Immune activation and cardiovascular disease in chronic HIV infection

Current Opinion in HIV and AIDS

Volumn 11, Issue 2, 2016, Pages 216-225

  Longenecker, Chris T ^a,b   Sullivan, Claire ^a,b   Baker, Jason V ^c,d  

^a University Hospitals Harrington Heart and Vascular Institute   (United States)

^b CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c HENNEPIN COUNTY MEDICAL CENTER   (United States)

^d UNIVERSITY OF MINNESOTA   (United States)

Author keywords

cardiovascular disease; HIV; immune activation

Indexed keywords

ANTI HUMAN IMMUNODEFICIENCY VIRUS AGENT;

ADAPTIVE IMMUNITY; ANTIVIRAL THERAPY; ATHEROSCLEROSIS; CARDIOVASCULAR DISEASE; CARDIOVASCULAR RISK; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; INNATE IMMUNITY; MACROPHAGE; MONOCYTE; PATHOGENESIS; PRIORITY JOURNAL; RANDOMIZED CONTROLLED TRIAL (TOPIC); REVIEW; T LYMPHOCYTE ACTIVATION; CARDIOVASCULAR DISEASES; COMPLICATION; HIV INFECTIONS; IMMUNOLOGY; RISK FACTOR;

CARDIOVASCULAR DISEASES; HIV INFECTIONS; HUMANS; RISK FACTORS;

EID: 84957436810     PISSN: 1746630X     EISSN: 17466318     Source Type: Journal    
DOI: 10.1097/COH.0000000000000227     Document Type: Review

References (90)

