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Are hemodynamics responsible for inflammatory changes in venous vessel walls? A quantitative study of wall-enhancing intracranial arteriovenous malformation draining veins

Janneck Stahl, Laura Stone McGuire, Mark Rizko, Sylvia Saalfeld, Philipp Berg, and Ali Alaraj

OBJECTIVE

Signal enhancement of vascular walls on vessel wall MRI might be a biomarker for inflammation. It has been theorized that contrast enhancement on vessel wall imaging (VWI) in draining veins of intracranial arteriovenous malformations (AVMs) may be associated with disease progression and development of venous stenosis. The aim of this study was to investigate the relationship between vessel wall enhancement and hemodynamic stressors along AVM draining veins.

METHODS

Eight AVM patients with 15 draining veins visualized on VWI were included. Based on MR venography data, patient-specific 3D surface models of the venous anatomy distal to the nidus were segmented. The enhanced vascular wall regions were manually extracted and mapped onto the venous surface models after registration of image data. Using image-based blood flow simulations applying patient-specific boundary conditions based on phase-contrast quantitative MR angiography, hemodynamics were investigated in the enhanced vasculature. For the shear-related parameters, time-averaged wall shear stress (TAWSS), oscillatory shear index (OSI), and relative residence time (RRT) were calculated. Velocity, oscillatory velocity index (OVI), and vorticity were extracted for the intraluminal flow-related hemodynamics.

RESULTS

Visual observations demonstrated overlap of enhancement with local lower shear stresses resulting from decreased velocities. Thus, higher RRT values were measured in the enhanced areas. Furthermore, nonenhancing draining veins showed on average slightly higher flow velocities and TAWSS. Significant decreases of 55% (p = 0.03) for TAWSS and of 24% (p = 0.03) for vorticity were identified in enhanced areas compared with near distal and proximal domains. Velocity magnitude in the enhanced region showed a nonsignificant decrease of 14% (p = 0.06). Furthermore, increases were present in the OSI (32%, p = 0.3), RRT (25%, p = 0.15), and OVI (26%, p = 0.3) in enhanced vessel sections, although the differences were not significant.

CONCLUSIONS

This novel multimodal investigation of hemodynamics in AVM draining veins allows for precise prediction of occurring shear- and flow-related phenomena in enhanced vessel walls. These findings may suggest low shear to be a local predisposing factor for venous stenosis in AVMs.

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Benefits of stereotactic radiosurgical anterior capsulotomy for obsessive-compulsive disorder: a meta-analysis

Rishabh Gupta, Jeffrey W. Chen, Natasha C. Hughes, Mohammad Hamo, Samuel Jean-Baptiste, Danika L. Paulo, Hani Chanbour, Run Fan, Fei Ye, Abhiram Vadali, Anthony Cmelak, and Sarah K. Bick

OBJECTIVE

Anterior capsulotomy (AC) is a therapeutic option for patients with severe, treatment-resistant obsessive-compulsive disorder (OCD). The procedure can be performed via multiple techniques, with stereotactic radiosurgery (SRS) gaining popularity because of its minimally invasive nature. The risk-benefit profile of AC performed specifically with SRS has not been well characterized. Therefore, the primary objective of this study was to characterize outcomes following stereotactic radiosurgical AC in OCD patients.

METHODS

Studies assessing mean Yale-Brown Obsessive Compulsive Scale (Y-BOCS) scores before and after stereotactic radiosurgical AC for OCD were included in this analysis. Inverse-variance fixed-effect modeling was used for pooling, and random-effects estimate of the ratio of means and standard mean differences were calculated at 6 months, 12 months, and the last follow-up for Y-BOCS scores, as well as the last follow-up for the Beck Depression Inventory (BDI)/BDI-II scores. A generalized linear mixed model was used to generate fixed- and random-effects models for categorical outcomes. Univariate random-effects meta-regression was used to evaluate associations between postoperative Y-BOCS scores and study covariates. Adverse events were summed across studies. Publication bias was assessed with Begg’s test.

