- Email: [email protected]
Assessment of parent report and actigraphy for sleep in children with autism spectrum disorders. Pilot study
Neurology, Psychiatry and Brain Research 23 (2017) 16–19
Contents lists available at ScienceDirect
Neurology, Psychiatry and Brain Research journal homepage: www.elsevier.com/locate/npbr
Assessment of parent report and actigraphy for sleep in children with autism spectrum disorders. Pilot study Nouf AlBackera,* , Shahid Bashirb a b
Department of Pediatric, Faculty of Medicine, King Saud University, Riyadh, Saudi Arabia Department of Physiology, Faculty of Medicine, King Saud University, Riyadh, Saudi Arabia
A R T I C L E I N F O
A B S T R A C T
Article history: Received 29 July 2016 Received in revised form 9 October 2016 Accepted 4 November 2016 Available online xxx
Objective: Sleep problems are common in children with autism spectrum disorders (ASD) and that in turn impact adversely on child behavioral problems. However, in Middle East, there have been few studies of sleep problems in children with ASD. The main objective of this study was to measures sleep pattern that differentiated ASD children with and without parental sleep concerns, and correlated with objective measures by actigraphy. Childhood Autism Rating Scale (CARS) score in ASD was used to measure the severity of score. Methods: The Children’s Sleep Habits Questionnaire (CSHQ) and actigraphy-measured data from 18 ASD children (15 males and 3 females; mean age 5.2 years) were evaluated. Results: ASD poor sleepers (based on CSHQ score) significantly differed from ASD good sleepers on actigraphic (sleep latency, sleep efficiency, fragmentation) and were reported severe behaviors problems based on CARS score. Conclusion: This work provides the basis for focused studies to understand sleep in ASD population and targeted interventions to improve it but large scale studies are recommended. The study also shows that sleep problem are related to problematic behavior in ASD children. ã 2016 Elsevier GmbH. All rights reserved.
1. Introduction Autism spectrum disorder (ASD) is a neurodevelopmental disorder characterized by impairments in communication, imagination, social interaction, and the presence of restricted and repetitive behavioral patterns (American Psychiatric Association, 2013). ASD is among the most enigmatic disorders of child development, with a dramatic increase in prevalence from 1 in 88 children in 2008 to 1 in 68 children in 2010 (Al-Salehi, Al-Hifthy, & Ghaziuddin, 2009). Prevalence of ASD in the Arab world ranges from 1.4 cases per 10000 to 29 per 10000 (Gottesman & Gould, 2003). The severity of clinical feature is quite variable in phenotypes (Couturier et al., 2005; Mulder et al., 2004; Prager, Bergstrom, Wynn, & Braga, 2016; Tuchman & Cuccaro, 2011). Sleep disorders are common associated conditions in ASD (Krakowiak, GoodlinJones, Hertz-Picciotto, Croen, & Hansen, 2008), with a prevalence estimated to range from 44 to 83% (Park et al., 2012; Tudor, Hoffman, & Sweeney, 2012). Defining sleep status can be
* Corresponding author. E-mail address: [email protected] (N. AlBacker). http://dx.doi.org/10.1016/j.npbr.2016.11.004 0941-9500/ã 2016 Elsevier GmbH. All rights reserved.
challenging in study ASD populations mostly data derived from parent report through Children’s Sleep Habits Questionnaire (CSHQ, Owens et al., 2000) (Owens, Spirito, & McGuinn, 2000). Children with ASD commonly have parentreported difficulties with sleep onset and maintenance including long sleep onset latencies, short night sleep duration,and early morning waking (Krakowiak et al., 2008; Richdale, Baker, Short, & Gradisar, 2014). It is not clear how parent reports of different sleep behaviors relate to each other in children with ASD. Research about sleep disorder in ASD population in Arab world is scare. Objective measures used to define sleep concerns in a child with ASD include actigraphy and polysomnography (PSG). PSG differentiated significant parental sleep concerns from those who did not had ASD children (Baker, Richdale, Short, & Gradisar, 2013; Malow, Marzec, McGrew, Wang, & Stone, 2006; Sivertsen, Posserud, Gillberg, Lundervold, & Hysing, 2012). There are some concern in children with ASD to tolerate PSG for tactile sensitivities and for sleeping with wires. Second issue about PSG is a costly methodology and the limited amount of information provided by a pediatric PSG study may not justify its large expense as compared to actigraphy, a modality that measures sleep and wake patterns based on limb movement. Actigraphy is less interfering than PSG.
