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      Free Glycogen in Vaginal Fluids Is Associated with Lactobacillus Colonization and Low Vaginal pH

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          Abstract

          Objective

          Lactobacillus dominates the lower genital tract microbiota of many women, producing a low vaginal pH, and is important for healthy pregnancy outcomes and protection against several sexually transmitted pathogens. Yet, factors that promote Lactobacillus remain poorly understood. We hypothesized that the amount of free glycogen in the lumen of the lower genital tract is an important determinant of Lactobacillus colonization and a low vaginal pH.

          Methods

          Free glycogen in lavage samples was quantified. Pyrosequencing of the 16S rRNA gene was used to identify microbiota from 21 African American women collected over 8–11 years.

          Results

          Free glycogen levels varied greatly between women and even in the same woman. Samples with the highest free glycogen had a corresponding median genital pH that was significantly lower (pH 4.4) than those with low glycogen (pH 5.8; p<0.001). The fraction of the microbiota consisting of Lactobacillus was highest in samples with high glycogen versus those with low glycogen (median = 0.97 vs. 0.05, p<0.001). In multivariable analysis, having 1 vs. 0 male sexual partner in the past 6 months was negatively associated, while BMI ≥30 was positively associated with glycogen. High concentrations of glycogen corresponded to higher levels of L. crispatus and L. jensenii, but not L. iners.

          Conclusion

          These findings show that free glycogen in genital fluid is associated with a genital microbiota dominated by Lactobacillus, suggesting glycogen is important for maintaining genital health. Treatments aimed at increasing genital free glycogen might impact Lactobacillus colonization.

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          Most cited references46

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          Nonspecific vaginitis. Diagnostic criteria and microbial and epidemiologic associations.

          Numerous previous studies of nonspecific vaginitis have yielded contradictory results regarding its cause and clinical manifestations, due to a lack of uniform case definition and laboratory methods. We studied 397 consecutive unselected female university students and applied sets of well defined criteria to distinguish nonspecific vaginitis from other forms of vaginitis and from normal findings. Using such criteria, we diagnosed nonspecific vaginitis in up to 25 percent of our study population; asymptomatic disease was recognized in more than 50 percent of those with nonspecific vaginitis. A clinical diagnosis of nonspecific vaginitis, based on simple office procedures, was correlated with both the presence and the concentration of Gardnerella vaginalis (Hemophilus vaginalis) in vaginal discharge, and with characteristic biochemical findings in vaginal discharge. Nonspecific vaginitis was also correlated with a history of sexual activity, a history of previous trichomoniasis, current use of nonbarrier contraceptive methods, and, particularly, use of an intrauterine device. G. vaginalis was isolated from 51.3 percent of the total population using a highly selective medium that detected the organism in lower concentration in vaginal discharge than did previously used media. Practical diagnostic criteria for standard clinical use are proposed. Application of such criteria should assist in clinical management of nonspecific vaginitis and in further study of the microbiologic and biochemical correlates and the pathogenesis of this mild but quite prevalent disease.
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            Vaginal microbiome: rethinking health and disease.

            Vaginal microbiota form a mutually beneficial relationship with their host and have a major impact on health and disease. In recent years our understanding of vaginal bacterial community composition and structure has significantly broadened as a result of investigators using cultivation-independent methods based on the analysis of 16S ribosomal RNA (rRNA) gene sequences. In asymptomatic, otherwise healthy women, several kinds of vaginal microbiota exist, the majority often dominated by species of Lactobacillus, while others are composed of a diverse array of anaerobic microorganisms. Bacterial vaginosis is the most common vaginal condition and is vaguely characterized as the disruption of the equilibrium of the normal vaginal microbiota. A better understanding of normal and healthy vaginal ecosystems that is based on their true function and not simply on their composition would help better define health and further improve disease diagnostics as well as the development of more personalized regimens to promote health and treat diseases.
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              The role of sexually transmitted diseases in HIV transmission.

              More than 42 million people worldwide are now infected with HIV, in spite of sustained prevention activities. Although the spread of HIV has been primarily sexual, epidemiological studies have indicated that the efficiency of the spread of HIV is poor, perhaps as infrequently as 1 in every 1,000 episodes of sexual intercourse. However, sexually transmitted diseases (STDs) that cause ulcers or inflammation greatly increase the efficiency of HIV transmission--by increasing both the infectiousness of, and the susceptibility to HIV infection. STDs might be particularly important in the early stages of a localized HIV epidemic, when people with risky sexual behaviour are most likely to become infected. In China, eastern Europe and Russia, there has been a remarkable increase in the incidence of STDs in recent years, and this is reflected in the rapid increase in the spread of HIV in these areas. Targeted STD detection and treatment should have a central role in HIV prevention in these emerging epidemics.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, USA )
                1932-6203
                2014
                17 July 2014
                : 9
                : 7
                : e102467
                Affiliations
                [1 ]Department of Immunology/Microbiology, Rush University, Chicago, Illinois, United States of America
                [2 ]The CORE Center, Cook County Health & Hospital System, Chicago, Illinois, United States of America
                [3 ]Institute for Genome Sciences, University of Maryland School of Medicine, Baltimore, Maryland, United States of America
                Fred Hutchinson Cancer Center, United States of America
                Author notes

                Competing Interests: The authors have declared that no competing interests exist.

                Conceived and designed the experiments: PM GTS. Performed the experiments: DG DB JR. Analyzed the data: PM ALH KMW JR AL GTS. Contributed reagents/materials/analysis tools: KMW MC JR. Contributed to the writing of the manuscript: PM ALH KMW JR GTS.

                Article
                PONE-D-14-16136
                10.1371/journal.pone.0102467
                4102502
                25033265
                f75aacd6-2f3d-4999-8732-8c1c536e61ca
                Copyright @ 2014

                This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                : 15 April 2014
                : 17 June 2014
                Page count
                Pages: 11
                Funding
                National Institutes of Health ( http://www.nih.gov/) P01 AI082971 and P30 AI 082151 (PI: GTS). National Institute of Allergy and Infectious Diseases (NIAID) ( http://www.niaid.nih.gov/Pages/default.aspx) UO1-AI-34994 (PI: MC) and National Cancer Institute ( http://www.cancer.gov/) and the National Institute on Drug Abuse ( http://www.drugabuse.gov/). This Women's Interagency HIV Study (WIHS at http://statepiaps.jhsph.edu/wihs/) substudy was funded by an American Recovery and Reinvestment Act (ARRA) NIAID supplement to the Chicago WIHS (ARRA PI: GTS). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Medicine and health sciences
                Infectious diseases
                Viral diseases
                HIV infections
                Sexually Transmitted Diseases
                Women's Health
                Obstetrics and Gynecology
                Gynecologic Infections
                Maternal Health
                Custom metadata
                The authors confirm that all data underlying the findings are fully available without restriction. All relevant data are within the paper and its Supporting Information files.

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