Article Text

Download PDFPDF

Effects of chronic exercise interventions on executive function among children and adolescents: a systematic review with meta-analysis
  1. Yue Xue1,2,
  2. Yanxiang Yang1,
  3. Tao Huang1
  1. 1 Department of Physical Education, Shanghai Jiao Tong University, Shanghai, China
  2. 2 School of Kinesiology, University of Minnesota, Minneapolis, Minnesota, USA
  1. Correspondence to Dr Tao Huang, Department of Physical Education, Shanghai Jiao Tong University, Minhang District, Shanghai 200240, China; taohuang{at}sjtu.edu.cn

Abstract

Objective To synthesise randomised controlled trials (RCTs) regarding the effects of chronic exercise interventions on different domain-specific executive functions (EFs) among children and adolescents.

Design Systematic review with meta-analysis.

Data sources PsycINFO, PubMed, SPORTDiscus, Academic Search Premier, Embase and Web of Science were searched.

Eligibility criteria for selecting studies RCTs or cluster RCT design, which employ chronic exercise interventions and target healthy children (age 6–12 years) and adolescents (age 13–17 years). We defined chronic exercise as physical activity (PA) which consists of multiple exercise sessions per week and lasts for an extended period of time (typically over 6 weeks).

Results We included 19 studies, with a total of 5038 participants. The results showed that chronic exercise interventions improved overall EFs (standardised mean difference (SMD)=0.20, 95% CI 0.09 to 0.30, p<0.05) and inhibitory control (SMD=0.26, 95% CI 0.08 to 0.45, P<0.05). In meta regression, higher body mass index was associated with greater improvements in overall EFs performance (β=0.03, 95% CI 0.0002 to 0.06, p<0.05), whereas age and exercise duration were not. In subgroup analysis by intervention modality, sports and PA programme (SMD=0.21, 95% CI 0.12 to 0.31, p<0.05) and curricular PA (SMD=0.39, 95% CI 0.08 to 0.69, p<0.05) improved overall EFs performance, but integrated PA did not (SMD=0.02, 95% CI −0.05 to 0.09, p>0.05). Interventions with a session length < 90 minutes improved overall EFs performance (SMD=0.24, 95%CI 0.10 to 0.39, p=0.02), but session length ≥ 90 minutes did not (SMD=0.05, 95%CI -0.03 to 0.14). No other moderator was found to have an effect.

Conclusions Despite small effect sizes, chronic exercise interventions, implemented in curricular or sports and PA programme settings, might be a promising way to promote multiple aspects of executive functions, especially inhibitory control.

  • exercise
  • brain
  • children
  • aerobics
  • adolescent

Statistics from Altmetric.com

Request Permissions

If you wish to reuse any or all of this article please use the link below which will take you to the Copyright Clearance Center’s RightsLink service. You will be able to get a quick price and instant permission to reuse the content in many different ways.

What is already known?

  • There is a consistent and positive effect of acute exercise on executive functions (EFs) across an individual’s lifespan.

  • In observational studies, physical activity (PA) and aerobic fitness are positively associated with EF among children and adolescents, especially on inhibitory control and working memory in children.

  • In experimental studies, the beneficial effects of chronic exercise on EF among children and adolescents are less obvious.

  • The relationship between chronic exercise and EFs may be moderated by individual factors, task-related factors and contextual factors.

What are the new findings?

  • There was a small but significant effect size of chronic exercise interventions on overall EFs and inhibitory control among children and adolescents.

  • There was no effect of chronic exercise interventions on working memory, cognitive flexibility, and planning.

  • The effect of chronic exercise on overall EFs was moderated by body mass index, intervention modality (ie, curricular PA, sports and PA programme, and integrated PA) and session length.

