American Journal of Epidemiology

American Journal of Epidemiology Advance Access originally published online on August 2, 2005
American Journal of Epidemiology 2005 162(5):397-403; doi:10.1093/aje/kwi222

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American Journal of Epidemiology Copyright © 2005 by the Johns Hopkins Bloomberg School of Public Health All rights reserved

META-ANALYSIS

Duration of Breastfeeding and Risk of Overweight: A Meta-Analysis

Thomas Harder¹, Renate Bergmann¹, Gerd Kallischnigg² and Andreas Plagemann¹

¹ Clinic of Obstetrics, Division of Experimental Obstetrics, Charité—University Medicine, Berlin, Germany
² Epidemiology Research Group, Institute of Public Health, Technical University, Berlin, Germany

Reprint requests to Dr. Thomas Harder, Clinic of Obstetrics, Division of Experimental Obstetrics, Campus Virchow-Klinikum, Charité—University Medicine Berlin, Augustenburger Platz 1, 13353 Berlin, Germany (e-mail: thomas.harder{at}charite.de).

Received for publication January 13, 2005. Accepted for publication May 3, 2005.

	ABSTRACT

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION References

 
Observational studies suggest a longer duration of breastfeeding to be associated dose dependently with a decrease in risk of overweight in later life. The authors performed a comprehensive meta-analysis of the existing studies on duration of breastfeeding and risk of overweight. Studies were included that reported the odds ratio and 95% confidence interval (or the data to calculate them) of overweight associated with breastfeeding and that reported the duration of breastfeeding and used exclusively formula-fed subjects as the referent. Seventeen studies met the inclusion criteria. By meta-regression, the duration of breastfeeding was inversely associated with the risk of overweight (regression coefficient = 0.94, 95% confidence interval (CI): 0.89, 0.98). Categorical analysis confirmed this dose-response association (<1 month of breastfeeding: odds ratio (OR) = 1.0, 95% CI: 0.65, 1.55; 1–3 months: OR = 0.81, 95% CI: 0.74, 0.88; 4–6 months: OR = 0.76, 95% CI: 0.67, 0.86; 7–9 months: OR = 0.67, 95% CI: 0.55, 0.82; >9 months: OR = 0.68, 95% CI: 0.50, 0.91). One month of breastfeeding was associated with a 4% decrease in risk (OR = 0.96/month of breastfeeding, 95% CI: 0.94, 0.98). The definitions of overweight and age had no influence. These findings strongly support a dose-dependent association between longer duration of breastfeeding and decrease in risk of overweight.

body weight; breast feeding; meta-analysis; obesity

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Abbreviations: CI, confidence interval; OR, odds ratio

	INTRODUCTION

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION References

 
The prevalences of overweight and obesity are increasing nearly worldwide. Therefore, a high priority has been given to research strategies to prevent the development of obesity. We have published a meta-analysis (1, 2) that showed breastfeeding, compared with formula feeding, to be associated with a decreased risk of overweight. Recently, this finding was confirmed by others (3). However, neither study investigated whether a relation exists between the duration of breastfeeding and the risk of overweight. This issue is of particularly high importance since it might support the causality of this association. Furthermore, it is highly relevant to clinical practice to know whether a longer duration of breastfeeding could lead to a stronger decrease in risk of overweight in later life. Therefore, we performed a meta-analysis of the relation between the duration of breastfeeding and the risk of overweight.

	MATERIALS AND METHODS

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION References

 
Study base
The meta-analysis was conducted according to the checklist of the Meta-analysis of Observational Studies in Epidemiology (MOOSE) group (4). We performed a literature search including the databases MEDLINE (US National Library of Medicine's database accessed through PubMed, 1966 through December 2003), CINAHL (Cumulative Index to Nursing and Allied Health Literature, 1982 through December 2003), SERFILE (bibliographic information on biomedical and health science serials, 2002–2003), and EMBASE (the Excerpta Medica database, 1989 through December 2003), using the terms breastfeeding, infant nutrition, weaning, overweight, obes* (truncated), and adipos* (truncated) in the full-text option, without language restrictions. Furthermore, a manual search was carried out on all the references cited in published original studies and in all reviews identified by the literature search (5–17). To be eligible, studies had to fulfill the following three inclusion criteria: 1) be an original report comparing breastfed subjects with exclusively formula-fed subjects (referent group) of any given age, 2) report the odds ratio and 95 percent confidence interval (or data to calculate them) of overweight or obesity associated with breastfeeding, and 3) report the duration of breastfeeding for at least one exposure group. Any definition of overweight or obesity was allowed. From review of the abstracts identified in the search, 49 articles were subjected to full review; 33 of these studies were excluded since they did not fulfill the inclusion criteria (18 studies did not provide data to calculate the odds ratio, nine studies did not use exclusively formula-fed probands as the referent, and six studies did not report the duration of breastfeeding). Details are available on request.

Of the 16 original reports that met the inclusion criteria (18–33), one consisted of two independent studies (24), so that 17 studies (16 cohort studies, one case-control study) were included in this meta-analysis. From these reports, data were abstracted in duplicate, using a standardized form.

