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Sexual Risk Factors and Bacterial Vaginosis: A Systematic Review and Meta-Analysis

  1. Katherine A. Fethers1,2,
  2. Christopher K. Fairley1,2,
  3. Jane S. Hocking2,
  4. Lyle C. Gurrin2, and
  5. Catriona S. Bradshaw1,3
  1. 1Melbourne Sexual Health Centre, The Alfred Hospital, Carlton
  2. 2School of Population Health, University of Melbourne, Melbourne, Victoria, Australia
  3. 3Department of Epidemiology and Preventive Medicine, Monash University, Melbourne, Victoria, Australia
  1. Reprints or correspondence: Dr. Katherine Fethers, Melbourne Sexual Health Centre, 580 Swanston St., Carlton, 3053, Victoria, Australia (kfethers{at}mshc.org.au), or Dr. Catriona Bradshaw, Melbourne Sexual Health Centre, 580 Swanston St., Carlton, 3053, Victoria, Australia (cbradshaw{at}mshc.org.au).
 
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Abstract

We performed a systematic review and meta-analysis of the association between sexual risk factors and bacterial vaginosis (BV). Forty-three studies reported new or multiple sexual partners and condom use relative to prevalent, incident, or recurrent BV. The summary estimate of the relative risk for the association between BV new or multiple male partners was 1.6 (95% confidence interval, 1.5–1.8), between BV and any female partners was 2.0 (95% confidence interval, 1.7–2.3), and between BV and condom use was 0.8 (95% confidence interval, 0.8–0.9). This review is the first to summarize available observational data for BV. It shows that BV is significantly associated with sexual contact with new and multiple male and female partners and that decreasing the number of unprotected sexual encounters may reduce incident and recurrent infection. Investigation of sexual transmission of BV is limited by the absence of a clear microbiological etiology; however, we have shown that the epidemiological profile of BV is similar to that of established sexually transmitted infections.

Bacterial vaginosis (BV) is one of the most common genital infections among women of reproductive age [1, 2], yet its precise etiology and whether it is sexually transmitted are unknown. BV is characterized by a disturbance of normal vaginal flora, with a loss of H202- producing Lactobacillus species and an increase in gram-variable coccobacilli, anerobic organisms, and genital mycoplasmas. Importantly, BV is associated with serious sequelae, such as chorioamnionitis, spontaneous abortion, preterm delivery, low birth weight, postpartum and postabortion endometritis [3–6], and increased susceptibility to HIV infection and other sexually transmitted infections (STIs) [7–9]. Current treatments result in unacceptably high recurrence rates [10, 11].

Over the past 30 years, there has been considerable debate over whether BV is a sexually transmitted condition or is simply an ecological imbalance of vaginal microflora that can arise as a consequence of a range of activities or factors. If we are to make any improvement in the efficacy of current therapies and to have an impact on the adverse sequelae associated with BV, we need to establish whether the high rates of recurrence after treatment with current therapies represent inadequate treatment and disease persistence or reinfection from sexual partners.

In the absence of a clear etiological agent, epidemiological studies can assist in understanding the contribution of sexual activity to the development of BV and to recurrence after therapy. Risk factors associated with established STIs include a recent change of sexual partner, an increased number of sexual partners, young age at coitarche, a previous history of STIs, inconsistent condom use, barriers to accessing health services, and young age. We undertook a systematic review and meta-analysis of the published literature that investigated factors associated with BV, with the aim of evaluating the epidemiological evidence that may support or refute the hypothesis that BV is sexually transmitted.

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Methods

A Medline search of the published literature was conducted that covered the period from 1992 (when Medline introduced the search heading “bacterial vaginosis”) through November 2007. Relevant articles published before 1992 that were cited in identified articles were also included.

Medline subject search terms included “bacterial vaginosis” and “vaginosis, bacterial,” and Medline qualifying terms included “epidemiology,” “transmission,” and “prevention/control.” The search headings “condoms,” “sex partners,” “incidence,” and “recurrence” were also used in combination with the topic search word “bacterial vaginosis.”

This search resulted in the retrieval of 1130 articles. Studies were reviewed for relevance to the sexual risk factors associated with BV. Studies were included if they were English language, the diagnosis of BV was made using the Amsel method or a Gram stain method (e.g., Nugent method), had at least 50 participants, and measured at least 1 of the following sexual risk factors: number of past sexual partners, recent change in or new sexual partner, and reported condom use. All study designs were included. Studies involving pregnant women and studies for which relative measures were not available (or raw data were not provided, if relative measures were not provided) were excluded. Cited references were also assessed for inclusion.

Available evidence was then prepared in figure form to summarize the key study findings. table 1 outlines the potential generalizability of the findings and the important confounding factors that have been controlled for in multivariable analyses (i.e., douching, smoking, frequency of sex, race, and age). For the purpose of this review, we selected the following main epidemiological associations with sexual risk: number of recent and past sexual partners, recent change in sexual partner (often reported as new sexual partner), and condom use.

The relative measures displayed in figures 1–3 were selected using the following hierarchies: adjusted measures were used when available, and crude ORs were included in their absence. When multiple measures of sexual risk were provided, more-recent time intervals were selected (e.g., data on the number of partners within the previous 12 months was preferred over data on lifetime number of sexual partners), and “new sexual partner” was used, if available, in preference to “multiple sex partners.” For treatment trials in which BV recurrence was the outcome, the additional risk factor of regular sexual partner was included, if reported, and was prioritized over new sexual partner. The reasoning behind this was that, in treatment trials, the probability that BV recurrence was due to a new partner was considered to be substantially less than the probability of “reinfection” from an existing partner.

