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Seizure 2003; 12: 577–584

doi:10.1016/S1059-1311(03)00095-5

Intraoperative electrocorticography in epilepsy surgery: useful or not? ABRAHAM KURUVILLA & ROLAND FLINK Department of Clinical Neurophysiology, Centre for Neuroscience, Uppsala University Hospital, SE-751 85 Uppsala, Sweden Correspondence to: Dr Abraham Kuruvilla, M.D., Diplomate—American Board of Neurology, Diplomate—American Board of Clinical Neurophysiology, Section of Electroencephalography, Department of Neurology, Sree Chitra Tirunal Institute for Medical Sciences and Technology, Trivandrum 695 011, India. E-mail: [email protected]

Intraoperative electrocorticography (ECoG) has been traditionally used in the surgical management of medically refractory partial epilepsies to identify the location and limits of the epileptogenic area, to guide the extent of resection, and to assess its completeness. Although in clinical use for many years, the basic questions regarding indications and limitations of this method has remained unanswered. ECoG plays a major role in tailored temporal lobectomies, whereas, it serves no practical purpose in standard resection of medial temporal lobe epilepsy (TLE) with magnetic resonance imaging (MRI) evidence of mesial temporal sclerosis (MTS). Residual hippocampal spikes, unaltered by resection, correlate with a greater proportion of seizure recurrence. Intraoperative hippocampal ECoG can allow sparing of functionally important hippocampus, thus minimising postoperative memory decline. ECoG eminently aids removal of developmental malformations of brain, and most importantly, the excision of highly epileptogenic cortical dysplasias (CDs) for deciding the extent of resection for best seizure control. The ECoG can be a valuable tool during multiple subpial transections (MST). © 2003 BEA Trading Ltd. Published by Elsevier Ltd. All rights reserved. Key words: electrocorticography; intraoperative electrocorticography; epilepsy; intractable epilepsy; epilepsy surgery.

INTRODUCTION Surgical treatment is a viable option in carefully selected patients with medically refractory localisation related epilepsies1 . Demonstration of a structural lesion in the magnetic resonance imaging (MRI) does not prove that it is the cause of epilepsy and additional electroencephalographic (EEG) evidence is required to establish that the lesion is in fact responsible for the patient’s seizures2, 3 . Surgical treatment of lesional epilepsy requires that the lesion be removed and the epileptogenic tissue removed or disconnected4 . For best results, both should be delineated before surgery. However, epileptogenic zones are at times difficult to identify, because they may be found in and around the margin of, or remote from a lesion5–8 . The scalp EEG is helpful but may not be precise enough to localize the epileptogenic area9 . For greater precision, either intraoperative or 1059–1311/$30.00

extraoperative subdural electrocorticography (ECoG) is often used to guide surgical resection of both the lesion and the epileptogenic zone10–12 . The success of epilepsy surgery depends on the accurate localisation and complete removal of the epileptogenic zone13, 14 . The area of interictal spiking or the irritative zone is often wider than the ictal onset zone (area where the seizure originates) which is the gold standard for localising the epileptogenic zone3, 13 . The outcome of epilepsy surgery becomes evident only after serial follow up. The EEG could be an early predictor of the long-term result of surgery15 . The surgical failure and postoperative persistence of seizures could be due to a variety of causes and it may differ from patient to patient. In the majority of cases, incomplete resection of the epileptogenic zone immediately adjacent to the resected area was thought to be the single most common cause until a few years ago16, 17 . Despite well defined electro-

© 2003 BEA Trading Ltd. Published by Elsevier Ltd. All rights reserved.

