predictors of seizure outcome after temporal lobectomy for intractable epilepsy

6
Predictors of seizure outcome after temporal lobectomy for intractable epilepsy About 10–20% of people who develop epilepsy will have epilepsy that is refractory to control with anticonvulsant medication (1). Surgical treatment is a widely used and important part of the management of patients with intractable epilepsy (2, 3). Its use has been increasing, although it is frequently considered an under-used treatment option (4). Anterior temporal lobectomy (ATL) is the most commonly performed operation (5, 6). Previous studies suggest that surgery controls seizures in up to about two-thirds of selected patients (7), although the reported rate of seizure freedom varies from 33 to 93%, according to a recent systematic review (8). The methods of patient selection and evaluation have changed over time. There is now a greater tendency toward early surgery (2) and more advanced ima- ging and mapping procedures before surgery (4, 9). Studies of predictors of seizure outcome after epilepsy surgery are heterogeneous and difficult to compare, and the results are partly conflicting (8, 10–22). Studies have included only children (20–21), adults, or both. Some studies have inclu- ded patients over a long time period, often decades, with apparent large variations in available tech- nology and presurgical evaluation (11, 16, 23). Studies also differ in types of epilepsies included, surgical techniques used and anatomical structures resected. Moreover, the choice of potential predic- tors varies, generally reflecting the available tech- nology at the time. Some studies include neuropathology specimens or early postoperative data among the included predictors. There are also differences in length of follow-up, the way outcome is measured or classified, and the analytical tech- niques used. Most studies are small and use univariate analysis, although several studies also have reported results from multivariate analyses (10, 14, 16, 17, 21, 22, 24, 25). In Norway, epilepsy surgery has been centralized since the early 1950s. The patients therefore undergo the same protocol for presurgical evalu- ation and selection, and are operated on by the same surgeons. A prospective database was started in 1986. PatientsÕ seizure outcomes were distributed across different Engel’s groups, and the proportion Acta Neurol Scand 2004: 109: 244–249 DOI: 10.1046/j.1600-0404.2003.00249.x Printed in UK. All rights reserved Copyright Ó Blackwell Munksgaard 2003 ACTA NEUROLOGICA SCANDINAVICA Stavem K, Bjørnæs H, Langmoen IA. Predictors of seizure outcome after temporal lobectomy for intractable epilepsy. Acta Neurol Scand 2004: 109: 244–249. Ó Blackwell Munksgaard 2003. Objectives – To assess predictors of outcome of temporal lobectomy for intractable epilepsy. Material and methods – In 63 adult patients operated with anterior temporal lobectomy during 1988–92, we used logistic regression analysis to assess predictors of being seizure-free (Engel’s class I) 2 years after surgery. As potential predictors, we included the following variables: gender, age at operation, age at onset of seizures, epilepsy duration, etiology, generalized vs not generalized seizures, seizure frequency, intelligence quotient, ictal electroencephalography, magnetic resonance imaging (MRI), single- photon emission computed tomography (SPECT), side of resection, and extent of the resection. Results – About 44% of the surgery patients were seizure-free (Engel’s class I) 2 years after surgery. In multivariate analysis (n ¼ 55), MRI pathology defined as atrophy in the temporal lobe, angioma, tumor or mesial temporal sclerosis (odds ratio, OR 7.4, 95%CI: 1.7–32.9) and extent of the hippocampal resection (increase of 1 cm) (OR 2.2, 95%CI: 1.1–4.6) predicted being seizure-free. Conclusion – Focal pathology in preoperative MRI and the extent of the hippocampal resection were the only significant predictors of being seizure-free after 2 years. K. Stavem 1,2 , H. Bjørnæs 3 , I. A. Langmoen 4,5 1 Foundation for Health Services Research (HELTEF) and 2 Department of Medicine, Akershus University Hospital, Nordbyhagen; 3 The National Centre for Epilepsy, Sandvika; 4 Department of Neurosurgery, National University Hospital, Oslo, Norway; 5 Department of Neurosurgery, Karolinska Hospital/Karolinska Institute, Stockholm, Sweden Key words: predictors; epilepsy surgery; partial epilepsy; seizures; neurosurgery Knut Stavem, Foundation for Health Services Research (HELTEF), Akershus University Hospital, NO-1474 Nordbyhagen, Norway Tel.: +47 67929460 Fax: +47 67929469 e-mail: [email protected] Accepted for publication October 17, 2003 244

