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Article: Usefulness and robustness of Immunoscore for personalized management of cancer patients.

Marliot, Florence / Pagès, Franck / Galon, Jérôme

2020 Volume 9, Issue 1, Page(s) 1832324

Abstract: This review details the analytical performance characteristics of the consensus Immunoscore, measuring the immune response to cancer, improving the estimation of risk of recurrence, and predicting response to treatment for patients with colon cancer. The ...

Abstract	This review details the analytical performance characteristics of the consensus Immunoscore, measuring the immune response to cancer, improving the estimation of risk of recurrence, and predicting response to treatment for patients with colon cancer. The analytical validation of Immunoscore has been documented. Immunoscore is a robust, reproducible, quantitative, and standardized immune assay, with a high prognostic performance, independent of all of the prognostic markers currently used in clinical practice. Immunoscore evaluation within the tumor microenvironment is clinically relevant, and Immunoscore was recently introduced into ESMO Clinical Practice Guidelines for colon cancer and into the WHO classification of the Digestive System Tumors. This paves the way for the use of Immunoscore in clinical practice in colorectal tumors and likely soon in many other solid tumors.
MeSH term(s)	Colonic Neoplasms/diagnosis ; Colorectal Neoplasms ; Humans ; Neoplasm Recurrence, Local ; Prognosis ; Tumor Microenvironment
Language	English
Publishing date	2020-10-13
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't ; Review
ZDB-ID	2645309-5
ISSN	2162-402X ; 2162-4011
ISSN (online)	2162-402X
ISSN	2162-4011
DOI	10.1080/2162402X.2020.1832324
Database	MEDical Literature Analysis and Retrieval System OnLINE

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Article ; Online: Immunoscore assay for the immune classification of solid tumors: Technical aspects, improvements and clinical perspectives.

Marliot, Florence / Lafontaine, Lucie / Galon, Jérôme

Methods in enzymology

2019 Volume 636, Page(s) 109–128

Abstract: The past two decades witnessed the appreciation of the importance of specific tumor-infiltrating immune cells in influencing tumor evolution. The discovery that a favorable immune contexture is linked to a prolonged patients' survival, and more ... ...

Abstract	The past two decades witnessed the appreciation of the importance of specific tumor-infiltrating immune cells in influencing tumor evolution. The discovery that a favorable immune contexture is linked to a prolonged patients' survival, and more specifically that intratumoral cytotoxic T lymphocytes hold powerful prognostic value, provided the foundations for the development of the Immunoscore. Immunoscore is a digital pathology, IHC-based immune assay measuring the densities of CD3
MeSH term(s)	CD8-Positive T-Lymphocytes/pathology ; Humans ; Lymphocytes, Tumor-Infiltrating/pathology ; Neoplasm Staging ; Neoplasms/pathology ; Prognosis
Language	English
Publishing date	2019-10-18
Publishing country	United States
Document type	Journal Article ; Review
ISSN	1557-7988
ISSN (online)	1557-7988
DOI	10.1016/bs.mie.2019.07.018
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Article: Therapeutic Implications of the Immunoscore in Patients with Colorectal Cancer.

El Sissy, Carine / Kirilovsky, Amos / Zeitoun, Guy / Marliot, Florence / Haicheur, Nacilla / Lagorce-Pagès, Christine / Galon, Jérôme / Pagès, Franck

Cancers

2021 Volume 13, Issue 6

Abstract: Four decades were needed to progress from the first demonstration of the independent prognostic value of lymphocytes infiltration in rectal cancers to the first recommendation from the international guidelines for the use of a standardized immune assay, ... ...