N. AlBacker, S. Bashir / Neurology, Psychiatry and Brain Research 23 (2017) 16–19
However, studies have shown mixed results in using actigraphy to define parental sleep concerns in ASD (Goodlin-Jones, Sitnick, Tang, Liu, & Anders, 2008; Hall et al., 2015; Sitnick, Goodlin-Jones, & Anders, 2008; Wiggs & Stores, 2004). The aim of the present study was to determine the relationship of parent-reported sleep pattern on the CSHQ, with actigraphy and Childhood Autism Rating Scale (CARS) as measures of social and cognitive impairments in patients with autism was screened among the measured parameters. 2. Material and methods 2.1. Subjects A total of 18 subjects diagnosed with an ASD, aged from 4 to 10 yrs-old (15 males, 3 females) were recruited for the study (Table 1). The study subjects had bodyweights between 16.5 kg to 48.3 kg. Patients fulfilled the criteria for the diagnosis of autism according to the 4th edition of the Diagnostic and Statistical Manual of Mental Disorders (American Psychiatric Association, 2013). The local Ethical Committee of the Faculty of Medicine, King Saud University, Riyadh, Saudi Arabia, approved this study. In addition, an informed written consent of participation in the study was signed by the parents or the legal guardians of the investigated subjects according to the Helsinki principles. 2.2. Sleep measures 2.2.1. Children’s sleep habits questionnaire (CSHQ) The CSHQ is a retrospective, 45-item parent questionnaire that has been validated to examine sleep behavior in young children including ASD (Owens et al., 2000). The CSHQ includes items relating to a number of key sleep domains that encompass the major presenting clinical sleep complaints in this age group: such as bedtime resistance, sleep anxiety, sleep onset delay, sleep duration, and night waking, as well as other dimensions such as sleep disordered and morning waking/daytime sleepiness. Parents are requested to recall sleep behaviors occurring over a recent week. 2.3. Clinical measure 2.3.1. Childhood autism rating scale (CARS) Study participants were evaluated using a CARS test conducted only by a single study investigator (NA) who observed the subjects and interviewed the parent(s). The CARS test is a 15-item behavioral rating scale (relating to people, emotional response, imitation, body use, object use, listening response, fear or nervousness, verbal communication, non-verbal communication, activity level, consistency of intellectual response, adaptation to change, taste, touch and smell response and general impressions) developed to identify autism as well as to quantitatively describe the severity of the disorder (Schopler, Reichler, & Rochen Renner, 1988). The CARS test is a well-established measure of autism severity and a reliable and stable indicator of autism in any child over 2 years of age as well as adolescents (Schopler et al., 1988).
Table 1 Participant characteristics.
Age (Years) Gender (Male) CARS Score
ASD-Poor Sleep n = 10
ASD-Good Sleep n = 8
7.2 2.14 8 7 mild and 3 severe
7.02 2.93 7 4 mild and 4 severe
17
2.4. Actigraphy Actigraphy measurements were obtained with the use of AW64 Actiwatch1 monitors (Philips Respironics, Bend OR). It is a noninvasive method of monitoring human rest/activity sleep cycles. Children were to undergo two consecutive weeks of actigraphy monitoring for her or his normal routines while the required data is being recorded in his or her natural sleep environment. Actigraphy has been used to assess sleep/wake behavior (Anders, Iosif, Schwichtenberg, Tang, & Goodlin-Jones, 2011; Sadeh, Gruber, & Raviv, 2002). Data from the actigraphs were downloaded to a personal computer where all sleep intervals were manually placed on an actogram, or visual representation of the actigraphy data. Following parameter was used to asses the sleep pattern: 1) the total nighttime sleep duration (TST). 2) Sleep efficiency (SE). 3) Sleep latency (SL). 4) Wake after sleep onset. 5) The fragmentation index (FI) (Souders et al., 2009). All sleep variables were calculated using Actiware V5 software (Philips Respironics, Bend OR).
2.5. Statistical analysis Actigraphy parameters were averaged across nights for each participant. Descriptive statistics were conducted on all major variables. Mann-Whitney U tests were used for pair-wise betweengroup comparisons. Spearman rank correlations (rs) were used to evaluate associations between actigraphic sleep variables, subjective sleep measures, and behavioral scales. Results are presented as mean (standard deviation) and given the pilot nature of the study, we did not pursue formal multiple comparison adjustment. A p-value of less than 0.05 was considered statistically significant. Analyses were performed using SPSS V 16 (Chicago, IL).
