{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,22]],"date-time":"2026-10-22T23:56:53Z","timestamp":1792713413948,"version":"4.5.0"},"reference-count":135,"publisher":"Frontiers Media SA","license":[{"start":{"date-parts":[[2022,12,16]],"date-time":"2022-12-16T00:00:00Z","timestamp":1671148800000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":["frontiersin.org"],"crossmark-restriction":true},"short-container-title":["Front. Cell. Infect. Microbiol."],"abstract":"<jats:p>Every year, millions of women are affected by genital tract disorders, such as bacterial vaginosis (BV), endometrial cancer, polycystic ovary syndrome (PCOS), endometriosis, and uterine fibroids (UFs). These disorders pose a significant economic burden on healthcare systems and have serious implications for health and fertility outcomes. This review explores the relationships between gut, vaginal, and uterine dysbiosis and the pathogenesis of various diseases of the female genital tract. In recent years, reproductive health clinicians and scientists have focused on the microbiome to investigate its role in the pathogenesis and prevention of such diseases. Recent studies of the gut, vaginal, and uterine microbiomes have identified patterns in bacterial composition and changes across individuals\u2019 lives associated with specific healthy and diseased states, particularly regarding the effects of the estrogen\u2013gut microbiome axis on estrogen-driven disorders (such as endometrial cancer, endometriosis, and UFs) and disorders associated with estrogen deficiency (such as PCOS). Furthermore, this review discusses the contribution of vitamin D deficiency to gut dysbiosis and altered estrogen metabolism as well as how these changes play key roles in the pathogenesis of UFs. More research on the microbiome influences on reproductive health and fertility is vital.<\/jats:p>","DOI":"10.3389\/fcimb.2022.1059825","type":"journal-article","created":{"date-parts":[[2022,12,16]],"date-time":"2022-12-16T05:30:10Z","timestamp":1671168610000},"update-policy":"https:\/\/doi.org\/10.3389\/crossmark-policy","source":"Crossref","is-referenced-by-count":106,"title":["Gut and genital tract microbiomes: Dysbiosis and link to gynecological disorders"],"prefix":"10.3389","volume":"12","author":[{"given":"Hoda","family":"Elkafas","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Melinique","family":"Walls","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ayman","family":"Al-Hendy","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Nahed","family":"Ismail","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1965","published-online":{"date-parts":[[2022,12,16]]},"reference":[{"key":"B1","doi-asserted-by":"publisher","DOI":"10.3389\/fmicb.2020.578007","article-title":"Endobolome, a new concept for determining the influence of microbiota disrupting chemicals (MDC) in relation to specific endocrine pathogenesis","volume":"11","author":"Aguilera","year":"2020","journal-title":"Front. Microbiol."},{"key":"B2","doi-asserted-by":"publisher","first-page":"473","DOI":"10.1055\/s-0037-1607264","article-title":"Uterine fibroids: burden and unmet medical need","volume":"35","author":"Al-Hendy","year":"2017","journal-title":"Semin. Reprod. Med."},{"key":"B3","doi-asserted-by":"publisher","first-page":"686","DOI":"10.1016\/j.fertnstert.2006.01.052","article-title":"Ethnic distribution of estrogen receptor-\u03b1 polymorphism is associated with a higher prevalence of uterine leiomyomas in black americans","volume":"86","author":"Al-Hendy","year":"2006","journal-title":"Fertil. Steril."},{"key":"B4","doi-asserted-by":"publisher","first-page":"1136","DOI":"10.1111\/apt.12706","article-title":"Higher plasma vitamin d is associated with reduced risk of Clostridium difficile infection in patients with inflammatory bowel diseases","volume":"39","author":"Ananthakrishnan","year":"2014","journal-title":"Aliment. Pharmacol. Ther."},{"key":"B5","doi-asserted-by":"publisher","first-page":"133","DOI":"10.1515\/bmc-2019-0017","article-title":"Endometriosis pathoetiology and pathophysiology: roles of vitamin a, estrogen, immunity, adipocytes, gut microbiome and melatonergic pathway on mitochondria regulation","volume":"10","author":"Anderson","year":"2019","journal-title":"Biomol. Concepts"},{"key":"B6","doi-asserted-by":"publisher","first-page":"101159","DOI":"10.1016\/j.ctcp.2020.101159","article-title":"Effect of oral consumption of vitamin d on uterine fibroids: a randomized clinical trial","volume":"39","author":"Arjeh","year":"2020","journal-title":"Complementary therapies Clin. Pract."},{"key":"B7","doi-asserted-by":"publisher","first-page":"83","DOI":"10.3390\/cancers10030083","article-title":"The complex interplay between chronic inflammation, the microbiome, and cancer: understanding disease progression and what we can do to prevent it","volume":"10","author":"Armstrong","year":"2018","journal-title":"Cancers"},{"key":"B8","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1038\/s41598-019-39700-6","article-title":"The endobiota study: comparison of vaginal, cervical, and gut microbiota between women with stage 3\/4 endometriosis and healthy controls","volume":"9","author":"Ata","year":"2019","journal-title":"Sci. Rep."