Pitfalls in assessing stromal tumor infiltrating lymphocytes (sTILs) in breast cancer.

Zuzana Kos; Elvire Roblin; Rim S. Kim; Stefan Michiels; Brandon D. Gallas; Weijie Chen; Koen K. van de Vijver; Shom Goel; Sylvia Adams; Sandra Demaria; Giuseppe Viale; Torsten O. Nielsen; Sunil S. Badve; W. Fraser Symmans; Christos Sotiriou; David L. Rimm; Stephen Hewitt; Carsten Denkert; Sibylle Loibl; Stephen J. Luen; John M. S. Bartlett; Peter Savas; Giancarlo Pruneri; Deborah A. Dillon; Maggie Chon U. Cheang; Andrew Tutt; Jacqueline A. Hall; Marleen Kok; Hugo M. Horlings; Anant Madabhushi; Jeroen van der Laak; Francesco Ciompi; Anne-Vibeke Laenkholm; Enrique Bellolio; Tina Gruosso; Stephen B. Fox; Juan Carlos Araya; Giuseppe Floris; Jan Hudeček; Leonie Voorwerk; Andrew H. Beck; Jen Kerner; Denis Larsimont; Sabine Declercq; Gert Van den Eynden; Lajos Pusztai; Anna Ehinger; Wentao Yang; Khalid AbdulJabbar; Yinyin Yuan; Rajendra Singh; Crispin Hiley; Maise Al Bakir; Alexander J. Lazar; Stephen Naber; Stephan Wienert; Miluska Castillo; Giuseppe Curigliano; Maria-Vittoria Dieci; Fabrice André; Charles Swanton; Jorge Reis-Filho; Joseph Sparano; Eva Balslev; I.-Chun Chen; Elisabeth Ida Specht Stovgaard; Katherine Pogue-Geile; Kim R. M. Blenman; Frédérique Penault-Llorca; Stuart Schnitt; Sunil R. Lakhani; Anne Vincent-Salomon; Federico Rojo; Jeremy P. Braybrooke; Matthew G. Hanna; M. Teresa Soler-Monsó; Daniel Bethmann; Carlos A. Castaneda; Karen Willard-Gallo; Ashish Sharma; Huang-Chun Lien; Susan Fineberg; Jeppe Thagaard; Laura Comerma; Paula Gonzalez-Ericsson; Edi Brogi; Sherene Loi; Joel Saltz; Frederick Klaushen; Lee Cooper; Mohamed Amgad; David A. Moore; Roberto Salgado

doi:10.1038/s41523-020-0156-0

Pitfalls in assessing stromal tumor infiltrating lymphocytes (sTILs) in breast cancer.

Zuzana Kos, Elvire Roblin, Rim S. Kim, Stefan Michiels, Brandon D. Gallas, Weijie Chen, Koen K. van de Vijver, Shom Goel, Sylvia Adams, Sandra Demaria, Giuseppe Viale, Torsten O. Nielsen, Sunil S. Badve, W. Fraser Symmans, Christos Sotiriou, David L. Rimm, Stephen Hewitt, Carsten Denkert, Sibylle Loibl, Stephen J. LuenJohn M. S. Bartlett, Peter Savas, Giancarlo Pruneri, Deborah A. Dillon, Maggie Chon U. Cheang, Andrew Tutt, Jacqueline A. Hall, Marleen Kok, Hugo M. Horlings, Anant Madabhushi, Jeroen van der Laak, Francesco Ciompi, Anne-Vibeke Laenkholm, Enrique Bellolio, Tina Gruosso, Stephen B. Fox, Juan Carlos Araya, Giuseppe Floris, Jan Hudeček, Leonie Voorwerk, Andrew H. Beck, Jen Kerner, Denis Larsimont, Sabine Declercq, Gert Van den Eynden, Lajos Pusztai, Anna Ehinger, Wentao Yang, Khalid AbdulJabbar, Yinyin Yuan, Rajendra Singh, Crispin Hiley, Maise Al Bakir, Alexander J. Lazar, Stephen Naber, Stephan Wienert, Miluska Castillo, Giuseppe Curigliano, Maria-Vittoria Dieci, Fabrice André, Charles Swanton, Jorge Reis-Filho, Joseph Sparano, Eva Balslev, I.-Chun Chen, Elisabeth Ida Specht Stovgaard, Katherine Pogue-Geile, Kim R. M. Blenman, Frédérique Penault-Llorca, Stuart Schnitt, Sunil R. Lakhani, Anne Vincent-Salomon, Federico Rojo, Jeremy P. Braybrooke, Matthew G. Hanna, M. Teresa Soler-Monsó, Daniel Bethmann, Carlos A. Castaneda, Karen Willard-Gallo, Ashish Sharma, Huang-Chun Lien, Susan Fineberg, Jeppe Thagaard, Laura Comerma, Paula Gonzalez-Ericsson, Edi Brogi, Sherene Loi, Joel Saltz, Frederick Klaushen, Lee Cooper, Mohamed Amgad, David A. Moore, Roberto Salgado

