Epilepsy & Behavior 21 (2011) 437–440

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Epilepsy & Behavior

j o u r n a l h o m e p a g e : w w w. e l s ev i e r. c o m / l o c a t e / ye b e h

Evaluation of sleep disturbances in children with epilepsy: A questionnaire-based

case–control study
Bosco Chan ⁎, Eric Yau Kin Cheong, Sui Fun Grace Ng, Yick Chun Chan, Qun Ui Lee, Kwok Yin Chan
Department of Pediatrics and Adolescent Medicine, Princess Margaret Hospital, Hong Kong

a r t i c l e i n f o a b s t r a c t

Article history: Epilepsy is a chronic neurological disorder accompanied by a wide range of comorbid conditions that can
Received 25 February 2011 adversely affect the quality of life of children. Sleep disturbances not only predispose children to mood,
Revised 3 May 2011 cognitive, and behavioral impairments, but also have a significant impact on physical health. The aim of
Accepted 6 May 2011
this study was to evaluate sleep patterns among Chinese children with epilepsy and healthy subjects in
Available online 24 June 2011
Hong Kong, and examine the relationship between parent-reported sleep problems and specific epilepsy
Keywords:
parameters. We conducted a cross-sectional, questionnaire-based, case–control study and included 63
Sleep children with epilepsy and 169 healthy children aged between 4 and 12 years. The Children's Sleep Habits
Epilepsy Questionnaire (CSHQ) was used as an assessment tool. Our results indicated that children with epilepsy have
Children similar sleep patterns but greater sleep disturbances compared with healthy subjects. Sleep problems should
Children's Sleep Habits Questionnaire not be overlooked, and a comprehensive review of the sleep habits of this group of patients should be
Sleep disturbance conducted.
Anticonvulsants Crown Copyright © 2011 Published by Elsevier Inc. All rights reserved.
Sodium valproate
Quality of life
Behavior

1. Introduction
Epilepsy is a chronic neurological disorder accompanied by a
wide range of comorbid conditions that can adversely affect the
quality of life of patients [1,2]. Children with epilepsy often exhibit
more behavioral problems and psychological disturbances than
healthy children [3]. Although sleep disturbance is one of the most
common behavioral problems among children with epilepsy [4], it
is frequently overlooked. Many practitioners and even parents
may view excessive tiredness as an unavoidable adverse effect of
antiepileptic medications [5]. In fact, the relationship between sleep
and epilepsy is complex and bidirectional [6].
The effects of sleep on epilepsy have been well documented in
previous studies [3–11]. Sleep has direct effects on the occurrence
of certain seizures and interictal epileptiform discharges. Sleep
deprivation is frequently used in long-term epilepsy monitoring,
and sleep itself may activate interictal activity in approximately
a third of patients with epilepsy and in up to 90% of those with sleep/
wake-related epilepsies [7]. Epileptic seizures, in turn, may disrupt
regulation of the sleep/wake cycle, and antiepileptic medications can
affect normal sleep architecture and reduce sleep efficiency [12]. In
addition, sleep disorders such as obstructive sleep apnea may coexist
with epilepsy and complicate seizure control [7]. Previous studies
have also suggested a positive association between daytime behav-
ioral problems and sleep disruption in children with epilepsy, and
treatment of sleep disturbances can reduce the prevalence of daytime
behavioral problems reported in these children [6,7,13,14].
Cultural and social factors are known to influence sleep patterns
in children. Most epidemiological studies have focused on Western
children, and few studies have examined the sleep patterns and
sleep problems of Chinese children with epilepsy [15]. We therefore
conducted a cross-sectional, questionnaire-based, case–control study
to compare Chinese children with epilepsy with healthy children at
two regional hospitals in Hong Kong. Our aims were to (1) evaluate
the parent-reported sleep patterns of Chinese children with epi-
lepsy; (2) characterize the types and frequencies of parent-reported
sleep problems in these children; and (3) examine the relationship
between parent-reported sleep problems and specific epilepsy
parameters.
2. Methods
2.1. Subjects

⁎ Corresponding author at: Department of Pediatrics and Adolescent Medicine,

Princess Margaret Hospital, 2–10 Princess Margaret Hospital Road, Lai Chi Kok,
Children aged 4 to 12 years with a diagnosis of epilepsy were
Kowloon, Hong Kong. Fax: + 852 2370 3466. recruited from the Pediatric Neurology Outpatient clinics at the
E-mail address: chbosco@netvigator.com (B. Chan). Department of Pediatrics and Adolescent Medicine at two regional

