Surgical Treatment of Extratemporal Epilepsy: Clinical, Radiologic, and Histopathologic Findings in 60 Patients

Epilep.psiu, 37( I1):1072-1080, 1996 Lippincott-Raven Publishers, Philadelphia 0 International League Against Epilepsy

Surgical Treatment of Extratemporal Epilepsy: Clinical, Radiologic, and Histopathologic Findings in 60 Patients

Josef Zentner, "Andreas Hufnagel, "furkhard Ostertun, $Helmut K. Wolf, Elga Behrens, Manuel G. Campos, ?Laszlo Solymosi, *Christian E. Elger, $Otmar D. Wiestler, and

Johannes Schramm

Departments of Neurosurgery, *Epileptology, fNeuroradiology, and SNeuropathology, University of Bonn, Bonn, Germany.

Summary: Purpose and Methods: The aim of this study was to analyze clinical, radiologic, and histopathologic findings in 60 consecutive patients with medically intractable extratemporal epilepsy who were operated on between November 1987 and May 1993.

Results: Histologically, there were distinct structural abnormalities in 50 (83%) of the surgical specimens. Signal abnormalities on magnetic resonance imaging (MRI) were present in all patients with neoplastic lesions (n = 17) and in 94% of patients with nonneoplastic focal lesions (n = 32). Overall, structural abnormalities were detected by MRI in 47 (96%) of 49 patients with focal lesions. During a mean follow-up of 4 years, 30 (54%) patients remained completely seizure free, 11 (20%) had S 2 seizures per year, seven (12%) showed a seizure reduction of >75%, and eight (14%) had <75% reduction in seizure frequency. The fraction of seizure-free patients was 12

(80%) of 15 in patients with neoplastic lesions, 16 (52%) of 31 in patients with nonneoplastic focal lesions, and two (20%) of 10 for those without histopathologic abnormalities. The differences in seizure outcome between patients with and without focal lesions were statistically significant (p < 0.05), if seizure- free outcome was compared with persistent seizures.

Conclusions: Focal lesions and particularly neoplasms are associated with improved postoperative seizure control compared with patients without histopathologic abnormalities. We advise caution in considering surgery to treat extratemporal epilepsy in patients who have normal MRI scans, because the outcome with the approach described in this study is poor in such cases. Key Words: Extratemporal epilepsy-Epilepsy surgery-Magnetic resonance imaging-Histopathology- Seizure outcome.

Although results of extratemporal resections in adult and pediatric patients with focal epilepsy have been reported previously, many of these included only a small number of patients and date from before the magnetic resonance imaging (MRI) era. Extratemporal resections

lepsy who have been followed up for a mean of 4 years. We analyzed the relation among clinical, radiologic, and histopathologic findings in detail.

PATIENTS AND METHODS were the most common early operations for epilepsy (1- 6). However, in recent epilepsy series, these procedures account for only 15-20% of cases, whereas -80% of all surgical procedures involve the temporal lobe (7). The ratio of temporal to extratemporal resections reflects pri- marily differences in the epileptogenic potential of different brain areas. However, it also reflects the difficul- ties encountered in attempting to define the epileptogenic zones in extratemporal epilepsy, which are often more diffuse and frequently overlap eloquent areas, preventing complete resection (8,9). We provide a comprehensive report on 60 consecutive patients with extratemporal epi-

This study included 60 consecutive patients who underwent surgical treatment for extratemporal epilepsy between November 1987 and April 1993 in the Depart- ment of Neurosurgery, University of Bonn. During the same period, nine patients with epilepsy of presumed extratemporal origin were not operated on because the presurgical evaluation demonstrated either multifocal or nonlocalizable ictal onsets. Only patients with a history of medically intractable epilepsy with a minimum duration of 1 year were included. All patients had had ad- equate trials of at least two first-line anticonvulsant drugs (AEDs) such as carbamazepine, phenytoin, phenobarbi- tal, or valproic acid.

Accepted July 15, 1996. Address correspondence and reprint requests to Dr. J. Zentner at

All patients underwent continuous video-EEG moni-

addition, subdural strip and grid electrodes were used to Department of Neurosurgery, University of Bonn, Sigmund-Freud- toring by by using In Strasse 25, 53105 Bonn, Germany.