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Predictors of seizure outcome after temporallobectomy for intractable epilepsy

About 10–20% of people who develop epilepsy willhave epilepsy that is refractory to control withanticonvulsant medication (1). Surgical treatmentis a widely used and important part of themanagement of patients with intractable epilepsy(2, 3). Its use has been increasing, although it isfrequently considered an under-used treatmentoption (4). Anterior temporal lobectomy (ATL) isthe most commonly performed operation (5, 6).Previous studies suggest that surgery controlsseizures in up to about two-thirds of selectedpatients (7), although the reported rate of seizurefreedom varies from 33 to 93%, according to arecent systematic review (8). The methods ofpatient selection and evaluation have changedover time. There is now a greater tendencytoward early surgery (2) and more advanced ima-ging and mapping procedures before surgery (4, 9).Studies of predictors of seizure outcome after

epilepsy surgery are heterogeneous and difficult tocompare, and the results are partly conflicting(8, 10–22). Studies have included only children(20–21), adults, or both. Some studies have inclu-

ded patients over a long time period, often decades,with apparent large variations in available tech-nology and presurgical evaluation (11, 16, 23).Studies also differ in types of epilepsies included,surgical techniques used and anatomical structuresresected. Moreover, the choice of potential predic-tors varies, generally reflecting the available tech-nology at the time. Some studies includeneuropathology specimens or early postoperativedata among the included predictors. There are alsodifferences in length of follow-up, the way outcomeis measured or classified, and the analytical tech-niques used. Most studies are small and useunivariate analysis, although several studies alsohave reported results from multivariate analyses(10, 14, 16, 17, 21, 22, 24, 25).In Norway, epilepsy surgery has been centralized

since the early 1950s. The patients thereforeundergo the same protocol for presurgical evalu-ation and selection, and are operated on by thesame surgeons. A prospective database was startedin 1986. Patients� seizure outcomes were distributedacross different Engel’s groups, and the proportion

Acta Neurol Scand 2004: 109: 244–249 DOI: 10.1046/j.1600-0404.2003.00249.xPrinted in UK. All rights reserved

Copyright � Blackwell Munksgaard 2003

ACTA NEUROLOGICASCANDINAVICA

Stavem K, Bjørnæs H, Langmoen IA. Predictors of seizure outcomeafter temporal lobectomy for intractable epilepsy.Acta Neurol Scand 2004: 109: 244–249. � Blackwell Munksgaard 2003.

Objectives – To assess predictors of outcome of temporal lobectomy forintractable epilepsy. Material and methods – In 63 adult patientsoperated with anterior temporal lobectomy during 1988–92, we usedlogistic regression analysis to assess predictors of being seizure-free(Engel’s class I) 2 years after surgery. As potential predictors, weincluded the following variables: gender, age at operation, age at onsetof seizures, epilepsy duration, etiology, generalized vs not generalizedseizures, seizure frequency, intelligence quotient, ictalelectroencephalography, magnetic resonance imaging (MRI), single-photon emission computed tomography (SPECT), side of resection,and extent of the resection. Results – About 44% of the surgerypatients were seizure-free (Engel’s class I) 2 years after surgery. Inmultivariate analysis (n ¼ 55), MRI pathology defined as atrophy inthe temporal lobe, angioma, tumor or mesial temporal sclerosis (oddsratio, OR 7.4, 95%CI: 1.7–32.9) and extent of the hippocampalresection (increase of 1 cm) (OR 2.2, 95%CI: 1.1–4.6) predicted beingseizure-free. Conclusion – Focal pathology in preoperative MRI andthe extent of the hippocampal resection were the only significantpredictors of being seizure-free after 2 years.