Figure 1
Figure 1

Forest plot of the association between new or multiple male sexual partners and bacterial vaginosis. Effect size is given as relative risk or OR (see table 1) and 95% CIs (whiskers) The summary relative risk was 1.6 (95% CI, 1.5–1.8) and is indicated by the vertical dashed line.

A summary estimate was calculated for the association of each risk factor with BV. A fixed-effects meta-analysis was used to generate a pooled measure of association between the risk of BV and sexual risk. Heterogeneity between the individual measures of association that contributed to the analysis was assessed using a test statistic that has a Χ2 distribution under the null hypothesis that the underlying effect size at the population level is the same across all studies. Publication bias was assessed by visual inspection of funnel plots that plotted the log of the effect size on the horizontal axis against the corresponding SE on the vertical axis. OpenEpi software, version 2.2.1 [54], was used to recalculate ORs and 95% CIs, and Stata software, version 9 (StataCorp), was used in creating the figures and performing the meta-analysis. P<.05 was considered to be statistically significant.

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Results

Of the 1130 identified articles, 43 satisfied the inclusion criteria, as follows: 10 cohort incidence studies, 3 cohort treatment recurrence studies, 5 case-control studies, and 25 cross-sectional studies (table 1).

Association between BV and male sexual partners. Twenty-eight studies fulfilled the inclusion criteria and reported numbers of male sexual partners and/or a recent change of male sexual partner (figure 1). Eight of these studies were cohort studies, and each of these 8 studies found an association between incident BV and increasing number of male sexual partners and/or a recent change of male partner (relative risk [RR] range, 1.3–2.5) [12–21]. Two studies were cohort treatment studies; 1 of these studies found a strong association between recurrent BV and remaining with a regular sex partner (RR, 3.1; 95% CI, 1.6–6.3), whereas the other study reported data only on having a new sexual partner and found no association with BV [10, 23]. Five studies were case-control studies, and 4 of these studies found a strong association between BV and increasing number of male sexual partners and/or a recent change of male partner (OR range, 1.6–3.8) [24–28]. Thirteen studies were cross-sectional studies, and 10 of these studies found evidence of an association between BV and increasing number of male sexual partners and/or a recent change of male partner (OR range, 1.3–5.4) [31–53].

There was a positive association between a history of male sexual partners and the risk of BV, with an estimated relative risk for association of 1.6 (95% CI, 1.5–1.8). There was strong evidence against the null hypothesis of homogeneity of effect size of BV risk associated with a history of male sexual partners (P<.01).

Association between BV and female sexual partners. Twelve studies reported data on sex with female partners in relation to BV and fulfilled the inclusion criteria (figure 2). One study was a cohort treatment study and found that BV recurrence was more likely if a woman reported having a female sexual partner after treatment (RR, 3.6; 95% CI, 1.5–8.5) [10]. Two studies were case-control studies, and 1 of these studies found a strong association between prevalent BV and recent sex with a female partner (OR, 2.0; 95% CI, 1.3–3.3); the other study demonstrated a trend toward an association between BV and a history of female partners but did not reach statistical significance (OR, 2.0; 95% CI, 0.9–4.4) [24, 28]. Nine studies were cross-sectional studies, and 3 of these found a strong association between BV and having an increased number of female sexual partners (OR range, 2.2–3.5) [30–42]. The other 6 studies were larger cross-sectional studies, and although they did not report data on the number of female sexual partners, they estimated large effect sizes for the association between BV and a history of any female sexual partner (OR range, 1.7–5.9) [40, 52, 36–51].

Figure 2
Figure 2

Forest plot of the association between any female sexual partner and bacterial vaginosis. Effect size is given as relative risk or OR (see table 1) and 95% CIs (whiskers) The summary relative risk was 2.0 (95% CI, 1.7–2.3) and is indicated by the vertical dashed line.

The estimated relative risk of 2.0 (95% CI, 1.7–2.3) showed a positive association between a history of female sexual partners and risk of BV. There was no evidence against the null hypothesis of homogeneity in effect sizes across studies contributing data to the overall estimate of risk of BV associated with a history of female sexual partners (P=.18).

Association between BV and condom use. Twenty studies fulfilled the inclusion criteria and reported data on condom use (figure 3). Measurement of condom use varied considerably across the studies and is reported for each study in table 1. Eight cohort studies, including 3 treatment trials, were included, and 5 of these studies found evidence of a reduction in the risk of incident or recurrent BV associated with the use of condoms (RR range, 0.2–0.9) [10, 15, 18, 21, 23, 16–22]. Three studies were case-control studies, and 1 of these studies found a strong negative (i.e., risk-reducing) association between BV and the use of condoms (OR, 0.5; 95% CI, 0.3–0.7) [24, 26, 28]. Nine studies were cross-sectional studies, and 5 of these studies found evidence of a negative association between BV and the use of condoms (OR, 0.3–0.6) [31, 33, 34, 45, 49, 29–50].

Figure 3
Figure 3

Forest plot of the association between condom use and bacterial vaginosis. Effect size is given as relative risk or OR (see table 1) and 95% CIs (whiskers) The summary relative risk was 0.8 (95% CI, 0.8–0.9) and is indicated by the vertical dashed line.

