{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,15]],"date-time":"2026-10-15T01:13:34Z","timestamp":1792026814835,"version":"4.4.0"},"reference-count":17,"publisher":"Journal of Neurosurgery Publishing Group (JNSPG)","issue":"5","content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"published-print":{"date-parts":[[2019,5]]},"abstract":"<jats:sec><jats:title>OBJECTIVE<\/jats:title><jats:p>This study was performed to identify the angiographic features of hemorrhagic-onset moyamoya disease (MMD) in comparison with those of patients with ischemic-onset MMD.<\/jats:p><\/jats:sec><jats:sec><jats:title>METHODS<\/jats:title><jats:p>This case-control study compared the data set of the Japan Adult Moyamoya (JAM) Trial with the angiographic data of adult patients with ischemic-onset MMD. The authors analyzed angiograms obtained at onset, classifying the collaterals into 3 subtypes: lenticulostriate anastomosis, thalamic anastomosis, and choroidal anastomosis. They then compared the extent of these collaterals, as indicated by the collateral development grade from 0 to 2 in each subtype, between the JAM Trial group and the ischemic-onset group. They also compared the involvement of the posterior cerebral artery (PCA) and Suzuki\u2019s angiographic staging between each group.<\/jats:p><\/jats:sec><jats:sec><jats:title>RESULTS<\/jats:title><jats:p>Among 89 ischemic-onset patients, 103 symptomatic hemispheres in 80 patients were analyzed and compared with 75 hemorrhagic hemispheres from the JAM Trial. The hemorrhagic-onset patients showed a significantly higher proportion of thalamic anastomosis (p = 0.043) and choroidal anastomosis (&lt; 0.001), as indicated by grade 2 in each subtype, compared with ischemic-onset patients. Suzuki\u2019s angiographic staging was significantly higher in the hemorrhagic group (&lt; 0.038). There was no difference in the extent of lenticulostriate anastomosis and PCA involvement between the groups.<\/jats:p><\/jats:sec><jats:sec><jats:title>CONCLUSIONS<\/jats:title><jats:p>In adult MMD, the characteristic pattern of the abnormal vascular networks at the base of the brain is different between each onset type. In light of the more prominent development of thalamic and choroidal anastomosis in the JAM Trial group in the present study, development of these collaterals, especially the choroidal collateral extending beyond the lateral ventricle, may play a critical role in hemorrhagic presentation in MMD.<\/jats:p><jats:p>Clinical trial registration no. C000000166 (<jats:ext-link xmlns:xlink=\"http:\/\/www.w3.org\/1999\/xlink\" ext-link-type=\"uri\" xlink:href=\"http:\/\/www.umin.ac.jp\/ctr\/index.htm\">http:\/\/www.umin.ac.jp\/ctr\/index.htm<\/jats:ext-link>)<\/jats:p><\/jats:sec>","DOI":"10.3171\/2017.11.jns171990","type":"journal-article","created":{"date-parts":[[2018,5,4]],"date-time":"2018-05-04T13:59:50Z","timestamp":1525442390000},"page":"1453-1459","source":"Crossref","is-referenced-by-count":64,"title":["Intrinsic development of choroidal and thalamic collaterals in hemorrhagic-onset moyamoya disease: case-control study of the Japan Adult Moyamoya Trial"],"prefix":"10.3171","volume":"130","author":[{"given":"Miki","family":"Fujimura","sequence":"first","affiliation":[{"name":"Department of Neurosurgery, Tohoku University Graduate School of Medicine, Sendai;"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Takeshi","family":"Funaki","sequence":"additional","affiliation":[{"name":"Department of Neurosurgery, Kyoto University Graduate School of Medicine, Kyoto;"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Kiyohiro","family":"Houkin","sequence":"additional","affiliation":[{"name":"Department of Neurosurgery, Hokkaido University Graduate School of Medicine, Sapporo;"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jun