Journal of Korean Neurosurgical Society

The Korean Neurosurgical Society (대한신경외과학회)
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Moyamoya Biomarkers

  • Smith, Edward R. (Department of Neurological Surgery, Boston Children's Hospital and Harvard Medical School)
  • Received : 2015.02.07
  • Accepted : 2015.04.09
  • Published : 2015.06.28
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Abstract

Moyamoya disease (MMD) is an arteriopathy of the intracranial circulation predominantly affecting the branches of the internal carotid arteries. Heterogeneity in presentation, progression and response to therapy has prompted intense study to improve the diagnosis and prognosis of this disease. Recent progress in the development of moyamoya-related biomarkers has stimulated marked interest in this field. Biomarkers can be defined as biologically derived agents-such as specific molecules or unique patterns on imaging-that can identify the presence of disease or help to predict its course. This article reviews the current categories of biomarkers relevant to MMD-including proteins, cells and genes-along with potential limitations and applications for their use.

Keywords

References

  1. Amano T, Inoha S, Wu CM, Matsushima T, Ikezaki K : Serum alpha1-antitrypsin level and phenotype associated with familial moyamoya disease. Childs Nerv Syst 19 : 655-658, 2003 https://doi.org/10.1007/s00381-003-0799-9
  2. Araki Y, Yoshikawa K, Okamoto S, Sumitomo M, Maruwaka M, Wakabayashi T : Identification of novel biomarker candidates by proteomic analysis of cerebrospinal fluid from patients with moyamoya disease using SELDI-TOF-MS. BMC Neurol 10 : 112, 2010 https://doi.org/10.1186/1471-2377-10-112
  3. Baird LC, Smith ER, Ichord R, Piccoli DA, Bernard TJ, Spinner NB, et al. : Moyamoya syndrome associated with Alagille syndrome : outcome after surgical revascularization. J Pediatr 166 : 470-473, 2015 https://doi.org/10.1016/j.jpeds.2014.10.067
  4. Bernard TJ, Fenton LZ, Apkon SD, Boada R, Wilkening GN, Wilkinson CC, et al. : Biomarkers of hypercoagulability and inflammation in childhood-onset arterial ischemic stroke. J Pediatr 156 : 651-656, 2010 https://doi.org/10.1016/j.jpeds.2009.10.034
  5. Choi H, Phi JH, Paeng JC, Kim SK, Lee YS, Jeong JM, et al. : Imaging of integrin $\alpha$(V)$\beta$(3) expression using (68)Ga-RGD positron emission tomography in pediatric cerebral infarct. Mol Imaging 12 : 213-217, 2013
  6. Codd PJ, Scott RM, Smith ER : Seckel syndrome and moyamoya. J Neurosurg Pediatr 3 : 320-324, 2009 https://doi.org/10.3171/2008.12.PEDS08205
  7. Fujimura M, Watanabe M, Narisawa A, Shimizu H, Tominaga T : Increased expression of serum Matrix Metalloproteinase-9 in patients with moyamoya disease. Surg Neurol 72 : 476-480; discussion 480, 2009 https://doi.org/10.1016/j.surneu.2008.10.009
  8. Fujiwara H, Momoshima S, Kuribayashi S : Leptomeningeal high signal intensity (ivy sign) on fluid-attenuated inversion-recovery (FLAIR) MR images in moyamoya disease. Eur J Radiol 55 : 224-230, 2005 https://doi.org/10.1016/j.ejrad.2004.11.009
  9. 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 99 Suppl 2 : S238-S240, 1997
  10. Goda M, Isono M, Ishii K, Kamida T, Abe T, Kobayashi H : Long-term effects of indirect bypass surgery on collateral vessel formation in pediatric moyamoya disease. J Neurosurg 100 (2 Suppl Pediatrics) : 156-162, 2004 https://doi.org/10.3171/ped.2004.100.2.0156