RESULTS

Eleven studies with 180 patients were eligible for inclusion. The mean Y-BOCS score decreased from 33.28 to 17.45 at the last-follow up (p < 0.001). Sixty percent of patients were classified as responders and 10% as partial responders, 18% experienced remission, and 4% had worsened Y-BOCS scores. The degree of improvement in the Y-BOCS score correlated with time since surgery (p = 0.046). In the random-effects model, the mean BDI at the last follow-up was not significantly different from that preoperatively. However, in an analysis performed with available paired pre- and postoperative BDI/BDI-II scores, there was significant improvement in the BDI/BDI-II scores postoperatively. Adverse events numbered 235, with headaches, weight change, mood changes, worsened depression/anxiety, and apathy occurring most commonly.

CONCLUSIONS

Stereotactic radiosurgical AC is an effective technique for treating OCD. Its efficacy is similar to that of AC performed via other lesioning techniques.

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Deep learning–based quantification of total bleeding volume and its association with complications, disability, and death in patients with aneurysmal subarachnoid hemorrhage

Ping Hu, Yanze Wu, Tengfeng Yan, Lei Shu, Feng Liu, Bing Xiao, Minhua Ye, Miaojing Wu, Shigang Lv, and Xingen Zhu

OBJECTIVE

The relationships between immediate bleeding severity, postoperative complications, and long-term functional outcomes in patients with aneurysmal subarachnoid hemorrhage (aSAH) remain uncertain. Here, the authors apply their recently developed automated deep learning technique to quantify total bleeding volume (TBV) in patients with aSAH and investigate associations between quantitative TBV and secondary complications, adverse long-term functional outcomes, and death.

METHODS

Electronic health record data were extracted for adult patients admitted to a single institution within 72 hours of aSAH onset between 2018 and 2021. An automatic deep learning model was used to fully segment and quantify TBV on admission noncontrast head CT images. Patients were subgrouped by TBV quartile, and multivariable logistic regression, restricted cubic splines, and subgroup analysis were used to explore the relationships between TBV and each clinical outcome.

RESULTS

A total of 819 patients were included in the study. Sixty-six (8.1%) patients developed hydrocephalus, while 43 (5.3%) experienced rebleeding, 141 (17.2%) had delayed cerebral ischemia, 88 (10.7%) died in the 12 months after discharge, and 208 (25.7%) had a modified Rankin Scale score ≥ 3 12 months after discharge. On multivariable analysis, patients in the highest TBV quartile (> 37.94 ml) had an increased risk of hydrocephalus (adjusted OR [aOR] 4.38, 95% CI 1.61–11.87; p = 0.004), rebleeding (aOR 3.26, 95% CI 1.03–10.33; p = 0.045), death (aOR 6.92, 95% CI 1.89–25.37; p = 0.004), and 12-month disability (aOR 3.30, 95% CI 1.62–6.72; p = 0.001) compared with the lowest TBV quantile (< 8.34 ml). The risks of hydrocephalus (nonlinear, p = 0.025), rebleeding, death, and disability (linear, p > 0.05) were positively associated with TBV by restricted cubic splines. In subgroup analysis, TBV had a stronger effect on 12-month outcome in female than male patients (p for interaction = 0.0499) and on rebleeding prevalence in patients with endovascular coiling than those with surgical clipping (p for interaction = 0.008).

CONCLUSIONS

Elevated TBV is associated with a greater risk of hydrocephalus, rebleeding, death, and poor prognosis.

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Epidemiology of moderate traumatic brain injury and factors associated with poor neurological outcome

Shu Utsumi, Shingo Ohki, and Nobuaki Shime

OBJECTIVE

The objective of this study was to investigate the epidemiology of moderate traumatic brain injury (TBI) and factors associated with poor neurological outcome.

METHODS

This multicenter retrospective cohort study used data from the Japan Trauma Data Bank from 2019 to 2022, including adult patients (aged > 17 years) with moderate TBI (Glasgow Coma Scale [GCS] score of 9–12). Patient characteristics, injury mechanism, details of intracranial injury, treatment, and outcome were investigated. Multivariate mixed-effects logistic regression analysis was used to examine factors associated with poor neurological outcome. Poor neurological outcome was defined as a Glasgow Outcome Scale score ranging between 1 and 3.

