Skip to main content

Histologic and Biochemical Composition of Carotid Plaque and Its Impact on Ultrasonographic Appearance

  • Chapter
  • First Online:
Multi-Modality Atherosclerosis Imaging and Diagnosis
  • 1245 Accesses

Abstract

Carotid ultrasound has been used in research as a tool to assess plaque composition and therefore indirectly plaque stability. Plaques that are prone to rupture are lipid rich, have a larger core covered by a thin fibrous cap, and are rich in inflammatory cells that secrete enzymes that degrade the extracellular matrix. This phenotype can be reflected in the ultrasound images. Echolucent plaques have more lipid, less calcium, more inflammation, and more matrix degradation than the echogenic ones, which can explain why they are also associated with higher risk for stroke. Further studies and technical improvements are needed so that carotid ultrasound can reflect more relevant plaque characteristics that are important for the risk of rupture and implementation in clinical scenarios. In the chapter, the pathophysiology of atherosclerosis is revised, as well as plaque composition. Finally, the focus is on how ultrasound has been contributing to the characterization of plaque components in the last decades, with a glimpse on the future trends.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 169.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 219.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 219.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  1. Aschoff L (1930) Die arteriosklerose. Mediz Klinik (suppl 1):1–20

    Google Scholar 

  2. Nordestgaard BG (1996) The vascular endothelial barrier – selective retention of lipoproteins. Curr Opin Lipidol 7(5):269–273

    Article  PubMed  CAS  Google Scholar 

  3. Palinski W, Hörkkö S, Miller E, Steinbrecher UP, Powell HC, Curtiss LK et al (1996) Cloning of monoclonal autoantibodies to epitopes of oxidized lipoproteins from apolipoprotein E-deficient mice. demonstration of epitopes of oxidized low density lipoprotein in human plasma. J Clin Invest 98(3):800–814

    Article  PubMed  CAS  Google Scholar 

  4. Palinski W, Rosenfeld ME, Ylä-Herttuala S, Gurtner GC, Socher SS, Butler SW et al (1989) Low density lipoprotein undergoes modification in vivo. Proc Natl Acad Sci USA 86:1372–1376

    Article  PubMed  CAS  Google Scholar 

  5. Seifert PS, Hugo F, Hansson GK, Bhakdi S (1989) Prelesional complement activation in experimental atherosclerosis. Terminal C5b-9 complement deposition coincides with cholesterol accumulation in the aortic intima of hypercholesterolemic rabbits. Lab Invest 60(6):747–754

    PubMed  CAS  Google Scholar 

  6. Walpola PL, Gotlieb AI, Cybulsky MI, Langille BL (1995) Expression of ICAM-1 and VCAM-1 and monocyte adherence in arteries exposed to altered shear stress. Arterioscler Thromb Vasc Biol 15(1):2–10

    Article  PubMed  CAS  Google Scholar 

  7. Brown MS, Goldstein JL (1983) Lipoprotein metabolism in the macrophage: implications for cholesterol deposition in atherosclerosis. Annu Rev Biochem 52:223–261 [Review]

    Article  PubMed  CAS  Google Scholar 

  8. Lehr HA, Seemuller J, Hubner C, Menger MD, Messmer K (1993) Oxidized LDL-induced leukocyte/endothelium interaction in vivo involves the receptor for platelet-activating factor. Arterioscler Thromb 13(7):1013–1018

    Article  PubMed  CAS  Google Scholar 

  9. Watson AD, Navab M, Hama SY, Sevanian A, Prescott SM, Stafforini DM et al (1995) Effect of platelet activating factor-acetylhydrolase on the formation and action of minimally oxidized low density lipoprotein. J Clin Invest 95:774–782

    Article  PubMed  CAS  Google Scholar 

  10. Hansson GK (1997) Cell-mediated immunity in atherosclerosis. Curr Opin Lipidol 8(5):301–311

    Article  PubMed  CAS  Google Scholar 

  11. Stemme S, Faber B, Holm J, Wiklund O, Witztum JL, Hansson GK (1995) T lymphocytes from human atherosclerotic plaques recognize oxidized low density lipoprotein. Proc Natl Acad Sci USA 92:3893–3897

