Perspective Current Perspectives on Physical Activity and Exercise Recommendations for Children and Adolescents With Autism Spectrum Disorders Sudha M. Srinivasan, Linda S. Pescatello, Anjana N. Bhat Recent evidence suggests that childhood obesity is increasing in children who are developing typically as well as in children with developmental disabilities such as autism spectrum disorders (ASDs). Impairments specific to autism as well as general environmental factors could lead to an imbalance between the intake and expenditure of energy, leading to obesity. In this article, we describe the mechanisms by which autism-specific impairments contribute to obesity. The evidence on exercise interventions to improve physical fitness, address obesity, and reduce autism-specific impairments in children and adolescents with ASDs is discussed. Limited evidence is currently available for exercise interventions in individuals with ASDs. Therefore, literature on other pediatric developmental disabilities and children who are developing typically was reviewed to provide recommendations for clinicians to assess physical activity levels, to promote physical fitness, and to reduce obesity in children and adolescents with ASDs. There is a clear need for further systematic research to develop sensitive assessment tools and holistic multisystem and multifactorial obesity interventions that accommodate the social communication, motor, and behavioral impairments of individuals with ASDs.

S.M. Srinivasan, MSPT, Physical Therapy Program, Department of Kinesiology, Neag School of Education, and Center for Health, Intervention, and Prevention, Department of Psychology, University of Connecticut, Storrs, Connecticut. L.S. Pescatello, PhD, FACSM, FAHA, Department of Kinesiology, Neag School of Education, and Center for Health, Intervention, and Prevention, Department of Psychology, University of Connecticut. A.N. Bhat, PT, PhD, Physical Therapy Program, Department of Kinesiology, Neag School of Education, Center for Health, Intervention, and Prevention, Department of Psychology, and Center for the Ecological Study of Perception and Action, Department of Psychology, University of Connecticut, Storrs, Connecticut. Mailing address: Physical Therapy Program, University of Connecticut–Storrs Campus, 358 Mansfield Rd, U1101, Storrs, CT 06269 (USA). Address all correspondence to Dr Bhat at: anjana.bhat@ uconn.edu. [Srinivasan SM, Pescatello LS, Bhat AN. Current perspectives on physical activity and exercise recommendations for children and adolescents with autism spectrum disorders. Phys Ther. 2014;94:875– 889.] © 2014 American Physical Therapy Association Published Ahead of Print: February 13, 2014 Accepted: February 10, 2014 Submitted: April 28, 2013 Post a Rapid Response to this article at: ptjournal.apta.org

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utism spectrum disorders (ASDs) are a group of multisystem neurodevelopmental disorders characterized by impairments in social interactions and communication skills and the presence of repetitive and stereotypical behaviors and interests.1 Children with ASDs have impairments in social communication domains such as reduced eye contact, problems with social reciprocity, and verbal and nonverbal communication delays.2,3 Stereotypical behaviors and interests in children with ASDs may include adherence to inflexible routines and motor stereotypies such as hand flapping or body rocking.4 In addition to these core diagnostic impairments, children with ASDs may have a range of impairments in cognitivebehavioral and perceptuomotor domains. Cognitive and behavioral impairments may include attention problems, intellectual delays, anxiety, depression, aggression, temper tantrums, and self-injurious behaviors.5,6 In terms of sensory impairments, children with autism may have difficulties in modulating tactile, auditory, visual, and vestibular inputs, with hyperresponsiveness or hyporesponsiveness to sensory stimuli.7 Children with ASDs may also have pervasive gross motor impairments such as poor visuomotor and bilateral coordination, as well as postural impairments in static and dynamic balance.8 –10 In addition, many children with ASDs have systemic comorbidities such as gastrointestinal disorders and

Available With This Article at ptjournal.apta.org • eTable: Studies on Improving Autism-Specific Symptoms: Details on Study Design, Participant Characteristics, Intervention Characteristics, Tests and Measures, and Results

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food sensitivities.11 Overall, ASDs are complex multisystem disorders characterized by a myriad of impairments in several domains. Obesity is a highly prevalent comorbidity in children with ASDs and might lead to significant health Nevertheless, consequences.12,13 current interventions for individuals with autism do not appear to address issues related to obesity risk and prevention. In light of the growing prevalence of ASDs in recent years,14 this review highlights the important issues related to physical inactivity and obesity in individuals with ASDs and encourages clinicians to develop and implement effective exercise interventions for this population. The specific aims of this article are: (1) to provide estimates on the prevalence of obesity in children and adolescents with ASDs; (2) to explain the mechanisms by which impairments characteristic of individuals with ASDs could contribute to obesity; (3) to discuss the evidence on exercise and physical activity (PA) interventions that address overweight and obesity, physical fitness, and autism-related impairments; and (4) to provide recommendations for assessment and intervention for individuals with ASDs.

who are typically developing but also in children with developmental disabilities such as ASDs, attention deficit hyperactivity disorder (ADHD), and Down syndrome.13,17–19 Children with ASDs are at least as likely to be overweight or obese as their peers who are developing typically.13 The prevalence of obesity in children with ASDs is 30.4% compared with 23.6% in age-matched children without ASDs.13 Among children with chronic disabilities, the prevalence of obesity is greater in children with ASDs than in children with other developmental disabilities, including ADHD and learning disability.18 The multisystem physical, psychosocial, and systemic impairments in this population may contribute to their higher obesity prevalence17,19 (see Figure for details). Obesity is associated with long-term physical and psychosocial consequences, including diabetes, stroke, osteoarthritis, increased cardiovascular risk, stigma, and depression.12,13,19 Overall, obesity is a significant comorbidity in individuals with ASDs, and it serves as a call for clinicians such as physical therapists, occupational therapists, and physical educators to address issues related to overweight and obesity in their clients with ASDs.

