Assessing Tumor-Infiltrating Lymphocytes in Solid Tumors: A Practical Review for Pathologists and Proposal for a Standardized Method from the International Immuno-Oncology Biomarkers Working Group: Part 2: TILs in Melanoma, Gastrointestinal Tract Carcinomas, Non-Small Cell Lung Carcinoma and Mesothelioma, Endometrial and Ovarian Carcinomas, Squamous Cell Carcinoma of the Head and Neck, Genitourinary Carcinomas, and Primary Brain Tumors

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 DemariaFraser Symmans, Paolo Nuciforo, Laura Comerma, E Aubrey 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

Research output: Contribution to journalReview article

84 Citations (Scopus)

Abstract

Assessment of the immune response to tumors is growing in importance as the prognostic implications of this response are increasingly recognized, and as immunotherapies are evaluated and implemented in different tumor types. However, many different approaches can be used to assess and describe the immune response, which limits efforts at implementation as a routine clinical biomarker. In part 1 of this review, we have proposed a standardized methodology to assess tumor-infiltrating lymphocytes (TILs) in solid tumors, based on the International Immuno-Oncology Biomarkers Working Group guidelines for invasive breast carcinoma. In part 2 of this review, we discuss the available evidence for the prognostic and predictive value of TILs in common solid tumors, including carcinomas of the lung, gastrointestinal tract, genitourinary system, gynecologic system, and head and neck, as well as primary brain tumors, mesothelioma and melanoma. The particularities and different emphases in TIL assessment in different tumor types are discussed. The standardized methodology we propose can be adapted to different tumor types and may be used as a standard against which other approaches can be compared. Standardization of TIL assessment will help clinicians, researchers and pathologists to conclusively evaluate the utility of this simple biomarker in the current era of immunotherapy.

Original languageEnglish (US)
Pages (from-to)311-335
Number of pages25
JournalAdvances in Anatomic Pathology
Volume24
Issue number6
DOIs
StatePublished - Jan 1 2017

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Tumor-Infiltrating Lymphocytes
Mesothelioma
Endometrial Neoplasms
Non-Small Cell Lung Carcinoma
Brain Neoplasms
Gastrointestinal Tract
Squamous Cell Carcinoma
Melanoma
Biomarkers
Carcinoma
Neoplasms
Immunotherapy
Urogenital System
Pathologists
Carcinoma, squamous cell of head and neck
Neck
Head
Research Personnel
Guidelines
Breast Neoplasms

Keywords

  • biomarkers
  • cancer
  • immunotherapy
  • lymphocytes
  • pathology
  • tumor-infiltrating

ASJC Scopus subject areas

  • Anatomy
  • Pathology and Forensic Medicine

Cite this

Assessing Tumor-Infiltrating Lymphocytes in Solid Tumors : A Practical Review for Pathologists and Proposal for a Standardized Method from the International Immuno-Oncology Biomarkers Working Group: Part 2: TILs in Melanoma, Gastrointestinal Tract Carcinomas, Non-Small Cell Lung Carcinoma and Mesothelioma, Endometrial and Ovarian Carcinomas, Squamous Cell Carcinoma of the Head and Neck, Genitourinary Carcinomas, and Primary Brain Tumors. / Hendry, Shona; Salgado, Roberto; Gevaert, Thomas; Russell, Prudence A.; John, Tom; Thapa, Bibhusal; Christie, Michael; Van De Vijver, Koen; Estrada, M. V.; Gonzalez-Ericsson, Paula I.; Sanders, Melinda; Solomon, Benjamin; Solinas, Cinzia; Van Den Eynden, Gert G.G.M.; Allory, Yves; Preusser, Matthias; Hainfellner, Johannes; Pruneri, Giancarlo; Vingiani, Andrea; Demaria, Sandra; Symmans, Fraser; Nuciforo, Paolo; Comerma, Laura; Thompson, E Aubrey; Lakhani, Sunil; Kim, Seong Rim; Schnitt, Stuart; Colpaert, Cecile; Sotiriou, Christos; Scherer, Stefan J.; Ignatiadis, Michail; Badve, Sunil; Pierce, Robert H.; Viale, Giuseppe; Sirtaine, Nicolas; Penault-Llorca, Frederique; Sugie, Tomohagu; Fineberg, Susan; Paik, Soonmyung; Srinivasan, Ashok; Richardson, Andrea; Wang, Yihong; Chmielik, Ewa; Brock, Jane; Johnson, Douglas B.; Balko, Justin; Wienert, Stephan; Bossuyt, Veerle; Michiels, Stefan; Ternes, Nils; Burchardi, Nicole; Luen, Stephen J.; Savas, Peter; Klauschen, Frederick; Watson, Peter H.; Nelson, Brad H.; Criscitiello, Carmen; O'Toole, Sandra; Larsimont, Denis; De Wind, Roland; Curigliano, Giuseppe; André, Fabrice; Lacroix-Triki, Magali; Van De Vijver, Mark; Rojo, Federico; Floris, Giuseppe; Bedri, Shahinaz; Sparano, Joseph; Rimm, David; Nielsen, Torsten; Kos, Zuzana; Hewitt, Stephen; Singh, Baljit; Farshid, Gelareh; Loibl, Sibylle; Allison, Kimberly H.; Tung, Nadine; Adams, Sylvia; Willard-Gallo, Karen; Horlings, Hugo M.; Gandhi, Leena; Moreira, Andre; Hirsch, Fred; Dieci, Maria V.; Urbanowicz, Maria; Brcic, Iva; Korski, Konstanty; Gaire, Fabien; Koeppen, Hartmut; Lo, Amy; Giltnane, Jennifer; Rebelatto, Marlon C.; Steele, Keith E.; Zha, Jiping; Emancipator, Kenneth; Juco, Jonathan W.; Denkert, Carsten; Reis-Filho, Jorge; Loi, Sherene; Fox, Stephen B.