    Article  PubMed  CAS  Google Scholar 

  12. Parums DV, Chadwick DR, Mitchinson MJ (1986) The localisation of immunoglobulin in chronic periaortitis. Atherosclerosis 61(2):117–123

    Article  PubMed  CAS  Google Scholar 

  13. Sohma Y, Sasano H, Shiga R, Saeki S, Suzuki T, Nagura H et al (1995) Accumulation of plasma cells in atherosclerotic lesions of Watanabe heritable hyperlipidemic rabbits. Proc Natl Acad Sci USA 92(11):4937–4941

    Article  PubMed  CAS  Google Scholar 

  14. Kovanen PT, Kaartinen M, Paavonen T (1995) Infiltrates of activated mast cells at the site of coronary atheromatous erosion or rupture in myocardial infarction. Circulation 92(5):1084–1088

    Article  PubMed  CAS  Google Scholar 

  15. Kleindienst R, Xu Q, Willeit J, Waldenberger FR, Weimann S, Wick G (1993) Immunology of atherosclerosis. Demonstration of heat shock protein 60 expression and T lymphocytes bearing alpha/beta or gamma/delta receptor in human atherosclerotic lesions. Am J Pathol 142(6):1927–1937

    PubMed  CAS  Google Scholar 

  16. Melian A, Geng YJ, Sukhova GK, Libby P, Porcelli SA (1999) CD1 expression in human atherosclerosis. A potential mechanism for T cell activation by foam cells. Am J Pathol 155(3):775–786

    Article  PubMed  CAS  Google Scholar 

  17. Imparato AM, Riles TS, Mintzer R, Baumann FG (1983) The importance of hemorrhage in the relationship between gross morphologic characteristics and cerebral symptoms in 376 carotid artery plaques. Ann Surg 197(2):195–203

    Article  PubMed  CAS  Google Scholar 

  18. Aburahma AF, Robinson P, Decanio R (1989) Prospective clinicopathologic study of carotid intraplague hemorrhage. Am Surg 55(3):169–173

    PubMed  CAS  Google Scholar 

  19. McCarthy MJ, Loftus IM, Thompson MM, Jones L, London NJ, Bell PR et al (1999) Angiogenesis and the atherosclerotic carotid plaque: an association between symptomatology and plaque morphology. J Vasc Surg 30(2):261–268

    Article  PubMed  CAS  Google Scholar 

  20. Neote K, Darbonne W, Ogez J, Horuk R, Schall TJ (1993) Identification of a promiscuous inflammatory peptide receptor on the surface of red blood cells. J Biol Chem 268(17):12247–12249

    PubMed  CAS  Google Scholar 

  21. Yuan XM, Brunk UT, Olsson AG (1995) Effects of iron- and hemoglobin-loaded human monocyte-derived macrophages on oxidation and uptake of LDL. Arterioscler Thromb Vasc Biol 15(9):1345–1351

    Article  PubMed  CAS  Google Scholar 

  22. Kolodgie FD, Gold HK, Burke AP, Fowler DR, Kruth HS, Weber DK et al (2003) Intraplaque hemorrhage and progression of coronary atheroma. N Engl J Med 349(24):2316–2325

    Article  PubMed  CAS  Google Scholar 

  23. Falk E, Shah PK, Fuster V (1995) Coronary plaque disruption. Circulation 92(3):657–671

    Article  PubMed  CAS  Google Scholar 

  24. Gertz SD, Roberts WC (1990) Hemodynamic shear force in rupture of coronary arterial atherosclerotic plaques. Am J Cardiol 66(19):1368–1372

    Article  PubMed  CAS  Google Scholar 

  25. Stein PD, Hamid MS, Shivkumar K, Davis TP, Khaja F, Henry JW (1994) Effects of cyclic flexion of coronary arteries on progression of atherosclerosis. Am J Cardiol 73(7):431–437

    Article  PubMed  CAS  Google Scholar 

  26. Cheng GC, Loree HM, Kamm RD, Fishbein MC, Lee RT (1993) Distribution of circumferential stress in ruptured and stable atherosclerotic lesions. A structural analysis with histopathological correlation. Circulation 87(4):1179–1187

    Article  PubMed  CAS  Google Scholar 

  27. Richardson PD, Davies MJ, Born GV (1989) Influence of plaque configuration and stress distribution on fissuring of coronary atherosclerotic plaques. Lancet 2(8669):941–944

