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Jarod L. Roland, Natalie Griffin, Carl D. Hacker, Ananth K. Vellimana, S. Hassan Akbari, Joshua S. Shimony, Matthew D. Smyth, Eric C. Leuthardt and David D. Limbrick Jr.

OBJECTIVE

Cerebral mapping for surgical planning and operative guidance is a challenging task in neurosurgery. Pediatric patients are often poor candidates for many modern mapping techniques because of inability to cooperate due to their immature age, cognitive deficits, or other factors. Resting-state functional MRI (rs-fMRI) is uniquely suited to benefit pediatric patients because it is inherently noninvasive and does not require task performance or significant cooperation. Recent advances in the field have made mapping cerebral networks possible on an individual basis for use in clinical decision making. The authors present their initial experience translating rs-fMRI into clinical practice for surgical planning in pediatric patients.

METHODS

The authors retrospectively reviewed cases in which the rs-fMRI analysis technique was used prior to craniotomy in pediatric patients undergoing surgery in their institution. Resting-state analysis was performed using a previously trained machine-learning algorithm for identification of resting-state networks on an individual basis. Network maps were uploaded to the clinical imaging and surgical navigation systems. Patient demographic and clinical characteristics, including need for sedation during imaging and use of task-based fMRI, were also recorded.

RESULTS

Twenty patients underwent rs-fMRI prior to craniotomy between December 2013 and June 2016. Their ages ranged from 1.9 to 18.4 years, and 12 were male. Five of the 20 patients also underwent task-based fMRI and one underwent awake craniotomy. Six patients required sedation to tolerate MRI acquisition, including resting-state sequences. Exemplar cases are presented including anatomical and resting-state functional imaging.

CONCLUSIONS

Resting-state fMRI is a rapidly advancing field of study allowing for whole brain analysis by a noninvasive modality. It is applicable to a wide range of patients and effective even under general anesthesia. The nature of resting-state analysis precludes any need for task cooperation. These features make rs-fMRI an ideal technology for cerebral mapping in pediatric neurosurgical patients. This review of the use of rs-fMRI mapping in an initial pediatric case series demonstrates the feasibility of utilizing this technique in pediatric neurosurgical patients. The preliminary experience presented here is a first step in translating this technique to a broader clinical practice.

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Gloria J. Guzmán Pérez-Carrillo, Christopher Owen, Katherine E. Schwetye, Spencer McFarlane, Ananth K. Vellimana, Soe Mar, Michelle M. Miller-Thomas, Joshua S. Shimony, Matthew D. Smyth and Tammie L. S. Benzinger

OBJECTIVE

Many patients with medically intractable epilepsy have mesial temporal sclerosis (MTS), which significantly affects their quality of life. The surgical excision of MTS lesions can result in marked improvement or even complete resolution of the epileptic episodes. Reliable radiological diagnosis of MTS is a clinical challenge. The purpose of this study was to evaluate the utility of volumetric mapping of the hippocampi for the identification of MTS in a case-controlled series of pediatric patients who underwent resection for medically refractory epilepsy, using pathology as a gold standard.

METHODS

A cohort of 57 pediatric patients who underwent resection for medically intractable epilepsy between 2005 and 2015 was evaluated. On pathological investigation, this group included 24 patients with MTS and 33 patients with non-MTS findings. Retrospective quantitative volumetric measurements of the hippocampi were acquired for 37 of these 57 patients. Two neuroradiologists with more than 10 years of experience who were blinded to the patients' MTS status performed the retrospective review of MR images. To produce the volumetric data, MR scans were parcellated and segmented using the FreeSurfer software suite. Hippocampal regions of interest were compared against an age-weighted local regression curve generated with data from the pediatric normal cohort. Standard deviations and percentiles of specific subjects were calculated. The sensitivity, specificity, positive predictive value (PPV), and negative predictive value (NPV) were determined for the original clinical read and the expert readers. Receiver operating characteristic curves were generated for the methods of classification to compare results from the readers with the authors' results, and an optimal threshold was determined. From that threshold the sensitivity, specificity, PPV, and NPV were calculated for the volumetric analysis.

RESULTS

With the use of quantitative volumetry, a sensitivity of 72%, a specificity of 95%, a PPV of 93%, an NPV of 78%, and an area under the curve of 0.84 were obtained using a percentage difference of normalized hippocampal volume. The resulting specificity (95%) and PPV (93%) are superior to the original clinical read and to Reader A and Reader B's findings (range for specificity 74%–86% and for PPV 64%–71%). The sensitivity (72%) and NPV (78%) are comparable to Reader A's findings (73% and 81%, respectively) and are better than those of the original clinical read and of Reader B (sensitivity 45% and 63% and NPV 71% and 70%, respectively).

