Faculty Bibliography

BACKGROUND:Aneurysms of the anterior choroidal artery (AChA) have been associated with high treatment-associated morbidity due to ischemic complications. OBJECTIVE:To report a large clinical experience of microsurgically treated AChA aneurysms and describe a systematic approach to reduce ischemic complications. METHODS:One hundred forty-six patients with AChA aneurysms were retrospectively reviewed from a prospectively maintained database. Clinical characteristics, surgical techniques, clinical outcomes, arterial infarction, and use of intraoperative adjuncts (ie, ultrasonography, indocyanine green videoangiography, and neuromonitoring) were analyzed. RESULTS:In total, one hundred forty-three aneurysms (97.9%) were clipped. Temporary clipping was utilized in 47 cases (32.2%) with mean occlusion time of 5.6 min. Arterial infarction occurred in 12 patients (8.2%). In clipped aneurysms, 90.5% were completely obliterated, 8.8% had minimal residual (<5% of original), and 0.7% were incompletely occluded (>5% of original). Mortality (2.7%) was limited to patients with high-grade subarachnoid hemorrhage. Indocyanine green videoangiography and neuromonitoring altered operative technique in ∼20% of cases. Multivariate logistic regression identified intraoperative rupture as the sole predictor for arterial infarction. CONCLUSION:Open microsurgical clipping remains a safe, effective treatment for AChA aneurysms. Microsurgical technique is paramount in preserving AChA patency and reducing ischemic complications. Despite increasing reliance on qualitative measures of AChA blood flow (videoangiography and ultrasonography) and neurophysiological monitoring, these technologies aid us infrequently. However, these adjuncts provide important safety checks for AChA patency. Temporary clipping must be used judiciously to lower the risk of intraoperative rupture while limiting possible ischemia in the AChA territory.

INTRODUCTION/BACKGROUND:Anterior inferior cerebellar artery (AICA) aneurysms are rare, accounting for 0.2%-1.3% of all intracranial aneurysms. The standard treatment is often endovascular embolization or neck clipping; however, sacrifice of the parent vessel is sometimes necessary. Addition of revascularization procedures is a subject of controversy. The occipital artery (OA) has been used as a donor for bypass, but recently there has been a trend toward intracranial-intracranial approaches. The posterior inferior cerebellar artery (PICA)-AICA side-to-side bypass may serve as a safe alternative. OBJECTIVE:To characterize the PICA-AICA side-to-side bypass and the OA-AICA end-to-side bypass and review the literature relevant to AICA revascularization. METHODS:We performed a far-lateral approach on 12 cadaveric specimens and analyzed the regional anatomy. On this basis, we performed either an OA-AICA or a PICA-AICA bypass and took morphometric measurements relevant to the technique. RESULTS:PICA-AICA bypass was successful in 6/12 specimens. The length of the flocculopeduncular segment was 42.6 ± 15.8 mm in the specimens in which the bypass was feasible and 26.2 ± 7.2 mm in those in which the bypass was not feasible (P = 0.04). Mean distance between AICA and PICA was 5.3 ± 4 mm in the specimens in which side-to-side bypass was feasible and 11.6 ± 4.2 mm in the specimens in which it was not (P = 0.02). OA-AICA end-to-side bypass was feasible in all the specimens (75% in the flocculopeduncular segment; 25% in the cortical segment). CONCLUSIONS:This is the first cadaveric study analyzing the PICA-AICA side-to-side bypass for AICA revascularization. Our analyses provide evidence for the feasibility of this bypass and document the anatomic variations that may indicate its use.

The neurovascular unit is composed of endothelial cells, vascular smooth muscle cells, pericytes, astrocytes and neurons. Through tightly regulated multi-directional cell signaling, the neurovascular unit is responsible for the numerous functionalities of the cerebrovasculature - including the regulation of molecular and cellular transport across the blood-brain barrier, angiogenesis, blood flow responses to brain activation and neuroinflammation. Historically, the study of the brain vasculature focused on endothelial cells; however, recent work has demonstrated that pericytes and vascular smooth muscle cells - collectively known as mural cells - play critical roles in many of these functions. Given this emerging data, a more complete mechanistic understanding of the cellular basis of brain vascular malformations is needed. In this review, we examine the integrated functions and signaling within the neurovascular unit necessary for normal cerebrovascular structure and function. We then describe the role of aberrant cell signaling within the neurovascular unit in brain arteriovenous malformations and identify how these pathways may be targeted therapeutically to eradicate or stabilize these lesions.

Dural arteriovenous fistulas (DAVFs) represent 10%-15% of all intracranial arteriovenous malformations.¹ DAVFs located in the posterior cranial fossa are rare and often present with intracranial hemorrhage and myelopathy.² Arterial supply could be provided by the meningeal branches of the vertebral artery and external and internal carotid arteries.³ A 68-year-old man presented with progressive lower-extremity weakness (Video 1). Magnetic resonance imaging revealed a patchy longitudinal cord signal abnormality extending from the cervicomedullary junction to C7. A tentorial DAVF supplied by the right posterior meningeal artery with drainage via dorsal and ventral perimedullary veins was identified on angiography. According to the Cognard classification, the patient's DAVF was determined to be high risk as a type V lesion with spinal venous drainage and progressive myelopathy.⁴ The fistula was embolized with 50% ethanol resulting in near-complete occlusion. However, follow-up angiography revealed a persistent arteriovenous shunt and slightly worsening symptoms for the patient. He underwent a sitting supracerebellar approach with a torcular craniotomy for successful clip ligation of the dural arteriovenous fistula. The patient was discharged with improvements in lower-extremity strength and no residual arteriovenous shunting in postoperative imaging.

