Literature DB >> 28621322

Reliability of tumor-infiltrating lymphocyte and tertiary lymphoid structure assessment in human breast cancer.

Laurence Buisseret1,2,3, Christine Desmedt2, Soizic Garaud1, Marco Fornili4, Xiaoxiao Wang1,2,3, Gert Van den Eyden5, Alexandre de Wind6, Sebastien Duquenne6, Anais Boisson1, Celine Naveaux1, Francoise Rothé2, Sandrine Rorive7, Christine Decaestecker7, Denis Larsimont6, Martine Piccart-Gebhart3, Elia Biganzoli4, Christos Sotiriou2,3, Karen Willard-Gallo1.   

Abstract

The presence of tumor-infiltrating lymphocytes (TIL), reflecting host immune activity, is frequently correlated with better clinical outcomes, particularly in HER2-positive and triple-negative breast cancer. Recent findings suggest that organization of immune infiltrates in tertiary lymphoid structures also has a beneficial effect on survival. This study investigated inter- and intra-observer variation in TIL assessment using conventional hematoxylin-eosin versus immunohistochemical staining to identify immune cells. Global, intratumoral, and stromal TIL, as well as tertiary lymphoid structures were scored independently by experienced pathologists on full-face tumor sections (n=124). The fidelity of scoring infiltrates in core biopsies compared to surgical specimens, and pathological assessment compared to quantitative digital analysis was also evaluated. The inter-observer concordance correlation coefficient was 0.80 for global, 0.72 for intratumoral, and 0.71 for stromal TIL, while the intra-observer concordance correlation coefficient was 0.90 for global, 0.77 for intratumoral, and 0.89 for stromal TIL using immunohistochemical stains. Correlations were lower with hematoxylin-eosin stains, particularly for intratumoral TIL, while global scores had the highest concordance correlation coefficients. Our study concluded that tertiary lymphoid structures are accurately and consistently scored using immunohistochemical but not hematoxylin-eosin stains. A strong association was observed between TIL in core biopsies and surgical samples (R2=0.74) but this did not extend to tertiary lymphoid structures (R2=0.26). TIL scored by pathologists and digital analysis were correlated but our analysis reveals a constant bias between these methods. These data challenge current criteria for TIL and tertiary lymphoid structure assessment in breast cancer and recommend that how pathologists evaluate immune infiltrates be reexamined for future studies.

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Year:  2017        PMID: 28621322     DOI: 10.1038/modpathol.2017.43

Source DB:  PubMed          Journal:  Mod Pathol        ISSN: 0893-3952            Impact factor:   7.842


  20 in total

1.  Systematic analysis of breast cancer morphology uncovers stromal features associated with survival.

Authors:  Andrew H Beck; Ankur R Sangoi; Samuel Leung; Robert J Marinelli; Torsten O Nielsen; Marc J van de Vijver; Robert B West; Matt van de Rijn; Daphne Koller
Journal:  Sci Transl Med       Date:  2011-11-09       Impact factor: 17.956

2.  Prognostic Significance of Tumor-Infiltrating Lymphocytes and the Tertiary Lymphoid Structures in HER2-Positive Breast Cancer Treated With Adjuvant Trastuzumab.

Authors:  Hee Jin Lee; Joo Young Kim; In Ah Park; In Hye Song; Jong Han Yu; Jin-Hee Ahn; Gyungyub Gong
Journal:  Am J Clin Pathol       Date:  2015-08       Impact factor: 2.493

3.  Tertiary lymphoid structures: prognostic significance and relationship with tumour-infiltrating lymphocytes in triple-negative breast cancer.

Authors:  Hee Jin Lee; In Ah Park; In Hye Song; Su-Jin Shin; Joo Young Kim; Jong Han Yu; Gyungyub Gong
Journal:  J Clin Pathol       Date:  2015-10-16       Impact factor: 3.411

4.  The evaluation of tumor-infiltrating lymphocytes (TILs) in breast cancer: recommendations by an International TILs Working Group 2014.

Authors:  R Salgado; C Denkert; S Demaria; N Sirtaine; F Klauschen; G Pruneri; S Wienert; G Van den Eynden; F L Baehner; F Penault-Llorca; E A Perez; E A Thompson; W F Symmans; A L Richardson; J Brock; C Criscitiello; H Bailey; M Ignatiadis; G Floris; J Sparano; Z Kos; T Nielsen; D L Rimm; K H Allison; J S Reis-Filho; S Loibl; C Sotiriou; G Viale; S Badve; S Adams; K Willard-Gallo; S Loi
Journal:  Ann Oncol       Date:  2014-09-11       Impact factor: 32.976

5.  Statistical methods for assessing agreement between two methods of clinical measurement.

Authors:  J M Bland; D G Altman
Journal:  Lancet       Date:  1986-02-08       Impact factor: 79.321

6.  Interobserver Agreement Between Pathologists Assessing Tumor-Infiltrating Lymphocytes (TILs) in Breast Cancer Using Methodology Proposed by the International TILs Working Group.

