Sleep and dreaming in children and adolescents with epilepsy

Schlaf und Träumen bei Kindern und Jugendlichen mit Epilepsie

Abstract

Background

Sleep problems are frequent in children and adolescents with epilepsy. The consequences of these problems, such as sleep deprivation and fatigue, can trigger epileptic seizures.

Objective

The purpose of this review was to scrutinize the effects of sleep and sleep disorders such as insomnia and parasomnias on epilepsy in childhood and adolescence.

Methods

Current databases were scoured for possible combinations of sleep and epilepsy in childhood and adolescence.

Results

The 24 studies included in this review showed that the most common sleep problems are disordered breathing, nightly awakenings, and excessive daytime sleepiness. A higher rate of parasomnias, shorter sleep duration, reduced sleep efficiency, and sleep-related anxieties were found more often in epileptic children. Furthermore, sleep problems are associated with the level of seizure control. However, no studies have investigated either the dreams or the chronotype of children and adolescents with epilepsy. Most of the studies used questionnaires, whereas few studies used polysomnography or actigraphy. Sometimes parents’ reports were implemented. The age range of the children and adolescents was 1.5 to 18.0 years.

Conclusion

The results of the current review underline the fact that sleep problems are not uncommon in children and adolescents with epilepsy. In spite of this, there is more research needed to scrutinize the connection between sleep and epilepsy, for example to work out factors influencing the sleep of epileptic children and adolescents.

Zusammenfassung

Hintergrund

Schlafprobleme finden sich häufig bei Kindern und Jugendlichen mit Epilepsie. Die Auswirkungen dieser Schlafprobleme, wie Schlafdeprivation oder auch Müdigkeit, können zur Auslösung epileptischer Anfälle führen.

Ziel

Das Ziel dieser Übersichtsarbeit war zu untersuchen, auf welche Weise Schlaf und Schlafstörungen, wie Insomnie und Parasomnien, Epilepsie im Kindes- und Jugendalter beeinflussen können.

Methoden

Gängige Suchmaschinen wurden nach möglichen Kombinationen zu Schlaf und Epilepsie im Kindes- und Jugendalter durchsucht.

Ergebnisse

Die 24 in die vorliegende Übersicht einbezogenen Studien zeigen, dass die verbreitetsten Schlafprobleme Atemstörungen, nächtliches Erwachen und exzessive Tagesschläfrigkeit sind. Eine höhere Rate an Parasomnien, kürzere Schlafdauer, reduzierte Schlafeffizienz und schlafbezogene Ängste fanden sich ebenfalls häufiger bei epileptischen Kindern. Zudem hängen Schlafprobleme mit dem Grad der Anfallskontrolle zusammen. Jedoch fanden sich weder Studien zu Träumen noch zum Chronotyp bei Kindern und Jugendlichen mit Epilepsie. Die meisten in den Studien verwendeten Erhebungsinstrumente waren Fragebögen, wenige Studien inkludierten Polysomnographie oder Aktigraphie. Manchmal wurde auch auf eine Fremdbeurteilung durch die Eltern zurückgegriffen. Der Altersbereich der Kinder und Jugendlichen lag zwischen 1,5 und 18,0 Jahren.

Schlussfolgerungen

Es ist bestätigt, dass Schlafprobleme bei Kindern und Jugendlichen mit Epilepsie nicht ungewöhnlich sind. Trotzdem sollte in zukünftigen Studien der Zusammenhang von Schlaf und Epilepsie genauer untersucht werden, beispielsweise durch Ermittlung von Faktoren, die den Schlaf bei epileptischen Kindern und Jugendlichen beeinflussen.

Epilepsy is a chronic disease characterized by continuous and recurrent epileptic seizures, and which involves neurobiological, cognitive, psychological, and social disturbances [16]. The International League Against Epilepsy (ILAE) states that an epileptic seizure is “a transient occurrence of signs and/or symptoms due to abnormal excessive or synchronous neuronal activity in the brain. The term transient is used as demarcated in time, with a clear start and finish” [40]. For an epilepsy diagnosis, one of three conditions has been complied with: 1) the person had at least two unprovoked seizures occurring less than 24 h apart or 2) one unprovoked seizure and a probability of further seizures or 3) an epilepsy syndrome is diagnosed [17]. The ILAE classifies epileptic seizures into self-limited seizure types, continuous seizure types, and further into focal seizures and generalized seizures [14]. Focal seizures begin within networks limited to one hemisphere. The ictal onset does not change across the seizures; each seizure type has a consistent site of onset. Generalized seizures, however, have inconsistent onsets from one seizure to another. They show beginnings at one point and then rapidly engage both hemispheres [7]. During a seizure, patients suffer from various symptoms such as impairment of awareness, aberrations of mental functioning, falls, sensory or motor phenomena, or convulsive movements [36]. Furthermore, epilepsy is a common neurological disease. In the United States, it is the fourth most common neurological problem [23]. Lifetime prevalence rates of epileptic seizures are 2–5 % [6]. The prevalence of active epilepsy in children and adolescents in Europe ranges from 3.2 to 5.1 % [18]. The incidence rate is high in childhood, as about 50 % of epilepsies begin either in childhood or retirement age [6].

