Sleep Medicine 83 (2021) 106e114

Contents lists available at ScienceDirect

Sleep Medicine
journal homepage: www.elsevier.com/locate/sleep

Original Article

Sleep disturbances in autism spectrum disorder without intellectual

impairment: relationship with executive function and psychiatric
symptoms
Laura Gisbert Gustemps a, b, c, *, 1, Jorge Lugo Marín a, 1, Imanol Setien Ramos b,
~ ez Jimenez b, Odile Romero Santo-Toma
Pol Iban s d, María Jose Jurado Luque d,
Pura Ballester Navarro , Antoni Esteve Cruella , Emiliano Díez Villoria h,
e, f g

Ricardo Canal Bedia i, Josep Antoni Ramos Quiroga a, b, c, i

a
Department of Psychiatry, Hospital Universitari Vall d’Hebron, Barcelona, Catalonia, Spain
b
Group of Psychiatry, Mental Health and Addictions, Vall d’Hebron Research Institute (VHIR), Barcelona, Catalonia, Spain
c
Department of Psychiatry and Legal Medicine, Universitat Auto noma de Barcelona, Barcelona, Spain
d
Sleep Unit, Hospital Universitari Vall d’Hebron, Barcelona, Catalonia, Spain
e
Neuropharmacology on Pain and Functional Diversity (NED) Research Group, Alicante Institute of Sanitary and Biomedical Research (ISABIAL), Alicante,
Spain
f
Department of Clinical Pharmacology, Organic Chemistry and Pediatrics, Miguel Herna ndez University of Elche, Elche, Spain
g
AdSalutem Institut del Son, Barcelona, Catalonia, Spain
h n Integral al Autismo-InFoAutismo, INICO-Instituto Universitario de Integracio
Centro de Atencio n en la Comunidad, University of Salamanca. Salamanca,
Spain
i
Biomedical Network Research Centre on Mental Health (CIBERSAM), Madrid, Spain

a r t i c l e i n f o a b s t r a c t

Article history: The autism spectrum disorder (ASD) is a neurodevelopmental condition, frequently accompanied by
Received 1 December 2020 medical and psychiatric pathology. One of the most commonly found problems associated with ASD is
Received in revised form sleep disturbances, which are estimated to affect approximately 80% of the people with ASD, not only
13 April 2021
during childhood but also in the adolescence and adult stages. Nevertheless, the relationship of these
Accepted 15 April 2021
sleep difficulties with autism severity, as well as other associated impairments such as executive func-
Available online 22 April 2021
tioning and psychiatric disorders (eg, depression), has not yet been widely studied. The main objective of
the present study was to explore the relationship between sleep disturbances, subjective measures of
Keywords:
Autism spectrum disorder
executive function, and psychiatric pathology in the ASD population. To reach that goal, a group of 89
Children participants with ASD (44 children/adolescents and 45 adults) was recruited and evaluated with self-
Adults reported measures of executive function performance and psychiatric pathology tests. Multivariate
Sleep analysis showed a significant association between sleep disturbances and psychiatric symptoms in both
Executive function ASD groups, with greater sleep disturbances predicting more severe psychiatric pathology. No significant
Psychopathology association was found with executive function in any group. Limitations included a small sample size and
lack of objective measures. Sleep problems seem to be associated with the severity of psychiatric pa-
thology throughout the lifespan, increasing the chance of developing psychiatric symptoms when they
were present. Improving sleep quality in ASD at all ages may result in preventing and/or decreasing
psychiatric pathology in this population.
© 2021 Elsevier B.V. All rights reserved.

* Corresponding author. Department of Psychiatry, Hospital Universitari Vall d’Hebron, Barcelona, Catalonia, Spain.
E-mail address: lgisbert@vhebron.net (L. Gisbert Gustemps).
1
These authors share first authorship.

