HIV/AIDS Epi Update - May 2004

Oral Sex and the Risk of HIV Transmission

Introduction

At A Glance

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

Poor oral health and the presence of other STIs may increase the risk of HIV transmission through oral sex.

The actual risk of HIV transmission through oral sex is difficult to assess since research subjects may underreport 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.

The risk of HIV transmission through unprotected anal and vaginal intercourse is well known. Estimates of the probability of per-sex-act (receptive penile-anal intercourse with ejaculation) HIV transmission among homosexual men in the USA range from 0.005 to 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 not as 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.

Another study attempted to calculate the population-attributable risk percentage (PAR%) for HIV prevalence associated with fellatio. PAR% refers to the incidence of a disease (in this case, HIV) in a population that can be attributed to a certain risk behaviour (in this case, fellatio). The study focused on MSM and found that the PAR% was 0.18% for MSM who had had one partner in the previous six months, 0.25% for two partners, and 0.31% for three partners.⁵

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 of rhesus monkeys to SIV, oral exposure of humans to HIV-1 likely carries the risk of infection.⁶
• 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.⁷
• Another study took oral tissue samples from non-infected subjects and exposed them to three types of HIV. The researchers found that normal human oral keratinocytes (NHOKs), which are produced in the mouth, can become infected with HIV and transmit the virus to adjacent leukocytes. Though certain orally produced glycolipids can inhibit HIV replication and the infectivity noted was lower than in blood plasma, the results still demonstrate the risk of potential HIV oral transmission.⁸

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 MSM with a recent diagnosis of HIV infection, it was found that 7.8% of subjects (eight of 102) were probably infected through receptive oral sex.⁹
• In a 1986-1988 prospective study of HIV infection and AIDS among MSM in the Netherlands, four of 102 cases of seroconversion (3.9%) likely occurred as a result of receptive oral intercourse.¹⁰
• In a 1990-1992 study of gay men with newly diagnosed HIV infection, six of 37 patients (16.2%) who had been infected within a year before testing claimed receptive oral sex as the only possible route of their infection.¹¹

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 MSM in the Netherlands, five of 102 seroconverters (4.9%) may have been infected through insertive orogenital or oral-anal intercourse.¹⁰
• In an early cohort study of MSM, two of five cases of HIV seroconversion were attributed to insertive orogenital sex.¹²

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

• In the UK, 13 cases of HIV transmission through orogenital 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 orogenital contact was the only risk.¹³
• In a US study describing the clinical and epidemiological features of primary HIV infection, four of 46 patients reported having had only unprotected orogenital contact during the suspected sexual 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.¹⁹
• In the Polaris study in Ontario, researchers examining the difference between recent seroconverters and HIV-negative MSM reported that 97% of the sample of seroconverters (n = 62) practised unprotected oral sex, as did 73% of HIV-negative MSM (n = 121). Further, 55% of recent seroconverters and 27% of HIV-negative MSM reported exposure to ejaculate while engaging in unprotected oral sex.²⁰

Oral Risk Behaviours among Heterosexuals

• In a study of female street youth involved in prostitution in Montreal, researchers found that condom use was extremely low during oral sex. Only 5% of girls involved in prostitution and 4% of girls not involved in prostitution used condoms while performing fellatio.²¹

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).²² A number of researchers have suggested, however, that bisexual activity may be underreported by gay women, and therefore that not all the cases of female-to-female transmission of HIV infection are authentic.²³

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).²⁴
• Cases of infection in men following oral sex with their female partners have been reported, including one in which a man was apparently infected through fellatio involving a prostitute.25,26
• In a study of 741 MSM in the Netherlands, orogenital contact was identified as an independent risk for HIV acquisition, although this result was not statistically significant.¹⁵
• 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.¹⁶
• In the Omega cohort in Quebec, 10 out of 629 MSM participants (1.6%) seroconverted and listed only unprotected receptive oral intercourse as the possible route of their infection.¹⁷
• In Australia, researchers looking at MSM and risk behaviours found that five out of 75 recently seroconverted subjects (6.7%) in the study were likely infected by oral intercourse. The authors note that it is difficult to be certain of the actual mode of transmission. The subjects had varying risk profiles: for example, one had a penile piercing that could have caused transmission, another had gingivitis and dental treatment, and another had had protected anal intercourse.¹⁸

