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Aaron A. Cohen-Gadol, Jeffrey W. Britton, Clifford R. Jack Jr., Jonathan A. Friedman, and W. Richard Marsh

✓ Transient neuroimaging abnormalities associated with seizure activity have received little attention in the literature. The authors report a focal magnetic resonance (MR) imaging abnormality of the corpus callosum in a patient following a secondary generalized seizure. A 27-year-old right-handed man presented with a history of medically refractory partial seizures since the age of 1 year. The results of an MR imaging study obtained 4 months prior to the patient undergoing video-electroencephalography monitoring were unremarkable. After the patient discontinued all antiepileptic medications, a secondary generalized seizure of right temporal origin was recorded. Five days later, repeated MR imaging revealed a nonenhancing 14 × 11—mm ovoid hyperintense lesion in the splenium of corpus callosum. The patient was asymptomatic, and his neurological and neurocognitive examinations remained unremarkable. Follow-up MR imaging 5 weeks and 1 year later demonstrated near-complete resolution of the lesion. Benign and transient abnormalities in the splenium can occur as a periictal phenomenon. A high index of suspicion and follow-up imaging may prevent further unwarranted intervention.

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Boby V. Maramattom, Jeffrey W. Britton, Gena R. Ghearing, and Eelco F. M. Wijdicks

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Aaron A. Cohen-Gadol, Jeffrey W. Britton, Frederic P. Collignon, Lisa M. Bates, Gregory D. Cascino, and Fredric B. Meyer

Object. Surgical treatment options for intractable seizures caused by a nonlesional epileptogenic focus located in the central sulcus region are limited. The authors describe an alternative surgical approach for treating medically refractory nonlesional perirolandic epilepsy.

Methods. Five consecutive patients who were treated between 1996 and 2000 for nonlesional partial epilepsy that had originated in the central lobule were studied. The patients' ages ranged from 16 to 56 years (mean 28.6 years; there were four men and one woman). The duration of their epilepsy ranged from 8 to 39 years (mean 20.2 years), with a mean seizure frequency of 19 partial seizures per week. Preoperative assessment included video electroencephalography (EEG) and subtracted ictal—interictal single-photon emission computerized tomography coregistered with magnetic resonance imaging (SISCOM). Patients underwent an awake craniotomy stereotactically guided by the ictal EEG and SISCOM studies. Cortical stimulation was used to identify the sensorimotor cortex and to reproduce the patient's aura. A subdural grid was then implanted based on these results. Subsequent postoperative ictal electrocorticographic recordings and cortical stimulation further delineated the site of seizure onset and functional anatomy. During a second awake craniotomy, a limited resection of the epileptogenic central lobule region was performed while function was continuously monitored intraoperatively. One resection was limited to the precentral gyrus, two to the postcentral gyrus, and in two the excisions involved regions of both the pre- and postcentral gyri.

In three patients a hemiparesis occurred postsurgery but later resolved. In the four patients whose resection involved the postcentral gyrus, transient cortical sensory loss and apraxia occurred, which completely resolved in three. Two patients are completely seizure free, two have experienced occasional nondisabling seizures, and one patient has benefited from a more than 75% reduction in seizure frequency. The follow-up period ranged from 2 to 5.5 years (mean 3.5 years).

Conclusions. A limited resection of the sensorimotor cortex may be performed with acceptable neurological morbidity in patients with medically refractory perirolandic epilepsy. This procedure is an alternative to multiple subpial transections in the surgical management of intractable nonlesional epilepsy originating from the sensorimotor cortex.

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Robert D. Ecker, Stephan J. Goerss, Fredric B. Meyer, Aaron A. Cohen-Gadol, Jeffrey W. Britton, and James A. Levine

✓ High-resolution dynamic infrared (DIR) imaging provides intraoperative real-time physiological, anatomical, and pathological information; however, DIR imaging has rarely been used in neurosurgical patients. The authors report on their initial experience with intraoperative DIR imaging in 30 such patients.

A novel, long-wave (8–10 µm), narrow-band, focal-plane-array infrared photodetector was incorporated into a camera system with a temperature resolution of 0.006°C, providing 65,000 pixels/frame at a data acquisition rate of 200 frames/second. Intraoperative imaging of patients was performed before and after surgery. Infrared data were subsequently analyzed by examining absolute differences in cortical temperatures, changes in temperature over time, and infrared intensities at varying physiological frequencies.

