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article2014
AUT0010.1177/1362361313518994AutismTudor et al.
Original Article
Pain as a predictor of sleep problems in youth with autism spectrum disorders
Autism 2015, Vol. 19(3) 292–300 © The Author(s) 2014 Reprints and permissions: sagepub.co.uk/journalsPermissions.nav DOI: 10.1177/1362361313518994 aut.sagepub.com
Megan E Tudor, Caitlin E Walsh, Emile C Mulder and Matthew D Lerner
Abstract Evidence suggests that pain interferes with sleep in youth with developmental disabilities. This study examined the relationship between pain and sleep problems in a sample of youth with parent-reported autism spectrum disorder (N = 62). Mothers reported on standardized measures of pain and sleep problems. Youth demonstrated atypically high levels of both observed pain and sleep problems. Pain predicted overall sleep disturbance and three specific sleep problems: sleep duration, parasomnias, and sleep-disordered breathing. These specific sleep problems were predicted by specific modalities of nonverbal pain communication (e.g. sleep duration problems were predicted by social communication of pain). Effects were consistent across probing of relevant moderators. These findings suggest that comprehensive assessment of both pain and sleep problems may provide important information for medical and behavioral treatment planning for youth with autism spectrum disorder. Keywords autism, communication, pain, sleep problems While social and communication deficits are considered core characteristics of autism spectrum disorders (ASD), health-related comorbidities are often reported to be common, and may be even more prevalent among youth with ASD than typically developing (TD) youth (e.g. Schieve et al., 2012; Shreck and Richdale, 2011). Two such factors, pain and sleep problems, may increase the likelihood for functional impairments and play an important role in quality of life in this population (Bauman, 2010). Additionally, these variables may in fact be related to one another among youth with intellectual and developmental disabilities (IDD), with pain disrupting sleep (Breau and Camfield, 2011), though no research has examined their relation in children with ASD specifically. Given the high incidence of these health-related problems and their unique impacts on overall functioning, this study seeks to elucidate how these comorbidities may manifest, as well as the magnitude and contours of their relationships in youth with ASD.
wakings, and parasomnias (e.g. night terrors, sleep-walking; Williams et al., 2004). In TD youth, lack of sleep can impair cognitive abilities and increase risk for behavioral problems (e.g. Sadeh et al., 2003). For youth with ASD, sleep problems have been associated with various functional impairments such as increased problem behavior (DeVincent et al., 2007) and exacerbated core symptoms (Hoffman et al., 2005; Schreck et al., 2004; Tudor et al., 2012). While evidence suggests that behavioral treatment (Christodulu and Durand, 2004) and melatonin-based pharmacological interventions (Andersen et al., 2008) may be helpful in improving the sleep of youth with ASD, sleep health is not regularly assessed and integrated into behavioral or medical treatment of these youth. Thus, the consideration of sleep problems may be an important, albeit largely overlooked, area of health-related functioning for youth with ASD.
Sleep problems and ASD Ample research suggests that youth with ASD experience more sleep problems than TD youth (e.g. Hoffman et al., 2006). Both parent report and observational evidence exist for a wide range of specific sleep problems occurring within this population, including sleep onset delay, night
Stony Brook University, USA Corresponding author: Megan E Tudor, Psychology Department, Stony Brook University, Stony Brook, NY 11794, USA. Email: [email protected]
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Pain and ASD Anecdotal reports and clinical impressions classically suggest that youth with ASD may display a blunted or absent response to pain. Notably, the Diagnostic and Statistical Manual of Mental Disorders (4th edition, text rev.; DSMIV-TR; American Psychiatric Association, 2000) indicates a “high threshold for pain” (p. 72) as a descriptive feature of the disorder. Thus far, two observational laboratorybased studies indicate that such youth display responses to pain that are similar to those of TD children, although they may exhibit more facial grimacing when experiencing pain (Messmer et al., 2008; Nader et al., 2004). These findings provide an initial insight into the unique nonverbal communication of pain via objective methods in this population. Together, they suggest that further research on how to adequately assess pain in this population is needed. Assessment of pain is a decidedly complex task (see Breivik et al., 2008) that may be even harder in the ASD population due to social and communication difficulties (Jyonouchi, 2010). The ability to recognize, label, and share particular health needs and experiences of pleasure or discomfort may be impaired (Breau and Burkitt, 2009). As such, youth with ASD may experience pain that goes unreported and, crucially, may be unrelated to a chronic medical condition, such as mild, normative aches and pains that many children might experience in their youth due to mild illness, injury, or digestive discomfort. Furthermore, youth with ASD may experience pain related to sensory integration problems, such as discomfort related to temperature, loud noises, or texture of clothing. Importantly, while youth with ASD may experience difficulty with reporting these various forms of pain, parent report of pain-related behavior does appear to provide a fair estimate of subjective pain experienced by youth with ASD (Nader et al., 2004). The review of a child’s medical history can also serve as a critical piece of a thorough pain assessment (Breau and Burkitt, 2009). Reports of gastrointestinal (GI) complaints and asthma are frequent in youth with ASD and are typically accompanied by pain-related behaviors (e.g. Horvath and Perman, 2002; Schieve et al., 2012). Necessity of medical care may also indicate pain in this population. Youth with ASD are reported as having more doctor visits, emergency care, and long-term medication usage than TD children (Gurney et al., 2006). With special importance to this study, sleep problems may also inform pain assessment for these youth, given that sleep problems serve as indicators for a variety of health problems that may be helpful in medical assessment among TD youth (Huntley et al., 2007; Palermo et al., 2007). Thus, consideration of comorbid medical (including sleep) problems may further inform the understanding of pain-related behaviors in this population of youth, especially those with more communication difficulties.
Relationships between sleep problems, pain, and ASD Pain and sleep problems are evidenced as being highly cooccurring in youth (e.g. Bruusgaard et al., 2000) with approximately half of TD youth with pain also experiencing significant sleep problems (Long et al., 2008). These two factors often exhibit bi-directional predictive relationships with one another, with more sleep problems predicting more pain and more pain predicting more sleep problems (e.g. Moldofsky, 2001). The latter relationship has been examined in youth with various disabilities. Sleep problems increase when pain is reported in populations of youth with physical disabilities (e.g. Wright et al., 2006) and intellectual disabilities (ID) (Ghanizadeh and Faghih, 2009). One previous study has examined the potential relationships between sleep problems and pain in youth with IDD, including ASD (Breau and Camfield, 2011). This study suggested that youth with IDD might be more likely to experience sleep problems, such as parasomnias, sleepdisordered breathing, and night wakings, if they are also reported as having pain-related health problems. Given the evidence for unique sleep and pain-related characteristics in ASD and the disorder’s high comorbidity with ID (Fombonne, 2003), as well as the relation between these characteristics found in other developmental disabilities (DDs) (Breau and Camfield, 2011; Ghanizadeh and Faghih, 2009), an examination of the sleep–pain relationships in youth with parent-reported ASD would fill an important gap in the literature. Such relationships also require careful examination of related factors that may influence the strength or presence of these relationships. As described above, both degree of communication abilities and the presence of pain-related health problems may influence these relationships. Additionally, GI problems and asthma represent specific health problems that are both prevalent in this population (e.g. Horvath and Perman, 2002; Schieve et al., 2012) and may contribute to both pain-related behavior and sleep problem report (e.g. Levy et al., 2006; Stores et al., 1998). Furthermore, the understanding of these relationships could further benefit from considering the particular modalities by which youth with ASD communicate their pain (e.g. social, facial), which may relate to specific sleep–pain relationships. The consideration of specific nonverbal communication may be of paramount importance to interpreting these relationships in this population.