K. Stavem1,2, H. Bjørnæs3,I. A. Langmoen4,51Foundation for Health Services Research (HELTEF) and2Department of Medicine, Akershus University Hospital,Nordbyhagen; 3The National Centre for Epilepsy,Sandvika; 4Department of Neurosurgery, NationalUniversity Hospital, Oslo, Norway; 5Department ofNeurosurgery, Karolinska Hospital/Karolinska Institute,Stockholm, Sweden

Key words: predictors; epilepsy surgery; partialepilepsy; seizures; neurosurgery

Knut Stavem, Foundation for Health Services Research(HELTEF), Akershus University Hospital, NO-1474Nordbyhagen, NorwayTel.: +47 67929460Fax: +47 67929469e-mail: [email protected]

Accepted for publication October 17, 2003

244

becoming seizure-free was lower than in some morerecent studies. This distribution of outcomes cre-ates an opportunity to identify predictors of afavorable seizure outcome.In this study, we wanted to identify possible

predictors of becoming seizure-free after temporallobectomy in a sample of patients operated in onecenter during a 5-year period with the sameprotocol for presurgical evaluation and selection.

Materials and methods

Subjects

In Norway, epilepsy surgery is performed incollaboration between the National Center forEpilepsy [preliminary selection, ictal and interictalvideo-electroencephalography (EEG) recordings,neuropsychological work-up and postoperativerehabilitation], and the Department of Neurosur-gery at the National Hospital (intracarotid amo-barbital test, brain imaging, functional mappingand surgical treatment). Magnetic resonance ima-ging (MRI) was used routinely in the evaluationfrom 1987. The protocol used for presurgicalevaluation has previously been published (26).From February 1, 1988 to December 31, 1992,

73 adult patients above 18 years of age wereoperated for epilepsy in Norway, of whom 63had an ATL and were included in this study. Allpatients had follow-up data after 2 years. Theselection criteria for the surgery were that thepatients would have epilepsy that was intractableto all other treatments, an intolerable seizuresituation, sufficient mental capacity to cooperateduring the presurgical evaluation and favorableresults of the Wada test regarding localizationof language and memory functions. For limitedresective surgery, the seizure-producing areashould be localized and dispensable (26).Among the patients where we retrospectively

obtained seizure classification (n ¼ 61), 79% hadcomplex partial seizures (as the only seizure type in44%, combined with simple partial in 5% and withsecondary generalization in 30%). The remainingpatients had simple partial seizures only (3%),simple partial with secondary generalization (6%),or complex partial seizures in combination withprimary generalized seizures (and sometimes alsosimple partial seizures) (12%).Before surgery, 24 (38%) of the 63 patients were

evaluated with intracranial electrodes. The opera-tive procedure was an individually tailored ATL,with excision of about two-thirds of the anterior partof the temporal lobe, including part of the lateraltemporal cortex, amygdala, hippocampus and para-

hippocampal gyrus. The tailoring was based on allavailable documentation from the presurgical eval-uation, including the seizure pattern, ictal andinterictal EEG recordings, preoperative MRI,Wada test results, and electrocorticography in allpatients. Additionally, some of the procedures wereperformed in local anesthesia. Two neurosurgeonsdid all the procedures.

Medical record abstraction

We reviewed the medical records of the patients inthe two institutions. The information in the pros-pective database was crosschecked against themedical records and supplemented when necessary.Intelligence quotient (IQ) for the patients wasassessed during the presurgical evaluation, usingthe Wechsler Adult Intelligence Scale (WAIS) (27).

Outcome assessment

The seizure situation for operated patients wascategorized according to Engel’s classification (7),as registered at follow-up 2 years after surgery.

