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).

Purpose

To investigate the incidence, distribution patterns, and influencing factors of asymptomatic CMBs in patients with moyamoya disease.

Material and 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.

Conclusion

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.

Keywords

Moyamoya disease cerebral microbleeds phase-sensitive imaging (PSI)susceptibility-weighted imaging (SWI)T2*-weighted imaging (T2*WI)

Get full access to this article

View all access options for this article.

References

Suzuki

Takaku

. Cerebrovascular “moyamoya” disease: disease showing abnormal net-like vessels in base of brain. Arch Neurol 1969; 20: 288–299.

Suzuki

Kodama

. Moyamoya disease: a review. Stroke 1983; 14: 104–109.

Takahashi

. Magnification angiography in moyamoya disease: new observations on collateral vessels. Radiology 1980; 136: 379–386.

Scott

Smith

. Moyamoya disease and moyamoya syndrome. N Engl J Med 2009; 360: 1226–1237.

Wakai

Tamakoshi

Ikezaki

. Epidemiological features of moyamoya disease in Japan: findings from a nationwide survey. Clin Neurol Neurosurg 1997; 99: 221–228.

Nishimoto

. Moyamoya disease. Neurol Med Chir (Tokyo) 1979; 19: 221–228.

Duan

Bao

Yang

. Moyamoya disease in China: its clinical features and outcomes. Stroke 2012; 43: 56–60.

Kikuta

Takagi

Nozaki

. Asymptomatic microbleeds in moyamoya disease: T2*-weighted gradient-echo magnetic resonance imaging study. J Neurosurg 2005; 102: 470–475.

Kikuta

Takagi

Nozaki

. The presence of multiple microbleeds as a predictor of subsequent cerebral hemorrhage in patients with moyamoya disease. Neurosurgery 2008; 62: 104–111.

10.

Ikezaki

Fukui

Inamura

. The current status of the treatment for hemorrhagic type moyamoya disease based on a 1995 nationwide survey in Japan. Clin Neurol Neurosurg 1997; 99: S183–S186.

11.

Takahashi

Miyamoto

. Moyamoya disease: recent progress and outlook. Neurol Med Chir (Tokyo) 2010; 50: 824–832.

12.

Ishikawa

Kuroda

Nakayama

. Prevalence of asymptomatic microbleeds in patients with moyamoya disease. Neurol Med Chir (Tokyo) 2005; 45: 495–500.

13.

Nandigam

Viswanathan

Deigado

. MR imaging detection of cerebral microbleeds: effect of susceptibility-weighted imaging, section thickness, and field strength. Am J Neuroradiol 2009; 30: 338–343.

14.

Goos

van der Flier

Knol

. Clinical relevance of improved microbleed detection by susceptibility-weighted magnetic resonance imaging. Stroke 2011; 42: 1894–1900.

15.

Mori

Miki

Kikuta

. Microbleeds in moyamoya disease: susceptibility-weighted imaging versus T2*-weighted imaging at 3 Tesla. Invest Radiol 2008; 43: 574–579.

16.

Fujii

Kanasaki

Matsusue

. Demonstration of cerebral venous variations in the region of the third ventricle on phase-sensitive imaging. Am J Neuroradiol 2010; 31: 55–59.

17.

Kikuta

Takagi

Nozaki

. Histological analysis of microbleed after surgical resection in a patient with moyaomya disease. Neurol Med Chir (Tokyo) 2007; 47: 564–567.

18.

Gregoire

Chaudhary

Brown

. The microbleed anatomical rating scale (MARS): reliability of a tool to map brain microbleeds. Neurology 2009; 73: 1759–1766.

19.

Moher

Liberati

Tetzlaff

. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. J Clin Epidemiol 2009; 62: 1006–1012.

20.

Kikuta

. Experiences using 3-tesla magnetic resonance imaging in the treatment of Moyamoya disease. Acta Neurochir Suppl 2008; 103: 123–126.

21.

Kuroda

Kashiwazaki

Ishikawa

. Incidence, locations, and longitudinal course of silent microbleeds in moyamoya disease: A prospective T2*-weighted MRI study. Stroke 2013; 44: 516–518.

22.

Chabriat

Bousser

. CADASIL. Cerebral autosomal dominant arteriopathy with subcortical infarcts and leukoencephalopathy. Adv Neuro 2003; l92: 147–150.

23.

Greenberg

Finklestein

Schaefer

. Petechial hemorrhages accompanying lobar hemorrhage: detection by gradient-echo MRI. Neurology 1996; 46: 1751–1754.

24.

Greenberg

O’Donnell

Schaefer

. MRI detection of new hemorrhages: potential marker of progression in cerebral amyloid angiopathy. Neurology 1999; 53: 1135–1138.

25.

Knudsen

Rosand

Karluk

. Clinical diagnosis of cerebral amyloid angiopathy: validation of the Boston criteria. Neurology 2001; 56: 537–539.

26.

Rosand

Muzikansky

Kumar

. Spatial clustering of hemorrhages in probable cerebral amyloid angiopathy. Ann Neurol 2005; 58: 459–462.

27.

Lee

Bae

Kwon

. Cerebral microbleeds are regionally associated with intracerebral hemorrhage. Neurology 2004; 62: 72–76.

28.

Ryan

Chowdhary

Britz

. Hemorrhage and risk of further hemorrhagic strokes following cerebral revascularization in Moyamoya disease: A review of the literature. Surg Neurol Int 2012; 3: 72–72.

29.

Yamashita

Oka

Tanaka

. Histopathology of the brain vascular network in moyamoya disease. Stroke 1983; 14: 50–58.

30.

Morioka

Hamada

Kawano

. Angiographic dilatation and branch extension of the anterior choroidal and posterior communicating arteries are predictors of hemorrhage in adult moyamoya patients. Stroke 2003; 34: 90–95.

31.

Ezura

Yoshimoto

Fujiwara

. Clinical and angiographic follow-up of childhood-onset moyamoya disease. Childs Nerv Syst 1995; 11: 591–594.

32.

Yoshida

Yoshimoto

Shirane

. Clinical course, surgical treatment, and long-term outcome of moyamoya patients with rebleeding after an episode of intracerebral hemorrhage: an extensive follow-up study. Stroke 1999; 30: 2272–2276.

33.

Kobayashi

Saeki

Oishi

. Long-term natural history of hemorrhagic moyamoya disease in 42 patients. J Neurosurg 2000; 93: 976–980.

34.

Fan

Zhang

Lam

. Cerebral microbleeds as a risk factor for subsequent intracerebral hemorrhages among patients with acute ischemic stroke. Stroke 2003; 34: 2459–2462.