Sleep disturbance in children with epilepsy

Sleep disturbance in children with epilepsy

Epilepsy & Behavior Epilepsy & Behavior 4 (2003) 651–658 www.elsevier.com/locate/yebeh Sleep disturbance in children with epilepsyq Danielle A. Becke...

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Epilepsy & Behavior Epilepsy & Behavior 4 (2003) 651–658 www.elsevier.com/locate/yebeh

Sleep disturbance in children with epilepsyq Danielle A. Becker,a,b,e,* Eileen B. Fennell,a,c,e and Paul R. Carneyb,c,d,e a

Department of Clinical and Health Psychology, University of Florida, Box 100165, Gainesville, FL 32610-0165, USA b Department of Pediatrics, University of Florida, Gainesville, FL, USA c Department of Neurology, University of Florida, Gainesville, FL, USA d Department of Neuroscience, University of Florida, Gainesville, FL, USA e McKnight Brain Institute, University of Florida, Gainesville, FL, USA Received 9 April 2003; revised 17 July 2003; accepted 6 August 2003

Abstract This study employed a validated pediatric sleep questionnaire to evaluate for sleep-disordered symptoms in children with epilepsy (n ¼ 14). Results were compared with those for age-matched children (n ¼ 14) with known obstructive sleep apnea. Subjects were enrolled from an outpatient epilepsy clinic and a pediatric sleep disorders clinic. We hypothesized that children with epilepsy would (1) report symptoms of sleep disturbance similar to those of children with documented obstructive sleep apnea, and (2) display behavioral disturbances on parent and child behavioral symptom measures. Results indicate that more than 50% of children with epilepsy had behavioral problems (n ¼ 14). No differences in snoring, excessive daytime sleepiness, and restless sleep were seen between the two subject groups. Results suggest that neurobehavioral problems in children with epilepsy may in part be attributed to an underlying sleep disturbance. Ó 2003 Elsevier Inc. All rights reserved. Keywords: Epilepsy; Seizures; Obstructive sleep apnea; Daytime sleepiness; Pediatric Sleep Questionnaire; Behavior; Children

1. Introduction Children with epilepsy often exhibit sleep complaints such as sleepwalking, night terrors, confusional arousals, restless sleep, sleep fragmentation, and excessive daytime drowsiness [1,2]. Children with epilepsy also exhibit more behavioral problems such as inattention, poor concentration, and opposition than children with chronic illness or normal children [3]. Several reports have suggested such behavioral problems may in part be linked to abnormal sleep. For instance, learning and behavioral problems were more frequent in children with epilepsy who reported frequent nighttime awakening [4]. In younger children between 5 and 11 years of age, poor sleep quality was associated with daytime inattention [5]. Although daytime sleep complaints and q This work was supported by the University of Florida Division of Sponsored Research (P.R.C.) and the ChildrenÕs Miracle Network (P.R.C.). * Corresponding author. Fax: 1-352-273-6156. E-mail address: [email protected]fl.edu (D.A. Becker).

1525-5050/$ - see front matter Ó 2003 Elsevier Inc. All rights reserved. doi:10.1016/j.yebeh.2003.08.004

behavioral problems often coexist with childhood epilepsy, they can be challenging to characterize and differentiate. We conducted a prospective questionnaire-based study aimed at identifying a relation between sleep disturbances and daytime behavioral problems in children with epilepsy. The validated pediatric sleep questionnaire assessed for sleep-related breathing disorders such as obstructive sleep apnea and upper airway resistance, snoring, and excessive daytime sleepiness [6]. We compared sleep complaints in 14 children with epilepsy with similar sleep complaints in 14 children with known obstructive sleep apnea. We hypothesized that children with epilepsy would (1) report symptoms of sleep disturbance similar to those of children with documented obstructive sleep apnea, and (2) display behavioral disturbances on parent and child behavioral symptom measures. Results indicate that more than 50% of children with epilepsy exhibit behavioral problems resembling those of children with documented obstructive sleep apnea. Overnight sleep studies in these children further demonstrated that children with epilepsy had

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apneas, hypopneas, sleep fragmentation, disrupted sleep, and decreased sleep onset latency, quantitatively resembling children with obstructive sleep apnea. These findings suggest that daytime behavior problems encountered in children with epilepsy may, in part, be attributed to an underlying primary sleep disorder. This is the first study we are aware of in which children with epilepsy were systematically examined for sleep-related behavioral problems.

