Brand 2015
Brand 2015
Brand 2015
Serge Brand 1,2,* Background: Prevalence rates of autism spectrum disorder (ASD) have increased dramatically
Stefanie Jossen 2,* in the last two decades. In addition to the core symptoms such as impaired communication, dif-
Edith Holsboer-Trachsler 1 ficulties in social interaction, and restricted and stereotypical patterns of behavior and interests,
Uwe Pühse 2 poor sleep and motor skill (MS) deficits have also been observed in children with ASD. On
Markus Gerber 2 the other hand, there is evidence that aerobic exercise training (AET) has a positive impact on
sleep, and that specific training improves MSs. Accordingly, the aim of the present pilot study
1
Psychiatric Clinics of the University
of Basel, Center for Affective, was to investigate to what extent a combination of AET and MS training (MST) would improve
Stress and Sleep Disorders (ZASS), sleep and physical performance in a small sample of children with ASD.
2
Department of Sport, Exercise Methods: Ten children with ASD (mean age: 10 years) took part in the study. After a thorough
and Health, Sport Science Section,
University of Basel, Basel, Switzerland medical examination and psychiatric assessment, children participated in thrice-weekly 60-minute
sessions of AET and MST lasting for 3 consecutive weeks. Sleep was assessed both objectively
*These authors contributed equally
to this work and share the first (sleep-encephalography [sleep-EEG]) and subjectively (parents’ questionnaire). MSs were assessed
authorship via standardized test batteries. Parents completed sleep and mood logs, and ratings of mood.
Results: Mild-to-moderate insomnia was reported in 70% of children. Compared to nights
without previous AET and MS, on nights following AET and MS, sleep efficiency increased
(d=1.07), sleep onset latency shortened (d=0.38), and wake time after sleep onset decreased for
63% of the sample (d=1.09), as assessed via sleep-EEG. Mood in the morning, as rated by parents,
improved after three weeks (d=0.90), as did MSs (ball playing, balance exercise: ds.0.6).
Conclusion: The pattern of results of this pilot study suggests that regular AET and MST
impact positively on sleep, MSs, and mood among children with ASD.
Keywords: physical activity, ball playing, balancing, insomnia, sleep efficiency, autism spec-
trum disorder, sleep-EEG
Introduction
There is an agreement within the scientific community that prevalence rates of mental
and neurological disorders have increased and have now overtaken those of cardio-
vascular diseases and cancer.1 Here, we focus on autism spectrum disorder (ASD),
understood as a neurodevelopmental condition characterized by severe impairment of
reciprocal social interactions and communication skills, and the presence of restricted,
stereotypical behaviors.2 Having ASD affects basic aspects of social behavior (eg, eye
Correspondence: Serge Brand contact, vocalization) and attention (to certain kinds of stimuli) and also motivation,
Psychiatric Clinics of the University of which in turn affects learning and opportunities for learning. At least for five rea-
Basel, Center for Affective, Stress and
Sleep Disorders (ZASS), Wilhelm Klein- sons, this mental and neurological disorder warrants special attention. First, there are
Strasse 27, 4012 Basel, Switzerland indications that advances in screening and diagnostics are associated with the rising
Tel +41 61 325 5114
Fax +41 61 325 5513
prevalence rates reported of ASD as compared, for instance, with cognitive disability3
Email [email protected] (for an opposing point of view, refer Baxter4). Second, it is estimated that, with respect
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Brand et al Dovepress
to disability-adjusted life years (DALYs; a measurement to showed that shortened sleep duration was associated with
assess “the sum of years lost due to premature mortality and lower social competences and increased stereotypical behav-
years lived with disability adjusted for severity”), autistic iors and autistic symptoms, a pattern also observed elsewhere.24
disorders account for more than 58 DALYs per 100,000 Further, Wiggs and Stores25 noted that sleep problems among
population, leading to substantial health loss over the life children with ASD persist over time, suggesting therefore that
span.4 Third, Croen et al5 estimated that, for example, in the sleep patterns remain relatively stable over time, a pattern also
USA, treatment of ASD was the most expensive category found among healthy 4.5-year-old preschoolers 1 year later,26
of special education, and that health care costs were three- and as well as in the transition to adolescence.27 In summary,
fold higher for children with ASD than for children with among children with ASD, sleep is impaired, remains stably
other mental or physical disorders. Fourth, the psychologi- poor, and seems to be one of the most characteristic features
cal burden for children with ASD and also for their close of the disorder beyond the core symptoms such as impairment
caregivers is extremely high.6 Fifth, there is a need of both of reciprocal social interactions and communication skills, and
scientific research and practical interventions to improve the the presence of restricted, stereotypical behaviors. One aim
sleep7–10 and motor skills (MSs) of children with ASD,11–13 of the present pilot study was therefore to investigate to what
with research having shown that poor sleep and poor MSs extent sleep in children with ASD might be improved by means
are problems for children with ASD, while poor sleep is also of PA, and more specifically via a combination of aerobic
a problem for their caregivers. exercise training (AET) and MS training (MST). Accordingly,
The aim of the present study was to investigate the influ- we hold that the present results might add to the extant litera-
ence of physical activity (PA) on MS, endurance perfor- ture on sleep research in which, to the best of our knowledge,
mance, and objective sleep in children with ASD. Therefore, the influence of PA on sleep in children with ASD has barely
in the next paragraphs, we first explain the importance of been investigated.
