Application of intracranial electrodes for long-range video EEG monitoring

  To investigate the application of intracranial electrode long-range recording in temporal lobe epilepsy localization and lateralization and to evaluate its clinical value. METHODS: Sixty patients with temporal lobe epilepsy localized by intracranial electrodes, with electrode types of subdural strips, fenestrations and deep electrodes, and surgical procedures including cranial drilling electrode implantation, stereotactic deep electrode implantation and bone flap craniotomy electrode implantation. Results: 34 frontal-temporal cortex electrodes were implanted, 7 frontal-frontal-temporal-occipital junction electrodes were implanted, 7 dual temporal cortex electrodes were implanted, 7 deep electrodes combined with temporal cortex electrodes were implanted, 3 anterior temporal-occipital junction electrodes were implanted, and 2 strip electrodes combined with fenestrated electrodes were implanted. The surgical procedures included anterior temporal lobectomy in 50 cases, combined frontal lobe epileptogenic foci resection in 7 cases, combined corpus callosotomy in 1 case, and posterior temporal-occipital neocortical foci resection combined with hippocampal amygdala resection in 2 cases. Conclusion: Intracranial electrode long-range recording is an effective examination method and an important localization tool that can be applied to temporal lobe epilepsy that is difficult to be localized and lateralized by noninvasive assessment methods.  Temporal lobe epilepsy (TLE) is one of the more common types of epilepsy, and its surgical effectiveness has been recognized. The determination of the location and laterality of the epileptogenic focus is a prerequisite and key to surgical treatment. The intracranial electrode long-range video electroencephalography (IVEEG) is an important preoperative assessment method in epilepsy surgery and has an irreplaceable value in the localization and lateralization of epileptogenic foci [1-3].  Subjects and methods 1. General data: From January 2006 to October 2010, 156 patients with temporal lobe epilepsy or multifocal epilepsy but predominantly temporal lobe epilepsy (subject to surgery) were identified by IVEEG at Beijing Tiantan Hospital. Among them, 35 were male and 25 were female; age ranged from 9 to 50 years, with a mean of (24.5±9.7) years. The medical history ranged from 1 to 40 years, with a mean of (13.1±8.6) years. Intracranial electrodes were placed on the left side in 13 cases, on the right side in 16 cases, and bilaterally in 31 cases. The seizure forms included simple partial seizures, complex partial seizures, complex partial seizures secondary to generalized seizures, generalized seizures, or multiple seizure forms simultaneously. All patients had one to two or more long-range scalp video electroencephalography (sVEEG) examinations before surgery. 24 patients had no MRI abnormalities and 36 patients had positive MRI findings, including temporal horn enlargement, hippocampal sclerosis, cortical atrophy, softening, arachnoid cyst, and choroidal fissure cyst. 20 patients had positron emission tomography (PET) examinations, 13 patients had magnetoencephalography (MEG) examinations Some patients underwent magnetic resonance spectroscopy (MRS) and other examinations.  Inclusion criteria [3-4]: IVEEG was used for patients with conflicting data on seizure symptoms, MRI and sVEEG and other non-invasive examinations, and difficult to localize and lateralize the epileptogenic focus. (4) Patients with complex seizure forms, not excluding multifocal epilepsy, who are difficult to localize and fix the side.  3. intracranial electrode selection and implantation method [1,3,5]: firstly, patients were evaluated according to their seizure form and the results of noninvasive examinations such as sVEEG, MRI, PET, MEG, etc. to initially determine the range of epileptogenic foci, select the intracranial electrode implantation site and implantation type according to the evaluation results, and design the surgical incision. (1) Selecting cortical electrode implantation for those who are difficult to locate (Figure 1): depending on the implantation site, skull drilling or bone flap craniotomy is selected to implant subdural strip electrodes or/and fenestrated electrodes. For example, frontal-temporal cortical electrode implantation, frontal-frontal-temporal-occipital junction cortical electrode implantation, etc.; (2) for those who are difficult to locate laterally, bilateral stereotactic deep electrode implantation is chosen (Figure 2): a stereotactic head frame (Leksell) is installed under local anesthesia, MRI is scanned, and the images are transmitted to the surgical planning system. Bilateral temporal cortex electrodes are placed at the same time as the deep electrode implantation. Alternatively, bilateral temporal cortex electrodes may be implanted, but they should be placed bilaterally and symmetrically, and the anterior contacts of the electrodes should touch the temporal floor.  