Current study This study aimed to examine pain-related behaviors as a predictor of sleep problems in youth with parent-reported ASD using standardized parent-report measurement of both variables. It was hypothesized that more pain-related behaviors would predict more sleep problems, as found in
294 earlier studies of TD youth and those with DDs (e.g. Breau and Camfield, 2011; Ghanizadeh and Faghih, 2009). Capitalizing on the use of standardized measures, this hypothesis was augmented by an exploration of the specific subtypes of sleep problems predicted by pain-related behaviors. We also compared the relative contribution of specific modalities of pain communication when predicting these specific sleep problems. In this context, it was expected that higher levels of facial pain communication would be the most prominent predictor of higher levels of specific sleep problems, given that this is the most common type of pain expression evidenced in youth with ASD (e.g. Messmer et al., 2008; Nader et al., 2004). Potential moderators of the pain–sleep relationship were also considered to elucidate the nature and clinical presentation of these factors, with the expectation that lower verbal ability, the presence of pain-related health conditions, and the presence of either GI problems or asthma would augment the obtained sleep–pain relationships.
Method Participants Youth with ASD were recruited through a local Autism Society online, listserv, and a bi-weekly Autism Society national newsletter emailed directly to listserv members. A subset of 62 biological mothers who completed a sufficient portion (80% or more) of the relevant measures for this investigation was drawn from a larger survey study reported elsewhere (Walsh et al., 2012).This subsample did not differ significantly from the overall sample in demographics. Child ages ranged from 3 to 18 years (M = 9.39, SD = 4.19). A total of 12 youth were female, consistent with the 4:1 sex ratio seen in ASD (Fombonne, 2003). Reported ethnicity was 3% Asian/Pacific Islander, 3% Native American, 3% Hispanic, 11% Black/African American, and 88% White/Caucasian. In regard to ASD diagnoses, parent report indicated 58% with autistic disorder, 30% with pervasive developmental disorder–not otherwise specified (PDD-NOS), and the remaining 20% with Asperger’s syndrome. Parents described their children as fully verbal (n = 41), partially verbal (n = 11), nonverbal (n = 1), or using assisted communication strategies (n = 2), and no response (n = 8). Of note, in the analyses including verbal ability (described under data analysis), verbal ability was collapsed into two groups: verbal (including fully or partially verbal) and nonverbal (including nonverbal and assisted communication). Youth with recorded response for verbal ability were not included in verbal ability analyses. In response to an open-ended query, a subset of the children was described as having at least one health problem that did not include their DD (n = 25). The most common health problems were GI problems (e.g. inflammatory
Autism 19(3) bowel diseases, food allergies; n = 11), asthma (n = 8), and severe seasonal allergies (n = 6). Some other reports included diabetes (n = 1), skin conditions (e.g. eczema; n = 2), and chronic infections (e.g. throat, ear; n = 3). The remaining 37 children were reported as having no relevant health problems.
Measures Non-Communicating Children’s Pain Checklist–Revised. The Non-Communicating Children’s Pain Checklist–Revised (NCCPC-R) is the most widely used and well-validated parent-report assessment of pain for populations with communication difficulties (Breau et al., 2002), which identifies 30 observable pain-related behaviors among children. Parents rate each item on a four-point Likert-type frequency scale from Not at All to Very Often over the past week. Of note, this is a commonly used retrospective variation of the measure, whereas the original measure was intended to be used over a 2-hour observation period (Breau et al., 2002). Higher scores indicate more frequent pain behaviors, which are associated with long-term, chronic pain in samples with cognitive impairments (Breau et al., 2000, 2001). Subscales include Vocal (e.g. whining), Social (e.g. seeking comfort), Facial (e.g. frowning), Activity (e.g. agitation), Body (e.g. protecting parts of body), Physiological (e.g. sweating), and Eating/Sleeping (e.g. sleep disturbance, disinterest in food). Subscale summation yields a score range from 0 to 49, with a cutoff score of 7 to identify a high likelihood of pain (Breau et al., 2002). Children’s Sleep Habits Questionnaire. The Children’s Sleep Habits Questionnaire (CSHQ) is a parent-report measure of behavioral and medical sleep problems in youth (Owens et al., 2000). While the measure was developed for schoolaged TD children, it has been implemented for a wider age range among youth with DDs (e.g. Honomichl et al., 2002; Tudor et al., 2012). Subscales include Bedtime Resistance (e.g. bedtime refusal), Sleep Onset Delay (e.g. extended sleep latency), Sleep Duration (e.g. having too little sleep), Sleep Anxiety (e.g. expressing fear about bedtime), Night Wakings (e.g. waking in the night), Parasomnias (e.g. sleep apnea, night terrors, restless leg syndrome), SleepDisordered Breathing (e.g. sleep apnea), and Daytime Sleepiness (e.g. appears sleepy during the day). Items are rated on a three-point Likert-type scale from Rarely (0–1 night per week) to Usually (5–7 nights per week), focusing in the child’s most recent typical week of sleep. These subscales yield a total sleep disturbance score, ranging from 33 to 99, with a clinical cutoff score of 41.
Procedure All questionnaires were completed through SurveyMonkey. com. Parents received recruitment flyers that advertised
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Tudor et al. payment for participating in an online study about youth with ASD. Upon following the provided link, parents completed the consent form. If parents did not consent, they were instructed to leave the website to discontinue their participation in the study. Participants who completed 80% or more of the study battery received an Amazon.com gift card worth US$20. Battery completion took approximately 1 h for each parent.
Data analysis Prior to conducting analyses, missing data were handled via mean subscale mean imputation. As necessary, variables were then transformed in order to meet assumptions of normality for regression analyses. Specifically, the Sleep-Disordered Breathing subscale of the CSHQ and the Physiological subscale of the NCCPC-R were both negatively skewed and, thus, a square root transformation was used. First, a univariate regression was performed with NCCPC-R Total as the predictor of the CSHQ Total Sleep Disturbance criterion. When a significant relationship was found, a multivariate regression was completed with NCCPC-R Total as the predictor of the eight CSHQ subscales to determine if the effects of observed pain-related behavior on sleep problems differed by the type of sleep disturbance. When this multivariate statistic was significant, univariate regressions were run predicting each of the CSHQ subscales from the NCCPC-R Total, using a Bonferroni correction of the alpha criterion for multiple comparisons (p ≤ .006), as these analyses were part of a large family of tests and were intended for further subsequent probing, thereby warranting a careful avoidance of Type I error. Multiple comparison corrections were not used for the remaining analyses given their novel and exploratory nature, as well as the insufficiently small sets of tests in each step. To examine if different types of painrelated behavior contributed differentially to any effects on sleep subscales found in the previous stage, a series of univariate multiple regressions were then performed with the seven NCCPC-R subscales as simultaneous predictors of the specific CSHQ subscales that were identified as significant in the previous analysis. Of note, one subscale of the NCCPC-R (Eating/Sleeping) was not included in NCCPC-R subscale analyses because of the possibility that the score may directly measure the same construct as the criterion variables; this subscale was included in the Total NCCPC-R score analysis in order to maintain the integrity of the standardized measure. Finally, moderation analyses were conducted to examine whether interactions between obtained effects of NCCPC-R subscales and parent-reported verbal ability, presence of pain-related health conditions, GI problems, or asthma significantly predicted the identified CSHQ subscales, and, therefore, better explained the obtained effects (see Holmbeck, 2002).
Statistical analyses were performed using the IBM Statistical Package for the Social Sciences Version 20 (SPSS; IBM Corp., 2011) and the MODPROBE macro (Hayes and Matthes, 2009).
Results Descriptive statistics The mean score for the NCCPC-R (M = 29.05) was high compared to normative information for this measure (Breau et al., 2002; Table 1). In the sample, 97% of the NCCPC-R Total scores were above 7. As seen in Table 1, Social communication of pain was the most commonly reported modality, with 100% of the sample endorsing at least one Social subscale item. In regard to sleep problems, 93% of the sample scored above 41 (M = 54.07) on the CSHQ. Also seen in Table 1, parasomnias was the most commonly reported sleep problem, with 95% of the sample endorsing at least one Parasomnias subscale item.
