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AIDS:
doi: 10.1097/QAD.0b013e32833dbdfd
Correspondence

Infectiousness of HIV-infected homosexual men in the era of highly active antiretroviral therapy

Baggaley, Rebecca Fa; White, Richard Gb; Boily, Marie-Claudec

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aMRC Centre for Outbreak Analysis and Modelling, Department of Infectious Disease Epidemiology, Faculty of Medicine, Imperial College London, UK

bInfectious Disease Epidemiology Unit, Department of Epidemiology and Population Health, London School of Hygiene and Tropical Medicine, UK

cDepartment of Infectious Disease Epidemiology, Faculty of Medicine, Imperial College London, London, UK.

Received 20 May, 2010

Accepted 30 June, 2010

The recent study by Jin et al. [1] provides estimates of infectiousness of anal intercourse (insertive circumcised and uncircumcised; receptive with and without ejaculation) for the male homosexual population of Sydney, Australia, in the highly active antiretroviral therapy (HAART) era. There is a lack of estimates of HIV infectiousness for homosexual men and for anal intercourse in general and especially for infectiousness with treatment. A recent literature review [2] found only four studies reporting estimates of HIV transmissibility per anal intercourse act. Therefore, the additional data presented by Jin et al. [1] are an important contribution to the literature. There are many methodological challenges when quantifying HIV infectiousness, which have been discussed elsewhere [3,4]. Although the best study design for quantifying per-act HIV infectiousness for heterosexual populations has involved discordant monogamous couples (although compromised with its own set of biases), these types of study have been seldom used for homosexual populations. It may be more difficult to recruit such participants if rates of monogamy are lower than among heterosexual populations, and monogamous homosexual couples may also not be very representative of the wider male homosexual community. The alternative approach used by Jin et al. [1] was to follow up initially HIV-seronegative homosexual men, testing annually for seroconversion and interviewing every 6 months for reports of types and frequencies of sexual exposure and the presumed serostatus of their sexual partners (categorized as HIV negative, positive or unknown). A similar approach has been used before for anal intercourse by Vittinghoff et al. [5] as well as for female sex workers [6,7]. However, Vittinghoff et al. [5] were unable to provide per-act estimates per positive exposure for insertive anal intercourse, only providing estimates per-act with an ‘infected or unknown serostatus’ partner and, therefore, may underestimate infectiousness per exposure, if HIV prevalence among unknown serostatus partners is low.

The per-act anal intercourse transmission probability estimates of Jin et al. [1] with respect to receptive unprotected anal intercourse [0.65%, 95% confidence interval (CI) 0.15–1.53 with withdrawal; 1.43%, 95% CI 0.48–2.85 with ejaculation], from a population with high (proposed 70%) HAART coverage, are remarkably similar to those estimates made preceding HAART (summary of four estimates: 1.4%, 95% CI 0.2–2.5, no differentiation by ejaculation [2], see Fig. 1 [2,5,8–10]). As the authors note, this result is surprising, given the reduction in community viral load that has been observed in some other homosexual populations following the introduction of HAART [11], and that such reductions in viral load are expected to reduce HIV infectiousness.

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Potential reasons why HIV infectiousness was not seen to decrease include higher infectiousness associated with various cofactors (sexually transmitted infection prevalence may be higher in male homosexual communities now, perhaps as a result of risk compensation in the HAART era); there may be unreported competing exposures through other routes of transmission, such as intravenous drug use; or the partners of study participants may not have been representative of the wider Australian homosexual population, for example, with lower HAART coverage. It would have been useful to have more information regarding the likely HAART coverage of the infected partners, in order to assess how concerning these unexpectedly high estimates for infectiousness are. Although the authors state that 70% of male homosexuals diagnosed in Australia are currently treated, estimates of the proportion of those infected who are diagnosed as well as an indication of adherence levels and average viral loads for those individuals receiving treatment are required to improve our understanding.

