Journal Article
. 2015 Feb; 107(3):.
doi: 10.1093/jnci/dju435.

Objective measurement and clinical significance of TILs in non-small cell lung cancer

Kurt A Schalper 1 Jason Brown 2 Daniel Carvajal-Hausdorf 2 Joseph McLaughlin 2 Vamsidhar Velcheti 2 Konstantinos N Syrigos 2 Roy S Herbst 2 David L Rimm 2 
Affiliations
  • PMID: 25650315
  •     22 References
  •     145 citations

Abstract

Background: Tumor-infiltrating lymphocytes (TILs) are usually measured using subjective methods. Studies suggest that TIL subtypes have independent roles in cancer and that they could support the use of novel immunostimulatory therapies. We simultaneously measured TIL subtypes in non-small cell lung cancer (NSCLC) samples using objective methods and determined their relationship with clinico-pathologic characteristics and survival.

Methods: Using multiplexed quantitative fluorescence (QIF), we measured the levels of CD3, CD8, and CD20 in 552 NSCLC from two independent collections represented in tissue microarrays (YTMA79, n = 202 and YTMA140, n = 350). The level of TILs was obtained in different tumor compartments using cytokeratin stain to define tumor cells and 4',6-Diamidino-2-Phenylindole. Association of TILs with clinical parameters was determined using univariate and multivariable analyses. All statistical tests were two-sided.

Results: In both NSCLC collections there was a low correlation between the three TIL markers (linear regression coefficients (R(2)) = 0.19-0.22, P < .001 for YTMA79 and R(2) = 0.23-0.32, P < .001 for YTMA140). No consistent association between the level of TIL subtypes and age, sex, smoking history, tumor size, stage, and histology type was found. In univariate analysis, an elevated CD3 or CD8 signal was statistically significantly associated with longer survival in both collections. However, only CD8 was independent from age, tumor size, histology, and stage in multivariable analysis. High CD20 was associated with longer survival in the YTMA79 cohort.

Conclusions: Increased levels of CD3 and CD8 + TILs are associated with better outcome in NSCLC, but only CD8 is independent from other prognostic variables. Objective measurement of TIL subpopulations could be useful to predict response or evaluate the local immune effect of anticancer immune checkpoint inhibitors.

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Xiaoliang Zhao, Bhaskar Kallakury, +7 authors, Giuseppe Giaccone.
J Thorac Oncol, 2019 Feb 09; 14(5). PMID: 30735815    Free PMC article.
Immune Cell Composition in Human Non-small Cell Lung Cancer.
Branislava Stankovic, Heidi Anine Korsmo Bjørhovde, +11 authors, Alexandre Corthay.
Front Immunol, 2019 Feb 19; 9. PMID: 30774636    Free PMC article.
Highly Cited.
Immunotherapy in Non-Small Cell Lung Cancer: Facts and Hopes.
Deborah B Doroshow, Miguel F Sanmamed, +6 authors, Roy S Herbst.
Clin Cancer Res, 2019 Mar 03; 25(15). PMID: 30824587    Free PMC article.
Highly Cited. Review.
Expression and clinical significance of PD-L1, B7-H3, B7-H4 and TILs in human small cell lung Cancer (SCLC).
Daniel Carvajal-Hausdorf, Mehmet Altan, +4 authors, Kurt A Schalper.
J Immunother Cancer, 2019 Mar 10; 7(1). PMID: 30850021    Free PMC article.
Proteogenomic landscape of squamous cell lung cancer.
Paul A Stewart, Eric A Welsh, +25 authors, Eric B Haura.
Nat Commun, 2019 Aug 10; 10(1). PMID: 31395880    Free PMC article.
Tumor-Infiltrating Lymphocytes in the Checkpoint Inhibitor Era.
Gerald P Linette, Beatriz M Carreno.
Curr Hematol Malig Rep, 2019 Jun 13; 14(4). PMID: 31187421    Free PMC article.
Review.
The role of B lymphocytes in the immuno-biology of non-small-cell lung cancer.
Akshay J Patel, Alex Richter, Mark T Drayson, Gary W Middleton.