3. Results 18 children participated in the study between November 2015 and March 2016. Out of the 18 children with ASD, 8 were classified by their parents as good sleepers (ASD-GS) and 10 were classified as poor sleepers (ASD-PS) based upon the CSHQ. The general characteristics of the study participants in Table 1. Sleep histories were reviewed in all participants. In the ASD-PS group (10 of 18) having moderate to severe sleep problems expressed by parents. Night wakings were of major concern in 9 of 18 children. In the ASD-GS group, 5 parents rated their children as having no sleep problems and 3 as having mild sleep problems. Several of the ASD good sleepers requested to go to bed at a scheduled time each night. CSHQ-reported bed-times derived using sleep diaries were not different from bed-times that were and event markers accompanying actigraphy records. In contrast, CSHQ-reported bed-times were different (p < 0.03) from actigraphy-measured times of sleep onset. All CSHQ scales differed significantly between the two groups (Table 2), scoring lower in ASD-GS than the ASD-PS groups. CSHQ subscale item scores for sleep-duration (p < 0.01), sleep anxiety (p < 0.04) and daytime sleepiness (p < 0.03) between two group (Table 2). Actigraphy parameters were significant difference for Sleep Latency (minutes), Sleep Efficiency (minutes), Wake After Sleep Onset (minutes), and Movement & Fragmentation Index among ASD-PS, ASD-GS (Table 3, Fig. 1).
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N. AlBacker, S. Bashir / Neurology, Psychiatry and Brain Research 23 (2017) 16–19
Table 2 Comparison of Children’s Sleep Habits Questionnaire Subscales Among ASD Poor Sleepers, ASD Good Sleepers.
Subscale Bedtime Resistance Sleep Onset Delay Sleep Duration Sleep Anxiety Night Wakings Sleep Disordered Breathing Daytime Sleepiness Total
ASD-PS
ASD-GS
Significance1
n = 10 7.8 3.2 2.1 1.1 4.9 1.4 6.9 1.8 6.4 2.7 4.2 1.8 14.8 4.3 54.2 7.8
n=8 7.2 2.4 1.7 0.08 3.9 1.2 5.6 1.5 5.6 1.4 4.1 1.1 12.4 2.1 46 9.1
0.54 0.03 0.01 0.04 0.07 0.20 0.03 0.02
Significant at <0.05 between ASD_GS and ASD_PS groups with Mann-Whitney U.
Table 3 Comparison of Actigraphy Parameters Among ASD Poor Sleepers, ASD Good Sleepers.
Actigraphy Measured Sleep Sleep Latency (minutes) Sleep Efficiency (minutes) Wake After Sleep Onset (minutes) Total Sleep Time (minutes) Movement & Fragmentation Index
ASD-PS
ASD-GS
Significance
n = 10 57.1 26.4 77.1 5.2 38.1 14.1 472.5 62.1 14.1 2.5
n=8 32.8 17.4 85.1 4.6 23.1 4.3 470.1 57.6 10.1 3.7
0.54 0.01 0.05 0.02 0.78 0.03
Significant at <0.05 between ASD_GS and ASD_PS groups with Mann-Whitney U.