https://doi.org/10.1016/j.sleep.2021.04.022
1389-9457/© 2021 Elsevier B.V. All rights reserved.
L. Gisbert Gustemps, J. Lugo Marín, I. Setien Ramos et al.
1. Introduction
The autism spectrum disorder (ASD) is one of the most
common neurodevelopmental disorders, with a prevalence of up
to 1 out of 68 children [1]. It is characterized by core deficits in
social communication and restricted interests, with repetitive be-
haviors [2]. Although ASD is defined as a neurodevelopmental
disorder because the symptoms appear within the first 3 years of
life, it is generally considered a lifelong disorder with negative
consequences for academic, work, social, and economic perfor-
mances and life quality [3].
Co-occurring mental health conditions have been frequently
reported in individuals with autism, with up to 70% of people with
autism are diagnosed as having at least one, and almost 50% are
diagnosed as having multiple co-occurring mental health condi-
tions [4-6]. Studies involving the pediatric population show
attention deficit hyperactivity disorder (ADHD), behavioral disor-
der, and anxiety disorders as the most prevalent co-occurring dis-
orders at these ages [4,7,8] whereas, when referring to adulthood,
besides ADHD and anxiety disorders, mood disorders are also
common [6,9,10]. In a recent review including studies of adults and
children, the co-occurring mental health conditions more
frequently reported in people with ASD were: ADHD (28%); anxiety
disorders (20%), sleep-wake disorders (12%), disruptive impulse-
control and conduct disorders (12%), depressive disorders (11%),
obsessive-compulsive disorder (5%), bipolar disorders (5%), and
schizophrenia spectrum disorders (4%) [5].
Regarding sleep disorders in the ASD population, studies show
high prevalence rates, reaching 86% [11-14] in childhood. These
difficulties are reported lifelong and, although the prevalence is
not so well established in adults, recent studies indi-
cate a prevalence range between 50 and 65% [15-18]. Two recent
meta-analyses of adults [19] and children [20], respectively,
reached consistent conclusions in both age groups regarding
sleep in ASD. In adulthood, the main difficulties in people with
ASD included longer sleep onset latency (SOL), lower sleep effi-
ciency (SE), and increased wake after sleep onset (WASO) [19].
These results were supported by subjective, polysomnographic,
and actigraphic data and are consistent with those of the meta-
analytic synthesis in children with ASD [20]. The main difference
was that children with ASD and controls did not differ in subjective
measures and actigraphy of SE, but they did so in polysomno-
graphic data. The authors suggest, among others, the possibility
that the sample sizes of the included studies could partially
explain these differences, as the results did not differ in direc-
tionality but rather, in significance [19].
The ongoing debate on the possible causes of sleep disorders in
ASD is open to different possible etiological explanations. Sleep
disruption might be a direct result of the ASD condition, as autism
severity is associated with poor sleep quality [17,21]. Biological
factors such as the genetically determined disruption of melatonin
pathways, which has been reported in the ASD condition [20],
might also be related. Frequently associated co-occurring psychi-
atric disorders in ASD, like ADHD and anxiety disorders in children
[22,23] and ADHD, anxiety, and mood disorders in adults [24-26],
have been shown to impact sleep. Moreover, medications known to
treat medical and behavioral conditions related to ASD, such as
stimulants, antipsychotics, and serotonin reuptake inhibitors
(SSRIs), may also disrupt the sleep-wake cycle in ASD [19,27].
Environmental factors like employment status [28,29], exposure to
blue light [30], and family environment [31] could also play a role in
sleep disorders in ASD.
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Sleep Medicine 83 (2021) 106e114
1.1. Sleep and psychiatric symptoms in ASD
Regarding disrupted sleep consequences, an impact is noted
both in the general population and in people with ASD. In typical
development, research consistently finds that children with sleep
problems are at risk for a host of internalizing and externalizing
symptoms [32]. In the adult population, the evidence shows link-
ages between sleep quality (SQ), and perceived stress, as well as
between SQ and positive and negative affect. Whereas poor sleep
accentuates negative affect (eg, anger or nervousness) and inhibits
positive emotions, good sleep promotes positive affect (eg, interest
or attentiveness) and protects from negative emotions. Positive
emotions themselves also protect the individual from the harmful
consequences of stress [33]. Thus, sleep may be crucial for
emotional processing, dealing with stress, and overall adequate
daily functioning. Specifically, in individuals with ASD, sleep
disruption can have potentially serious consequences [23], both
behavioral and cognitive. From the behavioral point of view, recent
research of youth has shown that insufficient sleep exacerbates the
severity of core ASD symptoms (eg, repetitive behaviors, social and
communication difficulties) [34,35] as well as other maladaptive
behaviors (eg, self-injury, tantrums, and aggression) [12,23].
Several studies have found that children with ASD and sleep dis-
turbances were more likely to engage in aggressive behaviors,
internalizing, externalizing, and total behavioral problems