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clinical syndromes of temporal lobe epilepsy (TLE) preoperatively, many patients relapse unexpectedly, either immediately or remotely from the time of surgery. The prominence of extrahippocampal and extratemporal epileptogenesis is found to be responsible for some of the surgical failures, irrespective of pathology. Thus, maturing epileptogenicity in a surgical scar is not considered to be a significant primary mechanism in patients who relapse after a seizure-free interval18 . The technique of ECoG, the intraoperative recording of cortical potentials, was pioneered by Penfield and Jasper in the early 1950s to map focal interictal spiking and to determine the extent of the resection19 . For the last five decades, intraoperative ECoG has been used to (1) localise the irritative zone, (2) to map out cortical functions, and (3) to predict the success of surgery for epilepsy. Despite its common use, only a few studies have been done to prove its effectiveness in these areas20 . The obvious advantages of the intraoperative ECoGs are: (i) they offer flexible placement of recording and stimulation electrodes; (ii) recordings can be performed before and after each stage of resection to assess the presence or absence of epileptiform activity; (iii) it allows direct electrical stimulation of the brain so that the regions involved in functions that must be spared by the resection (e.g. eloquent cortex) can be delineated with a high degree of confidence14, 21 . The major limitations of ECoG are: (i) the limited sampling time; (ii) spontaneous epileptiform activity consists exclusively of interictal spikes and sharp waves, and seizures are rarely recorded; (iii) it is impossible to distinguish primary epileptiform discharges from secondarily propagated discharges arising at a distant epileptogenic site; (iv) both the background activity and epileptiform discharges may be altered by the anaesthetics, narcotic analgesics and by the surgery itself14 . Despite the recent advances in clinical neurophysiology and its widespread utilisation in the surgical management of epilepsy, several questions about the role of ECoG in epilepsy surgery remains unanswered. About 80–84% of epilepsy surgery centres around the world still perform ECoG in some or all of their patients with partial epilepsy22, 23 . In this review, we intend to examine the current role and the future prospects of ECoG in surgery for medically refractory localisation related epilepsies.

CLINICAL NEUROPHYSIOLOGICAL DEFINITIONS AND LIMITATIONS Since intraoperative ECoGs are of very short duration, seizures are often not recorded and spontaneous

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epileptiform activity exclusively consists of interictal discharges. Lateralisation and some degree of localisation of the epileptogenic zone are absolutely necessary for allowing correct placement of electrodes during ECoG. The intraoperative ECoG, therefore, is not a substitute for presurgical evaluation14 . An epilepsy program can be successful only when the presurgical workup leads to a surgical resection, as much as possible, of the presumed epileptogenic zone (the region of cortex that generates epileptic seizures and the removal or disconnection of which is necessary and sufficient for seizure freedom) with a minimum of neurological or cognitive deficits. In this context, it should be remembered that the irritative zone (region of cortex that generates interictal epileptiform discharges in EEG) defined by different recording techniques (scalp, epidural, subdural and depth electrodes) will point to different cortical areas and have fairly overlapping but different significance. A scalp electrode-defined irritative zone gives the best overview and identification of the epileptogenic zone, but has poorly defined boundaries and is least sensitive. The epidural or subdural recording technique is very sensitive for detecting epileptiform discharges. However, its specificity for identifying the epileptogenic zone is unclear. These electrodes cover a very limited area of cortex and hence, it can provide only a limited overview. On the other hand, the depth electrode-defined irritative zone has essentially no value in defining the epileptogenic zone. ECoG electrodes, due to their close proximity to the generator permit a direct identification of the boundaries of the generator. This recording can explore only a limited surface of the brain and no overview of the whole brain, as obtained with scalp electrodes, is possible. The other difficulty during ECoG could be misidentification of clinically non-relevant sharp transients4 . The new epileptiform discharges not recorded on preresection ECoG presumably emerges from (1) surgical injury to irritated cortex, thought to be of no clinical significance24 , (2) activation by partial excision19 which may lead to postoperative seizures, or (3) from cortical isolation which is also considered benign25, 26 .

