wake patterns of generalized seizures in children

Epilepsia, 52(6):1076–1083, 2011 doi: 10.1111/j.1528-1167.2011.03023.x FULL-LENGTH ORIGINAL RESEARCH Circadian distribution and sleep/wake patterns ...
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Epilepsia, 52(6):1076–1083, 2011 doi: 10.1111/j.1528-1167.2011.03023.x

FULL-LENGTH ORIGINAL RESEARCH

Circadian distribution and sleep/wake patterns of generalized seizures in children *y1Marcin Zarowski, *1Tobias Loddenkemper, *Martina Vendrame, zAndreas V. Alexopoulos, zElaine Wyllie, and *Sanjeev V. Kothare *Department of Neurology, Division of Epilepsy and Clinical Neurophysiology, Children’s Hospital, Harvard Medical School, Boston, Massachusetts, U.S.A.; yPolysomnography and Sleep Research Unit, Department of Developmental Neurology, Poznan University of Medical Sciences, Poznan, Poland; and zEpilepsy Center, Neurological Institute, Cleveland Clinic, Cleveland, Ohio, U.S.A.

SUMMARY Purpose: To evaluate the relationship of sleep/awake and circadian patterns to generalized seizures. Methods: Charts of 1,044 consecutive pediatric epilepsy patients undergoing video-electroencephalography (EEG) monitoring (vEEG) over 5 years were reviewed: 962 patients were excluded due to focal epilepsy (556), nonepileptic recorded events (217), missing data (125), age over 21 years (59), and no recorded events or seizures (10). Seizure semiology of recorded seizures with generalized onset on EEG was classified according to the International League Against Epilepsy (ILAE) seizure semiology terminology, and analyzed based on occurrence during day (6 a.m. to 6 p.m.) or night and on their relationship to wakefulness and sleep, with calculated occurrence in 3-h time blocks throughout 24 h. Statistical analysis was performed with binomial testing. Key Findings: Three-hundred sixteen generalized seizures were analyzed in 77 children. Mean age was 6.4 years ± 5.4 (range 0.33–20 years), including 50.6% girls. Tonic and

The daily periodicity of seizures in patients with epilepsy was reported in the early neurology literature (LangdonDown & Brain, 1929). Although seizures may be perceived by patients as unpredictable events, the occurrence of seizures is not entirely random (Quigg, 2000). Gowers observed that ‘‘diurnal’’ seizures cluster at certain times of the day, namely upon awakening and in the late afternoon, and that ‘‘nocturnal’’ seizures tend to occur mainly at Accepted January 20, 2011; Early View publication March 22, 2011. Address correspondence to Sanjeev V. Kothare, MD, FAAP, Center for Pediatric Sleep Disorders, Division of Epilepsy and Clinical Neurophysiology, Department of Neurology, Children’s Hospital, Harvard Medical School, Fegan 9, 300 Longwood Avenue, Boston, MA 02115, U.S.A. E-mail: [email protected] 1 Both authors contributed equally to this manuscript. Wiley Periodicals, Inc. ª 2011 International League Against Epilepsy

tonic–clonic seizures were more frequently seen in sleep, whereas all other generalized semiologic seizure types occurred more frequently out of wakefulness. Clonic seizures had two peaks: (6–9 a.m.) and (noon to 3 p.m.) in wakefulness. Absence seizures occurred predominantly in wakefulness, (9 a.m. to noon and 6 p.m. to midnight). Atonic seizures occurred predominantly in wakefulness (noon to 6 p.m.). Myoclonic seizures occurred in wakefulness (6 a.m. to noon). Epileptic spasms had two peaks: (6–9 a.m. and 3–6 p.m.) in wakefulness. Significance: Circadian pattern and sleep–wake patterns are important considerations in characterization of generalized seizure types. Recognition and characterization of individual diurnal seizure patterns offer new diagnostic and therapeutic options, including EEG or long-term video EEG monitoring scheduling, differential (day/night) medication dosing, and a better understanding of pathophysiologic mechanisms underlying circadian patterns of epilepsy. KEY WORDS: Epilepsy monitoring, Circadian patterns, Generalized seizures, Semiology, Epilepsy.

bedtime and in the early morning hours before awakening (Langdon-Down & Brain, 1929; Griffiths & Fox, 1938). Janz (1962) noted that up to 45% of patients with primarily generalized tonic–clonic seizures had nocturnal seizures. Recent findings both in animal models and in human partial epilepsy suggest a direct circadian influence on seizures of limbic origin (Quigg et al., 1998, 2000). Patients with frontal lobe epilepsy typically have partial seizures arising from sleep (Bazil & Walczak, 1997), almost exclusively in stages I and II of non–rapid eye movement sleep (NREM) sleep (Herman et al., 2001; Minecan et al., 2002). Several studies have shown a marked effect of sleep on the timing of seizures (Janz, 1962; Touchon et al., 1991), and suggest that sleep increases the frequency, duration, and rate of secondary generalization of partial seizures (Montplaisir et al., 1987; Bazil & Walczak, 1997), but there are no data on the relationship of generalized seizures to diurnal rhythms,

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1077 Chronobiology of Generalized Seizures especially in children. The objective of our study was to evaluate the relationship of sleep–wake and circadian pattern with various subtypes of generalized seizures.

Methods Patient selection Charts of 1,044 consecutive pediatric epilepsy patients undergoing video–electroencephalography (EEG) monitoring (vEEG) over 5 years (1998–2002) were reviewed. Patients who met the following criteria were included: 1. Seizures during wake or/and sleep recorded by vEEG; 2. Video recording of seizures available for review; 3. Generalized seizures with no focal seizure-onset by history, or ictal-EEG; 4. Age £21 years. Four hundred eleven patients were excluded due to nonepileptic recorded events (217), missing data (125), age over 21 years (59), and no recorded events or seizures (10). Five hundred fifty-six patients were excluded due to presence of focal seizures based on ictal EEG recordings primarily supplemented with information from clinical history, previous EEG recordings, and magnetic resonance imaging (MRI) findings. MRI lesions were not used as supplemental information to exclude focal seizure patients from this study. A total of 77 patients with generalized seizures based on ictal EEG recordings were thus included. This work builds on and further expands data from a previously published study on 380 patients who were reviewed for semiology of seizures in generalized and focal epilepsy to evaluate for circadian patterns to these seizures (Loddenkemper et al., 2011). Continuous video-EEG monitoring and seizure semiology analysis All 77 subjects underwent continuous vEEG monitoring for a period ranging from 1–8 days (mean duration 3.0 € 1.6 days). The 10–20 international system of electrode placement was used for the EEG scalp recordings, with the additional placement of anterior temporal electrodes (American Clinical Neurophysiology Society, 1994). All video recordings were performed by digital video cameras in a closed-circuit system and were continuously monitored by dedicated EEG technologists. EEG and video data were saved and interpreted by board-certified epileptologists. Data were subsequently archived. Antiepileptic drugs (AEDs) were tapered in a patient-specific manner, with consideration of baseline seizure frequency and severity, history of status epilepticus, and indication for admission to the vEEG monitoring unit. Patients were allowed to choose their sleep and waking times, although scheduled hospital events, such as nursing and physician rounds, meals, and clinical vital sign assessments, may have interfered with their preferred schedules. A total of 316 clinical seizures were analyzed. Subclinical EEG seizures were excluded. Semiology of archived

seizures was analyzed and classified by two independent investigators (who were blinded to patient’s clinical history and EEG findings) according to the ILAE seizure semiology terminology (Berg et al., 2010). Category assignment was completed by consensus with a third electrophysiologist in rare cases of disagreement (