Comprehensive, up-to-date information on HIV/AIDS treatment, prevention, and policy from the University of California San Francisco

Researchers can consistently culture or otherwise detect HIV not only in blood, but also in semen (4-6) and cervical secretions (7-9) of infected persons. Infectious HIV exists in saliva,(7-13) tears,(14) and urine (15); however, it has only been recovered from these fluids at extremely low titers. In addition, no report has documented cases of HIV transmission by these fluids. Hence, saliva, tears, and urine are highly unlikely sources of HIV transmission.

Infectious HIV has also been isolated in breast milk, and transmission from HIV-infected mothers to nursing infants has been well documented.(16) Breast milk is not commonly encountered during sexual intercourse. However, should individuals accidentally or intentionally come in contact with HIV-infected breast milk during sex, care should be taken to avoid mucosal contact.

Epidemiologic evidence in support of male-to-male,(17-28) male-to-female,(29-43) and female-to-male (31,33,36,39,40,42-44) sexual transmission of HIV infection is abundant. The risk of HIV infection among women who have sex with women appears to be largely attributable to other risk factors (sex with men, injection drug use).(45-48) Female-to-female sexual transmission per se is uncommon, with rare case reports of possible HIV transmission by this route.(49-54) A 2003 case report suggested that sexual practices that can expose sex partners to each other's blood, such as the shared use of sex toys or vaginal penetration with hand ("fisting"), are a possible route of female-to-female sexual transmission.(54)

Results from early epidemiologic studies of HIV infection in homosexual men revealed that sexual activity with many different partners carries a high risk of HIV infection.(18,21-23) Many of the published reports of heterosexual transmission present no detailed data regarding this risk factor, presumably because the researchers examined transmission from HIV-infected persons to their monogamous sexual partners.(29,30,33,34,37,38,41) Researchers who did specifically analyze this issue were unable to demonstrate an association between number of sexual partners and risk of HIV infection, perhaps because the median number of partners was relatively low in these studies (1-4 partners in 5 years).(32,35,36)

Early research on selection advised that the choice of a partner was the most important determinant of transmission of HIV during a sexual encounter.(55) Current research has shifted emphasis from an explicit concern with absolute numbers of sexual partners to a model that situates an individual's selection of sexual partners in the context of the population seroprevalence, the likelihood that an individual has been tested for HIV, the likelihood that the test result was accurate, the likelihood of infection through insertive or receptive oral, vaginal, or anal sex, and the degree to which condom use reduces the probability of transmission during these acts. The model shows that individuals can reduce their risk by choosing a partner who has tested HIV negative, choosing a safer-sex act, using a condom, or some combination of these factors. For heterosexuals, whose population prevalence was modeled at 1%, choosing one risk-reduction behavior substantially reduced the absolute risk of HIV infection. However, for men who have sex with men (MSM), whose population prevalence was modeled at 10%, the choice of only one risk reduction behavior did not significantly lower the absolute risk of HIV infection.(56) As these models draw their assumptions from the epidemiology of HIV in developed-country settings, the applicability of their conclusions to high-prevalence heterosexual epidemics in the developing world seems limited. It is therefore important in high-prevalence settings to continue to encourage risk reduction behaviors that include both safer sex practices and HIV testing.

When both sexual partners are HIV positive, it is still reasonable to consider safer-sex practices to reduce the likelihood of infection from other sexually transmitted diseases, such as herpes, gonorrhea, chlamydia, syphilis, and hepatitis B and C viruses.

Case reports have confirmed that HIV-positive individuals can acquire different strains of HIV through sexual exposure.(57,58) Acquisition of a new strain of HIV in an individual who is already HIV-infected is known as superinfection. There is not yet a clear understanding of the probability of superinfection at the individual or population level, nor do we fully understand its impact on the long-term health of HIV-infected individuals. Superinfection may cause acute viral syndrome, and transmission of drug-resistant strains may reduce options for future ART,(59,60) suggesting a role for continued vigilance and safer-sex decision making by HIV-infected individuals even when both partners are infected.(56)

Heterosexual intercourse is presumed to be the most common mode of HIV infection worldwide. Studies of male-to-female and female-to-male transmission provide strong epidemiologic evidence that heterosexual transmission of HIV does occur via penile-vaginal intercourse.(31-41) Vaginal sex during menstruation may increase the risk of transmission from an infected female to an uninfected male,(40) but probably does not increase the risk of transmission from an infected male to an uninfected female.(43,55,56)