Statistical analysis

Descriptive statistics are presented with mean, SDand for time variables also with median andranges. Seizure frequencies are presented usingmedian and interquartile range.Odds ratios for being seizure-free (Engel’s class

I) 2 years after surgery were estimated usinglogistic regression analysis. We included the pre-dictors we considered most relevant after review ofprevious reports and a recent review (8), and thatwere available.We used the following independent variables:

age at time of survey, gender, age at operation, ageat onset of seizures, epilepsy duration, monthlyseizure frequency, intelligence quotient (WAIS),etiology (known or unknown), seizures (general-ized or not), MRI pathology (normal, unspecific,atrophy in the temporal lobe, angioma, tumor,infarction, mesial sclerosis, and other definedpathology), SPECT pathology (yes vs no), avariable for ictal EEG, whether operation wasperformed in the non-dominant hemisphere (rightside in right-handed patients/left in left-handed ornot; yes vs no/unknown), the extent of resection ofthe hippocampus (in cm) and the maximal lateralresection length (in cm).In further analysis, we classified the MRI find-

ings in three groups: (i) normal, (ii) distinct focalpathology with potentially favorable outcome(atrophy in the temporal lobe, angioma, mesial

Predictors of seizures after temporal lobectomy

245

sclerosis, and tumor), and (iii) less specific findings(unspecific, other atrophy, and other findings).Computed tomography scans were not included inthe analysis because of a low number of validresults (n ¼ 25), classification problems, and lackof significance previously reported (16). We createda dichotomous variable for classifying the ictalEEG. If ictal EEG showed focal theta-delta waves,focal sharp or spike waves, or focal desynchroni-zations, we classified the EEG as pointing toa focal lesion (yes), otherwise classified as �no�.A priori, we would expect signs of a focal lesionto indicate a favorable prognosis.The results of univariate and multivariate ana-

lysis are presented as odds ratios (OR) with 95%confidence intervals (95% CI) and P-values. ORfor continuous time variables are presented forincreases of 5 years. For seizure frequency, wereport for odds ratio for an increase of 50% of themedian seizure frequency in the total sample, i.e.for an increase of 10.25 seizures per month.In the multivariate analysis, we limited the

number of independent variables to six due to thelimited sample size. In this analysis, we includedindependent variables with P £ 0.25 in the univari-ate analysis. All independent variables were forcedinto the model. We then manually removed cova-riates from the model, examining changes in param-eters and stability of the model. The assumptions oflinearity in the logit were checked using Box-Tidwelltransformation. We checked the model for multi-collinearity and inspected the standardized residu-als. The Spearman’s rank correlation between theindependent variables in the multivariate logisticregression analysis were all <0.7.We chose a significance level of 5%, using two-

tailed tests. We used the SPSS for Windows (SPSSInc., Chicago, IL, USA) version 11.5 software forall analyses. The regional ethics review committeeapproved the study.

Results

When using Engel’s classification of outcome2 years after surgery, 28 of 63 patients (44%)were free of seizures (class I). Another nine patients(14%) were �almost seizure-free� (class II), six(10%) had worthwhile improvement (class III),while 20 (32%) reported no worthwhile improve-ment (class IV).The patients had a median age at first unpro-

voked seizure of 10 years (range: 0–39), median ageat surgery of 31.4 years (range: 16–55), and amedian presurgical duration of epilepsy of18.4 years (range: 1–53). Their IQs ranged 32 to133 (interquartile range: 76–105). Histological

examination of the specimens (n ¼ 61) showednormal tissue in 18 cases (30%), hippocampalsclerosis 13 (21%), malformations (angiomatousand hamartoma) eight (13%), cerebrovascular/trauma (ischemic, hemorrhagic, post-traumatic,scar) eight (18%), neoplasms six (10%) (oneunspecified low grade glioma, one astrocytoma,one microcystic glioma, one oligoastrocytoma, andtwo dysembryoplastic neuroepithelial tumor),post-inflammatory three (5%), and other five(8%). Median age at first unprovoked seizureaccording to histology for the largest groups:normal 9 years (n ¼ 18), hippocampal sclerosis 5(n ¼ 13), malformations 17 (n ¼ 8), neoplastic 15(n ¼ 6), and cerebrovascular/trauma 11 (n ¼ 8).Possible predictor variables for seizure status

