{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,11,3]],"date-time":"2026-11-03T00:00:08Z","timestamp":1793664008143,"version":"4.5.1"},"reference-count":57,"publisher":"MDPI AG","issue":"9","license":[{"start":{"date-parts":[[2023,8,25]],"date-time":"2023-08-25T00:00:00Z","timestamp":1692921600000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Medicina"],"abstract":"<jats:p>Contrary to popular belief, we have known for many years that the endometrium is not a sterile environment and is considered to be a low-biomass milieu compared to the vagina. Numerous trials and studies have attempted to establish a valid sampling method and assess its physiological composition, but no consensus has been reached. Many factors, such as ethnicity, age and inflammation, can influence the microbiome. Moreover, it possesses a higher alpha-diversity and, therefore, contains more diverse bacteria than the vagina. For instance, Lactobacillus has been shown to be a predominant genus in the vaginal microbiome of healthy women. Consequently, even if a majority of scientists postulate that a predominance of Lactobacillus inside the uterus improves reproductive outcomes, vaginal contamination by these bacteria during sampling cannot be ruled out. Certain pathologies, such as chronic endometritis, have been identified as inflammation perpetrators that hinder the embryo implantation process. This pro-inflammatory climate created by dysbiosis of the endometrial microbiota could induce secondary inflammatory mediators via Toll-like receptors, creating an environment conducive to the development of endometriosis and even promoting carcinogenesis. However, studies to this day have focused on small populations. In addition, there is no clearly defined healthy uterine composition yet. At most, only a few taxa have been identified as pathogenic. As sampling and analysis methods become increasingly precise, we can expect the endometrial microbiota to be incorporated into future diagnostic tools and treatments for women\u2019s health.<\/jats:p>","DOI":"10.3390\/medicina59091540","type":"journal-article","created":{"date-parts":[[2023,8,25]],"date-time":"2023-08-25T08:33:09Z","timestamp":1692952389000},"page":"1540","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":24,"title":["The Endometrial Microbiota: Challenges and Prospects"],"prefix":"10.3390","volume":"59","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-6199-143X","authenticated-orcid":false,"given":"Pauline","family":"Kaluanga Bwanga","sequence":"first","affiliation":[{"name":"Faculty of Medicine, University of Li\u00e8ge, 4000 Li\u00e8ge, Belgium"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Pierre-Luc","family":"Tremblay-Lemoine","sequence":"additional","affiliation":[{"name":"Department of Obstetrics and Gynecology, CHU of Liege\u2014Citadelle Site, University of Li\u00e8ge, 4000 Li\u00e8ge, Belgium"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Marie","family":"Timmermans","sequence":"additional","affiliation":[{"name":"Department of Obstetrics and Gynecology, CHU of Liege\u2014Citadelle Site, University of Li\u00e8ge, 4000 Li\u00e8ge, Belgium"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"St\u00e9phanie","family":"Ravet","sequence":"additional","affiliation":[{"name":"Center for Reproductive Medicine, University of Li\u00e8ge\u2014Citadelle Site, 4000 Liege, Belgium"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-4952-9637","authenticated-orcid":false,"given":"Carine","family":"Munaut","sequence":"additional","affiliation":[{"name":"Laboratory of Tumor and Development Biology, Giga-Cancer, University of Li\u00e8ge, 4000 Li\u00e8ge, Belgium"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Michelle","family":"Nisolle","sequence":"additional","affiliation":[{"name":"Department of Obstetrics and Gynecology, CHU of Liege\u2014Citadelle Site, University of Li\u00e8ge, 4000 Li\u00e8ge, Belgium"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-6162-1551","authenticated-orcid":false,"given":"Laurie","family":"Henry","sequence":"additional","affiliation":[{"name":"Department of Obstetrics and Gynecology, CHU of Liege\u2014Citadelle Site, University of Li\u00e8ge, 4000 Li\u00e8ge, Belgium"},{"name":"Center for Reproductive Medicine, University of Li\u00e8ge\u2014Citadelle Site, 4000 Liege, Belgium"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2023,8,25]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"S38","DOI":"10.1111\/j.1753-4887.2012.00493.x","article-title":"Defining the human microbiome","volume":"70","author":"Ursell","year":"2012","journal-title":"Nutr. Rev."