Infant growth and health outcomes

associated with 3 compared with 6 mo of

exclusive breastfeeding1,2,3
1. Michael S Kramer,
2. Tong Guo,
3. Robert W Platt,
4. Zinaida Sevkovskaya,
5. Irina Dzikovich,
6. Jean-Paul Collet,
7. Stanley Shapiro,
8. Beverley Chalmers,
9. Ellen Hodnett,
10. Irina Vanilovich,
11. Irina Mezen,
12. Thierry Ducruet,
13. George Shishko, and
14. Natalia Bogdanovich
+ Author Affiliations
1.
1
From the Departments of Pediatrics (MSK, RWP, and J-PC) and Epidemiology and
Biostatistics (MSK, TG, RWP, J-PC, SS, and TD), McGill University Faculty of
Medicine, Montreal; the Centre for Research in Womens Health (BC), Sunnybrook
Womens College Health Sciences Centre (BC), and Faculty of Nursing (EH), University
of Toronto; the Departments of Maternal and Child Health (ZS) and Foreign Relations
(IM), Belarussian Ministry of Health, Minsk, Belarus; and the Belarussian Maternal and
Child Health Research Institute (ID, IV, GS, and NB), Minsk, Belarus.

Next Section
Abstract
Background: Opinions and recommendations about the optimal duration of exclusive
breastfeeding have been strongly divided, but few published studies have provided direct
evidence on the relative risks and benefits of different breastfeeding durations in recipient
infants.
Objective: We examined the effects on infant growth and health of 3 compared with 6 mo of
exclusive breastfeeding.
Design: We conducted an observational cohort study nested within a large randomized trial in
Belarus by comparing 2862 infants exclusively breastfed for 3 mo (with continued mixed
breastfeeding through 6 mo) with 621 infants who were exclusively breastfed for 6 mo.
Regression to the mean, within-cluster correlation, and cluster- and individual-level confounding
variables were accounted for by using multilevel regression analyses.
Results: From 3 to 6 mo, weight gain was slightly greater in the 3-mo group [difference: 29
g/mo (95% CI: 13, 45 g/mo)], as was length gain [difference: 1.1 mm (0.5, 1.6 mm)], but the 6-
mo group had a faster length gain from 9 to 12 mo [difference: 0.9 mm/mo (0.3, 1.5 mm/mo)]
and a larger head circumference at 12 mo [difference: 0.19 cm (0.07, 0.31 cm)]. A significant
reduction in the incidence density of gastrointestinal infection was observed during the period
from 3 to 6 mo in the 6-mo group [adjusted incidence density ratio: 0.35 (0.13, 0.96)], but no
significant differences in risk of respiratory infectious outcomes or atopic eczema were apparent.
Conclusions: Exclusive breastfeeding for 6 mo is associated with a lower risk of gastrointestinal
infection and no demonstrable adverse health effects in the first year of life.
Breastfeeding
gastrointestinal infection
respiratory infection
growth
atopic eczema
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INTRODUCTION
The debate over the optimal duration of exclusive breastfeeding has been long and heated. The
belief that breast milk alone is nutritionally insufficient after 3 or 4 mo, combined with the fact
that weaning foods given in many developing countries are both nutritionally inadequate and
contaminated, has given rise to the so-called weanlings dilemma(1,2). Breastfeeding is a life-
and-death issue in developing countries; a recent meta-analysis reported markedly reduced
mortality (especially mortality due to infectious disease) with breastfeeding, even into the second
year of life (3).
In most developed countries, however, uncontaminated, nutritionally adequate complementary
foods are readily available, and growth faltering is relatively uncommon. With the resurgence of
breastfeeding initiation in developed countries, recent attention has turned to the importance of
promoting its duration and exclusivity. The epidemiologic evidence is now overwhelming that,
even in developed countries, breastfeeding protects against gastrointestinal and (to a lesser
degree) respiratory infection and that the protective effect is enhanced with greater duration and
exclusivity of breastfeeding (4,8).
