Abstract

Background

Childhood obesity predisposes to adult obesity and increases the risk of many diseases. Schools provide a vehicle to deliver public health interventions to all children.

Methods

Medline and Embase were used to undertake a systematic review of published studies of school-based interventions aimed at reducing the body mass index (BMI) of children ≤ 18 years. Preferred reporting items for systematic reviews and meta-analyses guidelines were followed, and eligible studies subjected to a random effects meta-analysis.

Results

Between 1991 and 2010, 43 published studies provided 60 measurements of effect. The pooled effect was a 0.17 (95% CI: 0.08, 0.26, P< 0.001) reduction in BMI. Heterogeneity was high (I2= 93.4%) but there was no significant small study bias (Egger's test, P= 0.422) nor significant variation by length of follow-up. The intervention comprised physical activity only in 11 (26%) studies, education only in three (7%), and combinations of these and improved nutrition in the remaining 29 (67%). On stratified analysis, physical activity used in isolation (−0.13, 95% CI: −0.22, −0.04, P= 0.001) or combined with improved nutrition (−0.17, 95% CI: −0.29, −0.06, P< 0.001) was associated with significant improvements in BMI. Interventions targeted at overweight/obese children reduced their BMI by 0.35 (95% CI: 0.12, 0.58, P= 0.003). Those delivered to all children reduced it by 0.16 (95% CI: 0.06, 0.25, P= 0.002).

Conclusions

There is growing evidence that school-based interventions that contain a physical activity component may be effective in helping to reduce BMI in children.

Introduction

The increasing prevalence of childhood obesity poses a major threat to public health. In the USA, the prevalence of severe [defined as body mass index (BMI) ≥ 99th centile] childhood obesity has tripled in the last 25 years.1 Obesity increases the risk of many conditions, including type II diabetes, hypertension, cardiovascular disease and musculoskeletal disease.2 Lifestyle behaviours developed in childhood tend to perpetuate into adulthood. Hence, obese children are more likely to become obese adults.3 The WHO4 has acknowledged that childhood interventions are required to combat adult obesity effectively. In the UK, education is free to all children between 3 and 18 years of age. Therefore, schools provide an ideal vehicle for delivering public health interventions to all children,5 including those from the most socio-economically deprived communities who are most at risk,6–8 and hardest to reach. According to the primary prevention strategy first mooted by Rose,9 small population shifts in BMI may be more effective at a population level than simply reducing the prevalence of obesity. The most recent meta-analysis of school-based interventions included studies published up to 2007.10 It demonstrated a significant reduction in the prevalence of obesity but, at that time, there was no evidence of a significant overall reduction in BMI. Because of the increasing public health importance of childhood obesity, many studies have been published more recently. Therefore, we conducted an up-to-date meta-analysis of published studies that evaluated the impact of school-based interventions on the body mass index (BMI) of pupils.

Methods

Systematic review

A literature review was conducted in parallel by H.V.L. and J.P.P. in accordance with the preferred reporting items for systematic reviews and meta-analyses (PRISMA) guidelines.11 The search was undertaken using the Medline and Embase databases, applying the following search terms and Boolean connectors to titles, abstracts and subject headings: (child OR children OR childhood OR toddler* OR school-age* OR schoolage* OR infant* OR pediatric* OR paediatric*) AND (school* OR kindergarten* OR creche OR nursery OR nurseries OR afterschool) AND (prevent* OR intervention*) AND [(obes* OR overweight OR (weight adj1 gain)) OR ((increase* OR gain* OR change*) adj2 (BMI OR body mass index))]. The electronic search was limited to studies conducted on human subjects of 18 years of age or younger that were published in or translated into English. No restrictions were placed on publication date so as to include as many studies as possible. Duplicate articles were excluded. The last date on which the electronic search was run was 21 February 2011. The identified articles were reviewed manually and the following inclusion criteria applied: Non-randomized intervention studies were not excluded. Where more than one article was found relating to the same study, the most recent publication was used. The reference lists of both review articles and eligible original articles were searched manually to identify any additional eligible articles not found as a result of the electronic search.

  • children aged 18 years of age or younger,

  • any intervention delivered in a school setting and aimed at decreasing BMI or weight,

  • effect reported as the mean change in BMI or this could be calculated from the pre- and post-intervention data provided and

  • inclusion of a control group which received no intervention beyond normal school-based activities and for which change in BMI was also reported or able to be calculated.

Meta-analysis

Study characteristics were extracted and recorded: publication year, country, age and sex of participants, study size and design, selection criteria, nature, timing and duration of the intervention, and length of follow-up. Where follow-up results were recorded at different time points, the longest follow-up measure was used and, where available, sub-group results were used in favour of overall results. For studies that did not report the confidence interval or standard deviation (SD) for the mean change in BMI, this was imputed from the studies that did. Correlation coefficients were derived for the intervention and control groups using the formula: Corr = (SD2baseline + SD2final − SD2change)/(2 × SDbaseline × SDfinal). The SD of the change in BMI was then calculated using the formula: √(SD2baseline + SD2final − (2 × Corr × SDbaseline × SDfinal)). A random effects meta-analysis was conducted on the full dataset and then repeated stratified by sex and then intervention type. I2 was calculated as a measure of heterogeneity between studies. Bias was assessed both subjectively, using a funnel plot, and formally, using Egger's regression asymmetry test for small study bias. The influence of individual studies on the overall effect size was assessed using a meta-influence plot and a cumulative meta-analysis was performed to determine whether the pooled effect size changed over time as new studies were published. Univariate and multivariate meta-regression analyses were used to determine the effect of specific study characteristics on the overall effect size and, therefore, potential sources of between-study heterogeneity. Meta-regression analyses were subjected to 20 000 permutations to adjust for multiple testing, and therefore reduce the chance of type 1 errors. The adjusted R2 and residual I2 values were calculated in order to determine how much of the effect size was accounted for by the study characteristics recorded and how much heterogeneity remained after taking account of these. A bubble plot was produced to determine whether there was any relationship between length of follow-up and effect size. All analyses were performed using Stata version 11.1.

