Association of Sexual Activity with Colonization and Vaginal Acquisition of Group B Streptococcus in Nonpregnant Women
Leslie A. Meyn1,
Donna M. Moore2,
Sharon L. Hillier1,,2 and
Marijane A. Krohn1,,2
1 Department of Obstetrics, Gynecology, and Reproductive Sciences, Magee-Womens Hospital, University of Pittsburgh, Pittsburgh, PA.
2 Magee-Womens Research Institute, Magee-Womens Hospital, University of Pittsburgh, Pittsburgh, PA.
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ABSTRACT
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In a longitudinal cohort study of 1,248 nonpregnant young women recruited from three Pittsburgh, Pennsylvania, health clinics in 19982000, the authors investigated risk factors associated with vaginal acquisition of group B Streptococcus (GBS). Rectal and vaginal swabs for GBS culture and demographic and behavioral interview data were obtained from the women at enrollment and at three 4-month intervals. Cox proportional hazards models were used to evaluate risk factors for GBS acquisition among the 1,089 women with follow-up data. At enrollment, 365 (29.2%) of the 1,248 study participants were vaginally colonized with GBS. Of 767 women who were GBS-negative at enrollment, 344 (44.9%) acquired vaginal GBS colonization during follow-up. The following factors were independently associated with vaginal acquisition of GBS at the 0.05 significance level: African-American race (hazard ratio (HR) = 1.5, 95% confidence interval (CI): 1.2, 1.9), having multiple sex partners during the past 4 months (HR = 1.7, 95% CI: 1.1, 2.5), having frequent sexual intercourse during the past 4 months (HR = 1.5, 95% CI: 1.1, 2.2), and having sexual intercourse within the 5 days prior to the follow-up visit (HR = 1.6, 95% CI: 1.3, 2.0). These results show that sexual activity is an important risk factor for vaginal acquisition of GBS.
regression analysis; risk factors; sex behavior; sexually transmitted diseases; streptococcal infections; Streptococcus agalactiae; vagina
Abbreviations:
CI, confidence interval; CNA plates, Columbia agar plates containing 5 percent sheep blood, colistin, and nalidixic acid; GBS, group B Streptococcus; HR, hazard ratio; OR, odds ratio
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INTRODUCTION
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Numerous cross-sectional studies have examined risk factors for colonization with group B Streptococcus (GBS). However, to our knowledge, there have been no published findings from longitudinal studies that have examined the factors associated with acquisition of GBS in the genital tract by young women. Hill et al. (1
) reported that none of 19 prepubertal girls were vaginally colonized with GBS, while another study of 171 postmenarchal adolescents (2
) found that approximately 20 percent were vaginally colonized. Several studies reported that 3642 percent of women visiting sexually transmitted disease clinics had genital GBS colonization (3

6
). There has been some evidence that sexual activity may be related to genital GBS colonization. Baker et al. (7
) found that vaginal GBS colonization was more prevalent among sexually experienced women than among women with no history of sexual intercourse. A large multicenter study of pregnant women found an increased risk of genital GBS colonization among those who had had both frequent sexual intercourse and multiple sex partners during the previous year (8
). Furthermore, a 1996 study found that heavy vaginal GBS colonization was associated with having multiple sex partners in the past 30 days among African-American women (9
). The purpose of this study was to examine the demographic and behavioral characteristics associated with vaginal and rectal GBS colonization in young nonpregnant women and to determine whether sexual activity was associated with acquisition of this organism.
