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I. Jonathan Pomeraniec, Dale Ding, Robert M. Starke, Kenneth C. Liu, E. Kelly Mrachek, M. Beatriz Lopes and Jason P. Sheehan

OBJECTIVE

Stereotactic radiosurgery (SRS) is a commonly employed treatment modality for brain arteriovenous malformations (AVMs). However, due to the low frequency of delayed cyst formation after AVM SRS, as well as the prolonged time interval between treatment and its occurrence, the characteristics of post-SRS cyst formation are not well defined. Therefore, the aims of this retrospective cohort study are to determine the rate of cyst formation after SRS for AVMs, identify predictive factors, and evaluate the clinical sequelae of post-SRS cysts.

METHODS

The authors analyzed an SRS database for AVM patients who underwent SRS at the University of Virginia and identified those who developed post-SRS cysts. Statistical analyses were performed to determine predictors of post-SRS cyst formation and the effect of cyst formation on new or worsening seizures after SRS.

RESULTS

The study cohort comprised 1159 AVM patients treated with SRS; cyst formation occurred in 17 patients (post-SRS cyst rate of 1.5%). Compared with patients who did not develop post-SRS cysts, those with cyst formation were treated with a greater number of radiosurgical isocenters (mean 3.8 vs 2.8, p = 0.047), had a longer follow-up (mean 132 vs 71 months, p < 0.001), were more likely to develop radiological radiation-induced changes (RIC) (64.7% vs 36.1%, p = 0.021), and had a longer duration of RIC (57 vs 21 months, p < 0.001). A higher number of isocenters (p = 0.014), radiological RIC (p = 0.002), and longer follow-up (p = 0.034) were found to be independent predictors of post-SRS cyst formation in the multivariate analysis. There was a trend toward a significant association between cyst formation and new or worsening seizures in univariate analysis (p = 0.054).

CONCLUSIONS

Patients with greater nidal complexity appear to be more prone to post-SRS cyst formation. The findings of this study emphasize the importance of long-term follow-up for patients who have undergone AVM SRS, even after nidal obliteration is achieved. Post-SRS cysts may be epileptogenic, although seizure outcomes after AVM SRS are multifactorial.

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Joseph S. Hudson, Yasunori Nagahama, Daichi Nakagawa, Robert M. Starke, Brian J. Dlouhy, James C. Torner, Pascal Jabbour, Lauren Allan, Colin P. Derdeyn, Jeremy D. W. Greenlee and David Hasan

OBJECTIVE

Intracranial stenting and flow diversion require the use of dual antiplatelet therapy (DAPT) to prevent in-stent thrombosis. DAPT may significantly increase the risk of hemorrhagic complications in patients who require subsequent surgical interventions. In this study, the authors sought to investigate whether DAPT is a risk factor for hemorrhagic complications associated with ventriculoperitoneal (VP) shunt placement in patients with aneurysmal subarachnoid hemorrhage (aSAH). Moreover, the authors sought to compare VP shunt complication rates with respect to the shunt’s location from the initial external ventricular drain (EVD) site.

METHODS

Patients with aSAH who presented to the authors’ institution from July 2009 through November 2016 and required VP shunt placement for persistent hydrocephalus were included. The rates of hemorrhagic complications associated with VP shunt placement were compared between patients who were on a regimen of DAPT (aspirin and clopidogrel) for use of a stent or flow diverter, and patients who underwent microsurgical clipping or coiling only and were not on DAPT using a backward stepwise multivariate analysis. Rates of radiographic hemorrhage and infection-related VP shunt revision were compared between patients who underwent VP shunt placement along the same track and those who underwent VP shunt placement at a different site (contralateral or posterior) from the initial EVD.

