Central Journal of Neurological Disorders & Stroke

Cite this article: Fujimoto A, Okanishi T, Yamazoe T, Yokota T, Sato K, et al. (2015) Seizure Semiology Predicts Mesial Temporal Structure Onset for MRI Lesional Temporal Lobe Epilepsy. J Neurol Disord Stroke 3(3): 1104. 1/5

*Corresponding authorAyataka Fujimoto, Seirei Hamamatsu General Hospital, Comprehensive Epilepsy Center, 2-12-12 Sumiyoshi, Naka-ku, Hamamatsu-shi, Shizuoka 430-8558, Japan, Tel: 8153-474-2222; Fax: 8153-475-7596; Email:

Submitted: 11 August 2015

Accepted: 22 September 2015

Published: 25 September 2015

Copyright© 2015 Fujimoto et al.

OPEN ACCESS

Keywords•Mesial temporal lobe epilepsy (mTLE)•Neocortical temporal lobe epilepsy (neoTLE)•MRI lesion•Seizure semiology•subdural electrode study

Research Article

Seizure Semiology Predicts Mesial Temporal Structure Onset for MRI Lesional Temporal Lobe EpilepsyAyataka Fujimoto*, Tohru Okanishi, Tomohiro Yamazoe, Takuya Yokota, Keishiro Sato, Mitsuyo Nishimura, Hideo Enoki and Takamichi YamamotoSeirei Hamamatsu General Hospital, Comprehensive Epilepsy Center, Japan

Abstract

Objective: Subdural electrodes (SEs) are important for determining the epileptogenic zone for epilepsy surgery. However, for a focus in the mesial temporal structure (MTS), the resection area is limited to the MTS. Since SE placement is a procedure used to determine the resection area, once the seizure onset zone is decided for mesial temporal lobe epilepsy (TLE), SEs are not always required. The purpose of this study was to review the pre-surgical examinations for MRI lesional TLE.

Methods: Patients with TLE secondary to an MRI lesion who underwent an SE study followed by focus resection were studied. The following were evaluated: MRI, fluorodeoxyglucose-positron emission tomography, 123I-iomazenil single-photon emission computed tomography, electroencephalogram (EEG), long-term video EEG, seizure semiology, SE study, and surgical treatment outcomes.

Results: There were 32 patients with TLE including 9 cases of brain tumors, 17 of hippocampal atrophy, 4 of traumatic brain injuries, and 2 of intracranial hemorrhage. The patients who exhibited typical complex partial seizure of TLE had mesial temporal lobe onsets proven by SE studies. The subsequent surgical treatment also proved that the epileptogenic zone was excised due to seizure freedom. Neuro-imaging and neurophysiological studies were mainly used to decide the laterality of the TLE focus. However, typical TLE seizure semiology leads to mesial temporal structure onset.

Conclusion: TLE secondary to an MRI lesion with typical TLE seizure semiology is highly associated with mesial temporal structure onset.

ABBREVIATIONSSE: Subdural Electrodes; MTS: Mesial Temporal Structure;

TLE: Temporal Lobe Epilepsy; EEG: Electroencephalogram; MRI: Magnetic Resonance Imaging; VEEG: Long-Term Scalp Video EEG; FDG-PET: Fluoro Deoxyglucose-Positron Emission Tomography; IMZ-SPECT:123I-Iomazenil Single-Photon Emission Computed Tomography

INTRODUCTIONTemporal lobe epilepsy (TLE) is drug-resistant localization-

related epilepsy with a favorable seizure outcome after surgery [1,2]. The presence of a focal brain lesion on magnetic resonance imaging (MRI) is one of the most reliable independent predictors of a good postoperative seizure outcome [3]. However, lesionectomy alone does not always provide seizure freedom [4, 5].

The utility of subdural electrodes (SEs) has been widely accepted by many centers performing epilepsy surgery worldwide. However, the practical usefulness of SEs for lesional TLE has been questioned by many because of its invasiveness and associated mortality and morbidity [6].

