Does disease etiology matter in long-term patency in extracranial-intracranial bypass?

OBJECTIVE: Extracranial-intracranial (EC-IC) bypass has been well described in chronic vaso-occlusive cerebrovascular diseases, including both moyamoya disease (MMD) and atherosclerotic disease (AD). This study aimed to compare factors associated with bypass occlusion between these two diseases. METHODS: An institutional database of 357 patients with intracranial bypass procedures performed between August 2001 and May 2022 was retrospectively reviewed. Patients with MMD and AD were selected for study. Baseline characteristics, surgical technique, and flow-related measurements were compared in relation to the outcome of bypass occlusion. RESULTS: A total of 232 patients met inclusion criteria (AD, n = 108; MMD, n = 124). The average age and sex differed significantly between groups (AD 57.2 years, 56.5% male; MMD 36.6 years, 31.5% male; p < 0.001). The modified Rankin Scale scores at surgery and at follow-up were higher in the AD group (p = 0.004 and p < 0.001, respectively), showing a slightly worse baseline functional status, and higher rates of stroke were observed in the AD group by last follow-up (p = 0.005). Patients with AD also were more likely to require an interpositional graft (p < 0.001). At last follow-up, rates of occlusion did not differ between AD and MMD groups (25.2% vs 25.4%, respectively). Of occluded bypasses, the AD group had more occlusions within 1 week compared to MMD (51.9% vs 35.5%, p = 0.176), although the difference was not significant. In patients with more than 1 year of follow-up and in those with more than 2 years of follow-up, MMD tended to have higher rates of occlusion (31.2% vs 26.1% [p = 0.558], and 26.4% vs 20.7% [p = 0.564]). Flow measurements did not differ between AD and MMD groups, but in subgroup analyses of patients with AD and those with MMD, both bypass flow and cut flow index predicted occlusion in both groups. CONCLUSIONS: Despite different disease etiologies treated with bypass, rates of occlusion at last follow-up did not vary between groups, although short-term follow-up would suggest earlier bypass failure in AD, and extended follow-up trended toward higher occlusion rates in MMD. Additionally, patients with AD were more likely to have further occurrences of stroke by last follow-up. Importantly, the bypass flow and cut flow index at the time of surgery predicted occlusion in both AD and MMD.

Complex intracranial aneurysms: a DELPHI study to define associated characteristics.

PURPOSE: Intracranial aneurysms present significant health risks, as their rupture leads to subarachnoid haemorrhage, which in turn has high morbidity and mortality rates. There are several elements affecting the complexity of an intracranial aneurysm. However, criteria for defining a complex intracranial aneurysm (CIA) in open surgery and endovascular treatment could differ, and actually there is no consensus on the definition of a "complex" aneurysm. This DELPHI study aims to assess consensus on variables defining a CIA. METHODS: An international panel of 50 members, representing various specialties, was recruited to define CIAs through a three-round Delphi process. The panelists participated in surveys with Likert scale responses and open-ended questions. Consensus criteria were established to determine CIA variables, and statistical analysis evaluated consensus and stability. RESULTS: In open surgery, CIAs were defined by fusiform or blister-like shape, dissecting aetiology, giant size (≥ 25 mm), broad neck encasing parent arteries, extensive neck surface, wall calcification, intraluminal thrombus, collateral branch from the sac, location (AICA, SCA, basilar), vasospasm context, and planned bypass (EC-IC or IC-IC). For endovascular treatment, CIAs included giant size, very wide neck (dome/neck ratio ≤ 1:1), and collateral branch from the sac. CONCLUSIONS: The definition of aneurysm complexity varies by treatment modality. Since elements related to complexity differ between open surgery and endovascular treatment, these consensus criteria of CIAs could even guide in selecting the best treatment approach.

Description of the local hemodynamic environment in intracranial aneurysm wall subdivisions.

