Towards the introduction of the 'Immunoscore' in the classification of malignant tumours

Jérôme Galon, Bernhard Mlecnik, Gabriela Bindea, Helen K. Angell, Anne Berger, Christine Lagorce, Alessandro Lugli, Inti Zlobec, Arndt Hartmann, Carlo Bifulco, Iris D. Nagtegaal, Richard Palmqvist, Giuseppe V. Masucci, Gerardo Botti, Fabiana Tatangelo, Paolo Delrio, Michele Maio, Luigi Laghi, Fabio Grizzi, Martin Asslaber & 28 others Corrado D'Arrigo, Fernando Vidal-Vanaclocha, Eva Zavadova, Lotfi Chouchane, Pamela S. Ohashi, Sara Hafezi-Bakhtiari, Bradly G. Wouters, Michael Roehrl, Linh Nguyen, Yutaka Kawakami, Shoichi Hazama, Kiyotaka Okuno, Shuji Ogino, Peter Gibbs, Paul Waring, Noriyuki Sato, Toshihiko Torigoe, Kyogo Itoh, Prabhu S. Patel, Shilin N. Shukla, Yili Wang, Scott Kopetz, Frank A. Sinicrope, Viorel Scripcariu, Paolo A. Ascierto, Francesco M. Marincola, Bernard A. Fox, Franck Pagès

Research output: Contribution to journalReview article

527 Citations (Scopus)

Abstract

The American Joint Committee on Cancer/Union Internationale Contre le Cancer (AJCC/UICC) TNM staging system provides the most reliable guidelines for the routine prognostication and treatment of colorectal carcinoma. This traditional tumour staging summarizes data on tumour burden (T), the presence of cancer cells in draining and regional lymph nodes (N) and evidence for distant metastases (M). However, it is now recognized that the clinical outcome can vary significantly among patients within the same stage. The current classification provides limited prognostic information and does not predict response to therapy. Multiple ways to classify cancer and to distinguish different subtypes of colorectal cancer have been proposed, including morphology, cell origin, molecular pathways, mutation status and gene expression-based stratification. These parameters rely on tumour-cell characteristics. Extensive literature has investigated the host immune response against cancer and demonstrated the prognostic impact of the in situ immune cell infiltrate in tumours. A methodology named 'Immunoscore' has been defined to quantify the in situ immune infiltrate. In colorectal cancer, the Immunoscore may add to the significance of the current AJCC/UICC TNM classification, since it has been demonstrated to be a prognostic factor superior to the AJCC/UICC TNM classification. An international consortium has been initiated to validate and promote the Immunoscore in routine clinical settings. The results of this international consortium may result in the implementation of the Immunoscore as a new component for the classification of cancer, designated TNM-I (TNM-Immune).

Original languageEnglish
Pages (from-to)199-209
Number of pages11
JournalJournal of Pathology
Volume232
Issue number2
DOIs
Publication statusPublished - Jan 2014

Fingerprint

Neoplasm Staging
Neoplasms
Colorectal Neoplasms
Tumor Burden
Lymph Nodes
Guidelines
Neoplasm Metastasis
Gene Expression
Mutation
Therapeutics

Keywords

  • classification
  • colon carcinoma
  • colorectal cancer
  • immune response
  • Immunoscore
  • predictive markers
  • prognostic markers
  • T cells
  • tumour microenvironment

ASJC Scopus subject areas

  • Pathology and Forensic Medicine

Cite this

Galon, J., Mlecnik, B., Bindea, G., Angell, H. K., Berger, A., Lagorce, C., ... Pagès, F. (2014). Towards the introduction of the 'Immunoscore' in the classification of malignant tumours. Journal of Pathology, 232(2), 199-209. https://doi.org/10.1002/path.4287