C.","family":"Takahashi","sequence":"additional","affiliation":[{"name":"Department of Neurosurgery, National Cerebral and Cardiovascular Center, Suita;"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Satoshi","family":"Kuroda","sequence":"additional","affiliation":[{"name":"Department of Neurosurgery, Graduate School of Medicine and Pharmaceutical Sciences, University of Toyama, Toyama; and"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yasutake","family":"Tomata","sequence":"additional","affiliation":[{"name":"Division of Epidemiology, Department of Health Informatics and Public Health, Tohoku University School of Public Health, Graduate School of Medicine, Sendai, Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Teiji","family":"Tominaga","sequence":"additional","affiliation":[{"name":"Department of Neurosurgery, Tohoku University Graduate School of Medicine, Sendai;"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Susumu","family":"Miyamoto","sequence":"additional","affiliation":[{"name":"Department of Neurosurgery, Kyoto University Graduate School of Medicine, Kyoto;"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1754","reference":[{"key":"b1","series-title":"Neurosurgery","doi-asserted-by":"publisher","first-page":"625","DOI":"10.1227\/NEU.0b013e3182333c47","article-title":"Quantitative angiographic comparison with the OSIRIS program between the direct and indirect revascularization modalities in adult moyamoya disease","volume":"70","author":"Bang JS","year":"2012","unstructured":"Bang JS, Kwon OK, Kim JE, Kang HS, Park H, Cho SY, : Quantitative angiographic comparison with the OSIRIS program between the direct and indirect revascularization modalities in adult moyamoya disease. Neurosurgery 70:625\u2013633, 201210.1227\/NEU.0b013e3182333c4721866061"},{"key":"b2","series-title":"Stroke","doi-asserted-by":"publisher","first-page":"3025","DOI":"10.1161\/STROKEAHA.114.005624","article-title":"Long-term outcomes after combined revascularization surgery in adult moyamoya disease","volume":"45","author":"Cho WS","year":"2014","unstructured":"Cho WS, Kim JE, Kim CH, Ban SP, Kang HS, Son YJ, : Long-term outcomes after combined revascularization surgery in adult moyamoya disease. Stroke 45:3025\u20133031, 20142518435910.1161\/STROKEAHA.114.005624"},{"key":"b3","series-title":"Tohoku J Exp Med","doi-asserted-by":"publisher","first-page":"45","DOI":"10.1620\/tjem.236.45","article-title":"Current status of revascularization surgery for moyamoya disease: special consideration for its \u2018internal carotid-external carotid (IC-EC) conversion\u2019 as the physiological reorganization system","volume":"236","author":"Fujimura M","year":"2015","unstructured":"Fujimura M, Tominaga T: Current status of revascularization surgery for moyamoya disease: special consideration for its \u2018internal carotid-external carotid (IC-EC) conversion\u2019 as the physiological reorganization system. Tohoku J Exp Med 236:45\u201353, 201510.1620\/tjem.236.4525971859"},{"key":"b4","series-title":"Neurol Med Chir (Tokyo)","doi-asserted-by":"publisher","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 M","year":"2012","unstructured":"Fujimura M, Tominaga T: Lessons learned from moyamoya disease: outcome of direct\/indirect revascularization surgery for 150 affected hemispheres. Neurol Med Chir (Tokyo) 52:327\u2013332, 201210.2176\/nmc.52.327"},{"key":"b5","series-title":"Clin Neurol Neurosurg","doi-asserted-by":"publisher","first-page":"S238","DOI":"10.1016\/S0303-8467(97)00082-6","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 99 (Suppl 2):S238\u2013S240, 199710.1016\/S0303-8467(97)00082-69409446"},{"key":"b6","series-title":"Neurol Med Chir (Tokyo)","doi-asserted-by":"publisher","first-page":"204","DOI":"10.2176\/nmc.oa.2014-0360","article-title":"Visualization of periventricular collaterals in moyamoya