Intracranial Plaque Enhancement in Patients with Cerebrovascular Events on High-Spatial-Resolution MR Images

Published Online:https://doi.org/10.1148/radiol.13122812

We have shown that intracranial atherosclerotic plaque enhancement can be used to identify lesions responsible for cerebrovascular ischemic events.

Purpose

To characterize intracranial plaque inflammation in vivo by using three-dimensional (3D) high-spatial-resolution contrast material–enhanced black-blood (BB) magnetic resonance (MR) imaging and to investigate the relationship between intracranial plaque inflammation and cerebrovascular ischemic events.

Materials and Methods

The study was approved by the institutional review board and was HIPAA compliant. Twenty-seven patients (19 men; mean age, 56.8 years ± 12.4 [standard deviation]) with cerebrovascular ischemic events (acute stroke, n = 20; subacute stroke, n = 2; chronic stroke, n = 3; transient ischemic attack, n = 2) underwent 3D time-of-flight MR angiography and contrast-enhanced BB 3-T MR imaging for intracranial atherosclerotic disease. Each identified plaque was classified as either culprit (the only or most stenotic lesion upstream from a stroke), probably culprit (not the most stenotic lesion upstream from a stroke), or nonculprit (not within the vascular territory of a stroke). Plaque contrast enhancement was categorized on BB MR images (grade 0, enhancement less than or equal to that of normal arterial walls seen elsewhere; grade 1, enhancement greater than grade 0 but less than that of the pituitary infundibulum; grade 2, enhancement greater than or equal to that of the pituitary infundibulum), and degree of contrast enhancement was calculated. Associations of the likelihood of being a culprit lesion with both plaque contrast enhancement and plaque thickness were estimated with ordinal logistic regression.

Results

Seventy-eight plaques were identified in 20 patients with acute stroke (21 [27%] culprit, 12 [15%] probably culprit, and 45 [58%] nonculprit plaques). In these patients, grade 2 contrast enhancement was associated with culprit plaques (odds ratio 34.6; 95% confidence interval: 4.5, 266.5 compared with grade 0) when adjusted for plaque thickness. Grade 0 was observed in only nonculprit plaques. Culprit plaques had a higher degree of contrast enhancement than did nonculprit plaques (25.9% ± 13.4 vs 13.6% ± 12.3, P = .003).

Conclusion

Contrast enhancement of intracranial atherosclerotic plaque is associated with its likelihood to have caused a recent ischemic event and may serve as a marker of its stability, thereby providing important insight into stroke risk.

© RSNA, 2014

Online supplemental material is available for this article.

