Atherosclerosis and Cardiovascular Complications in People Living with HIV: A Focused Review
Abstract
:1. Introduction
2. HIV-Mediated Molecular Mechanisms
3. Role of Chronic Inflammation and Immune Activation
3.1. Inflammatory Markers and Immune Activation
3.2. Demographic Influences on Inflammation and CVD
3.3. Gut Microbiota and Systemic Inflammation
3.4. Role of Activated T Cells and Monocytes
3.5. MAP-Kinase Signaling and HIV-Related Inflammation
3.6. Perivascular Adipose Tissue and HIV-Related Atherosclerosis
4. Metabolic Impairment in PLWH
5. Role of Co-Infections
6. Role of ART
6.1. Impact on Life Expectancy and Cardiovascular Risks
6.2. Insights from Clinical Studies: SMART and START
6.3. Dyslipidemia and ART Regimens
6.4. Considerations for Switching ART Regimens
7. Treatment and Prevention
Recommendation | Population | Details | Study/Source | Efficacy |
---|---|---|---|---|
Aspirin (for prevention) | Elderly without HIV | Increased risk of serious bleeding, no significant reduction in cardiovascular disease | ASPREE study [102] | Not recommended for primary prevention |
Aspirin | Adults aged 50–59 with >10% 10-year CVD risk | Considered if willing to take for at least ten years and not at increased bleeding risk | ACC [103] and AHA Guidelines [104,105] | Grade B recommendation |
Adults aged 60–69 with >10% 10-year CVD risk | Weigh the benefits and risks; consider if there is no history of bleeding and are willing to take it for ten years | ACC and AHA Guidelines | Grade C recommendation | |
Statins | PLWH with history of vascular disease or high CVD risk | Mandatory regardless of cholesterol levels; consider PCSK9 inhibitors and/or bempedoic acid if high-risk | European AIDS Clinical Society guidelines [109] | Reduces LDL-C, beneficial |
PLWH on protease inhibitors/ritonavir | Avoid simvastatin; use atorvastatin and rosuvastatin at low doses | Clinical recommendations | Avoid due to drug–drug interactions | |
Ezetimibe | PLWH not meeting LDL-C treatment targets | Considered if statin is not well tolerated or LDL-C targets are not met | Clinical trial (Saeedi et al.) [115] | Comparable LDL-C reduction, well-tolerated |
PCSK9 inhibitors (Evolocumab) | PLWH on maximally tolerated statin therapy | Reduced LDL-C significantly over 24 weeks, safe and well-tolerated | Double-blind trial (Boccara et al.) [116] | Significant LDL-C reduction, safe |
8. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
- Joint United Nations Programme on HIV/AIDS. The Path That Ends AIDS: UNAIDS Global AIDS Update 2023; Joint United Nations Programme on HIV/AIDS: Geneva, Switzerland, 2023; Volume 6. [Google Scholar]
- Rodés, B.; Cadiñanos, J.; Esteban-Cantos, A.; Rodríguez-Centeno, J.; Arribas, J.R. Ageing with HIV: Challenges and Biomarkers. EBioMedicine 2022, 77, 103896. [Google Scholar] [CrossRef]
- Autenrieth, C.S.; Beck, E.J.; Stelzle, D.; Mallouris, C.; Mahy, M.; Ghys, P. Global and Regional Trends of People Living with HIV Aged 50 and over: Estimates and Projections for 2000–2020. PLoS ONE 2018, 13, e0207005. [Google Scholar] [CrossRef]
- Cosentino, F.; Marino, A.; Anile, L.; Moscatt, V.; Gussio, M.; Boscia, V.; Bruno, R.; Nunnari, G.; Pulvirenti, A.; Privitera, G.F.; et al. Long-Term Survivors in a Cohort of People Living with HIV Diagnosed between 1985 and 1994: Predictive Factors Associated with More Than 25 Years of Survival. Infect Dis. Rep. 2023, 15, 70–83. [Google Scholar] [CrossRef]
- Celesia, B.M.; Marino, A.; Del Vecchio, R.F.; Bruno, R.; Palermo, F.; Gussio, M.; Nunnari, G.; Cacopardo, B. Is It Safe and Cost Saving to Defer the CD4+ Cell Count Monitoring in Stable Patients on ART with More than 350 or 500 Cells/ΜL? Mediterr. J. Hematol. Infect. Dis. 2019, 11, e2019063. [Google Scholar] [CrossRef] [PubMed]
- Marino, A.; Pavone, G.; Martorana, F.; Fisicaro, V.; Motta, L.; Spampinato, S.; Celesia, B.M.; Cacopardo, B.; Vigneri, P.; Nunnari, G. Navigating the Nexus: HIV and Breast Cancer—A Critical Review. Int. J. Mol. Sci. 2024, 25, 3222. [Google Scholar] [CrossRef]
- Feinstein, M.J.; Hsue, P.Y.; Benjamin, L.A.; Bloomfield, G.S.; Currier, J.S.; Freiberg, M.S.; Grinspoon, S.K.; Levin, J.; Longenecker, C.T.; Post, W.S. Characteristics, Prevention, and Management of Cardiovascular Disease in People Living with HIV: A Scientific Statement from the American Heart Association. Circulation 2019, 140, E98–E124. [Google Scholar] [CrossRef] [PubMed]
- Corti, N.; Menzaghi, B.; Orofino, G.; Guastavigna, M.; Lagi, F.; Di Biagio, A.; Taramasso, L.; De Socio, G.V.; Molteni, C.; Madeddu, G.; et al. Risk of Cardiovascular Events in People with HIV (PWH) Treated with Integrase Strand-Transfer Inhibitors: The Debate Is Not Over; Results of the SCOLTA Study. Viruses 2024, 16, 613. [Google Scholar] [CrossRef] [PubMed]