compared to those without sleep problems [12,36]. In a study in
preschool children (3e5 years) with pervasive developmental dis-
orders, the highest association was found between sleep problems
and parents’ ratings of hyperactive, inattentive, and oppositional
behaviors [34] To date, most research has focused on children, with
the relationship between sleep profiles and behavioral problems in
adult individuals with ASD being understudied [23].
1.2. Sleep and executive functioning in ASD
From the cognitive point of view, sleep problems have been
associated in the general population with impairments in academic
or occupational achievement and neuropsychological abilities,
including executive functions [37]. The term “executive functions”
refers to a set of cognitive processes that are involved in the control
and coordination of willful action towards future goals states [38].
The prefrontal cortex appears to be pivotal for carrying out many of
these higher and more complex cognitive processes’ functioning
[39] and, based on evidence from neuroimaging and cognitive
studies, it has been suggested that the prefrontal cortex may be
particularly vulnerable to the effects of sleep loss or disruption due
to its extensive use during normal waking [40].
Because of the documented relationship between sleep and
daytime cognitive performance in typical development, children
and adults with neurodevelopmental disorders, such as ASD, with
sleep disturbances might be at risk for difficulties in executive
functioning. This relationship has nonetheless been underexplored
in autism, and results from the scarce evidence are mixed.
Regarding the pediatric population, Reynolds and colleagues [21]
showed that parents’ reports of problematic sleep behaviors were
significantly associated with academic performance, intellectual
functioning, and executive functioning after controlling for the
severity of ASD, ADHD, and internalizing symptoms. However,
Maski et al. [41] found that sleep, though disrupted, still effectively
stabilized memory in children with ASD, although to a lesser de-
gree than in control participants. In a study with young adults
with ASD, the authors found a correlation between markers of
L. Gisbert Gustemps, J. Lugo Marín, I. Setien Ramos et al.
poor sleep and declarative memory but not with working memory
and sustained attention, as they had predicted [42]. Research is
needed to better clarify the impact of poor sleep on executive
functioning in autism.
1.3. The present study
Despite the high prevalence and severe effects of sleep distur-
bances in people with ASD, to date, most research has focused on
the behavioral domain in children and adolescents, whereas the
effects on the cognitive domain and/or in the adult population have
been neglected. Furthermore, little is known about how sleep in
ASD changes over time, and how these changes affect the in-
dividual's functioning.
In this context, we conducted a study to investigate the conse-
quences of sleep difficulties on the mental health and executive
functioning among children and adults with ASD. Our primary aim
was to determine how sleep difficulties may be related to psychi-
atric symptoms in children and adults with ASD. Within this aim,
we hypothesized that problematic sleep behaviors would predict
higher scores on psychopathology measures. Our second aim was
to assess the association between sleep and executive functioning.
We expected that greater severity of problematic sleep behaviors
would predict increased executive functioning difficulties.
2. Method
2.1. Participants
The study sample consisted of 89 participants with ASD,
44 children/adolescents (<18 years) and 45 adults (
18 years).
Recruitment was conducted in the Programa de Atencio  n Integral al
Trastorno del Espectro Autista (PAITEA [Program of Comprehensive
Care of Autism Spectrum Disorders]) at the Universitari Vall d’He-
bron Hospital. Inclusion criteria were a DSM-5 diagnosis of ASD
confirmed through the Autism Diagnostic Interview-Revised (ADI-
R) [43], and/or the Autism Diagnostic Observation Schedule (ADOS-
2) [44], and participants' agreement to take part in the study. A full
scale IQ below 70 in the participant with ASD, as measured with
standardized instruments, and language and cognitive barriers in
respondents (caregivers and ASD adults), as determined by clinical
judgment, were established as exclusion criteria.
2.2. Instruments
Sociodemographic and clinical variables were collected via
medical records. These were as follows: age, sex, pharmacolog-
ical treatment, and concomitant ADHD. ASD severity was deter-
mined with screening instruments, that is, the ADI-R for the child/
adolescent group and the Autism Quotient Short Form [45] for the
adult group (see details below).
The evaluation instruments were self-informed and parent-
reported questionnaires frequently used in clinical practice,
which measured sleep disturbances, executive function problems,
and psychiatric symptoms.
2.2.1. Child/adolescent group
2.2.1.1. Sleep. The Sleep Disturbance Scale for Children (SDSC [46];
is a 26-item instrument to assess sleep in children and adolescents
aged 3e18 years. It differentiates between conditions such as dis-
orders in initiating and maintaining sleep, respiratory disorders,
sleep arousal, sleep-wake transition disorders, excessive sleepiness,
restless legs syndrome/periodic limb movement syndrome/growth
pains, and sleep hyperhidrosis. Caregivers rate the frequency of
each behavior on a 5-point Likert scale (1 ¼ Never; 2 ¼ Occasionally
108
