Anjali L. Varigonda1, Juliet B. Edgcomb1, Bonnie T. Zima1
1 University of California Los Angeles – Psychiatry, Los Angeles, California, United States.
Received: 15/03/2020 – Accepted: 18/04/2020
Objective: he goal of this work was to perform a systematic review and meta-analysis evaluating and comparing exercise related improvements in various executive function (EF) domains among children and adolescents with attention-deficit hyperactivity disorder (ADHD), Autism Spectrum Disorders (ASD), and Fetal Alcohol Spectrum Disorders (FASD). Methods: A systematic literature research was conducted in PubMed, CENTRAL, and PsycInfo from October 1st, 2018 through January 30th, 2019 for original peer-reviewed articles investigating the relationship between exercise interventions and improvements in three domains of executive function (working memory, attention/set shifting, and response inhibition) among children and adolescents with ADHD, ASD, and FASD. Effect sizes (ES) were extracted and combined with random-effects meta-analytic methods. Covariates and moderators were then analyzed using meta-regression and subgroup analyses. Results: A total of 28 studies met inclusion criteria, containing information on 1,281 youth (N=1197 ADHD, N= 54 ASD, N=30 FASD). For ADHD, exercise interventions were associated with moderate improvements in attention/set-shifting (ES 0.38, 95% CI 0.01-0.75, k=14) and approached significance for working memory (ES 0.35, 95%CI -0.17-0.88, k=5) and response inhibition (ES 0.39, 95%CI -0.02-0.80, k=12). For ASD and FASD, exercise interventions were associated with large improvements in working memory (ES 1.36, 95%CI 1.08-1.64) and response inhibition (ES 0.78, 95%CI 0.21-1.35) and approached significance for attention/set-shifting (ES 0.69, 95% -0.28-1.66). There was evidence of substantial methodologic and substantive heterogeneity among studies. Sample size, mean age, study design, and the number or duration of intervention sessions did not significantly moderate the relationship between exercise and executive function. Conclusion: Exercise interventions among children and adolescents with neurodevelopmental disorders were associated with moderate improvements in executive function domains. Of note, studies of youth with ASD and FASD tended to report higher effect sizes compared to studies of youth with ADHD, albeit few existing studies. Exercise may be a potentially cost-effective and readily implementable intervention to improve executive function in these populations.
Varigonda AL et al. / Arch Clin Psychiatry. 2020;47(5):146-156
Keywords: Epidemiology, depression, anxiety, prisoners, MINI.
Neurodevelopmental disorders, specifically attention-deficit/ hyperactivity disorder (ADHD), autism spectrum disorder (ASD), and fetal alcohol spectrum disorders (FASD) affect approximately 1 out of 6 children in the United States1. ADHD has a high co- occurrence in children and adolescents with FASD and ASD, with prevalence estimates consistently over 50%-60%2,3. Executive function (EF), which refers to higher order cognitive processes that are responsible for purposeful goal-directed behavior4, is frequently compromised in children with ADHD, ASD, and FASD and is implicated in associated behavioral, socio-emotional, and cognitive impairments5.
Although stimulants remain the gold standard for treatment of EF deficits associated with ADHD, up to 30% of children do not show a beneficial response to stimulants6-8. Response to stimulants is even further reduced in children and adolescents with co-morbid autism or prenatal alcohol exposure (PAE)6-8. Furthermore, there is evidence that stimulants have a greater effect on certain EF measures such as attentional performance, and less of an effect on measures such as impulsivity9. Behavioral treatments are relatively difficult to implement, costly, and effects are hard to maintain after termination of treatment10. Research shows that as children with PAE mature, they exhibit problems with the misuse of alcohol, with estimates of prevalence rates ranging from 35% to 60%11. Therefore, new approaches to differentiate and treat the spectrum of EF impairments in children with ADHD, FASD, and ASD are needed.
