| HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
|
|
|
|||||||
|
|||||||||
ORIGINAL RESEARCH |
From the University of Pittsburgh, Pittsburgh, Pennsylvania; Magee-Womens Hospital and Magee-Womens Research Institute, Pittsburgh, Pennsylvania; University of Alabama School of Medicine, Birmingham, Alabama; Medical University of South Carolina, Charleston, South Carolina; Denver Health Medical Center, Denver, Colorado; and Boston Medical Center, Maxwell Finland Laboratory, Boston, Massachusetts.
Address reprint requests to: Roberta B. Ness, MD, MPH, University of Pittsburgh, Graduate School of Public Health, 130 DeSoto Street, Room 517 Parran Hall, Pittsburgh, PA 15261; E-mail: repro{at}pitt.edu.
 |
ABSTRACT |
|---|
TOP
 ABSTRACT MATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
|---|
METHODS: A total of 1200 women at high risk for sexually transmitted infections were enrolled from five clinical sites around the United States. Cross-sectional, structured interviews were conducted and vaginal swabs were self-obtained for Gram stain, culture, and DNA amplification tests for Neisseria gonorrhoeae and Chlamydia trachomatis.
RESULTS: Douching at least once per month was associated with an increased frequency of bacterial vaginosis. Those who douched recently (within 7 days) were at highest risk [odds ratio (OR) 2.1, 95% confidence interval (CI) 1.3, 3.1]. Douching for symptoms (OR 1.7, 95% CI 1.1, 2.6) and for hygiene (OR 1.3, 95% CI 1.0, 1.9) both related to bacterial vaginosis risk. The associations between douching and Gardnerella vaginalis, Mycoplasma hominis, and lack of hydrogen peroxide-producing lactobacilli were similar to those between douching and bacterial vaginosis. Gonococcal or chlamydial cervicitis was not associated with douching.
CONCLUSION: Douching for symptoms or hygiene, particularly frequent or recent douching, was associated with bacterial vaginosis and bacterial vaginosis-associated vaginal microflora, but not with gonococcal or chlamydial cervicitis.
Douching, a remarkably common practice in the United States1,2 may enhance the risk for vaginal infection. Human immunodeficiency virus (HIV) acquisition has been linked to douching, as have the sexually transmitted disease (STD)-related conditions, pelvic inflammatory disease (PID), preterm delivery, and cervical cancer.3–7
The mechanism by which douching predisposes to these diseases may be by disrupting the normal vaginal flora.8 In the healthy vagina, hydrogen peroxide (H2O2) + lactobacilli protect against endogenous bacteria (such as the anaerobic gram-negative rods Bacteroides and Prevotella, genital mycoplasmata, and Gardenerella vaginalis) and exogenous pathogens (such as Neisseria gonorrhoeae and Chlamydia trachomatis) by producing bacteriocins, as well as hydrogen peroxide and lactic acid, both of which lower the vaginal pH to a level inhospitable to many other bacteria.9 When the flora is disrupted, the H2O2-producing lactobacilli decrease in concentration and are replaced by an overgrowth of anaerobic and facultative aerobic bacteria.
To date, several cross sectional epidemiologic studies have shown an association between douching and bacterial vaginosis.10–14 Further, a single, small, prospective study found that douching for cleanliness or hygiene was independently associated with a two-fold risk of acquiring bacterial vaginosis.15 However, intervention experiments have found that the single use of nonmedicated douching products had a modest and transient effect on the vaginal microflora.16–19
Whether and how persistent douching as practiced in the community affects the various microflora found in the vagina remains unclear.13 In the only study to date that directly assessed this, Newton et al showed a 3.5-fold elevated risk of Trichomonas vaginalis and a 2.4-fold elevated risk of G vaginalis among women who douched.13 The study did not, however, characterize how frequency, recentness, and reason for douching impact vaginal microflora.
