the effect of physical activity interventions on children

10
REVIEW The Effect of Physical Activity Interventions on Childrens Cognition and Metacognition: A Systematic Review and Meta-Analysis Celia Alvarez-Bueno, MSc, Caterina Pesce, PhD, Iv an Cavero-Redondo, MSc, Mairena S anchez-L opez, PhD, Jos e Alberto Mart ınez-Hortelano, MSc, Vicente Mart ınez-Vizca ıno, MD Objective: The objective was twofold: to assess the effect of physical activity (PA) interventions on childrens and adolescentscognition and metacognition; and to deter- mine the characteristics of individuals and PA programs that enhance the development of cognitive and meta- cognitive functions. Method: We systematically searched MEDLINE, EMBASE, Cochrane Central Register of Controlled Trials, Web of Science, and PsycINFO databases from their inception to October 16, 2016. Intervention studies aimed at examining the exercisecognition interaction at a developmental age were included in this systematic re- view and meta-analysis. Random-effects models were used to calculate pooled effect size (ES) values and their corresponding 95% CIs. Subgroup analyses were con- ducted to examine the effect of participantsand PA pro- gramscharacteristics. Results: A total of 36 studies were included in this systematic review and meta-analysis. Pooled ES estimations were as follows: nonexecutive cognitive functions 0.23 (95% CI ¼ 0.090.37); core executive functions 0.20 (95% CI ¼ 0.100.30), including working memory (0.14 [95% CI ¼ 0.000.27]), selective atten- tioninhibition (0.26 [95% CI ¼ 0.100.41]), and cognitive exibility (0.11 [95% CI ¼0.10 to 0.32]); and metacognition 0.23 (95% CI ¼ 0.130.32), including higher-level executive functions (0.19 [95% CI ¼ 0.060.31]) and cognitive life skills (0.30 [95% CI ¼ 0.150.45]). Conclusion: PA benets several domains of cognition and metacognition in youth. Curricular physical educa- tion interventions and programs aimed at increasing daily PA seem to be the most effective. Key words: cognition, metacognition, physical activity, exercise J Am Acad Child Adolesc Psychiatry 2017;56(9):729738. T he relationship between physical activity (PA) and exercise with cognitive function (e.g., information processing, memory, attention) in children and adolescents has seen a growing interest during the past two decades. 1,2 Both PA, as any bodily movement produced by skeletal muscles through energy expenditure, and exercise, understood as repetitive, structured, and planned physical activity aimed to maintain or improve physical tness or health, have been related to cognitive function. 3 Evidence consistently supports that PA has a positive impact on cognitive function through several mechanisms, including angiogenesis, oxygen saturation, glucose delivery, cerebral blood ow, and neurotransmitter levels, 4 structural changes in brain volumes, 5 and improvement of brain functioning. 6 Furthermore, in exercise and cognition research, a joint neurocognitive and social-cognitive approach has been proposed 7 to highlight relevant intersections between higher-level executive functions and life skills, including creativity, decision making, and goal setting, which are essential for healthy child development. 8-10 Beyond the neurobiological, social, and cognitive in- uences of exercise, focus has recently been extended to examine the characteristics of PA interventions 1,11,12 that could result in greater benets in cognitive function because of their inherent cognitive and motor demands. 13 Thus, currently, a challenge is to identify the characteristics of PA interventions that are most efcient for promoting cognitive development, and also the pathways through which these inuences are transmitted. 6,14 Recent research has shown that PA interventions that jointly involve physical effort and emotional and social engagement challenge core cognitive functions, 15,16 as well as cognitive life skills, such as goal setting, problem solving, and self-regulation, a life skill relying on the efciency of a core executive function such as inhibition. 9,11,17-20 Several pathways behind the relationship between PA and cognitive domains have been suggested, including the hypothesis that PA inuences executive func- tion by stimulating motor tness or increasing the complexity of the PA programs in terms of creativity, diversity, and successfulness. 21,22 Previous systematic reviews and meta-analyses have shown the effectiveness of PA interventions on improving childrens and adolescentscognition. These reviews were Supplemental material cited in this article is available online. JOURNAL OF THE AMERICAN ACADEMY OF CHILD & ADOLESCENT PSYCHIATRY VOLUME 56 NUMBER 9 SEPTEMBER 2017 www.jaacap.org 729

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REVIEW

JOURNAL

VOLUM

The Effect of Physical Activity Interventions onChildren’s Cognition and Metacognition:A Systematic Review and Meta-AnalysisCelia �Alvarez-Bueno, MSc, Caterina Pesce, PhD, Iv�an Cavero-Redondo, MSc,

Mairena S�anchez-L�opez, PhD, Jos�e AlbertoMart�ınez-Hortelano, MSc, Vicente Mart�ınez-Vizca�ıno, MD

Objective: The objective was twofold: to assess the effectof physical activity (PA) interventions on children’s andadolescents’ cognition and metacognition; and to deter-mine the characteristics of individuals and PA programsthat enhance the development of cognitive and meta-cognitive functions.

