Advertisement

Child's Nervous System

, Volume 35, Issue 2, pp 309–314 | Cite as

Posterior circulation involvement and collateral flow pattern in moyamoya disease with the RNF213 polymorphism

  • Won-Hyung Kim
  • Sang-Dae KimEmail author
  • Myung-Hyun Nam
  • Jin-Man Jung
  • Sung-Won Jin
  • Sung-Kon Ha
  • Dong-Jun Lim
  • Hae-Bin Lee
Original Paper

Abstract

Purpose

Moyamoya disease is a chronic cerebrovascular disorder characterized by progressive stenosis of the circle of Willis with a compensatory collateral vessel network. Recent studies have identified the ring finger protein 213 gene (RNF213) as the unique susceptibility gene for moyamoya disease. The purpose of this study was to compare clinical features of moyamoya disease, especially angiographic findings, between patients with and without the RNF213 mutation.

Methods

Blood samples from 35 patients with moyamoya disease were obtained between May 2016 and May 2017. Information on age at the time of diagnosis, sex, and initial symptom were obtained via retrospective chart review. Angiographic records were evaluated.

Results

RNF213 variants were detected in the 28 of 35 patients (80%), including all pediatric patients (100%) and 18 of 25 adult patients (72%) in our cohort. Leptomeningeal collateral flow from posterior to anterior circulation was more frequent in the RNF213-negative group than in the RNF213-positive group (100% versus 38.9%; p = 0.020). Posterior cerebral arterial territorial involvement was more frequently observed in RNF213-positive patients than in RNF213-negative patients (50% versus 0%; p = 0.027).

Conclusions

RNF213 may play a significant role in the development of collateral anastomoses.

Keywords

RNF213 Moyamoya disease Cerebrovascular disorder Collateral anastomoses 

Notes

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Informed consent

Informed consent was obtained from all individual participants included in the study.

