Moyamoya disease and syndrome

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Moyamoya disease (MMD) is a rare disease characterized by progressive stenosis of the terminal part of the internal carotid arteries (ICA) and the proximal part of their branches, which is accompanied by the formation of collateral network that look like smoke clouds on angiography (Japanese terminology — moyamoya). If the disease is comorbid to other diseases, usually associated with acute or chronic inflammation, including autoimmune processes, it is designated as moyamoy syndrome (MMS). MMD and MMS are one of the causes of ischemic stroke and chronic cerebrovascular insufficiency in young and middle age, less often they lead to hemorrhages. The review presents data on epidemiology, morphology, pathogenesis (the role of genetic predisposition, inflammation, proangiogenic factors and immune disorders), clinical manifestations, instrumental diagnostics and treatment.

Keywords:

moyamoya disease

moyamoya syndrome

stroke

genetics

treatment

Authors:

L.A. Kalashnikova

Research Center of Neurology

ORCID: 0000-0003-1142-0548

Received:

24.01.2023

Accepted:

28.02.2023

List of references:

Takeuchi K, Shimizu K. Hypogenesis of bilateral internal carotid arteries. No To Shinkei. 1957;9:37-43.
Takeuchi K. Occlusive Diseases of the Carotid Artery: Especially on Their Surgical Treatment. Shinkei Shimpo. 1961;5:511-543.
Suzuki J, Takaku A. Cerebrovascular «Moaymoya» disease. Disease showing abnormal net-like vessels in base of brain. Arch Neurol. 1969;20:288-299. https://doi.org/10.1001/archneur.1969.00480090076012
Achrol AS, Guzman R, Lee M, Steinberg GK. Pathophysiology and genetic factors in moyamoya disease. Neurosurg Focus. 2009;26(4):E4. https://doi.org/10.3171/2009.1.FOCUS08302
Rafat N, Beck GC, Peña-Tapia PG, et al. Increased levels of circulating endothelial progenitor cells in patients with moyamoya disease. Stroke. 2009;40(2):432-438. https://doi.org/10.1161/STROKEAHA.108.529420
Kuroda S, Hashimoto N, Yoshimoto T, Iwasaki Y. Research Committee on Moyamoya Disease in Japan. Radiological findings, clinical course, and outcome in asymptomatic moyamoya disease: results of multicenter survey in Japan. Stroke. 2007;38:1430-1435. https://doi.org/10.1161/STROKEAHA.106.478297
Tominaga T. Overview. In: B.-K. Cho and T. Tominaga (eds.). Moyamoya Disease Update. Springer; 2010;3-11. https://doi.org/10.1007/978-4-431-99703-0
Mineharu Y, Liu W, Inoue K, et al. Autosomal dominant moyamoya disease maps to chromosome 17q25.3. Neurology. 2008;70:2357-2363. https://doi.org/10.1212/01.wnl.0000291012.49986.f9
Research Committee on the Pathology and Treatment of Spontaneous Occlusion of the Circle of Willis; Health Labour Sciences Research Grant for Research on Measures for Infractable Diseases: Guidelines for diagnosis and treatment of moyamoya disease (spontaneous occlusion of the circle of Willis). Neurol Med Chir (Tokyo). 2012;52:245-266. https://doi.org/10.2176/nmc.52.245
Houkin K, Mikami T. Moyamoya disease and moyamoya syndrome. In Wanebo J, Khan N, Zabramski J, Spetzler R (eds): Moyamoya Disease: Diagnosis and Treatment. New York, Thieme; 2014;3-9.
Hallemeier CL, Rich KM, Grubb RL, et al. Clinical features and outcome in North American adults with moyamoya phenomenon. Stroke. 2006;37(6):1490-1496. https://doi.org/10.1161/01.STR.0000221787.70503.ca
Lee SJ, Ahn JY. Stenosis of the proximal external carotid artery in an adult with moyamoya disease: moyamoya or atherosclerotic change? Neurol Med Chir (Tokyo). 2007;47(8):356-359. https://doi.org/10.2176/nmc.47.356
Fierini F, Barilarob A, Giambenec B, et al. Moyamoya in a patient with Sneddon’s syndrome. Clinical Neurology and Neurosurgery. 2015;129:34-36. https://doi.org/10.1016/j.clineuro.2014.12.001