Regression analyses An initial univariate regression showed that higher scores on the NCCPC-R predicted higher scores on CSHQ Total Sleep Disturbance (β = .47, p < .001, R2 = .22). A subsequent multivariate regression was significant (F(8, 68) = 6.21, p < .001, partial η2 = .48); thus, effects of NCCPC-R on the CSHQ subscales were probed. These regressions revealed that higher scores on the NCCPC-R predicted higher scores on three CSHQ subscales: Sleep Duration, Parasomnias, and Sleep-Disordered Breathing (Table 2). According to the final series of multiple regressions (Table 3), higher scores on the Sleep Duration subscale were predicted by higher scores on the Social subscale; higher scores on the Parasomnias subscale were predicted by higher levels on the Facial subscale; and higher scores on the Sleep-Disordered Breathing subscale were predicted by higher scores on the Vocal subscale. None of the moderation analyses suggested that parentreported verbal abilities, presence of comorbid health problems, or presence of GI-related health problems were significant moderators in the multiple regressions described above (all p > .19). Presence of asthma significantly moderated the relationship between SleepDisordered Breathing and the NCCPC-R Facial subscale (F = 4.14, ΔR2 = .05, p < .05). Per the data analytic plan, post hoc analysis was warranted to identify the direction of this relationship. Probing revealed that the relationship was present only among those without asthma (B = .52, p = .008). Given the counterintuitive nature of this finding, further examination was implemented to rule out the possibility that Sleep-Disordered Breathing (the least-reported sleep problem, see Table 1) might have presented with a truncated range of high scores and, potentially, that these
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Table 1. Untransformed means and standard deviations on the NCCPC-R and CSHQ (subscales and total scores). Subscale
Mean
CSHQ Bedtime Resistance Sleep Onset Delay Sleep Duration Sleep Anxiety Night Wakings Parasomnias Sleep-Disordered Breathing Daytime Sleepiness Total Sleep Disturbance NCCPC-R Vocal Social Facial Activity Body Physiological Total
Standard deviation
9.33 2.03 5.62 6.64 5.06 10.72 3.99 13.82 54.07
3.20 .81 1.95 2.13 1.78 2.57 1.22 3.30 9.37
4.59 6.22 4.78 2.66 4.61 3.78 29.05
3.33 2.97 4.20 1.45 4.53 4.03 18.95
n (% of sample) scoring >0 45 (73) 42 (68) 47 (76) 55 (89) 49 (79) 59 (95) 35 (56) 60 (97) 59 (95) 62 (100) 53 (85) 57 (92) 53 (85) 52 (84)
CSHQ: Children’s Sleep Habits Questionnaire; NCCPC-R: Non-Communicating Children’s Pain Checklist–Revised.
Table 2. Results of univariate regressions with NCCPC-R total predicting each CSHQ subscale. CSHQ subscale criterion
B
SE B
β
R2
Bedtime Resistance Sleep Onset Delay Sleep Duration Sleep Anxiety Night Wakings Parasomnias Sleep-Disordered Breathing Daytime Sleepiness
.02 .00 .01 .00 .00 .02 .00
.01 .00 .00 .00 .00 .01 .00
.33 .23 .39* .09 .15 .51* .44*
.11 .05 .15 .01 .02 .26 .20
.00
.00
.03
.03
CSHQ: Children’s Sleep Habits Questionnaire. *p < .006, Bonferroni-corrected alpha criterion. Dependent variables are listed in first column.
scores may have been associated with asthma. Therefore, post hoc analyses were used to compare scores on this scale between those with and without reported asthma, revealing no difference between these groups (t(60) =−.20, p = .84). The relationships predicting Sleep Duration and Parasomnias were not moderated by presence of asthma (all p > .37) and, therefore, these particular sleep problems required no further post hoc analyses.
Discussion This study is, to our knowledge, the first examination of pain–sleep problem relationships in youth with parentreported ASD. The results presented here provide novel
insights through the use of standardized measures and the consideration of various factors that are relevant to a more comprehensive picture of health for youth with ASD. Hypotheses were largely supported in that more painrelated behaviors over the past week predicted more overall sleep problems, as well as a subset of specific sleep problems: sleep duration, parasomnias, and sleep-disordered breathing. These specific sleep problems were further predicted by specific modalities of pain communication, although facial communication was not the only meaningful modality identified. Contrary to expectations, only asthma was identified as a meaningful moderator of one found relationship, in that more vocal communication of pain predicted more sleep-disordered breathing for youth without asthma. Overall, the study provided a multifaceted view of the effect that pain-related behaviors, including specific pain communication modalities, may have on sleep health in youth with ASD.
High prevalence of pain-related behaviors and sleep problems Over 90% of the current sample scored above the clinical cutoff range on the CSHQ, which is consistent with other recent reports on samples of youth with ASD (e.g. M = 48.2, 47.7, 67.4, respectively; Courtier et al., 2005; Hodge et al., 2013; Souders et al., 2009). The prevalence of significantly elevated parent-reported pain was also over 90% in the current sample and is, to our knowledge, a novel result regarding youth with ASD. However, it must be
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Tudor et al. Table 3. Results of multiple regressions with NCCPC-R subscales predicting those CSHQ subscales that were significantly predicted by overall NCCPC-R in univariate regressions. NCCPC-R predictor variable
Sleep-Disordered Breathing B
SE B
Intercept Vocal Social Facial Activity Body Physiological R2 F
11.5 .08 .54 .02 −.10 .00 .07
5.9 .04 2.81 .04 .23 .04 .04 .31 5.19**
Parasomnias
Sleep Duration
β
B
SE B
.25* .03 .07 −.07 .09 .34
68.5** .02 8.0 .61 .86 .02 −.17
27.3 .20 13.0 .16 1.1 .18 .17 .37 6.70***
β
B
SE B
β
.01 .08 .57** .13 .02 −.18
1.9 .00 12.9 .10 −.49 .01 .00
10.8 .08 5.14 .06 .42 .07 .07 .22 3.24**
.00 .36** .27 −.21 .05 .00
NCCPC-R: Non-Communicating Children’s Pain Checklist–Revised; F: Facial subscale. *p < .05; ** p< .01; *** p< .001.
noted that the normative data for this measure is based on a 2-hour observation period, rather than the 1-week retrospective report often used in previous iterations of this measure; thus comparison to previous reports using the 2-hour time frame should be made with caution. Researchers are currently in the process of procuring more well-specified cutoffs on the NCCPC-R for ASD populations and assessing validity among populations with high rates of medical comorbidities (Breau, 4 February 2013, personal communication). The initial findings here indicate a possibly elevated rate and intensity of parentreported clinical pain in youth with ASD. These elevated rates of sleep problems and pain-related behaviors indicate important medical and clinical considerations for youth with ASD. While these disturbances may be widely prevalent, they may be related to highly distinct etiologies across children; for example, one child with ASD may experience ongoing mild digestive discomfort, while another may experience severe inflammatory bowel disease. Nevertheless, these problems in any form may interfere with youth’s response to behavioral intervention and pharmacological treatments, as well as their ability to function in various social contexts. Together, the prevalence of these problems in the current sample supports increased consideration of these factors in assessment and treatment planning for youth with ASD.
Sleep problems predicted by pain-related behaviors Pain-related behavior predicted overall sleep problems, consistent with previous findings among youth with DDs (Breau and Camfield, 2011). However, the current results suggest that not all specific sleep problems are predicted by pain-related behaviors consistently. Problems with sleep duration, parasomnias, and sleep-disordered breathing were predicted by pain-related behaviors over and
above the other specific sleep problems. Breau and Camfield (2011) identified youth with parent-reported pain as experiencing more parasomnias and sleep-disordered breathing, but did not identify such a relationship in regard to sleep duration. Additionally, the previous study identified night wakings as occurring more frequently in youth with pain, in contrast to the current results. These dissimilar findings may be unique to the different mode of pain assessment used here. Specifically, our current use of a standardized pain measure for youth with communication difficulties may provide a more sensitive assessment than the dichotomous “pain” versus “no pain” measure used by previous study. Additionally, our sample may represent a diagnostically distinct group of youth, while the previous study recruited youth with a variety of DDs. This differentiation crucially indicates important differences in the pain–sleep relationship unique to this population, especially given that past research suggests that children with ASD experience more sleep problems and a larger variety of specific sleep problems than TD children, and those with Down Syndrome or Prader–Willi syndrome (Cotton and Richdale, 2006).
