{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,6,2]],"date-time":"2026-06-02T08:22:56Z","timestamp":1780388576713,"version":"3.54.1"},"reference-count":40,"publisher":"MDPI AG","issue":"22","license":[{"start":{"date-parts":[[2021,11,13]],"date-time":"2021-11-13T00:00:00Z","timestamp":1636761600000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100003141","name":"Consejo Nacional de Ciencia y Tecnolog\u00eda","doi-asserted-by":"publisher","award":["692895"],"award-info":[{"award-number":["692895"]}],"id":[{"id":"10.13039\/501100003141","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["IJMS"],"abstract":"<jats:p>Vaginal malodour is a sign of dysbiosis. The biogenic amines (BAs) cadaverine, putrescine and tyramine are known to be causative compounds. Recent reports suggest these compounds produced by pathogens might have a role beyond causing malodour; namely inhibiting the growth of lactobacilli bacteria that are crucial in the maintenance of vaginal homeostasis. The aim of this study was to identify whether certain lactobacilli strains could reduce BAs and to evaluate how Lactobacillus species were affected by these compounds. Using LC\u2013MS and HPLC-UV, five Lactobacillus crispatus strains were identified as being capable of significantly reducing BAs from the media under in vitro conditions. Through 16S rRNA gene sequencing of vaginal swabs exposed to Bas, cadaverine was found to reduce the relative abundance of lactobacilli. When L. crispatus was exposed to media supplemented with BAs with an HCl adjusted lower pH, its growth was enhanced, demonstrating the relevance of the maintenance of an acidic vaginal environment. If strains are to be developed for probiotic application to alleviate bacterial vaginosis and other conditions affecting large numbers of women worldwide, their ability to adapt to Bas and regulate pH should be part of the experimentation.<\/jats:p>","DOI":"10.3390\/ijms222212279","type":"journal-article","created":{"date-parts":[[2021,11,14]],"date-time":"2021-11-14T20:48:36Z","timestamp":1636922916000},"page":"12279","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":8,"title":["The Two-Way Interaction between the Molecules That Cause Vaginal Malodour and Lactobacilli: An Opportunity for Probiotics"],"prefix":"10.3390","volume":"22","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-0276-3373","authenticated-orcid":false,"given":"Scarlett","family":"Puebla-Barragan","sequence":"first","affiliation":[{"name":"Canadian Centre for Human Microbiome and Probiotics, Lawson Health Research Institute, 268 Grosvenor Street, London, ON N6A 4V2, Canada"},{"name":"Departments of Microbiology and Immunology, Surgery, and Biochemistry, Western University, London, ON N6A 4V2, Canada"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-3214-6130","authenticated-orcid":false,"given":"Polycronis Paul","family":"Akouris","sequence":"additional","affiliation":[{"name":"Canadian Centre for Human Microbiome and Probiotics, Lawson Health Research Institute, 268 Grosvenor Street, London, ON N6A 4V2, Canada"},{"name":"Departments of Microbiology and Immunology, Surgery, and Biochemistry, Western University, London, ON N6A 4V2, Canada"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-5905-6581","authenticated-orcid":false,"given":"Kait F.","family":"Al","sequence":"additional","affiliation":[{"name":"Canadian Centre for Human Microbiome and Probiotics, Lawson Health Research Institute, 268 Grosvenor Street, London, ON N6A 4V2, Canada"},{"name":"Departments of Microbiology and Immunology, Surgery, and Biochemistry, Western University, London, ON N6A 4V2, Canada"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-1877-160X","authenticated-orcid":false,"given":"Charles","family":"Carr","sequence":"additional","affiliation":[{"name":"Canadian Centre for Human Microbiome and Probiotics, Lawson Health Research Institute, 268 Grosvenor Street, London, ON N6A 4V2, Canada"},{"name":"Departments of Microbiology and Immunology, Surgery, and Biochemistry, Western University, London, ON N6A 4V2, Canada"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Britney","family":"Lamb","sequence":"additional","affiliation":[{"name":"Canadian Centre for Human Microbiome and Probiotics, Lawson Health Research Institute, 268 Grosvenor Street, London, ON N6A 4V2, Canada"},{"name":"Departments of Microbiology and Immunology, Surgery, and Biochemistry, Western University, London, ON N6A 4V2, Canada"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-0977-1656","authenticated-orcid":false,"given":"Mark","family":"Sumarah","sequence":"additional","affiliation":[{"name":"Agriculture and Agri-Food Canada, London, ON N5V 4T3, Canada"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Charlotte","family":"van