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MATERIALS AND METHODS
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This longitudinal cohort study was designed to describe the dynamics of loss and acquisition of GBS colonization over time. The institutional review board of Magee-Womens Hospital in Pittsburgh, Pennsylvania, approved the study. Women between the ages of 18 and 30 years who were seeking care that required a gynecologic examination or who were willing to self-obtain vaginal and rectal specimens were eligible for participation in this study. The other inclusion criteria were ability to provide written informed consent, willingness to return for three follow-up visits over the next 12 months, and willingness to provide serum samples. The exclusion criteria for this study included known pregnancy, current vaginal bleeding, current use of systemic antimicrobial agents that are active against GBS (penicillins, cephalosporins, or macrolides), use of an intravaginal product in the past 24 hours (douches, antifungal products, or spermicides), and conditions that would prevent participation in scheduled follow-up visits. Between 1998 and 2000, after written informed consent had been obtained, 1,248 women were enrolled from the following three Pittsburgh health clinics: the University of Pittsburgh Student Health Clinic, the Allegheny County Health Department Clinic, and the Family Health Council Clinic of Aliquippa. Rectal and vaginal swabs for GBS culture, a vaginal smear, and demographic and behavioral interview data were obtained from the women at enrollment and at three 4-month intervals for 12 months. The interviews were administered by trained research personnel and consisted of closed-format questions pertaining to demographic factors, use of cigarettes, alcohol, and marijuana, use of intravaginal products, contraception, and sexual activity during the past 4 months.
The vaginal and rectal swabs were placed in separate tubes of Amies transport medium (MML Diagnostics Packaging, Inc., Troutdale, Oregon). The vaginal swabs were inoculated onto Columbia agar plates containing 5 percent sheep blood (Prepared Media Laboratories, Mississauga, Ontario, Canada) and then placed into selective broth medium (Prepared Media Laboratories). The rectal swabs were inoculated onto Columbia agar plates containing 5 percent sheep blood, colistin, and nalidixic acid (CNA plates) (Prepared Media Laboratories) and then placed into selective broth medium (Prepared Media Laboratories). Both the plates and the broths were incubated overnight in 5 percent carbon dioxide at 37°C. The broths containing the vaginal and rectal swabs were then subcultured onto blood agar plates and CNA plates, respectively, and incubated overnight.
GBS was identified on the basis of colony morphology, ß hemolysis, and a negative 3 percent catalase reaction, and identification was confirmed by means of the PathoDX agglutination system (Diagnostic Products Corporation, Los Angeles, California) (10
). After a 48-hour incubation, the broths were again subcultured onto Sabouraud dextrose agar plates (Gibson Laboratories, Inc., Lexington, Kentucky) for detection of yeasts. Both the initial blood agar and the Sabouraud plates were examined for yeast, which was identified on the basis of colony morphology and the presence of hyphae upon Gram stain. The presence of yeast was defined as detection of growth from agar or broth. Vaginal Lactobacillus was identified by colony and Gram stain morphology. All lactobacilli were tested for hydrogen peroxide production using a qualitative assay on a tetramethylbenzidine agar plate. The agar plates were incubated for 2 days in an anaerobic glove box at 37°C and were then exposed to ambient air. Any hydrogen peroxide formed reacted with the horseradish peroxidase in the agar to oxidize the tetra-methylbenzidine, which turns the Lactobacillus colonies blue (11
). The vaginal smear was Gram-stained and evaluated for bacterial vaginosis according to the Nugent criteria (12
).
As of October 19, 2001, 1,028 of these women had completed a 4-month follow-up visit, 894 had completed an 8-month follow-up visit, and 842 had completed a 12-month follow-up visit, for a total of 973.4 woman-years of follow-up. At least one follow-up visit was obtained for 1,089 women (87.3 percent). The 159 women who were lost to follow-up were more likely to be smokers and to have more sexual partners (p < 0.05). These women were also less likely to have a normal Gram stain score (03) or to be colonized with hydrogen peroxide-producing Lactobacillus (p < 0.05). Since these factors, with the exception of smoking, were found to be associated with GBS colonization or acquisition in this study, it is likely that the nonadherent subjects would have been at increased risk of GBS acquisition. Therefore, their loss from the data set may have had the effect of underestimating the hazard ratios for acquisition of GBS.