4. Discussion Our findings support the hypothesis that parental reports of sleep concerns in children with ASD can be confirmed not only by comprehensive questionnaires but also by objective measures that include actigraphy. In this study, we showed that Children classified as poor sleepers in ASD had more sleep problems, had longer sleep latency on actigraphy, and more sleep fragmentation on actigraphy including and also had more behavioral problems as compared to good sleepers ASD. Our work is the first to simultaneously assess the ability actigraphy to distinguish sleep patterns in children with ASD based
on parental concern in Arab world. We had expected to find that actigraphy were comparable in distinguishing sleep patterns. However, while two week of actigraphy and sleep diaries were significantly positively correlated, mean values differed, with diaries underreporting sleep latency compared with actigraphy (Baker et al., 2013; Sivertsen et al., 2012). They concluded that actigraphy had poor agreement in detecting nocturnal awakenings compared to video recordings. Two other studies that included older children with ASD also found discrepancies between parent report and actigraphy, although in contrast to Goodlin-Jones et al. (2008) reported that parents appeared to over report sleep problems in their children (Anders et al., 2011; Wiggs & Stores, 2004). The differences between these studies and ours may be attributable to following factors restricted age range, with a sample limited to children without intellectual disability, epilepsy, or psychiatric conditions requiring psychotropic medications. Such factors may have contributed to the integrity of our data and decreased variability in actigraphic measurements. 4.1. Strengths/limitations The present study also attempted to minimize the effects of study drop-out for potential reactions for actigraphic wearing time and collection of data. These particular scoring CARS and CSHQ measurements were conducted by the study investigators on each child. For CARS score outcome measurement evaluated, the relative change for the parameter following 2-weeks of wearing actigraphy watch in comparison to parent report was examined. One of the potential limitations of the present study is the small sample size examined. The small sample size in the present study may have resulted in specific effects of CSHQ and actigraphy measurements being missed because of lack of statistical power to detect significant changes between the good and bad sleeper groups. The data from the present study provide the basis for a larger, more focused study on the promising elements. A further potential limitation of the present study is the exact mechanism of action of sleep was not elucidated from the present study. Finally, an additional potential limitation of the present
Fig. 1. Comparison of actigraphy parameters among ASD poor sleepers, ASD good sleepers.
N. AlBacker, S. Bashir / Neurology, Psychiatry and Brain Research 23 (2017) 16–19
study is the fact that the wearing time of actigraphy watch used may not have been optimal. 5. Conclusion In summary, our results suggest that actigraphy are complementary objective measures for defining sleep that substantiate parental report. Defining the phenotype of sleep in ASD, its relation to daytime behavior, and appropriate measurement modalities provides the foundation for focused studies of sleep pathophysiology and targeted interventions in this population. In addition, reports of sleep-onset delay on the CSHQ were more closely related to the objective measurements of this behavior following treatment. Acknowledgment Work on this study was supported by grant from Deanship of Scientific Research (RGP 216) King Saud University, Saudi Arabia. References Al-Salehi, S. M., Al-Hifthy, E. H., & Ghaziuddin, M. (2009). Autism in Saudi Arabia: Presentation, clinical correlates and comorbidity. Transcultural Psychiatry, 46 (June (2)), 340–347. http://dx.doi.org/10.1177/1363461509105823. American Psychiatric Association (2013). Diagnostic and statistical manual of mental disorders (DSM-V) 5. Arlington: American Psychiatric Association. Anders, T. F., Iosif, A. M., Schwichtenberg, A. J., Tang, K., & Goodlin-Jones, B. L. (2011). Six-month sleep-wake organization and stability in preschool-age children with autism, developmental delay, and typical development. Behavioral Sleep Medicine, 9, 92–106. http://dx.doi.org/10.1080/15402002.2011.557991. Baker, M., Richdale, A., Short, M., & Gradisar, M. (2013). An investigation of sleep patterns in adolescents with high-functioning autism spectrum disorder compared with typically developing adolescents. Developmental Neurorehabilitation, 16, 155–165. http://dx.doi.org/10.3109/ 17518423.2013.765518. Couturier, J. L., Speechley, K. N., Steele, M., Norman, R., Stringer, B., & Nicolson, R. (2005). Parental perception of sleep problems in children of normal intelligence with pervasive developmental disorders: Prevalence, severity, and pattern. Journal American Academy Child Adolescent Psychiatry, 44, 815–822. Goodlin-Jones, B. L., Sitnick, S. L., Tang, K., Liu, J., & Anders, T. F. (2008). The children’s sleep habits questionnaire in toddlers and preschool children. Journal Developmental Behavioral Pediatrics, 29, 82–88. Gottesman, I. I., & Gould, T. D. (2003). The endophenotype concept in psychiatry: Etymology and strategic intentions. American Journal Psychiatry, 160, 636–645.
