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Moyamoya Syndrome : A Window of Moyamoya Disease

  • Phi, Ji Hoon (Division of Pediatric Neurosurgery, Seoul National University Children's Hospital, Seoul National University College of Medicine) ;
  • Wang, Kyu-Chang (Division of Pediatric Neurosurgery, Seoul National University Children's Hospital, Seoul National University College of Medicine) ;
  • Lee, Ji Yeoun (Division of Pediatric Neurosurgery, Seoul National University Children's Hospital, Seoul National University College of Medicine) ;
  • Kim, Seung-Ki (Division of Pediatric Neurosurgery, Seoul National University Children's Hospital, Seoul National University College of Medicine)
  • Received : 2015.03.04
  • Accepted : 2015.04.29
  • Published : 2015.06.28

Abstract

Moyamoya-like vasculopathy develops in association with various systemic diseases and conditions, which is termed moyamoya syndrome. Relatively common diseases and conditions are related to moyamoya syndrome, including neurofibromatosis type 1, Down syndrome, thyroid disease, and cranial irradiation. Moyamoya syndrome shares phenotypical characteristics with idiopathic moyamoya disease. However, they differ in other details, including clinical presentations, natural history, and treatment considerations. The study of moyamoya syndrome can provide clinicians and researchers with valuable knowledge and insight. Although it is infrequently encountered in clinical practice, moyamoya-like vasculopathy can severely complicate outcomes for patients with various underlying diseases when the clinician fails to expect or diagnose moyamoya syndrome development. Furthermore, moyamoya syndrome could be used as a doorway to more enigmatic moyamoya disease in research. More comprehensive survey and investigation are required to uncover the secrets of all the moyamoya-like phenomena.