The most important role of an SE study in epilepsy surgery is to determine the epileptogenic zone, seizure onset zone, irritative zone, and symptomatogenic zone. Based on the SE study, the cortical resection area is eventually decided. However, seizures of temporal lobe origin are divided into those arising from the mesial temporal structure, the hippocampus or closely related structures (limbic temporal seizures), and those that arise from other lateral or inferior temporal regions (neocortical temporal seizures). Once the seizure onset area is found to be a mesial temporal structure, being different from a neocortical

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onset seizure, an invasive SE study is not always necessary. An SE study is sometimes not possible for epileptic seizures secondary to an MRI lesion due to increased intracranial pressure. SEs also has risks of nausea and vomiting, cerebrospinal fluid leakage, and acute subdural hematoma [7-10].

The purpose of this study was to evaluate the factors, including brain MRI, scalp electroencephalogram (EEG), long-term scalp video EEG (VEEG), epilepsy seizure semiology, fluorodeoxyglucose-positron emission tomography (FDG-PET), and 123I-iomazenil single-photon emission computed tomography (IMZ-SPECT), that are useful for identifying mesial temporal lobe onset for temporal lobe epilepsy secondary to an MRI lesion.

PATIENTS AND METHODSPatients with TLE secondary to an MRI lesion who

subsequently underwent focus resection surgery were studied. They had been followed-up for more than 2 years with complete seizure freedom. Their ages ranged from 7 to 59 years. There were 32 patients, 18 females and 14 males (Table1).

MRI, scalp EEG, VEEG, seizure semiology, FDG-PET, IMZ-SPECT, extra and intra-operative SE studies, and postoperative seizure outcome were evaluated.

MRI

MRI was performed according to our epilepsy protocol on a 1.5-T scanner (Discovery MR-750, GE, Milwaukee, WI, USA). The field of view was 220 mm × 220 mm, and the matrix was 256 × 256. The protocol included: sagittal T1-weighted spin echo sequence (5.0-mm slice thickness, 0.5-mm interslice gap, TR 650 ms, TE 16 ms), axial T2-weighted TSE sequence (5.0/1.0/2876/120), coronal T2-weighted TSE sequence (2.0/0.3/3719/120), coronal FLAIR, and axial FLAIR sequence (5.0/1.0/6000/120/1900). Sequences were angulated perpendicularly or parallel to the longitudinal axis of the hippocampal body on axial and coronal FLAIR. Gadolinium was administered when MRI showed a tumor lesion.

EEG

This study was performed for a total of 30 minutes using the 10-20 International system of electrode placement with the reference electrode on the auricle with the electrocardiogram.

VEEG

VEEG was performed until a habitual seizure was captured using the 10-20 international system of electrode placement with reference electrodes using Pz’ (1 cm behind Pz) with simultaneous video recording of the clinical manifestations. Antiepileptic drug dosages were decreased or the drugs were discontinued totally during recording.

Seizure semiology

Clinical ictal semiology was classified as favoring either mesial TLE or neocortical TLE localization. Based on their clinical manifestations, the seizures were classified by neurophysiologists E, F, and O into mesial TLE (mTLE) or neocortical TLE (neoTLE). Studies have shown that ipsilateral

limb automatism, contralateral dystonic posturing, or alimentary automatisms, staring, psychic phenomena, and viscerosensory auras are more commonly seen in mTLE [11-14]. In contrast, early aphasia, vestibular symptoms, auditory phenomena, and visual hallucinations have been associated with the temporal neocortex [15-17].

FDG-PET acquisition

Interictal brain metabolism was studied in all patients. PET scans were performed using an integrated PET/computed tomography (CT) camera (Discovery ST; GE Healthcare, Waukesha, WI, USA). The Discovery ST has an intrinsic spatial resolution of approximately 6 mm full width at half maximum (FWH), yielding PET slices with 4.6-mm center-to-center spacing. 18F-FDG (3.7-4MBq/kg of body weight) was injected intravenously with the patient in an awake and resting state, with eyes closed, in a quiet environment. Image acquisition started 60 min after injection and ended 15 min later. Images were reconstructed using an ordered subset expectation maximization algorithm, with 5 iterations and 32 subsets, and corrected for attenuation using a CT transmission scan.

