Sleep disorders in children with cerebral palsy

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1 Sleep disorders in children with cerebral palsy Christopher J Newman* MD, Central Remedial Clinic; Myra O Regan MSc PhD, Department of Statistics, Trinity College; Owen Hensey MD, Central Remedial Clinic, Dublin, Ireland. *Correspondence to first author at Central Remedial Clinic, Vernon Avenue, Clontarf, Dublin 3, Ireland. Christopher.Newman@chuv.ch To determine the frequency and predictors of sleep disorders in children with cerebral palsy (CP) we analyzed the responses of 173 parents who had completed the Sleep Disturbance Scale for Children. The study population included 100 males (57.8%) and 73 females (42.2%; mean age 8y 10mo [SD 1y 11mo]; range 6y 11y 11mo). Eighty-three children (48.0%) had spastic diplegia, 59 (34.1%) congenital hemiplegia, 18 (10.4%) spastic quadriplegia, and 13 (7.5%) dystonic/dyskinetic CP. Seventy-three children (42.2%) were in Gross Motor Function Classification System Level I, 33 (19.1%) in Level II, 30 (17.3%) in Level III, 23 (13.3%) in Level IV, and 14 (8.1%) in Level V. Thirty children (17.3%) had epilepsy. A total sleep problem score and six factors indicative of the most common areas of sleep disorder in childhood were obtained. Of the children in our study, 23% had a pathological total sleep score, in comparison with 5% of children in the general population. Difficulty in initiating and maintaining sleep, sleep wake transition, and sleep breathing disorders were the most frequently identified problems. Active epilepsy was associated with the presence of a sleep disorder (odds ratio [OR]=17.1, 95% confidence interval [CI] ), as was being the child of a single-parent family (OR=3.9, 95% CI ). Disorders of initiation and maintenance of sleep were more frequent in children with spastic quadriplegia (OR=12.9, 95% CI ), those with dyskinetic CP (OR=20.6, 95% CI ), and those with severe visual impairment (OR=12.5, 95% CI ). Both medical and environmental factors seem to contribute to the increased frequency of chronic sleep disorders in children with CP. On the basis of clinical experience it seems that children with cerebral palsy (CP) are liable to suffer from sleep disturbance; however, there is a lack of research and objective data to support this observation. Sleep may be vulnerable to several factors that are common in CP. Muscle spasms, other forms of musculo-skeletal pain, and the decreased ability to change body position during the night may all contribute to sleep difficulties and are related to the primary motor impairment. Epilepsy, which is frequently associated with CP, 1 is known to disturb sleep physiology and is likely to predispose to sleep disorders, 2 and several antiepileptic drugs can cause daytime sleepiness. Blindness or severe visual impairment, which may coexist with CP, can affect the timing and maintenance of sleep through their effect on melatonin secretion and the lack of light perception. 3 Glossoptosis and recurrent aspiration pneumonia related to gastro-oesophageal reflux are common in children with more severe total body involvement and can induce sleep-related breathing disturbances. Primary alterations in sleep architecture, possibly related to brainstem dysfunction, have also been reported in certain patients with athetoid CP. 4 Finally, it is most likely that the behavioural and psychological problems, as well as the familial and social stressors to which these children are exposed, have an effect on their sleep; however, this has not been investigated in any detail. So far the literature on sleep disorders in CP has been limited to case series of children or adults with severe spastic and dyskinetic CP. 4,5 No information is available about the prevalence of sleep disturbances throughout the whole spectrum of this condition. Our aim was to determine the frequency of sleep disorders in children with CP and to identify factors associated with these problems by analyzing parents responses to a validated sleep disturbance questionnaire. Materials and methods PARTICIPANTS The Central Remedial Clinic (Dublin, Ireland) physiotherapy department s clinical database was searched for all children aged 6 to 12 years who had a diagnosis of CP and a documented Gross Motor Function Classification System (GMFCS) 6 level. Clinical diagnoses based on the predominant type of motor impairment (spastic diplegia, congenital hemiplegia, spastic quadriplegia, dystonic/dyskinetic CP) had previously been established and recorded by an in-house medical consultant (paediatrician or paediatric neurologist) and s had been recorded by the children s in-house physical therapists. The Centre s physical therapists individually received a patient list 1 month before the beginning of the study to update s. There were 249 eligible children. Questionnaires were posted to their parents with a cover letter from the principal investigators describing the study design and requesting their cooperation. After 4 weeks, non-responders received a phone reminder from the first investigator. A total of 173 questionnaires were returned (response rate 69.5%). Parents signed consent for data use. The study was approved by the Central Remedial Clinic s institutional review board. DATA COLLECTION The parents completed the Sleep Disturbance Scale for Children. 7 This scale was originally validated on a sample of 1157 healthy children from the general population, from whom standardized norms were available. It investigates the 564 Developmental Medicine & Child Neurology 2006, 48:

