ORIGINAL CONTRIBUTION Reduction of Rapid Eye Movement Sleep by Diurnal and Nocturnal Seizures in Temporal Lobe Epilepsy Carl W. Bazil, MD, PhD; Luiz H. M. Castro, MD; Thaddeus S. Walczak, MD Background: Patients with brief, complex partial sei- maintenance of wakefulness test and 2 subjective drowsi- zures frequently suffer from tiredness and decreased pro- ness tests. ductivity that continue well beyond the postictal pe- riod. A possible explanation is that seizures, even when Results: Daytime seizures reduced REM from 18% ± 1% occurring during the day, disrupt sleep the following night. to 12% ± 2% (P = .003). Night seizures reduced REM from 16%±1%to6.8%±2%(P,.001). Night seizures also sig- Objective: To determine the effect of temporal lobe com- nificantly reduced stages 2 and 4 while increasing stage plex partial seizures on sleep structure and daytime 1 sleep. Night seizures, but not day seizures, signifi- drowsiness. cantly reduced sleep efficiency, increased time to first REM period, and increased drowsiness as measured by the Methods: Patients with temporal lobe epilepsy were ad- maintenance of wakefulness test. mitted for video-electroencephalography monitoring. All- night polysomnography was recorded under the follow- Conclusions: Temporal lobe complex partial seizures de- ing 3 conditions: seizure free, seizure during the day before crease REM sleep, particularly when occurring during sleep the recording, and seizure during the recording. Percent- but also when occurring on the previous day. This may, age of time in each sleep stage, sleep efficiency, and time in part, be responsible for the prolonged impairment of func- to first and second rapid eye movement (REM) period tioning that some patients report following seizures. were compared for seizure vs control conditions. Day- time drowsiness was also measured, using a modified Arch Neurol. 2000;57:363-368 PILEPTIC SEIZURES typically or during the previous day were com- last less than 2 minutes; pared with recordings in the same pa- however, patients may re- tient when no seizure occurred for at least port decreased perfor- 24 hours. By using patients as their own mance for days afterward. In controls, the effects of individual sei- Efact, 2 of the most prevalent complaints zures were examined independently of of patients with epilepsy are disturbed sleep other variables. and excessive daytime drowsiness,1 which in themselves may be sufficient to inter- RESULTS fere with patients’ ability to work or go to school. These symptoms may have a num- A total of 116 nights were recorded in 34 ber of causes. Epileptic seizures may dis- patients (1-7 nights per patient). Record- rupt sleep and be responsible for daytime ing characteristics are summarized in the drowsiness.2 Anticonvulsants may dis- Table. Our analysis used those record- rupt sleep,3-5 although their effects are vari- ings (87 recordings in 21 patients) in From the Department of able and often difficult to distinguish from which control and seizure conditions Neurology, Comprehensive the effects of seizures. Finally, the under- were recorded. Seven patients had Epilepsy Center, lying disease process causing seizures may DAYSZ and NTSZ recordings. The aver- Columbia-Presbyterian Medical be responsible for changes in sleep. age time during which recordings were Center, New York, NY In our study, all-night polysomnog- obtained was 5.9 nights (range, 2-13 (Dr Bazil); Hospital das Clinicas, São Paulo, Brazil raphy was performed in patients with in- nights). The average time from daytime (Dr Castro); and Minnesota tractable epilepsy who were admitted to seizure to start of recording was 8.5 Comprehensive Epilepsy Care an epilepsy monitoring unit to determine hours. Of the 21 patients, 18 had control (MINCEP), Minneapolis, Minn changes in sleep structure. Recordings in recordings first; 4 of these also had con- (Dr Walczak). which seizures occurred during the night trol recordings after at least 1 seizure ARCH NEUROL / VOL 57, MAR 2000 WWW.ARCHNEUROL.COM 363 ©2000 American Medical Association. All rights reserved. Downloaded From: https://jamanetwork.com/ on 09/28/2021 PATIENTS AND METHODS for sleep staging were used. Seizure and postictal epochs were not included in total sleep for our purposes. This modi- fication of the original Rechtschaffen and Kales criteria6 was To examine a relatively homogeneous population, only pa- essential, as diffuse delta typically seen after seizures is clearly tients with temporal lobe partial epilepsy (based on interic- not synonymous with any of the accepted sleep stages. Us- tal and ictal recordings) were included. Patients with known ing our method, stages 3 and 4 sleep possibly could be un- or suspected sleep disorders were excluded, although no derestimated, but it would be uncommon for patients to specific testing for sleep apnea or periodic limb move- pass directly into these stages without first entering stage ments was performed. No patient had exclusively diurnal 2. Similarly, mild slowing and attenuation