Roles of infectious agents in atherosclerosis and restenosis: An assessment of the evidence and need for future research

Circulation

Volumn 96, Issue 11, 1997, Pages 4095-4103

  Libby, Peter ^a   Egan, Debra ^b   Skarlatos, Sonia ^b  

^a BRIGHAM AND WOMEN S HOSPITAL   (United States)

^b NATIONAL HEART LUNG AND BLOOD INSTITUTE   (United States)

Author keywords

Endothelium; Leukocytes; Muscle smooth; Risk factors viruses

Indexed keywords

ATHEROGENESIS; ATHEROSCLEROSIS; CHLAMYDOPHILA PNEUMONIAE; CORONARY ARTERY DISEASE; CYTOMEGALOVIRUS; ENDOTHELIUM CELL; ENDOTOXEMIA; HERPES VIRUS; HOST SUSCEPTIBILITY; HUMAN; INFECTION; NONHUMAN; PRIORITY JOURNAL; RESTENOSIS; REVIEW; SEROEPIDEMIOLOGY; VASCULAR SMOOTH MUSCLE;

EID: 0030699298     PISSN: 00097322     EISSN: None     Source Type: Journal    
DOI: 10.1161/01.CIR.96.11.4095     Document Type: Review

References (91)

1. Melnick JL, Adam E, DeBakey ME. Possible role of cytomegalovirus in alherogenesis. JAMA. 1990;263:2204-2207.
2. Melnick JL, Adam E, Debakey ME. Cytomegalovirus and atherosclerosis. Eur Heart J. 1993;14:30-38.
3. Heiss G, Sharrett AR, Barnes R, Chambless LE, Szklo M, Alzola C. Carotid atherosclerosis measured by B-mode ultrasound in populations: associations with cardiovascular risk factors in the ARIC study. Am J Epidemiol. 1991;134:250-256.
4. Nieto FJ, Adam E, Sorlie P, Farzadegan H, Melnick JL, Comstock GW, Szklo M. Cohort study of cytomegalovirus infection as a risk factor for carotid intimal-medial thickening, a measure of subclinical atherosclerosis. Circulation. 1996;94:922-927. See comments.
5. Zhou YF, Leon MB, Waclawiw MA, Popma JJ, Yu ZX, Finkel T, Epstein SE. Association between prior cytomegalovirus infection and the risk of restenosis after coronary atherectomy. N Engl J Med. 1996;335:624-630.
6. Grattan MT, Moreno-Cabral CE, Starnes VA, Oyer PE, Stinson EB, Shumway NE. Cytomegalovirus infection is associated with cardiac allograft rejection and atherosclerosis. JAMA. 1989;261:3561-3566.
7. Pahl E, Fricker FJ, Armitage J, Griffith BP, Taylor S, Uretsky BF, Beerman LB, Zuberbuhler JR. Coronary arteriosclerosis in pediatric heart transplant survivors: limitation of long-term survival. J Pediatr. 1990;116:177-183.
8. Loebe M, Schuler S, Zais O, Warnecke H, Fleck E, Hetzer R. Role of cytomegalovirus infection in the development of coronary artery disease in the transplanted heart. J Heart Transplant. 1990;9:707-711.
9. Everett JP, Hershberger RE, Norman DJ, Chou S, Ratkovec RM, Cobanoglu A, Ott GY, Hosenpud JD. Prolonged cytomegalovirus infection with viremia is associated with development of cardiac allograft vasculopathy. J Heart Lung Transplant. 1992;11:S133-S137.
10. Dummer S, Lee A, Breinig MK, Kormos R, Ho M, Griffith B. Investigation of cytomegalovirus infection as a risk factor for coronary atherosclerosis in the explanted hearts of patients undergoing heart transplantation. J Med Virol. 1994;44:305-309.
11. Saikku P, Leinonen M, Mattila K, Ekman MR, Nieminen MS, Makela PH, Huttunen JK, Valtonen V. Serological evidence of an association of a novel Chlamydia, TWAR, with chronic coronary heart disease and acute myocardial infarction. Lancet. 1988;2:983-986.
12. Saikku P, Leinonen M, Tenkanen L, Linnanmaki E, Ekman MR, Manninen V, Manttari M, Frick MH, Huttunen JK. Chronic Chlamydia pneumoniae infection as a risk factor for coronary heart disease in the Helsinki Heart Study. Ann Intern Med. 1992;116:273-278. See comments.
13. Thom DH, Wang SP, Grayston JT, Siscovick DS, Stewart DK, Kronmal RA, Weiss NS. Chlamydia pneumoniae strain TWAR antibody and angiographically demonstrated coronary artery disease. Arterioscler Thromb. 1991;11:547-551.
