CRITICAL REVIEW AND INVITED COMMENTARY

Epilepsy surgery in patients with bilateral temporal lobe seizures: A systematic review *Yahya Aghakhani, †Xiaorong Liu, *‡Nathalie Jette, and *‡Samuel Wiebe Epilepsia, **(*):1–10, 2014 doi: 10.1111/epi.12856

SUMMARY

Dr. Yahya Aghakhani, is Assistant Professor of Neurology at the University of Calgary.

We explored the association between magnetic resonance imaging (MRI) lesion, degree of seizure laterality on intracranial electroencephalography (iEEG), and seizure outcome in patients with ambiguous or presumed bilateral temporal lobe epilepsy (BiTLE) on scalp EEG. We systematically reviewed the literature using Embase and MEDLINE up to May 31, 2012. Patients with bilateral iEEG, temporal lobe surgery, and follow-up ≥1 year were included. We undertook three separate analyses on patients whose scalp EEG showed ambiguous onset or BiTLE (1) group data of those whose iEEG demonstrated unilateral TLE, (2) group data of those whose iEEG demonstrated BiTLE, (3) individual patient analysis in those with BiTLE for whom iEEG seizure laterality data were provided. Of 1,403 patients with ambiguous or presumed BiTLE on scalp EEG, 1,027 (73%) proved to have unilateral TLE on iEEG and contributed to the first analysis. Of these, 58% had Engel class I and 9% Engel class II outcomes. Of 132 patients in the second analysis (true BiTLE), Engel class I and II outcomes were achieved in 23% and 14%, respectively. Of 41 patients in the third analysis, 66% and 2% had Engel class I and II outcomes, respectively. The median proportion of seizures ipsilateral to the resection on iEEG did not differ between BiTLE patients with Engel class I–II (76%) and Engel III–IV (78%) outcomes (p = 0.87). Patients with ambiguous or independent bitemporal seizure onset on scalp EEG achieved good surgical outcomes. Overall, a significantly higher proportion of patients achieved good outcomes when iEEG showed unilateral TLE (67%) than when it showed true BiTLE (45%). However, the degree of seizure lateralization in those with BiTLE was not associated with seizure outcome, and it has a limited role in selecting the side of surgery. KEY WORDS: Temporal lobe epilepsy, EEG, Epilepsy surgery, Outcome.

The positive impact of surgery on seizure control and physical and psychosocial function for patients with temporal lobe epilepsy (TLE) is well documented.1–7 Seizure semiology and diagnostic tools are essential components of

the presurgical evaluation to localize the seizure focus and assess surgical candidacy. However, in some cases these investigations provide conflicting results or suggest more than one seizure focus. In patients with TLE, in particular, contralateral temporal lobe abnormalities render the selection of suitable surgical candidates challenging. Can patients with independent bitemporal seizures still be good candidates for resective surgery? If so, is postsurgical seizure outcome similar in those with bitemporal seizures revealed by intracranial electroencephalography (iEEG) and those with unilateral seizures? Patients with multifocal epilepsy were historically thought to be poor surgical candidates,8–10 but case series in the past two decades show that some patients with indepen

Accepted September 30, 2014. *Department of Clinical Neurosciences, University of Calgary, Calgary, Alberta, Canada; †Institute of Neuroscience and the Second Affiliated Hospital, Guangzhou Medical University, Guangzhou, China; and ‡Department of Community Health Sciences, Institute of Public Health and Hotchkiss Brain Institute, University of Calgary, Calgary, Alberta, Canada Address correspondence to Yahya Agha-Khani, Clinical Neuroscience Department, University of Calgary, 4448 Front St SE, Calgary, Alberta T3M 1M4, Canada. E-mail: [email protected] Wiley Periodicals, Inc. © 2014 International League Against Epilepsy

