Lateralizing value of early head turning and ictal dystonia in temporal lobe seizures: a video-eeg study

Transcription

1 Seizure 2001; 10: doi: /seiz , available online at on Lateralizing value of early head turning and ictal dystonia in temporal lobe seizures: a video-eeg study HSIANG-YU YU, CHUN-HING YIU, DER-JEN YEN, CHIEN CHEN, YUH-CHERNG GUO, SHANG-YEONG KWAN, YUNG-YANG LIN & YANG-HSIN SHIH Departments of Neurology; Neurosurgery, The Neurological Institute,Taipei Veterans General Hospital and School of Medicine, National Yang-Ming University Correspondence to: Der-Jen Yen, MD, Department of Neurology, The Neurological Institute, Taipei Veterans General Hospital, 201 Sec.2, Shih-pai Road, Shih-pai, Taipei, Taiwan (ROC). vw1937@ms14.hinet.net To investigate early head turning, we retrospectively studied videotapes of 262 seizures from 82 patients who were seizure free after temporal lobectomy. Early head movements were arbitrarily classified into non-tonic turning, tonic turning, and absence of turning. Among the 222 seizures which showed early head turning, 168 (75.7%) had non-tonic turning and 54 (24.3%) had tonic turning. The direction of the first head turning was ipsilateral to the epileptogenic foci in 132 (78.6%) seizures with non-tonic turning and in 35 (64.8%) seizures showing tonic head turning. The proportion of seizures with turning towards the ipsilateral side in the presence of tonic and non-tonic head turning were significantly different (P= 0.04). Seventy-four seizures (28.2%) evolved to secondary generalization, more frequently found in seizures with early head turning (P= ) and especially those showing tonic turning (P< ). The direction of head turning immediately preceding secondary generalization was contralateral to the lesion side in 53 seizures (82.8%). Dystonic upper limb posturing occurred in 86 seizures (32.8%), exclusively contralateral to the seizure focus, whereas 65 (75.6%) were associated with initial head turning ipsilateral to the focus. In summary, temporal lobe seizures with tonic head turning tends to secondarily generalize and the direction of head turning before secondarily generalized was contralateral to the seizure foci. Earlier in the seizures the direction of non-tonic head turning tends to be towards the epileptogenic hemisphere. In addition, dystonic posturing of the extremities is a significant lateralizing sign to the contralateral hemisphere in temporal lobe seizures. c 2001 BEA Trading Ltd Key words: complex partial seizures; head turning; ictal dystonia; temporal lobe epilepsy; temporal lobectomy; video-eeg monitoring. INTRODUCTION Ictal manifestations of complex partial seizures (CPS) were diverse, and likely different among and within patients. In the literature, several clinical manifestations or automatisms in partial seizures including temporal lobe epilepsy (TLE) were reported to have reliable localizing or lateralizing values 1 6. These manifestations included ictal speech, post-ictal dysphasia, dystonic limb posturing, unilateral hand automatisms, ictal vomiting, unilateral eyelid blinking, and versive head and eye turning Head turning was not infrequent in seizures, however, its significance, when compared with other clinical manifestations, varied greatly across studies In some reports, the direction of head turning did not provide reliable lateralization as to the side of seizure onset 12, 15, 16, while in others the direction of versive (tonic) or non-versive (non-tonic) head turning showed good correlation to the epileptogenic side 8, 19, 20, 24. In this study, we evaluated the lateralizing value of head turning in seizures of temporal lobe origin. Seizures were captured during continuous video-electroencephalogram (EEG) monitoring that allowed precise correlation between clinical manifestations and EEG changes. In addition, only patients who underwent temporal lobectomy and had been seizure free were included. This inclusion criterion assured that the seizure foci have been accurately localized and removed. We also tried to analyse whether head turning could correlate with pathology findings in the temporal lobe /01/ $35.00/0 c 2001 BEA Trading Ltd

