Literature DB >> 32141229

Breastfeeding and childhood obesity: A 12-country study.

Jian Ma1, Yijuan Qiao1, Pei Zhao1, Wei Li1, Peter T Katzmarzyk2, Jean-Philippe Chaput3, Mikael Fogelholm4, Rebecca Kuriyan5, Estelle V Lambert6, Carol Maher7, Jose Maia8, Victor Matsudo9, Timothy Olds7, Vincent Onywera10, Olga L Sarmiento11, Martyn Standage12, Mark S Tremblay3, Catrine Tudor-Locke13, Gang Hu2.   

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 (Ptrend = .020) and 1.00, 0.64, 047, and 0.64 for high body fat (Ptrend = .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.
© 2020 The Authors. Maternal & Child Nutrition published by John Wiley & Sons Ltd.

Entities:  

Keywords:  breastfeeding; central; children; epidemiology; multination; obesity; obesitybody fat

Mesh:

Year:  2020        PMID: 32141229      PMCID: PMC7296809          DOI: 10.1111/mcn.12984

Source DB:  PubMed          Journal:  Matern Child Nutr        ISSN: 1740-8695            Impact factor:   3.092


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.

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.

METHODS

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

International study of childhood obesity, lifestyle and the environment (ISCOLE) field site characteristics

CountryWorld bank classificationNo. of study samples
BoysGirlsTotal
AustraliaHigh income182204386
CanadaHigh income192251443
FinlandHigh income190211401
PortugalHigh income221312533
United KingdomHigh income141183324
United StatesHigh income150213363
BrazilUpper middle income171183354
ChinaUpper middle income221192413
ColombiaUpper middle income350350700
South AfricaUpper middle income5070120
IndiaLower middle income185229414
KenyaLow income133156289
Total2,1862,5544,740
International study of childhood obesity, lifestyle and the environment (ISCOLE) field site characteristics

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.

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.

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).

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).

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).

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).

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

Characteristics of study participant by different feeding mode at 6 months

CharacteristicExclusive breastfeedingMixed feedingExclusive formula feedingTotal 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 school473 (26.5)405 (17.7)171 (25.8)1,049 (22.1)
Completed high school/some college786 (44.0)1,007 (43.9)360 (54.3)2,153 (45.4)
Bachelor's degree or postgraduate degree526 (29.5)880 (38.4)132 (19.9)1,538 (32.4)
Offspring characteristics at birth
Sex, N (%).064
Boys850 (47.6)1,017 (44.4)319 (48.1)2,186 (46.1)
Girls935 (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.

Characteristics of study participant by different feeding mode at 6 months 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

Odds ratios of obesity at 9‐ to 11‐year‐old children by different feeding mode and breastfeeding duration

No. of participatesNo. of casesOdds ratios (95% confidence intervals)
Model 1a Model 2b Model 3c
Feeding mode
Exclusive formula feeding6631191.001.001.00
Mixed feeding2,2922610.73 [0.57, 0.95]0.75 [0.57, 0.97]0.83 [0.64, 1.09]
Exclusive breastfeeding1,7852040.70 [0.54, 0.91]0.66 [0.50, 0.88]0.76 [0.57, 1.00]
Breastfeeding duration (months)
None6631191.001.001.00
1–613591520.74 [0.56, 0.98]0.74 [0.56, 0.99]0.84 [0.62, 1.12]
7–1213791590.70 [0.53, 0.92]0.70 [0.52, 0.93]0.80 [0.60, 1.08]
>1213391540.72 [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

Odds ratios of central obesity at 9‐ to 11‐year‐old children by different feeding mode and breastfeeding duration

