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Validation of choroidal anastomosis on high-resolution magnetic resonance imaging as an imaging biomarker in hemorrhagic moyamoya disease

  • Magnetic Resonance
  • Published:
European Radiology Aims and scope Submit manuscript

Abstract

Objectives

This study aimed to investigate the association between dilation and proliferation and anastomosis of perforating arteries, and intracranial hemorrhage in moyamoya disease (MMD) patients, using high-resolution magnetic resonance imaging (HRMRI).

Methods

Adult patients with MMD at advanced stages were prospectively enrolled and underwent HRMRI exams. Dilation and proliferation of the lenticulostriate artery (LSA), medullary artery, and anterior or posterior choroidal arteries (AChA or PChA) were assessed. Abnormal anastomoses were identified between (1) the LSA and the medullary or insular arteries; (2) the thalamo-geniculate, thalamo-tuberal, or thalamo-perforating arteries and the medullary or insular arteries; and (3) the AChA or PChA and the medullary or insular arteries. The association between these variables and hemorrhagic events was calculated using univariate and multivariate analyses.

Results

Fifty patients (14 men; mean age, 35.4 ± 9.7 years) were finally analyzed, including 17 hemorrhagic patients and 33 non-hemorrhagic patients. The inter-rater agreement for the qualitative evaluation of perforating arteries was good. Dilation and proliferation of the AChA or PChA (88.2% versus 54.5%, p = 0.027), and choroidal anastomosis (64.7% versus 18.2%, p = 0.002) were more frequently observed in patients with hemorrhage. Multivariate logistic regression showed that choroidal anastomosis remained significantly associated with hemorrhage (odds ratio = 5.95, 95% confidence interval = 1.21–29.25, p = 0.028).

Conclusions

Choroidal anastomosis is independently associated with hemorrhagic events in adult patients with MMD at advanced stages. HRMRI can provide detailed information on both the anatomies and abnormal collaterals in MMD, which facilitates risk estimates of bleeding in MMD.

Key Points

• High-resolution magnetic resonance imaging allows for the evaluation of perforating arteries in patients with moyamoya disease.

• Choroidal anastomosis is associated with hemorrhagic events in patients with moyamoya disease.

• High-resolution magnetic resonance imaging might facilitate further grading and classification of moyamoya vessels.

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Abbreviations

3D:

Three-dimensional

3 T:

3 Tesla

AChA:

Anterior choroidal artery

CI:

Confidence interval

CT:

Computed tomography

DSA:

Digital subtraction angiography

DWI:

Diffusion-weighted imaging

HRMRI:

High-resolution magnetic resonance imaging

IR:

Inversion recovery

LSA:

Lenticulostriate artery

MCA:

Middle cerebral artery

MMD:

Moyamoya disease

OR:

Odds ratio

PChA:

Posterior choroidal artery

SPACE:

Sampling Perfection with Application-optimized Contrast using different flip angle Evolutions

SWI:

Susceptibility-weighted imaging

TOF-MRA:

Time-of-flight magnetic resonance angiography

References

  1. Research Committee on the Pathology and Treatment of Spontaneous Occlusion of the Circle of Willis; Health Labour Sciences Research Grant for Research on Measures for Infractable Diseases (2012) Guidelines for diagnosis and treatment of moyamoya disease (spontaneous occlusion of the circle of Willis). Neurol Med Chir (Tokyo) 52:245–266

    Article  Google Scholar 

  2. Kuroda S, Houkin K (2008) Moyamoya disease: current concepts and future perspectives. Lancet Neurol 7:1056–1066

    Article  Google Scholar 

  3. Takahashi JC, Funaki T, Houkin K et al (2016) Significance of the hemorrhagic site for recurrent bleeding: prespecified analysis in the Japan Adult Moyamoya Trial. Stroke 47:37–43

    Article  Google Scholar 

  4. Kang S, Liu X, Zhang D et al (2019) Natural course of moyamoya disease in patients with prior hemorrhagic stroke. Stroke 50:1060–1066