Sleep problems predicted by pain-related communication Problems with sleep duration, parasomnias, and sleep-disordered breathing were all predicted by specific forms of pain-related communication. Problems with sleep duration were predicted by social communication of pain, such as comfort-seeking and being difficult to pacify. It is possible that youth who engage in social pain communication naturally sleep less because they are more likely to engage in attention- or comfort-seeking behavior before bed or during night wakings, thus shortening their sleep duration. Furthermore, mothers may report higher levels of sleep duration problems for these children because of their own
298 lack of sleep. Mothers of children with ASD appear more likely to experience sleep problems when their children experience sleep problems, possibly due to comfort-seeking or the need to supervise the child (Hodge et al., 2013; Lopez-Wagner et al., 2008). As such, the social communication of pain may predict shorter sleep duration because of the related behaviors that interfere with quickly transitioning to sleep and mothers’ inability to sleep. Parasomnias were predicted by facial communication of pain, such as grimacing or brow furrowing, which has been evinced as the most common observable form of pain expression in one laboratory study of young children with ASD (Nader et al., 2004). It is possible that parasomnias are predicted by facial communication of pain due to the grimacing and gnashing that may uniquely occur during parasomnias themselves (e.g. night terrors, nightmares), suggesting excessive overlap of measured constructs on these subscales. Future research may benefit from examining parent report of pain among youth with ASD who experience parasomnias, as pain-related behaviors may be subsumed within parasomnia behavioral presentation. Sleep-disordered breathing was predicted by vocal communication of pain, such as moaning or yelling. Like parasomnias, behavioral presentation of sleep-disordered breathing (e.g. gasping, snorting) may overlap with vocally communicated pain behaviors. However, asthma may be a significant predictor of sleep problems in youth with ASD (Liu et al., 2006) and related symptoms can often exacerbate at night (Bohadana et al., 2002). Here, asthma significantly moderated the relationship between vocal pain and sleep-disordered breathing, indicating it to only be present for those who were not reported to have asthma. It is possible that participants who experience sleep-disordered breathing are suffering from other respiratory-related complaints, such as allergies or obesity. Alternatively, youth with asthma may be more likely to exhibit respiratoryrelated problems across a variety of situations besides sleep and, subsequently, demonstrate multiple forms of pain-related communication, including nonvocal behaviors. Future research should further examine how painrelated behaviors are communicated among youth with ASD and various respiratory complaints as compared to those without respiratory complaints. Studies that incorporate observational and laboratory measures of both sleepdisordered breathing and daytime respiratory function may be especially useful in expanding upon the current results. Contrary to expectations, verbal ability and pain-related health condition (GI problems or asthma) did not moderate the obtained relationships between specific sleep problems and pain-related communication. This differs from previous findings related to youth with ID, wherein the presence of medical condition explained the relationships between pain and sleep problems (Ghanizadeh and Faghih, 2009). Most notably, the relationships demonstrated in the current study may reflect the severe behavioral disturbances
Autism 19(3) associated with ASD (e.g. Hartley et al., 2008; Lecavalier, 2006). Alternatively, the lack of moderating effects of verbal ability or health problems may reflect a high pain prevalence that is consistent across the sample regardless of diagnosed health conditions.
Limitations and future directions Several factors in this study limit interpretation and generalization results. First, the participants were recruited online and identified through parent report of diagnosis. Diagnostic confirmation is necessary to support diagnostic validity of the ASD sample. Similarly, all data were parent reported and, therefore, dependent on subjective recall of their child’s behaviors. While the pain measure used here is standardized for youth with communication difficulties, this high rate raises important questions about pain, and the measurement thereof, in youth with ASD. Presently, many NCCPC-R items may overlap with emotional distress, problem behavior, or other behavioral disturbances related to difficulties with communication, as seen in previous studies (e.g. Walsh et al., 2012), and further examination of the discriminant validity of this measure and measures of other behavioral symptoms is warranted. Furthermore, data were collected cross-sectionally. Data collection over multiple time periods could aid in understanding any potential causal relationships between pain and sleep problems and could be useful in identifying potential mediators (e.g. parenting style, parental stress). This study also possesses a moderate sample size and no comparison group. Future studies would benefit from inclusion of comparison samples of TD youth and those with other DDs to examine whether the obtained relationships are indeed unique to individuals with ASD. Similarly, comparing youth with ASD experiencing chronic pain versus acute pain, as well as those with and without confirmed medical conditions, may better explain differential pain– sleep relationships.
Clinical implications Based on the current results, pediatricians and clinicians who work with youth with ASD who also have sleep problems may consider assessing pain-related behaviors, which may otherwise not be part of a differential assessment procedure. Such information may be helpful in understanding where to first target pharmacological or behavioral intervention (e.g. pain-focused intervention versus sleepfocused intervention). Parents may also benefit from monitoring the sleep health of youth with ASD who display high levels of pain-related behaviors, given that these children may be more likely to experience sleep-disordered breathing, parasomnias, and shorter sleep intervals, all of which can impact their child’s functioning.
Tudor et al. Furthermore, the pain–sleep relationships suggested here may serve as indicators for designing antecedentbased interventions. For example, parents of youth with ASD who are experiencing parasomnias may benefit from understanding the antecedents of their child’s facial communication of pain. Results may assist parents in implementing preventive strategies for their child’s pain, which may have collateral effects on sleep. Identifying the antecedents and consequences of socially communicated pain could help parents and clinicians create interventions (e.g. increasing child’s self-soothing). Most importantly, future research may indicate that pain and sleep problems may have an impact on the quality of life for youth with ASD and their families by improving their overall health and functionality (e.g. Carr and Owen-DeSchryver, 2007; Koegel et al., 1992). Like those with other DDs, youth with ASD may experience sleep disrupted by pain-related behaviors, although the incidence of these problems may be higher in youth ASD and unique pain–sleep problem relationships may exist for this population. Overall, this study provides further insights into two areas of health-related functioning that may be frequently impacted for these youth. Further study of how pain and sleep problems relate to one another and may affect children’s daytime functioning, inform effective assessment procedures, and impact overall quality of life is encouraged. Acknowledgements The authors thank Dr Steve M Edelson for his valued support, and James Rankin for his research assistance. The study was made possible by and carried out in fond memory of Dr Edward G Carr.
Funding This study was funded by the Autism Research Institute (ARI).