Introduction

Executive function (EF) plays a crucial role in children’s and adolescents’ academic performance,1 social–emotional development,2 and mental and physical health.3 EF encompasses a series of higher-order cognitive processes, including reasoning, planning, completing goal-directed actions and so on.4 It can be divided into (1) core EFs (ie, inhibitory control, working memory and cognitive flexibility); and (2) higher-level EFs (eg, reasoning, planning and problem-solving).5 EF development, in part, depends on lifestyle and environment,6 7 and physical exercise is a potential intervention strategy for EF development. For example, some studies have revealed that exercise is beneficial to EFs and academic performance among children and adolescents.8 9

Exercise can be classified as acute exercise and chronic exercise. Chronic exercise constitutes exercise bouts which last a period of time per session, multiple sessions per week, over the course of weeks (typically over 6 weeks) or years, with specific aims such as improving physical fitness, performance or health.10 The nubmer of studies on the effects of chronic exercise interventions on EFs is relatively small and the findings are conflicting. In particular, observational studies indicate a positive relationship between chronic exercise and EFs in children and adolescents, and the effects on inhibitory control and working memory in children are especially pronounced.11–13 In experimental studies, however, the beneficial effects of chronic exercise on EFs in children and adolescents are less obvious.14–16

The relationship between chronic exercise and EFs may be moderated by individual factors, task-related factors and contextual factors. Specifically, moderating factors at individual level may include age, gender, pubertal stage, body composition, physical fitness, skill levels and so on; task-related moderating factors may include intensity, frequency, overall duration, training modality, type of cognition assessed, stability of the intervention outcomes over time and so on; contextual factors such as study settings (ie, in school, out of school and laboratory)5 may also moderate the potential intervention effects.5 For example, age may be a significant moderator because of the vast difference in the maturation of the prefrontal cortex among different age groups.8 Exercise volume may be a key moderator because of the potential dose relationship with EFs.17 School settings may play an important moderating role because of the social interactional impact and psychological activation during the intervention process.18

We identified three gaps in the literature. First, there is an inadequate consideration of key moderators in previous reviews, and correspondingly, inadequate subgroup and moderation analyses were performed by previous reviews.5 16 Second, few reviews distinguished EF from core EFs and higher-level EFs.5 16 Thus, in addition to the first gap, it is difficult to discern which specific variable of exercise contributes to a specific EF. Third, the existing reviews16 19 included observational or non-randomised controlled trial (non-RCT) studies with RCT studies in their selection criteria, and this may interfere with the conclusion of a causal relationship.

In response to these gaps in the literature, this review, including only RCTs and cluster RCTs, synthesises studies regarding the effects of chronic exercise interventions on domain-specific EFs among children and adolescents.

Methods

The systematic review and meta-analysis was performed following the guidelines from Preferred Reporting Items for Systematic Reviews and Meta-Analyses20 and Cochrane Collaboration handbook.21

Eligibility criteria

This review included studies with an RCT or cluster RCT design, targeted at healthy children (age 6–12 years) and adolescents (age 13–17 years).16 Specifically, participants with a diagnosed cognition disorder or with a physical condition that may interfere with them performing exercise were excluded. This review included studies that employed one or multiple types of chronic exercise modalities as an intervention (typically over 6 weeks) on at least one aspect of EF and excluded studies employing acute exercise or other combined interventions (eg, nutrition).

Literature search

The electronic databases PsycINFO, PubMed, SPORTDiscus, Academic Search Premier, Embase and Web of Science were searched for relevant studies. The combination of the three groups of search MeSH terms were used to locate studies: (1) chronic exercise, aerobic exercise, physical activity (PA), exercise, training and sports; (2) EF, working memory, inhibitory control, cognitive flexibility and planning; (3) child, adolescent, teens and youths. Reference lists of included studies were further examined as complementary sources. All included studies must be published in peer-reviewed journals with full text and conference abstracts were excluded. The language was restricted to English, and there was no restriction on publication year.

Collection of studies

Duplications of records from the searching of databases and reference lists were first excluded, then records which did not meet publication status, and language and publication year were excluded. Next, two authors (Y.X. and Y.Y.) screened the titles and abstracts independently to further exclude records according to the eligibility criteria. Following this, full-text articles were assessed independently by the two authors. Any disagreements were discussed with a third reviewer (T.H.) until a consensus was achieved.