Results

Systematic review

The electronic search identified 1886 articles and the manual search of reference lists identified a further 195. Following exclusion of 466 duplicate articles, the remaining 1615 articles were reviewed manually. Of these, 1572 were excluded: 913 were irrelevant, 240 involved no intervention and, in 84, the interventions were not school-based, 183 evaluated effect using a measure other than BMI, 144 did not provide essential data, one study was not published in English and seven papers were rendered redundant by more recent publications based on the same study. Therefore, 43 studies met all of the inclusion criteria and were included in the meta-analysis.12–54

The 43 studies were published between 1991 and 2010 and included a total of 36 579 pupils. Sixteen (37%) of the eligible studies were conducted in Europe,12–27 19 (44%) in America,28–46 5 (12%) in Asia,47–51 2 (5%) in Australasia52,53 and 1 (2%) in Africa54 (Table 1). Nine (21%) studies recruited more than 1000 pupils,24,27,28,31,37,41,45,47,48 and 38 (88%) were randomized or cluster-randomized-controlled trials.12–23,25–34,36–38,40–43,46–54 Two (5%) studies were based in nursery or kindergarten (under 5 years of age),33,34 26 (60%) in primary schools (5–11 years of age)12–17,19–21,24,25,28,29,31,36,37,39,41–49 and 15 (35%) in secondary schools (12–18 years of age).18,22,23,26,27,30,32,35,38,40,50–54 Thirty-seven (86%) studies included all pupils irrespective of baseline weight,12,14–28,30,31,33–37,39,41–49,52–54 but 6 (14%) restricted inclusion to overweight pupils.13,29,32,38,40,51 All of the interventions were conducted on school premises. Thirty-two (74%) took place during school-time,12,14–16,18–24,27,28,30–37,41–43,45–46,48–51,52 8 (19%) were conducted after school hours,13,17,25,29,39,40,44,54 and 3 (7%) used a combination of these approaches.24,45,51 The duration of the intervention ranged from 1 month to 6 years, and the maximum length of follow-up was 6 years.

Table 1

Characteristics of studies examining the effect of school-based interventions on body mass index

StudyYearCountryStudy designSexWeight criteriaSchool ageTimingIntervention typeIntervention duration (months)
Angelopoulos et al.122009GreeceCluster RCTMFNonePrimarySchool-timePA, N12
Barbeau292007USARCTFOverweightPrimaryAfter schoolPA10
Bayne-Smith302004USACluster RCTFNoneSecondarySchool-timePA, N24
Caballero et al.312003USARCTMFNonePrimarySchool-timePA, N36
Carrel et al.322005USARCTMFOverweightSecondarySchool-timePA, N9
Dennison et al.332004USARCTMFNonePre-schoolSchool-timeSB8
Donnelly et al.282009USACluster RCTMFNonePrimarySchool-timePA36
Duncan et al.172009UKRCTMFNonePrimaryAfter schoolPA15
El Ansari et al.542010EgyptRCTM, FNoneSecondaryAfter schoolPA3
Fitzgibbon et al.342006USACluster RCTMFNonePre-schoolSchool-timePA, N3
Flores351995USAEfficacy trialFNoneSecondarySchool-timePA, N3
Foster et al.362008USACluster RCTMFNonePrimarySchool-timeN24
Graf et al.132006GermanyCluster RCTMFOverweightPrimaryAfter schoolPA, N9
Graf et al.142008GermanyCluster RCTMFNonePrimarySchool-timeN48
Haerens et al.182006BelgiumCluster RCTM, FNoneSecondarySchool-timePA, N24
Harrell et al.371996USARCTMFNonePrimarySchool-timePA, N2
Harrison et al.192006IrelandCluster RCTMFNonePrimarySchool-timePA, SB4
James et al.152007UKCluster RCTMFNonePrimarySchool-timeN12
Jiang et al.472007ChinaCluster RCTM, FNonePrimaryBothPA, N, SB36
Johnston et al.382008USARCTMFOverweightSecondarySchool-timePA, N6
Kain et al.452008ChileNon RCTM, FNonePrimarySchool-timePA, N21
Kipping et al.202008UKPilot cluster RCTMFNonePrimarySchool-timePA, N, SB5
Kriemler et al.212009SwitzerlandCluster RCTMFNonePrimarySchool-timePA10
Li et al.482010ChinaCluster RCTMFNonePrimarySchool-timePA12
Lionis et al. 221991GreeceCluster RCTMFNoneSecondarySchool-timePA, N12
Manios et al.162002GreeceCluster RCTMFNonePrimarySchool-timePA, N72
Matvienko and Ahrabi-Fard392010USAQuasi-experimentalMFNonePrimaryAfter schoolPA1
