{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,5]],"date-time":"2026-10-05T16:57:48Z","timestamp":1791219468785,"version":"4.1.0"},"reference-count":34,"publisher":"MDPI AG","issue":"11","license":[{"start":{"date-parts":[[2018,10,24]],"date-time":"2018-10-24T00:00:00Z","timestamp":1540339200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["JCM"],"abstract":"<jats:p>Endometriosis occurs when endometrial tissue exists outside the uterine cavity. The presence of ectopic endometrial tissue and resultant inflammation cause serious symptoms, including chronic pelvic pain, dysmenorrhea, dyspareunia, and infertility. Pelvic inflammatory disease is caused by the ascension of pathogenic bacteria from the vagina to the uterus, Fallopian tubes, and ovaries. The factors involved in the pathogenesis of the two conditions are not clearly understood, but recent studies have suggested that disturbances of the female reproductive tract microbiota and inflammatory processes influence the development of both diseases. Using data from the National Health Insurance Research Database (NHIRD), we conducted a study to assess the association of pelvic inflammatory disease (PID) with endometriosis. An age-matched control group including patients without PID was selected. Patients with a pre-existing diagnosis of endometriosis were excluded. This nationwide retrospective cohort study, involving a total of 141,460 patients, demonstrated that patients with PID had a three-fold increase in the risk of developing endometriosis (HR = 3.02, 95% CI = 2.85\u20133.2).<\/jats:p>","DOI":"10.3390\/jcm7110379","type":"journal-article","created":{"date-parts":[[2018,10,24]],"date-time":"2018-10-24T05:08:00Z","timestamp":1540357680000},"page":"379","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":83,"title":["Association of Pelvic Inflammatory Disease with Risk of Endometriosis: A Nationwide Cohort Study Involving 141,460 Individuals"],"prefix":"10.3390","volume":"7","author":[{"given":"Fei-Wu","family":"Tai","sequence":"first","affiliation":[{"name":"School of Chinese Medicine, China Medical University, Taichung 40402, Taiwan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-2529-8125","authenticated-orcid":false,"given":"Cherry Yin-Yi","family":"Chang","sequence":"additional","affiliation":[{"name":"Department of Obstetrics and Gynecology, China Medical University Hospital, Taichung 40447, Taiwan"},{"name":"School of Medicine, China Medical University, Taichung 40402, Taiwan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jen-Huai","family":"Chiang","sequence":"additional","affiliation":[{"name":"Management Office for Health Data, China Medical University Hospital, Taichung 40447, Taiwan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Wu-Chou","family":"Lin","sequence":"additional","affiliation":[{"name":"School of Chinese Medicine, China Medical University, Taichung 40402, Taiwan"},{"name":"Department of Obstetrics and Gynecology, China Medical University Hospital, Taichung 40447, Taiwan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-9525-3232","authenticated-orcid":false,"given":"Lei","family":"Wan","sequence":"additional","affiliation":[{"name":"School of Chinese Medicine, China Medical University, Taichung 40402, Taiwan"},{"name":"Department of Biotechnology, Asia University, Taichung 41354, Taiwan"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2018,10,24]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"268","DOI":"10.1056\/NEJMra0804690","article-title":"Endometriosis","volume":"360","author":"Bulun","year":"2009","journal-title":"N. Engl. J. Med."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"366","DOI":"10.1016\/j.fertnstert.2011.05.090","article-title":"World Endometriosis Research Foundation Global Study of Women\u2019s Health Consortium. Impact of endometriosis on quality of life and work productivity: A multicenter study across ten countries","volume":"96","author":"Nnoaham","year":"2011","journal-title":"Fertil. Steril."},{"key":"ref_3","first-page":"93","article-title":"Metastatic or embolic endometriosis, due to the menstrual dissemination of endometrial tissue into the venous circulation","volume":"3","author":"Sampson","year":"1927","journal-title":"Am. J. Pathol."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"1789","DOI":"10.1016\/S0140-6736(04)17403-5","article-title":"Endometriosis","volume":"364","author":"Giudice","year":"2004","journal-title":"Lancet"},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"232","DOI":"10.1210\/en.2005-0426","article-title":"Transcriptional characterizations of differences between eutopic and ectopic endometrium","volume":"147","author":"Wu","year":"2006","journal-title":"Endocrinology"},{"key":"ref_6","first-page":"1118","article-title":"Interleukin-6 secretion in vitro is up-regulated in ectopic and eutopic endometrial stromal cells from women with endometriosis","volume":"81","author":"Tseng","year":"1996","journal-title":"J. Clin. Endocrinol. Metab."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"16","DOI":"10.1016\/j.fertnstert.2004.10.058","article-title":"A novel in vitro model of the early endometriotic lesion demonstrates that attachment of endometrial cells to mesothelial cells is dependent on the source of endometrial cells","volume":"84","author":"Lucidi","year":"2005","journal-title":"Fertil. Steril."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"2870","DOI":"10.1210\/en.2003-0043","article-title":"Expression profiling of endometrium from women with endometriosis reveals candidate genes for disease-based implantation failure and infertility","volume":"144","author":"Kao","year":"2003","journal-title":"Endocrinology"},{"key":"ref_9","first-page":"1621","article-title":"Immunolocalization and regulation of the chemokine rantes in human endometrial and endometriosis tissues and cells","volume":"82","author":"Hornung","year":"1997","journal-title":"J. Clin. Endocrinol. Metab."