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. Author manuscript; available in PMC: 2017 Jun 25.
Published in final edited form as: J Intellect Disabil Res. 2011 Nov 2;56(6):600–608. doi: 10.1111/j.1365-2788.2011.01499.x

Sleep in children and adolescents with Angelman syndrome: association with parent sleep and stress

S E Goldman 1, T J Bichell 2, K Surdyka 1, B A Malow 1
PMCID: PMC5483396  NIHMSID: NIHMS868899  PMID: 22044653

Abstract

Background

Sleep concerns are common in children with Angelman syndrome, with 20–80% of individuals having a decreased sleep need and/or abnormal sleep–wake cycles. The impact of these sleep behaviours on parental sleep and stress is not known.

Method

Through the use of standardised questionnaires, wrist actigraphy and polysomnography, we defined the sleep behaviours of 15 children/adolescents with Angelman syndrome and the association of the child/adolescents sleep behaviours on parental sleep behaviours and parental stress.

Results

Both children/adolescents and their parents exhibited over 1 h of wake time after sleep onset and fragmented sleep. Prolonged sleep latency in the child was associated with parent insomnia and daytime sleepiness. Additionally, variability in child total sleep time was associated with parental stress.

Conclusions

Poor sleep in children/adolescents with Angelman syndrome was associated with poor parental sleep and higher parental stress. Further work is warranted to identify the underlying causes of the poor sleep, and to relate these findings to daytime functioning, behaviour and the family unit.

Keywords: Angelman syndrome, child–parent sleep, parental stress, sleep problems

Introduction

Angelman syndrome, a neurodevelopmental disorder caused by the absence or non-functioning of the maternal UBE3A gene, occurs in an estimated one in 12 000 to one in 20 000 individuals (Williams et al. 2006; Pelc et al. 2008). There are four main genetic mechanisms underlying this disorder: (1) deletions of the 15q11–q13 region on the maternal chromosome (approximately 70% of the cases); (2) parental uniparental disomy in which there are two copies of the 15th chromosome inherited from the father and none from the mother (2–3% of the cases); (3) mutation in the UBE3A gene on maternal chromosome 15 (5–10% of the cases); and (4) an imprinting defect which causes the chromosome 15 inherited from the mother to have the paternal imprint for gene functioning silencing maternal genes in the 15q11–13 region (3–5% of the cases). An additional 10–15% of the cases are diagnosed according to clinical criteria but have no recognisable genetic mutation. Characteristics include developmental delay, intellectual disability (ID), recurrent seizures, lack of speech, and disorders of gait and balance (Williams et al. 2006; Williams 2010).

Sleep disturbances are common in Angelman syndrome, and are included in the diagnostic criteria established in 1995 and in the updated criteria published in 2006 (Williams et al. 1995, 2006). The prevalence of sleep problems in Angelman syndrome ranges from 20% to 80% (Williams et al. 2006). This variation in prevalence may relate to how sleep problems are defined (Pelc et al. 2008). Sleep problems appear more prevalent, and severe, in childhood between the ages of 2 and 9 years; however, in some individuals the sleep problems will persist (Clayton-Smith 1993; Bruni et al. 2004; Didden et al. 2004; Pelc et al. 2008).

Symptoms of insomnia, in particular difficulty initiating or maintaining sleep, are primary concerns (Clayton-Smith 1993; Zhadanova et al. 1999; Bruni et al. 2004; Berry et al. 2005; Walz et al. 2005); however, there have been reports that children with Angelman syndrome may need less sleep than typically developing children (Clayton-Smith 1993; Zhadanova et al. 1999; Bruni et al. 2004; Berry et al. 2005). Poor sleep in these children does not necessarily impact daytime alertness. Few studies have objectively investigated the specific sleep abnormalities present in this disorder. Miano et al. (2004, 2005) found reduced sleep efficiency, a lower percentage and duration of rapid eye movement sleep, and a higher percentage of slow wave sleep in children <8 years when compared to normal controls. Additional research is needed in this area.