A hyperplastic anterior choroidal artery is a vascular anomaly where the anterior choroidal artery supplies the posterior cerebral artery territory. We report a case of subarachnoid hemorrhage from a hyperplastic anterior choroidal artery with tandem fusiform aneurysms. The patient underwent a temporal craniotomy and transcortical transventricular transchoroidal-fissure approach for clip reconstruction. This case illustrates an unusual cerebrovascular pathology and approach to the ambient cistern.

OBJECTIVE:During the microsurgical clipping of known aneurysms, angiographically occult (AO) aneurysms are sometimes found and treated simultaneously to prevent their growth and protect the patient from future rupture or reoperation. The authors analyzed the incidence, treatment, and outcomes associated with AO aneurysms to determine whether limited surgical exploration around the known aneurysm was safe and justified given the known limitations of diagnostic angiography. METHODS:An AO aneurysm was defined as a saccular aneurysm detected using the operative microscope during dissection of a known aneurysm, and not detected on preoperative catheter angiography. A prospective database was retrospectively reviewed to identify patients with AO aneurysms treated microsurgically over a 20-year period. RESULTS:One hundred fifteen AO aneurysms (4.0%) were identified during 2867 distinct craniotomies for aneurysm clipping. The most common locations for AO aneurysms were the middle cerebral artery (60 aneurysms, 54.1%) and the anterior cerebral artery (20 aneurysms, 18.0%). Fifty-six AO aneurysms (50.5%) were located on the same artery as the known saccular aneurysm. Most AO aneurysms (95.5%) were clipped and there was no attributed morbidity. The most common causes of failed angiographic detection were superimposition of a large aneurysm (type 1, 30.6%), a small aneurysm (type 2, 18.9%), or an adjacent normal artery (type 3, 36.9%). Multivariate analysis identified multiple known aneurysms (odds ratio [OR] 3.45, 95% confidence interval [CI] 2.16-5.49, p < 0.0001) and young age (OR 0.981, 95% CI 0.965-0.997, p = 0.0226) as independent predictors of AO aneurysms. CONCLUSIONS:Meticulous inspection of common aneurysm sites within the surgical field will identify AO aneurysms during microsurgical dissection of another known aneurysm. Simultaneous identification and treatment of these additional undiagnosed aneurysms can spare patients later rupture or reoperation, particularly in those with multiple known aneurysms and a history of subarachnoid hemorrhage. Limited microsurgical exploration around a known aneurysm can be performed safely without additional morbidity.

OBJECTIVECerebral bypass procedures are microsurgical techniques to augment or restore cerebral blood flow when treating a number of brain vascular diseases including moyamoya disease, occlusive vascular disease, and cerebral aneurysms. With advances in endovascular therapy and evolving evidence-based guidelines, it has been suggested that cerebral bypass procedures are in a state of decline. Here, the authors characterize the national trends in cerebral bypass surgery in the United States from 2002 to 2014.METHODSUsing the National (Nationwide) Inpatient Sample, the authors extracted for analysis the data on all adult patients who had undergone cerebral bypass as indicated by ICD-9-CM procedure code 34.28. Indications for bypass procedures, patient demographics, healthcare costs, and regional variations are described. Results were stratified by indication for cerebral bypass including moyamoya disease, occlusive vascular disease, and cerebral aneurysms. Predictors of inpatient complications and death were evaluated using multivariable logistic regression analysis.RESULTSFrom 2002 to 2014, there was an increase in the annual number of cerebral bypass surgeries performed in the United States. This increase reflected a growth in the number of cerebral bypass procedures performed for adult moyamoya disease, whereas cases performed for occlusive vascular disease or cerebral aneurysms declined. Inpatient complication rates for cerebral bypass performed for moyamoya disease, vascular occlusive disease, and cerebral aneurysm were 13.2%, 25.1%, and 56.3%, respectively. Rates of iatrogenic stroke ranged from 3.8% to 20.4%, and mortality rates were 0.3%, 1.4%, and 7.8% for moyamoya disease, occlusive vascular disease, and cerebral aneurysms, respectively. Multivariate logistic regression confirmed that cerebral bypass for vascular occlusive disease or cerebral aneurysm is a statistically significant predictor of inpatient complications and death. Mean healthcare costs of cerebral bypass remained unchanged from 2002 to 20014 and varied with treatment indication: moyamoya disease $38,406 ± $483, vascular occlusive disease $46,618 ± $774, and aneurysm $111,753 ± $2381.CONCLUSIONSThe number of cerebral bypass surgeries performed for adult revascularization has increased in the United States from 2002 to 2014. Rising rates of surgical bypass reflect a greater proportion of surgeries performed for moyamoya disease, whereas bypasses performed for vascular occlusive disease and aneurysms are decreasing. Despite evolving indications, cerebral bypass remains an important surgical tool in the modern endovascular era and may be increasing in use. Stagnant complication rates highlight the need for continued interest in advancing available bypass techniques or technologies to improve patient outcomes.

OBJECTIVEBrain 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.METHODSTissues 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.RESULTSQuantitative 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.CONCLUSIONSBrain 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.