The enrollment data were analyzed using SPSS statistical software, release 10.1.4 (SPSS, Inc., Chicago, Illinois). Univariate associations of baseline characteristics with vaginal and/or rectal GBS colonization were tested using Pearson's chi-squared test, a chi-squared test for linear trend, or Fisher's exact test, where appropriate. The correlation between the density of GBS in the vagina and the density in the rectum was evaluated using Pearson's correlation coefficient. All statistical tests were evaluated at the 0.05 level of significance. Variables with p values less than 0.1 were considered for inclusion in a polytomous logistic regression model. Polytomous logistic regression was used to compare women with 1) rectal GBS colonization without vaginal GBS (rectum-positive, vagina-negative) and 2) vag-inal GBS colonization with or without rectal GBS (vagina-positive, rectum-positive or -negative) with 3) women who were GBS-negative at both sites at the enrollment visit (the reference group). The outcome variable was stratified in this manner because it was hypothesized that the use of intra-vaginal products, sexual behavior, and vaginal microflora would be associated with vaginal GBS colonization but not with rectal GBS colonization. Models were developed using forward stepwise regression based on the likelihood ratio test statistic. Variables were retained in the model if the Wald chi-squared test statistic had a p value of 0.05 or less.
Acquisition of vaginal GBS colonization was defined as being culture-negative in the vagina at the enrollment visit and culture-positive at the 4-, 8-, or 12-month visit. Cox proportional hazards models with interval-censored, time-dependent covariates were used to evaluate the risk factors associated with acquisition of vaginal GBS colonization. These models were developed using Stata statistical software, release 7.0 (Stata Corporation, College Station, Texas). Efron's method was used for handling tied failures, and the method of Lin and Wei (13
) was used to calculate the variance of the ß coefficients. Variables were considered for inclusion in these models if the p value from the log rank test for equality of survivor functions was less than 0.1. Forward stepwise regression was employed, and variables were retained in the model if the p value from the Wald chi-squared test statistic was 0.05 or less.
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RESULTS
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Of the 1,248 women enrolled, 764 (61.2 percent) were Caucasian, 434 (34.8 percent) were African-American, and 50 (4.0 percent) were Hispanic, Asian, Native American, or multiethnic. The latter 50 women were combined into one racial category, referred to as "other," for analysis. At the enrollment visit, 270 (21.6 percent) of the women were colonized with GBS in the rectum and vagina, 135 (10.8 percent) were colonized in the rectum only, and 95 (7.6 percent) were colonized in the vagina only, for an overall prevalence at either site of 40.1 percent. The densities of GBS in the vagina and rectum were highly correlated (r = 0.5, p < 0.001), with 852 (68.3 percent) of the vaginal-rectal pairs being concordant.
Tables 1 and 2 show the univariate associations of selected characteristics with vaginal and/or rectal GBS colonization for the 1,248 women at enrollment. GBS colonization was more prevalent in women enrolled from the Allegheny County Health Department and the Family Health Council of Aliquippa than in those enrolled from the University of Pittsburgh Student Health Clinic (p = 0.001). The other factors associated with GBS colonization were African-American race, marijuana use in the past 4 months, use of douche preparations in the past 4 months, use of yeast medication in the past 4 months, use of condoms containing the spermicide non-oxynol 9 in the past 4 months, a higher number of sexual partners in the past 4 months, more frequent sexual intercourse in the past 4 months, fewer days since last occasion of sexual intercourse, concurrent vaginal yeast colonization, and an intermediate Gram stain score (p < 0.05). Age, education, smoking in the past 4 months, alcohol use in the past 4 months, use of lubricated condoms in the past 4 months, use of spermicide in the past 4 months, and concurrent vaginal Lactobacillus colonization were not significantly associated with GBS colonization (p > 0.05).
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TABLE 1. Demographic and behavioral characteristics of nonpregnant women with vaginal and/or rectal group B Streptococcus at study enrollment, Pittsburgh, Pennsylvania, 19982000
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TABLE 2. Use of over-the-counter intravaginal products,* sexual activity, and presence of vaginal microflora among nonpregnant women with vaginal and/or rectal group B Streptococcus at study enrollment, Pittsburgh, Pennsylvania, 19982000
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Multivariable regression models were developed separately for number of sexual partners (model I), frequency of sexual activity (model II), and time since last sexual intercourse (model III), because of the high collinearity between these variables. For ease of discussion, we refer in this paper to the most conservative odds ratio estimates from the three models. Table 3 summarizes the polytomous logistic regression results for being colonized with GBS only in the rectum and being colonized with GBS in the vagina regardless of rectal colonization at the enrollment visit. Use of yeast medication during the past 4 months (odds ratio (OR) = 2.4, 95 percent confidence interval (CI): 1.4, 4.2) and use of condoms containing non-oxynol 9 (OR = 2.0, 95 percent CI: 1.2, 3.2) during the past 4 months were significantly associated with rectum-only colonization. Having an intermediate Gram stain score (OR = 0.4, 95 percent CI: 0.2, 0.9) was significantly inversely associated with rectum-only colonization in all three models, while a bacterial vaginosis Gram stain score (OR = 0.6, 95 percent CI: 0.4, 1.0) was significantly inversely associated in models I and II only (p < 0.05).