Intracranial aneurysms (IAs) pose severe health risks influenced by hemodynamics. This study focuses on the intricate characterization of hemodynamic conditions within the IA walls and their influence on bleb development, aiming to enhance understanding of aneurysm stability and the risk of rupture. The methods emphasized utilizing a comprehensive dataset of 359 IAs and 213 IA blebs from 268 patients to reconstruct patient-specific vascular models, analyzing blood flow using finite element methods to solve the unsteady Navier-Stokes equations, the segmentation of aneurysm wall subregions and the hemodynamic metrics wall shear stress (WSS), its metrics, and the critical points in WSS fields were computed and analyzed across different aneurysm subregions defined by saccular, streamwise, and topographical divisions. The results revealed significant variations in these metrics, correlating distinct hemodynamic environments with wall features on the aneurysm walls, such as bleb formation. Critical findings indicated that regions with low WSS and high OSI, particularly in the body and central regions of aneurysms, are prone to conditions that promote bleb formation. Conversely, areas exposed to high WSS and positive divergence, like the aneurysm neck, inflow, and outflow regions, exhibited a different but substantial risk profile for bleb development, influenced by flow impingements and convergences. These insights highlight the complexity of aneurysm behavior, suggesting that both high and low-shear environments can contribute to aneurysm pathology through distinct mechanisms.

Transcallosal Retroforniceal Transchoroidal Approach: To the Posterior Third Ventricle and Beyond.

BACKGROUND: The transcallosal retroforniceal transchoroidal approach represents an advanced neurosurgical technique that allows access to lesions located within the posterior third ventricle and mesencephalon. It relies on a comprehensive understanding of microsurgical anatomy and embryology, integrating modern neurosurgical operative techniques to minimize retraction and injury to the normal neuronal structures. METHODS: We report the cases of 2 patients undergoing treatment via this approach, one presenting with a thalamic cavernoma and the other with cystic low-grade glioma of the midbrain. RESULTS: In these 2 cases, the decision to use the transcallosal approach was mainly due to improved trajectory, gravitational retraction of the hemisphere, and improved delivery of the lesion into the operative field by gravity alone. CONCLUSIONS: Through a detailed description of the surgical approach and anatomy, we illustrate the feasibility of the transcallosal retroforniceal transchoroidal approach for accessing lesions located deeply in the brain.

Neuropsychological Test Performance Differentiates Subgroups of Individuals With Adult Moyamoya Disease: A Cross-Sectional Clinical Study.

BACKGROUND AND OBJECTIVES: Moyamoya disease (MMD) is a rare noninflammatory disorder involving progressive intracranial vasculopathy and impaired cerebral blood flow in the anterior circulation, resulting in stroke and cognitive impairment. We aimed to characterize cognitive impairment and the possible predictive value of sociodemographic and clinical characteristics of adults with MMD. METHODS: This cross-sectional study examined neurocognitive performance in a group of 42 consecutive adult patients (mean age = 40.52 years; 69% female) referred for a presurgical neuropsychological evaluation. Neuropsychological functioning was assessed with a comprehensive battery, and cognitive dysfunction was defined as 1.5 SDs below the mean. Neurocognitive performance correlated with clinical/demographic characteristics and disease markers. RESULTS: Most patients (91%) had a history of stroke, and 45% had cognitive deficits, most notably on measures of attention/speed (48%), executive functioning (47%), visuoconstruction (41%), and memory (31%-54%). Only higher educational attainment and poor collateral blood flow in the right hemisphere differentiated cognitively impaired (n = 19) and intact groups (n = 23), and MMD-related characteristics (eg, disease duration, stroke history) did not differentiate the 2 groups. CONCLUSION: Consistent with previous work, frontal-subcortical cognitive deficits (eg, deficits in mental speed, attention, executive functioning) were found in nearly half of patients with MMD and better cognitive performance was associated with factors related to cognitive reserve. Angiographic metrics of disease burden (eg, Suzuki rating, collateral flow) and hemodynamic reserve were not consistently associated with poorer cognitive outcomes, suggesting that cognition is a crucial independent factor to assess in MMD and has relevance for treatment planning and functional status.

Distribution of rupture sites and blebs on intracranial aneurysm walls suggests distinct rupture patterns in ACom and MCA aneurysms.