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"89","DOI":"10.1111\/j.1749-6632.2002.tb02769.x","article-title":"Angiogenic factors in endometriosis","volume":"955","author":"Taylor","year":"2002","journal-title":"Ann. N. Y. Acad. Sci."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"11","DOI":"10.1111\/j.1749-6632.2002.tb02761.x","article-title":"The epidemiology of endometriosis","volume":"955","author":"Cramer","year":"2002","journal-title":"Ann. N. Y. Acad. Sci."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"32","DOI":"10.1016\/j.fertnstert.2017.05.034","article-title":"Endometrial microbiota-new player in town","volume":"108","author":"Moreno","year":"2017","journal-title":"Fertil. Steril."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"2039","DOI":"10.1056\/NEJMra1411426","article-title":"Pelvic inflammatory disease","volume":"372","author":"Brunham","year":"2015","journal-title":"N. Engl. J. Med."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"167","DOI":"10.1097\/00000478-199002000-00008","article-title":"Endometrial histopathology in patients with culture-proved upper genital tract infection and laparoscopically diagnosed acute salpingitis","volume":"14","author":"Kiviat","year":"1990","journal-title":"Am. J. Surg. Pathol."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"1351","DOI":"10.1016\/j.fertnstert.2015.10.010","article-title":"Gynecologic health and disease in relation to the microbiome of the female reproductive tract","volume":"104","author":"Green","year":"2015","journal-title":"Fertil. Steril."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"97","DOI":"10.3389\/fphys.2015.00097","article-title":"Individualized medicine and the microbiome in reproductive tract","volume":"6","author":"Braundmeier","year":"2015","journal-title":"Front. Physiol."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"43","DOI":"10.1055\/s-0033-1361822","article-title":"Microbiota and pelvic inflammatory disease","volume":"32","author":"Sharma","year":"2014","journal-title":"Semin. Reprod. Med."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"117","DOI":"10.1097\/OLQ.0b013e31827c5a5b","article-title":"Does bacterial vaginosis cause pelvic inflammatory disease?","volume":"40","author":"Taylor","year":"2013","journal-title":"Sex. Transm. Dis."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"4610","DOI":"10.1172\/JCI57172","article-title":"Vaginal microbiome and sexually transmitted infections: An epidemiologic perspective","volume":"121","author":"Brotman","year":"2011","journal-title":"J. Clin. Investig."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"223","DOI":"10.1016\/S0015-0282(01)01878-7","article-title":"Treating endometriosis as an autoimmune disease","volume":"76","author":"Nothnick","year":"2001","journal-title":"Fertil. Steril."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"209","DOI":"10.1016\/j.ejogrb.2014.04.025","article-title":"Endometriosis and type 1 allergies\/immediate type hypersensitivity: A systematic review","volume":"179","author":"Bungum","year":"2014","journal-title":"Eur. J. Obstet. Gynecol. Reprod. Biol."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"500","DOI":"10.1093\/humupd\/dmv013","article-title":"Endometriosis: A high-risk population for major chronic diseases?","volume":"21","author":"Kvaskoff","year":"2015","journal-title":"Hum. Reprod. Update"},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"1627","DOI":"10.1016\/j.fertnstert.2009.07.1698","article-title":"Cancers, infections, and endocrine diseases in women with endometriosis","volume":"94","author":"Gemmill","year":"2010","journal-title":"Fertil. Steril."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"385","DOI":"10.1016\/S1470-2045(11)70404-1","article-title":"Association between endometriosis and risk of histological subtypes of ovarian cancer: A pooled analysis of case-control studies","volume":"13","author":"Pearce","year":"2012","journal-title":"Lancet Oncol."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"3358","DOI":"10.1093\/humrep\/det340","article-title":"Increased risk for ovarian cancer and borderline ovarian tumours in subfertile women with endometriosis","volume":"28","author":"Buis","year":"2013","journal-title":"Hum. Reprod."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"e2773","DOI":"10.1097\/MD.0000000000002773","article-title":"Increased risk of endometriosis in patients with lower genital tract infection: A nationwide cohort study","volume":"95","author":"Lin","year":"2016","journal-title":"Medicine"},{"key":"ref_27","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_28","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_29","doi-asserted-by":"crossref","first-page":"69","DOI":"10.1016\/j.ejogrb.2016.01.040","article-title":"Molecular detection of intrauterine microbial colonization in women with endometriosis","volume":"199","author":"Khan","year":"2016","journal-title":"Eur. J. Obstet. Gynecol. Reprod. Biol."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"875","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":"ref_31","doi-asserted-by":"crossref","first-page":"e611","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. Obstet. Gynecol."},{"key":"ref_32","first-page":"622","article-title":"A comparison of the fallopian tube\u2019s response to overt and silent salpingitis","volume":"73","author":"Patton","year":"1989","journal-title":"Obstet. Gynecol."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"611","DOI":"10.1586\/eci.11.53","article-title":"Immune interactions in endometriosis","volume":"7","author":"Herington","year":"2011","journal-title":"Expert Rev. Clin. Immunol."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/S0015-0282(00)01630-7","article-title":"Immunobiology of endometriosis","volume":"75","author":"Lebovic","year":"2001","journal-title":"Fertil. 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