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Hall, W. A., Hutton, E., Brant, R. F., Collet, J. P., Gregg, K., Saunders, R., et al. (2015). A randomized controlled trial of an intervention for infants’ behavioral sleep problems. BMC Pediatrics, 13(November (15)), 181. Krakowiak, P., Goodlin-Jones, B., Hertz-Picciotto, I., Croen, L. A., & Hansen, R. L. (2008). Sleep problems in children with autism spectrum disorders, developmental delays, and typical development: A population-based study. Journal Sleep Research, 17, 197–206. Malow, B. A., Marzec, M., McGrew, S. G., Wang, L., & Stone, W. (2006). Characterizing sleep in children with autism spectrum disorders: A multidimensional approach. Sleep, 29, 1563–1571. Mulder, E. J., Anderson, G. M., Kema, I. P., de Bildt, A., van Lang, N. D., den Boer, J. A., et al. (2004). Platelet serotonin levels in pervasive developmental disorders and mental retardation: Diagnostic group differences, within-group distribution, and behavioral correlates. Journal American Academy Child Adolescent Psychiatry, 43, 491–499. Owens, J. A., Spirito, A., & McGuinn, M. (2000). The Children’s Sleep Habits Questionnaire (CSHQ): Psychometric properties of a survey instrument for school-aged children. Sleep, 23, 1043–1051. Park, S., Cho, S.-C., Cho, I. H., Kim, B.-N., Kim, J.-W., Shin, M.-S., et al. (2012). Sleep problems and their correlates and comorbid psychopathology of children with autism spectrum disorders. Research in Autism Spectrum Disorders, 6, 1068– 1072. http://dx.doi.org/10.1016/j.rasd.2012.02.004. Prager, E. M., Bergstrom, H. C., Wynn, G. H., & Braga, M. F. (2016). The basolateral amygdala g-aminobutyric acidergic system in health and disease. Journal of Neuroscience Research, 94(June (6)), 548–567. Richdale, A. L., Baker, E., Short, M., & Gradisar, M. (2014). The role of insomnia, presleep arousal and psychopathology symptoms in daytime impairment in adolescents with high functioning autism spectrum disorder. Sleep Medicine, 15, 1082–1088. http://dx.doi.org/10.1016/j.sleep.2014.05.005. Sadeh, A., Gruber, R., & Raviv, A. (2002). Sleep, neurobehavioral functioning, and behavior problems in school-age children. Child Development, 73, 405–417. Schopler, E., Reichler, R., & Rochen Renner, B. (1988). The childhood autism rating scale. Western Psychological Services. Sitnick, S. L., Goodlin-Jones, B. L., & Anders, T. F. (2008). The use of actigraphy to study sleep disorders in preschoolers: Some concerns about detection of nighttime awakenings. Sleep, 31(3), 395–401. Sivertsen, B., Posserud, M. B., Gillberg, C., Lundervold, A. J., & Hysing, M. (2012). Sleep problems in children with autism spectrum problems: A longitudinal population-based study. Autism, 16, 139–150. http://dx.doi.org/10.1177/ 1362361311404255. Souders, M. C., Mason, T. B., Valladares, O., Bucan, M., Levy, S. E., Mandell, D., et al. (2009). Sleep behaviors and sleep quality in children with autism spectrum disorders. Sleep, 32, 1566–1578. Tuchman, R., & Cuccaro, M. (2011). Epilepsy and autism: Neurodevelopmental perspective. Current Neurology Neuroscience Reports, 11, 428–434. Tudor, M. E., Hoffman, C. D., & Sweeney, D. P. (2012). Children with autism: Sleep problems and symptom severity. Focus on Autism and Other Developmental Disabilities, 27, 254–262. http://dx.doi.org/10.1177/1088357612457989. Wiggs, L., & Stores, G. (2004). Sleep patterns and sleep disorders in children with autistic spectrum disorders: Insights using parent report and actigraphy. Developmental Medicine Child Neurology, 46, 372–380.
Contents lists available at ScienceDirect
Neurology, Psychiatry and Brain Research journal homepage: www.elsevier.com/locate/npbr
Assessment of parent report and actigraphy for sleep in children with autism spectrum disorders. Pilot study Nouf AlBackera,* , Shahid Bashirb a b
Department of Pediatric, Faculty of Medicine, King Saud University, Riyadh, Saudi Arabia Department of Physiology, Faculty of Medicine, King Saud University, Riyadh, Saudi Arabia
A R T I C L E I N F O
A B S T R A C T
Article history: Received 29 July 2016 Received in revised form 9 October 2016 Accepted 4 November 2016 Available online xxx
Objective: Sleep problems are common in children with autism spectrum disorders (ASD) and that in turn impact adversely on child behavioral problems. However, in Middle East, there have been few studies of sleep problems in children with ASD. The main objective of this study was to measures sleep pattern that differentiated ASD children with and without parental sleep concerns, and correlated with objective measures by actigraphy. Childhood Autism Rating Scale (CARS) score in ASD was used to measure the severity of score. Methods: The Children’s Sleep Habits Questionnaire (CSHQ) and actigraphy-measured data from 18 ASD children (15 males and 3 females; mean age 5.2 years) were evaluated. Results: ASD poor sleepers (based on CSHQ score) significantly differed from ASD good sleepers on actigraphic (sleep latency, sleep efficiency, fragmentation) and were reported severe behaviors problems based on CARS score. Conclusion: This work provides the basis for focused studies to understand sleep in ASD population and targeted interventions to improve it but large scale studies are recommended. The study also shows that sleep problem are related to problematic behavior in ASD children. ã 2016 Elsevier GmbH. All rights reserved.
