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Recent Advances in Moyamoya Disease: Pathophysiology and Treatment

  • Annick Kronenburg
  • Kees P. J. Braun
  • Albert van der Zwan
  • Catharina J. M. KlijnEmail author
Stroke (H Adams, Section Editor)
Part of the following topical collections:
  1. Topical Collection on Stroke

Abstract

Moyamoya disease is a progressive intracranial arteriopathy characterized by bilateral stenosis of the distal portion of the internal carotid artery and the proximal anterior and middle cerebral arteries, resulting in transient ischemic attacks or strokes. The pathogenesis of moyamoya disease remains unresolved, but recent advances have suggested exciting new insights into a genetic contribution as well as into other pathophysiological mechanisms. Treatment that may halt progression of the disease or even reverse the intracranial arteriopathy is yet to be found. There are strong indications that neurosurgical intervention, through direct, indirect, or combined revascularization surgery, can reduce the risk of ischemic stroke and possibly also cognitive dysfunction by improving cerebral perfusion, although randomized clinical trials have not been performed. Many questions regarding the indication for and timing of surgery remain unanswered. In this review, we discuss recent developments in the pathogenesis and treatment of moyamoya disease.

Keywords

Moyamoya Latest advancements Pathophysiology Genetics Revascularization Direct bypass Cerebral perfusion studies Neuroimaging Outcome Cognition 

Abbreviations

CBF

Cerebral blood flow

CT

Computed tomography

CVR

Cerebrovascular reserve

DSA

Digital subtraction angiography

EPC

Endothelial progenitor cell

ICA

Internal carotid artery

MCA

Middle cerebral artery

MMD

Moyamoya disease

MMP

Matrix metalloproteinase

MMS

Moyamoya syndrome

MMV

Moyamoya vasculopathy

MRI

Magnetic resonance imaging

PET

Positron emission tomography

RCT

Randomized controlled trial

SMC

Smooth muscle cell

STA

Superficial temporal artery

TIA

Transient ischemic attack

Notes

Compliance with Ethics Guidelines

Conflict of Interest

Annick Kronenburg, Kees P.J. Braun, and Albert van der Zwan declare that they have no conflict of interest.

Catharina J.M. Klijn has grants pending from the Dutch Brain Foundation [2012(1)-179], the Tutein Nolthenius Oldenhof Fund, and the Dutch Heart Foundation (Clinical Established Investigator grant 2012 T077).

Human and Animal Rights and Informed Consent

This article does not contain any studies with human or animal subjects performed by any of the authors.

