{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,6,22]],"date-time":"2026-06-22T13:44:17Z","timestamp":1782135857650,"version":"3.54.5"},"reference-count":39,"publisher":"Springer Science and Business Media LLC","issue":"1","license":[{"start":{"date-parts":[[2021,7,28]],"date-time":"2021-07-28T00:00:00Z","timestamp":1627430400000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"},{"start":{"date-parts":[[2021,7,28]],"date-time":"2021-07-28T00:00:00Z","timestamp":1627430400000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["BMC Women's Health"],"published-print":{"date-parts":[[2021,12]]},"abstract":"<jats:title>Abstract<\/jats:title>\n                  <jats:sec>\n                    <jats:title>Background<\/jats:title>\n                    <jats:p>Pelvic inflammatory disease (PID) is an important health issue for women. Infection and inflammation play an important role in carcinogenesis and PID has been reported to be associated with ovarian cancer in some small scale studies.<\/jats:p>\n                  <\/jats:sec>\n                  <jats:sec>\n                    <jats:title>Aim<\/jats:title>\n                    <jats:p>We sought to determine whether PID is associated with an elevated risk of ovarian cancer in Asian women.<\/jats:p>\n                  <\/jats:sec>\n                  <jats:sec>\n                    <jats:title>Methods<\/jats:title>\n                    <jats:p>Using data from Taiwan\u2019s National Health Insurance Research Database (NHIRD), our retrospective cohort study included women diagnosed with PID (cases) between the years of 2000 till 2012. Each case was matched with two women without PID (controls) by age and the year of first entry into the database. Both study cohorts were followed-up until the first event of ovarian cancer, withdrawal from the NHI program, death, or the end of the study period (December 31, 2012). Cox proportional hazards regression models were used to estimate crude and adjusted hazard ratios (HRs and aHRs) with their corresponding 95% confidence intervals (95% CIs) for the association of PID and ovarian cancer risk, with and without adjusting for potential confounders.<\/jats:p>\n                  <\/jats:sec>\n                  <jats:sec>\n                    <jats:title>Results<\/jats:title>\n                    <jats:p>\n                      During an approximate 10\u00a0years of follow-up, cases were significantly more likely than controls to develop ovarian cancer (incidence rates of 0.27 and 0.16 per 1,000 person-years, respectively;\n                      <jats:italic>P<\/jats:italic>\n                      \u2009&lt;\u20090.001). Women with a history of PID had a 1.49-fold elevated risk for ovarian cancer (aHR, 1.49; 95% CI, 1.21\u20131.84;\n                      <jats:italic>P<\/jats:italic>\n                      \u2009&lt;\u20090.001).\n                    <\/jats:p>\n                  <\/jats:sec>\n                  <jats:sec>\n                    <jats:title>Conclusion<\/jats:title>\n                    <jats:p>Our study evidence supports the contention that PID increases the risk of developing ovarian cancer among Taiwanese women. Gynecologists should undertake careful assessments and closely follow patients with PID, who are at long-term risk of developing ovarian cancer. Our findings need further verification in other international cohorts.<\/jats:p>\n                  <\/jats:sec>","DOI":"10.1186\/s12905-021-01413-2","type":"journal-article","created":{"date-parts":[[2021,7,28]],"date-time":"2021-07-28T09:02:42Z","timestamp":1627462962000},"update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":8,"title":["Association of pelvic inflammatory disease (PID) with ovarian cancer: a nationwide population-based retrospective cohort study from Taiwan"],"prefix":"10.1186","volume":"21","author":[{"given":"Cherry Yin-Yi","family":"Chang","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Kent Yu-Hsien","family":"Lin","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Chien-Chu","family":"Huang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Wu-Chou","family":"Lin","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"297","published-online":{"date-parts":[[2021,7,28]]},"reference":[{"key":"1413_CR1","first-page":"51","volume":"24","author":"KA Workowski","year":"2015","unstructured":"Workowski KA, Bolan GA. Sexually transmitted diseases treatment guidelines (2015). Reprod Endocrinol. 