Accepted Manuscript Title: The role of insomnia, pre-sleep arousal, and psychopathology symptoms in daytime impairment in adolescents with high-functioning autism spectrum disorder Author: Amanda L. Richdale, Emma Baker, Michelle Short, Michael Gradisar PII: DOI: Reference:
S1389-9457(14)00202-0 http://dx.doi.org/doi:10.1016/j.sleep.2014.05.005 SLEEP 2462
To appear in:
Sleep Medicine
Please cite this article as: Amanda L. Richdale, Emma Baker, Michelle Short, Michael Gradisar, The role of insomnia, pre-sleep arousal, and psychopathology symptoms in daytime impairment in adolescents with high-functioning autism spectrum disorder, Sleep Medicine (2014), http://dx.doi.org/doi:10.1016/j.sleep.2014.05.005. This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
The role of insomnia, pre-sleep arousal, and psychopathology symptoms in daytime impairment in adolescents with high-functioning autism spectrum disorder Amanda L. Richdale1, Emma Baker1, Michelle Short2 & Michael Gradisar3
1
Olga Tennison Autism Research Centre, School of Psychological Science, La Trobe
University, Melbourne, Australia 2
Centre for Sleep Research, University of South Australia, Adelaide, Australia
3
School of Psychology, Flinders University, Adelaide, Australia
Highlights Sleep and psychopathology in adolescents with autism spectrum disorder are examined. Insomnia and psychopathology were common in these adolescents with ASD. Psychopathology was associated with daytime functioning in adolescents with ASD.
Sleep was associated with daytime functioning in adolescents with ASD.
Our results have clinical implications for treating of these problems in ASD.
Correspondence to: Amanda Richdale Olga Tennison Autism Research Centre School of Psychological Science La Trobe University
Page 1 of 32
Kingsbury Drive, Bundoora VIC, 3086 AUSTRALIA p: +61 3 9479 1742 f: +61 3 9479 1956 email: [email protected]
Page 2 of 32
Abstract Objectives: Sleep disturbance and psychopathology are common during adolescence and are highly prevalent in individuals with a diagnosis of Autism Spectrum Disorder (ASD). The aim of this study was to investigate relationships between sleep disturbance, psychopathology symptoms, and daytime functioning in adolescents with high-functioning autism spectrum disorder (HFASD) compared to typically developing (TD) adolescents. Methods: Twenty-seven adolescents with HFASD and 27 age and sex-matched TD adolescents completed questionnaires related to sleep, psychopathology, and daytime functioning. Participants also completed a 7-day sleep/wake diary. A sub-sample of HFASD adolescents (55%) and all the TD adolescents wore an actigraphy monitor concurrently with the sleep diary. Results: Adolescents with HFASD had significantly higher scores for depressed mood, anxiety and pre-sleep arousal compared with TD adolescents, and poorer daytime functioning. There were more significant correlations between sleep variables and psychopathology variables, and sleep variables and daytime functioning in the HFASD group, than in the TD group. Standard regression found that sleep variables significantly accounted for 57% of the variance in daytime functioning symptoms of insufficient sleep in the HFASD group, while psychopathology variables accounted for 63% of the variance in daytime functioning. Conclusions: Both sleep disturbance and psychopathology are more prevalent in adolescents with HFASD and are major contributors to poor daytime functioning in these individuals.
Page 3 of 32
Keywords: Autism, Insomnia, Daytime Functioning, Anxiety, Arousal, Depression, Adolescence
Page 4 of 32
1.
Introduction Children and adolescents with an Autism Spectrum Disorder (ASD) are diagnosed on
the basis of atypical development of social interaction and social communication, as well as a restricted repertoire of interests and activities [1] (American Psychiatric Association, 2013). Intellectual capacity is often impaired, however people with an IQ >70 are classified as high-functioning ASD (HFASD). What is not captured by diagnostic criteria is that, relative to their peers, they are a population with higher rates of mood disorders [2, 3]. For instance, a recent meta-analysis found that 39.6% of children with ASD less than18 years had one or more co-morbid DSM-IV anxiety disorders [4]. Parents also report high levels of anxiety (79%) and depression (54%) in their school-aged children (aged 6-16 yrs) with high-functioning autism [5]. Anxiety symptoms experienced by children and adolescents with ASD include symptoms akin to somatic hyperarousal, such as ‘butterflies’, ‘nausea’ and ‘sweating’, as well as symptoms of cognitive hyperarousal such as ‘racing thoughts’ [6]. If these hyperarousal symptoms extend to the evening, they may inhibit their natural sleep onset process. Hyperarousal has been theorized to underlie both anxiety and insomnia symptoms in typically developing populations, but links with depression are more tenuous [7]. Presleep arousal, which includes both physiological processes (e.g., rapid heartbeat) and cognitive processes (e.g., an inability to stop ‘racing thoughts’) may significantly delay sleep onset, and over time may lead to insomnia symptoms [8]. Recently, Gregory and colleagues [8] assessed pre-sleep arousal in 123 children aged 8 to 10 years. Both somatic and cognitive arousal predicted child-reported sleep scores. Given several studies have now found high rates of both sleep disturbances and psychopathology in children and
Page 5 of 32
adolescents with HFASD [9-12], the important contribution of pre-sleep arousal to the sleep difficulties experienced by adolescents with HFASD remains unexamined. Empirical research supports theories of insomnia which posit that pre-sleep arousal plays a primary role in its development and maintenance [13, 14], and there is substantial evidence from TD adult and adolescent populations that sleep disruption and insomnia lead to poor daytime functioning, anxiety, and depression [7, 15, 16]. However, the associations between these factors in ASD adolescents have not been examined. Knowledge of such relationships may elucidate mechanisms involved between these often cited 'bi-directional relationships' between sleep and adaptive functioning (e.g., anxiety; [7, 17, 18]), which may in turn suggest effective treatment strategies to reduce insomnia symptoms and associated psychopathologies in HFASD populations. Thus, the aim of this study was to explore the relationships between pre-sleep arousal, insomnia symptoms, anxiety, depression, and daytime functioning in HFASD adolescents as compared with typically developing (TD) adolescents. 2.
Method and Materials
2.1
Participants Twenty-seven adolescents (Mage = 15.5±1.3yrs, 82%m) with a clinical diagnosis of
HFASD and 27 TD adolescents matched on age and gender (Mage = 15.5±1.1yrs, 82%m) participated. TD adolescents’ data were from an existing database of adolescents attending South Australian secondary schools [19]. Data were collected between May, 2010 and December, 2010. The two groups did not differ on puberty status, χ² (1, n = 49) = 0.17, p = 0.68, V = 0.05 [20]. The Social Communication Questionnaire (SCQ) [21] was completed by 25 of the 27 HFASD parents (M = 20.2, SD = 5.8). For the remaining two adolescents, 1
Page 6 of 32
parent provided their child’s diagnostic report, confirming an ASD diagnosis and the other was a client of an autism network that required a confirmed ASD diagnosis. All participants were attending mainstream secondary school. On a telephone screening questionnaire, 12 parents of HFASD adolescents provided an IQ score > 70 based on previous standardized assessments. All other parents indicated their child could read at an average to above average level. A complete description of the sample and sample recruitment can be found elsewhere [19]. 2.2
Sleep Measures
2.2.1
Insomnia Insomnia symptoms and severity were assessed using a modified Sleep Habits
Survey (mSHS) consisting of questions relating to sleep scheduling, sleep disturbances, insomnia symptoms , and daytime sleepiness. The mSHS was adapted from the School Sleep Habits Survey [22]. It is a 2-week retrospective questionnaire with 79 questions relating to sleep scheduling, sleep disturbances, and insomnia symptoms. Within the mSHS a set of questions based on the insomnia criteria within the ICSD-2 [23] were used to determine if adolescents met criteria for the definition of insomnia. Adolescents indicated if they experienced difficulties with initiating sleep, maintaining sleep or if sleep was nonrestorative, and if ‘yes’ they then indicated the symptom severity (from mild to very severe) and provided an estimate of duration (from 1 week to more than 6 months). Adolescents met criteria if they experienced at least one insomnia symptom, that the problem had lasted for at least one month and they also indicated impairment in daytime functioning (e.g., attention, concentration or memory impairment). Further details are reported elsewhere [19].
Page 7 of 32
2.2.2
Sleep Participants completed a 7-day sleep/wake diary (Mon-Sun). The following sleep
parameters were evaluated; time in bed (TIB), total sleep time (TST), sleep latency (SoL), wake after sleep onset (WASO) and sleep efficiency (SE%). Further details regarding the sleep diary are reported elsewhere [20]. Fifteen (55%) of the HFASD adolescents and all TD adolescents wore a MicroMini Motionlogger (Actigraphy) on their non-dominant wrist for the duration of the 7-day sleep/wake diary period. Data were digitized in 1-minute epochs using zero crossing mode, with a sensitivity of 0.05g and a bandwidth of 2-3 Hz, and analysed with Action W2 software (AMI) using the Sadeh algorithim. This algorithim has been validated for use with adolescent populations [24]. Further details regarding scoring and calculations of sleep parameters are reported elsewhere [19]. 2.2.3 Daytime Functioning The Chronic Sleep Reduction Questionnaire (CSRQ) was used to measure daytime functioning. The CSRQ provides a measure of the symptoms of chronic sleep reduction and thus the impact of sleep debt in children and adolescents [25]. It consists of 20 questions answered on a 3-point scale, and comprises four sub-scales measuring daytime functioning symptoms relating to: Shortness of Sleep (6 items), Sleepiness (4 items), Loss of Energy (5 items), and Irritation (5 items). A higher total score is a strong indicator of worse daytime functioning. The reliability and validity of the English version of the CSRQ was assessed on 236 Australian adolescents, average age 15.5 years [26]. It showed the same factor structure as the original Dutch version and good reliability with α = .87. Internal consistency here was excellent for the HFASD group with α = .87 and good for the TD group α = .73.
