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Epilepsy & Behavior 11 (2007) 578–581 www.elsevier.com/locate/yebeh
Brief Communication
Peri-ictal water drinking in temporal lobe epilepsy: Is it a reliable lateralizing sign? Anna Sz} ucs a,*, Andra´s Fogarasi b, Gyo¨rgy Ra´sonyi a, Anna Kelemen a, Lalit Narula a, Vanda To´th c, Jo´zsef Janszky c, Pe´ter Hala´sz a a
Epilepsy Center, National Institute of Psychiatry and Neurology, H-1021 Budapest, Hungary b Epilepsy Center, Bethesda Children’s Hospital, H-1146-Budapest, Hungary c Department of Neurology, University of Pe´cs, H-7624 Pe´cs, Hungary Received 27 June 2007; revised 19 July 2007; accepted 21 July 2007 Available online 1 October 2007
Abstract Peri-ictal water drinking has been reported to be a lateralizing sign to the right side in temporal lobe epilepsy (TLE). As peri-ictal water drinking is relatively common in our own patients with TLE, we wanted to evaluate its lateralization value for ourselves. We reviewed the data for 55 adult patients with TLE who had undergone epilepsy surgery with a favorable postoperative outcome in our center. Eight patients exhibited peri-ictal water drinking behavior. Five of them had a left temporal and three a right temporal epileptogenic region. We also analyzed cases of peri-ictal water drinking in the literature and found that the reported data do not support this behavior as a laterality indicator. In conclusion, we could not find any evidence for the lateralization value of peri-ictal water drinking in TLE. Ó 2007 Elsevier Inc. All rights reserved. Keywords: Lateralizing sign; Temporal lobe epilepsy; Ictal drinking
In this era of epilepsy surgery, localizing and lateralizing signs offered by seizure semiology are important in presurgical evaluation [1]. Seizure semiology may also help in better learning the neural network involved in epileptic seizures and the brain localization of clinical phenomena [2]. Peri-ictal water drinking (PIWD) has been reported to have right temporal localizing value [3]. Because we ourselves have occasionally observed PIWD, we were interested in evaluating its lateralizing value in our patient population.
gone presurgical evaluation between 1992 and 2005 at the National Institute of Psychiatry and Neurology, Budapest, Hungary, and had a favorable (Engel l or 2) postoperative outcome. Age at epilepsy onset ranged from 10 months to 35 years (mean, 13.8 ± 8.5), and age at video-EEG monitoring, from 9 to 49 years (mean, 30.4 ± 10.1). Postoperative histology revealed hippocampal sclerosis (36), focal cortical dysplasia (9), tumor (9) and cavernoma (1). For each patient, there were 2–7 (mean 3.7) archived seizures. PIWD was defined as the action of drinking within 2 minutes of an electrical seizure. We also reviewed the literature using Pubmed for the expressions periictal drinking, peri-ictal water drinking, epilepsy AND drinking, and thirst AND seizure, and evaluated the cases obtained for localization and lateralization of the epileptic focus.
2. Methods
3. Results
We analyzed the archived seizures of all 55 patients (30 males, 25 females) with temporal lobe epilepsy (TLE) who had had surgery and who had under-
3.1. Our patients
1. Introduction
*
Corresponding author. Present address: Neurology Department, National Institute of Psychiatry and Neurology, Huvosvolgyi Street 116, 1021 Budapest, Hungary. Fax: +36 1 391 5438. E-mail address:
[email protected] (A. Sz} ucs). 1525-5050/$ - see front matter Ó 2007 Elsevier Inc. All rights reserved. doi:10.1016/j.yebeh.2007.07.012
PIWD was observed in one or more recorded seizures of eight patients (14.5%) in our presurgically analyzed TLE group (Table 1). All patients were right-handed. None of the patients reported water drinking as a regular element
Left temporal cavernoma 4/5 None
1/1 None
Left
118 sec after seizure onset Left
36/F
25/F
38/M
34/F
30/M
30/F
J.K.
I.B.
A.M.
J.P.
S.S.
H.I.K.
Left temporal spikes
37/F J.S.
Left anterior temporal spikes Left temporal sharp waves Bitemporal independent spikes
38/M T.K.