Abstract	Four decades were needed to progress from the first demonstration of the independent prognostic value of lymphocytes infiltration in rectal cancers to the first recommendation from the international guidelines for the use of a standardized immune assay, namely the "Immunoscore" (IS), to accurately prognosticate colon cancers beyond the TNM-system. The standardization process included not only the IS conceptualization, development, fine-tuning, and validation by a large international consortium, but also a demonstration of the robustness and reproducibility across the world and testing of international norms and their effects on the IS. This is the first step of a major change of paradigm that now perceives cancer as the result of contradicting driving forces, i.e., the tumor expansion and the immune response, interacting dynamically and influencing the prognosis and the response to therapies. This prompted us to evaluate and evidence the capacity of the tumor immune status, as reflected by the IS, to accurately predict chemotherapy responses in an international, randomized cohort study of colon cancer. Moreover, we developed a derived IS performed on initial diagnostic biopsies (IS
Language	English
Publishing date	2021-03-13
Publishing country	Switzerland
Document type	Journal Article
ZDB-ID	2527080-1
ISSN	2072-6694
ISSN	2072-6694
DOI	10.3390/cancers13061281
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Article: Determination of Interactive States of Immune Checkpoint Regulators in Lung Metastases after Radiofrequency Ablation.

Miles, James / Soubeyran, Isabelle / Marliot, Florence / Pangon, Nicolas / Italiano, Antoine / Bellera, Carine / Ward, Stephen G / Pagès, Franck / Palussière, Jean / Larijani, Banafshé

Cancers

2022 Volume 14, Issue 23

Abstract: Background: Cases of the spontaneous regression of multiple pulmonary metastases, after radiofrequency ablation (RFA), of a single lung metastasis, have been documented to be mediated by the immune system. The interaction of immune checkpoints, e.g., PD- ...

Abstract	Background: Cases of the spontaneous regression of multiple pulmonary metastases, after radiofrequency ablation (RFA), of a single lung metastasis, have been documented to be mediated by the immune system. The interaction of immune checkpoints, e.g., PD-1/PD-L1 and CTLA-4/CD80, may explain this phenomenon. The purpose of this study is to identify and quantify immune mechanisms triggered by RFA of pulmonary metastases originating from colorectal cancer. Methods: We used two-site time-resolved Förster resonance energy transfer as determined by frequency-domain FLIM (iFRET) for the quantification of receptor-ligand interactions. iFRET provides a method by which immune checkpoint interaction states can be quantified in a spatiotemporal manner. The same patient sections were used for assessment of ligand-receptor interaction and intratumoral T-cell labeling. Conclusion: The checkpoint interaction states quantified by iFRET did not correlate with ligand expression. We show that immune checkpoint ligand expression as a predictive biomarker may be unsuitable as it does not confirm checkpoint interactions. In pre-RFA-treated metastases, there was a significant and negative correlation between PD-1/PD-L1 interaction state and intratumoral CD3+ and CD8+ density. The negative correlation of CD8+ and interactive states of PD-1/PD-L1 can be used to assess the state of immune suppression in RFA-treated patients.
Language	English
Publishing date	2022-11-22
Publishing country	Switzerland
Document type	Journal Article
ZDB-ID	2527080-1
ISSN	2072-6694
ISSN	2072-6694
DOI	10.3390/cancers14235738
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Article: Adaptive and Innate Immune Cells in Fetal Human Cytomegalovirus-Infected Brains

Sellier, Yann / Marliot, Florence / Bessières, Bettina / Stirnemann, Julien / Encha-Razavi, Ferechte / Guilleminot, Tiffany / Haicheur, Nacilla / Pages, Franck / Ville, Yves / Leruez-Ville, Marianne

Microorganisms. 2020 Jan. 25, v. 8, no. 2

2020

Abstract: Background: The understanding of the pathogenesis of cytomegalovirus (CMV)-induced fetal brain lesions is limited. We aimed to quantify adaptive and innate immune cells and CMV-infected cells in fetal brains with various degrees of brain damage. Methods: ...