Prevalence of Unprotected Oral Sex among Homosexual Males

• The Omega cohort study in Quebec examined the prevalence of unprotected oral sex among 400 MSM by the HIV serostatus of their partners. Researchers found rates for unprotected oral sex of seropositive male partner (receptive fellatio).²⁴
• Cases of infection in men following oral sex with their female partners have been reported, including one in which a man was apparently infected through fellatio involving a prostitute.^25,26
• On the other hand, a study in Madrid of 135 serodiscordant couples reported over 19,000 instances of unprotected oral sex between spouses without one seroconversion, showing that this behaviour requires further investigation.²⁷

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 of the cells that are the most susceptible to HIV.28 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).²⁹

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.13 For receptive fellatio, poor oral health and taking ejaculate in the mouth is a hazardous combination that increases the risk of HIV transmission.³⁰

• In a 1996 cross-sectional study of crack cocaine smokers, oral lesions were associated with HIV infection among persons who reported receptive oral sex.³¹
• 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.³²
• Of the eight MSM in the Options Project in San Francisco in 2000 who may have acquired their HIV infection through receptive oral intercourse, three reported oral problems, including occasional bleeding gums.⁹

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 carrying a negligible risk of HIV transmission regardless of condom use. Receptive fellatio between men, or between men and women, is classified as carrying 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). The CAS currently cautions that the risk of transmission from receptive fellatio is increased if lesions or sores are present in the mouth.³³
• With respect to insertive cunnilingus between men and women or between two women, the CAS regards this practice as carrying 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 carrying a negligible HIV risk.³³
• Both insertive and receptive anilingus, with or without a barrier, between partners of the same sex or opposite sex are viewed by the CAS as carrying a negligible risk of HIV transmission.³³
• The CAS emphasizes that the risk of transmission of HIV (or other STIs) 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.³³

Conclusions

The risk of HIV transmission through oral sex is difficult to assess because HIV seroconverters may underreport 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.³⁴ 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 of inhibitory substances in saliva.³⁴ Also, the HIV incidence and prevalence in the community, the role of antiretroviral therapy and the extent to which personal prophylaxis is adopted will influence the contribution of oral sex to HIV transmission.³⁴

