Significant response to pembrolizumab plus lenvatinib in Epstein–Barr-virus-associated intrahepatic cholangiocarcinoma: a case report

References

• Brindley PJ, Bachini M, Ilyas SI, Khan SA, Loukas A, Sirica AE, Teh BT, Wongkham S, Gores GJ. Cholangiocarcinoma [J]. Nat Rev Dis Primers. 2021;7(1):65. doi:10.1038/s41572-021-00300-2.
   PubMed Web of Science ®Google Scholar
• Saint A, Benchetrit M, Novellas S, Ouzan D, Falk AT, Leysalle A, Barriere J. Prolonged efficacy of pembrolizumab in a patient presenting a multi-treated metastatic hepatocholangiocarcinoma [J]. Therap Adv Gastroenterol. 2020. 13:1756284820935189. doi:10.1177/1756284820935189.
   Web of Science ®Google Scholar
• Song G, Shi Y, Meng L, Ma J, Huang S, Zhang J, Wu Y, Li J, Lin Y, Yang S, et al. Single-cell transcriptomic analysis suggests two molecularly subtypes of intrahepatic cholangiocarcinoma [J] 2022 13, 1642.
   Google Scholar
• Rizzo A, Ricci AD, Brandi G. Recent advances of immunotherapy for biliary tract cancer [J]. Expert Rev Gastroenterol Hepatol. 2021;15(5):527–7. doi:10.1080/17474124.2021.1853527.
   PubMed Web of Science ®Google Scholar
• Rizvi S, Khan SA, Hallemeier CL, Kelley RK, Gores GJ. Cholangiocarcinoma — evolving concepts and therapeutic strategies [J]. Nat Rev Clin Oncol. 2018;15(2):95–111. doi:10.1038/nrclinonc.2017.157.
   PubMed Web of Science ®Google Scholar
• Sommer CM, Kauczor HU, Pereira PL. Locoregional therapies of cholangiocarcinoma [J]. Visceral Medicine. 2016;32(6):414–420. doi:10.1159/000453010.
   PubMed Web of Science ®Google Scholar
• de Baere T, Deschamps F, Briggs P, Dromain C, Boige V, Hechelhammer L, Abdel-Rehim M, Aupérin A, Goere D, Elias D. Hepatic malignancies: percutaneous radiofrequency ablation during percutaneous portal or hepatic vein occlusion [J]. Radiology. 2008;248(3):1056–1066. doi:10.1148/radiol.2483070222.
   PubMed Web of Science ®Google Scholar
• Brandi G, Rizzo A, Dall’olio FG, Felicani C, Ercolani G, Cescon M, Frega G, Tavolari S, Palloni A, De Lorenzo S, et al. Percutaneous radiofrequency ablation in intrahepatic cholangiocarcinoma: a retrospective single-center experience [J]. Int J Hyperthermia. 2020; 37(1):479–485. doi:10.1080/02656736.2020.1763484.
   PubMed Web of Science ®Google Scholar
• Zeng FL, Chen JF. Application of Immune checkpoint inhibitors in the treatment of cholangiocarcinoma [J]. Technol Cancer Res Treat. 2021. 20:15330338211039952. doi:10.1177/15330338211039952.
   Web of Science ®Google Scholar
• Ricci AD, Rizzo A, Brandi G. Immunotherapy in biliary tract cancer: worthy of a second look [J]. Cancer Control. 2020;27(3):1073274820948047. doi:10.1177/1073274820948047.
   Web of Science ®Google Scholar
• Hao Z, Wang P. Lenvatinib in management of solid tumors [J]. Oncologist. 2020;25(2):e302–e310. doi:10.1634/theoncologist.2019-0407.
   PubMed Web of Science ®Google Scholar
• Lin J, Yang X, Long J, Zhao S, Mao J, Wang D, Bai Y, Bian J, Zhang L, Yang X, et al. Pembrolizumab combined with lenvatinib as non-first-line therapy in patients with refractory biliary tract carcinoma [J]. Hepatobiliary Surg Nutr. 2020; 9(4):414–424. doi:10.21037/hbsn-20-338.
   PubMed Web of Science ®Google Scholar
• Farrell PJ. Epstein–Barr Virus and cancer [J]. Annu Rev Pathol: Pathol Mech Dis. 2019;14(1):29–53. doi:10.1146/annurev-pathmechdis-012418-013023.
   PubMedGoogle Scholar
• Baxter D, Sacks B, Campbell BCV, Campbell BCV, Carpenter JS, Cognard C, Dippel D, Eesa M, Fischer U, Hausegger K, et al. Multisociety consensus quality improvement revised consensus statement for endovascular therapy of acute ischemic stroke [J]. Int J Stroke. 2018; 13(6):612–632. doi:10.1177/1747493018778713.
