Soluble CD14 is independently associated with coronary calcification and extent of subclinical vascular disease in treated HIV infection

AIDS

Volumn 28, Issue 7, 2014, Pages 969-977

  Longenecker, Chris T ^a,b   Jiang, Ying ^b   Orringer, Carl E ^a,b   Gilkeson, Robert C ^b,c   Debanne, Sara ^b   Funderburg, Nicholas T ^b   Lederman, Michael M ^b,c   Storer, Norma ^b,c   Labbato, Danielle E ^b,c   McComsey, Grace A ^b,c  

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

^b CASE WESTERN RESERVE UNIVERSITY   (United States)

^c UNIVERSITY HOSPITALS OF CLEVELAND   (United States)

Author keywords

carotid intima media thickness; coronary artery calcium; endothelial function; HIV; inflammation; microbial translocation; soluble CD14

Indexed keywords

ANTI HUMAN IMMUNODEFICIENCY VIRUS AGENT; C REACTIVE PROTEIN; CD14 ANTIGEN; CD163 ANTIGEN; D DIMER; FIBRINOGEN; HLA DR ANTIGEN; INTERLEUKIN 6; LOW DENSITY LIPOPROTEIN CHOLESTEROL; OSTEOCLAST DIFFERENTIATION FACTOR; OSTEOPROTEGERIN; SOLUBLE CD14 ANTIGEN; TUMOR NECROSIS FACTOR ALPHA RECEPTOR; UNCLASSIFIED DRUG; VASCULAR CELL ADHESION MOLECULE 1; VIRUS RNA;

ADULT; AFRICAN AMERICAN; ANTIVIRAL THERAPY; ARTERIAL WALL THICKNESS; ARTICLE; BRACHIAL ARTERY; CD4 LYMPHOCYTE COUNT; CD8+ T LYMPHOCYTE; CELL ACTIVATION; CONTROLLED STUDY; CORONARY ARTERY CALCIFICATION; CORONARY ARTERY CALCIUM SCORE; CROSS-SECTIONAL STUDY; DISEASE ASSOCIATION; ECHOGRAPHY; FEMALE; FRAMINGHAM RISK SCORE; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS INFECTED PATIENT; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; HYPEREMIA; INFLAMMATION; MAJOR CLINICAL STUDY; MALE; MONOCYTE; MULTIMODAL IMAGING; PRIORITY JOURNAL; RISK FACTOR; T LYMPHOCYTE ACTIVATION; VASCULAR DISEASE; ADOLESCENT; ASYMPTOMATIC DISEASES; BLOOD; CALCINOSIS; COMPLICATION; CORONARY BLOOD VESSEL; CORONARY DISEASE; HIV INFECTIONS; IMMUNOLOGY; MIDDLE AGED; PATHOLOGY; YOUNG ADULT;

ADOLESCENT; ADULT; ANTIGENS, CD14; ASYMPTOMATIC DISEASES; CALCINOSIS; CORONARY DISEASE; CORONARY VESSELS; CROSS-SECTIONAL STUDIES; FEMALE; HIV INFECTIONS; HUMANS; MALE; MIDDLE AGED; YOUNG ADULT;

EID: 84897498055     PISSN: 02699370     EISSN: 14735571     Source Type: Journal    
DOI: 10.1097/QAD.0000000000000158     Document Type: Article

References (104)