Page 8 of 32
2.3
Psychopathology Measures
2.3.1
Depressed Mood The Centre for Epidemiological Studies Depression scale (CES-D) was used to
measure depressed mood. The CES-D [27] is a short, self-report questionnaire designed to measure depressive symptomatology in the general population. It contains 20 items, which are symptoms of depression that have been used in previously validated, longer scales. Questions are answered on a 4-point scale with scores >16 representing risk for clinical depression. The CES-D contains one question about sleep ‘My sleep is restless’. This question was removed for the analyses reported here. In the current study, reliability for the scale with this item removed was excellent; α = .89 for the HFASD group and good for the TD group, α = .74. 2.3.2
Anxiety The anxiety subscale of the Depression, Anxiety and Stress Scale (DASS-21) was
used to assess general anxiety [28]. It consists of seven self-report items that assesses the severity of the core symptoms of anxiety, with participants rating each item on a 3-point scale. A total score is generated, which when multiplied by two gives a clinical score. Clinical scores < 8 are considered in the normal range. The reliability of the scale in the current study was excellent for the HFASD group, α = .86 and moderate for the TD group, α = .54 2.3.3
Pre-sleep Arousal The Sleep Anticipatory Anxiety Questionnaire (SAAQ) was used to measure pre-
sleep arousal. The SAAQ is a 10-item self-report questionnaire that measures a respondent’s level of anxiety related to sleep (pre-sleep arousal) on a 4-point scale (e.g., My
Page 9 of 32
heart is beating rapidly; I worry that I won’t get enough sleep) [29]. Three scores are obtained from the SAAQ: a total score (SAA-T) measuring overall anxiety about sleep, and two sub-scores (5 items each) measuring self-reported cognitive (SAA-C) and somatic (SAA-S) arousal while trying to fall asleep at night. Higher scores indicate greater pre-sleep arousal. In the current study internal consistency was excellent for the HFASD group, α = .92 and the TD group, α = .87 2.4
Procedure Institutional ethics approval was granted (Approval Numbers GE10/0009 1620 and
FUSBREC 4057; Approval Number HEC10-029). Families of adolescents with ASD who responded to an advertisement completed a telephone-screening questionnaire to determine the adolescent’s eligibility to participate. A letter of introduction, information about the study and a consent form were then posted to eligible families and after receipt of consent the adolescent and their parent or guardian was sent a study pack containing the research materials, including the actigraphy motion-logger where applicable. Prior to recruitment, HFASD adolescent identification codes were randomly selected for the actigraphy component of the study. When participants consented to the study, they were assigned an identification code, and if they were assigned a code that was associated with actigraphy they were invited participate in this part in this study. All HFASD participants assigned a code linked to the actigraphy agreed to complete this component of the study. Sleep diary and actigraphy data were collected for seven consecutive days, and participants were contacted by one of the researchers (EB) once during this period to check recording. Materials were all returned by reply-paid post. 2.5
Data Analysis
Page 10 of 32
Three HFASD adolescents did not complete the sleep diary, however none of these adolescents had been randomly selected to wear actigraphy monitors. Details are reported in Baker et al. [19]. A small number of responses were missing from questionnaires for the HFASD participants. Where there was only one item response missing from a scale the mean response for that subscale or scale was substituted. Three participants were each missing question 7 (Shortness of Sleep subscale) on the CSRQ; one participant was missing one question from each of the SAAQ and the DASS-21 anxiety scales; and two participants were missing one question each from the CES-D. If two or more items were missing, the respondent was removed from the analysis. As a result, one adolescent was excluded because there were no completed questionnaires and one participant was excluded from the SAAQ total scores analyses, as two questions were not completed. Data screening indicated that CSRQ and SAAQ all met assumptions for normality. There were four outliers for anxiety, one of which was extreme, and two outliers for depression, one of which was also extreme; all were from the HFASD group. Depression and anxiety are commonly associated with HFASD and thus outliers and extreme scores may be expected. The means (2.73, 13.43) and 5% trimmed means (2.28, 12.63) were not very different for anxiety or depression respectively and parametric statistics are robust to violations of normality [30] thus, these adolescents remained in the analyses and no data transformations were used. A series of Student’s t-tests for independent samples was employed to examine group differences on psychopathology variables. MANOVA was used to examine group differences for the CRSQ and SAAQ subscales. Pearson’s correlation analyses were used to
Page 11 of 32
determine the associations between sleep parameters, CSRQ, and psychopathology variables. Standard multiple regression was used to examine predictors of chronic sleep problems in both groups of adolescents using the CSRQ total score (daytime functioning) as the dependent variable and sleep or psychopathology measures as predictors. While the two sample sizes were small the minimum suggested ratio of cases to IVs is 5:1 [31]. Thus up to three predictor variables that correlated significantly with the CSRQ were considered for each regression. 3.
Results
3.1
Psychopathology and CSRQ scores in TD and HFASD Adolescents First, we examined whether adolescents with HFASD and TD adolescents differed
on anxiety, depression and pre-sleep arousal (see Table 1). The HFASD group had significantly higher depressed mood (t [37.08] = 2.30, p = .027, η2 = .09) and anxiety (t [34.34] = 2.17, p = .037, η2 = .08) compared to TD adolescents, both with moderate effect size. Furthermore, 10 (38.5%) HFASD adolescents and five (18.5%) TD adolescents had depression scores above the CES-D clinical cut-off (16) and five (19.2%) HFASD adolescents but no TD adolescents had clinical anxiety scores (> 7). Four adolescents in the HFASD group with scores above the clinical cut-off for anxiety were also above the clinical cut-off for depression. Adolescents with HFASD also had significantly higher pre-sleep arousal (SAA-T) than TD adolescents (t (50) = 2.25, p = .029, η2 = .09) with moderate effect size. Examining the two subscales, there was no statistically significant group effect (Wilks = .91, F (2, 49) = 2.48, p = .094, partial 2 = .09), but the effect size was moderate. The
Page 12 of 32
groups differed significantly on cognitive arousal (F (1, 50) = 4.73, p = .034, partial η2 = .09; moderate effect size), but not on the somatic subscale (F (1, 50) = 3.73, p = .059, partial η2 = .07; moderate effect size). After collapsing the SAAQ responses to give two categories, “Agree” (score of 2 or 3) and “Disagree” (score of 0 or 1) we also examined the individual questions, both to see which aspects of arousal most often occurred, and whether there were any differences in their occurrence across the two groups (Table 2). A larger proportion of HFASD adolescents positively endorsed all statements on the SAAQ, however only one statement, ‘I worry that I won’t be able to fall asleep’ was endorsed by significantly more HFASD than TD adolescents. While the HFASD adolescents had worse daytime functioning (CSRQ) than the TD adolescents (Table 1); this was not significant (t (42.36) = 1.54, p = .13, η2 = .04). Examining the four daytime functioning (CSRQ) subscales, there was a significant group effect (Wilks λ = .79, F (4, 48) = 3.17, p = .022, partial η2 = .21) with large effect size. Subscale scores were similar for Shortness of Sleep, Sleepiness, and Irritation but the HFASD group had a significantly higher mean score for the Loss of Energy sub-scale (F [1, 51] = 37.23, p = .002, partial η2 = .17) with strong effect size. 3.3
Associations between Sleep, Psychopathology and Daytime Functioning Pearson correlations were used to examine the linear relationships between sleep,
psychopathology and daytime functioning in HFASD and TD adolescents (Tables 3 and 4). Overall, there were more significant correlations between sleep variables and psychopathology, and sleep variables and daytime functioning in the HFASD group, than in the TD group. All psychopathology measures were moderately or strongly associated with daytime functioning in HFASD adolescents. Reporting a sleep problem, ICSD-2
Page 13 of 32
defined insomnia, and sleep variables from the sleep diary (bedtime, wake time and SE%) and actigraphy (sleep onset time and SoL) were all significantly associated with worse daytime functioning in HFASD adolescents. Reporting a sleep problem was strongly associated with depression and moderately or strongly associated with all measures of anxiety. ICSD-2 defined insomnia, and number of insomnia symptoms, were both related to all measures of anxiety, also the latter was strongly associated with depression. On the sleep diary, SE% and SoL were associated with depression and anxiety, also depression was related to wake time. For actigraphy, sleep duration was associated with SAA-C, while sleep onset was associated with both SAA-T and SAA-C. Significant associations for TD adolescents were moderate (Table 4). Depression and SAA-C were associated with ICSD-2 defined insomnia, while anxiety was related to reporting a sleep problem. On the sleep diary, night waking was associated with SAA-S. On actigraphy, SAA-T was associated with sleep length, and SAA-C was associated with both sleep length and wake time. In TD adolescents, daytime functioning was associated only with reporting insomnia and meeting criteria for ICSD-2 defined insomnia. Counterintuitively there was a moderate, non-significant negative correlation between WASO and daytime functioning; wake-time was also moderately but non-significantly associated with daytime functioning. 3.4
Predicting Daytime Functioning Using standard multiple regression the ability of sleep variables to predict daytime
functioning (CSRQ scores) was examined; next the ability of psychopathology variables to predict daytime functioning was examined. In selecting the variables, we examined those sleep and psychopathology variables that were significantly correlated with daytime
Page 14 of 32
functioning in each group (see Tables 3 and 4). Within the HFASD group, several independent variables were highly correlated (r > .70) however examination of Mahalanobis Distance and Cook’s Distance indicated that this was not a problem and inspection of Normal P-P plots and scatterplots met assumptions of normality. To take account of small sample size, adjusted R2 is reported for the final model [32]. For the HFASD group three predictor variables were entered into the sleep regression, reporting a sleep problem, number of ICSD-2 insomnia symptoms and morning wake time. The model was significant, adjusted R2 = .57, F (3, 20) = 11.23 p < .001, and accounted for 57% of the variance in CSRQ scores. Number of ICSD-2 insomnia symptoms was a significant, unique predictor within the model (p = .009) accounting for 15% of the variance in CSRQ scores in the HFASD group. Examining psychopathology as a predictor depression, anxiety, and SAA-T scores were entered in the regression model. The model was significant, adjusted R2 = .63, F (3, 20) = 13.81, p < .001, that is the model accounted for 63% of the variance in CSRQ scores. Sleep anxiety (SAA-T) was a significant, unique predictor within the model (p = .005) accounting for 16% of the variance in CSRQ scores. As both sleep and psychopathology variables independently accounted for a large proportion of the variance in CSRQ scores for the HFASD group we conducted hierarchical regression analyses to explore whether each of the psychopathology variables explained any additional variance in the CSRQ total score, after controlling for the sleep variables. In the first hierarchical regression the addition of DASS-anxiety at step 2 accounted for an additional 7% of the variance in CSRQ scores, F change (1, 19) = 4.48, p = .048, and the overall model accounted for 63.5% of the variance, adjusted R2 = .635, F (4, 19) = 11.08, p
Page 15 of 32
< .001. In the second hierarchical regression the addition of pre-sleep arousal (SAA-T) at step 2 accounted for an additional 15% of the variance in CSRQ scores, F change (1, 18) = 11.71, p = .003, and the overall model accounted for 72% of the variance, adjusted R2 = .72, F (4, 19) = 15.44, p < .001. In the final hierarchical regression, the addition of CES-D depression at step 2 accounted for an additional 11% of the variance in CSRQ scores, F change (1, 19) = 8.15, p = .01, and the overall model accounted for 68% of the variance, adjusted R2 = .68, F (4, 19) = 13.47, p < .001. Only reporting a sleep problem, and ICSD-insomnia, whose criteria overlap, were significantly associated with daytime functioning in the TD group, thus regression analyses were not conducted for this group. 4.