1525-5050/$ – see front matter. Crown Copyright © 2011 Published by Elsevier Inc. All rights reserved.
doi:10.1016/j.yebeh.2011.05.007
438 B. Chan et al. / Epilepsy & Behavior 21 (2011) 437–440
hospitals in Hong Kong. Evidence of a diagnosis of epilepsy was taken
from the medical records. All subjects had active epilepsy, meaning
that they had been experiencing seizures in the preceding year or
receiving prophylactic antiepileptic drugs. Parents or primary care-
takers who consented to participate in the study were asked to
complete the questionnaire in the outpatient clinic in front of the
investigators. Additional data collected included age, gender, age at
seizure onset, duration of illness, presence of developmental delay,
types of seizures, seizure frequency over the preceding 6 months,
predominance of nocturnal or daytime seizures, number and types
of antiepileptic drugs, timing of last dose before sleep, and therapy
duration.
A group of healthy subjects comparable with respect to age and sex
were recruited as a control group. They were selected from a total of
four kindergartens and primary schools in the same district. The aims
of the study were explained to school principals in the corresponding
target schools, and permission was obtained to conduct the study.
Two classes from each grade were randomly selected to yield a pool of
300 children to participate the study. The questionnaire and consent
form were distributed to parents by teachers with a letter explaining
the aim of the study. Parents completed the questionnaires on
their own and returned them to the teacher. All questionnaires were
collected and returned to the author.
Excluded were patients who (1) had a chronic respiratory disorder
or sleep-disordered breathing; (2) had a nonepileptic neurological
disorder; or (3) were taking medications to promote sleep.
The study ran from January to June 2009. Ethical approval was
given by the Kowloon West Cluster Clinical Research Ethics Committee
of Hong Kong Hospital Authority.
2.2. Assessment tool: Children's Sleep Habits Questionnaire
The Children's Sleep Habits Questionnaire (CSHQ) is a parent-
report questionnaire designated for use in assessment of sleep
patterns and sleep problems in children [16]. The validated Chinese-
language version of the CSHQ was used [17,18]. It asks for information
on sleep patterns and 33 sleep disturbance items relating to a number
of sleep domains conceptually grouped into eight subscales: Bedtime
Resistance, Sleep-Onset Delay, Sleep Duration, Sleep Anxiety, Night
Waking, Parasomnias, Sleep-Disordered Breathing, and Daytime
Sleepiness. Each item is rated on a 3-point scale that describes
the frequency of the behaviors. Parents were asked to recall sleep
behaviors occurring over a recent “typical” week. The Total CSHQ
score includes all eight subscale scores, and higher scores are
indicative of more disturbed sleep. A score of 41 has been reported
to be a sensitive cutoff for identification of probable sleep problems
in children [19].
2.3. Statistical analysis
Data processing and analysis were performed with SPSS Version
16.0. We performed multivariate analyses of covariance (MANCOVAs)
with gender as a between-subject factor and age as a covariate to
assess the effects of gender and age on sleep patterns for the control
and epilepsy groups. The dependent variables were compared with the
χ 2 test, Mann–Whitney U test, independent sample t test, and one-way
analysis of variance (ANOVA). Values were considered statistically
significant at P b 0.05.
3. Results
3.1. Demographic characteristics
Of the 300 questionnaires returned from the control group, 131
were excluded: 59 because of grossly incomplete data information,
47 because of history of allergic airway disease, and 25 because
subjects were taking medicines that might affect sleep architecture.
The remaining 169 questionnaires (56%) were included in the data
analysis. The control group consisted of 83 males (49.1%) and 86
females (50.9%) with a mean age of 7.7 ± 2.40. In the epilepsy group,
65 patients were approached, 2 of whom were excluded because of
a history of asthma. A total of 63 children were recruited into the
study. There were 31 males (49.2%) and 32 females (50.8%) with a
mean age of 8.35 ± 2.50. There were no significant age and gender
differences between the control and epilepsy groups.
3.2. Sleep patterns
In the control group, total sleep time during weekdays and weekends
was 8.89± 1.0 and 9.68 ± 1.45 hours, respectively. In the epilepsy
group, total sleep time was 8.93 ± 1.14 and 9.76 ± 1.21 hours, respec-
tively (Table 1). ANCOVA did not reveal significant differences between
the genders, but with advancing age, weekday and weekend bedtimes
were significantly postponed, weekday wake time was earlier but
weekend wake time was delayed, and the children slept significantly
less during weekday but more on the weekend.
3.3. Comparisons of CSHQ subscale scores of the epilepsy and control
groups
Comparisons of CSHQ subscale scores of the epilepsy and control
groups are outlined in Table 1. The children with epilepsy had higher
mean scores on all CSHQ subscales than controls, indicating that the
children with epilepsy were more likely to have parent-reported sleep
problems. ANCOVA indicated that the Total CSHQ score and all subscale
scores except Sleep Duration and Daytime Sleepiness were significantly
higher in the epilepsy group. Among the eight subscales, Bedtime
Resistance and Sleep Anxiety scores significantly declined with age, and
girls had higher Parasomnia scores than boys. Otherwise, ANCOVA
did not show significant differences with age and gender among the
different subscales (Table 2). In relation to the previously used [16,19]
cutoff score of 41 generated by analysis of the receiver operator
characteristic (ROC) curve that yielded a sensitivity of 0.80 and
specificity of 0.72, the mean total disturbance scores in both groups
were higher than the cutoff score (control group: 44.10 ± 6.43; epilepsy
group: 48.89 ± 6.83).
3.4. Correlation of scores with type of epilepsy (generalized or partial)
There were 40 children with generalized epilepsy and 23 children
with partial epilepsy. There were no significant age and sex difference
with respect to type of epilepsy. There were no significant differences
in age at onset, duration of illness, presence of developmental delay,
seizure frequency, predominant seizure time, and types and number
of anticonvulsants used between children with generalized and
those with partial epilepsy. Also, there were no statistically significant
differences in the eight subscale scores and Total score between the
two groups.
3.4.1. Correlation of scores with different epilepsy parameters
Table 2 summarizes the epilepsy characteristics. Children with
epilepsy and developmental delay had a significantly higher Bedtime
Resistance score (10.41 ± 2.84, P = 0.048) than those without devel-
opmental delay (8.95 ± 2.68). Children with no predominant seizure
time were reported to have more sleep disturbances than those with
an average frequency of predominantly daytime or nocturnal seizures
as reflected by the significantly higher Total (P = 0.001), Sleep Anxiety
(P = 0.022), Parasomnia (P = 0.009), Sleep-Disordered Breathing
(P = 0.012), and Daytime Sleepiness (P = 0.006) scores. Eighty-nine
percent of the children with epilepsy were taking antiepileptic drugs,
62% on monotherapy and 27% on polytherapy. Fifty-five percent of
the children with epilepsy were taking sodium valporate. Sodium
 B. Chan et al. / Epilepsy & Behavior 21 (2011) 437–440 439

