REVIEW
The effect of breastfeeding on childhood overweight and obesity: A systematic review of the literature Christen M. Lefebvre, MS, CPNP, CLC (Certified Pediatric Nurse Practitioner)1 & Rita Marie John, EdD, DNP, CPNP, PMHS (Associate Professor)2 1 2
Children’s Specialized Hospital, Mountainside, New Jersey Columbia University, New York, New York
Keywords Breastfeeding; children; child; nurse practitioners; obesity; pediatric; prevention. Correspondence Christen M. Lefebvre, MS, CPNP, CLC, Children’s Specialized Hospital, 150 New Providence Road, Mountainside, NJ 07092. Tel: 908-301-5491; Fax: 908-301-5408; E-mail: [email protected] Rita Marie John, EdD, DNP, CPNP, PMHS: E-mail: [email protected] Received: November 2011; accepted: July 2012 doi: 10.1111/2327-6924.12036
Abstract Background: Childhood obesity has reached epidemic proportions. There is increasing attention to the topic of prevention and continued debate as to whether breastfeeding (BF) is protective against childhood obesity. Previous systematic reviews on this topic were done in 2005 showing that BF was protective against childhood obesity but, because of confounding variables, the evidence was weak. Objective: To explore the current evidence of the effect of BF on childhood obesity and provide recommendations for the nurse practitioner (NP) as a primary care provider. Methods: A systematic review of the literature from 1/2005 to 3/2012 was done to assess the evidence on the relationship between BF and childhood obesity. Results: The majority of studies identified in this article showed a relationship between BF and obesity prevention, but because of confounding maternal, child, cultural, genetic, and environmental variables, the relationship remains unclear. Conclusions: While it is possible that there are protective benefits of BF on childhood obesity, it is difficult to prove because of confounding variables. However, because of other benefits for the mother and child, BF should be encouraged. Whether obesity in childhood can be prevented by BF remains unclear. Further research controlling for confounding variables is needed to provide concrete evidence.
Introduction Recently, there has been an enormous amount of attention on the worldwide childhood obesity epidemic. Prevention of obesity has been the subject of recent research because of continued failure of obesity treatment programs in children. The United States Preventive Service Task Force (2005) reported insufficient evidence for behavioral or other preventive interventions with obese children conducted in a primary care setting. In 2010, the White House Task Force on Childhood Obesity released an urgent report to the president of the United States calling attention to the extensive prevalence and effects of the problem, and recommended ways to appropriately handle the immense challenges of this growing crisis. The White House Task Force report focuses on 386
breastfeeding (BF) as a potential protective factor against childhood obesity and therefore urged healthcare professionals and others to promote, protect, encourage, and support BF (2010). Three separate meta-analyses concluded that being breastfed in infancy is associated with reduced risk of childhood obesity (Arenz, Ruckerl, Koletzko, & von Kries, 2004; Harder, Bergmann, Kallischnigg, & Plagemann, 2005; Owen, Martin, Whincup, Davey-Smith, & Cook, 2005). Harder et al. (2005) reported a 4% reduction in overweight for each month of BF, and Arenz et al. (2004) concluded that BF had a consistent effect on obesity prevention. However, none of the meta-analyses considered the heterogeneity of the studies in their reports and many of the included studies failed to adjust for parental body mass index (BMI; McCrory & Layte, 2012). Journal of the American Association of Nurse Practitioners 26 (2014) 386–401 C 2013 American Association of Nurse Practitioners
The effect of breastfeeding on childhood weight
C. M. Lefebvre & R. M. John
Table 1 Comorbidities of childhood obesity Body system
Obesity causes an increased risk for
Cardiovascular
Hypercholesterolemia (AAP, 2007) Hyperlipidemia (AAP, 2007) Hypertension (AAP, 2007) Increased risk of heart disease because of coronary artery disease (Berenson & Srinivasan, 2001) Hyperinsulinism (AAP, 2007) Insulin resistance (AAP, 2007) Impaired glucose tolerance (AAP, 2007) Type 2 diabetes mellitus (AAP, 2007) Menstrual irregularity (AAP, 2007) Increased linear growth (Wattigney, Srinivasan, Chen, Greenlund, & Berenson, 1999) Poor self-esteem (AAP, 2007) Depression (AAP, 2007) Eating disorders (Zametkin, Zoon, Klein, & Munson, 2004). Psychological stress promoting central obesity (Goldbacher, Matthews, & Salomon, 2005)
Endocrine
Mental health
Pulmonary
Shortening life span Orthopedic Gastrointestinal/hepatic
Asthma (AAP, 2007) Obstructive sleep apnea (AAP, 2007) Pickwickian syndrome (AAP, 2007) From 5 to 20 years, depending on age, sex, and degree of obese (Fontaine, Redden, Wage, Westfall, & Alison, 2003; Olshansky et al., 2005) Genu varum (AAP, 2007) Slipped capital femoral epiphysis (AAP, 2007) Nonalcoholic steatohepatitis (AAP, 2007) Gallstones (Khare, Everhart, Maurer, & Hill; 1995)
