Research Article| Volume 67, ISSUE 2, P255-262, August 2017

Lack of decline in hepatitis C virus incidence among HIV-positive men who have sex with men during 1990–2014

Published:April 13, 2017DOI:

      Background & Aims

      Hepatitis C virus (HCV) incidence among HIV-positive men who have sex with men (MSM) has increased since 2000, although there are regional differences. We aimed to 1) estimate trends in HCV incidence among HIV-positive MSM, 2) assess the association between incidence and geographical region, age and HIV-related measurements and, 3) assess temporal changes from HIV seroconversion to HCV infection.


      Data was used from MSM with well-estimated dates of HIV seroconversion from the CASCADE Collaboration (1990–2014). Smoothly varying trends in HCV incidence over time were allowed, using restricted cubic splines. The association of calendar year, age, CD4 count (lagged), HIV RNA (lagged), geographical region and HIV infection stage (recent vs. chronic) with HCV incidence were assessed using Poisson regression.


      Of 5,941 MSM, 337 acquired HCV during follow-up. HCV incidence significantly increased from 0.7/1,000 person-years in 1990 to 18/1,000 person-years in 2014. Recent calendar years, younger age, recent HIV infection and higher HIV RNA levels were significantly associated with HCV incidence, while CD4 count was not. Trends differed by geographical region; while incidence appeared to have stabilized in Western Europe and remained stable in Southern Europe, it continued to increase in Northern Europe in recent years. Time from HIV to HCV infection significantly decreased over time (p <0.001).


      HCV has continued to spread among HIV-positive MSM in recent years, but trends differ by geographical region. Interventions to decrease the risk of HCV acquisition and increase early diagnosis are warranted.

      Lay summary

      Hepatitis C virus infection continues to spread among HIV-positive men who have sex with men, especially among younger individuals. However, trends seem to differ by European region in recent years. Furthermore, men who have sex with men with a higher HIV RNA load were more likely to get infected with the hepatitis C virus. During recent HIV infection, MSM appear to be at higher risk of acquiring hepatitis C.

      Graphical abstract


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      Author names in bold designate shared co-first authorship

        • van der Helm J.J.
        • Prins M.
        • del Amo J.
        • Bucher H.C.
        • Chene G.
        • Dorrucci M.
        • et al.
        The hepatitis C epidemic among HIV-positive MSM: incidence estimates from 1990 to 2007.
        AIDS. 2011; 25: 1083-1091
        • Hagan H.
        • Jordan A.E.
        • Neurer J.
        • Cleland C.M.
        Incidence of sexually transmitted hepatitis C virus infection in HIV-positive men who have sex with men.
        AIDS. 2015; 29: 2335-2345
        • Vanhommerig J.W.
        • Stolte I.G.
        • Lambers F.A.
        • Geskus R.B.
        • van de Laar T.J.
        • Bruisten S.M.
        • et al.
        Stabilizing incidence of hepatitis C virus infection among men who have sex with men in Amsterdam.
        J Acquir Immune Defic Syndr. 2014; 66: e111-e115
        • Wandeler G.
        • Gsponer T.
        • Bregenzer A.
        • Gunthard H.F.
        • Clerc O.
        • Calmy A.
        • Rauch A.
        Hepatitis C virus infections in the Swiss HIV Cohort Study: a rapidly evolving epidemic.
        Clin Infect Dis. 2012; 55: 1408-1416
      1. CDC. Sexual transmission of hepatitis C virus among HIV-infected men who have sex with men-New York City, 2005-2010.
        MMWR Morb Mortal Wkly Rep. 2011; 60: 945-950
        • Apers L.
        • Vanden Berghe W.
        • De W.S.
        • Kabeya K.
        • Callens S.
        • Buyze J.
        • et al.
        Risk factors for HCV acquisition among HIV-positive MSM in Belgium.
        J Acquir Immune Defic Syndr. 2015; 68: 585-593
        • Nishijima T.
        • Shimbo T.
        • Komatsu H.
        • Hamada Y.
        • Gatanaga H.
        • Oka S.
        Incidence and risk factors for incident Hepatitis C infection among men who have sex with men with HIV-1 infection in a large Urban HIV clinic in Tokyo.
        J Acquir Immune Defic Syndr. 2014; 65: 213-217
        • Schmidt A.J.
        • Rockstroh J.K.
        • Vogel M.
        • An der H.M.
        • Baillot A.
        • Krznaric I.
        • et al.
        Trouble with bleeding: risk factors for acute hepatitis C among HIV-positive gay men from Germany–a case-control study.
        PLoS One. 2011; 6: e17781
        • Vanhommerig J.W.
        • Lambers F.A.
        • Schinkel J.
        • Geskus R.B.
        • Arends J.E.
        • van de Laar T.J.
        • et al.
        Risk factors for sexual transmission of hepatitis C virus among human immunodeficiency virus-infected men who have sex with men: a case-control study.
        Open Forum Infect Dis. 2015; 2: ofv115
        • Witt M.D.
        • Seaberg E.C.
        • Darilay A.
        • Young S.
        • Badri S.
        • Rinaldo C.R.
        • et al.
        Incident hepatitis C virus infection in men who have sex with men: a prospective cohort analysis, 1984–2011.
        Clin Infect Dis. 2013; 57: 77-84
        • van de Laar T.J.
        • Matthews G.V.
        • Prins M.
        • Danta M.
        Acute hepatitis C in HIV-infected men who have sex with men: an emerging sexually transmitted infection.
        AIDS. 2010; 24: 1799-1812
        • Burchell A.N.
        • Gardner S.L.
        • Mazzulli T.
        • Manno M.
        • Raboud J.
        • Allen V.G.
        • et al.
        Hepatitis C virus seroconversion among HIV-positive men who have sex with men with no history of injection drug use: Results from a clinical HIV cohort.
        Can J Infect Dis Med Microbiol. 2015; 26: 17-22
      2. CASCADE Collaboration. Changes in the uptake of antiretroviral therapy and survival in people with known duration of HIV infection in Europe: results from CASCADE.
        HIV Med. 2000; 1: 224-231
      3. United Nations (UN). Composition of macro geographical (continental) regions, geographical sub-regions, and selected economic and other groupings. 2016. Retrieved January 10, 2016 from

