Skip to main content

Advertisement

Log in

Association of intracranial vessel wall enhancement and cerebral hemorrhage in moyamoya disease: a high-resolution magnetic resonance imaging study

  • Original Communication
  • Published:
Journal of Neurology Aims and scope Submit manuscript

Abstract

Background and purpose

This study aimed to investigate the enhancement characteristics of vessel wall in patients with moyamoya disease (MMD) using 3D high-resolution magnetic resonance (MR) imaging and their relationship with initial and recurrent intracranial hemorrhage.

Methods

Consecutive patients with MMD were retrospectively analyzed and classified as intracranial hemorrhagic and non-hemorrhagic groups according to the CT or MR images. The clinical features and vessel wall characteristics were compared between the two groups. Logistic regression was performed to relate the vessel wall characteristics to the initial hemorrhage in MMD patients. Patients in hemorrhagic group were followed up after surgery to evaluate the relationship between vessel wall characteristics and recurrent hemorrhage.

Results

A total of 507 MMD patients including 79 hemorrhagic and 428 non-hemorrhagic MMD patients were recruited in the study. We found that hemorrhagic group had more patients with vessel wall enhancements (40.5% vs. 25.7%, p = 0.009) and more eccentric enhanced lesions (17.7% vs. 6.5%, p = 0.001) compared to those in non-hemorrhage group and vessel wall enhancements were independently associated with ipsilateral initial hemorrhage after adjusted for clinical factors (OR = 1.99, CI 1.20–3.28, p = 0.007). Furthermore, three recurrent intracranial hemorrhagic episodes in the present study were all observed in MMD patients with vessel wall enhancement during the long-term follow-up after surgery.

Conclusions

Wall enhancement of intracranial vessels was significantly associated with intracranial hemorrhage in MMD patients. Our findings suggest that vessel wall enhancement may serve as a marker of intracranial hemorrhage.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

Abbreviations

MMD:

Moyamoya disease

HRMRI:

High-resolution magnetic resonance vessel wall imaging

MRI:

Magnetic resonance imaging

SAH:

Subarachnoid hemorrhage

ICH:

Intraparenchymal hemorrhage

IVH:

Intraventricular hemorrhage

ICA:

Internal carotid artery

MCA:

Middle cerebral artery

ACA:

Anterior cerebral artery

References

  1. Research Committee on the Pathology and Treatment of Spontaneous Occlusion of the Circle of Willis (2012) Health labour sciences research grant for research on measures for infractable diseases. Guidelines for diagnosis and treatment of moyamoya disease (spontaneous occlusion of the circle of willis). Neurol Med Chir (Tokyo) 52:245–266. https://doi.org/10.2176/nmc.52.245

    Article  Google Scholar 

  2. Khan NI, Saherwala AA, Chen M, Salehian S, Salahuddin H, Welch BG et al (2019) Prevalence of and risk factors for cerebral microbleeds in moyamoya disease and syndrome in the american population. Cerebrovasc Dis Extra 9:139–147. https://doi.org/10.1159/000504530

    Article  PubMed  PubMed Central  Google Scholar 

  3. Wan M, Han C, Xian P, Yang WZ, Li DS et al (2015) Moyamoya disease presenting with subarachnoid hemorrhage: Clinical features and neuroimaging of a case series. Br J Neurosurg 29:804–810. https://doi.org/10.3109/02688697.2015.1071327

    Article  PubMed  Google Scholar 

  4. Liu P, Liu AH, Han C, Chen C, Lv XL, Li DS et al (2016) Difference in angiographic characteristics between hemorrhagic and nonhemorrhagic hemispheres associated with hemorrhage risk of moyamoya disease in adults: a self-controlled study. World Neurosurg 95:348–356. https://doi.org/10.1016/j.wneu.2016.08.033

    Article  PubMed  Google Scholar 

  5. Liu P, Han C, Li DS, Lv XL, Li YX et al (2016) Hemorrhagic moyamoya disease in children: clinical, angiographic features, and long-term surgical outcome. Stroke 47:240–243. https://doi.org/10.1161/STROKEAHA.115.010512

    Article  PubMed  Google Scholar 

  6. Liu W, Zhu S, Wang X, Yue X, Zhou Z, Wang H et al (2011) Evaluation of angiographic changes of the anterior choroidal and posterior communicating arteries for predicting cerebrovascular lesions in adult moyamoya disease. J Clin Neurosci 18:374–378. https://doi.org/10.1016/j.jocn.2010.05.032

    Article  CAS  PubMed  Google Scholar 

  7. Morioka M, Hamada J, Kawano T, Todaka T, Yano S, Kai Y et al (2003) Angiographic dilatation and branch extension of the anterior choroidal and posterior communicating arteries are predictors of hemorrhage in adult moyamoya patients. Stroke 34:90–95. https://doi.org/10.1161/01.str.0000047120.67507.0d

    Article  PubMed  Google Scholar 

  8. Han C, Li ML, Xu YY, Ye T, Xie CF, Gao S et al (2016) Adult moyamoya-atherosclerosis syndrome: Clinical and vessel wall imaging features. J Neurol Sci 369:181–184. https://doi.org/10.1016/j.jns.2016.08.020

    Article  PubMed  Google Scholar 

  9. Wu F, Han C, Liu Y, Liu Z, Yang X, Wu Y et al (2021) Validation of choroidal anastomosis on high-resolution magnetic resonance imaging as an imaging biomarker in hemorrhagic moyamoya disease. Eur Radiol. https://doi.org/10.1007/s00330-020-07479-0

