Advances in Clinical Classification of Moyamoya Disease

doi:10.3969/j.issn.1673-5765.2022.10.014

Abstract

Abstract: Moyamoya disease (MMD) is a cerebrovascular disease characterized by progressive stenosis of internal carotid arteries and their proximal branches with abnormal vascular network at skull base, which is clinically divided into ischemic, hemorrhagic and asymptomatic types. With the progress of diagnosis and treatment technology, the understanding of epidemiological characteristics of different clinical classification of MMD has developed. The majority of adult patients are ischemic type and the asymptomatic type is gradually increasing. The age of onset, genetic background, pathophysiological mechanism, collateral vascular compensation, distribution of involved vessels and prognosis of MMD were significantly different among different types. This article summarized the historical evolution of epidemiological characteristics, the possible genetic background, pathophysiological mechanism and imaging manifestations of different clinical classification of MMD, to provide new ideas for clinical treatment strategy of MMD.

Key words: Moyamoya disease; Clinical classification; Genetic; Mechanism; Treatment

摘要： 烟雾病（moyamoya disease，MMD）是一种颈内动脉末端及其分支起始处进行性狭窄伴颅底异常血管网形成的脑血管疾病，临床上常将其分为缺血型、出血型和无症状型。随着诊疗技术的进步，对MMD临床分型的流行病学特征认识也在不断发展。在成年患者中，缺血型MMD占有重要地位，无症状型亦呈逐渐增多的趋势。不同临床分型MMD的发病年龄、遗传背景、病理生理机制、侧支血管代偿、受累血管分布及其预后存在显著差异。本文总结了对MMD临床分型流行病学特征认识的历史演变，不同临床分型可能的遗传背景、病理生理机制和影像学表现上的差异，为基于不同临床分型的MMD治疗决策提供新的思路。

关键词: 烟雾病; 临床分型; 遗传; 机制; 治疗

HAN Guangsong, NI Jun. Advances in Clinical Classification of Moyamoya Disease [J]. Chinese Journal of Stroke, 2022, 17(10): 1120-1126.

韩广淞, 倪俊. 烟雾病临床分型研究进展[J]. 中国卒中杂志, 2022, 17(10): 1120-1126.

