Effect of choroidal collateral vessels on de novo hemorrhage in moyamoya disease: analysis of nonhemorrhagic hemispheres in the Japan Adult Moyamoya Trial

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OBJECTIVE

Following hemorrhagic stroke in moyamoya disease, de novo intracranial hemorrhage can occur in the previously unaffected nonhemorrhagic hemisphere. In the present analysis the authors intended to determine whether the presence in the nonhemorrhagic hemisphere of choroidal collateral vessels, which have been the focus of attention as a source of bleeding, affects the risk of de novo hemorrhage.

METHODS

The subject of focus of the present cohort study was the nonhemorrhagic hemispheres of adult patients with hemorrhagic moyamoya disease enrolled in the Japan Adult Moyamoya Trial and allocated to the nonsurgical arm. The variable of interest was the presence of choroidal collaterals (also termed choroidal anastomoses), identified with baseline angiography and represented by a connection (anastomosis) between the anterior or posterior choroidal arteries and the medullary arteries. The outcome measure was de novo hemorrhage during the 5-year follow-up period, assessed in all nonhemorrhagic hemispheres. The incidence of de novo hemorrhage in the collateral-positive and -negative groups was compared.

RESULTS

Choroidal collaterals were present in 15 of 36 (41.7%) nonhemorrhagic hemispheres analyzed. The overall annual risk of de novo hemorrhage was 2.0%. Three de novo hemorrhages occurred in the collateral-positive group, whereas no hemorrhage occurred in the collateral-negative group. The annual risk of de novo hemorrhage was significantly higher in the collateral-positive group than in the collateral-negative group (5.8% per year vs 0% per year; p = 0.017). All hemorrhage sites corresponded to the distribution of choroidal collaterals.

CONCLUSIONS

The present preliminary results suggest that the presence of choroidal collaterals affects the risk of de novo hemorrhage in the nonhemorrhagic hemisphere, subject to verification in larger studies. Further studies are needed to determine the optimal treatment strategy for nonhemorrhagic hemispheres and asymptomatic patients.

ABBREVIATIONS JAM = Japan Adult Moyamoya; PCA = posterior cerebral artery; TIA = transient ischemic attack.

Article Information

Correspondence Susumu Miyamoto: Kyoto University, Kyoto, Japan. miy@kuhp.kyoto-u.ac.jp.

INCLUDE WHEN CITING Published online February 8, 2019; DOI: 10.3171/2018.10.JNS181139.

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.

Headings

Figures

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    A 37-year-old woman treated conservatively and suffering de novo hemorrhage in the nonhemorrhagic hemisphere. A: CT image at enrollment revealing hemorrhage in the left periventricular area of the posterior part of the lateral ventricle. B: CT image obtained 3.5 years after enrollment revealing de novo hemorrhage in the nonhemorrhagic hemisphere (right hemisphere). The de novo hemorrhage is located in the right periventricular area of the posterior part of the lateral ventricle, corresponding to the distribution of the choroidal anastomosis. C and D: Anterior-posterior (C) and lateral (D) views of baseline right internal carotid angiography showing the typical finding of choroidal anastomosis, extreme dilation, and extension of the anterior choroidal artery with sudden deviation from the shape of the lateral ventricle at its peripheral portion (arrows).

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    A 54-year-old woman treated conservatively and suffering de novo hemorrhage in the nonhemorrhagic hemisphere. A: CT image at enrollment revealing hemorrhage in the right thalamus. B: CT image obtained 3.3 years after enrollment revealing de novo hemorrhage in the nonhemorrhagic hemisphere (left hemisphere). The de novo hemorrhage is located in the left periventricular area of the atrium of the lateral ventricle, corresponding to the distribution of the choroidal anastomosis. C and D: Anterior-posterior (C) and lateral (D) views of baseline left common carotid angiography showing extreme dilation and extension of the anterior choroidal artery with sudden deviation from the shape of the lateral ventricle at its peripheral portion (arrows), suggesting a positive finding of choroidal anastomosis.

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    A 43-year-old woman treated conservatively and suffering de novo hemorrhage in the nonhemorrhagic hemisphere. A: CT image at enrollment revealing hemorrhage in the left occipital area. B: CT image obtained 1.7 years after enrollment revealing de novo hemorrhage in the nonhemorrhagic hemisphere (right hemisphere). The de novo hemorrhage extends from the right periventricular area of the posterior part of the lateral ventricle, corresponding to the distribution of the choroidal anastomosis. C and D: Anterior-posterior (C) and lateral (D) views of baseline right internal carotid angiography showing extreme dilation and extension of the anterior choroidal artery with sudden deviation from the shape of the lateral ventricle at its peripheral portion (arrows), suggesting a positive finding of choroidal anastomosis.

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    Flow diagram for study inclusion.

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    Kaplan-Meier curve for de novo hemorrhage in all nonhemorrhagic hemispheres treated conservatively. Censored subjects are indicated by tick marks.

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    Kaplan-Meier curves for de novo hemorrhage in the choroidal-anastomosis-positive and -negative nonhemorrhagic hemispheres treated conservatively. Censored subjects are indicated by tick marks.

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    Supplementary analysis: Kaplan-Meier curves for de novo hemorrhage with the choroidal-anastomosis-positive nonhemorrhagic hemispheres treated surgically and conservatively (n = 25). Censored subjects are indicated by tick marks.

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