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8. Hunt PW, Martin JN, Sinclair E, Epling L, Teague J, Jacobson MA, et al. Valganciclovir reduces T cell activation in HIVinfected individuals with incomplete CD4R T cell recovery on antiretroviral therapy. J Infect Dis 2011; 203:1474-1483.
9. Sandler NG, Douek DC. Microbial translocation in HIV infection: causes, consequences and treatment opportunities. Nat Rev Microbiol 2012; 10:655-666.
10. Longenecker C, Funderburg N, Jiang Y, Debanne S, Storer N, Labbato D, et al. Markers of inflammation and CD8 T-cell activation, but not monocyte activation, are associated with subclinical carotid artery disease in HIV-infected individuals. HIV Med 2013; 14:385-390.
11. Kaplan RC, Sinclair E, Landay AL, Lurain N, Sharrett AR, Gange SJ, et al. T cell activation and senescence predict subclinical carotid artery disease in HIV-infected women. J Infect Dis 2011; 203:452-463.
12. Kaplan RC, Sinclair E, Landay AL, Lurain N, Sharrett AR, Gange SJ, et al. T cell activation predicts carotid artery stiffness among HIV-infected women. Atherosclerosis 2011; 217:207-213.
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15. Zanni MV, Abbara S, Lo J, Wai B, Hark D, Marmarelis E, et al. Increased coronary atherosclerotic plaque vulnerability by coronary computed tomography angiography in HIV-infected men. AIDS 2013; 27:1263-1272.
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24. Wilson PW, D'Agostino RB, Levy D, Belanger AM, Silbershatz H, Kannel WB. Prediction of coronary heart disease using risk factor categories. Circulation 1998; 97:1837-1847.
25. Ridker PM, Buring JE, Rifai N, Cook NR. Development and validation of improved algorithms for the assessment of global cardiovascular risk in women: the Reynolds Risk Score. JAMA 2007; 297:611-619.
26. Ridker PM, Paynter NP, Rifai N, Gaziano JM, Cook NR. C-reactive protein and parental history improve global cardiovascular risk prediction: the Reynolds Risk Score for men. Circulation 2008; 118:2243-22512244p following 2251.
27. McComsey GA, Kitch D, Sax PE, Tebas P, Tierney C, Jahed NC, et al. Peripheral and central fat changes in subjects randomized to abacavir-lamivudine or tenofovir-emtricitabine with atazanavir-ritonavir or efavirenz: ACTG Study A5224 s. Clin Infect Dis 2011; 53:185-196.
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29. Stein JH, Korcarz CE, Hurst RT, Lonn E, Kendall CB, Mohler ER, et al. Use of carotid ultrasound to identify subclinical vascular disease and evaluate cardiovascular disease risk: a consensus statement from the American Society of Echocardiography Carotid Intima-Media Thickness Task Force. Endorsed by the Society for Vascular Medicine. J Am Soc Echocardiogr 2008; 21:93-111.
30. Torriani FJ, Komarow L, Parker RA, Cotter BR, Currier JS, Dube MP, et al. Endothelial function in human immunodeficiency virus-infected antiretroviral-naive subjects before and after starting potent antiretroviral therapy: the ACTG (AIDS Clinical Trials Group) Study 5152s. J Am Coll Cardiol 2008; 52:569-576.
31. Grundy SM, Brewer HB Jr, Cleeman JI, Smith SC Jr, Lenfant C. Definition of metabolic syndrome: report of the National Heart, Lung, and Blood Institute/American Heart Association conference on scientific issues related to definition. Circulation 2004; 109:433-438.
32. Arroyo-Espliguero R, Avanzas P, Jeffery S, Kaski JC. CD14 and toll-like receptor 4: a link between infection and acute coronary events? Heart 2004; 90:983-988.
33. Bas S, Gauthier BR, Spenato U, Stingelin S, Gabay C. CD14 is an acute-phase protein. J Immunol 2004; 172:4470-4479.
