Relevance of interleukin-6 and D-dimer for serious non-AIDS morbidity and death among HIV-positive adults on suppressive antiretroviral therapy

PLoS ONE

Volumn 11, Issue 5, 2016, Pages

  Grund, Birgit ^a   Baker, Jason V ^b,c   Deeks, Steven G ^d,e   Wolfson, Julian ^f   Wentworth, Deborah ^f   Cozzi Lepri, Alessandro ^g   Cohen, Calvin J ^h   Phillips, Andrew ^g   Lundgren, Jens D ⁱ   Neaton, James D ^f  

^a UNIVERSITY OF MINNESOTA   (United States)

^b HENNEPIN COUNTY MEDICAL CENTER   (United States)

^c UNIVERSITY OF MINNESOTA MEDICAL SCHOOL   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

^e SAN FRANCISCO GENERAL HOSPITAL   (United States)

^f UNIVERSITY OF MINNESOTA   (United States)

^g UNIVERSITY COLLEGE LONDON   (United Kingdom)

^h GILEAD SCIENCES   (United States)

ⁱ UNIVERSITY OF COPENHAGEN   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIRETROVIRUS AGENT; C REACTIVE PROTEIN; D DIMER; INTERLEUKIN 6; RECOMBINANT INTERLEUKIN 2; VIRUS RNA; BIOLOGICAL MARKER; FIBRIN DEGRADATION PRODUCT; FIBRIN FRAGMENT D;

ADULT; ARTICLE; CARDIOVASCULAR DISEASE; CAUSE OF DEATH; CD4+ T LYMPHOCYTE; CEREBROVASCULAR ACCIDENT; COHORT ANALYSIS; CONTROLLED STUDY; DILUTION; DISEASE ASSOCIATION; FEMALE; HAZARD RATIO; HEART INFARCTION; HIGHLY ACTIVE ANTIRETROVIRAL THERAPY; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS INFECTED PATIENT; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; MAJOR CLINICAL STUDY; MALE; MORBIDITY; MORTALITY; PROPORTIONAL HAZARDS MODEL; RISK REDUCTION; BIOASSAY; BLOOD; HIV SEROPOSITIVITY; KAPLAN MEIER METHOD; METABOLISM; MIDDLE AGED;

ADULT; ANTIRETROVIRAL THERAPY, HIGHLY ACTIVE; BIOMARKERS; C-REACTIVE PROTEIN; ENDPOINT DETERMINATION; FEMALE; FIBRIN FIBRINOGEN DEGRADATION PRODUCTS; HIV SEROPOSITIVITY; HUMANS; INTERLEUKIN-6; KAPLAN-MEIER ESTIMATE; MALE; MIDDLE AGED; MORBIDITY; RISK REDUCTION BEHAVIOR;

EID: 84971264750     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0155100     Document Type: Article

References (45)

