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Robert T. Buckley, Anthony C. Wang, John W. Miller, Edward J. Novotny and Jeffrey G. Ojemann

OBJECTIVE

Laser ablation is a novel, minimally invasive procedure that utilizes MRI-guided thermal energy to treat epileptogenic and other brain lesions. In addition to treatment of mesial temporal lobe epilepsy, laser ablation is increasingly being used to target deep or inoperable lesions, including hypothalamic hamartoma (HH), subependymal giant cell astrocytoma (SEGA), and exophytic intrinsic hypothalamic/third ventricular tumors. The authors reviewed their early institutional experience with these patients to characterize clinical outcomes in patients undergoing this procedure.

METHODS

A retrospective cohort (n = 12) of patients undergoing laser ablation at a single institution was identified, and clinical and radiographic records were reviewed.

RESULTS

Laser ablation was successfully performed in all patients. No permanent neurological or endocrine complications occurred; 2 (17%) patients developed acute obstructive hydrocephalus or shunt malfunction following treatment. Laser ablation of HH resulted in seizure freedom (Engel Class I) in 67%, with the remaining patients having a clinically significant reduction in seizure frequency of greater than 90% compared with preoperative baseline (Engel Class IIB). Treatment of SEGAs resulted in durable clinical and radiographic tumor control in 2 of 3 cases, with one patient receiving adjuvant everolimus and the other receiving no additional therapy. Palliative ablation of hypothalamic/third ventricular tumors resulted in partial tumor control in 1 of 3 patients.

CONCLUSIONS

Early experience suggests that laser ablation is a generally safe, durable, and effective treatment for patients harboring HHs. It also appears effective for local control of SEGAs, especially in combination therapy with everolimus. Its use as a palliative treatment for intrinsic hypothalamic/deep intraventricular tumors was less successful and associated with a higher risk of serious complications. Additional experience and long-term follow-up will be beneficial in further characterizing the effectiveness and risk profile of laser ablation in treating these lesions in comparison with conventional resective surgery or stereotactic radiosurgery.

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Carter D. Wray, Sharon S. McDaniel, Russell P. Saneto, Edward J. Novotny Jr. and Jeffrey G. Ojemann

Object

Intraoperative electrocorticography (ECoG) is commonly used to guide the extent of resection, especially in lesion-associated intractable epilepsy. Interictal epileptiform discharges on postresective ECoG (post-ECoG) have been predictive of seizure recurrence in some studies, particularly in adults undergoing medial temporal lobectomy, frontal lesionectomy, or low-grade glioma resection. The predictive value of postresective discharges in pediatric epilepsy surgery has not been extensively studied.

Methods

The authors retrospectively examined the charts of all 52 pediatric patients who had undergone surgery with post-ECoG and had more than 1 year of follow-up between October 1, 2003, and October 1, 2009.

Results

Of the 52 pediatric patients, 37 patients showed residual discharges at the end of their resection and 73% of these patients were seizure free, whereas 15 patients had no residual discharges and 60% of them were seizure-free, which was not significantly different (p = 0.36, chi-square).

Conclusions

Electrocorticography-guided surgery was associated with excellent postsurgical outcome. Although this sample size was too small to detect a subtle difference, absence of epileptiform discharges on post-ECoG does not appear to predict seizure freedom in all pediatric patients referred for epilepsy surgery. Future studies with larger study samples would be necessary to confirm this finding and determine whether post-ECoG may be useful in some subsets of pediatric epilepsy surgery candidates.

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Kaitlyn Casimo, Fabio Grassia, Sandra L. Poliachik, Edward Novotny, Andrew Poliakov and Jeffrey G. Ojemann

Prior studies of functional connectivity following callosotomy have disagreed in the observed effects on interhemispheric functional connectivity. These connectivity studies, in multiple electrophysiological methods and functional MRI, have found conflicting reductions in connectivity or patterns resembling typical individuals. The authors examined a case of partial anterior corpus callosum connection, where pairs of bilateral electrocorticographic electrodes had been placed over homologous regions in the left and right hemispheres. They sorted electrode pairs by whether their direct corpus callosum connection had been disconnected or preserved using diffusion tensor imaging and native anatomical MRI, and they estimated functional connectivity between pairs of electrodes over homologous regions using phase-locking value. They found no significant differences in any frequency band between pairs of electrodes that had their corpus callosum connection disconnected and those that had an intact connection. The authors’ results may imply that the corpus callosum is not an obligatory mediator of connectivity between homologous sites in opposite hemispheres. This interhemispheric synchronization may also be linked to disruption of seizure activity.