Rationale The policy statement from the American Academy of Pediatrics (AAP) on childhood obesity developed guidelines for pediatricians to combat the obesity epidemic (AAP, 2007). The Heat Clinical Practice Guidelines Steering Work Group (HEAT) Campaign developed by the National Association of Pediatric Nurse Practitioners (NAPNAP) also developed guidelines for the practicing PNP to combat obesity using a culturally sensitive approach for each age (HEAT, 2006). Both policy statements encourage BF by mothers for at least 6 months and ideally for 1 year as well as using the BMI, a measure of adiposity based on height, weight, age, and sex, to be plotted on a growth chart (AAP, 2007; HEAT, 2006). Both organizations use the Centers for Disease Control and Prevention (CDC) definitions of overweight and obesity (Barlow & Expert Committee, 2007). A BMI at or above the 85th percentile but below the 95th percentile for age and sex is the definition of overweight in childhood. Obesity is defined as a BMI at or above the 95th percentile for the child’s age and sex (Barlow & Expert Committee, 2007). Counseling about weight is advised at every primary visit (AAP, 2007; Barlow & Expert Committee, 2007; HEAT, 2006). Chivers et al. (2010) used timing of adiposity rebound as a measurement of childhood obesity. Adiposity rebound is defined as the time
in which the BMI curve increases. BMI normally increases during the first year of life then decreases until between ages 4 and 8 years when fatness increases again (Chivers et al., 2010). The earlier the rebound occurs, the higher the adiposity is at the end of growth. Children who are obese have been shown to have much earlier adiposity rebounds compared to nonobese children (Chivers et al., 2010). In addition, there are several comorbidities associated with obesity, making prevention even more important. Table 1 lists the comorbidities found to be directly associated with childhood obesity. One of the many objectives of the Department of Health and Human Services’ (DHHS) Healthy People 2020 Campaign (2009) is to decrease the number of children who are obese, prevent inappropriate weight gain in children, promote BF, and increase BMI screening in primary care offices. Goals for promoting BF include increasing the number of mothers who breastfeed their babies with a goal of exclusive BF for 6 months, decreasing the percentage of breastfed newborns who receive supplemental formula feedings in the first 2 days of life, and increasing the percentage of employers who provide lactation programs (Department of Health and Human Services, 2009). BF is known to reduce respiratory and gastrointestinal infection in the neonate (Horta, Bhla, Martines, & Victora, 2007; Kramer, 2010). 387
The effect of breastfeeding on childhood weight
The recommendations from the AAP’s 2005 policy statement on BF concluded that infants should be breastfed exclusively for the first 6 months and continue to be breastfed with supplemental feedings during the second half of the first year of life. The AAP cited the evidence that BF protects against childhood obesity, asthma, infectious diseases, and certain cancers. The AAP reported that BF is highly cost effective and provides extensive benefits for the mother and child (AAP, 2005). Further evidence that BF is protective against the risk of obesity is found in the Endocrine Society’s clinical practice guidelines (2008). Experts recommend BF for a minimum of 6 months to prevent obesity based on the highest level of evidence set by the researchers’ grading system (August et al., 2008). Additionally, a comprehensive pediatric cost analysis study reported that if there was an increase of exclusive BF for 6 months to 90%, the United States could not only save $13 billion/year, but reduce the death rate by 911 persons annually, with most of them being infants.
Previous systematic reviews on the effect of BF on obesity Harder et al. (2005) used meta-regression analysis, a pool-first method, and a log-linear model to perform a comprehensive meta-analysis of current published studies. The objective was to assess if there is a dosedependent relationship of duration of any BF to the risk of being overweight. Twenty-one studies met the inclusion criteria. All of the included studies had a 95% confidence interval of the association of BF to overweight using BF duration compared to exclusively formula-fed subjects. The duration of BF was inversely and linearly associated with the risk of overweight. Each month of BF was found to cause a 4% decrease in the risk of overweight with a lasting effect of up to 9 months of age. As a result, there was up to a 36% reduction in overweight children. Categorical analysis showed a dose-dependent relationship of BF duration and decreased risk of overweight (Harder et al., 2005). However, four of the studies would not be significant if parental BMI was adjusted (McCrory & Layte, 2012). Another meta-analysis and systematic review examined the effect of infant feeding on later obesity (Owen et al., 2005). Twenty-eight studies were included based on odds ratios of obesity among breastfed subjects versus formula-fed subjects. All of the studies reported that BF was associated with a lower risk of obesity compared to formula feeding. Six studies controlled for three major confounding variables (parental obesity, maternal smoking, and social class) and found that the association between BF and reduction in overweight was decreased, but 388
C. M. Lefebvre & R. M. John
not eliminated. No studies found that BF was related to an increase in childhood obesity. The authors concluded that BF protects against obesity, but felt that further review of confounding factors was needed (Owen et al., 2005). Finally, Arenz et al. (2004) included nine studies in their review and reported a protective effect of BF despite the fact that their data showed no effect on obesity in four of their reviewed studies (Hediger, Overpeck, Kuczmarski, & Ruan, 2001; Li, Parsons, & Power, 2003; O’Callaghan, Williams, Andersen, Bor, & Najmans, 1997; Poulton & Williams, 2001). This review will update the previous systematic reviews and incorporate new evidence in the conclusions.
