{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,12]],"date-time":"2026-10-12T14:28:54Z","timestamp":1791815334787,"version":"4.3.4"},"reference-count":17,"publisher":"Frontiers Media SA","license":[{"start":{"date-parts":[[2022,5,6]],"date-time":"2022-05-06T00:00:00Z","timestamp":1651795200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100001809","name":"National Natural Science Foundation of China","doi-asserted-by":"publisher","award":["82171280"],"award-info":[{"award-number":["82171280"]}],"id":[{"id":"10.13039\/501100001809","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["frontiersin.org"],"crossmark-restriction":true},"short-container-title":["Front. Neurol."],"abstract":"<jats:sec><jats:title>Objective<\/jats:title><jats:p>To explore the long-term progression of neoangiogenesis after indirect revascularization for moyamoya disease (MMD).<\/jats:p><\/jats:sec><jats:sec><jats:title>Methods<\/jats:title><jats:p>We enrolled patients who were diagnosed with MMD and treated by encephaloduroarteriosynangiosis (EDAS) surgery at our center from December 2002 through September 2009. A comparative study between short-term (6\u201312 months) and long-term (duration \u2265 8 years) follow-up angiographies was performed. The development of collateral circulation through EDAS was graded according to the system described by the Matsushima grade system.<\/jats:p><\/jats:sec><jats:sec><jats:title>Results<\/jats:title><jats:p>A total of 78 patients who received indirect EDAS were enrolled in the study. The mean age at the first operation was 26.9 \u00b1 15.0 years. The Matsushima grades of the same hemisphere were higher at the long-term follow-up compared with the short-term follow-up. Importantly, no attenuation was observed in any hemisphere during the long-term follow-up. In total, 51 hemispheres (32.7%) and 26 hemispheres (16.6%) had progression during the short-term and the long-term follow-up, respectively. The ipsilateral Suzuki stage showed a significant negative correlation with progression pace. Furthermore, higher Suzuki stages were significantly correlated with the postsurgical Matsushima grade at both time points. A total of nine strokes (11.5%) occurred in 78 patients was reported at the long-term follow-up. The annual incidence rate of recurrent strokes was higher for the stage progression group than for the stable group.<\/jats:p><\/jats:sec><jats:sec><jats:title>Conclusion<\/jats:title><jats:p>For patients with MMD, postsurgical neoangiogenesis after indirect bypass continuously improved with time. The short-term progression of the internal carotid artery (ICA) might be attributed to cerebral revascularization, while the long-term progression should be attributed to the natural progression of the disease.<\/jats:p><\/jats:sec>","DOI":"10.3389\/fneur.2022.861187","type":"journal-article","created":{"date-parts":[[2022,5,6]],"date-time":"2022-05-06T08:11:36Z","timestamp":1651824696000},"update-policy":"https:\/\/doi.org\/10.3389\/crossmark-policy","source":"Crossref","is-referenced-by-count":13,"title":["Recognition of the Effect of Indirect Revascularization for Moyamoya Disease: The Balance Between the Stage Progression and Neoangiogenesis"],"prefix":"10.3389","volume":"13","author":[{"given":"Xiang-Yang","family":"Bao","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Qian-Nan","family":"Wang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Xiao-Peng","family":"Wang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ri-Miao","family":"Yang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Zheng-Xing","family":"Zou","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Qian","family":"Zhang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"De-Sheng","family":"Li","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Lian","family":"Duan","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1965","published-online":{"date-parts":[[2022,5,6]]},"reference":[{"key":"B1","doi-asserted-by":"publisher","first-page":"S11","DOI":"10.1016\/S0303-8467(97)00033-4","article-title":"Natural history of moyamoya disease: comparison of activity of daily living in surgery and non-surgery groups","volume":"99","author":"Choi","year":"1997","journal-title":"Clin Neurol Neurosurg."},{"key":"B2","doi-asserted-by":"publisher","first-page":"288","DOI":"10.1001\/archneur.1969.00480090076012","article-title":"Cerebrovascular \u201cmoyamoya\u201d disease. Disease showing abnormal net-like vessels in base of brain","volume":"20","author":"Suzuki","year":"1969","journal-title":"Arch Neurol."