Questions about sexual transmission of the hepatitis C virus (HCV) have been controversial since day one. Despite earlier uncertainty, there is no longer any question that HIV-positive men are acquiring HCV through sex with other men (as are HIV-negative gay men, although much less frequently). How best to protect ourselves depends on which specific sexual activities are riskiest – an issue for which the evidence is suggestive but not yet conclusive.

In the great majority of cases, the hepatitis C virus is transmitted by direct blood-to-blood contact: through needlestick injuries, by sharing needles or other injecting drug equipment. It can also be passed from mother to child during childbirth. (Before screening of donated blood became routine in 1990, many people also became infected through blood transfusions and infected blood products.)

At first it was believed that only blood-to-blood contact could transmit HCV. Early research in heterosexual couples found that sexual transmission was very rare: many studies found no occurrences in the couples followed, even over periods of many years.¹

However, the reality has proven quite different in HIV-positive gay and bisexual men. Despite some initial scepticism, sexual transmission is now the well-established cause of outbreaks of acute HCV infection among gay and bisexual men in a growing list of countries.

The first reports came from the UK in 2002, when physicians at two of London's largest HIV clinics reported new hepatitis C infections among HIV-positive gay men who did not use needles or have any other known risk factors for HCV, apart from having unprotected sex. The number of known UK cases has continued to grow, and outbreaks have also been documented in the Netherlands², Switzerland³, France⁴, Germany, Australia⁵ and the US.⁶ (Hepatitis C also has an international passport: detailed genetic analyses have shown that it is being transmitted from country to country among HIV-positive men.⁷)

Overall rates of hepatitis C infection (by any means of transmission, sexual or otherwise) are on the rise among HIV-positive gay and bisexual men in London and Brighton. According to data from HIV and sexual health clinics in those two cities, a total of 389 HIV-positive gay or bisexual men were diagnosed with hepatitis C between 2002 and 2006 (352 in London and 37 in Brighton).⁸ Infection rates increased by 20% each year during that time, from 56 cases in 2002 to 91 in 2006 – a trend that appears to be continuing.⁹

Over the same time interval, only six cases of HCV were reported among HIV-negative men (or those who did not know their status). Outbreaks in every country, in fact, are almost exclusively confined to HIV-positive men. This finding is not yet fully understood, and we will return to it later on.

Fisting has often been identified as the single largest risk factor for sexual HCV transmission. One of the largest UK studies compared 60 recently HCV-infected, HIV-positive gay men to 130 HIV-positive ‘controls’ who did not have hepatitis C. Men in this study who were insertive in fisting (fisting ‘tops’) were about three times more likely to have contracted HCV, and receptive partners (fisting ‘bottoms’) four times more.¹⁰ In another study of over 300 men, fisting appeared riskier still, carrying a nine-times greater risk of HCV infection, though this figure was only based on eleven actual cases of recent HCV infection.¹¹

However, men who have never fisted or engaged in other ‘heavy’ anal play have also become infected. Also, at least one study of HIV-positive gay men in New York did not find fisting to be significantly riskier than unprotected intercourse alone (a difference that may reflect different patterns of infection and sexual behaviour in different locations).¹² Fisting may account for significant numbers of hepatitis C infections, but it is probably not the only way the virus can be spread sexually.

Studies have consistently found other behaviours that increase the risk of contracting HCV sexually, including the use of sex toys (dildos), group sex, having large numbers of sexual partners, using recreational drugs during sex, rimming and having sexually transmitted infections (STIs) such as syphilis and herpes.^{13, 14, 15} Yet the single most common factor reported by men who have become HCV-infected is unprotected anal sex.

Many experts now believe that increasing numbers of men are becoming infected through barebacking (unprotected anal sex) alone. "I think the primary route of HCV transmission has shifted," says Martin Fisher, consultant physician at Brighton & Sussex Hospitals NHS Trust. "With the first cases we saw, the majority of those people reported more than just unprotected anal intercourse. They tended to be people with multiple partners and fairly vigorous sexual activity such as fisting and toys, often taking recreational drugs as well. The majority of individuals I now see with acute, newly diagnosed HCV don't report those risk factors, except for unprotected sex."