2. Methods 2.1. Subjects A total of 14 children with a known seizure disorder and 14 age- and gender-matched children diagnosed with polysomnography-confirmed obstructive sleep apnea were included in the study. Subjects diagnosed with epilepsy were recruited from the outpatient pediatric neurology clinic at the University of Florida. Children diagnosed with obstructive sleep apnea, who had previously completed the pediatric sleep questionnaire in conjunction with their sleep study, were obtained from an accredited sleep laboratory at the University of Florida. Parents of children with epilepsy were invited to participate in the study when, during a routine neurology visit, a medical review of systems revealed a variety of sleep complaints. Following the appointment, the children were referred for an overnight polysomnogram to further evaluate their sleep complaints, and subsequently they were invited to participate in our study. Selection criteria for children further included the following: diagnosis of epilepsy, as defined in the International League Against Epilepsy (ILAE) classification; taking no more than two anticonvulsant medications; no changes to medication regimen within the past month; age between 7 and 14 years and prepubertal with a Tanner score less than 4. Exclusion criteria for children included the following: IQ less than 70, as measured by the Receptive Scale on the Peabody Picture Vocabulary Test—Third Edition [7]; epilepsy caused by a progressive brain disorder; a significant history (within 2 years) of medical disease that may impair participation in the study (i.e., cardiovascular, hepatic, renal, gynecologic, musculoskeletal, gastrointestinal, metabolic, endocrine, or cancer with a metastatic potential); and a history of alcohol or drug abuse during the 1-year period prior to study participation. A previous consecutive 56-day seizure frequency and type were obtained from all participants at the time of enrollment. 2.2. Procedures Each child and parent gave assent and consent to take part in the study, which was approved by the

University of Florida Health Center Institutional Review Board. During an outpatient visit to the pediatric neurology clinic, parents of the children with epilepsy completed the parent sleep questionnaire on their childÕs behavior during sleep and wakefulness. The child and parent were then asked to complete a set of behavioral questionnaires (see Behavioral Measures). Patients were referred on for an overnight polysomnogram as part of standard diagnosis and care if they were highly suspected of having unconfirmed obstructive sleep apnea. Evaluation was based on chief complaint, review of systems, and positive endorsement of several items on the parent sleep questionnaire. These items included the presence of snoring, gasping sounds during the night, restless sleep, excessive daytime sleepiness, difficulty arousing in the morning, and frequent napping throughout the day, as such symptoms have been shown to suggest obstructive sleep apnea [8]. Patients with abnormal polysomnography were notified, seen for follow-up, and managed/treated accordingly. Parental reports on the nighttime behavior of children diagnosed with obstructive sleep apnea were collected from an accredited sleep laboratory at the University of Florida. As part of standard care of medical practice, overnight polysomnograms were performed on all children at an accredited sleep laboratory at the University of Florida Health Center, Gainesville, Florida. 2.3. Behavioral Measures 2.3.1. Pediatric Sleep Questionnaire Selected questions from the Pediatric Sleep Questionnaire [6] were used to assess the presence of sleep-disordered complaints. The Pediatric Sleep Questionnaire is a 70-item close-ended parent report measure with a yes/no/donÕt know response format. The questions cover a wide range of topics relevant to childrenÕs sleep, including items on sleep-disordered breathing, daytime sleepiness, and sleep hygiene. These questions were followed by open-ended questions about medical and family history. Within the Pediatric Sleep Questionnaire, validity and reliability have been established for a scale assessing childhood sleep-disordered breathing, and for subscales for snoring, sleepiness, and inattentive and hyperactive behavior [6]. Adequate internal consistency and reliability among the selected items used in the present study was demonstrated (CronbachÕs a ¼ 0:61). 2.3.2. Connors’ Parent Rating Scale—Revised, Long Form ConnorsÕ Parent Rating Scale—Revised, Long Form (CPRS-R:L) [9] is a parent report measure consisting of 80 items with 14 subscales that report on the behavior of youths aged 3–17 years. A T -score conversion from the