Objective The purpose of this article is to examine the recent research and literature of the effects of BF on childhood overweight and obesity from 2005 to the beginning of 2012. To examine whether BF can be protective against childhood overweight and obesity, we reviewed all current studies that assessed the relationship between BF and childhood overweight and obesity. The previous meta-analyses resulted in conflicting results of studies because of the inability to perform a valid and reliable research test using BF as a variable, and the presence of confounding variables.
Method This systematic review was performed according to the preferred reporting items for systematic reviews and meta-analyses (PRISMA) statement for reporting systematic reviews (Liberati et al., 2009). A protocol was established in which the criteria included research studies from any country, written in English, from 1/2005 to 3/ 2012, examining the relationship between BF and childhood obesity. Because it is impossible to do a randomized controlled trial randomly assigning exclusively BF or formula feedings to maternal–child dyads, it was decided to include any research studies, aside from case reports. It was decided not to limit the search to only research done in the United States because global diversity is reflected within the United States population. In addition, there is diversity within other countries as reflected by the ethnicity data from the some of the studies.
Information sources Studies were identified using PubMed, CINAHL, and Medline (including OvidMedline, Evidence-Based Medicine [EBM] reviews—Cochrane Database of
The effect of breastfeeding on childhood weight
C. M. Lefebvre & R. M. John
Systematic Reviews, EBM Reviews—ACP Journal Club, EBM Reviews—Database of Abstracts of Reviews of Effects, EBM Reviews—Cochrane Central Register of Controlled Trials, and EBM Reviews—Cochrane Methodology Register, EBM Reviews—Health Technology Assessment, EBM Reviews—NHS Economic Evaluation Database). Search terms included “breastfeeding, obesity prevention,” “breastfeeding, overweight prevention,” “breastfeeding, obesity,” “breastfeeding, overweight,” and “breastfeeding, adiposity.”
Study selection Two reviewers using the above criteria did eligibility assessment of studies independently. Disagreement was handled by discussion and consensus opinion. Table 2 shows a study retrieval flow diagram with the results of the literature search.
Data collection process including data items The information that was gathered on each study included the type of trial; the number, ages, gender, and ethnicity of the research subjects (SAGE); the country of and the method of data collection; the evaluation of parental BMI; how confounding variables were handled; the statistical analysis; the purpose; the extent of loss to follow-up; and the findings of the relationship of BF to obesity.
Results Twenty-one studies met the inclusion criteria for this systematic review after a search of PubMed, CINAHL, and Medline yielded a total of 871 articles. After adjusting for year of publication and duplications, there were 106 articles remaining. A full review of these articles eliminated another 85 articles because they did not meet the inclusion criteria. The combined sample size of all of the studies is 107,177. The ages of the research subjects vary from infancy to adults, complicating the interpretation. In addition, 35,526 of the subjects came from the nurse’s cohort study and the data on BF duration were obtained when the nurses were adults from 25 to 42 years of age, making these BF data exceptionally retrospective (Michels et al., 2007). In most of the studies, the primary outcome was the duration of BF and its effect on BMI. Two of the studies also looked at sugar sweetened beverages (Davis, Whaley, & Goran, 2012) and introduction of solid foods (Griffiths, Smeeth, Hawkins, Cole, & Dezateux, 2009; Michels et al., 2007) in a separate analysis within their studies. Table 3
is a detailed review of the studies that were included in the review.
Discussion Ten of 21 studies reported that BF was found to have no significant effect on childhood obesity in older children 4 years of age and up except for Durmus et al. (2011), who showed a relationship and decreased BMI at 3 and 6 months, but no effect at 1, 2, and 3 years. It should be noted that BMI is not an accurate measure in children under age 2 years. Of the 11 studies that showed that BF had a protective effect on childhood obesity, the authors discussed the limitations of their results. These limitations included inability to control for all confounding variables, appropriate statistical methods to control for confounding variables (Beyerlein, Toschke, and von Kries, 2008), a dropout rate exceeding 30% (Burke et al., 2005; Durmus et al., 2011; Huus et al., 2008), and the lack of effect in matched sibling pairs in his secondary group (Nelson, Gordon-Larsen, & Adair. 2005). Nine of the studies determined that the protective effect on childhood obesity provided by BF is dependent on duration. Two studies established a dose–response relationship by showing that BF duration and exclusivity both played significant roles in the prevention of childhood overweight and obesity (Fallahzadeh, Golestan, Rezvanian, & Ghasemian, 2009; Simon, Souza, & Souza, 2009). In contrast, Novotny et al. (2007) determined that any BF is protective against childhood obesity. It should be noted that only six of the studies used currently obtained data to determine the length of BF (Chivers et al., 2010; Durmus et al., 2011; Sabanayagam, Shankar, Chong, Wong, & Saw, 2009; Scholtens et al., 2007; Weyermann, Rothenbacher, & Brenner, 2006). The use of retrospective information is a definite limitation of the remainder of studies.
