Abstract
This study aimed to examine the association between breastfeeding and childhood obesity. A multinational cross‐sectional study of 4,740 children aged 9–11 years was conducted from 12 countries. Infant breastfeeding was recalled by parents or legal guardians. Height, weight, waist circumference, and body fat were obtained using standardized methods. The overall prevalence of obesity, central obesity, and high body fat were 12.3%, 9.9%, and 8.1%, respectively. After adjustment for maternal age at delivery, body mass index (BMI), highest maternal education, history of gestational diabetes, gestational age, and child's age, sex, birth weight, unhealthy diet pattern scores, moderate‐to‐vigorous physical activity, sleeping, and sedentary time, exclusive breastfeeding was associated with lower odds of obesity (odds ratio [OR] 0.76, 95% confidence interval, CI [0.57, 1.00]) and high body fat (OR 0.60, 95% CI [0.43, 0.84]) compared with exclusive formula feeding. The multivariable‐adjusted ORs based on different breastfeeding durations (none, 1–6, 6–12, and > 12 months) were 1.00, 0.74, 0.70, and 0.60 for obesity (P trend = .020) and 1.00, 0.64, 047, and 0.64 for high body fat (P trend = .012), respectively. These associations were no longer significant after adjustment for maternal BMI. Breastfeeding may be a protective factor for obesity and high body fat in 9‐ to 11‐year‐old children from 12 countries.
Keywords: breastfeeding, central, children, epidemiology, multination, obesity, obesitybody fat
Key messages
Childhood obesity is potentially affected by many factors. Several studies have shown that breastfeeding has a significant protective effect on childhood obesity, whereas others have shown a weak effect or no effect.
The present study examined the association between breastfeeding and the odds of childhood obesity in 9‐ to 11‐year‐old children from 12 countries.
We found that breastfeeding is associated with significantly reduced odds of general obesity and high body fat in 9‐ to 11‐year‐old children from 12 diverse countries.
1. INTRODUCTION
Obesity is an important lifestyle‐related public health problem worldwide. The prevalence of obesity in children has risen dramatically during the past few decades not only in developed countries but also in developing countries (Wu, 2013). Indeed, one recent review has reported that the prevalence of childhood overweight and obesity rose by 47.1% between 1980 and 2013 worldwide (Ng et al., 2014). Childhood overweight is a strong predictor of adult obesity (Whitaker, Wright, Pepe, Seidel, & Dietz, 1997) and other adverse health consequences, especially type 2 diabetes and cardiovascular disease in adolescence and adult life (Daniels, 2009; Goran, Ball, & Cruz, 2003). Thus obesity prevention is key to controlling its epidemic and identification of modifiable risk and protective factors is essential.
The benefits of breastfeeding in early childhood are well established. Breastfeeding is the recommended form of nutrition for the first 6 months of infant life. Current data on the impact of breastfeeding on overweight in childhood provide equivocal findings. Some studies have shown a significant protective effect (Armstrong & Reilly, 2002; Gillman et al., 2001; Grummer‐Strawn & Mei, 2004; Rito et al., 2019), whereas others have shown a weak effect or no effect (Hediger, Overpeck, Kuczmarski, & Ruan, 2001; Victora, Barros, Lima, Horta, & Wells, 2003). Data from two recent meta‐analyses have shown that breastfeeding was associated with a significantly reduced risk of later obesity in children (Horta, Loret de Mola, & Victora, 2015; Yan, Liu, Zhu, Huang, & Wang, 2014). The inconsistent nature of results from past work suggests that the association between breastfeeding and childhood overweight may be modified by one or more extraneous variables. Obesity is a multifactorial disorder with genetic, socio‐economic status, and lifestyle factors (e.g., physical activity and eating habits) as important predisposing factors (Hossain, Kawar, & El Nahas, 2007). Moreover, maternal history of gestational diabetes, birth weight, children's moderate‐to‐vigorous physical activity (MVPA), diet, sedentary behaviours, and sleeping duration may confound the association between breastfeeding and the risk of later childhood obesity. However, few studies were able to adjust for these factors simultaneously. The aim of the present study was to examine the association between breastfeeding and the odds of obesity in 9‐ to 11‐year‐old children from 12 countries while controlling for these purported confounders.
2. METHODS
2.1. Study design
The International Study of Childhood Obesity, Lifestyle and the Environment (ISCOLE) is a multinational cross‐sectional study conducted at urban and suburban sites in 12 countries (Australia, Brazil, Canada, China, Colombia, Finland, India, Kenya, Portugal, South Africa, United Kingdom, and the United States; Katzmarzyk et al., 2013). These countries were selected to represent diverse geographic and income groups according to the World Bank Classification (Table 1). More details on the study design and methods can be found elsewhere (Katzmarzyk et al., 2013). Written informed consent was obtained from parents or legal guardians, and child assent was also obtained as required by local Institutional/Ethical Review Boards before participation in the study.
Table 1.
Country | World bank classification | No. of study samples | ||
---|---|---|---|---|
Boys | Girls | Total | ||
Australia | High income | 182 | 204 | 386 |
Canada | High income | 192 | 251 | 443 |
Finland | High income | 190 | 211 | 401 |
Portugal | High income | 221 | 312 | 533 |
United Kingdom | High income | 141 | 183 | 324 |
United States | High income | 150 | 213 | 363 |
Brazil | Upper middle income | 171 | 183 | 354 |
China | Upper middle income | 221 | 192 | 413 |
Colombia | Upper middle income | 350 | 350 | 700 |
South Africa | Upper middle income | 50 | 70 | 120 |
India | Lower middle income | 185 | 229 | 414 |
Kenya | Low income | 133 | 156 | 289 |
Total | 2,186 | 2,554 | 4,740 |
2.2. Participants
A total of 7,372 children aged 9–11 years participated in the ISCOLE study, of whom 4,740 remained in the analytical sample for the present study after excluding participants who did not have valid data/information for accelerometry (N = 1,214), body mass index (BMI; N = 5), waist circumference (N = 5), percentage of body fat (N = 64), infant breast feeding (N = 426), birth weight (N = 355), gestational age (N = 108), maternal current BMI (N = 347), or other information (highest parental education, maternal history of gestational diabetes, and diet scores; N = 108). Participants who were excluded from the present analysis did not differ in BMI‐for‐age z‐scores but had a higher proportion of boys than those who were included in the analysis. Data were collected from September 2011 to December 2013.
