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Sleep Med. Author manuscript; available in PMC 2019 April 01.
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Published in final edited form as:


Sleep Med. 2018 April ; 44: 61–66. doi:10.1016/j.sleep.2018.01.008.

Exploring Sleep Quality of Young Children with Autism


Spectrum Disorder and Disruptive Behaviors
Cynthia R. Johnsona, Tristam Smithb, Alexandra DeMandc, Luc Lecavalierd, Victoria
Evansa, Matthew Gurkaa, Naomi Swiezye, Karen Bearssf, and Lawrence Scahillg
aUniversity of Florida, Department of Clinical & Health Psychology
bDepartment of Pediatrics, University of Rochester
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cUniversity of Pittsburgh
dNisonger Center & Ohio State University
eIndiana University
fSeattle Children’s Hospital & University of Washington
gMarcus Autism Center, Children’s Healthcare of Atlanta & Emory University 1920 Briarcliff Road
Atlanta

Abstract
Background and purpose—Sleep disturbances in autism spectrum disorder (ASD) are
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common and may impair daytime functioning and add to parental burden. In this well
characterized sample of young children with ASD and disruptive behaviors, we examine the
association of age and IQ in sleep disturbances using the Child Sleep Habits Questionnaire
modified for ASD (CSHQ-ASD). We also test whether children with poor sleep have greater
daytime behavioral problems than those with better sleep. Finally, we examine whether parental
stress is higher in children with greater disruptive behaviors and sleep disturbances.

Participants and methods—Participants were 177 with complete data of 180 children (mean
age 4.7) with ASD who had participated in a randomized clinical trial. Parents completed the
CSHQ-ASD and several other measures at study enrollment. The sample was divided into “poor
sleepers” (upper quartile on the total score of the CSHQ-ASD) and “good sleepers” (lower
quartile) for comparisons. Analyses were conducted to evaluate group differences on age, IQ,
daytime disruptive behavior, social disability and parental stress.
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*
Corresponding Author: Cynthia R. Johnson, Ph.D., University of Florida, Department of Clinical & Health Psychology Medicine,
1225 Center Dr, Room 3130, Gainesville, FL 32610 Avenue, Pittsburgh, PA 15213, Telephone: 412 897 7435, Fax: 352 273 6156,
[email protected].
The views expressed in this article are those of the authors and do not necessarily reflect the official position of the National Institute
of Mental Health, the National Institute of Research Resources, the National Institutes of Health, or any other part of the U.S.
Department of Health and Human Services. NIMH encourages publication of results and free scientific access to data. There were no
financial conflicts of interest.
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Johnson et al. Page 2

Results—The two groups of young children with ASD, good sleepers versus poor sleepers, were
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not different on age or cognitive level. Children in the poor sleeping group had significantly higher
daytime behavioral problems including irritability, hyperactivity, social withdrawal and
stereotypical behaviors. Parents in this group reported significantly higher levels of stress.

Conclusions—The finding of no age difference between good and poor sleepers in young
children with ASD and disruptive behaviors suggests that sleep problems are unlikely to resolve as
might be expected in typically developing children. Likewise, the good and poor sleepers did not
significantly differ in IQ. These findings add strong support for the need to screen for sleep
disturbances in all children with ASD, regardless of age and cognitive level. Poor sleepers
exhibited significantly greater daytime behavioral problems and parents of children in this group
reported significantly higher levels of stress. Above and beyond the co-occurring disruptive
behavior, poor sleep quality appears to pose substantial additive burden on child and parents..
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Introduction
Autism Spectrum Disorder (ASD) is characterized by social communication deficits,
restrictive interests and repetitive behavior (1) affecting 6.2 – 14.7 per 1000 children
depending on study design and sample ascertainment (2, 3). In addition to these core
diagnostic features, many children with ASD have co-occurring problems such as tantrums,
aggression, self-injury, hyperactivity, anxiety, depression, and sleep disturbance (4–9).
Although the etiological connections are not clear, children with ASD may have one or more
of these concomitant conditions. Sleep disturbances such as bedtime resistance, sleep-onset
association problems, delayed sleep onset, interrupted sleep and decreased total sleep time
have been reported in up to 80% of children with ASD (8–16).