sleep in psychological functioning, and we review research With regard to the association between PA and sleep,
on sleep in children with ASD. Next, we explain the influ- cross-sectional28–30 and longitudinal–interventional studies31
ence of PA on sleep. Last, we report the issue of MSs and have shown that PA has a positive influence on sleep. For
PA of children with ASD. example, Kalak et al31 observed objectively improved sleep
With respect to sleep, numerous studies confirm that suf- among adolescents following 3 weeks of morning jog-
ficient and restoring sleep is associated with more favorable ging, relative to controls. Studies carried out among older
psychological functioning;14–16 better-quality sleep is associ- children,32 adolescents,33 and adults34 have shown that acute
ated with better academic, cognitive, emotional, behavioral, bouts of PA improved sleep,32 that more vigorous exercise
and social performance. led to objectively improved sleep,33 and that adult regular
In children with ASD, sleep problems are common. First, exercisers, irrespective of the time of the day at which they
we note that the occurrence of ASD is associated with poor exercised, reported better sleep.34,35 Most importantly, posi-
sleep; Liu et al7 reported that prevalence rates of insomnia tive associations between PA and sleep were also found when
range between 40% and 80%,17,18 while Ming et al9 observed both PA and sleep were assessed objectively.30,36 Further, to
that sleep disorders are among the most prevalent comorbidi- our knowledge, Wachob and Lorenzi37 were the first to show
ties in ASD. Not surprisingly, the US National Sleep Founda- that among children with ASD, increased physical activity
tion identified children with ASD as one of the highest priority was associated with increased sleep quality. Overall, it is
populations for sleep research and treatment.19 Richdale and apparent that PA, irrespective of the time of the day at which
Schreck8 claimed that about two-thirds of children with ASD it is taken, has a positive impact on sleep. The aim of the
develop persisting sleep disorders. Concerning the associa- present study was accordingly to investigate whether physi-
tion between sleep disorders and IQ, Hare et al20 and Cortesi cal activity and more specifically AET and MST also have a
et al21 found higher sleep disturbances to be associated with positive impact on the sleep of children with ASD.
lower IQ in children with ASD, while Couturier et al22 found In addition to the core symptoms of ASD, MS deficits
sleep disturbances among the so-called high-functioning ASD are frequently observed in children with this disorder,38 with
children. Importantly, Cortesi et al21 found that parents of impairments ranging from 9.9% (borderline impairments)
children with ASD reported more impaired motor behavior to 72% (evident impairment). Following Jansiewicz et al39
(agitation, increased restricted and stereotypical behaviors) children with ASD often also meet the criteria of DSM-IV
following a night with severely impaired sleep, compared for functional motor impairments.12,40 Generally, children
to nights with more regular sleep. Likewise, Schreck et al23 with ASD show poorer performance in gross and fine MSs,
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Dovepress Physical activity and sleep in children with Autism Spectrum Disorder
motor flexibility, and balance.41–44 Further, Freitag et al42 demands for assistance and educational support; b) poor sleep
found an association between lower static and dynamic bal- and poor MSs are the most prominent impairments seen in ASD
ance and higher social withdrawal in children with ASD, besides the core symptoms; c) PA is an attractive and low-cost
while Rosenthal-Malek and Mitchell44 and Elliott et al45 intervention; d) any kind of improvement in the behavior and
found that regular PA reduced the occurrence of restricted sleep of children with ASD has benefits on the psychological
and stereotypical pattern of behavior. Teitelbaum et al46 functioning of their close caregivers;25,50,51 and e) the sleep
analyzed the motor behavior of 4- to 6-month-old infants patterns of family members are intertwined.52,53 Accordingly,
and observed that peculiarities in motor behavior at this age improved sleep in children with ASD should also improve the
such as the shape of the mouth and delays in some or all sleep of their close caregivers.
developmental milestones, including lying down, righting, The following hypotheses were formulated. First, fol-
sitting, crawling, and walking, predicted the emergence of lowing Dworak et al32, Wachob and Lorenzi37, and Brand et
ASD at the age of 3 years. Teitelbaum et al46 concluded that al33 we expected more favorable objective sleep parameters
movement disturbances seemed to be important aspects of such as extended deep sleep (DS), shorter sleep onset latency
the phenomenon of autism even at a stage when ASD has (SOL), and fewer awakenings after sleep onset following PA,
not yet been diagnosed. We note that, following Teitelbaum as compared to sleep without preceding PA. Second, follow-
et al46 movement disturbances are already observable during ing Kalak et al,31 Lang et al,30 and Gerber et al37 we expected
infancy and that, for example, following Rosenthal-Malek and improvements in sleep (eg, more DS, less light sleep, fewer
Mitchell44 and Elliott et al45 regular PA might favorably impact awakenings after sleep onset) as objectively assessed after
on restricted and stereotypical behavior. Further, Lang et al47 the intervention compared to sleep before the intervention.
speculated that poorer MS performance might also be due to Third, following Lang et al47 and Sowa and Meulenbroek49
more limited exercise opportunities and exercise activities. we expected that MSs (eg, ball playing, balancing) would
In this connection, Reid48 speculated that the lack of desire improve following the intervention. Fourth, following Kalak
to participate in social activities such as ball games or leisure et al31 we anticipated improved mood and daytime function-
activities could also lead to reduced exercise activities and ing in children with ASD after PA intervention, as reported
opportunities as compared to typically developing children. by parents.
Lang et al47 summarized the results of 18 studies focusing on
PA in individuals with ASD and concluded that regular PA Methods
impacted positively on stereotypical behaviors, aggression, Sample
self-harm, aberrant behavior during school classes, and school Children with ASD were recruited from schools and centers
performance. In a further meta-analysis of 16 studies of PA in the central part of German-speaking Switzerland (Kanton
in individuals with ASD, Sowa and Meulenbroek49 showed Berne, Switzerland). Recruitment of the participants for this
that individually tailored PA programs improved MSs and study was made via requests from various institutions that
behavior, as compared to standardized group programs. We are active in the field of autism in Switzerland. The inclusion
took these results into account and introduced a standard- criterion was clinical diagnosis of an ASD, as carried out by
ized, though individually performed, intervention program experienced psychiatrists and psychologists. Further, a medi-
consisting of AET and MST. To take into account children’s cal doctor, the parents, and the child decided together whether
individual skills, the training programs were individually the child was able to participate with the required frequency in
tailored to each participant. the training program. After parents signed the written informed
In conclusion, we note that children with ASD suffer from consent, a trained psychologist not otherwise involved in
poor sleep, and poor MSs, as compared to typically developing the study performed a psychiatric diagnosis based on the
children. However, research also shows that PA has the potential Autism Diagnostic Observation Schedule54 and the revised
to improve sleep, and almost by definition, MSs, though surpris- Autism Diagnostic Interview.55 Mean age was 10 years
ingly, there is little research on these topics among children with (standard deviation [SD] =2.34; age range: 7–13 years;
ASD. We took these observations into account in devising a females: 50%). Diagnosis was based on the ICD-10.56 Six out
pilot exploratory study of the extent to which an AET and MST of ten participants suffered from infantile autism, three suf-
intervention might lead to positive changes in sleep and MSs fered from Asperger syndrome, and one child suffered from
among a small sample of children with ASD. We believe that high-functioning autism. Further, a medical doctor not other-
the results may be of practical importance, given the following: wise involved in the study performed a brief medical check
a) prevalence rates of ASD are increasing, thus leading to higher to ensure that there were no medical risks in participating in
the AET and MST. Given that the structure of the autistic Tools
symptoms lacked homogeneity across participants, a specific Sleep
and individualized intervention was necessary. The Review Objective sleep
Board of the University of Basel (Switzerland) approved the The sleep-EEG device was applied four times: at the begin-
study, and the entire study was performed in accordance with ning and at the end of the study (nights not following PA),
the principles laid down in the Declaration of Helsinki. and two nights during the 2nd week following PA. Par-
ticipants were requested to adhere to their normal evening
Intervention routines, to go to bed at the usual time which was between
At the beginning of the intervention, for each child, an indi- 8 pm and 9 pm and to get up between 6 am and 7.30 am.
