Skip to main content

Advertisement

SpringerLink
Log in

Incremental value of plaque enhancement in predicting stroke recurrence in symptomatic intracranial atherosclerosis

  • Diagnostic Neuroradiology
  • Published:
Neuroradiology Aims and scope Submit manuscript

Abstract

Purpose

To investigate the association between plaque enhancement and stroke recurrence in subjects with intracranial atherosclerosis.

Methods

Ischemic stroke patients with symptomatic intracranial atherosclerosis were prospectively included and followed in a comprehensive stroke center. Pre- and post-contrast vessel wall images were used to evaluate plaque enhancement. Other established suggestive imaging markers were also acquired simultaneously. Univariate- and multivariate-adjusted Cox proportional hazard regression models were used to determine the association between plaque enhancement and stroke recurrence. Finally, receiver operating characteristic (ROC) curves were used to demonstrate the predictive value of different imaging markers.

Results

Of the 60 subjects included, 12 (20.0%) patients presented with ipsilateral stroke recurrence during the median 12-month follow-up. Cox proportional hazard regression models indicated that plaque enhancement was an independent risk factor associated with stroke recurrence after adjusted covariates, with a hazard ratio (HR) of 14.24 and 95% confidence interval (95% CI) (1.21, 168.11), p = 0.04. In addition, border zone infarction was also statistically significant in predicting stroke recurrence in multi-variable regression (HR = 3.80; 95% CI = 1.04, 13.80; p = 0.04). Collateral status was in marginal significance (HR = 0.25; 95% CI = 0.06, 1.08; p = 0.06). ROC analysis indicated that the area under the curve and 95% CI to identify stroke recurrence are 0.67 (0.51, 0.82) for plaque enhancement and 0.71 (0.54, 0.88) for infarction pattern and collateral status and may increase to 0.82 (0.70, 0.93) by combining the three markers above.

Conclusion

Plaque enhancement is independently associated with stroke recurrence in subjects with intracranial atherosclerosis and has added value to hemodynamic indicators in predicting stroke recurrence.

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
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  1. Qureshi AI, Caplan LR (2014) Intracranial atherosclerosis. Lancet 383(9921):984–998. https://doi.org/10.1016/S0140-6736(13)61088-0

    Article  PubMed  Google Scholar 

  2. Wang Y, Zhao X, Liu L, Soo YO, Pu Y, Pan Y, Wang Y, Zou X, Leung TW, Cai Y, Bai Q, Wu Y, Wang C, Pan X, Luo B, Wong KS (2014) Prevalence and outcomes of symptomatic intracranial large artery stenoses and occlusions in China: the Chinese Intracranial Atherosclerosis (CICAS) Study. Stroke 45(3):663–669. https://doi.org/10.1161/STROKEAHA.113.003508

    Article  PubMed  Google Scholar 

  3. Sun P, Liu L, Pan Y, Wang X, Mi D, Pu Y, Liu X, Duan W, Yan H, Wang C, Zhao X, Wang Y, Wang Y (2018) Intracranial atherosclerosis burden and stroke recurrence for symptomatic intracranial artery stenosis (sICAS). Aging Dis 9(6):1096–1102. https://doi.org/10.14336/AD.2018.0301

    Article  PubMed  PubMed Central  Google Scholar 

  4. Derdeyn CP, Chimowitz MI, Lynn MJ, Fiorella D, Turan TN, Janis LS, Montgomery J, Nizam A, Lane BF, Lutsep HL, Barnwell SL, Waters MF, Hoh BL, Hourihane JM, Levy EI, Alexandrov AV, Harrigan MR, Chiu D, Klucznik RP, Clark JM, CG MD, Johnson MD, Pride GJ, Lynch JR, Zaidat OO, Rumboldt Z, Cloft HJ (2014) Aggressive medical treatment with or without stenting in high-risk patients with intracranial artery stenosis (SAMMPRIS): the final results of a randomised trial. Lancet 383(9914):333–341. https://doi.org/10.1016/S0140-6736(13)62038-3

    Article  PubMed  Google Scholar 

  5. Kim BS, Chung PW, Park KY, Won HH, Bang OY, Chung CS, Lee KH, Kim GM (2017) Burden of intracranial atherosclerosis is associated with long-term vascular outcome in patients with ischemic stroke. Stroke 48(10):2819–2826. https://doi.org/10.1161/STROKEAHA.117.017806

    Article  PubMed  Google Scholar 

  6. Wabnitz AM, Derdeyn CP, Fiorella DJ, Lynn MJ, Cotsonis GA, Liebeskind DS, Waters MF, Lutsep H, Lopez-Cancio E, Turan TN, Montgomery J, Janis LS, Lane B, Chimowitz MI (2018) Hemodynamic markers in the anterior circulation as predictors of recurrent stroke in patients with intracranial stenosis. Stroke:A118020840. https://doi.org/10.1161/STROKEAHA.118.020840

