{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,25]],"date-time":"2026-09-25T15:41:53Z","timestamp":1790350913651,"version":"4.1.0"},"reference-count":31,"publisher":"Oxford University Press (OUP)","issue":"6","license":[{"start":{"date-parts":[[2026,6,10]],"date-time":"2026-06-10T00:00:00Z","timestamp":1781049600000},"content-version":"vor","delay-in-days":9,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"Region Stockholm","award":["500395"],"award-info":[{"award-number":["500395"]}]},{"name":"Region Stockholm","award":["SOS-2896-2501"],"award-info":[{"award-number":["SOS-2896-2501"]}]},{"name":"Oncological Department of S\u00f6dersjukhuset"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"published-print":{"date-parts":[[2026,6,4]]},"abstract":"<jats:title>Abstract<\/jats:title>\n                  <jats:sec>\n                    <jats:title>Objectives<\/jats:title>\n                    <jats:p>Tumor budding is an emerging micromorphologic predictor of recurrence in localized colorectal cancer (CRC). Whether its addition to established CRC recurrence risk factors routinely assessed in clinical practice improves prediction accuracy remains unclear.<\/jats:p>\n                  <\/jats:sec>\n                  <jats:sec>\n                    <jats:title>Methods<\/jats:title>\n                    <jats:p>This study included patients with stage I through III CRC. A detailed micromorphologic assessment was performed for each case according to protocol, using hematoxylin-eosin\u2013stained slides. Clinical characteristics, including treatment and follow-up data, were extracted from patient records. Two logistic regression models were devised to assess recurrence risk, both including established recurrence risk factors chosen a priori. One model also included tumor budding as a dichotomous variable. Receiver operating characteristic curves were used to evaluate and compare the prognostic performance of each model.<\/jats:p>\n                  <\/jats:sec>\n                  <jats:sec>\n                    <jats:title>Results<\/jats:title>\n                    <jats:p>Of the 1083 cases of CRC included in the study, 441 (41%) displayed tumor budding. Tumor budding was more common in right-sided colon cancer, following a right-to-left gradient in the bowel. It occurred more frequently in patients with adverse prognostic factors and in patients presenting with surgical emergencies necessitating emergency resection. Median follow-up time was 4.3\u2009years. Tumor budding was strongly associated with disease recurrence in univariate analysis, but the association was not maintained in multivariate analysis. There was no statistically significant difference between the areas under the curve of the 2 models.<\/jats:p>\n                  <\/jats:sec>\n                  <jats:sec>\n                    <jats:title>Conclusions<\/jats:title>\n                    <jats:p>Tumor budding did not substantially contribute to recurrence risk prediction in this study. Further research exploring the association between tumor budding, established recurrence risk factors, and CRC prognosis is warranted.<\/jats:p>\n                  <\/jats:sec>","DOI":"10.1093\/ajcp\/aqag057","type":"journal-article","created":{"date-parts":[[2026,5,1]],"date-time":"2026-05-01T12:17:09Z","timestamp":1777637829000},"source":"Crossref","is-referenced-by-count":2,"title":["Impact of tumor budding on recurrence risk prediction in stage I-III colorectal cancer: a Swedish cohort study"],"prefix":"10.1093","volume":"165","author":[{"ORCID":"https:\/\/orcid.org\/0009-0009-4558-5325","authenticated-orcid":false,"given":"Shabane","family":"Barot","sequence":"first","affiliation":[{"name":"Department of Clinical Science and Education, Karolinska Institutet , Stockholm,","place":["Sweden"]},{"name":"Department of Oncology, S\u00f6dersjukhuset , Stockholm,","place":["Sweden"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Mikael","family":"Andersson-Franko","sequence":"additional","affiliation":[{"name":"Department of Clinical Science and Education, Karolinska Institutet , Stockholm,","place":["Sweden"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Sam","family":"Ghazi","sequence":"additional","affiliation":[{"name":"Department of Laboratory Medicine, Division of Pathology, Karolinska Institutet , Stockholm,","place":["Sweden"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ulrik","family":"Lindforss","sequence":"additional","affiliation":[{"name":"Department of Molecular Medicine and Surgery, Karolinska Institutet , Stockholm,","place":["Sweden"]},{"name":"Department of Pelvic Cancer, GI Oncology and Colorectal Surgery Unit, Karolinska University Hospital , Stockholm,","place":["Sweden"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Petri","family":"Rantanen","sequence":"additional","affiliation":[{"name":"Department of Molecular Medicine and Surgery, Karolinska Institutet , Stockholm,","place":["Sweden"]},{"name":"Department of Pelvic Cancer, GI Oncology and Colorectal Surgery Unit, Karolinska University Hospital , Stockholm,","place":["Sweden"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Johannes","family":"Blom","sequence":"additional","affiliation":[{"name":"Department of Clinical Science and Education, Karolinska Institutet , Stockholm,","place":["Sweden"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Annika","family":"Lindblom","sequence":"additional","affiliation":[{"name":"Department of Molecular Medicine and Surgery, Karolinska Institutet , Stockholm,","place":["Sweden"]},{"name":"Department of Clinical Genetics and Genomics, Karolinska University Hospital , Stockholm,","place":["Sweden"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Annelie","family":"Liljegren","sequence":"additional","affiliation":[{"name":"Department of Oncology-Pathology, Karolinska Institutet , Stockholm,","place":["Sweden"]}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"286","published-online":{"date-parts":[[2026,6,10]]},"reference":[{"key":"2026061013232600600_aqag057-B1","doi-asserted-by":"publisher","first-page":"338","DOI":"10.1136\/gutjnl-2022-327736","article-title":"Global burden of colorectal cancer in 2020 and 2040: incidence and mortality estimates from GLOBOCAN","volume":"72","author":"Morgan","year":"2023","journal-title":"Gut"},{"key":"2026061013232600600_aqag057-B2","doi-asserted-by":"publisher","first-page":"229","DOI":"10.3322\/caac.21834","article-title":"Global cancer statistics 2022: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries","volume":"74","author":"Bray","year":"2024","journal-title":"CA Cancer J Clin"},{"key":"2026061013232600600_aqag057-B3","doi-asserted-by":"publisher","first-page":"3308","DOI":"10.3390\/cancers12113308","article-title":"Recurrence risk after radical colorectal cancer surgery-less than before, but how high is it?","volume":"12","author":"Osterman","year":"2020","journal-title":"Cancers (Basel)"},{"key":"2026061013232600600_aqag057-B4","doi-asserted-by":"publisher","first-page":"1291","DOI":"10.1016\/j.annonc.2020.06.022","article-title":"Localised colon cancer: ESMO Clinical Practice Guidelines for diagnosis, treatment and follow-up","volume":"31","author":"Argil\u00e9s","year":"2020","journal-title":"Ann Oncol"},{"key":"2026061013232600600_aqag057-B5","doi-asserted-by":"publisher","first-page":"93","DOI":"10.3322\/caac.21388","article-title":"The eighth edition AJCC Cancer Staging Manual: continuing to build a bridge from a population-based to a more \u201cpersonalized\u201d approach to cancer staging","volume":"67","author":"Amin","year":"2017","journal-title":"CA Cancer J Clin"},{"key":"2026061013232600600_aqag057-B6","doi-asserted-by":"publisher","first-page":"3","DOI":"10.1038\/s41698-018-0075-9","article-title":"Cancer prevention and screening: the next step in the era of precision medicine","volume":"3","author":"Loomans-Kropp","year":"2019","journal-title":"NPJ Precis Oncol"},{"key":"2026061013232600600_aqag057-B7","doi-asserted-by":"publisher","first-page":"iv22","DOI":"10.1093\/annonc\/mdx224","article-title":"Rectal cancer: ESMO Clinical Practice Guidelines for diagnosis, treatment and follow-up","volume":"28","author":"Glynne-Jones","year":"2017","journal-title":"Ann