The impact of sleep problems on parental sleep is understudied in typically developing children, and even less described in children with developmental disorders. Sleep problems in one family member often impact other members (Dahl & El-Sheikh 2007). In the general population, parents who perceive their child to have a sleep problem are more likely than those who do not to report having too little sleep (National Sleep Foundation 2004). Furthermore, the impact of the child’s sleep on the parent’s sleep is often the reason why a child’s sleep is brought to the attention of a medical professional (Polimeni et al. 2005). Robinson & Richdale (2004) found that parents of children with developmental disabilities, who reported sleep problems in their children, were more likely to note how the child’s sleep negatively affected theirs. Parents of children with autism were found to have poorer sleep quality and shorter sleep quantity than parents of typically developing children (Meltzer 2008). Parents of children with chronic illnesses were found to have sleep disruptions, which possibly explain their higher rates of negative daytime functioning (Meltzer & Moore 2008). Furthermore, mothers of children with poor sleep were found to have more mood problems, and stress problems, than those whose children did not have poor sleep (Meltzer & Mindell 2007). While evidence of poor night-time sleep in the child affecting parental sleep can be seen in other populations with developmental disabilities, minimal information is available on the association of disturbed sleep in children with Angelman syndrome and the impact of disturbed sleep on the primary caregiver.

In this study our goals were to: (1) obtain additional objective and subjective data on sleep in children/adolescents with Angelman syndrome; and (2) relate these sleep patterns to the primary parental caregivers sleep, daytime sleepiness and stress.

Method

Participants and procedure

The study population consisted of 16 children/adolescents, and the parent considered as the primary caregiver, participating in the Angelman Natural History Study at Vanderbilt University who volunteered to participate in the sleep protocol. The sleep protocol consisted of a sleep interview with a sleep clinician, overnight polysomnography (PSG) concurrent with wrist actigraphy, 28 nights of in-home wrist actigraphy and sleep diary, and a standardised sleep questionnaire. All caregivers provided consent, and the protocol was approved by the Institutional Review Board at Vanderbilt University.

Children, accompanied by the parent, were admitted to the Vanderbilt Sleep Research Core, located within the Vanderbilt Clinical Research Center (CRC) to undergo one night of PSG and actigraphy monitoring. After being admitted to the CRC, an actigraph was placed on the non-dominant wrist of the parent and child. The parent was instructed in the use of the devices including that they were to be worn nightly starting several hours before bedtime until waking the next morning, and as tolerated during the day for the next 27 days. Participants were allowed to fall asleep according to their usual bedtime routine and to awaken spontaneously. Lights out (time child first attempted to fall asleep) and lights on (time child awoke) were recorded by the PSG technologist at the beginning and end of the study.

Instrumentation

Actigraphy, used extensively in sleep research and clinical practice, has been validated as a highly reliable method to differentiate sleep from wake (Sadeh & Acebo 2002; Ancoli-Israel et al. 2003). The actiwatch is a small-computerised wristwatch-like device used to detect movement and can serve as a surrogate of sleep and wake (Sadeh & Acebo 2002). Actigraphy measurements were obtained with an Actiwatch AW-64® manufactured by Philips Respironics (Bend, OR, USA). Data from the actigraphs were downloaded to a personal computer where all sleep intervals were manually placed on an actogram. Sleep variables were calculated using Actiware V5 software (Philips Respironics, Bend, OR, USA). The time in bed was calculated from lights out until lights on the next morning. The total sleep duration was the sum of all sleep epochs within the interval between the time set on the actogram for night-time sleep and morning wake time. Sleep efficiency was calculated as the ratio of total night-time sleep duration to the total time in bed. Sleep latency was calculated as the time required for sleep onset after lights out (first attempt to go to sleep). Wake after sleep onset was measured as the sum of all wake epochs during the sleep period and reflects the number of minutes scored as wake that exceeded the sensitivity threshold. The fragmentation index captures all movement regardless of the intensity of the movement.