Although growth faltering is uncommon in developed countries, available data indicate that
infants following recent World Health Organization (WHO) feeding recommendations (ie, to
exclusively breastfeed until 46 mo of age and to continue breastfeeding with added
complementary foods up to 2 y of age) show a deceleration in both weight and length gains
relative to the international WHO/Centers for Disease Control and Prevention (CDC) growth
reference from 3 to 12 mo, with partial catch-up thereafter (9,13).
In the past few years, a split has developed concerning the recommended optimal duration of
exclusive breastfeeding. Until May 2001, the WHO recommended exclusive breastfeeding for 4
6 mo (14), while the United Nations Childrens Fund (UNICEF) recommended exclusive
breastfeeding for 6 mo (15). This difference led to vigorous and often acrimonious debate, not
only between the 2 United Nations agencies but also in the larger infant nutrition and public
health communities (16). The American Academy of Pediatrics has been ambivalent about this
issue; in 2 different sections of their 1998 Pediatric Nutrition Handbook (17), they alternatively
recommend human milk as the exclusive nutrient source during the first 6 mo (page 18) and
to delay introduction of solid foods until 4 to 6 mo (page 38). Because of the ongoing
controversy and polarization with respect to this issue, we carried out an observational cohort
study nested within a large randomized trial in the Republic of Belarus in an attempt to identify
the health effects of these alternative approaches to infant feeding.
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SUBJECTS AND METHODS
The methods undertaken in the Promotion of Breastfeeding Intervention Trial (PROBIT) are
described in detail in previous publications (18,19). Briefly, 31 maternity hospitals and 1 each of
their affiliated polyclinics (ie, the 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, breastfed, term newborns weighing 2500 g at birth were enrolled during their
postpartum hospital stay. Follow-up data were collected at polyclinic visits at 1, 2, 3, 6, 9, and 12
mo; home visits were made when a polyclinic visit was missed. At each of these visits, we
obtained data on infant feeding, illness, and growth. Because differences in growth were not
major hypotheses of PROBIT, which focused on reductions in infection and atopic eczema
(18,19), no attempts were made to standardize measurements of weight, length, and head
circumference.
Classification of the degree of breastfeeding was based on WHO definitions. 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 being
administered to the infant. An infant was considered to be exclusively breastfed at 6 mo if, in
addition to the above criteria, he or she was not receiving any other liquid or solid foods at the 6-
mo visit. (Although the controversy about the optimal duration of exclusive breastfeeding
concerns whether to breastfeed for 4 or 6 mo, we did not collect infant feeding information at 4
mo; therefore, our comparison was between breastfeeding durations of 3 and 6 mo.)
A total of 17 046 subjects were recruited from the 31 randomized sites; 555 (3.3%) subjects were
lost to follow-up before 12 mo. A 32nd site was also originally to be included as part of the
study, but it was excluded because of documented falsification of outcome data (18,19). Of the
entire randomly assigned cohort, 2862 infants were exclusively breastfed for 3 mo and were
introduced nonbreast milk liquids, solids, or both by 6 mo of age but continued to partially
breastfeed through 6 mo; 621 infants were exclusively breastfed for 6 mo. These 2 subcohorts
made up the subjects studied in this observational analysis and are referred to as the 3-mo and 6-
mo groups, respectively.
We used the algorithms of Rubin et al (20) to classify gastrointestinal and upper respiratory
infection, which were modified to ensure a minimum duration of infection of 2 d. Other types of
respiratory infections under study included croup, otitis media, wheezing, and pneumonia;
subjects were classified as having one of these infections if the infection had been diagnosed by
the chief polyclinic pediatrician and if the duration of infection was 2 d. Rashes were
considered to represent atopic eczema if they lasted 2 wk or recurred after clearing for 1 wk,
were itchy, and occurred on the face or extensor surfaces of the arms or the extensor surfaces of
the legs. Audits for the recorded data on any breastfeeding duration 3 mo, 1 episode of
gastrointestinal infection, and 2 episodes of respiratory infection were conducted on 20
polyclinic charts and 10 maternal interviews that were randomly selected by the investigators
from each study site. The results of these audits showed high concordance between the data from
the PROBIT forms and both the polyclinic chart and maternal interview data; no differences in
under- or overreporting were observed between the experimental and control sites (18,19).
