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Current Cancer Drug Targets

Editor-in-Chief

ISSN (Print): 1568-0096
ISSN (Online): 1873-5576

Review Article

Immunotherapy for Gastroesophageal Tumors: Is there still Hope for Efficacy?

Author(s): Hannah Christina Puhr and Aysegul Ilhan-Mutlu*

Volume 22, Issue 8, 2022

Published on: 17 March, 2022

Page: [651 - 666] Pages: 16

DOI: 10.2174/1568009622666220117101105

Price: $65

Abstract

Immunotherapy represents one of the biggest breakthroughs of the 21st century and redefined modern cancer treatment. Despite this new approach changing the treatment paradigm in various cancer entities, including lung and head-and-neck cancer, the efficacy of these treatment regimens varies in different patient subgroups, and so far, these treatment regimens have failed to meet the high expectations of gastroesophageal cancer patients. This review discusses new treatment approaches concerning immunotherapy in gastroesophageal cancer patients and sheds some light on ongoing trials and new treatment combinations.

Keywords: Esophageal neoplasm, stomach neoplasm, immunotherapy, immunogenic cell death, gastroesophageal cancer, gastric cancer, esophageal cancer.

Graphical Abstract

[1]
Ferlay, J.; Colombet, M.; Soerjomataram, I.; Mathers, C.; Parkin, D.M.; Piñeros, M.; Znaor, A.; Bray, F. Estimating the global cancer incidence and mortality in 2018: GLOBOCAN sources and methods. Int. J. Cancer, 2019, 144(8), 1941-1953.
[http://dx.doi.org/10.1002/ijc.31937] [PMID: 30350310]
[2]
National Cancer Institute Bethesda MD. SEER Cancer Stat Facts: Esophageal Cancer. Available from: https://seer.cancer.gov/statfacts/html/esoph.html (Accessed 25.11.2019).
[3]
National Cancer Institute Bethesda MD. SEER Cancer Stat Facts: Stomach Cancer. Available from: https://seer.cancer.gov/statfacts/html/stomach.html (Accessed 25.11.2019).
[4]
Vrána, D.; Matzenauer, M.; Neoral, Č.; Aujeský, R.; Vrba, R.; Melichar, B.; Rušarová, N.; Bartoušková, M.; Jankowski, J. From tumor immunology to immunotherapy in gastric and esophageal cancer. Int. J. Mol. Sci., 2018, 20(1), E13.
[http://dx.doi.org/10.3390/ijms20010013] [PMID: 30577521]
[5]
Puhr, H.C.; Preusser, M.; Prager, G.; Ilhan-Mutlu, A. New treatment options for advanced gastroesophageal tumours: Mature for the current practice? Cancers (Basel), 2020, 12(2), E301.
[http://dx.doi.org/10.3390/cancers12020301] [PMID: 32012895]
[6]
Lordick, F.; Shitara, K.; Janjigian, Y.Y. New agents on the horizon in gastric cancer. Ann. Oncol., 2017, 28(8), 1767-1775.
[http://dx.doi.org/10.1093/annonc/mdx051] [PMID: 28184417]
[7]
Kelly, R.J. Immunotherapy for esophageal and gastric cancer. Am. Soc. Clin. Oncol. Educ. Book, 2017, 37, 292-300.
[http://dx.doi.org/10.1200/EDBK_175231] [PMID: 28561677]
[8]
Topalian, S.L.; Hodi, F.S.; Brahmer, J.R.; Gettinger, S.N.; Smith, D.C.; McDermott, D.F.; Powderly, J.D.; Carvajal, R.D.; Sosman, J.A.; Atkins, M.B.; Leming, P.D.; Spigel, D.R.; Antonia, S.J.; Horn, L.; Drake, C.G.; Pardoll, D.M.; Chen, L.; Sharfman, W.H.; Anders, R.A.; Taube, J.M.; McMiller, T.L.; Xu, H.; Korman, A.J.; Jure-Kunkel, M.; Agrawal, S.; McDonald, D.; Kollia, G.D.; Gupta, A.; Wigginton, J.M.; Sznol, M. Safety, activity, and immune correlates of anti-PD-1 antibody in cancer. N. Engl. J. Med., 2012, 366(26), 2443-2454.
[http://dx.doi.org/10.1056/NEJMoa1200690] [PMID: 22658127]
[9]
Robert, C. A decade of immune-checkpoint inhibitors in cancer therapy. Nat. Commun., 2020, 11(1), 3801.
[http://dx.doi.org/10.1038/s41467-020-17670-y] [PMID: 32732879]
[10]
Kang, Y-K.; Boku, N.; Satoh, T.; Ryu, M-H.; Chao, Y.; Kato, K.; Chung, H.C.; Chen, J.S.; Muro, K.; Kang, W.K.; Yeh, K.H.; Yoshikawa, T.; Oh, S.C.; Bai, L.Y.; Tamura, T.; Lee, K.W.; Hamamoto, Y.; Kim, J.G.; Chin, K.; Oh, D.Y.; Minashi, K.; Cho, J.Y.; Tsuda, M.; Chen, L.T. Nivolumab in patients with advanced gastric or gastro-oesophageal junction cancer refractory to, or intolerant of, at least two previous chemotherapy regimens (ONO-4538-12, ATTRACTION-2): A randomised, double-blind, placebo-controlled, phase 3 trial. Lancet, 2017, 390(10111), 2461-2471.
[http://dx.doi.org/10.1016/S0140-6736(17)31827-5] [PMID: 28993052]
