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Hepatitis C is not commonly considered a sexually transmitted infection – it is usually passed through blood-to-blood contact. However, the sexual transmission of hepatitis C is an increasing concern among some gay and bisexual men and other men who have sex with men (gbMSM). Over the past two decades, sexual transmission of hepatitis C has predominantly occurred among gbMSM living with HIV. Recently a small but increasing number of HIV-negative gbMSM have been getting hepatitis C. This article reviews how hepatitis C is passed sexually, the types of sex where it can be passed and the rates of hepatitis C sexual transmission among gbMSM. It also includes strategies to reduce the likelihood of sexual transmission and recommendations for service providers working with gbMSM.

Why are we talking about sexual transmission of hepatitis C among gbMSM?

Drug use, and injection drug use in particular, is a well-understood pathway for hepatitis C transmission. Sexual transmission of hepatitis C isn’t as clear. The evidence suggests that sexual transmission of hepatitis C among heterosexual couples is rare.1 However, as we will discuss below, sexual transmission of hepatitis C can occur among gbMSM. Further, changing sexual practices among gbMSM2 using new HIV prevention approaches (such as PrEP) may be having an impact on the rates of sexual transmission of hepatitis C.

The Blueprint to inform hepatitis C elimination efforts in Canada indicates that gbMSM are an emerging priority population for efforts to eliminate hepatitis C infection. The Blueprint states that sexual transmission and/or transmission through drug use are the main risk factors for hepatitis C among gbMSM.3 However, hepatitis C infection may not be widely considered a priority for sexual health services and education for gbMSM.

It is challenging to understand the risk of sexual transmission among gbMSM, including separating the risks of transmitting hepatitis C through sex and through drug use. In the studies discussed in this article, where information on drug use is included in the research it is often based on self-reported data, which may be an underestimate because of the stigma that can be associated with drug use.

How is hepatitis C passed?

Hepatitis C is generally passed by direct blood-to-blood contact. This occurs when a person’s blood is exposed to the blood of someone with hepatitis C infection through a break or tear in the skin or mucous membranes. In Canada, the most common way a person gets hepatitis C is through sharing injection drug use equipment.7 Hepatitis C can also be passed through sharing equipment for smoking drugs, such as pipes and mouthpieces,8 and it can potentially be passed through sharing straws for snorting drugs.9

Although hepatitis C is not as easily transmitted through sex as HIV and hepatitis B,10 hepatitis C can enter the body through the rectal mucous membranes during sex. The hepatitis C virus is thought to enter the body through a tear in the mucous membrane of the rectum or by a sore caused by an ulcerative STI, such as syphilis. The virus can be passed into the rectum via a penis, hand (during fisting) or sex toy that has blood with hepatitis C on it.6 There is also evidence of high enough volumes of hepatitis C virus in the semen11 and rectal fluid12 of some gbMSM living with HIV to pass hepatitis C. (Note that hepatitis C has been detected in the semen11 and rectal fluid12 of gbMSM with and without detectable HIV viral loads).

What factors are linked to the sexual transmission of hepatitis C among gbMSM?

A cluster of factors have been associated with the sexual transmission of hepatitis C.5,6 For sexual transmission of hepatitis C to occur, there must be exposure to the hepatitis C virus in one or more of these situations:

  • condomless anal sex
  • fisting without a glove
  • sharing sex toys
  • multiple sex partners
  • group sex
  • anal douching
  • rectal bleeding
  • using recreational drugs before or during sex
  • having HIV
  • having an ulcerative STI (such as syphilis and lymphogranuloma venereum [LGV])