   PubMed Web of Science ®Google Scholar
• Sun K, Xu S, Wei J, Wang B, Owusu-Ansah KG, Wang W, Wu J, Zheng S. Clinicopathological features of 11 Epstein–Barr virus-associated intrahepatic cholangiocarcinoma at a single center in China [J]. Medicine (Baltimore). 2016;95(40):e5069. doi:10.1097/MD.0000000000005069.
   PubMed Web of Science ®Google Scholar
• Mishima S, Kawazoe A, Nakamura Y, Sasaki A, Kotani D, Kuboki Y, Bando H, Kojima T, Doi T, Ohtsu A, et al. Clinicopathological and molecular features of responders to nivolumab for patients with advanced gastric cancer [J]. J Immunother Cancer. 2019; 7(1):24. doi:10.1186/s40425-019-0514-3.
   PubMed Web of Science ®Google Scholar
• Banales JM, Cardinale V, Carpino G, Marzioni M, Andersen JB, Invernizzi P, Lind GE, Folseraas T, Forbes SJ, Fouassier L, et al. Cholangiocarcinoma: current knowledge and future perspectives consensus statement from the European Network for the Study of Cholangiocarcinoma (ENS-CCA) [J]. Nat Rev Gastro Hepat. 2016; 13: 261–280.
   PubMed Web of Science ®Google Scholar
• Park SY, Kim JH, Yoon HJ, Lee I-S, Yoon H-K, Kim K-P. Transarterial chemoembolization versus supportive therapy in the palliative treatment of unresectable intrahepatic cholangiocarcinoma [J]. Clin Radiol. 2011;66(4):322–328. doi:10.1016/j.crad.2010.11.002.
   PubMed Web of Science ®Google Scholar
• Hyder O, Marsh JW, Salem R, Petre EN, Kalva S, Liapi E, Cosgrove D, Neal D, Kamel I, Zhu AX, et al. Intra-arterial therapy for advanced intrahepatic cholangiocarcinoma: a multi-institutional analysis [J]. Ann Surg Oncol. 2013; 20(12):3779–3786. doi:10.1245/s10434-013-3127-y.
   PubMed Web of Science ®Google Scholar
• Laquière A, Boustière C, Leblanc S, Penaranda G, Désilets E, Prat F. Safety and feasibility of endoscopic biliary radiofrequency ablation treatment of extrahepatic cholangiocarcinoma [J]. Surg Endosc. 2016;30(3):1242–1248. doi:10.1007/s00464-015-4322-7.
   PubMed Web of Science ®Google Scholar
• Han K, Ko HK, Kim KW, Won HJ, Shin YM, Kim PN. Radiofrequency ablation in the treatment of unresectable intrahepatic cholangiocarcinoma: systematic review and meta-analysis [J]. J Vasc Interv Radiol. 2015;26(7):943–948. doi:10.1016/j.jvir.2015.02.024.
   PubMed Web of Science ®Google Scholar
• Boehm LM, Jayakrishnan TT, Miura JT, Zacharias AJ, Johnston FM, Turaga KK, Gamblin TC. Comparative effectiveness of hepatic artery based therapies for unresectable intrahepatic cholangiocarcinoma [J]. J Surg Oncol. 2015;111(2):213–220. doi:10.1002/jso.23781.
   PubMed Web of Science ®Google Scholar
• Lu Y, Liu L, Wu JC, Bie L-K, Gong B. Efficacy and safety of photodynamic therapy for unresectable cholangiocarcinoma: A meta-analysis [J]. Clin Res Hepatol Gastroenterol. 2015;39(6):718–724. doi:10.1016/j.clinre.2014.10.015.
   PubMed Web of Science ®Google Scholar
• Dolak W, Schreiber F, Schwaighofer H, Gschwantler M, Plieschnegger W, Ziachehabi A, Mayer A, Kramer L, Kopecky A, Schrutka-Kölbl C, et al. Endoscopic radiofrequency ablation for malignant biliary obstruction: a nationwide retrospective study of 84 consecutive applications [J]. Surg Endosc. 2014; 28(3):854–860. doi:10.1007/s00464-013-3232-9.
   PubMed Web of Science ®Google Scholar
• Valle JW, Wasan H, Johnson P, Jones E, Dixon L, Swindell R, Baka S, Maraveyas A, Corrie P, Falk S, et al. Gemcitabine alone or in combination with cisplatin in patients with advanced or metastatic cholangiocarcinomas or other biliary tract tumours: a multicentre randomised phase II study – the UK ABC-01 study [J]. Br J Cancer. 2009; 101(4):621–627. doi:10.1038/sj.bjc.6605211.
