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Surgical Treatment of Adult Moyamoya Disease

  • Cerebrovascular Disorders (DG Jamieson, Section Editor)
  • Published:
Current Treatment Options in Neurology Aims and scope Submit manuscript

Abstract

Purpose of review

Moyamoya disease (MMD) is being increasingly diagnosed with the development of radiological surveillance technology and increased accessibility to medical care. Accordingly, there have been several recent reports on treatment outcomes in MMD. In this review, we summarize recent advances in surgical treatment and outcomes of adult MMD, while addressing related controversies.

Recent findings

Recent studies suggest that revascularization surgery leads to significantly more favorable outcomes for stroke prevention, angiographic and hemodynamic changes, and clinical outcomes than does conservative treatment for adult patients with ischemic MMD. Moreover, direct revascularization methods should be considered as the first-line treatment over indirect methods, although the latter may be considered if a direct method is not possible. In cases of hemorrhagic MMD, several studies have demonstrated that surgical treatment is more effective than conservative treatment in preventing further hemorrhage. In addition to revascularization surgery, endovascular treatment is emerging as a breakthrough therapy for hemorrhagic MMD.

Summary

Accumulating evidence regarding the surgical treatment of adult MMD suggests the benefit of revascularization over conservative management for both ischemic and hemorrhagic patients. However, the benefit of revascularization in asymptomatic adult MMD remains unclear.

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  1. • Kim T, Lee H, Bang JS, Kwon OK, Hwang G, Oh CW. Epidemiology of Moyamoya Disease in Korea: Based on National Health Insurance Service Data. J Korean Neurosurg Soc. 2015;57(6):390–5. This report provides the latest epidemiologic features of MMD in Korea, as well as literature review concerning previous worldwide reports.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  2. Kim JS. Moyamoya disease: epidemiology, clinical features, and diagnosis. J Stroke. 2016;18(1):2–11.

    Article  PubMed  PubMed Central  Google Scholar 

  3. Chen PC, Yang SH, Chien KL, Tsai IJ, Kuo MF. Epidemiology of moyamoya disease in Taiwan: a nationwide population-based study. Stroke. 2014;45(5):1258–63.

    Article  PubMed  Google Scholar 

  4. Uchino K, Johnston SC, Becker KJ, Tirschwell DL. Moyamoya disease in Washington State and California. Neurology. 2005;65(6):956–8.

    Article  PubMed  Google Scholar 

  5. Yonekawa Y, Ogata N, Kaku Y, Taub E, Imhof HG. Moyamoya disease in Europe, past and present status. Clin Neurol Neurosurg. 1997;99(2):S58–60.

    Article  PubMed  Google Scholar 

  6. Phi JH, Wang KC, Lee JY, Kim SK. Moyamoya syndrome: a window of moyamoya disease. J Korean Neurosurg Soc. 2015;57(6): 408-14.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  7. Tho-Calvi SC, Thompson D, Saunders D, Agrawal S, Basu A, Chitre M, et al. Clinical features, course, and outcomes of a UK cohort of pediatric moyamoya. Neurology. 2018;90(9):e763–e70.

    Article  PubMed  Google Scholar 

  8. Lee S, Rivkin MJ, Kirton A, DeVeber G, Elbers J. International Pediatric Stroke S. Moyamoya Disease in Children: results From the International Pediatric Stroke Study. J Child Neurol. 2017;32(11):924–9.

    Article  PubMed  Google Scholar 

  9. Scott RM, Smith JL, Robertson RL, Madsen JR, Soriano SG, Rockoff MA. Long-term outcome in children with moyamoya syndrome after cranial revascularization by pial synangiosis. J Neurosurg. 2004;100(2 Suppl Pediatrics):142–9.

    PubMed  Google Scholar 

  10. Bang OY, Fujimura M, Kim SK. The pathophysiology of moyamoya disease: an update. J Stroke. 2016;18(1):12–20.

    Article  PubMed  PubMed Central  Google Scholar 

  11. Funaki T, Takahashi JC, Yoshida K, Takagi Y, Fushimi Y, Kikuchi T, et al. Periventricular anastomosis in moyamoya disease: detecting fragile collateral vessels with MR angiography. J Neurosurg. 2016;124(6):1766–72.

