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Co-existing intracranial and extracranial carotid atherosclerosis predicts large-artery atherosclerosis stroke recurrence: a single-center prospective study utilizing combined head-and-neck vessel wall imaging

  • Magnetic Resonance
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Abstract

Objectives

Intracranial and extracranial plaque features on high-resolution vessel wall imaging (HR-VWI) are associated with large-artery atherosclerosis (LAA) stroke recurrence. However, most studies have focused on a single vascular bed, and the prognostic value of combined intracranial and extracranial plaque features has yet to be studied. This study aimed to investigate the roles of plaque features, plaque number, and co-existing atherosclerosis in predicting stroke recurrence, utilizing combined head-and-neck HR-VWI.

Methods

From September 2016 to March 2020, participants with acute LAA ischemic strokes were prospectively enrolled and underwent combined head-and-neck HR-VWI. The participants were followed for stroke recurrence for at least 12 months or until a subsequent event occurred. The imaging features at baseline, including conventional and histogram plaque features, plaque number, and co-existing atherosclerosis, were evaluated. Univariable Cox regression analysis and the least absolute shrinkage and selection operator (lasso) method were used for variable screening. Multivariable Cox regression analyses were used to determine the independent risk factors of stroke recurrence.

Results

A total of 97 participants (59 ± 12 years, 63 men) were followed for a median of 30.9 months, and 21 participants experienced recurrent strokes. Multivariable Cox analysis identified co-existing intracranial high signal on T1-weighted fat-suppressed images (HST1) and extracranial carotid atherosclerosis (HR, 6.12; 95% CI, 2.52–14.82; p = 0.001) as an independent imaging predictor of stroke recurrence.

Conclusion

Co-existing intracranial HST1 and extracranial carotid atherosclerosis independently predicted LAA stroke recurrence. Combined head-and-neck HR-VWI is a promising technique for atherosclerosis imaging.

Clinical relevance statement

This prospective study using combined head-and-neck HR-VWI highlighted the necessity of both intracranial culprit plaque evaluation and multi-vascular bed assessment, adding value to the prediction of stroke recurrence.

Key Points

This study highlighted the necessity of both intracranial culprit plaque evaluation and multi-vascular bed assessment, adding value to the prediction of stroke recurrence.

This prospective study using combined head-and-neck HR-VWI found co-existing intracranial HST1 and extracranial carotid atherosclerosis to be independent predictors of stroke recurrence.

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Abbreviations

HR:

Hazard ratio

HR-VWI:

High-resolution vessel wall imaging

HST1:

High signal on T1-weighted fat-suppressed images

LAA:

Large-artery atherosclerosis

Lasso:

Least absolute shrinkage and selection operator

SI:

Signal intensity

TIA:

Transient ischemic attack

References

  1. Suo Y, Jing J, Pan Y et al (2021) Concurrent intracranial and extracranial artery stenosis and the prognosis of transient ischaemic symptoms or imaging-negative ischaemic stroke. Stroke Vasc Neurol 6:33–40

    Article  PubMed  Google Scholar 

  2. Xu Y, Yuan C, Zhou Z et al (2016) Co-existing intracranial and extracranial carotid artery atherosclerotic plaques and recurrent stroke risk: a three-dimensional multicontrast cardiovascular magnetic resonance study. J Cardiovasc Magn Reson 18:90

    Article  PubMed  PubMed Central  Google Scholar 

  3. Li J, Li D, Yang D et al (2020) Co-existing cerebrovascular atherosclerosis predicts subsequent vascular event: a multi-contrast cardiovascular magnetic resonance imaging study. J Cardiovasc Magn Reson 22:4

    Article  PubMed  PubMed Central  Google Scholar 

  4. 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  PubMed  PubMed Central  Google Scholar 

  5. Tian X, Tian B, Shi Z et al (2021) Assessment of intracranial atherosclerotic plaques using 3D Black-Blood MRI: comparison with 3D time-of-flight MRA and DSA. J Magn Reson Imaging 53:469–478

    Article  PubMed  Google Scholar 

  6. Wang Y, Liu X, Wu X, Degnan AJ, Malhotra A, Zhu C (2019) Culprit intracranial plaque without substantial stenosis in acute ischemic stroke on vessel wall MRI: a systematic review. Atherosclerosis 287:112–121

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Song JW, Pavlou A, Xiao J, Kasner SE, Fan Z, Messe SR (2021) Vessel wall magnetic resonance imaging biomarkers of symptomatic intracranial atherosclerosis: a meta-analysis. Stroke 52:193–202

