Indirect Cerebral Revascularization Research Articles

A novel system for evaluating collateralization of the external carotid artery after cerebral revascularization in moyamoya disease.

The objective of this retrospective study was to establish a novel system for evaluating collateralization of the external carotid artery in patients with moyamoya disease (MMD) following direct and indirect revascularization surgeries. The authors conducted a retrospective analysis of 456 patients diagnosed with MMD who underwent direct and indirect revascularization procedures at Beijing Tiantan Hospital, Capital Medical University, between January 2015 and May 2023. Using a newly proposed digital subtraction angiography (DSA)-based evaluation system, the authors assessed collateralization angiogenesis objectively and in a standardized manner. The authors' findings indicated that there was no significant difference in collateralization angiogenesis between patients undergoing direct or indirect cerebral revascularization (p = 0.702). However, after cerebral revascularization, patients with ischemic MMD exhibited significantly higher collateralization angiogenesis compared with those with hemorrhagic MMD (p = 0.007). Children with MMD demonstrated higher angiogenesis levels than adults (p < 0.001), but subgroup analysis showed age-specific variations. In adults, collateralization angiogenesis was significantly greater in those with ischemic MMD (p = 0.006), whereas in children, no significant difference was noted between ischemic and hemorrhagic MMD (p = 0.962). Furthermore, regardless of MMD type, direct and indirect revascularization methods yielded similar collateralization angiogenesis (p = 0.962 and p = 0.963, respectively). Importantly, the Matsushima grading system revealed significant differences in angiogenesis in patients with ischemic MMD (p < 0.001). The newly introduced DSA-based evaluation system offers an objective and standardized method for assessing collateralization angiogenesis in MMD. This study supports the efficacy of both direct and indirect revascularization surgical procedures and highlights distinct pathophysiological processes of ischemic and hemorrhagic disease subtypes. These findings contribute to a better understanding of surgical outcomes and aid in the selection of appropriate treatment strategies for patients with MMD.

59. A Multidisciplinary Approach to Combined Direct and Indirect Cerebral Revascularization Utilizing the Temporoparietal Fascia Flap

59. A Multidisciplinary Approach to Combined Direct and Indirect Cerebral Revascularization Utilizing the Temporoparietal Fascia Flap

Influence of Patient and Technical Variables on Combined Direct and Indirect Cerebral Revascularization: Case Series.

Cerebral bypass for flow augmentation is an important technique for selected neurosurgical patients, with multiple techniques used (direct, indirect, or combined). To assess the impact of patient and technical variables on direct and indirect bypass flow after combined revascularization. This was a retrospective, single-institution review of patients undergoing direct superficial temporal artery-to-middle cerebral artery bypass with indirect encephaloduro-myosynangiosis for moyamoya disease and steno-occlusive cerebrovascular disease over a 2-year period. We evaluated the effect of baseline patient characteristics, preoperative imaging characteristics, and operative variables on direct and indirect patency grades. Twenty-six hemispheres (8 moyamoya disease and 18 steno-occlusive cerebrovascular disease) in 23 patients were treated with combined revascularization. The mean patient age was 53.4 ± 19.1 years. Direct bypass patency was 96%. Over a mean follow-up of 8.3 ± 5.4 months, there were 3 strokes in the treated hemispheres (11.5%). The mean modified Rankin Scale score improved from 1.3 ± 1.1 preoperatively to 0.7 ± 0.8 postoperatively. Preservation of the nondonor superficial temporal artery branch was associated with a lower direct bypass grade ( P < .01), whereas greater mean time to maximum perfusion (Tmax)> 4 and >6 seconds and mismatch volumes were associated with higher direct bypass grades ( P < .05). Tmax >4-second volume inversely predicted indirect bypass patency. Patient and technical variables may influence the relative contributions of the direct and indirect components of combined revascularizations.

