Ictal dystonic posturing in mesial versus neocortical temporal lobe seizures

Ictal dystonic posturing in mesial versus neocortical temporal lobe seizures

Seizure (2005) 14, 269—273 www.elsevier.com/locate/yseiz Ictal dystonic posturing in mesial versus neocortical temporal lobe seizures ¨rner a, H. St...

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Seizure (2005) 14, 269—273

www.elsevier.com/locate/yseiz

Ictal dystonic posturing in mesial versus neocortical temporal lobe seizures ¨rner a, H. Stefan b, E. Ott a A. Holl a,*, M. Feichtinger a, E. Ko a b

Department of Neurology, Medical University of Graz, Auenbruggerplatz 22, 8036 Graz, Austria Department of Neurology, University of Erlangen-Nuremberg, Germany KEYWORDS Dystonic posturing; Temporal lobe epilepsy; Ictal seizure spread

Summary Purpose: Ictal contralateral dystonic posturing is a frequently observed clinical feature in temporal lobe seizures. It is generally interpreted as the result of spread of the ictal discharge into basal ganglia structure. In previous reports, analysing ictal behavior, a precise definition and description of the upper limb ictal dystonia is often lacking or contradictory. In our study we aimed to determine whether different subtypes of dystonia and their latency from the clinical onset of seizure might be of value for the differentiation between mesial temporal lobe epilepsy (MTLE) and neocortical temporal lobe epilepsy (NTLE). Methods: Eighty seizures (51 MTLE and 29 NTLE) and 30 patients (20 MTLE and 10 NTLE) were analyzed with regard to dystonic posturing of the upper limb. Ictal dystonia was subdivided into different subtypes according to distinct clinical features. Their frequency and latency from the clinical onset of seizure were assessed. Results: Frequencies of all subtypes were similar in MTLE and NTLE. Concerning the latencies contralateral dystonic posturing characterized by sustained muscle contractions with flexion of the wrist and fist closure, a frequently appearing feature, occurred significantly earlier in NTLE than in MTLE seizures. Conclusions: This difference between the two groups may provide a differentiation between an epileptic focus of mesial from neocortical temporal lobe origin. # 2005 BEA Trading Ltd. Published by Elsevier Ltd. All rights reserved.

Introduction Analysis of ictal behavior is an important investigative procedure in presurgical evaluation of epilepsy. It provides lateralization and localization of the seizure onset as well as a better understanding of seizure propagation in temporal lobe epilepsy (TLE). * Corresponding author. Tel.: +43 316 385 3137; fax: +43 316 385 3895. E-mail address: [email protected] (A. Holl).

In clinical practice, dystonic posturing of the upper limb, occurring more often contralateral to the epileptogenic focus, is a common clinical feature in complex partial seizures of temporal lobe origin.1,2 Several reports underline this diagnostic value of ictal dystonia, but the definition and description of dystonia varies considerably.2—4 The common accepted interpretation for the underlying pathophysiological basis of the development of ictal dystonic posturing is a spread of the ictal discharge into the basal ganglia structures.2,4

1059-1311/$ — see front matter # 2005 BEA Trading Ltd. Published by Elsevier Ltd. All rights reserved. doi:10.1016/j.seizure.2005.03.001

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In recent studies, dystonia–—not of epileptic origin but due to different lesions within the basal ganglia structures–—could be further classified according to their clinical appearance.5,6 The question arises whether certain dystonic features during an epileptic seizure might also be of clinical value for seizure focus localization, e.g. for differentiation between mesial temporal lobe epilepsy (MTLE) and lateral neocortical temporal lobe epilepsy (NTLE). The aim of this study, therefore, was to assess precisely different subtypes of the upper limb ictal dystonic posturing. Seizures of patients with mesial and neocortical temporal lobe epilepsy were analysed with respect to all subtypes of ictal dystonia. Frequency of occurrence and latency from the clinical onset of seizure were then compared in both patient groups. In other words, we aimed to evaluate whether clinical analysis of different features of ictal dystonic posturing may be of importance for differentiation between mesial versus neocortical temporal lobe epilepsy.

Materials and methods The study population consisted of 20 patients with MTLE and 10 patients with NTLE who underwent preoperative evaluation for intractable seizures between 1999 and 2003 in two epilepsy centers: Department of Neurology Epilepsy Unit, University of Graz, Austria; and Department of Neurology Center for epilepsy, University of Erlangen-Nuremberg, Germany. All patients underwent complete presurgical evaluation, including medical, neurological, and neuropsychological examination; video-EEG monitoring; brain MRI and interracial SPECT examination. The presurgical evaluation (including the MR criteria for hippocampal sclerosis) were the same in both centers. MTLE patients: The diagnosis of MTLE was based on surface EEG recordings consistent with medial temporal lobe seizure onset and on neuroimaging criteria of hippocampal sclerosis diagnosed on MRI without any other structural abnormalities. The MTLE group consisted of 12 men and 8 women (mean age 34 years). The diagnosis of NTLE was based on intracranial recordings with depth electrodes. Seven men and 3 women (mean age 35 years) met these criteria. All patients underwent epilepsy surgery after presurgical evaluation (11 patients, standard anterior temporal lobectomy; 19 patients, tailored temporal lobe resection), postoperative outcome was evaluated according to the Engel classification.

