{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,22]],"date-time":"2026-10-22T18:31:14Z","timestamp":1792693874855,"version":"4.5.0"},"reference-count":48,"publisher":"American Medical Association (AMA)","issue":"6","content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["JAMA Netw Open"],"abstract":"<jats:sec id=\"ab-zoi240508-4\"><jats:title>Importance<\/jats:title><jats:p>Moyamoya disease (MMD) is a rare chronic cerebrovascular disease, and the outcomes of bypass management in adult patients remain controversial.<\/jats:p><\/jats:sec><jats:sec id=\"ab-zoi240508-5\"><jats:title>Objective<\/jats:title><jats:p>To categorize adult MMD based on asymptomatic, ischemic, and hemorrhagic onset and compare the outcomes (death, hemorrhagic stroke [HS], and ischemic stroke [IS]) of bypass surgery (direct or indirect) with those of conservative management.<\/jats:p><\/jats:sec><jats:sec id=\"ab-zoi240508-6\"><jats:title>Design, Setting, and Participants<\/jats:title><jats:p>This retrospective, nationwide, population-based longitudinal cohort study used Korean National Health Insurance Research data to identify adults (aged \u226515 years) with MMD who were diagnosed between January 1, 2008, and December 31, 2020, and followed up until December 31, 2021 (median follow-up, 5.74 [IQR, 2.95-9.42] years). A total of 19\u202f700 participants (3194 with hemorrhagic, 517 with ischemic, and 15\u202f989 with asymptomatic MMD) were included. Data were analyzed from January 2 to April 1, 2023.<\/jats:p><\/jats:sec><jats:sec id=\"ab-zoi240508-7\"><jats:title>Exposures<\/jats:title><jats:p>Bypass surgery and conservative management.<\/jats:p><\/jats:sec><jats:sec id=\"ab-zoi240508-8\"><jats:title>Main Outcomes and Measures<\/jats:title><jats:p>Death constituted the primary outcome; secondary outcomes consisted of HS or IS. Kaplan-Meier survival curve and Cox proportional hazards regression analysis were applied. The propensity score\u2013matching and stratified analyses were performed to control covariate effects.<\/jats:p><\/jats:sec><jats:sec id=\"ab-zoi240508-9\"><jats:title>Results<\/jats:title><jats:p>A total of 19\u202f700 patients (mean [SD] age, 45.43 [14.98] years; 12\u202f766 [64.8%] female) were included. Compared with conservative management, bypass was associated with a reduced risk of death (adjusted hazard ratio [AHR], 0.50 [95% CI, 0.41-0.61]; <jats:italic>P<\/jats:italic>\u2009&amp;amp;lt;\u2009.001) and HS (AHR, 0.36 [0.30-0.40]; <jats:italic>P<\/jats:italic>\u2009&amp;amp;lt;\u2009.001) in hemorrhagic MMD; reduced risk of IS (AHR, 0.55 [95% CI, 0.37-0.81]; <jats:italic>P<\/jats:italic>\u2009=\u2009.002) in ischemic MMD; and reduced risk of death (AHR, 0.74 [95% CI, 0.66-0.84]; <jats:italic>P<\/jats:italic>\u2009&amp;amp;lt;\u2009.001) in asymptomatic MMD. However, bypass was associated with an increased risk of HS (AHR, 1.76 [95% CI, 1.56-2.00]; <jats:italic>P<\/jats:italic>\u2009&amp;amp;lt;\u2009.001) in asymptomatic MMD. Both direct and indirect bypass demonstrated similar effects in hemorrhagic and asymptomatic MMD, except only direct bypass was associated with a reduced risk of IS (AHR, 0.52 [95% CI, 0.33- 0.83]; <jats:italic>P<\/jats:italic>\u2009=\u2009.01) in ischemic MMD. After stratification, bypass was associated with a reduced risk of death in patients younger than 55 years with ischemic (AHR, 0.34 [95% CI, 0.13- 0.88]; <jats:italic>P<\/jats:italic>\u2009=\u2009.03) and asymptomatic (AHR, 0.69 [95% CI, 0.60-0.79]; <jats:italic>P<\/jats:italic>\u2009&amp;amp;lt;\u2009.001) MMD, but an increased risk of HS in patients 55 years or older with ischemic MMD (AHR, 2.13 [95% CI, 1.1-4.16]; <jats:italic>P<\/jats:italic>\u2009=\u2009.03).<\/jats:p><\/jats:sec><jats:sec id=\"ab-zoi240508-10\"><jats:title>Conclusions and Relevance<\/jats:title><jats:p>The findings of this cohort study of bypass outcomes for patients with MMD emphasize the importance of tailoring management strategies in adult patients based on onset types.