Ten-year experience with laparoscopic pedicled omental flap for cerebral revascularization in patients with Moyamoya disease

BackgroundThe omental flap has numerous extraperitoneal applications in reconstruction and revascularization given its favorable immunologic and angiogenic properties. In patients with Moyamoya disease, cerebral revascularization using a pedicled omental flap has proven to be a viable option following direct revascularization procedures. Historically, harvesting omentum involved laparotomy with the associated risk of complications; herein we describe outcomes from a 10-year experience of laparoscopic harvesting of pedicled omental flap for cerebral revascularization in Moyamoya patients. MethodsA retrospective chart review was performed of all patients with Moyamoya disease who underwent laparoscopic omental cerebral transposition between 2011 and 2021. Intraoperative and postoperative complications, length of stay (LOS), and outcomes at follow-up were analyzed. ResultsTwenty-one patients underwent the procedure during the study period. Three intraoperative complications occurred (one segmental transverse colectomy for mesenteric injury, one converted to omental free flap, and one requiring micro anastomosis). Average overall LOS was 6 ± 6 days, with 3 ± 3.5 days in the ICU (mean±SD). Following discharge, complications included epigastric incisional hernia at the graft fascial exit site, recurrent neck pain at subcutaneous tunneling site, and partial scalp necrosis. One patient required subsequent direct bypass seven months after the initial procedure owing to the progression of the disease. All other patients had partial or complete resolution of symptoms. ConclusionOur retrospective observational study indicates that laparoscopic pedicled omental flap mobilization and transposition is a safe and effective method of indirect cerebral revascularization in patients with Moyamoya disease. Level of evidenceN/A.

Abstract TP487: Comprehensive Profiling of Secreted Factors in the Cerebrospinal Fluid of Moyamoya Disease Patients

Background: Moyamoya disease (MMD) is a chronic cerebrovascular disease characterized by progressive occlusion of the internal carotid arteries leading to ischemic and hemorrhagic events. The underlying pathogenesis of MMD remains unclear. In this study we investigated key secreted molecules in the cerebrospinal fluid (CSF) of MMD patients including relation to the extent of neovascularization and eventual functional outcomes. Methods: This study included intraoperative CSF collected from 32 controls (Chiari malformation and cranial nerve hyperactive syndromes) and 73 MMD patients (ischemic: 39; hemorrhagic: 34) that underwent combined direct and indirect superficial temporal artery-middle cerebral artery revascularization procedure. 62 factors were analyzed using multiplex luminex assay, including angiogenic growth factors, cytokines, and chemokines. Cellular retinoic acid binding protein (CRBP1) was also measured using ELISA. Functional outcome was assessed using the modified Rankin scale score (mRS). Matsushima criteria was used for grading the neovascularization. Results: Forty molecules were significantly elevated in both MMD subtypes in comparison with controls. The common top highly secreted CSF proteins included platelet-derived growth factor bb, chemokine ligand 5 and plasminogen activator inhibitor 1 (p&lt;0.001). CRBP1 and other growth factors such as brain-derived nerve growth factor and basic fibroblast growth factor were also elevated in both MMD subtypes (p&lt;0.01). Our results also revealed a number of proteins not previously reported in MMD. Ingenuity pathway analysis indicated that the ischemic and hemorrhagic MMD subtypes exhibited similar cellular/molecular functions and pathways including cellular activation, migration and inflammatory response. Interestingly, while neuro-inflammation and dendritic cell pathways were activated in MMD patients, lipid signaling pathways involving nuclear receptors PPAR and LXR/RXR signaling were inhibited. Conclusions: CSF analysis revealed that a number of cytokines, chemokines and growth factors are elevated in both MMD subtypes. These molecules potentially contribute to the pathogenesis of MMD and could be potential future therapeutic targets.