},{"key":"B9","doi-asserted-by":"publisher","first-page":"1704","DOI":"10.1093\/humrep\/17.7.1704","article-title":"Endometriosis is associated with an altered profile of intestinal microflora in female rhesus monkeys","volume":"17","author":"Bailey","year":"2002","journal-title":"Hum. Reprod."},{"key":"B10","doi-asserted-by":"publisher","first-page":"45","DOI":"10.1016\/j.maturitas.2017.06.025","article-title":"Estrogen\u2013gut microbiome axis: physiological and clinical implications","volume":"103","author":"Baker","year":"2017","journal-title":"Maturitas"},{"key":"B11","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":"Frontiers in immunology"},{"key":"B12","doi-asserted-by":"publisher","first-page":"437","DOI":"10.1002\/ijc.28364","article-title":"Genetic variation in the TLR and NF-KB pathways and cervical and vulvar cancer risk: a population-based case-control study","volume":"134","author":"Bodelon","year":"2014","journal-title":"Int. J. Cancer."},{"key":"B13","doi-asserted-by":"publisher","first-page":"987","DOI":"10.1021\/acsinfecdis.0c00839","article-title":"Gut microbiota and gynecological cancers: a summary of pathogenetic mechanisms and future directions","volume":"7","author":"Borella","year":"2021","journal-title":"ACS Infect. Dis."},{"key":"B14","doi-asserted-by":"publisher","first-page":"698","DOI":"10.1016\/j.fertnstert.2015.05.031","article-title":"Role of vitamin d in uterine fibroid biology","volume":"104","author":"Brakta","year":"2015","journal-title":"Fertility sterility"},{"key":"B15","doi-asserted-by":"publisher","first-page":"258","DOI":"10.3322\/caac.21561","article-title":"Current recommendations and recent progress in endometrial cancer","volume":"69","author":"Brooks","year":"2019","journal-title":"CA: Cancer J. Clin."},{"key":"B16","first-page":"74","article-title":"MedEsperaInternational Medical Congress for Students and Young Doctors. 7, 3-5 mai 2018","volume-title":"Characterization of the human endometrial microbiome and its risks associated in infertility patients: a systematic review","author":"Burac","year":"2018"},{"key":"B17","doi-asserted-by":"publisher","first-page":"729","DOI":"10.1097\/JIM.0000000000000192","article-title":"Gut microbiota in multiple sclerosis: possible influence of immunomodulators","volume":"63","author":"Cantarel","year":"2015","journal-title":"J. Invest. Med."},{"key":"B18","doi-asserted-by":"publisher","first-page":"1524","DOI":"10.1177\/1535370214523890","article-title":"Vitamin d, immune regulation, the microbiota, and inflammatory bowel disease","volume":"239","author":"Cantorna","year":"2014","journal-title":"Exp. Biol. Med."},{"key":"B19","doi-asserted-by":"publisher","first-page":"8571","DOI":"10.2147\/CMAR.S217362","article-title":"Atopobium vaginae and Porphyromonas somerae induce proinflammatory cytokines expression in endometrial cells: a possible implication for endometrial cancer","volume":"11","author":"Caselli","year":"2019","journal-title":"Cancer Manage. Res."},{"key":"B20","doi-asserted-by":"publisher","first-page":"R81","DOI":"10.1530\/JME-21-0238","article-title":"Female reproductive dysfunctions and the gut microbiota","volume":"69","author":"Chadchan","year":"2022","journal-title":"J. Mol. Endocrinol."},{"key":"B21","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1007\/s11912-021-01079-x","article-title":"The microbiome and gynecologic cancer: current evidence and future opportunities","volume":"23","author":"Chambers","year":"2021","journal-title":"Curr. Oncol. Rep."},{"key":"B22","doi-asserted-by":"publisher","first-page":"309","DOI":"10.1111\/1471-0528.14631","article-title":"The role of the vaginal microbiome in gynaecological cancer","volume":"125","author":"Champer","year":"2018","journal-title":"BJOG"},{"key":"B23","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1038\/s41467-017-00901-0","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":"B24","doi-asserted-by":"publisher","first-page":"2051","DOI":"10.3390\/ijms19072051","article-title":"Vitamin d and uterine fibroids\u2013review of the literature and novel concepts","volume":"19","author":"Ciebiera","year":"2018","journal-title":"Int. J. Mol. Sci."},{"key":"B25","doi-asserted-by":"publisher","DOI":"10.3389\/fimmu.2016.00627","article-title":"Role of vitamin d in the hygiene hypothesis: the interplay between vitamin d, vitamin d receptors, gut microbiota, and immune response","volume":"7","author":"Clark","year":"2016","journal-title":"Front. Immunol."},{"key":"B26","doi-asserted-by":"publisher","first-page":"S222","DOI":"10.4103\/0019-5545.161483","article-title":"Postmenopausal syndrome","volume":"57","author":"Dalal","year":"2015","journal-title":"Indian J. Psychiatry"},{"key":"B27","doi-asserted-by":"publisher","first-page":"18","DOI":"10.1007\/s13679-017-0240-4","article-title":"Endocrine disruptors and obesity","volume":"6","author":"Darbre","year":"2017","journal-title":"Curr. Obes. Rep."