Sleep: An underemphasized aspect of health and development in neurorehabilitation

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Early Human Development journal homepage: www.elsevier.com/locate/earlhumdev

Sleep: An underemphasized aspect of health and development in neurorehabilitation A R T I C L E I N F O

A B S T R A C T

Keywords: Sleep Cerebral palsy Parents Neurorehabilitation Health Development

Sleep deficiency has unique causes and implications for children with neonatal brain injury; contributing to the development or exacerbation of neurodevelopmental impairments and yet it is an underemphasized aspect of health and development. There is very little research evidence to guide the management of sleep disorders in children with cerebral palsy, a common neurodevelopmental disability of childhood. This paper is a comprehensive review and analysis of the literature regarding what is known about sleep quantity and quality in children with cerebral palsy. The specific implications for children with cerebral palsy are explored including the adverse effects of sleep deficiency on general child development, physical health and growth, and mental functioning. The consequences for the family are also discussed. Finally, the assessment and management of sleep problems are summarized to provide guidance to clinicians who work in neurodevelopmental medicine.

1. Introduction Recent literature shows increasing recognition that sleep plays a critical role in child health and development [1]. More specifically, sleep plays an essential role in optimal general health, physical performance, and cognitive functioning of children with and without neurodevelopmental conditions [1,2]. Thus, sleep is emerging as an essential component of a triad of healthy behaviours, which also includes healthy diet and physical activity. Tremblay et al. [3] recently introduced the Canadian 24 h Movement guidelines [3] for children which, to our knowledge, are the first of its kind integrating recommendations for sleep in movement guidelines. Under the “whole day matters” philosophy, kids between the ages of five and 13 years old should sleep nine to 13 h each night, while eight to 10 h of sleep is recommended for youth aged 14- to 17-years [1]. Sleep deficiency is broadly defined as insufficient sleep or sleep patterns that interfere with physical and mental well-being. Sleep deficiency can result from inadequate amount (deprivation) or decreased quality of sleep. Chronic sleep loss and associated sleepiness and daytime impairments pose serious threats to childhood academic success and health, and are important public health issues [4]. For example, there is a growing body of research that suggests that sleep deficiency in childhood is associated with adverse outcomes including increased adiposity, challenges with emotional regulation, worse academic performance and decreased quality of life and well-being [1]. Understanding the implications of insufficient sleep during childhood is critical in developing promising strategies to optimize health and developmental outcomes. Sleep problems, such as bedtime resistance and night waking are common among all children during their first few years [5]. While the majority of children who are typically developing outgrow their sleep problems around school age, as many as 30% of preschool children continue to experience sleep deficiency and the same proportion of adolescents may not be getting the optimal amount or quality of sleep [1]. The prevalence of sleep disorders is much higher in children with neurodevelopmental disabilities, with a reported prevalence as high as 85% [2,6]. Therefore it is critical that clinicians who work with this population understand the unique causes and implications of sleep deficiency as well as the range of possible interventions to improve sleep. Sleep deficiency has unique causes and implications for infants who experienced neonatal brain injury and present with subsequent neurodevelopmental impairments. However, there has been little focus on sleep issues within this population. A review by Lelis et al. [7] included only 12 published papers on sleep in children with cerebral palsy (CP); three studies have been published since [8–10]. Increased awareness of the issues associated with sleep deficiency is needed to advance research and clinical practice regarding sleep assessment and management. Early recognition of sleep deficiency and use of strategies to ensure sufficient sleep can contribute to optimizing developmental potential and reducing the burden of sleep deprivation on the family. The goal of this article is to provide an overview of what is currently known about (1) the causes of sleep deficiency in children with CP; (2) the consequences of sleep deprivation on children with CP and their family; and (3) implications for clinicians in neurodevelopmental medicine.

http://dx.doi.org/10.1016/j.earlhumdev.2017.07.006

0378-3782/ © 2017 Elsevier B.V. All rights reserved.