Sleep and childhood epilepsy

Various studies have shown that epilepsy and sleep are correlated. Bazil (2003) reported that epileptic patients often suffer from insufficient sleep, inadequate sleep hygiene, coexisting sleep disorders, and circadian rhythm disturbances. The seizures themselves or the use of antiepileptic drugs (AEDs) can affect sleep [3]. Children suffering from epilepsy also often show changes in sleep architecture, with less rapid eye movement (REM) sleep and more stage 2 sleep than healthy controls [10]. Excessive daytime sleepiness, unrestful sleep, and more night awakenings are also frequent sleep-related problems in children with epilepsy [2, 3, 25, 30]. Furthermore, short sleep duration, poor quality of sleep, and anxieties are reported in the context of epilepsy [39]. Models concerning development and chronification of sleep problems report multifactorial risk factors and associations [25]. When epilepsy patients are asked about seizure provocation, sleep deprivation is the second most frequently mentioned factor, surpassed only by stress [15]. Vice versa, treatment of sleep problems in epileptic children could reduce their seizure frequency [31]. In addition, previous studies showed that sleep problems associated with epilepsy are related to a higher incidence of behavioral problems [19].

Childhood epilepsy and obstructive sleep apnea

Obstructive sleep apnea (OSA) was also a frequently observed phenomenon in children and adolescents suffering from epilepsy. In addition, this is associated with the severity of epilepsy and medication with AEDs [5, 26].

Childhood epilepsy and parasomnias

Besides sleep duration, low sleep hygiene, and insomnia symptoms, parasomnias such as nightmares could also be the cause of nightly awakenings and therefore result in insufficient sleep [32]. Various studies found that parasomnias occur more often in epileptic children [25, 28]. The American Psychiatric Association (APA) defines a nightmare as a dream which includes fear, anxiety, or other dysphoric emotions waking a person up directly and shifting rapidly into a state of full alertness. This leads to wakefulness and difficulty returning to sleep [1]. In adults with epilepsy, nightmares generally appear more often and are also related to seizure frequency [24]. Therefore, nightmares should also be taken into account when studying sleep problems in childhood epilepsy.

The purpose of this review was to scrutinize which sleep problems occur in children and adolescents with epilepsy and examine how sleep disorders such as insomnia and parasomnias might affect epilepsy.

Methods

For the systematic research, the four databases Psyindex, Psychinfo, Medline, and Google Scholar were used. The strategy searched for articles referring to sleep and sleep disorders in children and adolescents with epilepsy. The keywords used to find the articles were “epilepsy and child” paired with “chronotype”, “sleepiness”, “parasomnias”, “sleep”, “sleep disorder”, “nightmares”, and “dreaming”. The approach to including and excluding articles is shown in Fig. 1. The primary search with the keywords revealed 213,300 articles. After screening of title and abstract and exclusion of duplicates, 39 articles remained. All those unrelated to sleep and epilepsy in childhood were excluded. In a next step, the articles were analyzed for relevance and quality. A condition for inclusion was that the population was children and/or adolescents, and single-case studies and reviews were excluded. There was no time limit for the publication date. Finally, 24 studies were included in the review.

Fig. 1
figure1

Review process

Results

Overall, nine of the 24 studies were conducted in the USA, three in Brazil, and three in the UK. One study each was performed in India, Hungary, Egypt, China, Canada, Italy, the Netherlands, France, Turkey, and Malaysia. The age range of the children in the studies was 1.5 to 18.0 years. In 15 studies only questionnaires were used, 13 parental report and two parental plus self-report. Five studies collected their data with polysomnography, one of them in addition to parental and self-report, and one in addition to polygraphy. One study used actigraphy in addition to parental report and one the multiple sleep latency test in addition to self-report and polysomnography. One study used video-electroencephalography (EEG). The sample sizes of children with epilepsy varied from eleven to 331 children. Regarding design, 18 studies were cross sectional, 19 were controlled trails and included healthy controls, one study controlled with children suffering from OSA, and four studies did not have a control group. Dropouts were documented in seven studies.

Characteristics and results of the included studies are given in Table 1. The most common sleep problems of children and adolescents with epilepsy were night awakenings, excessive daytime sleepiness, and disordered breathing.

Table 1 Findings of studies investigating the relationship of sleep and epilepsy in children

Six studies registered shorter sleep duration of children and adolescents suffering from epilepsy. Eleven studies found more excessive daytime sleepiness and ten studies found insomnia symptoms such as more awakenings after sleep onset in children with epilepsy than in the control children. The same applied to OSA symptoms, with a higher presence of sleep-disordered breathing difficulties. Seven studies found a higher rate of parasomnias such as sleep talking or walking, nightmares, night terrors, teeth grinding, and head banging. Reduced sleep efficiency and sleep-related anxieties were also more common in epileptic children compared to healthy controls. The results are summarized in Fig. 2.