Methods to assess competence of indirect cerebral revascularization in children

we aimed to compare the capabilities of triplex ultrasound (TU) of vessels, magnetic resonance angiography (MRA), computed tomography angiography (CTA), and CCA in assessing the competence of indirect cerebral revascularization (ICR) in children. ICR was performed in 18 children in 24 hemispheres (24 operations). The results were evaluated by Matsushima classification-based comparison of the data of preoperative and postoperative clinical examinations, TU of the superficial temporal artery, magnetic resonance imaging (MRI) and computed tomography (CT) of vessels, and selective cerebral angiography. After surgery, improvements in the neurological and neuropsychological status were assessed. Matsushima grade A collaterals were found in 12 (50%) cases, grade B collaterals were present in 3 (13%) cases, grade C collaterals were present in 7 (29%) cases, and grade D collaterals were detected in 1 (4%) case; in 1 (4%) case, the superficial temporal artery was not enhanced. MR angiography visualized 18 (75%) indirect anastomoses, CT angiography revealed 4 indirect anastomoses, and TU visualized 4 indirect anastomoses. Comparison of preoperative and postoperative TU data for the superficial temporal artery revealed significant changes in blood flow in the form of increased rate indices and a decreased resistance index; mean values of indices for each angiographic class of revascularization and significant differences in pre- and postoperative observations were calculated. Examination of ICR competence using CCA is necessary in the presence of persistent clinical signs of chronic cerebral circulatory insufficiency, absence of increased blood flow and decreased peripheral resistance in the superficial temporal artery, and lack of anastomosis according to MRA. The most optimal techniques for postoperative examination are MRA with perfusion and diffusion maps and TU.

Combined Direct and Indirect Cerebral Revascularization Using Local and Flow-Through Flaps.

Extracranial-intracranial bypass is indicated in ischemic disease such as moyamoya, certain intracranial aneurysms, and other complex neurovascular diseases. In this article, we present our series of local and flow-through flaps for cerebral revascularization as an additional tool to provide direct and indirect revascularization and/or soft tissue coverage. A retrospective review of a prospectively maintained database was performed identifying nine patients. Ten direct arterial bypass procedures with nine indirect revascularization and/or soft tissue reconstruction were performed. Indications for arterial bypass included intracranial aneurysm (n = 2) and moyamoya disease (n = 8). Indications for soft tissue transfer included infected cranioplasty (one) and indirect cerebral revascularization (eight). Four flow-through flaps and five pedicled flaps were used including a flow-through radial forearm fasciocutaneous flap (one), flow-through radial forearm fascial flaps (three), and pedicled temporoparietal fascial (TPF) flaps with distal end anastomosis (five). The superficial temporal vessels (seven) and facial vessels (two) were used as the vascular inflow. Arterial bypass was established into the middle cerebral artery (six) and anterior communicating artery (three). There were no intraoperative complications. All flaps survived with no donor-site complications. In one case of flow-through TPF flap, the direct graft failed, but the indirect flap remained vascularized. Local and flow-through flaps can improve combined direct and indirect revascularization and provide soft tissue reconstruction. Minimal morbidity has been encountered in early outcomes though long-term results remain under investigation for these combined neurosurgery and plastic surgery procedures. The level of evidence is IV.

Evaluation of Encephaloduroarteriosynangiosis Efficacy Using Probabilistic Independent Component Analysis Applied to Dynamic Susceptibility Contrast Perfusion MRI.