Douching has also been linked to gonococcal and chlamydial cervicitis, although this result has been inconsistent.5,12,20,21 Furthermore, although a single, causal chain linking douching, bacterial vaginosis, gonococccal or chlamydial cervicitis, and PID has been proposed, direct evidence for some of the links and for the full chain remains elusive.6,22–25
Here we extend previous observations by evaluating comprehensive, cross sectional vaginal microbiology data and data on lower genital tract pathogens obtained from 1200 women, some of whom had never douched and some who had douched with various degrees of frequency and recentness, and for a series of reasons. We hypothesized that more frequent and recent douching would relate to bacterial vaginosis and bacterial vaginosis-related microflora.
|
MATERIALS AND METHODS |
|---|
|
TOP
ABSTRACTMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
|---|
At baseline, study staff taught each subject how to self-obtain vaginal specimens using a Q-tip-like cotton swab. In past studies, the correlation between self-obtained vaginal swabs and clinician-obtained specimens for the detection of C trachomatis and bacterial vaginosis have been excellent.26,27 Vaginal swabs were smeared onto slides by study staff at the bedside and these slides were air dried and later Gram stained at a centralized microbiology laboratory under the direction of one of us (SLH). A score of 0–10 was assigned in light of the relative proportions of large gram-positive rods (lactobacilli), small gram-negative or gram-variable rods (Bacteroides or Gardnerella), and curved gram-variable rods (Mobiluncus).28 The results were interpreted by a standardized method for the diagnosis of bacterial vaginosis as described by Nugent.28 A score of 0–3 was interpreted as consistent with normal vaginal flora; a score of 4–6, corresponding to disturbed flora, was designated as intermediate; and a score of 7–10 was considered to be bacterial vaginosis. Relative to clinical signs, the scoring system has been shown to have a specificity of 83% and a sensitivity of 89% for bacterial vaginosis in nonpregnant women.26
The laboratory staff were masked with respect to demographic characteristics and douching behaviors of the subjects.
Two swabs, placed in an anaerobic transport vial, were also shipped to the microbiology laboratory for characterization of the following: Lactobacillus species, anaerobic gram-negative rods, G vaginalis, group B streptococcus, enterococcus species, Escherichia coli, Candida species, Mycoplasma hominis, and Ureaplasma urealyticum. One vaginal swab was used to inoculate a human blood bilayer Tween agar for detection of G vaginalis, a Columbia blood agar for detection of group B streptococcus, enterococcus species, E coli, and Candida species. A second swab was used to inoculate a Rogosa agar for recovery of lactobacilli, a Brucella agar for recovery of anaerobic bacteria, and broth media for recovery of M hominis and U urealyticum.
Lactobacilli were identified to the genus level on the basis of Gram stain morphology and production of lactic acid. All lactobacilli were tested for production of H2O2 using a qualitative assay on a tetramethylbenzidine agar plate as previously described.9 Anaerobic gram-negative rods were identified based on lack of capacity to grow in oxygen and on the basis of Gram stain characteristics. Group B streptococci, E coli, and yeast were identified by standard methods. Mycoplasmata were identified by their characteristic morphology on the agar plate after subculture from the selective broths.
DNA amplification for N gonorrhoeae and C trachomatis was performed using a strand displacement DNA Amplification Assay (Becton Dickinson, Sparks, MD) from self-obtained vaginal swabs. In the first 450 women, testing of urine was also accomplished using both strand displacement DNA amplification and ligase chain reaction (LCX, Abbott Diagnostics, Abbott Park, IL) to confirm the adequacy of the self-obtained vaginal swab strand displacement DNA amplification result. The correlation between urine strand displacement DNA amplification and vaginal swab strand displacement DNA amplification was 100%, and therefore, in all subsequent participants, only the vaginal swab specimen was used. All positive test results for gonorrhea or chlamydial infection were reported to the clinical sites within 1 week of enrollment.