BF duration as a protective effect on childhood obesity Duration of BF of at least 4 months was shown to be statistically significant in reducing childhood obesity in four studies. Griffiths et al. (2009) found that children, from birth to 3 years old, who were breastfed for less than 4 months were heavier, had more adipose tissue, gained weight quicker, and were at a higher risk for obesity than children who were breastfed for at least 4 months. Similarly, at age 1, children who were breastfed for at least 4 months were found to have lower BMIs than children breastfed for less than 4 months (Scholtens et al., 2007). Children who were breastfed for less than or equal to 4 months had earlier adiposity rebound, higher BMI at 389
The effect of breastfeeding on childhood weight
C. M. Lefebvre & R. M. John
Table 2 Flow diagram for study retrieval
N = 871 articles identified from the literature search (466 from PubMed, 336 from Medline, including OvidMedline, EBM Reviews- Cochrane Database of Systematic Reviews, EBM Reviews- ACP Journal Club, EBM ReviewsDatabase of Abstracts of Reviews of Effects, EBM Reviews- Cochrane Central Register of Controlled Trials, EBM Reviews- Cochrane Methodology Register, EBM ReviewsHealth Technology Assessment, EBM Reviews- NHS Economic Evaluation Database, and 88 from CINHAL)
328 articles excluded for publication date prior to 2005
NN= = 542 543 60 articles removed for duplication in databases
N = 483 380 articles excluded after title and abstract review
N = 127 106 articles excluded after full text review
N = 21
time of rebound, and higher BMI over time compared to children breastfed for longer than 4 months (Chivers et al., 2010). Other studies showed correlations between different durations of BF on overweight and obesity in childhood. A minimum of 6 months was found to be protective in two studies (Toschke et al., 2007; Weyermann et al., 2006). Children who were breastfed for at least 6 months had a decreased risk of overweight compared to children breastfed for less than 3 months (Weyermann et al., 2006). One to 3 months of BF was recommended by Neutzling et al. (2009), and BF for 9 months, compared with BF for less than 3 months, was shown to be 390
protective for girls (boys showed a less consistent effect) in the study by Nelson, Gordon-Larsen, and Adair (2005). Exclusivity of BF has also been shown to have an effect on childhood obesity. Simon et al. (2009) found that exclusive BF for 6 months or more and BF for more than 24 months were protective factors against overweight and obesity. Children breastfed for greater than 24 months were also less likely to be overweight than children breastfed for 12–24 months, who were less likely to be overweight than children breastfed for shorter than 12 months (Fallahzadeh et al., 2009). The same trends were observed with BF exclusivity in this study (Fallahzadeh et al., 2009). For children exclusively
2291 3–6 year olds 1092 males 1199 females Ethnicity not reported Kuwait
SAGE and country
Burke et al. (2005) Longitudinal analysis study
2087 children at birth but decreased to 1430 children at 8 years Gender and ethnicity not specified Australia
9368 preschool children Beyerlein et al. 52% male (2008) 48% female Retrospective Ethnicity not reported analysis in which Germany duration of BF was missing for most of the subjects
Araujo et al. (2006) 1273 4 year olds Prospective 49.2% female population50.8% male based Ethnicity not reported birth cohort Brazil study
Al-Qaoud et al. (2009) Respective analysis study
Author and year Type of study Child’s gender Age Birthweight. Gestational age Duration of breastfeeding Mother’s age Mother BMI status Mother’s education
Confounding variables addressed
Interviews from the mother were Birthweight Maternal BMI done from birth until the Maternal education mother stopped BF. BMI scores Parity were then done on children at Maternal age 1, 3, 6, and 8 years of age Smoking status Retrospective BF information Data were analyzed using mixed models CI 95%
Socioeconomic status (SES) Maternal education Maternal smoking in pregnancy Maternal BMI at start of pregnancy Weight gain during pregnancy Infant skin color Infant sex Infant birthweight Asset index Gender Height, weight, and BMI were Age measured. Questionnaires were Smoking in pregnancy obtained TV watching Retrospective BF information Maternal BMI Linear, logistic, and quantile Parental social status regression model Early weight gain
Height, weight, and BMI were measured. Results were compared to data from the Kuwaiti Nutrition Surveillance System from 2003 to 2004 Retrospective breastfeeding information Multinomial logistical regression analysis 95% confidence interval (CI) Prospective cohort Retrospective BF information Logistic regression models 95% CI
Methods of data collection/statistical analysis
Table 3 Review of the literature from 2005 to 2011: summaries of studies (in alphabetical order)
No significant association between BF and its duration and obesity prevention Other factors suggested to play a role include diet, exercise, maternal BMI, gender, age, birthweight Felt results may reflect modernization of country leading to increase food consumption and sedentary lifestyle (not evaluated in study) • No loss to follow-up reported
To assess whether BF has an effect in different percentiles of children’s BMI distribution
In the linear regression model, no association was found In the logistic model there was a significant relationship The association between BF and childhood BMI might be related to the statistical method used to obtain results BF might prevent overweight and obesity rather than a shift in the entire BMI distribution A dose–response relationship was not found To research the Children who were breastfed >12 months had relationship between BF lower BMIs at 1 year old than those breastfed and childhood adiposity
