To the Editors:
HIV transmission affects certain risk groups disproportionately in France, particularly men having sex with men (MSM), in whom the incidence has remained very high in recent years.1 The frequency of other sexually transmitted infections (STI), including gonorrhea, syphilis, Chlamydia trachomatis, and lymphogranuloma venereum, has also increased, again mainly in MSM.2 Here, we describe time trends in self-reported sexual practices likely to be the source of HIV-1 infection among 806 MSM enrolled during primary HIV-1 infection between 1996 and 2010.
Patients are enrolled in the ongoing ANRS PRIMO cohort if they present during HIV-1 primary infection (incomplete Western blot, or p24 Ag/HIV RNA+ with a negative or weakly reactive enzyme-linked immunosorbent assay, or an interval between a negative and a positive enzyme-linked immunosorbent assay of less than 6 months).3,4 The median time between the estimated date of HIV infection and enrollment was 48 days (interquartile range: 36–67 days). Patients were asked about the likely circumstances of HIV infection at enrollment (sexual, intravenous, other) and their sexual preference, their number of sexual partners during the 6 months before diagnosis, and the following information on each partner: gender, HIV-1 serostatus (negative, positive, or unknown), steady or casual status, and condom use (never, seldom, often, or always). When patients attributed their infection to the sexual route, they were also asked if they could identify the likely sexual partner and practices. This questionnaire was clinician administered until 2000 and subsequently self-completed by the patients.
A total of 1245 HIV-1–infected subjects, 871 (70%) of whom were MSM, were enrolled in the cohort from 1996 to 2010. The number and proportion of MSM increased over time, from 64% in 1996–97 to 75% in 2010 (P trend = 0.01). Information on the sexual practices likely to be the source of HIV infection was provided by 806 MSM who attributed their infection to sexual contact. One-quarter of these MSM reported that unprotected orogenital sex was the likely source of infection. This proportion was lower (16.1%) and stable over time among the 396 MSM who could identify the likely source partner (Fig. 1, top panel). Unprotected anal sex was the main sexual practice (69.4%) to which these latter MSM attributed their HIV infection throughout the study period. MSM who could not identify the sexual partner likely to be the source of their infection (n = 410) increasingly reported unprotected orogenital sex as the sexual practice likely to have led to HIV infection, the proportion rising from 25.0% before 2000 to 46.1% in 2010 (P trend = 0.01) (Fig. 1, bottom panel). Among MSM who thought they were infected through orogenital sex, 37.6% also reported unprotected anal intercourse at least once during this 6-month period. When we reclassified these subjects as being infected through unprotected anal course, we still observed an increase in infections attributed to orogenital sex, from 16.3% in 2000 to 35.1% in 2010 (Fig. 1, bottom panel, solid line). Of note, a low percentage of patients (around 10%) reported condom failure as the source of infection, and this frequency was stable over time.
This study shows that, in France, an increasing percentage of men who have sex with men attribute their HIV infection to unprotected orogenital sex, when questioned soon after primary infection diagnosis. Oral sex has been reported as a potential source of HIV infection in MSM,5 but the precise risk is difficult to estimate because unprotected anogenital intercourse may be denied6 and the HIV serostatus of casual partners is often unknown.7 In addition, the event to which MSM attribute their HIV infection may not be the event actually responsible.8 It is conceivable that the increase in the proportion of cases of HIV infection self-attributed to unprotected orogenital sex might partly be due to a rise in underreporting of unprotected anal intercourse for reasons of social acceptability. However, the increase was only observed among MSM who could not identify their likely source partner. In addition, it was first noted after the switch from clinician- to self-administered questionnaires, and we have previously shown that such a switch leads to an increase, not a decrease, in the reporting of risky sexual practices such as unprotected anal sex.4 Our results are consistent with those of the national French Presse Gay study, which showed that orogenital sex among MSM is frequent between casual partners (98% of responders) and that semen exposure was higher in 2004 than in previous surveys (2000 and 1997) during sex with both steady and casual partners.9 The per-contact risk associated with unprotected receptive oral sex with partners of positive or unknown HIV serostatus has been estimated at about 0.04% (95% confidence interval: 0.01 to 0.17).10 However, the risk of infection may be much higher, notably in settings with a high prevalence of STIs, and a high prevalence of undiagnosed primary infection.11,12
Our data do not allow us to quantify the contribution of unprotected orogenital intercourse to the incidence of HIV infection in the MSM population. However, as this practice is known to be at risk of HIV infection, and given the increasing self-reporting of this practice as a likely source of infection, MSM should be warned of the risk of HIV infection through both unprotected anal and orogenital sex, particularly in settings where the prevalence of STIs and undiagnosed HIV infection is high, as in gay commercial venues.13 They also should be warned about the potential risk of HIV infection with oral disease manifestations.
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