The efficiency of heterosexual transmission of HIV and per-act risk of infection are the subjects of debate in the epidemiologic literature. Early epidemiologic studies on heterosexual transmission in Western countries established that male-to-female transmission in the vagina was significantly more likely than female-to-male transmission from the vagina,(39,40,43,61,62) with estimates in three studies ranging from 1.9,(40) 2.3,(61) and 8.0 (62) times greater efficiency of male-to-female transmission. Per-act infectivity in two studies (62,63) was found to be low: 0.0005 and 0.0009 for male-to-female transmission, and 0.0003 and 0.0001 for female-to-male transmission. However, studies conducted in developing countries have estimated that per-act transmission probabilities are greater by a factor of 10 (44,64) for both male-to-female and female-to-male transmission.(65)

Although the greater efficiency of male-to-female versus female-to-male transmission has also been observed in developing countries, a systematic review of the literature found a greatly enhanced efficiency of female-to-male transmission in the high-prevalence epidemics of Asia and sub-Saharan Africa. The ratio of male-to-female summary mean transmission rates in the developing world compared to the rate in Western countries was 2.9, whereas for female-to-male transmission this ratio was 341. Women in some developing countries may be more infectious due to higher prevalence of sexually transmitted infections (STIs) and untreated HIV disease, although the authors state that evidence for the relative importance of these factors is unclear. The greater susceptibility of men in developing countries is also difficult explain, and may include a low prevalence of male circumcision, poor genital hygiene, a high prevalence of genital ulcer disease, and a high prevalence of unprotected sex with women having a high probability of being HIV infected.(65)

Strong evidence exists that being the receptive partner in unprotected penile-anal intercourse is associated with a high risk of HIV infection. Transmission of HIV to the receptive partner probably occurs as a result of the deposition of HIV-infected semen on traumatized rectal mucosa. More recently, studies have suggested that exposure to infected pre-ejaculate through anal intercourse may also carry a high risk of transmission.(66) Unprotected receptive anal intercourse (URAI) has been consistently described as an independent risk factor for HIV infection among MSM.(18-28) One recent study estimated the per-act risk of HIV infection from URAI with a partner who is HIV-positive at 0.82% (82 in 10,000) and with a partner of unknown serostatus at 0.27% (27 in 10,000).(67)

Several investigators found that receptive penile-anal sex is also a risk factor for male-to-female transmission.(32,35,37,38,40,43) Others failed to find this association among heterosexual couples.(33,34,36,41) Of the latter studies, however, three had small sample sizes, which may have made a relationship between anal sex and HIV infection impossible to detect.(33,34,36) It is probable that unprotected anal sex between serodiscordant heterosexual partners carries a similar per-act risk as it would between MSM, with greater risk incurred by the receptive female partner.

Whether being the inserting partner in unprotected penile-anal sex is an independent risk factor for HIV infection is not well understood. Most early studies did not demonstrate a statistically significant association between this practice and HIV infection among MSM.(18-21,23,25,26,28) This was not taken as evidence that the behavior was free of risk.(27) One recent study has estimated the per-act risk of unprotected insertive anal sex with an HIV-positive or unknown status partner at 0.06% (6 in 10,000).(67) This risk, although 4-14 times less than that estimated for URAI, remains considerable. The lack of more complete information on the risk of unprotected insertive anal sex reflects the research community's attention to the riskier activity URAI, rather than any consensus that unprotected anal sex has been determined to be of low risk to the insertive partner.

Studies of transmission among MSM have revealed that rectal douching increases the risk of HIV infection.(20,21,23,27) A similar association between fisting (penetration of the anus with the hand) and HIV infection was observed in some studies,(18,19,27) but not others.(21) One presumptive mechanism for transmission via these practices is that they disrupt the mucosal barrier of the rectum and thus facilitate entry of HIV into the bloodstream during subsequent exposure to infected body fluids. In a large multicenter cohort study of MSM, the investigators devised a composite variable called "rectal trauma," composed of enema usage, receptive fisting, report of blood around the rectum, and evidence of scarring, fissure, or fistula on examination.(24) They found that higher rectal trauma scores correlated with increased risk of HIV infection.

Oral-penile contact (fellatio) is not an efficient route of HIV infection. Estimating precise per-act risk is difficult because so few people practice oral sex to the exclusion of other, higher-risk sexual activities. Nonetheless, the risk of infection from oral sex is believed to be extremely low. Early male-to-male transmission studies consistently failed to demonstrate an increased risk of HIV infection associated with the practice of oral-penile sex.(17-24,25-27) A more recent study of MSM confirmed earlier findings, and further estimated that on a population level, the risk of HIV infection among MSM that is attributable to oral sex is extremely low.(68) Most studies of male-to-female and female-to-male transmission also failed to show any increased risk of HIV infection associated with oral-penile sex.(35,36,38,40) A cohort study among heterosexual serodiscordant couples at an STI clinic in Spain found no seroconversions attributable to oral sex, supporting the conclusion that HIV transmission via oral-penile sex between heterosexuals was extremely low.(69)