In: Advances in Anatomic Pathology, Vol. 24, No. 6, 01.01.2017, p. 311-335.

Research output: Contribution to journalReview article

Hendry, S, Salgado, R, Gevaert, T, Russell, PA, John, T, Thapa, B, Christie, M, Van De Vijver, K, Estrada, MV, Gonzalez-Ericsson, PI, Sanders, M, Solomon, B, Solinas, C, Van Den Eynden, GGGM, Allory, Y, Preusser, M, Hainfellner, J, Pruneri, G, Vingiani, A, Demaria, S, Symmans, F, Nuciforo, P, Comerma, L, Thompson, EA, Lakhani, S, Kim, SR, Schnitt, S, Colpaert, C, Sotiriou, C, Scherer, SJ, Ignatiadis, M, Badve, S, Pierce, RH, Viale, G, Sirtaine, N, Penault-Llorca, F, Sugie, T, Fineberg, S, Paik, S, Srinivasan, A, Richardson, A, Wang, Y, Chmielik, E, Brock, J, Johnson, DB, Balko, J, Wienert, S, Bossuyt, V, Michiels, S, Ternes, N, Burchardi, N, Luen, SJ, Savas, P, Klauschen, F, Watson, PH, Nelson, BH, Criscitiello, C, O'Toole, S, Larsimont, D, De Wind, R, Curigliano, G, André, F, Lacroix-Triki, M, Van De Vijver, M, Rojo, F, Floris, G, Bedri, S, Sparano, J, Rimm, D, Nielsen, T, Kos, Z, Hewitt, S, Singh, B, Farshid, G, Loibl, S, Allison, KH, Tung, N, Adams, S, Willard-Gallo, K, Horlings, HM, Gandhi, L, Moreira, A, Hirsch, F, Dieci, MV, Urbanowicz, M, Brcic, I, Korski, K, Gaire, F, Koeppen, H, Lo, A, Giltnane, J, Rebelatto, MC, Steele, KE, Zha, J, Emancipator, K, Juco, JW, Denkert, C, Reis-Filho, J, Loi, S & Fox, SB 2017, 'Assessing Tumor-Infiltrating Lymphocytes in Solid Tumors: A Practical Review for Pathologists and Proposal for a Standardized Method from the International Immuno-Oncology Biomarkers Working Group: Part 2: TILs in Melanoma, Gastrointestinal Tract Carcinomas, Non-Small Cell Lung Carcinoma and Mesothelioma, Endometrial and Ovarian Carcinomas, Squamous Cell Carcinoma of the Head and Neck, Genitourinary Carcinomas, and Primary Brain Tumors', Advances in Anatomic Pathology, vol. 24, no. 6, pp. 311-335. https://doi.org/10.1097/PAP.0000000000000161
Hendry, Shona ; Salgado, Roberto ; Gevaert, Thomas ; Russell, Prudence A. ; John, Tom ; Thapa, Bibhusal ; Christie, Michael ; Van De Vijver, Koen ; Estrada, M. V. ; Gonzalez-Ericsson, Paula I. ; Sanders, Melinda ; Solomon, Benjamin ; Solinas, Cinzia ; Van Den Eynden, Gert G.G.M. ; Allory, Yves ; Preusser, Matthias ; Hainfellner, Johannes ; Pruneri, Giancarlo ; Vingiani, Andrea ; Demaria, Sandra ; Symmans, Fraser ; Nuciforo, Paolo ; Comerma, Laura ; Thompson, E Aubrey ; Lakhani, Sunil ; Kim, Seong Rim ; Schnitt, Stuart ; Colpaert, Cecile ; Sotiriou, Christos ; Scherer, Stefan J. ; Ignatiadis, Michail ; Badve, Sunil ; Pierce, Robert H. ; Viale, Giuseppe ; Sirtaine, Nicolas ; Penault-Llorca, Frederique ; Sugie, Tomohagu ; Fineberg, Susan ; Paik, Soonmyung ; Srinivasan, Ashok ; Richardson, Andrea ; Wang, Yihong ; Chmielik, Ewa ; Brock, Jane ; Johnson, Douglas B. ; Balko, Justin ; Wienert, Stephan ; Bossuyt, Veerle ; Michiels, Stefan ; Ternes, Nils ; Burchardi, Nicole ; Luen, Stephen J. ; Savas, Peter ; Klauschen, Frederick ; Watson, Peter H. ; Nelson, Brad H. ; Criscitiello, Carmen ; O'Toole, Sandra ; Larsimont, Denis ; De Wind, Roland ; Curigliano, Giuseppe ; André, Fabrice ; Lacroix-Triki, Magali ; Van De Vijver, Mark ; Rojo, Federico ; Floris, Giuseppe ; Bedri, Shahinaz ; Sparano, Joseph ; Rimm, David ; Nielsen, Torsten ; Kos, Zuzana ; Hewitt, Stephen ; Singh, Baljit ; Farshid, Gelareh ; Loibl, Sibylle ; Allison, Kimberly H. ; Tung, Nadine ; Adams, Sylvia ; Willard-Gallo, Karen ; Horlings, Hugo M. ; Gandhi, Leena ; Moreira, Andre ; Hirsch, Fred ; Dieci, Maria V. ; Urbanowicz, Maria ; Brcic, Iva ; Korski, Konstanty ; Gaire, Fabien ; Koeppen, Hartmut ; Lo, Amy ; Giltnane, Jennifer ; Rebelatto, Marlon C. ; Steele, Keith E. ; Zha, Jiping ; Emancipator, Kenneth ; Juco, Jonathan W. ; Denkert, Carsten ; Reis-Filho, Jorge ; Loi, Sherene ; Fox, Stephen B. / Assessing Tumor-Infiltrating Lymphocytes in Solid Tumors : A Practical Review for Pathologists and Proposal for a Standardized Method from the International Immuno-Oncology Biomarkers Working Group: Part 2: TILs in Melanoma, Gastrointestinal Tract Carcinomas, Non-Small Cell Lung Carcinoma and Mesothelioma, Endometrial and Ovarian Carcinomas, Squamous Cell Carcinoma of the Head and Neck, Genitourinary Carcinomas, and Primary Brain Tumors. In: Advances in Anatomic Pathology. 2017 ; Vol. 24, No. 6. pp. 311-335.
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TY - JOUR