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DSM-IV: Total subscale was used to assess attention problems and hyperactivity–impulsiveness. 2.3.3. Eyberg Child Behavior Inventory The Eyberg Child Behavior Inventory (ECBI) [10] was used to assess the presence of externalizing and opposition problems. ECBI is a 36-item parent report rating scale. It rates children aged 2–16 years on frequency of behaviors and on whether the childÕs behavior is problematic for the parent. In this study, a T score converted from an intensity score was used to assess the severity of problem behaviors. 2.3.4. Children’s Depression Inventory The ChildrenÕs Depression Inventory (CDI) [11] was used to assess the presence and severity of depressive symptoms in children aged 7–17. CDI is a self-report measure consisting of 27 items. The child was instructed to select one of three statements that best described his or her feelings over the past 2 weeks. In the analysis, the total CDI score was converted to a T score to assess depressive symptoms. 2.3.5. Revised Child Manifest Anxiety Scale The Revised Child Manifest Anxiety Scale (RCMAS) [12] was used to assess the presence and severity of anxiety. The RCMAS is a 37-item, self-report questionnaire designed to assess the level of anxiety in youths aged 6–19 years. It provides a total anxiety score along with four subscale scores: Physiological Anxiety, Worry/ Oversensitivity, Social Concerns/Concentration, and Lie. A T score from the total anxiety score was used for the analysis in this study. 2.4. Sleep parameters 2.4.1. Apnea þ hypopnea index The apnea + hypopnea index (AHI) is the number of apneas and hypopneas per hour of sleep, expressed as total number/total sleep time in hours (central apneas were not included in the calculation) [13]. AHI was used to quantify clinical respiratory disturbance in both samples. In children, any cessation in airflow greater than two normal respiratory cycles is considered an apnea, and an AHI >1/hour is considered abnormal [13,14]. 2.4.2. Sleep efficiency Sleep efficiency is defined as total sleep time  100/ time in bed. Sleep efficiency of 85% or less is considered abnormal [8,13]. 2.5. Analyses Sleep complaint frequencies obtained from the Pediatric Sleep Questionnaire were compared between the

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epilepsy and obstructive apnea groups. The pediatric sleep questionnaire items chosen for data analysis were selected based on the desire to include items that represented symptoms of obstructive sleep apnea. These items included snoring frequency, observed breathing problems, problem sleepiness, and restlessness. Chi-square (v2 ) and Fisher exact tests of significance were used to compare the relative frequencies of positively endorsed symptoms. ‘‘DonÕt know’’ responses were discounted when calculating these statistics. Polysomnography was used to document disrupted sleep in both samples. StudentÕs unpaired t tests were used to examine for group differences on the polysomnographic variables. Published normative data for each behavioral/emotional measure were used to examine severity of daytime behavioral symptoms for the epilepsy sample only. The sample was classified into clinical and nonclinical groups on each measure, based on published clinical cutoffs. The frequency of children with epilepsy that fell into clinical and nonclinical ranges was examined. All analyses were performed with SPSS Version 10.1 statistical software (SPSS Inc., Chicago, IL, USA). In tests of statistical significance, the level was set at 0.05.