In a standardized 20-minute interview conducted by trained research staff at each center, women were asked about the following aspects of their douching behavior: any douching in the past 2 months, frequency of douching in the past 2 months, most recent episode of douching, reason for douching, and type of product most often used. For purposes of analyses, these data were categorized into frequency (none, less than once per month, at least once per month) and recentness (7 or fewer days ago, 8–21 days ago, at least 22 days ago). These categorizations were consistent with previous literature.6,14,20 Women were asked to select one or more reasons for douching. These were categorized hierarchically into mutually exclusive categories of abnormal symptoms (including abnormal vaginal discharge, to reduce odor, and for bleeding between menses); before or after sex; and for hygiene (including general cleansing, after menses, because "it’s normal to douche," and to prevent pregnancy). Only three women reported that they had been advised by a health provider to douche so these were excluded from the analysis of reason for douching. We also asked the question, "The last time you douched what did you use?" Eighty-seven percent of those who douched reported using two major brands consisting of: purified water, sodium citrate, citric acid, vinegar, diazolidinyl urea, octoxynol-9, cetylpyridinium chloride, and edetate disodium, or purified water, vinegar, benzoic acid, "lemon mist," octoxynol-9, citric acid, sodium benzoate, disodium ethylenediaminetetra-acetic acid, and fragrance. Only ten women (1.9% of women who douched) used medicated douches.
Women were asked about demographic factors including age, race, highest completed level of education, income, marital status, and gravidity. They also reported relevant lifestyle behaviors such as tobacco smoking, number of sexual partners in the past 2 months, acquisition of a new partner in the past 2 months, contraception use, and sex with menses. Furthermore, they were requested to recall past episodes of sexually transmitted infections including PID, gonococcal cervicitis, chlamydial cervicitis, bacterial vaginosis, and trichomoniasis.
We evaluated data on douching, other potential risk factors, and vaginal microbiology, among women participating in the GYN Infections Follow-through Study at baseline. Cross sectional differences between groups were analyzed with the 
2 test for categorical variables. The proportion of women who reported various frequencies of douching, recentness of douching, type of douching product, and reason for douching, were determined within categories of normal vaginal flora, intermediate flora, and bacterial vaginosis.
Separate logistic regression models were run with each of the main independent variables: douching frequency, recentness, type of product, and reason for douching. Additional independent variables that had been identified on the basis of biologic plausibility and preliminary univariate analyses as possible confounders (Table 1
), were included in these models with the exception of highly co-linear variables and with the exception of income, which was missing for almost 10% of the cohort. Excluding income from multivariable models had little impact on the significance of the primary comparisons. Simplification of the models, with elimination of variables that were consistently insignificant (P < .10) and did not alter the effect size of the main independent by more than 10%, yielded a final model including: clinical site, age (continuous), race (black versus white or other), education (high school graduate or lesser attainment versus post-high school), history of trichomoniasis (yes/ no), gravidity (ever/never), current smoking (yes/no), sex with menses (yes/no), and hormonal contraceptive use within the past 2 months (yes/no). Separate multivariable models including this same set of covariates were run for each of the following microbiologic dependent variables: lack of H2O2 + lactobacilli, presence of bacterial vaginosis or intermediate flora, isolation of G vaginalis, isolation of M hominis, isolation of anaerobic pigmented gram-negative rods, gonococcal or chlamydial cervicitis, and yeast infections. Intermediate vaginal flora was combined with bacterial vaginosis into a single outcome because the two categories related similarly to all aspects of douching. For the same reason, H2O2 - lactobacilli and absence of lactobacilli were also combined into one outcome, as were gonococcal and chlamydial cervicitis.
|
|
RESULTS |
|---|
|
TOP
ABSTRACTMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
|---|
Forty percent of enrolled women had bacterial vaginosis and another 24% had intermediate vaginal flora. Women of black race, low education, low income, and a history of a sexually transmitted disease including PID, bacterial vaginosis, gonococcal cervicitis, chlamydial cervicitis, or trichomoniasis, were more likely to have bacterial vaginosis than normal flora (Table 1
). Furthermore, women who were ever pregnant, currently smoked, and had sex with menses were more likely to have bacterial vaginosis. Women using hormonal contraception were significantly less likely to have bacterial vaginosis, whereas consistent users showed a nonsignificant trend toward a lower bacterial vaginosis rate.
