Stereoelectroencephalography (sEEG) is a diagnostic procedure for a patient with refractory focal epilepsy that is performed to localize and define the epileptogenic zone. In contrast to grid electrodes, sEEG electrodes are implanted using minimal invasive operation techniques without large craniotomies. Stereoelectroencephalography is one of the intraoperative EEG techniques currently used in the presurgical work-up, and it is well-distinguished from other invasive techniques, such as subdural grids and strips.
Stereoelectroencephalography (SEEG) was originally developed by Jean Talairach and Bancaud.
SEEG depth electrodes enable exploration of deeply located structures and lesions, and of buried cortex, which are not easily assessable by subdural or other iEEG methods. Simultaneous recording of SEEG signals from deep and superficial brain structures allows, when the position of each electrode is precisely determined, delineation of a three-dimensional, spatial and temporal organization of epileptic activities. In the following chapter we discuss some specific indications (temporal or extra-temporal, lesional or non-lesional epilepsies) as well as the limits of the SEEG technique, with respect to some epileptological issues during presurgical evaluation 1).
The main advantage is the possibility to study the epileptogenic neuronal network in its dynamic and 3-dimensional aspect, with optimal time and space correlation, with the clinical semiology of the patient's seizures 2).
The accurate and automatic localisation of SEEG electrodes is crucial for determining the location of epileptic seizure onset.
Granados et al., presented a method robust to electrode bending that can accurately segment contact positions and bolt orientation. The techniques presented will allow further characterisation of bending within different brain regions 3).
Among other general indications for invasive intracranial electroencephalography (EEG) monitoring, its advantages include access to deep cortical structures, its ability to localize the epileptogenic zone when subdural grid electrodes have failed to do so, and its utility in the context of possible multifocal seizure onsets with the need for bihemispheric explorations.
In a study, Murakami et al., aim to examine the significance of magnetoencephalography dipole clusters and their relationship to stereo-electroencephalography findings, area of surgical resection, and seizure outcome. They also aim to define the positive and negative predictors based on magnetoencephalography dipole cluster characteristics pertaining to seizure-freedom. Included in this retrospective study were a consecutive series of 50 patients who underwent magnetoencephalography and stereo-electroencephalography at the Cleveland Clinic Epilepsy Center. Interictal magnetoencephalography localization was performed using a single equivalent current dipole model. Magnetoencephalography dipole clusters were classified based on tightness and orientation criteria. Magnetoencephalography dipole clusters, stereo-electroencephalography findings and area of resection were reconstructed and examined in the same space using the patient's own magnetic resonance imaging scan. Seizure outcomes at 1 year post-operative were dichotomized into seizure-free or not seizure-free. We found that patients in whom the magnetoencephalography clusters were completely resected had a much higher chance of seizure-freedom compared to the partial and no resection groups (P = 0.007). Furthermore, patients had a significantly higher chance of being seizure-free when stereo-electroencephalography completely sampled the area identified by magnetoencephalography as compared to those with incomplete or no sampling of magnetoencephalography results (P = 0.012). Partial concordance between magnetoencephalography and interictal or ictal stereo-electroencephalography was associated with a much lower chance of seizure freedom as compared to the concordant group (P = 0.0075). Patients with one single tight cluster on magnetoencephalography were more likely to become seizure-free compared to patients with a tight cluster plus scatter (P = 0.0049) or patients with loose clusters (P = 0.018). Patients whose magnetoencephalography clusters had a stable orientation perpendicular to the nearest major sulcus had a better chance of seizure-freedom as compared to other orientations (P = 0.042). Our data demonstrate that stereo-electroencephalography exploration and subsequent resection are more likely to succeed, when guided by positive magnetoencephalography findings. As a corollary, magnetoencephalography clusters should not be ignored when planning the stereo-electroencephalography strategy. Magnetoencephalography tight cluster and stable orientation are positive predictors for a good seizure outcome after resective surgery, whereas the presence of scattered sources diminishes the probability of favourable outcomes. The concordance pattern between magnetoencephalography and stereo-electroencephalography is a strong argument in favour of incorporating localization with non-invasive tools into the process of presurgical evaluation before actual placement of electrodes 5).
Willems et al., analyzed 18 consecutive patients (mean age: 30.5 years, range: 12-46; 61% female) undergoing invasive presurgical video-EEG monitoring via sEEG electrodes (n = 167 implanted electrodes) over a period of 2.5 years with robot-assisted implantation. There were no neurological deficits reported after implantation or explantation in any of the enrolled patients. Postimplantation imaging showed a minimal subclinical subarachnoid hemorrhage in one patient and further workup revealed a previously unknown factor VII deficiency. No injuries or status epilepticus occurred during video-EEG monitoring. In one patient, a seizure-related asymptomatic cross break of two fixation screws was found and led to revision surgery. Unspecific symptoms like headaches or low-grade fever were present in 10 of 18 (56%) patients during the first days of video-EEG monitoring and were transient. Postexplantation imaging showed asymptomatic and small bleedings close to four electrodes (2.8%).
