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Review

Recent advances of immunotherapy for biliary tract cancer

ORCID Icon, &
Pages 527-536 | Received 14 Oct 2020, Accepted 17 Nov 2020, Published online: 08 Jan 2021

References

  • Rizvi S, Gores GJ. Pathogenesis, diagnosis, and management of cholangiocarcinoma. Gastroenterology. 2013;145(6):1215‐1229.
  • Razumilava N, Gores GJ. Cholangiocarcinoma. Lancet. 2014;383(9935):2168–2179.
  • Rizvi S, Khan SA, Hallemeier CL, et al. Cholangiocarcinoma ‐ evolving concepts and therapeutic strategies. Nat Rev Clin Oncol. 2018;15(2):95‐111.
  • Banales JM, Cardinale V, Carpino G, et al. Expert consensus document: cholangiocarcinoma: current knowledge and future perspectives consensus statement from the European network for the study of cholangiocarcinoma (ENS-CCA). Nat Rev Gastroenterol Hepatol. 2016;13(5):261–280.
  • Rizzo A, Ricci AD, Tober N, et al. Second-line treatment in advanced biliary tract cancer: today and tomorrow. Anticancer Res. 2020;40(6):3013–3030.
  • Forner A, Vidili G, Rengo M, et al. Clinical presentation, diagnosis and staging of cholangiocarcinoma. Liver Int. 2019;39(Suppl 1):98–107.
  • Saha SK, Zhu AX, Fuchs CS. Brooks GA: forty-year trends in cholangiocarcinoma incidence in the US: intrahepatic disease on the rise. Oncologist. 2016;21:594–599.
  • Bridgewater JA, Goodman KA, Kalyan A, et al. Biliary tract cancer: epidemiology, radiotherapy, and molecular profiling. Am Soc Clin Oncol Educ Book. 2016;35:e194–203.
  • Banales JM, Marin JJG, Lamarca A, et al. Cholangiocarcinoma 2020: the next horizon in mechanisms and management. Nat Rev Gastroenterol Hepatol. 2020. DOI:10.1038/s41575-020-0310-z
  • Morizane C, Ueno M, Ikeda M, et al. New developments in systemic therapy for advanced biliary tract cancer. Jpn J Clin Oncol. 2018;48(8):703–711.
  • Brandi G, Rizzo A, Dall’Olio FG, et al. Percutaneous radiofrequency ablation in intrahepatic cholangiocarcinoma: a retrospective single-center experience. Int J Hyperthermia. 2020;37:479–485.
  • Kelley RK, Bridgewater J, Gores GJ, et al. Systemic therapies for intrahepatic cholangiocarcinoma. J Hepatol. 2020;72(2):353–363.
  • Zhao DY, Lim KH. Current biologics for treatment of biliary tract cancer. J Gastrointest Oncol. 2017;8(3):430–440.
  • Shroff RT, Kennedy EB, Bachini M, et al. Adjuvant therapy for resected biliary tract cancer: ASCO clinical practice guideline. J Clin Oncol. 2019;37(12):1015–1027.
  • Edeline J, Benabdelghani M, Bertaut A, et al. Gemcitabine and oxaliplatin chemotherapy or surveillance in resected biliary tract cancer (PRODIGE 12-ACCORD 18-UNICANCER GI): a randomized phase III study. J Clin Oncol. 2019;37(8):658–667.
  • Primrose JN, Fox RP, Palmer DH, et al. Capecitabine compared with observation in resected biliary tract cancer (BILCAP): a randomised, controlled, multicentre, phase 3 study. Lancet Oncol. 2019;20(5):663–673.
  • Tariq NU, McNamara MG, Valle JW. Biliary tract cancers: current knowledge, clinical candidates and future challenges. Cancer Manag Res. 2019;11:2623–2642.
  • Valle J, Wasan H, Palmer DH, et al. ABC-02 Trial Investigators. Cisplatin plus gemcitabine versus gemcitabine for biliary tract cancer. N Engl J Med. 2010;362:1273–1281.
  • Okusaka T, Nakachi K, Fukutomi A, et al. Gemcitabine alone or in combination with cisplatin in patients with biliary tract cancer: a comparative multicentre study in Japan. Br J Cancer. 2010;103:469–474.