No. of participatesNo. of casesOdds ratios (95% confidence intervals)
Model 1a Model 2b Model 3c
Feeding mode
Exclusive formula feeding663821.001.001.00
Mixed feeding2,2922150.80 [0.60, 1.07]0.85 [0.62, 1.13]0.96 [0.71, 1.31]
Exclusive breastfeeding1,7851730.81 [0.60, 1.09]0.80 [0.58, 1.08]0.92 [0.67, 1.27]
Breastfeeding duration (months)
None663821.001.001.00
1–61,3591230.87 [0.64, 1.19]0.89 [0.64, 1.22]1.02 [0.73, 1.43]
7–121,3791270.73 [0.54, 1.00]0.76 [0.55, 1.05]0.90 [0.64, 1.25]
>121,3391380.83 [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

Odds ratios of high body fat at 9‐ to 11‐year‐old children by different feeding mode and breastfeeding duration

OutcomesNo. of participateNo. of casesOdds ratios (95% confidence intervals)
Model 1a Model 2b Model 3c
Feeding mode
Exclusive formula feeding663891.001.001.00
Mixed feeding2,2921750.62 [0.46, 0.83]0.63 [0.46, 0.85]0.72 [0.52, 0.98]
Exclusive breastfeeding1,7851200.56 [0.41, 0.76]0.52 [0.38, 0.72]0.60 [0.43, 0.84]
Breastfeeding duration (months)
None663891.001.001.00
1–61,3591020.65 [0.47, 0.90]0.64 [0.46, 0.89]0.73 [0.52, 1.02]
7–121,379840.48 [0.34, 0.66]0.47 [0.33, 0.66]0.55 [0.38, 0.79]
>121,3391090.68 [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.

Odds ratios of obesity at 9‐ to 11‐year‐old children by different feeding mode and breastfeeding duration 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. Odds ratios of central obesity at 9‐ to 11‐year‐old children by different feeding mode and breastfeeding duration 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. Odds ratios of high body fat at 9‐ to 11‐year‐old children by different feeding mode and breastfeeding duration 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.

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.

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.
  44 in total

1.  Small sample inference for fixed effects from restricted maximum likelihood.

Authors:  M G Kenward; J H Roger
Journal:  Biometrics       Date:  1997-09       Impact factor: 2.571

2.  Childhood obesity: a growing global health hazard extending to adulthood.

Authors:  Jia-Feng Wu
Journal:  Pediatr Neonatol       Date:  2013-03-07       Impact factor: 2.083

3.  Predicting obesity in young adulthood from childhood and parental obesity.

Authors:  R C Whitaker; J A Wright; M S Pepe; K D Seidel; W H Dietz
Journal:  N Engl J Med       Date:  1997-09-25       Impact factor: 91.245

4.  Early infancy - a critical period for development of obesity.

Authors:  M W Gillman
Journal:  J Dev Orig Health Dis       Date:  2010-10       Impact factor: 2.401

5.  Metabolic syndrome in children and adolescents.

Authors:  Gautam K Singh
Journal:  Curr Treat Options Cardiovasc Med       Date:  2006-09

6.  Milk of patients with tightly controlled insulin-dependent diabetes mellitus has normal macronutrient and fatty acid composition.

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Journal:  Am J Clin Nutr       Date:  1993-06       Impact factor: 7.045

Review 7.  Long-term consequences of breastfeeding on cholesterol, obesity, systolic blood pressure and type 2 diabetes: a systematic review and meta-analysis.

Authors:  Bernardo L Horta; Christian Loret de Mola; Cesar G Victora
Journal:  Acta Paediatr       Date:  2015-12       Impact factor: 2.299

8.  Waist circumference percentiles in nationally representative samples of African-American, European-American, and Mexican-American children and adolescents.

Authors:  José R Fernández; David T Redden; Angelo Pietrobelli; David B Allison
Journal:  J Pediatr       Date:  2004-10       Impact factor: 4.406

Review 9.  Development of eating behaviors among children and adolescents.

Authors:  L L Birch; J O Fisher
Journal:  Pediatrics       Date:  1998-03       Impact factor: 7.124

10.  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.