    Article  PubMed  CAS  Google Scholar 

  28. Bogaty P, Hackett D, Davies G, Maseri A (1994) Vasoreactivity of the culprit lesion in unstable angina. Circulation 90(1):5–11

    Article  PubMed  CAS  Google Scholar 

  29. Crawford ES, Crawford JL (1984) Aortitis. In: Tracy TT (ed) Disease of the aorta Including an atlas of angiographic pathology and surgical technique. Williams & Wilkins, Baltimore/London, pp 272–86

    Google Scholar 

  30. Jander S, Sitzer M, Wendt A, Schroeter M, Buchkremer M, Siebler M et al (2001) Expression of tissue factor in high-grade carotid artery stenosis: association with plaque destabilization. Stroke 32(4):850–854

    Article  PubMed  CAS  Google Scholar 

  31. Bevilacqua MP, Schleef RR, Gimbrone MA Jr, Loskutoff DJ (1986) Regulation of the fibrinolytic system of cultured human vascular endothelium by interleukin 1. J Clin Invest 78(2):587–591

    Article  PubMed  CAS  Google Scholar 

  32. Fuster V, Lewis A (1994) Conner Memorial Lecture. Mechanisms leading to myocardial infarction: insights from studies of vascular biology. Circulation 90(4):2126–2146

    Article  PubMed  CAS  Google Scholar 

  33. Stary HC, Chandler AB, Dinsmore RE, Fuster V, Glagov S, Insull W Jr et al (1995) A definition of advanced types of atherosclerotic lesions and a histological classification of atherosclerosis : a report from the Committee on Vascular Lesions of the Council on Arteriosclerosis, American Heart Association. Circulation 92(5):1355–1374

    Article  PubMed  CAS  Google Scholar 

  34. Falk E (1983) Plaque rupture with severe pre-existing stenosis precipitating coronary thrombosis. Characteristics of coronary atherosclerotic plaques underlying fatal occlusive thrombi. Br Heart J 50(2):127–134

    Article  PubMed  CAS  Google Scholar 

  35. Davies MJ, Thomas AC (1985) Plaque fissuring – the cause of acute myocardial infarction, sudden ischaemic death, and crescendo angina. Br Heart J 53(4):363–373

    Article  PubMed  CAS  Google Scholar 

  36. Naghavi M, Libby P, Falk E, Casscells SW, Litovsky S, Rumberger J et al (2003) From vulnerable plaque to vulnerable patient: a call for new definitions and risk assessment strategies: part I. Circulation 108(14):1664–1672

    Article  PubMed  Google Scholar 

  37. Naghavi M, Libby P, Falk E, Casscells SW, Litovsky S, Rumberger J et al (2003) From vulnerable plaque to vulnerable patient: a call for new definitions and risk assessment strategies: part II. Circulation 108(15):1772–1778

    Article  PubMed  Google Scholar 

  38. Gronholdt ML, Nordestgaard BG, Schroeder TV, Vorstrup S, Sillesen H (2001) Ultrasonic echolucent carotid plaques predict future strokes. Circulation 104(1):68–73

    Article  PubMed  CAS  Google Scholar 

  39. Rubin JR, Bondi JA, Rhodes RS (1987) Duplex scanning versus conventional arteriography for the evaluation of carotid artery plaque morphology. Surgery 102(4):749–755

    PubMed  CAS  Google Scholar 

  40. Pedro LM, Pedro MM, Goncalves I, Carneiro TF, Balsinha C, Fernandes e Fernandes R et al (2000) Computer-assisted carotid plaque analysis: characteristics of plaques associated with cerebrovascular symptoms and cerebral infarction. Eur J Vasc Endovasc Surg 19(2):118–123

    Article  PubMed  CAS  Google Scholar 

  41. Meairs S, Hennerici M (1999) Four-dimensional ultrasonographic characterization of plaque surface motion in patients with symptomatic and asymptomatic carotid artery stenosis. Stroke 30(9):1807–1813

    Article  PubMed  CAS  Google Scholar 

  42. Kolodgie FD, Burke AP, Farb A, Gold HK, Yuan J, Narula J et al (2001) The thin-cap fibroatheroma: a type of vulnerable plaque: the major precursor lesion to acute coronary syndromes. Curr Opin Cardiol 16(5):285–292