References

[1] KIM J S. Moyamoya disease：epidemiology，clinical features，and diagnosis[J]. J Stroke，2016，18（1）：2-11.
[2] SHANG S L，ZHOU D，YA J Y，et al. Progress in moyamoya disease[J]. Neurosurg Rev，2020，43（2）：371-382.
[3] TAKEUCHI K，SHIMIZU K. Hypoplasia of the bilateral internal carotid arteries[J]. Brain Nerve，1957，9（1）：37-43.
[4] SATO Y，KAZUMATA K，NAKATANI E，et al. Characteristics of moyamoya disease based on national registry data in Japan[J]. Stroke，2019，50（8）：1973-1980.
[5] AHN I M，PARK D H，HANN H J，et al. Incidence，prevalence，and survival of moyamoya disease in Korea：a nationwide，population-based study[J]. Stroke，2014，45（4）：1090-1095.
[6] BAO X Y，WANG Q N，ZHANG Y，et al. Epidemiology of moyamoya disease in China：single-center，population-based study[J/OL]. World Neurosurg，2019，122：e917-e923[2022-04-20]. https://doi.org/10.1016/j.wneu.2018.10.175.
[7] ZHANG D，HUANG L G，HUANG Z，et al. Epidemiology of moyamoya disease in China：a nationwide hospital-based study[J/OL]. Lancet Reg Health West Pac，2021，18：100331[2022-04-20]. https://doi.org/10.1016/j.lanwpc.2021.100331.
[8] SUZUKI J，KODAMA N. Moyamoya disease-a review[J]. Stroke，1983，14（1）：104-109.
[9] KURODA S，HOUKIN K. Moyamoya disease：current concepts and future perspectives[J]. Lancet Neurol，2008，7（11）：1056-1066，2008.
[10] BABA T，HOUKIN K，KURODA S. Novel epidemiological features of moyamoya disease[J]. J Neurol Neurosurg Psychiatry，2008，79（8）：900-904.
[11] 高山，倪俊，黄家星，等. 烟雾病临床特点分析[J]. 中华神经科杂志，2006，39（3）：176-179.
[12] YAMADA M，FUJII K，FUKUI M. Clinical features and outcomes in patients with asymptomatic moyamoya disease-from the results of nation-wide questionnaire survey[J]. No Shinkei Geka，2005，33（4）：337-342.
[13] MIAO W，ZHAO P L，ZHANG Y S，et al. Epidemiological and clinical features of moyamoya disease in Nanjing，China[J]. Clin Neurol Neurosurg，2010，112（3）：199-203.
[14] DUAN L，BAO X Y，YANG W Z，et al. Moyamoya disease in China：its clinical features and outcomes[J]. Stroke，2012，43（1）：56-60.
[15] SCOTT R M，SMITH E R. Moyamoya disease and moyamoya syndrome[J]. N Engl J Med，2009，360（12）：1226-1237.
[16] WANG Y，YANG L P，WANG X T，et al. Meta-analysis of genotype and phenotype studies to confirm the predictive role of the RNF213 p. R4810K variant for moyamoya disease[J]. Eur J Neurol，2021，28（3）：823-836.
[17] WU Z Y，JIANG H Q，ZHANG L，et al. Molecular analysis of RNF213 gene for moyamoya disease in the Chinese Han population[J/OL]. PLoS One，2012，7（10）：e48179[2022-04-20]. https://doi.org/10.1371/journal.pone.0048179.
[18] CECCHI A C，GUO D C，REN Z，et al. RNF213 rare variants in an ethnically diverse population with moyamoya disease[J]. Stroke，2014，45（11）：3200-3207.
[19] BANG O Y，CHUNG J W，CHA J，et al. A polymorphism in RNF213 is a susceptibility gene for intracranial atherosclerosis[J/OL]. PLoS One，2016，11（6）：e0156607[2022-04-20]. https://doi.org/10.1371/journal.pone.0156607.
[20] RAFAT N，BECK G C H，PEÑA-TAPIA P G，et al. Increased levels of circulating endothelial progenitor cells in patients with moyamoya disease[J]. Stroke，2009，40（2）：432-438.
[21] GUO D C，PAPKE C L，TRAN FADULU V，et al. Mutations in smooth muscle alpha-actin（ACTA2）cause coronary artery disease，stroke，and moyamoya disease，along with thoracic aortic disease[J]. Am J Hum Genet，2009，84（5）：617-627.
[22] WANG X，HAN C，JIA Y J，et al. Proteomic profiling of exosomes from hemorrhagic moyamoya disease and dysfunction of mitochondria in endothelial cells[J]. Stroke，2021，52（10）：3351-3361.
[23] LU J L，WANG J Y，LIN Z D，et al. MMP-9 as a biomarker for predicting hemorrhagic strokes in moyamoya disease[J/OL]. Front Neurol，2021，12：721118[2022-04-20]. https://doi.org/10.3389/fneur.2021.721118.
[24] LU M M，ZHANG H T，LIU D Q，et al. Association of intracranial vessel wall enhancement and cerebral hemorrhage in moyamoya disease：a high-resolution magnetic resonance imaging study[J]. J Neurol，2021，268（12）：4768-4777.
[25] KATHUVEETIL A，SYLAJA P N，SENTHILVE-LAN S，et al. Vessel wall thickening and enhancement in high-resolution intracranial vessel wall imaging：a predictor of future ischemic events in moyamoya disease[J]. AJNR Am J Neuroradiol，2020，41（1）：100-105.
[26] ZHAO M，ZHANG D，WANG S，et al. Posterior circulation involvement in pediatric and adult patients with moyamoya disease：a single center experience in 574 patients[J]. Acta Neurol Belg，2018，118（2）：227-233.
[27] TAN C X，DUAN R，YE X，et al. Posterior circulation moyamoya disease versus primitive vertebral-basilar artery system moyamoya disease：new classification of moyamoya disease from the perspective of embryology[J/OL]. World Neurosurg，2016，96：222-229[2022-04-20]. https://doi.org/10.1016/j.wneu.2016.08.099.
[28] JANG D K，LEE K S，RHA H K，et al. Clinical and angiographic features and stroke types in adult moyamoya disease[J]. AJNR Am J Neuroradiol，2014，35（6）：1124-1131.
[29] FUNAKI T，TAKAHASHI J C，YOSHIDA K，et al. Periventricular anastomosis in moyamoya disease：detecting fragile collateral vessels with MR angiography[J]. J Neurosurg，2016，124（6）：1766-1772.
[30] HIRANO Y，MIYAWAKI S，IMAI H，et al. Differences in clinical features among different onset patterns in moyamoya disease[J]. J Clin Med，2021，10（13）：2815.
[31] KURODA S，AMORE Study Group. Asymptomatic moyamoya disease：literature review and ongoing AMORE study[J]. Neurol Med Chir（Tokyo），2015，55（3）：194-198.
[32] HERVÉ D，KOSSOROTOFF M，BRESSON D，et al. French clinical practice guidelines for moyamoya angiopathy[J]. Rev Neurol（Paris），2018，174（5）：292-303.
[33] 烟雾病治疗中国专家共识编写组. 烟雾病治疗中国专家共识[J]. 国际脑血管病杂志，2019，27（9）：645-650.
[34] LU J L，SHI G C，ZHAO Y L，et al. Effects and safety of aspirin use in patients after cerebrovascular bypass procedures[J]. Stroke Vasc Neurol，2021，6（4）：624-630.
[35] KURODA S，HASHIMOTO N，YOSHIMOTO T，et al. Radiological findings，clinical course，and outcome in asymptomatic moyamoya disease：results of multicenter survey in Japan[J]. Stroke，2007，38（5）：1430-1435.