Authors:  Shannon K Swisher; Yun Wu; Carlos A Castaneda; Genvieve R Lyons; Fei Yang; Coya Tapia; Xiuhong Wang; Sandro A A Casavilca; Roland Bassett; Miluska Castillo; Aysegul Sahin; Elizabeth A Mittendorf
Journal:  Ann Surg Oncol       Date:  2016-03-10       Impact factor: 5.344

7.  Quantitative image analysis of cellular heterogeneity in breast tumors complements genomic profiling.

Authors:  Yinyin Yuan; Henrik Failmezger; Oscar M Rueda; H Raza Ali; Stefan Gräf; Suet-Feung Chin; Roland F Schwarz; Christina Curtis; Mark J Dunning; Helen Bardwell; Nicola Johnson; Sarah Doyle; Gulisa Turashvili; Elena Provenzano; Sam Aparicio; Carlos Caldas; Florian Markowetz
Journal:  Sci Transl Med       Date:  2012-10-24       Impact factor: 17.956

8.  Tertiary lymphoid structures are associated with higher tumor grade in primary operable breast cancer patients.

Authors:  Stine L Figenschau; Silje Fismen; Kristin A Fenton; Christopher Fenton; Elin S Mortensen
Journal:  BMC Cancer       Date:  2015-03-06       Impact factor: 4.430

9.  Tumor-infiltrating lymphocyte composition, organization and PD-1/ PD-L1 expression are linked in breast cancer.

Authors:  Laurence Buisseret; Soizic Garaud; Alexandre de Wind; Gert Van den Eynden; Anais Boisson; Cinzia Solinas; Chunyan Gu-Trantien; Céline Naveaux; Jean-Nicolas Lodewyckx; Hugues Duvillier; Ligia Craciun; Isabelle Veys; Denis Larsimont; Martine Piccart-Gebhart; John Stagg; Christos Sotiriou; Karen Willard-Gallo
Journal:  Oncoimmunology       Date:  2016-12-14       Impact factor: 8.110

10.  A methodology to ensure and improve accuracy of Ki67 labelling index estimation by automated digital image analysis in breast cancer tissue.

Authors:  Arvydas Laurinavicius; Benoit Plancoulaine; Aida Laurinaviciene; Paulette Herlin; Raimundas Meskauskas; Indra Baltrusaityte; Justinas Besusparis; Darius Dasevicius; Nicolas Elie; Yasir Iqbal; Catherine Bor
Journal:  Breast Cancer Res       Date:  2014       Impact factor: 6.466

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  27 in total

Review 1.  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.

Authors:  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; 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
Journal:  Adv Anat Pathol       Date:  2017-09       Impact factor: 3.875

2.  Tumor-Infiltrating Lymphocytes in Patients Receiving Trastuzumab/Pertuzumab-Based Chemotherapy: A TRYPHAENA Substudy.

Authors:  Michail Ignatiadis; Gert Van den Eynden; Salgado Roberto; Marco Fornili; Yacine Bareche; Christine Desmedt; Françoise Rothé; Marion Maetens; David Venet; Esther Holgado; Virginia McNally; Astrid Kiermaier; Heidi M Savage; Timothy R Wilson; Javier Cortes; Andreas Schneeweiss; Karen Willard-Gallo; Elia Biganzoli; Christos Sotiriou
Journal:  J Natl Cancer Inst       Date:  2019-01-01       Impact factor: 13.506

Review 3.  Significance of evaluating tumor-infiltrating lymphocytes (TILs) and programmed cell death-ligand 1 (PD-L1) expression in breast cancer.

Authors:  Sasagu Kurozumi; Takaaki Fujii; Hiroshi Matsumoto; Kenichi Inoue; Masafumi Kurosumi; Jun Horiguchi; Hiroyuki Kuwano
Journal:  Med Mol Morphol       Date:  2017-09-21       Impact factor: 2.309

Review 4.  The tale of TILs in breast cancer: A report from The International Immuno-Oncology Biomarker Working Group.