34. Lederman MM, Calabrese L, Funderburg NT, Clagett B, Medvik K, Bonilla H, et al. Immunologic failure despite suppressive antiretroviral therapy is related to activation and turnover of memory CD4 cells. J Infect Dis 2011; 204:1217-1226.
35. Marchetti G, Cozzi-Lepri A, Merlini E, Bellistri GM, Castagna A, Galli M, et al. Microbial translocation predicts disease progression of HIV-infected antiretroviral-naive patients with high CD4R cell count. AIDS 2011; 25:1385-1394.
36. Thiebaut R, Charpentier C, Damond F, Taieb A, Antoine R, Capeau J, et al. Association of soluble CD14 and inflammatory biomarkers with HIV-2 disease progression. Clin Infect Dis 2012; 55:1417-1425.
37. Sandler NG, Wand H, Roque A, Law M, Nason MC, Nixon DE, et al. Plasma levels of soluble CD14 independently predict mortality in HIV infection. J Infect Dis 2011; 203:780-790.
38. Justice AC, Freiberg MS, Tracy R, Kuller L, Tate JP, Goetz MB, et al. Does an index composed of clinical data reflect effects of inflammation, coagulation, and monocyte activation on mortality among those aging with HIV? Clin Infect Dis 2012; 54:984-994.
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45. Blodget E, Shen C, Aldrovandi G, Rollie A, Gupta SK, Stein JH, et al. Relationship between microbial translocation and endothelial function in HIV infected patients. PLoS One 2012; 7:e42624.
46. Fitch KV, Srinivasa S, Abbara S, Burdo TH, Williams KC, Eneh P, et al. Noncalcified coronary atherosclerotic plaque and immune activation in HIV-infected women. J Infect Dis 2013; 208:1737-1746.
47. Mayne E, Funderburg NT, Sieg SF, Asaad R, Kalinowska M, Rodriguez B, et al. Increased platelet and microparticle activation in HIV infection: upregulation of P-selectin and tissue factor expression. J Acquir Immune Defic Syndr 2012; 59:340-346.
48. Lederman MM, Calabrese L, Funderburg NT, Clagett B, Medvik K, Bonilla H, et al. Immunologic failure despite suppressive antiretroviral therapy is related to activation and turnover of memory CD4 cells. J Infect Dis 2011; 204:1217-1226.
49. Funderburg NT, Zidar DA, Shive C, Lioi A, Mudd J, Musselwhite LW, et al. Shared monocyte subset phenotypes in HIV-1 infection and in uninfected subjects with acute coronary syndrome. Blood 2012; 120:4599-4608.
50. Funderburg NT, Mayne E, Sieg SF, Asaad R, Jiang W, Kalinowska M, et al. Increased tissue factor expression on circulating monocytes in chronic HIV infection: relationship to in vivo coagulation and immune activation. Blood 2010; 115:161-167.
51. Funderburg NT, Jiang Y, Debanne SM, Storer N, Labbato D, Clagett B, et al. Rosuvastatin treatment reduces markers of monocyte activation in HIV infected subjects on antiretroviral therapy. Clin Infect Dis 2013[Epub ahead of print].
52. Anderson TJ, Charbonneau F, Title LM, Buithieu J, Rose MS, Conradson H, et al. Microvascular function predicts cardiovascular events in primary prevention: long-term results from the Firefighters and Their Endothelium (FATE) study. Circulation 2011; 123:163-169.
53. Boccara F, Lang S, Meuleman C, Ederhy S, Mary-Krause M, Costagliola D, et al. HIV and coronary heart disease: time for a better understanding. J Am Coll Cardiol 2013; 61:511-523.
54. Freiberg MS, Chang CC, Kuller LH, Skanderson M, Lowy E, Kraemer KL, et al. HIV infection and the risk of acute myocardial infarction. JAMA Intern Med 2013; 173:1-9.
55. Hsue PY, Deeks SG, Hunt PW. Immunologic basis of cardiovascular disease in HIV-infected adults. J Infect Dis 2012; 205 (Suppl 3):S375-S382.