2015;24:51\u20136.","journal-title":"Reprod Endocrinol"},{"issue":"1","key":"1413_CR2","doi-asserted-by":"publisher","first-page":"12","DOI":"10.1155\/S1064744993000043","volume":"1","author":"M Toth","year":"1993","unstructured":"Toth M, et al. Pregnancy outcome following pelvic infection. Infect Dis Obstet Gynecol. 1993;1(1):12\u20135.","journal-title":"Infect Dis Obstet Gynecol"},{"issue":"4","key":"1413_CR3","first-page":"219","volume":"8","author":"L Westrom","year":"1995","unstructured":"Westrom L. Effect of pelvic inflammatory disease on fertility. Venereology. 1995;8(4):219\u201322.","journal-title":"Venereology"},{"issue":"7","key":"1413_CR4","doi-asserted-by":"publisher","first-page":"601","DOI":"10.1136\/sextrans-2011-050205","volume":"87","author":"N Bender","year":"2011","unstructured":"Bender N, et al. Chlamydia infection, pelvic inflammatory disease, ectopic pregnancy and infertility: cross-national study. Sex Transm Infect. 2011;87(7):601\u20138.","journal-title":"Sex Transm Infect"},{"issue":"1","key":"1413_CR5","doi-asserted-by":"publisher","first-page":"31","DOI":"10.1159\/000293209","volume":"30","author":"V Bychkov","year":"1990","unstructured":"Bychkov V. Ovarian pathology in chronic pelvic inflammatory disease. Gynecol Obstet Investig. 1990;30(1):31\u20133.","journal-title":"Gynecol Obstet Investig"},{"issue":"1","key":"1413_CR6","doi-asserted-by":"publisher","first-page":"104","DOI":"10.1158\/1055-9965.EPI-16-0459","volume":"26","author":"CB Rasmussen","year":"2017","unstructured":"Rasmussen CB, et al. Is pelvic inflammatory disease a risk factor for ovarian cancer? Cancer Epidemiol Biomarkers Prev. 2017;26(1):104\u20139.","journal-title":"Cancer Epidemiol Biomarkers Prev"},{"issue":"1","key":"1413_CR7","doi-asserted-by":"publisher","first-page":"8","DOI":"10.1093\/aje\/kww161","volume":"185","author":"CB Rasmussen","year":"2017","unstructured":"Rasmussen CB, et al. Pelvic inflammatory disease and the risk of ovarian cancer and borderline ovarian tumors: a pooled analysis of 13 case\u2013control studies. Am J Epidemiol. 2017;185(1):8\u201320.","journal-title":"Am J Epidemiol"},{"issue":"1","key":"1413_CR8","doi-asserted-by":"publisher","first-page":"839","DOI":"10.1186\/s12885-016-2857-1","volume":"16","author":"CC Shen","year":"2016","unstructured":"Shen CC, et al. Risk of uterine, ovarian and breast cancer following pelvic inflammatory disease: a nationwide population-based retrospective cohort study. BMC Cancer. 2016;16(1):839.","journal-title":"BMC Cancer"},{"issue":"22","key":"1413_CR9","doi-asserted-by":"publisher","first-page":"2705","DOI":"10.1001\/jama.291.22.2705","volume":"291","author":"BA Goff","year":"2004","unstructured":"Goff BA, et al. Frequency of symptoms of ovarian cancer in women presenting to primary care clinics. JAMA. 2004;291(22):2705\u201312.","journal-title":"JAMA"},{"issue":"4","key":"1413_CR10","doi-asserted-by":"publisher","first-page":"222","DOI":"10.1093\/jnci\/djp500","volume":"102","author":"MA Rossing","year":"2010","unstructured":"Rossing MA, et al. Predictive value of symptoms for early detection of ovarian cancer. J Natl Cancer Inst. 2010;102(4):222\u20139.","journal-title":"J Natl Cancer Inst"},{"issue":"11","key":"1413_CR11","first-page":"937","volume":"93","author":"CA Doubeni","year":"2016","unstructured":"Doubeni CA, Doubeni AR, Myers AE. Diagnosis and management of ovarian cancer. Am Fam Phys. 2016;93(11):937\u201344.","journal-title":"Am Fam Phys"},{"issue":"8","key":"1413_CR12","first-page":"667","volume":"5","author":"F Parazzini","year":"1996","unstructured":"Parazzini F, et al. Pelvic inflammatory disease and risk of ovarian cancer. Cancer Epidemiol Biomarkers Prev. 1996;5(8):667\u20139.","journal-title":"Cancer Epidemiol Biomarkers Prev"},{"issue":"7","key":"1413_CR13","doi-asserted-by":"publisher","first-page":"585","DOI":"10.1093\/oxfordjournals.aje.a117296","volume":"140","author":"HA Risch","year":"1994","unstructured":"Risch HA, Marrett LD, Howe GR. Parity, contraception, infertility, and the risk of epithelial ovarian cancer. Am J Epidemiol. 