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Autism 19(3) Moldofsky H (2001) Sleep and pain. Sleep Medicine Reviews 5: 385–396. Nader R, Oberlander T, Chambers C, et al. (2004) Expression of pain in children with autism. The Clinical Journal of Pain 20: 88–97. Owens JA, Spirito A and McGuinn M (2000) The Children’s Sleep Habits Questionnaire (CSHQ): psychometric properties of a survey instrument for school-aged children. Sleep 23: 1043–1051. Palermo TM, Toliver-Sokol M, Fonareva I, et al. (2007) Objective and subjective assessment of sleep in adolescents with chronic pain compared to healthy adolescents. The Clinical Journal of Pain 23: 812–820. Sadeh A, Gruber R and Raviv A (2003) Sleep, neurobehavioral functioning, and behavior problems in school-age children. Child Development 73: 405–417. Schieve LA, Gonzalez V, Boulet SL, et al. (2012) Concurrent medical conditions and health care use and needs among children with learning and behavioral developmental disabilities, National Health Interview Survey, 2006–2010. Research in Developmental Disabilities 33: 467–476. Shreck KA and Richdale AL (2011) Knowledge of childhood sleep: A possible variable in under or misdiagnosis of childhood sleep problems. Journal of Sleep Research 20: 589–597. Schreck KA, Mulick JA and Smith AF (2004) Sleep problems as possible predictors of intensified autism. Research in Developmental Disabilities 25: 57–66. Souders MC, Mason TB, Valladares O, et al. (2009) Sleep behaviors and sleep quality in children with autism spectrum disorders. Sleep 32: 1566–1578. Stores G, Ellis AJ, Wiggs L, et al. (1998) Sleep and psychological disturbance in nocturnal asthma. Archives of Disease in Childhood 78: 413–419. Tudor ME, Hoffman CD and Sweeney DP (2012) Children with autism: sleep problems and symptom severity. Focus on Autism and Other Developmental Disabilities 27: 254–262. Walsh CE, Mulder EC and Tudor ME (2012) Predictors of parent stress in a sample of children with ASD: pain, problem behavior, and parental coping. Research in Autism Spectrum Disorders 7: 256–264. Williams PG, Sears LL and Allard A (2004) Sleep problems in children with autism. Journal of Sleep Research 13: 265–268. Wright M, Tancredi A, Yundt B, et al. (2006) Sleep issues in children with physical disabilities and their families. Journal of Intellectual Disability Research 40: 518–528.
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article2014
AUT0010.1177/1362361313518994AutismTudor et al.
Original Article
Pain as a predictor of sleep problems in youth with autism spectrum disorders
Autism 2015, Vol. 19(3) 292–300 © The Author(s) 2014 Reprints and permissions: sagepub.co.uk/journalsPermissions.nav DOI: 10.1177/1362361313518994 aut.sagepub.com
Megan E Tudor, Caitlin E Walsh, Emile C Mulder and Matthew D Lerner
Abstract Evidence suggests that pain interferes with sleep in youth with developmental disabilities. This study examined the relationship between pain and sleep problems in a sample of youth with parent-reported autism spectrum disorder (N = 62). Mothers reported on standardized measures of pain and sleep problems. Youth demonstrated atypically high levels of both observed pain and sleep problems. Pain predicted overall sleep disturbance and three specific sleep problems: sleep duration, parasomnias, and sleep-disordered breathing. These specific sleep problems were predicted by specific modalities of nonverbal pain communication (e.g. sleep duration problems were predicted by social communication of pain). Effects were consistent across probing of relevant moderators. These findings suggest that comprehensive assessment of both pain and sleep problems may provide important information for medical and behavioral treatment planning for youth with autism spectrum disorder. Keywords autism, communication, pain, sleep problems While social and communication deficits are considered core characteristics of autism spectrum disorders (ASD), health-related comorbidities are often reported to be common, and may be even more prevalent among youth with ASD than typically developing (TD) youth (e.g. Schieve et al., 2012; Shreck and Richdale, 2011). Two such factors, pain and sleep problems, may increase the likelihood for functional impairments and play an important role in quality of life in this population (Bauman, 2010). Additionally, these variables may in fact be related to one another among youth with intellectual and developmental disabilities (IDD), with pain disrupting sleep (Breau and Camfield, 2011), though no research has examined their relation in children with ASD specifically. Given the high incidence of these health-related problems and their unique impacts on overall functioning, this study seeks to elucidate how these comorbidities may manifest, as well as the magnitude and contours of their relationships in youth with ASD.
wakings, and parasomnias (e.g. night terrors, sleep-walking; Williams et al., 2004). In TD youth, lack of sleep can impair cognitive abilities and increase risk for behavioral problems (e.g. Sadeh et al., 2003). For youth with ASD, sleep problems have been associated with various functional impairments such as increased problem behavior (DeVincent et al., 2007) and exacerbated core symptoms (Hoffman et al., 2005; Schreck et al., 2004; Tudor et al., 2012). While evidence suggests that behavioral treatment (Christodulu and Durand, 2004) and melatonin-based pharmacological interventions (Andersen et al., 2008) may be helpful in improving the sleep of youth with ASD, sleep health is not regularly assessed and integrated into behavioral or medical treatment of these youth. Thus, the consideration of sleep problems may be an important, albeit largely overlooked, area of health-related functioning for youth with ASD.
Sleep problems and ASD Ample research suggests that youth with ASD experience more sleep problems than TD youth (e.g. Hoffman et al., 2006). Both parent report and observational evidence exist for a wide range of specific sleep problems occurring within this population, including sleep onset delay, night
Stony Brook University, USA Corresponding author: Megan E Tudor, Psychology Department, Stony Brook University, Stony Brook, NY 11794, USA. Email: [email protected]
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Pain and ASD Anecdotal reports and clinical impressions classically suggest that youth with ASD may display a blunted or absent response to pain. Notably, the Diagnostic and Statistical Manual of Mental Disorders (4th edition, text rev.; DSMIV-TR; American Psychiatric Association, 2000) indicates a “high threshold for pain” (p. 72) as a descriptive feature of the disorder. Thus far, two observational laboratorybased studies indicate that such youth display responses to pain that are similar to those of TD children, although they may exhibit more facial grimacing when experiencing pain (Messmer et al., 2008; Nader et al., 2004). These findings provide an initial insight into the unique nonverbal communication of pain via objective methods in this population. Together, they suggest that further research on how to adequately assess pain in this population is needed. Assessment of pain is a decidedly complex task (see Breivik et al., 2008) that may be even harder in the ASD population due to social and communication difficulties (Jyonouchi, 2010). The ability to recognize, label, and share particular health needs and experiences of pleasure or discomfort may be impaired (Breau and Burkitt, 2009). As such, youth with ASD may experience pain that goes unreported and, crucially, may be unrelated to a chronic medical condition, such as mild, normative aches and pains that many children might experience in their youth due to mild illness, injury, or digestive discomfort. Furthermore, youth with ASD may experience pain related to sensory integration problems, such as discomfort related to temperature, loud noises, or texture of clothing. Importantly, while youth with ASD may experience difficulty with reporting these various forms of pain, parent report of pain-related behavior does appear to provide a fair estimate of subjective pain experienced by youth with ASD (Nader et al., 2004). The review of a child’s medical history can also serve as a critical piece of a thorough pain assessment (Breau and Burkitt, 2009). Reports of gastrointestinal (GI) complaints and asthma are frequent in youth with ASD and are typically accompanied by pain-related behaviors (e.g. Horvath and Perman, 2002; Schieve et al., 2012). Necessity of medical care may also indicate pain in this population. Youth with ASD are reported as having more doctor visits, emergency care, and long-term medication usage than TD children (Gurney et al., 2006). With special importance to this study, sleep problems may also inform pain assessment for these youth, given that sleep problems serve as indicators for a variety of health problems that may be helpful in medical assessment among TD youth (Huntley et al., 2007; Palermo et al., 2007). Thus, consideration of comorbid medical (including sleep) problems may further inform the understanding of pain-related behaviors in this population of youth, especially those with more communication difficulties.
Relationships between sleep problems, pain, and ASD Pain and sleep problems are evidenced as being highly cooccurring in youth (e.g. Bruusgaard et al., 2000) with approximately half of TD youth with pain also experiencing significant sleep problems (Long et al., 2008). These two factors often exhibit bi-directional predictive relationships with one another, with more sleep problems predicting more pain and more pain predicting more sleep problems (e.g. Moldofsky, 2001). The latter relationship has been examined in youth with various disabilities. Sleep problems increase when pain is reported in populations of youth with physical disabilities (e.g. Wright et al., 2006) and intellectual disabilities (ID) (Ghanizadeh and Faghih, 2009). One previous study has examined the potential relationships between sleep problems and pain in youth with IDD, including ASD (Breau and Camfield, 2011). This study suggested that youth with IDD might be more likely to experience sleep problems, such as parasomnias, sleepdisordered breathing, and night wakings, if they are also reported as having pain-related health problems. Given the evidence for unique sleep and pain-related characteristics in ASD and the disorder’s high comorbidity with ID (Fombonne, 2003), as well as the relation between these characteristics found in other developmental disabilities (DDs) (Breau and Camfield, 2011; Ghanizadeh and Faghih, 2009), an examination of the sleep–pain relationships in youth with parent-reported ASD would fill an important gap in the literature. Such relationships also require careful examination of related factors that may influence the strength or presence of these relationships. As described above, both degree of communication abilities and the presence of pain-related health problems may influence these relationships. Additionally, GI problems and asthma represent specific health problems that are both prevalent in this population (e.g. Horvath and Perman, 2002; Schieve et al., 2012) and may contribute to both pain-related behavior and sleep problem report (e.g. Levy et al., 2006; Stores et al., 1998). Furthermore, the understanding of these relationships could further benefit from considering the particular modalities by which youth with ASD communicate their pain (e.g. social, facial), which may relate to specific sleep–pain relationships. The consideration of specific nonverbal communication may be of paramount importance to interpreting these relationships in this population.
