Multicenter International Study of the Consensus Immunoscore for the Prediction of Relapse and Survival in Early-Stage Colon Cancer
Background: The prognostic value of Immunoscore was evaluated in Stage II/III colon cancer (CC) patients, but it remains unclear in Stage I/II, and in early-stage subgroups at risk. An international Society for Immunotherapy of Cancer (SITC) study evaluated the pre-defined consensus Immunoscore in t...
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MDPI AG
2023-01-01
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| Online Access: | https://www.mdpi.com/2072-6694/15/2/418 |
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| author | Bernhard Mlecnik Alessandro Lugli Gabriela Bindea Florence Marliot Carlo Bifulco Jiun-Kae Jack Lee Inti Zlobec Tilman T. Rau Martin D. Berger Iris D. Nagtegaal Elisa Vink-Börger Arndt Hartmann Carol I. Geppert Julie Kolwelter Susanne Merkel Robert Grützmann Marc Van den Eynde Anne Jouret-Mourin Alex Kartheuser Daniel Léonard Christophe Remue Julia Wang Prashant Bavi Michael H. A. Roehrl Pamela S. Ohashi Linh T. Nguyen SeongJun Han Heather L. MacGregor Sara Hafezi-Bakhtiari Bradly G. Wouters Giuseppe V. Masucci Emilia K. Andersson Eva Zavadova Michal Vocka Jan Spacek Lubos Petruzelka Bohuslav Konopasek Pavel Dundr Helena Skalova Kristyna Nemejcova Gerardo Botti Fabiana Tatangelo Paolo Delrio Gennaro Ciliberto Michele Maio Luigi Laghi Fabio Grizzi Tessa Fredriksen Bénédicte Buttard Lucie Lafontaine Pauline Maby Amine Majdi Assia Hijazi Carine El Sissy Amos Kirilovsky Anne Berger Christine Lagorce Christopher Paustian Carmen Ballesteros-Merino Jeroen Dijkstra Carlijn van de Water Shannon van Lent-van Vliet Nikki Knijn Ana-Maria Mușină Dragos-Viorel Scripcariu Boryana Popivanova Mingli Xu Tomonobu Fujita Shoichi Hazama Nobuaki Suzuki Hiroaki Nagano Kiyotaka Okuno Toshihiko Torigoe Noriyuki Sato Tomohisa Furuhata Ichiro Takemasa Prabhu Patel Hemangini H. Vora Birva Shah Jayendrakumar B. Patel Kruti N. Rajvik Shashank J. Pandya Shilin N. Shukla Yili Wang Guanjun Zhang Yutaka Kawakami Francesco M. Marincola Paolo A. Ascierto Bernard A. Fox Franck Pagès Jérôme Galon |
| author_facet | Bernhard Mlecnik Alessandro Lugli Gabriela Bindea Florence Marliot Carlo Bifulco Jiun-Kae Jack Lee Inti Zlobec Tilman T. Rau Martin D. Berger Iris D. Nagtegaal Elisa Vink-Börger Arndt Hartmann Carol I. Geppert Julie Kolwelter Susanne Merkel Robert Grützmann Marc Van den Eynde Anne Jouret-Mourin Alex Kartheuser Daniel Léonard Christophe Remue Julia Wang Prashant Bavi Michael H. A. Roehrl Pamela S. Ohashi Linh T. Nguyen SeongJun Han Heather L. MacGregor Sara Hafezi-Bakhtiari Bradly G. Wouters Giuseppe V. Masucci Emilia K. Andersson Eva Zavadova Michal Vocka Jan Spacek Lubos Petruzelka Bohuslav Konopasek Pavel Dundr Helena Skalova Kristyna Nemejcova Gerardo Botti Fabiana Tatangelo Paolo Delrio Gennaro Ciliberto Michele Maio Luigi Laghi Fabio Grizzi Tessa Fredriksen Bénédicte Buttard Lucie Lafontaine Pauline Maby Amine Majdi Assia Hijazi Carine El Sissy Amos Kirilovsky Anne Berger Christine Lagorce Christopher Paustian Carmen Ballesteros-Merino Jeroen Dijkstra Carlijn van de Water Shannon van Lent-van Vliet Nikki Knijn Ana-Maria Mușină Dragos-Viorel Scripcariu Boryana Popivanova Mingli Xu Tomonobu Fujita Shoichi Hazama Nobuaki Suzuki Hiroaki Nagano Kiyotaka Okuno Toshihiko Torigoe Noriyuki Sato Tomohisa Furuhata Ichiro Takemasa Prabhu Patel Hemangini H. Vora Birva Shah Jayendrakumar B. Patel Kruti N. Rajvik Shashank J. Pandya Shilin N. Shukla Yili Wang Guanjun Zhang Yutaka Kawakami Francesco M. Marincola Paolo A. Ascierto Bernard A. Fox Franck Pagès Jérôme Galon |
