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01-08-2018 | Original Investigation

Soluble CD163 and soluble CD14 plasma levels but not cellular HIV-DNA decrease during successful interferon-free anti-HCV therapy in HIV-1–HCV co-infected patients on effective combined anti-HIV treatment

Authors: Saverio G. Parisi, Samantha Andreis, Carlo Mengoli, Nicola Menegotto, Silvia Cavinato, Renzo Scaggiante, Massimo Andreoni, Giorgio Palù, Monica Basso, Anna Maria Cattelan

Published in: Medical Microbiology and Immunology | Issue 3-4/2018

Abstract

Soluble CD163, soluble CD14 and cellular HIV-1-DNA levels reflect two different aspects of HIV infection: immune activation and the reservoir of infected cells. The aim of this study was to describe their relationships in a cohort of HIV–HCV co-infected patients successfully treated for both HCV and HIV infections. Fifty-five patients were recruited and studied prior to the start of direct-acting antivirals (DAAs) (T0), at week 12 of DAA treatment (T1) and 24 weeks after T0 (T2). The subjects were classified as having undetectable plasma HIV viraemia (UV) or low-level viraemia (LLV) in the 18 months before T2. Plasma levels of sCD163 and of sCD14 were comparable in patients with UV and in subjects with LVL at T0, T1 and T2. The HIV DNA level was positively correlated with LLV but not with sCD163 and sCD14 levels; these two markers of inflammation were positively correlated (p = 0.017). Soluble CD163 and sCD14 decreased over time from T0 to T2 (p = 0.000 and p = 0.034, respectively). In conclusion, the significant decrease in sCD163 and sCD14 levels in patients cured of HCV infection, regardless of the presence of LLV, suggests a main role for HCV in immune activation in HIV–HCV co-infected patients.

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Sherman KE, Rouster SD, Chung RT, Rajicic N. Hepatitis C (2002) Virus prevalence among patients infected with human immunodeficiency virus: a cross-sectional analysis of the US adult AIDS Clinical Trials Group. Clin Infect Dis 34:831–837. https://doi.org/10.1086/339042 CrossRefPubMed

Sulkowski MS, Mehta SH, Torbenson MS, Higgins Y, Brinkley SC, de Oca RM, Moore RD, Afdhal NH, Thomas DL (2007) Rapid fibrosis progression among HIV/hepatitis C virus-co-infected adults. AIDS 21:2209–2216. https://doi.org/10.1097/QAD.0b013e3282f10de9 CrossRefPubMed

Knudsen TB, Ertner G, Petersen J, Møller HJ, Moestrup SK, Eugen-Olsen J, Kronborg G, Benfield T (2016) Plasma soluble CD163 level independently predicts all-cause mortality in HIV-1-infected individuals. J Infect Dis 214:1198–1204. https://doi.org/10.1093/infdis/jiw263 CrossRefPubMed

Sandler NG, Wand H, Roque A, Law M, Nason MC, Nixon DE, Pedersen C, Ruxrungtham K, Lewin SR, Emery S, Neaton JD, Brenchley JM, Deeks SG, Sereti I, Douek DC (2011) Plasma levels of soluble CD14 independently predict mortality in HIV infection. J Infect Dis 203:780–790. https://doi.org/10.1093/infdis/jiq118 CrossRefPubMedPubMedCentral

Møller HJ, Grønbaek H, Schiødt FV, Holland-Fischer P, Schilsky M, Munoz S, Hassanein T, Lee WM (2007) Soluble CD163 from activated macrophages predicts mortality in acute liver failure. J Hepatol 47:671–676. https://doi.org/10.1016/j.jhep.2007.05.014 CrossRefPubMedPubMedCentral

Dultz G, Gerber L, Zeuzem S, Sarrazin C, Waidmann O (2016) The macrophage activation marker CD163 is associated with IL28B genotype and hepatic inflammation in chronic hepatitis C virus infected patients. J Viral Hepat 23:267–273. https://doi.org/10.1111/jvh.12488 CrossRefPubMed