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2 Y. Aghakhani et al. dent bitemporal seizure, that is, bilateral temporal lobe epilepsy (BiTLE), may do well after unilateral temporal lobe resection.11–13 Yet, determining surgical candidacy and choosing the side of the resection among those with BiTLE, remains challenging. Although definite confirmation of BiTLE requires iEEG, the exact role of seizure-onset laterality ratio on iEEG (i.e., the proportion of seizures originating on one side and informing the side of surgery), and the presence of a lesion on magnetic resonance imaging MRI, are not well understood. Here, we explore seizure outcome in patients with ambiguous or bilateral independent temporal lobe seizure onset on scalp EEG who underwent iEEG, and we examine the prognostic role of seizure-onset laterality ratio on iEEG and MRI findings (lesional vs. nonlesional). We hypothesized that in these patients (1) the degree of seizure laterality on iEEG in isolation correlates poorly with surgical outcome, (2) a lesion on MRI may be associated with good outcome, and (3) seizure outcomes are superior in those whose iEEG demonstrates unilateral seizures than in those with bitemporal seizures.

lobe), (3) individual patient analysis of those whose iEEG demonstrated bitemporal seizure onset and had information for each individual regarding the degree of seizure onset laterality on iEEG (i.e., individual patient data were provided regarding proportion of seizures originating from either temporal lobe). There was no overlap between patients in the second and third analyses. Seizure outcome was categorized according to Engel’s classification.14 Because some studies grouped Engel class I–II as “good outcome” and Engel III–IV as “poor outcome,” we also analyzed outcomes using these two broad categories. In studies that did not distinguish between class I and class II, patients were conservatively categorized as class II. When the data permitted, results were statistically pooled using fixed or random-effects models, depending on data heterogeneity, which was assessed using I2 and the Q statistic. Proportions were compared using Fisher’s exact test, and continuous data were assessed with parametric or nonparametric tests as appropriate. Individual patient data were assessed visually and with descriptive statistics.

Methods

Results

Literature search and data abstraction We searched the Embase and MEDLINE databases for published articles in all languages until May 31, 2012, using sub-headings and keywords related to bilateral temporal lobe epilepsy (BiTLE), EEG, intracranial EEG (iEEG), temporal lobe surgery, and seizure outcomes (see Appendix S1 for full search strategy). We included articles describing original data of adults whose scalp EEG showed BiTLE or undetermined side of temporal lobe seizure onset, who underwent iEEG followed by temporal lobe surgery, with reported seizure outcomes with ≥1 year follow-up, and who were not focused selectively on subsets of patients with specific pathologies. Review articles were checked for relevant references. From eligible studies we abstracted year of publication, patient demographics and clinical characteristics, results of scalp EEG, number of recorded seizures on iEEG, seizure laterality, brain MRI findings, side of surgery, duration of follow-up, and seizure outcome. Study eligibility, full-text review, and data abstraction were performed independently by two reviewers, and disagreements were resolved by consensus.

The search identified 1,284 abstracts, of which 101 were selected for full text review (Fig. 1). Of these, 35 studies contributed to the first analysis (unilateral iEEG seizure onset), 10 to the second analysis (bilateral iEEG seizure onset), and 5 to the third analysis (bilateral iEEG seizure onset using individual patient data). The proportion of patients included in each analysis is shown in Figure 2.

Analysis Descriptive statistics were obtained for demographic and clinical features. We performed three separate analyses in patients whose scalp EEG showed bilateral or ambiguous seizure onset: (1) grouped analyses of those whose iEEG demonstrated unilateral seizure onset; (2) grouped analyses of those whose iEEG demonstrated bitemporal seizure onset but had no information regarding the iEEG laterality for each individual (i.e., no individual patient data on actual proportion of seizures originating from either temporal Epilepsia, **(*):1–10, 2014 doi: 10.1111/epi.12856

Analysis 1: Patients whose iEEG demonstrated unilateral temporal seizure onset (i.e., true unilateral TLE) Among 35 studies, the mean number of patients per study was 40 (standard deviation [SD], 38), 29 (83%) studies were published after 1990, 15 (43%) used a combination of subdural and depth electrodes, 11 (31%) used only subdural electrodes, and 9 (26%) used only depth electrodes. Of