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"1108","DOI":"10.1136\/gutjnl-2018-317503","article-title":"Role of the microbiome in human development","volume":"68","author":"Knight","year":"2019","journal-title":"Gut"},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"208","DOI":"10.3389\/fimmu.2018.00208","article-title":"Uterine Microbiota: Residents, Tourists, or Invaders?","volume":"9","author":"Baker","year":"2018","journal-title":"Front. Immunol."},{"key":"ref_4","first-page":"1","article-title":"The microbiota continuum along the female reproductive tract and its relation to uterine-related diseases","volume":"8","author":"Chen","year":"2017","journal-title":"Nat. Commun."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"8467","DOI":"10.1038\/s41598-022-12095-7","article-title":"Endometrial microbiome: Sampling, assessment, and possible impact on embryo implantation","volume":"12","author":"Reschini","year":"2022","journal-title":"Sci. Rep."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"337","DOI":"10.1016\/j.fertnstert.2018.04.041","article-title":"Relevance of assessing the uterine microbiota in infertility","volume":"110","author":"Moreno","year":"2018","journal-title":"Fertil. Steril."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"1021","DOI":"10.1093\/humrep\/deaa372","article-title":"Mapping the entire functionally active endometrial microbiota","volume":"36","author":"Molina","year":"2021","journal-title":"Hum. Reprod."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"1344","DOI":"10.1016\/j.fertnstert.2015.10.008","article-title":"Molecular characterization of the human microbiome from a reproductive perspective","volume":"104","author":"Mor","year":"2015","journal-title":"Fertil. Steril."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"344","DOI":"10.1016\/j.fertnstert.2018.04.012","article-title":"Endometritis: New time, new concepts","volume":"110","author":"Kitaya","year":"2018","journal-title":"Fertil. Steril."},{"key":"ref_10","doi-asserted-by":"crossref","unstructured":"Toson, B., Simon, C., and Moreno, I. (2022). The Endometrial Microbiome and Its Impact on Human Conception. Int. J. Mol. Sci., 23.","DOI":"10.3390\/ijms23010485"},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"132ra52","DOI":"10.1126\/scitranslmed.3003605","article-title":"Temporal Dynamics of the Human Vaginal Microbiota","volume":"4","author":"Gajer","year":"2012","journal-title":"Sci. Transl. Med."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"19213","DOI":"10.1038\/s41598-019-55720-8","article-title":"Postmenopause as a key factor in the composition of the Endometrial Cancer Microbiome (ECbiome)","volume":"9","author":"Walsh","year":"2019","journal-title":"Sci. Rep."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"350","DOI":"10.3389\/fcimb.2020.00350","article-title":"Structural Variations of Vaginal and Endometrial Microbiota: Hints on Female Infertility","volume":"10","author":"Riganelli","year":"2020","journal-title":"Front. Cell. Infect. Microbiol."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"122","DOI":"10.1097\/GCO.0000000000000782","article-title":"Microbiome as a predictor of implantation","volume":"34","author":"Gao","year":"2022","journal-title":"Curr. Opin. Obstet. Gynecol."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"R81","DOI":"10.1530\/REP-21-0120","article-title":"Current findings in endometrial microbiome: Impact on uterine diseases","volume":"163","year":"2022","journal-title":"Reproduction"},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"e13065","DOI":"10.1111\/aji.13065","article-title":"Endometrial microbes and microbiome: Recent insights on the inflammatory and immune \u201cplayers\u201d of the human endometrium","volume":"80","author":"Pontecorvi","year":"2018","journal-title":"Am. J. Reprod. Immunol."