    Article  CAS  PubMed  Google Scholar 

  8. Zhu C, Tian X, Degnan AJ et al (2018) Clinical significance of intraplaque hemorrhage in low- and high-grade basilar artery stenosis on high-resolution MRI. AJNR Am J Neuroradiol 39:1286–1292

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Qiao Y, Zeiler SR, Mirbagheri S et al (2014) Intracranial plaque enhancement in patients with cerebrovascular events on high-spatial-resolution MR images. Radiology 271:534–542

    Article  PubMed  Google Scholar 

  10. Ran Y, Wang Y, Zhu M et al (2020) Higher plaque burden of middle cerebral artery is associated with recurrent ischemic stroke: a quantitative magnetic resonance imaging study. Stroke 51:659–662

    Article  PubMed  Google Scholar 

  11. Shi Z, Li J, Zhao M et al (2020) Quantitative histogram analysis on intracranial atherosclerotic plaques: a high-resolution magnetic resonance imaging study. Stroke 51:2161–2169

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Gao S, Wang YJ, Xu AD, Li YS, Wang DZ (2011) Chinese ischemic stroke subclassification. Front Neurol 2:6

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Fan Z, Yang Q, Deng Z et al (2017) Whole-brain intracranial vessel wall imaging at 3 Tesla using cerebrospinal fluid-attenuated T1-weighted 3D turbo spin echo. Magn Reson Med 77:1142–1150

    Article  PubMed  Google Scholar 

  14. Yang Q, Deng Z, Bi X et al (2017) Whole-brain vessel wall MRI: a parameter tune-up solution to improve the scan efficiency of three-dimensional variable flip-angle turbo spin-echo. J Magn Reson Imaging 46:751–757

    Article  PubMed  Google Scholar 

  15. Yushkevich PA, Piven J, Hazlett HC et al (2006) User-guided 3D active contour segmentation of anatomical structures: significantly improved efficiency and reliability. Neuroimage 31:1116–1128

    Article  PubMed  Google Scholar 

  16. Barnett HJ, Taylor DW, Eliasziw M et al (1998) Benefit of carotid endarterectomy in patients with symptomatic moderate or severe stenosis. North American Symptomatic Carotid Endarterectomy Trial Collaborators. N Engl J Med 339:1415–1425

    Article  CAS  PubMed  Google Scholar 

  17. Qiao Y, Anwar Z, Intrapiromkul J et al (2016) Patterns and implications of intracranial arterial remodeling in stroke patients. Stroke 47:434–440

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Liu J, Balu N, Hippe DS et al (2016) Semi-automatic carotid intraplaque hemorrhage detection and quantification on magnetization-prepared rapid acquisition gradient-echo (MP-RAGE) with optimized threshold selection. J Cardiovasc Magn Reson 18:41

    Article  PubMed  PubMed Central  Google Scholar 

  19. van der Kolk AG, Zwanenburg JJ, Brundel M et al (2011) Intracranial vessel wall imaging at 7.0-T MRI. Stroke 42:2478–2484

    Article  PubMed  Google Scholar 

  20. Yamagishi M, Terashima M, Awano K et al (2000) Morphology of vulnerable coronary plaque: insights from follow-up of patients examined by intravascular ultrasound before an acute coronary syndrome. J Am Coll Cardiol 35:106–111

    Article  CAS  PubMed  Google Scholar 

  21. Zhu C, Sadat U, Patterson AJ, Teng Z, Gillard JH, Graves MJ (2014) 3D high-resolution contrast enhanced MRI of carotid atheroma–a technical update. Magn Reson Imaging 32:594–597

    Article  PubMed  Google Scholar 

  22. Shi Z, Li J, Zhao M et al (2021) Progression of plaque burden of intracranial atherosclerotic plaque predicts recurrent stroke/transient ischemic attack: a pilot follow-up study using higher-resolution MRI. J Magn Reson Imaging 54:560–570

    Article  PubMed  Google Scholar 

  23. Whitley E, Ball J (2002) Statistics review 4: sample size calculations. Crit Care 6:335–341

    Article  PubMed  PubMed Central  Google Scholar 

  24. Grothues F, Smith GC, Moon JC et al (2002) Comparison of interstudy reproducibility of cardiovascular magnetic resonance with two-dimensional echocardiography in normal subjects and in patients with heart failure or left ventricular hypertrophy. Am J Cardiol 90:29–34