References

  1. 1.
    Scott RM, Smith ER. Moyamoya disease and moyamoya syndrome. N Engl J Med. 2009;360:1226–37.PubMedCrossRefGoogle Scholar
  2. 2.
    Suzuki J, Takaku A. Cerebrovascular "moyamoya" disease. Disease showing abnormal net-like vessels in base of brain. Arch Neurol. 1969;20:288–99.PubMedCrossRefGoogle Scholar
  3. 3.
    Kleinloog R, Regli L, Rinkel GJ, Klijn CJ. Regional differences in incidence and patient characteristics of moyamoya disease: a systematic review. J Neurol Neurosurg Psychiatry. 2012;83:531–6.PubMedCrossRefGoogle Scholar
  4. 4.
    Cho HJ, Jung YH, Kim YD, et al. The different infarct patterns between adulthood-onset and childhood-onset moyamoya disease. J Neurol Neurosurg Psychiatry. 2011;82:38–40.PubMedCrossRefGoogle Scholar
  5. 5.
    Takekawa Y, Umezawa T, Ueno Y, Sawada T, Kobayashi M. Pathological and immunohistochemical findings of an autopsy case of adult moyamoya disease. Neuropathology. 2004;24:236–42.PubMedCrossRefGoogle Scholar
  6. 6.
    Hosoda Y, Ikeda E, Hirose S. Histopathological studies on spontaneous occlusion of the circle of Willis (cerebrovascular moyamoya disease). Clin Neurol Neurosurg. 1997;99 Suppl 2:S203–8.PubMedCrossRefGoogle Scholar
  7. 7.
    Kaku Y, Morioka M, Ohmori Y, et al. Outer-diameter narrowing of the internal carotid and middle cerebral arteries in moyamoya disease detected on 3D constructive interference in steady-state MR image: is arterial constrictive remodeling a major pathogenesis? Acta Neurochir (Wien). 2012;154:2151–7.CrossRefGoogle Scholar
  8. 8.
    Kim JM, Jung KH, Sohn CH, et al. High-resolution MR technique can distinguish moyamoya disease from atherosclerotic occlusion. Neurology. 2013;80:775–6.PubMedCrossRefGoogle Scholar
  9. 9.
    Yamashita M, Tanaka K, Matsuo T, et al. Cerebral dissecting aneurysms in patients with moyamoya disease. Report of two cases. J Neurosurg. 1983;58:120–5.PubMedCrossRefGoogle Scholar
  10. 10.
    Houkin K, Ito M, Sugiyama T, et al. Review of past research and current concepts on the etiology of moyamoya disease. Neurol Med Chir (Tokyo). 2012;52:267–77.Google Scholar
  11. 11.
    Jiang T, Perry A, Dacey Jr RG, Zipfel GJ, Derdeyn CP. Intracranial atherosclerotic disease associated with moyamoya collateral formation: histopathological findings. J Neurosurg. 2013;118:1030–4.PubMedCrossRefGoogle Scholar
  12. 12.
    Baba T, Houkin K, Kuroda S. Novel epidemiological features of moyamoya disease. J Neurol Neurosurg Psychiatry. 2008;79:900–4.PubMedCrossRefGoogle Scholar
  13. 13.
    Mineharu Y, Takenaka K, Yamakawa H, et al. Inheritance pattern of familial moyamoya disease: autosomal dominant mode and genomic imprinting. J Neurol Neurosurg Psychiatry. 2006;77:1025–9.PubMedCrossRefGoogle Scholar
  14. 14.
    Kraemer M, Heinemann FM, Horn PA, et al. Inheritance of moyamoya disease in a Caucasian family. Eur J Neurol. 2012;19:438–42.PubMedCrossRefGoogle Scholar
  15. 15.
    Herve D, Touraine P, Verloes A, et al. A hereditary moyamoya syndrome with multisystemic manifestations. Neurology. 2010;75:259–64.PubMedCrossRefGoogle Scholar
  16. 16.
    • Munot P, Saunders DE, Milewicz DM, et al. A novel distinctive cerebrovascular phenotype is associated with heterozygous Arg179 ACTA2 mutations. Brain. 2012;135:2506–14. This article describes the distinctive angiographic features of the intracranial vasculopathy associated with ACTA2 mutations.PubMedCrossRefGoogle Scholar