disease with flow-sensitive black-blood magnetic resonance angiography: preliminary experience","volume":"55","author":"Funaki T","year":"2015","unstructured":"Funaki T, Fushimi Y, Takahashi JC, Takagi Y, Araki Y, Yoshida K, : Visualization of periventricular collaterals in moyamoya disease with flow-sensitive black-blood magnetic resonance angiography: preliminary experience. Neurol Med Chir (Tokyo) 55:204\u2013209, 201510.2176\/nmc.oa.2014-0360"},{"key":"b7","series-title":"J Neurosurg","doi-asserted-by":"publisher","first-page":"777","DOI":"10.3171\/2016.11.JNS161650","article-title":"Angiographic features of hemorrhagic moyamoya disease with high recurrence risk: a supplementary analysis of the Japan Adult Moyamoya Trial","volume":"128","author":"Funaki T","year":"2018","unstructured":"Funaki T, Takahashi JC, Houkin K, Kuroda S, Takeuchi S, Fujimura M, : Angiographic features of hemorrhagic moyamoya disease with high recurrence risk: a supplementary analysis of the Japan Adult Moyamoya Trial. J Neurosurg 128:777\u2013784, 20182840973610.3171\/2016.11.JNS161650"},{"key":"b8","series-title":"J Neurosurg Pediatr","doi-asserted-by":"publisher","first-page":"626","DOI":"10.3171\/2013.9.PEDS13111","article-title":"Impact of posterior cerebral artery involvement on long-term clinical and social outcome of pediatric moyamoya disease","volume":"12","author":"Funaki T","year":"2013","unstructured":"Funaki T, Takahashi JC, Takagi Y, Yoshida K, Araki Y, Kikuchi T, : Impact of posterior cerebral artery involvement on long-term clinical and social outcome of pediatric moyamoya disease. J Neurosurg Pediatr 12:626\u2013632, 201310.3171\/2013.9.PEDS1311124138143"},{"key":"b9","series-title":"J Neurosurg","doi-asserted-by":"publisher","first-page":"1766","DOI":"10.3171\/2015.6.JNS15845","article-title":"Periventricular anastomosis in moyamoya disease: detecting fragile collateral vessels with MR angiography","volume":"124","author":"Funaki T","year":"2016","unstructured":"Funaki T, Takahashi JC, Yoshida K, Takagi Y, Fushimi Y, Kikuchi T, : Periventricular anastomosis in moyamoya disease: detecting fragile collateral vessels with MR angiography. J Neurosurg 124:1766\u20131772, 20162661317610.3171\/2015.6.JNS15845"},{"key":"b10","series-title":"Acta Neurochir (Wien)","doi-asserted-by":"publisher","first-page":"1282","DOI":"10.1007\/BF01411056","article-title":"A source of haemorrhage in adult patients with moyamoya disease: the significance of tributaries from the choroidal artery","volume":"138","author":"Irikura K","year":"1996","unstructured":"Irikura K, Miyasaka Y, Kurata A, Tanaka R, Fujii K, Yada K, : A source of haemorrhage in adult patients with moyamoya disease: the significance of tributaries from the choroidal artery. Acta Neurochir (Wien) 138:1282\u20131286, 199610.1007\/BF01411056"},{"key":"b11","series-title":"J Neurosurg","doi-asserted-by":"publisher","first-page":"1048","DOI":"10.3171\/2014.7.JNS132434","article-title":"Outcome in adult patients with hemorrhagic moyamoya disease after combined extracranial-intracranial bypass","volume":"121","author":"Jiang H","year":"2014","unstructured":"Jiang H, Ni W, Xu B, Lei Y, Tian Y, Xu F, : Outcome in adult patients with hemorrhagic moyamoya disease after combined extracranial-intracranial bypass. J Neurosurg 121:1048\u20131055, 201410.3171\/2014.7.JNS13243425127415"},{"key":"b12","series-title":"J Neurosurg","doi-asserted-by":"publisher","first-page":"1032","DOI":"10.3171\/jns.1984.61.6.1032","article-title":"Study of the posterior circulation in moyamoya disease. Clinical and neuroradiological evaluation","volume":"61","author":"Miyamoto S","year":"1984","unstructured":"Miyamoto S, Kikuchi H, Karasawa J, Nagata I, Ikota T, Takeuchi S: Study of the posterior circulation in moyamoya disease. Clinical and neuroradiological evaluation. J Neurosurg 