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 Table of Contents  
ORIGINAL ARTICLE
Year : 2021  |  Volume : 38  |  Issue : 4  |  Page : 209-218

Long-term surgical outcomes and predictors of surgical treatment in temporal lobe epilepsy


1 Department of Neurology, Gazi University Faculty of Medicine, Ankara, Turkey
2 Department of Neurosurgery, Gazi University Faculty of Medicine, Ankara, Turkey
3 Department of Nuclear Medicine, Gazi University Faculty of Medicine, Ankara, Turkey
4 Department of Radiology, Gazi University Faculty of Medicine, Ankara, Turkey
5 Department of Pediatric Neurology, Gazi University Faculty of Medicine, Ankara, Turkey

Date of Submission21-Oct-2021
Date of Decision29-Oct-2021
Date of Acceptance31-Oct-2021
Date of Web Publication29-Dec-2021

Correspondence Address:
Irem Yildirim
Department of Neurology, Gazi University Faculty of Medicine, Besevler, Ankara 06500
Turkey
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/nsn.nsn_200_21

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  Abstract 


Background: Surgical treatment of epilepsy is a favored modality in the management of refractory temporal lobe epilepsy (TLE) and known to be quite effective. The aim of this study was to evaluate the long-term outcomes in surgical treatment of TLE and to identify prognostic factors influencing postoperative seizure remission. Materials and Methods: The patients who underwent anterior temporal lobectomy (ATL) with the diagnosis of refractory TLE in our center between the years of 2006 and 2020 were included. Preoperative workup process was carried out by a multidisciplinary team and consisted of neuropsychological examination, long-term electroencephalography, brain magnetic resonance imaging (MRI), and fluorodeoxyglucose positron emission tomography (FDG-PET) for each patient. Postoperative assessment of seizure control was repeated every year following surgery and categorized according to Engel's outcome classification. The predictive value of baseline demographic, clinical, laboratory, imaging, and histopathological parameters on postoperative seizure control was also evaluated. Results: One hundred and forty-three patients who underwent ATL with the diagnosis of TLE were included. According to Engel's classification, the seizure freedom rate was found to be 83.2% at the 2nd year, 81.3% at the 4th year, and 79.2% at the 10th year after surgery. In the univariate analysis, febrile seizure (FS) history, unilateral interictal epileptiform discharges (IEDs), hippocampal sclerosis (HS) on MRI, unilateral temporal hypometabolism (HM) on FDG-PET, and HS in histopathology were predictors of seizure control at the postoperative 2nd and 10th years. FS history, unilateral localization of IEDs, and unilateral FDG-PET findings of temporal HM were found to be the independent predictors of postoperative seizure control on multivariate analysis. Conclusions: In the current study, we revealed that epilepsy surgery provides effective seizure control and represents a beneficial therapeutic option in refractory TLE. Our results also suggested that FS history, unilateral IEDs, and unilateral FDG-PET findings of temporal HM were independent predictors of seizure remission in these patients.

Keywords: Electroencephalography, refractory temporal lobe epilepsy, surgical treatment of epilepsy


How to cite this article:
Yildirim I, Gurses AA, Ataoglu EE, Kurt G, Akdemir UO, Oner AY, Hirfanoglu T, Atay LO, Serdaroglu A, Bilir E. Long-term surgical outcomes and predictors of surgical treatment in temporal lobe epilepsy. Neurol Sci Neurophysiol 2021;38:209-18

How to cite this URL:
Yildirim I, Gurses AA, Ataoglu EE, Kurt G, Akdemir UO, Oner AY, Hirfanoglu T, Atay LO, Serdaroglu A, Bilir E. Long-term surgical outcomes and predictors of surgical treatment in temporal lobe epilepsy. Neurol Sci Neurophysiol [serial online] 2021 [cited 2022 Jun 28];38:209-18. Available from: http://www.nsnjournal.org/text.asp?2021/38/4/209/334052




  Introduction Top


Temporal lobe epilepsy (TLE) is the most common localization-related epilepsy syndrome in adults. Previous reports have revealed that complete remission was achieved in only 8%–23% of TLE patients with antiepileptic drugs (AEDs) and surgical treatment was quite superior to medical therapy in these patients.[1],[2],[3],[4] Refractory TLE has been the most common indication for epilepsy surgery,[5],[6] and approximately 59%–82% of refractory TLE patients benefit from temporal lobe resection in terms of seizure remission.[7],[8],[9],[10],[11]

Surgery in TLE actually targets long-term seizure freedom. Postoperative seizure remission state is a quite dynamic process, and recurrence rate gradually decreases within years depending on many variables.[7],[12] Although seizures mostly recur within the first 6 months after surgery, recurrences may occur until 2–5 years postoperatively.[9],[13]