Table 1
Sleep patterns and CSHQ scores of subjects with epilepsy (n = 63) and controls (n = 169).

Controls Subjects with epilepsy P ANCOVA (F value)

n Mean ± SD n Mean ± SD Age Sex Controls/ subjects

Sleep pattern
Sleep time (hours in weekday) 164 8.89 ± 1.00 63 8.93 ± 1.14 0.792 19.19b 0.02 0.72
Sleep time (hours in weekend) 164 9.68 ± 1.45 63 9.76 ± 1.21 0.694 6.92c 3.77 0.01
Night wakening time (min) 53 2.41 ± 3.24 63 7.95 ± 22.13 0.073 0.01 1.12 2.74
CSHQ subscale
Bedtime Resistance (6)a 169 8.46 ± 2.51 63 9.46 ± 2.81 0.010 22.67b 0.62 10.69b
Sleep Onset Delay (1) 169 1.29 ± 0.53 63 1.67 ± 0.80 0.001 0.03 0.06 16.70b
Sleep Duration (3) 169 4.47 ± 1.46 63 4.76 ± 1.64 0.188 0.38 0.54 1.52
Sleep Anxiety (4) 169 5.21 ± 1.83 63 5.98 ± 2.03 0.006 13.05b 0.01 10.55b
Night Waking (3) 169 3.28 ± 0.84 63 3.79 ± 1.14 0.002 1.24 1.23 14.60b
Parasomnias (7) 169 8.07 ± 1.66 63 9.37 ± 2.14 b0.001 0.94 4.27d 24.92b
Sleep-Disordered Breathing (3) 169 3.33 ± 0.88 63 3.75 ± 1.03 0.005 0.16 0.24 9.09c
Daytime Sleepiness (8) 169 12.79 ± 3.26 63 13.37 ± 3.16 0.232 1.04 2.96 1.16
Total score (33) 169 44.10 ± 6.43 63 48.89 ± 6.83 b0.001 2.64 0.69 26.41b
a
Number in parentheses denotes number of items within the subscale.
b
P b 0.01.
c
P b 0.001.
d
P b 0.05.