Discussion
4.1
Sleep and Daytime Functioning As we have reported in detail elsewhere [19] adolescents with HFASD experience
more problems associated with sleep than TD adolescents. However, HFASD adolescents did not report significantly worse daytime functioning than TD adolescents. While the HFASD adolescents tended to report worse daytime functioning than TD adolescents, only ‘loss of energy' was significantly worse for the HFASD adolescents. This finding is consistent with the presence of more daytime fatigue reported by these adolescents with HFASD [19]. As expected, sleep variables were significantly associated with daytime functioning in the HFASD group, but not in the TD group. Correlations between sleep parameters and daytime functioning for the TD group were weak to moderate. Lack of significant correlations within the TD group may be attributed to low power due to our small sample
Page 16 of 32
size. Nevertheless, daytime functioning was moderately or strongly associated with all sleep variables for the HFASD adolescents. The majority of these correlations were significant, suggesting that in our sample poor sleep has a more deleterious impact on daytime functioning in HFASD than TD adolescents. 4.2
Psychopathology As expected, adolescents with HFASD had significantly more self-reported
symptoms of psychopathology than the TD adolescents. Increased prevalence of anxiety and depression in individuals with an ASD compared with TD individuals has been reported previously [3], but pre-sleep arousal has not previously been examined. In their meta-analysis, van Steensel et al. [4] reported the prevalence of GAD at 15%, and while the presence of any anxiety disorder averaged 39.6%, specific phobias (30%) and OCD (17%) were the most common; the latter are not measured by the DASS. In 38 adolescents (10-17 years) with HFASD, rate of any DSM-IV anxiety disorder by parent-report (semi-structured interview) was 28.9%, with phobias again being the most common. Thus, the rate of clinical levels of anxiety (19.5%) reported by our HFASD adolescents is within the range expected. The reported rate of clinical levels of depressive symptoms (38.5%) was within the range reported by parents of children and adolescents with HFASD. For example, Mayes et al. [5] found that 54% of parents of 6-16 year-olds with HFASD reported clinical levels of depression in their children, while using a semi-structured interview with parents, Mazefsky et al. [33] found that 18.4% of 10-17 year-olds with HFASD met criteria for any DSM-IV depressive disorder. Variability in reported rates of anxiety and depression in HFASD may relate to several factors including sample size, recruitment bias or sampling method, use of different
Page 17 of 32
measures of psychopathology, and whether parent-report or self-report is used. Both anxiety and depression are reported to increase with age in ASD [4, 5], and majority of studies to date have used only parent-report to examine psychopathology. In TD samples, there is often poor parent-child agreement for measures of psychopathology [33, 34]. Mazefsky et al. [33] argued that caution should be exercised with self-reported psychopathology in young people with HFASD. However Blakely-Smith et al. [33] found overall moderate parent-child agreement for anxiety symptoms in 63 children and adolescents (8-14 yrs) with HFASD. Furthermore, Richdale and Baglin [11] found some agreement for parent and child reported anxiety but little agreement on depression in 17, 8to 12-year-old children with HFASD. Taken together, agreement about the presence of psychopathology between parent- and child-report in HFASD samples may be similarly variable to that found in TD samples. In line with previous research [8, 35], our adolescents were more likely to experience cognitive arousal associated with sleep rather than somatic arousal. Furthermore, the HFASD adolescents experienced significantly more pre-sleep arousal, especially cognitive arousal, than did the TD adolescents. Additionally, significantly more HFASD adolescents endorsed the statement ‘I worry that I won’t be able to fall asleep’ than did TD adolescents. Our findings are consistent with self-reports of symptoms of cognitive and somatic arousal by children and adolescents with HFASD [6]. Thus, pre-sleep arousal, most commonly cognitive arousal, appears to contribute significantly to insomnia in these HFASD adolescents. 4.3
Sleep, Psychopathology, and Daytime Functioning
Page 18 of 32
As predicted anxiety, depression, and pre-sleep arousal were all associated moderately to strongly with daytime functioning (CSRQ), including subscales, for the HFASD adolescents, with almost all correlations being significant. In contrast, in the TD group, there were few significant moderate or strong associations between daytime functioning and psychopathology, with only anxiety and pre-sleep cognitive arousal having a moderate and significant association with daytime functioning. This suggests that for the HFASD group there is considerable overlap between poor sleep and elevated symptoms of psychopathology with both contributing significantly to poor daytime functioning in these young people. We conducted regression analyses to explore how well sleep and psychopathology variables predicted poor daytime functioning in the HFASD group. Sleep variables accounted for over half the variance in daytime functioning, with the number of ICSD-2 insomnia symptoms being a unique predictor. Similarly, around two thirds of the variance in daytime functioning was accounted for by psychopathology (anxiety, pre-sleep arousal, depression) and pre-sleep arousal was a unique predictor. Finally, using separate hierarchical regressions we explored the ability of each psychopathology measure to account for additional variance in daytime functioning after the contribution of the sleep variables had been accounted for. Anxiety, pre-sleep arousal, and depression all accounted for additional variance. Our findings thus suggest that there is a striking overlap between the daytime symptoms of chronic poor sleep and psychopathology for adolescents with HFASD where all measures of psychopathology showed significant relationships with daytime functioning as well as with sleep variables. This highlights the overlap between psychopathology and
Page 19 of 32
insomnia in individuals with HFASD, supporting previous reports of associations between both anxiety and depression and poor sleep [9-11, 36]. In particular, our results clearly suggest for the first time that pre-sleep arousal and therefore hyperarousal may play a significant role in insomnia in HFASD. The high rate of sleep problems and anxiety in children with HFASD and their continuation into adolescence is also likely to be a significant pre-disposing factor for the development of depression in these young people. While our findings require replication, future research should also explore whether in young children with HFASD, anxiety precedes sleep problems or vice versa or whether they arise together. 4.4
Clinical Implications
Given the known relationships between psychopathology and sleep disturbance in the general population [37], and the strong relationships found between psychopathology and sleep disturbance in the HFASD adolescents here, treating sleep disturbance or psychopathology in isolation in these adolescents may not lead to successful treatment outcomes. The presence of anxiety, depression or insomnia as the presenting complaint should be a red flag for the exploration of the other disorders as potential comorbid conditions. Furthermore, the impact of the treatment of anxiety or depression on insomnia or vice versa should be monitored, and co-treating the insomnia as part of any anxiety or depression intervention should occur. While both high rates of insomnia and psychopathology are acknowledged in HFASD and associations between the two have been reported [9-11, 36], emerging treatment studies do not consider these as comorbid conditions that require parallel treatment. Indeed, even monitoring the impact of the treatment of one condition has not been reported.
Page 20 of 32
Furthermore, the apparent importance of pre-sleep arousal for insomnia in HFASD suggests that treatments that reduce cognitive and somatic arousal associated with bedtime and sleep onset may be effective in the treatment of insomnia in this population. This has not been explored. Researchers are beginning to explore the usefulness of using or adapting cognitive behaviour therapy (CBT) for the treatment of anxiety in HFASD, with a small number of studies emerging in the past 5 years [e.g., 38]. There are concerns that difficulties inherent in ASD with regard to understanding their own and others cognitions and emotions and their literal thinking may impact on the effectiveness of CBT in this population. However there are now several treatment studies that suggest CBT can be effective, especially where these programs incorporate adaptations that allow for the social and adaptive behaviour difficulties that are associated with ASD [39]. This suggests that CBT-Insomnia (CBT-I) should be an effective treatment for insomnia in young people with HFASD. As for CBT, some modifications to CBT-I may be required, however the structured behavioural components of CBT-I are likely to be effective. The incorporation of stress reduction techniques (e.g., mindfulness) together with strict sleep hygiene and restriction of time in bed to time spent sleeping may be advantageous. Behavioural interventions including bedtime fading techniques have been shown to be useful treatments for sleep onset insomnia in young children with ASD [40, 41]. 4.5
Strengths and Limitations of the study The major strength of this study is that it comprised a sample of adolescents only
and participants were matched on age and sex [19]. A further strength is that we had both sleep diaries and actigraphy as measures of sleep and we obtained self-reports from the adolescents on measures of sleep and psychopathology. Further, this is the first study, that
Page 21 of 32
we are aware of, that has directly investigated pre-sleep arousal in adolescents with HFASD. Our findings indicate that pre-sleep arousal in this population is important for understanding the development and continuation of the insomnia frequently seen in this population. Given, the small sample size the power to detect differences between the two groups on daytime functioning may have been reduced. However, the daytime functioning results were similar to those reported by Dewald et al. [26], correlations between daytime functioning and psychopathology and sleep variables in the HFASD group were predominantly moderate or strong, while internal consistency for the three psychopathology scales was excellent, whereas for the TD adolescents it was moderate to good. A further limitation is the exploratory nature of the regression analyses, including restrictions imposed by our sample size. Replication of our findings with larger samples and examination of both insomnia and psychopathology in treatment studies will be important in future research, particularly in HFASD populations. This should clarify the role of psychopathology in the manifestation and maintenance of sleep disturbance in HFASD. 4.6
Conclusion
In conclusion, sleep and psychopathology were significant contributors to daytime functioning in the HFASD group, with moderate to strong correlations between measures and a large proportion of variance in daytime functioning accounted for by these variables. These relationships were considerably fewer and more modest in the TD group. Further pre-sleep arousal, in particular, cognitive arousal was prominent in the HFASD group. Thus, it appears that both chronic insomnia and elevated symptoms of psychopathology are major contributors to poor daytime functioning in HFASD. Given that anxiety may be more
Page 22 of 32
prevalent in lower functioning individuals with ASD than in HFASD [4], the role of anxiety in insomnia across the autism spectrum should be a focus of future investigation.
Page 23 of 32
References [1] American Psychiatric Association. Diagnostic and Statistical Manual of Mental Disorders. 5th ed. Arlington, VA: American Psychiatric Publishing, 2013. [2] American Academy of Child and Adolescent Psychiatry. Practice parameters for the assessment and treatment of children and adolescents with depressive disorders. AACAP. J Am Acad Child Adoles Psychiatry 2007;46(11):1503-1526. [3] Strang JF, Kenworthy L, Daniolos P, Case L, Wills MC, Martin A, et al. Depression and anxiety symptoms in children and adolescents with autism spectrum disorders without intellectual disability. Res Autism Spect Dis 2012;6(1):406-412. [4] van Steensel FJ, Bogels SM, Perrin S. Anxiety disorders in children and adolescents with autistic spectrum disorders: A meta analysis. Clin Child Fam Psychol Rev 2011;14(3):302-317. [5] Mayes SD, Calhoun SL, Murray MJ, Ahuja M, Smith LA. Anxiety, depression, and irritability in children with autism relative to other neuropsychiatric disorders and typical development. Research in Autism Spectrum Disorders 2011;5(1):474-485. [6] Ozsivadjian A, Knott F, Magiati I. Parent and child perspectives on the nature of anxiety in children and young people with autism spectrum disorders: a focus group study. Autism 2012;16(2):107-121. [7] Gregory AM, Sadeh A. (2012). Sleep, emotional and behavioral difficulties in children and adolescents Sleep Med Rev 2012;16(2):129-136. [8] Gregory AM, Willis TA, Wiggs L, Harvey AG, STEPS Team. Presleep arousal and sleep disturbances in children. Sleep 2008;31(12):1745-1747.
