Top

Journal of Neurology

Published in:

01-06-2023 | Acetylsalicylic Acid | Original Communication

Progression of initially unilateral Moyamoya angiopathy in Caucasian Europeans

Authors: Daniel Strunk, Rolf R. Diehl, Roland Veltkamp, Sven G. Meuth, Markus Kraemer

Published in: Journal of Neurology | Issue 9/2023

Abstract

Background

Moyamoya angiopathy (MMA) is a rare cause of stroke in Caucasians, but it is much more frequent in East Asia. Since 2021, diagnostic criteria not only comprise bilateral, but also unilateral MMA. Hitherto, progression of unilateral MMA has predominantly been described in East Asians. Our study aimed to analyze the occurrence and characteristics of progression of initially unilateral MMA in Caucasian Europeans.

Methods

By retrospective analysis of medical records of 200 European Caucasians with MMA, admitted to our German center between 2010 and 2022, cases of unilateral MMA and its progression, i.e. progressive ipsi- or novel contralateral arterial stenosis, during follow-up were identified. Kruskal Wallis Test and Fisher’s Exact Test were used to identify statistically significant differences between progressive and stable patients concerning demographic, clinical, laboratory, and radiographic features.

Results

Our cohort comprised 63 patients with initially unilateral MMA. Fourteen (22.2%) had an ipsi- (n = 3, 21.4%) or contralateral (n = 11, 78.6%) progression. Mean age of patients with progressive MMA at symptom onset was 32 ± 14.1 years. The ratio of women to men in this subgroup was 2.5:1. Mean follow-up period was 5.4 ± 3.7 years, mean age at progression was 39.9 ± 12.7 years. Mean time interval between penultimate follow-up and progression was 4.8 ± 4.5 years. Patients with progression showed affection of the posterior cerebral artery (p = 0.009) and suffered from vertigo (p = 0.009) significantly more often.

Conclusion

Unilateral MMA progresses in a substantial proportion in European Caucasians. Long-term follow-up is required due to potential late progression with consecutive symptoms and the need for bypass surgery.

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 (2012) Guidelines for diagnosis and treatment of moyamoya disease (spontaneous occlusion of the circle of Willis). Neurol Med Chir (Tokyo) 52:245–266. https://doi.org/10.2176/nmc.52.245CrossRef

Scott RM, Smith ER (2009) Moyamoya disease and moyamoya syndrome. N Engl J Med 360:1226–1237. https://doi.org/10.1056/NEJMra0804622CrossRefPubMed

Fullerton HJ, Stence N, Hills NK et al (2018) Focal cerebral arteriopathy of childhood. Stroke 49:2590–2596. https://doi.org/10.1161/STROKEAHA.118.021556CrossRefPubMedPubMedCentral

Steinlin M, Bigi S, Stojanovski B et al (2017) Focal cerebral arteriopathy: Do steroids improve outcome? Stroke 48:2375–2382. https://doi.org/10.1161/STROKEAHA.117.016818CrossRefPubMed

Kuroda S, Fujimura M, Takahashi J et al (2022) Diagnostic criteria for Moyamoya disease—2021 revised version. Neurol Med Chir (Tokyo) 62:307–312. https://doi.org/10.2176/jns-nmc.2022-0072CrossRefPubMed

Zhang Q, Wang R, Liu Y et al (2016) Clinical features and long-term outcomes of unilateral Moyamoya disease. World Neurosurg 96:474–482. https://doi.org/10.1016/j.wneu.2016.09.018CrossRefPubMed

Yeon JY, Shin HJ, Kong D-S et al (2011) The prediction of contralateral progression in children and adolescents with unilateral Moyamoya disease. Stroke 42:2973–2976. https://doi.org/10.1161/STROKEAHA.111.622522CrossRefPubMed

Hever P, Alamri A, Tolias C (2015) Moyamoya angiopathy—Is there a Western phenotype? Br J Neurosurg 29:765–771. https://doi.org/10.3109/02688697.2015.1096902CrossRefPubMed

Liu W, Senevirathna STMLD, Hitomi T et al (2013) Genomewide association study identifies no major founder variant in Caucasian moyamoya disease. J Genet 92:605–609. https://doi.org/10.1007/s12041-013-0304-5CrossRefPubMed

10.

Bersano A, Khan N, Fuentes B et al (2023) European Stroke Organisation (ESO) Guidelines on Moyamoya angiopathy: endorsed by Vascular European Reference Network (VASCERN). Eur Stroke J. https://doi.org/10.1177/23969873221144089CrossRefPubMedPubMedCentral

11.

Church EW, Bell-Stephens TE, Bigder MG et al (2020) Clinical course of unilateral Moyamoya disease. Neurosurgery 87:1262. https://doi.org/10.1093/neuros/nyaa284CrossRefPubMed

12.

Lee SC, Jeon JS, Kim JE et al (2014) Contralateral progression and its risk factor in surgically treated unilateral adult moyamoya disease with a review of pertinent literature. Acta Neurochir (Wien) 156:103–111. https://doi.org/10.1007/s00701-013-1921-8CrossRefPubMed

13.