3. Results The mean ages for children with epilepsy and obstructive sleep apnea were 10.7  2.2 and 10.3  2.2 years, respectively. The proportion male was 0.71 for both groups. No significant differences in age or gender existed between the two groups. There were differences in ethnicity between the two groups (epilepsy group: 0.93 Caucasian; obstructive sleep apnea group: 0.43 Caucasian). Of the 14 children diagnosed with epilepsy, all 14 (100%) had evidence of respiratory disturbance (AHI > 1; range, 1.5–35) during their overnight polysomnogram. Children diagnosed with obstructive sleep apnea all had an AHI P 5 (range, 5–99). StudentÕs unpaired t tests showed the two groups did not significantly differ on mean sleep latency (P ¼ 0:641), mean sleep efficiency (P ¼ 0:143), or mean AHI (P ¼ 0:277) variables. Differences were found in the average percentage of time spent in stages 3 and 4 of sleep (P < 0:05) and in REM sleep (P < 0:05). Polysomnographic data are summarized in Tables 1 and 2. Children diagnosed with complex partial epilepsy (57%) averaged three seizures (range, 0–10) over a 56-day period, while children with generalized epilepsy (43%) averaged 18 seizures (range, 0–100). Fifty percent of the children were seizure-free during the 56-day period. None of the children had documented seizures during the overnight polysomnogram study. Of the children diagnosed with epilepsy, 86% were on anticonvulsant medications. Four children were also on stimulant medication (methylphenidate HCl or methylphenidate). Stimulation

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Table 1 Mean polysomnography data for both groupsa Polysomnographic variable

Epilepsy group (N ¼ 14)

OSA group (N ¼ 14)

P value

Time in sleep stage (%SPT) Stage 1 Stage 2 Stages 3 + 4 Stage REM Sleep latency (min) Sleep efficiency (%) AHI (No./h)

5.207 48.543 22.200 18.093 20.071 89.764 9.954

6.678 42.592 34.569 12.692 22.923 83.300 18.691

0.388 0.088 0.026b 0.029b 0.641 0.143 0.277

a b

SPT, sleep period time; OSA, obstructive sleep apnea. P < 0:05.

Table 2 Epilepsy type, anticonvulsant medication, sleep complaints, and polysomnographic results in epilepsy sample Subject

1 2 3 4 5 6 7 8 9 10 11 12 13 14

Epilepsy type

Generalized Generalized Partial Generalized Partial Generalized Partial Partial Generalized Partial Partial Generalized Partial Partial

Medicationsa

V V, CN V C C, CN E C E M T, C T, Cl E L M

Sleep complaintsb

Polysomnographyc SL (min)

RL (min)

SE (%)

AHI (No./h)

AI (No./h)

PLM (No./h)

RS, EDS S, RS, EDS, TR S, EDS S, EDS RS, EDS S, RS, EDS RS S, RS S, RS, EDS S S, EDS S S, RS, EDS S, RS, EDS

7.50 31.00 17.00 9.00 13.00 2.50 32.00 21.00 3.00 27.00 9.00 50.00 25.50 33.50

69.50 115.50 172.50 136.50 78.50 107.00 73.00 269.50 184.00 60.00 163.50 113.00 76.50 61.50

94.3 91.6 93.7 96.3 87.9 85.8 91.1 75.3 92 91.8 94.2 81.6 92 89.1

3.20 1.50 19.70 6.20 9.20 2.30 4.80 19.60 1.50 14.30 35.00 3.30 16.30 2.10

1.30 1.10 15.90 3.40 3.90 3.10 7.20 10.10 0.70 6.50 35.50 2.60 4.90 1.00

0.00 12.40 1.80 0.00 0.00 0.00 0.00 26.30 0.00 0.30 0.00 0.00 0.50 0.20

a

Medications: V, valproate; C, carbamazepine; E, ethosuximide; T, topiramate; Cl, clonazepam; L, lamotrigine; CN, methylphenidate HCl; M, methylphenidate. b S, snore; RS, restless sleep; EDS, excessive daytime sleep; TR, trouble breathing. c SL, sleep latency; RL, REM latency; SE, sleep efficiency; AHI, apnea/hypopnea index; AI, arousal index; PLM, periodic limb movement.