The trajectory of sleep problems in typically developing (TD) children tends to be worst in
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the early preschool years and diminish over time(17). Although findings are not completely
uniform, age is not strongly related to sleep disturbances in children with ASD (18–21).
More recently, in a sample of 3–17 year olds, sleep difficulties were highest at ages 6–9 for
children with ASD during which time sleep disturbances had greatly decreased in TD
children (22). In one of the first studies to examine sleep longitudinally, sleep disturbances
emerged after 18 months and persisted through 11 years of age in children diagnostic with
ASD (23). This was in sharp contrast to the TD children in the study sample whose sleep
problems resolved in the preschool years.

In children with ASD, cognitive functioning has been proposed to play a role in sleep
problems, but the relationship is unresolved with studies offering mixed results. Although
some studies report that sleep problems are more common in children with ASD and lower
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cognitive abilities (20, 24–28) other studies have not confirmed this association (8, 14, 18,
19). Despite the inconsistencies, it is clear that sleep disturbances in children with ASD
occur across cognitive levels.

A growing literature supports links between poor sleep and behavioral and emotional
problems in children with ASD. Inattention, hyperactivity, aggression, self-injury and
anxiety are consistently more common in children with ASD and diminished sleep quality
(16, 29–32).

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Finally, sleep difficulties in children with ASD may impose additional stress on caregivers
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and foster negative attitudes toward the child (28, 33–35). Parents of children with ASD
have lower sleep quality than parents of typically developing children (36, 37), especially
when the child with ASD has sleep problems (38). Sleep problems are also associated with
maternal depressive symptoms (39).

The current study aimed to extend previous work in the area where findings thus far have
been equivocal, in a well characterized sample of young children with ASD and moderate to
severe disruptive behaviors. In this sample, we examine the role of age and IQ in sleep
disturbances. We also test whether children with poor sleep have greater daytime behavioral
problems and whether parental stress is greater in children with sleep disturbances compared
to those with ASD and adequate sleep.

Methods
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Sample
The sample consisted of 177 of the 180 children who participated in the Research Units on
Behavioral Intervention (RUBI) study (three participants had incomplete sleep data). RUBI
was a 24-week randomized controlled trial (RCT) of children ages 3–7 years of age who
were randomized to Parent Training (PT) or a Parent Education Program (PEP) (40, 41).
Eligible children were healthy, had a diagnosis of ASD, and moderate or greater severity of
disruptive as evidenced by a score of ≥ 15 on the Aberrant Behavior Checklist (ABC) and a
Clinical Global Impressions Severity (CGI-S) score of ≥ 4. Participants were on no
medication or on stable medication for at least 6 weeks and no planned changes for six
months were included. Diagnoses of Rett Disorder or Childhood Disintegrative Disorder,
any serious medical conditions or psychiatric disorder, developmental level of less than 18
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months and current or past enrollment in structured PT program were study exclusions. The
study was initiated prior to DSM-V (1). Thus, the ASD diagnoses were based on DSM-IV
criteria (42), corroborated by the Autism Diagnostic Observation Schedule (ADOS) (43, 44)
and Autism Diagnostic Interview – Revised (45). This six study sites included the Emory
University, Indiana University, Ohio State University, University of Pittsburgh, University of
Rochester and Yale University.

Study Measures
Demographics—Parents completed a demographic form at study entry.

Developmental/Cognitive functioning—The Abbreviated Battery of the Stanford-


Binet Intelligence Scales: 5th Edition(46) or the Mullen Scales of Early Learning(47) were
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used to assess each participant’s level of intellectual functioning. Most children were
assessed with the Stanford-Binet. The Mullen was used for children with limited language
skills, mental age below 3 years or children who were unable to complete the Stanford-
Binet.

