{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,3,4]],"date-time":"2026-03-04T05:37:07Z","timestamp":1772602627517,"version":"3.50.1"},"reference-count":39,"publisher":"Public Library of Science (PLoS)","issue":"3","license":[{"start":{"date-parts":[[2021,3,8]],"date-time":"2021-03-08T00:00:00Z","timestamp":1615161600000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100007137","name":"Helse Nord RHF","doi-asserted-by":"publisher","award":["SFP1134-13"],"award-info":[{"award-number":["SFP1134-13"]}],"id":[{"id":"10.13039\/501100007137","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100007137","name":"Helse Nord RHF","doi-asserted-by":"crossref","award":["HNF1517-20"],"award-info":[{"award-number":["HNF1517-20"]}],"id":[{"id":"10.13039\/501100007137","id-type":"DOI","asserted-by":"crossref"}]},{"DOI":"10.13039\/501100007137","name":"Helse Nord RHF","doi-asserted-by":"publisher","award":["HNF1468-19"],"award-info":[{"award-number":["HNF1468-19"]}],"id":[{"id":"10.13039\/501100007137","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100007465","name":"UiT The Arctic University of Norway","doi-asserted-by":"crossref","id":[{"id":"10.13039\/100007465","id-type":"DOI","asserted-by":"crossref"}]}],"content-domain":{"domain":["www.plosone.org"],"crossmark-restriction":false},"short-container-title":["PLoS ONE"],"abstract":"<jats:sec id=\"sec001\">\n<jats:title>Background<\/jats:title>\n<jats:p>Histological evaluation of ulcerative colitis (UC) patients has been debated ever since the first description of the disease and its role in follow-up has never been fully established. Recent evidence suggests an added benefit in accuracy when evaluating if the patient is in remission. Unfortunately, there are several different histological indices, and it is difficult to compare outcomes where different scores are applied. Histopathological evaluation is prone to subjective biases, despite the use of indices. In addition, these indices are developed by expert IBD pathologist, but applied at large, by general pathologist. Therefore, we evaluated the three most applied histological indices for UC on samples from patients in remission to compare test qualities and estimate their usefulness to identify remission by both general and GI specialized pathologist.<\/jats:p>\n<\/jats:sec>\n<jats:sec id=\"sec002\">\n<jats:title>Method<\/jats:title>\n<jats:p>Mucosal biopsies from 41 UC patients in clinical and endoscopic remission were collected as part of a larger study on UC. Three pathologists blinded to the patients\u2019 clinical status evaluated them using Geboes score (GS), Nancy Index (NI) and Robarts Histopathological Index (RHI). We calculated the agreement between the pathologists using Inter-class correlation (ICC) and visualized it with ICC-plots and Bland-Altman plots. Association between clinical factors and histological category were analysed by Fisher\u2019s exact test.<\/jats:p>\n<\/jats:sec>\n<jats:sec id=\"sec003\">\n<jats:title>Results<\/jats:title>\n<jats:p>The ICC value for GS, RHI and NI were 0.85, 0.73 and 0.70 respectively. The limits of agreement were \u00b16.1, \u00b14.0 and \u00b11.4, for GS, RHI and NI, respectively. Mayo endoscopic subgrade and UC clinical score did not show association with any histological scores. Despite clinical and endoscopic remission 7\u201335% of the patients displayed histological inflammation on a level classified as active disease, depending on the index and cut-off.<\/jats:p>\n<\/jats:sec>\n<jats:sec id=\"sec004\">\n<jats:title>Conclusion<\/jats:title>\n<jats:p>A substantial amount of UC patients in clinical and endoscopic remission display inflammation on a histological level, but the ability to classify these patients accurately and consistently could be improved.