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Tomoya Kamide, Halima Tabani, Michael M. Safaee, Jan-Karl Burkhardt and Michael T. Lawton

OBJECTIVE

While most paraclinoid aneurysms can be clipped with excellent results, new postoperative visual deficits are a concern. New technology, including flow diverters, has increased the popularity of endovascular therapy. However, endovascular treatment of paraclinoid aneurysms is not without procedural risks, is associated with higher rates of incomplete aneurysm occlusion and recurrence, and may not address optic nerve compression symptoms that surgical debulking can. The increasing endovascular management of paraclinoid aneurysms should be justified by comparisons to surgical benchmarks. The authors, therefore, undertook this study to define patient, visual, and aneurysm outcomes in the most common type of paraclinoid aneurysm: ophthalmic artery (OphA) aneurysms.

METHODS

Results from microsurgical clipping of 208 OphA aneurysms in 198 patients were retrospectively reviewed. Patient demographics, aneurysm morphology (size, calcification, etc.), clinical characteristics, and patient outcomes were recorded and analyzed.

RESULTS

Despite 20% of these aneurysms being large or giant in size, complete aneurysm occlusion was accomplished in 91% of 208 cases, with OphA patency preserved in 99.5%. The aneurysm recurrence rate was 3.1% and the retreatment rate was 0%. Good outcomes (modified Rankin Scale score 0–2) were observed in 96.2% of patients overall and in all 156 patients with unruptured aneurysms. New visual field defects (hemianopsia or quadrantanopsia) were observed in 8 patients (3.8%), decreased visual acuity in 5 (2.4%), and monocular blindness in 9 (4.3%). Vision improved in 9 (52.9%) of the 17 patients with preoperative visual deficits.

CONCLUSIONS

The most important risk associated with clipping OphA aneurysms is a new visual deficit. Meticulous microsurgical technique is necessary during anterior clinoidectomy, aneurysm dissection, and clip application to optimize visual outcomes, and aggressive medical management postoperatively might potentially decrease the incidence of delayed visual deficits. As the results of endovascular therapy and specifically flow diverters become known, they warrant comparison with these surgical benchmarks to determine best practices.

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Ethan A. Winkler, Harjus Birk, Jan-Karl Burkhardt, Xiaolin Chen, John K. Yue, Diana Guo, W. Caleb Rutledge, George F. Lasker, Carlene Partow, Tarik Tihan, Edward F. Chang, Hua Su, Helen Kim, Brian P. Walcott and Michael T. Lawton

OBJECTIVE

Brain arteriovenous malformations (bAVMs) are rupture-prone tangles of blood vessels with direct shunting of blood flow between arterial and venous circulations. The molecular and/or cellular mechanisms contributing to bAVM pathogenesis and/or destabilization in sporadic lesions have remained elusive. Initial insights into AVM formation have been gained through models of genetic AVM syndromes. And while many studies have focused on endothelial cells, the contributions of other vascular cell types have yet to be systematically studied. Pericytes are multifunctional mural cells that regulate brain angiogenesis, blood-brain barrier integrity, and vascular stability. Here, the authors analyze the abundance of brain pericytes and their association with vascular changes in sporadic human AVMs.

METHODS

Tissues from bAVMs and from temporal lobe specimens from patients with medically intractable epilepsy (nonvascular lesion controls [NVLCs]) were resected. Immunofluorescent staining with confocal microscopy was performed to quantify pericytes (platelet-derived growth factor receptor–beta [PDGFRβ] and aminopeptidase N [CD13]) and extravascular hemoglobin. Iron-positive hemosiderin deposits were quantified with Prussian blue staining. Syngo iFlow post–image processing was used to measure nidal blood flow on preintervention angiograms.

RESULTS

Quantitative immunofluorescent analysis demonstrated a 68% reduction in the vascular pericyte number in bAVMs compared with the number in NVLCs (p < 0.01). Additional analysis demonstrated 52% and 50% reductions in the vascular surface area covered by CD13- and PDGFRβ-positive pericyte cell processes, respectively, in bAVMs (p < 0.01). Reductions in pericyte coverage were statistically significantly greater in bAVMs with prior rupture (p < 0.05). Unruptured bAVMs had increased microhemorrhage, as evidenced by a 15.5-fold increase in extravascular hemoglobin compared with levels in NVLCs (p < 0.01). Within unruptured bAVM specimens, extravascular hemoglobin correlated negatively with pericyte coverage (CD13: r = −0.93, p < 0.01; PDGFRβ: r = −0.87, p < 0.01). A similar negative correlation was observed with pericyte coverage and Prussian blue–positive hemosiderin deposits (CD13: r = −0.90, p < 0.01; PDGFRβ: r = −0.86, p < 0.01). Pericyte coverage positively correlated with the mean transit time of blood flow or the time that circulating blood spends within the bAVM nidus (CD13: r = 0.60, p < 0.05; PDGFRβ: r = 0.63, p < 0.05). A greater reduction in pericyte coverage is therefore associated with a reduced mean transit time or faster rate of blood flow through the bAVM nidus. No correlations were observed with time to peak flow within feeding arteries or draining veins.