Children’s Sleep Habits Questionnaire (CSHQ)(48) is a 33-item, parent-report measure


designed to screen for sleep problems in children aged 4 to 10. A subsequent study
supported the validity of the CSHQ in children as young as two years of age (49). The

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CSHQ items are rated on a 3-point scale: 3 = usually (5–7 nights per week); 2 =sometimes
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(2–4 nights per week); and 1 = never/rarely (0–1 nights per week). In addition to the
frequency ratings, a ‘yes’ or ‘no’ response to the question “is this a problem?” is included.
The summation of the frequency ratings creates the total score, with higher scores reflecting
greater sleep disturbances. The original CSHQ has 8 subscales: bedtime resistance, sleep
onset delay, sleep duration, sleep anxiety, night wakings, parasomnias, sleep disordered
breathing, and daytime sleepiness. These subscales were based on the pediatric International
Classification of Sleep Disorder (48) and subsequent factor analyses have not confirmed
these subscales psychometrically (50–52). Although the CSHQ was not developed for
children with ASD, it has been widely used to characterize sleep problems in this
population. Recently, we explored the psychometric properties of the CSHQ in a relatively
large sample of 310 children with ASD (53). The revised measure includes 27-items (six
items did not load on any factor) with five components. The subscales were labeled: 1) Sleep
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Routine Problems (9 items); 2) Insufficient Sleep (5 items); 3) Sleep-Onset Association


Problems (4 items); 4) Parasomnia/Sleep Disordered Breathing (6 items); and 5) Sleep
Anxiety (3 items). This version of the CSHQ, here after called the CSHQ-ASD, was used in
this study. For purposes of this study, we used the total sleep score of the 27-item revised
measure.

Aberrant Behavior Checklist (ABC)(54) is a 58-item parent rating scale rated on a four-point
scale from 0 (not a problem) to 3 (severe in degree). The ABC contains five subscales:
Irritability (15 items), Social Withdrawal (16 items), Stereotypic Behavior (7 items),
Hyperactivity/Noncompliance (16 items), and Inappropriate Speech (4 items). The ABC has
been validated in children with ASD(55). The Irritability, Hyperactivity, and Social
Withdrawal subscales have been used as outcomes for several RCTs in ASD(40, 56–58).
Here we were interested in the Irritability and Hyperactivity/noncompliance subscales as
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indices of disruptive behavior, Social Withdrawal subscale as a measure of social disability,


and Stereotypy as an index of repetitive movements.

Parenting Stress Index- Short Form (PSI)(59) is a 36-item measure completed by parents of
children 3 months to 10 years of age designed to assess parental stress. Each item is rated on
a 5-point scale. The PSI includes three factors: Parental Distress, Parent-Child Dysfunctional
Interaction, and Difficult Child Characteristics. Example statements include, “I feel trapped
by my responsibilities as a parent,” “Sometimes I feel my child doesn’t like me and doesn’t
want to be close to me,” and “I feel that my child is very moody and easily upset.” The PSI
has good test-retest reliability (.96) and internal consistency (.90). A total score of 88 (85th
percentile) and above is considered in the clinically significant range for parental stress. This
measure has been shown to capture parental stress associated with raising a child with ASD
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and disruptive behavior. The PSI provides insight into parents’ internal emotional state, as
well as the stress related to child behavior and parent-child interactions(60).

Data Analyses
Data analyses were conducted using PASW statistics (Version 22)(61). We divided the
sample into “poor sleepers” (upper quartile on the total score of the CSHQ-ASD) and “good
sleepers” (lower quartile) for comparisons. Descriptive statistics were calculated for the

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entire sample as well as the two groups (poor sleepers; good sleepers). Chi Square test was
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performed to determine group differences in IQ (dichotomous variable of 70 and above,


lower than 70).. T-tests were conducted to evaluate group differences on age, daytime
disruptive behavior and parental stress.

Results
Demographic information is provided in Table 1. This sample was mostly Caucasian, non-
Hispanic and parents were relatively well educated. The mean age of the study sample
(N=177) was 4.7 ± 1.14 years. There were no age differences between the good sleepers (n=
52 with a CSHQ-ASD score in lower quartile) and poor sleepers (n= 46 with a CSHQ-ASD
score in upper quartile) (t=0.58; p = 0.57). In both good and poor sleep groups, over 70% of
participants had an IQ of 70 or above, and there was no significant difference in good
sleepers compared to poor sleeper on this dichotomous IQ variable (≥ 70; <70) (χ2=0.03, p
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= 0.87). In contrast, poor sleepers had significantly higher scores on the ABC Irritability,
Hyperactivity, Stereotypy and Social Withdrawal subscales. Likewise, all the subscales of
the PSI and the PSI total score were significantly higher in the poor sleeper group compared
to children in the good sleeper group.