Right anterior temporal spikes Bitemporal > left spikes
Left temporal and frontal desynchronization and crescendo rhythm Left temporal rhythmic pattern
Left
55 s after end
None
1 /2
Left hippocampal sclerosis Left hippocampal sclerosis Left hippocampal sclerosis 4/4 None 50–54 s after onset
43–45 s after onset Left
Left
2/3
Bilateral, R > L hippocampal sclerosis MRI normal 1/3
Late (>2 min) None 40 s after onset Right
1/3 20 s 110 s after end Right
Right anterior desynchronization rhythmic activity Crecsendo right temporal rhythmic activity Left temporal desynchronization and rhythm Left temporal rhythmic crescendo pattern Left temporal theta rhythm
3/7 20 s 100–110 s after onset Right
Age at operation/ gender
Interictal EEG
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Name
Trinka and co-workers reported [3] that all seven of their TLE-patients with PIWD who were successfully operated had a nondominant temporal epileptogenic region. Because we have also observed PIWD in 14.5% of our successfully operated, video-EEG-monitored patients with TLE, we could evaluate this finding in our patient population. Of 55 adult patients with TLE in our center with a favorable postoperative outcome (Engel 1 or 2), 8 exhibited PIWD. Five of the eight had a left and three had a right temporal epileptogenic region. Consequently, in our center, we could not attribute lateralization value to PIWD. In addition, we performed a systematic analysis of the published cases in the literature, and were not convinced
Table 1 Our patients who exhibited peri-ictal water drinking
4. Discussion
Seizure pattern
Side of temporal epileptogenic region
Time at which drinking began relative to electrical seizure activity
Contralateral spread
Number of water drinking seizures/ total recorded seizures
We found a total of 27 PIWD cases in the literature (Table 2). All had TLE. The epileptogenic region in Trinka and colleagues’ patients [3], as well as that in Janszky and colleagues’ cases [5] from Epilepsy Center Bethel, Bielfeld, Germany, was determined by ictal and interictal videoEEG monitoring, as well as an excellent/favorable postoperative outcome. Trinka and co-workers’ seven patients had a right (nondominant) epileptogenic region; of Janszky and colleagues’ seven patients, four had a left and three a right temporal epileptogenic region. In another 13 published cases, owing to different levels of evidence (Table 3), the side of the temporal epileptogenic region was less clear. In 10 of these 13 cases, the highest-level neuroimaging method available to screen for an epileptogenic lesion was pneumoencephalography or analog X-ray of the skull. Three patients had MRI; one of them [6] had a right temporal tumor with temporal epileptiform EEG abnormalities. In six cases, the best EEG evidence available was an interictal EEG (not a reliable method for defining the epileptogenic region in TLE). In these patients, the EEG lateralized to the left side in two and to the right side in four. Six patients had an ictal EEG recording: four of them exhibited right temporal ictal activity, and two, a left temporal seizure pattern. Three of those cases for whom a seizure pattern was recorded also underwent video-EEG monitoring. Two of them exhibited a left temporal seizure pattern during seizures with ictal water drinking. Two patients underwent surgery: one had right temporal lobe resection for TLE with hippocampal sclerosis with an Engel 1 outcome [7,8], and in the other, an epileptogenic right frontotemporal tumor was resected [6].
Right temporal rhythmic theta
3.2. Analysis of published cases of PIWD
Independent bitemporal spike focus Right temporal sharp waves
MRI lesion
of their seizures. All patients underwent temporal lobe resection based on the presurgical evaluation: five patients had left temporal and three had right temporal lobe resections. At 2–10 years of follow-up, all operated patients were reported as having an Engel l or 2 outcome [4].
Right hippocampal sclerosis Right temporal oligoastrocytoma
Brief Communication / Epilepsy & Behavior 11 (2007) 578–581
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Table 2 Side of epileptogenic region for those patients from the literature who exhibited peri-ictal water drinking Imaging method
Interictal EEG
Crapanzano Right et al., 1993 [8] Cascino et al., Right 1989 [7]
Right hippocampal atrophy Right hippocampal sclerosis
MRI MR
Right temporal sharp waves and slowing in Right temporal drowsiness Right anterior temporal Right temporal
Not recorded Yes
Re´millard et al., Left amygdala, 1982 [9] hippocampus
Widening of the anterior horn of left temporal lateral ventricle None
PEG
Bitemporal
Left temporal (deep electrodes)
Yes
Right temporal anterior lobectomy None
PEG
Independent bitemporal
Left temporal (deep electrodes)
Yes
None
PEG:
Right temporal epileptic focus
Not recorded
Not recorded
None
PEG
Left temporal
Not recorded
None
Right temporal inferomesial electrocorticography: spike, polyspike activity over the surface of the right temporal lobe Right inferomesial temporal
Right hemispheric slow and sharp activity trains
Not recorded Not recorded
Suspected side of epileptogenic region
Left hippocampus and amygdala Right
Left frontotemporal
Widening of the anterior horn of left temporal lateral ventricle Postmeningitis
Right
Right hemispheric PEG atrophy, enlarged right lateral ventricle
Right
Right hemispheric atrophy
Analog radiogram
Right?
Left infantile hemiplegia ?
?
Left Right inferiomesial, anterior Right
?