Page 24 of 32
[9] Mayes SD, Calhoun SL. (2009). Variables related to sleep problems in children with autism. Res Autism Spect Dis 2009;3(4): 931-941. [10] Goldman SE, McGrew SG, Johnson KP, Richdale AL, Clemons T, Malow BA. Sleep is associated with problem behaviors in children and adolescents with autism spectrum disorders. Res Autism Spect Dis 2011;5(3):1223-1229. [11] Richdale AL, Baglin C. Self-report and caregiver-report of sleep and psychopathology in children with high-functioning autism spectrum disorder: A pilot study. Dev Neurorehabil. Forthcoming 2013 [12] Allik H, Larsson JO, Smedje A. Insomnia in school-age children with Asperger syndrome or high-functioning autism. BMC Psychiatry 2006;6: 6-18. [13] Harvey AG. A cognitive model of insomnia. Beh Res Ther 2002;40(8):869-93. [14] Harvey AG. A cognitive theory and therapy for chronic insomnia. Journal of Cognitive Psychotherapy 2005;19: 41-59. [15] Dewald JF, Meijer AM, Oort FJ, Kerkhof GA. The influence of sleep quality, sleep duration and sleepiness on school performance in children and adolescents: a meta-analytic review. Sleep Med Rev 2010;14:179-189. [16] Lovato N, Gradisar M. (in press). A meta-analysis and model of the relationship between sleep and depression in adolescents: Recommendations for future research and clinical practice. Sleep Med Rev (in press). [17] Dahl RE, Harvey AG. (2007). Sleep in children and adolescents with behavioral and emotional disorders. Sleep Med Clins 2007;2:501-511. [18] Leahy E, Gradisar M. (2012). Dismantling the bi-directional relationship between paediatric sleep and anxiety. Clinical Psychologist 2012;16:44-56.
Page 25 of 32
[19] Baker E, Richdale A, Short M, Gradisar M. An investigation of sleep patterns in adolescents with high-functioning autism spectrum disorder compared with typically developing adolescents. Dev Neurorehabil 2013;16(3):155-165. [20] Carskadon MA, Acebo C. A self-administered rating scale for pubertal development. J Adolesc Health 1993;14(3):190-195. [21] Rutter M, Bailey A, Lord C. The social communication questionnaire manual. Los Angeles: Western Psychological Services, 2003. [22] Wolfson AR, Carskadon MA, Acebo C, Seifer R, Fallone G, Labyak SE, et al. Evidence for the validity of a sleep habits survey for adolescents. Sleep 2003;26(2):213216. [23] American Academy of Sleep Medicine. The international classification of sleep disorders: diagnostic and coding manual. 2nd ed. Westchester, III: American Academy of Sleep Medicine, 2005. [24] Sadeh A, Sharkey KM, Carskadon MA. Activity-based sleep-wake identification: An empirical test of methodological issues. Sleep 1994;17:201-207. [25] Meijer AM. Chronic sleep reduction, functioning at school and school achievement in preadolescents. J Sleep Res 2008;17(4):395-405. [26] Dewald JF, Short MA, Gradisar M, Oort FJ, Meijer AM. The chronic sleep reduction questionnaire (CSRQ): A cross-cultural comparison and validation in Dutch and Australian adolescents. J Sleep Res 2012;21(5):584-594. [27] Radloff LS. The CES-D scale: A self-report depression scale for research in the general population. Appl Psych Meas 1977;1(3):385-401.
Page 26 of 32
[28] Lovibond PF, Lovibond SH. The structure of negative emotional states: Comparison of the Depression Anxiety Stress Scales (DASS) with the Beck Depression and Anxiety Inventories. Behav Res Ther 1995;33(3):335-343. [29] Bootzin R, Shoham V, Kuo T. Sleep anticipatory anxiety questionnaire: A measure of anxiety about sleep. Sleep Res 1994; 23:188. [30] Norman G. Likert scales, levels of measurement and the “laws” of statistics. Adv Health Sci Educ 2010;15(5):625-632. [31] Coakes SJ, Steed L, Ong C. SPSS 16.0 for windows: Analysis without anguish. Australia: John Wiley and Sons, 2009. [32] Pallant J. SPSS Survival Manual: A step by step guide to data analysis using the SPSS program. 4th ed. Crows Nest, NSW: Allen & Unwin, 2011. [33] Mazefsky CA, Kao J, Oswald DP. Preliminary evidence suggesting caution in the use of psychiatric self-report measures with adolescents with high-functioning autism spectrum disorders. Res Autism Spect Dis 2011;5(1):164-174. [34] Blakeley-Smith A, Reaven J, Ridge K, Hepburn S. Parent–child agreement of anxiety symptoms in youth with autism spectrum disorders. Res Autism Spect Dis 2012;6(2):707716. [35] Lichstein KL, Rosenthal TL. Insomniacs' perceptions of cognitive versus somatic determinants of sleep disturbance. J Abnorm Psychol 1980;89(1):105-107. [36] Paavonen EJ, Vehkalahti K, Vanhala R, von Wendt L, Nieminen-von Wendt T, Aronen ET. Sleep in children with Asperger syndrome. J Autism Dev Disord 2008;38(1):41-51.
Page 27 of 32
[37] Breslau N, Roth T, Rosental L, Andreski P. Sleep disturbance and psychiatric disorders: A longitudinal epidemiological study of young adults. Biol Psychiatry 1996;39(6):411-418. [38] Chalfant AM, Rapee R, Carroll L. Treating anxiety disorders in children with high functioning autism spectrum disorders: A controlled trial.J Autism Dev Disord 2007; 37:1842-1857. [39] McNally Keehn RH, Lincoln AJ, Brown MZ, Chavira DA. The coping cat program for children with anxiety and autism spectrum disorder: A pilot randomized controlled trial. J Autism Dev Disord 2013;43:57-67. [40] Moon EC, Corkum P, Smith IM. Case study: A case-series evaluation of a behavioral sleep intervention for three children with autism and primary insomnia. J Ped Psychol 2011;36(1):47-54. [41] Turner KS, Johnson CR. Behavioral interventions to address sleep disturbances in children with autism spectrum disorders: A review. Topics Early Childhood Spec Ed 2013;33(3):144-152
Table 1 Groups Means for CSRQ Total Score and Psychopathology Variables HFASD
TD
n
M
SD
n
M
SD
CSRQ
26
37.08
7.79
27
34.30
5.00
Depression
26
16.35
11.32
27
10.63
5.83
Anxiety
26
3.77
4.37
27
1.74
1.95
Page 28 of 32
SAA-S
26
4.04
2.88
27
2.55
2.33
SAA-C
25
7.08
4.27
27
4.81
3.20
SAA-T
25
11.04
6.80
27
7.37
4.89
SAA: Sleep Anticipatory Anxiety
Page 29 of 32
30 Table 2. Examination of Individual SAA-Q Statements for each Group 1
Adolescents Agreeing with each Statement HFASD
TD
(n = 26)
(n = 27)
4 (15.4%)
1 (3.7%)
-
2 (7.7%)
0
-
3 (11.5%)
1 (3.7%)
-
2 (7.7%)
1 (3.7%)
-
13 (50%)
9 (33.3%)
.91
18 (69.2%)
11 (40.7%)
3.27
I worry that I won’t be able to fall asleep
13 (50%)
3 (11.1%)
7.75
I worry that I won’t get enough sleep
13 (50%)
7 (25.9%)
2.32
11 (44%)
8 (29.6%)
.62
8 (32%)
8 (29.6%)
0
SAA-Q Statements My muscles are tense
2
My heart is beating rapidly I feel “shaky”/trembling
2
2
I become short of breath
2
I become aware of my body (feeling itches, sweat, pain, nausea) I can’t stop my mind racing
I worry that I won’t be able to function the next day if I don’t sleep I worry that I will be tired and irritable the next day if I don’t sleep
3
3
2
1
Agree or Strongly Agree the symptom is present. Fisher’s Exact Test probability 3 n = 25 for HFASD group.
2
Page 30 of 32
31
Table 3 Correlations between the CSRQ and Psychopathology Variables CSRQ: HFASD (n = 26)1
CSRQ: TD (n = 27)
Psychopath Total
Short
Irritation
Loss of
Sleepiness
Total
Short
Irritation
Lo
Variable Sleep
Energy
Sleep
En
Depression
.71a
.42c
.72a
.54b
.70a
.30
-.02
.14
.3
Anxiety
.60a
.35
.60a
.45c
.58b
.49b
.23
.32
.
SAA-T
.81a
.53b
.75a
.64b
.75a
.22
.29
-.09
.
SAA-S
.76a
.47c
.66a
.62a
.73a
-.04
.11
-.24
-
SAA-C
.78a
.53b
.75a
.58b
.70a
.36d
.36d
.04
.
1 a
For some correlations, nHFASD = 25 and nTD = 26 due to missing data p ≤ .001, b p ≤ .01, c p ≤ .05, d .05 > p < .10
Page 31 of 32
32 Table 4 Correlations between Psychopathology, CSRQ and Sleep Variables HFASD (n = 26)1
Sleep Variable
TD (n = 27
CES-D
Anxiety
SAA-T
SAA-S
SAA-C
Sleep Problem
-.54b
-.48b-
-.62a
-.48b
-.63a
ICSD Ins
-.46c
-.42c
-.69a
-.54b
b
.53
b
.68
a
.60
a
.68
Bedtime
.28
.18
.37
.31
Wake time
.40
.17
.36
Total sleep
-.27
-.37
-.23
Sleep efficiency
-.43
c
c
-.46
.36
Sleep latency
.51c
.59b
WASO
.06
Sleep onset time Wake time
o
N ICSD Ins
CES-D
Anxiety
SAA-T
-
.62a
-.12
-.38c
-.21
-.69a
-.65a
-.46c
-.31
-.36
a
a
.31
.27
.25
.40
.43c
.16
.03
.02
.35
.35
.55b
.34
.23
.30
-.17
.23
-.22
.04
.15
.13
-.34
.33
-.49
b
.12
-.03
-.20
.33
.32
.29
.33
-.10
.01
.10
-.01
.00
.04
-.06
.19
-.09
.05
.27
.54c
.22
.54c
.35
.62b
.