Research output: Contribution to journal › Article › peer-review

Abstract

Stromal tumor-infiltrating lymphocytes (sTILs) are important prognostic and predictive biomarkers in triple-negative (TNBC) and HER2-positive breast cancer. Incorporating sTILs into clinical practice necessitates reproducible assessment. Previously developed standardized scoring guidelines have been widely embraced by the clinical and research communities. We evaluated sources of variability in sTIL assessment by pathologists in three previous sTIL ring studies. We identify common challenges and evaluate impact of discrepancies on outcome estimates in early TNBC using a newly-developed prognostic tool. Discordant sTIL assessment is driven by heterogeneity in lymphocyte distribution. Additional factors include: technical slide-related issues; scoring outside the tumor boundary; tumors with minimal assessable stroma; including lymphocytes associated with other structures; and including other inflammatory cells. Small variations in sTIL assessment modestly alter risk estimation in early TNBC but have the potential to affect treatment selection if cutpoints are employed. Scoring and averaging multiple areas, as well as use of reference images, improve consistency of sTIL evaluation. Moreover, to assist in avoiding the pitfalls identified in this analysis, we developed an educational resource available at www.tilsinbreastcancer.org/pitfalls.

Original language	English
Pages (from-to)	17
Number of pages	1
Journal	npj Breast Cancer
Volume	6
DOIs	https://doi.org/10.1038/s41523-020-0156-0
Publication status	Published - 2020

Keywords

Immunosurveillance
Prognostic markers

Access to Document

10.1038/s41523-020-0156-0

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Kos, Z., Roblin, E., Kim, R. S., Michiels, S., Gallas, B. D., Chen, W., van de Vijver, K. K., Goel, S., Adams, S., Demaria, S., Viale, G., Nielsen, T. O., Badve, S. S., Symmans, W. F., Sotiriou, C., Rimm, D. L., Hewitt, S., Denkert, C., Loibl, S., ... Salgado, R. (2020). Pitfalls in assessing stromal tumor infiltrating lymphocytes (sTILs) in breast cancer. npj Breast Cancer, 6, 17. https://doi.org/10.1038/s41523-020-0156-0

Pitfalls in assessing stromal tumor infiltrating lymphocytes (sTILs) in breast cancer. / Kos, Zuzana; Roblin, Elvire; Kim, Rim S.; Michiels, Stefan; Gallas, Brandon D.; Chen, Weijie; van de Vijver, Koen K.; Goel, Shom; Adams, Sylvia; Demaria, Sandra; Viale, Giuseppe; Nielsen, Torsten O.; Badve, Sunil S.; Symmans, W. Fraser; Sotiriou, Christos; Rimm, David L.; Hewitt, Stephen; Denkert, Carsten; Loibl, Sibylle; Luen, Stephen J.; Bartlett, John M. S.; Savas, Peter; Pruneri, Giancarlo; Dillon, Deborah A.; Cheang, Maggie Chon U.; Tutt, Andrew; Hall, Jacqueline A.; Kok, Marleen; Horlings, Hugo M.; Madabhushi, Anant; van der Laak, Jeroen; Ciompi, Francesco; Laenkholm, Anne-Vibeke; Bellolio, Enrique; Gruosso, Tina; Fox, Stephen B.; Araya, Juan Carlos; Floris, Giuseppe; Hudeček, Jan; Voorwerk, Leonie; Beck, Andrew H.; Kerner, Jen; Larsimont, Denis; Declercq, Sabine; Van den Eynden, Gert; Pusztai, Lajos; Ehinger, Anna; Yang, Wentao; AbdulJabbar, Khalid; Yuan, Yinyin; Singh, Rajendra; Hiley, Crispin; Bakir, Maise Al; Lazar, Alexander J.; Naber, Stephen; Wienert, Stephan; Castillo, Miluska; Curigliano, Giuseppe ; Dieci, Maria-Vittoria; André, Fabrice; Swanton, Charles; Reis-Filho, Jorge; Sparano, Joseph; Balslev, Eva; Chen, I.-Chun; Stovgaard, Elisabeth Ida Specht; Pogue-Geile, Katherine; Blenman, Kim R. M.; Penault-Llorca, Frédérique; Schnitt, Stuart; Lakhani, Sunil R.; Vincent-Salomon, Anne; Rojo, Federico; Braybrooke, Jeremy P.; Hanna, Matthew G.; Soler-Monsó, M. Teresa; Bethmann, Daniel; Castaneda, Carlos A.; Willard-Gallo, Karen; Sharma, Ashish; Lien, Huang-Chun; Fineberg, Susan; Thagaard, Jeppe; Comerma, Laura; Gonzalez-Ericsson, Paula; Brogi, Edi; Loi, Sherene; Saltz, Joel; Klaushen, Frederick; Cooper, Lee; Amgad, Mohamed; Moore, David A.; Salgado, Roberto.