Dynamic infrared imaging was applied in a variety of neurosurgical cases. After resection of an arteriovenous malformation, there was postoperative hyperperfusion of the surrounding brain parenchyma, which was consistent with a loss of autoregulation. Bypass patency and increased perfusion of adjacent brain were documented during two of three extracranial—intracranial bypasses. In seven of nine patients with epilepsy the results of DIR imaging corresponded to seizure foci that had been electrocorticographically mapped preoperatively. Dynamic infrared imaging demonstrated the functional cortex in four of nine patients undergoing awake resection and cortical stimulation. Finally, DIR imaging exhibited the distinct thermal footprints of 14 of 16 brain tumors.

Dynamic infrared imaging may prove to be a powerful adjunctive intraoperative diagnostic tool in the neurosurgical imaging armamentarium. Real-time assessment of cerebral vessel patency and cerebral perfusion are the most direct applications of this technology. Uses of this imaging modality in the localization of epileptic foci, identification of functional cortex during awake craniotomy, and determination of tumor border and intraoperative brain shift are avenues of inquiry that require further investigation.

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Aaron A. Cohen-Gadol, Brian G. Wilhelmi, Frederic Collignon, J. Bradley White, Jeffrey W. Britton, Denise M. Cambier, Teresa J. H. Christianson, W. Richard Marsh, Fredric B. Meyer, and Gregory D. Cascino

Object

The authors reviewed the long-term outcome of focal resection in a large group of patients who had intractable partial nonlesional epilepsy, including mesial temporal lobe sclerosis (MTS), and who were treated consecutively at a single institution. The goal of this study was to evaluate the long-term efficacy of epilepsy surgery and the preoperative factors associated with seizure outcome.

Methods

This retrospective analysis included 399 consecutive patients who underwent epilepsy surgery at Mayo Clinic in Rochester, Minnesota, between 1988 and 1996. The mean age of the patients at surgery was 32 ± 12 years (range 3–69 years), and the mean age at seizure onset was 12 ± 11 years (range 0–55 years). There were 214 female (54%) and 185 male (46%) patients. The mean duration of epilepsy was 20 ±12 years (range 1–56 years). The preceding values are given as the mean ± standard deviation.

Of the 399 patients, 237 (59%) had a history of complex partial seizures, 119 (30%) had generalized seizures, 26 (6%) had simple partial seizures, and 17 (4%) had experienced a combination of these. Preoperative evaluation included a routine and video-electroencephalography recordings, magnetic resonance imaging of the head according to the seizure protocol, neuropsychological testing, and a sodium amobarbital study. Patients with an undefined epileptogenic focus and discordant preoperative studies underwent an intracranial study. The mean duration of follow up was 6.2 ± 4.5 years (range 0.6–15.7 years). Seizure outcome was categorized based on the modified Engel classification. Time-to-event analysis was performed using Kaplan–Meier curves and Cox regression models to evaluate the risk factors associated with outcomes.

Among these patients, 372 (93%) underwent temporal and 27 (7%) had extratemporal resection of their epileptogenic focus. Histopathological examination of the resected specimens revealed MTS in 113 patients (28%), gliosis in 237 (59%), and normal findings in 49 (12%). Based on the Kaplan–Meier analysis, the probability of an Engel Class I outcome (seizure free, auras, or seizures related only to medication withdrawal) for the overall patient group was 81% (95% confidence interval [CI] 77–85%) at 6 months, 78% (CI 74–82%) at 1 year, 76% (CI 72–80%) at 2 years, 74% (CI 69–78%) at 5 years, and 72% (CI 67–77%) at 10 years postoperatively. The rate of Class I outcomes remained 72% for 73 patients with more than 10 years of follow up. If a patient was in Class I at 1 year postoperatively, the probability of seizure remission at 10 years postoperatively was 92% (95% CI 89–96%); almost all seizures occurred during the 1st year after surgery. Factors predictive of poor outcome from surgery were normal pathological findings in resected tissue (p = 0.038), male sex (p = 0.035), previous surgery (p < 0.001), and an extratemporal origin of seizures (p < 0.001).

Conclusions

The response to epilepsy surgery during the 1st follow-up year is a reliable indicator of the long-term Engel Class I postoperative outcome. This finding may have important implications for patient counseling and postoperative discontinuation of anticonvulsant medications.

