Can intraoperative electrocorticography be used to minimize the extent of resection in patients with temporal lobe epilepsy associated with hippocampal sclerosis?

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  • 1 Department of Neurosurgery, Juntendo University, Tokyo, Japan
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OBJECTIVE

Tailored surgery to extensively resect epileptogenic lesions using intraoperative electrocorticography (ioECoG) may improve seizure outcomes. However, resection of large areas is associated with decreased memory function postoperatively. The authors assessed whether ioECoG could provide useful information on how to minimize the focus resection and obtain better seizure outcomes without memory deterioration. They examined the postoperative seizure-free period and memory alteration in a retrospective cohort of patients with mesial temporal lobe epilepsy (TLE) due to hippocampal sclerosis (HS) in whom the extent of removal was determined using ioECoG findings.

METHODS

The authors enrolled 82 patients with TLE associated with HS who were treated surgically. Transsylvian amygdalohippocampectomy was indicated as the first step. When visual inspection identified interictal epileptic discharges from the lateral temporal lobe on ioECoG, anterior temporal lobectomy (ATL) was eventually performed. The patients were divided into the selective amygdalohippocampectomy (SA, n = 40) and ATL (n = 42) groups. Postoperative seizure outcomes were assessed at 1, 2, 3, 5, and 7 years postoperatively using the International League Against Epilepsy classification. The Kaplan-Meier survival analysis was applied to evaluate the period of seizure recurrence between the SA and ATL groups. Factors attributed to seizure recurrence were analyzed using the Cox proportional hazards model, and they were as follows: epileptic focal laterality; age at seizure onset (< 10 or ≥ 10 years old); seizure frequency (more than weekly or less than weekly seizures); history of focal to bilateral tonic-clonic seizure; infectious etiology; and surgical procedure. The Wechsler Memory Scale–Revised was used to evaluate memory function pre- and postoperatively.

RESULTS

Seizure outcomes were significantly worse in the SA group than in the ATL group at 2 years postoperatively (p = 0.045). The International League Against Epilepsy class 1 outcomes at 7 years postoperatively in the SA and ATL groups were 63% and 81%, respectively. Kaplan-Meier analysis showed that seizure recurred significantly earlier in the SA group than in the ATL group (p = 0.031). The 2-way ANOVA analysis was used to compare the SA and ATL groups in each memory category, and revealed that there was no significant difference regardless of the side of surgery.

CONCLUSIONS

Visual assessment of ioECoG cannot be used as an indicator to minimize epileptic focus resection in patients with TLE associated with HS. ATL is more effective in obtaining seizure-free outcomes; however, both ATL and SA can preserve memory function.

ABBREVIATIONS

AED = antiepileptic drug; ASO = age at seizure onset; ATL = anterior temporal lobectomy; FBTCS = focal to bilateral tonic-clonic seizure; HS = hippocampal sclerosis; ICE = intracranial electrode; IED = interictal epileptic discharge; ILAE = International League Against Epilepsy; ioECoG = intraoperative electrocorticography; SA = selective amygdalohippocampectomy; SEEG = stereotactic electroencephalography; TLE = temporal lobe epilepsy; WMS-R = Wechsler Memory Scale–Revised.

OBJECTIVE

Tailored surgery to extensively resect epileptogenic lesions using intraoperative electrocorticography (ioECoG) may improve seizure outcomes. However, resection of large areas is associated with decreased memory function postoperatively. The authors assessed whether ioECoG could provide useful information on how to minimize the focus resection and obtain better seizure outcomes without memory deterioration. They examined the postoperative seizure-free period and memory alteration in a retrospective cohort of patients with mesial temporal lobe epilepsy (TLE) due to hippocampal sclerosis (HS) in whom the extent of removal was determined using ioECoG findings.

METHODS

The authors enrolled 82 patients with TLE associated with HS who were treated surgically. Transsylvian amygdalohippocampectomy was indicated as the first step. When visual inspection identified interictal epileptic discharges from the lateral temporal lobe on ioECoG, anterior temporal lobectomy (ATL) was eventually performed. The patients were divided into the selective amygdalohippocampectomy (SA, n = 40) and ATL (n = 42) groups. Postoperative seizure outcomes were assessed at 1, 2, 3, 5, and 7 years postoperatively using the International League Against Epilepsy classification. The Kaplan-Meier survival analysis was applied to evaluate the period of seizure recurrence between the SA and ATL groups. Factors attributed to seizure recurrence were analyzed using the Cox proportional hazards model, and they were as follows: epileptic focal laterality; age at seizure onset (< 10 or ≥ 10 years old); seizure frequency (more than weekly or less than weekly seizures); history of focal to bilateral tonic-clonic seizure; infectious etiology; and surgical procedure. The Wechsler Memory Scale–Revised was used to evaluate memory function pre- and postoperatively.

RESULTS

Seizure outcomes were significantly worse in the SA group than in the ATL group at 2 years postoperatively (p = 0.045). The International League Against Epilepsy class 1 outcomes at 7 years postoperatively in the SA and ATL groups were 63% and 81%, respectively. Kaplan-Meier analysis showed that seizure recurred significantly earlier in the SA group than in the ATL group (p = 0.031). The 2-way ANOVA analysis was used to compare the SA and ATL groups in each memory category, and revealed that there was no significant difference regardless of the side of surgery.

CONCLUSIONS

Visual assessment of ioECoG cannot be used as an indicator to minimize epileptic focus resection in patients with TLE associated with HS. ATL is more effective in obtaining seizure-free outcomes; however, both ATL and SA can preserve memory function.

In Brief

The objective of this study was to find the efficacy of intraoperative electrocorticography in determining the extent of resection to obtain a better seizure outcome without memory deterioration in patients with temporal lobe epilepsy. This study confirmed that visual assessment of intraoperative electrocorticography alone could not determine the extent of resection. Hence, to concretely elucidate the epilepsy network, inclusion of computational features such as high-frequency oscillation and phase-amplitude coupling should be incorporated.

Surgical resection of epileptic foci is widely acknowledged to be effective in the management of patients with medically intractable temporal lobe epilepsy (TLE).1–3 Early surgery has been recommended for patients with hippocampal sclerosis (HS) because of its expected seizure-free outcomes.4 Although several studies have reported on whether selective amygdalohippocampectomy (SA) or anterior temporal lobectomy (ATL) contributes to seizure control, there is no consensus on which approach is better.5,6 The complication rates of SA and ATL are comparable, and it is currently recommended for surgeons to choose a technique that can be performed safely.2

Results of studies on postoperative memory function are also far from a consensus on memory alteration depending on the surgical procedure (either ATL or SA).7,8 Epilepsy involving large areas of the brain could worsen a patient’s memory. Therefore, ATL was considered to have a negative impact on postoperative memory function compared to SA. Especially in the dominant hemisphere, the lateral temporal area may have verbal memory functions and also compensates for the affected hippocampal function in patients with HS.9 Another important factor that is related to postoperative memory deterioration depends on the residual seizures. An ideal therapeutic choice is to find a rational balance between an effective minimum resection of the epileptogenic area and the maintenance of memory function.

