{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,7,8]],"date-time":"2026-07-08T19:42:37Z","timestamp":1783539757788,"version":"3.55.0"},"reference-count":30,"publisher":"Oxford University Press (OUP)","issue":"5","license":[{"start":{"date-parts":[[2019,2,15]],"date-time":"2019-02-15T00:00:00Z","timestamp":1550188800000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by-nc\/4.0\/"}],"funder":[{"name":"National Key Clinical Discipline"},{"name":"National Nature Science Fund of China","award":["81370498"],"award-info":[{"award-number":["81370498"]}]},{"DOI":"10.13039\/501100012245","name":"Science and Technology Planning Project of Guangdong Province","doi-asserted-by":"publisher","award":["2012B091100455"],"award-info":[{"award-number":["2012B091100455"]}],"id":[{"id":"10.13039\/501100012245","id-type":"DOI","asserted-by":"publisher"}]},{"name":"Science and Technology Project of Tianhe District, Guangdong Province, China","award":["201404KW018"],"award-info":[{"award-number":["201404KW018"]}]},{"name":"Medical Scientific and Technical Foundation of Guangdong Province","award":["A2016322"],"award-info":[{"award-number":["A2016322"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"published-print":{"date-parts":[[2019,10,1]]},"abstract":"<jats:title>Abstract<\/jats:title>\n               <jats:sec>\n                  <jats:title>Background and aim<\/jats:title>\n                  <jats:p>This cross-sectional study investigated the prevalence and risk factors of high-risk human papilloma virus (HPV) infection, especially types 16 and 18, and cervical neoplasia in female Inflammatory bowel disease (IBD) patients.<\/jats:p>\n               <\/jats:sec>\n               <jats:sec>\n                  <jats:title>Methods<\/jats:title>\n                  <jats:p>From July 2014 to January 2017, sexually active, female, Chinese IBD patients (21\u201360\u2009years) and age-matched controls underwent cervical ThinPrep cytology testing (TCT) and high-risk HPV-DNA detection, and completed questionnaires about awareness of cervical cancer and HPV. Cervical dysplasia was categorized as cervical intraepithelial neoplasia (CIN) 1, 2 and 3.<\/jats:p>\n               <\/jats:sec>\n               <jats:sec>\n                  <jats:title>Results<\/jats:title>\n                  <jats:p>Of 124 IBD patients (30 ulcerative colitis and 94 Crohn\u2019s disease), 17 (13.7%) had high-risk HPV among whom 9 (7.3%) had HPV 16\/18 infection and 4 (3.2%) had cervical CIN (3 CIN 3, 1 CIN 1) by pathology. Among 372 controls, 33 (8.9%) had high-risk HPV and only 1 (0.3%) had HPV 16 infection. Cervical TCT detected atypical squamous cells of unknown significance in one control; no control had CIN. The HPV 16\/18 infection rate and CIN prevalence were significantly higher in IBD patients than controls (both P\u2009&lt;\u20090.001). The HPV-infection rate was higher in patients administered methotrexate [P\u2009=\u20090.005, odds ratio (95% confidence interval) 4.76 (1.471\u201315.402)] or more than two immunosuppressants [P\u2009=\u20090.013, odds ratio (95% confidence interval) 3.64 (1.255\u201310.562)]. Thiopurine, steroid, infliximab and disease behavior\/location were not associated with HPV infection. Only 29.3% of patients had undergone cervical-cancer screening. Awareness of HPV infection and HPV-related cervical cancer was poor (28.2%).<\/jats:p>\n               <\/jats:sec>\n               <jats:sec>\n                  <jats:title>Conclusions<\/jats:title>\n                  <jats:p>Female IBD patients are at increased risk of high-risk HPV infection and cervical neoplasia, which may be associated with immunosuppressants. Education and routine follow-up with HPV-DNA testing and TCT are recommended, especially in female Chinese IBD patients.