Fig. 2
figure2

Frequency of sleep-related findings

Fig. 3
figure3

Sleep and epilepsy in childhood and adolescence. Sleep-related anxieties and disorders in children and adolescents suffering from epilepsy (CAESAR). Strong associations are marked with bold arrows

In the following analysis the studies were clustered into three groups: studies based on questionnaires, those based on polygraphy/polysomnography (objective data), and those based on polysomnography and questionnaires. Based on this classification, 15 studies were part of the first group, five of the second, and three of the third.

Studies based on questionnaires

Stores and colleagues [39] collected data on sleep and behavior in children suffering from epilepsy of different types with a mean age of 10.12 years (standard deviation, SD = 3.06 years) and 73 control children (mean age = 10.37 years, SD = 3.04 years) by implementing a parental questionnaire. Six of an overall total of 79 children with epilepsy had absences, 33 had other generalized epilepsies, 31 partial, and nine uncertain epilepsies. These authors used a sleep questionnaire of Simonds and Parraga [38] based on five sleep-related categories: poor-quality sleep, anxieties about sleep, disturbances during sleep, sleep-disordered breathing symptoms, and short sleep duration. Children with epilepsy had significantly more sleep problems and impairments on all sleep categories except sleep disturbances compared to controls. Furthermore, positive correlations of short sleep duration with anxiety, parasomnias with psychosomatic symptoms, and poor-quality sleep with inattention were found. In addition, in children with epilepsy, sleep-related anxiety was significantly affected by seizure frequency and age. This indicates that older children and children with better-controlled seizures had fewer sleep-related anxieties, while the five abovementioned sleep scores were not affected by gender, age, type of seizures, seizure frequency, or treatment. Excessive daytime sleepiness was also found more frequently in epileptic children, whereas no difference was found concerning parasomnias such as sleep talking or walking, nightmares, night terrors, teeth grinding, and head banging. In contrast to Stores and colleagues, the study of Cortesi and colleagues found a higher rate of awakenings after sleep onset, excessive daytime sleepiness, and also parasomnias such as sweating and twitching during sleep, sleep walking and talking, teeth grinding, and bedwetting [12]. In this study, 89 children with idiopathic epilepsy, 63 with primary generalized, and 26 with primary partial epilepsy, all on a valproic acid AED therapy, were compared to 48 siblings and 321 controls. All groups were aged 6–14 years with a mean age of 9.7 years in the epilepsy group, 9.2 years among the siblings, and 9.6 years in the healthy control group. Sleep was evaluated by the Sleep Behavior Questionnaire (SBQ). A known sleep disturbance led to exclusion. In line with Stores and colleagues, Cortesi et al. also found more sleep problems in epileptic children than in siblings and controls. They interpreted a higher score on the SBQ as more existing sleep problems. Another study compared the results of the Pediatric Sleep Questionnaire (PSQ) of epileptic children with results of children suffering from OSA. No differences were found concerning snoring, excessive daytime sleepiness, and unrestful sleep [4]. A further six studies implemented a parental questionnaire; Maganti and colleagues additionally used a self-report [30]. Two studies found a higher rate of excessive daytime sleepiness and parasomnias in the epileptic group aged 6–14 and 4–16 years, both were using the SBQ and the Child Behavior Checklist (CBCL) [8, 42]. The study of Byars and colleagues included the largest sample with 349 children suffering from epilepsy aged 6–14 years (mean = 9.6 years, SD = 2.5 years) and 226 sibling controls (mean age 9.6 years, SD = 2.4 years). Most of the epileptic children in this study had either generalized tonic–clonic seizures (23 %), complex partial (26 %), or partial with secondary generalization seizures (29 %) [8]. The study of Maganti and colleagues used a self-report questionnaire, the Pediatric Daytime Sleepiness Scale (PDSS); and a parental questionnaire, the PSQ concerning sleep. More excessive daytime sleepiness (75.8 vs. 15 %), sleep-disordered breathing (65 vs. 3.9 %), and parasomnias (53 vs. 4 %) were reported in parental reports of epileptic children, as was more disordered breathing. Children with epilepsy also experienced more daytime sleepiness as measured by the PDSS [29, 30]. In general, 40 parents of children with epilepsy reported worse sleep habits of their children (mean age 4.1 years, SD = 1.5 years) on the Sleep Habits Inventory for Preschool Children and the SBQ than the 40 parents of healthy controls, and these sleep problems were associated with seizure control [2]. The same study found more sleep-related anxieties and awakenings after sleep onset in children with epilepsy, and worse sleep habits in children on polytherapy (25 %) than in those on monotherapy (75 %). Nonrefractory epilepsy was suffered by 24 children and 16 had refractory epilepsy [2]. Ong et al. [34], using the Sleep Disturbance Scale for Children (SDSC), also detected a higher mean score of night wakings (15.0 vs. 11.0) and rather than sleep-related anxieties, more sleep-disordered breathing symptoms (4.3 vs. 3.6) in 92 children with epilepsy (mean age = 11.1 years) than in healthy siblings. Predominantly nocturnal seizures were experienced by 18 % of the epileptic children. A Chinese study found various symptoms such as sleep-related anxieties, night wakings, disordered breathing, and, in addition, excessive daytime sleepiness and parasomnias significantly more often in 63 children with epilepsy (mean age = 8.35 years, SD = 2.5 years) than in 169 controls (mean age = 7.7 years, SD = 2.4 years) using the Children’s Sleep Habits Questionnaire (CSHQ). Additionally, the authors controlled for medication which could influence the sleep architecture [9].