Method: We systematically searched MEDLINE,EMBASE, Cochrane Central Register of Controlled Trials,Web of Science, and PsycINFO databases from theirinception to October 16, 2016. Intervention studies aimedat examining the exercise–cognition interaction at adevelopmental age were included in this systematic re-view and meta-analysis. Random-effects models wereused to calculate pooled effect size (ES) values and theircorresponding 95% CIs. Subgroup analyses were con-ducted to examine the effect of participants’ and PA pro-grams’ characteristics.

Results: A total of 36 studies were included in thissystematic review and meta-analysis. Pooled ES

Supplemental material cited in this article is available online.

OF THE AMERICAN ACADEMY OF CHILD & ADOLESCENT PSYCHIATRY

E 56 NUMBER 9 SEPTEMBER 2017

estimations were as follows: nonexecutive cognitivefunctions 0.23 (95% CI ¼ 0.09�0.37); core executivefunctions 0.20 (95% CI ¼ 0.10�0.30), including workingmemory (0.14 [95% CI ¼ 0.00�0.27]), selective atten-tion�inhibition (0.26 [95% CI ¼ 0.10�0.41]), andcognitive flexibility (0.11 [95% CI ¼ �0.10 to 0.32]);and metacognition 0.23 (95% CI ¼ 0.13�0.32),including higher-level executive functions (0.19 [95%CI ¼ 0.06�0.31]) and cognitive life skills (0.30 [95%CI ¼ 0.15�0.45]).

Conclusion: PA benefits several domains of cognitionand metacognition in youth. Curricular physical educa-tion interventions and programs aimed at increasing dailyPA seem to be the most effective.

Key words: cognition, metacognition, physical activity,exercise

J Am Acad Child Adolesc Psychiatry 2017;56(9):729–738.

he relationship between physical activity (PA) andexercise with cognitive function (e.g., information

T processing, memory, attention) in children and

adolescents has seen a growing interest during the past twodecades.1,2 Both PA, as any bodily movement producedby skeletal muscles through energy expenditure, andexercise, understood as repetitive, structured, and plannedphysical activity aimed to maintain or improve physicalfitness or health, have been related to cognitive function.3

Evidence consistently supports that PA has a positiveimpact on cognitive function through several mechanisms,including angiogenesis, oxygen saturation, glucose delivery,cerebral blood flow, and neurotransmitter levels,4 structuralchanges in brain volumes,5 and improvement of brainfunctioning.6 Furthermore, in exercise and cognitionresearch, a joint neurocognitive and social-cognitiveapproach has been proposed7 to highlight relevantintersections between higher-level executive functionsand life skills, including creativity, decision making, and

goal setting, which are essential for healthy childdevelopment.8-10

Beyond the neurobiological, social, and cognitive in-fluences of exercise, focus has recently been extended toexamine the characteristics of PA interventions1,11,12 thatcould result in greater benefits in cognitive function becauseof their inherent cognitive and motor demands.13 Thus,currently, a challenge is to identify the characteristics of PAinterventions that are most efficient for promoting cognitivedevelopment, and also the pathways through which theseinfluences are transmitted.6,14 Recent research has shownthat PA interventions that jointly involve physical effort andemotional and social engagement challenge core cognitivefunctions,15,16 as well as cognitive life skills, such as goalsetting, problem solving, and self-regulation, a life skillrelying on the efficiency of a core executive function such asinhibition.9,11,17-20 Several pathways behind the relationshipbetween PA and cognitive domains have been suggested,including the hypothesis that PA influences executive func-tion by stimulating motor fitness or increasing thecomplexity of the PA programs in terms of creativity,diversity, and successfulness.21,22

Previous systematic reviews and meta-analyses haveshown the effectiveness of PA interventions on improvingchildren’s and adolescents’ cognition. These reviews were

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�ALVAREZ-BUENO et al.

mainly focused on describing the characteristics of in-terventions in terms of intensity, frequency, and session orintervention duration.2,23-27 Two previous meta-analyseshave examined the role of the qualitative characteristics ofPA interventions in the relationship between exercise andchildren’s cognition,12,26 although they did not distinguishbetween the cognitive outcomes that improved and thosethat did not.

To our knowledge, no review has evaluated the inde-pendent PA effects on each core cognitive executive function(inhibition, working memory, and cognitive flexibility) andmetacognition, extending the later construct to encompass aneuroscience perspective on higher-level executive func-tions28 and a social-cognitive perspective on cognitive lifeskills.17,29 Tomporowski et al.30 proposed that the benefits ofquantitatively and/or qualitatively different PA in-terventions in multiple cognitive subdomains might beinterrelated through mediation chains that link increasedexecutive function to improvements in metacognition andacademic achievement.30 However, current mediation evi-dence is only cross-sectional in nature and has not yetaddressed the potential role of metacognition,31,32 that is, theability to supervise and manage cognitive processes and touse knowledge to regulate behaviors,30 and distinguish itfrom cognition, which is understood as the set of mentalprocesses that contribute to perception, memory, intellect,and action.2 In sum, scientific evidence on the relationshipbetween PA and cognitive performance in childhood andadolescence, particularly with regard to possible moderatorsand mediating mechanisms, is clearly insufficient to explainhow and why PA may have an impact on academicachievement.

