Moyamoya disease and moyamoya syndrome in Ireland: patient demographics, mode of presentation and outcomes of EC-IC bypass surgery

Abstract

Background

There are no previously published reports regarding the epidemiology and characteristics of moyamoya disease or syndrome in Ireland.

Aims

To examine patient demographics, mode of presentation and the outcomes of extracranial-intracranial bypass surgery in the treatment of moyamoya disease and syndrome in Ireland.

Methods

All patients with moyamoya disease and syndrome referred to the National Neurosurgical Centre during January 2012–January 2019 were identified through a prospective database. Demographics, clinical presentation, radiological findings, surgical procedures, postoperative complications and any strokes during follow-up were recorded.

Results

Twenty-one patients were identified. Sixteen underwent surgery. Median age at diagnosis was 19 years. Fifteen were female. Mode of presentation was ischaemic stroke in nine, haemodynamic TIAs in eight, haemorrhage in three and incidental in one. Sixteen patients had Moyamoya disease, whereas five patients had moyamoya syndrome. Surgery was performed on 19 hemispheres in 16 patients. The surgical procedures consisted of ten direct (STA-MCA) bypasses, five indirect bypasses and four multiple burr holes. Postoperative complications included ischaemic stroke in one patient and subdural haematoma in one patient. The median follow-up period in the surgical group was 52 months; there was one new stroke during this period. Two patients required further revascularisation following recurrent TIAs. One patient died during follow-up secondary to tumour progression associated with neurofibromatosis type 1.

Conclusions

Moyamoya is rare but occurs in Caucasians in Ireland. It most commonly presents with ischaemic symptoms. Surgical intervention in the form of direct and indirect bypass is an effective treatment in the majority of cases.

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References

  1. 1.

    Takeuchi KS, K. (1957) Hypoplasia of bilateral internal carotid arteries. Brain Nerve 9:37–43

    Google Scholar 

  2. 2.

    Suzuki J, Takaku A (1969) Cerebrovascular “moyamoya” disease. Disease showing abnormal net-like vessels in base of brain. Arch Neurol 20(3):288–299

    CAS  Article  Google Scholar 

  3. 3.

    Wakai K, Tamakoshi A, Ikezaki K, Fukui M, Kawamura T, Aoki R, Kojima M, Lin Y, Ohno Y (1997) Epidemiological features of moyamoya disease in Japan: findings from a nationwide survey. Clin Neurol Neurosurg 99(Suppl 2):S1–S5

    Article  Google Scholar 

  4. 4.

    Baba T, Houkin K, Kuroda S (2008) Novel epidemiological features of moyamoya disease. J Neurol Neurosurg Psychiatry 79(8):900–904. https://doi.org/10.1136/jnnp.2007.130666

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  5. 5.

    Scott RM, Smith ER (2009) Moyamoya disease and moyamoya syndrome. N Engl J Med 360(12):1226–1237. https://doi.org/10.1056/NEJMra0804622

    CAS  Article  PubMed  Google Scholar 

  6. 6.

    Acker G, Goerdes S, Schmiedek P, Czabanka M, Vajkoczy P (2016) Characterization of clinical and radiological features of quasi-moyamoya disease among European Caucasians including surgical treatment and outcome. Cerebrovasc Dis 42(5–6):464–475. https://doi.org/10.1159/000448812

    Article  PubMed  Google Scholar 

  7. 7.

    Huang S, Guo ZN, Shi M, Yang Y, Rao M (2017) Etiology and pathogenesis of Moyamoya Disease: an update on disease prevalence. Int J Stroke 12(3):246–253. https://doi.org/10.1177/1747493017694393

    Article  PubMed  Google Scholar 

  8. 8.

    Kamada F, Aoki Y, Narisawa A, Abe Y, Komatsuzaki S, Kikuchi A, Kanno J, Niihori T, Ono M, Ishii N, Owada Y, Fujimura M, Mashimo Y, Suzuki Y, Hata A, Tsuchiya S, Tominaga T, Matsubara Y, Kure S (2011) A genome-wide association study identifies RNF213 as the first Moyamoya disease gene. J Hum Genet 56(1):34–40. https://doi.org/10.1038/jhg.2010.132

    CAS  Article  PubMed  Google Scholar 

  9. 9.

    Cho WS, Chung YS, Kim JE, Jeon JP, Son YJ, Bang JS, Kang HS, Sohn CH, Oh CW (2015) The natural clinical course of hemodynamically stable adult moyamoya disease. J Neurosurg 122(1):82–89. https://doi.org/10.3171/2014.9.jns132281

    Article  PubMed  Google Scholar 

  10. 10.

    Gross BA, Du R (2013) The natural history of moyamoya in a North American adult cohort. J Clin Neurosci 20(1):44–48. https://doi.org/10.1016/j.jocn.2012.08.002

    Article  PubMed  Google Scholar 

  11. 11.