The potential applicability of tailored surgery using intraoperative electrocorticography (ioECoG) has been proposed to achieve this balance.10,11 The advantages of tailored surgery for seizure control compared to those of standard ATL have not been clearly proven.12,13 There are some reports of improved seizure reduction in patients with HS and those with tumors who were treated with ioECoG.14–16 In addition to single-stage surgery with a tailored method, 2-stage surgeries with a combination of intracranial electrode (ICE) implantation and subsequent epileptic focal resection could be considered. Recently, a stereotactic electroencephalography (SEEG) methodology has been introduced and has been shown to be a less invasive, alternative way to elucidate epileptic areas.17 Even with SEEG, the surgical strategy is fundamentally staged. However, a single-stage surgery is more beneficial to patients. In this context, electrophysiological and imaging studies are needed to determine epileptogenic areas.

We believe that minimal resection leads to better functional preservation, and therefore we performed SA for TLE caused by HS. Before deciding to preserve temporal lobe structures other than the hippocampus, we recorded ioECoG to identify epileptic areas in the lateral temporal lobe. We hypothesized that ioECoG could provide some information on how to minimize the resected area to obtain better seizure outcomes and to maintain memory function. To test our hypothesis, we examined the seizure-free period after surgery and the degree of postoperative memory function in a cohort of patients with mesial TLE due to HS, in whom the extent of removal was determined using ioECoG findings. The difference between this study and previous studies was that ioECoG was not an indicator for additional resection but was used as a clue to restrict the extent of excision as much as possible. The amygdala and hippocampus were selectively removed using the transsylvian approach, ioECoG was recorded from the anterolateral temporal lobe, and additional lateral temporal lobe resections were performed when interictal epileptic discharges (IEDs) persisted.

Methods

Patients and Groups

We retrospectively enrolled 82 patients (including 31 male patients) with TLE due to HS who were surgically treated and followed up for at least 1 year at the epilepsy center of the Juntendo University Hospital, Tokyo, Japan, between 2005 and 2020. All patients underwent scalp video-EEG for 3 days to record their interictal and ictal epileptic discharges, and to correlate them with the seizure semiology using Neurofax (Nihon Kohden) with the 10–20 international system at a sampling rate of 500 Hz. All patients also underwent 3.0-T brain MRI and had apparent unilateral HS without any other coexisting findings. The inclusion criteria for this survey were as follows: 1) MRI showing unilateral HS without any other detectable etiologies; 2) at least 1 year of postsurgical follow-up; 3) postsurgical MRI showing adequate resection volume of hippocampus reaching to the end of the hippocampal body; 4) confirmation of HS by pathological examination of the resected hippocampal specimen; and 5) no permanent neurological sequelae after surgery. Our criteria for ICE implantation were discordant data among seizure semiology, imaging, and EEG findings. Especially in this study, some patients whose EEG abnormalities originated from extra-anterior temporal regions unilaterally and those who were suspected of having seizure semiology from outside the mesial temporal lobe underwent subdural electrode implantation.

A single neurosurgeon (H. Sugano) performed the surgeries in this study. We used the transsylvian approach to access the inferior horn of the lateral ventricle. After identifying the amygdala and hippocampus, we recorded ioECoG on the surface of the hippocampus, amygdala, and lateral temporal lobe by using platinum electrodes (Unique Medical). After resecting part of the amygdala and the hippocampus, ioECoG was again recorded on the surface of the lateral temporal lobe, and when IEDs persisted, the surgeon performed a lateral temporal lobectomy, which was restricted to 3.0 cm on the dominant side and 4.0 cm on the nondominant side from the temporal tip. We performed the standard ATL, including the superior temporal gyrus without further posterior resection, even when IEDs appeared beyond 3.0 cm on the dominant or 4.0 cm on the nondominant hemispheres on the ioECoG. Decision-making for lateral temporal resection depended on the epileptologist’s visual inspection of the ioECoG. Prior to 2015, anesthesia during ioECoG was maintained using 2.5% sevoflurane along with adequate muscle relaxants, but in 2016 this was changed to propofol. Regardless of the method of anesthesia used, we recorded the ioECoG under 40 to 50 on the bispectral index monitor values.

We classified the patients into the following two groups (SA and ATL) in order to investigate the usefulness of ioECoG by examining seizure and memory outcomes. The resected areas in the SA group were the amygdala, hippocampus, parahippocampal gyrus, and uncus; and those in the ATL group were the resection areas of the SA in addition to the superior, middle, and inferior temporal gyri, and the fusiform gyrus.

Seizure and Memory Outcome Evaluation

Postoperative seizure outcomes were assessed at 1, 2, 3, 5, and 7 years postoperatively using the International League Against Epilepsy (ILAE) classification.18 Comparisons of seizure outcomes by using the ILAE classification at each observation point were performed. The Kaplan-Meier survival analysis was applied to evaluate the period of seizure recurrence between the SA and ATL groups. The endpoint was defined as the first recurrence of seizures after surgery. We treated as a seizure recurrence not only habitual seizures but also other types of seizures associated with impairment of consciousness. Only auras with consciousness were not accounted for in the Kaplan-Meier analysis. We also determined the factors attributed to seizure recurrence by using the Cox proportional hazards model. We selected the following factors: epileptic focal laterality; age at seizure onset (ASO) (< 10 or ≥ 10 years old); seizure frequency (more than weekly or less than weekly seizures); history of focal to bilateral tonic-clonic seizure (FBTCS); infectious etiology; and surgical procedure. Patients’ antiepileptic drugs (AEDs) were never withdrawn following the 2-year period after surgery. We considered reducing the dose of AEDs with the patient’s consent after their seizures had completely ceased and when their EEGs could be considered normal. We compared the drug-free ratio between the ATL and SA groups.

The Wechsler Memory Scale–Revised (WMS-R), which consists of verbal memory, visual memory, general memory, attention, and delayed recall categories was used to evaluate memory functions before and after surgery. We compared the scores of each memory category before and after surgery, separately assessing left and right hemispheres. We also evaluated the group differences between the ATL and SA in each memory category, separately assessing left- and right-sided surgery.