In recent years, a growing body of literature has supported the growing role of exercise in improving cognition, notably EF12-14. Many converging lines of research into the biological underpinnings of exercise-based improvements in EF have been elucidated. Exercise has been shown to increase levels of norepinephrine, dopamine, and serotonin in the prefrontal cortex, hippocampus and striatum to affect mood and cognition15,16. It is posited that, as a result of exercise, increased levels of dopamine enhance attention, focus, and learning, whereas increases in norepinephrine improve executive function, reduce distractibility, modulate arousal, and enhance memory to assist in learning17,18. In animal models, exercise has been shown to reduce oxidative stress and improve neuroendocrine auto-regulation which has been shown to counteract stress and age-related neuronal degeneration19. Exercise has also been shown to directly cause morphological changes in the brain by increasing blood flow, and has also been shown to result in upregulation of brain- derived neurotrophic factor (BDNF), which plays an integral role in hippocampal functioning and long term potentiation for learning and memory, synaptic plasticity, neurogenesis, and neuroprotection20.
Exercise appears to improve EF in children and adolescents with attention-deficit/hyperactivity disorder (ADHD)14,21,22. Aerobic exercise interventions of at least 30 minutes show the most promise in improving EF deficits associated with ADHD22. Research provides further evidence that exercise induces improvements in executive function (EF) in children and adolescents with ADHD, more so than in typically developing children14,21,22. Although studies suggest that exercise induces similar improvements in EF in animal models exposed prenatally to alcohol, research evaluating the impact of exercise in EF in children and adolescents with prenatal alcohol exposure is lacking. To this date, there is only one study evaluating effectiveness of an exercise intervention on EF in children and adolescents with prenatal alcohol exposure23. Furthermore, research investigating whether exercise interventions have beneficial effects on some EF domains in children with neurodevelopmental disorders is lacking24.
The purpose of this systematic review and meta-analysis is to 1) examine potential differences in exercise related improvement in EF outcomes in different neurodevelopmental disorders, specifically ADHD, FASD, and ASD; 2) evaluate whether certain EF domains are more sensitive to the effects of exercise in children and adolescents with ADHD, FASD, and ASD; and 3) explore whether specific characteristics of participants or the exercise interventions can predict the magnitude of EF improvement in children and adolescents with ADHD, FASD, and ASD. To our knowledge, this is the first meta-analysis of existing studies investigating and comparing the effects of exercise on EF subdomains in children and adolescents with ADHD, FASD, and ASD.
A systematic literature review was performed using PubMed, CENTRAL, the Cochrane Collaboration database of controlled trials (in the Cochrane Library), and PsycInfo from October 1st, 2018 through January 30th, 2019. Keywords used in the search included (autism OR ADHD OR fetal alcohol exposure OR Fetal Alcohol Spectrum Disorders) AND (exercise OR physical activity OR physical fitness) AND (executive function tests OR executive function OR common neuropsychological measures of executive function). Search strategy was based on previous systematic reviews looking at executive function deficits in FASD and ADHD and can be found in the supplemental materials5. Reference lists of included manuscripts and related prior review articles were reviewed for additional studies13,22,24-30.
The meta-analysis followed the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) statement guidelines and adhered to protocol defined prior to data extraction. Only peer-reviewed English-language journal articles were included. The following additional inclusion criteria were applied: study participants 0-18 years old, the study participants were diagnosed with ADHD, ASD, or FASD, the study tested the effect of an exercise intervention on EF, the study used individual neuropsychological assessment tasks as an outcome measure. Studies were excluded if the study did not report an effect size, or statistic from which an effect size could be computed (i.e. book chapters, qualitative reviews). The following exclusion criteria were applied: the study measured domains of cognition other than executive function, the study did not report a measure of executive function directly obtained by assessment of the child (i.e. studies that relied on parent or teacher report), the study did not test the effect of an exercise intervention (i.e. observational studies). The literature search, title, and abstract screening, and evaluation of inclusion and exclusion criteria were performed independently by two of the study’s authors, with disagreements resolved via consensus ratings.
Effect sizes were extracted when the effect size measured the relationship between exercise intervention and executive function. If an effect size was not reported, data from which an effect size could be calculated (e.g. means and standard deviations) was extracted. Measures of executive function were divided into the following domains: working memory, attention/set-shifting, and response inhibition. When more than one domain was reported, a separate effect size was extracted (or calculated) for each domain.