1. Achhra AC, Amin J, Law MG, Emery S, Gerstoft J, Gordin FM, et al. Immunodeficiency and the risk of serious clinical endpoints in a well studied cohort of treated HIV-infected patients. AIDS. 2010; 24 (12):1877-86. doi: 10.1097/QAD.0b013e32833b1b26 PMID: 20588170; PubMed Central PMCID: PMCPMC2902669.
2. Antiretroviral Therapy Cohort Collaboration. Causes of death in HIV-1-infected patients treated with antiretroviral therapy, 1996-2006: collaborative analysis of 13 HIV cohort studies. Clinical Infectious Diseases. 2010; 50(10):1387-96. doi: http://dx.doi.org/10.1086/652283 PMID: 20380565; PubMed Central PMCID: PMCNIHMS308097 PMC3157754.
3. INSIGHT START Study Group, Lundgren JD, Babiker AG, Gordin F, Emery S, Grund B, et al. Initiation of Antiretroviral Therapy in Early Asymptomatic HIV Infection. N Engl J Med. 2015; 373 (9):795-807. doi: 10.1056/NEJMoa1506816 PMID: Medline:26192873.
4. Mocroft A, Phillips AN, Gatell J, Horban A, Ledergerber B, Zilmer K, et al. CD4 cell count and viral loadspecific rates of AIDS, non-AIDS and deaths according to current antiretroviral use. AIDS. 2013; 27 (6):907-18. PMID: Medline:23698060. doi: 10.1097/QAD.0b013e32835cb766
5. 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(9):e44454. Epub 2012/09/13. doi: 10.1371/journal.pone.0044454 PMID: 22970224; PubMed Central PMCID: PMCPmc3438173.
6. Nordell AD, McKenna M, Borges AH, Duprez D, Neuhaus J, Neaton JD, et al. Severity of cardiovascular disease outcomes among patients with HIV is related to markers of inflammation and coagulation. J Am Heart Assoc. 2014; 3(3). PMID: Medline:24870935.
7. Triant VA, Meigs JB, Grinspoon SK. Association of C-reactive protein and HIV infection with acute myocardial infarction. J Acquir Immune Defic Syndr. 2009; 51(3):268-73. PMID: Medline:19387353. doi: 10.1097/QAI.0b013e3181a9992c
8. Borges AH, Silverberg MJ, Wentworth D, Grulich AE, Fatkenheuer G, Mitsuyasu R, et al. Predicting risk of cancer during HIV infection: the role of inflammatory and coagulation biomarkers. AIDS. 2013; 27 (9):1433-41. Epub 2013/08/16. doi: 10.1097/QAD.0b013e32835f6b0c PMID: 23945504; PubMed Central PMCID: PMCPmc4046103.
9. Achhra AC, Amin J, Sabin C, Chu H, Dunn D, Kuller LH, et al. Reclassification of risk of death with the knowledge of D-dimer in a cohort of treated HIV-infected individuals. AIDS. 2012; 26(13):1707 -17. Epub 2012/05/23. doi: 10.1097/QAD.0b013e328355d659 PMID: 22614887.
10. Kuller LH, Tracy R, Belloso W, De Wit S, Drummond F, Lane HC, et al. Inflammatory and coagulation biomarkers and mortality in patients with HIV infection. PLoS Med. 2008; 5(10):e203. doi: http://dx.doi.org/10.1371/journal.pmed.0050203 PMID: 18942885.
11. Tien PC, Choi AI, Zolopa AR, Benson C, Tracy R, Scherzer R, et al. Inflammation and mortality in HIVinfected adults: analysis of the FRAM study cohort. J Acquir Immune Defic Syndr. 2010; 55(3):316-22. PMID: Medline:20581689. doi: 10.1097/QAI.0b013e3181e66216
12. Baker JV, Neuhaus J, Duprez D, Kuller LH, Tracy R, Belloso WH, et al. Changes in inflammatory and coagulation biomarkers: a randomized comparison of immediate versus deferred antiretroviral therapy in patients with HIV infection. J Acquir Immune Defic Syndr. 2011; 56(1):36-43. PMID: Medline:20930640. doi: 10.1097/QAI.0b013e3181f7f61a
13. Neuhaus J, Jacobs DR, Baker JV, Calmy A, Duprez D, La Rosa A, et al. Markers of inflammation, coagulation, and renal function are elevated in adults with HIV infection. The Journal of Infectious Diseases. 2010; 201(12):1788-95. doi: 10.1086/652749 PMID: 20446848; PubMed Central PMCID: PMCPMC2872049.
14. Danesh J, Kaptoge S, Mann AG, Sarwar N, Wood A, Angleman SB, et al. Long-term interleukin-6 levels and subsequent risk of coronary heart disease: two new prospective studies and a systematic review. PLoS Med. 2008; 5(4):e78. PMID: 18399716; PubMed Central PMCID: PMCPMC2288623. doi: 10.1371/journal.pmed.0050078