Current study This study aimed to examine pain-related behaviors as a predictor of sleep problems in youth with parent-reported ASD using standardized parent-report measurement of both variables. It was hypothesized that more pain-related behaviors would predict more sleep problems, as found in
294 earlier studies of TD youth and those with DDs (e.g. Breau and Camfield, 2011; Ghanizadeh and Faghih, 2009). Capitalizing on the use of standardized measures, this hypothesis was augmented by an exploration of the specific subtypes of sleep problems predicted by pain-related behaviors. We also compared the relative contribution of specific modalities of pain communication when predicting these specific sleep problems. In this context, it was expected that higher levels of facial pain communication would be the most prominent predictor of higher levels of specific sleep problems, given that this is the most common type of pain expression evidenced in youth with ASD (e.g. Messmer et al., 2008; Nader et al., 2004). Potential moderators of the pain–sleep relationship were also considered to elucidate the nature and clinical presentation of these factors, with the expectation that lower verbal ability, the presence of pain-related health conditions, and the presence of either GI problems or asthma would augment the obtained sleep–pain relationships.
Method Participants Youth with ASD were recruited through a local Autism Society online, listserv, and a bi-weekly Autism Society national newsletter emailed directly to listserv members. A subset of 62 biological mothers who completed a sufficient portion (80% or more) of the relevant measures for this investigation was drawn from a larger survey study reported elsewhere (Walsh et al., 2012).This subsample did not differ significantly from the overall sample in demographics. Child ages ranged from 3 to 18 years (M = 9.39, SD = 4.19). A total of 12 youth were female, consistent with the 4:1 sex ratio seen in ASD (Fombonne, 2003). Reported ethnicity was 3% Asian/Pacific Islander, 3% Native American, 3% Hispanic, 11% Black/African American, and 88% White/Caucasian. In regard to ASD diagnoses, parent report indicated 58% with autistic disorder, 30% with pervasive developmental disorder–not otherwise specified (PDD-NOS), and the remaining 20% with Asperger’s syndrome. Parents described their children as fully verbal (n = 41), partially verbal (n = 11), nonverbal (n = 1), or using assisted communication strategies (n = 2), and no response (n = 8). Of note, in the analyses including verbal ability (described under data analysis), verbal ability was collapsed into two groups: verbal (including fully or partially verbal) and nonverbal (including nonverbal and assisted communication). Youth with recorded response for verbal ability were not included in verbal ability analyses. In response to an open-ended query, a subset of the children was described as having at least one health problem that did not include their DD (n = 25). The most common health problems were GI problems (e.g. inflammatory
Autism 19(3) bowel diseases, food allergies; n = 11), asthma (n = 8), and severe seasonal allergies (n = 6). Some other reports included diabetes (n = 1), skin conditions (e.g. eczema; n = 2), and chronic infections (e.g. throat, ear; n = 3). The remaining 37 children were reported as having no relevant health problems.
Measures Non-Communicating Children’s Pain Checklist–Revised. The Non-Communicating Children’s Pain Checklist–Revised (NCCPC-R) is the most widely used and well-validated parent-report assessment of pain for populations with communication difficulties (Breau et al., 2002), which identifies 30 observable pain-related behaviors among children. Parents rate each item on a four-point Likert-type frequency scale from Not at All to Very Often over the past week. Of note, this is a commonly used retrospective variation of the measure, whereas the original measure was intended to be used over a 2-hour observation period (Breau et al., 2002). Higher scores indicate more frequent pain behaviors, which are associated with long-term, chronic pain in samples with cognitive impairments (Breau et al., 2000, 2001). Subscales include Vocal (e.g. whining), Social (e.g. seeking comfort), Facial (e.g. frowning), Activity (e.g. agitation), Body (e.g. protecting parts of body), Physiological (e.g. sweating), and Eating/Sleeping (e.g. sleep disturbance, disinterest in food). Subscale summation yields a score range from 0 to 49, with a cutoff score of 7 to identify a high likelihood of pain (Breau et al., 2002). Children’s Sleep Habits Questionnaire. The Children’s Sleep Habits Questionnaire (CSHQ) is a parent-report measure of behavioral and medical sleep problems in youth (Owens et al., 2000). While the measure was developed for schoolaged TD children, it has been implemented for a wider age range among youth with DDs (e.g. Honomichl et al., 2002; Tudor et al., 2012). Subscales include Bedtime Resistance (e.g. bedtime refusal), Sleep Onset Delay (e.g. extended sleep latency), Sleep Duration (e.g. having too little sleep), Sleep Anxiety (e.g. expressing fear about bedtime), Night Wakings (e.g. waking in the night), Parasomnias (e.g. sleep apnea, night terrors, restless leg syndrome), SleepDisordered Breathing (e.g. sleep apnea), and Daytime Sleepiness (e.g. appears sleepy during the day). Items are rated on a three-point Likert-type scale from Rarely (0–1 night per week) to Usually (5–7 nights per week), focusing in the child’s most recent typical week of sleep. These subscales yield a total sleep disturbance score, ranging from 33 to 99, with a clinical cutoff score of 41.
Procedure All questionnaires were completed through SurveyMonkey. com. Parents received recruitment flyers that advertised
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Tudor et al. payment for participating in an online study about youth with ASD. Upon following the provided link, parents completed the consent form. If parents did not consent, they were instructed to leave the website to discontinue their participation in the study. Participants who completed 80% or more of the study battery received an Amazon.com gift card worth US$20. Battery completion took approximately 1 h for each parent.
Data analysis Prior to conducting analyses, missing data were handled via mean subscale mean imputation. As necessary, variables were then transformed in order to meet assumptions of normality for regression analyses. Specifically, the Sleep-Disordered Breathing subscale of the CSHQ and the Physiological subscale of the NCCPC-R were both negatively skewed and, thus, a square root transformation was used. First, a univariate regression was performed with NCCPC-R Total as the predictor of the CSHQ Total Sleep Disturbance criterion. When a significant relationship was found, a multivariate regression was completed with NCCPC-R Total as the predictor of the eight CSHQ subscales to determine if the effects of observed pain-related behavior on sleep problems differed by the type of sleep disturbance. When this multivariate statistic was significant, univariate regressions were run predicting each of the CSHQ subscales from the NCCPC-R Total, using a Bonferroni correction of the alpha criterion for multiple comparisons (p ≤ .006), as these analyses were part of a large family of tests and were intended for further subsequent probing, thereby warranting a careful avoidance of Type I error. Multiple comparison corrections were not used for the remaining analyses given their novel and exploratory nature, as well as the insufficiently small sets of tests in each step. To examine if different types of painrelated behavior contributed differentially to any effects on sleep subscales found in the previous stage, a series of univariate multiple regressions were then performed with the seven NCCPC-R subscales as simultaneous predictors of the specific CSHQ subscales that were identified as significant in the previous analysis. Of note, one subscale of the NCCPC-R (Eating/Sleeping) was not included in NCCPC-R subscale analyses because of the possibility that the score may directly measure the same construct as the criterion variables; this subscale was included in the Total NCCPC-R score analysis in order to maintain the integrity of the standardized measure. Finally, moderation analyses were conducted to examine whether interactions between obtained effects of NCCPC-R subscales and parent-reported verbal ability, presence of pain-related health conditions, GI problems, or asthma significantly predicted the identified CSHQ subscales, and, therefore, better explained the obtained effects (see Holmbeck, 2002).