2 years following surgery are shown in Table 1,according to being seizure-free (Engel’s class I) ornot seizure-free (Engel’s classes II–IV). There wasno difference in age at surgery between men andwomen, with mean age (SD) of 31.0 (7.6) (n ¼ 27)and 31.6 (9.7) (n ¼ 36), respectively.In univariate logistic regression analysis, MRI

pathology, gender and hippocampal resectionlength were the strongest predictors of being seiz-ure-free 2 years after surgery (Table 2). Our EEGvariable and whether the seizures were generalizedor not, were not significant predictors. We dicho-tomized theWAIS score (<85 vs ‡85), however thisvariable also did not predict the outcome.In multivariate models, after adjusting for other

variables, gender was not a significant predictor ofbeing seizure-free. Only focal MRI pathology andhippocampal resection length remained significantpredictors in multivariate modeling (Table 2).

Discussion

We found that only focal pathology onMRI duringthe presurgical evaluation and hippocampal resec-tion lengthwere predictors of a seizure-free outcomeafterATL for intractable epilepsy. This supports thecapacity of MRI findings to predict seizure freedomin some previous studies (13, 14, 24, 28–30). Forexample, the following MRI findings have beenassociated with an improved prognosis: increasedipsilateral hippocampal signal or hippocampalatrophy (14, 29), or ipsilateral hippocampal scler-osis (24). In our study, we assessed outcome after2 years, which has previously been reported to be apredictor of long-term outcome (11, 15, 31, 32).Our findings also support a previous controlled

study that showed better results with more exten-sive resections of the hippocampus (33), but are incontrast to the findings in multivariable analysis ofno difference in outcome whether hippocampus

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was resected or not (25) or according to the size ofthe hippocampal resection (34, 35).We found no association of seizure outcome with

the extent of the lateral resection, in accordancewiththe findings of Herrmann et al. (36), but in contrastto the findings of others (37).Generally, the evidencefor the significance of the extent of the resections ismixed, for instance because of small samples, as inour study.Age was a significant predictor in univariate

analysis, however this finding was not consistentwhen adjusting for MRI findings and hippocampalresection length. Gender was not a significantpredictor of seizure outcome in multivariate ana-lysis in this study, in agreement with previousstudies (11, 24).

Our study included wide inclusion criteria, with-out a strict lower limit for IQ. However, there waslittle association of outcome with preoperativeWAIS scores or seizure frequency in this study,supporting previous findings (20, 38–40). This is incontrast to the findings in a recent large multicenterstudy, where patients with IQ £ 75 had a lowerchance of becoming seizure-free than patients withIQ > 75, although the group difference was smalland thought to have little clinical utility (41).We found no association between outcome after

2 years and age at operation, in line with somestudies (14, 25), but in contrast to others (24, 31).Furthermore, we found no association of durationof epilepsy with the outcome, consistent with someprevious reports (14, 20, 42), but in contrast to thefinding of Hennessy et al. (16). In previous studiesonly partial seizure has been reported to beassociated with seizure outcome after surgery(25), however, we could not demonstrate such anassociation in our sample.The proportion seizure-free (Engels’s class I)

patients after 2 years in our study was lower thanreported for some studies (28, 29), however similarto the reports of some other studies of temporallobe epilepsy surgery (11, 43). A recent systematicreview of 126 studies of temporal lobectomyreported that seizure freedom rates varied from33 to 93% in 99 studies, with a median of 70%seizure-free (8). The same study underscored theheterogeneity among the studies and their meth-odology. As in all surgery, variations can reflectdifferences in patient selection, preoperative eval-uation, extent of the resection and method foroutcome assessment. There is considerable diver-sity in the presurgical evaluation for epilepsysurgery and in the methods to determine outcome(8, 44, 45). The reports about epilepsy surgeryoutcomes have very different time spans, fre-quently including patients evaluated before theavailability of MRI (8). The distribution of MRIfindings varies between studies, indicating differ-ences in sample selection. Most studies of theprognostic value of MRI have not includedpatients in whom surgery was rejected because ofan epileptogenic lesion was not identified (43).Some studies have included postoperative resultsor observations in their analysis, while otherstudies use only preoperative data.Some limitations of the current study and the

design should be noted. Preoperative and investi-gative data were collected by medical recordabstraction, which has inherent limitations thatmight question the reliability of the data. Theproportion of positive MRI findings in our studywas low compared with more recent studies, prob-