References

  • 1. Wityk RJ, Lehman D, Klag M, Coresh J, Ahn H, Litt B. Race and sex differences in the distribution of cerebral atherosclerosis. Stroke 1996;27(11):1974–1980. Crossref, MedlineGoogle Scholar
  • 2. Wong LK. Global burden of intracranial atherosclerosis. Int J Stroke 2006;1(3):158–159. Crossref, MedlineGoogle Scholar
  • 3. Chen XY, Wong KS, Lam WW, Zhao HL, Ng HK. Middle cerebral artery atherosclerosis: histological comparison between plaques associated with and not associated with infarct in a postmortem study. Cerebrovasc Dis 2008;25(1-2):74–80. Crossref, MedlineGoogle Scholar
  • 4. Mazighi M, Labreuche J, Gongora-Rivera F, Duyckaerts C, Hauw JJ, Amarenco P. Autopsy prevalence of intracranial atherosclerosis in patients with fatal stroke. Stroke 2008;39(4):1142–1147. Crossref, MedlineGoogle Scholar
  • 5. Labadzhyan A, Csiba L, Narula N, Zhou J, Narula J, Fisher M. Histopathologic evaluation of basilar artery atherosclerosis. J Neurol Sci 2011;307(1-2):97–99. Crossref, MedlineGoogle Scholar
  • 6. Arenillas JF, Alvarez-Sabín J, Molina CA, et al. Progression of symptomatic intracranial large artery atherosclerosis is associated with a proinflammatory state and impaired fibrinolysis. Stroke 2008;39(5):1456–1463. Crossref, MedlineGoogle Scholar
  • 7. Qiao Y, Etesami M, Astor BC, Zeiler SR, Trout HH 3rd, Wasserman BA. Carotid plaque neovascularization and hemorrhage detected by MR imaging are associated with recent cerebrovascular ischemic events. AJNR Am J Neuroradiol 2012;33(4):755–760. Crossref, MedlineGoogle Scholar
  • 8. Kerwin WS, Oikawa M, Yuan C, Jarvik GP, Hatsukami TS. MR imaging of adventitial vasa vasorum in carotid atherosclerosis. Magn Reson Med 2008;59(3):507–514. Crossref, MedlineGoogle Scholar
  • 9. Aoki S, Shirouzu I, Sasaki Y, et al. Enhancement of the intracranial arterial wall at MR imaging: relationship to cerebral atherosclerosis. Radiology 1995;194(2):477–481. LinkGoogle Scholar
  • 10. Rudd JH, Fayad ZA. Imaging atherosclerotic plaque inflammation. Nat Clin Pract Cardiovasc Med 2008;5(Suppl 2):S11–S17. Crossref, MedlineGoogle Scholar
  • 11. Ibrahim T, Makowski MR, Jankauskas A, et al. Serial contrast-enhanced cardiac magnetic resonance imaging demonstrates regression of hyperenhancement within the coronary artery wall in patients after acute myocardial infarction. JACC Cardiovasc Imaging 2009;2(5):580–588. Crossref, MedlineGoogle Scholar
  • 12. Qiao Y, Steinman DA, Qin Q, et al. Intracranial arterial wall imaging using three-dimensional high isotropic resolution black blood MRI at 3.0 Tesla. J Magn Reson Imaging 2011;34(1):22–30. Crossref, MedlineGoogle Scholar
  • 13. Swartz RH, Bhuta SS, Farb RI, et al. Intracranial arterial wall imaging using high-resolution 3-tesla contrast-enhanced MRI. Neurology 2009;72(7):627–634. Crossref, MedlineGoogle Scholar
  • 14. Antiga L, Wasserman BA, Steinman DA. On the overestimation of early wall thickening at the carotid bulb by black blood MRI, with implications for coronary and vulnerable plaque imaging. Magn Reson Med 2008;60(5):1020–1028. Crossref, MedlineGoogle Scholar
  • 15. Nahab F, Cotsonis G, Lynn M, et al. Prevalence and prognosis of coexistent asymptomatic intracranial stenosis. Stroke 2008;39(3):1039–1041. Crossref, MedlineGoogle Scholar
  • 16. Chimowitz MI, Kokkinos J, Strong J, et al. The Warfarin-Aspirin Symptomatic Intracranial Disease Study. Neurology 1995;45(8):1488–1493. Crossref, MedlineGoogle Scholar
  • 17. Busse RF, Brau AC, Vu A, et al. Effects of refocusing flip angle modulation and view ordering in 3D fast spin echo. Magn Reson Med 2008;60(3):640–649. Crossref, MedlineGoogle Scholar
  • 18. van der Kolk AG, Zwanenburg JJ, Brundel M, et al. Intracranial vessel wall imaging at 7.0-T MRI. Stroke 2011;42(9):2478–2484. Crossref, MedlineGoogle Scholar
  • 19. Greenman RL, Wang X, Ngo L, Marquis RP, Farrar N. An assessment of the sharpness of carotid artery tissue boundaries with acquisition voxel size and field strength. Magn Reson Imaging 2008;26(2):246–253. Crossref, MedlineGoogle Scholar
  • 20. Longstreth WT Jr, Bernick C, Manolio TA, Bryan N, Jungreis CA, Price TR. Lacunar infarcts defined by magnetic resonance imaging of 3660 elderly people: the Cardiovascular Health Study. Arch Neurol 1998;55(9):1217–1225. Crossref, MedlineGoogle Scholar
  • 21. Fisher CM. Lacunar strokes and infarcts: a review. Neurology 1982;32(8):871–876. Crossref, MedlineGoogle Scholar
  • 22. Fleiss J. Statistical methods for rates and proportions. 2nd ed. New York, NY: Wiley, 1981; 218. Google Scholar