1. Introduction Autism spectrum disorder (ASD) is a neurodevelopmental disorder characterized by impairments in communication, imagination, social interaction, and the presence of restricted and repetitive behavioral patterns (American Psychiatric Association, 2013). ASD is among the most enigmatic disorders of child development, with a dramatic increase in prevalence from 1 in 88 children in 2008 to 1 in 68 children in 2010 (Al-Salehi, Al-Hifthy, & Ghaziuddin, 2009). Prevalence of ASD in the Arab world ranges from 1.4 cases per 10000 to 29 per 10000 (Gottesman & Gould, 2003). The severity of clinical feature is quite variable in phenotypes (Couturier et al., 2005; Mulder et al., 2004; Prager, Bergstrom, Wynn, & Braga, 2016; Tuchman & Cuccaro, 2011). Sleep disorders are common associated conditions in ASD (Krakowiak, GoodlinJones, Hertz-Picciotto, Croen, & Hansen, 2008), with a prevalence estimated to range from 44 to 83% (Park et al., 2012; Tudor, Hoffman, & Sweeney, 2012). Defining sleep status can be
* Corresponding author. E-mail address: [email protected] (N. AlBacker). http://dx.doi.org/10.1016/j.npbr.2016.11.004 0941-9500/ã 2016 Elsevier GmbH. All rights reserved.
challenging in study ASD populations mostly data derived from parent report through Children’s Sleep Habits Questionnaire (CSHQ, Owens et al., 2000) (Owens, Spirito, & McGuinn, 2000). Children with ASD commonly have parentreported difficulties with sleep onset and maintenance including long sleep onset latencies, short night sleep duration,and early morning waking (Krakowiak et al., 2008; Richdale, Baker, Short, & Gradisar, 2014). It is not clear how parent reports of different sleep behaviors relate to each other in children with ASD. Research about sleep disorder in ASD population in Arab world is scare. Objective measures used to define sleep concerns in a child with ASD include actigraphy and polysomnography (PSG). PSG differentiated significant parental sleep concerns from those who did not had ASD children (Baker, Richdale, Short, & Gradisar, 2013; Malow, Marzec, McGrew, Wang, & Stone, 2006; Sivertsen, Posserud, Gillberg, Lundervold, & Hysing, 2012). There are some concern in children with ASD to tolerate PSG for tactile sensitivities and for sleeping with wires. Second issue about PSG is a costly methodology and the limited amount of information provided by a pediatric PSG study may not justify its large expense as compared to actigraphy, a modality that measures sleep and wake patterns based on limb movement. Actigraphy is less interfering than PSG.