        • Vanhommerig J.W.
        • Thomas X.V.
        • van der Meer J.T.
        • Geskus R.B.
        • Bruisten S.M.
        • Molenkamp R.
        • et al.
        Hepatitis C virus (HCV) antibody dynamics following acute HCV infection and reinfection among HIV-infected men who have sex with men.
        Clin Infect Dis. 2014; 59: 1678-1685
        • Thomson E.C.
        • Nastouli E.
        • Main J.
        • Karayiannis P.
        • Eliahoo J.
        • Muir D.
        • et al.
        Delayed anti-HCV antibody response in HIV-positive men acutely infected with HCV.
        AIDS. 2009; 23: 89-93
      4. R: A language and environment for statistical computing (version 3.2.2, R Foundation for Statistical Computing, Vienna, Austria. URL, 2016.

      5. StataCorp. 2013. Stata Statistical Software: Release 13.
        StataCorp LP, College Station, TX2016
        • Boesecke C.
        • Grint D.
        • Soriano V.
        • Lundgren J.D.
        • d'Arminio M.A.
        • Mitsura V.M.
        • et al.
        Hepatitis C seroconversions in HIV infection across Europe: which regions and patient groups are affected?.
        Liver Int. 2015; 35: 2384-2391
        • Muriuki B.M.
        • Gicheru M.M.
        • Wachira D.
        • Nyamache A.K.
        • Khamadi S.A.
        Prevalence of hepatitis B and C viral co-infections among HIV-1 infected individuals in Nairobi, Kenya.
        BMC Res Notes. 2013; 9: 363
        • Paz-Bailey G.
        • Mendoza M.C.
        • Finlayson T.
        • Wejnert C.
        • Le B.
        • Rose C.
        • et al.
        Trends in condom use among MSM in the United States: the role of antiretroviral therapy and seroadaptive strategies.
        AIDS. 2016; 30: 1985-1990
        • Jansen I.A.
        • Geskus R.B.
        • Davidovich U.
        • Jurriaans S.
        • Coutinho R.A.
        • Prins M.
        • et al.
        Ongoing HIV-1 transmission among men who have sex with men in Amsterdam: a 25-year prospective cohort study.
        AIDS. 2011; 25: 493-501
        • Abara W.E.
        • Hess K.L.
        • Neblett F.R.
        • Bernstein K.T.
        • Paz-Bailey G.
        Syphilis Trends among Men Who Have Sex with Men in the United States and Western Europe: A Systematic Review of Trend Studies Published between 2004 and 2015.
        PLoS One. 2016; 11: e0159309
        • Giorgetti R.
        • Tagliabracci A.
        • Schifano F.
        • Zaami S.
        • Marinelli E.
        • Busardo F.P.
        When “chems” meet sex: a rising phenomenon called “ChemSex”.
        Curr Neuropharmacol. 2016; ([epub ahead of print])
        • Schmidt A.J.
        • Bourne A.
        • Weatherburn P.
        • Reid D.
        • Marcus U.
        • Hickson F.
        Illicit drug use among gay and bisexual men in 44 cities: Findings from the European MSM Internet Survey (EMIS).
        Int J Drug Policy. 2016; 24: 4-12
      6. EASL recommendations on treatment of hepatitis C 2015.
        J Hepatol. 2015; 63: 199-236
        • Martin N.K.
        • Thornton A.
        • Hickman M.
        • Sabin C.
        • Nelson M.
        • Cooke G.S.
        • et al.
        Can hepatitis C virus (HCV) direct-acting antiviral treatment as prevention reverse the hcv epidemic among men who have sex with men in the United Kingdom? Epidemiological and modeling insights.
        Clin Infect Dis. 2016; 62: 1072-1080
        • Salazar-Vizcaya L.
        • Kouyos R.D.
        • Zahnd C.
        • Wandeler G.
        • Battegay M.
        • Darling K.E.
        • et al.
        Hepatitis C virus transmission among human immunodeficiency virus-infected men who have sex with men: Modeling the effect of behavioral and treatment interventions.
        Hepatology. 2016; 64: 1856-1869
      7. Nijmeijer B, Sarrami Forooshani R, Steba G, Geijtenbeek T.B.H. Immune activation by HIV-1 enhances sexual transmission of HCV. 2016. Presented at the 10th Netherlands Conference on HIV Pathogenesis, Epidemiology and Treatment. Abstract number:08

        • Modjarrad K.
        • Vermund S.H.
        Effect of treating co-infections on HIV-1 viral load: a systematic review.
        Lancet Infect Dis. 2010; 10: 455-463
        • Lea T.
        • Mao L.
        • Hopwood M.
        • Prestage G.
        • Zablotska I.
        • de Wit J.
        • et al.
        Methamphetamine use among gay and bisexual men in Australia: Trends in recent and regular use from the Gay Community Periodic Surveys.
        Int J Drug Policy. 2016; 29: 66-72
      8. Acute hepatitis C in HIV-infected individuals: recommendations from the European AIDS Treatment Network (NEAT) consensus conference.
        AIDS. 2011; 25: 399-409