{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,27]],"date-time":"2026-10-27T03:20:57Z","timestamp":1793071257229,"version":"4.5.0"},"reference-count":29,"publisher":"Ovid Technologies (Wolters Kluwer Health)","issue":"2","license":[{"start":{"date-parts":[[2024,9,14]],"date-time":"2024-09-14T00:00:00Z","timestamp":1726272000000},"content-version":"unspecified","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by-nc-sa\/4.0"}],"content-domain":{"domain":["lww.com","ovid.com"],"crossmark-restriction":true},"short-container-title":[],"published-print":{"date-parts":[[2025,4]]},"abstract":"<jats:title>ABSTRACT<\/jats:title>\n                  <jats:sec>\n                    <jats:title>Background:<\/jats:title>\n                    <jats:p>Breast cancer is the most common cancer in women, with invasive breast carcinoma of no special type (IBC-NST) accounting for the majority of cases.<\/jats:p>\n                  <\/jats:sec>\n                  <jats:sec>\n                    <jats:title>Aim:<\/jats:title>\n                    <jats:p>This study aimed to evaluate the relationship between tumor budding (TB), which is the earliest histological indicator of tumor spread and represents epithelial\u2013mesenchymal transition, and prognostic factors as well as the effect of TB on survival in patients with IBC-NST, thereby demonstrating its potential prognostic value.<\/jats:p>\n                  <\/jats:sec>\n                  <jats:sec>\n                    <jats:title>Materials and Methods:<\/jats:title>\n                    <jats:p>This study included 278 cases of breast resection diagnosed with IBC-NST from 2014 to 2019. Total tumor buds were counted in 10 high-power fields of a hematoxylin and eosin\u2013stained section with the most infiltrative area at 400\u00d7 magnification. The cutoff value for TB was obtained using receiver operating characteristic analysis for mortality and recurrence risk; this cutoff value was used to classify TB into two categories: low and high grades. The relationship between TB and prognostic factors and the effect of TB on the survival of patients were investigated.<\/jats:p>\n                  <\/jats:sec>\n                  <jats:sec>\n                    <jats:title>Results:<\/jats:title>\n                    <jats:p>This study revealed a statistically significant relationship between high-grade TB and increased tumor size, advanced pathological primary tumor (pT) category, lymph node metastasis, lymphatic invasion, blood vessel invasion, increased recurrence, and mortality as well as reduced overall and disease-free survival.<\/jats:p>\n                  <\/jats:sec>\n                  <jats:sec>\n                    <jats:title>Conclusion:<\/jats:title>\n                    <jats:p>TB in breast carcinomas may have significant predictive value for prognosis. It emerges as a simple, reproducible, and cost-effective histological marker. With the standardization of evaluation criteria, TB may be readily integrated into routine pathological examination, thereby increasing its value in clinical patient management.<\/jats:p>\n                  <\/jats:sec>","DOI":"10.4103\/ijpm.ijpm_300_24","type":"journal-article","created":{"date-parts":[[2024,9,17]],"date-time":"2024-09-17T13:19:47Z","timestamp":1726579187000},"page":"317-323","update-policy":"https:\/\/doi.org\/10.1097\/lww.0000000000001000","source":"Crossref","is-referenced-by-count":2,"title":["Potential predictor of prognosis in breast carcinoma: Tumor budding"],"prefix":"10.4103","volume":"68","author":[{"given":"\u0130nci","family":"Usta","sequence":"first","affiliation":[{"name":"Department of Pathology, Faculty of Medicine, Trakya University, Edirne, Turkey"},{"name":"Department of Pathology, Ad\u0131yaman University Training and Research Hospital, Ad\u0131yaman, Turkey"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"T\u00fclin