Skip to main content

Advertisement

SpringerLink
Log in

Imaging of carotid artery disease: from luminology to function?

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

A Lucien Appel Prize to this article was published on 20 January 2004

Abstract

There have been tremendous advances in our ability to image atheromatous disease, particularly in the carotid artery, which is accessible and large enough to image. The repertoire of methodology available is growing, giving anatomical information on luminal narrowing which is approaching the level at which conventional carotid angiography will become very uncommon as CT and contrast-enhanced MR angiographic techniques become the norm. More exciting is the tentative ability to perform functional plaque imaging addressing enhancement patterns and macrophage activity using MR or positron-emission tomography techniques. These techniques, once rigorously evaluated, may, in addition to complex mathematical modelling of plaque, eventually allow us to assess true plaque risk. Time will best judge whether we will be able to move from the use of simple luminology to assessment of plaque function.

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. 1A–C.
Fig. 2A, B.
Fig. 3A, B.
Fig. 4.
Fig. 5A, B.
Fig. 6A, B.
Fig. 7.
Fig. 8.
Fig. 9.
Fig. 10.
Fig. 11.

Similar content being viewed by others

References

  1. Barnett HJM, Taylor DW, Eliasziw M, et al (1998) Benefit of carotid endarterectomy in patients with symptomatic moderate or severe stenosis. N Engl J Med 339: 1415–1425

    CAS  PubMed  Google Scholar 

  2. Ferguson GG, Eliasziw M, Barr HWK, et al (1999) The North American symptomatic carotid endarterectomy trial. Surgical results in 1415 patients. Stroke 30: 1751–1758

    CAS  PubMed  Google Scholar 

  3. European Carotid Surgery Trialists’ collaborative group (1991) MRC European carotid surgery trial: interim results for symptomatic patients with severe (70–99%) or with mild (0–29%) carotid stenosis. Lancet 337: 1235–1243

    PubMed  Google Scholar 

  4. Benavente O, Moher D, Pham B (1998) Carotid endarterectomy for asymptomatic carotid stenosis: a meta-analysis. Br Med J 317: 1477–1480

    CAS  Google Scholar 

  5. Halliday AW, Thomas DJ, Mansfield AO (1995) The asymptomatic carotid surgery trial (ACST). Int Angiol 14: 18–20

    CAS  Google Scholar 

  6. Moore WS, Barnett HJM, Beebe HG, et al (1995) Guidelines for carotid endarterectomy: a multidisciplinary consensus statement from the ad hoc committee, American Heart Association. Stroke 26: 188–201

    PubMed  Google Scholar 

  7. Mann JM, Davies MJ (1996) Vulnerable plaque: relation of characteristics to degree of stenosis in human coronary arteries. Circulation 94: 928–931

    CAS  PubMed  Google Scholar 

  8. Streifler JY, Eliasziw M, Fox AJ, et al (1994) Angiographic detection of carotid plaque ulceration. Comparison with surgical observations in a multicenter study. Stroke 24: 1130–1132

    Google Scholar 

  9. Heiserman JE, Dean BL, Hodak JA, et al (1994) Neurologic complications of cerebral angiography. AJNR 15: 1401–1407

    CAS  Google Scholar 

  10. North American symptomatic carotid endarterectomy trial collaborators (1991) Beneficial effect of carotid endarterectomy in symptomatic patients with high-grade carotid stenosis. N Engl J Med 325: 445–453

    PubMed  Google Scholar 

  11. Rothwell PM, Gibson RJ, Slattery J, Sellar RJ, Warlow CP (1994) Equivalence of measurements of carotid stenosis: comparison of three methods on 1001 angiograms. Stroke 25: 2435–2439

    CAS  PubMed  Google Scholar 

  12. Nederkoorn PJ, Mali WT, Eikelboom BC, et al (2002) Preoperative diagnosis of carotid artery stenosis: accuracy of noninvasive testing. Stroke 33: 2003–2008

    Article  PubMed  Google Scholar 

  13. Hosomi N, Mizushige K, Ohuyama H, et al (2001) Angiotensin-converting enzyme inhibition with enalapril slows progressive intima-media thickening of the common carotid artery in patients with non-insulin dependent diabetes mellitus. Stroke 32: 1539–1545.