  • Valle JW, Lamarca A, Goyal L, et al. New horizons for precision medicine in biliary tract cancers. Cancer Discov. 2017;10:8290.
  • Abou-Alfa GK, Macarulla T, Javle MM, et al. Ivosidenib in IDH1-mutant, chemotherapy-refractory cholangiocarcinoma (ClarIDHy): a multicentre, randomised, double-blind, placebo-controlled, phase 3 study. Lancet Oncol. 2020;21(6):796–807.
  • Rizzo A, Frega G, Ricci AD, et al. Anti-EGFR monoclonal antibodies in advanced biliary tract cancer: a systematic review and meta-analysis. Vivo. 2020 Mar–Apr;34(2):479–488.
  • Abou-Alfa GK, Sahai V, Hollebecque A, et al. Pemigatinib for previously treated, locally advanced or metastatic cholangiocarcinoma: a multicentre, open-label, phase 2 study. Lancet Oncol. 2020;pii: S1470-2045(20)30109–1.
  • Massa A, Varamo C, Vita F, et al. Evolution of the experimental models of cholangiocarcinoma. Cancers (Basel). 2020;12:2308.
  • Lamarca A, Barriuso J, McNamara MG, et al. Molecular targeted therapies: ready for “prime time” in biliary tract cancer. J Hepatol. 2020;73(1):170–185.
  • Krook MA, Lenyo A, Wilberding M, et al. Efficacy of FGFR inhibitors and combination therapies for acquired resistance in FGFR2-fusion cholangiocarcinoma. Mol Cancer Ther. 2020;19(3):847–857.
  • Athauda A, Fong C, Lau DK, et al. Broadening the therapeutic horizon of advanced biliary tract cancer through molecular characterisation. Cancer Treat Rev. 2020;86:101998.
  • Santoni M, Massari F, Di Nunno V, et al. Immunotherapy in renal cell carcinoma: latest evidence and clinical implications. Drugs Context. 2018;7:212528.
  • Mollica V, Rizzo A, Montironi R, et al. Current strategies and novel therapeutic approaches for metastatic urothelial carcinoma. Cancers (Basel). 2020;12(6):E1449.
  • Robert C, Long GV, Brady B, et al. Nivolumab in previously untreated melanoma without BRAF mutation. N Engl J Med. 2015;372:320–330.
  • Rosenberg JE, Hoffman-Censits J, Powles T, et al. Atezolizumab in patients with locally advanced and metastatic urothelial carcinoma who have progressed following treatment with platinum-based chemotherapy: a single-arm, multicentre, phase 2 trial. Lancet. 2016;7:1909–1920.
  • Borghaei H, Paz-Ares L, Horn L, et al. Nivolumab versus docetaxel in advanced nonsquamous non-small-cell lung cancer. N Engl J Med. 2015;373:1627–1639.
  • Lemery S, Keegan P, Pazdur R. First FDA approval agnostic of cancer site - when a biomarker defines the indication. N Engl J Med. 2017 Oct 12;377(15):1409–1412.
  • Mizrahi JD, Shroff RT. New treatment options for advanced biliary tract cancer. Curr Treat Options Oncol. 2020;21(8):63.
  • Sirica AE, Gores GJ, Groopman JD, et al. Intrahepatic cholangiocarcinoma: continuing challenges and translational advances. Hepatology. 2019;69(4):1803–1815.
  • Rizzo A, Ricci AD, Tavolari S, et al. Circulating tumor DNA in biliary tract cancer: current evidence and future perspectives. Cancer Genomics Proteomics. 2020;17(5):441–452.
  • Fostea RM, Fontana E, Torga G, et al. Recent progress in the systemic treatment of advanced/metastatic cholangiocarcinoma. Cancers (Basel). 2020 Sept 11;12(9):E2599.
  • Marcus L, Lemery SJ, Keegan P, et al. FDA approval summary: pembrolizumab for the treatment of microsatellite instability-high solid tumors. Clin Cancer Res. 2019 July 1;25(13):3753–3758.
  • Marabelle A, Fakih M, Lopez J, et al. Association of tumour mutational burden with outcomes in patients with advanced solid tumours treated with pembrolizumab: prospective biomarker analysis of the multicohort, open-label, phase 2 KEYNOTE-158 study. Lancet Oncol. 2020 Oct;21(10):1353–1365.