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TABLE 3. Adjusted risks of rectum-only and vaginal group B Streptococcus colonization in nonpregnant women at study enrollment (polytomous logistic regression model), Pittsburgh, Pennsylvania, 19982000
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African-American women (OR = 1.4, 95 percent CI: 1.1, 1.9) were significantly more likely to be colonized with GBS in the vagina, regardless of rectal GBS colonization, than Caucasian women, while women of other races were not more likely to be vaginally colonized (OR = 1.1, 95 percent CI: 0.6, 2.2). Concurrent vaginal yeast colonization (OR = 1.7, 95 percent CI: 1.3, 2.2) and an intermediate Gram stain score (OR = 2.0, 95 percent CI: 1.4, 2.8) were also associated with vaginal GBS colonization. In addition, the three measurements of sexual activity were all significantly associated with vaginal GBS colonization. For each measurement, the reference group was sexually inexperienced or abstinent women. Having had one sex partner during the past 4 months was associated with a 50 percent increased risk of vaginal colonization (OR = 1.5, 95 percent CI: 1.0, 2.3), while having had two or more sex partners was associated with a 70 percent increased risk (OR = 1.7, 95 percent CI: 1.0, 2.7) (p < 0.05). Women who had sexual intercourse an average of three or more times per week had a twofold increased risk (OR = 2.0, 95 percent CI: 1.2, 3.2), while women who had less frequent sexual intercourse were not significantly more likely to be vaginally colonized (OR = 1.4, 95 percent CI: 0.9, 2.1). Women who had had sexual intercourse within 5 days of study enrollment were 60 percent more likely to be vaginally colonized with GBS (OR = 1.6, 95 percent CI: 1.3, 2.1). The results for vaginal and/or rectal GBS acquisition in women who were negative at both sites at enrollment were similar to those for vaginal GBS acquisition in women who were GBS-negative in the vagina at enrollment regardless of rectal GBS colonization status; therefore, those results are not presented separately.
Table 4 shows rates of acquisition of GBS colonization in the vagina for the 767 women who were not vaginally colonized at enrollment and who returned for at least one follow-up visit. As of October 19, 2001, 344 (44.9 percent) of these women had acquired GBS colonization in the vagina during 561.7 woman-years at risk, for an overall rate of 61 acquisitions per 100 woman-years. African-American race, an educational level of high school or less, use of condoms containing non-oxynol 9 in the past 4 months, an increased number of sexual partners in the past 4 months, an increased frequency of sexual intercourse in the past 4 months, having had sexual intercourse within 5 days of the follow-up visit, and the absence of hydrogen peroxide-producing vaginal Lactobacillus at the previous visit were associated with higher rates of vaginal GBS acquisition (p < 0.05). No other factors were found to be significantly associated with the rate of vaginal GBS acquisition (p > 0.05).