- Cerrato, E.; Calcagno, A.; Ascenzo, F.D.; Biondi-Zoccai, G.; Mancone, M.; Marra, W.G.; Demarie, D.; Omedè, P.; Abbate, A.; Bonora, S.; et al. Cardiovascular Disease in HIV Patients: From Bench to Bedside and Backwards. Open Heart 2015, 2, e000174. [Google Scholar] [CrossRef]
- Eyawo, O.; Brockman, G.; Goldsmith, C.H.; Hull, M.W.; Lear, S.A.; Bennett, M.; Guillemi, S.; Franco-Villalobos, C.; Adam, A.; Mills, E.J.; et al. Risk of Myocardial Infarction among People Living with HIV: An Updated Systematic Review and Meta-Analysis. BMJ Open 2019, 9, e025874. [Google Scholar] [CrossRef]
- Klein, D.B.; Leyden, W.A.; Xu, L.; Chao, C.R.; Horberg, M.A.; Towner, W.J.; Hurley, L.B.; Marcus, J.L.; Quesenberry, C.P.; Silverberg, M.J. Declining Relative Risk for Myocardial Infarction Among HIV-Positive Compared With HIV-Negative Individuals With Access to Care. Clin. Infect. Dis. 2015, 60, 1278–1280. [Google Scholar] [CrossRef]
- Triant, V.A.; Lee, H.; Hadigan, C.; Grinspoon, S.K. Increased Acute Myocardial Infarction Rates and Cardiovascular Risk Factors among Patients with Human Immunodeficiency Virus Disease. J. Clin. Endocrinol. Metab. 2007, 92, 2506–2512. [Google Scholar] [CrossRef] [PubMed]
- Björkegren, J.L.M.; Lusis, A.J. Atherosclerosis: Recent Developments. Cell 2022, 185, 1630–1645. [Google Scholar] [CrossRef]
- Post, W.S.; Budoff, M.; Kingsley, L.; Palella, F.J.; Witt, M.D.; Li, X.; George, R.T.; Brown, T.T.; Jacobson, L.P. Associations between HIV Infection and Subclinical Coronary Atherosclerosis. Ann. Intern. Med. 2014, 160, 458–467. [Google Scholar] [CrossRef] [PubMed]
- Martini, S.; Ricci, E.D.; Masiello, A.; Zacà, S.; Celesia, B.M.; Ferrara, S.; Di Filippo, G.; Tartaglia, A.; Basile, R.; Angiletta, D.; et al. Evaluation of Myo-Intimal Media Thickness and Atheromatous Plaques in People Living with HIV from the Archiprevaleat Cohort vs. HIV-Negative Subjects. Biomedicines 2024, 12, 773. [Google Scholar] [CrossRef] [PubMed]
- Belgrave, K.; Shaikh, K.; Budoff, M.J. Risk of Peripheral Artery Disease in Human Immunodeficiency Virus Infected Individuals. Ann. Transl. Med. 2018, 6, S46. [Google Scholar] [CrossRef] [PubMed]
- Beckman, J.A.; Duncan, M.S.; Alcorn, C.W.; So-Armah, K.; Butt, A.A.; Goetz, M.B.; Tindle, H.A.; Sico, J.J.; Tracy, R.P.; Justice, A.C.; et al. Association of Human Immunodeficiency Virus Infection and Risk of Peripheral Artery Disease. Circulation 2018, 138, 255–265. [Google Scholar] [CrossRef]
- Roggero, R.; Robert-Hebmann, V.; Harrington, S.; Roland, J.; Vergne, L.; Jaleco, S.; Devaux, C.; Biard-Piechaczyk, M. Binding of Human Immunodeficiency Virus Type 1 Gp120 to CXCR4 Induces Mitochondrial Transmembrane Depolarization and Cytochrome C-Mediated Apoptosis Independently of Fas Signaling. J. Virol. 2001, 75, 7637–7650. [Google Scholar] [CrossRef]
- Avagimyan, A.; Pogosova, N.; Kakturskiy, L.; Sheibani, M.; Urazova, O.; Trofimenko, A.; Navasardyan, G.; Jndoyan, Z.; Abgaryan, K.; Fogacci, F.; et al. HIV-Related Atherosclerosis: State-of-the-Art-Review. Curr. Probl. Cardiol. 2023, 48, 101783. [Google Scholar] [CrossRef]
- Hijmans, J.G.; Stockelman, K.; Levy, M.; Madden Brewster, L.; Bammert, T.D.; Greiner, J.J.; Connick, E.; DeSouza, C.A. Effects of HIV-1 Gp120 and TAT-Derived Microvesicles on Endothelial Cell Function. J. Appl. Physiol. 2019, 126, 1242–1249. [Google Scholar] [CrossRef]
- Madzime, M.; Rossouw, T.M.; Theron, A.J.; Anderson, R.; Steel, H.C. Interactions of HIV and Antiretroviral Therapy With Neutrophils and Platelets. Front. Immunol. 2021, 12, 634386. [Google Scholar] [CrossRef]
- Hsue, P.Y.; Tawakol, A. Inflammation and Fibrosis in HIV: Getting to the Heart of the Matter. Circ. Cardiovasc. Imaging 2016, 9, e004427. [Google Scholar] [CrossRef] [PubMed]
- Feeney, E.R.; McAuley, N.; O’Halloran, J.A.; Rock, C.; Low, J.; Satchell, C.S.; Lambert, J.S.; Sheehan, G.J.; Mallon, P.W.G. The Expression of Cholesterol Metabolism Genes in Monocytes from HIV-Infected Subjects Suggests Intracellular Cholesterol Accumulation. J. Infect. Dis. 2013, 207, 628–637. [Google Scholar] [CrossRef] [PubMed]
- Wang, T.; Yi, R.; Green, L.A.; Chelvanambi, S.; Seimetz, M.; Clauss, M. Increased Cardiovascular Disease Risk In The HIV-Positive Population on ART: Potential Role of HIV-Nef and Tat. Cardiovasc. Pathol. 2015, 24, 279. [Google Scholar] [CrossRef] [PubMed]
- Pushkarsky, T.; Shilov, E.; Kruglova, N.; Naumann, R.; Brichacek, B.; Jennelle, L.; Sviridov, D.; Kruglov, A.; Nedospasov, S.A.; Bukrinsky, M. Short Communication: Accumulation of Neutral Lipids in Liver and Aorta of Nef-Transgenic Mice. AIDS Res. Hum. Retroviruses 2017, 33, 57–60. [Google Scholar] [CrossRef] [PubMed]
