Evaluating the prognostic significance of tumor-infiltrating lymphocytes in solid tumor: practice of a standardized method from the International Immuno-Oncology Biomarkers Working Group

References

• Bray F, Ferlay J, Soerjomataram I, Siegel RL, Torre LA, Jemal A. Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin. 2018;68(6):394–424. doi:10.3322/caac.2149230207593
   PubMed Web of Science ®Google Scholar
• Noh SH, Park SR, Yang HK, et al. Adjuvant capecitabine plus oxaliplatin for gastric cancer after D2 gastrectomy (CLASSIC): 5-year follow-up of an open-label, randomised phase 3 trial. Lancet Oncol. 2014;15(12):1389–1396. doi:10.1016/S1470-2045(14)70473-525439693
   PubMed Web of Science ®Google Scholar
• Bang YJ, Kim YW, Yang HK, et al. Adjuvant capecitabine and oxaliplatin for gastric cancer after D2 gastrectomy (CLASSIC): a phase 3 open-label, randomised controlled trial. Lancet. 2012;379(9813):315–321. doi:10.1016/S0140-6736(11)61873-422226517
   PubMed Web of Science ®Google Scholar
• Peng C, Liu J, Yang G, Li Y. The tumor-stromal ratio as a strong prognosticator for advanced gastric cancer patients: proposal of a new TSNM staging system. J Gastroenterol. 2018;53(5):606–617. doi:10.1007/s00535-017-1379-128815347
   PubMed Web of Science ®Google Scholar
• Mlecnik B, Tosolini M, Kirilovsky A, et al. Histopathologic-based prognostic factors of colorectal cancers are associated with the state of the local immune reaction. J Clin Oncol. 2011;29(6):610–618. doi:10.1200/JCO.2010.30.542521245428
   PubMed Web of Science ®Google Scholar
• Galon J, Mlecnik B, Bindea G, et al. Towards the introduction of the ‘Immunoscore’ in the classification of malignant tumours. J Pathol. 2014;232(2):199–209. doi:10.1002/path.428724122236
   PubMed Web of Science ®Google Scholar
• Saito T, Nishikawa H, Wada H, et al. Two FOXP3(+)CD4(+) T cell subpopulations distinctly control the prognosis of colorectal cancers. Nat Med. 2016;22(6):679–684. doi:10.1038/nm.408627111280
   PubMed Web of Science ®Google Scholar
• Brambilla E, Le Teuff G, Marguet S, et al. Prognostic effect of tumor lymphocytic infiltration in resectable non-small-cell lung cancer. J Clin Oncol. 2016;34(11):1223–1230. doi:10.1200/JCO.2015.63.097026834066
   PubMed Web of Science ®Google Scholar
• Ward MJ, Thirdborough SM, Mellows T, et al. Tumour-infiltrating lymphocytes predict for outcome in HPV-positive oropharyngeal cancer. Br J Cancer. 2014;110(2):489–500. doi:10.1038/bjc.2013.63924169344
   PubMed Web of Science ®Google Scholar
• Perez EA, Ballman KV, Tenner KS, et al. Association of stromal tumor-infiltrating lymphocytes with recurrence-free survival in the N9831 adjuvant trial in patients with early-stage Her2-positive breast cancer. JAMA Oncol. 2016;2(1):56–64. doi:10.1001/jamaoncol.2015.323926469139
   PubMed Web of Science ®Google Scholar
• Swisher SK, Wu Y, Castaneda CA, et al. Interobserver agreement between pathologists assessing tumor-infiltrating lymphocytes (TILs) in breast cancer using methodology proposed by the International TILs Working Group. Ann Surg Oncol. 2016;23(7):2242–2248. doi:10.1245/s10434-016-5173-826965699
   PubMed Web of Science ®Google Scholar
• Salgado R, Denkert C, Demaria S, et al. The evaluation of tumor-infiltrating lymphocytes (TILs) in breast cancer: recommendations by an International TILs Working Group 2014. Ann Oncol. 2015;26(2):259–271. doi:10.1093/annonc/mdu45025214542
   PubMed Web of Science ®Google Scholar
• Dieci MV, Radosevic-Robin N, Fineberg S, et al. Update on tumor-infiltrating lymphocytes (TILs) in breast cancer, including recommendations to assess TILs in residual disease after neoadjuvant therapy and in carcinoma in situ: a report of the International Immuno-Oncology Biomarker Working Group on Breast Cancer. Semin Cancer Biol. 2018;52(Pt 2):16–25. doi:10.1016/j.semcancer.2017.10.00329024776