Scott RM, Smith ER. Moyamoya disease and moyamoya syndrome. N Engl J Med. 2009;360:1226-1237. https://doi.org/10.1056/NEJMra0804622
Wei Yi-C, Liu C-H, Chang T-Y, et al. Coexisting diseases of moyamoya vasculopathy. J Stroke Cerebrovasc Dis. 2014;23(6):1344-1350. https://doi.org/10.1016/j.jstrokecerebrovasdis.2013.11.008
Chung J-W, Kim DH, Won H-H, et al. Moyamoya Disease and Spectrums of RNF213 Vasculopathy. Transl Stroke Res. 2020;11(4):580-589. https://doi.org/10.1007/s12975-019-00743-6
Feghali J, Xu R, Yang W, et al. Moyamoya disease versus moyamoya syndrome: comparison of presentation and outcome in 338 hemispheres. J Neurosurg. 2019;4:1-9. https://doi.org/10.3171/2019.6.JNS191099
Stejskal V, Šteiner I, Hornychová H, et al. Moyamoya disease associated with fibromuscular dysplasia of intrapulmonary bronchial arteries — a case report. Cardiovasc Pathol. 2020;45:107182. https://doi.org/10.1016/j.carpath.2019.107182
LiuY, Wu X, Fan Z, et al. Development of atherosclerotic-moyamoya syndrome with genetic variant of RNF213 p.R4810K and p.T1727M: A case report. Clin Neurol Neurosurg. 2018;168:163-166. https://doi.org/10.1016/j.clineuro.2018.01.034
Mikami T, Suzuki H, Komatsu K, Mikuni N. Influence of Inflammatory Disease on the Pathophysiology of Moyamoya Disease and Quasi-moyamoya Disease. Neurol Med Chir (Tokyo). 2019;59:361-370. https://doi.org/10.2176/nmc.ra.2019-0059
Hayashi K, Horie N, Suyama K, Nagata I. An epidemiological survey of moyamoya disease, unilateral moyamoya disease and quasi-moyamoya disease in Japan. Clin Neurol Neurosurg. 2013;115:930-933. https://doi.org/10.1016/j.clineuro.2012.09.020
Miao W, Zhao PL, Zhang YS, et al. Epidemiological and clinical features of moyamoya disease in Nanjing, China. Clinical Neurology and Neurosurgery. 2010;112:109-120. https://doi.org/10.1016/j.clineuro.2009.11.009
Hung CC, Tu YK, Su CF, et al. Epidemiological study of moyamoya disease in Taiwan. Clinical Neurology and Neurosurgery. 1997;99(suppl 2):23-25. https://doi.org/10.1016/s0303-8467(97)00036-x
Uchino K, Johnston SC, Becker KJ, Tirschwell DL. Moyamoya disease in Washington State and California. Neurology. 2005;65:956-958. https://doi.org/10.1212/01.wnl.0000176066.33797.82
Yonekawa Y, Fandino J, Hug M, et al. Moyamoya Angiopathy in Europe. Moyamoya Disease Update. Tokyo: Springer; 2010:361-369.
Kleinloog R, Regli L, Rinkel GJ, Klijn CJ. Regional differences in incidence and patient characteristics of moyamoya disease: a systematic review. J Neurol Neurosurg Psychiatry. 2012;83(5):531-536. https://doi.org/10.1136/jnnp-2011-301387
Chen PC, Yang SH, Chien KL, et al. Epidemiology of moyamoya disease in Taiwan: a nationwide population-based study. Stroke. 2014;45(5):1258-1263. https://doi.org/10.1161/STROKEAHA.113.004160
Graham JF, Matoba A. A survey of moyamoya disease in Hawaii. Clin Neurol Neurosurg. 1997;99(suppl 2):31-35. https://doi.org/10.1016/s0303-8467(97)00037-1
Fukui M. 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 Neurosurg. 1997;99:238-240.
LinR, Xie Z, Zhang J, et al. Clinical and immunopathological features of Moyamoya disease. PLoS One. 2012;7(4):e36386. https://doi.org/10.1371/journal.pone.0036386
Haltia M, Iivanainen M, Majuri H, Puranen M. Spontaneous occlusion of the circle of Willis (moyamoya syndrome). Clin Neuropathol. 1982;1(1):11-22.
Takagi Y, Kikuta K, Nozaki K, Hashimoto N. Histological features of middle cerebral arteries from patients treated for Moyamoya disease. Neurol Med Chir (Tokyo). 2007;47(1):1e4. https://doi.org/10.2176/nmc.47.1
Kraemer M, Keyvani K, Berlit P, et al. Histopathology of Moyamoya angiopathy in a European patient. J Neurol. 2019;266(9):2258-2262. https://doi.org/10.1007/s00415-019-09406-w
