Safe use of subdermal needles for intraoperative monitoring with MRI.

OBJECTIVE: The purpose of this study was to develop safe, site-specific procedures for placing and leaving subdermal needle leads for intraoperative monitoring (IOM) during intraoperative MRI procedures. METHODS: The authors tested a variety of standard subdermal needle electrodes designed and FDA-approved for IOM in the conventional operating room. Testing was used to determine the conditions necessary to avoid thermal injury and significant image artifacts with minimal disruption of IOM and MRI procedures. Phantom testing was performed with a fiber optic (lead) temperature monitoring system and was followed by testing of leads placed in a healthy volunteer. The volunteer testing used electrode placements typical of standard IOM cases, together with radiofrequency (RF) coil placement and imaging sequences routinely employed for these case types. Lead length was investigated to assess heating effects for electrodes placed within the RF coil. RESULTS: The authors found that conventional stainless steel (SS) and platinum/iridium (Pt/Ir) subdermal needles can be used safely without significant heating when placed outside the RF coil, and this accounts for the majority or entirety of electrode placements. When placed within the RF coil, Pt/Ir leads produced minimal image artifacts, while SS leads produced potentially significant artifacts. In phantom testing, significant heating was demonstrated in both SS and Pt/Ir leads placed within the RF coil, but only during high-resolution T2-weighted scanning. This problem was largely, but not completely, eliminated when leads were shortened to 25 cm. Human testing was unremarkable except for nonpainful heating detected in a few electrodes during thin-slice (1.5 mm) FLAIR scanning. Transient irritation (skin reddening along the needle tract) was noted at 2 of the electrodes with detectable heating. CONCLUSIONS: The authors were satisfied with the safety of their site-specific procedures and have begun with off-label use (following institutional review board approval and obtaining patient informed consent) of tested monitoring leads in cases that combine IOM and MRI. The authors recommend that all facilities perform their own site-specific testing of monitoring leads before proceeding with their routine use.

Improved mapping of interictal epileptiform discharges with EEG-fMRI and voxel-wise functional connectivity analysis.

OBJECTIVE: We describe a novel method to spatially map interictal epileptiform discharges (IEDs) through voxel-wise functional connectivity analysis of the functional magnetic resonance imaging (fMRI) portion of simultaneous electroencephalography (EEG)-fMRI data. This method measures the local synchronicity of fMRI signals associated with IED and, in contrast to conventional methods, does not require modeling of neural activities or hemodynamic response. METHODS: Simultaneous EEG-fMRI was performed on six patients with focal epilepsy. IED events were detected from the EEG data. The fMRI data was subdivided into time segments of 20 s in length, and then reorganized into one set of concatenated time series containing the IED events and many sets without IEDs. Local degree centrality (LDC), a metric of functional connectivity, was computed for each brain voxel to summarize its signal correlations to brain voxels within 14 mm of physical distance. This computation was repeated for each set of concatenated time series, yielding one whole-brain LDC map for time with the IED events and many maps for time without IED. A statistical score was computed for each voxel to detect the voxels with significant LDC value differences associated with IEDs. The fMRI data were also processed separately by conventional methods for comparison. RESULTS: In all six patients, regions with significant LDC increase during IEDs were concordant in location to both simultaneous EEG and the epileptogenic focus determined from separate clinical studies. In contrast, results from the conventional methods were concordant in only three patients. SIGNIFICANCE: We show that for focal epilepsy, voxel-wise functional connectivity analysis of EEG-fMRI data may improve IED localization and EEG concordance compared to the conventional analysis. This new analytic method may improve the robustness of interictal EEG-fMRI as a technique for mapping the epileptogenic focus, and helps study the local synchronization aspect of the epileptic network.

Interictal PET and ictal subtraction SPECT: sensitivity in the detection of seizure foci in patients with medically intractable epilepsy.

