{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,23]],"date-time":"2026-09-23T17:48:44Z","timestamp":1790185724213,"version":"4.1.0"},"reference-count":31,"publisher":"Journal of Neurosurgery Publishing Group (JNSPG)","issue":"6","content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"published-print":{"date-parts":[[2024,6,1]]},"abstract":"<jats:sec>\n<jats:title>OBJECTIVE<\/jats:title>\n<jats:p>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.<\/jats:p>\n<\/jats:sec>\n<jats:sec>\n<jats:title>METHODS<\/jats:title>\n<jats:p>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)\u2013based evaluation system, the authors assessed collateralization angiogenesis objectively and in a standardized manner.<\/jats:p>\n<\/jats:sec>\n<jats:sec>\n<jats:title>RESULTS<\/jats:title>\n<jats:p>The authors\u2019 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 &lt; 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 &lt; 0.001).<\/jats:p>\n<\/jats:sec>\n<jats:sec>\n<jats:title>CONCLUSIONS<\/jats:title>\n<jats:p>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.<\/jats:p>\n<\/jats:sec>","DOI":"10.3171\/2023.10.jns231660","type":"journal-article","created":{"date-parts":[[2023,12,30]],"date-time":"2023-12-30T01:20:07Z","timestamp":1703899207000},"page":"1707-1715","source":"Crossref","is-referenced-by-count":9,"title":["A novel system for evaluating collateralization of the external carotid artery after cerebral revascularization in moyamoya disease"],"prefix":"10.3171","volume":"140","author":[{"given":"Wenjie","family":"Li","sequence":"first","affiliation":[{"name":"Department of Neurosurgery, Beijing Tiantan Hospital, Capital Medical University, Beijing;"},{"name":"China National Clinical Research Center for Neurological Diseases, Beijing; and"},{"name":"Center of Stroke, Beijing Institute for Brain Disorders, Beijing, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Meng","family":"Zhao","sequence":"additional","affiliation":[{"name":"Department of Neurosurgery, Beijing Tiantan Hospital, Capital Medical University, Beijing;"},{"name":"China National Clinical Research Center for Neurological Diseases, Beijing; and"},{"name":"Center of Stroke, Beijing Institute for Brain Disorders, Beijing, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Xingju","family":"Liu","sequence":"additional","affiliation":[{"name":"Department of Neurosurgery, Beijing Tiantan Hospital, Capital Medical University, Beijing;"},{"name":"China National Clinical Research Center for Neurological Diseases, Beijing; and"},{"name":"Center of Stroke, Beijing Institute for Brain Disorders, Beijing, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Peijiong","family":"Wang","sequence":"additional","affiliation":[{"name":"Department of Neurosurgery, Beijing Tiantan Hospital, Capital Medical University, Beijing;"},{"name":"China National Clinical Research Center for Neurological Diseases, Beijing; and"},{"name":"Center of Stroke, Beijing Institute for Brain Disorders, Beijing, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Huan","family":"Zhu","sequence":"additional","affiliation":[{"name":"Department of Neurosurgery, Beijing Tiantan Hospital, Capital Medical University, Beijing;"},{"name":"China National Clinical Research Center for Neurological Diseases, Beijing; and"},{"name":"Center of Stroke, Beijing Institute for Brain Disorders, Beijing, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Qihang","family":"Zhang","sequence":"additional","affiliation":[{"name":"Department of Neurosurgery, Beijing Tiantan Hospital, Capital Medical University, Beijing;"},{"name":"China National Clinical Research Center for Neurological Diseases, Beijing; and"},{"name":"Center of Stroke, Beijing Institute for Brain Disorders, Beijing, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Chenyu","family":"Zhu","sequence":"additional","affiliation":[{"name":"Department of Neurosurgery, Beijing Tiantan Hospital, Capital Medical University, Beijing;"},{"name":"China National Clinical Research Center for Neurological Diseases, Beijing; and"},{"name":"Center of Stroke, Beijing Institute for Brain Disorders, Beijing, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Qian","family":"Zhang","sequence":"additional","affiliation":[{"name":"Department of Neurosurgery, Beijing Tiantan Hospital, Capital Medical University, Beijing;"},{"name":"China National Clinical