Statistical analyses were performed using the IBM Statistical Package for the Social Sciences Version 20 (SPSS; IBM Corp., 2011) and the MODPROBE macro (Hayes and Matthes, 2009).
Results Descriptive statistics The mean score for the NCCPC-R (M = 29.05) was high compared to normative information for this measure (Breau et al., 2002; Table 1). In the sample, 97% of the NCCPC-R Total scores were above 7. As seen in Table 1, Social communication of pain was the most commonly reported modality, with 100% of the sample endorsing at least one Social subscale item. In regard to sleep problems, 93% of the sample scored above 41 (M = 54.07) on the CSHQ. Also seen in Table 1, parasomnias was the most commonly reported sleep problem, with 95% of the sample endorsing at least one Parasomnias subscale item.
Regression analyses An initial univariate regression showed that higher scores on the NCCPC-R predicted higher scores on CSHQ Total Sleep Disturbance (β = .47, p < .001, R2 = .22). A subsequent multivariate regression was significant (F(8, 68) = 6.21, p < .001, partial η2 = .48); thus, effects of NCCPC-R on the CSHQ subscales were probed. These regressions revealed that higher scores on the NCCPC-R predicted higher scores on three CSHQ subscales: Sleep Duration, Parasomnias, and Sleep-Disordered Breathing (Table 2). According to the final series of multiple regressions (Table 3), higher scores on the Sleep Duration subscale were predicted by higher scores on the Social subscale; higher scores on the Parasomnias subscale were predicted by higher levels on the Facial subscale; and higher scores on the Sleep-Disordered Breathing subscale were predicted by higher scores on the Vocal subscale. None of the moderation analyses suggested that parentreported verbal abilities, presence of comorbid health problems, or presence of GI-related health problems were significant moderators in the multiple regressions described above (all p > .19). Presence of asthma significantly moderated the relationship between SleepDisordered Breathing and the NCCPC-R Facial subscale (F = 4.14, ΔR2 = .05, p < .05). Per the data analytic plan, post hoc analysis was warranted to identify the direction of this relationship. Probing revealed that the relationship was present only among those without asthma (B = .52, p = .008). Given the counterintuitive nature of this finding, further examination was implemented to rule out the possibility that Sleep-Disordered Breathing (the least-reported sleep problem, see Table 1) might have presented with a truncated range of high scores and, potentially, that these
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Table 1. Untransformed means and standard deviations on the NCCPC-R and CSHQ (subscales and total scores). Subscale
Mean
CSHQ Bedtime Resistance Sleep Onset Delay Sleep Duration Sleep Anxiety Night Wakings Parasomnias Sleep-Disordered Breathing Daytime Sleepiness Total Sleep Disturbance NCCPC-R Vocal Social Facial Activity Body Physiological Total
Standard deviation
9.33 2.03 5.62 6.64 5.06 10.72 3.99 13.82 54.07
3.20 .81 1.95 2.13 1.78 2.57 1.22 3.30 9.37
4.59 6.22 4.78 2.66 4.61 3.78 29.05
3.33 2.97 4.20 1.45 4.53 4.03 18.95
n (% of sample) scoring >0 45 (73) 42 (68) 47 (76) 55 (89) 49 (79) 59 (95) 35 (56) 60 (97) 59 (95) 62 (100) 53 (85) 57 (92) 53 (85) 52 (84)
CSHQ: Children’s Sleep Habits Questionnaire; NCCPC-R: Non-Communicating Children’s Pain Checklist–Revised.
Table 2. Results of univariate regressions with NCCPC-R total predicting each CSHQ subscale. CSHQ subscale criterion
B
SE B
β
R2
Bedtime Resistance Sleep Onset Delay Sleep Duration Sleep Anxiety Night Wakings Parasomnias Sleep-Disordered Breathing Daytime Sleepiness
.02 .00 .01 .00 .00 .02 .00
.01 .00 .00 .00 .00 .01 .00
.33 .23 .39* .09 .15 .51* .44*
.11 .05 .15 .01 .02 .26 .20
.00
.00
.03
.03
CSHQ: Children’s Sleep Habits Questionnaire. *p < .006, Bonferroni-corrected alpha criterion. Dependent variables are listed in first column.
scores may have been associated with asthma. Therefore, post hoc analyses were used to compare scores on this scale between those with and without reported asthma, revealing no difference between these groups (t(60) =−.20, p = .84). The relationships predicting Sleep Duration and Parasomnias were not moderated by presence of asthma (all p > .37) and, therefore, these particular sleep problems required no further post hoc analyses.
Discussion This study is, to our knowledge, the first examination of pain–sleep problem relationships in youth with parentreported ASD. The results presented here provide novel
insights through the use of standardized measures and the consideration of various factors that are relevant to a more comprehensive picture of health for youth with ASD. Hypotheses were largely supported in that more painrelated behaviors over the past week predicted more overall sleep problems, as well as a subset of specific sleep problems: sleep duration, parasomnias, and sleep-disordered breathing. These specific sleep problems were further predicted by specific modalities of pain communication, although facial communication was not the only meaningful modality identified. Contrary to expectations, only asthma was identified as a meaningful moderator of one found relationship, in that more vocal communication of pain predicted more sleep-disordered breathing for youth without asthma. Overall, the study provided a multifaceted view of the effect that pain-related behaviors, including specific pain communication modalities, may have on sleep health in youth with ASD.
High prevalence of pain-related behaviors and sleep problems Over 90% of the current sample scored above the clinical cutoff range on the CSHQ, which is consistent with other recent reports on samples of youth with ASD (e.g. M = 48.2, 47.7, 67.4, respectively; Courtier et al., 2005; Hodge et al., 2013; Souders et al., 2009). The prevalence of significantly elevated parent-reported pain was also over 90% in the current sample and is, to our knowledge, a novel result regarding youth with ASD. However, it must be
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Tudor et al. Table 3. Results of multiple regressions with NCCPC-R subscales predicting those CSHQ subscales that were significantly predicted by overall NCCPC-R in univariate regressions. NCCPC-R predictor variable
Sleep-Disordered Breathing B
SE B
Intercept Vocal Social Facial Activity Body Physiological R2 F
11.5 .08 .54 .02 −.10 .00 .07
5.9 .04 2.81 .04 .23 .04 .04 .31 5.19**
Parasomnias
Sleep Duration
β
B
SE B
.25* .03 .07 −.07 .09 .34
68.5** .02 8.0 .61 .86 .02 −.17
27.3 .20 13.0 .16 1.1 .18 .17 .37 6.70***
β
B
SE B
β
.01 .08 .57** .13 .02 −.18
1.9 .00 12.9 .10 −.49 .01 .00
10.8 .08 5.14 .06 .42 .07 .07 .22 3.24**
.00 .36** .27 −.21 .05 .00
NCCPC-R: Non-Communicating Children’s Pain Checklist–Revised; F: Facial subscale. *p < .05; ** p< .01; *** p< .001.
noted that the normative data for this measure is based on a 2-hour observation period, rather than the 1-week retrospective report often used in previous iterations of this measure; thus comparison to previous reports using the 2-hour time frame should be made with caution. Researchers are currently in the process of procuring more well-specified cutoffs on the NCCPC-R for ASD populations and assessing validity among populations with high rates of medical comorbidities (Breau, 4 February 2013, personal communication). The initial findings here indicate a possibly elevated rate and intensity of parentreported clinical pain in youth with ASD. These elevated rates of sleep problems and pain-related behaviors indicate important medical and clinical considerations for youth with ASD. While these disturbances may be widely prevalent, they may be related to highly distinct etiologies across children; for example, one child with ASD may experience ongoing mild digestive discomfort, while another may experience severe inflammatory bowel disease. Nevertheless, these problems in any form may interfere with youth’s response to behavioral intervention and pharmacological treatments, as well as their ability to function in various social contexts. Together, the prevalence of these problems in the current sample supports increased consideration of these factors in assessment and treatment planning for youth with ASD.
