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RESEARCH ARTICLE (Open Access)

Hepatitis C virus infection in HIV-infected men in Singapore, 2006–2018: incidence and associated factors

Li Wei Ang https://orcid.org/0000-0002-0036-255X A G , Chiaw Yee Choy B , Oon Tek Ng B C D , Yee Sin Leo B C D E F and Chen Seong Wong B C D
+ Author Affiliations
- Author Affiliations

A National Public Health and Epidemiology Unit, National Centre for Infectious Diseases, 16 Jalan Tan Tock Seng, 308442, Singapore.

B Department of Infectious Diseases, National Centre for Infectious Diseases, 16 Jalan Tan Tock Seng, 308442, Singapore.

C Department of Infectious Diseases, Tan Tock Seng Hospital, 11 Jalan Tan Tock Seng, 308433, Singapore.

D Lee Kong Chian School of Medicine, Nanyang Technological University, 11 Mandalay Road, 308232, Singapore.

E Saw Swee Hock School of Public Health, National University of Singapore, 16 Medical Drive, 117597, Singapore.

F Yong Loo Lin School of Medicine, National University of Singapore, 10 Medical Drive, 117597, Singapore.

G Corresponding author. Email: Li_Wei_Ang@ncid.sg

Sexual Health 18(3) 221-231 https://doi.org/10.1071/SH20197
Submitted: 31 October 2020  Accepted: 23 February 2021   Published: 21 June 2021

Journal Compilation © CSIRO 2021 Open Access CC BY-NC

Abstract

Background: The epidemiology of hepatitis C virus (HCV) infection in people living with HIV has been evolving, with increasing evidence of permucosal (sexual) transmission identified predominantly in HIV-positive men who have sex with men (MSM). The aim of this study was to estimate the incidence rate and elucidate epidemiological factors associated with HCV infection among HIV-infected men in Singapore from 2006 to 2018. Methods: A retrospective cohort study was conducted using a clinical database maintained by the Clinical HIV Program at the National Centre for Infectious Diseases, Singapore. Factors associated with incident HCV infections were identified using Cox proportional hazards regression analyses. Results: Among 1348 HIV-infected male patients who were HCV seronegative at baseline, 64 (4.7%) subsequently tested positive for HCV, giving an incidence of 0.88 per 100 person-years of follow-up (PYFU) (95% confidence interval (CI) 0.69–1.13). The incidence rate of HCV seroconversion increased from 0.33 (95% CI 0.12–0.71) per 100 PYFU in 2010–2012 to 1.93 (95% CI 1.36–2.67) in 2016–2018. Independent factors associated with incident HCV infection were younger age groups at HIV diagnosis versus ≥45 years, HIV acquisition via MSM or via both sexual contact and intravenous drug use versus heterosexual transmission, HIV diagnosis in later periods versus 2006–2009, and recent syphilis acquisition. Conclusions: An increasing trend of incident HCV infection was seen in HIV-infected men, particularly for MSM. Preventive and behavioural interventions should be targeted at HIV-infected individuals engaged in high-risk sexual behaviour.

Keywords: co-infections, HIV/AIDS, men who have sex with men, syphilis, hepatitis C virus infection, epidemiology, risk factors, preventive intervention.


References

[1]  National Institutes of Health. HIV and opportunistic infections, coinfections, and conditions. 2020. Available at https://hivinfo.nih.gov/understanding-hiv/fact-sheets/hiv-and-hepatitis-c [accessed 24 October 2020].

[2]  Platt L, Easterbrook P, Gower E, McDonald B, Sabin K, McGowan C, et al Prevalence and burden of HCV co-infection in people living with HIV: a global systematic review and meta-analysis. Lancet Infect Dis 2016; 16 797–808.
Prevalence and burden of HCV co-infection in people living with HIV: a global systematic review and meta-analysis.Crossref | GoogleScholarGoogle Scholar | 26922272PubMed |