Thus, the aims of this systematic review and meta-analysis were: to assess the effect of PA interventions onchildren’s and adolescents’ cognition, distinguishing be-tween core executive functions and metacognition; and todetermine which individual and joint PA program charac-teristics are most favorable to aid the development ofcognitive and metacognitive functions.

METHODThis systematic review and meta-analysis was guided by thePreferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) Statement33 and the Cochrane CollaborationHandbook.34 The protocol for this systematic review and meta-analysis was registered on PROSPERO (CRD42015029913) and ispublished elsewhere.35

Search StrategyA literature search was independently performed by two reviewers(C.A. and C.P.), and studies were identified through a combinationof resources. First, a systematic search was performed in MEDLINE,EMBASE, Cochrane Central Register of Controlled Trials, CochraneDatabase of Systematic Reviews, Web of Science, and PsycINFOdatabases from their inception to October 16, 2016. The searchstrategy combined the following relevant terms: “physical activity,”“physical education,” “exercise,” “fitness,” and “sport”; “cognition,”“executive,” “executive function,” “cognitive control,” “intelli-gence,” “memory,” “attention,” and “metacognition”; “life skills,”

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“goal setting,” “problem solving,” and “self-regulation”; “braindevelopment,” “brain health,” “neural,” “neuroelectric,” “neuro-trophic,” “neurotrophin,” and “hormone”; “children,” “childhood,”“pre-schooler,” “schoolchildren,” “preadolescent,” “adolescent,”and “adolescence” and “trial” and “effect*.” Second, the referencelists of the included articles in this review, and the list of thoseincluded in previous systematic reviews and meta-analyses, werereviewed for any additional relevant study.

EligibilityStudies concerning the relationship between PA interventions andchildren’s and adolescents’ cognition were included in the meta-analysis. Inclusion criteria were as follows. Regarding partici-pants, studies included healthy children from 4 to 18 years of age(whose target population was not preterm children or with disor-ders that could limit the generalization of the data). Regardingintervention characteristics, studies included PA programs aimedat enhancing (referring to an increased amount of time devoted toPA) or enriching (referring to a deliberate increase in nonphysical,that is, coordinative and/or cognitive, demands of PA tasks) PAsessions. We classified the interventions into school-time and afterschool-time PA. Among the former, we distinguished thefollowing: curricular physical education, integrated PA (activebreaks or teaching subjects such as mathematics with physicallyactive tasks), and extracurricular PA (active recess or lunch timePA); the latter included after-school PA or sports programs.Regarding outcomes, studies included cognitive performance as-sessments of nonexecutive cognitive functions, core executivefunctions, and/or metacognition. Finally, regarding study design,studies included randomized controlled trials (RCTs), non-RCTs,and controlled pre�post studies.

Studies were excluded when they met the following exclusioncriteria: included an adult population; were based on the acutemeasurement of the effect of PA on cognition (i.e., thosemeasuring cognition during or immediately after the exertion ofsingle bouts of physical activity); included children with anyphysical or mental disorders that could impede or limit theirparticipation in the intervention program activities; and were notpublished in English or Spanish.

Search and Data ExtractionTwo researchers (C.A. and C.P.) independently screened all ab-stracts of the retrieved articles, excluding those studies that did notmeet eligibility criteria. The full texts of selected studies wereretrieved, and the same two authors independently collected thefollowing data of each study meeting the previously defined criteria:year of publication, country of the study, number of participants (incontrol and intervention groups), age of participants, control con-dition and PA intervention(s) duration, school time when PA in-terventions took place and task characteristics of the intervention,intervention design, length of intervention in weeks, and mainoutcomes and instruments for their measurement (Tables S1 and S2,available online). The authors of the included studies were contactedwhen a lack of information was detected. Disagreements in datacollection were settled by consensus. Cohen’s36 k was used to assessagreement between reviewers.

Studies were classified into three groups according to theirmeasured outcomes: nonexecutive cognitive functions; core execu-tive functions including: working memory, cognitive flexibility, andinhibition, with the latter including response inhibition and inter-ference control for selective attention28; and metacognition,including higher-level executive functions (planning, fluid

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intelligence–abstract reasoning, and problem solving)28 and cogni-tive life skills.7,30

Quality AssessmentAfter concealing information about authors, affiliations, date andsource of each manuscript, two investigators (C.A. and I.C.) inde-pendently assessed their methodological quality. Disagreementswere solved by consensus.

The Jadad scale37 was used to assess the methodological qualityof RCTs. The scale included the evaluation of three domains:randomization, double blinding, and description of withdrawalsand dropouts. Each item could be scored as “1” or “0” if the studydid or did not satisfy it. Randomization and double blinding couldscore one extra point if they were described in detail. Based on this,each study could score between 0 and 5.

The Effective Public Health Practice Project (EPHPP) QualityAssessment Tool for Quantitative Studies38 was used to assess thequality of non-RCTs and controlled pre–post studies. Studies wereevaluated in seven domains: selection bias, study design, con-founders, blinding, data collection method, and withdrawals anddrop-outs. Each domain could be scored as strong, moderate, orweak, and studies could be classified as strong (with no weak do-mains), moderate (with one weak domain), or weak (with two ormore weak domains).