Authors:  Marie Ng; Tom Fleming; Margaret Robinson; Blake Thomson; Nicholas Graetz; Christopher Margono; Erin C Mullany; Stan Biryukov; Cristiana Abbafati; Semaw Ferede Abera; Jerry P Abraham; Niveen M E Abu-Rmeileh; Tom Achoki; Fadia S AlBuhairan; Zewdie A Alemu; Rafael Alfonso; Mohammed K Ali; Raghib Ali; Nelson Alvis Guzman; Walid Ammar; Palwasha Anwari; Amitava Banerjee; Simon Barquera; Sanjay Basu; Derrick A Bennett; Zulfiqar Bhutta; Jed Blore; Norberto Cabral; Ismael Campos Nonato; Jung-Chen Chang; Rajiv Chowdhury; Karen J Courville; Michael H Criqui; David K Cundiff; Kaustubh C Dabhadkar; Lalit Dandona; Adrian Davis; Anand Dayama; Samath D Dharmaratne; Eric L Ding; Adnan M Durrani; Alireza Esteghamati; Farshad Farzadfar; Derek F J Fay; Valery L Feigin; Abraham Flaxman; Mohammad H Forouzanfar; Atsushi Goto; Mark A Green; Rajeev Gupta; Nima Hafezi-Nejad; Graeme J Hankey; Heather C Harewood; Rasmus Havmoeller; Simon Hay; Lucia Hernandez; Abdullatif Husseini; Bulat T Idrisov; Nayu Ikeda; Farhad Islami; Eiman Jahangir; Simerjot K Jassal; Sun Ha Jee; Mona Jeffreys; Jost B Jonas; Edmond K Kabagambe; Shams Eldin Ali Hassan Khalifa; Andre Pascal Kengne; Yousef Saleh Khader; Young-Ho Khang; Daniel Kim; Ruth W Kimokoti; Jonas M Kinge; Yoshihiro Kokubo; Soewarta Kosen; Gene Kwan; Taavi Lai; Mall Leinsalu; Yichong Li; Xiaofeng Liang; Shiwei Liu; Giancarlo Logroscino; Paulo A Lotufo; Yuan Lu; Jixiang Ma; Nana Kwaku Mainoo; George A Mensah; Tony R Merriman; Ali H Mokdad; Joanna Moschandreas; Mohsen Naghavi; Aliya Naheed; Devina Nand; K M Venkat Narayan; Erica Leigh Nelson; Marian L Neuhouser; Muhammad Imran Nisar; Takayoshi Ohkubo; Samuel O Oti; Andrea Pedroza; Dorairaj Prabhakaran; Nobhojit Roy; Uchechukwu Sampson; Hyeyoung Seo; Sadaf G Sepanlou; Kenji Shibuya; Rahman Shiri; Ivy Shiue; Gitanjali M Singh; Jasvinder A Singh; Vegard Skirbekk; Nicolas J C Stapelberg; Lela Sturua; Bryan L Sykes; Martin Tobias; Bach X Tran; Leonardo Trasande; Hideaki Toyoshima; Steven van de Vijver; Tommi J Vasankari; J Lennert Veerman; Gustavo Velasquez-Melendez; Vasiliy Victorovich Vlassov; Stein Emil Vollset; Theo Vos; Claire Wang; XiaoRong Wang; Elisabete Weiderpass; Andrea Werdecker; Jonathan L Wright; Y Claire Yang; Hiroshi Yatsuya; Jihyun Yoon; Seok-Jun Yoon; Yong Zhao; Maigeng Zhou; Shankuan Zhu; Alan D Lopez; Christopher J L Murray; Emmanuela Gakidou
Journal:  Lancet       Date:  2014-05-29       Impact factor: 79.321

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  9 in total

Review 1.  Interactions between Growth of Muscle and Stature: Mechanisms Involved and Their Nutritional Sensitivity to Dietary Protein: The Protein-Stat Revisited.