| author_sort | Bernhard Mlecnik |
| collection | DOAJ |
| description | Background: The prognostic value of Immunoscore was evaluated in Stage II/III colon cancer (CC) patients, but it remains unclear in Stage I/II, and in early-stage subgroups at risk. An international Society for Immunotherapy of Cancer (SITC) study evaluated the pre-defined consensus Immunoscore in tumors from 1885 AJCC/UICC-TNM Stage I/II CC patients from Canada/USA (Cohort 1) and Europe/Asia (Cohort 2). METHODS: Digital-pathology is used to quantify the densities of CD3+ and CD8+ T-lymphocyte in the center of tumor (CT) and the invasive margin (IM). The time to recurrence (TTR) was the primary endpoint. Secondary endpoints were disease-free survival (DFS), overall survival (OS), prognosis in Stage I, Stage II, Stage II-high-risk, and microsatellite-stable (MSS) patients. RESULTS: High-Immunoscore presented with the lowest risk of recurrence in both cohorts. In Stage I/II, recurrence-free rates at 5 years were 78.4% (95%-CI, 74.4–82.6), 88.1% (95%-CI, 85.7–90.4), 93.4% (95%-CI, 91.1–95.8) in low, intermediate and high Immunoscore, respectively (HR (Hi vs. Lo) = 0.27 (95%-CI, 0.18–0.41); <i>p</i> < 0.0001). In Cox multivariable analysis, the association of Immunoscore to outcome was independent (TTR: HR (Hi vs. Lo) = 0.29, (95%-CI, 0.17–0.50); <i>p</i> < 0.0001) of the patient’s gender, T-stage, sidedness, and microsatellite instability-status (MSI). A significant association of Immunoscore with survival was found for Stage II, high-risk Stage II, T4N0 and MSS patients. The Immunoscore also showed significant association with TTR in Stage-I (HR (Hi vs. Lo) = 0.07 (95%-CI, 0.01–0.61); <i>P</i> = 0.016). The Immunoscore had the strongest (69.5%) contribution χ<sup>2</sup> for influencing survival. Patients with a high Immunoscore had prolonged TTR in T4N0 tumors even for patients not receiving chemotherapy, and the Immunoscore remained the only significant parameter in multivariable analysis. CONCLUSION: In early CC, low Immunoscore reliably identifies patients at risk of relapse for whom a more intensive surveillance program or adjuvant treatment should be considered. |
| first_indexed | 2024-03-09T13:17:48Z |
| format | Article |
| id | doaj.art-c23a558bb6574ff7a9c3c43460cfaba0 |
| institution | Directory Open Access Journal |
| issn | 2072-6694 |
| language | English |
| last_indexed | 2024-03-09T13:17:48Z |
| publishDate | 2023-01-01 |
| publisher | MDPI AG |
| record_format | Article |
| series | Cancers |