Measures of attention/set shifting included the following: Wisconsin Card Sorting Test, Cognitive Battery Test (a mixed measure of Paced serial addition, size ordering, listening span, digit span backwards, and visual coding), the Color Trails Test Part 1, the Trail Making Test, Eriksen Flanker Test, Test of Everyday Attention, Connor’s Continuous Performance Test, the Visual Pursuit Test, Task Switching Paradigm, and the Auditory Oddball Test. Measures of working memory included the following: Digit Span, Digit Symbol Test, Visual Sequential Memory Test, Corsi Block Tapping Test, and Automated Working Memory Assessment Test. Measures of response inhibition included the following: Stroop Color and Word Test, Go/ No Go Test, Determination Test, Stop Signal Task, STOPIT Task, and Children’s Color Trails Test Part 2. The following data were extracted from each study when reported: participant characteristics including diagnosis, mean age, and stimulant medication use; sample size; study year; study design (crossover, parallel, or single-group pretest- posttest); duration of exercise intervention (i.e. one-time exercise vs weekly exercise); exercise intensity (low vs moderate or high intensity); and type of exercise (running, cycling, mixed exercises, or other). Moderate or High intensity exercise was defined by exercise that reaches at least 50% of the maximal heart rate as defined by the American College of Sports Medicine (ACSM) guidelines31.
As studies reported different measurement methods, standardized mean different estimates of difference in executive function domain scores were used as effect size (ES) estimates. ES estimates were converted to Hedges’ g to provide an unbiased ES adjusted for small sample sizes. An ES of 0.2 is considered to be low, 0.5 moderate, and 0.8 large32. The 95% Confidence Interval for each ES was also calculated. The ES of each executive function domain represents the average ES estimate derived from each of its relevant neuropsychological measures. At least three independent datasets had to be available to calculate a summary ES. The DerSimonian- Laird (D-L)33 random effects method of meta-analyses was used to pool effect size estimates. This method accounts for variability between studies and allows for generalization of results beyond the sample population34. Each domain of EF (attention/set shifting, working memory, and response inhibition) was pooled separately. Between-study heterogeneity was assessed with the I2 statistic and Cochran’s Q. Confidence intervals were inspected for each pooled SMD and regression coefficient to evaluate the interval estimate of each population parameter. To assess for possible impact of continuous covariates on effect measures, meta-regression was performed on effect size estimates on sample size N, mean age, and year of study publication. A covariate was investigated using meta- regression when at least three independent datasets provided data on the potential moderator. Begg’s and Egger’s tests35,36, were conducted to assess for publication bias and funnel plots were visually inspected. Statistical Analyses were carried out in STATA Version 15.1 (College Station, TX: StataCorp, LLC). P-values were two-tailed, and an alpha level of 0.05 conferred statistical significance. The study did not meet criteria for IRB review.
To ascertain potential sources of heterogeneity between studies, subgroup meta-analyses were performed to further evaluate sources of variability. Between-study heterogeneity within subgroups was assessed using the I2 statistic. Subgroup analyses were conducted for categories for which sufficient data was reported (k > or equal to 2). The following subgroups were assessed: (1) duration (single vs multiple session intervention), (2) intensity (moderate or high vs low), (3) type of exercise intervention (running, cycling, mixed, and other), and (4) study design (repeated measures vs intervention/control).
A total of 256 potentially relevant studies were retrieved, including 107 from PubMed, 39 from CENTRAL, and 110 from PsycInfo. After duplicates were removed, the titles and abstracts of 255 references were assessed for eligibility. Of these, 79 were excluded, and 176 full- text articles were screened. Finally, 28 studies met eligibility criteria, of which 23 assessed children with ADHD, four studies assessed ASD, and one study assessed FASD. Due to the relatively small number of ASD and FASD studies, these studies were combined. The study inclusion (PRISMA) flow chart is displayed in Figure 1.
ADHD and exercise
The total number of participants in the selected studies was 1,197. The number of participants per study varied from 1237 to 55238. Exercise interventions varied in terms of frequency, intensity, and type of exercise (refer to Table 1). Detailed characteristics on the included studies are presented in Table 1.
