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Progression of initially unilateral Moyamoya angiopathy in Caucasian Europeans

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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.

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References

  1. 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.52.245

    Article  Google Scholar 

  2. Scott RM, Smith ER (2009) Moyamoya disease and moyamoya syndrome. N Engl J Med 360:1226–1237. https://doi.org/10.1056/NEJMra0804622

    Article  CAS  PubMed  Google Scholar 

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

    Article  PubMed  PubMed Central  Google Scholar 

  4. 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.117.016818

    Article  PubMed  Google Scholar 

  5. 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.2022-0072

    Article  PubMed  Google Scholar 

  6. 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.2016.09.018

    Article  PubMed  Google Scholar 

  7. 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.111.622522

    Article  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  9. 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/s12041-013-0304-5

    Article  PubMed  Google Scholar 

  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/10.1177/23969873221144089

    Article  PubMed  PubMed Central  Google Scholar 

  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/nyaa284

    Article  PubMed  Google Scholar 

  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/s00701-013-1921-8

    Article  PubMed  Google Scholar 

  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/a000364

    Article  PubMed  Google Scholar 

  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.0000000000007819

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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/s00415-018-9154-7

    Article  PubMed  Google Scholar 

  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/E17

    Article  PubMed  Google Scholar 

  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/10.1159/000093238

    Article  PubMed  Google Scholar 

  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/s00701-022-05153-6

    Article  PubMed  Google Scholar 

  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.JNS203913

    Article  PubMed  Google Scholar 

  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.122.025676

    Article  PubMed  PubMed Central  Google Scholar 

  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/10.1159/000352065

    Article  PubMed  Google Scholar 

  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/s12975-021-00940-2

    Article  CAS  PubMed  Google Scholar 

  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.2021.10.007

    Article  Google Scholar 

  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.118.023972

    Article  PubMed  Google Scholar 

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Authors and Affiliations

  1. Department of Neurology, European Reference Center for Moyamoya Angiopathy (VASCERN, ERN), Alfried Krupp Hospital, Alfried-Krupp-Straße 21, 45131, Essen, Germany

    Daniel Strunk, Rolf R. Diehl, Roland Veltkamp & Markus Kraemer

  2. Department of Brain Sciences, Imperial College London, London, UK

    Roland Veltkamp

  3. Department of Neurology, Medical Faculty, Heinrich-Heine University Düsseldorf, Düsseldorf, Germany

    Sven G. Meuth & Markus Kraemer

Authors
  1. Daniel Strunk
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  2. Rolf R. Diehl
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  3. Roland Veltkamp
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  4. Sven G. Meuth
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  5. Markus Kraemer
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Contributions

All authors were involved in drafting the article or revising it critically for important intellectual content, and all authors approved the final version to be published. Study conception and design: MK. Acquisition of data: DS and MK. Analysis and interpretation of data: RRD, DS and MK. Revision of the manuscript for intellectual content and interpretation of the data: RV, SGM.

Corresponding author

Correspondence to Markus Kraemer.

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The authors declare no competing interests.

Ethical approval

This study was performed in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki Declaration.

Research ethic and patient consent

This work is based on retrospective data collection, obtained from the routine monitoring of patients’ treatments and their clinical evaluation in the hospital setting. As such, and according to national regulations, it does not require specific approval from the ethics committee.

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Strunk, D., Diehl, R.R., Veltkamp, R. et al. Progression of initially unilateral Moyamoya angiopathy in Caucasian Europeans. J Neurol 270, 4415–4422 (2023). https://doi.org/10.1007/s00415-023-11793-0

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  • DOI: https://doi.org/10.1007/s00415-023-11793-0

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