{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,11,13]],"date-time":"2026-11-13T06:03:07Z","timestamp":1794549787796,"version":"4.9.1"},"reference-count":79,"publisher":"Springer Science and Business Media LLC","issue":"1","license":[{"start":{"date-parts":[[2021,9,23]],"date-time":"2021-09-23T00:00:00Z","timestamp":1632355200000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"},{"start":{"date-parts":[[2021,9,23]],"date-time":"2021-09-23T00:00:00Z","timestamp":1632355200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"}],"funder":[{"DOI":"10.13039\/501100000024","name":"Canadian Institutes of Health Research","doi-asserted-by":"publisher","award":["MFE-381806"],"award-info":[{"award-number":["MFE-381806"]}],"id":[{"id":"10.13039\/501100000024","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100000024","name":"Canadian Institutes of Health Research","doi-asserted-by":"publisher","award":["MOP142230"],"award-info":[{"award-number":["MOP142230"]}],"id":[{"id":"10.13039\/501100000024","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["Sci Rep"],"abstract":"<jats:title>Abstract<\/jats:title>\n                  <jats:p>\n                    Endometriosis is a chronic, estrogen-dependent gynecological condition affecting approximately 10% of reproductive age women. The most widely accepted theory of its etiology includes retrograde menstruation. Recent reports suggest the uterus is not sterile. Thus, the refluxed menstrual effluent may carry bacteria, and contribute to inflammation, the establishment and growth of endometriotic lesions. Here, we compared and contrasted uterine bacteria (endometrial microbiota) in people with surgically confirmed presence (N\u2009=\u200912) or absence of endometriosis (N\u2009=\u20099) using next-generation 16S rRNA gene sequencing. We obtained an average of\u2009&gt;\u20099000 sequence reads per endometrial biopsy, and found the endometrial microbiota of people with endometriosis was more diverse (greater Shannon Diversity Index and proportion of \u2018Other\u2019 taxa) than symptomatic controls (with pelvic pain, surgically confirmed absence of endometriosis; diagnosed with other benign gynecological conditions). The relative abundance of bacterial taxa enriched in the endometrial microbiota of people with endometriosis belonged to the Actinobacteria phylum (Gram-positive),\n                    <jats:italic>Oxalobacteraceae<\/jats:italic>\n                    (Gram-negative) and\n                    <jats:italic>Streptococcaceae<\/jats:italic>\n                    (Gram-positive) families, and\n                    <jats:italic>Tepidimonas<\/jats:italic>\n                    (Gram-negative) genus, while those enriched in the symptomatic controls belonged to the\n                    <jats:italic>Burkholderiaceae<\/jats:italic>\n                    (Gram-negative) family, and\n                    <jats:italic>Ralstonia<\/jats:italic>\n                    (Gram-negative) genus. Taken together, results suggest the endometrial microbiota is perturbed in people with endometriosis.\n                  <\/jats:p>","DOI":"10.1038\/s41598-021-98380-3","type":"journal-article","created":{"date-parts":[[2021,9,23]],"date-time":"2021-09-23T06:57:49Z","timestamp":1632380269000},"update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":72,"title":["Endometrial microbiota is more diverse in people with endometriosis than symptomatic controls"],"prefix":"10.1038","volume":"11","author":[{"given":"Jocelyn M.","family":"Wessels","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Miguel A.","family":"Dom\u00ednguez","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Nicholas A.","family":"Leyland","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Sanjay K.","family":"Agarwal","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Warren G.","family":"Foster","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"297","published-online":{"date-parts":[[2021,9,23]]},"reference":[{"key":"98380_CR1","doi-asserted-by":"publisher","DOI":"10.23736\/S2724-606X.21.04779-1","author":"L Masciullo","year":"2021","unstructured":"Masciullo, L. et al. A deep insight into pelvic pain and endometriosis: A review of the literature from pathophysiology to clinical expressions. Minerva Obstet. Gynecol. https:\/\/doi.org\/10.23736\/S2724-606X.21.04779-1 (2021).","journal-title":"Minerva Obstet. Gynecol."