  11. Guo DC, Papke CL, Tran-Fadulu V, Regalado ES, Avidan N, Johnson RJ, et al. : Mutations in smooth muscle alpha-actin (ACTA2) cause coronary artery disease, stroke, and Moyamoya disease, along with thoracic aortic disease. Am J Hum Genet 84 : 617-627, 2009 https://doi.org/10.1016/j.ajhg.2009.04.007
  12. Han H, Pyo CW, Yoo DS, Huh PW, Cho KS, Kim DS : Associations of Moyamoya patients with HLA class I and class II alleles in the Korean population. J Korean Med Sci 18 : 876-880, 2003 https://doi.org/10.3346/jkms.2003.18.6.876
  13. Harada M, Miyoshi H, Uno M, Okada T, Hisaoka S, Hori A, et al. : Neuronal impairment of adult moyamoya disease detected by quantified proton MRS and comparison with cerebral perfusion by SPECT with tc-99m HM-PAO : a trial of clinical quantification of metabolites. J Magn Reson Imaging 10 : 124-129, 1999 https://doi.org/10.1002/(SICI)1522-2586(199908)10:2<124::AID-JMRI3>3.0.CO;2-T
  14. Hishikawa T, Tokunaga K, Sugiu K, Date I : Clinical and radiographic features of moyamoya disease in patients with both cerebral ischaemia and haemorrhage. Br J Neurosurg 27 : 198-201, 2013 https://doi.org/10.3109/02688697.2012.717983
  15. Hojo M, Hoshimaru M, Miyamoto S, Taki W, Nagata I, Asahi M, et al. : Role of transforming growth factor-beta1 in the pathogenesis of moyamoya disease. J Neurosurg 89 : 623-629, 1998 https://doi.org/10.3171/jns.1998.89.4.0623
  16. Hong SH, Wang KC, Kim SK, Cho BK, Park MH : Association of HLA-DR and -DQ genes with familial moyamoya disease in Koreans. J Korean Neurosurg Soc 46 : 558-563, 2009 https://doi.org/10.3340/jkns.2009.46.6.558
  17. 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
  18. 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
  19. Jackson EM, Lin N, Manjila S, Scott RM, Smith ER : Pial synangiosis in patients with moyamoya younger than 2 years of age. J Neurosurg Pediatr 13 : 420-425, 2014 https://doi.org/10.3171/2014.1.PEDS13251
  20. Jung KH, Chu K, Lee ST, Park HK, Kim DH, Kim JH, et al. : Circulating endothelial progenitor cells as a pathogenetic marker of moyamoya disease. J Cereb Blood Flow Metab 28 : 1795-1803, 2008 https://doi.org/10.1038/jcbfm.2008.67
  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. Kang HS, Kim JH, Phi JH, Kim YY, Kim JE, Wang KC, et al. : Plasma matrix metalloproteinases, cytokines and angiogenic factors in moyamoya disease. J Neurol Neurosurg Psychiatry 81 : 673-678, 2010 https://doi.org/10.1136/jnnp.2009.191817
  24. Kang HS, Moon YJ, Kim YY, Park WY, Park AK, Wang KC, et al. : Smooth-muscle progenitor cells isolated from patients with moyamoya disease : novel experimental cell model. J Neurosurg 120 : 415-425, 2014 https://doi.org/10.3171/2013.9.JNS131000
  25. Kashiwagi S, Yamashita T, Katoh S, Kitahara T, Nakashima K, Yasuhara S, et al. : Regression of moyamoya vessels and hemodynamic changes after successful revascularization in childhood moyamoya disease. Acta Neurol Scand Suppl 166 : 85-88, 1996
  26. Kawaguchi S, Sakaki T, Morimoto T, Kakizaki T, Kamada K : Characteristics of intracranial aneurysms associated with moyamoya disease. A review of 111 cases. Acta Neurochir (Wien) 138 : 1287-1294, 1996 https://doi.org/10.1007/BF01411057