Data extraction

The data of publication year, participant description, study design, instrument, EF variables, study region and settings of eligible studies were extracted and summarised in table 1. According to the Cochrane Collaboration Handbook,21 the mean and SD values of pre-to-post intervention difference were first extracted. More specifically, the change values, if not reported, were calculated by: ‘Mean change = Mean post – Mean pre’ and ‘SD change = SQRT[(SD pre 2 +SD post 2) – (2*Corr*SD post*SD pre)]’, where Corr (correlation coefficient) was set as 0.5.21 For those studies which only provided ‘SE’ and ‘95% CI’, the SD was calculated based on the following formula: (1) SD=SE* SQRT (N), where N is sample size; (2) SD=SQRT (N) * [(UCI − LCI)/3.92], where U=upper CI, L=lower CI. When incorporating the sample size of a cluster RCT, the formulas in ‘16.3.5 Example of incorporating a cluster-randomised trial’ of Cochrane Handbook were followed. The design effect for the trial as a whole was calculated as: 1 + (M – 1) ICC, where M is the average cluster size in the trial, and intraclass correlation coefficient (ICC) was set as 0.02.21

Table 1

Studies included for meta-analysis

Assessment of risk of bias

Two authors (Y.X. and Y.Y.) assessed the study quality according to the PEDro scale.22 The summary of the quality assessment was presented in table 2. Any disagreements were discussed with a third reviewer (T.H.) until a consensus was achieved.

Table 2

Quality assessment of included studies

Statistical analysis

R studio software V.1.1.453 (RStudio, Boston, Massachusetts, USA) was used to conduct the meta-analysis. Considering the different outcomes and units of cognitive measures used in the studies, standardised mean differences (SMD) of pre-post intervention were calculated and given weight by its inverse variance. Cohen’s d values of 0.2, 0.5, 0.8 represent small, moderate and large effect size, respectively.21 A random-effects model was used based on the assumption of different true effect size.21 The heterogeneity was assessed with I2 and p-value for Q statistic. I2 values of 25%, 50%, 75% indicate small, medium and large amount of heterogeneity, respectively.21 Publication bias was assessed by Egger’s test and visually presented with a funnel plot where necessary.23

Additional statistical analysis included: (1) when studies included two intervention groups, their data were combined to create a ‘single pair-wise comparison’21; (2) when studies used two or more instruments to measure the same EF domain, only the more common-used one was included19; (3) for studies that reported multiple results on one cognitive task, the result of more-executive demanding condition was included (eg, incongruent trials in Flanker task)19; (4) when studies conducted two or more measurements, only the last measurement was included.19

After conducting a meta-analysis for overall EFs, subgroup analyses were performed based on the specific EF domains: (1) three core EFs: inhibitory control, working memory and cognitive flexibility; and (2) higher-level EF, namely planning herein.

To investigate the potential moderating effects, meta-regressions were performed based on continuous variables including age, body mass index (BMI) and intervention duration, while subgroup analyses were performed based on categorical variables including study design (RCT or cluster RCT), intervention modality, frequency and session length. The selection of these moderators was principally inspired by Álvarez-Bueno et al 5 and Wiebe and Karbach.3 For the intervention modalities, this review classified intervention modality as (1) curricular PA; (2) integrated PA, including physically active academic lessons, breaks and homework; and (3) sports and PA programmes, including after-school PA and other sports programmes.19 Sensitivity analyses were conducted by excluding studies from meta-analysis one by one.

Results

The initial search retrieved 1303 peer-reviewed articles (figure 1). After removing duplications and reviewing the titles, 407 articles were eligible for further screening. Through a careful reading of the abstracts, 32 articles were eligible for thorough examination. Finally, 13 of these 32 articles were excluded because they had no control group, lacked randomisation, focused on preschool children or had duplicate samples.

Figure 1

Flow diagram of each stage of the study selection.