  7. Takaya N, Yuan C, Chu B, Saam T, Underhill H, Cai J, Tran N, Polissar NL, Isaac C, Ferguson MS, Garden GA, Cramer SC, Maravilla KR, Hashimoto B, Hatsukami TS (2006) Association between carotid plaque characteristics and subsequent ischemic cerebrovascular events: a prospective assessment with MRI—initial results. Stroke 37(3):818–823. https://doi.org/10.1161/01.STR.0000204638.91099.91

    Article  PubMed  Google Scholar 

  8. Gupta A, Baradaran H, Al-Dasuqi K, Knight-Greenfield A, Giambrone AE, Delgado D, Wright D, Teng Z, Min JK, Navi BB, Iadecola C, Kamel H (2016) Gadolinium enhancement in intracranial atherosclerotic plaque and ischemic stroke: a systematic review and meta-analysis. J Am Heart Assoc 5(8). https://doi.org/10.1161/JAHA.116.003816

  9. Li D, Zhao H, Chen X, Chen S, Qiao H, He L, Li R, Xu J, Yuan C, Zhao X (2018) Identification of intraplaque haemorrhage in carotid artery by simultaneous non-contrast angiography and intraPlaque haemorrhage (SNAP) imaging: a magnetic resonance vessel wall imaging study. Eur Radiol 28(4):1681–1686. https://doi.org/10.1007/s00330-017-5096-1

    Article  PubMed  Google Scholar 

  10. Lee DK, Kim JS, Kwon SU, Yoo SH, Kang DW (2005) Lesion patterns and stroke mechanism in atherosclerotic middle cerebral artery disease: early diffusion-weighted imaging study. Stroke 36(12):2583–2588. https://doi.org/10.1161/01.STR.0000189999.19948.14

    Article  PubMed  Google Scholar 

  11. Lopez-Cancio E, Matheus MG, Romano JG, Liebeskind DS, Prabhakaran S, Turan TN, Cotsonis GA, Lynn MJ, Rumboldt Z, Chimowitz MI (2014) Infarct patterns, collaterals and likely causative mechanisms of stroke in symptomatic intracranial atherosclerosis. Cerebrovasc Dis 37(6):417–422. https://doi.org/10.1159/000362922

    Article  PubMed  PubMed Central  Google Scholar 

  12. Liu S, Luo Y, Wang C, Tang R, Sheng Z, Xie W, Chai S, Guo Y, Chai C, Yang Q, Fan Z, Chang B, Xia S (2019) Combination of plaque characteristics, pial collaterals, and hypertension contributes to misery perfusion in patients with symptomatic middle cerebral artery stenosis. J Magn Reson Imaging. https://doi.org/10.1002/jmri.26778

  13. Yuan HW, Ji RJ, Wang AL, Lin YJ, Chen HF, Xu ZQ, Peng GP, Luo BY (2019) A grading scale for pial collaterals in middle cerebral artery total occlusion based on time-of-flight MR angiography source images. Magn Reson Med Sci 18(1):62–69. https://doi.org/10.2463/mrms.mp.2018-0001

    Article  PubMed  Google Scholar 

  14. Chimowitz MI, Lynn MJ, Howlett-Smith H, Stern BJ, Hertzberg VS, Frankel MR, Levine SR, Chaturvedi S, Kasner SE, Benesch CG, Sila CA, Jovin TG, Romano JG (2005) Comparison of warfarin and aspirin for symptomatic intracranial arterial stenosis. N Engl J Med 352(13):1305–1316. https://doi.org/10.1056/NEJMoa043033

    Article  CAS  PubMed  Google Scholar 

  15. Mandell DM, Mossa-Basha M, Qiao Y, Hess CP, Hui F, Matouk C, Johnson MH, Daemen MJ, Vossough A, Edjlali M, Saloner D, Ansari SA, Wasserman BA, Mikulis DJ (2017) Intracranial vessel wall MRI: principles and expert consensus recommendations of the American Society of Neuroradiology. AJNR Am J Neuroradiol 38(2):218–229. https://doi.org/10.3174/ajnr.A4893

    Article  CAS  PubMed  Google Scholar 

  16. Vakil P, Vranic J, Hurley MC, Bernstein RA, Korutz AW, Habib A, Shaibani A, Dehkordi FH, Carroll TJ, Ansari SA (2013) T1 gadolinium enhancement of intracranial atherosclerotic plaques associated with symptomatic ischemic presentations. AJNR Am J Neuroradiol 34(12):2252–2258. https://doi.org/10.3174/ajnr.A3606