medication was discontinued for 72 hours prior to the sleep study, including the day that the polysomnogram was performed. Stimulation medication was continued the day following the polysomnogram. On the Fisher exact tests and v2 analyses no between-group differences were found in (1) the frequency of snoring [v2 ð1; N ¼ 25Þ ¼ 0:82, P > 0:05] (P ¼ 1:00 FisherÕs exact test), (2) daytime sleepiness complaints [v2 ð1; N ¼ 28Þ ¼ 0:01, P > 0:05] (P ¼ 1:00 FisherÕs exact test), and (3) restless sleep endorsements [v2 ð1; N ¼ 22Þ ¼ 3:38, P > 0:05] (P ¼ 0:115 FisherÕs exact test). Differences were found with troubled breathing [v2 ð1; N ¼ 25Þ ¼ 17:54, P < 0:01] (P < 0:01 FisherÕs exact test), and cessation of breathing [v2 ð1; N ¼ 27Þ ¼ 7:42, P < 0:01] (P < 0:05 FisherÕs exact test), with greater frequency of disturbance reported in children with obstructive sleep apnea. Graphic representation of these results is presented in Fig. 1. On the behavioral report measures administered to the epilepsy sample and their parents, 9 of the 14 subjects (64%) fell in the clinical range on the Connors

Fig. 1. Comparison of sleep complaint frequency between children with epilepsy and children with obstructive sleep apnea (OSA).

Parent Rating Scale. This suggests that nine of the children met clinical criteria for attention problems and hyperactivity–impulsiveness. On the Eyberg Child Behavior Inventory, six (43%) were in the clinical range, suggesting they met clinical criteria for the presence of

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Table 3 Clinical and nonclinical ranges of behavioral problems and frequencies of sleep complaints in children with epilepsya Measure

1 Sleep complaint

2 Sleep complaints

>2 Sleep complaints

CPRS-R:L Clinical Nonclinical

0 3

5 (36%) 1 (7%)

4 (28%) 1 (7%)

ECBI Clinical Nonclinical

0 3

4 (28%) 2 (14%)

2 (14%) 3 (21%)

CDI Clinical Nonclinical

0 3

1 (7%) 5 (36%)

0 (0%) 5 (36%)

RCMAS Clinical Nonclinical

1 2

1 (7%) 5 (36%)

2 (14%) 3 (21%)

a CPRS-R:L, ConnorsÕ Parent Rating Scale—Revised, Long Form; ECBI, Eyberg Child Behavior Inventory; CDI, ChildrenÕs Depression Inventory; RCMAS, Revised Child Manifest Anxiety Scale.

externalizing and opposition problems. On the ChildrenÕs Depression Inventory, one (7%) child fell in the clinical range, suggesting that child met clinical criteria for the diagnosis of clinical depression. Finally, four (29%) subjects scored in the clinical range on the Revised Child Manifest Anxiety Scale, suggesting clinically significant anxiety problems. The reported frequencies of internalizing versus externalizing behaviors differed among the group. The incidence of mood disorders was low compared with the amount of overt symptoms of attention/hyperactivity and opposition problems. Sleep complaint and behavior problem frequencies in the epilepsy sample are summarized in Table 3.

4. Discussion Disorders of sleep have an impact on the quality of life of both children and their caregivers [1]. Sleep disturbance and daytime sleepiness can present as a variety of clinical problems including inattention, depression, headache, and seizure [2]. Common sleep disorders in children include sleep respiratory syndromes, such as obstructive sleep apnea, primary snoring, and upper airway resistance syndrome. Obstructive sleep apnea is characterized by repetitive episodes of upper airway obstruction or cessation of breathing during sleep [13,15], and is often associated with blood oxygen saturation reduction and consequent arousals and sleep disruption. Individuals with obstructive sleep apnea may have complaints of excessive sleepiness or poor sleep [15]. Obstructive sleep apnea results in sleep fragmentation and can contribute to excessive daytime sleepiness [16]. Children with severe sleep-disordered breathing often experience multiple respiratory obstructive episodes, which may be associated with arousal, hypoxemia, and oxygen desaturation [1]. When chronic, this pattern leads to sleep deprivation and excessive daytime