1. Henry K, Melroe H, Huebsch J, et al. Severe premature coronary artery disease with protease inhibitors. Lancet 1998; 351: 1328.
2. So-Armah K, Freiberg MS. Cardiovascular disease risk in an aging HIV population: not just a question of biology. Curr Opin HIV AIDS 2014; 9: 346-354.
3. Longenecker CT, Triant VA. Initiation of antiretroviral therapy at high CD4 cell counts: does it reduce the risk of cardiovascular disease? Curr Opin HIV AIDS 2014; 9: 54-62.
4. Freiberg MS, Chang CC, Kuller LH, et al. HIV infection and the risk of acute myocardial infarction. JAMA Intern Med 2013; 1-9.
5. Sico JJ, Chang CC, So-Armah K, et al. HIV status and the risk of ischemic stroke among men. Neurology 2015; 84: 1933-1940.
6. Butt AA, Chang CC, Kuller L, et al. Risk of heart failure with human immunodeficiency virus in the absence of prior diagnosis of coronary heart disease. Arch Intern Med 2011; 171: 737-743.
7. Tseng ZH, Secemsky EA, Dowdy D, et al. Sudden cardiac death in patients with human immunodeficiency virus infection. J Am Coll Cardiol 2012; 59: 1891-1896.
8. Womack JA, Chang CC, So-Armah KA, et al. HIV infection and cardiovascular disease in women. J Am Heart Assoc 2014; 3: e001035.
9. Post WS, Budoff M, Kingsley L, et al. Associations between HIV infection and subclinical coronary atherosclerosis. Ann Intern Med 2014; 160: 458-467.
10. Zanni MV, Abbara S, Lo J, et al. Increased coronary atherosclerotic plaque vulnerability by coronary computed tomography angiography in HIV-infected Men. AIDS 2013; 27: 1263-1272.
11. Thiara DK, Liu CY, Raman F, et al. Abnormal myocardial function is related to myocardial steatosis and diffuse myocardial fibrosis in HIV-infected adults. J Infect Dis 2015; 212: 1544-1551.
12. Holloway CJ, Ntusi N, Suttie J, et al. Comprehensive cardiac magnetic resonance imaging and spectroscopy reveal a high burden of myocardial disease in HIV patients. Circulation 2013; 128: 814-822.
13. Ingle SM, May MT, Gill MJ, et al. Impact of risk factors for specific causes of death in the first and subsequent years of antiretroviral therapy among HIVinfected patients. Clin Infect Dis 2014; 59: 287-297.
14. Rasmussen LD, Helleberg M, May MT, et al. Myocardial infarction among Danish HIV-infected individuals: population-attributable fractions associated with smoking. Clin Infect Dis 2015; 60: 1415-1423.
15. Klein DB, Leyden WA, Xu L, et al. 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.
16. Armah KA, Chang CC, Baker JV, et al. Prehypertension, hypertension, and the risk of acute myocardial infarction in HIV-infected and -uninfected veterans. Clin Infect Dis 2014; 58: 121-129.
17. Krishnan S, Schouten JT, Atkinson B, et al. Changes in metabolic syndrome status after initiation of antiretroviral therapy. J Acquir Immune Defic Syndr 2015; 68: 73-80.
18. Tien PC, SchneiderMF, Cox C, et al. Association of HIV infection with incident diabetes mellitus: impact of using hemoglobin A1C as a criterion for diabetes. J Acquir Immune Defic Syndr 2012; 61: 334-340.
19. Srinivasa S, Grinspoon SK. Metabolic and body composition effects of newer antiretrovirals in HIV-infected patients. Eur J Endocrinol 2014; 170: R185-202.
20. Sodora DL, Silvestri G. Immune activation and AIDS pathogenesis. AIDS 2008; 22: 439-446.
21. Lichtenstein KA, Armon C, Buchacz K, et al. Low CD4+ T cell count is a risk factor for cardiovascular disease events in the HIV outpatient study. Clin Infect Dis 2010; 51: 435-447.
22. Hsue PY, Deeks SG, Hunt PW. Immunologic basis of cardiovascular disease in HIV-infected adults. J Infect Dis 2012; 205 (Suppl 3): S375-382.
23. Sabin CA, Ryom L, De Wit S, et al. Associations between immune depression and cardiovascular events in HIV infection. AIDS 2013; 27: 2735-2748.
24. Silverberg MJ, Leyden WA, Xu L, et al. Immunodeficiency and risk of myocardial infarction among HIV-positive individuals with access to care. J Acquir Immune Defic Syndr 2014; 65: 160-166.
25. Baker JV, Peng G, Rapkin J, et al. CD4+ count and risk of non-AIDS diseases following initial treatment for HIV infection. AIDS 2008; 22: 841-848.
26. Freiberg MS, Chang CC, Kuller LH, et al. HIV infection and the risk of acute myocardial infarction. JAMA Intern Med 2013; 173: 614-622.