We compared the 2 study groups at baseline and at 3 mo with the use of t tests for continuous
variables and chi-square tests for categorical variables. The primary analysis of study outcomes
was based on linear mixed models (PROC MIXED) for continuous (growth) outcomes and
generalized linear mixed models (PROC GLIMMIX) for dichotomous outcomes, accounting for
both cluster-level (geographic region, urban compared with rural location, and hospital) and
individual-level (birth weight, maternal education, and number of siblings in the household)
covariates. Weight-for-age, length-for-age, and weight-for-length z scores were calculated by
using EPIINFO 2000 (CDC, Atlanta) based on the sex- and age-specific WHO/CDC reference
(21). The mixed models for growth outcomes controlled for anthropometric measures from birth
to 3 mo (to control for regression to the mean) and accounted for within-cluster (within-hospital)
correlation and for the repeated-measures nature of these outcomes. Maternal smoking (any
smoking during pregnancy) was also included as an individual-level covariate for analysis of
respiratory tract infection. Finally, for analysis of atopic eczema, family atopic history (a positive
history of asthma, allergic rhinitis, or atopic eczema in the mother, the father, or a sibling) was
also included as an individual-level covariate. The results of the PROC MIXED models are
reported as adjusted differences (and the 95% CIs), whereas those for GLIMMIX models are
reported as adjusted odds ratios (and the 95% CIs). Incidence density ratios (IDRs) and their
95% CIs were estimated according to Poisson modeling within GLIMMIX by using the same
cluster- and individual-level covariates listed above. All statistical analyses were carried out with
the use of SAS software (version 8.2; SAS Institute, Inc, Cary, NC).
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RESULTS
At baseline, infants who were exclusively breastfed for 3 mo were not significantly different
from the other PROBIT infants who were not exclusively breastfed for 3 mo with respect to
mean birth weight (3442 compared with 3437 g, respectively), birth length (51.9 cm for both),
and head circumference (35.1 compared with 34.9 cm, respectively). Maternal age, family atopic
history, and number of other children at home were also not significantly different between the 2
groups (data not shown). Not surprisingly, however, mothers who did not exclusively breastfeed
their infants for 3 mo were less well-educated (12.8 compared with 16.6% completed
university; P < 0.0001) and were more likely to smoke cigarettes during pregnancy (2.5%
compared with 1.5%; P < 0.001).
Baseline data for the 3-mo and 6-mo study groups are compared in Table 1. No significant
differences between the 2 groups were observed, except for a significantly higher prevalence of
family atopic history and lower mean birth length and head circumference in the 6-mo group.
Differences in intakes of formula, juices, cereals, and other solid foods at 6 mo were observed
between the 2 groups. In the 3-mo group, 14.5% were receiving infant formula (most, 14
times/d), 83.6% were receiving juices (usually once or twice per day), 54.8% were receiving
cereals (most, 1 time/d), and 78.2% were receiving other solid foods (most, 1 time/d) at 6 mo;
only 5.2% were receiving water, 5.1% cow milk, and 0.2% other milks.
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TABLE 1
Baseline comparison of mothers and their infants exclusively breastfed for 3 or 6 mo
Weight and length gains in the 3-mo and 6-mo groups are compared in Table 2. For the period
from 3 to 6 mo, both measures were higher in the 3-mo group, ie, those infants who received
complementary foods in addition to continued breastfeeding between 3 and 6 mo. Some catch-up
in length gain occurred in the 6-mo group between 9 and 12 mo. As shown in Table 3, the
differences in weight gain were reflected in slightly (0.080.09) but significantly higher weight-
for-age z scores in the 3-mo group at 6, 9, and 12 mo, although the means remained at 0.50.6
in both groups. For length-for-age, the mean z scores were near 0 (the WHO/CDC reference
mean) at 6 and 9 mo, although they were significantly higher in the 3-mo group. By 12 mo,
however, the difference in length-for-age had disappeared, and both groups exceeded the
reference mean. Differences in weight-for-length z scores were not statistically significant at any
age.
