Epilepsy Research (2010) 89, 133—141

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Intra-operative electrocorticography in lesional

M. Tripathi, A. Garg, S. Gaikwad, C.S. Bal, Sarkar Chitra, K. Prasad, H.H. Dash, B.S. Sharma, P. Sarat. Chandra ∗

Neurosciences Center, All India Institute of Medical Sciences, New Delhi, India

Received 19 June 2009; received in revised form 26 November 2009; accepted 26 December 2009 Available online 15 January 2010

KEYWORDS Summary Intra-operative electrocorticography (ECoG) is useful in to delin- Electrocorticography; eate margins of epileptogenic zone, guide resection and evaluate completeness of resection in Intra-operative surgically remediable intractable . The study evaluated 157 cases (2000—2008). The electrocorticography; preoperative evaluation also included ictal SPECT (122) and PET in 32 cases. All were lesional Epilepsy; cases, 51% (81) of patients had >1 /day and another 1/3rd (51) had >1/week. Pre and Intractable epilepsy; post resection ECoG was performed in all cases. A total of 372 recordings were performed Epilepsy surgery; in 157 cases. Second post-operative recordings (42) and third post-operative recordings (16) Electrical mapping were also performed. Site of recordings included lateral temporal (61), frontal (39), parietal (37), hippocampal (16) and occipital (4). 129/157 cases (82%) showing improvement on ECoG, 30/42 cases showed improvement in 2nd post resection, 8/16 showed improvement in the 3rd post-operative ECoG. 116/157 (73%) patients had good outcome (Engel I and II) at follow up (12—94 months, mean 18.2 months). Of these, 104 patients (80%) showed improvement on post- operative ECoG. 12 had good outcome despite no improvement on ECoG. The improvement in ECoG correlated significantly with clinical improvement [Sensitivity: 100% (95% CI; 96—100%); specificity: 68.3% (95% CI; 51.8—81.4%); positive predictive value: 89.9% (95% CI, 83.1—94.3%); negative predictive value: 100% (95% CI, 85—100%)]. The level of agreement was 91.72% (kappa: 0.76). Concluding, pre and post resection ECoG correlated with its grade of severity and clinical outcome. © 2010 Elsevier B.V. All rights reserved.

Introduction

Electrocorticography along with cortical stimulation map- ∗ ping was perhaps first described by Penfield (1939). Using Corresponding author at: Room 607, 6th Floor, Center, All India Institute of Medical Sciences [AIIMS], New Delhi this, they demonstrated that stimulation of the supplemen- 110 029, India. tary area resulted in simultaneous movements and tonic E-mail addresses: [email protected], posturing of both proximal and distal muscles along with [email protected] (P.Sarat. Chandra). speech arrest.

0920-1211/$ — see front matter © 2010 Elsevier B.V. All rights reserved. doi:10.1016/j.eplepsyres.2009.12.007 134 M. Tripathi et al.

