Combination of checkpoint inhibitors with radiotherapy in esophageal squamous cell carcinoma treatment: A novel strategy

Xiu-Yong Liao, Chao-Yuan Liu, Jian-Feng He, Li-Shu Wang, Tao Zhang, Xiu-Yong Liao, Chao-Yuan Liu, Jian-Feng He, Li-Shu Wang, Tao Zhang

Abstract

Despite the rapid development of numerous types of treatment, including radiotherapy (RT) as the main strategy, esophageal squamous cell carcinoma (ESCC) has a poor prognosis. Recent studies demonstrated that immunotherapy can improve the survival of patients with locally advanced and metastatic ESCC. Furthermore, previous studies reported that the expression of programmed death-ligand 1 is significantly associated with esophageal cancer prognosis. At present, several ongoing clinical trials have extended the use of immunotherapy from palliative and salvage treatments to neoadjuvant treatment with concurrent chemoradiation. The first- or second-line treatments were used to explore antitumor efficacy with reduced adverse events. The combination of RT and immunotherapy can exert a local therapeutic effect and improve the function of the immune system, enhancing antitumor efficacy. This review investigated the role of immunotherapy and radiotherapy in ESCC and described the potential efficacy of combining immunotherapy with radiotherapy in ESCC.

Keywords: checkpoint inhibitors; esophageal cancer; immunotherapy; radiotherapy.

Copyright: © Liao et al.

Figures

Figure 1.
Figure 1.
Radiotherapy accelerates the production of Tregs, reduces radiation-induced tumor death and contributes to tumor escape from immune surveillance. These events suppress the antitumor immune response. B7 is a peripheral membrane protein found on activated antigen presenting cells which interaction with CTLA-4 on T cells promotes antitumor immunity. Tregs, regulatory T cells; CTLA-4, cytotoxic T-lymphocyte-associated protein 4; DC, dendritic cell; MHC, major histocompatibility complex; PD-1, programmed cell death 1; PD-L1, programmed death-ligand 1.
Figure 2.
Figure 2.
Combining radiation with anti-PD-L1, anti-PD-1 and anti-CTLA-4 activates effector T cells and promotes the recruitment and infiltration of immune cells, enhancing the abscopal effect. This ultimately increases the recognition and killing of tumor cells by the immune system. B7 is a peripheral membrane protein found on activated antigen presenting cells which interaction with CTLA-4 on T cells promotes antitumor immunity. CTLA-4, cytotoxic T-lymphocyte-associated protein 4; DC, dendritic cell; MHC, major histocompatibility complex; PD-1, programmed cell death 1; PD-L1, programmed death-ligand 1.

References

    1. Siegel RL, Miller KD, Jemal A. Cancer statistics, 2015. CA Cancer J Clin. 2015;65:5–29. doi: 10.3322/caac.21254.
    1. Arnold M, Soerjomataram I, Ferlay J, Forman D. Global incidence of esophageal cancer by histological subtype in 2012. Gut. 2015;64:381–387. doi: 10.1136/gutjnl-2014-308124.
    1. Edgren G, Adami HO, Weiderpass E, Nyrén O. A global assessment of the oesophageal adenocarcinoma epidemic. Gut. 2013;62:1406–1414. doi: 10.1136/gutjnl-2012-302412.
    1. Kitagawa Y, Uno T, Oyama T, Kato K, Kato H, Kawakubo H, Kawamura O, Kusano M, Kuwano H, Takeuchi H, et al. Esophageal cancer practice guidelines 2017 edited by the Japan Esophageal Society: Part 1. Esophagus. 2019;16:1–24. doi: 10.1007/s10388-018-0641-9.
    1. Ferlay J, Soerjomataram I, Dikshit R, Eser S, Mathers C, Rebelo M, Parkin DM, Forman D, Bray F. Cancer incidence and mortality worldwide: Sources, methods and major patterns in GLOBOCAN 2012. Int J Cancer. 2015;136:E359–E386. doi: 10.1002/ijc.29210.
    1. Lin DC, Wang MR, Koef HP. Genomic and epigenomic aberrations in esophageal squamous cell carcinoma and implications for patients. Gastroenterology. 2018;154:374–389. doi: 10.1053/j.gastro.2017.06.066.
    1. Sawada G, Niida A, Uchi R, Hirata H, Shimamura T, Suzuki Y, Shiraishi Y, Chiba K, Imoto S, Takahishi Y, et al. Genomic landscape of esophageal squamous cell carcinoma in a Japanese population. Gastroenterology. 2016;150:1171–1182. doi: 10.1053/j.gastro.2016.01.035.
    1. Talukdar FR, di Pietro M, Secricer M, Moehler M, Goepgert K, Lima SSC, Pinto LFR, Hendricks D, Parker MI, Herceg Z. Molecular landscape of esophageal cancer: Implications for early detection and personalized therapy. Ann NY Acad Sci. 2018;1434:342–359. doi: 10.1111/nyas.13876.
    1. Pakkala S, Ramalingam SS. Personalized therapy for lung cancer: Striking a moving target. JCI Insight. 2018;3:120858. doi: 10.1172/jci.insight.120858.