},{"key":"98380_CR2","doi-asserted-by":"publisher","first-page":"422","DOI":"10.1016\/S0002-9378(15)30003-X","volume":"14","author":"JA Sampson","year":"1927","unstructured":"Sampson, J. A. Peritoneal endometriosis due to menstrual dissemination of endometrial tissue into the peritoneal cavity. Am. J. Obstet. Gynecol. 14, 422\u2013469 (1927).","journal-title":"Am. J. Obstet. Gynecol."},{"key":"98380_CR3","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1155\/2014\/179515","volume":"2014","author":"S Sourial","year":"2014","unstructured":"Sourial, S., Tempest, N. & Hapangama, D. K. Theories on the pathogenesis of endometriosis. Int. J. Reprod. Med. 2014, 1\u201310 (2014).","journal-title":"Int. J. Reprod. Med."},{"key":"98380_CR4","doi-asserted-by":"publisher","first-page":"523","DOI":"10.1016\/j.fertnstert.2017.01.009","volume":"107","author":"SH Ahn","year":"2017","unstructured":"Ahn, S. H., Singh, V. & Tayade, C. Biomarkers in endometriosis: Challenges and opportunities. Fertil. Steril. 107, 523\u2013532 (2017).","journal-title":"Fertil. Steril."},{"key":"98380_CR5","doi-asserted-by":"publisher","first-page":"778","DOI":"10.1016\/j.biocel.2010.03.008","volume":"42","author":"PG Signorile","year":"2010","unstructured":"Signorile, P. G. & Baldi, A. Endometriosis: New concepts in the pathogenesis. Int. J. Biochem. Cell Biol. 42, 778\u2013780 (2010).","journal-title":"Int. J. Biochem. Cell Biol."},{"key":"98380_CR6","doi-asserted-by":"publisher","first-page":"1653","DOI":"10.1002\/jcp.22888","volume":"227","author":"PG Signorile","year":"2012","unstructured":"Signorile, P. G. et al. Embryologic origin of endometriosis: Analysis of 101 human female fetuses. J. Cell Physiol. 227, 1653\u20131656 (2012).","journal-title":"J. Cell Physiol."},{"key":"98380_CR7","doi-asserted-by":"publisher","first-page":"33","DOI":"10.1080\/15476278.2016.1145317","volume":"12","author":"Z Makiyan","year":"2016","unstructured":"Makiyan, Z. New theory of uterovaginal embryogenesis. Organogenesis 12, 33\u201341 (2016).","journal-title":"Organogenesis"},{"key":"98380_CR8","doi-asserted-by":"publisher","first-page":"106","DOI":"10.1196\/annals.1434.014","volume":"1127","author":"IE Sasson","year":"2008","unstructured":"Sasson, I. E. & Taylor, H. S. Stem cells and the pathogenesis of endometriosis. Ann. N. Y. Acad. Sci. 1127, 106\u2013115 (2008).","journal-title":"Ann. N. Y. Acad. Sci."},{"key":"98380_CR9","doi-asserted-by":"publisher","first-page":"2807","DOI":"10.1016\/j.cell.2021.04.041","volume":"184","author":"PTK Saunders","year":"2021","unstructured":"Saunders, P. T. K. & Horne, A. W. Endometriosis: Etiology, pathobiology, and therapeutic prospects. Cell 184, 2807\u20132824 (2021).","journal-title":"Cell"},{"key":"98380_CR10","doi-asserted-by":"publisher","first-page":"1244","DOI":"10.1056\/NEJMra1810764","volume":"382","author":"KT Zondervan","year":"2020","unstructured":"Zondervan, K. T., Becker, C. M. & Missmer, S. A. Endometriosis. N. Engl. J. Med. 382, 1244\u20131256 (2020).","journal-title":"N. Engl. J. Med."},{"issue":"451","key":"98380_CR11","first-page":"e1","volume":"208","author":"CM Peterson","year":"2013","unstructured":"Peterson, C. M. et al. Risk factors associated with endometriosis: Importance of study population for characterizing disease in the ENDO Study. Am. J. Obstet. Gynecol. 208(451), e1\u2013e11 (2013).","journal-title":"Am. J. Obstet. Gynecol."},{"key":"98380_CR12","doi-asserted-by":"publisher","first-page":"2171","DOI":"10.1093\/humrep\/deu169","volume":"29","author":"P Vercellini","year":"2014","unstructured":"Vercellini, P. et al. \u2019Behind blue eyes\u2019\u2020: The association between eye colour and deep infiltrating endometriosis. Hum. Reprod. 29, 2171\u20132175 (2014).","journal-title":"Hum. Reprod."},{"key":"98380_CR13","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1016\/j.bpobgyn.2018.06.001","volume":"51","author":"AL Shafrir","year":"2018","unstructured":"Shafrir, A. L. et al. Risk for and consequences of endometriosis: A critical epidemiologic review. Best Pract. Res. Clin. Obstet. Gynaecol. 51, 1\u201315 (2018).","journal-title":"Best Pract. Res. Clin. Obstet. Gynaecol."