Hepatitis C (2015) guidance: AASLD-IDSA recommendations for testing, managing, and treating adults infected with hepatitis C virus. Hepatology 62:932–954. https://doi.org/10.1002/hep.27950 CrossRef

EACS (2017) EACS Guidelines Version 9.0 October 2017

Sikavi C, Chen PH, Lee AD, Saab EG, Choi G, Saab S (2017) Hepatitis C and human immunodeficiency virus co-infection in the era of direct-acting antiviral agents: no longer a difficult to treat population. Hepatology. https://doi.org/10.1002/hep.29642. (Epub ahead of print)CrossRef

10.

Simmons B, Saleem J, Heath K, Cooke GS, Hill A (2015) Long-term treatment outcomes of patients infected with hepatitis C virus: a systematic review and meta-analysis of the survival benefit of achieving a sustained virological response. Clin Infect Dis 61:730–740. https://doi.org/10.1093/cid/civ396 CrossRefPubMedPubMedCentral

11.

Berenguer J, Rodríguez-Castellano E, Carrero A, Von Wichmann MA, Montero M, Galindo MJ, Mallolas J, Crespo M, Téllez MJ, Quereda C, Sanz J, Barros C, Tural C, Santos I, Pulido F, Guardiola JM, Rubio R, Ortega E, Montes ML, Jusdado JJ, Gaspar G, Esteban H, Bellón JM, González-García J (2017) Eradication of hepatitis C virus and non-liver-related non-acquired immune deficiency syndrome-related events in human immunodeficiency virus/hepatitis C virus coinfection. Hepatology 66:344–356. https://doi.org/10.1002/hep.29071 CrossRefPubMedPubMedCentral

12.

Wong JK, Hezareh M, Günthard HF, Havlir DV, Ignacio CC, Spina CA, Richman DD (1997) Recovery of replication-competent HIV despite prolonged suppression of plasma viremia. Science 278:1291–1295CrossRefPubMed

13.

Sarmati L, D’Ettorre G, Parisi SG, Andreoni M (2015) HIV replication at low copy number and its correlation with the HIV reservoir: a clinical perspective. Curr HIV Res 13:250–257. https://doi.org/10.2174/1570162X13666150407142539 CrossRefPubMedPubMedCentral

14.

Parisi SG, Andreis S, Basso M, Cavinato S, Scaggiante R, Franzetti M, Andreoni M, Palù G, Cattelan AM (2017) Time course of cellular HIV-DNA and low-level HIV viremia in HIV–HCV co-infected patients whose HCV infection had been successfully treated with directly acting antivirals. Med Microbiol Immunol 206:419–428. https://doi.org/10.1007/s00430-017-0518- CrossRefPubMed

15.

Rozera G, Fabbri G, Lorenzini P, Mastrorosa I, Timelli L, Zaccarelli M, Amendola A, Vergori A, Plazzi MM, Cicalini S, Antinori A, Capobianchi MR, Abbate I, Ammassari A (2017) Peripheral blood HIV-1 DNA dynamics in antiretroviral-treated HIV/HCV co-infected patients receiving directly-acting antivirals. PLoS One 12:e0187095. https://doi.org/10.1371/journal.pone.0187095 CrossRefPubMedPubMedCentral

16.

Højen JF, Rasmussen TA, Andersen KL, Winckelmann AA, Laursen RR, Gunst JD, Møller HJ, Fujita M, Østergaard L, Søgaard OS, Dinarello CA, Tolstrup M (2015) Interleukin-37 expression is increased in chronic HIV-1-infected individuals and is associated with inflammation and the size of the total viral reservoir. Mol Med 21:337–345. https://doi.org/10.2119/molmed.2015.00031 CrossRefPubMedPubMedCentral

17.