Prevalence of Obesity in Individuals With ASDs

Contributing Factors for Obesity in Children and Obesity is caused by a positive Adolescents With ASDs

energy balance in the body due to increased energy intake or decreased energy expenditure, or both.15 The most common indicator to classify obesity in children is the body mass index (BMI), which is defined as the ratio of the weight (in kilograms) to the square of the height (in meters squared).15 Children with BMI at the 95th percentile or higher are classified as obese, and children with BMI at the 85th percentile or higher are considered overweight.15,16 There is growing evidence that obesity is a major concern not just in children

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In this section, we will discuss the factors contributing to obesity in children and adolescents with ASDs using the framework proposed by Rimmer and colleagues for individuals with disabilities.20 We have customized this framework to highlight the antecedents of obesity relevant to children with ASDs (see Figure for details). There are 4 potential factors contributing to obesity in individuals with ASDs: low physical activity levels, poor nutrition, medication use and metabolic abnor-

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Physical Activity and Exercise Recommendations for Autism Spectrum Disorders malities, and lack of knowledge or awareness20 (Figure). Physical activity levels and nutrition directly affect the balance between energy expenditure and intake and contribute to obesity in both children who are developing typically and those with disabilities. Additional indirect contributions to obesity in individuals with ASDs could come from the intake of certain medications, metabolic and hormonal abnormalities, and certain autism-specific impairments. Physical Activity Levels in Individuals With ASDs Children with disabilities are less likely to engage in sustained and vigorous exercise compared with children without disabilities.20,21 Specifically, physical activity levels in children with ASDs were significantly lower compared with their peers who were developing typically.22,23 They lacked involvement in team and non-team sports and engaged in more solitary physical activities such as bicycling and swimming.24 Limited physical activity levels in individuals with ASDs may be attributed to their impairments in motor, social communication, sensory, and behavioral domains. Previous empirical reports suggest that more than 50% of children diagnosed with ASDs demonstrate movement difficulties based on standardized motor assessments.25,26 Poor motor skills including difficulties with motor coordination and balance in this subset of children with ASDs may limit their activity choices.24,27 For example, the inability to perform complex motor activities may lead to preferences for simple and sedentary activities such as watching television or using the computer.23,27 In addition, social communication impairments of children with ASDs could significantly impair their abilities to engage in “group” sports and form peer relationships. Sensory processing probJune 2014

Figure. Contributing factors for obesity in children and adolescents with autism spectrum disorders (ASDs) and the direct and indirect pathways by which autism-specific impairments and environmental factors contribute to the development of obesity in individuals with ASDs.

lems are common in autism, with various studies suggesting that 42% to 100% of children with ASDs may demonstrate problems in various sensory domains, including tactile, auditory, and visual modalities.7,28,29 Sensory modulation problems in children with autism may affect their competence in play and lead to avoidance of activities providing intense sensory stimulation.27 Similarly, behavioral problems or preferences such as highly restricted interests, adherence to inflexible schedules, and a preference for highly predictable, structured activities may limit the activity choices of children with ASDs.23,27 Finally, environmental factors at the family or community level, such as lack of time and resources or unsupportive peer groups, could affect the physical activity behaviors of individuals with ASDs.21,30 To summarize, the multisystem social communication, sensorimotor, and behavioral impair-

ments in children with ASDs, as well as several environmental factors, may contribute to reduced physical activity profiles, thereby leading to obesity. Nutritional Patterns in Individuals With ASDs Nutritional problems such as overly selective food choices can contribute to obesity in children with ASDs. Bandini and colleagues31 compared the food intake patterns of 53 children with ASDs with those of 58 children who were developing typically and found that children with ASDs refused offered foods more (41.7% of foods offered) than children who were developing typically (18.9% of foods offered). Moreover, children with ASDs demonstrated a more limited food repertoire, measured over 3 days, compared with their peers who were developing typically. Nutritional patterns of individuals with ASDs could be affected by 3

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Physical Activity and Exercise Recommendations for Autism Spectrum Disorders autism-specific impairments: problems in sensory modulation, systemic gastrointestinal comorbidities, and social communication impairments. Children with autism may have oral, olfactory, and gustatory hypersensitivity, leading to aversion to foods of certain textures or smells and a reduced consumption of healthy foods.31,32 In addition, more than 70% of individuals with ASDs demonstrate gastrointestinal problems, including chronic constipation, abdominal discomfort, diarrhea, and reflux, as well as food allergies such as lactose intolerance and inflammatory reactions to gluten and casein.11 These systemic comorbidities could additionally compromise the nutritional habits of children with ASDs. Social communication impairments in this population may compound their nutritional problems, thereby contributing to the development of obesity. Specifically, children with autism who are high functioning may realize their difficulties in developing and maintaining friendships with peers, which, in turn, may lead to feelings of depression and isolation and a tendency for binge eating.20 Studies suggest that between 46% and 89% of individuals with ASDs demonstrate problematic feeding behaviors and food selectivity in that they may prefer diets that are energy-dense and starchy, such as sweetened beverages and pizza, and do not consume low energy-dense foods, such as fruits, vegetables, lean protein, and high-fiber foods.32–35 Lastly, several environmental factors, including parent preferences for energy-dense diets or the use of high energy-dense, edible reinforcers, may influence the dietary patterns of children with ASDs.20,35,36 Taken together, there is substantial evidence suggesting that autismspecific impairments and environmental factors could contribute to