Melnyk et al.402007USAPilot RCTMFOverweightSecondaryAfter schoolPA, N2
Mihas et al.232009GreeceRCTMFNoneSecondarySchool-timePA, N3
Mo-suwan et al.491998ThailandCluster RCTM, FNonePrimarySchool-timePA7
Nader et al.411999USACluster RCTMFNonePrimarySchool-timePA, N36
Peralta et al.522009AustraliaPilot RCTMNoneSecondarySchool-timePA, N, SB6
Plachta-Danielzik et al.242007GermanyQuasi-RCTMFNonePrimarySchool-timePA, SB12
Robinson421999USARCTMFNonePrimarySchool-timeSB6
Salcedo Aguilar et al.252010SpainCluster RCTMFNonePrimaryAfter schoolPA6
Sichieri et al.462008BrazilCluster RCTMFNonePrimarySchool-timeN7
Simon et al.262008FranceRCTMFNoneSecondaryBothPA, SB48
Singh et al.272009NetherlandsRCTMFNoneSecondarySchool-timePA, N, SB8
Singhal et al.502010IndiaCluster RCTMFNoneSecondarySchool-timePA, N6
Stock et al.432007CanadaPilot prospective studyMFNonePrimarySchool-timePA, N5
Vandongen et al.531995AustraliaCluster RCTM, FNoneSecondaryBothPA, N9
Wong et al.512008SingaporeRCTMOverweightSecondarySchool-timePA3
Yin et al.442005USACluster RCTMFNonePrimaryAfter schoolPA8
StudyYearCountryStudy designSexWeight criteriaSchool ageTimingIntervention typeIntervention duration (months)
Angelopoulos et al.122009GreeceCluster RCTMFNonePrimarySchool-timePA, N12
Barbeau292007USARCTFOverweightPrimaryAfter schoolPA10
Bayne-Smith302004USACluster RCTFNoneSecondarySchool-timePA, N24
Caballero et al.312003USARCTMFNonePrimarySchool-timePA, N36
Carrel et al.322005USARCTMFOverweightSecondarySchool-timePA, N9
Dennison et al.332004USARCTMFNonePre-schoolSchool-timeSB8
Donnelly et al.282009USACluster RCTMFNonePrimarySchool-timePA36
Duncan et al.172009UKRCTMFNonePrimaryAfter schoolPA15
El Ansari et al.542010EgyptRCTM, FNoneSecondaryAfter schoolPA3
Fitzgibbon et al.342006USACluster RCTMFNonePre-schoolSchool-timePA, N3
Flores351995USAEfficacy trialFNoneSecondarySchool-timePA, N3
Foster et al.362008USACluster RCTMFNonePrimarySchool-timeN24
Graf et al.132006GermanyCluster RCTMFOverweightPrimaryAfter schoolPA, N9
Graf et al.142008GermanyCluster RCTMFNonePrimarySchool-timeN48
Haerens et al.182006BelgiumCluster RCTM, FNoneSecondarySchool-timePA, N24
Harrell et al.371996USARCTMFNonePrimarySchool-timePA, N2
Harrison et al.192006IrelandCluster RCTMFNonePrimarySchool-timePA, SB4
James et al.152007UKCluster RCTMFNonePrimarySchool-timeN12
Jiang et al.472007ChinaCluster RCTM, FNonePrimaryBothPA, N, SB36
Johnston et al.382008USARCTMFOverweightSecondarySchool-timePA, N6
Kain et al.452008ChileNon RCTM, FNonePrimarySchool-timePA, N21
Kipping et al.202008UKPilot cluster RCTMFNonePrimarySchool-timePA, N, SB5
Kriemler et al.212009SwitzerlandCluster RCTMFNonePrimarySchool-timePA10
Li et al.482010ChinaCluster RCTMFNonePrimarySchool-timePA12
Lionis et al. 221991GreeceCluster RCTMFNoneSecondarySchool-timePA, N12
Manios et al.162002GreeceCluster RCTMFNonePrimarySchool-timePA, N72
Matvienko and Ahrabi-Fard392010USAQuasi-experimentalMFNonePrimaryAfter schoolPA1
Melnyk et al.402007USAPilot RCTMFOverweightSecondaryAfter schoolPA, N2
Mihas et al.232009GreeceRCTMFNoneSecondarySchool-timePA, N3
Mo-suwan et al.491998ThailandCluster RCTM, FNonePrimarySchool-timePA7
Nader et al.411999USACluster RCTMFNonePrimarySchool-timePA, N36
Peralta et al.522009AustraliaPilot RCTMNoneSecondarySchool-timePA, N, SB6
Plachta-Danielzik et al.242007GermanyQuasi-RCTMFNonePrimarySchool-timePA, SB12
Robinson421999USARCTMFNonePrimarySchool-timeSB6
Salcedo Aguilar et al.252010SpainCluster RCTMFNonePrimaryAfter schoolPA6
Sichieri et al.462008BrazilCluster RCTMFNonePrimarySchool-timeN7
Simon et al.262008FranceRCTMFNoneSecondaryBothPA, SB48
Singh et al.272009NetherlandsRCTMFNoneSecondarySchool-timePA, N, SB8
Singhal et al.502010IndiaCluster RCTMFNoneSecondarySchool-timePA, N6
Stock et al.432007CanadaPilot prospective studyMFNonePrimarySchool-timePA, N5
Vandongen et al.531995AustraliaCluster RCTM, FNoneSecondaryBothPA, N9
Wong et al.512008SingaporeRCTMOverweightSecondarySchool-timePA3
Yin et al.442005USACluster RCTMFNonePrimaryAfter schoolPA8

