The Possible Role of Herpesviruses in the Pathogenesis of Coronary Atherosclerosis

Julia A. Kotova, Veronika I. Shevzova, Anna A. Zuikova, Olga N. Krasnorutskaya, Natalia V. Strahova, Elena Yu. Esina

 
International Journal of Biomedicine. 2021;11(4):391-396.
DOI: 10.21103/Article11(4)_RA1
Originally published December 10, 2021

Abstract: 

Cardiovascular diseases are still the dominant cause of death worldwide. Coronary artery disease (CAD) is the most common type of heart disease and the leading cause of death for both men and women. Coronary atherosclerosis underlies multiple clinical manifestations ranging from asymptomatic to stable angina, acute coronary syndrome, MI, heart failure, and sudden cardiac death. The prerequisites for a closer study of the pathogenesis of the atherosclerotic process were the development of atherosclerotic vascular lesions at a younger age and the rapid progression of the process. Currently, it is generally accepted that CAD is a multifactorial disease. Attention is drawn to hereditary disorders of the receptor apparatus, endothelial dysfunction, and lipid metabolism disorders. In addition, latent viral infections are one of the etiopathogenetic factors in the development of atherosclerosis. A number of scientific studies have confirmed the relationship between infectious agents and the development of atherosclerotic vascular lesions. The viral etiology of the development and progression of atherosclerosis is the subject of debate among scientists around the world.

Keywords: 
herpesviruses • coronary atherosclerosis • Toll-like receptors • vascular endothelial cells
References: 
  1. World Health Organization. Prevention of Cardiovascular Disease. Guidelines for assessment and management of cardiovascular risk. Geneva, 2007.
  2. Burnett JR. Lipids, lipoproteins, atherosclerosis and cardiovascular disease. Clin Biochem Rev. 2004 Feb;25(1):2. 
  3. Huszar D, Varban ML, Rinninger F, Feeley R, Arai T, Fairchild-Huntress V, et al. Increased LDL cholesterol and atherosclerosis in LDL receptor-deficient mice with attenuated expression of scavenger receptor B1. Arterioscler Thromb Vasc Biol. 2000 Apr;20(4):1068-73. doi: 10.1161/01.atv.20.4.1068. 
  4. Mainous AG 3rd, Everett CJ, Diaz VA, Player MS, Gebregziabher M, Smith DW. Life stress and atherosclerosis: a pathway through unhealthy lifestyle. Int J Psychiatry Med. 2010;40(2):147-61. doi: 10.2190/PM.40.2.b. 
  5. van Leeuwen R, Ikram MK, Vingerling JR, Witteman JC, Hofman A, de Jong PT. Blood pressure, atherosclerosis, and the incidence of age-related maculopathy: the Rotterdam Study. Invest Ophthalmol Vis Sci. 2003 Sep;44(9):3771-7. doi: 10.1167/iovs.03-0121. 
  6. Kovacic S, Bakran M. Genetic susceptibility to atherosclerosis. Stroke Res Treat. 2012;2012:362941. doi: 10.1155/2012/362941.
  7. O'Donnell CJ. Family history, subclinical atherosclerosis, and coronary heart disease risk: barriers and opportunities for the use of family history information in risk prediction and prevention. Circulation. 2004 Oct 12;110(15):2074-6. doi: 10.1161/01.CIR.0000145539.77021.AC. 
  8. Epstein SE, Zhou YF, Zhu J. Infection and atherosclerosis: emerging mechanistic paradigms. Circulation. 1999 Jul 27;100(4):e20-8. doi: 10.1161/01.cir.100.4.e20. 
  9. Mayerl C, Lukasser M, Sedivy R, Niederegger H, Seiler R, Wick G. Atherosclerosis research from past to present--on the track of two pathologists with opposing views, Carl von Rokitansky and Rudolf Virchow. Virchows Arch. 2006 Jul;449(1):96-103. doi: 10.1007/s00428-006-0176-7.
  10.  Virchow R. Cellular Pathology. London: John Churchill; 1858.
  11. Libby P. Inflammation in atherosclerosis. Arterioscler Thromb Vasc Biol. 2012 Sep;32(9):2045-51. doi: 10.1161/ATVBAHA.108.179705. 
  12. Muhlestein JB, Anderson JL. Chronic infection and coronary artery disease. Cardiol Clin. 2003 Aug;21(3):333-62. doi: 10.1016/s0733-8651(03)00054-7. 
