Hepatitis C virus (HCV) infection has been estimated to affect 170 million individuals worldwide, of whom 4 to 5 million are coinfected with HIV.1 There are currently 55,000 to 78,000 people with HCV infection in Switzerland, and anti-HCV prevalence in the general Swiss population is estimated to be between 0.7% and 1.0%.2 Transmission of HCV occurs via percutaneous exposure to blood through, for example, transfusion of contaminated blood products and injecting drug use (IDU).3
Since 2000, incident HCV infection in the developed world has risen sharply among HIV-positive men who have sex with men (MSM).1,4–7 Large population studies point to the mechanism of transmission being permucosal, rather than percutaneous, through exposure to blood8 and possibly semen,9 in other words, via sexual transmission.10 Hepatitis C virus infection in HIV-positive MSM is associated with having more than 1 sexual partner,11,12 engaging in high-risk sexual behavior, including unprotected anal intercourse (UAI) and group sex,8,12 with ulcerative sexually transmitted infection (STI), notably syphilis,11,13 and with traumatic sexual practices (TSPs).8 Nonsexual transmission through recreational drug use may also play a role, either directly through shared paraphernalia12,14 or indirectly through behavioral disinhibition.8,14
In Switzerland, figures from the Swiss HIV Cohort Study demonstrate an 18-fold increase in incident HCV in the HIV-positive MSM population between 1998 and 2011,7 with infection risk being associated with UAI.7,15 It has recently been reported that the sexual spread of HCV observed in the Swiss HIV Cohort Study is focused on MSM in whom the HIV genetic bottleneck at transmission was wide, implying high-risk sexual behavior and mucosal barrier impairment.16
Hepatitis C virus prevalence and incidence among HIV-negative MSM is much lower than that in HIV-positive MSM6,17,18 but has reported to be higher than that of the general (non-MSM) population.17 When observed, HIV infection in HIV-negative MSM has been associated with ulcerative STI, TSP, and UAI with HCV-positive partners.18
The 2015 sexually transmitted diseases treatment guidelines of the Centers for Disease Control and Prevention propose annual HCV testing for HIV-positive MSM, with more frequent testing in individuals at high risk, and for individuals whose sexual partners are HCV positive.19 The European AIDS Clinical Society currently recommends regular HCV screening in HIV-positive but not in HIV-negative MSM.20 In their recommendations for testing for STI in MSM, the British Association for Sexual Health and HIV does not propose HCV screening in HIV-negative MSM unless individuals report a high-risk profile.21 With these HCV testing recommendations, it is possible that HIV-negative MSM, even those who present for STI screening, are unaware of HCV.
We examined HCV awareness (risk factors, disease course, and treatment) among MSM attending screening clinics and meeting places in southwest Switzerland against behavioral risk factors reported. As a secondary objective, we examined HCV seroprevalence in this group.
This study was approved by the Ethics Committee of the Canton of Vaud, Switzerland.
Study Design and Participant Inclusion
The study took place between 1st June 2011 and 31st August 2012 as part of a regional prevention and screening program. Men who have sex with men were recruited in the Swiss Lemanic region of southwest Switzerland (Cantons of Geneva and Vaud) from 2 broad settings: (1) Checkpoint Geneva, a community health center for MSM focusing on prevention of HIV and other STI and providing screening and counseling and (2) meeting places where prevention activities were organized, both indoor (saunas, sex clubs) and outdoor (Pride event and cruising areas).
Individuals were invited by trained field workers to participate in a questionnaire-based survey (see later). Individuals could participate only once and known positive HCV status was the only exclusion criterion. The percentage of participating individuals out of those approached was calculated, but nonparticipating individuals were not assessed. At the end of the questionnaire, participants were offered rapid testing for HCV.
Questionnaires were completed anonymously under field worker supervision. Participant age, nationality, canton of residence, and sexual preference (response options: “homosexual” or “bisexual”) were recorded. The first section of the questionnaire was adapted from a questionnaire validated elsewhere22 and covered HIV status (response options: “positive,” “negative,” “unknown,” and “rather not say”), date of last HIV test, and history of STI screening and treatment in the preceding 12 months. The second section covered HCV risk factors: (1) recreational drug taking, either currently, within the preceding 12 months or previously, and whether or not by intravenous injection; (2) history of UAI (response options: “yes” or “no”) and type of partner: stable, casual, and/or anonymous (response options: “yes,” “no,” and “sometimes”); (3) number of sexual partners in the preceding 12 months and the number of partners with whom UAI practiced; (4) history of UAI with a partner of different or unknown HIV status; and (5) history of TSPs (response options: “active” or “passive” in each case), type of partner with whom these practices were performed (response options: “stable,” “casual,” and/or “anonymous,” and “never,” “often,” and “always”), and venue (response options: “home,” “sex club,” “meeting places”; “private sex parties”; and “never,” “often,” and “always”).