    1. Ducreux M, Chamseddine A, Laurent-Puig P, Smolenschi C, Hollebecque A, Dartigues P, Samallin E, Boige V, Malka D, Gelli M. Molecular targeted therapy of BRAF-mutant colorectal cancer. Ther Adv Med Oncol. 2019;11:1758835919856494. doi: 10.1177/1758835919856494.
    1. Lam KO, Kwong DLW. Target therapy for esophageal adenocarcinoma. Methods Mol Biol. 2018;1756:51–65. doi: 10.1007/978-1-4939-7734-5_5.
    1. Thuss-Patience PC, Shah MA, Ohtsu A, Van Cutsem E, Ajani JA, Castro H, Mansoor W, Chung HC, Bodoky G, Shitara K, et al. Trastuzumab emtansine versus taxane use for previously treated HER2-positive locally advanced or metastatic gastric or gastro-esophageal junction adenocarcinoma (GATSBY): An international randomised, open-label, adaptive, phase 2/3 study. Lancet Oncol. 2017;18:640–653. doi: 10.1016/S1470-2045(17)30111-0.
    1. Cunningham D, Tebbutt NC, Davidenko I. Phase III, randomized, double-blind, multicenter, placebo (P)-controlled trial of rilotumumab (R) plus epirubicin, cisplatin and capecitabine (ECX) as first-line therapy in patients (pts) with advanced MET-positive (pos) gastric or gastresophageal junction (G/GEJ) cancer: RILOMET-1 study. J Clin Oncol. 2017;33(Suppl 15):4000. doi: 10.1200/jco.2015.33.15_suppl.4000.
    1. Hecht JR, Bang YJ, Qin SK, Chung HC, Xu JM, Park JO, Jeziorski K, Shparyk Y, Hoff PM, Sobrero A, et al. Lapatinib in combination with capecitabine plus oxaliplatin in Human Epidermal Growth Factor Receptor 2-positive advanced or metastatic gastric, esophageal, or gastresophageal adenocarcinoma: TRIO-013/LOGiC-A randomized phase III trial. J Clin Oncol. 2016;34:443–451. doi: 10.1200/JCO.2015.62.6598.
    1. Karlsson AK, Saleh SN. Checkpoint inhibitors for malignant melanoma: A systematic review and meta-analysis. Clin Cosmet Investig Dermatol. 2017;10:325–339. doi: 10.2147/CCID.S120877.
    1. Herzberg B, Campo MJ, Gainor JF. Immune checkpoint inhibitors in non-small cell lung cancer. Oncologist. 2017;22:81–88. doi: 10.1634/theoncologist.2016-0189.
    1. Raufi AG, Klempner SJ. Immunotherapy for advanced gastric and esophageal cancer: Preclinical rationale and ongoing clinical investigations. J Gastrointest Oncol. 2015;6:561–569.
    1. Kudo T, Hamamoto Y, Kato K, Ura T, Kojima T, Tsushima T, Hironaka S, Hara H, Satoh T, Iwasa S, et al. Nivolumab treatment for oesophageal squamous-cell carcinoma: An open-label, multicentre, phase 2 trial. Lancet Oncol. 2017;18:631–639. doi: 10.1016/S1470-2045(17)30181-X.
    1. Kojima T, Doi T. Immunotherapy for esophageal squamous cell carcinoma. Curr Oncol Rep. 2017;19:33. doi: 10.1007/s11912-017-0590-9.
    1. Kang J, Demaria S, Formenti S. Current clinical trials testing the combination of immunotherapy with radiotherapy. J Immunother Cancer. 2016;4:51. doi: 10.1186/s40425-016-0156-7.
    1. Weichselbaum RR, Liang H, Deng L, Fu YX. Radiotherapy and immunotherapy: A beneficial liaison? Nat Rev Clin Oncol. 2017;14:365–379. doi: 10.1038/nrclinonc.2016.211.
    1. Prasad NR, Karthigeyan M, Vikram K, Parthasarathy R, Reddy KS. Palliative radiotherapy in esophageal cancer. Indian J Surg. 2015;77:34–38. doi: 10.1007/s12262-013-0817-4.
    1. Matuschek C, Bölke E, Zahra T, Knoefel WT, Peiper M, Budach W, Erhardt A, Scherer A, Baldus SE, Gerber PA, et al. Gattermann N, Orth K. Trimodal therapy in squamous cell carcinoma of the esophagus. Eur J Med Res. 2011;16:437–444. doi: 10.1186/2047-783X-16-10-437.
    1. Baskar R, Dai J, Wenlong N, Yeo R, Yeoh KW. Biological response of cancer cells to radiation treatment. Front Mol Biosci. 2014;1:24. doi: 10.3389/fmolb.2014.00024.
    1. Gong J, Le TQ, Massarelli E, Hendifar AE, Tuli R. Radiation therapy and PD-1/PD-L1 blockade: The clinical development of an evolving anticancer combination. J Immunother Cancer. 2018;6:46. doi: 10.1186/s40425-018-0361-7.
