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Victoria L. Morgan, Baxter P. Rogers, Hernán F. J. González, Sarah E. Goodale and Dario J. Englot

OBJECTIVE

Seizure outcome after mesial temporal lobe epilepsy (mTLE) surgery is complex and diverse, even across patients with homogeneous presurgical clinical profiles. The authors hypothesized that this is due in part to variations in network connectivity across the brain before and after surgery. Although presurgical network connectivity has been previously characterized in these patients, the objective of this study was to characterize presurgical to postsurgical functional network connectivity changes across the brain after mTLE surgery.

METHODS

Twenty patients with drug-refractory unilateral mTLE (5 left side, 10 female, age 39.3 ± 13.5 years) who underwent either selective amygdalohippocampectomy (n = 13) or temporal lobectomy (n = 7) were included in the study. Presurgical and postsurgical (36.6 ± 14.3 months after surgery) functional connectivity (FC) was measured with 3-T MRI and compared with findings in age-matched healthy controls (n = 44, 21 female, age 39.3 ± 14.3 years). Postsurgical connectivity changes were then related to seizure outcome, type of surgery, and presurgical disease parameters.

RESULTS

The results demonstrated significant decreases of FC from control group values across the brain after surgery that were not present before surgery, including many contralateral hippocampal connections distal to the surgical site. Postsurgical impairment of contralateral precuneus to ipsilateral occipital connectivity was associated with seizure recurrence. Presurgical impairment of the contralateral precuneus to contralateral temporal lobe connectivity was associated with those who underwent selective amygdalohippocampectomy compared to those who had temporal lobectomy. Finally, changes in thalamic connectivity after surgery were linearly related to duration of epilepsy and frequency of consciousness-impairing seizures prior to surgery.

CONCLUSIONS

The widespread contralateral hippocampal FC changes after surgery may be a reflection of an ongoing epileptogenic progression that has been altered by the surgery, rather than a direct result of the surgery itself. This network evolution may contribute to long-term seizure outcome. Therefore, the combination of presurgical network mapping with the understanding of the dynamic effects of surgery on the networks may ultimately be used to create predictors of the likelihood of long-term seizure recurrence in individual patients after mTLE surgery.

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Victoria L. Morgan, Baxter P. Rogers, Adam W. Anderson, Bennett A. Landman and Dario J. Englot

OBJECTIVE

The objectives of this study were to identify functional and structural network properties that are associated with early versus long-term seizure outcomes after mesial temporal lobe epilepsy (mTLE) surgery and to determine how these compare to current clinically used methods for seizure outcome prediction.

METHODS

In this case-control study, 26 presurgical mTLE patients and 44 healthy controls were enrolled to undergo 3-T MRI for functional and structural connectivity mapping across an 8-region network of mTLE seizure propagation, including the hippocampus (left and right), insula (left and right), thalamus (left and right), one midline precuneus, and one midline mid-cingulate. Seizure outcome was assessed annually for up to 3 years. Network properties and current outcome prediction methods related to early and long-term seizure outcome were investigated.

RESULTS

A network model was previously identified across 8 patients with seizure-free mTLE. Results confirmed that whole-network propagation connectivity patterns inconsistent with the mTLE model predict early surgical failure. In those patients with networks consistent with the mTLE network, specific bilateral within-network hippocampal to precuneus impairment (rather than unilateral impairment ipsilateral to the seizure focus) was associated with mild seizure recurrence. No currently used clinical variables offered the same ability to predict long-term outcome.

CONCLUSIONS

It is known that there are important clinical differences between early surgical failure that lead to frequent disabling seizures and late recurrence of less frequent mild seizures. This study demonstrated that divergent network connectivity variability, whole-network versus within-network properties, were uniquely associated with these disparate outcomes.

