Arteriosclerosis, Thrombosis, and Vascular Biology. 1995;15:1512-1531
© 1995 American Heart Association, Inc.
Articles |
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
Abstract This report is the continuation of two earlier reports that defined human arterial intima and precursors of advanced atherosclerotic lesions in humans. This report describes the characteristic components and pathogenic mechanisms of the various advanced atherosclerotic lesions. These, with the earlier definitions of precursor lesions, led to the histological classification of human atherosclerotic lesions found in the second part of this report. The Committee on Vascular Lesions also attempted to correlate the appearance of lesions noted in clinical imaging studies with histological lesion types and corresponding clinical syndromes. In the histological classification, lesions are designated by Roman numerals, which indicate the usual sequence of lesion progression. The initial (type I) lesion contains enough atherogenic lipoprotein to elicit an increase in macrophages and formation of scattered macrophage foam cells. As in subsequent lesion types, the changes are more marked in locations of arteries with adaptive intimal thickening. (Adaptive thickenings, which are present at constant locations in everyone from birth, do not obstruct the lumen and represent adaptations to local mechanical forces). Type II lesions consist primarily of layers of macrophage foam cells and lipid-laden smooth muscle cells and include lesions grossly designated as fatty streaks. Type III is the intermediate stage between type II and type IV (atheroma, a lesion that is potentially symptom-producing). In addition to the lipid-laden cells of type II, type III lesions contain scattered collections of extracellular lipid droplets and particles that disrupt the coherence of some intimal smooth muscle cells. This extracellular lipid is the immediate precursor of the larger, confluent, and more disruptive core of extracellular lipid that characterizes type IV lesions. Beginning around the fourth decade of life, lesions that usually have a lipid core may also contain thick layers of fibrous connective tissue (type V lesion) and/or fissure, hematoma, and thrombus (type VI lesion). Some type V lesions are largely calcified (type Vb), and some consist mainly of fibrous connective tissue and little or no accumulated lipid or calcium (type Vc).
Key Words: atherosclerosis • lesion • AHA Medical/Scientific Statements
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U. J. Schoepf, C. R. Becker, B. M. Ohnesorge, and E. K. Yucel CT of Coronary Artery Disease Radiology, July 1, 2004; 232(1): 18 - 37. [Abstract] [Full Text] [PDF]
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J. Golledge, M. McCann, S. Mangan, A. Lam, and M. Karan Osteoprotegerin and Osteopontin Are Expressed at High Concentrations Within Symptomatic Carotid Atherosclerosis Stroke, July 1, 2004; 35(7): 1636 - 1641. [Abstract] [Full Text] [PDF]
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 S. Bro, F. Moeller, C. B. Andersen, K. Olgaard, and L. B. Nielsen Increased Expression of Adhesion Molecules in Uremic Atherosclerosis in Apolipoprotein-E-Deficient Mice J. Am. Soc. Nephrol., June 1, 2004; 15(6): 1495 - 1503. [Abstract] [Full Text] [PDF]
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N. Stadler, R. A. Lindner, and M. J. Davies Direct Detection and Quantification of Transition Metal Ions in Human Atherosclerotic Plaques: Evidence for the Presence of Elevated Levels of Iron and Copper Arterioscler Thromb Vasc Biol, May 1, 2004; 24(5): 949 - 954. [Abstract] [Full Text]
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 A. M. Troen, E. Lutgens, D. E. Smith, I. H. Rosenberg, and J. Selhub The atherogenic effect of excess methionine intake PNAS, December 9, 2003; 100(25): 15089 - 15094. [Abstract] [Full Text] [PDF]
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T. T. Tuomisto, A. Korkeela, J. Rutanen, H. Viita, J. H. Brasen, M. S. Riekkinen, T. T. Rissanen, K. Karkola, Z. Kiraly, K. Kolble, et al. Gene Expression in Macrophage-Rich Inflammatory Cell Infiltrates in Human Atherosclerotic Lesions as Studied by Laser Microdissection and DNA Array: Overexpression of HMG-CoA Reductase, Colony Stimulating Factor Receptors, CD11A/CD18 Integrins, and Interleukin Receptors Arterioscler Thromb Vasc Biol, December 1, 2003; 23(12): 2235 - 2240. [Abstract] [Full Text] [PDF]
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D. de Kleijn and G. Pasterkamp Toll-like receptors in cardiovascular diseases Cardiovasc Res, October 15, 2003; 60(1): 58 - 67. [Abstract] [Full Text] [PDF]
