Focal epilepsy is a common clinical manifestation of structural brain abnormalities, such as focal cortical dysplasias, low-grade glioneuronal tumors, poststroke, and posttraumatic atrophy .
Intraoperative electrocorticography (iopECoG) was first introduced in the 1930s by Penfield and Jasper . This popular diagnostic tool is used in a wide range of epilepsy surgeries to improve localization of the epileptogenic foci prior to resection, to tailor the resection itself, and to verify the absence of epileptic activity following the resection. However, the value of iopECoG remains controversial, especially in an era where preoperative localization techniques have significantly improved the ability to localize the epileptogenic zone (EZ), and extraoperative ECoG has become more available. In addition, postoperative seizure control may vary, depending on the timing of surgery, preoperative evaluation methods, location, underlying pathological causes, detection method, and anesthesia. Therefore the actual contribution of iopECoG is difficult to evaluate and almost impossible to isolate. In this chapter, we attempt to present the advantages and disadvantages of iopECoG, based on characteristics of epileptiform activity, type of lesion, and location.
Advantages of intraoperative electrocorticography
Intraoperative electrocorticography in resection of tissue with epileptiform activity
Several studies compare seizure outcomes following iopECoG versus other methods. A comparison of resection outcomes amongst 103 patients (lesional and nonlesional MRI), when comparing iopECoG to invasive extraoperative monitoring, showed that the best outcomes were obtained with resection of both the seizure-onset zone and iopECoG abnormalities (including seizures and spike locations) (22/33 good outcome, 67%, p =.008). There was a significantly better outcome in children with complete resection of iopECoG-identified spike populations (14/26, 62% good outcome) compared to when none were resected (4/14, 29%, p =.043) .
Another retrospective cohort study quantified and characterized iopECoG in 34 children, and demonstrated a higher frequency of epileptiform discharges (ED) and high-frequency oscillations (ripples, 80–250 Hz, fast ripples, 250–500 Hz) rates in children with malformation cortical dysplasia (MCD) compared with non-MCD. In patients where residual higher frequencies of EDs and ripple rates were seen, there was a lower seizure freedom rate postoperatively .
Intraoperative electrocorticography in low-grade epilepsy associated neuroepithelial tumors
Lesional epilepsy, especially that caused by low-grade tumors, which have a prolonged and chronic course, is associated with biochemical and morphological alternations of the surrounding tissue. These changes may cause hyperexcitability of the area in proximity to the lesion, leading to refractory epilepsy in 50% of the cases . It is thought that epileptogenicity is related to tissues surrounding the lesion rather than the lesion itself . Additionally, in over 50% of children with glioneuronal tumors, a concomittant focal cortical dysplasia is also present. Removal of the epileptogenic cortex in addition to the lesion was superior to lesionectomy only, with seizure freedom rates of 91% versus 54% respectively. When utilizing iopECoG in cases of intractable epilepsy associated with low-grade gliomas, Berger et al. reported 91% postoperative seizure control, of whom 53% (24/45) were seizure-free with no antiseizure medications (54 months follow-up) . When analyzing the results focusing on the pediatric age group (under 18 years of age), 85% of patients were seizure-free with no medications.
Further support for the use of iopECoG was received by Yao et al., who compared the seizure outcome of 108 patients with low-grade glial tumors who underwent either gross total resection, or gross total resection including epilepsy areas guided by iopECoG . A statistically significant difference was found. In the iopECoG-guided group, 74% of patients were completely seizure-free (Engel Class I) and 96% were Engel Class I or II, while only 39% were seizure freedom and 78% Engel class I or II were in the gross total resection (GTR)-only group ( p <.05). Furthermore, Lombardi et al. examined temporal lobe low-grade gliomas in the absence of MRI features of hippocampal sclerosis. They showed that only 50% achieved an Engel I outcome (4/8), while the other half showed no worthwhile improvement . On this basis, they recommended iopECoG specifically in temporal gliomas with no signs of hippocampal involvement on imaging.
Furthermore, the association between use of iopECoG and improved seizure control was reported in a study of 157 cases of lesional epilepsy . In this study, out of 73% of the patients who had a good clinical outcome, 80% showed reductions in EDs following iopECoG, with greatest benefit for lesions localized within the temporal lobe. In the study, with 3.1 years follow-up, a positive predictive value of 89.9% was reported (95%CI, 83.1%–94.3%). A recent meta-analysis was conducted of iopECoG-guided resections for low-grade tumor-associated epilepsy. A total of 31 studies encompassing 1115 patients were included and indeed identified a significant benefit of iopECoG compared to lesionectomy alone .
