Vaginal sex and the risk of HIV transmission

If the HIV-positive partner is taking antiretroviral treatment and has a fully suppressed viral load (‘undetectable’), the risk of HIV transmission through condomless vaginal intercourse is zero.

The PARTNER study recruited 548 heterosexual couples where one partner had HIV and fully suppressed viral load on antiretroviral treatment. During a median follow-up period of 1.3 years, the couples reported over 36,000 vaginal sex acts without condoms. No HIV transmissions occurred. The investigators concluded that the risk of HIV transmission through vaginal intercourse in these circumstances was effectively zero (Rodger).

When HIV is not suppressed by antiretroviral treatment, vaginal intercourse without a condom is a highly efficient route of HIV transmission because high concentrations of HIV can occur in semen and vaginal fluids, and because the genital tissues are very susceptible to infection. HIV can pass through the cells of the vaginal lining (epithelium) by migrating through specific cells and/or by passing through non-intact tissue. This allows the virus to reach the inner vaginal lining, which is rich in immune cells through which it can establish systemic infection.

Cells located beneath the surface of the cervix are particularly vulnerable to HIV infection, especially during adolescence and during a woman's first pregnancy, or due to infection with human papillomavirus and chlamydia.

A meta-analysis of studies of heterosexual HIV transmission found that, in high-income countries prior to the introduction of combination therapy, the risk per sexual act was 0.04% if the female partner was HIV positive and the male partner was HIV negative. The risk was 0.08% when the male partner was HIV positive and the female partner HIV negative. However, these rates were considerably higher when the source partner was in either the very early or the late stage of HIV infection, when one partner had a sexually transmitted infection that causes genital sores, and also in studies done in lower-income countries (Boily).

A woman is usually at greater risk of HIV infection from an HIV-positive man than vice versa. This may be due to several factors. Compared with the penis, the amounts of tissue cells susceptible to infection and/or damage are likely higher within the vagina. A woman may often take large quantities of semen into her vagina, which quickly comes into contact with the more vulnerable tissue of the cervix and may remain there for a period of time.

While women are at greater risk of infection from an HIV-positive male partner, condomless vaginal intercourse is also high risk for men, because damaged penile tissue and the mucous membranes in the urethra and on the head of the penis – particularly underneath the foreskin – form a point of infection.

Many other factors affect the level of risk associated with vaginal intercourse, including recent infection, sexually transmitted infections and male circumcision.

Recent infection

The first few weeks or months after HIV has entered a person’s body, their viral load is usually extremely high and they are very infectious.

Viral load is the term used to describe the amount of HIV circulating in the body. As viral load rises, so does infectiousness. On the other hand, when viral load is so low as to be undetectable, there is no risk at all of HIV transmission.

For example, a study of heterosexual couples in Rakai, Uganda, where one partner was HIV positive and the other HIV negative at the start of the study, showed that the likelihood of HIV transmission is highest in the first two and a half months following initial infection with HIV, and that this correlated with higher viral load levels in early HIV infection. The researchers estimated that relative to chronic infection, infectiousness during primary infection was enhanced 26-fold (Hollingsworth).

As people are usually unaware of their infection at this stage, they are not taking treatment and may inadvertently expose sexual partners to HIV. People who have HIV without realising it are much more likely to be involved in HIV transmission than people who know they have HIV, as the latter can receive treatment.

Sexually transmitted infections

Most sexually transmitted infections, especially those which cause ulceration, including herpes simplex 2 (HSV-2), syphilis, gonorrhoea, and chlamydia, increase HIV-negative partners’ risk of acquiring HIV during vaginal intercourse. HIV-negative people with recurrent STIs may be at increased ongoing risk of HIV infection.

In people living with HIV who are not taking HIV treatment, STIs also lead to increased genital shedding of HIV, which increases the risk of transmitting HIV to others. Nonetheless, STIs do not increase the risk of HIV transmission from people who are taking effective HIV treatment and have an undetectable viral load. In the PARTNER study, there was not a single HIV transmission even though many study participants had STIs.

There are two main reasons for the effect of STIs on HIV transmission. Firstly, many (although not all) STIs can cause ulcers, sores or lesions. They provide a direct physical route of entry for HIV in an uninfected person. Secondly, immune cells that are, themselves, prone to HIV infection – such as activated T-cells and dendritic cells – are prone to be present in greater numbers at the site of an infection.