<\/jats:p>\n<\/jats:sec>","DOI":"10.1371\/journal.pone.0248224","type":"journal-article","created":{"date-parts":[[2021,3,8]],"date-time":"2021-03-08T18:26:46Z","timestamp":1615228006000},"page":"e0248224","update-policy":"https:\/\/doi.org\/10.1371\/journal.pone.corrections_policy","source":"Crossref","is-referenced-by-count":15,"title":["Real-life evaluation of histologic scores for Ulcerative Colitis in remission"],"prefix":"10.1371","volume":"16","author":[{"ORCID":"https:\/\/orcid.org\/0000-0003-4787-7603","authenticated-orcid":true,"given":"Christian B\u00f8rde","family":"Arkteg","sequence":"first","affiliation":[]},{"ORCID":"https:\/\/orcid.org\/0000-0002-8250-3992","authenticated-orcid":true,"given":"Sveinung","family":"Wergeland S\u00f8rbye","sequence":"additional","affiliation":[]},{"given":"Lene","family":"Buhl Riis","sequence":"additional","affiliation":[]},{"given":"Stig Manfred","family":"Dalen","sequence":"additional","affiliation":[]},{"given":"Jon","family":"Florholmen","sequence":"additional","affiliation":[]},{"ORCID":"https:\/\/orcid.org\/0000-0003-4375-0509","authenticated-orcid":true,"given":"Rasmus","family":"Goll","sequence":"additional","affiliation":[]}],"member":"340","published-online":{"date-parts":[[2021,3,8]]},"reference":[{"issue":"4","key":"pone.0248224.ref001","doi-asserted-by":"crossref","first-page":"1250","DOI":"10.1053\/j.gastro.2009.06.061","article-title":"Colectomy Rate Comparison After Treatment of Ulcerative Colitis With Placebo or Infliximab","volume":"137","author":"WJ Sandborn","year":"2009","journal-title":"Gastroenterology"},{"key":"pone.0248224.ref002","first-page":"23","article-title":"Has infliximab influenced the course and prognosis of acute severe ulcerative colitis?","volume":"13","author":"A Viscido","year":"2019","journal-title":"Biologics"},{"issue":"8","key":"pone.0248224.ref003","doi-asserted-by":"crossref","first-page":"1017","DOI":"10.1016\/j.cgh.2006.05.020","article-title":"Risks and benefits of infliximab for the treatment of Crohn\u2019s disease","volume":"4","author":"CA Siegel","year":"2006","journal-title":"Clinical gastroenterology and hepatology: the official clinical practice journal of the American Gastroenterological Association"},{"issue":"9","key":"pone.0248224.ref004","doi-asserted-by":"crossref","first-page":"1324","DOI":"10.1038\/ajg.2015.233","article-title":"Selecting Therapeutic Targets in Inflammatory Bowel Disease (STRIDE): Determining Therapeutic Goals for Treat-to-Target","volume":"110","author":"L Peyrin-Biroulet","year":"2015","journal-title":"The American journal of gastroenterology"},{"issue":"2","key":"pone.0248224.ref005","doi-asserted-by":"crossref","first-page":"144","DOI":"10.1093\/ecco-jcc\/jjy113","article-title":"ECCO-ESGAR Guideline for Diagnostic Assessment in IBD Part 1: Initial diagnosis, monitoring of known IBD, detection of complications","volume":"13","author":"C Maaser","year":"2019","journal-title":"Journal of Crohn\u2019s & colitis"},{"key":"pone.0248224.ref006","article-title":"British Society of Gastroenterology consensus guidelines on the management of inflammatory bowel disease in adults","author":"CA Lamb","year":"2019","journal-title":"Gut"},{"issue":"6","key":"pone.0248224.ref007","doi-asserted-by":"crossref","first-page":"874","DOI":"10.14309\/ajg.0000000000000183","article-title":"A Treat-to-Target Update in Ulcerative Colitis","volume":"114","author":"R Ungaro","year":"2019","journal-title":"A Systematic Review. American Journal of