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2. The causes of sleep deficiency in children with CP CP is a non-progressive injury to the developing brain in the pre-, peri or postnatal period that results in a movement or posture disorder leading to activity limitations [11]. With a prevalence varying from 2.0 to 3.6 cases per 1000 live births [12–14], CP is a common neurodevelopmental disability of childhood. Children with CP present with a range of motor abilities that can affect the ability of the child to perform motor tasks. In addition, many children have co-existing morbidities including seizure disorders, cognitive impairments, and vision and hearing impairments [11] that can also affect their abilities to perform daily functional activities. Infants and children at risk for or diagnosed with CP are often followed by specialized professional teams such as neonatal follow-up clinics, neurodevelopmental or rehabilitation clinics for children with CP. The early focus of parents and clinicians includes medical management as well as optimizing infant development. Participation in age appropriate activities is emphasized as children enter pre-school and school programs. Over the last decade, physical activity promotion and reduction of sedentary behaviour has become an important focus of rehabilitation programs, in an effort to enhance function and long-term health. In contrast, sleep in children with CP has only recently been recognized as an important part of the formula to promote long-term health, in line with “the whole day matters” philosophy in typically developing children [5,15]. There is evidence that children with CP are seven to twelve times more likely to experience sleep disorders, when compared to their peers [6]. Difficulties with all aspects of sleep have been reported in children with CP, which may be related to common co-morbid medical conditions [16–19]. Lelis et al. [7] performed a review of the literature specific to sleep and children with CP and identified eleven reported types of sleep disorders; 1) sleep hyperhidrosis; 2) disorders of arousal; 3) difficult morning awakening; 4) sleep disordered breathing; 5) bruxism; 6) insomnia; 7) nightmares; 8) parasomnias (e.g., sleepwalking); 9) difficulties in initiating and maintaining night time sleep (night waking); 10) sleep-wake transition disorders; and 11) sleep anxiety. These sleep disorders can be caused by a number of intrinsic factors related to various medical conditions that affect the following systems/aspects of health: 1) Neurological system; 2) Mental health (including behavioural disorders and co-morbidities such as autism spectrum disorder); 3) Ophthalmological; 4) Hearing; 5) Upper airway; 6) Pulmonary; 7) Gastrointestinal; and 8) Musculoskeletal system. Extrinsic factors such as socio-familial factors and clinical, surgical and pharmacological interventions may also have an adverse effect on sleep [7]. Common examples and consequences of these issues are presented in Table 1. Concerns about sleep of children and adolescents with CP have been reported to vary by age and gross motor function and often consist of multiple factors that impede sleep [20]. In a study of 154 children and adolescents, participants identified sleep routines, settling routines, daytime activities, and behaviour and sensory regulation as primary concerns. Concerns for children and adolescents with more significant motor involvement were mostly related to posture, movement control, breathing, reflux and digestion, and temperature and perspiration. Issues with settling routines were of more concern for children under six [20]. In summary, sleep issues are a common occurrence among children with CP. There is a range of factors (intrinsic and extrinsic) that contribute, often in combination, to the manifestation and persistence of sleep problems. 3. The consequences of sleep problems for children with CP and their families Sleep serves a crucial restorative and protective role. Effective sleep has been associated with immune and cardiovascular function and many essential growth and restorative processes such as muscle growth, tissue repair, release of growth hormone and synthesis of proteins [21]. Various theories regarding the role of sleep in human functioning have emphasized physical and psychological restoration, energy conservation, consolidation of memories, discharge of emotions, brain growth, and other basic biological functions including immune system maintenance [22]. Consequences of sleep deficiency for children who are typically developing include adverse physical and mental health outcomes, including negative consequences for academic performance and learning [23]. This section summarizes the most important findings in the literature in combination with clinical observations and the potential relevance to Table 1 Factors related to sleep in children with CP. Factors

Examples

Consequences related to sleep

Intrinsic Neurological Mental health

Epilepsy/nocturnal seizures Behavioural issues

Arousals and awakenings Failure to register daytime and night-time cues, irritability, oppositional behaviour, anxiety, low mood, over activity and poor attention span Circadian rhythm abnormalities resulting in delayed secretion of nocturnal melatonin Frightened, disoriented Breathing disorders, upper airway obstruction, mixed sleep apnoea, recurrent aspiration pneumonia Breathing disorders and possible sleep apnoea Breathing disorders leading to arousals and wakes Arousals and wakes

Ophthalmological

Blindness/visual impairment

Hearing Upper airway

Hearing impairment Abnormal airway muscle tone

Pulmonary Gastrointestinal Musculoskeletal

Pulmonary aspiration Gastro-oesophageal reflux Muscle spasms or other forms of musculoskeletal pain, decreased ability to change body position

Extrinsic Socio-familial variables Clinical surgical and pharmacological interventions

Bed-sharinga Use of devices (orthosis, night worn splints, postural equipment), medication, major surgery (e.g. scoliosis, corrective hip surgery).

