Evidence map›Paper›PMID 28777142›Full record

ReviewAdvances in anatomic pathology2017

Assessing Tumor-infiltrating Lymphocytes in Solid Tumors: A Practical Review for Pathologists and Proposal for a Standardized Method From the International Immunooncology Biomarkers Working Group: Part 1: Assessing the Host Immune Response, TILs in Invasive Breast Carcinoma and Ductal Carcinoma In Situ, Metastatic Tumor Deposits and Areas for Further Research.

Shona Hendry, Roberto Salgado, Thomas Gevaert, Prudence A Russell, Tom John, Bibhusal Thapa, Michael Christie, Koen van de Vijver, M V Estrada, Paula I Gonzalez-Ericsson and 90 more

2 registry-linked trialsOpen access · greenAbstract readReview
In one paragraph

Review in Advances in anatomic pathology, 2017. The graph could read no effect estimate from its abstract, so it casts no vote on the map. It is linked to 2 registered trials, which are not on this map. Cited by 414 papers, 3 of them syntheses that pooled it.

0numbers the graph read from it
0cells of the map it votes in
414citing papers in PubMed, 3 pooled it
20.3field-weighted citation impact, top 1% of its field
1 · What the graph read from it

What it found

Each row is one number read from the abstract, on the scale the paper reported it, with its interval. Left of the dashed line favours the treatment, right favours the comparator. Under each row is the sentence it came from. New to these charts? A ten-minute tutorial.

The abstract states no effect estimate the extractor could read, or names no intervention and outcome on the map, so this paper lights no cell and moves no belief. It is still indexed, cited and linked below.

2 · The registry

The trial behind it

Trials whose registry record cites this paper, or whose number appears in the abstract. A trial that started after this paper was published is citing it as background, not reporting it.

NCT04403984 unknown statusnot on this map

Investigation of the Prognostic Value of Genomic Alterations or Protein Expression in Patients With Operated Early Breast Cancer of Luminal A or Luminal B Subtypes

TypeobservationalSponsorHellenic Cooperative Oncology GroupRan2013 to 2023Enrolled750ConditionsBreast Cancer
NCT06416436 phase1withdrawnnot on this mapstarted 2024, after this paper: background citation

Immunotherapy in Combination With Ablative Radiosurgery to Ultra-high DoSes (ICARUS): A Phase I Dose-escalation Radiosurgery Study in Metastatic Cancers

TypeinterventionalSponsorUniversity of Kansas Medical CenterRan2024 to 2024Enrolled0ConditionsSolid TumorArmsAtezolizumab, Stereotactic Ablative Radiotherapy (SBRT)
3 · Its place in the literature

Who cites it

414 citing papers in PubMed, 3 syntheses or guidelines pooled it, 706 citations in OpenAlex.

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  11. The relationship of EBER, EGFR, p16, and E-cadherin expressions with epithelial-mesenchymal transition and tumor budding in laryngeal squamous cell carcinoma.European archives of oto-rhino-laryngology : official journal of the European Federation of Oto-Rhino-Laryngological Societies (EUFOS) : affiliated with the German Society for Oto-Rhino-Laryngology - Head and Neck Surgery · 2026
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354 more citing papers are in PubMed but not listed here.

4 · The record

Corrections and comments

PubMed lists nothing against this paper. Absence here is not a guarantee, only a check that was made.

5 · Who and what money

Authors and funding

100 authors at 20 institutions in 18 countries.