1994;140(7):585\u201397.","journal-title":"Am J Epidemiol"},{"issue":"1","key":"1413_CR14","doi-asserted-by":"publisher","first-page":"10","DOI":"10.1016\/0002-9378(89)90221-4","volume":"161","author":"P Hartge","year":"1989","unstructured":"Hartge P, et al. A case-control study of epithelial ovarian cancer. Am J Obstet Gynecol. 1989;161(1):10\u20136.","journal-title":"Am J Obstet Gynecol"},{"issue":"5","key":"1413_CR15","doi-asserted-by":"publisher","first-page":"714","DOI":"10.1093\/oxfordjournals.aje.a113353","volume":"115","author":"S Franceschi","year":"1982","unstructured":"Franceschi S, et al. Risk factors for epithelial ovarian cancer in Italy. Am J Epidemiol. 1982;115(5):714\u20139.","journal-title":"Am J Epidemiol"},{"issue":"2","key":"1413_CR16","doi-asserted-by":"publisher","first-page":"137","DOI":"10.1615\/CritRevImmunol.2013006813","volume":"33","author":"B Charbonneau","year":"2013","unstructured":"Charbonneau B, et al. The immune system in the pathogenesis of ovarian cancer. Crit RevTM Immunol. 2013;33(2):137\u201364.","journal-title":"Crit RevTM Immunol"},{"issue":"5","key":"1413_CR17","doi-asserted-by":"publisher","first-page":"263","DOI":"10.1016\/j.bj.2017.08.002","volume":"40","author":"M-S Tsai","year":"2017","unstructured":"Tsai M-S, et al. Chang Gung Research Database: a multi-institutional database consisting of original medical records. Biomed J. 2017;40(5):263\u20139.","journal-title":"Biomed J"},{"issue":"3","key":"1413_CR18","doi-asserted-by":"publisher","first-page":"527","DOI":"10.1016\/S0889-8545(02)00014-1","volume":"29","author":"RT Burkman","year":"2002","unstructured":"Burkman RT. Reproductive hormones and cancer: ovarian and colon cancer. Obstet Gynecol Clin N Am. 2002;29(3):527\u201340.","journal-title":"Obstet Gynecol Clin N Am"},{"issue":"1","key":"1413_CR19","doi-asserted-by":"publisher","first-page":"85","DOI":"10.1016\/S0029-7844(96)00369-9","volume":"89","author":"NR Abu-Rustum","year":"1997","unstructured":"Abu-Rustum NR, Barakat RR, Curtin JP. Ovarian and uterine disease in women with colorectal cancer. Obstet Gynecol. 1997;89(1):85\u20137.","journal-title":"Obstet Gynecol"},{"issue":"4","key":"1413_CR20","doi-asserted-by":"publisher","first-page":"771","DOI":"10.1093\/oxfordjournals.aje.a115030","volume":"128","author":"M Mori","year":"1988","unstructured":"Mori M, et al. Reproductive, genetic, and dietary risk factors for ovarian cancer. Am J Epidemiol. 1988;128(4):771\u20137.","journal-title":"Am J Epidemiol"},{"issue":"23","key":"1413_CR21","doi-asserted-by":"publisher","first-page":"2339","DOI":"10.1056\/NEJMra012284","volume":"348","author":"R Wooster","year":"2003","unstructured":"Wooster R, Weber BL. Breast and ovarian cancer. N Engl J Med. 2003;348(23):2339\u201347.","journal-title":"N Engl J Med"},{"issue":"5","key":"1413_CR22","doi-asserted-by":"publisher","first-page":"1237","DOI":"10.1093\/humrep\/dei462","volume":"21","author":"A Melin","year":"2006","unstructured":"Melin A, et al. Endometriosis and the risk of cancer with special emphasis on ovarian cancer. Hum Reprod. 2006;21(5):1237\u201342.","journal-title":"Hum Reprod"},{"issue":"4","key":"1413_CR23","doi-asserted-by":"publisher","first-page":"271","DOI":"10.1111\/j.1467-789X.2005.00175.x","volume":"6","author":"NF Chu","year":"2005","unstructured":"Chu NF. Prevalence of obesity in Taiwan. Obes Rev. 2005;6(4):271\u20134.","journal-title":"Obes Rev"},{"issue":"6917","key":"1413_CR24","doi-asserted-by":"publisher","first-page":"860","DOI":"10.1038\/nature01322","volume":"420","author":"LM Coussens","year":"2002","unstructured":"Coussens LM, Werb Z. Inflammation and cancer. Nature. 