},{"key":"98380_CR14","doi-asserted-by":"publisher","first-page":"101","DOI":"10.1515\/reveh-2020-0046","volume":"36","author":"D Sirohi","year":"2020","unstructured":"Sirohi, D., Al Ramadhani, R. & Knibbs, L. D. Environmental exposures to endocrine disrupting chemicals (EDCs) and their role in endometriosis: A systematic literature review. Rev. Environ Health 36, 101\u2013115 (2020).","journal-title":"Rev. Environ Health"},{"key":"98380_CR15","first-page":"151","volume":"64","author":"J Halme","year":"1984","unstructured":"Halme, J., Hammond, M. G., Hulka, J. F., Raj, S. G. & Talbert, L. M. Retrograde menstruation in healthy women and in patients with endometriosis. Obstet. Gynecol. 64, 151\u2013154 (1984).","journal-title":"Obstet. Gynecol."},{"key":"98380_CR16","doi-asserted-by":"publisher","first-page":"728","DOI":"10.1007\/s43032-020-00370-9","volume":"28","author":"F Murgia","year":"2021","unstructured":"Murgia, F. et al. Metabolic profile of patients with severe endometriosis: A prospective experimental study. Reprod. Sci. 28, 728\u2013735 (2021).","journal-title":"Reprod. Sci."},{"key":"98380_CR17","doi-asserted-by":"publisher","first-page":"327","DOI":"10.1016\/j.fertnstert.2018.10.013","volume":"111","author":"PR Koninckx","year":"2019","unstructured":"Koninckx, P. R. et al. Pathogenesis of endometriosis: The genetic\/epigenetic theory. Fertil. Steril. 111, 327\u2013340 (2019).","journal-title":"Fertil. Steril."},{"key":"98380_CR18","doi-asserted-by":"publisher","first-page":"1","DOI":"10.3390\/ijms21051765","volume":"21","author":"S Angioni","year":"2020","unstructured":"Angioni, S. et al. Genetic characterization of endometriosis patients: Review of the literature and a prospective cohort study on a Mediterranean population. Int. J. Mol. Sci. 21, 1\u201324 (2020).","journal-title":"Int. J. Mol. Sci."},{"key":"98380_CR19","doi-asserted-by":"publisher","first-page":"2317","DOI":"10.1101\/gr.096651.109","volume":"19","author":"J Peterson","year":"2009","unstructured":"Peterson, J. et al. The NIH human microbiome project. Genome Res. 19, 2317\u20132323 (2009).","journal-title":"Genome Res."},{"key":"98380_CR20","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1371\/journal.pbio.1002533","volume":"14","author":"R Sender","year":"2016","unstructured":"Sender, R., Fuchs, S. & Milo, R. Revised estimates for the number of human and bacteria cells in the body. PLoS Biol. 14, 1\u201314 (2016).","journal-title":"PLoS Biol."},{"key":"98380_CR21","doi-asserted-by":"publisher","first-page":"1687","DOI":"10.1093\/oxfordjournals.humrep.a019470","volume":"11","author":"PE Egbase","year":"1996","unstructured":"Egbase, P. E. et al. Incidence of microbial growth from the tip of the embryo transfer catheter after embryo transfer in relation to clinical pregnancy rate following in-vitro fertilization and embryo transfer. Hum. Reprod. (Oxford, England) 11, 1687\u20131689 (1996).","journal-title":"Hum. Reprod. (Oxford, England)"},{"key":"98380_CR22","doi-asserted-by":"publisher","first-page":"1118","DOI":"10.1016\/S0015-0282(00)01624-1","volume":"74","author":"DE Moore","year":"2000","unstructured":"Moore, D. E. et al. Bacteria in the transfer catheter tip influence the live-birth rate after in vitro fertilization. Fertil. Steril. 74, 1118\u20131124 (2000).","journal-title":"Fertil. Steril."},{"key":"98380_CR23","doi-asserted-by":"publisher","first-page":"395","DOI":"10.1007\/s10815-007-9146-5","volume":"24","author":"H Selman","year":"2007","unstructured":"Selman, H. et al. Examination of bacterial contamination at the time of embryo transfer, and its impact on the IVF\/pregnancy outcome. J. Assist. Reprod. Genet. 24, 395\u2013399 (2007).","journal-title":"J. Assist. Reprod. Genet."},{"key":"98380_CR24","doi-asserted-by":"publisher","first-page":"129","DOI":"10.1007\/s10815-015-0614-z","volume":"33","author":"JM Franasiak","year":"2016","unstructured":"Franasiak, J. M. et al. Endometrial microbiome at the time of embryo transfer: Next-generation sequencing of the 16S ribosomal subunit. J. Assist. Reprod. Genet. 33, 129\u2013136 (2016).","journal-title":"J. Assist. Reprod. Genet."