    CAS  PubMed  Google Scholar 

  14. Spence JD, Eliasziw M, DiCicco M, Hackam DG, Galil R, Lohmann T (2002) Carotid plaque area: a tool for targeting and evaluating vascular preventive therapy. Stroke 33: 2916–2922

    Article  PubMed  Google Scholar 

  15. AbuRahma AF, Wulu JT, Crotty B (2002) Carotid plaque ultrasonic heterogeneity and severity of stenosis. Stroke 33: 1772–1775

    Article  PubMed  Google Scholar 

  16. Tegos TJ, Kalomiris KJ, Sabetai MM, Kalodiki E, Nicolaides AN (2001) Significance of sonographic tissue and surface characteristics of carotid plaques. AJNR 22: 1605–1612

    CAS  Google Scholar 

  17. Tegos TJ, Sebetai MM, Nicolaides AN, et al (2000) Comparability of the ultrasonic tissue characteristics of carotid plaques. J Ultrasound Med 19: 399–407

    CAS  PubMed  Google Scholar 

  18. Tegos TJ, Sohail M, Sabetai MM, et al (2000) Echomorphologic and histopathologic characteristics of unstable carotid plaques. AJNR 21: 1937–1944

    CAS  Google Scholar 

  19. de Korte CL, Pasterkamp G, van der Steen AFW, Woutman HA, Bom N (2000) Characterisation of plaque components with intravascular ultrasound elastography in human femoral and coronary arteries in vitro. Circulation 102: 617–623

    PubMed  Google Scholar 

  20. Leclerc X, Godefroy O, Lucas C, et al (1999) Internal carotid arterial stenosis: CT angiography with volume rendering. Radiology 210: 673–682

    CAS  PubMed  Google Scholar 

  21. Porsche C, Walker LJ, Mendelow AD, Birchall D (2002) Assessment of vessel wall thickness in carotid atherosclerosis using spiral CT angiography. Eur J Vasc Endovasc Surg 23: 437–440

    Article  CAS  PubMed  Google Scholar 

  22. Anderson GB, Ashforth R, Steinke DE, Ferdinandy R, Findlay JM (2000) CT angiography for the detection and characterization of carotid artery bifurcation disease. Stroke 31: 2168–2174

    CAS  PubMed  Google Scholar 

  23. Walker LJ, Ismail A, McMeekin W, Lambert D, Mendelow AD, Birchall D (2002) Computed tomography angiography for the evaluation of carotid atherosclerotic plaque. Correlation with histopathology of endarterectomy specimens. Stroke 33: 977–981

    Article  PubMed  Google Scholar 

  24. Hunt JL, Fauirman R, Mitchell ME, et al (2002) Bone formation in carotid plaques. A clinicopathological study. Stroke 33: 1214–1219

    Article  PubMed  Google Scholar 

  25. Litt AW, Eidelman EM, Pinto RS, et al (1991) Diagnosis of carotid artery stenosis: comparison of 2D time-of-flight MR angiography with contrast angiography in 50 patients. AJNR 12: 149–154

    CAS  Google Scholar 

  26. Anderson CM, Saloner D, Lee RE, et al (1992) Assessment of carotid artery stenosis by MR angiography: comparison with X-ray angiography and color-coded Doppler ultrasound. AJNR 13: 989–1003

    CAS  Google Scholar 

  27. Westwood ME, Kelly S, Berry E, et al (2002) Use of magnetic resonance angiography to select candidates with recently symptomatic carotid stenosis for surgery: systematic review. Br Med J 324: 198

    Article  Google Scholar 

  28. Patel MR, Klufas RA, Kim D, Edelman RR, Kent KC (1993) MR angiography of the carotid bifurcation: artefacts and limitations. Am J Roentgenol 162: 1431–1437

    Google Scholar 

  29. Huston J, Fain SB, Wald JT, et al (2001) Carotid artery: elliptic centric contrast-enhanced MR angiography compared with conventional angiography. Radiology 218: 138–143

    PubMed  Google Scholar 

  30. Phan T, Huston J, Bernstein MA, Reiderer SJ, Brown RD (2001) Contrast-enhanced magnetic resonance angiography of the cervical vessels. Experience with 422 patients. Stroke 32: 2282–2286

    CAS  PubMed  Google Scholar 

  31. Johnston DCC, Eastwood JD, Nguyen T, Goldstein LB (2002) Contrast-enhanced magnetic resonance angiography of carotid arteries: utility in routine clinical practice. Stroke 33: 2834–2838

    Article  PubMed  Google Scholar 

  32. Wutke R, Lang W, Fellner C, et al (2002) High-resolution, contrast-enhanced magnetic resonance angiography with elliptic centric k-space ordering of supra-aortic arteries compared with selective X-ray angiography. Stroke 33: 1522–1529

    Article  PubMed  Google Scholar 

  33. Choudhury RP, Fuster V, Badimon JJ, Fisher EA, Fayad ZA (2002) MRI and characterization of atherosclerotic plaque. emerging applications and molecular imaging. Arterioscler Thromb Vasc Biol 22: 1065–1074