Women with bacterial vaginosis were much more likely than women with normal vaginal flora to lack H2O2 + lactobacilli (19.1% of those with bacterial vaginosis had H2O2 + lactobacilli isolated versus 76.5% with normal flora) (Table 2). This relationship to bacterial vaginosis was less apparent for H2O2 - lactobacilli. The pathogenic sexually transmitted infections N gonorrhoeae and C trachomatis were significantly increased among women with intermediate flora and bacterial vaginosis, as were many of the anaerobes and facultative aerobes tested. Among the indigenous vaginal bacteria, the strongest associations to bacterial vaginosis were found for G vaginalis, M hominis, and anaerobic pigmented gram-negative rods. Each of these indigenous vaginal bacteria was also significantly associated with douching (data not shown).
|
), douching once or more per month elevated the risk of having bacterial vaginosis or intermediate vaginal flora by 1.4-fold. Those who douched recently (within the past 7 days) were at even higher risk of having bacterial vaginosis/intermediate flora [odds ratio (OR) 2.1, 95% confidence interval (CI) 1.3,3.1]. Most women reported douching for symptoms or hygiene, both of which elevated bacterial vaginosis/intermediate flora risk. Only 94 women reported douching before or after sex, and in this group bacterial vaginosis/ intermediate flora risk was not elevated. The lack of relationship between douching before/after sex and bacterial vaginosis/intermediate flora could not be accounted for by a reduction in sexual frequency or douching frequency in the douching before/after sex group. Indeed, women in this group reported a statistically higher frequency of sexual intercourse, on average, than other women in the study (2.9 times per week versus 2.3 times per week) and a statistically higher frequency of douching (2.0 times versus 1.7 times).
|
The relationships between douching and lack of H2O2 + lactobacilli were similar to those between douching and bacterial vaginosis/intermediate flora. Table 3 also shows the associations between douching frequency, recentness, and reason for the outcomes of G vaginalis and mycoplasmata. These analyses generally support the patterns seen for the outcome of lack of H2O2 + lactobacilli. Not shown in tables are that the relationship between anaerobic nonpigmented gram-negative rods was much like that for G vaginalis and M hominis.
In contrast to these positive findings, there was no consistent relationship between douching and N gonorrhoeae or C trachomatis infection. Furthermore, yeast infections were not related to douching in multivariable models. Finally, 446 women reported washing with a cloth inserted in the vagina. Although this appeared to relate to bacterial vaginosis and endogenous vaginal bacteria in univariate models, washcloth use lost all significance in multivariable models (data not shown).
|
DISCUSSION |
|---|
|
TOP
ABSTRACTMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
|---|
Our data are consistent with several studies that examined a possible link between douching and the clinical or Gram stain diagnosis of bacterial vaginosis. In the only prospective study to date, Hawes et al enrolled women from STD clinics and found that women who douched for hygiene had a 2.1-fold increased risk of acquisition of bacterial vaginosis.15 Several other cross sectional analyses have generally confirmed this finding. Douching has been linked to bacterial vaginosis independent of other confounding factors in pregnant US women,10 nonpregnant US women,14 nonpregnant women attending STD clinics in London, England,11 and non-pregnant female sex workers in Nairobi, Kenya.12 There was a trend toward an association between douching and bacterial vaginosis among adolescent women in 13 US cities.29 In the study from Nairobi,12 the use of homemade soap and water douches (almost all women used homemade solutions) elevated the risk of bacterial vaginosis; however, water alone did not. Beyond that one observation, however, differential effects on bacterial vaginosis from various douching products, frequencies, recentness, and reasons have been little studied.
