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      Lactobacillus crispatus inhibits growth of Gardnerella vaginalis and Neisseria gonorrhoeae on a porcine vaginal mucosa model

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          Abstract

          Background

          The vaginal microbiota can impact the susceptibility of women to bacterial vaginosis (BV) and sexually transmitted infections (STIs). BV is characterized by depletion of Lactobacillus spp., an overgrowth of anaerobes (often dominated by Gardnerella vaginalis) and a pH > 4.5. BV is associated with an increased risk of acquiring STIs such as chlamydia and gonorrhea. While these associations have been identified, the molecular mechanism(s) driving the risk of infections are unknown. An ex vivo porcine vaginal mucosal model (PVM) was developed to explore the mechanistic role of Lactobacillus spp. in affecting colonization by G. vaginalis and Neisseria gonorrhoeae.

          Results

          The data presented here demonstrate that all organisms tested can colonize and grow on PVM to clinically relevant densities. Additionally, G. vaginalis and N. gonorrhoeae form biofilms on PVM. It was observed that lactic acid, acetic acid, and hydrochloric acid inhibit the growth of G. vaginalis on PVM in a pH-dependent manner. N. gonorrhoeae grows best in the presence of lactic acid at pH 5.5, but did not grow well at this pH in the presence of acetic acid. Finally, a clinical Lactobacillus crispatus isolate (24-9-7) produces lactic acid and inhibits growth of both G. vaginalis and N. gonorrhoeae on PVM.

          Conclusions

          These data reveal differences in the effects of pH, various acids and L. crispatus on the growth of G. vaginalis and N. gonorrhoeae on a live vaginal mucosal surface. The PVM is a useful model for studying the interactions of commensal vaginal microbes with pathogens and the mechanisms of biofilm formation on the vaginal mucosa.

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          Most cited references 74

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          Bacterial vaginosis is a strong predictor of Neisseria gonorrhoeae and Chlamydia trachomatis infection.

          To evaluate whether bacterial vaginosis predicts the acquisition of sexually transmitted diseases (STDs), we studied 255 nonpregnant female subjects aged 15-30 who reported recent sexual contact with a male partner in whom either gonococcal or chlamydial urethritis or nongonococcal urethritis was diagnosed. Compared to subjects with normal vaginal flora, subjects with bacterial vaginosis were more likely to test positive for Neisseria gonorrhoeae (odds ratio [OR], 4.1; 95% confidence interval [CI], 1.7-9.7) and Chlamydia trachomatis (OR, 3.4; 95% CI, 1.5-7.8). Subjects colonized vaginally by hydrogen peroxide-producing lactobacilli were less likely to receive a diagnosis of chlamydial infection or gonorrhea than subjects without such lactobacilli. Bacterial vaginosis was a strong predictor of gonorrhea and chlamydial infection among subjects who reported recent exposure to a male partner with urethritis. These data support the importance of vaginal flora in the defense against STD acquisition.
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            The identification of vaginal Lactobacillus species and the demographic and microbiologic characteristics of women colonized by these species.

            Lactobacillus acidophilus has been reported to be the predominant vaginal species. Vaginal lactobacilli isolated from 215 sexually active women were identified using whole-chromosomal DNA probes to 20 American Type Culture Collection Lactobacillus strains. Most women were colonized by L. crispatus (32%), followed by L. jensenii (23%), a previously undescribed species designated L. 1086V (15%), L. gasseri (5%), L. fermentum (0.3%), L. oris (0.3%), L. reuteri (0.3%), L. ruminis (0.3%), and L. vaginalis (0.3%). H2O2 was produced by 95% of L. crispatus and 94% of L. jensenii isolates, compared with only 9% of L. 1086V. Colonization by L. crispatus or L. jensenii was positively associated with being white (P /=20 years (P=.05), barrier contraceptive usage (P=.008), and lower frequency of bacterial vaginosis (P<.001) and gonorrhea (P=.03). L. crispatus and L. jensenii, not L. acidophilus, are the most common species of vaginal lactobacilli.
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              Adherent biofilms in bacterial vaginosis.

              Bacterial vaginosis is a common infectious disorder. Although known since ancient times, little progress has occurred in identifying causal factors. Our aims were to study the bacterial community structure and the spatial organization of microbiota on the epithelial surfaces of vaginal biopsy specimens. We investigated the composition and spatial organization of bacteria associated with the vaginal epithelium in biopsy specimens from 20 patients with bacterial vaginosis and 40 normal premenopausal and postmenopausal controls using a broad range of fluorescent bacterial group-specific rRNA-targeted oligonucleotide probes. Bacterial vaginosis was associated with greater occurrence and higher concentrations of a variety of bacterial groups. However, only Gardnerella vaginalis developed a characteristic adherent biofilm that was specific for bacterial vaginosis. A biofilm comprised of confluent G vaginalis with other bacterial groups incorporated in the adherent layer is a prominent feature of bacterial vaginosis. II-2.
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                Author and article information

                Contributors
                bresh006@umn.edu
                VEdwards@som.umaryland.edu
                jravel@som.umaryland.edu
                peter377@umn.edu
                Journal
                BMC Microbiol
                BMC Microbiol
                BMC Microbiology
                BioMed Central (London )
                1471-2180
                9 December 2015
                9 December 2015
                2015
                : 15
                Affiliations
                [ ]Department of Experimental and Clinical Pharmacology, College of Pharmacy, University of Minnesota, 4-442 McGuire Translational Research Facility, 2001 6th St. SE, Minneapolis, MN 55455 USA
                [ ]Institute for Genome Sciences, University of Maryland, School of Medicine, Bio Park II, 6th Floor, 801 West Baltimore St., Baltimore, MD 21201 USA
                Article
                608
                10.1186/s12866-015-0608-0
                4675025
                © Breshears et al. 2015

                Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

                Funding
                Funded by: FundRef http://dx.doi.org/10.13039/100007249, University of Minnesota (US);
                Award ID: 22928
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/100000060, National Institute of Allergy and Infectious Diseases (US);
                Award ID: U19AI084044
                Award Recipient :
                Categories
                Research Article
                Custom metadata
                © The Author(s) 2015

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