The mechanisms behind intracranial aneurysm formation and rupture are not fully understood, with factors such as location, patient demographics, and hemodynamics playing a role. Additionally, the significance of anatomical features like blebs in ruptures is debated. This highlights the necessity for comprehensive research that combines patient-specific risk factors with a detailed analysis of local hemodynamic characteristics at bleb and rupture sites. Our study analyzed 359 intracranial aneurysms from 268 patients, reconstructing patient-specific models for hemodynamic simulations based on 3D rotational angiographic images and intraoperative videos. We identified aneurysm subregions and delineated rupture sites, characterizing blebs and their regional overlap, employing statistical comparisons across demographics, and other risk factors. This work identifies patterns in aneurysm rupture sites, predominantly at the dome, with variations across patient demographics. Hypertensive and anterior communicating artery (ACom) aneurysms showed specific rupture patterns and bleb associations, indicating two pathways: high-flow in ACom with thin blebs at impingement sites and low-flow, oscillatory conditions in middle cerebral artery (MCA) aneurysms fostering thick blebs. Bleb characteristics varied with gender, age, and smoking, linking rupture risks to hemodynamic factors and patient profiles. These insights enhance understanding of the hemodynamic mechanisms leading to rupture events. This analysis elucidates the role of localized hemodynamics in intracranial aneurysm rupture, challenging the emphasis on location by revealing how flow variations influence stability and risk. We identify two pathways to wall failure-high-flow and low-flow conditions-highlighting the complexity of aneurysm behavior. Additionally, this research advances our knowledge of how inherent patient-specific characteristics impact these processes, which need further investigation.

Occipital artery to vertebral artery bypass for treatment of bilateral vertebral artery occlusion with QMRA as an adjunct to diagnostic assessment.

PURPOSE: Stroke, the second leading cause of death globally, often involves ischemia in the vertebrobasilar territory. This condition is underexplored, despite significant morbidity and mortality risks. The purpose of this study is to present a case of occipital artery to V3 segment vertebral artery bypass, emphasizing the role of quantitative magnetic resonance angiography (qMRA) in assessing flow and guiding surgical intervention. METHODS: A 66-year-old man with bilateral vertebral artery occlusion presented acute symptoms. qMRA was employed to evaluate flow dynamics and determine the feasibility of a flow augmentation bypass surgery. The occipital artery to left vertebral artery bypass (OA-to-VA) was performed, utilizing an inverted hockey-stick incision and an antegrade inside-out technique. The patency of the bypass was confirmed using both Doppler probe and Indocyanine green. RESULTS: Postoperative assessments, including computed tomography angiography (CTA) and qMRA, demonstrated the patency of the bypass with improved flow in the basilar artery and left vertebral artery. The patient's condition remained stable postoperatively, with residual peripheral palsy of the left facial nerve. CONCLUSION: In conclusion, the presented case illustrates the efficacy of the OA-to-VA bypass in addressing symptomatic bilateral vertebral artery occlusion. The study underscores the pivotal role of qMRA in pre- and postoperative assessments, providing noninvasive flow quantification for diagnostic considerations and long-term follow-up in patients with vertebrobasilar insufficiency.

Most Promising Approaches to Improve Brain AVM Management: ARISE I Consensus Recommendations.

Brain arteriovenous malformations (bAVMs) are complex, and rare arteriovenous shunts that present with a wide range of signs and symptoms, with intracerebral hemorrhage being the most severe. Despite prior societal position statements, there is no consensus on the management of these lesions. ARISE (Aneurysm/bAVM/cSDH Roundtable Discussion With Industry and Stroke Experts) was convened to discuss evidence-based approaches and enhance our understanding of these complex lesions. ARISE identified the need to develop scales to predict the risk of rupture of bAVMs, and the use of common data elements to perform prospective registries and clinical studies. Additionally, the group underscored the need for comprehensive patient management with specialized centers with expertise in cranial and spinal microsurgery, neurological endovascular surgery, and stereotactic radiosurgery. The collection of prospective multicenter data and gross specimens was deemed essential for improving bAVM characterization, genetic evaluation, and phenotyping. Finally, bAVMs should be managed within a multidisciplinary framework, with clinical studies and research conducted collaboratively across multiple centers, harnessing the collective expertise and centralization of resources.

A patient-specific circle of Willis blood flow model in predicting outcomes of balloon test occlusion.