The hypothesis for a successful epilepsy surgery is based Despite its common use, only a few studies are available on the principle that removal of both lesional as well as to prove its worthiness and establish evidence justifying its the surrounding epileptogenic area is necessary for achiev- necessity (Keene et al., 2000) ing seizure freedom (Luders and Awad, 1991). Hence, it is In this paper, we present our experience with ECoG to important that, both should be delineated before surgery. determine if it provided useful information for predicting However, epileptogenic zones are often difficult to identify, surgical success and review the current role and controver- because they may be found in and around the margin of, sies of ECoG in surgery for surgically remediable epilepsy or remote from a lesion (Cascino et al., 1992; Awad et al., and also review the existing literature. 1991a,b; Wennberg et al., 1999). The scalp EEG is helpful but may not be precise enough to localize the epileptogenic area (Westmoreland, 1998). For greater precision, either intra- Material and methods operative or extra-operative subdural electrocorticography (ECoG) is often used to guide surgical resection of both the The present study reviewed all the ECoG recordings, patient imaging lesion and the epileptogenic zone (Pathak and Blume, 1997; and electrophysiological data from January 2000 till October 2008 Pilcher et al., 1993; Tran et al., 1997). performed at our center. The area of interictal spiking or the irritative zone is often All the patients underwent a standard work up for medically intractable epilepsy. Inclusion criteria for this series included only wider than the ictal onset zone (area where the seizure orig- those cases with a MRI substrate i.e. lesional cases with intractable inates) which is considered as a gold standard for localizing epilepsy with concordance seen on video EEG, MRI, PET and/or the epileptogenic zone (Luders et al., 1993). ictal—interictal SPECT.In patients, where no concordance was found Failure of seizure freedom following surgery could be due were subjected to invasive video EEG. Similarly in hippocampal scle- to a variety of causes and varies from patient to patient. In rosis, the present series included only unilateral pathology with the majority of cases, incomplete resection of the epilepto- concordance. The frequency of were >1/day in 51% (81 genic zone immediately adjacent to the resected area was cases), >1/week in 31% (51 cases), >1/month in 12% (19 cases) and thought to be the single most common cause until a few >1/year in only 6 cases. This included a detailed clinical history, years ago (Awad et al., 1991a,b; Wyler et al., 1989). interictal EEG’s, long-term video EEG (VEEG), epilepsy protocol MR Intra-operative electrocorticography (ECoG) is widely imaging, and SPECT. Ictal SPECT in addition was performed in 122 cases and PET in 32 cases. Patients were selected for ECoG guided utilized for electrical mapping of the epileptogenic zone resection only if there was a concordance of at least 3/4 parameters during epilepsy surgery. It is useful to delineate the mar- i.e. VEEG, MRI, interictal/ictal SPECT, and PET (flurodeoxyglucose). gins epileptogenic zone, guides the surgeon in achieving PET was not usually done for lesions seen on MR imaging unless resection and is also of value to evaluate the complete- there was discordance between the VEEG, SPECT and MR imaging ness of resection. It has been found to be particularly useful data. PET was preferred for lesions like cortical dysplasias, tuberous in resective surgeries of neocortical foci (especially devel- sclerosis and patients with ‘substrate negative’ pathologies. opmental lesions like cortical dysplasias) and for tailored The ECoG recordings in the earlier part of the study were per- resections in hippocampal sclerosis (Ojemann, 1992). The formed using a 32-channel machine (Nihon Kohden). Since 2007, we ECoG can be a valuable tool during multiple subpial tran- have been using a 64-channel machine (Nicolet, Viasys). Recording sections (MST). from neocortical surfaces were usually performed by using a large grid (32 contacts) to cover the entire area representing the lesion its The technique of ECoG, was pioneered by Penfield and perilesional areas. Recording from the (in mesial tem- Jasper in the early 1950s to map focal interictal spiking poral sclerosis) was done after performing a antero lateral temporal and to determine the extent of the resection (Penfield and lobectomy, by placing 1 × 4 strip electrode over the hippocampus. Jasper, 1954). The obvious advantages of the intra-operative Post-operative recordings were done both from the margin of the ECoG’s are: (i) they allow placement of recording and stim- area and nearby exposed normal parenchyma. The reference ulation electrodes; (ii) recordings can be performed before electrode was placed over the forehead. The recordings were per- and after each stage of resection to assess the completeness formed both by the referential and bipolar derivations. of surgery; (iii) it allows direct electrical stimulation of the All the ECoG interpretation was done by a single neurologist brain so that the regions involved in functions may be spared who was blinded to the anatomical location of the grid. The ECoG by the resection (e.g. eloquent cortex) (iv) no risks associ- in all cases was performed under standard anesthetic conditions with induction using isoflurane. After and dural open- ated with long-term placement e.g. infection (Zumsteg and ing, anesthesia was maintained with nitrous oxide and intravenous Wieser, 2000). The major limitations of ECoG are: (i) the narcotics with reduction (to 0.5% of isoflurane) inhalational agents. limited sampling time; (ii) spontaneous epileptiform activ- Core body temperature was maintained above 35.5 ◦C. The low- ity consists exclusively of interictal spikes and sharp waves, frequency filter was set at 1 Hz, the high frequency filter at 70 Hz, and seizures are rarely recorded. Thus in most of the cases, and sensitivity was between 300 and 5000 ␮V/mm depending on localization of the ictal focus is based on a hypothesis that the amplitude of the background and discharges. ECoG abnormali- it corresponds to the interictal activity, which is yet to be ties were graded using the following score that emphasized changes proven (iii) it is difficult to distinguish primary epileptiform in background frequencies along with the presence of interictal or discharges from secondarily propagated discharges arising ictal epileptiform activity. at a distant epileptogenic site; (iv) both, the background activity and epileptiform discharges may be altered by the Method of grading anesthetics, narcotic analgesics and by the surgery itself (Zumsteg and Wieser, 2000). We preferred to use the grading described by Mathern et al. About 80—84% of epilepsy surgery centers around the (Mathern et al., 2000; Cepeda et al., 2005, 2006). The scoring sys- world still perform ECoG in some or all of their patients with tem was prospectively performed in 62 patients. In the rest of the partial epilepsy (Engel, 1987). patients, the ECoG Intraoperative Electrocorticography in Lesional Epilepsy 135