Figure 1. Flowchart of the reviewed abstracts and articles. Epilepsia ILAE

5 Bilateral Temporal Lobe Epilepsy Table 2. Patients with ambiguous or bilateral temporal lobe seizure onset on scalp EEG, who underwent bilateral iEEG, were proven to have a unilateral focus, underwent resection with follow-up ≥1 year and no MRI or pathology data Ambiguous or BiTLE Scalp (n)

Study, year 35

Barry et al. (1992) Brekelmans et al. (1998)36 Burgerman et al. (1995)37 Chung et al. (1991)8 Hirsch et al. (1991)38 Holmes et al. (2003)10 Lieb et al. (1981)39 MacDougall et al. (2009)40 Mayanagi et al. (1996)41 So et al. (1989)42 Spencer et al. (1990)43 Spencer et al. (1996)44 Theodore et al. (1997)45 Van Buren et al. (1975)46 Van Gompel et al. (2010)47 Total n (%)

19 44 48 23 166 42 99 93 24 57 44 50 22 12 41 784

Uni on iEEG with Surgery n 13 (68%) 44 (100%) 46 (96%) 19 (83%) 78 (47%) 25 (60%) 52 (53%) 56 (60%) 24 (100%) 23 (40%) 22 (50%) 50 (100%) 17 (77%) 9 (75%) 27 (66%) 505 (64)

Surgical outcomes MRI data NA NA NA NA NA NA NA NA NA NA NA NA NA NA NA

Pathology NS NA NA NA NS NS NA NS NA NA NA NA NA NS NA

Engel I 0 34 36 7 52 16 19 32 0 6 19 27 11 3 16 278 (55%)

Engel II

Engel III–IV

a

4 10 10 6 26 9 25 24 0 14 3 23 6 6 6 172 (34%)

9 0 0 6 0 0 8 0 24a 3 0 0 0 0 5 55 (11%)

NL, normal; AbNL, abnormal (focal lesion); Uni, unilateral; Bi, bilateral; MTS, mesial temporal sclerosis; NS, pathologic data were not correlated with outcome in original article; NA, pre-MRI era, MRI data were not reported or no individual patient data to collaborate with outcome. Patients with bilateral temporal lobe epilepsy but no resection, extratemporal or multifocal seizures, and 70% of patients. Good surgical outcomes (Engel class I and II) can still be achieved in patients with ambiguous or BiTLE seizure onset on scalp EEG. In patients with demonstrated BiTLE on iEEG, the probability of good seizure outcome was 45% (ranging from 38 to 68%). Overall, a significantly higher proportion of patients achieved good outcomes when iEEG showed unilateral TLE (67%) than true BiTLE (45%). Although iEEG was useful for localizing the seizure focus to one temporal lobe in the majority of patients, the seizure lateralization ratio in patients with BiTLE did not predict seizure outcome. A sufficient seizure sample and congruence of data are emphasized in surgical decisionmaking.

Disclosures None of the authors has any conflict of interest to disclose. We confirm that we have read the Journal’s position on issues involved in ethical publication and affirm that this report is consistent with those guidelines.

Funding None.

9 Bilateral Temporal Lobe Epilepsy

Additional Contributors Yahya Aghakhani: Abstract and article review, data extraction, manuscript review; Xiaorong Liu: Abstract and article review, data extraction, manuscript review; Nathalie Jette: Intellectual contribution, manuscript review; Samuel Wiebe: Intellectual contribution, statistical analysis, manuscript review.

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Supporting Information Additional Supporting Information may be found in the online version of this article: Appendix S1. The full search strategy.

Epilepsy surgery in patients with bilateral temporal lobe seizures: a systematic review.

We explored the association between magnetic resonance imaging (MRI) lesion, degree of seizure laterality on intracranial electroencephalography (iEEG...
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