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Analysis of risk factors and clinical sequelae of direct electrical cortical stimulation–induced seizures and afterdischarges in patients undergoing awake mapping

Zachary A. Abecassis, Amit B. Ayer, Jessica W. Templer, Ketan Yerneni, Nikhil K. Murthy and Matthew C. Tate

OBJECTIVE

Intraoperative stimulation has emerged as a crucial adjunct in neurosurgical oncology, aiding maximal tumor resection while preserving sensorimotor and language function. Despite increasing use in clinical practice of this stimulation, there are limited data on both intraoperative seizure (IS) frequency and the presence of afterdischarges (ADs) in patients undergoing such procedures. The objective of this study was to determine risk factors for IS or ADs, and to determine the clinical consequences of these intraoperative events.

METHODS

A retrospective chart review was performed for patients undergoing awake craniotomy (both first time and repeat) at a single institution from 2013 to 2018. Hypothesized risk factors for ADs/ISs in patients were evaluated for their effect on ADs and ISs, including tumor location, tumor grade (I–IV), genetic markers (isocitrate dehydrogenase 1/2, O 6-methylguanine-DNA methyltransferase [MGMT] promoter methylation, chromosome 1p/19q codeletion), tumor volume, preoperative seizure status (yes/no), and dosage of preoperative antiepileptic drugs for each patient. Clinical outcomes assessed in patients with IS or ADs were duration of surgery, length of stay, presence of perioperative deficits, and postoperative seizures. Chi-square analysis was performed for binary categorical variables, and a Student t-test was used to assess continuous variables.

RESULTS

A total of 229 consecutive patients were included in the analysis. Thirty-five patients (15%) experienced ISs. Thirteen (37%) of these 35 patients had experienced seizures that were appreciated clinically and noted on electrocorticography simultaneously, while 8 patients (23%) experienced ISs that were electrographic alone (no obvious clinical change). MGMT promoter methylation was associated with an increased prevalence of ISs (OR 3.3, 95% CI 1.2–7.8, p = 0.02). Forty patients (18%) experienced ADs. Twenty-three percent of patients (9/40) with ISs had ADs prior to their seizure, although ISs and ADs were not statistically associated (p = 0.16). The presence of ADs appeared to be correlated with a shorter length of stay (5.1 ± 2.6 vs 6.1 ± 3.7 days, p = 0.037). Of the clinical features assessed, none were found to be predictive of ADs. Neither IS nor AD, or the presence of either IS or AD (65/229 patients), was a predictor for increased length of stay, presence of perioperative deficits, or postoperative seizures.

CONCLUSIONS

ISs and ADs, while commonly observed during intraoperative stimulation for brain mapping, do not negatively affect patient outcomes.

In Journal of Neurosurgery Publish Before Print

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Association between supratentorial pediatric high-grade gliomas involved with the subventricular zone and decreased survival: a multi-institutional retrospective study

Akshitkumar M. Mistry, Nishit Mummareddy, Travis S. CreveCoeur, Jock C. Lillard, Brandy N. Vaughn, Jean-Nicolas Gallant, Andrew T. Hale, Natalie Griffin, John C. Wellons III, David D. Limbrick Jr., Paul Klimo Jr. and Robert P. Naftel

OBJECTIVE

The subventricular zone (SVZ), housed in the lateral walls of the lateral ventricles, is the largest neurogenic niche in the brain. In adults, high-grade gliomas in contact or involved with the SVZ are associated with decreased survival. Whether this association holds true in the pediatric population remains unexplored. To address this gap in knowledge, the authors conducted this retrospective study in a pediatric population with high-grade gliomas treated at three comprehensive centers in the United States.

METHODS

The authors retrospectively identified 63 patients, age ≤ 21 years, with supratentorial WHO grade III–IV gliomas treated at three academic centers. Basic demographic and clinical data regarding presenting signs and symptoms and common treatment variables were obtained. Preoperative MRI studies were evaluated to assess SVZ contact by tumor and to quantify tumor volume.