Masuda J, Ogata J, Yutani C. Smooth muscle cell proliferation and localization of macrophages and T cells in the occlusive intracranial major arteries in moyamoya disease. Stroke. 1993;24(12):1960-1967. https://doi.org/10.1161/01.str.24.12.1960
Guey S, Tournier-Lasserve E, Hervé D, Kossorotoff M. Moyamoya disease and syndromes: from genetics to clinical management Review. Appl Clin Genet. 2015;8:49-68. eCollection 2015. https://doi.org/10.2147/TACG.S42772
Jiang T, Perry A, Dacey RGJr, et al. Intracranial atherosclerotic disease associated with moyamoya collateral formation: histopathological findings. J Neurosurg. 2013;118(5):1030-1034. https://doi.org/10.3171/2013.1.JNS12565
Ikeda E, Hosoda Y. Distribution of thrombotic lesions in the cerebral arteries in spontaneous occlusion of the circle of Willis: cerebrovascular moyamoya disease. Clin Neuropathol. 1993;12(1):44-48.
Yamashita M, Oka K, Tanaka K. Histopathology of the brain vascular network in moyamoya disease. Stroke. 1983;14:50-58. https://doi.org/10.1161/01.STR.14.1.50
Nagasaka T, Shiozawa Z, Kobayashi M, et al. Autopsy findings in Down’s syndrome with cerebrovascular disorder. Clin Neuropathol. 1996;15(3):145-149.
Watabe N, Akiko N, Hiroaki A, et al. An autopsy case of Down’s syndrome with moyamoya syndrome. No Shinkei Geka. 2005;33(9):925-929.
Bang OY, Fujimura M, Kim S-K. The Pathophysiology of Moyamoya Disease: An Update. Journal of Stroke. 2016;18(1):12-20. https://doi.org/10.5853/jos.2015.01760
Kamada F, Aoki Y, Narisawa A, et al. A genome-wide association study identifies RNF213 as the first Moyamoya disease gene. J Hum Genet. 2011;56(1):34-40. https://doi.org/10.1038/jhg.2010.132
Liu W, Morito D, Takashima S, et al. Identification of RNF213 as a susceptibility gene for moyamoya disease and its possible role in vascular development. PLoS ONE. 2011;6(7):e22542. https://doi.org/10.1371/journal.pone.0022542
Bang OY, Chung JW, Kim DH, et al. Moyamoya Disease and Spectrums of RNF213 Vasculopathy. Transl Stroke Res. 2020;11(4):580-589. https://doi.org/10.1007/s12975-019-00743-6
Park YS, An HJ, Kim JO, et al. The role of RNF213 4810G>A and 4950G>Avariants in patients with moyamoya disease in Korea. Int J Mol Sci. 2017;18(11):E2477. https://doi.org/10.3390/ijms18112477
Koizumi A, Kobayashi H, Hitomi T, et al. A new horizon of moyamoya disease and associated health risks explored through RNF213. Environ Health Prev Med. 2016;21(2):55-70. https://doi.org/10.1007/s12199-015-0498-7
Grangeon L, Guey S, Schwitalla JC, et al. Clinical and molecular features of 5 European multigenerational families with moyamoya angiopathy. Stroke. 2019;50(4):789-796. https://doi.org/10.1161/STROKEAHA.118.023972
Mertens R, Graupera M, Gerhardt H, et al. The Genetic Basis of Moyamoya Disease. Transl Stroke Res. 2022;13(1):25-45. https://doi.org/10.1007/s12975-021-00940-2
Zhang Q, Liu Y, Zhang D, et al. RNF213 as the major susceptibility gene for Chinese patients with moyamoya disease and its clinical relevance. J Neurosurg. 2017;126(4):1106-1113. https://doi.org/10.3171/2016.2.JNS152173
Zhang Q, Liu Y, Yu L, et al. The Association of the RNF213 p.R4810K Polymorphism with Quasi-Moyamoya Disease and a Review of the Pertinent Literature. World Neurosurg. 2017;99:701-708. https://doi.org/10.1016/j.wneu.2016.12.119
Xu S, Wei W, Zhang F, et al. Transcriptomic profiling of intracranial arteries in adult patients with moyamoya disease reveals novel insights into its pathogenesis front mol neurosci. Front Mol Neurosci. 2022;15:881954. eCollection 2022. https://doi.org/10.3389/fnmol.2022.881954
Shang S, Zhou D, Ya J, et al. Progress in moyamoya disease. Neurosurg Rev. 2020;43(2):371-382. https://doi.org/10.1007/s10143-018-0994-5