The effect of breastfeeding on childhood overweight and obesity: A systematic review of the literature Christen M. Lefebvre, MS, CPNP, CLC (Certified Pediatric Nurse Practitioner)1 & Rita Marie John, EdD, DNP, CPNP, PMHS (Associate Professor)2 1 2
Children’s Specialized Hospital, Mountainside, New Jersey Columbia University, New York, New York
Keywords Breastfeeding; children; child; nurse practitioners; obesity; pediatric; prevention. Correspondence Christen M. Lefebvre, MS, CPNP, CLC, Children’s Specialized Hospital, 150 New Providence Road, Mountainside, NJ 07092. Tel: 908-301-5491; Fax: 908-301-5408; E-mail: [email protected] Rita Marie John, EdD, DNP, CPNP, PMHS: E-mail: [email protected] Received: November 2011; accepted: July 2012 doi: 10.1111/2327-6924.12036
Abstract Background: Childhood obesity has reached epidemic proportions. There is increasing attention to the topic of prevention and continued debate as to whether breastfeeding (BF) is protective against childhood obesity. Previous systematic reviews on this topic were done in 2005 showing that BF was protective against childhood obesity but, because of confounding variables, the evidence was weak. Objective: To explore the current evidence of the effect of BF on childhood obesity and provide recommendations for the nurse practitioner (NP) as a primary care provider. Methods: A systematic review of the literature from 1/2005 to 3/2012 was done to assess the evidence on the relationship between BF and childhood obesity. Results: The majority of studies identified in this article showed a relationship between BF and obesity prevention, but because of confounding maternal, child, cultural, genetic, and environmental variables, the relationship remains unclear. Conclusions: While it is possible that there are protective benefits of BF on childhood obesity, it is difficult to prove because of confounding variables. However, because of other benefits for the mother and child, BF should be encouraged. Whether obesity in childhood can be prevented by BF remains unclear. Further research controlling for confounding variables is needed to provide concrete evidence.
Introduction Recently, there has been an enormous amount of attention on the worldwide childhood obesity epidemic. Prevention of obesity has been the subject of recent research because of continued failure of obesity treatment programs in children. The United States Preventive Service Task Force (2005) reported insufficient evidence for behavioral or other preventive interventions with obese children conducted in a primary care setting. In 2010, the White House Task Force on Childhood Obesity released an urgent report to the president of the United States calling attention to the extensive prevalence and effects of the problem, and recommended ways to appropriately handle the immense challenges of this growing crisis. The White House Task Force report focuses on 386
breastfeeding (BF) as a potential protective factor against childhood obesity and therefore urged healthcare professionals and others to promote, protect, encourage, and support BF (2010). Three separate meta-analyses concluded that being breastfed in infancy is associated with reduced risk of childhood obesity (Arenz, Ruckerl, Koletzko, & von Kries, 2004; Harder, Bergmann, Kallischnigg, & Plagemann, 2005; Owen, Martin, Whincup, Davey-Smith, & Cook, 2005). Harder et al. (2005) reported a 4% reduction in overweight for each month of BF, and Arenz et al. (2004) concluded that BF had a consistent effect on obesity prevention. However, none of the meta-analyses considered the heterogeneity of the studies in their reports and many of the included studies failed to adjust for parental body mass index (BMI; McCrory & Layte, 2012). Journal of the American Association of Nurse Practitioners 26 (2014) 386–401 C 2013 American Association of Nurse Practitioners
The effect of breastfeeding on childhood weight
C. M. Lefebvre & R. M. John
Table 1 Comorbidities of childhood obesity Body system
Obesity causes an increased risk for
Cardiovascular
Hypercholesterolemia (AAP, 2007) Hyperlipidemia (AAP, 2007) Hypertension (AAP, 2007) Increased risk of heart disease because of coronary artery disease (Berenson & Srinivasan, 2001) Hyperinsulinism (AAP, 2007) Insulin resistance (AAP, 2007) Impaired glucose tolerance (AAP, 2007) Type 2 diabetes mellitus (AAP, 2007) Menstrual irregularity (AAP, 2007) Increased linear growth (Wattigney, Srinivasan, Chen, Greenlund, & Berenson, 1999) Poor self-esteem (AAP, 2007) Depression (AAP, 2007) Eating disorders (Zametkin, Zoon, Klein, & Munson, 2004). Psychological stress promoting central obesity (Goldbacher, Matthews, & Salomon, 2005)
Endocrine
Mental health
Pulmonary
Shortening life span Orthopedic Gastrointestinal/hepatic
Asthma (AAP, 2007) Obstructive sleep apnea (AAP, 2007) Pickwickian syndrome (AAP, 2007) From 5 to 20 years, depending on age, sex, and degree of obese (Fontaine, Redden, Wage, Westfall, & Alison, 2003; Olshansky et al., 2005) Genu varum (AAP, 2007) Slipped capital femoral epiphysis (AAP, 2007) Nonalcoholic steatohepatitis (AAP, 2007) Gallstones (Khare, Everhart, Maurer, & Hill; 1995)