4. Postoperative EEG monitoring and surgery: All patients returned to the ward after surgery for long-range VEEG monitoring, and the EMS digital video EEG monitoring system was used to record seizure and interictal EEG and to determine whether the recorded seizure form was consistent with the patient’s plain seizures.  Results 1. Type of intracranial electrodes: In 60 patients, frontal-temporal cortex electrode implantation was performed in 34 cases (21 unilateral and 13 bilateral), frontal-frontal-temporal-occipital junction electrode implantation in 7 cases (5 unilateral and 2 bilateral), deep electrode combined with temporal cortex electrode implantation in 7 cases, and double temporal cortex electrode implantation in 7 cases (including combined single frontal electrode implantation in 3 cases and combined unilateral temporal-occipital junction electrode implantation in 1 case). 3 cases of anterior temporal-occipital junction electrode implantation (1 unilateral case, 2 bilateral cases), and 2 cases of combined strip electrode implantation fenestrated electrode implantation.   For patients with extensive spikes on intraoperative EEG monitoring, microcurrent thermal cautery could be performed at the same time if necessary.  Complications: 1 case of postoperative decompression with bone flap due to cerebral edema and 1 case of intracranial hemorrhage with hematoma removal + decompression with bone flap were performed in this group.  4. Pathological examination: 2 of 60 patients were nodular cell glioma, 1 case had been treated with gamma knife showing radiation necrosis, and the pathology of the remaining 57 patients was consistent with the pathological manifestation of medial temporal lobe epilepsy.  Discussion TLE is epilepsy originating from the temporal lobe and characterized by simple partial seizures, complex partial seizures, or secondary generalized seizures, and surgery is an important treatment for TLE. Typical TLE seizures are preceded by aura such as rising abdominal sensation, déjà vu, or manifestations of fear and phantom smells, followed by slow movement, gaze, oropharyngeal automatisms, ipsilateral limb automatisms (such as groping), etc. About half of the patients have secondary generalized tonic-clonic seizures, with drowsiness and disorientation in the later stages of seizures. MRI shows hippocampal atrophy and temporal horn enlargement, PET shows interictal hypometabolism, and MRS shows reduced signal of ipsilateral neuronal marker N-hexylaspartate (NAA). However, if the above manifestations are atypical, the EEG cannot be localized due to the wide range of spikes, or the manifestations of other parts of epilepsy are combined, or there are multiple seizure forms, it is difficult to localize them by non-invasive examination methods alone, and then invasive examination methods, i.e. intracranial electrode implantation, are required.  Because sVEEG is affected by the conduction medium of the skull and scalp, it can only provide the approximate extent of epileptic discharges, whereas IVEEG can accurately and clearly record the EEG signal at the onset of seizures with almost no interference [6], therefore, IVEEG is an important method for determining the origin of epilepsy and can significantly improve the accuracy of localization and lateralization of epileptogenic foci, which has important Due to the different clinical seizure symptoms, imaging and electrophysiological findings in different patients, before applying IVEEG, a comprehensive assessment should be made, and the type of intracranial electrodes and implantation method should be individualized according to different situations.  First, for epilepsy that cannot be localized, especially multifocal epilepsy, electrode type and implantation site should be selected according to the results of phase I evaluation. When the patient’s seizures showed symptoms of complex partial seizures, no abnormality was seen in the temporal lobe of MRI, and the EEG showed unilateral frontal and temporal spike-wave discharges, it was difficult to determine the frontal or temporal origin by noninvasive assessment methods, unilateral frontal-temporal electrode implantation was selected, in 21 cases in this group, by skull drilling and placing cortical strip electrodes in the frontal lobe direction and anterior temporal lobe direction, respectively; for bilateral frontal-temporal spike-wave discharges, bilateral frontal -temporal electrode implantation, 13 cases in this group. Similarly, if the EEG showed temporal and temporo-occipital spike discharges, unilateral anterior temporal-temporo-occipital junction electrodes were selected for implantation (1 case in this group), and for bilateral anterior temporal-temporo-occipital junction discharges, bilateral electrodes were selected for implantation (2 cases in this group). If the spike wave range was extensive and the EEG showed frontal, temporal and temporo-occipital junction discharge on one side, unilateral frontal-frontal-temporo-occipital junction electrode implantation was selected (5 cases in this group), and bilateral electrode implantation was selected for those with bilateral discharge (2 cases in this group).  