vidual training plan was created. A training frequency of Sleep-EEG recordings were performed at home using a
three sessions per week was planned with the intervention as one-channel EEG device (Fp2-A1; electro-oculogram;
a whole lasting 3 weeks. Each training session consisted of electromyogram; Somnowatch®; Randersacker, Germany).
a 30-minute bicycle workout (AET) followed by 30 minutes Sleep polygraphs were visually analyzed by two experi-
of training in coordination and especially in balance (MST). enced raters according to the standard procedures.59 Sleep
The choice of a bicycle workout was made for the follow- parameters were analyzed according to the definitions in
ing reasons. Cycle training is easily adapted to individual the standard program described by Lauer et al.60 The device
motor abilities and allows specific progressive steps. In was applied at about 7.30 pm by a lab technician. The device
addition, it allows training in the endurance zone. Accord- provides assessment of total sleep time, sleep period time,
ing to Youngstedt et al57 endurance training in particular SOL, sleep efficiency (SE), stages 1–4, light sleep (stages 1
may have a positive influence on sleep. Additionally, the and 2), slow wave sleep (SWS; stages 3 and 4), rapid eye
ability to cycle is an important capacity in everyday life and movement sleep, rapid eye movement sleep latency, and
allows participation in social activities. Explicit facilitation number and time of awakenings after sleep onset.
of coordination ability (concrete balance and ball skills) Four sleep-EEG measurements were made: one at the
has a scientific basis. Limitations have been reported for beginning and one at the end of the study together with one
autistic children in gross and fine MSs as well as problems on a night following PA training and one on a night that did
with balance.42,58 Likewise, in some studies, children with an not follow PA. To determine whether sleep improved over
ASD have displayed reduced ball skills.38 The intervention the course of the study, sleep-EEGs on the first night were
was executed in a highly structured manner and was based compared with sleep-EEGs on the last night. To determine
on the “Applied Behavioral Analysis” (ABA) method. ABA whether acute bouts of exercising influenced sleep, sleep-
is based on the principles of operant conditioning with posi- EEGs with and sleep-EEGs without PA during the preceding
tive reinforcement as the principal feature. Children were day were compared.
positively reinforced verbally with compliments for every
successful trial (playing with ball; balancing) and every effort Subjective sleep
on the bicycle. Further, daily and weekly improvements in Parents completed the Insomnia Severity Index (ISI),61 a
skills were visualized with graphs and scales at home in the screening tool for insomnia. The seven items, answered on
child’s bedroom. Further, the training was adjusted according 5-point rating scales (1= not at all, 5= very much), refer to
to the characteristics of autism present in each participant difficulty in falling asleep, difficulties maintaining sleep,
and was aimed at the important concept of errorless learning. increased daytime fatigue, and worrying about sleep. The
Accordingly, the aims of MST were as follows: throwing a higher the overall score, the more the respondent is assumed
ball with one and two hands to the coach over a distance of to suffer from insomnia (Cronbach’s alpha =0.89). Addition-
3–5 m (measurement: number of trials without interruption, ally, the following cut-off criteria61 were applied: 0–7 points:
that is, without losing the ball) and balancing (standing on no clinically significant insomnia; 8–14 points: subthreshold
one leg, jumping, jumping zigzag, balancing) on the beam insomnia; 15–21 points: clinical insomnia (moderate sever-
(moderate-to-large sizes) without interruptions for at least ity); and 22–28 points: clinical insomnia (severe).
30 seconds (measurement: balancing time in seconds).
Specific skills were assessed at the beginning and at the end Sleep schedules and sleep-related psychological
of the intervention. Trials were repeated three times, and functioning
the best trial was used as baseline and as end point of the To assess sleep schedules and sleep-related psychological
intervention. functioning, we administered a brief questionnaire based
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Dovepress Physical activity and sleep in children with Autism Spectrum Disorder
on the Pittsburgh Sleep Quality Index.62 Parents were asked practical importance), and d.0.80 indicating large (ie,
about sleep duration (hours), SOL (minutes), and number crucial practical importance) effect sizes. All statistics were
of awakenings after sleep onset for the last 5 working days. processed using SPSS® 20.0 (IBM Corporation, Armonk,
Additionally, parents reported, on 8-point Likert-scales, for NY, USA) for Apple McIntosh®.
the mornings: sleep quality (1= very good sleep quality),
feeling of being restored (1= completely restored), and mood Results
in the morning (1= very good mood). The log was completed All children participated in all assessments, activities, and
the 1st and the 3rd week, and data were aggregated to form sleep measurements.
composite variables for the 1st week and for the 3rd week
(Cronbach’s alpha =0.84). Subjective sleep over time (ISI scores)
Subjective sleep scores did not change over time (baseline:
Statistical analysis mean =11.60, SD =6.02; end of the study: mean =10.81,
An odds ratio was calculated to estimate the odds of suffering SD =6.76; t(9)=0.63, P=0.55). Seven out of ten children were
from insomnia in the present sample of children with ASD categorized as suffering from subthreshold to clinically relevant
as compared to typically developing children. To compare insomnia. Compared to normative data (insomnia scores:
subjective sleep quality over time, a t-test for paired samples 20%–25%),26 the odds of suffering from insomnia were 9.33-
was performed. To compare objective sleep measures over fold higher in children with ASD than in typically developing
time, a series of t-tests for paired samples was performed. children (odds ratio =9.33, confidence interval =1.19–72.99).