Oncol"},{"key":"2026061013232600600_aqag057-B8","doi-asserted-by":"publisher","first-page":"101","DOI":"10.1038\/s41571-020-0422-y","article-title":"Tumour budding in solid cancers","volume":"18","author":"Lugli","year":"2021","journal-title":"Nat Rev Clin Oncol"},{"key":"2026061013232600600_aqag057-B9","doi-asserted-by":"publisher","first-page":"628","DOI":"10.1016\/j.annonc.2022.03.002","article-title":"Tumor budding is an independent prognostic factor in stage III colon cancer patients: a post-hoc analysis of the IDEA-France phase III trial (PRODIGE-GERCOR)","volume":"33","author":"Basile","year":"2022","journal-title":"Ann Oncol"},{"key":"2026061013232600600_aqag057-B10","volume-title":"TNM Classification of Malignant Tumors","author":"Brierley","year":"2016","edition":"8th ed"},{"key":"2026061013232600600_aqag057-B11","volume-title":"Nationellt v\u00e5rdprogram f\u00f6r tjock- och \u00e4ndtarmscancer Stockholm","author":"Sweden RCCi","year":"2025"},{"key":"2026061013232600600_aqag057-B12","doi-asserted-by":"publisher","first-page":"301","DOI":"10.1007\/DCR.0b013e3181c3ed05","article-title":"Tumor budding and survival after potentially curative resection of node-positive colon cancer","volume":"53","author":"Sy","year":"2010","journal-title":"Dis Colon Rectum"},{"key":"2026061013232600600_aqag057-B13","doi-asserted-by":"publisher","first-page":"831","DOI":"10.1038\/bjc.2016.274","article-title":"Systematic review and meta-analysis of the impact of tumour budding in colorectal cancer","volume":"115","author":"Rogers","year":"2016","journal-title":"Br J Cancer"},{"key":"2026061013232600600_aqag057-B14","doi-asserted-by":"publisher","first-page":"1886","DOI":"10.1200\/JCO.18.02059","article-title":"Prospective multicenter study on the prognostic and predictive impact of tumor budding in stage II colon cancer: results from the SACURA trial","volume":"37","author":"Ueno","year":"2019","journal-title":"J Clin Oncol"},{"key":"2026061013232600600_aqag057-B15","doi-asserted-by":"publisher","first-page":"e801","DOI":"10.1097\/DCR.0000000000002345","article-title":"Is high-grade tumor budding an independent prognostic factor in stage II colon cancer?","volume":"66","author":"Kyong Shin","year":"2023","journal-title":"Dis Colon Rectum"},{"key":"2026061013232600600_aqag057-B16","doi-asserted-by":"publisher","first-page":"700","DOI":"10.1038\/s41416-020-0954-z","article-title":"Tumour budding and its clinical implications in gastrointestinal cancers","volume":"123","author":"Zlobec","year":"2020","journal-title":"Br J Cancer"},{"key":"2026061013232600600_aqag057-B17","doi-asserted-by":"publisher","first-page":"367","DOI":"10.1007\/s10552-023-01802-y","article-title":"Combined associations of a healthy lifestyle and body mass index with colorectal cancer recurrence and survival: a cohort study","volume":"35","author":"Barot","year":"2024","journal-title":"Cancer Causes Control"},{"key":"2026061013232600600_aqag057-B18","doi-asserted-by":"publisher","first-page":"1831","DOI":"10.21873\/anticanres.11518","article-title":"Defining new colorectal cancer syndromes in a population-based cohort of the disease","volume":"37","author":"Forsberg","year":"2017","journal-title":"Anticancer Res"},{"key":"2026061013232600600_aqag057-B19","doi-asserted-by":"publisher","first-page":"619","DOI":"10.1007\/s00535-011-0520-9","article-title":"Analysis of colorectal cancer morphology in relation to sex, age, location, and family history","volume":"47","author":"Ghazi","year":"2012","journal-title":"J Gastroenterol"},{"key":"2026061013232600600_aqag057-B20","doi-asserted-by":"publisher","first-page":"2688","DOI":"10.2353\/ajpath.2010.100298","article-title":"Colorectal cancer susceptibility loci in a population-based study: associations with morphological parameters","volume":"177","author":"Ghazi","year":"2010","journal-title":"Am J Pathol"},{"key":"2026061013232600600_aqag057-B21","volume-title":"AJCC Cancer Staging Manual","author":"American Joint Committee on Cancer","year":"1997","edition":"5th ed."