A. Holl et al.

After surgery all patients presented good outcome (Engel class 1 or 2) for at least 2 years. The symptomatology (analysis of the video recordings) and ictal EEG were repeatedly reviewed for the occurrence of dystonic posturing of the upper limb during the seizures of these patients by one auther (A.H.). If there was uncertainity according the type of dystonic posturing or the latency of occurrence of dystonia the findings were then reviewed by a second author (M.F.). If there was disagreement the recording was reviewed by the two authors simultaneously and a consensus obtained. Dystonic posturing was defined according to the Ad Hoc Committee (1984) as a syndrome dominated by sustained muscle contractions, frequently causing twisting and repetitive movements, or abnormal postures.7 According to the observed phenomenology of dystonic posturing in our study we divided ictal dystonia into one group characterized by sustained muscle contractions (Type I) and another group with predominance of myoclonic jerks during dystonia (Type II). Both groups were further subdivided according to posturing of the distal joints: (i) with abduction of the thumb, (ii) with flexion of the wrist and fist closure, and (iii) with hyperextension of all fingers. Thus, in total, ictal dystonic phenomenology was subdivided into six subtypes (Type I (A— C) and Type II (A—C), see Table 1). Two to six seizures per patient were analysed. Subtype of dystonia as well as side and latency from ictal onset (in seconds) was determined in all seizures separately. Clinical ictal onset was defined as the moment of initial recognition of an aura or of the first evidence of abnormal movement or altered responsiveness. A total of 80 seizures were analyzed (51 in the MTLE group and 29 in the NTLE group).

Statistical analysis Statistical analysis was done using SPSS 9.0. For comparisons of each evaluated subtype of dystonic posturing it was averaged for the seizures in which it occurred in an individual, and the groups were then Table 1 Clinical subtypes of ictal dystonic posturing of the upper limb. Type I: Sustained muscle contractions A: with abduction of the thumb B: with flexion of the wrist and fist closure C: with hyperextension of all fingers Type II: Myoclonic dystonia A: with abduction of the thumb B: with flexion of the wrist and fist closure C: with hyperextension of all fingers

Ictal dystonic posturing in mesial versus neocortical temporal lobe seizures

compared using Fisher’s exact test. For comparison of latencies of each subtype of dystonic posturing in NTLE and MTLE one-way analysis of variance (ANOVA) was used. Statistical significance was assumed when a < 0.05.

Results Dystonic posturing of the upper limb was generally a frequently observed feature in both groups. It was present in 39 of 51 MTLE seizures (77%) and in 28 of 29 NTLE seizures (97%). It was mostly observed contralateral to the seizure focus determined by EEG: in 69% of MTLE seizures and 90% of NTLE seizures. Concerning the six subtypes of contralateral dystonic posturing of the upper limb the most frequently observed subtype was dystonia with sustained muscle contractions combined with flexion of the wrist and fist closure (Type IB) (total 47 seizures (77%), MTLE: 28 seizures (88%), NTLE: 19 seizures (73%)). This dystonic pattern occurred with a high constancy in a given patient; 17 patients presented this pattern and it could be found in 80—100% of their analysed seizures. Dystonia with sustained muscle contractions in combination with abduction of the thumb (Type IA) or hyperextension of all fingers (Type IC) was never observed in any seizure of the two patient groups. Compared to dystonia with sustained muscle contractions, dystonic posturing predominated by myoclonic jerks was rarely observed in our analyses and frequencies of its subtypes (abduction of the thumb (Type IIA), flexion of the wrist and fist closure (Type IIB) and hyperextension of all fingers (Type IIC), respectively) were equally distributed (see Table 2). There were, in general, no significant differences between MTLE and NTLE concerning the frequencies of all six subtypes of ictal dystonia.

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In contrast comparison of mean latencies of contralateral sustained dystonic posturing including flexion of the wrist and fist closure (Type IB) between MTLE and NTLE seizures resulted in a statistically significant difference (mean latencies: 19 s and 7 s, respectively; p = 0.001). There were no significant differences between the groups concerning the latencies of the other five subtypes of dystonic posturing.