The estimated relative risk of 0.8 (95% CI, 0.8–0.9) showed that condom use was protective against BV. There was evidence against the null hypothesis of homogeneity of effect size across studies contributing data to the overall estimate of risk of BV associated with condom use (P<.01).

Publication bias. Funnel plots showing the log of the effect size against the corresponding SE were constructed (figures 4–6). The plots for studies that report data on male and female sexual partners suggest that there is some publication bias against small studies that report smaller effect sizes. The funnel plot for studies that report data on condom use suggests that there is some publication bias against small studies that report positive associations.

Figure 4
Figure 4

Funnel plot to assess publication bias among studies examining the association between male sex partners and bacterial vaginosis.

Figure 5
Figure 5

Funnel plot to assess publication bias among studies examining the association between female sex partners and bacterial vaginosis.

Figure 6
Figure 6

Funnel plot to assess publication bias among studies examining the association between condom use and bacterial vaginosis.

Table 1
Table 1

Systematic review of characteristics of 43 studies of bacterial vaginosis (BV).

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Discussion

This systematic review and meta-analysis indicate that prevalent and incident BV is consistently associated with new or multiple male and female sexual partners and lack of condom use. Investigation of the sexual transmission of BV is limited by the absence of a clear microbiological etiology; however, we have shown that the epidemiological profile of BV is similar to that of established STIs. To our knowledge, this is the first systematic review and meta-analysis of the sexual risk factors associated with BV.

There are a number of factors that must be considered when interpreting these findings. There was evidence of heterogeneity of effect size across the studies, particularly for the exposures of male partners and condom use. This is to be expected because of the large variability in the studies, particularly with respect to study design, study population, and exposure definition. The measurements of the key exposure variables in this meta-analysis were not always consistent. The most pertinent example was the measurement of condom use, for which the definition of reported condom use (e.g., 100% condom use, consistent condom use) and time periods varied considerably across studies. Strong evidence against the null hypothesis of homogeneity suggests that there is a distribution of effect sizes across the target populations covered by the studies that contributed data to this analysis. The pooled estimate of the effect sizes, then, represents the mean of the varying effect size across all populations. The funnel plots also demonstrated asymmetry of the scatter at the top of the vertical axis, which suggests that studies with small estimated effect sizes and large SEs (as the result of a small sample size) were withheld from publication. We acknowledge these inherent difficulties, but we would argue that this is unavoidable with a meta-analysis of observational studies and that the combined data consistently indicates that BV is associated with an overall increase in sexual risk.

Exposure to increased numbers of male sex partners or having a recent change of male partner increased the risk of developing BV 1.6-fold in this meta-analysis. Unfortunately, in the absence of a clear etiological agent or agents, it has proven to be difficult to investigate male carriage of BV; however, studies have isolated BV-associated organisms from the male genital tract [55–57]. Lack of male circumcision has been associated with a number of STIs, including genital ulcer disease [58, 59] and HIV infection [60]. It is, therefore, biologically plausible that, if BV is transmitted by males, the foreskin could facilitate survival of BV organisms and render an uncircumcized male a more efficient or more prolonged transmitter of infection. Importantly, recent data do suggest that male circumcision status may affect female BV infection rates. Cherpes et al. [14] found that female partners of uncircumcized men were more likely to have BV (RR, 1.9; 95% CI, 1.0–3.5), and observational data from Rakai in Uganda similarly suggest that male circumcision may offer protection for women against BV (RR, 0.9; range, 0.8–0.9) [61]. Further support for sexual transmission of BV comes from a treatment trial by Bradshaw et al. [10], included in this review, that found BV recurrence was 3 times more common among women who remained with their regular sexual partner after treatment and was significantly less likely among women who changed sexual partners. A recent study by Schwebke et al. [21] also found that male sexual contacts of women with BV reported a significantly higher number of female partners than did the male partners of women without BV, indicating that perhaps men with higher numbers of partners are more likely to be exposed to and possibly transmit BV.

A strong and consistent association between BV and a history of female sexual partners was apparent in this meta-analysis; report of a female sexual partner conferred a 2-fold risk of BV infection. In the studies that quantified partners, there was a trend towards increasing risk of BV with a higher number of female sexual partners. Although this finding is in contrast with the epidemiology of bacterial STIs, such as chlamydia and gonorrhea, sexual contact between women has been associated with transmission of human papilloma virus, herpes simplex virus, trichomoniasis, and other STIs [62–66]. Evidence of female-to-female transmission of BV emerged in the 1950s, when asymptomatic volunteers were directly inoculated with the vaginal secretions of women with BV, and BV was established in the recipients [67]. It is possible that the exchange of vaginal secretions during sexual contact and a potentially longer duration of infectiousness of BV in woman, compared with in men, confer a higher level of risk of BV for women who have sex with women. Consistent with this, studies of monogamous female couples demonstrate extremely high concordance for BV (73%–95%) [41, 68]. There is a need for female partner treatment trials to assess the effect on BV recurrence, but in the interim, on the basis of the body of published literature, it may be appropriate to offer partner testing and treatment for women with BV who have sex with women.