A series of t-tests for paired samples was also performed to
compare the sleep and mood log data between the 1st and Objective sleep over time
the 3rd week, as well as the dimensions of MSs. To com- Table 1 gives the descriptive and statistical objective sleep
pare objective sleep parameters between nights following parameters at the beginning and at the end of the study. No
PA and nights without preceding PA, as a first step, the two significant changes were observed.
measurements of nights following PA and the two nights not
following PA were separately aggregated to single nights Objective sleep on nights with previous
with or without preceding PA. This was followed by a series PA and nights without previous PA
of t-tests for paired samples. Table 2 gives the descriptive and statistical objective sleep
Test results with an alpha level of below 0.05 were parameters for nights preceded by PA and nights without
reported as significant. However, we placed particular preceding PA. Relative to nights without preceding PA,
emphasis on effect sizes, which take into account mean dif- on nights following PA, SE increased, relative DS or SWS
ferences and SDs without being sensitive to sample sizes. increased, and awakening times after sleep onset and SOL
For t-tests, these were calculated following Cohen63 with decreased (all effect sizes were medium to large). No differ-
0.20,d.0.49 indicating small (ie, negligible practical ences were observed for total sleep time, number of awaken-
importance), 0.50,d,0.79 indicating medium (ie, moderate ings after sleep onset, or light sleep.
Table 1 Descriptive and statistical overview of objective sleep variables at baseline and at the end of the study 3 weeks later
Time points Effect sizes
Baseline End of the study
Mean SD Mean SD
TST (hour:minutes) 7:55 46:52 7:49 53:10 0.15 [S]
Sleep efficiency (%) 93.03 4.57 96.76 1.801 0.13 [S]
Sleep onset latency (minutes:seconds) 15:20 14:21 18:12 14:43 0.09 [S]
Number of awakenings after sleep onset 5.56 2.03 5.35 4.34 0.17 [S]
Time awake after sleep onset (minutes:seconds) 27:37 19:19 17:87 15:34 0.19 [S]
Time light sleep (hour:minutes) 3:24 0:23 3:26 1:04 0.09 [S]
Light sleep (%) 43.00 7.34 42.68 16.46 0.14 [S]
Time deep sleep (hour:minutes) 2:21 0:42 2:47 0:56 0.21 [S]
Deep sleep (%) 29.34 7.86 31.45 8.67 0.21 [S]
REM sleep (hour:minutes) 1:27 0:35 1:11 0:33 0.47 [S]
REM sleep (%) 18.32 4.24 14.93 5.14 0.72 [M]
Abbreviations: SD, standard deviation; TST, total sleep time; REM, rapid eye movement; S, small; M, medium.
Table 2 Comparisons of objective sleep data from nights following physical activity and nights not following physical activity
Intervention Effect sizes
Without previous PA With previous PA
Mean SD Mean SD
TST (hours:minutes) 7:45 1:03 7:35 1:53 0.11 [S]
Sleep efficiency (%) 93.03 4.570 96.76 1.80 1.07 [L]
Sleep onset latency (minutes:seconds) 13:20 15:27 09:24 6:37 0.38 [S]
Number of awakenings after sleep onset 6.00 1.528 3.67 2.94 0.39 [S]
Time awake after sleep onset (minutes:seconds) 30:37 22:11 11:46 11:26 1.09 [L]
Time light sleep (hours:minutes) 3:31 0:29 3:26 1:41 0.07 [S]
Light sleep (%) 45.80 5.43 43.60 14.47 0.20 [S]
Time deep sleep (hours:minutes) 2:32 0:42 2:41 0:25 0.26 [S]
Deep sleep (%) 32.80 7.67 36.63 8.27 0.51 [M]
REM sleep (hours:minutes) 0:55 0:34 1:06 0:45 0.28 [S]
REM sleep (%) 11.83 4.68 14.05 5.68 0.42 [S]
Abbreviations: PA, physical activity; SD, standard deviation; TST, total sleep time; REM, rapid eye movement; S, small; M, medium; L, large.
Sleep and mood, as assessed via sleep AET and MST during the day are able to improve specific
logs sleep parameters such as SE (d=1.07), wake time after sleep
Table 3 gives the descriptive aggregated values from week 1 onset (d=1.09), and SOL (d=0.38). It is also worth noting
and week 3 and the comparison between these 2 weeks. Sub- that the amount of SWS increased (d=0.48), given that on
jective sleep quality and mood in the morning improved over
time (moderate-to-large effect sizes). No meaningful effect
Table 3 Descriptive and statistical overview of the sleep and
sizes were observed on any other dimensions.
mood values in the morning, as reported in the logs and as rated
by parents
Motor skills Mean SD t-value Significance ES
Table 4 gives the descriptive and statistical MS performance at Sleep quality (1= excellent, 8= very poor)
the beginning and at the end of the intervention. Improvements Week 1 3.60 1.78 1.11 0.29 0.51
Week 3 2.88 1.11
were observed for catching, throwing a ball with one and two Seeming to be restored (1= absolutely restored, 8= not at all restored)
hands, and balancing (standing on one leg, jumping, jumping Week 1 3.95 1.57 0.74 0.913 0.05
zigzag, balancing) on the beam (moderate-to-large sizes). Week 3 3.40 1.33
Mood morning (1= excellent, 8= very poor)
Week 1 3.85 1.00 1.87 0.094 0.90
Discussion Week 3 2.90 1.10
Tiredness evening (1= not at all, 8= extreme tiredness)
The key findings of the present study are that in a small sam- Week 1 5.52 1.76 -0.465 0.653 0.08
ple of children with ASD, a 3-week intervention involving Week 3 5.66 1.53
Light switched off (hour:minutes)
AET and MST improved specific MSs and led to improved
Week 1 21:04 1:11 -0.324 0.753 0.05
objectively assessed sleep on nights following PA as com- Week 3 21:08 1:17
pared to nights not preceded by PA. Mood also improved Sleep onset latency (hour:minutes)
Week 1 0:29 0:14 -0.803 0.443 0.39
over time.