<\/jats:p><\/jats:sec>","DOI":"10.1001\/jamanetworkopen.2024.15102","type":"journal-article","created":{"date-parts":[[2024,6,6]],"date-time":"2024-06-06T15:33:21Z","timestamp":1717688001000},"page":"e2415102","source":"Crossref","is-referenced-by-count":32,"title":["Outcomes of Bypass Surgery in Adult Moyamoya Disease by Onset Type"],"prefix":"10.1001","volume":"7","author":[{"given":"Yong Cheol","family":"Lim","sequence":"first","affiliation":[{"name":"Department of Neurosurgery, Ajou University School of Medicine, Ajou University Hospital, Suwon, Republic of Korea"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Eunyoung","family":"Lee","sequence":"additional","affiliation":[{"name":"Department of Neurology, McGovern Medical School, The University of Texas Health Science Center at Houston"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jihye","family":"Song","sequence":"additional","affiliation":[{"name":"Department of Neurosurgery, Ajou University School of Medicine, Ajou University Hospital, Suwon, Republic of Korea"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"10","published-online":{"date-parts":[[2024,6,6]]},"reference":[{"issue":"11","key":"zoi240508r1","doi-asserted-by":"publisher","first-page":"1056","DOI":"10.1016\/S1474-4422(08)70240-0","article-title":"Moyamoya disease: current concepts and future perspectives.","volume":"7","author":"Kuroda","year":"2008","journal-title":"Lancet Neurol"},{"issue":"12","key":"zoi240508r2","doi-asserted-by":"publisher","first-page":"1226","DOI":"10.1056\/NEJMra0804622","article-title":"Moyamoya disease and moyamoya syndrome.","volume":"360","author":"Scott","year":"2009","journal-title":"N Engl J Med"},{"issue":"8","key":"zoi240508r3","doi-asserted-by":"publisher","first-page":"747","DOI":"10.1016\/S1474-4422(22)00165-X","article-title":"Moyamoya disease: diagnosis and interventions.","volume":"21","author":"Ihara","year":"2022","journal-title":"Lancet Neurol"},{"issue":"1","key":"zoi240508r4","doi-asserted-by":"publisher","first-page":"2","DOI":"10.5853\/jos.2015.01627","article-title":"Moyamoya disease: epidemiology, clinical features, and diagnosis.","volume":"18","author":"Kim","year":"2016","journal-title":"J Stroke"},{"issue":"4","key":"zoi240508r5","doi-asserted-by":"publisher","first-page":"1090","DOI":"10.1161\/STROKEAHA.113.004273","article-title":"Incidence, prevalence, and survival of moyamoya disease in Korea: a nationwide, population-based study.","volume":"45","author":"Ahn","year":"2014","journal-title":"Stroke"},{"issue":"5","key":"zoi240508r6","doi-asserted-by":"publisher","first-page":"1258","DOI":"10.1161\/STROKEAHA.113.004160","article-title":"Epidemiology of moyamoya disease in Taiwan: a nationwide population-based study.","volume":"45","author":"Chen","year":"2014","journal-title":"Stroke"},{"issue":"1","key":"zoi240508r7","doi-asserted-by":"publisher","first-page":"42","DOI":"10.1161\/STROKEAHA.107.490714","article-title":"Prevalence and clinicoepidemiological features of moyamoya disease in Japan: findings from a nationwide epidemiological survey.","volume":"39","author":"Kuriyama","year":"2008","journal-title":"Stroke"},{"issue":"1","key":"zoi240508r8","doi-asserted-by":"publisher","first-page":"115","DOI":"10.1161\/STROKEAHA.119.027285","article-title":"Prevalence of intracranial aneurysms in patients with systemic vessel aneurysms: a nationwide cohort study.","volume":"51","author":"Song","year":"2020","journal-title":"Stroke"},{"issue":"6","key":"zoi240508r9","doi-asserted-by":"publisher","DOI":"10.1161\/JAHA.120.019009","article-title":"Prevalence of intracranial aneurysm in patients with aortic disease in Korea: a nationwide population-based study.","volume":"10","author":"Song","year":"2021","journal-title":"J Am Heart Assoc"},{"issue":"9","key":"zoi240508r10","doi-asserted-by":"publisher","first-page":"2752","DOI":"10.1161\/STROKEAHA.120.029251","article-title":"Familial risk for moyamoya disease among first-degree relatives, based on a population-based aggregation study in