- Bernard, M.A.; Han, X.; Inderbitzin, S.; Agbim, I.; Zhao, H.; Koziel, H.; Tachado, S.D. HIV-Derived SsRNA Binds to TLR8 to Induce Inflammation-Driven Macrophage Foam Cell Formation. PLoS ONE 2014, 9, e104039. [Google Scholar] [CrossRef]
- Fülöp, T.; Herbein, G.; Cossarizza, A.; Witkowski, J.M.; Frost, E.; Dupuis, G.; Pawelec, G.; Larbi, A. Cellular Senescence, Immunosenescence and HIV. In HIV and Aging; Interdisciplinary Topics in Gerontology and Geriatrics; Karger International: Basel, Switzerland, 2016; Volume 42. [Google Scholar] [CrossRef]
- Marino, A.; Zafarana, G.; Ceccarelli, M.; Cosentino, F.; Moscatt, V.; Bruno, G.; Bruno, R.; Benanti, F.; Cacopardo, B.; Celesia, B.M. Immunological and Clinical Impact of DAA-Mediated HCV Eradication in a Cohort of HIV/HCV Coinfected Patients: Monocentric Italian Experience. Diagnostics 2021, 11, 2336. [Google Scholar] [CrossRef]
- Ghamar Talepoor, A.; Doroudchi, M. Immunosenescence in Atherosclerosis: A Role for Chronic Viral Infections. Front. Immunol. 2022, 13, 945016. [Google Scholar] [CrossRef]
- Worm, S.W.; Hsue, P. Role of Biomarkers in Predicting CVD Risk in the Setting of HIV Infection? Curr. Opin. HIV AIDS 2010, 5, 467–472. [Google Scholar] [CrossRef]
- Henning, R.J.; Greene, J.N. The Epidemiology, Mechanisms, Diagnosis and Treatment of Cardiovascular Disease in Adult Patients with HIV. Am. J. Cardiovasc. Dis. 2023, 13, 101. [Google Scholar]
- Lembas, A.; Załęski, A.; Peller, M.; Mikuła, T.; Wiercińska-Drapało, A. Human Immunodeficiency Virus as a Risk Factor for Cardiovascular Disease. Cardiovasc. Toxicol. 2024, 24, 1–14. [Google Scholar] [CrossRef]
- Hsue, P.Y.; Hunt, P.W.; Schnell, A.; Kalapus, S.C.; Hoh, R.; Ganz, P.; Martin, J.N.; Deeks, S.G. Role of Viral Replication, Antiretroviral Therapy, and Immunodeficiency in HIV-Associated Atherosclerosis. AIDS 2009, 23, 1059–1067. [Google Scholar] [CrossRef] [PubMed]
- Hanna, D.B.; Moon, J.Y.; Haberlen, S.A.; French, A.L.; Palella, F.J.; Gange, S.J.; Witt, M.D.; Kassaye, S.; Lazar, J.M.; Tien, P.C.; et al. Carotid Artery Atherosclerosis Is Associated with Mortality in HIV-Positive Women and Men. AIDS 2018, 32, 2393–2403. [Google Scholar] [CrossRef] [PubMed]
- Triant, V.A.; Perez, J.; Regan, S.; Massaro, J.M.; Meigs, J.B.; Grinspoon, S.K.; D’Agostino, R.B. Cardiovascular Risk Prediction Functions Underestimate Risk in HIV Infection. Circulation 2018, 137, 2203–2214. [Google Scholar] [CrossRef]
- Althoff, K.N.; Gange, S.J.; Klein, M.B.; Brooks, J.T.; Hogg, R.S.; Bosch, R.J.; Horberg, M.A.; Saag, M.S.; Kitahata, M.M.; Justice, A.C.; et al. Late Presentation for Human Immunodeficiency Virus Care in the United States and Canada. Clin. Infect. Dis. 2010, 50, 1512–1520. [Google Scholar] [CrossRef] [PubMed]
- Brenchley, J.M.; Price, D.A.; Schacker, T.W.; Asher, T.E.; Silvestri, G.; Rao, S.; Kazzaz, Z.; Bornstein, E.; Lambotte, O.; Altmann, D.; et al. Microbial Translocation Is a Cause of Systemic Immune Activation in Chronic HIV Infection. Nat. Med. 2006, 12, 1365–1371. [Google Scholar] [CrossRef] [PubMed]
- Tulkens, J.; Vergauwen, G.; Van Deun, J.; Geeurickx, E.; Dhondt, B.; Lippens, L.; De Scheerder, M.A.; Miinalainen, I.; Rappu, P.; De Geest, B.G.; et al. Increased Levels of Systemic LPS-Positive Bacterial Extracellular Vesicles in Patients with Intestinal Barrier Dysfunction. Gut 2020, 69, 191–193. [Google Scholar] [CrossRef]
- Vujkovic-Cvijin, I.; Dunham, R.M.; Iwai, S.; Maher, M.C.; Albright, R.G.; Broadhurst, M.J.; Hernandez, R.D.; Lederman, M.M.; Huang, Y.; Somsouk, M.; et al. Dysbiosis of the Gut Microbiota Is Associated with HIV Disease Progression and Tryptophan Catabolism. Sci. Transl. Med. 2013, 5, 193ra91. [Google Scholar] [CrossRef]
- Pan, Z.; Wu, N.; Jin, C. Intestinal Microbiota Dysbiosis Promotes Mucosal Barrier Damage and Immune Injury in HIV-Infected Patients. Can. J. Infect. Dis. Med. Microbiol. 2023, 2023, 3080969. [Google Scholar] [CrossRef]
- Isnard, S.; Royston, L.; Scott, S.C.; Mabanga, T.; Lin, J.; Fombuena, B.; Bu, S.; Berini, C.A.; Goldberg, M.S.; Finkelman, M.; et al. Translocation of Bacterial LPS Is Associated with Self-Reported Cognitive Abilities in Men Living with HIV Receiving Antiretroviral Therapy. AIDS Res. Ther. 2023, 20, 30. [Google Scholar] [CrossRef]
- Ouyang, J.; Yan, J.; Zhou, X.; Isnard, S.; Harypursat, V.; Cui, H.; Routy, J.P.; Chen, Y. Relevance of Biomarkers Indicating Gut Damage and Microbial Translocation in People Living with HIV. Front. Immunol. 2023, 14, 1173956. [Google Scholar] [CrossRef]