Sleep problems predicted by pain-related behaviors Pain-related behavior predicted overall sleep problems, consistent with previous findings among youth with DDs (Breau and Camfield, 2011). However, the current results suggest that not all specific sleep problems are predicted by pain-related behaviors consistently. Problems with sleep duration, parasomnias, and sleep-disordered breathing were predicted by pain-related behaviors over and
above the other specific sleep problems. Breau and Camfield (2011) identified youth with parent-reported pain as experiencing more parasomnias and sleep-disordered breathing, but did not identify such a relationship in regard to sleep duration. Additionally, the previous study identified night wakings as occurring more frequently in youth with pain, in contrast to the current results. These dissimilar findings may be unique to the different mode of pain assessment used here. Specifically, our current use of a standardized pain measure for youth with communication difficulties may provide a more sensitive assessment than the dichotomous “pain” versus “no pain” measure used by previous study. Additionally, our sample may represent a diagnostically distinct group of youth, while the previous study recruited youth with a variety of DDs. This differentiation crucially indicates important differences in the pain–sleep relationship unique to this population, especially given that past research suggests that children with ASD experience more sleep problems and a larger variety of specific sleep problems than TD children, and those with Down Syndrome or Prader–Willi syndrome (Cotton and Richdale, 2006).
Sleep problems predicted by pain-related communication Problems with sleep duration, parasomnias, and sleep-disordered breathing were all predicted by specific forms of pain-related communication. Problems with sleep duration were predicted by social communication of pain, such as comfort-seeking and being difficult to pacify. It is possible that youth who engage in social pain communication naturally sleep less because they are more likely to engage in attention- or comfort-seeking behavior before bed or during night wakings, thus shortening their sleep duration. Furthermore, mothers may report higher levels of sleep duration problems for these children because of their own
298 lack of sleep. Mothers of children with ASD appear more likely to experience sleep problems when their children experience sleep problems, possibly due to comfort-seeking or the need to supervise the child (Hodge et al., 2013; Lopez-Wagner et al., 2008). As such, the social communication of pain may predict shorter sleep duration because of the related behaviors that interfere with quickly transitioning to sleep and mothers’ inability to sleep. Parasomnias were predicted by facial communication of pain, such as grimacing or brow furrowing, which has been evinced as the most common observable form of pain expression in one laboratory study of young children with ASD (Nader et al., 2004). It is possible that parasomnias are predicted by facial communication of pain due to the grimacing and gnashing that may uniquely occur during parasomnias themselves (e.g. night terrors, nightmares), suggesting excessive overlap of measured constructs on these subscales. Future research may benefit from examining parent report of pain among youth with ASD who experience parasomnias, as pain-related behaviors may be subsumed within parasomnia behavioral presentation. Sleep-disordered breathing was predicted by vocal communication of pain, such as moaning or yelling. Like parasomnias, behavioral presentation of sleep-disordered breathing (e.g. gasping, snorting) may overlap with vocally communicated pain behaviors. However, asthma may be a significant predictor of sleep problems in youth with ASD (Liu et al., 2006) and related symptoms can often exacerbate at night (Bohadana et al., 2002). Here, asthma significantly moderated the relationship between vocal pain and sleep-disordered breathing, indicating it to only be present for those who were not reported to have asthma. It is possible that participants who experience sleep-disordered breathing are suffering from other respiratory-related complaints, such as allergies or obesity. Alternatively, youth with asthma may be more likely to exhibit respiratoryrelated problems across a variety of situations besides sleep and, subsequently, demonstrate multiple forms of pain-related communication, including nonvocal behaviors. Future research should further examine how painrelated behaviors are communicated among youth with ASD and various respiratory complaints as compared to those without respiratory complaints. Studies that incorporate observational and laboratory measures of both sleepdisordered breathing and daytime respiratory function may be especially useful in expanding upon the current results. Contrary to expectations, verbal ability and pain-related health condition (GI problems or asthma) did not moderate the obtained relationships between specific sleep problems and pain-related communication. This differs from previous findings related to youth with ID, wherein the presence of medical condition explained the relationships between pain and sleep problems (Ghanizadeh and Faghih, 2009). Most notably, the relationships demonstrated in the current study may reflect the severe behavioral disturbances
Autism 19(3) associated with ASD (e.g. Hartley et al., 2008; Lecavalier, 2006). Alternatively, the lack of moderating effects of verbal ability or health problems may reflect a high pain prevalence that is consistent across the sample regardless of diagnosed health conditions.
Limitations and future directions Several factors in this study limit interpretation and generalization results. First, the participants were recruited online and identified through parent report of diagnosis. Diagnostic confirmation is necessary to support diagnostic validity of the ASD sample. Similarly, all data were parent reported and, therefore, dependent on subjective recall of their child’s behaviors. While the pain measure used here is standardized for youth with communication difficulties, this high rate raises important questions about pain, and the measurement thereof, in youth with ASD. Presently, many NCCPC-R items may overlap with emotional distress, problem behavior, or other behavioral disturbances related to difficulties with communication, as seen in previous studies (e.g. Walsh et al., 2012), and further examination of the discriminant validity of this measure and measures of other behavioral symptoms is warranted. Furthermore, data were collected cross-sectionally. Data collection over multiple time periods could aid in understanding any potential causal relationships between pain and sleep problems and could be useful in identifying potential mediators (e.g. parenting style, parental stress). This study also possesses a moderate sample size and no comparison group. Future studies would benefit from inclusion of comparison samples of TD youth and those with other DDs to examine whether the obtained relationships are indeed unique to individuals with ASD. Similarly, comparing youth with ASD experiencing chronic pain versus acute pain, as well as those with and without confirmed medical conditions, may better explain differential pain– sleep relationships.
Clinical implications Based on the current results, pediatricians and clinicians who work with youth with ASD who also have sleep problems may consider assessing pain-related behaviors, which may otherwise not be part of a differential assessment procedure. Such information may be helpful in understanding where to first target pharmacological or behavioral intervention (e.g. pain-focused intervention versus sleepfocused intervention). Parents may also benefit from monitoring the sleep health of youth with ASD who display high levels of pain-related behaviors, given that these children may be more likely to experience sleep-disordered breathing, parasomnias, and shorter sleep intervals, all of which can impact their child’s functioning.
Tudor et al. Furthermore, the pain–sleep relationships suggested here may serve as indicators for designing antecedentbased interventions. For example, parents of youth with ASD who are experiencing parasomnias may benefit from understanding the antecedents of their child’s facial communication of pain. Results may assist parents in implementing preventive strategies for their child’s pain, which may have collateral effects on sleep. Identifying the antecedents and consequences of socially communicated pain could help parents and clinicians create interventions (e.g. increasing child’s self-soothing). Most importantly, future research may indicate that pain and sleep problems may have an impact on the quality of life for youth with ASD and their families by improving their overall health and functionality (e.g. Carr and Owen-DeSchryver, 2007; Koegel et al., 1992). Like those with other DDs, youth with ASD may experience sleep disrupted by pain-related behaviors, although the incidence of these problems may be higher in youth ASD and unique pain–sleep problem relationships may exist for this population. Overall, this study provides further insights into two areas of health-related functioning that may be frequently impacted for these youth. Further study of how pain and sleep problems relate to one another and may affect children’s daytime functioning, inform effective assessment procedures, and impact overall quality of life is encouraged. Acknowledgements The authors thank Dr Steve M Edelson for his valued support, and James Rankin for his research assistance. The study was made possible by and carried out in fond memory of Dr Edward G Carr.
Funding This study was funded by the Autism Research Institute (ARI).
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