Review
Intravaginal practices, bacterial vaginosis, and women's susceptibility to HIV infection: epidemiological evidence and biological mechanisms

https://doi.org/10.1016/S1473-3099(05)70298-XGet rights and content

Summary

Intravaginal practices such as “dry sex” and douching have been suggested as a risk factor that may increase women's susceptibility to HIV infection. These behaviours appear common in different populations across sub-Saharan Africa, where practices include the use of antiseptic preparations, traditional medicines, or the insertion of fingers or cloths into the vagina. We systematically review the evidence for the association between women's intravaginal practices and HIV infection. Although a number of cross-sectional studies have shown that prevalent HIV infection is more common among women reporting intravaginal practices, the temporal nature of this association is unclear. Current evidence suggests that bacterial vaginosis, which is a likely risk factor for HIV infection, may be a mediator of the association between intravaginal practices and HIV. Although biologically plausible mechanisms exist, there is currently little epidemiological evidence suggesting that intravaginal practices increase women's susceptibility to HIV infection. Further research into factors that increase women's susceptibility to HIV will help to inform the design of vaginal microbicides and other HIV prevention interventions.

Introduction

As the HIV pandemic continues its expansion around the globe, women of reproductive age face persistent high risks of HIV infection. In sub-Saharan Africa, where an estimated 8% of all adults are infected with HIV, approximately 60% of all infections are among women,1 and in some parts of southern Africa as many of one-third of pregnant women attending antenatal clinics are infected with the virus.2

Women's risk of HIV infection continues despite the relatively low probability of male-to-female HIV transmission by vaginal intercourse under normal conditions.3, 4, 5, 6, 7, 8 Although biological exposures that facilitate transmission of HIV are widely thought to have an important role in the population spread of the disease, only a handful of cofactors have been conclusively identified to date. Most notable among these cofactors are sexually transmitted diseases, including ulcerative and non-ulcerative infections.9, 10, 11, 12, 13 A range of other factors have been postulated to enhance women's biological susceptibility to HIV, with mixed findings for intercourse during menses8 and the use of hormonal contraceptives.14, 15 A number of other factors that may be important in increasing the transmissibility of HIV, including the dynamics of acute HIV infection and lack of male circumcision, are under investigation.16, 17 Given the continued high incidence of HIV in many parts of the world, determining the circumstances that increase women's risk of HIV infection is important for focusing ongoing HIV prevention efforts.

Women's intravaginal practices have been linked anecdotally to increased susceptibility to HIV infection.18, 19, 20 Commonly referred to as “dry sex” practices, a broader concept of intravaginal practices has emerged in recent years that encompasses wiping, cleansing, douching, or the insertion of substances into the vagina.21 These behaviours have been documented in a range of settings, including the USA,22, 23 the Caribbean,24 southeast Asia,25 and sub-Saharan Africa.26, 27, 28, 29 In Africa, there is evidence to suggest that intravaginal practices may be common in many settings where HIV is most prevalent. Although many behaviours associated with increased risk of HIV infection (eg, non-use of condoms) have proven difficult to modify,30 intravaginal practices may be more amenable to intervention.21 If intravaginal practices do truly increase women's risk of HIV, these practices may be an important avenue for future prevention efforts. In addition to the possible role of reduced intravaginal practices as an intervention for HIV prevention, better understandings of the mechanisms by which intravaginal products may influence women's susceptibility to HIV are relevant for other forms of HIV prevention. There is particular interest in how intravaginal practices may affect cervicovaginal flora or epithelial tissues, or both, and evidence in this area may have important implications for the development of vaginal microbicides for HIV prevention.31, 32

Here we systematically review the evidence for the association between women's intravaginal practices and HIV infection. To help understand the potential for intravaginal practices to function as a cofactor in HIV transmission, we also review evidence for the biological mechanisms that are commonly postulated to be involved in the association, including alterations in vaginal flora characteristic of bacterial vaginosis and epithelial disruptions to the cervix or vagina.