- Fragkou, P.C.; Moschopoulos, C.D.; Dimopoulou, D.; Triantafyllidi, H.; Birmpa, D.; Benas, D.; Tsiodras, S.; Kavatha, D.; Antoniadou, A.; Papadopoulos, A. Cardiovascular Disease and Risk Assessment in People Living with HIV: Current Practices and Novel Perspectives. Hell. J. Cardiol. 2023, 71, 42–54. [Google Scholar] [CrossRef]
- Krikke, M.; van Lelyveld, S.F.L.; Tesselaar, K.; Arends, J.E.; Hoepelman, I.M.; Visseren, F.L.J. The Role of T Cells in the Development of Cardiovascular Disease in HIV-Infected Patients. Atherosclerosis 2014, 237, 92–98. [Google Scholar] [CrossRef] [PubMed]
- Sarkar, S.; Brown, T.T. Lipid Disorders in People with HIV. In Endotext [Internet]; Feingold, K.R., Anawalt, B., Blackman, M.R., Boyce, A., Chrousos, G., Corpas, E., de Herder, W.W., Dhatariya, K., Dungan, K., Hofland, J., et al., Eds.; MDText.com, Inc.: South Dartmouth, MA, USA, 2000. [Google Scholar] [PubMed]
- Jung, S.H.; Lee, K.T. Atherosclerosis by Virus Infection—A Short Review. Biomedicines 2022, 10, 2634. [Google Scholar] [CrossRef]
- Ekabe, C.J.; Clinton, N.A.; Kehbila, J.; Franck, N.C. The Role of Inflammasome Activation in Early HIV Infection. J. Immunol. Res. 2021, 2021, 1487287. [Google Scholar] [CrossRef] [PubMed]
- Grebe, A.; Hoss, F.; Latz, E. NLRP3 Inflammasome and the IL-1 Pathway in Atherosclerosis. Circ. Res. 2018, 122, 1722–1740. [Google Scholar] [CrossRef]
- Bryk, D.; Olejarz, W.; Zapolska-Downar, D. Mitogen-Activated Protein Kinases in Atherosclerosis. Postep. Hig. Med. Dosw. 2014, 68, 10–22. [Google Scholar] [CrossRef]
- Wu, X.; Liu, Z.; Liao, W. The Involvement of Gaseous Signaling Molecules in Plant MAPK Cascades: Function and Signal Transduction. Planta 2021, 254, 127. [Google Scholar] [CrossRef] [PubMed]
- Narasimhan, P.; Liu, J.; Song, Y.S.; Massengale, J.L.; Chan, P.H. VEGF Stimulates the ERK 1/2 Signaling Pathway and Apoptosis in Cerebral Endothelial Cells after Ischemic Conditions. Stroke 2009, 40, 1467–1473. [Google Scholar] [CrossRef]
- Pache, L.; Marsden, M.D.; Teriete, P.; Portillo, A.J.; Heimann, D.; Kim, J.T.; Soliman, M.S.A.; Dimapasoc, M.; Carmona, C.; Celeridad, M.; et al. Pharmacological Activation of Non-Canonical NF-ΚB Signaling Activates Latent HIV-1 Reservoirs In Vivo. Cell Rep. Med. 2020, 1, 100037. [Google Scholar] [CrossRef]
- Avagimyan; Aznauryan, A.; Chernova, A. The Role of Viral Infection in the Mechanisms of Initiation of Atherogenesis and Destabilization of Atheroma. Cardiol. Belarus 2019, 11, 947–953. [Google Scholar]
- Hartmann, S.; Jakobus, C.; Rengstl, B.; Döring, C.; Newrzela, S.; Brodt, H.R.; Wolf, T.; Hansmann, M.L. Spindle-Shaped CD163+ Rosetting Macrophages Replace CD4 + T-Cells in HIV-Related Classical Hodgkin Lymphoma. Mod. Pathol. 2013, 26, 648–657. [Google Scholar] [CrossRef] [PubMed]
- Sluimer, J.C.; Kolodgie, F.D.; Bijnens, A.P.J.J.; Maxfield, K.; Pacheco, E.; Kutys, B.; Duimel, H.; Frederik, P.M.; van Hinsbergh, V.W.M.; Virmani, R.; et al. Thin-Walled Microvessels in Human Coronary Atherosclerotic Plaques Show Incomplete Endothelial Junctions. Relevance of Compromised Structural Integrity for Intraplaque Microvascular Leakage. J. Am. Coll. Cardiol. 2009, 53, 1517–1527. [Google Scholar] [CrossRef] [PubMed]
- Peyracchia, M.; De Lio, G.; Montrucchio, C.; Omedè, P.; d’Ettore, G.; Calcagno, A.; Vullo, V.; Cerrato, E.; Pennacchi, M.; Sardella, G.; et al. Evaluation of Coronary Features of HIV Patients Presenting with ACS: The CUORE, a Multicenter Study. Atherosclerosis 2018, 274, 218–226. [Google Scholar] [CrossRef] [PubMed]
- Hsu, D.C.; Ma, Y.F.; Hur, S.; Li, D.; Rupert, A.; Scherzer, R.; Kalapus, S.C.; Deeks, S.; Sereti, I.; Hsue, P.Y. Plasma IL-6 Levels Are Independently Associated with Atherosclerosis and Mortality in HIV-Infected Individuals on Suppressive Antiretroviral Therapy. AIDS 2016, 30, 2065–2074. [Google Scholar] [CrossRef] [PubMed]
- Subramanian, S.; Tawakol, A.; Burdo, T.H.; Abbara, S.; Wei, J.; Vijayakumar, J.; Corsini, E.; Abdelbaky, A.; Zanni, M.V.; Hoffmann, U.; et al. Arterial Inflammation in Patients with HIV. JAMA 2012, 308, 379–386. [Google Scholar] [CrossRef] [PubMed]
- Lagathu, C.; Béréziat, V.; Gorwood, J.; Fellahi, S.; Bastard, J.P.; Vigouroux, C.; Boccara, F.; Capeau, J. Metabolic Complications Affecting Adipose Tissue, Lipid and Glucose Metabolism Associated with HIV Antiretroviral Treatment. Expert. Opin. Drug Saf. 2019, 18, 829–840. [Google Scholar] [CrossRef]
- Masenga, S.K.; Elijovich, F.; Koethe, J.R.; Hamooya, B.M.; Heimburger, D.C.; Munsaka, S.M.; Laffer, C.L.; Kirabo, A. Hypertension and Metabolic Syndrome in Persons with HIV. Curr. Hypertens. Rep. 2020, 22, 78. [Google Scholar] [CrossRef]