RESULTS

A total of 1638 patients were included in the study; 67% were male, with a median age of 73 years and a median Injury Severity Score (ISS) of 17. The major mechanism of injury was falls in 545 patients (33%); subdural hematoma and cerebral contusions were both common intracranial injuries in 482 study participants (29%) each. Two hundred forty-seven patients (15%) underwent craniotomy and 366 (22%) were managed with mechanical ventilation. There were 765 patients (47%) with poor neurological outcome, of whom 215 (13%) died in the hospital. Older age (≥ 65 years; adjusted odds ratio [aOR] 4.66, 95% CI 3.54–6.12), higher Charlson Comorbidity Index (CCI; aOR 1.27, 95% CI 1.14–1.42), GCS scores of 9 (aOR 1.50, 95% CI 1.08–2.09) and 10 (aOR 1.37, 95% CI 1.01–1.85), and severe trauma (ISS > 15; aOR 1.93, 95% CI 1.49–2.50) were associated with poor prognosis. Additionally, patients who required mechanical ventilation (aOR 1.76, 95% CI 1.27–2.42) and craniotomy (aOR 1.57, 95% CI 1.08–2.28) had a poor neurological outcome. Administration of tranexamic acid (aOR 0.74, 95% CI 0.58–0.94) and intensive care unit (ICU) admission (aOR 0.69, 95% CI 0.52–0.93) were associated with improved neurological outcome.

CONCLUSIONS

Almost half of the patients with moderate TBI had poor neurological outcome at hospital discharge. Several factors including older age, higher CCI, GCS scores of 9 or 10, severe trauma, and mechanical ventilation or craniotomy were found to be associated with poor neurological outcome in patients with moderate TBI. Additionally, these data suggest that tranexamic acid administration and admission to the ICU might be important for improving prognosis. Further investigations are warranted to elucidate the appropriate management for patients with moderate TBI.

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Periprocedural intravenous heparin in patients with acute ischemic stroke treated with endovascular thrombectomy after intravenous thrombolysis

Hao Wang, Kang Yuan, Xianjun Huang, Yi Zhong, Mengdi Xie, Ruidong Ye, Yunfei Han, Qiushi Lv, Qingshi Zhao, and Rui Liu

OBJECTIVE

The benefit-to-risk ratio of periprocedural heparin in patients treated with endovascular thrombectomy (EVT) after intravenous thrombolysis (IVT) remains unclear. This study aimed to evaluate the potential effects of periprocedural heparin on clinical outcomes of EVT after IVT.

METHODS

The authors retrospectively analyzed patients from multicenter studies treated with EVT after IVT in the anterior circulation. The endpoints were unfavorable outcome (defined as modified Rankin Scale score ≥ 3 at 90 days), 90-day mortality, symptomatic intracranial hemorrhage (SICH), successful recanalization, and early neurological deterioration. Patients were divided into two groups based on whether they were treated with heparin (heparin-treated group) or not (untreated group), and the efficacy and safety outcomes were compared using multivariable logistic regression models and propensity score–matching methods.

RESULTS

Among the 322 included patients (mean age 67.4 years, 54.3% male), 32% of patients received periprocedural heparin. In multivariable analyses, the administration of periprocedural heparin was a significant predictor for unfavorable outcome (OR 2.821, 95% CI 1.15–7.326; p = 0.027), SICH (OR 24.925, 95% CI 2.363–780.262; p = 0.025), and early neurological deterioration (OR 5.344, 95% CI 1.299–28.040; p = 0.029). Regarding successful recanalization and death, no significant differences between the groups were found after propensity score matching.

CONCLUSIONS

The results showed that periprocedural heparin is associated with an increased risk of unfavorable outcomes and SICH in patients treated with EVT after IVT. Further studies are warranted to evaluate the utility and safety of periprocedural heparin.

