Giuseppe Casaceli

Stereoelectroencephalography: Surgical methodology, safety, and stereotactic application accuracy in 500 procedures

BACKGROUND Stereoelectroencephalography (SEEG) methodology, originally developed by Talairach and Bancaud, is progressively gaining popularity for the presurgical invasive evaluation of drug-resistant epilepsies. OBJECTIVE To describe recent SEEG methodological implementations carried out in our center, to evaluate safety, and to analyze in vivo application accuracy in a consecutive series of 500 procedures with a total of 6496 implanted electrodes. METHODS Four hundred nineteen procedures were performed 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). RESULTS 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. CONCLUSION 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.

What is the role of the uncinate fasciculus? Surgical removal and proper name retrieval

The functional role of the uncinate fasciculus is still a matter of debate. We examined 44 patients submitted to awake surgery for removal of a left frontal or temporal glioma. In 18 patients, the removal included the uncinate fasciculus. We compared patients with or without removal on a series of neuropsychological tasks, performed at different time intervals: pre-surgery, in the first week after surgery and 3 months after surgery. Functional magnetic resonance and diffusion tensor imaging, fibre-tracking techniques were performed before surgery. At the last examination, patients with uncinate removal were significantly impaired in naming of famous faces and objects as compared with patients without removal. We further divided patients according to the site of the tumour (either frontal or temporal). At the follow-up, patients with a temporal glioma who underwent uncinate removal had the worst loss of performance in famous face naming. In addition, on the same task, the group with a frontal glioma that underwent resection of the frontal part of the uncinate performed significantly worse than the group with a frontal glioma but without uncinate removal. In conclusion, the resection of the uncinate fasciculus, in its frontal or temporal part, has long-lasting consequences for famous face naming. We suggest that this fibre tract is part of a circuitry involved in the retrieval of word form for proper names. Retrieval of conceptual knowledge was intact.

Intraoperative use of diffusion tensor imaging fiber tractography and subcortical mapping for resection of gliomas: technical considerations

Resection of lesions involving motor or language areas or pathways requires the intraoperative identification of functional cortical and subcortical sites for effectively and safe guidance. Diffusion tensor (DT) imaging and fiber tractography are MR imaging techniques based on the concept of anisotropic water diffusion in myelinated fibers, which enable 3D reconstruction and visualization of white matter tracts and provide information about the relationship of these tracts to the tumor mass. The authors routinely used DT imaging fiber tractography to reconstruct various tracts involved in the motor and/or language system in a large series of patients with lesions involving the motor and/or language areas or pathways. The DT imaging fiber tractography data were loaded into the neuronavigational system and combined intraoperatively with those obtained from direct electrical stimulation applied at the subcortical level. In this paper the authors report the results of their experience, describing the findings for each tract and discussing technical aspects of the combined use as well as the pitfalls.

Role of diffusion tensor magnetic resonance tractography in predicting the extent of resection in glioma surgery

Diffusion tensor imaging (DTI) tractography enables the in vivo visualization of the course of white matter tracts inside or around a tumor, and it provides the surgeon with important information in resection planning. This study is aimed at assessing the ability of preoperative DTI tractography in predicting the extent of the resection achievable in surgical removal of gliomas. Patients with low-grade gliomas (LGGs; 46) and high-grade gliomas (HGGs; 27) were studied using a 3T scanner according to a protocol including a morphological study (T2, fluid-attenuated inversion-recovery, T1 sequences) and DTI acquisitions (b = 1000 s/mm(2), 32 gradient directions). Preoperative tractography was performed off-line on the basis of a streamline algorithm, by reconstructing the inferior fronto-occipital (IFO), the superior longitudinal fascicle (SLF), and the corticospinal tract (CST). For each patient, the relationship between each bundle reconstructed and the lesion was analyzed. Initial and residual tumor volumes were measured on preoperative and postoperative 3D fluid-attenuated inversion-recovery images for LGGs and postcontrast T1-weighted scans for HGGs. The presence of intact fascicles was predictive of a better surgical outcome, because these cases showed a higher probability of total resection than did subtotal and partial resection. The presence of infiltrated or displaced CST or infiltrated IFO was predictive of a lower probability of total resection, especially for tumors with preoperative volume <100 cm(3). DTI tractography can thus be considered to be a promising tool for estimating preoperatively the degree of radicality to be reached by surgical resection. This information will aid clinicians in identifying patients who will mostly benefit from surgery.

Epilepsy surgery of focal cortical dysplasia-associated tumors.