  17. 17.
    Roder C, Nayak NR, Khan N, et al. Genetics of moyamoya disease. J Hum Genet. 2010;55:711–6.PubMedCrossRefGoogle Scholar
  18. 18.
    •• Liu W, Morito D, Takashima S, et al. Identification of RNF213 as a susceptibility gene for moyamoya disease and its possible role in vascular development. PLoS One. 2011;6:e22542. This study (as well as [19]) has identified RNF213 as the first MMD gene.PubMedCentralPubMedCrossRefGoogle Scholar
  19. 19.
    •• Kamada F, Aoki Y, Narisawa A, et al. A genome-wide association study identifies RNF213 as the first moyamoya disease gene. J Hum Genet. 2011;56:34–40. This study (as well as [18]) has identified RNF213 as the first MMD gene.PubMedCrossRefGoogle Scholar
  20. 20.
    Wu Z, Jiang H, Zhang L, et al. Molecular analysis of RNF213 gene for moyamoya disease in the Chinese Han population. PLoS One. 2012;7:e48179.PubMedCentralPubMedCrossRefGoogle Scholar
  21. 21.
    Liu W, Hitomi T, Kobayashi H, Harada KH, Koizumi A. Distribution of moyamoya disease susceptibility polymorphism p.R4810K in RNF213 in East and Southeast Asian populations. Neurol Med Chir (Tokyo). 2012;52:299–303.Google Scholar
  22. 22.
    Miyawaki S, Imai H, Takayanagi S, et al. Identification of a genetic variant common to moyamoya disease and intracranial major artery stenosis/occlusion. Stroke. 2012;43:3371–4.PubMedCrossRefGoogle Scholar
  23. 23.
    Hitomi T, Habu T, Kobayashi H, et al. Downregulation of securin by the variant RNF213 R4810K reduces angiogenic activity of induced pluripotent stem cell-derived vascular endothelial cells from moyamoya patients. Biochem Biophys Res Commun. 2013;438(1):13–9.PubMedCrossRefGoogle Scholar
  24. 24.
    Miyatake S, Miyake N, Touho H, et al. Homozygous c.14576G > A variant of RNF213 predicts early-onset and severe form of moyamoya disease. Neurology. 2012;78:803–10.PubMedCrossRefGoogle Scholar
  25. 25.
    Achrol AS, Guzman R, Lee M, Steinberg GK. Pathophysiology and genetic factors in moyamoya disease. Neurosurg Focus. 2009;26:E4.PubMedCrossRefGoogle Scholar
  26. 26.
    Houkin K, Ito M, Sugiyama T, et al. Review of past research and current concepts on the etiology of moyamoya disease. Neurol Med Chir (Tokyo). 2012;52:267–77.Google Scholar
  27. 27.
    Kang HS, Kim JH, Phi JH, et al. Plasma matrix metalloproteinases, cytokines and angiogenic factors in moyamoya disease. J Neurol Neurosurg Psychiatry. 2010;81:673–8.PubMedCrossRefGoogle Scholar
  28. 28.
    Rundhaug JE. Matrix metalloproteinases and angiogenesis. J Cell Mol Med. 2005;9:267–85.PubMedCrossRefGoogle Scholar
  29. 29.
    Fujimura M, Watanabe M, Narisawa A, Shimizu H, Tominaga T. Increased expression of serum matrix metalloproteinase-9 in patients with moyamoya disease. Surg Neurol. 2009;72:476–80. discussion 480.PubMedCrossRefGoogle Scholar
  30. 30.
    Kim JH, Jung JH, Phi JH, et al. Decreased level and defective function of circulating endothelial progenitor cells in children with moyamoya disease. J Neurosci Res. 2010;88:510–8.PubMedGoogle Scholar
  31. 31.
    Kang HS, Kim JH, Phi JH, et al. Plasma matrix metalloproteinases, cytokines and angiogenic factors in moyamoya disease. J Neurol Neurosurg Psychiatry. 2010;81:673–8.PubMedCrossRefGoogle Scholar
  32. 32.
    Jung KH, Chu K, Lee ST, et al. Circulating endothelial progenitor cells as a pathogenetic marker of moyamoya disease. J Cereb Blood Flow Metab. 2008;28:1795–803.PubMedCrossRefGoogle Scholar