},{"key":"B28","doi-asserted-by":"publisher","first-page":"1829","DOI":"10.3945\/jn.112.161711","article-title":"Endogenous and exogenous equol are antiestrogenic in reproductive tissues of apolipoprotein e-null mice","volume":"142","author":"Dewi","year":"2012","journal-title":"J. Nutr."},{"key":"B29","doi-asserted-by":"publisher","first-page":"293","DOI":"10.1210\/er.2009-0002","article-title":"Endocrine-disrupting chemicals: an endocrine society scientific statement","volume":"30","author":"Diamanti-Kandarakis","year":"2009","journal-title":"Endocrine Rev."},{"key":"B30","doi-asserted-by":"publisher","first-page":"1337","DOI":"10.5897\/AJMR2016.8046","article-title":"Gut bacterial microbiota in psoriasis: a case control study","volume":"10","author":"Doaa","year":"2016","journal-title":"Afr. J. Microbiol. Res."},{"key":"B31","doi-asserted-by":"publisher","first-page":"11971","DOI":"10.1073\/pnas.1002601107","article-title":"Delivery mode shapes the acquisition and structure of the initial microbiota across multiple body habitats in newborns","volume":"107","author":"Dominguez-Bello","year":"2010","journal-title":"Proc. Natl. Acad. Sci."},{"key":"B32","doi-asserted-by":"publisher","first-page":"503","DOI":"10.2147\/IJWH.S163961","article-title":"Diet-induced vitamin d deficiency triggers inflammation and DNA damage profile in murine myometrium","volume":"10","author":"ElHusseini","year":"2018","journal-title":"Int. J. women\u2019s Health"},{"key":"B33","doi-asserted-by":"crossref","first-page":"101","DOI":"10.1016\/B978-0-12-801238-3.64527-0","article-title":"Leiomyomas","volume-title":"Encyclopedia of reproduction","author":"ElKafas","year":"2018"},{"key":"B34","doi-asserted-by":"publisher","first-page":"e100","DOI":"10.1016\/j.fertnstert.2019.07.382","article-title":"Targeting activated pro-inflammatory pathway in primed myometrial stem cells with vitamin D3 and paricalcitol","volume":"112","author":"Elkafas","year":"2019","journal-title":"Fertility Sterility"},{"key":"B35","doi-asserted-by":"crossref","first-page":"260","DOI":"10.21608\/aprh.2021.66748.1124","article-title":"Endocrine-Disrupting Chemicals and Vitamin D Deficiency in the Pathogenesis of Uterine Fibroids","volume":"5","author":"Elkafas","year":"2021","journal-title":"Journal of advanced pharmacy research"},{"key":"B36","doi-asserted-by":"publisher","first-page":"481","DOI":"10.1055\/s-0037-1607205","article-title":"Origin of uterine fibroids: conversion of myometrial stem cells to tumor-initiating cells","volume":"35","author":"Elkafas","year":"2017","journal-title":"Semin. Reprod. Med."},{"key":"B37","doi-asserted-by":"publisher","first-page":"194","DOI":"10.1016\/j.ajog.2013.08.008","article-title":"The health disparities of uterine fibroid tumors for African American women: a public health issue","volume":"210","author":"Eltoukhi","year":"2014","journal-title":"Am. J. obstetrics gynecology"},{"key":"B38","doi-asserted-by":"publisher","DOI":"10.3389\/fonc.2020.00120","article-title":"Microbiome and breast cancer: new role for an ancient population","volume":"10","author":"Eslami-S","year":"2020","journal-title":"Front. Oncol."},{"key":"B39","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pone.0092193","article-title":"Exercise prevents weight gain and alters the gut microbiota in a mouse model of high fat diet-induced obesity","volume":"9","author":"Evans","year":"2014","journal-title":"PLos One"},{"key":"B40","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pone.0039745","article-title":"Association of fecal microbial diversity and taxonomy with selected enzymatic functions","volume":"7","author":"Flores","year":"2012","journal-title":"PLos One"},{"key":"B41","doi-asserted-by":"publisher","first-page":"1341","DOI":"10.1016\/j.fertnstert.2015.10.021","article-title":"Introduction: microbiome in human reproduction","volume":"104","author":"Franasiak","year":"2015","journal-title":"Fertility sterility"},{"key":"B42","doi-asserted-by":"publisher","first-page":"129","DOI":"10.1007\/s10815-015-0614-z","article-title":"Endometrial microbiome at the time of embryo transfer: next-generation sequencing of the 16S ribosomal subunit","volume":"33","author":"Franasiak","year":"2016","journal-title":"J. assisted Reprod. Genet."},{"key":"B43","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1186\/1471-2172-8-5","article-title":"Vitamin d and the vitamin d receptor are critical for control of the innate immune response to colonic injury","volume":"8","author":"Froicu","year":"2007","journal-title":"BMC Immunol."},{"key":"B44","doi-asserted-by":"publisher","first-page":"4632","DOI":"10.1210\/jc.2014-2222","article-title":"Associations of the fecal microbiome with urinary estrogens and estrogen metabolites in postmenopausal women","volume":"99","author":"Fuhrman","year":"2014","journal-title":"J. Clin. Endocrinol. Metab."},{"key":"B45","doi-asserted-by":"publisher","first-page":"392","DOI":"10.1038\/nm.4517","article-title":"Current understanding of the human microbiome","volume":"24","author":"Gilbert","year":"2018","journal-title":"Nat. Med."