    Kang S, Liu X, Zhang D, Wang R, Zhang Y, Zhang Q, Yang W, Zhao JZ (2019) Natural course of moyamoya disease in patients with prior hemorrhagic stroke. Stroke 50(5):1060–1066. https://doi.org/10.1161/strokeaha.118.022771

    Article  PubMed  Google Scholar 

  12. 12.

    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(5):245–266

    Article  Google Scholar 

  13. 13.

    Bang JS, Kwon OK, Kim JE, Kang HS, Park H, Cho SY, Oh CW (2012) Quantitative angiographic comparison with the OSIRIS program between the direct and indirect revascularization modalities in adult moyamoya disease. Neurosurgery 70(3):625–632; discussion 632-623. https://doi.org/10.1227/NEU.0b013e3182333c47

    Article  PubMed  Google Scholar 

  14. 14.

    Jiang H, Ni W, Xu B, Lei Y, Tian Y, Xu F, Gu Y, Mao Y (2014) Outcome in adult patients with hemorrhagic moyamoya disease after combined extracranial-intracranial bypass. J Neurosurg 121(5):1048–1055. https://doi.org/10.3171/2014.7.jns132434

    Article  PubMed  Google Scholar 

  15. 15.

    Kim T, Oh CW, Kwon OK, Hwang G, Kim JE, Kang HS, Cho WS, Bang JS (2016) Stroke prevention by direct revascularization for patients with adult-onset moyamoya disease presenting with ischemia. J Neurosurg 124(6):1788–1793. https://doi.org/10.3171/2015.6.jns151105

    Article  PubMed  Google Scholar 

  16. 16.

    Kuroda S, Houkin K, Ishikawa T, Nakayama N, Iwasaki Y (2010) Novel bypass surgery for moyamoya disease using pericranial flap: its impacts on cerebral hemodynamics and long-term outcome. Neurosurgery 66(6):1093–1101; discussion 1101. https://doi.org/10.1227/01.neu.0000369606.00861.91

    Article  PubMed  Google Scholar 

  17. 17.

    Miyamoto S, Yoshimoto T, Hashimoto N, Okada Y, Tsuji I, Tominaga T, Nakagawara J, Takahashi JC (2014) Effects of extracranial-intracranial bypass for patients with hemorrhagic moyamoya disease: results of the Japan Adult Moyamoya trial. Stroke 45(5):1415–1421. https://doi.org/10.1161/strokeaha.113.004386

    Article  PubMed  Google Scholar 

  18. 18.

    Hong JM, Lee SJ, Lee JS, Choi MH, Lee SE, Choi JW, Lim YC (2018) Feasibility of multiple burr hole with erythropoietin in acute moyamoya patients. Stroke 49(5):1290–1295. https://doi.org/10.1161/strokeaha.117.020566

    CAS  Article  PubMed  Google Scholar 

  19. 19.

    Cho WS, Kim JE, Kim CH, Ban SP, Kang HS, Son YJ, Bang JS, Sohn CH, Paeng JC, Oh CW (2014) Long-term outcomes after combined revascularization surgery in adult moyamoya disease. Stroke 45(10):3025–3031. https://doi.org/10.1161/strokeaha.114.005624

    Article  PubMed  Google Scholar 

  20. 20.

    Bao XY, Duan L, Yang WZ, Li DS, Sun WJ, Zhang ZS, Zong R, Han C (2015) Clinical features, surgical treatment, and long-term outcome in pediatric patients with moyamoya disease in China. Cerebrovasc Dis 39(2):75–81. https://doi.org/10.1159/000369524

    Article  PubMed  Google Scholar 

  21. 21.

    Central Statistics Office (2019) StatBank Census Populations. Central Statistics Office. https://statbank.cso.ie/px/pxeirestat/Statire/SelectVarVal/Define.asp?Maintable=EY029&Planguage=0. Accessed 13/01/19

  22. 22.

    Central Statistics Office (2019) StatBank Estimated Populations. Central Statistics Office. https://statbank.cso.ie/px/pxeirestat/Statire/SelectVarVal/Define.asp?maintable=PEA21&PLanguage=0. Accessed 13/01/19

  23. 23.

    Donaghy R (1967) Patch and bypass in microangeional surgery. Microvascular Surgery St Louis: CV Mosby:75–86

  24. 24.

    Yasargil MG (1969) Anastomosis between the superficial temporal artery and a branch of the middle cerebral artery. Microsurg Appl Neurosurg:105–115

  25. 25.

    Chang S, G. S (2000) Superficial temporal artery to middle cerebral artery anastomosis. Tech Neurosurg 6 (2):86–100

  26. 26.