Rationale The policy statement from the American Academy of Pediatrics (AAP) on childhood obesity developed guidelines for pediatricians to combat the obesity epidemic (AAP, 2007). The Heat Clinical Practice Guidelines Steering Work Group (HEAT) Campaign developed by the National Association of Pediatric Nurse Practitioners (NAPNAP) also developed guidelines for the practicing PNP to combat obesity using a culturally sensitive approach for each age (HEAT, 2006). Both policy statements encourage BF by mothers for at least 6 months and ideally for 1 year as well as using the BMI, a measure of adiposity based on height, weight, age, and sex, to be plotted on a growth chart (AAP, 2007; HEAT, 2006). Both organizations use the Centers for Disease Control and Prevention (CDC) definitions of overweight and obesity (Barlow & Expert Committee, 2007). A BMI at or above the 85th percentile but below the 95th percentile for age and sex is the definition of overweight in childhood. Obesity is defined as a BMI at or above the 95th percentile for the child’s age and sex (Barlow & Expert Committee, 2007). Counseling about weight is advised at every primary visit (AAP, 2007; Barlow & Expert Committee, 2007; HEAT, 2006). Chivers et al. (2010) used timing of adiposity rebound as a measurement of childhood obesity. Adiposity rebound is defined as the time
in which the BMI curve increases. BMI normally increases during the first year of life then decreases until between ages 4 and 8 years when fatness increases again (Chivers et al., 2010). The earlier the rebound occurs, the higher the adiposity is at the end of growth. Children who are obese have been shown to have much earlier adiposity rebounds compared to nonobese children (Chivers et al., 2010). In addition, there are several comorbidities associated with obesity, making prevention even more important. Table 1 lists the comorbidities found to be directly associated with childhood obesity. One of the many objectives of the Department of Health and Human Services’ (DHHS) Healthy People 2020 Campaign (2009) is to decrease the number of children who are obese, prevent inappropriate weight gain in children, promote BF, and increase BMI screening in primary care offices. Goals for promoting BF include increasing the number of mothers who breastfeed their babies with a goal of exclusive BF for 6 months, decreasing the percentage of breastfed newborns who receive supplemental formula feedings in the first 2 days of life, and increasing the percentage of employers who provide lactation programs (Department of Health and Human Services, 2009). BF is known to reduce respiratory and gastrointestinal infection in the neonate (Horta, Bhla, Martines, & Victora, 2007; Kramer, 2010). 387
The effect of breastfeeding on childhood weight
The recommendations from the AAP’s 2005 policy statement on BF concluded that infants should be breastfed exclusively for the first 6 months and continue to be breastfed with supplemental feedings during the second half of the first year of life. The AAP cited the evidence that BF protects against childhood obesity, asthma, infectious diseases, and certain cancers. The AAP reported that BF is highly cost effective and provides extensive benefits for the mother and child (AAP, 2005). Further evidence that BF is protective against the risk of obesity is found in the Endocrine Society’s clinical practice guidelines (2008). Experts recommend BF for a minimum of 6 months to prevent obesity based on the highest level of evidence set by the researchers’ grading system (August et al., 2008). Additionally, a comprehensive pediatric cost analysis study reported that if there was an increase of exclusive BF for 6 months to 90%, the United States could not only save $13 billion/year, but reduce the death rate by 911 persons annually, with most of them being infants.
Previous systematic reviews on the effect of BF on obesity Harder et al. (2005) used meta-regression analysis, a pool-first method, and a log-linear model to perform a comprehensive meta-analysis of current published studies. The objective was to assess if there is a dosedependent relationship of duration of any BF to the risk of being overweight. Twenty-one studies met the inclusion criteria. All of the included studies had a 95% confidence interval of the association of BF to overweight using BF duration compared to exclusively formula-fed subjects. The duration of BF was inversely and linearly associated with the risk of overweight. Each month of BF was found to cause a 4% decrease in the risk of overweight with a lasting effect of up to 9 months of age. As a result, there was up to a 36% reduction in overweight children. Categorical analysis showed a dose-dependent relationship of BF duration and decreased risk of overweight (Harder et al., 2005). However, four of the studies would not be significant if parental BMI was adjusted (McCrory & Layte, 2012). Another meta-analysis and systematic review examined the effect of infant feeding on later obesity (Owen et al., 2005). Twenty-eight studies were included based on odds ratios of obesity among breastfed subjects versus formula-fed subjects. All of the studies reported that BF was associated with a lower risk of obesity compared to formula feeding. Six studies controlled for three major confounding variables (parental obesity, maternal smoking, and social class) and found that the association between BF and reduction in overweight was decreased, but 388
C. M. Lefebvre & R. M. John
not eliminated. No studies found that BF was related to an increase in childhood obesity. The authors concluded that BF protects against obesity, but felt that further review of confounding factors was needed (Owen et al., 2005). Finally, Arenz et al. (2004) included nine studies in their review and reported a protective effect of BF despite the fact that their data showed no effect on obesity in four of their reviewed studies (Hediger, Overpeck, Kuczmarski, & Ruan, 2001; Li, Parsons, & Power, 2003; O’Callaghan, Williams, Andersen, Bor, & Najmans, 1997; Poulton & Williams, 2001). This review will update the previous systematic reviews and incorporate new evidence in the conclusions.
