Oral Sex and the Risk of HIV Transmission

HIV/AIDS Epi Updates

At A Glance

Unprotected oral sex has been associated with HIV infection in some studies.

Poor oral health increases the risk of HIV transmission from oral sex.

The actual risk of HIV transmission through oral sex is difficult to assess since research subjects may under-report sexual activities that are of higher risk.

Oral sex, particularly unprotected receptive fellatio with ejaculation, should be considered as a potential risk behaviour for HIV transmission.

April 2003

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Oral Sex and the Risk of HIV Transmission

Introduction

The risk of HIV transmission through unprotected anal and vaginal intercourse is well known. Estimates of the per-sex-act probability of HIV transmission among homosexual men in the US through receptive penile-anal intercourse with ejaculation range from 0.005-0.03 during the asymptomatic phase of infection¹ to as high as 0.1-0.3 during primary HIV infection.² Analyses of data from North American and European studies of long-term heterosexual couples estimate the per-sex-act probability of HIV transmission through penile-vaginal intercourse to be approximately 0.001.³ However, the independent risk of HIV transmission through orogenital contact has been more difficult to study and is less well understood. One study calculated the per-sex-act probability of HIV transmission in a cohort of men who have sex with men (MSM) and determined that for unprotected receptive anal intercourse, the probability was 0.82% per act, for unprotected insertive anal intercourse 0.06%, and for unprotected receptive oral intercourse with ejaculation 0.04%.⁴ This remains the only study available that provides a probability for oral transmission, and further study is required to corroborate these estimates. This report updates current information on oral sex and the risk of HIV transmission. Current recommendations on the use of condoms for oral intercourse are also reviewed.

Laboratory and Animal Studies: Evidence Links HIV Infection to Oral Intercourse in Humans

• An animal study found that the minimal dose of simian immunodeficiency virus (SIV) (a virus closely related to HIV-1) required to achieve infection in adult rhesus monkeys through oral exposure was 6,000 times lower than was the minimal dose needed to achieve infection after rectal exposure. The researchers concluded that as with oral exposure to SIV by rhesus monkeys, oral exposure to HIV-1 by humans likely carries the risk of infection.⁵

• In a laboratory study designed to explore the oral transmission of HIV by seminal fluid and colostrum, normal donor samples of human milk, colostrum, seminal fluid, and blood were separately combined with samples of saliva and HIV-infected white blood cells. All samples, in normal physiologic volumes, prevented saliva from inactivating the HIV infected blood cells, leading the researchers to conclude that successful oral transmission of HIV by seminal fluid, milk, and colostrum may occur.⁶

Oral Sex Between Homosexual Males: Not as Safe as once Perceived

Several epidemiological studies have examined the risk of HIV infection through unprotected receptive oral intercourse (receptive fellatio):

• In a 1996-1999 study of homosexual men recently diagnosed with HIV infection, it was found that 7.8% of subjects (eight of 102) were probably infected through receptive oral sex.⁷

• In a 1986-1988 prospective study of HIV infection and AIDS among homosexual men in the Netherlands, four of 102 cases of seroconversion (3.9%) likely occurred as a result of receptive oral intercourse.⁸

• In a 1990-1992 study of newly diagnosed HIV- infected gay men, six of 37 patients who had been infected within a year before testing claimed only receptive oral sex as the possible route of their infection.⁹

Several studies have also explored the possibility of HIV transmission through unprotected insertive orogenital intercourse (insertive fellatio) or insertive oral-anal sex (insertive anilingus):

• In a prospective study of HIV infection among homosexual men in the Netherlands, five of 102 seroconverters (4.9%) may have been infected through insertive orogenital or oral-anal intercourse.⁸

• In an early cohort study of homosexual men, two of five cases of HIV seroconversion were attributed to insertive orogenital sex.¹⁰

Additional reports or studies, while not distinguishing the type of oral sex between homosexual men, further suggest the possibility of HIV transmission through oral-penile/oral-anal contact:

• In the UK, 13 cases of HIV transmission through oro-genital contact had been reported to the public health authorities up to December 1998. In two of these cases, the reporting physician was not convinced that oro-genital contact was the only risk.¹¹

• In a study to describe the clinical and epidemiologic features of primary HIV infection, four of 46 patients reported having had only unprotected orogenital contact during the suspected sexual encounter that led to their seroconversion.¹²

• In a study of 741 homosexual men in the Netherlands, orogenital contact was identified as an independent risk for HIV acquisition, although this result was not statistically significant.¹³

• In a US study, homosexual males who were participating in a hepatitis B study were found to have a higher risk of HIV infection from both orogenital and oro-anal contact.¹⁴

• In the Omega cohort in Quebec, 10 out of 629 (1.6%) MSM participants seroconverted and listed only unprotected receptive oral intercourse as the possible route of their infection.¹⁵

Prevalence of Oral Sex among Homosexual Males

• The Omega cohort study in Quebec examined the prevalence of unprotected oral sex among MSM by the HIV serostatus of their partners. Researchers found rates for unprotected oral sex of 94% with a seronegative regular partner, 91% with a regular partner of unknown serostatus, and 88% with a seropositive regular partner. For casual partners the rates were 92% with unknown or seronegative partners and 73% with seropositive partners.¹⁶

Female-to-Female Transmission of HIV through Oral Intercourse: Truth or Bias?