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TABLE 4. Risk factors for acquisition of vaginal group B Streptococcus in nonpregnant women, Pittsburgh, Pennsylvania, 19982001
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Table 5 shows results from the Cox proportional hazards models. Again, models were developed separately for number of sexual partners (model I), frequency of sexual activity (model II), and time since last sexual intercourse (model III). African-American race was an independent risk factor for acquisition of vaginal GBS (hazard ratio (HR) = 1.5, 95 percent CI: 1.2, 1.9), as was the absence of hydrogen peroxide-producing vaginal Lactobacillus at the previous visit (HR = 1.2, 95 percent CI: 1.0, 1.5; p = 0.04). Women of "other" races were not more likely to acquire GBS in the vagina (HR = 0.9, 95 percent CI: 0.5, 1.8) than were Caucasian women. Having multiple sex partners was associated with a 70 percent increased risk (HR = 1.7, 95 percent CI: 1.1, 2.5), while women who had had only one sex partner during the previous 4 months were not significantly more likely to acquire vaginal GBS than sexually inexperienced or abstinent women (HR = 1.4, 95 percent CI: 1.0, 1.9). Similarly, women who had sexual intercourse three or more times per week were significantly more likely to acquire vaginal GBS (HR = 1.5, 95 percent CI: 1.1, 2.2), while women who had less frequent sexual intercourse were not (HR = 1.4, 95 percent CI: 1.0, 1.9). Having had sexual intercourse within 5 days of the follow-up visit was associated with a 60 percent increased risk of vaginal GBS acquisition (HR = 1.6, 95 percent CI: 1.3, 2.0).
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TABLE 5. Adjusted hazard of acquiring vaginal group B Streptococcus in nonpregnant women, Pittsburgh, Pennsylvania, 19982001
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DISCUSSION
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To our knowledge, this is the first study to have used polytomous logistic regression to differentiate between risk factors for vaginal and rectal-only GBS colonization, and the first to have evaluated the risk factors involved in acquisition of GBS colonization. However, many of the results of these analyses support those of previous reports.
The results of this study showed that sexual activity during the previous 4 months was associated with vaginal GBS colonization but not with rectal-only colonization in young nonpregnant women. Women who had multiple sex partners or frequent (three or more times per week) or recent (within the past 5 days) sexual intercourse had significantly higher risks of vaginal GBS colonization than less sexually active women and women who reported having no sexual activity during the past 4 months. Baker et al. (7
) also found that vaginal GBS colonization was more prevalent among 426 sexually experienced women than among 56 women with no history of sexual intercourse. However, they did not find an association between colonization and frequency of sexual intercourse or number of lifetime sex partners. The Vaginal Infections and Prematurity Study, a multicenter study of 7,742 pregnant women, found increased risk of genital GBS colonization among women who had had both frequent sexual intercourse and multiple sex partners during the previous year (8
). A 1996 study of 192 African-American and Hispanic women with a known positive sexually transmitted disease test or a history of a sexually transmitted disease contact found that heavy vaginal GBS colonization was associated with having multiple sex partners in the past 30 days among African-American women (9
). However, a study of 171 postmenarchal adolescent girls (2
) and another study of 300 women being treated at a sexually transmitted disease clinic in Sweden (14
) found no association between sexual activity and GBS colonization. Both of those studies were smaller than the current study, and the former study categorized sexual activity as being present or absent, while the latter compared women who had had multiple partners in the previous month with those who had had either one partner or no partner. Our study included three different measurements of sexual activity, each of which distinguished women who reported no sexual activity during the past 4 months from those who reported infrequent sexual activity as well as those who reported frequent sexual activity.
Multiple partners, frequent sexual intercourse, and recent sexual intercourse were also associated with increased risks of vaginal GBS acquisition in this study. This suggests either that GBS can be sexually transmitted or that sexual activity alters the microenvironment in a manner that makes it more permissive of GBS colonization. There has been evidence that sexual transmission may play a role in GBS colonization. A 1981 study in London, United Kingdom, reported higher GBS carriage rates among fathers of GBS-colonized babies (50 percent) than among fathers of noncolonized babies (24 percent) (15
). A 1991 Japanese study found GBS in the urine of 39 (54.9 percent) husbands of 71 GBS-positive women and found that 31 (91.2 percent) of 34 of these couples were co-colonized with identical GBS serotypes (16
).