  27. Kawashima M, Noguchi T, Takase Y, Nakahara Y, Matsushima T : Decrease in leptomeningeal ivy sign on fluid-attenuated inversion recovery images after cerebral revascularization in patients with Moyamoya disease. AJNR Am J Neuroradiol 31 : 1713-1718, 2010 https://doi.org/10.3174/ajnr.A2124
  28. Kelly ME, Bell-Stephens TE, Marks MP, Do HM, Steinberg GK : Progression of unilateral moyamoya disease : a clinical series. Cerebrovasc Dis 22 : 109-115, 2006 https://doi.org/10.1159/000093238
  29. Kennedy BC, McDowell MM, Yang PH, Wilson CM, Li S, Hankinson TC, et al. : Pial synangiosis for moyamoya syndrome in children with sickle cell anemia : a comprehensive review of reported cases. Neurosurg Focus 36 : E12, 2014
  30. Khan N, Yonekawa Y : Moyamoya angiopathy in Europe. Acta Neurochir Suppl 94 : 149-152, 2005 https://doi.org/10.1007/3-211-27911-3_24
  31. Kim JH, Jung JH, Phi JH, Kang HS, Kim JE, Chae JH, et al. : Decreased level and defective function of circulating endothelial progenitor cells in children with moyamoya disease. J Neurosci Res 88 : 510-518, 2010
  32. Kim SK, Yoo JI, Cho BK, Hong SJ, Kim YK, Moon JA, et al. : Elevation of CRABP-I in the cerebrospinal fluid of patients with Moyamoya disease. Stroke 34 : 2835-2841, 2003 https://doi.org/10.1161/01.STR.0000100159.43123.D7
  33. Kim YI, Phi JH, Paeng JC, Choi H, Kim SK, Lee YS, et al. : In vivo evaluation of angiogenic activity and its correlation with efficacy of indirect revascularization surgery in pediatric moyamoya disease. J Nucl Med 55 : 1467-1472, 2014 https://doi.org/10.2967/jnumed.114.142430
  34. Kirkham FJ, DeBaun MR : Stroke in children with sickle cell disease. Curr Treat Options Neurol 6 : 357, 2004 https://doi.org/10.1007/s11940-996-0028-4
  35. 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
  36. Kuroda S, Hashimoto N, Yoshimoto T, Iwasaki Y; Research Committee on Moyamoya Disease in Japan : Radiological findings, clinical course, and outcome in asymptomatic moyamoya disease : results of multicenter survey in Japan. Stroke 38 : 1430-1435, 2007 https://doi.org/10.1161/STROKEAHA.106.478297
  37. Kuroda S, Ishikawa T, Houkin K, Nanba R, Hokari M, Iwasaki Y : Incidence and clinical features of disease progression in adult moyamoya disease. Stroke 36 : 2148-2453, 2005 https://doi.org/10.1161/01.STR.0000182256.32489.99
  38. Kusaka N, Sugiu K, Tokunaga K, Katsumata A, Nishida A, Namba K, et al. : Enhanced brain angiogenesis in chronic cerebral hypoperfusion after administration of plasmid human vascular endothelial growth factor in combination with indirect vasoreconstructive surgery. J Neurosurg 103 : 882-890, 2005 https://doi.org/10.3171/jns.2005.103.5.0882
  39. Lee JY, Kim SK, Cheon JE, Choi JW, Phi JH, Kim IO, et al. : Posterior cerebral artery involvement in moyamoya disease : initial infarction and angle between PCA and basilar artery. Childs Nerv Syst 29 : 2263-2269, 2013 https://doi.org/10.1007/s00381-013-2123-7
  40. Lin N, Baird L, Koss M, Kopecky KE, Gone E, Ullrich NJ, et al. : Discovery of asymptomatic moyamoya arteriopathy in pediatric syndromic populations : radiographic and clinical progression. Neurosurg Focus 31 : E6, 2011