},{"key":"B3","doi-asserted-by":"publisher","first-page":"476","DOI":"10.1161\/STROKEAHA.117.018563","article-title":"Surgical management of moyamoya disease","volume":"49","author":"Acker","year":"2018","journal-title":"Stroke."},{"key":"B4","doi-asserted-by":"publisher","first-page":"427","DOI":"10.1016\/j.wneu.2017.09.001","article-title":"Chronologic evaluation of cerebral hemodynamics by dynamic susceptibility contrast magnetic resonance imaging after indirect bypass surgery for moyamoya disease","volume":"108","author":"Ishii","year":"2017","journal-title":"World Neurosurg."},{"key":"B5","doi-asserted-by":"publisher","first-page":"1898","DOI":"10.3171\/2017.12.JNS172246","article-title":"Encephaloduroarteriosynangiosis for hemorrhagic moyamoya disease: long-term outcome of a consecutive series of 95 adult patients from a single center","volume":"130","author":"Wang","year":"2019","journal-title":"J Neurosurg."},{"key":"B6","doi-asserted-by":"publisher","first-page":"e482","DOI":"10.1016\/j.wneu.2018.04.076","article-title":"Long-term outcomes after encephaloduroarteriosynangiosis in adult patients with moyamoya disease presenting with ischemia","volume":"115","author":"Bao","year":"2018","journal-title":"World Neurosurg."},{"key":"B7","doi-asserted-by":"publisher","first-page":"173","DOI":"10.3171\/2018.2.PEDS17591","article-title":"Encephaloduroarteriosynangiosis for pediatric moyamoya disease: long-term follow-up of 100 cases at a single center","volume":"22","author":"Zhang","year":"2018","journal-title":"J Neurosurg Pediatr."},{"key":"B8","doi-asserted-by":"publisher","first-page":"901","DOI":"10.1177\/0883073818798515","article-title":"Encephaloduroarteriosynangiosis for pediatric moyamoya disease: a single-center experience with 67 cases in China","volume":"33","author":"Wang","year":"2018","journal-title":"J Child Neurol."},{"key":"B9","doi-asserted-by":"publisher","first-page":"480","DOI":"10.3171\/2017.5.JNS17353","article-title":"Direct vs. indirect revascularization in the treatment of moyamoya disease","volume":"129","author":"Park","year":"2018","journal-title":"J Neurosurg."},{"key":"B10","doi-asserted-by":"publisher","first-page":"91","DOI":"10.1007\/s00062-018-0748-3","article-title":"Time course of neoangiogenesis after indirect bypass surgery for moyamoya disease : comparison of short-term and long-term follow-up angiography","volume":"30","author":"Zhao","year":"2018","journal-title":"Clin Neuroradiol."},{"key":"B11","doi-asserted-by":"publisher","first-page":"245","DOI":"10.2176\/nmc.52.245","article-title":"Guidelines for diagnosis and treatment of moyamoya disease (spontaneous occlusion of the circle of Willis)","volume":"52","author":"Nobuo","year":"2012","journal-title":"Neurol Med Chir"},{"key":"B12","doi-asserted-by":"publisher","first-page":"305","DOI":"10.1159\/000343225","article-title":"Clinical features, surgical treatment and long-term outcome in adult patients with Moyamoya disease in China","volume":"34","author":"Bao","year":"2012","journal-title":"Cerebrovasc Dis."},{"key":"B13","doi-asserted-by":"publisher","first-page":"75","DOI":"10.1159\/000369524","article-title":"Clinical features, surgical treatment, and long-term outcome in pediatric patients with moyamoya disease in China","volume":"39","author":"Bao","year":"2015","journal-title":"Cerebrovasc Dis."},{"key":"B14","doi-asserted-by":"publisher","first-page":"401","DOI":"10.1227\/00006123-199209000-00003","article-title":"Surgical treatment of moyamoya disease in pediatric patients, comparison between the results of indirect and direct revascularization procedures","volume":"31","author":"Matsushima","year":"1992","journal-title":"Neurosurgery."},{"key":"B15","doi-asserted-by":"publisher","first-page":"156","DOI":"10.3171\/ped.2004.100.2.0156","article-title":"Long-term effects of indirect bypass surgery on collateral vessel formation in pediatric moyamoya disease","volume":"100","author":"Goda","year":"2004","journal-title":"J Neurosurg"},{"key":"B16","doi-asserted-by":"publisher","first-page":"1180","DOI":"10.1097\/SCS.0000000000005256","article-title":"Cerebral revascularization accelerates the angiographic staging progression of the operated hemisphere in a pediatric patient with moyamoya disease","volume":"30","author":"Yu","year":"2019","journal-title":"J Craniofac Surg."},{"key":"B17","doi-asserted-by":"publisher","first-page":"1342","DOI":"10.1161\/01.STR.27.8.1342","article-title":"Surgical therapy for adult moyamoya disease. 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