While the majority of studies on epilepsy surgery have focused on postoperative outcomes, which is now a quite well-known issue, the number of studies investigating the predictors of postoperative seizure control is limited and the results are contradictory. Clinical predictors that were reported in the previous studies included gender, age of disease onset, disease duration, febrile seizure (FS) history, presence of focal to bilateral tonic-clonic seizures (FBTCSs), presence of hippocampal sclerosis (HS) on pathology, side of surgery, extent of resection (total-subtotal), and unilateral localization of interictal epileptiform discharges (IEDs) on electroencephalography (EEG).[14],[15],[16],[17],[18],[19]

The objectives of this study were long-term assessment of seizure control after surgery and identification of prognostic factors related to postoperative remission in patients with refractory TLE.


  Materials and Methods Top


Patient selection and preoperative workup

This retrospective study was conducted in Gazi University Medical Faculty Epilepsy Center. Medical records of patients who underwent standard anterior temporal lobectomy (ATL) between the years of 2006 and 2020 with a diagnosis of refractory TLE were reviewed. Among 167 patients, 143 with a follow-up duration of 10 years or more were included in the study. All patients were aged over 17 years. The same standard preoperative evaluation protocol was performed in each patient. The study protocol was approved by the local ethics committee.

As the first step of preoperative evaluation, detailed medical history was obtained from all patients and full physical and neurological examinations were completed. After clinical evaluation, all patients underwent long-term scalp EEG monitorization, using a 32-channel montage in the guidance of a 10–20 electrode system and together with anterior temporal electrodes. The patients were monitored until adequate number of typical seizures was observed. On EEG, the presence of IEDs at a rate of 80% or greater in only a single temporal lobe was accepted as unilateral. For localization (temporal or extratemporal) and lateralization (right or left) of seizures, both clinical signs and interictal-ictal EEG changes were taken into consideration.

Cranial magnetic resonance imaging (MRI) records of all patients were compatible with temporal lobe protocol, including included axial and sagittal T1-weighted, axial T2-weighted, oblique coronal fluid-attenuated inversion recovery perpendicular to the long axis of both hippocampi, and three-dimensional (3D) inversion recovery (IR) [Figure 1]a and [Figure 1]b. The whole-brain volumetric series were acquired using a 3D IR technique. During the previous years, MRI had been performed via a 1.5T MR scanner (Ge Signa Excite, Milwaukee, USA). However, a 3T MR scanner (Magnetom Verio; Siemens, Erlangen, Germany) has been used for the last 9 years. The images were reviewed by expert neuroradiologists.
Figure 1: Brain magnetic resonance imaging of a 27-year-old male with 6-year history of focal impaired awareness seizures twice a week. The patient was diagnosed left temporal lobe epilepsy. (a) Preoperative images demonstrating increased T2 signal and atrophy on the left hippocampus which indicate left hippocampal sclerosis, (b) Postoperative images 2 months after surgery

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Brain fluorodeoxyglucose positron emission tomography (FDG-PET) was performed in all patients, and static brain PET images were acquired using a Discovery ST PET-computed tomography scanning system (GE Medical Systems, Milwaukee, WI, USA). Experienced nuclear medicine specialists evaluated the images with respect to the presence of regional hypometabolism (HM), which is an expected abnormal finding in the epileptogenic zone [Figure 2].
Figure 2: Brain fluorodeoxyglucose positron emission tomography images of the patient in [Figure 1], demonstrating diffuse temporal hypometabolism on the left side

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Psychiatric examination and neuropsychological tests were completed for all patients prior to surgery. None had a psychiatric disorder that would be a contraindication for surgery. Preoperative neuropsychological tests were applied by a neuropsychologist in the form of a standard battery. All patients underwent WADA test or functional MRI in order to obtain information about hemispheric lateralization of language and memory functions and make an opinion about possible postoperative deficits.

The results of standard workup process prior to surgery were reviewed in a multidisciplinary surgery conference. Decision to perform a surgical intervention was given and surgical technique was specified if there was consistency in the results of clinical, electrophysiological, neuroimaging, and neuropsychological examinations.

The same neurosurgeon performed anterior temporal lobectomies. During the standard surgical procedure, the neurosurgeon removed the medial structures, including hippocampus, parahippocampal gyrus, and amygdalar nucleus together with ATL. All patients underwent standard anterior temporal resection and also tumor resection was performed when required.