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the nutritional imbalance observed in individuals with ASDs. Use of Prescription Medication and Metabolic Abnormalities in Individuals With ASDs Long-term use of prescription medications could contribute to obesity in individuals with ASDs. Children and adolescents with ASDs are commonly prescribed psychoactive drugs, including antipsychotics, antidepressants, antianxiety drugs, and stimulants, for their behavioral or psychiatric symptoms.37 However, some drugs, such as the antipsychotic risperidone, often lead to significant weight gain.38,39 Risperidone treatment for 6 months led to weight gains of 8.2 kg in children with ASDs and 5.4 kg in adults with ASDs.38 It is proposed that antipsychotics have a potent serotonin-blocking action.38,39 Serotonin is the brain satiety factor that helps control feeding behaviors, and the blocking of serotonin may lead to increased appetite and significant weight gain.38,39 Similarly, antipsychotics may desensitize the leptin receptors in the brain and reduce the sensitivity of the satiety center to feedback signals from peripheral adipocytes, leading to overeating and weight gain.39 Hormonal and metabolic imbalances in individuals with ASDs also could contribute to obesity. Specifically, individuals with ASDs may have an imbalance between proinflammatory and anti-inflammatory hormones.40 Proinflammatory mediators such as leptin secreted by the adipose tissue have been implicated in the development of obesity.41 Leptin is involved in the regulation of energy balance and body weight at the hypothalamic level, and higher levels of leptin are associated with increased fat mass and BMI in children.41 On the other hand, anti-inflammatory mediators such as transforming growth factor beta-1 (TGF-␤1) and adiponectin secreted by the adipose tissue are

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known to exert protective effects against metabolic disturbances in the body.40 In some studies, children and adolescents with ASDs had higher plasma levels of leptin and lower levels of adiponectin and TGF-␤1 compared with children without ASDs.40 – 42 Taken together, the use of medications or the presence of hormonal and metabolic imbalances may contribute to energy imbalance and obesity in children and adults with ASDs. Knowledge or Awareness in Individuals With ASDs Children and adolescents with ASDs may not understand the long-term risks associated with obesity and the healthy lifestyle habits to counter them.20 This finding may be especially true for children with autism, who are low functioning and have cognitive impairments. Moreover, children with ASDs may have problems with self-regulation of eating and physical activity patterns.20 Parent or caregiver perceptions about the overall importance of physical activity also play a critical role in determining the physical activity profiles of their children. Parents of children with ASDs frequently reported that intense treatments such as applied behavioral analysis (ABA) for about 30 to 40 hours per week were quite stressful and time-consuming.17,20,30 Therefore, a heightened level of caregiver burden and predominantly sedentary activities during ABA therapies may lead to neglect of physical activity and nutrition in children and adolescents with ASDs.

Exercise and Physical Activity Interventions for Individuals With ASDs Despite the growing evidence for obesity in individuals with ASDs, there is surprisingly little research assessing the efficacy of physical activity interventions for the treat-

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Physical Activity and Exercise Recommendations for Autism Spectrum Disorders ment of obesity and promotion of physical fitness. A recent systematic review of exercise interventions for individuals with ASDs revealed that only 5 of the 18 studies assessed improvements in physical fitness, whereas the remaining studies focused on improvements in behavioral and cognitive skills.43 In this section, we review the existing literature on physical activity interventions aimed at enhancing physical fitness and reducing obesity and overweight as well as impairments related to autism in the behavioral, cognitive, and motor domains (Tabs. 1 and 2 and the eTable [available at ptjournal.apta.org]). Physical Activity Interventions to Address Obesity and Enhance Physical Fitness in Individuals With ASDs Existing reviews on the positive effects of exercise interventions in individuals with ASDs have suggested that regular exercise has beneficial effects in alleviating social, behavioral, cognitive, and motor impairments of autism.43,44 However, these reviews did not provide any definitive conclusions or recommendations regarding the effects of exercise on cardiovascular and musculoskeletal fitness or obesity outcomes. Our review of the literature revealed a total of 10 studies that targeted physical fitness or obesity in children and adolescents with ASDs. We have provided a comprehensive summary of individual study characteristics in Tables 1 and 2. Overall, these studies suggest that exercise promotes cardiovascular and musculoskeletal fitness but has limited effects on overweight or obesity status. Interestingly, despite the growing concern of obesity in individuals with ASDs, not all the studies listed in Tables 1 and 2 included systematic measures of obesity and body composition as preinterventionJune 2014

postintervention assessments. Moreover, only 2 studies exclusively targeted weight reduction in children and adolescents with ASDs.45,46 Pitetti and colleagues45 implemented a graded treadmill training protocol for 9 months in adolescents with developmental disabilities, including autism, and found a significant increase in calorie expenditure and a decrease in BMI in the group of children who received treadmill training compared with the children in the control group. Similarly, Hinckson and colleagues46 implemented a comprehensive 10-week, family-centered weight management program including components of physical activity and nutritional and psychological counseling for individuals with disabilities and their families. Although they did not find any significant improvements in body composition, parents reported positive changes in lifestyle habits of their children postintervention.46 The majority of the studies promoting exercise did not particularly focus on obesity outcomes, and most studies did not include both nutritional and exercise components in the intervention program. Although the volume of literature on physical activity interventions for improving physical fitness in individuals with ASDs appears significant, the evidence is weakened by several shortcomings such as a lack of control groups or between-subjects designs, an emphasis on singlesubject or within-subject designs, relatively small sample sizes (ie, 1–23 individuals with ASDs), and a dearth of long-term outcomes (ie, follow-up assessments present in only 2 of the 10 studies). The studies showed considerable variability in terms of intervention characteristics using the FITT (Frequency, Intensity, Time, and Type) model (see Tabs. 1 and 2 for details). Most studies provided exercise training 2 or 3 times a week with durations varying from 20 min-