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EXTRATEMPORAL EPILEPSY 1073

identify the epileptogenic area. Extraoperative electro- corticographic (ECoG) studies were performed in 30 (50%) patients. Of these, 14 patients had subdural strip electrodes only, and three patients had subdural grids only. Subdural strip and grid electrodes were used in eight patients; strip and hippocampal depth electrodes, in three patients; and a combination of grids, strips, and hippocampal depth electrodes were used in two patients. Interictal activity and a minimum of two seizures were recorded from implanted electrodes. EEG evaluation was performed according to guidelines described elsewhere (10-12). In addition, functional mapping by using evoked potentials and observing the results of stimulating different electrode contacts was performed if the epileptogenic zone overlapped brain areas of high functionality or if the planned resection would be in close prox- imity to functionally important brain areas. Details of the subdural mapping technique have been published previously (12-15). Most patients with implanted electrodes received antibiotics prophylactically. In the remaining 30 patients, intraoperative ECoG was performed by using grid and strip electrodes. The site and extent of each resection was based on the ictal and interictal EEG findings and the presence of MRI-demonstrated structural lesions. Other information contributing to localization of the epileptogenic area included a detailed seizure history and consideration of seizure semiology, neuropsycho- logic evaluation, psychiatric evaluation, and in many cases, intracarotid amobarbital testing.

The necessity for implanting intracranial electrodes was based on MRI and noninvasive EEG findings, as well as on seizure semiology. If all noninvasive findings pointed clearly to a circumscribed epileptogenic zone, intraoperative monitoring of interictal epileptiform activity was used to help delineate the boundaries of resection. If noninvasive data did not adequately depict an epileptogenic zone but did permit developing a hypothesis about the assumed area of seizure onset, intracranial electrodes were implanted for long-term extraoperative monitoring.

Preoperative MRI scans on 59 patients were available for review. One patient did not have an MRI scan because of metal implants. Forty-three of 59 MRI studies were performed at the University of Bonn Medical Cen- ter. The remaining 16 scans were obtained at various other institutions. At the University of Bonn, MRI was carried out by using a 1.5-T unit (Philips Gyroscan Sl5). Sagittal TI-weighted (Tlw) images (TR/TE/slice thickness = 500-600 ms/l5-25 ms/8-10 mm) and axial proton density (PDw)- and T,-weighted (T2w) images (TR/ TE/slice-thickness = 2.0-2.5 ms/20-30 and 80-120 ms/ 6-8 mm) were obtained routinely. Usually, spin-echo (SE) scans were also performed. T,-weighted gradient echo sequences (GFE) were acquired only when it was necessary to detect calcifications or old hemorrhage. If a

tumor was suspected, additional coronal and axial Tlw images with and without gadolinium-diethylenetriaminepentaacetic acid (DTPA) were acquired by using similar parameters. MRI examinations done at other institutions used widely varying techniques. By using systems of various manufacturers and field strengths, slices were generally 1-2 mm thicker than those obtained at our institution, whereas acquisition of one Tlw and one T2w scan in two different planes was standard. Sometimes no PDw images were available.

All preoperative MRI scans were reviewed retrospec- tively by a neuroradiologist (B.O.) blinded to all clinical information. MRI findings were classified as follows: neoplasm, nonneoplastic lesion, signal abnormality of uncertain significance, and no lesion. The term “uncertain” was used if the findings were not conclusive because of insufficient image quality, questionable partial volume effects, or lack of appropriate sequences or sec- tional planes.

The following surgical procedures were performed: frontal lobectomy (n = 16), frontal topectomy (n = 24), parietal topectomy (n = 7), and occipital topectomy (n = 13). In general, intracerebral lesions, either detected on MRI or visible intraoperatively, were completely excised. Eleven patients had been operated on previously (10 lesionectomies, one anterior callosotomy). In nine of the 10 patients with lesionectomies, the extent of the previous resection was enlarged based on electrophysi- ologic data, and additional epileptogenic cortex was re- moved. In the tenth patient, who had had a left frontal topectomy, a left frontal lobectomy was performed. The right supplementary motor area was resected in the one patient who had previously had an anterior callosotomy.

Frontal lobectomy was guided by standard anatomic landmarks, sparing the premotor and motor cortex and the frontal speech area on the dominant side. This was the procedure of choice when all or most of the frontal lobe was involved initially in a regional seizure onset, or if one or several MRI-detected lesions were either diffuse or multilocular. In patients with a localized seizure origin and MRI-detected lesion, a topectomy was performed. Topectomy of a functional-lesional epileptogenic complex in the frontal lobe or other location was tailored according to preoperative or intraoperative ECoG studies and the results of functional localization studies. The area of resection included the zones of maxi- mum interictal and ictal epileptic activity in all patients. Frontal topectomies were centered in the paramedian area (including the cingulate gyrus), the polar and basal area, or the lateral convexity. However, there was a marked overlap among these types based on functional and structural localization studies.

