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Epileptic Disorders

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Electrocorticography Volume 2, numéro 1, Mars 2000

Introduction

Electrocorticography (ECOG) is a neurophysiological technique used to record cortical potentials from the exposed brain in the operating room. It has been in common use for over four decades in the surgical treatment of people with medically refractory epilepsy [1, 2]. This paper revisits the role of ECOG. The main reason for recording an ECOG has been to confirm and outline the actual site and extent of the epileptogenic process prior to resection. After the resection has been completed, ECOG has been used to determine if all the potentially epileptogenic tissue has been removed. Both of these roles have been questioned.

The technique

The ECOG records the same type of cerebral potentials as the scalp electroencephalogram, except that the dispersion and attenuation of the potential by the scalp and skull is not present. In theory, this should allow for better localization of the origin of the epileptogenic tissue causing the patient's habitual seizures. Because of the short recording time available for ECOG and the limitations of electrode placement posed by the surgical exposure, the possibility of recording ictal events is rare. The ECOG relies on the presence of interictal epileptiform discharges for the identification of the irritative/epileptic zone. Careful preoperative planning is required. The clinical history, electroencephalographic studies (both ictal and interictal), and imaging studies need to be carefully reviewed to define the area of resection and exposure needed for adequate ECOG recording prior to surgery.

The actual technique of recording an ECOG has changed little since its introduction. Throughout the time of the recording, continuous close communication between the clinical neurophysiologist and the neurosurgeon is required. The clinical neurophysiologist must be able to read and interpret the recording as it is being done. Any modifications of electrode position and montages must be done at that time. This requires that the recording apparatus be either in the operating room or in the operating room gallery with a two way communication system in place.

Standard sixteen channel EEG equipment can give very adequate ECOG recordings. As ECOG records directly from the brain, modifications in recording sensitivities, filters, and time constants will be required. Electrodes need to be able to sit on the leptomeninges and move with the pulsations of the brain. Either flexible ball electrodes mounted on a fixed horseshoe frame or a series of electrodes implanted in a soft flexible silastic grid can be used. The advantage of the ball electrodes over strip electrodes is that they can be sterilized and reused, cutting down costs. Due to the lack of adequate sterilization techniques, silastic implanted electrode should be used only once.

For accurate localization of the epileptogenic area, the electrodes need to be placed an equal distance apart. Montages should consist of a minimum of four electrodes in a straight chain. The use of montages using angulated electrode placement should be avoided as this can lead to false localization. If simultaneous recording from multiple chains of electrodes is planned, the electrodes must be of equal distance in both vertical and horizontal planes. This will allow for bipolar recordings to be done, as well as, referential recordings. When single chains of electrodes are used only, both referential and bipolar recordings should be done simultaneously. Various referential electrode placements can be used (such as mastoid, cervical region, and bone flap).

To record from the deeper structures (such as the mesial temporal regions) either four contact depth electrode can be inserted through the brain to reach the deeper structure or a flexible silastic four-electrode grid can be inserted under the temporal/frontal region. The placement of a chain of electrodes over the cortical surface at the same time as the recording allows for a better understanding of the propagation of the abnormal cerebral potentials.

Total recording time is about thirty minutes, although longer times are occasionally necessary. Methohexital and alfentanil have been reported to "activate the epileptic zone" [3, 4]. These techniques should be done only after adequate standard recordings of the exposed brain have been done. Careful interpretation of the areas of "activation" must be made as the potential to "activate" regions outside the true irritative/epileptic zones has been reported.

In adults, the ECOG recording is usually done with the patient in the awake state; however, in children this is not often possible. The anaesthetic agents used for the operative procedure can have significant effects on the ECOG. Sufentanil, fentanyl, alfentanil, propofil methohexital have been reported to produce epileptiform changes on ECOG, whereas halothane, barbituates and benzodiazepines may suppress the epileptic activity [3-7]. Both nitrous oxide and isoflurane have been reported to affect the ECOG, but more recent reports have suggested that this is not the case when low concentrations are used [8, 9]. For these reasons, it is recommended that in patients be maintained on nitrous oxide, isoflurane and non-depolarizing muscle relaxants be used during ECOG recording.