There is also limited information about how douching influences patterns of vaginal microorganisms. Newton et al recently published such a report examining a variety of environmental influences including douching.13 Douching more than once per month was associated with G vaginalis and T vaginalis but not with lactobacillus species, Ureaplasma, or Mycoplasma. However, the study methods did not distinguish between H2O2 + and H2O2 - lactobacilli, and the investigators did not include methods for the isolation of anaerobes.
Several intervention studies, providing insight into short-term effects, have been used to extrapolate about the chronic impact of douching on the vaginal microenvironment. These studies suggest that different douching solutions have different antibacterial effects. For example, Pavlova and Tao found that antiseptic douches inhibited all vaginal microorganisms including lactobacilli, whereas commercial douches containing mostly vinegar and water inhibited pathogens but not lactobacillus.17 Onderdonk et al showed only a transient reduction in bacterial counts with a mild acetic acid solution, whereas a providineiodine solution had a marked bacteriocidal effect.19 How long this antibacterial effect lasts has been unclear. Monif et al found that bacterial counts rebounded after 120 minutes, with lactobacilli being the first to recover.18 Juliano et al suggested long-term delays in bacterial regrowth even after short exposures to antiseptic douches.16 However, no study observed the impact of repeated douching. Recent (within 7 days) douching had the greatest impact on vaginal microecology in our study. This finding, supported by our previous report among women with PID,6 suggests that douching may have relatively immediate effects on vaginal microbiology that rebalance over time. However, the vaginal flora of women who douche repeatedly may not balance out to a stable H2O2 + predominant pattern. Once the predominance of H2O2 + lactobacilli is disrupted, the stability of finding H2O2 + lactobacilli in the vagina over time is reduced.15
Finally, douching before and after sex appeared to have less influence on the vaginal microflora than did douching for hygiene or abnormal symptoms. This may be because any adverse effect of douching may be outweighed by a beneficial effect on the bacterial vaginosis acquisition associated with sex.30 Having a new sex partner and having multiple sex partners has been associated with bacterial vaginosis in the past.15,31–34 Although we could not confirm these associations here, we did find sex during menses strongly related to bacterial vaginosis.
We did not find that douching was associated with gonococcal or chlamydial cervicitis. Previous studies have been inconsistent on this point.5,12,20,21,29 Our population may have provided particularly conservative estimates of the douching and bacterial STD relationship because all women were at high risk for STDs and therefore much alike with regard to STD risk. We did find that women with intermediate flora or bacterial vaginosis had a higher prevalence of gonococcal or chlamydial cervical infection. Further study will be needed to sort out the interrelationships between douching, bacterial vaginosis, and STDs.
Our study provides weight to an increasingly consistent literature linking douching to bacterial vaginosis. Particular strengths of our study included the large number of women studied, the use of consistent enrollment and data collection protocols, the use of an expert microbiology laboratory masked to each woman’s reported douching behavior, and the internal consistency shown between microbiologic outcomes. However, a major weakness was that the cross sectional design provides no assurance that douching preceded bacterial vaginosis. To reduce the possibility that abnormal vaginal symptoms instigated douching, we separately present data for women who douched for hygiene and those who douched for symptoms. The relationships between douching and vaginal microflora were relatively similar in these two groups.
Although our study design cannot completely exclude the possibility that unmeasured confounding might have influenced our result, the homogeneity of this high risk population and comprehensive statistical adjustment within multivariable models limit the likelihood that confounding accounted for our findings.
