Skip to main content
SpringerLink
Log in

Assessment of quantitative methods for enhancement measurement on vessel wall magnetic resonance imaging evaluation of intracranial atherosclerosis

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

Abstract

Purpose

Quantitative measures of vessel wall magnetic resonance imaging (vwMRI) for the evaluation of intracranial atherosclerotic disease (ICAD) offers standardization not available with previously used qualitative approaches that may be difficult to replicate.

Methods

vwMRI studies performed to evaluate ICAD that had caused a stroke were analyzed. Two blinded reviewers qualitatively rated culprit lesions for the presence of enhancement on T1 delay alternating with nutation for tailored excitation (DANTE) SPACE images. At least 3 months later, quantitative analysis was performed of the same images, comparing lesion enhancement to reference structures. Cohen’s kappa and intraclass correlation coefficients were calculated to assess agreement. Ratios of enhancement of lesions to references were compared to qualitative ratings.

Results

Studies from 54 patients met inclusion criteria. A mean of 49 (90.7%) lesions were qualitatively rated as enhancing, with good inter-rater agreement (κ = 0.783). Among reference structure candidates, low infundibulum demonstrated the highest inter-rater agreement on pre- and post-contrast imaging. The ratio of percentage increase in plaque signal following contrast to the same measure in low infundibulum demonstrated the highest agreement with qualitative assessment, with highest agreement seen with a ratio of 0.8 set as a threshold (κ = 0.675).

Conclusion

Quantitative metrics can yield objective data to better standardize techniques and acceptance of vwMRI evaluation of ICAD. The low infundibulum had the highest inter-rater agreement on both pre- and post-contrast images and is best suited as a normally enhancing reference structure. Such quantitative techniques should be implemented in future research of vwMRI for the evaluation of ICAD.

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

References

  1. Mossa-Basha M, Alexander M, Gaddikeri S, Yuan C, Gandhi D (2016) Vessel wall imaging for intracranial vascular disease evaluation. J Neurointerv Surg 8(11):1154–1159. https://doi.org/10.1136/neurintsurg-2015-012127

    Article  PubMed  PubMed Central  Google Scholar 

  2. de Havenon A, Mossa-Basha M, Shah L, Kim SE, Park M, Parker D, McNally JS (2017) High-resolution vessel wall MRI for the evaluation of intracranial atherosclerotic disease. Neuroradiology 59(12):1193–1202. https://doi.org/10.1007/s00234-017-1925-9

    Article  PubMed  Google Scholar 

  3. 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, Vessel Wall Imaging Study Group of the American Society of N (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 

  4. Cogswell PM, Siero JCW, Lants SK, Waddle S, Davis LT, Gilbert G, Hendrikse J, Donahue MJ (2018) Variable impact of CSF flow suppression on quantitative 3.0T intracranial vessel wall measurements. J Magn Reson Imaging 48(4):1120–1128. https://doi.org/10.1002/jmri.26028

    Article  PubMed  Google Scholar 

  5. Li L, Chai JT, Biasiolli L, Robson MD, Choudhury RP, Handa AI, Near J, Jezzard P (2014) Black-blood multicontrast imaging of carotid arteries with DANTE-prepared 2D and 3D MR imaging. Radiology 273(2):560–569. https://doi.org/10.1148/radiol.14131717

    Article  PubMed  Google Scholar 

  6. Li L, Miller KL, Jezzard P (2012) DANTE-prepared pulse trains: a novel approach to motion-sensitized and motion-suppressed quantitative magnetic resonance imaging. Magn Reson Med 68(5):1423–1438. https://doi.org/10.1002/mrm.24142

    Article  PubMed  Google Scholar 

  7. 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

  8. Kim JM, Jung KH, Sohn CH, Moon J, Han MH, Roh JK (2012) Middle cerebral artery plaque and prediction of the infarction pattern. Arch Neurol 69(11):1470–1475. https://doi.org/10.1001/archneurol.2012.1018