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Hillary A. Shurtleff, Dwight Barry, Timothy Firman, Molly H. Warner, Rafael L. Aguilar-Estrada, Russell P. Saneto, John D. Kuratani, Richard G. Ellenbogen, Edward J. Novotny and Jeffrey G. Ojemann

OBJECT

Outcomes of focal resection in young children with early-onset epilepsy are varied in the literature due to study differences. In this paper, the authors sought to define the effect of focal resection in a small homogeneous sample of children who were otherwise cognitively intact, but who required early surgical treatment. Preservation of and age-appropriate development of intelligence following focal resection was hypothesized.

METHODS

Cognitive outcome after focal resection was retrospectively reviewed for 15 cognitively intact children who were operated on at the ages of 2–6 years for lesion-related, early-onset epilepsy. Intelligence was tested prior to and after surgery. Effect sizes and confidence intervals for means and standard deviations were used to infer changes and differences in intelligence between 1) groups (pre vs post), 2) left versus right hemisphere resections, and 3) short versus long duration of seizures prior to resection.

RESULTS

No group changes from baseline occurred in Full Scale, verbal, or nonverbal IQ. No change from baseline intelligence occurred in children who underwent left or right hemisphere surgery, including no group effect on verbal scores following surgery in the dominant hemisphere. Patients with seizure durations of less than 6 months prior to resection showed improvement from their presurgical baseline in contrast to those with seizure duration of greater than 6 months prior to surgery, particularly in Wechsler Full Scale IQ and nonverbal intelligence.

CONCLUSIONS

This study suggests that surgical treatment of focal seizures in cognitively intact preschool children is likely to result in seizure remediation, antiepileptic drug discontinuation, and no significant decrement in intelligence. The latter finding is particularly significant in light of the longstanding concern associated with performing resections in the language-dominant hemisphere. Importantly, shorter seizure duration prior to resection can result in improved cognitive outcome, suggesting that surgery for this population should occur sooner to help improve intelligence outcomes.

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Carter D. Wray, Diana L. Kraemer, Tong Yang, Sandra L. Poliachik, Andrew L. Ko, Andrew Poliakov, Adam O. Hebb, Edward J. Novotny and Jeffrey G. Ojemann

The presurgical evaluation of patients with epilepsy often requires an intracranial study in which both subdural grid electrodes and depth electrodes are needed. Performing a craniotomy for grid placement with a stereotactic frame in place can be problematic, especially in young children, leading some surgeons to consider frameless stereotaxy for such surgery. The authors report on the use of a system that uses electromagnetic impulses to track the tip of the depth electrode. Ten pediatric patients with medically refractory focal lobar epilepsy required placement of both subdural grid and intraparenchymal depth electrodes to map seizure onset. Presurgical frameless stereotaxic targeting was performed using a commercially available electromagnetic image-guided system. Freehand depth electrode placement was then performed with intraoperative guidance using an electromagnetic system that provided imaging of the tip of the electrode, something that has not been possible using visually or sonically based systems. Accuracy of placement of depth electrodes within the deep structures of interest was confirmed postoperatively using CT and CT/MR imaging fusion. Depth electrodes were appropriately placed in all patients. Electromagnetic-tracking–based stereotactic targeting improves the accuracy of freehand placement of depth electrodes in patients with medically refractory epilepsy. The ability to track the electrode tip, rather than the electrode tail, is a major feature that enhances accuracy. Additional advantages of electromagnetic frameless guidance are discussed.

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Fabio Grassia, Andrew V. Poliakov, Sandra L. Poliachik, Kaitlyn Casimo, Seth D. Friedman, Hillary Shurtleff, Carlo Giussani, Edward J. Novotny Jr., Jeffrey G. Ojemann and Jason S. Hauptman

OBJECTIVE

Functional connectivity magnetic resonance imaging (fcMRI) is a form of fMRI that allows for analysis of blood oxygen level–dependent signal changes within a task-free, resting paradigm. This technique has been shown to have efficacy in evaluating network connectivity changes with epilepsy. Presurgical data from patients with unilateral temporal lobe epilepsy were evaluated using the fcMRI technique to define connectivity changes within and between the diseased and healthy temporal lobes using a within-subjects design.