Korea.","volume":"51","author":"Ahn","year":"2020","journal-title":"Stroke"},{"issue":"5","key":"zoi240508r11","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","year":"2014","journal-title":"Stroke"},{"issue":"12","key":"zoi240508r12","doi-asserted-by":"publisher","first-page":"3662","DOI":"10.1161\/STROKEAHA.122.040330","article-title":"Depression or anxiety according to management modalities in patients with unruptured intracranial aneurysms.","volume":"53","author":"Lim","year":"2022","journal-title":"Stroke"},{"issue":"11","key":"zoi240508r13","doi-asserted-by":"publisher","first-page":"2272","DOI":"10.1161\/01.STR.30.11.2272","article-title":"Clinical course, surgical management, and long-term outcome of moyamoya patients with rebleeding after an episode of intracerebral hemorrhage: an extensive follow-up study.","volume":"30","author":"Yoshida","year":"1999","journal-title":"Stroke"},{"issue":"5","key":"zoi240508r14","first-page":"1049","article-title":"High-risk age for rebleeding in patients with hemorrhagic moyamoya disease: long-term follow-up study.","volume":"52","author":"Morioka","year":"2003","journal-title":"Neurosurgery"},{"issue":"5","key":"zoi240508r15","doi-asserted-by":"publisher","first-page":"1060","DOI":"10.1161\/STROKEAHA.118.022771","article-title":"Natural course of moyamoya disease in patients with prior hemorrhagic stroke.","volume":"50","author":"Kang","year":"2019","journal-title":"Stroke"},{"key":"zoi240508r16","doi-asserted-by":"publisher","first-page":"161","DOI":"10.1016\/j.wneu.2017.03.146","article-title":"Ischemic stroke in young adults with moyamoya disease: prognostic factors for stroke recurrence and functional outcome after revascularization.","volume":"103","author":"Zhao","year":"2017","journal-title":"World Neurosurg"},{"issue":"10","key":"zoi240508r17","doi-asserted-by":"publisher","first-page":"2148","DOI":"10.1161\/01.STR.0000182256.32489.99","article-title":"Incidence and clinical features of disease progression in adult moyamoya disease.","volume":"36","author":"Kuroda","year":"2005","journal-title":"Stroke"},{"issue":"5","key":"zoi240508r18","doi-asserted-by":"publisher","first-page":"1430","DOI":"10.1161\/STROKEAHA.106.478297","article-title":"Radiological findings, clinical course, and outcome in asymptomatic moyamoya disease: results of multicenter survey in Japan.","volume":"38","author":"Kuroda","year":"2007","journal-title":"Stroke"},{"issue":"1","key":"zoi240508r19","doi-asserted-by":"publisher","first-page":"44","DOI":"10.1016\/j.jocn.2012.08.002","article-title":"The natural history of moyamoya in a North American adult cohort.","volume":"20","author":"Gross","year":"2013","journal-title":"J Clin Neurosci"},{"issue":"1","key":"zoi240508r20","doi-asserted-by":"publisher","first-page":"82","DOI":"10.3171\/2014.9.JNS132281","article-title":"The natural clinical course of hemodynamically stable adult moyamoya disease.","volume":"122","author":"Cho","year":"2015","journal-title":"J Neurosurg"},{"issue":"1-2","key":"zoi240508r21","doi-asserted-by":"publisher","first-page":"381","DOI":"10.1016\/j.jns.2015.11.018","article-title":"Long term outcome and predictors of ischemic stroke recurrence in adult moyamoya disease.","volume":"359","author":"Noh","year":"2015","journal-title":"J Neurol Sci"},{"issue":"6","key":"zoi240508r22","doi-asserted-by":"publisher","first-page":"1494","DOI":"10.1161\/STROKEAHA.122.041932","article-title":"Five-year stroke risk and its predictors in asymptomatic moyamoya disease: Asymptomatic Moyamoya Registry (AMORE).","volume":"54","author":"Kuroda","year":"2023","journal-title":"Stroke"},{"issue":"12","key":"zoi240508r23","doi-asserted-by":"publisher","first-page":"3572","DOI":"10.1161\/STROKEAHA.122.039584","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","year":"2022","journal-title":"Stroke"},{"key":"zoi240508r24","doi-asserted-by":"publisher","first-page":"283","DOI":"10.1016\/j.wneu.2017.03.101","article-title":"Long-term outcome after conservative treatment and direct bypass surgery of moyamoya