  • 23. Xu WH, Li ML, Gao S, et al. In vivo high-resolution MR imaging of symptomatic and asymptomatic middle cerebral artery atherosclerotic stenosis. Atherosclerosis 2010;212(2):507–511. Crossref, MedlineGoogle Scholar
  • 24. Kern R, Steinke W, Daffertshofer M, Prager R, Hennerici M. Stroke recurrences in patients with symptomatic vs asymptomatic middle cerebral artery disease. Neurology 2005;65(6):859–864. Crossref, MedlineGoogle Scholar
  • 25. Wasserman BA, Smith WI, Trout HH 3rd, Cannon RO 3rd, Balaban RS, Arai AE. Carotid artery atherosclerosis: in vivo morphologic characterization with gadolinium-enhanced double-oblique MR imaging initial results. Radiology 2002;223(2):566–573. LinkGoogle Scholar
  • 26. Yuan C, Kerwin WS, Ferguson MS, et al. Contrast-enhanced high resolution MRI for atherosclerotic carotid artery tissue characterization. J Magn Reson Imaging 2002;15(1):62–67. Crossref, MedlineGoogle Scholar
  • 27. Wasserman BA. Advanced contrast-enhanced MRI for looking beyond the lumen to predict stroke: building a risk profile for carotid plaque. Stroke 2010;41(10 Suppl):S12–S16. Crossref, MedlineGoogle Scholar
  • 28. Wasserman BA, Wityk RJ, Trout HH 3rd, Virmani R. Low-grade carotid stenosis: looking beyond the lumen with MRI. Stroke 2005;36(11):2504–2513. Crossref, MedlineGoogle Scholar
  • 29. de Boer OJ, van der Wal AC, Teeling P, Becker AE. Leucocyte recruitment in rupture prone regions of lipid-rich plaques: a prominent role for neovascularization? Cardiovasc Res 1999;41(2):443–449. Crossref, MedlineGoogle Scholar
  • 30. Celletti FL, Waugh JM, Amabile PG, Brendolan A, Hilfiker PR, Dake MD. Vascular endothelial growth factor enhances atherosclerotic plaque progression. Nat Med 2001;7(4):425–429. Crossref, MedlineGoogle Scholar
  • 31. Rudd JH, Warburton EA, Fryer TD, et al. Imaging atherosclerotic plaque inflammation with [18F]-fluorodeoxyglucose positron emission tomography. Circulation 2002;105(23):2708–2711. Crossref, MedlineGoogle Scholar
  • 32. Calcagno C, Cornily JC, Hyafil F, et al. Detection of neovessels in atherosclerotic plaques of rabbits using dynamic contrast enhanced MRI and 18F-FDG PET. Arterioscler Thromb Vasc Biol 2008;28(7):1311–1317. Crossref, MedlineGoogle Scholar
  • 33. Phinikaridou A, Ruberg FL, Hallock KJ, et al. In vivo detection of vulnerable atherosclerotic plaque by MRI in a rabbit model. Circ Cardiovasc Imaging 2010;3(3):323–332. Crossref, MedlineGoogle Scholar
  • 34. Vergouwen MD, Silver FL, Mandell DM, Mikulis DJ, Swartz RH. Eccentric narrowing and enhancement of symptomatic middle cerebral artery stenoses in patients with recent ischemic stroke. Arch Neurol 2011;68(3):338–342. Crossref, MedlineGoogle Scholar
  • 35. Lau AY, Zhao Y, Chen C, et al. Dual antiplatelets reduce microembolic signals in patients with transient ischemic attack and minor stroke: subgroup analysis of CLAIR study. Int J Stroke 2013 Mar 12. [Epub ahead of print] Google Scholar
  • 36. Wang TH, Bhatt DL, Fox KA, et al. An analysis of mortality rates with dual-antiplatelet therapy in the primary prevention population of the CHARISMA trial. Eur Heart J 2007;28(18):2200–2207. Crossref, MedlineGoogle Scholar
  • 37. Chimowitz MI, Lynn MJ, Derdeyn CP, et al. Stenting versus aggressive medical therapy for intracranial arterial stenosis. N Engl J Med 2011;365(11):993–1003. Crossref, MedlineGoogle Scholar
  • 38. Aoki S, Aoki K, Ohsawa S, Nakajima H, Kumagai H, Araki T. Dynamic MR imaging of the carotid wall. J Magn Reson Imaging 1999;9(3):420–427. Crossref, MedlineGoogle Scholar
  • 39. Lipinski MJ, Amirbekian V, Frias JC, et al. MRI to detect atherosclerosis with gadolinium-containing immunomicelles targeting the macrophage scavenger receptor. Magn Reson Med 2006;56(3):601–610. Crossref, MedlineGoogle Scholar
  • 40. Nahrendorf M, Jaffer FA, Kelly KA, et al. Noninvasive vascular cell adhesion molecule-1 imaging identifies inflammatory activation of cells in atherosclerosis. Circulation 2006;114(14):1504–1511. Crossref, MedlineGoogle Scholar
  • 41. Kooi ME, Cappendijk VC, Cleutjens KB, et al. Accumulation of ultrasmall superparamagnetic particles of iron oxide in human atherosclerotic plaques can be detected by in vivo magnetic resonance imaging. Circulation 2003;107(19):2453–2458. Crossref, MedlineGoogle Scholar

Article History

Received December 19, 2012; revision requested January 31, 2013; revision received June 24; accepted July 10; final version accepted October 8.
Published online: Jan 16 2014
Published in print: May 2014