Besides the effect of epilepsy on children’s sleep, the parent–child sleeping arrangement was also investigated by some studies. Larson et al. [28] found, apart from a higher score of parasomnias, more night wakings, shorter sleep duration, and excessive daytime sleepiness, as well as more parent–child room sharing and co-sleeping on the CSHQ, the Pittsburgh Sleep Quality Index (PSQI), and the Iowa Fatigue Scale (IFS) in 105 epileptic children (mean age = 6.19 years) compared to 79 controls (mean age = 5.32 years). In this sample, the epilepsy group had significantly more comorbidities than the control group, including attention deficit hyperactivity disorder (ADHD)/attention deficit disorder (ADD; 7.6 vs. 1.3 %), development delay (66.3 vs. 5.3 %), autism spectrum (22.9 vs. 2.5 %), respiratory comorbidities (7.6 vs. 0 %), gastroesophageal reflux (18.1 vs. 1.3 %), and other comorbidities (6.3 vs. 27.6 %) [28]. As in previous studies, Gutter and colleagues also reported more sleep problems in 130 children and adolescents with epilepsy (mean age = 7.82 years, SD = 1.86 years), such as reduced sleep efficiency, more sleep-related disordered breathing problems, shorter sleep duration, more night wakings, and excessive daytime sleepiness compared to 166 controls (mean age = 7.66 years, SD = 1.83 years) [22]. Of the epilepsy group, 6.15 % had comorbidities, compared to just 3.01 % of the control group. The authors implemented three questionnaires: the Sleep Disturbance Scale for Children (SDSC), the Medical Outcomes Study-Sleep Scale (MOSS‑S), and the Groningen Sleep Quality Scale (GSQS) [22]. A recent study by Urquhart et al. compared 33 children with epilepsy—12 suffering from focal seizures, 19 from generalized seizures, and two suffering from an unclassified seizure type—with 42 typically developing children [41]. Age range in the epilepsy group was 5 to 12 years with a median of 9 years; the control group were aged between 4 and 8.5 years, with a median age of 6 years. The parents of epileptic children reported higher rates of OSA on the Pediatric Sleep Questionnaire Sleep-Related Breathing Disorder Scale (PSQ-SRBD) and also higher rates of excessive daytime sleepiness on the Epworth Sleepiness Scale (ESS) than parents of controls. Of the epilepsy group, 55 % showed a conspicuous score (> 0.33) concerning OSA, whereas just 7 % of the controls showed these scores. The same applied to excessive daytime sleepiness: 30 % of the epileptic children versus 5 % of controls showed abnormal scores (≥ 10) [41].

To improve the sleep problems, melatonin was used for intervention and was effective [13, 20]. In detail, 23 children with intractable epilepsy, 52.1 % with generalized seizures, and 47.8 % with partial seizures who received oral melatonin before bedtime, showed a significant improvement regarding their sleep problems such as bedtime resistance, sleep duration, sleep latency, frequent nocturnal arousals, sleep walking, excessive daytime sleepiness, enuresis nocturna, teeth grinding, and sleep apnea surveyed with the CSHQ, as well as a reduction in seizure severity [13]. Similar results were found in 31 epileptic children, 16 of whom received melatonin and 15 a placebo. Different seizures types including absences, complex partial, generalized tonic–clonic seizures, and Lennox-Gastaut Syndrome did not differ between the groups. The percentage decrease in median sleep score in the melatonin group was 24.4 (range 0.0–34.9) [20].

Studies based on polysomnography

On average, the following studies based on polysomnography and/or polygraphy found less sleep problems than studies collecting data with questionnaires or both questionnaires and polysomnography.