EFFECT OF ANAESTHESIA ON ECoG Anaesthesia is considered as an unmitigated drawback, whereas manipulation of anaesthetic levels can be used to optimise the display of epileptiform activity. Due to the effect of general anaesthesia, ECoG can at times show a disappointing and surprising lack of spike activity in the area of exploration27 . The local anaesthesia, essential for intraoperative

Intraoperative electrocorticography in epilepsy surgery

functional mapping, avoids these problems; but creates more technical difficulties. In addition, local anaesthesia may not be feasible in young children and apprehensive adults28 . Halogenated inhalational anaesthetics (halothane, nitrous oxide, desflurane, enflurane, isoflurane, sevoflurane) produce dose-related reduction in amplitude and frequency of EEG after initial activation29 . Since all general anaesthetics have serious drawbacks and, if general anaesthesia is absolutely necessary in an uncooperative patient, a short acting barbiturate may be used27, 30 . Eventhough satisfactory ECoG can be recorded with light anaesthesia, its effect on ECoG is in question31 . Discontinuing short acting anaesthetics 10–15 minutes before recording often yields satisfactory ECoG28 . Most narcotics, with the exception of alfentanil, have little influence on ECoG spike activity32 . High dose intravenous opioids (e.g. alfentanyl at 50 µg/kg as bolus) are known to increase the intraoperative epileptiform activity during epilepsy surgery, thereby facilitating localisation of the epileptogenic zone. Ramifentanil, a novel ultra-short acting opioid, has an elimination half-life of less than 10 minutes. When compared to baseline ECoG, intravenous bolus dose of ramifentanil significantly increase the frequency of spikes in the epileptogenic zone while suppressing activity in surrounding normal brain during epilepsy surgery. Such observations facilitate localisation of the epileptogenic zone while minimizing resection of the non-epileptogenic eloquent brain. Thus, ramifentanil’s short elimination half-life may facilitate neurologic function testing immediately after epilepsy surgery33 . Intravenous sedative-hypnotic drugs (barbiturates, droperidol, benzodiazepines, propofol, etomidate) produce dose-related depression of the EEG after initial activation, while muscle relaxants have minimal effect on the EEG29 . Activating agents like methohexital may increase cortical spike frequency and distribution27, 28 . Low dose methohexital (0.5 mg/kg) has been used to enhance epileptiform activity during ECoG in surgery to remove seizure foci34 . Etomidate can enhance epileptic activity at low doses (0.1 mg/kg) and may induce seizures in epileptic patients as do barbiturates such as methohexital34 . Propofol produces dose-dependent depression of the EEG similar to barbiturates. It can also enhance interictal activity in some patients, while producing burst-suppression and electrical silence at high doses. Despite its suppressive activity, propofol has become a popular agent for conscious sedation during epilepsy surgery to identify and ablate seizure foci. Because of its rapid metabolism, propofol can be used to induce sleep during portions of the craniotomy. The rapid elimination of this agent allows subsequent awake testing and ECoG29 .

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ECoG IN SURGERY FOR TEMPORAL LOBE EPILEPSY Although intraoperative ECoG has been in clinical use for many decades, the validity of this procedure in guiding resective TLE is still uncertain28 . The standard en bloc anterior temporal lobectomy was pioneered by Falconer et al.35 at Maudsley Hospital, UK, nearly five decades ago. As the custom of the day, this group always performed pre and post resection ECoG, but they never used the spike data to guide their operation. Like Falconer et al.35 , many recent studies reveal that ECoG spikes are not useful for determining the boundaries of epileptogenic anterior temporal resection. However, the practice of using intraoperative ECoG to tailor anterior temporal resections still persists at many centres36 . Schwartz et al.37 performed pre and post resection intraoperative ECoG on 29 consecutive patients with mesial TLE who underwent standard non-tailored resections by one surgeon. All these patients had only temporal interictal spikes and mesial temporal sclerosis (MTS) on preoperative MRI and, the pathological examination of resected tissue confirmed MTS in all patients. After a mean follow up of 25 months, 72% were seizure-free and 28% had some seizure after the first postoperative month. Among the total number of patients, 14 (48%) had active interictal discharges outside the area of planned resection revealed by preresection ECoG. The authors concluded that neither the presence of these spikes nor their mean frequency correlated with seizure outcome. In the above study, 11 (38%) patients had residual spikes after resection and 18 (62%) had new spikes on postresection ECoG. The persistent spikes increased in frequency after resection in all outcome groups and neither of these findings nor the mean spike frequency of residual or new spikes correlated with seizure outcome. In the surgical treatment of TLE, the extent of hippocampal resection varies among surgeons. Most surgeons believe that maximising the extent of hippocampal removal improves outcome with respect to seizures. However, no consensus exists as to how much of hippocampus should be resected38–42 . The most common cause of surgical failure in TLE is thought to be inadequate hippocampal resection43, 44 . Extended or larger hippocampal resection can lead to greater impairment of verbal and non-verbal memory following dominant and non-dominant temporal resections, respectively45–48 . Other investigators have negated the above contention and pointed out that there is no correlation between the extent of hippocampal resection and memory impairment49–51 . Other studies reveal that a lack of pathologically demonstrated hippocampal neuronal loss correlates most closely with postoperative memory decline52–58 .