- Aurpibul, L.; Namwongprom, S.; Sudjaritruk, T.; Ounjaijean, S. Metabolic Syndrome, Biochemical Markers, and Body Composition in Youth Living with Perinatal HIV Infection on Antiretroviral Treatment. PLoS ONE 2020, 15, e0230707. [Google Scholar] [CrossRef]
- Scherzer, R.; Heymsfield, S.B.; Lee, D.; Powderly, W.G.; Tien, P.C.; Bacchetti, P.; Shlipak, M.G.; Grunfeld, C. Decreased Limb Muscle and Increased Central Adiposity Are Associated with 5-Year All-Cause Mortality in HIV Infection. AIDS 2011, 25, 1405–1414. [Google Scholar] [CrossRef]
- Srinivasa, S.; Fitch, K.V.; Torriani, M.; Zanni, M.V.; Defilippi, C.; Christenson, R.; Maehler, P.; Looby, S.E.; Lo, J.; Grinspoon, S.K. Relationship of Visceral and Subcutaneous Adipose Depots to Markers of Arterial Injury and Inflammation among Individuals with HIV. AIDS 2019, 33, 229–236. [Google Scholar] [CrossRef] [PubMed]
- Palella, F.J.; McKibben, R.; Post, W.S.; Li, X.; Budoff, M.; Kingsley, L.; Witt, M.D.; Jacobson, L.P.; Brown, T.T. Anatomic Fat Depots and Coronary Plaque among Human Immunodeficiency Virus-Infected and Uninfected Men in the Multicenter AIDS Cohort Study. Open Forum Infect. Dis. 2016, 3, ofw098. [Google Scholar] [CrossRef] [PubMed]
- Zicari, S.; Sessa, L.; Cotugno, N.; Ruggiero, A.; Morrocchi, E.; Concato, C.; Rocca, S.; Zangari, P.; Manno, E.C.; Palma, P. Immune Activation, Inflammation, and Non-AIDS Co-Morbidities in HIV-Infected Patients under Long-Term ART. Viruses 2019, 11, 200. [Google Scholar] [CrossRef]
- Márquez, M.; Romero-Cores, P.; Montes-Oca, M.; Martín-Aspas, A.; Soto-Cárdenas, M.J.; Guerrero, F.; Fernández-Gutiérrez, C.; Girón-González, J.A. Immune Activation Response in Chronic HIV-Infected Patients: Influence of Hepatitis C Virus Coinfection. PLoS ONE 2015, 10, e0119568. [Google Scholar] [CrossRef]
- Maidji, E.; Somsouk, M.; Rivera, J.M.; Hunt, P.W.; Stoddart, C.A. Replication of CMV in the Gut of HIV-Infected Individuals and Epithelial Barrier Dysfunction. PLoS Pathog. 2017, 13, e1006202. [Google Scholar] [CrossRef]
- Henrich, T.J.; Hobbs, K.S.; Hanhauser, E.; Scully, E.; Hogan, L.E.; Robles, Y.P.; Leadabrand, K.S.; Marty, F.M.; Palmer, C.D.; Jost, S.; et al. Human Immunodeficiency Virus Type 1 Persistence Following Systemic Chemotherapy for Malignancy. J. Infect. Dis. 2017, 216, 254–262. [Google Scholar] [CrossRef]
- Gianella, S.; Anderson, C.M.; Var, S.R.; Oliveira, M.F.; Lada, S.M.; Vargas, M.V.; Massanella, M.; Little, S.J.; Richman, D.D.; Strain, M.C.; et al. Replication of Human Herpesviruses Is Associated with Higher HIV DNA Levels during Antiretroviral Therapy Started at Early Phases of HIV Infection. J. Virol. 2016, 90, 3944–3952. [Google Scholar] [CrossRef] [PubMed]
- Bedimo, R.; Abodunde, O. Metabolic and Cardiovascular Complications in HIV/HCV-Co-Infected Patients. Curr. HIV/AIDS Rep. 2016, 13, 328–339. [Google Scholar] [CrossRef]
- Marino, A.; Caltabiano, E.; Zagami, A.; Onorante, A.; Zappalà, C.; Locatelli, M.E.; Pampaloni, A.; Scuderi, D.; Bruno, R.; Cacopardo, B. Rapid Emergence of Cryptococcal Fungemia, Mycobacterium Chelonae Vertebral Osteomyelitis and Gastro Intestinal Stromal Tumor in a Young HIV Late Presenter: A Case Report. BMC Infect. Dis. 2018, 18, 693. [Google Scholar] [CrossRef]
- Maggi, P.; Maserati, R.; Antonelli, G. Atherosclerosis in HIV Patients: A New Face for an Old Disease? AIDS Rev. 2006, 8, 204–209. [Google Scholar] [PubMed]
- Maggi, P.; Perilli, F.; Lillo, A.; Carito, V.; Epifani, G.; Bellacosa, C.; Pastore, G.; Regina, G. An Ultrasound-Based Comparative Study on Carotid Plaques in HIV-Positive Patients vs. Atherosclerotic and Arteritis Patients: Atherosclerotic or Inflammatory Lesions? Coron. Artery Dis. 2007, 18, 23–29. [Google Scholar] [CrossRef] [PubMed]
- Soliman, E.; Sharma, S.; Arastéh, K.; Wohl, D.; Achhra, A.; Tambussi, G.; O’Connor, J.; Stein, J.; Duprez, D.; Neaton, J.; et al. Baseline Cardiovascular Risk in the INSIGHT Strategic Timing of AntiRetroviral Treatment (START) Trial. HIV Med. 2015, 16, 46–54. [Google Scholar] [CrossRef]
- Byonanebye, D.M.; Polizzotto, M.N.; Begovac, J.; Grabmeier-Pfistershammer, K.; Abela, I.; Castagna, A.; de Wit, S.; Mussini, C.; Vehreschild, J.J.; d’Arminio Monforte, A.; et al. Incidence of Dyslipidemia in People with HIV Who Are Treated with Integrase Inhibitors versus Other Antiretroviral Agents. AIDS 2021, 35, 869–882. [Google Scholar] [CrossRef]
- Boccara, F.; Ghislain, M.; Meyer, L.; Goujard, C.; Le May, C.; Vigouroux, C.; Bastard, J.P.; Fellahi, S.; Capeau, J.; Cohen, A.; et al. Impact of Protease Inhibitors on Circulating PCSK9 Levels in HIV-Infected Antiretroviral-Naive Patients from an Ongoing Prospective Cohort. AIDS 2017, 31, 2367–2376. [Google Scholar] [CrossRef]