Follow-up visits with regard to seizure status and AED use were provided by the same epileptologist for all patients. During the first year after surgery; follow up visits were performed in the 2nd and 6th months. After the 6th month visit,, control examinations were repeated every year. In accordance with our AED discontinuation protocol, we recommended the same preoperative drug regimen to all patients during 6 months after surgery. At the end of the 6th month, gradual AED tapering was started which lasted approximately 1½ years. Two years after the surgery, patients were completely medication free.

Postoperative seizure outcome was categorized according to Engel's outcome classification (Class I: free of disabling seizures, Class II: rare disabling seizures, Class III: worthwhile improvement, and Class IV: no worthwhile improvement).[20] Baseline parameters were compared between seizure-free (Engel's Class I) and nonseizure-free (Engel's Class II, III, IV) groups. The seizure status of the groups was recorded at the 6th month following surgery and then at the 1st, 2nd, 3rd, 4th, and 10th years, respectively.

Data acquisition

Various preoperative parameters that may predict postoperative outcome were recorded for each patient. These parameters included age, gender, disease duration, seizure type (FBTCS±), lateralization of temporal lobe, FS history, type of surgery, ipsilateral occurrence of temporal IEDs, unilateral HS on brain MRI, and unilateral temporal HM on PET. Other recorded parameters were AED use after surgery and histopathology results of the surgical specimens.

Statistical analysis

Statistical analyses were performed using SPSS version 20.0 (SPSS, Inc., Chicago, Illinois, USA). Normally distributed continuous parameters were presented as mean ± standard deviation, and Student's t-test was applied for comparison between the groups. Categorical data were presented as percentages and compared using Chi-square test. In order to identify the potential predictors of favorable surgical outcome, a univariate logistic regression analysis was used. The variables with P < 0.25 were separately evaluated and further analyzed by a multivariable model. After applying a multivariate logistic regression analysis, independent predictors of surgical outcome were identified. Odds ratios, 95% confidence interval (CI), and the Wald statistics for each independent variable were also calculated for a seizure-free outcome at the 2nd and 10th years after the surgery. P < 0.05 was accepted as statistically significant.


  Results Top


The demographic and clinical characteristics of the study group are given in [Table 1]. The mean age of the patients was 28.3 ± 7.8 (range, 17–55) years and the mean disease duration before surgery was 15.8 ± 15.0 (range, 1–46) years. Disease duration was shorter than 11 years in 36 (25.2%), between 11 and 20 years in 71 (49.7%), and longer than 20 years in 36 (25.2%) patients. The patients were followed up for 144.47 ± 14.52 (range, 120–168) months after surgery. ATL was performed in 131 (91.6%) and lesionectomy together with ATL was performed in 12 (8.4%) patients. The surgical side was left temporal lobe in 79 (55.2%) and right temporal lobe in 64 (44.8%) patients.
Table 1: Demographical and clinical characteristics of the patients (n=143)

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Histopathological findings of 143 patients were as follows: 119 (83.2%) – HS, 8 (5.5%) – cortical dysplasia (CD), 3 (2.1%) – arteriovenous malformation (AVM), 6 (4.2%) – tumor, 1 (0.7%) – tuberous sclerosis, 2 (1.4%) – meningioma, and 2 (1.4%) – gliosis.

The percentage of seizure-free patients in the postoperative follow-up visits is presented in [Figure 3]. The percentage of Engel's Class I patients was 95.8% at the 6th month, 89.5% at the 12th month, 83.2% at the 24th month, 82.1% at the 36th month, 81.3% at the 48th month, and 81.8% at the 60th month. At the 10th year of surgery, 79.2% of the patients were still meeting Engel's Class I criteria.
Figure 3: Rates of seizure-free patients (Engel's Class I) according to the postoperative follow-up periods

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At the postoperative 2nd year, demographic parameters, disease duration before surgery, side of surgery, presence of FBTCS, type of surgery, or histopathological findings did not demonstrate a significant difference between the seizure-free (Engel's Class I) and nonseizure-free groups (Engel's Class II, III, IV) (P > 0.05). Frequencies of HS on MRI, unilateral temporal HM on PET, FS history, and unilateral temporal IEDs on EEG were significantly higher in the seizure-free group (P = 0.004, P < 0.02, P < 0.037, and P < 0.001, respectively).

At the 10th year follow-up, only frequencies of unilateral IEDs on EEG, HS on histopathological examination, and FS history were found to be higher in the seizure-free group (P = 0.030, P < 0.040, and P < 0.034, respectively). No significant difference was observed between the two groups regarding other demographic and clinical parameters (P > 0.05).