RESULTS

Sixty-three patients, including 34 males (54%), had a median age of 12.3 years (IQR 6.50–16.2) and a median tumor volume of 39.4 ml (IQR 19.4–65.8). Tumors contacting the SVZ (SVZ+) were noted in 34 patients (54%) and overall were larger than those not in contact with the SVZ (SVZ−; 51.1 vs 27.3, p = 0.002). The SVZ+ tumors were also associated with decreased survival. However, age, tumor volume, tumor grade, and treatment with chemotherapy and/or radiation were not associated with survival in the 63 patients. In the univariable analysis, near-total resection, gross-total resection, and seizure presentation were associated with increased survival (HR = 0.23, 95% CI 0.06–0.88, p = 0.03; HR = 0.26, 95% CI 0.09–0.74, p = 0.01; and HR = 0.46, 95% CI 0.22–0.97, p = 0.04, respectively). In a multivariable stepwise Cox regression analysis, only SVZ+ tumors remained significantly associated with decreased survival (HR = 1.94, 95% CI 1.03–3.64, p = 0.04).

CONCLUSIONS

High-grade glioma contact with the SVZ neural stem cell niche was associated with a significant decrease in survival in the pediatric population, as it is in the adult population. This result suggests that tumor contact with the SVZ is a general negative prognosticator in high-grade glioma independent of age group and invites biological investigations to understand the SVZ’s role in glioma pathobiology.

In Journal of Neurosurgery: Pediatrics Publish Before Print

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Chiari type I malformation: role of the Chiari Severity Index and Chicago Chiari Outcome Scale

Ranbir Ahluwalia, Jarrett Foster, Earllondra Brooks, Jaims Lim, Shilin Zhao, Stephen R. Gannon, Bradley Guidry, John Wellons III and Chevis N. Shannon

OBJECTIVE

The authors aimed to determine whether the Chiari Severity Index (CSI), and other clinical variables, can be used as a predictor of postoperative outcomes for Chiari type I malformation (CM-I) using the modified Chicago Chiari Outcome Scale (mCCOS) as the postoperative measure.

METHODS

The cohort included patients 18 years of age and younger who were treated for CM-I between 2010 and 2015 who had at least 12 months of clinical and radiographic follow-up. CSI grades were assigned using preoperative clinical and neuroimaging data. Clinical, radiographic, and operative data were obtained from medical records. Kruskal-Wallis tests and Spearman correlations were conducted to assess for differences among CSI grades. Linear and ordinal regressions were conducted to evaluate predictors of the mCCOS and its components. Statistical significance was set a priori at p < 0.05.

RESULTS

A total of 65 patients were included in the final cohort. The average age at the time of surgery and the mean mCCOS score were 9.8 ± 4.9 years and 10.4 ± 1.4, respectively. There were no significant differences in the mean mCCOS scores or CSI grades. Pre- and postoperative syrinx sizes were similar across the total patient cohort with median sizes of 7.4 and 3.7 mm, respectively. After controlling for age at the time of surgery, whether duraplasty and/or arachnoid dissection was performed, CSI preoperative score did not predict postoperative mCCOS score. No clinical variable could predict total mCCOS score. When the mCCOS was broken down into 3 subcomponents (pain, non-pain, and complications), only one relationship was identified. Those patients who presented with no headache had a statistically significant decrease in their pain (neck pain, shoulder pain, or dysesthesia in the upper extremities) as measured by the pain component of the mCCOS (χ2 [2, n = 20] = 6.43, p = 0.04). All other preclinical predictors, including CSI grades, were nonsignificant in demonstrating correlations to the mCCOS subcomponents.

CONCLUSIONS

CSI grade was not found to be a marker of surgical outcome as measured by the mCCOS in this study. There were no correlations between the clinical variables and covariates investigated with the mCCOS. The lack of variation in mCCOS scores across this cohort may suggest that the mCCOS is not adequate for detecting differences in postsurgical outcomes. Further investigation is warranted to make this determination.

In Journal of Neurosurgery: Pediatrics Publish Before Print

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Comparative efficacy of autologous versus cadaveric saphenous vein grafts in cerebral revascularization surgery

Christopher J. Stapleton, Ahmed E. Hussein, Mandana Behbahani, Ali Alaraj, Sepideh Amin-Hanjani and Fady T. Charbel

OBJECTIVE

Cerebral bypasses are performed for the purpose of either flow augmentation for ischemic cerebrovascular disease or flow replacement for vessel sacrifice during complex aneurysm or tumor surgery. Saphenous vein grafts (SVGs) are commonly used interposition grafts. The authors of this study sought to compare the efficacy of autologous versus cadaveric SVGs in a large series of cerebral bypasses using interposition vein grafts with long-term angiographic follow-up.

