ArticleEBioMedicine2020
Tumour budding, poorly differentiated clusters, and T-cell response in colorectal cancer.
Erratum issuedOpen access · goldAbstract read
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Article in EBioMedicine, 2020. The graph could read no effect estimate from its abstract, so it casts no vote on the map. An erratum has been issued. Cited by 27 papers.
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27citing papers in PubMed
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Who cites it
27 citing papers in PubMed, 56 citations in OpenAlex.
- Development and internal validation of a prognostic nomogram for cancer-specific survival among elderly unresected colorectal cancer patients receiving chemotherapy: a retrospective SEER database study.Translational cancer research · 2026Article
- Tumor Budding in Colorectal Carcinoma-From Incidental Observation to Prognostic Marker: Lessons Learned from Colorectal Cancer Assessment.Medicina (Kaunas, Lithuania) · 2026Review
- Characterization of Lymphocyte Subsets in Peripheral Blood of Patients with Colorectal Cancer.Journal of gastrointestinal cancer · 2026Article
- Exploratory analysis of tumor budding density in resected synchronous and metachronous colorectal liver metastases.Frontiers in oncology · 2026Article
- The immune microenvironment of colorectal cancer.Nature reviews. Cancer · 2025Review
- Optimizing Prognostic Assessment in High-Risk Head and Neck Squamous Cell Carcinomas: The Impact of Tumor Budding and a Novel Histomorphological Scoring System.Cancer medicine · 2025Article
- Single-cell and spatial omics unravel the spatiotemporal biology of tumour border invasion and haematogenous metastasis.Clinical and translational medicine · 2024Review
- Correlations of pathomorphological parameters between lesions at the invasive front and lymph node metastases in colorectal cancer: a retrospective clinical study.Journal of the Egyptian National Cancer Institute · 2024Article
- Use of Deep Learning to Evaluate Tumor Microenvironmental Features for Prediction of Colon Cancer Recurrence.Cancer research communications · 2024Article
- High KRT17 expression in tumour budding indicates immunologically 'hot' tumour budding and predicts good survival in patients with colorectal cancer.Clinical & translational immunology · 2024Article
- Article
- Bayesian risk prediction model for colorectal cancer mortality through integration of clinicopathologic and genomic data.NPJ precision oncology · 2023Article
- Bone marrow adipocytes induce cancer-associated fibroblasts and immune evasion, enhancing invasion and drug resistance.Cancer science · 2023Article
- Simultaneous analysis of tumor-infiltrating immune cells density, tumor budding status, and presence of lymphoid follicles in CRC tissue.Scientific reports · 2022Article
- Immune cell profiles in the tumor microenvironment of early-onset, intermediate-onset, and later-onset colorectal cancer.Cancer immunology, immunotherapy : CII · 2022Article
- Desmoplastic Reaction, Immune Cell Response, and Prognosis in Colorectal Cancer.Frontiers in immunology · 2022Article
- Coffee Intake of Colorectal Cancer Patients and Prognosis According to Histopathologic Lymphocytic Reaction and T-Cell Infiltrates.Mayo Clinic proceedings · 2022Article
- Novel Criteria for Intratumoral Budding with Prognostic Relevance for Colon Cancer and Its Histological Subtypes.International journal of molecular sciences · 2021Article
- Refining the ITBCC tumor budding scoring system with a "zero-budding" category in colorectal cancer.Virchows Archiv : an international journal of pathology · 2021Article
- Association ofClinical cancer research : an official journal of the American Association for Cancer Research · 2021Article
Corrections and comments
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Authors and funding
26 authors at 6 institutions in 3 countries.
Kenji FujiyoshiProgram in MPE Molecular Pathological Epidemiology, Department of Pathology, Brigham and Women's Hospital, Harvard Medical School, Boston, MA, USA; Department of Surgery, Kurume University, Kurume, Fukuoka, Japan.
Juha P VäyrynenProgram in MPE Molecular Pathological Epidemiology, Department of Pathology, Brigham and Women's Hospital, Harvard Medical School, Boston, MA, USA; Department of Medical Oncology, Dana-Farber Cancer Institute and Harvard Medical School, Boston, Massachusetts, USA; Cancer and Translational Medicine Research Unit, Medical Research Center Oulu, Oulu University Hospital, and University of Oulu, Oulu, Finland.
Jennifer BorowskyProgram in MPE Molecular Pathological Epidemiology, Department of Pathology, Brigham and Women's Hospital, Harvard Medical School, Boston, MA, USA.
David J PapkeDepartment of Pathology, Brigham and Women's Hospital, and Harvard Medical School, Boston, Massachusetts, USA.
Kota ArimaProgram in MPE Molecular Pathological Epidemiology, Department of Pathology, Brigham and Women's Hospital, Harvard Medical School, Boston, MA, USA.
Koichiro HarukiProgram in MPE Molecular Pathological Epidemiology, Department of Pathology, Brigham and Women's Hospital, Harvard Medical School, Boston, MA, USA.
Junko KishikawaProgram in MPE Molecular Pathological Epidemiology, Department of Pathology, Brigham and Women's Hospital, Harvard Medical School, Boston, MA, USA.