[3]  Salmon-Ceron D, Nahon P, Layese R, Bourcier V, Sogni P, Bani-Sadr F, et al Human immunodeficiency virus/hepatitis C virus (HCV) co-infected patients with cirrhosis are no longer at higher risk for hepatocellular carcinoma or end-stage liver disease as compared to HCV mono-infected patients. Hepatology 2019; 70 939–54.
Human immunodeficiency virus/hepatitis C virus (HCV) co-infected patients with cirrhosis are no longer at higher risk for hepatocellular carcinoma or end-stage liver disease as compared to HCV mono-infected patients.Crossref | GoogleScholarGoogle Scholar | 30569448PubMed |

[4]  Chen TY, Ding EL, Seage Iii GR, Kim AY. Meta-analysis: increased mortality associated with hepatitis C in HIV-infected persons is unrelated to HIV disease progression. Clin Infect Dis 2009; 49 1605–15.
Meta-analysis: increased mortality associated with hepatitis C in HIV-infected persons is unrelated to HIV disease progression.Crossref | GoogleScholarGoogle Scholar | 19842982PubMed |

[5]  World Health Organization. Combating hepatitis B and C to reach elimination by 2030. 2016. Available at https://www.who.int/hepatitis/publications/hep-elimination-by-2030-brief/en/ [accessed 10 December 2019].

[6]  Jin F, Matthews GV, Grulich AE. Sexual transmission of hepatitis C virus among gay and bisexual men: a systematic review. Sex Health 2017; 14 28–41.
Sexual transmission of hepatitis C virus among gay and bisexual men: a systematic review.Crossref | GoogleScholarGoogle Scholar | 27712618PubMed |

[7]  Browne R, Asboe D, Gilleece Y, Atkins M, Mandalia S, Gazzard B, et al Increased numbers of acute hepatitis C infections in HIV positive homosexual men: is sexual transmission feeding the increase? Sex Transm Infect 2004; 80 326–7.
Increased numbers of acute hepatitis C infections in HIV positive homosexual men: is sexual transmission feeding the increase?Crossref | GoogleScholarGoogle Scholar | 15295139PubMed |

[8]  Gambotti L, Batisse D, Colin-de-Verdiere N, Delaroque-Astagneau E, Desenclos JC, Dominguez S, et al Acute hepatitis C infection in HIV positive men who have sex with men in Paris, France, 2001–2004. Euro Surveill 2005; 10 535
Acute hepatitis C infection in HIV positive men who have sex with men in Paris, France, 2001–2004.Crossref | GoogleScholarGoogle Scholar |

[9]  Götz HM, van Doornum G, Niesters HG, den Hollander JG, Thio HB, de Zwart O. A cluster of acute hepatitis C virus infection among men who have sex with men: results from contact tracing and public health implications. AIDS 2005; 19 969–74.
A cluster of acute hepatitis C virus infection among men who have sex with men: results from contact tracing and public health implications.Crossref | GoogleScholarGoogle Scholar | 15905679PubMed |

[10]  Danta M, Brown D, Bhagani S, Pybus OG, Sabin CA, Nelson M, et al Recent epidemic of acute hepatitis C virus in HIV positive men who have sex with men linked to high-risk sexual behaviours. AIDS 2007; 21 983–91.
Recent epidemic of acute hepatitis C virus in HIV positive men who have sex with men linked to high-risk sexual behaviours.Crossref | GoogleScholarGoogle Scholar | 17457092PubMed |

[11]  Giraudon I, Ruf M, Maguire H, Charlett A, Ncube F, Turner J, et al Increase in diagnosed newly acquired hepatitis C in HIV-positive men who have sex with men across London and Brighton, 2002–2006: is this an outbreak? Sex Transm Infect 2008; 84 111–5.
Increase in diagnosed newly acquired hepatitis C in HIV-positive men who have sex with men across London and Brighton, 2002–2006: is this an outbreak?Crossref | GoogleScholarGoogle Scholar | 17932125PubMed |

[12]  Urbanus AT, van de Laar TJ, Stolte IG, Schinkel J, Heijman T, Coutinho RA, et al Hepatitis C virus infections among HIV infected men who have sex with men: an expanding epidemic. AIDS 2009; 23 F1–7.
Hepatitis C virus infections among HIV infected men who have sex with men: an expanding epidemic.Crossref | GoogleScholarGoogle Scholar | 19542864PubMed |