2 Head turning in temporal lobe epilepsy 429 MATERIALS AND METHODS Patients The population studied included adult Chinese patients who underwent anterior temporal lobectomy (ATL) for treatment of medically intractable TLE at Taipei Veterans General Hospital between August 1990 and August Only patients who had remained seizure-free post-operatively for 2 years or longer were included (Engel s classification I) 25. Pre-surgical evaluation The pre-surgical evaluation included continuous video-eeg monitoring with scalp and sphenoid electrodes, brain magnetic resonance imaging, singlephoton emission computed tomography (SPECT), positron emission tomography, neuropsychological testing, and the intracarotid amobarbital test. Foramen ovale electrodes were implanted in six patients and subdural electrodes in one patient who had ambiguous temporal lobe onset. Selection for ATL was based on congruence of the above data. Tailored temporal lobectomy was performed under general anaesthesia guided by intra-operative electrocorticography and recording from depth electrodes aimed freehand at the amygdala and hippocampus. Resected specimens from all patients were sent for pathological analysis. Seizures Seizure videotapes were reviewed by one of the authors (HY Yu) who did not participate in the presurgical evaluation of patients and was blind to the side of surgical resection and neuropathological diagnosis. All seizures occurred during or after acute withdrawal of antiepileptic drugs. We included only CPS with semiology and EEG findings comparable to CPS of temporal lobe onset established by the International Classification of Epilepsies and Epileptic Syndromes 1. Simple partial seizures or non-habitual seizures were not included for analysis. The interictal and ictal EEG changes were printed on EEG paper and reviewed by visual analysis (DJ Yen and CH Yiu). Clinical seizure onset was defined as the initial appearance of blank staring, automatisms, abnormal movements or reaction to the environment, or the push-button event if the patient had a warning. Initiation of the ictal EEG patterns consisted of either attenuation or semirhythmic to rhythmic discharges arising from the temporal electrodes with or without epileptiform morphological features. Clinical manifestations of interest including head turning were marked on the EEG paper, so their time lags to the EEG and clinical onsets could be determined. Ictal clinical manifestations We analysed initial head turning which implied the direction of the first head turning because the patient might sometimes turn his/her head to both sides during this period. In this study, we arbitrarily defined early head turning as active movements of the head and neck occurring in the first 30 s of seizures, which were carried through a range of 15 degrees and lasted 3 s. Accordingly, the following three categories may encompass ictal head movements: (1) Tonic head turning (versive) indicated an unquestionably forced head deviation, resulting in a sustained unnatural positioning of the head. (2) Non-tonic head turning (non-versive) was a mild and wandering movement that was not sustained and may be seemingly voluntary. (3) Absence of head turning could be due to either symmetric tonic neck contraction resulting in no obvious head turning or absence of head movement at all. The direction of head turning immediately preceding secondary generalization was also assessed in all seizures that secondarily generalized. Dystonic posturing of the extremities was characterized by a sustained, unnatural hand posturing with forced flexion or extension of the fingers along with a rotatory component in the wrist and elbow with or without shoulder involvement. Eye deviation was not included in this study because it could not be easily observed from the videotapes. Statistical analysis The chi-square test was used for comparison of the lateralizing value of tonic and non-tonic head turning and the tendency to secondary generalization. The Kruskal Wallis test was used to evaluate the significance of the time lag of initial head turning in different groups of patients. A P value of <0.05 was considered as significant. RESULTS Patients In all, 82 TLE patients had 262 seizures for analysis (mean 3.2 seizures per patient). There are 51 men and 31 women, aged years (mean 29.9 years), with a

3 430 Hsiang-Yu Yu et al. mean seizure history of 16.4 years. Forty-one patients had right ATL (139 seizures) and 41 patients had left ATL (123 seizures). Pathological diagnosis revealed hippocampal sclerosis in 72 patients (87.8%) and lesional in 10 patients. The latter included two with arteriovenous malformations and eight with tumours. Direction of head turning Early head turning occurred in 222 seizures (84.7%) from 77 patients (Table 1). These episodes included non-tonic turning in 168 seizures (75.7%) from 69 patients and tonic turning in 66 seizures from 31 patients. The latter included 12 tonic turning being preceded by non-tonic turning. Forty seizures (15.3%) were categorized in the group containing patients with the absence of head turning. Table 1: Early head turning in temporal lobe seizures from patients who were seizure-free after temporal lobectomy. Seizure focus Right temporal lobe Left temporal lobe (139 seizures) (123 seizures) Head turning/ initial direction Right Left Right Left Non-tonic 71 (18) 19 (1) 17 (8) 61 (11) Tonic 13 (10) 14 (11) 5 (1) 22 (11) Immobile 22 (2) 18 (1) Numbers in parentheses are the number of seizures that secondarily generalized. Among 168 seizures with non-tonic head turning (Table 1), 132 (78.6%) had initial turning ipsilateral to the epileptogenic focus. While in the tonic group, 64.8% had initial head turning ipsilateral to the epileptogenic focus and 35.2% contralateral to the side of focus. Non-tonic head turning appeared to have a better lateralizing value than the tonic head turning (P= 0.04). Head turning and secondary generalization Seventy-four seizures (28.2%) secondarily generalized in this study. Seizures with early head turning, either tonic or non-tonic, showed a higher tendency (71/222) to secondarily generalize as compared to seizures (3/40) without head turning ( P= ). In addition, seizures with tonic head turning (33/54) tend to secondarily generalize more easily than seizures with non-tonic head turning (38/168) ( P< ). Furthermore, the direction of head turning occurring immediately before secondary generalization was contralateral to the epileptogenic focus in 53 seizures (82.9%) out of 64 seizures that have clearly identified turning. Dystonic posturing of extremities Eighty-six seizures (32.8%) demonstrated dystonic posturing of the extremities, which were exclusively unilateral and contralateral to the epileptogenic focus. Among these, 65 seizures (52 non-tonic and 13 tonic) (75.6%), showed initial head turning contralateral to the side of the dystonic extremities or ipsilateral to the epileptogenic focus. Relation between head turning and neuropathological findings The occurrence ratio of tonic or non-tonic head turning in seizures from patients with hippocampal sclerosis is not significantly different from that in the lesional group (P= 0.995) (Table 2). Latency of the initial head turning The time latency for the initial head turning to the clinical onset did not show a significant difference between tonic and non-tonic seizures, regardless of etiologies. In non-tonic head turning, the average time was 6.33 ± 5.94 s vs ± 3.58 s for ipsilateral turning and contralateral turning, respectively. In tonic head turning it was 6.96 ± 5.34 s vs ± 5.19 s for ispilateral turning and contralateral turning, respectively. DISCUSSION The occurrence of head turning varied greatly among patients with different seizure patterns or foci 12 24, There were no unique definitions of head turning in these reports, some even lack clear definitions 15, 26, 29. In this study we enrolled only patients who had undergone ATL with favourable outcome. These inclusion criteria ensured that the epileptogenic foci had been removed and the correlation between foci and early head turning movement were accurate. In this study, early head turning occurred in 84.7% of seizures of temporal lobe origin. This figure was not very different from 78.2% of all seizures presenting head turning by Fakhoury and Aboul-Khalil 24 using similar definitions in 32 TLE patients who became seizure free after temporal lobectomy. Regarding lateralizing value of head turning, patients with partial epilepsy of temporal and extratemporal origin, including frontal and parieto-occipital

4 Head turning in temporal lobe epilepsy 431 Table 2: Early head turning in seizures from patients of temporal lobe epilepsy with different etiologies. Seizure focus Right temporal lobe Left temporal lobe (139 seizures) (123 seizures) HS (122) Lesional (17) HS (106) Lesional (17) Head turning/ R L R L R L R L initial direction Non-tonic Tonic Immobile HS: hippocampal sclerosis, lesional: arteriovenous malformation and tumours, L: left, R: right. focus, no localizing or lateralizing significance was noted for non-versive head turning or slight head rotation 15, 17. In studies with TLE patients, nonetheless, non-tonic head turning showed a 50% to 80% positive predictive value for lateralizing the seizure focus 20, 22. Fakhoury and Aboul-Khalil 24 reported that 162 from 187 temporal lobe seizures (87%) first displayed head turning ipsilateral to the focus (94% in the first 30 s). However, the patterns of head turning were not clearly described, both tonic and non-tonic head turning were taken into consideration together. We demonstrated that non-tonic early head turning had a trend to predict an ipsilateral seizure focus in 78.6% of temporal lobe seizures. Explanations for non-tonic head turning included a response to a stimulus or aura 20. Ipsilateral turning may be due to inhibition of the ipsilateral hemisphere by ictal discharges and subsequently relative attentional and motor predominance of the contralateral hemisphere 19, 20, 23, 24. Whether initial tonic head turning has lateralizing value in partial epilepsy was also controversial. In patients with TLE, however, some studies strongly favoured initial tonic