Using polysomnography for one night, Clemens and Oláh [11] investigated 11 children aged 6–15 years with benign epilepsy with rolandic spikes compared to eight controls without central nervous system impairment or psychological alterations. Waking was the only sleep parameter that was more frequently observed in children suffering from epilepsy than in controls, with 24 vs. 6 min. Nunes and colleagues [33] also used polysomnography to prove sleep problems in 17 children with partial refractory epilepsy aged 4.7–16.2 years compared to 11 controls aged 7.17–18.8 years. These authors divided the epilepsy group in two subgroups, i.e., those with and those without ictal episodes during the recording. Both groups showed a reduced total bed time and reduced sleep duration in comparison to controls [32]. Because of limited data, Jain et al. [26] scrutinized OSA in 84 epileptic children with polysomnography. Children were divided into subgroups of seizure frequency for mild (N = 52) and severe refractory (N = 32) epilepsy. Symptoms of OSA were more frequent in children suffering from severe epilepsy than in those with mild epilepsy. However, there were no differences between children with generalized seizures, partial seizures, and complex partial seizures in terms of the prevalence of OSA [26]. In another study focusing on the diagnosis of sleep disorders, Jain and colleagues [27] identified 40 % of 108 epileptic children with an incorrectly diagnosed sleep disorder based on the initial symptoms, 30 % as having an unexpected sleep disorder, and 10 % as having no sleep disorder when checking the diagnosis with polysomnography [27].

When comparing 31 children with drug-resistant epilepsies, 21 with symptomatic localization-related epilepsy, and ten with idiopathic localization-related epilepsy aged 1.5–16.4 years (mean = 8.7 years) to ten children with benign epilepsy with rolandic spikes aged 6–10 years (mean = 8.1 years), it became apparent that the drug-resistant children had reduced stage N3 sleep, REM sleep, and sleep efficiency. Compared to 23 healthy, nonsnoring controls aged 3–15.4 years (mean = 8.3 years), these authors showed a shorter sleep duration and more night wakings [37]. Concerning AEDs, Palm and colleagues [35] scrutinized the daytime vigilance before and after (5–6 months later) discontinuation of AEDs in nine children with epilepsy aged 8.3–12.8 years (mean = 10.5 years). Five of the nine epileptic children had benign epilepsy of childhood with rolandic spikes, two had primary generalized and a further two had partial epilepsy. The results showed that the epilepsy patients had a higher daytime sleepiness than 18 controls aged 8.8–12.6 years (mean = 10.6 years), although there was no difference after discontinuation of the AEDs [35].

A study concerning chronotype was conducted by Gurkas and colleagues with 170 children suffering from different seizure types using video-EEG monitoring [21]. Mean age of the children was 11.4 years (SD = 4.1 years); 34 out of the epilepsy group had generalized seizures, 37 had temporal, 23 frontal, 9 occipital, and 3 parietal seizures. Most of the children suffered from multilobar seizures (N = 64). Specific seizures occurred in specific circadian patterns: tonic, clonic, and hypermotor seizures were more frequent in sleep, whereas auras, dialeptic, hypomotor, myoclonic, atonic seizures, and epileptic spasms were more frequent in wakefulness. Tonic seizures were the most frequent seizure type during sleep, with 127 cases. In addition, hypermotor seizures were also more common at night, whereas the other seizure types occurring in sleep did not show significant differences in terms of the time of the day. Generalized, temporal lobe, occipital, and parietal seizures were mostly seen during the daytime. In contrast, frontal lobe seizures appeared more frequently at night and in sleep (between 24:00 and 03:00 h) [21].

Studies based on polysomnography and questionnaires

In a study by Becker, Fennell, and Carney [5], who used both questionnaires and polysomnography, the relationship between sleep disruptions and seizure frequency, along with behavioral and emotional problems were investigated. Of the epilepsy sample, 57 % had a generalized epilepsy syndrome. Parental questionnaire, the PSQ, a self-rating questionnaire, and polysomnography were implemented. Of 30 children with epilepsy (mean age 10.3 years, SD = 2.1 years), 80 % showed sleep disruptions according to polysomnography. Causes of night wakings were either obstructive sleep apnea, disturbances of sleep architecture, or sleep fragmentation [5].

Holley and colleagues also compared actigraphy data to parental report. No differences in actigraphy data between 23 children with epilepsy aged 6.0–13.38 years (mean = 9.97 years, SD = 2.04 years) and 50 without aged 6.02–11.03 years (mean = 9.29 years, SD = 1.23 years) were found, although parents reported significantly more night wakings, parasomnias, and shorter sleep duration on the CSHQ when having a child with epilepsy [25].

In summary, although various studies concerning epilepsy in children and adolescents in relation to sleep and sleep problems and disorders exist, no studies to date were found which have specifically investigated dreams or nightmares in children and adolescents with epilepsy, or how these might affect their epilepsy.

