Skip to main content

Advertisement

SpringerLink
Log in

Development and External Validation of Nomogram for Cerebral Infarction in Moyamoya Diseases

  • Original Article
  • Published:
Translational Stroke Research Aims and scope Submit manuscript

Abstract

More than 60% of moyamoya disease (MMD) patients suffers cerebral ischemia and preoperative cerebral infarction (CI) increases the risk of postoperative stroke and unfavorable outcome. We established a nomogram system for risk stratification of CI to help tailoring individualized management. We enrolled 380 patients including 680 hemispheres for the training cohort from our hospital and 183 patients including 348 hemispheres for the validation cohort from multicenter. A nomogram for CI was formulated based on the multivariable logistic regression analysis. The predictive accuracy and discriminative ability of nomogram were determined with concordance index (C-index) and calibration curve. For the training cohort, 246 hemispheres (36.2%) were found with CI. In multivariable logistic regression used generalized estimating equations approach, anterior choroidal artery (AchA) grade (grade 1, OR 0.214, 95%CI 0.124–0.372, P < 0.001; grade 2, OR 0.132, 95%CI 0.066–0.265, P < 0.001), cerebral perfusion (OR 4.796, 95%CI 2.922–7.872; P < 0.001), white matter hyperintensity (OR 3.652, 95%CI 1.933–6.902; P < 0.001), brush sign (OR 3.555, 95%CI 2.282–5.538; P < 0.001), and ivy sign (equivocal, OR 4.752, 95%CI 2.788–8.099, P < 0.001; present, OR 8.940, 95%CI 4.942–16.173, P < 0.001) were significant factors for CI. The C-index of the nomogram for predicting cerebral infarction was 0.890 (95%CI 0.866–0.915) in the training cohort and 0.847 (95%CI 0.805–0.889) in the validation cohort. The nomogram composed of AchA grade, cerebral perfusion, white matter hyperintensity, brush sign, and ivy sign could provide risk stratification of CI before surgery in patients with MMD. Active treatment might be recommended before CI, which could reduce the risk of stroke after surgery.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

Data Availability

Data that support the findings of this study are available from the corresponding author upon reasonable request.

References

  1. Research Committee on the Pathology and Treatment of Spontaneous Occlusion of the Circle of Willis ea. Guidelines for diagnosis and treatment of moyamoya disease (spontaneous occlusion of the circle of Willis). Neurologia Medico-Chirurgica. 2012;52(5):245–66. https://doi.org/10.2176/nmc.52.245.

    Article  Google Scholar 

  2. Cho WS, Chung YS, Kim JE, Jeon JP, Son YJ, Bang JS, Kang HS, Sohn CH, Oh CW. The natural clinical course of hemodynamically stable adult moyamoya disease. J Neurosurg. 2015;122(1):82–9. https://doi.org/10.3171/2014.9.Jns132281.

    Article  PubMed  Google Scholar 

  3. Kraemer M, Heienbrok W, Berlit P. Moyamoya disease in Europeans. Stroke. 2008;39(12):3193–200. https://doi.org/10.1161/strokeaha.107.513408.

    Article  PubMed  Google Scholar 

  4. Jeon JP, Kim JE, Cho WS, Bang JS, Son YJ, Oh CW. Meta-analysis of the surgical outcomes of symptomatic moyamoya disease in adults. J Neurosurg. 2018;128(3):793–9. https://doi.org/10.3171/2016.11.Jns161688.

    Article  PubMed  Google Scholar 

  5. Miyamoto S, Yoshimoto T, Hashimoto N, Okada Y, Tsuji I, Tominaga T, Nakagawara J, Takahashi JC. Effects of extracranial-intracranial bypass for patients with hemorrhagic moyamoya disease: results of the Japan adult moyamoya trial. Stroke. 2014;45(5):1415–21. https://doi.org/10.1161/strokeaha.113.004386.

    Article  PubMed  Google Scholar 

  6. Chen Y, Ma L, Yang S, Burkhardt JK, Lu J, Ye X, Jiang W, Ren Z, Wang R, Chen X, Zhao Y. Quantitative angiographic hemodynamic evaluation after revascularization surgery for moyamoya disease. Transl Stroke Res. 2020;11(5):871–81. https://doi.org/10.1007/s12975-020-00781-5.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  7. Kazumata K, Ito M, Tokairin K, Ito Y, Houkin K, Nakayama N, Kuroda S, Ishikawa T, Kamiyama H. 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. https://doi.org/10.3171/2014.1.Jns13946.