15. Danesh J, Whincup P, Walker M, Lennon L, Thomson A, Appleby P, et al. Fibrin D-dimer and coronary heart disease: prospective study and meta-analysis. Circulation. 2001; 103(19):2323-7. PMID: 11352877.
16. Emerging Risk Factors Collaboration, Kaptoge S, Di Angelantonio E, Lowe G, Pepys MB, Thompson SG, et al. C-reactive protein concentration and risk of coronary heart disease, stroke, and mortality: an individual participant meta-analysis. Lancet. 2010; 375(9709):132-40. PMID: 20031199; PubMed Central PMCID: PMCPMC3162187. doi: 10.1016/S0140-6736(09)61717-7
17. Pai JK, Pischon T, Ma J, Manson JE, Hankinson SE, Joshipura K, et al. Inflammatory markers and the risk of coronary heart disease in men and women. N Engl J Med. 2004; 351(25):2599-610. PMID: Medline:15602020.
18. Di Castelnuovo A, Agnoli C, de Curtis A, Giurdanella MC, Sieri S, Mattiello A, et al. Elevated levels of D-dimers increase the risk of ischaemic and haemorrhagic stroke. Findings from the EPICOR Study. Thrombosis and Haemostasis. 2014; 112(2014-07-17). doi: 10.1160/TH14-04-0297
19. Luc G, Bard J-M, Juhan-Vague I, Ferrieres J, Evans A, Amouyel P, et al. C-reactive protein, interleukin- 6, and fibrinogen as predictors of coronary heart disease: the PRIME Study. Arterioscler Thromb Vasc Biol. 2003; 23(7):1255-61. PMID: Medline:12775578.
20. Ridker PM, Rifai N, Stampfer MJ, Hennekens CH. Plasma concentration of interleukin-6 and the risk of future myocardial infarction among apparently healthy men. Circulation. 2000; 101(15):1767-72. PMID: Medline:10769275.
21. Smith A, Patterson C, Yarnell J, Rumley A, Ben-Shlomo Y, Lowe G. Which hemostatic markers add to the predictive value of conventional risk factors for coronary heart disease and ischemic stroke? The Caerphilly Study. Circulation. 2005; 112(20):3080-7. PMID: Medline:16286603.
22. Kuller LH, Tracy RP, Shaten J, Meilahn EN. Relation of C-reactive protein and coronary heart disease in the MRFIT nested case-control study. Multiple Risk Factor Intervention Trial. American Journal of Epidemiology. 1996; 144(6):537-47. PMID: Medline:8797513.
23. Allin KH, Bojesen SE, Nordestgaard BG. Baseline C-reactive protein is associated with incident cancer and survival in patients with cancer. Journal of Clinical Oncology: official journal of the American Society of Clinical Oncology. 2009; 27(13):2217-24. doi: 10.1200/JCO.2008.19.8440 PMID: Medline:19289618.
24. Il'yasova D, Colbert LH, Harris TB, Newman AB, Bauer DC, Satterfield S, et al. Circulating levels of inflammatory markers and cancer risk in the health aging and body composition cohort. Cancer Epidemiol Biomarkers Prev. 2005; 14(10):2413-8. PMID: Medline:16214925.
25. Tian G, Mi J, Wei X, Zhao D, Qiao L, Yang C, et al. Circulating interleukin-6 and cancer: A meta-analysis using Mendelian randomization. Sci Rep. 2015; 5:11394. PMID: Medline:26096712. doi: 10.1038/srep11394
26. Bash LD, Erlinger TP, Coresh J, Marsh-Manzi J, Folsom AR, Astor BC. Inflammation, hemostasis, and the risk of kidney function decline in the Atherosclerosis Risk in Communities (ARIC) Study. Am J Kidney Dis. 2009; 53(4):596-605. PMID: Medline:19110358. doi: 10.1053/j.ajkd.2008.10.044
27. Di Castelnuovo A, de Curtis A, Costanzo S, Persichillo M, Olivieri M, Zito F, et al. Association of D-dimer levels with all-cause mortality in a healthy adult population: findings from the MOLI-SANI study. Haematologica. 2013; 98(9):1476-80. doi: 10.3324/haematol.2012.083410 PMID: 23645692
28. Folsom AR, Delaney JAC, Lutsey PL, Zakai NA, Jenny NS, Polak JF, et al. Associations of factor VIII (c), D-dimer, and plasmin-antiplasmin with incident cardiovascular disease and all-cause mortality. Am J Hematol. 2009; 84(6):349-53. doi: 10.1002/Ajh.21429 PMID: Medline:19472201; PubMed Central PMCID: PMC2950108.