27. Triant VA, Regan S, Lee H, et al. Association of immunologic and virologic factors with myocardial infarction rates in a US healthcare system. J Acquir Immune Defic Syndr 2010; 55: 615-619.
28. Lang S, Mary-Krause M, Simon A, et al. HIV replication and immune status are independent predictors of the risk of myocardial infarction in HIV-infected individuals. Clin Infect Dis 2012; 55: 600-607.
29. Group ISS. Initiation of Antiretroviral Therapy in Early Asymptomatic HIV Infection. N Engl J Med 2015; 373: 795-807.
30. Papagno L, Spina CA, Marchant A, et al. Immune activation and CD8+ T-cell differentiation towards senescence in HIV-1 infection. PLoS Biol 2004; 2: E20.
31. 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: 243-253.
32. Kaplan RC, Sinclair E, Landay AL, et al. T cell activation and senescence predict subclinical carotid artery disease in HIV-infected women. J Infect Dis 2011; 203: 452-463.
33. Hunt PW, Brenchley J, Sinclair E, et al. Relationship between T cell activation and CD4+ T cell count in HIV-seropositive individuals with undetectable plasma HIV RNA levels in the absence of therapy. J Infect Dis 2008; 197: 126-133.
34. Naeger DM, Martin JN, Sinclair E, et al. Cytomegalovirus-specific T cells persist at very high levels during long-term antiretroviral treatment of HIV disease. PLoS One 2010; 5: e8886.
35. Hsue PY, Hunt PW, Sinclair E, et al. Increased carotid intima-media thickness in HIV patients is associated with increased cytomegalovirus-specific T-cell responses. AIDS 2006; 20: 2275-2283.
36. Parrinello CM, Sinclair E, Landay AL, et al. Cytomegalovirus immunoglobulin G antibody is associated with subclinical carotid artery disease among HIVinfected women. J Infect Dis 2012; 205: 1788-1796.
37. Sacre K, Hunt PW, Hsue PY, et al. A role for cytomegalovirusspecific CD4+CX3CR1+ T cells and cytomegalovirus-induced T-cell immunopathology in HIV-associated atherosclerosis. AIDS 2012; 26: 805-814.
38. Huck DM, Okello E, Mirembe G, et al. Role of natural auto-antibodies among Ugandans with rheumatic heart disease and HIV.. Orland, FL: American Heart Association Scientific Sessions; 2015.
39. Libby P, Ridker PM, Hansson GK. Inflammation in atherosclerosis: from pathophysiology to practice. J Am Coll Cardiol 2009; 54: 2129-2138.
40. 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: 1788-1795.
41. Armah KA, McGinnis K, Baker J, et al. HIV status, burden of comorbid disease and biomarkers of inflammation, altered coagulation and monocyte activation. Clin Infect Dis 2012; 55: 126-136.
42. Crowe SM, Westhorpe CL, Mukhamedova N, et al. The macrophage: the intersection between HIV infection and atherosclerosis. J Leukoc Biol 2010; 87: 589-598.
43. Martin GE, Gouillou M, Hearps AC, et al. Age-associated changes in monocyte and innate immune activation markers occur more rapidly in HIV infected women. PLoS One 2013; 8: e55279.
44. Funderburg NT, Zidar DA, Shive C, et al. Shared monocyte subset phenotypes in HIV-1 infection and in uninfected subjects with acute coronary syndrome. Blood 2012; 120: 4599-4608.
45. Hearps AC, Maisa A, Cheng WJ, et al. HIV infection induces age-related changes to monocytes and innate immune activation in young men that persist despite combination antiretroviral therapy. AIDS 2012; 26: 843-853.
46. Scherberich JE, Nockher WA. CD14++ monocytes, CD14+/CD16+ subset and soluble CD14 as biological markers of inflammatory systemic diseases and monitoring immunosuppressive therapy. Clin Chem Lab Med 1999; 37: 209-213.
47. Wilson EM, Singh A, Hullsiek KH, et al. Monocyte activation phenotypes are associated with biomarkers of inflammation and coagulation in chronic HIV infection. J Infect Dis 2014; 210: 1396-1406.
48. +DR++ monocytes are a major source of TNF. J Immunol 2002; 168: 3536-3542.
49. Ellery PJ, Tippett E, Chiu YL, et al. The CD16+ monocyte subset is more permissive to infection and preferentially harbors HIV-1 in vivo. J Immunol 2007; 178: 6581-6589.
50. Baker JV, Huppler Hullsiek K, Singh A, et al. Immunologic predictors of coronary artery calcium progression in a contemporary HIV cohort. AIDS 2014; 28.
