Results of surgery in patients with refractory extratemporal epilepsy with normal or nonlocalizing magnetic resonance findings investigated with subdural grids
Cukiert A1, Buratini JA, Machado E, Sousa A, Vieira JO, Argentoni M, Forster C, Baldauf C.
ABSTRACT – PURPOSE
To study the efficacy of extensive coverage of the brain surface with subdural grids in defining extratemporal cortical areas amenable for resection in patients with refractory extratemporal epilepy (R-ExTE) and normal or nonlocalizing magnetic resonance imaging (MRI) scans.
Sixteen patients with R-ExTE were studied. Eleven patients had simple partial, eight had complex partial, and three had supplementary motor area seizures. Seizure frequency ranged from three per month to daily episodes. Interictal EEG showed large focal spiking areas in 11 patients, secondary bilateral synchrony in four, and was normal in one patient. Surface ictal recordings were nonlocalizing in six patients, and in 10, they disclosed large ictal focal spiking areas. MRI was normal in 10 patients, and in six patients, focal nonlocalizing potentially epileptogenic lesions were found. All patients were given an extensive coverage of the cortical convexity with subdural electrodes through large unilateral (n = 13) or bilateral (n = 3) craniotomies. Bipolar cortical stimulation was carried out through the implanted electrodes.
Interictal invasive recording findings showed widespread spiking areas in 13 patients and secondary bilateral synchrony in three. Ictal invasive recordings showed focal seizure onset in all patients. There were six frontal, two parietal, one temporooccipital, four rolandic, and three posterior quadrant resections. Thirteen patients had been rendered seizure free after surgery, and three had > or =90% of seizure-frequency reduction. Pathologic findings included gliosis (n = 10), cortical dysplasia (n = 5), or no abnormalities (n = 1). Six patients had transient postoperative neurologic morbidity.
Extensive subdural electrodes coverage seems to be an effective way to investigate patients with R-ExTE and normal or nonlocalizing MRI findings.
The surgical treatment of refractory extratemporal epilepsy (R-ExTE) has always represented a challenge. The surgical results that have been published in the pre–magnetic resonance imaging (MRI) era were poorer then those obtained in the treatment of patients with temporal lobe epilepsy (1–3). After the appearance of MRI, it has been possible to detect potentially epileptogenic lesions preoperatively, and the surgical results obtained in patients with R-ExTE have improved considerably (4–6). Conversely, patients with R-ExTE and normal or nonlocalizing MR scans still represent the most difficult patients to handle, and they frequently need invasive recordings. The paradigms for invasive electrode placement vary from one center to the other, including the use of depth, subdural, epidural, and foramen ovale electrodes (7–10). Subdural grids and strips have been used to cover the cortical convexity and mesial surfaces. Subdural strips are easier to implant, usually through a burr-hole or small craniotomy, but the cortical coverage is not extensive. Subdural grids cover a larger cortical area but need large craniotomies to be inserted. We studied the efficacy of an extensive coverage of the brain surface with subdural grids in defining extratemporal cortical areas amenable for resection in patients with R-ExTE.
Sixteen patients with R-ExTE were studied. All patients were studied from 1997 to 2000. These patients represented all the group of patients with refractory extratemporal epilepsy and nonlocalizing MRI investigated with subdural electrodes during that period. They were given prolonged video-EEG monitoring and had high-resolution MR scanning before invasive recordings. In all patients, cortical resection was performed after subdural grids implantation. The clinical summary and preimplantation findings of these patients are shown in Table 1.
Ages ranged from 8 to 28 years (m = 20.5 years), and the age at onset of the epileptic syndrome ranged from 1 to 7 years (m = 3.5 years). Eleven patients had simple partial (somatosensitive in three, motor in six, versive in one, visual in one, and aphasic blockage in three), eight had complex partial, and three had supplementary motor area (SMA) seizures. Seizure frequency ranged from three per month to daily episodes. Interictal EEG showed large focal spiking areas in 11 patients, secondary bilateral synchrony in four, and normal in one patient. Surface ictal recordings were nonlocalizing in six patients, and in 10, it disclosed large ictal focal spiking areas. MRI was normal in 10 patients, and in six patients, focal nonlocalizing potentially epileptogenic lesions were found: congenital porencephaly (n = 3), hemispheric atrophy (n = 1), multifocal areas of cortical dysplasia (n = 1), and bioccipital anoxic lesions (n = 1).