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TABLE 2
Comparison of weight and length gains in infants exclusively breastfed for 3 or 6 mo
1

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TABLE 3
Comparison of anthropometric z scores in infants exclusively breastfed for 3 or 6 mo
1

Weight-for-age z scores < 2 were rare at all 3 ages in both groups: 0 of 620 compared with 2 of
2841 at 6 mo, 1 of 612 compared with 3 of 2796 at 9 mo, and 1 of 617 compared with 4 of 2849
at 12 mo in the 6-mo compared with the 3-mo groups, respectively. Low (< 2) length-for-age z
scores were more common, but they did not differ significantly between the 6-mo and 3-mo
groups at 6, 9, and 12 mo, respectively: 14 of 619 compared with 42 of 2841 [RR: 1.53 (95% CI:
0.84, 2.78)], 14 of 611 compared with 44 of 2795 [RR: 1.46 (95% CI: 0.80, 2.64)], and 4 of 617
compared with 28 of 2849 [RR: 0.66 (95% CI: 0.23, 1.87)], respectively. As with weight-for-
age, weight-for-length z scores <2 were also rare at all 3 ages: 0 of 619 compared with 7 of
2841 at 6 mo, 2 of 611 compared with 8 of 2795 at 9 mo, and 1 of 617 compared with 4 of 2849
at 12 mo, respectively, in the 6-mo and 3-mo groups, respectively. High (> 2) z scores were far
more common than were low z scores at all 3 ages, especially for weight-for-age and weight-for-
length, but the scores did not differ significantly between the 2 feeding groups.
Despite the slightly higher head circumference at birth in the 3-mo group (Table 1), mean (
SD) head circumference was similar in the 3-mo and 6-mo groups at 6 mo [43.44 1.46
compared with 43.34 1.53 cm; difference: 0.10 (95% CI: 0.02, 0.22) cm] and 9 mo [45.45
1.43 compared with 45.52 1.46 cm; difference: 0.06 (95% CI: 0.18, 0.06) cm]; it was
significantly higher in the 6-mo group, however, at 12 mo [47.06 1.49 compared with 47.25
1.50 cm; difference: 0.19 (95% CI: 0.31, 0.07) cm].
The incidence of atopic and infectious outcomes during the first 12 mo of life is shown in Table
4. No significant difference was observed in the risk of atopic eczema, 2 episodes of
wheezing, 2 episodes of any respiratory or upper respiratory infection, 1 episode of otitis
media, or hospitalization for respiratory infection.
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TABLE 4
Comparison of first-year incidence of atopic and infectious outcomes in infants exclusively
breastfed for 3 or 6 mo
1

The risk of one or more episodes of gastrointestinal infection was significantly lower in the 6-mo
group [adjusted OR: 0.61 (95% CI: 0.41, 0.93)], even after control for geographic origin, urban
compared with rural location, maternal education, birth weight, and number of siblings in the
household. The reduction in the risk of hospitalization for gastrointestinal infection was not
statistically significant however. To further explore the timing of the protective effect against
gastrointestinal infection, we used a Poisson model (within GLIMMIX) to estimate the adjusted
IDR during the periods 03, 36, and 612 mo; the analysis for 612 mo was restricted to those
infants who continued breastfeeding (ie, were not weaned) throughout the period. As expected,
no significant difference was observed from 0 to 3 mo (when both groups were exclusively
breastfed); the adjusted IDR in the 6-mo group was 0.97 (95% CI: 0.46, 2.04). The protective
effect was very strong during the 36-mo period [adjusted IDR: 0.35 (95% CI: 0.13, 0.96)] but
did not persist at 612 mo [adjusted IDR: 0.90 (95% CI: 0.46, 1.78)].
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DISCUSSION
The main benefit associated with exclusive breastfeeding for 6 mo compared with that associated
with exclusive breastfeeding at 3 mo was a significant reduction in the risk of gastrointestinal
infection. This benefit was limited to the actual period (from 3 to 6 mo) during which feeding
differed in the 2 study groups, ie, the protective effect did not persist beyond 6 mo but was of
substantial magnitude despite the extremely low incidence of gastrointestinal infection in both
study groups (Table 4). Continued exclusive breastfeeding for 6 mo reduced the incidence
density by nearly two-thirds from 3 to 6 mo.