Shona HendryDepartments of *Pathology §§§Medical Oncology, Peter MacCallum Cancer Centre, Melbourne †The Sir Peter MacCallum Department of Oncology Departments of **Pathology ∥∥Medicine, University of Melbourne ¶¶Department of Anatomical Pathology, Royal Melbourne Hospital, Parkville #Department of Anatomical Pathology, St Vincent's Hospital Melbourne, Fitzroy ††Department of Medical Oncology, Austin Health ‡‡Olivia Newton-John Cancer Research Institute, Heidelberg §§School of Cancer Medicine, La Trobe University, Bundoora §§§§§Centre for Clinical Research and School of Medicine, The University of Queensland ∥∥∥∥∥Pathology Queensland, Royal Brisbane and Women's Hospital, Brisbane §§§§§§§§§§The Cancer Research Program, Garvan Institute of Medical Research, Darlinghurst ∥∥∥∥∥∥∥∥∥∥Australian Clinical Labs, Bella Vista ‡‡‡‡‡‡‡‡‡‡‡‡Directorate of Surgical Pathology, SA Pathology §§§§§§§§§§§§Discipline of Medicine, Adelaide University, Adelaide, Australia ***********Department of Surgical Oncology, Netherlands Cancer Institute †††††††††††††Department of Pathology ##Divisions of Diagnostic Oncology & Molecular Pathology, Netherlands Cancer Institute-Antoni van Leeuwenhoek, Amsterdam, The Netherlands ###Université Paris-Est ****INSERM, UMR 955 ††††Département de pathologie, APHP, Hôpital Henri-Mondor, Créteil ∥∥∥∥∥∥∥∥∥Service de Biostatistique et d'Epidémiologie, Gustave Roussy, CESP, Inserm U1018, Université-Paris Sud, Université Paris-Saclay ¶¶¶¶¶¶¶¶¶¶INSERM Unit U981, and Department of Medical Oncology, Gustave Roussy, Villejuif ##########Faculté de Médecine, Université Paris Sud, Kremlin-Bicêtre †††††††Department of Surgical Pathology and Biopathology, Jean Perrin Comprehensive Cancer Centre ‡‡‡‡‡‡‡University of Auvergne UMR1240, Clermont-Ferrand, France ‡‡‡‡Department of Medicine, Clinical Division of Oncology §§§§Institute of Neurology, Comprehensive Cancer Centre Vienna, Medical University of Vienna, Vienna ††††††††††††††Institute of Pathology, Medical University of Graz, Austria ∥∥∥∥European Institute of Oncology ¶¶¶¶School of Medicine ######Department of Pathology, Istituto Europeo di Oncologia, University of Milan, Milan ¶¶¶¶¶¶¶¶¶¶¶¶¶Department of Surgery, Oncology and Gastroenterology, University of Padova #############Medical Oncology 2, Veneto Institute of Oncology IOV-IRCCS, Padua, Italy †††††Molecular Oncology Group, Vall d'Hebron Institute of Oncology, Barcelona †††††††††††Pathology Department, IIS-Fundacion Jimenez Diaz, UAM, Madrid, Spain §Department of Pathology and TCRU, GZA ¶¶¶Department of Pathology, GZA Ziekenhuizen, Antwerp ∥Laboratory of Experimental Urology, Department of Development and Regeneration, KU Leuven ‡‡‡‡‡‡‡‡‡‡‡Department of Pathology, University Hospital Leuven, Leuven, Belgium ¶Department of Pathology, AZ Klina, Brasschaat ††††††Department of Pathology, GZA Ziekenhuizen, Sint-Augustinus, Wilrijk ∥∥∥Molecular Immunology Unit ‡‡‡‡‡‡Department of Medical Oncology, Institut Jules Bordet, Université Libre de Bruxelles ‡Breast Cancer Translational Research Laboratory/Breast International Group, Institut Jules Bordet **************European Organisation for Research and Treatment of Cancer (EORTC) Headquarters *******Department of Pathology, Institut Jules Bordet, Université Libre de Bruxelles, Brussels, Belgium §§§§§§§Department of Surgery, Kansai Medical School, Hirakata, Japan #######Severance Biomedical Science Institute and Department of Medical Oncology, Yonsei University College of Medicine, Seoul, South Korea ∥∥∥∥∥∥∥∥Tumor Pathology Department, Maria Sklodowska-Curie Memorial Cancer Center ¶¶¶¶¶¶¶¶Institute of Oncology, Gliwice Branch, Gliwice, Poland ‡‡‡‡‡‡‡‡‡‡‡‡‡‡Pathology and Tissue Analytics, Roche Innovation Centre Munich, Penzberg †††††††††Institute of Pathology, Charité Universitätsmedizin Berlin ‡‡‡‡‡‡‡‡‡VMscope GmbH, Berlin ¶¶¶¶¶¶¶¶¶German Breast Group GmbH, Neu-Isenburg, Germany **********Trev & Joyce Deeley Research Centre, British Columbia Cancer Agency ††††††††††Department of Biochemistry and Microbiology, University of Victoria, Victoria Departments of ‡‡‡‡‡‡‡‡‡‡Medical Genetics #########Pathology and Laboratory Medicine ¶¶¶¶¶¶¶¶¶¶¶Department of Pathology and Laboratory Medicine, Genetic Pathology Evaluation Centre, University of British Columbia, Vancouver, BC ###########Department of Pathology and Laboratory Medicine, University of Ottawa, Ottawa, Canada §§§§§§§§§§§Department of Pathology and Laboratory Medicine, Weill Cornell Medical College, Doha, Qatar ‡‡‡‡‡‡‡‡Department of Pathology and Laboratory Medicine, Rhode Island Hospital and Lifespan Medical Center §§§§§§§§Warren Alpert Medical School of Brown University, Providence ¶¶¶¶¶National Surgical Adjuvant Breast and Bowel Project Operations