{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2025,11,20]],"date-time":"2025-11-20T13:05:34Z","timestamp":1763643934327,"version":"build-2065373602"},"reference-count":36,"publisher":"MDPI AG","issue":"15","license":[{"start":{"date-parts":[[2023,7,26]],"date-time":"2023-07-26T00:00:00Z","timestamp":1690329600000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"MUR-PNRR M4C2I1.3 PE6 project PE00000019 Heal Italia","award":["CUP: E83C22004670001"],"award-info":[{"award-number":["CUP: E83C22004670001"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Cancers"],"abstract":"<jats:p>A higher frequency of mucinous and signet-ring cell colonic adenocarcinoma has been reported in inflammatory bowel disease (IBD). The primary aim was to investigate the frequency of mucinous and signet-ring cell colorectal adenocarcinoma in patients with IBD (Cases) versus age-matched non-IBD Controls. The secondary aims were to compare the characteristics of these two histotypes of colorectal cancer (CRC) in IBD patients vs. Controls and to search for specific risk factors in IBD. In a case\u2013control study, all IBD patients with CRC diagnosed from 2000 to 2022 were enrolled and matched for age (1:2) with non-IBD Controls with CRC. The study population included 120 CRC patients (40 IBD, 80 Controls). In IBD, CRC included standard adenocarcinoma in 23 (57.5%) patients mucinous\/signet-ring cell adenocarcinoma in 17 (42.5%) patients. The proportion of mucinous\/signet-ring cell adenocarcinoma was higher in IBD than in Controls (17 [42.5%] vs. 18 [22.5%]; p = 0.03). In rectal CRC, the proportion of mucinous\/signet-ring cell adenocarcinoma was higher than standard adenocarcinoma in IBD (8 [47.1%] vs. 4 [17.4%]; p = 0.04) but not in Controls (4 [22.2%] vs. 20 [32.2%]; p = 0.59). In rectal CRC, the proportion of these two histotypes was higher in Cases than in Controls (8\/12 [66.6%] vs. 4\/24 [16.6%]; p = 0.008), with no risk factors identified in IBD. CRC was more frequently represented by mucinous\/signet-ring cell adenocarcinoma in IBD than in age-matched non-IBD Controls. In IBD, these two CRC histotypes were more frequent in the rectum.<\/jats:p>","DOI":"10.3390\/cancers15153803","type":"journal-article","created":{"date-parts":[[2023,7,27]],"date-time":"2023-07-27T02:07:17Z","timestamp":1690423637000},"page":"3803","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":8,"title":["Mucinous and Signet-Ring Cell Colonic Adenocarcinoma in Inflammatory Bowel Disease: A Case\u2013Control Study"],"prefix":"10.3390","volume":"15","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-0803-7903","authenticated-orcid":false,"given":"Benedetto","family":"Neri","sequence":"first","affiliation":[{"name":"Gastroenterology Unit, Department of Systems Medicine, University \u201cTor Vergata\u201d of Rome, 00133 Roma, Italy"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Roberto","family":"Mancone","sequence":"additional","affiliation":[{"name":"Gastroenterology Unit, Department of Systems Medicine, University \u201cTor Vergata\u201d of Rome, 00133 Roma, Italy"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Luca","family":"Savino","sequence":"additional","affiliation":[{"name":"Pathology Unit, Department of Biomedicine and Prevention, University \u201cTor Vergata\u201d of Rome, 00133 Roma, Italy"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Sara","family":"Schiavone","sequence":"additional","affiliation":[{"name":"Gastroenterology Unit, Department of Systems Medicine, University \u201cTor Vergata\u201d of Rome, 00133 Roma, Italy"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-5380-3144","authenticated-orcid":false,"given":"Vincenzo","family":"Formica","sequence":"additional","affiliation":[{"name":"Medical Oncology Unit, Department of Systems Medicine, University \u201cTor Vergata\u201d of Rome, 00133 Roma, Italy"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Francesca","family":"Pizzi","sequence":"additional","affiliation":[{"name":"Gastroenterology Unit, Department of Systems Medicine, University \u201cTor Vergata\u201d of Rome, 00133 Roma, Italy"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-4980-6289","authenticated-orcid":false,"given":"Silvia","family":"Salvatori","sequence":"additional","affiliation":[{"name":"Gastroenterology Unit, Department of Systems Medicine, University \u201cTor Vergata\u201d of Rome, 00133 Roma, Italy"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-5013-7484","authenticated-orcid":false,"given":"Michelangela","family":"Mossa","sequence":"additional","affiliation":[{"name":"Gastroenterology