der Veer","sequence":"additional","affiliation":[{"name":"Department of Infectious Diseases, Public Health Service (GGD), Nieuwe Achtergracht 100, 1018 WT Amsterdam, The Netherlands"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-3674-598X","authenticated-orcid":false,"given":"Remco","family":"Kort","sequence":"additional","affiliation":[{"name":"Department of Molecular Cell Biology, Faculty of Science, O2 Lab Building, Vrije Universiteit Amsterdam, De Boelelaan 1108, 1081 HZ Amsterdam, The Netherlands"},{"name":"ARTIS-Micropia, Plantage Kerklaan 38-40, 1018 CZ Amsterdam, The Netherlands"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-3591-6436","authenticated-orcid":false,"given":"Jeremy","family":"Burton","sequence":"additional","affiliation":[{"name":"Canadian Centre for Human Microbiome and Probiotics, Lawson Health Research Institute, 268 Grosvenor Street, London, ON N6A 4V2, Canada"},{"name":"Departments of Microbiology and Immunology, Surgery, and Biochemistry, Western University, London, ON N6A 4V2, Canada"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-9658-5696","authenticated-orcid":false,"given":"Gregor","family":"Reid","sequence":"additional","affiliation":[{"name":"Canadian Centre for Human Microbiome and Probiotics, Lawson Health Research Institute, 268 Grosvenor Street, London, ON N6A 4V2, Canada"},{"name":"Departments of Microbiology and Immunology, Surgery, and Biochemistry, Western University, London, ON N6A 4V2, Canada"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2021,11,13]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"14174","DOI":"10.1038\/srep14174","article-title":"A multi-platform metabolomics approach identifies highly specific biomarkers of bacterial diversity in the vagina of pregnant and non-pregnant women","volume":"5","author":"McMillan","year":"2015","journal-title":"Sci. Rep."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"49","DOI":"10.1097\/LGT.0b013e31822b7512","article-title":"Genital malodor in women: A modern reappraisal","volume":"16","author":"Subramanian","year":"2012","journal-title":"J. Low. Genit. Tract Dis."},{"key":"ref_3","unstructured":"FAO\/WHO Working Group (2002). Report of a Joint FAO\/WHO Expert Consultation on Evaluation of Health and Nutrition Properties of Probiotics in Food Including Powder Milk with Live Lactic acid Bacteria, FAO. Available online: http:\/\/www.fao.org\/3\/a0512e\/a0512e.pdf."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"506","DOI":"10.1038\/nrgastro.2014.66","article-title":"The International Scientific Association for Probiotics and Prebiotics consensus statement on the scope and appropriate use of the term probiotic","volume":"11","author":"Hill","year":"2014","journal-title":"Nat. Rev. Gastroenterol. Hepatol."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"747","DOI":"10.1016\/j.tim.2021.03.010","article-title":"Lacticaseibacillus rhamnosus GR-1, a.k.a. Lactobacillus rhamnosus GR-1: Past and future perspectives","volume":"8","author":"Petrova","year":"2021","journal-title":"Trends Microbiol."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"1278","DOI":"10.3389\/fmicb.2018.01278","article-title":"Comparative genomic and phenotypic analysis of the vaginal probiotic Lactobacillus rhamnosus GR-1","volume":"9","author":"Petrova","year":"2018","journal-title":"Front. Microbiol."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"269","DOI":"10.1111\/j.1472-765X.2008.02477.x","article-title":"Improved treatment of vulvovaginal candidiasis with fluconazole plus probiotic Lactobacillus rhamnosus GR-1 and Lactobacillus reuteri RC-14","volume":"48","author":"Martinez","year":"2009","journal-title":"Lett. Appl. Microbiol."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"75","DOI":"10.1016\/j.ejogrb.2012.12.031","article-title":"Efficacy of orally applied probiotic capsules for bacterial vaginosis and other vaginal infections: A double-blind, randomized, placebo-controlled study","volume":"168","author":"Vujic","year":"2013","journal-title":"Eur. J. Obstet. Gynecol. Reprod. Biol."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"449","DOI":"10.1080\/14787210.2017.1300061","article-title":"Probiotic use in an infectious disease setting","volume":"15","author":"Reid","year":"2017","journal-title":"Expert Rev. Anti-Infect. Ther."},{"key":"ref_10","first-page":"27799","article-title":"Changes in vaginal microbiota following antimicrobial and probiotic therapy","volume":"26","author":"Macklaim","year":"2015","journal-title":"Microb. Ecol. Health Dis."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"e03068-20","DOI":"10.1128\/AEM.03068-20","article-title":"Biogenic amines increase the odds of bacterial vaginosis and affect the growth of and lactic acid production by vaginal Lactobacillus spp.","volume":"87","author":"Borgogna","year":"2021","journal-title":"Appl. Environ. Microbiol."