Table 1 Patient characteristics according to Engel's classification of postoper-ative outcome 2 years postoperatively. Values are mean (SD) unless statedotherwise

Class I(N ¼ 25–28)

ClassesII–IV

(N ¼ 31–34)

Gender, no. of women (%) 12 (43) 24 (69)Age at operation (years) 30.5 (8.7) 32.1 (8.9)Epilepsy duration (years) 19.7 (9.8) 18.7 (10.4)Intelligence quotient 91 (19) 89 (18)Known etiology, n (%) 12 (44) 12 (48)*Seizure frequency per month, median (IQR) 13 (5–50) 30 (10–60)Generalized seizures, n (%) 15 (54) 12 (36)Seizure pattern, n (%)Complex partial/simple partial 13 (46) 19 (58)Complex partial/simple partialwith generalization

11 (39) 11 (33)

Others/combinations/primary generalized 4 (14) 3 (9)Ictal EEG findings, n (%)Focal theta-delta waves 7 (25) 7 (20)Focal sharp or spike waves 10 (36) 10 (29)Focal desyncronizations 1 (4) 1 (3)

MRI findings, n (%)Normal 9 (36) 20 (63)Atrophy in the temporal lobe 6 (24) 0 (0)Angioma 3 (12) 3 (9)Mesial sclerosis 0 (0) 2 (6)Tumor 2 (8) 0 (0)Others 5 (18) 7 (20)

Pathology on SPECT, n (%) 13 (54) 17 (50)Side, right resections, n (%) 14 (50) 14 (40)Operated non-dominant hemisphere, n (%) 15 (56) 24 (69)Extent of the resection (cm)Hippocampus 1.4 (1.1) 0.8 (0.8)Maximal lateral resection 5.2 (1.1) 5.5 (1.3)

Pathology findingsNormal 7 (27) 11 (31)Hippocampal sclerosis 7 (27) 6 (17)Malformations 3 (11) 5 (14)Neoplastic 4 (14) 2 (6)Cerebrovascular/trauma 3 (12) 5 (14)Inflammatory/infectious 0 (0) 3 (9)Focal gliosis 2 (8) 2 (6)Not available 2 (7) 1 (3)

* n ¼ 25

Predictors of seizures after temporal lobectomy

247

ably reflecting the evolution of MRI protocols. Arecent study reporting MRI findings between 1988and 1993 reported a similar proportion of structuralabnormalities on MRI as in the present study (43).The power of our study was limited because of alimited sample size, hence it was not feasible to dofurther analyses on subgroups.In conclusion, in this sample with wide inclu-

sion criteria we found that focal pathology inMRI during presurgical evaluation and hippo-campal resection length were the only predictorsof being seizure-free after ATL for intractableepilepsy. However, because of a limited samplesize our results should be interpreted with cau-tion. Several measures in recent series have beenassociated with seizure outcome, including focalfindings on MRI and positron emission tomo-graphy, histological findings, and converging indi-cators of pathology from the intracarotidamobarbital test (12, 14, 19, 24, 25). The rela-tionship between these factors would have to beassessed in a larger study.Improved presurgical evaluation and selection of

patients for epilepsy surgery during the last decade,may lead to a larger proportion of seizure-freepatients in future series. A more restrictive selec-tion of patients for surgery could lead to a higherproportion of patients achieving freedom fromseizures. Inherently, this would lead to a denial ofsurgery for patients with a lower probability of

becoming seizure-free, but who might possiblybenefit from epilepsy surgery.

Acknowledgements

Thanks to Bjørn Guldvog, Yngve Løyning and Eivind Hauglie-Hanssen for their contribution to establish this project.

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