Coronary heart disease in patients with human immunodeficiency virus infection
- Authors: Alieva A.M.1, Batov M.A.2, Skripnichenko E.A.1, Teplova N.V.1, Baykova I.E.1, Valiev R.K.3, Akhmedova M.F.4, Kotikova I.A.1, Melikulov A.A.4, Nikitin I.G.1
-
Affiliations:
- The Russian National Research Medical University named after N.I. Pirogov
- P. Hertsen Moscow Oncology Research Institute — Branch of the National Medical Research Radiological Centre
- The Loginov Moscow Clinical Scientific Center
- AKFA Medline
- Issue: Vol 29, No 1 (2023)
- Pages: 29-42
- Section: Reviews
- URL: https://journals.rcsi.science/0869-2106/article/view/131860
- DOI: https://doi.org/10.17816/medjrf112317
- ID: 131860
Cite item
Abstract
According to the World Health Organization, more than 38 million people are carriers of the human immunodeficiency virus (HIV). The relative risk of cardiovascular events in patients with HIV infection is 1.5–2 times higher than those without it. An HIV-positive status is associated with a 50% increased risk of acute myocardial infarction. The mechanisms of CVD development caused by HIV activity are not fully understood, and the contribution of traditional risk factors cannot fully explain such a high potential for coronary heart disease (CHD) in patients with HIV infection. Data suggest that HIV-associated chronic inflammation and immune system activation may lead to progressive endothelial dysfunction and vascular damage. The pathogenesis of atherosclerosis and, consequently, CHD in HIV infection is extremely versatile and poorly studied. The key mechanisms in HIV-associated CHD include the effect of HIV proteins on immunocompetent cells and vascular endothelium, immunodeficiency, translocation of microorganisms from the gut, and chronic inflammation with platelet activation. Despite considerable progress in understanding HIV-associated cardiovascular disease, many unresolved questions remain. Even with effective viral suppression, inflammation and immune dysregulation appear to increase the risk of cardiovascular complications. The lack of large-scale clinical studies on the prevention and treatment of cardiovascular disease in HIV is very important. Nevertheless, some important features should be considered in the management of patients with HIV infection.
Full Text
##article.viewOnOriginalSite##About the authors
Amina M. Alieva
The Russian National Research Medical University named after N.I. Pirogov
Author for correspondence.
Email: amisha_alieva@mail.ru
ORCID iD: 0000-0001-5416-8579
SPIN-code: 2749-6427
MD, Cand. Sci. (Med.), associate professor
Russian Federation, 1, Ostrovityanova street, 117997, MoscowMaxim A. Batov
P. Hertsen Moscow Oncology Research Institute — Branch of the National Medical Research Radiological Centre
Email: md.batov@gmail.com
ORCID iD: 0000-0002-3780-4358
SPIN-code: 5850-7711
resident physician
Russian Federation, MoscowElina A. Skripnichenko
The Russian National Research Medical University named after N.I. Pirogov
Email: elkaskrip@gmail.com
ORCID iD: 0000-0001-6321-8419
SPIN-code: 3176-2080
PhD student
Russian Federation, 1, Ostrovityanova street, 117997, MoscowNatalia V. Teplova
The Russian National Research Medical University named after N.I. Pirogov
Email: teplova.nv@yandex.ru
ORCID iD: 0000-0002-7181-4680
SPIN-code: 9056-1948
MD, Dr. Sci. (Med.), professor
Russian Federation, 1, Ostrovityanova street, 117997, MoscowIrina E. Baykova
The Russian National Research Medical University named after N.I. Pirogov
Email: 1498553@mail.ru
ORCID iD: 0000-0003-0886-6290
SPIN-code: 3054-8884
MD, Cand. Sci. (Med.), associate professor
Russian Federation, 1, Ostrovityanova street, 117997, MoscowRamiz K. Valiev
The Loginov Moscow Clinical Scientific Center
Email: radiosurgery@bk.ru
ORCID iD: 0000-0003-1613-3716
SPIN-code: 2855-2867
MD, Cand. Sci. (Med.)
Russian Federation, MoscowMadina F. Akhmedova
AKFA Medline
Email: drmadina@yandex.ru
ORCID iD: 0000-0002-6184-6742
SPIN-code: 7395-4676
MD, Cand. Sci. (Med.)
Uzbekistan, TashkentIrina A. Kotikova
The Russian National Research Medical University named after N.I. Pirogov
Email: kotikova.ia@mail.ru
ORCID iD: 0000-0001-5352-8499
SPIN-code: 1423-7300
student
Russian Federation, 1, Ostrovityanova street, 117997, MoscowAlisher A. Melikulov
AKFA Medline
Email: melikulov.alisher@yandex.ru
ORCID iD: 0000-0002-5164-9702
SPIN-code: 1086-0141
MD, Dr. Sci. (Med.)
