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Jonathan J. Lee, David J. Segar, John F. Morrison, William M. Mangham, Shane Lee, and Wael F. Asaad

OBJECTIVE

Early radiographic findings in patients with traumatic brain injury (TBI) have been studied in hopes of better predicting injury severity and outcome. However, prior attempts have generally not considered the various types of intracranial hemorrhage in isolation and have typically not excluded patients with potentially confounding extracranial injuries. Therefore, the authors examined the associations of various radiographic findings with short-term outcome to assess the potential utility of these findings in future prognostic models.

METHODS

The authors retrospectively identified 1716 patients who had experienced TBI without major extracranial injuries, and categorized them into the following TBI subtypes: subdural hematoma (SDH), traumatic subarachnoid hemorrhage, intraparenchymal hemorrhage (which included intraventricular hemorrhage), and epidural hematoma. They specifically considered isolated forms of hemorrhage, in which only 1 subtype was present.

RESULTS

In general, the presence of an isolated SDH was more likely to result in worse outcomes than the presence of other isolated forms of traumatic intracranial hemorrhage. Discharge to home was less likely and perihospital mortality rates were generally higher in patients with SDH. These findings were not simply related to age and were not fully captured by the admission Glasgow Coma Scale (GCS) score. The presence of SDH had a much higher sensitivity for poor outcome than the presence of other TBI subtypes, and was more sensitive for these poor outcomes than having a low GCS score (3–8).

CONCLUSIONS

In these ways, SDH was the most important finding associated with poor outcome, and the authors show that consideration of SDH, specifically, can augment age and GCS score in classification and prognostic models for TBI.

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Jonathan J. Lee, Dave Clarke, Eric Hoverson, Elizabeth C. Tyler-Kabara, and Winson S. Ho

Laser interstitial thermal therapy (LITT) is increasingly used as a surgical option for the treatment of epilepsy. Placement of the laser fibers relies on stereotactic navigation with cranial fixation pins. In addition, the laser fiber is stabilized in the cranium during the ablation using a cranial bolt that assumes maturity of the skull. Therefore, younger infants (< 2 years of age) have traditionally not been considered as candidates for LITT. However, LITT is an appealing option for patients with familial epilepsy syndromes, such as tuberous sclerosis complex (TSC), due to the multiplicity of lesions and the likely need for multiple procedures. A 4-month-old infant with TSC presented with refractory focal seizures despite receiving escalating doses of 5 antiepileptic medications. Electrographic and clinical seizures occurred numerous times daily. Noninvasive evaluations, including MRI, magnetoencephalography, scalp EEG, and SPECT, localized the ictal onset to a left frontal cortical tuber in the premotor area. In this paper, the authors report a novel technique to overcome the challenges of performing LITT in an infant with an immature skull by repurposing the Navigus biopsy skull mount for stereotactic placement of a laser fiber using electromagnetic-based navigation. The patient underwent successful ablation of the tuber and remained seizure free 4 months postoperatively. To the authors’ knowledge, this is the youngest reported patient to undergo LITT. A safe method is described to perform LITT in an infant using commonly available tools without dedicated instrumentation beyond standard stereotactic navigation, a biopsy platform, and the Visualase system.

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Filippo Agnesi, Susannah J. Tye, Jonathan M. Bledsoe, Christoph J. Griessenauer, Christopher J. Kimble, Gary C. Sieck, Kevin E. Bennet, Paul A. Garris, Charles D. Blaha, and Kendall H. Lee

Object

In a companion study, the authors describe the development of a new instrument named the Wireless Instantaneous Neurotransmitter Concentration System (WINCS), which couples digital telemetry with fast-scan cyclic voltammetry (FSCV) to measure extracellular concentrations of dopamine. In the present study, the authors describe the extended capability of the WINCS to use fixed potential amperometry (FPA) to measure extracellular concentrations of dopamine, as well as glutamate and adenosine. Compared with other electrochemical techniques such as FSCV or high-speed chronoamperometry, FPA offers superior temporal resolution and, in combination with enzyme-linked biosensors, the potential to monitor nonelectroactive analytes in real time.