Cancer Immunol Immunother, 2020 Jan 07; 69(3). PMID: 31901949    Free PMC article.
Review.
High-Plex Predictive Marker Discovery for Melanoma Immunotherapy-Treated Patients Using Digital Spatial Profiling.
Maria I Toki, Christopher R Merritt, +7 authors, David L Rimm.
Clin Cancer Res, 2019 Jun 14; 25(18). PMID: 31189645    Free PMC article.
Advances and challenges in immunotherapy of small cell lung cancer.
Hanfei Guo, Lingyu Li, Jiuwei Cui.
Chin J Cancer Res, 2020 Mar 21; 32(1). PMID: 32194311    Free PMC article.
Coordinated signals from PARP-1 and PARP-2 are required to establish a proper T cell immune response to breast tumors in mice.
Lucia Moreno-Lama, Miguel A Galindo-Campos, +11 authors, José Yélamos.
Oncogene, 2020 Feb 01; 39(13). PMID: 32001817
A new method for predicting survival in stage I non-small cell lung cancer patients: nomogram based on macrophage immunoscore, TNM stage and lymphocyte-to-monocyte ratio.
Jiani Gao, Yijiu Ren, +11 authors, Chang Chen.
Ann Transl Med, 2020 May 13; 8(7). PMID: 32395514    Free PMC article.
Report on computational assessment of Tumor Infiltrating Lymphocytes from the International Immuno-Oncology Biomarker Working Group.
Mohamed Amgad, Elisabeth Specht Stovgaard, +66 authors, International Immuno-Oncology Biomarker Working Group.
NPJ Breast Cancer, 2020 May 16; 6. PMID: 32411818    Free PMC article.
Review.
Phase I/Ib Study of Pembrolizumab Plus Vorinostat in Advanced/Metastatic Non-Small Cell Lung Cancer.
Jhanelle E Gray, Andreas Saltos, +14 authors, Amer A Beg.
Clin Cancer Res, 2019 Aug 15; 25(22). PMID: 31409616    Free PMC article.
Identification and Analysis of Dysfunctional Genes and Pathways in CD8+ T Cells of Non-Small Cell Lung Cancer Based on RNA Sequencing.
Xuefang Tao, Xiaotang Wu, Tao Huang, Deguang Mu.
Front Genet, 2020 May 28; 11. PMID: 32457792    Free PMC article.
Molecular subtypes of oropharyngeal cancer show distinct immune microenvironment related with immune checkpoint blockade response.
Min Hwan Kim, Jae-Hwan Kim, +15 authors, Hye Ryun Kim.
Br J Cancer, 2020 Apr 03; 122(11). PMID: 32235905    Free PMC article.
A four-factor immune risk score signature predicts the clinical outcome of patients with spinal chordoma.
Ming-Xiang Zou, Yue Pan, +7 authors, Jing Li.
Clin Transl Med, 2020 Jun 09; 10(1). PMID: 32508056    Free PMC article.
Precision Medicine for NSCLC in the Era of Immunotherapy: New Biomarkers to Select the Most Suitable Treatment or the Most Suitable Patient.
Giovanni Rossi, Alessandro Russo, +13 authors, Carlo Genova.
Cancers (Basel), 2020 May 06; 12(5). PMID: 32365882    Free PMC article.
Review.
Targeting Autophagy Facilitates T Lymphocyte Migration by Inducing the Expression of CXCL10 in Gastric Cancer Cell Lines.
Qingyuan Meng, Yihong Zhang, Liangbiao George Hu.
Front Oncol, 2020 Jun 26; 10. PMID: 32582551    Free PMC article.
Single-cell transcriptome and antigen-immunoglobin analysis reveals the diversity of B cells in non-small cell lung cancer.
Jian Chen, Yun Tan, +16 authors, Peng Zhang.
Genome Biol, 2020 Jun 26; 21(1). PMID: 32580738    Free PMC article.
Resistance to immune checkpoint inhibitors in non-small cell lung cancer: biomarkers and therapeutic strategies.
Robert J Walsh, Ross A Soo.