Attention and set-shifting
Fourteen studies investigated the relationship between exercise interventions and attention and set-shifting scores. Of these, 5 studies reported scores pre- and post-exercise intervention and pre- and post-control intervention21,39-42, three studies reported post-exercise intervention and post-control intervention scores only43-45, and 1 study reported pre- and post-exercise intervention scores only46. Five studies included a healthy (non-ADHD) control group38,43,47-50.
The overall pooled ES was 0.38 (95% CI 0.01-0.75, k = 14) (Figure 2). The I2 test of heterogeneity was statistically significant (I2 = 99.7%, df = 13, p < 0.01), and thus subgroup analyses were conducted to identify substantive and methodological sources of heterogeneity. Type of exercise was a significant moderator of ES, wherein studies that involved running as the exercise intervention tended to find more robust ES (g = 0.49, 95% CI 0.12-0.86, k = 5) compared to other types of exercise (cycling: g = 0.16, 95% CI -0.41-0.72, k = 3; mixed exercises: g = 0.19, 95% CI -0.17-0.55, k = 2; other: g = 0.50, 95% CI-0.34-1.33, k = 4). Meta-regression analyses suggested that participant age and year of study publication were not significant predictors of ES. Subgroups analyses found that presence of healthy control group, study design, duration, intensity, and comorbid medication were not significant moderators of ES. Egger’s test demonstrated evidence of publication bias (t(13) = -2.43, p = 0.032), wherein smaller studies tended to report stronger associations between exercise intervention and improvement in attention and set-shifting scores.
Five studies investigated the relationship between exercise interventions and working memory scores. Of these, four studies reported scores pre- and post-exercise intervention and pre- and post-control intervention39,40,51,52. One study reported post-exercise and post-control scores only53. The overall pooled ES was 0.35 (95% CI -0.17-0.88, k = 5) (Figure 2). The I2 test of heterogeneity was statistically significant (I2 = 99.5%, df = 4, p < 0.01). Meta-regression analyses suggested that study size, participant age and year of study publication were not significant predictors of ES. Subgroup analyses were limited due to small number of total studies. Begg’s and Egger’s tests, as well as visual inspection of the funnel plot, did not demonstrate evidence of publication bias.
Twelve studies investigated the relationship between exercise interventions and response-inhibition scores. Of these, nine studies reported scores pre- and post-exercise intervention and pre- and post-control intervention, two studies reported post-exercise intervention and post-control intervention scores only54,55 and one study reported pre- and post- exercise scores only46. Only one study included a healthy (non-ADHD) control group49.
The overall pooled ES was 0.39 (95% CI -0.02-0.80, k = 12) (Figure 2). The I2 test of heterogeneity was statistically significant (I2 = 99.5%, df = 11, p < 0.01), and thus subgroup analyses were conducted to identify substantive and methodological sources of heterogeneity. Meta-regression analyses suggested that study size, participant age and year of study publication were not significant predictors of ES. Subgroup analyses suggested that studies including participants taking co-morbid ADHD medication tended to report higher ES of the relationship between exercise interventions and response inhibition scores (with comorbid medications: ES 0.50, 95% CI 0.17-0.82; without comorbid medication ES 0.28, 95% CI-0.46-1.03). Presence of healthy control group, study design, duration, intensity, and type of exercise were not significant moderators of ES. Begg’s and Egger’s tests, as well as visual inspection of the funnel plot, did not demonstrate evidence of publication bias.
ASD/FASD and exercise
Five studies conducted exercise interventions for children with ASD/FASD (total N of participants was 84). Studies were small: the sample size of persons with ASD/FASD ranged from 1056 to 3023. All studies used a within-subjects randomized crossover design, with the exception one study57 which used an A-B sequential design (control then intervention). No studies included a healthy control group. Exercise interventions varied in terms of frequency, intensity, and type of exercise. Detailed characteristics on the included studies are presented in Table 1.
Attention and set-shifting
The overall pooled ES was 0.69 (95% CI -0.28-1.66, k = 4) (Figure 3). The I2 test of heterogeneity was statistically significant (I2 = 98.5%, df = 3, p < 0.01). Meta-regressions of sample size N, mean age of study participants, and year of study publication on ES were not significant. Begg’s and Egger’s tests did not demonstrate evidence of publication bias.