IMZ-SPECT

123I-IMZ-SPECT) was conducted on a scanner (GE Infinia Hawkeye 4) using 123I-IMZ while the patient was in the interictal state. IMZ-SPECT technique was performed for 30 min starting at 180 min after the intravenous injection of 167MBq of 123I-IMZ (Nihon Medi-Physics Co. Ltd, Hyogo, Japan).

Surgery and histopathology

All but three patients with cavernomas underwent extra-operative subdural electrode studies followed by focus resection with lesionectomy. The three patients with a cavernoma underwent intra-operative electro-corticography (EcoG) followed by lesionectomy. All specimens were submitted for histopathological study. Only Engel class Ia patients were included in this study to prove the total resection of the epileptogenic zone.

RESULTS AND DISCUSSION

Results

MRI: There were 9 brain tumors (3 cavernomas and 6 glial tumors), 17 cases of hippocampal atrophy (HA), 4 cases of traumatic brain injuries, and 2 cases of intracranial hemorrhage (ICH) (Table 1).

EEG: EEG could detect epileptiform discharges in 23 of 32 patients (72%). Among them, except for one patient (Patient 2, bilateral TLE), 22 EEGs were concordant with the focus side. Among the remaining 9 (28%) of 33 patients, 7 EEGs (22%) were normal, and 2 (6%) EEGs showed focal slowing over the ipsilateral area of the focus hemisphere.

VEEG: At least two habitual seizures were captured during VEEG study in 31 (97%) patients. One (3%) patient (Patient 13) did not have any habitual seizures during two weeks of monitoring, even though her anti-epileptic medications were discontinued in the last half of the study. Among the 97% of VEEGs, only one VEEG (Patient 2) showed independent bilateral temporal ictal EEG discharges. The VEEG could detect focus

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Table 1: Patients and Pre-Surgical examinations.

Pt. age(FU) sex Epilepsy Semiology MRI Pathology EEG VEEG PET IMZ

1 37(6) F L.mTLE Typical CPS HA FCD HS R.FT R.FT R.T R.T

2 47(6) F biTLE Typical CPS L.HA HS Bil T Bil L.T L.T

3 25(6) M R.neoTLE Atypcal cavernoma Cavernoma R.FT L.FT R.T R.T

4 24(5) F R.mTLE Typical CPS HA FCD HS R.FT R.FT L.T R.T

5 38(5) F R.mTLE Typical CPS HA HS R.FT R.FT R.T unlear

6 19(5) M R.mTLE Typical CPS DNET DNET R.FT R.FT R.T R.T

7 21(5) M R.mTLE Typical CPS HA FCD R.FT R.FT unclear R.T

8 9(4) M L.mTLE Typical CPS HA FCD HS R.FT R.T R.T R.T

9 21(4) F R.neoTLE Atypical HA FCD HS R.FT R.FT R.T R.T

10 35(3) F R.neoTLE Atypical Multi-cavernomas Cavernoma R.FT R.FT multiple multiple