N. AlBacker, S. Bashir / Neurology, Psychiatry and Brain Research 23 (2017) 16–19
However, studies have shown mixed results in using actigraphy to define parental sleep concerns in ASD (Goodlin-Jones, Sitnick, Tang, Liu, & Anders, 2008; Hall et al., 2015; Sitnick, Goodlin-Jones, & Anders, 2008; Wiggs & Stores, 2004). The aim of the present study was to determine the relationship of parent-reported sleep pattern on the CSHQ, with actigraphy and Childhood Autism Rating Scale (CARS) as measures of social and cognitive impairments in patients with autism was screened among the measured parameters. 2. Material and methods 2.1. Subjects A total of 18 subjects diagnosed with an ASD, aged from 4 to 10 yrs-old (15 males, 3 females) were recruited for the study (Table 1). The study subjects had bodyweights between 16.5 kg to 48.3 kg. Patients fulfilled the criteria for the diagnosis of autism according to the 4th edition of the Diagnostic and Statistical Manual of Mental Disorders (American Psychiatric Association, 2013). The local Ethical Committee of the Faculty of Medicine, King Saud University, Riyadh, Saudi Arabia, approved this study. In addition, an informed written consent of participation in the study was signed by the parents or the legal guardians of the investigated subjects according to the Helsinki principles. 2.2. Sleep measures 2.2.1. Children’s sleep habits questionnaire (CSHQ) The CSHQ is a retrospective, 45-item parent questionnaire that has been validated to examine sleep behavior in young children including ASD (Owens et al., 2000). The CSHQ includes items relating to a number of key sleep domains that encompass the major presenting clinical sleep complaints in this age group: such as bedtime resistance, sleep anxiety, sleep onset delay, sleep duration, and night waking, as well as other dimensions such as sleep disordered and morning waking/daytime sleepiness. Parents are requested to recall sleep behaviors occurring over a recent week. 2.3. Clinical measure 2.3.1. Childhood autism rating scale (CARS) Study participants were evaluated using a CARS test conducted only by a single study investigator (NA) who observed the subjects and interviewed the parent(s). The CARS test is a 15-item behavioral rating scale (relating to people, emotional response, imitation, body use, object use, listening response, fear or nervousness, verbal communication, non-verbal communication, activity level, consistency of intellectual response, adaptation to change, taste, touch and smell response and general impressions) developed to identify autism as well as to quantitatively describe the severity of the disorder (Schopler, Reichler, & Rochen Renner, 1988). The CARS test is a well-established measure of autism severity and a reliable and stable indicator of autism in any child over 2 years of age as well as adolescents (Schopler et al., 1988).
Table 1 Participant characteristics.
Age (Years) Gender (Male) CARS Score
ASD-Poor Sleep n = 10
ASD-Good Sleep n = 8
7.2 2.14 8 7 mild and 3 severe
7.02 2.93 7 4 mild and 4 severe
17
2.4. Actigraphy Actigraphy measurements were obtained with the use of AW64 Actiwatch1 monitors (Philips Respironics, Bend OR). It is a noninvasive method of monitoring human rest/activity sleep cycles. Children were to undergo two consecutive weeks of actigraphy monitoring for her or his normal routines while the required data is being recorded in his or her natural sleep environment. Actigraphy has been used to assess sleep/wake behavior (Anders, Iosif, Schwichtenberg, Tang, & Goodlin-Jones, 2011; Sadeh, Gruber, & Raviv, 2002). Data from the actigraphs were downloaded to a personal computer where all sleep intervals were manually placed on an actogram, or visual representation of the actigraphy data. Following parameter was used to asses the sleep pattern: 1) the total nighttime sleep duration (TST). 2) Sleep efficiency (SE). 3) Sleep latency (SL). 4) Wake after sleep onset. 5) The fragmentation index (FI) (Souders et al., 2009). All sleep variables were calculated using Actiware V5 software (Philips Respironics, Bend OR).
2.5. Statistical analysis Actigraphy parameters were averaged across nights for each participant. Descriptive statistics were conducted on all major variables. Mann-Whitney U tests were used for pair-wise betweengroup comparisons. Spearman rank correlations (rs) were used to evaluate associations between actigraphic sleep variables, subjective sleep measures, and behavioral scales. Results are presented as mean (standard deviation) and given the pilot nature of the study, we did not pursue formal multiple comparison adjustment. A p-value of less than 0.05 was considered statistically significant. Analyses were performed using SPSS V 16 (Chicago, IL).
3. Results 18 children participated in the study between November 2015 and March 2016. Out of the 18 children with ASD, 8 were classified by their parents as good sleepers (ASD-GS) and 10 were classified as poor sleepers (ASD-PS) based upon the CSHQ. The general characteristics of the study participants in Table 1. Sleep histories were reviewed in all participants. In the ASD-PS group (10 of 18) having moderate to severe sleep problems expressed by parents. Night wakings were of major concern in 9 of 18 children. In the ASD-GS group, 5 parents rated their children as having no sleep problems and 3 as having mild sleep problems. Several of the ASD good sleepers requested to go to bed at a scheduled time each night. CSHQ-reported bed-times derived using sleep diaries were not different from bed-times that were and event markers accompanying actigraphy records. In contrast, CSHQ-reported bed-times were different (p < 0.03) from actigraphy-measured times of sleep onset. All CSHQ scales differed significantly between the two groups (Table 2), scoring lower in ASD-GS than the ASD-PS groups. CSHQ subscale item scores for sleep-duration (p < 0.01), sleep anxiety (p < 0.04) and daytime sleepiness (p < 0.03) between two group (Table 2). Actigraphy parameters were significant difference for Sleep Latency (minutes), Sleep Efficiency (minutes), Wake After Sleep Onset (minutes), and Movement & Fragmentation Index among ASD-PS, ASD-GS (Table 3, Fig. 1).