[13]  Rauch A, Rickenbach M, Weber R, Hirschel B, Tarr PE, Bucher HC, et al Unsafe sex and increased incidence of hepatitis C virus infection among HIV-infected men who have sex with men: the Swiss HIV Cohort Study. Clin Infect Dis 2005; 41 395–402.
Unsafe sex and increased incidence of hepatitis C virus infection among HIV-infected men who have sex with men: the Swiss HIV Cohort Study.Crossref | GoogleScholarGoogle Scholar | 16007539PubMed |

[14]  Bottieau E, Apers L, Van Esbroeck M, Vandenbruaene M, Florence E. Hepatitis C virus infection in HIV-infected men who have sex with men: sustained rising incidence in Antwerp, Belgium, 2001-2009. Euro Surveill 2010; 15 19673
Hepatitis C virus infection in HIV-infected men who have sex with men: sustained rising incidence in Antwerp, Belgium, 2001-2009.Crossref | GoogleScholarGoogle Scholar | 20929655PubMed |

[15]  Wandeler G, Gsponer T, Bregenzer A, Günthard HF, Clerc O, Calmy A, et al Hepatitis C virus infections in the Swiss HIV Cohort Study: a rapidly evolving epidemic. Clin Infect Dis 2012; 55 1408–16.
Hepatitis C virus infections in the Swiss HIV Cohort Study: a rapidly evolving epidemic.Crossref | GoogleScholarGoogle Scholar | 22893583PubMed |

[16]  van Santen DK, van der Helm JJ, Del Amo J, Meyer L, D’Arminio Monforte A, Price M, et al Lack of decline in hepatitis C virus incidence among HIV-positive men who have sex with men during 1990–2014. J Hepatol 2017; 67 255–62.
Lack of decline in hepatitis C virus incidence among HIV-positive men who have sex with men during 1990–2014.Crossref | GoogleScholarGoogle Scholar | 28412290PubMed |

[17]  Matthews GV, Hellard M, Kaldor J, Lloyd A, Dore GJ, et al Further evidence of HCV sexual transmission among HIV-positive men who have sex with men: response to Danta. AIDS 2007; 21 2112–3.
Further evidence of HCV sexual transmission among HIV-positive men who have sex with men: response to Danta.Crossref | GoogleScholarGoogle Scholar | 17885306PubMed |

[18]  Matthews GV, Hellard M, Haber P, Yeung B, Marks P, Baker D, et al Characteristics and treatment outcomes among HIV-infected individuals in the Australian Trial in Acute Hepatitis C. Clin Infect Dis 2009; 48 650–8.
Characteristics and treatment outcomes among HIV-infected individuals in the Australian Trial in Acute Hepatitis C.Crossref | GoogleScholarGoogle Scholar | 19191653PubMed |

[19]  Luetkemeyer A, Hare CB, Stansell J, Tien PC, Charlesbois E, Lum P, et al Clinical presentation and course of acute hepatitis C infection in HIV-infected patients. J Acquir Immune Defic Syndr 2006; 41 31–6.
Clinical presentation and course of acute hepatitis C infection in HIV-infected patients.Crossref | GoogleScholarGoogle Scholar | 16340470PubMed |

[20]  Samandari T, Tedaldi E, Armon C, Hart R, Chmiel JS, Brooks JT, et al Incidence of hepatitis C virus infection in the Human Immunodeficiency Virus Outpatient Study Cohort, 2000–2013. Open Forum Infect Dis 2017; 4 ofx076
Incidence of hepatitis C virus infection in the Human Immunodeficiency Virus Outpatient Study Cohort, 2000–2013.Crossref | GoogleScholarGoogle Scholar | 28616444PubMed |

[21]  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; 65 213–7.
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.Crossref | GoogleScholarGoogle Scholar | 24185533PubMed |