METHODS

All intracranial bypass procedures performed between 2001 and 2018 were reviewed. Demographic, clinical, angiographic, and operative data were recorded and then analyzed according to SVG type.

RESULTS

A total of 308 consecutive intracranial bypasses were performed during the study period, 53 (17.2%) of which were bypasses with an interposition SVG (38 autologous, 15 cadaveric). At a median follow-up of 2.2 months (IQR 0.2–29.1), 39 (73.6%) bypasses were patent (26 [68.4%] autologous, 13 [86.7%] cadaveric, p = 0.30). Comparing autologous and cadaveric SVG recipients, there were no statistically significant differences in age (p = 0.50), sex (p > 0.99), history of smoking (p = 0.75), hypertension (p > 0.99), diabetes mellitus (p = 0.13), indication for bypass (p = 0.27), or SVG diameter (p = 0.65). While there were higher intraoperative (autologous, 100.0 ml/min, IQR 84.3–147.5; cadaveric, 80.0 ml/min, IQR 47.3–107.8; p = 0.11) and postoperative (autologous, 142.2 ml/min, IQR 76.8–160.8; cadaveric, 92.0 ml/min, IQR 69.2–132.2; p = 0.42) volumetric flow rates in the autologous SVGs compared to those in the cadaveric SVGs, the difference between the two groups did not reach statistical significance. In addition, the blood flow index, or ratio of postoperative to intraoperative blood flow, for each bypass was similar between the groups (autologous, 1.3, IQR 0.9–1.6; cadaveric, 1.5, IQR 1.0–2.3; p = 0.37). Kaplan-Meier estimates showed no difference in bypass patency rates over time between autologous and cadaveric SVGs (p = 0.58).

CONCLUSIONS

Cadaveric SVGs are a reasonable interposition graft option in cerebral revascularization surgery when autologous grafts are not available.

In Journal of Neurosurgery Publish Before Print

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Compassionate use of a custom 3D-printed sacral implant for revision of failing sacrectomy: case report

Grégoire P. Chatain and Michael Finn

Reconstruction of the spinopelvic continuity after sacral resection for primary sacral tumors remains challenging. Complex anatomical and biomechanical factors of this transition zone may be addressed with the advancement of 3D-printed implants. Here, the authors report on a 67-year-old patient with a sacral chordoma who initially underwent total en bloc sacrectomy followed by standard spinopelvic reconstruction. Pseudarthrosis and instrumentation failure of the lumbosacral junction construct subsequently developed. A custom 3D-printed sacral prosthesis was created using high-resolution CT images. Emergency Food and Drug Administration approval was obtained, and the custom device was implanted as a salvage reconstruction surgery. Made of porous titanium mesh, the custom artificial sacrum was placed in the defect based on the anticipated osteotomic planes and was fixed with a screw-rod system along with a fibular bone strut graft. At the 18-month follow-up, the patient was disease free and walking short distances with assistance. CT revealed excellent bony incorporation into the graft.

The use of a custom 3D-printed prosthesis in spinal reconstruction has been rarely reported, and its application in sacral reconstruction and long-term outcome are novel. While the implant was believed to be critical in endowing the region with enough biomechanical stability to promote healing, the procedure was difficult and several key learning points were discovered along the way.

In Journal of Neurosurgery: Spine Publish Before Print

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Critical role of platelet-derived growth factor–α in angiogenesis after indirect bypass in a murine moyamoya disease model

Tomohide Hayashi, Seiji Yamamoto, Takeru Hamashima, Hisashi Mori, Masakiyo Sasahara and Satoshi Kuroda

OBJECTIVE

This study aimed to clarify the underlying mechanism of pathognomonic angiogenesis between the temporal muscle and neocortex after indirect bypass for moyamoya disease by shedding light on the role of platelet-derived growth factor receptor–α (PDGFRα) in angiogenesis.

METHODS

The gene for PDGFRα was systemically inactivated in adult mice (α-KO mice). The Pdgfra-preserving mice (Flox mice) and α-KO mice were exposed to bilateral common carotid artery stenosis (BCAS) by using microcoils. One week later the animals underwent encephalomyosynangiosis (EMS) on the right side. Cerebral blood flow (CBF) was serially measured using a laser Doppler flowmeter. Histological analysis was performed on the distribution of CD31-positive vessels and collagen deposit at 28 days after BCAS. Reverse transcription polymerase chain reaction (RT-PCR) was performed to assess the expression of collagen mRNA in the skin fibroblasts derived from Flox and α-KO mice.