Abstract	Background: The understanding of the pathogenesis of cytomegalovirus (CMV)-induced fetal brain lesions is limited. We aimed to quantify adaptive and innate immune cells and CMV-infected cells in fetal brains with various degrees of brain damage. Methods: In total, 26 archived embedded fetal brains were studied, of which 21 were CMV-infected and classified in severely affected (n = 13) and moderately affected (n = 8), and 5 were uninfected controls. The respective magnitude of infected cells, immune cells (CD8⁺, B cells, plasma cells, NK cells, and macrophages), and expression of immune checkpoint receptors (PD-1/PD-L1 and LAG-3) were measured by immunochemistry and quantified by quantitative imaging analysis. Results: Quantities of CD8⁺, plasma cells, NK cells, macrophages, and HCMV⁺ cells and expression of PD-1/PD-L1 and LAG-3 were significantly higher in severely affected than in moderately affected brains (all p values < 0.05). A strong link between higher number of stained cells for HCMV/CD8 and PD-1 and severity of brain lesions was found by component analysis. Conclusions: The higher expression of CD8, PD-1, and LAG-3 in severely affected brains could reflect immune exhaustion of cerebral T cells. These exhausted T cells could be ineffective in controlling viral multiplication itself, leading to more severe brain lesions. The study of the functionality of brain leucocytes ex vivo is needed to confirm this hypothesis.
Keywords	brain ; brain damage ; humans ; immunochemistry ; macrophages ; pathogenesis
Language	English
Dates of publication	2020-0125
Publishing place	Multidisciplinary Digital Publishing Institute
Document type	Article
ZDB-ID	2720891-6
ISSN	2076-2607
ISSN	2076-2607
DOI	10.3390/microorganisms8020176
Database	NAL-Catalogue (AGRICOLA)

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Article ; Online: Rational bases for the use of the Immunoscore in routine clinical settings as a prognostic and predictive biomarker in cancer patients.

Kirilovsky, Amos / Marliot, Florence / El Sissy, Carine / Haicheur, Nacilla / Galon, Jérôme / Pagès, Franck

International immunology

2016 Volume 28, Issue 8, Page(s) 373–382

Abstract: The American Joint Committee on Cancer/Union Internationale Contre le Cancer (AJCC/UICC) tumor, nodes, metastasis (TNM) classification system based on tumor features is used for prognosis estimation and treatment recommendations in most cancers. However, ...

Abstract	The American Joint Committee on Cancer/Union Internationale Contre le Cancer (AJCC/UICC) tumor, nodes, metastasis (TNM) classification system based on tumor features is used for prognosis estimation and treatment recommendations in most cancers. However, the clinical outcome can vary significantly among patients within the same tumor stage and TNM classification does not predict response to therapy. Therefore, many efforts have been focused on the identification of new markers. Multiple tumor cell-based approaches have been proposed but very few have been translated into the clinic. The recent demonstration of the essential role of the immune system in tumor progression has allowed great advances in the understanding of this complex disease and in the design of novel therapies. The analysis of the immune infiltrate by imaging techniques in large patient cohorts highlighted the prognostic impact of the in situ immune cell infiltrate in tumors. Moreover, the characterization of the immune infiltrates (e.g. type, density, distribution within the tumor, phenotype, activation status) in patients treated with checkpoint-blockade strategies could provide information to predict the disease outcome. In colorectal cancer, we have developed a prognostic score ('Immunoscore') that takes into account the distribution of the density of both CD3(+) lymphocytes and CD8(+) cytotoxic T cells in the tumor core and the invasive margin that could outperform TNM staging. Currently, an international retrospective study is under way to validate the Immunoscore prognostic performance in patients with colon cancer. The use of Immunoscore in clinical practice could improve the patients' prognostic assessment and therapeutic management.
Language	English
Publishing date	2016-08
Publishing country	England
Document type	Journal Article ; Review
ZDB-ID	1013745-2
ISSN	1460-2377 ; 0953-8178
ISSN (online)	1460-2377
ISSN	0953-8178
DOI	10.1093/intimm/dxw021
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Article: Adaptive and Innate Immune Cells in Fetal Human Cytomegalovirus-Infected Brains.