    Article  CAS  PubMed  Google Scholar 

  34. Quick HH, Debatin JF, Ladd DL (2002) MR imaging of the vessel wall. Eur Radiol 12: 889–900

    Article  PubMed  Google Scholar 

  35. Hayes CE, Mathis CM, Yuan C (1996) Surface coil phased arrays for high-resolution imaging of the carotid arteries. J Magn Reson Imaging 1: 109–112

    Google Scholar 

  36. Yuan C, Murakami JW, Hayes CE, et al (1995) Phased-array magnetic resonance imaging of the carotid bifurcation: preliminary results in healthy volunteers and in a patient with atherosclerotic disease. J Magn Reson Imaging 5: 561–565

    CAS  PubMed  Google Scholar 

  37. Martin AJ, Gotlieb AI, Henkelman RM (1995) High-resolution MR imaging of human arteries. J Magn Reson Imaging 5: 93–100

    CAS  PubMed  Google Scholar 

  38. Coombs BD, Rapp JH, Ursell PC, Reilly LM, Saloner D (2001) Structure of plaque at carotid bifurcation. High-resolution MRI with histological correlation. Stroke 32: 2516–2521

    CAS  PubMed  Google Scholar 

  39. Raynaud JS, Bridal SL, Toussaint JF, et al (1998) Characterization of atherosclerotic plaque components by high resolution quantitative MR and US imaging. J Magn Reson Imaging 8: 622–629

    CAS  PubMed  Google Scholar 

  40. Correia LCL, Atalar E, Kelemen MD, et al (1997) Intravascular magnetic resonance imaging of aortic atherosclerotic plaque composition. Arterioscler Thromb Vasc Biol 17: 3626–3632

    CAS  PubMed  Google Scholar 

  41. Rogers WJ, Prichard JW, Hu Y-L, et al (2000) Characterization of signal properties in atherosclerotic plaque components by intravascular MRI. Arterioscler Thromb Vasc Biol 20: 1824–1830

    CAS  PubMed  Google Scholar 

  42. Yuan C, Beach KW, Smith LH, Hatsukami TS (1998) Measurement of atherosclerotic carotid plaque size in vivo using high resolution magnetic resonance imaging. Circulation 98: 2666–2671

    CAS  PubMed  Google Scholar 

  43. Yuan C, Lin E, Millard J, Hwang JN (1999) Closed contour edge detection of black blood vessel lumen and outer wall boundaries in black-blood MR images. Magn Reson Imaging 17: 257–266

    Article  CAS  PubMed  Google Scholar 

  44. Toussaint JF, Southern JF, Fuster V, Kantor HL (1995) T2-weighted contrast for NMR characterization of human atherosclerosis. Arterioscler Thromb Vasc Biol 15: 1533–1542

    Google Scholar 

  45. Toussaint J-F, LaMuraglia GM, Southern JF, Fuster V, Kantor HL (1996) Magnetic resonance images lipid, fibrous, calcified, hemorrhagic, and thrombotic components of human atherosclerosis in vivo. Circulation 94: 932–938

    CAS  PubMed  Google Scholar 

  46. Hatsukami TS, Ross R, Polissar NL, Yuan C (2000) Visualization of fibrous cap thickness and rupture in human atherosclerotic carotid plaque in vivo with high-resolution magnetic resonance imaging. Circulation 102: 959–964

    CAS  PubMed  Google Scholar 

  47. Yuan C, Mitsumori LM, Ferguson MS, et al (2001) In vivo accuracy of multispectral magnetic resonance imaging for identifying lipid-rich necrotic cores and intraplaque hemorrhage in advanced human carotid plaques. Circulation 104: 2051–2056

    CAS  PubMed  Google Scholar 

  48. Fayad ZA, Fuster V (2001) Clinical imaging of high-risk or vulnerable atherosclerotic plaque. Circ Res 89: 305–316

    CAS  PubMed  Google Scholar 

  49. Yuan C, Mitsumori LM, Beach KW, Maravilla KR (2001) Carotid atherosclerotic plaque: noninvasive MR characterization and identification of vulnerable lesions. Radiology 221: 285–299

    CAS  PubMed  Google Scholar 

  50. Ross R (1999) Atherosclerosis—an inflammatory disease. N Engl J Med 340: 115–126

    CAS  PubMed  Google Scholar 

  51. Elkind MS, Cheng J, Boden-Albala B, et al (2002) Tumor necrosis factor levels are associated with carotid atherosclerosis. Stroke 33: 31–38

