HIV transmission among gay men through oral sex and other uncommon routes: case series of HIV seroconverters, Sydney
Richters, Julieta; Grulich, Andrewb; Ellard, Jeannea; Hendry, Olympiab; Kippax, Susana
aNational Centre in HIV Social Research, and bNational Centre in HIV Epidemiology and Clinical Research, University of New South Wales, Sydney, NSW 2052, Australia.
Sponsorship: The National Centre in HIV Social Research and the National Centre in HIV Epidemiology and Clinical Research are supported by grants from the Australian government's Department of Health and Ageing.
Received: 11 December 2002; revised: 19 March and 23 April 2003; accepted: 20 May 2003.
Seventy-five homosexual men with recently acquired HIV were interviewed about their risk behaviour. Fifty-nine reported unprotected anal intercourse, and one shared injecting equipment, with a partner not known to be HIV negative. Of the remaining 15, 11 reported protected anal intercourse. In five of the 15 we judged oral sex to be the most likely source of infection, including three men who had a genital piercing. The possible transmission risk from genital piercing should be investigated.
Among homosexual men, unprotected receptive anal intercourse poses the highest risk of HIV transmission. Although it is agreed that the risk of transmission through oral sex is low, the precise degree of risk is difficult to establish [1–6] and sporadic cases have been reported .
Between 1993 and 1999, 75 homosexually active men in Sydney, with documented recent seroconversion, were interviewed in depth about the event(s) that may have led to their infection. A questionnaire schedule about all risk events in the previous 6 months was also administered. Transcripts were studied in detail and discrepancies discussed until investigators achieved consensus on each case.
To decide the most likely mode of transmission in each case we established a risk hierarchy. On the basis of epidemiological data, per-contact risk estimates and physiological plausibility [1,7–11], we assumed that sharing a needle for drug injection, unprotected receptive and insertive anal intercourse were high risk, and that condom-protected receptive and insertive anal intercourse, blood or semen contact with an open wound, oral sex and penile–anal external contact without insertion (`nudging') were medium to low risk. We regarded visits to dentists or blood donation in Australia, stepping on a discarded syringe, sex with a verified HIV-negative partner and mosquito bites as representing no risk. We adjusted in each case for the probability that the partner was infected, his likely viral load, timing in relation to any seroconversion illness, the presence of skin lesions, whether ejaculation occurred, and the length and vigour of the sexual act.
One man reported sharing injecting equipment with an HIV-positive partner. Fifty-nine men had had at least one episode of unprotected anal intercourse with an HIV-positive partner or one of unknown serostatus. Some of these men did not at first report brief or partial insertion as ‘intercourse', and regarded themselves as having had 100% safe sex. Some initially reported oral sex as their most likely source of infection. The remaining 15 men were judged to have acquired HIV through a less common route. Eleven of the 15 men also had protected anal intercourse, which they often assumed was 100% safe and did not report until questioned in detail.
We initially expected that the most plausible cases of oral transmission would be those involving receptive fellatio with ejaculation . However, in three of the five cases in which we judged oral transmission to be likely, insertive fellatio by a man with a penile piercing was the highest risk implicated. It is difficult to be certain that the risk pattern here is entirely a matter of the physical risk associated with a skin lesion rather than of the higher risk of exposure to positive partners, as the gay subculture of men involved in the leather scene, many of whom practise bondage and discipline and other esoteric sexual practices such as fisting, has a high proportion of HIV-positive men . Although aware that being pierced posed a risk of HIV or hepatitis C if the procedure was performed unhygienically, most men were unaware of any further risk once the initial wound had apparently healed.
Of the other two cases of likely oral transmission, one had no anal intercourse but receptive oral sex with ejaculation when he had gingivitis and dental treatment (open wound in mouth). The other had a single instance of condom-protected receptive anal intercourse with a man having anal sex for the first time, and multiple oral sex contacts with casual partners.
In studies attempting to quantify the risk of seroconversion associated with a particular sexual act, the ambiguity of some narratives would be seen purely as an obstacle to accuracy, or perhaps as a reason for excluding them from analysis. However, the apparently clear categories of questionnaire data do not remove such ambiguity but merely conceal it. Our in-depth interviews are likely to have elicited data that would not have been reported in a written questionnaire study. In one study, 55% of men who initially denied receptive anal intercourse in a written questionnaire later recalled it when they were interviewed . However, it is still possible that not all high-risk exposures were reported. Even a skilled interviewer cannot elicit a clear account of an event that is remembered through an emotional or drug-induced haze, or which was confusing to the respondent at the time. Definitions vary; a man who does not define fellatio or nudging as ‘sex’ will be unlikely to remember and report it. Reports of protected anal intercourse often emerged late in interviews when men had argued that their oral exposure was a more likely source of infection than their protected anal sex. Breaches in ‘safety protocol’ such as nudging or brief intromission without a condom were often ignored or concealed until probing questions were asked.