Sellier, Yann / Marliot, Florence / Bessières, Bettina / Stirnemann, Julien / Encha-Razavi, Ferechte / Guilleminot, Tiffany / Haicheur, Nacilla / Pages, Franck / Ville, Yves / Leruez-Ville, Marianne

Microorganisms

2020 Volume 8, Issue 2

Abstract	Background: The understanding of the pathogenesis of cytomegalovirus (CMV)-induced fetal brain lesions is limited. We aimed to quantify adaptive and innate immune cells and CMV-infected cells in fetal brains with various degrees of brain damage. Methods: In total, 26 archived embedded fetal brains were studied, of which 21 were CMV-infected and classified in severely affected ( Results: Quantities of CD8 Conclusions: The higher expression of CD8, PD-1, and LAG-3 in severely affected brains could reflect immune exhaustion of cerebral T cells. These exhausted T cells could be ineffective in controlling viral multiplication itself, leading to more severe brain lesions. The study of the functionality of brain leucocytes ex vivo is needed to confirm this hypothesis.
Language	English
Publishing date	2020-01-25
Publishing country	Switzerland
Document type	Journal Article
ZDB-ID	2720891-6
ISSN	2076-2607
ISSN	2076-2607
DOI	10.3390/microorganisms8020176
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Article ; Online: The "Immunoscore" in rectal cancer: could we search quality beyond quantity of life?

Oncotarget

2022 Volume 13, Page(s) 18–31

Abstract: Because of the function and anatomical environment of the rectum, therapeutic strategies for local advanced rectal cancer (LARC) must deal with two challenging stressors that are a high-risk of local and distal recurrences and a high-risk of poor quality ...

Abstract	Because of the function and anatomical environment of the rectum, therapeutic strategies for local advanced rectal cancer (LARC) must deal with two challenging stressors that are a high-risk of local and distal recurrences and a high-risk of poor quality of life (QoL). Over the last three decades, advances in screening tests, therapies, and combined-modality treatment options and strategies have improved the prognosis of patients with LARC. However, owing to the heterogeneous nature of LARC and genetic status, the patient may not respond to a specific therapy and may be at increased risk of side-effects without the life-prolonging benefit. Indeed, each therapy can cause its own side-effects, which may worsen by a combination of treatments resulting in long-term poor QoL. In LARC, QoL has become even more essential with the increasing incidence of rectal cancer in young individuals. Herein, we analyzed the value of the Immunoscore-Biopsy (performed on tumor biopsy at diagnosis) in predicting outcomes, alone or in association with clinical and imaging data, for each therapy used in LARC.
MeSH term(s)	Chemoradiotherapy/methods ; Humans ; Neoadjuvant Therapy/methods ; Neoplasm Recurrence, Local/pathology ; Prognosis ; Quality of Life ; Rectal Neoplasms/pathology ; Rectum/pathology ; Treatment Outcome
Language	English
Publishing date	2022-01-05
Publishing country	United States
Document type	Journal Article
ZDB-ID	2560162-3
ISSN	1949-2553 ; 1949-2553
ISSN (online)	1949-2553
ISSN	1949-2553
DOI	10.18632/oncotarget.28100
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Article: Multi-Institutional Evaluation of Pathologists' Assessment Compared to Immunoscore.