Sleep Medicine 83 (2021) 106e114
(once or twice per month or less); 3 ¼ Sometimes (once or twice per
week; 4 ¼ 3 or 5 times per week; 5 ¼ Always (daily)). A total score of
39 or above is considered clinically significant, with higher scores
suggesting greater sleep problems. This instrument is consid-
ered reliable and valid, as high internal consistency (Cronbach's
alpha ¼ 0.79) and adequate reliability (r ¼ 0.71) were found in the
original validation [46,47]. Several studies have used the SDSC in
the ASD population [48,49], showing its usefulness in the screening
of sleep disturbances in children with ASD.
2.2.1.2. Psychiatric symptoms. The Child Behavior Checklist 6:18
(CBCL 6e18 years old [50]; is a caregiver-reported measure that
assesses specific internalizing and externalizing problem behaviors.
Caregivers rate the frequency of each behavior on a 3-point Likert
scale (0 ¼ Not True; 1 ¼ A Little, or Sometimes True; 2 ¼ Very True,
or Often True). The scores are added and converted into T-scores
(M ¼ 50, SD ¼ 10) on the analytically derived Syndrome scales, with
higher scores suggesting greater behavioral problems. The Syn-
drome scales combine to form a composite score of Internalization
Problems, Externalization Problems, and Total Problems. A T-score
of 65 (or above) is generally considered clinically significant. Good
psychometric properties have been reported within ASD groups
[51], with higher than acceptable reliability coefficients (l-2 > 0.70)
on all the clinical scales [52]. This questionnaire has been widely
reported for use with children and adolescents with ASD [53,54].
2.2.1.3. Executive function. The Behavioral Rating Inventory of Ex-
ecutive Function (BRIEF-2 Family report [55]; is a questionnaire
completed by a relative/caregiver, which assesses executive func-
tions depending on the degree of the observed frequency of a
series of behaviors in the child or adolescent. It consists of 63 items
that are answered on a frequency scale (never, sometimes, and
frequently). The BRIEF-2 Family provides scores on several scales
related to executive functions: inhibition, self-monitoring, switch-
ing, emotional control, initiative, working memory, planning, or-
ganization, and task monitoring. Their combination gives rise to the
four indices of behavioral, emotional, cognitive, and global regu-
lation of executive functions. The raw scores are transformed into
age-corrected T-scores. A score greater than 70 on any of the scales
indicates clinically significant difficulties. Very high internal con-
sistency has been reported for the Index and Composite scores
(Cronbach's alpha ¼ 0.90 - 0.97) as well as for test-retest reliability
(r > 0.80) [56]. It has been shown to be adequate for the screening
of executive difficulties in the ASD population [57].
2.2.1.4. Autism severity. The ADI-R [43] is a clinician-administered
interview developed for evaluating ASD in early life stages. Scores
are classified into four categories: Reciprocal Social Interaction,
Communication (verbal, non-verbal), Restricted Repetitive and
Stereotyped Behaviors, and Abnormal Development. The sum of
the scores of these four subscales was considered as a global
measure of the severity of ASD in the present study.
2.2.2. Adult group
2.2.2.1. Sleep. The Pittsburgh Sleep Quality Index (PSQI [58]; is
a self-report questionnaire developed to measure sleep quality
in clinical populations. The PSQI measures seven components of
sleep: sleep quality, latency, duration, habitual sleep efficiency, use
of medications, disturbance, and daytime dysfunction. Participants
rate the items on a scale ranging from 0 to 3, with positive scores
indicating a greater amount of sleep dysfunction. The PSQI has been
tested both in the general population and in specific psychiatric
populations and found to be accurate in distinguishing good and
bad sleep patterns [59]. A score greater than 5 is considered clini-
cally significant, with higher scores suggesting greater sleep
L. Gisbert Gustemps, J. Lugo Marín, I. Setien Ramos et al.
problems. A good overall reliability coefficient was found in the
original validation (Cronbach's alpha ¼ 0.83) It has been used to
screen sleep disturbances in adults with ASD [17,60].
2.2.2.2. Psychiatric symptoms. The Symptom Checklist 90 Revised
(SCL-90-R [61]; is a multidimensional 90-item self-report ques-
tionnaire developed to screen for a range of psychopathological
symptoms in the adult population. The items refer to the occur-
rence during the preceding week, and scores can be organized into
nine subscales: Somatization, Obsessive-Compulsive, Interpersonal
Sensitivity, Depression, Anxiety, Hostility, Phobic Anxiety, Paranoid
Ideation, and Psychoticism. The Global Severity Index (GSI) is the
summary measure of the nine subscales. A T-score of 60 or above is
considered clinically significant. Psychometric properties, including
internal consistency, test-retest reliability, and convergent/diver-
gent validity, are good to very good [62], with an excellent global
Cronbach coefficient (Cronbach's alpha ¼ 0.98) reported in the
Spanish population (Bald [63]. This questionnaire has been used in
populations with ASD to measure psychopathological status
[4,64,65].
2.2.2.3. Executive function. The Behavior Reporting Inventory Ex-
ecutive Function - Adult version (BRIEF-A [66]; is a 75-item self-
administered questionnaire that captures the daily difficulties
related to executive functions in the adult population. The BRIEF-A
provides scores on several scales related to executive functions:
Inhibition, Self-Monitoring, Switching, Emotional Control, Initia-
tive, Working Memory, Plan/Organize, Organization of Materials,
and Task Monitoring. The results produce a composite index score,
the Global Executive Composite, and two subscript scores, the
Behavioral Regulation Index and the Metacognition Index. The raw
scores are transformed into age-corrected T-scores. A score equal to
or greater than 60 on any of the scales indicates clinically significant
difficulties. For the present study, the informant version of the
BRIEF-A was chosen to resemble the measure used in the Child/
Adolescent group. Validity and reliability studies have been con-
ducted with the BRIEF-A in different population groups, finding
good psychometric properties [67,68]. Reliability was higher for the
informant than for the self-report form, ranging for the clinical
scales from 0.80 to 0.93 in the normative samples and from 0.85 to
0.95 in mixed clinical samples [69]. It has also been shown to be
useful to identify executive difficulties in adults with ASD [70].
2.2.2.4. Autism severity. The AQ-Short [45] is a 28-item self-
administered questionnaire that assesses the presence of ASD-
related characteristics in adults. It has been widely used as a
measure of the severity of autism in adults with ASD [71,72]. A good
reliability coefficient was found for the non-clinical Spanish pop-
ulation (Cronbach's alpha ¼ 0.88) and acceptable reliability for the
adult group with ASD (Cronbach's alpha ¼ 0.79) [73]. The total
score ranges from 28 to 112 points, with a score equal to or greater
than 63 suggesting ASD in the Spanish validation [73].
2.3. Procedure
Potential participants were recruited routinely via clinical
practice and were asked to give their written consent to participate.
For the Child/Adolescent group, caregivers completed the assess-
ment measures whereas, in the Adult group, the adults with ASD
filled in the questionnaires, except for the BRIEF-A, which was
completed by an informant. The evaluation instruments were
delivered in person, and the participants completed them at home.
After completion, they were requested to return the questionnaires
during any of the next programmed visits to our Unit.
109
Sleep Medicine 83 (2021) 106e114
2.4. Statistical analysis
Once the evaluation instruments were returned, statistical
analyses were performed with the statistic “R” software (R version
4.0.0 (2020-04-24, Copyright 2015 The R Foundation for Statistical
Computing). The qualitative variables were described as number
and percentage. The quantitative variables were described as
mean and standard deviation or median and interquartile range
(IQR). Confidence intervals for all analyses were established at 95%.
A set of regression analyses were conducted to study the rela-
tionship between sleep measures (predictors) and executive
function and psychiatric symptoms (outcomes). For this purpose,
only total scores were considered both for sleep and clinical
measures. The statistical approach was established as follows: (i) A
univariate model was built with the predictors (sleep measures)
for each age group. Also, demographic (age and sex) and data from
clinical records (ADHD concomitance, pharmacological treatment,
and ASD severity score) were included to study significant re-
lationships with the outcome variables (executive function and
psychiatric symptoms); (ii) The variables associated with signifi-
cant changes in the univariate analysis (p < 0.05) and the clinically
relevant variables were included in a multivariate linear regression
model.
2.5. Ethics
Ethics approval was obtained from Hospital Universitari Vall
d’Hebron Ethics Committee of Research and Medication.
3. Results
3.1. Descriptive data
Table 1 shows the results of the sociodemographic and clinical
data, and the mean scores in the main studied variables. The mean
age of the participants was 10.5 years (SD ¼ 2.8) and 30.4 years
(SD ¼ 13.5) for the Child/Adolescent and Adult groups, respectively.
In both ASD groups, male participants were predominant (84.1%
and 75.6%, respectively). Also, almost half of the Child/Adolescent
participants were on medication (45.5%), whereas in the Adult
group, two-thirds of the whole sample was medicated (66.7%). A
high ADHD concomitance was found in both age populations
(54.5% and 64.5%, respectively). The mean total scores for all
questionnaire variables exceeded the clinical cutoff scores.
3.2. Child/adolescent group
3.2.1. Univariate analysis
The results of the univariate linear regression analysis found the
following variables reaching significance for the CBCL Total Score:
Sex (b ¼ 6.25, 95% CI [-11.81, 0.69], p ¼ 0.028), ADHD concom-
itance (b ¼ 5.62, 95% CI [1.66, 9.58], p ¼ 0.007), Pharmacological
Treatment (b ¼ 4.93, 95% CI [0.88, 8.97], p ¼ 0.018), and SDSC Total
Score (b ¼ 0.27, 95% CI [0.13, 0.41], p < 0.001). None of the variables
reached significance in the univariate linear regression analysis for
the BRIEF-2-Family Global Executive Composite (See Appendix 1).
3.2.2. Multivariate analysis
Multivariate linear regression analysis was conducted with the
studied variables, resulting as follows: Sex (b ¼ 4.96, 95% CI
[-9.5, 0.43], p ¼ 0.033), ADHD concomitance (b ¼ 3.65, 95% CI
[-0.08, 7.38], p ¼ 0.055), Pharmacological Treatment (b ¼ 1.8, 95% CI
[-1.96, 5.56], p ¼ 0.34), and SDSC Total Score (b ¼ 0.24, 95% CI [0.11,
0.36], p ¼ 0.001) (Table 2).
L. Gisbert Gustemps, J. Lugo Marín, I. Setien Ramos et al. Sleep Medicine 83 (2021) 106e114