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Bornali Kundu, Andrea A. Brock, Dario J. Englot, Christopher R. Butson and John D. Rolston

Traumatic brain injury (TBI) is a looming epidemic, growing most rapidly in the elderly population. Some of the most devastating sequelae of TBI are related to depressed levels of consciousness (e.g., coma, minimally conscious state) or deficits in executive function. To date, pharmacological and rehabilitative therapies to treat these sequelae are limited. Deep brain stimulation (DBS) has been used to treat a number of pathologies, including Parkinson disease, essential tremor, and epilepsy. Animal and clinical research shows that targets addressing depressed levels of consciousness include components of the ascending reticular activating system and areas of the thalamus. Targets for improving executive function are more varied and include areas that modulate attention and memory, such as the frontal and prefrontal cortex, fornix, nucleus accumbens, internal capsule, thalamus, and some brainstem nuclei. The authors review the literature addressing the use of DBS to treat higher-order cognitive dysfunction and disorders of consciousness in TBI patients, while also offering suggestions on directions for future research.

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Alvin Y. Chan, John D. Rolston, Brian Lee, Sumeet Vadera and Dario J. Englot

OBJECTIVE

Corpus callosotomy is a palliative surgery for drug-resistant epilepsy that reduces the severity and frequency of generalized seizures by disconnecting the two cerebral hemispheres. Unlike with resection, seizure outcomes remain poorly understood. The authors systematically reviewed the literature and performed a meta-analysis to investigate rates and predictors of complete seizure freedom and freedom from drop attacks after corpus callosotomy.

METHODS

PubMed, Web of Science, and Scopus were queried for primary studies examining seizure outcomes after corpus callosotomy published over 30 years. Rates of complete seizure freedom or drop attack freedom were recorded. Variables showing a potential relationship to seizure outcome on preliminary analysis were subjected to formal meta-analysis.

RESULTS

The authors identified 1742 eligible patients from 58 included studies. Overall, the rates of complete seizure freedom and drop attack freedom after corpus callosotomy were 18.8% and 55.3%, respectively. Complete seizure freedom was significantly predicted by the presence of infantile spasms (OR 3.86, 95% CI 1.13–13.23), normal MRI findings (OR 4.63, 95% CI 1.75–12.25), and shorter epilepsy duration (OR 2.57, 95% CI 1.23–5.38). Freedom from drop attacks was predicted by complete over partial callosotomy (OR 2.90, 95% CI 1.07–7.83) and idiopathic over known epilepsy etiology (OR 2.84, 95% CI 1.35–5.99).

CONCLUSIONS

The authors report the first systematic review and meta-analysis of seizure outcomes in both adults and children after corpus callosotomy for epilepsy. Approximately one-half of patients become free from drop attacks, and one-fifth achieve complete seizure freedom after surgery. Some predictors of favorable outcome differ from those in resective epilepsy surgery.

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Michael C. Dewan, Robert Shults, Andrew T. Hale, Vishad Sukul, Dario J. Englot, Peter Konrad, Hong Yu, Joseph S. Neimat, William Rodriguez, Benoit M. Dawant, Srivatsan Pallavaram and Robert P. Naftel

OBJECTIVE

Stereotactic electroencephalography (SEEG) is being used with increasing frequency to interrogate subcortical, cortical, and multifocal epileptic foci. The authors describe a novel technique for SEEG in patients with suspected epileptic foci refractory to medical management.

METHODS

In the authors’ technique, standard epilepsy evaluation and neuroimaging are used to create a hypothesis-driven SEEG plan, which informs the 3D printing of a novel single-path, multiple-trajectory, omnidirectional platform. Following skull-anchor platform fixation, electrodes are sequentially inserted according to the preoperative plan. The authors describe their surgical experience and technique based on a review of all cases, adult and pediatric, in which patients underwent invasive epilepsy monitoring via SEEG during an 18-month period at Vanderbilt University Medical Center. Platform and anatomical variables influencing localization error were evaluated using multivariate linear regression.

RESULTS

Using this novel technology, 137 electrodes were inserted in 15 patients with focal epilepsy with favorable recording results and no clinical complications. The mean entry point localization error was 1.42 mm (SD 0.98 mm), and the mean target point localization error was 3.36 mm (SD 2.68 mm). Platform distance, electrode trajectory angle, and intracranial distance, but not skull thickness, were independently associated with localization error.