Statistical AnalysisDetailed statistical procedures used in this meta-analysis havebeen reported elsewhere.35 A standardized mean difference scorewas calculated for each specific variable using Cohen’s d index,39

in which positive ES values indicate higher scores in outcomes infavor of the intervention group. The pooled ES was estimatedusing a random-effects model based on the Der Simonian andLaird method. Heterogeneity across studies was assessed usingthe I2 statistic. Values of <25%, 25% to 50%, and >50% areconsidered to represent small, medium, and large amounts ofinconsistency, respectively. The influence of each study in thepooled ES estimates was examined using sensitivity analyses. Forassessing publication bias, the Egger regression asymmetry test40

was used. The trim-and-fill41 computation was used to assess theeffect of publication bias on the interpretation of results. Onlythose studies providing complete data for pre- and post-intervention measurements and including a control group wereincluded in the meta-analysis.

Some additional statistical aspects that should be detailed herewere as follows. First, when studies included two cohorts or twointervention groups, their data were analyzed as independentsamples. Second, when studies used two or more tests for measuringthe same variable, the average effect size was calculated. Third,when studies reported two or more follow-up measurements, onlythe last measurement was considered. Finally, an interferenceoutcome for a Stroop-like test or Flanker-like test was calculated asfollows: incongruent test�congruent test or commissiontest�omission test.

A pooled ES was calculated for the following three groups ofcognitive domains: nonexecutive cognitive functions; core executivefunctions; and metacognition. In addition, subgroup analyses wereconducted considering individual tasks within each domain: coreexecutive function (working memory, cognitive flexibility, and se-lective attention�inhibition [for the last, an additional analysis wasconducted by considering selective attention and inhibition mea-surements separately]); and metacognition (higher-level executivefunctions [including planning, fluid intelligence, e.g., reasoning and

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problem solving, and creativity] and cognitive life skills [includingself-awareness of goal setting, problem solving, and positivethinking skills]).

Subgroup analyses were performed based on different aspectsof the intervention: the school time when PA intervention tookplace, distinguishing between curricular physical education, inte-grated or extracurricular PA, and after-school PA and sportsprograms; and task characteristics, distinguishing between quan-titative and qualitative characteristics of the PA intervention,considering whether the interventions were designed as enhancedor enriched PA. Interventions could be both enhanced andenriched when the manipulation included additional physicallyactive times, and deliberately increased coordinative and cognitivetask requirements.

Other subgroup analyses were performed based on some vari-ables that could act as confounders: children’s weight status,comparing the effectiveness of studies considering when studiesprovided the effectiveness of the interventions on overweight andobese children; and time and accuracy of cognitive test performance,considering the papers that reported the effect of the intervention onaccuracy, time, or both separately.

In addition, random-effects meta-regression analyses were per-formed to determine whether the children’s age (in years), the lengthof the intervention (in weeks), and the study quality could be relatedwith the effectiveness of the intervention on each outcome.

Statistical analyses were performed using StataSE software,version 14 (StataCorp, College Station, TX).

RESULTSThe search retrieved a total of 4,582 articles. Of those, 777were removed as duplicates, and 3,805 were screened basedon the title and the abstract (Figure S1, available online). Theoverall percentage of agreement between the reviewers ondata extraction, as assessed using Cohen’s k statistic,was 0.91.

A total of 36 papers were included in this systematic re-view,6,9,10,19,20,42-72 of which only five were non-RCT de-signs.42,44,59,64,66 Characteristics of the included studies aredisplayed in Table S1 (available online). Studies were con-ducted in 15 countries: United States (10 studies), India (5),Italy (5), Australia (2), Germany (2), Greece (2), theNetherlands (2), Denmark (1), Iran (1), South Africa (1),Spain (1), Switzerland (1), Taiwan (1), Turkey (1), and theUnited Kingdom (1). The total sample included 5,527 chil-dren and adolescents (2,308 in control group), who were 4 to14 years of age. Three studies included only overweight andobese children,48,49,57 and three studies addressed themoderating role of children’s weight status.10,47,53

The interventions, which were mostly performedduring curricular school time, were aimed at increasingthe amount of PA or qualitatively enrichingPA,9,10,19,20,43,46,47,51,53,54,61,62,64-67,69 and at adding classroom-based PA during daily lessons targeted to learning varioussubjects through being physically active (integratedPA),50,60,63,68 unrelated to subject learning (activebreaks),52,71 or PA during recess (e.g., active lunch).70

Furthermore, several studies developed after-school PAprograms,6,42,44,45,48,49,55-57,72 two of them during summercamp.58,59

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Overall, the interventions resulted in an increase in PAtime from 15 to 120 minutes per day, except one interventionstudy that included 480 minutes per day, 7 days per week,but was limited to the time of summer camp vacations.59

Only three studies included data from two cohorts,9,64,66

and 14 studies included more than one intervention group,four of them without a control group.45,46,58,69 For thosestudies with more than one intervention group, experi-mental groups differed in exercise intensity,43,45,48,49,65

duration,48,49 PA type,46,52,53,56,58-61,65,69 or educators whodelivered the intervention activities (generalist versusspecialist teachers).61 The length of interventions rangedbroadly from 4 weeks9,58,60,71 to 54 weeks.54

Systematic ReviewTable S2 (available online) describes the relevant character-istics of the included studies. Seven studies10,43,48,49,51,52,71

reported information regarding the efficacy of PA in-terventions on cognitive domains that do not or only mini-mally rely on executive function. In all of them, nonexecutivefunctions improved as a result of the intervention. Four ofthose studies included two experimental groups thatdiffered in exercise intensity,43,48,49 duration,48 or PA type,52

and yielded controversial results. Two studies48,49 did notfind dose�response relationships; however, two otherstudies43,52 found that increases in the duration and intensityof the sessions was associated with greater improvements innonexecutive functions.