Uzbekistan, TashkentIgor G. Nikitin
The Russian National Research Medical University named after N.I. Pirogov
Email: igor.nikitin.64@mail.ru
ORCID iD: 0000-0003-1699-0881
SPIN-code: 3595-1990
MD, Dr. Sci. (Med.), professor
Russian Federation, 1, Ostrovityanova street, 117997, MoscowReferences
- Malebranche D. HIV care has improved dramatically-but not for everyone. Nature. 2022;605(7910):S24–S25. doi: 10.1038/d41586-022-01350-6
- Pokrovsky VV, Ulumbekova GE, Petrachkov IV. Organization of medical care for infection caused by human immunodeficiency virus. Healthcare Management: News. Views. Education. Bulletin of VSHOUZ. 2022;8(2):108–130. (In Russ). doi: 10.33029/2411-8621-2022-8-2-108-130
- Patel AA, Budoff MJ. Coronary artery disease in patients with HIV infection: an update. Am J Cardiovasc Drugs. 2021;21(4):411–417. doi: 10.1007/s40256-020-00451-9
- Shah ASV, Stelzle D, Lee KK, et al. Global burden of atherosclerotic cardiovascular disease in people living with HIV: systematic review and meta-analysis. Circulation. 2018;138(11):1100–1112. doi: 10.1161/circulationaha.117.033369
- Triant VA, Lee H, Hadigan C, Grinspoon SK. Increased acute myocardial infarction rates and cardiovascular risk factors among patients with human immunodeficiency virus disease. J Clin Endocrinol Metab. 2007;92(7):2506–2512. doi: 10.1210/jc.2006-2190
- Freiberg MS, Chang CC, Kuller LH, et al. HIV infection and the risk of acute myocardial infarction. JAMA Intern Med. 2013;173(8): 614–622. doi: 10.1001/jamainternmed.2013.3728
- Durand M, Sheehy O, Baril JG, et al. Association between HIV infection, antiretroviral therapy, and risk of acute myocardial infarction: a cohort and nested case-control study using Quebec’s public health insurance database. J Acquir Immune Defic Syndr. 2011;57(3):245–253. doi: 10.1097/qai.0b013e31821d33a5
- Jong E, Louw S, van Gorp EC, et al. The effect of initiating combined antiretroviral therapy on endothelial cell activation and coagulation markers in South African HIV-infected individuals. Thromb Haemost. 2010;104(6):1228–1234. doi: 10.1160/th10-04-0233
- Arildsen H, Sørensen KE, Ingerslev JM, et al. Endothelial dysfunction, increased inflammation, and activated coagulation in HIV-infected patients improve after initiation of highly active antiretroviral therapy. HIV Med. 2013;14(1):1–9. doi: 10.1111/j.1468-1293.2012.01027.x
- Neuhaus J, Jacobs DR Jr, Baker JV, et al. Markers of inflammation, coagulation, and renal function are elevated in adults with HIV infection. J Infect Dis. 2010;201(12):1788–1795. doi: 10.1086/652749
- Dhawan S, Puri RK, Kumar A, et al. Human immunodeficiency virus-1-tat protein induces the cell surface expression of endothelial leukocyte adhesion molecule-1, vascular cell adhesion molecule-1, and intercellular adhesion molecule-1 in human endothelial cells. Blood. 1997;90(4):1535–1544. doi: 10.1182/blood.V90.4.1535
- Wang D, Melancon JK, Verbesey J, et al. Microvascular endothelial dysfunction and enhanced thromboxane and endothelial contractility in patients with HIV. J AIDS Clin Res. 2013;4(12):267. doi: 10.4172/2155-6113.1000267
- Tawakol A, Ishai A, Li D, et al. Association of arterial and lymph node inflammation with distinct inflammatory pathways in human immunodeficiency virus infection. JAMA Cardiol. 2017;2(2):163–171. doi: 10.1001/jamacardio.2016.4728
- Falcão M da C, Zírpoli JC, Albuquerque VM, et al. Association of biomarkers with atherosclerosis and risk for coronary artery disease in patients with HIV. Arq Bras Cardiol. 2012;99(5):971–978. doi: 10.1590/s0066-782x2012005000093
- Sandler NG, Wand H, Roque A, et al. Plasma levels of soluble CD14 independently predict mortality in HIV infection. J Infect Dis. 2011;203(6):780–790. doi: 10.1093/infdis/jiq118
