Clinical Study Received: March 24, 2014 Accepted after revision: July 14, 2014 Published online: October 28, 2014

Stereotact Funct Neurosurg 2014;92:372–380 DOI: 10.1159/000366003

Different Surgical Approaches for Mesial Temporal Epilepsy: Resection Extent, Seizure, and Neuropsychological Outcomes Hana Malikova a, f Lenka Kramska b Zdenek Vojtech c, g Roman Liscak d Jan Sroubek e Jiri Lukavsky h Rastislav Druga f   

 

 

 

 

 

 

Departments of a Radiology, b Clinical Psychology, c Neurology, d Radiation and Stereotactic Neurosurgery and e Neurosurgery, Epilepsy Center, Na Homolce Hospital, f Institute of Anatomy, 2nd Medical Faculty, and g Department of Neurology, 3rd Medical Faculty, Charles University in Prague, and h Institute of Psychology, Academy of Sciences of the Czech Republic, Prague, Czech Republic  

 

 

 

 

 

Key Words Epilepsy surgery · Temporal lobe epilepsy · Memory · Outcome · MRI volumetry · Amygdalohippocampectomy

Abstract Background: Surgical therapy of intractable mesial temporal lobe epilepsy (MTLE) is an effective and well-established treatment. Objectives: We compared two different surgical approaches, standard microsurgical anterior temporal resection (ATL) and stereotactic radiofrequency amygdalohippocampectomy (SAHE) for MTLE, with respect to the extent of resection or destruction, clinical outcomes, and complications. Material and Methods: 75 MTLE patients were included: 41 treated by SAHE (11 right sided, 30 left sided) and 34 treated by ATL (21 right sided, 13 left sided). Results: SAHE and ATL seizure control were comparable (Engel I in 75.6 and 76.5% 2 years after surgery and 79.3 and 76.5% 5 years after procedures, respectively). The neuropsychological results of SAHE patients were better than in ATL. In SAHE patients, no memory deficit was found. Hippocampal (60.6 ± 18.7%) and amygdalar (50.3 ± 21.9%) volume reduction by SAHE was significantly lower than by ATL (86.0 ± 12.7% and 80.2 ± 20.9%, respectively). The overall rate of surgical nonsilent complications without permanent neurological deficit after ATL was 11.8%, and another 8.8% silent infarctions were

© 2014 S. Karger AG, Basel 1011–6125/14/0926–0372$39.50/0 E-Mail [email protected] www.karger.com/sfn

found on MRI. The rate of clinically manifest complications after SAHE was 4.9%. The rate of visual field defects after SAHE was expectably less frequent than after ATL. Conclusion: Seizure control by SAHE was comparable to ATL. However, SAHE was safer with better neuropsychological results. © 2014 S. Karger AG, Basel

Introduction

Surgical therapy of intractable temporal lobe epilepsy (TLE) is an effective and well-established treatment that brings seizure relief in 60–70% of patients [1]. For many years, various types of standard temporal resections have been used for the treatment of mesial TLE (MTLE). Anterior temporal resection (ATL) is still the most commonly used surgical procedure. However, it is also known that the surgical treatment of TLE bears the risk of memory impairment. In the interest of preserving memory function and quality of life, minimal surgical approaches are still being sought. Selective transcortical amygdalohippocampectomy (AHE) was first described by Niemeyer [2] in 1957. The goal of this procedure is to remove the medial structures of the temporal lobe (hippocampus, amygdala, parahippocampus) while minimizing neocortical resection. Later, Yasargil et al. [3] proposed a strictly meHana Malikova, MD, PhD Department of Radiology, Na Homolce Hospital Roentgenova 2 CZ–150 00 Prague 5 (Czech Republic) E-Mail hana.malikova @ homolka.cz

