{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,25]],"date-time":"2026-09-25T03:12:20Z","timestamp":1790305940322,"version":"4.1.0"},"reference-count":52,"publisher":"Journal of Neurosurgery Publishing Group (JNSPG)","issue":"1","content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"published-print":{"date-parts":[[2020,1]]},"abstract":"<jats:sec><jats:title>OBJECTIVE<\/jats:title><jats:p>The effect of indirect revascularization to improve cerebral perfusion for moyamoya disease (MMD) is based on ingrowth of new vessels into the cortical brain. Preoperative indicators for neoangiogenesis would be helpful to the selection of appropriate procedures for MMD patients but have not yet been investigated. Our study aimed to identify potential predictors for neovascularization after indirect bypass surgery.<\/jats:p><\/jats:sec><jats:sec><jats:title>METHODS<\/jats:title><jats:p>The authors reviewed consecutive cases with complete clinical and radiological documentation of patients who had undergone surgery between December 2010 and January 2018. Patients who were treated with indirect bypass surgery were included. Cerebrovascular characteristics were evaluated by catheter angiography. Neoangiogenesis after indirect bypass was determined as \u201cgood\u201d or \u201cpoor\u201d based on the Matsushima standard. Univariate and multivariate analyses were performed to identify predictors for neoangiogenesis after indirect bypass. Subgroup analyses by onset type and surgical type were carried out to identify specific predictors for different populations.<\/jats:p><\/jats:sec><jats:sec><jats:title>RESULTS<\/jats:title><jats:p>In total, 231 hemispheres of 209 patients (mean \u00b1 SD age 23.06 \u00b1 15.09 years, range 3\u201361 years) were retrospectively included. In 146 (63.2%) hemispheres, good neoangiogenesis was observed after indirect revascularization. Multivariate analysis showed that the status of ICA moyamoya vessels (p &lt; 0.001, OR [95% CI] 3.242 [2.007\u20135.236]) is a predictor of favorable neoangiogenesis after indirect bypass surgery, whereas hemorrhagic onset (p &lt; 0.001, OR [95% CI] 0.138 [0.054\u20130.353]) is a risk factor for poor neoangiogenesis. In addition, younger age was significantly associated with good neovascularization in patients with hemorrhagic onset (p <jats:italic>=<\/jats:italic> 0.027, OR [95% CI] 0.893 [0.808\u20130.987]), whereas age was not a significant predictor for neovascularization in non\u2013hemorrhagic-onset patients (p = 0.955). Hemispheres with good revascularization had lower incidence of rebleeding, lower modified Rankin Scale scores, and more improvement of symptoms during long-term follow-up (p = 0.026, 0.006, and 0.013, respectively).<\/jats:p><\/jats:sec><jats:sec><jats:title>CONCLUSIONS<\/jats:title><jats:p>Hemorrhagic onset predicts poor neovascularization after indirect bypass surgery for MMD patients. Abundant ICA moyamoya vessels indicate good neoangiogenesis after indirect bypass and vice versa, whereas absent ICA moyamoya vessels predict poor revascularization. Good neovascularization was associated with better long-term outcome. Future studies are needed to further address this issue and clarify the underlying pathophysiological mechanisms.<\/jats:p><\/jats:sec>","DOI":"10.3171\/2018.9.jns181562","type":"journal-article","created":{"date-parts":[[2019,2,27]],"date-time":"2019-02-27T00:15:01Z","timestamp":1551226501000},"page":"98-108","source":"Crossref","is-referenced-by-count":29,"title":["Predictors of neoangiogenesis after indirect revascularization in moyamoya disease: a multicenter retrospective study"],"prefix":"10.3171","volume":"132","author":[{"given":"Yahui","family":"Zhao","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jiaxi","family":"Li","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Junlin","family":"Lu","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Qian","family":"Zhang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Dong","family":"Zhang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Rong","family":"Wang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yuanli","family":"Zhao","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Xiaolin","family":"Chen","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1754","reference":[{"key":"ref401","doi-asserted-by":"crossref","first-page":"258","DOI":"10.1136\/jnnp-2012-302236","article-title":"Long term outcome after conservative and surgical treatment of haemorrhagic moyamoya disease","volume":"84","author":"Liu","year":"2013","journal-title":"J Neurol Neurosurg Psychiatry"},{"key":"ref521","first-page":"3570","article-title":"Clinical and angiographic outcomes after combined direct and indirect bypass in adult patients with moyamoya disease: a retrospective study of 76 procedures","volume":"15","author":"Zhao","year":"2018","journal-title":"Exp Ther Med"},{"key":"ref51","doi-asserted-by":"crossref","first-page":"327","DOI":"10.2176\/nmc.52.327","article-title":"Lessons learned from moyamoya disease: outcome of direct\/indirect revascularization surgery for 150 affected hemispheres","volume":"52","author":"Fujimura","year":"2012","journal-title":"Neurol Med Chir (Tokyo)"},{"key":"ref431","doi-asserted-by":"crossref","first-page":"S156","DOI":"10.1016\/S0303-8467(97)00056-5","article-title":"Long-term results of surgically treated moyamoya disease","volume":"99","author":"Nakashima","year":"1997","journal-title":"Clin Neurol Neurosurg"},{"key":"ref151","doi-asserted-by":"crossref","first-page":"401","DOI":"10.1227\/00006123-199209000-00003","article-title":"Surgical treatment of moyamoya disease in pediatric patients\u2014comparison between the results of indirect and direct revascularization procedures","volume":"31","author":"Matsushima","year":"1992","journal-title":"Neurosurgery"},{"key":"ref111","doi-asserted-by":"crossref","first-page":"1456","DOI":"10.1227\/01.NEU.0000333810.49283.39","article-title":"Combined encephaloduroarteriosynangiosis and bifrontal encephalogaleo (periosteal) synangiosis in pediatric moyamoya disease","volume":"62","author":"Kim","year":"2008","journal-title":"Neurosurgery"},{"key":"ref501","doi-asserted-by":"crossref","first-page":"288","DOI":"10.1001\/archneur.1969.00480090076012","article-title":"Cerebrovascular \"moyamoya\" disease. 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