Discussion

The purpose of this review was to evaluate the association between sleep and sleep disorders with epilepsy in childhood and adolescence. The search strategy identified 24 studies which met the required criteria and addressed sleep in children suffering from epilepsy. The main results of this review are in line with previous research. Sleep problems occur more often in children and adolescents suffering from epilepsy than in controls [2, 25]. Different sleep problems were found, such as more night wakings, excessive daytime sleepiness, more disordered breathing symptoms, parasomnias (which were mostly not further differentiated), shorter sleep duration, reduced sleep efficiency, and more sleep-related anxieties. Besides this, the studies implemented a wide variety of measurements regarding sleep. Self- and parent-assessments were used in 15 studies, whereas no studies used self-assessment only. Only seven studies implemented objective data to investigate sleep quality. In summary, the heterogeneity of sleep measurements made interpretation of the findings difficult, as did the fact that the investigated samples differed regarding disorder (epilepsy type), symptom severity, and kind of disease; furthermore, as Gurkas and colleagues reported, different seizure types occur in specific circadian patterns and sleep/wake distributions, which means that different epilepsy types influence sleep in different ways [21]. Therefore, the results of these studies are not fully generalizable to all children and adolescents suffering from epilepsy. However, no studies were identified reporting a missing association between epilepsy and sleep problems in children and adolescents. One might therefore assume that the association be proven; however, the possibility of publication bias should be kept in mind. Furthermore, cross-sectional designs do not allow any causal conclusions concerning the relationship between epilepsy and sleep to be drawn. More longitudinal studies are therefore needed. Concerning the significance or lack of significant results, several explanations are imaginable. First, sample sizes varied from 11 children in the epilepsy group to 331. Furthermore, studies used different measurements and exclusion criteria. Most used parental questionnaires and self-reports, only a small number (three) used polysomnography alone, and only three used combined versions. In addition, some studies excluded children who took AEDs, whereas in other studies these children were included. Another problem was the mixed profile of epilepsy disorders. Few studies investigated a specific epilepsy type, but many did not differentiate within the subtypes. Future research should control for subtypes of epilepsy.

Furthermore, the diversity of parental reports, self-reports, standardized questionnaires, and single questions, as well as that of the objective methods, might have caused differing results, since results concerning sleep factors differed between actigraphy and parental questionnaire. For example, objective methods showed no significant difference between children with epilepsy and controls, but parental questionnaire did. Parents reported significantly more night wakings, parasomnias, and a higher sleep duration [25]. The authors proposed parental anxieties and a higher selective attention as a reason behind this effect [24].

Many studies reported night wakings, whereas less found sleep-related anxiety in children suffering from epilepsy. One reason may be that some studies included questions about sleep-related anxieties. Others investigated the frequency of co-sleeping and found more in the epilepsy group [28], which could be a consequence of sleep-related anxiety of these children, but also of parental anxiety, as described above. However, no studies were found concerning dreams or nightmares of children and adolescents suffering from epilepsy. Therefore, these associations have to be proven in future research.

Based the presented findings, a model concerning sleep-related problems and disorders in children and adolescents suffering from epilepsy (CAESAR) was developed (Fig. 3). Most reported findings are marked with bold arrows.

That sleep problems are common in children and adolescents with epilepsy is undoubtable. The causes of these problems are multifactorial [25], since psychosocial factors can also influence the children’s sleep. Medication or some specific epilepsy types per se can also generate sleep problems; however, as already mentioned, more longitudinal studies are needed to draw causal conclusions. Moreover, it is important to keep in mind that sleep deprivation may trigger epileptic seizures [15]. Furthermore, it may be possible that treatment of sleep disorders in childhood improves quality of life and reduces seizure frequency [3, 31].

Practical conclusion

Sleep problems should not be disregarded in the diagnosis and treatment of childhood epilepsy. Consequences of sleep problems are more severe for patients with than without epilepsy [3]. Future research should investigate sleep problems in detail and with regard to the various epilepsy types. It would also be of interest to focus on the nonconformity of objective methods and parental report, and, since data are currently limited, to scrutinize the dreams of children and adolescents with epilepsy.

References

  1. 1.

    American Psychiatric Association (2013) Diagnostic and statistical manual of mental disorders, 5th edn. American Psychiatric Publ, Washington

    Google Scholar 

  2. 2.

    Batista BHB, Nunes ML (2007) Evaluation of sleep habits in children with epilepsy. Epilepsy Behav 11(1):60–64

    Article  PubMed  Google Scholar 

  3. 3.

    Bazil CW (2003) Epilepsy and sleep disturbance. Epilepsy Behav 4:39–45

    Article  Google Scholar 

  4. 4.

    Becker DA, Fennell EB, Carney PR (2003) Sleep disturbance in children with epilepsy. Epilepsy Behav 4(6):651–658

    Article  PubMed  Google Scholar 

  5. 5.

    Becker DA, Fennell EB, Carney PR (2004) Daytime behavior and sleep disturbance in childhood epilepsy. Epilepsy Behav 5(5):708–715

    Article  PubMed  Google Scholar 

  6. 6.