<\/jats:p>\n               <\/jats:sec>","DOI":"10.1093\/gastro\/goy053","type":"journal-article","created":{"date-parts":[[2019,1,24]],"date-time":"2019-01-24T20:47:30Z","timestamp":1548362850000},"page":"338-344","source":"Crossref","is-referenced-by-count":24,"title":["High-risk human papilloma virus infection and cervical neoplasm in female inflammatory bowel disease patients: a cross-sectional study"],"prefix":"10.1093","volume":"7","author":[{"given":"Miao","family":"Li","sequence":"first","affiliation":[{"name":"Department of Gastroenterology, The Sixth Affiliated Hospital of Sun Yat-sen University, Guangzhou, Guangdong, China"},{"name":"Guangdong Provincial Key Laboratory of Colorectal and Pelvic Floor Diseases, The Sixth Affiliated Hospital, Sun Yat-sen University, Guangzhou, Guangdong, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Qing-Fan","family":"Yang","sequence":"additional","affiliation":[{"name":"Department of Gastroenterology, The Sixth Affiliated Hospital of Sun Yat-sen University, Guangzhou, Guangdong, China"},{"name":"Guangdong Provincial Key Laboratory of Colorectal and Pelvic Floor Diseases, The Sixth Affiliated Hospital, Sun Yat-sen University, Guangzhou, Guangdong, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Qian","family":"Cao","sequence":"additional","affiliation":[{"name":"Department of Gastroenterology, Sir Run Run Shaw Hospital, School of Medicine, Zhejiang University, Hangzhou, Zhejiang, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jian","family":"Tang","sequence":"additional","affiliation":[{"name":"Department of Gastroenterology, The Sixth Affiliated Hospital of Sun Yat-sen University, Guangzhou, Guangdong, China"},{"name":"Guangdong Provincial Key Laboratory of Colorectal and Pelvic Floor Diseases, The Sixth Affiliated Hospital, Sun Yat-sen University, Guangzhou, Guangdong, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yu","family":"Gao","sequence":"additional","affiliation":[{"name":"Guangdong Provincial Key Laboratory of Colorectal and Pelvic Floor Diseases, The Sixth Affiliated Hospital, Sun Yat-sen University, Guangzhou, Guangdong, China"},{"name":"Obstetrical Department, The Sixth Affiliated Hospital of Sun Yat-sen University, Guangzhou, Guangdong, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Min","family":"Zhi","sequence":"additional","affiliation":[{"name":"Department of Gastroenterology, The Sixth Affiliated Hospital of Sun Yat-sen University, Guangzhou, Guangdong, China"},{"name":"Guangdong Provincial Key Laboratory of Colorectal and Pelvic Floor Diseases, The Sixth Affiliated Hospital, Sun Yat-sen University, Guangzhou, Guangdong, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Kang","family":"Chao","sequence":"additional","affiliation":[{"name":"Department of Gastroenterology, The Sixth Affiliated Hospital of Sun Yat-sen University, Guangzhou, Guangdong, China"},{"name":"Guangdong Provincial Key Laboratory of Colorectal and Pelvic Floor Diseases, The Sixth Affiliated Hospital, Sun Yat-sen University, Guangzhou, Guangdong, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ming-Li","family":"Su","sequence":"additional","affiliation":[{"name":"Department of Gastroenterology, The Sixth Affiliated Hospital of Sun Yat-sen University, Guangzhou, Guangdong, China"},{"name":"Guangdong Provincial Key Laboratory of Colorectal and Pelvic Floor Diseases, The Sixth Affiliated Hospital, Sun Yat-sen University, Guangzhou, Guangdong, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Wei-Min","family":"Huang","sequence":"additional","affiliation":[{"name":"Guangdong Provincial Key Laboratory of Colorectal and Pelvic Floor Diseases, The Sixth Affiliated Hospital, Sun Yat-sen University, Guangzhou, Guangdong, China"},{"name":"Medical Diagnostic Center, The Sixth Affiliated Hospital of Sun Yat-sen University, Guangzhou, Guangdong, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yan","family":"Yi","sequence":"additional","affiliation":[{"name":"Guangdong Provincial Key Laboratory of Colorectal and Pelvic Floor Diseases, The Sixth Affiliated Hospital, Sun Yat-sen University, Guangzhou, Guangdong, China"},{"name":"Medical Diagnostic Center, The Sixth Affiliated Hospital of Sun Yat-sen University, Guangzhou, Guangdong, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Sui-Yan","family":"Xia","sequence":"additional","affiliation":[{"name":"Guangdong Provincial Key Laboratory of Colorectal and Pelvic Floor Diseases, The Sixth Affiliated Hospital, Sun Yat-sen University, Guangzhou, Guangdong, China"},{"name":"Medical Diagnostic Center, The Sixth Affiliated Hospital of Sun Yat-sen University, Guangzhou, Guangdong, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ling-Jie","family":"Huang","sequence":"additional","affiliation":[{"name":"Department