Neurologically intact patients with epileptogenic lesions involving areas of high functionality present some of the most difficult surgical decisions (9). In these cases,

Epilepsia, Vol. 37, No. 11, 1996

1074 J. ZENTNER ET AL.

TABLE 1. Clinical findings

Age at Duration of Age at Histopathologic surgery seizures seizure onset

diagnosis meanhnge (yr) meadrange (yr) meadrange (yr)

Neoplasm 23.6 3 4 4 8.8 2-24 14.8 1-33 Nonneoplastic lesion 22.3 1 4 9 13.9 2-35 8.3 G 3 0 No specific lesion 24.9 1 3 4 3 15.3 5-28 9.8 7-22 All patients 22.9 1 4 9 12.8 2-35 10.4 0-33

resection was done by emptying gyri, leaving intact the pial banks. The ultrasonic aspirator was used in some patients (16). The central rolandic area was resected from the sylvian fissure to a point 3 cm above, identifying the central arteries and veins and leaving them intact (8).

All operative specimens were reviewed by two neu- ropathologists (H.K.W. and O.D.W.). Hematoxylin and eosin-stained sections were available from all cases. Nissl stains and combined hematoxylin-eosin-luxol-fast- blue stains also were available in the majority of cases. In selected cases, additional special stains (Elastic-van- Gieson, reticulin, Bodian) were performed. In all tumor cases, some or all of the following immunohistochemical reactions were carried out: glial fibrillary acid protein (GFAP), synaptophysin, neurofilament protein (NFP), neuron-specific enolase (NSE), and S- 100 protein. His- topathologic findings were divided into three groups: neoplasm, nonneoplastic focal lesion, and absence of any specific histopathologic abnormalities. Tumors were classified according to the revised World Health Orga- nization (WHO) classification scheme for tumors of the nervous system (17).

Follow-up information was available for 56 (93%) patients based on regular outpatient hospital visits at 3- to 12-month intervals. Four patients were lost to follow-up. Two of these were from other countries and did not return; the other two patients did not keep their outpatient appointments for unknown reasons. Postoperative follow-up ranged from 20 to 85 months (mean, 48 months). Patients were assigned to four different outcome classes based on their postoperative seizure status: (a) seizure free or only auras since surgery; (b) rare seizures (fewer than two per year); (c) reduction of seizure frequency >75%; and (d) unchanged (<75% reduction of seizure frequency). This classification is similar to that of Engel et al. (7). In contrast to the classification of Engel et al., however, patients were not included in class one (seizure free), if complex-partial or secondarily general- ized seizures had occurred in the early postoperative period and the patient became seizure free for >1 or 2 years thereafter.

Student’s t test was used for statistical comparison of continuous variables if the destribution was normal, and Wilcoxon’s test if it was not. Discrete variables were compared by using cross-tabulation including the Fisher test for small subgroups.

RESULTS

Clinical findings There were 39 male and 21 female patients, who

ranged in age from 1 to 49 years (mean, 22.9 years). Age at surgery, duration of seizures, and age at seizure onset related to the histopathologic diagnosis are given in Table 1. As determined by Student’s t test, seizure duration was significantly less in patients with neoplasms compared with those with nonneoplastic lesions or those without specific abnormalities (p < 0.05). In contrast, age at seizure onset was significantly older in patients with neoplasms as compared with those with nonneoplastic lesions and those without significant abnormalities (p < 0.05), but there was considerable overlap between the two groups. Patients’ age at surgery did not differ significantly with respect to any of these groups.

Histopathologic findings Histopathologic examination of the operative speci-

mens revealed neoplasms in 17 (28%) patients, nonneoplastic focal lesions in 33 (55%) cases, and no abnormalities in 10 (17%) patients.

Gangliogliomas were the most frequent tumors (n = lo), and all tumors were of low histopathologic grade (Table 2) . Among nonneoplastic focal lesions, glioneuronal malformations and cavernous malformations were observed most frequently (Table 3). More detailed de- scriptions of the histopathologic findings have been published elsewhere (18).