The strongest evidence is for herpes simplex virus type 2 (HSV-2). A meta-analysis found that having HSV-2 was associated with an increased risk of acquiring HIV both in the general population (an increase of 270%) and in higher risk groups such as sex workers and men who have sex with men (170%). Having a recent HSV-2 infection was associated with an almost five-fold (470%) increased risk of acquiring HIV, probably because genital ulceration, viral shedding and inflammation in the genital tract are most severe in new HSV-2 infections and tend to decrease over time (Looker).

Gonorrhoea, chlamydia and trichomoniasis have been shown to increase risk of HIV infection in women (Laga). Trichomonas vaginalis increases the risk of HIV acquisition for women (Masha).

Human papillomavirus, the cause of genital warts, is associated with an increased risk of HIV infection in women regardless of whether it is an HPV type that causes genital warts or a type associated with cervical cancer (Houlihan). The presence of human papillomavirus in cells in the penis also increases the risk of acquisition in men (Rositch).

Male circumcision

Men are less likely to acquire HIV through vaginal intercourse if they are circumcised. There is strong biological and epidemiological evidence for this.

Circumcision is believed to reduce the risk of male infection because it removes the vulnerable tissue inside the foreskin, which contains Langerhans cells (a type of cell particularly vulnerable to HIV infection). The area under the foreskin is also vulnerable to trauma, and is more likely to become abraded if sufficient lubrication is not present. Also, uncircumcised men may be more vulnerable to sexually transmitted infections (STIs), because the area under the foreskin can retain bacteria acquired during sex, thus increasing the chance that an infection will become established.

Three randomised controlled trials of circumcision demonstrated that circumcision lowers HIV-negative men’s risk of acquiring HIV by between 51 and 60%. They also showed benefits in terms of lowering rates of sexually transmitted infections. The studies were conducted in South Africa (Auvert), Kenya (Bailey) and Uganda (Gray).

The World Health Organization recommends that circumcision programmes should be an integral part of HIV prevention programmes in countries with generalised HIV epidemics. In the United States, the Centers for Disease Control and Prevention (CDC) recommends that healthcare providers can inform their patients that medical male circumcision “male circumcision reduces, but does not eliminate, the risk of acquiring HIV” by men during vaginal sex.

Male circumcision does not reduce the risk of HIV transmission from men to female partners.

Schistosomiasis

Schistosomiasis (also known as bilharzia) is a widespread infection in sub-Saharan Africa and other tropical countries. Schistosomiasis is caused by a parasitic worm that lives in fresh water and is acquired by bathing in infested water. The infection can cause a localised immune response and genital lesions, increasing the risk of HIV transmission and acquisition.

In a study of over 1000 HIV-serodiscordant couples in Zambia (Wall), women who had schistosomiasis had an 40% increased risk of acquiring HIV. In addition, when an HIV-positive man or woman had schistosomiasis, there was a greater risk of HIV transmission to their sexual partner.

Bacterial vaginosis

Bacterial vaginosis is a type of vaginal inflammation caused by the overgrowth of bacteria naturally found in the vagina, which upsets the natural balance. Signs and symptoms may include a discharge, an odour, itching and burning during urination.

It appears that bacterial vaginosis is associated with an increased risk of acquiring HIV. A meta-analysis of four prospective studies conducted in sub-Saharan Africa found a 61% increased risk of HIV acquisition in women (Atashhili). In a Kenyan study, bacterial vaginosis and HSV-2 infection were the two strongest risk factors measured for HIV acquisition over a 20-year period (Masese).

Practices such as douching, washing and drying the vagina may undermine the body’s innate defences and make bacterial vaginosis more common.

Withdrawal before ejaculation

The chances of infection may be lessened during condomless vaginal intercourse if ejaculation does not take place. An early study found that after 20 months, none of the heterosexual couples who had consistently practised withdrawal experienced the seroconversion of the HIV-negative partner (De Vincenzi).

Vaginal dryness

Rougher sex and/or vaginal dryness may lead to vaginal or penile abrasions, which may increase the chances of infection.

Reduction of vaginal lubrication becomes more common with age, possibly increasing risk in post-menopausal women. Younger women in early puberty may also produce less vaginal and cervical secretions, perhaps increasing their vulnerability to HIV infection and contributing to the disproportionate prevalence of HIV amongst adolescent women (Holmberg).

How you can reduce the risk

Effective protective measures are:

• The HIV-positive partner taking effective HIV treatment and having an undetectable viral load.
• The HIV-negative partner taking pre-exposure prophylaxis (PrEP).
• Condoms and lubricant.
• As an emergency measure, post-exposure prophylaxis (PEP).