14. Thom DH, Grayston JT, Siscovick DS, Wang SP, Weiss NS, Daling JR. Association of prior infection with Chlamydia pneumoniae and angiographically demonstrated coronary artery disease. JAMA. 1992;268:68-72.
15. Hahn DL, Golubjatnikov R. Smoking is a potential confounder of the Chlamydia pneumoniae-coronary artery disease association. Arterioscler Thromb. 1992;12:945-947.
16. Galloway DA, McDougall JK. The oncogenic potential of herpes simplex viruses: evidence for a 'hit-and-run' mechanism. Nature. 1983;302:21-24.
17. Benditt EP, Barrett T, McDougall JK. Viruses in the etiology of atherosclerosis. Proc Natl Acad Sci U S A. 1983;80:6386-6389.
18. Hendrix MG, Salimans MM, van Boven CP, Bruggeman CA. High prevalence of latently present cytomegalovirus in arterial walls of patients suffering from grade III atherosclerosis. Am. J Pathol. 1990;136:23-28.
19. Wu TC, Hruban RH, Ambinder RF, Pizzorno M, Cameron DE, Baumgartner WA, Reitz BA, Hayward GS, Hutchins GM. Demonstration of cytomegalovirus nucleic acids in the coronary arteries of transplanted hearts. Am J Pathol. 1992;140:739-747.
20. Kol A, Sperti G, Shani J, Schulhoff N, van de Greef W, Landini MP, La Placa M, Maseri A, Crea F, Cytomegalovirus replication is not a cause of instability in unstable angina. Circulation. 1995;91:1910-1913.
21. Hendrix MG, Dormans PH, Kitslaar P, Bosman F, Bruggeman CA. The presence of cytomegalovirus nucleic acids in arterial walls of atherosclerotic and nonatherosclerotic patients. Am J Pathol. 1989;134:1151-1157.
22. Hendrix MG, Daumen M, Bruggeman CA. Cytomegalovirus nucleic acid distribution within the human vascular tree. Am J Pathol. 1991;138:563-567.
23. Grayston JT, Kuo CC, Camphell LA, Benditt EP. Chlamydia pneumoniae, strain TWAR and atherosclerosis. Eur Heart J. 1993;14:66-71.
24. Jackson LA, Campbell LA, Schmidt RA, Kuo C-C, Cappuccio AL, Lee MJ, Grayston JT. Specificity of detection of Chlamydia pneumoniae in cardiovascular atheroma: evaluation of the innocent bystander hypothesis. Am J Pathol. 1997;150:1785-1790.
25. Kuo CC, Shor A, Campbell LA, Fukushi H, Patton DL, Grayston JT. Demonstration of Chlamydia pneumoniae in atherosclerotic lesions of coronary arteries. J Infect Dis. 1993;167:841-849.
26. Kuo CC, Gown AM, Benditt EP, Grayston JT. Detection of Chlamydia pneumoniae in aortic lesions of atherosclerosis by immunocytochemical stain. Arterioscler Thromb. 1993;13:1501-1504.
27. Kuo CC, Grayston JT, Campbell LA, Goo YA, Wissler RW, Benditt EP. Chlamydia pneumoniae (TWAR) in coronary arteries of young adults (15-34 years old). Proc Natal Acad Sci U S A. 1995;92:6911-6914.
28. Grayston JT, Kuo CC, Coulson AS, Campbell LA, Lawrence RD, Lee MJ, Strandness ED, Wang SP. Chlamydia pneumoniae (TWAR) in atherosclerosis of the carotid artery. Circulation. 1995;92:3397-3400. See comments.
29. Muhlestein JB, Hammond EH, Carlquist JF, Radicke E, Thomson MJ, Karagounis LA, Woods ML, Anderson JL. Increased incidence of Chlamydia species within the coronary arteries of patients with symptomatic atherosclerotic versus other forms of cardiovascular disease. J Am Coll Cardiol. 1996;27:1555-1561.
30. Weiss SM, Roblin PM, Gaydos CA, Cummings P, Patton DL, Schulhoff N, Shani J, Frankel R, Penney K, Quinn TC, Hammerschlag MR, Schachter J. Failure to detect Chlamydia pneumoniae in coronary atheromas of patients undergoing atherectomy. J Infect Dis. 1996;173:957-962.
31. Cook PJ, Lip GY. Infectious agents and atherosclerotic vascular disease. Q J Med. 1996;89:727-735.
32. Minick CR, Fabricant CG, Fabricant J, Litrenta MM. Atheroarteriosclerosis induced by infection with a herpesvirus. Am J Pathol. 1979;96:673-706.