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Intraoperative hippocampal ECoG can predict how much hippocampus should be resected to achieve maximal seizure-free outcome, thus allowing to spare the functionally important hippocampus38 . McKhann et al.38 in a prospective study comprising 140 consecutive patients who underwent surgery for TLE with pathological diagnosis of either MTS with neuronal loss (MTS group) or mild gliosis without neuronal loss (non-MTS group) concluded that, using an intraoperatively tailored strategy, individuals with a larger hippocampal resection (>2.5 cm) were not more likely to have seizure-free outcomes than patients with smaller resections. Additionally, in both MTS and non-MTS groups, the residual hippocampal (not cortical or parahippocampal) epileptiform activity detected on postresection ECoG correlated with worse seizure outcomes. The above findings provide evidence that intraoperative hippocampal ECoG can predict the required extent of hippocampal resection in surgery for TLE. When all ECoG-confirmed epileptogenic hippocampal tissue is not removed intraoperatively, outcome from medial TLE surgery is significantly worse38 . Thus, extending hippocampal resections posteriorly on the basis of the hippocampal ECoG is the only form of ECoG based tailoring of temporal resection of demonstrable value. In contrast, ECoG serves no practical purpose in anatomically standardised temporal lobectomies. Selective amygdalohippocampectomies are typically followed intraoperatively by a marked increase of interictal spiking unrelated to seizure outcome, and ECoGs may even be potentially misleading in such situations59 . A recent data on ECoG from the University of British Columbia (UBC) reiterated that the differentiation of ECoG features may enhance the utility and contribution of this time honoured method28 . The authors used a simple descriptive method intraoperatively to differentiate the spike discharges of different character. Accordingly, spikes were classified into four categories: (a) independent foci were spikes occurring only at a single or consistent group of electrodes; (b) synchronous foci appear at other sites in concert with identified independent foci; (c) residual spikes are unresected spikes that continue to discharge at the same location with same morphology and behavior during postresection recording; (d) postexcision activation is the new appearance of epileptiform activity with a different location, behavior and morphology than preresection recording19 . Analysing data from 86 TLE surgeries at the UBC, above authors28 concluded that independent foci might be more important for epileptogenesis than synchronous foci. These investigators added that the postexcision activation appeared to be a benign process and, more importantly, the residual spikes unaltered by resection correlated with a greater proportion of seizure recurrence.