Indirect cerebral revascularization has been successfully used for treatment in Moyamoya disease and symptomatic intracranial atherosclerosis. While angiographic neovascularization has been demonstrated after surgery, measurements of local tissue perfusion are scarce and may not reflect the reported successful clinical outcomes. We investigated probabilistic independent component analysis and conventional perfusion parameters from DSC-MR imaging to measure postsurgical changes in tissue perfusion. In this prospective study, 13 patients underwent unilateral indirect cerebral revascularization and DSC-MR imaging before and after surgery. Conventional perfusion parameters (relative cerebral blood volume, relative cerebral blood flow, and TTP) and probabilistic independent components that reflect the relative contributions of DSC signals consistent with arterial, capillary, and venous hemodynamics were calculated and examined for significant changes after surgery. Results were compared with postsurgical DSA studies to determine whether changes in tissue perfusion were due to postsurgical neovascularization. Before surgery, tissue within the affected hemisphere demonstrated a high probability for hemodynamics consistent with venous flow and a low probability for hemodynamics consistent with arterial flow, whereas the contralateral control hemisphere demonstrated the reverse. Consistent with symptomatic improvement, the probability for venous hemodynamics within the affected hemisphere decreased with time after surgery (P = .002). No other perfusion parameters demonstrated this association. Postsurgical DSA revealed an association between an increased preoperative venous probability in the symptomatic hemisphere and neovascularization after surgery. Probabilistic independent component analysis yielded sensitive measurements of changes in local tissue perfusion that may be associated with newly formed vasculature after indirect cerebral revascularization surgery.

Reduction in Overt and Silent Stroke Recurrence Rate Following Cerebral Revascularization Surgery in Children with Sickle Cell Disease and Severe Cerebral Vasculopathy.

Children with sickle cell disease (SCD) and moyamoya may benefit from indirect cerebral revascularization surgery in addition to chronic blood transfusion therapy for infarct prevention. We sought to compare overt and silent infarct recurrence rates in children with SCD undergoing revascularization. This was a retrospective cohort study of all children with SCD and moyamoya treated at two children's hospitals. Clinical events and imaging studies were reviewed. Twenty-seven children with SCD and confirmed moyamoya receiving chronic transfusion therapy were identified, of whom 12 underwent indirect cerebral revascularization. Two subjects had postoperative transient ischemic attacks and another had a subarachnoid blood collection, none of which caused permanent consequences. Two subjects had surgical wound infections. Among these 12 children, the rate of overt and silent infarct recurrence decreased from 13.4 infarcts/100 patient-years before revascularization to 0 infarcts/100 patient-years after revascularization (P = 0.0057); the postrevascularization infarct recurrence rate was also significantly lower than the overall infarct recurrence of 8.87 infarcts/100 patient-years in 15 children without cerebral revascularization (P = 0.025). The rate of overt and silent infarct recurrence was significantly lower following indirect cerebral revascularization. A prospective study of cerebral revascularization in children with SCD is needed.

Cerebral Blood Flow Improvement after Indirect Revascularization for Pediatric Moyamoya Disease: A Statistical Analysis of Arterial Spin-Labeling MRI.

The severity of Moyamoya disease is generally scaled with conventional angiography and nuclear medicine. Arterial spin-labeling MR imaging is now acknowledged for the noninvasive quantification of cerebral blood flow. This study aimed to analyze CBF modifications with statistical parametric mapping of arterial spin-labeling MR imaging in children undergoing an operation for Moyamoya disease. We included 15 children treated by indirect cerebral revascularization with multiple burr-holes between 2011 and 2013. Arterial spin-labeling MR imaging and T1 sequences were then analyzed under SPM8, according to the general linear model, before and after the operation (3 and 12 months). Voxel-based analysis was performed at the group level, comparing all diseased hemispheres with all normal hemispheres and, at the individual level, comparing each patient with a control group. Group analysis showed statistically significant preoperative hypoperfusion in the MCA territory in the Moyamoya hemispheres and a significant increase of cerebral perfusion in the same territory after revascularization (P < .05 family-wise error-corrected). Before the operation, individual analysis showed significant hypoperfusion for each patient co-localized with the angiographic defect on DSA. All except 1 patient had improvement of CBF after revascularization, correlated with their clinical status. SPM analysis of arterial spin-labeling MR imaging offers a noninvasive evaluation of preoperative cerebral hemodynamic impairment and an objective assessment of postoperative improvement in children with Moyamoya disease.