References

  1. 1.
    Ahn IM, Park DH, Hann HJ, Kim KH, Kim HJ, Ahn HS (2014) Incidence, prevalence, and survival of moyamoya disease in Korea: a nationwide, population-based study. Stroke 45:1090–1095.  https://doi.org/10.1161/STROKEAHA.113.004273 CrossRefGoogle Scholar
  2. 2.
    Amin-Hanjani S, Singh A, Rifai H, Thulborn KR, Alaraj A, Aletich V, Charbel FT (2013) Combined direct and indirect bypass for moyamoya: quantitative assessment of direct bypass flow over time. Neurosurgery 73:962–968CrossRefGoogle Scholar
  3. 3.
    Fujimura M, Sonobe S, Nishijima Y, Niizuma K, Sakata H, Kure S, Tominaga T (2014) Genetics and biomarkers of moyamoya disease: significance of RNF213 as a susceptibility gene. J Stroke 16:65–72.  https://doi.org/10.5853/jos.2014.16.2.65 CrossRefGoogle Scholar
  4. 4.
    Fukui M (1997) Guidelines for the diagnosis and treatment of spontaneous occlusion of the circle of Willis (‘moyamoya’ disease). Clin Neurol Neurosurg 99:S238–S240CrossRefGoogle Scholar
  5. 5.
    Hishikawa T, Tokunaga K, Sugiu K, Date I (2013) Assessment of the difference in posterior circulation involvement between pediatric and adult patients with moyamoya disease. J Neurosurg 119:961–965.  https://doi.org/10.3171/2013.6.JNS122099 CrossRefGoogle Scholar
  6. 6.
    Hishikawa T, Tokunaga K, Sugiu K, Date I (2013) Clinical and radiographic features of moyamoya disease in patients with both cerebral ischaemia and haemorrhage. Br J Neurosurg 27:198–201CrossRefGoogle Scholar
  7. 7.
    Hishikawa T, Tokunaga K, Sugiu K, Date I (2014) Long-term outcomes in adult patients with ischemic-type moyamoya disease involving posterior circulation. Acta Neurochir 156:1745–1751.  https://doi.org/10.1007/s00701-014-2136-3 CrossRefGoogle Scholar
  8. 8.
    Imai H, Miyawaki S, Ono H, Nakatomi H, Yoshimoto Y, Saito N (2015) The importance of encephalo-myo-synangiosis in surgical revascularization strategies for moyamoya disease in children and adults. World Neurosurg 83:691–699.  https://doi.org/10.1016/j.wneu.2015.01.016 CrossRefGoogle Scholar
  9. 9.
    Ito A, Fujimura M, Niizuma K, Kanoke A, Sakata H, Morita-Fujimura Y, Kikuchi A, Kure S, Tominaga T (2015) Enhanced post-ischemic angiogenesis in mice lacking RNF213; a susceptibility gene for moyamoya disease. Brain Res 1594:310–320.  https://doi.org/10.1016/j.brainres.2014.11.014 CrossRefGoogle Scholar
  10. 10.
    Kamada F, Aoki Y, Narisawa A, Abe Y, Komatsuzaki S, Kikuchi A, Kanno J, Niihori T, Ono M, Ishii N (2011) A genome-wide association study identifies RNF213 as the first moyamoya disease gene. J Hum Genet 56:34–40CrossRefGoogle Scholar
  11. 11.
    Karasawa J, Kikuchi H, Furuse S, Kawamura J, Sakaki T (1978) Treatment of moyamoya disease with STA-MCA anastomosis. J Neurosurg 49:679–688CrossRefGoogle Scholar
  12. 12.
    Kim J-M, Lee S-H, Roh J-K (2009) Changing ischaemic lesion patterns in adult moyamoya disease. J Neurol Neurosurg Psychiatry 80:36–40CrossRefGoogle Scholar
  13. 13.
    Kim T, Lee H, Bang JS, Kwon O-K, Hwang G, Oh CW (2015) Epidemiology of moyamoya disease in Korea: based on national health insurance service data. J Korean Neurosurg Soc 57:390–395CrossRefGoogle Scholar
  14. 14.
    Kim EH, Yum MS, Ra YS, Park JB, Ahn JS, Kim GH, Goo HW, Ko TS, Yoo HW (2016) Importance of RNF213 polymorphism on clinical features and long-term outcome in moyamoya disease. J Neurosurg 124:1221–1227.  https://doi.org/10.3171/2015.4.JNS142900 CrossRefGoogle Scholar
  15. 15.
    Kim DY, Son JP, Yeon JY, Kim GM, Kim JS, Hong SC, Bang OY (2017) Infarct pattern and collateral status in adult moyamoya disease: a multimodal magnetic resonance imaging study. Stroke 48:111–116.  https://doi.org/10.1161/STROKEAHA.116.014529 CrossRefGoogle Scholar
  16. 16.
    Koizumi A, Kobayashi H, Liu W, Fujii Y, Senevirathna ST, Nanayakkara S, Okuda H, Hitomi T, Harada KH, Takenaka K, Watanabe T, Shimbo S (2013) P.R4810K, a polymorphism of RNF213, the susceptibility gene for moyamoya disease, is associated with blood pressure. Environ Health Prev Med 18:121–129.  https://doi.org/10.1007/s12199-012-0299-1 CrossRefGoogle Scholar
  17. 17.
    Kuroda S, Ishikawa T, Houkin K, Iwasaki Y (2002) Clinical significance of posterior cerebral artery stenosis/occlusion in moyamoya disease. No shinkei geka Neurol Surg 30:1295–1300Google Scholar
  18. 18.
    Liu W, Morito D, Takashima S, Mineharu Y, Kobayashi H, Hitomi T, Hashikata H, Matsuura N, Yamazaki S, Toyoda A (2011) Identification of RNF213 as a susceptibility gene for moyamoya disease and its possible role in vascular development. PLoS One 6:e22542CrossRefGoogle Scholar
  19. 19.
    Liu W, Hitomi T, Kobayashi H, Harada KH, Koizumi A (2012) Distribution of moyamoya disease susceptibility polymorphism p. R4810K in RNF213 in East and Southeast Asian populations. Neurol Med Chir 52:299–303CrossRefGoogle Scholar
  20. 20.
    Matsushima T, Fukui M, Kitamura K, Hasuo K, Kuwabara Y, Kurokawa T (1990) Encephalo-duro-arterio-synangiosis in children with moyamoya disease. Acta Neurochir 104:96–102CrossRefGoogle Scholar
  21. 21.
    Miyamoto S, Kikuchi H, Karasawa J, Nagata I, Ikota T, Takeuchi S (1984) Study of the posterior circulation in moyamoya disease: clinical and neuroradiological evaluation. J Neurosurg 61:1032–1037CrossRefGoogle Scholar
  22. 22.
    Miyawaki S, Imai H, Shimizu M, Yagi S, Ono H, Mukasa A, Nakatomi H, Shimizu T, Saito N (2013) Genetic variant RNF213 c.14576G>A in various phenotypes of intracranial major artery stenosis/occlusion. Stroke 44:2894–2897.  https://doi.org/10.1161/STROKEAHA.113.002477 CrossRefGoogle Scholar
  23. 23.
    Mugikura S, Takahashi S, Higano S, Shirane R, Kurihara N, Furuta S, Ezura M, Takahashi A (1999) The relationship between cerebral infarction and angiographic characteristics in childhood moyamoya disease. Am J Neuroradiol 20:336–343Google Scholar
  24. 24.
    Mugikura S, Takahashi S, Higano S, Shirane R, Sakurai Y, Yamada S (2002) Predominant involvement of ipsilateral anterior and posterior circulations in moyamoya disease. Stroke 33:1497–1500CrossRefGoogle Scholar
  25. 25.
    Storey A, Michael Scott R, Robertson R, Smith E (2017) Preoperative transdural collateral vessels in moyamoya as radiographic biomarkers of disease. J Neurosurg Pediatr 19:289–295CrossRefGoogle Scholar
  26. 26.
    Suzuki J, Kodama N (1983) Moyamoya disease--a review. Stroke 14:104–109CrossRefGoogle Scholar
  27. 27.
    Suzuki J, Takaku A (1969) Cerebrovascular moyamoya disease: disease showing abnormal net-like vessels in base of brain. Arch Neurol 20:288–299CrossRefGoogle Scholar
  28. 28.
    Yamada I, Himeno Y, Suzuki S, Matsushima Y (1995) Posterior circulation in moyamoya disease: angiographic study. Radiology 197:239–246CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Department of NeurosurgeryKorea University Medical Center, Ansan HospitalAnsanSouth Korea
  2. 2.Department of Laboratory MedicineKorea University Medical Center, Ansan HospitalAnsanSouth Korea
  3. 3.Department of NeurologyKorea University Medical Center, Ansan HospitalAnsanSouth Korea

Personalised recommendations