Week 3 0:37 0:21
Four hypotheses were formulated, and each is now con- Number of awakenings after sleep onset
sidered in turn. Week 1 1.07 1.13 -1.21 0.395 0.32
Week 3 1.30 1.40
Our first hypothesis was that favorable objective sleep Duration of awakenings (hour:minutes)
parameters would be more positive following PA, as com- Week 1 0:05 0:06 -1.133 0.286 0.36
pared to sleep without prior PA, and this hypothesis was Week 3 0:08 0:10
Wake time (hour:minutes)
supported. Accordingly, the present findings confirm those Week 1 6:48 1:00 0.379 0.714 0.10
of previous research,36,37 though in our view, they also Week 3 6:42 1:04
TST (hour:minutes)
expand upon previous findings because we were able to Week 1 9:07 0:26 1.615 0.141 0.32
show this association among children with ASD. Thus, for Week 3 8:46 0:51
children with ASD, physical activities in the form of both Abbreviations: SD, standard deviation; ES, effect size; TST, total sleep time.
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Dovepress Physical activity and sleep in children with Autism Spectrum Disorder
Table 4 Descriptive and statistical overview of motor skill Our second hypothesis was that objective sleep would
performance at the beginning and at the end of the intervention increase following the intervention, but this was not sup-
(N=10)
ported, a finding at odds with previous research.31 Accord-
Mean SD t-value Significance
ingly, there is reason to suppose that the intervention may
Ball
a
not have been of sufficient duration, frequency, or intensity
Catching
Baseline 10.40 3.52 to influence sleep regulation, and ultimately, brain activity
End 14.32 3.45 in the longer term. However, we note that in the present
Throwing
study, children’s subjective sleep was rated by their parents,
Baseline 7.41 4.54
End 9.30 2.46 which further adds to the difficultly of comparisons with
Sum ball skills other studies.
Baseline 8.9 5.47 -4.302 0.002
Our third hypothesis was that MSs would improve
End 11.8 4.71
Balancing one leg; large beam following the intervention, and this hypothesis was fully
Baseline 21.89 4.85 confirmed; children improved in areas related to fine MSs
End 29.93 3.99 such as catching a ball and throwing a ball with one or with
Balancing two legs; moderate beam
Baseline 33.78 6.45 two hands (ds=0.57–2.40). Likewise, fine MSs in balancing
End 40.78 5.45 (standing on one leg, forward, jumping zigzag, balancing
Sum balancingb on a beam) improved dramatically (ds=0.51–5.66). Accord-
Baseline 27.40 5.82 3.030 0.014
End 35.40 5.71 ingly, the present pattern of results fits well with previous
Notes: aPerformances of catching with one and two hands were aggregated. research.47,49 However, these results differ from and add
b
Performance of balancing with one and two legs on the moderate and large beam. to previous research because these improvements were
Abbreviation: SD, standard deviation.
observed within the relatively short time lapse of 3 weeks, or
after just nine sessions, and in which both skill training and
a behavioral level, these sleep indices are among the most endurance performance were trained. Thus, improvements
irritating issues for both the children affected and their close appeared quite rapidly. There is a broad agreement that in
caregivers. Indeed, low SE, long sleep onset latencies, and children with ASD, physical and leisure time activities are
frequent awakenings after sleep onset are often observed in reduced relative to typically developing children, which in
children with ASD,17,18,25 and it seems that both AET and turn will affect learning and opportunities for learning.68–70
MST counteract these difficulties. However, the present data For example, MacDonald et al13 recorded an average for
do not provide any insight into underlying psychophysiologi- moderate-to-strenuous PA of 17 minutes per day after school
cal mechanisms. Whereas Lang et al47 for example, argued for children with ASD, and an average of 10 minutes per day
that physical fatigue is the key factor leading to increased after school for adolescents with ASD. MacDonald et al13
sleep after PA in children with ASD, there are at least three did not compare these averages with evidence from typically
other possibilities. First, we note that SWS increased, and developing children, though other studies71 have reported
Dworak et al32 have speculated that the amount of SWS is substantially higher rates of moderate-to-vigorous PA in
homeostasis-regulated and directly linked to brain energy typically developing children and adolescents. MacDonald
metabolism. Accordingly, it is conceivable that SWS is et al13 noted in addition that 43% of their ASD participants
necessary for replenishment, since brain energy metabo- were overweight. Being overweight during childhood and
lism decreases dramatically during SWS.64,65 Second, it is adolescence is associated with increased risk of cardiovas-
conceivable that increased PA may have improved SWS cular and psychological issues during adulthood,72 thus jus-
via an increase in growth hormone (GH) secretion. 66,67 tifying any additional effort to promote PA among children
Third, we also observed that the wake time after sleep onset with ASD. In this regard, Pitetti et al73 showed that a walking
decreased by 63% (d=1.09), and we know that, for instance, program lasting 9 months both increased physical strength
both increased secretion of GH and adenosine and reduced and reduced body mass index in ten adolescents with ASD,
secretion of cortisol are associated with less interrupted relative to a control condition.