Statistical Analysis

SPSS version 26.0 (IBM Japan) was used for data analysis. Before the statistical analysis, the normal distribution of numeric data was evaluated; parametric analysis was indicated for data with normal distribution, and nonparametric analysis was indicated for data with nonnormal distribution and for categorized data. The unpaired t-test or the chi-square test were used to analyze the differences in each parameter between the SA and ATL groups. Differences in seizure outcomes between the SA and ATL groups using ILAE classification at 1, 2, 3, 5, and 7 years postoperatively was evaluated using the Kruskal-Wallis test. The number of AEDs in each group before and after surgery was evaluated using the paired t-test. The Kaplan-Meier survival analysis was performed for the SA and ATL groups to determine the cumulative risks of seizure recurrence after each surgical procedure.

The Cox proportional regression analysis for seizure recurrence was performed, and the hazards ratio was calculated. WMS-R memory scores were compared before surgery between the SA and the ATL groups with respect to laterality by using an unpaired t-test. Changes in each memory score of the WMS-R before and after surgery were analyzed using the paired t-test. Comparison of the differences in each of the memory test scores between the SA and ATL groups was performed using the 2-way repeated ANOVA. Statistical significance was set at p < 0.05.

Institutional Review Board Approval

This study was a retrospective analysis, and data were obtained using the opt-in and opt-out methods. Registration and analysis were approved by the ethics committee of Juntendo University. Parents and patients consented to the collection and storage of their clinical information.

Results

Patient Characteristics

No patient had any permanent neurological sequelae such as motor paresis or aphasia after either surgery in our HS surgical series. We evaluated postsurgical MRI and confirmed adequate volume of hippocampal resection for all patients in the series.

The number of patients, their sex, ASO, age at surgery, laterality of epileptic focus, number with infectious etiology, number with FBTCS, seizure frequency, number of AEDs, and number of ICE implantations in each group are shown in Table 1. There was no difference in these factors between the two groups, except in seizure frequency. The ATL group had frequent seizures that were more than weekly (p < 0.01). The number of ICE implantations tended to be higher in the ATL group, but this difference was not statistically significant.

TABLE 1.

Characteristics of patients in this study

SAATLp Value
No. (female)40 (26)42 (25)NA
Median FU in days234424910.825
ASO in yrs (mean ± SD)14.8 ± 8.818.8 ± 13.10.111
Age in yrs at surgery (mean ± SD)34.4 ± 13.934.6 ± 14.90.945
Laterality of focus (lt:rt)26:1422:200.246
Infectious etiology5120.073
FBTCS15170.782
Seizure frequency (≥ weekly)15310.002*
No. of AEDs (mean ± SD)2.35 ± 0.92.29 ± 0.80.775
ICE implantation490.097

FU = follow-up; NA = not applicable.

The clinical characteristics in the SA and ATL groups were the same, except for seizure frequency. The ATL group had more patients with frequent seizures than the SA group. Infectious cause and ICE implantation tended to be higher in the ATL group, but these differences were not statistically significant.

Statistically significant (p < 0.05).

Seizure Outcome Following SA and ATL

The seizure outcomes using the ILAE classification at 1, 2, 3, 5, and 7 years postoperatively are shown in Fig. 1. The seizure outcome was significantly worse in the SA group than in the ATL group 2 years postoperatively (p = 0.045). The ILAE class 1 outcomes 7 years postoperatively were 12/19 (63%) and 17/21 (81%) patients in the SA and ATL groups, respectively. Three patients in the SA group and 1 patient in the ATL group relapsed when their AEDs were reduced, and they became seizure-free again after returning to the previous AED prescription. Remodifying the AED prescription after seizure recurrence succeeded in restoring a seizure-free state in 11 patients in the SA group and in 6 patients in the ATL group. The number of AEDs was significantly reduced from 2.3 ± 0.8 to 1.3 ± 1.1 (p = 0.03) in the ATL group. In the SA group, the number of AEDs was also reduced from 2.4 ± 0.9 to 1.6 ± 1.1 (p < 0.01). Discontinuation of AEDs was achieved in 12 patients (28.6%) in the ATL group and in 7 patients (17.5%) in the SA group.

FIG. 1.
FIG. 1.

ILAE classification result in the SA and ATL groups. Seizure outcome combined with class 1 and 2 in the ILAE classification gradually deteriorated in the SA groups. The Kruskal-Wallis test showed a statistically significant difference between the SA and ATL groups at 2 years postoperatively (p = 0.045). Left: ILAE classification results of the SA group. Right: ILAE classification results of the ATL group.

The Kaplan-Meier analysis showed that seizure recurrence occurred significantly earlier in the SA group than in the ATL group (p = 0.031) (Fig. 2). The estimated time of seizure recurrence was 2458 days (95% CI 1874–3043 days) in the SA group and 4647 days (95% CI 3937–5356 days) in the ATL group. The Cox proportional regression hazards model for seizure recurrence revealed that infectious etiology and type of surgical procedure (ATL) were significant factors (Table 2). The hazard ratios for seizure recurrence of infectious etiology and surgical procedure type were 4.050 and 0.494, respectively.

FIG. 2.
FIG. 2.

Kaplan-Meier analysis for seizure recurrence. Kaplan-Meier analysis with the log-rank method shows that patients in the SA group experienced a relapse of their seizures earlier than those in the ATL group, with a statistically significant difference (p = 0.031). The endpoint of this analysis was when the patient experienced recurrence of habitual seizures and/or impaired awareness seizures.

TABLE 2.

Cox regression analysis related to seizure recurrence in patients with TLE

p ValueHazard Ratio95% CI
Epileptic focus laterality0.369NANA
Age at seizure onset (≤10 yrs)0.879NANA
Seizure frequency (≥ weekly)0.660NANA
FBTCS0.662NANA
Infectious etiology0.008*4.0501.440–11.391
Surgical procedure (ATL)0.013*0.4940.284–0.861

Infectious etiology and surgical procedure type were significant factors for seizure recurrence.

Statistically significant (p < 0.05).

Postsurgical Memory Function

Memory function was compared by WMS-R before and after surgery for patients with left TLE in the ATL (n = 12) and SA (n = 18) groups. Postoperative WMS-R was performed a median of 1.0 year after surgery. The number of patients with right TLE in whom evaluation with the WMS-R was performed before and after surgery was 10 in the ATL group and 9 in the SA group. The postoperative WMS-R was performed a median of 1.1 years after surgery. Preoperative memory scores on WMS-R evaluation revealed no significant group differences between SA and ATL for each hemisphere.