60c
.20
.05
.01
.41
.24
.44
.39
.44
.42
.17
.23
.35
.49
CSRQ
.73
Sleep Diary
2
Actigraphy
c
Sleep length
-.43
-.04
-.48
-.24
-.61
-.48
-.05
.05
.46c
Sleep latency
.35
.17
.34
.27
.36
.57c
.09
.28
.06
1
nHFASD varies from 23 – 26 participants and nTD varies from 25-27 participants due to missing data 2 n = 15 for HFASD group (for some correlations n = 14 due to missing data). a p ≤ .001, b p ≤ .01, c p ≤ .05
Page 32 of 32
SA
S1389-9457(14)00202-0 http://dx.doi.org/doi:10.1016/j.sleep.2014.05.005 SLEEP 2462
To appear in:
Sleep Medicine
Please cite this article as: Amanda L. Richdale, Emma Baker, Michelle Short, Michael Gradisar, The role of insomnia, pre-sleep arousal, and psychopathology symptoms in daytime impairment in adolescents with high-functioning autism spectrum disorder, Sleep Medicine (2014), http://dx.doi.org/doi:10.1016/j.sleep.2014.05.005. This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
The role of insomnia, pre-sleep arousal, and psychopathology symptoms in daytime impairment in adolescents with high-functioning autism spectrum disorder Amanda L. Richdale1, Emma Baker1, Michelle Short2 & Michael Gradisar3
1
Olga Tennison Autism Research Centre, School of Psychological Science, La Trobe
University, Melbourne, Australia 2
Centre for Sleep Research, University of South Australia, Adelaide, Australia
3
School of Psychology, Flinders University, Adelaide, Australia
Highlights Sleep and psychopathology in adolescents with autism spectrum disorder are examined. Insomnia and psychopathology were common in these adolescents with ASD. Psychopathology was associated with daytime functioning in adolescents with ASD.
Sleep was associated with daytime functioning in adolescents with ASD.
Our results have clinical implications for treating of these problems in ASD.
Correspondence to: Amanda Richdale Olga Tennison Autism Research Centre School of Psychological Science La Trobe University
Page 1 of 32
Kingsbury Drive, Bundoora VIC, 3086 AUSTRALIA p: +61 3 9479 1742 f: +61 3 9479 1956 email: [email protected]
Page 2 of 32
Abstract Objectives: Sleep disturbance and psychopathology are common during adolescence and are highly prevalent in individuals with a diagnosis of Autism Spectrum Disorder (ASD). The aim of this study was to investigate relationships between sleep disturbance, psychopathology symptoms, and daytime functioning in adolescents with high-functioning autism spectrum disorder (HFASD) compared to typically developing (TD) adolescents. Methods: Twenty-seven adolescents with HFASD and 27 age and sex-matched TD adolescents completed questionnaires related to sleep, psychopathology, and daytime functioning. Participants also completed a 7-day sleep/wake diary. A sub-sample of HFASD adolescents (55%) and all the TD adolescents wore an actigraphy monitor concurrently with the sleep diary. Results: Adolescents with HFASD had significantly higher scores for depressed mood, anxiety and pre-sleep arousal compared with TD adolescents, and poorer daytime functioning. There were more significant correlations between sleep variables and psychopathology variables, and sleep variables and daytime functioning in the HFASD group, than in the TD group. Standard regression found that sleep variables significantly accounted for 57% of the variance in daytime functioning symptoms of insufficient sleep in the HFASD group, while psychopathology variables accounted for 63% of the variance in daytime functioning. Conclusions: Both sleep disturbance and psychopathology are more prevalent in adolescents with HFASD and are major contributors to poor daytime functioning in these individuals.
Page 3 of 32
Keywords: Autism, Insomnia, Daytime Functioning, Anxiety, Arousal, Depression, Adolescence
Page 4 of 32
1.
Introduction Children and adolescents with an Autism Spectrum Disorder (ASD) are diagnosed on
the basis of atypical development of social interaction and social communication, as well as a restricted repertoire of interests and activities [1] (American Psychiatric Association, 2013). Intellectual capacity is often impaired, however people with an IQ >70 are classified as high-functioning ASD (HFASD). What is not captured by diagnostic criteria is that, relative to their peers, they are a population with higher rates of mood disorders [2, 3]. For instance, a recent meta-analysis found that 39.6% of children with ASD less than18 years had one or more co-morbid DSM-IV anxiety disorders [4]. Parents also report high levels of anxiety (79%) and depression (54%) in their school-aged children (aged 6-16 yrs) with high-functioning autism [5]. Anxiety symptoms experienced by children and adolescents with ASD include symptoms akin to somatic hyperarousal, such as ‘butterflies’, ‘nausea’ and ‘sweating’, as well as symptoms of cognitive hyperarousal such as ‘racing thoughts’ [6]. If these hyperarousal symptoms extend to the evening, they may inhibit their natural sleep onset process. Hyperarousal has been theorized to underlie both anxiety and insomnia symptoms in typically developing populations, but links with depression are more tenuous [7]. Presleep arousal, which includes both physiological processes (e.g., rapid heartbeat) and cognitive processes (e.g., an inability to stop ‘racing thoughts’) may significantly delay sleep onset, and over time may lead to insomnia symptoms [8]. Recently, Gregory and colleagues [8] assessed pre-sleep arousal in 123 children aged 8 to 10 years. Both somatic and cognitive arousal predicted child-reported sleep scores. Given several studies have now found high rates of both sleep disturbances and psychopathology in children and
Page 5 of 32
adolescents with HFASD [9-12], the important contribution of pre-sleep arousal to the sleep difficulties experienced by adolescents with HFASD remains unexamined. Empirical research supports theories of insomnia which posit that pre-sleep arousal plays a primary role in its development and maintenance [13, 14], and there is substantial evidence from TD adult and adolescent populations that sleep disruption and insomnia lead to poor daytime functioning, anxiety, and depression [7, 15, 16]. However, the associations between these factors in ASD adolescents have not been examined. Knowledge of such relationships may elucidate mechanisms involved between these often cited 'bi-directional relationships' between sleep and adaptive functioning (e.g., anxiety; [7, 17, 18]), which may in turn suggest effective treatment strategies to reduce insomnia symptoms and associated psychopathologies in HFASD populations. Thus, the aim of this study was to explore the relationships between pre-sleep arousal, insomnia symptoms, anxiety, depression, and daytime functioning in HFASD adolescents as compared with typically developing (TD) adolescents. 2.
Method and Materials
2.1
Participants Twenty-seven adolescents (Mage = 15.5±1.3yrs, 82%m) with a clinical diagnosis of
HFASD and 27 TD adolescents matched on age and gender (Mage = 15.5±1.1yrs, 82%m) participated. TD adolescents’ data were from an existing database of adolescents attending South Australian secondary schools [19]. Data were collected between May, 2010 and December, 2010. The two groups did not differ on puberty status, χ² (1, n = 49) = 0.17, p = 0.68, V = 0.05 [20]. The Social Communication Questionnaire (SCQ) [21] was completed by 25 of the 27 HFASD parents (M = 20.2, SD = 5.8). For the remaining two adolescents, 1
Page 6 of 32
parent provided their child’s diagnostic report, confirming an ASD diagnosis and the other was a client of an autism network that required a confirmed ASD diagnosis. All participants were attending mainstream secondary school. On a telephone screening questionnaire, 12 parents of HFASD adolescents provided an IQ score > 70 based on previous standardized assessments. All other parents indicated their child could read at an average to above average level. A complete description of the sample and sample recruitment can be found elsewhere [19]. 2.2
Sleep Measures
2.2.1
Insomnia Insomnia symptoms and severity were assessed using a modified Sleep Habits
Survey (mSHS) consisting of questions relating to sleep scheduling, sleep disturbances, insomnia symptoms , and daytime sleepiness. The mSHS was adapted from the School Sleep Habits Survey [22]. It is a 2-week retrospective questionnaire with 79 questions relating to sleep scheduling, sleep disturbances, and insomnia symptoms. Within the mSHS a set of questions based on the insomnia criteria within the ICSD-2 [23] were used to determine if adolescents met criteria for the definition of insomnia. Adolescents indicated if they experienced difficulties with initiating sleep, maintaining sleep or if sleep was nonrestorative, and if ‘yes’ they then indicated the symptom severity (from mild to very severe) and provided an estimate of duration (from 1 week to more than 6 months). Adolescents met criteria if they experienced at least one insomnia symptom, that the problem had lasted for at least one month and they also indicated impairment in daytime functioning (e.g., attention, concentration or memory impairment). Further details are reported elsewhere [19].
Page 7 of 32
2.2.2
Sleep Participants completed a 7-day sleep/wake diary (Mon-Sun). The following sleep
parameters were evaluated; time in bed (TIB), total sleep time (TST), sleep latency (SoL), wake after sleep onset (WASO) and sleep efficiency (SE%). Further details regarding the sleep diary are reported elsewhere [20]. Fifteen (55%) of the HFASD adolescents and all TD adolescents wore a MicroMini Motionlogger (Actigraphy) on their non-dominant wrist for the duration of the 7-day sleep/wake diary period. Data were digitized in 1-minute epochs using zero crossing mode, with a sensitivity of 0.05g and a bandwidth of 2-3 Hz, and analysed with Action W2 software (AMI) using the Sadeh algorithim. This algorithim has been validated for use with adolescent populations [24]. Further details regarding scoring and calculations of sleep parameters are reported elsewhere [19]. 2.2.3 Daytime Functioning The Chronic Sleep Reduction Questionnaire (CSRQ) was used to measure daytime functioning. The CSRQ provides a measure of the symptoms of chronic sleep reduction and thus the impact of sleep debt in children and adolescents [25]. It consists of 20 questions answered on a 3-point scale, and comprises four sub-scales measuring daytime functioning symptoms relating to: Shortness of Sleep (6 items), Sleepiness (4 items), Loss of Energy (5 items), and Irritation (5 items). A higher total score is a strong indicator of worse daytime functioning. The reliability and validity of the English version of the CSRQ was assessed on 236 Australian adolescents, average age 15.5 years [26]. It showed the same factor structure as the original Dutch version and good reliability with α = .87. Internal consistency here was excellent for the HFASD group with α = .87 and good for the TD group α = .73.