Sleep disorders, disorders of arousal Pain, discomfort, side effects of medication (decreased rapid eye movement in REM sleep, abnormal body movements according to the stage of sleep)

a The relationship between sleep deficiency and co-sleeping is complex as parents will often sleep with their child to ensure necessary medical care is provided during the night. Therefore it is important to consider that parents choose co-sleeping arrangements because their children have difficulty maintaining sleep and not to assume that co-sleeping is a cause of sleep issues [8].

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children with CP and their parents including the adverse effects of sleep deficiency on general child development, physical health and growth, and mental functioning including behaviour, learning, memory, and mood [24]. 3.1. Effects of sleep deficiency on child health and development 3.1.1. General health Sleep deficiency has been linked to increased frequency of illnesses such as flu, cold, gastroenteritis and other infectious diseases in adolescents who are typically developing [25]. Poor sleep may contribute to sub-optimal immune system performance including compromised T cell function [21]. The combination of pre-existing conditions in children with CP, such as decreased pulmonary function and decreased immune function due to sleep deficiency could potentially result in increased susceptibility to common respiratory illnesses. Furthermore, children with more significant motor impairments may be at increased risk for recurrent respiratory illness due to decreased lung function [26,27]. In addition to increasing risk of common infectious diseases, poor sleep has been associated with increased vulnerability to diseases of inflammatory origin in the longer term such as cardiovascular disease and diabetes [25]. Since increased incidence of both cardiovascular disease and diabetes have been reported in adults with CP [28], it is important to understand all of the potential contributing factors, including the role of sleep, in maintaining optimal health. 3.1.2. Physical health and growth A systematic review of research evidence [1] suggests that shorter sleep duration is associated with higher adiposity indicators in typically developing children [29]. Although it has not been specifically evaluated, it is reasonable to assume that this relationship also exists for children with CP. Individuals with CP have higher levels of self-reported fatigue, which in turn is associated with increased adiposity (i.e. Body Mass Index (BMI) and waist circumference) [30]. Although research on the topic is lacking, clinically, it can be observed that sleep deprivation in adolescents with CP may lead to increased fatigue levels in the day time resulting in difficulties with coping with physical and mental demands, which in turn may lead to impaired sleep due to anxiety and increased stress levels. Hence, it is possible that children with CP may be at risk for a negative spiral of fatigue, anxiety and sleep deficiency. The effects of sleep deficiency on mental health in children with CP require further evaluation. Children with CP grow more slowly than children without chronic health conditions [31], with differences in growth increasing with increasing age [32]. In addition, children who have difficulty walking or do not walk, grow more slowly than children with CP who walk independently [33]. Presumably this relationship can be explained by decreased growth stimulating forces through bone, however the production of growth hormone also stimulates skeletal growth [34]. The secretion of growth hormone is closely linked to the sleep-waking cycle and is highest during the first 90 min of night time sleep [35]. Theoretically, sleep deficiency, and subsequent decreased secretion of growth hormone could potentially lead to decreased lean muscle mass, muscle strength, bone density, and possibly physical functioning as it does in other groups of children [36]. While it is likely that decreased growth in children with CP who are non-ambulatory is related to decreased weight bearing [37], sleep disorders could potentially be another contributing factor to impaired growth in children with CP. This topic warrants further investigation. 3.1.3. Mental functioning Thirty to 50% of children with CP have a diagnosis intellectual disability [38]. In addition, many children with bilateral motor involvement primarily in the legs (diplegic CP) or unilateral involvement (hemiplegic CP) can have less obvious but noteworthy cognitive impairments. Children with unilateral CP may exhibit deficits across all four domains of executive function (i.e., higher level thinking required to apply strategies and manage attention) – attentional control, cognitive flexibility, goal setting, and information processing [39,40]. Since executive function is crucial for performance in many daily activities, it is important to consider how sleep deficiency in children with CP can exacerbate pre-existing cognitive impairments, daily functioning and pre-existing difficulties with school performance [23]. For example, sleep loss has a negative impact on attention [41] and erodes executive function, particularly on tasks requiring learning and flexible thinking [42]. There is increasing awareness that many school-aged children, adolescents and young adults with CP face challenges to mental health, which may present as depression and anxiety [43]. Of note, in a health service utilization study among young adults with CP in Canada, mental illness was the third most common reason for hospital admission [44]. One can hypothesize that chronic stress may contribute to altered brain maturation that affects physical and mental health and overall well-being [45]. Chronic stress may negatively impact sleep quantity and quality, which, in turn, might make it difficult for children and youth to regulate emotions, and keep their attention during tasks in daily life [46]. Research is needed to investigate trajectories of children with CP combined with new frontier research on brain development, sleep deprivation and chronic stress responses. 3.2. Effects of sleep deficiency of the child on the family In addition to the ‘direct’ effects of sleep disorders as described above, we must also consider the consequences of a child's disturbed sleep in a broader context. Childhood sleep issues have direct implications for families because sleep patterns of other family members (e.g. parents or siblings) are also often disturbed when a child experiences sleep deficiency [6,47–49] One study that reported a high rate of sleep issues in children with CP, also confirmed that many (40%) of their mothers also experienced poor sleep quality [48] and that poor maternal sleep quality was associated with maternal depression. Parents of children with neurodevelopmental disabilities may experience increased stress as a result of increased caregiving demands [50]. In addition to the effects of chronic stress on sleep quality, parents may also experience sleep deficiency because of the need to provide care for their child at night. For example epileptic seizures, position changes required because of lack of mobility, and special care requirements such as tube feeding may require attention in the middle of the night. Children who experience pain may also wake in the night, requiring the attention of a parent. A recent study showed that nearly 40% of children with CP required parental attention on at least once a night [48]. In this study, 74% of parents reported that their own daytime functioning was impaired as a result of their child's sleep disorder [48]. Parents may change their sleeping habits to accommodate increased night-time caregiving. For example, co-sleeping, or bed or bedroom sharing with family members has been reported significantly higher for parents of children with motor disabilities, mainly CP, (11.8%) compared to children with other disabilities or