Polysomnography

Polysomnography data were obtained using the Nihon-Kohden 9200 sleep acquisition system. Monitoring included 21-channel electroencephalography (to evaluate for epileptic seizures), electrooculography, chin and bilateral leg (tibialis anterior) electromyography, nasal thermistor, nasal pressure transducer, electrocardiography, thoracic and abdominal effort, and pulse oximetry. Video was recorded simultaneously as part of the PSG recording. Sleep parameters were calculated for each PSG study by the sleep software package (Polysmith Acquisition and Review software, version 4.0.17.0; Neurotronics, Inc.). Total sleep time was the total time comprised of epochs of sleep, with sleep efficiency calculated as the ratio of total sleep time to total time in bed. Sleep latency was calculated as the time to the first epoch of sleep after lights out, and wake time after sleep onset, as the total time comprised of epochs of wake after sleep onset. Arousal index was calculated based on the American Academy of Sleep Medicine definition of an electroencephalography arousal (Iber et al. 2007). Following acquisition, PSG data were manually scored by a single sleep technologist, using standard criteria (Iber et al. 2007) and reviewed by the senior author.

Questionnaires

Children’s Sleep Habits Questionnaire

Sleep behaviours were evaluated using the Children’s Sleep Habits Questionnaire (CSHQ). The CSHQ is a validated parental questionnaire consisting of 45 items relating to sleep complaints over the past month. The majority of questions are answered on a 3-point scale (1 = rarely, 2 = sometimes, 3 = usually). A total score is calculated, as well as sub-scale scores that measure insomnia-related aspects of sleep including sleep anxiety, sleep duration, sleep onset delay, night wakings, bedtime resistance and other dimensions such as sleep-disordered breathing, parasomnias and daytime sleepiness (Owens et al. 2000). The CSHQ has been used in children with a variety of neurodevelopmental disorders (Malow et al. 2006; Goodlin-Jones et al. 2008) with demonstrated validity and reliability in these disorders.

Parental sleep and stress

Three self-administered questionnaires were used to evaluate the parents sleep behaviours and stress. The Insomnia Severity Index (ISI; Morin 1993) was used by the parents to evaluate the severity of their own insomnia. The ISI has been validated as a measure to detect changes in perceived sleep difficulties in adults with insomnia (Bastien et al. 2001). The ISI contains five questions reflecting areas such as the severity of the insomnia problems and how they interfere with daily functioning. The Epworth Sleepiness Scale (ESS; Johns 1991) was used to evaluate the general level of daytime sleepiness in the parents. The ESS consists of eight questions representing typical daytime situations commonly found in daily life. It has been validated as a reliable method to distinguish normal individuals from those with a wide range of sleep disorders. The Parenting Stress Index Short Form (PSI-SF; Abiden 1995) was used to assess parenting stress. The PSI-SF measures the parental stress arising from factors inherent to the child, inherent to the parent and factors associated with parent–child interaction. It is widely used for measuring parental stress in autism spectrum disorders (Zaidman-Zait et al. 2010). The PSI-SF consists of 36 items that measure the key constructs of parental distress, parental–child dysfunctional interactions, and the extent the parent considers the child to be difficult and a total score. It also includes a scale that evaluates the extent the parent answers the questionnaire with a bias to present themselves in the most favourable manner and to minimise the problems or stress in the parent–child relationship (defensive responding).

Statistical analysis

Descriptive statistics were conducted on all major variables. Actigraphy data for parent and child were averaged across nights for each participant. Spearman rank correlations (rs) were used to evaluate associations between PSG sleep variables, actigraphy sleep variables and subjective sleep measures. Mann–Whitney U-tests were used to determine overall difference between parent and child on the sleep variables. 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 sas V9.2 software (Cary, NC, USA).

Results

A total of 16 parents consented to participate in the study. Questionnaires were completed on 15 (94%) participants, overnight PSGs were performed on 14 (88%) participants, and 10 (63%) participants completed a minimum of seven night’s in-home actigraphy. Seven (44%) participants had PSG and actigraphy data recorded on the same night, and actigraphy data were obtained from 13 (81%) parents. One parent withdrew from the study prior to the start of the PSG and another parent completed only the questionnaires, as she believed that the PSG and actigraphy would be problematic for her child to complete.

Children ranged in age from 2 to 16 years with a mean (standard deviation) of 6.5 (4.4) years. There were nine (60%) girls and six (40%) boys; 10 (67%) children were deletion-positive, three (20%) children had uniparental disomy, one child had an imprinting centre mutation and one child had an imprinting centre mosaic genotype (this child had only questionnaire data). All children were on at least one medication. The primary medications and number of participants using that medication were: melatonin (n = 8, 53%), clonazepam (n = 7, 47%), gastrointestinal medication (n = 7, 47%), topiramate (n = 3, 20%) and other medications (n = 9, 60%). All parents participating in the parental part of the study were mothers.