    Article  PubMed  Google Scholar 

  8. Kuroda S, Kashiwazaki D, Hirata K, Shiga T, Houkin K, Tamaki N. Effects of surgical revascularization on cerebral oxygen metabolism in patients with moyamoya disease: an 15O-gas positron emission tomographic study. Stroke. 2014;45(9):2717–21. https://doi.org/10.1161/strokeaha.114.006009.

    Article  PubMed  CAS  Google Scholar 

  9. Yu L, Ma L, Huang Z, Shi Z, Wang R, Zhao Y, Zhang D. Revascularization surgery in patients with ischemic-type moyamoya disease: predictors for postoperative stroke and long-term outcomes. World Neurosurg. 2019;128:e582–96. https://doi.org/10.1016/j.wneu.2019.04.214.

    Article  PubMed  Google Scholar 

  10. Deng X, Gao F, Zhang D, Zhang Y, Wang R, Wang S, Cao Y, Zhao Y, Pan Y, Ye X, Liu X, Zhang Q, Wang J, Yang Z, Zhao M, Zhao J. Effects of different surgical modalities on the clinical outcome of patients with moyamoya disease: a prospective cohort study. J Neurosurg. 2018;128(5):1327–37. https://doi.org/10.3171/2016.12.Jns162626.

    Article  PubMed  Google Scholar 

  11. Suzuki J, Takaku A. Cerebrovascular, “moyamoya” disease. Disease showing abnormal net-like vessels in base of brain. Arch Neurol. 1969;20(3):288–99. https://doi.org/10.1001/archneur.1969.00480090076012.

    Article  PubMed  CAS  Google Scholar 

  12. Morioka M, Hamada J, Kawano T, Todaka T, Yano S, Kai Y, Ushio Y. Angiographic dilatation and branch extension of the anterior choroidal and posterior communicating arteries are predictors of hemorrhage in adult moyamoya patients. Stroke. 2003;34(1):90–5. https://doi.org/10.1161/01.str.0000047120.67507.0d.

    Article  PubMed  Google Scholar 

  13. Fazekas F, Chawluk JB, Alavi A, Hurtig HI, Zimmerman RA. MR Signal abnormalities at 15 T in Alzheimer’s dementia and normal aging. AJR Am J Roentgenol. 1987;149(2):351–6. https://doi.org/10.2214/ajr.149.2.351.

    Article  Google Scholar 

  14. Horie N, Morikawa M, Nozaki A, Hayashi K, Suyama K, Nagata I. “Brush Sign” on susceptibility-weighted MR imaging indicates the severity of moyamoya disease. AJNR Am J Neuroradiol. 2011;32(9):1697–702. https://doi.org/10.3174/ajnr.A2568.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  15. Lu J, Zhao Y, Li M, Ma L, Chen Y, Wang R, Ye X, Wang H, Chen X, Zhao Y. Clinical implications of the “brush sign” in susceptibility-weighted imaging for moyamoya disease. Cerebrovasc Dis (Basel Switzerland). 2021;50(2):147–55. https://doi.org/10.1159/000511936.

    Article  Google Scholar 

  16. Yoon HK, Shin HJ, Chang YW. "Ivy sign" in childhood moyamoya disease: depiction on FLAIR and contrast-enhanced T1-weighted MR images. Radiology. 2002;223(2):384–9.https://doi.org/10.1148/radiol.2232011094

  17. Yin H, Liu X, Zhang D, Zhang Y, Wang R, Zhao M, Zhao J. A novel staging system to evaluate cerebral hypoperfusion in patients with moyamoya disease. Stroke. 2018;49(12):2837–43. https://doi.org/10.1161/strokeaha.118.022628.

    Article  PubMed  Google Scholar 

  18. Jang DK, Lee KS, Rha HK, Huh PW, Yang JH, Park IS, Ahn JG, Sung JH, Han YM. Bypass surgery versus medical treatment for symptomatic moyamoya disease in adults. J Neurosurg. 2017;127(3):492–502. https://doi.org/10.3171/2016.8.Jns152875.