2 occurrence of sleep disorders during the previous 6 months. The scale contains 26 items rated on a Likert-type scale, e.g. How many hours sleep does your child get on most nights? (1 indicates 9 11h, 2 indicates 8 9h, 3 indicates 7 8h, 4 indicates 5 7h, and 5 indicates <5h) and The child startles or jerks parts of the body while falling asleep (1, never; 2, occasionally [once or twice or less/mo]; 3, sometimes [once to twice/wk]; 4, often [three to five times/wk]; 5, always [daily]). The sum of scores provided a total sleep score and the original factor analysis yielded six sleep disturbance factors representing the most common areas of sleep disorders in childhood and adolescence: (1) disorders of sleep-related breathing; (2) disorders of initiating and maintaining sleep; (3) disorders of arousal (sleepwalking, sleep terrors, nightmares); (4) disorders of sleep wake transition (hypnic jerks, rhythmic movement disorders, hypnagogic hallucinations, nocturnal hyperkinesias, bruxism); (5) excessive somnolence; and (6) sleep hyperhydrosis (excessive sweating during sleep). This scale was selected because of its thorough validation, its good level of internal consistency and test retest reliability, the availability of normal data, and the overlap of the normative age group (6y 6mo 15y 4mo) with that assessed in the present study; furthermore, age and sex showed no significant effect on total sleep scores in the normal population. The scale was completed with items regarding the parents marital status and current parental employment. Questions about medication use, the presence of epilepsy, whether this was controlled or active (0 vs 1 or more seizures during the previous month), and severe visual impairment or blindness were also included. After peer discussion we inserted two further items possibly associated with sleep disorders: bedsharing with parent(s) and the use of positioning devices (i.e. night splints or sleeping systems). Information about the type of CP (spastic diplegia, congenital hemiplegia, spastic quadriplegia, dystonic/dyskinetic CP) and (I V in order of increasing severity of motor impairment) was retrieved from our clinical database. STATISTICAL ANALYSIS General characteristics of the study population were analyzed by frequencies and cross-tabulations. The total sleep score and each sleep disturbance factor score were converted into a binary variable based on normative data: 7 a T-score of more than 70 (>95th centile) was regarded as pathological, and a score of 70 or less was taken as the normal range. Frequencies of pathological scores were established for total sleep problems and individual sleep disturbance factors. Univariate analyses of associations between a pathological total sleep score, physical parameters (CP type,, epilepsy, severe visual impairment, use of postural equipment at least 3 nights/wk) and socio-familial parameters (sex, age, parents marital status, parental unemployment [of both parents in a two-parent family or of the single parent], and bed-sharing) were performed, and crude odds ratios (OR) with their 95% confidence intervals (CI) were computed. These parameters were then entered in a single step as independent variables into an unconditional binary logistic regression. Dum- my variables were created for categorical parameters. The same independent variables were used to perform multivariable analyses for each sleep disorder factor (except sleep hyperhydrosis, whose prevalence approached that of the normative sample). Variables that showed no contribution to all of the sleep factors (p>0.20) were excluded from this model. Overall model evaluation was performed with omnibus tests of model coefficients. Each model was assessed for goodness of fit with the Hosmer and Lemeshow χ 2 statistic (p<0.10 indicating a lack of fit). Analyses were performed with SPSS (version 12.0) p 0.05 was considered significant. Results GENERAL CHARACTERISTICS The study population consisted of 100 males (57.8%) and 73 females (42.2%) with a mean age of 8 years 10 months (SD 1y 11mo; range 6y 6mo 15y 4mo). There were 31 children of oneparent families (17.9%), and unemployment was reported in 12 families (6.9%). Data about CP types and s are summarized in Table I. Thirty children (17.3%) were reported to have epilepsy and were all receiving antiepileptic medication. Twenty of them had had no recent seizure (11.6%) and 10 had experienced at least one seizure during the preceding month (5.8%). Epilepsy affected 7/83 (8.4%) children with diplegia, 9/59 of those with hemiplegia (15.3%), 9/18 