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Comprehensive characterization of intracranial hemorrhage in deep brain stimulation: a systematic review of literature from 1987 to 2023

Cletus Cheyuo, Artur Vetkas, Can Sarica, Suneil K. Kalia, Mojgan Hodaie, and Andres M. Lozano

OBJECTIVE

Deep brain stimulation (DBS) is an effective treatment for medically refractory movement disorders and other neurological conditions. To comprehensively characterize the prevalence, locations, timing of detection, clinical effects, and risk factors of DBS-related intracranial hemorrhage (ICH), the authors performed a systematic review of the published literature.

METHODS

PubMed, EMBASE, and Web of Science were searched using 2 concepts: cerebral hemorrhage and brain stimulation, with filters for English, human studies, and publication dates 1980–2023. The inclusion criteria were the use of DBS intervention for any human neurological condition, with documentation of hemorrhagic complications by location and clinical effect. Studies with non-DBS interventions, no documentation of hemorrhage outcome, patient cohorts of ≤ 10, and pediatric patients were excluded. The risk of bias was assessed using Centre for Evidence-Based Medicine Levels of Evidence. The authors performed proportional meta-analysis for ICH prevalence.

RESULTS

A total of 63 studies, with 13,056 patients, met the inclusion criteria. The prevalence of ICH was 2.9% (fixed-effects model, 95% CI 2.62%–3.2%) per patient and 1.6% (random-effects model, 95% CI 1.34%–1.87%) per DBS lead, with 49.6% being symptomatic. The ICH rates did not change with time. ICH most commonly occurred around the DBS lead, with 16% at the entry point, 31% along the track, and 7% at the target. Microelectrode recording (MER) during DBS was associated with increased ICH rate compared to DBS without MER (3.5 ± 2.2 vs 2.1 ± 1.4; p[T ≤ t] 1-tail = 0.038). Other reported ICH risk factors include intraoperative systolic blood pressure > 140 mm Hg, sulcal DBS trajectories, and multiple microelectrode insertions. Sixty percent of ICH was detected at 24 hours postoperatively and 27% intraoperatively. The all-cause mortality rate of DBS was 0.4%, with ICH accounting for 22% of deaths. Single-surgeon DBS experience showed a weak inverse correlation (r = −0.27, p = 0.2189) between the rate of ICH per lead and the number of leads implanted per year.

CONCLUSIONS

This study provides level III evidence that MER during DBS is a risk factor for ICH. Other risk factors include intraoperative systolic blood pressure > 140 mm Hg, sulcal trajectories, and multiple microelectrode insertions. Avoidance of these risk factors may decrease the rate of ICH.

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A comprehensive review on the development of sporadic cerebral arteriovenous malformations: from Padget to next-generation sequencing

Stephanie A. Coffman, Keyan Peterson, Nicholas Contillo, Kyle M. Fargen, and Stacey Q. Wolfe

Cerebral arteriovenous malformations (AVMs) are a leading cause of intracerebral hemorrhage in both children and young adults. With the continued advancement of science and technology, the understanding of the pathophysiology behind the development of these lesions has evolved. From early theory published by Harvey Cushing and Percival Bailey in 1928, Tumors Arising from the Blood-vessels of the Brain: Angiomatous Malformations and Hemangioblastoma, which regarded AVMs as tumors arising from blood vessels, to the meticulous artistry of Dorcas Padget’s embryological cataloguing of the cerebral vasculature in 1948, to the proliferative capillaropathy theory of Yaşargil in 1987, to Ramey’s 2014 hierarchical model of vascular development, there have been multiple hypotheses of congenital, developmental, and genetic two-hit theories in the pathogenesis of AVMs. Most recent evidence implicates somatic KRAS mutations in the cerebral endothelium, producing an important understanding of the pathogenesis of this disease, which is critical to the development of targeted therapeutics. The authors present the historical progression of their understanding of AVM pathogenesis. They focus on the foundation laid by early pioneers, discussing embryological anatomy and vasculogenesis, the prominent theories of AVM development that have emerged over time, and culminate in an overview of the most current understanding of the pathogenesis of these complex vascular lesions and the clinical implications of our scientific progress.