Towards the introduction of the 'Immunoscore' in the classification of malignant tumours. / Galon, Jérôme; Mlecnik, Bernhard; Bindea, Gabriela; Angell, Helen K.; Berger, Anne; Lagorce, Christine; Lugli, Alessandro; Zlobec, Inti; Hartmann, Arndt; Bifulco, Carlo; Nagtegaal, Iris D.; Palmqvist, Richard; Masucci, Giuseppe V.; Botti, Gerardo; Tatangelo, Fabiana; Delrio, Paolo; Maio, Michele; Laghi, Luigi; Grizzi, Fabio; Asslaber, Martin; D'Arrigo, Corrado; Vidal-Vanaclocha, Fernando; Zavadova, Eva; Chouchane, Lotfi; Ohashi, Pamela S.; Hafezi-Bakhtiari, Sara; Wouters, Bradly G.; Roehrl, Michael; Nguyen, Linh; Kawakami, Yutaka; Hazama, Shoichi; Okuno, Kiyotaka; Ogino, Shuji; Gibbs, Peter; Waring, Paul; Sato, Noriyuki; Torigoe, Toshihiko; Itoh, Kyogo; Patel, Prabhu S.; Shukla, Shilin N.; Wang, Yili; Kopetz, Scott; Sinicrope, Frank A.; Scripcariu, Viorel; Ascierto, Paolo A.; Marincola, Francesco M.; Fox, Bernard A.; Pagès, Franck.

In: Journal of Pathology, Vol. 232, No. 2, 01.2014, p. 199-209.