In order to determine the potential predictors of postoperative outcomes, a univariate logistic regression analysis was performed, and the results are presented in [Table 2]. Presence of IEDs on EEG, FS history, unilateral HS on brain MRI, and presence of unilateral temporal HM on PET were predictors of postoperative seizure control at the 2nd year (P < 0.001, P = 0.004, P < 0.001, and P < 0.001, respectively).
Table 2: Univariate analysis of variables at the 2nd year after surgery for Engel's I outcome

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Another univariate logistic regression analysis was performed for the same parameters at the 10th year, and the results are presented in [Table 3]. Presence of unilateral temporal IEDs on EEG, FS history, HS in histopathological evaluation, and presence of unilateral temporal HM on PET were found to be predictors of postoperative seizure control (P < 0.001, P < 0.001, P = 0.030, and P = 0.022, respectively).
Table 3: Univariate analysis of variables at the 10th year after surgery for Engel's I outcome

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Predictors detected in the univariate analyses were further evaluated in a multivariate model, and the results of these multivariate logistic regression analyses are given in [Table 4]. Unilateral localization of temporal IEDs on EEG, FS history, and unilateral temporal HM on PET were found to be independent predictors of postoperative seizure control at the 2nd and 10th years.
Table 4: Multivariate logistic regression analysis for postoperative Engel's I outcome at the 2nd and 10th years

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  Discussion Top


Epilepsy surgery ensures seizure remission in approximately 70% in refractory TLE patients.[21],[22],[23] In the current study, surgical outcomes were quite successful and 89.5% of the patients had no seizures at the 12th month following surgery. Seizure remission rates were 83.2% at the 24th month and 81.3% at the 48th month. At the 10th year following surgery, 79.2% of the patients were still meeting the criteria for Engel's Class I.

Despite the advances in epilepsy surgery within the last decade, detailed studies investigating the prognostic indicators of surgical outcome are still scarce. Therefore, we evaluated predictive clinical factors likely to affect postoperative seizure remission in TLE.

In our study, postoperative 2nd-year findings demonstrated that unilateral localization of interictal epileptiform activity, FS history, unilateral HS on brain MRI, and unilateral temporal HM on PET were predictive factors associated with good postoperative prognosis. At the postoperative 10th year, unilateral localization of interictal epileptiform activity, FS history, HS in histopathology, and unilateral temporal HM on PET were found to be the clinical predictors of favorable surgical outcome. However, the significance of unilateral HS on brain MRI and histopathology was disappeared in the multivariate analysis. Based on these findings, we demonstrated that unilateral temporal IEDs on EEG, FS history, and unilateral temporal HM on PET were independent predictors of postoperative seizure control.

In our study, FS history was found to have a significant prognostic effect on outcome. While some previous studies also reported a predictive value of FS on favorable surgical outcomes,[14],[24],[25] others did not come up with a similar result.[26],[27] Prognostic effect of FS history on postoperative outcome might be based on its association with HS. In the light of translational studies indicating the sustained effects of FS on hippocampal excitability through influencing both expression of ion channels and GABAA receptor-mediated neurotransmission, it is possible to hypothesize that FS contributes to HS and epileptogenesis, as well.[28]

Cranial MRI has quite high sensitivity and specificity for detection of HS, and HS can be found in TLE patients at a rate of up to 90%.[29] Detection of HS on MRI was shown to be an important predictor of favorable surgical outcome in TLE.[17],[30],[31] In the previous series, HS was observed in 58%–72% of TLE patients, whereas MRI was reported to be normal in about 16%.[2],[7],[32] In the present study, HS was detected in 119 (83.2%) of the patients on cranial MRI. We noted that cranial MRI can predict good surgical outcome at the postoperative 2nd year; however, this effect disappeared when evaluated together with other variables using multivariate regression analysis. This might have resulted from the evaluation of MRI-positive patients together with MRI-negative ones. Although outcomes of patients with normal MRI are considered to be poor, recent studies have supported that this group has similar outcomes with patients who have HS if the results of PET, EEG, and other preoperative evaluations are consistent and if the lesion is localized to a single focus. The underlying pathophysiology in these cases has not been clarified yet; however, it is suggested to be a syndrome different from HS, which could be surgically treated.[32],[33]