Table 1
Demographic and clinical statistics.

Child/Adolescent (n ¼ 44) Adult (n ¼ 45)

Mean (SD) Mean (SD)

Age (mean ± SD) 10.5 ± 2.8 Age (mean ± SD) 30.4 ± 13.5
Sex (male %) 84.1 Sex (male %) 75.6
Pharmacological treatment (%) 45.5 Pharmacological treatment (%) 66.7
ADHD concomitance (%) 54.5 ADHD concomitance (%) 64.4
Sleep measures
SDSC PSQI
Disorders of initiating and maintaining sleep 14.5 (4.4) Subjective sleep quality 1.4 (0.7)
Restless legs syndrome 2.3 (1.5) Sleep latency 1.6 (1)
Sleep breathing disorders 4.6 (2.4) Sleep duration 0.7 (1.1)
Disorders of arousal 4.3 (1.7) Sleep efficiency 1 (1.1)
Sleep-wake transition disorders 12.3 (4.5) Sleep disturbances 1.5 (0.7)
Disorders of excessive somnolence 10 (4) Use of sleep medication 1 (1.3)
Sleep hyperhidrosis 3.9 (2.7) Daytime dysfunction 1.2 (0.8)
SDSC Total Score 49.5 (13.2) Global PSQI Index 8.1 (3.6)
Executive Function Measures
BRIEF Parent BRIEF-A (informant)
Inhibition 67.3 (11.6) Inhibit 57.1 (11.9)
Self-Monitoring 70.2 (10.8) Self-Monitor 56.8 (11.9)
Shifting 81.4 (14) Plan/Organize 63.9 (11.8)
Emotional Control 67.2 (11.1) Shift 62.9 (12.9)
Initiation 72 (9.7) Initiate 61.3 (10.4)
Working Memory 71.2 (9.5) Task Monitor 63.1 (12)
Planning 69.9 (8.8) Emotional Control 58.4 (11.1)
Organization 65.9 (14.5) Working Memory 65.3 (13.6)
Task Monitoring 64.8 (8.6) Organization of Materials 56.4 (10.7)
Behavioral Regulation Index 70.2 (11) Behavioral Regulation Index 59.7 (11.3)
Emotional Regulation Index 77.2 (11) Metacognition Index 63.3 (10.9)
Cognitive Regulation Index 72.4 (9.6) Global Executive Composite 62.4 (10.9)
Global Executive Composite 76.8 (10.5)
Psychiatric Symptoms
CBCL Parent SCL-90-R
Anxious/Depressed 67.2 (10.7) Somatization 56.7 (12.8)
Withdrawn/Depressed 69.3 (8.6) Obsessive-Compulsive 66 (8.6)
Somatic Complaints 57 (6.2) Interpersonal Sensitivity 65.2 (11.1)
Social Problems 69.3 (10.4) Depression 63.2 (12.2)
Thought Problems 68.5 (8.7) Anxiety 61 (11.5)
Attention Problems 75.1 (9.4) Anger-Hostility 58.4 (10.8)
Rule-Breaking Behavior 59.4 (7.8) Phobic Anxiety 61.5 (13.5)
Aggressive Behavior 62.5 (11.5) Paranoid Ideation 63.4 (10.9)
CBCL Internalizing total score 68.1 (8) Psychoticism 63.8 (11.6)
CBCL Externalizing total score 61.1 (8.7) Global Symptoms Index 64.6 (11.5)
CBCL Total score 67.1 (7)
Autism severity
ADI-R Sum of subscales 34.7 (12.3) AQ-Short Total Score 75 (15.1)