ECoG Score 1: Normal background of mixed gamma, beta and showed electrical improvement at surgery. The distribution alpha frequencies of moderate to low amplitude (i.e., usually of these patients included (with both electrical and clinical <20—30 mV). A few low amplitude spikes could be observed good outcome) temporal: 44/61; 72%, frontal: 20/39; 51%, ECoG Score 2: Loss of fast (>20 Hz) background frequencies, but parietal: 24/37; 64%, hippocampal: 14/16 and occipital 2/4. otherwise a background of mixed alpha, beta and delta frequen- 12 patients thus had a good clinical outcome despite having cies of low to moderate amplitude. Repeated but non-continuous, no intra-operative electrical improvement. spikes, polyspikes or paroxysmal fast activity of medium amplitude often observed Analyzing the scoring system, out of 157 preoperative ECoG Score 3: Mostly 6—20 Hz background frequencies with some recordings, 124 (78%) had scores of 2 & 3. 21 (13%) cases localized nearly continuous interictal epileptiform features of had a score of 4 and only 12 (7%) had a score 5. moderate amplitude or persistent repetitive spiking. Very rarely, The pathologies included cortical dysplasias [54], tuber- electrographic seizures can be captured ous sclerosis [11], mesial temporal sclerosis [16], tumors: ECoG Score 4: Slow (<6 Hz) background frequencies with continu- [29] (dysembryoplastic neuroepithelial tumor (DNT): 19 ous synchronous features of moderate to high amplitude. Multiple cases, ganglioglioma: 7 cases, pilocytic astrocytoma: 3 independent epileptiform abnormalities (polyspikes, paroxysmal cases). There were 11 tuberculomas and 5 neurocysticer- fast activity and electrographic seizures) could be recorded cosis. Thirty-two (20.9%) specimens showed dual lesions, ECoG Score 5: Slow rhythmic usually synchronous background majority (84%) of which were focal cortical dysplasia (FCD) (<4 Hz), often of high amplitude. Continuous synchronized or inde- pendent high amplitude epileptiform abnormalities in multiple with coexisting ganglioglioma (GG-15 cases) or DNT (12 cortical sites could be observed. Ictal discharges were rarely cases), while the others were mesial temporal sclerosis recorded but observed in surrounding cortex (MTS) in conjunction with parasitic cysts (2 cases) and with cavernoma (1 case). Other less common, yet significant find- An ECoG score of 2—5 is considered abnormal and these areas ings in terms of causative etiologies of seizures included should always be included within the resective zone. An ECoG Score subpial gliosis (19 cases), old haemorrhage (7 cases), non- 1 is considered relevant depending on its relation to the lesion. specific changes (5 cases). Three of five of the last had For instance, if there was widespread activity consistent with ECoG normal MR imaging, however ictal SPECT, PET and VEEG Score 1 activity, then ‘chasing the spikes’ was avoided and the max- suggested a strong concordance. imally abnormal area was resected. If this activity is more focal and The improvement in ECoG correlated significantly with amenable to surgical resection, then it was utilized for guiding surgi- clinical improvement [Sensitivity: 100% (95% CI; 96—100%); cal resection. Surgery always included wide resection, making sure specificity: 68.3% (95% CI; 51.8—81.4%); positive predic- that the subcortical white matter was also included in the resection. A post resection ECoG was always performed. If significant abnor- tive value: 89.9% (95% CI, 83.1—94.3%); negative predictive mal activity was still noted from the margins, further resection was value: 100% (95% CI, 85—100%)]. The level of agreement performed. was 91.72% (kappa: 0.76). All the results are summarized The final post-operative recording was considered improved if in Table 1. the recording was normal or showed ECoG score 1 in certain situa- ECoG seemed to correlate better with clinically good out- tions as described above. come for temporal lesions. 95% (58/61) of patients from Preoperatively, intra and post-operatively, patients were con- both hippocampal and lateral temporal with good outcome tinued on the same antiepileptic drugs (AED’s) monitored with had also demonstrated adequate electrical improvement on appropriate serum levels. ECoG (Figs. 1 and 2). The outcome was classified using Engel grading (Engel, 1987)at 12 months follow up. All patients underwent a 30 min EEG at 3, 6, and 12 months at follow up. Discussion