Overall, sEEG is a safe and well-tolerated procedure. Systematic imaging after implantation and explantation helps to identify clinically silent complications of sEEG. In the literature, complication rates of up to 4.4% in sEEG and in 49.9% of subdural EEG are reported; however, systematic imaging after explantation was not performed throughout the studies, which may have led to underreporting of associated complications 6).
Over a period of 4 years, Serletis et al., prospectively identified 200 patients with refractory epilepsy who collectively underwent 2663 tailored SEEG electrode implantations for invasive intracranial EEG monitoring and extraoperative mapping. The first 122 patients underwent conventional Leksell frame-based SEEG electrode placement; the remaining 78 patients underwent frameless stereotaxy under robotic guidance, following acquisition of a stereotactic ROSA robotic device at the authors' institution. Electrodes were placed according to a preimplantation hypothesis of the presumed epileptogenic zone, based on a standardized preoperative workup including video-EEG monitoring, MRI, PET, ictal SPECT, and neuropsychological assessment. Demographic features, seizure semiology, number and location of implanted SEEG electrodes, and location of the epileptogenic zone were recorded and analyzed for all patients. For patients undergoing subsequent craniotomy for resection, the type of resection and procedure-related complications were prospectively recorded. These results were analyzed and correlated with pathological diagnosis and postoperative seizure outcomes.
The epileptogenic zone was confirmed by SEEG in 154 patients (77%), of which 134 (87%) underwent subsequent craniotomy for epileptogenic zone resection. Within this cohort, 90 patients had a minimum follow-up of at least 12 months; therein, 61 patients (67.8%) remained seizure free, with an average follow-up period of 2.4 years. The most common pathological diagnosis was focal cortical dysplasia Type I (55 patients, 61.1%). Per electrode, the surgical complications included wound infection (0.08%), hemorrhagic complications (0.08%), and a transient neurological deficit (0.04%) in a total of 5 patients (2.5%). One patient (0.5%) ultimately died due to intracerebral hematoma directly ensuing from SEEG electrode placement 7).
Five patients (three male, age 5-33 years) with drug-resistant focal epilepsy presented a single NH at brain MRI. Following video-EEG monitoring, patients underwent SEEG recording to better identify the epileptogenic zone. All patients received RF-THC of the NH, using contiguous contacts of the electrodes employed for recording. The contacts for RF-THC lesions were chosen according to anatomical (intranodular position) and electrical (intranodular ictal low-voltage fast activity) criteria.
At SEEG recordings, ictal discharge originated from the NH alone in three cases and from the NH and ipsilateral hippocampus in one case. In the remaining case, different sites of ictal onset, including the NH, were identified within the left frontal lobe. No adverse effects related to the RF-THC procedures were observed, apart from a habitual seizure that occurred during coagulation in one patient. Postprocedural sustained seizure freedom was detected in four cases (mean follow-up 33.5 months). In the case with left frontal multifocal ictal activity, RF-THC of the NH provided no benefit on seizures, and the patient is seizure-free after left frontal lobe resection.
SEEG-guided RF-THC proved to be a safe and effective option in our small case-series of NH-related focal epilepsy. The indications to this treatment were strictly dependent on findings of intracerebral recording by SEEG, which can define the role of the NH in the generation of the ictal discharge 8).
Four hundred nineteen procedures were performed in the Claudio Munari Centre for Epilepsy and Parkinson Surgery, Niguarda Ca' Granda Hospital, Milano, Italy with the traditional 2-step surgical workflow, which was modified for the subsequent 81 procedures. The new workflow entailed acquisition of brain 3-dimensional angiography and magnetic resonance imaging in frameless and markerless conditions, advanced multimodal planning, and robot-assisted implantation. Quantitative analysis for in vivo entry point and target point localization error was performed on a sub–data set of 118 procedures (1567 electrodes).
The methodology allowed successful implantation in all cases. Major complication rate was 12 of 500 (2.4%), including 1 death for indirect morbidity. Median entry point localization error was 1.43 mm (interquartile range, 0.91-2.21 mm) with the traditional workflow and 0.78 mm (interquartile range, 0.49-1.08 mm) with the new one (P < 2.2 × 10). Median target point localization errors were 2.69 mm (interquartile range, 1.89-3.67 mm) and 1.77 mm (interquartile range, 1.25-2.51 mm; P < 2.2 × 10), respectively.
SEEG is a safe and accurate procedure for the invasive assessment of the epileptogenic zone. Traditional Talairach methodology, implemented by multimodal planning and robot-assisted surgery, allows direct electrical recording from superficial and deep-seated brain structures, providing essential information in the most complex cases of drug-resistant epilepsy 9).
Fifteen patients (9 girls and 6 boys, mean age 34.1 ± 7.3 months, range 21-45 months), potentially candidates to receive surgical treatment for their focal drug-resistant epilepsy, were evaluated using stereo-EEG recording for a detailed definition of the epileptogenic zone. Stereoelectroencephalography was indicated because neuroradiological (brain MRI) and video-EEG data failed to adequately localize the epileptogenic zone. Stereotactic placement of multicontact intracerebral electrodes was preceded by the acquisition of all pertinent anatomical information from structural and functional MRI and from brain angiography, enabling the accurate targeting of desired structures through avascular trajectories. Stereoelectroencephalography monitoring attempted to record habitual seizures; electrical stimulations were performed to induce seizures and for the functional mapping of eloquent areas. Stereoelectroencephalography-guided microsurgery, when indicated, pointed to removal of the epileptogenic zone and seizure control.