2002;420(6917):860.","journal-title":"Nature"},{"issue":"9","key":"1413_CR25","doi-asserted-by":"publisher","first-page":"900","DOI":"10.1016\/S1470-2045(11)70165-6","volume":"12","author":"HW Lin","year":"2011","unstructured":"Lin HW, et al. Risk of ovarian cancer in women with pelvic inflammatory disease: a population-based study. Lancet Oncol. 2011;12(9):900\u20134.","journal-title":"Lancet Oncol"},{"issue":"2","key":"1413_CR26","doi-asserted-by":"publisher","first-page":"346","DOI":"10.1016\/j.ygyno.2016.08.318","volume":"143","author":"CB Rasmussen","year":"2016","unstructured":"Rasmussen CB, et al. Increased risk of borderline ovarian tumors in women with a history of pelvic inflammatory disease: A nationwide population-based cohort study. Gynecol Oncol. 2016;143(2):346\u201351.","journal-title":"Gynecol Oncol"},{"issue":"5","key":"1413_CR27","doi-asserted-by":"publisher","first-page":"415","DOI":"10.1007\/s10552-017-0873-3","volume":"28","author":"Z Zhou","year":"2017","unstructured":"Zhou Z, et al. Pelvic inflammatory disease and the risk of ovarian cancer: a meta-analysis. Cancer Causes Control. 2017;28(5):415\u201328.","journal-title":"Cancer Causes Control"},{"issue":"2","key":"1413_CR28","doi-asserted-by":"publisher","first-page":"129","DOI":"10.1093\/jnci\/djy084","volume":"111","author":"B Trabert","year":"2019","unstructured":"Trabert B, et al. Antibodies against chlamydia trachomatis and ovarian cancer risk in two independent populations. J Natl Cancer Inst. 2019;111(2):129\u201336.","journal-title":"J Natl Cancer Inst"},{"issue":"5","key":"1413_CR29","first-page":"447","volume":"4","author":"HA Risch","year":"1995","unstructured":"Risch HA, Howe GR. Pelvic inflammatory disease and the risk of epithelial ovarian cancer. Cancer Epidemiol Biomarkers Prev. 1995;4(5):447\u201351.","journal-title":"Cancer Epidemiol Biomarkers Prev"},{"key":"1413_CR30","doi-asserted-by":"publisher","first-page":"110","DOI":"10.1016\/j.canep.2018.05.011","volume":"55","author":"LM Stewart","year":"2018","unstructured":"Stewart LM, et al. Risk of high-grade serous ovarian cancer associated with pelvic inflammatory disease, parity and breast cancer. Cancer Epidemiol. 2018;55:110\u20136.","journal-title":"Cancer Epidemiol"},{"key":"1413_CR31","doi-asserted-by":"publisher","first-page":"645045","DOI":"10.1155\/2014\/645045","volume":"2014","author":"IM Zardawi","year":"2014","unstructured":"Zardawi IM. Primary fallopian tube carcinoma arising in the setting of chronic pelvic inflammatory disease. Case Rep Med. 2014;2014:645045.","journal-title":"Case Rep Med"},{"issue":"2 Part 1","key":"1413_CR32","doi-asserted-by":"publisher","first-page":"395","DOI":"10.1097\/AOG.0b013e31829d4376","volume":"122","author":"DI Lipschutz","year":"2013","unstructured":"Lipschutz DI. Long-term mortality associated with oophorectomy compared with ovarian conservation in the Nurses\u2019 Health Study. Obstet Gynecol. 2013;122(2 Part 1):395\u20136.","journal-title":"Obstet Gynecol"},{"issue":"3","key":"1413_CR33","doi-asserted-by":"publisher","first-page":"476","DOI":"10.1097\/AOG.0000000000001592","volume":"128","author":"EC Evans","year":"2016","unstructured":"Evans EC, et al. Salpingo-oophorectomy at the time of benign hysterectomy: a systematic review. Obstet Gynecol. 2016;128(3):476\u201385.","journal-title":"Obstet Gynecol"},{"issue":"3","key":"1413_CR34","doi-asserted-by":"publisher","first-page":"261","DOI":"10.1056\/NEJMoa052627","volume":"354","author":"KM Schmeler","year":"2006","unstructured":"Schmeler KM, et al. Prophylactic surgery to reduce the risk of gynecologic cancers in the Lynch syndrome. N Engl J Med. 2006;354(3):261\u20139.","journal-title":"N Engl J Med"},{"issue":"11","key":"1413_CR35","doi-asserted-by":"publisher","first-page":"1081","DOI":"10.1007\/s10552-018-1082-4","volume":"29","author":"HK Park","year":"2018","unstructured":"Park HK, et al. Benign gynecologic conditions are associated with ovarian cancer risk in African-American women: a case-control study. Cancer Causes Control. 