[22]  Lin AWC, Wong KH, Chan K. More safer sex intervention needed for HIV-positive MSM with higher education level for prevention of sexually transmitted hepatitis C. J Int AIDS Soc 2014; 17 19663
More safer sex intervention needed for HIV-positive MSM with higher education level for prevention of sexually transmitted hepatitis C.Crossref | GoogleScholarGoogle Scholar |

[23]  Lee S, Lee SH, Lee SJ, Kim KH, Lee JE, Cho H, et al Incidence and risk factors of hepatitis C virus infection among human immunodeficiency virus (HIV) patients in a large HIV clinic in South Korea. Korean J Intern Med 2016; 31 772–8.
Incidence and risk factors of hepatitis C virus infection among human immunodeficiency virus (HIV) patients in a large HIV clinic in South Korea.Crossref | GoogleScholarGoogle Scholar | 27117318PubMed |

[24]  Ho SY, Su LH, Sun HY, Huang YS, Chuang YC, Huang MH, et al Trends of recent hepatitis C virus infection among HIV-positive men who have sex with men in Taiwan, 2011–2018. EClinicalMedicine 2020; 24 100441
Trends of recent hepatitis C virus infection among HIV-positive men who have sex with men in Taiwan, 2011–2018.Crossref | GoogleScholarGoogle Scholar | 32637905PubMed |

[25]  Nijmeijer BM, Koopsen J, Schinkel J, Prins M, Geijtenbeek TB. Sexually transmitted hepatitis C virus infections: current trends, and recent advances in understanding the spread in men who have sex with men. J Int AIDS Soc 2019; 22 e25348
Sexually transmitted hepatitis C virus infections: current trends, and recent advances in understanding the spread in men who have sex with men.Crossref | GoogleScholarGoogle Scholar | 31468692PubMed |

[26]  Choy CY, Ang LW, Ng OT, Leo YS, Wong CS. Factors associated with hepatitis B and C co-infection among HIV-infected patients in Singapore, 2006–2017. Trop Med Infect Dis 2019; 4 87
Factors associated with hepatitis B and C co-infection among HIV-infected patients in Singapore, 2006–2017.Crossref | GoogleScholarGoogle Scholar |

[27]  Ministry of Health Singapore. Update on the HIV/AIDS situation in Singapore 2018 (June 2019). 2019. Available at https://www.moh.gov.sg/resources-statistics/infectious-disease-statistics/hiv-stats/update-on-the-hiv-aids-situation-in-singapore-2018-(june-2019) [accessed 30 September 2019].

[28]  Wong YJ, Cheen MH, Hsiang JC, Kumar R, Tan J, Teo EK, et al Economic evaluation of direct-acting antivirals for the treatment of genotype 3 hepatitis C infection in Singapore. JGH Open 2019; 3 210–6.
Economic evaluation of direct-acting antivirals for the treatment of genotype 3 hepatitis C infection in Singapore.Crossref | GoogleScholarGoogle Scholar | 31276038PubMed |

[29]  Soh BYM, Kumar R, Ekstrom VSM, Lin CYH, Thangaraju S, Tan HH, et al Prevalence of hepatitis C virus infection and the IL28B genotype polymorphism among blood donors and high-risk populations. Singapore Med J 2019; 60 34–9.
Prevalence of hepatitis C virus infection and the IL28B genotype polymorphism among blood donors and high-risk populations.Crossref | GoogleScholarGoogle Scholar | 29926111PubMed |

[30]  Chaillon A, Sun X, Cachay ER, Looney D, Wyles D, Garfein RS, et al Primary incidence of hepatitis C virus infection among HIV-infected men who have sex with men in San Diego, 2000–2015. Open Forum Infect Dis 2019; 6 ofz160
Primary incidence of hepatitis C virus infection among HIV-infected men who have sex with men in San Diego, 2000–2015.Crossref | GoogleScholarGoogle Scholar | 31041355PubMed |

[31]  Gamage DG, Read TR, Bradshaw CS, Hocking JS, Howley K, Chen MY, et al Incidence of hepatitis-C among HIV infected men who have sex with men (MSM) attending a sexual health service: a cohort study. BMC Infect Dis 2011; 11 39
Incidence of hepatitis-C among HIV infected men who have sex with men (MSM) attending a sexual health service: a cohort study.Crossref | GoogleScholarGoogle Scholar | 21291565PubMed |