  • Piha-Paul SA, Oh DY, Ueno M, et al. Efficacy and safety of pembrolizumab for the treatment of advanced biliary cancer: results from the KEYNOTE-158 and KEYNOTE-028 studies. Int J Cancer. 2020 Oct 15;147(8):2190–2198.
  • Kim RD, Chung V, Alese OB, et al. A phase 2 multi-institutional study of nivolumab for patients with advanced refractory biliary tract cancer. JAMA Oncol. 2020 June 1;6(6):888–894.
  • Ueno M, Ikeda M, Morizane C, et al. Nivolumab alone or in combination with cisplatin plus gemcitabine in Japanese patients with unresectable or recurrent biliary tract cancer: a non-randomised, multicentre, open-label, phase 1 study. Lancet Gastroenterol Hepatol. 2019 Aug;4(8):611–621.
  • Ioka T, Ueno M, Oh DY, et al. Evaluation of safety and tolerability of durvalumab (D) with or without tremelimumab (T) in patients (pts) with biliary tract cancer (BTC). J Clin Oncol. 2019;37:387.
  • Teicher BA. TGFβ-directed therapeutics: 2020. Pharmacol Ther. 2020 Aug;21:107666.
  • Yoo C, Oh DY, Choi HJ, et al. Phase I study of bintrafusp alfa, a bifunctional fusion protein targeting TGF-β and PD-L1, in patients with pretreated biliary tract cancer. J Immunother Cancer. 2020 May;8(1):e000564.
  • Song X, Hu Y, Li Y, et al. Overview of current targeted therapy in gallbladder cancer. Signal Transduct Target Ther. 2020 Oct 7;5(1):230.
  • Buchbinder EI, Desai A. CTLA-4 and PD-1 pathways: similarities, differences, and implications of their inhibition. Am J Clin Oncol. 2016 Feb;39(1):98–106.
  • Rotte A. Combination of CTLA-4 and PD-1 blockers for treatment of cancer. J Exp Clin Cancer Res. 2019 June 13;38(1):255.
  • Lee HT, Lee SH, Heo YS. Molecular interactions of antibody drugs targeting PD-1, PD-L1, and CTLA-4 in immuno-oncology. Molecules. 2019 Mar 26;24(6):1190.
  • Rowshanravan B, Halliday N, Sansom DM. CTLA-4: a moving target in immunotherapy. Blood. 2018 Jan 4;131(1):58–67.
  • Kelley RK, Mitchell E, Behr S, et al. Phase II trial of pembrolizumab (PEM) plus granulocyte macrophage colony stimulating factor (GM-CSF) in advanced biliary cancers (ABC). JCO. 2018;36:386.
  • Klein O, Kee D, Nagrial A, et al. Evaluation of combination nivolumab and ipilimumab immunotherapy in patients with advanced biliary tract cancers: subgroup analysis of a phase 2 nonrandomized clinical trial. JAMA Oncol. 2020;30:e202814.
  • Uprety D. Chemo-immunotherapy: the beginning of a new era in lung cancer. Clin Lung Cancer. 2019 Mar;20(2):63–65.
  • Shafique M, Tanvetyanon T. Immunotherapy alone or chemo-immunotherapy as front-line treatment for advanced non-small cell lung cancer. Expert Opin Biol Ther. 2019 Mar;19(3):225–232.
  • Rassy E, Flippot R, Albiges L. Tyrosine kinase inhibitors and immunotherapy combinations in renal cell carcinoma. Ther Adv Med Oncol. 2020 Mar;18(12):1758835920907504.
  • Mossenta M, Busato D, Baboci L, et al. New insight into therapies targeting angiogenesis in hepatocellular carcinoma. Cancers (Basel). 2019 July 31;11(8):1086.
  • Kwilas AR, Ardiani A, Donahue RN, et al. Dual effects of a targeted small-molecule inhibitor (cabozantinib) on immune-mediated killing of tumor cells and immune tumor microenvironment permissiveness when combined with a cancer vaccine. J Transl Med. 2014 Nov;13(12):294.
  • Wang Y, Jiang M, Zhu J, et al. The safety and efficacy of lenvatinib combined with immune checkpoint inhibitors therapy for advanced hepatocellular carcinoma. Biomed Pharmacother. 2020 Oct;14(132):110797.