At least two ictal single-photon emission computed tomography (SPECT) scans were available in seven patients (VI, VII, IX, XI, XII, XIII, and XIV). All patients with SMA-type seizures (VI, VII, IX) and two patients (XII and XIV) with somatomotor seizures had normal ictal SPECT scans; patient XI and XIII had right and left frontal hyperperfusion, respectively.
All patients were given an extensive coverage of the cortical convexity with subdural electrodes through large unilateral (n = 13) or bilateral (n = 3) craniotomies. The number of implanted electrodes ranged from 64 to 160 contacts. Bipolar cortical stimulation was carried out through the implanted electrodes using squares pulses with current varying from 3 to 8 mA, 0.1 ms in duration, and 100 Hz. Follow-up time ranged from 1 to 4 years (m = 1.9 years).
Interictal invasive recording findings showed widespread spiking areas in 13 patients and secondary bilateral synchrony in three (Table 2). Ictal invasive recordings showed focal seizure onset in all patients. All patients underwent cortical resections that included the entire ictal zone and the most active interictal areas as well, whenever possible, sparing eloquent cortical regions defined by means of preresection cortical stimulation. There were six frontal (Fig. 1), two parietal, one temporooccipital, four rolandic (Fig. 2), and three posterior quadrant resections. Posterior quadrant resections included the removal of the occipital, parietal, and posterior temporal cortex. Additionally, a posterior transventricular hippocampectomy was performed.
Figure 1. Patient IX, who showed a large frontomesial focus and secondary bilateral synchrony. A: Skull radiograph showing the extensive bilateral frontomesial subdural electrodes coverage. B: Intraoperative view of the left hemisphere with superimposed invasive neurophysiologic data. The frontal pole is on the left side, the parietal lobe is on the right, and the mesial surface is seen superiorly. Pink tags, epileptogenic area; green tags, motor strip; blue tag, Broca’s area; double line, extent of resection.
Figure 2. Patient XII, who disclosed a focus restricted to the dominant rolandic areas. A: Skull radiograph showing coverage of almost all the left hemisphere.B: Intraoperative view of the left hemisphere with superimposed invasive neurophysiologic data. The frontal pole is on the right side, the parietal lobe is on the left, and the sylvian fissure is seen superiorly. Ruler in centimeters. White tag, Broca’s area; dark blue tags, motor strip; light blue tags, epileptogenic area; yellow tag, site from which the patient’s typical simple partial seizure was obtained after cortical stimulation; double line, extent of resection. EEG seizure onset preceded or was concomitant with the clinical manifestations in all patients. Seizures initiated simultaneously in up to three contiguous electrodes in eight patients; in four to six electrodes in four patients, and in more than six electrodes in four patients. No patient had seizures starting simultaneously in different noncontiguous cortical areas. Seizure-onset patterns included low-amplitude fast activity evolving into a recruiting rhythm (n = 9), rhythmic theta activity (n = 4), and high-amplitude spiking (n = 3).
Only one patient had SMA seizures originating from the SMA proper. The other two patients had epileptogenic zones outside this region. Interestingly, in one of these patients, the same typical SMA seizures could be triggered by the stimulation of both SMA cortex. Patients with simple partial motor or somatosensitive seizures also disclosed epileptogenic areas well beyond the boundaries of the rolandic cortex. In only one of eight patients with such seizures was the epileptogenic area restricted to the rolandic gyri, whereas in the other seven, ictally spiking areas anterior or posterior to the rolandic cortex were present.
The ability to reproduce stimuli during cortical stimulation helped patients to define further their simple partial seizures, and in 68% of them, the typical partial seizures were obtained. Only one of 11 patients in whom cortical stimulation effectively reproduced the typical simple partial seizure has not been rendered seizure free after surgery. Conversely, no simple partial seizures could be elicited by cortical stimulation in two of three patients who have not been rendered seizure free after surgery.
