Direct, indirect, and combined revascularization in Moyamoya disease and syndrome: a scope review and illustrative case report
DOI:
https://doi.org/10.34119/bjhrv8n6-403Keywords:
Moyamoya disease, cerebral revascularization, combined modality therapy, scoping review, case reportsAbstract
This paper reviews the literature on combined revascularization in Moyamoya disease (MMD) and Moyamoya syndrome (MMS), comparing its clinical outcomes and indications with those of direct and indirect techniques, and presents a pediatric case to illustrate its applicability. A scoping review was conducted following PRISMA-ScR (2020), including studies from 2019 to 2025 indexed in PubMed, SciELO, BVSalud, and Cochrane. Eligible studies evaluated direct, indirect, or combined revascularization in MMD/MMS. Screening and data extraction were performed independently by two reviewers, with disagreements resolved by a third. A pediatric MMS case treated with combined revascularization was also reported following CARE Guidelines (2017). The review showed that early surgical treatment reduces ischemic and hemorrhagic events, improves headaches, and decreases long-term morbidity and mortality. Direct and combined bypass techniques provided superior functional outcomes and more reliable long-term revascularization, while indirect procedures remained safe and effective, especially in children. Combined revascularization offered the advantages of both methods, ensuring immediate and sustained reperfusion, improved cerebrovascular reserve, and favorable neurological recovery, although it may involve transient postoperative hemodynamic changes and require broader surgical exposure. The pediatric case demonstrated successful bilateral patency, improved perfusion, neoangiogenesis, and preserved neurological function without major complications. Overall, the choice of technique should be individualized based on clinical profile, anatomy, and risk. Combined revascularization emerges as a safe, effective, and reproducible strategy, particularly beneficial for patients with extensive hemispheric involvement.
References
NAVANDHAR, P. S. et al. Moyamoya disease: advances in diagnosis, treatment, and surgical interventions. Cureus, v. 16, n. 5, p. e59826, 2024. DOI: 10.7759/cureus.59826.
LAI, P. M. R. et al. Direct vs indirect revascularization in a North American cohort of Moyamoya disease. Neurosurgery, v. 89, n. 2, p. 315-322, 2021. DOI: 10.1093/neuros/nyab156.
WANG, Q. N. et al. Encephaloduroarteriosynangiosis for hemorrhagic Moyamoya disease: long-term outcome of a consecutive series of 95 adult patients from a single center. Journal of Neurosurgery, v. 130, n. 6, p. 1898-1905, 2019. DOI: 10.3171/2017.12.JNS172246.
DOHERTY, R. J. et al. Moyamoya disease and Moyamoya syndrome in Ireland: patient demographics, mode of presentation, and outcomes of EC-IC bypass surgery. Irish Journal of Medical Science, v. 190, n. 1, p. 335-344, 2021. DOI: 10.1007/s11845-020-02280-w.
HARA, S. et al. Imaging pattern and the mechanisms of postoperative infarction after indirect revascularization in patients with Moyamoya disease. World Neurosurgery, v. 155, p. e510-e521, 2021. DOI: 10.1016/j.wneu.2021.08.098.
SUM, C. H. et al. Surgical revascularization for Moyamoya angiopathy: clinical and radiological outcomes of direct and indirect bypasses in 86 affected hemispheres. Journal of Clinical Neuroscience, v. 99, p. 66-72, 2022. DOI: 10.1016/j.jocn.2022.02.036.
ARAKI, Y. et al. Surgical designs of revascularization for Moyamoya disease: 15 years of experience in a single center. World Neurosurgery, v. 139, p. e325-e334, 2020. DOI: 10.1016/j.wneu.2020.03.217.
ONG, J. A. et al. Revascularisation surgery for paediatric Moyamoya disease: the Singapore experience. Journal of Clinical Neuroscience, v. 82, Pt. B, p. 207-213, 2020. DOI: 10.1016/j.jocn.2020.11.008.
ALWAKAA, O. et al. Characterizing revascularization after encephalo-duro-arterio-synangiosis (EDAS) in adult patients with Moyamoya disease using the orbital grading system. World Neurosurgery, publicado online em 10 set. 2024. DOI: 10.1016/j.wneu.2024.09.026.
SAITO, H. et al. Specific clinical features and one-stage revascularization surgery for Moyamoya disease with severe cerebral ischemia in the territory of posterior cerebral artery. Acta Neurochirurgica (Wien), v. 163, n. 2, p. 583-592, 2021. DOI: 10.1007/s00701-020-04580-7.
SHIMIZU, T. et al. Large craniotomy increases the risk of minor perioperative complications in revascularization surgery for Moyamoya disease. World Neurosurgery, v. 141, p. e498-e507, 2020. DOI: 10.1016/j.wneu.2020.05.227.