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"1","DOI":"10.3389\/fphys.2015.00253","article-title":"Vaginal biogenic amines: Biomarkers of bacterial vaginosis or precursors to vaginal dysbiosis?","volume":"6","author":"Nelson","year":"2015","journal-title":"Front. Physiol."},{"key":"ref_13","doi-asserted-by":"crossref","unstructured":"Puebla-Barragan, S., Watson, E., van der Veer, C., Chmiel, J.A., Carr, C., Burton, J.P., Sumarah, M., Kort, R., and Reid, G. (2021). Interstrain variability of human vaginal lactobacillus crispatus for metabolism of biogenic amines and antimicrobial activity against urogenital pathogens. Molecules, 26.","DOI":"10.3390\/molecules26154538"},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"2772","DOI":"10.1016\/j.micinf.2006.08.008","article-title":"Clinical study comparing probiotic Lactobacillus GR-1 and RC-14 with metronidazole vaginal gel to treat symptomatic bacterial vaginosis","volume":"8","author":"Anukam","year":"2006","journal-title":"Microbes Infect."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"131","DOI":"10.1016\/S0928-8244(02)00465-0","article-title":"Oral use of Lactobacillus rhamnosus GR-1 and L. fermentum RC-14 significantly alters vaginal flora: Randomized, placebo-controlled trial in 64 healthy women","volume":"35","author":"Reid","year":"2003","journal-title":"FEMS Immunol. Med. Microbiol."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"487","DOI":"10.1111\/j.1348-0421.2009.00154.x","article-title":"Effect of Lactobacillus rhamnosus GR-1 and Lactobacillus reuteri RC-14 on the ability of Candida albicans to infect cells and induce inflammation","volume":"53","author":"Martinez","year":"2009","journal-title":"Microbiol. Immunol."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"49","DOI":"10.1111\/j.1574-695X.2001.tb01549.x","article-title":"Oral probiotics can resolve urogenital infections","volume":"30","author":"Reid","year":"2001","journal-title":"FEMS Immunol. Med. Microbiol."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"147","DOI":"10.1111\/j.1574-695X.2012.00994.x","article-title":"Substances released from probiotic Lactobacillus rhamnosus GR-1 potentiate NF-\u039aB activity in Escherichia coli-stimulated urinary bladder cells","volume":"66","author":"Karlsson","year":"2012","journal-title":"FEMS Immunol. Med. Microbiol."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"4874","DOI":"10.1128\/AEM.07724-11","article-title":"Expression of the arginine deiminase pathway genes in Lactobacillus sakei is strain dependent and is affected by the environmental pH","volume":"78","author":"Rimaux","year":"2012","journal-title":"Appl. Environ. Microbiol."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"2239","DOI":"10.1128\/AEM.71.5.2239-2243.2005","article-title":"Relationship between pH and medium dissolved solids in terms of growth and metabolism of lactobacilli and Saccharomyces cerevisiae during ethanol production","volume":"71","author":"Narendranath","year":"2005","journal-title":"Appl. Environ. Microbiol."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"3060","DOI":"10.1128\/AEM.71.6.3060-3067.2005","article-title":"Survival of probiotic lactobacilli in acidic environments is enhanced in the presence of metabolizable sugars","volume":"71","author":"Corcoran","year":"2005","journal-title":"Appl. Environ. Microbiol."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"69","DOI":"10.1016\/j.ijgo.2015.11.018","article-title":"Vaginal fluid pH and buffer capacity for predicting false preterm labor in Japanese women","volume":"134","author":"Noguchi","year":"2016","journal-title":"Int. J. Gynecol. Obstet."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"e02200-17","DOI":"10.1128\/AEM.02200-17","article-title":"Promising prebiotic candidate established by evaluation of lactitol, lactulose, raffinose, and oligofructose for maintenance of a Lactobacillus-dominated vaginal microbiota","volume":"84","author":"Collins","year":"2017","journal-title":"Appl. Environ. Microbiol."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"49","DOI":"10.1186\/s40168-019-0667-9","article-title":"Comparative genomics of human Lactobacillus crispatus isolates reveals genes for glycosylation and glycogen degradation: Implications for in vivo dominance of the vaginal microbiota","volume":"7","author":"Hertzberger","year":"2019","journal-title":"Microbiome"},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"1323","DOI":"10.1128\/jcm.30.5.1323-1326.1992","article-title":"Defined medium simulating genital tract secretions for growth of vaginal microflora","volume":"30","author":"Geshnizgani","year":"1992","journal-title":"J. Clin. Microbiol."