    Article  CAS  PubMed  Google Scholar 

  17. van der Kolk AG, Zwanenburg JJ, Brundel M, Biessels GJ, Visser F, Luijten PR, Hendrikse J (2011) Intracranial vessel wall imaging at 7.0-T MRI. Stroke 42(9):2478–2484. https://doi.org/10.1161/STROKEAHA.111.620443

    Article  PubMed  Google Scholar 

  18. Xu W (2019) High-resolution MRI of intracranial large artery diseases: how to use it in clinical practice? Stroke Vasc Neurol 4(2):102–104. https://doi.org/10.1136/svn-2018-000210

    Article  PubMed  PubMed Central  Google Scholar 

  19. Hur J, Park J, Kim YJ, Lee HJ, Shim HS, Choe KO, Choi BW (2010) Use of contrast enhancement and high-resolution 3D black-blood MRI to identify inflammation in atherosclerosis. JACC Cardiovasc Imaging 3(11):1127–1135. https://doi.org/10.1016/j.jcmg.2010.08.012

    Article  PubMed  Google Scholar 

  20. Kwee RM, Qiao Y, Liu L, Zeiler SR, Wasserman BA (2019) Temporal course and implications of intracranial atherosclerotic plaque enhancement on high-resolution vessel wall MRI. Neuroradiology 61(6):651–657. https://doi.org/10.1007/s00234-019-02190-4

    Article  PubMed  Google Scholar 

  21. Kim JM, Jung KH, Sohn CH, Moon J, Shin JH, Park J, Lee SH, Han MH, Roh JK (2016) Intracranial plaque enhancement from high resolution vessel wall magnetic resonance imaging predicts stroke recurrence. Int J Stroke 11(2):171–179. https://doi.org/10.1177/1747493015609775

    Article  PubMed  Google Scholar 

  22. Feng X, Chan KL, Lan L, Abrigo J, Liu J, Fang H, Xu Y, Soo Y, Leng X, Leung TW (2019) Stroke mechanisms in symptomatic intracranial atherosclerotic disease. Stroke:A119025732. https://doi.org/10.1161/STROKEAHA.119.025732

  23. Raghuram K, Durgam A, Kohlnhofer J, Singh A (2018) Relationship between stroke recurrence, infarct pattern, and vascular distribution in patients with symptomatic intracranial stenosis. J Neurointerv Surg 10(12):1161–1163. https://doi.org/10.1136/neurintsurg-2017-013735

    Article  PubMed  Google Scholar 

Download references

Funding

This study is supported by the Beijing Municipal Science & Technology Commission (Z171100001017019), the Beijing Municipal Administration of Hospitals’ Ascent Plan (DFL20152201), the Tsinghua University Initiative Scientific Research Program (20161080076), and the Beijing Municipal Health Bureau Project (2013-2-034).

Author information

Authors and Affiliations

  1. Department of Neurology, Beijing Tsinghua Changgung Hospital, School of Clinical Medicine, Tsinghua University, No.168 of Litang Road, Changping District, Beijing, 102218, China

    Xiaowei Song, Wendeng Xu, Duoduo Hou & Jian Wu

  2. Department of Radiology, Beijing Tsinghua Changgung Hospital, School of Clinical Medicine, Tsinghua University, Beijing, 102218, China

    Xihai Zhao, Lixue Wang, Yilan Xu & Zhuozhao Zheng

  3. Center for Biomedical Imaging Research, Department of Biomedical Engineering, Tsinghua University School of Medicine, Beijing, 100084, China

    Xihai Zhao

  4. Neurovascular Imaging Research Core and Stroke Center, Department of Neurology, University of California at Los Angeles, Los Angeles, CA, 90024, USA

    David S. Liebeskind

  5. Tsinghua University Hospital, Beijing, 100084, China

    Jian Wu

Authors
  1. Xiaowei Song
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Xihai Zhao
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. David S. Liebeskind
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Lixue Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Wendeng Xu
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Yilan Xu
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Duoduo Hou
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Zhuozhao Zheng
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Jian Wu
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Jian Wu.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

All procedures performed in this study were in accordance with the ethical standards of the institutional research committee and with the 1964 Helsinki Declaration and its later amendments; the protocol was also approved by the local ethics committee.

Informed consent

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

Additional information

Publisher’s note

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

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Song, X., Zhao, X., Liebeskind, D.S. et al. Incremental value of plaque enhancement in predicting stroke recurrence in symptomatic intracranial atherosclerosis. Neuroradiology 62, 1123–1131 (2020). https://doi.org/10.1007/s00234-020-02418-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00234-020-02418-8

Keywords

Search

Navigation