    Article  PubMed  Google Scholar 

  9. Qiao Y, Zeiler SR, Mirbagheri S, Leigh R, Urrutia V, Wityk R, Wasserman BA (2014) Intracranial plaque enhancement in patients with cerebrovascular events on high-spatial-resolution MR images. Radiology 271(2):534–542. https://doi.org/10.1148/radiol.13122812

    Article  PubMed  PubMed Central  Google Scholar 

  10. Skarpathiotakis M, Mandell DM, Swartz RH, Tomlinson G, Mikulis DJ (2013) Intracranial atherosclerotic plaque enhancement in patients with ischemic stroke. AJNR Am J Neuroradiol 34(2):299–304. https://doi.org/10.3174/ajnr.A3209

    Article  CAS  PubMed  Google Scholar 

  11. 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 

  12. 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 

  13. Xu P, Lv L, Li S, Ge H, Rong Y, Hu C, Xu K (2015) Use of high-resolution 3.0-T magnetic resonance imaging to characterize atherosclerotic plaques in patients with cerebral infarction. Exp Ther Med 10(6):2424–2428. https://doi.org/10.3892/etm.2015.2815

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Zou XD, Chung YC, Zhang L, Han Y, Yang Q, Jia J (2015) Middle cerebral artery atherosclerotic plaques in recent small subcortical infarction: a three-dimensional high-resolution MR study. Biomed Res Int 2015:540217. https://doi.org/10.1155/2015/540217

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Teng Z, Peng W, Zhan Q, Zhang X, Liu Q, Chen S, Tian X, Chen L, Brown AJ, Graves MJ, Gillard JH, Lu J (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(7):2206–2214. https://doi.org/10.1007/s00330-015-4008-5

    Article  PubMed  Google Scholar 

  16. Alexander MD, Yuan C, Rutman A, Tirschwell DL, Palagallo G, Gandhi D, Sekhar LN, Mossa-Basha M (2016) High-resolution intracranial vessel wall imaging: imaging beyond the lumen. J Neurol Neurosurg Psychiatry 87(6):589–597. https://doi.org/10.1136/jnnp-2015-312020

    Article  PubMed  PubMed Central  Google Scholar 

  17. 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(1–2):74–80. https://doi.org/10.1159/000111525

    Article  PubMed  Google Scholar 

  18. Kerwin WS, Oikawa M, Yuan C, Jarvik GP, Hatsukami TS (2008) MR imaging of adventitial vasa vasorum in carotid atherosclerosis. Magn Reson Med 59(3):507–514. https://doi.org/10.1002/mrm.21532

    Article  CAS  PubMed  Google Scholar 

  19. Qiao Y, Etesami M, Astor BC, Zeiler SR, Trout HH 3rd, Wasserman BA (2012) Carotid plaque neovascularization and hemorrhage detected by MR imaging are associated with recent cerebrovascular ischemic events. AJNR Am J Neuroradiol 33(4):755–760. https://doi.org/10.3174/ajnr.A2863

    Article  CAS  PubMed  Google Scholar 

  20. Swartz RH, Bhuta SS, Farb RI, Agid R, Willinsky RA, Terbrugge KG, Butany J, Wasserman BA, Johnstone DM, Silver FL, Mikulis DJ (2009) Intracranial arterial wall imaging using high-resolution 3-tesla contrast-enhanced MRI. Neurology 72(7):627–634. https://doi.org/10.1212/01.wnl.0000342470.69739.b3

    Article  CAS  PubMed  Google Scholar 

  21. Vergouwen MD, Silver FL, Mandell DM, Mikulis DJ, Swartz RH (2011) Eccentric narrowing and enhancement of symptomatic middle cerebral artery stenoses in patients with recent ischemic stroke. Arch Neurol 68(3):338–342. https://doi.org/10.1001/archneurol.2011.20

    Article  PubMed  Google Scholar 

  22. Wasserman BA, Smith WI, Trout HH 3rd, Cannon RO 3rd, Balaban RS, Arai AE (2002) Carotid artery atherosclerosis: in vivo morphologic characterization with gadolinium-enhanced double-oblique MR imaging initial results. Radiology 223(2):566–573. https://doi.org/10.1148/radiol.2232010659