Study characteristics

Overall, 19 studies were included in the meta-analysis and the study characteristics are summarised in table 1. Ten studies were RCTs17 24–32 and 9 studies33–41 were clustered RCTs. Regarding the study region, 11 studies were conducted in Europe, 5 in America, 2 in Asia and 1 in Oceania. The total sample included 4320 children and 718 adolescents aged from 6 to 17 years. There were 18 studies investigating the effects of chronic exercise on core EFs, of which, 16 studies assessed inhibitory control, 9 studies assessed working memory and 6 studies assessed cognitive flexibility. Compared with the studies exploring the effect of chronic exercise on core EFs, there are significantly fewer studies exploring higher-level EFs, with only two in planning and none in other higher-level EFs. Regarding the exercise intervention protocols, there were only 3 studies with sessions over 90 min, 10 studies with more than five sessions per week and 8 studies with durations over 24 weeks. The major confounding factors considered in the studies included age, BMI, duration, study design, intervention modality, frequency and session length.

The quality of the included studies is presented in table 2. In general, those studies were scored as fairly high quality, with a mean quality score of 7.1, because they were (cluster) RCTs. Moreover, over half of the studies (12 out of 19) were school-based interventions, including active class and breaks, curricular PA and extracurricular PA, whereas the remaining 9 studies were conducted in after school-time settings such as an afterschool PA programme or day camp.

Meta-analysis of effects on EFs

As illustrated by figure 2, the pooled SMD of overall EF was 0.20 (95% CI 0.09 to 0.30, p<0.05), with large heterogeneity (I2=76%, p<0.01). Regarding core EFs, the SMD was 0.26 (95% CI 0.08 to 0.45) for inhibitory control, with large heterogeneity (I2=84%, p<0.01); 0.10 (95% CI −0.05 to 0.25) for working memory, with medium heterogeneity (I2=58%, p=0.02); and 0.14 (95% CI −0.03 to 0.31) for cognitive flexibility, with medium heterogeneity (I2=58%, p=0.04). Regarding the higher-level EF, the SMD was 0.16 for planning (95% CI −0.13 to 0.45), with small heterogeneity (I2=0%, p=0.43). The high heterogeneity for core EFs reflects the importance of taking various moderator factors into consideration when analysing the effects of chronic exercise.

Figure 2

Forest plot for meta-analysis regarding the effect of chronic exercise on different EF domains. (1) core EFs: cognition flexibility, inhibitory control, and working memory (2) higher level EF: planning.

Moderator analysis

Table 3 summarises the results from the meta-regressions and subgroup analyses for overall EFs. In the meta-regressions, higher BMI was positively associated with greater SMD (β=0.03, 95% CI 0.0002 to 0.06, p<0.05, adjusted R2=32.09). Age and intervention duration were not related to changes in SMD.

Table 3

Moderator analysis of chronic exercise and EFs

In the subgroup analyses, the effect of chronic exercises on EFs was significantly moderated by intervention modality and session length, but not by study design and frequency. As illustrated by figure 3, the SMD was 0.02 (95% CI −0.05 to 0.09) for integrated PA (ie, physically active academic lessons, breaks and homework), with small heterogeneity (I2=23%, p=0.22); and 0.21 (95% CI 0.12 to 0.31) for sports and PA programme, with small heterogeneity (I2=0%, p=0.46). At the same time, the SMD for curricular PA was 0.39 (95% CI 0.08 to 0.69), with large heterogeneity (I2=85%, p<0.01). With regard to the exercise session length, the SMD for interventions with a session length < 90 minutes was 0.24 (95%CI 0.10 to 0.39, p=0.02) with large heterogeneity (I2=79.5%, p<0.01), whereas the SMD for interventions with a session length ≥ 90 minutes was 0.05 (95%CI -0.03 to 0.14).

Figure 3

Forest plot for subgroup analysis of intervention modality (curricular PA, integrated PA, and sports and PA program) as a moderator.

Sensitivity analysis

Two studies36 39 were found to be major contributors to the high heterogeneity by the leave-one-out sensitivity analysis. After excluding these two studies, heterogeneity was medium (I2=41.1%, p=0.01), and the pooled SMD of overall cognitive measures was 0.12 (95% CI 0.05 to 0.19).

Publication bias

The funnel plot is presented in the online supplementary figure 1. Egger’s test was used to assess publication bias (t=2.44, df=31, p=0.02). The results indicated the possibility of publication bias for all included studies.23

Supplementary file 1 Funnel plot.