Objective The purpose of this article is to examine the recent research and literature of the effects of BF on childhood overweight and obesity from 2005 to the beginning of 2012. To examine whether BF can be protective against childhood overweight and obesity, we reviewed all current studies that assessed the relationship between BF and childhood overweight and obesity. The previous meta-analyses resulted in conflicting results of studies because of the inability to perform a valid and reliable research test using BF as a variable, and the presence of confounding variables.
Method This systematic review was performed according to the preferred reporting items for systematic reviews and meta-analyses (PRISMA) statement for reporting systematic reviews (Liberati et al., 2009). A protocol was established in which the criteria included research studies from any country, written in English, from 1/2005 to 3/ 2012, examining the relationship between BF and childhood obesity. Because it is impossible to do a randomized controlled trial randomly assigning exclusively BF or formula feedings to maternal–child dyads, it was decided to include any research studies, aside from case reports. It was decided not to limit the search to only research done in the United States because global diversity is reflected within the United States population. In addition, there is diversity within other countries as reflected by the ethnicity data from the some of the studies.
Information sources Studies were identified using PubMed, CINAHL, and Medline (including OvidMedline, Evidence-Based Medicine [EBM] reviews—Cochrane Database of
The effect of breastfeeding on childhood weight
C. M. Lefebvre & R. M. John
Systematic Reviews, EBM Reviews—ACP Journal Club, EBM Reviews—Database of Abstracts of Reviews of Effects, EBM Reviews—Cochrane Central Register of Controlled Trials, and EBM Reviews—Cochrane Methodology Register, EBM Reviews—Health Technology Assessment, EBM Reviews—NHS Economic Evaluation Database). Search terms included “breastfeeding, obesity prevention,” “breastfeeding, overweight prevention,” “breastfeeding, obesity,” “breastfeeding, overweight,” and “breastfeeding, adiposity.”
Study selection Two reviewers using the above criteria did eligibility assessment of studies independently. Disagreement was handled by discussion and consensus opinion. Table 2 shows a study retrieval flow diagram with the results of the literature search.
Data collection process including data items The information that was gathered on each study included the type of trial; the number, ages, gender, and ethnicity of the research subjects (SAGE); the country of and the method of data collection; the evaluation of parental BMI; how confounding variables were handled; the statistical analysis; the purpose; the extent of loss to follow-up; and the findings of the relationship of BF to obesity.
Results Twenty-one studies met the inclusion criteria for this systematic review after a search of PubMed, CINAHL, and Medline yielded a total of 871 articles. After adjusting for year of publication and duplications, there were 106 articles remaining. A full review of these articles eliminated another 85 articles because they did not meet the inclusion criteria. The combined sample size of all of the studies is 107,177. The ages of the research subjects vary from infancy to adults, complicating the interpretation. In addition, 35,526 of the subjects came from the nurse’s cohort study and the data on BF duration were obtained when the nurses were adults from 25 to 42 years of age, making these BF data exceptionally retrospective (Michels et al., 2007). In most of the studies, the primary outcome was the duration of BF and its effect on BMI. Two of the studies also looked at sugar sweetened beverages (Davis, Whaley, & Goran, 2012) and introduction of solid foods (Griffiths, Smeeth, Hawkins, Cole, & Dezateux, 2009; Michels et al., 2007) in a separate analysis within their studies. Table 3
is a detailed review of the studies that were included in the review.
Discussion Ten of 21 studies reported that BF was found to have no significant effect on childhood obesity in older children 4 years of age and up except for Durmus et al. (2011), who showed a relationship and decreased BMI at 3 and 6 months, but no effect at 1, 2, and 3 years. It should be noted that BMI is not an accurate measure in children under age 2 years. Of the 11 studies that showed that BF had a protective effect on childhood obesity, the authors discussed the limitations of their results. These limitations included inability to control for all confounding variables, appropriate statistical methods to control for confounding variables (Beyerlein, Toschke, and von Kries, 2008), a dropout rate exceeding 30% (Burke et al., 2005; Durmus et al., 2011; Huus et al., 2008), and the lack of effect in matched sibling pairs in his secondary group (Nelson, Gordon-Larsen, & Adair. 2005). Nine of the studies determined that the protective effect on childhood obesity provided by BF is dependent on duration. Two studies established a dose–response relationship by showing that BF duration and exclusivity both played significant roles in the prevention of childhood overweight and obesity (Fallahzadeh, Golestan, Rezvanian, & Ghasemian, 2009; Simon, Souza, & Souza, 2009). In contrast, Novotny et al. (2007) determined that any BF is protective against childhood obesity. It should be noted that only six of the studies used currently obtained data to determine the length of BF (Chivers et al., 2010; Durmus et al., 2011; Sabanayagam, Shankar, Chong, Wong, & Saw, 2009; Scholtens et al., 2007; Weyermann, Rothenbacher, & Brenner, 2006). The use of retrospective information is a definite limitation of the remainder of studies.