Drug use and sex

Where drug use is present, it is difficult to tease apart the extent to which drug use versus sex contributes to the transmission of hepatitis C. For example, party and play or chemsex is when certain drugs are used by gbMSM before or during sex to facilitate, sustain or enhance sexual encounters. The risk of hepatitis C transmission through party and play is twofold, through drug use and through sex. Hepatitis C can be acquired through shared drug use equipment. There is also concern that booty bumping or boofing (inserting drugs into the rectum) can damage and/or irritate the tissue of the rectum, which could increase the risk of sexual transmission of hepatitis C.13 Party and play is also associated with types of sex that overlap with sexual risk factors for hepatitis C. For example, gbMSM who party and play are more likely to participate in condomless anal sex with one or more partners and participate in group sex compared with gbMSM who do not party and play.14 Thus, deciphering whether new hepatitis C infections among gbMSM who party and play were acquired through drug use or sex is challenging.

What are the rates of sexually acquired hepatitis C infection among gbMSM?

gbMSM living with HIV

In the early 2000s, reports began to appear of hepatitis C outbreaks among populations of gbMSM living with HIV where the vast majority of the men did not report typical blood-related risks for transmission, such as injection drug use or medical/dental care in countries where universal precautions to prevent hepatitis C infection have not been consistently implemented.6,15 These were the first reports to suggest that hepatitis C could be passed through sex. Over time, as more research was published globally on rates of hepatitis C infection among gbMSM living with HIV, it became accepted that sex was a pathway for transmission of hepatitis C among gbMSM living with HIV.6,10,16

Two international systematic reviews reported that the hepatitis C prevalence rate among HIV-positive gbMSM with no history of injection drug use is about seven in 100.17,18 This is higher than the estimated prevalence rate of five in 100 among gbMSM with/without HIV in a survey across five cities in Canada.19

An international systematic review reported about 6.4 new hepatitis C infections per 1000 person-years among gbMSM living with HIV.17 Another systematic review found a slightly higher rate of 7.8 new hepatitis C infections per 1000 person-years among gbMSM living with HIV, although injection drug use was not excluded from this analysis.20 There was a trend toward an increasing number of new hepatitis C infections in HIV-positive gbMSM over time.20 A Canadian study of data from Ontario (data from 2000 to 2010) reported 5.1 new hepatitis C infections per 1000 person-years among HIV-positive gbMSM without a self-reported history of injection drug use.21

Re-infection with hepatitis C is also a concern because a person who has been cured of hepatitis C or who has spontaneously cleared the virus can get hepatitis C again if they are re-exposed to the hepatitis C virus. High re-infection rates have been reported among gbMSM living with HIV. A review of research from North America and Europe reported 100 to 150 hepatitis C re-infections per 1000 person-years among gbMSM living with HIV.22 This demonstrates that there is an ongoing high risk of hepatitis C re-infection among some gbMSM living with HIV.

HIV-negative gbMSM

HIV-negative gbMSM have much lower rates of new hepatitis C infections than HIV-positive gbMSM. Rates ranged from 0.4 to 1.5 new hepatitis C infections per 1000 person-years among HIV-negative gbMSM.16

Recently, there have been reports of sexually acquired hepatitis C infection among HIV-negative gbMSM who are taking PrEP to prevent HIV.5,15,16 A meta-analysis of PrEP trials reported 13 new hepatitis C infections per 1000 person-years.23 A report from France found a marked increase in hepatitis C incidence among gbMSM using PrEP from three new infections per 1000 person-years in 2016 to 34 new infections per 1000 person-years in 2017.24 Although still high, the rate of new hepatitis C infections among PrEP users was lower in a recent study in Toronto, at seven new infections per 1000 person-years.25

It is important to note that unlike research on hepatitis C infections among gbMSM living with HIV, recent studies of hepatitis C infections among gbMSM using PrEP have included gbMSM who report drug use. Drug use is often identified as a contributing factor to hepatitis C infections among gbMSM using PrEP, including through party and play.16

Another contributing factor is that gbMSM on PrEP are more likely to be tested for hepatitis C because routine screening for STIs and hepatitis C is standard practice, and so they are more likely to be diagnosed with a hepatitis C infection than gbMSM who are not on PrEP. This also means that gbMSM taking PrEP are more likely to get linked to care and cured of hepatitis C infection in a timely way.