Page 8 of 32
2.3
Psychopathology Measures
2.3.1
Depressed Mood The Centre for Epidemiological Studies Depression scale (CES-D) was used to
measure depressed mood. The CES-D [27] is a short, self-report questionnaire designed to measure depressive symptomatology in the general population. It contains 20 items, which are symptoms of depression that have been used in previously validated, longer scales. Questions are answered on a 4-point scale with scores >16 representing risk for clinical depression. The CES-D contains one question about sleep ‘My sleep is restless’. This question was removed for the analyses reported here. In the current study, reliability for the scale with this item removed was excellent; α = .89 for the HFASD group and good for the TD group, α = .74. 2.3.2
Anxiety The anxiety subscale of the Depression, Anxiety and Stress Scale (DASS-21) was
used to assess general anxiety [28]. It consists of seven self-report items that assesses the severity of the core symptoms of anxiety, with participants rating each item on a 3-point scale. A total score is generated, which when multiplied by two gives a clinical score. Clinical scores < 8 are considered in the normal range. The reliability of the scale in the current study was excellent for the HFASD group, α = .86 and moderate for the TD group, α = .54 2.3.3
Pre-sleep Arousal The Sleep Anticipatory Anxiety Questionnaire (SAAQ) was used to measure pre-
sleep arousal. The SAAQ is a 10-item self-report questionnaire that measures a respondent’s level of anxiety related to sleep (pre-sleep arousal) on a 4-point scale (e.g., My
Page 9 of 32
heart is beating rapidly; I worry that I won’t get enough sleep) [29]. Three scores are obtained from the SAAQ: a total score (SAA-T) measuring overall anxiety about sleep, and two sub-scores (5 items each) measuring self-reported cognitive (SAA-C) and somatic (SAA-S) arousal while trying to fall asleep at night. Higher scores indicate greater pre-sleep arousal. In the current study internal consistency was excellent for the HFASD group, α = .92 and the TD group, α = .87 2.4
Procedure Institutional ethics approval was granted (Approval Numbers GE10/0009 1620 and
FUSBREC 4057; Approval Number HEC10-029). Families of adolescents with ASD who responded to an advertisement completed a telephone-screening questionnaire to determine the adolescent’s eligibility to participate. A letter of introduction, information about the study and a consent form were then posted to eligible families and after receipt of consent the adolescent and their parent or guardian was sent a study pack containing the research materials, including the actigraphy motion-logger where applicable. Prior to recruitment, HFASD adolescent identification codes were randomly selected for the actigraphy component of the study. When participants consented to the study, they were assigned an identification code, and if they were assigned a code that was associated with actigraphy they were invited participate in this part in this study. All HFASD participants assigned a code linked to the actigraphy agreed to complete this component of the study. Sleep diary and actigraphy data were collected for seven consecutive days, and participants were contacted by one of the researchers (EB) once during this period to check recording. Materials were all returned by reply-paid post. 2.5
Data Analysis
Page 10 of 32
Three HFASD adolescents did not complete the sleep diary, however none of these adolescents had been randomly selected to wear actigraphy monitors. Details are reported in Baker et al. [19]. A small number of responses were missing from questionnaires for the HFASD participants. Where there was only one item response missing from a scale the mean response for that subscale or scale was substituted. Three participants were each missing question 7 (Shortness of Sleep subscale) on the CSRQ; one participant was missing one question from each of the SAAQ and the DASS-21 anxiety scales; and two participants were missing one question each from the CES-D. If two or more items were missing, the respondent was removed from the analysis. As a result, one adolescent was excluded because there were no completed questionnaires and one participant was excluded from the SAAQ total scores analyses, as two questions were not completed. Data screening indicated that CSRQ and SAAQ all met assumptions for normality. There were four outliers for anxiety, one of which was extreme, and two outliers for depression, one of which was also extreme; all were from the HFASD group. Depression and anxiety are commonly associated with HFASD and thus outliers and extreme scores may be expected. The means (2.73, 13.43) and 5% trimmed means (2.28, 12.63) were not very different for anxiety or depression respectively and parametric statistics are robust to violations of normality [30] thus, these adolescents remained in the analyses and no data transformations were used. A series of Student’s t-tests for independent samples was employed to examine group differences on psychopathology variables. MANOVA was used to examine group differences for the CRSQ and SAAQ subscales. Pearson’s correlation analyses were used to
Page 11 of 32
determine the associations between sleep parameters, CSRQ, and psychopathology variables. Standard multiple regression was used to examine predictors of chronic sleep problems in both groups of adolescents using the CSRQ total score (daytime functioning) as the dependent variable and sleep or psychopathology measures as predictors. While the two sample sizes were small the minimum suggested ratio of cases to IVs is 5:1 [31]. Thus up to three predictor variables that correlated significantly with the CSRQ were considered for each regression. 3.
Results
3.1
Psychopathology and CSRQ scores in TD and HFASD Adolescents First, we examined whether adolescents with HFASD and TD adolescents differed
on anxiety, depression and pre-sleep arousal (see Table 1). The HFASD group had significantly higher depressed mood (t [37.08] = 2.30, p = .027, η2 = .09) and anxiety (t [34.34] = 2.17, p = .037, η2 = .08) compared to TD adolescents, both with moderate effect size. Furthermore, 10 (38.5%) HFASD adolescents and five (18.5%) TD adolescents had depression scores above the CES-D clinical cut-off (16) and five (19.2%) HFASD adolescents but no TD adolescents had clinical anxiety scores (> 7). Four adolescents in the HFASD group with scores above the clinical cut-off for anxiety were also above the clinical cut-off for depression. Adolescents with HFASD also had significantly higher pre-sleep arousal (SAA-T) than TD adolescents (t (50) = 2.25, p = .029, η2 = .09) with moderate effect size. Examining the two subscales, there was no statistically significant group effect (Wilks = .91, F (2, 49) = 2.48, p = .094, partial 2 = .09), but the effect size was moderate. The
Page 12 of 32
groups differed significantly on cognitive arousal (F (1, 50) = 4.73, p = .034, partial η2 = .09; moderate effect size), but not on the somatic subscale (F (1, 50) = 3.73, p = .059, partial η2 = .07; moderate effect size). After collapsing the SAAQ responses to give two categories, “Agree” (score of 2 or 3) and “Disagree” (score of 0 or 1) we also examined the individual questions, both to see which aspects of arousal most often occurred, and whether there were any differences in their occurrence across the two groups (Table 2). A larger proportion of HFASD adolescents positively endorsed all statements on the SAAQ, however only one statement, ‘I worry that I won’t be able to fall asleep’ was endorsed by significantly more HFASD than TD adolescents. While the HFASD adolescents had worse daytime functioning (CSRQ) than the TD adolescents (Table 1); this was not significant (t (42.36) = 1.54, p = .13, η2 = .04). Examining the four daytime functioning (CSRQ) subscales, there was a significant group effect (Wilks λ = .79, F (4, 48) = 3.17, p = .022, partial η2 = .21) with large effect size. Subscale scores were similar for Shortness of Sleep, Sleepiness, and Irritation but the HFASD group had a significantly higher mean score for the Loss of Energy sub-scale (F [1, 51] = 37.23, p = .002, partial η2 = .17) with strong effect size. 3.3
Associations between Sleep, Psychopathology and Daytime Functioning Pearson correlations were used to examine the linear relationships between sleep,
psychopathology and daytime functioning in HFASD and TD adolescents (Tables 3 and 4). Overall, there were more significant correlations between sleep variables and psychopathology, and sleep variables and daytime functioning in the HFASD group, than in the TD group. All psychopathology measures were moderately or strongly associated with daytime functioning in HFASD adolescents. Reporting a sleep problem, ICSD-2
Page 13 of 32
defined insomnia, and sleep variables from the sleep diary (bedtime, wake time and SE%) and actigraphy (sleep onset time and SoL) were all significantly associated with worse daytime functioning in HFASD adolescents. Reporting a sleep problem was strongly associated with depression and moderately or strongly associated with all measures of anxiety. ICSD-2 defined insomnia, and number of insomnia symptoms, were both related to all measures of anxiety, also the latter was strongly associated with depression. On the sleep diary, SE% and SoL were associated with depression and anxiety, also depression was related to wake time. For actigraphy, sleep duration was associated with SAA-C, while sleep onset was associated with both SAA-T and SAA-C. Significant associations for TD adolescents were moderate (Table 4). Depression and SAA-C were associated with ICSD-2 defined insomnia, while anxiety was related to reporting a sleep problem. On the sleep diary, night waking was associated with SAA-S. On actigraphy, SAA-T was associated with sleep length, and SAA-C was associated with both sleep length and wake time. In TD adolescents, daytime functioning was associated only with reporting insomnia and meeting criteria for ICSD-2 defined insomnia. Counterintuitively there was a moderate, non-significant negative correlation between WASO and daytime functioning; wake-time was also moderately but non-significantly associated with daytime functioning. 3.4
Predicting Daytime Functioning Using standard multiple regression the ability of sleep variables to predict daytime
functioning (CSRQ scores) was examined; next the ability of psychopathology variables to predict daytime functioning was examined. In selecting the variables, we examined those sleep and psychopathology variables that were significantly correlated with daytime
Page 14 of 32
functioning in each group (see Tables 3 and 4). Within the HFASD group, several independent variables were highly correlated (r > .70) however examination of Mahalanobis Distance and Cook’s Distance indicated that this was not a problem and inspection of Normal P-P plots and scatterplots met assumptions of normality. To take account of small sample size, adjusted R2 is reported for the final model [32]. For the HFASD group three predictor variables were entered into the sleep regression, reporting a sleep problem, number of ICSD-2 insomnia symptoms and morning wake time. The model was significant, adjusted R2 = .57, F (3, 20) = 11.23 p < .001, and accounted for 57% of the variance in CSRQ scores. Number of ICSD-2 insomnia symptoms was a significant, unique predictor within the model (p = .009) accounting for 15% of the variance in CSRQ scores in the HFASD group. Examining psychopathology as a predictor depression, anxiety, and SAA-T scores were entered in the regression model. The model was significant, adjusted R2 = .63, F (3, 20) = 13.81, p < .001, that is the model accounted for 63% of the variance in CSRQ scores. Sleep anxiety (SAA-T) was a significant, unique predictor within the model (p = .005) accounting for 16% of the variance in CSRQ scores. As both sleep and psychopathology variables independently accounted for a large proportion of the variance in CSRQ scores for the HFASD group we conducted hierarchical regression analyses to explore whether each of the psychopathology variables explained any additional variance in the CSRQ total score, after controlling for the sleep variables. In the first hierarchical regression the addition of DASS-anxiety at step 2 accounted for an additional 7% of the variance in CSRQ scores, F change (1, 19) = 4.48, p = .048, and the overall model accounted for 63.5% of the variance, adjusted R2 = .635, F (4, 19) = 11.08, p
Page 15 of 32
< .001. In the second hierarchical regression the addition of pre-sleep arousal (SAA-T) at step 2 accounted for an additional 15% of the variance in CSRQ scores, F change (1, 18) = 11.71, p = .003, and the overall model accounted for 72% of the variance, adjusted R2 = .72, F (4, 19) = 15.44, p < .001. In the final hierarchical regression, the addition of CES-D depression at step 2 accounted for an additional 11% of the variance in CSRQ scores, F change (1, 19) = 8.15, p = .01, and the overall model accounted for 68% of the variance, adjusted R2 = .68, F (4, 19) = 13.47, p < .001. Only reporting a sleep problem, and ICSD-insomnia, whose criteria overlap, were significantly associated with daytime functioning in the TD group, thus regression analyses were not conducted for this group. 4.