USA, United States of America; UK, United Kingdom; RCT, randomized-controlled trial; M, male only; F, female only; MF, male and female reported together; M, F, male and female reported separately; PA, physical activity; N, nutrition; SB, sedentary behaviour.

Table 1

Characteristics of studies examining the effect of school-based interventions on body mass index

StudyYearCountryStudy designSexWeight criteriaSchool ageTimingIntervention typeIntervention duration (months)
Angelopoulos et al.122009GreeceCluster RCTMFNonePrimarySchool-timePA, N12
Barbeau292007USARCTFOverweightPrimaryAfter schoolPA10
Bayne-Smith302004USACluster RCTFNoneSecondarySchool-timePA, N24
Caballero et al.312003USARCTMFNonePrimarySchool-timePA, N36
Carrel et al.322005USARCTMFOverweightSecondarySchool-timePA, N9
Dennison et al.332004USARCTMFNonePre-schoolSchool-timeSB8
Donnelly et al.282009USACluster RCTMFNonePrimarySchool-timePA36
Duncan et al.172009UKRCTMFNonePrimaryAfter schoolPA15
El Ansari et al.542010EgyptRCTM, FNoneSecondaryAfter schoolPA3
Fitzgibbon et al.342006USACluster RCTMFNonePre-schoolSchool-timePA, N3
Flores351995USAEfficacy trialFNoneSecondarySchool-timePA, N3
Foster et al.362008USACluster RCTMFNonePrimarySchool-timeN24
Graf et al.132006GermanyCluster RCTMFOverweightPrimaryAfter schoolPA, N9
Graf et al.142008GermanyCluster RCTMFNonePrimarySchool-timeN48
Haerens et al.182006BelgiumCluster RCTM, FNoneSecondarySchool-timePA, N24
Harrell et al.371996USARCTMFNonePrimarySchool-timePA, N2
Harrison et al.192006IrelandCluster RCTMFNonePrimarySchool-timePA, SB4
James et al.152007UKCluster RCTMFNonePrimarySchool-timeN12
Jiang et al.472007ChinaCluster RCTM, FNonePrimaryBothPA, N, SB36
Johnston et al.382008USARCTMFOverweightSecondarySchool-timePA, N6
Kain et al.452008ChileNon RCTM, FNonePrimarySchool-timePA, N21
Kipping et al.202008UKPilot cluster RCTMFNonePrimarySchool-timePA, N, SB5
Kriemler et al.212009SwitzerlandCluster RCTMFNonePrimarySchool-timePA10
Li et al.482010ChinaCluster RCTMFNonePrimarySchool-timePA12
Lionis et al. 221991GreeceCluster RCTMFNoneSecondarySchool-timePA, N12
Manios et al.162002GreeceCluster RCTMFNonePrimarySchool-timePA, N72
Matvienko and Ahrabi-Fard392010USAQuasi-experimentalMFNonePrimaryAfter schoolPA1
Melnyk et al.402007USAPilot RCTMFOverweightSecondaryAfter schoolPA, N2
Mihas et al.232009GreeceRCTMFNoneSecondarySchool-timePA, N3
Mo-suwan et al.491998ThailandCluster RCTM, FNonePrimarySchool-timePA7
Nader et al.411999USACluster RCTMFNonePrimarySchool-timePA, N36
Peralta et al.522009AustraliaPilot RCTMNoneSecondarySchool-timePA, N, SB6
Plachta-Danielzik et al.242007GermanyQuasi-RCTMFNonePrimarySchool-timePA, SB12
Robinson421999USARCTMFNonePrimarySchool-timeSB6
Salcedo Aguilar et al.252010SpainCluster RCTMFNonePrimaryAfter schoolPA6
Sichieri et al.462008BrazilCluster RCTMFNonePrimarySchool-timeN7
Simon et al.262008FranceRCTMFNoneSecondaryBothPA, SB48
Singh et al.272009NetherlandsRCTMFNoneSecondarySchool-timePA, N, SB8
Singhal et al.502010IndiaCluster RCTMFNoneSecondarySchool-timePA, N6
Stock et al.432007CanadaPilot prospective studyMFNonePrimarySchool-timePA, N5
Vandongen et al.531995AustraliaCluster RCTM, FNoneSecondaryBothPA, N9
Wong et al.512008SingaporeRCTMOverweightSecondarySchool-timePA3
Yin et al.442005USACluster RCTMFNonePrimaryAfter schoolPA8
StudyYearCountryStudy designSexWeight criteriaSchool ageTimingIntervention typeIntervention duration (months)
Angelopoulos et al.122009GreeceCluster RCTMFNonePrimarySchool-timePA, N12
Barbeau292007USARCTFOverweightPrimaryAfter schoolPA10
Bayne-Smith302004USACluster RCTFNoneSecondarySchool-timePA, N24
Caballero et al.312003USARCTMFNonePrimarySchool-timePA, N36
Carrel et al.322005USARCTMFOverweightSecondarySchool-timePA, N9
Dennison et al.332004USARCTMFNonePre-schoolSchool-timeSB8
Donnelly et al.282009USACluster RCTMFNonePrimarySchool-timePA36
Duncan et al.172009UKRCTMFNonePrimaryAfter schoolPA15
El Ansari et al.542010EgyptRCTM, FNoneSecondaryAfter schoolPA3
Fitzgibbon et al.342006USACluster RCTMFNonePre-schoolSchool-timePA, N3
Flores351995USAEfficacy trialFNoneSecondarySchool-timePA, N3
Foster et al.362008USACluster RCTMFNonePrimarySchool-timeN24
Graf et al.132006GermanyCluster RCTMFOverweightPrimaryAfter schoolPA, N9
Graf et al.142008GermanyCluster RCTMFNonePrimarySchool-timeN48
Haerens et al.182006BelgiumCluster RCTM, FNoneSecondarySchool-timePA, N24
Harrell et al.371996USARCTMFNonePrimarySchool-timePA, N2
Harrison et al.192006IrelandCluster RCTMFNonePrimarySchool-timePA, SB4
James et al.152007UKCluster RCTMFNonePrimarySchool-timeN12
Jiang et al.472007ChinaCluster RCTM, FNonePrimaryBothPA, N, SB36
Johnston et al.382008USARCTMFOverweightSecondarySchool-timePA, N6
Kain et al.452008ChileNon RCTM, FNonePrimarySchool-timePA, N21
Kipping et al.202008UKPilot cluster RCTMFNonePrimarySchool-timePA, N, SB5
Kriemler et al.212009SwitzerlandCluster RCTMFNonePrimarySchool-timePA10
Li et al.482010ChinaCluster RCTMFNonePrimarySchool-timePA12
Lionis et al. 221991GreeceCluster RCTMFNoneSecondarySchool-timePA, N12
Manios et al.162002GreeceCluster RCTMFNonePrimarySchool-timePA, N72
Matvienko and Ahrabi-Fard392010USAQuasi-experimentalMFNonePrimaryAfter schoolPA1
Melnyk et al.402007USAPilot RCTMFOverweightSecondaryAfter schoolPA, N2
Mihas et al.232009GreeceRCTMFNoneSecondarySchool-timePA, N3
Mo-suwan et al.491998ThailandCluster RCTM, FNonePrimarySchool-timePA7
Nader et al.411999USACluster RCTMFNonePrimarySchool-timePA, N36
Peralta et al.522009AustraliaPilot RCTMNoneSecondarySchool-timePA, N, SB6
Plachta-Danielzik et al.242007GermanyQuasi-RCTMFNonePrimarySchool-timePA, SB12
Robinson421999USARCTMFNonePrimarySchool-timeSB6
Salcedo Aguilar et al.252010SpainCluster RCTMFNonePrimaryAfter schoolPA6
Sichieri et al.462008BrazilCluster RCTMFNonePrimarySchool-timeN7
Simon et al.262008FranceRCTMFNoneSecondaryBothPA, SB48
Singh et al.272009NetherlandsRCTMFNoneSecondarySchool-timePA, N, SB8
Singhal et al.502010IndiaCluster RCTMFNoneSecondarySchool-timePA, N6
Stock et al.432007CanadaPilot prospective studyMFNonePrimarySchool-timePA, N5
Vandongen et al.531995AustraliaCluster RCTM, FNoneSecondaryBothPA, N9
Wong et al.512008SingaporeRCTMOverweightSecondarySchool-timePA3
Yin et al.442005USACluster RCTMFNonePrimaryAfter schoolPA8

USA, United States of America; UK, United Kingdom; RCT, randomized-controlled trial; M, male only; F, female only; MF, male and female reported together; M, F, male and female reported separately; PA, physical activity; N, nutrition; SB, sedentary behaviour.

Fifteen (35%) studies used a single intervention (Table 2): 10 (23%) just physical activity and five (12%) just education. The remaining 28 (65%) used combinations of two of more interventions. In total, 34 (79%) interventions included a physical activity component (such as improved physical education lessons or extra games at break times), 12 (28%) included a behavioural component (such as teaching self-management, self-esteem and decision-making skills) and 6 (14%) included an environmental component (such as changes to school meals or installation of healthy vending machines). Thirty-two of the interventions included one or more educational components (such as a change in the focus of regular lessons, additional lessons, newsletters or workbooks): 28 included education on nutrition, 22 education on physical activity and 9 education on sedentary behaviour. Three (7%) studies targeted only girls,29,30,31 and two (5%) targeted only boys.51,52 The remaining 38 (88%) included both girls and boys but 7 of these reported results separately by sex sub-group.18,25,45,47,49,53,54 Therefore, the 43 studies provided a total of 60 results for inclusion in the meta-analysis.

