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Invited Review Articles

Immunoscore: a novel prognostic tool. Association with clinical outcome, response to treatment and survival in several malignancies

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Pages 432-443 | Received 28 Oct 2019, Accepted 11 Feb 2020, Published online: 16 Mar 2020

References

  • Galon J, Lugli A, Bifulco C, et al. World-Wide Immunoscore Task Force: meeting report from the “Melanoma Bridge”, Napoli, November 30th-December 3rd, 2016. J Transl Med. 2017;15:212.
  • Galon J, Mlecnik B, Bindea G, et al. Towards the introduction of the ‘Immunoscore’ in the classification of malignant tumors. J Pathol. 2014;232:199–209.
  • Guo G, Wang Y, Zhou Y, et al. Immune cell concentrations among the primary tumor microenvironment in colon cancer patients predicted by clinicopathologic characteristics and blood indexes. J Immunother Cancer. 2019;7:179.
  • McCarty WC. Principles of prognosis in cancer. JAMA. 1931;96:30–33.
  • Shankaran V, Ikeda H, Bruce AT, et al. IFN-gamma and lymphocytes prevent primary tumor development and shape tumor immunogenicity. Nature. 2001;410:1107–1111.
  • Fridman WH, Pages F, Sautes-Fridman C, et al. The immune contexture in human tumors: impact on clinical outcome. Nat Rev Cancer. 2012;12:298–306.
  • Pagès F, Kirilovsky A, Mlecnik B, et al. In situ cytotoxic and memory T cells predict outcome in patients with early-stage colon cancer. JCO. 2009;27:5944–5951.
  • Clemente CG, Mihm MC Jr, Bufalino R, et al. Prognostic value of tumor infiltrating lymphocytes in the vertical growth phase of primary cutaneous melanoma. Cancer. 1996;77:1303–1310.
  • Dieu-Nosjean MC, Antoine M, Danel C, et al. Long-term survival for patients with non-small-cell lung cancer with intratumoral lymphoid structures. J Clin Oncol. 2008;26:4410–4417.
  • Tahkola K, Mecklin JP, Wirta EV, et al. High immune cell score predicts improved survival in pancreatic cancer. Virchows Arch. 2018;472:653–665.
  • Yao W, He JC, Yang Y, et al. The prognostic value of tumor-infiltrating lymphocytes in hepatocellular carcinoma: a systematic review and meta-analysis. Sci Rep. 2017;7:7525.
  • Ali HR, Provenzano E, Dawson SJ, et al. Association between CD8+ T-cell infiltration and breast cancer survival in 12,439 patients. Ann Oncol. 2014;25:1536–1543.
  • 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. 2016;5:e1057388.
  • Geng Y, Shao Y, He W, et al. Prognostic role of tumor-infiltrating lymphocytes in lung cancer: a meta-analysis. Cell Physiol Biochem. 2015;37:1560–1571.
  • Galon J, Costes A, Sanchez-Cabo F, et al. Type, density, and location of immune cells within human colon tumors predict clinical outcome. Science. 2006;313:1960–1964.
  • Galon J, Pagès F, Marincola FM, et al. Cancer classification using the Immunoscore: a worldwide task force. J Transl Med. 2012;10:205.
  • Pagès F, Mlecnik B, Marliot F, et al. International validation of the consensus Immunoscore for the classification of colon cancer: a prognostic and accuracy study. Lancet. 2018;391:2128–2139.
  • Wang Y, Lin HC, Huang MY, et al. The immunoscore system predicts prognosis after liver metastasectomy in colon cancer liver metastases. Cancer Immunol Immunother. 2018;67:435–444.
  • Viganò L, Capussotti L, Lapointe R, et al. Early recurrence after liver resection for colon metastases: Risk factors, prognosis, and treatment. A LiverMetSurvey-based study of 6,025 patients. Ann Surg Oncol. 2014;21:1276–1286.