},{"key":"B46","doi-asserted-by":"publisher","first-page":"3","DOI":"10.1002\/ijgo.13102","article-title":"Epidemiology and management of uterine fibroids","volume":"149","author":"Giuliani","year":"2020","journal-title":"Int. J. Gynecology Obstetrics."},{"key":"B47","doi-asserted-by":"publisher","first-page":"554","DOI":"10.1016\/j.tem.2021.04.014","article-title":"Gut and vaginal microbiomes on steroids: implications for women\u2019s health","volume":"32","author":"Graham","year":"2021","journal-title":"Trends Endocrinol. Metab."},{"key":"B48","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pone.0153196","article-title":"Association between polycystic ovary syndrome and gut microbiota","volume":"11","author":"Guo","year":"2016","journal-title":"PLos One"},{"key":"B49","doi-asserted-by":"publisher","first-page":"103696","DOI":"10.1016\/j.micpath.2019.103696","article-title":"Crosstalk between vaginal microbiome and female health: a review","volume":"136","author":"Gupta","year":"2019","journal-title":"Microbial pathogenesis"},{"key":"B50","doi-asserted-by":"publisher","first-page":"151","DOI":"10.1095\/biolreprod.113.107714","article-title":"1, 25-dihydroxyvitamin d3 reduces extracellular matrix-associated protein expression in human uterine fibroid cells","volume":"150","author":"Halder","year":"2013","journal-title":"Biol. Reprod. 89(6)"},{"key":"B51","doi-asserted-by":"publisher","first-page":"2407","DOI":"10.1093\/humrep\/det265","article-title":"Vitamin D3 inhibits expression and activities of matrix metalloproteinase-2 and-9 in human uterine fibroid cells","volume":"28","author":"Halder","year":"2013","journal-title":"Hum. Reprod."},{"key":"B52","doi-asserted-by":"publisher","first-page":"e7502","DOI":"10.7717\/peerj.7502","article-title":"Factors affecting the composition of the gut microbiota, and its modulation","volume":"7","author":"Hasan","year":"2019","journal-title":"PeerJ."},{"key":"B53","doi-asserted-by":"publisher","first-page":"163","DOI":"10.3390\/diagnostics10030163","article-title":"Microbiome profile of deep endometriosis patients: comparison of vaginal fluid, endometrium and lesion","volume":"10","author":"Hernandes","year":"2020","journal-title":"Diagnostics"},{"key":"B54","doi-asserted-by":"publisher","first-page":"52","DOI":"10.1111\/cen.14198","article-title":"Association between polycystic ovary syndrome and the vaginal microbiome: a case-control study","volume":"93","author":"Hong","year":"2020","journal-title":"Clin. Endocrinol."},{"key":"B55","doi-asserted-by":"publisher","first-page":"643","DOI":"10.1210\/endrev\/bnaa012","article-title":"Selective progesterone receptor modulators\u2013mechanisms and therapeutic utility","volume":"41","author":"Islam","year":"2020","journal-title":"Endocrine Rev."},{"key":"B56","doi-asserted-by":"publisher","first-page":"735","DOI":"10.1016\/j.bpobgyn.2008.01.010","article-title":"Management of symptomatic fibroids: conservative surgical treatment modalities other than abdominal or laparoscopic myomectomy","volume":"22","author":"Istre","year":"2008","journal-title":"Best Pract. Res. Clin. Obstetrics Gynaecology"},{"key":"B57","doi-asserted-by":"publisher","first-page":"5644","DOI":"10.3390\/ijms22115644","article-title":"Intricate connections between the microbiota and endometriosis","volume":"22","author":"Jiang","year":"2021","journal-title":"Int. J. Mol. Sci."},{"key":"B58","doi-asserted-by":"publisher","first-page":"2446","DOI":"10.1093\/humrep\/deu222","article-title":"Intra-uterine microbial colonization and occurrence of endometritis in women with endometriosis","volume":"29","author":"Khan","year":"2014","journal-title":"Hum. Reprod."},{"key":"B59","doi-asserted-by":"publisher","first-page":"431","DOI":"10.33073\/pjm-2021-043","article-title":"Can Lactobacillus spp. be a factor reducing the risk of miscarriage","volume":"70","author":"Kiecka","year":"2021","journal-title":"Polish J. Microbiol."},{"key":"B60","doi-asserted-by":"publisher","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":"Fertility sterility."},{"key":"B61","doi-asserted-by":"publisher","first-page":"1473","DOI":"10.1007\/s00404-011-2047-y","article-title":"Relationship between endometriosis and cancer from current perspective","volume":"284","author":"Kokcu","year":"2011","journal-title":"Arch. gynecology obstetrics."},{"key":"B62","doi-asserted-by":"publisher","first-page":"228","DOI":"10.1016\/j.jsbmb.2010.02.004","article-title":"1\u03b1-hydroxylase and innate immune responses to 25-hydroxyvitamin d in colonic cell lines","volume":"121","author":"Lagishetty","year":"2010","journal-title":"J. Steroid Biochem. Mol. Biol."},{"key":"B63","doi-asserted-by":"publisher","first-page":"232","DOI":"10.1038\/s41585-020-0286-z","article-title":"The microbiome and gynaecological cancer development, prevention and therapy","volume":"17","author":"\u0141aniewski","year":"2020","journal-title":"Nat. Rev. Urol."},{"key":"B64","doi-asserted-by":"publisher","first-page":"68.e1","DOI":"10.1016\/j.ajog.2016.02.036","article-title":"The gut microbiota: a puppet master in the pathogenesis of endometriosis","volume":"215","author":"Laschke","year":"2016","journal-title":"Am. J. Obstet. Gynecol."