sleepiness [17]. Sleep disruption and daytime sleepiness have been linked to daytime behavioral problems including poor school performance and externalizing untoward behaviors [18–22]. Epilepsy, a disorder that often affects a childÕs cognitive, social, and emotional well-being, also appears to have important secondary effects on sleep [4]. Alterations in total sleep time, sleep latency, and spontaneous awakenings have been reported in children with epilepsy [23,24]. Seizure disorders can affect both the quality and architecture of sleep [25]. Epileptic discharges may cause sleep disruption, preventing normal progression through sleep stages. For instance, in children with primary generalized tonic–clonic seizures, REM sleep may be decreased by 50% [26]. In partial epilepsy, where sleep disruption is less common, it has been shown that only those suffering from multiple nocturnal seizures experience a reduction in their proportion of REM sleep [27]. The lack of research on the clinical manifestations of sleep-related breathing disorders in children makes differentiation of diagnosis more challenging. Normal sleep–wake states have been described in children from infancy to 12 years of age [28]. However, comprehensive published norms clearly defining generalized pediatric sleep patterns, normal and abnormal, have not been available. This may in part be explained by the time, effort, and resources needed to conduct epidemiological research in this area. While some sleep pattern analysis is available in the adult literature, acquisition of pediatric data is more cumbersome in light of developmental considerations. Research in adults has benefitted from the existence of several validated questionnaires to assess for obstructive sleep apnea [29,30]. For example, the Epworth Sleepiness Scale is a questionnaire widely used for adult patients with sleep disorders [30]. However, few published questionnaires have been designed to assess sleep-related pediatric complaints and symptoms. In an ongoing effort to develop a pediatric questionnaire to

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help assess children for sleep disorders, Chervin and collaborators designed and validated the Pediatric Sleep Questionnaire. This questionnaire instrument includes assessment for sleep-related breathing disorders, snoring, excessive daytime sleepiness, and inattentive/ hyperactive behavioral symptoms [6]. We compared children with epilepsy and sleep complaints to children with known obstructive sleep apnea, as anecdotal evidence has suggested that children with epilepsy may have symptoms compatible with a primary sleep disorder. We hypothesized that (1) parents of children with epilepsy would endorse symptoms on a pediatric sleep questionnaire consistent with a primary sleep disorder, and (2) among children with epilepsy, there would be more evidence of daytime behavioral problems in children with sleep complaints. Children with known obstructive sleep apnea were employed for direct comparison of the qualitative aspects of childhood sleep. Results showed that no significant differences existed with respect to the occurrence of snoring, excessive daytime sleepiness, and restless sleep complaints between the children with epilepsy and those with obstructive sleep apnea. Respiratory problems such as troubled breathing and/or cessation of breathing were infrequently endorsed by the children with epilepsy or their parents. Overnight polysomnography was performed to determine if the children with epilepsy had disturbed sleep due to a respiratory disturbance, nocturnal seizures, sleep fragmentation, abnormal sleep architecture, and periodic leg movements of sleep (Tables 1 and 2). Interestingly, all 14 children with epilepsy in this study had an AHI greater than 1, whereas children with documented obstructive sleep apnea had AHIs of 5 or greater, indicating that sleep-disordered breathing may coexist with epilepsy. These findings were not interpreted as due to nocturnal seizures, as no behavioral or electroencephalographic seizures were encountered during the overnight polysomnograms in each of the children evaluated. Behavioral report measures were used to evaluate the severity of behavioral disturbance in the group with epilepsy. Results indicated that more than half of the epilepsy sample (64%) had attention problems and hyperactivity–impulsiveness. Further, 43% of the sample had problems with externalizing and oppositional behavior. Only 7 to 29% of the children reported internalizing behavior problems, clearly distinguishing these symptoms from externalizing behavior problems (Table 3). While 12 to 25% of all school-aged children are reported to experience behavioral and/or emotional disorders [31,32], children with disrupted sleep are reported to display increased behavioral problems such as aggression and opposition [19–22]. Problem behavioral estimates calculated in this study exceed the prevalence estimates for attention hyperactivity deficit disorder and opposition defiant disorder in the general pediatric