    Bell G, Sander J (2001) CPD – education and self-assessment the epidemiology of epilepsy. Seizure 10(4):306–316

    CAS  Article  PubMed  Google Scholar 

  7. 7.

    Berg AT, Berkovic SF, Brodie MJ et al (2010) Revised terminology and concepts for organization of seizures and epilepsies: report of the ILAE Commission on Classification and Terminology, 2005–2009. Epilepsia 51(4):676–685

    Article  PubMed  Google Scholar 

  8. 8.

    Byars AW, Byars KC, Johnson CS et al (2008) The relationship between sleep problems and neuropsychological functioning in children with first recognized seizures. Epilepsy Behav 13(4):607–613

    Article  PubMed  PubMed Central  Google Scholar 

  9. 9.

    Chan B, Cheong EYK, Ng SFG et al (2011) Evaluation of sleep disturbances in children with epilepsy: a questionnaire-based case-control study. Epilepsy Behav 21(4):437–440

    Article  PubMed  Google Scholar 

  10. 10.

    Chan S, Chevalier-Riffard C, Sayer H et al (2016) Sleep architecture and memory consolidation in children with focal epilepsy. Lancet 387:24

    Article  Google Scholar 

  11. 11.

    Clemens B, Oláh R (1987) Sleep studies in benign epilepsy of childhood with Rolandic spikes. I. sleep pathology. Epilepsia 28(1):20–23

    CAS  Article  PubMed  Google Scholar 

  12. 12.

    Cortesi F, Giannotti F, Ottaviano S (1999) Sleep problems and daytime behavior in childhood idiopathic epilepsy. Epilepsia 40(11):1557–1565

    CAS  Article  PubMed  Google Scholar 

  13. 13.

    Elkhayat HA, Hassanein SM, Tomoum HY et al (2010) Melatonin and sleep-related problems in children with intractable epilepsy. Pediatr Neurol 42(4):249–254

    Article  PubMed  Google Scholar 

  14. 14.

    Engel J (2001) A proposed diagnostic scheme for people with epileptic seizures and with epilepsy: report of the ILAE Task Force on Classification and Terminology. Epilepsia 42(6):796–803

    Article  PubMed  Google Scholar 

  15. 15.

    Ferlisi M, Shorvon S (2014) Seizure precipitants (triggering factors) in patients with epilepsy. Epilepsy Behav 33:101–105

    Article  PubMed  Google Scholar 

  16. 16.

    Fisher RS, van Boas WE, Blume W et al (2005) Epileptic seizures and epilepsy: definitions proposed by the international league against epilepsy (ILAE) and the international bureau for epilepsy (IBE). Epilepsia 46(4):470–472

    Article  PubMed  Google Scholar 

  17. 17.

    Fisher RS, Acevedo C, Arzimanoglou A et al (2014) ILAE official report: a practical clinical definition of epilepsy. Epilepsia 55(4):475–482

    Article  PubMed  Google Scholar 

  18. 18.

    Forsgren L, Beghi E, Oun A et al (2005) The epidemiology of epilepsy in Europe – a systematic review. Eur J Neurol 12(4):245–253

    CAS  Article  PubMed  Google Scholar 

  19. 19.

    Giannotti F, Cortesi F, Bruni O (1994) Sleep habits in children with idiopathic epilepsy. Sleep Res 23:361

    Google Scholar 

  20. 20.

    Gupta M, Aneja S, Kohli K (2005) Add-on melatonin improves sleep behavior in children with epilepsy. J Child Neurol 20(2):112–115

    Article  PubMed  Google Scholar 

  21. 21.

    Gurkas E, Serdaroglu A, Hirfanoglu T et al (2016) Sleep-wake distribution and circadian patterns of epileptic seizures in children. Eur J Paediatr Neurol 20(4):549–554

    Article  PubMed  Google Scholar 

  22. 22.

    Gutter T, Brouwer OF, de Weerd AW (2013) Subjective sleep disturbances in children with partial epilepsy and their effects on quality of life. Epilepsy Behav 28(3):481–488

    Article  PubMed  Google Scholar 

  23. 23.

    Hirtz D, Thurman DJ, Gwinn-Hardy K et al (2007) How common are the “common” neurologic disorders? Neurology 68(5):326–337

    CAS  Article  PubMed  Google Scholar 

  24. 24.

    Hoeppner JB, Garron DC, Cartwright RD (1984) Self-reported sleep disorder symptoms in epilepsy. Epilepsia 25(4):434–437

    CAS  Article  PubMed  Google Scholar 

  25. 25.

    Holley S, Whitney A, Kirkham FJ et al (2014) Executive function and sleep problems in childhood epilepsy. Epilepsy Behav 37:20–25

    CAS  Article  PubMed  Google Scholar 

  26. 26.

    Jain SV, Simakajornboon S, Shapiro SM et al (2012) Obstructive sleep apnea in children with epilepsy: prospective pilot trial. Acta Neurol Scand 125(1):e3–e6

    CAS  Article  PubMed  Google Scholar 

  27. 27.