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Long-term radiographic and endocrinological outcomes of stereotactic radiosurgery for recurrent or residual nonfunctioning pituitary adenomas

Ahmed Shaaban, Chloé Dumot, Georgios Mantziaris, Sam Dayawansa, Selcuk Peker, Yavuz Samanci, Ahmed M. Nabeel, Wael A. Reda, Sameh R. Tawadros, Khaled Abdel Karim, Amr M. N. El-Shehaby, Reem M. Emad Eldin, Ahmed Ragab Abdelsalam, Roman Liscak, Jaromir May, Elad Mashiach, Fernando De Nigris Vasconcellos, Kenneth Bernstein, Douglas Kondziolka, Herwin Speckter, Ruben Mota, Anderson Brito, Shray K. Bindal, Ajay Niranjan, L. Dade Lunsford, Carolina Gesteira Benjamin, Timoteo Almeida, Jennifer Z. Mao, David Mathieu, Jean-Nicolas Tourigny, Manjul Tripathi, Joshua David Palmer, Jennifer Matsui, Joseph Crooks, Rodney E. Wegner, Matthew J. Shepard, and Jason P. Sheehan

OBJECTIVE

Stereotactic radiosurgery (SRS) is used for the treatment of residual/recurrent nonfunctional pituitary adenoma (NFPA). The aim of this study was to evaluate the factors related to long-term tumor control and delayed endocrinopathies following SRS.

METHODS

This retrospective, multicenter study included patients with recurrent/residual NFPA treated with single-fraction SRS; they were then divided into two arms. The first arm included patients with at least 5 years of radiographic follow-up and all patients with local tumor progression. The second arm included patients with at least 5 years of endocrinological follow-up and all patients who developed endocrinopathy. Study endpoints were tumor control and new or worsening hypopituitarism after SRS and were analyzed using Cox regression and Kaplan-Meier methodology.

RESULTS

There were 360 patients in the tumor control arm (median age 52.7 [IQR 42.9–61] years, 193 [53.6%] males) and 351 patients in the hypopituitarism arm (median age 52.5 [IQR 43–61] years, 186 [53.0%] males). The median follow-up in the tumor control evaluation group was 7.95 (IQR 5.7–10.5) years. Tumor control rates at 5, 8, 10, and 15 years were 93% (95% CI 90%–95%), 87% (95% CI 83%–91%), 86% (95% CI 82%–90%), and 69% (95% CI 59%–81%), respectively. The median follow-up in the endocrinopathy evaluation group was 8 (IQR 5.9–10.7) years. Pituitary function preservation rates at 5, 8, 10, and 15 years were 83% (95% CI 80%–87%), 81% (95% CI 77%–85%), 78% (95% CI 74%–83%), and 71% (95% CI 63%–79%), respectively. A margin dose > 15 Gy (HR 0.8, 95% CI 0.7–0.9; p < 0.001) and a delay from last resection to SRS > 1 year (HR 0.9, 95% CI 0.7–0.9; p = 0.04) were significant factors related to tumor control in multivariable analysis. A maximum dose to the pituitary stalk ≤ 10 Gy (HR 1.1, 95% CI 1.09–1.2; p < 0.001) was associated with pituitary function preservation. New visual deficits after SRS occurred in 7 (1.94%) patients in the tumor control group and 8 (2.3%) patients in the endocrinopathy group. Other new cranial nerve deficits post-SRS occurred in 4 of 160 patients with data in the tumor control group and 3 of 140 patients with data in the endocrinopathy group.

CONCLUSIONS

SRS affords favorable and durable tumor control for the vast majority of NFPAs. Post-SRS hypopituitarism occurs in a minority of patients, but this risk increases with time and warrants long-term follow-up.

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Microsurgical anatomy of the olfactory filaments in the nasal mucosa

Hasan Barış Ilgaz, Kamran Urgun, Ulaş Yener, Melike Mut, James K. Liu, and Kaan Yağmurlu

OBJECTIVE

The aim of this study was to examine the distribution of olfactory filaments (OFs) in the nasal mucosa to facilitate preservation of olfactory function in endonasal approaches and preparation of a nasoseptal flap.