Consistent use of condoms during intercourse should offer protection against an STI. However, the effectiveness of condoms has been difficult to establish for a number of STIs, particularly viral pathogens, such as herpes simplex virus and human papilloma virus. There are a number of inherent problems in assessing condom use that may systematically reduce the measured protection conferred by condoms in observational studies; these include the highly variable measurement of condom use across studies, incorrect usage, condom breakages, frequent overreporting of condom use, and the amalgamation of condoms with diaphragms in some studies that broadly report protection with “barrier methods.” Despite these inherent limitations, reported condom use was found to be protective against prevalent and incident BV in this review (RR, 0.8; 95% CI, 0.8–0.9). Importantly, this is comparable with the protective effect of condom use reported for chlamydia or gonorrhea when the infection status of the partner is unknown (OR, 0.8; 95% CI, 0.7–1.0) [69]. When a sexual partner is known to be infected with an STI, such as chlamydia or gonorrhea, condoms have been shown to confer a greater degree of protection (OR, 0.4; 95% CI, 0.2–1.0) [69, 70].

A body of epidemiological evidence does not support the hypothesis that BV is sexually transmitted. Five of 6 treatment trials failed to reduce recurrence of BV in women whose male partners were treated [71–76]. This has been considered to be strong evidence against sexual transmission of BV; however, there were methodological limitations in these trials, including the use of single-dose therapies, no measures of partner adherence, and a high rate of loss to follow-up in some studies. A further complicating factor is that, in the absence of a clear etiological agent or agents, it is possible that we are not currently using effective therapies and, therefore, are not able to demonstrate an effect from partner treatment.

BV was diagnosed in women who did not report a history of vaginal intercourse in 2 studies [53, 77]. Both, however, involved young women who were categorized on the basis of self-report of vaginal sex. Neither study collected information on nonpenetrative genital contact and orogenital or digital-genital practices. In addition, 1 of the studies found 8 cases of BV among 52 “virginal” adolescents, and although none of the cases were treated, only 1 case of BV persisted at 3 months. This very high rate of spontaneous clearance could raise concern regarding the validity of BV diagnosed in this study.

A final consideration in addressing possible sexual transmission of BV is whether the association between BV and increased number of sexual partners may arise as a consequence of microbial disruption due to more-frequent sexual activity, rather than representing sexual transmission of a pathogen. This has been considered by a number of investigators, and in our systematic review, 4 of 5 cohort studies, 2 of 2 case-control studies, and 2 of 4 cross-sectional studies found that the number of male sexual partners remained independently associated with BV once the frequency of sexual activity was controlled for by multivariable analysis.

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Conclusions

As the microbiological etiology of BV has not been determined, any progress in establishing how this infection is transmitted is greatly impeded. Until we have this direct evidence, we need to consider the data generated from analyses of observational studies. This review is, to our knowledge, the first to summarize the observational data; it is consistent with the hypothesis that BV is transmitted to a woman by sexual contact with either a man or woman, and it indicates that condom use may prevent transmission. Understanding the contribution of sexual risk factors to the development of BV is integral, not only to improving current management of this condition, but also to reducing the serious sequelae associated with BV, such as preterm delivery, and to developing strategies to reduce HIV transmission in populations in which there is a high prevalence of BV. These findings are of relevance to practicing clinicians in the field and may inform public health policy. Although these data cannot be interpreted as evidence that BV is an STI, the results of this meta-analysis suggest that reducing the number of sexual partners and reducing the number of unprotected sexual exposures decreases the risk of incident and recurrent BV.

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Acknowledgments

Financial support. K.A.F. is supported by The Royal Australasian College of Physicians Scholarship for Sexual Health Research. C.S.B., J.S.H., and L.C.G. are supported by the Australian National Health and Medical Research Council Fellowship program.

Potential conflicts of interest. All authors: no conflicts.

  • Received June 20, 2008.
  • Accepted August 12, 2008.
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References