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medical conditions (7.9%) and is associated with decreased parent sleep quality [8]. Age, house crowding, severe visual impairment and pathological sleep were found to be the main factors associated with co-sleeping. The majority of parents reported the need for special care of the child at night, mainly to care for a child who has epilepsy [8]. In summary, frequent night-time monitoring and care needs of a child with CP can have detrimental impact on parents' sleep quality and quantity. Child sleep disturbance can affect parental sleep, and is associated with increased parental daytime sleepiness, stress, depression, fatigue, and impairment of health and social functioning [49,51]. Decreased wellbeing, and other health issues have also been noted in mothers of children with CP [48]. Consideration of the family system context suggests that a child's sleep problems need to be recognized as a broader concern because of the potential physical and emotional toll on the family. 4. Clinical implications Sleep is an underemphasized area of paediatric clinical practice and health care professionals may not be adequately prepared to use evidencebased information to support parent decision-making regarding their child's sleep [52]. In addition, there is very little research evidence to guide the management of sleep disorders in this population. In this section, we will review what is currently known about sleep assessment and intervention and implications for clinicians in neurodevelopmental medicine. 4.1. Increased awareness of sleep issues Since successful management of chronic sleep disruption may decrease family stress and improve child functioning and development, it is important to consider the implications for health care professionals who work with children and youth with neurodevelopmental disabilities. Despite the emphasis in the literature on physical activity over the past ten years, recommendations for physical activity are only beginning to be applied by healthcare practitioners [53]. Therefore, it may take several years for sleep assessment and management strategies to be addressed as part of routine clinical practice [53]. Delays in addressing sleep problems in children with CP in clinical settings are compounded by the fact that sleep issues in this population are under-reported and under recognized. This gap is worrisome, since a survey of Canadian parents published in 2012 reveals that “sleep issues” rank fourth among areas of concern by parents of children with CP under the age of six [54]. Likewise, almost 96% of parents consider sleep issues to be a somewhat or very important topic of discussion [54]. Therefore, sleep should be a standard item for review at routine follow-up in paediatric care. Asking questions such as ‘Does your child have any problems falling or staying asleep?’ and ‘Do the sleep disturbances of your child impact your own sleep or health?’ is a good start to identifying difficulties [55]. If families self-identify issues regarding either sleep quantity or quality, further assessment is warranted. 4.2. Assessment of sleep problems in CP The first step in assessing a child with CP with a sleep problem must be clinical based on a comprehensive medical history and physical examination. The medical history should include questions about history of current or previous medical issues and sleep habits. Implementation of an assessment tool within a routine follow-up or monitoring clinic is a good first option for clinicians interested in sleep duration and schedule and sleep related behaviours and interactions. A variety of methods for assessment of sleep problems are available to clinicians. Fig. 1 provides an

Fig. 1. Sleep assessment methods.