61:1032\u20131037, 198410.3171\/jns.1984.61.6.10326502231"},{"key":"b13","series-title":"Stroke","doi-asserted-by":"publisher","first-page":"1415","DOI":"10.1161\/STROKEAHA.113.004386","article-title":"Effects of extracranial-intracranial bypass for patients with hemorrhagic moyamoya disease: results of the Japan Adult Moyamoya Trial","volume":"45","author":"Miyamoto S","year":"2014","unstructured":"Miyamoto S, Yoshimoto T, Hashimoto N, Okada Y, Tsuji I, Tominaga T, : Effects of extracranial-intracranial bypass for patients with hemorrhagic moyamoya disease: results of the Japan Adult Moyamoya Trial. Stroke 45:1415\u20131421, 20142466820310.1161\/STROKEAHA.113.004386"},{"key":"b14","series-title":"Stroke","doi-asserted-by":"publisher","first-page":"90","DOI":"10.1161\/01.STR.0000047120.67507.0D","article-title":"Angiographic dilatation and branch extension of the anterior choroidal and posterior communicating arteries are predictors of hemorrhage in adult moyamoya patients","volume":"34","author":"Morioka M","year":"2003","unstructured":"Morioka M, Hamada J, Kawano T, Todaka T, Yano S, Kai Y, : Angiographic dilatation and branch extension of the anterior choroidal and posterior communicating arteries are predictors of hemorrhage in adult moyamoya patients. Stroke 34:90\u201395, 20031251175610.1161\/01.STR.0000047120.67507.0D"},{"key":"b15","series-title":"Neurol Med Chir (Tokyo)","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":"Research Committee on the Pathology and Treatment of Spontaneous Occlusion of the Circle of Willis","year":"2012","unstructured":"Research Committee on the Pathology and Treatment of Spontaneous Occlusion of the Circle of Willis: Guidelines for diagnosis and treatment of moyamoya disease (spontaneous occlusion of the circle of Willis). Neurol Med Chir (Tokyo) 52:245\u2013266, 201210.2176\/nmc.52.245"},{"key":"b16","series-title":"Arch Neurol","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 J","year":"1969","unstructured":"Suzuki J, Takaku A: Cerebrovascular \u201cmoyamoya\u201d disease. Disease showing abnormal net-like vessels in base of brain. Arch Neurol 20:288\u2013299, 1969577528310.1001\/archneur.1969.00480090076012"},{"key":"b17","series-title":"Stroke","doi-asserted-by":"publisher","first-page":"37","DOI":"10.1161\/STROKEAHA.115.010819","article-title":"Significance of the hemorrhagic site for recurrent bleeding: prespecified analysis in the Japan Adult Moyamoya Trial","volume":"47","author":"Takahashi JC","year":"2016","unstructured":"Takahashi JC, Funaki T, Houkin K, Inoue T, Ogasawara K, Nakagawara J, : Significance of the hemorrhagic site for recurrent bleeding: prespecified analysis in the Japan Adult Moyamoya Trial. Stroke 47:37\u201343, 201610.1161\/STROKEAHA.115.01081926645256"}],"container-title":["Journal of Neurosurgery"],"original-title":[],"link":[{"URL":"https:\/\/thejns.org\/view\/journals\/j-neurosurg\/130\/5\/article-p1453.xml","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/thejns.org\/downloadpdf\/journals\/j-neurosurg\/130\/5\/article-p1453.xml","content-type":"text\/html","content-version":"vor","intended-application":"syndication"},{"URL":"https:\/\/thejns.org\/downloadpdf\/journals\/j-neurosurg\/130\/5\/article-p1453.xml","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2023,3,26]],"date-time":"2023-03-26T06:56:58Z","timestamp":1679813818000},"score":1,"resource":{"primary":{"URL":"https:\/\/thejns.org\/view\/journals\/j-neurosurg\/130\/5\/article-p1453.xml"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2019,5]]},"references-count":17,"journal-issue":{"issue":"5"},"URL":"https:\/\/doi.org\/10.3171\/2017.11.jns171990","relation":{},"ISSN":["0022-3085","1933-0693"],"issn-type":[{"value":"0022-3085","type":"print"},{"value":"1933-0693","type":"electronic"}],"subject":[],"published":{"date-parts":[[2019,5]]}}}