Section snippets

Search strategy and selection criteria

Materials for this review were identified though searches of Medline, Current Contents, and Popline, as well as abstracts from International AIDS Conferences between 1996 and 2004. Database search terms included “intravaginal practices”, “douche” or “douching”, “vaginal cleaning”, “dry sex”, “sexually transmitted diseases”, and “HIV”. Additional sources were identified through references from relevant articles as well as contacts with leading investigators in the field. Articles were included

Results

From 289 articles identified during the literature search, 93 articles were identified for inclusion in the review because they presented primary data on women's intravaginal practices and/or the putative mechanisms that may be involved in increasing the risk of HIV or other sexually transmitted infections. Of these articles, 25 studies presented data on the prevalence of intravaginal practices; the key features of these studies are summarised in the table. 12 of the 25 studies were included in

Discussion

Existing research into the mechanisms of sexual transmission of HIV to women has focused on different physiological and immunological vulnerabilities of the female reproductive tract, and factors that may enhance susceptibility to infection. Although a range of pathways have been suggested, there is still no definitive understanding of how HIV infects the female reproductive tract, and as a result, vaginal microbicides and other new HIV prevention technologies have targeted a number of

Search strategy and selection criteria

These are described in the text.

References (100)

  • A Helfgott et al.

    Vaginal infections in human immunodeficiency virus-infected women

    Am J Obstet Gynecol

    (2000)
  • DJ Jamieson et al.

    Longitudinal analysis of bacterial vaginosis: findings from the HIV epidemiology research study

    Obstet Gynecol

    (2001)
  • MJ Wawer et al.

    Control of sexually transmitted diseases for AIDS prevention in Uganda: a randomised community trial

    Lancet

    (1999)
  • CW Critchlow et al.

    Determinants of cervical ectopia and of cervicitis: age, oral contraception, specific cervical infection, smoking, and douching

    Am J Obstet Gynecol

    (1995)
  • HR Harrison et al.

    Cervical Chlamydia trachomatis infection in university women: relationship to history, contraception, ectopy, and cervicitis

    Am J Obstet Gynecol

    (1985)
  • WC Louv et al.

    Oral contraceptive use and the risk of chlamydial and gonococcal infections

    Am J Obstet Gynecol

    (1989)
  • G Walraven et al.

    The burden of reproductive-organ disease in rural women in The Gambia, West Africa

    Lancet

    (2001)
  • M Miller et al.

    Networks, resources and risk among women who use drugs

    Soc Sci Med

    (2001)
  • Report on the global AIDS epidemic, 2004

    (2004)
  • Report on the national HIV and syphilis antenatal seroprevalence survey in South Africa, 2003

    (2004)
  • RA Royce et al.

    Sexual transmission of HIV

    N Engl J Med

    (1997)
  • TD Mastro et al.

    HIV type 1 transmission probabilities: estimates from epidemiological studies

    AIDS Res Hum Retroviruses

    (1998)
  • NS Padian et al.

    The effect of number of exposures on the risk of heterosexual HIV transmission

    J Infect Dis

    (1990)
  • A Nicolosi et al.

    The efficiency of male-to-female and female-to-male sexual transmission of the human immunodeficiency virus: a study of 730 stable couples

    Epidemiology

    (1994)
  • I De Vincenzi

    A longitudinal study of human immunodeficiency virus transmission by heterosexual partners

    N Engl J Med

    (1994)
  • M Laga et al.

    Non-ulcerative sexually transmitted diseases as risk factors for HIV-1 transmission in women: results from a cohort study

    AIDS

    (1993)
  • RH Gray et al.

    Relative risks and population attributable fraction of incident HIV associated with symptoms of sexually transmitted diseases and treatable symptomatic sexually transmitted diseases in Rakai District, Uganda

    AIDS

    (1999)
  • DT Fleming et al.

    From epidemiological synergy to public health policy and practice: the contribution of other sexually transmitted diseases to sexual transmission of HIV infection

    Sex Transm Infect

    (1999)
  • H Martin et al.

    Hormonal contraception, sexually transmitted diseases, and risk of heterosexual transmission of human immunodeficiency virus type 1

    J Infect Dis

    (1998)
  • CS Morrison et al.