2.3. Measurements
A demographic and family health history questionnaire was completed by parents or legal guardians. The questionnaire collected information on maternal highest education, maternal history of gestational diabetes, child's age, sex, birth weight, infant feeding mode, maternal age at delivery, and gestational age. The maternal highest education was collapsed into three categories: did not complete high school, completed high school or college, and completed bachelor or postgraduate degree. The maternal height and weight were collected in 9‐ to 11‐year‐old children. The child's parents or guardians were asked whether the child was fed breast milk, the age when the child completely stopped being fed breast milk, the age when the child was first fed formula, and the age when the child completely stopped fed formula. These responses were classified into three categories for the first 6 months: exclusive breastfeeding, mixed feeding, and exclusive formula feeding.
2.4. Dietary intake
A food frequency questionnaire that was adapted from the Health Behavior in School‐aged Children Survey (Currie et al., 2008; Mikkilä et al., 2015) was administered to all ISCOLE participants. The food frequency questionnaire asks the participants their “usual” consumption of 23 food categories, with response categories including never, less than once per week, once per week, 2–4 days per week, 5–6 days per week, once a day every day, and more than once a day. Two diet scores that represented an “unhealthy diet pattern” (with positive loadings for fast food, hamburgers, soft drinks, sweets, fried food, etc.) and a “healthy diet pattern” (with positive loadings for vegetables, fruit, whole grains, low‐fat milk, etc.) were obtained using principal components analyses (Mikkilä et al., 2015).
2.5. Anthropometry measurement
A battery of anthropometric measurements was taken according to standardized procedures across all study sites. Height was measured without shoes using a Seca 213 portable stadiometer (Hamburg, Germany), after a deep inhalation with the participant's head in the Frankfurt plane. Waist circumference was measured with a nonelastic tape held midway between the lower rib margin and the iliac crest at the end of a gentle expiration. Waist circumference was measured on the bare skin in all countries except in Australia where it was measured over light clothing. The regression equation (y = 0.994x − 0.42) developed by McCarthy et al. was applied to the Australian data to correct for the over‐the‐clothes measurement (McCarthy, Ellis, & Cole, 2003). Each measurement was repeated, and the average was used for analyses (a third measurement was obtained if the first two measurements were greater than 0.5 cm apart, and the average of the two closest measurements was used in analyses).
The participant's weight and body fat were measured using a portable Tanita SC‐240 Body Composition Analyser (Arlington Heights, IL, USA) after all outer clothing, heavy pocket items, and shoes and socks were removed. Two measurements were obtained, and the average was used in analyses (a third measurement was obtained if the first two measurements were more than 0.5 kg or 2.0% apart, for weight and percentage body fat, respectively, and the closest two were averaged for analyses). The Tanita SC‐240 showed acceptable accuracy for estimating percent body fat when compared with dual‐energy X‐ray absorptiometry, supporting its use in field studies (Barreira, Staiano, & Katzmarzyk, 2013). BMI was calculated by dividing weight in kilograms by the square of height in metres. BMI z‐scores were computed using age‐ and sex‐specific reference data from the World Health Organization (De Onis et al., 2007). General obesity was defined as BMI z‐scores greater than +2 SD. Central obesity was defined as waist circumference ≥ 90th percentile of National Health and Nutrition Examination Survey III reference (Fernandez, Redden, Pietrobelli, & Allison, 2004; Singh, 2006). High body fat was defined as body fat ≥90th percentile of National Health and Nutrition Examination Survey IV reference (Laurson, Eisenmann, & Welk, 2011).
2.6. Accelerometry
An ActiGraph GT3X+ accelerometer (ActiGraph, LLC, Pensacola, FL, USA) was used to objectively measure MVPA, sedentary time, and sleep period time. The accelerometer was worn at the waist on an elasticized belt on the right mid‐axillary line. Participants were encouraged to wear the accelerometer 24 hr per day (removing only for water‐related activities) for at least 7 days (plus an initial familiarization day and the morning of the final day), including two weekend days. The minimal amount of accelerometer data that was considered acceptable was 4 days with at least 10 hr of waking wear time per day, including at least one weekend day (Katzmarzyk et al., 2013). Nocturnal sleep duration was estimated from the accelerometer data using a fully automated algorithm for 24‐hr waist‐worn accelerometers that was validated for ISCOLE (Barreira et al., 2015). This algorithm produces more precise estimates of sleep duration than previous algorithms and captures total sleep time from sleep onset to the end of sleep, including all epochs and wakefulness after onset (Barreira et al., 2015). The weekly total sleep time averages were calculated using only days where valid sleep was accumulated (total sleep period time ≥ 160 min) and only for participants with at least three nights of valid sleep, including one weekend day (Tudor‐Locke, Barreira, Schuna, Mire, & Katzmarzyk, 2014). After exclusion of total sleep time and awake nonwear time (any sequence of ≥20 consecutive minutes of zero activity counts), MVPA was defined as all activity ≥574 counts per 15 s and total sedentary time (SED) as all epochs ≤25 counts per 15 s, consistent with the widely used Evenson cut‐offs (Evenson, Catellier, Gill, Ondrak, & McMurray, 2008).