valproate was the only anticonvulsant associated with a significantly between subjects who took their last dose within 2 hours of sleep and
higher Total CSHQ score (50.89 ± 7.49 vs 46.39 ± 4.96, P = 0.008) and those whose last dose was taken more than 2 hours before sleep.
a significantly higher Night Waking score (4.09 ± 1.31 vs 3.43 ± 0.74,
P = 0.022). Eight percent of children were taking clobazam, and they 4. Discussion
had a significantly higher Sleep-Disordered Breathing score than
those not taking this medication (5.0 ± 1.59 vs 3.64 ± 0.91, P = 0.043). Epilepsy is a chronic disorder that often affects the cognitive,
Assessment of the correlation of duration of therapy and time of social, and emotional well-being of children. Although sleep disorders
last dose before sleep with CSHQ scores revealed no statistically are common in general pediatric patients, sleep disturbance is more
significant differences in subscale and Total scores between subjects prevalent in children with epilepsy but frequently is overlooked
treated less than than 2 years and those treated more than 2 years and [4,9,10,20]. In this study, we compared the sleep patterns and sleep
problems of healthy children and children with epilepsy, and we
believe that this is the first questionnaire-based case–control study on
Table 2 sleep and epilepsy in Hong Kong.
Epilepsy characteristics. With respect to the CSHQ, the mean Total score for both groups
(control group: 44.10 ± 6.43; epilepsy group: 48.89 ± 6.83) was
Epilepsy characteristic Number (%) of patients
higher than the cutoff score of 41 used in previous studies [16,19].
Sex This in keeping with Liu and colleagues’ study which compared the
Male 31 (49%)
Female 32 (51%)
sleep patterns and problems among schoolchildren in the United
Developmental delaya States and China with the CSHQ (Chinese children, 42.11 ± 7.43; US
No 41 (65%) children, 38.71 ± 5.51) [15] and indicates that apart from biological
Yes 22 (35%) factors, different cultural and social factors can influence sleep
Seizure frequency over past 6 months
problems in children. The CSHQ is a useful assessment tool for
No attack 26 (41%)
At least once over past 6 months 18 (29%) screening sleep problems and tracking treatment effects in children
At least once every month 7 (11%) with neurodevelopmental disorders [16,17]. However, we suggest the
At least once every week 7 (11%) cutoff value of 41 characterizing a problem sleeper should not be
At least once every day 5 (8%) applied to Chinese children, probably because of genetic or sociocul-
Seizure time
Daytime predominant 29 (46%)
tural differences.
Nocturnal predominant 23 (37%) We found that the Total CSHQ score and all subscale scores, with
No predominant timing in sleep cycle 11 (17%) the exception of Sleep Duration and Daytime Sleepiness, were
Treatment significantly higher in the epilepsy group. We used healthy controls
Monotherapy 39 (62%)
to minimize the effect of cultural and social variations in our locality,
Polytherapy 17 (27%)
No therapy 7 (11%) and our results are consistent with previous studies [4,9,10,21]. This
Medication used indicates that children with epilepsy in Hong Kong are more likely
Valproate 35 (55%) to have parent-reported sleep problems. There are several possible
Carbamazepine 17 (27%) explanations. First, because of parental concern over seizure occur-
Topiramate 8 (13%)
rence during sleep, children with epilepsy may be co-sleeping with
Levetiracetam 9 (14%)
Clonazepam 2 (3%) a caregiver, enabling parents to perform frequent nighttime checks.
Gabapentin 1 (2%) This can lead to increased sleep fragmentation and night awakening
Clobazam 5 (8%) and cause poor sleep and anxiety, as well as an increase in the parent-
Lamotrigine 1 (2%)
reported rate of sleep problems during co-sleeping [22]. Second,
Phenobarbital 2 (3%)
Nitrazepam 1 (2%) parents of children with epilepsy suffer more stress than parents of
Vigabatrin 1 (2%) children without disabilities, and sleep problems are an additional
a
Developmental delay is defined as delay in development in the gross motor, fine
burden on these families. Parents may be more lax, for example, in
motor, language, or cognitive area, or previous assessment and receipt of developmental limit setting, which may contribute to bedtime resistance or difficult
training or special training. behavior on night awakenings [23,24].
440 B. Chan et al. / Epilepsy & Behavior 21 (2011) 437–440
We detected a number of interesting relationships between sleep
and different epilepsy parameters in children with epilepsy. Children
with no predominant seizure time had more sleep disturbances than
those with an average frequency of predominantly daytime or nocturnal
seizures. Moreover, although type of seizure may influence sleep
organization, and a previous study has shown that generalized seizures
are more often associated with poorer sleep habits [8], we could not