Willis, Joseph / Anders, Robert A / Torigoe, Toshihiko / Hirohashi, Yoshihiko / Bifulco, Carlo / Zlobec, Inti / Mlecnik, Bernhard / Demaria, Sandra / Choi, Won-Tak / Dundr, Pavel / Tatangelo, Fabiana / Di Mauro, Annabella / Baldin, Pamela / Bindea, Gabriela / Marliot, Florence / Haicheur, Nacilla / Fredriksen, Tessa / Kirilovsky, Amos / Buttard, Bénédicte /

Vasaturo, Angela / Lafontaine, Lucie / Maby, Pauline / El Sissy, Carine / Hijazi, Assia / Majdi, Amine / Lagorce, Christine / Berger, Anne / Van den Eynde, Marc / Pagès, Franck / Lugli, Alessandro / Galon, Jérôme

Cancers

2023 Volume 15, Issue 16

Abstract: Background: The Immunoscore (IS) is a quantitative digital pathology assay that evaluates the immune response in cancer patients. This study reports on the reproducibility of pathologists' visual assessment of CD3+- and CD8+-stained colon tumors, ... ...

Abstract	Background: The Immunoscore (IS) is a quantitative digital pathology assay that evaluates the immune response in cancer patients. This study reports on the reproducibility of pathologists' visual assessment of CD3+- and CD8+-stained colon tumors, compared to IS quantification. Methods: An international group of expert pathologists evaluated 540 images from 270 randomly selected colon cancer (CC) cases. Concordance between pathologists' T-score, corresponding hematoxylin-eosin (H&E) slides, and the digital IS was evaluated for two- and three-category IS. Results: Non-concordant T-scores were reported in more than 92% of cases. Disagreement between semi-quantitative visual assessment of T-score and the reference IS was observed in 91% and 96% of cases before and after training, respectively. Statistical analyses showed that the concordance index between pathologists and the digital IS was weak in two- and three-category IS, respectively. After training, 42% of cases had a change in T-score, but no improvement was observed with a Kappa of 0.465 and 0.374. For the 20% of patients around the cut points, no concordance was observed between pathologists and digital pathology analysis in both two- and three-category IS, before or after training (all Kappa < 0.12). Conclusions: The standardized IS assay outperformed expert pathologists' T-score evaluation in the clinical setting. This study demonstrates that digital pathology, in particular digital IS, represents a novel generation of immune pathology tools for reproducible and quantitative assessment of tumor-infiltrated immune cell subtypes.
Language	English
Publishing date	2023-08-10
Publishing country	Switzerland
Document type	Journal Article
ZDB-ID	2527080-1
ISSN	2072-6694
ISSN	2072-6694
DOI	10.3390/cancers15164045
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Article: Mise au point sur l’Immunoscore et ses potentielles implications cliniques.

El Sissy, Carine / Marliot, Florence / Haicheur, Nacilla / Kirilovsky, Amos / Scripcariu, Dragos / Lagorce-Pagès, Christine / Galon, Jérôme / Pagès, Franck

Annales de pathologie

2017 Volume 37, Issue 1, Page(s) 29–38

Abstract: The role of the immune response at the tumor site is now recognized as crucial in the clinical course of patients with cancer. The importance of the immune cell type, their functional orientation, their density and location within the tumor's regions ( ... ...

Title translation	Focus on the Immunoscore and its potential clinical implications.
Abstract	The role of the immune response at the tumor site is now recognized as crucial in the clinical course of patients with cancer. The importance of the immune cell type, their functional orientation, their density and location within the tumor's regions (tumor/invasion margin) has recently been shown and were grouped together under the term "immune contexture". A strong infiltration by cytotoxic and memory T cells in a Th1-polarized tumor microenvironment appears to have a major prognosis impact. A test called Immunoscore taking into account these various parameters has been suggested to measure in a simple, reproducible and robust manner the intra- and peritumoral immune response. The prognostic value of Immunoscore has recently been validated in colon cancers by a large international retrospective study under the aegis of the Society for Immunotherapy of Cancer (SITC). The Immunoscore could have several potential clinical applications such as prognostic as well as theranostic.
Language	French
Publishing date	2017-02
Publishing country	France
Document type	English Abstract ; Journal Article
ZDB-ID	225720-8
ISSN	0242-6498
ISSN	0242-6498
DOI	10.1016/j.annpat.2016.12.010
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