Ther Adv Med Oncol, 2020 Jul 17; 12. PMID: 32670423    Free PMC article.
Review.
CDK7 inhibitor THZ1 enhances antiPD-1 therapy efficacy via the p38α/MYC/PD-L1 signaling in non-small cell lung cancer.
Jian Wang, Ruiguang Zhang, +14 authors, Gang Wu.
J Hematol Oncol, 2020 Jul 22; 13(1). PMID: 32690037    Free PMC article.
Pembrolizumab for management of patients with NSCLC and brain metastases: long-term results and biomarker analysis from a non-randomised, open-label, phase 2 trial.
Sarah B Goldberg, Kurt A Schalper, +21 authors, Harriet M Kluger.
Lancet Oncol, 2020 Apr 07; 21(5). PMID: 32251621    Free PMC article.
Microarray analysis of the expression profile of immune-related gene in rapid recurrence early-stage lung adenocarcinoma.
Jie Liu, Xiao Yang, +9 authors, Dong Wang.
J Cancer Res Clin Oncol, 2020 Jun 20; 146(9). PMID: 32556504    Free PMC article.
Competition NMR for Detection of Hit/Lead Inhibitors of Protein-Protein Interactions.
Bogdan Musielak, Weronika Janczyk, +4 authors, Tad Holak.
Molecules, 2020 Jul 08; 25(13). PMID: 32630327    Free PMC article.
Expression Analysis and Significance of PD-1, LAG-3, and TIM-3 in Human Non-Small Cell Lung Cancer Using Spatially Resolved and Multiparametric Single-Cell Analysis.
Ila Datar, Miguel F Sanmamed, +22 authors, Kurt A Schalper.
Clin Cancer Res, 2019 May 06; 25(15). PMID: 31053602    Free PMC article.
Highly Cited.
An integrated classifier improves prognostic accuracy in non-metastatic gastric cancer.
Xiaofang Xing, Shuqin Jia, +15 authors, Jiafu Ji.
Oncoimmunology, 2020 Sep 18; 9(1). PMID: 32939321    Free PMC article.
VISTA/PD-1H: a potential target for non-small cell lung cancer immunotherapy.
Juan-Manuel Hernandez-Martinez, Edgar Vergara, +2 authors, Oscar Arrieta.
J Thorac Dis, 2019 Feb 13; 10(12). PMID: 30746169    Free PMC article.
Multiplexed Immunohistochemistry for Molecular and Immune Profiling in Lung Cancer-Just About Ready for Prime-Time?
Paul Hofman, Cécile Badoual, +8 authors, Marius Ilié.
Cancers (Basel), 2019 Mar 02; 11(3). PMID: 30818873    Free PMC article.
Review.
Prognostic value of tumor-infiltrating lymphocytes in melanoma: a systematic review and meta-analysis.
Qiaofen Fu, Nan Chen, +9 authors, Gaofeng Li.
Oncoimmunology, 2019 May 31; 8(7). PMID: 31143514    Free PMC article.
Highly Cited. Review.
KRAS-Driven Lung Adenocarcinoma and B Cell Infiltration: Novel Insights for Immunotherapy.
Rosamaria Pinto, Daniela Petriella, +9 authors, Simona De Summa.
Cancers (Basel), 2019 Aug 14; 11(8). PMID: 31405063    Free PMC article.
Immune contexture analysis in immuno-oncology: applications and challenges of multiplex fluorescent immunohistochemistry.
Reshma Shakya, Tam Hong Nguyen, Nigel Waterhouse, Rajiv Khanna.
Clin Transl Immunology, 2020 Oct 20; 9(10). PMID: 33072322    Free PMC article.
Review.
Significantly different immunoscores in lung adenocarcinoma and squamous cell carcinoma and a proposal for a new immune staging system.
Ziqing Zeng, Fan Yang, +5 authors, Xiubao Ren.
Oncoimmunology, 2020 Oct 27; 9(1). PMID: 33101777    Free PMC article.
The Effect of Mouse Strain, Sex, and Carcinogen Dose on Toxicity and the Development of Lung Dysplasia and Squamous Cell Carcinomas in Mice.