Discussion
This study examined sleep in a sample of young children (age 3 to 7 years) with ASD with
moderate to severe disruptive behavior. The well characterized sample included participants
from a randomized trial of parent training versus parent education (40, 41). Pre-treatment
primary caregivers (mothers in most cases) completed numerous paper and pencil measures
at study enrollment. For this study we stratified the sample in order to compare children who
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had sleep disturbances to children who did not. Sleep disturbance was measured on the 27-
item CSHQ-ASD. This modified version has fewer items than the original 33-item CSHQ
and has a different factor structure.(53).

We found no evidence of an association between age and sleep disturbance in our sample.
This finding should be interpreted with caution in view of the restricted age range of 3–7
years. However, this range does include the period in which TD children show the sharpest
decline in sleep problems(23). Because our finding suggests that sleep problems are unlikely
to resolve as might be expected in similar ages of TD children, early treatment for sleep
disturbances for young children with ASD may be warranted (9). Likewise, the good and
poor sleepers did not significantly differ in IQ. Collectively, these findings add support the
value of screening for sleep disturbances in all children with ASD, regardless of age and
cognitive level.
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Although significant differences were not observed for age or cognitive functioning, poor
sleepers had significantly higher mean scores on four of five ABC subscales (Irritability,
Hyperactivity, Social Withdrawal, and Stereotypy). The largest differences in children with
poor sleep were in irritability and hyperactivity/noncompliance, suggesting a possible
connection between poor sleep and degradation in externalizing, daytime behaviors. This
relationship between sleep behaviors and similar externalizing behaviors has been reported

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previously in primarily correlation studies (16, 30, 32, 33, 62). Our cross section design does
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not allow determination of the direction of this relationship, but either direction is plausible
and has been suggested in the general pediatric literature for children without ASD (63, 64).
A child who sleeps poorly is likely to be more irritable and hyperactive, but conversely
children who are irritable and hyperactive may not settle for sleep. Further inquiry is called
for with longitudinal study designs to disentangle the likely bidirectional associations and
their magnitude (63, 65). Given our findings here and previous work, clinicians providing
empirically supported parent training interventions for disruptive behavior in children with
ASD should also consider integrating sleep interventions in the treatment plan(40).

In addition to scores on disruptive behavior measures, the Social Withdrawal and Stereotypy
subscales on the ABC were significantly different for the two groups with higher scores for
the poor sleepers. The Social Withdrawal subscale is a reliable indicator of social disability
in children with ASD and is sensitive to change with treatment (57). This finding suggests
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those children with poorer sleep display more social disability, but again causality or
direction of this interaction is not clear. Higher scores on the ABC Stereotypy subscale in
the poor sleepers also suggests an interaction. Although measured on different instruments,
the increase in stereotypical behaviors is similar to other reports of increased repetitive and
ritualistic behaviors in children with ASD and sleep problems (25, 30). In a prior sleep
treatment study, we speculated that greater stereotypy was related to poorer treatment
response, but the sample size was insufficient to examine this possibility (9). Again, further
studies with designs that will allow examination of the complex interactions between sleep,
social disability and repetitive behaviors are needed.