of Gastroenterology, Sir Run Run Shaw Hospital, School of Medicine, Zhejiang University, Hangzhou, Zhejiang, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yuan","family":"Zhao","sequence":"additional","affiliation":[{"name":"Department of Gastroenterology, Sir Run Run Shaw Hospital, School of Medicine, Zhejiang University, Hangzhou, Zhejiang, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Xiao-Hong","family":"Wang","sequence":"additional","affiliation":[{"name":"Guangdong Provincial Key Laboratory of Colorectal and Pelvic Floor Diseases, The Sixth Affiliated Hospital, Sun Yat-sen University, Guangzhou, Guangdong, China"},{"name":"Obstetrical Department, The Sixth Affiliated Hospital of Sun Yat-sen University, Guangzhou, Guangdong, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Xiao-Ying","family":"Liu","sequence":"additional","affiliation":[{"name":"Guangdong Provincial Key Laboratory of Colorectal and Pelvic Floor Diseases, The Sixth Affiliated Hospital, Sun Yat-sen University, Guangzhou, Guangdong, China"},{"name":"Obstetrical Department, The Sixth Affiliated Hospital of Sun Yat-sen University, Guangzhou, Guangdong, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Lin","family":"Lin","sequence":"additional","affiliation":[{"name":"Guangdong Provincial Key Laboratory of Colorectal and Pelvic Floor Diseases, The Sixth Affiliated Hospital, Sun Yat-sen University, Guangzhou, Guangdong, China"},{"name":"Obstetrical Department, The Sixth Affiliated Hospital of Sun Yat-sen University, Guangzhou, Guangdong, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Pin-Jin","family":"Hu","sequence":"additional","affiliation":[{"name":"Department of Gastroenterology, The Sixth Affiliated Hospital of Sun Yat-sen University, Guangzhou, Guangdong, China"},{"name":"Guangdong Provincial Key Laboratory of Colorectal and Pelvic Floor Diseases, The Sixth Affiliated Hospital, Sun Yat-sen University, Guangzhou, Guangdong, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Xiang","family":"Gao","sequence":"additional","affiliation":[{"name":"Department of Gastroenterology, The Sixth Affiliated Hospital of Sun Yat-sen University, Guangzhou, Guangdong, China"},{"name":"Guangdong Provincial Key Laboratory of Colorectal and Pelvic Floor Diseases, The Sixth Affiliated Hospital, Sun Yat-sen University, Guangzhou, Guangdong, China"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"286","published-online":{"date-parts":[[2019,2,15]]},"reference":[{"key":"2019103013414729400_goy053-B1","doi-asserted-by":"crossref","first-page":"2137","DOI":"10.1200\/JCO.2005.05.2308","article-title":"Patterns of cancer incidence, mortality, and prevalence across five continents: defining priorities to reduce cancer disparities in different geographic regions of the world","volume":"24","author":"Kamangar","year":"2006","journal-title":"J Clinc Oncol"},{"key":"2019103013414729400_goy053-B2","first-page":"C1","article-title":"HPV and cervical cancer in the world 2007 report","volume":"25","author":"Castellsague","year":"2007","journal-title":"Vaccine"},{"key":"2019103013414729400_goy053-B3","first-page":"241","article-title":"Incidence and mortality of cervical cancer in China, 2014","volume":"40","author":"Gu","year":"2018","journal-title":"Zhonghua Zhong Liu Za Zhi"},{"key":"2019103013414729400_goy053-B4","doi-asserted-by":"crossref","first-page":"12","DOI":"10.1002\/(SICI)1096-9896(199909)189:1<12::AID-PATH431>3.0.CO;2-F","article-title":"Human papillomarvirus is a necessary cause of invasive cervical cancer worldwide","volume":"189","author":"Walboomer","year":"1999","journal-title":"J Pathol"},{"key":"2019103013414729400_goy053-B5","doi-asserted-by":"crossref","first-page":"244","DOI":"10.1136\/jcp.55.4.244","article-title":"The causal relation between human papillomavirus and cervical cancer","volume":"55","author":"Bosch","year":"2002","journal-title":"J Clin Pathol"},{"key":"2019103013414729400_goy053-B6","doi-asserted-by":"crossref","first-page":"343","DOI":"10.1093\/rheumatology\/keq304","article-title":"Meta-analysis of systemic lupus erythematosus and the risk of cervical neoplasia","volume":"50","author":"Liu","year":"2011","journal-title":"Rheumatology (Oxford)"},{"key":"2019103013414729400_goy053-B7","doi-asserted-by":"crossref","first-page":"365","DOI":"10.1177\/0961203311425517","article-title":"Cervical human papillomavirus infection in Mexican women with systemic lupus erythematosus or rheumatoid arthritis","volume":"21","author":"Rojo-Contreras","year":"2012","journal-title":"Lupus"},{"key":"2019103013414729400_goy053-B8","first-page":"1763","article-title":"Increased incidence of cervical intraepithelial neoplasia in women with systemic lupus erythematosus treated with intravenous cyclophosphamide","volume":"31","author":"Ognenovski","year":"2004","journal-title":"J Rheumatol"},{"key":"2019103013414729400_goy053-B9","doi-asserted-by":"crossref","first-page":"2823","DOI":"10.1001\/jama.296.23.2823","article-title":"Cancer incidence before and after kidney transplantation","volume":"296","author":"Vajdic","year":"2006","journal-title":"JAMA"},{"key":"2019103013414729400_goy053-B10","doi-asserted-by":"crossref","first-page":"427","DOI":"10.1038\/nature06005","article-title":"Unravelling the pathogenesis of inflammatory bowel disease","volume":"448","author":"Xavier","year":"2007","journal-title":"Nature"},{"key":"2019103013414729400_goy053-B11","doi-asserted-by":"crossref","first-page":"165","DOI":"10.1093\/gastro\/gow046","article-title":"Perioperative use of immunosuppressive medications in patients with Crohn\u2019s disease in the new \u2018biological era\u2019","volume":"5","author":"Lightner","year":"2017","journal-title":"Gastroenterol Rep (Oxf)"},{"key":"2019103013414729400_goy053-B12","doi-asserted-by":"crossref","first-page":"1249","DOI":"10.1016\/S0140-6736(94)92150-4","article-title":"Long-term neoplasia risk after azathioprine treatment in inflammatory bowel disease","volume":"343","author":"Connell","year":"1994","journal-title":"Lancet"},{"key":"2019103013414729400_goy053-B13","doi-asserted-by":"crossref","first-page":"598","DOI":"10.1111\/j.1365-2036.2008.03766.x","article-title":"Screening differences and risk of cervical cancer in inflammatory bowel disease","volume":"28","author":"Hutfless","year":"2008","journal-title":"Aliment Pharmacol Ther"},{"key":"2019103013414729400_goy053-B14","doi-asserted-by":"crossref","first-page":"451","DOI":"10.1053\/j.gastro.2008.10.021","article-title":"Risk of cervical abnormalities in women with inflammatory bowel disease: a population-based nested case-control study","volume":"136","author":"Singh","year":"2009","journal-title":"Gastroenterology"},{"key":"2019103013414729400_goy053-B15","doi-asserted-by":"crossref","first-page":"6167","DOI":"10.3748\/wjg.v12.i38.6167","article-title":"Abnormalities of uterine cervix in women with inflammatory bowel disease","volume":"12","author":"Bhatia","year":"2006","journal-title":"World J Gastroenterol"},{"key":"2019103013414729400_goy053-B16","doi-asserted-by":"crossref","first-page":"1621","DOI":"10.1002\/ibd.20959","article-title":"Lack of association between cervical dysplasia and IBD: a large case-control study","volume":"15","author":"Lees","year":"2009","journal-title":"Inflamm Bowel Dis"},{"key":"2019103013414729400_goy053-B17","doi-asserted-by":"crossref","first-page":"518","DOI":"10.1056\/NEJMoa021641","article-title":"Epidemiologic classification of human papillomavirus types associated with cervical cancer","volume":"348","author":"Mu\u00f1oz","year":"2003","journal-title":"N Engl J Med"},{"key":"2019103013414729400_goy053-B18","doi-asserted-by":"crossref","first-page":"147","DOI":"10.3322\/caac.21139","article-title":"American Cancer Society, American Society for Colposcopy and Cervical Pathology, and American Society for Clinical Pathology screening guidelines for the prevention and early detection of cervical cancer","volume":"62","author":"Saslow","year":"2012","journal-title":"CA Cancer J Clin"},{"key":"2019103013414729400_goy053-B19","doi-asserted-by":"crossref","first-page":"71","DOI":"10.1002\/jcb.240590910","article-title":"Cervical intraepithelial neoplasia","volume":"23","author":"Crum","year":"1995","journal-title":"J Cell Biochem Suppl"},{"key":"2019103013414729400_goy053-B20","doi-asserted-by":"crossref","first-page":"1360","DOI":"10.1136\/annrheumdis-2013-204993","article-title":"Risk of high-grade cervical dysplasia and cervical cancer in women with systemic inflammatory diseases: a population-based