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Materials and Methods This single-center study was retrospective and nonrandomized. Patient Selection All patients were first surgically treated for intractable MTLE between 2004 and 2011. Requirements for inclusion into this study were as follows: (1) patients indicated and followed at our center, (2) completed 2 years of clinical follow-up including electrophysiological data, and (3) completed preoperative and 1-year postoperative MRI. Although neuropsychological examination was also an important part of the study, patients with incomplete preoperative or postoperative neuropsychological assessments were not excluded. We excluded all patients referred for treatment from other institutions due to incompleteness of preoperative and postoperative data, as well as patients who previously failed surgery or Gamma Knife radiosurgery. For instance, a patient with failed SAHE (Engel III) underwent a second operation, successful ATL (Engel IA), and was included only in the SAHE group and not to the ATL group. Requirement criteria were fulfilled by 41 patients treated by SAHE and 34 patients treated by ATL. Our preoperative standard diagnostic protocol included: MRI, FDG-PET, scalp video-EEG, neuropsychological assessments, and Wada tests. According to the results of preoperative evaluations, all patients suffered from chronic medically intractable MTLE.

ATL and SAHE for the Treatment of MTLE

Surgical methods were suggested to the patients and they were allowed to choose one. All subjects were fully informed and provided informed consent. The study was approved by the local ethical committee. SAHE Technique The stereotactic radiofrequency technique published by Liscak et al. [5] using the Leksell Stereotactic System with a coordinate frame attached to a patient’s head and MRI neuronavigation was used. We used occipital access, and thermocoagulation lesions were created in the long axis of the amygdalohippocampal complex (AHC). SAHE was carried out by a string electrode with a flexible 10-mm bold active tip. Local temperature was 75 or 88 ° C depending on probe thickness.  

 

Technique of ATL We used the ATL technique described by Roberti et al. [11]. This type of resection involves resection of the amygdala, hippocampus, temporal pole, and parahippocampal gyrus, with a resection line in the temporal neocortex extending 2–2.5 cm from the temporal tip. All operations were performed under MRI 3-dimensional (3D) neuronavigation. In some patients, the extent of resection was evaluated by intraoperative MRI. MRI Methods Preoperative diagnostic MRI examinations and postoperative MRI follow-ups were performed on a 1.5-tesla whole-body MRI system. In addition to common diagnostic sequences, the diagnostic MRI protocol included: TSE T2/PD WI axial, T2 WI turbo FLAIR axial and coronal, TSE T2 WI coronal, SE T1 WI sagittal plane (coronal planes were orientated perpendicular to the long axis of the hippocampus), and a T1 3D volume acquisition sequence (voxel size: 1.0 × 1.0 × 1.0 mm, slab: 1, slices per slab 176, slice thickness: 1 mm). Diagnosis of mesial temporal sclerosis was made from MRI hippocampal volumetry according to a well-defined protocol [12] and visual assessment of the signal intensity of the hippocampus. Volumes were measured from preoperative 3D scans obtained the day of the operation or several days before, and from the scans obtained 1 year after surgery. The extent of resection was calculated as the percent difference between preoperative and postoperative volumes. MRI scans for SAHE navigation and for neuronavigation of microsurgical ATL were performed on a 1.5-tesla whole-body MRI system. A T1 3D volume acquisition sequence (voxel size: 1.0 × 1.0 × 1.0 mm, slab: 1, slices per slab: 176, slice thickness: 1 mm) was used. MRI scans for SAHE neuronavigation were acquired with a stereotactic frame attached to the head of the patient, and an indicator box. Intraoperative MRI was performed on a 1.5-tesla whole-body MRI system using TSE T2 WI coronal and axial, and SE T1 WI coronal sequences. Evaluation of Clinical Outcome with Respect to Seizures An experienced neurologist determined the clinical seizure outcome by assessing full clinical examinations including EEG monitoring, laboratory tests, MRI, and patient seizure diaries. Clinical seizure outcomes were assessed each year after operation using the Engel classification [13]. According to our standards, antiepileptic medical therapy was not changed in any patient for at least 2 years after surgery.