find any significant difference between the subjects with generalized
and those with partial epilepsy. The only significant difference was the
predominant use of sodium valproate in generalized epilepsy and of
carbamazepine in partial epilepsy; it is common clinical practice in our
locality to prescribe these medications as first-line treatments.
Antiepileptic medications have been shown to affect sleep duration,
sleep latency, and sleep architecture [5–7]. Adverse antiepileptic drug
effects are a major obstacle to achievement of optimal dosing for
seizure control. Common adverse effects include tiredness, sleepiness,
unsteadiness, memory problems, and difficulty concentrating [25,26].
Traditional anticonvulsants and polytherapy are more commonly
associated with sleep problems [10,27]. However, we cannot demon-
strate any significant differences between traditional and newer
antiepileptic agents or between monotherapy and polytherapy.
Among the different antiepileptic medications, sodium valproate is
the only anticonvulsant that was associated with a significantly higher
Total score and Night Waking score. Our finding is consistent with
previous studies. Sodium valproate may increase arousals, increase
slow wave sleep, decrease REM sleep, and cause excessive sleepiness
[7]. Schmitt et al. have recently shown that termination of sodium
valproate after long-term treatment can lead to a significant reduction
in sleep duration in children older than 6 years of age [28]. We may,
therefore, need to identify and adjust the bedtime schedule to prevent
subsequent development of behavioral sleep problems.
An association between epilepsy and obstructive sleep apnea
has been reported [9,13]. Benzodiazepines may cause suppression
of responsiveness of carbon dioxide and oxygen desaturation and
increase upper airway musculature relaxation, which may increase
the risk of sleep apnea [7]. This is consistent with our observation that
children on clobazam are reported to have more sleep-disordered
breathing problems. Therapeutic intervention for coexisting obstruc-
tive sleep apnea can help to decrease daytime behavioral problems
and improve seizure control [13]. Although we failed to demonstrate
any significant difference in treatment duration and time of last dose
before sleep, choosing antiepileptic agents that minimally interfere
with sleep, using monotherapy and minimum effective dosages,
and paying attention to the specific time of drug administration, can
lead to improvement of sleep as well as quality of life in patients with
epilepsy and excessive daytime somnolence.
Bedtime resistance is commonly encountered in children with
neurodevelopmental disabilities [29]. Doo and Wing [17] examined
the sleep problems of children with pervasive developmental disorders
in Hong Kong, and bedtime resistance was the most commonly reported
sleep problem. We find that children with epilepsy and developmental
delay also have a more significant bedtime resistance problem than
those without developmental delay. Appropriate sleep hygiene, includ-
ing regular sleep and wake times, reduced environmental stimulation,
and routine activities before bedtime must be emphasized and planned
carefully in order to promote good sleep health for these children.
Several limitations are associated with this study. First, the
evaluation of sleep disturbances was based mainly on parental reports
instead of objective measures such as overnight polysomnography
or actigraphy; hence reporting bias may have influenced self-report
measures. This may overestimate or underestimate the actual preva-
lence of sleep problems among these children. Second, the children in
the control group were recruited from four kindergartens and primary
schools, and the results for this sample may not be generalizable to
all children in Hong Kong. Moreover, only 169 of 300 control families
who returned questionnaires (56%) were included in data analysis.
It is unclear whether and to what extent the study results could have
been affected by the excluded samples.
5. Conclusion
In summary, our findings demonstrate that children with epilepsy
have greater sleep disturbances than healthy subjects in Hong Kong.
Sleep disturbances not only predispose children to mood, cognitive,
and behavioral impairments, but also have a significant impact on
physical health which may be even more pronounced in children with
epilepsy. Sleep habits should be comprehensively reviewed when a
sleep problem is identified in children with epilepsy. Other param-
eters such as seizure types and patterns, coexisting sleep-disordered
breathing, and types and methods of administration of antiepileptic
medications should be considered in the evaluation. Appropriate
sleep hygiene should be encouraged, and parents should be educated
about the impact on sleep to reduce families’ stress and burden.
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