Seizure pattern
VideoOperation EEG monitoring
Not recorded
None
Right centrotemporoparietal dysfunction without epileptogenic activity Left temporal and anterior Sylvian Not recorded disturbance, no sharp waves, no spikes Epileptogenic activity over the inferomesial Not recorded surface of the right temporal lobe
Not recorded Not recorded Not recorded
None
Not recorded
Right temporal
Not recorded Not recorded Yes
Minimal dilation of left PEG lateral ventricle, smaller left hemicranium ? Analog Right anterior and temporal focus radiogram Right frontotemporal Right temporal epileptic abnormality tumor Yes
Ictal EEG started during seizure: generalized rhythmic theta, some sharp waves and delta from right frontotemporal area Not recorded
Despland et al., 1985 [6] Trinka et al., 2003 [3]
Right
Janszky et al., 2007 [5]
3 Right
Yes
Right temporal
Yes
4 Left
Yes
Left temporal
Yes
7 Right
None
Not recorded
None None
None Operation of the tumor Right temporal resection Right temporal resection Left temporal resection
Brief Communication / Epilepsy & Behavior 11 (2007) 578–581
Cerebral lesion
Author
Brief Communication / Epilepsy & Behavior 11 (2007) 578–581 Table 3 Analysis of the 27 published cases with respect to the highest level of evidence for the side of temporal lobe epileptogenic region Level of evidence
All published cases: 27
Right temporal
Left temporal
Interictal EEG Ictal EEG:video-EEG monitoring Epilepsy surgery
6 6:3
4 4:1
2 2:2
15
10
4
of the lateralizing value of PIWD. Our findings, as well as those of Re´millard and colleagues [9] suggesting a random right or left temporal origin of ictal drinking, seem to be in agreement with physiological studies on central fluid control indicating a midline thirst-controlling system [10]. We cannot explain the difference between our reseults and those of Trinka and colleagues. The fast contralateral propagation in some patients may be an explanation, because in cases of quick contralateral spread, the laterality of any semiological element may be unclear. We observed rapid (<20 seconds) contralateral spread in two of our patients with a primary right temporal seizure onset. In these cases, it is uncertain which of the two involved temporal lobes generated the PIWD. Another explanation for the contradictory data might be that the numbers of patients in these studies were too small. A well-powered study involving more patients can resolve this problem.
Conflicts of interest statement Herewith we state that no author has a conflict of interest.
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Acknowledgements The authors thank the Hungarian Neuroimaging Foundation and the Hungarian Research Council (ETT219/ 2006), and the OTKA (OTKA F68720) for their financial support. J.J. and A.F. were supported by the Bolyai Fellowship. A.F. was supported by Grant D 048517 from the Hungarian Scientific Research Fund. We confirm that we have read the Journal’s position on issues involved in ethical publication and affirm that this report is consistent with those guidelines. References [1] Loddenkemper T, Kotagal P. Lateralizing signs during seizures in focal epilepsy. Epilepsy Behav 2005;7:1–17. [2] Penfield W. Epilepsy, the great teacher: the progress of one pupil. Acta Neurol Scand 1967;43:1–10. [3] Trinka E, Walser G, Unterberger I, et al. Peri-ictal water drinking lateralizes seizure onset to the nondominant temporal lobe. Neurology 2003;60:873–6. [4] Engel Jr J, Van Ness P, Rasmussen TB, Ojemann LM. Outcome with respect to epileptic seizures. In: Engel Jr J, editor. Surgical treatment of the epilepsies. New York: Raven Press; 1993. p. 609–21. [5] Janszky J, Fogarasi A, Toth V, et al. Peri-ictal vegetative symptoms in temporal lobe epilepsy. Epilepsy Behav 2007;11:125–9. [6] Despland PA, Rousselle J, Regli F. Electroclinical study of partial complex epilepsy: paroxysmal need to drink. Rev Electroencephalogr Neurophysiol Clin 1985;14:293–6. [7] Cascino GD, Sutula TP. Thirst and compulsive water drinking in medial basal limbic epilepsy: an electroclinical and neuropathological correlation. J Neurol Neurosurg Psychiatry 1989;52:680–1. [8] Crapanzano KA, Casanova MF, Toro VE, Gallagher B. Drinking behavior as a result of right hippocampal ictal focus. Biol Psychiatry 1993;15:889–92. [9] Re´millard GM, Andermann F, Gloor P, Olivier A, Martin JB. Water drinking as ictal behavior in complex partial seizures. Neurology 1982;31:117–24. [10] Denton D, Shade R, Zamarippa F, et al. Correlation of regional cerebral blood flow and change of plasma sodium concentration during genesis and satiation of thirst. Proc Natl Acad Sci USA 1999;96:2532–7.