| spelling | doaj.art-c23a558bb6574ff7a9c3c43460cfaba02023-11-30T21:33:35ZengMDPI AGCancers2072-66942023-01-0115241810.3390/cancers15020418Multicenter International Study of the Consensus Immunoscore for the Prediction of Relapse and Survival in Early-Stage Colon CancerBernhard Mlecnik0Alessandro Lugli1Gabriela Bindea2Florence Marliot3Carlo Bifulco4Jiun-Kae Jack Lee5Inti Zlobec6Tilman T. Rau7Martin D. Berger8Iris D. Nagtegaal9Elisa Vink-Börger10Arndt Hartmann11Carol I. Geppert12Julie Kolwelter13Susanne Merkel14Robert Grützmann15Marc Van den Eynde16Anne Jouret-Mourin17Alex Kartheuser18Daniel Léonard19Christophe Remue20Julia Wang21Prashant Bavi22Michael H. A. Roehrl23Pamela S. Ohashi24Linh T. Nguyen25SeongJun Han26Heather L. MacGregor27Sara Hafezi-Bakhtiari28Bradly G. Wouters29Giuseppe V. Masucci30Emilia K. Andersson31Eva Zavadova32Michal Vocka33Jan Spacek34Lubos Petruzelka35Bohuslav Konopasek36Pavel Dundr37Helena Skalova38Kristyna Nemejcova39Gerardo Botti40Fabiana Tatangelo41Paolo Delrio42Gennaro Ciliberto43Michele Maio44Luigi Laghi45Fabio Grizzi46Tessa Fredriksen47Bénédicte Buttard48Lucie Lafontaine49Pauline Maby50Amine Majdi51Assia Hijazi52Carine El Sissy53Amos Kirilovsky54Anne Berger55Christine Lagorce56Christopher Paustian57Carmen Ballesteros-Merino58Jeroen Dijkstra59Carlijn van de Water60Shannon van Lent-van Vliet61Nikki Knijn62Ana-Maria Mușină63Dragos-Viorel Scripcariu64Boryana Popivanova65Mingli Xu66Tomonobu Fujita67Shoichi Hazama68Nobuaki Suzuki69Hiroaki Nagano70Kiyotaka Okuno71Toshihiko Torigoe72Noriyuki Sato73Tomohisa Furuhata74Ichiro Takemasa75Prabhu Patel76Hemangini H. Vora77Birva Shah78Jayendrakumar B. Patel79Kruti N. Rajvik80Shashank J. Pandya81Shilin N. Shukla82Yili Wang83Guanjun Zhang84Yutaka Kawakami85Francesco M. Marincola86Paolo A. Ascierto87Bernard A. Fox88Franck Pagès89Jérôme Galon90INSERM, Laboratory of Integrative Cancer Immunology, 75006 Paris, FranceInstitute of Pathology, University of Bern, 3008 Bern, SwitzerlandINSERM, Laboratory of Integrative Cancer Immunology, 75006 Paris, FranceINSERM, Laboratory of Integrative Cancer Immunology, 75006 Paris, FranceDepartment of Pathology, Providence Portland Medical Center, Portland, OR 97213, USADepartment of Biostatistics, M.D. Anderson Cancer Center, University of Texas, Houston, TX 77030, USAInstitute of Pathology, University of Bern, 3008 Bern, SwitzerlandInstitute of Pathology, University of Bern, 3008 Bern, SwitzerlandDepartment of Medical Oncology, University Hospital of Bern, 3010 Bern, SwitzerlandPathology Department, Radboud University, 6500 HC Nijmegen, The NetherlandsPathology Department, Radboud University, 6500 HC Nijmegen, The NetherlandsDepartment of Pathology, University Erlangen-Nürnberg, 91054 Erlangen, GermanyDepartment of Pathology, University Erlangen-Nürnberg, 91054 Erlangen, GermanyDepartment of Pathology, University Erlangen-Nürnberg, 91054 Erlangen, GermanyDepartment of Surgery, University Erlangen-Nürnberg, 91054 Erlangen, GermanyDepartment of Surgery, University Erlangen-Nürnberg, 91054 Erlangen, GermanyInstitut Roi Albert II, Department of Medical Oncology, Cliniques Universitaires St-Luc, 1200 Brussels, BelgiumDepartment of Pathology, Cliniques Universitaires St-Luc, 1200 Brussels, BelgiumInstitut Roi Albert II, Department of Digestive Surgery, Cliniques Universitaires St-Luc Université Catholique de Louvain, 1200 Brussels, BelgiumInstitut Roi Albert II, Department of Digestive Surgery, Cliniques Universitaires St-Luc Université Catholique de Louvain, 1200 Brussels, BelgiumInstitut Roi Albert II, Department of Digestive Surgery, Cliniques Universitaires St-Luc Université