11 20(3) M mTLE Typical CPS R.cont FCD HS R.FT R.FT R.FT R.FT

12 20(3) M mTLE Typical CPS R.cont FCD HS R.FT R.T R.T R.T

13 55(3) F R.neoTLE Atypical HA FCD HS Normal N/A R.T unlear

14 11(3) F mTLE Typical CPS Low grade glioma Low G Normal L.FT R.T R.T

15 25(3) F mTLE Typical CPS HA HS L.FT L.FT L.T L.T

16 7(3) F mTLE Typical CPS DNET DNET L.FT R.FT L.T L.T

17 52(3) M mTLE Typical CPS R.FTcont+R.HS Cont+FCD R.F L.T R.FT R.FT

18 33(3) M L.neoTLE Atypical Cavernoma Cavernoma L.T L.FT L.T L.T

19 43(3) M L.mTLE Typical CPS ICH hemisiderin L.FT R.FT L.T L.T

20 45(3) M R.mTLE Typical CPS ICH hemisiderin R.FT R.FT R.T R.T

21 38(3) M R.mTLE Typical CPS DNET DNET R.FT L.T R.T R.T

22 35(3) F L.mTLE Typical CPS Oligo Oligo L.T R.FT L.T L.T

23 31(3) M R.mTLE Typical CPS HA FCD HS R.FT R.FT unclear unlear

24 53(3) F R.mTLE Typical CPS HA FCD HS Normal L.FT R.T R.T

25 31(3) F L.mTLE Typical CPS L.FTcont+L.HS Cont+FCD L.FT R.FT L.T L.T

26 38(3) F L.mTLE Typical CPS HA FCD HS focal slow R.FT R.T R.T

27 25(3) M R.mTLE Typical CPS HA FCD HS Normal R.FT R.T R.T

28 12(2) F R.mTLE Typical CPS HA FCD HS Normal R.FT R.T R.T

29 59(2) F L.mTLE Typical CPS HA HS Normal R.FT R.T R.T

30 41(2) F R.mTLE Typical CPS HA HS Normal R.FT R.T unlear

31 44(2) M R.mTLE Typical CPS DNET DNET focal slow L.FT R.T R.T

32 51(2) F R.mTLE Typical CPS HA FCD HS L.FT R.FT L.T L.TAbbreviations: Pt: Patient; FU: Follow-Up Period; F: Female; M: Male; L: Left; R: Right; Mtle: Mesial Temporal Lobe Epilepsy; Bi: Bilateral; Neo TLE: Neocortical Temporal Lobe Epilepsy; CPS: Complex Partial Seizure; HA: Hippocampal Atrophy; DNET: Dysembryoplastic Neuroepithelial Tumors; Multi: Multiple; Cont: Contusion; FT: Front temporal; T: Temporal; ICH: Intracranial Hemorrhage; Oligo: Oligodendroglioma; FCD: Focal Cortical Dysplasia

laterality with 97% accuracy. However, it was not possible to clarify the difference between mesial and neocortical temporal onset using VEEG changes.

Seizure semiology

On the VEEG, 31 (97%) patients showed their habitual seizure semiology; 27 patients showed ipsilateral limb automatism, contralateral dystonic posturing, oroalimentary automatisms, staring, psychic phenomena, and viscerosensory auras seen in typical temporal lobe epilepsy. Common semiologies of the 27 patients were staring and oroalimentary automatisms. However,

5 of 32 patients (patients 3, 9, 10, 13, and 18) showed 100% secondary generalization. All of these 5 patients also had very short periods of staring and mouthing, as seen in typical mTLE semiology just before convulsion. However, the seizures quickly led to secondary generalization. One of the four patients (Patient 3) also had a hypermotor seizure.

FDG-PET: FDG-PET showed concordance with the focus side in 29 (90%) of 32 patients. However, it could only clarify focus laterality, but not mesial/neocortical foci.

IMZ-SPECT: IMZ-SPECT showed concordance with the focus

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side in 27 (84%) patients. This study also did not define mesial and neocortical foci.

Surgical outcome and histopathology

Based on the MRI, EEG, VEEG, FDG-PET, IMZ-SPECT, and seizure semiology, the laterality of the TLE was determined. Therefore, all but 3 patients with cavernomas underwent extra-operative SE studies. The 3 patients with cavernoma who showed atypical seizure semiology underwent intra-operative ECoG. The study showed epileptiform discharges near the cavernoma, but not in the parahippocampal gyri, frontal lobe, and parietal lobe. The three patients with cavernomas subsequently underwent cavernoma resection only. The two patients (Patients 9 and 13) with atypical seizure semiology had a neocortical epileptogenic zone that quickly spread to the hippocampus. Since they had hippocampal atrophy on MRI and quick ictal epileptic discharge propagation from onset to the hippocampus, they underwent anterior temporal lobectomy including the epileptogenic zone with amygdala hippocampectomy. The 27 patients with typical TLE semiology underwent anterior temporal lobectomy with amygdala hippocampectomy and lesionectomy on the language non-dominant hemisphere and selective transcortical hippocampectomy and lesionectomy on the language-dominant hemisphere. All of the patients have been free of seizures after the operations for more than 2 years.