Keywords

References

  1. Bajaj A, Li QF, Zheng Q, Pumiglia K : Loss of NF1 expression in human endothelial cells promotes autonomous proliferation and altered vascular morphogenesis. PLoS One 7 : e49222, 2012 https://doi.org/10.1371/journal.pone.0049222
  2. Berk AT, Saatci AO, Erçal MD, Tunç M, Ergin M : Ocular findings in 55 patients with Down's syndrome. Ophthalmic Genet 17 : 15-19, 1996 https://doi.org/10.3109/13816819609057864
  3. Booth F, Yanofsky R, Ross IB, Lawrence P, Oen K : Primary antiphospholipid syndrome with moyamoya-like vascular changes. Pediatr Neurosurg 31 : 45-48, 1999 https://doi.org/10.1159/000028830
  4. Bowers DC, Liu Y, Leisenring W, McNeil E, Stovall M, Gurney JG, et al. : Late-occurring stroke among long-term survivors of childhood leukemia and brain tumors : a report from the Childhood Cancer Survivor Study. J Clin Oncol 24 : 5277-5282, 2006 https://doi.org/10.1200/JCO.2006.07.2884
  5. Cairns AG, North KN : Cerebrovascular dysplasia in neurofibromatosis type 1. J Neurol Neurosurg Psychiatry 79 : 1165-1170, 2008 https://doi.org/10.1136/jnnp.2007.136457
  6. Chiang CS, Hong JH, Stalder A, Sun JR, Withers HR, McBride WH : Delayed molecular responses to brain irradiation. Int J Radiat Biol 72 : 45-53, 1997 https://doi.org/10.1080/095530097143527
  7. Czarkowski M, Hilgertner L, Powałowski T, Radomski D : The stiffness of the common carotid artery in patients with Graves' disease. Int Angiol 21 : 152-157, 2002
  8. Desai SS, Paulino AC, Mai WY, Teh BS : Radiation-induced moyamoya syndrome. Int J Radiat Oncol Biol Phys 65 : 1222-1227, 2006 https://doi.org/10.1016/j.ijrobp.2006.01.038
  9. Fajardo LF : The pathology of ionizing radiation as defined by morphologic patterns. Acta Oncol 44 : 13-22, 2005 https://doi.org/10.1080/02841860510007440
  10. Franklyn JA, Boelaert K : Thyrotoxicosis. Lancet 379 : 1155-1166, 2012 https://doi.org/10.1016/S0140-6736(11)60782-4
  11. Fulcher T, Griffin M, Crowley S, Firth R, Acheson R, O'Meara N : Diabetic retinopathy in Down's syndrome. Br J Ophthalmol 82 : 407-409, 1998 https://doi.org/10.1136/bjo.82.4.407
  12. Ghosh PS, Rothner AD, Emch TM, Friedman NR, Moodley M : Cerebral vasculopathy in children with neurofibromatosis type 1. J Child Neurol 28 : 95-101, 2013 https://doi.org/10.1177/0883073812441059
  13. Hasle H, Clemmensen IH, Mikkelsen M : Risks of leukaemia and solid tumours in individuals with Down's syndrome. Lancet 355 : 165-169, 2000 https://doi.org/10.1016/S0140-6736(99)05264-2
  14. Ikeda H, Sasaki T, Yoshimoto T, Fukui M, Arinami T : Mapping of a familial moyamoya disease gene to chromosome 3p24.2-p26. Am J Hum Genet 64 : 533-537, 1999 https://doi.org/10.1086/302243
  15. Im SH, Oh CW, Kwon OK, Kim JE, Han DH : Moyamoya disease associated with Graves disease : special considerations regarding clinical significance and management. J Neurosurg 102 : 1013-1017, 2005 https://doi.org/10.3171/jns.2005.102.6.1013
  16. Inoue TK, Ikezaki K, Sasazuki T, Matsushima T, Fukui M : Linkage analysis of moyamoya disease on chromosome 6. J Child Neurol 15 : 179-182, 2000 https://doi.org/10.1177/088307380001500307
  17. Jacks T, Shih TS, Schmitt EM, Bronson RT, Bernards A, Weinberg RA : Tumour predisposition in mice heterozygous for a targeted mutation in Nf1. Nat Genet 7 : 353-361, 1994 https://doi.org/10.1038/ng0794-353
  18. Jea A, Smith ER, Robertson R, Scott RM : Moyamoya syndrome associated with Down syndrome : outcome after surgical revascularization. Pediatrics 116 : e694-e701, 2005 https://doi.org/10.1542/peds.2005-0568
  19. Jeong HC, Kim YJ, Yoon W, Joo SP, Lee SS, Park YW : Moyamoya syndrome associated with systemic lupus erythematosus. Lupus 17 : 679-682, 2008 https://doi.org/10.1177/0961203307087375