    Article  PubMed  CAS  Google Scholar 

  43. Virmani R, Kolodgie FD, Burke AP, Farb A, Schwartz SM (2000) Lessons from sudden coronary death. A comprehensive morphological classification scheme for atherosclerotic lesions. Arterioscler Thromb Vasc Biol 20:1262–1275

    Article  PubMed  CAS  Google Scholar 

  44. Goldstein JA, Demetriou D, Grines CL, Pica M, Shoukfeh M, O’Neill WW (2000) Multiple complex coronary plaques in patients with acute myocardial infarction. N Engl J Med 343(13):915–922

    Article  PubMed  CAS  Google Scholar 

  45. Moulton KS (2001) Plaque angiogenesis and atherosclerosis. Curr Atheroscler Rep 3(3):225–233

    Article  PubMed  CAS  Google Scholar 

  46. Targonski PV, Bonetti PO, Pumper GM, Higano ST, Holmes DR Jr, Lerman A (2003) Coronary endothelial dysfunction is associated with an increased risk of cerebrovascular events. Circulation 107(22):2805–2809

    Article  PubMed  Google Scholar 

  47. Varnava AM, Mills PG, Davies MJ (2002) Relationship between coronary artery remodeling and plaque vulnerability. Circulation 105(8):939–943

    Article  PubMed  Google Scholar 

  48. Farb A, Burke AP, Tang AL, Liang TY, Mannan P, Smialek J et al (1996) Coronary plaque erosion without rupture into a lipid core. A frequent cause of coronary thrombosis in sudden coronary death. Circulation 93(7):1354–1363

    Article  PubMed  CAS  Google Scholar 

  49. Kolodgie FD, Burke AP, Wight TN, Virmani R (2004) The accumulation of specific types of proteoglycans in eroded plaques: a role in coronary thrombosis in the absence of rupture. Curr Opin Lipidol 15(5):575–582

    Article  PubMed  CAS  Google Scholar 

  50. Waksman R, Serruys PW (2004) Handbook of the vulnerable plaque. Taylor & Francis Group, London

    Google Scholar 

  51. Falk E (1992) Why do plaques rupture? Circulation 86(6 Suppl):III30–III42

    PubMed  CAS  Google Scholar 

  52. Falk E, Fuster V (1995) Angina pectoris and disease progression. Circulation 92(8):2033–2035

    Article  PubMed  CAS  Google Scholar 

  53. Jespersen SK, Wilhjelm JE, Sillesen H (1998) Multi-angle compound imaging. Ultrason Imaging 20(2):81–102

    Article  PubMed  CAS  Google Scholar 

  54. Kern R, Szabo K, Hennerici M, Meairs S (2004) Characterization of carotid artery plaques using real-time compound B-mode ultrasound. Stroke 35(4):870–875

    Article  PubMed  Google Scholar 

  55. Delcker A, Schurks M, Polz H (1999) Development and applications of 4-D ultrasound (dynamic 3-D) in neurosonology. J Neuroimaging 9(4):229–234

    PubMed  CAS  Google Scholar 

  56. Fenster A, Landry A, Downey DB, Hegele RA, Spence JD (2004) 3D ultrasound imaging of the carotid arteries. Curr Drug Targets Cardiovasc Haematol Disord 4(2):161–175

    Article  PubMed  CAS  Google Scholar 

  57. Reilly LM, Lusby RJ, Hughes L, Ferrell LD, Stoney RJ, Ehrenfeld WK (1983) Carotid plaque histology using real-time ultrasonography. Clinical and therapeutic implications. Am J Surg 146(2):188–193

    Article  PubMed  CAS  Google Scholar 

  58. Johnson JM, Kennelly MM, Decesare D, Morgan S, Sparrow A (1985) Natural history of asymptomatic carotid plaque. Arch Surg 120(9):1010–1012

    Article  PubMed  CAS  Google Scholar 

  59. Gray-Weale AC, Graham JC, Burnett JR, Byrne K, Lusby RJ (1988) Carotid artery atheroma: comparison of preoperative B-mode ultrasound appearance with carotid endarterectomy specimen pathology. J Cardiovasc Surg (Torino) 29(6):676–681