MRI findings MRI findings related to histopathologic diagnoses are

listed in Table 4. There were signal abnormalities on MRI in 49 (83%) of 59 cases. All neoplasms were detected on MRI, and in 15 (88%) patients, the signal abnormality was correctly interpreted as a neoplasm. In two (12%) tumor patients, the MRI revealed signal abnormalities of uncertain significance.

In 32 patients with histopathologically verified nonneoplastic focal lesions, MRI scans were abnormal in 30 (94%). The specifity of MRI in nonneoplastic lesions was 69%. In two (6%) patients, MRI was normal.

Of 10 patients without histopathologic abnormalities, MRI revealed signal abnormalities of uncertain signifi-

TABLE 2. Histopathologic diagnoses in 17 neoplasms

Specimens

Histopathologic diagnosis n %

Ganglioglioma (WHO grade I) 9 53 Ganglioglioma (WHO grade 11) 1 6 Astrocytoma (WHO grade 11) 4 23 Oligodendroglioma (WHO grade 11) 2 12 Oligoastrocytoma (WHO grade 11) 1 6 Total 17 100

Epilepsia, Vol. 37, NO. 1 I , 1996


TABLE 3. Diagnoses in 33 nonneoplastic focal lesions

Specimens

Histopathologic diagnosis n %

Glioneuronal hamartia Hamartoma Cavernoma Arteriovenous malformation Heterotopia Gliomesodermal scar Ossification Necrosis Gliosis Old hematoma Old abscess wall Total

7 22 1 3 6 18 3 9 1 3 4 12 1 3 5 15 3 9 1 3 1 3

33 100

cance in two (20%) patients and was normal in eight (80%) patients.

Operative complications There was no operative or postoperative mortality.

Postoperative complications occurred in six (10%) patients. Three patients had deep wound infection. Neuro- logic abnormalities occurred in three patients: hemiparesis (n = 2) and aphasia (n = 1). However, complications eventually resolved completely in two patients; only one patient had a persistent hemiparesis of moderate severity related to a subdural empyema that required surgical evacuation.

Seizure outcome The outcome with respect to seizure control is shown

in Table 5. Overall, 86% of patients became seizure free or had a worthwhile improvement after surgery (classes I to 111); 14% had no appreciable reduction in seizure frequency. Of 11 patients in whom additional resection of epileptogenic cortex was performed after an initial unsuccessful lesionectomy, eight became seizure free, one had a >75% reduction of seizures, and two had no worthwhile improvement.

The most favorable results were observed in patients with neoplastic lesions: 80% of such patients were seizure free, and 20% had no more than two seizures per year. The percentage of patients with nonneoplastic focal

TABLE 4. MRI and histopathologic diagnosis in 59 patients with extratemporal epilepsy

N e o p 1 as m

MRI diagnosis n %

Neoplasm 15 88 Nonneoplastic

lesion Uncertain 2 12 No lesion Total 17 100

_ _

_ _

Nonneoplastic lesion

n %

4 13

22 69 4 13 2 6

32 100

No lesion Total

n % n % ~~

19 32

22 31 2 20 8 14 8 80 10 17

10 100 59 100

_ _

_ _

MRI, magnetic resonance imaging.

TABLE 5. Seizure outcome in 56 patients related to histopathologic diagnosis

Nonneoplastic

Outcome _ _ _ _ _ _ class n % n % n % n %

Neoplasm lesion No lesion Total

I 12 80 16 52 2 20 30 54 I1 3 20 6 19 2 20 11 20

5 16 2 20 7 12 111 4 13 4 40 8 14 IV

Total 15 100 31 100 10 100 56 100

_ _ _ _

lesions who became seizure free was noticeably lower (52%). Only two (20%) of 10 patients without histopathologic abnormalities became seizure free. However, six (60%) of these patients showed worthwhile improvement (outcome classes I to 111). The differences in seizure outcome between patients with focal lesios and those without are statistically significant (p < 0.05).

Location of the resective procedure did not affect seizure outcome (Table 6). It is noteworthy that patients who underwent frontal topectomy had a much better outcome than patients who underwent frontal lobectomy (Table 7). This may reflect the fact that frontal topectomy was performed mainly in patients with regional seizure onsets.