},{"key":"98380_CR25","doi-asserted-by":"publisher","first-page":"684","DOI":"10.1016\/j.ajog.2016.09.075","volume":"215","author":"I Moreno","year":"2016","unstructured":"Moreno, I. et al. Evidence that the endometrial microbiota has an effect on implantation success or failure. Am. J. Obstet. Gynecol. 215, 684\u2013703 (2016).","journal-title":"Am. J. Obstet. Gynecol."},{"key":"98380_CR26","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1038\/s41467-016-0009-6","volume":"8","author":"C Chen","year":"2017","unstructured":"Chen, C. et al. The microbiota continuum along the female reproductive tract and its relation to uterine-related diseases. Nat. Commun. 8, 1\u201311 (2017).","journal-title":"Nat. Commun."},{"key":"98380_CR27","doi-asserted-by":"publisher","first-page":"15","DOI":"10.1016\/j.humic.2017.01.004","volume":"3","author":"X Tao","year":"2017","unstructured":"Tao, X. et al. Characterizing the endometrial microbiome by analyzing the ultra-low bacteria from embryo transfer catheter tips in IVF cycles: Next generation sequencing (NGS) analysis of the 16S ribosomal gene. Hum. Microbiome J. 3, 15\u201321 (2017).","journal-title":"Hum. Microbiome J."},{"key":"98380_CR28","doi-asserted-by":"publisher","first-page":"297","DOI":"10.1002\/rmb2.12105","volume":"17","author":"K Kyono","year":"2018","unstructured":"Kyono, K., Hashimoto, T., Nagai, Y. & Sakuraba, Y. Analysis of endometrial microbiota by 16S ribosomal RNA gene sequencing among infertile patients: A single-center pilot study. Reprod. Med. Biol. 17, 297\u2013306 (2018).","journal-title":"Reprod. Med. Biol."},{"key":"98380_CR29","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1155\/2019\/4893437","volume":"2019","author":"K Kitaya","year":"2019","unstructured":"Kitaya, K., Nagai, Y., Arai, W., Sakuraba, Y. & Ishikawa, T. Characterization of microbiota in endometrial fluid and vaginal secretions in infertile women with repeated implantation failure. Mediators Inflamm. 2019, 1\u201310 (2019).","journal-title":"Mediators Inflamm."},{"key":"98380_CR30","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1038\/s41598-019-46173-0","volume":"9","author":"AD Winters","year":"2019","unstructured":"Winters, A. D. et al. Does the endometrial cavity have a molecular microbial signature?. Sci. Rep. 9, 1\u201317 (2019).","journal-title":"Sci. Rep."},{"key":"98380_CR31","doi-asserted-by":"publisher","first-page":"1","DOI":"10.3390\/diagnostics10030163","volume":"10","author":"C Hernandes","year":"2020","unstructured":"Hernandes, C. et al. Microbiome profile of deep endometriosis patients: Comparison of vaginal fluid, endometrium and lesion. Diagnostics 10, 1\u201311 (2020).","journal-title":"Diagnostics"},{"key":"98380_CR32","doi-asserted-by":"publisher","first-page":"296","DOI":"10.1016\/j.ajog.2020.01.031","volume":"222","author":"I Moreno","year":"2020","unstructured":"Moreno, I. et al. The first glimpse of the endometrial microbiota in early pregnancy. Am. J. Obstet. Gynecol. 222, 296\u2013305 (2020).","journal-title":"Am. J. Obstet. Gynecol."},{"key":"98380_CR33","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1186\/s12941-020-00356-0","volume":"19","author":"W Wei","year":"2020","unstructured":"Wei, W., Zhang, X., Tang, H., Zeng, L. & Wu, R. Microbiota composition and distribution along the female reproductive tract of women with endometriosis. Ann. Clin. Microbiol. Antimicrob. 19, 1\u20138 (2020).","journal-title":"Ann. Clin. Microbiol. Antimicrob."},{"key":"98380_CR34","doi-asserted-by":"publisher","first-page":"1","DOI":"10.3389\/fimmu.2018.00208","volume":"9","author":"JM Baker","year":"2018","unstructured":"Baker, J. M., Chase, D. M. & Herbst-Kralovetz, M. M. Uterine microbiota: Residents, tourists, or invaders?. Front. Immunol. 9, 1\u201316 (2018).","journal-title":"Front. Immunol."},{"key":"98380_CR35","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1186\/s13073-016-0368-y","volume":"8","author":"MRS Walther-Ant\u00f3nio","year":"2016","unstructured":"Walther-Ant\u00f3nio, M. R. S. et al. Potential contribution of the uterine microbiome in the development of endometrial cancer. Genome Med. 8, 1\u201315 (2016).","journal-title":"Genome Med."