- Qi Q, Hua S, Clish CB, et al. Plasma tryptophan-kynurenine metabolites are altered in human immunodeficiency virus infection and associated with progression of carotid artery atherosclerosis. Clin Infect Dis. 2018;67(2):235–242. doi: 10.1093/cid/ciy053
- Doring Y, Soehnlein O, Weber C. Neutrophil extracellular traps in atherosclerosis and atherothrombosis. Circ Res. 2017;120(4): 736–743. doi: 10.1161/circresaha.116.309692
- Mojoli A, Goncalves BS, Temerozo JR, et al. Neutrophil extracellular traps from healthy donors and HIV-1-infected individuals restrict HIV-1 production in macrophages. Sci Rep. 2020;10(1):19603. doi: 10.1038/s41598-020-75357-2
- Knight JS, Luo W, O’Dell AA, et al. Peptidylarginine deiminase inhibition reduces vascular damage and modulates innate immune responses in murine models of atherosclerosis. Circ Res. 2014; 114(6):947–956. doi: 10.1161/circresaha.114.303312
- Ishizaki A, Bi X, Nguyen LV, et al. Effects of short-term probiotic ingestion on immune profiles and microbial translocation among HIV-1-infected Vietnamese children. Int J Mol Sci. 2017;8(10):2185. doi: 10.3390/ijms18102185
- Tincati C, Douek DC, Marchetti G. Gut barrier structure, mucosal immunity and intestinal microbiota in the pathogenesis and treatment of HIV infection. AIDS Res. 2019;13:19. doi: 10.1186/s12981-016-0103-1
- Ouyang J, Zaongo SD, Zhang X, et al. Microbiota-meditated immunity abnormalities facilitate hepatitis b virus co-infection in people living with HIV: a review. Front Immunol. 2022;12:755890. doi: 10.3389/fimmu.2021.755890
- El-Far M, Tremblay CL. Gut microbial diversity in HIV infection post combined antiretroviral therapy: a key target for prevention of cardiovascular disease. Curr Opin HIV AIDS. 2018;13(1):38–44. doi: 10.1097/coh.0000000000000426
- Wang Z, Qi Q. Gut microbial metabolites associated with HIV infection. Future Virol. 2019;14(5):335–347. doi: 10.2217/fvl-2019-0002
- Hileman CO, Longenecker CT, Carman TL, et al. Elevated D-dimer is independently associated with endothelial dysfunction: a cross-sectional study in HIV-infected adults on antiretroviral therapy. Antivir Ther. 2012;17(7):1345–1349. doi: 10.3851/imp2297
- Sinha A, Ma Y, Scherzer R, et al. Role of T-cell dysfunction, inflammation, and coagulation in microvascular disease in HIV. J Am Heart Assoc. 2016;5(12):e004243. doi: 10.1161/jaha.116.004243
- Getawa S, Adane T. Coagulation parameters in human immunodeficiency virus infected patients: a systematic review and meta-analysis. AIDS Res Treat. 2022;2022:6782595. doi: 10.1155/2022/6782595
- Tien PC, Benson C, Zolopa AR, et al. The study of fat redistribution and metabolic change in HIV infection (FRAM): methods, design, and sample characteristics. Am J Epidemiol. 2006;163(9):860–869. doi: 10.1093/aje/kwj111
- Madden E, Lee G, Kotler DP, et al. Association of antiretroviral therapy with fibrinogen levels in HIV-infection. AIDS. 2008;22(6): 707–715. doi: 10.1097/QAD.0b013e3282f560d9
- Graham SM, Nance RM, Chen J, et al. Elevated plasma von willebrand factor levels are associated with subsequent ischemic stroke in persons with treated HIV infection. Open Forum Infect Dis. 2021;8(11):ofab521. doi: 10.1093/ofid/ofab521
- Funderburg NT. Markers of coagulation and inflammation often remain elevated in ART-treated HIV-infected patients. Curr Opin HIV AIDS. 2014;9(1):80–86. doi: 10.1097/coh.0000000000000019
- Siddiqui MA, Yamashita M. Toll-like receptor (TLR) signaling enables cyclic GMP-AMP synthase (cGAS) sensing of HIV-1 infection in macrophages. mBio. 2021;12(6):e0281721. doi: 10.1128/mBio.02817-21
- Hurley A, Smith M, Karpova T, et al. Enhanced effector function of CD8(+) T cells from healthy controls and HIV-infected patients occurs through thrombin activation of protease-activated receptor 1. J Infect Dis. 2013;207(4):638–650. doi: 10.1093/infdis/jis730