sleep continuity.67 Whereas the present data did not allow Overall, our findings suggest that specific MST can be
us to test these possibilities, future studies should therefore successful in terms of specific improvements. However, a
assess neuro-endocrinological processes during sleep in limitation of the present study is that it remained unclear as
children with ASD. to what extent these improvements produced reductions in
stereotypical pattern of behavior and interests. Future studies completion of the study that the Children’s Sleep Habits
might therefore assess possible changes in these aspects of Questionnaire (CSHQ)74 would have been a better option
ASD following PA interventions. We were unable to replicate because the CSHQ assesses not only sleep quality, as we did
the findings of Rosenthal-Malek and Mitchell44 and Elliott with the ISI, but also information about sleep structures (bed
et al45 that regular PA reduced restricted and stereotypical time, awakenings, etc) and also respiration and parasomnias
pattern of behavior. (night walking, night terrors, etc). This holds particularly true
Our fourth and last hypothesis was that mood and day- because breathing-related issues are often observed among
time functioning would improve following a PA interven- children with ASD.75 Sixth, the study design does not allow
tion. This hypothesis was only partially confirmed, in that us to say whether the favorable effects are due to the AET,
mood in the morning improved but there were no changes the MST, or their combination. Seventh, we are aware that
in any of the other psychological characteristics assessed. the variety of MSs is not limited to biking, ball playing,
The following are possible reasons for the lack of significant and balancing, though, given that children with ASD suffer
differences: (a) the time interval of 3 weeks was too short from a broad variety of impaired MSs,76 we hold that bik-
to produce the relevant changes; (b) logs were completed ing and ball playing provide a good start toward increased
by parents and thus did not involve self-perceptions; and (c) and ultimately socially more involving activities. Last, half
there may have been changes over time on other psychologi- of the participants were female; this ratio is at odds with
cal dimensions but too subtle to be captured by the ques- epidemiologic data showing sex ratios of 3–4:1 in favor of
tionnaires used. On the other hand, we note that also among males. Accordingly, the present sample is unrepresentative
healthy adolescents, not all dimensions of psychological as regards sex distribution.
functioning changed following a PA intervention lasting
3 weeks; whereas mood and pain perception improved, Conclusion
perceived stress and coping strategies did not,31 suggesting Among a small sample of children with ASD, regular AET
therefore that positive changes should not necessarily be and MST delivered over a period of 3 weeks improved objec-
expected on all dimensions. In our opinion, this observa- tive sleep on nights immediately following the training and
tion does help to make some sense of the lack of significant improved MSs.
differences found in the present study.
Despite the new findings, several limitations warrant Acknowledgment
against overgeneralization of the present results. First, the We thank Nick Emler (University of Surrey, UK) for proof-
sample size is small, and statistical power is low, though we reading the paper.
relied on effect size calculations, which take into account
mean differences and SDs without being sensitive to sample Disclosure
sizes. Second, the study design involved a within-group- and The authors report no conflicts of interest in this work.
pre–post-comparison; future studies might also add control
groups such as children with ASD on a waiting list and References
1. Khan NZ, Gallo LA, Arghir A, et al. Autism and the grand challenges
healthy controls. Third, there was no longer term follow-up; in global mental health. Autism Res. 2012;5(3):156–159.
future studies might also prolong the intervention, evaluate 2. American Psychiatric Association. Diagnostic and Statistical Manual
of Mental Disorders (DSM 5). 5th ed. Washington, DC: American Psy-
the ecological validity of the intervention, and investigate chiatric Association; 2013.
to what extent the intervention had an impact, for example, 3. Wisconsin. 2015. Available from: http://www.sped.dpi.wi.gov/sped_
on the family system as studies show that burden is higher ccreports. Accessed January 14, 2015.
4. Baxter AJ, Brugha TS, Erskine HE, Scheurer RW, Vos T, Scott JG. The
for mothers of children with ASD than it is for mothers of epidemiology and global burden of autism spectrum disorders. Psychol
children with other mental disorders.25 Fourth, all ques- Med. 2014;11:1–13.
5. Croen LA, Najjar DV, Ray GT, Lotspeich L, Bernal P. A comparison
tionnaires were completed by parents (usually mothers); of health care utilization and costs of children with and without autism
self-reported data would have been useful, though there is spectrum disorders in a large group-model health plan. Pediatrics. 2006;
agreement that the self-reports and compliance of children 118(4):e1203–e1211.
6. Feinberg E, Augustyn M, Fitzgerald E, et al. Improving maternal mental
with ASD are not always reliable. Future studies should health after a child’s diagnosis of autism spectrum disorder: results from
try to assess self-reports and reports from others such as a randomized clinical trial. JAMA Pediatr. 2014;168(1):40–46.
7. Liu X, Hubbard JA, Fabes RA, Adam JB. Sleep disturbances and cor-
teachers and health care providers. Fifth, with regard to the relates of children with autism spectrum disorders. Child Psychiatry
assessment of children’s sleep, we became aware only after Hum Dev. 2006;37:179–191.
1918 submit your manuscript | www.dovepress.com Neuropsychiatric Disease and Treatment 2015:11
Dovepress
Dovepress Physical activity and sleep in children with Autism Spectrum Disorder
8. Richdale AL, Schreck KA. Sleep problems in autism spectrum disor- 30. Lang C, Brand S, Feldmeth AK, Holsboer-Trachsler E, Pühse U, Gerber M.
ders: prevalence, nature and possible biopsychosocial aetiologies. Sleep Increased self-reported and objectively assessed physical activity
Med Rev. 2009;13:403–411. predict sleep quality among adolescents. Physiol Behav. 2013;120:
9. Ming X, Brimacombe M, Chaaban J, Zimmerman-Bier B, Wagner GC. 46–53.
Autism spectrum disorders: concurrent clinical disorders. J Child 31. Kalak N, Gerber M, Kirov R, et al. Thirty minutes of daily morning
Neurol. 2008;23(1):6–13. running for three weeks improved sleep and psychological functioning
10. Paavonen EJ, Vehkalahti K, Vanhala R, Von Wendt L, Nieminen-von in healthy adolescents compared to controls. J Adolesc Health. 2012;51:
Wendt T, Aronen ET. Sleep in children with Asperger syndrome. 615–622.
J Autism Dev Dis. 2008;38:41–51. 32. Dworak M, Wiater A, Alfer D, Stephan E, Hollmann W, Strüder HK.
11. Green D, Charman T, Pickles A, et al. Impairment in movement skills Increased slow wave sleep and reduced stage 2 sleep in children depend-
of children with autistic spectrum disorders. Dev Med Child Neurol. ing on exercise intensity. Sleep Med. 2008;9(3):266–272.
2009;51:311–316. 33. Brand S, Kalak N, Gerber M, Kirov R, Pühse U, Holsboer-Trachsler E.
12. Fournier KA, Hass CJ, Naik SK, Lodha N, Cauraugh JH. Motor coor- High self-perceived exercise exertion before bedtime is associated
dination in autism spectrum disorders: a synthesis and meta-analysis. with greater objectively assessed sleep efficiency. Sleep Med. 2014;15:
J Autism Dev Dis. 2010;40:1227–1240. 1031–1036.