  33. 33.
    Zou D, Zhao J, Zhang D, et al. Enhancement expression of bFGF in Chinese patients with moyamoya disease. Biomed Environ Sci. 2011;24:74–80.PubMedGoogle Scholar
  34. 34.
    Koh EJ, Kim HN, Ma TZ, Choi HY, Kwak YG. Comparative analysis of serum proteomes of moyamoya disease and normal controls. J Korean Neurosurg Soc. 2010;48:8–13.PubMedCentralPubMedCrossRefGoogle Scholar
  35. 35.
    Araki Y, Yoshikawa K, Okamoto S, et al. Identification of novel biomarker candidates by proteomic analysis of cerebrospinal fluid from patients with moyamoya disease using SELDI-TOF-MS. BMC Neurol. 2010;10:112.PubMedCentralPubMedCrossRefGoogle Scholar
  36. 36.
    • Lin R, Xie Z, Zhang J, et al. Clinical and immunopathological features of moyamoya disease. PLoS One. 2012;7:e36386. This study reports the immunological results from a large group of MMD patients (n = 65), including the histopathological features of three patients.PubMedCentralPubMedCrossRefGoogle Scholar
  37. 37.
    • Sigdel TK, Shoemaker LD, Chen R, et al. Immune response profiling identifies autoantibodies specific to moyamoya patients. Orphanet J Rare Dis. 2013;8:45. This is the first study to provide high-throughput analysis of autoantibodies in MMD.PubMedCentralPubMedCrossRefGoogle Scholar
  38. 38.
    Bower RS, Mallory GW, Nwojo M, et al. Moyamoya disease in a primarily white, Midwestern US population: increased prevalence of autoimmune disease. Stroke. 2013;44:1997–9.PubMedCrossRefGoogle Scholar
  39. 39.
    Li H, Zhang ZS, Dong ZN, et al. Increased thyroid function and elevated thyroid autoantibodies in pediatric patients with moyamoya disease: a case-control study. Stroke. 2011;42:1138–9.PubMedCrossRefGoogle Scholar
  40. 40.
    Kim SJ, Heo KG, Shin HY, et al. Association of thyroid autoantibodies with moyamoya-type cerebrovascular disease: a prospective study. Stroke. 2010;41:173–6.PubMedCrossRefGoogle Scholar
  41. 41.
    Kraemer M, Berlit P, Diesner F, Khan N. What is the expert's option on antiplatelet therapy in moyamoya disease? Results of a worldwide survey. Eur J Neurol. 2012;19:163–7.PubMedCrossRefGoogle Scholar
  42. 42.
    • 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 Intractable Diseases. Guidelines for diagnosis and treatment of moyamoya disease (spontaneous occlusion of the circle of Willis). Neurol Med Chir (Tokyo). 2012;52:245–66. This article extensively reports the evidence-based guidelines for the diagnosis and treatment of MMV.Google Scholar
  43. 43.
    Smith ER. Moyamoya arteriopathy. Curr Treat Options Neurol. 2012;14:549–56.PubMedCrossRefGoogle Scholar
  44. 44.
    Ganesan V. Moyamoya: to cut or not to cut is not the only question. A paediatric neurologist's perspective. Dev Med Child Neurol. 2010;52:10–3.PubMedCrossRefGoogle Scholar
  45. 45.
    Khan N, Dodd R, Marks MP, et al. Failure of primary percutaneous angioplasty and stenting in the prevention of ischemia in moyamoya angiopathy. Cerebrovasc Dis. 2011;31:147–53.PubMedCrossRefGoogle Scholar
  46. 46.
    • Smith ER, Scott RM. Spontaneous occlusion of the circle of Willis in children: pediatric moyamoya summary with proposed evidence-based practice guidelines. A review. J Neurosurg Pediatr. 2012;9:353–60. This article offers practical guidelines with specific evidence-based guidelines for (surgical) treatment.PubMedCrossRefGoogle Scholar
  47. 47.