Statistical analysis
Unadjusted odds ratios and 95 percent confidence intervals were calculated directly from the data given in the articles, where possible. Otherwise, the published odds ratio and 95 percent confidence interval were used. We used three different approaches to investigate by means of meta-analytical techniques whether a relation exists between the duration of breastfeeding and the risk of overweight. First, a weighted meta-regression was performed (34), using the duration of breastfeeding as the independent variable and the weighted odds ratio for overweight in breastfed probands, compared with formula-fed subjects, as the dependent variable. Second, the pooled odds ratio for overweight in breastfed subjects was calculated separately for five predefined categories of duration of breastfeeding. Third, the pool-first method (35) was used to combine the regression coefficients obtained from the studies.

Meta-regression analysis.
For meta-regression analysis, all duration-specific odds ratios had to be related to the respective duration of breastfeeding. Since the duration of breastfeeding was reported as categorical data with a certain range in the studies (e.g., 1–3 months, 4–6 months, and so on), the median of the upper and lower limits of each category was assigned to the particular estimate in each study (35). Estimates were plotted against the respective duration of breastfeeding as the independent variable. Since the scatterplot revealed a linear relation, a weighted meta-regression (34) with duration of breastfeeding as the covariate was performed (random-effects model). The regression coefficient with its 95 percent confidence interval was delogarithmized for data presentation.

Categorical analysis.
A pooled odds ratio for overweight in breastfed subjects was calculated for the five separate predefined categories of duration of breastfeeding: less than 1 month, 1–3 months, 4–6 months, 7–9 months, and more than 9 months. Since the Cochrane Q-based test revealed significant heterogeneity in each case, a random-effects model was used throughout.

Trend estimation.
To studies that provided data for more than two categories of duration of breastfeeding, we applied the "pool-first method" (35) to quantify the dose-response relation. This was possible for 11 studies (19–23, 25, 28–32). After visual inspection of the plots to ascertain model adequacy, we calculated a study-specific regression coefficient and corresponding 95 percent confidence interval for each study by use of a log-linear model. After exponentiation, the resulting odds ratio and 95 percent confidence interval for change in risk for each month of breastfeeding were pooled with a random-effects model.

Subgroup analysis.
Two subgroup analyses were performed. First, we calculated separate estimates for all studies that used body mass index to measure overweight and for all that did not. Second, age-specific estimates were pooled in the predefined subgroups 0–5 years and 6 or more years by the random-effects model.

Publication bias and statistical software.
Publication bias was assessed by inspection of the funnel plot and by formal testing for funnel plot asymmetry using the Begg test and the Egger test. Calculations were performed using STATA, version 8, software (Stata Corporation, College Station, Texas).

	RESULTS

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION References

 
Study characteristics of included reports are displayed in tables 1 and 2. From the 17 studies that reported duration of breastfeeding, 14 gave data for more than one category of duration of breastfeeding, leading to 52 estimates included in the meta-regression analysis. Visual inspection of the scatterplot revealed that the relation between duration of breastfeeding and risk of overweight was linear. In the weighted meta-regression, duration of breastfeeding was significantly negatively related to risk of overweight (regression coefficient: 0.94, 95 percent confidence interval (CI): 0.89, 0.98) (figure 1).

View this table: [in this window] [in a new window]   TABLE 1. Characteristics of the 17 studies, ordered alphabetically by first author, that are included in this meta-analysis, according to origin, design, data source, age, study size, loss to follow-up, exposure assessment method, and type of breastfeeding

 

View this table: [in this window] [in a new window]   TABLE 2. Characteristics of the 17 studies, ordered alphabetically by first author, that are included in this meta-analysis, according to duration of breastfeeding, outcome assessment, definition of overweight/obesity, and confounders

 

View larger version (13K): [in this window] [in a new window]   FIGURE 1. Scatterplot and meta-regression line of log odds ratio of risk of overweight/obesity associated with breastfeeding, according to duration of breastfeeding. A total of 17 studies provided 52 estimates of duration of breastfeeding and overweight. Weighted meta-regression revealed a significant inverse linear relation between the duration of breastfeeding and the risk of overweight (regression coefficient = 0.94, 95% confidence interval: 0.89, 0.98).

 
Table 3 shows the results of categorical analysis. From 1 month of breastfeeding onward, the risk of subsequent overweight continuously decreased up to a reduction of more than 30 percent, reaching a plateau at 9 months of breastfeeding.

View this table: [in this window] [in a new window]   TABLE 3. Duration of breastfeeding and risk of overweight: categorial analysis (random-effects model)

 
Figure 2 shows the forest plot with odds ratio and 95 percent confidence interval and the pooled estimate for the reduction in risk of overweight for each month of breastfeeding, calculated from trend analysis by a random-effects model. Each month of breastfeeding was found to be associated with a 4 percent decrease in risk (odds ratio (OR) = 0.96/month of breastfeeding, 95 percent CI: 0.94, 0.98). A fixed-effects model revealed a similar pooled odds ratio and a nearly identical 95 percent confidence interval (OR = 0.96, 95 percent CI: 0.95, 0.98).