In this study, most memory categories were unchanged after surgery, but some categories showed significant differences (Table 3). In left-sided surgeries, delayed recall significantly improved after both surgeries. In right-sided surgery, both the SA and ATL groups showed significant improvements in verbal and general memorization. The 2-way ANOVA that was used to compare the SA and ATL groups in each memory category revealed no significant difference between sides of surgery.

TABLE 3.

Comparisons of memory outcomes using WMS-R in patients with TLE

Memory OutcomeSAATL
BeforeAfterBeforeAfter
Lt-sided op
 Verbal memory80.9 ± 15.682.9 ± 18.071.9 ± 13.473.3 ± 16.3
 Visual memory95.7 ± 17.8101.2 ± 13.183.3 ± 17.393.4 ± 20.6
 General memory82.4 ± 17.286.0 ± 18.271.9 ± 13.977.6 ± 16.2*
 Attention97.1 ± 17.9100.8 ± 17.390.0 ± 15.392.8 ± 17.0
 Delayed recall76.1 ± 14.886.1 ± 17.6*69.4 ± 16.377.6 ± 20.6*
Rt-sided op
 Verbal memory80.3 ± 18.285.9 ± 20.9*86.0 ± 18.496.8 ± 16.1*
 Visual memory91.8 ± 19.599.1 ± 21.293.7 ± 18.596.3 ± 18.3
 General memory80.9 ± 19.887.6 ± 22.9*85.0 ± 20.695.5 ± 17.7*
 Attention89.4 ± 20.093.8 ± 20.098.5 ± 14.0102.7 ± 15.5
 Delayed recall78.2 ± 20.086.1 ± 24.185.6 ± 18.393.6 ± 16.9

For left-sided surgery, delayed recall significantly improved after both surgery types. The general memory improved after ATL. For right-sided surgery, both the SA and ATL groups showed significant improvement in verbal and general memory.

Statistically significant (p < 0.05).

Discussion

Patient Characteristics of the SA and ATL Groups

The characteristics of the SA and ATL groups in this study were generally uniform because strict inclusion criteria were used in selecting the participants to determine the utility of ioECoG. Patents in the ATL group had a tendency to develop severe epilepsy because of higher seizure frequency and a slightly higher requirement for ICE implantation. The main reason for ICE implantation in this study was to make an assessment after a scalp EEG showed a wide distribution beyond the unilateral anterior temporal lobe. This phenomenon might be related to the fact that IEDs remained in the lateral temporal lobe in the ioECoG, which is an indicator of ATL. In addition, both groups had no difference in etiology, presence of FBTCS, or ASO. Therefore, it can be deduced that ioECoG findings were the single indicator to determine whether or not to resect the lateral temporal lobe in this study.

Seizure Outcome Following SA and ATL

While some studies demonstrated similar seizure outcomes after ATL and SA, some meta-analyses have revealed that ATL has superior seizure freedom results compared to SA.5,19–23 Our data were similar to those of previous reports. Our result suggests that the lateral temporal lobe is involved in one of the important epileptic networks in patients with TLE caused by HS. For lesional TLEs caused by brain tumor, focal cortical dysplasia, amygdala enlargement, and cavernous angiomas it is known that the hippocampus is a part of the epilepsy network, and the treatment of both hippocampus and the lesion is recommended to obtain good seizure control.15,24 The controversy whether TLE with HS is a strictly focal epilepsy or a network-based mechanism has not been resolved. We should consider an epileptic mechanism with functional and/or pathological networking.25–28 When considering the seizure mechanism based on the epilepsy network, cases in which seizures ceased after SA are those in which the epileptic network was limited to the resected structures, whereas cases that require ATL are those with a wider network. We should also consider the running-down phenomenon after epileptic focus resection.29 Even if seizures recurred, the seizures of some patients could be controlled by modifying their AEDs in both groups, especially in the SA group. This means that the residual epileptic network located in the lateral temporal lobe can be controlled using prompt AED treatment.30

The clinical factors related to seizure recurrence have been reported to include the following: FBTCS, infectious etiology, early ASO or longer epilepsy duration, and temporal plus epilepsy.31–33 In our factor analysis, the infectious etiology and type of surgical procedure were proven to be independent predictors of early seizure recurrence after surgery. Infections such as meningitis and encephalitis are known to be an etiology of difficult to treat forms of epilepsy.31 In general, inflammation caused by infection affects broad temporal and/or extratemporal regions. Although we strictly selected patients with only HS in this study, inflammatory changes could have involved broader areas with resulting extension of epileptogenicity.

In this study, ioECoG findings were the information source for the decision to perform an additional lateral temporal lobectomy. Our visual inspection of ioECoG could not identify hidden epileptogenicity; therefore, we concluded that ioECoG had a limited value for decision-making on preservation of lateral temporal lobe. In order to improve the accuracy of ioECoG beyond visual inspection, high-frequency oscillation analysis has been added for detecting epileptogenic zones even during intraoperative recordings.34,35 In addition, computational features of electrophysiological findings, such as phase-amplitude coupling and entropy have recently attracted attention due to their ability to reveal epileptogenicity.36,37 These EEG computational modalities could be used for ioECoG records in the future. We should consider that some patients who underwent ATL could have had the same seizure outcome if they had undergone the SA, because it is possible for false-positive spikes in the ioECoG to have been perceived during our visual assessment.

Postsurgical Memory Function

Our results showed that there was no difference in memory function changes between the SA and ATL groups. A systematic review showed no difference in intelligence outcomes between these surgical procedures.20 Sauvigny et al. reported that ATL after SA in patients with residual seizures resulted in improved seizure control and preserved memory function.38 The meaning of these reports reflected similar findings to ours. In this study we evaluated the change of memory function for each surgical technique, comparing left and right hemispheres. However, it is important to note that the ATL group had a higher preoperative seizure frequency than the SA group (Table 1), and also had worse preoperative memory function performance on the dominant side (Table 3). Therefore, we should consider that the ATL group might have had a wider range of epileptic network involvement and extent of neurological damage. Lobectomy for the already damaged area might have preserved memory function, whereas eventually normal temporal structure resection would have impaired it.

It has been reported that visual confrontation naming is affected following ATL, particularity involving the left superior temporal gyrus, and recognition of famous faces is impaired after right-sided ATL.39 These functions are probably due to wide connectivity mainly in lateral temporal lobes, which was not evaluated by our current neurophysiological battery.40 Therefore, our resection of lateral temporal lobe was restricted to within 3.0 cm from temporal tip in the dominant and 4.0 cm in the nondominant hemispheres. A minimal resection could possibly preserve neural function. We should meticulously evaluate the long-term outcomes following different resection techniques with respect to seizure, memory, speech, and psychological deficit.