Oral-penile contact is not completely risk free, however.(68-70) A study of per-contact risk of infection to the receptive partner found that the probability of infection was 0.06% with a known HIV-positive partner and 0.04% with partners of unknown status. Although these are low probabilities, the authors suggest that oral-penile sex may play a larger role in the epidemic among MSM as more men adopt these behaviors as risk reduction measures.(67) Several case reports have implicated oral-penile contact as a source of male-to-male transmission.(71-73) The most convincing of these reports described a homosexual man who seroconverted despite having had only oral-genital contacts (and no anal-genital contacts) for at least 5 years preceding the estimated date of seroconversion.(73) In one study of heterosexual transmission, repeated oral sex was associated with transmission of HIV from men with AIDS to their spouses, although competing risks also showed significant associations in this study.(31) Because so few people practice oral-penile sex to the exclusion of other sexual practices, it is very difficult to recruit and retain subjects for epidemiologic studies of the HIV risk associated with this practice. Only one study was able to do this (68); another examined monogamous serodiscordant couples whose only unprotected sexual activity was oral sex.(69) No serocoversions were observed in either study. Despite the case reports, the epidemiologic evidence suggests that unprotected oral-penile sex is a low-risk activity.

Oral-genital sex, both oral-penile and oral-vaginal, can transmit STIs other than HIV with varying degrees of efficiency. Receptive oral-penile sex carries the risk of pharyngeal gonorrheal infection for both men and women, and insertive oral-penile sex, although carrying only extremely low, hypothetical risk of HIV infection to the insertive partner, carries a demonstrable risk of urethral gonorrheal infection. Other risks of receptive oral-genital sex include small probabilities of human papillomavirus and hepatitis C transmission. Insertive oral-penile sex is an efficient route for the transmission of herpes simplex virus (HSV).(70) The damage that many STIs cause to mucosa can conceivably increase the likelihood of transmission of HIV through oral sex, although this risk has not been quantified.

The risk of HIV transmission through oral-vaginal sex (cunnilingus) has received less attention than oral-penile sex. There have been case reports of female-to-male (74) and female-to-female (52) transmission of HIV infection via oral-vaginal sex. One study found an association between oral-vaginal sex and female-to-male transmission of HIV, although competing risks also showed significant associations in this study.(31) As with oral-penile sex, conducting an epidemiologic study that can examine oral-vaginal sex in the absence of competing HIV risk behaviors is difficult, and no such studies have been reported. However, all studies that have controlled for competing risk behaviors (35,36,38,40,69,70) have concluded that oral-vaginal sex is extremely low risk.

Although oral-anal contact is not an independent risk factor for HIV infection based on data from male-to-male transmission studies,(18-20,22,23,25-28) it may be a marker for other high-risk sexual practices. Univariate analysis showed an increased risk of HIV infection associated with oral-anal sex. This association was no longer statistically significant once the authors controlled for other high-risk behaviors.(19,22) Oral-anal sex has been shown to be a route of transmission for hepatitis A and B, and parasitic infections such as giardiasis and amebiasis.(70)

On the basis of the evidence just summarized, the following subjects should be incorporated into education and counseling intended to reduce sexual transmission of HIV.

Decisions About Sexual Activity

Because sexual contact is the major transmission route for HIV infection, eliminating sexual contact eliminates risk of transmission by this route. Abstinence, however, may be neither desirable nor practicable for many people. Nonetheless, it is an important option to consider, as some persons may feel that at least limited periods of abstinence may be the best choice under certain circumstances.

Decisions About Partner Selection

Sexual contact with many persons increases the probability of coming in contact with an HIV-infected partner. Thus, one risk-reducing strategy to consider is a reduction in the number of sexual partners, but this in no way reduces the risk of infection by sexual contact with even a single partner who is HIV positive. Because risk of HIV infection derives only from exposure to HIV-infected partners, avoiding sexual exposure with partners known or likely to be HIV infected would be an appropriate risk-reduction strategy for many people, but in many cases it is not possible to tell whether or not a given partner is HIV positive. One reasonable approach is to choose a partner who is at low risk of being HIV infected and then practice safer-sex techniques with that partner.

Decisions About Specific Sexual Practices

Evidence shows that some sexual practices are associated with a greater risk of HIV transmission than others. Proper use of barrier methods can reduce the risk of transmission associated with many of these practices. Thus, decision making about safer sex involves choices about specific sexual practices in addition to choices about partner selection. Based on the scientific evidence discussed in this chapter, Table 2 classifies sexual practices by their level of risk for HIV transmission.

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