Center/NRG Oncology, Pittsburgh, PA †††Breast Cancer Research Program, Vanderbilt Ingram Cancer Center, Vanderbilt University Departments of ‡‡‡Pathology, Microbiology and Immunology ########Department of Medicine, Vanderbilt University Medical Centre *********Vanderbilt Ingram Cancer Center, Nashville §§§§§§§§§Department of Pathology, Yale University School of Medicine, New Haven ∥∥∥∥∥∥∥∥∥∥∥Department of Oncology, Montefiore Medical Centre, Albert Einstein College of Medicine ∥∥∥∥∥∥∥Montefiore Medical Center ¶¶¶¶¶¶¶The Albert Einstein College of Medicine, Bronx, NY ********Department of Pathology, Brigham and Women's Hospital #####Cancer Research Institute and Department of Pathology, Beth Israel Deaconess Cancer Center ******Harvard Medical School ¶¶¶¶¶¶¶¶¶¶¶¶Division of Hematology-Oncology, Beth Israel Deaconess Medical Center ††††††††Department of Cancer Biology ‡‡‡‡‡‡‡‡‡‡‡‡‡Dana-Farber Cancer Institute, Boston, MA ∥∥∥∥∥∥∥∥∥∥∥∥∥Department of Medicine, Division of Medical Oncology, University of Colorado Anschutz Medical Campus, Aurora, CO ‡‡‡‡‡Department of Cancer Biology, Mayo Clinic, Jacksonville, FL ∥∥∥∥∥∥Department of Pathology and Laboratory Medicine, Indiana University, Indianapolis, IN ¶¶¶¶¶¶Cancer Immunotherapy Trials Network, Central Laboratory and Program in Immunology, Fred Hutchinson Cancer Research Center, Seattle, WA ††††††††††††Department of Pathology, New York University Langone Medical Centre ############New York University Medical School *************Perlmutter Cancer Center §§§§§§§§§§§§§Pulmonary Pathology, New York University Center for Biospecimen Research and Development, New York University ***************Department of Pathology, Memorial Sloan-Kettering Cancer Center ####Departments of Radiation Oncology and Pathology, Weill Cornell Medicine, New York, NY *****Department of Pathology, University of Texas M.D. Anderson Cancer Center, Houston, TX ∥∥∥∥∥∥∥∥∥∥∥∥Pathology Department, Stanford University Medical Centre, Stanford ∥∥∥∥∥∥∥∥∥∥∥∥∥∥Department of Pathology, Stanford University, Palo Alto ***Department of Pathology, School of Medicine, University of California, San Diego §§§§§§§§§§§§§§Research Pathology, Genentech Inc., South San Francisco, CA *************Laboratory of Pathology, Center for Cancer Research, National Cancer Institute, National Institutes of Health, Bethesda ¶¶¶¶¶¶¶¶¶¶¶¶¶¶Translational Sciences, MedImmune, Gaithersberg, MD §§§§§§Academic Medical Innovation, Novartis Pharmaceuticals Corporation, East Hanover ##############Translational Medicine, Merck & Co. Inc., Kenilworth, NJ.
Roberto Salgado
Thomas Gevaert
Prudence A Russell
Tom John
Bibhusal Thapa
Michael Christie
Koen van de Vijver
M V Estrada
Paula I Gonzalez-Ericsson
Melinda Sanders
Benjamin Solomon
Cinzia Solinas
Gert G G M Van den Eynden
Yves Allory
Matthias Preusser
Johannes Hainfellner
Giancarlo Pruneri
Andrea Vingiani
Sandra Demaria
Fraser Symmans
Paolo Nuciforo
Laura Comerma
E A Thompson
Sunil Lakhani
Seong-Rim Kim
Stuart Schnitt
Cecile Colpaert
Christos Sotiriou
Stefan J Scherer
Michail Ignatiadis
Sunil Badve
Robert H Pierce
Giuseppe Viale
Nicolas Sirtaine
Frederique Penault-Llorca
Tomohagu Sugie
Susan Fineberg
Soonmyung Paik
Ashok Srinivasan
Andrea Richardson
Yihong Wang
Ewa Chmielik
Jane Brock
Douglas B Johnson
Justin Balko
Stephan Wienert
Veerle Bossuyt
Stefan Michiels
Nils Ternes
Nicole Burchardi
Stephen J Luen
Peter Savas
Frederick Klauschen
Peter H Watson
Brad H Nelson
Carmen Criscitiello
Sandra O'Toole
Denis Larsimont
Roland de Wind
Giuseppe Curigliano
Fabrice André
Magali Lacroix-Triki
Mark van de Vijver
Federico Rojo
Giuseppe Floris
Shahinaz Bedri
Joseph Sparano
David Rimm
Torsten Nielsen
Zuzana Kos
Stephen Hewitt
Baljit Singh
Gelareh Farshid
Sibylle Loibl
Kimberly H Allison
Nadine Tung
Sylvia Adams
Karen Willard-Gallo
Hugo M Horlings
Leena Gandhi
Andre Moreira
Fred Hirsch
Maria V Dieci
Maria Urbanowicz
Iva Brcic
Konstanty Korski
Fabien Gaire
Hartmut Koeppen
Amy Lo
Jennifer Giltnane
Marlon C Rebelatto
Keith E Steele
Jiping Zha
Kenneth Emancipator
Jonathan W Juco
Carsten Denkert
Jorge Reis-Filho
Sherene Loi
Stephen B Fox
Peter MacCallum Cancer Centre · AUUniversité Libre de Bruxelles · BECenter of Molecular Immunology (Cuba) · CUCharité - Universitätsmedizin Berlin · DEUniversité Paris-Sud · FRAlbert Einstein College of Medicine · USBC Cancer Agency · CABrigham and Women's Hospital · USEuropean Institute of Oncology · ITGerman Breast group · DEIndiana University School of MedicineInserm · FRMerck & Co., Inc., Rahway, NJ, USA (United States) · USMolecular Oncology (United States) · USNRG Oncology · USRoche (Switzerland) · CHStanford University · USThe Netherlands Cancer Institute · NLVanderbilt University · USYale University · US