    Article  CAS  PubMed  Google Scholar 

  52. Curry AJ, Portig I, Goodall JC, Kirkpatrick PJ, Gaston JSH (2000) T lymphocyte lines isolated from atheromatous plaque contain cells capable of responding to Chlamydia antigens. Clin Exp Immunol 121: 261–269

    Article  CAS  PubMed  Google Scholar 

  53. van der Meer IM, de Maat MPM, Hak AE, et al (2002) C-reactive protein predicts progression of atherosclerosis measured at various sites in the arterial tree: the Rotterdam study. Stroke 33: 2750–2755

    Article  PubMed  Google Scholar 

  54. Kiechl S, Werner P, Egger G, et al (2002) Active and passive smoking, chronic infections, and the risk of carotid atherosclerosis. Prospective results from the Bruneck study. Stroke 33: 2170–2176

    Article  PubMed  Google Scholar 

  55. Labarrere CA, Lee JB, Nelson DR, Al-Hassani M, Miller SJ, Pitts DE (2002) C-reactive protein, arterial endothelial activation, and development of transplant coronary artery disease: a prospective study. Lancet 360: 1462–1467

    Article  CAS  PubMed  Google Scholar 

  56. Moreno PR, Falk E, Palacios IF, Newell JB, Fuster V, Fallon JT (1994) Macrophage infiltration in acute coronary syndromes. Implications for plaque rupture. Circulation 90: 775–778

    CAS  PubMed  Google Scholar 

  57. Prager M, Turel Z, Speidl WS, et al (2002) Chlamydia pneumoniae in carotid artery atherosclerosis: a comparison of its presence in atherosclerotic plaque, healthy vessels, and circulating leukocytes from the same individuals. Stroke 33: 2756–2761

    Article  PubMed  Google Scholar 

  58. Vallabhajosula S, Fuster V (1997) Atherosclerosis: imaging techniques and the evolving role of nuclear medicine. J Nucl Med 38: 1788–1796

    CAS  PubMed  Google Scholar 

  59. Vallabhajosula S (1999) Radioisotropic imaging of atheroma. In: Fuster V (ed) The vulnerable atherosclerotic plaque: understanding, identification, and modification. Futurea Publishing Company, Armonk NY, pp 213–229

  60. Rudd JH, Warburton EA, Fryer TD, et al (2002) Imaging atherosclerotic plaque inflammation with [18F]-fluorodeoxyglucose positron emission tomography. Circulation 105: 2708–2711

    Article  CAS  PubMed  Google Scholar 

  61. Lin W, Abendschein DR, Haake EM (1997) Contrast-enhanced magnetic resonance angiography of carotid arterial wall in pigs. J Magn Reson Imaging 7: 183–190

    CAS  PubMed  Google Scholar 

  62. Wasserman BA, Smith WI, Trout HH, Cannon RO, Balaban RS, Arai AE (2002) Carotid artery atherosclerosis: in vivo morphologic characterization with gadolinium-enhanced double-oblique MR imaging-initial results. Radiology 223: 566–573

    PubMed  Google Scholar 

  63. Mack MG, Balzer JO, Straub R, Eichler K, Vogl TJ (2002) Superparamagnetic iron oxide-enhanced MR imaging of head and neck lymph nodes. Radiology 222: 239–244

    PubMed  Google Scholar 

  64. Ruehm SG, Corot C, Vogt P, Kolb S, Debatin JF (2001) Magnetic resonance imaging of atherosclerotic plaque with ultrasmall superparamagnetic particles of iron oxide in hyperlipidemic rabbits. Circulation 103: 415–422

    CAS  PubMed  Google Scholar 

  65. Schmitz SA, Taupitz M, Wagner S, et al (2002) Iron oxide-enhanced magnetic resonance imaging of atherosclerotic plaques. Postmortem analysis of accuracy, inter-observer agreement, and pitfalls. Invest Radiol 37: 405–411

    Article  CAS  PubMed  Google Scholar 

  66. Schulz UGR, Rothwell PM (2001) Sex differences in carotid bifurcation anatomy and the distribution of atherosclerotic plaque. Stroke 32: 1525–1531

    CAS  PubMed  Google Scholar 

  67. Schulz UGR, Rothwell PM (2001) Major variation in carotid bifurcation anatomy. A possible risk factor for plaque development? Stroke 32: 2522–2529

    CAS  PubMed  Google Scholar 

  68. Wedding KL, Draney MT, Herfkens RJ, Zarins CK, Taylor CA, Pelc NJ (2002) Measurement of vessel wall strain using cine phase contrast MRI. J Magn Reson Imaging 15: 418–428