In: npj Breast Cancer, Vol. 6, 2020, p. 17.

Research output: Contribution to journal › Article › peer-review

Kos, Z, Roblin, E, Kim, RS, Michiels, S, Gallas, BD, Chen, W, van de Vijver, KK, Goel, S, Adams, S, Demaria, S, Viale, G, Nielsen, TO, Badve, SS, Symmans, WF, Sotiriou, C, Rimm, DL, Hewitt, S, Denkert, C, Loibl, S, Luen, SJ, Bartlett, JMS, Savas, P, Pruneri, G, Dillon, DA, Cheang, MCU, Tutt, A, Hall, JA, Kok, M, Horlings, HM, Madabhushi, A, van der Laak, J, Ciompi, F, Laenkholm, A-V, Bellolio, E, Gruosso, T, Fox, SB, Araya, JC, Floris, G, Hudeček, J, Voorwerk, L, Beck, AH, Kerner, J, Larsimont, D, Declercq, S, Van den Eynden, G, Pusztai, L, Ehinger, A, Yang, W, AbdulJabbar, K, Yuan, Y, Singh, R, Hiley, C, Bakir, MA, Lazar, AJ, Naber, S, Wienert, S, Castillo, M, Curigliano, G , Dieci, M-V, André, F, Swanton, C, Reis-Filho, J, Sparano, J, Balslev, E, Chen, I-C, Stovgaard, EIS, Pogue-Geile, K, Blenman, KRM, Penault-Llorca, F, Schnitt, S, Lakhani, SR, Vincent-Salomon, A, Rojo, F, Braybrooke, JP, Hanna, MG, Soler-Monsó, MT, Bethmann, D, Castaneda, CA, Willard-Gallo, K, Sharma, A, Lien, H-C, Fineberg, S, Thagaard, J, Comerma, L, Gonzalez-Ericsson, P, Brogi, E, Loi, S, Saltz, J, Klaushen, F, Cooper, L, Amgad, M, Moore, DA & Salgado, R 2020, 'Pitfalls in assessing stromal tumor infiltrating lymphocytes (sTILs) in breast cancer.', npj Breast Cancer, vol. 6, pp. 17. https://doi.org/10.1038/s41523-020-0156-0