[32]  Pradat P, Huleux T, Raffi F, Delobel P, Valantin M, Poizot-Martin I, et al Incidence of new hepatitis C virus infection is still increasing in French MSM living with HIV. AIDS 2018; 32 1077–82.
Incidence of new hepatitis C virus infection is still increasing in French MSM living with HIV.Crossref | GoogleScholarGoogle Scholar | 29438195PubMed |

[33]  van de Laar TJ, Van der Bij AK, Prins M, Bruisten SM, Brinkman K, Ruys TA, et al Increase in HCV incidence among men who have sex with men in Amsterdam most likely caused by sexual transmission. J Infect Dis 2007; 196 230–8.
Increase in HCV incidence among men who have sex with men in Amsterdam most likely caused by sexual transmission.Crossref | GoogleScholarGoogle Scholar | 17570110PubMed |

[34]  Medland NA, Chow EP, Bradshaw CS, Read TH, Sasadeusz JJ, Fairley CK. Predictors and incidence of sexually transmitted Hepatitis C virus infection in HIV positive men who have sex with men. BMC Infect Dis 2017; 17 185
Predictors and incidence of sexually transmitted Hepatitis C virus infection in HIV positive men who have sex with men.Crossref | GoogleScholarGoogle Scholar | 28253838PubMed |

[35]  Ang LW, Wong CS, Ng OT, Leo YS. Incidence of syphilis among HIV-infected men in Singapore, 2006–2017: temporal trends and associated risk factors. Sex Transm Infect 2020; 96 293–9.
Incidence of syphilis among HIV-infected men in Singapore, 2006–2017: temporal trends and associated risk factors.Crossref | GoogleScholarGoogle Scholar | 31371448PubMed |

[36]  Thurnheer MC, Weber R, Toutous-Trellu L, Cavassini M, Elzi L, Schmid P, et al Occurrence, risk factors, diagnosis and treatment of syphilis in the prospective observational Swiss HIV Cohort Study. AIDS 2010; 24 1907–16.
Occurrence, risk factors, diagnosis and treatment of syphilis in the prospective observational Swiss HIV Cohort Study.Crossref | GoogleScholarGoogle Scholar | 20616699PubMed |

[37]  Abara WE, Hess KL, Neblett Fanfair R, Bernstein KT, 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
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.Crossref | GoogleScholarGoogle Scholar | 27556925PubMed |

[38]  Kirby Institute. HIV, viral hepatitis and sexually transmissible infections in Australia: annual surveillance report 2017. Sydney: Kirby Institute, UNSW Sydney; 2017. Available at https://kirby.unsw.edu.au/sites/default/files/kirby/report/SERP_Annual-Surveillance-Report-2017_compressed.pdf [accessed 16 January 2020].

[39]  Tucker JD, Yin Y-P, Wang B, Chen X-S, Cohen MS. An expanding syphilis epidemic in China: epidemiology, behavioural risk and control strategies with a focus on low-tier female sex workers and men who have sex with men. Sex Transm Infect 2011; 87 ii16–8.
An expanding syphilis epidemic in China: epidemiology, behavioural risk and control strategies with a focus on low-tier female sex workers and men who have sex with men.Crossref | GoogleScholarGoogle Scholar | 22110145PubMed |

[40]  Action for AIDS Singapore. Press Room: MSM outreach HIV testing project round 6 (2013). 2013. Available at https://afa.org.sg/portfolio-item/msm-outreach-hiv-testing-project-round-6/ [accessed 15 February 2019].