Discussion

Main study findings

This review included only RCT studies with consideration of various moderators to examine the effects of various types of chronic exercise interventions (typically over 6 weeks) on EF among children and adolescents. We found a small but significant effect size of chronic exercise interventions on overall EFs and inhibitory control. In addition, the effect of chronic exercise on overall EFs was moderated by BMI and intervention modality.

Comparisons with previous studies

Our findings of a small effect size on overall EFs and inhibitory control extends a 2014 systematic review that included 19 articles.16 In that study, chronic exercise has no significant effect on overall EFs, without further investigation on specific EF domains. Importantly, there were only five chronic exercise studies in that review and the authors did not limit their review to RCTs. Our findings are strongly supported by another systematic review, which included 36 studies.19 Álvarez-Bueno et al 19 reported a small effect size of chronic exercise on overall EFs and inhibitory control with large heterogeneity. They also revealed a small effect size on higher-level EFs, including planning, with small heterogeneity. Despite the similar results to our findings, their review also included non-RCT studies, similar to Verburgh et al.16 Additionally, they deemed two cohorts or intervention groups as independent samples in their meta-analysis, and this may inflate the true sample size and distort the true weight of each study.

Although aerobic exercise has relatively broad positive effects across a variety of cognitive functions, the benefits of exercise intervention seem to be more significant for EFs.42 However, there is no consensus on which cognitive task is more sensitive to exercise interventions. Among the three core EFs, previous reviews have suggested that inhibitory control is especially sensitive to chronic exercise interventions among children and adolescents,3 19 and our findings also support this point. Among higher-level EFs, our results on the planning domain indicated no effect size with low heterogeneity. However, since there were only two included studies with outcome of this domain, it is premature to draw a clear conclusion.

BMI as a moderator

Between-study heterogeneity is common in a meta-analysis,43 and, in our findings, the effect of chronic exercise interventions on overall EFs and inhibitory control has high heterogeneity, whereas the one on working memory, cognitive flexibility and planning has small or medium heterogeneity. It is worth noting that the meta-regression revealed that the BMI is a moderator on the effect of chronic exercise on EFs, which means that the effects of exercise interventions were comparatively larger on the population with higher BMI. Previous studies have shown that children with excessive body weight demonstrated poorer EF.44 45 Therefore, the potential change of EFs determined by the proportion of overweight participants in the sample may explain the inconsistent findings among the general population. Crucially, it is possible that the children with obesity may benefit more from chronic exercise than their normal-weight peers.

Intervention modality and session length as moderators

In addition to BMI, intervention modality (ie, curricular PA, sports and PA programme, and integrated PA) and session length were also recognised as moderators in our review. The beneficial effects of chronic exercise on overall EFs were observed in the modalities of curricular PA as well as the sports and PA programme rather than integrated PA. Although integrated PA in classrooms is posited to be a promising intervention strategy, current studies have identified that this kind of interventions had no significant effects on EFs. In addition, interventions with a session length < 90 minutes had a positive effect on overall EFs, whereas the exercise session length ≥ 90 minutes had no significant effects on EFs. The reasons for the findings are not clear. As opposed to sports programme and curricular PA, integrated PA possesses less amount of social component and group dynamics. Additionally, the exercise intensity of classroom-integrated PA may be lower than that of sports programme and curricular PA. The results may therefore be partly explained. Also, since these studies had no long-term follow-ups, it remains unclear whether a potential benefit will emerge after a longer period postintervention of integrated PA. Nevertheless, given that no adverse effects were observed, integrated PA in classroom might be a potential way to intervene sedentary behaviour among children and adolescents, without impairment in cognitive development.

As well as integrated PA, cognitively engaging exercise, which is characterised with increased cognitive demands and challenges inherited in the exercise, is also attracting significant attention in this field. Recent studies40 46 47 have hypothesised that cognitive engagement and efforts, instead of physical fitness or exercise dose, may bring about functional changes and contribute to improvements in EFs. Therefore, if an intervention modality involves cognitive engagement, it might enhance the effectiveness of exercise intervention on EFs.