  13. Rosenfeld ME, Campbell LA. Pathogens and atherosclerosis: update on the potential contribution of multiple infectious organisms to the pathogenesis of atherosclerosis. Thromb Haemost. 2011 Nov;106(5):858-67. doi: 10.1160/TH11-06-0392. 
  14. Rupprecht HJ, Blankenberg S, Bickel C, Rippin G, Hafner G, Prellwitz W, et al.; AutoGene Investigators. Impact of viral and bacterial infectious burden on long-term prognosis in patients with coronary artery disease. Circulation. 2001 Jul 3;104(1):25-31. doi: 10.1161/hc2601.091703.
  15. Watt S, Aesch B, Lanotte P, Tranquart F, Quentin R. Viral and bacterial DNA in carotid atherosclerotic lesions. Eur J Clin Microbiol Infect Dis. 2003 Feb;22(2):99-105. doi: 10.1007/s10096-002-0867-1. 
  16. Fabricant CG, Fabricant J, Minick CR, Litrenta MM. Herpesvirus-induced atherosclerosis in chickens. Fed Proc. 1983 May 15;42(8):2476-9.
  17. Lawson JS. Multiple Infectious Agents and the Origins of Atherosclerotic Coronary Artery Disease. Front Cardiovasc Med. 2016 Sep 12;3:30. doi: 10.3389/fcvm.2016.00030. 
  18. Nikitskaya EA, Maryukhnich EV, Savvinova PP, Pinegina NV, Shpektor AV,  Vasilieva EYu, Margolis LB. Human herpesviruses and atherosclerosis. Modern point of view. Creative Cardiology. 2015;2:54–62. doi: 10.15275/kreatkard.2015.02.05.
  19. Yamashiroya HM, Ghosh L, Yang R, Robertson AL Jr. Herpesviridae in the coronary arteries and aorta of young trauma victims. Am J Pathol. 1988 Jan;130(1):71-9. 
  20. Xenaki E, Hassoulas J, Apostolakis S, Sourvinos G, Spandidos DA. Detection of cytomegalovirus in atherosclerotic plaques and nonatherosclerotic arteries. Angiology. 2009 Aug-Sep;60(4):504-8. doi: 10.1177/0003319708322390. 
  21. Horváth R, Cerný J, Benedík J Jr, Hökl J, Jelínková I, Benedík J. The possible role of human cytomegalovirus (HCMV) in the origin of atherosclerosis. J Clin Virol. 2000 Feb;16(1):17-24. doi: 10.1016/s1386-6532(99)00064-5. 
  22. Binkley PF, Cooke GE, Lesinski A, Taylor M, Chen M, Laskowski B, et al. Evidence for the role of Epstein Barr Virus infections in the pathogenesis of acute coronary events. PLoS One. 2013;8(1):e54008. doi: 10.1371/journal.pone.0054008. 
  23. Kotronias D, Kapranos N. Herpes simplex virus as a determinant risk factor for coronary artery atherosclerosis and myocardial infarction. In Vivo. 2005 Mar-Apr;19(2):351-7. 
  24. 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 Nov;80(5):1317-21. doi: 10.1172/JCI113208.
  25. Raza-Ahmad A, Klassen GA, Murphy DA, Sullivan JA, Kinley CE, Landymore RW, Wood JR. Evidence of type 2 herpes simplex infection in human coronary arteries at the time of coronary artery bypass surgery. Can J Cardiol. 1995 Dec;11(11):1025-9. 
  26. Zhu J, Quyyumi AA, Norman JE, Costello R, Csako G, Epstein SE. The possible role of hepatitis A virus in the pathogenesis of atherosclerosis. J Infect Dis. 2000 Dec;182(6):1583-7. doi: 10.1086/317613. Epub 2000 Oct 13. Erratum in: J Infect Dis 2001 Feb 1;183(3):521.
  27. Ishizaka N, Ishizaka Y, Takahashi E, Toda Ei E, Hashimoto H, Ohno M, et al. Increased prevalence of carotid atherosclerosis in hepatitis B virus carriers. Circulation. 2002 Mar 5;105(9):1028-30. doi: 10.1161/hc0902.105718.
  28. Butt AA, Xiaoqiang W, Budoff M, Leaf D, Kuller LH, Justice AC. Hepatitis C virus infection and the risk of coronary disease. Clin Infect Dis. 2009 Jul 15;49(2):225-32. doi: 10.1086/599371. 