who had spastic quadriplegia (50%), and 5/13 children with dyskinetic CP (38.5%). Ten children were reported to be blind or severely visually impaired (5.8%). Fifty-one families reported using night postural equipment with their children (29.5%). This was used every night for 28 children (16.2%), three to five nights per week for 10 children (5.8%), and two nights or less per week in 13 children (7.5%). Bed-sharing occurred at least once a week in 39 families (22.5%). It was reported to take place every night in 16 families (9.2%), three to five nights per week in 12 families (6.9%), and one to two nights per week in 11 families (6.4%). SLEEP DISTURBANCE SCALE FOR CHILDREN RESULTS Thirty-nine children (22.5%) had a pathological total sleep score. Forty-two children had difficulty in initiating and maintaining sleep (24.3%), 31 had sleep wake transition disorders Table I: Baseline medical data with number of cerebral palsy (CP) types and Gross Motor Function Classification System (GMFCS) levels Diagnosis Diplegia, n Hemiplegia, n Quadriplegia, n Dyskinetic CP, n Total, n (%) I (42.2) II (19.1) III (17.3) IV (13.3) V (8.1) Total, n (%) 83 (48.0) 59 (34.1) 18 (10.4) 13 (7.5) 173 Sleep Disorders in Cerebral Palsy Christopher J Newman et al. 565

3 (17.9%), 25 experienced sleep-related breathing disorders (14.5%), 19 had excessive somnolence (11.0%), 14 had disorders of arousal (8.1%), and 10 were reported to have sleep hyperhydrosis (5.8%). Ninety-seven children had none of these sleep disorders (56.1%), 36 children presented one sleep disorder (20.8%), 24 had two sleep disorders (13.9%), 11 had three sleep disorders (6.4%), and five children had between four and six sleep disorders (2.9%). On multivariable analysis a pathological total sleep score (Table II) was significantly associated with the presence of active epilepsy (OR=17.1, 95% CI ; p=0.004) as well as with being the child of a single-parent family (OR=3.9, 95% CI ; p=0.014), and sleeping with parents (OR=6.3, 95% CI ; p<0.001). For the sleep factor analysis (Table III) the variables age, parental unemployment, and postural equipment were excluded from the final model because these had no significant contribution to any of the factors. The overall model evaluation suggested that for sleep breathing disorders all of the variables were unrelated to the outcome (data not shown). Disorders of initiation and maintenance of sleep were associated with diagnoses of spastic quadriplegia (OR=12.9, 95% CI ; p=0.009), dyskinetic CP (OR=20.6, 95% CI ; p=0.002), and severe visual impairment (OR=12.5, 95% CI ; p=0.002), as well as with bed-sharing (OR=4.8; 95% CI ; p=0.001). Sleep wake transition disorders were less frequent in Table II: Univariable and multivariable analyses of variables associated with a pathological total sleep disorder score Characteristic n Total sleep disorder Crude OR Corrected OR (95% CI) (95% CI) Age, y Baseline Baseline ( ) 0.9 ( ) ( ) 0.7 ( ) Sex, M/F 100/ ( ) 0.6 ( ) Parental status Single ( ) 3.9 ( ) Unemployed ( ) 1.1 ( ) CP type Diplegia 83 Baseline Baseline Hemiplegia ( ) 1.0 ( ) Quadriplegia ( ) 2.5 ( ) Dyskinetic ( ) 2.9 ( ) I 73 Baseline Baseline II ( ) 1.1 ( ) III ( ) 0.7 ( ) IV ( ) 0.4 ( ) V ( ) 0.6 ( ) Severe visual loss ( ) 3.9 ( ) Epilepsy None 143 Baseline Baseline Controlled ( ) 1.0 ( ) Active ( ) 17.1 ( ) Postural equipment ( ) 1.8 ( ) Bed-sharing ( ) 6.3 ( ) Significant results (p 0.05) are indicated in bold type. OR, odds ratio; CI, confidence interval; CP, cerebral palsy; GMFCS, Gross Motor Function Classification System. 6 females (OR=0.3, 95% CI ; p=0.013) and more frequent with bed-sharing (OR=6.9, 95% CI ; p<0.001). Disorders of excessive somnolence were associated with active epilepsy (OR=10.1, 95% CI ; p=0.008). Disorders of arousal occurred less in females (OR=0.1, 95% CI ; p=0.015) and more in children of single parents (OR=5.3, 95% CI ; p=0.021). Each of these models achieved satisfactory goodness of fit with the Hosmer Lemeshow χ 2 statistic (degrees of freedom=8; total sleep score χ 2 =8.06, p=0.43; disorders of initiation and maintenance of sleep χ 2 =4.84, p=0.77; sleep wake transition disorders χ 2 =3.57, p=0.89; disorders of excessive somnolence χ 2 =8.28, p=0.40; disorders of arousal χ 2 =4.02, p=0.86). Discussion Children with CP experience a high frequency of sleep problems compared with those with no chronic health condition. Estimations of the prevalence of sleep disorders in schoolchildren from the general population vary widely from 10% to more than 40% in different epidemiological studies This is probably due to the absence of consensus on what threshold constitutes clinical sleep pathology. In our study 44% of the children presented at least one clinically significant sleep disorder. On the normative Sleep Disturbance Scale for Children a pathological total sleep score is defined to affect 5% of children in a normal population. 