    CAS  Google Scholar 

  60. Langsfeld M, Gray-Weale AC, Lusby RJ (1989) The role of plaque morphology and diameter reduction in the development of new symptoms in asymptomatic carotid arteries. J Vasc Surg 9(4):548–557

    PubMed  CAS  Google Scholar 

  61. Geroulakos G, Ramaswami G, Nicalaides A, James K, Labropoulos N, Belcaro G et al (1993) Characterization of symptomatic and asymptomatic carotid plaques using high-resolution real-time ultrasonography. Br J Surg 80:1274–1277

    Article  PubMed  CAS  Google Scholar 

  62. Group ECPS (1995) Carotid artery plaque composition: relationship to clinical presentation and ultrasound B-mode imaging. Eur J Vasc Endovasc Surg 10:23–30

    Article  Google Scholar 

  63. Hallerstam S, Carlstrom C, Zetterling M, Konrad P, Rosfors S (2000) Carotid atherosclerosis in relation to symptoms from the territory supplied by the carotid artery. Eur J Vasc Endovasc Surg 19(4):356–361

    Article  PubMed  CAS  Google Scholar 

  64. Holdsworth RJ, McCollum PT, Bryce JS, Harrison DK (1995) Symptoms, stenosis and carotid plaque morphology. Is plaque morphology relevant? Eur J Vasc Endovasc Surg 9(1):80–85

    Article  PubMed  CAS  Google Scholar 

  65. Elatrozy T, Nicolaides A, Tegos T, Zarka AZ, Griffin M, Sabetai M (1998) The effect of B-mode ultrasonic image standardisation on the echodensity of symptomatic and asymptomatic carotid bifurcation plaques. Int Angiol 17(3):179–186

    PubMed  CAS  Google Scholar 

  66. Elatrozy T, Nicolaides A, Tegos T, Griffin M (1998) The objective characterisation of ultrasonic carotid plaque features. Eur J Vasc Endovasc Surg 16(3):223–230

    Article  PubMed  CAS  Google Scholar 

  67. el-Barghouty N, Geroulakos G, Nicolaides A, Androulakis A, Bahal V (1995) Computer-assisted carotid plaque characterisation. Eur J Vasc Endovasc Surg 9(4):389–393

    Article  PubMed  CAS  Google Scholar 

  68. El-Barghouty N, Nicoalides A, Bahal V, Geroulakos G, Androulakis A (1996) The identification of the high risk carotid plaque. Eur J Vasc Endovasc Surg 11:470–478

    Article  PubMed  CAS  Google Scholar 

  69. Pedro LM, Pedro MM, Goncalves I, Carneiro TF, Balsinha C, Fernandes e Fernandes R et al (1999) [Atheroma plaque of the carotid bifurcation: how to identify an “active” lesion?]. Rev Port Cardiol 18(7–8):699–708

    PubMed  CAS  Google Scholar 

  70. Biasi GM, Mingazzini PM, Baronio L, Piglionica MR, Ferrari SA, Elatrozy TS et al (1998) Carotid plaque characterization using digital image processing and its potential in future studies of carotid endarterectomy and angioplasty. J Endovasc Surg 5(3):240–246

    Article  PubMed  CAS  Google Scholar 

  71. O’Holleran LW, Kennelly MM, McClurken M, Johnson JM (1987) Natural history of asymptomatic carotid plaque. Five year follow-up study. Am J Surg 154(6):659–662

    Article  PubMed  Google Scholar 

  72. Polak JF, Shemanski L, O’Leary DH, Lefkowitz D, Price TR, Savage PJ et al (1998) Hypoechoic plaque at US of the carotid artery: an independent risk factor for incident stroke in adults aged 65 years or older. Cardiovascular Health Study. Radiology 208(3):649–654

    PubMed  CAS  Google Scholar 

  73. Liapis CD, Kakisis JD, Kostakis AG (2001) Carotid stenosis. Factors affecting symptomatology. Stroke 32:2782–2786

    Article  PubMed  CAS  Google Scholar 

  74. Mathiesen EB, Bonaa KH, Joakimsen O (2001) Echolucent plaques are associated with high risk of ischemic cerebrovascular events in carotid stenosis: the tromso study. Circulation 103(17):2171–2175

    Article  PubMed  CAS  Google Scholar 

  75. Sterpetti AV, Schultz RD, Feldhaus RJ, Davenport KL, Richardson M, Farina C et al (1988) Ultrasonographic features of carotid plaque and the risk of subsequent neurologic deficits. Surgery 104(4):652–660