head turning as a sign of contralateral seizure focus 17, 20, 22. In our study, initial tonic head turning occurred less frequently and had a less lateralizing value compared with non-tonic head turning. Our results echoed the report of Marks et al. 28 who studied patients who underwent temporal lobectomy with favourable outcomes and showed that versive head turning at anytime during partial seizure predicted 60% contralateral focus. Furthermore, in depth electrode EEG study, the incidence of ipsilateral and contralateral tonic head turns was almost even while ictal discharges were strictly confined to one temporal lobe 12. We also found that seizures with early tonic turning had a tendency to evolve to secondary generalization, and the direction of tonic head turning that immediately preceded secondary generalization was always contralateral to the seizure focus. Similar conclusions have been reported in other studies 19, 25, 28. Only a few studies in the literature mentioned time latency of head turning with varied results 2, 8, 20, 24. Chee et al. and Bleasel et al. 8, 20 found that version appeared earlier in the extratemporal group than the TLE group. In patients with TLE, ipsilateral head turning occurred earlier than contralateral first head turning 24. However, we found no difference in time latency between ipsilateral and contralateral head turning. The discrepancy could be related to different observation time; Fakhoury and Aboul-Khalil 24 also included later head turning which occurred 375 s after clinical seizure onset and most of the contralateral turning occurred 30 s after seizure onset. Dystonic posturing occurred in 32.8% of seizures in our patients, which was exclusively unilateral and contralateral to seizure focus as in previous reports 7 9, 23. This phenomenon has been widely regarded as the single most reliable lateralizing sign in TLE and is well explained by ictal hyperperfusion in the ipsilateral basal ganglia 23. In our study, three quarters (75.6%) of seizures with dystonic posturing were associated with initial head turning contralateral to the dystonic extremities, or ipsilateral to the seizure focus. Fakhoury et al. mentioned the high coincidence of dystonic posturing with head turning in their patients (79%) and cited animal experiments, including high-frequency stimulation and dopaminergic response studies, to support the role of caudate nucleus and putamen involvement and particularly, fronto-striatal connections in the genesis of concomitant dystonic posturing and ipsilateral or contralateral head turning 24. Saygi et al. 2 also attributed ipsilateral or contralateral head turning to the spread of ictal discharges to the hippocampus or amygdala, respectively. There was no differences in the occurrence rate of ipsilateral or contralateral head turning in patients with hippocampal sclerosis or tumours in the temporal lobe in Saygi s study 2. However, the patients with tumours were much more likely to present contralateral head turning in the first 5 s of seizure. This observation indirectly implied that the tumour etiology could be in favour of an early amygdalar ictal spread. In our patients, different etiologies in the temporal lobe did not seem to considerably affect the spreading of ictal

5 432 Hsiang-Yu Yu et al. discharges to either the basal ganglia or frontal lobe because there were no significant difference in the occurrence of head turning or latency in either group of patients. Traditionally, head turning has been interpreted as a lateralizing sign contralateral to the direction of turning. However, our findings suggest that head turning has a lateralizing value to the contralateral hemisphere only when immediately preceding secondary generalization, as reported by Kernan et al. 19 and Fakhoury and Aboul-Kahlil 24. Otherwise, the direction of head turning tends to be towards the epileptogenic hemisphere, particularly if head version is non-tonic. In contrast, dystonic posturing of the extremities is a significant lateralizing sign to the contralateral hemisphere in temporal lobe seizures. ACKNOWLEDGEMENTS This study was supported in part by a grant from Taipei Veterans General Hospital and Yen Tjing Ling Medical Foundation. We thank Wen-Yung Sheng for her invaluable assistance in our statistical analysis. REFERENCES 1. Commission on Classification and Terminology of the International League Against Epilepsy. Proposal for revised classification of epilepsies and epileptic syndromes. Epilepsia 1989; 30: Saygi, S., Spencer, S. S., Scheyer, R., Katz, A., Mattson, R. and Spencer, D. D. Differentiation of temporal lobe ictal behavior associated with hippocampal sclerosis and tumors of temporal lobe. Epilepsia 1994; 35: Salanova, V., Morris, H. H., Van Ness, P., Kotagal, P., Wyllie, E. and Lüders, H. Frontal