A total of 29 studies6,10,19,20,42,44-51,53-57,59-62,65-70,72 re-ported improvements in core executive functions. Elevenstudies included more than one intervention group: threedid not find differences between intervention groups,46,48,49

and the remaining eight studies reported differences infavor of aerobic exercise,56 yoga,59 coordinative or cogni-tively enriched PA carried out by specialists,53,61 integratedPA,60,69 or team games65 or the moderate intensity group.45

The 15 studies9,10,19,43,46,48,49,51,52,58,61,63,64,67,70 in whichmetacognition was an outcome reported postinterventionimprovements in its domains. Studies including more thanone intervention group43,46,48,49,52,58 failed to find significantdifferences in improvements.

Study QualityOf the 31 RCTs in which quality was assessed usingthe Jadad scale, only two scored five points,6,51 sixscored four points,43,46,49,10,67,69 13 scored threepoints,19,47,48,50,53,57,61-63,65,68,70,71 nine scored twopoints,18,20,45,52,54-56,60,72 and one scored one point.58 All of thestudies included information regarding the randomizationmethod, and only two did not provide information about thewithdrawals and dropouts. However, only four studiesproperly described the double-blinding method used(Table S3, available online).

Of the five non-RCTs in which quality was assessed usingthe EPHPP tool, four42,44,59,66 scored as weak and one asmoderate.64 The worst-scored items were the following: datacollection, because the tools for primary outcomes were notdescribed as reliable and valid; and the descriptions of the

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withdrawals and drop-outs, because the papers did notdescribe the number and/or the reasons for the withdrawalsand drop-outs (Table S3, available online).

Meta-AnalysisNonexecutive Cognitive Functions. The pooled ES estimationfor PA intervention effects on cognitive performances not, oronly minimally, relying on executive functions was 0.23(95% CI ¼ 0.09�0.37). There was small heterogeneity amongthe studies (I2 ¼ 21.9%; p ¼ .199) (Figure 1A).

Core Executive Functions. For core executive functions(including performance on selective attention tests requiringexecutive interference control), the pooled ES estimation was0.20 (95% CI ¼ 0.10�0.30). There was large heterogeneitybetween the studies (I2 ¼ 70.0%; p < .001) (Figure 1B).

Data for the working memory subgroup analysis showeda pooled ES of 0.14 (95% CI ¼ 0.00�0.27). There was me-dium heterogeneity among the studies (I2 ¼ 48.0%; p ¼ .027).

The pooled ES for selective attention�inhibition sub-group analysis, including the outcomes of selective attentiontests requiring executive interference control, was 0.26 (95%CI ¼ 0.10�0.41). There was large heterogeneity among thestudies (I2 ¼ 76.0%, p < .001). When a complementaryanalysis was performed for measures of inhibition processand selective attention separately, the pooled ESs were 0.38(95% CI ¼ 0.13�0.63) and 0.13 (95% CI ¼ �0.07 to 0.33),respectively. There was large heterogeneity in both groupsof studies (I2 ¼ 86.2% and 66.8%, respectively).

Finally, for the cognitive flexibility subgroup, the pooledES was 0.11 (95% CI ¼ �0.10 to 0.32), with large heteroge-neity across studies (I2 ¼ 68.7%; p ¼ .013).

Metacognition. The pooled ES for PA programs on meta-cognition was 0.23 (95% CI ¼ 0.13�0.32), with small het-erogeneity between studies (I2 ¼ 4.7%; p ¼ .398) (Figure 1C).

The pooled ES for the subgroup of higher-level executivefunctions was 0.19 (95% CI ¼ 0.06�0.31), and heterogeneitywas small (I2 ¼ 12.9%; p ¼ .315).

For cognitive life skills, the pooled ES estimation was 0.30(95% CI ¼ 0.15�0.45) with no heterogeneity among thestudies (I2 ¼ 0.0%, p ¼ .549).

Subgroup Analysis. Subgroup analysis by the school timewhen PA interventions took place (curricular physical edu-cation, integrated or extracurricular PA, and after-school PA)showed that curricular physical education programs broadlybenefited the following: nonexecutive cognitive functions(ES ¼ 0.42; 95% CI ¼ 0.14�0.70); the selective atten-tion�inhibition component of core executive functions (ES ¼0.41; 95% CI ¼ 0.15�0.67); and higher-level executive func-tions (ES ¼ 0.25; 95% CI ¼ 0.06�0.43). On the other hand, noPA intervention influenced working memory or cognitiveflexibility. This subgroup comparison could not be per-formed for cognitive life skills, which were measured only incurricular physical education programs (ES ¼ 0.30; 95% CI ¼0.15�0.45) (Table S4, available online).