    PubMed  CAS  Google Scholar 

  76. Leahy AL, McCollum PT, Feeley TM, Sugrue M, Grouden MC, O’Connell DJ et al (1988) Duplex ultrasonography and selection of patients for carotid endarterectomy: plaque morphology or luminal narrowing? J Vasc Surg 8(5):558–562

    PubMed  CAS  Google Scholar 

  77. Matalanis G, Lusby RJ (1988) Is there still a place for carotid endarterectomy? Clin Exp Neurol 25:17–26

    PubMed  CAS  Google Scholar 

  78. Giannoni MF, Speziale F, Faraglia V, Sbarigia E, Zaccaria A, Lauri D et al (1991) Minor asymptomatic carotid stenosis contralateral to carotid endarterectomy (CEA): our experience. Eur J Vasc Surg 5(3):237–245

    Article  PubMed  CAS  Google Scholar 

  79. Belcaro G, Laurora G, Cesarone MR, De Sanctis MT, Incandela L, Fascetti E et al (1993) Ultrasonic classification of carotid plaques causing less than 60% stenosis according to ultrasound morphology and events. J Cardiovasc Surg (Torino) 34(4):287–294

    CAS  Google Scholar 

  80. Comerota AJ, Katz ML, White JV, Grosh JD (1990) The preoperative diagnosis of the ulcerated carotid atheroma. J Vasc Surg 11(4):505–510

    PubMed  CAS  Google Scholar 

  81. Bluth EI, McVay LV 3rd, Merritt CR, Sullivan MA (1988) The identification of ulcerative plaque with high resolution duplex carotid scanning. J Ultrasound Med 7(2):73–76

    PubMed  CAS  Google Scholar 

  82. O’Leary DH, Holen J, Ricotta JJ, Roe S, Schenk EA (1987) Carotid bifurcation disease: prediction of ulceration with B-mode US. Radiology 162(2):523–525

    PubMed  Google Scholar 

  83. Bassiouny HS, Sakaguchi Y, Mikucki SA, McKinsey JF, Piano G, Gewertz BL et al (1997) Juxtalumenal location of plaque necrosis and neoformation in symptomatic carotid stenosis. J Vasc Surg 26:589–594

    Article  Google Scholar 

  84. Pedro LM, Fernandes e Fernandes J, Pedro MM, Goncalves I, Dias NV, Fernandes e Fernandes R et al (2002) Ultrasonographic risk score of carotid plaques. Eur J Vasc Endovasc Surg 24(6):492–498

    Article  PubMed  CAS  Google Scholar 

  85. Sabetai MM, Tegos TJ, Nicolaides AN, El-Atrozy TS, Dhanjil S, Griffin M et al (2000) Hemispheric symptoms and carotid plaque echomorphology. J Vasc Surg 31(1 Pt 1):39–49

    Article  PubMed  CAS  Google Scholar 

  86. Iannuzzi A, Wilcosky T, Mercuri M, Rubba P, Bryan FA, Bond MG (1995) Ultrasonographic correlates of carotid atherosclerosis in transient ischemic attack and stroke. Stroke 26(4):614–619

    Article  PubMed  CAS  Google Scholar 

  87. Wolverson MK, Bashiti HM, Peterson GJ (1983) Ultrasonic tissue characterisation of atheromatous plaques using a high resolution real time scanner. Ultrasound Med Biol 9:599–609

    Article  PubMed  CAS  Google Scholar 

  88. Montauban van Swijndregt AD, Elbers HR, Moll FL, de Letter J, Ackerstaff RG (1998) Ultrasonographic characterization of carotid plaques. Ultrasound Med Biol 24(4):489–493

    Article  PubMed  CAS  Google Scholar 

  89. Montauban van Swijndregt AD, Elbers HR, Moll FL, de Letter J, Ackerstaff RG (1999) Cerebral ischemic disease and morphometric analyses of carotid plaques. Ann Vasc Surg 13(5):468–474

    Article  PubMed  CAS  Google Scholar 

  90. Kardoulas DG, Katsamouris AN, Gallis PT, Philippides TP, Anagnostakos NK, Gorgoyannis DS et al (1996) Ultrasonographic and histologic characteristics of symptom-free and symptomatic carotid plaque. Cardiovasc Surg 4(5):580–590