Thirteen patients had been rendered seizure free after surgery, and three had 90% seizure-frequency reduction. Pathological findings included gliosis (with loss of gray matter; n = 10), cortical dysplasia (n = 5), or no abnormalities (n = 1). Six patients had transient postoperative neurologic morbidity: hemiparesis (n = 1; 4 days), facial paresis with dysphasia (n = 3; 1 week, 1 week, and 2 weeks, respectively), facial paresis only (n = 1; 2 weeks), and unilateral crural paresis (n = 1; 1 month). All patients given posterior quadrant resections (I, III, and X) were hemianoptic preoperatively.
Eighty-one percent of the patients in this series were rendered seizure free after surgery. This might be considered a good surgical outcome rate compared with previously published data (11–15). Some aspects of the resections performed in this series may be emphasized. The extent of the resections was larger than those performed in patients with temporal lobe epilepsy. They were maximized to include the ictal and prevailing interictal areas and were limited basically by the presence of eloquent cortex, or most frequently, by dominant draining veins. Special attention was paid to keep the surrounding arteries and veins intact when performing subpial resections near or inside eloquent cortex (i.e., rolandic or perirolandic). All transient neurologic morbidity seen in these patients was expected preoperatively and was directly related to the cortical areas defined as targets for removal (i.e., facial paresis after lower rolandic resections) (16). Contrary to others’ findings (17), our preliminary experience with multiple subpial transections alone in eloquent extratemporal cortex has been very poor (personal communication). We prefer to resect relatively eloquent cortex (i.e., face area cortex) and leave absolutely eloquent cortex intact.
Four patients had areas of microdysgenesis not detected preoperatively by MRI. Conversely, the main pathological finding was gliosis with loss of gray matter, mostly compatible with the normal preoperative MR scans. In contrast to patients with subpial gliotic changes alone, the patients with gliosis and gray matter loss seem to have a better surgical outcome. In these four patients with preoperatively undetected cortical dysplasia, there was no alteration of the gyral pattern, which was also true for the patients in whom gliosis was found. It is unlikely that improvement in anatomic MR techniques would allow us to detect further abnormalities in these types of patients.
As noted by others (18), there was no localizing clinical sign in our three patients with SMA-type seizures. Neither the direction of head rotation nor the asymmetric posturing was able to predict the SMA involved in the generation of seizures. The only way to localize foci adequately in patients with SMA seizures, secondary bilateral synchrony, and normal MRI was extensive invasive coverage of the frontal mesial surface and convexity. Even using this paradigm, a bilateral and synchronous sentinel spike was seen immediately or a few seconds before the ictal recruiting pattern could be seen over one of the mesial surfaces. This might be related to a more widespread epileptogenesis in these patients. Our findings showed that patients with SMA and somatomotor seizures often have extra-SMA and extrarolandic epileptogenic zones. These findings further emphasized the need for adequately defining epileptogenic and symptomatogenic zones in these patients. Complex partial seizures were seen arising from all cerebral lobes. As compared with those originating from the temporal lobes, extratemporal complex partial seizures originated from a much larger cortical surface, and in five of eight patients, the epileptogenic area was multilobar. There was a better surgical outcome in patients in whom cortical stimulation was able to reproduce the patient’s typical seizure.
Ictal SPECT would be able to define the quadrant (anterior, posterior; left or right) in ∼50% of the patients with extratemporal refractory epilepsy and normal MRI, but it lacks the spatial and anatomic resolution needed to obviate the need for invasive recordings. Conversely, in the majority of the patients, intensive video-EEG monitoring is able to guide adequately the establishment of a subdural grid implantation pattern. All patients with refractory extratemporal epilepsy and normal MRI have been ultimately given invasive recordings in our series if cortical resection is being contemplated. Subdural grid coverage should be extensive in such patients; limited coverage of the cortical surface with subdural strips or epidural electrodes may very likely lead to inadequate localization or mapping.
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