    Article  PubMed  Google Scholar 

  12. Ge P, Zhang Q, Ye X, Wang S, Zhang D, Zhao J. Clinical Features, surgical treatment, and long-term outcome in children with hemorrhagic moyamoya disease. J Stroke Cerebrovasc Dis. 2018.

  13. Liu P, Han C, Li DS, Lv XL, Li YX, Duan L. Hemorrhagic moyamoya disease in children: clinical, angiographic features, and long-term surgical outcome. Stroke. 2016;47(1):240–3.

    Article  PubMed  Google Scholar 

  14. Jang DK, Lee KS, Rha HK, Huh PW, Yang JH, Park IS, et al. Bypass surgery versus medical treatment for symptomatic moyamoya disease in adults. J Neurosurg. 2017;127(3):492–502.

    Article  PubMed  Google Scholar 

  15. • Deng X, Gao F, Zhang D, Zhang Y, Wang R, Wang S, et al. Effects of different surgical modalities on the clinical outcome of patients with moyamoya disease: a prospective cohort study. J Neurosurg. 2017:1–11. This large-scaled prospective study reports that direct revascularization is more effective for preventing ischemic stroke than indirect revascularization, while there is no difference for preventing recurrent hemorrhage.

  16. Hallemeier CL, Rich KM, Grubb RL Jr, Chicoine MR, Moran CJ, Cross DT 3rd, et al. Clinical features and outcome in North American adults with moyamoya phenomenon. Stroke. 2006;37(6):1490–6.

    Article  PubMed  Google Scholar 

  17. Ikezaki K, Han DH, Kawano T, Kinukawa N, Fukui M. A clinical comparison of definite moyamoya disease between South Korea and Japan. Stroke. 1997;28(12):2513–7.

    Article  PubMed  CAS  Google Scholar 

  18. Kim T, Oh CW, Bang JS, Kim JE, Cho WS. Moyamoya disease: treatment and outcomes. J Stroke. 2016;18(1):21–30.

    Article  PubMed  PubMed Central  Google Scholar 

  19. Cho WS, Lee HY, Kang HS, Kim JE, Bang JS, Oh CW. Symptomatic cerebral hyperperfusion on SPECT after indirect revascularization surgery for Moyamoya disease. Clin Nucl Med. 2013;38(1):44–6.

    Article  PubMed  Google Scholar 

  20. Kim CY, Wang KC, Kim SK, Chung YN, Kim HS, Cho BK. Encephaloduroarteriosynangiosis with bifrontal encephalogaleo(periosteal)synangiosis in the pediatric moyamoya disease: the surgical technique and its outcomes. Childs Nerv Syst. 2003;19(5–6):316–24.

    Article  PubMed  Google Scholar 

  21. Kim SK, Wang KC, Kim IO, Lee DS, Cho BK. Combined encephaloduroarteriosynangiosis and bifrontal encephalogaleo (periosteal) synangiosis in pediatric moyamoya disease. Neurosurgery. 2008;62(6 Suppl 3):1456–64.

    PubMed  Google Scholar 

  22. Lee JY, Kim SK, Phi JH, Wang KC. Posterior Cerebral Artery Insufficiency in Pediatric Moyamoya Disease. J Korean Neurosurg Soc. 2015;57(6):436–9.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  23. Matsushima T, Fukui M, Kitamura K, Hasuo K, Kuwabara Y, Kurokawa T. Encephalo-duro-arterio-synangiosis in children with moyamoya disease. Acta Neurochir (Wien). 1990;104(3–4):96–102.

    Article  CAS  Google Scholar 

  24. Kim T, Bang JS, Kwon OK, Hwang G, Kim JE, Kang HS, et al. Hemodynamic changes after unilateral revascularization for moyamoya disease: serial assessment by quantitative magnetic resonance angiography. Neurosurgery. 2017;81(1):111–9.

    Article  PubMed  Google Scholar 

  25. Czabanka M, Pena-Tapia P, Scharf J, Schubert GA, Munch E, Horn P, et al. Characterization of direct and indirect cerebral revascularization for the treatment of European patients with moyamoya disease. Cerebrovasc Dis. 2011;32(4):361–9.

    Article  PubMed  CAS  Google Scholar 

  26. Cho WS, Kim JE, Kim CH, Ban SP, Kang HS, Son YJ, et al. Long-term outcomes after combined revascularization surgery in adult moyamoya disease. Stroke. 2014;45(10):3025–31.

    Article  PubMed  Google Scholar 

  27. • Kim T, Oh CW, Kwon OK, Hwang G, Kim JE, Kang HS, et al. Stroke prevention by direct revascularization for patients with adult-onset moyamoya disease presenting with ischemia. J Neurosurg. 2016;124(6):1788–93. This article reports the effectiveness of direct revascularization for preventing further stroke of ischemic presenting adult MMD patients.

    Article  PubMed  Google Scholar 

  28. •• Jeon JP, Kim JE, Cho WS, Bang JS, Son YJ, Oh CW. Meta-analysis of the surgical outcomes of symptomatic moyamoya disease in adults. J Neurosurg. 2017:1–7. This meta-analysis covers recent literatures regarding surgical outcomes of symptomatic adult MMD in the context of the benefit of revascularization over conservative treatment.

  29. Kim DS, Huh PW, Kim HS, Kim IS, Choi S, Mok JH, et al. Surgical treatment of moyamoya disease in adults: combined direct and indirect vs. indirect bypass surgery. Neurol Med Chir (Tokyo). 2012;52(5):333–8.

    Article  Google Scholar 

  30. Ge P, Zhang Q, Ye X, Liu X, Deng X, Li H, et al. Long-term outcome after conservative treatment and direct bypass surgery of moyamoya disease at late suzuki stage. World Neurosurg. 2017;103:283–90.

    Article  PubMed  Google Scholar 

  31. Luo R, Gao F, Deng X, Zhang D, Zhang Y. Results of conservative follow-up or surgical treatment of moyamoya patients who present without hemorrhage, transient ischemic attack, or stroke. World Neurosurg. 2017;108:683–9.

    Article  PubMed  Google Scholar 

  32. Cho WS, Chung YS, Kim JE, Jeon JP, Son YJ, Bang JS, et al. The natural clinical course of hemodynamically stable adult moyamoya disease. J Neurosurg. 2015;122(1):82–9.

    Article  PubMed  Google Scholar 

  33. Noh HJ, Kim SJ, Kim JS, Hong SC, Kim KH, Jun P, et al. Long term outcome and predictors of ischemic stroke recurrence in adult moyamoya disease. J Neurol Sci. 2015;359(1–2):381–8.

    Article  PubMed  Google Scholar 

  34. Deng X, Gao F, Zhang D, Zhang Y, Wang R, Wang S, et al. Direct versus indirect bypasses for adult ischemic-type moyamoya disease: a propensity score-matched analysis. J Neurosurg. 2017:1–7.

  35. Arias EJ, Dunn GP, Washington CW, Derdeyn CP, Chicoine MR, Grubb RL Jr, et al. Surgical revascularization in north american adults with moyamoya phenomenon: long-term angiographic follow-up. J Stroke Cerebrovasc Dis. 2015;24(7):1597–608.

    Article  PubMed  PubMed Central  Google Scholar 

  36. Kim KM, Kim JE, Cho WS, Kang HS, Son YJ, Han MH, et al. Natural history and risk factor of recurrent hemorrhage in hemorrhagic adult moyamoya disease. Neurosurgery. 2017;81(2):289–96.

    Article  PubMed  Google Scholar 

  37. •• Kim H, Jang DK, Han YM, Sung JH, Park IS, Lee KS, et al. Direct bypass versus indirect bypass in adult moyamoya angiopathy with symptoms or hemodynamic instability: a meta-analysis of comparative studies. World Neurosurg. 2016;94:273–84. This meta-analysis covers literatures to compare the effectiveness between direct and indirect revascualrization in terms of stroke prevention, angiographic, and hemodynamic outcomes.

    Article  PubMed  Google Scholar 

  38. Fujii K, Ikezaki K, Irikura K, Miyasaka Y, Fukui M. The efficacy of bypass surgery for the patients with hemorrhagic moyamoya disease. Clin Neurol Neurosurg. 1997;99(2):S194–5.

    Article  PubMed  Google Scholar 

  39. Yoshida Y, Yoshimoto T, Shirane R, Sakurai Y. Clinical course, surgical management, and long-term outcome of moyamoya patients with rebleeding after an episode of intracerebral hemorrhage: an extensive follow-Up study. Stroke. 1999;30(11):2272–6.