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E. K. Arkenbout, M. van Bragt, E. Eldering, C. van Bree, J. M. Grimbergen, P. H.A. Quax, H. Pannekoek, and C. J.M. de Vries TR3 Orphan Receptor Is Expressed in Vascular Endothelial Cells and Mediates Cell Cycle Arrest Arterioscler Thromb Vasc Biol, September 1, 2003; 23(9): 1535 - 1540. [Abstract] [Full Text] [PDF]
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T. Q. Nhan, W. C. Liles, A. Chait, J. T. Fallon, and S. M. Schwartz The p17 Cleaved Form of Caspase-3 Is Present Within Viable Macrophages In Vitro and in Atherosclerotic Plaque Arterioscler Thromb Vasc Biol, July 1, 2003; 23(7): 1276 - 1282. [Abstract] [Full Text] [PDF]
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R. E. Murphy, A. R. Moody, P. S. Morgan, A. L. Martel, G.S. Delay, S. Allder, S. T. MacSweeney, W. G. Tennant, J. Gladman, J. Lowe, et al. Prevalence of Complicated Carotid Atheroma as Detected by Magnetic Resonance Direct Thrombus Imaging in Patients With Suspected Carotid Artery Stenosis and Previous Acute Cerebral Ischemia Circulation, June 24, 2003; 107(24): 3053 - 3058. [Abstract] [Full Text] [PDF]
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L. M. Belalcazar, A. Merched, B. Carr, K. Oka, K.-H. Chen, L. Pastore, A. Beaudet, and L. Chan Long-Term Stable Expression of Human Apolipoprotein A-I Mediated by Helper-Dependent Adenovirus Gene Transfer Inhibits Atherosclerosis Progression and Remodels Atherosclerotic Plaques in a Mouse Model of Familial Hypercholesterolemia Circulation, June 3, 2003; 107(21): 2726 - 2732. [Abstract] [Full Text] [PDF]
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M.E. Kooi, V.C. Cappendijk, K.B.J.M. Cleutjens, A.G.H. Kessels, P.J.E.H.M. Kitslaar, M. Borgers, P.M. Frederik, M.J.A.P. Daemen, and J.M.A. van Engelshoven Accumulation of Ultrasmall Superparamagnetic Particles of Iron Oxide in Human Atherosclerotic Plaques Can Be Detected by In Vivo Magnetic Resonance Imaging Circulation, May 20, 2003; 107(19): 2453 - 2458. [Abstract] [Full Text] [PDF]
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V. de Waard, T. A.E. van Achterberg, N. J. Beauchamp, H. Pannekoek, and C. J.M. de Vries Cardiac Ankyrin Repeat Protein (CARP) Expression in Human and Murine Atherosclerotic Lesions: Activin Induces Carp in Smooth Muscle Cells Arterioscler Thromb Vasc Biol, January 1, 2003; 23(1): 64 - 68. [Abstract] [Full Text] [PDF]
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S. de Jongh, M. R. Lilien, J. op't Roodt, E. S. G. Stroes, H. D. Bakker, and J. J. P. Kastelein Early statin therapy restores endothelial function in children with familial hypercholesterolemia J. Am. Coll. Cardiol., December 18, 2002; 40(12): 2117 - 2121. [Abstract] [Full Text] [PDF]
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T. Naruko, M. Ueda, K. Haze, A. C. van der Wal, C. M. van der Loos, A. Itoh, R. Komatsu, Y. Ikura, M. Ogami, Y. Shimada, et al. Neutrophil Infiltration of Culprit Lesions in Acute Coronary Syndromes Circulation, December 3, 2002; 106(23): 2894 - 2900. [Abstract] [Full Text] [PDF]
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 M. Sandrock, D.-C. Cheng, D. Schmitz, and A. Schmidt-Trucksass Quantification of the Wall Inhomogeneity in B-mode Sonographic Images of the Carotid Artery J. Ultrasound Med., December 1, 2002; 21(12): 1395 - 1404. [Abstract] [Full Text] [PDF]
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H. Sun, H. Unoki, X. Wang, J. Liang, T. Ichikawa, Y. Arai, M. Shiomi, S. M. Marcovina, T. Watanabe, and J. Fan Lipoprotein(a) Enhances Advanced Atherosclerosis and Vascular Calcification in WHHL Transgenic Rabbits Expressing Human Apolipoprotein(a) J. Biol. Chem., November 27, 2002; 277(49): 47486 - 47492. [Abstract] [Full Text] [PDF]
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N. Kataoka, K. Iwaki, K. Hashimoto, S. Mochizuki, Y. Ogasawara, M. Sato, K. Tsujioka, and F. Kajiya Measurements of endothelial cell-to-cell and cell-to-substrate gaps and micromechanical properties of endothelial cells during monocyte adhesion PNAS, November 26, 2002; 99(24): 15638 - 15643. [Abstract] [Full Text] [PDF]
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C. R. Kiefer, J. B. McKenney, J. F. Trainor, and L. M. Snyder Maturation-Dependent Acquired Coronary Structural Alterations and Atherogenesis in the Dahl Sodium-Sensitive Hypertensive Rat Circulation, November 5, 2002; 106(19): 2486 - 2490. [Abstract] [Full Text] [PDF]