Unit, Department of Systems Medicine, University \u201cTor Vergata\u201d of Rome, 00133 Roma, Italy"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Stefano","family":"Migliozzi","sequence":"additional","affiliation":[{"name":"Gastroenterology Unit, Department of Systems Medicine, University \u201cTor Vergata\u201d of Rome, 00133 Roma, Italy"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Mariasofia","family":"Fiorillo","sequence":"additional","affiliation":[{"name":"Gastroenterology Unit, Department of Systems Medicine, University \u201cTor Vergata\u201d of Rome, 00133 Roma, Italy"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Cristina","family":"Morelli","sequence":"additional","affiliation":[{"name":"Medical Oncology Unit, Department of Systems Medicine, University \u201cTor Vergata\u201d of Rome, 00133 Roma, Italy"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0009-0006-7913-5320","authenticated-orcid":false,"given":"Alessandro","family":"Moscardelli","sequence":"additional","affiliation":[{"name":"Gastroenterology Unit, Department of Systems Medicine, University \u201cTor Vergata\u201d of Rome, 00133 Roma, Italy"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Elisabetta","family":"Lolli","sequence":"additional","affiliation":[{"name":"Gastroenterology Unit, Department of Systems Medicine, University \u201cTor Vergata\u201d of Rome, 00133 Roma, Italy"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Emma","family":"Calabrese","sequence":"additional","affiliation":[{"name":"Gastroenterology Unit, Department of Systems Medicine, University \u201cTor Vergata\u201d of Rome, 00133 Roma, Italy"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Giuseppe S.","family":"Sica","sequence":"additional","affiliation":[{"name":"Department of Surgery, University \u201cTor Vergata\u201d of Rome, 00133 Roma, Italy"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-1339-9076","authenticated-orcid":false,"given":"Giovanni","family":"Monteleone","sequence":"additional","affiliation":[{"name":"Gastroenterology Unit, Department of Systems Medicine, University \u201cTor Vergata\u201d of Rome, 00133 Roma, Italy"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-9056-1957","authenticated-orcid":false,"given":"Livia","family":"Biancone","sequence":"additional","affiliation":[{"name":"Gastroenterology Unit, Department of Systems Medicine, University \u201cTor Vergata\u201d of Rome, 00133 Roma, Italy"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"1968","published-online":{"date-parts":[[2023,7,26]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"649","DOI":"10.1093\/ecco-jcc\/jjx008","article-title":"Third European evidence-based consensus on diagnosis and management of ulcerative colitis. Part 1: Definitions, diagnosis, extra-intestinal manifestations, pregnancy, cancer surveillance, surgery, and ileo\u2014Anal pouch disorders","volume":"11","author":"Magro","year":"2017","journal-title":"J. Crohns Colitis"},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"3","DOI":"10.1093\/ecco-jcc\/jjw168","article-title":"3rd European evidence-based consensus on the diagnosis and management of Crohn\u2019s disease 2016: Part 1: Diagnosis and medical management","volume":"11","author":"Dignass","year":"2017","journal-title":"J. Crohns Colitis"},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"800","DOI":"10.1097\/MIB.0b013e3182802af7","article-title":"Five-year mortality in colorectal cancer patients with ulcerative colitis or Crohn\u2019s disease: A nationwide population-based cohort study","volume":"19","author":"Ording","year":"2013","journal-title":"Inflamm. Bowel Dis."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"1043","DOI":"10.1053\/j.gastro.2021.05.063","article-title":"AGA clinical practice update on endoscopic surveillance and management of colorectal dysplasia in Inflammatory Bowel Diseases: Expert Review","volume":"161","author":"Murthy","year":"2021","journal-title":"Gastroenterology"},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"153","DOI":"10.1016\/S0140-6736(05)17706-X","article-title":"Colorectal cancer","volume":"365","author":"Weitz","year":"2005","journal-title":"Lancet"},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"526","DOI":"10.1136\/gut.48.4.526","article-title":"The risk of colorectal cancer in ulcerative colitis: A metanalysis","volume":"48","author":"Eaden","year":"2001","journal-title":"Gut"},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"1441","DOI":"10.1056\/NEJMra1403718","article-title":"Cancers complicating Inflammatory Bowel Disease","volume":"372","author":"Beaugerie","year":"2015","journal-title":"N. Engl. J. Med."