Sleep behaviours

Subjective sleep measures

Parents in this study all reported that their child had a sleep problem, and five (33%) parents reported some degree of co-sleeping with their child. Subjective measures of sleep are presented in Table 1. When compared to the normative sample published by Owens et al. (2000), children/adolescents with Angelman syndrome scored higher on all CSHQ sub-scales.

Table 1.

Children’s Sleep Habits Questionnaire (CSHQ) sub-scale scores in children/adolescents with Angelman syndrome compared to normative sample

CSHQ sub-scale Angelman syndrome (n = 15) Normative sample* (n = 469)
Bedtime resistance 8.2 (2.9) 7.1 (1.9)
Sleep onset latency 1.5 (0.8) 1.3 (0.5)
Sleep anxiety 6.0 (1.4) 4.9 (1.5)
Sleep duration 5.6 (1.6) 3.2 (0.9)
Night wakings 5.8 (1.6) 3.5 (0.9)
Parasomnias 10.4 (1.4) 8.1 (1.3)
Sleep-disordered breathing 4.4 (1.4) 3.2 (0.6)
Daytime sleepiness 11.4 (3.2) 9.6 (2.8)
Sleep total 49.0 (7.3) 41
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*

Normative sample from Owens et al. (2000).

Objective sleep measures

Table 2 presents the PSG and actigraphy results of the child and the actigraphy results of the parent. Wilcoxon signed-rank tests to evaluate differences between each sleep variable obtained by actigraphy on the night of the PSG and the average for all nights of in-home actigraphy showed no differences. There were also no differences found between the PSG sleep variables and the actigraphy-calculated sleep variables on the night of the PSG. No differences were found between parent and child sleep for average sleep latency, average total sleep time, standard deviation for time in bed and standard deviation of total sleep time. However, parent and child sleep differed for average time in bed, average wake after sleep onset, average sleep fragmentation, standard deviation for wake after sleep onset and the standard deviation for fragmented sleep.

Table 2.

Objective sleep measurements [mean (standard deviation)] of children/adolescents with Angelman syndrome and their parent

Sleep measurement/measure Sleep onset latency (min) Sleep duration (min) Night wakings WASO (min) Fragmentation (index) Time in bed (min)
Child – polysomnography 37.6 (50.3) 373.9 (132.8) 57.2 (91.5) 10.8 (14.4) 504.4 (107.0)
Child – actigraphy on polysomnography night 32.9 (33.1) 381.9 (100.5) 123.0 (85.0) 52.5 (21.2) 499.9 (149.5)
Child – in-home actigraphy 40.8 (23.3) 405.5 (54.8) 114.0 (32.5) 49.7 (6.1) 519.6 (63.5)
Parent – in-home actigraphy 31.7 (22.5) 379.5 (47.6) 63.8 (30.0) 35.0 (11.9) 443.4 (65.3)
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WASO, wake after sleep onset.

Associations between subjective and objective sleep measures

Table 3 presents the associations between the actigraphy-measured child and parent sleep parameters and the CSHQ domains. Actigraphy measures of night-time waking (wake after sleep onset) were highly associated between child in-home actigraphy and actigraphy on the PSG night (rs = 0.76), and child in-home actigraphy and the PSG (rs = 0.64). Additionally, a high association was found between the average amount of wake after sleep onset on in-home actigraphy and the actigraphy-measured time in bed on the night of the PSG (rs = 0.64).

Table 3.

Spearman rank correlations (rs) between sleep variables measured by actigraphy and parental reported sleep problems in children/adolescents with Angelman syndrome*

Children’s Sleep Habits Questionnaire sub-scales
Sleep anxiety Sleep delay Sleep duration Night wakenings Parasomnias
Child actigraphy – polysomnography night
 Sleep latency
 Wake after sleep onset −0.95 0.82
 Fragmentation index −0.76
 Time in bed −0.86
Child actigraphy – in home
 Sleep latency
 Fragmentation index 0.60
 Sleep duration 0.66 0.69
Parent actigraphy – in home
 Wake after sleep onset 0.59
 Fragmentation index 0.70
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*

Only values with rs > 0.50 and P < 0.001 are reported.