RESULTS

A total of 443 patients were admitted for the management of aSAH. Eighty of these patients eventually required VP shunt placement. Thirty-two patients (40%) had been treated with stent-assisted coiling or flow diverters and required DAPT, whereas 48 patients (60%) had been treated with coiling without stents or surgical clipping and were not on DAPT at the time of VP shunt placement. A total of 8 cases (10%) of new hemorrhage were observed along the intracranial proximal catheter of the VP shunt. Seven of these hemorrhages were observed in patients on DAPT, and 1 occurred in a patient not on DAPT. After multivariate analysis, only DAPT was significantly associated with hemorrhage (OR 31.23, 95% CI 2.98–327.32; p = 0.0001). One patient (3%) on DAPT who experienced hemorrhage required shunt revision for hemorrhage-associated proximal catheter blockage. The remaining 7 hemorrhages were clinically insignificant. The difference in rates of hemorrhage between shunt placement along the same track and placement at a different site of 0.07 was not significant (6/47 vs 2/32, p = 0.46). The difference in infection-related VP shunt revision rate was not significantly different (1/47 vs 3/32, p = 0.2978).

CONCLUSIONS

This clinical series confirms that, in patients with ruptured aneurysms who are candidates for stent-assisted coiling or flow diversion, the risk of clinically significant VP shunt–associated hemorrhage with DAPT is low. In an era of evolving endovascular therapeutics, stenting or flow diversion is a viable option in select aSAH patients.

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Allan D. Levi, Robert M. Starke, Ricardo J. Komotar and Robert E. Harbaugh

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Yasunori Nagahama, Lauren Allan, Daichi Nakagawa, Mario Zanaty, Robert M. Starke, Nohra Chalouhi, Pascal Jabbour, Robert D. Brown Jr., Colin P. Derdeyn, Enrique C. Leira, Joseph Broderick, Marc Chimowitz, James C. Torner and David Hasan

OBJECTIVE

Clinical vasospasm and delayed cerebral ischemia (DCI) are devastating complications of aneurysmal subarachnoid hemorrhage (aSAH). Several theories involving platelet activation have been postulated as potential explanations of the development of clinical vasospasm and DCI. However, the effects of dual antiplatelet therapy (DAPT; aspirin and clopidogrel) on clinical vasospasm and DCI have not been previously investigated. The objective of this study was to evaluate the effects of DAPT on clinical vasospasm and DCI in aSAH patients.

METHODS

Analysis of patients treated for aSAH during the period from July 2009 to April 2014 was performed in a single-institution retrospective study. Patients were divided into 2 groups: patients who underwent stent-assisted coiling or placement of flow diverters requiring DAPT (DAPT group) and patients who underwent coiling only without DAPT (control group). The frequency of symptomatic clinical vasospasm and DCI and of hemorrhagic complications was compared between the 2 groups, utilizing univariate and multivariate logistic regression.

RESULTS

Of 312 aSAH patients considered for this study, 161 met the criteria for inclusion and were included in the analysis (85 patients in the DAPT group and 76 patients in the control group). The risks of clinical vasospasm (OR 0.244, CI 95% 0.097–0.615, p = 0.003) and DCI (OR 0.056, CI 95% 0.01–0.318, p = 0.001) were significantly lower in patients receiving DAPT. The rates of hemorrhagic complications associated with placement of external ventricular drains and ventriculoperitoneal shunts were similar in both groups (4% vs 2%, p = 0.9).

CONCLUSIONS

The use of DAPT was associated with a lower risk of clinical vasospasm and DCI in patients treated for aSAH, without an increased risk of hemorrhagic complications.

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Christoph J. Griessenauer, Robert M. Starke, Paul M. Foreman, Philipp Hendrix, Mark R. Harrigan, Winfield S. Fisher III, Nilesh A. Vyas, Robert H. Lipsky, Mingkuan Lin, Beverly C. Walters, Jean-Francois Pittet and Mali Mathru

OBJECTIVE

Endothelin-1, a potent vasoconstrictor, and its receptors may be involved in the pathogenesis of aneurysmal subarachnoid hemorrhage (aSAH), clinical vasospasm, delayed cerebral ischemia (DCI), and functional outcome following aSAH. In the present study, common endothelin single nucleotide polymorphisms (SNPs) and their relation to aSAH were evaluated.

METHODS

Blood samples from all patients enrolled in the Cerebral Aneurysm Renin Angiotensin System (CARAS) study were used for genetic evaluation. The CARAS study prospectively enrolled patients with aSAH at 2 academic institutions in the US from 2012 to 2015. Common endothelin SNPs were detected using 5′ exonnuclease (TaqMan) genotyping assays. Analysis of associations between endothelin SNPs and aSAH and its clinical sequelae was performed.