   PubMed Web of Science ®Google Scholar
• Lamarca A, Ross P, Wasan HS, Hubner RA, McNamara MG, Lopes A, Manoharan P, Palmer D, Bridgewater J, Valle JW. Advanced intrahepatic cholangiocarcinoma: Post Hoc analysis of the ABC-01, -02, and -03 clinical trials [J]. JNCI J Nat Cancer Inst. 2019. 112:200–210. doi:10.1093/jnci/djz071.
   Google Scholar
• Rizzo A, RIcci AD, Tober N, Nigro MC, Mosca M, Palloni A, Abbati F, Frega G, De Lorenzo S, Tavolari S, et al. Second-line treatment in advanced biliary tract cancer: today and tomorrow [J]. Anticancer Res. 2020; 40(6):3013–3030. doi:10.21873/anticanres.14282.
   PubMed Web of Science ®Google Scholar
• Rizzo A, Ricci AD, Brandi G. Durvalumab: an investigational anti-PD-L1 antibody for the treatment of biliary tract cancer [J]. Expert Opin Investig Drugs. 2021;30(4):343–350. doi:10.1080/13543784.2021.1897102.
   PubMed Web of Science ®Google Scholar
• Ricci AD, Rizzo A, Brandi G. The DNA damage repair (DDR) pathway in biliary tract cancer (BTC): a new Pandora’s box? [J] ESMO Open. 2020;5(5):e001042. doi:10.1136/esmoopen-2020-001042.
   PubMed Web of Science ®Google Scholar
• Rizzo A, Brandi G. First-line chemotherapy in advanced biliary tract cancer ten years after the ABC-02 trial: “And yet it moves!” [J]. Cancer Treat Res Commun. 2021. 27:100335. doi:10.1016/j.ctarc.2021.100335.
   PubMedGoogle Scholar
• McNamara MG, Bridgewater J, Palmer DH, Faluyi O, Wasan H, Patel A, Ryder WD, Barber S, Gnanaranjan C, Ghazaly E, et al. A phase Ib study of NUC‐1031 in combination with cisplatin for the first‐line treatment of patients with advanced biliary tract cancer (ABC‐08) [J]. Oncologist. 2020; 26(4):e669–e678. doi:10.1002/onco.13598.
   PubMed Web of Science ®Google Scholar
• Shroff RT, Javle MM, Xiao L, Kaseb AO, Varadhachary GR, Wolff RA, Raghav KPS, Iwasaki M, Masci P, Ramanathan RK, et al. Gemcitabine, cisplatin, and nab-paclitaxel for the treatment of advanced biliary tract cancers: A phase 2 clinical trial [J]. JAMA Oncol. 2019; 5(6):824–830. doi:10.1001/jamaoncol.2019.0270.
   PubMed Web of Science ®Google Scholar
• Nakamura H, Arai Y, Totoki Y, Shirota T, Elzawahry A, Kato M, Hama N, Hosoda F, Urushidate T, Ohashi S, et al. Genomic spectra of biliary tract cancer [J]. Nat Genet. 2015; 47(9):1003–1010. doi:10.1038/ng.3375.
   PubMed Web of Science ®Google Scholar
• Rizvi S, Borad MJ, Patel T, Gores G. Cholangiocarcinoma: molecular pathways and therapeutic opportunities [J]. Semin Liver Dis. 2014;34(04):456–464. doi:10.1055/s-0034-1394144.
   PubMedGoogle Scholar
• Saborowski A, Saborowski M, Davare MA, Druker BJ, Klimstra DS, Lowe SW. Mouse model of intrahepatic cholangiocarcinoma validates FIG–ROS as a potent fusion oncogene and therapeutic target [J]. Proc Natl Acad Sci. 2013;110(48):19513–19518. doi:10.1073/pnas.1311707110.
   PubMed Web of Science ®Google Scholar
• Zhang J, Jiao J, Cermelli S, Muir K, Jung KH, Zou R, Rashid A, Gagea M, Zabludoff S, Kalluri R, et al. miR-21 inhibition reduces liver fibrosis and prevents tumor development by inducing apoptosis of CD24+ progenitor cells [J]. Cancer Res. 2015; 75(9):1859–1867. doi:10.1158/0008-5472.CAN-14-1254.
   PubMed Web of Science ®Google Scholar
• Yao L, Han C, Song K, Zhang J, Lim K, Wu T. Omega-3 polyunsaturated fatty acids upregulate 15-PGDH expression in cholangiocarcinoma cells by inhibiting miR-26a/b expression [J]. Cancer Res. 2015;75(7):1388–1398. doi:10.1158/0008-5472.CAN-14-2561.
   PubMed Web of Science ®Google Scholar
• Li X, Wenes M, Romero P, Huang SCC, Fendt S-M, Ho P-C. Navigating metabolic pathways to enhance antitumour immunity and immunotherapy [J]. Nat Rev Clin Oncol. 2019;16(7):425–441. doi:10.1038/s41571-019-0203-7.