Table 2

Types of school-based intervention used in studies examining the effect on body mass index

StudyEducational
EnvironmentalBehaviouralPhysical
Physical activityNutritionSedentary behaviour
Angelopoulous12
Barbeau29
Bayne-Smith30
Caballero et al.31
Carrel et al.32
Dennison et al.33
Donnelly et al.28
Duncan et al.17
El Ansari et al.54
Fitzgibbon et al.34
Flores35
Foster et al.36
Graf et al.13
Graf et al.14
Haerens Group 118
Haerens Group 218
Harrell et al.37
Harrison et al.19
James et al.15
Jiang et al.47
Johnston et al.38
Kain et al.45
Kipping et al.20
Kriemler et al.21
Li et al.48
Lionis et al.22
Manios et al.16
Matvienko and Ahrabi-Fard39
Melnyk et al.40
Mihas et al.23
Mo-suwan et al.49
Nader et al.41
Peralta et al.52
Plachta-Danielzik et al.24
Robinson42
Salcedo Aguilar et al.25
Sichieri et al.46
Simon et al.26
Singh et al.27
Singhal et al.50
Stock et al.43
Vandongen Group 153
Vandongen Group 253
Vandongen Group 353
Vandongen Group 453
Vandongen Group 553
Wong et al.51
Yin et al.44
StudyEducational
EnvironmentalBehaviouralPhysical
Physical activityNutritionSedentary behaviour
Angelopoulous12
Barbeau29
Bayne-Smith30
Caballero et al.31
Carrel et al.32
Dennison et al.33
Donnelly et al.28
Duncan et al.17
El Ansari et al.54
Fitzgibbon et al.34
Flores35
Foster et al.36
Graf et al.13
Graf et al.14
Haerens Group 118
Haerens Group 218
Harrell et al.37
Harrison et al.19
James et al.15
Jiang et al.47
Johnston et al.38
Kain et al.45
Kipping et al.20
Kriemler et al.21
Li et al.48
Lionis et al.22
Manios et al.16
Matvienko and Ahrabi-Fard39
Melnyk et al.40
Mihas et al.23
Mo-suwan et al.49
Nader et al.41
Peralta et al.52
Plachta-Danielzik et al.24
Robinson42
Salcedo Aguilar et al.25
Sichieri et al.46
Simon et al.26
Singh et al.27
Singhal et al.50
Stock et al.43
Vandongen Group 153
Vandongen Group 253
Vandongen Group 353
Vandongen Group 453
Vandongen Group 553
Wong et al.51
Yin et al.44
Table 2

Types of school-based intervention used in studies examining the effect on body mass index

StudyEducational
EnvironmentalBehaviouralPhysical
Physical activityNutritionSedentary behaviour
Angelopoulous12
Barbeau29
Bayne-Smith30
Caballero et al.31
Carrel et al.32
Dennison et al.33
Donnelly et al.28
Duncan et al.17
El Ansari et al.54
Fitzgibbon et al.34
Flores35
Foster et al.36
Graf et al.13
Graf et al.14
Haerens Group 118
Haerens Group 218
Harrell et al.37
Harrison et al.19
James et al.15
Jiang et al.47
Johnston et al.38
Kain et al.45
Kipping et al.20
Kriemler et al.21
Li et al.48
Lionis et al.22
Manios et al.16
Matvienko and Ahrabi-Fard39
Melnyk et al.40
Mihas et al.23
Mo-suwan et al.49
Nader et al.41
Peralta et al.52
Plachta-Danielzik et al.24
Robinson42
Salcedo Aguilar et al.25
Sichieri et al.46
Simon et al.26
Singh et al.27
Singhal et al.50
Stock et al.43
Vandongen Group 153
Vandongen Group 253
Vandongen Group 353
Vandongen Group 453
Vandongen Group 553
Wong et al.51
Yin et al.44
StudyEducational
EnvironmentalBehaviouralPhysical
Physical activityNutritionSedentary behaviour
Angelopoulous12
Barbeau29
Bayne-Smith30
Caballero et al.31
Carrel et al.32
Dennison et al.33
Donnelly et al.28
Duncan et al.17
El Ansari et al.54
Fitzgibbon et al.34
Flores35
Foster et al.36
Graf et al.13
Graf et al.14
Haerens Group 118
Haerens Group 218
Harrell et al.37
Harrison et al.19
James et al.15
Jiang et al.47
Johnston et al.38
Kain et al.45
Kipping et al.20
Kriemler et al.21
Li et al.48
Lionis et al.22
Manios et al.16
Matvienko and Ahrabi-Fard39
Melnyk et al.40
Mihas et al.23
Mo-suwan et al.49
Nader et al.41
Peralta et al.52
Plachta-Danielzik et al.24
Robinson42
Salcedo Aguilar et al.25
Sichieri et al.46
Simon et al.26
Singh et al.27
Singhal et al.50
Stock et al.43
Vandongen Group 153
Vandongen Group 253
Vandongen Group 353
Vandongen Group 453
Vandongen Group 553
Wong et al.51
Yin et al.44

Meta-analysis

Of the 60 results, 40 suggested a reduction in BMI in the intervention group compared with the control group12,13,16–19,21–23,25,26,29–31,34–36,38,39,42–45,47–53 and 16 achieved statistical significance.12,16,18,21–23,29,32,33,45,47,48,54 In the overall random effects meta-analysis, the pooled estimate of BMI change was −0.17 kg/m2 (95% CI: −0.26, −0.08, P< 0.001; Fig. 1). In the stratified analyses, the reduction reached statistical significance in girls (−0.28, 95% CI: −0.50, −0.06, P= 0.012) but not boys (−0.17, 95% CI: −0.26, −0.08, P= 0.533). Following stratification by intervention type, the reduction in BMI was statistically significant for physical activity used in isolation (−0.13, 95% CI: −0.22, −0.04), and in combination with improved nutrition (−0.17, 95% CI: −0.29, −0.06). Of the 60 results, six were derived from interventions targeted at overweight or obese children and the remaining 54 were delivered to all children. When the meta-analysis was re-run separately for these two sub-groups, interventions delivered to just overweight and obese children produced a change in BMI of −0.35 (95% CI: −0.58, −0.12, P= 0.003) and interventions delivered to all children produced a change of −0.16 (95% CI: −0.25, −0.06, P= 0.002).