2.7. Statistical analyses
One‐way analysis of variance and chi‐square test were used to compare mean levels of continuous variables and percentage of categorical variables among children with different feeding mode status. Multilevel logistic regression models were used to estimate the association between infant feeding mode and the odds of childhood obesity, central obesity, and high body fat. We defined child as Level 1, school as Level 2, and study site as Level 3 for the multilevel analyses. Study site and school were considered to have random effects. The denominator degrees of freedom for statistical tests pertaining to fixed effects were calculated using the Kenward and Roger (1997) approximation. The analyses were adjusted for maternal age at delivery, current maternal BMI, maternal education, maternal history of gestational diabetes, birth weight, child's unhealthy diet pattern scores, MVPA, sleeping duration, sedentary behaviours time, and child's age and sex. The criterion for statistical significance was P < .05. All statistical analyses were performed with SPSS for Windows, Version 21.0 (Statistics 21, SPSS, IBM, USA) or SAS for Windows, Version 9.4 (SAS Institute, Cary, NC, USA).
3. RESULTS
A total of 4,740 children (2,186 boys and 2,554 girls) were included in the present study. The distribution of sample sizes across sites is presented in Table 1. General characteristics of the study population are presented in Table 2. The overall prevalence of general obesity, central obesity, and high body fat were 12.3%, 9.9%, and 8.1%.
Table 2.
Characteristic | Exclusive breastfeeding | Mixed feeding | Exclusive formula feeding | Total | P value |
---|---|---|---|---|---|
Maternal characteristics | |||||
Age at delivery (years) | 28.5 (5.9) | 28.6 (5.6) | 27.7 (5.7) | 28.4 (5.7) | .003 |
Current body mass index (kg/m2) | 25.2 (4.5) | 25.6 (4.7) | 27.1 (6.5) | 25.6 (4.9) | <.001 |
History of gestational diabetes, N (%) | 63 (3.5) | 108 (4.7) | 35 (5.3) | 206 (4.3) | .082 |
Education, N (%) | <.001 | ||||
Did not complete high school | 473 (26.5) | 405 (17.7) | 171 (25.8) | 1,049 (22.1) | |
Completed high school/some college | 786 (44.0) | 1,007 (43.9) | 360 (54.3) | 2,153 (45.4) | |
Bachelor's degree or postgraduate degree | 526 (29.5) | 880 (38.4) | 132 (19.9) | 1,538 (32.4) | |
Offspring characteristics at birth | |||||
Sex, N (%) | .064 | ||||
Boys | 850 (47.6) | 1,017 (44.4) | 319 (48.1) | 2,186 (46.1) | |
Girls | 935 (52.4) | 1,275 (55.6) | 344 (51.9) | 2,554 (53.9) | |
Birth weight (g) | 3310 (566) | 3,259 (579) | 3274 (609) | 3,280 (579) | .020 |
Gestational age (weeks) | 38.8 (2.0) | 38.6 (2.2) | 38.3 (2.4) | 38.6 (2.2) | <.001 |
Offspring characteristics at age 9–11 years | |||||
Age (years) | 10.4 (0.6) | 10.4 (0.5) | 10.4 (0.6) | 10.4 (0.6) | .031 |
Body mass index (kg/m2) | 18.2 (3.4) | 18.3 (3.3) | 19.1 (3.8) | 18.4 (3.4) | <.001 |
Waist circumference (cm) | 64.0 (8.8) | 64.3 (8.6) | 65.1 (9.7) | 64.3 (8.9) | .033 |
Body fat (%) | 20.3 (7.5) | 20.8 (7.5) | 22.3 (8.1) | 20.8 (7.6) | <.001 |
Unhealthy diet pattern score | −0.2 (0.7) | −0.2 (0.8) | 0.1 (1.1) | −0.1 (0.9) | <.001 |
Moderate‐to‐vigorous physical activity (min/day) | 60.3 (24.5) | 59.9 (25.2) | 57.0 (23.0) | 59.6(24.7) | .012 |
Sedentary time (min/day) | 519 (67.6) | 516 (68.1) | 522 (67.3) | 518 (67.8) | .126 |
Duration of night sleep (min/day) | 528 (53.0) | 527 (53.2) | 531 (53.6) | 528 (53.2) | .168 |
General obesity, N (%)a | 204 (11.4) | 261 (11.4) | 119 (17.9) | 584 (12.3) | <.001 |
Central obesity, N (%)b | 173 (9.7) | 215 (9.4) | 82 (12.4) | 470 (9.9) | <.071 |
High body fat, N (%)c | 120 (6.7) | 175 (7.6) | 89 (13.4) | 384 (8.1) | <.001 |
Data are means (SD) or number (%).
General obesity was defined as BMI z‐score ≥ 2 SD for age and gender specific distribution based on the World Health Organization growth reference.
Central obesity was defined as waist circumference ≥ 90th percentile for age and gender specific distribution using National Health and Nutrition Examination Survey III reference.
High body fat was defined as body fat ≥90th percentile for age and gender specific distribution using National Health and Nutrition Examination Survey IV reference.