RESULTS

Samples from 149 patients with aSAH and 50 controls were available for analysis. In multivariate logistic regression analysis, the TG (odds ratio [OR] 2.102, 95% confidence interval [CI] 1.048–4.218, p = 0.036) and TT genotypes (OR 7.884, 95% CI 1.003–61.995, p = 0.05) of the endothelin-1 T/G SNP (rs1800541) were significantly associated with aSAH. There was a dominant effect of the G allele (CG/GG genotypes; OR 4.617, 95% CI 1.311–16.262, p = 0.017) of the endothelin receptor A G/C SNP (rs5335) on clinical vasospasm. Endothelin SNPs were not associated with DCI or functional outcome.

CONCLUSIONS

Common endothelin SNPs were found to be associated with presentation with aSAH and clinical vasospasm. Further studies are required to elucidate the relevant pathophysiology and its potential implications in the treatment of patients with aSAH.

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David Hasan, Mario Zanaty, Robert M. Starke, Elias Atallah, Nohra Chalouhi, Pascal Jabbour, Amit Singla, Waldo R. Guerrero, Daichi Nakagawa, Edgar A. Samaniego, Nnenna Mbabuike, Rabih G. Tawk, Adnan H. Siddiqui, Elad I. Levy, Roberta L. Novakovic, Jonathan White, Clemens M. Schirmer, Thomas G. Brott, Hussain Shallwani and L. Nelson Hopkins

OBJECTIVE

The overall risk of ischemic stroke from a chronically occluded internal carotid artery (COICA) is around 5%–7% per year despite receiving the best available medical therapy. Here, authors propose a radiographic classification of COICA that can be used as a guide to determine the technical success and safety of endovascular recanalization for symptomatic COICA and to assess the changes in systemic blood pressure following successful revascularization.

METHODS

The radiographic images of 100 consecutive subjects with COICA were analyzed. A new classification of COICA was proposed based on the morphology, location of occlusion, and presence or absence of reconstitution of the distal ICA. The classification was used to predict successful revascularization in 32 symptomatic COICAs in 31 patients, five of whom were female (5/31 [16.13%]). Patients were included in the study if they had a COICA with ischemic symptoms refractory to medical therapy. Carotid artery occlusion was defined as 100% cross-sectional occlusion of the vessel lumen as documented on CTA or MRA and confirmed by digital subtraction angiography.

RESULTS

Four types (A–D) of radiographic COICA were identified. Types A and B were more amenable to safe revascularization than types C and D. Recanalization was successful at a rate of 68.75% (22/32 COICAs; type A: 8/8; type B: 8/8; type C: 4/8; type D: 2/8). The perioperative complication rate was 18.75% (6/32; type A: 0/8 [0%]; type B: 1/8 [12.50%]; type C: 3/8 [37.50%], type D: 2/8 [25.00%]). None of these complications led to permanent morbidity or death. Twenty (64.52%) of 31 subjects had improvement in their symptoms at the 2–6 months’ follow-up. A statistically significant decrease in systolic blood pressure (SBP) was noted in 17/21 (80.95%) patients who had successful revascularization, which persisted on follow-up (p = 0.0001). The remaining 10 subjects in whom revascularization failed had no significant changes in SBP (p = 0.73).

CONCLUSIONS

The pilot study suggested that our proposed classification of COICA may be useful as an adjunctive guide to determine the technical feasibility and safety of revascularization for symptomatic COICA using endovascular techniques. Additionally, successful revascularization may lead to a significant decrease in SBP postprocedure. A Phase 2b trial in larger cohorts to assess the efficacy of endovascular revascularization using our COICA classification is warranted.

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Dylan Russell, Travis Peck, Dale Ding, Ching-Jen Chen, Davis G. Taylor, Robert M. Starke, Cheng-Chia Lee and Jason P. Sheehan

OBJECTIVE

Embolization of brain arteriovenous malformations (AVMs) prior to stereotactic radiosurgery (SRS) has been reported to negatively affect obliteration rates. The goal of this systematic review and meta-analysis was to compare the outcomes of AVMs treated with embolization plus SRS (E+SRS group) and those of AVMs treated with SRS alone (SRS group).

