Lessons from sudden coronary death: A comprehensive morphological classification scheme for atherosclerotic lesions

Arteriosclerosis, Thrombosis, and Vascular Biology

Volumn 20, Issue 5, 2000, Pages 1262-1275

  Virmani, Renu ^a   Kolodgie, Frank D ^a   Burke, Allen P ^a   Farb, Andrew ^a   Schwartz, Stephen M ^b  

^a ARMED FORCES INSTITUTE OF PATHOLOGY   (United States)

^b UNIVERSITY OF WASHINGTON   (United States)

Author keywords

Atherosclerosis classification; Coronary vessels pathology; Erosion; Rupture; Sudden coronary death

Indexed keywords

ARTICLE; ATHEROSCLEROSIS; ATHEROSCLEROTIC PLAQUE; AUTOPSY; CAUSE OF DEATH; CORONARY ARTERY DISEASE; DISEASE CLASSIFICATION; FIBROMUSCULAR DYSPLASIA; HISTOPATHOLOGY; HUMAN; NONHUMAN; PRIORITY JOURNAL; SUDDEN DEATH;

EID: 0034019601     PISSN: 10795642     EISSN: None     Source Type: Journal    
DOI: 10.1161/01.ATV.20.5.1262     Document Type: Article

References (75)

1. Davies MJ, Thomas AC. Plaque fissuring: the cause of acute myocardial infarction, sudden ischaemic death, and crescendo angina. Br Heart J. 1985;53:363-373.
2. Davies MJ. Anatomic features in victims of sudden coronary death: coronary artery pathology. Circulation. 1992;85:119-124.
3. Stary HC, Chandler AB, Glagov S, Guyton JR, Insull W Jr, Rosenfeld ME, Schaffer SA, Schwartz CJ, Wagner WD, Wissler RW. A definition of initial, fatty streak, and intermediate lesions of atherosclerosis: a report from the Committee on Vascular Lesions of the Council on Arteriosclerosis, American Heart Association. Arterioscler Thromb. 1994;14: 840-856.
4. Stary HC, Chandler AB, Dinsmore RE, Fuster V, Glagov S, Insull W Jr, Rosenfeld ME, Schwartz CJ, Wagner WD, Wissler RW. 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. Arterioscler Thromb Vasc Biol. 1995;15:1512-1531.
5. Virchow R. Cellular Pathology Based on Physiological and Pathological Histology. Birmingham, Ala: Classics of Medicine Library; 1858.
6. Ross R. Atherosclerosis: an inflammatory disease. N Engl J Med. 1999; 340:115-126.
7. Falk E, Shah PK, Fuster V. Coronary plaque disruption. Circulation. 1995;92:657-671.
8. Nobuyoshi M, Tanaka M, Nosaka H, Kimura T, Yokoi H, Hamasaki N, Kim K, Shindo T, Kimura K. Progression of coronary atherosclerosis: is coronary spasm related to progression? J Am Coll Cardiol. 1991;18: 904-910.
9. Giroud D, Li JM, Urban P, Meier B, Rutishauer W. Relation of the site of acute myocardial infarction to the most severe coronary arterial stenosis at prior angiography. Am J Cardiol. 1992;69:729-732.
10. Ambrose JA, Winters SL, Arora RR, Eng A, Riccio A, Gorlin R, Fuster V. Angiographic evolution of coronary artery morphology in unstable angina. J Am Coll Cardiol. 1986;7:472-478.
11. Caligiuri G, Levy B, Pernow J, Thoren P, Hansson GK. Myocardial infarction mediated by endothelin receptor signaling in hypercholesterolemic mice. Proc Natl Acad Sci U S A. 1999;96:6920-6924.
12. Prescott MF, Hasler-Rapacz J, von Linden-Reed J, Rapacz J. Familial hypercholesterolemia associated with coronary atherosclerosis in swine bearing different alleles for apolipoprotein B. Ann N Y Acad Sci. 1995; 748:283-292.
13. Fishbein MC, Siegel RJ. Pathology of coronary atherosclerosis: implications for intravascular ultrasound imaging. In: Siegel RJ, ed. Intravascular Ultrasound Imaging in Coronary Artery Disease. New York, NY: Marcel Dekker Inc; 1998:1-17.
14. Arbustini E, Grasso M, Diegoli M, Pucci A, Bramerio M, Ardissino D, Angoli L, de Servi S, Bramucci E, Mussini A, et al. Coronary atherosclerotic plaques with and without thrombus in ischemic heart syndromes: a morphologic, immunohistochemical, and biochemical study. Am J Cardiol. 1991;68:36B-50B.
15. van der Wal AC, Becker AE, van der Loos CM, Das PK. Site of intimai rupture or erosion of thrombosed coronary atherosclerotic plaques is characterized by an inflammatory process irrespective of the dominant plaque morphology. Circulation. 1994;89:36-44.