Other potential reasons for the heterogeneity

While the high heterogeneity of pooled effects on overall EFs was partly explained by BMI, intervention modality and session length, our study found that the effect of chronic exercise on EFs was not moderated by other variables such as study design, age, duration, or frequency. This may be due to four potential reasons. First, the high variability among adherence to the exercise protocol varied from study to study and it might lead to the inconsistencies.48 Second, it is especially hard for researchers to control the potential exercise and sports participation of the control group when they are out of the study context, and this may further influence the effect sizes.48 Third, although many studies have taken moderating factors such as age, gender and pubertal stage into consideration, other factors with high inter-individual variability, such as genotype, may also have influenced the intervention effects.48 Lastly, there is no gold standard measurement for EFs thus far.29 Therefore, the cognitive measurements in the included studies may partly explain the incongruous results within the same domain.

Over half of the included studies (12 out of 19) were enacted under real-life settings (eg, school) rather than laboratory settings, which may increase the generalisability of their results. However, while the settings might increase the generalisability, the sample size is comparatively small. It is important to note that most studies conducted post hoc analyses rather than calculating the sample size in advance based on the power requirement and expected effect size. Thus, it may impact the reliability of their results.

Strengths and limitations

One strength of this systematic review is the strict inclusion of RCT studies and exclusion of observational or longitudinal studies. This strict inclusion increases the reliability of the causal relationship inferences. Another strength is the full consideration of various key moderators such as intervention modality, study design, age, duration, frequency and BMI. This provides a much clearer picture than previous reviews of the effects of chronic exercise interventions on EFs. The limitation of this review is the inclusion of various cognitive tasks, which may lead to the high heterogeneity in this review. Furthermore, although we made a comprehensive literature search and an objective study selection, the Egger’s test indicated a possibility of publication bias. Therefore, the findings of the meta-analysis need to be interpreted with caution. Another limitation is the inadequate number of studies in adolescents included. Because of this, the effects of chronic exercise on EFs among different age groups remain to be determined. The third limitation is the insufficient number of studies on the higher-level EFs, which need to be further studied. Lastly, some other potential moderators may not be identified and addressed in our review.

Future studies need to pay particular attention to exploring the following aspects. First, higher-level EFs should be given more attention due to the extremely limited number of studies. Second, more studies in adolescents are needed, considering that different age groups have different speeds and stages of EF development. Third, whether cognitive engagement is a key moderator and whether it substitutes the moderation effect of other potential variables should be further validated. Lastly, longer follow-ups are recommended to track the long-term effects of exercise interventions over time.

Conclusion

This review demonstrated that, despite the small effect sizes, chronic exercise interventions might be a promising way to promote multiple aspects of EFs, especially inhibitory control. Chronic exercise interventions implemented in modalities of curricular PA or sports and PA programme might be particularly beneficial to EFs among children and adolescents. Children with higher BMI appeared to benefit more from exercise interventions.

Acknowledgments

A significant portion of the earlier version of this paper was developed at Physical Activity Epidemiology Laboratory of the University of Minnesota under the mentorship of Dr Zan Gao while YX was a student of the joint Master’s program of Shanghai Jiao Tong University and the Universality of Minnesota and received training in the Laboratory. The authors would like to thank Dr Zan Gao, director of the Laboratory, for his valuable contributions on the earlier draft of the paper. The authors would also like to thank Daniel J McDonough for his useful feedback on an earlier draft of the paper. Finally, they would like to thank Lauren Klaffke, a writing consultant at the University of Minnesota Center for Writing, for her help brainstorming and revising an earlier draft of this paper.

References

Footnotes

  • Contributors YX: contributed to the design of the study, literature search, data screening and extraction, conducted all statistical analyses and wrote the first draft of the manuscript. YY: contributed to the literature search, data screening and extraction, statistical analyses, and critically reviewed and revised the manuscript. TH: contributed to the design of the study, data screening and data interpretation, critically reviewed and revised the manuscript. All authors approved the submission.

  • Funding TH was supported by Shanghai Pujiang Program (16PJC052) and the research project from General Administration of Sport of China (2017B044).

  • Competing interests None declared.

  • Provenance and peer review Not commissioned; externally peer reviewed.

  • Correction notice This article has been corrected since it published Online First. An acknowledgement section has been added.

  • Patient consent for publication Not required.