PURPOSE: Interictal positron emission tomography (PET) and ictal subtraction single photon emission computed tomography (SPECT) of the brain have been shown to be valuable tests in the presurgical evaluation of epilepsy. To determine the relative utility of these methods in the localization of seizure foci, we compared interictal PET and ictal subtraction SPECT to subdural and depth electrode recordings in patients with medically intractable epilepsy. METHODS: Between 2003 and 2009, clinical information on all patients at our institution undergoing intracranial electroencephalography (EEG) monitoring was charted in a prospectively recorded database. Patients who underwent preoperative interictal PET and ictal subtraction SPECT were selected from this database. Patient characteristics and the findings on preoperative interictal PET and ictal subtraction SPECT were analyzed. Sensitivity of detection of seizure foci for each modality, as compared to intracranial EEG monitoring, was calculated. KEY FINDINGS: Fifty-three patients underwent intracranial EEG monitoring with preoperative interictal PET and ictal subtraction SPECT scans. The average patient age was 32.7 years (median 32 years, range 1-60 years). Twenty-seven patients had findings of reduced metabolism on interictal PET scan, whereas all 53 patients studied demonstrated a region of relative hyperperfusion on ictal subtraction SPECT suggestive of an epileptogenic zone. Intracranial EEG monitoring identified a single seizure focus in 45 patients, with 39 eventually undergoing resective surgery. Of the 45 patients in whom a seizure focus was localized, PET scan identified the same region in 25 cases (56% sensitivity) and SPECT in 39 cases (87% sensitivity). Intracranial EEG was concordant with at least one study in 41 cases (91%) and both studies in 23 cases (51%). In 16 (80%) of 20 cases where PET did not correlate with intracranial EEG, the SPECT study was concordant. Conversely, PET and intracranial EEG were concordant in two (33%) of the six cases where the SPECT did not demonstrate the seizure focus outlined by intracranial EEG. Thirty-three patients had surgical resection and >2 years of follow-up, and 21 of these (64%) had Engel class 1 outcome. No significant effect of imaging concordance on seizure outcome was seen. SIGNIFICANCE: Interictal PET and ictal subtraction SPECT studies can provide important information in the preoperative evaluation of medically intractable epilepsy. Of the two studies, ictal subtraction SPECT appears to be the more sensitive. When both studies are used together, however, they can provide complementary information.

Surgical techniques for investigating the role of the insula in epilepsy: a review.

Intracranial electroencephalography monitoring of the insula is an important tool in the investigation of the insula in medically intractable epilepsy and has been shown to be safe and reliable. Several methods of placing electrodes for insular coverage have been reported and include open craniotomy as well as stereotactic orthogonal and stereotactic anterior and posterior oblique trajectories. The authors review each of these techniques with respect to current concepts in insular epilepsy.

Brain stimulation for the treatment of epilepsy.

Direct brain stimulation is an emerging treatment of epilepsy. Scheduled or responsive stimulation has been applied. The most explored targets for scheduled stimulation are the anterior nucleus of the thalamus and the hippocampus. The anterior nucleus of the thalamus was studied in a large multicenter trial. There was a significant seizure reduction with the stimulator "on" versus "off" during several months after stimulator implantation. The hippocampus as stimulation target has not yet been studied in a large randomized trial. Responsive stimulation applies a stimulus whenever epileptiform activity occurs. It requires on-line detection of epileptiform activity. This concept is based on the observation that epileptiform activity during functional mapping can be aborted by brief pulses of cortical stimulation. Current technology is able to detect seizure activity intracranially on-line and delivers a high frequency stimulus if epileptiform activity is detected. A large randomized multicenter trial has been conducted testing this system for focal epilepsy.

Intractable occipital lobe epilepsy: clinical characteristics and surgical treatment.

Intractable occipital lobe epilepsy remains a surgical challenge. Clinical characteristics of 14 patients were analyzed. Twelve patients had surgery, seven patients had visual auras (50%) and only eight patients (57%) had posterior scalp EEG changes. Ictal single-proton emission computed tomography (SPECT) incorrectly localized in 7 of 10 patients. Six patients (50%) had Engel's class I outcome. Patients with inferior occipital seizure onset appeared to fare better (three of four class I) than patients with lateral or medial occipital seizure onset (three of eight class I). Patients who had all three occipital surfaces covered with electrodes had a better outcome (four of five class I) than patients who had limited electroencephalography (EEG) coverage (two of seven class I). Magnetic resonance imaging (MRI) lesions did not guarantee a seizure free outcome. In conclusion, visual auras, scalp EEG, and imaging findings are not reliable for correct identification of occipital onset. Occipital seizure onset can be easily missed in nonlesional epilepsy. Comprehensive intracranial EEG coverage of all three occipital surfaces leads to better outcomes.