The goal of the present study was to evaluate the clinical characteristics and postoperative seizure outcome of epileptogenic tumors associated with focal cortical dysplasias (FCDs) compared to both solitary FCD type I and solitary tumors. Particular attention is given to FCD type IIIb (tumors associated with FCD type I), which have been recently classified as a separate entity. We retrospectively reviewed the clinical charts of 1,109 patients who were operated on for drug‐resistant focal epilepsy, including 492 patients with a histologic diagnosis of solitary FCD I and II (83 and 157 cases, respectively), solitary tumors (179 cases), and FCD‐associated tumors (73 cases, 58 of which met the criteria of FCD IIIb of the new International League Against Epilepsy [ILAE] classification). The different subgroups were evaluated for clinical characteristics and postoperative surgical outcome. Clinical variables and postoperative seizure outcome of patients with coexisting tumor and FCDs (FCD IIIb and tumor associated FCD II) were similar to those of patients with a solitary tumor and differed significantly from patients with solitary FCDs. Nevertheless, tumors associated with FCDs are characterized by a striking male predominance and a higher seizure frequency as compared to solitary tumors. Patients with drug‐resistant focal epilepsy secondary to a solitary tumor or with a tumor‐associated FCD have similar basic clinical presentation and postoperative seizure outcome. Nevertheless, the epileptogenic contribution of the associated FCDs can be crucial, and it needs to be adequately assessed. The impact of FCD on tumor‐related epilepsy deserves future research in order to optimize the surgical strategies aimed at seizure relief.

Four-dimensional maps of the human somatosensory system

Significance Here, we show how anatomical and functional data recorded from patients undergoing stereo-EEG can be combined to generate highly resolved four-dimensional maps of human cortical processing. We used this technique, which provides spatial maps of the active cortical nodes at a millisecond scale, to depict the somatosensory processing following electrical stimulation of the median nerve in nearly 100 patients. The results showed that human somatosensory system encompasses a widespread cortical network including a phasic component, centered on primary somatosensory cortex and neighboring motor, premotor, and inferior parietal regions, as well as a tonic component, centered on the opercular and insular areas, lasting more than 200 ms. A fine-grained description of the spatiotemporal dynamics of human brain activity is a major goal of neuroscientific research. Limitations in spatial and temporal resolution of available noninvasive recording and imaging techniques have hindered so far the acquisition of precise, comprehensive four-dimensional maps of human neural activity. The present study combines anatomical and functional data from intracerebral recordings of nearly 100 patients, to generate highly resolved four-dimensional maps of human cortical processing of nonpainful somatosensory stimuli. These maps indicate that the human somatosensory system devoted to the hand encompasses a widespread network covering more than 10% of the cortical surface of both hemispheres. This network includes phasic components, centered on primary somatosensory cortex and neighboring motor, premotor, and inferior parietal regions, and tonic components, centered on opercular and insular areas, and involving human parietal rostroventral area and ventral medial-superior-temporal area. The technique described opens new avenues for investigating the neural basis of all levels of cortical processing in humans.

Cerebral Angiography for Multimodal Surgical Planning in Epilepsy Surgery: Description of a New Three-Dimensional Technique and Literature Review.

OBJECTIVE Cerebrovascular imaging is critical for safe and accurate planning of Stereo-ElectroEncephaloGraphy (SEEG) electrode trajectory. We developed a new technique for Cone Beam Computed Tomography (CBCT) Three-Dimensional Digital Subtraction Angiography (3D DSA). METHODS The workflow core is the acquisition of computed tomography datasets without (bone mask) and with selective injection of contrast medium in the main brain-feeding arteries, followed by dataset registration and subtraction. The images were acquired with the O-armTM 1000 System (Medtronic). Images were postprocessed with FSL software package. We retrospectively analyzed 191 3D DSA procedures and qualitatively analyzed the quality of each 3D DSA dataset. RESULTS The quality of 3D DSA was good in 150 procedures, sufficient in 37, and poor in 4. 3D rendering of the vascular tree was helpful for both SEEG implantation and resective surgery planning. Angiography complications occurred in only one procedure that was aborted due to a major allergic reaction to contrast medium. No other complications directly related to 3D DSA occurred. Minor intracerebral hemorrhage occurred in 2/191 patients after SEEG implantation, with no permanent sequelae. CONCLUSIONS CBCT 3D DSA is a safe diagnostic procedure for SEEG electrode trajectory planning and for 3D reconstructions of the vascular tree in multimodal scenes for resections. The high fidelity and geometric accuracy contribute to the safety of electrode implantation.