    Roach ES, Golomb MR, Adams R, et al. Management of stroke in infants and children: a scientific statement from a Special Writing Group of the American Heart Association Stroke Council and the Council on Cardiovascular Disease in the Young. Stroke. 2008;39:2644–91.PubMedCrossRefGoogle Scholar
  48. 48.
    Fung LW, Thompson D, Ganesan V. Revascularisation surgery for paediatric moyamoya: a review of the literature. Childs Nerv Syst. 2005;21:358–64.PubMedCrossRefGoogle Scholar
  49. 49.
    Gross BA, Du R. The natural history of moyamoya in a North American adult cohort. J Clin Neurosci. 2013;20:44–8.PubMedCrossRefGoogle Scholar
  50. 50.
    Kuroda S, Ishikawa T, Houkin K, et al. Incidence and clinical features of disease progression in adult moyamoya disease. Stroke. 2005;36:2148–53.PubMedCrossRefGoogle Scholar
  51. 51.
    Abla AA, Gandhoke G, Clark JC, et al. Surgical outcomes for moyamoya angiopathy at Barrow Neurological Institute with comparison of adult indirect EDAS bypass, adult direct STA-MCA bypass and pediatric bypass: 154 revascularization surgeries in 140 affected hemispheres. Neurosurgery. 2013;73(3):430–9.PubMedCrossRefGoogle Scholar
  52. 52.
    Guzman R, Lee M, Achrol A, et al. Clinical outcome after 450 revascularization procedures for moyamoya disease. Clinical article. J Neurosurg. 2009;111:927–35.PubMedCrossRefGoogle Scholar
  53. 53.
    Bao XY, Duan L, Li DS, et al. Clinical features, surgical treatment and long-term outcome in adult patients with moyamoya disease in China. Cerebrovasc Dis. 2012;34:305–13.PubMedCrossRefGoogle Scholar
  54. 54.
    Dusick JR, Gonzalez NR, Martin NA. Clinical and angiographic outcomes from indirect revascularization surgery for moyamoya disease in adults and children: a review of 63 procedures. Neurosurgery. 2011;68:34–43. discussion 43.PubMedCrossRefGoogle Scholar
  55. 55.
    Duan L, Bao XY, Yang WZ, et al. Moyamoya disease in China: its clinical features and outcomes. Stroke. 2012;43:56–60.PubMedCrossRefGoogle Scholar
  56. 56.
    Mukawa M, Nariai T, Matsushima Y, et al. Long-term follow-up of surgically treated juvenile patients with moyamoya disease. J Neurosurg Pediatr. 2012;10:451–6.PubMedCrossRefGoogle Scholar
  57. 57.
    Kawabori M, Kuroda S, Nakayama N, et al. Effective surgical revascularization improves cerebral hemodynamics and resolves headache in pediatric moyamoya disease. World Neurosurg. 2012. doi: 10.1016/j.wneu.2012.08.005.PubMedGoogle Scholar
  58. 58.
    Okada Y, Kawamata T, Kawashima A, et al. The efficacy of superficial temporal artery-middle cerebral artery anastomosis in patients with moyamoya disease complaining of severe headache. J Neurosurg. 2012;116:672–9.PubMedCrossRefGoogle Scholar
  59. 59.
    Chao K, Steinberg GK. Re: "Effective surgical revascularization improves cerebral hemodynamics and resolves headache in pediatric moyamoya disease". World Neurosurg. 2012. doi: 10.1016/j.wneu.2012.11.018.Google Scholar
  60. 60.
    Miyamoto S, Japan Adult Moyamoya Trial Group. Study design for a prospective randomized trial of extracranial-intracranial bypass surgery for adults with moyamoya disease and hemorrhagic onset—the Japan Adult Moyamoya Trial Group. Neurol Med Chir (Tokyo). 2004;44:218–9.CrossRefGoogle Scholar
  61. 61.
    Liu X, Zhang D, Shuo W, et al. Long term outcome after conservative and surgical treatment of haemorrhagic moyamoya disease. J Neurol Neurosurg Psychiatry. 2013;84:258–65.PubMedCrossRefGoogle Scholar
