Obstetrics and Gynecology

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ACOG publications are protected by copyright and = all=20 rights are reserved. ACOG publications may not be reproduced in = any form=20 or by any means without written permission from the copyright = owner. This=20 includes the posting of electronic files on the Internet, = transferring=20 electronic files to other persons, distributing printed output, = and=20 photocopying. Requests for authorization to make photocopies = should be=20 directed to: Copyright Clearing Center, 222 Rosewood Drive, = Danvers, MA=20 01923 (978) 750-8400

Original=20 Research

November=20 2003

Volume 102, Number = 5, Part=20 1
Pages 927 -=20 933=20

Bacterial Vaginosis in = Sexually=20 Experienced and Non-Sexually Experienced Young Women = Entering the=20 Military

Sophia Yen, MD,^a=20 Mary-Ann Shafer, MD,^a=20 Jeanne Moncada, MT,^b=20 Christopher J. Campbell, MC USN, = CDR,^d=20 Scott D. Flinn, MC USN,^c=20 and Cherrie B. Boyer, PhD^a=20

Objective: To estimate = the=20 prevalence of bacterial vaginosis by Nugent Gram stain = criteria in a=20 nonclinic national sample of young women entering recruit = training;=20 to examine clinical associations with bacterial vaginosis; = and to=20 evaluate the performance of a pH test card and Papanicolaou = smear=20 against Gram stain as screening tools for bacterial = vaginosis.=20

Methods: A = cross-sectional study=20 of 1938 women was conducted. Self-collected vaginal swabs = were=20 applied to a colorimetric pH test card and a glass slide for = Gram=20 stain evaluation according to the Nugent criteria. = Papanicolaou=20 smears and samples for sexually transmitted diseases = screening were=20 collected during routine entry pelvic examinations.=20

Results: Bacterial = vaginosis=20 prevalence was 27%, with 28% in sexually experienced and 18% = in=20 non-sexually experienced women (P =3D .001). = Bacterial=20 vaginosis prevalence was 11% in Asian/Pacific Islanders, = which was=20 lower than in other nonwhite ethnic groups (P =3D = .004).=20 Clinically, bacterial vaginosis was directly related to = multiple=20 sexual partners (P =3D .026), self-report of vaginal = discharge=20 (P =3D .001), self-report of vaginal odor (P = < .001),=20 and concurrent Chlamydia trachomatis infection = (P =3D=20 .002), and inversely related to hormonal contraceptive use = (P=20 =3D .013). Vaginal discharge did not achieve statistical = significance=20 in multivariate analysis. Compared with the Nugent criteria, = the=20 sensitivities and specificities for bacterial vaginosis = diagnosis=20 were as follows: colorimetric pH test: 72% and 67%; = Papanicolaou=20 smear: 72% and 79%, respectively.=20

Conclusion: Among these = diverse=20 young women, bacterial vaginosis occurs commonly in both = sexually=20 experienced and inexperienced young women and differs by = race and=20 ethnicity. The pH colorimetric test and Papanicolaou smear = performed=20 moderately well as screening tools for bacterial vaginosis. = The=20 inverse relationship of bacterial vaginosis with hormonal=20 contraceptive use and its direct relationship with C=20 trachomatis need further study.=20

^aDivision of = Adolescent=20 Medicine, Department of Pediatrics, University of = California, San=20 Francisco, California, USA
^bDepartment of Laboratory = Medicine,=20 University of California, San Francisco, California, = USA=20
^cBeaufort Naval = Hospital,=20 Beaufort, South Carolina, USA
^dNaval Special Warfare Group ONE, = San=20 Diego, California, USA=20

This study was supported by a Department of Defense grant = under=20 the Women's Health Initiative (DAMD17-95-C-5077) and in part = by the=20 Leadership Education in Adolescent Health (LEAH), Maternal = and Child=20 Health Bureau (Grant MCH000978).=20

The authors thank Kelli Betsinger, BA, and Alex = Dubovtsev, PhD,=20 for performance of the laboratory tests; and Jesse Canchola, = MS,=20 Jason Chang, BS, and Lance Pollack, PhD, for their = statistical=20 expertise.=20

(Obstet Gynecol 2003:102:927-933. =C2=A9 2003 by The = American College=20 of Obstetricians and Gynecologists.)