33. Pyrzak R, Shih JC. Detection of specific DNA segments of Marek's disease herpes virus in Japanese quail susceptible to atherosclerosis. Atherosclerosis. 1987;68:77-85.
34. Shih JC, Pyrzak R, Guy JS. Discovery of noninfectious viral genes complementary to Marek's disease herpes virus in quail susceptible to cholesterol-induced atherosclerosis. J Nutr. 1989;119:294-298.
35. Lemstrom K, Koskinen P, Krogerus L, Daemen M, Bruggeman C, Hayry P. Cytomegalovirus antigen expression, endothelial cell proliferation, and intimal thickening in rat cardiac allografts after cytomegalovirus infection. Circulation. 1995;92:2594-2604.
36. Koskinen P, Lemstrom K, Bruggeman C, Lautenschlager I, Hayry P. Acute cytomegalovirus infection induces a subendothelial inflammation (endothelialitis) in the allograft vascular wall: a possible linkage with enhanced allograft arteriosclerosis. Am J Pathol. 1994;144:41-50.
37. Moazed TC, Kuo C, Patton DL, Grayston JT, Campbell LA. Experimental rabbit models of Chlamydia pneumoniae infection. Am J Pathol. 1996;148:667-676.
38. Moazed TC, Kuo C, Grayston JT, Campbell LA. Murine models of Chlamydia pneumoniae infection and atherosclerosis. J Infect Dis. 1997;175:883-890.
39. Hajjar DP, Pomerantz KB, Falcone DJ, Weksler BB, Grant AJ. Herpes simplex virus infection in human arterial cells: implications in arteriosclerosis. J Clin Invest. 1987;80:1317-1321.
40. Ho DD, Rota TR, Hirsch MS. Infection of human endothelial cells by human T-lymphotropic virus type I. Proc Natl Acad Sci U S A. 1984;81:7588-7590.
41. Van Dam-Mieras MC, Bruggeman CA, Muller AD, Debie WH, Zwaal RF. Induction of endothelial cell procoagulant activity by cytomegalovirus infection. Thromb Res. 1987;47:69-75.
42. Span AH, Frederik PM, Grauls G, Van Boven GP, Bruggeman CA. CMV induced vascular injury: an electron-microscopic study in the rat. In Vivo. 1993;7:567-573.
43. Steinhoff G, You XM, Steinmuller C, Boeke K, Stals FS, Bruggeman CA, Haverich A. Induction of endothelial adhesion molecules by rat cytomegalovirus in allogeneic lung transplantation in the rat. Scand J Infect Dis. 1995;99(suppl):58-60.
44. Gaydos CA, Summersgill JT, Sahney NN, Ramirez JA, Quinn TC. Replication of Chlamydia pneumoniae in vitro in human macrophages, endothelial cells, and aortic artery smooth muscle cells. Infect Immun. 1996;64:1614-1620.
45. Beatty WL, Byrne GI, Morrison RP. Morphologic and antigenic characterization of Interferon gamma-mediated persistent Chlamydia trachomatis infection in vitro. Proc Natl Acad U S A. 1993;90:3998-4002.
46. Beatty WL, Byrne GI, Morrison RP. Repeated and persistent infection with Chlamydia and the development of chronic inflammation and disease. Trends Microbiol. 1994;2:94-98. See comments.
47. Beatty WL, Morrison RP, Byrne GI. Persistent chlamydiae: from cell culture to a paradigm for chlamydial pathogenesis. Microbiol Rev. 1994;58:686-699.
48. Visser MR, Tracy PB, Vercellotti GM, Goodman JL, White JG, Jacob HS. Enhanced thrombin generation and platelet binding on herpes simplex virus-infected endothelium. Proc Natl Acad U S A. 1988;85:8227-8230.
49. Etingin OR, Silverstein RL, Friedman HM, Hajjar DP. Viral activation of the coagulation cascade: molecular interactions at the surface of infected endothelial cells. Cell. 1990;61:657-662.
50. Bok RA, Jacob HS, Balla J, Juckett M, Stella T, Shatos MA, Vercellotti GM. Herpes simplex virus decreases endothelial cell plasminogen activator inhibitor. Thramb Haemost. 1993;69:253-258.
51. Visser MR, Vercellotti GM. Herpes simplex virus and atherosclerosis. Eur Heart J. 1993;14:39-42.