  62. 62.
    Ryan RW, Chowdhary A, Britz GW. Hemorrhage and risk of further hemorrhagic strokes following cerebral revascularization in moyamoya disease: a review of the literature. Surg Neurol Int. 2012;3:72.PubMedCentralPubMedCrossRefGoogle Scholar
  63. 63.
    Lee JY, Phi JH, Wang KC, et al. Neurocognitive profiles of children with moyamoya disease before and after surgical intervention. Cerebrovasc Dis. 2011;31:230–7.PubMedCrossRefGoogle Scholar
  64. 64.
    Karzmark P, Zeifert PD, Bell-Stephens TE, Steinberg GK, Dorfman LJ. Neurocognitive impairment in adults with moyamoya disease without stroke. Neurosurgery. 2012;70:634–8.PubMedCrossRefGoogle Scholar
  65. 65.
    Weinberg DG, Rahme RJ, Aoun SG, Batjer HH, Bendok BR. Moyamoya disease: functional and neurocognitive outcomes in the pediatric and adult populations. Neurosurg Focus. 2011;30:E21.PubMedCrossRefGoogle Scholar
  66. 66.
    Nakamizo A, Kikkawa Y, Hiwatashi A, Matsushima T, Sasaki T. Executive function and diffusion in frontal white matter of adults with moyamoya disease. J Stroke Cerebrovasc Dis. 2013. doi: 10.1016/j.jstrokecerebrovasdis.2013.03.022.PubMedGoogle Scholar
  67. 67.
    Calviere L, Ssi Yan Kai G, Catalaa I, et al. Executive dysfunction in adults with moyamoya disease is associated with increased diffusion in frontal white matter. J Neurol Neurosurg Psychiatry. 2012;83:591–3.PubMedCrossRefGoogle Scholar
  68. 68.
    Khan N, Schuknecht B, Boltshauser E, et al. Moyamoya disease and moyamoya syndrome: experience in Europe; choice of revascularisation procedures. Acta Neurochir (Wien). 2003;145:1061–71. discussion 1071.CrossRefGoogle Scholar
  69. 69.
    Lee M, Zaharchuk G, Guzman R, et al. Quantitative hemodynamic studies in moyamoya disease: a review. Neurosurg Focus. 2009;26:E5.PubMedCentralPubMedCrossRefGoogle Scholar
  70. 70.
    Han JS, Mikulis DJ, Mardimae A, et al. Measurement of cerebrovascular reactivity in pediatric patients with cerebral vasculopathy using blood oxygen level-dependent MRI. Stroke. 2011;42:1261–9.PubMedCrossRefGoogle Scholar
  71. 71.
    Zaharchuk G, Do HM, Marks MP, et al. Arterial spin-labeling MRI can identify the presence and intensity of collateral perfusion in patients with moyamoya disease. Stroke. 2011;42:2485–91.PubMedCentralPubMedCrossRefGoogle Scholar
  72. 72.
    Noguchi T, Kawashima M, Irie H, et al. Arterial spin-labeling MR imaging in moyamoya disease compared with SPECT imaging. Eur J Radiol. 2011;80:e557–62.PubMedCrossRefGoogle Scholar
  73. 73.
    Rim NJ, Kim HS, Shin YS. Kim SY Which CT perfusion parameter best reflects cerebrovascular reserve?: correlation of acetazolamide-challenged CT perfusion with single-photon emission CT in moyamoya patients. AJNR Am J Neuroradiol. 2008;29:1658–63.PubMedCrossRefGoogle Scholar
  74. 74.
    Zhang J, Wang J, Geng D, et al. Whole-brain CT perfusion and CT angiography assessment of moyamoya disease before and after surgical revascularization: preliminary study with 256-slice CT. PLoS One. 2013;8:e57595.PubMedCentralPubMedCrossRefGoogle Scholar
  75. 75.
    Guzman R, Steinberg GK. Direct bypass techniques for the treatment of pediatric moyamoya disease. Neurosurg Clin N Am. 2010;21:565–73.PubMedCrossRefGoogle Scholar
  76. 76.
    Khan N, Yonekawa Y. Moyamoya angiopathy in Europe: the beginnings in Zürich, practical lessons learned, increasing awareness and future perspectives. Acta Neurochir Suppl. 2008;103:127–30.PubMedCrossRefGoogle Scholar