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Nicholas M. Wetjen, W. Richard Marsh, Fredric B. Meyer, Gregory D. Cascino, Elson So, Jeffrey W. Britton, S. Matthew Stead, and Gregory A. Worrell

Object

Patients with normal MR imaging (nonlesional) findings and medically refractory extratemporal epilepsy make up a disproportionate number of nonexcellent outcomes after epilepsy surgery. In this paper, the authors investigated the usefulness of intracranial electroencephalography (iEEG) in the identification of surgical candidates.

Methods

Between 1992 and 2002, 51 consecutive patients with normal MR imaging findings and extratemporal epilepsy underwent intracranial electrode monitoring. The implantation of intracranial electrodes was determined by seizure semiology, interictal and ictal scalp EEG, SPECT, and in some patients PET studies. The demographics of patients at the time of surgery, lobar localization of electrode implantation, duration of follow-up, and Engel outcome score were abstracted from the Mayo Rochester Epilepsy Surgery Database. A blinded independent review of the iEEG records was conducted for this study.

Results

Thirty-one (61%) of the 51 patients who underwent iEEG ultimately underwent resection for their epilepsy. For 28 (90.3%) of the 31 patients who had epilepsy surgery, adequate information regarding follow-up (> 1 year), seizure frequency, and iEEG recordings was available. Twenty-six (92.9%) of 28 patients had frontal lobe resections, and 2 had parietal lobe resections. The most common iEEG pattern at seizure onset in the surgically treated group was a focal high-frequency discharge (in 15 [53.6%] of 28 patients). Ten (35.7%) of the 28 surgically treated patients were seizure free. Fourteen (50%) had Engel Class I outcomes, and overall, 17 (60.7%) had significant improvement (Engel Class I and IIAB with ≥80% seizure reduction). Focal high-frequency oscillation at seizure onset was associated with Engel Class I surgical outcome (12 [85.7%] of 14 patients, p = 0.02), and it was uncommon in the nonexcellent outcome group (3 [21.4%] of 14 patients).

Conclusions

A focal high-frequency oscillation (> 20 Hz) at seizure onset on iEEG may identify patients with nonlesional extratemporal epilepsy who are likely to have an Engel Class I outcome after epilepsy surgery. The prospect of excellent outcome in nonlesional extratemporal lobe epilepsy prior to intracranial monitoring is poor (14 [27.5%] of 51 patients). However, iEEG can further stratify patients and help identify those with a greater likelihood of Engel Class I outcome after surgery.

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Hirotaka Hasegawa, Jamie J. Van Gompel, W. Richard Marsh, Robert E. Wharen Jr., Richard S. Zimmerman, David B. Burkholder, Brian N. Lundstrom, Jeffrey W. Britton, and Fredric B. Meyer

OBJECTIVE

Surgical site infection (SSI) is a rare but significant complication after vagus nerve stimulator (VNS) placement. Treatment options range from antibiotic therapy alone to hardware removal. The optimal therapeutic strategy remains open to debate. Therefore, the authors conducted this retrospective multicenter analysis to provide insight into the optimal management of VNS-related SSI (VNS-SSI).

METHODS

Under institutional review board approval and utilizing an institutional database with 641 patients who had undergone 808 VNS-related placement surgeries and 31 patients who had undergone VNS-related hardware removal surgeries, the authors retrospectively analyzed VNS-SSI.

RESULTS

Sixteen cases of VNS-SSI were identified; 12 of them had undergone the original VNS placement procedure at the authors’ institutions. Thus, the incidence of VNS-SSI was calculated as 1.5%. The mean (± standard deviation) time from the most recent VNS-related surgeries to infection was 42 (± 27) days. Methicillin-sensitive staphylococcus was the usual causative bacteria (58%). Initial treatments included antibiotics with or without nonsurgical procedures (n = 6), nonremoval open surgeries for irrigation (n = 3), generator removal (n = 3), and total or near-total removal of hardware (n = 4). Although 2 patients were successfully treated with antibiotics alone or combined with generator removal, removal of both the generator and leads was eventually required in 14 patients. Mild swallowing difficulties and hoarseness occurred in 2 patients with eventual resolution.