Another finding on memory evaluation was that both groups showed improvement in verbal memory after surgery in patients with right TLE. This is also the same result as in a previous report.29 In general, surgery on the left side is thought to deteriorate verbal memory, whereas that on the right side is thought to reduce visual memory.41,42 Another accepted result is that limiting the extent of resection had a favorable effect on postoperative memory ability.43 In our study, all memory category results never declined in spite of laterality. Helmstaedter et al. reported long-term cognitive outcomes in patients with TLE and found recovered verbal memory, achievement of seizure-free outcomes, and reduction in AEDs.44 It is also noteworthy in our evaluation that patients with left TLE showed significant improvement in delayed recall after surgery. Waldman et al. reported that ripples in the neocortex of the dominant temporal lobe were associated with verbal memory function; and they are considered normal physiological ripples.45 The physiological ripples are associated with verbal and recall memory functions that can be impaired by the interference of pathological ripples from epileptic areas. Therefore, ATL could modulate physiological ripples and result in delayed improvement in memory.

Limitations

In the first half of this study, anesthesia during ioECoG was achieved using sevoflurane; however, we used propofol in the second half. We could not determine the difference in the ioECoG findings using visual inspection; therefore, we used the findings regardless of which anesthetic agent patients received in this study.

Given that we did not use the WMS-R for memory evaluation at the beginning of this study, the number of comparisons on memory function was relatively small. In order to determine whether surgical procedures affect memory function, particularly in the longer term, evaluation of serial memory tests is required. Nevertheless, we found no changes when comparing memory function at approximately 1 year (median) after operation. The language function, especially naming, had deteriorated after dominant-side ATL; imaging recognition, especially for faces, was impaired by nondominant-hemisphere ATL.39 These effects were not systematically examined in this study—rather they were inferred from the verbal and visual memory results of the WMS-R.

Conclusions

This study showed that visual assessment of ioECoG was not contributing to minimize the resection of epileptic foci in patients with TLE associated with HS. ATL provided a better rate of seizure-free outcomes, and ATL and SA both preserved memory function. Although the visual ioECoG analysis could not assess the extent of the epilepsy network, there are still expectations for ioECoG to contribute to the improvement of surgical outcomes. It will be necessary to elucidate the epilepsy network by using computational analyses to obtain objective biomarkers.

Acknowledgments

This study was made possible thanks to the advice of neuropsychologist Dr. Keiko Fusegi. This study was supported by Health and Labor Sciences research grants on rare and intractable diseases to Dr. Sugano from the Ministry of Health, Labor and Welfare, Japan (H29-nanchitou-ippan-010); JST CREST (grant no. JPMJCR20F1); and Kaken-hi (grant no. 21K09160).

Disclosures

The authors report no conflict of interest concerning the materials or methods used in this study or the findings specified in this paper.

Author Contributions

Conception and design: Sugano, Iimura. Acquisition of data: Sugano, Iimura, Suzuki, Mitsuhashi, Higo, Ueda, Nishioka. Analysis and interpretation of data: Sugano, Iimura, Suzuki, Tamrakar. Drafting the article: Sugano. Critically revising the article: Sugano, Tamrakar, Karagiozov, Nakajima. Reviewed submitted version of manuscript: Sugano, Iimura, Karagiozov, Nakajima. Approved the final version of the manuscript on behalf of all authors: Sugano. Statistical analysis: Sugano, Iimura. Administrative/technical/material support: Sugano, Suzuki, Tamrakar, Mitsuhashi, Karagiozov, Nakajima. Study supervision: Sugano, Nakajima.

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    • Export Citation
  • 10

    Burkholder DB, Sulc V, Hoffman EM, Cascino GD, Britton JW, So EL, et al. Interictal scalp electroencephalography and intraoperative electrocorticography in magnetic resonance imaging-negative temporal lobe epilepsy surgery. JAMA Neurol. 2014;71(6):702709.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 11

    Grewal SS, Alvi MA, Perkins WJ, Cascino GD, Britton JW, Burkholder DB, et al. Reassessing the impact of intraoperative electrocorticography on postoperative outcome of patients undergoing standard temporal lobectomy for MRI-negative temporal lobe epilepsy. J Neurosurg. 2019;132(2):605614.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 12

    Falowski SM, Wallace D, Kanner A, Smith M, Rossi M, Balabanov A, et al. Tailored temporal lobectomy for medically intractable epilepsy: evaluation of pathology and predictors of outcome. Neurosurgery. 2012;71(3):703709.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 13

    San-juan D, Tapia CA, González-Aragón MF, Martínez Mayorga A, Staba RJ, Alonso-Vanegas M. The prognostic role of electrocorticography in tailored temporal lobe surgery. Seizure. 2011;20(7):564569.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 14

    Roessler K, Heynold E, Buchfelder M, Stefan H, Hamer HM. Current value of intraoperative electrocorticography (iopECoG). Epilepsy Behav. 2019;91:2024.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 15

    Sugano H, Shimizu H, Sunaga S. Efficacy of intraoperative electrocorticography for assessing seizure outcomes in intractable epilepsy patients with temporal-lobe-mass lesions. Seizure. 2007;16(2):120127.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 16

    Yao PS, Zheng SF, Wang F, Kang DZ, Lin YX. Surgery guided with intraoperative electrocorticography in patients with low-grade glioma and refractory seizures. J Neurosurg. 2018;128(3):840845.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 17

    Dührsen L, Sauvigny T, Ricklefs FL, Hamel W, Koeppen JA, Hebel JM, et al. Decision-making in temporal lobe epilepsy surgery based on invasive stereo-electroencephalography (sEEG). Neurosurg Rev. 2020;43(5):14031408.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 18

    Wieser HG, Blume WT, Fish D, Goldensohn E, Hufnagel A, King D, et al. ILAE Commission Report. Proposal for a new classification of outcome with respect to epileptic seizures following epilepsy surgery. Epilepsia. 2001;42(2):282286.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 19

    Bauman K, Devinsky O, Liu AA. Temporal lobe surgery and memory: lessons, risks, and opportunities. Epilepsy Behav. 2019;101(Pt A):106596.