  • Lin J, Yang X, Long J, et al. Pembrolizumab combined with lenvatinib as non-first-line therapy in patients with refractory biliary tract carcinoma. Hepatobiliary Surg Nutr. 2020 Aug;9(4):414–424.
  • Arkenau HT, Martin-Liberal J, Calvo E, et al. Ramucirumab plus pembrolizumab in patients with previously treated advanced or metastatic biliary tract cancer: nonrandomized, open-label, phase I trial (JVDF). Oncologist. 2018;23:1407–e136.
  • Rizzo A, Mollica V, Cimadamore A, et al. Is there a role for immunotherapy in prostate cancer? Cells. 2020 Sept 8;9(9):E2051.
  • Arora S, Velichinskii R, Lesh RW, et al. Existing and emerging biomarkers for immune checkpoint immunotherapy in solid tumors. Adv Ther. 2019 Oct;36(10):2638–2678.
  • Reisländer T, Groelly FJ, Tarsounas M. DNA damage and cancer immunotherapy: a STING in the tale. Mol Cell. 2020 Oct 1;80(1):21–28.
  • Chakrabarti S, Kamgar M, Mahipal A. Targeted therapies in advanced biliary tract cancer: an evolving paradigm. Cancers (Basel). 2020 July 24;12(8):2039.
  • Ricci AD, Rizzo A, Brandi G. Immunotherapy in biliary tract cancer: worthy of a second look. Cancer Control. 2020 July–Aug;27(3):1073274820948047.
  • Mouw KW, Goldberg MS, Konstantinopoulos PA, et al. DNA damage and repair biomarkers of immunotherapy response. Cancer Discov. 2017 July 7;(7):675–693. DOI:10.1158/2159-8290.CD-17-0226
  • Ko EC, Formenti SC. Radiation therapy to enhance tumor immunotherapy: a novel application for an established modality. Int J Radiat Biol. 2019 July;95(7):936–939.
  • Rizzo A, Tavolari S, Ricci AD, et al. Molecular features and targeted therapies in extrahepatic cholangiocarcinoma: promises and failures. Cancers (Basel). 2020 Nov 4;12(11):E3256.
  • Gibney GT, Weiner LM, Atkins MB. Predictive biomarkers for checkpoint inhibitor-based immunotherapy. Lancet Oncol. 2016 Dec;17(12):e542–e551.
  • Teng F, Meng X, Kong L, et al. Progress and challenges of predictive biomarkers of anti PD-1/PD-L1 immunotherapy: a systematic review. Cancer Lett. 2018 Feb 1;414:166–173.
  • Sabbatino F, Villani V, Yearley JH, et al. PD-L1 and HLA class I antigen expression and clinical course of the disease in intrahepatic cholangiocarcinoma. Clin Cancer Res. 2016;22:470–478.
  • Ye Y, Zhou L, Xie X, et al. Interaction of B7-H1 on intrahepatic cholangiocarcinoma cells with PD-1 on tumor-infiltrating T cells as a mechanism of immune evasion. J Surg Oncol. 2009;100:500–504.
  • Fontugne J, Augustin J, Pujals A, et al. PD-L1 expression in perihilar and intrahepatic cholangiocarcinoma. Oncotarget. 2017;8:24644–24651.
  • Gani F, Nagarajan N, Kim Y, et al. Program death 1 immune checkpoint and tumor microenvironment: implications for patients with intrahepatic cholangiocarcinoma. Ann Surg Oncol. 2016;23:2610–2617.
  • Lim YJ, Koh J, Kim K, et al. High ratio of programmed cell death protein 1 (PD-1)(+)/CD8(+) tumor-infiltrating lymphocytes identifies a poor prognostic subset of extrahepatic bile duct cancer undergoing surgery plus adjuvant chemoradiotherapy. Radiother Oncol. 2015;117:165–170.
  • Mou H, Yu L, Liao Q, et al. Successful response to the combination of immunotherapy and chemotherapy in cholangiocarcinoma with high tumour mutational burden and PD-L1 expression: a case report. BMC Cancer. 2018;18:1105.
  • Weinberg BA, Xiu J, Lindberg MR, et al. Molecular profiling of biliary cancers reveals distinct molecular alterations and potential therapeutic targets. J Gastrointest Oncol. 2019;10:652–662.
