The Application of Molecular Methods Towards an Understanding of the Role of the Vaginal Microbiome in Health and Disease

Borgogna, Joanna-Lynn C.; Yeoman, Carl J.

doi:10.1016/bs.mim.2017.08.003

Cited by 8 publications

(8 citation statements)

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“…We have previously hypothesized that the biosynthesis of BAs within the vagina reduces Lactobacillus species-mediated protection and alters the microenvironment sufficiently to enable colonization by a diverse set of anaerobic bacterial species, as observed in molecular-BV (1,3,5,32,53). We examined this hypothesis in the context of both an observational cohort study and in vitro experimentation to examine the direct influence of BAs on Lactobacillus species growth properties and lactic acid production.…”

Section: Discussionmentioning

confidence: 99%

Biogenic Amines Increase the Odds of Bacterial Vaginosis and Affect the Growth of and Lactic Acid Production by Vaginal Lactobacillus spp.

Borgogna

Shardell

Grace

et al. 2021

Appl Environ Microbiol

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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 0-3 to Nugent scores of 7-10, 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 spp. 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. Importance: Lactobacillus spp. are credited with providing the primary defense against gynecological conditions, including BV, most notably through the acidification of the vaginal microenvironment which results from their production of lactic acid. The microbial production of BAs has been hypothesized to play a mechanistic role in diminishing Lactobacillus spp.-mediated protection, enabling the colonization and outgrowth of diverse anaerobic bacterial species associated with BV. Herein, we demonstrate that in vivo increases in the most commonly observed BAs are associated with a loss of Lactobacillus spp. and the development of BV, measured by Nugent score. Further, we show that BAs formed by amino acid decarboxylase enzymes negatively affect the growth of type-strains of the most common vaginal Lactobacillus spp. and separately alter their production of lactic acid. These results suggest that BAs destabilize vaginal Lactobacillus spp. and may play an important and direct role in diminishing their protection of the vaginal microenvironment.

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Section: Discussionmentioning

confidence: 99%

Biogenic Amines Increase the Odds of Bacterial Vaginosis and Affect the Growth of and Lactic Acid Production by Vaginal Lactobacillus spp.

Borgogna

Shardell

Grace

et al. 2021

Appl Environ Microbiol

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“…Previous studies have shown that antibody response to PRRS virus following PRRS infection is associated with reproductive outcomes during natural PRRS infection 7,8 . In addition, a relationship between the microbiota and immune response has been observed 5 . We, therefore, hypothesized that microbiota collected after MLV PRRS vaccination may be an alternative indicator of reproductive performance in commercial sows.…”

Section: Discussionmentioning

confidence: 99%

“…In beef cattle, the vaginal microbiota was used to distinguish between heifers that were able to establish pregnancy from those that were not 2 , suggesting its potential to be used to identify animals with favorable reproductive performance. In addition, relationships between the microbiota and immune response have been previously observed 5 . Therefore, microbiota collected after modified live virus (MVL) porcine reproductive and respiratory syndrome (PRRS) vaccination may be an alternative indicator of reproductive performance in commercial sows.…”

mentioning

confidence: 95%

Vaginal microbiota diverges in sows with low and high reproductive performance after porcine reproductive and respiratory syndrome vaccination

Sanglard

Schmitz‐Esser

Gray³

et al. 2020

Sci Rep

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previous studies have demonstrated evidence for a relationship between the vaginal microbiome and reproductive performance, suggesting the vaginal microbiota may serve as a tool to predict farrowing outcomes in commercial pigs. in this study, we compared the vaginal microbiome in sows with low and high farrowing performance and used it to classify animals with contrasting reproductive outcomes in commercial sows following immune challenge with porcine respiratory and reproductive syndrome (PRRS) vaccination. Eighteen microbes were differentially abundant (q-value < 0.05) between the Low and High farrowing performance groups. Among them, Campylobacter, Bacteroides, Porphyromonas, Lachnospiraceae unclassified, Prevotella, and Phascolarctobacterium were also selected in the discriminant and linear regression analyses, and could be used as potential biomarkers for reproductive outcomes. The correct classification rate in the two groups was 100%. In conclusion, this study demonstrates that vaginal microbiota collected after pRRS vaccination could be potentially used to classify sows into having low or high farrowing performance in commercial herds.