Discussion A precise description of the seizure symptomatology may be useful to receive reliable information about the site of seizure onset as well as seizure spread. In clinical practice, ictal dystonic posturing of the upper limb contralateral to the epileptogenic focus is usually considered as a frequently observed feature during seizures of temporal lobe origin.1,2,4,8 In the present study the phenomenology of the upper limb ictal dystonia was analyzed, subdivided into six subtypes according different clinical features and the latency of each subtype was evaluated. In our analyses unilateral contralateral dystonic posturing characterized by sustained muscle contractions, a frequently appearing feature, occurred significantly earlier in NTLE than in MTLE seizures. Comparison of all other subtypes of ictal dystonic posturing did not show any important difference–— neither in frequency nor in latency–—between both patient groups. Little is known about symptomatic dystonia observed during epileptic seizures. Previous subdural recordings and SPECT studies support the hypothesis that unilateral ictal dystonic posturing is caused by the spread of ictal discharges into the ipsilateral subcortical basal ganglia structures.2,4 Also, recent PET studies suggest that the basal ganglia are involved in the generation of ictal dystonic

Table 2 Results of ictal contralateral dystonic posturing of the upper limb. Clinical features

MTLE

NTLE

Number of patients (n = 14)

Number of seizures (n = 35)

Mean latency (s)

Number of patients (n = 9)

Number of seizures (n = 26)

Mean latency (s)

Type I A B C

0 11 (78%) 0

0 28 (80%) 0

0 19* 0

0 6 (66%) 0

0 19 (73%) 0

0 7* 0

Type II A B C

1 (7%) 1 (7%) 1 (7%)

3 (9%) 2 (6%) 2 (6%)

10 9 29

2 (22%) 0 1 (11%)

5 (20%) 0 2 (8%)

19 0 24

*

Statistically significant ( p < 0.05).

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posturing in TLE but a more detailed analysis about seizure spread into different basal ganglia structures has not been evaluated until now.3,9 The purpose of the present study was to analyse, therefore, the process of the seizure spread by use of precise observation of the contralateral ictal dystonia. Over the last decade there have been many reports describing movement disorders caused by lesions in structures of the basal ganglia (e.g. tumours, vascular malformations, haemorrhages, trauma or infarctions).10—13 Dystonia was often related to lesions located within the striatopallidal complex (especially the putamen), the thalamus, or the brainstem.14—20 More precise anatomoclinical correlations were often lacking because of difficulties to assess the exact extent of the brain area involved. Two recent studies, however, described clinical features of dystonia according to a precise location of the lesion within the basal ganglia using three-dimensional T1-weighted magnetic resonance imaging sequence and stereotactic analysis.5,6 Their results suggested that dystonia associated with striatopallidal lesions compared to dystonia due to thalamic lesions presents different clinical features and pathophysiologic mechanisms. Whereas lesions of the striatopallidal system caused sustained dystonic spasms, dystonia in patients with thalamic lesions was characterized by action and posture myoclonus mainly of the upper limb. These results suggest that striatopallidal and thalamic dystonia may have different pathophysiologic bases but might both lead to a dysfunction of the cortico-striato-pallido-thalamo-cortical loop leading to overactivity in primary and supplementary motor areas. In comparison, dystonia in our study is epileptic in nature. In the majority of the patients it was characterized by sustained dystonic contractions usually leading to fist closure and flexion of the wrist (comparable to striatopallidal dystonia). In fewer cases, it was predominated by myoclonic jerks of variable amplitude (similar to thalamic dystonia). Both, ‘‘striatopallidal’’ and ‘‘thalamic’’ dystonia occurred in similar frequency in MTLE and NTLE seizures but we observed a difference in latency of the ‘‘striatopallidal’’ type between the two patient groups. Analysis of seizure spread is difficult. Ictal discharges from a mesial temporal lobe epileptic focus were most often reported to spread first into the ipsilateral temporal neocortex, but also early propagation into the ipsilateral frontal lobe and the contralateral hippocampal formation is repeatedly described in the literature.21—23 Less is known about neocortical temporal lobe seizure propagation in temporal lobe epilepsy.

A. Holl et al.

In our study, clinical analysis of dystonic posturing showed a significant earlier occurrence of the ‘‘striatopallidal’’ type in NTLE than in MTLE seizures suggesting a rapid seizure propagation from the neocortical focus into the striatopallidal complex compared to a ‘‘delayed’’ spread of ictal discharges from mesial temporal structures into the striatum/ pallidum. This dystonic subtype predominated by sustained muscle contractions was the most frequently one observed in our patients and can be regarded as a reliable clinical feature as it occurred with a high constancy in a given patient. Those subtypes, which are characterized by myoclonic jerks did not show similar differences. This observation may be of clinical value as seizure analysis and assessment of latency of this ictal dystonic subtype might help to differentiate between an epileptic focus of mesial from neocortical temporal lobe origin.

Conclusions The results of our study suggest that seizures originating in the temporal neocortex spread fast into structures responsible for dystonic posturing characterized by sustained muscle contractions with fist closure and flexion of the wrist. The difference of the latency of this dystonic subtype may provide a differentiation between an epileptic focus of mesial from neocortical temporal lobe origin.

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Ictal dystonic posturing in mesial versus neocortical temporal lobe seizures

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