Pediatric Moyamoya Disease: Indirect Revascularization

  • Mario K. Teo
  • Jeremiah N. Johnson
  • Gary K. Steinberg


Moyamoya disease (MMD) is an idiopathic, chronic, occlusive cerebrovascular disease that involves bilateral stenosis or occlusion of the terminal internal carotid or proximal middle and anterior cerebral arteries. Development of basal collateral channels, including hypertrophy of the lenticulostriate and thalamoperforating arteries, results in characteristic “moyamoya vessels.” It is from the angiographic appearance of these vessels that the name moyamoya is derived, meaning “haziness” or “puff of smoke” in Japanese [1, 2]. Patients with moyamoya syndrome (MMS) present with identical clinical and angiographic features as those with MMD, but have an underlying associated condition, such as Down’s syndrome, neurofibromatosis, sickle cell disease, primordial dwarfism, or previous cranial irradiation [3].


Moyamoya disease Indirect bypass EDAS EMS EGPS Omental transposition 



Anterior cerebral artery


Cerebral blood flow


Common carotid artery


Cerebrovascular reserve capacity


Digital subtraction angiography

DWI + ve

Diffusion Weighted Image positive


External carotid artery














Internal carotid artery


Middle cerebral artery


Middle meningeal artery


Moyamoya disease


Moyamoya syndrome


Multiple burr holes


Magnetic resonance


Occipital artery


Posterior cerebral artery


Single photon emission computed tomography


Superficial temporal artery


Transient ischemia attack


Xenon-enhanced computed tomography


  1. 1.
    Suzuki J, Kodama N. Moyamoya disease--a review. Stroke. 1983;14(1):104–9.CrossRefPubMedGoogle Scholar
  2. 2.
    Chang SD, Steinberg GK. Superficial temporal artery to middle cerebral artery anastomosis. In: Steinberg GK, editor. Techniques in neurosurgery. Philadelphia: Lippincott Williams and Wilkins; 2000. p. 86–100.Google Scholar
  3. 3.
    Fukui M. Guidelines for the diagnosis and treatment of spontaneous occlusion of the circle of Willis (‘moyamoya’ disease). Research Committee on Spontaneous Occlusion of the Circle of Willis (Moyamoya Disease) of the Ministry of Health and Welfare, Japan. Clin Neurol Neurosurg. 1997;99 Suppl 2:S238–40.CrossRefPubMedGoogle Scholar
  4. 4.
    Kuriyama S, Kusaka Y, Fujimura M, Wakai K, Tamakoshi A, Hashimoto S, et al. Prevalence and clinicoepidemiological features of moyamoya disease in Japan: findings from a nationwide epidemiological survey. Stroke. 2008;39(1):42–7.CrossRefPubMedGoogle Scholar
  5. 5.
    Liu XJ, Zhang D, Wang S, Zhao YL, Teo M, Wang R, et al. Clinical features and long-term outcomes of moyamoya disease: a single-center experience with 528 cases in China. J Neurosurg. 2015;122(2):392–9.CrossRefPubMedGoogle Scholar
  6. 6.
    Scott RM, Smith ER. Moyamoya disease and moyamoya syndrome. N Engl J Med. 2009;360(12):1226–37.CrossRefPubMedGoogle Scholar
  7. 7.
    Cook DJ, Mukerji N, Furtado S, Steinberg GK: Moyamoya Disease. In: Lanzer P (ed) PanVascular Medicine, 2nd edition, Springer Heidelberg New York Dordrecht London, 2015, chapter 106, pp. 2944–2967.Google Scholar
  8. 8.
    Starke RM, Crowley RW, Maltenfort M, Jabbour PM, Gonzalez LF, Tjoumakaris SI, et al. Moyamoya disorder in the United States. Neurosurgery. 2012;71(1):93–9.CrossRefPubMedGoogle Scholar
  9. 9.
    Uchino K, Johnston SC, Becker KJ, Tirschwell DL. Moyamoya disease in Washington State and California. Neurology. 2005;65(6):956–8.CrossRefPubMedGoogle Scholar
  10. 10.
    Kossorotoff M, Herve D, Toulgoat F, Renaud C, Presles E, Chabriat H, et al. Paediatric moyamoya in mainland France: a comprehensive survey of academic neuropaediatric centres. Cerebrovasc Dis. 2012;33(1):76–9.CrossRefPubMedGoogle Scholar
  11. 11.