    Article  PubMed  Google Scholar 

  23. Yuan C, Kerwin WS, Ferguson MS, Polissar N, Zhang S, Cai J, Hatsukami TS (2002) Contrast-enhanced high resolution MRI for atherosclerotic carotid artery tissue characterization. J Magn Reson Imaging 15(1):62–67

    Article  Google Scholar 

  24. Xu WH, Li ML, Gao S, Ni J, Yao M, Zhou LX, Peng B, Feng F, Jin ZY, Cui LY (2012) Middle cerebral artery intraplaque hemorrhage: prevalence and clinical relevance. Ann Neurol 71(2):195–198. https://doi.org/10.1002/ana.22626

    Article  PubMed  Google Scholar 

  25. Smirniotopoulos JG, Murphy FM, Rushing EJ, Rees JH, Schroeder JW (2007) Patterns of contrast enhancement in the brain and meninges. Radiographics 27(2):525–551. https://doi.org/10.1148/rg.272065155

    Article  PubMed  Google Scholar 

  26. Samuels OB, Joseph GJ, Lynn MJ, Smith HA, Chimowitz MI (2000) A standardized method for measuring intracranial arterial stenosis. AJNR Am J Neuroradiol 21(4):643–646

    CAS  PubMed  Google Scholar 

  27. Warfarin-Aspirin Symptomatic Intracranial Disease Trial I (2003) Design, progress and challenges of a double-blind trial of warfarin versus aspirin for symptomatic intracranial arterial stenosis. Neuroepidemiology 22(2):106–117. https://doi.org/10.1159/000068744

    Article  Google Scholar 

  28. McNally JS, McLaughlin MS, Hinckley PJ, Treiman SM, Stoddard GJ, Parker DL, Treiman GS (2015) Intraluminal thrombus, intraplaque hemorrhage, plaque thickness, and current smoking optimally predict carotid stroke. Stroke 46(1):84–90. https://doi.org/10.1161/STROKEAHA.114.006286

    Article  PubMed  Google Scholar 

  29. Yamada N, Higashi M, Otsubo R, Sakuma T, Oyama N, Tanaka R, Iihara K, Naritomi H, Minematsu K, Naito H (2007) Association between signal hyperintensity on T1-weighted MR imaging of carotid plaques and ipsilateral ischemic events. AJNR Am J Neuroradiol 28(2):287–292

    CAS  PubMed  Google Scholar 

  30. Portanova A, Hakakian N, Mikulis DJ, Virmani R, Abdalla WM, Wasserman BA (2013) Intracranial vasa vasorum: insights and implications for imaging. Radiology 267(3):667–679. https://doi.org/10.1148/radiol.13112310

    Article  PubMed  Google Scholar 

  31. Turan TN, Bonilha L, Morgan PS, Adams RJ, Chimowitz MI (2011) Intraplaque hemorrhage in symptomatic intracranial atherosclerotic disease. J Neuroimaging 21(2):e159–e161. https://doi.org/10.1111/j.1552-6569.2009.00442.x

    Article  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Radiology and Imaging Sciences, University of Utah, Salt Lake City, UT, USA

    Matthew D. Alexander, Seong-Eun Kim, Dennis L. Parker & Joseph S. McNally

  2. Department of Neurosurgery, University of Utah, 30 North 1900 East, Room 1A071, Salt Lake City, UT, 84132, USA

    Matthew D. Alexander

  3. Department of Neurology, University of Utah, Salt Lake City, UT, USA

    Adam de Havenon

Authors
  1. Matthew D. Alexander
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Adam de Havenon
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Seong-Eun Kim
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Dennis L. Parker
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Joseph S. McNally
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Matthew D. Alexander.

Ethics declarations

Funding

No funding was received for this study.

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

All procedures performed in the studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki Declaration and its later amendments or comparable ethical standards.

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

Alexander, M.D., de Havenon, A., Kim, SE. et al. Assessment of quantitative methods for enhancement measurement on vessel wall magnetic resonance imaging evaluation of intracranial atherosclerosis. Neuroradiology 61, 643–650 (2019). https://doi.org/10.1007/s00234-019-02167-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00234-019-02167-3

Keywords

Search

Navigation