Research on re-infection with hepatitis C among gbMSM taking PrEP indicates that they have a high risk of re-infection. PrEP studies in France and the Netherlands have reported 10 new hepatitis C infections per 1000 person-years for the first hepatitis C infection, but 250 new hepatitis C infections per 1000 person-years among those who have already had hepatitis C.16

Together, these studies indicate that sexual transmission of hepatitis C is mainly occurring among gbMSM living with HIV, with a recent increase in the number of hepatitis C infections among HIV-negative gbMSM taking PrEP.5 These studies also demonstrate an ongoing high risk of hepatitis C re-infection among some gbMSM.

What can explain the rates of sexually acquired hepatitis C infection?

There are several theories as to why gbMSM living with HIV are disproportionally affected by the sexual transmission of hepatitis C, in comparison with gbMSM without HIV. Some of the reasons may be related to having HIV. For example, HIV may contribute to a deterioration of the rectal mucous membrane of a person living with HIV, which may make it easier for the hepatitis C virus to pass through during receptive anal sex.6,10 There is also conflicting evidence about whether a low CD4 count may contribute to susceptibility to hepatitis C infection because of a suppressed immune system.6,16

Another theory on why higher rates of hepatitis C may be seen in HIV-positive men is that HIV is more sexually infectious than hepatitis C, so gbMSM having types of sex that pass both infections are more likely to get HIV before hepatitis C.6,15 An additional theory is that the higher rates of hepatitis C infection among HIV-positive gbMSM may be random.6,15 Once hepatitis C entered the population of gbMSM living with HIV, hepatitis C may have been “ring-fenced” around gbMSM living with HIV through practices such as serosorting (people living with HIV choosing to only have sex with people who also have HIV).6,10,15 Research analyzing strains of hepatitis C virus to trace patterns of infection supports this theory. The studies suggest there was a rapid expansion of gbMSM-specific hepatitis C virus strains in Europe after 1996, which followed the introduction of highly effective antiretroviral therapy for HIV.6,26 The studies also suggest that hepatitis C was being passed among gbMSM living with HIV and that there was minimal overlap with strains of hepatitis C virus among injection drug use networks.26

With new, highly effective strategies to prevent HIV, such as PrEP and an undetectable HIV viral load, sexual networks of gbMSM with and without HIV may be overlapping more. Research analyzing strains of hepatitis C virus found that HIV-negative gbMSM taking (or eligible for) PrEP have hepatitis C infections with virus strains that circulate in networks of HIV-positive gbMSM.5,16 PrEP is recommended for gbMSM who are considered at risk for HIV, including those who have condomless sex and/or have had an STI.4 These factors may also increase risk for sexual transmission of hepatitis C, which probably helps to explain the higher rates of new hepatitis C infections among gbMSM taking PrEP than among HIV-negative gbMSM who are not taking PrEP.

Recommendations for service providers

Integrate hepatitis C education into existing sexual health and HIV services for gbMSM:

  • Know hepatitis C risk factors. Educate gbMSM about the sexual transmission of hepatitis C. Encourage gbMSM having sex that could lead to hepatitis C to:
    • use a new condom for each partner, including on sex toys
    • use a new glove for each partner when fisting
    • use individual lube containers and regularly apply lube
  • For gbMSM who party and play, know where to refer them to harm reduction services such as needle and syringe programs if they are using drugs.
    • Encourage gbMSM who party and play to use new injection drug use equipment every time and to use their own drug use equipment for smoking and snorting drugs.
  • Educate about re-infection. For gbMSM who have had hepatitis C and may be exposed to the hepatitis C virus again, let them know they can be re-infected. Share prevention information, strategies and resources. Encourage routine hepatitis C RNA screening for re-infection every 6–12 months.
  • Know where to refer gbMSM to get tested for hepatitis C. Encourage gbMSM who may be exposed to hepatitis C to get tested regularly for hepatitis C as a part of routine STI screening. Let them know there is highly effective treatment to cure hepatitis C.