Subgroup analysis based on task characteristics of theintervention (quantitatively enhanced PA, qualitativelyenriched PA, or both) (Table S4, available online) showedthat nonexecutive cognitive functions were improved mostly

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FIGURE 1 Pooled estimated effect size for nonexecutive cognitive functions (a), core executive functions (b), and metacognition (c).Note: Positive effect size (ES) values indicate higher score in outcomes in favor of the intervention group. BART ¼ Ballon AnalogueRisk Task; CANTAB ¼ Cambridge Neuropsychological Test Battery; CAS ¼ Cognitive Assessment System; IGF-M ¼ SpanishOverall and Factorial Intelligence Test; M-WCST ¼ modified version of Wisconsin Card Sorting Test; RFFT ¼ Ruff Figural FluencyTest; RNG ¼ random number generation; WISC ¼ Wechsler Intelligence Scale for Children.

PHYSICAL ACTIVITY INTERVENTIONS AND CHILDREN’S COGNITION

in enhanced PA programs (ES ¼ 0.21; 95% CI ¼ 0.07�0.35).With regard to core executive functions, working memorybenefited mostly from enhanced PA programs (ES ¼ 0.28;95% CI ¼ 0.04�0.52), whereas selective attention�inhibitionbenefited mostly from enriched PA programs (ES ¼ 0.49;95% CI ¼ 0.05�0.93), and cognitive flexibility did not benefitfrom any type of intervention. Finally, higher-level executivefunctions improved through enhanced PA (ES ¼ 0.21; 95%CI ¼ 0.09�0.34), whereas cognitive life skills were evaluatedonly in enriched PA (ES ¼ 0.30; 95% CI ¼ 0.15�0.45).

Subgroup analysis by children’s weight status could beperformed only for the selective attention�inhibition sub-domain. Six overweight and/or obese children comparisongroups were extracted from four studies.47-49,57 The pooledES estimation when considering only overweight and/orobese children was �0.02 (95% CI ¼ �0.22 to 0.17).

When subgroup analyses were conducted based on theindividual and joint effects on cognitive performance timeand accuracy, only inhibition and cognitive flexibility couldbe considered (Table S5, available online). The pooled ES for

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studies focused on accuracy outcomes was 0.15 (95%CI¼ 0.01�0.29), for those focused on performance time (i.e.,reaction time, or time to test completion) �0.25 (95%CI ¼ �0.45 to �0.04), and for those including both accuracyand performance time, the pooled ES for accuracy was 0.29(95% CI ¼ 0.04�0.54), whereas the pooled ES for timewas �0.05 (95% CI ¼ �0.20 to 0.11).

Random-EffectsMeta-RegressionModel. The random-effectsmeta-regression model showed that the effect of PAinterventions on children’s nonexecutive functions waspositively associated with children’s age (b ¼ 0.08; 95%CI ¼ 0.00�0.15; p ¼ .036) and on children’s working memorywas negatively associated with length of intervention(b ¼ �0.01; 95% CI ¼ �0.02 to �0.01; p ¼ .023) (Table S6,available online).

Moreover, this model showed that study quality was alsonot related to the heterogeneity observed across the studies.

Sensitivity Analyses. Sensitivity analyses suggested thatthe pooled ES estimation for working memory was modifiedonly when removing studies by Fisher et al.,51 Kamijo et al.,55

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FIGURE 1 (continued).

�ALVAREZ-BUENO et al.

Manjunath et al.,59 and Mavilidi et al.60 (Table S7, availableonline).

Publication Bias. Funnel plots indicated significant publi-cation bias for the pooled subgroup analyses of workingmemory only (p < .10) (Figure S2, available online). Inaddition, trim-and-fill computation showed that six studieswere needed for removing publication bias from workingmemory subgroup (p ¼ .628).

DISCUSSIONTo our knowledge, this is the first systematic review andmeta-analysis that separately summarizes evidenceregarding the effectiveness of PA interventions on children’sand adolescents’ nonexecutive cognitive functions, core ex-ecutive functions, and metacognition. Overall, this review

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shows that PA programs benefit multiple facets of nonex-ecutive (ES ¼ 0.23), executive (ES ¼ 0.20), and metacognitive(ES ¼ 0.23) functions and skills in children and adolescents.In addition, our data showed that curricular physical edu-cation and programs aimed at increasing the amount ofexercise seem to be the most effective.

Subgroup analyses showed that the domains of cognitionmost sensitive to exercise were working memory (ES ¼ 0.14),inhibition (ES ¼ 0.26), higher-level executive functions (ES ¼0.19), and cognitive life skills (ES ¼ 0.30). However, indi-vidual and task characteristics, as well as the school timewhen the PA interventions took place, have some influenceon these effects. Participants’ age seems to uniquely act as anamplifier of the size of intervention effects in nonexecutivefunctions. With regard to the context in which PA in-terventions were conducted, curricular physical education

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FIGURE 1 (continued).