disease at late Suzuki stage.","volume":"103","author":"Ge","year":"2017","journal-title":"World Neurosurg"},{"key":"zoi240508r25","doi-asserted-by":"publisher","first-page":"304","DOI":"10.1016\/j.wneu.2016.07.087","article-title":"Indirect bypass surgery may be more beneficial for symptomatic patients with moyamoya disease at early Suzuki stage.","volume":"95","author":"Wang","year":"2016","journal-title":"World Neurosurg"},{"key":"zoi240508r26","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 (\u201cmoyamoya\u201d disease).","volume":"99","author":"Fukui","year":"1997","journal-title":"Clin Neurol Neurosurg"},{"issue":"1","key":"zoi240508r27","doi-asserted-by":"publisher","first-page":"21","DOI":"10.5853\/jos.2015.01739","article-title":"Moyamoya disease: treatment and outcomes.","volume":"18","author":"Kim","year":"2016","journal-title":"J Stroke"},{"issue":"8","key":"zoi240508r28","doi-asserted-by":"publisher","first-page":"1342","DOI":"10.1161\/01.STR.27.8.1342","article-title":"Surgical therapy for adult moyamoya disease: can surgical revascularization prevent the recurrence of intracerebral hemorrhage?","volume":"27","author":"Houkin","year":"1996","journal-title":"Stroke"},{"issue":"8","key":"zoi240508r29","doi-asserted-by":"publisher","DOI":"10.1016\/j.jstrokecerebrovasdis.2022.106588","article-title":"Outcomes of medical management alone for adult patients with cerebral misery perfusion due to ischemic moyamoya disease.","volume":"31","author":"Ogasawara","year":"2022","journal-title":"J Stroke Cerebrovasc Dis"},{"issue":"1","key":"zoi240508r30","doi-asserted-by":"publisher","first-page":"18","DOI":"10.1136\/jnnp.61.1.18","article-title":"Evidence of misery perfusion and risk for recurrent stroke in major cerebral arterial occlusive diseases from PET.","volume":"61","author":"Yamauchi","year":"1996","journal-title":"J Neurol Neurosurg Psychiatry"},{"issue":"12","key":"zoi240508r31","doi-asserted-by":"publisher","first-page":"1055","DOI":"10.1001\/jama.280.12.1055","article-title":"Importance of hemodynamic factors in the prognosis of symptomatic carotid occlusion.","volume":"280","author":"Grubb","year":"1998","journal-title":"JAMA"},{"issue":"12","key":"zoi240508r32","doi-asserted-by":"publisher","first-page":"2513","DOI":"10.1161\/01.STR.28.12.2513","article-title":"A clinical comparison of definite moyamoya disease between South Korea and Japan.","volume":"28","author":"Ikezaki","year":"1997","journal-title":"Stroke"},{"issue":"5","key":"zoi240508r33","doi-asserted-by":"publisher","first-page":"439","DOI":"10.3171\/ped.2005.103.5.0439","article-title":"Headache in pediatric moyamoya disease: review of 204 consecutive cases.","volume":"103","author":"Seol","year":"2005","journal-title":"J Neurosurg"},{"issue":"1","key":"zoi240508r34","doi-asserted-by":"publisher","first-page":"211","DOI":"10.1148\/radiology.196.1.7784569","article-title":"Moyamoya disease: comparison of assessment with MR angiography and MR imaging versus conventional angiography.","volume":"196","author":"Yamada","year":"1995","journal-title":"Radiology"},{"issue":"2","key":"zoi240508r35","doi-asserted-by":"publisher","first-page":"445","DOI":"10.1148\/radiology.195.2.7724764","article-title":"Circle of Willis: evaluation with spiral CT angiography, MR angiography, and conventional angiography.","volume":"195","author":"Katz","year":"1995","journal-title":"Radiology"},{"issue":"2","key":"zoi240508r36","doi-asserted-by":"publisher","first-page":"83","DOI":"10.1016\/S1090-3798(98)80046-9","article-title":"Evaluation of magnetic resonance angiography with selective maximum intensity projection in patients with childhood moyamoya disease.","volume":"2","author":"Takanashi","year":"1998","journal-title":"Eur J Paediatr Neurol"},{"issue":"6","key":"zoi240508r37","doi-asserted-by":"publisher","first-page":"1788","DOI":"10.3171\/2015.6.JNS151105","article-title":"Stroke prevention by direct revascularization for patients with adult-onset moyamoya disease presenting with