CONCLUSIONS

Volumetric measurement of the hippocampi outperforms expert readers in specificity and PPV, and it demonstrates comparable to superior sensitivity and NPV. Volumetric measurements can complement anatomical imaging for the identification of MTS, much like a computer-aided detection tool would. The implementation of this approach in the daily clinical workflow could significantly improve diagnostic accuracy.

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Anna Jeong, Jennifer Strahle, Ananth K. Vellimana, David D. Limbrick Jr., Matthew D. Smyth and Mary Bertrand

OBJECTIVE

Electrical status epilepticus of sleep (ESES) is a rare electrographic pattern associated with global regression, which is often poorly responsive to traditional epilepsy treatments and can have a devastating and permanent neurocognitive outcome. The authors analyzed clinical, electroencephalographic, and neuropsychological outcomes in 9 patients with refractory ESES treated with functional hemispherotomy to illustrate the wide clinical spectrum associated with the disease and explore the role of hemispherotomy in its treatment.

METHODS

During the period between 2003 and 2015, 80 patients underwent hemispherotomy at the authors' institution. Video electroencephalography (EEG) reports were reviewed for ESES or continuous spikes and waves during sleep (CSWS). Patients with preoperative ESES (> 85% slow-wave sleep occupied by spike waves), a unilateral structural lesion amenable to surgery, and more than 6 months of follow-up data were included in the analysis. Clinical data, EEG recordings, neuropsychological testing, and parental and clinician reports were retrospectively reviewed.

RESULTS

Nine patients were eligible for study inclusion. Age at seizure onset ranged from birth to 4.2 years (mean 1.9 years), age at ESES diagnosis ranged from 3.5 to 8.8 years (mean 6.0 years), and age at hemispherotomy ranged from 3.7 to 11.5 years (mean 6.8 years). All patients had drug-resistant epilepsy. The duration of epilepsy prior to hemispherotomy ranged from 2.7 to 8.9 years (mean ± SD, 5.0 ± 2.2 years). Engel Class I seizure outcome was observed in all 9 children, with a mean follow-up of 3.0 years (range 0.5–6.1 years). Hemispherotomy terminated ESES in 6 of 6 patients with available postoperative sleep EEG. All children had preoperative neuropsychological impairments. Developmental regression was halted postoperatively, but none of the children returned to their original pre-ESES baseline. Four children demonstrated academic gains, 2 of whom transitioned to mainstream classes.

CONCLUSIONS

Children with drug-resistant ESES and a unilateral structural lesion should be evaluated for hemispherotomy as they may experience the cessation of seizures, termination of ESES, and improvement in neuropsychological status.

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Chad W. Washington, Colin P. Derdeyn, Rajat Dhar, Eric J. Arias, Michael R. Chicoine, DeWitte T. Cross, Ralph G. Dacey Jr., Byung Hee Han, Christopher J. Moran, Keith M. Rich, Ananth K. Vellimana and Gregory J. Zipfel

OBJECT

Studies show that phosphodiesterase-V (PDE-V) inhibition reduces cerebral vasospasm (CVS) and improves outcomes after experimental subarachnoid hemorrhage (SAH). This study was performed to investigate the safety and effect of sildenafil (an FDA-approved PDE-V inhibitor) on angiographic CVS in SAH patients.

METHODS

A2-phase, prospective, nonrandomized, human trial was implemented. Subarachnoid hemorrhage patients underwent angiography on Day 7 to assess for CVS. Those with CVS were given 10 mg of intravenous sildenafil in the first phase of the study and 30 mg in the second phase. In both, angiography was repeated 30 minutes after infusion. Safety was assessed by monitoring neurological examination findings and vital signs and for the development of adverse reactions. For angiographic assessment, in a blinded fashion, pre- and post-sildenafil images were graded as “improvement” or “no improvement” in CVS. Unblinded measurements were made between pre- and post-sildenafil angiograms.

RESULTS

Twelve patients received sildenafil; 5 patients received 10 mg and 7 received 30 mg. There were no adverse reactions. There was no adverse effect on heart rate or intracranial pressure. Sildenafil resulted in a transient decline in mean arterial pressure, an average of 17% with a return to baseline in an average of 18 minutes. Eight patients (67%) were found to have a positive angiographic response to sildenafil, 3 (60%) in the low-dose group and 5 (71%) in the high-dose group. The largest degree of vessel dilation was an average of 0.8 mm (range 0–2.1 mm). This corresponded to an average percentage increase in vessel diameter of 62% (range 0%–200%).