56. van Lelyveld SF, Gras L, Kesselring A, Zhang S, De Wolf F, Wensing AM, et al. Long-term complications in patients with poor immunological recovery despite virological successful HAART in Dutch ATHENA cohort. AIDS 2012; 26:465-474.
57. Duprez DA, Neuhaus J, Kuller LH, Tracy R, Belloso W, De Wit S, et al. Inflammation, coagulation and cardiovascular disease in HIV-infected individuals. PLoS One 2012; 7:e44454.
58. Hunt PW. HIV and inflammation: mechanisms and consequences. Current HIV/AIDS Rep 2012; 9:139-147.
59. Giralt M, Domingo P, Villarroya F. Adipose tissue biology and HIV-infection. Best practice & research. Clin Endocrinol Metab 2011; 25:487-499.
60. Hunt PW, Martin JN, Sinclair E, Epling L, Teague J, Jacobson MA, et al. Valganciclovir reduces T cell activation in HIVinfected individuals with incomplete CD4R T cell recovery on antiretroviral therapy. J Infect Dis 2011; 203:1474-1483.
61. Sandler NG, Douek DC. Microbial translocation in HIV infection: causes, consequences and treatment opportunities. Nat Rev Microbiol 2012; 10:655-666.
62. Longenecker C, Funderburg N, Jiang Y, Debanne S, Storer N, Labbato D, et al. Markers of inflammation and CD8 T-cell activation, but not monocyte activation, are associated with subclinical carotid artery disease in HIV-infected individuals. HIV Med 2013; 14:385-390.
63. Kaplan RC, Sinclair E, Landay AL, Lurain N, Sharrett AR, Gange SJ, et al. T cell activation and senescence predict subclinical carotid artery disease in HIV-infected women. J Infect Dis 2011; 203:452-463.
64. Kaplan RC, Sinclair E, Landay AL, Lurain N, Sharrett AR, Gange SJ, et al. T cell activation predicts carotid artery stiffness among HIV-infected women. Atherosclerosis 2011; 217:207-213.
65. Kelesidis T, Kendall MA, Yang OO, Hodis HN, Currier JS. Biomarkers of microbial translocation and macrophage activation: association with progression of subclinical atherosclerosis in HIV-1 infection. J Infect Dis 2012; 206:1558-1567.
66. Subramanian S, Tawakol A, Burdo TH, Abbara S, Wei J, Vijayakumar J, et al. Arterial inflammation in patients with HIV. JAMA 2012; 308:379-386.
67. Zanni MV, Abbara S, Lo J, Wai B, Hark D, Marmarelis E, et al. Increased coronary atherosclerotic plaque vulnerability by coronary computed tomography angiography in HIV-infected men. AIDS 2013; 27:1263-1272.
68. Burdo TH, Lo J, Abbara S, Wei J, Delelys ME, Preffer F, 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.
69. Yeboah J, McClelland RL, Polonsky TS, Burke GL, Sibley CT, O'Leary D, et al. Comparison of novel risk markers for improvement in cardiovascular risk assessment in intermediate-risk individuals. JAMA 2012; 308:788-795.
70. Hulten E, Mitchell J, Scally J, Gibbs B, Villines TC. HIV positivity, protease inhibitor exposure and subclinical atherosclerosis: a systematic review and meta-analysis of observational studies. Heart 2009; 95:1826-1835.
71. Lo J, Abbara S, Shturman L, Soni A, Wei J, Rocha-Filho JA, et al. Increased prevalence of subclinical coronary atherosclerosis detected by coronary computed tomography angiography in HIV-infected men. AIDS 2010; 24:243-253.
72. Hsue PY, Ordovas K, Lee T, Reddy G, Gotway M, Schnell A, et al. Carotid intima-media thickness among human immunodeficiency virus-infected patients without coronary calcium. Am J Cardiol 2012; 109:742-747.
73. Jenny NS, Brown ER, Detrano R, Folsom AR, Saad MF, Shea S, et al. Associations of inflammatory markers with coronary artery calcification: results from the Multi-Ethnic Study of Atherosclerosis. Atherosclerosis 2010; 209:226-229.
