Browsing by Author "Brotman, Rebecca M."

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Biogenic Amines Increase the Odds of Bacterial Vaginosis and Affect the Growth of and Lactic Acid Production by Vaginal Lactobacillus spp.
(American Society for Microbiology, 2021-04) Borgogna, Joanna-Lynn C.; Shardell, Michelle D.; Grace, Savannah G.; Santori, Elisa K.; Americus, Benjamin; Li, Zhong; Ulanov, Alexander; Forney, Larry; Nelson, Tiffanie M.; Brotman, Rebecca M.; Ravel, Jacques; Yeoman, Carl J.
Bacterial vaginosis (BV) is the most common vaginal disorder of reproductive-aged women, yet its etiology remains enigmatic. One clinical symptom of BV, malodor, is linked to the microbial production of biogenic amines (BA). Using targeted liquid chromatography mass spectrometry, we analyzed 149 longitudinally collected vaginal samples to determine the in vivo concentrations of the most common BAs and then assessed their relationship to BV and effect upon the growth kinetics of axenically cultured vaginal Lactobacillus species. Increases in cadaverine, putrescine, and tyramine were associated with greater odds of women transitioning from L. crispatus-dominated vaginal microbiota to microbiota that have a paucity of Lactobacillus spp. and from Nugent scores of 0 to 3 to Nugent scores of 7 to 10, consistent with BV. Exposure to putrescine lengthened the lag time and/or slowed the growth of all vaginal Lactobacillus spp. except L. jensenii 62G. L. iners AB107’s lag time was lengthened by cadaverine but reduced in the presence of spermidine and spermine. The growth rate of L. crispatus VPI 3199 was slowed by cadaverine and tyramine, and strain-specific responses to spermine and spermidine were observed. BAs were associated with reduced production of d- and l-lactic acid by vaginal Lactobacillus spp., and this effect was independent of their effect upon Lactobacillus species growth. The exceptions were higher levels of d- and l-lactic acid by two strains of L. crispatus when grown in the presence of spermine. Results of this study provide evidence of a direct impact of common biogenic amines on vaginal Lactobacillus spp.
Cigarette smoking is associated with an altered vaginal tract metabolomic profile
(2018-01) Nelson, Tiffanie M.; Borgogna, Joanna-Lynn C.; Michalek, R. D.; Roberts, David W.; Rath, J. M.; Glover, E. D.; Ravel, Jacques; Shardell, M. D.; Yeoman, Carl J.; Brotman, Rebecca M.
Cigarette smoking has been associated with both the diagnosis of bacterial vaginosis (BV) and a vaginal microbiota lacking protective Lactobacillus spp. As the mechanism linking smoking with vaginal microbiota and BV is unclear, we sought to compare the vaginal metabolomes of smokers and non-smokers (17 smokers/19 non-smokers). Metabolomic profiles were determined by gas and liquid chromatography mass spectrometry in a cross-sectional study. Analysis of the 16S rRNA gene populations revealed samples clustered into three community state types (CSTs) ---- CST-I (L. crispatus-dominated), CST-III (L. iners-dominated) or CST-IV (low-Lactobacillus). We identified 607 metabolites, including 12 that differed significantly (q-value < 0.05) between smokers and non-smokers. Nicotine, and the breakdown metabolites cotinine and hydroxycotinine were substantially higher in smokers, as expected. Among women categorized to CST-IV, biogenic amines, including agmatine, cadaverine, putrescine, tryptamine and tyramine were substantially higher in smokers, while dipeptides were lower in smokers. These biogenic amines are known to affect the virulence of infective pathogens and contribute to vaginal malodor. Our data suggest that cigarette smoking is associated with differences in important vaginal metabolites, and women who smoke, and particularly women who are also depauperate for Lactobacillus spp., may have increased susceptibilities to urogenital infections and increased malodor.
Perceived Stress and Molecular-BV in the NIH Longitudinal Study of Vaginal Flora
(Oxford University Press, 2021-05) Turpin, Rodman; Slopen, Natalie; Borgogna, Joanna C.; Yeoman, Carl J.; He, Xin; Miller, Ryan S.; Klebanoff, Mark A.; Ravel, Jacques; Brotman, Rebecca M.