  20. Jett K, Friedman JM : Clinical and genetic aspects of neurofibromatosis 1. Genet Med 12 : 1-11, 2010
  21. Kainth DS, Chaudhry SA, Kainth HS, Suri FK, Qureshi AI : Prevalence and characteristics of concurrent down syndrome in patients with moyamoya disease. Neurosurgery 72 : 210-215; discussion 215, 2013 https://doi.org/10.1227/NEU.0b013e31827b9beb
  22. Kamada F, Aoki Y, Narisawa A, Abe Y, Komatsuzaki S, Kikuchi A, et al. : A genome-wide association study identifies RNF213 as the first Moyamoya disease gene. J Hum Genet 56 : 34-40, 2011 https://doi.org/10.1038/jhg.2010.132
  23. Keene DL, Johnston DL, Grimard L, Michaud J, Vassilyadi M, Ventureyra E : Vascular complications of cranial radiation. Childs Nerv Syst 22 : 547-555, 2006 https://doi.org/10.1007/s00381-006-0097-4
  24. Kim SJ, Heo KG, Shin HY, Bang OY, Kim GM, Chung CS, et al. : Association of thyroid autoantibodies with moyamoya-type cerebrovascular disease : a prospective study. Stroke 41 : 173-176, 2010 https://doi.org/10.1161/STROKEAHA.109.562264
  25. Kim SK, Cho BK, Phi JH, Lee JY, Chae JH, Kim KJ, et al. : Pediatric moyamoya disease : an analysis of 410 consecutive cases. Ann Neurol 68 : 92-101, 2010 https://doi.org/10.1002/ana.21981
  26. 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 11 : 417-425, 2013 https://doi.org/10.3171/2012.12.PEDS12281
  27. Kuroda S, Houkin K : Moyamoya disease : current concepts and future perspectives. Lancet Neurol 7 : 1056-1066, 2008 https://doi.org/10.1016/S1474-4422(08)70240-0
  28. Lee HS, Seol HJ, Kong DS, Shin HJ : Moyamoya syndrome precipitated by cranial irradiation for craniopharyngioma in children. J Korean Neurosurg Soc 50 : 535-537, 2011 https://doi.org/10.3340/jkns.2011.50.6.535
  29. Leno C, Mateo I, Cid C, Berciano J, Sedano C : Autoimmunity in Down's syndrome : another possible mechanism of Moyamoya disease. Stroke 29 : 868-869, 1998 https://doi.org/10.1161/01.STR.29.4.868
  30. Malav IC, Kothari SS : Renal artery stenosis due to neurofibromatosis. Ann Pediatr Cardiol 2 : 167-169, 2009 https://doi.org/10.4103/0974-2069.58323
  31. Mineharu Y, Liu W, Inoue K, Matsuura N, Inoue S, Takenaka K, et al. : Autosomal dominant moyamoya disease maps to chromosome 17q25.3. Neurology 70 (24 Pt 2) : 2357-2363, 2008 https://doi.org/10.1212/01.wnl.0000291012.49986.f9
  32. Miyatake S, Miyake N, Touho H, Nishimura-Tadaki A, Kondo Y, Okada I, et al. : Homozygous c.14576G>A variant of RNF213 predicts early-onset and severe form of moyamoya disease. Neurology 78 : 803-810, 2012 https://doi.org/10.1212/WNL.0b013e318249f71f
  33. Morris B, Partap S, Yeom K, Gibbs IC, Fisher PG, King AA : Cerebrovascular disease in childhood cancer survivors : a Children's Oncology Group Report. Neurology 73 : 1906-1913, 2009 https://doi.org/10.1212/WNL.0b013e3181c17ea8
  34. Norton KK, Xu J, Gutmann DH : Expression of the neurofibromatosis I gene product, neurofibromin, in blood vessel endothelial cells and smooth muscle. Neurobiol Dis 2 : 13-21, 1995 https://doi.org/10.1006/nbdi.1995.0002
  35. Ohba S, Nakagawa T, Murakami H : Concurrent Graves' disease and intracranial arterial stenosis/occlusion : special considerations regarding the state of thyroid function, etiology, and treatment. Neurosurg Rev 34 : 297-304; discussion 304, 2011 https://doi.org/10.1007/s10143-011-0311-z
  36. Panegyres PK, Morris JG, O'Neill PJ, Balleine R : Moyamoya-like disease with inflammation. Eur Neurol 33 : 260-263, 1993 https://doi.org/10.1159/000116950