In the subgroup of 30 patients in whom extraoperative electrocortigraphic studies had been performed, areas of seizure origin as well as areas of persistent interictal epileptiform discharge were determined and compared with the areas of resection as shown by postoperative MRI. Whereas 14 (67%) of 21 patients in whom the area of seizure origin was completely excised became seizure free, only three (33%) of nine patients with incomplete resection became free of seizures. Moreover, 12 (92%) of 13 patients with a complete resection but only 11 (65%) of 17 patients with an incomplete resection of the zone of persistent interictal spiking reached outcome classes I (seizure free) or I1 (fewer than two seizures per

Illustrative case reports Figures 1 through 3 provide representative examples

of patients with extratemporal epilepsy. Clinical data are given briefly in the respective legends.

Year).

TABLE 6. Seizure outcome related to location of the resection

Frontal Parietal Occipital

class n % n % n % Outcome _______ ~

Total

n %

I 18 50 4 57 8 62 I1 6 17 2 29 3 23

2 15 111 5 1 4 - - IV 7 1 9 1 1 4 - - Total 36 100 7 100 13 100

30 54 11 20 7 12 8 14

56 100

Epilepsia, Vol. 37, NO. 11, 1996


TABLE 7 . Seizure outcome of 36 patients with frontal lobe epilepsy: frontal lobectomy versus topectomy

Lobectomy Topectomy Total

Outcome class n % n % n %

DISCUSSION

The most common problems encountered in evaluat- ing patients with extratemporal seizure foci for surgery include poor EEG localization of interictal spikes and of seizure onset, the presence of a widespread, often ill- defined epileptogenic area, and the extension of the proposed area of resection into brain areas of high functionality (8,19-21). These characteristics of extratemporal epileptogenic foci are major obstacles to their successful surgical treatment.

Controversy exists about whether the epileptogenic area in lesional cases can be sufficiently defined by in-

I 2 13 16 76 18 50 I1 4 27 2 10 6 17 111 4 27 1 4 5 14 IV 5 33 2 10 7 19 Total 15 100 21 100 36 100

FIG. 1. A 26-year-old patient with a 13- year history of seizures originating in the lateral frontal lobe. A: T1-weighted magnetic resonance imaging (Tlw MRI) with gadolinium-diethylenetriaminepentaacetic acid (Gd-DTPA) showing an almost isoin- tense left frontolateral tumor with ring- shaped enhancement. B: Postoperative T l w MRI with Gd-DTPA showing complete resection of the tumor and the epileptogenic zone. Histopathologic evaluation of the operative specimen revealed a ganglioglioma (WHO grade I). C: Results of chronic extraoperative evaluation dem- onstrating the seizure-onset zone adjacent to the lesion and the precentral gyrus. Cor- tical areas involved in language function could not be established. Immediately after surgery, the patient had an expressive aphasia, from which recovery was complete within 6 weeks. The patient has been seizure free for >14 months.



A B

Preoperative Postoperative

C

I3 2,5 mV Spike amplitude

Spike average of 111 Spikes

60 ms=Spike Delay

terictal data alone or whether recording of ictal activity is necessary (22). There is general agreement that nonle- sional extratemporal epilepsy requires intracranial electrodes to record ictal events. The extent of the resection can be determined by either invasive extraoperative localization techniques or by intraoperative ECoG (23). At the 1992 Palm Desert Conference on Epilepsy, 34 (72%) of 47 centers reported that resection of the ictal-onset zone was their main objective. Seventeen (36%) centers relied heavily on interictal EEG spiking, and 15 (32%) used both. Even with invasive monitoring, 20 (43%) centers refined margins of resection further by using intra-

FIG. 2. A 14-year-old boy in whom a previous right precentral partial lesionectomy had not controlled seizures. The patient became seizure free after a second operation with complete excision of the lesion and the epileptogenic zone (follow-up, 32 months). There were no postoperative complications. The lesion was a ganglioglioma with increased cellularity and nuclear pleo- morphism but no frank anaplasia. It was classified as WHO grade II. In addition, there were multiple microscopic glioneuronal malformations. A: T1- weighted magnetic resonance imaging (Tlw MRI) shows the frontolateral defect resulting from the first resection. B: T1 w MRI with gadolinium-diethylenetriaminepentaacetic acid (Gd-DTPA) shows the postoperative defect after the second procedure. C: Amplitude- latency topographic map of interictal spike activity in relation to the chronically implanted 64-contact subdural grid. From a spike-free zone in the cen- ter of the grid overlying the site of the first resection, spikes propagated mainly to the anterior and posterior edges of the grid, as shown by short spike latencies from the earliest spike in the middle of the grid and increas- ingly longer spike latencies toward the edges of the grid. The maximally active interictal zone is also indicated by the highest averaged spike amplitude. D: Schematic drawing of the averaged spikes of the topogram. The average spike amplitude at each grid contact is indicated by the height of the spike symbol. Its latency from the earliest spike in the cluster is indicated by the fraction of black coloring in the square under the spike symbol filled from left to right (maximally 60 ms).