Laura Riolobos, Ekram A Gad, +5 authors, Mary L Disis.
Cancer Prev Res (Phila), 2019 May 19; 12(8). PMID: 31101634    Free PMC article.
Differential Expression and Significance of PD-L1, IDO-1, and B7-H4 in Human Lung Cancer.
Kurt A Schalper, Daniel Carvajal-Hausdorf, +7 authors, David L Rimm.
Clin Cancer Res, 2016 Jul 22; 23(2). PMID: 27440266    Free PMC article.
Highly Cited.
Lung Adenocarcinoma and Squamous Cell Carcinoma Gene Expression Subtypes Demonstrate Significant Differences in Tumor Immune Landscape.
Hawazin Faruki, Gregory M Mayhew, +3 authors, Myla Lai-Goldman.
J Thorac Oncol, 2017 Mar 28; 12(6). PMID: 28341226    Free PMC article.
Highly Cited.
Identification of Proteomic Features To Distinguish Benign Pulmonary Nodules from Lung Adenocarcinoma.
Simona G Codreanu, Megan D Hoeksema, +8 authors, Pierre P Massion.
J Proteome Res, 2017 Jul 22; 16(9). PMID: 28731711    Free PMC article.
Tumor-infiltrating CD8+ T cells combined with tumor-associated CD68+ macrophages predict postoperative prognosis and adjuvant chemotherapy benefit in resected gastric cancer.
Jun Lu, Yu Xu, +8 authors, Chang-Ming Huang.
BMC Cancer, 2019 Sep 16; 19(1). PMID: 31521128    Free PMC article.
Heat shock factor 5 correlated with immune infiltration serves as a prognostic biomarker in lung adenocarcinoma.
Rusidanmu Aizemaiti, Zhigang Wu, +2 authors, Xiayi Lv.
Int J Med Sci, 2021 Jan 05; 18(2). PMID: 33390814    Free PMC article.
Gene signature based on B cell predicts clinical outcome of radiotherapy and immunotherapy for patients with lung adenocarcinoma.
Linzhi Han, Hongjie Shi, +6 authors, Conghua Xie.
Cancer Med, 2020 Oct 25; 9(24). PMID: 33098370    Free PMC article.
Baseline immunity and impact of chemotherapy on immune microenvironment in cervical cancer.
Yi Zhang, Minhua Yu, +14 authors, Wen Di.
Br J Cancer, 2020 Oct 23; 124(2). PMID: 33087896    Free PMC article.
Clinical impact of the tumor immune microenvironment in completely resected stage IIIA(N2) non-small cell lung cancer based on an immunoscore approach.
Wen Feng, Yuan Li, +6 authors, Xiao-Long Fu.
Ther Adv Med Oncol, 2021 Jan 26; 13. PMID: 33488784    Free PMC article.
[Overview of Multiplex Immunohistochemistry and Immunofluorescence Techniques 
in the Lung Cancer Immunotherapy].
Wenjia Sun, Jianya Zhou, Jianying Zhou.
Zhongguo Fei Ai Za Zhi, 2021 Jan 23; 24(1). PMID: 33478189    Free PMC article.
Review.
CD137+ T-Cells: Protagonists of the Immunotherapy Revolution.
Alessio Ugolini, Marianna Nuti.
Cancers (Basel), 2021 Feb 04; 13(3). PMID: 33530328    Free PMC article.
Review.
Evaluation of pembrolizumab for the treatment of advanced non-small cell lung cancer: a retrospective, single-centre, single-arm study.
Tianxing Guo, Yun Ding, +7 authors, Xiaojie Pan.
J Thorac Dis, 2021 Feb 12; 13(1). PMID: 33569208    Free PMC article.
Emerging biomarkers for neoadjuvant immune checkpoint inhibitors in operable non-small cell lung cancer.
Monika Pradhan, Mathieu Chocry, +2 authors, Tina Cascone.
Transl Lung Cancer Res, 2021 Feb 12; 10(1). PMID: 33569339    Free PMC article.
Review.