Gastroenterology"},{"issue":"3","key":"pone.0248224.ref008","doi-asserted-by":"crossref","first-page":"408","DOI":"10.1136\/gutjnl-2015-309598","article-title":"Beyond endoscopic mucosal healing in UC: histological remission better predicts corticosteroid use and hospitalisation over 6 years of follow-up","volume":"65","author":"RV Bryant","year":"2016","journal-title":"Gut"},{"key":"pone.0248224.ref009","first-page":"5832051","article-title":"Correlation between Histological Activity and Endoscopic, Clinical, and Serologic Activities in Patients with Ulcerative Colitis","volume":"2016","author":"DB Kim","year":"2016","journal-title":"Gastroenterology research and practice"},{"issue":"8","key":"pone.0248224.ref010","doi-asserted-by":"crossref","first-page":"726","DOI":"10.1055\/s-0034-1391863","article-title":"Complete mucosal healing defined by endoscopic Mayo subscore still demonstrates abnormalities by novel high definition colonoscopy and refined histological gradings","volume":"47","author":"M Iacucci","year":"2015","journal-title":"Endoscopy"},{"issue":"10","key":"pone.0248224.ref011","doi-asserted-by":"crossref","first-page":"749","DOI":"10.1177\/1756283X17722926","article-title":"The prognostic value of histology in ulcerative colitis in clinical remission with mesalazine","volume":"10","author":"G Frieri","year":"2017","journal-title":"Therapeutic Advances in Gastroenterology"},{"issue":"5","key":"pone.0248224.ref012","doi-asserted-by":"crossref","first-page":"765","DOI":"10.1177\/2050640617752207","article-title":"Prognostic value of histological activity in patients with ulcerative colitis in deep remission: A prospective multicenter study","volume":"6","author":"T Lobat\u00f3n","year":"2018","journal-title":"United European Gastroenterology Journal"},{"issue":"4","key":"pone.0248224.ref013","doi-asserted-by":"crossref","first-page":"1099","DOI":"10.1053\/j.gastro.2007.08.001","article-title":"Histologic inflammation is a risk factor for progression to colorectal neoplasia in ulcerative colitis: a cohort study","volume":"133","author":"RB Gupta","year":"2007","journal-title":"Gastroenterology"},{"key":"pone.0248224.ref014","article-title":"ECCO Position Paper: Harmonisation of the approach to Ulcerative Colitis Histopathology","author":"F Magro","year":"2020","journal-title":"Journal of Crohn\u2019s & colitis"},{"issue":"2","key":"pone.0248224.ref015","doi-asserted-by":"crossref","first-page":"159","DOI":"10.1007\/s40265-016-0676-y","article-title":"Mucosal Healing in Ulcerative Colitis: A Comprehensive Review","volume":"77","author":"P Boal Carvalho","year":"2017","journal-title":"Drugs"},{"issue":"6","key":"pone.0248224.ref016","doi-asserted-by":"crossref","first-page":"887","DOI":"10.1016\/j.gie.2018.08.018","article-title":"The emerging role of histologic disease activity assessment in ulcerative colitis","volume":"88","author":"RK Pai","year":"2018","journal-title":"Gastrointestinal Endoscopy"},{"issue":"3","key":"pone.0248224.ref017","doi-asserted-by":"crossref","first-page":"564","DOI":"10.1097\/01.MIB.0000437986.00190.71","article-title":"Histologic evaluation of ulcerative colitis: a systematic review of disease activity indices","volume":"20","author":"MH Mosli","year":"2014","journal-title":"Inflammatory bowel diseases"},{"issue":"3","key":"pone.0248224.ref018","doi-asserted-by":"crossref","first-page":"404","DOI":"10.1136\/gut.47.3.404","article-title":"A reproducible grading scale for histological assessment of inflammation in ulcerative colitis","volume":"47","author":"K Geboes","year":"2000","journal-title":"Gut"},{"issue":"1","key":"pone.0248224.ref019","doi-asserted-by":"crossref","first-page":"50","DOI":"10.1136\/gutjnl-2015-310393","article-title":"Development