    Article  PubMed  CAS  Google Scholar 

  91. Lammie GA, Wardlaw J, Allan P, Ruckley CV, Peek R, Signorini DF (2000) What pathological components indicate carotid atheroma activity and can these be identified reliably using ultrasound? Eur J Ultrasound 11(2):77–86

    Article  PubMed  CAS  Google Scholar 

  92. Leen EJ, Feeley TM, Colgan MP, O’Malley MK, Moore DJ, Hourihane DO et al (1990) “Haemorrhagic” carotid plaque does not contain haemorrhage. Eur J Vasc Surg 4(2):123–128

    Article  PubMed  CAS  Google Scholar 

  93. Milei J, Parodi JC, Ferreira M, Barrone A, Grana DR, Matturri L (2003) Atherosclerotic plaque rupture and intraplaque hemorrhage do not correlate with symptoms in carotid artery stenosis. J Vasc Surg 38(6):1241–1247

    Article  PubMed  Google Scholar 

  94. El-Barghouty NM, Levine T, Ladva S, Flanagan A, Nicolaides A (1996) Histological verification of computerised carotid plaque characterisation. Eur J Vasc Endovasc Surg 11(4):414–416

    Article  PubMed  CAS  Google Scholar 

  95. Gronholdt ML, Sillesen H, Wiebe BM, Laursen H, Nordestgaard BG (2001) Increased acute phase reactants are associated with levels of lipoproteins and increased carotid plaque volume. Eur J Vasc Endovasc Surg 21(3):227–234

    Article  PubMed  CAS  Google Scholar 

  96. Gronholdt ML, Nordestgaard BG, Nielsen TG, Sillesen H (1996) Echolucent carotid artery plaques are associated with elevated levels of fasting and postprandial triglyceride-rich lipoproteins. Stroke 27(12):2166–2172

    Article  PubMed  CAS  Google Scholar 

  97. Gronholdt ML, Nordestgaard BG, Bentzon J, Wiebe BM, Zhou J, Falk E et al (2002) Macrophages are associated with lipid-rich carotid artery plaques, echolucency on B-mode imaging, and elevated plasma lipid levels. J Vasc Surg 35(1):137–145

    PubMed  Google Scholar 

  98. Gronholdt ML, Wiebe BM, Laursen H, Nielsen TG, Schroeder TV, Sillesen H (1997) Lipid-rich carotid artery plaques appear echolucent on ultrasound B-mode images and may be associated with intraplaque haemorrhage. Eur J Vasc Endovasc Surg 14(6):439–445

    Article  PubMed  CAS  Google Scholar 

  99. Goncalves I, Lindholm MW, Pedro LM, Dias N, Fernandes e Fernandes J, Fredrikson GN et al (2004) Elastin and calcium rather than collagen or lipid content are associated with echogenicity of human carotid plaques. Stroke 35(12):2795–2800

    Article  PubMed  CAS  Google Scholar 

  100. Goncalves I, Moses J, Pedro LM, Dias N, Fernandes e Fernandes J, Nilsson J et al (2003) Echolucency of carotid plaques correlates with plaque cellularity. Eur J Vasc Endovasc Surg 26(1):32–38

    Article  PubMed  CAS  Google Scholar 

  101. Cheuk BL, Cheng SW (2011) Annexin A1 expression in atherosclerotic carotid plaques and its relationship with plaque characteristics. Eur J Vasc Endovasc Surg 41(3):364–371

    Article  PubMed  CAS  Google Scholar 

  102. Turu MM, Krupinski J, Catena E, Rosell A, Montaner J, Rubio F et al (2006) Intraplaque MMP-8 levels are increased in asymptomatic patients with carotid plaque progression on ultrasound. Atherosclerosis 187(1):161–169

    Article  PubMed  CAS  Google Scholar 

  103. Vik A, Mathiesen EB, Noto AT, Sveinbjornsson B, Brox J, Hansen JB (2007) Serum osteoprotegerin is inversely associated with carotid plaque echogenicity in humans. Atherosclerosis 191(1):128–134