Authors:  D Joe Millward
Journal:  Nutrients       Date:  2021-02-25       Impact factor: 5.717

2.  Breastfeeding may benefit cardiometabolic health of children exposed to increased gestational glycemia in utero.

Authors:  Yi Ying Ong; Wei Wei Pang; Jonathan Y Huang; Izzuddin M Aris; Suresh Anand Sadananthan; Mya-Thway Tint; Wen Lun Yuan; Ling-Wei Chen; Yiong Huak Chan; Neerja Karnani; S Sendhil Velan; Marielle V Fortier; Jonathan Choo; Lieng Hsi Ling; Lynette Shek; Kok Hian Tan; Peter D Gluckman; Fabian Yap; Yap-Seng Chong; Keith M Godfrey; Mary F-F Chong; Shiao-Yng Chan; Johan G Eriksson; Mary E Wlodek; Yung Seng Lee; Navin Michael
Journal:  Eur J Nutr       Date:  2022-02-06       Impact factor: 4.865

3.  Associations between Breastfeeding Duration and Obesity Phenotypes and the Offsetting Effect of a Healthy Lifestyle.

Authors:  Jiajia Dang; Ting Chen; Ning Ma; Yunfei Liu; Panliang Zhong; Di Shi; Yanhui Dong; Zhiyong Zou; Yinghua Ma; Yi Song; Jun Ma
Journal:  Nutrients       Date:  2022-05-10       Impact factor: 6.706

4.  BMI Trajectories During the First 2 Years, and Their Associations With Infant Overweight/Obesity: A Registered Based Cohort Study in Taizhou, China.

Authors:  Tian Zhang; Ying Song; Haoyue Teng; Yue Zhang; Jianan Lu; Linghua Tao; Yanjie Jin; Jieyun Yin; Danhong Zhou
Journal:  Front Pediatr       Date:  2021-05-12       Impact factor: 3.418

Review 5.  Co-Evolution of Breast Milk Lipid Signaling and Thermogenic Adipose Tissue.

Authors:  Tamás Röszer
Journal:  Biomolecules       Date:  2021-11-16

6.  Increased Gestational Weight Gain is Associated with a Higher Risk of Offspring Adiposity Before Five Years of Age: A Population-Based Cohort Study.

Authors:  Shuang Zhang; Nan Li; Weiqin Li; Leishen Wang; Enqing Liu; Tao Zhang; Wei Dong; Jiujing Chen; Junhong Leng
Journal:  Diabetes Metab Syndr Obes       Date:  2022-08-08       Impact factor: 3.249

7.  Association between breastfeeding, parents' body mass index and birth weight with obesity indicators in children.

Authors:  Maurício Dos Santos; Gerson Ferrari; Clemens Drenowatz; José Matheus Estivaleti; Eduardo Rossato de Victo; Luis Carlos de Oliveira; Victor Matsudo
Journal:  BMC Pediatr       Date:  2022-10-18       Impact factor: 2.567

8.  Breastfeeding and childhood obesity: A 12-country study.

Authors:  Jian Ma; Yijuan Qiao; Pei Zhao; Wei Li; Peter T Katzmarzyk; Jean-Philippe Chaput; Mikael Fogelholm; Rebecca Kuriyan; Estelle V Lambert; Carol Maher; Jose Maia; Victor Matsudo; Timothy Olds; Vincent Onywera; Olga L Sarmiento; Martyn Standage; Mark S Tremblay; Catrine Tudor-Locke; Gang Hu
Journal:  Matern Child Nutr       Date:  2020-03-05       Impact factor: 3.092

Review 9.  Microbial Colonization From the Fetus to Early Childhood-A Comprehensive Review.

Authors:  Viola Senn; Dirk Bassler; Rashikh Choudhury; Felix Scholkmann; Franziska Righini-Grunder; Raphael N Vuille-Dit-Bile; Tanja Restin
Journal:  Front Cell Infect Microbiol       Date:  2020-10-30       Impact factor: 5.293

  9 in total

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