Stereotact Funct Neurosurg 2014;92:372–380 DOI: 10.1159/000366003

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sial resection, the transsylvian selective AHE. It has repeatedly been proven that selective AHE can achieve better neuropsychological outcome with comparable seizure control [4]. Stereotactic surgery is a minimally invasive selective approach [5]. Initial attempts with stereotactic therapy were published in the 1970s and involved brachytherapy [6] or radiofrequency thermolesions [7]. At that time, modern neuroimaging and diagnostic methods were not available, and many cases were very likely underdiagnosed and visualization of the target structures was impossible. Therefore, clinical seizure outcomes were not satisfying and the method was abandoned. In 1999, Parrent and Blume [8] reintroduced stereotactic radiofrequency amygdalohippocampectomy (SAHE) using sophisticated, modern methods: the Leksell stereonavigation system and MRI control. However, their results also were not optimal. We have used a modified SAHE method since 2004 based on the principles introduced by Vladyka [7]. In our previous studies we have reported satisfying seizure and neuropsychological outcomes [9, 10]. The aim of the present study was to compare two different surgical approaches for MTLE therapy (ATL and SAHE) with respect to the extent of resection or destruction, seizure and neuropsychological outcomes, and complications.

Neuropsychological Evaluation All patients underwent neuropsychological assessment preoperatively and 12 months after surgery. Patients were tested in 2 sessions on 2 consecutive days. On the first day, a psychological interview and the Wechsler Adult Intelligence Scale – Revised (WAISR) were performed [14]. On the second day, memory function was assessed by the Wechsler Memory Scale – Revised (WMS-R) [14]. Statistics Results were analyzed in the R programming environment [15]. Data are summarized using means ± SD and medians. Differences between pre- and postoperative neuropsychological results were evaluated using paired t tests. Comparison of resection extent by both procedures (volumetry) was performed by an unpaired t test.

Eleven patients operated on the right side had completely concordant preoperative data from MRI, scalp video-EEG monitoring, and FDG-PET; 9 patients underwent invasive EEG monitoring. Thirty-two patients underwent preoperative and 1-year postoperative neuropsychological examinations, and 10 patients refused Wada tests for memory and speech localization. Speech was localized on the left side in 19 patients and on the right side in 3. Memory was localized on the left side in 11 patients, on the right side in 9, on both sides in 1, and was nonspecific in 1. Preoperative MRI Data Preoperative MRI data are summarized in table 1. All pathology in the operation field in the ATL group was histologically proven.

Results

ATL Group We included 34 patients after ATL; 20 females and 14 males, mean age 38.7 ± 11.3 years (median: 39) and mean education 12.2 ± 1.8 years (median: 12). Twenty-four patients were right handed, 2 patients were left handed, and 6 were ambidextrous. Thirteen subjects were operated on the left side, 21 patients on the right side. Six subjects operated on the left side had completely concordant preoperative data from MRI, scalp video-EEG monitoring, and FDG-PET; 1 patient underwent invasive EEG monitoring. 374

Stereotact Funct Neurosurg 2014;92:372–380 DOI: 10.1159/000366003

Extent of Resection or Destruction of AHC according to Volumetry Data One year after SAHE, stereotactic lesions appeared as postnecrotic oblong pseudocysts surrounded by atrophic tissue with gliosis. Pseudocysts always spared the dorsal part of the hippocampus, then attacked the hippocampus and the amygdala with some individual asymmetry and caused partial destruction of these structures. The remnant dorsal part of the hippocampus in both groups was obviously atrophic 1 year after therapy. Hippocampal and amygdalar volume reduction by SAHE (60.6 ± 18.7% and 50.3 ± 21.9%, respectively) was significantly lower than by ATL (86.0 ± 12.7% and 80.2 ± 20.9%, respectively). MRI volumetry data after SAHE and ATL are summarized in table 2. In the ATL group, 13 patients were evaluated by intraoperative MRI, while 21 patients did not undergo intraoperative MRI. MRI volumetry of the residual hippocampus and of the amygdala in both subgroups were comparable. MRI volumetry data and the rate of ischemic complications are summarized in table 3. Evaluation of the extent of resection by intraoperative MRI was associated with more complications without any effect on the extent of resection. Complications No death or permanent neurological deficits occurred in either group. SAHE Group We observed 2 symptomatic complications (4.9%) in SAHE-treated patients; 1 meningitis requiring antibiotic therapy and 1 case of transitory anomia caused probably by a small cortical hematoma in the entry point of the probe, which resolved spontaneously. We found upper quadrantanopia in 2 patients (4.9%). Malikova/Kramska/Vojtech/Liscak/ Sroubek/Lukavsky/Druga