Mascia C, Lichtner M, Zuccalà P, Vita S, Tieghi T, Marocco R, Savinelli S, Rossi R, Iannetta M, Campagna M, Schiavone F, Mengoni F, Russo G, Mastroianni CM, Vullo V (2017) Active HCV infection is associated with increased circulating levels of interferon-gamma (IFN-γ)-inducible protein-10 (IP-10), soluble CD163 and inflammatory monocytes regardless of liver fibrosis and HIV coinfection. Clin Res Hepatol Gastroenterol 41:644–655. https://doi.org/10.1016/j.clinre.2017.04.007 CrossRefPubMed

18.

Castéra L, Vergniol J, Foucher J, Le Bail B, Chanteloup E, Haaser M, Darriet M, Couzigou P, De Lédinghen V (2005) Prospective comparison of transient elastography, Fibrotest, APRI, and liver biopsy for the assessment of fibrosis in chronic hepatitis C. Gastroenterology 128:343–350. https://doi.org/10.1053/j.gastro.2004.11.018 CrossRefPubMed

19.

Parisi SG, Andreis S, Mengoli C, Scaggiante R, Ferretto R, Manfrin V, Cruciani M, Giobbia M, Boldrin C, Basso M, Andreoni M, Palù G, Sarmati L (2012) Baseline cellular HIV DNA load predicts HIV DNA decline and residual HIV plasma levels during effective antiretroviral therapy. J Clin Microbiol 50:258–263. https://doi.org/10.1128/JCM.06022-11 CrossRefPubMedPubMedCentral

20.

Hepatitis Drug Interactions website, website, http://www.hepdruginteractions.org. Accessed 12 Oct 2017

21.

Parisi SG, Sarmati L, Andreis S, Scaggiante R, Cruciani M, Ferretto R, Manfrin V, Basso M, Andreoni M, Mengoli C, Palù G (2015) Strong and persistent correlation between baseline and follow-up HIV-DNA levels and residual viremia in a population of naïve patients with more than 4 years of effective antiretroviral therapy. Clin Microbiol Infect 21:288.e5-7. https://doi.org/10.1016/j.cmi.2014.10.009 CrossRefPubMed

22.

Besson GJ, Lalama CM, Bosch RJ, Gandhi RT, Bedison MA, Aga E, Riddler SA, McMahon DK, Hong F, Mellors JW (2014) HIV-1 DNA decay dynamics in blood during more than a decade of suppressive antiretroviral therapy. Clin Infect Dis 59:1312–1321. https://doi.org/10.1093/cid/ciu585 CrossRefPubMedPubMedCentral

23.

McComsey G, Kitch D, Daar ES, Tierney C, Jahed NC, Melbourne K, Ha B, Brown TT, Bloom A, Fedarko N, Sax PE (2012) Inflammation markers after randomization to abacavir/lamivudine or tenofovir/emtricitabine with efavirenz or atazanavir/ritonavir. AIDS 26:1371–1385. https://doi.org/10.1097/QAD.0b013e328354f4fb CrossRefPubMedPubMedCentral

24.

Kirkegaard-Klitbo DM, Mejer N, Knudsen TB, Møller HJ, Moestrup SK, Poulsen SD, Kronborg G, Benfield T (2017) Soluble CD163 predicts incident chronic lung, kidney and liver disease in HIV infection. AIDS 31:981–988. https://doi.org/10.1097/QAD.0000000000001432 CrossRefPubMed

25.

Weaver LK, Hintz-Goldstein KA, Pioli PA, Wardwell K, Qureshi N, Vogel SN, Guyre PM (2006) Pivotal advance: activation of cell surface toll-like receptors causes shedding of the hemoglobin scavenger receptor CD163. J Leukoc Biol 80:26–35. https://doi.org/10.1189/jlb.1205756 CrossRefPubMed

26.

Etzerodt A, Rasmussen MR, Svendsen P, Chalaris A, Schwarz J, Galea I, Møller HJ, Moestrup SK (2014) Structural basis for inflammation-driven shedding of CD163 ectodomain and tumor necrosis factor-α in macrophages. J Biol Chem 289:778–788. https://doi.org/10.1074/jbc.M113.520213 CrossRefPubMed

27.