Jiang H, Toscano JF, Schiraldi M, et al. Differential Expression of Vascular Endothelial Growth Factor-A 165 Isoforms Between Intracranial Atherosclerosis and Moyamoya Disease. J Stroke Cerebrovasc Dis. 2019;28(2):360-368. https://doi.org/10.1016/j.jstrokecerebrovasdis.2018.10.004
Mejia-Munne JC, Ellis JA, Feldstein NA, et al. Moyamoya and Inflammation. World Neurosurg. 2017;100:575-578. https://doi.org/10.1016/j.wneu.2017.01.012
Fox BM, Dorschel KB, Lawton MT, Wanebo JE. Pathophysiology of Vascular Stenosis and Remodeling in Moyamoya Disease. Front Neurol. 2021;12:661578. eCollection 2021. https://doi.org/10.3389/fneur.2021.661578
Han DH, Nam DH, Oh CW. Moyamoya disease in adults: characteristics of clinical presentation and outcome after encephalo-duro-arterio-synangiosis. Clin Neurol Neurosurg. 1997;99(suppl 2):151-155. https://doi.org/10.1016/s0303-8467(97)00058-9
Fukui M, Kono S, Sueishi K, Ikezaki K. Moyamoya disease. Neuropathology. 2000;20(suppl):61-64. https://doi.org/10.1046/j.1440-1789.2000.00300.x
Scott RM, Smith JL, Robertson RL, et al. Long-term outcome in children with moyamoya syndrome after cranial revascularization by pial synangiosis. J Neurosurg. 2004;100(2 suppl Pediatrics):142-149. https://doi.org/10.3171/ped.2004.100.2.0142
Kraemer M, Heienbrok W, Berlit P. Moyamoya disease in Europeans. Stroke. 2008;39(12):3193-3200. https://doi.org/10.1161/STROKEAHA.107.513408
Zach V, Bezov D, Lipton RB, Ashina S. Headache associated with moyamoya disease: a case story and literature review. J Headache Pain. 2010;11(1):79-82. https://doi.org/10.1007/s10194-009-0181-8
Mikami T, Ochi S, Houkin K, et al. Predictive factors for epilepsy in moyamoya disease. J Stroke Cerebrovasc Dis. 2015;24(1):17-23. https://doi.org/10.1016/j.jstrokecerebrovasdis.2014.07.050
Alramadan A, Haq AU, Basindwah S, Alshail E. Seizure outcome in moyamoya after indirect revascularization in pediatric patients: Retrospective study and literature review. Surg Neurol Int. 2021;12:73. https://doi.org/10.25259/SNI_633_2020
Kuroda N, Fujimoto A, Okanishi T, et al. Epilepsy surgery for a patient with neurofibromatosis type 1 concomitant with moyamoya syndrome. Case Reports. J Clin Neurosci. 2019;61:307-310. https://doi.org/10.1016/j.jocn.2018.10.050
Shi Z, Wen Y-J, Huang Z, et al. Different aspects of cognitive function in adult patients with moyamoya disease and its clinical subtypes. Stroke Vasc Neurol. 2020;5(1):86-96. https://doi.org/10.1136/svn-2019-000309
Yang S, Wang X, Liao W, et al. High-resolution MRI of the vessel wall helps to distinguish moyamoya disease from atherosclerotic moyamoya syndrome. Clin Radiol. 2021;76(5):392.e11-392.e19. https://doi.org/10.1016/j.crad.2020.12.023
Yamada I, Suzuki S, Matsushima Y. Moyamoya disease: diagnostic accuracy of MRI. Neuroradiology. 1995;37:356-361. https://doi.org/10.1007/BF00588011
Hu P, Sun J, Jin Y, et al. Conventional computed tomography and axial magnetic resonance t2-weighted imaging of horizontal segment of middle cerebral artery in moyamoya disease or syndrome in adult patients. J Stroke Cerebrovasc Dis. 2015;24(11):2555-2560. https://doi.org/10.1016/j.jstrokecerebrovasdis.2015.07.005
Kaku Y, Morioka M, Ohmori Y, et al. Outer-diameter narrowing of the internal carotid and middle cerebral arteries in moyamoya disease detected on 3d constructive interference in steady-state MR image: is arterial constrictive remodeling a major pathogenesis? Acta Neurochir. 2012;154:2151-2157. https://doi.org/10.1007/s00701-012-1472-4
Yuan M, Liu ZQ, Wang ZQ. High-resolution MR imaging of the arterial wall in moyamoya disease. Neurosci Lett. 2015;584:77-82. https://doi.org/10.1016/j.neulet.2014.10.021