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"382","DOI":"10.1053\/j.gastro.2012.04.054","article-title":"Incidence and mortality of colorectal adenocarcinoma in persons with inflammatory bowel disease from 1998 to 2010","volume":"143","author":"Herrinton","year":"2012","journal-title":"Gastroenterology"},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"451","DOI":"10.1053\/j.gastro.2003.11.010","article-title":"Severity of inflammation is a risk factor for colorectal neoplasia in Ulcerative Colitis","volume":"126","author":"Rutter","year":"2004","journal-title":"Gastroenterology"},{"key":"ref_10","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":"Gupta","year":"2007","journal-title":"Gastroenterology"},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"48","DOI":"10.1067\/mge.2002.125367","article-title":"Increased risk of colorectal neoplasia in patients with primary sclerosing cholangitis and ulcerative colitis: A meta-analysis","volume":"56","author":"Soetikno","year":"2002","journal-title":"Gastrointest. Endosc."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"35","DOI":"10.1016\/j.ejim.2021.08.010","article-title":"Surveillance and management of colorectal dysplasia and cancer in inflammatory bowel disease: Current practice and future perspectives","volume":"93","author":"Wijnands","year":"2021","journal-title":"Eur. J. Intern. Med."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"180","DOI":"10.1016\/j.canlet.2012.02.031","article-title":"Pan-colonic field defects are detected by CGH in the colons of UC patients with dysplasia\/cancer","volume":"320","author":"Lai","year":"2012","journal-title":"Cancer Lett."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"344","DOI":"10.1093\/gastro\/gov022","article-title":"Overexpression of p53 predicts colorectal neoplasia risk in patients with inflammatory bowel disease and mucosa changes indefinite for dysplasia","volume":"3","author":"Horvath","year":"2015","journal-title":"Gastroenterol. Rep."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"1161","DOI":"10.1007\/s10350-004-0932-1","article-title":"A 10-year outcomes evaluation of mucinous and signet ring cell carcinoma of the colon and rectum","volume":"48","author":"Kang","year":"2005","journal-title":"Dis. Colon Rectum"},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"950","DOI":"10.1136\/gut.35.7.950","article-title":"Similarity of colorectal cancer in Crohn\u2019s disease and ulcerative colitis: Implications for carcinogenesis and prevention","volume":"35","author":"Choi","year":"1994","journal-title":"Gut"},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"749","DOI":"10.1136\/gut.2005.082909","article-title":"The Montreal classification of inflammatory bowel disease: Controversies, consensus, and implications","volume":"55","author":"Satsangi","year":"2006","journal-title":"Gut"},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"827","DOI":"10.1093\/ecco-jcc\/jjac187","article-title":"ECCO Guidelines on Inflammatory Bowel Disease and Malignancies","volume":"17","author":"Gordon","year":"2022","journal-title":"J. Crohns Colitis"},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"1445","DOI":"10.1111\/apt.17495","article-title":"Risk of colorectal neoplasia according to histologic disease activity in patients with inflammatory bowel disease and colonic post-inflammatory polyps","volume":"57","author":"Wolf","year":"2023","journal-title":"Aliment. Pharmacol. Ther."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"1333","DOI":"10.1053\/j.gastro.2018.11.067","article-title":"Dutch Initiative on Crohn and Colitis. No association between pseudopolyps and colorectal neoplasia in patients with Inflammatory Bowel Diseases","volume":"156","author":"Mahmoud","year":"2019","journal-title":"Gastroenterology"},{"key":"ref_21","unstructured":"Bosman, F.T., Carneiro, F., Hruban, R.H., and Theise, N.D. (2010). WHO Classification of Tumours of the Digestive System, World Health Organization Classification of Tumours. [4th ed.]."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"319","DOI":"10.1097\/SLA.0000000000005339","article-title":"Survival outcomes and clinicopathological features in inflammatory bowel disease-associated colorectal cancer: A Systematic Review and Meta-analysis","volume":"276","author":"Lu","year":"2022","journal-title":"Ann. Surg."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"635","DOI":"10.1097\/MCG.0000000000000817","article-title":"Clinical and histopathologic features of colorectal adenocarcinoma in Crohn\u2019s Disease","volume":"52","author":"Galata","year":"2018","journal-title":"J. Clin. Gastroenterol."