  • Pagès F, Berger A, Camus M, et al. Effector memory T cells, early metastasis, and survival in colon cancer. N Engl J Med. 2005;353:2654–2666.
  • Mlecnik B, Tosolini M, Kirilovsky A, et al. Histopathologic-based prognostic factors of colon cancers are associated with the state of the local immune reaction. JCO. 2011;29:610–618.
  • Mlecnik B, Van den Eynde M, Bindea G, et al. Comprehensive intrametastatic immune quantification and major impact of Immunoscore on survival. J Natl Cancer Inst. 2018. DOI:10.1093/jnci/djx123.
  • Piras F, Colombari R, Minerba L, et al. The predictive value of CD8, CD4, CD68, and human leukocyte antigen-D-related cells in the prognosis of cutaneous malignant melanoma with vertical growth phase. Cancer. 2005;104:1246–1254.
  • Erdag G, Schaefer JT, Smolkin ME, et al. Immunotype and immunohistologic characteristics of tumor-infiltrating immune cells are associated with clinical outcome in metastatic melanoma. Cancer Res. 2012;72:1070–1080.
  • Tarhini AA, Edington H, Butterfield LH, et al. Immune monitoring of the circulation and the tumor microenvironment in patients with regionally advanced melanoma receiving neoadjuvant ipilimumab. PLoS One. 2014;9:e87705.
  • Tietze JK, Angelova D, Heppt MV, et al. The proportion of circulating CD45RO+CD8+ memory T cells is correlated with clinical response in melanoma patients treated with ipilimumab. Eur J Cancer. 2017;75:268–279.
  • Hiraoka K, Miyamoto M, Cho Y, et al. Concurrent infiltration by CD8+ T cells and CD4+ T cells is a favourable prognostic factor in non-small-cell lung carcinoma. Br J Cancer. 2006;94:275–280.
  • Paulsen EE, Kilvaer T, Khanehkenari MR, et al. CD45RO(+) Memory T lymphocytes-a candidate marker for TNM-Immunoscore in squamous non-small cell lung cancer. Neoplasia. 2015;17:839–848.
  • Tang Y, Xu X, Guo S, et al. An increased abundance of tumor-infiltrating regulatory T cells is correlated with the progression and prognosis of pancreatic ductal adenocarcinoma. PLoS One. 2014;9:e91551.
  • Sun C, Xu J, Song J, et al. The predictive value of centre tumour CD8+ T cells in patients with hepatocellular carcinoma: comparison with Immunoscore. Oncotarget. 2015;6:35602–35615.
  • Gabrielson A, Wu Y, Wang H, et al. Intratumoral CD3 and CD8 T-cell densities associated with relapse-free survival in HCC. Cancer Immunol Res. 2016;4:419–430.
  • Schoenberg MB, Hao J, Bucher JN, et al. Perivascular tumor-infiltrating leukocyte scoring for prognosis of resected hepatocellular carcinoma patients. Cancers (Basel). 2018;10:389.
  • Ding W, Xu X, Qian Y, et al. Prognostic value of tumor-infiltrating lymphocytes in hepatocellular carcinoma: A meta-analysis. Medicine (Baltimore). 2018;97:e13301.
  • Adams S, Gray RJ, Demaria S, et al. Prognostic value of tumor-infiltrating lymphocytes in triple-negative breast cancers from two phase III randomized adjuvant breast cancer trials: ECOG 2197 and ECOG 1199. J Clin Oncol. 2014;32:2959–2966.
  • Xu Y, Lan S, Zheng Q. Prognostic significance of infiltrating immune cell subtypes in invasive ductal carcinoma of the breast. Tumori. 2018;104:196–201.
  • Farsaci B, Donahue RN, Grenga I, et al. Analyses of pretherapy peripheral Immunoscore and response to vaccine therapy. Cancer Immunol Res. 2016;4:755–765.