Intraoperative electrocorticography in extratemporal epilepsy
While temporal lobe epilepsy is the most frequent location of focal epilepsy in adults, extratemporal resections are more common in the pediatric age group, with lower rates of seizure freedom. In a metaanalysis including 1259 pediatric patients undergoing resection of extratemporal foci, seizure freedom (Engel Class I outcome) was achieved in 56% when iopECoG was used, compared to 63% when iopECoG was not used; however, the indications for iopECoGs use were not stated, and may represent more complex cases . Amongst children following iopECoG-guided single-stage extratemporal surgical resection, 59% were seizure-free; to note that parietal and occipital resections had a seizure-free liklihood of 100% .
Intraoperative electrocorticography in temporal epilepsy
In 1991 Stefan et al. confirmed the reliability of ECoG for mapping epileptogenic tissue in 30 cases of temporal epilepsy . Using depth electrodes, they were able to elicit a typical aura in 43% of the patients, particularly when stimulation was delivered to the amygdaloid region.
In an attempt to localize and map the electrical network involved in refractory temporal epilepsy (onset and propagation) and tailor the resection, postresection computer analysis of iopECoG was performed in 42 cases . No association was found between the location of leading regions, greatest amplitude or incidence, and seizure outcome. However, not removing the leading regions was strongly and significantly associated with poor seizure outcomes. These results emphasize the potential ability of intraoperative recording to highlight the areas involved in generating seizures and spare unnecessary resection of regions that represent secondary involvement.
Similar to the results previously mentioned in extratemporal epilepsy, Chen et al. describe the role of preresection iopECoG in 22 cases of unilateral hippocampal sclerosis . Seizure freedom was reported in 82% of patients where preresection spikes were restricted to the mesiobasal region, compared to 55% with other patients (1 year follow-up).
The most challenging cases in epilepsy surgery are nonlesional or MRI-negative cases. The preoperative investigation encompasses different imaging modalities, attempting to obtain the most accurate extraoperative localization of seizure-onset zone and its function. Extraoperative ECoG (eopECoG) is one of the important tools for this purpose. With increasing availability and the technological advances in eopECoG, the utility of iopECoG became even more questionable. However, both Burkholder and Grewal showed that complete resection of interictal discharges recorded during iopECoG lead to statistically significant improved seizure outcome . A large meta-analysis of 18 studies showed that there was no benefit of iopECoG at the study level, but with on analysis of individual participant data of 7 studies (231 patients), iopECoG was associated with better seizure outcomes. and especially for focal cortical dysplasias .
Disadvantages of intraoperative electrocorticography
Intraoperative EcoG has several limitations. First, the added value of its use is debatable. Second, there is the risk of adding neurological morbidity while “chasing” the abnormal pathology. Other limitations include a higher cost (due to special equipment and longer operating room time), the availability of trained personnel, and lengthening of procedure time .
Does intraoperative electrocorticography truly improve epilepsy outcome?
As summarized above, a body of literature does support the added value of iopECoG. However, when reviewing the supportive data regarding iopECoG, it is mainly based on series from at least 20–30 years ago. Over recent years, the presurgical evaluation, including noninvasive as well as invasive (SEEG), has enhanced the understanding and definition of the epileptogenic network before the actual resection. Thus the added value of iopECoG has diminished .
Most studies have found that for both recent-onset and prolonged lesional epilepsy, GTR of the lesion is the treatment of choice, with no additional resection, and therefore iopECoG has limited value. Even in the presence of associated dysplastic tissue (common in glioneuronal tumors), there is no need for preventive resection, since for the vast majority of patients, a GTR of the tumor will lead to seizure freedom. This is also true for chronic epilepsy, although the cure rates are less than for recent-onset epilepsy. Chronic drug-resistant epilepsy differs from recent-onset epilepsy, as there may not be establishment of secondary epileptogenic networks. For the vast majority of recent-onset epilepsies related to tumors, a GTR of the tumor will lead to good seizure outcomes.
Previous studies of iopECoG have often included mixed populations, such as both children and adults. Different pathologies, locations, and epilepsy durations were also often clustered together, such as temporal and extratemporal, or glioneuronal tumors together with others. Disadvantages recent metaanalysis by Goel et al., cited above showed that there are discrepancies in the value of iopECoG depending on the pathologies ( Fig. 8.1 ).