  29. Ishizaka N, Ishizaka Y, Takahashi E, Tooda Ei, Hashimoto H, Nagai R, Yamakado M. Association between hepatitis C virus seropositivity, carotid-artery plaque, and intima-media thickening. Lancet. 2002 Jan 12;359(9301):133-5. doi: 10.1016/s0140-6736(02)07339-7. 
  30. Sharma S, Garg I, Ashraf MZ. TLR signalling and association of TLR polymorphism with cardiovascular diseases. Vascul Pharmacol. 2016 Dec;87:30-37. doi: 10.1016/j.vph.2016.10.008.
  31. Adamczak DM. The Role of Toll-Like Receptors and Vitamin D in Cardiovascular Diseases-A Review. Int J Mol Sci. 2017 Oct 27;18(11):2252. doi: 10.3390/ijms18112252. 
  32. Tobias P, Curtiss LK. Thematic review series: The immune system and atherogenesis. Paying the price for pathogen protection: toll receptors in atherogenesis. J Lipid Res. 2005 Mar;46(3):404-11. doi: 10.1194/jlr.R400015-JLR200. 
  33. Mullick AE, Tobias PS, Curtiss LK. Modulation of atherosclerosis in mice by Toll-like receptor 2. J Clin Invest. 2005 Nov;115(11):3149-56. doi: 10.1172/JCI25482. 
  34. Curtiss LK, Black AS, Bonnet DJ, Tobias PS. Atherosclerosis induced by endogenous and exogenous toll-like receptor (TLR)1 or TLR6 agonists. J Lipid Res. 2012 Oct;53(10):2126-2132. doi: 10.1194/jlr.M028431. 
  35. Michelsen KS, Wong MH, Shah PK, Zhang W, Yano J, Doherty TM, et al. Lack of Toll-like receptor 4 or myeloid differentiation factor 88 reduces atherosclerosis and alters plaque phenotype in mice deficient in apolipoprotein E. Proc Natl Acad Sci U S A. 2004 Jul 20;101(29):10679-84. doi: 10.1073/pnas.0403249101. 
  36. Ding Y, Subramanian S, Montes VN, Goodspeed L, Wang S, Han C, et al. Toll-like receptor 4 deficiency decreases atherosclerosis but does not protect against inflammation in obese low-density lipoprotein receptor-deficient mice. Arterioscler Thromb Vasc Biol. 2012 Jul;32(7):1596-604. doi: 10.1161/ATVBAHA.112.249847. 
  37. Ishibashi M, Sayers S, D'Armiento JM, Tall AR, Welch CL. TLR3 deficiency protects against collagen degradation and medial destruction in murine atherosclerotic plaques. Atherosclerosis. 2013 Jul;229(1):52-61. doi: 10.1016/j.atherosclerosis.2013.03.035.
  38. Karper JC, Ewing MM, Habets KL, de Vries MR, Peters EA, van Oeveren-Rietdijk AM, et al. Blocking toll-like receptors 7 and 9 reduces postinterventional remodeling via reduced macrophage activation, foam cell formation, and migration. Arterioscler Thromb Vasc Biol. 2012 Aug;32(8):e72-80. doi: 10.1161/ATVBAHA.112.249391. 
  39. Li B, Xia Y, Hu B. Infection and atherosclerosis: TLR-dependent pathways. Cell Mol Life Sci. 2020 Jul;77(14):2751-2769. doi: 10.1007/s00018-020-03453-7.
  40. Ross R. Atherosclerosis--an inflammatory disease. N Engl J Med. 1999 Jan 14;340(2):115-26. doi: 10.1056/NEJM199901143400207.
  41. Sorlie PD, Nieto FJ, Adam E, Folsom AR, Shahar E, Massing M. A prospective study of cytomegalovirus, herpes simplex virus 1, and coronary heart disease: the atherosclerosis risk in communities (ARIC) study. Arch Intern Med. 2000 Jul 10;160(13):2027-32. doi: 10.1001/archinte.160.13.2027. 
  42. Siscovick DS, Schwartz SM, Corey L, Grayston JT, Ashley R, Wang SP, et al. Chlamydia pneumoniae, herpes simplex virus type 1, and cytomegalovirus and incident myocardial infarction and coronary heart disease death in older adults : the Cardiovascular Health Study. Circulation. 2000 Nov 7;102(19):2335-40. doi: 10.1161/01.cir.102.19.2335
  43. 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 Aug 29;335(9):624-30. doi: 10.1056/NEJM199608293350903. 