ischemia.","volume":"124","author":"Kim","year":"2016","journal-title":"J Neurosurg"},{"issue":"9","key":"zoi240508r38","doi-asserted-by":"publisher","first-page":"824","DOI":"10.2176\/nmc.50.824","article-title":"Moyamoya disease: recent progress and outlook.","volume":"50","author":"Takahashi","year":"2010","journal-title":"Neurol Med Chir (Tokyo)"},{"issue":"2","key":"zoi240508r39","first-page":"463","article-title":"Effects of surgical revascularization on peripheral artery aneurysms in moyamoya disease: report of three cases.","volume":"49","author":"Kuroda","year":"2001","journal-title":"Neurosurgery"},{"issue":"3","key":"zoi240508r40","doi-asserted-by":"publisher","first-page":"485","DOI":"10.1016\/j.jocn.2011.05.036","article-title":"Disappearance of aneurysms associated with moyamoya disease after STA-MCA anastomosis with encephaloduro myosynangiosis.","volume":"19","author":"Ni","year":"2012","journal-title":"J Clin Neurosci"},{"issue":"1","key":"zoi240508r41","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","year":"2016","journal-title":"Stroke"},{"issue":"6","key":"zoi240508r42","doi-asserted-by":"publisher","first-page":"976","DOI":"10.3171\/jns.2000.93.6.0976","article-title":"Long-term natural history of hemorrhagic moyamoya disease in 42 patients.","volume":"93","author":"Kobayashi","year":"2000","journal-title":"J Neurosurg"},{"key":"zoi240508r43","doi-asserted-by":"publisher","first-page":"S194","DOI":"10.1016\/S0303-8467(97)00078-4","article-title":"The efficacy of bypass surgery for the patients with hemorrhagic moyamoya disease.","volume":"99","author":"Fujii","year":"1997","journal-title":"Clin Neurol Neurosurg"},{"issue":"2","key":"zoi240508r44","doi-asserted-by":"publisher","first-page":"1709","DOI":"10.1007\/s10143-021-01689-w","article-title":"Surgical revascularization vs. conservative treatment for adult hemorrhagic moyamoya disease: analysis of rebleeding in 322 consecutive patients.","volume":"45","author":"Yu","year":"2022","journal-title":"Neurosurg Rev"},{"issue":"3","key":"zoi240508r45","doi-asserted-by":"publisher","first-page":"793","DOI":"10.3171\/2016.11.JNS161688","article-title":"Meta-analysis of the surgical outcomes of symptomatic moyamoya disease in adults.","volume":"128","author":"Jeon","year":"2018","journal-title":"J Neurosurg"},{"key":"zoi240508r46","doi-asserted-by":"publisher","first-page":"179","DOI":"10.1016\/j.wneu.2016.04.083","article-title":"Perioperative complications and long-term outcomes after bypasses in adults with moyamoya disease: a systematic review and meta-analysis.","volume":"92","author":"Sun","year":"2016","journal-title":"World Neurosurg"},{"issue":"5","key":"zoi240508r47","doi-asserted-by":"publisher","first-page":"1523","DOI":"10.3171\/2015.8.JNS15504","article-title":"Direct versus indirect revascularization procedures for moyamoya disease: a comparative effectiveness study.","volume":"126","author":"Macyszyn","year":"2017","journal-title":"J Neurosurg"},{"issue":"2","key":"zoi240508r48","doi-asserted-by":"publisher","first-page":"94","DOI":"10.1159\/000356350","article-title":"Clinical course of asymptomatic adult moyamoya disease.","volume":"37","author":"Jo","year":"2014","journal-title":"Cerebrovasc Dis"}],"container-title":["JAMA Network Open"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/jamanetwork.com\/journals\/jamanetworkopen\/articlepdf\/2819638\/lim_2024_oi_240508_1717008673.52405.pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2024,6,6]],"date-time":"2024-06-06T15:33:26Z","timestamp":1717688006000},"score":1,"resource":{"primary":{"URL":"https:\/\/jamanetwork.com\/journals\/jamanetworkopen\/fullarticle\/2819638"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2024,6,6]]},"references-count":48,"journal-issue":{"issue":"6","published-print":{"date-parts":[[2024,6,3]]}},"URL":"https:\/\/doi.org\/10.1001\/jamanetworkopen.2024.15102","relation":{},"ISSN":["2574-3805"],"issn-type":[{"value":"2574-3805","type":"electronic"}],"subject":[],"published":{"date-parts":[[2024,6,6]]}}}