  • 20

    Hu WH, Zhang C, Zhang K, Meng FG, Chen N, Zhang JG. Selective amygdalohippocampectomy versus anterior temporal lobectomy in the management of mesial temporal lobe epilepsy: a meta-analysis of comparative studies. J Neurosurg. 2013;119(5):10891097.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 21

    Dorfer C, Czech T, Aull-Watschinger S, Baumgartner C, Jung R, Kasprian G, et al. Mesial temporal lobe epilepsy: long-term seizure outcome of patients primarily treated with transsylvian selective amygdalohippocampectomy. J Neurosurg. 2018;129(1):174181.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 22

    Elsharkawy AE, Alabbasi AH, Pannek H, Oppel F, Schulz R, Hoppe M, et al. Long-term outcome after temporal lobe epilepsy surgery in 434 consecutive adult patients. J Neurosurg. 2009;110(6):11351146.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 23

    Lee AT, Burke JF, Chunduru P, Molinaro AM, Knowlton R, Chang EF. A historical cohort of temporal lobe surgery for medically refractory epilepsy: a systematic review and meta-analysis to guide future nonrandomized controlled trial studies. J Neurosurg. 2019;133(1):7178.

    • Search Google Scholar
    • Export Citation
  • 24

    Nowak A, Rysz A, Dziedzic T, Czernicki T, Kunert P, Maj E, Marchel A. Predictors of Class I epilepsy surgery outcome in tumour-related chronic temporal lobe epilepsy in adults. Neurol Neurochir Pol. 2019;53(6):466475.

    • Search Google Scholar
    • Export Citation
  • 25

    Abel TJ, Woodroffe RW, Nourski KV, Moritani T, Capizzano AA, Kirby P, et al. Role of the temporal pole in temporal lobe epilepsy seizure networks: an intracranial electrode investigation. J Neurosurg. 2018;129(1):165173.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 26

    Busby N, Halai AD, Parker GJM, Coope DJ, Lambon Ralph MA. Mapping whole brain connectivity changes: the potential impact of different surgical resection approaches for temporal lobe epilepsy. Cortex. 2019;113:114.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 27

    Foesleitner O, Sigl B, Schmidbauer V, Nenning KH, Pataraia E, Bartha-Doering L, et al. Language network reorganization before and after temporal lobe epilepsy surgery. J Neurosurg. 2020;134(6):16941702.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 28

    Larivière S, Weng Y, Vos de Wael R, Royer J, Frauscher B, Wang Z, et al. Functional connectome contractions in temporal lobe epilepsy: microstructural underpinnings and predictors of surgical outcome. Epilepsia. 2020;61(6):12211233.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 29

    Schmeiser B, Hammen T, Steinhoff BJ, Zentner J, Schulze-Bonhage A. Long-term outcome characteristics in mesial temporal lobe epilepsy with and without associated cortical dysplasia. Epilepsy Res. 2016;126:147156.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 30

    Sheikh SR, Nair D, Gross RE, Gonzalez-Martinez J. Tracking a changing paradigm and the modern face of epilepsy surgery: a comprehensive and critical review on the hunt for the optimal extent of resection in mesial temporal lobe epilepsy. Epilepsia. 2019;60(9):17681793.

    • Search Google Scholar
    • Export Citation
  • 31

    Barba C, Rheims S, Minotti L, Guénot M, Hoffmann D, Chabardès S, et al. Temporal plus epilepsy is a major determinant of temporal lobe surgery failures. Brain. 2016;139(Pt 2):444451.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 32

    Barba C, Minotti L, Job AS, Kahane P. The insula in temporal plus epilepsy. J Clin Neurophysiol. 2017;34(4):324327.

  • 33

    Janszky J, Janszky I, Schulz R, Hoppe M, Behne F, Pannek HW, Ebner A. Temporal lobe epilepsy with hippocampal sclerosis: predictors for long-term surgical outcome. Brain. 2005;128(Pt 2):395404.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 34

    Weiss SA, Berry B, Chervoneva I, Waldman Z, Guba J, Bower M, et al. Visually validated semi-automatic high-frequency oscillation detection aides the delineation of epileptogenic regions during intra-operative electrocorticography. Clin Neurophysiol. 2018;129(10):20892098.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 35

    Zweiphenning WJ, van ’t Klooster MA, van Diessen E, van Klink NE, Huiskamp GJ, Gebbink TA, et al. High frequency oscillations and high frequency functional network characteristics in the intraoperative electrocorticogram in epilepsy. Neuroimage Clin. 2016;12:928939.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 36

    Demuru M, Kalitzin S, Zweiphenning W, van Blooijs D, Van’t Klooster M, Van Eijsden P, et al. The value of intra-operative electrographic biomarkers for tailoring during epilepsy surgery: from group-level to patient-level analysis. Sci Rep. 2020;10(1):14654.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 37

    Zhang R, Ren Y, Liu C, Xu N, Li X, Cong F, et al. Temporal-spatial characteristics of phase-amplitude coupling in electrocorticogram for human temporal lobe epilepsy. Clin Neurophysiol. 2017;128(9):17071718.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 38

    Sauvigny T, Brückner K, Dührsen L, Heese O, Westphal M, Stodieck SR, Martens T. Neuropsychological performance and seizure control after subsequent anteromesial temporal lobe resection following selective amygdalohippocampectomy. Epilepsia. 2016;57(11):17891797.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 39

    Rice GE, Caswell H, Moore P, Hoffman P, Lambon Ralph MA. The roles of left versus right anterior temporal lobes in semantic memory: a neuropsychological comparison of postsurgical temporal lobe epilepsy patients. Cereb Cortex. 2018;28(4):14871501.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 40

    Hermann BP, Perrine K, Chelune GJ, Barr W, Loring DW, Strauss E, et al. Visual confrontation naming following left anterior temporal lobectomy: a comparison of surgical approaches. Neuropsychology. 1999;13(1):39.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 41

    Helmstaedter C, Richter S, Röske S, Oltmanns F, Schramm J, Lehmann TN. Differential effects of temporal pole resection with amygdalohippocampectomy versus selective amygdalohippocampectomy on material-specific memory in patients with mesial temporal lobe epilepsy. Epilepsia. 2008;49(1):8897.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 42

    Foged MT, Vinter K, Stauning L, Kjær TW, Ozenne B, Beniczky S, et al. Verbal learning and memory outcome in selective amygdalohippocampectomy versus temporal lobe resection in patients with hippocampal sclerosis. Epilepsy Behav. 2018;79:180187.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 43

    Morino M, Uda T, Naito K, Yoshimura M, Ishibashi K, Goto T, et al. Comparison of neuropsychological outcomes after selective amygdalohippocampectomy versus anterior temporal lobectomy. Epilepsy Behav. 2006;9(1):95100.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 44

    Helmstaedter C, Elger CE, Vogt VL. Cognitive outcomes more than 5 years after temporal lobe epilepsy surgery: remarkable functional recovery when seizures are controlled. Seizure. 2018;62:116123.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 45

    Waldman ZJ, Camarillo-Rodriguez L, Chervenova I, Berry B, Shimamoto S, Elahian B, et al. Ripple oscillations in the left temporal neocortex are associated with impaired verbal episodic memory encoding. Epilepsy Behav. 2018;88:3340.