utes to 1 hour. In terms of exercise type, both aerobic training and resistance training have been provided. Modalities used for aerobic training include treadmill, cycling, aquatic exercises, and exergaming.45,47–50 Studies typically implemented aerobic exercise at moderate to vigorous intensities. Programs that focused on resistance training mainly targeted upper limb and lower limb muscles using free weights, body weight, and machines.47,51 Overall, conclusions drawn from empirical evidence on efficacy of physical activity interventions to improve fitness and obesity status in individuals with ASDs, although promising, are currently limited due to the lack of rigorous study designs. Physical Activity Interventions for Treating Autism-Related Impairments in Individuals With ASDs Children with ASDs have received a variety of exercise interventions to reduce autism-specific impairments such as problem behaviors, stereotypical behaviors, and inattention, as well as to improve academic performance, social responding, peer relations, and perceptuomotor skills (see more details in the eTable). Several exercise modalities, including swimming, jogging, cycling, weight training, walking, and horseback riding, have been used.43,44 A meta-analysis of 16 studies suggested that, on average, exercise interventions led to a 37% improvement in overall symptomatology of autism, specifically, behavioral and academic improvements.44 In terms of behavioral skills of children with ASDs, vigorous intensity exercises such as jogging, roller-skating, hydrotherapy exercises, and exergames have been used to reduce the frequency of stereotypical behaviors,50,52,53 aggressive or self-injurious behaviors, and hyperactivity.54 In terms of academic performance, physical exercise preceding classroom lessons led to an

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S

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W

W

Lochbaum and Crews47

Hayakawa and Kobayashi51

W

W

Magnusson et al84

Hinckson et al46

17

6

12 (7 E, 5 C)

30 (15 TD, 15 ASD)

23

5

16

10 (5 E, 5 C)

9

1

Sample Size

7–21

9–15

6–12

7–12

15–19

16–21

6–11

14–19

5–9

9

Age Range (y)

Autism, ID

ASD

ASD, CP, MM, DD

HF ASD

Autism, ID

Autism, ID

ASD, CP, MM, DD

Autism with ID

ASD, CP, DD, DCD, BI

ASD

Diagnosis

10

8–12

14

14

12

12–14 (7 wk of AT, 7 wk of RT)

14

36

26 (14 in group, 12 at home)

10

Duration (wk)

2

2

2

2

1

3

2

2, progressed to 5

2

3

Frequency (Sessions/ Week)

Not reported

Not reported

50%–70% of HRmax

Not reported

Not reported for AT, 30 reps of back stretch and ipsilateral machine

AT: 65%–70% of HRmax RT: 60% of maximal weight lift, 3 sets of 12 reps; progressed to 85% of maximal weight lift, 3 sets of 6–8 reps

50%–70% of HRmax

Speed of 2.4–3.5 mph; progressed to 3.7–4.1 mph

AT: 50%–60% of HRmax, progressed to 75%–80% of HRmax RT: 1 set of 6–15 reps using 6RM; progression by increasing weight

Not reported

Intensity

60

60 (alternated between only AT and AT⫹RT)

40 (AT: 20, progresed to 30)

60

Physical activity sessions, including pool sessions at individual and family level, nutrition and lifestyle modification counseling

High-intensity interval training, aerobic exercises, plyometrics, RT using box jumps, box step-up, press-ups, and curl-ups

E: aquatic program with aerobic and strengthening components C: standard treatment, no aquatic program

Aquatic program involving floor and group activities

Sprint training, bicycle ergometer, back stretch, hand and foot ipsilateral machine

AT: stationary cycling RT: leg press, low row, chest press, shoulder press, biceps curl, stomach crunches

AT: 20 RT: ⬍60

30

Aquatic program focusing on aerobic and strengthening exercises

Treadmill training

AT: whole-body movements to music, obstacle courses, ball games, and follow-the-leader games RT: strengthening exercises for upper and lower body and trunk muscles using TheraBand elastic bands (The Hygenic Corp, Akron, Ohio), ball, free weights, and body weight

Hallwick method of hydrotherapy

Type

50

8, progressed to 20

60 (AT: 30, RT: 15–25)

60

Time (min)

Intervention Characteristics

a S⫽single subject, W⫽within-subjects, B⫽between-subjects, WRM⫽within-subjects repeated-measures, E⫽experimental group, C⫽control group, TD⫽typically developing, ASD⫽autism spectrum disorders, CP⫽cerebral palsy, DD⫽developmental delay, BI⫽brain injury, DCD⫽developmental coordination disorder, ID⫽intellectual disability, HF⫽high functioning, MM⫽myelomeningocele, AT⫽aerobic training, RT⫽resistance training, HRmax⫽maximum heart rate, RM⫽repetition maximum, reps⫽repetitions.

B

Fragala-Pinkham et al49

WRM

W

Fragala-Pinkham et al85

Pan48

B

W

Pitetti et al45

Fragala-Pinkham et al90

al52

Study

Study Design

Participant Characteristics

Studies on Improving Physical Fitness and Reducing Obesity: Details on Study Design, Participant Characteristics, and Intervention Characteristicsa

Table 1. Physical Activity and Exercise Recommendations for Autism Spectrum Disorders

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Physical Activity and Exercise Recommendations for Autism Spectrum Disorders Table 2. Studies on Improving Fitness and Reducing Obesity: Details on Dependent Variables, Test Measures, and Resultsa Study

Domain: Dependent Variables and Tests

Results

Cardiovascular: peak V˙O2 in 6MWT, 22.86 running test Musculoskeletal: thrust test, standing broad jump, dynamometry for grip strength, shoulder flexion, and knee extension Flexibility: sit-and-reach test, trunk lateral flexion and hyperextension Balance: single-leg balance test (eyes open and eyes closed) Aquatic skills: aquatic orientation checklist Stereotyped behaviors: frequency 45 minutes before and after hydrotherapy