Associations between child’s and parental sleep and stress

To evaluate the association of the child’s sleep with the parent’s daytime sleepiness, insomnia and stress, we examined Spearman rank correlations (rs) between the average values obtained for the in-home actigraphy and the parent’s subjective questionnaires. The child’s average sleep latency was associated with a higher level of daytime sleepiness measured by the ESS (rs = 0.71) and more symptoms of insomnia as measured by the ISI (rs = 0.66). Total sleep time variability was associated with the following scales from the Parental Stress Index-SF: Defensive Responding (rs = 0.64), Parental Distress Scale (rs = 0.72), and the Total Score (rs = 0.61).

Discussion

Our study employed a multimodal approach to examine sleep in children with Angelman syndrome, and their primary caregiver, using subjective and objective measurements. Our results are consistent with previous research showing sleep problems in these children and highlighting the importance of understanding nocturnal awakenings and restless sleep. Furthermore, our findings showing disrupted night-time sleep of the parents in association with the parent’s report of problems with the child’s sleep duration suggest that the parents’ sleep quality is affected by the child/adolescents sleep.

We found an association between a longer sleep duration on in-home actigraphy and parent report of parasomnias on the CSHQ. We also saw an association of the parasomnia scale with measurements of disrupted night-time sleep, wake after sleep onset and the fragmented index. Parasomnias, movement problems, daytime somnolence and disordered breathing have also been reported in one survey (Bruni et al. 2004). The parasomnia scale on the CSHQ is broad, including the items bedwetting, talking and walking in sleep, waking screaming or sweating, and restless sleep/excessive movement. A high frequency of bruxism, enuresis, sleep terrors and sleepwalking, as well as restless sleep, has been reported in another questionnaire study in Angelman syndrome (Bruni et al. 2004). It is not surprising therefore that given the inclusion of the question related to restless sleep/excessive movement on the parasomnia scale, this scale was significant in our study. Furthermore, compared to Owens et al.’ normative sample of children (Owens et al. 2000), the parents of children in our study reported higher levels of parasomnias, sleep-disordered breathing and daytime sleepiness.

Night wakings were noted both subjectively by parental report and objectively with actigraphy and PSG. Wake after sleep onset measured by PSG averaged almost 1 h over all children and, when measured with actigraphy, both in the laboratory and at home, averaged almost 2 h. These findings, along with the high fragmentation index in both the sleep lab and at home, highlight the disturbed sleep in these individuals. These objective measurements support previous subjective reports of other researchers who have noted frequent night wakings, and sleep maintenance problems, to be severe and more prevalent than settling problems in children with Angelman syndrome (Didden et al. 2002). A prior case series of adults with Angelman syndrome using wrist actigraphy showed similar fragmented sleep to our children (Anderson et al. 2008). A high frequency of abnormal movements, including restless sleep, have previously been reported with the suggestion that these nocturnal movements might be part of the extrapyramidal symptoms of Angelman syndrome including tremors, myoclonus and dyskinesia (Bruni et al. 2004).

Our study is the first to our knowledge to look at the sleep patterns and parenting stress in parents of children with Angelman syndrome. Previous studies have shown that sleep problems in children with ID are related to family functioning (Richdale et al. 2000; Didden et al. 2002; Meltzer & Mindell 2007). High levels of disturbed sleep, such as wake after sleep onset and fragmented sleep, are often associated with increased stress and other medical problems in adults. Parents of children with developmental disabilities have been shown to experience higher levels of stress than parents of typically developing children (Doo & Wing 2006; Sung et al. 2008; Zaidman-Zait et al. 2010). While sleep is one possible source of parental stress, these causes are most likely multifactorial. Our study extends this finding to parents of children with Angelman syndrome. The association of child sleep, parent daytime sleepiness and insomnia found in this study suggests that in a caregiver population that is already stressed, attention to the caregiver’s sleep is important to minimise potential adverse effects.

