences were observed.
The results for the parents and teachers evaluations of the
childrens behavior are summarized in Table 4, of the atopic
outcomes in Table 5, and of the dental outcomes in Table 6. No
statistically significant differences were observed between the
EBF3 and EBF6 groups for any of these outcomes.

1073

EXCLUSIVE BREASTFEEDING FOR 3 OR 6 MO

TABLE 5
Comparison of atopic outcomes in children who had been exclusively
breastfed for 3 mo (EBF3) or for 6 mo (EBF6)1

Outcome

1
2

EBF6

Adjusted odds
ratio
(95% CI)2
Outcome

2947
244 (10.1)

524
56 (10.7)

1.3 (0.9, 1.9)

78 (3.2)

11 (2.1)

0.8 (0.4, 1.7)

35 (1.4)
116 (4.8)

9 (1.7)
23 (4.4)

1.2 (0.6, 2.4)

1.3 (0.8, 2.1)

84 (3.5)

14 (2.7)

1.0 (0.5, 2.0)

92 (3.8)

23 (4.4)

1.1 (0.7, 2.0)

Total DMFT
Incisor DMFT
Proportion with total
DMFT 1 [n (%)]
Proportion with total
DMFT 2 [n (%)]
Proportion with incisor
DMFT 1 [n (%)]
Proportion with incisor
DMFT 2 [n (%)]

EBF3
(n = 2424)

EBF6
(n = 524)

Adjusted difference,
EBF6 EBF3,
or odds ratio
(95% CI)2

4.4 6 3.73
0.5 6 1.1
1999 (82.5)

3.9 6 3.3
0.5 6 1.1
425 (81.1)

0.0 (20.3, 0.4)

0.0 (20.1, 0.1)
0.9 (0.7, 1.2)

1868 (77.1)

390 (74.4)

0.9 (0.7, 1.1)

483 (19.9)

97 (18.5)

0.8 (0.6, 1.04)

351 (14.5)

81 (15.5)

1.0 (0.7, 1.3)

DMFT, decayed, missing, or filled teeth.

Adjusted differences based on linear mixed models; adjusted odds
ratios based on generalized linear mixed models.
3
Mean 6 SD (all such values).
2

19 (0.8)

2 (0.4)

1923
259 (13.5)
210 (10.9)
195 (10.1)
263 (13.7)

47
38
33
40

397
(11.8)
(9.6)
(8.3)
(10.1)

147 (7.6)
504 (26.2)

23 (5.8)
97 (24.4)

0.6 (0.1, 2.2)

1.0
1.1
1.2
0.8

(0.7,
(0.7,
(0.8,
(0.6,

1.5)
1.8)
1.8)
1.3)

0.9 (0.6, 1.6)

1.1 (0.8, 1.5)

ISAAC, International Study of Asthma and Allergy in Childhood.

Based on generalized linear mixed models.

6 compared with 3 mo of exclusive breastfeeding suggests that

the differences achieved by the experimental intervention can be
entirely explained by the large increase in the prevalence of
exclusive breastfeeding at 3 mo in the experimental compared
with the control groups (43.3% compared with 6.4%), with no
significant additional benefit of continuing exclusive breastfeeding to 6 mo. We emphasize, however, that the EBF3 group
continued to be partially breastfed to 6 mo, which may have
allowed the benefits of breastfeeding (be they physiologic,
psychological, or a combination thereof) to accrue to those who
had been exclusively breastfed for 3 mo. Moreover, the small
number of infants exclusively breastfed for 6 mo limited our
power to detect modest differences between the 2 feeding groups.
Although prolonged exclusive breastfeeding has been advocated as a preventive measure against obesity, we observed higher
mean BMI and other measures of adiposity in the EBF6 group
than in the EBF3 group. These findings, however, contrast with
those of our intention-to-treat analyses from PROBIT (13) and
the results of a meta-analysis of observational studies (17), which
suggest no effects of prolonged and exclusive breastfeeding. The
findings from the current analysis thus seem unlikely to represent
a true causal effect of exclusive breastfeeding for 6 mo and
suggest that the causality may have been reversed. Mothers of
infants who were already on a faster weight gain trajectory during
infancy may have therefore felt more confident (or were encouraged by family members or the pediatrician) to continue
exclusive breastfeeding, rather than to supplement breastfeeding
with formula and/or solid foods (18, 19).
The absence of any apparent benefits of 6 rather than 3 mo of
exclusive breastfeeding on the 6.5-y outcomes reported in this

study do not detract from the previously reported benefits on

reduced incidence of gastrointestinal infection between 3 and
6 mo in the EBF6 group nor the results of the previously cited
systematic review, which indicated that 6 mo of exclusive
breastfeeding provides additional benefits in terms of prolonged
postpartum amenorrhea and more rapid postpartum weight loss in
the mother (2). Thus, the overall evidence suggests overall health
benefits from exclusive breastfeeding for 6 mo, although these
benefits appear to be limited to the period during which exclusive
breastfeeding is practiced rather than to a long-term programming effect.
The authors responsibilities were as followsMSK, FA, BM, EF, J-PC,
EH, and BC: designed the study and participated in the drafting and/or revision of the manuscript; MSK, LM, NB, FA, BM, EF, IM, and SI: planned the
field work and data collection; and MSK, RWP, and MD: carried out the statistical analysis. None of the authors had any conflict of interest concerning
the topic or contents of this article.

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ISAAC Questionnaire
n
Ever had
wheezing [n (%)]
Wheezing in
past 12 mo [n (%)]
Ever had asthma [n (%)]
Ever had hay fever
symptoms [n (%)]
Hay fever symptoms in
past 12 mo [n (%)]
Recurrent itchy
rash [n (%)]
Ever had eczema [n (%)]
Skin-prick tests
n
House dust mite [n (%)]
Cat [n (%)]
Birch pollen [n (%)]
Mixed northern
grasses [n (%)]
Alternaria [n (%)]
1 Positive [n (%)]

EBF3

TABLE 6
Comparison of dental caries outcomes in children who had been
exclusively breastfed for 3 mo (EBF3) or for 6 mo (EBF6)1

1074

KRAMER ET AL

9. Kramer MS, Chalmers B, Hodnett ED, et al. Promotion of breastfeeding

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associated with 3 compared with 6 months of exclusive breastfeeding.
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pressure at age 6.5 years: new evidence from a large randomized trial.
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