For the pre-surgical evaluation, except for the seizure semiology, MRI, EEG, VEEG, FDG-PET, and IMZ-SPECT were only able to determine the laterality of the TLE. However, seizure semiology provided not only the laterality but also identified mesial/lateral onset for patients with TLE secondary to MRI lesions in this study.

Histopathology showed there were 9 brain tumors, with 3 cavernomas, 4 dysembryo plastic neuroepithelial tumors (DNETs), 1 WHO grade I oligodendroglioma, and 1 nonspecific low-grade glial tumor (Patient 14). There were 18 cases of hippocampal sclerosis with or without focal cortical dysplasia (FCD). There were two cases of contusional brain injuries with hippocampal sclerosis and FCDs. There were two cases of hemosiderin deposits after ICH. Of the two ICH cases, one had an angiographically occult arteriovenous malformation (AVM), and the other one had an idiopathic ICH.

DISCUSSIONThe International League Against Epilepsy (ILAE) has

said that ictal recording with use of minor or major invasive recording techniques may be unnecessary if there is concordance between interictal scalp EEG findings and clinical, brain imaging, and neuropsychological data, and if the epileptic nature and semiology of the patient’s attacks are not in doubt [18]. According to Castro [19], the surgical outcome was not influenced by contralateral VEEG seizure onset or contralateral increased flow on ictal SPECT. Wyllie also mentioned that epilepsy surgery was successful for patients with a congenital or early-acquired brain lesion, despite abundant generalized or bilateral epileptiform discharges on EEG [20]. The MRI finding of hippocampal atrophy (HA) is a potent predictor of surgical success in patients with medically refractory mTLE [21,22]. There is a high concordance of MRI and interictal and ictal EEG data in these cases [23], as

the present study has also shown. In cases where the presurgical evaluation indicates concordant MRI and interictal and ictal EEG findings, surgery is indicated, with good surgical outcomes, obviating invasive monitoring studies. On the other hand, compared to gross-total lesionectomy alone, significantly higher rates of seizure freedom were observed with the addition of hippocampectomy, corticectomy, or both hippocampectomy and corticectomy [24,25].

There were four patients with a contusional brain. All of the histopathological specimens had focal cortical dysplasia (FCD). The patient with asymptomatic FCD could have a potential epileptic zone. And then, head trauma might cause epileptic spells for these four patients.

CONCLUSIONFor mTLE, the most important procedure to achieve freedom

from seizures is mesial structure resection. However, for TLE secondary to an MRI lesion that exhibits typical temporal lobe epilepsy semiology, lesionectomy alone does not achieve freedom from seizures. Currently, videotaping, cell phone movies, and digital camera movies are easily available to capture seizure semiology. Once a patient’s seizure semiology is recognized objectively, selected patients with typical TLE semiology secondary to an MRI lesion may undergo amygdala hippocampectomy with or without MRI lesionectomy directly. However, neuropsychological studies, language dominancy on the Wada test, and functional MRI have to be considered for epilepsy surgery. TLE secondary to an MRI lesion that exhibits typical TLE seizure semiology was associated with mesial temporal structure onset in the present study.

ACKNOWLEDGEMENTSAuthor contributions to the study and manuscript preparation

include the following.

Epilepsy surgery operation: Fujimoto, Yamazoe and Yamamoto.

Acquisition of data: Fujimoto, Okanihi, Sato, Yokota, Enoki and Nishimura

Analysis and interpretation of data: Fujimoto, Okanishi and Enoki.

Conflict of Interest

The authors report no conflict of interest concerning the patients or methods used in this study or the findings specified in this paper. All members of The Japan Neurosurgical Society (Fujimoto, Yamazoe and Yamamoto) have registered the online Self-reported COI Disclosure Statement Forms.

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Fujimoto A, Okanishi T, Yamazoe T, Yokota T, Sato K, et al. (2015) Seizure Semiology Predicts Mesial Temporal Structure Onset for MRI Lesional Temporal Lobe Epilepsy. J Neurol Disord Stroke 3(3): 1104.

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