    1. Wan S, Pestka S, Jubin RG, Lyu YL, Tsai YC, Liu LF. Chemotherapeutics and radiation stimulate MHC class I expression through elevated interferon-beta signaling in breast cancer cells. PLoS One. 2012;7:e32542. doi: 10.1371/journal.pone.0032542.
    1. Wang Y, Deng W, Li N, Neri S, Sharma A, Jiang W, Lin SH. Combining immunotherapy and radiotherapy for cancer treatment: Current challenges and future directions. Front Pharmacol. 2018;9:185. doi: 10.3389/fphar.2018.00185.
    1. Persa E, Balogh A, Sáfrány G, Lumniczky K. The effect of ionizing radiation on regulatory T cells in health and disease. Cancer Lett. 2015;368:252–261. doi: 10.1016/j.canlet.2015.03.003.
    1. Facciabene A, Motz GT, Coukos G. T-regulatory cells: Key players in tumor immune escape and angiogenesis. Cancer Res. 2012;72:2162–2171. doi: 10.1158/0008-5472.CAN-11-3687.
    1. Liu S, Sun X, Luo J, Zhu H, Yang X, Guo Q, Song Y, Sun X. Effects of radiation on T regulatory cells in normal states and cancer: Mechanisms and clinical implications. Am J Cancer Res. 2015;5:3276–3285.
    1. Tang J, Shalabi A, Hubbard-Lucey VM. Comprehensive analysis of the clinical immune-oncology landscape. Ann Oncol. 2018;29:84–91. doi: 10.1093/annonc/mdx755.
    1. Pardoll DM. The blockade of immune checkpoints in cancer immunotherapy. Nat Rev Cancer. 2012;12:252–264. doi: 10.1038/nrc3239.
    1. Riaz N, Havel JJ, Makarov V, Desrichard A, Urba WJ, Sims JS, Hodi FS, Marin-Algarra S, Mandal R, Sharfman WH, et al. Tumor and microenvironment evoluation during immunotherapy with nivolumab. Cell. 2017;171:934–949.e16. doi: 10.1016/j.cell.2017.09.028.
    1. Kono K, Mimura K, Yamada R, Ujiie D, Hayase S, Tada T, Hanayama H, Min AKT, Shibata M, Momma T, et al. Current status of cancer immunotherapy for esophageal squamous cell carcinoma. Esophagus. 2018;15:1–9. doi: 10.1007/s10388-017-0596-2.
    1. Memarnejadian A, Meilleur CE, Shaler CR, Khazaie K, Bennink JR, Schell TD, Haeryfar SMM. PD-1 blockade promotes epitope spreading in anticancer CD8+ T cell responses by preventing fratricidal death of subdominant clones to relieve immunodomination. J Immunol. 2017;199:3348–3359. doi: 10.4049/jimmunol.1700643.
    1. Tanaka K, Miyata H, Sugimura K, Kanemura T, Hamada-Uematsu M, Mizote Y, Yamasaki M, Wada H, Nakajima K, Takiguchi S, et al. Negative influence of programmed death-1-ligands on the survival of esophageal cancer patients treated with chemotherapy. Cancer Sci. 2016;107:726–733. doi: 10.1111/cas.12938.
    1. Chen L, Deng H, Lu M, Xu B, Wang Q, Jiang J, Wu C. B7-H1 expression associates with tumor invasion and predicts patient's survival in human esophageal cancer. Int J Clin Exp Pathol. 2014;7:6015–6023.
    1. Wang X, Teng F, Kong L, Yu J. PD-L1 expression in human cancers and its association with clinical outcomes. Onco Targets Ther. 2016;9:5023–5039. doi: 10.2147/OTT.S105862.
    1. Liu Y, Cheng Y, Xu Y, Wang Z, Du X, Li C, Peng J, Gao L, Liang X, Ma C. Increased expression of programmed cell death protein 1 on NK cells inhibits NK-cell-mediated anti-tumor function and indicates poor prognosis in digestive cancers. Oncogene. 2017;36:6143–6153. doi: 10.1038/onc.2017.209.
    1. Leng C, Li Y, Qin J, Ma J, Liu X, Cui Y, Sun H, Wang Z, Hua X, Yu Y, et al. Relationship between expression of PD-L1 and PD-L2 on esophageal squamous cell carcinoma and the antitumor effects of CD8+ T cells. Oncol Rep. 2016;35:699–708. doi: 10.3892/or.2015.4435.
    1. Hatogai K, Kitano S, Fujii S, Kojima T, Daiko H, Nomura S, Yoshino T, Ohtsu A, Takiguchi Y, Doi T, Ochiai A. Comprehensive immunohistochemical analysis of tumor microenvironment immune status in esophageal squamous cell carcinoma. Oncogarget. 2016;7:47252–47264.
    1. Jiang D, Song Q, Wang H, Huang J, Wang H, Hou J, Li X, Xu Y, Sujie A, Zeng H, et al. Independent prognostic role of PD-L1expression in patients with esophageal squamous cell carcinoma. Oncogarget. 2017;8:8315–8329.