   PubMed Web of Science ®Google Scholar
• Piha-Paul SA, Oh DY, Ueno M, Malka D, Chung HC, Nagrial A, Kelley RK, Ros W, Italiano A, Nakagawa K, et al. Efficacy and safety of pembrolizumab for the treatment of advanced biliary cancer: Results from the KEYNOTE-158 and KEYNOTE-028 studies [J]. Int J Cancer. 2020; 147(8):2190–2198. doi:10.1002/ijc.33013.
   PubMed Web of Science ®Google Scholar
• Ueno M, Ikeda M, Sasaki T, Nagashima F, Mizuno N, Shimizu S, Ikezawa H, Hayata N, Nakajima R, Morizane C. Phase 2 study of lenvatinib monotherapy as second-line treatment in unresectable biliary tract cancer: primary analysis results [J]. BMC Cancer. 2020;20(1):1105. doi:10.1186/s12885-020-07365-4.
   PubMed Web of Science ®Google Scholar
• Zhu S, Liu C, Dong Y, Shao J, Liu B, Shen J. A retrospective study of lenvatinib monotherapy or combined with programmed cell death protein 1 antibody in the treatment of patients with hepatocellular carcinoma or intrahepatic cholangiocarcinoma in China [J]. Front Oncol. 2021. 11:788635. doi:10.3389/fonc.2021.788635.
   PubMed Web of Science ®Google Scholar
• Zhang Z, Zhang W, Wang H, Hu B, Wang Z, Lu S. Successful treatment of advanced intrahepatic cholangiocarcinoma with a high tumor mutational burden and PD-L1 expression by PD-1 blockade combined with tyrosine kinase inhibitors: A case report [J]. Front Immunol. 2021. 12:744571. doi:10.3389/fimmu.2021.744571.
   PubMed Web of Science ®Google Scholar
• Gomez-Roca C, Yanez E, Im S-A, Castanon Alvarez E, Senellart H, Doherty M, García-Corbacho J, Lopez JS, Basu B, Maurice-Dror C, et al. LEAP-005: A phase II multicohort study of lenvatinib plus pembrolizumab in patients with previously treated selected solid tumors—results from the colorectal cancer cohort [J]. J Clin Oncol. 2021; 39(3_suppl):94–94. doi:10.1200/JCO.2021.39.3_suppl.94.
   Web of Science ®Google Scholar
• Mertens JC, Rizvi S, Gores GJ. Targeting cholangiocarcinoma [J]. Biochim Biophys Acta Mol Basis Dis. 2018;1864(4):1454–1460. doi:10.1016/j.bbadis.2017.08.027.
   PubMed Web of Science ®Google Scholar
• Huang YH, Zhang CZ, Huang QS, Yeong J, Wang F, Yang X, He Y-F, Zhang X-L, Zhang H, Chen S-L, et al. Clinicopathologic features, tumor immune microenvironment and genomic landscape of Epstein-Barr virus-associated intrahepatic cholangiocarcinoma [J]. J Hepatol. 2021; 74(4):838–849. doi:10.1016/j.jhep.2020.10.037.
   PubMed Web of Science ®Google Scholar
• Wang J, Ge J, Wang Y, Xiong F, Guo J, Jiang X, Zhang L, Deng X, Gong Z, Zhang S, et al. EBV miRnas BART11 and BART17-3p promote immune escape through the enhancer-mediated transcription of PD-L1 [J]. Nat Commun. 2022; 13(1):866. doi:10.1038/s41467-022-28479-2.
   PubMed Web of Science ®Google Scholar
• Wang L, Dong H, Ni S, Huang D, Tan C, Chang B, Sheng W. Programmed death-ligand 1 is upregulated in intrahepatic lymphoepithelioma-like cholangiocarcinoma [J]. Oncotarget. 2016;7(43):69749–69759. doi:10.18632/oncotarget.11949.
   PubMedGoogle Scholar
• Naseem M, Barzi A, Brezden-Masley C, Puccini A, Berger MD, Tokunaga R, Battaglin F, Soni S, McSkane M, Zhang W, et al. Outlooks on Epstein-Barr virus associated gastric cancer [J]. Cancer Treat Rev. 2018; 66:15–22. doi:10.1016/j.ctrv.2018.03.006.
   PubMed Web of Science ®Google Scholar
• Shigeta K, Datta M, Hato T, Kitahara S, Chen IX, Matsui A, Kikuchi H, Mamessier E, Aoki S, Ramjiawan RR, et al. Dual programmed death receptor-1 and vascular endothelial growth factor receptor-2 blockade promotes vascular normalization and enhances antitumor immune responses in hepatocellular carcinoma [J]. Hepatology. 2020; 71(4):1247–1261. doi:10.1002/hep.30889.
   PubMed Web of Science ®Google Scholar