13. MacDonald M, Esposito P, Ulrich D. The physical activity patterns of 34. Buman MP, Phillips BA, Youngstedt SD, Kline CE, Hirshkowitz M.
children with autism. BMC Res Notes. 2011;4:422–426. Does nighttime exercise really disturb sleep? Results from the 2013
14. Gregory AM, Sadeh A. Sleep, emotional and behavioral difficulties in National Sleep Foundation Sleep in America Poll. Sleep Med. 2014;15:
children and adolescents. Sleep Med Rev. 2012;16(2):129–136. 755–761.
15. Lemola S, Räikkönen K, Scheier MF, et al. Sleep quantity, quality and 35. Loprinzi PD, Cardinal BJ. Association between objectively-measured
optimism in children. J Sleep Res. 2011;20:12–20. physical activity and sleep, NHANES 2005–2006. Mental Health Phys
16. Kalak N, Lemola S, Brand S, Holsboer-Trachsler E, Grob A. Sleep Act. 2011;4:65–69.
duration and subjective psychological well-being in adolescence: 36. Gerber M, Brand S, Herrmann C, Colledge F, Holsboer-Trachsler E,
a longitudinal study in Switzerland and Norway. Neuropsychiatr Dis Pühse U. Increased objectively assessed vigorous-intensity exercise is
Treat. 2014;10:1199–1207. associated with reduced stress, increased mental health and good objec-
17. Souders MC, Mason TB, Valladares O, et al. Sleep behaviors and tive and subjective sleep in young adults. Physiol Behav. 2014;135:
sleep quality in children with autism spectrum disorders. Sleep. 2009; 17–24.
32(12):1566–1578. 37. Wachob D, Lorenzi DG. Brief report: Influence of physical activity on
18. Sikora DM, Johnson K, Clemons T, Katz T. The relationship between sleep quality in children with Autism. J Autism Dev Disord. 2015.
sleep problems and daytime behavior in children of different ages with 38. Hinckson EA, Dickinson A, Water T, Sands M, Penman L. Physical
autism spectrum disorders. Pediatrics. 2012;130(suppl 2):S83–S90. activity, dietary habits and overall health in overweight and obese chil-
19. Mindell JA, Emslie G, Blumer J, et al. Pharmacologic management of dren and youth with intellectual disability or autism. Res Dev Disabil.
insomnia in children and adolescents: consensus statement. Pediatrics. 2013;34:1170–1178.
2006;117:e1223–e1232. 39. Jansiewicz EM, Goldberg MC, Newschaffer CJ, Denckla MB, Landa R,
20. Hare DJ, Jones S, Evershed K, Hare DJ, Jones S, Evershed K. Objective Mostofsky SH. Motor signs distinguish children with high functioning
investigation of the sleep-wake cycle in adults with intellectual dis- autism and Asperger’s syndrome from controls. J Autism Dev Disord.
abilities and autistic spectrum disorders. J Intellect Disabil Res. 2006; 2006;36:613–621.
50:701–710. 40. MacDonald M, Lord C, Ulrich DA. Motor skills and calibrated autism
21. Cortesi F, Giannotti F, Ivanenko A, Johnson K. Sleep in children with severity in young children with autism spectrum disorder. Adapt Phys
autistic spectrum disorder. Sleep Med. 2010;11:659–664. Activ Q. 2014;31:95–105.
22. Couturier JL, Speechley KN, Steele M, Norman R, Stringer B, Nicolson R. 41. Dodd S. Autismus. Heidelberg: Spektrum Akadmischer Verlag;
Parental perception of sleep problems in children of normal intelligence 2007.
with pervasive developmental disorders: prevalence, severity, and pat- 42. Freitag CM. Autismus-Spektrum-Störungen. München: Ernst Reinhardt,
tern. J Am Acad Child Adolesc Psychiatry. 2005;44:815–822. GmbH & Co KG; 2008.
23. Schreck KA, Mulick JA, Smith AF. Sleep problems as possible pre- 43. Freitag CM, Kieser C, Schneider M, Von Gontard A. Quantitative
dictors of intensified symptoms of autism. Res Dev Disabil. 2004;25: assessment of neuromotor function in adolescents with high function-
57–66. ing autism and asperger syndrome. J Autism Dev Disord. 2007;37:
24. Malow BA, Marzec ML, McGrew SG, Wang L, Henderson LM, 948–959.
Stone WL. Characterizing sleep in children with autism spectrum disor- 44. Rosenthal-Malek A, Mitchell S. The effects of exercise on the self-
ders: a multidimensional approach. Sleep. 2006;29(12):1563–1571. stimulatory behaviors of adolescents with autism. J Autism Dev Disord.
25. Wiggs L, Stores G. Sleep patterns and sleep disorders in children with 1997;27(I):193–201.
autistic spectrum disorders: insights using parent report and actigraphy. 45. Elliott RO, Dobbin AR, Rose GD, Soper HV. Vigorous, aerobic exercise
Dev Med Child Neurol. 2004;46:372–380. versus general motor training activities: effects on maladaptive and
26. Hatzinger M, Brand S, Perren S, et al. In pre-school children, sleep stereotypic behaviors of adults with both autism and mental retardation.
objectively assessed via sleep-EEGs remains stable over 12 months J Autism Dev Disord. 1994;24(5):565–576.
and is related to psychological functioning, but not to cortisol secretion. 46. Teitelbaum P, Teitelbaum O, Nye J, Fryman J, Maurer RG. Movement
J Psychiatr Res. 2013;47:1809–1814. analysis in infancy may be useful for early diagnosis of autism. Proc
27. Brand S, Hatzinger M, Stadler C, et al. Does objectively assessed sleep Natl Acad Sci U S A. 1998;95(23):13982–13987.
at five years predict sleep and psychological functioning at 14 years? 47. Lang R, Kern-Koegel L, Ashbaugh K, Regester A, Ence W, Smith W.
Hmm, yes and no! J Psychiatr Res. 2015;60:148–155. “Physical exercise and individuals with autism spectrum disorders:
28. Brand S, Gerber M, Beck J, Hatzinger M, Pühse U, Holsboer-Trachsler E. a systematic review. Res Autism Spectr Disord. 2010;4:565–576.