    Hormonal contraceptive use, cervical ectopy, and the acquisition of cervical infections

    Sex Transm Dis

    (2004)
  • MJ Wawer et al.

    Rates of HIV-1 transmission per coital act, by stage of HIV-1 infection, in Rakai, Uganda

    J Infect Dis

    (2005)
  • R Gray et al.

    Male circumcision and the risk of sexually transmitted infections and HIV in Rakai, Uganda

    AIDS

    (2004)
  • JE Brown et al.

    Traditional intravaginal practices and the heterosexual transmission of disease: a review

    Sex Transm Dis

    (2000)
  • Douching is indirectly linked to HIV infection in female sex workers

    International Family Planning Perspectives

    (2001)
  • JH van de Wijgert et al.

    Intravaginal practices in Zimbabwe: which women engage in them and why?

    Culture, Health & Sexuality

    (2001)
  • BA Koblin et al.

    Douching practices among women at high risk of HIV infection in the United States: implications for microbicide testing and use

    Sex Transm Dis

    (2002)
  • B Foxman et al.

    Interrelationships among douching practices, risky sexual practices, and history of self-reported sexually transmitted diseases in an urban population

    Sex Transm Dis

    (1998)
  • DT Halperin

    Dry sex practices and HIV infection in the Dominican Republic and Haiti

    Sex Transm Infect

    (1999)
  • ME Beksinska et al.

    The practice and prevalence of dry sex among men and women in South Africa: a risk factor for sexually transmitted infections?

    Sex Transm Infect

    (1999)
  • GA Dallabetta et al.

    Traditional vaginal agents: use and association with HIV infection in Malawian women

    AIDS

    (1995)
  • NS Morar et al.

    Vaginal insertion and douching practices among sex workers at truck stops in KwaZulu-Natal

    S Afr Med J

    (1998)
  • A Harrison et al.

    Prevention of HIV/AIDS in South Africa: a review of behaviour change interventions, evidence and options for the future

    S Afr J Sci

    (2000)
  • JH van de Wijgert et al.

    Effect of intravaginal practices on the vaginal and cervical mucosa of Zimbabwean women

    J Acquir Immune Defic Syndr

    (2000)
  • JH van de Wijgert et al.

    Intravaginal practices, vaginal flora disturbances, and acquisition of sexually transmitted diseases in Zimbabwean women

    J Infect Dis

    (2000)
  • QA Karim et al.

    Reducing the risk of HIV infection among South African sex workers: socioeconomic and gender barriers

    Am J Public Health

    (1995)
  • JM Mann et al.

    HIV infection and associated risk factors in female prostitutes in Kinshasa, Zaire

    AIDS

    (1988)
  • T Palanuvej et al.

    Lack of demonstrable association between use of cervicovaginal mucosal irritant and HIV infection in female commercial sex workers in Thailand

    AIDS

    (1998)
  • T Siraprapasiri et al.

    Risk factors for HIV among prostitutes in Chiangmai, Thailand

    AIDS

    (1991)
  • PH Kilmarx et al.

    HIV-1 seroconversion in a prospective study of female sex workers in northern Thailand: continued high incidence among brothel-based women

    AIDS

    (1998)
  • AO Runganga et al.

    The vaginal use of herbs/substances: an HIV transmission facilitatory factor?

    AIDS Care

    (1995)
  • Cited by (166)

    • Perceived stress and incident sexually transmitted infections in a prospective cohort

      2019, Annals of Epidemiology
      Citation Excerpt :

      The vaginal microbiome offers protection in part through the influential action of Lactobacillus spp. Species of vaginal Lactobacillus spp. can provide broad-spectrum protection through production of copious amounts of lactic acid [36], bacteriocins [29,32,37–39], antagonistic bacteriocin-like substances [40], and biosurfactants [41] and through their ability to adhere to mucus, forming a physical barrier against incoming pathogens [42] and disrupting biofilms [43]. Considering behavioral pathways, high perceived stress has been associated with a 2.4-fold greater odds of reporting problems using condoms, and depression was associated with 50% lower odds of using condoms consistently [44].

    View all citing articles on Scopus
    View full text