Circumcision and male-to-male sexual transmission of HIV

In recent years, evidence from observational studies in sub-Saharan Africa has shown that circumcised men have a lower risk of acquiring HIV infection than uncircumcised men [1]. The proposed mechanism by which the circumcised state might protect against HIV infection is twofold. First, the inner surface of the foreskin contains Langerhans cells, which have HIV receptors, and is also vulnerable to traumatic epithelial disruptions during intercourse. Second, an intact foreskin exposes a man to a greater risk of ulcerative sexually transmitted infections, which in themselves are a risk factor for HIV acquisition. The evidence that circumcision may protect against HIV infection is now considered strong enough that trials evaluating the efficacy of circumcision as part of an HIV prevention package have been advocated [2]. Almost all of the literature suggesting that circumcision protects against HIV infection in men has been conducted in heterosexual individuals, mostly in developing countries [3]. We examined the relationship between circumcision and HIV transmission in homosexual men in Sydney, Australia. Between 1993 and 1999, we interviewed 74 homosexual men shortly after their diagnosis with newly acquired HIV infection. Men were asked to nominate an event of unprotected anal intercourse (UAI) with a serodiscordant or HIV status-unknown partner at which they believe they became HIV infected. If there was more than one such high-risk event, the interviewer selected the highest risk event as the occasion on which HIV was most likely to have been transmitted. Participants were also asked to report all instances of UAI in the 6 months before seroconversion. We hypothesized that if the presence of a foreskin was important in HIV transmission, then those men who were infected by insertive UAI would be more likely to be uncircumcised than those infected by receptive UAI. Sixty-three men nominated an event of UAI as their highest risk activity. After clarification of the most likely high-risk event by the interviewer, the highest risk practice reported was insertive UAI in 11 men, and receptive UAI in 52. Of the 11 men in whom insertive UAI was deemed the most likely mode of HIV transmission, all but one reported no receptive UAI in the 6 months before seroconversion (one reported receptive UAI with a single regular partner who was definitely HIV negative). Overall, 20 men were uncircumcised (27%). There was no association between circumcision and reporting insertive UAI as the highest risk practice (odds ratio 0.89, 95% confidence interval 0.18–5.98, see Table 1). Of the additional 11 men who denied UAI as the event that they believed led to their infection, eight also denied having had UAI in the previous 6 months. Of these eight, three were uncircumcised (38%).Table 1: Reported highest risk practice and circumcision status in 63 homosexual men infected with HIV through unprotected anal intercourse. Our finding that 17% of homosexual men with newly acquired HIV infection reported insertive UAI as their highest risk activity suggests that insertive UAI is an important means of HIV transmission in this population. However, we found no association between circumcision status and infection by insertive UAI. In addition, men who had seroconverted despite no reported event of UAI were also no more likely to be uncircumcised. These data strongly suggest that the foreskin is not the main source of HIV infection in homosexual men who become infected by insertive UAI, and that other sites, such as the distal urethra, must be important in HIV infection. The limitations of this study are that it was based on relatively small numbers, and it is possible that some men who reported receptive UAI as their highest risk behaviour may have been infected by insertive UAI. In addition, it is possible that men may have been reluctant to report an event of receptive UAI because of its perceived social unacceptability. The relationship between circumcision and HIV risk has rarely been examined in homosexual men [4]. A cross-sectional study [5] found that uncircumcised homosexual American men were more likely to have prevalent HIV infection (adjusted odds ratio 2.0, 95% confidence interval 1.0–4.0), but it was not known whether these men had been infected by insertive or receptive intercourse. Our data showing that there is no difference in the circumcision status of men infected by receptive or insertive UAI, in a population with a circumcision prevalence of approximately 75%, suggests that circumcision is not strongly protective against HIV infection in homosexual men. Larger studies, preferably of prospective design, are needed to confirm the absence of a relationship between circumcision and HIV infection risk in gay men. In the meantime, educational messages to homosexual men should continue to emphasize that insertive anal sex is a high-risk activity for HIV transmission whether or not the insertive partner is circumcised. Andrew E. Grulicha Olympia Hendrya Edward Clarka Susan Kippaxb John M. Kaldora