  44. Sambiase NV, Higuchi ML, Nuovo G, Gutierrez PS, Fiorelli AI, Uip DE, Ramires JA. CMV and transplant-related coronary atherosclerosis: an immunohistochemical, in situ hybridization, and polymerase chain reaction in situ study. Mod Pathol. 2000 Feb;13(2):173-9. doi: 10.1038/modpathol.3880032. 
  45. Tufano A, Di Capua M, Coppola A, Conca P, Cimino E, Cerbone AM, Di Minno G. The infectious burden in atherothrombosis. Semin Thromb Hemost. 2012 Jul;38(5):515-23. doi: 10.1055/s-0032-1315759. 
  46. Khoretonenko MV, Leskov IL, Jennings SR, Yurochko AD, Stokes KY. Cytomegalovirus infection leads to microvascular dysfunction and exacerbates hypercholesterolemia-induced responses. Am J Pathol. 2010 Oct;177(4):2134-44. doi: 10.2353/ajpath.2010.100307. 
  47. Gombos RB, Brown JC, Teefy J, Gibeault RL, Conn KL, Schang LM, Hemmings DG. Vascular dysfunction in young, mid-aged and aged mice with latent cytomegalovirus infections. Am J Physiol Heart Circ Physiol. 2013 Jan 15;304(2):H183-94. doi: 10.1152/ajpheart.00461.2012. 
  48. Carlquist JF, Muhlestein JB, Horne BD, Hart NI, Lim T, Habashi J, et al. Cytomegalovirus stimulated mRNA accumulation and cell surface expression of the oxidized LDL scavenger receptor, CD36. Atherosclerosis. 2004 Nov;177(1):53-9. doi: 10.1016/j.atherosclerosis.2004.07.010. 
  49. Jarvis MA, Nelson JA. Human cytomegalovirus persistence and latency in endothelial cells and macrophages. Curr Opin Microbiol. 2002 Aug;5(4):403-7. doi: 10.1016/s1369-5274(02)00334-x. 
  50. Strååt K, de Klark R, Gredmark-Russ S, Eriksson P, Söderberg-Nauclér C. Infection with human cytomegalovirus alters the MMP-9/TIMP-1 balance in human macrophages. J Virol. 2009 Jan;83(2):830-5. doi: 10.1128/JVI.01363-08.
  51. Lunardi C, Dolcino M, Peterlana D, Bason C, Navone R, Tamassia N, et al. Endothelial cells' activation and apoptosis induced by a subset of antibodies against human cytomegalovirus: relevance to the pathogenesis of atherosclerosis. PLoS One. 2007 May 30;2(5):e473. doi: 10.1371/journal.pone.0000473. 
  52. Popović M, Smiljanić K, Dobutović B, Syrovets T, Simmet T, Isenović ER. Human cytomegalovirus infection and atherothrombosis. J Thromb Thrombolysis. 2012 Feb;33(2):160-72. doi: 10.1007/s11239-011-0662-x. 
  53. Shen K, Xu L, Chen D, Tang W, Huang Y. Human cytomegalovirus-encoded miR-UL112 contributes to HCMV-mediated vascular diseases by inducing vascular endothelial cell dysfunction. Virus Genes. 2018 Apr;54(2):172-181. doi: 10.1007/s11262-018-1532-9. 
  54.  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 Jul 15;265(5170):391-4. doi: 10.1126/science.8023160. 
  55. Fan T, Lu H, Hu H, Shi L, McClarty GA, Nance DM,et al. Inhibition of apoptosis in chlamydia-infected cells: blockade of mitochondrial cytochrome c release and caspase activation. J Exp Med. 1998 Feb 16;187(4):487-96. doi: 10.1084/jem.187.4.487. 
  56. Zhou YF, Guetta E, Yu ZX, Finkel T, Epstein SE. Human cytomegalovirus increases modified low density lipoprotein uptake and scavenger receptor mRNA expression in vascular smooth muscle cells. J Clin Invest. 1996 Nov 1;98(9):2129-38. doi: 10.1172/JCI119019.
  57. Chanouzas D, Sagmeister M, Dyall L, Sharp P, Powley L, Johal S, et al. The host cellular immune response to cytomegalovirus targets the endothelium and is associated with increased arterial stiffness in ANCA-associated vasculitis. Arthritis Res Ther. 2018 Aug 29;20(1):194. doi: 10.1186/s13075-018-1695-8. 
  58. Ait-Oufella H, Taleb S, Mallat Z, Tedgui A. Recent advances on the role of cytokines in atherosclerosis. Arterioscler Thromb Vasc Biol. 2011 May;31(5):969-79. doi: 10.1161/ATVBAHA.110.207415.