Authors:  Khalid El Bairi; Harry R Haynes; Elizabeth Blackley; Susan Fineberg; Jeffrey Shear; Sophia Turner; Juliana Ribeiro de Freitas; Daniel Sur; Luis Claudio Amendola; Masoumeh Gharib; Amine Kallala; Indu Arun; Farid Azmoudeh-Ardalan; Luciana Fujimoto; Luz F Sua; Shi-Wei Liu; Huang-Chun Lien; Pawan Kirtani; Marcelo Balancin; Hicham El Attar; Prerna Guleria; Wenxian Yang; Emad Shash; I-Chun Chen; Veronica Bautista; Jose Fernando Do Prado Moura; Bernardo L Rapoport; Carlos Castaneda; Eunice Spengler; Gabriela Acosta-Haab; Isabel Frahm; Joselyn Sanchez; Miluska Castillo; Najat Bouchmaa; Reena R Md Zin; Ruohong Shui; Timothy Onyuma; Wentao Yang; Zaheed Husain; Karen Willard-Gallo; An Coosemans; Edith A Perez; Elena Provenzano; Paula Gonzalez Ericsson; Eduardo Richardet; Ravi Mehrotra; Sandra Sarancone; Anna Ehinger; David L Rimm; John M S Bartlett; Giuseppe Viale; Carsten Denkert; Akira I Hida; Christos Sotiriou; Sibylle Loibl; Stephen M Hewitt; Sunil Badve; William Fraser Symmans; Rim S Kim; Giancarlo Pruneri; Shom Goel; Prudence A Francis; Gloria Inurrigarro; Rin Yamaguchi; Hernan Garcia-Rivello; Hugo Horlings; Said Afqir; Roberto Salgado; Sylvia Adams; Marleen Kok; Maria Vittoria Dieci; Stefan Michiels; Sandra Demaria; Sherene Loi
Journal:  NPJ Breast Cancer       Date:  2021-12-01

Review 5.  Tertiary lymphoid structures in cancer - considerations for patient prognosis.

Authors:  Luis Munoz-Erazo; Janet L Rhodes; Valentine C Marion; Roslyn A Kemp
Journal:  Cell Mol Immunol       Date:  2020-05-15       Impact factor: 11.530

6.  How the variability between computer-assisted analysis procedures evaluating immune markers can influence patients' outcome prediction.

Authors:  Marylène Lejeune; Benoît Plancoulaine; Nicolas Elie; Ramon Bosch; Laia Fontoura; Izar de Villasante; Anna Korzyńska; Andrea Gras Navarro; Esther Sauras Colón; Carlos López
Journal:  Histochem Cell Biol       Date:  2021-08-12       Impact factor: 4.304

7.  Immune Checkpoint Molecules on Tumor-Infiltrating Lymphocytes and Their Association with Tertiary Lymphoid Structures in Human Breast Cancer.

Authors:  Cinzia Solinas; Soizic Garaud; Pushpamali De Silva; Anaïs Boisson; Gert Van den Eynden; Alexandre de Wind; Paolo Risso; Joel Rodrigues Vitória; François Richard; Edoardo Migliori; Grégory Noël; Hugues Duvillier; Ligia Craciun; Isabelle Veys; Ahmad Awada; Vincent Detours; Denis Larsimont; Martine Piccart-Gebhart; Karen Willard-Gallo
Journal:  Front Immunol       Date:  2017-10-30       Impact factor: 7.561

Review 8.  Microenvironmental regulation of tumour immunity and response to immunotherapy.

Authors:  Mark M Kockx; Mark McCleland; Hartmut Koeppen
Journal:  J Pathol       Date:  2021-05-19       Impact factor: 7.996

9.  Tumor-Infiltrating B Lymphocyte Profiling Identifies IgG-Biased, Clonally Expanded Prognostic Phenotypes in Triple-Negative Breast Cancer.

Authors:  Robert J Harris; Anthony Cheung; Joseph C F Ng; Roman Laddach; Alicia M Chenoweth; Silvia Crescioli; Matthew Fittall; Diana Dominguez-Rodriguez; James Roberts; Dina Levi; Fangfang Liu; Elena Alberts; Jelmar Quist; Aida Santaolalla; Sarah E Pinder; Cheryl Gillett; Niklas Hammar; Sheeba Irshad; Mieke Van Hemelrijck; Deborah K Dunn-Walters; Franca Fraternali; James F Spicer; Katie E Lacy; Sophia Tsoka; Anita Grigoriadis; Andrew N J Tutt; Sophia N Karagiannis
Journal:  Cancer Res       Date:  2021-06-15       Impact factor: 13.312

10.  Immune Infiltration in Invasive Lobular Breast Cancer.

Authors:  Christine Desmedt; Roberto Salgado; Marco Fornili; Giancarlo Pruneri; Gert Van den Eynden; Gabriele Zoppoli; Françoise Rothé; Laurence Buisseret; Soizic Garaud; Karen Willard-Gallo; David Brown; Yacine Bareche; Ghizlane Rouas; Christine Galant; François Bertucci; Sherene Loi; Giuseppe Viale; Angelo Di Leo; Andrew R Green; Ian O Ellis; Emad A Rakha; Denis Larsimont; Elia Biganzoli; Christos Sotiriou
Journal:  J Natl Cancer Inst       Date:  2018-07-01       Impact factor: 13.506

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