{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,7]],"date-time":"2026-10-07T16:15:18Z","timestamp":1791389718901,"version":"4.3.3"},"reference-count":51,"publisher":"Georg Thieme Verlag KG","issue":"05","content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Semin Reprod Med"],"published-print":{"date-parts":[[2023,9]]},"abstract":"<jats:title>Abstract<\/jats:title><jats:p>Studies have proven the significance of microbial communities in various parts of the human body for health. In recent years it has been discovered that the uterine cavity is not sterile, and endometrium has its own microbiome which appears to have an impact on female fertility and gynecological pathologies. Lactobacillus has shown to dominate the microbial profile in the uterus and is considered an indicator of a healthy uterine environment. Yet, many argue that the Lactobacillus dominance is due to vaginal contamination during the sampling process. To date there is no clearly defined healthy endometrial microbial profile, which is largely due to the fact that determining the microbial community from the endometrium is complicated, and there is currently no consensus on sampling methods for the endometrial microbiome. As a result, this restricts ability to replicate discoveries made in other cohorts. Here we aim to give an overview of the sampling methods used and discuss what impedes the endometrial microbiome studies as well as how to reach a consensus on the study design. This knowledge could be incorporated into the future research and the knowledge on endometrial microbiome could be included into the diagnostics and treatment of female reproductive health.<\/jats:p>","DOI":"10.1055\/s-0043-1777361","type":"journal-article","created":{"date-parts":[[2023,12,9]],"date-time":"2023-12-09T00:45:58Z","timestamp":1702082758000},"page":"144-150","source":"Crossref","is-referenced-by-count":7,"title":["Uterine Microbiome: Does the Sampling Technique Matter?"],"prefix":"10.1055","volume":"41","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-9722-5876","authenticated-orcid":false,"given":"Kreete","family":"L\u00fcll","sequence":"additional","affiliation":[{"name":"Institute of Genomics, Estonian Genome Centre, University of Tartu, Tartu, Estonia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-8688-9717","authenticated-orcid":false,"given":"Elin","family":"Org","sequence":"additional","affiliation":[{"name":"Institute of Genomics, Estonian Genome Centre, University of Tartu, Tartu, Estonia"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"194","published-online":{"date-parts":[[2023,12,8]]},"reference":[{"key":"ref1","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":"L K Ursell","year":"2012","journal-title":"Nutr Rev"},{"issue":"06","key":"ref2","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":"M G Dominguez-Bello","year":"2019","journal-title":"Gut"},{"issue":"01","key":"ref3","doi-asserted-by":"crossref","first-page":"55","DOI":"10.1038\/s41579-020-0433-9","article-title":"Gut microbiota in human metabolic health and disease","volume":"19","author":"Y Fan","year":"2021","journal-title":"Nat Rev Microbiol"},{"key":"ref4","doi-asserted-by":"crossref","first-page":"208","DOI":"10.3389\/fimmu.2018.00208","article-title":"Uterine microbiota: Residents, tourists, or invaders?","volume":"9","author":"J M Baker","year":"2018","journal-title":"Front Immunol"},{"issue":"03","key":"ref5","doi-asserted-by":"crossref","first-page":"298","DOI":"10.1093\/humupd\/dmy048","article-title":"Identification and evaluation of the microbiome in the female and male reproductive tracts","volume":"25","author":"R Koedooder","year":"2019","journal-title":"Hum Reprod Update"},{"issue":"04","key":"ref6","doi-asserted-by":"crossref","first-page":"393","DOI":"10.1093\/humupd\/dmy012","article-title":"How 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Gynekol"},{"issue":"02","key":"ref13","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":"E Cicinelli","year":"2015","journal-title":"Hum Reprod"},{"issue":"05","key":"ref14","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":"E Cicinelli","year":"2014","journal-title":"Reprod Sci"},{"issue":"04","key":"ref15","doi-asserted-by":"crossref","first-page":"799","DOI":"10.1016\/j.fertnstert.2004.05.076","article-title":"Can endometrial infection\/inflammation explain implantation failure, spontaneous abortion, and preterm birth after in vitro 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Res"},{"issue":"01","key":"ref19","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":"M RS Walther-Ant\u00f3nio","year":"2016","journal-title":"Genome Med"},{"issue":"01","key":"ref20","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":"D M Walsh","year":"2019","journal-title":"Sci Rep"},{"issue":"01","key":"ref21","doi-asserted-by":"crossref","first-page":"9905","DOI":"10.1038\/s41598-019-46173-0","article-title":"Does the endometrial cavity have a molecular microbial signature?","volume":"9","author":"A D Winters","year":"2019","journal-title":"Sci 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Sola-Leyva","year":"2021","journal-title":"Hum