Increase in balance, agility, power scores, handgrip strength, upper and lower limb strength, flexibility, and cardiovascular endurance; amount of stereotypical movements reduced postintervention

Fragala-Pinkham et al90

Cardiovascular: walking efficiency using energy expenditure index, shuttle run, 1-mile walk/run Musculoskeletal: curl-ups, push-ups, dynamometry for peak isometric strength of hip abductors, knee extensors, and ankle plantar flexors Gross motor and functional skills: GMFM, PEDI, BOTMP Flexibility: sit-and-reach test

6 of 9 children improved in cardiovascular outcomes such as walking efficiency, energy expenditure, and walk/run times; 7 of 9 children improved in muscle strength; 6 of 9 children improved gross motor and functional skills; 5 of 9 children improved in flexibility; improvements in some dependent measures were not sustained after a home exercise program

Pitetti et al45

Cardiovascular: caloric expenditure per minute on treadmill using V˙O2 and METs Obesity: weight and BMI

Decrease in BMI for experimental group from baseline to postintervention; no such differences seen in the control group

Fragala-Pinkham et al85

Cardiovascular: half mile walk/run Musculoskeletal: modified curl-ups and dynamometry for peak isometric strength of knee extensors, knee flexors, hip abductors, and ankle plantar flexors Gross motor: PEDI, floor to stand Obesity: baseline BMI percentile

Decrease in time to complete half-mile walk/run

Lochbaum and Crews47

Cardiovascular: power work capacity Musculoskeletal: leg press, bench press

3 participants showed 33%, 50%, and 33% increase in cardiovascular fitness; 2 participants showed 19% and 28% improvements on bench press and 29% and 12% improvements on leg press, respectively

Hayakawa and Kobayashi51

Cardiovascular: 10-m walk, 10-m obstacle, 50-m dash Obesity: weight, % body fat Flexibility: hip joint split angle

Decrease in time to complete 10-m walk, 10-m obstacle, and 50-m dash tests

Pan48

Cardiovascular: V˙O2 on 16-m PACER multistage shuttle run Musculoskeletal: curl-ups Obesity: body composition, fat-free mass, fat mass, % body fat Flexibility: Sit and reach test

Improvements in cardiovascular fitness, muscular endurance, flexibility, and aquatic skills in children who were developing typically and children with ASDs; no changes in BMI or % body fat

Fragala-Pinkham et al49

Cardiovascular: half-mile walk/run Musculoskeletal: modified curl-ups and isometric push-ups Aquatic skills: swimming classification scale, YMCA water skills checklist Gross motor: PEDI

Improvement in swimming skills in the aquatic intervention group; no between-group differences

Magnusson et al84

Cardiovascular: V˙O2 during modified Bruce protocol Musculoskeletal: 1-RM bench press, maximal press-up test, 1-RM leg press, maximal curl-up test Flexibility: sit-and-reach test Balance: modified Romberg test

Improvements in cardiovascular fitness, abdominal strength, and frequency of problematic behaviors; improvements in flexibility approaching significance; improvements in positive behaviors toward physical activity based on parent reports

Hinckson et al46

Cardiovascular: 6MWT Obesity: weight, BMI, waist circumference

Improvements in 6MWT distance sustained at follow-up; parents reported decreased consumption of confectionary postintervention

Yilmaz et

al52

a ˙ Vo2⫽volume of oxygen consumed, 6MWT⫽Six-Minute Walk Test, GMFM⫽Gross Motor Function Measure, PEDI⫽Pediatric Evaluation of Disability Inventory, BOTMP⫽Bruininks-Oseretsky Test of Motor Proficiency, MET⫽metabolic equivalent, PACER⫽Progressive Aerobic Cardiovascular Endurance Run, RM⫽repetition maximum, BMI⫽body mass index, YMCA⫽Young Men’s Christian Association.

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Physical Activity and Exercise Recommendations for Autism Spectrum Disorders increase in academic responding and on-task behaviors while reducing disruptive behaviors in class in children with ASDs.55–57 Moreover, the amount of time spent in physical activity positively correlated with engagement in class.56 In terms of addressing social skills, aquatic and equine therapies have been used to reduce antisocial and aggressive behavior and improve social responding and peer relations in children with autism.58,59 Lastly, recreational pool exercises48,58 and horseback riding59 have been used to facilitate gross motor coordination and balance in children with autism. Overall, there is considerable evidence from several studies that exercise interventions are effective in improving motor, social, and behavioral skills of individuals with ASDs.44

torial programs promoting physical activity, nutritious diet, lifestyle education or modification, and parental or caregiver education are more effective in addressing obesityrelated issues in children with developmental disabilities than programs that concentrate on a single component such as diet or exercise.20,36,60 Therefore, an effective treatment plan must involve a collaborative effort among the family, special educators and caregivers, physical therapists/occupational therapists/physical educators, and nutrition experts to ensure long-term improvements. However, as physical therapists and exercise physiologists, our recommendations for assessment and treatment in this section are aimed at the physical activity side of the energy balance equation.

Clinical Implications for Assessment and Treatment of Individuals With ASDs

Recommendations for Assessment In this section, we briefly discuss various standardized tests and measures to assess obesity, cardiovascular and muscular fitness, and physical activity levels in children and adolescents. A comprehensive list of these measures is provided in Table 3. These tests and measures could be used to measure a child’s or adolescent’s baseline performance as well as changes during and after the exercise intervention. Common methods for obesity assessment in children and adolescents include BMI, waist circumference, and skinfold thickness measures.16 Different exercise tests and associated quantitative measures listed in Table 3 could be used to measure cardiovascular and muscular fitness in children and adults.

