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

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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.


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.


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.


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.

ABBREVIATIONS CI = confidence interval; JAM = Japan Adult Moyamoya; OR = odds ratio; PCA = posterior cerebral artery.

Article Information

Correspondence Susumu Miyamoto, Department of Neurosurgery, Graduate School of Medicine, Kyoto University, 54 Shogoin Kawahara-cho, Sakyo-ku, Kyoto 606-8507, Japan. email:

INCLUDE WHEN CITING Published online April 14, 2017; DOI: 10.3171/2016.11.JNS161650.

Disclosures The authors report no conflict of interest concerning the materials or methods used in this study or the findings specified in this paper.

© AANS, except where prohibited by US copyright law.



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    Schematic illustration showing angiographic definition of lenticulostriate (A), thalamic (B; dotted lines represent the medial posterior choroidal artery), and choroidal (C) anastomoses. The gray area indicates the ventricle. *Includes collaterals from the posterior choroidal artery. The panels to the left of the dashed vertical line are representative of a carotid artery angiogram, and those to the right of this line are representative of a vertebral artery angiogram. a. = artery; ChA = choroidal artery; ICA = internal carotid artery; LSA = lenticulostriate artery; MedA = medullary artery; MPchA = medial posterior choroidal artery; PCA = posterior cerebral artery; PcomA = posterior communicating artery; TPA = thalamoperforating artery; TTA = thalamotuberal artery; VA = vertebral artery.

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    Typical angiographic findings of lenticulostriate (A), thalamic (B and C), and choroidal (D) anastomoses. Anteroposterior and lateral views are shown in the upper row and lower row, respectively. The origins of thalamic anastomoses include the posterior communicating (B) and posterior cerebral (C) arteries. The perforating or choroidal arteries are indicated by arrows; the medullary arteries are indicated by arrowheads.

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    Flow diagram for inclusion.

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    Graphic display of univariate ORs for posterior hemorrhage.

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    Topographical analysis showing the relationship between bleeding points (gray dots) and collaterals. Black dots represent each collateral detected. For ease of recognition, all bleeding points are presented as on the left hemisphere. Gray shading indicates the basal ganglia and thalamus.

  • View in gallery

    Schematic illustration showing the conceptual relationship between collaterals and hemorrhage locations.



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