After adjustment for maternal age at delivery, education, history of gestational diabetes, gestational age, and child's age, sex, birth weight, unhealthy diet pattern scores, MVPA, sleeping time, and SED (multivariable‐adjusted Model 2), the odds ratio (OR) of childhood general obesity was significantly lower among children with exclusive breastfeeding (OR 0.66, 95% confidence interval, CI [0.50, 0.88]) compared with those with exclusive formula feeding (reference group), and this association was still significant after additional adjustment for current maternal BMI (multivariable‐adjusted Model 3; OR 0.76, 95% CI [0.57, 1.00]; Table 3). We did not find any significant associations of exclusive breastfeeding, mixed feeding, and exclusive formula feeding with the odds of central obesity in different multivariable‐adjusted models (Table 4). The multivariable‐adjusted (Model 3) ORs of high body fat were significantly lower among children with exclusive breastfeeding (OR 0.60, 95% CI [0.43, 0.84]) and among children with mixed feeding (OR 0.72, 95% CI [0.52, 0.98]) compared with those with exclusive formula feeding (Table 5).
Table 3.
No. of participates | No. of cases | Odds ratios (95% confidence intervals) | |||
---|---|---|---|---|---|
Model 1a | Model 2b | Model 3c | |||
Feeding mode | |||||
Exclusive formula feeding | 663 | 119 | 1.00 | 1.00 | 1.00 |
Mixed feeding | 2,292 | 261 | 0.73 [0.57, 0.95] | 0.75 [0.57, 0.97] | 0.83 [0.64, 1.09] |
Exclusive breastfeeding | 1,785 | 204 | 0.70 [0.54, 0.91] | 0.66 [0.50, 0.88] | 0.76 [0.57, 1.00] |
Breastfeeding duration (months) | |||||
None | 663 | 119 | 1.00 | 1.00 | 1.00 |
1–6 | 1359 | 152 | 0.74 [0.56, 0.98] | 0.74 [0.56, 0.99] | 0.84 [0.62, 1.12] |
7–12 | 1379 | 159 | 0.70 [0.53, 0.92] | 0.70 [0.52, 0.93] | 0.80 [0.60, 1.08] |
>12 | 1339 | 154 | 0.72 [0.54, 0.96] | 0.68 [0.50, 0.91] | 0.75 [0.55, 1.02] |
P for trend | .046 | .020 | .083 |
Model 1 adjusted for childs age and sex.
Model 2 adjusted for maternal age at delivery and education, maternal history of gestational diabetes and gestational age, and childs unhealthy diet pattern scores, birth weight, moderate‐to‐vigorous physical activity, sleeping time, sedentary time, age, and sex.
Model 3 adjusted for variables in Model 3 and also for maternal body mass index.
Table 4.
No. of participates | No. of cases | Odds ratios (95% confidence intervals) | |||
---|---|---|---|---|---|
Model 1a | Model 2b | Model 3c | |||
Feeding mode | |||||
Exclusive formula feeding | 663 | 82 | 1.00 | 1.00 | 1.00 |
Mixed feeding | 2,292 | 215 | 0.80 [0.60, 1.07] | 0.85 [0.62, 1.13] | 0.96 [0.71, 1.31] |
Exclusive breastfeeding | 1,785 | 173 | 0.81 [0.60, 1.09] | 0.80 [0.58, 1.08] | 0.92 [0.67, 1.27] |
Breastfeeding duration (months) | |||||
None | 663 | 82 | 1.00 | 1.00 | 1.00 |
1–6 | 1,359 | 123 | 0.87 [0.64, 1.19] | 0.89 [0.64, 1.22] | 1.02 [0.73, 1.43] |
7–12 | 1,379 | 127 | 0.73 [0.54, 1.00] | 0.76 [0.55, 1.05] | 0.90 [0.64, 1.25] |
>12 | 1,339 | 138 | 0.83 [0.60, 1.14] | 0.81 [0.58, 1.12] | 0.91 [0.65, 1.27] |
P for trend | .218 | .173 | .407 |
Model 1 adjusted for childs age and sex.
Model 2 adjusted for maternal age at delivery and education, maternal history of gestational diabetes and gestational age, and childs unhealthy diet pattern scores, birth weight, moderate‐to‐vigorous physical activity, sleeping time, sedentary time, age, and sex.
Model 3 adjusted for variables in Model 3 and also for maternal body mass index.
Table 5.
Outcomes | No. of participate | No. of cases | Odds ratios (95% confidence intervals) | ||
---|---|---|---|---|---|
Model 1a | Model 2b | Model 3c | |||
Feeding mode | |||||
Exclusive formula feeding | 663 | 89 | 1.00 | 1.00 | 1.00 |
Mixed feeding | 2,292 | 175 | 0.62 [0.46, 0.83] | 0.63 [0.46, 0.85] | 0.72 [0.52, 0.98] |
Exclusive breastfeeding | 1,785 | 120 | 0.56 [0.41, 0.76] | 0.52 [0.38, 0.72] | 0.60 [0.43, 0.84] |
Breastfeeding duration (months) | |||||
None | 663 | 89 | 1.00 | 1.00 | 1.00 |
1–6 | 1,359 | 102 | 0.65 [0.47, 0.90] | 0.64 [0.46, 0.89] | 0.73 [0.52, 1.02] |
7–12 | 1,379 | 84 | 0.48 [0.34, 0.66] | 0.47 [0.33, 0.66] | 0.55 [0.38, 0.79] |
>12 | 1,339 | 109 | 0.68 [0.49, 0.95] | 0.64 [0.46, 0.90] | 0.72 [0.51, 1.02] |
P for trend | .024 | .012 | .060 |
Model 1 adjusted for childs age and sex.
Model 2 adjusted for maternal age at delivery and education, maternal history of gestational diabetes and gestational age, and childs unhealthy diet pattern scores, birth weight, moderate‐to‐vigorous physical activity, sleeping time, sedentary time, age, and sex.
Model 3 adjusted for variables in Model 3 and also for maternal body mass index.