52. Kaner RJ, Baird A, Mansukhani A, Basilico C, Summers BD, Florkiewicz RZ, Hajjar DP. Fibroblast growth factor receptor is a portal of cellular entry for herpes simplex virus type 1. Science. 1990;248:1410-1413. See comments.
53. Key NS, Vercellotti GM, Winkelmann JC, Moldow CF, Goodman JL, Esmon NL, Esmon CT, Jacob HS. Infection of vascular endothelial cells with herpes simplex virus enhances tissue factor activity and reduces thrombomodulin expression. Proc Natl Acad U S A. 1990;87:7095-7099.
54. Key NS, Bach RR, Vercellotti GM, Moldow CF. Herpes simplex virus type I does not require productive infection to induce tissue factor in human umbilical vein endothelial cells. Lab Invest. 1993;68:645-651.
55. van Dam-Mieras MC, Muller AD, van Hinsbergh VW, Mullers WJ, Bomans PH, Bruggeman CA. The procoagulant response of cytomegalovirus infected endothelial cells. Thromb Haemost. 1992;68:364-370.
56. Vercellotti GM. Proinflammatory and procoagulant effects of herpes simplex infection on human endothelium. Blood Cells. 1990;16:209-215.
57. Benditt EP, Benditt JM. Evidence for a monoclonal origin of human atherosclerotic plaques. Proc Natl Acad U S A. 1973;70:1753-1756.
58. Benditt EP. Implications of the monoclonal character of human atherosclerotic plaques. Am J Pathol. 1977;86:693-702.
59. Nachtigal M, Legrand A, Greenspan P, Nachtigal SA, Nagpal ML. Immortalization of rabbit vascular smooth muscle cells after transfection with a fragment of the BglII N region of herpes simplex virus type 2 DNA. Intervirology. 1990;31:166-174.
60. Speir E, Modali R, Huang ES, Leon MB, Shawl F, Finkel T, Epstein SE. Potential role of human cytomegalovirus and p53 interaction in coronary restenosis. Science. 1994;265:391-394.
61. Kovacs A, Weber M, Burns L, Jacob H, Vercellotti G. Cytoplasmic sequestration of p53 in cytomegalovirus-infected human endothelial cells. Am J Pathol. 1996;149:1531-1539.
62. Hajjar DP, Fabricant CG, Minick CR, Fabricant J. Virus-induced atherosclerosis. Herpesvirus infection alters aortic cholesterol metabolism and accumulation. Am J Pathol. 1986;122:62-70.
63. Hajjar DP. Warner-Lambert/Parke-Davis Award Lecture. Viral pathogenesis of atherosclerosis: impact of molecular mimicry and viral genes. Am J Pathol. 1991;139:1195-1211.
64. Libby P. Vascular Cells Produce and Respond to Cytokines. In: Hansson GK, Libby P, eds. Immune Functions of the Vessel Wall. Amsterdam, Netherlands: Harwood Academic Publishers; 1996:45-64.
65. Dudding L, Haskill S, Clark BD, Auron PE, Sporn S, Huang ES. Cytomegalovirus infection stimulates expression of monocyte-associated mediator genes. J Immunol. 1989;143:3343-3352.
66. Gosselin J, Flamand L, D'Addario M, Hiscott J, Menezes J. Infection of peripheral blood mononuclear cells by herpes simplex and Epstein-Barr viruses: differential induction of interleukin 6 and tumor necrosis factor-alpha. J Clin Invest. 1992;89:1849-1856.
67. Smith PD, Saini SS, Raffeld M, Manischewitz JF, Wahl SM. Cytomegalovirus induction of tumor necrosis factor-alpha by human monocytes and mucosal macrophages. J Clin Invest. 1992;90:1642-1648.
68. Almeida GD, Porada CD, St Jeor S, Ascensao JL, Human cytomegalovirus alters interleukin-6 production by endothelial cells. Blood. 1994;83:370-376.
69. Libby P, Ordovàs JM, Auger KR, Robbins H, Birinyi LK, Dinarello CA. Endotoxin and tumor necrosis factor induce interleukin-1 gene expression in adult human vascular endothelial cells. Am J Pathol. 1936;124:179-186.
70. Libby P, Ordovas JM, Birinyi LK, Auger KR, Dinarello CA. Inducible interleukin-1 expression in human vascular smooth muscle cells. J Clin Invest. 1986;78:1432-1438.
71. Warner SJC, Libby P. Human vascular smooth muscle cells: target for and source of tumor necrosis factor. J Immunol. 1989;142:100-109.
