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      Clinical and Radiological Outcomes After Revascularization of Hemorrhagic Moyamoya Disease

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          Abstract

          Objective: To evaluate clinical and radiological outcomes after revascularization of hemorrhagic moyamoya disease (MMD).

          Materials and Methods: We retrospectively collected patients with hemorrhagic MMD who received revascularization from January 2011 to June 2018 at a high-volume stroke center. Rebleeding, ischemic stroke, modified Rankin Scale (mRS) and death after revascularization were used to evaluate long-term clinical outcome. Poor neurological outcome was defined as a mRS>2. The changes of original and revascularization collaterals were used to evaluate radiological outcome. The clinical and radiological outcomes between patients with different surgical revascularization were compared.

          Results: A total of 312 patients (319 hemispheres) were recruited, including 133 hemispheres (41.7%) with indirect revascularization and 186 hemispheres (58.3%) with direct revascularization. In 308 hemispheres with clinical follow-up data, Postoperative rebleeding, ischemic stroke, poor neurological outcome and death occurred in 13.0% (40/308), 2.6% (8/308), 12.0% (37/308), and 6.2% (19/308) of the hemispheres, respectively. The rates of postoperative rebleeding (8.5 vs. 19.1%, P = 0.006) and poor neurological outcome (8.5 vs. 16.8%, P = 0.026) were lower in hemispheres with direct revascularization than those with indirect revascularization. However, there was no statistically significant difference in the rates of postoperative ischemic stroke (1.1 vs. 4.6%, P = 0.129) and death (4.5 vs. 8.4%, P = 0.162) between the two groups. Multivariate logistic regression analysis indicated that the risk of postoperative rebleeding was higher in those with untreated aneurysms, repetitive bleeding episodes, normal perfusion status, and indirect revascularization ( P < 0.05). In 78 hemispheres with radiological follow-up data, the regression of moyamoya vessels, anterior choroidal artery (AchA), posterior communicating artery (PcomA) and aneurysms were present in 44.9, 47.4, 25.6, and 11.5% of the hemispheres, respectively. The regression of original collaterals and establishment of revascularization collaterals were more significant in hemispheres with direct revascularization than those with indirect revascularization ( P < 0.05).

          Conclusion: Direct revascularization may be superior to indirect revascularization for prevention of rebleeding and poor neurological outcome in adults with hemorrhagic MMD. The risk of postoperative rebleeding was higher in those with untreated aneurysms, repetitive bleeding episodes, normal perfusion status, and indirect revascularization. The regression of original collaterals and establishment of revascularization collaterals after revascularization were more significant in hemispheres with direct revascularization than those with indirect revascularization.

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          Most cited references30

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          Moyamoya disease and moyamoya syndrome.

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            Moyamoya disease: current concepts and future perspectives.

            Moyamoya disease is an uncommon cerebrovascular disease that is characterised by progressive stenosis of the terminal portion of the internal carotid artery and its main branches. The disease is associated with the development of dilated, fragile collateral vessels at the base of the brain, which are termed moyamoya vessels. The incidence of moyamoya disease is high in east Asia, and familial forms account for about 15% of patients with this disease. Moyamoya disease has several unique clinical features, which include two peaks of age distribution at 5 years and at about 40 years. Most paediatric patients have ischaemic attacks, whereas adult patients can have ischaemic attacks, intracranial bleeding, or both. Extracranial-intracranial arterial bypass, including anastomosis of the superficial temporal artery to the middle cerebral artery and indirect bypass, can help prevent further ischaemic attacks, although the beneficial effect on haemorrhagic stroke is still not clear. In this Review, we summarise the epidemiology, aetiology, clinical features, diagnosis, surgical treatment, and outcomes of moyamoya disease. Recent updates and future perspectives for moyamoya disease will also be discussed.
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              Effects of extracranial-intracranial bypass for patients with hemorrhagic moyamoya disease: results of the Japan Adult Moyamoya Trial.

              About one half of those who develop adult-onset moyamoya disease experience intracranial hemorrhage. Despite the extremely high frequency of rebleeding attacks and poor prognosis, measures to prevent rebleeding have not been established. The purpose of this study is to determine whether extracranial-intracranial bypass can reduce incidence of rebleeding and improve patient prognosis.
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                Author and article information

                Contributors
                Journal
                Front Neurol
                Front Neurol
                Front. Neurol.
                Frontiers in Neurology
                Frontiers Media S.A.
                1664-2295
                07 May 2020
                2020
                : 11
                : 382
                Affiliations
                [1] 1Department of Neurology, Beijing Tiantan Hospital, Capital Medical University , Beijing, China
                [2] 2China National Clinical Research Center for Neurological Diseases, Center of Stroke, Beijing Institute for Brain Disorders , Beijing, China
                [3] 3Department of Neurosurgery, Beijing Tiantan Hospital, Capital Medical University , Beijing, China
                Author notes

                Edited by: Nishant K. Mishra, Icahn School of Medicine at Mount Sinai, United States

                Reviewed by: Won-Sang Cho, Seoul National University Hospital, South Korea; Yasushi Takagi, Tokushima University, Japan

                *Correspondence: Dong Zhang zhangdong0660@ 123456aliyun.com

                This article was submitted to Stroke, a section of the journal Frontiers in Neurology

                Article
                10.3389/fneur.2020.00382
                7221061
                32457693
                2d7011e0-02db-4d61-ac23-94a072895117
                Copyright © 2020 Kang, Lu, Ju, Ji, Wang, Shen, Yu, Gao, Zhang and Zhao.

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

                History
                : 10 February 2020
                : 15 April 2020
                Page count
                Figures: 3, Tables: 6, Equations: 0, References: 33, Pages: 10, Words: 6313
                Categories
                Neurology
                Original Research

                Neurology
                moyamoya disease,moyamoya syndrome,intracranial hemorrhage,revascularization,rebleeding
                Neurology
                moyamoya disease, moyamoya syndrome, intracranial hemorrhage, revascularization, rebleeding

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