During the ECOG, electrical stimulation of the cortex has been used to localize the area of epileptic seizure onset, as well as to map the area of cortex responsible for motor, sensory and language functions. While the ECOG is being recorded, an electrical stimulus is delivered between two ball electrodes or between adjacent silastic enclosed electrodes. This stimulus consists of a 0.5 to 2 nsec diphasic pulse applied at 50-60 Hz over 1 to 5 seconds with an intensity of 0.5 to 2.0 mA and a voltage of 1 to 15 V. The site of the patient's habitual seizure aura is noted, as well as the regions of maximal after-discharges. These discharges are in the form of high frequency stereotypic paroxysms such as spikes, rhythmical sharp waves or spike wave sequences. The discharge usually ends abruptly. It may be localized or spread to multiple electrode sites.

Validity

In order to examine the validity of ECOG, a Medline literature search from 1985 to the present was performed using the key words electrocorticography, ECOG, intra-operative recording, and epilepsy. As complete coverage of the medical literature for a given topic using Medline is often incomplete, a search of the references quoted in each of the articles was made. The data were reviewed by type of resection (i.e. temporal, extra-temporal or lesional) and the degree of evidence in support or against the use of ECOG for each of the previously stated reasons.

Nonlesional temporal lobe resections

According to Rasmussen [10], the removal of the "epileptogenic zone" (the anatomical site of seizure onset), as well as the surrounding tissue which might potentially be recruited into the critical mass of tissue, is required for a successful surgical outcome. ECOG has been reported to provide useful information for the localization of this area at the time of surgery [11-15].

Thirty-two papers on this topic were located by our search technique The review of these papers revealed little evidence that actually established the true value of the procedure in this role. All that have been published have been in the form of retrospective case studies or case series without a proper control group. Some investigators have questioned the role of this procedure [16].

Epileptiform discharges were reported to have been recorded from the temporal lobe in all of the papers located by our search mechanism. These waveforms were similar to those recorded from the scalp electroencephalogram, consisting of isolated spikes, brief bursts of spikes or runs of sharp waves . They were often multifocal with a wide distribution over the exposed temporal cortex. More commonly, the epileptiform discharges were reported to have been recorded from the hippocampal structures and inferiomesial surfaces of the temporal tip. To a much lesser extent , they were recorded from the lateral temporal cortices and more so from the posterior temporal cortices [15, 17-21]. Propagation of the epileptiform discharge was commonly seen from the hippocampus, to and from the subtemporal cortex [19, 21].

Parent-Raymond et al. [22] have suggested that in addition to these epileptiform discharges, delta wave activity might also give useful information as to the location of the epileptiform tissue in patients in whom spikes were not found on ECOG. With the help of spectral analysis of the ECOG data, the maximum area of delta frequency activity was determined in forty patients. In twenty-two patients, this area coincided with the region of maximum spike activity. This association was statistically more frequent than would have been predicted. The authors do suggest caution when using this method in individual cases.

In theory, ECOG recordings could be expected to provide information missed on a scalp electroencephalogram especially activity from the mesial surface of the temporal lobe. Few studies have actually addressed this question. Devinsky et al. [23] in a report of a retrospective review of thirty-three patients with medically refractory epilepsy who underwent temporal lobectomy, found eight patients in whom the ECOG recorded epileptiform discharges not previously found by scalp electroencephalograms even with the use of sphenoidal electrodes. On the other hand, Engel et al. [24] noted that no additional information was obtained from the ECOG compared to the preoperative scalp electroencephalogram.

ECOG seldom records ictal events, but rather interictal epileptiform activity. The relationship between the epileptic zone (area of origin of the epileptic seizure) and the irritative zone (area of maximum interictal epileptiform discharge) is not completely understood. In particular, the degree to which the two zones overlap, especially on the ECOG recording is unclear. It has been hypothesized that the more frequent these discharges are within an area, the more likely it is that this area lies within the epileptic zone [21]. Alarcon et al. [21] found that the removal of this area resulted in a significantly better chance of a good surgical outcome, even if areas of less frequent discharging were left untouched. If the area of maximal discharging was not completely resected, the surgical outcome was more likely to be poor. An earlier study by Tran et al. [25] had found no association between surgical outcome and frequency of epileptiform discharges. This study used the visual analysis of the ECOG record by the electroencephalographer, whereas Alarcon had used a computerized spike detection program.