Similar to other neurodevelopmental disorders, the aetiology of insomnia in Angelman syndrome is most likely multifactorial rather than due to one specific component. In Angelman syndrome, biological abnormalities in the circadian control of sleep are a plausible cause of insomnia. The possibility of disturbed melatonin metabolism has been suggested based on the response to melatonin treatment in small trials (Braam et al. 2008). Psychological factors, such as reliance on parents to promote sleep (Walz et al. 2005), or associating the bedroom with activities other than sleep, are also likely to be involved. Other causes or contributing factors to insomnia in Angelman syndrome may include primary sleep disorders such as nightmares (Walz et al. 2005) or epileptic seizures (Clayton-Smith 1993). Independent of epileptic seizures, sleep continuity and architecture may be disrupted by frequent interictal epileptiform activity or by abnormal high-amplitude rhythmic slow wave discharges that are characteristic findings in the waking electroencephalographies of Angelman syndrome patients (Dan & Boyd 2003).

High wake after sleep onset has previously been reported in children with Angelman syndrome. Using PSG, Miano et al. (2005) showed a higher percentage of wake after sleep onset, and a higher rate of awakenings per hour, in children with Angelman syndrome than children with ID, or epilepsy.

The strengths of our study include the use of a validated questionnaire, wrist actigraphy and PSG that measure both objective and subjective sleep. Limitations are a small sample size across a large age range where sleep patterns may differ. There was also incomplete data, which was due in part to parents’ concerns about their children’s abilities to tolerate PSG. Additionally, participants were part of the Angelman Natural History Study and may not be representative of the general Angelman population.

In summary, our study shows the presence of high nocturnal waking and arousals in children/adolescents with Angelman syndrome, as well as evidence suggesting high fragmentation and night-time wakings of parents of these children/adolescents that are potentially associated with the sleep of their child. Research to identify potential causes of these arousals, for example, seizures or interictal epileptiform activity, is warranted. Improvement in the child’s sleep not only will benefit the child’s health and well-being, but also offers promise for improving the sleep and daytime vigilance of the parents.

Acknowledgments

This research was supported in part by a Donna and Jay Richards – Hobbs Discovery Grant from the Vanderbilt Kennedy Center for Research on Human Development, Vanderbilt University Medical Center, as well as in part by Vanderbilt CTSA Grant 1 UL1 RR024975 from the National Center for Research Resources, National Institutes of Health.

Footnotes

Institution where work was performed: Vanderbilt University Medical Center.

