Adult moyamoya disease (MMD) is known to have high incidence of cerebral microbleeds (cMBs); however, the clinical significance still remains unclear. We investigated the frequency of cMBs in a large number of patients and analyzed the patterns of MB distribution in association with the location of the hematoma and moyamoya vessels.
We studied 259 consecutive patients with MMD using prospectively collected database. One hundred ninety-one patients were eligible for the present study, and image analysis was performed retrospectively. The presence of cMBs and remains of hemorrhage were determined using gradient-echo T2*-weighted sequence (1.5 T). The development of moyamoya vessels was assessed on source images of time-of-flight magnetic resonance angiography. The analysis consists of descriptive assessment of the spatial relationship between cMB, remains of hemorrhage, and moyamoya vessels. Statistical analysis was performed to calculate relative risk ratio in the presence of cMBs in relation to the remains of hemorrhage (macrohematoma), age of onset, and the presence of concomitant moyamoya vessels.
Thirty MBs were observed in 20 adult MMD patients (16.9%). MBs were located predominantly in the periventricular white matter (63.3%) followed by the basal ganglia/thalami (20%). Comparing the patients with cMBs from those without, hematoma was more frequently observed in patients with cMBs (odds ratio [OR] 4.29; 95% confidence interval [CI] 1.58-11.62; P = .0062). Patients with adult onset was more likely to demonstrate cMBs (14.4%) compared with the patients with pediatric onset (4.1%) (OR 3.93; 95% CI 1.11-13.91). Moyamoya vessels appeared in the lateral part of the trigon, and the periventricular white matter was significantly associated with the presence of cMBs (lateral part of the trigon; OR 3.29 [1.59-6.82], P = .0019, periventricle of the body of lateral ventricle; OR 2.40 [1.20-4.79], P = .0214, respectively). cMBs accompanied concomitant arteries in 23 (76.7%) lesions. The subependymal–leptomeningeal artery anastomosis was the most common pattern (n = 20, 66.7%).
Spatial relationship was demonstrated between the moyamoya vessels and perivascular hemosiderin deposition particularly around the subependymal–leptomeningeal anastomosis, suggesting the mechanism for the development of cMBs in MMD. Present study further supports previous findings that cMBs potentially serve as a marker for the bleeding-prone microangiopathy in MMD. The significance of the present study lies in selecting optimal surgical candidate for preventing future hemorrhage by the presence of the cMBs, whereas current surgical indication relying on the degree of ischemia frequently fails to detect patients with future hemorrhage.
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Published online: February 19, 2014
Accepted: December 3, 2013
Received in revised form: October 10, 2013
Received: July 22, 2013
Funding: No grants or funding sources are pertinent to this article.
Conflicts of interest: None.
© 2014 National Stroke Association. Published by Elsevier Inc. All rights reserved.