Moyamoya disease: A case of vanishing cerebral vessels

To provide an overview of moyamoya disease (MMD) including pathophysiology, epidemiology, clinical presentation, diagnosis, treatment, and prognosis. Selected clinical and epidemiological studies, review articles, and diagnostic guidelines for MMD. MMD is a rare cerebrovascular disease characterized by progressive stenosis of the distal internal carotid arteries and their major branches. The dilated and fragile basal collateral circulations display a "puff of smoke" appearance and thus are called moyamoya vessels. Other unique features of MMD include 2:1 female preponderance and its peak incidence in two age groups: early childhood and adults in their mid-40s. The pathophysiology of MMD is unclear and possible causes include genetic linkage, angiogenesis, autoimmune disease, cranial radiation, and infection of the head and neck. Most patients are symptomatic and may present with ischemic or hemorrhagic strokes, seizure, or headache. The diagnosis depends on clinical presentation and radiographic imaging, and disease progression may be halted with direct or indirect cerebral revascularization. It is important to make a correct diagnosis and provide appropriate treatment to reduce the morbidity and mortality associated with MMD. A prompt referral for possible surgical revascularization offers the best chance to reduce additional cerebral injuries and improve clinical outcomes.

Characterization of Direct and Indirect Cerebral Revascularization for the Treatment of European Patients with Moyamoya Disease

Background: The best revascularization strategy for moyamoya disease (MMD) remains unknown. Our aim was to characterize angiographic revascularization effects of a bilateral standardized revascularization approach, consisting of superficial temporal artery (STA)-middle cerebral artery (MCA) bypass and encephalomyosynangiosis (EMS) on one hemisphere and single EMS on the contralateral hemisphere of each patient, and to compare the effects of both revascularization strategies on cerebral hemodynamics. Methods: In 30 patients (18 females/12 males, age 8–63 years), standardized revascularization was performed. Digital subtraction angiography was performed preoperatively and at 7 days, 6 months and 12 months postoperatively. STA-MCA and EMS functions were graded I (poor), II (medium) or III (extensive) according to angiographic aspects. In 20 patients, cerebrovascular reserve capacity (CVRC) was assessed pre- and postoperatively (at 12 months) using xenon CT. Results: After 12 months, STA-MCA/EMS function was grade 1 in 40/40%, grade 2 in 27/26%, and grade 3 in 27/10% of hemispheres, respectively. Twelve months after surgery, single EMS showed grade I in 37%, grade II in 27%, and grade III in 20% of hemispheres. Combined revascularization improved CVRC significantly compared to preoperative measurement (preoperative: 16.5 ± 34.6% vs. postoperative: 60.8 ± 64.22%; p < 0.05). Single EMS did not improve CVRC significantly (preoperative: 21.8 ± 35.9% vs. postoperative: 34.8 ± 63.0%; p < 0.05). Conclusions: Combined and indirect revascularization may be successfully applied in a bilateral standardized approach. STA-MCA/EMS is superior to single EMS in restoring CVRC in adult MMD patients.

Clinical and Angiographic Outcomes From Indirect Revascularization Surgery for Moyamoya Disease in Adults and Children: A Review of 63 Procedures