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"276","DOI":"10.1111\/his.14922","article-title":"Non-conventional dysplasia is frequently associated with low-grade tubuloglandular and mucinous adenocarcinomas in inflammatory bowel disease","volume":"83","author":"Akarca","year":"2023","journal-title":"Histopathology"},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"1780","DOI":"10.1093\/ibd\/izy057","article-title":"Distinct histopathologic and molecular alterations in Inflammatory Bowel Disease-Associated Intestinal Adenocarcinoma: c-MYC amplification is common and associated with mucinous\/signet ring cell differentiation","volume":"24","author":"Hartman","year":"2018","journal-title":"Inflamm. Bowel Dis."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"13","DOI":"10.1186\/s40880-019-0361-0","article-title":"Mucinous colorectal adenocarcinoma: Clinical pathology and treatment options","volume":"39","author":"Luo","year":"2019","journal-title":"Cancer Commun."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"940","DOI":"10.1093\/ecco-jcc\/jjab217","article-title":"Gastroenteropancreatic Neuroendocrine Neoplasms in patients with Inflammatory Bowel Disease: An ECCO CONFER Multicentre Case Series","volume":"16","author":"Festa","year":"2022","journal-title":"J. Crohns Colitis"},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"9","DOI":"10.1111\/1751-2980.12937","article-title":"Histological scores in inflammatory bowel disease","volume":"22","author":"Neri","year":"2021","journal-title":"J. Dig. Dis."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"1429","DOI":"10.1245\/s10434-007-9757-1","article-title":"Two subtypes of mucinous adenocarcinoma of the colorectum: Clinicopathological and genetic features","volume":"15","author":"Leopoldo","year":"2008","journal-title":"Ann. Surg. Oncol."},{"key":"ref_30","first-page":"1486","article-title":"Clinicopathological and Molecular Specificities of Inflammatory Bowel Disease-Related Colorectal Neoplastic Lesions: The Role of Inflammation","volume":"12","author":"Svrcek","year":"2018","journal-title":"J. Crohns Colitis."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"892","DOI":"10.1016\/j.cgh.2017.11.041","article-title":"High risk of anal and rectal cancer in patients with anal and\/or perianal Crohn\u2019s Disease","volume":"16","author":"Beaugerie","year":"2018","journal-title":"Clin. Gastroenterol. Hepatol."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"78","DOI":"10.1007\/s10350-003-0014-9","article-title":"Incidence and survival of mucinous adenocarcinoma of the colorectum: A population-based study from an Asian country","volume":"47","author":"Du","year":"2004","journal-title":"Dis. Colon Rectum"},{"key":"ref_33","first-page":"1022","article-title":"Mucinous carcinomas of the colon and rectum. An analysis of 62 stage B and C lesions","volume":"115","author":"Connelly","year":"1991","journal-title":"Arch. Pathol. Lab. Med."},{"key":"ref_34","doi-asserted-by":"crossref","unstructured":"Neri, B., Scribano, M.L., Armuzzi, A., Castiglione, F., D\u2019Inc\u00e0, R., Orlando, A., Festa, S., Riegler, G., Fries, W., and Meucci, G. (2022). Incident Colorectal Cancer in Inflammatory Bowel Disease. Cancers, 14.","DOI":"10.3390\/cancers14030721"},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"1891","DOI":"10.1002\/1097-0142(197604)37:4<1891::AID-CNCR2820370439>3.0.CO;2-Z","article-title":"Mucinous carcinoma of the colon and rectum","volume":"37","author":"Symonds","year":"1976","journal-title":"Cancer"},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"1068","DOI":"10.1136\/jcp.41.10.1068","article-title":"Influence of mucinous components on survival in colorectal adenocarcinomas: A multivariate analysis","volume":"41","author":"Halvorsen","year":"1988","journal-title":"J. Clin. Pathol."}],"container-title":["Cancers"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2072-6694\/15\/15\/3803\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T20:19:43Z","timestamp":1760127583000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2072-6694\/15\/15\/3803"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2023,7,26]]},"references-count":36,"journal-issue":{"issue":"15","published-online":{"date-parts":[[2023,8]]}},"alternative-id":["cancers15153803"],"URL":"https:\/\/doi.org\/10.3390\/cancers15153803","relation":{},"ISSN":["2072-6694"],"issn-type":[{"type":"electronic","value":"2072-6694"}],"subject":[],"published":{"date-parts":[[2023,7,26]]}}}