Background
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.
Methods
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.
Results
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%).
Conclusions
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.
Key Words
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References
- Cerebrovascular “moyamoya” disease. Disease showing abnormal net-like vessels in base of brain.Arch Neurol. 1969; 20: 288-299
- Asymptomatic microbleeds in moyamoya disease: T2*-weighted gradient-echo magnetic resonance imaging study.J Neurosurgery. 2005; 102: 470-475
- Histological analysis of microbleed after surgical resection in a patient with moyamoya disease.Neurol Med Chir. 2007; 47: 564-567
- The presence of multiple microbleeds as a predictor of subsequent cerebral hemorrhage in patients with moyamoya disease.Neurosurgery. 2008; 62 (discussion 111-102): 104-111
- Prevalence of asymptomatic microbleeds in patients with moyamoya disease.Neurol Med Chir. 2005; 45 (discussion 500): 495-500
- Incidence, locations, and longitudinal course of silent microbleeds in moyamoya disease: a prospective t2*-weighted MRI study.Stroke. 2013; 44: 516-518
- Microbleeds in moyamoya disease: susceptibility-weighted imaging versus T2*-weighted imaging at 3 Tesla.Invest Radiol. 2008; 43: 574-579
- Guidelines for the diagnosis and treatment of spontaneous occlusion of the Circle of Willis ('moyamoya' disease). Research committee on spontaneous occlusion of the Circle of Willis (moyamoya disease) of the ministry of health and welfare, Japan.Clin Neurol Neurosurgery. 1997; 99: S238-S240
- The Microbleed Anatomical Rating Scale (MARS): reliability of a tool to map brain microbleeds.Neurology. 2009; 73: 1759-1766
- Novel magnetic resonance angiography stage grading for moyamoya disease.Cerebrovasc Dis (Basel, Switzerland). 2005; 20: 347-354
- Histopathologic analysis of foci of signal loss on gradient-echo T2*-weighted MR images in patients with spontaneous intracerebral hemorrhage: evidence of microangiopathy-related microbleeds.AJNR Am J Neuroradiol. 1999; 20: 637-642
- Cerebral microbleeds: histopathological correlation of neuroimaging.Cerebrovasc Dis (Basel, Switzerland). 2011; 32: 528-534
- Cerebral microbleeds predict impending intracranial hemorrhage in infective endocarditis.Cerebrovasc Dis (Basel, Switzerland). 2011; 32: 483-488
- Infective endocarditis with symptomatic cerebral complications: contribution of cerebral magnetic resonance imaging.Cerebrovasc Dis (Basel, Switzerland). 2013; 35: 327-336
- Hematoma expansion following acute intracerebral hemorrhage.Cerebrovasc Dis (Basel, Switzerland). 2013; 35: 195-201
- Cerebrovascular disease: new data on surgical therapy for pediatric moyamoya disease.Nat Rev Neurol. 2010; 6: 242-243
- Moyamoya disease with repeated intraventricular hemorrhage due to aneurysm rupture. Report of two cases.J Neurosurgery. 1994; 80: 328-331
- A source of haemorrhage in adult patients with moyamoya disease: the significance of tributaries from the choroidal artery.Acta Neurochir. 1996; 138: 1282-1286
- Effects of surgical revascularization on peripheral artery aneurysms in moyamoya disease: report of three cases.Neurosurgery. 2001; 49 (discussion 467-468): 463-467
- Long-term natural history of hemorrhagic moyamoya disease in 42 patients.J Neurosurg. 2000; 93: 976-980
- Microvasculature of the human cerebral white matter: Arteries of the deep white matter.Neuropathology. 2003; 23: 111-118
- Features of the cerebral vascular pattern that predict vulnerability to perfusion or oxygenation deficiency: an anatomic study.AJNR Am J Neuroradiol. 1990; 11: 431-439
- Computed tomography of cerebral infarction along the distribution of the basal perforating arteries. Part ii: thalamic arterial group.Radiology. 1985; 155: 119-130
- Computed tomography of cerebral infarction along the distribution of the basal perforating arteries. Part i: striate arterial group.Radiology. 1985; 155: 107-118
- Changing ischaemic lesion patterns in adult moyamoya disease.J Neurol Neurosurgery Psychiatry. 2009; 80: 36-40
- Microanatomy of the subependymal arteries of the lateral ventricle.Surg Neurol. 2005; 63 (discussion 458): 451-458
- Histopathological studies on spontaneous occlusion of the Circle of Willis (cerebrovascular moyamoya disease).Clin Neurol Neurosurgery. 1997; 99: S203-S208
- The human periventricular arterial blood supply and the anatomy of cerebral infarctions.Eur Neurol. 1971; 5: 321-334
- Dyke award. The search for human telencephalic ventriculofugal arteries.AJNR Am J Neuroradiol. 1991; 12: 215-222
- The ventriculofugal arteries.AJNR Am J Neuroradiol. 1992; 13: 413-415
- Improving interrater agreement about brain microbleeds: development of the brain observer microbleed scale (bombs).Stroke. 2009; 40: 94-99
- Cerebral microbleeds: a guide to detection and interpretation.Lancet Neurol. 2009; 8: 165-174
Article info
Publication history
Published online: February 19, 2014
Accepted:
December 3,
2013
Received in revised form:
October 10,
2013
Received:
July 22,
2013
Footnotes
Funding: No grants or funding sources are pertinent to this article.
Conflicts of interest: None.
Identification
DOI: https://doi.org/10.1016/j.jstrokecerebrovasdis.2013.12.007
Copyright
© 2014 National Stroke Association. Published by Elsevier Inc. All rights reserved.