- Antoniak S, Owens AP, Baunacke M, et al. PAR-1 contributes to the innate immune response during viral infection. J Clin Invest. 2013;123(3):1310–1322. doi: 10.1172/jci66125
- Khawaja AA, Taylor KA, Lovell AO, et al. HIV antivirals affect endothelial activation and endothelial-platelet crosstalk. Circ Res. 2020;127(11):1365–1380. doi: 10.1161/circresaha.119.316477
- Alieva AM, Sozykin AV, Lyalina VV, et al. Modern view on the problem of atherosclerosis in HIV-positive people. Russian Cardiology Bulletin. 2022;17(2):25–32. (In Russ). doi: 10.17116/Cardiobulletin20221702125
- Feinstein MJ, Hsue PY, Benjamin LA, et al. Characteristics, prevention, and management of cardiovascular disease in people living with HIV: a scientific statement from the American Heart Association. Circulation. 2019;140(2):e98–e124. doi: 10.1161/cir.0000000000000695
- Peyracchia M, De Lio G, Montrucchio C, et al. Evaluation of coronary features of HIV patients presenting with ACS: the CUORE, a multicenter study. Atherosclerosis. 2018;274:218–226. doi: 10.1016/j.atherosclerosis.2018.05.001
- Lo J, Abbara S, Shturman L, et al. Increased prevalence of subclinical coronary atherosclerosis detected by coronary computed tomography angiography in HIV-infected men. AIDS. 2010;24(2): 243–253. doi: 10.1097/QAD.0b013e328333ea9e
- Laurent C, Marcal AL, Prieto-Gonzalez S, et al. HIV-associated vasculitis. Part II: histologic and angiographic diagnostic reconfirmation after an uncontrolled HIV infection and fatal outcome. Clin Exp Rheumatol. 2019;suppl 117(2):151–152.
- Fitch KV, Fulda ES, Grinspoon SK. Statins for primary cardiovascular disease prevention among people with HIV: emergent directions. Curr Opin HIV AIDS. 2022;17(5):293–300. doi: 10.1097/coh.0000000000000752
- O’Dwyer EJ, Bhamra-Ariza P, Rao S, et al. Lower coronary plaque burden in patients with HIV presenting with acute coronary syndrome. Open Heart. 2016;3(2):e000511. doi: 10.1136/openhrt-2016-000511
- Theodoropoulos K, Mennuni M, Sartori S, et al. Quantitative angiographic characterisation of coronary artery disease in patients with human immunodeficiency virus (HIV) infection undergoing percutaneous coronary intervention. EuroIntervention. 2017;12(14):1757–1765. doi: 10.4244/eij-d-15-00409
- Becker AC, Sliwa K, Stewart S, et al. Acute coronary syndromes in treatment-naïve black south africans with human immunodeficiency virus infection. J Interv Cardiol. 2010;23(1):70–77. doi: 10.1111/j.1540-8183.2009.00520.x
- Perelló R, Calvo M, Miró O, et al. Clinical presentation of acute coronary syndrome in HIV infected adults: a retrospective analysis of a prospectively collected cohort. Eur J Intern Med. 2011;22(5): 485–488. doi: 10.1016/j.ejim.2011.02.017
- Nadel J, O’Dwyer E, Emmanuel S, et al. High-risk coronary plaque, invasive coronary procedures, and cardiac events among HIV-positive individuals and matched controls. J Cardiovasc Comput Tomogr. 2016;10(5):391–397. doi: 10.1016/j.jcct.2016.07.018
- Vachiat A, McCutcheon K, Tsabedze N, et al. HIV and ischemic heart disease. J Am Coll Cardiol. 2017;69(1):73–82. doi: 10.1016/j.jacc.2016.09.979
- Hauguel-Moreau M, Boccara F, Boyd A, et al. Platelet reactivity in human immunodeficiency virus infected patients on dual antiplatelet therapy for an acute coronary syndrome: the EVERE2ST-HIV study. Eur Heart J. 2017;38(21):1676–1686. doi: 10.1093/eurheartj/ehw583
- McCutcheon K, Triantafyllis AS, Van den Eynde J, et al. Coronary revascularization in patients with HIV. Trends Cardiovasc Med. 2022;32(3):163–169. doi: 10.1016/j.tcm.2021.02.006
- Smilowitz NR, Gupta N, Guo Y, et al. Influence of human immunodeficiency virus seropositive status on the in-hospital management and outcomes of patients presenting with acute myocardial infarction. J Invasive Cardiol. 2016;28(10):403–409.
