Clinical and Radiological Outcomes After Revascularization of Hemorrhagic Moyamoya Disease

Abstract

Objective: To evaluate clinical and radiological outcomes after revascularization of hemorrhagic moyamoya disease (MMD). Materials and Methods: We retrospectively collected patients with hemorrhagic MMD who received revascularization from January 2011 to June 2018 at a high-volume stroke center. Rebleeding, ischemic stroke, modified Rankin Scale (mRS) and death after revascularization were used to evaluate long-term clinical outcome. Poor neurological outcome was defined as a mRS>2. The changes of original and revascularization collaterals were used to evaluate radiological outcome. The clinical and radiological outcomes between patients with different surgical revascularization were compared. Results: A total of 312 patients (319 hemispheres) were recruited, including 133 hemispheres (41.7%) with indirect revascularization and 186 hemispheres (58.3%) with direct revascularization. In 308 hemispheres with clinical follow-up data, Postoperative rebleeding, ischemic stroke, poor neurological outcome and death occurred in 13.0% (40/308), 2.6% (8/308), 12.0% (37/308), and 6.2% (19/308) of the hemispheres, respectively. The rates of postoperative rebleeding (8.5 vs. 19.1%, P = 0.006) and poor neurological outcome (8.5 vs. 16.8%, P = 0.026) were lower in hemispheres with direct revascularization than those with indirect revascularization. However, there was no statistically significant difference in the rates of postoperative ischemic stroke (1.1 vs. 4.6%, P = 0.129) and death (4.5 vs. 8.4%, P = 0.162) between the two groups. Multivariate logistic regression analysis indicated that the risk of postoperative rebleeding was higher in those with untreated aneurysms, repetitive bleeding episodes, normal perfusion status, and indirect revascularization (P < 0.05). In 78 hemispheres with radiological follow-up data, the regression of moyamoya vessels, anterior choroidal artery (AchA), posterior communicating artery (PcomA) and aneurysms were present in 44.9, 47.4, 25.6, and 11.5% of the hemispheres, respectively. The regression of original collaterals and establishment of revascularization collaterals were more significant in hemispheres with direct revascularization than those with indirect revascularization (P < 0.05). Conclusion: Direct revascularization may be superior to indirect revascularization for prevention of rebleeding and poor neurological outcome in adults with hemorrhagic MMD. The risk of postoperative rebleeding was higher in those with untreated aneurysms, repetitive bleeding episodes, normal perfusion status, and indirect revascularization. The regression of original collaterals and establishment of revascularization collaterals after revascularization were more significant in hemispheres with direct revascularization than those with indirect revascularization.

Keywords: intracranial hemorrhage; moyamoya disease; moyamoya syndrome; rebleeding; revascularization.

Figure 1

Study flow chart of patient selection.

Figure 2

Kaplan–Meier curves for rebleeding incidence in 308 hemorrhagic hemispheres with different revascularization surgery.

Figure 3

Two cases of hemorrhagic MMD with direct or indirect revascularization. (A–D) A 20-year-old female patient with hemorrhagic MMD, who received direct revascularization. Preoperative DSA showed dilation of AchA and PcomA (A). Postoperative DSA a year later showed significant regression of dilated AchA and PcomA (B), with substantial revascularization collaterals (C,D). She was followed-up for 56 months without rebleeding. (E–H) A 19-year-old female patient with hemorrhagic MMD, who received indirect revascularization. Preoperative DSA showed mild dilatation of AchA (E). Postoperative DSA a year later showed that the regression of dilatated AchA was not significant (F), with moderate revascularization collaterals (G,H). She was followed-up for 48 months without rebleeding.