    1. Borghaei H, Paz-Ares L, Horn L, Spigel DR, Steins M, Ready NE, Chow LQ, Vokes EE, Felip E, Holgado E, et al. Nivolumab versus docetaxel in advanced non-squamous non-small cell lung cancer. N Engl J Med. 2015;373:1627–1639. doi: 10.1056/NEJMoa1507643.
    1. Katsuya Y, Fujita Y, Horinouchi H, Ohe Y, Watanabe S, Tsuta K. Immunohistochemical status of PD-L1 in thymoma and thymic carci-noma. Lung Cancer. 2015;88:154–159. doi: 10.1016/j.lungcan.2015.03.003.
    1. Fay AP, Signoretti S, Callea M, Telό GH, McKay RR, Song J, Carvo I, Lampron ME, Kaymakcalan MD, Poli-de-Figueiredo CE, et al. Programmed death ligand-1 expression in adrenocortical carcinoma: An exploratory biomarker study. J Immunother Cancer. 2015;3:3. doi: 10.1186/s40425-015-0047-3.
    1. Mansfield AS, Roden AC, Peikert T, Sheinin YM, Harrington SM, Krco CJ, Dong H, Kwon ED. B7-H1 expression in malig-nant pleural mesothelioma is associated with sarcomatoid histology and poor prognosis. J Thorac Oncol. 2014;9:1036–1040. doi: 10.1097/JTO.0000000000000177.
    1. Lipson EJ, Vincent JG, Loyo M, Kagohara LT, Luber BS, Wang H, Xu H, Nayar SK, Wang TS, Sidransky D, et al. PD-L1 expression in the Merkel cell carcinoma microenvironment: Association with in ammation, Merkel cell polyomavirus and overall survival. Cancer Immunol Res. 2013;1:54–63. doi: 10.1158/2326-6066.CIR-13-0034.
    1. Conway JR, Kofman E, Mo SS, Elmarakeby H, Van Allen E. Genomics of response to immune checkpoint therapies for cancer: Implications for precision medicine. Genome Med. 2018;10:93. doi: 10.1186/s13073-018-0605-7.
    1. Doi T, Piha-Paul SA, Jalal SI, Mai-Dang H, Yuan S, Koshiji M, Csiki I, Bennouna J. Pembrolizumab (MK-3475) for patients (pts) with advanced esophageal carcinoma: Preliminary results from KEYNOTE-028. J Clin Oncol. 2015;33(15 Suppl):S4010. doi: 10.1200/jco.2015.33.15_suppl.4010.
    1. Doi T, Piha-Paul SA, Jalal SI, Mai-Dang H, Saraf S, Koshiji M, Csiki I, Bennouna J. Updated results for the advanced esophageal carcinoma cohort of the phase Ib KEYNOTE-028 study of pembrolizumab. J Clin Oncol. 2016;34(15 Suppl):S4046. doi: 10.1200/JCO.2016.34.15_suppl.4046.
    1. Stenger M. Immunotherapy in Advanced Esophageal Carcinoma. . [Nov 29;2017 ];The ASCO Post. 2017
    1. Doi T, Bennouna J, Shen L, Enzinger PC, Wang R, Csiki I, Koshiji M, Shah MA. KEYNOTE-181: Phase 3, open-label study of second-line pembrolizumab vs single-agent chemotherapy in patients with advanced/metastatic esophageal adenocarcinoma. J Clin Oncol. 2017;34(15 Suppl)
    1. Shah MA, Kojima T, Enzinger PC, Hochhauser D, Raimbourg J, Hollebecque A, Lordick F, Kim SB, Tajika M, Kim HT, et al. Pembrolizumab for patients with previously treated metastatic adenocarcinoma or squamous cell carcinoma of the esophagus: Phase 2 KEYNOTE-180 study. J Clin Oncol. 2018;36(15 Suppl):S4049. doi: 10.1200/JCO.2018.36.15_suppl.4049.
    1. Kitagawa Y, Doki Y, Kato K, Ura T. Two year survival and safety update for esophageal squamous cell carcinoma treated with nivolumab (ATTRACTION-01/ONO-4538-07) Anna Oncol. 2017;28(Suppl 5):v209–v268.
    1. Yuriy Y, Alexander PO, Calvo E, Joseph W, Kim, Antonio PA, Sharma P, Johanna KP. Nivolumab ± ipilimumab in pts with advanced (adv)/metastatic chemotherapy-refractory (CTx-R) gastric (G), esophageal (E), or gastroesophageal junction (GEJ) cancer: CheckMate 032 study. J Clin Oncol. 2017;35(Suppl 15):4014. doi: 10.1200/JCO.2017.35.15_suppl.4014.
    1. Greally M, Molena D, Sihag S, Wu Abraham JC, Shah PM, Fein Carly, Capanu M, Kelsen DP, Janjigian YY, Ilson DH, et al. Phase Ib/II trial of durvalumab and chemoradiation (CRT) with carboplatin/paclitaxel for esophageal and gastroesophageal junction (GEJ) adenocarcinoma. J Clin Oncol. 2018;4:172. doi: 10.1200/JCO.2018.36.4_suppl.172.