    Karasawa J, Kikuchi H, Furuse S, Sakaki T, Yoshida Y (1977) A surgical treatment of “moyamoya” disease “encephalo-myo synangiosis”. Neurol Med Chir (Tokyo) 17(1 Pt 1):29–37

    CAS  Article  Google Scholar 

  27. 27.

    Kinugasa K, Mandai S, Kamata I, Sugiu K, Ohmoto T (1993) Surgical treatment of moyamoya disease: operative technique for encephalo-duro-arterio-myo-synangiosis, its follow-up, clinical results, and angiograms. Neurosurgery 32(4):527–531

    CAS  Article  Google Scholar 

  28. 28.

    Sainte-Rose C, Oliveira R, Puget S, Beni-Adani L, Boddaert N, Thorne J, Wray A, Zerah M, Bourgeois M (2006) Multiple bur hole surgery for the treatment of moyamoya disease in children. J Neurosurg 105(6 Suppl):437–443. https://doi.org/10.3171/ped.2006.105.6.437

    Article  PubMed  Google Scholar 

  29. 29.

    Matsushima Y, Fukai N, Tanaka K, Tsuruoka S, Inaba Y, Aoyagi M, Ohno K (1981) A new surgical treatment of moyamoya disease in children: a preliminary report. Surg Neurol 15(4):313–320

    CAS  Article  Google Scholar 

  30. 30.

    Takahashi JC, Miyamoto S (2010) Moyamoya disease: recent progress and outlook. Neurol Med Chir (Tokyo) 50(9):824–832

    Article  Google Scholar 

  31. 31.

    Hever P, Alamri A, Tolias C (2015) Moyamoya angiopathy - is there a Western phenotype? Br J Neurosurg 29(6):765–771. https://doi.org/10.3109/02688697.2015.1096902

    Article  PubMed  Google Scholar 

  32. 32.

    Hori S, Kashiwazaki D, Yamamoto S, Acker G, Czabanka M, Akioka N, Kuwayama N, Vajkoczy P, Kuroda S (2018) Impact of interethnic difference of collateral angioarchitectures on prevalence of hemorrhagic stroke in moyamoya disease. Neurosurgery. 85:134–146. https://doi.org/10.1093/neuros/nyy236

    Article  Google Scholar 

  33. 33.

    Yamamoto S, Hori S, Kashiwazaki D, Akioka N, Kuwayama N, Kuroda S (2018) Longitudinal anterior-to-posterior shift of collateral channels in patients with moyamoya disease: an implication for its hemorrhagic onset. J Neurosurg:1–7. https://doi.org/10.3171/2017.9.jns172231

  34. 34.

    Kuriyama S, Kusaka Y, Fujimura M, Wakai K, Tamakoshi A, Hashimoto S, Tsuji I, Inaba Y, Yoshimoto T (2008) Prevalence and clinicoepidemiological features of moyamoya disease in Japan: findings from a nationwide epidemiological survey. Stroke 39(1):42–47. https://doi.org/10.1161/strokeaha.107.490714

    Article  PubMed  Google Scholar 

  35. 35.

    Goto Y, Yonekawa Y (1992) Worldwide distribution of moyamoya disease. Neurol Med Chir (Tokyo) 32(12):883–886

    CAS  Article  Google Scholar 

  36. 36.

    Acker G, Goerdes S, Schneider UC, Schmiedek P, Czabanka M, Vajkoczy P (2015) Distinct clinical and radiographic characteristics of moyamoya disease amongst European Caucasians. Eur J Neurol 22(6):1012–1017. https://doi.org/10.1111/ene.12702 Epub 2015 Apr 6

    CAS  Article  PubMed  Google Scholar 

  37. 37.

    Kraemer M, Heienbrok W, Berlit P (2008) Moyamoya disease in Europeans. Stroke 39(12):3193–3200. https://doi.org/10.1161/strokeaha.107.513408

    Article  PubMed  Google Scholar 

  38. 38.

    Saarela M, Mustanoja S, Pekkola J, Tyni T, Hernesniemi J, Kivipelto L, Tatlisumak T (2017) Moyamoya vasculopathy - patient demographics and characteristics in the Finnish population. Int J Stroke 12(1):90–95. https://doi.org/10.1177/1747493016669847

    Article  PubMed  Google Scholar 

  39. 39.

    Khan N, Schuknecht B, Boltshauser E, Capone A, Buck A, Imhof HG, Yonekawa Y (2003) Moyamoya disease and Moyamoya syndrome: experience in Europe; choice of revascularisation procedures. Acta Neurochir 145(12):1061–1071; discussion 1071. https://doi.org/10.1007/s00701-003-0148-5

    CAS  Article  PubMed  Google Scholar 

  40. 40.

    Liu J. ZW, Wang W. (2010) Moyamoya disease in China. In: Cho BK. TT (ed) Moyamoya disease update. Springer, Tokyo, pp 370–373. https://doi.org/10.1007/978-4-431-99703-0_51

  41. 41.