The authors addressed the uncertainty regarding ‘unknown’ serostatus and presumed HIV-negative sexual partners by undertaking uncertainty analysis, varying the HIV prevalence of the ‘unknown’ and presumed HIV-negative partner populations from 5–15% and 0.5–2%, respectively, based on prevalence studies from the locality. It would be informative if this analysis could be extended to reflect the uncertainty in HAART coverage levels in order to explore how sensitive the HIV infectiousness estimates are to the assumed proportion of sexual partners on treatment.

However, even in the absence of further information, levels of HAART are likely to be substantial and so the authors' observation that their per-act estimates are not markedly different from those made in the absence of HAART remains a concerning finding. Community viral load studies covering the Sydney population may help to explain these findings, although the association between viral load and HIV infectiousness for sexual transmission, particularly for anal intercourse, remains to be definitively proven. It would also be useful, if data are available or for future cohorts, to ascertain the treatment status of infected partners wherever possible, in order to make estimates of anal intercourse infectiousness stratified by treatment status. This study and our review have clearly highlighted the need for more data on HIV infectiousness for sexual transmission among homosexual men [1,2].

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Acknowledgement

There are no conflicts of interest.

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References

1. Jin F, Jansson J, Law M, Prestage GP, Zablotska I, Imrie JC, et al. Per-contact probability of HIV transmission in homosexual men in Sydney in the era of HAART. AIDS 2010; 24:907–913.

2. Baggaley RF, White RG, Boily MC. HIV transmission risk through anal intercourse: systematic review, meta-analysis and implications for HIV prevention. Int J Epidemiol 2010. [Epub ahead of print]; DOI: 10.1093/ije/dyq057.

3. Powers KA, Poole C, Pettifor AE, Cohen MS. Rethinking the heterosexual infectivity of HIV-1: a systematic review and meta-analysis. Lancet Infect Dis 2008; 8:553–563.

4. Boily MC, Baggaley RF, Wang L, Masse B, White RG, Hayes RJ, Alary M. Heterosexual risk of HIV-1 infection per sexual act: systematic review and meta-analysis of observational studies. Lancet Infect Dis 2009; 9:118–129.

5. Vittinghoff E, Douglas J, Judson F, McKirnan D, MacQueen K, Buchbinder SP. Per-contact risk of human immunodeficiency virus transmission between male sexual partners. Am J Epidemiol 1999; 150:306–311.

6. Gilbert PB, McKeague IW, Eisen G, Mullins C, Gueye NA, Mboup S, Kanki PJ. Comparison of HIV-1 and HIV-2 infectivity from a prospective cohort study in Senegal. Stat Med 2003; 22:573–593.

7. Donnelly C, Leisenring W, Kanki P, Awerbuch T, Sandberg S. Comparison of transmission rates of HIV-1 and HIV-2 in a cohort of prostitutes in Senegal. Bull Math Biol 1993; 55:731–743.

8. DeGruttola V, Seage GR 3rd, Mayer KH, Horsburgh CR Jr. Infectiousness of HIV between male homosexual partners. J Clin Epidemiol 1989; 42:849–856.

9. Leynaert B, Downs AM, de Vincenzi I. Heterosexual transmission of human immunodeficiency virus: variability of infectivity throughout the course of infection. European Study Group on Heterosexual Transmission of HIV. Am J Epidemiol 1998; 148:88–96.

10. Halperin DT, Shiboski SC, Palefsky SC, Padian NS. High level of HIV-1 infection from anal intercourse: a neglected risk factor in heterosexual AIDS prevention [abstract #ThPeC7438]. Int Conf AIDS 7–12 July 2002; University of California, San Francisco, United States; 2002. p. 14.

11. Das-Douglas M, Chu P, Santos G-M, Scheer S, McFarland W, Vittinghoff E, Colfax G. Decreases in community viral load are associated with a reduction in new HIV diagnoses in San Francisco [abstract #33]. In: 17th Conference on Retroviruses and Opportunistic Infections; 16–19 February 2010; San Francisco, California, USA; 2010.

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