74. Hamirani YS, Pandey S, Rivera JJ, Ndumele C, Budoff MJ, Blumenthal RS, et al. Markers of inflammation and coronary artery calcification: a systematic review. Atherosclerosis 2008; 201:1-7.
75. Matthews DR, Hosker JP, Rudenski AS, Naylor BA, Treacher DF, Turner RC. Homeostasis model assessment: insulin resistance and beta-cell function from fasting plasma glucose and insulin concentrations in man. Diabetologia 1985; 28:412-419.
76. Wilson PW, D'Agostino RB, Levy D, Belanger AM, Silbershatz H, Kannel WB. Prediction of coronary heart disease using risk factor categories. Circulation 1998; 97:1837-1847.
77. Ridker PM, Buring JE, Rifai N, Cook NR. Development and validation of improved algorithms for the assessment of global cardiovascular risk in women: the Reynolds Risk Score. JAMA 2007; 297:611-619.
78. Ridker PM, Paynter NP, Rifai N, Gaziano JM, Cook NR. C-reactive protein and parental history improve global cardiovascular risk prediction: the Reynolds Risk Score for men. Circulation 2008; 118:2243-22512244p following 2251.
79. McComsey GA, Kitch D, Sax PE, Tebas P, Tierney C, Jahed NC, et al. Peripheral and central fat changes in subjects randomized to abacavir-lamivudine or tenofovir-emtricitabine with atazanavir-ritonavir or efavirenz: ACTG Study A5224 s. Clin Infect Dis 2011; 53:185-196.
80. Funderburg NT, Zidar DA, Shive C, Lioi A, Mudd J, Musselwhite LW, et al. Shared monocyte subset phenotypes in HIV-1 infection and in uninfected subjects with acute coronary syndromes. Blood 2012; 120:4599-4608.
81. Stein JH, Korcarz CE, Hurst RT, Lonn E, Kendall CB, Mohler ER, et al. Use of carotid ultrasound to identify subclinical vascular disease and evaluate cardiovascular disease risk: a consensus statement from the American Society of Echocardiography Carotid Intima-Media Thickness Task Force. Endorsed by the Society for Vascular Medicine. J Am Soc Echocardiogr 2008; 21:93-111.
82. Torriani FJ, Komarow L, Parker RA, Cotter BR, Currier JS, Dube MP, et al. Endothelial function in human immunodeficiency virus-infected antiretroviral-naive subjects before and after starting potent antiretroviral therapy: the ACTG (AIDS Clinical Trials Group) Study 5152s. J Am Coll Cardiol 2008; 52:569-576.
83. Grundy SM, Brewer HB Jr, Cleeman JI, Smith SC Jr, Lenfant C. Definition of metabolic syndrome: report of the National Heart, Lung, and Blood Institute/American Heart Association conference on scientific issues related to definition. Circulation 2004; 109:433-438.
84. Arroyo-Espliguero R, Avanzas P, Jeffery S, Kaski JC. CD14 and toll-like receptor 4: a link between infection and acute coronary events? Heart 2004; 90:983-988.
85. Bas S, Gauthier BR, Spenato U, Stingelin S, Gabay C. CD14 is an acute-phase protein. J Immunol 2004; 172:4470-4479.
86. Lederman MM, Calabrese L, Funderburg NT, Clagett B, Medvik K, Bonilla H, et al. Immunologic failure despite suppressive antiretroviral therapy is related to activation and turnover of memory CD4 cells. J Infect Dis 2011; 204:1217-1226.
87. Marchetti G, Cozzi-Lepri A, Merlini E, Bellistri GM, Castagna A, Galli M, et al. Microbial translocation predicts disease progression of HIV-infected antiretroviral-naive patients with high CD4R cell count. AIDS 2011; 25:1385-1394.
88. Thiebaut R, Charpentier C, Damond F, Taieb A, Antoine R, Capeau J, et al. Association of soluble CD14 and inflammatory biomarkers with HIV-2 disease progression. Clin Infect Dis 2012; 55:1417-1425.
89. Sandler NG, Wand H, Roque A, Law M, Nason MC, Nixon DE, et al. Plasma levels of soluble CD14 independently predict mortality in HIV infection. J Infect Dis 2011; 203:780-790.