Electrical stimulation of the cortex at the time of ECOG has been used in further localization of the epileptic zone [1, 13]. The site of reproduction of the habitual aura of the patient by electrical cortical simulation has been reported by some investigators to have strong correlation with the epileptic zone [26-28]. This was particularly the case when the area from which the responses were elicited also coincided with the region exhibiting the greatest epileptic discharge. Gloor [13] commented that this was less likely to be the case if an afterdischarge occurred, especially it if spreads to distant areas. In this situation the clinical symptomatology may not be related to this area of stimuli, but reflect a distant area to which the discharge had spread.

After-discharges arising from electrical cortical stimulation are of questionable value in the localization of the epilep-

tic zone. It is not uncommon for after discharge to issue from regions of the brain from which no epileptiform abnormalities had been recorded on ECOG [1, 13, 29]. The thresholds for after discharge has been reported to show considerable variability [16].

New epileptiform discharges can appear after the excision; when along the margin of the resection, they may be representing a cortical disturbance caused by the manipulation of the brain at the time of surgery and may not have prognostic significance. Discharges some distance from the resection margin may be more predictive of a poor surgical outcome. These differences may explain the difference in the reported use of postresection ECOG in predicting surgical outcome. This cannot be confirmed from the reported studies as the area of residual discharge in relation to the resection margin was often unclear.

The role of the ECOG in determining the surgical outcome is unclear. McBride et al. [30] and Engel et al. [24] did not find an association between the site of dominant intraoperative ECOG epileptiform discharge and the surgical outcome. Correlation between the location of discharge and underlying pathology was also not found [24].

Bengzon et al. [31] noted a significant difference in the surgical outcome between patients with residual spikes compared to spike-free postresection recordings. Thirty-six percent of patients who were seizure-free postsurgery had residual spike; whereas 75% of patients who were not seizure-free had residual spikes on post-resection ECOG. These findings were similar to those reported by Jasper [1], Foil et al. [32], Wyllie et al. [33], Drake et al. [34], Tanaka et al. [35] and McBride et al. [30].

Other investigators have not been able to confirm the relationship between the degree of epileptiform discharges seen on the post-resection ECOG and the outcome [16, 36-39]. This was especially the case in patients in whom selective amygdalo-hippocampectomy was done. In this situation, new epileptiform discharges were often recorded from the temporal cortex after completion of the procedure. These discharges were found to have no predictive value [40, 41].

A possible explanation for the lack of consensus as to the role of the ECOG in the prediction of surgical outcome may lie in the surgical procedure itself. Most centres that have reported the use of ECOG-performed standardized temporal lobe resections. Only a few centres actually tailored the resection according to ECOG findings [42].

Nonlesional extra-temporal resections

Evidence in support of the use of ECOG in extra-temporal resections is scant (six papers). Most of the literature pertaining to this topic is related to lesional cases, and will be covered in that section. Quesney et al. [43-45] noted that in patients whose seizures originated in the frontal lobes, there was no clear relationship between the amount of epileptogenic tissue removed and a successful surgical outcome. The reason for this may lie in the anatomical and functional peculiarities of this region, which permits the epileptiform discharge to vary in location from a specific region, to multilobular or even bifrontal. Similar findings have been noted in ECOG recordings of patients with seizures arising from the centroparietal region and occipital areas [43, 44].

For patients with non-lesional, medically refractory extra-temporal epilepsy, the use of subdural grid electrodes may prove to be the answer to this question. As this procedure allows ictal events to be recorded, there is a greater possibility that the epileptic zone will be identified. Another approach may involve the use of other imaging techniques, for example positron emission tomography [46].

Lesional, temporal and extratemporal resections

The use of ECOG in patients in whom structural lesions have been identified on imaging studies remains controversial. Traditional wisdom based on the Montreal Neurological Institute experience holds that optimum seizure control is achieved when the lesion is removed with the surrounding epileptogenic cortex as determined by ECOG [45-48]. This point of view has been supported by Pilcher et al. [49] who found that eleven out of twelve patients who underwent surgery for ganglioglioma, were seizure-free at 3.1 years post-surgery compared with a literature control of twenty-one out of thirty-nine (54%) patients with ganglioglioma in whom only the lesion was resected. They noted that the epileptogenic zone was topographically distinct from the region of the tumour-involved brain. It usually encompassed a large surface area. Non-epileptiform high-amplitude slow waves were recorded on ECOG predominantly in tumour-involved cortex, while epileptiform spike discharges were recorded over normal-appearing cortex. They felt that these discharges represented the epileptogenic zone. The removal of this area increased the chance of a better outcome.