  • Balch CM, Soong SJ, Murad TM, Ingalls AL, Madox WA. A multifactorial analysis of melanoma: II. Prognostic factors in patients with stage I (localized) melanoma. Surgery. 1979;86:343–351.
  • Day CL Jr, Mihm MC Jr, Lew RA, et al. Prognostic factors for patients with clinical stage I melanoma of intermediate thickness (1.51-3.99 mm). A conceptual model for tumor growth and metastasis. Ann Surg. 1982;195:35–43.
  • Elder DE, Guerry D 4th, VanHorn M, et al. The role of lymph node dissection for clinical stage I malignant melanoma of intermediate thickness (1.51-3.99 mm). Cancer. 1985;56:413–418.
  • Hotta K, Sho M, Fujimoto K, et al. Prognostic significance of CD45RO + memory T cells in renal cell carcinoma. Br J Cancer. 2011;105:1191–1196.
  • Hodi FS, O'Day SJ, McDermott DF, et al. Improved survival with ipilimumab in patients with metastatic melanoma. N Engl J Med. 2010;363:711–723.
  • Music M, Prassas I, Diamandis EP. Optimizing cancer immunotherapy: Is it time for personalized predictive biomarkers?. Crit Rev Clin Lab Sci. 2018;55:466–479.
  • Galon J, Fox BA, Bifulco CB, et al. Immunoscore and immunoprofiling in cancer: an update from the melanoma and immunotherapy bridge 2015. J Transl Med. 2016;14:273–278.
  • Mozzillo N, Caracò C, Marone U, et al. Superficial and deep lymph node dissection for stage III cutaneous melanoma: clinical outcome and prognostic factors. World J Surg Onc. 2013;11:36.
  • Siegel RL, Miller KD, Jemal A. Cancer statistics, 2019. CA A Cancer J Clin. 2019;69:7–34.
  • Duan MC, Zhong XN, Liu GN, et al. The Treg/Th17 paradigm in lung cancer. J Immunol Res. 2014;2014:1–9.
  • Bremnes RM, Busund LT, Kilvaer TL, et al. The role of tumor-infiltrating lymphocytes in development, progression, and prognosis of non-small cell lung cancer. J Thorac Oncol. 2016;11:789–800.
  • Donnem T, Hald SM, Paulsen EE, et al. Stromal CD8+ T-cell density - a promising supplement to TNM staging in non-small cell lung cancer. Clin Cancer Res. 2015;21:2635–2643.
  • Li D, Xie K, Wolff R, et al. Pancreatic cancer. Lancet. 2004;363:1049–1057.
  • Seppanen H, Juuti A, Mustonen H, et al. The results of pancreatic resections and long-term survival for pancreatic ductal adenocarcinoma: a single institution experience. Scand J Surg. 2017;106:54–61.
  • Petrizzo A, Buonaguro L. Application of the Immunoscore as prognostic tool for hepatocellular carcinoma. J Immunother Cancer. 2016;4:71.
  • Taube JM, Galon J, Sholl LM, et al. Implications of the tumor immune microenvironment for staging and therapeutics. Mod Pathol. 2018;31:214–234.
  • Criscitiello C, Esposito A, Trapani D, et al. Prognostic and predictive value of tumor infiltrating lymphocytes in early breast cancer. Cancer Treat Rev. 2016;50:205–207.
  • Yu X, Zhang Z, Wang Z, et al. Prognostic and predictive value of tumor-infiltrating lymphocytes in breast cancer: a systematic review and meta-analysis. Clin Transl Oncol. 2016;18:497–506.
  • Zitvogel L, Apetoh L, Ghiringhelli F, et al. Immunological aspects of cancer chemotherapy. Nat Rev Immunol. 2008;8:59–73.
  • Sperduto PW, Berkey B, Gaspar LE, et al. A new prognostic index and comparison to three other indices for patients with brain metastases: an analysis of 1,960 patients in the RTOG database. Int J Radiat Oncol Biol Phys. 2008;70:510–514.
  • Berghoff AS, Kiesel B, Widhalm G, et al. Programmed death ligand 1 expression and tumor-infiltrating lymphocytes in glioblastoma. Neuro Oncol. 2015;17:1064–1075.

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