Overall, then, among over 1200 women at high risk for acquiring sexually transmitted infections, douching, particularly recent douching, was associated with bacterial vaginosis, lack of H2O2 + lactobacilli, and presence of bacterial vaginosis-associated anaerobes and facultative aerobes. Because bacterial vaginosis has been linked to acquisition of HIV, preterm birth, and PID, these data add to growing concerns about the adverse health effects from douching.
|
Footnotes |
|---|
The authors thank the following individuals whose dedication to working with the women enrolled in the GYN Infections Follow-through Study made this study possible: Susie Alagasarmy, Julie Beuler, Debbie Carr, Hope Cohen-Webb, Leslie Curll, Christine Donahue, Amanda Farmer, Janice French, Melissa Girman, Alice Howell, Juliette Hunt, Ellen Klein, Faye LeBoeuf, April Lehman, Rosalyn Liu, Ingrid Macio, Kathleen McKenna, Kim Miller, Megan Mundy, Anne Rideout, Jacqueline Travasso, Jennifer Watts, and Casey Zuckerman. The authors also thank Sevgi Aral, PhD, for helping to devise data collection instruments and Lori Burleigh and Barbara Kolodjiez for technical assistance.
Received November 28, 2001. Received in revised form April 2, 2002. Accepted April 18, 2002.
|
REFERENCES |
|---|
|
TOP
ABSTRACTMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
|---|
2. Abma JC, Chandra A, Mosher WD, Peterson LS, Piccinino LJ. Fertility, family planning, and women’s health: New data from the 1995 National Survey of Family Growth. Vital Health Stat 23 1997:1–114.
3. LaRuche G, Messou N, Ali-Napo L, Noba V, Faye-Kette H, Combe P, et al. Vaginal douching: Association with lower genital tract infections in African pregnant women. Sex Transm Dis 1999;26:191–6.[Medline]
4. Zhang J, Thomas G, Leybovich E. Vaginal douching and adverse health effects: A meta-analysis. Am J Public Health 1997;87:1207–11.
5. Stergachis A, Scholes D, Heidrich FE, Sherer DM, Holmes KK, Stamm WE. Selective screening for Chlamydia trachomatis infection in a primary care population of women. Am J Epidemiol 1993;138:143–53.
6. Ness RB, Soper DE, Holley RL, Peipert J, Randall H, Sweet RL, et al. Douching and endometritis: Results from the PID evaluation and clinical health (PEACH) study. Sex Transm Dis 2001;28:240–5.[Medline]
7. Gresenguet G, Kreiss JK, Chapko MK, Hillier SL, Weiss NS. HIV infection and vaginal douching in central Africa. AIDS 1997;11:101–6.[Medline]
8. Rosenberg MJ, Phillips RS. Does douching promote ascending infection? J Reprod Med 1992;37:930–8.[Medline]
9. Hillier SL, Krohn MA, Rabe LK, Klebanoff SJ, Eschenbach DA. The normal vaginal flora, H2O2-producing lactobacilli, and bacterial vaginosis in pregnant women. Clin Infect Dis 1993;16:S273–81.
10. Royce RA, French JI, Savitz DA, Thorp J. Vaginal douching, bacterial vaginosis, and preterm birth. Congr Epidemiol Abstr 2001;S161.
11. Rajamanoharan S, Low N, Jones SB, Pozniak AL. Bacterial vaginosis, ethnicity, and the use of genital cleaning agents: A case control study. Sex Transm Dis 1999;404–9.
12. Fonck K, Kaul R, Keli F, Bwayo JJ, Ngugi EN, Moses S, et al. Sexually transmitted infections and vaginal douching in a population of female sex workers in Nairobi, Kenya. Sex Transm Infect 2001;77:271–5.
13. Newton ER, Piper JM, Shain RN, Perdue ST, Peairs W. Predictors of the vaginal microflora. Am J Obstet Gynecol 2001;184:845–55.[Medline]
14. Holzman C, Leventhal JM, Jones NM, Wang J, BV Study Group. Factors linked to bacterial vaginosis in nonpregnant women. Am J Public Health 2001;91:1664–70.