Fig. 1

Forest plot of randomized-effects meta-analysis of studies examining the effect of school-based interventions on body mass index. ES, effect size; CI, confidence interval; M, male; F, female.

Overall, heterogeneity was high (I2 = 93.4%). In the multivariate meta-regression analysis, none of the study characteristics were significant predictors of effect size study. The adjusted R2 for the multivariate meta-regression analysis was 9.74% and the residual I2 value was 86.7%. The funnel plot showed no major asymmetry (Fig. 2), and Egger's test was non-significant (bias coefficient −0.692, 95% CI: −2.407, 1.022, P= 0.422). The meta-influence plot showed that three results obtained from two studies had a large impact on the overall effect size.12,47 In the cumulative meta-analysis, the earliest studies showed a larger effect size but the pooled estimate has been stable and statistically significant since 2007. The bubble plot showed no relationship between the length of follow-up and effect size (Fig. 3).

Fig. 2

Funnel plot of studies examining the effect of school-based interventions on body mass index.

Fig. 3

Bubble plot of the univariate relationship between length of follow-up and reported effect size among studies examining the effect of school-based interventions on body mass index. The size of the bubble is proportional to the weight of studies in the meta-analysis.

Discussion

Main findings of the study

There is accumulating evidence that school-based interventions can significantly reduce children's BMI, especially if they include a physical exercise component. The evidence is reasonably consistent, in that a relatively large number of studies have now demonstrated a benefit. The effect size did not vary by length of follow-up suggesting that the benefits may be maintained over time, but only one study has followed-up participants for more than 4 years. Evidence of significant benefit is currently lacking for interventions that do not include a physical activity component. The absolute reduction in BMI was greater for interventions targeted at overweight and obese children, but studies delivered to all children nonetheless produced a significant reduction in overall BMI.

What is already known on this topic?

The prevalence of childhood obesity in developed countries is high and increasing, focusing attention on the urgent need to identify effective interventions.1 Interventions can be targeted at individuals, families, the whole population or our obesogenic environment and all play a role. In a recent survey, 65% of American citizens believed that schools have a major role to play in tackling the obesity epidemic and only 7% believe that the school had no role to play at all.55 The current NICE5 guidelines also recommend school-based interventions.

Earlier meta-analyses demonstrated conflicting results.10,56–58 The most recent, published in 2009, included 19 studies published up to 2007.10 Since then, an additional 21 eligible studies have been published. Therefore, an updated review is timely.

What this study adds?

Previous meta-analyses had already demonstrated the potential of school-based interventions to reduce the prevalence of obesity. Inclusion of more recent studies enabled us to demonstrate that a statistically significant reduction in overall BMI is also achievable. The absolute benefit was a 0.17 kg/m2 reduction in BMI. This was statistically significant but is unlikely to be clinically significant at an individual level. It may, nonetheless, produce tangible health benefits at a population level. As first described by Rose, a small shift in population distribution can be an effective primary preventative strategy because more events occur among the large number of individuals at moderate risk than the small number at high risk.10

Strengths and limitations

Our study included data collected on 36 579 pupils, and was conducted in accordance with PRISMA guidelines. Random effects meta-analysis was chosen over fixed-effect because of differences in inclusion criteria and the nature of the intervention. Published studies have used a number of different anthropometric measures. By necessity, the meta-analysis needed to be based on studies using the same measure. Following a preliminary review, we chose BMI change as it was the most commonly used measure, enabling us to include the maximum number of studies. The need to exclude similar studies that used other measures, such as individual percentage fat mass or the overall percentage of pupils that were overweight, is an obvious limitation. Use of BMI z-score would have been preferable to the use of absolute BMI. However, only a minority of studies reported their results in terms of a change in z-score, therefore this was not possible. Furthermore, BMI may not be the best measure of childhood adiposity nor the best predictor of adult adiposity.59 Where studies reported change in BMI adjusted for potential confounders, the adjusted result was used in the meta-analysis. However, some studies reported only unadjusted results which may be subject to bias. Some studies did not report SDs or confidence intervals for their results. In order to include as many studies as possible, we derived SDs for 16 studies that did not report this information. Since, the correlation coefficients for intervention and control groups were within one decimal place of each other (0.802 for intervention groups and 0.891 for control groups), this approach is unlikely to have introduced a large or systematic error and enabled us to include the maximum number of studies. Because of the small number of studies conducted in this area, we included non-randomized intervention studies. This is likely to have added to the heterogeneity of the results. In the future, as more studies become available, it would be useful to repeat the meta-analysis excluding non-randomized studies.

Conclusions

School-based interventions can reduce the BMI of pupils. The meta-analysis identified several areas where further research would be useful. The interventions examined to date appear to be less effective in boys than girls and further work is required to explore the reasons and whether they require modifications to the school-based interventions or an alternative approach. Existing studies suggest a benefit up to 6 years follow-up. Further research is required to determine whether it is maintained thereafter. Benefit has been demonstrated for a number of different types of intervention. Further research is required to determine the ideal type of intervention, taking cognisance of cost-effectiveness as well as clinical effectiveness.

References

1
Skelton
JA
Cook
SR
Auinger
P
, et al. 
Prevalence and trends of severe obesity among US children and adolescents
Acad Pediatr
2009
, vol. 
9
 
5
(pg. 
322
-
9
)
2
Ebbeling
CB
Pawlak
DB
Ludwig
DS
Childhood obesity: public-health crisis, common sense cure
Lancet
2002
, vol. 
260
 (pg. 
473
-
82
)
3
Ylihärsilä
H
Kajantie
E
Osmond
C
, et al. 
Body mass index during childhood and adult body composition in men and women aged 56–70 y
Am J Clin Nutr
2008
, vol. 
87
 (pg. 
1769
-
75
)
4
World Health Organisation
Obesity: preventing and managing the global epidemic: report of a WHO consultation
World Health Organ Tech Rep Ser
2000
, vol. 
894
 (pg. 
1
-
253
http://whqlibdoc.who.int/trs/WHO_TRS_894.pdf (21 February 2011, date last accessed)
5
National Institute for Health and Clinical Excellence
 