CONCLUSIONS

The results from this Phase I safety and proof-of-concept trial assessing the use of intravenous sildenafil in patients with CVS show that sildenafil is safe and well tolerated in the setting of SAH. Furthermore, the angiographic data suggest that sildenafil has a positive impact on human CVS.

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David J. Daniels, Ananth K. Vellimana, Gregory J. Zipfel and Giuseppe Lanzino

Object

In this paper the authors' goal was to review the clinical features and outcome of patients with intracranial dural arteriovenous fistulas (DAVFs) who presented with hemorrhage.

Methods

A retrospective study of 28 patients with DAVFs who presented with intracranial hemorrhage to 2 separate institutions was performed. The information reviewed included clinical presentation, location and size of hemorrhage, angiographic features, treatment, and clinical and radiologically documented outcomes. Clinical and radiological follow-up were available in 27 of 28 patients (mean follow-up 17 months).

Results

The vast majority of patients were male (86%), and the most common presenting symptom was sudden-onset headache. All DAVFs had cortical venous drainage, and about one-third were associated with a venous varix. The most common location was tentorial (75%). Treatment ranged from endovascular (71%), surgical (43%), Gamma Knife surgery (4%), or a combination of modalities. The majority of fistulas (75%) were completely obliterated, and most patients experienced excellent clinical outcome (71%, modified Rankin Scale score of 0 or 1). There were no complications in this series.

Conclusions

Case series, including the current one, suggest that the vast majority of patients who present with intracranial hemorrhage from a DAVF are male. The most common location for DAVFs presenting with hemorrhage is tentorial. Excellent outcomes are achieved with individualized treatment, which includes various therapeutic strategies alone or in combination. Despite the hemorrhagic presentation, almost two-thirds of patients experience a full recovery with no or minimal residual symptoms.

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Ananth K. Vellimana, Yasha Kadkhodayan, Keith M. Rich, DeWitte T. Cross III, Christopher J. Moran, Allyson R. Zazulia, Jin-Moo Lee, Michael R. Chicoine, Ralph G. Dacey Jr., Colin P. Derdeyn and Gregory J. Zipfel

Object

The aim of this study was to define the optimal treatment for patients with symptomatic intraluminal carotid artery thrombus (ICAT).

Methods

The authors performed a retrospective chart review of patients who had presented with symptomatic ICAT at their institution between 2001 and 2011.

Results

Twenty-four patients (16 males and 8 females) with ICAT presented with ischemic stroke (18 patients) or transient ischemic attack ([TIA], 6 patients). All were initially treated using anticoagulation with or without antiplatelet drugs. Eight of these patients had no or only mild carotid artery stenosis on initial angiography and were treated with medical management alone. The remaining 16 patients had moderate or severe carotid stenosis on initial angiography; of these, 10 underwent delayed revascularization (8 patients, carotid endarterectomy [CEA]; 2 patients, angioplasty and stenting), 2 refused revascularization, and 4 were treated with medical therapy alone. One patient had multiple TIAs despite medical therapy and eventually underwent CEA; the remaining 23 patients had no TIAs after treatment. No patient suffered ischemic or hemorrhagic stroke while on anticoagulation therapy, either during the perioperative period or in the long-term follow-up; 1 patient died of an unrelated condition. The mean follow-up was 16.4 months.

Conclusions

Results of this study suggest that initial anticoagulation for symptomatic ICAT leads to a low rate of recurrent ischemic events and that carotid revascularization, if indicated, can be safely performed in a delayed manner.

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Ananth K. Vellimana, Andria L. Ford, Jin-Moo Lee, Colin P. Derdeyn and Gregory J. Zipfel

Symptomatic intracranial arterial disease is associated with a high rate of recurrent ischemic events. The management of this condition is controversial, with some advocating medical therapy as a sole means of treatment and others recommending endovascular therapy in addition to best medical management. In rare cases, surgical intervention is considered. A thorough review of the available literature was performed, and treatment recommendations based on these data are provided.