    Baba T, Houkin K, Kuroda S. Novel epidemiological features of moyamoya disease. J Neurol Neurosurg Psychiatry. 2008;79(8):900–4.CrossRefPubMedGoogle Scholar
  12. 12.
    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.PubMedGoogle Scholar
  13. 13.
    Khan N, Schuknecht B, Boltshauser E, Capone A, Buck A, Imhof HG, et al. Moyamoya disease and Moyamoya syndrome: experience in Europe; choice of revascularisation procedures. Acta Neurochir (Wien). 2003;145(12):1061–71.CrossRefGoogle Scholar
  14. 14.
    Sainte-Rose C, Oliveira R, Puget S, Beni-Adani L, Boddaert N, Thorne J, et al. Multiple bur hole surgery for the treatment of moyamoya disease in children. J Neurosurg. 2006;105(6 Suppl):437–43.PubMedGoogle Scholar
  15. 15.
    Kim SK, Wang KC, Kim IO, Lee DS, Cho BK. Combined encephaloduroarteriosynangiosis and bifrontal encephalogaleo(periosteal)synangiosis in pediatric moyamoya disease. Neurosurgery. 2002;50(1):88–96.PubMedGoogle Scholar
  16. 16.
    Han DH, Kwon OK, Byun BJ, Choi BY, Choi CW, Choi JU, et al. 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 (Wien). 2000;142(11):1263–74.CrossRefGoogle Scholar
  17. 17.
    Yonekawa Y, Kawano T. Follow-up study of 632 cases in spontaneous occlusion of the circle of Willis registered from 1983 to 1991. In: Yonekawa Y, editor. The Research Committee on Spontaneous Occlusion of the Circle of Willis (Moyamoya Disease) of the Ministry of Health and Welfare, Japan: Annual Report 1991. Osaka: National Cardiovascular Center; 1992. p. 41–7.Google Scholar
  18. 18.
    Olds MV, Griebel RW, Hoffman HJ, Craven M, Chuang S, Schutz H. The surgical treatment of childhood moyamoya disease. J Neurosurg. 1987;66(5):675–80.CrossRefPubMedGoogle Scholar
  19. 19.
    Kraemer M, Heienbrok W, Berlit P. Moyamoya disease in Europeans. Stroke. 2008;39(12):3193–200.CrossRefPubMedGoogle Scholar
  20. 20.
    Kim SK, Seol HJ, Cho BK, Hwang YS, Lee DS, Wang KC. Moyamoya disease among young patients: its aggressive clinical course and the role of active surgical treatment. Neurosurgery. 2004;54(4):840–6.CrossRefPubMedGoogle Scholar
  21. 21.
    Scott RM. Moyamoya syndrome: a surgically treatable cause of stroke in the pediatric patient. Clin Neurosurg. 2000;47:378–84.PubMedGoogle Scholar
  22. 22.
    Scott RM. Surgery for moyamoya syndrome? Yes. Arch Neurol. 2001;58(1):128–9.CrossRefPubMedGoogle Scholar
  23. 23.
    Karasawa J, Kikuchi H, Furuse S, Sakaki T, Yoshida Y. A surgical treatment of “moyamoya” disease “encephalo-myo synangiosis”. Neurol Med Chir (Tokyo). 1977;17(1):29–37.CrossRefGoogle Scholar
  24. 24.
    Irikura K, Miyasaka Y, Kurata A, Tanaka R, Yamada M, Kan S, et al. The effect of encephalo-myo-synangiosis on abnormal collateral vessels in childhood moyamoya disease. Neurol Res. 2000;22(4):341–6.CrossRefPubMedGoogle Scholar
  25. 25.
    Kono S, Oka K, Sueishi K, Sonobe M. Histopathological studies on spontaneous vault moyamoya and revascularized collaterals formed by encephalomyosynangiosis. Clin Neurol Neurosurg. 1997;99 Suppl 2:S209–12.CrossRefPubMedGoogle Scholar
  26. 26.
    Takeuchi S, Tsuchida T, Kobayashi K, Fukuda M, Ishii R, Tanaka R, et al. Treatment of moyamoya disease by temporal muscle graft ‘encephalo-myo-synangiosis’. Childs Brain. 1983;10(1):1–15.PubMedGoogle Scholar
  27. 27.
    Tu YK, Liu HM, Kuo MF, Wang PJ, Hung CC. Combined encephalo-arterio-synangiosis and encephalo-myo-synangiosis in the treatment of moyamoya disease. Clin Neurol Neurosurg. 1997;99 Suppl 2:S118–22.CrossRefPubMedGoogle Scholar
  28. 28.
    Yoshioka N, Tominaga S. Cerebral revascularization using muscle free flap for ischemic cerebrovascular disease in adult patients. Neurol Med Chir (Tokyo). 1998;38(8):464–8.CrossRefGoogle Scholar
  29. 29.
    Park JH, Yang SY, Chung YN, Kim JE, Kim SK, Han DH, et al. Modified encephaloduroarteriosynangiosis with bifrontal encephalogaleoperiosteal synangiosis for the treatment of pediatric moyamoya disease. Technical note. J Neurosurg. 2007;106(3 Suppl):237–42.PubMedGoogle Scholar