Along with the significantly higher daytime behavior problems in the poor sleep group,
parenting stress was pointedly higher as well. All subscales of the PSI were significantly
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greater in the poor sleeper group compared to the good sleeper group. This indicates that
parents face greater burden when a child with ASD has the combined clinical picture of
disruptive behavior and poor sleep patterns. As noted, the potentially bidirectional nature of
these associations deserves more investigation in the field of ASD. It may be that poor child
sleep increases parental stress; just as plausible is that parent stress and poor parent-child
interactions unsettle the child’ sleep. These complex, transactional relationships between
parent-child interactions around bedtime and nighttime have been examined in young
children with typical development (66–68), but not in children with ASD. These
relationships should be studied within a biopsychosocial context as proposed by Sadeh and
colleagues (69, 70). Understanding these relationships is particularly important for treatment
development as it has been shown that parenting practices can be modified to benefit their
children with ASD in other areas (40, 41, 71–73).
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This study has several limitations that warrant consideration. First, our sample of children
with ASD included a narrow age range from age 3 to 7 years. To be included in the study, all
children had to have at least moderate levels of disruptive behaviors. This requirement limits
the generalizability of the findings. Although IQ did not seem related to sleep disturbances
in this sample, there is a chance that we underestimated IQ given the verbal requirements of
the two measures usedthe IQ tests used (74). Moreover, 87% of our sample was Caucasian,
which may not representative of all young children with ASD and disruptive behaviors.

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Nonetheless, our findings support an interaction between sleep disturbances, disruptive


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behavior, social disability, repetitive behaviors, and parental stress in young children with
ASD. These documented associations indicate the need for further study on the underlying
multifaceted mechanisms related to develop of sleep patterns in children with ASD.

Based on our findings here and the extant literature suggesting that poor sleep is linked to a
variety of daytime behavior problems and parent stress but possibly not to age or cognitive
level, further study of sleep within a comprehensive biopsychosocial model is needed to
advance our understanding of why some young children with ASD have significantly
disrupted sleep patterns and others do not is warranted. Such studies could examine the
relative contributions of child biomarkers to include cortisol and serotonin given reported
abnormalities in ASD which may affect circadian rhythms (75–78). Linkages between
frequently co-occurring psychiatric conditions in ASD such as anxiety or attention problem
and sleep patterns should be explored in longitudinal studies to move beyond correlation.
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Despite the demonstrated contributions of parent and family variables in disrupted in sleep
patterns in typically developing children, parental behavior at bedtime and interrupted sleep
patterns of young children with ASD are unexplored (66, 68, 79, 80). The role of other
family characteristics in sleep disturbances in children such as socioeconomic status and
family composition; which have studied in other pediatric populations have not been
examined in ASD. Learning more about these complex interactions of biological and
environmental factors will promote development of more tailored interventions to improve
sleep quality in children with ASD. With improved sleep, better outcome for children with
ASD could be expected.

Supplementary Material
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Refer to Web version on PubMed Central for supplementary material.

Acknowledgments
Funding: This work was funded by the National Institute of Mental Health by grants to Yale University/Emory
University (MH081148; principal investigator: Dr. Scahill), the University of Pittsburgh (MH080965; principal
investigator: Dr. Johnson), Ohio State University (MH081105; principal investigator: Dr. Lecavalier), Indiana
University (MH081221; principal investigator: Dr Swiezy), and the University of Rochester (MH080906; principal
investigator: Dr. Smith). The project described in this publication also was supported by a University of Rochester
Clinical and Translational Scholar Award (CTSA) (UL1 TR000042) from the National Center for Advancing
Translational Sciences of the National Institutes of Health (NIH); a CTSA (UL1 RR024139) and grant from the
National Center for Research Resources (NCRR) (5KL2RR024138), a component of the NIH; and the NIH
Roadmap for Medical Research. This work was supported in part by a Public Health Service grant (UL1
RR025008) from the CTSA program of the NIH NCRR at Emory University School of Medicine and also
supported by the Marcus Foundation,
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Highlights
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• No age difference between good and poor sleepers in young children with
ASD and disruptive behaviors were seen. This suggests that sleep problems
are unlikely to resolve as might be expected in similar ages of children with
typical development.

• Likewise, the good and poor sleepers did not significantly differ in IQ. These
findings add strong support for the need to screen for sleep disturbances in all
children with ASD, regardless of age and cognitive level.

• In contrast, poor sleepers exhibited significant more daytime behaviors to


include irritability hyperactivity, social withdrawal and stereotypical
behaviors
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• Parents of the poor sleep group experienced significantly more stress.