2018;29(11):1081\u201391.","journal-title":"Cancer Causes Control"},{"issue":"2","key":"1413_CR36","doi-asserted-by":"publisher","first-page":"331","DOI":"10.1016\/j.ygyno.2005.11.033","volume":"101","author":"E Somigliana","year":"2006","unstructured":"Somigliana E, et al. Association between endometriosis and cancer: a comprehensive review and a critical analysis of clinical and epidemiological evidence. Gynecol Oncol. 2006;101(2):331\u201341.","journal-title":"Gynecol Oncol"},{"issue":"3","key":"1413_CR37","doi-asserted-by":"publisher","first-page":"217","DOI":"10.1093\/aje\/155.3.217","volume":"155","author":"RB Ness","year":"2002","unstructured":"Ness RB, et al. Infertility, fertility drugs, and ovarian cancer: a pooled analysis of case-control studies. Am J Epidemiol. 2002;155(3):217\u201324.","journal-title":"Am J Epidemiol"},{"issue":"4","key":"1413_CR38","doi-asserted-by":"publisher","first-page":"499","DOI":"10.1016\/S0015-0282(16)58557-4","volume":"66","author":"EE Wallach","year":"1996","unstructured":"Wallach EE, Bristow RE, Karlan BY. Ovulation induction, infertility, and ovarian cancer risk. Fertil Steril. 1996;66(4):499\u2013507.","journal-title":"Fertil Steril"},{"issue":"1","key":"1413_CR39","doi-asserted-by":"publisher","first-page":"37","DOI":"10.1097\/AOG.0b013e31825a6bc9","volume":"120","author":"HC Wiesenfeld","year":"2012","unstructured":"Wiesenfeld HC, et al. Subclinical pelvic inflammatory disease and infertility. Obstet Gynecol. 2012;120(1):37\u201343.","journal-title":"Obstet Gynecol"}],"container-title":["BMC Women's Health"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/link.springer.com\/content\/pdf\/10.1186\/s12905-021-01413-2.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/link.springer.com\/article\/10.1186\/s12905-021-01413-2\/fulltext.html","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/link.springer.com\/content\/pdf\/10.1186\/s12905-021-01413-2.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2021,7,28]],"date-time":"2021-07-28T09:02:57Z","timestamp":1627462977000},"score":1,"resource":{"primary":{"URL":"https:\/\/bmcwomenshealth.biomedcentral.com\/articles\/10.1186\/s12905-021-01413-2"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2021,7,28]]},"references-count":39,"journal-issue":{"issue":"1","published-print":{"date-parts":[[2021,12]]}},"alternative-id":["1413"],"URL":"https:\/\/doi.org\/10.1186\/s12905-021-01413-2","relation":{"has-preprint":[{"id-type":"doi","id":"10.21203\/rs.3.rs-112758\/v1","asserted-by":"object"}]},"ISSN":["1472-6874"],"issn-type":[{"value":"1472-6874","type":"electronic"}],"subject":[],"published":{"date-parts":[[2021,7,28]]},"assertion":[{"value":"20 November 2020","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"17 July 2021","order":2,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"28 July 2021","order":3,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}},{"order":1,"name":"Ethics","group":{"name":"EthicsHeading","label":"Declarations"}},{"value":"All experimental protocols were approved by China Medical University Hospital\u2019s Review Board and Ethics Committee (CMUH number: CMUH-104-REC2-115 (CR-4)). all methods were performed in accordance with the relevant guidelines and regulations (Declaration of Helsinki). The informed consent for the study was waived off by China Medical University Hospital\u2019s Review Board and Ethics Committee (For the study purpose, the small databank from NHIRD is form one million individuals randomly recruited as subjects obtained from NHIRD. The use of data for our study was permitted by the National Health Research Institute. Protocol for the protection of subjects' privacy already under de-link and unable to identify personally.","order":2,"name":"Ethics","group":{"name":"EthicsHeading","label":"Ethics approval and consent to participate"}},{"value":"Not applicable.","order":3,"name":"Ethics","group":{"name":"EthicsHeading","label":"Consent for publication"}},{"value":"The authors declare that they have no competing interests.","order":4,"name":"Ethics","group":{"name":"EthicsHeading","label":"Competing interests"}}],"article-number":"274"}}