“Brush Sign” on Susceptibility-Weighted MR Imaging Indicates the Severity of Moyamoya Disease

Discussion

This is the first report showing characteristics of the DMV in MMD by using SWI techniques. Susceptibility-weighted MR imaging is a high spatial resolution 3D gradient-echo MR imaging technique with phase postprocessing that accentuates the paramagnetic properties of blood products such as deoxyhemoglobin, intracellular methemoglobin, and hemosiderin.¹⁰ This technique can show prominent hypointense signals in the draining veins within areas of impaired perfusion. Uncoupling between oxygen supply and demand in hypoperfused tissue may cause a relative increase of deoxyhemoglobin levels and a decrease of oxyhemoglobin in the tissue capillaries and the draining veins. Therefore, SWI has been applied to various pathologies of the brain that affect magnetic inhomogeneity, such as stroke,^8,11 trauma,⁸ cerebral cavernous malformation,^12,13 arteriovenous malformation,¹⁴ dural arteriovenous fistula,¹⁵ pathophysiology affecting iron storage conditions,^16–18 brain tumor,¹⁹ and cerebral amyloid angiopathy.²⁰ It is noteworthy that this method has the potential to demonstrate increased oxygen extraction in focal cerebral ischemia.⁸

In MMD, increased conspicuity of DMVs was found in patients with TIA and infarct, implying that impaired perfusion occurred in the deep white matter. This result supports the specification that conspicuous DMVs indicate increased oxygen extraction or venous stasis, and this indicates a part of misery perfusion in this area.^8,21 Susceptibility-weighted MR imaging shows prominent hypointense signals in the draining veins within areas of impaired perfusion. Therefore, this would account for the increased visibility of veins in these regions, making it valuable to anticipate the extent of impaired perfusion in MMD without contrast-enhanced CT or MR imaging, SPECT, or PET. Alternatively, DSC-weighted bolus tracking MR imaging and ASL are the latest additions to the growing number of techniques available for quantitative hemodynamic analysis.⁵ ASL is becoming more clinically relevant for evaluating CBF because this method has other advantages, including lack of radiation, lack of intravenous contrast agent, and the ability to repeat the study. In terms of MMD, however, the delayed arterial times through collateral pathways can cause a significant underestimation of CBF as well as errors due to labeling agent that remains in the feeding vessels rather than being extracted into the brain parenchyma.⁴ Moreover, patients with MMD are in a chronic state of cerebral vasodilation and have a reduced or absent CVR. Therefore, CVR is also a valuable hemodynamic indicator in MMD, though there have been no MR imaging techniques reported for the assessment of CVR so far. Here, we first show SWI could correlate with hemodynamics in SPECT, especially CVR.

Another interesting finding in this study is that SWI stage and CBF and CVR were not so impaired in patients presenting with hemorrhage compared with those presenting with TIA or infarct. Intracranial hemorrhage is a common in feature in adult patients with MMDs with a mortality rate of approximately 20%, and it is the largest risk factor contributing to the poor prognosis with this entity.^22,23 Hemodynamic stress to the Moyamoya vessels has been suggested as a cause for the hemorrhagic presentation, and some reports showed Moyamoya vessels and aneurysms associated with MMD resolved after bypass surgery.^24,25 The prophylactic effect of bypass surgery against cerebral hemorrhage remains uncertain, and this issue will be clarified by a prospective, randomized trial in Japan (Japan Adult Moyamoya Trial). Here, we showed severe hemodynamic compromise was not obvious in the hemorrhagic group. Although there is less consensus regarding the hemodynamic findings in hemorrhagic MMD, some supportive reports have so far shown that CBF in MMD is not significantly lower in any presentations and that there is a significant difference in CBV and OEF between the patients with ischemia and hemorrhage, with a higher CBV and increased OEF (lower CVR) in the ischemic group.^26,27 Moreover, the disturbances in cerebral hemodynamics are usually less prominent in adults with MMD than in pediatric patients.^28,29 Together, this suggests that hemodynamic impairment does not always contribute to the hemorrhagic presentation, which is common in adults.

The SWI technique also can detect MBs, reported to be a predictor for hemorrhage in MMD.³⁰ MBs were detected in 18.8% (3 in hemorrhage groups and 3 in TIA groups) in our series. The incidence of MBs is reported as 14.8%–42%, depending on MR imaging quality such as 1.5T versus 3T or T2* versus SWI technique.^31–33 The significance of MBs in patients with an ischemic presentation is still controversial. Kikuta et al³² reported MBs occurred with equal probability regardless of the MMD onset type (44% in hemorrhage versus 43% in ischemia). In contrast, Ishikawa et al³³ reported that patients with hemorrhage had more MBs than those with ischemia (33.3% in hemorrhage versus 11.1% in ischemia). Initially, the characteristic clinical feature of MMD suggests that a patient could have both ischemic and hemorrhagic stroke, and 13% of patients with MMD with hemorrhage have experienced ischemic attacks before admission.³⁴ Further study is necessary to determine whether MBs are specific for a hemorrhagic presentation.

Several limitations in this study should be addressed. First, this study was performed as a preoperative study and did not interpret SWI data for decision making for revascularization surgery. Second, we could not characterize the signal intensity change of the DMV on SWI after revascularization surgery. Therefore, the utility of SWI to predict whether a patient with MMD would benefit from bypass surgery is still not clear. In our institute, the main indication for revascularization surgery was symptomatic MMD and asymptomatic MMD with impaired hemodynamics (lower CBF and CVR) when evaluated by SPECT. Direct and indirect combined bypass surgery (STA-MCA anastomosis with encephalomyosynangiosis) was mainly performed for the patients with MMD, and indirect bypass surgery (encephalo-duro-arterio-synangiosis) was selected in case the STA was not developed. In this study, direct and indirect combined bypass was performed in 17 patients, indirect bypass was performed in 3 patients, and 13 patients were treated conservatively. More data should be accumulated by using SWI to address these limitations. Third, this study was not a quantitative analysis and SWI could not replace other modalities for the assessment of the cerebral hemodynamics. Nevertheless, SWI could be a simple and powerful technique to assess CVR in MMD without acetazolamide challenges.