Reprod"},{"issue":"132","key":"ref37","doi-asserted-by":"crossref","first-page":"132ra52","DOI":"10.1126\/scitranslmed.3003605","article-title":"Temporal dynamics of the human vaginal microbiota","volume":"4","author":"P Gajer","year":"2012","journal-title":"Sci Transl Med"},{"issue":"01","key":"ref38","doi-asserted-by":"crossref","first-page":"485","DOI":"10.3390\/ijms23010485","article-title":"The endometrial microbiome and its impact on human conception","volume":"23","author":"B Toson","year":"2022","journal-title":"Int J Mol Sci"},{"issue":"06","key":"ref39","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":"E S Pelzer","year":"2018","journal-title":"Antonie van Leeuwenhoek"},{"key":"ref40","first-page":"267","article-title":"The uterine peristaltic pump. Normal and impeded sperm transport within the female genital tract","volume":"424","author":"G Kunz","year":"1997","journal-title":"Adv Exp Med Biol"},{"key":"ref41","doi-asserted-by":"crossref","first-page":"87","DOI":"10.1186\/s12915-014-0087-z","article-title":"Reagent and laboratory contamination can critically impact sequence-based microbiome analyses","volume":"12","author":"S J Salter","year":"2014","journal-title":"BMC Biol"},{"issue":"01","key":"ref42","doi-asserted-by":"crossref","first-page":"2","DOI":"10.1111\/lam.13091","article-title":"Identification and removal of contaminating microbial DNA from PCR reagents: impact on low-biomass microbiome analyses","volume":"68","author":"L F Stinson","year":"2019","journal-title":"Lett Appl Microbiol"},{"issue":"04","key":"ref43","doi-asserted-by":"crossref","first-page":"982","DOI":"10.1111\/1755-0998.13011","article-title":"Laboratory contamination over time during low-biomass sample analysis","volume":"19","author":"L S Weyrich","year":"2019","journal-title":"Mol Ecol Resour"},{"issue":"05","key":"ref44","doi-asserted-by":"crossref","first-page":"e97876","DOI":"10.1371\/journal.pone.0097876","article-title":"Common contaminants in next-generation sequencing that hinder discovery of low-abundance microbes","volume":"9","author":"M Laurence","year":"2014","journal-title":"PLoS One"},{"issue":"03","key":"ref45","doi-asserted-by":"crossref","first-page":"297","DOI":"10.1002\/rmb2.12105","article-title":"Analysis of endometrial microbiota by 16S ribosomal RNA gene sequencing among infertile patients: a single-center pilot study","volume":"17","author":"K Kyono","year":"2018","journal-title":"Reprod Med Biol"},{"key":"ref46","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":"K Kitaya","year":"2019","journal-title":"Mediators Inflamm"},{"issue":"01","key":"ref47","doi-asserted-by":"crossref","first-page":"87","DOI":"10.1016\/S0378-1097(02)01190-4","article-title":"Identification of mixed bacterial DNA contamination in broad-range PCR amplification of 16S rDNA V1 and V3 variable regions by pyrosequencing of cloned amplicons","volume":"219","author":"N Grahn","year":"2003","journal-title":"FEMS Microbiol Lett"},{"key":"ref48","doi-asserted-by":"crossref","first-page":"24","DOI":"10.1186\/s13099-016-0103-7","article-title":"Inherent bacterial DNA contamination of extraction and sequencing reagents may affect interpretation of microbiota in low bacterial biomass samples","volume":"8","author":"A Glassing","year":"2016","journal-title":"Gut Pathog"},{"issue":"01","key":"ref49","doi-asserted-by":"crossref","first-page":"226","DOI":"10.1186\/s40168-018-0605-2","article-title":"Simple statistical identification and removal of contaminant sequences in marker-gene and metagenomics data","volume":"6","author":"N M Davis","year":"2018","journal-title":"Microbiome"},{"issue":"01","key":"ref50","doi-asserted-by":"crossref","first-page":"14","DOI":"10.1002\/edn3.11","article-title":"microDecon: a highly accurate read-subtraction tool for the post-sequencing removal of contamination in metabarcoding studies","volume":"1","author":"D T McKnight","year":"2019","journal-title":"Environ DNA"},{"issue":"01","key":"ref51","doi-asserted-by":"crossref","first-page":"28","DOI":"10.1186\/s40168-016-0175-0","article-title":"Adjusting microbiome profiles for differences in microbial load by spike-in bacteria","volume":"4","author":"F St\u00e4mmler","year":"2016","journal-title":"Microbiome"}],"container-title":["Seminars in Reproductive Medicine"],"original-title":[],"language":"en","link":[{"URL":"http:\/\/www.thieme-connect.de\/products\/ejournals\/pdf\/10.1055\/s-0043-1777361.pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2024,11,5]],"date-time":"2024-11-05T13:51:44Z","timestamp":1730814704000},"score":1,"resource":{"primary":{"URL":"http:\/\/www.thieme-connect.de\/DOI\/DOI?10.1055\/s-0043-1777361"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2023,9]]},"references-count":51,"journal-issue":{"issue":"05","published-online":{"date-parts":[[2024,2,6]]},"published-print":{"date-parts":[[2023,9]]}},"URL":"https:\/\/doi.org\/10.1055\/s-0043-1777361","archive":["Portico","CLOCKSS"],"relation":{},"ISSN":["1526-8004","1526-4564"],"issn-type":[{"value":"1526-8004","type":"print"},{"value":"1526-4564","type":"electronic"}],"subject":[],"published":{"date-parts":[[2023,9]]}}}