Only two pilot studies (reporting data from 22 children) investigated the relationship between exercise interventions and working memory (Anderson-Hanley, 2011). Both studies reported a significant improvement of working memory following exercise intervention, using an A-B sequential control design. The overall pooled ES was 1.36 (95% CI 1.08-1.64, k = 2).
The overall pooled ES was 0.78 (95% CI 0.21-1.35, k = 4) (Figure 3). The I2 test of heterogeneity was statistically significant (I2 = 92.7%, df = 3, p < 0.01). Meta-regressions of sample size N, mean age of study participants, and year of study publication on ES were not significant. Begg’s and Egger’s tests did not demonstrate evidence of publication bias.
Exercise interventions among children and adolescents with neurodevelopmental disorders were associated with moderate improvements in executive function domains. Of note, studies of youth with ASD and FASD tended to report higher effect sizes compared to studies of youth with ADHD, albeit few existing studies. Exercise may be a potentially cost-effective and readily implementable intervention to improve executive function in these populations.
For ADHD, exercise interventions were associated with moderate improvements in attention/set-shifting and approached significance for working memory and response inhibition. Although this meta-analysis supports previous research13,26 indicating exercise is associated with moderate improvements in EF in ADHD, it challenges a previous meta-analysis’s findings that exercise has specific beneficial effects on response inhibition and working memory relative to attention or set shifting in children and adults with ADHD24. Nevertheless, it supports the notion that exercise may have specific beneficial effects in certain EF domains depending on the diagnosis. For ASD and FASD, exercise interventions were associated with large improvements in EF, notably response inhibition and working memory. This was a surprising result given the relative dearth of exercise intervention studies in ASD and FASD compared to ADHD. Sample size, mean age, study design, and the number or duration of intervention sessions did not significantly moderate the relationship between exercise and EF. Running interventions, compared to other forms of exercise, trended toward significance in moderating the effect of exercise on attention and set shifting in children and adolescents with ADHD. Only in the ADHD subgroup did stimulant medication use seem to moderate the relationship of exercise on improvement in response-inhibition but not in attention/ set shifting or working memory.
Given the potential clinical implications of this meta-analysis, it is important to discuss the study’s potential limitations. Heterogeneity in outcome measures made comparisons across studies difficult and resultant heterogeneity of ES estimates was high. As studies varied with regard to randomization and control of confounding variables, causal inferences must be limited. It also impeded attempts to explore predictors of better response to exercise. We sought to explore possible sources of heterogeneity using subgroup and meta- regression analyses. Results of meta-regressions should be interpreted with some caution due to the possibility of Type I errors, a known limitation of meta-regression35. Study bias was also evident in the existing literature, with a positive Egger’s test for the association of exercise interventions and attention/set-shifting, wherein small studies tended to demonstrate larger effects than studies, suggesting that small negative studies are less likely to be published, and thus not included in the meta-analysis. Although exercise interventions were associated with large improvements in working memory in ASD and FASD (ES 1.36, 95% CI 1.08-1.64), conclusions are limited given the availability of only 2 studies.
Moving forward, studies using more standardized and robust methodologies, including larger sample sizes across a diverse range of comorbidities, are needed before recommendations can be made with regard to the dose, intensity, duration, and type of exercise. Further understanding of the effects of particular exercises on specific executive functioning domains (attention, set shifting, response inhibition, working memory) could be helpful in tailoring individualized exercise programs for children with different neurodevelopmental disorders. Research investigating the effect of co-morbid stimulant use to augment benefits of exercise in neurodevelopmental disorders is needed. Finally, research investigating the putative mechanisms for those improvements (i.e. BDNF or dopamine receptor upregulation) could be helpful in identifying additional treatments for children with executive functioning impairments.
Exercise interventions among children and adolescents with neurodevelopmental disorders are associated with moderate improvements in executive function, particularly in children and adolescents with ASD and FASD. Exercise may improve some EF domains more than others depending on the diagnosis. This meta- analysis finds that exercise has a moderate effect on EF in children and adolescents with ADHD and a large effect on EF in children and adolescents with FASD and ASD. There is a need to further investigate the relationship between exercise interventions and different domains of EF in children and adolescents with neurodevelopmental disorders, especially in ASD and FASD.
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