Author Manuscript
Author Manuscript

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Johnson et al. Page 13

Table 1

Descriptive Characteristics of Study Sample


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Total Sample Good Sleepers Poor Sleepers p value


N=177 N= 52 N =46

Mean (SD) age (in years) 4.7 (1.14) 4.81 (1.07) 4.67 (1.23) 0.57

Intellectual Levela # (%) # (%) # (%)

≥70 132 (74.6) 40 (76.9) 34 (73.9) 0.87

<70 43 (24.3) 12 (23.1) 11 (23.9)

Gender
Male 155 (87.6) 46 (88.5) 38 (82.6)

Female 22 (12.4) 6 (11.5) 8 (17.4)

Diagnosis
Asperger 5 (2.8) 3 (5.7) 0 (0)
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Autism 116 (65.5) 36 (69.2) 26 (56.5)

PDD 50 (28.2) 13 (25) 17 (37)

Race/Ethnicity
Caucasian/White 154 (87) 46 (88.5) 40 (86.9)

African American 14 (7.9) 2 (3.8) 5 (10.9)

Asian 6 (3.4) 3 (5.8) 3 (3.1)

Pacific Islander 2 (1.1) 0 (0) 1 (2.2)

Other/Mixed 1 (.6) 1 (1.9) 0 (0)

Hispanic 26 (14.7) 5 (9.6) 11 (23.9)

Non-Hispanic 151 (85.3) 47 (90.4) 35 (76.1)

Maternal Education
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Advanced degree 51 (28.8) 17 (32.7) 12 (26.1)

College degree 57 (32.2) 21 (40.4) 11 (23.9)

Some College 54 (30.5) 12 (23.1) 17 (37.0)

High school 7 (7.9) 2 (3.8) 5 (10.9)


Some high school 1 (.6) 0 (0.0) 1 (2.2)

ASD CSHQ Mean (SD) Mean (SD) Mean (SD)


Sleep Routine Problems 13.81 (3.60) 10.85 (1.79) 17.91 (2.76)

Insufficient Sleep 7.58 (2.61) 5.92 (1.15) 9.13 (3.04)

Sleep-onset Association Problems 6.4 (2.93) 4.63 (1.36) 9.46 (2.66)

SDB/Parasomnias 9.02(2.37) 7.29 (1.53) 11.24 (2.29)

Sleep Anxiety 4.12 (1.22) 3.42 (.67) 4.93 (1.34)


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Total 40.94 (8.62) 32.12 (2.49) 52.67 (5.08)

a
2 missing

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Table 2

ABC & PSI Results

Total Sample Good Sleepers Poor Sleepers


N=177 N=52 N=46
Johnson et al.

Mean (SD) Mean (SD)a Mean (SD) t- statistic p value

ADOS Total 15.09 (4.57) 14.75 (4.46) 15.07 (4.33) 0.36 .72

ABC Subscales
Irritability 23.80 (6.29) 22.12 (5.34) 25.83 (7.25) 2.85 .005*

Social Withdrawal/Lethargy 12.87 (8.22) 11.81 (7.32) 15.59 (8.52) 2.34 .021*

Stereotypic Behavior 6.39 (4.92) 6.08 (4.79) 8.11 (4.73) 2.11 .038*

Hyperactivity/Noncompliance 30.34 (9.32) 28.13 (9.34) 33.96 (9.13) 3.11 .002*

Inappropriate Speech 5.75 (3.15) 5.33 (3.22) 6.52 (3.13) 1.86 .066

PSI Subscales Mean (SD) %ile Mean (SD) %ilea Mean (SD) %ileb

Parental Distress 32.95 (8.72) 74 30.22 (8.34) 65 35.69 (9.72) 79 2.91 .005*

Parent-Child Dysfunctional Interaction 28.85 (7.49) 83 26.31 (5.77) 79 31.76 (7.39) 89 3.96 .000*

Difficult Child 42.55 (7.54) 94 40.63 (7.25) 91 44.98 (9.13) 97 2.54 .013*

Total Stress 104.13 (20.04) 91 97.16 (17.27) 87 111.53 (24.99) 95 3.22 .002*

a
3 PSI missing
b
1 PSI missing

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*
Significant
Page 14

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