Integrate hepatitis C testing services into existing sexual health and HIV services:

  • routine screening for hepatitis C with other STIs for gbMSM who might be exposed to hepatitis C through sex, including gbMSM taking PrEP and/or who party and play
  • routine RNA screening for hepatitis C re-infection for gbMSM who have been treated or cleared hepatitis C and who might be exposed to hepatitis C through sex

Integrate sexual health and harm reduction services and programs to support gbMSM:

  • Some gbMSM may not feel comfortable within traditional harm reduction settings. Broadening programs for gbMSM so that hepatitis C is integrated into sexual health and harm reduction services, for example around party and play, could help to bridge some of these service gaps.

 

References

  1. Dodge JL, Terrault NA. Sexual transmission of hepatitis C: a rare event among heterosexual couples. Journal of Coagulation Disorders. 2014:4(1):38-9.
  2. Brogan N, et al. Canadian results from the European Men-who-have-sex-with-men Internet survey (EMIS-2017). Can Commun Dis Rep 2019;45(11):271-82. Available from: https://www.canada.ca/en/public-health/services/reports-publications/canada-communicable-disease-report-ccdr/monthly-issue/2019-45/issue-11-november-7-2019/article-1-canadian-men-who-have-sex-with-men-survey-results.html
  3. Canadian Network on Hepatitis C Blueprint Writing Committee and Working Groups. Blueprint to Inform Hepatitis C Elimination Efforts in Canada. Montreal, QC: Canadian Network on Hepatitis C; 2019. Available from: https://www.canhepc.ca/en/blueprint/publication
  4. Tan DHS, Hull MW, Yoong D, et al. Canadian guideline on HIV pre-exposure prophylaxis and non-occupational postexposure prophylaxis. CMAJ. 2017;189(47):E1448-E1458. Available from: http://www.cmaj.ca/content/189/47/E1448
  5. Lockhart, et al. Sexually transmitted hepatitis C infection: the evolving epidemic in HIV-positive and HIV-negative MSM. Current Opinion in Infectious Diseases. 2019;32:31-7.
  6. van de Larr TJW and Richel O. Emerging viral STIs among HIV-positive men who have sex with men: the era of hepatitis C virus and human papillomavirus. Sexually Transmitted Infections. 2017;93:368-76.
  7. Trubnikov M, Yan P, Archibald C. Estimated prevalence of hepatitis C virus infection in Canada, 2011. Canada Communicable Disease Report. 2014 Dec 18; 40-19. Available from: http://www.phac-aspc.gc.ca/publicat/ccdr-rmtc/14vol40/dr-rm40-19/surveillance-b-eng.php
  8. Strike C, Hopkins S, Watson TM, et al. Best Practice Recommendations for Canadian Harm Reduction Programs that Provide Service to People Who Use Drugs and are at Risk for HIV, HCV, and Other Harms: Part 1. Toronto, ON: Working Group on Best Practice for Harm Reduction Programs in Canada; 2013.
  9. Aaron S, McMahon JM, Milano D, et al. Intranasal transmission of hepatitis C virus: virological and clinical evidence. Clinical Infectious Diseases. 2008;47(7):931-4.
  10. Page EE, Nelson M. Hepatitis C and sex. Clinical Medicine (London, England). 2016;16(2):189-92.
  11. Turner SS, Gianella S, Yip MJ, et al. Shedding of hepatitis C virus in semen of human immunodeficiency virus-infected men. Open Forum Infectious Diseases. 2016;3(2):ofw057.
  12. Foster AL, Gaisa MM, Hijdra RM, et al. Shedding of hepatitis C virus into the rectum of HIV-infected men who have sex with men. Clinical Infectious Diseases. 2017;64(3):284-8.
  13. Rivers Allen J, Bridge, W. Strange routes of administration for substances of abuse. American Journal of Psychiatry Residents’ Journal. 2017;1:7-11.