72. Loppnow H, Libby P, Freudenberg M, Krauss JH, Weckesser J, Mayer H. Cytokine induction by lipopolysaccharide (LPS) corresponds to lethal toxicity and is inhibited by non toxic Rhodobacter capsulatus LPS. Infect Immun. 1990;58:3743-3750.
73. Sedmak DD, Knight DA, Vook NC, Waldman JW. Divergent patterns of ELAM-1, ICAM-1, and VCAM-1 expression on cytomegalovirus-infected endothelial cells. Transplantation. 1994;58:1379-1385.
74. Etingin OR, Silverstein RL, Hajjar DP. Identification of a monocyte receptor on herpesvirus-infected endothelial cells. Proc Natl Acad U S A. 1991;88:7200-7203.
75. Van Lenten B, Hama SY, de Beer F, Stafforini DM, McIntyre TM, Prescott SM, La Du B, Fogelman AM, Navab M. Anti-inflammatory HDL becomes pro-inflammatory during the acute phase response: loss of protective effect of HDL against LDL oxidation in aortic wall cell cocultures. J Clin Invest. 1995;96:2758-2767.
76. Pesonen E, Rapola J, Viikari J, Turtinen J, Akerblom HK. Altered serum lipid profile after systemic infection in children: risk factor for CHD? Eur Heart J. 1993;14:7-11.
77. Nieminen MS, Manila K, Valtonen V. Infection and inflammation as risk factors for myocardial infarction. Eur Heart J. 1993;14:12-16.
78. Davies MJ, Thomas AC. Plaque fissuring: the cause of acute myocardial infarction, sudden ischemic death, and crescendo angina. Br Heart J. 1985;53:363-373.
79. Libby P, Loppnow H, Girard J. The Roles of Endothelial Cells in Septic Shock. In: Beaufils F, Mercier JC. eds. Chocs septiques en Pediatric. Paris, France: Arnette; 1989:25-32.
80. Parrillo JE, Parker MM, Natanson C, Suffredini AF, Danner RL, Cunnion RE, Ognibene FP. Septic shock in humans: advances in the understanding of pathogenesis, cardiovascular dysfunction, and therapy. Ann Intern Med. 1990;113:227-242.
81. Fleet JC, Clinton SK, Salomon RN, Loppnow H, Libby P. Atherogenic diets enhance endotoxin-stimulated interleukin-1 and tumor necrosis factor gene expression in rabbit aortae. J Nutr. 1992;122:294-305.
82. Libby P. Do vascular wall cytokines promote atherogenesis? Hosp Pract. 1992;27:51-58.
83. Brusehke AV, Kramer J Jr, Bal ET, Haque IU, Detrano RC, Goormastic M. The dynamics of progression of coronary atherosclerosis studied in 168 medically treated patients who underwent coronary arteriography three times. Am Heart J. 1989;117:296-305. See comments.
84. Buja LM. Does atherosclerosis have an infectious etiology? Circulation. 1996;94:872-873.
85. Marshall BJ. Helicobacter pylori in peptic ulcer: have Koch's postulates been fulfilled? Ann Med. 1995;27:565-568.
86. Fredericks DN, Relman DA. Sequence-based identification of microbial pathogens: a reconsideration of Koch's postulates. Clin Microbiol Rev. 1996;9:18-33.
87. Hardwicke MA, Schaffer PA. Differential effects of nerve growth factor and dexamelhasone on herpes simplex virus type 1 oriL- and oriS-dependent DNA replication in PC12 cells. Journal of Virology. 1997;71:3580-3587.
88. Capron L. Chiamydia in coronary plaques: hidden culprit or harmless hobo? Nat Med. 1996;2:856-857
89. Danesh J, Collins R, Peto R. Chronic infections and coronary heart disease: is there a link? Lancet. 1997;350:430-436.
90. Gupta S, Leatham EW, Carrington D, Mendall MA, Kaski JC, Camot AJ. Elevated Chlamydia pneumoniae antibodies, cardiovascular events, and azithromycin in male survivors of myocardial infarction. Circulation. 1997;96:404-407.
91. Gurfinkel E, Bozovich G, Daroca A, Beck E, Mautner B, for the ROXIS Study Group. Randomised trial of roxithromycin in non-Q-wave coronary syndromes: ROXIS pilot study. Lancet. 1997;350:404-407.