    1. Chung HC, Arkenau HT, Wyrwicz L, Oh DY, Lee KW, Infante JR, Chin KM, Heydebreck AV, Kang YK, Safran H. Safety, PD-L1 expression, and clinical activity of avelumab (MSB0010718C), an anti-PD-L1 antibody, in patients with advanced gastric or gastroesophageal junction cancer. J Clin Oncol. 2016;34(4 Suppl):S167. doi: 10.1200/jco.2016.34.4_suppl.167.
    1. Smyth E, Thuss-Patience PC. Immune checkpoint inhibition in gastro-oesophageal cancer. Oncol Res Treat. 2018;41:272–280. doi: 10.1159/000489099.
    1. Bang Y, Golan T, Lin CC, Kang YK, Wainberg ZA, Wasserstrom H, Jin J, Mi G, McNeely SC, Laing N, et al. Interim safety and clinical activity in patients (pts) with locally advanced and unresectable or metastatic gastric or gastroesophageal junction (G/GEJ) adenocarcinoma from a multicohort phase I study of ramucirumab (R) plus durvalumab (D) J Clin Oncol. 2018;36(4 Suppl):S92. doi: 10.1200/JCO.2018.36.4_suppl.92.
    1. Taieb J, Moehler M, Boku N, Ajani JA, Yañez Ruiz E, Ryu MH, Guenther S, Chand V, Bang YJ. Evolution of checkpoint inhibitors for the treatment of metastatic gastric cancers: Current status and future perspectives. Cancer Treat Rev. 2016;66:104–113. doi: 10.1016/j.ctrv.2018.04.004.
    1. Mole RH. Whole body irradiation-radiobiology or medicine? Br J Radiol. 1953;26:234–241. doi: 10.1259/0007-1285-26-305-234.
    1. Abuodeh Y, Venkat P, Kim S. Systematic review of case reports on the abscopal effect. Curr Probl Cancer. 2016;40:25–37. doi: 10.1016/j.currproblcancer.2015.10.001.
    1. Siva S, MacManus MP, Martin RF, Martin OA. A Abscopal effects of radiation therapy: A clinical review for the radiobiologist. Cancer Lett. 2013;356:82–90. doi: 10.1016/j.canlet.2013.09.018.
    1. Van Limbergen EJ, De Ruysscher DK, Olive Pimentel V, Marcus D, Berbee M, Hoeben A, Rekers N, Theys J, Yaromina A, Dubois LJ, Lambin P. Combining radiotherapy with immunotherapy: The past, the present and the future. Br J Radiol. 2017;90:20170157. doi: 10.1259/bjr.20170157.
    1. Jing W, Gershan JA, Weber J, Tlomak D, Mcolash L, Sabatos-Peyton C, Johnson BD. Combined immune checkpoint protein blockade and low dose whole body irradiation as immunotherapy for myeloma. J Immunother Cancer. 2015;3:2. doi: 10.1186/s40425-014-0043-z.
    1. Salama AK, Postow MA, Salama JK. Irradiation and immunotherapy: From concept to the clinic. Cancer. 2016;122:1659–1671. doi: 10.1002/cncr.29889.
    1. Reynders K, Illidge T, Siva S, Chang JY, De Ruysscher D. The abscopal effect of local radiotherapy: Using immunotherapy to make a rare event clinically relevant. Cancer Treat Rev. 2015;41:503–510. doi: 10.1016/j.ctrv.2015.03.011.
    1. Twyman-Saint Victor C, Rech AJ, Maity A, Rengan R, Pauken KE, Stelekati E, Benci JL, Xu B, Dada H, Odorizzi PM, et al. Radiation and dual checkpoint blockade activates non-redundant immune mechanisms in cancer. Nature. 2015;520:373–377. doi: 10.1038/nature14292.
    1. Schoenhals JE, Seyedin SN, Tang C, Cortez MA, Niknam S, Tsouka E, Chang JY, Hahn SM, Welsh JW. Preclinical rationale and clinical considerations for radiotherapy plus immunotherapy: Going beyond local control. Cancer J. 2016;22:130–137. doi: 10.1097/PPO.0000000000000181.
    1. Son CH, Fleming GF, Moroney JW. Potential role of radiation therapy in augmenting the activity of immunotherapy for gynecologic cancers. Cancer Manag Res. 2017;9:553–563. doi: 10.2147/CMAR.S116683.
    1. Frey B, Rückert M, Deloch L, Rühle PF, Derer A, Fietkau R, Gaipl US. Immunomodulation by ionizing radiation-impact for design of radio- immunotherapies and for treatment of inflammatory diseases. Immunol Rev. 2017;280:231–248. doi: 10.1111/imr.12572.
    1. Lhuillier C, Rudqvist NP, Elemento O, Formenti SC, Demaria S. Radiation therapy and anti-tumor immunity: Exposing immunogenic mutations to the immune system. Genome Med. 2019;11:40. doi: 10.1186/s13073-019-0653-7.
    1. Kim KJ, Kim JH, Lee SJ, Lee EJ, Shin EC, Seong J. Radiation improves antitumor effect of immune checkpoint inhibitor in murine hepatocellular carcinoma model. Oncotarget. 2017;8:41242–41255.