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"933","DOI":"10.1007\/s10482-017-0992-6","article-title":"A role for the endometrial microbiome in dysfunctional menstrual bleeding","volume":"111","author":"Pelzer","year":"2018","journal-title":"Antonie Van Leeuwenhoek Int. J. Gen. Mol. Microbiol."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"624","DOI":"10.1016\/j.ajog.2020.06.004","article-title":"Menstruation: Science and society","volume":"223","author":"Critchley","year":"2020","journal-title":"Am. J. Obstet. Gynecol."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"103634","DOI":"10.1016\/j.jri.2022.103634","article-title":"Uterine microbiota plasticity during the menstrual cycle: Differences between healthy controls and patients with recurrent miscarriage or implantation failure","volume":"151","author":"Vomstein","year":"2022","journal-title":"J. Reprod. Immunol."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"469","DOI":"10.1038\/nri.2017.64","article-title":"The unique immunological and microbial aspects of pregnancy","volume":"17","author":"Mor","year":"2017","journal-title":"Nat. Rev. Immunol."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"1315","DOI":"10.1111\/j.1471-0528.2009.02237.x","article-title":"Predictive value for preterm birth of abnormal vaginal flora, bacterial vaginosis and aerobic vaginitis during the first trimester of pregnancy","volume":"116","author":"Donders","year":"2009","journal-title":"BJOG Int. J. Obstet. Gynaecol."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"srep14174","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_23","doi-asserted-by":"crossref","first-page":"684","DOI":"10.1016\/j.ajog.2016.09.075","article-title":"Evidence that the endometrial microbiota has an effect on implantation success or failure","volume":"215","author":"Moreno","year":"2016","journal-title":"Am. J. Obstet. Gynecol."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"4893437","DOI":"10.1155\/2019\/4893437","article-title":"Characterization of Microbiota in Endometrial Fluid and Vaginal Secretions in Infertile Women with Repeated Implantation Failure","volume":"2019","author":"Kitaya","year":"2019","journal-title":"Mediat. Inflamm."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"707","DOI":"10.1016\/j.fertnstert.2019.05.015","article-title":"Endometrial microbiota in infertile women with and without chronic endometritis as diagnosed using a quantitative and reference range-based method","volume":"112","author":"Liu","year":"2019","journal-title":"Fertil. Steril."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"1743","DOI":"10.1373\/clinchem.2018.289306","article-title":"Systematic Comparison of Bacterial Colonization of Endometrial Tissue and Fluid Samples in Recurrent Miscarriage Patients: Implications for Future Endometrial Microbiome Studies","volume":"64","author":"Liu","year":"2018","journal-title":"Clin. Chem."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1186\/s40168-021-01184-w","article-title":"Endometrial microbiota composition is associated with reproductive outcome in infertile patients","volume":"10","author":"Moreno","year":"2022","journal-title":"Microbiome"},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"216","DOI":"10.3109\/00016349509008942","article-title":"Sterility of the uterine cavity","volume":"74","author":"Kristiansen","year":"1995","journal-title":"Acta Obstet. et Gynecol. Scand."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"5967","DOI":"10.1038\/s41467-021-26215-w","article-title":"Direct on-swab metabolic profiling of vaginal microbiome host interactions during pregnancy and preterm birth","volume":"12","author":"Pruski","year":"2021","journal-title":"Nat. Commun."},{"key":"ref_30","first-page":"1692","article-title":"Kocuria Kristinae in Catheter Associated Urinary Tract Infection: A Case Report","volume":"7","author":"Tewari","year":"2013","journal-title":"J. Clin. Diagn. Res."