Predictors of neoangiogenesis after indirect revascularization in moyamoya disease: a multicenter retrospective study

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  • Department of Neurosurgery, Beijing Tiantan Hospital, Capital Medical University, 6th Tiantanxili, Beijing, China
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OBJECTIVE

The effect of indirect revascularization to improve cerebral perfusion for moyamoya disease (MMD) is based on ingrowth of new vessels into the cortical brain. Preoperative indicators for neoangiogenesis would be helpful to the selection of appropriate procedures for MMD patients but have not yet been investigated. Our study aimed to identify potential predictors for neovascularization after indirect bypass surgery.

METHODS

The authors reviewed consecutive cases with complete clinical and radiological documentation of patients who had undergone surgery between December 2010 and January 2018. Patients who were treated with indirect bypass surgery were included. Cerebrovascular characteristics were evaluated by catheter angiography. Neoangiogenesis after indirect bypass was determined as “good” or “poor” based on the Matsushima standard. Univariate and multivariate analyses were performed to identify predictors for neoangiogenesis after indirect bypass. Subgroup analyses by onset type and surgical type were carried out to identify specific predictors for different populations.

RESULTS

In total, 231 hemispheres of 209 patients (mean ± SD age 23.06 ± 15.09 years, range 3–61 years) were retrospectively included. In 146 (63.2%) hemispheres, good neoangiogenesis was observed after indirect revascularization. Multivariate analysis showed that the status of ICA moyamoya vessels (p < 0.001, OR [95% CI] 3.242 [2.007–5.236]) is a predictor of favorable neoangiogenesis after indirect bypass surgery, whereas hemorrhagic onset (p < 0.001, OR [95% CI] 0.138 [0.054–0.353]) is a risk factor for poor neoangiogenesis. In addition, younger age was significantly associated with good neovascularization in patients with hemorrhagic onset (p = 0.027, OR [95% CI] 0.893 [0.808–0.987]), whereas age was not a significant predictor for neovascularization in non–hemorrhagic-onset patients (p = 0.955). Hemispheres with good revascularization had lower incidence of rebleeding, lower modified Rankin Scale scores, and more improvement of symptoms during long-term follow-up (p = 0.026, 0.006, and 0.013, respectively).

CONCLUSIONS

Hemorrhagic onset predicts poor neovascularization after indirect bypass surgery for MMD patients. Abundant ICA moyamoya vessels indicate good neoangiogenesis after indirect bypass and vice versa, whereas absent ICA moyamoya vessels predict poor revascularization. Good neovascularization was associated with better long-term outcome. Future studies are needed to further address this issue and clarify the underlying pathophysiological mechanisms.

ABBREVIATIONS ACA = anterior cerebral artery; DSA = digital subtraction angiography; EC-IC = extracranial-intracranial; EDAS = encephaloduroarteriosynangiosis; EDGS = encephalodurogaleo(periosteal)synangiosis; ICA = internal carotid artery; MBH = multiple burr hole; MD = moyamoya disease; mRS = modified Rankin Scale; OphA = ophthalmic artery; PCA = posterior cerebral artery; STA = superficial temporal artery; TIA = transient ischemic attack.

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Contributor Notes

Correspondence Yuanli Zhao: Beijing Tiantan Hospital, Capital Medical University, Beijing, China. zhaoyuanli@126.com.

INCLUDE WHEN CITING Published online January 25, 2019; DOI: 10.3171/2018.9.JNS181562.

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

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