   PubMed Web of Science ®Google Scholar
• Hendry S, Salgado R, Gevaert T, et al. 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. Adv Anat Pathol. 2017;24(6):311–335. doi:10.1097/PAP.000000000000016128777143
   PubMed Web of Science ®Google Scholar
• Kang BW, Kim JG, Lee IH, Bae HI, Seo AN. Clinical significance of tumor-infiltrating lymphocytes for gastric cancer in the era of immunology. World J Gastrointest Oncol. 2017;9(7):293–299. doi:10.4251/wjgo.v9.i7.29328808502
   PubMed Web of Science ®Google Scholar
• Harris LN, Ismaila N, McShane LM, et al. Use of biomarkers to guide decisions on adjuvant systemic therapy for women with early-stage invasive breast cancer: American society of clinical oncology clinical practice guideline. J Clin Oncol. 2016;34(10):1134–1150. doi:10.1200/JCO.2015.65.228926858339
   PubMed Web of Science ®Google Scholar
• Jiang D, Liu Y, Wang H, et al. Tumour infiltrating lymphocytes correlate with improved survival in patients with esophageal squamous cell carcinoma. Sci Rep. 2017;7:44823. doi:10.1038/srep4482328322245
   PubMed Web of Science ®Google Scholar
• Pruneri G, Vingiani A, Bagnardi V, et al. Clinical validity of tumor-infiltrating lymphocytes analysis in patients with triple-negative breast cancer. Ann Oncol. 2016;27(2):249–256. doi:10.1093/annonc/mdv57126598540
   PubMed Web of Science ®Google Scholar
• Savas P, Salgado R, Denkert C, et al. Clinical relevance of host immunity in breast cancer: from TILs to the clinic. Nat Rev Clin Oncol. 2016;13(4):228–241. doi:10.1038/nrclinonc.2015.21526667975
   PubMed Web of Science ®Google Scholar
• Berghoff AS, Fuchs E, Ricken G, et al. Density of tumor-infiltrating lymphocytes correlates with extent of brain edema and overall survival time in patients with brain metastases. Oncoimmunology. 2015;5(1):e1057388. doi:10.1080/2162402X.2015.105738826942067
   PubMed Web of Science ®Google Scholar
• Gu-Trantien C, Loi S, Garaud S, et al. CD4(+) follicular helper T cell infiltration predicts breast cancer survival. J Clin Invest. 2013;123(7):2873–2892. doi:10.1172/JCI6742823778140
   PubMed Web of Science ®Google Scholar
• Brown JR, Wimberly H, Lannin DR, Nixon C, Rimm DL, Bossuyt V. Multiplexed quantitative analysis of CD3, CD8, and CD20 predicts response to neoadjuvant chemotherapy in breast cancer. Clin Cancer Res. 2014;20(23):5995–6005. doi:10.1158/1078-0432.CCR-14-162225255793
   PubMed Web of Science ®Google Scholar
• Liu JY, Yuan JP, Geng XF, Qu AP, Li Y. Morphological study and comprehensive cellular constituents of milky spots in the human omentum. Int J Clin Exp Pathol. 2015;8(10):12877–12884.26722479
   PubMed Web of Science ®Google Scholar
• Yu X, Zhang Z, Wang Z, Wu P, Qiu F, Huang J. Prognostic and predictive value of tumor-infiltrating lymphocytes in breast cancer: a systematic review and meta-analysis. Clin Transl Oncol. 2016;18(5):497–506. doi:10.1007/s12094-015-1391-y26459255
   PubMed Web of Science ®Google Scholar
• Dieci MV, Criscitiello C, Goubar A, et al. Prognostic value of tumor-infiltrating lymphocytes on residual disease after primary chemotherapy for triple-negative breast cancer: a retrospective multicenter study. Ann Oncol. 2014;25(3):611–618. doi:10.1093/annonc/mdt55624401929
   PubMed Web of Science ®Google Scholar
• Loi S, Michiels S, Salgado R, et al. Tumor infiltrating lymphocytes are prognostic in triple negative breast cancer and predictive for trastuzumab benefit in early breast cancer: results from the FinHER trial. Ann Oncol. 2014;25(8):1544–1550. doi:10.1093/annonc/mdu11224608200
   PubMed Web of Science ®Google Scholar