},{"key":"B65","doi-asserted-by":"publisher","first-page":"204","DOI":"10.1055\/s-0030-1251477","article-title":"New directions in the epidemiology of uterine fibroids","volume":"28","author":"Laughlin","year":"2010","journal-title":"Semin. Reprod. Med."},{"key":"B66","doi-asserted-by":"publisher","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":"Fertility Sterility."},{"key":"B67","doi-asserted-by":"publisher","DOI":"10.3389\/fmicb.2017.00324","article-title":"Dysbiosis of gut microbiota associated with clinical parameters in polycystic ovary syndrome","volume":"8","author":"Liu","year":"2017","journal-title":"Front. Microbiol."},{"key":"B68","doi-asserted-by":"publisher","first-page":"2736","DOI":"10.3390\/ijms19092736","article-title":"The anti-inflammatory effects of vitamin d in tumorigenesis","volume":"19","author":"Liu","year":"2018","journal-title":"Int. J. Mol. Sci."},{"key":"B69","doi-asserted-by":"publisher","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":"2021","journal-title":"Int. J. Cancer."},{"key":"B70","doi-asserted-by":"publisher","first-page":"374","DOI":"10.1002\/med.20083","article-title":"The evolution of progesterone receptor ligands","volume":"27","author":"Madauss","year":"2007","journal-title":"Medicinal Res. Rev."},{"key":"B71","doi-asserted-by":"publisher","first-page":"15","DOI":"10.1016\/j.coviro.2021.10.010","article-title":"The female reproductive tract virome: understanding the dynamic role of viruses in gynecological health and disease","volume":"52","author":"Madere","year":"2022","journal-title":"Curr. Opin. Virology."},{"key":"B72","doi-asserted-by":"crossref","first-page":"207","DOI":"10.1016\/B978-0-7020-6896-6.00014-4","article-title":"The microbiota in immunity and inflammation","volume-title":"Clinical immunology","author":"Maynard","year":"2019"},{"key":"B73","doi-asserted-by":"publisher","first-page":"2934","DOI":"10.1002\/1097-0142(197706)39:6<2934::AID-CNCR2820390680>3.0.CO;2-P","article-title":"Current status of estrogen and progesterone receptors in breast cancer","volume":"39","author":"McGuire","year":"1977","journal-title":"Cancer"},{"key":"B74","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1007\/s11940-015-0344-7","article-title":"The gut microbiome in multiple sclerosis","volume":"17","author":"Mielcarz","year":"2015","journal-title":"Curr. Treat options Neurol."},{"key":"B75","doi-asserted-by":"publisher","first-page":"813","DOI":"10.1016\/j.fertnstert.2016.11.028","article-title":"Investigation of the microbiota of the reproductive tract in women undergoing a total hysterectomy and bilateral salpingo-oopherectomy","volume":"107","author":"Miles","year":"2017","journal-title":"Fertility sterility"},{"key":"B76","doi-asserted-by":"publisher","DOI":"10.3389\/fmicb.2016.01936","article-title":"Lactobacilli dominance and vaginal pH: why is the human vaginal microbiome unique","volume":"7","author":"Miller","year":"2016","journal-title":"Front. Microbiol."},{"key":"B77","doi-asserted-by":"publisher","first-page":"190","DOI":"10.1111\/j.1600-0897.2010.00943.x","article-title":"The effects of commensal bacteria on innate immune responses in the female genital tract","volume":"65","author":"Mirmonsef","year":"2011","journal-title":"Am. J. Reprod. Immunol."},{"key":"B78","doi-asserted-by":"publisher","first-page":"611. e1","DOI":"10.1016\/j.ajog.2014.11.043","article-title":"Colonization of the upper genital tract by vaginal bacterial species in nonpregnant women","volume":"212","author":"Mitchell","year":"2015","journal-title":"Am. J. obstetrics gynecology"},{"key":"B79","doi-asserted-by":"publisher","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. obstetrics gynecology"},{"key":"B80","doi-asserted-by":"publisher","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":"B81","doi-asserted-by":"publisher","first-page":"40","DOI":"10.1002\/rmb2.12249","article-title":"Deciphering the effect of reproductive tract microbiota on human reproduction","volume":"18","author":"Moreno","year":"2019","journal-title":"Reprod. Med. Biol."},{"key":"B82","doi-asserted-by":"publisher","first-page":"163","DOI":"10.1023\/A:1014820500738","article-title":"Loss of co-ordinate expression of progesterone receptors a and b is an early event in breast carcinogenesis","volume":"72","author":"Mote","year":"2002","journal-title":"Breast Cancer Res. Treat"},{"key":"B83","doi-asserted-by":"publisher","first-page":"159","DOI":"10.1080\/19490976.2018.1494466","article-title":"Intestinal luminal putrescine is produced by collective biosynthetic pathways of the commensal microbiome","volume":"10","author":"Nakamura","year":"2019","journal-title":"Gut Microbes"},{"key":"B84","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pone.0108924","article-title":"Fecal bacterial community changes associated with isoflavone metabolites in postmenopausal women after soy bar consumption","volume":"9","author":"Nakatsu","year":"2014","journal-title":"PLos One"},{"key":"B85","doi-asserted-by":"publisher","first-page":"848","DOI":"10.1126\/science.1127059","article-title":"Escherichia coli induces DNA double-strand breaks in eukaryotic cells","volume":"313","author":"Nougayr\u00e8de","year":"2006","journal-title":"Science"},{"key":"B86","doi-asserted-by":"publisher","first-page":"17053","DOI":"10.1073\/pnas.1313650110","article-title":"Paracrine activation of WNT\/\u03b2-catenin pathway in uterine leiomyoma stem cells promotes tumor growth","volume":"110","author":"Ono","year":"2013","journal-title":"Proc. Natl. Acad. Sci."