    Article  PubMed  Google Scholar 

  69. Kohler U, Marshall I, Robertson MB, Long Q, Xu XY, Hoskins PR (2001) MRI measurement of wall shear stress vectors in bifurcation models and comparison with CFD predictions. J Magn Reson Imaging 14: 563–573

    Article  CAS  PubMed  Google Scholar 

  70. Zienkiewicz OC, Taylor RL (1991) The finite element method. McGraw-Hill, New York

  71. Steinman DA, Thomas JB, Ladak HM, Milner JS, Rutt BK, Spence JD (2002) Reconstruction of carotid bifurcation hemodynamics and wall thickness using computational fluid dynamics and MRI. Magn Reson Med 47: 149–59

    Article  PubMed  Google Scholar 

  72. Crisby M, Nordin-Fredriksson G, Shah PK, Yano J, Zhu J, Nilsson J (2001) Pravastatin treatment increases collagen content and decreases lipid content, inflammation, metalloproteinases, and cell death in human carotid plaques. Implications for plaque stabilization. Circulation 103: 926–933

    CAS  PubMed  Google Scholar 

  73. Thies F, Garry JMC, Yaqoob P, et al (2003) Association of n-3 polyunsaturated fatty acids with stability of atherosclerotic plaques: a randomised controlled trial. Lancet 361: 477–485

    Article  CAS  PubMed  Google Scholar 

  74. Ichihara K, Satoh K (2002) Disparity between angiographic regression and clinical event rates with hydrophobic statins. Lancet 359: 2195–2198

    Article  PubMed  Google Scholar 

  75. Anon (1994) Effect of simvastatin on coronary atheroma: the multicentre anti-atheroma study (MAAS). Lancet 344: 633–638

    PubMed  Google Scholar 

  76. Jukema JW, Bruschke AVG, van Boven J, et al (1995) Effects of lipid lowering by pravastatin on progression and regression of coronary artery disease in symptomatic men with normal to moderately elevated serum cholesterol levels. The regression growth evaluation statin study (REGRESS). Circulation 91: 2528–2540

    CAS  PubMed  Google Scholar 

  77. Pitt B, Mancini GBJ, Ellis SG, Rosman HS, Park JS, McGovern ME (1995) Pravastatin limitation of atherosclerosis in coronary arteries (PLAC I): reduction in atherosclerosis progression and clinical events. J Am Coll Cardiol 26: 1133–1139

    Article  CAS  PubMed  Google Scholar 

  78. Helft G, Worthley SG, Fuster V, et al (2002) Progression and regression of atherosclerotic lesions. Monitoring with serial noninvasive magnetic resonance imaging. Circulation 105: 993–998

    Article  PubMed  Google Scholar 

  79. Zhao X-Q, Yuan C, Hatsukami TS, et al (2001) Effects of prolonged intensive lipid-lowering therapy on the characteristics of carotid atherosclerotic plaques in vivo by MRI. A case-control study. Arterioscler Thromb Vasc Bio 21: 1623–1629

    CAS  Google Scholar 

  80. Corti R, Fayad ZA, Fuster V, et al (2001) Effects of lipid-lowering by simvastatin on human atherosclerotic lesions. A longitudinal study of high-resolution, noninvasive magnetic resonance imaging. Circulation 104: 249–252

    CAS  PubMed  Google Scholar 

Download references

Acknowledgements

I am grateful for the expertise and advice of Nagui Antoun, Lol Berman, John Brown, Charlotte Cash, John Clark, Richard Coulden, Justin Cross, Tim Fryer, Martin Goddard, Jo Horsley, Martin Graves, Nick Higgins, Jean U-King-Im, Peter Kirkpatrick, Alonso Peña, John Pickard, James Rudd, Clare Sims, Rikin Trivedi, Liz Warburton, Liqun Wang and Peter Weissberg. Sinerem™ was kindly provided by Guerbet. Studies were funded by grants from NHS R&D Health Technology Assessment programme, the Stroke Association, the Wellcome Trust and GlaxoSmithKline.

Author information

Authors and Affiliations

  1. University Department of Radiology, Addenbrooke’s Hospital, Hills Road, Cambridge, CB2 2QQ, UK

    J. H. Gillard

Authors
  1. J. H. Gillard
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to J. H. Gillard.

Additional information

An addendum to this article can be found at http://dx.doi.org/10.1007/s00234-004-1161-y

Rights and permissions

Reprints and permissions

About this article

Cite this article

Gillard, J.H. Imaging of carotid artery disease: from luminology to function?. Neuroradiology 45, 671–680 (2003). https://doi.org/10.1007/s00234-003-1054-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00234-003-1054-5

Key words

Search

Navigation