    Article  PubMed  CAS  Google Scholar 

  104. Staub D, Partovi S, Schinkel AF, Coll B, Uthoff H, Aschwanden M et al (2011) Correlation of carotid artery atherosclerotic lesion echogenicity and severity at standard US with intraplaque neovascularization detected at contrast-enhanced US. Radiology 258(2):618–626

    Article  PubMed  Google Scholar 

  105. Owen DR, Shalhoub J, Miller S, Gauthier T, Doryforou O, Davies AH et al (2010) Inflammation within carotid atherosclerotic plaque: assessment with late-phase contrast-enhanced US. Radiology 255(2):638–644

    Article  PubMed  Google Scholar 

  106. Goncalves I, Stenström K, Skog G, Mattsson S, Nitulescu M, Nilsson J (2010) Dating components of human atherosclerotic plaques. Circ Res 106:1174–1177

    Article  PubMed  CAS  Google Scholar 

  107. Wohlin M, Sundstrom J, Andren B, Larsson A, Lind L (2009) An echolucent carotid artery intima-media complex is a new and independent predictor of mortality in an elderly male cohort. Atherosclerosis 205(2):486–491

    Article  PubMed  CAS  Google Scholar 

  108. Lind L, Andersson J, Ronn M, Gustavsson T (2007) The echogenecity of the intima-media complex in the common carotid artery is closely related to the echogenecity in plaques. Atherosclerosis 195(2):411–414

    Article  PubMed  CAS  Google Scholar 

  109. Kim DE, Kim JY, Schellingerhout D, Kim EJ, Kim HK, Lee S et al (2010) Protease imaging of human atheromata captures molecular information of atherosclerosis, complementing anatomic imaging. Arterioscler Thromb Vasc Biol 30(3):449–456

    Article  PubMed  CAS  Google Scholar 

  110. Nagano K, Yamagami H, Tsukamoto Y, Nagatsuka K, Yasaka M, Nagata I et al (2008) Quantitative evaluation of carotid plaque echogenicity by integrated backscatter analysis: correlation with symptomatic history and histologic findings. Cerebrovasc Dis 26(6):578–583

    Article  PubMed  Google Scholar 

  111. Ostling G, Hedblad B, Berglund G, Goncalves I (2007) Increased echolucency of carotid plaques in patients with type 2 diabetes. Stroke 38(7):2074–2078

    Article  PubMed  Google Scholar 

  112. Andersson J, Sundstrom J, Gustavsson T, Hulthe J, Elmgren A, Zilmer K et al (2009) Echogenecity of the carotid intima-media complex is related to cardiovascular risk factors, dyslipidemia, oxidative stress and inflammation: the Prospective Investigation of the Vasculature in Uppsala Seniors (PIVUS) study. Atherosclerosis 204(2):612–618

    Article  PubMed  CAS  Google Scholar 

  113. Kadoglou NP, Gerasimidis T, Moumtzouoglou A, Kapelouzou A, Sailer N, Fotiadis G et al (2008) Intensive lipid-lowering therapy ameliorates novel calcification markers and GSM score in patients with carotid stenosis. Eur J Vasc Endovasc Surg 35(6):661–668

    Article  PubMed  CAS  Google Scholar 

  114. Ostling G, Goncalves I, Wikstrand J, Berglund G, Nilsson J, Hedblad B (2011) Long-term treatment with low-dose metoprolol CR/XL is associated with increased plaque echogenicity: the Beta-blocker Cholesterol-lowering Asymptomatic Plaque Study (BCAPS). Atherosclerosis 215(2):440–445

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Isabel Gonçalves .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2014 Springer Science+Business Media, LLC

About this chapter

Cite this chapter

Gonçalves, I. (2014). Histologic and Biochemical Composition of Carotid Plaque and Its Impact on Ultrasonographic Appearance. In: Saba, L., Sanches, J., Pedro, L., Suri, J. (eds) Multi-Modality Atherosclerosis Imaging and Diagnosis. Springer, New York, NY. https://doi.org/10.1007/978-1-4614-7425-8_16

Download citation

  • DOI: https://doi.org/10.1007/978-1-4614-7425-8_16

  • Published:

  • Publisher Name: Springer, New York, NY

  • Print ISBN: 978-1-4614-7424-1

  • Online ISBN: 978-1-4614-7425-8

  • eBook Packages: MedicineMedicine (R0)

Publish with us

Policies and ethics