    Article  PubMed  CAS  Google Scholar 

  40. Yamada S, Oki K, Itoh Y, Kuroda S, Houkin K, Tominaga T, et al. Effects of surgery and antiplatelet therapy in ten-year follow-up from the Registry Study of Research Committee on Moyamoya Disease in Japan. J Stroke Cerebrovasc Dis. 2016;25(2):340–9.

    Article  PubMed  Google Scholar 

  41. Jiang H, Ni W, Xu B, Lei Y, Tian Y, Xu F, et al. Outcome in adult patients with hemorrhagic moyamoya disease after combined extracranial-intracranial bypass. J Neurosurg. 2014;121(5):1048–55.

    Article  PubMed  Google Scholar 

  42. •• Miyamoto S, Yoshimoto T, Hashimoto N, Okada Y, Tsuji I, Tominaga T, et al. Effects of extracranial-intracranial bypass for patients with hemorrhagic moyamoya disease: results of the Japan Adult Moyamoya Trial. Stroke. 2014;45(5):1415–21. This randomized controlled trial is a milestone work elucidating the effectiveness of direct revascularization for preventing recurrent hemorrhage of hemorrhagic MMD patients.

    Article  PubMed  Google Scholar 

  43. Kuroda S, Hashimoto N, Yoshimoto T, Iwasaki Y. Research Committee on Moyamoya Disease in J. Radiological findings, clinical course, and outcome in asymptomatic moyamoya disease: results of multicenter survey in Japan. Stroke. 2007;38(5):1430–5.

    Article  PubMed  Google Scholar 

  44. Kuroda S, Ishikawa T, Houkin K, Nanba R, Hokari M, Iwasaki Y. Incidence and clinical features of disease progression in adult moyamoya disease. Stroke. 2005;36(10):2148–53.

    Article  PubMed  Google Scholar 

  45. Lee SB, Kim DS, Huh PW, Yoo DS, Lee TG, Cho KS. Long-term follow-up results in 142 adult patients with moyamoya disease according to management modality. Acta Neurochir (Wien). 2012;154(7):1179–87.

    Article  Google Scholar 

  46. Huang Z, Ding X, Men W, Zhang D, Zhao Y, Wang R, et al. Clinical features and outcomes in 154 patients with haemorrhagic moyamoya disease: comparison of conservative treatment and surgical revascularization. Neurol Res. 2015;37(10):886–92.

    Article  PubMed  Google Scholar 

  47. Kobayashi E, Saeki N, Oishi H, Hirai S, Yamaura A. Long-term natural history of hemorrhagic moyamoya disease in 42 patients. J Neurosurg. 2000;93(6):976–80.

    Article  PubMed  CAS  Google Scholar 

  48. Morioka M, Hamada J, Todaka T, Yano S, Kai Y, Ushio Y. High-risk age for rebleeding in patients with hemorrhagic moyamoya disease: long-term follow-up study. Neurosurgery. 2003;52(5):1049–54.

    PubMed  Google Scholar 

  49. Jo KI, Yeon JY, Hong SC, Kim JS. Clinical course of asymptomatic adult moyamoya disease. Cerebrovasc Dis. 2014;37(2):94–101.

    Article  PubMed  Google Scholar 

  50. Koss M, Scott RM, Irons MB, Smith ER, Ullrich NJ. Moyamoya syndrome associated with neurofibromatosis Type 1: perioperative and long-term outcome after surgical revascularization. J Neurosurg Pediatr. 2013;11(4):417–25.

    Article  PubMed  Google Scholar 

  51. Jea A, Smith ER, Robertson R, Scott RM. Moyamoya syndrome associated with Down syndrome: outcome after surgical revascularization. Pediatrics. 2005;116(5):e694–701.

    Article  PubMed  Google Scholar 

  52. Abla AA, Gandhoke G, Clark JC, Oppenlander ME, Velat GJ, Zabramski JM, et al. Surgical outcomes for moyamoya angiopathy at barrow neurological institute with comparison of adult indirect encephaloduroarteriosynangiosis bypass, adult direct superficial temporal artery-to-middle cerebral artery bypass, and pediatric bypass: 154 revascularization surgeries in 140 affected hemispheres. Neurosurgery. 2013;73(3):430–9.

    Article  PubMed  Google Scholar 

  53. Bang JS, Kwon OK, Kim JE, Kang HS, Park H, Cho SY, et al. Quantitative angiographic comparison with the OSIRIS program between the direct and indirect revascularization modalities in adult moyamoya disease. Neurosurgery. 2012;70(3):625–32.