- Alvi, R.M.; Neilan, A.M.; Tariq, N.; Awadalla, M.; Afshar, M.; Banerji, D.; Rokicki, A.; Mulligan, C.; Triant, V.A.; Zanni, M.V.; et al. Protease Inhibitors and Cardiovascular Outcomes in Patients With HIV and Heart Failure. J. Am. Coll. Cardiol. 2018, 72, 518–530. [Google Scholar] [CrossRef] [PubMed]
- Bruder-Nascimento, T.; Kress, T.C.; Kennard, S.; Belin de Chantemèle, E.J. Hiv Protease Inhibitor Ritonavir Impairs Endothelial Function via Reduction in Adipose Mass and Endothelial Leptin Receptor-Dependent Increases in Nadph Oxidase 1 (Nox1), c-c Chemokine Receptor Type 5 (Ccr5), and Inflammation. J. Am. Heart Assoc. 2020, 9, e018074. [Google Scholar] [CrossRef] [PubMed]
- Ryom, L.; Lundgren, J.D.; El-Sadr, W.; Reiss, P.; Kirk, O.; Law, M.; Phillips, A.; Weber, R.; Fontas, E.; d’Arminio Monforte, A.; et al. Cardiovascular Disease and Use of Contemporary Protease Inhibitors: The D:A:D International Prospective Multicohort Study. Lancet HIV 2018, 5, e291–e300. [Google Scholar] [CrossRef]
- Martini, S.; Pisaturo, M.; Russo, A.; Palamone, M.G.; Russo, M.T.; Zollo, V.; Maggi, P.; Coppola, N. Evaluation of Lipid Profile and Intima Media Thickness in Antiretroviral-Experienced HIV-Infected Patients Treated with Protease Inhibitor-Based Regimens versus Protease Inhibitor-Sparing Regimens. Pathogens 2023, 12, 925. [Google Scholar] [CrossRef] [PubMed]
- Hatleberg, C.I.; Ryom, L.; Sabin, C. Cardiovascular Risks Associated with Protease Inhibitors for the Treatment of HIV. Expert. Opin. Drug Saf. 2021, 20, 1351–1366. [Google Scholar] [CrossRef]
- Pistarà, E.; Raddusa, M.S.P.; Bellocchi, B.; Campanella, E.; Moscatt, V.; Ceccarelli, M.; Celesia, B.M. Management Del Paziente HIV Positivo Con Infarto Del Miocardio: Interazioni Farmacologiche e Ottimizzazione Della Terapia. J. HIV Ageing 2022, 7, 37–40. [Google Scholar] [CrossRef]
- Molina, J.M.; Clotet, B.; van Lunzen, J.; Lazzarin, A.; Cavassini, M.; Henry, K.; Kulagin, V.; Givens, N.; de Oliveira, C.F.; Brennan, C. Once-Daily Dolutegravir versus Darunavir plus Ritonavir for Treatment-Naive Adults with HIV-1 Infection (FLAMINGO): 96 Week Results from a Randomised, Open-Label, Phase 3b Study. Lancet HIV 2015, 2, e127–e136. [Google Scholar] [CrossRef]
- Deutschmann, E.; Bucher, H.C.; Jaeckel, S.; Gibbons, S.; McAllister, K.; Scherrer, A.U.; Braun, D.L.; Cavassini, M.; Hachfeld, A.; Calmy, A.; et al. Prevalence of Potential Drug-Drug Interactions in Patients of the Swiss HIV Cohort Study in the Era of HIV Integrase Inhibitors. Clin. Infect. Dis. 2021, 73, e2145–e2152. [Google Scholar] [CrossRef]
- Venter, W.D.F.; Sokhela, S.; Simmons, B.; Moorhouse, M.; Fairlie, L.; Mashabane, N.; Serenata, C.; Akpomiemie, G.; Masenya, M.; Qavi, A.; et al. Dolutegravir with Emtricitabine and Tenofovir Alafenamide or Tenofovir Disoproxil Fumarate versus Efavirenz, Emtricitabine, and Tenofovir Disoproxil Fumarate for Initial Treatment of HIV-1 Infection (ADVANCE): Week 96 Results from a Randomised, Phase 3, Non-Inferiority Trial. Lancet HIV 2020, 7, e666–e676. [Google Scholar] [CrossRef]
- Bansi-Matharu, L.; Phillips, A.; Oprea, C.; Grabmeier-Pfistershammer, K.; Günthard, H.F.; De Wit, S.; Guaraldi, G.; Vehreschild, J.J.; Wit, F.; Law, M.; et al. Contemporary Antiretrovirals and Body-Mass Index: A Prospective Study of the RESPOND Cohort Consortium. Lancet HIV 2021, 8, e711–e722. [Google Scholar] [CrossRef] [PubMed]
- O’Halloran, J.A.; Sahrmann, J.; Parra-Rodriguez, L.; Vo, D.T.; Butler, A.M.; Olsen, M.A.; Powderly, W.G. Integrase Strand Transfer Inhibitors Are Associated with Incident Diabetes Mellitus in People with Human Immunodeficiency Virus. Clin. Infect. Dis. 2022, 75, 2060–2065. [Google Scholar] [CrossRef] [PubMed]
- Byonanebye, D.M.; Polizzotto, M.N.; Neesgaard, B.; Sarcletti, M.; Matulionyte, R.; Braun, D.L.; Castagna, A.; de Wit, S.; Wit, F.; Fontas, E.; et al. Incidence of Hypertension in People with HIV Who Are Treated with Integrase Inhibitors versus Other Antiretroviral Regimens in the RESPOND Cohort Consortium. HIV Med. 2022, 23, 895–910. [Google Scholar] [CrossRef] [PubMed]
- Taramasso, L.; Tatarelli, P.; Ricci, E.; Madeddu, G.; Menzaghi, B.; Squillace, N.; De Socio, G.V.; Martinelli, C.; Gulminetti, R.; Maggi, P.; et al. Improvement of Lipid Profile after Switching from Efavirenz or Ritonavir-Boosted Protease Inhibitors to Rilpivirine or Once-Daily Integrase Inhibitors: Results from a Large Observational Cohort Study (SCOLTA). BMC Infect. Dis. 2018, 18, 357. [Google Scholar] [CrossRef]
- Mallon, P.W.G.; Brunet, L.; Fusco, J.S.; Prajapati, G.; Beyer, A.; Fusco, G.P.; Wohlfeiler, M.B. Lipid Changes After Switch From TDF to TAF in the OPERA Cohort: LDL Cholesterol and Triglycerides. Open Forum Infect. Dis. 2022, 9, ofab621. [Google Scholar] [CrossRef] [PubMed]