The multivariable‐adjusted (Model 2) ORs based on different breastfeeding durations (none, 1–6, 6–12, and > 12 months) were 1.00, 0.74, 0.70, and 0.60 for obesity (P for trend = .020; Table 3) and 1.00, 0.64, 047, and 0.64 (P for trend = .012; Table 5), respectively. These associations were no longer significant for childhood obesity and were still significant for high body fat among children with breastfeeding at 7–12 months after additional adjustment for maternal BMI.
4. DISCUSSION
In this multinational cross‐sectional study, we found that breastfeeding was a protective factor for childhood general obesity and high body fat in 9‐ to 11‐year‐old children from 12 countries.
An increased prevalence of childhood overweight and obesity has been observed worldwide over the past few decades, indicating a need for strategies to prevent obesity. Therapeutic interventions aimed at encouraging weight loss in children with obesity are costly and have had unsatisfactory long‐term success rates (Canadian Medical Association, 1994). There is some evidence that the odds of obesity are primed by exposures early in life. Among these factors, breastfeeding has been hypothesized as a potential protective factor against overweight (Armstrong & Reilly, 2002; Gillman et al., 2001; Grummer‐Strawn & Mei, 2004; von Kries et al., 1999). Although numerous studies support the protective effect of increased breastfeeding duration against childhood and adolescent obesity, other studies do not. Vehapoglu et al. (2014) found no association between the duration of breastfeeding and childhood obesity in children aged 2–14 years. Our study with large sample sizes from 12 diverse countries found a stronger association of breastfeeding with the risk of high body fat, a significant association of breastfeeding with the risk of general obesity, and a nonsignificant association of breastfeeding with the risk of central obesity among children aged 9–11 years when potential confounders were controlled. Thus, our study suggested that previous studies with only BMI measure in children may have underestimated the true effect of breastfeeding on obesity risk. The lack of effect of breastfeeding on central adiposity risk was found, and more studies are needed to assess this association.
Childhood overweight and obesity reflect the convergence of many biological, economic, and social factors. No single factor has been shown to protect a child from obesity. The difference in the results of previous studies may be due to the control of different confounding factors. Inconsistent findings in previous research may be a consequence of several limitations such as varying definitions of breastfeeding, different age periods of measurement, and lack of adjustment for additional possible confounders. Breastfeeding from diabetic mothers may increase the risk of becoming overweight (Plagemann, Harder, Franke, & Kohlhoff, 2002). Increased glucose and insulin content of breast milk of diabetic mothers (Jovanovic‐Peterson, Fuhrmann, Hedden, Walker, & Peterson, 1989) may contribute to effects of breastfeeding on infant growth, although some investigators have found no difference in macronutrient content of breast milk of well‐controlled diabetic mothers (van Beusekom et al., 1993). A recent study showed that the effect of breastfeeding on reducing the risk of obesity in later years is achieved in the first year of life (Scholtens et al., 2007). Current dietary and lifestyle factors are maybe more responsible for reducing the risk of obesity. So the evaluation of physical activity and dietary intake of the children are important confounding factors in assessing the relationship between obesity and breastfeeding. Al‐Qaoud and Prakash found that maternal BMI was a strong predictor of child BMI status. Children of mothers with obesity are 1.94 times more likely to be overweight and 2.63 times more likely to be obese than children of healthy‐weight mothers. Many studies have also shown that maternal BMI was a strong predictor of obesity (Burdette, Whitaker, Hall, & Daniels, 2006; Hediger et al., 2001). Some studies found mixed effects of breastfeeding on a child's weight status, depending on the degree to which confounders were controlled. Our findings made it possible to adjust for several important confounding factors, such as maternal age at delivery, maternal education, maternal history of gestational diabetes, gestational age, current maternal BMI, child's age and sex, unhealthy diet pattern scores, healthy diet pattern scores, MVPA, sleep time, and sedentary time.
Our study provides good evidence that breastfeeding may be protective of the development of obesity in childhood. Several possible biological mechanisms could be responsible for the protection of breastfeeding against childhood obesity. First, the nutritional and bioactive characteristics of human milk might be associated with childhood obesity. Breast milk contains hormones such as leptin, adiponectin, and ghrelin, and all these factors relate to the regulation of the content of adipose tissue. Studies have found that formula‐fed children might have higher plasma concentrations of insulin compared with those who had breastfeeding, and these higher concentrations of insulin would be expected to stimulate fat deposition and the early development of adipocytes (Lucas et al., 1980). Furthermore, breast milk also contains bioactive factors that may modulate epidermal growth factor and tumour necrosis factor, both of which are known to inhibit adipocyte differentiation in vitro (Hauner, Rohrig, & Petruschke, 1995). Second, early infant nutrition is one of the most powerful environmental factors determining early growth and development. After the first 3–4 months of life, breast‐fed infants gain less weight than formula‐fed infants (Kramer et al., 2002). Gaining less weight in infancy predicts lower rates of obesity in childhood and into adulthood (Gillman, 2010). Nutritional intake and metabolism in the critical or sensitive period of life development may lead to “programmed” or “metabolic imprinting” and will exert long‐term and lifelong effects on body structure, function, and substance metabolism. Third, the establishment of self‐regulation of food intake in infancy is extremely important to nutritional balance in childhood and even adulthood. It has been proposed that infants are born with some ability to regulate their energy intake in response to internal appetite cues (Birch & Fisher, 1998). However, this innate ability might be disrupted by the type of milk (human vs. nonhuman) and by the feeding mode (breast vs. bottle; Bartok & Ventura, 2009). It is postulated that breast‐fed infants have the ability to self‐regulate their energy intake to match their energy needs (Dewey & Lonnerdal, 1986). The sucking strength of infants varies according to their hunger, and the secretion of breast milk varies with the infant's sucking stimulation. Therefore, breast‐fed children can automatically control the food intake according to their own requirement, whereas formula‐fed infants are passive. Because parents do not think milk should be left in the bottle, it may cause formula‐fed children to overeat milk. The control of caregivers in formula feeding could lead to infants' poor self‐regulation on the basis of internal cues of hunger and satiety. Overconsumption of food increases the risk of obesity. To a greater extent than bottle‐fed infants, infants who are nursing typically let their mothers know when they are full by coming off the breast, which could lead to better self‐regulation of energy intake as they grow (Li, Fein, & Grummer‐Strawn, 2010).