A. Kuruvilla & R. Flink

ELECTRICAL STIMULATION AND FUNCTIONAL MAPPING Electrical stimulation during ECoG recordings in patients undergoing epilepsy surgery under local anaesthesia was pioneered by Penfield and Jasper in the early 1950s19 . This novel procedure shed light into the functional anatomy of brain, especially with reference to intraoperative mapping of speech areas and identification of somatosensory/somatomotor cortex. Electrical stimulation is instrumental in the localisation of these regions, thus excluded from surgical removal. An equally important role of electrical stimulation is to reproduce the patient’s habitual warning or aura and partial seizures by local cortical or depth electrode stimulation. If the area that triggers the patient’s habitual attack coincides with the region of active spiking, this could be a convincing demonstration of the epileptogenic zone27 . In a study comprising 30 randomly selected patients with medically refractory TLE at Montreal Neurological Institute, Stefan et al.42 concluded that ECoG provides reliable intraoperative mapping of epileptogenic brain tissue to be resected. All patients underwent intraoperative ECoG as well as electrical stimulation using cortical and acute depth electrodes prior to temporal lobectomy. Special emphasis was placed on the reproduction of patient’s warning by electrical stimulation of mesial temporal lobe structures. A remarkable correlation was found between the symptoms induced by stimulation and the patient’s habitual warning, thus providing additional intraoperative localising evidence regarding the anatomical substrate involved in the genesis of habitual seizure. Another important utility of intraoperative electrical stimulation is to assess the cortical sites involved in memory functions, thereby providing further insight into the mechanisms of memory and also to avoid memory deficits after epilepsy surgery60 .

ECoG IN EXTRATEMPORAL RESECTIONS Extratemporal epilepsy (ETE) constitutes a more heterogenous group and differs in many ways from the better-known temporal lobe epilepsies61 . ETE is classified according to the presumed site of origin of seizure. Frontal, parietal and occipital focal epilepsies exist and various territorial overlaps may occur62, 63 . In ETE, epileptic foci are difficult to localise solely by clinical semiology; however, advanced imaging techniques have aided in the better localisation of epileptogenic area. The commonest causes of ETE are cortical dysgenesis and tumours and, these two aetiological groups constitute 30–70% of all ETEs64 .

Intraoperative electrocorticography in epilepsy surgery

EEG and ECoG are valuable tools for defining the epileptogenic zone beyond the structural lesion. Surgical therapy is guided by the nature of the lesion and the epileptogenic zone61–64 . Levesque et al.65 proposed the term ‘dual pathology’ to highlight the coincidence of extratemporal (ET) lesions with MTS. The coexistence of various types of lesions is described along with MTS64, 66–74 . The commonest lesions coexisting with MTS are cortical dysgenesis, periventricular heterotopia and porencephalic cysts69, 73, 75 . In addition to these, combination of lesions other than MTS can also occur as ‘dual pathology’. Vascular malformations and neoplasms67 or cortical dysgenesis and neoplasms75 are a couple of examples in such a category. It is important to distinguish patients with dual pathology from patients with isolated hippocampal sclerosis because the former usually presents with refractory epilepsy and hence has less favourable outcomes. In a report by Cascino et al.8 , lesionectomy was performed on three patients who, in addition to the lesion, had signs of MTS on MRI. During the outcome analysis, all three had class IV outcome76 while nine patients with single lesion had a good outcome after lesionectomy. This underscores that, in the setting of lesional epilepsy and hippocampal sclerosis, the mesial structures should be resected, if there are no major risks from a neuropsychological standpoint. On the contrary, if mesial structures are to be spared due to neuropsychological reasons, ECoG is useful to allow sparing of functionally important hippocampus. Frontal lobe epilepsy (FLE) is the second largest group among localisation related epilepsies, commonest being TLE77–79 . A large epileptogenic zone is the rule in ETE, particularly FLE. Estimating the boundaries of the surgically relevant epileptogenic zone has been a challenge in ETE. The interictal and ictal EEG patterns of ETE can be often misleading in their localising features. Unusual phenomena such as multifocal epileptiform discharges and secondary bilateral synchrony are seen61 . Absence or paucity of interictal discharges is one of the features of ETE. The interictal spikes noted in the ECoG of patients with FLEs show a continuum from localised to regional, multilobar or even bifrontal or widespread distributions, with no clear relationship to the amount of epileptogenic tissue resected for successful seizure control62 . Interictal spikes detected in ECoG extended outside subsequently resected tissue in about 75% of patients who underwent frontal lobectomy and in 91% of patients treated by corticectomies in different locations. On the other hand, similar ECoG finding was observed in 40% of individuals who underwent temporal lobectomies or amygdalohippocampectomies80, 81 . Despite the aforementioned difficulties in localisation of the boundaries of epileptogenic zone, ECoG