RESULTS

BCAS significantly reduced CBF up to approximately 70% of the control level at 28 days after the onset. There was no significant difference in CBF between Flox and α-KO mice. EMS significantly enhanced the improvement of CBF on the ipsilateral side of Flox mice, but not α-KO mice. EMS significantly induced the development of CD31-positive vessels in both the neocortex and temporal muscle on the ipsilateral side of Flox mice, but not α-KO mice. Deposition of collagen was distinctly observed between them in Flox mice, but not α-KO mice. Expression of mRNA of collagen type 1 alpha 1 (Col1a1) and collagen type 3 alpha 1 (Col3a1) was significantly downregulated in the skin fibroblasts from α-KO mice.

CONCLUSIONS

This is the first study that denotes the role of a specific growth factor in angiogenesis after EMS for moyamoya disease by inactivating its gene in mice. The findings strongly suggest that PDGFRα signal may play an important role in developing spontaneous angiogenesis between the temporal muscle and neocortex after EMS in moyamoya disease.

In Journal of Neurosurgery Publish Before Print

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Effects of implantation of a deep brain stimulation device on patient weight in Parkinson’s disease and essential tremor

Nikolas R. Monteferrante, Brian G. Wilhelmi, Margaret Lambert and Francisco A. Ponce

OBJECTIVE

Deep brain stimulation (DBS) is a well-established therapy for treating neurological movement disorders. Some patients who have received DBS therapy have noticed significant weight gain. Further investigation into correlations between patient characteristics and weight gain following DBS device implantation, which the authors here have done, will provide physicians with useful clinical information.

METHODS

The authors performed a retrospective study of patients with Parkinson’s disease (PD) and essential tremor (ET) who had received DBS therapy in the period from 2012 to 2017. Patient weights had been recorded preoperatively and at 3, 6, and 12 months postoperatively. These data were used to compare patient characteristics, including diagnosis, body mass index (BMI), sex, levodopa equivalent dose (LED), and change in Unified Parkinson’s Disease Rating Scale (UPDRS) score. For PD patients, a quantile multivariate regression analysis was used to examine whether significant correlations existed between several of these patient characteristics, as well as age and weight gain following implantation.

RESULTS

PD patients had gained a significant amount of weight at 3 months (mean [SE] 2.66 [0.428] kg, p < 0.001), 6 months (3.64 [0.492] kg, p < 0.001), and 12 months (4.18 [0.540] kg, p < 0.001) after DBS placement. Patients who had undergone subthalamic nucleus (STN) DBS device placement gained, on average, more weight than the patients with globus pallidus internus (GPi) placement at both 6 months (mean 2.558 [1.020] kg, p = 0.01) and 12 months (2.358 [1.130] kg, p = 0.04). BMI in the STN cohort was greater than that in the GPi cohort at 6 months (mean difference [SE] 2.60 [1.127] kg/m2, p = 0.02) and at 12 months (2.36 [1.112] kg/m2, p = 0.04). A reduction in LED was negatively correlated with weight change at 6 months (r = −0.33, p < 0.001) and 12 months (r = −0.41, p < 0.001). There was no weight gain correlated with DBS therapy for ET.

CONCLUSIONS

PD patients experienced a significant change in weight over time after DBS therapy, whereas ET patients did not. PD patients with an STN target site experienced greater weight gain, on average, than those with a GPi target site. Furthermore, there was a significant increase in BMI at 6 and 12 months in patients with an STN target compared to that in patients with a GPi target. PD patients whose LED was reduced after DBS gained more weight at 6 and 12 months after surgery than the patients whose LED was kept at the same level or increased.