METHODS

Using presurgical fcMRI data from pediatric patients with unilateral temporal lobe epilepsy, the authors performed seed-based analyses within the diseased and healthy temporal lobes. Connectivity within and between temporal lobe seeds was measured and compared.

RESULTS

In the cohort studied, local ipsilateral temporal lobe connectivity was significantly increased on the diseased side compared to the healthy temporal lobe. Connectivity of the diseased side to the healthy side, on the other hand, was significantly reduced when compared to connectivity of the healthy side to the diseased temporal lobe. A statistically significant regression was observed when comparing the changes in local ipsilateral temporal lobe connectivity to the changes in inter–temporal lobe connectivity. A statistically significant difference was also noted in ipsilateral connectivity changes between patients with and those without mesial temporal sclerosis.

CONCLUSIONS

Using fcMRI, significant changes in ipsilateral temporal lobe and inter–temporal lobe connectivity can be appreciated in unilateral temporal lobe epilepsy. Furthermore, fcMRI may have a role in the presurgical evaluation of patients with intractable temporal lobe epilepsy.

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Peter C. Gerszten, Edward A. Monaco III, Mubina Quader, Josef Novotny Jr., Jong Oh Kim, John C. Flickinger and M. Saiful Huq

Object

Cone beam computed tomography (CBCT) image guidance technology has been adopted for use in spine radiosurgery. There is concern regarding the ability to safely and accurately perform spine radiosurgery without the use of implanted fiducials for image guidance in postsurgical cases in which titanium instrumentation and/or methylmethacrylate (MMA) has been implanted. In this study the authors prospectively evaluated the accuracy of the patient setup for spine radiosurgery by using CBCT image guidance in the context of orthopedic hardware at the site of disease.

Methods

The positioning deviations of 31 single-fraction spine radiosurgery treatments in patients with spinal implants were prospectively evaluated using the Elekta Synergy S 6-MV linear accelerator with a beam modulator and CBCT image guidance combined with a robotic couch that allows positioning correction in 3 translational and 3 rotational directions. To measure patient movement, 3 quality-assurance CBCT studies were performed and recorded: before, halfway through, and after radiosurgical treatment. The positioning data and fused images of planning CTs and CBCTs from the treatments were analyzed to determine intrafractional patient movements. From each of 3 CBCTs, 3 translational and 3 rotational coordinates were obtained.

Results

The prescribed dose to the gross tumor volume for the cohort was 12–18 Gy (mean 14 Gy) utilizing 9–14 coplanar intensity-modulated radiation therapy (IMRT) beams (mean 10 beams). At the halfway point of the radiosurgery, the translational variations and standard deviations were 0.6 ± 0.6, 0.4 ± 0.4, and 0.5 ± 0.5 mm in the lateral (X), longitudinal (Y), and anteroposterior (Z) directions, respectively. The magnitude of the 3D vector (X,Y,Z) was 1.1 ± 0.7 mm. Similarly, the variations immediately after treatment were 0.5 ± 0.3, 0.4 ± 0.4, and 0.5 ± 0.6 mm along the X, Y, and Z directions, respectively. The 3D vector was 1.0 ± 0.6 mm. The mean rotational angles were 0.3 ± 0.4, 0.5 ± 0.6, and 0.3 ± 0.4° along yaw, roll, and pitch, respectively, at the halfway point and 0.3 ± 0.4, 0.6 ± 0.6, and 0.4 ± 0.5° immediately after treatment.

Conclusions

Cone beam CT image guidance used for patient setup for spine radiosurgery was highly accurate despite the presence of spinal instrumentation and/or MMA at the level of the target volume. The presence of such spinal implants does not preclude safe treatment via spine radiosurgery in these patients.

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Carter D. Wray, Tim M. Blakely, Sandra L. Poliachik, Andrew Poliakov, Sharon S. McDaniel, Edward J. Novotny, Kai J. Miller and Jeffrey G. Ojemann

Object

The gold-standard method for determining cortical functional organization in the context of neurosurgical intervention is electrical cortical stimulation (ECS), which disrupts normal cortical function to evoke movement. This technique is imprecise, however, as motor responses are not limited to the precentral gyrus. Electrical cortical stimulation also can trigger seizures, is not always tolerated, and is often unsuccessful, especially in children. Alternatively, endogenous motor and sensory signals can be mapped by somatosensory evoked potentials (SSEPs), functional MRI (fMRI), and electrocorticography of high gamma (70–150 Hz) signal power, which reflect normal cortical function. The authors evaluated whether these 4 modalities of mapping sensorimotor function in children produce concurrent results.