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can be a valuable tool during surgery of malformations of cortical development (MCD). In a widely quoted and elaborate study comprising 34 patients with intractable partial epilepsy associated with cortical dysplasia (CD), Palmini et al.82 , described continuous or frequent rhythmic epileptogenic discharges recorded directly from cortical dysplastic lesions during intraoperative ECoG. Three distinctive patterns were described by these authors: (a) repetitive electrographic seizures; (b) repetitive bursting discharges; and (c) continuous or quasicontinuous rhythmic spiking. One of these patterns was present in 67% of patients with intractable partial epilepsy associated with CD and in only 1 of 40 (2.5%) patients with intractable partial epilepsy associated with other types of structural lesions. In addition, 75% of patients who underwent excision of cortical tissue displaying ictal or continuous epileptogenic discharges showed a favourable outcome. On the contrary, uniformly poor outcome was observed in those patients in whom areas containing the ictal or continuous epileptogenic discharges remained in situ. These authors concluded that intraoperative ECoG identification of this highly and intrinsically epileptogenic dysplastic cortical tissue is crucial to decide the extent of excision for best seizure control82 . The removal of ECoG identified dispensable epileptogenic cortex surrounding a highly epileptogenic developmental malformation or neoplastic or cicatrical lesion in any location yields better control of epilepsy than lesionectomy alone83 .

ECoG IN MULTIPLE SUBPIAL TRANSECTIONS The technique of multiple subpial transections (MST) was introduced by Morrell et al.84 to surgically treat intractable epilepsy with seizure foci in primary sensorimotor or language areas. Because of the columnar organization of the cerebral cortex, vertical transections theoretically disrupt only horizontally oriented axons while preserving the vertically oriented architecture and cortical function. Orbach et al.85 evaluated the long-term outcome after MST in a large cohort of 54 patients with medically refractory epilepsy. After subdural grid and strip placement and occasionally depth electrodes, these patients underwent cortical mapping to identify primary sensorimotor or language cortex. If a seizure focus was found to be overlying eloquent cortex, MSTs were made. The surgical sites were classified as being restricted to the temporal lobe, restricted to extratemporal lobe/s, or combined temporal and extratemporal. The patients whose surgery was restricted to the temporal lobe were markedly less likely to have a poor outcome (Engel scale: grade IV)76 than those whose surgery included extratemporal sites (7%

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for temporal surgery vs. 20 and 26% for extratemporal and combined surgery, respectively). Approximately 82% of the patients achieved long-term seizure outcome within 2 years after surgery, but the remaining 18% had significant worsening of seizure control between 2 and 5 years postoperatively. The above study indicates that the utility of ECoG in MST is invaluable.

CONCLUSIONS The utility of intraoperative ECoG during anatomically standardised temporal resections is limited. ECoG may be needed to guide the resection by mapping eloquent cortex or to determine the extent of epileptogenic area not visualised on neuroimaging. Residual spikes on ECoG, unaltered by the resection, correlate with a poor seizure control. Intraoperative hippocampal ECoG can predict the required extent of hippocampal resection to maximize seizure-free outcome. This can also help to minimize the postoperative memory decline, by sparing of possibly functionally important hippocampus. Thus, ECoG plays a major role in tailored temporal lobectomies. The clues provided by the intraoperative ECoG during removal of MCD, like CDs, is invaluable. We would like to conclude with the following quotation from Quesney and Niedermeyer27 : “Electrocorticography holds a firm place as an explorative method in the mapping of the interictal epileptic activity during seizure surgery, although interpretation of findings may be difficult. Electrocorticography is not merely an enhancement of the academic stature of seizure surgery, but a truly helpful method in assessing the extent of epileptic activity”.

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