  30. 30.
    Matsushima Y, Fukai N, Tanaka K, Tsuruoka S, Inaba Y, Aoyagi M, et al. A new surgical treatment of moyamoya disease in children: a preliminary report. Surg Neurol. 1981;15(4):313–20.CrossRefPubMedGoogle Scholar
  31. 31.
    Kashiwagi S, Kato S, Yamashita K, Takasago T, Akimura T, Okamura S, et al. Revascularization with split duro-encephalo-synangiosis in the pediatric moyamoya disease--surgical result and clinical outcome. Clin Neurol Neurosurg. 1997;99 Suppl 2:S115–7.CrossRefPubMedGoogle Scholar
  32. 32.
    Kinugasa K, Mandai S, Kamata I, Sugiu K, Ohmoto T. Surgical treatment of moyamoya disease: operative technique for encephalo-duro-arterio-myo-synangiosis, its follow-up, clinical results, and angiograms. Neurosurgery. 1993;32(4):527–31.CrossRefPubMedGoogle Scholar
  33. 33.
    Karasawa J, Touho H, Ohnishi H, Miyamoto S, Kikuchi H. Cerebral revascularization using omental transplantation for childhood moyamoya disease. J Neurosurg. 1993;79(2):192–6.CrossRefPubMedGoogle Scholar
  34. 34.
    Stoodley MA, Steinberg GK. Omental transplantation for moyamoya disease. In: Ikezaki K, Loftus CM, editors. Moyamoya disease. Rolling Meadows: American Association of Neurological Surgeons; 2001. p. 185–97.Google Scholar
  35. 35.
    Navarro R, Chao K, Gooderham PA, Bruzoni M, Dutta S, Steinberg GK. Less invasive pedicled omental-cranial transposition in pediatric patients with moyamoya disease and failed prior revascularization. Neurosurgery. 2014;10 Suppl 1:1–14.PubMedGoogle Scholar
  36. 36.
    Touho H, Karasawa J, Ohnishi H. Cerebral revascularization using gracilis muscle transplantation for childhood moyamoya disease. Surg Neurol. 1995;43(2):191–7.CrossRefPubMedGoogle Scholar
  37. 37.
    Miyamoto S, Kikuchi H, Karasawa J, Nagata I, Yamazoe N, Akiyama Y. Pitfalls in the surgical treatment of moyamoya disease. Operative techniques for refractory cases. J Neurosurg. 1988;68(4):537–43.CrossRefPubMedGoogle Scholar
  38. 38.
    Matsushima T, Inoue TK, Suzuki SO, Inoue T, Ikezaki K, Fukui M, et al. Surgical techniques and the results of a fronto-temporo-parietal combined indirect bypass procedure for children with moyamoya disease: a comparison with the results of encephalo-duro-arterio-synangiosis alone. Clin Neurol Neurosurg. 1997;99 Suppl 2:S123–7.CrossRefPubMedGoogle Scholar
  39. 39.
    Pandey P, Steinberg GK. Outcome of repeat revascularization surgery for moyamoya disease after an unsuccessful indirect revascularization. Clinical article. J Neurosurg. 2011;115(2):328–36.CrossRefPubMedGoogle Scholar
  40. 40.
    Matsushima T, Inoue T, Katsuta T, Natori Y, Suzuki S, Ikezaki K, et al. An indirect revascularization method in the surgical treatment of moyamoya disease--various kinds of indirect procedures and a multiple combined indirect procedure. Neurol Med Chir (Tokyo). 1998;38(Suppl):297–302.CrossRefGoogle Scholar
  41. 41.
    Shrestha P, Sakamoto S, Ohba S, Shibukawa M, Kiura Y, Okazaki T, et al. Multiple concurrent anastomotic procedures in the management of moyamoya disease: a case report with review of literature. Hiroshima J Med Sci. 2008;57(1):47–51.PubMedGoogle Scholar
  42. 42.
    Houkin K, Kuroda S, Nakayama N. Cerebral revascularization for moyamoya disease in children. Neurosurg Clin N Am. 2001;12(3):575–84.PubMedGoogle Scholar
  43. 43.
    Kazumata K, Ito M, Tokairin K, Ito Y, Houkin K, Nakayama N, et al. The frequency of postoperative stroke in moyamoya disease following combined revascularization: a single-university series and systematic review. J Neurosurg. 2014;121(2):432–40.CrossRefPubMedGoogle Scholar
  44. 44.