African-American women had a 40 percent increased risk of vaginal GBS colonization at enrollment and a 50 percent increased risk of acquiring GBS in the vagina within 412 months of enrollment, as compared with Caucasian women or women of "other" races, after adjustment for other factors. No association was found between ethnicity and colonization with GBS only in the rectum at enrollment. Previous studies have shown that among pregnant women, African Americans are more likely to be genitally colonized with GBS than Caucasians (8
, 17
, 18
). However, two smaller studies of adolescents (2
) and nonpregnant women (7
) found no association between ethnicity and vaginal GBS colonization. The reason for the racial differences in GBS colonization and acquisition is unknown. One hypothesis is that African-American women may have lower serum antibody levels to GBS than Caucasian women, making them more susceptible to colonization. However, Campbell et al. (17
) did not find racial differences in serum concentrations of GBS capsular polysaccharide-specific immunoglobulin G antibody in an ethnically diverse population of 3,307 pregnant women. Some authors have speculated that there may be ethnic differences in mucosal surface receptors for GBS (9
).
Concurrent vaginal yeast colonization and an intermediate Gram stain score were significantly associated with vaginal GBS colonization at enrollment but not with GBS acquisition. This suggests that factors associated with these conditions may be similar to those associated with GBS colonization, but they are not part of the underlying mechanism for acquisition. Having multiple sex partners and having an intermediate Gram stain score were associated with heavy vaginal yeast colonization in this cohort (19
). Regan et al. (8
) also found that concurrent vaginal yeast colonization was a risk factor for genital GBS colonization.
The absence of hydrogen peroxide-producing vaginal Lactobacillus at the previous visit was significantly associated with vaginal GBS acquisition in these women. The absence of hydrogen peroxide-producing Lactobacillus in the vagina has been found to be associated with bacterial vaginosis, symptomatic candidiasis, and vaginal colonization by some genital pathogens, such as Gardnerella vaginalis and Bacteroides, in pregnant women but not associated with GBS colonization (20
). However, this earlier study did not investigate vaginal acquisition of GBS or other microorganisms. In another study, Women who lacked vaginal lactobacilli were found to have increased risks of acquiring human immunodeficiency virus type 1 and gonorrhea (21
). It has also been shown that women who lack hydrogen peroxide-producing vaginal Lactobacillus are more likely to acquire bacterial vaginosis (22
).
The use of condoms containing non-oxynol 9 during the past 4 months and use of yeast medication during the past 4 months were found to be significantly associated with GBS colonization in the rectum only at enrollment. This was an unusual finding, since these products are typically used in the vagina. One explanation may be that the use of these products inhibits the growth or adherence of GBS in the vagina, so that GBS was more often detected only in the rectums of women who used these products. While information on the effect of antimycotic medications on GBS has not been published, Ross et al. (23
) examined the effects of Candida albicans infection and clotrimazole treatment on group D Streptococcus in vitro. In the absence of C. albicans, concentrations of group D Streptococcus decreased after 1 day of exposure to clotrimazole and continued to decrease over a 5-day period (23
).
Women without predominantly Lactobacillus vaginal flora were less likely to be vaginally colonized by GBS, but these women were no less likely to be colonized rectally by this organism. Thus, a large proportion of women who were colonized only in the rectum had predominantly Lactobacillus vaginal flora, as assessed by Gram stain. These data suggest that the presence of hydrogen peroxide-producing lactobacilli in the vagina provide colonization resistance to GBS, with the result that GBS remains localized within the gastrointestinal tracts of these women.
Sexual activity was not only associated with vaginal GBS colonization in this cohort of nonpregnant women but also played a role in acquisition of the organism in the vagina. It is not likely that the underlying association is entirely one of sexual transmission, since colonization and acquisition also differed by race and by the presence of other vaginal microorganisms. Vaginal/penile intercourse may also cause disturbances of the vaginal ecosystem, which enhances the attachment and growth of GBS in the vagina.
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ACKNOWLEDGMENTS
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This research was supported by contract NO1-AI-75326 from the National Institute of Allergy and Infectious Diseases.
The authors acknowledge the support and cooperation of the staffs of the Family Health Council Clinic of Aliquippa, the Allegheny Health Department Clinic, and the University of Pittsburgh Student Health Clinic.
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NOTES
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Correspondence to Leslie A. Meyn, Department of Obstetrics, Gynecology, and Reproductive Sciences, Magee-Womens Hospital, 300 Halket Street, Pittsburgh, PA 15213 (e-mail: lmeyn{at}mail.magee.edu).
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Received for publication July 18, 2001.
Accepted for publication January 11, 2002.