Intrinsic development of choroidal and thalamic collaterals in hemorrhagic-onset moyamoya disease: case-control study of the Japan Adult Moyamoya Trial

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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.


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’s angiographic staging between each group.


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 (< 0.001), as indicated by grade 2 in each subtype, compared with ischemic-onset patients. Suzuki’s angiographic staging was significantly higher in the hemorrhagic group (< 0.038). There was no difference in the extent of lenticulostriate anastomosis and PCA involvement between the groups.


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.

Clinical trial registration no. C000000166 (

ABBREVIATIONS EC-IC = extracranial-intracranial; ICA = internal carotid artery; JAM = Japan Adult Moyamoya; MMD = moyamoya disease; PCA = posterior cerebral artery.

Article Information

Correspondence Miki Fujimura: Tohoku University Graduate School of Medicine, Sendai, Japan.

INCLUDE WHEN CITING Published online May 4, 2018; DOI: 10.3171/2017.11.JNS171990.

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

© AANS, except where prohibited by US copyright law.



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    Angiographic findings of representative cases of each onset type. A and B: A 49-year-old man with hemorrhage. A carotid artery angiogram indicated a dilated choroidal artery extending beyond the lateral ventricle (asterisks in A and B). The thalamic perforators are also dilated and extended (arrows in A and B). C and D: A 28-year-old woman presenting with a transient ischemic attack. A carotid artery angiogram demonstrated lenticulostriate arteries extending beyond the level of the pericallosal artery (arrows in C and D). The choroidal artery was dilated, but its extension was below the level of the lateral ventricle (asterisk in D).

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    The prevalence of high angiographic score (grade 2) according to each collateral pattern. Statistical significance was determined by chi-square test. Figure is available in color online only.



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