Methods

The WINCS design incorporated a transimpedance amplifier with associated analog circuitry for FPA; a microprocessor; a Bluetooth transceiver; and a single, battery-powered, multilayer, printed circuit board. The WINCS was tested with 3 distinct recording electrodes: 1) a carbon-fiber microelectrode (CFM) to measure dopamine; 2) a glutamate oxidase enzyme–linked electrode to measure glutamate; and 3) a multiple enzyme–linked electrode (adenosine deaminase, nucleoside phosphorylase, and xanthine oxidase) to measure adenosine. Proof-of-principle analyses included noise assessments and in vitro and in vivo measurements that were compared with similar analyses by using a commercial hardwired electrochemical system (EA161 Picostat, eDAQ; Pty Ltd). In urethane-anesthetized rats, dopamine release was monitored in the striatum following deep brain stimulation (DBS) of ascending dopaminergic fibers in the medial forebrain bundle (MFB). In separate rat experiments, DBS-evoked adenosine release was monitored in the ventrolateral thalamus. To test the WINCS in an operating room setting resembling human neurosurgery, cortical glutamate release in response to motor cortex stimulation (MCS) was monitored using a large-mammal animal model, the pig.

Results

The WINCS, which is designed in compliance with FDA-recognized consensus standards for medical electrical device safety, successfully measured dopamine, glutamate, and adenosine, both in vitro and in vivo. The WINCS detected striatal dopamine release at the implanted CFM during DBS of the MFB. The DBS-evoked adenosine release in the rat thalamus and MCS-evoked glutamate release in the pig cortex were also successfully measured. Overall, in vitro and in vivo testing demonstrated signals comparable to a commercial hardwired electrochemical system for FPA.

Conclusions

By incorporating FPA, the chemical repertoire of WINCS-measurable neurotransmitters is expanded to include glutamate and other nonelectroactive species for which the evolving field of enzyme-linked biosensors exists. Because many neurotransmitters are not electrochemically active, FPA in combination with enzyme-linked microelectrodes represents a powerful intraoperative tool for rapid and selective neurochemical sampling in important anatomical targets during functional neurosurgery.

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Arvind C. Mohan, Howard L. Weiner, Carrie A. Mohila, Adekunle Adesina, Murali Chintagumpala, Daniel Curry, Andrew Jea, Jonathan J. Lee, Sandi K. Lam, William E. Whitehead, Robert Dauser, Daniel Yoshor, and Guillermo Aldave

OBJECTIVE

The indication for and timing of surgery for epilepsy associated with low-grade mixed neuronal-glial tumors may be controversial. The purpose of this study was to evaluate the effect of resection and associated variables on epilepsy and on progression-free survival (PFS).

METHODS

A retrospective chart review of patients treated between 1992 and 2016 was conducted to identify individuals with epilepsy and low-grade gliomas or neuronal-glial tumors who underwent resective surgery. Data analyzed included age at epilepsy onset, age at surgery, extent of resection, use of electrocorticography, the number of antiepileptic drugs (AEDs) before and after surgery, the presence of dysplasia, Engel class, histological findings, and PFS. The institutional review board protocol was specifically approved to conduct this study.

RESULTS

A total of 107 patients were identified. The median follow-up was 4.9 years. The most common pathology was dysembryoplastic neuroepithelial tumor (36.4%), followed by ganglioglioma (31.8%). Eighty-four percent of patients had Engel class I outcomes following surgery. Gross-total resection was associated with a higher likelihood of an Engel class I outcome (90%) as compared to subtotal resection (58%) (p = 0.0005). Surgery reduced the AED burden, with 40% of patients requiring no AEDs after surgery (p < 0.0001). Children with neurodevelopmental comorbidities (n = 5) uniformly did not experience seizure improvement following resection (0% vs 83% overall; p < 0.0001). Electrocorticography was used in 33% of cases and did not significantly increase class I outcomes. PFS was 90% at 5 years. Eleven percent of tumors recurred, with subtotal resection more likely to result in recurrence (hazard ratio 5.3, p = 0.02). Histological subtype showed no significant impact on recurrence.

CONCLUSIONS

Gross-total resection was strongly associated with Engel class I outcome and longer PFS. Further studies are needed to elucidate the suitable time for surgery and to identify factors associated with oncological transformation.