  1. ↵
    1. Allsworth JE,
    2. Peipert JF
    . Prevalence of bacterial vaginosis: 2001–2004 national health and nutrition examination survey data. Obstet Gynecol 2007;109:114-20.
    CrossRefMedlineWeb of Science
  2. ↵
    1. Lamont RF,
    2. Morgan DJ,
    3. Wilden SD,
    4. Taylor-Robinson D
    . Prevalence of bacterial vaginosis in women attending one of three general practices for routine cervical cytology. Int J STD AIDS 2000;11:495-8.
    Abstract/FREE Full Text
  3. ↵
    1. Goldenberg RL,
    2. Andrews WW,
    3. Yuan AC,
    4. MacKay HT,
    5. St Louis ME
    . Sexually transmitted diseases and adverse outcomes of pregnancy. Clin Perinatol 1997;24:23-41.
    MedlineWeb of Science
    1. Gravett MG,
    2. Nelson HP,
    3. DeRouen T,
    4. Critchlow C,
    5. Eschenbach DA,
    6. Holmes KK
    . Independent associations of bacterial vaginosis and Chlamydia trachomatis infection with adverse pregnancy outcome. JAMA 1986;256:1899-903.
    Abstract/FREE Full Text
    1. Hillier SL,
    2. Nugent RP,
    3. Eschenbach DA,
    4. et al
    . Association between bacterial vaginosis and preterm delivery of a low-birth-weight infant. The Vaginal Infections and Prematurity Study Group. N Engl J Med 1995;333:1737-42.
    CrossRefMedlineWeb of Science
  6. ↵
    1. Meis PJ,
    2. Goldenberg RL,
    3. Mercer B,
    4. et al
    . The preterm prediction study: significance of vaginal infections. National Institute of Child Health and Human Development Maternal-Fetal Medicine Units Network. Am J Obstet Gynecol 1995;173:1231-5.
    CrossRefMedlineWeb of Science
  7. ↵
    1. Wiesenfeld HC,
    2. Hillier SL,
    3. Krohn MA,
    4. Landers DV,
    5. Sweet RL
    . Bacterial vaginosis is a strong predictor of Neisseria gonorrhoeae and Chlamydia trachomatis infection. Clin Infect Dis 2003;36:663-8.
    Abstract/FREE Full Text
    1. Taha TE,
    2. Hoover DR,
    3. Dallabetta GA,
    4. et al
    . Bacterial vaginosis and disturbances of vaginal flora: association with increased acquisition of HIV. AIDS 1998;12:1699-706.
    CrossRefMedlineWeb of Science
  9. ↵
    1. Cherpes TL,
    2. Melan MA,
    3. Kant JA,
    4. Cosentino LA,
    5. Meyn LA,
    6. Hillier SL
    . Genital tract shedding of herpes simplex virus type 2 in women: effects of hormonal contraception, bacterial vaginosis, and vaginal group B Streptococcus colonization. Clin Infect Dis 2005;40:1422-8.
    Abstract/FREE Full Text
  10. ↵
    1. Bradshaw CS,
    2. Morton AN,
    3. Hocking J,
    4. et al
    . High recurrence rates of bacterial vaginosis over the course of 12 months after oral metronidazole therapy and factors associated with recurrence. J Infect Dis 2006;193:1478-89.
    Abstract/FREE Full Text
  11. ↵
    1. Koumans EH,
    2. Markowitz LE,
    3. Hogan V
    . Indications for therapy and treatment recommendations for bacterial vaginosis in nonpregnant and pregnant women: a synthesis of data. Clin Infect Dis 2002;35(Suppl 1):S152-72.
  12. ↵
    1. Avonts D,
    2. Sercu M,
    3. Heyerick P,
    4. Vandermeeren I,
    5. Meheus A,
    6. Piot P
    . Incidence of uncomplicated genital infections in women using oral contraception or an intrauterine device: a prospective study. Sex Transm Dis 1990;17:23-9.
    MedlineWeb of Science
    1. Barbone F,
    2. Austin H,
    3. Louv WC,
    4. Alexander WJ
    . A follow-up study of methods of contraception, sexual activity, and rates of trichomoniasis, candidiasis, and bacterial vaginosis. Am J Obstet Gynecol 1990;163:510-4.
    MedlineWeb of Science
  14. ↵
    1. Cherpes TL,
    2. Hillier SL,
    3. Meyn LA,
    4. Busch JL,
    5. Krohn MA
    . A delicate balance: risk factors for acquisition of bacterial vaginosis include sexual activity, absence of hydrogen peroxide-producing lactobacilli, black race, and positive herpes simplex virus type 2 serology. Sex Transm Dis 2008;35:78-83.
    CrossRefMedlineWeb of Science
  15. ↵
    1. Hawes SE,
    2. Hillier SL,
    3. Benedetti J,
    4. et al
    . Hydrogen peroxide-producing lactobacilli and acquisition of vaginal infections. J Infect Dis 1996;174:1058-63.
    Abstract/FREE Full Text
  16. ↵
    1. Hutchinson KB,
    2. Kip KE,
    3. Ness RB
    . Condom use and its association with bacterial vaginosis and bacterial vaginosis-associated vaginal microflora. Epidemiology 2007;18:702-8.
    CrossRefMedline
    1. McClelland RS,
    2. Lavreys L,
    3. Katingima C,
    4. et al
    . Contribution of HIV-1 infection to acquisition of sexually transmitted disease: a 10-year prospective study. J Infect Dis 2005;191:333-8.
    Abstract/FREE Full Text
  18. ↵
    1. Nagot N,
    2. Ouedraogo A,
    3. Defer MC,
    4. Vallo R,
    5. Mayaud P,
    6. Van de Perre P