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overview of the most common assessment methods ranked based on usability and the degree of subjectivity/objectivity [56]. Subjective and objective measures are discussed in the following paragraphs. 4.2.1. Subjective measurement of sleep Three questionnaires that have been used with children with CP and their parents are 1) the Sleep Disturbance Scale for Children, a validated parent report questionnaire for children ages 3 to 18 years; [57] 2) the Children's Sleep Habits Questionnaire (CSHQ), a brief validated questionnaire for parents designed to assess sleep of children ages 4 to 10 years with disabilities [58] and, 3) the “BEARS”, another simple clinical screening survey that focuses on Bedtime resistance, Excessive daytime sleepiness, Awakenings during the night, Regularity, and Snoring [59]. Parents may struggle to provide an accurate history, as they may witness only portions of night time events. Therefore, while parent report questionnaires are limited by parents' inability to monitor their child throughout the night, they may be a good option for an initial assessment of potential sleep issues. Sleep logs (sleep-wake diaries) provide another option for parents as they can document information on bedtime, frequency and duration of night-time awakenings, nap frequency and duration, time of morning waking, and total sleep time. A minimum of 2 weeks of data collection, including weekends is recommended to reflect an accurate picture of the sleep issues. When interpreting these self (or parent)-report tools, it is important to recognize that sleep duration is typically overestimated compared with more objective measures [60]. For example, time in bed does not necessarily reflect actual sleep duration as the child may experience difficulty falling asleep or awake during the night when the parent is unaware. Therefore, questionnaires or logs are likely an effective first line strategy for assessment. Children who may have serious sleep problems that are not resolved by basic strategies or who are suspected of having sleep apnoea require objective sleep assessments. Particularly when the focus of the investigation is on sleep quality or sleep architecture, the need for more sophisticated methods increases because of the serious limitations of the subjective parental reports [56]. In summary, the advantages of questionnaires, diaries and daily logs are the fact that they are easy to use, inexpensive and can measure a wide range of sleep parameters in various contexts. These tools are typically readily available since that do not require special equipment or technological knowledge. A limitation of these measures is that information is influenced by response bias, compliance and response burden. 4.2.2. Objective measurement of sleep Polysomnography is considered the gold standard of sleep assessment. It is based on laboratory monitoring that usually includes electrical brain activity (EEG), muscle activation (EMG), eye movements (EOG), breathing efforts and oxygen saturation sensors (oximetry). It can be performed in ambulatory (outpatient) or clinical settings where it can be combined with (supervised) video monitoring. Advantages are its ability to provide detailed information on sleep architecture and clinical differential diagnoses. It can sometimes be mandatory to definitively diagnose a certain sleep disorder, for example in the case of sleep apnoea. However, it may be of limited value in cases of insomnia disorder or circadian rhythm disorders. In addition, the setting (i.e., wires, sleep lab) may create challenges with producing representative sleep. This method is costly and labour intensive, and may not be available in some locations. In addition to polysomnography, sleep propensity can be assessed with a multiple sleep latency test (MSLT). This method consists of a series of naps at two hour intervals under strictly standardized conditions. It is recommended to combine this test with a sleep diary and/or actigraphy one week prior to the MSLT. Actigraphy is a cost-effective way to assess sleep wake patterns for extended periods of time in the child's natural environment [56]. It is a wristwatch-like device that continuously detects and stores data on movement. Some devices also record data on light. Data are downloaded and computer algorithms are used to estimate time in- and out of bed, total sleep and wake times and sleep efficiency. Estimate is made based on the amount of movement of the device since there is usually little or no movement during sleep. Clinical guidelines and research suggest that wrist actigraphy is useful when assessing sleep patterns, in the evaluation of circadian rhythm sleep disorders, insomnia and sometimes as an adjunct to home monitoring of sleep-disordered breathing. Actigraphy has been well validated for the estimation of night-time sleep parameters in paediatric populations [60]. It is much cheaper, less obtrusive and usually better tolerated than polysomnography. In addition to validated measurements of sleep, the widespread availability of home video cameras and smartphones can increase the opportunity for physicians to observe and assess episodes of abnormal movement or behaviour during sleep from videos captured at home. Videosomnography is based on video recordings of sleep that can be done in the natural sleep environment. One or more video cameras in the child's room make it possible to record and later to identify sleep-wake patterns. These patterns include parental interventions and the child's behaviour during night-time waking episodes [61]. In addition, portable home sleep monitoring devices are currently underway that, at least in typically developing subjects, yield equivalent results to manual scoring of polysomnography on evaluating sleep architecture and continuity [62]. Circadian rhythm can be objectified using melatonin measurements, most often performed in saliva. It can be used to detect abnormal melatonin production or circadian rhythm disorders, especially in adolescents with sleep onset problems or blindness. In most cases the dim light melatonin onset can be estimated sufficiently based on sleep logs or actigraphy [63], but when treatment is unsuccessful or there are doubts about the correct diagnosis (for example if sleep onset problems are caused by delayed sleep phase syndrome, cognitive overactivation of behavioural problems) it can direct further treatment. In summary, when assessing sleep it is important to realize that evaluation of sleep problems requires a thorough history of the child's 24-hour routine (with a focus on bedtime habits, night-time behaviour, naps, and daytime behaviour). Sleep assessment through one or a combination of subjective and objective measures can inform the following dimensions: (a) duration, (b) quality, (c) brain activity patterns—or sleep architecture, and (d) schedule or circadian aspects (consistency (i.e., day-to-day variability), and continuity (i.e., variability in sleep duration within the same night)) [56]. 5. Management of sleep problems The previous paragraphs illustrate the need for an integrative approach in evaluating and treating sleep problems and disorders in children with CP and their families. Unfortunately, there is limited data available on therapeutic approaches in children with neurodevelopmental disorders such as CP [64]. As a consequence this section of the manuscript is based primarily on clinical experience with other patient groups and expert opinion. Once the cause of the sleep disorder is identified it is important to treat comorbid conditions that contribute to the cause of the sleep disorder,