    Andaluz N, Choutka O, Zuccarello M. Trends in the management of adult moyamoya disease in the United States: results of a nationwide survey. World Neurosurg. 2010;73(4):361–4.CrossRefPubMedGoogle Scholar
  45. 45.
    Fung LW, Thompson D, Ganesan V. Revascularisation surgery for paediatric moyamoya: a review of the literature. Childs Nerv Syst. 2005;21(5):358–64.CrossRefPubMedGoogle Scholar
  46. 46.
    Tripathi P, Tripathi V, Naik RJ, Patel JM. Moya Moya cases treated with encephaloduroarteriosynangiosis. Indian Pediatr. 2007;44(2):123–7.PubMedGoogle Scholar
  47. 47.
    Isono M, Ishii K, Kamida T, Inoue R, Fujiki M, Kobayashi H. Long-term outcomes of pediatric moyamoya disease treated by encephalo-duro-arterio-synangiosis. Pediatr Neurosurg. 2002;36(1):14–21.CrossRefPubMedGoogle Scholar
  48. 48.
    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.CrossRefPubMedGoogle Scholar
  49. 49.
    Kawaguchi S, Okuno S, Sakaki T. Effect of direct arterial bypass on the prevention of future stroke in patients with the hemorrhagic variety of moyamoya disease. J Neurosurg. 2000;93(3):397–401.CrossRefPubMedGoogle Scholar
  50. 50.
    Ishikawa T, Houkin K, Kamiyama H, Abe H. Effects of surgical revascularization on outcome of patients with pediatric moyamoya disease. Stroke. 1997;28(6):1170–3.CrossRefPubMedGoogle Scholar
  51. 51.
    Kim DS, Kang SG, Yoo DS, Huh PW, Cho KS, Park CK. Surgical results in pediatric moyamoya disease: angiographic revascularization and the clinical results. Clin Neurol Neurosurg. 2007;109(2):125–31.CrossRefPubMedGoogle Scholar
  52. 52.
    Houkin K, Kuroda S, Ishikawa T, Abe H. Neovascularization (angiogenesis) after revascularization in moyamoya disease. Which technique is most useful for moyamoya disease? Acta Neurochir (Wien). 2000;142(3):269–76.CrossRefGoogle Scholar
  53. 53.
    Houkin K, Ishikawa T, Yoshimoto T, Abe H. Direct and indirect revascularization for moyamoya disease surgical techniques and peri-operative complications. Clin Neurol Neurosurg. 1997;99 Suppl 2:S142–5.CrossRefPubMedGoogle Scholar
  54. 54.
    Matsushima T, Inoue T, Suzuki SO, Fujii K, Fukui M, Hasuo K. Surgical treatment of moyamoya disease in pediatric patients--comparison between the results of indirect and direct revascularization procedures. Neurosurgery. 1992;31(3):401–5.CrossRefPubMedGoogle Scholar
  55. 55.
    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.CrossRefPubMedGoogle Scholar
  56. 56.
    Golby AJ, Marks MP, Thompson RC, Steinberg GK. Direct and combined revascularization in pediatric moyamoya disease. Neurosurgery. 1999;45(1):50–60.PubMedGoogle Scholar
  57. 57.
    Wang MY, Steinberg GK. Rapid and near-complete resolution of moyamoya vessels in a patient with moyamoya disease treated with superficial temporal artery-middle cerebral artery bypass. Pediatr Neurosurg. 1996;24(3):145–50.CrossRefPubMedGoogle Scholar
  58. 58.
    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 [Research Support, Non-US Gov’t]. 2003;19(5–6):316–24.CrossRefGoogle Scholar
  59. 59.
    Suzuki Y, Negoro M, Shibuya M, Yoshida J, Negoro T, Watanabe K. Surgical treatment for pediatric moyamoya disease: use of the superficial temporal artery for both areas supplied by the anterior and middle cerebral arteries. Neurosurgery. 1997;40(2):324–9; discussion 9–30.CrossRefPubMedGoogle Scholar
  60. 60.
    Miyamoto S, Akiyama Y, Nagata I, Karasawa J, Nozaki K, Hashimoto N, et al. Long-term outcome after STA-MCA anastomosis for moyamoya disease. Neurosurg Focus. 1998;5(5):e5.CrossRefPubMedGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2016

Authors and Affiliations

  • Mario K. Teo
    • 1
  • Jeremiah N. Johnson
    • 1
  • Gary K. Steinberg
    • 2
  1. 1.Department of NeurosurgeryStanford University School of MedicineStanfordUSA
  2. 2.Department of Neurosurgery, R281Stanford University School of MedicineStanfordUSA

Personalised recommendations