    . Association between bacterial vaginosis and herpes simplex virus type-2 infection: implications for HIV acquisition studies. Sex Transm Infect 2007;83:365-8.
    Abstract/FREE Full Text
    1. Nansel TR,
    2. Riggs MA,
    3. Yu KF,
    4. Andrews WW,
    5. Schwebke JR,
    6. Klebanoff MA
    . The association of psychosocial stress and bacterial vaginosis in a longitudinal cohort. Am J Obstet Gynecol 2006;194:381-6.
    CrossRefMedlineWeb of Science
    1. Ness RB,
    2. Kip KE,
    3. Soper DE,
    4. Stamm CA,
    5. Rice P,
    6. Richter HE
    . Variability of bacterial vaginosis over 6- to 12-month intervals. Sex Transm Dis 2006;33:381-5.
    CrossRefMedlineWeb of Science
  21. ↵
    1. Schwebke J,
    2. Desmond RA
    . Risk factors for bacterial vaginosis in women at high risk for sexually transmitted diseases. Sex Transm Dis 2005;32:654-8.
    CrossRefMedlineWeb of Science
  22. ↵
    1. Sanchez S,
    2. Garcia PJ,
    3. Thomas KK,
    4. Catlin M Holmes KK
    . Intravaginal metronidazole gel versus metronidazole plus nystatin ovules for bacterial vaginosis: a randomized controlled trial. Am J Obstet Gynecol 2004;191:1898-906.
    CrossRefMedlineWeb of Science
  23. ↵
    1. Schwebke JR,
    2. Desmond RA
    . A randomized trial of the duration of therapy with metronidazole plus or minus azithromycin for treatment of symptomatic bacterial vaginosis. Clin Infect Dis 2007;44:213-9.
    Abstract/FREE Full Text
  24. ↵
    1. Bradshaw CS,
    2. Morton AN,
    3. Garland SM,
    4. Morris MB,
    5. Moss LM,
    6. Fairley CK
    . Higher-risk behavioral practices associated with bacterial vaginosis compared with vaginal candidiasis. Obstet Gynecol 2005;106:105-14.
    MedlineWeb of Science
    1. Brotman RM,
    2. Erbelding EJ,
    3. Jamshidi RM,
    4. Klebanoff MA,
    5. Zenilman JM,
    6. Ghanem KG
    . Findings associated with recurrence of bacterial vaginosis among adolescents attending sexually transmitted diseases clinics. J Pediatr Adolesc Gynecol 2007;20:225-31.
    CrossRefMedlineWeb of Science
  26. ↵
    1. Chiaffarino F,
    2. Parazzini F,
    3. De Besi P,
    4. Lavezzari M
    . Risk factors for bacterial vaginosis. Eur J Obstet Gynecol Reprod Biol 2004;117:222-6.
    CrossRefMedlineWeb of Science
    1. Larsson PG,
    2. Platz-Christensen JJ,
    3. Sundstrom E
    . Is bacterial vaginosis a sexually transmitted disease? Int J STD AIDS 1991;2:362-4.
    MedlineWeb of Science
  28. ↵
    1. Smart S,
    2. Singal A,
    3. Mindel A
    . Social and sexual risk factors for bacterial vaginosis. Sex Transm Infect 2004;80:58-62.
    Abstract/FREE Full Text
  29. ↵
    1. Ahmed S,
    2. Lutalo T,
    3. Wawer M,
    4. et al
    . HIV incidence and sexually transmitted disease prevalence associated with condom use: a population study in Rakai, Uganda. AIDS 2001;15:2171-9.
    CrossRefMedlineWeb of Science
  30. ↵
    1. Bailey JV,
    2. Farquhar C,
    3. Owen C
    . Bacterial vaginosis in lesbians and bisexual women. Sex Transm Dis 2004;31:691-4.
    CrossRefMedlineWeb of Science
  31. ↵
    1. Brabin L,
    2. Fairbrother E,
    3. Mandal D,
    4. et al
    . Biological and hormonal markers of chlamydia, human papillomavirus, and bacterial vaginosis among adolescents attending genitourinary medicine clinics. Sex Transm Infect 2005;81:128-32.
    Abstract/FREE Full Text
    1. Bukusi EA,
    2. Cohen CR,
    3. Meier AS,
    4. et al
    . Bacterial vaginosis: risk factors among Kenyan women and their male partners. Sex Transm Dis 2006;33:361-7.
    CrossRefMedlineWeb of Science
  33. ↵
    1. Calzolari E,
    2. Masciangelo R,
    3. Milite V,
    4. Verteramo R
    . Bacterial vaginosis and contraceptive methods. Int J Gynaecol Obstet 2000;70:341-6.
    CrossRefMedline
  34. ↵
    1. Cu-Uvin S,
    2. Hogan JW,
    3. Warren D,
    4. et al
    . Prevalence of lower genital tract infections among human immunodeficiency virus (HIV)-seropositive and high-risk HIV-seronegative women. HIV Epidemiology Research Study Group. Clin Infect Dis 1999;29:1145-50.
    Abstract/FREE Full Text
    1. Evans BA,
    2. Kell PD,
    3. Bond RA,
    4. MacRae KD
    . Racial origin, sexual lifestyle, and genital infection among women attending a genitourinary medicine clinic in London (1992). Sex Transm Infect 1998;74:45-9.
    Abstract
  36. ↵
    1. Evans AL,
    2. Scally AJ,
    3. Wellard SJ,
    4. Wilson JD
    . Prevalence of bacterial vaginosis in lesbians and heterosexual women in a community setting. Sex Transm Infect 2007;83:470-5.
    Abstract/FREE Full Text
    1. Fethers K,
    2. Marks C,
    3. Mindel A,
    4. Estcourt CS
    . Sexually transmitted infections and risk behaviours in women who have sex with women. Sex Transm Infect 2000;76:345-9.
    Abstract/FREE Full Text
    1. Guerreiro D,
    2. Gigante MA,