[41]  Wee S, Barrett ME, Lian WM, Jayabaskar T, Chan KW. Determinants of inconsistent condom use with female sex workers among men attending the STD clinic in Singapore. Sex Transm Infect 2004; 80 310–4.
Determinants of inconsistent condom use with female sex workers among men attending the STD clinic in Singapore.Crossref | GoogleScholarGoogle Scholar | 15295132PubMed |

[42]  Wong ML, Sen P, Wong CM, Tjahjadi S, Govender M, Koh TT, et al Human immunodeficiency virus (HIV) prevention education in Singapore: challenges for the future. Ann Acad Med Singap 2012; 41 602–9.
| 23303119PubMed |

[43]  Hoornenborg E, Achterbergh RCA, Schim van der Loeff MF, Davidovich U, Hogewoning A, de Vries HJC, et al MSM starting preexposure prophylaxis are at risk of hepatitis C virus infection. AIDS 2017; 31 1603–10.
MSM starting preexposure prophylaxis are at risk of hepatitis C virus infection.Crossref | GoogleScholarGoogle Scholar | 28657964PubMed |

[44]  Hasse B, Ledergerber B, Hirschel B, Vernazza P, Glass TR, Jeannin A, et al Frequency and determinants of unprotected sex among HIV-infected persons: the Swiss HIV cohort study. Clin Infect Dis 2010; 51 1314–22.
Frequency and determinants of unprotected sex among HIV-infected persons: the Swiss HIV cohort study.Crossref | GoogleScholarGoogle Scholar | 21034200PubMed |

[45]  Hagan H, Jordan AE, Neurer J, Cleland CM. Incidence of sexually transmitted hepatitis C virus infection in HIV-positive men who have sex with men. AIDS 2015; 29 2335–45.
Incidence of sexually transmitted hepatitis C virus infection in HIV-positive men who have sex with men.Crossref | GoogleScholarGoogle Scholar | 26258525PubMed |

[46]  Centers for Disease Control and Prevention (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; 60 945–50.
| 21775948PubMed |

[47]  van de Laar T, Pybus O, Bruisten S, Brown D, Nelson M, Bhagani S, et al Evidence of a large, international network of HCV transmission in HIV-positive men who have sex with men. Gastroenterology 2009; 136 1609–17.
Evidence of a large, international network of HCV transmission in HIV-positive men who have sex with men.Crossref | GoogleScholarGoogle Scholar | 19422083PubMed |

[48]  Serpaggi J, Chaix ML, Batisse D, Dupont C, Vallet-Pichard A, Fontaine H, et al Sexually transmitted acute infection with a clustered genotype 4 hepatitis C virus in HIV-1-infected men and inefficacy of early antiviral therapy. AIDS 2006; 20 233–40.
Sexually transmitted acute infection with a clustered genotype 4 hepatitis C virus in HIV-1-infected men and inefficacy of early antiviral therapy.Crossref | GoogleScholarGoogle Scholar | 16511416PubMed |

[49]  van de Laar T, Pybus O, Bruisten S, Brown D, Nelson M, Bhagani S, et al Evidence of a large, international network of HCV transmission in HIV-positive men who have sex with men. Gastroenterology 2009; 136 1609–17.
Evidence of a large, international network of HCV transmission in HIV-positive men who have sex with men.Crossref | GoogleScholarGoogle Scholar | 19422083PubMed |

[50]  Chaillon A, Sun X, Cachay ER, Looney D, Wyles D, Garfein RS, et al Primary incidence of hepatitis C virus infection among HIV-infected men who have sex with men in San Diego, 2000–2015. Open Forum Infect Dis 2019; 6 ofz160
Primary incidence of hepatitis C virus infection among HIV-infected men who have sex with men in San Diego, 2000–2015.Crossref | GoogleScholarGoogle Scholar | 31041355PubMed |

[51]  National Centre for Infectious Diseases (NCID). Recommendations for the use of antiretroviral therapy in adults living with HIV in Singapore. Singapore HIV Congress, 30 November 2019. Available at https://www.ncid.sg/About-NCID/OurDepartments/Documents/ART%20Recommendations.pdf [accessed 23 January 2020].

[52]  Panel on Opportunistic Infections in Adults and Adolescents with HIV. Guidelines for the prevention and treatment of opportunistic infections in adults and adolescents with HIV: recommendations from the Centers for Disease Control and Prevention, the National Institutes of Health, and the HIV Medicine Association of the Infectious Diseases Society of America. 2020. Available at https://clinicalinfo.hiv.gov/sites/default/files/guidelines/documents/Adult_OI.pdf [accessed 7 December 2020].