Research Center for Neurological Diseases, Beijing; and"},{"name":"Center of Stroke, Beijing Institute for Brain Disorders, Beijing, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jizong","family":"Zhao","sequence":"additional","affiliation":[{"name":"Department of Neurosurgery, Beijing Tiantan Hospital, Capital Medical University, Beijing;"},{"name":"China National Clinical Research Center for Neurological Diseases, Beijing; and"},{"name":"Center of Stroke, Beijing Institute for Brain Disorders, Beijing, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yan","family":"Zhang","sequence":"additional","affiliation":[{"name":"Department of Neurosurgery, Beijing Tiantan Hospital, Capital Medical University, Beijing;"},{"name":"China National Clinical Research Center for Neurological Diseases, Beijing; and"},{"name":"Center of Stroke, Beijing Institute for Brain Disorders, Beijing, China"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1754","reference":[{"issue":"12","key":"b1","series-title":"N Engl J Med","first-page":"1226","article-title":"Moyamoya disease and moyamoya syndrome","volume":"360","author":"Scott RM","year":"2009","unstructured":"Scott RM, Smith ER. Moyamoya disease and moyamoya syndrome. N Engl J Med. 2009;360(12):1226\u20131237."},{"issue":"1","key":"b2","series-title":"J Stroke","first-page":"2","article-title":"Moyamoya disease: epidemiology, clinical features, and diagnosis","volume":"18","author":"Kim JS","year":"2016","unstructured":"Kim JS. Moyamoya disease: epidemiology, clinical features, and diagnosis. J Stroke. 2016;18(1):2\u201311."},{"issue":"2","key":"b3","series-title":"Curr Neuropharmacol","first-page":"292","article-title":"Progression in moyamoya disease: clinical features, neuroimaging evaluation, and treatment","volume":"20","author":"Zhang X","year":"2022","unstructured":"Zhang X, Xiao W, Zhang Q,  Progression in moyamoya disease: clinical features, neuroimaging evaluation, and treatment. Curr Neuropharmacol. 2022;20(2):292\u2013308."},{"issue":"3","key":"b4","series-title":"J Neurol","first-page":"574","article-title":"Moyamoya angiopathy: long-term follow-up study in a Finnish population","volume":"266","author":"Savolainen M","year":"2019","unstructured":"Savolainen M, Mustanoja S, Pekkola J,  Moyamoya angiopathy: long-term follow-up study in a Finnish population. J Neurol. 2019;266(3):574\u2013581."},{"key":"b5","series-title":"Lancet Reg Health West Pac","first-page":"100331","article-title":"Epidemiology of moyamoya disease in China: a nationwide hospital-based study","volume":"18","author":"Zhang D","year":"2021","unstructured":"Zhang D, Huang L, Huang Z,  Epidemiology of moyamoya disease in China: a nationwide hospital-based study. Lancet Reg Health West Pac. 2021;18:100331."},{"issue":"1","key":"b6","series-title":"J Stroke","first-page":"21","article-title":"Moyamoya disease: treatment and outcomes","volume":"18","author":"Kim T","year":"2016","unstructured":"Kim T, Oh CW, Bang JS, Kim JE, Cho WS. Moyamoya disease: treatment and outcomes. J Stroke. 2016;18(1):21\u201330."},{"issue":"2","key":"b7","series-title":"J Neurosurg","first-page":"480","article-title":"Direct versus indirect revascularization in the treatment of moyamoya disease","volume":"129","author":"Park SE","year":"2018","unstructured":"Park SE, Kim JS, Park EK, Shim KW, Kim DS. Direct versus indirect revascularization in the treatment of moyamoya disease. J Neurosurg. 2018;129(2):480\u2013489."},{"issue":"2","key":"b8","series-title":"Stroke","first-page":"476","article-title":"Surgical management of moyamoya disease","volume":"49","author":"Acker G","year":"2018","unstructured":"Acker G, Fekonja L, Vajkoczy P. Surgical management of moyamoya disease. Stroke. 2018;49(2):476\u2013482."},{"issue":"12","key":"b9","series-title":"Stroke","first-page":"3572","article-title":"Direct, indirect, and combined extracranial-to-intracranial bypass for adult moyamoya disease: an updated systematic review and meta-analysis","volume":"53","author":"Nguyen VN","year":"2022","unstructured":"Nguyen VN, Motiwala M, Elarjani T,  Direct, indirect, and combined extracranial-to-intracranial bypass for adult moyamoya disease: an updated systematic review and meta-analysis. Stroke. 2022;53(12):3572\u20133582."