    3. Teles LC
    . Sexually transmitted diseases and reproductive tract infections among contraceptive users. Int J Gynaecol Obstet 1998;63(Suppl 1):S167-73.
    CrossRefMedline
    1. Holzman C,
    2. Leventhal JM,
    3. Qiu H,
    4. Jones NM,
    5. Wang J
    . Factors linked to bacterial vaginosis in nonpregnant women. Am J Public Health 2001;91:1664-70.
    Abstract/FREE Full Text
  40. ↵
    1. Koumans EH,
    2. Sternberg M,
    3. Bruce C,
    4. et al
    . The prevalence of bacterial vaginosis in the United States, 2001–2004; associations with symptoms, sexual behaviors, and reproductive health. Sex Transm Dis 2007;34:864-9.
    CrossRefMedlineWeb of Science
  41. ↵
    1. Marrazzo JM,
    2. Koutsky LA,
    3. Eschenbach DA,
    4. Agnew K,
    5. Stine K,
    6. Hillier SL
    . Characterization of vaginal flora and bacterial vaginosis in women who have sex with women. J Infect Dis 2002;185:1307-13.
    Abstract/FREE Full Text
  42. ↵
    1. McCaffrey M,
    2. Varney P,
    3. Evans B,
    4. Taylor-Robinson D
    . Bacterial vaginosis in lesbians: evidence for lack of sexual transmission. Int J STD AIDS 1999;10:305-8.
    Abstract/FREE Full Text
    1. Moi H
    . Prevalence of bacterial vaginosis and its association with genital infections, inflammation, and contraceptive methods in women attending sexually transmitted disease and primary health clinics. Int J STD AIDS 1990;1:86-94.
    Medline
    1. Morris MC,
    2. Rogers PA,
    3. Kinghorn GR
    . Is bacterial vaginosis a sexually transmitted infection? Sex Transm Infect 2001;77:63-8.
    Abstract/FREE Full Text
  45. ↵
    1. Myer L,
    2. Denny L,
    3. Telerant R,
    4. Souza M,
    5. Wright TC Jr,
    6. Kuhn L
    . Bacterial vaginosis and susceptibility to HIV infection in South African women: a nested case-control study. J Infect Dis 2005;192:1372-80.
    Abstract/FREE Full Text
    1. Nilsson U,
    2. Hellberg D,
    3. Shoubnikova M,
    4. Nilsson S,
    5. Mardh PA
    . Sexual behavior risk factors associated with bacterial vaginosis and Chlamydia trachomatis infection. Sex Transm Dis 1997;24:241-6.
    MedlineWeb of Science
    1. Patel V,
    2. Weiss HA,
    3. Mabey D,
    4. et al
    . The burden and determinants of reproductive tract infections in India: a population based study of women in Goa, India. Sex Transm Infect 2006;82:243-9.
    Abstract/FREE Full Text
    1. Peters N,
    2. Van Leeuwen AM,
    3. Pieters WJ,
    4. Hollema H,
    5. Quint WG,
    6. Burger MP
    . Bacterial vaginosis is not important in the etiology of cervical neoplasia: a survey on women with dyskaryotic smears. Sex Transm Dis 1995;22:296-302.
    MedlineWeb of Science
  49. ↵
    1. Schwebke JR,
    2. Desmond RA,
    3. Oh MK
    . Predictors of bacterial vaginosis in adolescent women who douche. Sex Transm Dis 2004;31:433-6.
    MedlineWeb of Science
  50. ↵
    1. Shoubnikova M,
    2. Hellberg D,
    3. Nilsson S,
    4. Mardh PA
    . Contraceptive use in women with bacterial vaginosis. Contraception 1997;55:355-8.
    CrossRefMedlineWeb of Science
  51. ↵
    1. Skinner CJ,
    2. Stokes J,
    3. Kirlew Y,
    4. Kavanagh J,
    5. Forster GE
    . A case-controlled study of the sexual health needs of lesbians. Genitourin Med 1996;72:277-80.
    MedlineWeb of Science
  52. ↵
    1. Warren D,
    2. Klein RS,
    3. Sobel J,
    4. et al
    . A multicenter study of bacterial vaginosis in women with or at risk for human immunodeficiency virus infection. Infect Dis Obstet Gynecol 2001;9:133-41.
    Medline
  53. ↵
    1. Yen S,
    2. Shafer MA,
    3. Moncada J,
    4. Campbell CJ,
    5. Flinn SD,
    6. Boyer CB
    . Bacterial vaginosis in sexually experienced and non-sexually experienced young women entering the military. Obstet Gynecol 2003;102:927-33.
    CrossRefMedlineWeb of Science
  54. ↵
    1. Dean AG,
    2. Sullivan KM,
    3. Soe MM
    . OpenEpi: open source epidemiologic statistics for public health, version 2.2.1. Available at: http://www.openepi.com. Accessed 20 October 2008.
  55. ↵
    1. Hillier SL,
    2. Rabe LK,
    3. Muller CH,
    4. Zarutskie P,
    5. Kuzan FB,
    6. Stenchever MA
    . Relationship of bacteriologic characteristics to semen indices in men attending an infertility clinic. Obstet Gynecol 1990;75:800-4.
    MedlineWeb of Science
    1. Holst E
    . Reservoir of four organisms associated with bacterial vaginosis suggests lack of sexual transmission. J Clin Microbiol 1990;28:2035-9.
    Abstract/FREE Full Text
  57. ↵
    1. Serour F,
    2. Samra Z,
    3. Kushel Z,
    4. Gorenstein A,
    5. Dan M
    . Comparative periurethral bacteriology of uncircumcised and circumcised males. Genitourin Med 1997;73:288-90.
    MedlineWeb of Science
  58. ↵
    1. Van Howe RS