lobe seizures: Electroclincial syndrome. Epilepsia 1995; 36: Williamson, P. D., Spencer, D. D., Spencer, S. S., Novelly, R. A. and Mattson, R. H. Complex partial seizures of frontal lobe origin. Annals of Neurology 1985; 18: Delgado-Escueta, A. V. and Walsh, G. O. Type I complex partial seizures of hippocampal origin: excellent results of anterior temporal lobectomy. Neurology 1985; 35: Maldonado, H. M., Delgado-Escueta, Walsh, G. O., Swartz, B. E. and Rand, R. W. Complex partial seizures of hippocampal and amygdalar origin. Epilepsia 1988; 29: Kotagal, P., Lüders, H., Morris, H. H. et al. Dystonic posturing in complex partial seizures of temporal lobe onset: A new lateralizing sign. Neurology 1989; 39: Bleasel, A., Kotagal, P., Kankirawatana, P. and Rybicki, L. Lateralizing value semiology of ictal limb posturing and version in temporal lobe and extratemporal epilepsy. Epilepsia 1997; 38: Yen, D. J., Yu, H. Y., Yiu, C. H., Shih, Y. H., Kwan, S. Y. and Su, M. S. The lateralizing value of upper extremity movements in complex partial seizures of temporal lobe origin: a video- EEG study. Journal of Epilepsy 1998; 11: Benbadis, S. R., Kotagal, P. and Klem, G. H. Unilateral blinking: A lateralizing sign in partial seizures. Neurology 1996; 46: Gabr, M., Lüders, H., Dinner, D., Morris, H. and Wyllie, E. Speech manifestation in lateralization of temporal lobe seizures. Annals of Neurology 1989; 25: Quesney, L. F. Clinical and EEG features of complex partial seizures of temporal lobe origin. Epilepsia 1986; 27 (Suppl. 2): S27 S Quesney, L. F., Constain, M., Fish, D. R. and Rasmussen, T. The clinical differentiation of seizures arising in the parasagittal and anterolaterodorsal frontal convexities. Archives of Neurology 1990; 47: Ferrier, C. H., Engelsman, J., Alarcón, G., Binnie, C. C. and Polkey, C. E. Prognostic factors in presurgical assessment of frontal lobe epilepsy. Journal of Neurology, Neurosurgery and Psychiatry 1999; 66: Robillard, A., Saint-Hilaire, J. M., Mercier, M. and Bouvier, G. The lateralizing and localizing value of adversion in epileptic seizures. Neurology 1983; 33: Ochs, R., Gloor, P., Quesney, F., Ives, J. and Olivier, A. Does head-turning during a seizures have lateralizing or localizing significance? Neurology 1984; 34: Wyllie, E., Lüders, H., Moris, H. H., Lesser, R. P., Dinner, D. S. and Goldstick, L. The lateralizing significance of versive head and eye movements during epileptic seizures. Neurology 1986; 36: McLachlan, R. S. The significance of head and eye turning in seizures. Neurology 1987; 37: Kernan, J. C., Devinsky, O., Luciano, D. J., Vazquez, B. and Perrine, K. Lateralizing significance of head and eye deviation in secondary generalized tonic-clonic seizures. Neurology 1993; 43: Chee, M. W. L., Kotagal, I. P., Van Ness, P. C., Gragg, L., Murphy, D. and Lüders, H. Lateralizing signs in intractable partial epilepsy: blinded multiple-observer analysis. Neurology 1993; 43: Jayakar, P., Duchowny, M., Resnick, T. and Alvarez, L. Ictal head deviation: lateralizing significance of the pattern of head movement. Neurology 1992; 42: Serles, W., Pataraia, E., Olbrich, A., Aull, A., Lehrner, J., Leutmezer, F., Deecke, L. and Baumgartner, C. Clinical seizures lateralization in mesial temporal lobe epilepsy. Difference between patients with unitemporal and bitemporal interictal spikes. Neurology 1993; 50: Newton, M. R., Berkovic, S. F., Austin, M. C., Reutes, D. C., Mckay, W. J. and Bladin, P. F. Dystonic, clinical lateralization and regional blood flow changes in temporal lobe seizures. Neurology 1992; 42: Fakhoury, T. and Aboul-Khalil, B. Association of ipsilateral head turning and dystonia in temporal lobe seizures. Epilepsia 1995; 36: Engel, J. Outcome with respect to epileptogenic seizures. In: Surgical Treatment of the Epilepsies. 2 nd Edition (Ed. J. Engel). New York, Raven Press, 1993: pp O Brien, T. J., Kilpatrick, C., Murrie, V., Vogrin, S., Morris, K. and Cook, M. J. Temporal lobe epilepsy caused by mesial temporal sclerosis and temporal neocortical lesions. A clinical and electroencephalographic study of 46 pathologically proven cases. Brain 1996; 119: Williamson, P. D., Thadani, V. M., French, J. A., Darcey, T. M., Mattson, R. H., Spencer, S. S. and Spencer, D. D. Medial temporal lobe epilepsy: videotape analysis of objective clinical seizure characteristics. Epilepsia 1998; 39: Marks, W. J. and Laxer, K. D. Semiology of temporal lobe seizures: value in lateralizing the seizure focus. Epilepsia 1998; 39: Niaz, F. E., Abou-Khalil, B. and Fakhoury, T. The generalized tonic-clonic seizure in partial versus generalized epilepsy: semiologic differences. Epilepsia 1999; 40: Lieb, J. P., Dasheiff, R. M. and Engel, J. Role of the frontal lobes in the propagation of mesial temporal seizures. Epilepsia 1991; 32: