Skip to main content
SpringerLink
Log in

Hemodynamics is associated with vessel wall remodeling in patients with middle cerebral artery stenosis

  • Head and Neck
  • Published:
European Radiology Aims and scope Submit manuscript

Abstract

Objectives

To evaluate the relationship between hemodynamics and vessel wall remodeling patterns in middle cerebral artery (MCA) stenosis based on high-resolution magnetic resonance imaging and computational fluid dynamics (CFD).

Methods

Forty consecutive patients with recent ischemic stroke or transient ischemic attack attributed to unilateral atherosclerotic MCA stenosis (50–99%) were prospectively recruited. All patients underwent a cross-sectional scan of the stenotic MCA vessel wall. The parameters of the vessel wall, the number of patients with acute infarction, translesional wall shear stress ratio (WSSR), wall shear stress in stenosis (WSSs), and translesional pressure ratio were obtained. The patients were divided into positive remodeling (PR) and negative remodeling (NR) groups. The differences in vessel wall parameters and hemodynamics were compared. Correlations between the parameters of the vessel wall and hemodynamics were calculated.

Results

Of the 40 patients, 16 had PR, 19 had NR, and the other 5 displayed non-remodeling. The PR group had a smaller lumen area (p = 0.004), larger plaque area (p < 0.001), normal wall index (p = 0.004), and higher WSSR (p = 0.004) and WSSs (p = 0.023) at the most narrowed site. The PR group had more enhanced plaques (12 vs 6, p = 0.03). The number of patients with acute stroke in the PR group was more than that in the NR group (11 vs 4, p = 0.01). The remodeling index (r = 0.376, p = 0.026) and plaque area (r = 0.407, p = 0.015) showed a positive correlation with WSSR, respectively.

Conclusions

Hemodynamics plays a role in atherosclerotic plaques and vessel wall remodeling. Individuals with greater hemodynamic values might be more prone to stroke.

Key Points

• Stenotic plaques in middle cerebral artery with positive remodeling have smaller lumen area and larger resp. higher plaque area, normal wall index, translesional wall shear stress ratio, and wall shear stress than negative remodeling.

• The remodeling index and plaque area are positively correlated with translesional wall shear stress ratio.

• Hemodynamic may help to understand the role of positive remodeling in the development of acute stroke.

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

Similar content being viewed by others

Abbreviations

CFD:

Computational fluid dynamics

CTA:

Computed tomography angiography

DWI:

Diffusion-weighted imaging

FLAIR:

Fluid-attenuated inversion recovery

HRMRI:

High-resolution magnetic resonance imaging

ICAD:

Intracranial atherosclerotic disease

ICC:

Intraclass correlation coefficients

LA:

Lumen area

MCA:

Middle cerebral artery

MIP:

Maximum intensity projection

MRA:

Magnetic resonance angiography

NR:

Negative remodeling

NWI:

Normal wall index

PA:

Plaque area

PDWI:

Proton density–weighted imaging

PR:

Positive remodeling

RP:

Translesional pressure ratio

WSSR:

Translesional wall shear stress ratio

WSSs:

Wall shear stress in stenosis

References

  1. Zhang DF, Chen YC, Chen H et al (2017) A high-resolution MRI study of relationship between remodeling patterns and ischemic stroke in patients with atherosclerotic middle cerebral artery stenosis. Front Aging Neurosci 9:140

    Article  Google Scholar 

  2. Wang Y, Zhao X, Liu L et al (2014) Prevalence and outcomes of symptomatic intracranial large artery stenoses and occlusions in China: the Chinese Intracranial Atherosclerosis (CICAS) Study. Stroke 45:663–669

    Article  Google Scholar 

  3. Arenillas JF (2011) Intracranial atherosclerosis: current concepts. Stroke 42:16

    Article  Google Scholar 

  4. 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  Google Scholar 

  5. Wu F, Zhang Q, Dong K et al (2019) Whole-brain magnetic resonance imaging of plaque burden and lenticulostriate arteries in patients with different types of stroke. Ther Adv Neurol Disord 12:1756286419833295

    Article  Google Scholar 

  6. 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  Google Scholar 

  7. Ryu CW, Jahng GH, Shin HS (2014) Gadolinium enhancement of atherosclerotic plaque in the middle cerebral artery: relation to symptoms and degree of stenosis. AJNR Am J Neuroradiol 35:2306–2310

    Article  Google Scholar 

  8. Wang E, Shao S, Li S et al (2019) High-resolution MRI study of the relationship between plaque enhancement and ischemic stroke events in patients with intracranial atherosclerotic stenosis. Front Neurol 9:1154

    Article  Google Scholar 

  9. Teng Z, Peng W, Zhan Q et al (2016) An assessment on the incremental value of high-resolution magnetic resonance imaging to identify culprit plaques in atherosclerotic disease of the middle cerebral artery. Eur Radiol 26:2206–2214

    Article  Google Scholar 

  10. Hartmann M, von Birgelen C, Mintz GS et al (2006) Relation between baseline plaque burden and subsequent remodelling of atherosclerotic left main coronary arteries: a serial intravascular ultrasound study with long-term (> or =12 months) follow-up. Eur Heart J 27:1778–1784

    Article  Google Scholar 

  11. Birnbaum Y, Fishbein MC, Luo H et al (1997) Regional remodeling of atherosclerotic arteries: a major determinant of clinical manifestations of disease. J Am Coll Cardiol 30:1149–1164

    Article  CAS  Google Scholar 

  12. Lee HN, Ryu CW, Yun SJ (2018) Vessel-wall magnetic resonance imaging of intracranial atherosclerotic plaque and ischemic stroke: a systematic review and meta-analysis. Front Neurol 9:1032

    Article  CAS  Google Scholar 

  13. Douglas PS, Pontone G, Hlatky MA et al (2015) Clinical outcomes of fractional flow reserve by computed tomographic angiography-guided diagnostic strategies vs. usual care in patients with suspected coronary artery disease: the prospective longitudinal trial of FFR(CT): outcome and resource impacts study. Eur Heart J 36:3359–3367

    Article  CAS  Google Scholar 

  14. Huang X, Yin X, Xu Y et al (2016) Morphometric and hemodynamic analysis of atherosclerotic progression in human carotid artery bifurcations. Am J Physiol Heart Circ Physiol 310:8

    Article  Google Scholar 

  15. Samady H, Eshtehardi P, McDaniel MC et al (2011) Coronary artery wall shear stress is associated with progression and transformation of atherosclerotic plaque and arterial remodeling in patients with coronary artery disease. Circulation 124:779–788

    Article  CAS  Google Scholar 

  16. Steinman DA, Pereira VM (2019) How patient specific are patient-specific computational models of cerebral aneurysms? An overview of sources of error and variability. Neurosurg Focus 47(1):E14

    Article  Google Scholar 

  17. Leng X, Lan L, Ip HL et al (2018) Translesional pressure gradient and leptomeningeal collateral status in symptomatic middle cerebral artery stenosis. Eur J Neurol 25:404–410

    Article  CAS  Google Scholar 

  18. Leng X, Lan L, Ip HL et al (2019) Hemodynamics and stroke risk in intracranial atherosclerotic disease. Ann Neurol 85:752–764

    Article  CAS  Google Scholar 

  19. Xu WH, Li ML, Gao S et al (2010) In vivo high-resolution MR imaging of symptomatic and asymptomatic middle cerebral artery atherosclerotic stenosis. Atherosclerosis 212:507–511

    Article  CAS  Google Scholar 

  20. Liao S, Deng Z, Wang Y et al (2018) Different mechanisms of two subtypes of perforating artery infarct in the middle cerebral artery territory: a high-resolution magnetic resonance imaging study. Front Neurol 9:657

    Article  Google Scholar 

  21. Laugesen E, Hoyem P, Thrysoe S et al (2018) Negative carotid artery remodeling in early type 2 diabetes mellitus and increased carotid plaque vulnerability in obesity as assessed by magnetic resonance imaging. J Am Heart Assoc 7:008677

    Article  Google Scholar 

  22. Glagov S, Weisenberg E, Zarins CK et al (1987) Compensatory enlargement of human atherosclerotic coronary arteries. N Engl J Med 316:1371–1375

    Article  CAS  Google Scholar 

  23. Hardie AD, Kramer CM, Raghavan P et al (2007) The impact of expansive arterial remodeling on clinical presentation in carotid artery disease: a multidetector CT angiography study. AJNR Am J Neuroradiol 28:1067–1070

    Article  CAS  Google Scholar 

  24. Zhao DL, Deng G, Xie B et al (2015) High-resolution MRI of the vessel wall in patients with symptomatic atherosclerotic stenosis of the middle cerebral artery. J Clin Neurosci 22:700–704

    Article  Google Scholar 

  25. Dieleman N, Yang W, Abrigo JM et al (2016) Magnetic resonance imaging of plaque morphology, burden, and distribution in patients with symptomatic middle cerebral artery stenosis. Stroke 47:1797–1802

    Article  Google Scholar 

  26. Shen M, Gao P, Zhang Q et al (2018) Middle cerebral artery atherosclerosis and deep subcortical infarction: a 3T magnetic resonance vessel wall imaging study. J Stroke Cerebrovasc Dis 27:3387–3392

    Article  Google Scholar 

  27. Jia Q, Liu H, Li Y et al (2017) Combination of magnetic resonance angiography and computational fluid dynamics may predict the risk of stroke in patients with asymptomatic carotid plaques. Med Sci Monit 23:479–488

    Article  Google Scholar 

  28. Zhao X, Miller ZE, Yuan C (2009) Atherosclerotic plaque imaging by carotid MRI. Curr Cardiol Rep 11:70–77

    Article  Google Scholar 

  29. Xaplanteris P, Fournier S, Pijls NHJ et al (2018) Five-year outcomes with PCI guided by fractional flow reserve. N Engl J Med 379:250–259

    Article  Google Scholar 

  30. Groen HC, Gijsen FJ, van der Lugt A et al (2007) Plaque rupture in the carotid artery is localized at the high shear stress region: a case report. Stroke 38:2379–2381

    Article  Google Scholar 

  31. Balaguru UM, Sundaresan L, Manivannan J et al (2016) Disturbed flow mediated modulation of shear forces on endothelial plane: a proposed model for studying endothelium around atherosclerotic plaques. Sci Rep 6:27304

    Article  CAS  Google Scholar 

  32. Tuenter A, Selwaness M, Arias Lorza A et al (2016) High shear stress relates to intraplaque haemorrhage in asymptomatic carotid plaques. Atherosclerosis 251:348–354

    Article  CAS  Google Scholar 

  33. Lan L, Leng X, Ip V et al (2018) Sustaining cerebral perfusion in intracranial atherosclerotic stenosis: the roles of antegrade residual flow and leptomeningeal collateral flow. J Cereb Blood Flow Metab 23:10

    Google Scholar 

  34. Amin-Hanjani S, Pandey DK, Rose-Finnell L et al (2016) Effect of hemodynamics on stroke risk in symptomatic atherosclerotic vertebrobasilar occlusive disease. JAMA Neurol 73:178–185

    Article  Google Scholar 

Download references

Funding

No funding was received.

Author information

Author notes

  1. Danfeng Zhang and Xinying Wu contributed equally to this work.

Authors and Affiliations

  1. Department of Radiology, Nanjing First Hospital, Nanjing Medical University, Nanjing, 210006, Jiangsu, China

    Danfeng Zhang, Xinying Wu, Jie Tang, Peng Wang, Guo Zhong Chen & Xindao Yin

Authors
  1. Danfeng Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Xinying Wu
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jie Tang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Peng Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Guo Zhong Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Xindao Yin
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Guo Zhong Chen or Xindao Yin.

Ethics declarations

Guarantor

The scientific guarantor of this publication is Xindao Yin.

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 study.

Informed consent

All recruited patients provided verbal or written informed consent before examined.

Ethical approval

Institutional Review Board approval was obtained.

Methodology

• Prospective

• Case-control study

• Performed at one institution

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

Zhang, D., Wu, X., Tang, J. et al. Hemodynamics is associated with vessel wall remodeling in patients with middle cerebral artery stenosis. Eur Radiol 31, 5234–5242 (2021). https://doi.org/10.1007/s00330-020-07607-w

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00330-020-07607-w

Keywords

Search

Navigation