51. Ziegler-Heitbrock L. The CD14+ CD16+ blood monocytes: their role in infection and inflammation. J Leukoc Biol 2007; 81: 584-592.
52. Ancuta P, Rao R, Moses A, et al. Fractalkine preferentially mediates arrest and migration of CD16+ monocytes. J Exp Med 2003; 197: 1701-1707.
53. van de Veerdonk FL, Netea MG. Diversity: a hallmark of monocyte society. Immunity 2010; 33: 289-291.
54. Aspinall AI, Curbishley SM, Lalor PF, et al. CX (3)CR1 and vascular adhesion protein-1-dependent recruitment of CD16(+) monocytes across human liver sinusoidal endothelium. Hepatology 2010; 51: 2030-2039.
55. Rogacev KS, Cremers B, Zawada AM, et al. CD14++CD16+ monocytes independently predict cardiovascular events: a cohort study of 951 patients referred for elective coronary angiography. J Am Coll Cardiol 2012; 60: 1512-1520.
56. Kelesidis T, Kendall MA, Yang OO, et al. Biomarkers of microbial translocation and macrophage activation: association with progression of subclinical atherosclerosis in HIV-1 infection. J Infect Dis 2012; 206: 1558-1567.
57. Longenecker CT, Jiang Y, Orringer CE, et al. Soluble CD14 is independently associated with coronary calcification and extent of subclinical vascular disease in treated HIV infection. AIDS 2014; 28: 969-977.
58. Burdo TH, Lo J, Abbara S, et al. Soluble CD163, a novel marker of activated macrophages, is elevated and associated with noncalcified coronary plaque in HIV-infected patients. J Infect Dis 2011; 204: 1227-1236.
59. Fitch KV, Srinivasa S, Abbara S, et al. Noncalcified coronary atherosclerotic plaque and immune activation in HIV-infected women. J Infect Dis 2013; 208: 1737-1746.
60. McKibben RA, Margolick JB, Grinspoon S, et al. Elevated levels of monocyte activationmarkers are associated with subclinical atherosclerosis in men with and those without HIV infection. J Infect Dis 2015; 211: 1219-1228.
61. Subramanian S, Tawakol A, Burdo TH, et al. Arterial inflammation in patients with HIV. JAMA 2012; 308: 379-386.
62. Walker JA, Sulciner ML, Nowicki KD, et al. Elevated numbers of CD163+ macrophages in hearts of simian immunodeficiency virus-infected monkeys correlate with cardiac pathology and fibrosis. AIDS Res Human Retroviruses 2014; 30: 685-694.
63. Feeney ER, McAuley N, O'Halloran JA, et al. The expression of cholesterol metabolism genes in monocytes from HIV-infected subjects suggests intracellular cholesterol accumulation. J Infect Dis 2013; 207: 628-637.
64. Lo J, Rosenberg ES, Fitzgerald ML, et al. High-density lipoprotein-mediated cholesterol efflux capacity is improved by treatment with antiretroviral therapy in acute human immunodeficiency virus infection. Open Forum Infect Dis 2014; 1: ofu108.
65. Liang H, Duan Z, Li D, et al. Higher levels of circulating monocyte-platelet aggregates are correlated with viremia and increased sCD163 levels in HIV-1 infection. Cell Mol Immunol 2015; 12: 435-443.
66. Maisa A, Hearps AC, Angelovich TA, et al. Monocytes from HIV-infected individuals show impaired cholesterol efflux and increased foam cell formation after transendothelial migration. AIDS 2015; 29: 1445-1457.
67. Brenchley JM, Price DA, Schacker TW, et al. Microbial translocation is a cause of systemic immune activation in chronic HIV infection. Nat Med 2006; 12: 1365-1371.
68. Gupta SK, Mi D, Dube MP, et al. Pentoxifylline, inflammation, and endothelial function in HIV-infected persons: a randomized, placebo-controlled trial. PLoS One 2013; 8: e60852.
69. Hileman CO, Carman TL, Gripshover BM, et al. Salsalate is poorly tolerated and fails to improve endothelial function in virologically suppressed HIVinfected adults. AIDS 2010; 24: 1958-1961.
70. Gupta SK, Johnson RM, Saha C, et al. Improvement in HIV-related endothelial dysfunction using the anti-inflammatory agent salsalate: a pilot study. AIDS 2008; 22: 653-655.
71. Hileman CO, Carman TL, Storer NJ, et al. Omega-3 fatty acids do not improve endothelial function in virologically suppressed HIV-infected men: a randomized placebo-controlled trial. AIDS Res Hum Retroviruses 2012; 28: 649-655.