18
N. AlBacker, S. Bashir / Neurology, Psychiatry and Brain Research 23 (2017) 16–19
Table 2 Comparison of Children’s Sleep Habits Questionnaire Subscales Among ASD Poor Sleepers, ASD Good Sleepers.
Subscale Bedtime Resistance Sleep Onset Delay Sleep Duration Sleep Anxiety Night Wakings Sleep Disordered Breathing Daytime Sleepiness Total
ASD-PS
ASD-GS
Significance1
n = 10 7.8 3.2 2.1 1.1 4.9 1.4 6.9 1.8 6.4 2.7 4.2 1.8 14.8 4.3 54.2 7.8
n=8 7.2 2.4 1.7 0.08 3.9 1.2 5.6 1.5 5.6 1.4 4.1 1.1 12.4 2.1 46 9.1
0.54 0.03 0.01 0.04 0.07 0.20 0.03 0.02
Significant at <0.05 between ASD_GS and ASD_PS groups with Mann-Whitney U.
Table 3 Comparison of Actigraphy Parameters Among ASD Poor Sleepers, ASD Good Sleepers.
Actigraphy Measured Sleep Sleep Latency (minutes) Sleep Efficiency (minutes) Wake After Sleep Onset (minutes) Total Sleep Time (minutes) Movement & Fragmentation Index
ASD-PS
ASD-GS
Significance
n = 10 57.1 26.4 77.1 5.2 38.1 14.1 472.5 62.1 14.1 2.5
n=8 32.8 17.4 85.1 4.6 23.1 4.3 470.1 57.6 10.1 3.7
0.54 0.01 0.05 0.02 0.78 0.03
Significant at <0.05 between ASD_GS and ASD_PS groups with Mann-Whitney U.
4. Discussion Our findings support the hypothesis that parental reports of sleep concerns in children with ASD can be confirmed not only by comprehensive questionnaires but also by objective measures that include actigraphy. In this study, we showed that Children classified as poor sleepers in ASD had more sleep problems, had longer sleep latency on actigraphy, and more sleep fragmentation on actigraphy including and also had more behavioral problems as compared to good sleepers ASD. Our work is the first to simultaneously assess the ability actigraphy to distinguish sleep patterns in children with ASD based
on parental concern in Arab world. We had expected to find that actigraphy were comparable in distinguishing sleep patterns. However, while two week of actigraphy and sleep diaries were significantly positively correlated, mean values differed, with diaries underreporting sleep latency compared with actigraphy (Baker et al., 2013; Sivertsen et al., 2012). They concluded that actigraphy had poor agreement in detecting nocturnal awakenings compared to video recordings. Two other studies that included older children with ASD also found discrepancies between parent report and actigraphy, although in contrast to Goodlin-Jones et al. (2008) reported that parents appeared to over report sleep problems in their children (Anders et al., 2011; Wiggs & Stores, 2004). The differences between these studies and ours may be attributable to following factors restricted age range, with a sample limited to children without intellectual disability, epilepsy, or psychiatric conditions requiring psychotropic medications. Such factors may have contributed to the integrity of our data and decreased variability in actigraphic measurements. 4.1. Strengths/limitations The present study also attempted to minimize the effects of study drop-out for potential reactions for actigraphic wearing time and collection of data. These particular scoring CARS and CSHQ measurements were conducted by the study investigators on each child. For CARS score outcome measurement evaluated, the relative change for the parameter following 2-weeks of wearing actigraphy watch in comparison to parent report was examined. One of the potential limitations of the present study is the small sample size examined. The small sample size in the present study may have resulted in specific effects of CSHQ and actigraphy measurements being missed because of lack of statistical power to detect significant changes between the good and bad sleeper groups. The data from the present study provide the basis for a larger, more focused study on the promising elements. A further potential limitation of the present study is the exact mechanism of action of sleep was not elucidated from the present study. Finally, an additional potential limitation of the present
Fig. 1. Comparison of actigraphy parameters among ASD poor sleepers, ASD good sleepers.
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