Catholique de Louvain, 1200 Brussels, BelgiumCurandis, New York, NY 10583, USADepartment of Laboratory Medicine and Pathobiology, University of Toronto, Toronto, ON M5S 1A8, CanadaDepartment of Pathology, Laboratory Medicine Program, University Health Network, 11-E444, Toronto, ON M5G 2C4, CanadaPrincess Margaret Cancer Centre, Toronto, ON M5G 2C1, CanadaPrincess Margaret Cancer Centre, Toronto, ON M5G 2C1, CanadaPrincess Margaret Cancer Centre, Toronto, ON M5G 2C1, CanadaPrincess Margaret Cancer Centre, Toronto, ON M5G 2C1, CanadaDepartment of Pathology, Laboratory Medicine Program, University Health Network, 11-E444, Toronto, ON M5G 2C4, CanadaPrincess Margaret Cancer Centre, Toronto, ON M5G 2C1, CanadaDepartment of Oncology-Pathology, Karolinska Institutet, Karolinska University, 17177 Stockholm, SwedenDepartment of Oncology-Pathology, Karolinska Institutet, Karolinska University, 17177 Stockholm, SwedenDepartment of Oncology, First Faculty of Medicine, General University Hospital in Prague, Charles University, 12808 Prague, Czech RepublicDepartment of Oncology, First Faculty of Medicine, General University Hospital in Prague, Charles University, 12808 Prague, Czech RepublicDepartment of Oncology, First Faculty of Medicine, General University Hospital in Prague, Charles University, 12808 Prague, Czech RepublicDepartment of Oncology, First Faculty of Medicine, General University Hospital in Prague, Charles University, 12808 Prague, Czech RepublicDepartment of Oncology, First Faculty of Medicine, General University Hospital in Prague, Charles University, 12808 Prague, Czech RepublicInstitute of Pathology, First Faculty of Medicine, General University Hospital in Prague, Charles University, 12808 Prague, Czech RepublicInstitute of Pathology, First Faculty of Medicine, General University Hospital in Prague, Charles University, 12808 Prague, Czech RepublicInstitute of Pathology, First Faculty of Medicine, General University Hospital in Prague, Charles University, 12808 Prague, Czech RepublicDepartment of Pathology, Istituto Nazionale Tumori IRCCS Fondazione G. Pascale, 80131 Napoli, ItalyDepartment of Pathology, Istituto Nazionale Tumori IRCCS Fondazione G. Pascale, 80131 Napoli, ItalyColorectal Surgery Department, Instituto Nazionale Tumori IRCCS Fondazione G. Pascale, 80131 Napoli, ItalyIRCCS Istituto Nazionale Tumori “Regina Elena”, 00128 Rome, ItalyCenter for Immuno-Oncology, University Hospital, 53100 Siena, ItalyLaboratory of Molecular Gastroenterology, IRCCS Humanitas Research Hospital, Rozzano, 20090 Milan, ItalyDepartment of Immunology and Inflammation, IRCCS Humanitas Research Hospital, Rozzano, 20090 Milan, ItalyINSERM, Laboratory of Integrative Cancer Immunology, 75006 Paris, FranceINSERM, Laboratory of Integrative Cancer Immunology, 75006 Paris, FranceINSERM, Laboratory of Integrative Cancer Immunology, 75006 Paris, FranceINSERM, Laboratory of Integrative Cancer Immunology, 75006 Paris, FranceINSERM, Laboratory of Integrative Cancer Immunology, 75006 Paris, FranceINSERM, Laboratory of Integrative Cancer Immunology, 75006 Paris, FranceINSERM, Laboratory of Integrative Cancer Immunology, 75006 Paris, FranceINSERM, Laboratory of Integrative Cancer Immunology, 75006 Paris, FranceINSERM, Laboratory of Integrative Cancer