PHYSICAL ACTIVITY INTERVENTIONS AND CHILDREN’S COGNITION

lessons seem to be the most appropriate framework toimprove children’s cognition. The influence of the nature ofactivities included in the PA programs seems to be greateron core and higher-level executive functions. Althoughincreasing the amount of PA appears to improve children’sworking memory and higher-level executive functions,enriched PA programs with flexible cognitive-oriented tasksimplying greater coordinative and cognitive demands seemto particularly improve inhibitory efficiency.

Developmental evidence concerning the beneficial effectsof PA interventions on cognition has been growing duringthe last decades. However, not all exercise produces thesame results, in such a way that animal studies have shownthat complex and random activities result in greater neuralgrowth in the hippocampus, cerebellum, and cerebralcortices than simple and repetitive actions.73 Thus, at pre-sent, evidence consistently supports that not all forms ofexercise influence cognition equally,4,11,21 and that exercisesrequiring complex, controlled, and adaptive cognition andmovement have a greater impact on executive functions.13

Our analyses also showed that classroom-based PA didnot have a positive impact on children’s cognition,23 at leastwhen evidence on this in-school intervention type wasmerged with other noncurricular types of school-time PA

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(e.g., recess-time PA), and as compared with the greaterimpact of curricular physical education.

Previous research has reported an association betweenworking memory and cardiorespiratory and muscularfitness levels, and also between inhibition processes andsome components of enriched PA games such as decision-making or tactical cooperation.22 Although most of the ac-tivities included in the PA interventions were not deliber-ately designed to involve coordinative and cognitivedemands, the interventions often included a variety of ac-tivities that did not emphasize task repetition; rather, theyimplied a progressive increase in task complexity, ensuring acognitive effort that might help cognitive development.21,74

In this meta-analysis, we classified as “enriched” onlythose PA interventions in which the coordinative andcognitive demands were deliberately manipulated. Suchkinds of deliberate cognitive enrichment of exercise pro-grams seem to be useful for promoting the development ofinhibitory functions, which plays a crucial role in theachievement of academic goals and life skills that areessential to positive youth development.75,76

In addition, our meta-analysis shows that when speedand accuracy in tasks tapping core executive functions areconsidered, only accuracy is improved by PA interventions.

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�ALVAREZ-BUENO et al.

Behind this finding could be the fact that children are notable to independently control their speed and accuracy inresponse to an impulse, but they could be able to control thespeed–accuracy trade-offs77; therefore, the sensory perfor-mance (accuracy) could be improved without improving themotoric stage (reaction time).

There has been a growing concern about the world-wide alarming increase in overweight and obesity prev-alence rates in children. Physical inactivity and changes ineating habits have been identified as key factors for thisdramatic change in children’s body composition. Evi-dence suggests a negative complex relationship betweenweight status and motor and cognitive development,78,79

although changes in the anatomy and function of thebrain of overweight and obese children have also beenhighlighted.79 Mediation analyses suggest that motordevelopment mediates the relationship between weightstatus and cognitive performance,14 and therefore it seemsimportant to elucidate whether it would be expected thatoverweight and/or obese children involved in PA pro-grams reap greater benefits in terms of cognitive devel-opment and academic achievement than their normal-weight peers. Our results did not show a significantlyhigher ES in overweight and/or obese children in theintervention groups than the overweight and/or obesechildren in the control groups. Nevertheless, these resultsshould be considered with caution, because most of thestudies did not provide effect data by weight status, andonly six presented separate data for overweight and/orobese children.

The main point of our findings is that they consistentlysupport that curricular PA programs seem to be the mosteffective interventions for promoting the development ofa broad range of cognitive and metacognitive functionsand skills. Therefore, increasing physical educationcurricular time does not negatively affect but alsoeven promotes cognitive development and academicachievement.1,2,23,63 Moreover, it should be taken intoaccount that although this review has exclusively focusedon school-based structured PA interventions, the benefitson health and cognition of any of these programs wouldpresumably be extended far beyond the school. Thus,scientific evidence on the effectiveness of interventionsthat jointly include motor and cognitive stimulation inschool-based activities, along with that on the promo-tion of complementary outdoor free-play experiences, isnecessary to amplify the benefits of school-based enrichedPA programs.62

Nevertheless, it should also be noted that there is a lack ofinformation regarding school-based interventions design;therefore, studies should describe in more detail the meth-odologies, cognitive variables involved in the interventions,and the compliance and acceptability of the programs inorder to make definitive conclusions regarding their effec-tiveness.12 Furthermore, considering the importance of earlybrain development processes in the acquisition of core ex-ecutive functions, metacognition, and life skills later in lifeand their relation to academic achievement, it seems essen-tial to gather information regarding the maintenance of the

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beneficial effects of PA interventions on children’s and ad-olescents’ cognition over time, after intervention cessation.We have not been able to state how long the benefits ofschool-based PA programs could be maintained over time,as there is a lack of follow-up studies measuring outcomesafter intervention cessation.50,61