Research output: Contribution to journalReview article

Galon, J, Mlecnik, B, Bindea, G, Angell, HK, Berger, A, Lagorce, C, Lugli, A, Zlobec, I, Hartmann, A, Bifulco, C, Nagtegaal, ID, Palmqvist, R, Masucci, GV, Botti, G, Tatangelo, F, Delrio, P, Maio, M, Laghi, L, Grizzi, F, Asslaber, M, D'Arrigo, C, Vidal-Vanaclocha, F, Zavadova, E, Chouchane, L, Ohashi, PS, Hafezi-Bakhtiari, S, Wouters, BG, Roehrl, M, Nguyen, L, Kawakami, Y, Hazama, S, Okuno, K, Ogino, S, Gibbs, P, Waring, P, Sato, N, Torigoe, T, Itoh, K, Patel, PS, Shukla, SN, Wang, Y, Kopetz, S, Sinicrope, FA, Scripcariu, V, Ascierto, PA, Marincola, FM, Fox, BA & Pagès, F 2014, 'Towards the introduction of the 'Immunoscore' in the classification of malignant tumours', Journal of Pathology, vol. 232, no. 2, pp. 199-209. https://doi.org/10.1002/path.4287
Galon J, Mlecnik B, Bindea G, Angell HK, Berger A, Lagorce C et al. Towards the introduction of the 'Immunoscore' in the classification of malignant tumours. Journal of Pathology. 2014 Jan;232(2):199-209. https://doi.org/10.1002/path.4287
Galon, Jérôme ; Mlecnik, Bernhard ; Bindea, Gabriela ; Angell, Helen K. ; Berger, Anne ; Lagorce, Christine ; Lugli, Alessandro ; Zlobec, Inti ; Hartmann, Arndt ; Bifulco, Carlo ; Nagtegaal, Iris D. ; Palmqvist, Richard ; Masucci, Giuseppe V. ; Botti, Gerardo ; Tatangelo, Fabiana ; Delrio, Paolo ; Maio, Michele ; Laghi, Luigi ; Grizzi, Fabio ; Asslaber, Martin ; D'Arrigo, Corrado ; Vidal-Vanaclocha, Fernando ; Zavadova, Eva ; Chouchane, Lotfi ; Ohashi, Pamela S. ; Hafezi-Bakhtiari, Sara ; Wouters, Bradly G. ; Roehrl, Michael ; Nguyen, Linh ; Kawakami, Yutaka ; Hazama, Shoichi ; Okuno, Kiyotaka ; Ogino, Shuji ; Gibbs, Peter ; Waring, Paul ; Sato, Noriyuki ; Torigoe, Toshihiko ; Itoh, Kyogo ; Patel, Prabhu S. ; Shukla, Shilin N. ; Wang, Yili ; Kopetz, Scott ; Sinicrope, Frank A. ; Scripcariu, Viorel ; Ascierto, Paolo A. ; Marincola, Francesco M. ; Fox, Bernard A. ; Pagès, Franck. / Towards the introduction of the 'Immunoscore' in the classification of malignant tumours. In: Journal of Pathology. 2014 ; Vol. 232, No. 2. pp. 199-209.
@article{22ccbc3f530849b0b96dbb30e3eaa5ff,
title = "Towards the introduction of the 'Immunoscore' in the classification of malignant tumours",
abstract = "The American Joint Committee on Cancer/Union Internationale Contre le Cancer (AJCC/UICC) TNM staging system provides the most reliable guidelines for the routine prognostication and treatment of colorectal carcinoma. This traditional tumour staging summarizes data on tumour burden (T), the presence of cancer cells in draining and regional lymph nodes (N) and evidence for distant metastases (M). However, it is now recognized that the clinical outcome can vary significantly among patients within the same stage. The current classification provides limited prognostic information and does not predict response to therapy. Multiple ways to classify cancer and to distinguish different subtypes of colorectal cancer have been proposed, including morphology, cell origin, molecular pathways, mutation status and gene expression-based stratification. These parameters rely on tumour-cell characteristics. Extensive literature has investigated the host immune response against cancer and demonstrated the prognostic impact of the in situ immune cell infiltrate in tumours. A methodology named 'Immunoscore' has been defined to quantify the in situ immune infiltrate. In colorectal cancer, the Immunoscore may add to the significance of the current AJCC/UICC TNM classification, since it has been demonstrated to be a prognostic factor superior to the AJCC/UICC TNM classification. An international consortium has been initiated to validate and promote the Immunoscore in routine clinical settings. The results of this international consortium may result in the implementation of the Immunoscore as a new component for the classification of cancer, designated TNM-I (TNM-Immune).",
keywords = "classification, colon carcinoma, colorectal cancer, immune response, Immunoscore, predictive markers, prognostic markers, T cells, tumour microenvironment",
author = "J{\'e}r{\^o}me Galon and Bernhard Mlecnik and Gabriela Bindea and Angell, {Helen K.} and Anne Berger and Christine Lagorce and Alessandro Lugli and Inti Zlobec and Arndt Hartmann and Carlo Bifulco and Nagtegaal, {Iris D.} and Richard Palmqvist and Masucci, {Giuseppe V.} and Gerardo Botti and Fabiana Tatangelo and Paolo Delrio and Michele Maio and Luigi Laghi and Fabio Grizzi and Martin Asslaber and Corrado D'Arrigo and Fernando Vidal-Vanaclocha and Eva Zavadova and Lotfi Chouchane and Ohashi, {Pamela S.} and Sara Hafezi-Bakhtiari and Wouters, {Bradly G.} and Michael Roehrl and Linh Nguyen and Yutaka Kawakami and Shoichi Hazama and Kiyotaka Okuno and Shuji Ogino and Peter Gibbs and Paul Waring and Noriyuki Sato and Toshihiko Torigoe and Kyogo Itoh and Patel, {Prabhu S.} and Shukla, {Shilin N.} and Yili Wang and Scott Kopetz and Sinicrope, {Frank A.} and Viorel Scripcariu and Ascierto, {Paolo A.} and Marincola, {Francesco M.} and Fox, {Bernard A.} and Franck Pag{\`e}s",
year = "2014",
month = "1",
doi = "10.1002/path.4287",
language = "English",
volume = "232",
pages = "199--209",
journal = "Journal of Pathology",
issn = "0022-3417",
publisher = "John Wiley and Sons Ltd",
number = "2",

}

TY - JOUR

T1 - Towards the introduction of the 'Immunoscore' in the classification of malignant tumours

AU - Galon, Jérôme

AU - Mlecnik, Bernhard

AU - Bindea, Gabriela

AU - Angell, Helen K.

AU - Berger, Anne

AU - Lagorce, Christine

AU - Lugli, Alessandro

AU - Zlobec, Inti

AU - Hartmann, Arndt

AU - Bifulco, Carlo

AU - Nagtegaal, Iris D.

AU - Palmqvist, Richard

AU - Masucci, Giuseppe V.

AU - Botti, Gerardo

AU - Tatangelo, Fabiana

AU - Delrio, Paolo

AU - Maio, Michele

AU - Laghi, Luigi

AU - Grizzi, Fabio

AU - Asslaber, Martin

AU - D'Arrigo, Corrado

AU - Vidal-Vanaclocha, Fernando

AU - Zavadova, Eva

AU - Chouchane, Lotfi

AU - Ohashi, Pamela S.