operative ECoG, and 11 (23%) centers said that they always used both intraoperative ECoG and previous ictal recordings (24). In our series, the zone of resection was determined by invasive recordings and intraoperative ECoG in equal numbers of patients. Intraoperative ECoG was used to delineate the boundaries of the resection in patients in whom a clear hypothesis as to the location of the epileptogenic zone had been obtained from noninvasive recordings and MRI studies. However, the results obtained with both methods cannot easily be compared for the following reasons. First, with one exception, no seizures were recorded intraoperatively . Second, intraop-



A B

D

R

0 Seizure Origin

0 Shoulder (Motor)

0 Shoulder (Paraesthesias)

@ Arm (Motor)

(E3 Hand (Motor)

erative corticography was limited to the site of resection and its vicinity and rarely included recordings from non- surgical lobes and never from the contralateral hemisphere. Third, patients may have been negatively selected in the group that were evaluated extraoperatively, because the location of the epileptogenic zone was not as clearly established as in the patients who underwent intraoperative ECoG only. Finally, further bias may have been introduced because all patients in whom the epileptogenic zone overlapped areas of high functionality had chronically implanted subdural grid and strip electrodes.

In addition to recording interictal and ictal activity, extraoperative functional mapping was performed by

FIG. 3. Resection of the epileptogenic zone within the right supplementary sen- sorimotor area (SSMA) in a 27-year-old man with hypermotor seizures since age 17 years. A: Proton density-weighted magnetic resonance imaging (MRI) shows an area of increased signal in the right parietal region without mass effect and edema. B: T1-weighted (Tlw) MRI shows extent of the resection. The lesion was a glioneuronal malformation. C: Re- cording of a seizure starting in GR03-04 and GR04-06. D: Results of extraoperative evaluation showing the seizure- onset zone in the parasagittal precentral right cortex, as well as the SSMA and location of distinct motor areas. Immedi- ately after surgery, the patient had a typi- cal SSMA syndrome with left hemiataxia and left hemiparesis; the findings resolved within 2 weeks. During 15 months of postoperative follow-up, the patient had one series of left arm seizures when AEDs were tapered; he has otherwise been seizure free.

stimulating different contacts of implanted electrodes and by recording evoked potentials. By using convergent information from noninvasive and invasive recordings, including functional testing, we constructed maps delin- eating the area of resection in relation to structural lesions and brain areas of high functionality. Thus the extent of the resection was defined according to EEG data and information regarding structural and functional localization, as proposed by Davies and Weeks (25). Al- ternatively, functional mapping can also be performed intraoperatively in an awake patient by using local an- esthesia (23,26). We have not used this approach in our patients.

Epilepsia. Vol. 37, No. 11, 1996


Recently we used the procedure of multiple subpial transections (MST) described by Morrell et al. (27), either alone or in addition to a resection in seizure foci encroaching on areas of high functionality. Postoperative follow-up in these patients was too short to allow inclu- sion in the series presented here. Our experience in 18 patients so far suggests that even transection of central hemispheric areas is not followed by permanent major neurologic deficits. However, the effects of this procedure on seizure outcome are still pending.

There has been particular interest in recent years to the relation between epilepsy and structural brain lesions. In our series, neuropathologic examination revealed focal structural abnormalities in 50 (83%) of 60 cases. Non- neoplastic lesions were observed most frequently (55%). That all lesions were histologically benign corresponds well with the typically long history of seizures, although seizure duration was significantly shorter in patients with neoplasms compared with those with nonneoplastic lesions and those without abnormalities.

MRI is more sensitive in detecting small structural lesions than is computed tomography (CT), with the exception of small areas of calcification. In our series, MRI revealed structural abnormalities in 83% of patients. Sen- sitivity and specifity of the findings were highest in tumors (100% and 88%, respectively). In nontumoral lesions, MRI was abnormal in 30 (94%) of 32 cases, but only 22 (69%) of these lesions were interpreted as not being tumors. Seven patients in our series had normal routine MRI scans. Because EEG studies in these patients showed consistent interictal and ictal foci, the MRI scans were repeated with special attention to the areas of electrical abnormalities; in all cases, abnormalities were now recognized, and the majority proved to be glioneuronal hamartomas.