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"640","DOI":"10.1177\/1933719113508817","article-title":"Chronic Endometritis Due to Common Bacteria Is Prevalent in Women with Recurrent Miscarriage as Confirmed by Improved Pregnancy Outcome After Antibiotic Treatment","volume":"21","author":"Cicinelli","year":"2014","journal-title":"Reprod. Sci."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"844","DOI":"10.1016\/j.fertnstert.2016.02.023","article-title":"Optimal uterine anatomy and physiology necessary for normal implantation and placentation","volume":"105","author":"Pirtea","year":"2016","journal-title":"Fertil. Steril."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"255","DOI":"10.1111\/j.1600-0897.2007.00511.x","article-title":"Antigen-Presenting Cells and Materno-Fetal Tolerance: An Emerging Role for Dendritic Cells","volume":"58","author":"Rukavina","year":"2007","journal-title":"Am. J. Reprod. Immunol."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"357","DOI":"10.1017\/S0029665110001886","article-title":"Immunology of pregnancy","volume":"69","author":"Thornton","year":"2010","journal-title":"Proc. Nutr. Soc."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"75","DOI":"10.1530\/REP-14-0395","article-title":"Biopsy-induced inflammatory conditions improve endometrial receptivity: The mechanism of action","volume":"149","author":"Gnainsky","year":"2015","journal-title":"Reproduction"},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"2823","DOI":"10.3389\/fimmu.2019.02823","article-title":"Immunological Role of the Maternal Uterine Microbiome in Pregnancy: Pregnancies Pathologies and Alterated Microbiota","volume":"10","author":"Bardos","year":"2020","journal-title":"Front. Immunol."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"939","DOI":"10.1016\/j.rbmo.2021.02.003","article-title":"Impact of chronic endometritis in infertility: A SWOT analysis","volume":"42","author":"Fabregues","year":"2021","journal-title":"Reprod. Biomed. Online"},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"106","DOI":"10.1016\/j.fertnstert.2015.09.025","article-title":"Chronic endometritis in women with recurrent pregnancy loss and recurrent implantation failure: Prevalence and role of office hysteroscopy and immunohistochemistry in diagnosis","volume":"105","author":"Bouet","year":"2016","journal-title":"Fertil. Steril."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"323","DOI":"10.1093\/humrep\/deu292","article-title":"Prevalence of chronic endometritis in repeated unexplained implantation failure and the IVF success rate after antibiotic therapy","volume":"30","author":"Cicinelli","year":"2014","journal-title":"Hum. Reprod."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"125","DOI":"10.1002\/rmb2.12083","article-title":"Bacterial contamination hypothesis: A new concept in endometriosis","volume":"17","author":"Khan","year":"2018","journal-title":"Reprod. Med. Biol."},{"key":"ref_41","doi-asserted-by":"crossref","unstructured":"Boucher, A., Brichant, G., Gridelet, V., Nisolle, M., Ravet, S., Timmermans, M., and Henry, L. (2022). Implantation Failure in Endometriosis Patients: Etiopathogenesis. J. Clin. Med., 11.","DOI":"10.3390\/jcm11185366"},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"2446","DOI":"10.1093\/humrep\/deu222","article-title":"Intra-uterine microbial colonization and occurrence of endometritis in women with endometriosis\u2020","volume":"29","author":"Khan","year":"2014","journal-title":"Hum. Reprod."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"2860","DOI":"10.1016\/j.fertnstert.2010.04.053","article-title":"Escherichia coli contamination of menstrual blood and effect of bacterial endotoxin on endometriosis","volume":"94","author":"Khan","year":"2010","journal-title":"Fertil. Steril."},{"key":"ref_44","doi-asserted-by":"crossref","unstructured":"Tai, F., Chang, C.Y., Chiang, J., Lin, W., and Wan, L. (2018). Association of Pelvic Inflammatory Disease with Risk of Endometriosis: A Nationwide Cohort Study Involving 141,460 Individuals. J. Clin. Med., 7.","DOI":"10.3390\/jcm7110379"},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"18877","DOI":"10.1038\/s41598-021-98380-3","article-title":"Endometrial microbiota is more diverse in people with endometriosis than symptomatic controls","volume":"11","author":"Wessels","year":"2021","journal-title":"Sci. Rep."