title: High incidence of asymptomatic cerebral microbleeds in patients with hemorrhagic onset-type moyamoya disease: a phase-sensitive MRI study and meta-analysis.
abstract: BACKGROUND
  Moyamoya disease is a relatively rare cerebrovascular occlusive disorder. Several studies have reported cerebral microbleeds (CMBs) in moyamoya disease patients using T2*-weighted imaging (T2*WI) and/or susceptibility-weighted imaging (SWI).
  
  
  OBJECTIVE
  To investigate the incidence, distribution patterns, and influencing factors of asymptomatic CMBs in patients with moyamoya disease.
  
  
  METHODS
  Phase-sensitive imaging (PSI) was used to investigate 27 consecutive moyamoya disease patients with a 3-T magnetic resonance imaging system, then a meta-analysis of 245 patients (asymptomatic moyamoya disease, n = 23; ischemic moyamoya disease, n = 161; hemorrhagic moyamoya disease, n = 61) from four previous individual studies and our PSI study was performed. The meta-analysis was performed in accordance with the Preferred Reporting Items for Systematic reviews and Meta-Analyses (PRISMA) guidelines. Based on the clinical and radiological data, we divided the studies into different model groups to calculate the incidence of CMBs and discuss the distribution patterns of CMBs.
  
  
  RESULTS
  Thirty-five asymptomatic CMBs were demonstrated in 14 moyamoya disease patients (51.9%) in our PSI study. Of these, 45.7% were located in the periventricular white matter. In the meta-analysis, the pooled incidence of asymptomatic CMBs in moyamoya disease was 46% (95% confidence interval [CI], 28.2-63.8%) on SWI or PSI and 29.6% (95% CI, 17.4-41.7%) on T2*WI. Statistical analysis showed that PSI or SWI offered better detection of CMBs in moyamoya disease than T2*WI, and 3-T T2*WI offered better detection than 1.5-T T2*WI. Furthermore, hemorrhagic onset-type moyamoya disease correlated with a high incidence of asymptomatic CMBs.
  
  
  CONCLUSIONS
  PSI or SWI can detect CMBs better than T2*WI, and 3-T T2*WI. Hemorrhagic onset-type moyamoya disease seems to correlate with a high incidence of asymptomatic CMBs. The meta-analysis indicates that asymptomatic CMBs may be an important factor for hemorrhagic stroke risk. Long-term evaluation of CMBs using PSI or SWI may contribute to the management of moyamoya disease.
authors.affiliation: Division of Radiology, Department of Pathophysiological Therapeutic Science, Tottori University, Yonago, Japan.
authors.forename: Ying
authors.initials: Y
authors.lastname: Qin
authors.affiliation: Division of Radiology, Department of Pathophysiological Therapeutic Science, Tottori University, Yonago, Japan ogawa@med.tottori-u.ac.jp.
authors.forename: Toshihide
authors.initials: T
authors.lastname: Ogawa
authors.affiliation: Division of Radiology, Department of Pathophysiological Therapeutic Science, Tottori University, Yonago, Japan.
authors.forename: Shinya
authors.initials: S
authors.lastname: Fujii
authors.affiliation: Division of Radiology, Department of Pathophysiological Therapeutic Science, Tottori University, Yonago, Japan.
authors.forename: Yuki
authors.initials: Y
authors.lastname: Shinohara
authors.affiliation: Division of Radiology, Department of Pathophysiological Therapeutic Science, Tottori University, Yonago, Japan.
authors.forename: Shin-Ichiro
authors.initials: S
authors.lastname: Kitao
authors.affiliation: Division of Radiology, Department of Pathophysiological Therapeutic Science, Tottori University, Yonago, Japan.
authors.forename: Fuminori
authors.initials: F
authors.lastname: Miyoshi
authors.affiliation: Division of Radiology, Department of Pathophysiological Therapeutic Science, Tottori University, Yonago, Japan.
authors.forename: Marie
authors.initials: M
authors.lastname: Takasugi
authors.affiliation: Department of Neurological Sciences, Division of Neurosurgery, Faculty of Medicine, Tottori University, Yonago, Japan.
authors.forename: Takashi
authors.initials: T
authors.lastname: Watanabe
authors.affiliation: Division of Radiology, Department of Pathophysiological Therapeutic Science, Tottori University, Yonago, Japan.
authors.forename: Toshio
authors.initials: T
authors.lastname: Kaminou
mesh_terms: D000293:Adolescent; D000328:Adult; D000368:Aged; D001921:Brain / Q000098:blood supply / Q000473:pathology; D002543:Cerebral Hemorrhage / Q000453:epidemiology* / Q000473:pathology*; D002648:Child; D015897:Comorbidity; D005260:Female; D006801:Humans; D015994:Incidence; D008279:Magnetic Resonance Imaging / Q000379:methods*; D008297:Male; D008833:Microcirculation; D008875:Middle Aged; D009072:Moyamoya Disease / Q000453:epidemiology* / Q000473:pathology*; D012307:Risk Factors; D055815:Young Adult
keywords: Moyamoya disease; T2*-weighted imaging (T2*WI); cerebral microbleeds; phase-sensitive imaging (PSI); susceptibility-weighted imaging (SWI)