Bacterial vaginosis is the most common cause of vaginal = discharge=20 in the United States.¹=20 It is a clinical syndrome associated with the presence of a = group of=20 microorganisms rather than a single etiologic agent. = Bacterial=20 vaginosis is characterized by a shift in the vaginal flora = from the=20 normal Lactobacillus-dominant species to a mixed = flora,=20 including Gardnerella vaginalis, Bacteroides = species,=20 Mobiluncus species, and Mycoplasma hominis. = Bacterial=20 vaginosis is associated with reproductive health morbidity,=20 including pelvic inflammatory disease,^2-4=20 preterm birth, premature rupture of membranes,⁵=20 chorioamnionitis,⁶=20 spontaneous abortion,⁷=20 and post-gynecologic surgery infection.⁸=20 From the available studies that focus largely on sexually=20 transmitted disease (STD) clinic patients and pregnant = women,=20 bacterial vaginosis prevalence is estimated to range from 7% = among=20 asymptomatic women attending general practice clinics⁹=20 to 46% among women attending STD clinics.¹⁰=20

Traditionally, bacterial vaginosis diagnosis is defined=20 clinically by the presence of three of the four Amsel = criteria: 1)=20 vaginal pH > 4.5, 2) presence of adherent white = discharge, 3)=20 detection of "clue cells" by wet mount, and 4) presence of = an amine=20 odor after the addition of potassium hydroxide (also known = as the=20 "whiff" test).¹¹=20 Additional laboratory-based methods of bacterial vaginosis = diagnosis=20 have included culture for G vaginalis, biochemical = tests for=20 metabolic by-products of vaginal bacteria (gas=20 chromatography),¹¹=20 and colorimetric tests for enzymes produced by bacterial = vaginosis=20 organisms (sialidase).¹²=20 However, these methods remain research tools and are not = widely=20 available in clinical settings. The Papanicolaou smear has = also been=20 examined as a potential tool to diagnose bacterial vaginosis = because=20 of its widespread use, but reported results have been only = fair=20 (sensitivity 32-55%).^13,14=20

Most recently, researchers have adopted Gram stain = evaluation of=20 vaginal secretions as the gold standard for bacterial = vaginosis=20 diagnosis because of its higher sensitivity^15,16=20 and reproducibility (r =3D .82)¹⁷=20 than the clinically based Amsel criteria.¹⁸=20 The best Gram method is considered to be that of Nugent et=20 al.¹⁷=20 In this method, a standardized scoring system ranging from 0 = to 10=20 points is used. However, many clinicians have not adopted = this Gram=20 stain method for diagnosis of bacterial vaginosis because it = requires more time to perform and a trained laboratory = technician to=20 read the slides. Recently, new methods, such as a = colorimetric pH=20 and amine detection card, have been developed to achieve a = rapid=20 "point-of-care" diagnosis of bacterial vaginosis. These new=20 techniques eliminate the need for microscopy to detect "clue = cells,"¹⁶=20 which is time-consuming, and the "whiff" test, which is a = subjective=20 assessment for the presence of amines by the clinician.=20

Because of the evolving importance of bacterial vaginosis = to=20 women's reproductive health and new diagnostic tools = becoming=20 available to the practitioner, we undertook this study to 1) = estimate the prevalence of bacterial vaginosis by Nugent = Gram stain=20 criteria in a healthy, nonpregnant, nonclinic sample of both = sexually experienced and inexperienced young women from = throughout=20 the United States, 2) examine sociodemographic factors (race = or=20 ethnicity) and clinical factors (sexual behavior, = contraception,=20 current or past STDs) associated with a bacterial vaginosis=20 diagnosis, and 3) assess the performance of a rapid = colorimetric pH=20 test card and the Papanicolaou smear as screening methods = for=20 bacterial vaginosis compared with the Nugent Gram stain = criteria.=20

Materials and Methods=20

This study represents the baseline clinical data = collected from=20 women recruits participating in a larger longitudinal = intervention=20 study to prevent STDs and unintended pregnancy. All women = who=20 entered recruit training for the United States Marine Corps = between=20 June 1999 and June 2000 and completed the required routine = pelvic=20 examination with STD screening and a Papanicolaou smear = within 2=20 weeks of arrival were eligible for participation in the = study.=20

Voluntary, written, informed consent to participate in = the study=20 was obtained by female civilian research assistants before = data=20 collection. Women were free to decline participation and = were not=20 penalized in any manner if they did so. The institutional = review=20 boards of the University of California, San Francisco and = the=20 Beaufort Naval Hospital in South Carolina approved the = protocol.=20