Kos, Zuzana ; Roblin, Elvire ; Kim, Rim S. ; Michiels, Stefan ; Gallas, Brandon D. ; Chen, Weijie ; van de Vijver, Koen K. ; Goel, Shom ; Adams, Sylvia ; Demaria, Sandra ; Viale, Giuseppe ; Nielsen, Torsten O. ; Badve, Sunil S. ; Symmans, W. Fraser ; Sotiriou, Christos ; Rimm, David L. ; Hewitt, Stephen ; Denkert, Carsten ; Loibl, Sibylle ; Luen, Stephen J. ; Bartlett, John M. S. ; Savas, Peter ; Pruneri, Giancarlo ; Dillon, Deborah A. ; Cheang, Maggie Chon U. ; Tutt, Andrew ; Hall, Jacqueline A. ; Kok, Marleen ; Horlings, Hugo M. ; Madabhushi, Anant ; van der Laak, Jeroen ; Ciompi, Francesco ; Laenkholm, Anne-Vibeke ; Bellolio, Enrique ; Gruosso, Tina ; Fox, Stephen B. ; Araya, Juan Carlos ; Floris, Giuseppe ; Hudeček, Jan ; Voorwerk, Leonie ; Beck, Andrew H. ; Kerner, Jen ; Larsimont, Denis ; Declercq, Sabine ; Van den Eynden, Gert ; Pusztai, Lajos ; Ehinger, Anna ; Yang, Wentao ; AbdulJabbar, Khalid ; Yuan, Yinyin ; Singh, Rajendra ; Hiley, Crispin ; Bakir, Maise Al ; Lazar, Alexander J. ; Naber, Stephen ; Wienert, Stephan ; Castillo, Miluska ; Curigliano, Giuseppe ; Dieci, Maria-Vittoria ; André, Fabrice ; Swanton, Charles ; Reis-Filho, Jorge ; Sparano, Joseph ; Balslev, Eva ; Chen, I.-Chun ; Stovgaard, Elisabeth Ida Specht ; Pogue-Geile, Katherine ; Blenman, Kim R. M. ; Penault-Llorca, Frédérique ; Schnitt, Stuart ; Lakhani, Sunil R. ; Vincent-Salomon, Anne ; Rojo, Federico ; Braybrooke, Jeremy P. ; Hanna, Matthew G. ; Soler-Monsó, M. Teresa ; Bethmann, Daniel ; Castaneda, Carlos A. ; Willard-Gallo, Karen ; Sharma, Ashish ; Lien, Huang-Chun ; Fineberg, Susan ; Thagaard, Jeppe ; Comerma, Laura ; Gonzalez-Ericsson, Paula ; Brogi, Edi ; Loi, Sherene ; Saltz, Joel ; Klaushen, Frederick ; Cooper, Lee ; Amgad, Mohamed ; Moore, David A. ; Salgado, Roberto. / Pitfalls in assessing stromal tumor infiltrating lymphocytes (sTILs) in breast cancer. In: npj Breast Cancer. 2020 ; Vol. 6. pp. 17.

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title = "Pitfalls in assessing stromal tumor infiltrating lymphocytes (sTILs) in breast cancer.",

abstract = "Stromal tumor-infiltrating lymphocytes (sTILs) are important prognostic and predictive biomarkers in triple-negative (TNBC) and HER2-positive breast cancer. Incorporating sTILs into clinical practice necessitates reproducible assessment. Previously developed standardized scoring guidelines have been widely embraced by the clinical and research communities. We evaluated sources of variability in sTIL assessment by pathologists in three previous sTIL ring studies. We identify common challenges and evaluate impact of discrepancies on outcome estimates in early TNBC using a newly-developed prognostic tool. Discordant sTIL assessment is driven by heterogeneity in lymphocyte distribution. Additional factors include: technical slide-related issues; scoring outside the tumor boundary; tumors with minimal assessable stroma; including lymphocytes associated with other structures; and including other inflammatory cells. Small variations in sTIL assessment modestly alter risk estimation in early TNBC but have the potential to affect treatment selection if cutpoints are employed. Scoring and averaging multiple areas, as well as use of reference images, improve consistency of sTIL evaluation. Moreover, to assist in avoiding the pitfalls identified in this analysis, we developed an educational resource available at www.tilsinbreastcancer.org/pitfalls.",