CONCLUSIONS

Brain pericyte number and coverage are reduced in sporadic bAVMs and are lowest in cases with prior rupture. In unruptured bAVMs, pericyte reductions correlate with the severity of microhemorrhage. A loss of pericytes also correlates with a faster rate of blood flow through the bAVM nidus. This suggests that pericytes are associated with and may contribute to vascular fragility and hemodynamic changes in bAVMs. Future studies in animal models are needed to better characterize the role of pericytes in AVM pathogenesis.

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Jan-Karl Burkhardt, George F. Lasker, Ethan A. Winkler, Helen Kim and Michael T. Lawton

As the population ages, the question of how to manage brain arteriovenous malformations in the elderly becomes increasingly relevant. Is resection a reasonable option for these patients? In this study, the authors examined the outcomes of surgical patients 60 years or older and found that favorable outcomes were achieved with careful patient selection. Preoperative grading scales were more predictive of outcomes in patients older than 65 years than in those 60–65 years of age.

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Ethan A. Winkler, Jan-Karl Burkhardt, W. Caleb Rutledge, Jonathan W. Rick, Carlene P. Partow, John K. Yue, Harjus Birk, Ashley M. Bach, Kunal P. Raygor and Michael T. Lawton

OBJECTIVE

Shunt-dependent hydrocephalus is an important cause of morbidity following aneurysmal subarachnoid hemorrhage (aSAH) in excess of 20% of cases. Hydrocephalus leads to prolonged hospital and ICU stays, well as to repeated surgical interventions, readmissions, and complications associated with ventriculoperitoneal (VP) shunts, including shunt failure and infection. Whether variations in surgical technique at the time of aneurysm treatment may modify rates of shunt dependency remains a matter of debate. Here, the authors report on their experience with tandem fenestration of the lamina terminalis (LT) and membrane of Liliequist (MoL) at the time of open microsurgical repair of the ruptured aneurysm.

METHODS

The authors conducted a retrospective review of 663 consecutive patients with aSAH treated from 2005 to 2015 by open microsurgery via a pterional or orbitozygomatic craniotomy by the senior author (M.T.L.). Data collected from review of the electronic medical record included age, Hunt and Hess grade, Fisher grade, need for an external ventricular drain, and opening pressure. Patients were stratified into those undergoing no fenestration and those undergoing tandem fenestration of the LT and MoL at the time of surgical repair. Outcome variables, including VP shunt placement and timing of shunt placement, were recorded and statistically analyzed.

RESULTS

In total, shunt-dependent hydrocephalus was observed in 15.8% of patients undergoing open surgical repair following aSAH. Tandem microsurgical fenestration of the LT and MoL was associated with a statistically significant reduction in shunt dependency (17.9% vs 3.2%, p < 0.01). This effect was confirmed with multivariate analysis of collected variables (multivariate OR 0.09, 95% CI 0.03–0.30). Number-needed-to-treat analysis demonstrated that tandem fenestration was required in approximately 6.8 patients to prevent a single VP shunt placement. A statistically significant prolongation in days to VP shunt surgery was also observed in patients treated with tandem fenestration (26.6 ± 19.4 days vs 54.0 ± 36.5 days, p < 0.05).

CONCLUSIONS

Tandem fenestration of the LT and MoL at the time of open microsurgical clipping and/or bypass to secure ruptured anterior and posterior circulation aneurysms is associated with reductions in shunt-dependent hydrocephalus following aSAH. Future prospective randomized multicenter studies are needed to confirm this result.

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Gyang Markus Bot, Jan-Karl Burkhardt, Nalin Gupta and Michael T. Lawton

Analysis of direct STA-MCA bypass procedures in young children to achieve flow augmentation via direct revascularization.

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Justin R. Mascitelli, Seungwon Yoon, Tyler S. Cole, Helen Kim and Michael T. Lawton

OBJECTIVE

Although numerous arteriovenous malformation (AVM) grading scales consider eloquence in risk assessment, none differentiate the types of eloquence. The purpose of this study was to determine if eloquence subtype affects clinical outcome.

METHODS

This is a retrospective review of a prospectively collected clinical database of brain AVMs treated with microsurgery in the period from 1997 to 2017. The only inclusion criterion for this study was the presence of eloquence as defined by the Spetzler-Martin grading scale. Eloquence was preoperatively categorized by radiologists. Poor outcome was defined as a modified Rankin Scale (mRS) score 3–6, and worsening clinical status was defined as an increase in the mRS score at follow-up. Logistic regression analyses were performed.