Vaginal microbiota provide the first line of defense against urogenital infections primarily through protective actions of Lactobacillus spp. Perceived stress increases susceptibility to infection through several mechanisms, including suppression of immune function. We investigated if stress was associated with deleterious changes to vaginal bacterial composition in a subsample of 572 women in the Longitudinal Study of Vaginal Flora, sampled from 1999 through 2002. Using Cox proportional-hazard models, both unadjusted and adjusted for sociodemographics and sexual behaviors, participants who exhibited a 5 unit-increase in Cohen’s perceived stress scale had greater risk (aHR=1.40, 95% CI 1.13-1.74) of developing molecular bacterial vaginosis (BV), a state with low Lactobacillus abundance and diverse anaerobic bacteria. A 5-unit stress increase was also associated with greater risks for transitioning from the L. iners-dominated community state type (26% higher) to molecular-BV (aHR=1.26, 95% CI 1.01-1.56) or maintaining molecular-BV from baseline (aHR=1.23, 95% CI 1.01-1.47). Inversely, women with baseline molecular-BV reporting a 5-unit stress increase were less likely to transition to microbiota dominated by L. crispatus, L. gasseri, or L. jensenii (aHR=0.81, 95% CI 0.68-0.99). These findings suggest psychosocial stress is associated with vaginal microbiota composition, inviting a more mechanistic exploration of the relationship between psychosocial stress and molecular-BV.
Vaginal biogenic amines: biomarkers of bacterial vaginosis or precursors to vaginal dysbiosis?
(2015-09) Nelson, Tiffanie M.; Borgogna, Joanna-Lynn C.; Brotman, Rebecca M.; Ravel, Jacques; Walk, Seth T.; Yeoman, Carl J.
Bacterial vaginosis (BV) is the most common vaginal disorder among reproductive age women. One clinical indicator of BV is a â€œfishyâ€ odor. This odor has been associated with increases in several biogenic amines (BAs) that may serve as important biomarkers. Within the vagina, BA production has been linked to various vaginal taxa, yet their genetic capability to synthesize BAs is unknown. Using a bioinformatics approach, we show that relatively few vaginal taxa are predicted to be capable of producing BAs. Many of these taxa (Dialister, Prevotella, Parvimonas, Megasphaera, Peptostreptococcus, and Veillonella spp.) are more abundant in the vaginal microbial community state type (CST) IV, which is depleted in lactobacilli. Several of the major Lactobacillus species (L. crispatus, L. jensenii, and L. gasseri) were identified as possessing gene sequences for proteins predicted to be capable of putrescine production. Finally, we show in a small cross sectional study of 37 women that the BAs putrescine, cadaverine and tyramine are significantly higher in CST IV over CSTs I and III. These data support the hypothesis that BA production is conducted by few vaginal taxa and may be important to the outgrowth of BV-associated (vaginal dysbiosis) vaginal bacteria.
Vaginal microbiota of American Indian women and associations with measures of psychosocial stress
(Public Library of Science, 2021-12) Borgogna, Joanna-Lynn C.; Anastario, Michael; Firemoon, Paula; Rink, Elizabeth; Ricker, Adriann; Ravel, Jacques; Brotman, Rebecca M.; Yeoman, Carl J.
Molecular-bacterial vaginosis (BV) is characterized by low levels of vaginal Lactobacillus species and is associated with higher risk of sexually transmitted infections (STI). Perceived psychosocial stress is associated with increased severity and persistence of infections, including STIs. American Indians have the highest rates of stress and high rates of STIs. The prevalence of molecular-BV among American Indian women is unknown. We sought to evaluate measures of psychosocial stress, such as historic loss (a multigenerational factor involving slavery, forced removal from one’s land, legally ratified race-based segregation, and contemporary discrimination) and their association with the vaginal microbiota and specific metabolites associated with BV, in 70 Northwestern Plains American Indian women. Demographics, perceived psychosocial stressors, sexual practices, and known BV risk factors were assessed using a modified version of the American Indian Service Utilization, Psychiatric Epidemiology, Risk and Protective Factors Project survey. Self-collected mid-vaginal swabs were profiled for bacterial composition by 16S rRNA gene amplicon sequencing and metabolites quantified by targeted liquid-chromatography mass spectrometry. Sixty-six percent of the participants were classified as having molecular-BV, with the rest being either dominated by L. crispatus (10%) or L. iners (24%). High levels of lifetime trauma were associated with higher odds of having molecular-BV (adjusted Odds Ratio (aOR): 2.5, 95% Credible Interval (CrI): 1.1–5.3). Measures of psychosocial stress, including historic loss and historic loss associated symptoms, were significantly associated with lifestyle and behavioral practices. Higher scores of lifetime trauma were associated with increased concentrations of spermine (aFC: 3.3, 95% CrI: 1.2–9.2). Historic loss associated symptoms and biogenic amines were the major correlates of molecular-BV. Historical loss associated symptoms and lifetime trauma are potentially important underlying factors associated with BV.