Funding

Yale Clinical and Translational Science Award (U Component)UL1TR001863 · NCATS · YALE UNIVERSITY · PI John H. Krystal, LUCILA OHNO-MACHADO · 2016 to 2026
$102.9M
Vanderbilt Clinical Oncology Research Career Development ProgramK12CA090625 · NCI · VANDERBILT UNIVERSITY MEDICAL CENTER · PI Debra L. Friedman, Paula Jill Hurley · 2001 to 2026
$16.9M
Montefiore Academic Community NCORP ProgramUG1CA189859 · NCI · MONTEFIORE MEDICAL CENTER (BRONX, NY) · PI Balazs Halmos, Della Makower · 2014 to 2026
$10.8M
Predicting and profiling long-term survival after immune checkpoint inhibitionK23CA204726 · NCI · VANDERBILT UNIVERSITY MEDICAL CENTER · PI JOHNSON, DOUGLAS B · 2016 to 2020
$756k
NCATS NIH HHS UL1 TR001863NCI NIH HHS K12 CA090625NCI NIH HHS K23 CA204726
6 · The paper itself

Abstract

Assessment of tumor-infiltrating lymphocytes (TILs) in histopathologic specimens can provide important prognostic information in diverse solid tumor types, and may also be of value in predicting response to treatments. However, implementation as a routine clinical biomarker has not yet been achieved. As successful use of immune checkpoint inhibitors and other forms of immunotherapy become a clinical reality, the need for widely applicable, accessible, and reliable immunooncology biomarkers is clear. In part 1 of this review we briefly discuss the host immune response to tumors and different approaches to TIL assessment. We propose a standardized methodology to assess TILs in solid tumors on hematoxylin and eosin sections, in both primary and metastatic settings, based on the International Immuno-Oncology Biomarker Working Group guidelines for TIL assessment in invasive breast carcinoma. A review of the literature regarding the value of TIL assessment in different solid tumor types follows in part 2. The method we propose is reproducible, affordable, easily applied, and has demonstrated prognostic and predictive significance in invasive breast carcinoma. This standardized methodology may be used as a reference against which other methods are compared, and should be evaluated for clinical validity and utility. Standardization of TIL assessment will help to improve consistency and reproducibility in this field, enrich both the quality and quantity of comparable evidence, and help to thoroughly evaluate the utility of TILs assessment in this era of immunotherapy.

Indexed as

AnimalsBiomarkers, TumorBreast NeoplasmsCarcinoma, Intraductal, NoninfiltratingHumansLymphocytes, Tumor-InfiltratingNeoplasms, Second PrimaryPathologistsBiomarkers, Tumor

Identifiers

PMID28777142
PMCPMC5564448
OpenAlexW2766985996

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Registered trials

Read under generation 80e0d062 · epoch 390. Bibliography from PubMed, PubMed Central and OpenAlex; grants from NIH RePORTER; trial links from ClinicalTrials.gov; estimates, votes and beliefs from the OpenQuestion graph.