METHODS

A literature review was performed using PubMed to identify studies with 10 or more AVM patients and obliteration data for both E+SRS and SRS groups. A meta-analysis was performed to compare obliteration rates between the E+SRS and SRS groups.

RESULTS

Twelve articles comprising 1716 patients were eligible for analysis. Among the patients with radiological follow-up data, complete obliteration was achieved in 48.4% of patients (330/681) in the E+SRS group compared with 62.7% of patients (613/978) in the SRS group. A meta-analysis of the pooled data revealed that the obliteration rate was significantly lower in the E+SRS group (OR 0.51, 95% CI 0.41–0.64, p < 0.00001). Symptomatic adverse radiation effects were observed in 6.6% (27/412 patients) and 11.1% (48/433 patients) of the E+SRS and SRS groups, respectively. The annual post-SRS hemorrhage rate was 2.0%–6.5% and 0%–2.0% for the E+SRS and SRS groups, respectively. The rates of permanent morbidity were 0%–6.7% and 0%–13.5% for the E+SRS and SRS groups, respectively.

CONCLUSIONS

Arteriovenous malformation treatment with combined embolization and SRS is associated with lower obliteration rates than those with SRS treatment alone. However, this comparison does not fully account for differences in the initial AVM characteristics in the E+SRS group as compared with those in the SRS group. Further studies are warranted to address these limitations.

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Badih Daou, Elias Atallah, Nohra Chalouhi, Robert M. Starke, Jeffrey Oliver, Maria Montano, Pascal Jabbour, Robert H. Rosenwasser and Stavropoula I. Tjoumakaris

OBJECTIVE

The Pipeline embolization device (PED) has become a valuable tool in the treatment of cerebral aneurysms. Although failures with PED treatment have been reported, the characteristics and course of these aneurysms remain a topic of uncertainty.

METHODS

Electronic medical records and imaging studies were reviewed for all patients treated with the PED between July 2010 and March 2015 to identify characteristics of patients and aneurysms with residual filling after PED treatment.

RESULTS

Of 316 cases treated at a single institution, 281 patients had a long-term follow-up. A total of 52 (16.4%) aneurysms with residual filling were identified and constituted the study population. The mean patient age in this population was 58.8 years. The mean aneurysm size was 10.1 mm ± 7.15 mm. Twelve aneurysms were fusiform (23%). Of the aneurysms with residual filling, there were 20 carotid ophthalmic (CO) aneurysms (20% of all CO aneurysms treated), 10 other paraclinoid aneurysms (16.4% of all paraclinoid aneurysms), 7 posterior communicating artery (PCoA) aneurysms (21.9% of all PCoA aneurysms), 7 cavernous internal carotid artery (ICA) aneurysms (14.9% of all cavernous ICA aneurysms), 4 vertebrobasilar (VB) junction aneurysms (14.8% of all VB junction aneurysms), and 3 middle cerebral artery (MCA) aneurysms (25% of all MCA aneurysms). Eleven patients underwent placement of more than one PED (21.2%), with a mean number of devices of 1.28 per case. Eight of 12 aneurysms were previously treated with a stent (15.4%). Nineteen patients underwent re-treatment (36.5%); the 33 patients who did not undergo re-treatment (63.5%) were monitored by angiography or noninvasive imaging. In multivariate analysis, age older than 65 years (OR 2.65, 95% CI 1.33–5.28; p = 0.05), prior stent placement across the target aneurysm (OR 2.94, 95% CI 1.15–7.51; p = 0.02), aneurysm location in the distal anterior circulation (MCA, PCoA, and anterior choroidal artery: OR 2.72, 95% CI 1.19–6.18; p = 0.017), and longer follow-up duration (OR 1.06, 95% CI 1.03–1.09; p < 0.001) were associated with incomplete aneurysm occlusion.

CONCLUSIONS

While the PED can allow for treatment of large, broad-necked aneurysms with high efficacy, treatment failures do occur (16.4%). Aneurysm size, shape, and previous treatment may influence treatment outcome.

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George M. Ghobrial, Michael Y. Wang, Barth A. Green, Howard B. Levene, Glen Manzano, Steven Vanni, Robert M. Starke, George Jimsheleishvili, Kenneth M. Crandall, Marina Dididze and Allan D. Levi

OBJECTIVE

The aim of this study was to determine the efficacy of 2 common preoperative surgical skin antiseptic agents, ChloraPrep and Betadine, in the reduction of postoperative surgical site infection (SSI) in spinal surgery procedures.