    1. Oweida A, Lennon S, Calame D, Korpela S, Bhatia S, Sharma J, Graham C, Binder D, Serkova N, Raben D, et al. Ionizing radiation sensitizes tumors to PD-L1 immune checkpoint blockade in orthotopic murine head and neck squamous cell carcinoma. Oncoimmunology. 2017;6:e1356153. doi: 10.1080/2162402X.2017.1356153.
    1. Aguilera T, Rafat M, Kariolis M, Eyben RV, Graves E, Giaccia A. Tumor immunologic heterogeneity influences response to radiation and combination immunotherapy. J Immunother Cancer. 2015;3:P345. doi: 10.1186/2051-1426-3-S2-P345.
    1. Sharabi AB, Nirschl CJ, Kochel CM, Nirschl TR, Francica BJ, Velarde E, Deweese TL, Drake CG. Stereotactic radiation therapy augments antigen-specific PD-1-mediated antitumor immune responses via cross-presentation of tumor antigen. Cancer Immunol Res. 2015;3:345–355. doi: 10.1158/2326-6066.CIR-14-0196.
    1. Deng L, Liang H, Burnette B, Beckett M, Darga T, Weichselbaum RR, Fu YX. Irradiation and anti-PD-L1 treatment synergistically promote antitumor immunity in mice. J Clin Invest. 2014;124:687–695. doi: 10.1172/JCI67313.
    1. Asna N, Livoff A, Batash R, Debbi R, Schaffer P, Rivkind T, Schaffer M. Radiation therapy and immunotherapy-a potential combination in cancer treatment. Curr Oncol. 2018;25:e454–e460. doi: 10.3747/co.25.4002.
    1. Lazzari C, Karachaliou N, Bulotta A, Viganó M, Mirabile A, Brioschi E, Santarpia M, Gianni L, Rosell R, Gregorc V. Combination of immunotherapy with chemotherapy and radiotherapy in lung cancer: Is this the beginning of the end for cancer? Ther Adv Med Oncol. 2018;10:1758835918762094. doi: 10.1177/1758835918762094.
    1. Ahmed KA, Stallworth DG, Kim Y, Johnstone PA, Harrison LB, Caudell JJ, Yu HH, Etame AB, Weber JS, Gibney GT. Clinical outcomes of melanoma brain metastases treated with stereotactic radiation and anti-PD-1 therapy. Ann Oncol. 2016;27:434–441. doi: 10.1093/annonc/mdw417.
    1. Qian JM, Yu JB, Kluger HM, Chiang VL. Timing and type of immune checkpoint therapy affect the early radiographic response of melanoma brain metastases to stereotactic radiosurgery. Cancer. 2016;122:3051–3058. doi: 10.1002/cncr.30138.
    1. Pike LRG, Bang A, Ott P, Balboni T, Taylor A, Catalano P, Rawal B, Spektor A, Krishnan M, Cagney D, et al. Radiation and PD-1 inhibition: Favorable outcomes after brain-directed radiation. Radiother Oncol. 2017;124:98–103. doi: 10.1016/j.radonc.2017.06.006.
    1. Chen MF, Chen PT, Chen WC, Lu MS, Lin PY, Lee KD. The role of PD-L1 in the radiation response and prognosis for esophageal squamous cell carcinoma related to IL-6 and T-cell immunosuppression. Oncotarget. 2016;7:7913–7924.
    1. Stahl M, Budach W. Definitive chemoradiotherapy. J Thorac Dis. 2017;9(Suppl 8):S792–S798. doi: 10.21037/jtd.2017.05.05.
    1. Matzenauer M, Vrána D, Vlachová Z, Aujesky R, Vrba R, Neoral C, Melichar B. Stereotactic radiotherapy in the treatment of local recurrences of esophageal cancer. Oncol Lett. 2017;13:1807–1810. doi: 10.3892/ol.2017.5605.
    1. Luke JJ, Lemons JM, Karrison TG, Pitroda SP, Melotek JM, Zha Y, Al-Hallaq HA, Arina A, Khodarev NN, Janisch L, et al. Safety and clinical activity of pembrolizumab and multisite stereotactic body radiotherapy in patients with advanced solid tumors. J Clin Oncol. 2018;36:1611–1618. doi: 10.1200/JCO.2017.76.2229.
    1. Wu P, Wu D, Li L, Chai Y, Huang J. PD-L1 and survival in solid tumors: A meta-analysis. PLoS One. 2015;10:e0131403. doi: 10.1371/journal.pone.0131403.
    1. Alsaab HO, Sau S, Alzhrani R, Tatiparti K, Bhise K, Kashaw SK, Iyer AK. PD-1 and PD-L1 checkpoint signaling inhibition for cancer immunotherapy: Mechanism, combinations, and clinical outcome. Front Pharmacol. 2017;8:561. doi: 10.3389/fphar.2017.00561.