  14. Sewell J, Miltz A, Lampe FC, et al. Poly drug use, chemsex drug use, and associations with sexual risk behaviour in HIV-negative men who have sex with men attending sexual health clinics. International Journal of Drug Policy. 2017;43:33-43.
  15. Price JC, McKinney JE, Crouch PC, et al. Sexually acquired hepatitis C infection in HIV-uninfected men who have sex with men using preexposure prophylaxis against HIV. Journal of Infectious Diseases. 2019;219:1373-6.
  16. Nijmeijer BM, Koopsen J, Schinkel J, et al. Sexually transmitted hepatitis C virus infections: current trends, and recent advances in understanding the spread in men who have sex with men. Journal of the International AIDS Society. 2019;22(Suppl 6):e25348.
  17. Jin F, Matthews GV, Grulich AE. Sexual transmission of hepatitis C virus among gay and bisexual men: a systematic review. Sexual Health. 2017;14:28-41.
  18. Jordan AE, Perlman DC, Neurer J, et al. Prevalence of hepatitis C virus infection among HIV+ men who have sex with men: a systematic review and meta-analysis. International Journal of STD & AIDS. 2017;28(2):145-59.
  19. Public Health Agency of Canada. M-Track: Enhanced Surveillance of HIV, Sexually Transmitted and Blood-Borne Infections, and Associated Risk Behaviours among Men Who Have Sex with Men in Canada. Phase 1 report. Ottawa, ON: Centre for Communicable Diseases and Infection Control, Infectious Disease and Prevention and Control Branch, Public Health Agency of Canada [Online]; 2011]. Available from: http://librarypdf.catie.ca/PDF/ATI-20000s/26403.pdf
  20. Ghisla V, Scherrer AU, Nicca D, et al. Incidence of hepatitis C in HIV positive and negative men who have sex with men 2000-2016: a systematic review and meta-analysis. Infection. 2017;45:309-21.
  21. Burchell AN, Gardner SL, Mazzulli T, 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. Canadian Journal of Infectious Diseases & Medical Microbiology. 2015;26(1):17-22.
  22. Midgard H, Weir A, Palmateer N, et al. HCV epidemiology in high-risk groups and the risk of reinfection. Journal of Hepatology. 2016;65:S33-S45.
  23. Werner RN, Gaskins M, Nast A, et al. Incidence of sexually transmitted infections in men who have sex with men and who are at substantial risk of HIV infection – a meta-analysis of data from trials and observational studies of HIV pre-exposure prophylaxis. PLoS ONE. 2018;13(12):e0208107.
  24. Ramière C, Charre C, Miailhes P, et al. Patterns of HCV transmission in HIV-infected and HIV-negative men having sex with men. Clinical Infectious Diseases. 2019;69(12):2127-35.
  25. Tabatabavakili S, Cerocchi O, Hansen BE, et al. 2019. Incidence of hepatitis C virus infection among users of HIV PrEP in a large academic centre in Toronto, Canada In: Abstracts of the AASLD Liver Meeting, Boston, Massachusetts, November 8–12, 2019. Abstract 0281. Available from: https://plan.core-apps.com/tristar_aasld19/abstract/0b8716de6c519b8c26b6b46a115481e3
  26. Chan DP, Sun HY, Wong HT, et al. Sexually acquired hepatitis C infection: a review. International Journal of Infectious Diseases. 2016;49:47-58.

 

About the author(s)

Rivka Kushner is CATIE’s knowledge specialist in Hepatitis C. She has a Master’s of Public Health in Health Promotion from the University of Toronto. Before joining CATIE, Rivka worked on provincial and national research and knowledge exchange projects in workplace health and environmental sustainability.