• Luen SJ, Salgado R, Fox S, et al. Tumour-infiltrating lymphocytes in advanced HER2-positive breast cancer treated with pertuzumab or placebo in addition to trastuzumab and docetaxel: a retrospective analysis of the CLEOPATRA study. Lancet Oncol. 2017;18(1):52–62. doi:10.1016/S1470-2045(16)30631-327964843
   PubMed Web of Science ®Google Scholar
• Wein L, Savas P, Luen SJ, Virassamy B, Salgado R, Loi S. Clinical validity and utility of tumor-infiltrating lymphocytes in routine clinical practice for breast cancer patients: current and future directions. Front Oncol. 2017;7:156. doi:10.3389/fonc.2017.0015628824872
   PubMed Web of Science ®Google Scholar
• Luen SJ, Savas P, Fox SB, Salgado R, Loi S. Tumour-infiltrating lymphocytes and the emerging role of immunotherapy in breast cancer. Pathology. 2017;49(2):141–155. doi:10.1016/j.pathol.2016.10.01028049579
   PubMed Web of Science ®Google Scholar
• Denkert C, von Minckwitz G, Darb-Esfahani S, et al. Tumour-infiltrating lymphocytes and prognosis in different subtypes of breast cancer: a pooled analysis of 3771 patients treated with neoadjuvant therapy. Lancet Oncol. 2018;19(1):40–50. doi:10.1016/S1470-2045(17)30904-X29233559
   PubMed Web of Science ®Google Scholar
• Zheng X, Song X, Shao Y, et al. Prognostic role of tumor-infiltrating lymphocytes in gastric cancer: a meta-analysis. Oncotarget. 2017;8(34):57386–57398. doi:10.18632/oncotarget.1806528915679
   PubMedGoogle Scholar
• Kim KJ, Lee KS, Cho HJ, et al. Prognostic implications of tumor-infiltrating FoxP3+regulatory T cells and CD8+cytotoxic T cells in microsatellite-unstable gastric cancers. Hum Pathol. 2014;45(2):285–293. doi:10.1016/j.humpath.2013.09.00424331841
   PubMed Web of Science ®Google Scholar
• Wang B, Xu DZ, Yu X, et al. Association of intra-tumoral infiltrating macrophages and regulatory t cells is an independent prognostic factor in gastric cancer after radical resection. Ann Surg Oncol. 2011;18(9):2585–2593. doi:10.1245/s10434-011-1609-321347781
   PubMed Web of Science ®Google Scholar
• Kawazoe A, Kuwata T, Kuboki Y, et al. Clinicopathological features of programmed death ligand 1 expression with tumor-infiltrating lymphocyte, mismatch repair, and Epstein-Barr virus status in a large cohort of gastric cancer patients. Gastric Cancer. 2017;20(3):407–415. doi:10.1007/s10120-016-0631-327629881
   PubMed Web of Science ®Google Scholar
• Solinas C, Pusole G, Demurtas L, et al. Tumor infiltrating lymphocytes in gastrointestinal tumors: controversies and future clinical implications. Crit Rev Oncol Hematol. 2017;110:106–116. doi:10.1016/j.critrevonc.2016.11.01628109400
   PubMed Web of Science ®Google Scholar
• Horne ZD, Jack R, Gray ZT, et al. Increased levels of tumor-infiltrating lymphocytes are associated with improved recurrence-free survival in stage 1A non-small-cell lung cancer. J Surg Res. 2011;171(1):1–5. doi:10.1016/j.jss.2011.03.06821571304
   PubMed Web of Science ®Google Scholar
• Feng W, Li Y, Shen L, et al. Prognostic value of tumor-infiltrating lymphocytes for patients with completely resected stage IIIA(N2) non-small cell lung cancer. Oncotarget. 2016;7(6):7227–7240. doi:10.18632/oncotarget.697926811495
   PubMedGoogle Scholar
• Schreiber RD, Old LJ, Smyth MJ. Cancer immunoediting: integrating immunity’s roles in cancer suppression and promotion. Science. 2011;331(6024):1565–1570. doi:10.1126/science.120348621436444
   PubMed Web of Science ®Google Scholar
• Cancer Genome Atlas Research Network. Comprehensive molecular characterization of gastric adenocarcinoma. Nature. 2014;513(7517):202–209. doi:10.1038/nature1348025079317
   PubMed Web of Science ®Google Scholar
• Nagase H, Takeoka T, Urakawa S, et al. ICOS+ Foxp3(+) TILs in gastric cancer are prognostic markers and effector regulatory T cells associated with Helicobacter pylori. Int J Cancer. 2017;140(3):686–695. doi:10.1002/ijc.3047527756099
   PubMed Web of Science ®Google Scholar