    Article  Google Scholar 

  5. Kahn A, Kaur G, Stein L, Tuhrim S, Dhamoon MS (2018) Treatment course and outcomes after revascularization surgery for moyamoya disease in adults. J Neurol 265:2666–2671

    Article  Google Scholar 

  6. Iwama T, Morimoto M, Hashimoto N, Goto Y, Todaka T, Sawada M (1997) Mechanism of intracranial rebleeding in moyamoya disease. Clin Neurol Neurosurg 99(Suppl 2):S187–S190

    Article  Google Scholar 

  7. Irikura K, Miyasaka Y, Kurata A et al (1996) A source of haemorrhage in adult patients with moyamoya disease: the significance of tributaries from the choroidal artery. Acta Neurochir (Wien) 138:1282–1286

    Article  CAS  Google Scholar 

  8. Morioka M, Hamada J, Kawano T 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

    Article  Google Scholar 

  9. Yamamoto S, Hori S, Kashiwazaki D, Akioka N, Kuwayama N, Kuroda S (2018) Longitudinal anterior-to-posterior shift of collateral channels in patients with moyamoya disease: an implication for its hemorrhagic onset. J Neurosurg 130:884–890

    Article  Google Scholar 

  10. Funaki T, Takahashi JC, Yoshida K et al (2016) Periventricular anastomosis in moyamoya disease: detecting fragile collateral vessels with MR angiography. J Neurosurg 124:1766–1772

    Article  Google Scholar 

  11. Mandell DM, Mossa-Basha M, Qiao Y et al (2017) Intracranial vessel wall MRI: principles and expert consensus recommendations of the American Society of Neuroradiology. AJNR Am J Neuroradiol 38:218–229

    Article  CAS  Google Scholar 

  12. Zhang Z, Fan Z, Kong Q et al (2019) Visualization of the lenticulostriate arteries at 3 T using black-blood T1-weighted intracranial vessel wall imaging: comparison with 7 T TOF-MRA. Eur Radiol 29:1452–1459

    Article  Google Scholar 

  13. Mossa-Basha M, de Havenon A, Becker KJ et al (2016) Added value of vessel wall magnetic resonance imaging in the differentiation of moyamoya vasculopathies in a non-Asian Cohort. Stroke 47:1782–1788

    Article  Google Scholar 

  14. Suzuki J, Takaku A (1969) Cerebrovascular “moyamoya” disease. Disease showing abnormal net-like vessels in base of brain. Arch Neurol 20:288–299

    Article  CAS  Google Scholar 

  15. Miyakoshi A, Funaki T, Fushimi Y et al (2019) Identification of the bleeding point in hemorrhagic moyamoya disease using fusion images of susceptibility-weighted imaging and time-of-flight MRA. AJNR Am J Neuroradiol 40:1674–1680

    CAS  PubMed  PubMed Central  Google Scholar 

  16. Liu W, Zhu S, Wang X 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

    Article  CAS  Google Scholar 

  17. Funaki T, Fushimi Y, Takahashi JC et al (2015) Visualization of periventricular collaterals in moyamoya disease with flow-sensitive black-blood magnetic resonance angiography: preliminary experience. Neurol Med Chir (Tokyo) 55:204–209

    Article  Google Scholar 

  18. Okuchi S, Okada T, Fujimoto K et al (2014) Visualization of lenticulostriate arteries at 3 T: optimization of slice-selective off-resonance sinc pulse-prepared TOF-MRA and its comparison with flow-sensitive black-blood MRA. Acad Radiol 21:812–816

    Article  Google Scholar 

  19. Ma SJ, Sarabi MS, Yan L et al (2019) Characterization of lenticulostriate arteries with high resolution black-blood T1-weighted turbo spin echo with variable flip angles at 3 and 7Tesla. Neuroimage 199:184–193