16. Farb A, Burke AP, Tang AL, Liang TY, Mannan P, Smialek J, Virmani R. Coronary plaque erosion without rupture into a lipid core: a frequent cause of coronary thrombosis in sudden coronary death. Circulation. 1996;93:1354-1363.
17. Farb A, Tang AL, Burke AP, Sessums L, Liang Y, Virmani R. Sudden coronary death: frequency of active coronary lesions, inactive coronary lesions, and myocardial infarction. Circulation. 1995;92:1701-1709.
18. Burke AP, Farb A, Liang YH, Smialek J, Virmani R. Effect of hypertension and cardiac hypertrophy on coronary artery morphology in sudden cardiac death. Circulation. 1996;94:3138-3145.
19. Burke AP, Farb A, Malcom GT, Liang YH, Smialek J, Virmani R. Coronary risk factors and plaque morphology in men with coronary disease who died suddenly. N Engl J Med. 1997;336:1276-1282.
20. Burke AP, Farb A, Kolodgie FD, Malcom GT, Virmani R. Healed ruptured plaques are frequent in men with severe coronary disease and are associated with elevated total/high density lipoprotein (HDL) cholesterol. Circulation. 1997;96(suppl I):I-235. Abstract.
21. Burke AP, Farb A, Malcom GT, Liang Y, Smialek J, Virmani R. Effect of risk factors on the mechanism of acute thrombosis and sudden coronary death in women. Circulation. 1998;97:2110-2116.
22. Burke AP, Farb A, Malcom GT, Liang Y, Smialek JE, Virmani R. Plaque rupture and sudden death related to exertion in men with coronary artery disease. JAMA. 1999;281:921-926.
23. Fishbein MC, Siegel RJ. How big are coronary atherosclerotic plaques that rupture? Circulation. 1996;94:2662-2666.
24. de Feyter PJ, Ozaki Y, Baptista J, Escaned J, Di Mario C, de Jaegere PP, Serruys PW, Roelandt JR. Ischemia-related lesion characteristics in patients with stable or unstable angina: a study with intracoronary angioscopy and ultrasound. Circulation. 1995;92:1408-1413.
25. Velican D, Velican C. Atherosclerotic involvement of the coronary arteries of adolescents and young adults. Atherosclerosis. 1980;36: 449-460.
26. Wissler RW, Vesselinovitch D. Comparative pathogenetic patterns in atherosclerosis. Adv Lipid Res. 1968;6:181-206.
27. Armstrong ML, Heistad DD, Megan MB, Lopez JA, Harrison DG. Reversibility of atherosclerosis. Cardiovasc Clin. 1990;20:113-126.
28. Strong JP, Malcom GT, McMahan CA, Tracy RE, Newman WP III, Herderick EE, Cornhill JF. Prevalence and extent of atherosclerosis in adolescents and young adults: implications for prevention from the Pathobiological Determinants of Atherosclerosis in Youth Study. JAMA. 1999; 281:727-735.
29. Kim DN, Schmee J, Lee KT, Thomas WA. Atherosclerotic lesions in the coronary arteries of hyperlipidemic swine, part 1: cell increases, divisions, losses and cells of origin in first 90 days on diet. Atherosclerosis. 1987;64:231-42.
30. Schwartz SM, deBlois D, O'Brien ER. The intima: soil for atherosclerosis and restenosis. Circ Res. 1995;77:445-465.
31. McCaffrey TA, Du B, Consigli S, Szabo P, Bray PJ, Hartner L, Weksler BB, Sanborn TA, Bergman G, Bush HL Jr. Genomic instability in the type II TGF-betal receptor gene in atherosclerotic and restenotic vascular cells. J Clin Invest. 1997;100:2182-2188.
32. Tabas I, Li Y, Brocia RW, Xu SW, Swenson TL, Williams KJ. Lipoprotein lipase and sphingomyelinase synergistically enhance the association of atherogenic lipoproteins with smooth muscle cells and extracellular matrix: a possible mechanism for low density lipoprotein and lipoprotein(a) retention and macrophage foam cell formation. J Biol Chem. 1993;268:20419-21432.
33. Burke AP, Weber D, Farb A, Kolodgie FD, Malcom GT, Virmani R. Coronary calcification: insights from sudden coronary death victims. Z Kardiol. In press.
34. Davies MJ, Woolf N, Rowles PM, Pepper J. Morphology of the endothelium over atherosclerotic plaques in human coronary arteries. Br Heart J. 1988;60:459-464.
35. Taylor KE, Glagov S, Zarins CK. Preservation and structural adaptation of endothelium over experimental foam cell lesions: quantitative ultrastructural study. Arteriosclerosis. 1989;9:881-894.
36. Rosenfeld ME, Tsukada T, Chait A, Bierman EL, Gown AM, Ross R. Fatty streak expansion and maturation in Watanabe Heritable Hyperlipemic and comparably hypercholesterolemic fat-fed rabbits. Arteriosclerosis. 1987;7:24-34.
37. Kolodgie FD, Virmani R, Rice HE, Mergner WJ. Vascular reactivity during the progression of atherosclerotic plaque: a study in Watanabe heritable hyperlipidemic rabbits. Circ Res. 1990;66:1112-1126.
38. Kragel AH, Reddy SG, Wittes JT, Roberts WC. Morphometric analysis of the composition of atherosclerotic plaques in the four major epicardial coronary arteries in acute myocardial infarction and in sudden coronary death. Circulation. 1989;80:1747-1756.
39. Constantinides P. Plaque fissuring in human coronary thrombosis. J Atheroscler Res. 1966;6:1-17.
40. Paterson JC. Capillary rupture with intimai hemorrhage as a causative factor in coronary thrombosis. Arch Pathol. 1938;25:474-487.
41. Junqueira LCU, Bignolas G, Brentani RR. Picrosirius staining plus polarization microscopy: a specific method for collagen detection in tissue sections. Histochem J. 1979;11:447-455.
42. Davies MJ. Stability and instability: two faces of coronary atherosclerosis: the Paul Dudley White Lecture, 1995. Circulation. 1996:94: 2013-2020.
43. Glagov S, Weisenberg E, Zarins CK, Stankunavicius R, Kolettis GJ. Compensatory enlargement of human atherosclerotic coronary arteries. N Engl J Med. 1987;316:1371-1375.
44. Clarkson TB, Prichard RW, Morgan TM, Petrick GS, Klein KP. Remodeling of coronary arteries in human and nonhuman primates. JAMA. 1994;271:289-294.
45. Mintz GS, Popma JJ, Pichard AD, Kent KM, Satler LF, Wong C, Hong MK, Kovach JA, Leon MB. Arterial remodeling after coronary angioplasty: a serial intravascular ultrasound study. Circulation. 1996;94: 35-43.
46. Sec HS, Lombardi DM, Polinsky P, Powell-Braxton L, Bunting S, Schwartz SM, Rosenfeld ME. Peripheral vascular stenosis in apolipoprotein E-deficient mice: potential roles of lipid deposition, medial atrophy, and adventitial inflammation. Arterioscler Thromb Vase Biol. 1997;17:3593-3601.
47. Thompson RW. Basic science of abdominal aortic aneurysms: emerging therapeutic strategies for an unresolved clinical problem. Curr Opin Cardiol. 1996;11:504-518.
48. Andersen HR, Maeng M, Thorwest M, Falk E. Remodeling rather than neointimal formation explains luminal narrowing after deep vessel wall injury: insights from a porcine coronary (re)stenosis model. Circulation. 1996;93:1716-1724.
49. Kakuta T, Usui M, Coats WD Jr. Currier JW, Numano F, Faxon DP. Arterial remodeling at the reference site after angioplasty in the atherosclerotic rabbit model. Arterioscler Thromb Vase Biol. 1998;18:47-51.
50. Katsumata N, Shimokawa H, Seto M, Kozai T, Yamawaki T, Kuwata K, Egashira K, Ikegaki I, Asano T, Sasaki Y, Takeshita A. Enhanced myosin light chain phosphorylations as a central mechanism for coronary artery spasm in a swine model with interleukin-1β. Circulation. 1997;96: 4357-4363.
51. Sangiorgi G, Taylor AT, Farb A, et al. Histopathology of post-percutaneous transluminal coronary angioplasty remodeling in human coronary arteries. Am Heart J. In press.
52. Courtman DW, Schwartz SM, Hart CE. Sequential injury of the rabbit abdominal aorta induces intramural coagulation and luminal narrowing independent of intimai mass: extrinsic pathway inhibition eliminates luminal narrowing. Circ Res. 1998;82:996-1006.
53. Kolpakov V, Polishchuk R, Bannykh S, Rekhter M, Solovjev P, Romanov Y, Tararak E, Antonov A, Mironov A. Atherosclerosis-prone branch regions in human aorta: microarchitecture and cell composition of intima. Atherosclerosis. 1996;122:173-189.
54. Bylock A, Bondjers G, Jansson I, Hansson HA. Surface ultrastructure of human arteries with special reference to the effects of smoking. Acta Pathol Microbiol Scand [A]. 1979;87A:201-209.
55. Pittilo RM, Bull HA, Gulati S, Rowles PM, Blow CM, Machin SJ, Woolf N. Nicotine and cigarette smoking: effects on the ultrastructure of aortic endothelium. Int J Exp Pathol. 1990;71:573-586.