Exercising, sleep-EEG patterns, and psychological functioning are related 48. Reid G. Understanding physical activity in youths with autism spectrum
among adolescents. World J Biol Psychiatry. 2010;11:129–140. disorders. Palaestra. 2005;21(4):6–7.
29. Brand S, Beck J, Gerber M, Hatzinger M, Holsboer-Trachsler E. Evi- 49. Sowa M, Meulenbroek R. Effects of physical exercise on autism spectrum
dence of favorable sleep-EEG patterns in adolescent male vigorous disorders: a meta-analysis. Res Autism Spectr Disord. 2012;6:46–57.
football players compared to controls. World J Biol Psychiatry. 2010;11: 50. Meltzer LJ. Brief report: sleep in parents of children with autism spec-
465–475. trum disorders. J Pediatr Psychol. 2008;33:380–386.
51. Dykens EM, Fisher MH, Taylor JL, Lambert W, Miodrag N. Reduc- 65. Nofzinger EA, Buysse DJ, Miewald JM, et al. Human regional cerebral
ing distress in mothers of children with autism and other disabilities: glucose metabolism during non-rapid eye movement sleep in relation
a randomized trial. Pediatrics. 2014;134(2):e454–e463. to waking. Brain. 2000;125:1105–1115.
52. Kalak N, Gerber M, Kirov R, et al. The relation of objective sleep 66. Wideman L, Weltman JY, Hartman ML, Veldhuis JD, Weltman A.
patterns, depressive symptoms, and sleep disturbances in adoles- Growth hormone release during acute and chronic aerobic and resistance
cent children and their parents: a sleep-EEG study with 47 families. exercise. Sports Med. 2002;32:987–1004.
J Psychiatr Res. 2012;46:1374–1382. 67. Steiger A, Dresler M, Kluge M, Schüssler P. Pathology of sleep,
53. Bajoghli H, Alipouri A, Holsboer-Trachsler E, Brand S. Sleep patterns hormones and depression. Pharmacopsychiatry. 2013;46(suppl 1):
and psychological functioning in families in northeastern Iran; evidence S30–S35.
for similarities between adolescent children and their parents. J Adolesc. 68. Hilton CL, Crouch MC, Israel H. Out-of-school participation patterns in
2013;36:1103–1113. children with high-functioning autism spectrum disorders. Am J Occup
54. Lord C, Rutter M, DiLavore P, Risi S. Autism Diagnostic Observation Ther. 2008;62:554–563.
Schedule: Manual. Los Angeles: Western Psychological Services; 69. Hochhauser M, Engel-Yeger B. Sensory processing abilities and their
1999. relation to participation in leisure activities among children with high
55. Rutter M, Le Couteur A, Lord C. Autism Diagnostic Interview-Revised – functioning autism spectrum disorder (HFASD). Res Autism Spectr
WPS. WPS ed. Los Angeles: Western Psychological Services; 2003. Disord. 2010;4:746–754.
56. WHO. 2015. Available from: http://www.who.int/classifications/icd/ 70. Potvin MC, Snider L, Prelock P, Kehayia E, Wood-Dauphinee S.
en/. Accessed January 22, 2015. Recreational participation of children with high functioning autism.
57. Youngstedt SD, O’Connor PJ, Dishman RK. The effects of acute exer- J Autism Dev Disord. 2012;43:445–457.
cise on sleep: a quantitative synthesis. Sleep. 1997;20(3):203–214. 71. Brand S, Gerber M, Kalak N, et al. Adolescents with greater mental
58. Landa R, Garrett-Mayer E. Development in infants with autism spec- toughness show higher sleep efficiency, more deep sleep and fewer
trum disorders: a prospective study. J Child Psychol Psychiatry. 2006; awakenings after sleep onset. J Adolesc Health. 2014;54:109–113.
47:629–638. 72. McMullen S. Childhood obesity: the impact on long-term risk of
59. Rechtschaffen A, Kales A. A Manual for Standardized Terminology, metabolic and CVD is not necessarily inevitable. Proc Nutr Soc. 2014;
Techniques and Scoring System for Sleep Stages of Human Subjects. 73(3):389–396.
Brain Information Service. Los Angeles: Brain Research Institute; 1968. 73. Pitetti KH, Rendoff AD, Grover T, Beets MW. The efficacy of a 9-month
NIH Publ. No. 204. treadmill walking program on the exercise capacity and weight reduc-
60. Lauer CJ, Riemann D, Wiegand M, Berger M. From early to late tion for adolescents with severe autism. J Autism Dev Disord. 2007;
adulthood: changes in EEG sleep of depressed patients and healthy 37:997–1006.
volunteers. Biol Psychiatry. 1991;29:979–993. 74. Owens JA, Spirito A, McGuinn M. The Children’s Sleep Habits Ques-
61. Bastien CH, Vallières A, Morin CM. Validation of the Insomnia Severity tionnair (CSHQ): psychometric properties of a survey instrument for
Index as an outcome measure for insomnia research. Sleep Med. 2001; school-aged children. Sleep. 2000;23:1043–1051.
2:97–307. 75. Hoffman CD, Sweeney DP, Gilliam JE, Apodaca DD, Lopez-Wagner MC,
62. Buysse DJ, Reynolds CF, Monk TH, Berman SR, Kupfer DJ. The Castillo MM. Sleep problems and symptomatology in children with
Pittsburgh Sleep Quality Index: new instrument for psychiatric practice autism. Focus Autism Other Dev Disabil. 2005;20:194–200.
and research. Psychiatry Res. 1989;28:193–213. 76. Gowen E, Hamilton A. Motor abilities in autism: a review using a
63. Cohen J. Statistical Power Analysis for the Behavioural Sciences. computational context. J Autism Dev Disord. 2013;43:323–344.
2nd ed. Hillsdale, NJ: Lawrence Erlbaum Associates; 1988.
64. Benington J, Heller H. Restoration of brain energy metabolism as the
function of sleep. Prog Neurobiol. 1995;45:347–360.
1920 submit your manuscript | www.dovepress.com Neuropsychiatric Disease and Treatment 2015:11
Dovepress