The design of PA and motor learning interventions forchildren and adolescents with contents and delivery strate-gies tailored to specifically enhance their executive functionis emerging as a promising way to promote motor andcognitive development.14,80,81 However, well-designed PAprograms joining motor and cognitive stimulation should becomplemented with the great variety of outdoor free-playexperiences that seem to amplify the benefits of school-based enriched PE programs.62

The limitations of this study are those common tosystematic reviews and meta-analyses. In addition, weshould highlight the following aspects that could limitthe robustness of our results. First, we found sig-nificant publication bias only for working memory;however, we cannot affirm that publication bias did notaffect other variables due to poor results being unpub-lished because we did not search for unpublished studiesor include grey literature. Second, the results of thismeta-analysis were obtained after some data manipula-tion, which could generate some bias. Third, less than50% of the studies included in the systematic reviewscored as good quality; conversely, meta-regressionmodels showed that study quality was not related toheterogeneity among studies. Fourth, cognitive perfor-mance was measured across the studies using a widevariety of tools, but measurements were standardized bycalculating the ES. Finally, participants’ age and thelength or type of interventions could influence our esti-mations; thus, subgroup analysis and meta-regressionswere performed to minimize this possible source of biasand heterogeneity.

In conclusion, this systematic review and meta-analysissupports that PA interventions are useful strategies tofoster the development of children’s cognition (nonexecu-tive cognitive functions, core executive functions, andhigher-level executive functions). Moreover, this studyshows that curricular exercise and programs aimed atincreasing the time dedicated to PA are more likely toproduce an effect on children’s and adolescents’ cognition.This information should be jointly considered with previ-ous research that has highlighted the positive effects ofphysical activity on children’s health.82,83 It also might berelevant for policy and decision makers in order to designnew strategies not only for promoting children’s cognitivedevelopment, and, as a consequence, better academic per-formance, but also for improving mental health (reducinganxiety/depressive disorders, improving self-esteem)82

and preventing cardiovascular disease.84 Including thisevidence in good practice guidelines in educationand public health might lead to counteracting thecurrent school trend of PA reduction. For this purpose,qualified professionals71 are essential in designing PAstrategies tailored to enhance children’s and adolescents’

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PHYSICAL ACTIVITY INTERVENTIONS AND CHILDREN’S COGNITION

executive functions, and thereby motor and cognitivedevelopment promotion.14,80,81 Future reviews shouldaddress the efficacy, for children’s cognitive development,of environment-based programs tailored to create favor-able surroundings for playground games and PA. &

Accepted June 29, 2017.

Mrs. �Alvarez-Bueno, Mr. Cavero-Redondo, Dr. S�anchez-L�opez, Mr. Mart�ınez-Hortelano, and Dr. Mart�ınez-Vizca�ıno are with Universidad de Castilla-LaMancha, Health and Social Research Center, Cuenca, Spain. Dr. S�anchez-L�opez is also with Universidad de Castilla-La Mancha, School of Education,Ciudad Real, Spain. Dr. Mart�ınez-Vizca�ıno is also with Universidad Aut�onomade Chile, Facultad de Ciencias de la Salud, Talca, Chile. Dr. Pesce is withHuman and Health Sciences, Italian University Sport and Movement “ForoItalico,” Rome, Italy.

Mrs. �Alvarez-Bueno is supported by a grant from the Spanish Ministry of Ed-ucation, Culture and Sport (FPU13/03137). Mr. Cavero-Redondo and Mr.Mart�ınez-Hortelano are supported by grants from the University of Castilla�LaMancha (FPU13/01582 and PREDUCLM16/14, respectively).

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Dr. Mart�ınez-Vizca�ıno, Dr. Caterina Pesce, and Mrs. �Alvarez-Bueno designedthe study. Dr. Mart�ınez-Vizca�ıno was the Principal Investigator and Guarantor.Dr. Pesce, Mrs. �Alvarez-Bueno, and Dr. Mart�ınez-Vizca�ıno were the maincoordinators of the study. Dr. Pesce, Mrs. �Alvarez-Bueno, Mr. Mart�ınez-Hor-telano, and Mr. Cavero-Redondo conducted the study. Mr. Mart�ınez-Horte-lano, Mr. Cavero-Redondo, Dr. S�anchez-L�opez, and Dr. Pesce providedstatistical and epidemiological support. Dr. Mart�ınez-Vizca�ıno wrote the articlewith the support of Dr. S�anchez-L�opez, Dr. Pesce, Mrs. �Alvarez-Bueno, Mr.Cavero-Recondo, and Mr. Mart�ınez-Hortelano and revised it critically. All ofthe authors revised and approved the final version of the manuscript.

Disclosure: Drs. Pesce, S�anchez-L�opez, Mart�ınez-Vizca�ıno, Mrs. �Alvarez-Bueno, Mr. Cavero-Redondo, and Mr. Mart�ınez-Hortelano report nobiomedical financial interests or potential conflicts of interest.

Correspondence to Mairena S�anchez-L�opez, PhD, Social and Health CareResearch Center, Universidad de Castilla-La Mancha, Ciudad Real, Spain;e-mail: [email protected]

0890-8567/$36.00/ª2017 American Academy of Child and AdolescentPsychiatry

http://dx.doi.org/10.1016/j.jaac.2017.06.012

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