- Lacey, A.; Tinago, W.; Power, N.R.; Alvarez, E.; Macken, A.J.; Sheehan, G.; Lambert, J.S.; Cotter, A.G.; Mallon, P.W.G. Investigating the Effect of Antiretroviral Switch to Tenofovir Alafenamide on Lipid Profiles in People Living with HIV within the UCD ID Cohort. J. Virus Erad. 2018, 4, 11. [Google Scholar] [CrossRef]
- Taramasso, L.; Berruti, M.; Briano, F.; Di Biagio, A. The Switch from Tenofovir Disoproxil Fumarate to Tenofovir Alafenamide Determines Weight Gain in Patients on Rilpivirine-Based Regimen. AIDS 2020, 34, 877–881. [Google Scholar] [CrossRef]
- Sax, P.E.; Erlandson, K.M.; Lake, J.E.; McComsey, G.A.; Orkin, C.; Esser, S.; Brown, T.T.; Rockstroh, J.K.; Wei, X.; Carter, C.C.; et al. Weight Gain Following Initiation of Antiretroviral Therapy: Risk Factors in Randomized Comparative Clinical Trials. Clin. Infect. Dis. 2020, 71, 1379–1389. [Google Scholar] [CrossRef]
- Huhn, G.D.; Shamblaw, D.J.; Baril, J.G.; Hsue, P.Y.; Mills, B.L.; Nguyen-Cleary, T.; McCallister, S.; Das, M. Atherosclerotic Cardiovascular Disease Risk Profile of Tenofovir Alafenamide versus Tenofovir Disoproxil Fumarate. Open Forum Infect. Dis. 2020, 7, ofz472. [Google Scholar] [CrossRef] [PubMed]
- Myerson, M.; Malvestutto, C.; Aberg, J.A. Management of Lipid Disorders in Patients Living with HIV. J. Clin. Pharmacol. 2015, 55, 957–974. [Google Scholar] [CrossRef]
- Rokx, C.; Verbon, A.; Rijnders, B.J.A. Short Communication: Lipids and Cardiovascular Risk after Switching HIV-1 Patients on Nevirapine and Emtricitabine/Tenofovir-DF to Rilpivirine/Emtricitabine/Tenofovir-DF. AIDS Res. Hum. Retroviruses 2015, 31, 363–367. [Google Scholar] [CrossRef] [PubMed]
- Molina, J.M.; Squires, K.; Sax, P.E.; Cahn, P.; Lombaard, J.; DeJesus, E.; Lai, M.T.; Xu, X.; Rodgers, A.; Lupinacci, L.; et al. Doravirine versus Ritonavir-Boosted Darunavir in Antiretroviral-Naive Adults with HIV-1 (DRIVE-FORWARD): 48-Week Results of a Randomised, Double-Blind, Phase 3, Non-Inferiority Trial. Lancet HIV 2018, 5, e211–e220. [Google Scholar] [CrossRef] [PubMed]
- Orkin, C.; Squires, K.E.; Molina, J.M.; Sax, P.E.; Wong, W.W.; Sussmann, O.; Kaplan, R.; Lupinacci, L.; Rodgers, A.; Xu, X.; et al. Doravirine/Lamivudine/Tenofovir Disoproxil Fumarate Is Non-Inferior to Efavirenz/Emtricitabine/Tenofovir Disoproxil Fumarate in Treatment-Naive Adults with Human Immunodeficiency Virus-1 Infection: Week 48 Results of the DRIVE-AHEAD Trial. Clin. Infect. Dis. 2019, 68, 535–544. [Google Scholar] [CrossRef]
- Kumar, P.; Johnson, M.; Molina, J.M.; Rizzardini, G.; Cahn, P.; Bickel, M.; Wan, H.; Xu, Z.J.; Morais, C.; Sklar, P.; et al. Switching to DOR/3TC/TDF Maintains HIV-1 Virologic Suppression through Week 144 in the DRIVE-SHIFT Trial. J. Acquir. Immune Defic. Syndr. 2021, 87, 801–805. [Google Scholar] [CrossRef]
- Maggi, P.; Ricci, E.D.; Martinelli, C.V.; De Socio, G.V.; Squillace, N.; Molteni, C.; Masiello, A.; Orofino, G.; Menzaghi, B.; Bellagamba, R.; et al. Lipids and Transaminase in Antiretroviral-Treatment-Experienced People Living with HIV, Switching to a Doravirine-Based vs. a Rilpivirine-Based Regimen: Data from a Real-Life Setting. Viruses 2023, 15, 1612. [Google Scholar] [CrossRef]
- De Socio, G.V.; Ricci, E.; Parruti, G.; Calza, L.; Maggi, P.; Celesia, B.M.; Orofino, G.; Madeddu, G.; Martinelli, C.; Menzaghi, B.; et al. Statins and Aspirin Use in HIV-Infected People: Gap between European AIDS Clinical Society Guidelines and Clinical Practice: The Results from HIV-HY Study. Infection 2016, 44, 589–597. [Google Scholar] [CrossRef]
- McNeil, J.J.; Woods, R.L.; Nelson, M.R.; Reid, C.M.; Kirpach, B.; Wolfe, R.; Storey, E.; Shah, R.C.; Lockery, J.E.; Tonkin, A.M.; et al. Effect of Aspirin on Disability-Free Survival in the Healthy Elderly. N. Engl. J. Med. 2018, 379, 1499–1508. [Google Scholar] [CrossRef]
- Arnett, D.K.; Blumenthal, R.S.; Albert, M.A.; Buroker, A.B.; Goldberger, Z.D.; Hahn, E.J.; Himmelfarb, C.D.; Khera, A.; Lloyd-Jones, D.; McEvoy, J.W.; et al. 2019 ACC/AHA Guideline on the Primary Prevention of Cardiovascular Disease: A Report of the American College of Cardiology/American Heart Association Task Force on Clinical Practice Guidelines. J. Am. Coll. Cardiol. 2019, 74, e177–e232. [Google Scholar] [CrossRef]
- Hira, R.S.; Gosch, K.L.; Kazi, D.S.; Yeh, R.W.; Kataruka, A.; Maddox, T.M.; Shah, T.; Jneid, H.; Bhatt, D.L.; Virani, S.S. Potential Impact of the 2019 ACC/AHA Guidelines on the Primary Prevention of Cardiovascular Disease Recommendations on the Inappropriate Routine Use of Aspirin and Aspirin Use Without a Recommended Indication for Primary Prevention of Cardiovascular Disease in Cardiology Practices: Insights From the NCDR PINNACLE Registry. Circ. Cardiovasc. Qual. Outcomes 2022, 15, E007979. [Google Scholar] [CrossRef]