The final section concerned HCV awareness. Participants were asked if they were aware of HCV (response options: “yes” or “no”). Those responding, yes were then asked further questions to assess the details of awareness. They were asked if a person infected with HCV is always symptomatic, if they had an acquaintance or a sexual partner who has HCV, if HCV can be transmitted via blood or anal sex, if HCV is cured without treatment, if a treatment of HCV exists, if HCV has serious complications, and if they had ever been screened for HCV (response options: “yes,” “no,” and “don't know”).
Upon questionnaire completion, participants received an information sheet about HCV and were then invited to be tested for HCV on site using an oral test, OraQuick HCV Rapid Antibody Test (OraSure Technologies Inc, Bethlehem, PA), with high sensitivity and specificity compared with standard screening using blood assays.23,24 Tests were performed by trained personnel, and results were provided within 30 minutes. In the event of a positive result, referral was made to the local infectious diseases clinic for confirmation and counseling. Hepatitis C virus antibody tests were provided at a preferential price by MSD (Lucerne, Switzerland), which had no impact on study design.
Data are presented as mean (SD), median (interquartile range), or percentages. Continuous data were analysed using Student t test; categorical data were examined using the χ2 or Fisher exact test. Analyses were conducted using Microsoft Excel 2008 (Microsoft Corporation, Redmond, WA).
Characteristics of Study Participants
Of 918 MSM approached, 654 (71%) agreed to participate and were of HCV negative or unknown status. The percentage of participation varied with venue, with most participants (536/654; 82%) enrolled via Checkpoint Geneva (Table 1). Mean (SD) age was 35 years (8.9 years; range, 16–80 years); 512 (78%) of 654 were homosexual and 486 (74%) of 654 were Swiss or from neighboring countries (Table 2).
HIV and STI History
Twenty-one participants (of 654; 3.2%) disclosed positive HIV status (Table 2). Of 633 participants with nonpositive HIV status, 414 (65%) had been tested in the preceding 12 months and 67 (11%) had never been tested. Regarding STI history, 337 (52%) of 654 participants had undergone STI screening and 72 (11%) of 654 had been diagnosed as having an STI in the preceding 12 months; 13 participants (of 654; 2%) had been diagnosed as having syphilis.
HCV Risk Factors
Recreational drug use was reported by 219 (33%) of 654 participants, with 203 (31%) of 654 reporting drug use currently or within the preceding 12 months. Four individuals (0.6%) had a history of IDU, either active (3 individuals) or within the preceding 12 months (1 individual).
Of all participants, 357 (of 654; 55%) reported UAI, 168 (47%) of 357 had casual partners, and 93 (26%) of 357 had anonymous partners. The median number of all sexual partners in the preceding 12 months was 5 (range, 0–400), whereas the median number of partners with whom UAI was practiced was 1 (range, 0–50). Regardless of whether UAI was practiced regularly, 321 (49%) of 654 reported UAI with a partner of different or unknown HIV status during the preceding 12 months. Participants of HIV positive or unknown HIV status were more likely to report such nonserosorting compared with participants of negative or undisclosed status (68% vs. 43%, P < 0.0001); of the 21 known HIV-positive participants, 16 (76%) had practiced UAI with a partner of different or unknown HIV status in the preceding year. Participants not serosorting underwent STI screening less frequently (0.7 times in preceding 12 months compared with 0.9 times, P = 0.02), but there was no difference in the number of STI diagnoses during this period (0.13 vs. 0.1, P = 0.16).
Regarding TSP, 103 (16%) of 654 reported receptive TSP, of whom 51 (of 103; 50%) and 33 (of 103; 32%) reported these with casual or anonymous partners, respectively. Most (88/103; 85%) reported engaging in these activities at home.
Of 654 participants, 302 (46%) were aware of HCV (Tables 1 and 3); awareness was higher among Checkpoint than meeting area clients (49% vs. 33%, P = 0.04). Of 302 participants aware of HCV, 23% knew someone HCV infected and 5.3% reporting having a current or previous HCV-positive sexual partner. Regarding transmission risk, most (>80% of participants aware of HCV; 38% of all participants) knew that HCV could be transmitted via blood or anal sex. Fewer than half (47%) knew if a treatment exists. Finally, 153 participants (of 302; 51%) reported previous screening for HCV; 10% were unsure.
Hepatitis C virus awareness was not associated with HIV status (P > 0.9), STI history (P > 0.9), UAI in the preceding 12 months (P > 0.9), or being Swiss (P > 0.9); none of these variables were associated with individual questions on HCV awareness.
A single HCV-positive individual (of 654; 0.2%) was identified on rapid testing with OraQuick HCV Rapid Antibody Test and was confirmed as positive on serological testing. He was a 28-year-old HIV-negative Swiss citizen, whose single risk factor was UAI with 2 stable partners during the preceding 12 months. He had no history of recent STI, TSP, or current or previous drug use.
In this group of predominantly HIV-negative, European MSM, we observed that almost half were aware of HCV and that knowledge was high concerning HCV transmission risks (>80%) and consequences of infection (>90%). Regarding high-risk behavior, UAI during the preceding 12 months, including with partners of different or unknown HIV status, was reported by half the participants and 1 in 10 participants had never been tested for HIV. Hepatitis C virus seroprevalence in this study population was low (0.2%).