and validation of a histological index for UC","volume":"66","author":"MH Mosli","year":"2017","journal-title":"Gut"},{"issue":"1","key":"pone.0248224.ref020","doi-asserted-by":"crossref","first-page":"43","DOI":"10.1136\/gutjnl-2015-310187","article-title":"Development and validation of the Nancy histological index for UC","volume":"66","author":"A Marchal-Bressenot","year":"2017","journal-title":"Gut"},{"issue":"3","key":"pone.0248224.ref021","first-page":"305","article-title":"A Simplified Geboes Score for Ulcerative Colitis","volume":"11","author":"A Jauregui-Amezaga","year":"2017","journal-title":"Journal of Crohn\u2019s and Colitis"},{"issue":"18","key":"pone.0248224.ref022","doi-asserted-by":"crossref","first-page":"1754","DOI":"10.1056\/NEJMoa1513248","article-title":"Ozanimod Induction and Maintenance Treatment for Ulcerative Colitis","volume":"374","author":"WJ Sandborn","year":"2016","journal-title":"The New England journal of medicine"},{"issue":"5","key":"pone.0248224.ref023","doi-asserted-by":"crossref","first-page":"685","DOI":"10.1038\/ajg.2016.50","article-title":"Histology Grade Is Independently Associated With Relapse Risk in Patients With Ulcerative Colitis in Clinical Remission: A Prospective Study","volume":"111","author":"T Zenlea","year":"2016","journal-title":"The American journal of gastroenterology"},{"issue":"3","key":"pone.0248224.ref024","doi-asserted-by":"crossref","first-page":"194","DOI":"10.4103\/1319-3767.80383","article-title":"Biological and histological parameters as predictors of relapse in ulcerative colitis: a prospective study. Saudi journal of gastroenterology: official journal of the","volume":"17","author":"S Azad","year":"2011","journal-title":"Saudi Gastroenterology Association"},{"issue":"4","key":"pone.0248224.ref025","doi-asserted-by":"crossref","first-page":"594","DOI":"10.1136\/gutjnl-2017-315545","article-title":"Comparison of different histological indexes in the assessment of UC activity and their accuracy regarding endoscopic outcomes and faecal calprotectin levels","volume":"68","author":"F Magro","year":"2019","journal-title":"Gut"},{"key":"pone.0248224.ref026","article-title":"Definitions of response and remission for the Robarts Histopathology Index","author":"RK Pai","year":"2018","journal-title":"Gut"},{"key":"pone.0248224.ref027","article-title":"Comparison of the Nancy Index With Continuous Geboes Score: Histological Remission and Response in Ulcerative Colitis","author":"F Magro","year":"2020","journal-title":"Journal of Crohn\u2019s and Colitis"},{"issue":"2","key":"pone.0248224.ref028","doi-asserted-by":"crossref","first-page":"174","DOI":"10.1136\/gut.32.2.174","article-title":"Microscopic activity in ulcerative colitis: what does it mean","volume":"32","author":"SA Riley","year":"1991","journal-title":"Gut"},{"issue":"1","key":"pone.0248224.ref029","doi-asserted-by":"crossref","first-page":"13","DOI":"10.1053\/gast.2001.20912","article-title":"Clinical, biological, and histologic parameters as predictors of relapse in ulcerative colitis","volume":"120","author":"A Bitton","year":"2001","journal-title":"Gastroenterology"},{"issue":"11","key":"pone.0248224.ref030","doi-asserted-by":"crossref","first-page":"1684","DOI":"10.1038\/ajg.2012.301","article-title":"Prognostic value of serologic and histologic markers on clinical relapse in ulcerative colitis patients with mucosal healing","volume":"107","author":"T Bessissow","year":"2012","journal-title":"The American journal of gastroenterology"},{"issue":"1","key":"pone.0248224.ref031","doi-asserted-by":"crossref","first-page":"159","DOI":"10.2307\/2529310","article-title":"The