29. Harris TB, Ferrucci L, Tracy RP, Corti MC, Wacholder S, Ettinger WH Jr., et al. Associations of elevated interleukin-6 and C-reactive protein levels with mortality in the elderly. Am J Med. 1999; 106(5):506-12. PMID: Medline:10335721.
30. Rajasuriar R, Khoury G, Kamarulzaman A, French MA, Cameron PU, Lewin SR. Persistent immune activation in chronic HIV infection: do any interventions work? AIDS. 2013; 27(8):1199-208. doi: 10.1097/QAD.0b013e32835ecb8b PMID: WOS:000318156400002.
31. Butler SL, Valdez H, Westby M, Perros M, June CH, Jacobson JM, et al. Disease-modifying therapeutic concepts for HIV in the era of highly active antiretroviral therapy. J Acquir Immune Defic Syndr. 2011; 58(3):297-303. doi: 10.1097/QAI.0b013e31822ccfcc PMID: 21792065.
32. El-Sadr WM, Lundgren JD, Neaton JD, Gordin F, Abrams D, Arduino RC, et al. CD4+ count-guided interruption of antiretroviral treatment. N Engl J Med. 2006; 355(22):2283-96. PMID: 17135583.
33. El-Sadr W, Grund B, Neuhaus J, Babiker A, Cohen C, Darbyshire J, et al. Risk for opportunistic disease and death after reinitiating continuous antiretroviral therapy in patients with HIV previously receiving episodic therapy - a randomized trial. Annals of Internal Medicine. 2008; 149(5):289-W62. PMID: ISI:000259229300001.
34. Abrams D, Levy Y, Losso MH, Babilker A, Collins G, Cooper DA, et al. Interleukin-2 Therapy in Patients with HIV Infection. New England Journal of Medicine. 2009; 361(16):1548-59. PMID: ISI:000270777000008. doi: 10.1056/NEJMoa0903175
35. CIOMS Working Group. Introductiory Guide for Standardised MedDRA Queries (SMQs) Version 12.0. In: International Federation of Pharmaceutical Manufacturers and Associations (IFPMA), editor. 2009.
36. Kowalska JD, Friis-Moller N, Kirk O, Bannister W, Mocroft A, Sabin C, et al. The Coding Causes of Death in HIV (CoDe) Project: initial results and evaluation of methodology. Epidemiology. 2011; 22 (4):516-23. PMID: Medline:21522013. doi: 10.1097/EDE.0b013e31821b5332
37. Sakkinen PA, Macy EM, Callas PW, Cornell ES, Hayes TE, Kuller LH, et al. Analytical and biologic variability in measures of hemostasis, fibrinolysis, and inflammation: assessment and implications for epidemiology. Am J Epidemiol. 1999; 149(3):261-7. PMID: Medline:9927222.
38. Burnham K, Anderson D. Multimodel inference - understanding AIC and BIC in model selection. Sociological Methods & Research. 2004; 33(2):261-304. doi: 10.1177/0049124104268644 PMID: WOS:000224706300004.
39. Hughes MD. Regression dilution in the proportional hazards model. Biometrics. 1993; 49(4):1056-66. PMID: 8117900.
40. Knuiman MW, Divitini ML, Buzas JS, Fitzgerald PE. Adjustment for regression dilution in epidemiological regression analyses. Ann Epidemiol. 1998; 8(1):56-63. S1047279797001075 [pii]. PMID: 9465995.
41. R Development Core Team. R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing; 2014. Available: http://www.r-project.org.
42. Ridker PM. Testing the inflammatory hypothesis of atherothrombosis: scientific rationale for the cardiovascular inflammation reduction trial (CIRT). J Thromb Haemost. 2009; 7 Suppl 1:332-9. PMID: Medline:19630828. doi: 10.1111/j.1538-7836.2009.03404.x
43. National Institute of Allergy and Infectious Diseases (NIAID). NIH Launches Largest Clinical Trial Focused on HIV-Related Cardiovascular Disease. NIH News 2015 [cited 2015 26 September]. Available: http://www.niaid.nih.gov/news/newsreleases/2015/Pages/REPRIEVE.aspx.
44. Borges AH, Silverberg MJ, Wentworth D, Grulich AE, Fatkenheuer G, Mitsuyasu R, et al. Predicting risk of cancer during HIV infection: the role of inflammatory and coagulation biomarkers. AIDS. 2013; 27 (9):1433-41. PMID: Medline:23945504. doi: 10.1097/QAD.0b013e32835f6b0c
45. Tripodi A, Mannucci PM. The coagulopathy of chronic liver disease. N Engl J Med. 2011; 365 (2):147-56. PMID: Medline:21751907. doi: 10.1056/NEJMra1011170