    Birkeland P, Lauritsen J (2018) Incidence of moyamoya disease in Denmark: a population-based register study. Acta Neurochir Suppl 129:91–93. https://doi.org/10.1007/978-3-319-73739-3_13

    Article  PubMed  Google Scholar 

  42. 42.

    Kleinloog R, Regli L, Rinkel GJ, Klijn CJ (2012) Regional differences in incidence and patient characteristics of moyamoya disease: a systematic review. J Neurol Neurosurg Psychiatry 83(5):531–536. https://doi.org/10.1136/jnnp-2011-301387

    Article  PubMed  Google Scholar 

  43. 43.

    Han DH, Kwon OK, Byun BJ, Choi BY, Choi CW, Choi JU, Choi SG, Doh JO, Han JW, Jung S, Kang SD, Kim DJ, Kim HI, Kim HD, Kim MC, Kim SC, Kim Y, Kwun BD, Lee BG, Lim YJ, Moon JG, Park HS, Shin MS, Song JH, Suk JS, Yim MB (2000) A co-operative study: clinical characteristics of 334 Korean patients with moyamoya disease treated at neurosurgical institutes (1976-1994). The Korean Society for Cerebrovascular Disease. Acta Neurochir 142(11):1263–1273 discussion 1273-1264

    CAS  Article  Google Scholar 

  44. 44.

    Ikezaki K, Han DH, Kawano T, Kinukawa N, Fukui M (1997) A clinical comparison of definite moyamoya disease between South Korea and Japan. Stroke 28(12):2513–2517

    CAS  Article  Google Scholar 

  45. 45.

    Gross BA, Du R (2013) Adult moyamoya after revascularization. Acta Neurochir 155(2):247–254. https://doi.org/10.1007/s00701-012-1545-4

    Article  PubMed  Google Scholar 

  46. 46.

    Oliveira RS, Amato MC, Simao GN, Abud DG, Avidago EB, Specian CM, Machado HR (2009) Effect of multiple cranial burr hole surgery on prevention of recurrent ischemic attacks in children with moyamoya disease. Neuropediatrics 40(6):260–264. https://doi.org/10.1055/s-0030-1249069

    Article  PubMed  Google Scholar 

  47. 47.

    Funaki T, Takahashi JC, Takagi Y, Yoshida K, Araki Y, Kikuchi T, Kataoka H, Iihara K, Sano N, Miyamoto S (2014) Incidence of late cerebrovascular events after direct bypass among children with moyamoya disease: a descriptive longitudinal study at a single center. Acta Neurochir 156(3):551–559; discussion 559. https://doi.org/10.1007/s00701-013-1975-7

    Article  PubMed  Google Scholar 

  48. 48.

    Kalani MY, Rangel-Castilla L, Ramey W, Nakaji P, Albuquerque FC, McDougall CG, Spetzler RF, Zabramski JM (2015) Indications and results of direct cerebral revascularization in the modern era. World Neurosurg 83(3):345–350. https://doi.org/10.1016/j.wneu.2014.10.013

    Article  PubMed  Google Scholar 

  49. 49.

    Thines L, Petyt G, Aguettaz P, Bodenant M, Himpens FX, Lenci H, Henon H, Gauthier C, Hossein-Foucher C, Cordonnier C, Lejeune JP (2015) Surgical management of Moyamoya disease and syndrome: current concepts and personal experience. Rev Neurol (Paris) 171(1):31–44. https://doi.org/10.1016/j.neurol.2014.08.007

    CAS  Article  Google Scholar 

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Acknowledgments

The authors would like to thank Ms. Deirdre Nolan and Ms. Paula Corr from the audit and research department, Beaumont Hospital, for helping with chart reviews and data collection.

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Correspondence to Mohsen Javadpour.

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Conflict of interest

DJH McCabe’s research group has received grant funding from the Trinity College Dublin Innovation Bursary, the Meath Foundation, Ireland, The Vascular Neurology Research Foundation, Ireland and an unrestricted educational grant from SINNOWA Medical Science & Technology Co., China. None of the above charities or funding bodies had any influence on the conduct of this study, or had any influence on the decision to submit the final manuscript for publication.

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This study was approved by the institutional audit board of Beaumont Hospital, Dublin, Ireland.

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Doherty, R.J., Caird, J., Crimmins, D. et al. Moyamoya disease and moyamoya syndrome in Ireland: patient demographics, mode of presentation and outcomes of EC-IC bypass surgery. Ir J Med Sci (2020). https://doi.org/10.1007/s11845-020-02280-w

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Keywords

  • Extracranial-intracranial bypass
  • Incidence
  • Moyamoya disease
  • Moyamoya syndrome
  • Prevalence
  • Revascularisation