population [33]. It has been suggested that such daytime behavioral complaints often seen in children with epilepsy may be due in part to prolonged subclinical arousals and disturbed arousal mechanisms [34]. Limitations of the present study include small sample size and statistical power for the analyses. In attempting to address the problem of power, FisherÕs exact tests were used to calculate an exact probability value for the relationship between two dichotomous variables [35]. Nevertheless, despite our limited sample size, our findings were both statistically and clinically significant. Second, a comparative sample of children with known obstructive sleep apnea was contrasted with the epilepsy group in this study. Comparative normative data would have been preferred, but were unavailable to date. While the lack of normative data may in part be explained by the time, effort, and resources needed for collection, future comparison is warranted. Next, all but two children in our epilepsy sample were on anticonvulsant medication. Anticonvulsant medications have been shown to alter time spent asleep, sleep latency, and sleep architecture [36,37]. However, sleep disturbances have also been found to continue after the discontinuation of anticonvulsant therapy [24]. Our present group was not big enough to detect effects of anticonvulsant medication on sleep patterns (Table 2). In addition, four children were on stimulant medications. Stimulant medications have also been shown to affect sleep parameters by prolonging sleep latency and onset of the first REM cycle [38]. However, it is difficult to determine the relationship between medication effects and sleep disturbance given the reported link between symptoms of sleep-disordered breathing and problems with inattention and hyperactivity [39]. Lastly, report questionnaires may be confounded by subjectivity of the informant. We attempted to address this issue by evaluating objective polysomnographic data along with the reported sleep complaints. The results from this study further confirm previous reports that epilepsy appears to have important secondary effects on sleep and behavior [4]. Children with epilepsy experience alterations in total sleep, sleep architecture, sleep latency, and spontaneous arousals [23– 25]. They also experience a greater incidence of sleep fragmentation and daytime drowsiness [1]. These disruptions in sleep can be caused by epileptiform discharges [1], lack of melatonin variation [40], and anticonvulsant medication [36]. Nighttime awakenings and daytime sleepiness have been associated with daytime problems in learning and behavior in children with epilepsy [4]. We recently showed that REM latency and length of apnea events were also related to behavioral and emotional problems in children with epilepsy [41]. Nevertheless, sleep also has the tendency of activating epileptic discharges [42]. Sleep disorders that fragment sleep and produce daytime

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sleepiness may cause an increase in seizure frequency and produce difficulty in obtaining seizure control [1]. Treatment of sleep apnea has been shown to reduce both seizure frequency and severity in children and adults with epilepsy [1,43]. In light of the current study, treatment of sleep disturbance in children with epilepsy may also reduce the incidence of daytime behavioral problems. Future studies of children with epilepsy before and after treatment for sleep disorders are necessary to confirm this relationship. The present results underscore the need for further diagnostic sleep inquiry for children with epilepsy and concomitant sleep complaints, as unrecognized sleep disturbances in these children may contribute to behavioral problems and increased seizure frequency. These findings further support an association between sleep-disordered breathing and daytime behavioral symptoms, including sleepiness, hyperactivity, poor school performance, and aggression [19–22]. Although this study was conducted on a select group of children with epilepsy and sleep complaints, the results may have important relevance to the clinical care of children with epilepsy. Treatment of sleep disorders is likely to improve the quality of life and daily functioning for these children by reducing daytime behavioral and cognitive problems. Future research should explore potential associations between the regulation of sleep and the control of attention, along with accompanying emotional, behavioral, and cognitive problems. Additional exploration of these relationships with a larger sample size and normal control group may be beneficial in the assessment and treatment of sleep complaints. A reduction in behavioral and cognitive symptoms associated with disrupted sleep may eventually lead to an improvement in the quality of life for children with epilepsy.

Acknowledgments The authors thank Lucia Manubens-Carney for reviewing the manuscript. We also thank and acknowledge the secretarial and nursing staff of the Department of Pediatrics, Division of Pediatric Neurology, as well as the staff at the University of Florida Sleep Laboratory.

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