METHODS

Two preoperative surgical skin antiseptic agents—ChloraPrep (2% chlorhexidine gluconate and 70% isopropyl alcohol) and Betadine (7.5% povidone-iodine solution)—were prospectively compared across 2 consecutive time periods for all consecutive adult neurosurgical spine patients. The primary end point was the incidence of SSI.

RESULTS

A total of 6959 consecutive spinal surgery patients were identified from July 1, 2011, through August 31, 2015, with 4495 (64.6%) and 2464 (35.4%) patients treated at facilities 1 and 2, respectively. Sixty-nine (0.992%) SSIs were observed. There was no significant difference in the incidence of infection between patients prepared with Betadine (33 [1.036%] of 3185) and those prepared with ChloraPrep (36 [0.954%] of 3774; p = 0.728). Neither was there a significant difference in the incidence of infection in the patients treated at facility 1 (52 [1.157%] of 4495) versus facility 2 (17 [0.690%] of 2464; p = 0.06). Among the patients with SSI, the most common indication was degenerative disease (48 [69.6%] of 69). Fifty-one (74%) patients with SSI had undergone instrumented fusions in the index operation, and 38 (55%) patients with SSI had undergone revision surgeries. The incidence of SSI for minimally invasive and open surgery was 0.226% (2 of 885 cases) and 1.103% (67 of 6074 cases), respectively.

CONCLUSIONS

The choice of either ChloraPrep or Betadine for preoperative skin antisepsis in spinal surgery had no significant impact on the incidence of postoperative SSI.

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Mohana Rao Patibandla, Dale Ding, Hideyuki Kano, Robert M. Starke, John Y. K. Lee, David Mathieu, Jamie Whitesell, John T. Pierce, Paul P. Huang, Douglas Kondziolka, Caleb Feliciano, Rafael Rodriguez-Mercado, Luis Almodovar, Inga S. Grills, Danilo Silva, Mahmoud Abbassy, Symeon Missios, Gene H. Barnett, L. Dade Lunsford and Jason P. Sheehan

OBJECTIVE

The role of and technique for stereotactic radiosurgery (SRS) in the management of arteriovenous malformations (AVMs) have evolved over the past four decades. The aim of this multicenter, retrospective cohort study was to compare the SRS outcomes of AVMs treated during different time periods.

METHODS

The authors selected patients with AVMs who underwent single-session SRS at 8 different centers from 1988 to 2014 with follow-up ≥ 6 months. The SRS eras were categorized as early (1988–2000) or modern (2001–2014). Statistical analyses were performed to compare the baseline characteristics and outcomes of the early versus modern SRS eras. Favorable outcome was defined as AVM obliteration, no post-SRS hemorrhage, and no permanently symptomatic radiation-induced changes (RICs).

RESULTS

The study cohort comprised 2248 patients with AVMs, including 1584 in the early and 664 in the modern SRS eras. AVMs in the early SRS era were significantly smaller (p < 0.001 for maximum diameter and volume), and they were treated with a significantly higher radiosurgical margin dose (p < 0.001). The obliteration rate was significantly higher in the early SRS era (65% vs 51%, p < 0.001), and earlier SRS treatment period was an independent predictor of obliteration in the multivariate analysis (p < 0.001). The rates of post-SRS hemorrhage and radiological, symptomatic, and permanent RICs were not significantly different between the two groups. Favorable outcome was achieved in a significantly higher proportion of patients in the early SRS era (61% vs 45%, p < 0.001), but the earlier SRS era was not statistically significant in the multivariate analysis (p = 0.470) with favorable outcome.

CONCLUSIONS

Despite considerable advances in SRS technology, refinement of AVM selection, and contemporary multimodality AVM treatment, the study failed to observe substantial improvements in SRS favorable outcomes or obliteration for patients with AVMs over time. Differences in baseline AVM characteristics and SRS treatment parameters may partially account for the significantly lower obliteration rates in the modern SRS era. However, improvements in patient selection and dose planning are necessary to optimize the utility of SRS in the contemporary management of AVMs.