RESULTS

Two hundred forty-one patients (49.4% female; average age 33.9 years) with eloquent brain AVMs were included in this review. Of the AVMs (average size 2.7 cm), 54.4% presented with hemorrhage, 46.2% had deep venous drainage, and 17.0% were diffuse. The most common eloquence type was sensorimotor (46.1%), followed by visual (27.0%) and language (22.0%). Treatments included microsurgery alone (32.8%), microsurgery plus embolization (51.9%), microsurgery plus radiosurgery (7.9%), and all three modalities (7.5%). Motor mapping was used in 9% of sensorimotor AVM cases, and awake speech mapping was used in 13.2% of AVMs with language eloquence. Complications occurred in 24 patients (10%). At the last follow-up (average 24 months), 71.4% of the patients were unchanged or improved and 16.6% had a poor outcome. There was no statistically significant difference in the baseline patient and AVM characteristics among the different subtypes of eloquence. In a multivariate analysis, in comparison to visual eloquence, both sensorimotor (OR 7.4, p = 0.004) and language (OR 6.5, p = 0.015) eloquence were associated with poor outcomes. Additionally, older age (OR 1.31, p = 0.016) and larger AVM size (OR 1.37, p = 0.034) were associated with poor outcomes.

CONCLUSIONS

Unlike visual eloquence, sensorimotor and language eloquence were associated with worse clinical outcomes after the resection of eloquent AVMs. This nuance in AVM eloquence demands consideration before deciding on microsurgical intervention, especially when numerical grading systems produce a score near the borderline between operative and nonoperative management.

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M. Yashar S. Kalani, Michael T. Lawton and Robert F. Spetzler

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André Beer-Furlan, Diego A. Servián, Ricardo L. Carrau and Daniel M. Prevedello

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Ali Tayebi Meybodi, Arnau Benet and Michael T. Lawton

The V3 segment of the vertebral artery (VA) has been studied in various clinical scenarios, such as in tumors of the craniovertebral junction and dissecting aneurysms. However, its use as a donor artery in cerebral revascularization procedures has not been extensively studied. In this report, the authors summarize their clinical experience in cerebral revascularization procedures using the V3 segment as a donor. A brief anatomical description of the relevant techniques is also provided.

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Seungwon Yoon, Jan-Karl Burkhardt and Michael T. Lawton

OBJECTIVE

Large cohort analysis concerning intracerebral bypass patency in patients with long-term follow-up (FU) results is rarely reported in the literature. The authors analyzed the long-term patency of extracranial-to-intracranial (EC-IC) and intracranial-to-intracranial (IC-IC) bypass procedures.

METHODS

All intracranial bypass procedures performed between 1997 and 2017 by a single surgeon were screened. Patients with postoperative imaging (CT angiography, MR angiography, or catheter angiography) were included and grouped into immediate (< 7 days), short-term (7 days–1 year), and long-term (> 1 year) FU groups. Data on patient demographics, bypass type, interposition graft type, bypass indication, and radiological patency were collected and analyzed with univariate and multivariate (adjusted multiple regression) models.

RESULTS

In total, 430 consecutive bypass procedures were performed during the study period (FU time [mean ± SD] 0.9 ± 2.2 years, range 0–17 years). Twelve cases were occluded at FU imaging, resulting in an overall cumulative patency rate of 97%. All bypass occlusions occurred within a week of revascularization. All patients in the short-term FU group (n = 76, mean FU time 0.3 ± 0.3 years) and long-term FU group (n = 89, mean FU time 4.1 ± 3.5 years) had patent bypasses at last FU. Patients who presented with aneurysms had a lower rate of patency than those with moyamoya disease or chronic vessel occlusion (p = 0.029). Low-flow bypasses had a significantly higher patency rate than high-flow bypasses (p = 0.033). In addition, bypasses with one anastomosis site compared to two anastomosis sites showed a significantly higher bypass patency (p = 0.005). No differences were seen in the patency rate among different grafts, single versus bilateral, or between EC-IC and IC-IC bypasses.

CONCLUSIONS

The overall bypass patency of 97% indicates a high likelihood of success with microsurgical revascularization. Surgical indication (ischemia), low-flow bypass, and number of anastomosis (one site) were associated with higher patency rates. EC-IC and IC-IC bypasses have comparable patency rates, supporting the use of intracranial reconstructive techniques. Bypasses that remain patent 1 week postoperatively and have the opportunity to mature have a high likelihood of remaining patent in the long term. In experienced hands, cerebral revascularization is a durable treatment option with high patency rates.