BACKGROUND AND PURPOSE: Balloon test occlusion (BTO) evaluates cerebral ischemic tolerance before internal carotid artery (ICA) sacrifice but carries risks like dissection and thrombosis. This study introduces a new approach using a patient-specific circle of Willis (COW) blood flow model, based on non-invasive quantitative MR angiography (qMRA) measurements, to predict the outcomes of BTO. METHODS: We developed individualized COW blood flow models for 43 patients undergoing BTO. These models simulated blood flow and pressure under normal conditions and with the ICA occlusion. We then compared the model's predictions of blood flow changes due to the simulated ICA occlusion to actual qMRA measurements before the BTO. RESULTS: For all 31 BTO failures, the ipsilateral hemisphere showed an average flow decrease of 15 ± 10% (mean ± standard deviation), compared to 3 ± 2% in the contralateral hemisphere. In all 12 BTO passes, these figures were 6 ± 3% and 1 ± 0.8%, respectively. Notably, all BTO passes had less than a 10% reduction in the ipsilateral hemisphere. In contrast, 65% of BTO failures and 67% single-photon emission computed tomography (SPECT) failures exhibited a decrease of 10% or more in the same region. CONCLUSION: Blood flow reduction exceeding 10% in the ipsilateral hemisphere during BTO is a strong predictor of failure in both BTO and SPECT. Our patient-specific COW blood flow models, incorporating detailed flow and arterial geometry data, offered valuable insights for predicting BTO outcomes. These models are especially beneficial for situations where conducting BTO or SPECT is clinically impractical.

Comapping Cellular Content and Extracellular Matrix with Hemodynamics in Intact Arterial Tissues Using Scanning Immunofluorescent Multiphoton Microscopy.

Deviation of blood flow from an optimal range is known to be associated with the initiation and progression of vascular pathologies. Important open questions remain about how the abnormal flow drives specific wall changes in pathologies such as cerebral aneurysms where the flow is highly heterogeneous and complex. This knowledge gap precludes the clinical use of readily available flow data to predict outcomes and improve treatment of these diseases. As both flow and the pathological wall changes are spatially heterogeneous, a crucial requirement for progress in this area is a methodology for acquiring and comapping local vascular wall biology data with local hemodynamic data. Here, we developed an imaging pipeline to address this pressing need. A protocol that employs scanning multiphoton microscopy was developed to obtain three-dimensional (3D) datasets for smooth muscle actin, collagen, and elastin in intact vascular specimens. A cluster analysis was introduced to objectively categorize the smooth muscle cells (SMC) across the vascular specimen based on SMC actin density. Finally, direct quantitative comparison of local flow and wall biology in 3D intact specimens was achieved by comapping both heterogeneous SMC data and wall thickness to patient-specific hemodynamic results.

The correlation of cerebral arteriovenous malformation flow measured by quantitative MR angiography on MR-detected arteriovenous malformation microhemorrhage.

OBJECTIVE: The objective of this study was to assess the relationship of arteriovenous malformation (AVM) blood flow measured by quantitative MR angiography (QMRA) in nonruptured AVMs with MR-detected microhemorrhage. METHODS: All patients with unruptured AVMs who received baseline QMRA and gradient echo or susceptibility-weighted MRI were retrospectively reviewed (2004-2022). Imaging data, clinical history, and AVM angioarchitectural and flow features were collected and assessed. AVM flow was calculated from the difference of flow within primary arterial feeders from their contralateral counterparts. A review of the MR images determined the presence of microhemorrhages. Analysis of descriptive statistics, chi-square test, and binomial logistic regression were performed. RESULTS: Of 634 patients with cerebral AVMs at a single center, 89 patients met the inclusion criteria (54 with microhemorrhage and 35 without microhemorrhage). The calculated AVM flow was significantly higher in the group with a microhemorrhage (447.9 ± 193.1 ml/min vs 287.6 ± 235.7 ml/min, p = 0.009). In addition, the presence of venous anomaly, arterial ectasia, and diffuse nidus was significantly associated with microhemorrhage (p = 0.017, p = 0.041, and p = 0.041, respectively). Binary logistic regression found that higher flow predicted the presence of microhemorrhage (OR 1.002, 95% CI 1.000-1.004; p = 0.031). The highest AVM flow quartile significantly predicted the presence of venous anomaly (OR 3.840, 95% CI 1.037-14.213; p = 0.044), diffuse nidus (OR 6.800, 95% CI 1.766-25.181; p = 0.005), and arterial ectasia (OR 13.846, 95% CI 1.905-122.584; p = 0.018). CONCLUSIONS: This study represents the first to examine the association between flow measurements on QMRA with microhemorrhage in unruptured AVMs. Higher AVM flow, venous anomaly, arterial ectasia, and diffuse AVM nidus were related to a higher likelihood of AVM microhemorrhage. Higher AVM flow was present in AVMs with venous anomalies, a diffuse nidus, and arterial ectasia, indicating a possible interaction between these angioarchitectural findings, AVM flow, and microhemorrhage. These findings suggest a relationship between higher AVM flow and the risk of microhemorrhage.