Obesity: schools. NICE 2006; CG43: section 1.1.5 http://guidance.nice.org.uk/CG43 (21 February 2011, date last accessed)
6
Sobal
J
Stunkard
AJ
Socioeconomic status and obesity: a review of the literature
Psychol Bull
1989
, vol. 
105
 (pg. 
260
-
75
)
7
McLaren
L
Socioeconomic status and obesity
Epidemiol Rev
2007
, vol. 
29
 (pg. 
29
-
48
)
8
McLaren
L
Godley
J
MacNairn
IA
Social class, gender, and time use: implications for the social determinants of body weight?
Health Rep
2009
, vol. 
20
 (pg. 
65
-
73
)
9
Rose
G
Sick individuals and sick populations
Int J Epidemiol
1986
, vol. 
14
 (pg. 
32
-
8
)
10
Gonzalez-Suarez
C
Worley
A
Grimmer-Somers
VD
, et al. 
School-based interventions on childhood obesity: a meta-analysis
Am J Prev Med
2009
, vol. 
37
 (pg. 
418
-
27
)
11
Liberati
A
Altman
DG
Tetzlaff
J
, et al. 
The PRISMA statement for reporting systematic reviews and meta-analyses of studies that evaluate healthcare interventions: explanation and elaboration
BMJ
2009
, vol. 
339
 pg. 
b2700
 
12
Angelopoulos
PD
Milionis
HJ
Grammatikaki
E
, et al. 
Changes in BMI and blood pressure after a school based intervention: the CHILDREN study
Eur J Public Health
2009
, vol. 
19
 (pg. 
319
-
25
)
13
Graf
C
Koch
B
Bjarnason-Wehrens
B
, et al. 
Who benefits from intervention in, as opposed to screening of, overweight and obese children?
Cardiol Young
2006
, vol. 
16
 (pg. 
474
-
80
)
14
Graf
C
Koch
B
Falkowski
G
, et al. 
School-based prevention: effects on obesity and physical performance after 4 years
J Sports Sci
2008
, vol. 
26
 (pg. 
987
-
94
)
15
James
J
Thomas
P
Kerr
D
Preventing childhood obesity: two year follow-up results from the Christchurch obesity prevention programme in schools (CHOPPS)
BMJ
2007
, vol. 
335
 
7623
pg. 
762
 
16
Manios
Y
Moschandreas
J
Hatzis
C
, et al. 
Health and nutrition education in primary schools of Crete: changes in chronic disease risk factors following a 6-year intervention programme
Br J Nutr
2002
, vol. 
88
 (pg. 
315
-
24
)
17
Duncan
MJ
Al Nakeeb
Y
Nevill
AM
Effects of a 6-week circuit training intervention on body esteem and body mass index in British primary school children
Body Image
2009
, vol. 
6
 (pg. 
216
-
20
)
18
Haerens
L
Deforche
B
Maes
L
, et al. 
Body mass effects of a physical activity and healthy food intervention in middle schools
Obesity
2006
, vol. 
14
 (pg. 
847
-
54
)
19
Harrison
M
Burns
CF
McGuinness
M
, et al. 
Influence of a health education intervention on physical activity and screen time in primary school children: ‘Switch Off: Get Active
J Sci Med Sport
2006
, vol. 
9
 (pg. 
388
-
94
)
20
Kipping
RR
Payne
C
Lawlor
DA
Randomised controlled trial adapting US school obesity prevention to England
Arch Dis Child
2008
, vol. 
93
 (pg. 
469
-
73
)
21
Kriemler
S
Zahner
L
Schindler
C
, et al. 
Effect of a school based physical activity programme (KISS) on fitness and adiposity in primary schoolchildren: cluster randomised controlled trial
BMJ
2010
, vol. 
340
 pg. 
c785
 
