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J Neurosurg. 2018 Mar;128(3):777-784. doi: 10.3171/2016.11.JNS161650. Epub 2017 Apr 14.

Angiographic features of hemorrhagic moyamoya disease with high recurrence risk: a supplementary analysis of the Japan Adult Moyamoya Trial.

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1Department of Neurosurgery, Kyoto University Graduate School of Medicine, Kyoto.
2Department of Neurosurgery, National Cerebral and Cardiovascular Center, Suita.
3Department of Neurosurgery, Hokkaido University Graduate School of Medicine, Sapporo.
4Department of Neurosurgery, Graduate School of Medicine and Pharmaceutical Sciences, University of Toyama.
5Department of Neurosurgery, Nagaoka Chuo General Hospital, Nagaoka.
6Department of Neurosurgery, Tohoku University Graduate School of Medicine, Sendai; and.
7Division of Epidemiology, Department of Health Informatics and Public Health, Tohoku University School of Public Health, Graduate School of Medicine, Sendai,Japan.


OBJECTIVE In this paper, the authors set out to identify the angiographic features of moyamoya disease with posterior hemorrhage, which is a strong predictor of rebleeding. METHODS This cross-sectional study used the data set of the Japan Adult Moyamoya Trial (clinical trial registration no.: C000000166 [ ]). The panel designed the ancillary measurement of angiography at onset, classifying the collateral vessels into 3 subtypes: lenticulostriate anastomosis, thalamic anastomosis, and choroidal anastomosis. The association between each collateral and the hemorrhage site (anterior vs posterior) was assessed in the hemorrhagic hemisphere by using multivariate adjustment for potential confounders, including age, sex, and involvement of the posterior cerebral artery (PCA). The association was confirmed through topographical analysis of bleeding points. RESULTS Among the 80 participants, 75 hemorrhagic hemispheres of 75 patients were analyzed. Lenticulostriate anastomosis was detected in 21 (28.0%) hemorrhagic hemispheres, thalamic anastomosis in 22 (29.3%), and choroidal anastomosis in 35 (46.7%). Choroidal anastomosis was a factor associated with posterior hemorrhage (OR 2.77 [95% CI 1.08-7.10], p = 0.034) and remained statistically significant after the multivariate adjustment (OR 2.66 [95% CI 1.00-7.07], p = 0.049). PCA involvement was also associated with posterior hemorrhage in both univariate and multivariate analyses. Topographical analysis revealed good correspondence between bleeding points associated with positive choroidal anastomosis and the anatomical distribution of the choroidal arteries, including the thalamus and the wall of the atrium. CONCLUSIONS Choroidal anastomosis and PCA involvement are characteristic of posterior hemorrhage in moyamoya disease. Choroidal anastomosis might be considered a potential source of posterior hemorrhage at high risk of rebleeding.


CI = confidence interval; JAM = Japan Adult Moyamoya; OR = odds ratio; PCA = posterior cerebral artery; bypass surgery; cerebral angiography; intracerebral hemorrhage; moyamoya disease; vascular disorders


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