Kitchens RL, Thompson PA (2005) Modulatory effects of sCD14 and LBP on LPS-host cell interactions. J Endotoxin Res 11:225–229. https://doi.org/10.1179/096805105X46565 CrossRefPubMed

28.

Brenchley JM, Price DA, Schacker TW, Asher TE, Silvestri G, Rao S, Kazzaz Z, Bornstein E, Lambotte O, Altmann D, Blazar BR, Rodriguez B, Teixeira-Johnson L, Landay A, Martin JN, Hecht FM, Picker LJ, Lederman MM, Deeks SG, Douek DC (2006) Microbial translocation is a cause of systemic immune activation in chronic HIV infection. Nat Med 12:1365–1371. https://doi.org/10.1038/nm1511 CrossRefPubMed

29.

Hatano H, Jain V, Hunt PW, Lee TH, Sinclair E, Do TD, Hoh R, Martin JN, McCune JM, Hecht F, Busch MP, Deeks SG (2013) Cell-based measures of viral persistence are associated with immune activation and programmed cell death protein 1 (PD-1)-expressing CD4 + T cells. J Infect Dis 208:50–56. https://doi.org/10.1093/infdis/jis630 CrossRefPubMed

30.

Mavigner M, Delobel P, Cazabat M, Dubois M, L’faqihi-Olive FE, Raymond S, Pasquier C, Marchou B, Massip P, Izopet J (2009) HIV-1 residual viremia correlates with persistent T-cell activation in poor immunological responders to combination antiretroviral therapy. PLoS One 4:e7658. https://doi.org/10.1371/journal.pone.0007658. DOI:10.1371/journal.pone.0007658CrossRefPubMedPubMedCentral

31.

Falasca F, Di Carlo D, De Vito C, Bon I, d’Ettorre G, Fantauzzi A, Mezzaroma I, Fimiani C, Re MC, Vullo V, Antonelli G, Turriziani O (2017) Evaluation of HIV-DNA and inflammatory markers in HIV-infected individuals with different viral load patterns. BMC Infect Dis 17:581. https://doi.org/10.1186/s12879-017-2676-2 CrossRefPubMedPubMedCentral

32.

Cihlar T, Fordyce M (2016) Current status and prospects of HIV treatment. Curr Opin Virol 18:50–56. https://doi.org/10.1016/j.coviro.2016.03.004 CrossRefPubMed

33.

Kostadinova L, Shive CL, Judge C, Zebrowski E, Compan A, Rife K, Hirsch A, Falck-Ytter Y, Schlatzer DM, Li X, Chance MR, Rodriguez B, Popkin DL, Anthony DD (2016) During hepatitis C virus (HCV) infection and HCV-HIV coinfection, an elevated plasma level of autotaxin is associated with lysophosphatidic acid and markers of immune activation that normalize during interferon-free HCV Therapy. J Infect Dis 214:1438–1448. https://doi.org/10.1093/infdis/jiw372 CrossRefPubMed

34.

Mascia C, Vita S, Zuccalà P, Marocco R, Tieghi T, Savinelli S, Rossi R, Iannetta M, Pozzetto I, Furlan C, Mengoni F, Mastroianni CM, Vullo V, Lichtner M (2017) Changes in inflammatory biomarkers in HCV-infected patients undergoing direct acting antiviral-containing regimens with or without interferon. PLoS One 12:e0179400. https://doi.org/10.1371/journal.pone.0179400 CrossRefPubMedPubMedCentral

35.

Chew KW, Hua L, Bhattacharya D, Butt AA, Bornfleth L, Chung RT, Andersen JW, Currier JS (2014) The effect of hepatitis C virologic clearance on cardiovascular disease biomarkers in human immunodeficiency virus/hepatitis C virus coinfection. Open Forum Infect Dis 1:ofu104. https://doi.org/10.1093/ofid/ofu104 CrossRefPubMedPubMedCentral

36.