While oral sex is a lower risk activity than unprotected anal or vaginal intercourse, repeated exposures may increase the risk. Although the risk of acquiring HIV through oral sex is low, the higher rates of practising oral sex indicate that it may contribute to significant numbers of HIV cases among MSM. 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):849-56.
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 Immune Defic Syndr 1994;7(11):1169-84.
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 et al.
   Per-contact risk of human immuno-deficiency virus transmission between male sexual partners. Am J Epidemiol 1999;150(3):306-11.
5. Page-Shafer K, Shiboski CH, Osmond DH 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 2002;16(17):2350-52.
6. Baba TW, Trichel AM, An L et al.
   Infection and AIDS in adult macaques after non-traumatic oral exposure to cell-free SIV. Science 1996;272(5267): 1486-89.
7. Baron S, Poast J, Richardson J et al.
   Oral transmission of human immuno-deficiency virus by infected seminal fluid and milk: a novel mechanism. J Infect Dis 2000;181(2):498-504.
8. Liu X, Zha J, Chen H et al.
   Human immunodeficiency virus type 1 infection and replication in normal human oral keratinocytes. J Virol 2003;77(6): 3470-76.
9. Dillon B, Hecht FM, Swanson M et al.
   Primary HIV infections associated with oral transmission. 7th Conference on Retroviruses and Opportunistic Infections, San Francisco, January 30th-February 2nd, 2000 (abstract 473).
10. Keet IP, Albrecht van Lent N, Sandfort TG et al.
    Orogenital sex and the transmission of HIV among homosexual men. AIDS 1992;6(2):223-26.
11. Grutzmeir S, Bratt G Ramstedt G et al.
    HIV transmission in gay men in Stockholm 1990-1992. International Conference on AIDS, 1993 (abstract PO-CO2-2584).
12. Rozenbaum W, Gharakhanian S, Cardon B et al.
    HIV transmission by oral sex. Lancet 1988;1(8599):1395.
13. Robinson EK, Evans BG.
    Oral sex and HIV transmissions. AIDS 1999; 13(6):737-8.
14. Schacker T, Collier AC, Hughes J et al.
    Clinical and epidemiologic features of primary HIV infection. Ann Intern Med 1996;125(4):257-64.
15. Van Griensven GJP, Tielman RAP, Goudsmit J et al.
    Risk factors and prevalence of HIV antibodies in homosexual men in the Netherlands. Am J Epidemiol 1987;125(6):1048-57.
16. Darrow WW, Echenberg DF, Jaffe HW et al.
    Risk factors for human immunodeficiency virus (HIV) infections in homosexual men. Am J Public Health 1987;77(4):479-83.
17. Alary M, Remis RS, Otis J et al., 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.
18. Richters J, Grulich A, Ellard J et al.
    HIV transmission among gay men through oral sex and other uncommon routes: case series of HIV seroconverters, Sydney. AIDS. 2003;17(15):2269-71.
19. Remis RS, Dufour A, Alary M et al., 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).
20. Calzavara L, Burchell AN, Remis RS et al.
    Delayed application of condoms is a risk factor for human immunodeficiency virus infection among homosexual and bisexual men. Am J Epidemiol 2003;157(3):210-7.
21. Weber AE, Boivin JF, Blais L et al.
    HIV risk profile and prostitution among female street youths. J Urban Health 2002;79(4):525-35.
22. Perry S, Jacobsberg L, Fogel K.
    Orogenital transmission of human immunodeficiency virus. Ann Intern Med 1989;111(11):951-52.
23. Edwards S, Carne C.
    Oral sex and the transmission of viral STIs. Sex Transm Infect 1998;74(1):6-10.
24. Puro V, Narciso P, Girardi E et al.
    Male to female transmission of human immunodeficiency virus by orogenital sex. Eur J Clin Microbiol Infect Dis 1991;10(1):47.
25. 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.
26. Quarto M, Germinario C, Troiano T et al.
    HIV transmission by fellatio. Eur J Epidemiol 1990;6(3):339-40.
27. Del Romero J, Marincovich B, Castilla J et al.
    Evaluating the risk of HIV transmission through unprotected orogenital sex. AIDS 2002;16(9): 1296-97.
28. Reucroft S, Swain J. Saliva thwarts HIV. New Scientist 1998;157(2117):23.
29. Baron S. Oral transmission of HIV, a rarity: emerging hypotheses. J Dent Res 2001;80(7):1602-4.
30. Sayler D.
    Oral oversights. Surviv News (Atlanta, Ga) Nov 10, 2001
31. Faruque S, Edlin BR, McCoy CB et al.
    Crack cocaine smoking and oral sores in three inner-city neighborhoods. J Acquir Immune Defic Syndr Hum Retrovirol 1996;13(1):87-92.
32. 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).
33. Canadian AIDS Society.
    HIV transmission: guidelines for assessing risk: a resource for educators, counsellors, and health care providers. Ottawa: CAS, 1999.
34. Rothenberg RB, Scarlett M, Del Rio C et al.
    Oral transmission of HIV. AIDS 1998;12(16):2095-2105.

[Back] [Table of Contents] [Next]