- Peyracchia M, Verardi R, Rubin SR, et al. In-hospital and long-term outcomes of HIV-positive patients undergoing PCI according to kind of stent: a meta-analysis. J Cardiovasc Med (Hagerstown). 2019;20(5):321–326. doi: 10.2459/JCM.0000000000000767
- Ren X, Trilesskaya M, Kwan DM, et al. Comparison of outcomes using bare metal versus drug-eluting stents in coronary artery disease patients with and without human immunodeficiency virus infection. Am J Cardiol. 2009;104(2):216–222. doi: 10.1016/j.amjcard.2009.03.036
- Yanagawa B, Verma S, Dwivedi G, et al. Cardiac surgery in HIV patients: state of the Art. Can J Cardiol. 2019;35(3):320–325. doi: 10.1016/j.cjca.2018.11.006
- Wollner G, Zimpfer D, Manduric M, et al. Outcomes of coronary artery bypass grafting in patients with human immunodeficiency virus infection. J Card Surg. 2020;35(10):2543–2549. doi: 10.1111/jocs.14828
- Dominici C, Chello M. Impact of human immunodeficiency virus (HIV) infection in patients undergoing cardiac surgery: a systematic review. Rev Cardiovasc Med. 2020;21(3):411–418. doi: 10.31083/j.rcm.2020.03.104
- Poznyak AV, Bezsonov EE, Borisov EE, et al. Atherosclerosis in HIV patients: what do we know so far? Int J Mol Sci. 2022;23(5):2504. doi: 10.3390/ijms23052504
- Leyes P, Cofan M, González-Cordón A, et al. Increased cholesterol absorption rather than synthesis is involved in boosted protease inhibitor-associated hypercholesterolaemia. AIDS. 2018;32(10): 1309–1316. doi: 10.1097/qad.0000000000001837
- Mulligan K, Grunfeld C, Tai VW, et al. Hyperlipidemia and insulin resistance are induced by protease inhibitors independent of changes in body composition in patients with HIV infection. J Acquir Immune Defic Syndr. 2000;23(1):35–43. doi: 10.1097/00126334-200001010-00005
- Martinez E, Gonzalez-Cordon A, Ferrer E, et al. Early lipid changes with atazanavir/ritonavir or darunavir/ritonavir. HIV Med. 2014;16(6):330–338. doi: 10.1111/hiv.12121
- Jain RG, Furfine ES, Pedneault L, et al. Metabolic complications associated with antiretroviral therapy. Antiviral Res. 2001;51(3): 151–177. doi: 10.1016/S0166-3542(01)00148-6
- Palacios R, Pérez-Hernández IA, Martínez MA, et al. Efficacy and safety of switching to abacavir/lamivudine (ABC/3TC) plus rilpivirine (RPV) in virologically suppressed HIV-infected patients on HAART. Eur J Clin Microbiol Infect Dis. 2016;36(5):815–819. doi: 10.1007/s10096-016-2602-3
- Myerson M, Malvestutto C, Aberg JA. Management of lipid disorders in patients living with HIV. J Clin Pharmacol. 2015;55(9): 957–974. doi: 10.1002/jcph.473
- Lagathu C, Béréziat V, Gorwood J, et al. Metabolic complications affecting adipose tissue, lipid and glucose metabolism associated with HIV antiretroviral treatment. Expert Opin Drug Saf. 2019;18(9): 829–840. doi: 10.1080/14740338.2019.1644317
- Thompson MA, Horberg MA, Agwu AL, et al. Primary care guidance for persons with human immunodeficiency virus: 2020 update by the HIV medicine association of the infectious diseases society of America. Clin Infect Dis. 2021;73(11):e3572–e3605. doi: 10.1093/cid/ciaa1391
- Dube MP, Stein JH, Aberg JA, et al. Guidelines for the evaluation and management of dyslipidemia in human immunodeficiency virus (HIV)-infected adults receiving antiretroviral therapy: recommendations of the HIV medicine association of the infectious disease society of America and the adult. Clin Infect Dis. 2003;37(5):613–627. doi: 10.1086/378131
- Fichtenbaum CJ, Gerber JG, Rosenkranz SL, et al. Pharmacokinetic interactions between protease inhibitors and statins in HIV seronegative volunteers: ACTG Study A5047. AIDS. 2002;16(4):569–577. doi: 10.1097/00002030-200203080-00008
- Vavlukis M, Vavlukis A. Adding ezetimibe to statin therapy: latest evidence and clinical implications. Drugs Context. 2018;7:212534. doi: 10.7573/dic.212534
- Jacobson TA, Maki KC, Orringer CE, et al. National lipid association recommendations for patient-centered management of dyslipidemia: part 2. J Clin Lipidol. 2015;9(Suppl 6):S1–S122. doi: 10.1016/j.jacl.2015.09.002