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“…CST IV is characterised by a paucity in Lactobacillus , high vaginal pH (>4.5), and high relative abundances of various anaerobic bacteria, including Gardnerella, Prevotella , and Atopobium spp . These microbial features are also characteristic of bacterial vaginosis (BV), which can be associated with a myriad of symptoms and adverse health outcomes, leading to the proposal of CST IV being termed ‘molecular‐BV’ …”

Section: Introductionmentioning

confidence: 99%

The vaginal metabolome and microbiota of cervical HPV‐positive and HPV‐negative women: a cross‐sectional analysis

Borgogna

Shardell

Santori

et al. 2019

BJOG

109

105

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Objective Characterise the vaginal metabolome of cervical HPVinfected and uninfected women.Design Cross-sectional.Sample Thirty-nine participants, 13 categorised as HPV-negative and 26 as HPV-positive (any genotype; HPV + ), 14 of whom were positive with at least one high-risk HPV strain (hrHPV).Method Self-collected mid-vaginal swabs were profiled for bacterial composition by 16S rRNA gene amplicon sequencing, metabolites by both gas and liquid chromatography mass spectrometry, and 37 types of HPV DNA. Main outcome measures Metabolite abundances.Results Vaginal microbiota clustered into Community State Type (CST) I (Lactobacillus crispatus-dominated), CST III (Lactobacillus iners-dominated), and CST IV (low-Lactobacillus, 'molecular-BV'). HPV + women had higher biogenic amine and phospholipid concentrations compared with HPVwomen after adjustment for CST and cigarette smoking. Metabolomic profiles of HPV + and HPV À women differed in strata of CST. In CST III, there were higher concentrations of biogenic amines and glycogen-related metabolites in HPV + women than in HPVwomen. In CST IV, there were lower concentrations of glutathione, glycogen, and phospholipid-related metabolites in HPV + participants than in HPVparticipants. Across all CSTs, women with hrHPV strains had lower concentrations of amino acids, lipids, and peptides compared with women who had only low-risk HPV (lrHPV). ConclusionsThe vaginal metabolome of HPV + women differed from HPV À women in terms of several metabolites, including biogenic amines, glutathione, and lipid-related metabolites. If the temporal relation between increased levels of reduced glutathione and oxidised glutathione and HPV incidence/persistence is confirmed in future studies, anti-oxidant therapies may be considered as a non-surgical HPV control intervention. Keywords 16S rRNA gene amplicon sequencing, human papillomavirus, vaginal metabolome, vaginal microbiota. Tweetable abstract Metabolomics study: Vaginal microenvironment of HPV + women may be informative for nonsurgical interventions. Please cite this paper as: Borgogna JC, Shardell MD, Santori EK, Nelson TM, Rath JM, Glover ED, Ravel J, Gravitt PE, Yeoman CJ, Brotman RM. The vaginal metabolome and microbiota of cervical HPV-positive and HPV-negative women: a cross-sectional analysis.

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The Application of Molecular Methods Towards an Understanding of the Role of the Vaginal Microbiome in Health and Disease

Cited by 8 publications

References 293 publications

Biogenic Amines Increase the Odds of Bacterial Vaginosis and Affect the Growth of and Lactic Acid Production by Vaginal Lactobacillus spp.

Biogenic Amines Increase the Odds of Bacterial Vaginosis and Affect the Growth of and Lactic Acid Production by Vaginal Lactobacillus spp.

Vaginal microbiota diverges in sows with low and high reproductive performance after porcine reproductive and respiratory syndrome vaccination

The vaginal metabolome and microbiota of cervical HPV‐positive and HPV‐negative women: a cross‐sectional analysis

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