The participants reported their reproductive health = history,=20 including STD history and current gynecologic symptoms, on a = standard clinic form before undergoing a pelvic examination = in the=20 Well Women's Clinic. Sexual experience was defined for the = purposes=20 of this study as having had vaginal intercourse at least = once.=20

For the first-void urine and self-collected vaginal = swabs,=20 participants received specific instructions from research = assistants=20 on the proper collection of the first-void urine (first 20 = mL in a=20 marked cup) and three self-collected vaginal swabs (insert = each swab=20 1 to 2 inches, rotate swab around in vagina three times, and = place=20 in plastic transport tube). Self-collected low vaginal swabs = are=20 increasingly being used for STD diagnosis and screening and = have=20 been found to be more sensitive than and as specific as = urine=20 samples.^19-22=20 One cotton swab was used for Trichomonas vaginalis = detection.=20 One of the Dacron swabs was used for bacterial vaginosis = Gram stain=20 analysis and colorimetric pH testing. The second Dacron swab = was=20 used for LCx testing (Abbott Laboratories, Abbott Park, IL) = for=20 Chlamydia trachomatis and Neisseria = gonorrhoeae. The=20 vaginal samples were transported to the clinic's laboratory = within 5=20 minutes of collection. Vaginal and first-void urine samples = targeted=20 for identification of C trachomatis and N = gonorrhoeae=20 were kept at 4C immediately after collection in the clinic = and=20 frozen at -70C in the hospital freezer within 24 hours of=20 collection. They were shipped overnight air freight to the = to the=20 laboratory based at San Francisco General Hospital (J. = Schachter,=20 PhD, laboratory director) in batches, maintaining the cold = chain=20 with specialized shipping containers with dry ice.=20

During the routine pelvic examination, endocervical = samples were=20 obtained for C trachomatis and N gonorrhoeae = with the=20 LCx kit swabs according to the manufacturer's directions, = and=20 endocervical samples for Papanicolaou smears were obtained = with a=20 cytobrush applied to a glass slide and fixed with a = preservative=20 spray. After the clinician collected the endocervical swabs, = specimens were transported maintaining the cold chain to the = Navy=20 Hospital.=20

For C trachomatis and N gonorrhoeae = testing,=20 vaginal, first-void urine, and endocervical samples were = processed=20 according to manufacturer's directions for ligase chain = reaction=20 tests (LCx). A positive on any of the samples (vaginal, = first-void=20 urine, or endocervical) was considered positive for = infection with=20 the respective organism for our analysis purposes. (It is = important=20 to note that 90% of the chlamydia tests were run by LCx = before March=20 1, 2001, before problems with false positives were = encountered due=20 to changes by the manufacturer. All positives identified in = the=20 final 10% of samples run after March 1, 200l were retested = and=20 confirmed).=20

For T vaginalis testing, the second self-collected = vaginal=20 swab was tested for T vaginalis with the Trichomonas = In-Pouch=20 TV (Biomed Diagnostics, San Jose, CA) according to the=20 manufacturer's instructions. They were incubated in pouches = at=20 collection at 37C and read for the presence of T = vaginalis at=20 2 and 5 days of inoculation by trained research assistants.=20

To diagnose bacterial vaginosis according to the Nugent = Gram=20 stain criteria (the Nugent criteria), the vaginal swabs were = rolled=20 onto glass slides within 5 minutes of the self-collection. = The=20 slides were then air-dried, stored, and transported in = batches by=20 overnight air freight on a monthly basis to the laboratory = based at=20 San Francisco General Hospital. The slides were Gram-stained = and=20 evaluated by a trained laboratory technologist (JM). The = Nugent=20 criteria score vaginal flora as normal (0-3), intermediate = (4-6) and=20 positive (7-10) for bacterial vaginosis.¹⁷=20 Only Gram stains with Nugent scores of 7-10 were considered = positive=20 for bacterial vaginosis.=20

To assess vaginal pH (FemExam pH and Amine TestCard, = Litmus=20 Concepts Inc., Santa Clara, CA), after the self-collected = swab was=20 applied to a glass slide (for bacterial vaginosis), the swab = was=20 then applied to the FemExam test card to detect elevated pH, = according to the manufacturer's directions. If the pH was = >4.6,=20 the pH test area shows a blue plus (+) sign. Readings were = performed=20 in the clinic's laboratory by a trained research laboratory=20 technician, who was unaware of the woman's history and the=20 clinician's findings on examination. (The amine portion of = test card=20 was not included in analysis because the test could not be = performed=20 according to manufacturer's directions, ie, immediately at = bedside.)=20