There are several strengths in the present study. First, we used a globally diverse sample (including 12 countries from different geographic regions and economic levels) to test our hypothesis, thus increasing the external validity of our findings. These populations include children living in different stages of nutritional status including population with the double burden of malnutrition. Second, childhood obesity reflects the convergence of many biological, economic, and social factors. Accordingly, we collected data on many factors associated with obesity to control for the impact of confounding factors. Nevertheless, there are several limitations in our study. First, the cross‐sectional design precludes us from making cause‐and‐effect inferences. Second, this is a retrospective study. Breastfeeding data were based on self‐report, and mothers may forget when they introduced formula that could be biased or inaccurate; however, one study found that maternal recall was a valid and reliable estimate of breastfeeding initiation and duration (Li, Scanlon, & Serdula, 2005). Third, we did not collect the information whether the parent introduced solids/liquids in addition to breast milk before 4/6 months, which did not meet the strict definition of exclusive breastfeeding. Fourth, maternally reported birth weights, gestational age, and other neonatal events may have been inaccurately recalled.
5. CONCLUSION
In conclusion, breastfeeding was associated with significantly reduced odds of general obesity and high body fat in 9‐ to 11‐year‐old children from around the world. Greater allocation of health care and community resources to promote and support breastfeeding may benefit children and adolescents by reducing their odds for overweight and obesity.
CONFLICTS OF INTEREST
The authors reported no other potential conflicts of interest.
CONTRIBUTIONS
PK, JC, MF, RK, EL, CM, JM, VM, TO, VO, OS, MS, MT, CT, and GH designed the research study, performed the research, and revised the manuscript. JM, YQ, PZ, and WL analysed the data. JM, YQ, and HG wrote the paper. All authors have read and approved the final manuscript.
ACKNOWLEDGMENTS
The International Study of Childhood Obesity, Lifestyle and the Environment (ISCOLE) was funded by The Coca‐Cola Company (PBRC 2010–352). With the exception of requiring that the study be global in nature, the funder had no role in the design and conduct of the study; collection, management, analysis, and interpretation of the data; and preparation, review, or approval of the manuscript. Dr Hu was partly supported by a grant from the National Institute of Diabetes and Digestive and Kidney Diseases (R01DK100790) and the National Institute of General Medical Sciences (U54GM104940) of the National Institutes of Health.
Ma J, Qiao Y, Zhao P, et al. Breastfeeding and childhood obesity: A 12‐country study. Matern Child Nutr. 2020;16:e12984 10.1111/mcn.12984
Jian Ma and Yijuan Qiao contributed equally to this work and should be considered co‐first authors.
REFERENCES
- Armstrong, J. , & Reilly, J. J. (2002). Breastfeeding and lowering the risk of childhood obesity. Lancet, 359(9322), 2003–2004. 10.1016/s0140-6736(02)08837-2 [DOI] [PubMed] [Google Scholar]
- Barreira, T. V. , Schuna, J. M. Jr. , Mire, E. F. , Katzmarzyk, P. T. , Chaput, J. P. , Leduc, G. , & Tudor‐Locke, C. (2015). Identifying children's nocturnal sleep using 24‐h waist accelerometry. Medicine and Science in Sports and Exercise, 47(5), 937–943. 10.1249/mss.0000000000000486 [DOI] [PubMed] [Google Scholar]
- Barreira, T. V. , Staiano, A. E. , & Katzmarzyk, P. T. (2013). Validity assessment of a portable bioimpedance scale to estimate body fat percentage in White and African–American children and adolescents. Pediatric Obesity, 8(2), e29–e32. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Bartok, C. J. , & Ventura, A. K. (2009). Mechanisms underlying the association between breastfeeding and obesity. International Journal of Pediatric Obesity, 4(4), 196–204. 10.3109/17477160902763309 [DOI] [PubMed] [Google Scholar]
- Birch, L. L. , & Fisher, J. O. (1998). Development of eating behaviors among children and adolescents. Pediatrics, 101(3 Pt 2), 539–549. [PubMed] [Google Scholar]
- Burdette, H. L. , Whitaker, R. C. , Hall, W. C. , & Daniels, S. R. (2006). Maternal infant‐feeding style and children's adiposity at 5 years of age. Archives of Pediatrics & Adolescent Medicine, 160(5), 513–520. 10.1001/archpedi.160.5.513 [DOI] [PubMed] [Google Scholar]
- Canadian Medical Association (1994). Periodic Health Examination, 1994 update: 1. Obesity in childhood. Canadian Task Force on the Periodic Health Examination. CMAJ, 150(6), 871–879. [PMC free article] [PubMed] [Google Scholar]
- Currie, C. , & G. S., Godeau E, et al. (2008). Inequalities in children's health: HBSC international report from the 2005/2006 survey. Geneva: World Health Organization. [Google Scholar]