    1. Mazel M, Jacot W, Pantel K, Bartkowiak K, Topart D, Cayrefourcq L, Rossille D, Maudelonde T, Fest T, Alix-Panabières C. Frequent expression of PD-L1 on circulating breast cancer cells. Mol Oncol. 2015;9:1773–1782. doi: 10.1016/j.molonc.2015.05.009.
    1. Ilié M, Szafer-Glusman E, Hofman V, Chamorey E, Lalvee S, Selva E, Leroy S, Marquette CH, Kowanetz M, Hedge P, et al. Detection of PD-L1 in circulating tumor cells and white blood cells from patients with advanced non-small-cell lung cancer. Ann Oncol. 2018;29:193–199. doi: 10.1093/annonc/mdx636.
    1. Nicolazzo C, Raimondi C, Mancini M, Caponnetto S, Gradilone A, Gandini O, Mastromartino M, Del Bene G, Prete A, Longo F, et al. Monitoring PD-L1 positive circulating tumor cells in non-small cell lung cancer patients treated with the PD-1 inhibitor nivolumab. Sci Rep. 2016;6:31726. doi: 10.1038/srep31726.
    1. Guibert N, Delaunay M, Lusque A, Boubekeur N, Rouquette I, Clermont E, Mourlanette J, Gouin S, Dormoy I, Favre G, et al. PD-L1 expression in circulating tumor cells of advanced non-small cell lung cancer patients treated with nivolumab. Lung Cancer. 2018;120:108–112. doi: 10.1016/j.lungcan.2018.04.001.
    1. Yue C, Jiang Y, Li P, Wang Y, Xue J, Li N, Li D, Wang R, Dang Y, Hu Z, et al. Dynamic change of PD-L1 expression on circulating tumor cells in advanced solid tumor patients undergoing PD-1 blockade therapy. Oncoimmunology. 2918;7:e1438111. doi: 10.1080/2162402X.2018.1438111.
    1. Zhu X, Lang J. Soluble PD-1 and PD-L1: Predictive and prognostic significance in cancer. Oncotarget. 2017;8:97671–97682.
    1. Cohen EEW, Bell RB, Bifulco CB, Burtness B, Gillison ML, Harrington KJ, Le QT, Lee NY, Leidner R, Lewis RL, et al. The Society for Immunotherapy of Cancer consensus statement on immunotherapy for the treatment of squamous cell carcinoma of the head and neck (HNSCC) J Immunother Cancer. 2019;7:184. doi: 10.1186/s40425-019-0662-5.
    1. Califano J, Leong PL, Koch WM, Eisenberger CF, Sidransky D, Westra WH. Second esophageal tumors in patients with head and neck squamous cell carcinoma: An assessment of clonal relationships. Clin Cancer Res. 1999;5:1862–1867.
    1. The Cancer Genome Atlas Research Network, corp-author. Integrated genomic characterization of oesophageal carcinoma. Nature. 2017;541:169–175. doi: 10.1038/nature20805.
    1. Predina JD, Judy B, Aliperti LA, Fridlender ZG, Blouin A, Kapoor V, Laguna B, Nakagawa H, Rustgi AK, Aguilar L, et al. Neoadjuvant in situ gene-mediated cytotoxic immunotherapy improves postoperative outcomes in novel syngeneic esophageal carcinoma models. Cancer Gene Ther. 2011;18:871–883. doi: 10.1038/cgt.2011.56.
    1. Sharabi AB, Lim M, DeWeese TL, Drake CG. Radiation and checkpoint blockade immunotherapy: Radiosensitisation and potential mechanisms of synergy. Lancet Oncol. 2015;16:e498–509. doi: 10.1016/S1470-2045(15)00007-8.
    1. Marciscano AE, Walker JM, McGee HM, Kim MM, Kunos CA, Monjazeb AM, Shiao SL, Tran PT, Ahmed MM. Incorporating radiation oncology into immunotherapy: Proceedings from the ASTRO-SITC-NCI immunotherapy workshop. J Immunother Cancer. 2018;6:6. doi: 10.1186/s40425-018-0317-y.
    1. Pitt JM, Marabelle A, Eggermont A, Soria JC, Kroemer G, Zitvogel L. Targeting the tumor microenvironment: Removing obstruction to anticancer immune responses and immunotherapy. Anna Oncol. 2016;27:1482–1492. doi: 10.1093/annonc/mdw168.
    1. Tang H, Qiao J, Fu YX. Immunotherapy and tumor microenvironment. Cancer Lett. 2016;370:85–90. doi: 10.1016/j.canlet.2015.10.009.
    1. Schaaf MB, Garg AD, Agostinis P. Defining the role of the tumor vasculature in antitumor immunity and immunotherapy. Cell Death Dis. 2018;9:115. doi: 10.1038/s41419-017-0061-0.
    1. Hendry SA, Farnsworth RH, Solomon B, Achen MG, Stacker SA, Fox SB. The role of the tumor vasculature in the host immune response: Implications for therapeutic strategies targeting the tumor microenvironment. Front Immunol. 2016;7:621. doi: 10.3389/fimmu.2016.00621.
    1. Kallman RF, Dorie MJ. Tumor oxygenation and reoxygenation during radiation therapy: Their importance in predicting tumor response. Int J Radiat Oncol Biol Phys. 1986;12:681–685. doi: 10.1016/0360-3016(86)90080-5.