Despite earlier indications to the contrary (28,29), extratemporal resections are generally not so successful as temporal lobe resections (9,21,25). In our series, 86% of patients benefited from surgery. This corresponds favor- ably with the survey results presented by Engel et al. (7), based on 1,098 extratemporal resections. The prognosis for seizure control is more favorable when seizures are related to a focal lesion: 91% of such patients improved after surgery compared with only 60% of patients without lesions. Robitaille et al. (30) did not find that prognosis correlated with any specific type of pathologic con- dition. However, we found that 80% of our patients with neoplastic lesions became seizure free postoperatively in contrast to only 52% of patients with nonneoplastic lesions. We believe that histopathologic findings provide prognostically relevant information. However, seizure outcome was not related to the location of the epileptogenic zone.

An important management question is whether excision of the lesion and its epileptogenic zone offers better

results than lesionectomy alone. The available literature is conflicting. Some investigators have suggested that lesionectomy alone is sufficient (3 1,32), whereas others have emphasized the need to resect associated epileptogenic brain areas (15,33,34). Awad et al. (35) achieved seizure control in 17 (94%) of 18 patients with complete lesion excision regardless of the extent of associated brain tissue resection. Seizure control was obtained in five (83%) of six patients with incomplete lesion excision and complete resection of the seizure focus, but seizures were controlled in only 12 (52%) of 23 patients with incomplete lesion excision and incomplete seizure focus resection. In their study, the epileptogenic zone was defined by prolonged invasive interictal and ictal EEG recordings by using chronically implanted subdural electrodes. The authors concluded that although complete lesion resection offers the best chance to control seizures, many patients can benefit from resection of the epileptogenic brain area that may have a variable relation to the lesion (35). Affirmatively, in our patients, seizure outcome was better if the zone of seizure origin and the zone of maximal interictal spiking were completely excised. Therefore a total excision of both areas seems to be necessary for optimal seizure control. In contrast, re- moval of remote regions with only occasional interictal spikes appears not essential.

REFERENCES

1. 2.

3.

4.

5.

6.

I .

8.

9.

10.

11.

12.

13.

14.

Horsley V. Brain surgery. Br Med J 1886;2:670-5. Krause F, Heyman F. Lehrbuch der Chirurgischen Operationen. Berlin: Urban und Schwarzenberg, 1914. Omorokov L. Kozhevnikov’s epilepsy in Siberiero. 2 Neurol Psy- chiatr 1927; 107:487-96. Foerster 0, Altenburger H. Elektrobiologische Vorgange in der menschlichen Hirnrinde. Dtsch Z Nervenheilk 1935;135:277-88. Sachs E. The subpial resection of the cortex in the treatment of Jacksonian epilepsy (Horsley operation) with observations on areas 4 and 6. Brain 1935;58:492-523. Penfield W, Jasper H. Epilepsy and the functional anatomy of the human brain. Boston: Little, Brown, 1954. Engel J, Van Ness P, Rasmussen T, et al. Outcome with respect to epileptic seizures. In: Engel J, ed. Surgical treatment of epilepsies. New York: Raven Press, 1993:609-22. Olivier A, Awad I. Extratemporal resections. In: Engel J, ed. Sur- gical treatment of epilepsies. New York: Raven Press, 1993:489- 500. Haglund MM, Ojeman GA. Extratemporal resective surgery for epilepsy. Neurosurg Clin North Am 1993;4:283-92. Hufnagel A, Elger CE, Pels H, et al. Prognostic significance of ictal and interictal epileptiform activity in temporal lobe epilepsy. Epilepsia 1994;35:1146-53. Hufnagel A, Poersch M, Elger CE, et al. The clinical and prognostic relevance of the postictal slow focus in the electrocortico- gram. J Electroenccephalogr Clin Neurophysiol 1995;94: 12-8. Hufnagel A, Elger CE, Helmstaedter C, Fernandez G, Steinkamp J . Die Wertigkeit der cortikalen Elektrostimulation fur die prachirur- gische Epilepsiediagnostik. In: Verhandlungen der Deutschen Ge- sellschaji fur Neurologie. Wien: Springer, 1995:3 14-8. Luders H, Lesser RP, Hahn JF, et al. Cortical somatosensory evoked potentials in response to hand stimulation. J Neurosurg 1983;58:885-94. Morris HH, Liiders H, Hahn JF, et al. Neurophysiological tech-

Epilepsia, Vol. 37, No, 11, 1996


niques as an aid to surgical treatment of primary brain tumors. Ann Neurol 1986;19:559-67.