Immunology, 75006 Paris, FranceINSERM, Laboratory of Integrative Cancer Immunology, 75006 Paris, FranceDepartment of Molecular Microbiology and Immunology, Oregon Health and Science University, Portland, OR 97239, USADepartment of Molecular Microbiology and Immunology, Oregon Health and Science University, Portland, OR 97239, USAPathology Department, Radboud University, 6500 HC Nijmegen, The NetherlandsPathology Department, Radboud University, 6500 HC Nijmegen, The NetherlandsPathology Department, Radboud University, 6500 HC Nijmegen, The NetherlandsPathology Department, Radboud University, 6500 HC Nijmegen, The NetherlandsDepartment of Surgical Oncology, Regional Institute of Oncology, University of Medicine and Pharmacy “Grigore T. Popa”, 700115 Iaşi, RomaniaDepartment of Surgical Oncology, Regional Institute of Oncology, University of Medicine and Pharmacy “Grigore T. Popa”, 700115 Iaşi, RomaniaDivision of Cellular Signaling, Institute for Advanced Medical Research, School of Medicine, Keio University, Tokyo 160-8582, JapanDivision of Cellular Signaling, Institute for Advanced Medical Research, School of Medicine, Keio University, Tokyo 160-8582, JapanDivision of Cellular Signaling, Institute for Advanced Medical Research, School of Medicine, Keio University, Tokyo 160-8582, JapanDepartment of Translational Research and Developmental Therapeutics against Cancer, Yamaguchi University School of Medicine, Yamaguchi 755-8505, JapanDepartment of Gastroenterological, Breast and Endocrine Surgery, Yamaguchi University Graduate School of Medicine, Yamaguchi 753-8511, JapanDepartment of Gastroenterological, Breast and Endocrine Surgery, Yamaguchi University Graduate School of Medicine, Yamaguchi 753-8511, JapanDepartment of Surgery, School of Medicine, Kindai University, Osaka-sayama 589-0014, JapanDepartment of Pathology, Sapporo Medical University, Sapporo 060-8556, JapanDepartment of Pathology, Sapporo Medical University, Sapporo 060-8556, JapanDepartment of Surgery, Surgical Oncology, and Science, Sapporo Medical University, Sapporo 060-8556, JapanDepartment of Surgery, Surgical Oncology, and Science, Sapporo Medical University, Sapporo 060-8556, JapanThe Gujarat Cancer & Research Institute, Asarwa, Ahmedabad 380016, IndiaThe Gujarat Cancer & Research Institute, Asarwa, Ahmedabad 380016, IndiaThe Gujarat Cancer & Research Institute, Asarwa, Ahmedabad 380016, IndiaThe Gujarat Cancer & Research Institute, Asarwa, Ahmedabad 380016, IndiaThe Gujarat Cancer & Research Institute, Asarwa, Ahmedabad 380016, IndiaThe Gujarat Cancer & Research Institute, Asarwa, Ahmedabad 380016, IndiaThe Gujarat Cancer & Research Institute, Asarwa, Ahmedabad 380016, IndiaInstitute for Cancer Research, School of Basic Medical Science, Xi’an 710061, ChinaInstitute for Cancer Research, School of Basic Medical Science, Xi’an 710061, ChinaDivision of Cellular Signaling, Institute for Advanced Medical Research, School of Medicine, Keio University, Tokyo 160-8582, JapanKite Pharma, Santa Monica, CA 90404, USAMelanoma Cancer Immunotherapy and Innovative Therapies Unit, Istituto Nazionale Tumori IRCCS Fondazione “G. Pascale”, 80131 Napoli, ItalyDepartment of Molecular Microbiology and Immunology, Oregon Health and Science University, Portland, OR 