90. Justice AC, Freiberg MS, Tracy R, Kuller L, Tate JP, Goetz MB, et al. Does an index composed of clinical data reflect effects of inflammation, coagulation, and monocyte activation on mortality among those aging with HIV? Clin Infect Dis 2012; 54:984-994.
91. Reiner AP, Lange EM, Jenny NS, Chaves PH, Ellis J, Li J, et al. Soluble CD14: genomewide association analysis and relationship to cardiovascular risk and mortality in older adults. Arterioscler Thromb Vasc Biol 2013; 33:158-164.
92. Koenig W, Khuseyinova N, Hoffmann MM, Marz W, Frohlich M, Hoffmeister A, et al. CD14 C(-260)-T polymorphism, plasma levels of the soluble endotoxin receptor CD14, their association with chronic infections and risk of stable coronary artery disease. J Am Coll Cardiol 2002; 40:34-42.
93. Morange PE, Saut N, Alessi MC, Frere C, Hawe E, Yudkin JS, et al. Interaction between the C-260T polymorphism of the CD14 gene and the plasma IL-6 concentration on the risk of myocardial infarction: the HIFMECH study. Atherosclerosis 2005; 179:317-323.
94. Morange PE, Tiret L, Saut N, Luc G, Arveiler D, Ferrieres J, et al. TLR4/Asp299Gly, CD14/C-260T, plasma levels of the soluble receptor CD14 and the risk of coronary heart disease: the PRIME Study. Eur J Hum Genet 2004; 12:1041-1049.
95. Merlini E, Luzi K, Suardi E, Barassi A, Cerrone M, Martinez JS, et al. T-cell phenotypes, apoptosis and inflammation in HIVR patients on virologically effective cART with early atherosclerosis. PLoS One 2012; 7:e46073.
96. Kaplan RC, Landay AL, HodisHN, Gange SJ, Norris PJ, Young M, et al. Potential cardiovascular disease risk markers among HIVinfected women initiating antiretroviral treatment. J Acquir Immune Defic Syndr 2012; 60:359-368.
97. Blodget E, Shen C, Aldrovandi G, Rollie A, Gupta SK, Stein JH, et al. Relationship between microbial translocation and endothelial function in HIV infected patients. PLoS One 2012; 7:e42624.
98. Fitch KV, Srinivasa S, Abbara S, Burdo TH, Williams KC, Eneh P, et al. Noncalcified coronary atherosclerotic plaque and immune activation in HIV-infected women. J Infect Dis 2013; 208:1737-1746.
99. Mayne E, Funderburg NT, Sieg SF, Asaad R, Kalinowska M, Rodriguez B, et al. Increased platelet and microparticle activation in HIV infection: upregulation of P-selectin and tissue factor expression. J Acquir Immune Defic Syndr 2012; 59:340-346.
100. Lederman MM, Calabrese L, Funderburg NT, Clagett B, Medvik K, Bonilla H, et al. Immunologic failure despite suppressive antiretroviral therapy is related to activation and turnover of memory CD4 cells. J Infect Dis 2011; 204:1217-1226.
101. Funderburg NT, Zidar DA, Shive C, Lioi A, Mudd J, Musselwhite LW, et al. Shared monocyte subset phenotypes in HIV-1 infection and in uninfected subjects with acute coronary syndrome. Blood 2012; 120:4599-4608.
102. Funderburg NT, Mayne E, Sieg SF, Asaad R, Jiang W, Kalinowska M, et al. Increased tissue factor expression on circulating monocytes in chronic HIV infection: relationship to in vivo coagulation and immune activation. Blood 2010; 115:161-167.
103. Funderburg NT, Jiang Y, Debanne SM, Storer N, Labbato D, Clagett B, et al. Rosuvastatin treatment reduces markers of monocyte activation in HIV infected subjects on antiretroviral therapy. Clin Infect Dis 2013[Epub ahead of print].
104. Anderson TJ, Charbonneau F, Title LM, Buithieu J, Rose MS, Conradson H, et al. Microvascular function predicts cardiovascular events in primary prevention: long-term results from the Firefighters and Their Endothelium (FATE) study. Circulation 2011; 123:163-169.