7,11 This total sleep score reflects the overall quality of sleep, for which the 95th centile threshold is likely to identify children who have clinically significant sleep disruption requiring intervention and exceeding more benign sleep disturbances that are commonplace in childhood. The children in our group presented a more than fourfold prevalence of these total sleep disorders at 22.5%. Similarly, specific disorders of initiation and maintenance of sleep, of sleep wake transition, of sleep breathing, of excessive daytime somnolence, and of arousal were all elevated in our population of children with CP. The principal factor associated with a total sleep disturbance in our study was the presence of active epilepsy, which was also associated with excessive daytime somnolence. However, in epileptic children who were seizure-free there was no increase in total sleep problems nor in any of the individual sleep disorders. Similarly, Cortesi et al. 12 reported that in children with idiopathic epilepsy, those with ongoing seizures presented more sleep problems than those who were seizure-free. Potential interactions between sleep problems and epilepsy are multiple and complex. Children with epilepsy are likely to be predisposed to clinical sleep disorders for a variety of reasons; 2 conversely, sleep loss or disturbance may lead to an increase in the frequency of seizures. 13 We could not infer whether our participants presented either one or a combination of both of these phenomena. Another factor that tends to be implicated in the sleep disorders of children with epilepsy is the use of antiepileptic medication, especially that causing daytime sleepiness. 14 In our study the seizure-free epileptic children, who were all receiving antiepileptic treatment, had no increase in excessive diurnal somnolence. Daytime drowsiness was much more strongly associated with persistent seizures than with antiepileptic drugs, either as a result of the disruptive effect of seizures on sleep physiology or as an expression of post-ictal effects. A similar observation was reported by Lindblom et al. 15 in 293 children and adults 566 Developmental Medicine & Child Neurology 2006, 48:

4 with learning disability* living in a rehabilitation centre. In their multivariable analysis active epilepsy was found to be a strong independent predictor of increased daytime sleep, whereas neither neuroleptic nor sleep-provoking medication was associated with this problem. This illustrates the difficulty of weighing the effects of inadequate seizure control against possible side effects of medication when patients present with excessive daytime sleepiness, and the importance of systematically enquiring about sleep loss or disruption in such cases. Disorders of initiation and maintenance of sleep were strongly associated with certain physical factors. Children with total body involvement (spastic quadriplegia and dystonic/dyskinetic CP) were significantly more affected. Several reasons may be invoked such as the increased occurrence of pain or involuntary movements in these children. Yet the degree of functional motor impairment recorded on the GMFCS was not associated with an increase in sleeplessness. An alternative possibility is that children with total body involvement may be more prone to disorders of initiation and maintenance of sleep as a result of increased behavioural, psychological, and adaptive difficulties. The coexistence of intellectual impairment was not investigated in our study because of the difficulty of ascertaining this by mail survey. However, cognitive difficulties frequently affect children with total body involvement CP and are highly associated with sleep problems, especially sleeplessness. 16,17 It may also be that factors primarily related to the localization and extent of cerebral damage in these cases, such as the brainstem dysfunction described in children with dyskinetic CP by Hayashi et al., 4 may affect the architecture of sleep. The second physical factor that was strongly associated with disorders of initiation and maintenance of sleep was the presence of severe visual impairment or blindness. The increased prevalence of sleeplessness in blind children is well recognized *North American usage: mental retardation. and has been reported in several studies It is believed to be caused primarily by a lack of light perception, although behavioural factors may also underlie some of these sleep wake cycle disorders, and some of these children do seem to respond to strict daytime and night-time routines. 21 We observed that females were less affected by sleep wake transition disorders and disorders of arousal than males. Most previous studies in normal populations have shown little significant effect of sex on sleep disorders. 