},{"key":"B87","doi-asserted-by":"publisher","first-page":"1799","DOI":"10.1093\/humrep\/der108","article-title":"Microbial colonization of follicular fluid: alterations in cytokine expression and adverse assisted reproduction technology outcomes","volume":"26","author":"Pelzer","year":"2011","journal-title":"Hum. Reprod."},{"key":"B88","doi-asserted-by":"publisher","first-page":"324","DOI":"10.1016\/j.chom.2011.10.003","article-title":"Microbiome and malignancy","volume":"10","author":"Plottel","year":"2011","journal-title":"Cell Host Microbe"},{"key":"B89","doi-asserted-by":"publisher","first-page":"735","DOI":"10.1093\/biolre\/ioy097","article-title":"Endocrine disruptor exposure during development increases incidence of uterine fibroids by altering DNA repair in myometrial stem cells","volume":"99","author":"Prusinski Fernung","year":"2018","journal-title":"Biol. Reprod."},{"key":"B90","doi-asserted-by":"publisher","first-page":"2519","DOI":"10.1007\/s10815-021-02247-5","article-title":"The impact of the female genital tract microbiome in women health and reproduction: a review","volume":"38","author":"Punz\u00f3n-Jim\u00e9nez","year":"2021","journal-title":"J. Assisted Reprod. Genet."},{"key":"B91","doi-asserted-by":"publisher","first-page":"9","DOI":"10.1155\/2022\/3934877","article-title":"Effect of ejiao (Asini corii colla) and turtle carapace glue on gut microbiota in nude mice with uterine fibroids based on high-throughput sequencing of 16SrRNA gene","volume":"2022","author":"Qiu","year":"2022","journal-title":"Evidence-Based Complementary Altern. Med"},{"key":"B92","doi-asserted-by":"publisher","first-page":"1894070","DOI":"10.1080\/19490976.2021.1894070","article-title":"The impact of the gut microbiota on the reproductive and metabolic endocrine system","volume":"13","author":"Qi","year":"2021","journal-title":"Gut Microbes"},{"key":"B93","doi-asserted-by":"publisher","first-page":"3073","DOI":"10.1007\/s43032-021-00583-6","article-title":"Combination of dydrogesterone and antibiotic versus antibiotic alone for chronic endometritis: a randomized controlled trial study","volume":"28","author":"Qu","year":"2021","journal-title":"Reprod. Sci."},{"key":"B94","doi-asserted-by":"publisher","first-page":"4680","DOI":"10.1073\/pnas.1002611107","article-title":"Vaginal microbiome of reproductive-age women","author":"Ravel","year":"2011","journal-title":"Proc. Natl. Acad. Sci. 108(Supplement"},{"key":"B95","doi-asserted-by":"publisher","first-page":"17915","DOI":"10.18632\/oncotarget.24681","article-title":"Microbiota effects on cancer: from risks to therapies","volume":"9","author":"Rea","year":"2018","journal-title":"Oncotarget."},{"key":"B96","doi-asserted-by":"publisher","first-page":"13","DOI":"10.1016\/j.bpobgyn.2015.11.015","article-title":"Hormones and pathogenesis of uterine fibroids","volume":"34","author":"Reis","year":"2016","journal-title":"Best Pract. Res. Clin. Obstetrics Gynaecology"},{"key":"B97","doi-asserted-by":"publisher","first-page":"1263","DOI":"10.1111\/bph.13622","article-title":"The potential health effects of dietary phytoestrogens","volume":"174","author":"Rietjens","year":"2017","journal-title":"Br. J. Pharmacol."},{"key":"B98","doi-asserted-by":"publisher","first-page":"14","DOI":"10.3390\/microorganisms7010014","article-title":"What is the healthy gut microbiota composition? a changing ecosystem across age, environment, diet, and diseases","volume":"7","author":"Rinninella","year":"2019","journal-title":"Microorganisms"},{"key":"B99","doi-asserted-by":"publisher","first-page":"2564","DOI":"10.3390\/nu11112564","article-title":"Impact of vitamin d deficit on the rat gut microbiome","volume":"11","author":"Robles-Vera","year":"2019","journal-title":"Nutrients"},{"key":"B100","doi-asserted-by":"publisher","DOI":"10.3389\/fcimb.2017.00396","article-title":"Gut dysbiosis in animals due to environmental chemical exposures","volume":"7","author":"Rosenfeld","year":"2017","journal-title":"Front. Cell. Infection Microbiol."},{"key":"B101","doi-asserted-by":"publisher","first-page":"220","DOI":"10.1016\/j.tree.2019.11.004","article-title":"The reproductive microbiome: an emerging driver of sexual selection, sexual conflict, mating systems, and reproductive isolation","volume":"35","author":"Rowe","year":"2020","journal-title":"Trends Ecol. Evol."