    Jain SV, Simakajornboon N, Glauser TA (2013) Provider practices impact adequate diagnosis of sleep disorders in children with epilepsy. J Child Neurol 28(5):589–595

    Article  PubMed  Google Scholar 

  28. 28.

    Larson AM, Ryther RCC, Jennesson M et al (2012) Impact of pediatric epilepsy on sleep patterns and behaviors in children and parents. Epilepsia 53(7):1162–1169

    Article  PubMed  Google Scholar 

  29. 29.

    Maganti R, Hausman N, Koehn M et al (2006) Corrigendum to “Excessive daytime sleepiness and sleep complaints among children with epilepsy” [Epilepsy Behav. 8 (2006) 272–277]. Epilepsy Behav 9(1):216–217

    Article  Google Scholar 

  30. 30.

    Maganti R, Hausman N, Koehn M et al (2006) Excessive daytime sleepiness and sleep complaints among children with epilepsy. Epilepsy Behav 8(1):272–277

    Article  PubMed  Google Scholar 

  31. 31.

    Malow BA, Weatherwax KJ, Chervin RD et al (2003) Identification and treatment of obstructive sleep apnea in adults and children with epilepsy: a prospective pilot study. Sleep Med 4(6):509–515

    Article  PubMed  Google Scholar 

  32. 32.

    Merlino G, Piani A, Dolso P et al (2006) Sleep disorders in patients with end-stage renal disease undergoing dialysis therapy. Nephrol Dial Transplant 21(1):184–190

    Article  PubMed  Google Scholar 

  33. 33.

    Nunes ML, Ferri R, Arzimanoglou A et al (2003) Sleep organization in children with partial refractory epilepsy. J Child Neurol 18(11):763–766

    Article  PubMed  Google Scholar 

  34. 34.

    Ong LC, Yang WW, Wong SW et al (2010) Sleep habits and disturbances in Malaysian children with epilepsy. J Paediatr Child Health 46(3):80–84

    Article  PubMed  Google Scholar 

  35. 35.

    Palm L, Anderson H, Elmqvist D et al (1992) Daytime sleep tendency before and after discontinuation of antiepileptic drugs in preadolescent children with epilepsy. Epilepsia 33(4):687–691

    CAS  Article  PubMed  Google Scholar 

  36. 36.

    Panayiotopoulos CP (2005) The epilepsies. Bladon Medical Publ, Chipping Norton

    Google Scholar 

  37. 37.

    Pereira AM, Bruni O, Ferri R et al (2012) The impact of epilepsy on sleep architecture during childhood. Epilepsia 53(9):1519–1525

    Article  PubMed  Google Scholar 

  38. 38.

    Simonds JF, Parraga H (1982) Prevalence of sleep disorders and sleep behaviors in children and adolescents. J Am Acad Child Psychiatry 21(4):383–388

    CAS  Article  PubMed  Google Scholar 

  39. 39.

    Stores G, Wiggs L, Campling G (1998) Sleep disorders and their relationship to psychological disturbance in children with epilepsy. Child Care Health Dev 24(1):5–19

    CAS  Article  PubMed  Google Scholar 

  40. 40.

    Trinka E, Cock H, Hesdorffer D et al (2015) A definition and classification of status epilepticus – Report of the ILAE Task Force on Classification of Status Epilepticus. Epilepsia 56(10):1515–1523

    Article  PubMed  Google Scholar 

  41. 41.

    Urquhart DS, Kehinde OO, Mclellan AE (2016) Observational pilot study of reported symptoms of obstructive sleep apnoea in children with epilepsy. Dev Med Child Neurol. doi:10.1111/dmcn.13173

    PubMed  Google Scholar 

  42. 42.

    Wirrell E, Blackman M, Barlow K et al (2005) Sleep disturbances in children with epilepsy compared with their nearest-aged siblings. Dev Med Child Neurol 47(11):754–759

    Article  PubMed  Google Scholar 

Download references

Author information

Affiliations

Authors

Corresponding author

Correspondence to Angelika A. Schlarb.

Ethics declarations

Conflict of interest

A.A. Schlarb, R. Christen, M. G. Claßen, and C. G. Bien declare that they have no competing interests.

This article does not contain any studies with human participants or animals performed by any of the authors.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Schlarb, A.A., Christen, R., Claßen, M. et al. Sleep and dreaming in children and adolescents with epilepsy. Somnologie 20, 242–250 (2016). https://doi.org/10.1007/s11818-016-0077-1

Download citation

Keywords

  • Apnea
  • Sleep disorders
  • Sleep deprivation
  • Parasomnias
  • Epilepsy

Schlüsselwörter

  • Apnoe
  • Schlafstörungen
  • Schlafentzug
  • Parasomnien
  • Epilepsie