Although 3T MRI has been shown to enhance the detection of subtle lesions at a rate of 20%–48% in comparison to 1–1.5T MRI, another neuroimaging method is required in patients reported to have normal MRI.[34],[35] Therefore, many epilepsy clinics routinely use FDG-PET for preoperative evaluation. FDG-PET localizes the epileptogenic focus with 85%–90% accuracy in TLE patients. In MRI-negative patients, regional HM on FDG-PET is observed at a rate of 60%–82%.[36],[37],[38] A large meta-analysis found that the predictive value of ipsilateral HM was 86% for good surgical outcomes, whereas it was 71%–80% in the group with normal MRI.[39] In many series including a previous research of our group, the surgical outcomes of MRI-negative patients were comparable to the patients with HS.[33],[36],[37],[38],[39],[40] Ipsilateral HM on FDG-PET shows a high correlation with the onset of ictal EEG in cases undergoing intracranial monitoring.[39],[41] Based on this, the need for intracranial monitoring can be reduced in cases with normal MRI, when all other findings are consistent. In addition, the need for preoperative invasive EEG monitoring, its cost and complication risks as well, can also be decreased. In our series, while MRI-negative patients underwent invasive EEG monitoring initially, the surgery decision was made without invasive monitoring in the recent years, in the case of consistent ictal electrophysiological findings on scalp EEG, HM on FDG-PET, and neuropsychological tests.

In line with the numerous previous reports, our results revealed that unilateral IEDs were significant independent predictors of the 2nd- and 10th-year outcomes.[12],[42],[43] On the other hand, there are some studies which do not support this finding.[44],[45] In the case of clear localization of unilateral IEDs on the surgical side, they serve as good predictors of favorable postoperative outcome. However, widespread IEDs may indicate the probability of diffuse irritative zone and thus poor postoperative prognosis. In a prospective study, seizures were reported to decrease by more than 90% in patients who had IEDs localized in the operated temporal lobe, whereas the rate of seizure freedom was found to be 54% if the IEDs were less lateralized.[46]

Many recent studies have reported that surgical success in TLE regarding seizure remission depends on histopathological and MRI findings. HS was the most frequently encountered histopathology in patients with refractory TLE. However, in addition to HD, CD, tumor, and vascular abnormalities, hippocampal specimens that include normal neurons which progress with reactive gliosis were also encountered.[47] Together with predominating HS cases, our study also included a number of patients with other pathologies such as tumor, CD, AVM, and nonspecific gliosis.

It was shown that postoperative prognosis was quite good in cases with mesial TLE associated with HS.[43],[44],[45],[46] Compared to other pathologies, the seizure recurrence rate was lower in patients with HS. The rate of seizure remission was reported to be 85% at the 1st year and 74% after 5 years.[46] Similar to previous literature, our results demonstrated a seizure remission rate of 79.4% at the end of 10-year follow-up. In a previous study, the seizure remission rate was lower in patients with CD compared to patients with HS, tumor, or vascular lesions.[48] In a recent series of pediatric TLE patients, resection of temporal MRI abnormalities other than HS was found to be associated with better long-term outcome.[49]

In our study, the effect of HS on postoperative outcome was significant at the 10th year, however, this effect was disappeared in the multivariate analysis. Failure of histopathology in predicting postoperative prognosis can be explained by high number of HS and tumor cases having good prognosis, together with CD and AVM cases. As a result, more precise interpretation of the effects of histopathology on outcome would be possible when the patients having HS alone are compared with similar number of patients having other pathologies.

FBTCSs in TLE indicate rapid spread of seizures. In the current study, we observed that FBTCS had no effect on surgical outcome, in line with the previous reports.[44],[50] On the other hand, some studies have suggested that the presence and frequency of FBTCS have a predictive value for negative surgical outcomes.[14],[16],[17] In a previous study, seizure freedom in patients without FBTCS was found to be 2.2 times higher than the ones with FBTCS at the 5th year following surgery.[50] Taken together, FBTCS in TLE is associated with higher grade of HS, more than one irritative zone, larger hypometabolic area on PET, and thus, a diffuse epileptogenic zone. Therefore, it might be plausible to expect a poorer surgical outcome in patients with FBTCS.

The present study has some limitations due to its retrospective design; however, this applies to all other studies on surgical outcomes. It is quite difficult to perform a prospective study on epilepsy surgery due to personal decisions that stand for randomization. Nevertheless, the present study included a quite large number of patients and good follow-up duration as compared to other studies regarding this subject.


  Conclusions Top


Many predictors for surgical outcomes in TLE have been determined to date. In the current study, we revealed that unilateral temporal IEDs on EEG, FS history, and unilateral temporal HM on FDG-PET were independent predictors of postoperative seizure control. Our findings can be useful in selection of appropriate refractory TLE patients for surgical treatment.

Declaration of patient consent

The authors certify that they have obtained all appropriate patient consent forms. In the form the patient(s) has/have given his/her/their consent for his/her/their images and other clinical information to be reported in the journal. The patients understand that their names and initials will not be published and due efforts will be made to conceal their identity, but anonymity cannot be guaranteed.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.



 
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