CONCLUSIONS

The multiple-trajectory, single-path, omnidirectional platform offers satisfactory accuracy and favorable clinical results, while avoiding cumbersome frames and prohibitive up-front costs associated with other SEEG technologies.

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Matthew J. Shepard and W. Jeffrey Elias

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Dario J. Englot, Stephen T. Magill, Seunggu J. Han, Edward F. Chang, Mitchel S. Berger and Michael W. McDermott

OBJECT

Meningioma is the most common benign intracranial tumor, and patients with supratentorial meningioma frequently suffer from seizures. The rates and predictors of seizures in patients with meningioma have been significantly under-studied, even in comparison with other brain tumor types. Improved strategies for the prediction, treatment, and prevention of seizures in patients with meningioma is an important goal, because tumor-related epilepsy significantly impacts patient quality of life.

METHODS

The authors performed a systematic review of PubMed for manuscripts published between January 1980 and September 2014, examining rates of pre- and postoperative seizures in supratentorial meningioma, and evaluating potential predictors of seizures with separate meta-analyses.

RESULTS

The authors identified 39 observational case series for inclusion in the study, but no controlled trials. Preoperative seizures were observed in 29.2% of 4709 patients with supratentorial meningioma, and were significantly predicted by male sex (OR 1.74, 95% CI 1.30–2.34); an absence of headache (OR 1.77, 95% CI 1.04–3.25); peritumoral edema (OR 7.48, 95% CI 6.13–9.47); and non–skull base location (OR 1.77, 95% CI 1.04–3.25). After surgery, seizure freedom was achieved in 69.3% of 703 patients with preoperative epilepsy, and was more than twice as likely in those without peritumoral edema, although an insufficient number of studies were available for formal meta-analysis of this association. Of 1085 individuals without preoperative epilepsy who underwent resection, new postoperative seizures were seen in 12.3% of patients. No difference in the rate of new postoperative seizures was observed with or without perioperative prophylactic anticonvulsants.

CONCLUSIONS

Seizures are common in supratentorial meningioma, particularly in tumors associated with brain edema, and seizure freedom is a critical treatment goal. Favorable seizure control can be achieved with resection, but evidence does not support routine use of prophylactic anticonvulsants in patients without seizures. Limitations associated with systematic review and meta-analysis should be considered when interpreting these results.

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John D. Rolston, Dario J. Englot, Arnau Benet, Jing Li, Soonmee Cha and Mitchel S. Berger

OBJECT

The dominant hemisphere frontal operculum may contain critical speech and language pathways, and due to these properties, patients with tumors of the opercular region may be at higher risk for postoperative speech dysfunction. However, the likelihood of incurring temporary or permanent language dysfunction is unknown.

METHODS

The authors retrospectively analyzed their cohort of patients with frontal gliomas to identify those tumors that predominantly involved the dominant frontal operculum. Each tumor was classified as involving the pars orbitalis, pars triangularis, pars opercularis, or a combination of some or all of these areas. The authors then identified and compared characteristics between those patients experiencing transient or permanent speech deficits, as opposed to those with no language dysfunction.

RESULTS

Forty-three patients were identified for inclusion in this analysis. Transient deficits occurred in 12 patients (27.9%), while 4 patients (9.8%) had persistent deficits involving language. Individuals with preoperative language deficits and patients with seizures characterized by speech dysfunction appear to be at the highest risk to develop a deficit (relative risks 3.09 and 1.75, respectively). No patient with a tumor involving the pars orbitalis experienced a persistent deficit.

CONCLUSIONS

Resection of gliomas is widely recognized as a critical element of improved outcome. Given the low rate of language morbidity reported in this group of patients, resection of gliomas within the dominant frontal operculum is well-tolerated with acceptable morbidity and, in this particular location, should not be a deterrent in the overall management of these tumors.