Tumor β-catenin expression is associated with immune evasion in non-small cell lung cancer with high tumor mutation burden.
Satoshi Muto, Yuki Ozaki, +18 authors, Hiroyuki Suzuki.
Oncol Lett, 2021 Feb 13; 21(3). PMID: 33574942    Free PMC article.
AURKA and FAM83A are prognostic biomarkers and correlated with Tumor-infiltrating Lymphocytes in smoking related Lung Adenocarcinoma.
Mengyu Zhang, Chen Huo, +4 authors, Yiqing Qu.
J Cancer, 2021 Feb 23; 12(6). PMID: 33613763    Free PMC article.
Immune landscape and a promising immune prognostic model associated with TP53 in early-stage lung adenocarcinoma.
Chengde Wu, Xiang Rao, Wei Lin.
Cancer Med, 2020 Dec 15; 10(3). PMID: 33314730    Free PMC article.
The Importance of STK11/LKB1 Assessment in Non-Small Cell Lung Carcinomas.
Baharia Mograbi, Simon Heeke, Paul Hofman.
Diagnostics (Basel), 2021 Feb 13; 11(2). PMID: 33572782    Free PMC article.
Review.
Tsukushi is a novel prognostic biomarker and correlates with tumor-infiltrating B cells in non-small cell lung cancer.
Hao Huang, Ding Zhang, +10 authors, Yashuang Zhao.
Aging (Albany NY), 2021 Jan 12; 13(3). PMID: 33428594    Free PMC article.
Prognostic biomarker TUBA1C is correlated to immune cell infiltration in the tumor microenvironment of lung adenocarcinoma.
Tingting Bian, Miaosen Zheng, +6 authors, Yifei Liu.
Cancer Cell Int, 2021 Mar 04; 21(1). PMID: 33653340    Free PMC article.
An immune-related seven-lncRNA signature for head and neck squamous cell carcinoma.
Yue Chen, Tian-Qi Luo, +4 authors, Yan-Ping Mao.
Cancer Med, 2021 Mar 05; 10(7). PMID: 33660378    Free PMC article.
Remarkable response to pembrolizumab with platinum-doublet in PD-L1-low pulmonary sarcomatoid carcinoma: A case report.
Hirokazu Taniguchi, Shinnosuke Takemoto, +14 authors, Hiroshi Mukae.
Thorac Cancer, 2021 Feb 20; 12(7). PMID: 33605089    Free PMC article.
Elevated serum interleukin-8 is associated with enhanced intratumor neutrophils and reduced clinical benefit of immune-checkpoint inhibitors.
Kurt A Schalper, Michael Carleton, +18 authors, Ignacio Melero.
Nat Med, 2020 May 15; 26(5). PMID: 32405062    Free PMC article.
[Effect of Pembrolizumab on T Lymphocyte Subsets in Patients with Advanced 
Non-small Cell Lung Cancer and Its Therapeutic Effect].
Yun Wang, Yuyang Wang, +2 authors, Xiaochun Zhang.
Zhongguo Fei Ai Za Zhi, 2021 Apr 06; 24(3). PMID: 33819968    Free PMC article.
Elevated Pretreatment Fibrinogen-to-Lymphocyte Percentage Ratio Predict Tumor Staging and Poor Survival in Non-Small Cell Lung Cancer Patients with Chemotherapy or Surgery Combined with Chemotherapy.
Meifang Liu, Jie Yang, Lagen Wan, Rui Zhao.
Cancer Manag Res, 2021 Jul 01; 13. PMID: 34188545    Free PMC article.
Computational pathology reveals unique spatial patterns of immune response in H&E images from COVID-19 autopsies: preliminary findings.
Germán Corredor, Paula Toro, +10 authors, Anant Madabhushi.
J Med Imaging (Bellingham), 2021 Jul 17; 8(Suppl 1). PMID: 34268443    Free PMC article.
CD147 regulates antitumor CD8+ T-cell responses to facilitate tumor-immune escape.
Yatong Chen, Jing Xu, +10 authors, Zhi-Nan Chen.
Cell Mol Immunol, 2020 Nov 13; 18(8). PMID: 33177695    Free PMC article.