97239, USAINSERM, Laboratory of Integrative Cancer Immunology, 75006 Paris, FranceINSERM, Laboratory of Integrative Cancer Immunology, 75006 Paris, FranceBackground: The prognostic value of Immunoscore was evaluated in Stage II/III colon cancer (CC) patients, but it remains unclear in Stage I/II, and in early-stage subgroups at risk. An international Society for Immunotherapy of Cancer (SITC) study evaluated the pre-defined consensus Immunoscore in tumors from 1885 AJCC/UICC-TNM Stage I/II CC patients from Canada/USA (Cohort 1) and Europe/Asia (Cohort 2). METHODS: Digital-pathology is used to quantify the densities of CD3+ and CD8+ T-lymphocyte in the center of tumor (CT) and the invasive margin (IM). The time to recurrence (TTR) was the primary endpoint. Secondary endpoints were disease-free survival (DFS), overall survival (OS), prognosis in Stage I, Stage II, Stage II-high-risk, and microsatellite-stable (MSS) patients. RESULTS: High-Immunoscore presented with the lowest risk of recurrence in both cohorts. In Stage I/II, recurrence-free rates at 5 years were 78.4% (95%-CI, 74.4–82.6), 88.1% (95%-CI, 85.7–90.4), 93.4% (95%-CI, 91.1–95.8) in low, intermediate and high Immunoscore, respectively (HR (Hi vs. Lo) = 0.27 (95%-CI, 0.18–0.41); <i>p</i> < 0.0001). In Cox multivariable analysis, the association of Immunoscore to outcome was independent (TTR: HR (Hi vs. Lo) = 0.29, (95%-CI, 0.17–0.50); <i>p</i> < 0.0001) of the patient’s gender, T-stage, sidedness, and microsatellite instability-status (MSI). A significant association of Immunoscore with survival was found for Stage II, high-risk Stage II, T4N0 and MSS patients. The Immunoscore also showed significant association with TTR in Stage-I (HR (Hi vs. Lo) = 0.07 (95%-CI, 0.01–0.61); <i>P</i> = 0.016). The Immunoscore had the strongest (69.5%) contribution χ<sup>2</sup> for influencing survival. Patients with a high Immunoscore had prolonged TTR in T4N0 tumors even for patients not receiving chemotherapy, and the Immunoscore remained the only significant parameter in multivariable analysis. CONCLUSION: In early CC, low Immunoscore reliably identifies patients at risk of relapse for whom a more intensive surveillance program or adjuvant treatment should be considered.https://www.mdpi.com/2072-6694/15/2/418Immunoscorecolon cancerprognosispredictive biomarkersearly-stagetumor microenvironment |
| spellingShingle | Bernhard Mlecnik Alessandro Lugli Gabriela Bindea Florence Marliot Carlo Bifulco Jiun-Kae Jack Lee Inti Zlobec Tilman T. Rau Martin D. Berger Iris D. Nagtegaal Elisa Vink-Börger Arndt Hartmann Carol I. Geppert Julie Kolwelter Susanne Merkel Robert Grützmann Marc Van den Eynde Anne Jouret-Mourin Alex Kartheuser Daniel Léonard Christophe Remue Julia Wang Prashant Bavi Michael H. A. Roehrl Pamela S. Ohashi Linh T. Nguyen SeongJun Han Heather L. MacGregor Sara Hafezi-Bakhtiari Bradly G. Wouters Giuseppe V. Masucci Emilia K. Andersson Eva Zavadova Michal Vocka Jan Spacek Lubos Petruzelka Bohuslav Konopasek Pavel Dundr Helena Skalova Kristyna Nemejcova Gerardo Botti Fabiana Tatangelo Paolo Delrio Gennaro Ciliberto Michele Maio Luigi Laghi Fabio Grizzi Tessa Fredriksen Bénédicte Buttard Lucie Lafontaine Pauline Maby Amine Majdi Assia Hijazi Carine El Sissy Amos Kirilovsky