Berger et al. [50] reported a series of children and adults with intractable epilepsy, associated with low grade tumour. Forty-one out of forty-five of these patients (91%) became seizure-free. They did not advocate the use of ECOG in patients with lesion and occasional or new onset of seizures, but felt it should be used in individuals with medically refractory epilepsy associated with low grade tumour. This was particularly the case in children, where there was a significantly better chance of seizure control. Cohen et al. [51] reported similar findings in 98 patients with cavernous hemangioma. Gonzalez et al. [52] also reported greater control of seizures when the tumour was resected with ECOG-guided removal of the seizure focus. Drake et al. [34] reported the results of a series of children with structural lesions of the temporal lobe using ECOG guidance. They again emphasized the concept that seizure activity often originated from the brain tissue adjacent to the tumour.

Others have not felt that ECOG guidance is necessary in this group of patients. Resections have been restricted to the tumour margins as delineated on imaging studies and at the time of surgery [53-55]. The literature states that if the lesion has not been completely removed, seizures will continue despite the removal of the "epileptogenic zone" [56, 57].

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 have not been prospectively done. Tran et al. [58] attempted a controlled retrospective series review in which patients with structural lesions present underwent resection of the lesion to normal tissue margins. ECOG was recorded pre- and post-resection, but not used to determine the amount of surgical resection. Patient outcome was based upon seizure-free state. ECOGs were analysed for spike distribution and spike discharge rate. Spikes were found to be over the tumour bed as well as in the surrounding tissues. Spike distribution in the pre-resection ECOG did not correlate with outcome. On post-resection ECOG, spikes were noted along the edge of the resection as well as extra-marginally in equal amounts between patients who became 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. Like temporal cortical resections, the presence of post-resection spikes does not appear to correlate with outcome. A case may be made for the use of ECOG in patients with dual pathology to assess the degree of epileptogenesis in the distant site [59]. Clarke et al. [60] have suggested that even in this case, the lesion must be removed if good seizure control is to be obtained.

Cortical dysplastic lesions are often associated with severe, partial epilepsies of childhood and can prove refractory to medical management leading to the need for surgical resection. Palmini et al. [61] have reported long runs of epileptiform discharges on ECOG consisting of repetitive electrographic seizures, repetitive bursting discharges or continuous rhythmic spiking. They felt that these discharges were often co-localized with the magnetic resonance imaging-defined lesion. The completeness of resection of the epileptiform activity on ECOC correlated with the surgical outcome. Wennberg et al. [62] noted similar findings in lesion-related frontal lobe resection. This would suggest a role for ECOG in these cases to determine the location and extent of resection at the time of surgery. Holmes et al. [63] caution that neocortical lesions on magnetic resonance imaging (MRI) do not necessarily indicate the site of ictal onset of partial epilepsy. They reported on twenty adult patients with medically refractory epilepsy where the MRI showed a focal lesion. Electroencephalogram suggested that ictal onsets were in different areas. Surgery was based on electrographic data. Fifty percent of patients were seizure free at follow up. Thirty-five percent had a greater than 75% reduction in their seizures.

 

CONCLUSION

For several decades, ECOG recordings have been routinely used in the surgical management of patients with medically refractory epilepsy. Using this technique, confirmation of epileptiform activity on pre-operative scalp electroencephalogram has usually been demonstrated at the time of surgery. It also allows for direct exploration and recording of the mesial surfaces of the cerebral cortex. With this information, tailored resections of epileptogenic tissue can be performed. Whether tailored resections have better outcome than standard resections of the temporal lobe, remains unclear. In order to answer this question, carefully designed, controlled prospective study will need to be done, controlling for variables such as the type of resection, location and degree of epileptiform disturbance on ECOG, and outcome measures such as seizure control and psycho-social status. It is quite possible that the results of ECOG-guided and standard temporal resection will be very similar, when the size and extent of the surgical resection will turn out to be the same in both groups.

The role of ECOG in extratemporal and lesional resection is different in the case of temporal resection. The ECOG appears to be beneficial in lesional resections in patients with refractory epilepsy. Its use in new onset cases is less clear. Also its use in patients with dual pathology remains unclear. Controlled prospective studies again would be helpful.

Extratemporal resections need to be well planned prior to surgery. Imaging studies such as MRI and PET have proven helpful in localizing the site of epileptogenicity. The degree of electrographic spread of epileptiform discharges suggests that chronic intracranial recordings may be needed to provide more accurate and complete information about the seizure origin than intraoperative ECOG.