Obesity in individuals with ASDs results from a variety of contributing factors at the individual and environmental levels. In the following sections, we provide recommendations for assessment and treatment of clients with ASDs for practicing clinicians. As discussed above, our critical review of the current literature on exercise in individuals with ASDs suggests that there is a lack of highquality evidence supporting the use of exercise interventions for improving physical fitness and reducing overweight and obesity. Hence, we will largely draw upon literature from children who are developing typically and children with other pediatric developmental disabilities to provide recommendations for individuals with ASDs. We acknowledge that obesity is a complex problem and holistic interventions that address both sides of the energy balance equation at the personal and environmental level are necessary. The literature suggests that multifac-

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Clinicians must choose exercise tests appropriately depending on the functional capacity, motor skill level, and intellectual level of the child or adolescent with ASD.61 For example, for children with poor trunk control, supported cycling might be

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a better modality to assess cardiovascular fitness than treadmill walking, which places greater demands on the postural system. Clinicians will have to modify the testing protocol for individuals with ASDs who are low functioning by choosing a familiar exercise modality and by providing verbal encouragement and handover-hand assistance to reduce their client’s anxiety.60,62 It would be important to assess the activity levels of children and adolescents with ASDs at baseline and postintervention to evaluate the efficacy of physical activity and lifestyle-modification interventions. Quantitative measures for physical activity include heart rate monitoring, accelerometry, pedometry, electronic screen devices, and inclinometry.63 Qualitative measures of physical activity include diaries, logbooks, and survey questionnaires.63 These can be self-report assessments, or they can be completed by parents or teachers. Self-report questionnaires are not recommended for children under 10 years of age or for children who are low functioning due to their inability to accurately recall physical activity behaviors.63 Both quantitative and qualitative measures require about a week of data collection to obtain an accurate estimate of habitual physical activity levels.63,64 Each measurement, quantitative or qualitative, is associated with some degree of error. An ideal measurement would be one that is objective (ie, associated with the lowest degree of error and highest interobserver agreement).65 Clinicians and researchers should make efforts to reduce measurement error and improve the reliability of their measures and tools. We recommend that clinicians use a combination of quantitative and qualitative measures to obtain objective and reliable estimates of physical fitness and physical activity levels when devel-

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Physical Activity and Exercise Recommendations for Autism Spectrum Disorders Table 3. Measures for Assessing Physical Fitness and Physical Activity Levels in Children and Adolescents With Autism Spectrum Disordersa Measures to Assess Physical Fitness Obesity

Cardiovascular Fitness

Measures index16

Body mass Waist circumference16 Skinfold thickness16

Tests

Measures Test46

Six-Minute Walk Cycle ergometer47 Treadmill45,84 1-mile walk/run85,86 Shuttle run test48,86

Calculated at rest and at peak exertion Heart rate62 Volume of oxygen consumed60 Minute ventilation62 Rate of perceived exertion87,88

Muscular Fitness Tests

Measures

Sit-ups48,49,86 Push-ups48,49,86 Flexed arm hang-up89 Standing long jump89 Dynamometer for limb muscles49

Strength: muscle torque or 1-repetition maximum47,49 Endurance: timed tests, (eg, number of sit-ups in 30 s)48,49,85

Measures to Assess Physical Activity Levels Measures

Method of Use

Data Output

Quantitative Heart rate monitoring

Chest strap and accompanying wrist watch display

Heart rate in real time used to calculate energy expenditure

Accelerometer

Worn on a belt over the hip

Body movements provide estimates of physical activity levels

Inclinometer

Worn around thigh using a strap or adhesive pads

Time spent in different postures such as sitting, standing, and so on

Pedometer

Worn on a belt around the hip

Number of steps taken or walking distance

Direct observation

Live session or video recording across bouts

Frequency, intensity, type, and duration of different activities to judge MET values

Screen monitoring devices

Unit attached to a television or a computer

Time spent viewing the electronic screen over a specific period of time

Self-report or parent or teacher report

Retrospective recall using questionnaires in hard copy/electronic formats or interviews using telephone/in-person/web chats

Frequency, intensity, type, and duration of different activities to judge MET values

Activity diaries or logs

Prospective or current logs using hard copy/ electronic formats

Minutes spent in specific behaviors in real time

Qualitative

a

MET⫽metabolic equivalent.

oping interventions or monitoring progress. Recommendations for Treatment Current interventions for children with autism mainly target their core social communication and academic impairments.66 Such interventions include ABA,67 Teaching and Education of Autistic and Related Communication Handicapped Children (TEACHH),68 and Picture Exchange Communication System (PECS).69 These approaches primarily involve sedentary, tabletop activities in which children with ASDs practice social communication skills in highly structured and confined environments.68,69 Therefore, the onus is on clinicians to promote interventions June 2014

based on movement and physical activity to not only address autismspecific impairments but also reduce obesity and enhance fitness. Although motor and physical activity deficits are not central to the disorder, it is likely that addressing the motor deficiencies and reduced physical activity levels may indirectly affect the core social communication impairments of individuals with ASDs by providing greater opportunities for socialization with peers, better attentional focus, and improved motor performance.9,56,57 Therefore, we recommend that motor and physical activity–related goals be included within the plan of care for individuals with ASDs, given the multisystem

and systemic effects of exercise interventions. There is strong evidence emerging from literature on children who are developing typically and individuals with developmental disabilities such as Down syndrome and cerebral palsy regarding the efficacy of aerobic and resistance training programs in improving physical fitness and achieving weight reduction.60,70 –77 For example, a meta-analysis of 17 randomized controlled trials that implemented nonsurgical interventions for addressing obesity in children and adolescents between 2 and 18 years of age who were developing typically showed that physical activity interventions with durations