  41. Liu W, Morito D, Takashima S, Mineharu Y, Kobayashi H, Hitomi T, et al. : Identification of RNF213 as a susceptibility gene for moyamoya disease and its possible role in vascular development. PLoS One 6 : e22542, 2011 https://doi.org/10.1371/journal.pone.0022542
  42. Malek AM, Connors S, Robertson RL, Folkman J, Scott RM : Elevation of cerebrospinal fluid levels of basic fibroblast growth factor in moyamoya and central nervous system disorders. Pediatr Neurosurg 27 : 182-189, 1997 https://doi.org/10.1159/000121249
  43. Maruwaka M, Yoshikawa K, Okamoto S, Araki Y, Sumitomo M, Kawamura A, et al. : Biomarker research for moyamoya disease in cerebrospinal fluid using surface-enhanced laser desorption/ionization time-of-flight mass spectrometry. J Stroke Cerebrovasc Dis 24 : 104-111, 2015 https://doi.org/10.1016/j.jstrokecerebrovasdis.2014.07.028
  44. Masuda J, Ogata J, Yutani C : Smooth muscle cell proliferation and localization of macrophages and T cells in the occlusive intracranial major arteries in moyamoya disease. Stroke 24 : 1960-1967, 1993 https://doi.org/10.1161/01.STR.24.12.1960
  45. 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
  46. 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
  47. Moftakhar P, Smith ER, Choulakian A, Scott RM, Danielpour M : Moyamoya disease in children with congenital dwarfing conditions. Pediatr Neurosurg 46 : 373-380, 2010 https://doi.org/10.1159/000322017
  48. Munot P, Saunders DE, Milewicz DM, Regalado ES, Ostergaard JR, Braun KP, et al. : A novel distinctive cerebrovascular phenotype is associated with heterozygous Arg179 ACTA2 mutations. Brain 135 (Pt 8) : 2506-2514, 2012 https://doi.org/10.1093/brain/aws172
  49. Nanba R, Kuroda S, Ishikawa T, Houkin K, Iwasaki Y : Increased expression of hepatocyte growth factor in cerebrospinal fluid and intracranial artery in moyamoya disease. Stroke 35 : 2837-2842, 2004 https://doi.org/10.1161/01.STR.0000148237.13659.e6
  50. Ni G, Liu W, Huang X, Zhu S, Yue X, Chen Z, et al. : Increased levels of circulating SDF-$1{\alpha}$ and CD34+ CXCR4+ cells in patients with moyamoya disease. Eur J Neurol 18 : 1304-1309, 2011 https://doi.org/10.1111/j.1468-1331.2011.03393.x
  51. Qaiser R, Scott RM, Smith ER : Identification of an association between Robinow syndrome and moyamoya. Pediatr Neurosurg 45 : 69-72, 2009 https://doi.org/10.1159/000204907
  52. Qureshi IA, Mehler MF : Emerging role of epigenetics in stroke : part 1 : DNA methylation and chromatin modifications. Arch Neurol 67 : 1316-1322, 2010
  53. Qureshi IA, Mehler MF : The emerging role of epigenetics in stroke : II. RNA regulatory circuitry. Arch Neurol 67 : 1435-1441, 2010
  54. Roach ES, Golomb MR, Adams R, Biller J, Daniels S, Deveber G, 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 39 : 2644-2691, 2008 https://doi.org/10.1161/STROKEAHA.108.189696
  55. Roder C, Peters V, Kasuya H, Nishizawa T, Wakita S, Berg D, et al. : Analysis of ACTA2 in European Moyamoya disease patients. Eur J Paediatr Neurol 15 : 117-122, 2011 https://doi.org/10.1016/j.ejpn.2010.09.002
  56. Romeo MJ, Espina V, Lowenthal M, Espina BH, Petricoin EF 3rd, Liotta LA : CSF proteome : a protein repository for potential biomarker identification. Expert Rev Proteomics 2 : 57-70, 2005 https://doi.org/10.1586/14789450.2.1.57
  57. Sakurai K, Horiuchi Y, Ikeda H, Ikezaki K, Yoshimoto T, Fukui M, et al. : A novel susceptibility locus for moyamoya disease on chromosome 8q23. J Hum Genet 49 : 278-281, 2004 https://doi.org/10.1007/s10038-004-0143-6