In Journal of Neurosurgery Publish Before Print

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Efficacy of intraarterial superselective indocyanine green videoangiography in cerebral arteriovenous malformation surgery in a hybrid operating room

Kenji Shimada, Tadashi Yamaguchi, Takeshi Miyamoto, Shu Sogabe, Masaaki Korai, Toshiyuki Okazaki, Yasuhisa Kanematsu, Junichiro Satomi, Shinji Nagahiro and Yasushi Takagi

OBJECTIVE

Although intravenous indocyanine green (ICG) videoangiography has been reported to be useful when applied to cerebral arteriovenous malformation (AVM) surgery, the ICG that remains after the procedure makes it difficult to understand the anatomy, to evaluate nidus blood flow changes, and to repeat ICG videoangiography within a short time. Intraarterial ICG videoangiography has emerged as a way to overcome these limitations. The current study presents the results of intraarterial ICG videoangiography undertaken in patients with cerebral AVMs.

METHODS

Intraarterial ICG videoangiography was performed in 13 patients with cerebral AVMs. Routine intraoperative digital subtraction angiography at the authors’ institution is performed in a hybrid operating room during AVM surgery and includes the added step of injecting ICG to the contrast medium that is administered through a catheter.

RESULTS

Predissection studies were able to visualize the feeder in 12 of 13 cases. The nidus was visualized in 12 of 13 cases, while the drainer was visualized in all cases. After total dissection of the nidus, there was no ICG filling in the drainers found in any of the cases. Washout of the ICG took 4.4 ± 1.3 seconds in the feeders, 9.2 ± 3.5 seconds in the drainers, and 20.9 ± 3.4 seconds in all of the vessels. Nidus flow reduction was confirmed during dissection in 9 of 9 cases. Flow reduction was easy to recognize due to each span being very short. Color-encoded visualization and objective data obtained by Flow 800 analysis reinforced these findings.

CONCLUSIONS

The results showed that intraarterial ICG videoangiography was more useful than intravenous ICG videoangiography in cerebral AVM surgery. This was especially effective in the identification of the feeder, nidus, and drainer and in the assessment of the flow dynamics of the nidus. Use of Flow 800 made it simpler and easier to evaluate these findings.

In Journal of Neurosurgery Publish Before Print

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Erratum. A points-based algorithm for prognosticating clinical outcome of Chiari malformation Type I with syringomyelia: results from a predictive model analysis of 82 surgically managed adult patients

Sumit Thakar

In Journal of Neurosurgery: Spine Publish Before Print

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Hydrocephalus in children with ruptured cerebral arteriovenous malformation

Sarah Stricker, Grégoire Boulouis, Sandro Benichi, Florent Gariel, Lorenzo Garzelli, Kevin Beccaria, Anais Chivet, Timothee de Saint Denis, Syril James, Giovanna Paternoster, Michel Zerah, Marie Bourgeois, Nathalie Boddaert, Francis Brunelle, Philippe Meyer, Stephanie Puget, Olivier Naggara and Thomas Blauwblomme

OBJECTIVE

Hydrocephalus is a strong determinant of poor neurological outcome after intracerebral hemorrhage (ICH). In children, ruptured brain arteriovenous malformations (bAVMs) are the dominant cause of ICH. In a large prospective cohort of pediatric patients with ruptured bAVMs, the authors analyzed the rates and predictive factors of hydrocephalus requiring acute external ventricular drainage (EVD) or ventriculoperitoneal shunt (VPS).

METHODS

The authors performed a single-center retrospective analysis of the data from a prospectively maintained database of children admitted for a ruptured bAVM since 2002. Admission clinical and imaging predictors of EVD and VPS placement were analyzed using univariate and multivariate statistical models.

RESULTS

Among 114 patients (mean age 9.8 years) with 125 distinct ICHs due to ruptured bAVM, EVD and VPS were placed for 55/125 (44%) hemorrhagic events and 5/114 patients (4.4%), respectively. A multivariate nominal logistic regression model identified low initial Glasgow Coma Scale (iGCS) score, hydrocephalus on initial CT scan, the presence of intraventicular hemorrhage (IVH), and higher modified Graeb Scale (mGS) score as strongly associated with subsequent need for EVD (all p < 0.001). All children who needed a VPS had initial hydrocephalus requiring EVD and tended to have higher mGS scores.

CONCLUSIONS

In a large cohort of pediatric patients with ruptured bAVM, almost half of the patients required EVD and 4.4% required permanent VPS. Use of a low iGCS score and a semiquantitative mGS score as indicators of the IVH burden may be helpful for decision making in the emergency setting and thus improve treatment.

In Journal of Neurosurgery: Pediatrics Publish Before Print