seen postictally or nocturnal seizures. Patients were admitted consecu- would not be scored as stage 1 sleep, and this stage could tively to the Epilepsy Monitoring Unit at Columbia- be underestimated. Presbyterian Medical Center, New York, NY, for diagnosis The initial night of recording was not used in the analy- or surgical evaluation. Temporal onset seizures were veri- sis (to control for first-night effects)7; however, patients ad- fied by video-electroencephalographic (EEG) monitor- hered to the sleep schedule on that night. ing, and computerized seizure detection ensured that un- Control polysomnograms were defined as no seizure witnessed seizures were detected. Most patients were for at least 24 hours before sleep onset and during the re- receiving maintenance anticonvulsant therapy, although this cording. Polysomnograms following daytime seizures was typically decreased and sometimes discontinued dur- (DAYSZ condition) were defined as a seizure between 7 AM ing the admission. Patients taking or withdrawing from bar- and 11 PM on the day the recording began. Polysomno- biturate or benzodiazepine therapy were excluded (includ- grams with night seizures (NTSZ condition) were defined ing patients who received a single dose of a benzodiazepine as a seizure during the recording (after sleep onset). Pa- following a seizure cluster). Beverages containing caffeine tients were identified who had at least 1 control and 1 DAYSZ were not allowed. and/or NTSZ polysomnogram; these were used in the sub- In addition to the usual 10-20 array of scalp elec- sequent analysis. Sleep efficiency, percentage of time in trodes, patients had bilateral outer canthus electrodes and each sleep stage, time to first and second rapid eye move- chin electromyograph electrodes plus a subtemporal chain ment (REM) period, and total sleep time were calculated. of electrodes (total, 29 scalp electrodes). Seizures were di- For nights with seizures, a subanalysis was made when agnosed using video-EEG with the full scalp array. The sub- seizures occurred before or after the first REM period. All jects were not sleep deprived on the nights before record- results were compared using a paired t test vs controls. ing or during recording and were not allowed daytime naps. When more than 1 suitable recording was obtained, the Nurses instructed the patients to sleep at 11 PM and awak- results were averaged before comparisons using the ened them at 7 AM; however, precise “lights-off” times were paired t test. not recorded. Although the patients were in shared rooms Between 1 and 3 PM daily, patients were administered on a hospital ward, efforts were made to optimize sleeping 3 tests of drowsiness. Subjective measures included the Stan- conditions. During recordings, the doors of the room re- ford Sleepiness Scale (SSS),8 where the patient chooses a mained closed, the lights off, and the patients undisturbed description giving a numerical result from 1 to 7, and a lin- unless a seizure occurred. Following seizures, patients were ear analog scale of drowsiness (LASD). For the latter, pa- encouraged to return to sleep. If a benzodiazepine was given tients were asked to mark their drowsiness on a 100-mm after prolonged or repeated seizures, the night was not in- line, from alert to sleepy, yielding a result from 0 to 100. cluded in the analysis. In addition, a more objective nap test was performed that Polysomnography was scored in 30-second epochs, ac- was a modification of the maintenance of wakefulness test cording to standard technique,6 by reformatting digital EEG (MOW).9 For our MOW, patients were placed in a quiet, to polysomnographic channels and settings. Because there dark room in the supine position and instructed to stay was not always a precise lights-off time, scoring began at awake. The time to sleep was recorded (determined by 3 sleep onset (defined by 3 consecutive epochs of stage 1 or consecutive stage 1 epochs or a single epoch of another sleep 1 epoch of stage 2 sleep) and continued until awakening stage), giving a number from 0 to 20. The standard MOW in the morning by the staff. Therefore, sleep latency could includes 5 scheduled recordings in a day. The SSS and LASD not be determined, and total recording time varied some- were administered immediately before each MOW. All tests what. Sleep efficiency is generally defined as time asleep were performed on days meeting the inclusion criteria for as a percentage of time in bed (lights off to lights on). For the polysomnogram portion of the study, and therefore were this study sleep efficiency was calculated somewhat differ- not performed on the day of admission or on the follow- ently from the standard, as percentage of time asleep from ing day. The SSS, LASD, and MOW all give numerical re- sleep onset until awakening. This would likely result in sults that were compared using a paired t test. When more higher numbers, but comparisons between groups should than 1 suitable test was obtained, the results were aver- still be valid.