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Daniel M. Sciubba, Joseph C. Noggle, Ananth K. Vellimana, Hassan Alosh, Matthew J. McGirt, Ziya L. Gokaslan and Jean-Paul Wolinsky

Object

Stabilization of the cervical spine can be challenging when instrumentation involves the axis. Fixation with C1–2 transarticular screws combined with posterior wiring and bone graft placement has yielded excellent fusion rates, but the technique is technically demanding and places the vertebral arteries (VAs) at risk. Placement of screws in the pars interarticularis of C-2 as described by Harms and Melcher has allowed rigid fixation with greater ease and theoretically decreases the risk to the VA. However, fluoroscopy is suggested to avoid penetration laterally, medially, and superiorly to avoid damage to the VA, spinal cord, and C1–2 joint, respectively. The authors describe how, after meticulous dissection of the C-2 pars interarticularis, such screws can be placed accurately and safely without the use of fluoroscopy.

Methods

Prospective follow-up was performed in 55 consecutive patients who underwent instrumented fusion of C-2 by a single surgeon. The causes of spinal instability and type and extent of instrumentation were documented. All patients underwent preoperative CT or MR imaging scans to determine the suitability of C-2 screw placement. Intraoperatively, screws were placed following dissection of the posterior pars interarticularis. Postoperative CT scans were performed to determine the extent of cortical breach. Patients underwent clinical follow-up, and complications were recorded as vascular or neurological. A CT-based grading system was created to characterize such breaches objectively by location and magnitude via percentage of screw diameter beyond the cortical edge (0 = none; I = < 25% of screw diameter; II = 26–50%; III = 51–75%; IV = 76–100%).

Results

One-hundred consecutive screws were placed in the pedicle of the axis by a single surgeon using external landmarks only. In 10 cases, only 1 screw was placed because of a preexisting VA anatomy or bone abnormality noted preoperatively. In no case was screw placement aborted because of complications noted during drilling. Early complications occurred in 2 patients and were limited to 1 wound infection and 1 transient C-2 radiculopathy. There were 15 total breaches (15%), 2 of which occurred in the same patient. Twelve breaches were lateral (80%), and 3 were superior (20%). There were no medial breaches. The magnitude of the breach was classified as I in 10 cases (66.7% of breaches), II in 3 cases (20% of breaches), III in 1 case (6.7%), and IV in 1 case (6.7%).

Conclusions

Free-hand placement of screws in the C-2 pedicle can be done safely and effectively without the use of intraoperative fluoroscopy or navigation when the pars interarticularis/pedicle is assessed preoperatively with CT or MR imaging and found to be suitable for screw placement. When breaches do occur, they are overwhelmingly lateral in location, breach < 50% of the screw diameter, and in the authors' experience, are not clinically significant.

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Daniel M. Sciubba, Joseph C. Noggle, Ananth K. Vellimana, James E. Conway, Ryan M. Kretzer, Donlin M. Long and Ira M. Garonzik

Object

Laminar fixation of the axis with crossing bilateral screws has been shown to provide rigid fixation with a theoretically decreased risk of vertebral artery damage compared with C1–2 transarticular screw fixation and C-2 pedicle screw fixation. Some studies, however, have shown restricted rigidity of such screws compared with C-2 pedicle screws, and others note that anatomical variability exists within the posterior elements of the axis that may have an impact on successful placement. To elucidate the clinical impact of such screws, the authors report their experience in placing C-2 laminar screws in adult patients over a 2-year period, with emphasis on clinical outcome and technical placement.

Methods

Sixteen adult patients with cervical instability underwent posterior cervical and cervicothoracic fusion procedures at our institution with constructs involving C-2 laminar screws. Eleven patients were men and 5 were women, and they ranged in age from 28 to 84 years (mean 57 years). The reasons for fusion were degenerative disease (9 patients) and treatment of trauma (7 patients). In 14 patients (87.5%) standard translaminar screws were placed, and in 2 (12.5%) an ipsilateral trajectory was used. All patients underwent preoperative radiological evaluation of the cervical spine, including computed tomography scanning with multiplanar reconstruction to assess the posterior anatomy of C-2. Anatomical restrictions for placement of standard translaminar screws included a deeply furrowed spinous process and/or an underdeveloped midline posterior ring of the axis. In these cases, screws were placed into the corresponding lamina from the ipsilateral side, allowing bilateral screws to be oriented in a more parallel, as opposed to perpendicular, plane. All patients were followed for > 2 years to record rates of fusion, instrumentation failure, and other complications.

Results

Thirty-two screws were placed without neurological or vascular complications. The mean follow-up duration was 27.3 months. Complications included 2 revisions, one for pseudarthrosis and the other for screw pullout, and 3 postoperative infections.

Conclusions

Placement of laminar screws into the axis from the standard crossing approach or via an ipsilateral trajectory may allow a safe, effective, and durable means of including the axis in posterior cervical and cervicothoracic fusion procedures.