In the US, where sexually transmitted HCV only surfaced among gay men more recently, barebacking appears to be a greater contributor than fisting. Daniel Fierer, Assistant Professor of Medicine at New York's Mount Sinai School of Medicine, was one of the investigators on the New York study mentioned above. Fierer and team "looked at a relatively small number of patients, but we did a very carefully matched statistical analysis. When we removed people with any history of injection drug use, we found that fisting and sex while high were not significant risks: it was largely receptive unprotected sex. Insertive partners were not the ones becoming infected."

Identifying risky activities is not the same as explaining just how HCV transmission occurs – a question that is not yet definitively answered. As Daniel Fierer puts it, "Men who are getting infected are engaging in a lot of activities. That tells us the milieu in which it's happening, but doesn't necessarily disentangle the causal factors."

The link between fisting and HCV transmission suggests that the virus is most easily transmitted through damaged rectal tissues – an explanation that seems plausible and perhaps intuitively ‘right’. Delicate, blood vessel-laden rectal tissues are easily damaged by fisting or other intense anal play (such as large dildos and sex toys), creating an open pathway for infection. Rectal tissue could conceivably be vulnerable to infection even if not ‘roughed up’ by heavy play.

With the first cases we saw, the majority of those people reported multiple partners and fairly vigorous sexual activity such as fisting and toys, often taking recreational drug as well.

The majority of those individuals I now see with acute, newly diagnosed HCV don't report those risk factors, except for unprotected sex.

Martin Fisher

Brighton and Sussex

Hospitals NHS Trust

But virus from the infected partner still has to find its way there – and how it does so is still being debated. Is it through blood, semen, or both? Whether HCV can be transmitted through semen is under debate. Studies have found the virus at detectable, but low, levels in the semen of 10 to 40% of HCV-infected men.¹⁶ Fisher and Fierer both point out that HCV has been found in semen at higher levels in HIV-positive than in HIV-negative individuals. Yet even in HIV-positive men, seminal HCV levels are usually so small that many experts doubt they could cause infection. A small, recent study detected HCV in the semen of only a minority of co-infected men in the UK, and levels in semen were at most a few hundredths of a percent of those usually found in the bloodstream. Seminal HCV levels in the study were 230 IUs (international units)/ml or less. An international unit can vary from 0.9 to 5.2 copies/ml, depending on the test used, so this translates into 200 to 1200 copies: but most detectable seminal viral loads in this study translated into below 150 copies/ml by any test. In contrast, typical bloodstream levels run into the millions of copies/ml.¹⁷

It could be argued that risky sex, whether barebacking or fisting, are contributing factors: i.e., the more risky activities you engage in, the more likely you are to contract HCV. One analysis of a group of men in the UK found just such a "cumulative" outcome when four separate factors were considered – unprotected anal sex, group sex, recreational drug use, and "mucosally traumatic" practices like fisting and sex toys. Two or more of these activities made for a nine times greater risk of infection, but engaging in three or all four increased the risk by more than 23-fold.¹⁸

Group sex sessions may provide even more opportunity for the virus to be spread. In a study from Germany, although unprotected anal sex was widespread among the men studied, only being fisted (receptive), rectal bleeding, and drug use during group sex were significant risks for sexual HCV transmission. The researchers went on to conjecture that in group sex situations, some people may serve as "carriers" who pass HCV between others.¹⁹ Specifically, fisting ’tops’ (insertive partners) with multiple bottom (receptive) fisting partners in the same session may carry HCV-infected blood from one to the other.

Not everyone buys into this hypothesis – Fierer finds it "a tortured explanation" – yet even without it, group sessions still bring together a wide range of risks. They often exclusively involve unprotected sex between HIV-positive men who have chosen to serosort (i.e., restrict unprotected sex to other HIV-positive partners) and often involve heavy sex play and recreational drugs. Together, these factors could conspire to produce a setting ripe for HCV transmission.

With new HCV infections amongst HIV-positive men vastly outnumbering those in HIV-negative men, HIV itself clearly plays a central role in HCV transmission. Precisely what that role is has yet to be determined. Behaviour, rather than biology, may be at least part of the explanation: "if you've recently acquired HIV then you're likely to be in a high-risk period of your life, which could put you at risk of HCV as well," says Fisher. 