Secondly, for TLE that cannot be fixed laterally, such as MRI showing hippocampal sclerotic changes inconsistent with EEG monitoring results, or MRI negative but VEEG showing bilateral temporal lobe spikes, deep hippocampal electrode implantation combined with temporal lobe cortex electrode implantation should be performed. For medial temporal lobe epilepsy of unilateral origin, surgery is effective and should be preferred. However, in patients with bilateral independent origin of temporal lobe epilepsy, the decision of whether to operate and the surgical approach should be made carefully according to the patient’s condition [10-11]. Although temporal lobe epileptic discharges are mostly transmitted within the frontal and temporal lobes ipsilaterally, they can sometimes be transmitted directly to the contralateral hippocampal structures through the dorsal hippocampal association without passing through the ipsilateral cortex [4,12]. Bilateral temporal lobe abnormal epileptiform discharges are one of the most frequently encountered types of epilepsy in clinical practice. In this group, 7 cases of deep electrodes combined with temporal lobe cortex electrodes were implanted, and 7 cases of double temporal cortex electrodes were implanted (including 3 cases combined with single frontal electrode implantation and 1 case combined with unilateral temporo-occipital junction electrode implantation).   When designing the site of cranial drilling, the design should take into account the incision of resective surgery. A cranial CT examination is performed on the same day or the next day after surgery to determine the location of the electrodes and to understand whether there is intracranial hemorrhage. Positive and lateral cranial X-ray plain radiographs were performed in some patients.  Regarding the surgical approach in this group of patients, unilateral anterior temporal lobectomy was performed in 50 cases (83%) in this group if the origin was unilateral or if one side was predominant despite bilateral origin. In patients with TLE combined with frontal lobe epileptogenic foci, frontal lobe epileptogenic foci were combined with anterior temporal lobectomy according to intraoperative EEG, in 7 cases (12%) in this group. In one patient in this group, IVEEG showed bilateral frontal and bitemporal spikes, but predominantly left temporal, clinical symptoms showed rapid spread to the contralateral side, and the patient had fallen seizures, and corpus callosotomy was performed in combination with anterior temporal lobectomy (2%). In two patients of this group, IVEEG showed a posterior temporal origin, but the patients showed medial temporal lobe seizure manifestations such as abdominal rising sensation during seizures, and partial hippocampal resection was performed along with temporo-occipital neocortical focal resection (3%).  Complications of intracranial electrode implantation, Tanriverdi et al [13] reported 1.8% and 0.8% chance of infection and intracranial hemorrhage in 491 patients, while Van Gompel et al [5] reported 198 cases of intracranial electrode implantation with 5 cases of infection (2.5%) and 6 cases of hematoma (3.0%). In this group, one case of debridement decompression was performed for cerebral edema and one case of hematoma removal + debridement decompression was performed for intracranial hemorrhage, and there were no fatal cases. The pathology of the remaining 57 cases was consistent with the manifestation of medial temporal lobe epilepsy, except for 2 patients whose postoperative pathology was nodular cell glioma and 1 case who had undergone gamma knife treatment showing radiation necrosis.  In conclusion, when noninvasive preoperative evaluation methods are difficult to identify the epileptogenic focus, IVEEG is a necessary option. However, IVEEG is an invasive examination method and cannot cover all brain tissues indefinitely, so it is very important to carefully analyze the information of noninvasive examination and select the correct intracranial electrode implantation location. Under the existing technical conditions, IVEEG still has its irreplaceable application value, and proper application can benefit patients. It is believed that the efficacy of IVEEG will be further improved with the maturity of the implementation technology and the continuous progress of the detection methods.