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primary sleep disorders and behaviours and circumstances that contribute to sleep problems. 5.1. Management of comorbid conditions The clinician may consider targeted (pharmaco)therapy for the treatment of the comorbid conditions identified in association with sleep disturbances, such as physical problems (pain, spasticity, gastro-oesophageal reflux) as well as mental health issues that may interfere with sleep (e.g., depression, anxiety, ADHD). For instance, if pain disturbs sleep, analgesics can be used to reduce pain and discomfort during the night. Oral medication such as a low dose of oral baclofen at night time might be considered for the reduction of discomfort associated with spasticity. There is some evidence that injections with botulinum toxin serotype A not only reduces spasticity and accompanying pain but also seems to be associated with improved sleep quality in children with CP [10]. Nocturnal seizures can diminish total sleep time, reduce sleep quality and alter circadian rhythms and therefore effective seizure management may also be an important consideration for effective sleep. 5.2. Management of ‘primary’ sleep disorders As discussed throughout the manuscript, children with CP also have a higher prevalence of certain ‘primary’ sleep disorders. Particular worth mentioning are sleep-related breathing disorders (SBD). Children with (suspected) SBD benefit from referrals to respiratory (sleep) specialists, increased physical activity (if obesity is an issue), reduction of environmental allergens and potentially continuous positive airway pressure [65]. 5.3. Management of sleep onset problems due to circadian rhythm disorders Circadian rhythm disorders are common in the general population, especially in adolescents of whom 3% suffer from delayed sleep phase syndrome [66]. This percentage increases in children with ADHD or autism spectrum disorders [67]. Once a circadian rhythm disorder is identified, chronotherapy supported by bright light therapy and occasionally timed administration of melatonin may be effective for resolving sleeping issues [68]. In addition, it is advisable to and avoid blue-spectrum light in the evening [69] for its melatonin suppressing effects and due to the fact that use of mobile devices is thought to increase arousal due to increased cognitive demands. 5.4. Management of chronic insomnia – behavioural strategies It is possible that insomnia may persist following the treatment of co-morbidities or primary sleep disorders, warranting specific behavioural management strategies. Behavioural strategies to improve sleep and daily functioning have not been studied in children with CP specifically, but have shown to be effective in otherwise healthy children, children with ADHD [70]. In addition, there have been promising results of these strategies in children with autism spectrum disorder or intellectual disabilities [71,72]. Behavioural strategies often include the following components: education about normal sleep, sleep hygiene, parent-child interaction, extinction strategies and cognitive behavioural therapy. Sleep hygiene is defined as a set of sleep-related behaviours that expose persons to activities and cues that prepare them for and promote appropriately timed and effective sleep [73]. These sleep promotion practices and habits may be grouped into 4 categories: [46] (1) environmental (e.g., temperature, noise level, ambient light); (2) scheduling (e.g., regular bed- and wake times including weekends and vacations); (3) sleep practices (e.g., bedtime routine); and (4) physiologic (e.g., regular exercise, and timing of meals). It is important to realize that this sleep promoting behaviour starts during the day and includes ensuring that children are getting enough (morning) daylight, avoidance of caffeinated beverages, particularly later in the day, and opportunities to unwind before going to bed. It seems to be of utmost importance that children, particularly children with ADHD, autism spectrum disorder or sensory processing disorders, find an appropriate balance between mental/physical exercise and relaxation. This approach promotes sensory integration, prevents hyperarousal and hyperexcitability and therefore promotes sleep. Bedtimes need to be adjusted to the estimated sleep need [74]. In this respect it is important to realize that sleep need is dependent on age, not on the level of cognitive functioning, something that, in our experience, is often not realized by parents and physicians. For example a 10 year-old child has a sleep duration of 9–10 h, which means that a bedtime of 9 pm is appropriate even if the child functions at the level of a baby/toddler. Parent – child interaction plays an important role in childhood insomnia and even more so in children with a history of medical problems. For example anxiety regarding epilepsy at night increases the interference of parents at night, whereas frequent hospital stays may hamper the development of self-initiated settling methods (i.e. learning how to sleep by themselves). In young children with behavioural insomnia of childhood, a behavioural approach with extinction methods is commonly advised. These methods are described in more detail elsewhere [75]. It is thought that adolescents with insomnia may benefit from cognitive behavioural therapy [76], but studies in adolescents with CP are lacking. 5.5. Pharmacotherapy for insomnia As a last resort, pharmacological treatment for insomnia can have beneficial effects. Unfortunately, the research evidence is sparse and inconclusive. Melatonin is increasingly prescribed to many children with CP and other neurodevelopmental disorders, and has demonstrated efficacy in improving sleep, by reducing sleep-onset latency or slightly increasing total sleep time, especially in those with sleep onset problems [77]. Other medications include melatonin receptor agonists, gabapentin, tricyclic anti-depressants, atypical anti psychotics hypnotics and clonidine [64]. Finally, it is important to realize that certain medications can contribute to maintaining sleep disorders (e.g. hypnotics causing SBD of Lamotrigine causing insomnia).