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Patient Selection Data SAHE Group We included 41 patients treated by SAHE: 21 females and 20 males, mean age 38.8 ± 11.4 years (median: 36), and mean education 11.7 ± 2.2 years (median: 12). Thirtythree patients were right handed, 4 patients were left handed, and 4 were ambidextrous. Thirty patients were treated on the left side, 11 on the right side. Seventeen subjects operated on the left side had complete concordant preoperative data from MRI, scalp video-EEG monitoring, and FDG-PET; 4 patients underwent invasive EEG monitoring. Seven patients operated on the right side had completely concordant preoperative data from MRI, scalp video-EEG monitoring, and FDG-PET; 2 patients underwent invasive EEG monitoring. All patients underwent neuropsychological examinations preoperatively and 1 year after operation; 5 patients refused Wada tests for memory and speech localization. Speech was localized on the left side in 33 patients, on the right side in 1, on both sides in 1, and was nonspecific in 1. Memory was localized on the left side in 25 patients, on the right side in 7, on both sides in 1, and was nonspecific in 3 patients.

Table 1. Preoperative MRI data a SAHE (n = 41)

MRI pathology

Left SAHE (n = 30)

Unilateral MTS MTS negative Bilateral MTS Dual pathology

25 patients (83.3%) 4 patients (13.3%) 1 patient (3.3%)

Other MRI lesions elsewhere

Right SAHE (n = 11) 10 patients (90.9%) 1 patient (9.1%) 0 patients 1 bilateral parahippocampal cortical dysplasia 1 unilateral parahippocampal cortical dysplasia 1 subependymal heterotopy of grey matter 2 cavernous malformations 2 hypophyseal adenomas 1 bilateral occipital cortical lesions

b ATL (n = 34)

MRI pathology

Left ATL (n = 13)

Right ATL (n = 21)

Unilateral MTS MTS negative Bilateral MTS Other lesions in mesial temporal structures Dual pathology

11 patients (84.6%) 0 patients 0 patients 1 (7.7%) DNET 1 (7.7%) schizencephaly 1 (7.7%) parahippocampal cortical dysplasia

14 patients (66.7%) 4 patients (19.0%) 1 patient (4.8%) 1 (4.8%) gangliocytoma 1 (4.8%) amygdalar and hippocampal hamartoma 1 bilateral frontal polymicrogyria 1 contralateral parahippocampal cortical dysplasia 1 cavernous malformation 2 (9.5%) nontemporal postoperative changes after surgical treatment of abscess and posttraumatic changes

Other MRI lesions elsewhere

1 (7.7%) AVM

MTS = Mesial temporal sclerosis; DNET = dysembryoplastic neuroepithelial tumor; AVM = arteriovenous malformation.

Table 2. Comparisons of the extent of resection or destruction by SAHE and ATL

Hippocampal volume reduction, % (max./min.) Amygdalar volume reduction, % (max./min.) Remnant dorsal length of hippocampus, mm

SAHE

ATL

p

60.6±18.7 (16/84) 50.3±21.9 (0/88) 16±8

86.0±12.7 (57/100) 80.2±20.9 (0/100) 9±7

Different surgical approaches for mesial temporal epilepsy: resection extent, seizure, and neuropsychological outcomes.

Surgical therapy of intractable mesial temporal lobe epilepsy (MTLE) is an effective and well-established treatment...
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