    • PubMed
    • Search Google Scholar
    • Export Citation

Images from Minchev et al. (pp 479–488).

  • View in gallery

    ILAE classification result in the SA and ATL groups. Seizure outcome combined with class 1 and 2 in the ILAE classification gradually deteriorated in the SA groups. The Kruskal-Wallis test showed a statistically significant difference between the SA and ATL groups at 2 years postoperatively (p = 0.045). Left: ILAE classification results of the SA group. Right: ILAE classification results of the ATL group.

  • View in gallery

    Kaplan-Meier analysis for seizure recurrence. Kaplan-Meier analysis with the log-rank method shows that patients in the SA group experienced a relapse of their seizures earlier than those in the ATL group, with a statistically significant difference (p = 0.031). The endpoint of this analysis was when the patient experienced recurrence of habitual seizures and/or impaired awareness seizures.

  • 1

    Choi H, Sell RL, Lenert L, Muennig P, Goodman RR, Gilliam FG, Wong JB. Epilepsy surgery for pharmacoresistant temporal lobe epilepsy: a decision analysis. JAMA. 2008;300(21):24972505.

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  • 2

    Jobst BC, Cascino GD. Resective epilepsy surgery for drug-resistant focal epilepsy: a review. JAMA. 2015;313(3):285293.

  • 3

    Lamberink HJ, Otte WM, Blümcke I, Braun KPJ. Seizure outcome and use of antiepileptic drugs after epilepsy surgery according to histopathological diagnosis: a retrospective multicentre cohort study. Lancet Neurol. 2020;19(9):748757.

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  • 4

    Engel J Jr, McDermott MP, Wiebe S, Langfitt JT, Stern JM, Dewar S, et al. Early surgical therapy for drug-resistant temporal lobe epilepsy: a randomized trial. JAMA. 2012;307(9):922930.

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  • 5

    Josephson CB, Dykeman J, Fiest KM, Liu X, Sadler RM, Jette N, Wiebe S. Systematic review and meta-analysis of standard vs selective temporal lobe epilepsy surgery. Neurology. 2013;80(18):16691676.

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  • 6

    Schramm J. Temporal lobe epilepsy surgery and the quest for optimal extent of resection: a review. Epilepsia. 2008;49(8):12961307.

  • 7

    Gleissner U, Helmstaedter C, Schramm J, Elger CE. Memory outcome after selective amygdalohippocampectomy: a study in 140 patients with temporal lobe epilepsy. Epilepsia. 2002;43(1):8795.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 8

    Morino M, Ichinose T, Uda T, Kondo K, Ohfuji S, Ohata K. Memory outcome following transsylvian selective amygdalohippocampectomy in 62 patients with hippocampal sclerosis. J Neurosurg. 2009;110(6):11641169.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 9

    Alpherts WC, Vermeulen J, van Rijen PC, da Silva FH, van Veelen CW. Standard versus tailored left temporal lobe resections: differences in cognitive outcome?. Neuropsychologia. 2008;46(2):455460.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 10

    Burkholder DB, Sulc V, Hoffman EM, Cascino GD, Britton JW, So EL, et al. Interictal scalp electroencephalography and intraoperative electrocorticography in magnetic resonance imaging-negative temporal lobe epilepsy surgery. JAMA Neurol. 2014;71(6):702709.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 11

    Grewal SS, Alvi MA, Perkins WJ, Cascino GD, Britton JW, Burkholder DB, et al. Reassessing the impact of intraoperative electrocorticography on postoperative outcome of patients undergoing standard temporal lobectomy for MRI-negative temporal lobe epilepsy. J Neurosurg. 2019;132(2):605614.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 12

    Falowski SM, Wallace D, Kanner A, Smith M, Rossi M, Balabanov A, et al. Tailored temporal lobectomy for medically intractable epilepsy: evaluation of pathology and predictors of outcome. Neurosurgery. 2012;71(3):703709.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 13

    San-juan D, Tapia CA, González-Aragón MF, Martínez Mayorga A, Staba RJ, Alonso-Vanegas M. The prognostic role of electrocorticography in tailored temporal lobe surgery. Seizure. 2011;20(7):564569.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 14

    Roessler K, Heynold E, Buchfelder M, Stefan H, Hamer HM. Current value of intraoperative electrocorticography (iopECoG). Epilepsy Behav. 2019;91:2024.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 15

    Sugano H, Shimizu H, Sunaga S. Efficacy of intraoperative electrocorticography for assessing seizure outcomes in intractable epilepsy patients with temporal-lobe-mass lesions. Seizure. 2007;16(2):120127.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 16

    Yao PS, Zheng SF, Wang F, Kang DZ, Lin YX. Surgery guided with intraoperative electrocorticography in patients with low-grade glioma and refractory seizures. J Neurosurg. 2018;128(3):840845.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 17

    Dührsen L, Sauvigny T, Ricklefs FL, Hamel W, Koeppen JA, Hebel JM, et al. Decision-making in temporal lobe epilepsy surgery based on invasive stereo-electroencephalography (sEEG). Neurosurg Rev. 2020;43(5):14031408.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 18

    Wieser HG, Blume WT, Fish D, Goldensohn E, Hufnagel A, King D, et al. ILAE Commission Report. Proposal for a new classification of outcome with respect to epileptic seizures following epilepsy surgery. Epilepsia. 2001;42(2):282286.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 19

    Bauman K, Devinsky O, Liu AA. Temporal lobe surgery and memory: lessons, risks, and opportunities. Epilepsy Behav. 2019;101(Pt A):106596.

  • 20

    Hu WH, Zhang C, Zhang K, Meng FG, Chen N, Zhang JG. Selective amygdalohippocampectomy versus anterior temporal lobectomy in the management of mesial temporal lobe epilepsy: a meta-analysis of comparative studies. J Neurosurg. 2013;119(5):10891097.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 21

    Dorfer C, Czech T, Aull-Watschinger S, Baumgartner C, Jung R, Kasprian G, et al. Mesial temporal lobe epilepsy: long-term seizure outcome of patients primarily treated with transsylvian selective amygdalohippocampectomy. J Neurosurg. 2018;129(1):174181.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 22

    Elsharkawy AE, Alabbasi AH, Pannek H, Oppel F, Schulz R, Hoppe M, et al. Long-term outcome after temporal lobe epilepsy surgery in 434 consecutive adult patients. J Neurosurg. 2009;110(6):11351146.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 23

    Lee AT, Burke JF, Chunduru P, Molinaro AM, Knowlton R, Chang EF. A historical cohort of temporal lobe surgery for medically refractory epilepsy: a systematic review and meta-analysis to guide future nonrandomized controlled trial studies. J Neurosurg. 2019;133(1):7178.