  37. Parsa CF, Almer Z : Supranumerary optic disc vessels may indicate reduced systemic angiogenesis in Down syndrome. Br J Ophthalmol 92 : 432-433, 2008 https://doi.org/10.1136/bjo.2007.124248
  38. Ram G, Chinen J : Infections and immunodeficiency in Down syndrome. Clin Exp Immunol 164 : 9-16, 2011 https://doi.org/10.1111/j.1365-2249.2011.04335.x
  39. Rea D, Brandsema JF, Armstrong D, Parkin PC, deVeber G, MacGregor D, et al. : Cerebral arteriopathy in children with neurofibromatosis type 1. Pediatrics 124 : e476-e483, 2009 https://doi.org/10.1542/peds.2009-0152
  40. Rosser TL, Vezina G, Packer RJ : Cerebrovascular abnormalities in a population of children with neurofibromatosis type 1. Neurology 64 : 553-555, 2005 https://doi.org/10.1212/01.WNL.0000150544.00016.69
  41. Scott RM, Smith ER : Moyamoya disease and moyamoya syndrome. N Engl J Med 360 : 1226-1237, 2009 https://doi.org/10.1056/NEJMra0804622
  42. Seol HJ, Shin DC, Kim YS, Shim EB, Kim SK, Cho BK, et al. : Computational analysis of hemodynamics using a two-dimensional model in moyamoya disease. J Neurosurg Pediatr 5 : 297-301, 2010 https://doi.org/10.3171/2009.10.PEDS09452
  43. Shanahan P, Hutchinson M, Bohan A, O' Donoghue D, Sheahan K, Owens A : Hemichorea, moya-moya, and ulcerative colitis. Mov Disord 16 : 570-572, 2001 https://doi.org/10.1002/mds.1095
  44. Smith ER, Scott RM : Moyamoya : epidemiology, presentation, and diagnosis. Neurosurg Clin N Am 21 : 543-551, 2010 https://doi.org/10.1016/j.nec.2010.03.007
  45. Sobata E, Ohkuma H, Suzuki S : Cerebrovascular disorders associated with von Recklinghausen's neurofibromatosis : a case report. Neurosurgery 22 : 544-549, 1988 https://doi.org/10.1227/00006123-198803000-00016
  46. Suzuki S, Mitsuyama T, Horiba A, Fukushima S, Hashimoto N, Kawamata T : Moyamoya disease complicated by Graves' disease and type 2 diabetes mellitus : report of two cases. Clin Neurol Neurosurg 113 : 325-329, 2011 https://doi.org/10.1016/j.clineuro.2010.11.022
  47. Tanigawara T, Yamada H, Sakai N, Andoh T, Deguchi K, Iwamura M : Studies on cytomegalovirus and Epstein-Barr virus infection in moyamoya disease. Clin Neurol Neurosurg 99 Suppl 2 : S225-S228, 1997
  48. Ullrich NJ, Robertson R, Kinnamon DD, Scott RM, Kieran MW, Turner CD, et al. : Moyamoya following cranial irradiation for primary brain tumors in children. Neurology 68 : 932-938, 2007 https://doi.org/10.1212/01.wnl.0000257095.33125.48
  49. Vis JC, Duffels MG, Winter MM, Weijerman ME, Cobben JM, Huisman SA, et al. : Down syndrome : a cardiovascular perspective. J Intellect Disabil Res 53 : 419-425, 2009 https://doi.org/10.1111/j.1365-2788.2009.01158.x
  50. Williams VC, Lucas J, Babcock MA, Gutmann DH, Korf B, Maria BL : Neurofibromatosis type 1 revisited. Pediatrics 123 : 124-133, 2009 https://doi.org/10.1542/peds.2007-3204
  51. Xu J, Ismat FA, Wang T, Yang J, Epstein JA : NF1 regulates a Ras-dependent vascular smooth muscle proliferative injury response. Circulation 116 : 2148-2156, 2007 https://doi.org/10.1161/CIRCULATIONAHA.107.707752
  52. Yamada H, Deguchi K, Tanigawara T, Takenaka K, Nishimura Y, Shinoda J, et al. : The relationship between moyamoya disease and bacterial infection. Clin Neurol Neurosurg 99 Suppl 2 : S221-S224, 1997
  53. Yamauchi T, Tada M, Houkin K, Tanaka T, Nakamura Y, Kuroda S, et al. : Linkage of familial moyamoya disease (spontaneous occlusion of the circle of Willis) to chromosome 17q25. Stroke 31 : 930-935, 2000 https://doi.org/10.1161/01.STR.31.4.930
  54. Yonekawa Y, Ogata N, Kaku Y, Taub E, Imhof HG : Moyamoya disease in Europe, past and present status. Clin Neurol Neurosurg 99 Suppl 2 : S58-S60, 1997

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