Results According to Rasmussen (1983), the removal of the ‘‘epileptogenic zone’’ consisting of the lesion and a sur- rounding critical mass of tissue is required for a successful All the patients were preoperatively evaluated in Neurology surgical outcome. ECoG has been reported to provide use- Unit I. All the ECoG’s were interpreted by the same neurol- ful information for the localization of this area at the time ogist and operated by a single surgeon. The study included of surgery (Engel, 1987; Green et al., 1949; Walker, 1949; 157 cases who underwent a total of 372 recordings each for Gloor, 1975; Chatrian and Quesney, 1997; Walker et al., about 30 min. post-operative recordings were performed in 1960; Tsai et al., 1993a,b). all, 2nd post-operative recordings in 42 (28%) and third post- While there have been a number of publications related operative recordings in 16 cases (6.7%). Sites of recordings to ECoG, most of them have been case reports or series with- included temporal (61 cases; with frontal overlay in 8 cases), out a proper control group. Hence the role of the technique frontal (39 cases; with a small temporal overlay in 4 and pari- has been questioned (Walker et al., 1960). etal overlay in 3 cases), hippocampal (16) and occipital in 4 The potential advantages of ECoG are mentioned below cases. with the corresponding literature review. A total of 129/157 patients (82%) had satisfactory improvement on post resection ECoG. A total of 116/157 (73%) had a good outcome (Engel grade I and II) at a follow Potential advantages of ECoG up varying from 12 to 94 months (mean 18.2 months). As per location, patients with good outcome included lateral tem- The ECoG activity is similar to that recorded from the scalp poral (46/61; 75%), frontal (25/39; 64%), parietal (27/37; electroencephalogram, consisting of isolated spikes, brief 72%), hippocampal (15/16; 93%), and occipital was 3/4. Of bursts of spikes or runs of sharp waves. However, they the 116 patients with good outcome, 104 (89%) patients look more magnified as they are recorded directly from the 136 M. Tripathi et al.