Veselinovic N, Zidverc-Trajkovic J, Semnic R et al (2014) Moyamoya, unilateral to bilateral in one year. Vasa 43:284–286. https://doi.org/10.1024/0301-1526/a000364CrossRefPubMed

14.

Kim TW, Seo BR, Kim JH, Kim YO Rapid Progression of Unilateral Moyamoya Disease. J Korean Neurosurg Soc 49:65–67

15.

Hervé D, Ibos-Augé N, Calvière L et al (2019) Predictors of clinical or cerebral lesion progression in adult moyamoya angiopathy. Neurology 93:e388–e397. https://doi.org/10.1212/WNL.0000000000007819CrossRefPubMedPubMedCentral

16.

Savolainen M, Mustanoja S, Pekkola J et al (2019) Moyamoya angiopathy: long-term follow-up study in a Finnish population. J Neurol 266:574–581. https://doi.org/10.1007/s00415-018-9154-7CrossRefPubMed

17.

Smith ER, Scott RM (2008) Progression of disease in unilateral moyamoya syndrome. Neurosurg Focus 24:E17. https://doi.org/10.3171/FOC/2008/24/2/E17CrossRefPubMed

18.

Kelly ME, Bell-Stephens TE, Marks MP et al (2006) Progression of unilateral Moyamoya disease: a clinical series. Cerebrovasc Dis 22:109–115. https://doi.org/10.1159/000093238CrossRefPubMed

19.

Tian X, Hu M, Zhang J (2022) The contralateral progression in a cohort of Chinese adult patients with unilateral moyamoya disease after revascularization: a single-center long-term retrospective study. Acta Neurochir (Wien) 164:1837–1844. https://doi.org/10.1007/s00701-022-05153-6CrossRefPubMed

20.

Mineharu Y, Takagi Y, Koizumi A et al (2021) Genetic and nongenetic factors for contralateral progression of unilateral moyamoya disease: the first report from the SUPRA Japan Study Group. J Neurosurg 136:1005–1014. https://doi.org/10.3171/2021.3.JNS203913CrossRefPubMed

21.

Ok T, Jung YH, Kim J et al (2022) RNF213 R4810K variant in suspected unilateral Moyamoya disease predicts contralateral progression. J Am Heart Assoc 11:e025676. https://doi.org/10.1161/JAHA.122.025676CrossRefPubMedPubMedCentral

22.

Mineharu Y, Takagi Y, Takahashi JC et al (2013) Rapid progression of unilateral Moyamoya disease in a patient with a family history and an RNF213 risk variant. Cerebrovasc Dis 36:155–157. https://doi.org/10.1159/000352065CrossRefPubMed

23.

Mertens R, Graupera M, Gerhardt H et al (2022) The genetic basis of Moyamoya disease. Transl Stroke Res 13:25–45. https://doi.org/10.1007/s12975-021-00940-2CrossRefPubMed

24.

Hackenberg A, Battilana B, Hebeisen M et al (2021) Preoperative clinical symptomatology and stroke burden in pediatric moyamoya angiopathy: defining associated risk variables. Eur J Paediatr Neurol EJPN Off J Eur Paediatr Neurol Soc 35:130–136. https://doi.org/10.1016/j.ejpn.2021.10.007CrossRef

25.

Grangeon L, Guey S, Schwitalla JC et al (2019) Clinical and molecular features of 5 European multigenerational families with Moyamoya angiopathy. Stroke 50:789–796. https://doi.org/10.1161/STROKEAHA.118.023972CrossRefPubMed

Title: Progression of initially unilateral Moyamoya angiopathy in Caucasian Europeans
Authors: Daniel Strunk
Rolf R. Diehl
Roland Veltkamp
Sven G. Meuth
Markus Kraemer
Publication date: 01-06-2023
Publisher: Springer Berlin Heidelberg
Keywords: Acetylsalicylic Acid
Acetylsalicylic Acid
Published in: Journal of Neurology / Issue 9/2023
Print ISSN: 0340-5354
Electronic ISSN: 1432-1459
DOI: https://doi.org/10.1007/s00415-023-11793-0

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Progression of initially unilateral Moyamoya angiopathy in Caucasian Europeans

Abstract

Background

Methods

Results

Conclusion

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Abstract

Background

Methods

Results

Conclusion

Please log in to get access to this content

Other articles of this Issue 9/2023

Morphological and molecular comparison of HIV-associated and sporadic inclusion body myositis

Neurodegeneration in the retina of motoneuron diseases: a longitudinal study in amyotrophic lateral sclerosis and Kennedy’s disease

Clinical features and maternal and fetal outcomes in women with Guillain-Barré syndrome in pregnancy

The expanding spectrum of antibody-associated cerebellar ataxia: report of two new cases of anti-AP3B2 ataxia

Eculizumab for the treatment of glycine receptor antibody associated stiff-person syndrome

Impacts of exposure to ambient temperature and altitude on the burden of stroke