keywords = "Immunosurveillance, Prognostic markers",

author = "Zuzana Kos and Elvire Roblin and Kim, {Rim S.} and Stefan Michiels and Gallas, {Brandon D.} and Weijie Chen and {van de Vijver}, {Koen K.} and Shom Goel and Sylvia Adams and Sandra Demaria and Giuseppe Viale and Nielsen, {Torsten O.} and Badve, {Sunil S.} and Symmans, {W. Fraser} and Christos Sotiriou and Rimm, {David L.} and Stephen Hewitt and Carsten Denkert and Sibylle Loibl and Luen, {Stephen J.} and Bartlett, {John M. S.} and Peter Savas and Giancarlo Pruneri and Dillon, {Deborah A.} and Cheang, {Maggie Chon U.} and Andrew Tutt and Hall, {Jacqueline A.} and Marleen Kok and Horlings, {Hugo M.} and Anant Madabhushi and {van der Laak}, Jeroen and Francesco Ciompi and Anne-Vibeke Laenkholm and Enrique Bellolio and Tina Gruosso and Fox, {Stephen B.} and Araya, {Juan Carlos} and Giuseppe Floris and Jan Hude{\v c}ek and Leonie Voorwerk and Beck, {Andrew H.} and Jen Kerner and Denis Larsimont and Sabine Declercq and {Van den Eynden}, Gert and Lajos Pusztai and Anna Ehinger and Wentao Yang and Khalid AbdulJabbar and Yinyin Yuan and Rajendra Singh and Crispin Hiley and Bakir, {Maise Al} and Lazar, {Alexander J.} and Stephen Naber and Stephan Wienert and Miluska Castillo and Giuseppe Curigliano and Maria-Vittoria Dieci and Fabrice Andr{\'e} and Charles Swanton and Jorge Reis-Filho and Joseph Sparano and Eva Balslev and I.-Chun Chen and Stovgaard, {Elisabeth Ida Specht} and Katherine Pogue-Geile and Blenman, {Kim R. M.} and Fr{\'e}d{\'e}rique Penault-Llorca and Stuart Schnitt and Lakhani, {Sunil R.} and Anne Vincent-Salomon and Federico Rojo and Braybrooke, {Jeremy P.} and Hanna, {Matthew G.} and Soler-Mons{\'o}, {M. Teresa} and Daniel Bethmann and Castaneda, {Carlos A.} and Karen Willard-Gallo and Ashish Sharma and Huang-Chun Lien and Susan Fineberg and Jeppe Thagaard and Laura Comerma and Paula Gonzalez-Ericsson and Edi Brogi and Sherene Loi and Joel Saltz and Frederick Klaushen and Lee Cooper and Mohamed Amgad and Moore, {David A.} and Roberto Salgado",

year = "2020",

doi = "10.1038/s41523-020-0156-0",

language = "English",

volume = "6",

pages = "17",

journal = "npj Breast Cancer",

issn = "2374-4677",

publisher = "Nature Publishing Group",

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TY - JOUR

T1 - Pitfalls in assessing stromal tumor infiltrating lymphocytes (sTILs) in breast cancer.

AU - Kos, Zuzana

AU - Roblin, Elvire

AU - Kim, Rim S.

AU - Michiels, Stefan

AU - Gallas, Brandon D.

AU - Chen, Weijie

AU - van de Vijver, Koen K.

AU - Goel, Shom

AU - Adams, Sylvia

AU - Demaria, Sandra

AU - Viale, Giuseppe

AU - Nielsen, Torsten O.

AU - Badve, Sunil S.

AU - Symmans, W. Fraser

AU - Sotiriou, Christos

AU - Rimm, David L.

AU - Hewitt, Stephen

AU - Denkert, Carsten

AU - Loibl, Sibylle

AU - Luen, Stephen J.

AU - Bartlett, John M. S.

AU - Savas, Peter

AU - Pruneri, Giancarlo

AU - Dillon, Deborah A.

AU - Cheang, Maggie Chon U.

AU - Tutt, Andrew

AU - Hall, Jacqueline A.

AU - Kok, Marleen

AU - Horlings, Hugo M.

AU - Madabhushi, Anant

AU - van der Laak, Jeroen

AU - Ciompi, Francesco

AU - Laenkholm, Anne-Vibeke

AU - Bellolio, Enrique

AU - Gruosso, Tina

AU - Fox, Stephen B.

AU - Araya, Juan Carlos

AU - Floris, Giuseppe

AU - Hudeček, Jan

AU - Voorwerk, Leonie

AU - Beck, Andrew H.

AU - Kerner, Jen

AU - Larsimont, Denis

AU - Declercq, Sabine

AU - Van den Eynden, Gert

AU - Pusztai, Lajos

AU - Ehinger, Anna

AU - Yang, Wentao

AU - AbdulJabbar, Khalid

AU - Yuan, Yinyin

AU - Singh, Rajendra

AU - Hiley, Crispin

AU - Bakir, Maise Al

AU - Lazar, Alexander J.