15. Wyllie E, Liiders H, Morris HH, et al. Clinical outcome after complete or partial cortical resection for intractable epilepsy. Neu- rology 1987;37:1634-41.

16. Olivier A. Commentary: cortical resections. In: Engel J, ed. Sur- gical treatment of epilepsies. New York Raven Press, 1987:405- 16.

17. Kleihues P, Burger PC, Scheithauer BW. Histological typing of tumors of the central nervous system. 2nd ed. Berlin: Springer, 1993.

18. Wolf HK, Zentner J, Hufnagel A, et al. Surgical pathology of chronic epileptic seizure disorders: experience with 63 specimens from extratemporal corticectomies, lobectomies and functional hemispherectomies. Acta Neuropathol 1993;86:466-72.

19. Quesney LF. Extratemporal epilepsy: clinical presentation, preoperative EEG localization and outcome. Acta Neurol Scand Suppl 1992; 1408 1-94.

20. Williamson PD, Spencer SS. Clinical and EEG features of complex partial seizures of extratemporal origin. Epilepsia 1986;27(suppl 2):S4643.

21. Talairach J, Bancaud J, Boris A, et al. Surgical therapy for frontal epilepsies. In: Chauvel P, Delgado-Escueta AV, Halgren E, et al., eds. New York: Raven Press, 1992:707-32. (Advances in neurol-

22. Engel J. Approaches to localization of the epileptogenic lesion. In: Engel J, ed. Surgical treatment of the epilepsies. New York Raven Press, 1987:75-9.

23. Ojemann GA. Surgical therapy for medically intractable epilepsy. J Neurosurg 1987;66:489-99.

24. Spencer DD, Ojemann GA. Overview of therapeutic procedures. In: Engel J, ed. Surgical treatment of the epilepsies. New York Raven Press. 1993:455-71.

ogy; vol 57).

26. Ojemann GA, Ojemann J, Lettich E, Berger M. Cortical language localization in left, dominant hemisphere. J Neurosurg 1989;71: 3 16-26.

27. Morrell F, Whisler WW, Bleck TP. Multiple subpial transection: a new approach to the surgical treatment of focal epilepsy. J Neu- rosurg 1989;70:231-9.

28. Rasmussen T. Surgery for epilepsy arising in regions other than the temporal and frontal lobes. In: Purpura DP, Penry JK, Walter RD, eds. Neurosurgical management of the epilepsies. New York Raven Press, 1975:207-6. (Advances in neurology; vol 8).

29. Rasmussen T. Surgery of frontal lobe epilepsy. In: Purpura DP, Penry JK, Walter RD, eds. Neurosurgical management of the epilepsies. New York: Raven Press, 1975: 197-205. (Advances in neurology; vol 8).

30. Robitaille Y, Rasmussen T, Dubeau F, et al. Histopathology of non-neoplastic lesions in frontal lobe epilepsy: review of 180 cases with recent MRI and PET correlations. In: Chauvel P, Delgado- Escueta AV, Halgren E, Bancaud J, eds. Frontal lobe seizures and epilepsies. New York Raven Press, 1992:499-5 13.

31. Goldring S, Gregorie EM. Surgical management using epidural recordings to localize the seizure focus: review of 100 cases. J Neurosurg 1973;60:457-66.

32. Petrovici AC. Epilepsy in temporal lobe tumors. Eur Neuroll971; 5:201-14.

33. Spencer DD, Spencer S S , Mattson RH, Williamson PD. Intrace- rebral masses in patients with intractable partial epilepsy. Neurol- ogy 1984:34:432-6.

34. Drake J, Hoffman HJ, Kobayashi J, Hwang P, Becker LE. Surgical management of children with temporal lobe epilepsy and mass lesions. Neurosurgery 1987;21:792-7.

25. Davies KG, Weeks RD. Cortical resections for intractable epilepsy of extratemporal origin: experience with seventeen cases over eleven years. Br J Neurosurg 1993;7:343-53.

35. Awad IA, Rosenfeld J, Ah1 J, et al. Intractable epilepsy and structural lesions of the brain: mapping, resection strategies, and seizure outcome. Epilepsia 1991;32: 179-86.

Epilepsia, Vol. 37, No. 1 I , 1996

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Surgical Treatment of Extratemporal Epilepsy: Clinical, Radiologic, and Histopathologic Findings in 60 Patients