},{"key":"2026061013232600600_aqag057-B22","author":"Loughrey","year":"2023"},{"key":"2026061013232600600_aqag057-B23","doi-asserted-by":"publisher","first-page":"2071","DOI":"10.1016\/j.ejca.2005.06.012","article-title":"Cancer staging and survival in colon cancer is dependent on the quality of the pathologists\u2019 specimen examination","volume":"41","author":"Jestin","year":"2005","journal-title":"Eur J Cancer"},{"key":"2026061013232600600_aqag057-B24","doi-asserted-by":"publisher","first-page":"2912","DOI":"10.1200\/JCO.2003.05.062","article-title":"Colon cancer survival is associated with increasing number of lymph nodes analyzed: a secondary survey of intergroup trial INT-0089","volume":"21","author":"Le Voyer","year":"2003","journal-title":"J Clin Oncol"},{"key":"2026061013232600600_aqag057-B25","doi-asserted-by":"publisher","first-page":"41","DOI":"10.1007\/s00384-023-04334-8","article-title":"Comparison of short-term surgical outcomes and long-term survival between emergency and elective surgery for colorectal cancer: a systematic review and meta-analysis","volume":"38","author":"Zhou","year":"2023","journal-title":"Int J Colorectal Dis"},{"key":"2026061013232600600_aqag057-B26","doi-asserted-by":"publisher","first-page":"22","DOI":"10.1186\/s13643-023-02441-9","article-title":"Prognostic impact of tumor budding in rectal cancer after neoadjuvant therapy: a systematic review and meta-analysis","volume":"13","author":"Li","year":"2024","journal-title":"Syst Rev"},{"key":"2026061013232600600_aqag057-B27","doi-asserted-by":"publisher","first-page":"1299","DOI":"10.1038\/modpathol.2017.46","article-title":"Recommendations for reporting tumor budding in colorectal cancer based on the International Tumor Budding Consensus Conference (ITBCC) 2016","volume":"30","author":"Lugli","year":"2017","journal-title":"Mod Pathol"},{"key":"2026061013232600600_aqag057-B28","doi-asserted-by":"publisher","first-page":"151","DOI":"10.1016\/j.ctrv.2014.12.007","article-title":"The role of tumour budding in predicting survival in patients with primary operable colorectal cancer: a systematic review","volume":"41","author":"van Wyk","year":"2015","journal-title":"Cancer Treat Rev"},{"key":"2026061013232600600_aqag057-B29","doi-asserted-by":"publisher","first-page":"1340","DOI":"10.1097\/PAS.0000000000000504","article-title":"Tumor budding in colorectal carcinoma: confirmation of prognostic significance and histologic cutoff in a population-based cohort","volume":"39","author":"Graham","year":"2015","journal-title":"Am J Surg Pathol"},{"key":"2026061013232600600_aqag057-B30","doi-asserted-by":"publisher","first-page":"251","DOI":"10.1097\/PAS.0000000000002166","article-title":"Tumor budding assessment in colorectal carcinoma: normalization revisited","volume":"48","author":"Cyr","year":"2024","journal-title":"Am J Surg Pathol"},{"key":"2026061013232600600_aqag057-B31","doi-asserted-by":"publisher","first-page":"380","DOI":"10.1200\/JCO.2007.14.1291","article-title":"Individualized prediction of colon cancer recurrence using a nomogram","volume":"26","author":"Weiser","year":"2008","journal-title":"J Clin Oncol"}],"container-title":["American Journal of Clinical Pathology"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/academic.oup.com\/ajcp\/article-pdf\/165\/6\/aqag057\/68505503\/aqag057.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"syndication"},{"URL":"https:\/\/academic.oup.com\/ajcp\/article-pdf\/165\/6\/aqag057\/68505503\/aqag057.pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2026,6,10]],"date-time":"2026-06-10T17:23:35Z","timestamp":1781112215000},"score":1,"resource":{"primary":{"URL":"https:\/\/academic.oup.com\/ajcp\/article\/doi\/10.1093\/ajcp\/aqag057\/8705217"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2026,6]]},"references-count":31,"journal-issue":{"issue":"6","published-print":{"date-parts":[[2026,6,4]]}},"URL":"https:\/\/doi.org\/10.1093\/ajcp\/aqag057","relation":{},"ISSN":["0002-9173","1943-7722"],"issn-type":[{"value":"0002-9173","type":"print"},{"value":"1943-7722","type":"electronic"}],"subject":[],"published-other":{"date-parts":[[2026,6]]},"published":{"date-parts":[[2026,6]]},"article-number":"aqag057"}}