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"297","DOI":"10.1128\/jcm.29.2.297-301.1991","article-title":"Reliability of diagnosing bacterial vaginosis is improved by a standardized method of Gram stain interpretation","volume":"29","author":"Nugent","year":"1991","journal-title":"J. Clin. Microbiol."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"170","DOI":"10.1128\/jcm.18.1.170-177.1983","article-title":"Diagnosis of bacterial vaginosis by direct Gram stain of vaginal fluid","volume":"18","author":"Spiegel","year":"1983","journal-title":"J. Clin. Microbiol."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"4026","DOI":"10.1128\/JCM.39.11.4026-4031.2001","article-title":"Analysis of bacterial vaginosis-related amines in vaginal fluid by gas chromatography and mass spectrometry","volume":"39","author":"Wolrath","year":"2001","journal-title":"J. Clin. Microbiol."},{"key":"ref_29","unstructured":"Sprouffske, K. (2021, July 25). Simple Metrics to Summarize Growth Curves. Available online: https:\/\/cran.r-project.org\/package=growthcurver\/index.html."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"184","DOI":"10.1016\/j.aca.2007.11.014","article-title":"Single hollow fiber SLM extraction of polyamines followed by tosyl chloride derivatization and HPLC determination","volume":"606","author":"Dziarkowska","year":"2008","journal-title":"Anal. Chim. Acta"},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"100094","DOI":"10.1016\/j.xcrm.2020.100094","article-title":"Ureteral stent microbiota is associated with patient comorbidities but not antibiotic exposure","volume":"1","author":"Al","year":"2020","journal-title":"Cell Rep. Med."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"1403","DOI":"10.1111\/1462-2920.13023","article-title":"Every base matters: Assessing small subunit rRNA primers for marine microbiomes with mock communities, time series and global field samples","volume":"18","author":"Parada","year":"2016","journal-title":"Environ. Microbiol."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"971","DOI":"10.1080\/10618600.2015.1131161","article-title":"Displaying variation in large datasets: Plotting a visual summary of effect sizes","volume":"25","author":"Gloor","year":"2016","journal-title":"J. Comput. Graph. Stat."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"15","DOI":"10.1186\/2049-2618-2-15","article-title":"Unifying the analysis of high-throughput sequencing datasets: Characterizing RNA-seq, 16S rRNA gene sequencing and selective growth experiments by compositional data analysis","volume":"2","author":"Fernandes","year":"2014","journal-title":"Microbiome"},{"key":"ref_35","doi-asserted-by":"crossref","unstructured":"Fernandes, A.D., Macklaim, J.M., Linn, T.G., Reid, G., and Gloor, G.B. (2013). ANOVA-like differential expression (ALDEx) analysis for mixed population RNA-seq. PLoS ONE, 8.","DOI":"10.1371\/journal.pone.0067019"},{"key":"ref_36","unstructured":"Oksanen, J., Blanchet, G., Friendly, M., Kindt, R., Legendre, P., McGlinn, D., Minchin, P., O\u2019Hara, R., Simpson, G., and Solymos, P. (2021, July 25). Vegan: Community Ecology Package. Available online: http:\/\/cran.r-project.org\/web\/packages\/vegan\/index.html."},{"key":"ref_37","unstructured":"Kassambara, A. (2021, July 25). Rstatix: Pipe-Friendly Framework for Basic Statistical Tests. Available online: http:\/\/cran.r-project.org\/web\/packages\/rstatix\/index.html."},{"key":"ref_38","unstructured":"Lenth, R. (2021, July 25). Emmeans: Estimated Marginal Means, Aka Least-Squares Means. Available online: http:\/\/cran.r-project.org\/web\/packages\/emmeans\/index.html."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"1","DOI":"10.18637\/jss.v011.i10","article-title":"Econometric computing with HC and HAC covariance matrix estimators","volume":"11","author":"Zeileis","year":"2004","journal-title":"J. Stat. Softw."},{"key":"ref_40","doi-asserted-by":"crossref","unstructured":"Wickham, H. (2016). Ggplot2: Elegant Graphics for Data Analysis, Springer.","DOI":"10.1007\/978-3-319-24277-4_9"}],"container-title":["International Journal of Molecular Sciences"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/1422-0067\/22\/22\/12279\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T07:29:47Z","timestamp":1760167787000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/1422-0067\/22\/22\/12279"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2021,11,13]]},"references-count":40,"journal-issue":{"issue":"22","published-online":{"date-parts":[[2021,11]]}},"alternative-id":["ijms222212279"],"URL":"https:\/\/doi.org\/10.3390\/ijms222212279","relation":{},"ISSN":["1422-0067"],"issn-type":[{"value":"1422-0067","type":"electronic"}],"subject":[],"published":{"date-parts":[[2021,11,13]]}}}