    Article  Google Scholar 

  20. Funaki T, Takahashi JC, Houkin K et al (2018) Angiographic features of hemorrhagic moyamoya disease with high recurrence risk: a supplementary analysis of the Japan Adult Moyamoya Trial. J Neurosurg 128:777–784

    Article  Google Scholar 

  21. Takagi Y, Kikuta K, Nozaki K et al (2007) Expression of hypoxia-inducing factor-1 alpha and endoglin in intimal hyperplasia of the middle cerebral artery of patients with moyamoya disease. Neurosurgery 60:338–345 discussion 345

    Article  Google Scholar 

  22. Yamashita M, Oka K, Tanaka K (1983) Histopathology of the brain vascular network in moyamoya disease. Stroke 14:50–58

    Article  CAS  Google Scholar 

  23. Matsushige T, Kraemer M, Schlamann M et al (2016) Ventricular microaneurysms in moyamoya angiopathy visualized with 7 T MR angiography. AJNR Am J Neuroradiol 37:1669–1672

    Article  CAS  Google Scholar 

  24. Rhim JK, Cho YD, Jeon JP et al (2018) Ruptured aneurysms of collateral vessels in adult onset moyamoya disease with hemorrhagic presentation. Clin Neuroradiol 28:191–199

    Article  Google Scholar 

  25. Togao O, Hiwatashi A, Obara M et al (2018) 4D ASL-based MR angiography for visualization of distal arteries and leptomeningeal collateral vessels in moyamoya disease: a comparison of techniques. Eur Radiol 28:4871–4881

    Article  Google Scholar 

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Funding

This study has received funding by the Funds for International Cooperation and Exchange of the National Natural Science Foundation of China (81961128030), Beijing Talent Training (2018000020124G147), Beijing Nova Program Foundation (Z181100006218108), and the Beijing Natural Science Foundation (L172043).

Author information

Author notes

  1. Fang Wu and Cong Han contributed equally to this work.

Authors and Affiliations

  1. Department of Radiology, Xuanwu Hospital, Capital Medical University, Beijing, China

    Fang Wu, Yuehong Liu, Xiaoxu Yang, Jingwen Du, Yu Wu & Qi Yang

  2. Department of Neurosurgery, the Fifth Medical Centre of PLA General Hospital, Beijing, China

    Cong Han & Lian Duan

  3. Department of Neurosurgery, the General Hospital of Central Theater Command, Wuhan, Hubei, China

    Zhiwen Liu

  4. Department of Radiology, Aerospace Center Hospital, Beijing, China

    Ye Wu

  5. Department of Radiology, University of Cagliari, Cagliari, Italy

    Luca Saba

  6. Department of Neurology, Xuanwu Hospital, Capital Medical University, Beijing, China

    Qian Zhang

  7. Biomedical Imaging Research Institute, Cedars-Sinai Medical Center, and Departments of Medicine and Bioengineering, University of California, Los Angeles, CA, USA

    Zhaoyang Fan & Debiao Li

Authors
  1. Fang Wu
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  2. Cong Han
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Corresponding authors

Correspondence to Lian Duan or Qi Yang.

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The scientific guarantor of this publication is Qi Yang.

Conflict of interest

The authors of this manuscript declare no relationships with any companies, whose products or services may be related to the subject matter of the article.

Statistics and biometry

No complex statistical methods were necessary for this paper.

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Written informed consent was obtained from all subjects (patients) in this study.

Written informed consent was waived by the Institutional Review Board.

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Institutional Review Board approval was obtained.

Methodology

• prospective

• cross-sectional study/diagnostic or prognostic study/observational

• performed at one institution

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Wu, F., Han, C., Liu, Y. et al. Validation of choroidal anastomosis on high-resolution magnetic resonance imaging as an imaging biomarker in hemorrhagic moyamoya disease. Eur Radiol 31, 4548–4556 (2021). https://doi.org/10.1007/s00330-020-07479-0

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  • DOI: https://doi.org/10.1007/s00330-020-07479-0

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