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Physical Activity and Exercise Recommendations for Autism Spectrum Disorders Table 4. Physical Activity Programs for Children and Adolescents With Autism Spectrum Disorders (ASDs)a Component of Exercise

Initial Prescription

Progression

Aerobic exercise programs for children and adolescents with ASDs Frequency

3 d/wk

5 d/wk, preferably all days of the week

Intensity

Moderate physical activity

Vigorous physical activity

Time

20–30 min/d accumulated over short bouts

45–60 min/d accumulated over bouts

Type

Jogging, walk/run interval training, cycling, swimming, treadmill training, exergames (eg, Wii, Dance Dance Revolution [Nintendo of America Corp, Redmond, Washington], cyber cycling)

Resistance exercise program for children and adolescents with ASDs Frequency

1 d/wk

2 d/wk

Intensity

10–15 RM

After 6 mo, progress to 8–10 RM Do not go below 6 RM in children

Time

1 set of 6–15 reps

2–3 sets of 8–12 reps, provide 2–3 min of break between sets, gradually reduce breaks between sets

Type

In children less than age 10 y, calisthenics and activities such as jumping, climbing, throwing In children above age 10 y, a strengthening program for muscles of upper and lower extremities and trunk using free weight, TheraBand elastic bands (The Hygenic Corp, Akron, Ohio), and body weight resistance. Machines such as leg press, leg row, shoulder press, chest press with light resistance can be used with caution and supervision.

Flexibility and neuromuscular training program for children and adolescents with ASDs Frequency

1–2 times per week

Time

1h

Type

Muscle stretching exercises for major arm and leg muscles, therapeutic horseback riding, aquatic exercises, yoga, tai-chi

a Exercise guidelines based on literature in children and adolescents with ASDs, other pediatric developmental disabilities, and recommendations of the US Department of Health and Human Services for children who are developing typically.101 RM⫽repetition maximum, reps⫽repetitions.

ranging between 6 weeks and 24 months had a moderate-sized treatment effect (effect size⫽⫺0.52) on measures of adiposity, including percent body fat and fat-free mass.72 Similarly, a recent meta-analysis of 14 studies assessing the efficacy of exercise programs in individuals with intellectual disability indicated an overall positive effect of exercise on physiological measures of cardiorespiratory and musculoskeletal fitness, including volume of oxygen ˙ O2), pulmonary venconsumption (V ˙ E), and muscle force tilation (V production.70 A review of studies adhering to exercise guidelines recommended by the American College of Sports Medicine (ACSM) for improving cardiovascular fitness in individuals with Down syndrome showed that exercise pro884

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grams were effective in increasing ˙ O2, peak V ˙ E, maximum workpeak V load achieved, and time to exhaustion in this population.60 Given the lack of ACSM guidelines for exercise prescription in individuals with ASDs, our exercise recommendations for this population are largely based on studies in children who were developing typically and those with other developmental disabilities. We recommend an exercise program combining components of aerobic, resistance, flexibility, and neuromuscular training for maximum gains in fitness and body composition (details of FITT parameters of exercise are provided in Tab. 4). The majority of the evidence for exercise interventions in individuals with developmental disabilities including ASDs discussed above

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stems from studies conducted at the individual level. However, largescale obesity treatment and prevention programs at the community and school levels have been implemented in children who are typically developing and to some extent in individuals with special needs.78 – 81 Children spend a large portion of their day in school; hence, schoolbased programs may be valuable in developing healthy lifestyle practices in children.81 A Cochrane review provided definitive evidence for the beneficial effects of schoolbased programs on duration of physical activity, television viewing, max˙ O2, and blood cholesterol imum V levels of participants between 6 and 18 years of age.81 School-based interventions typically include components of health education, teacher June 2014

Physical Activity and Exercise Recommendations for Autism Spectrum Disorders Table 5. Specific Recommendations for Exercise Sessions Involving Children With Autism Spectrum Disorders (ASDs) Domain Structure of the environment

Specific Recommendations 1. Predictability and familiarity are important. Follow a familiar exercise schedule. 2. Conduct sessions in the same physical space.68 3. Exercise must be done in thermoneutral environments because children have immature thermoregulatory systems.61 4. Use visual cues to indicate the child’s spot and distinguish the space used. 5. Consider the needs of the child when setting up the environment. For example, avoid distractions, bright lights, and loud sounds for children with hypersensitivity. 6. Use visual picture schedules to provide structure to the session.69 This approach helps children with ASDs to understand the progression in the session and anticipate transitions. 7. Allow time for the child to adapt to any new activity.

Exercise considerations

1. Use adaptive equipment to accommodate the motor impairments of the child.51,83 2. Use heart rate monitors to monitor exercise performance; for children who are intolerant, use pictorial scales such as the pediatric OMNI scale to assess perceived exertion.87 3. For children taking antipsychotic medications, use perceived exertion scales because medications can affect resting and exercise heart rates and blood pressure.61 4. Children who are low functioning may need individual sessions, and children who are high functioning may benefit from group exercise programs. 5. Progress gradually based on individual abilities. 6. Give sufficient breaks and avoid overwhelming the child. 7. Give sufficient time for warm-up and cool-down within a session. 8. Look out for negative behaviors such as tantrums, nonadherence, and self-injurious behaviors. If these behaviors are observed, ask the child to communicate that the activity be stopped. Seek advice from caregivers on best ways to address negative behaviors.66,67 9. Encourage parents to incorporate physical activity in the daily repertoire of the child at home by involving the child in daily chores. 10. Provide different enjoyable activity choices that will help the child succeed.