Methods

The authors retrospectively examined the charts of all patients who underwent epilepsy surgery at Seattle Children's Hospital between July 20, 1999, and July 1, 2011, and they included all patients in whom the primary motor or somatosensory cortex was localized via 2 or more of the following tests: ECS, SSEP, fMRI, or high gamma electrocorticography (hgECoG).

Results

Inclusion criteria were met by 50 patients, whose mean age at operation was 10.6 years. The youngest patient who underwent hgECoG mapping was 2 years and 10 months old, which is younger than any patient reported on in the literature. The authors localized the putative sensorimotor cortex most often with hgECoG, followed by SSEP and fMRI; ECS was most likely to fail to localize the sensorimotor cortex.

Conclusions

Electrical cortical stimulation, SSEP, fMRI, and hgECoG generally produced concordant localization of motor and sensory function in children. When attempting to localize the sensorimotor cortex in children, hgECoG was more likely to produce results, was faster, safer, and did not require cooperation. The hgECoG maps in pediatric patients are similar to those in adult patients published in the literature. The sensorimotor cortex can be mapped by hgECoG and fMRI in children younger than 3 years old to localize cortical function.

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Sandra L. Poliachik, Andrew V. Poliakov, Laura A. Jansen, Sharon S. McDaniel, Carter D. Wray, John Kuratani, Russell P. Saneto, Jeffrey G. Ojemann and Edward J. Novotny Jr

Object

Imaging-guided surgery (IGS) systems are widely used in neurosurgical practice. During epilepsy surgery, the authors routinely use IGS landmarks to localize intracranial electrodes and/or specific brain regions. The authors have developed a technique to coregister these landmarks with pre- and postoperative scans and the Montreal Neurological Institute (MNI) standard space brain MRI to allow 1) localization and identification of tissue anatomy; and 2) identification of Brodmann areas (BAs) of the tissue resected during epilepsy surgery. Tracking tissue in this fashion allows for better correlation of patient outcome to clinical factors, functional neuroimaging findings, and pathological characteristics and molecular studies of resected tissue.

Methods

Tissue samples were collected in 21 patients. Coordinates from intraoperative tissue localization were downloaded from the IGS system and transformed into patient space, as defined by preoperative high-resolution T1-weighted MRI volume. Tissue landmarks in patient space were then transformed into MNI standard space for identification of the BAs of the tissue samples.

Results

Anatomical locations of resected tissue were identified from the intraoperative resection landmarks. The BAs were identified for 17 of the 21 patients. The remaining patients had abnormal brain anatomy that could not be meaningfully coregistered with the MNI standard brain without causing extensive distortion.

Conclusions

This coregistration and landmark tracking technique allows localization of tissue that is resected from patients with epilepsy and identification of the BAs for each resected region. The ability to perform tissue localization allows investigators to relate preoperative, intraoperative, and postoperative functional and anatomical brain imaging to better understand patient outcomes, improve patient safety, and aid in research.

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Kurt E. Weaver, Andrew Poliakov, Edward J. Novotny, Jared D. Olson, Thomas J. Grabowski and Jeffrey G. Ojemann

OBJECTIVE

The acquisition and refinement of cognitive and behavioral skills during development is associated with the maturation of various brain oscillatory activities. Most developmental investigations have identified distinct patterns of low-frequency electrophysiological activity that are characteristic of various behavioral milestones. In this investigation, the authors focused on the cross-sectional developmental properties of high-frequency spectral power from the brain’s default mode network (DMN) during goal-directed behavior.

METHODS

The authors contrasted regionally specific, time-evolving high gamma power (HGP) in the lateral DMN cortex between 3 young children (age range 3–6 years) and 3 adults by use of electrocorticography (ECoG) recordings over the left perisylvian cortex during a picture-naming task.

RESULTS

Across all participants, a nearly identical and consistent response suppression of HGP, which is a functional signature of the DMN, was observed during task performance recordings acquired from ECoG electrodes placed over the lateral DMN cortex. This finding provides evidence of relatively early maturation of the DMN. Furthermore, only HGP relative to evoked alpha and beta band power showed this level of consistency across all participants.

CONCLUSIONS

Regionally specific, task-evoked suppression of the high-frequency components of the cortical power spectrum is established early in brain development, and this response may reflect the early maturation of specific cognitive and/or computational mechanisms.