D.","family":"Yalta","sequence":"additional","affiliation":[{"name":"Department of Pathology, Faculty of Medicine, Trakya University, Edirne, Turkey"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Nuray","family":"Can","sequence":"additional","affiliation":[{"name":"Department of Pathology, Faculty of Medicine, Trakya University, Edirne, Turkey"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Necdet","family":"S\u00fct","sequence":"additional","affiliation":[{"name":"Department of Biostatistics, Faculty of Medicine, Trakya University, Edirne, Turkey"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ebru","family":"Ta\u015ftekin","sequence":"additional","affiliation":[{"name":"Department of Pathology, Faculty of Medicine, Trakya University, Edirne, Turkey"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Fulya \u00d6.","family":"Puyan","sequence":"additional","affiliation":[{"name":"Department of Pathology, Faculty of Medicine, Trakya University, Edirne, Turkey"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ufuk","family":"Usta","sequence":"additional","affiliation":[{"name":"Department of Pathology, Faculty of Medicine, Trakya University, Edirne, Turkey"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ezgi G.","family":"Erdo\u011fan","sequence":"additional","affiliation":[{"name":"Department of Pathology, Faculty of Medicine, Trakya University, Edirne, Turkey"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Elif M.","family":"Demirta\u015f","sequence":"additional","affiliation":[{"name":"Department of Pathology, Faculty of Medicine, Trakya University, Edirne, Turkey"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Merve","family":"Ba\u011f\u0131\u015f","sequence":"additional","affiliation":[{"name":"Department of Pathology, Faculty of Medicine, Trakya University, Edirne, Turkey"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Erkan","family":"\u00d6zcan","sequence":"additional","affiliation":[{"name":"Department of Medical Oncology, Faculty of Medicine, Trakya University, Edirne, Turkey"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"\u0130rfan","family":"\u00c7i\u00e7in","sequence":"additional","affiliation":[{"name":"Department of Medical Oncology, Faculty of Medicine, Trakya University, Edirne, Turkey"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"276","published-online":{"date-parts":[[2024,9,14]]},"reference":[{"key":"R2-20250721","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/bs.pmbts.2017.07.002","article-title":"Breast cancer epidemiology, prevention, and screening","volume":"151","author":"Winters","year":"2017","journal-title":"Prog Mol Biol Transl Sci"},{"key":"R5-20250721","doi-asserted-by":"crossref","first-page":"43","DOI":"10.1615\/CritRevOncog.v18.i1-2.40","article-title":"On the origin of cancer metastasis","volume":"18","author":"Seyfried","year":"2013","journal-title":"Crit Rev Oncog"},{"key":"R6-20250721","doi-asserted-by":"crossref","first-page":"670","DOI":"10.1016\/j.cell.2016.11.037","article-title":"Emerging biological principles of metastasis","volume":"168","author":"Lambert","year":"2017","journal-title":"Cell"},{"key":"R7-20250721","doi-asserted-by":"crossref","first-page":"117","DOI":"10.1007\/s10911-010-9178-9","article-title":"Epithelial-mesenchymal transition in cancer: Parallels between normal development and tumor progression","volume":"15","author":"Micalizzi","year":"2010","journal-title":"J Mammary Gland Biol Neoplasia"},{"key":"R8-20250721","doi-asserted-by":"crossref","first-page":"1438","DOI":"10.1172\/JCI38019","article-title":"Epithelial-mesenchymal transitions: The importance of changing cell state in development and disease","volume":"119","author":"Acloque","year":"2009","journal-title":"J Clin Invest"},{"key":"R9-20250721","doi-asserted-by":"crossref","first-page":"1420","DOI":"10.1172\/JCI39104","article-title":"The basics of epithelial-mesenchymal transition","volume":"119","author":"Kalluri","year":"2009","journal-title":"J