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Claudio E. Tatsui, R. Jason Stafford, Jing Li, Jonathan N. Sellin, Behrang Amini, Ganesh Rao, Dima Suki, Amol J. Ghia, Paul Brown, Sun-Ho Lee, Charles E. Cowles, Jeffrey S. Weinberg, and Laurence D. Rhines

OBJECT

High-grade malignant spinal cord compression is commonly managed with a combination of surgery aimed at removing the epidural tumor, followed by spinal stereotactic radiosurgery (SSRS) aimed at local tumor control. The authors here introduce the use of spinal laser interstitial thermotherapy (SLITT) as an alternative to surgery prior to SSRS.

METHODS

Patients with a high degree of epidural malignant compression due to radioresistant tumors were selected for study. Visual analog scale (VAS) scores for pain and quality of life were obtained before and within 30 and 60 days after treatment. A laser probe was percutaneously placed in the epidural space. Real-time thermal MRI was used to monitor tissue damage in the region of interest. All patients received postoperative SSRS. The maximum thickness of the epidural tumor was measured, and the degree of epidural spinal cord compression (ESCC) was scored in pre- and postprocedure MRI.

RESULTS

In the 11 patients eligible for study, the mean VAS score for pain decreased from 6.18 in the preoperative period to 4.27 within 30 days and 2.8 within 60 days after the procedure. A similar VAS interrogating the percentage of quality of life demonstrated improvement from 60% preoperatively to 70% within both 30 and 60 days after treatment. Imaging follow-up 2 months after the procedure demonstrated a significant reduction in the mean thickness of the epidural tumor from 8.82 mm (95% CI 7.38–10.25) before treatment to 6.36 mm (95% CI 4.65–8.07) after SLITT and SSRS (p = 0.0001). The median preoperative ESCC Grade 2 was scored as 4, which was significantly higher than the score of 2 for Grade 1b (p = 0.04) on imaging follow-up 2 months after the procedure.

CONCLUTIONS

The authors present the first report on an innovative minimally invasive alternative to surgery in the management of spinal metastasis. In their early experience, SLITT has provided local control with low morbidity and improvement in both pain and the quality of life of patients.

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Jonathan M. Bledsoe, Christopher J. Kimble, Daniel P. Covey, Charles D. Blaha, Filippo Agnesi, Pedram Mohseni, Sidney Whitlock, David M. Johnson, April Horne, Kevin E. Bennet, Kendall H. Lee, and Paul A. Garris

Object

Emerging evidence supports the hypothesis that modulation of specific central neuronal systems contributes to the clinical efficacy of deep brain stimulation (DBS) and motor cortex stimulation (MCS). Real-time monitoring of the neurochemical output of targeted regions may therefore advance functional neurosurgery by, among other goals, providing a strategy for investigation of mechanisms, identification of new candidate neurotransmitters, and chemically guided placement of the stimulating electrode. The authors report the development of a device called the Wireless Instantaneous Neurotransmitter Concentration System (WINCS) for intraoperative neurochemical monitoring during functional neurosurgery. This device supports fast-scan cyclic voltammetry (FSCV) at a carbon-fiber microelectrode (CFM) for real-time, spatially and chemically resolved neurotransmitter measurements in the brain.

Methods

The FSCV study consisted of a triangle wave scanned between −0.4 and 1 V at a rate of 300 V/second and applied at 10 Hz. All voltages were compared with an Ag/AgCl reference electrode. The CFM was constructed by aspirating a single carbon fiber (r = 2.5 μm) into a glass capillary and pulling the capillary to a microscopic tip by using a pipette puller. The exposed carbon fiber (that is, the sensing region) extended beyond the glass insulation by ~ 100 μm. The neurotransmitter dopamine was selected as the analyte for most trials. Proof-of-principle tests included in vitro flow injection and noise analysis, and in vivo measurements in urethane-anesthetized rats by monitoring dopamine release in the striatum following high-frequency electrical stimulation of the medial forebrain bundle. Direct comparisons were made to a conventional hardwired system.