Discussion
4.1
Sleep and Daytime Functioning As we have reported in detail elsewhere [19] adolescents with HFASD experience
more problems associated with sleep than TD adolescents. However, HFASD adolescents did not report significantly worse daytime functioning than TD adolescents. While the HFASD adolescents tended to report worse daytime functioning than TD adolescents, only ‘loss of energy' was significantly worse for the HFASD adolescents. This finding is consistent with the presence of more daytime fatigue reported by these adolescents with HFASD [19]. As expected, sleep variables were significantly associated with daytime functioning in the HFASD group, but not in the TD group. Correlations between sleep parameters and daytime functioning for the TD group were weak to moderate. Lack of significant correlations within the TD group may be attributed to low power due to our small sample
Page 16 of 32
size. Nevertheless, daytime functioning was moderately or strongly associated with all sleep variables for the HFASD adolescents. The majority of these correlations were significant, suggesting that in our sample poor sleep has a more deleterious impact on daytime functioning in HFASD than TD adolescents. 4.2
Psychopathology As expected, adolescents with HFASD had significantly more self-reported
symptoms of psychopathology than the TD adolescents. Increased prevalence of anxiety and depression in individuals with an ASD compared with TD individuals has been reported previously [3], but pre-sleep arousal has not previously been examined. In their meta-analysis, van Steensel et al. [4] reported the prevalence of GAD at 15%, and while the presence of any anxiety disorder averaged 39.6%, specific phobias (30%) and OCD (17%) were the most common; the latter are not measured by the DASS. In 38 adolescents (10-17 years) with HFASD, rate of any DSM-IV anxiety disorder by parent-report (semi-structured interview) was 28.9%, with phobias again being the most common. Thus, the rate of clinical levels of anxiety (19.5%) reported by our HFASD adolescents is within the range expected. The reported rate of clinical levels of depressive symptoms (38.5%) was within the range reported by parents of children and adolescents with HFASD. For example, Mayes et al. [5] found that 54% of parents of 6-16 year-olds with HFASD reported clinical levels of depression in their children, while using a semi-structured interview with parents, Mazefsky et al. [33] found that 18.4% of 10-17 year-olds with HFASD met criteria for any DSM-IV depressive disorder. Variability in reported rates of anxiety and depression in HFASD may relate to several factors including sample size, recruitment bias or sampling method, use of different
Page 17 of 32
measures of psychopathology, and whether parent-report or self-report is used. Both anxiety and depression are reported to increase with age in ASD [4, 5], and majority of studies to date have used only parent-report to examine psychopathology. In TD samples, there is often poor parent-child agreement for measures of psychopathology [33, 34]. Mazefsky et al. [33] argued that caution should be exercised with self-reported psychopathology in young people with HFASD. However Blakely-Smith et al. [33] found overall moderate parent-child agreement for anxiety symptoms in 63 children and adolescents (8-14 yrs) with HFASD. Furthermore, Richdale and Baglin [11] found some agreement for parent and child reported anxiety but little agreement on depression in 17, 8to 12-year-old children with HFASD. Taken together, agreement about the presence of psychopathology between parent- and child-report in HFASD samples may be similarly variable to that found in TD samples. In line with previous research [8, 35], our adolescents were more likely to experience cognitive arousal associated with sleep rather than somatic arousal. Furthermore, the HFASD adolescents experienced significantly more pre-sleep arousal, especially cognitive arousal, than did the TD adolescents. Additionally, significantly more HFASD adolescents endorsed the statement ‘I worry that I won’t be able to fall asleep’ than did TD adolescents. Our findings are consistent with self-reports of symptoms of cognitive and somatic arousal by children and adolescents with HFASD [6]. Thus, pre-sleep arousal, most commonly cognitive arousal, appears to contribute significantly to insomnia in these HFASD adolescents. 4.3
Sleep, Psychopathology, and Daytime Functioning
Page 18 of 32
As predicted anxiety, depression, and pre-sleep arousal were all associated moderately to strongly with daytime functioning (CSRQ), including subscales, for the HFASD adolescents, with almost all correlations being significant. In contrast, in the TD group, there were few significant moderate or strong associations between daytime functioning and psychopathology, with only anxiety and pre-sleep cognitive arousal having a moderate and significant association with daytime functioning. This suggests that for the HFASD group there is considerable overlap between poor sleep and elevated symptoms of psychopathology with both contributing significantly to poor daytime functioning in these young people. We conducted regression analyses to explore how well sleep and psychopathology variables predicted poor daytime functioning in the HFASD group. Sleep variables accounted for over half the variance in daytime functioning, with the number of ICSD-2 insomnia symptoms being a unique predictor. Similarly, around two thirds of the variance in daytime functioning was accounted for by psychopathology (anxiety, pre-sleep arousal, depression) and pre-sleep arousal was a unique predictor. Finally, using separate hierarchical regressions we explored the ability of each psychopathology measure to account for additional variance in daytime functioning after the contribution of the sleep variables had been accounted for. Anxiety, pre-sleep arousal, and depression all accounted for additional variance. Our findings thus suggest that there is a striking overlap between the daytime symptoms of chronic poor sleep and psychopathology for adolescents with HFASD where all measures of psychopathology showed significant relationships with daytime functioning as well as with sleep variables. This highlights the overlap between psychopathology and
Page 19 of 32
insomnia in individuals with HFASD, supporting previous reports of associations between both anxiety and depression and poor sleep [9-11, 36]. In particular, our results clearly suggest for the first time that pre-sleep arousal and therefore hyperarousal may play a significant role in insomnia in HFASD. The high rate of sleep problems and anxiety in children with HFASD and their continuation into adolescence is also likely to be a significant pre-disposing factor for the development of depression in these young people. While our findings require replication, future research should also explore whether in young children with HFASD, anxiety precedes sleep problems or vice versa or whether they arise together. 4.4
Clinical Implications
Given the known relationships between psychopathology and sleep disturbance in the general population [37], and the strong relationships found between psychopathology and sleep disturbance in the HFASD adolescents here, treating sleep disturbance or psychopathology in isolation in these adolescents may not lead to successful treatment outcomes. The presence of anxiety, depression or insomnia as the presenting complaint should be a red flag for the exploration of the other disorders as potential comorbid conditions. Furthermore, the impact of the treatment of anxiety or depression on insomnia or vice versa should be monitored, and co-treating the insomnia as part of any anxiety or depression intervention should occur. While both high rates of insomnia and psychopathology are acknowledged in HFASD and associations between the two have been reported [9-11, 36], emerging treatment studies do not consider these as comorbid conditions that require parallel treatment. Indeed, even monitoring the impact of the treatment of one condition has not been reported.
Page 20 of 32
Furthermore, the apparent importance of pre-sleep arousal for insomnia in HFASD suggests that treatments that reduce cognitive and somatic arousal associated with bedtime and sleep onset may be effective in the treatment of insomnia in this population. This has not been explored. Researchers are beginning to explore the usefulness of using or adapting cognitive behaviour therapy (CBT) for the treatment of anxiety in HFASD, with a small number of studies emerging in the past 5 years [e.g., 38]. There are concerns that difficulties inherent in ASD with regard to understanding their own and others cognitions and emotions and their literal thinking may impact on the effectiveness of CBT in this population. However there are now several treatment studies that suggest CBT can be effective, especially where these programs incorporate adaptations that allow for the social and adaptive behaviour difficulties that are associated with ASD [39]. This suggests that CBT-Insomnia (CBT-I) should be an effective treatment for insomnia in young people with HFASD. As for CBT, some modifications to CBT-I may be required, however the structured behavioural components of CBT-I are likely to be effective. The incorporation of stress reduction techniques (e.g., mindfulness) together with strict sleep hygiene and restriction of time in bed to time spent sleeping may be advantageous. Behavioural interventions including bedtime fading techniques have been shown to be useful treatments for sleep onset insomnia in young children with ASD [40, 41]. 4.5
Strengths and Limitations of the study The major strength of this study is that it comprised a sample of adolescents only
and participants were matched on age and sex [19]. A further strength is that we had both sleep diaries and actigraphy as measures of sleep and we obtained self-reports from the adolescents on measures of sleep and psychopathology. Further, this is the first study, that
Page 21 of 32
we are aware of, that has directly investigated pre-sleep arousal in adolescents with HFASD. Our findings indicate that pre-sleep arousal in this population is important for understanding the development and continuation of the insomnia frequently seen in this population. Given, the small sample size the power to detect differences between the two groups on daytime functioning may have been reduced. However, the daytime functioning results were similar to those reported by Dewald et al. [26], correlations between daytime functioning and psychopathology and sleep variables in the HFASD group were predominantly moderate or strong, while internal consistency for the three psychopathology scales was excellent, whereas for the TD adolescents it was moderate to good. A further limitation is the exploratory nature of the regression analyses, including restrictions imposed by our sample size. Replication of our findings with larger samples and examination of both insomnia and psychopathology in treatment studies will be important in future research, particularly in HFASD populations. This should clarify the role of psychopathology in the manifestation and maintenance of sleep disturbance in HFASD. 4.6
Conclusion
In conclusion, sleep and psychopathology were significant contributors to daytime functioning in the HFASD group, with moderate to strong correlations between measures and a large proportion of variance in daytime functioning accounted for by these variables. These relationships were considerably fewer and more modest in the TD group. Further pre-sleep arousal, in particular, cognitive arousal was prominent in the HFASD group. Thus, it appears that both chronic insomnia and elevated symptoms of psychopathology are major contributors to poor daytime functioning in HFASD. Given that anxiety may be more
Page 22 of 32
prevalent in lower functioning individuals with ASD than in HFASD [4], the role of anxiety in insomnia across the autism spectrum should be a focus of future investigation.
Page 23 of 32
References [1] American Psychiatric Association. Diagnostic and Statistical Manual of Mental Disorders. 5th ed. Arlington, VA: American Psychiatric Publishing, 2013. [2] American Academy of Child and Adolescent Psychiatry. Practice parameters for the assessment and treatment of children and adolescents with depressive disorders. AACAP. J Am Acad Child Adoles Psychiatry 2007;46(11):1503-1526. [3] Strang JF, Kenworthy L, Daniolos P, Case L, Wills MC, Martin A, et al. Depression and anxiety symptoms in children and adolescents with autism spectrum disorders without intellectual disability. Res Autism Spect Dis 2012;6(1):406-412. [4] van Steensel FJ, Bogels SM, Perrin S. Anxiety disorders in children and adolescents with autistic spectrum disorders: A meta analysis. Clin Child Fam Psychol Rev 2011;14(3):302-317. [5] Mayes SD, Calhoun SL, Murray MJ, Ahuja M, Smith LA. Anxiety, depression, and irritability in children with autism relative to other neuropsychiatric disorders and typical development. Research in Autism Spectrum Disorders 2011;5(1):474-485. [6] Ozsivadjian A, Knott F, Magiati I. Parent and child perspectives on the nature of anxiety in children and young people with autism spectrum disorders: a focus group study. Autism 2012;16(2):107-121. [7] Gregory AM, Sadeh A. (2012). Sleep, emotional and behavioral difficulties in children and adolescents Sleep Med Rev 2012;16(2):129-136. [8] Gregory AM, Willis TA, Wiggs L, Harvey AG, STEPS Team. Presleep arousal and sleep disturbances in children. Sleep 2008;31(12):1745-1747.