Naohiko AkimotoProgram in MPE Molecular Pathological Epidemiology, Department of Pathology, Brigham and Women's Hospital, Harvard Medical School, Boston, MA, USA.
Tomotaka UgaiProgram in MPE Molecular Pathological Epidemiology, Department of Pathology, Brigham and Women's Hospital, Harvard Medical School, Boston, MA, USA.
Mai Chan LauProgram in MPE Molecular Pathological Epidemiology, Department of Pathology, Brigham and Women's Hospital, Harvard Medical School, Boston, MA, USA.
Simeng GuProgram in MPE Molecular Pathological Epidemiology, Department of Pathology, Brigham and Women's Hospital, Harvard Medical School, Boston, MA, USA.
Shanshan ShiProgram in MPE Molecular Pathological Epidemiology, Department of Pathology, Brigham and Women's Hospital, Harvard Medical School, Boston, MA, USA.
Melissa ZhaoProgram in MPE Molecular Pathological Epidemiology, Department of Pathology, Brigham and Women's Hospital, Harvard Medical School, Boston, MA, USA.
Annacarolina Fabiana Lucia Da SilvaProgram in MPE Molecular Pathological Epidemiology, Department of Pathology, Brigham and Women's Hospital, Harvard Medical School, Boston, MA, USA.
Tyler S TwomblyProgram in MPE Molecular Pathological Epidemiology, Department of Pathology, Brigham and Women's Hospital, Harvard Medical School, Boston, MA, USA.
Hongmei NanDepartment of Epidemiology, Richard M. Fairbanks School of Public Health, Indiana University, Indianapolis, Illinois, USA; Indiana University Melvin and Bren Simon Cancer Center, Indianapolis, Illinois, USA.
Jeffrey A MeyerhardtDepartment of Medical Oncology, Dana-Farber Cancer Institute and Harvard Medical School, Boston, Massachusetts, USA.
Mingyang SongClinical and Translational Epidemiology Unit, Massachusetts General Hospital and Harvard Medical School, Boston, Massachusetts, USA; Division of Gastroenterology, Massachusetts General Hospital, Boston, Massachusetts, USA; Department of Nutrition, Harvard T.H. Chan School of Public Health, Boston, Massachusetts, USA.
Xuehong ZhangDepartment of Nutrition, Harvard T.H. Chan School of Public Health, Boston, Massachusetts, USA.
Kana WuDepartment of Nutrition, Harvard T.H. Chan School of Public Health, Boston, Massachusetts, USA; Channing Division of Network Medicine, Department of Medicine, Brigham and Women's Hospital and Harvard Medical School, Boston, Massachusetts, USA; Department of Epidemiology, Harvard T.H. Chan School of Public Health, Boston, Massachusetts, USA.
Andrew T ChanClinical and Translational Epidemiology Unit, Massachusetts General Hospital and Harvard Medical School, Boston, Massachusetts, USA; Division of Gastroenterology, Massachusetts General Hospital, Boston, Massachusetts, USA; Channing Division of Network Medicine, Department of Medicine, Brigham and Women's Hospital and Harvard Medical School, Boston, Massachusetts, USA; Department of Immunology and Infectious Diseases, Harvard T.H. Chan School of Public Health, Boston, MA, USA.
Charles S FuchsYale Cancer Center, New Haven, Connecticut, USA; Department of Medicine, Yale School of Medicine, New Haven, Connecticut, USA; Smilow Cancer Hospital, New Haven, Connecticut, USA.
Jochen K LennerzDepartment of Pathology, Massachusetts General Hospital and Harvard Medical School, Boston, Massachusetts, USA.
Marios GiannakisDepartment of Medical Oncology, Dana-Farber Cancer Institute and Harvard Medical School, Boston, Massachusetts, USA; Broad Institute of MIT and Harvard, Cambridge, Massachusetts, USA; Department of Medicine, Brigham and Women's Hospital and Harvard Medical School, Boston, Massachusetts, USA.
Jonathan A NowakProgram in MPE Molecular Pathological Epidemiology, Department of Pathology, Brigham and Women's Hospital, Harvard Medical School, Boston, MA, USA.
Shuji OginoProgram in MPE Molecular Pathological Epidemiology, Department of Pathology, Brigham and Women's Hospital, Harvard Medical School, Boston, MA, USA; Department of Epidemiology, Harvard T.H. Chan School of Public Health, Boston, Massachusetts, USA; Broad Institute of MIT and Harvard, Cambridge, Massachusetts, USA; Cancer Immunology and Cancer Epidemiology Programs, Dana-Farber Harvard Cancer Center, Boston, Massachusetts, USA. Electronic address: sogino@bwh.harvard.edu.