Clin Invest"},{"key":"R10-20250721","doi-asserted-by":"crossref","first-page":"651","DOI":"10.18632\/oncotarget.199","article-title":"Epithelial mesenchymal transition and tumor budding in aggressive colorectal cancer: Tumor budding as oncotarget","volume":"1","author":"Zlobec","year":"2010","journal-title":"Oncotarget"},{"key":"R11-20250721","doi-asserted-by":"crossref","first-page":"503","DOI":"10.1007\/s10549-020-05810-3","article-title":"The histopathological and molecular features of breast carcinoma with tumour budding-A systematic review and meta-analysis","volume":"183","author":"Lloyd","year":"2020","journal-title":"Breast Cancer Res Treat"},{"issue":"3","key":"R12-20250721","doi-asserted-by":"crossref","first-page":"497","DOI":"10.15562\/bmj.v5i3.335","article-title":"Tumor budding in breast carcinoma: Relation to E cadherin, MMP 9 expression, and metastasis risk","volume":"5","author":"Sriwidyani","year":"2016","journal-title":"Bali Med J"},{"key":"R13-20250721","doi-asserted-by":"crossref","first-page":"12","DOI":"10.5493\/wjem.v8.i2.12","article-title":"Prognostic role of tumor budding in breast cancer","volume":"8","author":"Voutsadakis","year":"2018","journal-title":"World J Exp Med"},{"key":"R14-20250721","doi-asserted-by":"crossref","first-page":"51","DOI":"10.3390\/jcm5050051","article-title":"Tumor budding: The name is EMT. Partial EMT","volume":"5","author":"Grigore","year":"2016","journal-title":"J Clin Med"},{"key":"R15-20250721","doi-asserted-by":"crossref","first-page":"627","DOI":"10.1007\/BF02238588","article-title":"Prognostic value of tumor \u201cbudding\u201d in patients with colorectal cancer","volume":"36","author":"Hase","year":"1993","journal-title":"Dis Colon Rectum"},{"key":"R16-20250721","doi-asserted-by":"crossref","first-page":"127","DOI":"10.1046\/j.1365-2559.2002.01324.x","article-title":"Tumour \u201cbudding\u201d as an index to estimate the potential of aggressiveness in rectal cancer","volume":"40","author":"Ueno","year":"2002","journal-title":"Histopathology"},{"key":"R17-20250721","doi-asserted-by":"crossref","first-page":"1299","DOI":"10.1038\/modpathol.2017.46","article-title":"Recommendations for reporting tumor budding in colorectal cancer based on the \u0131nternational tumor budding consensus conference (ITBCC) 2016","volume":"30","author":"Lugli","year":"2017","journal-title":"Mod Pathol"},{"key":"R18-20250721","doi-asserted-by":"crossref","first-page":"269","DOI":"10.1016\/j.prp.2013.01.009","article-title":"The prognostic value of tumor budding in invasive breast cancer","volume":"209","author":"Liang","year":"2013","journal-title":"Pathol Res Pract"},{"key":"R19-20250721","doi-asserted-by":"crossref","first-page":"195","DOI":"10.4103\/IJPM.IJPM_151_19","article-title":"Expanding the scope of tumor budding","volume":"62","author":"D'Antonio","year":"2019","journal-title":"Indian J Pathol Microbiol"},{"key":"R20-20250721","doi-asserted-by":"crossref","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":"R21-20250721","doi-asserted-by":"crossref","first-page":"459","DOI":"10.1007\/s00428-021-03059-9","article-title":"Improving tumor budding reporting in colorectal cancer: A Delphi consensus study","volume":"479","author":"Haddad","year":"2021","journal-title":"Virchows Arch"},{"key":"R22-20250721","doi-asserted-by":"crossref","first-page":"45","DOI":"10.1007\/s00292-021-01016-6","article-title":"[Tumor budding in colorectal cancer-information for clinical use and instructions for practical evaluation","volume":"43","author":"M\u00fcller","year":"2022","journal-title":"Pathologe"},{"key":"R23-20250721","doi-asserted-by":"crossref","first-page":"310","DOI":"10.1186\/1477-7819-12-310","article-title":"Prognostic value of poorly differentiated clusters in invasive breast cancer","volume":"12","author":"Sun","year":"2014","journal-title":"World J Surg