22
Lionis
C
Kafatos
A
Vlachonikolis
J
, et al. 
The effects of a health education intervention program among Cretan adolescents
Prev Med
1991
, vol. 
20
 (pg. 
685
-
99
)
23
Mihas
C
Mariolis
A
Manios
Y
, et al. 
Evaluation of a nutrition intervention in adolescents of an urban area in Greece: short- and long-term effects of the VYRONAS study
Public Health Nutr
2010
, vol. 
13
 (pg. 
712
-
19
)
24
Plachta-Danielzik
S
Pust
S
Asbeck
I
, et al. 
Four-year follow-up of school-based intervention on overweight children: the KOPS study
Obesity
2007
, vol. 
15
 (pg. 
3159
-
69
)
25
Salcedo Aguilar
F
Martinez-Vizcaino
V
Sanchez Lopez
M
, et al. 
Impact of an after-school physical activity program on obesity in children
J Pediatr
2010
, vol. 
157
 (pg. 
36
-
42
)
26
Simon
C
Schweitzer
B
Oujaa
M
, et al. 
Successful overweight prevention in adolescents by increasing physical activity: a 4-year randomized controlled intervention
Int J Obes
2008
, vol. 
32
 (pg. 
1489
-
98
)
27
Singh
AS
Chin
MJM
Brug
J
, et al. 
Dutch obesity intervention in teenagers: effectiveness of a school-based program on body composition and behavior
Arch Pediatr Adolesc Med
2009
, vol. 
163
 (pg. 
309
-
17
)
28
Donnelly
JE
Greene
JL
Gibson
CA
, et al. 
Physical activity across the curriculum (PAAC): a randomized controlled trial to promote physical activity and diminish overweight and obesity in elementary school children
Prev Med
2009
, vol. 
49
 (pg. 
336
-
41
)
29
Barbeau
P
Johnson
MH
Howe
CA
, et al. 
Ten months of exercise improves general and visceral adiposity, bone, and fitness in black girls
Obesity
2007
, vol. 
15
 (pg. 
2077
-
85
)
30
Bayne-Smith
M
Fardy
PS
Azzollini
A
, et al. 
Improvements in heart health behaviors and reduction in coronary artery disease risk factors in urban teenaged girls through a school-based intervention: the PATH program
Am J Public Health
2004
, vol. 
94
 (pg. 
1538
-
43
)
31
Caballero
B
Clay
T
Davis
SM
, et al. 
Pathways: a school-based, randomized controlled trial for the prevention of obesity in American Indian schoolchildren
Am J Clin Nutr
2003
, vol. 
78
 (pg. 
1030
-
8
)
32
Carrel
L
Clark
RR
Peterson
SE
, et al. 
Improvement of fitness, body composition, and insulin sensitivity in overweight children in a school-based exercise program: a randomized, controlled study
Arch Pediatr Adolesc Med
2005
, vol. 
159
 (pg. 
963
-
8
)
33
Dennison
BA
Russo
TJ
Burdick
PA
, et al. 
An intervention to reduce television viewing by preschool children
Arch Pediatr Adolesc Med
2004
, vol. 
158
 (pg. 
170
-
6
)
34
Fitzgibbon
ML
Stolley
MR
Schiffer
L
, et al. 
Hip-hop to health junior for Latino preschool children
Obesity
2006
, vol. 
14
 (pg. 
1616
-
25
)
35
Flores
R
Dance for health: improving fitness in African American and Hispanic adolescents
Public Health Rep
1995
, vol. 
110
 (pg. 
189
-
93
)
36
Foster
GD
Sherman
S
Borradaile
KE
, et al. 
A policy-based school intervention to prevent overweight and obesity
Pediatrics
2008
, vol. 
121
 (pg. 
e794
-
802
)
37
Harrell
JS
McMurray
RG
Bangdiwala
SI
, et al. 
Effects of a school-based intervention to reduce cardiovascular disease risk factors in elementary-school children: the cardiovascular health in children (CHIC) study
J Pediatr
1996
, vol. 
128
 (pg. 
797
-
805
)
38
Johnston
CA
Tyler
C
Fullerton
G
, et al. 
Effects of a school-based weight maintenance program for Mexican-American children: results at 2 years
Obesity
2010
, vol. 
18
 (pg. 
542
-
7
)
39
Matvienko
O
Ahrabi-Fard
I
The effects of a 4-week after-school program on motor skills and fitness of kindergarten and first-grade students
Am J Health Promot
2010
, vol. 
24
 (pg. 
299
-
303
)
40
Melnyk
BM
Small
L
Morrison-Beedy
D
, et al. 
The COPE Healthy Lifestyles TEEN program: feasibility, preliminary efficacy, and lessons learned from an after school group intervention with overweight adolescents
J Pediatr Health Care
2007
, vol. 
21
 (pg. 
315
-
22
)
41
Nader
PR
Stone
EJ
Lytle
LA
, et al. 
Three-year maintenance of improved diet and physical activity: the CATCH cohort. Child and adolescent trial for cardiovascular health
Arch Pediatr Adolesc Med
1999
, vol. 
153
 (pg. 
695
-
704
)
42
Robinson
TN
Reducing children's television viewing to prevent obesity: a randomized controlled trial
JAMA
1999
, vol. 
282
 (pg. 
1561
-
7
)
43
Stock
S
Miranda
C
Evans
S
, et al. 
Healthy buddies: a novel, peer-led health promotion program for the prevention of obesity and eating disorders in children in elementary school
Pediatrics
2007
, vol. 
120
 (pg. 
e1059
-
68
)
44
Yin
Z
Gutin
B
Johnson
MH
, et al. 
An environmental approach to obesity prevention in children: Medical College of Georgia FitKid Project year 1 results
Obes Res
2005
, vol. 
13
 (pg. 
2153
-
61
)
45
Kain
J
Leyton
B
Cerda
R
, et al. 
Two-year controlled effectiveness trial of a school-based intervention to prevent obesity in Chilean children
Public Health Nutr
2009
, vol. 
12
 (pg. 
1451
-
61
)
46
Sichieri
R
Trotte
AP
de Souza
RA
, et al. 
School randomised trial on prevention of excessive weight gain by discouraging students from drinking sodas
Public Health Nutr
2009
, vol. 
12
 (pg. 
197
-
202
)
47
Jiang
J
Xia
X
Greiner
T
, et al. 
The effects of a 3-year obesity intervention in schoolchildren in Beijing
Child Care Health Dev
2007
, vol. 
33
 (pg. 
641
-
6
)
48
Li
YP
Hu
XQ
Schouten
EG
, et al. 
Report on childhood obesity in China (8): effects and sustainability of physical activity intervention on body composition of Chinese youth
Biomed Environ Sci
2010
, vol. 
23
 (pg. 
180
-
7
)
49
Mo-suwan
L
Pongprapai
S
Junjana
C
, et al. 
Effects of a controlled trial of a school-based exercise program on the obesity indexes of preschool children
Am J Clin Nutr
1998
, vol. 
68
 (pg. 
1006
-
11
)
50
Singhal
N
Misra
A
Shah
P
, et al. 
Effects of controlled school-based multi-component model of nutrition and lifestyle interventions on behavior modification, anthropometry and metabolic risk profile of urban Asian Indian adolescents in North India
Eur J Clin Nutr
2010
, vol. 
64
 (pg. 
364
-
73
)
51
Wong
PC
Chia
MY
Tsou
IY
, et al. 
Effects of a 12-week exercise training programme on aerobic fitness, body composition, blood lipids and C-reactive protein in adolescents with obesity
Ann Acad Med Singapore
2008
, vol. 
37
 (pg. 
286
-
93
)
52
Peralta
LR
Jones
RA
Okely
AD
Promoting healthy lifestyles among adolescent boys: the fitness improvement and lifestyle awareness program RCT
Prev Med
2009
, vol. 
48
 (pg. 
537
-
42
)
53
Vandongen
R
Jenner
DA
Thompson
C
, et al. 
A controlled evaluation of a fitness and nutrition intervention program on cardiovascular health in 10- to 12-year-old children
Prev Med
1995
, vol. 
24
 (pg. 
9
-
22
)
54
El Ansari
W
El Ashker
S
Moseley
L
Associations between physical activity and health parameters in adolescent pupils in Egypt
Int J Environ Res Public Health.
2010
, vol. 
7
 (pg. 
1649
-
69
)
55
Lake Snell Perry & Associates
Obesity as a public health issue: a look at solutions
2003
 
www.phsi.harvard.edu/health_reform/poll_results.pdf (21 February 2011, date last accessed)
56
Sharma
M
School-based interventions for childhood and adolescent obesity
Obes Rev
2006
, vol. 
7
 (pg. 
261
-
9
)
57
Budd
GM
Volpe
SL
School-based obesity prevention: research, challenges and recommendations
J Sch Health
2006
, vol. 
76
 (pg. 
485
-
95
)
58
Katz
DL
O'Connell
M
Njike
VY
, et al. 
Strategies for the prevention and control of obesity in the school setting: systematic review and meta-analysis
Int J Obes
2008
, vol. 
32
 (pg. 
1780
-
9
)
59
Nooyens
ACJ
Koppes
LLJ
Visscher
TLS
, et al. 
Adolescent skinfold thickness is a better predictor of high body fatness in adults than is body mass index: the Amsterdam growth and health longitudinal study
Am J Clin Nutr
2007
, vol. 
85
 (pg. 
1533
-
9
)

Appendix: PRISMA flowchart of study selection in the systematic review

graphic