  58. Scott RM, Smith ER : Moyamoya disease and moyamoya syndrome. N Engl J Med 360 : 1226-1237, 2009 https://doi.org/10.1056/NEJMra0804622
  59. 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 100 (2 Suppl Pediatrics) : 142-149, 2004 https://doi.org/10.3171/ped.2004.100.2.0142
  60. Shimojima K, Yamamoto T : ACTA2 is not a major disease-causing gene for moyamoya disease. J Hum Genet 54 : 687-688, 2009 https://doi.org/10.1038/jhg.2009.91
  61. Smith ER, McClain CD, Heeney M, Scott RM : Pial synangiosis in patients with moyamoya syndrome and sickle cell anemia : perioperative management and surgical outcome. Neurosurg Focus 26 : E10, 2009
  62. Smith ER, Scott RM : Progression of disease in unilateral moyamoya syndrome. Neurosurg Focus 24 : E17, 2008
  63. 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 9 : 353-360, 2012 https://doi.org/10.3171/2011.12.PEDS1172
  64. Smith JJ, Sorensen AG, Thrall JH : Biomarkers in imaging : realizing radiology's future. Radiology 227 : 633-638, 2003 https://doi.org/10.1148/radiol.2273020518
  65. Soriano SG, Cowan DB, Proctor MR, Scott RM : Levels of soluble adhesion molecules are elevated in the cerebrospinal fluid of children with moyamoya syndrome. Neurosurgery 50 : 544-549, 2002
  66. Strimbu K, Tavel JA : What are biomarkers? Curr Opin HIV AIDS 5 : 463-466, 2010 https://doi.org/10.1097/COH.0b013e32833ed177
  67. Sugiyama T, Kuroda S, Nakayama N, Tanaka S, Houkin K : Bone marrow-derived endothelial progenitor cells participate in the initiation of moyamoya disease. Neurol Med Chir (Tokyo) 51 : 767-773, 2011 https://doi.org/10.2176/nmc.51.767
  68. Suzuki J, Takaku A : Cerebrovascular "moyamoya" disease. Disease showing abnormal net-like vessels in base of brain. Arch Neurol 20 : 288-299, 1969 https://doi.org/10.1001/archneur.1969.00480090076012
  69. Takahashi A, Sawamura Y, Houkin K, Kamiyama H, Abe H : The cerebrospinal fluid in patients with moyamoya disease (spontaneous occlusion of the circle of Willis) contains high level of basic fibroblast growth factor. Neurosci Lett 160 : 214-216, 1993 https://doi.org/10.1016/0304-3940(93)90416-I
  70. Takeuchi K, Shimizu K : Hypoplasia of the bilateral internal carotid arteries. Brain Nerve 9 : 37-43, 1957
  71. 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
  72. Yamada M, Fujii K, Fukui M : [Clinical features and outcomes in patients with asymptomatic moyamoya disease--from the results of nation-wide questionnaire survey]. No Shinkei Geka 33 : 337-342, 2005
  73. Yanagawa Y, Sugiura T, Suzuki K, Okada Y : Moyamoya disease associated with positive findings for rheumatoid factor and myeloperoxidase-anti-neutrophil cytoplasmic antibody. West Indian Med J 56 : 282-284, 2007
  74. Yoshihara T, Taguchi A, Matsuyama T, Shimizu Y, Kikuchi-Taura A, Soma T, et al. : Increase in circulating CD34-positive cells in patients with angiographic evidence of moyamoya-like vessels. J Cereb Blood Flow Metab 28 : 1086-1089, 2008 https://doi.org/10.1038/jcbfm.2008.1
  75. Yoshimoto T, Houkin K, Takahashi A, Abe H : Angiogenic factors in moyamoya disease. Stroke 27 : 2160-2165, 1996 https://doi.org/10.1161/01.STR.27.12.2160

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