[53]  Workowski KA, Bolan GA, Centers for Disease Control and Prevention Sexually transmitted diseases treatment guidelines, 2015. MMWR Recomm Rep 2015; 64 1–137. [Erratum in MMWR Recomm Rep 2015; 64(33): 924]
| 26042815PubMed |

[54]  European AIDS Treatment Network (NEAT) Acute Hepatitis C Infection Consensus Panel Acute hepatitis C in HIV-infected individuals: recommendations from the European AIDS Treatment Network (NEAT) consensus conference. AIDS 2011; 25 399–409.
Acute hepatitis C in HIV-infected individuals: recommendations from the European AIDS Treatment Network (NEAT) consensus conference.Crossref | GoogleScholarGoogle Scholar | 21139491PubMed |

[55]  Sun HY, Chang SY, Yang ZY, Lu CL, Wu H, Yeh CC, et al Recent hepatitis C virus infections in HIV-infected patients in Taiwan: incidence and risk factors. J Clin Microbiol 2012; 50 781–7.
Recent hepatitis C virus infections in HIV-infected patients in Taiwan: incidence and risk factors.Crossref | GoogleScholarGoogle Scholar | 22189113PubMed |

[56]  Bottieau E, Apers L, Van Esbroeck M, Vandenbruaene M, Florence E. Hepatitis C virus infection in HIV-infected men who have sex with men: sustained rising incidence in Antwerp, Belgium, 2001–2009. Euro Surveill 2010; 15 19673
Hepatitis C virus infection in HIV-infected men who have sex with men: sustained rising incidence in Antwerp, Belgium, 2001–2009.Crossref | GoogleScholarGoogle Scholar | 20929655PubMed |

[57]  Reiberger T. Acute hepatitis C virus infection in HIV-infected men who have sex with men: should we change our screening practice? Clin Infect Dis 2014; 59 1694–5.
Acute hepatitis C virus infection in HIV-infected men who have sex with men: should we change our screening practice?Crossref | GoogleScholarGoogle Scholar | 25186589PubMed |

[58]  Martin TC, Martin NK, Hickman M, Vickerman P, Page EE, Everett R, et al Hepatitis C virus reinfection incidence and treatment outcome among HIV-positive MSM. AIDS 2013; 27 2551–7.
Hepatitis C virus reinfection incidence and treatment outcome among HIV-positive MSM.Crossref | GoogleScholarGoogle Scholar | 23736152PubMed |

[59]  Linas BP, Wong AY, Schackman BR, Kim AY, Freedberg KA. Cost-effective screening for acute hepatitis C virus infection in HIV-infected men who have sex with men. Clin Infect Dis 2012; 55 279–90.
Cost-effective screening for acute hepatitis C virus infection in HIV-infected men who have sex with men.Crossref | GoogleScholarGoogle Scholar | 22491339PubMed |

[60]  World Health Organization. Hepatitis C. 2019. Available at www.who.int/news-room/fact-sheets/detail/hepatitis-c [accessed 13 January 2020].

[61]  Thomson EC, 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.
Delayed anti-HCV antibody response in HIV-positive men acutely infected with HCV.Crossref | GoogleScholarGoogle Scholar | 19050390PubMed |

[62]  Strasak AM, Kim AY, Lauer GM, de Sousa PS, Ginuino CF, Fernandes CA, et al Antibody dynamics and spontaneous viral clearance in patients with acute hepatitis C infection in Rio de Janeiro, Brazil. BMC Infect Dis 2011; 11 15
Antibody dynamics and spontaneous viral clearance in patients with acute hepatitis C infection in Rio de Janeiro, Brazil.Crossref | GoogleScholarGoogle Scholar | 21226945PubMed |

[63]  Vanhommerig JW, Thomas XV, van der Meer JT, Geskus RB, Bruisten SM, 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 1678–85.
Hepatitis C virus (HCV) antibody dynamics following acute HCV infection and reinfection among HIV-infected men who have sex with men.Crossref | GoogleScholarGoogle Scholar | 25186590PubMed |