Abstract
In clinical work, the magnetic resonance imaging markers of cerebral small vessel disease (CSVD) are frequently observed in moyamoya disease (MMD), but the clinical significance of these markers in MMD remains unclear. This study aimed to fill this gap and systematically investigate its clinical significance. In this retrospective cohort study, we screened all adult patients with MMD hospitalized from January 2016 to January 2020 and collected their baseline clinical and imaging information. Univariate and multivariate logistic regression analyses were then performed to determine which imaging markers were independently associated with MMD characteristics, including cerebrovascular morphology, cerebral hemodynamics, cerebrovascular events, and postoperative collateral formation (PCF). A total of 312 cerebral hemispheres images were collected from the 156 patients with MMD. Using multivariate logistic regression analysis, the following results were generated: (1) The presence of lacunes (OR, 2.094; 95% CI, 1.109–3.955; p = 0.023) and severe white matter hyperintensities (WMH) (OR, 3.204; 95% CI, 1.742–5.892; p < 0.001) were associated with a Suzuki stage ≥ IV; (2) the presence of lacunes (OR, 6.939; 95% CI, 3.384–14.230; p < 0.001), higher numbers of enlarged perivascular spaces in centrum semiovale (CSO-EPVS) (OR, 1.046; 95% CI, 1.024–1.067; p < 0.001), and severe WMH (OR, 2.764; 95% CI, 1.463–5.223; p = 0.002) were associated with the reduced regional cerebral blood flow; (3) the presence of lacunes (OR, 12.570; 95% CI, 2.893–54.624; p = 0.001), higher numbers of CSO-EPVS (OR, 1.103; 95% CI, 1.058–1.150; p < 0.001), and severe WMH (OR, 5.982; 95% CI, 1.727–20.716; p = 0.005) were associated with ischemic cerebrovascular events; (4) the higher number of CSO-EPVS (OR, 1.077; 95% CI, 1.026–1.131; p = 0.003) was associated with good PCF. The lacunes, WMH, and CSO-EPVS were independently associated with these MMD characteristics. In conclusion, this study provided a novel and potential framework for the practical assessment of MMD by magnetic resonance imaging.
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References
Kuroda S, Houkin K. Moyamoya disease: current concepts and future perspectives. Lancet Neurol. 2008;7(11):1056–66.
Hervé D, Ibos-Augé N, Calvière L, Rogan C, Labeyrie MA, Guichard JP, et al. Predictors of clinical or cerebral lesion progression in adult moyamoya angiopathy. Neurology. 2019;93(4):e388–97.
Tho-Calvi SC, Thompson D, Saunders D, Agrawal S, Basu A, Chitre M, et al. Clinical features, course, and outcomes of a UK cohort of pediatric moyamoya. Neurology. 2018;90(9):e763–70.
Kang S, Liu X, Zhang D, Wang R, Zhang Y, Zhang Q, et al. Natural course of moyamoya disease in patients with prior hemorrhagic stroke. Stroke. 2019;50(5):1060–6.
Miyamoto S, Yoshimoto T, Hashimoto N, Okada Y, Tsuji I, Tominaga T, et al. Effects of extracranial-intracranial bypass for patients with hemorrhagic moyamoya disease: results of the Japan Adult Moyamoya Trial. Stroke. 2014;45(5):1415–21.
Kuroda S, Hashimoto N, Yoshimoto T, Iwasaki Y. Radiological findings, clinical course, and outcome in asymptomatic moyamoya disease: results of multicenter survey in Japan. Stroke. 2007;38(5):1430–5.
Guidelines for diagnosis and treatment of moyamoya disease (spontaneous occlusion of the circle of Willis). Neurol Med Chir (Tokyo). 2012;52(5):245–66.
Yin H, Liu X, Zhang D, Zhang Y, Wang R, Zhao M, et al. A novel staging system to evaluate cerebral hypoperfusion in patients with moyamoya disease. Stroke. 2018;49(12):2837–43.
Komatsu K, Mikami T, Noshiro S, Miyata K, Wanibuchi M, Mikuni N. Reversibility of white matter hyperintensity by revascularization surgery in moyamoya disease. J Stroke Cerebrovasc Dis. 2016;25(6):1495–502.
Kikuta K, Takagi Y, Nozaki K, Sawamoto N, Fukuyama H, Hashimoto N. The presence of multiple microbleeds as a predictor of subsequent cerebral hemorrhage in patients with moyamoya disease. Neurosurgery. 2008;62(1):104–11, 111–2.
Kuribara T, Mikami T, Komatsu K, Suzuki H, Ohnishi H, Houkin K, et al. Prevalence of and risk factors for enlarged perivascular spaces in adult patients with moyamoya disease. BMC Neurol. 2017;17(1):149.
Yu J, Du Q, Xie H, Chen J, Chen J. What and why: the current situation and future prospects of “ivy sign” in moyamoya disease. Ther Adv Chronic Dis. 2020;11:1754251780.
Xu T, Feng Y, Wu W, Shen F, Ma X, Deng W, et al. The predictive values of different small vessel disease scores on clinical outcomes in mild ICH patients. J Atheroscler Thromb. 2021.
Pantoni L. Cerebral small vessel disease: from pathogenesis and clinical characteristics to therapeutic challenges. Lancet Neurol. 2010;9(7):689–701.
Charidimou A, Martinez-Ramirez S, Reijmer YD, Oliveira-Filho J, Lauer A, Roongpiboonsopit D, et al. Total magnetic resonance imaging burden of small vessel disease in cerebral amyloid angiopathy: an imaging-pathologic study of concept validation. JAMA Neurol. 2016;73(8):994–1001.