8,22 Laberge et al. 23 found that sleep talking was more common in males and that leg restlessness was more frequent in females; in the validation study of the Sleep Disturbance Scale for Children, females were prone to daytime somnolence. There is no clear explanation for the sex predisposition to certain types of sleep disorder that we observed in our study, and further investigation is warranted to confirm these findings. Environmental factors were also associated with an increase in certain sleep disorders. Children of single parents were more likely to have a total sleep disorder and to suffer from disorders of arousal. It is possible that the psychological effects of parental separation may induce events such as sleep terrors or nightmares, accounting for the increase in disorders of arousal. Parental unemployment was also associated with a pathological total sleep disorder score in the univariate analysis; however, this had no significant effect when correcting for other variables. External stressors have been shown to affect the quality of sleep in normal children. Lozoff et al. 24 described that factors such as an accident or illness in the family, unaccustomed absence of the mother during the day, or maternal depressed mood led to an increase in sleep problems. We also found that bed-sharing was associated with an increase in total sleep disorders, disorders of initiation and maintenance of sleep, and sleep wake transition disorders. Several studies have reported an increase in sleep problems associated with the practice of bed-sharing However, this clear association Table III: Multivariable analysis of variables associated with pathological sleep disorder factors Characteristic n DIMS SWTD DES DOA OR (95% CI) OR (95% CI) OR (95% CI) OR (95% CI) Sex, M/F 100/ ( ) 0.3 ( ) 0.7 ( ) 0.1 ( ) Single parent ( ) 2.3 ( ) 3.3 ( ) 5.3 ( ) CP type Diplegia 83 Baseline Hemiplegia ( ) 1.3 ( ) 0.9 ( ) 0.4 ( ) Quadriplegia ( ) 0.5 ( ) 4.9 ( ) 12.9 ( ) Dyskinesia ( ) 0.7 ( ) 5.5 ( ) 0 I 73 Baseline II ( ) 1.7 ( ) 0.6 ( ) 0.1 ( ) III ( ) 0.5 ( ) 0.3 ( ) 0.2 ( ) IV ( ) 4.7 ( ) 0.3 ( ) 0.2 ( ) V ( ) 0.5 ( ) 0.5 ( ) 0 Severe visual loss ( ) 0.5 ( ) 3.1 ( ) 0 Epilepsy None 143 Baseline Controlled ( ) 1.0 ( ) 0.2 ( ) 0 Active ( ) 0.7 ( ) 10.1 ( ) 0.6 ( ) Bed-sharing ( ) 6.9 ( ) 3.3 ( ) 1.0 ( ) Significant results (p 0.05) are indicated in bold type. DIMS, disorders of initiation and maintenance of sleep; SWTD, disorders of sleep wake transition; DES, disorders of excessive somnolence; DOA, disorders of arousal; OR, odds ratio; CI, confidence interval; CP, cerebral palsy; GMFCS, Gross Motor Function Classification System. 6 Sleep Disorders in Cerebral Palsy Christopher J Newman et al. 567

5 between several sleep problems and bed-sharing does not shed light on relations of cause and effect. Sleep problems may be the reason for parents to sleep alongside their child but the process of bed-sharing can also encourage certain sleep disorders. Parents who share a bed with their child are also ideally placed to observe a number of sleep-related events (such as night awakenings, hypnic jerks, and nocturnal hyperkinesias) that would otherwise remain unnoticed. The use of night positioning equipment did not seem to affect quality of sleep. This is a frequent preoccupation of carers, and reports of settling or sleeping difficulties related to the use of night-time splints are encountered in clinical practice. The non-appearance of these difficulties in our analysis probably occurred because when children s sleep is affected by this equipment its use is usually abandoned. There are potential limitations to consider in the interpretation of our results. A degree of non-response bias is possible despite a satisfactory response rate approaching 70%. However, when comparing for known parameters such as age, sex, type of CP, and s there was no significant difference between responders and non-responders. The accuracy of parental reporting may also be questioned. However, faced with a large sample this was the only readily available source of information. In addition, parental reports of sleep disturbance and objective measurement of sleep have been shown to agree. 29,30 Conclusion We believe that sleep should be systematically addressed in all children with CP. We have shown that they have a high likelihood of presenting chronic sleep disorders and that these are associated with both physical factors (active epilepsy, total body involvement, severe visual impairment) and environmental factors (single-parent household, bed-sharing). Further research is necessary to identify the precise aetiological pathways that lead to sleep disruption and to investigate the consequences of sleep disorders on these children s physical and psychological health as well as on their family s quality of life. Similarly, the optimal management of these disorders in children with CP remains to be determined with precision, be it through behavioural intervention, pharmacological treatment, or a combination of these approaches. DOI: /S Accepted for publication 28th October Acknowledgements During this work the first author was supported by grants from the Swiss National Science Foundation, CEREBRAL (Swiss Foundation for Children with Cerebral Palsy), and the Swiss Paraplegics Foundation. References 1. Wallace SJ. (2001) Epilepsy in cerebral palsy. Dev Med Child Neurol 43: Stores G. (2001) Sleep patterns in the epilepsies. In: Stores G, Wiggs L, editors. 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