    Article  PubMed  PubMed Central  Google Scholar 

  10. Ya J, Zhou D, Ding J, Ding Y, Ji X, Yang Q et al (2020) High-resolution combined arterial spin labeling MR for identifying cerebral arterial stenosis induced by moyamoya disease or atherosclerosis. Ann Transl Med 8:87. https://doi.org/10.21037/atm.2019.12.140

    Article  PubMed  PubMed Central  Google Scholar 

  11. Muraoka S, Araki Y, Taoka T, Kawai H, Okamoto S, Uda K et al (2018) Prediction of intracranial arterial stenosis progression in patients with moyamoya vasculopathy: contrast-enhanced high-resolution magnetic resonance vessel wall imaging. World Neurosurg 116:e1114–e1121. https://doi.org/10.1016/j.wneu.2018.05.181

    Article  PubMed  Google Scholar 

  12. Chen XY, Wong KS, Lam WW, Zhao HL, Ng HK (2008) Middle cerebral artery atherosclerosis: histological comparison between plaques associated with and not associated with infarct in a postmortem study. Cerebrovasc Dis 25:74–80. https://doi.org/10.1159/000111525

    Article  PubMed  Google Scholar 

  13. Wang M, Yang Y, Zhou F, Li M, Liu R, Guan M et al (2017) The contrast enhancement of intracranial arterial wall on high-resolution MRI and its clinical relevance in patients with moyamoya vasculopathy. Sci Rep 7:44264. https://doi.org/10.1038/srep44264

    Article  PubMed  PubMed Central  Google Scholar 

  14. Bley TA, Uhl M, Venhoff N, Thoden J, Langer M, Markl M (2007) 3T MRI reveals cranial and thoracic inflammatory changes in giant cell arteritis. Clin Rheumatol 26:448–450. https://doi.org/10.1007/s10067-005-0160-7

    Article  CAS  PubMed  Google Scholar 

  15. Zhao S, Liu W, Feng C, Zhang X, Cai W, Luo M (2020) Effect and molecular mechanisms of collateral vessel growth mediated by activation of transient receptor potential vanilloid type 1. J Vasc Res 57:185–194. https://doi.org/10.1159/000506516

    Article  CAS  PubMed  Google Scholar 

  16. Natori T, Sasaki M, Miyoshi M, Ito K, Ohba H, Miyazawa H et al (2016) Intracranial plaque characterization in patients with acute ischemic stroke using pre- and post-contrast three-dimensional magnetic resonance vessel wall imaging. J Stroke Cerebrovasc Dis 25:1425–1430. https://doi.org/10.1016/j.jstrokecerebrovasdis.2015.12.032

    Article  PubMed  Google Scholar 

  17. Ryoo S, Cha J, Kim SJ, Choi JW, Ki CS, Kim KH et al (2014) High-resolution magnetic resonance wall imaging findings of Moyamoya disease. Stroke 45:2457–2460. https://doi.org/10.1161/STROKEAHA.114.004761

    Article  PubMed  Google Scholar 

  18. Yu LB, Zhang Q, Shi ZY, Wang MQ, Zhang D (2015) High-resolution magnetic resonance imaging of moyamoya disease. Chin Med J (Engl) 128:3231–3237. https://doi.org/10.4103/0366-6999.170257

    Article  Google Scholar 

  19. Kathuveetil A, Sylaja PN, Senthilvelan S, Kesavadas C, Banerjee M, Jayanand Sudhir B (2020) vessel wall thickening and enhancement in high-resolution intracranial vessel wall imaging: a predictor of future ischemic events in moyamoya disease. AJNR Am J Neuroradiol 41:100–105. https://doi.org/10.3174/ajnr.A6360

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Hirano Y, Miyawaki S, Imai H, Hongo H, Ohara K, Dofuku S et al (2020) Association between the onset pattern of adult moyamoya disease and risk factors for stroke. Stroke 51:3124–3128. https://doi.org/10.1161/STROKEAHA.120.030653

    Article  CAS  PubMed  Google Scholar 

  21. Samaniego EA, Roa JA, Zhang H, Koscik TR, Ortega-Gutierrez S, Bathla G et al (2020) Increased contrast enhancement of the parent vessel of unruptured intracranial aneurysms in 7T MR imaging. J Neurointerv Surg 12:1018–1022. https://doi.org/10.1136/neurintsurg-2020-015915

    Article  PubMed  Google Scholar 

  22. Willemink MJ, Coolen BF, Dyvorne H, Robson PM, Bander I, Ishino S et al (2020) Ultra-high resolution, 3-dimensional magnetic resonance imaging of the atherosclerotic vessel wall at clinical 7T. PLoS ONE 15:e0241779. https://doi.org/10.1371/journal.pone.0241779

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgments

This study was supported by the grants of National Natural Science Foundation of China (82001774), Beijing Natural Science Foundation (7212100) and Beijing Science and Technology Project (Z161100000516194).

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Cong Han or Jianming Cai.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical standards

This study has been approved by the appropriate ethics committee and has therefore been performed in accordance with the ethical standards laid down in the 1964 Declaration of Helsinki and its later amendments. All persons gave their informed consent prior to their inclusion in the study.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Lu, M., Zhang, H., Liu, D. et al. Association of intracranial vessel wall enhancement and cerebral hemorrhage in moyamoya disease: a high-resolution magnetic resonance imaging study. J Neurol 268, 4768–4777 (2021). https://doi.org/10.1007/s00415-021-10587-6

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00415-021-10587-6

Keywords

Navigation