Wardlaw JM, Smith EE, Biessels GJ, Cordonnier C, Fazekas F, Frayne R, et al. Neuroimaging standards for research into small vessel disease and its contribution to ageing and neurodegeneration. Lancet Neurol. 2013;12(8):822–38.
Shaaban CE, Jorgensen DR, Gianaros PJ, Mettenburg J, Rosano C. Cerebrovascular disease: neuroimaging of cerebral small vessel disease. Prog Mol Biol Transl Sci. 2019;165:225–55.
Caprio FZ, Maas MB, Rosenberg NF, Kosteva AR, Bernstein RA, Alberts MJ, et al. Leukoaraiosis on magnetic resonance imaging correlates with worse outcomes after spontaneous intracerebral hemorrhage. Stroke. 2013;44(3):642–6.
Charidimou A, Boulouis G, Roongpiboonsopit D, Auriel E, Pasi M, Haley K, et al. Cortical superficial siderosis multifocality in cerebral amyloid angiopathy: a prospective study. Neurology. 2017;89(21):2128–35.
Das AS, Regenhardt RW, Vernooij MW, Blacker D, Charidimou A, Viswanathan A. Asymptomatic cerebral small vessel disease: insights from population-based studies. J Stroke. 2019;21(2):121–38.
Wenz H, Wenz R, Maros M, Ehrlich G, Al-Zghloul M, Groden C, et al. Incidence, locations, and longitudinal course of cerebral microbleeds in European moyamoya. Stroke. 2017;48(2):307–13.
Kim JM, Park KY, Kim HR, Ahn HY, Pantoni L, Park MS, et al. Association of bone mineral density to cerebral small vessel disease burden. Neurology. 2021;96(9):e1290–300.
Staals J, Makin SD, Doubal FN, Dennis MS, Wardlaw JM. Stroke subtype, vascular risk factors, and total MRI brain small-vessel disease burden. Neurology. 2014;83(14):1228–34.
Fazekas F, Chawluk JB, Alavi A, Hurtig HI, Zimmerman RA. MR signal abnormalities at 1.5 T in Alzheimer’s dementia and normal aging. AJR Am J Roentgenol. 1987;149(2):351–6.
Suzuki J, Takaku A. Cerebrovascular “moyamoya” disease. Disease showing abnormal net-like vessels in base of brain. Arch Neurol. 1969;20(3):288–99.
Matsushima T, Inoue T, Suzuki SO, Fujii K, Fukui M, Hasuo K. Surgical treatment of moyamoya disease in pediatric patients–comparison between the results of indirect and direct revascularization procedures. Neurosurgery. 1992;31(3):401–5.
Ge P, Ye X, Liu X, Deng X, Wang J, Wang R, et al. Angiographic outcomes of direct and combined bypass surgery in moyamoya disease. Front Neurol. 2019;10:1267.
Zhao Y, Li J, Lu J, Zhang Q, Zhang D, Wang R, et al. Predictors of neoangiogenesis after indirect revascularization in moyamoya disease: a multicenter retrospective study. J Neurosurg. 2019;1–11.
Vermeer SE, Longstreth WT, Koudstaal PJ. Silent brain infarcts: a systematic review. Lancet Neurol. 2007;6(7):611–9.
Santos M, Gold G, Kövari E, Herrmann FR, Bozikas VP, Bouras C, et al. Differential impact of lacunes and microvascular lesions on poststroke depression. Stroke. 2009;40(11):3557–62.
Choi P, Ren M, Phan TG, Callisaya M, Ly JV, Beare R, et al. Silent infarcts and cerebral microbleeds modify the associations of white matter lesions with gait and postural stability: population-based study. Stroke. 2012;43(6):1505–10.
Vernooij MW, van der Lugt A, Ikram MA, Wielopolski PA, Niessen WJ, Hofman A, et al. Prevalence and risk factors of cerebral microbleeds: the Rotterdam Scan Study. Neurology. 2008;70(14):1208–14.
Konstas AA, Goldmakher GV, Lee TY. Theoretic basis and technical implementations of CT perfusion in acute ischemic stroke, part 2: technical implementations. AJNR Am J Neuroradiol. 2009;30(5):885–92.
Acknowledgements
We sincerely thank Rui Guo and Zhiyuan Yu for they have provided general advice and guidance on statistical analysis.
Funding
This study was supported by funding from the National Key R&D Program of China (No. 2018YFA0108603); 1·3·5 Project for Disciplines of Excellence, West China Hospital, Sichuan University (No. 2018HXFH007); Clinical Research Innovation Project, West China Hospital, Sichuan University (No. 2019HXCX07); 1·3·5 Project for Disciplines of Excellence⁃Clinical Research Incubation Project, West China Hospital, Sichuan University (No. 2021HXFH014); Science and Technology Department of Sichuan Province (No. 2020YFS0223); and 1·3·5 Project for Disciplines of Excellence, West China Hospital, Sichuan University (No. 2018HXFH010).
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Conceptualization, H.S. and Y.L.; methodology, H.S., Y.L., and C.Y.; formal analysis and investigation, W.L., C.X., Y.R., and A.X.; writing (original draft preparation), H.S. and W.L.; writing (review and editing): L.M., R.T., Y.L., and X.W.; funding acquisition, Y.L. and C.Y.; supervision, Y.L. and C.Y..
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The study was approved by the Institutional Review Board and Ethics Committee of West China Hospital, Sichuan University (No. 2018–219).
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Sun, H., Li, W., Xia, C. et al. Magnetic Resonance Imaging Markers of Cerebral Small Vessel Disease in Adults with Moyamoya Disease. Transl. Stroke Res. 13, 533–542 (2022). https://doi.org/10.1007/s12975-021-00973-7
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DOI: https://doi.org/10.1007/s12975-021-00973-7