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6. Conclusion An increasing body of research documents the negative impact of sleep loss on child health and development across a range of domains (physical, cognitive, emotional). While the literature on sleep patterns in children with CP and the impact of insufficient sleep on performance are lacking, there is a robust body of evidence documenting global performance impairments and negative health effects associated with a lack of sleep. Sleep deficiency can directly affect general health, physical performance, and cognitive functioning across the lifespan. Increasing awareness of the presence and the broad range of consequences of inadequate sleep in every child with CP is critical in the care for this population. Clinicians therefore must prioritise the management of sleep problems in children with CP with the potential to improve the well-being and development of the child, and the well-being of their (main) carers. Key guidelines

• The prevalence of sleep disorders in children with CP is much higher than in typically developing children. • Sleep deficiency can affects the well-being of the entire family. • Recognizing and treating sleep disorders in children with CP could potentially improve clinical outcomes and quality of life. Further research in this area is needed.

Research directions

• There are various studies that have investigated sleep and related outcomes; however no interventions/trials were specifically designed to improve sleep in children with CP. In particular there is a lack of research evaluating the effects on parents. • Patient oriented, inductive research should be used to identify strategies to improve sleep in children with CP and their families. • A care pathway regarding sleep co-created by parents and clinicians would provide a valuable tool for clinicians who work with children with developmental disabilities.