CONCLUSIONS

Removal of the VNS including electrode leads combined with antibiotic administration is the definitive treatment but has a risk of causing dysphagia. If the surgeon finds dense scarring around the vagus nerve, the prudent approach is to snip the electrode close to the nerve as opposed to attempting to unwind the lead completely.

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Sanjeet S. Grewal, Mohammed Ali Alvi, William J. Perkins, Gregory D. Cascino, Jeffrey W. Britton, David B. Burkholder, Elson So, Cheolsu Shin, Richard W. Marsh, Fredric B. Meyer, Gregory A. Worrell, and Jamie J. Van Gompel

OBJECTIVE

Almost 30% of the patients with suspected temporal lobe epilepsy (TLE) have normal results on MRI. Success rates for resection of MRI-negative TLE are less favorable, ranging from 36% to 76%. Herein the authors describe the impact of intraoperative electrocorticography (ECoG) augmented by opioid activation and its effect on postoperative seizure outcome.

METHODS

Adult and pediatric patients with medically resistant MRI-negative TLE who underwent standardized ECoG at the time of their elective anterior temporal lobectomy (ATL) with amygdalohippocampectomy between 1990 and 2016 were included in this study. Seizure recurrence comprised the primary outcome of interest and was assessed using Kaplan-Meier and multivariable Cox regression analysis plots based on distribution of interictal epileptiform discharges (IEDs) recorded on scalp electroencephalography, baseline and opioid-induced IEDs on ECoG, and extent of resection.

RESULTS

Of the 1144 ATLs performed at the authors’ institution between 1990 and 2016, 127 (11.1%) patients (81 females) with MRI-negative TLE were eligible for this study. Patients with complete resection of tissue generating IED recorded on intraoperative ECoG were less likely to have seizure recurrence compared to those with incomplete resection on univariate analysis (p < 0.05). No difference was found in seizure recurrence between patients with bilateral independent IEDs and unilateral IEDs (p = 0.15), presence or absence of opioid-induced epileptiform activation (p = 0.61), or completeness of resection of tissue with opioid-induced IEDs on intraoperative ECoG (p = 0.41).

CONCLUSIONS

The authors found that incomplete resection of IED-generating tissue on intraoperative ECoG was associated with an increased chance of seizure recurrence. However, they found that induction of epileptiform activity with intraoperative opioid activation did not provide useful intraoperative data predictive of improving operative results for temporal lobectomy in MRI-negative epilepsy.

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Panagiotis Kerezoudis, Sanjeet S. Grewal, Matthew Stead, Brian Nils Lundstrom, Jeffrey W. Britton, Cheolsu Shin, Gregory D. Cascino, Benjamin H. Brinkmann, Gregory A. Worrell, and Jamie J. Van Gompel

OBJECTIVE

Epilepsy surgery is effective for lesional epilepsy, but it can be associated with significant morbidity when seizures originate from eloquent cortex that is resected. Here, the objective was to describe chronic subthreshold cortical stimulation and evaluate its early surgical safety profile in adult patients with epilepsy originating from seizure foci in cortex that is not amenable to resection.

METHODS

Adult patients with focal drug-resistant epilepsy underwent intracranial electroencephalography monitoring for evaluation of resection. Those with seizure foci in eloquent cortex were not candidates for resection and were offered a short therapeutic trial of continuous subthreshold cortical stimulation via intracranial monitoring electrodes. After a successful trial, electrodes were explanted and permanent stimulation hardware was implanted.

RESULTS

Ten patients (6 males) who underwent chronic subthreshold cortical stimulation between 2014 and 2016 were included. Based on radiographic imaging, intracranial pathologies included cortical dysplasia (n = 3), encephalomalacia (n = 3), cortical tubers (n = 1), Rasmussen encephalitis (n = 1), and linear migrational anomaly (n = 1). The duration of intracranial monitoring ranged from 3 to 20 days. All patients experienced an uneventful postoperative course and were discharged home with a median length of stay of 10 days. No postoperative surgical complications developed (median follow-up length 7.7 months). Seizure severity and seizure frequency improved in all patients.

CONCLUSIONS

The authors’ institutional experience with this small group shows that chronic subthreshold cortical stimulation can be safely and effectively performed in appropriately selected patients without postoperative complications. Future investigation will provide further insight to recently published results regarding mechanism and efficacy of this novel and promising intervention.