},{"issue":"1","key":"b10","series-title":"Radiology","first-page":"107","article-title":"Moya moya disease: use of digital subtraction angiography in its diagnosis","volume":"157","author":"Hasuo K","year":"1985","unstructured":"Hasuo K, Tamura S, Kudo S,  Moya moya disease: use of digital subtraction angiography in its diagnosis. Radiology. 1985;157(1):107\u2013111."},{"issue":"1","key":"b11","series-title":"Stroke","first-page":"117","article-title":"The specificity of the collaterals to the brain through the study and surgical treatment of moyamoya disease","volume":"17","author":"Matsushima Y","year":"1986","unstructured":"Matsushima Y, Inaba Y. The specificity of the collaterals to the brain through the study and surgical treatment of moyamoya disease. Stroke. 1986;17(1):117\u2013122."},{"issue":"suppl 2","key":"b12","series-title":"Clin Neurol Neurosurg","first-page":"S238","article-title":"Guidelines for the diagnosis and treatment of spontaneous occlusion of the circle of Willis (\u2018moyamoya\u2019 disease). Research Committee on Spontaneous Occlusion of the Circle of Willis (Moyamoya Disease) of the Ministry of Health and Welfare, Japan","volume":"99","author":"Fukui M","year":"1997","unstructured":"Fukui M. Guidelines for the diagnosis and treatment of spontaneous occlusion of the circle of Willis (\u2018moyamoya\u2019 disease). Research Committee on Spontaneous Occlusion of the Circle of Willis (Moyamoya Disease) of the Ministry of Health and Welfare, Japan.Clin Neurol Neurosurg. 1997;99(suppl 2):S238-S240."},{"issue":"3","key":"b13","series-title":"Arch Neurol","first-page":"288","article-title":"Cerebrovascular \"moyamoya\" disease. Disease showing abnormal net-like vessels in base of brain","volume":"20","author":"Suzuki J","year":"1969","unstructured":"Suzuki J, Takaku A. Cerebrovascular \"moyamoya\" disease. Disease showing abnormal net-like vessels in base of brain. Arch Neurol. 1969;20(3):288\u2013299."},{"issue":"11","key":"b14","series-title":"Lancet Neurol","first-page":"1056","article-title":"Moyamoya disease: current concepts and future perspectives","volume":"7","author":"Kuroda S","year":"2008","unstructured":"Kuroda S, Houkin K. Moyamoya disease: current concepts and future perspectives. Lancet Neurol. 2008;7(11):1056\u20131066."},{"issue":"8","key":"b15","series-title":"Lancet Neurol","first-page":"747","article-title":"Moyamoya disease: diagnosis and interventions","volume":"21","author":"Ihara M","year":"2022","unstructured":"Ihara M, Yamamoto Y, Hattori Y,  Moyamoya disease: diagnosis and interventions. Lancet Neurol. 2022;21(8):747\u2013758."},{"issue":"11","key":"b16","series-title":"Stroke","first-page":"3304","article-title":"Neurosurgical advances in the treatment of moyamoya disease","volume":"42","author":"Pandey P","year":"2011","unstructured":"Pandey P, Steinberg GK. Neurosurgical advances in the treatment of moyamoya disease. Stroke. 2011;42(11):3304\u20133310."},{"key":"b17","series-title":"World Neurosurg","first-page":"273","article-title":"Direct bypass versus indirect bypass in adult moyamoya angiopathy with symptoms or hemodynamic instability: a meta-analysis of comparative studies","volume":"94","author":"Kim H","year":"2016","unstructured":"Kim H, Jang DK, Han YM,  Direct bypass versus indirect bypass in adult moyamoya angiopathy with symptoms or hemodynamic instability: a meta-analysis of comparative studies. World Neurosurg. 2016;94:273\u2013284."},{"issue":"5","key":"b18","series-title":"J Neurosurg","first-page":"1327","article-title":"Effects of different surgical modalities on the clinical outcome of patients with moyamoya disease: a prospective cohort study","volume":"128","author":"Deng X","year":"2018","unstructured":"Deng X, Gao F, Zhang D,  Effects of different surgical modalities on the clinical outcome of patients with moyamoya disease: a prospective cohort study. J Neurosurg. 2018;128(5):1327\u20131337."},{"issue":"3","key":"b19","series-title":"J Neurosurg","first-page":"793","article-title":"Meta-analysis of the surgical outcomes of symptomatic moyamoya disease in adults","volume":"128","author":"Jeon JP","year":"2018","unstructured":"Jeon JP, Kim JE, Cho WS, Bang JS, Son YJ, Oh CW. Meta-analysis of the surgical outcomes of symptomatic moyamoya disease in adults. J Neurosurg. 2018;128(3):793\u2013799."