3.3. Adult group
3.3.1. Univariate analysis
The results of the univariate linear regression analysis found the
following variables reaching significance for the SCL-90-R Global
Symptoms Index: PSQI Global Index (b ¼ 1.48, 95% CI [0.61, 2.34],
p ¼ 0.001), and AQ-Short Total Score (b ¼ 0.35, 95% CI [0.15, 0.56],
p ¼ 0.001). None of the variables reached significance in the uni-
variate linear regression analysis for the BRIEF-A Global Executive
Composite (See Appendix 1).
3.3.2. Multivariate analysis
Multivariate linear regression analysis was conducted with the
studied variables, resulting as follows: PSQI Global Index (b ¼ 1.14,
95% CI [0.29, 1.99], p ¼ 0.009) and AQ-Short Total Score (b ¼ 0.27,
95% CI [0.07, 0.48], p ¼ 0.01) (Table 3).
4. Discussion
The main objective of the present study was to explore the
relationship between sleep disturbances and executive functions
and psychiatric symptoms in children/adolescents and adults with
110
ASD without intellectual disability. The results suggest that sleep
difficulties predict psychiatric pathology in both age groups. No
association between sleep problems and executive function per-
formance was found. These results add value to previous literature
on the association of sleep disturbances and psychiatric symptoms/
executive functioning. Moreover, to our knowledge, this is the first
study using sleep disturbances as a predictor of psychiatric symp-
toms and executive functioning in adults with ASD without
accompanying intellectual impairment.
4.1. Sleep and psychiatric symptoms
Psychiatric disorders seem to be related to sleep difficulties in
both age groups of participants with ASD. In the case of the Child/
Adolescent group, our results resemble previous literature on the
association of sleep problems and emotional/behavioral disorders
in children and adolescents with ASD [74,75]. Malow et al. [76]
found that children with ASD with parent-reported sleep distur-
bances obtained higher scores on the affective domain of the CBCL
than children with ASD without sleep problems. More recently,
Johnson et al. [77] reported similar findings, with “poor sleeper”
children with ASD obtaining higher scores on the irritability,
L. Gisbert Gustemps, J. Lugo Marín, I. Setien Ramos et al.
Table 2
Regression analysis for the outcome variable (CBCL Total Score) in the Child/
Adolescent group (n ¼ 44).
Variables Estimate (b) CI (lower) CI (upper) p
(Intercept) 53.4 46.79 60.02
Sex (Female) 4.96 9.5 0.43
ADHD concomitance (Yes) 3.65 0.08 7.38
Pharmacological Treatment (Yes) 1.8 1.96 5.56
SDSC Total Score 0.24 0.11 0.36
R2 46.54
Table 3
Regression analysis for the outcome variable (SCL-90-R Global Symptoms Index) in
the Adult group (n ¼ 45).
Variables Estimate (b) CI (lower) CI (upper)
(Intercept) 34.91 19.89 49.93
Global PSQI Index 1.14 0.29 1.99
AQ-Short Total Score 0.27 0.07 0.48
R2 33.18
hyperactivity, social withdrawal, and stereotypical behaviors of
the CBCL. When comparing children/adolescents with ASD with
their peers without ASD, a greater presence of sleep disturbances
was found in the former [78], but the association of sleep disor-
ders and psychiatric symptoms has also been reported in typically
developing children/adolescents [79-81]. Addressing specific
sleep disorders, arousal disorders and excessive somnolence
related to greater thought and behavioral problems have been
reported in children/adolescents with ASD [82]. Overall, these
findings suggest that improving sleep quality may decrease
emotional and behavioral symptoms in children/adolescents with
ASD. In this regard, some intervention studies have addressed this
issue [83,84]. Malow et al. [85] reported that a brief cognitive-
behavior intervention with the caregivers of children with ASD
was effective in reducing their scores on the CBCL Anxiety/
Depression, Withdrawal, ADHD, and Attention scales. Also,
Papadopoulos et al. [86] found an improvement in behavioral
problems after sleep behavioral intervention, which was main-
tained for up to 6 months. Future studies on sleep intervention
with children/adolescents with ASD should include psychiatric
symptoms measures to evaluate the impact of sleep treatment on
behavioral and emotional disorders. Studies must also control for
other significant variables, especially concurrent ADHD and
pharmacological treatment, both of which accounted for much of
the variance in our regression model (see Table 2).
For adults with ASD, sleep disturbances also seem to predict a
worse outcome at the psychopathological level. Studies addressing
sleep problems’ association with psychiatric symptoms, such as
anxiety and depression, have found a high co-occurrence between
the two disorders in the general adult population [87,88]. This
relationship has been scarcely explored in adults with ASD
[18,23,89]. One study using both subjective and objective measures
found that adult participants with ASD and co-occurring psychi-
atric symptoms had a higher total sleep time when compared to
adults with ASD without accompanying psychiatric symptoms [60].
Also, Jovevska et al. [17] reported poorer sleep quality in young and
middle-aged adults with ASD when compared with typically
developed peers, with females with ASD being more vulnerable to
developing sleep problems. Of interest, co-occurring mental health
conditions predicted worse sleep behavior in adult groups both
with and without ASD. More studies are needed to clarify this as-
sociation between sleep disturbances and mental health. Studies on
sleep intervention in adults with ASD, including pharmacological
[90] and non-pharmacological treatment [91], have not reported
Sleep Medicine 83 (2021) 106e114
collateral effects on psychiatric symptoms. Future research designs
must include psychopathology measures to evaluate this outcome.
Regarding differences between the Child/Adolescent and Adult
groups in the regression analyses, we highlight the differences in
<0.001 the evaluation instruments between the two groups. Whereas the
0.033 Child/Adolescent group evaluation was based on parent-report
0.55 instruments, in the Adult group, it consisted of self-report mea-
0.34
sures. Moreover, in the case of the autism severity instruments, we
0.001
note that the ADI-R is a clinician-administered interview that
covers the early developmental years of the participant with
ASD, whereas the AQ-Short is a self-administered questionnaire