Oncol"},{"key":"R24-20250721","doi-asserted-by":"crossref","first-page":"363","DOI":"10.1007\/s10549-015-3333-3","article-title":"High tumor budding stratifies breast cancer with metastatic properties","volume":"150","author":"Salhia","year":"2015","journal-title":"Breast Cancer Res Treat"},{"key":"R25-20250721","doi-asserted-by":"crossref","first-page":"1066","DOI":"10.1038\/bjc.2015.287","article-title":"The relationship between tumour budding, the tumour microenvironment and survival in patients with invasive ductal breast cancer","volume":"113","author":"Gujam","year":"2015","journal-title":"Br J Cancer"},{"key":"R26-20250721","doi-asserted-by":"crossref","first-page":"222","DOI":"10.1016\/j.humpath.2017.06.008","article-title":"High tumor budding count is associated with adverse clinicopathologic features and poor prognosis in breast carcinoma","volume":"66","author":"Li","year":"2017","journal-title":"Hum Pathol"},{"key":"R27-20250721","doi-asserted-by":"crossref","first-page":"171","DOI":"10.33545\/pathol.2019.v2.i1c.25","article-title":"PDK. Evaluation of clinicopathologic significance of tumor budding in breast carcinoma","volume":"2","author":"Masilamani","year":"2019","journal-title":"Int J Clin Diagn Pathol"},{"key":"R28-20250721","doi-asserted-by":"crossref","first-page":"222","DOI":"10.4103\/IJPM.IJPM_120_18","article-title":"Tumor budding in infiltrating breast carcinoma: Correlation with known clinicopathological parameters and hormone receptor status","volume":"62","author":"Agarwal","year":"2019","journal-title":"Indian J Pathol Microbiol"},{"key":"R29-20250721","doi-asserted-by":"crossref","first-page":"S117","DOI":"10.4103\/IJPM.IJPM_731_18","article-title":"Tumor budding in invasive breast cancer \u2013An indispensable budding touchstone","volume":"63","author":"Kumarguru","year":"2020","journal-title":"Indian J Pathol Microbiol"},{"key":"R30-20250721","doi-asserted-by":"crossref","first-page":"196","DOI":"10.3390\/biomedicines9020196","article-title":"Joint tumor bud-MMP\/TIMP count at the invasive front improves the prognostic evaluation of invasive breast carcinoma","volume":"9","author":"Gonz\u00e1lez","year":"2021","journal-title":"Biomedicines"},{"key":"R31-20250721","doi-asserted-by":"crossref","first-page":"151792","DOI":"10.1016\/j.anndiagpath.2021.151792","article-title":"Tumor budding is a reliable predictor for death and metastasis in invasive ductal breast cancer and correlates with other prognostic clinicopathological parameters","volume":"54","author":"Okcu","year":"2021","journal-title":"Ann Diagn Pathol"},{"key":"R33-20250721","doi-asserted-by":"crossref","first-page":"818869","DOI":"10.3389\/fonc.2021.818869","article-title":"Breast cancer classification based on tumor budding and stem cell-related signatures facilitate prognosis evaluation","volume":"11","author":"Xiang","year":"2022","journal-title":"Front Oncol"}],"container-title":["Indian Journal of Pathology and Microbiology"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.ovid.com\/10.4103\/ijpm.ijpm_300_24","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2026,8,14]],"date-time":"2026-08-14T16:29:23Z","timestamp":1786724963000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.ovid.com\/10.4103\/ijpm.ijpm_300_24"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2024,9,14]]},"references-count":29,"journal-issue":{"issue":"2","published-print":{"date-parts":[[2025]]}},"URL":"https:\/\/doi.org\/10.4103\/ijpm.ijpm_300_24","relation":{},"ISSN":["0377-4929","0974-5130"],"issn-type":[{"value":"0377-4929","type":"print"},{"value":"0974-5130","type":"electronic"}],"subject":[],"published":{"date-parts":[[2024,9,14]]},"assertion":[{"value":"2024-04-16","name":"received","label":"Received","group":{"name":"publication_history","label":"Publication History"}},{"value":"2024-08-13","name":"accepted","label":"Accepted","group":{"name":"publication_history","label":"Publication History"}}]}}