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Investigating the impact of condomless vaginal intercourse and lubricant use on the vaginal metabolome: a pre-post observational study
  1. Joanna-Lynn C Borgogna1,2,
  2. Savannah G Grace2,
  3. Johanna B Holm3,
  4. Tadeo Aviles Zuniga1,
  5. Herlin Kadriu1,2,
  6. Xin He4,
  7. Sarah R McCoski2,
  8. Jacques Ravel3,5,
  9. Rebecca M Brotman5,6,
  10. Carl J Yeoman1,2
  1. 1Department of Microbiology and Cell Biology, Montana State University, Bozeman, Montana, USA
  2. 2Department of Animal and Range Sciences, Montana State University, Bozeman, Montana, USA
  3. 3Department of Microbiology and Immunology, University of Maryland School of Medicine, Baltimore, Maryland, USA
  4. 4Department of Epidemiology and Biostatistics, University of Maryland School of Public Health, College Park, Maryland, USA
  5. 5Institute for Genome Sciences, University of Maryland School of Medicine, Baltimore, Maryland, USA
  6. 6Department of Epidemiology and Public Health, University of Maryland School of Medicine, Baltimore, Maryland, USA
  1. Correspondence to Carl J Yeoman, Department of Animal & Range Sciences, Montana State University Bozeman, Bozeman, Montana 59717, USA; carl.yeoman{at}montana.edu

Abstract

Objective The vaginal metabolome is a significant factor in the vaginal microenvironment, and data are emerging on its independent role in urogenital health. Condomless vaginal intercourse and personal lubricant use are common practices that may affect the vaginal metabolome. The aim of the present study is to describe the associations between condomless intercourse and lubricant use on the vaginal metabolome.

Methods This study used archived mid-vaginal swabs from a 10-week observational cohort of reproductive age women who self-collected samples and recorded behavioural diaries daily. Cases and controls were defined as participants who self-reported condomless vaginal intercourse with or without lubricant use, respectively. Samples were drawn prior to and following condomless vaginal intercourse. Twenty-two case participants were race/ethnicity matched to 22 control participants. Mid-vaginal swabs were subjected to 16S rRNA gene amplicon sequencing and untargeted ultrahigh performance liquid chromatography tandem mass spectroscopy metabolomics. Bayesian mixed-effects regression (unadjusted and adjusted for the vaginal microbiota) was used to evaluate differences in metabolite concentration associated with vaginal intercourse and lubricant use.

Results Both condomless penile–vaginal intercourse and lubricant use were independently associated with higher (up to 8.3-fold) concentrations of metabolites indicative of epithelial damage (eg, sarcosine) and many host-produced antioxidants. Lubricant use was significantly associated with increases in lipids related to cellular damage, host-produced sphingolipids (antimicrobials), antioxidants and salicylate, a cooling agent common to lubricants, in a study design which controls for the independent effect of intercourse. Metabolites involved in oxidative stress and salicylate were strongly correlated with several molecular bacterial vaginosis-associated bacteria.

Conclusions This study provides important foundational data on how condomless vaginal–penile intercourse and lubricant use affect the vaginal metabolome and may affect the protective mechanisms in the vaginal microenvironment.

  • CONDOMS
  • MOLECULAR BIOLOGY
  • Sexual Behavior

Data availability statement

All data relevant to the study are included in the article or uploaded as supplementary information. Fold changes and 95% credible intervals from Bayesian regression are included as online supplemental data 1. The Enzyme Commission (EC) numbers used to identify microbial biosynthetic pathways in VIRGO and human biosynthetic pathways in BRENDA or KEGG are available as a supplemental dataset (online supplemental data 2). The metabolite dataset and participant characteristics used and/or analysed during the current study are included as a supplemental dataset (online supplemental data 3). The sequence data are available in SRA under BioProject accession number PRJNA208535.

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Data availability statement

All data relevant to the study are included in the article or uploaded as supplementary information. Fold changes and 95% credible intervals from Bayesian regression are included as online supplemental data 1. The Enzyme Commission (EC) numbers used to identify microbial biosynthetic pathways in VIRGO and human biosynthetic pathways in BRENDA or KEGG are available as a supplemental dataset (online supplemental data 2). The metabolite dataset and participant characteristics used and/or analysed during the current study are included as a supplemental dataset (online supplemental data 3). The sequence data are available in SRA under BioProject accession number PRJNA208535.

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Footnotes

  • Handling editor Nigel Field

  • Contributors RMB conceived the study. J-LCB, SGG, HK, TAZ and CJY conducted the statistical analysis; J-LCB and JBH performed VIRGO analyses. J-LCB, RMB, XH, SRM and CJY advised on statistical analysis and interpretation of results. J-LCB, SRM and CJY wrote the main manuscript. J-LCB, SRM, SGG, HK, CJY, JBH, XH, RMB and JR contributed to data interpretation, drafting and reviewing the paper. All authors read and approved the final manuscript. CJY is the acting guarantor.

  • Funding This research was supported by the National Institutes of Health's (NIH) National Institutes of General Medical Sciences (https://www.nigms.nih.gov/) and the National Institute for Allergy & Infectious Disease (https://www.niaid.nih.gov/) under award numbers UH-2AI083264 (JR), K01-AI080974 (RMB), R01-AI119012 (RMB) and P20GM103474 (CJY), and by the Montana Agricultural Experiment Station (https://agresearch.montana.edu/maes.html) under award numbers MONB00113 (CJY). The sponsors played no role in the study design, and the content is solely the responsibility of the authors and does not necessarily represent the official views of the NIH.

  • Competing interests JR is the cofounder of LUCA Biologics, a biotechnology company focusing on translating microbiome research into live biotherapeutics drugs for women’s health. All remaining authors have no disclosures to declare.

  • Provenance and peer review Not commissioned; externally peer reviewed.

  • Supplemental material This content has been supplied by the author(s). It has not been vetted by BMJ Publishing Group Limited (BMJ) and may not have been peer-reviewed. Any opinions or recommendations discussed are solely those of the author(s) and are not endorsed by BMJ. BMJ disclaims all liability and responsibility arising from any reliance placed on the content. Where the content includes any translated material, BMJ does not warrant the accuracy and reliability of the translations (including but not limited to local regulations, clinical guidelines, terminology, drug names and drug dosages), and is not responsible for any error and/or omissions arising from translation and adaptation or otherwise.