Propagation of the epileptiform discharge was commonly Table 1 Summary of results. seen from the hippocampus, to and from the subtemporal Total no. of cases 157 cases with 392 cortex (Kanazawa et al., 1996; Graf et al., 1984; Alarcon et recordings al., 1997). In the present study, only 20% of patients had ictal patterns, while a majority of patients (78%) had interictal Post resection recordings patterns. Prolonged sustained ictal activity was recorded in First recording 157 (100%) only 7% of cases. Second recording 42 (28%) One study (Panet-Raymond and Gotman, 1990) has sug- Third recording 16 (6.7%) gested that in addition to these epileptiform discharges, Site of recordings activity might also give useful information as Temporal (with frontal 61(8) to the location of the epileptiform tissue in patients in overlay) whom spikes were not found on ECoG. [n = 40]. However, Frontal (with frontal, 39(4, 3) the authors do suggest caution when using this method in parietal overlay) individual cases. Hippocampal 16 Devinsky (2004) found new epileptiform discharges on Occipital 4 ECoG in 24% of , which were not pre- viously found by scalp electroencephalograms even with the Pathologies use of sphenoidal electrodes. On the other hand, Engel et Cortical dysplasias (CD) 54 al. (1976) did not obtained any additional information from Tuberous sclerosis 11 the ECoG compared to the preoperative scalp EEG. Hippocampal sclerosis (HS) 16 ECoG seldom records ictal events, but rather interictal Tumors 29 epileptiform activity. The relationship between the epilep- Dual pathology 32 tic zone (area of origin of the epileptic seizure) and the (CD + ganglioglioma: irritative zone (area of maximum interictal epileptiform 15; CD + dysembryonic discharge) is not completely understood. In particular, the neuroepithelial degree to which the two zones overlap, especially on the tumor: 12; ECoG recording is unclear. It has been hypothesized that HS + parasitic cysts: 1; the frequency of this activity is proportional to the proxim- HS + cavernoma: 1) ity to the ‘epileptogenic area’. Alarcon et al. (1997) found Subpial gliosis 19 that the removal of this area lead to a good surgical out- Old haemorrhage 7 come, even if areas of less frequent discharging were left Non-specific changes 5 untouched. If the area of maximal discharging was not com- Outcome assessment Follow up: 12—94 pletely resected, the surgical outcome was more likely to months (mean 18.2 be poor. An earlier study (Tran et al., 1995) had found no months) such association. However it should be noted that the lat- Good outcome (Engel I and II); 116/157 (73%); ter study has used visual analysis of the ECoG as compared Total no. patients showing 129/157 (82%); the former study which used a computerized spike detection improvement on ECoG; No. of program. patients showing good clinical In the present study, 73% of the patients who have outcome + improvement on a good clinical outcome showed improved ECoG scores ECoG in 90% of these patients. ECoG seemed to correlate Clinical outcome (Engel I and II) as per location better in temporal lesions with regard to clinical out- Lateral temporal 46/61; 75% come (95%). It should be however noted that most of Frontal 25/39; 64% the patients in the present series were lesional epilep- Parietal 27/37; 72% sies. Hippocampal 15/16; 93% Electrical stimulation of the cortex at the time of ECoG Occipital 3/4 is useful for further localization of the epiletogenic zone Clinical outcome as per ECoG score of severity (Gloor, 1975). The area of brain producing aura of the Scores 2 and 3 124 (78%) patient on electrical cortical simulation has been reported Scores 4 21 (13%) to have strong correlation with the epileptic zone (Bernier Scores 5 12 (7%) et al., 1990; Wieser et al., 1979; Halgren et al., 1978). This was particularly the case when the area from which the responses matched closely with the area exhibiting the surface of the brain. They are often multifocal with a wide greatest epileptic discharge seen on ECoG. However, this distribution and have been commonly recorded from tem- hypothesis was not agreed upon in a study (Gloor, 1975), poral cortex. More commonly, the epileptiform discharges where they proposed that the clinical symptomatology may were reported to have been recorded from the hippocam- not be related to this area of stimuli, but reflects a distant pal structures and inferiomesial surfaces of the temporal area to which the discharge has spread. tip. To a much lesser extent, they were recorded from the After-discharges arising from electrical cortical stimu- lateral temporal cortices and more so from the posterior lation are of questionable value in the localization of the temporal cortices (Walker, 1949; Gloor, 1975; Chatrian and epileptic zone. (Penfield and Jasper, 1954; Gloor, 1975; Quesney, 1997; Stefon et al., 1991; Tsai et al., 1993a,b). Ajmone, 1973). Intraoperative Electrocorticography in Lesional Epilepsy 137

Figure 1 (a) MR imaging, axial section showing multiple tubers with a sub ependymal giant cell astrocytoma in the ventricle of a 3 year old male child with tuberous sclerosis, with 8—10 seizures in a week. PET (b) showed a large hypometabolic area corresponding to the large tuber in the left frontal lobe. Video EEG showed the ictal onset with slowing in F8 corresponding to the MRI and PET. At surgery (c), marked abnormality in this area was seen on ECoG (d). Note the ECoG has been scored as described in the text. Following a large frontal resection, post resection ECoG still showed significant activity (e and f) from the posterior margin of the surgical resection. Following a second resection (g), the ECoG showed return to normalcy (h). Note the line drawn in (g) shows the margin of cortex after the first resection. Patient as 16 months of follow up had Engel Class I outcome.