At the Beaufort Naval Hospital's regional laboratory, one = cytopathologist reviewed the endocervical Papanicolaou = examination=20 slides according to standard Bethesda criteria.²³=20 The cytopathologist was unaware of the presence or absence = of=20 vaginal symptoms in the women and of the purpose of the = study.=20 Papanicolaou diagnoses consistent with bacterial vaginosis = were=20 defined as a report specifying "clue cells and/or = non-specific=20 vaginitis."=20

The associations between Nugent criteria diagnoses of = bacterial=20 vaginosis and race or ethnicity, contraceptive use, history = of=20 sexually transmitted infections, and history of sexual = activity were=20 examined with 3Dchi=20 ²=20 and Fisher exact tests where applicable. In the case of = ethnicity,=20 the 15 post hoc pairwise comparisons were assessed with = Fisher exact=20 tests and a modified Bonferroni correction to control for = type I=20 error.²⁴=20 Significant correlates were included in a logistic = regression model=20 to determine whether those univariate relationships remained = while=20 adjusting for other significant correlates. The sensitivity, = specificity, and positive and negative predictive values of = the pH=20 colorimetric test and Papanicolaou smears were assessed with = the=20 Nugent criteria used as the diagnostic standard.=20

Results=20

Of the 2157 participants (94% of those who were = approached), 1938=20 had complete data for assessment of bacterial vaginosis = according to=20 the Nugent criteria; 1652 had complete data for analysis of=20 colorimetric test card performance (samples were excluded if = there=20 was blood on the swab, which made the results invalid); and = 1858 had=20 complete data for Papanicolaou performance analysis.=20

Selected demographic and clinical characteristics of the = study=20 sample are shown in Table=20 1. The study participants were on average 19.1 years old = (standard deviation =3D 2.1 years, range 17-33; 75% were = between ages=20 17-19 years), ethnically and racially diverse, and most had=20 experienced vaginal sexual intercourse in their lifetime = (86%). Of=20 the participants, 19% reported vaginal discharge, and 6.6% = reported=20 vaginal odor. Findings consistent with bacterial vaginosis = were=20 reported on 35% of Papanicolaou smears. Of the sexually = experienced=20 participants, 11.4% were infected with C trachomatis, = 2.3%=20 with N gonorrhoeae, and 1.7% with T vaginalis. =

The overall prevalence of bacterial vaginosis by the = Nugent=20 criteria was 27% (516 of 1938; 95% confidence interval [CI] = 25%,=20 29%), with differences in rates according to sexual = experience: 28%=20 (468 of 1675; 95% CI 26%, 30%) among the sexually = experienced and=20 18% (48 of 263; 95% CI 14%, 23%) among the non-sexually = experienced=20 (P =3D .001). Bacterial vaginosis prevalence also = differed by=20 race or ethnicity (P =3D .004): 25% in whites, 32% in = blacks,=20 30% in Hispanics, 34% in Native Americans, 11% in = Asian/Pacific=20 Islanders, and 26% in other groups (see Table=20 2). Post hoc comparisons revealed that the lower = bacterial=20 vaginosis prevalence in Asian/Pacific Islanders was = significantly=20 different when compared with blacks and Hispanics. No other = ethnic=20 differences achieved statistical significance.=20

Univariate analysis showed that several clinical factors = were=20 associated with bacterial vaginosis diagnosis. Bacterial = vaginosis=20 was positively related to self-report of vaginal discharge = (P=20 =3D .001) and self-report of vaginal odor (P < = .001), but=20 the relationship with clinician detection of vaginal = discharge was=20 not significant (Table=20 3). Among those sexually experienced, having multiple = sexual=20 partners in the past 3 months (P =3D .026) and C=20 trachomatis (P =3D .002) infection were found to = be=20 associated with bacterial vaginosis. In contrast, there was = an=20 inverse relationship between a bacterial vaginosis diagnosis = and=20 report of hormonal contraceptive use (P =3D .013) (Table=20 4). Bacterial vaginosis was not significantly associated = with=20 prior STD history, barrier contraception use, nor with = current T=20 vaginalis or N gonorrhoeae infections.=20