METHODS

One formalin-fixed and 9 fresh cadaveric silicone-injected specimens with 20 total sides were studied to measure the distance of the OFs to the anatomical landmarks and compare the OF presence in the nasal septum mucosa (NSM) and ethmoidal mucosa (EM).

RESULTS

The mean distance from the first to the last OF was 19.37 ± 2.16 mm in the NSM and 23.44 ± 5.42 mm in the EM. The NSM had a mean of 7.55 ± 1.31 OFs and the EM had 14.3 ± 1.78. Average OF lengths were measured at 6.44 ± 1.48 (range 3.75–12.40) mm in the NSM and 8.05 ± 1.76 (range 4.14–13.20) mm in the EM. The mean values of the EM measurements were compared with those of the NSM; the number of OFs, the distance between the first and last OF, the average OF length, and the number of OFs between anterior and posterior ethmoidal arteries in the NSM were significantly less (p < 0.05) than those in the EM. The distance between the first OF to the nasal bone on the NSM was greater than on the EM.

CONCLUSIONS

Compared with the EM, the OFs are significantly fewer in number and smaller in size in the NSM. The uppermost edge of the nasoseptal flap incision in the NSM might be safer to start below 12 mm from the cribriform plate for OF protection.

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Patterns of recurrence and disease progression in patients with positive-margin olfactory neuroblastoma following primary resection

Megan M. J. Bauman, Jeffrey P. Graves, Travis J. Haller, Ryan A. McMillan, David M. Routman, Aditya Raghunathan, Janalee K. Stokken, Michael J. Link, Eric J. Moore, Garret Choby, and Jamie J. Van Gompel

OBJECTIVE

Olfactory neuroblastoma (ONB) is a rare, malignant tumor of the sinonasal tract that arises from olfactory epithelium. Although surgery is the preferred first-line treatment, tumor involvement of adjacent structures may preclude the ability to achieve negative margins during initial resection. Herein, the authors examine the oncological outcomes of patients with positive margins after primary resection of ONB, with the aim of determining predictors of disease progression and patterns of recurrence.

METHODS

The authors performed an institutional review of 25 patients with positive-margin ONB after resection. Cox survival analyses were used to determine any statistically significant predictors of worse progression-free survival (PFS) and overall survival (OS).

RESULTS

A total of 93 patients who were diagnosed with ONB were identified, of whom 25 patients had positive margins following their primary resection. Eleven (44%) had a delayed finding of positive margins that were initially negative in the operating room but returned as positive on final pathology. Four patients had subtotal resection (STR), whereas the remaining patients underwent gross-total resection. Twenty-four patients received adjuvant radiotherapy (96%), and 15 additionally received adjuvant chemotherapy (60%). Fourteen patients (56%) experienced recurrence/progression at a median time of 35 months following resection (IQR 19–70 months). Local recurrence occurred in 10 patients (40%), regional in 9 (36%), and distant metastasis in 2 (8%). In Cox survival analyses, the 5-year PFS and OS were 55.1% and 79.2%, respectively. Kadish stage D was predictive of worse PFS in univariate (hazard ratio [HR] 15.67, 95% CI 3.38–72.61, p < 0.001) and multivariate (HR 15.46, 95% CI 1.45–164.91, p = 0.023) analyses. Hyams grade, adjuvant chemotherapy, and primary radiotherapy were not associated with PFS. Furthermore, Kadish stage D and STR were predictive of worse OS in univariate analysis (HR 12.64, 95% CI 2.03–78.86, p = 0.007; HR 7.31, 95% CI 1.45–36.84, p = 0.016; respectively). However, local and regional recurrence was not associated with worse OS.

CONCLUSIONS

Approximately half of patients with positive-margin ONB may experience disease recurrence. Patients with an advanced disease stage (Kadish D) may have a higher likelihood of developing recurrence/progression. Furthermore, patients with tumor burden following resection (STR and Kadish D) may have worse OS. However, in positive-margin ONB with no gross disease following initial resection, the presence of disease recurrence does not significantly alter survival when receiving salvage therapy.