Wu F, Han C, Liu Y, et al. Validation of choroidal anastomosis on high-resolution magnetic resonance imaging as an imaging biomarker in hemorrhagic moyamoya disease. Eur Radiol. 2021;31(7):4548-4556. https://doi.org/10.1007/s00330-020-07479-0
Ohta T, Tanaka H, Kuroiwa T. Diffuse leptomeningeal enhancement, «ivy sign», in magnetic resonance images of moyamoya disease in childhood: case report. Neurosurgery. 1995;37:1009-1012.
Vuignier S, Ito M, Kurisu K, et al. Ivy sign, misery perfusion, and asymptomatic moyamoya disease: flair imaging and (15)o-gas positron emission tomography. Acta Neurochir. 2013;155:2097-2104. https://doi.org/10.1007/s00701-013-1860-4
Mori N, Mugikura S, Higano S, et al. The leptomeningeal “ivy sign” on fluid-attenuated inversion recovery MR imaging in moyamoya disease: a sign of decreased cerebral vascular reserve? AJNR Am J Neuroradiol. 2009;30:930-935. https://doi.org/10.3174/ajnr.A1504
Zaharchuk G, Do HM, Marks MP, et al. Arterial spin-labeling MRI can identify the presence and intensity of collateral perfusion in patients with moyamoya disease. Stroke. 2011;42:2485-U2183. https://doi.org/10.1161/STROKEAHA.111.616466
Noguchi T, Kawashima M, Nishihara M, et al. Arterial spin-labeling MR imaging in Moyamoya disease compared with clinical assessments and other MR imaging findings. Eur J Radiol. 2013;82:840-847. https://doi.org/10.1016/j.ejrad.2013.08.040
Li J, Jin M, Sun X, et al. Imaging of Moyamoya Disease and Moyamoya Syndrome. Journal of Computer Assisted Tomography. 2019;43(2):257-263. https://doi.org/10.1097/rct.0000000000000834
Arai N, Horiguchi T, Takahashi S, et al. Hemodynamic stress distribution identified by SPECT reflects ischemic symptoms of Moyamoya disease patients. Neurosurg Rev. 2020;43(5):1323-1329. https://doi.org/10.1007/s10143-019-01145-w
Ruan LT, Duan YY, Cao TS, et al. Color and power Doppler sonography of extracranial and intracranial arteries in Moyamoya disease. J Clin Ultrasound. 2006;34:60-69. https://doi.org/10.1002/jcu.20201
Wang Y, Chen L, Wang Y, et al. Hemodynamic study with duplex ultrasonography on combined (direct/indirect) revascularization in adult moyamoya disease. J Stroke Cerebrovasc Dis. 2014;23:2573-2579. https://doi.org/10.1016/j.jstrokecerebrovasdis.2014.05.024
Kim JS, Kim Y-J, Ahn S-H, Kim BJ. Location of cerebral atherosclerosis: Why is there a difference between East and West? Int J Stroke. 2018;13(1):35-46. https://doi.org/10.1177/1747493016647736
Chen Z, Wu X, Zhou D, et al. Characteristics of cerebral ischemic stroke based on moyamoya disease and atherosclerosis-associated intracranial arterial stenosis. Neurol Sci. 2022;43(2):1087-1096. https://doi.org/10.1007/s10072-021-05359-z
Fujimura M, Tominaga T, Kuroda S, et al. 2021 Japanese Guidelines for the Management of Moyamoya Disease: Guidelines from the Research Committee on Moyamoya Disease and Japan Stroke Society. Neurol Med Chir (Tokyo). 2022;62(4):165-170. https://doi.org/10.2176/jns-nmc.2021-0382
Shulgina AA, Lukshin VA, Korshunov AE, et al. Modern trends in diagnosis and surgical treatment of moyamoya disease. Zhurnal Voprosy Neirokhirurgii im. N.N. Burdenko. 2020;84(4):90-103. (In Russ., In Engl.). https://doi.org/10.17116/neiro20208404190
Lukshin VA, Shulgina AA, Usachev DYu, et al. Ischemic complications following surgical treatment of moyamoya disease: risk factors and prevention. Zhurnal Voprosy Neirokhirurgii im. N.N. Burdenko. 2021;85(6):26-35. (In Russ., In Engl.). https://doi.org/10.17116/neiro20218506126
Winkler EA, Yue JK, Deng H, et al. National trends in cerebral bypass surgery in the United States, 2002-2014. Neurosurg Focus. 2019;46(2):E4. https://doi.org/10.3171/2018.11.FOCUS18530

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