    Article  PubMed  Google Scholar 

  19. Ha EJ, Kim KH, Wang KC, Phi JH, Lee JY, Choi JW, Cho BK, Yang J, Byun YH, Kim SK. Long-term outcomes of indirect bypass for 629 children with moyamoya disease: longitudinal and cross-sectional analysis. Stroke. 2019;50(11):3177–83. https://doi.org/10.1161/strokeaha.119.025609.

    Article  PubMed  Google Scholar 

  20. Nielsen TH, Abhinav K, Sussman ES, Han SS, Weng Y, Bell-Stephens T, Heit JJ, Steinberg GK. Direct versus indirect bypass procedure for the treatment of ischemic moyamoya disease: results of an individualized selection strategy. J Neurosurg. 2020;134(5):1578–89. https://doi.org/10.3171/2020.3.Jns192847.

    Article  PubMed  Google Scholar 

  21. Chen J, Duan L, Xu WH, Han YQ, Cui LY, Gao S. Microembolic signals predict cerebral ischaemic events in patients with moyamoya disease. European J Neurol. 2014;21(5):785–90. https://doi.org/10.1111/ene.12392.

    Article  CAS  Google Scholar 

  22. Kim SK, Cho BK, Phi JH, Lee JY, Chae JH, Kim KJ, Hwang YS, Kim IO, Lee DS, Lee J, Wang KC. Pediatric moyamoya disease: an analysis of 410 consecutive cases. Ann Neurol. 2010;68(1):92–101. https://doi.org/10.1002/ana.21981.

    Article  PubMed  Google Scholar 

  23. Funaki T, Takahashi JC, Houkin K, Kuroda S, Takeuchi S, Fujimura M, Tomata Y, Miyamoto S. High rebleeding risk associated with choroidal collateral vessels in hemorrhagic moyamoya disease: analysis of a nonsurgical cohort in the Japan Adult Moyamoya Trial. J Neurosurg. 2019;130(2):337–673. https://doi.org/10.3171/2017.9.Jns17576.

    Article  Google Scholar 

  24. Jiang H, Ni W, Xu B, Lei Y, Tian Y, Xu F, Gu Y, Mao Y. Outcome in adult patients with hemorrhagic moyamoya disease after combined extracranial-intracranial bypass. J Neurosurg. 2014;121(5):1048–55. https://doi.org/10.3171/2014.7.Jns132434.

    Article  PubMed  Google Scholar 

  25. Pantoni L, Garcia JH. Pathogenesis of leukoaraiosis: a review. Stroke. 1997;28(3):652–9. https://doi.org/10.1161/01.str.28.3.652.

    Article  PubMed  CAS  Google Scholar 

  26. van Swieten JC, van den Hout JH, van Ketel BA, Hijdra A, Wokke JH, van Gijn J. Periventricular lesions in the white matter on magnetic resonance imaging in the elderly. A morphometric correlation with arteriolosclerosis and dilated perivascular spaces. Brain : J Neurol. 1991;114(Pt 2):761–74. https://doi.org/10.1093/brain/114.2.761.

    Article  Google Scholar 

  27. Debette S, Markus HS. The clinical importance of white matter hyperintensities on brain magnetic resonance imaging: systematic review and meta-analysis. BMJ (Clin Res ed). 2010;341:c3666. https://doi.org/10.1136/bmj.c3666.

    Article  Google Scholar 

  28. Akhtar N, Salam A, Kamran S, D’Souza A, Imam Y, Bermejo PG, Wadiwala MF, Own A, ElSotouhy A, Vattoth S, Bourke P, Bhutta Z, Joseph S, Santos M, Khan RA, Shuaib A. Pre-existing small vessel disease in patients with acute stroke from the Middle East, Southeast Asia, and Philippines. Transl Stroke Res. 2018;9(3):274–82. https://doi.org/10.1007/s12975-017-0578-7.

    Article  PubMed  Google Scholar 

  29. Bang OY, Chung JW, Kim DH, Won HH, Yeon JY, Ki CS, Shin HJ, Kim JS, Hong SC, Kim DK, Koizumi A. Moyamoya disease and spectrums of RNF213 vasculopathy. Transl Stroke Res. 2020;11(4):580–9. https://doi.org/10.1007/s12975-019-00743-6.