Anne Berger Christine Lagorce Christopher Paustian Carmen Ballesteros-Merino Jeroen Dijkstra Carlijn van de Water Shannon van Lent-van Vliet Nikki Knijn Ana-Maria Mușină Dragos-Viorel Scripcariu Boryana Popivanova Mingli Xu Tomonobu Fujita Shoichi Hazama Nobuaki Suzuki Hiroaki Nagano Kiyotaka Okuno Toshihiko Torigoe Noriyuki Sato Tomohisa Furuhata Ichiro Takemasa Prabhu Patel Hemangini H. Vora Birva Shah Jayendrakumar B. Patel Kruti N. Rajvik Shashank J. Pandya Shilin N. Shukla Yili Wang Guanjun Zhang Yutaka Kawakami Francesco M. Marincola Paolo A. Ascierto Bernard A. Fox Franck Pagès Jérôme Galon Multicenter International Study of the Consensus Immunoscore for the Prediction of Relapse and Survival in Early-Stage Colon Cancer Cancers Immunoscore colon cancer prognosis predictive biomarkers early-stage tumor microenvironment |
| title | Multicenter International Study of the Consensus Immunoscore for the Prediction of Relapse and Survival in Early-Stage Colon Cancer |
| title_full | Multicenter International Study of the Consensus Immunoscore for the Prediction of Relapse and Survival in Early-Stage Colon Cancer |
| title_fullStr | Multicenter International Study of the Consensus Immunoscore for the Prediction of Relapse and Survival in Early-Stage Colon Cancer |
| title_full_unstemmed | Multicenter International Study of the Consensus Immunoscore for the Prediction of Relapse and Survival in Early-Stage Colon Cancer |
| title_short | Multicenter International Study of the Consensus Immunoscore for the Prediction of Relapse and Survival in Early-Stage Colon Cancer |
| title_sort | multicenter international study of the consensus immunoscore for the prediction of relapse and survival in early stage colon cancer |
| topic | Immunoscore colon cancer prognosis predictive biomarkers early-stage tumor microenvironment |
| url | https://www.mdpi.com/2072-6694/15/2/418 |
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multicenterinternationalstudyoftheconsensusimmunoscoreforthepredictionofrelapseandsurvivalinearlystagecoloncancer AT christopherpaustian multicenterinternationalstudyoftheconsensusimmunoscoreforthepredictionofrelapseandsurvivalinearlystagecoloncancer AT carmenballesterosmerino multicenterinternationalstudyoftheconsensusimmunoscoreforthepredictionofrelapseandsurvivalinearlystagecoloncancer AT jeroendijkstra multicenterinternationalstudyoftheconsensusimmunoscoreforthepredictionofrelapseandsurvivalinearlystagecoloncancer AT carlijnvandewater multicenterinternationalstudyoftheconsensusimmunoscoreforthepredictionofrelapseandsurvivalinearlystagecoloncancer AT shannonvanlentvanvliet multicenterinternationalstudyoftheconsensusimmunoscoreforthepredictionofrelapseandsurvivalinearlystagecoloncancer AT nikkiknijn multicenterinternationalstudyoftheconsensusimmunoscoreforthepredictionofrelapseandsurvivalinearlystagecoloncancer AT anamariamusina multicenterinternationalstudyoftheconsensusimmunoscoreforthepredictionofrelapseandsurvivalinearlystagecoloncancer AT dragosviorelscripcariu multicenterinternationalstudyoftheconsensusimmunoscoreforthepredictionofrelapseandsurvivalinearlystagecoloncancer AT boryanapopivanova multicenterinternationalstudyoftheconsensusimmunoscoreforthepredictionofrelapseandsurvivalinearlystagecoloncancer