},{"key":"98380_CR36","doi-asserted-by":"publisher","first-page":"1708","DOI":"10.1002\/ijc.33428","volume":"148","author":"W Lu","year":"2021","unstructured":"Lu, W. et al. Dysbiosis of the endometrial microbiota and its association with inflammatory cytokines in endometrial cancer. Int. J. Cancer 148, 1708\u20131716 (2021).","journal-title":"Int. J. Cancer"},{"key":"98380_CR37","doi-asserted-by":"publisher","first-page":"2860-3.e1-3","DOI":"10.1016\/j.fertnstert.2010.04.053","volume":"94","author":"KN Khan","year":"2010","unstructured":"Khan, K. N. et al. Escherichia coli contamination of menstrual blood and effect of bacterial endotoxin on endometriosis. Fertil. Steril. 94, 2860-3.e1-3 (2010).","journal-title":"Fertil. Steril."},{"issue":"1","key":"98380_CR38","first-page":"1","volume":"1","author":"J Puca","year":"2016","unstructured":"Puca, J. & Hoyne, G. F. Microbial dysbiosis and disease pathogenesis of endometriosis, could there be a link?. Allied J. Med. Res. 1(1), 1\u20139 (2016).","journal-title":"Allied J. Med. Res."},{"key":"98380_CR39","doi-asserted-by":"publisher","first-page":"125","DOI":"10.1002\/rmb2.12083","volume":"17","author":"KN Khan","year":"2018","unstructured":"Khan, K. N. et al. Bacterial contamination hypothesis: A new concept in endometriosis. Reprod. Med. Biol. 17, 125\u2013133 (2018).","journal-title":"Reprod. Med. Biol."},{"key":"98380_CR40","doi-asserted-by":"publisher","first-page":"239","DOI":"10.1111\/1471-0528.15916","volume":"127","author":"M Leonardi","year":"2020","unstructured":"Leonardi, M., Hicks, C., El-Assaad, F., El-Omar, E. & Condous, G. Endometriosis and the microbiome: A systematic review. BJOG 127, 239\u2013249 (2020).","journal-title":"BJOG"},{"key":"98380_CR41","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1242\/dmm.039669","volume":"12","author":"JM Wessels","year":"2019","unstructured":"Wessels, J. M. et al. Medroxyprogesterone acetate alters the vaginal microbiota and microenvironment in women and increases susceptibility to HIV-1 in humanized mice. Dis. Model. Mech. 12, 1\u201313 (2019).","journal-title":"Dis. Model. Mech."},{"key":"98380_CR42","doi-asserted-by":"publisher","first-page":"817","DOI":"10.1016\/S0015-0282(97)81391-X","volume":"67","author":"ASRM","year":"1997","unstructured":"ASRM. Revised American Society for Reproductive Medicine classification of endometriosis: 1996. Fertil. Steril. 67, 817\u2013821 (1997).","journal-title":"Fertil. Steril."},{"key":"98380_CR43","doi-asserted-by":"publisher","first-page":"3","DOI":"10.1016\/S0015-0282(16)30062-0","volume":"1","author":"RW Noyes","year":"1950","unstructured":"Noyes, R. W., Hertig, A. T. & Rock, J. Dating the endometrial biopsy. Fertil. Steril. 1, 3\u201311 (1950).","journal-title":"Fertil. Steril."},{"key":"98380_CR44","doi-asserted-by":"publisher","first-page":"3846","DOI":"10.1128\/AEM.02772-10","volume":"77","author":"AK Bartram","year":"2011","unstructured":"Bartram, A. K., Lynch, M. D. J., Stearns, J. C., Moreno-Hagelsieb, G. & Neufeld, J. D. Generation of multimillion-sequence 16S rRNA gene libraries from complex microbial communities by assembling paired-end illumina reads. Appl. Environ. Microbiol. 77, 3846\u20133852 (2011).","journal-title":"Appl. Environ. Microbiol."},{"key":"98380_CR45","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1186\/s40168-017-0314-2","volume":"5","author":"FJ Whelan","year":"2017","unstructured":"Whelan, F. J. & Surette, M. G. A comprehensive evaluation of the sl1p pipeline for 16S rRNA gene sequencing analysis. Microbiome 5, 1\u201313 (2017).","journal-title":"Microbiome"},{"key":"98380_CR46","doi-asserted-by":"publisher","first-page":"e0187612","DOI":"10.1371\/journal.pone.0187612","volume":"12","author":"JM Wessels","year":"2017","unstructured":"Wessels, J. M. et al. Association of high-risk sexual behaviour with diversity of the vaginal microbiota and abundance of Lactobacillus. PLoS ONE 12, e0187612 (2017).","journal-title":"PLoS ONE"},{"key":"98380_CR47","doi-asserted-by":"publisher","first-page":"R60","DOI":"10.1186\/gb-2011-12-6-r60","volume":"12","author":"N Segata","year":"2011","unstructured":"Segata, N. et al. Metagenomic biomarker discovery and explanation. Genome Biol. 12, R60 (2011).","journal-title":"Genome Biol."},{"key":"98380_CR48","unstructured":"Oksanen, J. B., Guillaume, F., Friendly, M., Kindt, R., Legendre, P., McGlinn, D., Minchin, P. R., O'Hara, R. B., Simpson, G. L., Solymos, P. M., Stevens, H. H., Szoecs, E. Wagner, H. vegan: Community ecology package. In R package version 24-1 (2016)."