T1 - Assessing Tumor-Infiltrating Lymphocytes in Solid Tumors

T2 - A Practical Review for Pathologists and Proposal for a Standardized Method from the International Immuno-Oncology Biomarkers Working Group: Part 2: TILs in Melanoma, Gastrointestinal Tract Carcinomas, Non-Small Cell Lung Carcinoma and Mesothelioma, Endometrial and Ovarian Carcinomas, Squamous Cell Carcinoma of the Head and Neck, Genitourinary Carcinomas, and Primary Brain Tumors

AU - Hendry, Shona

AU - Salgado, Roberto

AU - Gevaert, Thomas

AU - Russell, Prudence A.

AU - John, Tom

AU - Thapa, Bibhusal

AU - Christie, Michael

AU - Van De Vijver, Koen

AU - Estrada, M. V.

AU - Gonzalez-Ericsson, Paula I.

AU - Sanders, Melinda

AU - Solomon, Benjamin

AU - Solinas, Cinzia

AU - Van Den Eynden, Gert G.G.M.

AU - Allory, Yves

AU - Preusser, Matthias

AU - Hainfellner, Johannes

AU - Pruneri, Giancarlo

AU - Vingiani, Andrea

AU - Demaria, Sandra

AU - Symmans, Fraser

AU - Nuciforo, Paolo

AU - Comerma, Laura

AU - Thompson, E Aubrey

AU - Lakhani, Sunil

AU - Kim, Seong Rim

AU - Schnitt, Stuart

AU - Colpaert, Cecile

AU - Sotiriou, Christos

AU - Scherer, Stefan J.

AU - Ignatiadis, Michail

AU - Badve, Sunil

AU - Pierce, Robert H.