Aside from reports of UAI, with or without HIV serosorting, our study population was strikingly low risk for HCV: 3% disclosed positive HIV status, 2% had been treated for syphilis, median sexual partner numbers were low, 16% engaged in TSP, and 0.6% reported IDU. It is possible that recruiting most participants from screening clinics led to selection bias and an artificially low-risk profile. This might explain why only a single participant was newly diagnosed as having HCV. If selection bias did play a role, it is possible that our observed HCV seroprevalence, and indeed HCV awareness, did not reflect the situation among the MSM we were unable to survey.
Some data exist from other countries on HCV awareness among MSM. Hepatitis C virus awareness among HIV-positive and HIV-negative MSM in the Amsterdam Cohort Studies was higher than in our population at 80% and 70%, respectively, with 92% of participants being aware of HCV transmission through “unsafe sex.”25 In the United States, among 58 HIV-positive MSM with HCV risk factors, 54% rated their HCV risk as not high.26 In Australia, among a small sample of HIV-positive MSM newly coinfected with HCV, two-thirds demonstrated limited knowledge of HCV risk.27 To our knowledge, ours is the first study to examine HCV awareness among predominantly HIV-negative MSM in Switzerland.
Schmidt et al.22 recently reported a study performed among 840 MSM in Zurich, north Switzerland, in which individuals were screened for HCV when they presented to a Checkpoint center to test for HIV and STI. Hepatitis C virus seroprevalence in this group was 0.83%, and sexual HCV transmission was not increased among HIV-negative MSM. Hepatitis C virus infection was significantly associated with HIV-positive status, non-Swiss origin, and non–injection drug use.22 The Zurich population had a similar proportion of HIV-positive participants (2.3%) to ours, but IDU was more common and participants were not excluded if they were known to be HCV positive.
Our study has limitations. Selection bias, as described earlier, may have overestimated HCV awareness. HIV prevalence may be inaccurate because the figure was based on participant disclosure; to maximize MSM participation, the survey was kept brief and including HIV testing would have required additional consent and time. It is possible that HIV prevalence was underreported, although the figure of 3.2% is higher than that of the general population (0.4%28). Another important limitation relates to the questions on drug taking in the questionnaire. Our study took place shortly before the publication of emerging trends in the UK in recreational drug use among MSM. The use of crystal methamphetamine, mephedrone, and γ-butyrolactone has increased in certain MSM communities, and intravenous injection of the former 2, known as slamming, has also increased in the context of sexual activity.14,29 In 2012, 80% of users of crystal methamphetamine and mephedrone attending a London clinic were injecting these drugs.29 Sex occurring between men under the influence of these drugs, so-called chemsex, can lead to UAI with high numbers of sexual partners.14 A report commissioned by 3 London boroughs entitled “The Chemsex Study” describes increasing use of these new drugs, and of slamming and chemsex, in clubs, cruising areas, saunas, and at public and private sex parties. These venues had minimal representation in our study, and these drugs were not mentioned in the questionnaire. The question on drug taking “by intravenous injection” in our questionnaire may have been taken to imply injection of drugs such as heroin and with this a profile that would not fit with MSM who inject crystal methamphetamine or mephedrone recreationally and who include high-income professionals.29 It is possible, were we to repeat this study and to ask specifically about these drugs, slamming or chemsex, that a different pattern of IDU would emerge in the Swiss Lemanic region (K.D. and M.C., unpublished observations).
Although drug use and injecting has been observed more frequently among HIV-positive MSM,14 given the rates of UAI with partners of different or unknown HIV status we have observed, there is a potential for overspill between HIV-positive and HIV-negative MSM populations. We observed high rates of UAI and of UAI without serosorting, particularly among HIV-positive individuals. We would argue, in this rapidly evolving HCV epidemic in Switzerland and in the face of high-risk sexual practices, that HCV counseling should be offered to MSM regardless of HIV status and testing should be offered to MSM engaging in high-risk practices. Although Schmidt et al. concluded in their article on MSM in Zurich that there was no reason for promoting HCV testing among all MSM in Switzerland, their conclusion was based on data predating the changing HCV epidemiology and drug use patterns among some MSM. Indeed, in Switzerland, members of the Swiss Federal Office of Public Health and Swiss Experts in Viral Hepatitis recently presented a consensus on at-risk populations for HCV infection which included MSM, individuals who use intranasal drugs, and sexual partners of individuals with HCV infection.2
This is the first study exploring HCV awareness among MSM in Switzerland. Although only 1 new case of HCV infection was diagnosed, high levels of UAI and UAI without HIV serosorting were reported and HCV awareness in this population was less than 100%. With the caveat that there was potential recruitment bias in our study, the low HCV seroprevalence observed suggests that HCV screening of non-HIV-positive MSM would not be cost-effective. Against this, we observe some high-risk behavior among HIV-negative MSM and those of unknown HIV status. In the light of these observations and of emerging HCV transmission trends elsewhere in Europe, we would suggest that HCV counseling and testing should be offered to all MSM presenting risk factors for HCV infection, regardless of HIV status.
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