- Cofer, L.B.; Barrett, T.J.; Berger, J.S. Aspirin for the Primary Prevention of Cardiovascular Disease: Time for a Platelet-Guided Approach. Arterioscler. Thromb. Vasc. Biol. 2022, 42, 1207–1216. [Google Scholar] [CrossRef]
- Avgousti, H.; Feinstein, M.J. Prevention and Treatment of Cardiovascular Disease in HIV: Practical Insights in an Evolving Field. Top. Antivir. Med. 2023, 31, 559–565. [Google Scholar] [PubMed]
- O’Brien, M.P.; Hunt, P.W.; Kitch, D.W.; Klingman, K.; Stein, J.H.; Funderburg, N.T.; Berger, J.S.; Tebas, P.; Clagett, B.; Moisi, D.; et al. A Randomized Placebo Controlled Trial of Aspirin Effects on Immune Activation in Chronically Human Immunodeficiency Virus-Infected Adults on Virologically Suppressive Antiretroviral Therapy. Open Forum Infect. Dis. 2017, 4, ofw278. [Google Scholar] [CrossRef] [PubMed]
- Marcantoni, E.; Garshick, M.S.; Schwartz, T.; Ratnapala, N.; Cambria, M.; Dann, R.; O’Brien, M.; Heguy, A.; Berger, J.S. Antiplatelet Effects of Clopidogrel Vs Aspirin in Virologically Controlled HIV: A Randomized Controlled Trial. JACC Basic Transl. Sci. 2022, 7, 1086–1097. [Google Scholar] [CrossRef]
- EACS Guidelines|EACSociety. Available online: https://www.eacsociety.org/guidelines/eacs-guidelines/ (accessed on 13 March 2024).
- Feinstein, M.J.; Achenbach, C.J.; Stone, N.J.; Lloyd-Jones, D.M. A Systematic Review of the Usefulness of Statin Therapy in HIV-Infected Patients. Am. J. Cardiol. 2015, 115, 1760–1766. [Google Scholar] [CrossRef] [PubMed]
- Funderburg, N.T.; Jiang, Y.; Debanne, S.M.; Labbato, D.; Juchnowski, S.; Ferrari, B.; Clagett, B.; Robinson, J.; Lederman, M.M.; McComsey, G.A. Rosuvastatin Reduces Vascular Inflammation and T-Cell and Monocyte Activation in HIV-Infected Subjects on Antiretroviral Therapy. J. Acquir. Immune Defic. Syndr. 2015, 68, 396–404. [Google Scholar] [CrossRef] [PubMed]
- Longenecker, C.T.; Eckard, A.R.; McComsey, G.A. Statins to Improve Cardiovascular Outcomes in Treated HIV Infection. Curr. Opin. Infect. Dis. 2016, 29, 1–9. [Google Scholar] [CrossRef]
- Maggi, P.; De Socio, G.V.; Cicalini, S.; D’Abbraccio, M.; Dettorre, G.; Di Biagio, A.; Martinelli, C.; Nunnari, G.; Rusconi, S.; Sighinolfi, L.; et al. Statins and Aspirin in the Prevention of Cardiovascular Disease among HIV-Positive Patients between Controversies and Unmet Needs: Review of the Literature and Suggestions for a Friendly Use. AIDS Res. Ther. 2019, 16, 11. [Google Scholar] [CrossRef]
- Grinspoon, S.K.; Fitch, K.V.; Zanni, M.V.; Fichtenbaum, C.J.; Umbleja, T.; Aberg, J.A.; Overton, E.T.; Malvestutto, C.D.; Bloomfield, G.S.; Currier, J.S.; et al. Pitavastatin to Prevent Cardiovascular Disease in HIV Infection. N. Engl. J. Med. 2023, 389, 687–699. [Google Scholar] [CrossRef]
- Saeedi, R.; Johns, K.; Frohlich, J.; Bennett, M.T.; Bondy, G. Lipid Lowering Efficacy and Safety of Ezetimibe Combined with Rosuvastatin Compared with Titrating Rosuvastatin Monotherapy in HIV-Positive Patients. Lipids Health Dis. 2015, 14, 57. [Google Scholar] [CrossRef] [PubMed]
- Boccara, F.; Kumar, P.N.; Caramelli, B.; Calmy, A.; López, J.A.G.; Bray, S.; Cyrille, M.; Rosenson, R.S.; Baker, D.; Bloch, M.; et al. Evolocumab in HIV-Infected Patients With Dyslipidemia: Primary Results of the Randomized, Double-Blind BEIJERINCK Study. J. Am. Coll. Cardiol. 2020, 75, 2570–2584. [Google Scholar] [CrossRef] [PubMed]
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content. |
© 2024 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Paternò Raddusa, M.S.; Marino, A.; Celesia, B.M.; Spampinato, S.; Giarratana, C.; Venanzi Rullo, E.; Cacopardo, B.; Nunnari, G. Atherosclerosis and Cardiovascular Complications in People Living with HIV: A Focused Review. Infect. Dis. Rep. 2024, 16, 846-863. https://doi.org/10.3390/idr16050066
Paternò Raddusa MS, Marino A, Celesia BM, Spampinato S, Giarratana C, Venanzi Rullo E, Cacopardo B, Nunnari G. Atherosclerosis and Cardiovascular Complications in People Living with HIV: A Focused Review. Infectious Disease Reports. 2024; 16(5):846-863. https://doi.org/10.3390/idr16050066
Chicago/Turabian StylePaternò Raddusa, Michele Salvatore, Andrea Marino, Benedetto Maurizio Celesia, Serena Spampinato, Carmen Giarratana, Emmanuele Venanzi Rullo, Bruno Cacopardo, and Giuseppe Nunnari. 2024. "Atherosclerosis and Cardiovascular Complications in People Living with HIV: A Focused Review" Infectious Disease Reports 16, no. 5: 846-863. https://doi.org/10.3390/idr16050066