Measurement of Observer Agreement for Categorical Data","volume":"33","author":"JR Landis","year":"1977","journal-title":"Biometrics"},{"issue":"5","key":"pone.0248224.ref032","doi-asserted-by":"crossref","first-page":"1308","DOI":"10.1093\/ije\/dyr109","article-title":"A graphical method for assessing agreement with the mean between multiple observers using continuous measures","volume":"40","author":"M Jones","year":"2011","journal-title":"International Journal of Epidemiology"},{"issue":"2","key":"pone.0248224.ref033","doi-asserted-by":"crossref","first-page":"155","DOI":"10.1016\/j.jcm.2016.02.012","article-title":"A Guideline of Selecting and Reporting Intraclass Correlation Coefficients for Reliability Research","volume":"15","author":"TK Koo","year":"2016","journal-title":"J Chiropr Med"},{"issue":"1","key":"pone.0248224.ref034","doi-asserted-by":"crossref","first-page":"55","DOI":"10.5217\/ir.2018.16.1.55","article-title":"Association of endoscopic and histological remission with clinical course in patients of ulcerative colitis","volume":"16","author":"V Narang","year":"2018","journal-title":"Intest Res."},{"issue":"8","key":"pone.0248224.ref035","doi-asserted-by":"crossref","first-page":"991","DOI":"10.1016\/j.cgh.2013.02.030","article-title":"Histologic Markers of Inflammation in Patients With Ulcerative Colitis in Clinical Remission","volume":"11","author":"L Rosenberg","year":"2013","journal-title":"Clinical Gastroenterology and Hepatology"},{"issue":"7","key":"pone.0248224.ref036","doi-asserted-by":"crossref","first-page":"1162","DOI":"10.1136\/gutjnl-2018-316702","article-title":"Responsiveness of histological disease activity indices in ulcerative colitis: a post hoc analysis using data from the TOUCHSTONE randomised controlled trial","volume":"68","author":"V Jairath","year":"2019","journal-title":"Gut"},{"issue":"1","key":"pone.0248224.ref037","doi-asserted-by":"crossref","first-page":"S7","DOI":"10.1038\/modpathol.2014.132","article-title":"Eosinophils in the GI tract: How many is too many and what do they mean?","volume":"28","author":"RK Yantiss","year":"2015","journal-title":"Modern Pathology"},{"issue":"6","key":"pone.0248224.ref038","doi-asserted-by":"crossref","first-page":"1194","DOI":"10.1097\/MIB.0b013e318280e75f","article-title":"Correlation between the endoscopic and histologic score in assessing the activity of ulcerative colitis","volume":"19","author":"B Lemmens","year":"2013","journal-title":"Inflammatory bowel diseases."},{"issue":"11","key":"pone.0248224.ref039","doi-asserted-by":"crossref","first-page":"1438","DOI":"10.1016\/j.crohns.2014.05.003","article-title":"Endoscopic biopsy samples of naive \"colitides\" patients: role of basal plasmacytosis","volume":"8","author":"V Villanacci","year":"2014","journal-title":"Journal of Crohn\u2019s & colitis"}],"container-title":["PLOS ONE"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.pone.0248224","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2021,3,8]],"date-time":"2021-03-08T18:27:58Z","timestamp":1615228078000},"score":1,"resource":{"primary":{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.pone.0248224"}},"subtitle":[],"editor":[{"given":"Val\u00e9rie","family":"Pittet","sequence":"first","affiliation":[]}],"short-title":[],"issued":{"date-parts":[[2021,3,8]]},"references-count":39,"journal-issue":{"issue":"3","published-online":{"date-parts":[[2021,3,8]]}},"URL":"https:\/\/doi.org\/10.1371\/journal.pone.0248224","relation":{},"ISSN":["1932-6203"],"issn-type":[{"value":"1932-6203","type":"electronic"}],"subject":[],"published":{"date-parts":[[2021,3,8]]}}}