  77. 77.
    Patel NN, Mangano FT, Klimo Jr P. Indirect revascularization techniques for treating moyamoya disease. Neurosurg Clin N Am. 2010;21:553–63.PubMedCrossRefGoogle Scholar
  78. 78.
    McLaughlin N, Martin NA. Effectiveness of burr holes for indirect revascularization in patients with moyamoya disease—a review of the literature. World Neurosurg. 2013. doi: 10.1016/j.wneu.2013.05.010.Google Scholar
  79. 79.
    Oliveira RS, Amato MC, Simao GN, et al. Effect of multiple cranial burr hole surgery on prevention of recurrent ischemic attacks in children with moyamoya disease. Neuropediatrics. 2009;40:260–4.PubMedCrossRefGoogle Scholar
  80. 80.
    Kim DS, Huh PW, Kim HS, et al. Surgical treatment of moyamoya disease in adults: combined direct and indirect vs. indirect bypass surgery. Neurol Med Chir (Tokyo). 2012;52:333–8.Google Scholar
  81. 81.
    Hayashi T, Shirane R, Tominaga T. Additional surgery for postoperative ischemic symptoms in patients with moyamoya disease: the effectiveness of occipital artery-posterior cerebral artery bypass with an indirect procedure: technical case report. Neurosurgery. 2009;64:E195–6. discussion E196.PubMedCrossRefGoogle Scholar
  82. 82.
    Horiuchi T, Kusano Y, Asanuma M, Hongo K. Posterior auricular artery-middle cerebral artery bypass for additional surgery of moyamoya disease. Acta Neurochir (Wien). 2012;154:455–6.CrossRefGoogle Scholar
  83. 83.
    Kawashima A, Kawamata T, Yamaguchi K, Hori T, Okada Y. Successful superficial temporal artery-anterior cerebral artery direct bypass using a long graft for moyamoya disease: technical note. Neurosurgery. 2010;67:ons145–9. discussion ons149.PubMedCrossRefGoogle Scholar
  84. 84.
    Kuroda S, Houkin K, Ishikawa T, Nakayama N, Iwasaki Y. Novel bypass surgery for moyamoya disease using pericranial flap: its impacts on cerebral hemodynamics and long-term outcome. Neurosurgery. 2010;66:1093–101. discussion 1101.PubMedCrossRefGoogle Scholar
  85. 85.
    McLaughlin N, Martin NA. Meningeal management for optimal revascularization from middle meningeal artery. J Neurosurg. 2013;118:104–8.PubMedCrossRefGoogle Scholar
  86. 86.
    Kronenburg A, Esposito G, Fierstra J, Braun K, Regli L. Combined bypass technique for contemporary revascularization of unilateral MCA and bilateral frontal territories in moyamoya vasculopathy. Acta Neurochir Suppl. 2014;119, in press.Google Scholar
  87. 87.
    Muto J, Oi S. Intradural arteriosynangiosis in pediatric moyamoya disease: modified technique of encephalo-duro-arterio-synangiosis with reduced operative damage to already growing revascularization. Childs Nerv Syst. 2009;25:607–12.PubMedCrossRefGoogle Scholar
  88. 88.
    Pandey P, Steinberg GK. Neurosurgical advances in the treatment of moyamoya disease. Stroke. 2011;42:3304–10.PubMedCrossRefGoogle Scholar
  89. 89.
    Zhao WG, Luo Q, Jia JB, Yu JL. Cerebral hyperperfusion syndrome after revascularization surgery in patients with moyamoya disease. Br J Neurosurg. 2013;27:321–5.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2013

Authors and Affiliations

  • Annick Kronenburg
    • 1
  • Kees P. J. Braun
    • 1
  • Albert van der Zwan
    • 1
  • Catharina J. M. Klijn
    • 1
    Email author
  1. 1.Department of Neurology and NeurosurgeryBrain Center Rudolf Magnus, UMC UtrechtUtrechtThe Netherlands

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