Brigham and Women's Hospital · USHarvard University · USBroad Institute · USIndiana University Health · USKurume University · JPYale Cancer Center · US
Funding
Statistical MethodsP01CA087969 · NCI · BRIGHAM AND WOMEN'S HOSPITAL · PI ELIASSEN, A. HEATHER, TAMIMI, RULLA M · 2000 to 2019
$77.8MValidity of Diet and Activity Measures in WomenP01CA055075 · NCI · HARVARD UNIVERSITY (SCH OF PUBLIC HLTH) · PI RIMM, ERIC B · 1991 to 2009
$41.8MTissue and Pathology ResourcesP50CA127003 · NCI · DANA-FARBER CANCER INST · PI SHIVDASANI, RAMESH A · 2007 to 2023
$33.2MLong Term Multidisciplinary Study of Cancer in Women: The Nurses Health StudyUM1CA186107 · NCI · BRIGHAM AND WOMEN'S HOSPITAL · PI ELIASSEN, A. HEATHER, STAMPFER, MEIR · 2014 to 2023
$22.3MCancer Epidemiology Cohort in Male Health ProfessionalsU01CA167552 · NCI · HARVARD UNIVERSITY D/B/A HARVARD SCHOOL OF PUBLIC HEALTH · PI Lorelei Mucci, Walter C. Willett · 2017 to 2026
$17.0MCancer Epidemiology Cohort in Male Health ProfessionalsUM1CA167552 · NCI · HARVARD SCHOOL OF PUBLIC HEALTH · PI WILLETT, WALTER C. · 2012 to 2016
$11.5MSpatial Immunopathological Epidemiology of Colorectal Adenoma-Carcinoma SpectrumR01CA248857 · NCI · FRED HUTCHINSON CANCER RESEARCH CENTER · PI Jonathan Andrew Nowak, Shuji Ogino · 2020 to 2026
$6.6MInflammation and Colorectal NeoplasiaR01CA137178 · NCI · MASSACHUSETTS GENERAL HOSPITAL · PI CHAN, ANDREW T · 2009 to 2019
$6.5MAccelerating Transdisciplinary Epidemiology of Colorectal CancerR35CA197735 · NCI · DANA-FARBER CANCER INST · PI OGINO, SHUJI · 2015 to 2021
$6.0MDietary And Lifestyle Determinants Of Colon Cancer Recurrence and SurvivalR01CA118553 · NCI · YALE UNIVERSITY · PI FUCHS, CHARLES S · 2007 to 2019
$4.4MImpact of Celecoxib and Inflammation on Survival in Stage III Colon CancerR01CA169141 · NCI · YALE UNIVERSITY · PI FUCHS, CHARLES S · 2013 to 2018
$3.9MIlluminating the evolutionary history of colorectal cancer metastasis: basic principles and clinical applicationsR37CA225655 · NCI · MASSACHUSETTS GENERAL HOSPITAL · PI NAXEROVA, KAMILA · 2018 to 2024
$3.0MNCI NIH HHS K07 CA188126NCI NIH HHS P01 CA055075NCI NIH HHS P01 CA087969NCI NIH HHS P50 CA127003NCI NIH HHS R01 CA118553NCI NIH HHS R01 CA137178NCI NIH HHS R01 CA151993NCI NIH HHS R01 CA169141NCI NIH HHS R01 CA248857NCI NIH HHS R35 CA197735NCI NIH HHS R37 CA225655NCI NIH HHS U01 CA167552NCI NIH HHS UM1 CA167552NCI NIH HHS UM1 CA186107NIDDK NIH HHS K24 DK098311
Abstract
backgroundTumour budding and poorly differentiated clusters (PDC) represent forms of tumour invasion. We hypothesised that T-cell densities (reflecting adaptive anti-tumour immunity) might be inversely associated with tumour budding and PDC in colorectal carcinoma.
methodsUtilising 915 colon and rectal carcinomas in two U.S.-wide prospective cohort studies, and multiplex immunofluorescence combined with machine learning algorithms, we assessed CD3, CD4, CD8, CD45RO (PTPRC), and FOXP3 co-expression patterns in lymphocytes. Tumour budding and PDC at invasive fronts were quantified by digital pathology and image analysis using the International tumour Budding Consensus Conference criteria. Using covariate data of 4,420 incident colorectal cancer cases, inverse probability weighting (IPW) was integrated with multivariable logistic regression analysis that assessed the association of T-cell subset densities with tumour budding and PDC while adjusting for selection bias due to tissue availability and potential confounders, including microsatellite instability status.
findingsTumour budding counts were inversely associated with density of CD3
interpretationTumour epithelial naïve and memory cytotoxic T cell densities are inversely associated with tumour budding at invasive fronts, suggesting that cytotoxic anti-tumour immunity suppresses tumour microinvasion.
Indexed as
AdultAgedCD3 ComplexCD4 AntigensCD8 AntigensColorectal NeoplasmsFemaleForkhead Transcription FactorsHumansLeukocyte Common AntigensLymphocytes, Tumor-InfiltratingMaleMiddle AgedNeoplasm InvasivenessT-Lymphocyte SubsetsCD3 ComplexCD4 AntigensCD8 AntigensForkhead Transcription FactorsFOXP3 protein, humanLeukocyte Common Antigensadenocarcinomaartificial intelligenceclinical outcomesepithelial mesenchymal transitionhost-tumour interactionmolecular pathological epidemiology
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