AU - Viale, Giuseppe

AU - Sirtaine, Nicolas

AU - Penault-Llorca, Frederique

AU - Sugie, Tomohagu

AU - Fineberg, Susan

AU - Paik, Soonmyung

AU - Srinivasan, Ashok

AU - Richardson, Andrea

AU - Wang, Yihong

AU - Chmielik, Ewa

AU - Brock, Jane

AU - Johnson, Douglas B.

AU - Balko, Justin

AU - Wienert, Stephan

AU - Bossuyt, Veerle

AU - Michiels, Stefan

AU - Ternes, Nils

AU - Burchardi, Nicole

AU - Luen, Stephen J.

AU - Savas, Peter

AU - Klauschen, Frederick

AU - Watson, Peter H.

AU - Nelson, Brad H.

AU - Criscitiello, Carmen

AU - O'Toole, Sandra

AU - Larsimont, Denis

AU - De Wind, Roland

AU - Curigliano, Giuseppe

AU - André, Fabrice

AU - Lacroix-Triki, Magali

AU - Van De Vijver, Mark

AU - Rojo, Federico

AU - Floris, Giuseppe

AU - Bedri, Shahinaz

AU - Sparano, Joseph

AU - Rimm, David

AU - Nielsen, Torsten

AU - Kos, Zuzana

AU - Hewitt, Stephen

AU - Singh, Baljit

AU - Farshid, Gelareh

AU - Loibl, Sibylle

AU - Allison, Kimberly H.

AU - Tung, Nadine

AU - Adams, Sylvia

AU - Willard-Gallo, Karen

AU - Horlings, Hugo M.

AU - Gandhi, Leena

AU - Moreira, Andre

AU - Hirsch, Fred

AU - Dieci, Maria V.

AU - Urbanowicz, Maria

AU - Brcic, Iva

AU - Korski, Konstanty

AU - Gaire, Fabien

AU - Koeppen, Hartmut

AU - Lo, Amy

AU - Giltnane, Jennifer

AU - Rebelatto, Marlon C.

AU - Steele, Keith E.

AU - Zha, Jiping

AU - Emancipator, Kenneth

AU - Juco, Jonathan W.

AU - Denkert, Carsten

AU - Reis-Filho, Jorge

AU - Loi, Sherene

AU - Fox, Stephen B.

PY - 2017/1/1

Y1 - 2017/1/1

N2 - Assessment of the immune response to tumors is growing in importance as the prognostic implications of this response are increasingly recognized, and as immunotherapies are evaluated and implemented in different tumor types. However, many different approaches can be used to assess and describe the immune response, which limits efforts at implementation as a routine clinical biomarker. In part 1 of this review, we have proposed a standardized methodology to assess tumor-infiltrating lymphocytes (TILs) in solid tumors, based on the International Immuno-Oncology Biomarkers Working Group guidelines for invasive breast carcinoma. In part 2 of this review, we discuss the available evidence for the prognostic and predictive value of TILs in common solid tumors, including carcinomas of the lung, gastrointestinal tract, genitourinary system, gynecologic system, and head and neck, as well as primary brain tumors, mesothelioma and melanoma. The particularities and different emphases in TIL assessment in different tumor types are discussed. The standardized methodology we propose can be adapted to different tumor types and may be used as a standard against which other approaches can be compared. Standardization of TIL assessment will help clinicians, researchers and pathologists to conclusively evaluate the utility of this simple biomarker in the current era of immunotherapy.

AB - Assessment of the immune response to tumors is growing in importance as the prognostic implications of this response are increasingly recognized, and as immunotherapies are evaluated and implemented in different tumor types. However, many different approaches can be used to assess and describe the immune response, which limits efforts at implementation as a routine clinical biomarker. In part 1 of this review, we have proposed a standardized methodology to assess tumor-infiltrating lymphocytes (TILs) in solid tumors, based on the International Immuno-Oncology Biomarkers Working Group guidelines for invasive breast carcinoma. In part 2 of this review, we discuss the available evidence for the prognostic and predictive value of TILs in common solid tumors, including carcinomas of the lung, gastrointestinal tract, genitourinary system, gynecologic system, and head and neck, as well as primary brain tumors, mesothelioma and melanoma. The particularities and different emphases in TIL assessment in different tumor types are discussed. The standardized methodology we propose can be adapted to different tumor types and may be used as a standard against which other approaches can be compared. Standardization of TIL assessment will help clinicians, researchers and pathologists to conclusively evaluate the utility of this simple biomarker in the current era of immunotherapy.

KW - biomarkers

KW - cancer

KW - immunotherapy

KW - lymphocytes

KW - pathology

KW - tumor-infiltrating

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DO - 10.1097/PAP.0000000000000161

M3 - Review article

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JO - Advances in Anatomic Pathology

JF - Advances in Anatomic Pathology

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