To evaluate whether these significant univariate = relationships=20 are still obtained when adjusted for each other, a multiple = logistic=20 regression analysis was performed with diagnosis of = bacterial=20 vaginosis by Nugent criteria as the outcome on a model = containing=20 all correlates with a P value less than .10 on the = univariate=20 test of significance. Of the seven correlates in the model, = only=20 self-reported vaginal discharge was not significant. = Ethnicity,=20 sexual experience, self-reported vaginal odor, having = multiple=20 sexual partners in the past 3 months, C trachomatis=20 infection, and report of hormonal contraceptive use were all = significant correlates of bacterial vaginosis diagnosis (see = Table=20 5).=20

In a multiple logistic regression analysis to confirm = differences=20 identified in univariate analyses, Asian/Pacific Islanders = were=20 designated as the reference group for ethnicity. Native = American,=20 black, and Hispanic respondents all had significantly higher = odds of=20 a bacterial vaginosis diagnosis than did Asian/Pacific = Islander=20 respondents (see Table=20 5). The comparisons of whites to Asian/Pacific Islanders = and=20 members of other ethnic groups to Asian/Pacific Islanders = were in=20 the expected direction but did not achieve statistical = significance=20 as defined by the Bonferroni correction. The logistic = regression=20 model achieved good fit as assessed by the Hosmer-Lemeshow=20 goodness-of-fit test ( 3Dchi=20 ²₈=20 =3D 8.80, P =3D .359).=20

Calculations to assess the performance profiles of the pH = colorimetric test and Papanicolaou smear showed that the = sensitivity=20 and specificity of a positive pH test were 72% and 67%, = respectively=20 (95% CIs 68%, 76% and 64%, 70%, respectively). The = performance of=20 the Papanicolaou smear yielded a sensitivity of 72% (95% CI = 68%,=20 76%) and a specificity of 79% (95% CI 77%, 81%) for = detection of=20 bacterial vaginosis with the Nugent criteria used as the = standard.=20

Discussion=20

The prevalence of bacterial vaginosis according to the = Nugent=20 criteria among a healthy, racially and ethnically diverse = sample of=20 young women from throughout the United States was found to = be 27%,=20 with a significantly higher rate among the sexually = experienced=20 (28%) compared with those without sexual experience (18%). = This=20 confirms previous research that showed a significant = positive=20 relationship between sexual experience and the presence of = microbes=20 associated with bacterial vaginosis.¹⁷=20 Women entering the military represent a unique diverse = national=20 sample to study, when compared with previous bacterial = vaginosis=20 research that has focused largely on women attending = gynecology,=20 prenatal, and STD clinics.^{9,10,15,25-27}=20 When compared with other studies in which the Nugent = criteria were=20 used, our overall bacterial vaginosis prevalence rate was = higher=20 than the 7% prevalence found in asymptomatic general = practice=20 patients⁹=20 and more consistent with samples of women attending family=20 planning²⁶=20 and STD clinics.²⁷=20

Our sample of 263 young women who report never = experiencing=20 vaginal intercourse is the largest sample of non-sexually=20 experienced women to date evaluated for bacterial vaginosis = with the=20 Nugent criteria by five-fold (based on a systematic search = with the=20 PubMed search engine; search terms "bacterial vaginosis," = "virgin,"=20 "sexual," "experience," "gardnerella"; including all = languages;=20 covering the dates mid1960s until June 2003 and based on = review of=20 all articles in this bibliography). Previous smaller studies = of=20 non-sexually experienced young women and girls in which = Amsel=20 criteria were used showed prevalences ranging from 0% = (n =3D=20 18)¹¹=20 to 12% (n =3D 52).²⁸=20 Our higher prevalence among both the sexually experienced = and=20 non-sexually experienced women is most likely due to our use = of the=20 Nugent criteria for diagnosis, which is more sensitive than = the=20 clinically based Amsel criteria. Previous studies have shown = that=20 the Amsel criteria have a sensitivity of only 35-56% and = specificity=20 of 96-99% when compared with the Nugent criteria.^15,16=20 It is also possible that the young women underreported prior = sexual=20 experience if such activity was involuntary. Finally, our = reported=20 prevalence among the sexually experienced cohort is = consistent with=20 previous studies in which the Nugent criteria were = used.^16,18,26,27=20