},{"key":"98380_CR49","doi-asserted-by":"publisher","first-page":"2089","DOI":"10.4014\/jmb.1709.09027","volume":"27","author":"BR Kim","year":"2017","unstructured":"Kim, B. R. et al. Deciphering diversity indices for a better understanding of microbial communities. J. Microbiol. Biotechnol. 27, 2089\u20132093 (2017).","journal-title":"J. Microbiol. Biotechnol."},{"key":"98380_CR50","first-page":"193","volume":"73","author":"MN D'Alterio","year":"2021","unstructured":"D\u2019Alterio, M. N. et al. Possible role of microbiome in the pathogenesis of endometriosis. Minerva Obstet. Gynecol. 73, 193\u2013214 (2021).","journal-title":"Minerva Obstet. Gynecol."},{"key":"98380_CR51","doi-asserted-by":"publisher","first-page":"1","DOI":"10.21767\/2476-1974.100036","volume":"02","author":"MA Cregger","year":"2017","unstructured":"Cregger, M. A. et al. Reproductive microbiomes: Using the microbiome as a novel diagnostic tool for endometriosis. Reprod. Immunol. Open Access 02, 1\u20137 (2017).","journal-title":"Reprod. Immunol. Open Access"},{"key":"98380_CR52","doi-asserted-by":"publisher","first-page":"72","DOI":"10.1002\/rmb2.12250","volume":"18","author":"K Kyono","year":"2019","unstructured":"Kyono, K., Hashimoto, T., Kikuchi, S., Nagai, Y. & Sakuraba, Y. A pilot study and case reports on endometrial microbiota and pregnancy outcome: An analysis using 16S rRNA gene sequencing among IVF patients, and trial therapeutic intervention for dysbiotic endometrium. Reprod. Med. Biol. 18, 72\u201382 (2019).","journal-title":"Reprod. Med. Biol."},{"key":"98380_CR53","doi-asserted-by":"publisher","first-page":"1743","DOI":"10.1373\/clinchem.2018.289306","volume":"64","author":"Y Liu","year":"2018","unstructured":"Liu, Y. et al. Systematic comparison of bacterial colonization of endometrial tissue and fluid samples in recurrent miscarriage patients: Implications for future endometrial microbiome studies. Clin. Chem. 64, 1743\u20131752 (2018).","journal-title":"Clin. Chem."},{"key":"98380_CR54","doi-asserted-by":"publisher","first-page":"121","DOI":"10.1016\/j.cell.2014.03.011","volume":"157","author":"Y Belkaid","year":"2014","unstructured":"Belkaid, Y. & Hand, T. W. Role of the microbiota in immunity and inflammation. Cell 157, 121\u2013141 (2014).","journal-title":"Cell"},{"key":"98380_CR55","first-page":"1","volume":"6","author":"K Aagaard","year":"2014","unstructured":"Aagaard, K. et al. The placenta harbors a unique microbiome. Sci. Transl. Med. 6, 1\u201312 (2014).","journal-title":"Sci. Transl. Med."},{"key":"98380_CR56","doi-asserted-by":"publisher","first-page":"2446","DOI":"10.1093\/humrep\/deu222","volume":"29","author":"KN Khan","year":"2014","unstructured":"Khan, K. N. et al. Intra-uterine microbial colonization and occurrence of endometritis in women with endometriosis\u2020. Hum. Reprod. 29, 2446\u20132456 (2014).","journal-title":"Hum. Reprod."},{"key":"98380_CR57","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1038\/s41598-019-39700-6","volume":"9","author":"B Ata","year":"2019","unstructured":"Ata, B. et al. The endobiota study: comparison of vaginal, cervical and gut microbiota between women with stage 3\/4 endometriosis and healthy controls. Sci. Rep. 9, 1\u20139 (2019).","journal-title":"Sci. Rep."},{"key":"98380_CR58","doi-asserted-by":"publisher","first-page":"1","DOI":"10.21037\/atm-20-1309","volume":"8","author":"S Chen","year":"2020","unstructured":"Chen, S. et al. Microbiome of the lower genital tract in Chinese women with endometriosis by 16s-rRNA sequencing technique: A pilot study. Ann. Transl. Med. 8, 1\u201313 (2020).","journal-title":"Ann. Transl. Med."},{"key":"98380_CR59","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1111\/aji.13147","volume":"82","author":"K Akiyama","year":"2019","unstructured":"Akiyama, K. et al. Molecular detection of microbial colonization in cervical mucus of women with and without endometriosis. Am. J. Reprod. Immunol. 82, 1\u20139 (2019).","journal-title":"Am. J. Reprod. Immunol."