  59. Apostolou F, Gazi IF, Lagos K, Tellis CC, Tselepis AD, Liberopoulos EN, Elisaf M. Acute infection with Epstein-Barr virus is associated with atherogenic lipid changes. Atherosclerosis. 2010 Oct;212(2):607-13. doi: 10.1016/j.atherosclerosis.2010.06.006. 
  60. Gargouri B, Nasr R, Mseddi M, Benmansour R, Lassoued S. Induction of Epstein-Barr virus (EBV) lytic cycle in vitro causes lipid peroxidation, protein oxidation and DNA damage in lymphoblastoid B cell lines. Lipids Health Dis. 2011 Jul 1;10:111. doi: 10.1186/1476-511X-10-111. 
  61. Bennett MR, Sinha S, Owens GK. Vascular Smooth Muscle Cells in Atherosclerosis. Circ Res. 2016 Feb 19;118(4):692-702. doi: 10.1161/CIRCRESAHA.115.306361. 
  62. Kutikhin AG, Yuzhalin AE, Brusina EB, Tsitko EA. [The role of viruses in the development of atherosclerosis: evidence from basic research]. Epidemiology and Vaccinal Prevention. 2013;2(69):66–72. [Article in Russian].
  63. Melnick JL, Petrie BL, Dreesman GR, Burek J, McCollum CH, DeBakey ME. Cytomegalovirus antigen within human arterial smooth muscle cells. Lancet. 1983 Sep 17;2(8351):644-7. doi: 10.1016/s0140-6736(83)92529-1.
  64. Wu YP, Sun DD, Wang Y, Liu W, Yang J. Herpes Simplex Virus Type 1 and Type 2 Infection Increases Atherosclerosis Risk: Evidence Based on a Meta-Analysis. Biomed Res Int. 2016;2016:2630865. doi: 10.1155/2016/2630865. 
  65. 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 Sci U S A. 1988 Nov;85(21):8227-30. doi: 10.1073/pnas.85.21.8227. 
  66. Key NS, Vercellotti GM, Winkelmann JC, Moldow CF, Goodman JL, Esmon NL, et al. Infection of vascular endothelial cells with herpes simplex virus enhances tissue factor activity and reduces thrombomodulin expression. Proc Natl Acad Sci U S A. 1990 Sep;87(18):7095-9. doi: 10.1073/pnas.87.18.7095. 
  67. 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 May 18;61(4):657-62. doi: 10.1016/0092-8674(90)90477-v. 
  68. White DW, Suzanne Beard R, Barton ES. Immune modulation during latent herpesvirus infection. Immunol Rev. 2012 Jan;245(1):189-208. doi: 10.1111/j.1600-065X.2011.01074.x. 
  69. Decman V, Freeman ML, Kinchington PR, Hendricks RL. Immune control of HSV-1 latency. Viral Immunol. 2005;18(3):466-73. doi: 10.1089/vim.2005.18.466. 
  70. Callan MF. The immune response to Epstein-Barr virus. Microbes Infect. 2004 Aug;6(10):937-45. doi: 10.1016/j.micinf.2004.04.014. 
  71. Moss P, Khan N. CD8(+) T-cell immunity to cytomegalovirus. Hum Immunol. 2004 May;65(5):456-64. doi: 10.1016/j.humimm.2004.02.014. 
  72.  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 Sep 1;94(5):922-7. doi: 10.1161/01.cir.94.5.922.
  73. Sorlie PD, Adam E, Melnick SL, Folsom A, Skelton T, Chambless LE, et al. Cytomegalovirus/herpesvirus and carotid atherosclerosis: the ARIC Study. J Med Virol. 1994 Jan;42(1):33-7. doi: 10.1002/jmv.1890420107. 
  74. Vliegen I, Duijvestijn A, Grauls G, Herngreen S, Bruggeman C, Stassen F. Cytomegalovirus infection aggravates atherogenesis in apoE knockout mice by both local and systemic immune activation. Microbes Infect. 2004 Jan;6(1):17-24. doi: 10.1016/j.micinf.2003.09.024. 
  75. Krebs P, Scandella E, Bolinger B, Engeler D, Miller S, Ludewig B. Chronic immune reactivity against persisting microbial antigen in the vasculature exacerbates atherosclerotic lesion formation. Arterioscler Thromb Vasc Biol. 2007 Oct;27(10):2206-13. doi: 10.1161/ATVBAHA.107.141846. 