To date, there have been several reports of HIV transmission through orogenital contact between lesbians (cunnilingus).¹⁷ A number of researchers have suggested, however, that bisexual activity may be under-reported by gay women, and therefore that not all of the cases of female-to-female transmission of HIV infection are authentic.¹⁸

Possible Transmission of HIV Between Heterosexual Partners as a Result of Oral Intercourse

• There are several reported cases in the literature of women who acquired HIV infection after performing oral sex on their seropositive male partner (receptive fellatio).¹⁹

• Cases of infection in men following oral sex with their female partners have been reported, including one in which a man was apparently infected via fellatio involving a prostitute.^20,21

Potential Co-Factors for HIV Transmission during Oral Sex

Saliva that does not contain blood presents no potential for transmission, as research has shown that an enzyme in saliva inhibits HIV. In general, the mouth and throat are well defended against HIV: the oral mucosal lining contains few cells that are the most susceptible to HIV.²² Other research notes that saliva contains several HIV inhibitors, such as peroxidases and thrombospondin-1, and that the hypotonicity of saliva disrupts the transmission of infected leukocytes (white blood cells).²³

Case reports identify factors potentially associated with increased risk of HIV transmission through oral sex: oral trauma, sores, inflammation, concomitant sexually transmitted infections, ejaculation in the mouth, and systemic immune suppression.¹¹ For receptive fellatio, poor oral health and taking ejaculate in the mouth is a hazardous combination that increases the risk of HIV transmission.²⁴

• In a 1996 cross-sectional study of crack cocaine smokers, oral lesions were associated with HIV infection among persons who reported receptive oral sex.²⁵

• A 1993 study of female sex trade workers found that crack users who inconsistently used condoms when performing oral sex on their clients were more likely to be infected with HIV than were those who consistently used condoms when performing fellatio.²⁶

• Of the eight homosexual men in the Options Project who may have acquired their HIV infection through receptive oral intercourse, three reported oral problems, including occasional bleeding gums.⁷

Oral Sex and "Safer Sex Counselling": Existing Views and Recommendations

• The Canadian AIDS Society (CAS) currently classifies insertive fellatio between men, or between women and men, as having a negligible risk of HIV transmission regardless of condom use. Receptive fellatio between men, or between men and women, is classified as having negligible risk if a condom is used and as low risk if a condom is not used (whether or not semen is taken in the mouth). CAS presently cautions that the risk of transmission from receptive fellatio is increased if lesions or sores are present in the mouth.²⁷

• With respect to insertive cunnilingus between men and women or between two women, CAS regards this practice as having a negligible risk of HIV transmission if a barrier is used, and as low risk if no barrier is used (regardless of menstrual status). Receptive cunnilingus between men and women or between two women is regarded as having a negligible HIV risk.²⁷

• Both insertive and receptive anilingus, with or without a barrier, between partners of the same sex or opposite sex, are viewed by CAS as having a negligible risk of HIV transmission.²⁷

• CAS emphasizes that the risk of transmission of HIV (or other STDs) from any of these types of oral intercourse can be effectively reduced by the proper use of a latex barrier (condom or dental dam), and thus advocates the avoidance of unprotected orogenital or oro-anal contact.²⁷

Conclusions

The risk of HIV transmission through oral sex is difficult to assess because HIV seroconverters may under-report other higher-risk sexual practices. A literature review identified exposure to HIV through unprotected oral intercourse as an independent risk factor for HIV acquisition in only three (12.5%) of 24 epidemiological studies designed to examine risk of HIV from different sexual exposures.²⁸ It indicates that the importance of oral sex to HIV transmission is a complex result of the relative frequency of oral sex (among other activities), the infectivity of oral secretions and its modification by oral pathology, and the resistance to infection by inhibitory substances in saliva.²⁸ Also, the HIV incidence and prevalence in the community, the role of the antiretroviral therapy and the extent to which personal prophylaxis is adopted will influence the contribution of oral sex to HIV transmission.²⁸

While oral sex is a lower risk activity than unprotected anal or vaginal intercourse, repeated exposures may increase the risk. Safer sex practices should consider oral sex, particularly unprotected receptive fellatio with ejaculation, as a potential risk behaviour for HIV transmission.

References

1. DeGruttola V, Seage GR III, Mayer KH, Horsburgh CR. Infectiousness of HIV between male homosexual partners. J Clin Epidemiol 1989; 42(9): 849-856.

2. Jacquez JA, Koopman JS Simon CP, Longini IM Jr. Role of the primary infection in epidemics of HIV infection in gay cohorts. J Acquir Immun Deific Syndr 1994; 7(11):1169-1184.

3. Mastro TD, de Vincenzi I. Probabilities of sexual HIV-1 transmission. AIDS 1996; 10(Suppl A):S75-S82.

4. 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(3):306-11.