  • Nakamura H, Arai Y, Totoki Y, et al. Genomic spectra of biliary tract cancer. Nat Genet. 2015;47:1003–1010.
  • Silva VW, Askan G, Daniel TD, et al. Biliary carcinomas: pathology and the role of DNA mismatch repair deficiency. Chin Clin Oncol. 2016;5:62.
  • Kunk PR, Obeid JM, Winters K, et al. Mismatch repair deficiency in cholangiocarcinoma. JCO. 2018;36:269.
  • Winkelmann R, Schneider M, Hartmann S, et al. Microsatellite instability occurs rarely in patients with cholangiocarcinoma: a retrospective study from a german tertiary care hospital. Int J Mol Sci. 2018;19:1421.
  • Minchom A, Aversa C, Lopez J. Dancing with the DNA damage response: next-generation anti-cancer therapeutic strategies. Ther Adv Med Oncol. 2018 July;13(10):1758835918786658.
  • Lamarca A, Barriuso J, McNamara MG, et al. Biliary tract cancer: state of the art and potential role of DNA damage repair. Cancer Treat Rev. 2018 Nov;70:168–177.
  • Malenica I, Donadon M, Lleo A. Molecular and immunological characterization of biliary tract cancers: a paradigm shift towards a personalized medicine. Cancers (Basel). 2020;12:2190.
  • Spizzo G, Puccini A, Xiu J, et al. Molecular profile of BRCA-mutated biliary tract cancers. ESMO Open. 2020 June;5(3):e000682.
  • Ricci AD, Rizzo A, Brandi G. The DNA damage repair (DDR) pathway in biliary tract cancer (BTC): a new Pandora’s box? ESMO Open. 2020;5:e001042.
  • Binnewies M, Roberts EW, Kersten K, et al. Understanding the tumor immune microenvironment (TIME) for effective therapy. Nat Med. 2018;24:541–550.
  • Wei SC, Duffy CR, Allison JP. Fundamental mechanisms of immune checkpoint blockade therapy. Cancer Discov. 2018;8:1069–1086.
  • Woo SR, Corrales L, Gajewski TF. Innate immune recognition of cancer. Annu Rev Immunol. 2015;33:445–474.
  • Krenkel O, Tacke F. Liver macrophages in tissue homeostasis and disease. Nat Rev Immunol. 2017;17:306–321.
  • Jain A, Kwong LN, Javle M. Genomic profiling of biliary tract cancers and implications for clinical practice. Curr Treat Options Oncol. 2016 Nov;17(11):58.
  • Xie C, McGrath NA, Monge Bonilla C, et al. Systemic treatment options for advanced biliary tract carcinoma. J Gastroenterol. 2020 Oct;55(10):944–957.
  • Haber PK, Sia D. Translating cancer genomics for precision oncology in biliary tract cancers. Discov Med. 2019 Nov–Dec;28(155):255–265.
  • Chai Y. Immunotherapy of biliary tract cancer. Tumour Biol. 2016 Mar;37(3):2817–2821.
  • Franses JW, Hong TS, Zhu AX. Nivolumab with gemcitabine plus cisplatin for biliary cancers: as easy as ABC? Lancet Gastroenterol Hepatol. 2019 Aug;4(8):575–577.
  • Dalgleish AG. Why do the majority of patients not respond at all, or only partially or transiently, to immunotherapy? Expert Rev Anticancer Ther. 2019 Dec;19(12):1001–1003.
  • Fumet JD, Limagne E, Thibaudin M, et al. Immunogenic cell death and elimination of immunosuppressive cells: a double-edged sword of chemotherapy. Cancers (Basel). 2020 Sept 16;12(9):E2637.
  • Li W, Deng Y, Chu Q, et al. Gut microbiome and cancer immunotherapy. Cancer Lett. 2019 Apr 10;447:41–47.
  • Gopalakrishnan V, Helmink BA, Spencer CN, et al. The influence of the gut microbiome on cancer, immunity, and cancer immunotherapy. Cancer Cell. 2018 Apr 9;33(4):570–580.
  • Mahipal A, Kommalapati A, Tella SH, et al. Novel targeted treatment options for advanced cholangiocarcinoma. Expert Opin Investig Drugs. 2018 Sept;27(9):709–720.

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