},{"key":"98380_CR60","doi-asserted-by":"publisher","first-page":"2367","DOI":"10.1007\/s43032-021-00506-5","volume":"28","author":"A Svensson","year":"2021","unstructured":"Svensson, A., Brunkwall, L., Roth, B., Orho-Melander, M. & Ohlsson, B. Associations between endometriosis and gut microbiota. Reprod. Sci. 28, 2367\u20132377 (2021).","journal-title":"Reprod. Sci."},{"key":"98380_CR61","doi-asserted-by":"publisher","DOI":"10.1007\/s00404-021-06057-z","author":"J Shan","year":"2021","unstructured":"Shan, J., Ni, Z., Cheng, W., Zhou, L., Zhai, D., Sun, S. & Yu, C. Gut microbiota imbalance and its correlations with hormone and inflammatory factors in patients with stage 3\/4 endometriosis. Arch. Gynecol. Obstet. https:\/\/doi.org\/10.1007\/s00404-021-06057-z (2021).","journal-title":"Arch. Gynecol. Obstet."},{"key":"98380_CR62","doi-asserted-by":"publisher","first-page":"1064","DOI":"10.1007\/s43032-019-00113-5","volume":"27","author":"AR Perrotta","year":"2020","unstructured":"Perrotta, A. R. et al. The vaginal microbiome as a tool to predict rASRM stage of disease in endometriosis: A pilot study. Reprod. Sci. 27, 1064\u20131073 (2020).","journal-title":"Reprod. Sci."},{"key":"98380_CR63","doi-asserted-by":"publisher","first-page":"1","DOI":"10.3389\/fcimb.2020.00467","volume":"10","author":"Y Moosa","year":"2020","unstructured":"Moosa, Y., Kwon, D., de Oliveira, T. & Wong, E. B. Determinants of vaginal microbiota composition. Front. Cell Infect. Microbiol. 10, 1\u20139 (2020).","journal-title":"Front. Cell Infect. Microbiol."},{"key":"98380_CR64","doi-asserted-by":"publisher","first-page":"220","DOI":"10.1038\/nature11550","volume":"489","author":"CA Lozupone","year":"2012","unstructured":"Lozupone, C. A., Stombaugh, J. I., Gordon, J. I., Jansson, J. K. & Knight, R. Diversity, stability and resilience of the human gut microbiota. Nature 489, 220\u2013230 (2012).","journal-title":"Nature"},{"issue":"68","key":"98380_CR65","first-page":"e1","volume":"215","author":"MW Laschke","year":"2016","unstructured":"Laschke, M. W. & Menger, M. D. The gut microbiota: A puppet master in the pathogenesis of endometriosis?. Am. J. Obstet. Gynecol. 215(68), e1\u2013e4 (2016).","journal-title":"Am. J. Obstet. Gynecol."},{"key":"98380_CR66","doi-asserted-by":"publisher","first-page":"1010","DOI":"10.1080\/09513590.2020.1766440","volume":"36","author":"D Vigan\u00f3","year":"2020","unstructured":"Vigan\u00f3, D. et al. How is small bowel permeability in endometriosis patients? A case control pilot study. Gynecol. Endocrinol. 36, 1010\u20131014 (2020).","journal-title":"Gynecol. Endocrinol."},{"key":"98380_CR67","doi-asserted-by":"publisher","first-page":"839","DOI":"10.1016\/S0140-6736(21)00389-5","volume":"397","author":"HS Taylor","year":"2021","unstructured":"Taylor, H. S., Kotlyar, A. M. & Flores, V. A. Endometriosis is a chronic systemic disease: Clinical challenges and novel innovations. Lancet 397, 839\u2013852 (2021).","journal-title":"Lancet"},{"key":"98380_CR68","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1371\/journal.pone.0226835","volume":"14","author":"J Hantschel","year":"2019","unstructured":"Hantschel, J. et al. Effect of endometriosis on the fecal bacteriota composition of mice during the acute phase of lesion formation. PLoS ONE 14, 1\u201312 (2019).","journal-title":"PLoS ONE"},{"key":"98380_CR69","doi-asserted-by":"publisher","first-page":"1704","DOI":"10.1093\/humrep\/17.7.1704","volume":"17","author":"MT Bailey","year":"2002","unstructured":"Bailey, M. T. & Coe, C. L. Endometriosis is associated with an altered profile of intestinal microflora in female rhesus monkeys. Hum. Reprod. 17, 1704\u20131708 (2002).","journal-title":"Hum. Reprod."},{"key":"98380_CR70","doi-asserted-by":"publisher","first-page":"607","DOI":"10.1093\/humrep\/dex372","volume":"33","author":"M Yuan","year":"2018","unstructured":"Yuan, M. et al. Endometriosis induces gut microbiota alterations in mice. Hum. Reprod. 33, 607\u2013616 (2018).","journal-title":"Hum. Reprod."},{"key":"98380_CR71","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1111\/aji.13307","volume":"84","author":"Z Ni","year":"2020","unstructured":"Ni, Z. et al. Correlation of fecal metabolomics and gut microbiota in mice with endometriosis. Am. J. Reprod. Immunol. 84, 1\u201314 (2020).","journal-title":"Am. J. Reprod. Immunol."