5. Baba TW, Trichel AM, An L, Liska V, Martin LN, Murphy- Corb M, and Ruprecht RM. Infection and AIDS in adult macaques after non-traumatic oral exposure to cell-free SIV. Science 1996; 272(5267):1486-1489.

6. Baron S, Poast J, Richardson J, Nguyen D, Cloyd M. Oral transmission of human immunodeficiency virus by infected seminal fluid and milk: a novel mechanism. J Infect Dis 2000; 181(2):498-504.

7. Dillon B, Hecht FM, Swanson M, Goupil-Sormany I, Grant RM, Chesney MA, Kahn JO. Primary HIV Infections Associated with Oral Transmission. 7th Conference on Retroviruses and Opportunistic Infections. San Francisco, January 30th-February 2nd, 2000 (abstract 473).

8. Keet IP, Albrecht van Lent N, Sandfort TG, Coutinho RA, van Griensven GJ. Orogential sex and the transmission of HIV among homosexual men. AIDS 1992; 6(2):223-226.

9. Grutzmeir S, Bratt G Ramstedt G, et al. HIV transmission in gay men in Stockholm 1990-1992. 1993 International Conference on AIDS (abstract PO-CO2-2584).

10. Rozenbaum W, Gharakhanian S, Cardon B, Duval E, Coulaud JP. HIV transmission by oral sex. Lancet 1988; 1(8599):1395.

11. Robinson EK, Evans BG. Oral sex and HIV transmissions. AIDS 1999;13(6):737-8.

12. Schacker T, Collier AC, Hughes J, Shea T, Corey L. Clinical and epidemiologic features of primary HIV infection. Ann Intern Med 1996;125(4):257-264.

13. van Griensven GJP, Tielman RAP, Goudsmit J, van der Noordaa J, de Wolf F, de Vroome EM, Coutinho RA. Risk factors and prevalence of HIV antibodies in homosexual men in the Netherlands. Am J Epidemiol 1987; 125(6):1048-1057.

14. Darrow WW, Echenberg DF, Jaffe HW, O'Malley PM, Byers RH, Getchell JP, Curran JW. Risk factors for human immunodeficiency virus (HIV) infections in homosexual men. Am J Public Health 1987; 77(4):479-83.

15. Alary M, Remis RS, Otis J, Masse B, Turmel B, LeClerc R, Lavoie R, Vincelette J, Parent R, the Omega Study Group. Risk factors for HIV seroconversion among men having sex with men (MSM) in Montreal. Can J Infect Dis 2002; 13(Suppl A):46A.

16. Remis RS, Dufour A, Alary M, Otis J, Vincelette J, Masse B, Turmel B, LeClerc R, the Omega Study Group. Patterns of oral sex among men who have affective and sexual relations with other men (MASM) in Montreal, Quebec. Can J Infect Dis 1998; 9(Suppl A):31A (Abstract 210).

17. Perry S, Jacobsberg L, Fogel K. Orogenital transmission of human immunodeficiency virus. Ann Intern Med 1989;111(11):951-952.

18. Edwards S, Carne C. Oral sex and the transmission of viral STIs. Sex Transm Inf 1998; 74(1):6-10.

19. Puro V, Narciso P, Girardi E, Antonelli L, Zaccarelli M, Visco G. Male to female transmission of human immunodeficiency virus by orogenital sex. Eur J Clin Microbiol Infect Dis 1991; 10(1):47.

20. Spitzer PG, Weiner NJ. Transmission of HIV infection from a woman to a man by oral sex. N Engl J Med 1989; 320(4):251.

21. Quarto M, Germinario C, Troiano T, Fontana A, Barbuti S. HIV transmission by fellatio. Eur J Epidemiol 1990; 6(3):339-340.

22. Reucroft S, Swain J. Saliva thwarts HIV. New Sci 1998; 157(2117):23.

23. Baron S. Oral transmission of HIV, a rarity: emerging hypotheses. J Dent Res 2001 Jul; 80(7):1602-4.

24. Sayler D. Oral oversights. Surviv News (Atlanta Ga) 2001 Nov; 10.

25. Faruque S, Edlin BR, McCoy CB,Word CO, Larsen SA, Schmidt DS, Von Bargen JC, Serrano Y. Crack cocaine smoking and oral sores in three inner-city neighborhoods. J Acquir Immune Defic Syndr Hum Retrovirol 1996; 13(1):87-92.

26. Wallace JI, Weiner AP. Intravenous drug use, inconsistent use, and fellatio in relationship to crack smoking as risky behaviour for acquiring HIV among streetwalkers, New York City, April 1989-December 1993. HIV Infected Women's Conference, February 22-24, 1995 (abstract S62).

27. Canadian AIDS Society. HIV transmission: guidelines for assessing risk: a resource for educators, counsellors, and health care providers. 1999, Ottawa.

28. Rothenberg RB, Scarlett M, Del Rio C, Reznik D, O' Daniels C. Oral transmission of HIV. AIDS 1998; 12(16):2095-2105.

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