Automatic Trajectory Planner for StereoElectroEncephaloGraphy Procedures: A Retrospective Study

In StereoElectroEncephaloGraphy (SEEG) procedures, intracerebral electrodes are implanted in order to identify the epileptogenic zone in drug-resistant epileptic patients. This paper presents an automatic multitrajectory planner that computes the best trajectory in terms of distance from vessels and guiding screws angle, once the candidate entry and target regions are quickly and roughly defined. The planning process is designed also to spare some brain structures, such as cella media and trigone of the lateral ventricles and brain stem. The planner was retrospectively evaluated on 15 patients who had previously undergone SEEG investigation. Quantitative comparison was performed computing for each patient and for each electrode trajectory 1) the Euclidean distance from the closest vessel; 2) the trajectory incidence angle (guiding screws angle); and 3) the sulcality value. The automatic planner proved to satisfy the clinical requirements, planning safe trajectories in a clinical-compatible timeframe. Qualitative evaluation performed by three neurosurgeons showed that the automatically computed trajectories would have been accepted by them.

Implantation of Stereoelectroencephalography Electrodes: A Systematic Review

Background: Stereoelectroencephalography (SEEG) was developed by Talairach and Bancaud in Paris in the late 1950s. Subsequently, the Talairach methodology was adopted at a number of additional centers in Europe and Canada. Technical aspects remained essentially unchanged for the following 30 years. Only in the last two decades, because of advancements in image-guided surgery systems, robotics, and computer-aided planning, use of SEEG has become more widespread, and reports describing these new developments have been published. Objectives: This systematic review was designed to assess published reports of SEEG surgical techniques and safety profile. Data sources: An electronic search was performed of Medline, Embase, and Scopus databases. In addition, the content pages of several standard epilepsy surgery textbooks were searched. Full-text English studies describing SEEG surgical technique or pertinent epidemiological data were included. Conference abstracts, reviews, posters, editorials, comments, and letters were excluded. Results: Three hundred fifty-nine of 2,903 potentially eligible studies published by 32 centers were reviewed. Thirty-one of these primarily discussed the surgical technique. Thirty-five major complications (including 4 fatalities) were reported among 4,000 patients (0.8%) implanted with 33,000 electrodes. Limitations: The number of SEEG patients is likely to be underestimated because only a few groups have exhaustively reported their experience. Moreover, it is possible that a number of teams performing SEEG have not published studies on the topic. Conclusions: Rigorous SEEG, thanks to its basic principles and updated technologies, is a safe and accurate method to define the epileptogenic zone by means of stereotactically implanted intracerebral electrodes.

Multimodal responses induced by cortical stimulation of the parietal lobe: a stereo-electroencephalography study

The functional complexity of the parietal lobe still represents a challenge for neurophysiological and functional neuroimaging studies. While the somatosensory functions of the anterior parietal cortex are well established, the posterior parietal cortex has a relevant role in processing the sensory information, including visuo-spatial perception, visual attention, visuo-motor transformations and other complex and not completely understood functions. We retrospectively analysed all the clinical manifestations induced by intracerebral bipolar electrical stimulation in 172 patients suffering from drug-resistant focal epilepsy (mean age 25.6, standard deviation 11.6; 44% females and 56% males) with at least one electrode stereotactically implanted in the parietal cortex. A total of 1186 electrical stimulations were included in the analysis, of which 88 were subsequently excluded because of eliciting pathological electric activity or inducing ictal symptomatology. In the dominant parietal lobe, clinical responses were observed for 56 (25%) of the low-frequency stimulations and for 76 (50%) of the high-frequency stimulations. In the non-dominant parietal lobe, 111 (27%) low-frequency and 176 (55%) high-frequency stimulations were associated with a clinical response. Body scheme alteration was the only clinical effect showing a lateralization, as they were evoked only in the non-dominant hemisphere. The occurrence of somatosensory sensations, motor symptoms, dysarthria and multimodal responses were significantly associated with stimulation of the postcentral gyrus (odds ratio: 5.83, P < 0.001; odds ratio: 8.77, P < 0.001; odds ratio: 5.44, P = 0.011; odds ratio: 8.33, P = 0.006; respectively). Stimulation of the intraparietal sulcus was associated with the occurrence of sensory illusions or hallucinations (odds ratio: 8.68, P < 0.001) and eyeball/eyelid movements or sensations (odds ratio: 4.35, P = 0.047). To our knowledge, this is the only currently available complete revision of electrical stimulation of the entire parietal cortex with the aim to evaluate the neurophysiology of this relevant brain region. Our analysis offers a general overview of the multiple roles of the parietal cortex and supports its crucial involvement in different networks related to complex integrative functions.media-1vid110.1093/brain/awv187_video_abstractawv187_video_abstract.