- Daniels, S. R. (2009). Complications of obesity in children and adolescents. International Journal of Obesity, 33(1), S60–S65. 10.1038/ijo.2009.20 [DOI] [PubMed] [Google Scholar]
- De Onis, M. , Onyanga, A. W. , Borghi, E. , Siyam, A. , Nishida, C. , & Siekmann, J. (2007). Development of a WHO growth reference for school‐aged children and adolescents. Bull WHO, 85, 660–667. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Dewey, K. G. , & Lonnerdal, B. (1986). Infant self‐regulation of breast milk intake. Acta Paediatrica Scandinavica, 75(6), 893–898. [DOI] [PubMed] [Google Scholar]
- Evenson, K. R. , Catellier, D. J. , Gill, K. , Ondrak, K. S. , & McMurray, R. G. (2008). Calibration of two objective measures of physical activity for children. Journal of Sports Sciences, 26(14), 1557–1565. 10.1080/02640410802334196 [DOI] [PubMed] [Google Scholar]
- Fernandez, J. R. , Redden, D. T. , Pietrobelli, A. , & Allison, D. B. (2004). Waist circumference percentiles in nationally representative samples of African‐American, European‐American, and Mexican‐American children and adolescents. The Journal of Pediatrics, 145(4), 439–444. 10.1016/j.jpeds.2004.06.044 [DOI] [PubMed] [Google Scholar]
- Gillman, M. W. (2010). Early infancy—A critical period for development of obesity. Journal of Developmental Origins of Health and Disease, 1(5), 292–299. 10.1017/s2040174410000358 [DOI] [PMC free article] [PubMed] [Google Scholar]
- Gillman, M. W. , Rifas‐Shiman, S. L. , Camargo, C. A. Jr. , Berkey, C. S. , Frazier, A. L. , Rockett, H. R. , … Colditz, G. A. (2001). Risk of overweight among adolescents who were breastfed as infants. JAMA, 285(19), 2461–2467. 10.1001/jama.285.19.2461 [DOI] [PubMed] [Google Scholar]
- Goran, M. I. , Ball, G. D. , & Cruz, M. L. (2003). Obesity and risk of type 2 diabetes and cardiovascular disease in children and adolescents. The Journal of Clinical Endocrinology and Metabolism, 88(4), 1417–1427. 10.1210/jc.2002-021442 [DOI] [PubMed] [Google Scholar]
- Grummer‐Strawn, L. M. , & Mei, Z. (2004). Does breastfeeding protect against pediatric overweight? Analysis of longitudinal data from the Centers for Disease Control and Prevention Pediatric Nutrition Surveillance System. Pediatrics, 113(2), e81–e86. [DOI] [PubMed] [Google Scholar]
- Hauner, H. , Rohrig, K. , & Petruschke, T. (1995). Effects of epidermal growth factor (EGF), platelet‐derived growth factor (PDGF) and fibroblast growth factor (FGF) on human adipocyte development and function. European Journal of Clinical Investigation, 25(2), 90–96. [DOI] [PubMed] [Google Scholar]
- Hediger, M. L. , Overpeck, M. D. , Kuczmarski, R. J. , & Ruan, W. J. (2001). Association between infant breastfeeding and overweight in young children. JAMA, 285(19), 2453–2460. [DOI] [PubMed] [Google Scholar]
- Horta, B. L. , Loret de Mola, C. , & Victora, C. G. (2015). Long‐term consequences of breastfeeding on cholesterol, obesity, systolic blood pressure and type 2 diabetes: A systematic review and meta‐analysis. Acta Paediatrica, 104(467), 30–37. 10.1111/apa.13133 [DOI] [PubMed] [Google Scholar]
- Hossain, P. , Kawar, B. , & El Nahas, M. (2007). Obesity and diabetes in the developing world—A growing challenge. The New England Journal of Medicine, 356(3), 213–215. 10.1056/NEJMp068177 [DOI] [PubMed] [Google Scholar]
- Jovanovic‐Peterson, L. , Fuhrmann, K. , Hedden, K. , Walker, L. , & Peterson, C. M. (1989). Maternal milk and plasma glucose and insulin levels: Studies in normal and diabetic subjects. Journal of the American College of Nutrition, 8(2), 125–131. [DOI] [PubMed] [Google Scholar]
- Katzmarzyk, P. T. , Barreira, T. V. , Broyles, S. T. , Champagne, C. M. , Chaput, J. P. , Fogelholm, M. , … Church, T. S. (2013). The International Study of Childhood Obesity, Lifestyle and the Environment (ISCOLE): Design and methods. BMC Public Health, 13, 900 10.1186/1471-2458-13-900 [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kenward, M. G. , & Roger, J. H. (1997). Small sample inference for fixed effects from restricted maximum likelihood. Biometrics, 53(3), 983–997. [PubMed] [Google Scholar]
- Kramer, M. S. , Guo, T. , Platt, R. W. , Shapiro, S. , Collet, J. P. , Chalmers, B. , … Vanilovich, I. (2002). Breastfeeding and infant growth: Biology or bias? Pediatrics, 110(2 Pt 1), 343–347. 10.1542/peds.110.2.343 [DOI] [PubMed] [Google Scholar]
- Laurson, K. R. , Eisenmann, J. C. , & Welk, G. J. (2011). Body fat percentile curves for U.S. children and adolescents. American Journal of Preventive Medicine, 41(4 Suppl 2), S87–S92. 10.1016/j.amepre.2011.06.044 [DOI] [PubMed] [Google Scholar]
- Li, R. , Fein, S. B. , & Grummer‐Strawn, L. M. (2010). Do infants fed from bottles lack self‐regulation of milk intake compared with directly breastfed infants? Pediatrics, 125(6), e1386–e1393. 10.1542/peds.2009-2549 [DOI] [PubMed] [Google Scholar]