    • Search Google Scholar
    • Export Citation
  • 24

    Nowak A, Rysz A, Dziedzic T, Czernicki T, Kunert P, Maj E, Marchel A. Predictors of Class I epilepsy surgery outcome in tumour-related chronic temporal lobe epilepsy in adults. Neurol Neurochir Pol. 2019;53(6):466475.

    • Search Google Scholar
    • Export Citation
  • 25

    Abel TJ, Woodroffe RW, Nourski KV, Moritani T, Capizzano AA, Kirby P, et al. Role of the temporal pole in temporal lobe epilepsy seizure networks: an intracranial electrode investigation. J Neurosurg. 2018;129(1):165173.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 26

    Busby N, Halai AD, Parker GJM, Coope DJ, Lambon Ralph MA. Mapping whole brain connectivity changes: the potential impact of different surgical resection approaches for temporal lobe epilepsy. Cortex. 2019;113:114.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 27

    Foesleitner O, Sigl B, Schmidbauer V, Nenning KH, Pataraia E, Bartha-Doering L, et al. Language network reorganization before and after temporal lobe epilepsy surgery. J Neurosurg. 2020;134(6):16941702.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 28

    Larivière S, Weng Y, Vos de Wael R, Royer J, Frauscher B, Wang Z, et al. Functional connectome contractions in temporal lobe epilepsy: microstructural underpinnings and predictors of surgical outcome. Epilepsia. 2020;61(6):12211233.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 29

    Schmeiser B, Hammen T, Steinhoff BJ, Zentner J, Schulze-Bonhage A. Long-term outcome characteristics in mesial temporal lobe epilepsy with and without associated cortical dysplasia. Epilepsy Res. 2016;126:147156.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 30

    Sheikh SR, Nair D, Gross RE, Gonzalez-Martinez J. Tracking a changing paradigm and the modern face of epilepsy surgery: a comprehensive and critical review on the hunt for the optimal extent of resection in mesial temporal lobe epilepsy. Epilepsia. 2019;60(9):17681793.

    • Search Google Scholar
    • Export Citation
  • 31

    Barba C, Rheims S, Minotti L, Guénot M, Hoffmann D, Chabardès S, et al. Temporal plus epilepsy is a major determinant of temporal lobe surgery failures. Brain. 2016;139(Pt 2):444451.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 32

    Barba C, Minotti L, Job AS, Kahane P. The insula in temporal plus epilepsy. J Clin Neurophysiol. 2017;34(4):324327.

  • 33

    Janszky J, Janszky I, Schulz R, Hoppe M, Behne F, Pannek HW, Ebner A. Temporal lobe epilepsy with hippocampal sclerosis: predictors for long-term surgical outcome. Brain. 2005;128(Pt 2):395404.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 34

    Weiss SA, Berry B, Chervoneva I, Waldman Z, Guba J, Bower M, et al. Visually validated semi-automatic high-frequency oscillation detection aides the delineation of epileptogenic regions during intra-operative electrocorticography. Clin Neurophysiol. 2018;129(10):20892098.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 35

    Zweiphenning WJ, van ’t Klooster MA, van Diessen E, van Klink NE, Huiskamp GJ, Gebbink TA, et al. High frequency oscillations and high frequency functional network characteristics in the intraoperative electrocorticogram in epilepsy. Neuroimage Clin. 2016;12:928939.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 36

    Demuru M, Kalitzin S, Zweiphenning W, van Blooijs D, Van’t Klooster M, Van Eijsden P, et al. The value of intra-operative electrographic biomarkers for tailoring during epilepsy surgery: from group-level to patient-level analysis. Sci Rep. 2020;10(1):14654.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 37

    Zhang R, Ren Y, Liu C, Xu N, Li X, Cong F, et al. Temporal-spatial characteristics of phase-amplitude coupling in electrocorticogram for human temporal lobe epilepsy. Clin Neurophysiol. 2017;128(9):17071718.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 38

    Sauvigny T, Brückner K, Dührsen L, Heese O, Westphal M, Stodieck SR, Martens T. Neuropsychological performance and seizure control after subsequent anteromesial temporal lobe resection following selective amygdalohippocampectomy. Epilepsia. 2016;57(11):17891797.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 39

    Rice GE, Caswell H, Moore P, Hoffman P, Lambon Ralph MA. The roles of left versus right anterior temporal lobes in semantic memory: a neuropsychological comparison of postsurgical temporal lobe epilepsy patients. Cereb Cortex. 2018;28(4):14871501.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 40

    Hermann BP, Perrine K, Chelune GJ, Barr W, Loring DW, Strauss E, et al. Visual confrontation naming following left anterior temporal lobectomy: a comparison of surgical approaches. Neuropsychology. 1999;13(1):39.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 41

    Helmstaedter C, Richter S, Röske S, Oltmanns F, Schramm J, Lehmann TN. Differential effects of temporal pole resection with amygdalohippocampectomy versus selective amygdalohippocampectomy on material-specific memory in patients with mesial temporal lobe epilepsy. Epilepsia. 2008;49(1):8897.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 42

    Foged MT, Vinter K, Stauning L, Kjær TW, Ozenne B, Beniczky S, et al. Verbal learning and memory outcome in selective amygdalohippocampectomy versus temporal lobe resection in patients with hippocampal sclerosis. Epilepsy Behav. 2018;79:180187.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 43

    Morino M, Uda T, Naito K, Yoshimura M, Ishibashi K, Goto T, et al. Comparison of neuropsychological outcomes after selective amygdalohippocampectomy versus anterior temporal lobectomy. Epilepsy Behav. 2006;9(1):95100.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 44

    Helmstaedter C, Elger CE, Vogt VL. Cognitive outcomes more than 5 years after temporal lobe epilepsy surgery: remarkable functional recovery when seizures are controlled. Seizure. 2018;62:116123.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 45

    Waldman ZJ, Camarillo-Rodriguez L, Chervenova I, Berry B, Shimamoto S, Elahian B, et al. Ripple oscillations in the left temporal neocortex are associated with impaired verbal episodic memory encoding. Epilepsy Behav. 2018;88:3340.

    • PubMed
    • Search Google Scholar
    • Export Citation

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