15. Hawes SE, Hillier SL, Benedetti J, Stevens CE, Koutsky LA, Wolner-Hanssen P, et al. Hydrogen peroxide-producing lactobacilli and acquisition of vaginal infections. J Infect Dis 1996;174:1058–63.[Medline]
16. Juliano C, Piu L, Gavini E, Zanetti S, Fadda G. In vitro antibacterial activity of antiseptics against vaginal lactobacilli. Eur J Clin Microbiol Infect Dis 1992;11:1166–9.[Medline]
17. Pavlova SI, Tao L. In vitro inhibition of commercial douche products against vaginal microflora. Infect Dis Obstet Gynecol 2000;8:99–104.[Medline]
18. Monif GR, Thompson JL, Stephens HD, Baer H. Quantitative and qualitative effects of povidoneiodine liquid and gel on the aerobic and anaerobic flora of the female genital tract. Am J Obstet Gynecol 1980;137:432–8.[Medline]
19. Onderdonk AB, Delaney ML, Hinkson PL, Dubois AM. Quantitative and qualitative effects of douche reparations on vaginal microflora. Obstet Gynecol 1992;80:333–8.[Medline]
20. Scholes D, Stergachis A, Ichikawa LE, Heidrich FE, Holmes KK, Stamm WE. Vaginal douching as a risk factor for cervical Chlamydia trachomatis infection. Obstet Gynecol 1998;91:993–7.[Abstract]
21. Beck-Sague CM, Farshy CE, Jackson TK, Guillory L, Edelkind D, Bullard JC, et al. Detection of Chlamydia trachomatis cervical infection by urine tests among adolescents clinics. J Adolesc Health 1998;22:197–204.[Medline]
22. Koumans EH, Kendrick JS. Preventing adverse sequelae of bacterial vaginosis: A public health program and research agenda. Sex Transm Dis 2001;28:292–6.[Medline]
23. Soper DE, Brockwell NJ, Dalton HP, Johnson D. Observations concerning the microbial etiology of acute salpingitis. Am J Obstet Gynecol 1994;170:1008–17.[Medline]
24. Hillier SL, Kiviat NB, Hawes SE, Hasselquist MB, Hanssen PW, Eschenbach DA, et al. Role of bacterial vaginosis-associated microorganisms in endometritis. Am J Obstet Gynecol 1996;175:435–41.[Medline]
25. Peipert JF, Montagno AB, Cooper AS, Sung CJ. Bacterial vaginosis as a risk factor for upper genital tract infection. Am J Obstet Gynecol 1997;177:1184–7.[Medline]
26. Schwebke JR, Hillier SL, Sobel JD, McGregor JA, Sweet RL. Validity of the vaginal Gram stain for the diagnosis of bacterial vaginosis. Obstet Gynecol 1996;88:573–6.[Abstract]
27. Wiesenfeld HC, Heine P, Rideout A, Macio I, DiBiasi F, Sweet RL. The vaginal introitus: A novel site for Chlamydia trachomatis testing in women. Am J Obstet Gynecol 1996;174:1542–6.[Medline]
28. Nugent BP, Krohn MA, Hillier SL. Reliability of diagnosing bacterial vaginosis by a standardized method of Gram stain interpretation. J Clin Microbiol 1991;29:297–301.
29. Vermund SH, Sarr M, Murphy DA, Levin L, Abdallian SE, Ma Y, et al. Douching practices among HIV infected and uninfected adolescents in the United States. J Adolesc Health 2001;29(Suppl. 3):80–6.