    Article  PubMed  Google Scholar 

  25. Chen XY, Wong KS, Lam WW, Ng HK (2014) High signal on T1 sequence of magnetic resonance imaging confirmed to be intraplaque haemorrhage by histology in middle cerebral artery. Int J Stroke 9:E19

    Article  PubMed  Google Scholar 

  26. Wu F, Song H, Ma Q et al (2018) Hyperintense plaque on intracranial vessel wall magnetic resonance imaging as a predictor of artery-to-artery embolic infarction. Stroke 49:905–911

    Article  PubMed  PubMed Central  Google Scholar 

  27. Hoshino T, Sissani L, Labreuche J et al (2018) Prevalence of systemic atherosclerosis burdens and overlapping stroke etiologies and their associations with long-term vascular prognosis in stroke with intracranial atherosclerotic disease. JAMA Neurol 75:203–211

    Article  PubMed  Google Scholar 

  28. Lindenholz A, van der Kolk AG, van der Schaaf IC et al (2020) Intracranial atherosclerosis assessed with 7-T MRI: evaluation of patients with ischemic stroke or transient ischemic attack. Radiology 295:162–170

    Article  PubMed  Google Scholar 

  29. Zwartbol MHT, Geerlings MI, Ghaznawi R, Hendrikse J, van der Kolk AG, Group U-SS (2019) Intracranial atherosclerotic burden on 7T MRI is associated with markers of extracranial atherosclerosis: the SMART-MR Study. AJNR Am J Neuroradiol 40:2016–2022

    CAS  PubMed  PubMed Central  Google Scholar 

  30. Leng X, Hurford R, Feng X et al (2021) Intracranial arterial stenosis in Caucasian versus Chinese patients with TIA and minor stroke: two contemporaneous cohorts and a systematic review. J Neurol Neurosurg Psychiatry. https://doi.org/10.1136/jnnp-2020-325630

    Article  PubMed  Google Scholar 

  31. Li D, Dai W, Cai Y et al (2018) Atherosclerosis in stroke-related vascular beds and stroke risk: a 3-D MR vessel wall imaging study. Ann Clin Transl Neurol 5:1599–1610

    Article  PubMed  PubMed Central  Google Scholar 

  32. Kasner SE, Chimowitz MI, Lynn MJ et al (2006) Predictors of ischemic stroke in the territory of a symptomatic intracranial arterial stenosis. Circulation 113:555–563

    Article  PubMed  Google Scholar 

  33. Liu S, Tang R, Xie W et al (2021) Plaque characteristics and hemodynamics contribute to neurological impairment in patients with ischemic stroke and transient ischemic attack. Eur Radiol 31:2062–2072

    Article  CAS  PubMed  Google Scholar 

  34. Lu M, Zhang H, Liu D et al (2022) Vessel wall enhancement as a predictor of arterial stenosis progression and poor outcomes in moyamoya disease. Eur Radiol. https://doi.org/10.1007/s00330-022-09223-2

    Article  PubMed  PubMed Central  Google Scholar 

  35. 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 61:651–657

    Article  PubMed  Google Scholar 

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Funding

This work was supported by the Natural Scientific Foundation of China (NSFC) (Grant No. 82171916 to S. Xia) and the Natural Science Foundation of Tianjin (Grant No. 20JCQNJC01250 to C. Cao). This work was also funded by the Tianjin Key Medical Discipline (Specialty) Construction Project. Chengcheng Zhu was supported by United States National Institute of Health (NIH) grants R01HL162743 and R00HL136883.

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Correspondence to Shuang Xia.

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The scientific guarantor of this publication is Shuang Xia.

Conflict of interest

Authors Xianchang Zhang and Jinxia Zhu are employees of Siemens Healthineers. The remaining authors declare no relationships with any companies whose products or services may be related to the subject matter of the article.

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No complex statistical methods were necessary for this paper.

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Written informed consent was provided by all participants or their authorized proxy.

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Institutional review board approval was obtained.

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• Prospective study

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• Performed at one institution

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Wu, G., Zhu, C., Wang, H. et al. Co-existing intracranial and extracranial carotid atherosclerosis predicts large-artery atherosclerosis stroke recurrence: a single-center prospective study utilizing combined head-and-neck vessel wall imaging. Eur Radiol 33, 6970–6980 (2023). https://doi.org/10.1007/s00330-023-09654-5

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