Results

The WINCS, designed in compliance with FDA-recognized consensus standards for medical electrical device safety, consisted of 4 modules: 1) front-end analog circuit for FSCV (that is, current-to-voltage transducer); 2) Bluetooth transceiver; 3) microprocessor; and 4) direct-current battery. A Windows-XP laptop computer running custom software and equipped with a Universal Serial Bus–connected Bluetooth transceiver served as the base station. Computer software directed wireless data acquisition at 100 kilosamples/second and remote control of FSCV operation and adjustable waveform parameters. The WINCS provided reliable, high-fidelity measurements of dopamine and other neurochemicals such as serotonin, norepinephrine, and ascorbic acid by using FSCV at CFM and by flow injection analysis. In rats, the WINCS detected subsecond striatal dopamine release at the implanted sensor during high-frequency stimulation of ascending dopaminergic fibers. Overall, in vitro and in vivo testing demonstrated comparable signals to a conventional hardwired electrochemical system for FSCV. Importantly, the WINCS reduced susceptibility to electromagnetic noise typically found in an operating room setting.

Conclusions

Taken together, these results demonstrate that the WINCS is well suited for intraoperative neurochemical monitoring. It is anticipated that neurotransmitter measurements at an implanted chemical sensor will prove useful for advancing functional neurosurgery.

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Ching-Jen Chen, Dale Ding, Cheng-Chia Lee, Kathryn N. Kearns, I. Jonathan Pomeraniec, Christopher P. Cifarelli, David E. Arsanious, Roman Liscak, Jaromir Hanuska, Brian J. Williams, Mehran B. Yusuf, Shiao Y. Woo, Natasha Ironside, Rebecca M. Burke, Ronald E. Warnick, Daniel M. Trifiletti, David Mathieu, Monica Mureb, Carolina Benjamin, Douglas Kondziolka, Caleb E. Feliciano, Rafael Rodriguez-Mercado, Kevin M. Cockroft, Scott Simon, Heath B. Mackley, Samer G. Zammar, Neel T. Patel, Varun Padmanaban, Nathan Beatson, Anissa Saylany, John Y. K. Lee, Jason P. Sheehan, and on behalf of the International Radiosurgery Research Foundation

OBJECTIVE

Investigations of the combined effects of neoadjuvant Onyx embolization and stereotactic radiosurgery (SRS) on brain arteriovenous malformations (AVMs) have not accounted for initial angioarchitectural features prior to neuroendovascular intervention. The aim of this retrospective, multicenter matched cohort study is to compare the outcomes of SRS with versus without upfront Onyx embolization for AVMs using de novo characteristics of the preembolized nidus.

METHODS

The International Radiosurgery Research Foundation AVM databases from 1987 to 2018 were retrospectively reviewed. Patients were categorized based on AVM treatment approach into Onyx embolization (OE) and SRS (OE+SRS) or SRS alone (SRS-only) cohorts and then propensity score matched in a 1:1 ratio. The primary outcome was AVM obliteration. Secondary outcomes were post-SRS hemorrhage, all-cause mortality, radiological and symptomatic radiation-induced changes (RICs), and cyst formation. Comparisons were analyzed using crude rates and cumulative probabilities adjusted for competing risk of death.

RESULTS

The matched OE+SRS and SRS-only cohorts each comprised 53 patients. Crude rates (37.7% vs 47.2% for the OE+SRS vs SRS-only cohorts, respectively; OR 0.679, p = 0.327) and cumulative probabilities at 3, 4, 5, and 6 years (33.7%, 44.1%, 57.5%, and 65.7% for the OE+SRS cohort vs 34.8%, 45.5%, 59.0%, and 67.1% for the SRS-only cohort, respectively; subhazard ratio 0.961, p = 0.896) of AVM obliteration were similar between the matched cohorts. The secondary outcomes of the matched cohorts were also similar. Asymptomatic and symptomatic embolization-related complication rates in the matched OE+SRS cohort were 18.9% and 9.4%, respectively.

CONCLUSIONS

Pre-SRS AVM embolization with Onyx does not appear to negatively influence outcomes after SRS. These analyses, based on de novo nidal characteristics, thereby refute previous studies that found detrimental effects of Onyx embolization on SRS-induced AVM obliteration. However, given the risks incurred by nidal embolization using Onyx, this neoadjuvant intervention should be used judiciously in multimodal treatment strategies involving SRS for appropriately selected large-volume or angioarchitecturally high-risk AVMs.