},{"key":"B102","doi-asserted-by":"publisher","first-page":"195","DOI":"10.1016\/j.chom.2013.07.012","article-title":"Fusobacterium nucleatum promotes colorectal carcinogenesis by modulating e-cadherin\/\u03b2-catenin signaling via its FadA adhesin","volume":"14","author":"Rubinstein","year":"2013","journal-title":"Cell Host Microbe"},{"key":"B103","doi-asserted-by":"publisher","first-page":"93","DOI":"10.2147\/IJWH.S38800","article-title":"Serum vitamin D3 level inversely correlates with uterine fibroid volume in different ethnic groups: a cross-sectional observational study","volume":"5","author":"Sabry","year":"2013","journal-title":"Int. J. women\u2019s Health"},{"key":"B104","doi-asserted-by":"publisher","first-page":"2916","DOI":"10.3390\/jcm10132916","article-title":"How the gut microbiome links to menopause and obesity, with possible implications for endometrial cancer development","volume":"10","author":"Schreurs","year":"2021","journal-title":"J. Clin. Med."},{"key":"B105","doi-asserted-by":"publisher","first-page":"338","DOI":"10.1093\/infdis\/jiu089","article-title":"Role of Gardnerella vaginalis in the pathogenesis of bacterial vaginosis: a conceptual model","volume":"210","author":"Schwebke","year":"2014","journal-title":"J. Infect. Dis."},{"key":"B106","doi-asserted-by":"crossref","DOI":"10.3390\/ijms222413440","article-title":"Human gut microbiota in health and selected cancers","volume":"22","author":"S\u0119dzikowska","year":"2021","journal-title":"International Journal of Molecular Sciences"},{"key":"B107","doi-asserted-by":"publisher","first-page":"1363","DOI":"10.1007\/s00404-021-06057-z","article-title":"Gut microbiota imbalance and its correlations with hormone and inflammatory factors in patients with stage 3\/4 endometriosis","volume":"304","author":"Shan","year":"2021","journal-title":"Arch. Gynecology Obstetrics."},{"key":"B108","doi-asserted-by":"publisher","first-page":"247","DOI":"10.1016\/j.fertnstert.2010.07.1041","article-title":"Vitamin d inhibits proliferation of human uterine leiomyoma cells via catechol-o-methyltransferase","volume":"95","author":"Sharan","year":"2011","journal-title":"Fertility sterility"},{"key":"B109","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1186\/s12967-017-1175-y","article-title":"Influence of diet on the gut microbiome and implications for human health","volume":"15","author":"Singh","year":"2017","journal-title":"J. Trans. Med."},{"key":"B110","doi-asserted-by":"publisher","DOI":"10.3389\/fimmu.2019.01042","article-title":"Vitamin d deficiency in the gulf cooperation council: exploring the triad of genetic predisposition, the gut microbiome and the immune system","volume":"10","author":"Singh","year":"2019","journal-title":"Front. Immunol."},{"key":"B111","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1038\/s41598-020-77806-4","article-title":"The potential role of vitamin d supplementation as a gut microbiota modifier in healthy individuals","volume":"10","author":"Singh","year":"2020","journal-title":"Sci. Rep."},{"key":"B112","doi-asserted-by":"publisher","first-page":"451","DOI":"10.1113\/JP271694","article-title":"The vaginal microbiota, host defence and reproductive physiology","volume":"595","author":"Smith","year":"2017","journal-title":"J. Physiol."},{"key":"B113","doi-asserted-by":"publisher","first-page":"5756","DOI":"10.3390\/ijms23105756","article-title":"The role of microbiota in the immunopathogenesis of endometrial cancer","volume":"23","author":"Sobstyl","year":"2022","journal-title":"Int. J. Mol. Sci."},{"key":"B114","doi-asserted-by":"publisher","first-page":"227","DOI":"10.1038\/nrmicro2974","article-title":"The gut microbiota\u2013masters of host development and physiology","volume":"11","author":"Sommer","year":"2013","journal-title":"Nat. Rev. Microbiol."},{"key":"B115","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1038\/nrdp.2016.43","article-title":"Uterine fibroids","volume":"2","author":"Stewart","year":"2016","journal-title":"Nat. Rev. Dis. Primers"},{"key":"B116","doi-asserted-by":"publisher","first-page":"2367","DOI":"10.1007\/s43032-021-00506-5","article-title":"Associations between endometriosis and gut microbiota","volume":"28","author":"Svensson","year":"2021","journal-title":"Reprod. Sci."},{"key":"B117","doi-asserted-by":"publisher","first-page":"15","DOI":"10.1016\/j.humic.2017.01.004","article-title":"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","volume":"3","author":"Tao","year":"2017","journal-title":"Hum. Microbiome J."},{"key":"B118","doi-asserted-by":"publisher","first-page":"54","DOI":"10.1016\/j.tem.2018.11.001","article-title":"Sex, microbes, and polycystic ovary syndrome","volume":"30","author":"Thackray","year":"2019","journal-title":"Trends Endocrinol. Metab."},{"key":"B119","doi-asserted-by":"publisher","first-page":"104","DOI":"10.1016\/j.mehy.2012.04.016","article-title":"Dysbiosis of gut microbiota (DOGMA)\u2013a novel theory for the development of polycystic ovarian syndrome","volume":"79","author":"Tremellen","year":"2012","journal-title":"Med. Hypotheses"},{"key":"B120","doi-asserted-by":"publisher","DOI":"10.3389\/fphys.2020.01108","article-title":"Comparative analysis of lower genital tract microbiome between PCOS and healthy women","volume":"11","author":"Tu","year":"2020","journal-title":"Front. Physiol."