The role of the ECoG in determining the surgical outcome poral cortex after completion of the procedure. These is unclear. McBride et al. (1991) and Engel (1987) did not find discharges were found to have no predictive value (Cendes an association between the site of dominant intra-operative et al., 1993; Blume et al., 1997; Ojemann, 1992). However, ECoG epileptiform discharge and the surgical outcome. Cor- one interesting study did demonstrate progressive decrease relation between the location of discharge and underlying in the abnormality of ECoG with progressive excision of the pathology was also not found (Engel et al., 1976). amygdala and hippocampus (Oliveira et al., 2006). Bengzon et al. (1968) noted a significant difference in A possible explanation for the lack of consensus in the the surgical outcome between patients with residual spikes usefulness of ECoG to predict seizure outcome may lie in compared to spike-free post resection recordings. Thirty- the surgical procedure itself. While most centers that have six percent of patients who were seizure-free post-surgery reported the use of ECoG-performed standardized temporal had residual spike; whereas 75% of patients who were not lobe resections, only a few actually tailored the resection seizure-free had residual spikes on post resection ECoG. according to ECoG findings (Ojemann, 1992; McKhann et al., These findings were similar to those reported by others 2000). (Penfield and Jasper, 1954; Fiol et al., 1993; Wyllie et al., In the present series, of a total of 157 cases, 77 (49%) 1987; Tanaka et al., 1996; McBride et al., 1991). were operated for temporal foci. Of these 61(79%) had a Other investigators have not been able to confirm good clinical outcome (Engel I and II). In 58 (95%) of these the relationship between the degree of epileptiform dis- cases, ECoG showed a significant improvement following charges seen on the post resection ECoG and the outcome resection. However we do agree that while we did per- (Walker et al., 1960; Falconer, 1958; Fenyes et al., 1961; form repeat resections for lateral temporal lesions, tailored Gibbs et al., 1958; Gallentine and Mikati, 2009). This was resections were not performed for hippocampal lesions. especially the case in patients in whom selective amygdalo- While hippocampal recordings were performed in cases of hippocampectomy was performed. In this situation, new mesial temporal sclerosis, resection of amygdale and hip- epileptiform discharges were often recorded from the tem- pocampus was done as per standard procedure. 138 M. Tripathi et al.

was topographically distinct from the region of the tumor- involved brain and its removal increased the chance of a better outcome. Another series also (Berger et al., 1993) reported patients with intractable epilepsy, associated with low grade tumors undergoing surgery with better outcome under ECoG- guidance. Forty-one out of 45 of these patients (91%) became seizure-free and the use of ECoG was advocated. Similar findings were reported with cavernous hemangiomas (Cohen et al., 1995). Other studies also reported greater control of seizures in both children and adults when per- formed under ECoG guidance (Gonzalez and Elridge, 1962; Drake et al., 1987) These studies have been based on retrospective review of case series. Comparison between ECoG-guided resections and non-ECoG-guided resection for similar groups of lesions Figure 2 shows the distribution of patients (upper line) ver- have not been prospectively done. There was one report sus the no. of patients with good clinical outcome (middle line) of an attempted (Tran et al., 1997) controlled retrospec- and the no. of patients who have had good clinical outcome tive series review in which patients with structural lesions along with significant improvement seen on ECoG. The improve- present underwent resection of the lesion to normal tis- ment in ECoG correlated significantly with the clinical outcome. sue margins. ECoG was recorded pre- and post resection, The improvement in ECoG correlated significantly with clinical but not used to determine the amount of surgical resec- improvement [Sensitivity: 100% (95% CI; 96—100%); specificity: tion. Patient outcome was based upon seizure-free state. 68.3% (95% CI; 51.8—81.4%); positive predictive value: 89.9% ECoGs were analysed for spike distribution and spike dis- (95% CI, 83.1—94.3%); negative predictive value: 100% (95% charge rate. Spike distribution in the pre resection ECoG did CI, 85—100%)]. LT: lateral temporal, FR: frontal, PAR: parietal, not correlate with outcome. On post resection ECoG, spikes HIPP: hippocampal, OCC: occipital. were noted along the edge of the resection as well as extra- marginally in equal amounts between patients who became Non-lesional extratemporal resections seizure-free post resection and those who did not. These findings support the use of lesionectomy as the first step in seizure control in lesional cases. In the present study though Evidence supporting usefulness of ECoG in extratemporal not prospective, post resection ECoG was performed in all resections is scanty. Most of the literature usually pertains cases (157); 28% requiring a second post resection recording to lesional cases. Some studies (Quesney, 1992; Sadanova et and 6.7% requiring a third post resection recording. al., 1992) have pointed out that in patients whose seizures Palmini et al. (1995) have reported long runs of originated in the frontal lobes, showed no clear relationship epileptiform discharges on ECoG consisting of repetitive between the amount of epileptogenic tissue removed and electrographic seizures, repetitive bursting discharges or a successful surgical outcome. Similar findings have been continuous rhythmic spiking which were often co-localized noted in ECoG recordings of patients with seizures arising with MR imaging. The completeness of resection of the from the centroparietal region and occipital areas (Quesney, epileptiform activity on ECOC correlated with the surgical 1992; Sadanova et al., 1992). outcome. (Tripathi et al., 2008; Wennberg et al., 1999). These findings suggest that for non-lesional extratempo- The experience presented here represents ECoG from ral epilepsies, the best solution may to use subdural grids. all pathologies collected from a single center. Though this Another approach may involve the use of other imaging tech- seems heterogeneous in approach, a much larger sample size niques, for example positron emission tomography along will be required to validate comparisons between individual with more recent techniques with MR imaging (Olson et al., pathologies. This paper represents day to day practice of 1990; Chandra et al., 2006). applicability of ECoG over heterogeneous etiologies.