Instructions, feedback, and reinforcement

1. Avoid long verbal instructions. Be brief and precise in your instructions. 2. Whenever possible, combine verbal and visual instructions. For example, use visual picture schedules and instructions such as “do this.” 3. Provide manual guidance during the motor activities as required. 4. Exercising with a peer/sibling who is developing typically could be motivating for the child. 5. Provide verbal and gestural reinforcement in the form of good jobs and hi-fives.67 6. Provide breaks from activity to do favorite sensory activities. Stickers, small toys, or healthy edibles should be used to ensure adherence to exercise.

training, changes to school curriculum or schedule to increase physical activity, provision of nutritious food, and parent education or counseling.15,78 – 81 The Activity Bursts in the Classroom (ABC) and Motivate, Adapt, and Play (MAP) programs in the United States as well as the modified Mind, Exercise, Nutrition. . .Do It! (MEND) program in New Zealand are examples of such programs.46,78,80 For example, the ABC program is a school-based intervention encouraging physical activity in children who are developing typically using multiple 10-minute activity breaks within the regular daily curriculum.78 These breaks were utilized to promote physical activities that could vary in complexity from basic breaks between classes to whole body movements for fitness to imaginary June 2014

and learning-based play to facilitate the learning of art, music, math, and science concepts, thereby leading to improvements in physical fitness and academic performance.78 Community-based programs such as the “Best Buddies” program also have been implemented to improve fitness in children with disabilities. This is an inclusive physical education program that pairs a child with special needs with a peer who is developing typically (see details at the Best Buddies website82). Overall, there are only a handful of comprehensive programs for children with special needs, and hardly any for those with autism. Therefore, we recommend the implementation of multifactorial and multisystem community or school-level inter-

ventions to address physical fitness and obesity/overweight concerns in children with developmental disabilities. Specific Recommendations for Clinicians Working With Individuals With ASDs Working with individuals with ASDs is challenging; therefore, in this section we provide specific recommendations for clinicians working directly with children with ASDs (see Tab. 5 for details). The following discussion provides general guidelines; however, it is important to tailor the exercise program to the individual needs of each client to maintain interest and long-term adherence to a physically active lifestyle.

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Physical Activity and Exercise Recommendations for Autism Spectrum Disorders Our recommendations are based on principles taken from contemporary treatment approaches for individuals with ASDs, such as ABA,67 TEACHH,68 and PECS.69 These principles inform 2 important aspects of an exercise intervention: the structure of the exercise environment and the nature of the clinician’s interaction, including instructions, feedback, and reinforcement (Tab. 5). The structure of the environment should be consistent, well demarcated, and limited in space depending on program needs and must encourage attentional focus and engagement.67,68 Children with ASDs will need graded prompting or feedback in the form of brief initial verbal instructions, associated visual cues using demonstrations or picture schedules, and hand-overhand feedback when appropriate.67,69 Given the presence of motor impairments in more than 50% of children with ASDs,25,26 they may need adaptive modifications to exercise equipment such as hand rails or harnesses for a treadmill or stabilizers or rollers for a bicycle.51,83 Moreover, the choice of exercise modality will depend on the motor and social impairments of the child. For example, for children with balance impairments, supported stationary cycling might be more appropriate than jogging due to lower demands on the postural system. Children with motor incoordination will benefit from sports activities enhancing upper-limb or whole body coordination in comfortable, noncompetitive, and nonintimidating environments. Furthermore, children with ASDs who are low functioning may require individual-level programs, whereas group-based programs may be more appropriate for children with a high level of functioning. Overall, we recommend that clinicians consider the individual needs of their clients and make appropriate modifications to the environment, exercise equipment, and the nature of their inter886

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actions to ensure their clients’ success within the exercise program. Limitations of the Current Research and Future Directions Current research is restricted to documenting the prevalence of obesity and determining the PA levels and food patterns of individuals with ASDs. Few studies have examined the links between obesity and autism-specific impairments or developed effective obesity interventions in individuals with ASDs. There is a greater focus on using aerobic exercise to enhance PA and reduce the autism-specific impairments of individuals with ASDs, with little evidence for the effects of resistance or neuromuscular training. There is also limited literature on holistic, multifactorial interventions involving a team effort to address obesity issues. Moreover, current literature on exercise interventions for ASDs is limited due to small heterogeneous samples, lack of control groups, presence of confounding factors, and lack of long-term followup. Therefore, in the future, clinical researchers should use rigorous research designs to investigate the unique contributions of autismspecific impairments to obesity and develop multifactorial and multilevel obesity interventions for individuals with ASDs. We acknowledge that conducting high-quality, large-scale randomized controlled trials for systematically addressing issues of overweight and obesity and improving physical fitness in individuals with ASDs is a daunting task, but given the various health concerns associated with obesity, there is an urgent need for clinical researchers to bring issues related to physical fitness to the forefront in this population. All authors provided concept/idea/project design and writing. Ms Srinivasan and Dr Bhat provided clerical support. Dr Pescatello provided consultation (including review of manuscript before submission).

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The authors thank Jill Livingston for her help and support with the literature review for the manuscript. Dr Bhat thanks the National Institutes of Mental Health (grants R21MH089441 and R33MH089441) and Autism Speaks (grant 8137) for their funding support in developing novel, embodied interventions for children with autism spectrum disorders. The content of the manuscript is solely the responsibility of the authors and does not necessarily represent the official views of the National Institutes of Health. DOI: 10.2522/ptj.20130157

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99 Watters RG, Watters WE. Decreasing selfstimulatory behavior with physical exercise in a group of autistic boys. J Autism Dev Disord. 1980;10:379 –387. 100 Powers S, Thibadeau S, Rose K. Antecedent exercise and its effects on self-stimulation. Behav Interv. 1992;7:15–22.

101 US Department of Health and Human Services and US Department of Agriculture. Dietary Guidelines for Americans. 6th ed. Washington, DC: Government Printing Office; January 2005.

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