Page 24 of 32
[9] Mayes SD, Calhoun SL. (2009). Variables related to sleep problems in children with autism. Res Autism Spect Dis 2009;3(4): 931-941. [10] Goldman SE, McGrew SG, Johnson KP, Richdale AL, Clemons T, Malow BA. Sleep is associated with problem behaviors in children and adolescents with autism spectrum disorders. Res Autism Spect Dis 2011;5(3):1223-1229. [11] Richdale AL, Baglin C. Self-report and caregiver-report of sleep and psychopathology in children with high-functioning autism spectrum disorder: A pilot study. Dev Neurorehabil. Forthcoming 2013 [12] Allik H, Larsson JO, Smedje A. Insomnia in school-age children with Asperger syndrome or high-functioning autism. BMC Psychiatry 2006;6: 6-18. [13] Harvey AG. A cognitive model of insomnia. Beh Res Ther 2002;40(8):869-93. [14] Harvey AG. A cognitive theory and therapy for chronic insomnia. Journal of Cognitive Psychotherapy 2005;19: 41-59. [15] Dewald JF, Meijer AM, Oort FJ, Kerkhof GA. The influence of sleep quality, sleep duration and sleepiness on school performance in children and adolescents: a meta-analytic review. Sleep Med Rev 2010;14:179-189. [16] Lovato N, Gradisar M. (in press). A meta-analysis and model of the relationship between sleep and depression in adolescents: Recommendations for future research and clinical practice. Sleep Med Rev (in press). [17] Dahl RE, Harvey AG. (2007). Sleep in children and adolescents with behavioral and emotional disorders. Sleep Med Clins 2007;2:501-511. [18] Leahy E, Gradisar M. (2012). Dismantling the bi-directional relationship between paediatric sleep and anxiety. Clinical Psychologist 2012;16:44-56.
Page 25 of 32
[19] Baker E, Richdale A, Short M, Gradisar M. An investigation of sleep patterns in adolescents with high-functioning autism spectrum disorder compared with typically developing adolescents. Dev Neurorehabil 2013;16(3):155-165. [20] Carskadon MA, Acebo C. A self-administered rating scale for pubertal development. J Adolesc Health 1993;14(3):190-195. [21] Rutter M, Bailey A, Lord C. The social communication questionnaire manual. Los Angeles: Western Psychological Services, 2003. [22] Wolfson AR, Carskadon MA, Acebo C, Seifer R, Fallone G, Labyak SE, et al. Evidence for the validity of a sleep habits survey for adolescents. Sleep 2003;26(2):213216. [23] American Academy of Sleep Medicine. The international classification of sleep disorders: diagnostic and coding manual. 2nd ed. Westchester, III: American Academy of Sleep Medicine, 2005. [24] Sadeh A, Sharkey KM, Carskadon MA. Activity-based sleep-wake identification: An empirical test of methodological issues. Sleep 1994;17:201-207. [25] Meijer AM. Chronic sleep reduction, functioning at school and school achievement in preadolescents. J Sleep Res 2008;17(4):395-405. [26] Dewald JF, Short MA, Gradisar M, Oort FJ, Meijer AM. The chronic sleep reduction questionnaire (CSRQ): A cross-cultural comparison and validation in Dutch and Australian adolescents. J Sleep Res 2012;21(5):584-594. [27] Radloff LS. The CES-D scale: A self-report depression scale for research in the general population. Appl Psych Meas 1977;1(3):385-401.
Page 26 of 32
[28] Lovibond PF, Lovibond SH. The structure of negative emotional states: Comparison of the Depression Anxiety Stress Scales (DASS) with the Beck Depression and Anxiety Inventories. Behav Res Ther 1995;33(3):335-343. [29] Bootzin R, Shoham V, Kuo T. Sleep anticipatory anxiety questionnaire: A measure of anxiety about sleep. Sleep Res 1994; 23:188. [30] Norman G. Likert scales, levels of measurement and the “laws” of statistics. Adv Health Sci Educ 2010;15(5):625-632. [31] Coakes SJ, Steed L, Ong C. SPSS 16.0 for windows: Analysis without anguish. Australia: John Wiley and Sons, 2009. [32] Pallant J. SPSS Survival Manual: A step by step guide to data analysis using the SPSS program. 4th ed. Crows Nest, NSW: Allen & Unwin, 2011. [33] Mazefsky CA, Kao J, Oswald DP. Preliminary evidence suggesting caution in the use of psychiatric self-report measures with adolescents with high-functioning autism spectrum disorders. Res Autism Spect Dis 2011;5(1):164-174. [34] Blakeley-Smith A, Reaven J, Ridge K, Hepburn S. Parent–child agreement of anxiety symptoms in youth with autism spectrum disorders. Res Autism Spect Dis 2012;6(2):707716. [35] Lichstein KL, Rosenthal TL. Insomniacs' perceptions of cognitive versus somatic determinants of sleep disturbance. J Abnorm Psychol 1980;89(1):105-107. [36] Paavonen EJ, Vehkalahti K, Vanhala R, von Wendt L, Nieminen-von Wendt T, Aronen ET. Sleep in children with Asperger syndrome. J Autism Dev Disord 2008;38(1):41-51.
Page 27 of 32
[37] Breslau N, Roth T, Rosental L, Andreski P. Sleep disturbance and psychiatric disorders: A longitudinal epidemiological study of young adults. Biol Psychiatry 1996;39(6):411-418. [38] Chalfant AM, Rapee R, Carroll L. Treating anxiety disorders in children with high functioning autism spectrum disorders: A controlled trial.J Autism Dev Disord 2007; 37:1842-1857. [39] McNally Keehn RH, Lincoln AJ, Brown MZ, Chavira DA. The coping cat program for children with anxiety and autism spectrum disorder: A pilot randomized controlled trial. J Autism Dev Disord 2013;43:57-67. [40] Moon EC, Corkum P, Smith IM. Case study: A case-series evaluation of a behavioral sleep intervention for three children with autism and primary insomnia. J Ped Psychol 2011;36(1):47-54. [41] Turner KS, Johnson CR. Behavioral interventions to address sleep disturbances in children with autism spectrum disorders: A review. Topics Early Childhood Spec Ed 2013;33(3):144-152
Table 1 Groups Means for CSRQ Total Score and Psychopathology Variables HFASD
TD
n
M
SD
n
M
SD
CSRQ
26
37.08
7.79
27
34.30
5.00
Depression
26
16.35
11.32
27
10.63
5.83
Anxiety
26
3.77
4.37
27
1.74
1.95
Page 28 of 32
SAA-S
26
4.04
2.88
27
2.55
2.33
SAA-C
25
7.08
4.27
27
4.81
3.20
SAA-T
25
11.04
6.80
27
7.37
4.89
SAA: Sleep Anticipatory Anxiety
Page 29 of 32
30 Table 2. Examination of Individual SAA-Q Statements for each Group 1
Adolescents Agreeing with each Statement HFASD
TD
(n = 26)
(n = 27)
4 (15.4%)
1 (3.7%)
-
2 (7.7%)
0
-
3 (11.5%)
1 (3.7%)
-
2 (7.7%)
1 (3.7%)
-
13 (50%)
9 (33.3%)
.91
18 (69.2%)
11 (40.7%)
3.27
I worry that I won’t be able to fall asleep
13 (50%)
3 (11.1%)
7.75
I worry that I won’t get enough sleep
13 (50%)
7 (25.9%)
2.32
11 (44%)
8 (29.6%)
.62
8 (32%)
8 (29.6%)
0
SAA-Q Statements My muscles are tense
2
My heart is beating rapidly I feel “shaky”/trembling
2
2
I become short of breath
2
I become aware of my body (feeling itches, sweat, pain, nausea) I can’t stop my mind racing
I worry that I won’t be able to function the next day if I don’t sleep I worry that I will be tired and irritable the next day if I don’t sleep
3
3
2
1
Agree or Strongly Agree the symptom is present. Fisher’s Exact Test probability 3 n = 25 for HFASD group.
2
Page 30 of 32
31
Table 3 Correlations between the CSRQ and Psychopathology Variables CSRQ: HFASD (n = 26)1
CSRQ: TD (n = 27)
Psychopath Total
Short
Irritation
Loss of
Sleepiness
Total
Short
Irritation
Lo
Variable Sleep
Energy
Sleep
En
Depression
.71a
.42c
.72a
.54b
.70a
.30
-.02
.14
.3
Anxiety
.60a
.35
.60a
.45c
.58b
.49b
.23
.32
.
SAA-T
.81a
.53b
.75a
.64b
.75a
.22
.29
-.09
.
SAA-S
.76a
.47c
.66a
.62a
.73a
-.04
.11
-.24
-
SAA-C
.78a
.53b
.75a
.58b
.70a
.36d
.36d
.04
.
1 a
For some correlations, nHFASD = 25 and nTD = 26 due to missing data p ≤ .001, b p ≤ .01, c p ≤ .05, d .05 > p < .10
Page 31 of 32
32 Table 4 Correlations between Psychopathology, CSRQ and Sleep Variables HFASD (n = 26)1
Sleep Variable
TD (n = 27
CES-D
Anxiety
SAA-T
SAA-S
SAA-C
Sleep Problem
-.54b
-.48b-
-.62a
-.48b
-.63a
ICSD Ins
-.46c
-.42c
-.69a
-.54b
b
.53
b
.68
a
.60
a
.68
Bedtime
.28
.18
.37
.31
Wake time
.40
.17
.36
Total sleep
-.27
-.37
-.23
Sleep efficiency
-.43
c
c
-.46
.36
Sleep latency
.51c
.59b
WASO
.06
Sleep onset time Wake time
o
N ICSD Ins
CES-D
Anxiety
SAA-T
-
.62a
-.12
-.38c
-.21
-.69a
-.65a
-.46c
-.31
-.36
a
a
.31
.27
.25
.40
.43c
.16
.03
.02
.35
.35
.55b
.34
.23
.30
-.17
.23
-.22
.04
.15
.13
-.34
.33
-.49
b
.12
-.03
-.20
.33
.32
.29
.33
-.10
.01
.10
-.01
.00
.04
-.06
.19
-.09
.05
.27
.54c
.22
.54c
.35
.62b
.
60c
.20
.05
.01
.41
.24
.44
.39
.44
.42
.17
.23
.35
.49
CSRQ
.73
Sleep Diary
2
Actigraphy
c
Sleep length
-.43
-.04
-.48
-.24
-.61
-.48
-.05
.05
.46c
Sleep latency
.35
.17
.34
.27
.36
.57c
.09
.28
.06
1
nHFASD varies from 23 – 26 participants and nTD varies from 25-27 participants due to missing data 2 n = 15 for HFASD group (for some correlations n = 14 due to missing data). a p ≤ .001, b p ≤ .01, c p ≤ .05
Page 32 of 32
SA