Funding Dr. Jan Willem Gorter holds the Scotiabank Chair in Child Health Research. Dr. Pritchard-Wiart is supported by the Canadian Child Health Clinician Scientist Training Program (CCHCSP), the Women and Children's Health Research Institute through the generous support of the Stollery Children's Hospital Foundation and Alberta PolicyWise for Children and Families. Conflict of interest None. Acknowledgements The authors wish to acknowledge the work of Dr. A. Pijpers and S. Pillen from Kempenhaeghe (Centre for sleep Medicine, Heeze, The Netherlands) for their valuable contributions to this manuscript. References [1] J.P. Chaput, C.E. Gray, V.J. Poitras, V. Carson, R. Gruber, T. Olds, et al., Systematic review of the relationships between sleep duration and health indicators in school-aged children and youth, Appl. Physiol. Nutr. Metab. 41 (2016) S266–S282. [2] C.J. Newman, M. O'Regan, O. Hensey, Sleep disorders in children with cerebral palsy, Dev. Med. Child Neurol. 48 (2006) 564–568. [3] M.S. Tremblay, V. Carson, J.P. Chaput, S. Connor Gorber, T. Dinh, M. Duggan, et al., Canadian 24-hour movement guidelines for children and youth: an integration of physical activity, sedentary behaviour, and sleep, Appl. Physiol. Nutr. Metab. 41 (2016) S311–S327. [4] J. Owens, Adolescent Sleep Working G, Committee on A, Insufficient sleep in adolescents and young adults: an update on causes and consequences, Pediatrics 134 (2014) e921–e932. [5] I. Michaud, J.P. Chaput, Are Canadian children and adolescents sleep deprived? Public Health 141 (2016) 126–129. [6] E. Simard-Tremblay, E. Constantin, R. Gruber, R.T. Brouillette, M. Shevell, Sleep in children with cerebral palsy: a review, J. Child Neurol. 26 (2011) 1303–1310. [7] A.L. Lelis, M.V. Cardoso, W.A. Hall, Sleep disorders in children with cerebral palsy: an integrative review, Sleep Med. Rev. 30 (2015) 63–71. [8] D. Jacquier, C.J. Newman, Co-sleeping in school-aged children with a motor disability: a comparative population-based study, Dev. Med. Child Neurol. (2016). [9] J. Garcia, B. Wical, W. Wical, L. Schaffer, T. Wical, H. Wendorf, et al., Obstructive sleep apnea in children with cerebral palsy and epilepsy, Dev. Med. Child Neurol. 58 (2016) 1057–1062. [10] V. Binay Safer, S. Ozbudak Demir, E. Ozkan, Guneri F. Demircioglu, Effects of botulinum toxin serotype a on sleep problems in children with cerebral palsy and on mothers sleep quality and depression, Neurosciences (Riyadh) 21 (2016) 331–337. [11] P. Rosenbaum, N. Paneth, A. Leviton, M. Goldstein, M. Bax, D. Damiano, et al., A report: the definition and classification of cerebral palsy April 2006, Dev. Med. Child Neurol. 109 (2007) 8–14. [12] S.M. Reid, J.B. Carlin, D.S. Reddihough, Rates of cerebral palsy in victoria, australia, 1970 to 2004: has there been a change? Dev. Med. Child Neurol. 53 (2011) 907–912. [13] Braun K. Van Naarden, N. Doernberg, L. Schieve, D. Christensen, A. Goodman, M. Yeargin-Allsopp, Birth prevalence of cerebral palsy: a population-based study, Pediatrics 137 (2016). [14] M. Yeargin-Allsopp, Braun K. Van Naarden, N.S. Doernberg, R.E. Benedict, R.S. Kirby, M.S. Durkin, Prevalence of cerebral palsy in 8-year-old children in three areas of the United States in 2002: a multisite collaboration, Pediatrics 121 (2008) 547–554. [15] O. Verschuren, P. McPhee, P. Rosenbaum, J.W. Gorter, The formula for health and well-being in individuals with cerebral palsy: physical activity, sleep, and nutrition, Dev. Med. Child Neurol. 58 (2016) 989–990. [16] H. Hemmingsson, A.M. Stenhammar, K. Paulsson, Sleep problems and the need for parental night-time attention in children with physical disabilities, Child Care Health Dev. 35 (2009) 89–95. [17] R.W. Atmawidjaja, S.W. Wong, W.W. Yang, L.C. Ong, Sleep disturbances in malaysian children with cerebral palsy, Dev. Med. Child Neurol. 56 (2014) 681–685. [18] D.E. Sandella, L.M. O'Brien, L.K. Shank, S.A. Warschausky, Sleep and quality of life in children with cerebral palsy, Sleep Med. 12 (2011) 252–256.

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Olaf Verschuren⁎ Brain Center Rudolf Magnus, Center of Excellence for Rehabilitation Medicine, University Medical Center Utrecht, Rembrandtkade 10, 3583TM Utrecht, The Netherlands Jan Willem Gorter1 CanChild Centre for Childhood Disability Research, Department of Pediatrics, McMaster University, Hamilton L8S 1C7, Canada Lesley Pritchard-Wiart Department of Physical Therapy, Faculty of Rehabilitation Medicine, University of Alberta, Edmonton, AB, Canada Glenrose Rehabilitation Hospital, Edmonton, AB, Canada E-mail address: [email protected]

⁎

1

Corresponding author.

Dr. Jan Willem Gorter holds the Scotiabank Chair in Child Health Research.

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