    1. Jiang W, Chan CK, Weissman IL, Kim BYS, Hahn SM. Immune priming of the tumor microenvironment by radiation. Trends Cancer. 2016;2:638–645. doi: 10.1016/j.trecan.2016.09.007.
    1. Wolchok JD, Hoos A, O'Day S, Weber JS, Hamid O, Lebbé C, Maio M, Binder M, Bohnsack O, Nichol G, et al. Guidelines for the evaluation of immune therapy activity in solid tumors: Immune-related response criteria. Clin Cancer Res. 2009;15:7412–7420. doi: 10.1158/1078-0432.CCR-09-1624.
    1. Somarouthu B, Lee SI, Urban T, Sadow CA, Harris GJ, Kambadakone A. Immune-related tumour response assessment criteria: A comprehensive review. Br J Radiol. 2018;91:20170457. doi: 10.1259/bjr.20170457.
    1. Hoos A, Wolchok JD, Humphrey RW, Hodi FS. CCR 20th anniversary commentary: Immune-related response criteria-capturing clinical activity in immuno-oncology. Clin Cancer Res. 2015;21:4989–4991. doi: 10.1158/1078-0432.CCR-14-3128.
    1. Hodi FS, Hwu WJ, Kefford R, Weber JS, Daud A, Hamid O, Patnaik A, Ribas A, Robert C, Gangadhar TC, et al. Evaluation of immune-related response criteria and RECIST v1.1 in patients with advanced melanoma treated with pembrolizumab. J Clin Oncol. 2016;34:1510–1517. doi: 10.1200/JCO.2015.64.0391.
    1. Postow MA, Sidlow R, Hellmann MD. Immune-related adverse events associated with immune checkpoint blockade. N Engl J Med. 2018;378:158–168. doi: 10.1056/NEJMra1703481.
    1. Yovino S, Grossman SA. Severity, etiology and possible consequences of treatment-related lymphopenia in patients with newly diagnosed high-grade gliomas. CNS Oncol. 2012;1:149–154. doi: 10.2217/cns.12.14.
    1. Davuluri R, Jiang W, Fang P, Xu C, Komaki R, Gomez DR, Welsh J, Cox JD, Crane CH, Hsu CC, Lin SH. Lymphocyte nadir and esophageal cancer survival outcomes after chemoradiation therapy. Int J Radiat Oncol Biol Phys. 2017;99:128–135. doi: 10.1016/j.ijrobp.2017.05.037.
    1. Yamashita H, Haga A, Takenaka R, Kiritoshi T, Okuma K, Ohtomo K, Nakagawa K. Efficacy and feasibility of ambulatory treatment-based monthly nedaplatin plus S-1 in definitive or salvage concurrent chemoradiotherapy for early, advanced, and relapsed esophageal cancer. Radiat Oncol. 2016;11:4. doi: 10.1186/s13014-016-0587-9.
    1. Chen HY, Ma XM, Ye M, Hou YL, Xie HY, Bai YR. Esophageal perforation during or after conformal radiotherapy for esophageal carcinoma. J Radiat Res. 2014;55:940–947. doi: 10.1093/jrr/rru031.
    1. Roeder F, Nicolay NH, Nguyen T, Saleh-Ebrahimi L, Askoxylakis V, Bostel T, Zwicker F, Debus J, Timke C, Huber PE. Intensity modulated radiotherapy (IMRT) with concurrent chemotherapy as definitive treatment of locally advanced esophageal cancer. Radiat Oncol. 2014;9:191. doi: 10.1186/1748-717X-9-191.
    1. Hong MH, Kim H, Park SY, Kim DJ, Lee CG, Cho J, Kim JH, Kim HR, Kim YH, Park SR, Cho BC. A phase II trial of preoperative chemoradiotherapy and pembrolizumab for locally advanced esophageal squamous cell carcinoma (ESCC) J Clin Oncol. 2019;37(15 Suppl):S4027. doi: 10.1200/JCO.2019.37.15_suppl.4027.
    1. Katz M, Bauer TW, Varadhachary G, Acquavella N, Petroni G, Bullock T, Slingluff CL, Rahma OE. A randomized multicenter phase Ib/II study to assess the safety and the immunological effect of chemoradiation therapy (CRT) in combination with pembrolizumab (anti-PD1) to CRT alone in patients with resectable or borderline resectable pancreatic cancer. J Clin Oncol. 2015;3(Suppl 2):P167.
    1. Van Hagen P, Hulshof MC, Van Lanschot JJ, Steyerberg EW, van Berge Henegouwen MI, Wijnhoven BP, Richel DJ, Nieuwenhuijzen GA, Hospers GA, Bonenkamp JJ, et al. Preoperative chemora-diotherapy for esophageal or junctional cancer. N Engl J Med. 2012;366:2074–2084. doi: 10.1056/NEJMoa1112088.
    1. U.S. Department of Health and Human Services, corp-author. Common Terminology Criteria for Adverse Events (CTCAE) v5.0. . [Nov 27;2017 ];

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