References

  1. Abiden RR. Parenting Stress Index. 3. PAR Psychological Assessment Resources; Lutz, FL: 1995. [Google Scholar]
  2. Ancoli-Israel S, Cole R, Alessi C, Chambers M, Moorcroft W, Pollack CP. The role of actigraphy in the study of sleep and circadian rhythms. Sleep. 2003;26:342–71. doi: 10.1093/sleep/26.3.342. [DOI] [PubMed] [Google Scholar]
  3. Anderson B, Pilsworth S, Jamieson S, Ray J, Shneerson JM, Lennox GG. Sleep disturbance in adults with Angelman syndrome. Sleep and Biological Rhythms. 2008;6:95–101. [Google Scholar]
  4. Bastien CH, Vallieres A, Morin CM. Validation of the Insomnia Severity Index as an outcome measure for insomnia research. Sleep Medicine. 2001;2:297–307. doi: 10.1016/s1389-9457(00)00065-4. [DOI] [PubMed] [Google Scholar]
  5. Berry RJ, Leitner RP, Clarke AR, Einfeld SL. Behavioral aspects of Angelman syndrome: a case control study. American Journal of Medical Genetics. Part A. 2005;132A:8–12. doi: 10.1002/ajmg.a.30154. [DOI] [PubMed] [Google Scholar]
  6. Braam W, Didden R, Smits MG, Curfs LMG. Melatonin for chronic insomnia in Angelman syndrome: a randomized placebo-controlled trial. Journal of Child Neurology. 2008;23:649–54. doi: 10.1177/0883073808314153. [DOI] [PubMed] [Google Scholar]
  7. Bruni O, Ferri R, D’Agostino G, Miano S, Roccella M, Maurizio E. Sleep disturbances in Angelman syndrome: a questionnaire study. Brain and Development. 2004;26:233–40. doi: 10.1016/S0387-7604(03)00160-8. [DOI] [PubMed] [Google Scholar]
  8. Clayton-Smith J. Clinical research on Angelman syndrome in the United Kingdom: observations on 82 affected individuals. American Journal of Medical Genetics. 1993;46:12–15. doi: 10.1002/ajmg.1320460105. [DOI] [PubMed] [Google Scholar]
  9. Dahl RE, El-Sheikh M. Considering sleep in a family context: introduction to the special issue. Journal of Family Psychology. 2007;21:1–3. doi: 10.1037/0893-3200.21.1.1. [DOI] [PubMed] [Google Scholar]
  10. Dan B, Boyd SG. Angelman syndrome reviewed from a neurophysiological perspective. The UBE3A-GABRB3 hypothesis. Neuropediatrics. 2003;34:169–76. doi: 10.1055/s-2003-42213. [DOI] [PubMed] [Google Scholar]
  11. Didden R, Korzilius H, Aperlo B, Overloop C, Vries M. Sleep problems and daytime problem behaviours in children with intellectual disability. Journal of Intellectual Disability Research. 2002;46:537–47. doi: 10.1046/j.1365-2788.2002.00404.x. [DOI] [PubMed] [Google Scholar]
  12. Didden R, Korzilius H, Smits MG, Curfs LM. Sleep problems in individuals with Angelman syndrome. American Journal on Mental Retardation. 2004;109:275–84. doi: 10.1352/0895-8017(2004)109<275:SPIIWS>2.0.CO;2. [DOI] [PubMed] [Google Scholar]
  13. Doo S, Wing YK. Sleep problems of children with pervasive developmental disorders: correlation with parental stress. Developmental Medicine and Child Neurology. 2006;48:650–5. doi: 10.1017/S001216220600137X. [DOI] [PubMed] [Google Scholar]
  14. Goodlin-Jones BL, Sitnick SL, Tang K, Liu J, Anders TF. The Children’s Sleep Habits Questionnaire in toddlers and preschool children. Journal of Developmental and Behavioral Pediatrics. 2008;29:82–8. doi: 10.1097/dbp.0b013e318163c39a. [DOI] [PubMed] [Google Scholar]
  15. Iber C, Ancoi-Israel S, Chesson A, Quan S. AASM Manual for the Scoring of Sleep and Associated Events: Rules, Terminology and Technical Specification. AASM; Westchester, IL: 2007. [Google Scholar]
  16. Johns MW. A new method for measuring daytime sleepiness: the Epworth Sleepiness Scale. Sleep. 1991;14:540–5. doi: 10.1093/sleep/14.6.540. [DOI] [PubMed] [Google Scholar]
  17. Malow BA, Marzec ML, McGrew SG, Wang L, Stone W. Characterizing sleep in children with autism spectrum disorders: a multidimensional approach. Sleep. 2006;29:1563–71. doi: 10.1093/sleep/29.12.1563. [DOI] [PubMed] [Google Scholar]
  18. Meltzer LJ. Brief report: sleep in parents of children with autism spectrum disorders. Journal of Pediatric Psychology. 2008;33:380–91. doi: 10.1093/jpepsy/jsn005. [DOI] [PubMed] [Google Scholar]
  19. Meltzer LJ, Mindell JA. Relationship between child sleep disturbances and maternal sleep, mood, and parenting stress: a pilot study. Journal of Family Psychology. 2007;21:67–73. doi: 10.1037/0893-3200.21.1.67. [DOI] [PubMed] [Google Scholar]