AU - Naber, Stephen

AU - Wienert, Stephan

AU - Castillo, Miluska

AU - Curigliano, Giuseppe

AU - Dieci, Maria-Vittoria

AU - André, Fabrice

AU - Swanton, Charles

AU - Reis-Filho, Jorge

AU - Sparano, Joseph

AU - Balslev, Eva

AU - Chen, I.-Chun

AU - Stovgaard, Elisabeth Ida Specht

AU - Pogue-Geile, Katherine

AU - Blenman, Kim R. M.

AU - Penault-Llorca, Frédérique

AU - Schnitt, Stuart

AU - Lakhani, Sunil R.

AU - Vincent-Salomon, Anne

AU - Rojo, Federico

AU - Braybrooke, Jeremy P.

AU - Hanna, Matthew G.

AU - Soler-Monsó, M. Teresa

AU - Bethmann, Daniel

AU - Castaneda, Carlos A.

AU - Willard-Gallo, Karen

AU - Sharma, Ashish

AU - Lien, Huang-Chun

AU - Fineberg, Susan

AU - Thagaard, Jeppe

AU - Comerma, Laura

AU - Gonzalez-Ericsson, Paula

AU - Brogi, Edi

AU - Loi, Sherene

AU - Saltz, Joel

AU - Klaushen, Frederick

AU - Cooper, Lee

AU - Amgad, Mohamed

AU - Moore, David A.

AU - Salgado, Roberto

PY - 2020

Y1 - 2020

N2 - Stromal tumor-infiltrating lymphocytes (sTILs) are important prognostic and predictive biomarkers in triple-negative (TNBC) and HER2-positive breast cancer. Incorporating sTILs into clinical practice necessitates reproducible assessment. Previously developed standardized scoring guidelines have been widely embraced by the clinical and research communities. We evaluated sources of variability in sTIL assessment by pathologists in three previous sTIL ring studies. We identify common challenges and evaluate impact of discrepancies on outcome estimates in early TNBC using a newly-developed prognostic tool. Discordant sTIL assessment is driven by heterogeneity in lymphocyte distribution. Additional factors include: technical slide-related issues; scoring outside the tumor boundary; tumors with minimal assessable stroma; including lymphocytes associated with other structures; and including other inflammatory cells. Small variations in sTIL assessment modestly alter risk estimation in early TNBC but have the potential to affect treatment selection if cutpoints are employed. Scoring and averaging multiple areas, as well as use of reference images, improve consistency of sTIL evaluation. Moreover, to assist in avoiding the pitfalls identified in this analysis, we developed an educational resource available at www.tilsinbreastcancer.org/pitfalls.

AB - Stromal tumor-infiltrating lymphocytes (sTILs) are important prognostic and predictive biomarkers in triple-negative (TNBC) and HER2-positive breast cancer. Incorporating sTILs into clinical practice necessitates reproducible assessment. Previously developed standardized scoring guidelines have been widely embraced by the clinical and research communities. We evaluated sources of variability in sTIL assessment by pathologists in three previous sTIL ring studies. We identify common challenges and evaluate impact of discrepancies on outcome estimates in early TNBC using a newly-developed prognostic tool. Discordant sTIL assessment is driven by heterogeneity in lymphocyte distribution. Additional factors include: technical slide-related issues; scoring outside the tumor boundary; tumors with minimal assessable stroma; including lymphocytes associated with other structures; and including other inflammatory cells. Small variations in sTIL assessment modestly alter risk estimation in early TNBC but have the potential to affect treatment selection if cutpoints are employed. Scoring and averaging multiple areas, as well as use of reference images, improve consistency of sTIL evaluation. Moreover, to assist in avoiding the pitfalls identified in this analysis, we developed an educational resource available at www.tilsinbreastcancer.org/pitfalls.

KW - Immunosurveillance

KW - Prognostic markers

U2 - 10.1038/s41523-020-0156-0

DO - 10.1038/s41523-020-0156-0

M3 - Article

VL - 6

SP - 17

JO - npj Breast Cancer

JF - npj Breast Cancer

SN - 2374-4677

ER -

Pitfalls in assessing stromal tumor infiltrating lymphocytes (sTILs) in breast cancer.

Abstract

Keywords

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