},{"key":"B121","doi-asserted-by":"publisher","DOI":"10.771.7\/peerj.1602","article-title":"Characterisation of the human uterine microbiome in non-pregnant women through deep sequencing of the V1-2 region of the 16S rRNA gene","volume":"4","author":"Verstraelen","year":"2016","journal-title":"PeerJ"},{"key":"B122","doi-asserted-by":"publisher","first-page":"141","DOI":"10.1677\/JOE-10-0072","article-title":"Inflammatory events in endometrial adenocarcinoma","volume":"206","author":"Wallace","year":"2010","journal-title":"J. Endocrinol."},{"key":"B123","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1186\/s13073-016-0368-y","article-title":"Potential contribution of the uterine microbiome in the development of endometrial cancer","volume":"8","author":"Walther-Ant\u00f3nio","year":"2016","journal-title":"Genome Med."},{"key":"B124","doi-asserted-by":"publisher","DOI":"10.3389\/fmicb.2017.00738","article-title":"Colonization and succession within the human gut microbiome by archaea, bacteria, and microeukaryotes during the first year of life","volume":"8","author":"Wampach","year":"2017","journal-title":"Front. Microbiol."},{"key":"B125","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1186\/s12866-020-01779-7","article-title":"High-throughput sequencing study of the effect of transabdominal hysterectomy on intestinal flora in patients with uterine fibroids","volume":"20","author":"Wang","year":"2020","journal-title":"BMC Microbiol."},{"key":"B126","doi-asserted-by":"publisher","first-page":"71","DOI":"10.1016\/J.ENG.2017.01.008","article-title":"The human microbiota in health and disease","volume":"3","author":"Wang","year":"2017","journal-title":"Engineering"},{"key":"B127","doi-asserted-by":"publisher","first-page":"113437","DOI":"10.1016\/j.ygcen.2020.113437","article-title":"Regulation of endocrine systems by the microbiome: perspectives from comparative animal models","volume":"292","author":"Williams","year":"2020","journal-title":"Gen. Comp. Endocrinol."},{"key":"B128","doi-asserted-by":"publisher","first-page":"2","DOI":"10.1097\/GRF.0000000000000164","article-title":"Epidemiology of uterine fibroids\u2013from menarche to menopause","volume":"59","author":"Wise","year":"2016","journal-title":"Clin. obstetrics gynecology"},{"key":"B129","doi-asserted-by":"publisher","first-page":"1082","DOI":"10.1136\/gutjnl-2014-307436","article-title":"Intestinal epithelial vitamin d receptor deletion leads to defective autophagy in colitis","volume":"64","author":"Wu","year":"2015","journal-title":"Gut"},{"key":"B130","doi-asserted-by":"publisher","first-page":"678","DOI":"10.1210\/endrev\/bnab039","article-title":"Comprehensive review of uterine fibroids: developmental origin, pathogenesis, and treatment","volume":"43","author":"Yang","year":"2022","journal-title":"Endocrine Rev."},{"key":"B131","doi-asserted-by":"publisher","first-page":"607","DOI":"10.1093\/humrep\/dex372","article-title":"Endometriosis induces gut microbiota alterations in mice","volume":"33","author":"Yuan","year":"2018","journal-title":"Hum. Reprod."},{"key":"B132","doi-asserted-by":"publisher","first-page":"371","DOI":"10.1080\/07315724.2019.1657515","article-title":"A new approach to polycystic ovary syndrome: the gut microbiota","volume":"39","author":"Yurtda\u015f","year":"2020","journal-title":"J. Am. Coll. Nutr."},{"key":"B133","doi-asserted-by":"publisher","first-page":"186. e1","DOI":"10.1016\/j.ajog.2008.08.064","article-title":"Enhanced estrogen-induced proliferation in obese rat endometrium","volume":"200","author":"Zhang","year":"2009","journal-title":"Am. J. obstetrics gynecology"},{"key":"B134","doi-asserted-by":"publisher","first-page":"153","DOI":"10.1016\/j.jsbmb.2005.06.024","article-title":"Vitamin d receptor (VDR) ablation alters carcinogen-induced tumorigenesis in mammary gland, epidermis and lymphoid tissues","volume":"97","author":"Zinser","year":"2005","journal-title":"J. Steroid Biochem. Mol. Biol."},{"key":"B135","first-page":"271","article-title":"The path forward on endocrine disruptors requires focus on the basics","volume":"149","author":"Zoeller","year":"2016","journal-title":"Toxicological Sci."}],"updated-by":[{"DOI":"10.3389\/fcimb.2023.1211349","type":"erratum","label":"Erratum","source":"publisher","updated":{"date-parts":[[2023,5,12]],"date-time":"2023-05-12T00:00:00Z","timestamp":1683849600000}}],"container-title":["Frontiers in Cellular and Infection Microbiology"],"original-title":[],"link":[{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fcimb.2022.1059825\/full","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2023,5,12]],"date-time":"2023-05-12T11:03:48Z","timestamp":1683889428000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fcimb.2022.1059825\/full"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2022,12,16]]},"references-count":135,"alternative-id":["10.3389\/fcimb.2022.1059825"],"URL":"https:\/\/doi.org\/10.3389\/fcimb.2022.1059825","relation":{"erratum":[{"id-type":"doi","id":"10.3389\/fcimb.2023.1211349","asserted-by":"object"}]},"ISSN":["2235-2988"],"issn-type":[{"value":"2235-2988","type":"electronic"}],"subject":[],"published":{"date-parts":[[2022,12,16]]},"article-number":"1059825"}}