AT minglixu multicenterinternationalstudyoftheconsensusimmunoscoreforthepredictionofrelapseandsurvivalinearlystagecoloncancer AT tomonobufujita multicenterinternationalstudyoftheconsensusimmunoscoreforthepredictionofrelapseandsurvivalinearlystagecoloncancer AT shoichihazama multicenterinternationalstudyoftheconsensusimmunoscoreforthepredictionofrelapseandsurvivalinearlystagecoloncancer AT nobuakisuzuki multicenterinternationalstudyoftheconsensusimmunoscoreforthepredictionofrelapseandsurvivalinearlystagecoloncancer AT hiroakinagano multicenterinternationalstudyoftheconsensusimmunoscoreforthepredictionofrelapseandsurvivalinearlystagecoloncancer AT kiyotakaokuno multicenterinternationalstudyoftheconsensusimmunoscoreforthepredictionofrelapseandsurvivalinearlystagecoloncancer AT toshihikotorigoe multicenterinternationalstudyoftheconsensusimmunoscoreforthepredictionofrelapseandsurvivalinearlystagecoloncancer AT noriyukisato multicenterinternationalstudyoftheconsensusimmunoscoreforthepredictionofrelapseandsurvivalinearlystagecoloncancer AT tomohisafuruhata multicenterinternationalstudyoftheconsensusimmunoscoreforthepredictionofrelapseandsurvivalinearlystagecoloncancer AT ichirotakemasa multicenterinternationalstudyoftheconsensusimmunoscoreforthepredictionofrelapseandsurvivalinearlystagecoloncancer AT prabhupatel multicenterinternationalstudyoftheconsensusimmunoscoreforthepredictionofrelapseandsurvivalinearlystagecoloncancer AT hemanginihvora multicenterinternationalstudyoftheconsensusimmunoscoreforthepredictionofrelapseandsurvivalinearlystagecoloncancer AT birvashah multicenterinternationalstudyoftheconsensusimmunoscoreforthepredictionofrelapseandsurvivalinearlystagecoloncancer AT jayendrakumarbpatel multicenterinternationalstudyoftheconsensusimmunoscoreforthepredictionofrelapseandsurvivalinearlystagecoloncancer AT krutinrajvik multicenterinternationalstudyoftheconsensusimmunoscoreforthepredictionofrelapseandsurvivalinearlystagecoloncancer AT shashankjpandya multicenterinternationalstudyoftheconsensusimmunoscoreforthepredictionofrelapseandsurvivalinearlystagecoloncancer AT shilinnshukla multicenterinternationalstudyoftheconsensusimmunoscoreforthepredictionofrelapseandsurvivalinearlystagecoloncancer AT yiliwang multicenterinternationalstudyoftheconsensusimmunoscoreforthepredictionofrelapseandsurvivalinearlystagecoloncancer AT guanjunzhang multicenterinternationalstudyoftheconsensusimmunoscoreforthepredictionofrelapseandsurvivalinearlystagecoloncancer AT yutakakawakami multicenterinternationalstudyoftheconsensusimmunoscoreforthepredictionofrelapseandsurvivalinearlystagecoloncancer AT francescommarincola multicenterinternationalstudyoftheconsensusimmunoscoreforthepredictionofrelapseandsurvivalinearlystagecoloncancer AT paoloaascierto multicenterinternationalstudyoftheconsensusimmunoscoreforthepredictionofrelapseandsurvivalinearlystagecoloncancer AT bernardafox multicenterinternationalstudyoftheconsensusimmunoscoreforthepredictionofrelapseandsurvivalinearlystagecoloncancer AT franckpages multicenterinternationalstudyoftheconsensusimmunoscoreforthepredictionofrelapseandsurvivalinearlystagecoloncancer AT jeromegalon multicenterinternationalstudyoftheconsensusimmunoscoreforthepredictionofrelapseandsurvivalinearlystagecoloncancer |