AU - Hafezi-Bakhtiari, Sara

AU - Wouters, Bradly G.

AU - Roehrl, Michael

AU - Nguyen, Linh

AU - Kawakami, Yutaka

AU - Hazama, Shoichi

AU - Okuno, Kiyotaka

AU - Ogino, Shuji

AU - Gibbs, Peter

AU - Waring, Paul

AU - Sato, Noriyuki

AU - Torigoe, Toshihiko

AU - Itoh, Kyogo

AU - Patel, Prabhu S.

AU - Shukla, Shilin N.

AU - Wang, Yili

AU - Kopetz, Scott

AU - Sinicrope, Frank A.

AU - Scripcariu, Viorel

AU - Ascierto, Paolo A.

AU - Marincola, Francesco M.

AU - Fox, Bernard A.

AU - Pagès, Franck

PY - 2014/1

Y1 - 2014/1

N2 - The American Joint Committee on Cancer/Union Internationale Contre le Cancer (AJCC/UICC) TNM staging system provides the most reliable guidelines for the routine prognostication and treatment of colorectal carcinoma. This traditional tumour staging summarizes data on tumour burden (T), the presence of cancer cells in draining and regional lymph nodes (N) and evidence for distant metastases (M). However, it is now recognized that the clinical outcome can vary significantly among patients within the same stage. The current classification provides limited prognostic information and does not predict response to therapy. Multiple ways to classify cancer and to distinguish different subtypes of colorectal cancer have been proposed, including morphology, cell origin, molecular pathways, mutation status and gene expression-based stratification. These parameters rely on tumour-cell characteristics. Extensive literature has investigated the host immune response against cancer and demonstrated the prognostic impact of the in situ immune cell infiltrate in tumours. A methodology named 'Immunoscore' has been defined to quantify the in situ immune infiltrate. In colorectal cancer, the Immunoscore may add to the significance of the current AJCC/UICC TNM classification, since it has been demonstrated to be a prognostic factor superior to the AJCC/UICC TNM classification. An international consortium has been initiated to validate and promote the Immunoscore in routine clinical settings. The results of this international consortium may result in the implementation of the Immunoscore as a new component for the classification of cancer, designated TNM-I (TNM-Immune).

AB - The American Joint Committee on Cancer/Union Internationale Contre le Cancer (AJCC/UICC) TNM staging system provides the most reliable guidelines for the routine prognostication and treatment of colorectal carcinoma. This traditional tumour staging summarizes data on tumour burden (T), the presence of cancer cells in draining and regional lymph nodes (N) and evidence for distant metastases (M). However, it is now recognized that the clinical outcome can vary significantly among patients within the same stage. The current classification provides limited prognostic information and does not predict response to therapy. Multiple ways to classify cancer and to distinguish different subtypes of colorectal cancer have been proposed, including morphology, cell origin, molecular pathways, mutation status and gene expression-based stratification. These parameters rely on tumour-cell characteristics. Extensive literature has investigated the host immune response against cancer and demonstrated the prognostic impact of the in situ immune cell infiltrate in tumours. A methodology named 'Immunoscore' has been defined to quantify the in situ immune infiltrate. In colorectal cancer, the Immunoscore may add to the significance of the current AJCC/UICC TNM classification, since it has been demonstrated to be a prognostic factor superior to the AJCC/UICC TNM classification. An international consortium has been initiated to validate and promote the Immunoscore in routine clinical settings. The results of this international consortium may result in the implementation of the Immunoscore as a new component for the classification of cancer, designated TNM-I (TNM-Immune).

KW - classification

KW - colon carcinoma

KW - colorectal cancer

KW - immune response

KW - Immunoscore

KW - predictive markers

KW - prognostic markers

KW - T cells

KW - tumour microenvironment

UR - http://www.scopus.com/inward/record.url?scp=84890280907&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=84890280907&partnerID=8YFLogxK

U2 - 10.1002/path.4287

DO - 10.1002/path.4287

M3 - Review article

VL - 232

SP - 199

EP - 209

JO - Journal of Pathology

JF - Journal of Pathology

SN - 0022-3417

IS - 2

ER -