Several forms of indirect cerebral revascularization have been proposed to promote neovascularity to the ischemic brain. To present clinical and angiographic outcomes of indirect revascularization by encephaloduroarteriosynangiosis and burr holes for the treatment of Moyamoya disease in adults and children. Data from 63 hemispheres treated in 42 patients (average age, 30 years; 33 adults; 30 female patients; median follow-up, 14 months) were reviewed. In hemispheres with preoperative and postoperative (6- to 12-month) angiograms available, superficial temporal artery (STA) and middle meningeal artery (MMA) diameters were measured. Preoperative and postoperative corrected arterial sizes were compared. Seven patients (17%) had transient ischemic attacks that resolved within 1 month of surgery. No patients suffered moyamoya-related hemorrhage after treatment. Two patients developed additional symptoms many years after surgery. In 18 hemispheres with preoperative and postoperative angiograms, there was an average postoperative increase in STA and MMA diameters of 51% (P = .003) and 49% (P = .002), respectively. Both children and adults displayed revascularization. Two patients did not demonstrate increased vessel size. STA blush and new branches and MMA blush and new branches were identified in 12, 14, 14, and 16 hemispheres, respectively. Angiographic blush was identified in 59% of frontal and 19% of parietal burr holes (P = .03). Surgical complications included 2 subdural hemorrhages requiring evacuation and 2 new ischemic deficits (1 transient). Indirect revascularization by encephaloduroarteriosynangiosis and burr holes for moyamoya results in long-term resolution of ischemic and hemorrhagic manifestations in 95% of adults and children. The MMA appears to contribute significantly to the revascularization on follow-up angiograms with increased size and neovascularity comparable to that of the STA. Angiographically, parietal burr holes do not contribute as significantly as frontal burr holes.

Indirect Cerebral Revascularization

Indirect Cerebral Revascularization

Cerebral Revascularization Using Omentum and Muscle Free Flap for Ischemic Cerebrovascular Disease

Background Indirect cerebral revascularization has been generally accepted in the management of brain ischemia in moyamoya disease. We performed indirect cerebral revascularization by using omental flap and muscle flap techniques for the treatment of ischemic cerebrovascular disease. Methods Ten patients with ischemic cerebrovascular disease including three with adult moyamoya disease underwent this procedure (omental flap on eight sides and muscle flap on five sides). The muscle used for the flap was the serratus anterior muscle on two sides and shaved latissimus dorsi muscle on three sides. Angiography and cerebral blood flow studies were performed in all patients preoperatively and postoperatively. All patients demonstrated severely impaired cerebrovascular reserve capacity due to occlusive disease. Results There was one patient each with perioperative death and intracranial infection following omental flap loss, and two patients had perioperative strokes. The average follow-up period was 23.2 months. Of the nine surviving patients, all eight except for the one with flap loss had good outcome with complete resolution of neurologic episodes. Conclusions It is concluded that this method seems to be effective in selected patients with ischemic cerebrovascular disease.

P-3-239 - Alteration of telomerase activity during differentiation of A172 human glioblastoma cells

Moyamoya syndrome (MMS) in patients with sickle cell disease (SCD) accentuates the risk of recurrent strokes. Chronic transfusion therapy (CTT) is an excellent option for preventing recurrent strokes in most patients with SCD. In SCD with MMS, CTT may fail as a long-term solution. Cerebral revascularization, in the form of extracranial-intracranial bypass, has been shown to prevent recurrent strokes in this cohort. We review the evolution of this paradigm shift in the management of SCD-associated MMS. A systematic review, adhering to the Preferred Reporting Items for Systematic Reviews and Meta-Analyses protocol, was conducted. Our primary objectives were 1) to study the evolution of cerebral revascularization techniques in management of MMS in SCD and 2) to analyze the impact of neurosurgical intervention in this high-risk population. Four patients with SCD-associated MMS, who underwent indirect cerebral revascularization at our institute were retrospectively reviewed. A summary of 13 articles chronicling the advent and subsequent evolution of cerebral revascularization as a viable treatment strategy for stroke prevention in SCD-associated MMS is presented. The literature review suggests that early detection and surgical intervention (in addition to CTT) could significantly reduce stroke recurrence and improve neurocognitive outcome. Our short series of 4 patients also had a good outcome and no recurrence of strokes postoperatively. The literature emphasizes the use of a traditional standardized protocol for early identification (transcranial Dopplers, selective magnetic resonance angiography, and CTT). Early treatment and screening that involves early magnetic resonance angiography and referral to neurosurgery for revascularization may be considered for this high-risk population.