30. Tevi-Benissan C, Belec L, Levy M, Schneider-Faveau V, Si Mohamed A, Hallouin MC, et al. In vivo semen-associated pH neutralization of cervicovaginal secretions. Clin Diagn Lab Immunol 1997;4:367–74.[Abstract]
31. Borbone F, Austin H, Louv WC, 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.[Medline]
32. Avonts D, Sercu M, Heyerick P, Vandermeeren I, Meheus A, 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.[Medline]
33. Hart G. Factors associated with trichomoniasis, candidiasis and bacterial vaginosis. Int J STD AIDS 1993:4:21–5.[Medline]
34. Nilsson U, Hellberg D, Shoubnikova M, Nilsson S, Mardh PA. Sexual behavior risk factors associated with bacterial vaginosis and Chlamydia trachomatis infection. Sex Transm Dis 1997;241–6.
This article has been cited by other articles:
|
|
 |
|
  K. A. Stoner, L. K. Rabe, M. N. Austin, L. A. Meyn, and S. L. Hillier Quantitative Survival of Aerobic and Anaerobic Microorganisms in Port-A-Cul and Copan Transport Systems J. Clin. Microbiol., August 1, 2008; 46(8): 2739 - 2744. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 P T Lan, C S. Lundborg, H D Phuc, A Sihavong, M Unemo, N T K Chuc, T H Khang, and I Mogren Reproductive tract infections including sexually transmitted infections: a population-based study of women of reproductive age in a rural district of Vietnam Sex Transm Inf, April 1, 2008; 84(2): 126 - 132. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 J. E. Allsworth and J. F. Peipert Prevalence of Bacterial Vaginosis: 2001 2004 National Health and Nutrition Examination Survey Data Obstet. Gynecol., January 1, 2007; 109(1): 114 - 120. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
R. D. Stapleton, J. M. Kahn, L. E. Evans, C. W. Critchlow, and C. M. Gardella Risk Factors for Group B Streptococcal Genitourinary Tract Colonization in Pregnant Women Obstet. Gynecol., December 1, 2005; 106(6): 1246 - 1252. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 R. B. Ness, K. E. Kip, S. L. Hillier, D. E. Soper, C. A. Stamm, R. L. Sweet, P. Rice, and H. E. Richter A Cluster Analysis of Bacterial Vaginosis-associated Microflora and Pelvic Inflammatory Disease Am. J. Epidemiol., September 15, 2005; 162(6): 585 - 590. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
C. S. Bradshaw, A. N. Morton, S. M. Garland, M. B. Morris, L. M. Moss, and C. K. Fairley Higher-Risk Behavioral Practices Associated With Bacterial Vaginosis Compared With Vaginal Candidiasis Obstet. Gynecol., July 1, 2005; 106(1): 105 - 114. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
R. B. Ness, S. L. Hillier, K. E. Kip, H. E. Richter, D. E. Soper, C. A. Stamm, J. A. McGregor, D. C. Bass, P. Rice, and R. L. Sweet Douching, Pelvic Inflammatory Disease, and Incident Gonococcal and Chlamydial Genital Infection in a Cohort of High-Risk Women Am. J. Epidemiol., January 15, 2005; 161(2): 186 - 195. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
M S Steele, E Bukusi, C R Cohen, B A Shell-Duncan, and K K Holmes Male genital hygiene beliefs and practices in Nairobi, Kenya Sex Transm Inf, December 1, 2004; 80(6): 471 - 476. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
J. Zhang, M. Hatch, D. Zhang, J. Shulman, E. Harville, and A. G. Thomas Frequency of Douching and Risk of Bacterial Vaginosis in African-American Women Obstet. Gynecol., October 1, 2004; 104(4): 756 - 760. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 X. Zhou, S. J. Bent, M. G. Schneider, C. C. Davis, M. R. Islam, and L. J. Forney Characterization of vaginal microbial communities in adult healthy women using cultivation-independent methods Microbiology, August 1, 2004; 150(8): 2565 - 2573. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 Bacterial Vaginosis: Making the Diagnosis and Reducing the Incidence Journal Watch (General), November 26, 2002; 2002(1126): 2 - 2. [Full Text]
|
|
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
| HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