León A, Leal L, Torres B, Lucero C, Inciarte A, Arnedo M, Plana M, Vila J, Gatell JM, García F (2015) Association of microbial translocation biomarkers with clinical outcome in controllers HIV-infected patients. AIDS 29:675–681. https://doi.org/10.1097/QAD.0000000000000596 CrossRefPubMed

37.

Kazankov K, Barrera F, Møller HJ, Bibby BM, Vilstrup H, George J, Grønbaek H (2014) Soluble CD163, a macrophage activation marker, is independently associated with fibrosis in patients with chronic viral hepatitis B and C. Hepatology 60:521–530. https://doi.org/10.1002/hep.27129 CrossRefPubMed

38.

Gandhi RT, McMahon DK, Bosch RJ, Lalama CM, Cyktor JC, Macatangay BJ, Rinaldo CR, Riddler SA, Hogg E, Godfrey C, Collier AC, Eron JJ, Mellors JW (2017) Levels of HIV-1 persistence on antiretroviral therapy are not associated with markers of inflammation or activation. PLoS Pathog 13:e1006285. https://doi.org/10.1371/journal.ppat.1006285 CrossRefPubMedPubMedCentral

39.

Shmagel KV, Saidakova EV, Shmagel NG, Korolevskaya LB, Chereshnev VA, Robinson J, Grivel JC, Douek DC, Margolis L, Anthony DD, Lederman MM (2016) Systemic inflammation and liver damage in HIV/hepatitis C virus coinfection. HIV Med 17:581–589. https://doi.org/10.1111/hiv.12357 CrossRefPubMedPubMedCentral

40.

Sarmati L, Parisi SG, Nicastri E, d’Ettorre G, Palmisano L, Andreotti M, Andreoni C, Giuliano M, Gatti F, Boldrin C, Palù G, Vullo V, Vella S, Andreoni M (2005) Association between cellular human immunodeficiency virus DNA level and immunological parameters in patients with undetectable plasma viremia level during highly active antiretroviral therapy. J Clin Microbiol 43:6183–6185. https://doi.org/10.1128/JCM.43.12.6183-6185.2005 CrossRefPubMedPubMedCentral

41.

Burgard M, Boufassa F, Viard JP, Garrigue I, Ruffault A, Izopet J, Vabret A, Descamps D, Colson P, Seigneurin JM, Rouzioux C (2009) Factors influencing peripheral blood mononuclear cell associated HIV-1 DNA level after long-term suppressive antiretroviral therapy in 236 patients. AIDS 23:2165–2171. https://doi.org/10.1097/QAD.0b013e32833032d4 CrossRefPubMed

42.

Fourati S, Flandre P, Calin R, Carcelain G, Soulie C, Lambert-Niclot S, Maiga A, Ait-Arkoub Z, Tubiana R, Valantin MA, Autran B, Katlama C, Calvez V, Marcelin AG (2014) Factors associated with a low HIV reservoir in patients with prolonged suppressive antiretroviral therapy. J Antimicrob Chemother 69:753–766. https://doi.org/10.1093/jac/dkt428 CrossRefPubMed

Title: Soluble CD163 and soluble CD14 plasma levels but not cellular HIV-DNA decrease during successful interferon-free anti-HCV therapy in HIV-1–HCV co-infected patients on effective combined anti-HIV treatment
Authors: Saverio G. Parisi
Samantha Andreis
Carlo Mengoli
Nicola Menegotto
Silvia Cavinato
Renzo Scaggiante
Massimo Andreoni
Giorgio Palù
Monica Basso
Anna Maria Cattelan
Publication date: 01-08-2018
Publisher: Springer Berlin Heidelberg
Published in: Medical Microbiology and Immunology / Issue 3-4/2018
Print ISSN: 0300-8584
Electronic ISSN: 1432-1831
DOI: https://doi.org/10.1007/s00430-018-0538-1

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Soluble CD163 and soluble CD14 plasma levels but not cellular HIV-DNA decrease during successful interferon-free anti-HCV therapy in HIV-1–HCV co-infected patients on effective combined anti-HIV treatment

Abstract

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