View larger version (12K): [in this window] [in a new window]   FIGURE 2. Odds ratios (with corresponding 95% confidence intervals in parentheses) for overweight, per month of breastfeeding. Studies are ordered alphabetically by first author. The pooled or "combined" odds ratio (OR) was calculated by a random-effects model.

 
In only two of these studies (22, 31) was the influence of the duration of exclusive breastfeeding analyzed. The pooled odds ratio for risk of overweight per month of exclusive breastfeeding was 0.94 (95 percent CI: 0.89, 0.99; random-effects model).

Subgroup analyses revealed that the definition of overweight influenced the estimate only slightly. In studies that used body mass index to define overweight, the pooled odds ratio was 0.96 (95 percent CI: 0.94, 0.98) for eight studies, while the odds ratio was 0.93 (95 percent CI: 0.87, 0.99) for the three studies that used another measure to define overweight or obesity. Similarly, the age at examination had only a marginal influence on the magnitude of the effect of duration of breastfeeding on risk of overweight. The pooled odds ratio from all five studies investigating probands up to or including 5 years of age was 0.97 (95 percent CI: 0.94, 0.99), while in older subjects aged 6 or more years, it was 0.96 (95 percent CI: 0.93, 0.99) for six studies. No evidence of publication bias was observed, as indicated by a symmetric funnel plot (not shown) and a nonsignificant Begg test (p = 0.64) and Egger test (p = 0.77).

	DISCUSSION

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION References

 
Using three different techniques, we show that a longer duration of breastfeeding is associated with a larger decrease in risk of overweight. Each of the three methods used in our study has its own advantages and limitations. Meta-regression analysis is known to be highly flexible with regard to the shape of the dose-response relation (34). However, the duration-specific estimates from one study are not completely independent from each other as they have the same referent category in each case, which could bias the result. This disadvantage can be at least partly overcome by the use of separate categories of duration of breastfeeding. However, because of the smaller sample sizes in some of the categories, the power of the statistical analysis might be limited. The "pool-first method" (35) is highly flexible with regard to the shape of the dose-response-relation, and it ensures complete independence of all included estimates. However, as a minimum of three categories is needed to calculate the study-specific regression coefficient in the log-linear model, in the case of our meta-analysis, the use of this technique had to be restricted to studies from which study-specific regression coefficients could be calculated. Nevertheless, in essence, all three methods came to the same result of an inverse linear association between duration of breastfeeding and risk of overweight in later life. However, it has to be considered that all studies performed until now on breastfeeding and risk of overweight are secondary analyses of health surveys or of studies designed primarily to answer different questions.

One major methodological problem to overcome in a meta-analysis of breastfeeding and risk of overweight is the change of the definition of overweight over time. Following the proposal of the Meta-analysis of Observational Studies in Epidemiology group (4), we included any definition of overweight and investigated the possible consequences of this strategy by subgroup analysis. In fact, the definition of overweight had only a minor impact on the pooled estimate.

Eight of the studies (18, 22, 24–27, 31, 32) gave duration-specific, confounder-adjusted estimates, some only for subsets of the data. Because of this small sample size and considering the fact that the type and number of confounders differed largely among these studies, we did not calculate a pooled estimate of the confounder-adjusted odds ratio. Remarkably, only three (19, 21, 22) of the 17 studies gave some basic information on ethnicity, mostly by declaring a "mixed" ethnic background of the population. Therefore, it is unclear to date whether the effect of breastfeeding on risk of overweight is restricted to certain ethnic groups and might be confounded by social class. Taken together, a statistically based decision on the role of confounding could not be derived from the data here. However, Savitz (36) has postulated that, in general, the existence of a dose-response relation reduces the likelihood of an association to be completely due to confounding, since increasingly implausible scenarios are required for the exposure-confounder association to exaggerate the dose-response gradient.

The mechanisms by which breastfeeding affects the risk of overweight are still unclear. Breastfeeding results in a lower body weight gain during the critical neonatal period, obviously caused by a lower mean caloric intake in breastfed infants, compared with formula-fed neonates (37). A lower body weight gain during neonatal life has been shown to lead to decreased risk of obesity in adolescence and adulthood (38). In animal experiments, the kind of neonatal nutrition was shown to influence the development of neuroendocrine circuits in the mediobasal hypothalamus that regulates appetite control and body weight, with long-term consequences for risk of obesity (for review, refer to reference 39). These mechanisms might also explain why a longer duration of breastfeeding is associated with a stronger decrease in risk of overweight in later life.

In summary, we found that the duration of breastfeeding is inversely and linearly associated with the risk of overweight. The risk of overweight was reduced by 4 percent for each month of breastfeeding. This effect lasted up to a duration of breastfeeding of 9 months and was independent of the definition of overweight and age at follow-up. Even if interpreted as being of relatively small size, this association, if causal, might be of importance for the general population. Since the majority of studies analyzed here used partially breastfed subjects, it might be concluded that, beyond exclusive breastfeeding, also longer partial breastfeeding up to 9 months leads to a greater decrease in risk of overweight in later life, which might be considered in future clinical recommendations.

	ACKNOWLEDGMENTS

 
Conflict of interest: none declared.

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TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION References

 

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