- Li, R. , Scanlon, K. S. , & Serdula, M. K. (2005). The validity and reliability of maternal recall of breastfeeding practice. Nutrition Reviews, 63(4), 103–110. 10.1111/j.1753-4887.2005.tb00128.x [DOI] [PubMed] [Google Scholar]
- Lucas, A. , Sarson, D. L. , Blackburn, A. M. , Adrian, T. E. , Aynsley‐Green, A. , & Bloom, S. R. (1980). Breast vs bottle: Endocrine responses are different with formula feeding. Lancet, 1(8181), 1267–1269. [DOI] [PubMed] [Google Scholar]
- McCarthy, H. D. , Ellis, S. M. , & Cole, T. J. (2003). Central overweight and obesity in British youth aged 11–16 years: Cross sectional surveys of waist circumference. BMJ, 326(7390), 624 10.1136/bmj.326.7390.624 [DOI] [PMC free article] [PubMed] [Google Scholar]
- Mikkilä, V. , Vepsäläinen, H. , Saloheimo, T. , Gonzalez, S. A. , Meisel, J. D. , & Hu, G. (2015). An international comparison of dietary patterns in 9–11‐year‐old children. International Journal of Obesity Supplements, 5, S17–S21. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Ng, M. , Fleming, T. , Robinson, M. , Thomson, B. , Graetz, N. , Margono, C. , … Gakidou, E. (2014). Global, regional, and national prevalence of overweight and obesity in children and adults during 1980–2013: A systematic analysis for the Global Burden of Disease Study 2013. Lancet, 384(9945), 766–781. 10.1016/s0140-6736(14)60460-8 [DOI] [PMC free article] [PubMed] [Google Scholar]
- Plagemann, A. , Harder, T. , Franke, K. , & Kohlhoff, R. (2002). Long‐term impact of neonatal breast‐feeding on body weight and glucose tolerance in children of diabetic mothers. Diabetes Care, 25(1), 16–22. [DOI] [PubMed] [Google Scholar]
- Rito, A. I. , Buoncristiano, M. , Spinelli, A. , Salanave, B. , Kunesova, M. , Hejgaard, T. , … Breda, J. (2019). Association between characteristics at birth, breastfeeding and obesity in 22 countries: The WHO European Childhood Obesity Surveillance Initiative ‐ COSI 2015/2017. Obesity Facts, 12(2), 226–243. 10.1159/000500425 [DOI] [PMC free article] [PubMed] [Google Scholar]
- Scholtens, S. , Gehring, U. , Brunekreef, B. , Smit, H. A. , de Jongste, J. C. , Kerkhof, M. , … Wijga, A. H. (2007). Breastfeeding, weight gain in infancy, and overweight at seven years of age: The prevention and incidence of asthma and mite allergy birth cohort study. American Journal of Epidemiology, 165(8), 919–926. 10.1093/aje/kwk083 [DOI] [PubMed] [Google Scholar]
- Singh, G. K. (2006). Metabolic syndrome in children and adolescents. Current Treatment Options in Cardiovascular Medicine, 8(5), 403–413. [DOI] [PubMed] [Google Scholar]
- Tudor‐Locke, C. , Barreira, T. V. , Schuna, J. M. Jr. , Mire, E. F. , & Katzmarzyk, P. T. (2014). Fully automated waist‐worn accelerometer algorithm for detecting children's sleep‐period time separate from 24‐h physical activity or sedentary behaviors. Applied Physiology, Nutrition, and Metabolism, 39(1), 53–57. 10.1139/apnm-2013-0173 [DOI] [PubMed] [Google Scholar]
- van Beusekom, C. M. , Zeegers, T. A. , Martini, I. A. , Velvis, H. J. , Visser, G. H. , van Doormaal, J. J. , & Muskiet, F. A. (1993). Milk of patients with tightly controlled insulin‐dependent diabetes mellitus has normal macronutrient and fatty acid composition. The American Journal of Clinical Nutrition, 57(6), 938–943. [DOI] [PubMed] [Google Scholar]
- Vehapoglu, A. , Yazici, M. , Demir, A. D. , Turkmen, S. , Nursoy, M. , & Ozkaya, E. (2014). Early infant feeding practice and childhood obesity: The relation of breast‐feeding and timing of solid food introduction with childhood obesity. Journal of Pediatric Endocrinology & Metabolism, 27(11–12), 1181–1187. 10.1515/jpem-2014-0138 [DOI] [PubMed] [Google Scholar]
- Victora, C. G. , Barros, F. , Lima, R. C. , Horta, B. L. , & Wells, J. (2003). Anthropometry and body composition of 18 year old men according to duration of breast feeding: Birth cohort study from Brazil. BMJ, 327(7420), 901 10.1136/bmj.327.7420.901 [DOI] [PMC free article] [PubMed] [Google Scholar]
- von Kries, R. , Koletzko, B. , Sauerwald, T. , von Mutius, E. , Barnert, D. , Grunert, V. , & von Voss, H. (1999). Breast feeding and obesity: Cross sectional study. BMJ, 319(7203), 147–150. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Whitaker, R. C. , Wright, J. A. , Pepe, M. S. , Seidel, K. D. , & Dietz, W. H. (1997). Predicting obesity in young adulthood from childhood and parental obesity. The New England Journal of Medicine, 337(13), 869–873. 10.1056/nejm199709253371301 [DOI] [PubMed] [Google Scholar]
- Wu, J. F. (2013). Childhood obesity: A growing global health hazard extending to adulthood. Pediatrics and Neonatology, 54(2), 71–72. 10.1016/j.pedneo.2013.01.002 [DOI] [PubMed] [Google Scholar]
- Yan, J. , Liu, L. , Zhu, Y. , Huang, G. , & Wang, P. P. (2014). The association between breastfeeding and childhood obesity: A meta‐analysis. BMC Public Health, 14, 1267 10.1186/1471-2458-14-1267 [DOI] [PMC free article] [PubMed] [Google Scholar]