Given our large sample, we were able to examine bacterial = vaginosis prevalence by race and ethnicity and found a = significantly=20 lower rate among Asian/Pacific Islanders compared with = Native=20 Americans, blacks, and Hispanics. This is consistent with = previous=20 studies, which showed a trend toward lower rates of = bacterial=20 vaginosis in pregnant Asian/Pacific Islanders and British=20 Asians.²⁹=20 Although bacterial vaginosis is not a sexually transmitted=20 infection, these findings follow the pattern of infection = for a=20 number of STDs. However, the lower prevalence among = Asian/Pacific=20 Islanders remained significant despite adjusting for all the = other=20 significant correlates, including sexual experience and C = trachomatis infection status. Perhaps the difference in=20 prevalence by ethnicity could be explained by differences in = douching practices (which has been associated with bacterial = vaginosis²⁶)=20 or foreign body use (eg, tampons,²⁶=20 sex toys, etc) that might affect the vaginal ecosystem, as = well as=20 biologic factors, which might vary by ethnicity, that we did = not=20 examine in this study. More detailed studies on behavioral = and=20 biologic factors associated with bacterial vaginosis among = diverse=20 ethnic or racial groups are clearly warranted.=20

Frequently, clinicians diagnose vaginal infections by = syndromic=20 diagnosis, relying mainly on history and the observation of=20 discharge.³⁰=20 Clinicians are accustomed to investigating vaginal = discharge, but=20 our findings of the association of bacterial vaginosis and=20 self-reported vaginal odor adds another symptom for which = clinicians=20 can query their patients. Our findings support the use of pH = to=20 assist in the diagnosis of bacterial vaginosis for = clinicians=20 without access to microscopy, given its reasonable = sensitivity (72%)=20 but keeping in mind its lower specificity (67%), when = compared with=20 the Nugent criteria as the gold standard for diagnosis. The=20 Papanicolaou smear might prove to be useful under some = circumstances=20 to screen for bacterial vaginosis. We found the sensitivity = and=20 specificity for the Papanicolaou smear (70% and 79%, = respectively)=20 to be comparable to and consistent with previous studies = reporting=20 sensitivities ranging from 55% to 89% and specificities from = 85% to=20 96%.^14,16=20 If bacterial vaginosis is determined to pose a significant = morbidity=20 for nonpregnant women, the Papanicolaou smear might be a = reasonable=20 "first-line" screening tool during routine gynecologic = examinations=20 of healthy populations, given its moderate performance and = that it=20 adds no cost to the routine pelvic examination of adult = women.=20

Finally, regarding clinical correlates of bacterial = vaginosis,=20 our finding of an increased prevalence of bacterial = vaginosis among=20 those women with C trachomatis infection is supported = by=20 other research,³¹=20 which suggest that bacterial vaginosis might facilitate STD=20 infection by decreasing local secretory leukocyte protease = inhibitor=20 levels. Although we did not find an association between N = gonorrhoeae and T vaginalis infection and = bacterial=20 vaginosis, this is most likely due to the low number of = positives=20 (39 and 28, respectively), given that the difference in = bacterial=20 vaginosis prevalence was the same as that with C = trachomatis=20 infection. Furthermore, the finding of an association = between=20 hormonal contraception and bacterial vaginosis, which = suggests a=20 possible protective factor against bacterial vaginosis, has = been=20 described by other groups as well.^26,32-36=20 Given that our study is cross-sectional, no causal = relationship can=20 be determined. Further research is indicated to explain the=20 associations between bacterial vaginosis and both C=20 trachomatis and hormonal contraception.=20

In summary, bacterial vaginosis is prevalent among young = women=20 who have and have not experienced vaginal intercourse and = varies by=20 race or ethnicity. The Papanicolaou smear and pH testing = performed=20 moderately well as screening tests for bacterial vaginosis. = Finally,=20 this study reinforces the need for more research on the = inverse=20 relationship between bacterial vaginosis and hormonal = contraceptive=20 use and the direct relationship between bacterial vaginosis = and C=20 trachomatis infection.=20

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Address reprint requests to: Sophia Yen, MD, 3333 = California=20 Avenue, Suite 245, Box 0503, San Francisco, CA 94143; = E-mail: syen@itsa.ucsf.edu

Received April 10, 2003.
Received in = revised=20 form July 9, 2003.
Accepted July 17,=20 2003.

Copyright =C2=A9 2003 by = The American=20 College of Obstetricians and Gynecologists
Published by = Elsevier=20 Science Inc.
Visit Obstetrics & Gynecology online at = http://www.greenjournal.org/ =

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