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 C. Kluft, R. Kleemann, and M.P.M. de Maat How best to counteract the enemies? By controlling inflammation in the coronary circulation Eur. Heart J. Suppl., November 1, 2002; 4(suppl_G): G53 - G65. [Abstract] [PDF]
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R Ezzahiri, H.J.M.G Nelissen-Vrancken, H.A.J.M Kurvers, F.R.M Stassen, I Vliegen, G.E.L.M Grauls, M.M.L van Pul, P.J.E.H.M Kitslaar, and C.A Bruggeman Chlamydophila pneumoniae (Chlamydia pneumoniae) accelerates the formation of complex atherosclerotic lesions in Apo E3-Leiden mice Cardiovasc Res, November 1, 2002; 56(2): 269 - 276. [Abstract] [Full Text] [PDF]
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J.H.P. Lardenoye, M.R. de Vries, C.W.G.M. Lowik, Q. Xu, C.R. Dhore, J.P.M. Cleutjens, V.W.M. van Hinsbergh, J.H. van Bockel, and P.H.A. Quax Accelerated Atherosclerosis and Calcification in Vein Grafts: A Study in APOE*3 Leiden Transgenic Mice Circ. Res., October 4, 2002; 91(7): 577 - 584. [Abstract] [Full Text] [PDF]
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E. K. Arkenbout, V. de Waard, M. van Bragt, T. A.E. van Achterberg, J. M. Grimbergen, B. Pichon, H. Pannekoek, and C. J.M. de Vries Protective Function of Transcription Factor TR3 Orphan Receptor in Atherogenesis: Decreased Lesion Formation in Carotid Artery Ligation Model in TR3 Transgenic Mice Circulation, September 17, 2002; 106(12): 1530 - 1535. [Abstract] [Full Text] [PDF]
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P.J. Gallagher More histological information in acute coronary death Eur. Heart J., September 2, 2002; 23(18): 1406 - 1408. [Full Text] [PDF]
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G. Marsche, A. Hammer, O. Oskolkova, K. F. Kozarsky, W. Sattler, and E. Malle Hypochlorite-modified High Density Lipoprotein, a High Affinity Ligand to Scavenger Receptor Class B, Type I, Impairs High Density Lipoprotein-dependent Selective Lipid Uptake and Reverse Cholesterol Transport J. Biol. Chem., August 23, 2002; 277(35): 32172 - 32179. [Abstract] [Full Text] [PDF]
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H. C. McGill Jr, C. A. McMahan, E. E. Herderick, A. W. Zieske, G. T. Malcom, R. E. Tracy, J. P. Strong, and for the Pathobiological Determinants of Atheroscle Obesity Accelerates the Progression of Coronary Atherosclerosis in Young Men Circulation, June 11, 2002; 105(23): 2712 - 2718. [Abstract] [Full Text] [PDF]
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M. Van Eck, I. S. T. Bos, W. E. Kaminski, E. Orso, G. Rothe, J. Twisk, A. Bottcher, E. S. Van Amersfoort, T. A. Christiansen-Weber, W.-P. Fung-Leung, et al. Leukocyte ABCA1 controls susceptibility to atherosclerosis and macrophage recruitment into tissues PNAS, April 30, 2002; 99(9): 6298 - 6303. [Abstract] [Full Text] [PDF]
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K. Edfeldt, J. Swedenborg, G. K. Hansson, and Z.-q. Yan Expression of Toll-Like Receptors in Human Atherosclerotic Lesions: A Possible Pathway for Plaque Activation Circulation, March 12, 2002; 105(10): 1158 - 1161. [Abstract] [Full Text] [PDF]
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A. C. Terentis, S. R. Thomas, J. A. Burr, D. C. Liebler, and R. Stocker Vitamin E Oxidation in Human Atherosclerotic Lesions Circ. Res., February 22, 2002; 90(3): 333 - 339. [Abstract] [Full Text] [PDF]
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J. T.B. Crawley, D. A. Goulding, V. Ferreira, N. J. Severs, and F. Lupu Expression and Localization of Tissue Factor Pathway Inhibitor-2 in Normal and Atherosclerotic Human Vessels Arterioscler Thromb Vasc Biol, February 1, 2002; 22(2): 218 - 224. [Abstract] [Full Text] [PDF]
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J. M. Upston, X. Niu, A. J. Brown, R. Mashima, H. Wang, R. Senthilmohan, A. J. Kettle, R. T. Dean, and R. Stocker Disease Stage-Dependent Accumulation of Lipid and Protein Oxidation Products in Human Atherosclerosis Am. J. Pathol., February 1, 2002; 160(2): 701 - 710. [Abstract] [Full Text] [PDF]
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A. P. Burke, F. D. Kolodgie, A. Farb, D. Weber, and R. Virmani Morphological Predictors of Arterial Remodeling in Coronary Atherosclerosis Circulation, January 22, 2002; 105(3): 297 - 303. [Abstract] [Full Text] [PDF]
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P. M. McCabe, J. A. Gonzales, J. Zaias, A. Szeto, M. Kumar, A. J. Herron, and N. Schneiderman Social Environment Influences the Progression of Atherosclerosis in the Watanabe Heritable Hyperlipidemic Rabbit Circulation, January 22, 2002; 105(3): 354 - 359. [Abstract] [Full Text] [PDF]
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