addressing the current severity of the autistic traits. Also, other
factors such as differences in the score range and respondent bias
(eg, insight) may have affected the results found in these analyses.
p
4.2. Sleep and executive function
<0.001
0.009
0.01 Regarding executive function, our results indicate no relation-
ship with sleep disturbances, as none of the measures was signif-
icant in either age group of participants with ASD. Prior studies of
sleep problems and executive function in populations with ASD
have obtained inconsistent results. Reynolds et al. [21] found that
sleep disturbances did not predict executive functioning as
measured with the BRIEF Metacognition and Behavioral Regulation
Indices in children with ASD. Cremone-Caira et al. [92] found that
sleep problems and executive function performance predicted
ADHD severity in children with ASD, although sleep did not
mediate or moderate the relationship between executive func-
tioning and ADHD symptoms. Calhoun et al. [93], found working
memory deficits to be associated with learning problems in ado-
lescents with ASD and sleep disturbances but not among those
without sleep difficulties. A recent study found sleep disturbances
to be related to the BRIEF scores in children with ASD, ADHD, and in
typically developing peers [94]. Interestingly, this association dis-
appeared after accounting for anxiety in the group with ASD but
not in the group with ADHD, indicating that executive function
impairment is better explained by anxiety symptoms in the ASD
group than by sleep quality. These discrepancies throughout prior
literature may be due to the conceptualization of executive function
being too broad, with self-report measures that are incapable of
capturing naturalistic functioning. Future studies should include an
objective evaluation of executive functioning and better define the
concept of executive function to relate it to sleep problems and to
capture the difficulties observed in daily functioning in participants
with ASD.
Sleep problems have been reported to be related to poorer ex-
ecutive functioning in adult general population [95]. Studies
exploring this relationship in adults with ASD are limited. One
study correlated polysomnographic outcomes with a set of cogni-
tive non-verbal tasks, finding significant association between var-
iables indicating poor sleep and selective attention, sensory-motor
procedural memory and cognitive procedural memory [42]. More
studies must be conducted to shed light on this issue.
4.3. Limitations
Although our results are promising, a set of limitations should
be considered. First, the small sample size and sampling method
may compromise the generalization of the results. Also, when
measuring sleep problems and executive functioning, not only
subjective measures capturing self-perceived difficulties should be
considered, but also objective measures, such as actigraphy or
polysomnography in the case of sleep disturbances, and neuro-
psychological tools (eg, Wisconsin Card Sorting Test) to measure
executive functioning would be of interest. Also, concerning age, a
111
L. Gisbert Gustemps, J. Lugo Marín, I. Setien Ramos et al.
wide heterogeneity can be observed in sleep concerns through
different developmental stages [17]. In our study, the division made
between children/adolescents and adults may be insufficient to
capture age-related sleep problems. Although this aim was beyond
the scope of the present study, further research should attempt
to establish age-specific sleep disturbance profiles to achieve
broader knowledge about this matter. Finally, more ASD-specific
instruments for the evaluation of sleep disturbances are needed
to establish profiles and relate them to the development or main-
tenance of psychiatric symptomatology.
4.4. Clinical implications
Our findings support the association of sleep disturbances and
psychiatric symptoms, with greater sleep problems increasing the
severity of psychiatric symptoms both in children/adolescents and
adults with ASD. Thus, sleep intervention might improve not only
sleep quality but also ameliorate the psychiatric impairment in
these population groups. Sleep intervention should be included in
the therapeutic approach to patients with ASD.
4.5. Future directions
More studies are needed to explore the relationship between
sleep difficulties and mental health status, determining which
sleep difficulties are related to certain psychiatric symptoms. Also,
in-depth studies addressing the association of executive function
with sleep problems are warranted. For this purpose, objective
measures evaluating real-based executive functioning must be
included in the research methods.
CRediT authorship contribution statement
Laura Gisbert Gustemps: Conceptualization, Methodology,
Formal analysis, Investigation, Resources, Writing e original draft.
Jorge Lugo Marín: Conceptualization, Methodology, Formal anal-
ysis, Investigation, Resources, Writing e original draft. Imanol
Setien Ramos: Conceptualization, Methodology, Formal analysis,
Investigation, Resources, Writing e review & editing. Pol Iban ~ ez
Jimenez: Conceptualization, Methodology, Writing e review &
editing. Odile Romero Santo-Toma s: Conceptualization, Writing e
review & editing. María Jose  Jurado Luque: Conceptualization,
Writing e review & editing. Pura Ballester Navarro: Conceptuali-
zation, Writing e review & editing. Antoni Esteve Cruella: Writing
e review & editing. Emiliano Díez Villoria: Formal analysis,
Writing e review & editing. Ricardo Canal Bedia: Writing e review
& editing. Josep Antoni Ramos Quiroga: Writing e review &
editing, Supervision.
Acknowledgments
The statistical analysis was carried out in the Statistics and
Bioinformatics Unit (UEB) Vall d’Hebron Hospital Research Institute
(VHIR). The authors also want to thank Dr. Virginia Navascue s for
her diligent proofreading of this paper.
Conflict of interest
The authors declare no conflict of interest regarding any of the
results of this study.
The ICMJE Uniform Disclosure Form for Potential Conflicts of
Interest associated with this article can be viewed by clicking on the
following link: https://doi.org/10.1016/j.sleep.2021.04.022.
112
Sleep Medicine 83 (2021) 106e114
Appendix A. Supplementary data
Supplementary data to this article can be found online at
https://doi.org/10.1016/j.sleep.2021.04.022.
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