56. Bennett MR, Evan GI, Schwartz SM. Apoptosis of human vascular smooth muscle cells derived from normal vessels and coronary atherosclerotic plaques. J Clin Invest. 1995;95:2266-2274.
57. Geng YJ, Henderson LE, Levesque EB, Muszynski M, Libby P. Fas is expressed in human atherosclerotic intima and promotes apoptosis of cytokine-primed human vascular smooth muscle cells. Arterioscler Thromb Vasc Biol. 1997;17:2200-2208.
58. Taylor AJ, Farb AA, Angello DA, Burwell LR, Virmani R. Proliferative activity in coronary atherectomy tissue: clinical, histopathologic, and immunohistochemical correlates. Chest. 1995;108:815-820.
59. O'Brien ER, Alpers CE, Stewart DK, Ferguson M, Tran N, Gordon D, Benditt EP, Hinohara T, Simpson JB, Schwartz SM. Proliferation in primary and restenotic coronary atherectomy tissue: implications for antiproliferative therapy. Circ Res. 1993;73:223-231.
60. Nobuyoshi M, Kimura T, Ohishi H, Horiuchi H, Nosaka H, Hamasaki N, Yokoi H, Kim K. Restenosis after percutaneous transluminal coronary angioplasty: pathologic observations in 20 patients. J Am Coll Cardiol. 1991;17:433-439.
61. Tollman MJ, Hall JL, Mann MJ, Zhang L, Gibbons GH. Inhibition of neointimal cell bcl-x expression induces apoptosis and regression of vascular disease. Nat Med. 1998;4:222-227.
62. Imanishi T, McBride J, Ho Q, O'Brien KD, Schwartz SM, Han DKM. Expression of cellular FLICE-inhibitory protein in human coronary arteries and in a rat vascular injury model. Am J Pathol. 2000;156: 125-137.
63. Henney AM, Wakeley PR, Davies MJ, Foster K, Hembry R, Murphy G, Humphries S. Localization of stromelysin gene expression in atherosclerotic plaques by in situ hybridization. Proc Natl Acad Sci U S A. 1991;88:8154-8158.
64. Libby P, Hansson GK. Involvement of the immune system in human atherogenesis: current knowledge and unanswered questions. Lab Invest. 1991;64:5-15.
65. Nicoletti A, Kaveri S, Caligiuri G, Bariety J, Hansson GK. Immunoglobulin treatment reduces atherosclerosis in apo E knockout mice. J Clin Invest. 1998;102:910-918.
66. Zhou X, Stemme S, Hansson GK. Evidence for a local immune response in atherosclerosis: CD4+ T cells infiltrate lesions of apolipoprotem-E-deficient mice. Am J Pathol. 1996;149:359-366.
67. Zhou X Paulsson G, Stemme S, Hansson GK. Hypercholesterolemia is associated with a T helper (Th) 1/TH2 switch of the autoimmune response in atherosclerotic apo E-knockout mice. J Clin Invest. 1998;101: 1717-1725.
68. Galis ZS, Sukhova GK, Libby P. Microscopic localization of active proteases by in situ zymography: detection of matrix metalloproteinase activity in vascular tissue. FASEB J. 1995;9:974-980.
69. Sukhova GK, Shi GP, Simon DI, Chapman HA, Libby P. Expression of the elastolytic cathepsins S and K in human atheroma and regulation of their production in smooth muscle cells. J Clin Invest. 1998;102: 576-583.
70. Sukhova GK, Schonbeck U, Rabkin E, Schoen FJ, Poole AR, Billinghurst RC, Libby P. Evidence for increased collagenolysis by interstitial collagenases-1 and -3 in vulnerable human atheromatous plaques. Circulation. 1999;99:2503-2509.
71. Schonbeck U, Mach F, Sukhova GK, Atkinson E, Levesque E, Herman M, Graber P Basset P, Libby P. Expression of stromelysm-3 in atherosclerotic lesions: regulation via CD40-CD40 ligand signaling in vitro and in vivo. J Exp Med. 1999;189:843-853.
72. Desrochers PE, Mookhtiar K, Van Wart HE, Hasty KA, Weiss SJ. Proteolytic inactivation of αl-proteinase inhibitor and al-antichymotrypsin by oxidatively activated human neutrophil metalloproteinases. J Biol Chem. 1992;267:5005-5012.
73. Hazen SL, Hsu FF, Gaut JP, Crowley JR, Heinecke JW. Modification of proteins and lipids by myeloperoxidase. Methods Enzymol. 1999;300: 88-105.
74. Nemerson Y, Esnouf MP. Activation of a proteolytic system by a membrane lipoprotein: mechanism of action of tissue factor. Proc Natl Acad Sci U S A. 1973;70:310-314.
75. Wilcox JN, Smith KM, Schwartz SM, Gordon D. Localization of tissue factor in the normal vessel wall and in the atherosclerotic plaque. Proc Natl Acad Sci U S A. 1989;86:2839-2843.