Robotic image-guided depth electrode implantation in the evaluation of medically intractable epilepsy.

OBJECT: The authors describe their experience with a technique for robotic implantation of depth electrodes in patients concurrently undergoing craniotomy and placement of subdural monitoring electrodes for the evaluation of intractable epilepsy. METHODS: Patients included in this study underwent evaluation in the Dartmouth Surgical Epilepsy Program and were recommended for invasive seizure monitoring with depth electrodes between 2006 and the present. In all cases an image-guided robotic system was used during craniotomy for concurrent subdural grid electrode placement. A total of 7 electrodes were placed in 4 patients within the time period. RESULTS: Three of 4 patients had successful localization of seizure onset, and 2 underwent subsequent resection. Of the patients who underwent resection, 1 is now seizure free, and the second has only auras. There was 1 complication after subpial grid placement but no complications related to the depth electrodes. CONCLUSIONS: Robotic image-guided placement of depth electrodes with concurrent craniotomy is feasible, and the technique is safe, accurate, and efficient.

Functional magnetic resonance imaging of the primary somatosensory cortex in piglets.

OBJECT: The piglet is an excellent model for the developing human brain, and has been used increasingly in various centers for studies of traumatic brain injury and other insults. Unlike rodent or primate models, however, there are few behavioral scales for the piglet, and the available ones are used to test general responsiveness rather than specific functional outcome. The differing behavioral repertoires of animals of different ages provide an additional challenge when age-dependent injury responses are compared. To overcome these experimental limitations of piglets in brain injury research, the authors developed a functional magnetic resonance (fMR) imaging paradigm that can be used to track recovery in the somatosensory cortex over time in anesthetized animals of different ages. METHODS: Fifteen fMR imaging studies in eight piglets were performed before and after scaled cortical impact injury to the primary somatosensory cortex subserving snout sensation. Specific anesthetic and imaging protocols enabled visualization of cortical activation, and comparison with somatosensory evoked potentials obtained before and after injury was obtained. A piglet brain template for group-level analysis of these data was constructed, similar to the fMR imaging techniques used in humans, to allow for group comparisons and longitudinal change analysis over time. CONCLUSIONS: Loss of function in a specifically traumatized cortical region and its subsequent recovery over time can now be demonstrated visually by fMR imaging in the piglet. Besides its value in understanding intrinsic recovery mechanisms and plasticity at different ages, this functional outcome measure will enable the use of the piglet model in treatment trials specifically designed for the immature brain.

Source localization using a current-density minimization approach.

Determining the location of cortical activity from electroencephalographic (EEG) data is important clinically. In this paper, a method is presented which uses the powerful optimization method of simulated annealing in conjunction with a finite-element-based model of the search domain for single-time slice solution of the EEG-inverse problem. The algorithm highlights a new objective function based on the current-density boundary integral associated with the finite-element formulation as the basis for parameter optimization. In two-dimensional experiments in a shallow tank containing saline, single dipoles are located within 2 mm. Simulations studying the algorithms response to structured noise are also presented. The new objective function is shown to take advantage of the natural framework associated with finite-elements and the results suggest that the approach is capable of resolving dipole locations in simulations and experiments.

Occipitotemporal hippocampal depth electrodes in intracranial epilepsy monitoring: safety and utility.

OBJECT: Intracranial monitoring for epilepsy has been proven to enhance diagnostic accuracy and provide localizing information for surgical treatment of intractable seizures. The authors investigated the usefulness of hippocampal depth electrodes in the era of more advanced imaging techniques. METHODS: Between 1988 and 2010, 100 patients underwent occipitotemporal hippocampal depth electrode (OHDE) implantation as part of invasive seizure monitoring, and their charts were retrospectively reviewed. The authors' technique involved the stereotactically guided (using the Leksell model G frame) implantation of a 12-contact depth electrode directed along the long axis of the hippocampus, through an occipital twist drill hole. RESULTS: Of the 100 patients (mean age 35.0 years [range 13-58 years], 51% male) who underwent intracranial investigation, 84 underwent resection of the seizure focus. Magnetic resonance imaging revealed mesial temporal sclerosis (MTS) in 27% of patients, showed abnormal findings without MTS in 55% of patients, and showed normal findings in 18% of patients. One patient developed a small asymptomatic occipital hemorrhage around the electrode tract. The use of OHDEs enabled epilepsy resection in 45.7% of patients who eventually underwent standard or selective temporal lobe resection. The hippocampal formation was spared during surgery because data obtained from the depth electrodes showed no or only secondary involvement in 14% of patients with preoperative temporal localization. The use of OHDEs prevented resections in 12% of patients with radiographic evidence of MTS. Eighty-three percent of patients who underwent resection had Engel Class I (68%) or II (15%) outcome at 2 years of follow-up. CONCLUSIONS: The use of OHDEs for intracranial epilepsy monitoring has a favorable risk profile, and in the authors' experience it proved to be a valuable component of intracranial investigation. The use of OHDEs can provide the sole evidence for resection of some epileptogenic foci and can also result in hippocampal sparing or prevent likely unsuccessful resection in other patients.