    Article  PubMed  Google Scholar 

  30. Li SJ, Xiong J, He Y, Xiao YY, Mao DA, Liu LQ. A rare case of pediatric moyamoya disease with reversible white matter lesions in a 3-year-old Chinese girl. Child’s Nerv Syst. 2020;36(1):197–201. https://doi.org/10.1007/s00381-019-04391-x.

    Article  Google Scholar 

  31. Komatsu K, Mikami T, Noshiro S, Miyata K, Wanibuchi M, Mikuni N. Reversibility of white matter hyperintensity by revascularization surgery in Moyamoya disease. J Stroke Cerebrovasc Dis. 2016;25(6):1495–502. https://doi.org/10.1016/j.jstrokecerebrovasdis.2016.02.035.

    Article  PubMed  Google Scholar 

  32. Sun H, Li W, Xia C, Ren Y, Ma L, Xiao A, You C, Wang X, Tian R, Liu Y. Magnetic resonance imaging markers of cerebral small vessel disease in adults with Moyamoya disease. Transl Stroke Res. 2022;13(4):533–42. https://doi.org/10.1007/s12975-021-00973-7

  33. Ohta T, Tanaka H, Kuroiwa T. Diffuse leptomeningeal enhancement, “ivy sign,” in magnetic resonance images of moyamoya disease in childhood: case report. Neurosurgery. 1995;37(5):1009–12. https://doi.org/10.1227/00006123-199511000-00024.

    Article  PubMed  CAS  Google Scholar 

  34. Kawashima M, Noguchi T, Takase Y, Ootsuka T, Kido N, Matsushima T. Unilateral hemispheric proliferation of ivy sign on fluid-attenuated inversion recovery images in moyamoya disease correlates highly with ipsilateral hemispheric decrease of cerebrovascular reserve. AJNR Am J Neuroradiol. 2009;30(9):1709–16. https://doi.org/10.3174/ajnr.A1679.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  35. Kaku Y, Iihara K, Nakajima N, Kataoka H, Fukushima K, Iida H, Hashimoto N. The leptomeningeal ivy sign on fluid-attenuated inversion recovery images in moyamoya disease: positron emission tomography study. Cerebrovasc Dis (Basel Switzerland). 2013;36(1):19–25. https://doi.org/10.1159/000351143.

    Article  Google Scholar 

Download references

Acknowledgements

The authors thank Pro.Aizhong Liu, who is professor of the department of Epidemiology and Health Statistics, Xiangya School of Public Health, Central South University, for providing some advices on statistical analysis.

Funding

This work was supported by the National Natural Science Foundation of China (Grant No. 82001274 to Dr. Huang) and the Natural Science Foundation of Hunan Province of China (Grant No. 2021JJ40994 to Dr. Huang).

Author information

Authors and Affiliations

  1. Department of Neurosurgery, Xiangya Hospital, Central South University, Changsha, 410008, China

    Pan Chen, Ying Wang, Shifu Li, Dong Tang, Fenghua Chen & Zheng Huang

  2. Department of Radiology, Xiangya Hospital, Central South University, Changsha, 410008, China

    Shuai Yang & Feiyue Zeng

  3. Department of Neurosurgery, Beijing Tiantan Hospital, Capital Medical University, Beijing, 100070, China

    Lebao Yu & Dong Zhang

  4. Department of Neurosurgery, Hunan Children’s Hospital, Changsha, 410007, China

    Wei Ding & Shuihua Wu

Authors
  1. Pan Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ying Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Shifu Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Dong Tang
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Shuai Yang
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Feiyue Zeng
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Lebao Yu
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Dong Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Wei Ding
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Shuihua Wu
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Fenghua Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Zheng Huang
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Zheng Huang.

Ethics declarations

Ethics Approval

All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki Declaration and its later amendments or comparable ethical standards. The study was approved by the institutional review board of Xiangya Hospital.

Consent to Participate

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

Competing Interests

The authors declare that they have no competing interests.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 2.29 MB)

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Chen, P., Wang, Y., Li, S. et al. Development and External Validation of Nomogram for Cerebral Infarction in Moyamoya Diseases. Transl. Stroke Res. 14, 890–898 (2023). https://doi.org/10.1007/s12975-023-01127-7

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12975-023-01127-7

Keywords

Search

Navigation