This case series cannot quantify the risk associated with oral sex. It is clear from the cohort and case–control studies that have analysed the risk that it is very low . Cohort studies of serodiscordant couples in whom sexual behaviour data are collected prospectively have not identified any cases of orogenital transmission [14,15]. Nevertheless, it is likely that cases of HIV transmission through unusual routes do occur.
Our participants were recruited through a network of general practitioners with high HIV caseloads. It is possible that men whose transmission route was uncommon were more likely to be referred to the study.
Among Sydney's gay and homosexually active men, condom use for oral sex has been neither recommended nor adopted since the advent of AIDS . Our findings suggest a need to investigate HIV transmission by breaches in skin integrity and to increase men's awareness of this issue. Body piercings, particularly of the genitals, may constitute a breach even when the skin has apparently healed on the surface, as the presence of a metal stud or ring may well cause ongoing subclinical inflammation . Furthermore, inflammatory skin conditions such as psoriasis can allow the entry of HIV, and are poorly recognized among gay men as constituting a potential site of entry for HIV. Dentists should explicitly warn patients about the infection risk associated with oral sex after performing invasive procedures or diagnosing gingivitis.
1. Mastro TD, de Vincenzi I. Probabilities of sexual HIV-1 transmission. AIDS
1996, 10 (Suppl A)
2. Ostrow DG, Di Franceisco WJ, Chmiel JS, Wagstaff DA, Wesch J. A case–control study of HIV-1 seroconversion and risk-related behaviours in the Chicago MACS/CCS cohort, 1984–1992. Am J Epidemiol
3. Williams DI, Stephenson JM, Hart GJ, Copas A, Johnson AM, Williams IG. A case–control study of HIV seroconversion in gay men 1988–1993: what are the current risk factors? Genitourin Med
4. Burcham JL, Tindall B, Marmor M, Cooper DA, Berry G, Penny R. Incidence and risk factors for HIV seroconversion in a cohort of Sydney homosexual men. Med J Aust
5. Osmond DH, Page K, Wiley J, Garrett K, Sheppard HW, Moss AR, et al
. HIV infection in homosexual and bisexual men 18 to 29 years of age: the San Francisco Young Men's Study. Am J Public Health
6. Page-Schafer K, Veugelers PJ, Moss AR, Strathdee S, Kaldor JM, van Griensven GJP. Sexual risk behaviour and risk factors for HIV-1 seroconversion in homosexual men participating in the Tricontinental Seroconverter Study, 1982–1994. Am J Epidemiol
7. Rothenberg RB, Scarlett M, del Rio C, Reznik D, O'Daniels C. Oral transmission of HIV. AIDS
8. 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
9. Dillon B, Hecht F, Swanson M, Goupil-Sormany I, Grant RM, Chesney MA, Kahn JO. Primary HIV infections associated with oral transmission.
In: 7th Conference on Retroviruses and Opportunistic Infections
. San Francisco, 2000 [Abstract 473].
10. Hawkins DA. Oral sex and HIV transmission. Sex Transm Infect
11. Samuel MC, Hessol N, Shiboski S, Engel RR, Speed TP, Winkelstein W Jr. Factors associated with human immunodeficiency virus seroconversion in homosexual men in three San Francisco cohort studies, 1984–1989. J Acquir Immune Defic Syndr
12. Kippax S, Campbell D, Van de Ven P, Crawford J, Prestage G, Knox S, et al
. Cultures of sexual adventurism as markers of HIV seroconversion: a case control study in a cohort of Sydney gay men. AIDS Care
13. Keet IPM, Albrecht van Lent N, Sandfort TGM, Coutinho RA, van Griensven GJP. Orogenital sex and the transmission of HIV among homosexual men. AIDS
14. Page-Shafer K, Shiboski CH, Osmond DH, Dilley J, McFarland W, Shiboski SC, et al
. Risk of HIV infection attributable to oral sex among men who have sex with men and in the population of men who have sex with men. AIDS
15. Del Romero J, Marincovich B, Castilla J, García S, Campo J, Hernándo V, et al
. Evaluating the risk of HIV transmission through unprotected orogenital sex [Research letter]. AIDS
16. Kippax S, Noble J, Prestage G, Crawford JM, Campbell D, Baxter D, et al
. Sexual negotiation in the AIDS era: negotiated safety revisited. AIDS
17. Gokhale R, Hernon M, Ghosh A. Genital piercing and sexually transmitted infections [Letter]. Sex Transm Infect
© 2003 Lippincott Williams & Wilkins, Inc.
What does "Remember me" mean?
By checking this box, you'll stay logged in until you logout. You'll get easier access to your articles, collections,
media, and all your other content, even if you close your browser or shut down your
To protect your most sensitive data and activities (like changing your password),
we'll ask you to re-enter your password when you access these services.
What if I'm on a computer that I share with others?
If you're using a public computer or you share this computer with others, we recommend
that you uncheck the "Remember me" box.
Data is temporarily unavailable. Please try again soon.