},{"key":"98380_CR72","first-page":"1","volume":"2020","author":"Y Cao","year":"2020","unstructured":"Cao, Y., Jiang, C., Jia, Y., Xu, D. & Yu, Y. Letrozole and the traditional Chinese medicine, Shaofu Zhuyu decoction, reduce endometriotic disease progression in rats: A potential role for gut microbiota. Evid. Based Complement Alternat. Med. 2020, 1\u201314 (2020).","journal-title":"Evid. Based Complement Alternat. Med."},{"key":"98380_CR73","doi-asserted-by":"publisher","first-page":"1106","DOI":"10.1093\/humrep\/dez041","volume":"34","author":"SB Chadchan","year":"2019","unstructured":"Chadchan, S. B. et al. Antibiotic therapy with metronidazole reduces endometriosis disease progression in mice: A potential role for gut microbiota. Hum. Reprod. 34, 1106\u20131116 (2019).","journal-title":"Hum. Reprod."},{"key":"98380_CR74","first-page":"1","volume":"95","author":"WC Lin","year":"2016","unstructured":"Lin, W. C., Chang, C. Y. Y., Hsu, Y. A., Chiang, J. H. & Wan, L. Increased risk of endometriosis in patients with lower genital tract infection: A nationwide cohort study. Medicine (United States) 95, 1\u20138 (2016).","journal-title":"Medicine (United States)"},{"key":"98380_CR75","doi-asserted-by":"publisher","first-page":"1","DOI":"10.3390\/jcm7110379","volume":"7","author":"FW Tai","year":"2018","unstructured":"Tai, F. W., Chang, C. Y. Y., Chiang, J. H., Lin, W. C. & Wan, L. Association of pelvic inflammatory disease with risk of endometriosis: A nationwide cohort study involving 141,460 individuals. J. Clin. Med. 7, 1\u201311 (2018).","journal-title":"J. Clin. Med."},{"key":"98380_CR76","first-page":"209","volume":"11","author":"PR Koninckx","year":"2019","unstructured":"Koninckx, P. R. et al. Infection as a potential cofactor in the genetic-epigenetic pathophysiology of endometriosis: A systematic review. Facts Views Vis. Obgyn. 11, 209\u2013216 (2019).","journal-title":"Facts Views Vis. Obgyn."},{"key":"98380_CR77","doi-asserted-by":"publisher","first-page":"69","DOI":"10.1016\/j.ejogrb.2016.01.040","volume":"199","author":"KN Khan","year":"2016","unstructured":"Khan, K. N. et al. Molecular detection of intrauterine microbial colonization in women with endometriosis. Eur. J. Obstet. Gynecol. Reprod. Biol. 199, 69\u201375 (2016).","journal-title":"Eur. J. Obstet. Gynecol. Reprod. Biol."},{"key":"98380_CR78","first-page":"1","volume":"22","author":"S-R Lee","year":"2021","unstructured":"Lee, S.-R. et al. Altered composition of microbiota in women with ovarian endometrioma: Microbiome analyses of extracellular vesicles in the peritoneal fluid. Int. J. Mol. Sci. 22, 1\u201312 (2021).","journal-title":"Int. J. Mol. Sci."},{"key":"98380_CR79","doi-asserted-by":"publisher","first-page":"695","DOI":"10.1007\/s00705-010-0643-y","volume":"155","author":"AL Vestergaard","year":"2010","unstructured":"Vestergaard, A. L. et al. Low prevalence of DNA viruses in the human endometrium and endometriosis. Arch. Virol. 155, 695\u2013703 (2010).","journal-title":"Arch. Virol."}],"container-title":["Scientific Reports"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.nature.com\/articles\/s41598-021-98380-3.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/www.nature.com\/articles\/s41598-021-98380-3","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/www.nature.com\/articles\/s41598-021-98380-3.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2024,9,8]],"date-time":"2024-09-08T14:59:12Z","timestamp":1725807552000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.nature.com\/articles\/s41598-021-98380-3"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2021,9,23]]},"references-count":79,"journal-issue":{"issue":"1","published-online":{"date-parts":[[2021,12]]}},"alternative-id":["98380"],"URL":"https:\/\/doi.org\/10.1038\/s41598-021-98380-3","relation":{},"ISSN":["2045-2322"],"issn-type":[{"value":"2045-2322","type":"electronic"}],"subject":[],"published":{"date-parts":[[2021,9,23]]},"assertion":[{"value":"1 June 2021","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"2 September 2021","order":2,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"23 September 2021","order":3,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"The authors declare no competing interests.","order":1,"name":"Ethics","group":{"name":"EthicsHeading","label":"Competing interests"}}],"article-number":"18877"}}