cohort study","volume":"74","author":"Kim","year":"2015","journal-title":"Ann Rheum Dis"},{"key":"2019103013414729400_goy053-B21","doi-asserted-by":"crossref","first-page":"631","DOI":"10.1111\/j.1572-0241.2007.01582.x","article-title":"Higher incidence of abnormal Pap smears in women with inflammatory bowel disease","volume":"103","author":"Kane","year":"2008","journal-title":"Am J Gastroenterol"},{"key":"2019103013414729400_goy053-B22","doi-asserted-by":"crossref","first-page":"910","DOI":"10.1016\/0002-9378(88)90093-2","article-title":"Smoking and cervical intraepithelial neoplasia: nicotine and cotimne in serum and cervical mucns in smokers and nonsmokers","volume":"158","author":"Hellberg","year":"1988","journal-title":"Am J Obstet Gynecol"},{"key":"2019103013414729400_goy053-B23","doi-asserted-by":"crossref","first-page":"813","DOI":"10.1001\/jama.297.8.813","article-title":"Prevalence of HPV infection among females in the United States","volume":"297","author":"Dunne","year":"2007","journal-title":"JAMA"},{"key":"2019103013414729400_goy053-B24","doi-asserted-by":"crossref","first-page":"823","DOI":"10.1097\/00001703-199312000-00018","article-title":"Contraception choice and sexually transmitted disease","volume":"5","author":"Barnhart","year":"1993","journal-title":"Curr Opin Obstet Gynecol"},{"key":"2019103013414729400_goy053-B25","doi-asserted-by":"crossref","first-page":"1030","DOI":"10.1016\/j.jaci.2012.07.049","article-title":"Warts and all: human papillomavirus in primary immunodeficiencies","volume":"130","author":"Leiding","year":"2012","journal-title":"J Allergy Clin Immunol"},{"key":"2019103013414729400_goy053-B26","doi-asserted-by":"crossref","first-page":"1491","DOI":"10.1007\/s10552-016-0826-2","article-title":"The association of medication use with clearance or persistence of oral HPV infection","volume":"27","author":"Lam","year":"2016","journal-title":"Cancer Causes Control"},{"key":"2019103013414729400_goy053-B27","doi-asserted-by":"crossref","first-page":"127","DOI":"10.1159\/000051612","article-title":"Widespread cutaneous carcinomas associated with human papillomaviruses 5, 14 and 20 after introduction of methotrexate in two long-term PUVA-treated patients","volume":"202","author":"Zumtobel","year":"2001","journal-title":"Dermatology (Basel)"},{"key":"2019103013414729400_goy053-B28","doi-asserted-by":"crossref","first-page":"55","DOI":"10.1007\/s40615-015-0112-0","article-title":"Human papilloma virus awareness among Hispanic females with inflammatory bowel disease","volume":"3","author":"Rivera-Acosta","year":"2016","journal-title":"J Racial Ethn Health Disparities"},{"key":"2019103013414729400_goy053-B29","doi-asserted-by":"crossref","first-page":"E6","DOI":"10.1002\/ibd.22836","article-title":"Women with inflammatory bowel disease do not receive adequate cervical cancer screening or pregnancy counseling","volume":"19","author":"Greywoode","year":"2013","journal-title":"Inflamm Bowel Dis"},{"key":"2019103013414729400_goy053-B30","doi-asserted-by":"crossref","first-page":"945","DOI":"10.1093\/ecco-jcc\/jjv141","article-title":"European evidence-based consensus: inflammatory bowel disease and malignancies","volume":"9","author":"Annese","year":"2015","journal-title":"J Crohns Colitis"}],"container-title":["Gastroenterology Report"],"original-title":[],"language":"en","link":[{"URL":"http:\/\/academic.oup.com\/gastro\/article-pdf\/7\/5\/338\/30333101\/goy053.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"syndication"},{"URL":"http:\/\/academic.oup.com\/gastro\/article-pdf\/7\/5\/338\/30333101\/goy053.pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2019,10,30]],"date-time":"2019-10-30T15:03:21Z","timestamp":1572447801000},"score":1,"resource":{"primary":{"URL":"https:\/\/academic.oup.com\/gastro\/article\/7\/5\/338\/5320444"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2019,2,15]]},"references-count":30,"journal-issue":{"issue":"5","published-online":{"date-parts":[[2019,2,15]]},"published-print":{"date-parts":[[2019,10,1]]}},"URL":"https:\/\/doi.org\/10.1093\/gastro\/goy053","relation":{},"ISSN":["2052-0034"],"issn-type":[{"value":"2052-0034","type":"electronic"}],"subject":[],"published-other":{"date-parts":[[2019,10]]},"published":{"date-parts":[[2019,2,15]]}}}