Vertebral Artery to Middle Cerebral Artery Bypass for Flow Augmentation.

BACKGROUND AND IMPORTANCE: Extracranial-intracranial bypass remains an enduring procedure for a select group of patients suffering from steno-occlusive cerebrovascular disease. Although the superficial temporal artery (STA) to middle cerebral artery (MCA) bypass is most familiar among neurosurgeons, particular circumstances preclude the use of an STA donor. In such cases, alternative revascularization strategies must be pursued. CLINICAL PRESENTATION: A 63-year-old female presented with symptoms of hemodynamic insufficiency and was found to have left common carotid artery occlusion at the origin. She experienced progressive watershed ischemia and pressure-dependent fluctuations in her neurological examination despite maximum medical therapy. The ipsilateral STA was unsuitable for use as a donor vessel. We performed an extracranial vertebral artery (VA) to MCA bypass with a radial artery interposition graft. CONCLUSION: This technical case description and accompanying surgical video review the relevant anatomy and surgical technique for a VA-MCA bypass. The patient was ultimately discharged home at her preoperative neurological baseline with patency of the bypass. The VA can serve as a useful donor vessel for cerebral revascularization procedures in pathologies ranging from malignancies of the head and neck to cerebral aneurysms and cerebrovascular steno-occlusive disease.

WITHDRAWN: A narrative review of techniques for surgical revascularization of the extracranial vertebral artery in vertebrobasilar insufficiency.

The Publisher regrets that this article is an accidental duplication of an article that has already been published in Neurochirurgie, volume 70. https://doi.org/10.1016/j.neuchi.2023.101516. The duplicate article has therefore been withdrawn. The full Elsevier Policy on Article Withdrawal can be found at https://www.elsevier.com/about/policies/article-withdrawal.

A narrative review of techniques for surgical revascularization of the extracranial vertebral artery in vertebrobasilar insufficiency.

Vertebrobasilar insufficiency is a condition characterized by poor blood flow through the posterior circulation of the brain, which supplies the brainstem, thalamus, hippocampus, cerebellum, occipital lobes, and medial temporal lobes. Narrowing or occlusion of the vertebral arteries may be result in a range of neurological symptoms, including dizziness, imbalance, dysarthria, and even stroke. If symptomatic patients fail medical management, revascularization of the vertebral artery should be considered. Restoration of blood flow may involve transluminal balloon angioplasty or stent placement; however, certain cases may still require surgical intervention. The complexity of surgical revascularization of the vertebral artery requires careful consideration of skull base and neck anatomy. This review article will focus on bypass of the vertebral artery in the setting of ischemic pathology, describing the technique, anatomical nuances, steps involved in preoperative planning, and postoperative management.

Transfontanelle photoacoustic imaging of intraventricular brain hemorrhages in live sheep.

Intraventricular (IVH) and periventricular (PVH) hemorrhages in preterm neonates are common because the periventricular blood vessels are still developing up to 36 weeks and are fragile. Currently, transfontanelle ultrasound (US) imaging is utilized for screening for IVH and PVH, largely through the anterior fontanelle. However for mild hemorrhages, inconclusive diagnoses are common, leading to failure to detect IVH/PVH or, when other clinical symptoms are present, use of second stage neuroimaging modalities requiring transport of vulnerable patients. Yet even mild IVH/PVH increases the risk of moderate-severe neurodevelopmental impairment. Here, we demonstrate the capability of transfontanelle photoacoustic imaging (TFPAI) to detect IVH and PVH in-vivo in a large animal model. TFPAI was able to detect IVH/PVH as small as 0.3 mL in volume in the brain (p < 0.05). By contrast, US was able to detect hemorrhages as small as 0.5 mL. These preliminary results suggest TFPAI could be translated into a portable bedside imaging probe for improved diagnosis of clinically relevant brain hemorrhages in neonates.