Complementary feeding between 3 and 6 mo was associated with increases in both weight gain
and length gain during that period, although by 12 mo the difference in weight-for-age z score
was only 0.08, and no significant difference was observed in either length-for-age or weight-for-
length. Weight-for-age and weight-for-length z scores remained well above the reference mean
of 0 through 12 mo, which reflects both the selection criteria (inclusion of healthy newborns with
a birth weight 2500 g and a gestational age 37 wk) for participation in PROBIT (18,19) and
the rapid average weight gain of PROBIT infants (22). The latter may reflect culturally
determined infant feeding practices in Belarus.
An intriguing finding was a significantly larger head circumference at 12 mo in the 6-mo group.
This difference was small (0.19 cm), however, and may have occurred by chance. Whether the
difference will persist over time and whether it is associated with the previously reported benefits
in neurocognitive function associated with prolonged breastfeeding (23,29) is uncertain but will
be an important focus of the future follow-up of PROBIT infants.
Despite the substantially and significantly lower risk of atopic eczema associated with random
assignment to the experimental intervention in our initial trial (19), no significant difference was
observed for this outcome (or for recurrent wheezing) in the observational comparison of infants
in the 3-mo and 6-mo groups. When combined with the results of our trial, these observational
findings suggest that exclusive breastfeeding for 3 mo with continued breastfeeding through 6
mo provides equivalent protection against atopic eczema to exclusive breastfeeding for 6 mo.
These data are consistent with those from other studies included in a recent systematic review
including longer-term atopic outcomes (especially asthma) as well (30).
Two important limitations of our study should be mentioned. First, although PROBIT was
designed as a randomized trial, the study groups reported herein are based on an observational
design. In other words, randomized allocation has been ignored in these analyses and, thus,
residual confounding might theoretically have biased our results. Second, anthropometric
measurements were not standardized among study sites (see Subjects and Methods); the
increased (random) error in measuring weight, length, and head circumference should have been
nondifferential and therefore might have reduced the observed differences in growth outcomes
between the 2 study groups.
In summary, Belarussian infants breastfed exclusively for 6 mo had a significantly lower
incidence and incidence density of gastrointestinal infection between 3 and 6 mo of age than did
infants exclusively breastfed for 3 mo (with continued mixed breastfeeding through 6 mo);
morbidity due to respiratory infection and atopic eczema in the first year of life was not
significantly different between the 2 groups. No persistent benefits of introducing
complementary foods between 3 and 6 mo were shown. We observed more rapid weight and
length gains between 3 and 6 mo in infants who were introduced to complementary foods
between 3 and 6 mo, but little difference remained by 12 mo. Combined with other evidence that
was recently systematically reviewed (30), there are no apparent risks in recommending, as a
general policy, exclusive breastfeeding for the first 6 mo of life. Thus, our findings support the
World Health Assemblys recently revised infant feeding recommendation that mothers
exclusively breastfeed their infants for 6 mo (31). Future follow-up of the PROBIT cohort should
provide information about possible long-term consequences of these differences in duration of
exclusive breastfeeding.
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Acknowledgments
MSK, ZS, ID, J-PC, SS, BC, EH, GS, and IM participated in the study design. ID, IV, GS, NB,
and TD collected the data. TG, TD, MSK, RWP, J-PC, and SS analyzed the data. MSK, RWP, J-
PC, SS, BC, and EH wrote the manuscript. None of the authors had any financial or personal
interest in any company or organization sponsoring the research.
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Footnotes
2 Supported by grants from the Thrasher Research Fund, the National Health Research
Development Program (Health Canada), UNICEF, and the Department of Nutrition for
Health and Development, World Health Organization, Geneva.
3 Reprints not available. Address correspondence to MS Kramer, 1020 Pine Avenue
West, Montreal, Quebec, Canada H3A 1A2. E-mail: michael.kramer@mcgill.ca.
Received October 1, 2002.
Accepted January 15, 2003.
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