},{"issue":"5","key":"b20","series-title":"Neurosurgery","first-page":"852","article-title":"Strategies for and outcome of repeat revascularization surgery for moyamoya disease: an American institutional series","volume":"81","author":"Teo M","year":"2017","unstructured":"Teo M, Johnson J, Steinberg GK. Strategies for and outcome of repeat revascularization surgery for moyamoya disease: an American institutional series. Neurosurgery. 2017;81(5):852\u2013859."},{"issue":"2","key":"b21","series-title":"Neurosurgery","first-page":"201","article-title":"Synergistic interactions between direct and indirect bypasses in combined procedures: the significance of indirect bypasses in moyamoya disease","volume":"80","author":"Uchino H","year":"2017","unstructured":"Uchino H, Kim JH, Fujima N,  Synergistic interactions between direct and indirect bypasses in combined procedures: the significance of indirect bypasses in moyamoya disease. Neurosurgery. 2017;80(2):201\u2013209."},{"issue":"4","key":"b22","series-title":"AJNR Am J Neuroradiol","first-page":"741","article-title":"Postoperative evaluation of moyamoya disease with perfusion-weighted MR imaging: initial experience","volume":"24","author":"Lee SK","year":"2003","unstructured":"Lee SK, Kim DI, Jeong EK,  Postoperative evaluation of moyamoya disease with perfusion-weighted MR imaging: initial experience. AJNR Am J Neuroradiol. 2003;24(4):741\u2013747."},{"issue":"3","key":"b23","series-title":"Radiology","first-page":"630","article-title":"Revascularization evaluation in adult-onset moyamoya disease after bypass surgery: superselective arterial spin labeling perfusion MRI compared with digital subtraction angiography","volume":"297","author":"Hwang I","year":"2020","unstructured":"Hwang I, Cho WS, Yoo RE,  Revascularization evaluation in adult-onset moyamoya disease after bypass surgery: superselective arterial spin labeling perfusion MRI compared with digital subtraction angiography. Radiology. 2020;297(3):630\u2013637."},{"issue":"1","key":"b24","series-title":"Bull Tokyo Med Dent Univ","first-page":"7","article-title":"Angiographic demonstration of cerebral revascularization after encephalo-duro-arterio-synangiosis (EDAS) performed on pediatric moyamoya patients","volume":"29","author":"Matsushima Y","year":"1982","unstructured":"Matsushima Y, Aoyagi M, Fukai N, Tanaka K, Tsuruoka S, Inaba Y. Angiographic demonstration of cerebral revascularization after encephalo-duro-arterio-synangiosis (EDAS) performed on pediatric moyamoya patients. Bull Tokyo Med Dent Univ. 1982;29(1):7\u201317."},{"issue":"suppl","key":"b25","series-title":"Neurol Med Chir (Tokyo)","first-page":"297","article-title":"An indirect revascularization method in the surgical treatment of moyamoya disease\u2014various kinds of indirect procedures and a multiple combined indirect procedure","volume":"38","author":"Matsushima T","year":"1998","unstructured":"Matsushima T, Inoue T, Katsuta T,  An indirect revascularization method in the surgical treatment of moyamoya disease\u2014various kinds of indirect procedures and a multiple combined indirect procedure. Neurol Med Chir (Tokyo). 1998;38(suppl):297-302."},{"issue":"2","key":"b26","series-title":"Neurosurgery","first-page":"315","article-title":"Direct vs indirect revascularization in a North American cohort of moyamoya disease","volume":"89","author":"Lai PMR","year":"2021","unstructured":"Lai PMR, Patel NJ, Frerichs KU,  Direct vs indirect revascularization in a North American cohort of moyamoya disease. Neurosurgery. 2021;89(2):315\u2013322."},{"issue":"1","key":"b27","series-title":"Skull Base","first-page":"27","article-title":"Moyamoya disease in adults: the role of cerebral revascularization","volume":"15","author":"Zipfel GJ","year":"2005","unstructured":"Zipfel GJ, Fox DJ Jr, Rivet DJ. Moyamoya disease in adults: the role of cerebral revascularization. Skull Base. 2005;15(1):27\u201341."},{"issue":"12","key":"b28","series-title":"Stroke","first-page":"2160","article-title":"Angiogenic factors in moyamoya disease","volume":"27","author":"Yoshimoto T","year":"1996","unstructured":"Yoshimoto T, Houkin K, Takahashi A, Abe H. Angiogenic factors in moyamoya disease. Stroke. 1996;27(12):2160\u20132165."},{"issue":"4","key":"b29","series-title":"Int J Mol Sci","first-page":"1696","article-title":"Pathological circulating factors in moyamoya disease","volume":"22","author":"Fang YC","year":"2021","unstructured":"Fang YC, Wei LF, Hu CJ, Tu YK. Pathological circulating factors in moyamoya disease. 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