Lesional, temporal and extratemporal resections Electrical stimulation and cortical mapping The use of ECoG in patients with structural lesions on imag- ing studies remains one of its best used indications albeit Electrical stimulation during ECoG recordings for epilepsy being controversial. Earlier studies from Montreal Neuro- surgery under local anaesthesia was first performed and logical Institute suggest a good outcome when the lesion is developed by Penfield and Jasper in the early 1950s (Penfield removed with the surrounding epileptogenic cortex as deter- and Jasper, 1954). This procedure provided insight into the mined by ECoG (Sadanova et al., 1992; Rasmussen, 1975). functional anatomy of brain, particularly towards location This point of view has been supported by Pilcher et al. (1993) of language, motor and sensory areas. Electrical stimula- who found that eleven out of twelve patients who underwent tion still forms a key procedure for localization of these surgery for ganglioglioma, were seizure-free at 3.1 years areas thus preventing neurological deficits following resec- post-surgery compared with a literature control of 21 out tion of an epileptogenic focus. Another important usefulness of 39 (54%) patients with ganglioglioma in whom only the is reproduction of the patient’s habitual aura and partial lesion was resected. They noted that the epileptogenic zone seizures by local cortical or depth electrode stimulation. Intraoperative Electrocorticography in Lesional Epilepsy 139