    Article  PubMed  Google Scholar 

  54. Bao XY, Duan L, Li DS, Yang WZ, Sun WJ, Zhang ZS, et al. Clinical features, surgical treatment and long-term outcome in adult patients with Moyamoya disease in China. Cerebrovasc Dis. 2012;34(4):305–13.

    Article  PubMed  Google Scholar 

  55. Gross BA, Du R. Adult moyamoya after revascularization. Acta Neurochir (Wien). 2013;155(2):247–54.

    Article  Google Scholar 

  56. Hyun SJ, Kim JS, Hong SC. Prognostic factors associated with perioperative ischemic complications in adult-onset moyamoya disease. Acta Neurochir (Wien). 2010;152(7):1181–8.

    Article  Google Scholar 

  57. Sun H, Wilson C, Ozpinar A, Safavi-Abbasi S, Zhao Y, Nakaji P, et al. Perioperative complications and long-term outcomes after bypasses in adults with moyamoya disease: a systematic review and meta-analysis. World Neurosurg. 2016;92:179–88.

    Article  PubMed  Google Scholar 

  58. Fujimura M, Kaneta T, Mugikura S, Shimizu H, Tominaga T. Temporary neurologic deterioration due to cerebral hyperperfusion after superficial temporal artery-middle cerebral artery anastomosis in patients with adult-onset moyamoya disease. Surg Neurol. 2007;67(3):273–82.

    Article  PubMed  Google Scholar 

  59. Fujimura M, Shimizu H, Inoue T, Mugikura S, Saito A, Tominaga T. Significance of focal cerebral hyperperfusion as a cause of transient neurologic deterioration after extracranial-intracranial bypass for moyamoya disease: comparative study with non-moyamoya patients using N-isopropyl-p-[(123)I]iodoamphetamine single-photon emission computed tomography. Neurosurgery. 2011;68(4):957–64.

    Article  PubMed  Google Scholar 

  60. Kim JE, Oh CW, Kwon OK, Park SQ, Kim SE, Kim YK. Transient hyperperfusion after superficial temporal artery/middle cerebral artery bypass surgery as a possible cause of postoperative transient neurological deterioration. Cerebrovasc Dis. 2008;25(6):580–6.

    Article  PubMed  Google Scholar 

  61. Uchino H, Kuroda S, Hirata K, Shiga T, Houkin K, Tamaki N. Predictors and clinical features of postoperative hyperperfusion after surgical revascularization for moyamoya disease: a serial single photon emission CT/positron emission tomography study. Stroke. 2012;43(10):2610–6.

    Article  PubMed  Google Scholar 

  62. Zhao WG, Luo Q, Jia JB, Yu JL. Cerebral hyperperfusion syndrome after revascularization surgery in patients with moyamoya disease. Br J Neurosurg. 2013;27(3):321–5.

    Article  PubMed  Google Scholar 

  63. Hayashi K, Horie N, Suyama K, Nagata I. Incidence and clinical features of symptomatic cerebral hyperperfusion syndrome after vascular reconstruction. World Neurosurg. 2012;78(5):447–54.

    Article  PubMed  Google Scholar 

  64. Khan N, Dodd R, Marks MP, Bell-Stephens T, Vavao J, Steinberg GK. Failure of primary percutaneous angioplasty and stenting in the prevention of ischemia in moyamoya angiopathy. Cerebrovasc Dis. 2011;31(2):147–53.

    Article  PubMed  Google Scholar 

  65. Kim T, Kwon OK, Oh CW, Bang JS, Hwang G, Lee YJ. Intracranial stenting using a drug-eluting stent for moyamoya disease involving supraclinoid ICA: a case report. Neurol Med Chir (Tokyo). 2014;54(2):136–8.

    Article  Google Scholar 

  66. Kim SH, Kwon OK, Jung CK, Kang HS, Oh CW, Han MH, et al. Endovascular treatment of ruptured aneurysms or pseudoaneurysms on the collateral vessels in patients with moyamoya disease. Neurosurgery. 2009;65(5):1000–4.

    Article  PubMed  Google Scholar 

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Lee, S.U., Oh, C.W., Kwon, OK. et al. Surgical Treatment of Adult Moyamoya Disease. Curr Treat Options Neurol 20, 22 (2018). https://doi.org/10.1007/s11940-018-0511-8

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