  20. Meltzer LJ, Moore M. Sleep disruptions in parents of children and adolescents with chronic illnesses: prevalence, causes, and consequences. Journal of Pediatric Psychology. 2008;33:279–91. doi: 10.1093/jpepsy/jsm118. [DOI] [PubMed] [Google Scholar]
  21. Miano S, Bruni O, Leuzzi V, Elia M, Verrillo E, Ferri R. Sleep polygraphy in Angelman syndrome. Clinical Neurophysiology. 2004;115:938–45. doi: 10.1016/j.clinph.2003.11.004. [DOI] [PubMed] [Google Scholar]
  22. Miano S, Bruni O, Elia M, Musumeci SA, Verrillo E, Ferri R. Sleep breathing and periodic leg movement pattern in Angelman syndrome: a polysomnographic study. Clinical Neurophysiology. 2005;116:2685–92. doi: 10.1016/j.clinph.2005.08.005. [DOI] [PubMed] [Google Scholar]
  23. Morin CM. Insomnia: Psychological Assessment and Management. Guilford Press; New York: 1993. [Google Scholar]
  24. National Sleep Foundation. Final Report: 2004 Sleep in America Poll 2004 [Google Scholar]
  25. Owens JA, Spirito A, McGuinn M. The Children’s Sleep Habits Questionnaire (CSHQ): psychometric properties of a survey instrument for school-aged children. Sleep. 2000;23:1043–51. [PubMed] [Google Scholar]
  26. Pelc K, Cheron G, Boyd SG, Dan B. Are there distinctive sleep problems in Angelman syndrome? Sleep Medicine. 2008;9:434–41. doi: 10.1016/j.sleep.2007.07.001. [DOI] [PubMed] [Google Scholar]
  27. Polimeni MA, Richdale AL, Francis AJP. A survey of sleep problems in autism, Asperger’s disorder and typically developing children. Journal of Intellectual Disability Research. 2005;49:260–8. doi: 10.1111/j.1365-2788.2005.00642.x. [DOI] [PubMed] [Google Scholar]
  28. Richdale A, Frances A, Gavidia-Payne S, Cotton S. Stress, behaviour, and sleep problems in children with an intellectual disability. Journal of Intellectual & Developmental Disability. 2000;25:147–61. [Google Scholar]
  29. Robinson AM, Richdale AL. Sleep problems in children with an intellectual disability: parental perceptions of sleep problems, and views of treatment effectiveness. Child: Care, Health and Devolpment. 2004;30:139–50. doi: 10.1111/j.1365-2214.2004.00395.x. [DOI] [PubMed] [Google Scholar]
  30. Sadeh A, Acebo C. The role of actigraphy in sleep medicine. Sleep Medicine Reviews. 2002;6:113–24. doi: 10.1053/smrv.2001.0182. [DOI] [PubMed] [Google Scholar]
  31. Sung V, Hiscock H, Sciberras E, Efron D. Sleep problems in children with attention-deficit/hyperactivity disorder: prevalence and the effect on the child and family. Archives of Pediatrics and Adolescent Medicine. 2008;162:336–42. doi: 10.1001/archpedi.162.4.336. [DOI] [PubMed] [Google Scholar]
  32. Walz NC, Beebe D, Byars K. Sleep in individuals with Angelman syndrome: parent perceptions of patterns and problems. American Journal of Mental Retardation. 2005;110:243–52. doi: 10.1352/0895-8017(2005)110[243:SIIWAS]2.0.CO;2. [DOI] [PubMed] [Google Scholar]
  33. Williams CA. The behavioral phenotype of the Angelman syndrome. American Journal of Medical Genetics. Part C: Seminars in Medical Genetics. 2010;154C:432–7. doi: 10.1002/ajmg.c.30278. [DOI] [PubMed] [Google Scholar]
  34. Williams CA, Angelman H, Clayton-Smith J, Driscoll DJ, Hendrickson JE, Knoll JHM, et al. Angelman syndrome: consensus for diagnostic criteria. American Journal of Medical Genetics. 1995;56:237–8. doi: 10.1002/ajmg.1320560224. [DOI] [PubMed] [Google Scholar]
  35. Williams CA, Beaudet AL, Clayton-Smith J, Knoll JH, Kyllerman M, Laan LL, et al. Angelman syndrome 2005: updated consensus for diagnostic criteria. American Journal of Medical Genetics. Part A. 2006;140A:413–18. doi: 10.1002/ajmg.a.31074. [DOI] [PubMed] [Google Scholar]
  36. Zaidman-Zait A, Mirenda P, Zumbo BD, Wellington S, Dua V, Kalynchuk K. An item response theory analysis of the Parenting Stress Index-Short Form with parents of children with autism spectrum disorders. Journal of Child Psychology and Psychiatry, and Allied Disciplines. 2010;51:1269–77. doi: 10.1111/j.1469-7610.2010.02266.x. [DOI] [PubMed] [Google Scholar]
  37. Zhadanova IV, Wurtman RJ, Wagstaff J. Effects of a low dose of melatonin on sleep in children with Angelman syndrome. Journal of Pediatric Endocrinology & Metabolism. 1999;12:57–67. doi: 10.1515/jpem.1999.12.1.57. [DOI] [PubMed] [Google Scholar]

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