CHEN, T. et al. The progression of pathophysiology of Moyamoya disease. Neurosurgery, v. 93, n. 3, p. 502-509, 2023. DOI: 10.1227/neu.0000000000002455.
OSHIIMA, H.; KATAYAMA, Y. Discovery of cerebrovascular Moyamoya disease: research during the late 1950s and early 1960s. Child’s Nervous System, v. 28, n. 4, p. 497-500, 2012. DOI: 10.1007/s00381-012-1708-x.
SUZUKI, J.; TAKAKU, A. Cerebrovascular “Moyamoya” disease. Disease showing abnormal net-like vessels in base of brain. Archives of Neurology, v. 20, n. 3, p. 288-299, 1969. DOI: 10.1001/archneur.1969.00480090076012.
GOREN, O. et al. Encephaloduroarteriosynangiosis with dural inversion for Moyamoya disease in a pediatric and adult population—a single-center 20-year experience. World Neurosurgery, v. 149, p. e16-e21, 2021. DOI: 10.1016/j.wneu.2021.02.102.
ACKER, G.; FEKONJA, L.; VAJKOCZY, P. Surgical management of Moyamoya disease. Stroke, v. 49, n. 2, p. 476-482, 2018. DOI: 10.1161/STROKEAHA.117.018563.
FEGHALI, J. et al. Moyamoya disease versus Moyamoya syndrome: comparison of presentation and outcome in 338 hemispheres. Journal of Neurosurgery, v. 133, n. 5, p. 1441-1449, 2020. DOI: 10.3171/2019.6.JNS191099.
KURODA, S. et al. Diagnostic criteria for Moyamoya disease—2021 revised version. Neurologia Medico-Chirurgica (Tokyo), v. 62, n. 7, p. 307-312, 2022. DOI: 10.2176/jns-nmc.2022-0072.
TRICCO, A. C. et al. PRISMA extension for scoping reviews (PRISMA-ScR): checklist and explanation. Annals of Internal Medicine, v. 169, n. 7, p. 467-473, 2018. DOI: 10.7326/M18-0850.
HOWICK, J. et al. Explanation of the 2011 Oxford Centre for Evidence-Based Medicine (OCEBM) Levels of Evidence (Background Document). Oxford Centre for Evidence-Based Medicine, 2011. Available at: https://www.cebm.ox.ac.uk/resources/levels-of-evidence/explanation-of-the-2011-ocebm-levels-of-evidence/. Accessed: 20 Oct. 2025.
RILEY, D. S. et al. CARE guidelines for case reports: explanation and elaboration document. Journal of Clinical Epidemiology, v. 89, p. 218-235, 2017. DOI: 10.1016/j.jclinepi.2017.04.026.
ZHU, C.; WANG, Y.; LI, J. Safety analysis of STA-MCA bypass combined with EDAS in the treatment of patients with Moyamoya disease. Medicine (Baltimore), v. 104, n. 12, p. e41769, 2025. DOI: 10.1097/MD.0000000000041769.
ZHOU, X. P. et al. A prospective study on hemodynamics of combined bypass surgery in the treatment of Moyamoya disease. Journal of Craniofacial Surgery, v. 36, n. 6, p. 2012-2017, 2025. DOI: 10.1097/SCS.0000000000011234.
SHAHBANDI, A. et al. The management of symptomatic Moyamoya disease in pediatric patients: a systematic review and meta-analysis. Neurosurgery, v. 97, n. 1, p. 65-81, 2024. DOI: 10.1227/neu.0000000000003277.
LEE, K. S. et al. Surgical revascularizations for pediatric Moyamoya: a systematic review, meta-analysis, and meta-regression analysis. Child’s Nervous System, v. 39, n. 5, p. 1225-1243, 2023. DOI: 10.1007/s00381-023-05868-6.
NGUYEN, V. N. et al. Surgical techniques and indications for treatment of adult Moyamoya disease. Frontiers in Surgery, v. 9, 966430, 2022. DOI: 10.3389/fsurg.2022.966430.
ZHANG, X. H. et al. Comparison of revascularization and conservative treatment for hemorrhagic Moyamoya disease in East Asian countries: a single-center case series and a systematic review with meta-analysis. Frontiers in Neurology, v. 14, 1169440, 2023. DOI: 10.3389/fneur.2023.1169440.
ABOUKAIS, R. et al. The evaluation of intracranial bypass patency in neurosurgical practice. Neurochirurgie, v. 67, n. 2, p. 125-131, 2021. DOI: 10.1016/j.neuchi.2020.10.001.