  76. Melnychuk RM, Smith P, Kreklywich CN, Ruchti F, Vomaske J, Hall L, et al. Mouse cytomegalovirus M33 is necessary and sufficient in virus-induced vascular smooth muscle cell migration. J Virol. 2005 Aug;79(16):10788-95. doi: 10.1128/JVI.79.16.10788-10795.2005.
  77. Vliegen I, Duijvestijn A, Stassen F, Bruggeman C. Murine cytomegalovirus infection directs macrophage differentiation into a pro-inflammatory immune phenotype: implications for atherogenesis. Microbes Infect. 2004 Oct;6(12):1056-62. doi: 10.1016/j.micinf.2004.05.020. 
  78. Du Y, Zhang G, Liu Z. Human cytomegalovirus infection and coronary heart disease: a systematic review. Virol J. 2018 Feb 6;15(1):31. doi: 10.1186/s12985-018-0937-3.
  79. Horváth R, Cerný J, Benedík J Jr, Hökl J, Jelínková I, Benedík J. The possible role of human cytomegalovirus (HCMV) in the origin of atherosclerosis. J Clin Virol. 2000 Feb;16(1):17-24. doi: 10.1016/s1386-6532(99)00064-5. 
  80. Izadi M, Fazel M, Saadat SH, Nasseri MH, Ghasemi M, Dabiri H, et al. Cytomegalovirus localization in atherosclerotic plaques is associated with acute coronary syndromes: report of 105 patients. Methodist Debakey Cardiovasc J. 2012 Apr-Jun;8(2):42-6. doi: 10.14797/mdcj-8-2-42. 
  81. Beristain-Covarrubias N, Perez-Toledo M, Thomas MR, Henderson IR, Watson SP, Cunningham AF. Understanding Infection-Induced Thrombosis: Lessons Learned From Animal Models. Front Immunol. 2019 Nov 5;10:2569. doi: 10.3389/fimmu.2019.02569.
  82.  Kohler JA, Munoz FM, Goss JA, Miloh TA. Viral upper respiratory infection at pediatric liver transplantation is associated with hepatic artery thrombosis. Liver Transpl. 2017 Nov;23(11):1477-1481. doi: 10.1002/lt.24866.
  83. Yang Y, Tang H. Aberrant coagulation causes a hyper-inflammatory response in severe influenza pneumonia. Cell Mol Immunol. 2016 Jul;13(4):432-42. doi: 10.1038/cmi.2016.1.
  84. Cui S, Fu Z, Feng Y, Xie X, Ma X, Liu T, et al. The disseminated intravascular coagulation score is a novel predictor for portal vein thrombosis in cirrhotic patients with hepatitis B. Thromb Res. 2018 Jan;161:7-11. doi: 10.1016/j.thromres.2017.11.010.
  85. Rahbar A, Söderberg-Nauclér C. Human cytomegalovirus infection of endothelial cells triggers platelet adhesion and aggregation. J Virol. 2005 Feb;79(4):2211-20. doi: 10.1128/JVI.79.4.2211-2220.2005.
  86. Taveira A, Ponroy N, Mueller NJ, Millard AL. Entry of human cytomegalovirus into porcine endothelial cells depends on both the cellular vascular origin and the viral strain. Xenotransplantation. 2014 Jul-Aug;21(4):324-40. doi: 10.1111/xen.12097. 
  87. Doyle B, Caplice N. Plaque neovascularization and antiangiogenic therapy for atherosclerosis. J Am Coll Cardiol. 2007 May 29;49(21):2073-80. doi: 10.1016/j.jacc.2007.01.089.
  88. Haji SA, Starling RC, Avery RK, Mawhorter S, Tuzcu EM, Schoenhagen P, et al. Donor hepatitis-C seropositivity is an independent risk factor for the development of accelerated coronary vasculopathy and predicts outcome after cardiac transplantation. J Heart Lung Transplant. 2004 Mar;23(3):277-83. doi: 10.1016/S1053-2498(03)00148-7. 
  89. Simanek AM, Dowd JB, Pawelec G, Melzer D, Dutta A, Aiello AE. Seropositivity to cytomegalovirus, inflammation, all-cause and cardiovascular disease-related mortality in the United States. PLoS One. 2011 Feb 17;6(2):e16103. doi: 10.1371/journal.pone.0016103. 

Download Article
Received August 30, 2021.
Accepted October 17, 2021.
©2021 International Medical Research and Development Corporation.