If the area that triggers the patient’s habitual attack and Jasper, 1954), (2) partial excision which may lead to postop- coincides with the region of active spiking, this clearly delin- erative seizures, or (3) from cortical isolation which is also eates the epileptogenic zone (Quesney and Niedermeyer, considered benign (Wennberg et al., 1997; Wennberg et al., 1993). In a study comprising 30 randomly selected patients 1999). with medically refractory TLE (Stefan et al., 1996), found that that ECoG provides reliable intra-operative mapping of epileptogenic brain tissue to be resected. All patients Conclusion underwent intra-operative ECoG as well as electrical stim- ulation using cortical and acute depth electrodes prior to ECoG while being widely used in epilepsy surgery is but temporal lobectomy. Special emphasis was placed on the still controversial in its efficacy and utility. This is partic- reproduction of patient’s warning by electrical stimulation ularly so as there are no prospective randomized studies. of mesial temporal lobe structures. A strong correlation was Despite its limitations, it remains a necessary tool in epilepsy found between the symptoms induced by stimulation and surgery. In our study, of a total of 73% (116/157) had a good the patient’s habitual warning, thus providing additional outcome following resective surgeries, 90% showed electri- intra-operative localizing evidence regarding the anatomical cal improvement in post resection ECoG. More than a third substrate involved in the genesis of habitual seizure. of our patients seemed to have benefitted from 2nd and Another important utility of intra-operative electrical 3rd post resection recording which allowed the surgeon to stimulation is to assess the cortical sites involved in memory extend the degree of resection. The improvement in ECoG functions, thereby providing further insight into the mech- correlated significantly with clinical improvement. However anisms of memory and also to avoid memory deficits after the conclusion should be taken with caution as we do agree epilepsy surgery (Ojemann and Dodrill, 1985). upon certain short comings in this paper (1) The same scoring Identification of the central sulcus, which can be difficult system was used for all pathologies i.e. cortical dysplasias visually when anatomy becomes distorted by pathology, can (CD) vs. others. It is expected that in CD, the pre resec- either be identified by motor mapping or by somatosensory- tion ECoG scores would be more abnormal e.g. 3—4. (2) evoked potentials (phase reversal technique) (Sala et al., The ‘‘shock effect’’ on ECoG following surgical resection 2002). The latter is often most helpful in children younger which may provide a false post resection score. (3) In con- than 5 years (Berger, 1995), when direct electrical stimula- trast to this, transient excitatory effect of the surrounding tion of the motor cortex often requires higher intensities cortex following resection may not require resection as this of current than that needed to elicit an AD (Goldring may subside on its own. However with a background of a and Gregorie, 1984). Intra-operative mapping for language majority of our patients having a high seizure frequency (51% requires an awake patient, and can really only be performed with >1 episode/day) encouraged us to perform this study. in the adolescent patients. Younger children require place- This relatively unique scenario provided us a back ground ment of subdural electrodes and extra-operative functional to understand the relationship of the lesional MRI patholo- mapping. gies to quantitative abnormalities seen on ECoG pre and post resection and to further correlate it with the clinical outcome. Limitations of ECoG We also agree to the fact that an adequate resection in lesional epilepsy usually leads to a good outcome and The epileptiform activity seen on ECoG exclusively consists may not exactly reflect the usefulness of ECoG. However of interictal discharges. An hypothesis for lateralization and the authors would also like to reiterate that there are few localization of the epilepitogenic foci is essential before such large studies reported in literature, and this can form placement of ECoG electrodes. That is the reason, they are the basis of initiating prospective studies e.g. randomizing best suitable in lesional cases where concordance has been patients with or without post resection ECoG and evaluating established with other investigations before surgery. the outcome. However, it should be emphasized that the irritative zone, the area generating interictal activity may have different localization depending on the different type of Acknowledgement investigation. For instance, a scalp EEG gives the best overview but cannot delineate the margins and is least sensi- This study was partly supported by a grant from Department tive. The subdural electrodes while can accurately map the of Biotechnology, Ministry of Science and Technology, India. margin will provide only a limited overview as its area of cov- erage is limited. In contrast, the depth electrode defined irritative zone has practically no value. ECoG electrodes, References due to their close proximity, permit a direct identification of the boundaries of the generator. This recording can explore Ajmone, C. Marson, 1973. Electrocortigraphy. In: Remon, A. (Ed.), only a limited surface of the brain and no overview of the Handbook of electroencephalogram And Clinical Neurophysiol- ogy, Vol 10C. Elsevier, Amsterdam, pp. 3—49. whole brain, as obtained with scalp electrodes, is possible. Alarcon, G., Garcia Seoane, J.J., Binnie, C.D., Martin Miguel, M.C., The other limitation of ECoG is the potential misinterpre- Juler, J., Polkey, C.E., Elwes, R.D., Ortiz Blasco, J.M., 1997. tation of clinically non-relevant sharp transients. The new Origin and propagation of interictal discharges in the acute epileptiform discharges not recorded on pre resection ECoG electrocorticogram. Implications for pathophysiology and sur- presumably emerges from (1) surgical injury to irritated cor- gical treatment of temporal lobe epilepsy. Brain 120, 2259— tex, thought to be of no clinical significance (Penfield and 2282. 140 M. Tripathi et al.

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