YAO, F. et al. Assessment of transient cerebral hemodynamic disturbance via whole-brain computed tomography perfusion after extracranial-intracranial bypass in ischemic Moyamoya disease. World Neurosurgery, v. 146, p. e112-e121, 2021. DOI: 10.1016/j.wneu.2020.10.046.
McNEIL, E. et al. Superficial temporal artery size changes after encephaloduroarteriosynangiosis for the treatment of Moyamoya disease. World Neurosurgery, v. 190, p. e774-e780, 2024. DOI: 10.1016/j.wneu.2024.07.217.
COULDWELL, M. W. et al. Right frontotemporal craniotomy for ECA-to-MCA direct and indirect bypass and occipital artery indirect bypass to the posterior circulation: case report. Journal of Neurosurgery: Pediatrics, v. 27, n. 2, p. 180-184, 2020. DOI: 10.3171/2020.7.PEDS20181.
HWANG, J. K. et al. The feasibility of performing multiple burr hole surgery in pediatric Moyamoya patients as a response to failed mEDAS. Child’s Nervous System, v. 37, n. 7, p. 2233-2238, 2021. DOI: 10.1007/s00381-021-05093-z.
TORTORA, D. et al. Spatial coefficient of variation applied to arterial spin labeling MRI may contribute to predict surgical revascularization outcomes in pediatric Moyamoya vasculopathy. Neuroradiology, v. 62, n. 8, p. 1003-1015, 2020. DOI: 10.1007/s00234-020-02446-4.
APPIREDY, R. et al. Surgery for Moyamoya disease in children. Journal of Child Neurology, v. 34, n. 9, p. 517-529, 2019. DOI: 10.1177/0883073819844854.
BYUN, Y. H. et al. Preservation of the arachnoid membrane during encephaloduroarteriosynangiosis reduces postoperative complications without undermining the surgical outcome in pediatric Moyamoya disease. World Neurosurgery, v. 130, p. e406-e416, 2019. DOI: 10.1016/j.wneu.2019.06.103.
KURODA, S.; HOUKIN, K. Moyamoya disease: current concepts and future perspectives. Lancet Neurology, v. 7, n. 11, p. 1056-1066, 2008. DOI: 10.1016/S1474-4422(08)70240-0.
YU, J. et al. Cerebral hyperperfusion syndrome after revascularization surgery in patients with Moyamoya disease: systematic review and meta-analysis. World Neurosurgery, v. 135, p. 357-366.e4, 2020. DOI: 10.1016/j.wneu.2019.11.065.
HORIE, N. et al. De novo ivy sign indicates postoperative hyperperfusion in Moyamoya disease. Stroke, v. 45, n. 5, p. 1488-1491, 2014. DOI: 10.1161/STROKEAHA.114.004755.
GONZALEZ, N. R. et al. Adult Moyamoya disease and syndrome: current perspectives and future directions: a scientific statement from the American Heart Association/American Stroke Association. Stroke, v. 54, n. 10, p. e465-e479, 2023. DOI: 10.1161/STR.0000000000000443.
PILGRAM-PASTOR, S.; CHAPOT, R.; KRAEMER, M. The angiographic presentation of European Moyamoya angiopathy. Journal of Neurology, v. 269, n. 2, p. 997-1006, 2022. DOI: 10.1007/s00415-021-10684-6.
COOK, D. J. et al. Moyamoya disease. In: LANZER, P. PanVascular Medicine. Berlin; Heidelberg: Springer, 2014. DOI: 10.1007/978-3-642-37393-0_102-1.
SUDHIR, B. J. et al. The mechanobiological theory: a unifying hypothesis on the pathogenesis of Moyamoya disease based on a systematic review. Neurosurgical Focus, v. 51, n. 3, p. E6, 2021. DOI: 10.3171/2021.6.FOCUS21281.
FILIMONOVA, E. et al. Myelin damage and cortical atrophy in watershed regions in patients with Moyamoya angiopathy. Frontiers in Neuroscience, v. 16, p. 982829, 2022. DOI: 10.3389/fnins.2022.982829.
AHTAM, B. et al. Diffusion-weighted magnetic resonance imaging demonstrates white matter alterations in watershed regions in children with Moyamoya without stroke or silent infarct. Pediatric Neurology, v. 143, p. 89-94, 2023. DOI: 10.1016/j.pediatrneurol.2023.03.005.
AHTAM, B. et al. Symptoms do not predict white matter injury in the watershed regions in children with Moyamoya. Journal of Pediatrics, v. 276, p. 114372, 2025. DOI: 10.1016/j.jpeds.2024.114372.
LAWTON, M. T. Seven Bypasses: Tenets and Techniques for Revascularization. New York: Thieme Medical Publishers, 2018.