Quantitative Blood Flow Reduction in Selective Embolization of Intranidal Fistula of Cerebral Arteriovenous Malformations: Case Series.

BACKGROUND AND OBJECTIVES: Arteriovenous malformations (AVMs) are often associated with high-flow intranidal fistulas (INFs). Although INF embolization has been suggested to provide higher reduction of total AVM flow compared with regular pedicle embolization, this effect has not previously been quantified. The aim of this study was to characterize the effect of AVM INF embolization on total AVM flow. METHODS: This study is an Institutional Review Board-approved, retrospective case series of patients from 2010 to 2022 with AVMs, both with and without INFs, who underwent quantitative magnetic resonance angiography and endovascular embolization. RESULTS: Twenty patients accounted for 35 separate embolization sessions: 13 patients with INFs underwent a total 21 embolizations and 12 patients without INFs had 14 embolizations. No significant differences were found between groups on age, sex, laterality, drainage pattern, and Spetzler-Martin grade. However, AVMs with INFs were larger than the control group (12.7 vs 8.37 cm 3 , P = .049). Baseline pre-embolization AVM flow significantly differed between AVM with INF vs control groups (522 vs 320 cc/min, P = .005). Similarly, postembolization AVM flow also differed between AVM with INF and control groups (392 vs 224 cc/min, P = .008), with a larger decrease in flow per vessel per embolization session within the AVM INF group compared with controls (101.5 vs 33.2 cc/min, P < .001). Repeated measure analysis of variance showed significant differences pre-embolization and postembolization AVM flow between those with INFs vs controls ( P < .001). CONCLUSION: This study represents the first to examine the effect of INF embolization on total AVM flow. AVMs with INFs showed higher baseline flow, and targeted embolization toward INFs significantly lowered AVM flow in comparison with controls without INFs. The results of this study emphasize the importance of recognizing the presence of INFs within AVMs and their embolization to reduce AVM flow as part of a multistep management paradigm.

Preoperative embolization of brain arteriovenous malformation and efficacy in intraoperative blood loss reduction: a quantitative study.

BACKGROUND: Embolization of brain arteriovenous malformations (bAVMs) is often used as adjuvant therapy to microsurgical resection to reduce the high-risk features of bAVMs such as large size and high flow. However, the effect of preoperative embolization on surgical performance and patient outcome has shown mixed results. Heterogeneity in treatment goals, selection criteria, and unpredictable changes in bAVM hemodynamics after partial embolization may account for these uncertain findings. In this study we use an objective quantitative technique to assess the impact of preoperative embolization on intraoperative blood loss (IBL). METHODS: Patients with bAVM treated with microsurgical resection only or in combination with preoperative embolization from 2012 to 2022 were retrospectively reviewed. Patients were included if quantitative magnetic resonance angiography was performed prior to any treatment. Correlation of baseline bAVM flow, volume, and IBL was evaluated between the two groups. Additionally, bAVM flow prior to and after embolization was compared. RESULTS: Forty-three patients were included, 31 of whom required preoperative embolization (20 had more than one session). Mean bAVM initial flow (362.3 mL/min vs 89.6 mL/min, p=0.001) and volume (9.6 mL vs 2.8 mL, p=0.001) were significantly higher in the preoperative embolization group; flow decreased significantly after embolization (408.0 mL/min vs 139.5 mL/min, p<0.001). IBL was comparable between the two groups (258.6 mL vs 141.3 mL, p=0.17). Linear regression continued to show a significant difference in initial bAVM flow (p=0.03) but no significant difference in IBL (p=0.53). CONCLUSION: Patients with larger bAVMs who underwent preoperative embolization had comparable IBL to those with smaller bAVMs undergoing only surgical treatment. Preoperative embolization of high-flow bAVMs facilitates surgical resection, reducing the risk of IBL.

Ultra-widefield and high-speed spiral laser scanning OR-PAM: System development and characterization.

Photoacoustic microscopy (PAM) is a high-resolution imaging modality that has been mainly implemented with small field of view applications. Here, we developed a fast PAM system that utilizes a unique spiral laser scanning mechanism and a wide acoustic detection unit. The developed system can image an area of 12.5 cm2 in 6.4 s. The system has been characterized using highly detailed phantoms. Finally, the imaging capabilities of the system were further demonstrated by imaging a sheep brain ex vivo and a rat brain in vivo.