},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"15","DOI":"10.1186\/s12941-020-00356-0","article-title":"Microbiota composition and distribution along the female reproductive tract of women with endometriosis","volume":"19","author":"Wei","year":"2020","journal-title":"Ann. Clin. Microbiol. Antimicrob."},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"1064","DOI":"10.1007\/s43032-019-00113-5","article-title":"The Vaginal Microbiome as a Tool to Predict rASRM Stage of Disease in Endometriosis: A Pilot Study","volume":"27","author":"Perrotta","year":"2020","journal-title":"Reprod. Sci."},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"1106","DOI":"10.1093\/humrep\/dez041","article-title":"Antibiotic therapy with metronidazole reduces endometriosis disease progression in mice: A potential role for gut microbiota","volume":"34","author":"Chadchan","year":"2019","journal-title":"Hum. Reprod."},{"key":"ref_49","doi-asserted-by":"crossref","unstructured":"Molina, N.M., Sola-Leyva, A., Saez-Lara, M.J., Plaza-Diaz, J., Tubi\u0107-Pavlovi\u0107, A., Romero, B., Clavero, A., Mozas-Moreno, J., Fontes, J., and Altm\u00e4e, S. (2020). New Opportunities for Endometrial Health by Modifying Uterine Microbial Composition: Present or Future?. Biomolecules, 10.","DOI":"10.3390\/biom10040593"},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"210","DOI":"10.1053\/j.gastro.2010.09.048","article-title":"Lack of Commensal Flora in Helicobacter pylori\u2013Infected INS-GAS Mice Reduces Gastritis and Delays Intraepithelial Neoplasia","volume":"140","author":"Lofgren","year":"2011","journal-title":"Gastroenterology"},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"800","DOI":"10.1038\/nrc3610","article-title":"The microbiome and cancer","volume":"13","author":"Schwabe","year":"2013","journal-title":"Nat. Rev. Cancer"},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"80","DOI":"10.1126\/science.aaa4972","article-title":"Cancer and the microbiota","volume":"348","author":"Garrett","year":"2015","journal-title":"Science"},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"232","DOI":"10.1038\/s41585-020-0286-z","article-title":"The microbiome and gynaecological cancer development, prevention and therapy","volume":"17","author":"Ilhan","year":"2020","journal-title":"Nat. Rev. Urol."},{"key":"ref_54","doi-asserted-by":"crossref","unstructured":"Fulbright, L.E., Ellermann, M., and Arthur, J.C. (2017). The microbiome and the hallmarks of cancer. PLoS Pathog., 13.","DOI":"10.1371\/journal.ppat.1006480"},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"122","DOI":"10.1186\/s13073-016-0368-y","article-title":"Potential contribution of the uterine microbiome in the development of endometrial cancer","volume":"8","author":"Chen","year":"2016","journal-title":"Genome Med."},{"key":"ref_56","doi-asserted-by":"crossref","first-page":"1708","DOI":"10.1002\/ijc.33428","article-title":"Dysbiosis of the endometrial microbiota and its association with inflammatory cytokines in endometrial cancer","volume":"148","author":"Lu","year":"2020","journal-title":"Int. J. Cancer"},{"key":"ref_57","doi-asserted-by":"crossref","first-page":"97","DOI":"10.1126\/science.aan4236","article-title":"Gut microbiome modulates response to anti\u2013PD-1 immunotherapy in melanoma patients","volume":"359","author":"Gopalakrishnan","year":"2018","journal-title":"Science"}],"container-title":["Medicina"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/1648-9144\/59\/9\/1540\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T20:39:13Z","timestamp":1760128753000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/1648-9144\/59\/9\/1540"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2023,8,25]]},"references-count":57,"journal-issue":{"issue":"9","published-online":{"date-parts":[[2023,9]]}},"alternative-id":["medicina59091540"],"URL":"https:\/\/doi.org\/10.3390\/medicina59091540","relation":{},"ISSN":["1648-9144"],"issn-type":[{"value":"1648-9144","type":"electronic"}],"subject":[],"published":{"date-parts":[[2023,8,25]]}}}