BF duration as a protective effect on childhood obesity Duration of BF of at least 4 months was shown to be statistically significant in reducing childhood obesity in four studies. Griffiths et al. (2009) found that children, from birth to 3 years old, who were breastfed for less than 4 months were heavier, had more adipose tissue, gained weight quicker, and were at a higher risk for obesity than children who were breastfed for at least 4 months. Similarly, at age 1, children who were breastfed for at least 4 months were found to have lower BMIs than children breastfed for less than 4 months (Scholtens et al., 2007). Children who were breastfed for less than or equal to 4 months had earlier adiposity rebound, higher BMI at 389
The effect of breastfeeding on childhood weight
C. M. Lefebvre & R. M. John
Table 2 Flow diagram for study retrieval
N = 871 articles identified from the literature search (466 from PubMed, 336 from Medline, including OvidMedline, EBM Reviews- Cochrane Database of Systematic Reviews, EBM Reviews- ACP Journal Club, EBM ReviewsDatabase of Abstracts of Reviews of Effects, EBM Reviews- Cochrane Central Register of Controlled Trials, EBM Reviews- Cochrane Methodology Register, EBM ReviewsHealth Technology Assessment, EBM Reviews- NHS Economic Evaluation Database, and 88 from CINHAL)
328 articles excluded for publication date prior to 2005
NN= = 542 543 60 articles removed for duplication in databases
N = 483 380 articles excluded after title and abstract review
N = 127 106 articles excluded after full text review
N = 21
time of rebound, and higher BMI over time compared to children breastfed for longer than 4 months (Chivers et al., 2010). Other studies showed correlations between different durations of BF on overweight and obesity in childhood. A minimum of 6 months was found to be protective in two studies (Toschke et al., 2007; Weyermann et al., 2006). Children who were breastfed for at least 6 months had a decreased risk of overweight compared to children breastfed for less than 3 months (Weyermann et al., 2006). One to 3 months of BF was recommended by Neutzling et al. (2009), and BF for 9 months, compared with BF for less than 3 months, was shown to be 390
protective for girls (boys showed a less consistent effect) in the study by Nelson, Gordon-Larsen, and Adair (2005). Exclusivity of BF has also been shown to have an effect on childhood obesity. Simon et al. (2009) found that exclusive BF for 6 months or more and BF for more than 24 months were protective factors against overweight and obesity. Children breastfed for greater than 24 months were also less likely to be overweight than children breastfed for 12–24 months, who were less likely to be overweight than children breastfed for shorter than 12 months (Fallahzadeh et al., 2009). The same trends were observed with BF exclusivity in this study (Fallahzadeh et al., 2009). For children exclusively
2291 3–6 year olds 1092 males 1199 females Ethnicity not reported Kuwait
SAGE and country
Burke et al. (2005) Longitudinal analysis study
2087 children at birth but decreased to 1430 children at 8 years Gender and ethnicity not specified Australia
9368 preschool children Beyerlein et al. 52% male (2008) 48% female Retrospective Ethnicity not reported analysis in which Germany duration of BF was missing for most of the subjects
Araujo et al. (2006) 1273 4 year olds Prospective 49.2% female population50.8% male based Ethnicity not reported birth cohort Brazil study
Al-Qaoud et al. (2009) Respective analysis study
Author and year Type of study Child’s gender Age Birthweight. Gestational age Duration of breastfeeding Mother’s age Mother BMI status Mother’s education
Confounding variables addressed
Interviews from the mother were Birthweight Maternal BMI done from birth until the Maternal education mother stopped BF. BMI scores Parity were then done on children at Maternal age 1, 3, 6, and 8 years of age Smoking status Retrospective BF information Data were analyzed using mixed models CI 95%
Socioeconomic status (SES) Maternal education Maternal smoking in pregnancy Maternal BMI at start of pregnancy Weight gain during pregnancy Infant skin color Infant sex Infant birthweight Asset index Gender Height, weight, and BMI were Age measured. Questionnaires were Smoking in pregnancy obtained TV watching Retrospective BF information Maternal BMI Linear, logistic, and quantile Parental social status regression model Early weight gain
Height, weight, and BMI were measured. Results were compared to data from the Kuwaiti Nutrition Surveillance System from 2003 to 2004 Retrospective breastfeeding information Multinomial logistical regression analysis 95% confidence interval (CI) Prospective cohort Retrospective BF information Logistic regression models 95% CI
Methods of data collection/statistical analysis
Table 3 Review of the literature from 2005 to 2011: summaries of studies (in alphabetical order)
No significant association between BF and its duration and obesity prevention Other factors suggested to play a role include diet, exercise, maternal BMI, gender, age, birthweight Felt results may reflect modernization of country leading to increase food consumption and sedentary lifestyle (not evaluated in study) • No loss to follow-up reported
To assess whether BF has an effect in different percentiles of children’s BMI distribution
In the linear regression model, no association was found In the logistic model there was a significant relationship The association between BF and childhood BMI might be related to the statistical method used to obtain results BF might prevent overweight and obesity rather than a shift in the entire BMI distribution A dose–response relationship was not found To research the Children who were breastfed >12 months had relationship between BF lower BMIs at 1 year old than those breastfed and childhood adiposity