In fact, many HIV-positive gay men who contract hepatitis C sexually seem to do so shortly after their HIV infection. A study conducted at St Mary’s Hospital in London found that 7% of gay men diagnosed with HIV at the hospital between 1999 and 2006 went on to become infected with HCV through sex. On average, the time between HIV infection and diagnosis of hepatitis C was just under two years.²⁰

Still, any difference in sexual behaviour between HIV-positive and HIV-negative men does not seem sufficient to explain the enormous difference in rates of HCV. Martin Fisher suggests that, "We'd see more crossover from HIV-positive to HIV-negative men if that were the only factor. So I think there is something immunological going on as well, that we haven't yet characterised, that puts you at greater risk of acquiring HCV if you are HIV-positive."

Using recreational drugs as a sex stimulant (‘sex while high’) is also repeatedly identified in studies as another risk factor for hepatitis C transmission. This may be due to the way drug use influences sex (men who get fisted may be more likely to use drugs), and/or by the way the drugs themselves are taken – and gay men who use drugs may not be aware of all the risks.

For instance, HCV is known to be easily spread through shared straws or other equipment for snorting drugs: as a straw or ‘bullet’ gets passed around, miniscule amounts of blood can pass from one person's nasal membranes to the next. Needle use, with all its potential risks for HCV transmission, is also not unknown among gay men. HCV can easily be spread through shared equipment other than needles themselves. Spoons or other equipment used to dissolve drugs for injection, and filters used to filter substances, can easily transfer HCV from a used needle to a new one.

Of course, many HIV-positive gay men use condoms as a matter of course and do not fist or go to sex parties: they are likely to be as safe from contracting HCV as it is possible for a sexually active gay man to be. At the other end of the spectrum, fisting, group sex and drug use appear to present the greatest risks. But what about those HIV-positive gay men who choose to serosort but do not engage in more hardcore activities like fisting and group sex? These men may face the biggest uncertainties about HCV risk – in the face of which, the most frequent advice is caution.

As Martin Fisher puts it, "We would like to be able to say, 'HCV is transmitted like this, and therefore here is what you need to do to avoid getting it.' Unfortunately I think we're at too early a stage to be able to give such definitive guidance, and I think we have to be honest about that. We simply have to tell people what we know: that there probably is an increased risk with any sexual activity with exposure to semen, and almost certainly more so with blood."

According to Daniel Fierer, the bottom line is "awareness in the gay community that you can get HCV sexually. This is a new and unfortunate risk in serosorting. Let's assume the risk is significant, and take precautions. That may not be popular, but it is simple."

One challenge is that men who have chosen to serosort may already have disengaged from standard safer-sex messaging. (Dire, but overblown, warnings of reinfection with HIV ‘superbugs’ may well have bolstered scepticism toward "condoms for all, all the time" messages.)

That, says Marc Thompson of the Terrence Higgins Trust (THT), was a significant challenge for his organisation in providing information to positive men who bareback. "We knew we were dealing with men who were already quite well-informed about safer sex issues, who didn't engage with typical safer-sex messaging, and who had made decisions around their own sexual health already."

Their first step, then, was not to talk but to listen. In a series of focus groups, and others at THT met with the men likely most at risk for HCV, those who frequently fist, have rough sex, and use drugs. Those who had already been co-infected with HIV and HCV had a clear message for their peers: hepatitis C is not just another STI. "Gay men may think of sexually transmitted infections (STIs) as things that can often be treated fairly easily: a trip to the clinic, a couple of pills. The men in our groups wanted us to stress how debilitating hepatitis C is, and how completely different HCV treatment is from the treatments for other STIs." That message – that HCV treatment is lengthy and hard to tolerate – was "loud and clear," says Thompson.

Which brings us back to the question: in the absence of certainty about what's risky, what is the best prevention advice? "We're just trying to present all the info as it stands," says Thompson. "We're not the condom police, but we have not ruled out unprotected anal intercourse as a means of HCV transmission, so that has to be put out there, along with all the other information we have to date."

Finally, one more factor is probably contributing to hepatitis C transmission as well as worsening life for those infected: the fear, shame and stigma of the disease. Gay men with hepatitis C have said they feel “grubby, skanky, isolated and ashamed." They have called HCV "the big new white elephant in the room”, something gay men are "scared of, but that nobody is talking about." Men with HCV have described an "us and them situation" in which their dual diagnosis excludes them from the “camaraderie of just being HIV-positive.”²¹

Clearly, as a community we have a mandate to help HIV-positive men avoid co-infection. Yet, as we continue to battle stigma against people with HIV, it would be a sad irony if our own community opened its arms to people with one virus but turned its back on those with another.