Brain MRI revealed an anatomical lesion in 13 patients (lobar in 2 cases, multilobar or hemispheric in 11 cases) and was unremarkable in 2 patients. One patient underwent 2 stereo-EEG studies. The arrangement of the intracerebral electrodes was unilateral in all but 1 case. One patient died the day following electrode placement due to massive brain edema and profound hyponatremia of undetermined cause. In 8 cases intracerebral electrical stimulations allowed mapping of functionally critical areas; in 3 other cases that received purposeful placement of electrodes in presumably eloquent areas, no functional response was obtained. Of the 14 patients who completed stereo-EEG monitoring, 1 was excluded from surgery for multifocality of seizures and 13 underwent operations. Postoperatively, 2 patients exhibited an anticipated, permanent motor deficit, 3 experienced a transient motor deficit, and 2 experienced transient worsening of a preexisting motor deficit. Three patients developed a permanent homonymous hemianopia after posterior resections. Histological analysis revealed cortical malformations in 10 cases. Of the 10 patients with a postoperative follow-up of at least 12 months, 6 (60%) were seizure-free (Engel Class Ia), 2 (20%) experienced a significant reduction of seizures (Engel Class II), and 2 (20%) were unchanged (Engel Class IV).
The present study indicates that stereo-EEG plays a prominent role in the presurgical evaluation of focal epilepsies also in the first years of life and that it may offer a surgical option in particularly complex cases that would have scarcely benefitted from further medical treatment. Results of stereo-EEG-guided resective surgery were excellent, with 80% of patients exhibiting a substantial improvement in seizures. In consideration of the potentially life-threatening risks of major intracranial surgery in this specific age group, the authors recommend reserving stereo-EEG evaluations for infants with realistic chances of benefiting from surgery 10).
Two-hundred fifteen stereotactic implantations of multilead intracerebral electrodes were performed in 211 patients (4 patients were explored twice), who showed variable patterns of localizing incoherence among electrical (interictal/ictal scalp electroencephalography), clinical (ictal semeiology), and anatomic (magnetic resonance imaging [MRI]) investigations. MRI scanning showed a lesion in 134 patients (63%; associated with mesial temporal sclerosis in 7) and no lesion in 77 patients (37%; with mesial temporal sclerosis in 14 patients). A total of 2666 electrodes (mean, 12.4 per patient) were implanted (unilaterally in 175 procedures and bilaterally in 40). For electrode targeting, stereotactic stereoscopic cerebral angiograms were used in all patients, coupled with a coregistered three-dimensional MRI scan in 108 patients.
One hundred eighty-three patients (87%) were scheduled for resective surgery after SEEG recording, and 174 have undergone surgery thus far. Resections sites were temporal in 47 patients (27%), frontal in 55 patients (31.6%), parietal in 14 patients (8%), occipital in one patient (0.6%), rolandic in one patient (0.6%), and multilobar in 56 patients (32.2%). Outcome on seizures (Engel's classification) in 165 patients with a follow-up period of more than 12 months was: Class I, 56.4%; Class II, 15.1%; Class III, 10.9%; and Class IV, 17.6%. Outcome was significantly associated with the results of MRI scanning (P = 0.0001) and with completeness of lesion removal (P = 0.038). Morbidity related to electrode implantation occurred in 12 procedures (5.6%), with severe permanent deficits from intracerebral hemorrhage in 2 (1%) patients.
SEEG is a useful and relatively safe tool in the evaluation of surgical candidates when noninvasive investigations fail to localize the epileptogenic zone. SEEG-based resective surgery may provide excellent results in particularly complex drug-resistant epilepsies 11).
By using these permanently implanted depth electrodes, Guénot et al are able to perform radiofrequency (RF)-thermolesions of the epileptic foci. We report the technical data required to perform such multiple cortical thermolesions, as well as preliminary results in terms of seizure outcome in a group of 20 patients.
Lesions were performed by using 100- to 110-mA bipolar current (50 V), applied for 10 to 50 s. Each thermocoagulation produced a 5- to 7-mm diameter cortical lesion. In total, two to 16 lesions were performed in each of the 20 patients. Lesions were placed without anesthesia. No general or neurologic complication occurred during the procedures. Two transient postprocedure side effects, consisting of paresthetic sensations in the mouth and mild apraxia of the hand, were observed.
At a follow-up time of 8 to 31 months (mean, 19 months), 15% of the patients became seizure free, 40% experienced a > or =80% reduction of their seizure frequency, and 45% were not significantly improved.
SEEG-guided RF thermolesions is a safe technique. The preliminary results indicate that such lesions can lead to a significant reduction of seizure frequency and could be proposed as a palliative procedure if no resective surgery is possible. A randomized controlled trial is needed to determine which patients are likely to respond to SEEG-guided RF thermolesions. 12).