Subdural interhemispheric grid electrodes for intracranial epilepsy monitoring: feasibility, safety, and utility: clinical article.

OBJECT: Intracranial monitoring for epilepsy has been proven to enhance diagnostic accuracy and provide localizing information for surgical treatment of intractable seizures. The authors investigated their experience with interhemispheric grid electrodes (IHGEs) to assess the hypothesis that they are feasible, safe, and useful. METHODS: Between 1992 and 2010, 50 patients underwent IHGE implantation (curvilinear double-sided 2 × 8 or 3 × 8 grids) as part of arrays for invasive seizure monitoring, and their charts were retrospectively reviewed. RESULTS: Of the 50 patients who underwent intracranial investigation with IHGEs, 38 eventually underwent resection of the seizure focus. These 38 patients had a mean age of 30.7 years (range 11-58 years), and 63% were males. Complications as a result of IHGE implantation consisted of transient leg weakness in 1 patient. Of all the patients who underwent resective surgery, 21 (55.3%) had medial frontal resections, 9 of whom (43%) had normal MRI results. Localization in all of these cases was possible only because of data from IHGEs, and the extent of resection was tailored based on these data. Of the 17 patients (44.7%) who underwent other cortical resections, IHGEs were helpful in excluding medial seizure onset. Twelve patients did not undergo resection because of nonlocalizable or multifocal disease; in 2 patients localization to the motor cortex precluded resection. Seventy-one percent of patients who underwent resection had Engel Class I outcome at the 2-year follow-up. CONCLUSIONS: The use of IHGEs in intracranial epilepsy monitoring has a favorable risk profile and in the authors' experience proved to be a valuable component of intracranial investigation, providing the sole evidence for resection of some epileptogenic foci.

Stereotactic depth electrode investigation of the insula in the evaluation of medically intractable epilepsy.

OBJECT: The authors describe their experience with stereotactic implantation of insular depth electrodes in patients with medically intractable epilepsy. METHODS: Between 2001 and 2009, 20 patients with epilepsy and suspected insular involvement during seizures underwent intracranial electrode array implantation at the authors' institution. All patients had either 1 or 2 insular depth electrodes placed as part of an intracranial array. RESULTS: A total of 29 insular depth electrodes were placed using a frontal oblique trajectory. Eleven patients had a single insular electrode placed and 8 patients had 2 insular electrodes placed unilaterally. One patient had bilateral insular electrodes implanted. Postoperative imaging demonstrated satisfactory placement in all but 1 instance, and there was no associated morbidity or mortality. Fourteen patients underwent a subsequent resection, involving the frontal lobe (9 patients), temporal lobe (4), or frontotemporal lobes (1), and of these, 11 currently have Engel Class I outcome. Two patients (10%) had seizures originating within the insula and another 5 patients (25%) demonstrated early specific insular involvement. Neither patient with an insular seizure focus went on to resection. All 5 of the patients with early specific insular involvement underwent an insula-sparing resective procedure with Engel Class I outcome in all cases. CONCLUSIONS: Stereotactic placement of insular electrodes via a frontal oblique approach is a safe and efficient technique for investigating insular involvement in medically intractable epilepsy. The information obtained from insular recording can be valuable for appreciating the degree of insular contribution to seizures, allowing localization to the insula or clearer implication of other sites.

Technique for the localization of intracranially implanted electrodes.