    . Genital ulcerative disease and sexually transmitted urethritis and circumcision: a meta-analysis. Int J STD AIDS 2007;18:799-809.
    Abstract/FREE Full Text
  59. ↵
    1. Weiss HA,
    2. Thomas SL,
    3. Munabi SK,
    4. Hayes RJ
    . Male circumcision and risk of syphilis, chancroid, and genital herpes: a systematic review and meta-analysis. Sex Transm Infect 2006;82:101-9.
    Abstract/FREE Full Text
  60. ↵
    1. Weiss HA,
    2. Quigley MA,
    3. Hayes RJ
    . Male circumcision and risk of HIV infection in sub-Saharan Africa: a systematic review and meta-analysis. AIDS 2000;14:2361-70.
    CrossRefMedlineWeb of Science
  61. ↵
    1. Tobian A,
    2. Serwadda D,
    3. Quinn T
    . Program and abstracts of the 15th Conference on Retroviruses and Opportunistic Infections (Boston, Massachusetts). 2008. Trial of male circumcision: prevention of HSV-2 in men and vaginal infections in female partners, Rakai, Uganda [abstract 28LB].
  62. ↵
    1. Centers for Disease Control and Prevention
    . Sexually transmitted diseases treatment guidelines 2006. Special populations: women who have sex with women. Atlanta, GA: Centers for Disease Control and Prevention; 2006.
    1. Bailey JV,
    2. Farquhar C,
    3. Owen C,
    4. Mangtani P
    . Sexually transmitted infections in women who have sex with women. Sex Transm Infect 2004;80:244-6.
    Abstract/FREE Full Text
    1. Kellock D,
    2. O'Mahony CP
    . Sexually acquired metronidazole-resistant trichomoniasis in a lesbian couple. Genitourin Med 1996;72:60-1.
    MedlineWeb of Science
    1. Carroll N,
    2. Goldstein RS,
    3. Lo W,
    4. Mayer KH
    . Gynecological infections and sexual practices of Massachusetts lesbian and bisexual women. J Gay Lesbian Med Assoc 1997;1:15-23.
    CrossRef
  66. ↵
    1. Marrazzo JM,
    2. Koutsky LA,
    3. Stine KL,
    4. et al
    . Genital human papillomavirus infection in women who have sex with women. J Infect Dis 1998;178:1604-9.
    Abstract/FREE Full Text
  67. ↵
    1. Gardner HL,
    2. Dukes CD
    . Haemophilus vaginalis vaginitis: a newly defined specific infection previously classified non-specific vaginitis. Am J Obstet Gynecol 1955;69:962-76.
    MedlineWeb of Science
  68. ↵
    1. Berger BJ,
    2. Kolton S,
    3. Zenilman JM,
    4. Cummings MC,
    5. Feldman J,
    6. McCormack WM
    . Bacterial vaginosis in lesbians: a sexually transmitted disease. Clin Infect Dis 1995;21:1402-5.
    Abstract/FREE Full Text
  69. ↵
    1. Warner L,
    2. Newman DR,
    3. Austin HD,
    4. et al
    . Condom effectiveness for reducing transmission of gonorrhea and chlamydia: the importance of assessing partner infection status. Am J Epidemiol 2004;159:242-51.
    Abstract/FREE Full Text
  70. ↵
    1. Holmes KK,
    2. Levine R,
    3. Weaver M
    . Effectiveness of condoms in preventing sexually transmitted infections. Bull World Health Organ 2004;82:454-61.
    MedlineWeb of Science
  71. ↵
    1. Colli E,
    2. Landoni M,
    3. Parazzini F
    . Treatment of male partners and recurrence of bacterial vaginosis: a randomised trial. Genitourin Med 1997;73:267-70.
    MedlineWeb of Science
    1. Moi H,
    2. Erkkola R,
    3. Jerve F,
    4. et al
    . Should male consorts of women with bacterial vaginosis be treated? Genitourin Med 1989;65:263-8.
    MedlineWeb of Science
    1. Swedberg J,
    2. Steiner JF,
    3. Deiss F,
    4. Steiner S,
    5. Driggers DA
    . Comparison of single-dose vs one-week course of metronidazole for symptomatic bacterial vaginosis. JAMA 1985;254:1046-9.
    Abstract/FREE Full Text
    1. Vejtorp M,
    2. Bollerup AC,
    3. Vejtorp L,
    4. et al
    . Bacterial vaginosis: a double-blind randomized trial of the effect of treatment of the sexual partner. Br J Obstet Gynaecol 1988;95:920-6.
    MedlineWeb of Science
    1. Vutyavanich T,
    2. Pongsuthirak P,
    3. Vannareumol P,
    4. Ruangsri RA,
    5. Luangsook P
    . A randomized double-blind trial of tinidazole treatment of the sexual partners of females with bacterial vaginosis. Obstet Gynecol 1993;82:550-4.
    CrossRefMedlineWeb of Science
  76. ↵
    1. Mengel MB,
    2. Berg AO,
    3. Weaver CH,
    4. et al
    . The effectiveness of single-dose metronidazole therapy for patients and their partners with bacterial vaginosis. J Fam Pract 1989;28:163-71.
    MedlineWeb of Science
  77. ↵
    1. Bump RC,
    2. Buesching WJ 3rd
    . Bacterial vaginosis in virginal and sexually active adolescent females: evidence against exclusive sexual transmission. Am J Obstet Gynecol 1988;158:935-9.
    MedlineWeb of Science
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  1. Clin Infect Dis. (2008) 47 (11): 1426-1435. doi: 10.1086/592974
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