72. Wasko MC, Dasgupta A, Hubert H, et al. Propensity-adjusted association of methotrexate with overall survival in rheumatoid arthritis. Arthritis Rheum 2013; 65: 334-342.
73. Mann DL, McMurray JJ, Packer M, et al. Targeted anticytokine therapy in patients with chronic heart failure: results of the Randomized Etanercept Worldwide Evaluation (RENEWAL). Circulation 2004; 109: 1594-1602.
74. Chung ES, Packer M, Lo KH, et al. Randomized, double-blind, placebocontrolled, pilot trial of infliximab, a chimeric monoclonal antibody to tumor necrosis factor-alpha, in patients with moderate-to-severe heart failure: results of the anti-TNF Therapy Against Congestive Heart Failure (ATTACH) trial. Circulation 2003; 107: 3133-3140.
75. Abbate A, Kontos MC, Abouzaki NA, et al. Comparative safety of interleukin-1 blockade with anakinra in patients with ST-segment elevation acute myocardial infarction (from the VCU-ART and VCU-ART2 pilot studies). Am J Cardiol 2015; 115: 288-292.
76. Van Tassell BW, Arena R, Biondi-Zoccai G, et al. Effects of interleukin-1 blockade with anakinra on aerobic exercise capacity in patients with heart failure and preserved ejection fraction (from the D-HART pilot study). Am J Cardiol 2014; 113: 321-327.
77. Lo J, Lu MT, Ihenachor EJ, et al. Effects of statin therapy on coronary artery plaque volume and high-risk plaque morphology in HIV-infected patients with subclinical atherosclerosis: a randomised, double-blind, placebo-controlled trial. Lancet HIV 2015; 2: e52-e63.
78. Longenecker CT, Jiang Y, Debanne SM, et al. Rosuvastatin arrests progression of carotid intima-media thickness in treated HIV. In 22nd Conference on Retroviruses and Opportunistic Infections (CROI). Seattle, Washington, USA; 2015.
79. Ganesan A, Crum-Cianflone N, Higgins J, et al. High dose atorvastatin decreases cellular markers of immune activation without affecting HIV-1 RNA levels: results of a double-blind randomized placebo controlled clinical trial. J Infect Dis 2011; 203: 756-764.
80. Nakanjako D, Ssinabulya I, Nabatanzi R, et al. Atorvastatin reduces T-cell activation and exhaustion among HIV-infected cART-treated suboptimal immune responders in Uganda: a randomised crossover placebo-controlled trial. Trop Med Int Health 2015; 20: 380-390.
81. Overton ET, Sterrett S, Westfall AO, et al. Effects of atorvastatin and pravastatin on immune activation and T-cell function in antiretroviral therapy- suppressed HIV-1-infected patients. AIDS 2014; 28: 2627-2631.
82. De Wit S, Delforge M, Necsoi CV, Clumeck N. Downregulation of CD38 activation markers by atorvastatin in HIV patients with undetectable viral load. AIDS 2011; 25: 1332-1333.
83. Funderburg NT, Jiang Y, Debanne SM, et al. 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.
84. Zanni MV, Fitch KV, Feldpausch M, et al. 2013 American College of Cardiology/American Heart Association and 2004 Adult Treatment Panel III cholesterol guidelines applied to HIV-infected patients with/without subclinical high-risk coronary plaque. AIDS 2014; 28: 2061-2070.
85. Seshasai SR, Wijesuriya S, Sivakumaran R, et al. Effect of aspirin on vascular and nonvascular outcomes: meta-analysis of randomized controlled trials. Arch Intern Med 2012; 172: 209-216.
86. O'Brien M, Montenont E, Hu L, et al. Aspirin attenuates platelet activation and immune activation in HIV-1-infected subjects on antiretroviral therapy: a pilot study. J Acquir Immune Defic Syndr 2013; 63: 280-288.
87. Boccara F, Auclair M, Cohen A, et al. HIV protease inhibitors activate the adipocyte renin angiotensin system. Antivir Ther 2010; 15: 363-375.
88. Srinivasa S, Fitch KV, Wong K, et al. RAAS activation is associated with visceral adiposity and insulin resistance among HIV-infected patients. J Clin Endocrinol Metab 2015; 100: 2873-2882.
89. Baker JV, Huppler Hullsiek K, Prosser R, et al. Angiotensin converting enzyme inhibitor and HMG-CoA reductase inhibitor as adjunct treatment for persons with HIV infection: a feasibility randomized trial. PLoS One 2012; 7: e46894.
90. Lake JE, Tseng CH, Currier JS. A pilot study of telmisartan for visceral adiposity in HIV infection: the metabolic abnormalities, telmisartan, and HIV infection (MATH) trial. PLoS One 2013; 8: e58135.