OBJECT: The anatomical localization of electrodes in the human brain is important for the interpretation of pathophysiological (epileptifom spikes, seizures) and functional data (stimulation mapping, evoked potentials). Electroencephalography and evoked potentials are volume-conducted field effects that are most easily interpreted with knowledge of the location and topology of adjacent structures, and brain stimulation techniques produce current fields whose effects are highly dependent on the geometry of electrode assemblies in relation to adjacent structures. In this paper, the authors describe a straightforward method for implanted electrode localization, and detail their experience to date with the technique. METHODS: The described method is based on the coregistration of preoperative MR imaging studies with postimplant CT scans by using standard mutual information optimization of rigid body transformation of the CT to the MR image. Fused images of the MR and thresholded CT images are derived, and electrodes are visualized using various standard computer projections, renderings, and measurement tools. RESULTS: The authors have successfully used the described method over an extended period to localize electrode contacts in intracranial implants for seizure localization, and in long-term implants for movement disorders and seizure control. The accuracy of localization is very good, although it is dependent on image quality and possible brain shift between acquisition of the CT and MR images. CONCLUSIONS: This method is easily implemented and is useful for a wide variety of clinical and research applications. It is a straightforward process to extend it to additional image modalities that are emerging for surgical planning and image guidance.

Statistical mapping of scalp-recorded ictal EEG records using wavelet analysis.

PURPOSE: The wavelet transform (WT) is well suited for the analysis of signals whose characteristics vary rapidly over time. We devised a computerized method for objective scoring of scalp-recorded seizures that takes advantage of the WT. METHODS: Using wavelet coefficients as a metric, we devised a statistical scoring method aimed at detecting significant and sustained rhythmic buildup. The approach was used to create spatiotemporal significance maps for each seizure. Each seizure was also independently analyzed by computer and an expert reader not involved in the clinical workup or computer analysis of these patients. Hierarchical decision rules for determining seizure lateralization and localization were established from a training set of seizures and subsequently tested on those from an independent test set of seizures. The test dataset included a total of 57 scalp-recorded seizures from 18 patients, each with a > or =12-month seizure-free surgical outcome. RESULTS: Validation was determined by the site of surgical resection. Of the 57 seizure records in the test dataset, the computerized approach resulted in 48 correctly lateralized seizures as compared to 34 for the expert reader. Further, the computer correctly localized 41 seizures to the expert's 31. CONCLUSIONS: The method presented appears to provide an objective basis for the intrachannel scoring of ictal EEGs with minimal interference from artifacts and intermittent discharges. Although the approach has so far shown a substantial improvement over expert scoring in estimating the lateralization and locus of seizure onset, further testing is required to fully evaluate fully its diagnostic accuracy.

Validation of ictal single photon emission computed tomography with depth encephalography and epilepsy surgery.

Many centers have reported that ictal single photon emission computed tomography (SPECT) localizes regions of seizure onset with greater sensitivity and specificity than interictal SPECT. Here we report interictal and ictal SPECT scan results in both lesional and nonlesional cases. Using technetium hexamethyl propylamenamine oxide (HMPAO) or ethyl cysteinate dimer (ECD), these scans were done in 52 patients with partial and secondarily generalized seizures. Twenty-five had normal MRI and 27 showed structural lesions. None had mesial temporal sclerosis clearly identified on MRI. All 52 subsequently had interictal and ictal intracranial EEG studies that appeared to localize the seizure focus. Thirty-nine patients had surgery and have been followed for 2 or more years. Interictal SPECT scans showed focal hypoperfusion consistent with intracranial EEG localization of the seizure focus in 29% of patients. In another 13%, there was correct lateralization but not localization. Ictal SPECT scans showed focal hyperperfusion consistent with intracranial EEG localization of the seizure focus in 52% of patients. In another 25%, there was correct lateralization but not localization. The presence or absence of structural lesions on MRI did not affect ictal hyperperfusion or its correlation with intracranial EEG. Thirty-nine patients had resective surgery, of whom 62% had class I outcomes. There was a trend towards better outcome when ictal SPECT data were concordant with intracranial EEG data. The presence or absence of structural lesions on MRI did not affect the likelihood of class I outcome. Ictal SPECT is superior to interictal SPECT in localizing and lateralizing seizure foci. Its results correlate well with intracranial EEG, but in more than one third of cases, the latter shows focal seizure onset in areas that do not show focal hyperperfusion. Surgical outcome tends to be better when the two modalities give concordant results.