Cancer Immunotherapies: From Efficacy to Resistance Mechanisms - Not Only Checkpoint Matters.
Shuyue Wang, Kun Xie, Tengfei Liu.
Front Immunol, 2021 Aug 10; 12. PMID: 34367148    Free PMC article.
Review.
Nivolumab monotherapy or combination therapy with ipilimumab for lung cancer: a systemic review and meta-analysis.
Huihui Jiang, Aiqun Xu, +6 authors, Ran Wang.
Cancer Cell Int, 2021 Aug 16; 21(1). PMID: 34391428    Free PMC article.
Review.
High Counts of CD68+ and CD163+ Macrophages in Mantle Cell Lymphoma Are Associated With Inferior Prognosis.
Philippa Li, Ji Yuan, +7 authors, Zenggang Pan.
Front Oncol, 2021 Sep 17; 11. PMID: 34527580    Free PMC article.
Best Practices for Technical Reproducibility Assessment of Multiplex Immunofluorescence.
Caddie Laberiano-Fernández, Sharia Hernández-Ruiz, Frank Rojas, Edwin Roger Parra.
Front Mol Biosci, 2021 Sep 18; 8. PMID: 34532339    Free PMC article.
Review.
Single-cell RNA sequencing reveals distinct tumor microenvironmental patterns in lung adenocarcinoma.
Philip Bischoff, Alexandra Trinks, +17 authors, Frederick Klauschen.
Oncogene, 2021 Oct 20;. PMID: 34663877
Improved Immunotherapy Efficacy by Vascular Modulation.
Emma L Newport, Ana Rita Pedrosa, +2 authors, José M Muñoz-Félix.
Cancers (Basel), 2021 Oct 24; 13(20). PMID: 34680355    Free PMC article.
Review.
Clinical Efficacy and Future Prospects of Immunotherapy in Lung Cancer.
Tomonari Kinoshita, Hideki Terai, Tomonori Yaguchi.
Life (Basel), 2021 Oct 24; 11(10). PMID: 34685400    Free PMC article.
Review.
Spatially resolved analysis of the T cell immune contexture in lung cancer-associated brain metastases.
Benjamin Y Lu, Richa Gupta, +10 authors, Sarah B Goldberg.
J Immunother Cancer, 2021 Oct 22; 9(10). PMID: 34670827    Free PMC article.
Correlation between schistosomiasis and CD8+ T cell and stromal PD-L1 as well as the different prognostic role of CD8+ T cell and PD-L1 in schistosomal-associated colorectal cancer and non-schistosomal-associated colorectal cancer.
Weixia Wang, Hongyan Jing, +10 authors, Limei Wang.
World J Surg Oncol, 2021 Nov 09; 19(1). PMID: 34743724    Free PMC article.
Relationships of N6-Methyladenosine-Related Long Non-Coding RNAs With Tumor Immune Microenvironment and Clinical Prognosis in Lung Adenocarcinoma.
Jianhui Zhao, Xi Lin, Jinman Zhuang, Fei He.
Front Genet, 2021 Nov 16; 12. PMID: 34777460    Free PMC article.
Spatial Mapping and Immunomodulatory Role of the OX40/OX40L Pathway in Human Non-Small Cell Lung Cancer.
Angelo Porciuncula, Micaela Morgado, +5 authors, Kurt A Schalper.
Clin Cancer Res, 2021 Sep 15; 27(22). PMID: 34518312    Free PMC article.
Tumor cell PD-L1 expression is a strong predictor of unfavorable prognosis in immune checkpoint therapy-naive clear cell renal cell cancer.
Katharina Möller, Christoph Fraune, +20 authors, Till S Clauditz.
Int Urol Nephrol, 2021 Apr 03; 53(12). PMID: 33797012    Free PMC article.
Early lung carcinogenesis and tumor microenvironment observed by single-cell transcriptome analysis.
Eun Young Kim, Yoon Jin Cha, +5 authors, Yoon Soo Chang.
Transl Oncol, 2021 Nov 21; 15(1). PMID: 34800916    Free PMC article.