[11]
Kato, K.; Cho, B.C.; Takahashi, M.; Okada, M.; Lin, C-Y.; Chin, K.; Kadowaki, S.; Ahn, M.J.; Hamamoto, Y.; Doki, Y.; Yen, C.C.; Kubota, Y.; Kim, S.B.; Hsu, C.H.; Holtved, E.; Xynos, I.; Kodani, M.; Kitagawa, Y. Nivolumab versus chemotherapy in patients with advanced oesophageal squamous cell carcinoma refractory or intolerant to previous chemotherapy (ATTRACTION-3): A multicentre, randomised, open-label, phase 3 trial. Lancet Oncol., 2019, 20(11), 1506-1517.
[http://dx.doi.org/10.1016/S1470-2045(19)30626-6] [PMID: 31582355]
[12]
Administration FaD. FDA approves nivolumab for esophageal squamous cell carcinoma. 2020. Available from: https://www.fda.gov/drugs/drug-approvals-and-databases/fda-approves-nivolumab-esophageal-squamous-cell-carcinoma (Accessed 23/09/2020).
[13]
Agency, E.M. Opdivo: Pending EC decision. 2020. Available from: https://www.ema.europa.eu/en/medicines/human/summaries-opinion/opdivo-1 (Accessed 31/10/2020).
[14]
Martinson, H.A.; Mallari, D.; Richter, C.; Wu, T.T.; Tiesinga, J.; Alberts, S.R.; Olnes, M.J. Molecular classification of gastric cancer among Alaska native people. Cancers (Basel), 2020, 12(1), E198.
[http://dx.doi.org/10.3390/cancers12010198] [PMID: 31941061]
[15]
Satake, H.; Lee, K.W.; Chung, H.C.; Lee, J.; Yamaguchi, K.; Chen, J.-S. Pembrolizumab (pembro) versus standard of care chemotherapy (chemo) in patients with advanced gastric or gastroesophageal junction adenocarcinoma: Asian subgroup analysis of KEYNOTE-062. J. Clin. Oncol., 2020, 38(15_suppl), 4523.
[http://dx.doi.org/10.1200/JCO.2020.38.15_suppl.4523]
[16]
Davis, A.A.; Patel, V.G. The role of PD-L1 expression as a predictive biomarker: an analysis of all US Food and Drug Administration (FDA) approvals of immune checkpoint inhibitors. J. Immunother. Cancer, 2019, 7(1), 278.
[http://dx.doi.org/10.1186/s40425-019-0768-9] [PMID: 31655605]
[17]
Yamashita, K.; Iwatsuki, M.; Ajani, J.A.; Baba, H. Programmed death ligand-1 expression in gastrointestinal cancer: Clinical significance and future challenges. Ann. Gastroenterol. Surg., 2020, 4(4), 369-378.
[http://dx.doi.org/10.1002/ags3.12348] [PMID: 32724880]
[18]
Park, Y.; Koh, J.; Na, H.Y.; Kwak, Y.; Lee, K.-W.; Ahn, S.-H. PD-L1 testing in gastric cancer by the combined positive score of the 22C3 PharmDx and SP263 assay with clinically relevant cut-offs. Cancer Res. Treat., 2020, 52(3), 661-670.
[http://dx.doi.org/10.4143/crt.2019.718]
[19]
Fuchs, C.S.; Doi, T.; Jang, R.W.; Muro, K.; Satoh, T.; Machado, M.; Sun, W.; Jalal, S.I.; Shah, M.A.; Metges, J.P.; Garrido, M.; Golan, T.; Mandala, M.; Wainberg, Z.A.; Catenacci, D.V.; Ohtsu, A.; Shitara, K.; Geva, R.; Bleeker, J.; Ko, A.H.; Ku, G.; Philip, P.; Enzinger, P.C.; Bang, Y.J.; Levitan, D.; Wang, J.; Rosales, M.; Dalal, R.P.; Yoon, H.H. Safety and efficacy of pembrolizumab monotherapy in patients with previously treated advanced gastric and gastroesophageal junction cancer: Phase 2 clinical KEYNOTE-059 trial. JAMA Oncol., 2018, 4(5), e180013.
[http://dx.doi.org/10.1001/jamaoncol.2018.0013] [PMID: 29543932]
[20]
Kojima, T.; Shah, M.A.; Muro, K.; Francois, E.; Adenis, A.; Hsu, C.H.; Doi, T.; Moriwaki, T.; Kim, S.B.; Lee, S.H.; Bennouna, J.; Kato, K.; Shen, L.; Enzinger, P.; Qin, S.K.; Ferreira, P.; Chen, J.; Girotto, G.; de la Fouchardiere, C.; Senellart, H.; Al-Rajabi, R.; Lordick, F.; Wang, R.; Suryawanshi, S.; Bhagia, P.; Kang, S.P.; Metges, J.P. Randomized phase III KEYNOTE-181 study of pembrolizumab versus chemotherapy in advanced esophageal cancer. J. Clin. Oncol., 2020, 38(35), 4138-4148.
[http://dx.doi.org/10.1200/JCO.20.01888] [PMID: 33026938]
[21]
Polom, K.; Marano, L.; Marrelli, D.; De Luca, R.; Roviello, G.; Savelli, V.; Tan, P.; Roviello, F. Meta-analysis of microsatellite instability in relation to clinicopathological characteristics and overall survival in gastric cancer. Br. J. Surg., 2018, 105(3), 159-167.
[http://dx.doi.org/10.1002/bjs.10663] [PMID: 29091259]
[22]
Le, D.T.; Uram, J.N.; Wang, H.; Bartlett, B.R.; Kemberling, H.; Eyring, A.D.; Skora, A.D.; Luber, B.S.; Azad, N.S.; Laheru, D.; Biedrzycki, B.; Donehower, R.C.; Zaheer, A.; Fisher, G.A.; Crocenzi, T.S.; Lee, J.J.; Duffy, S.M.; Goldberg, R.M.; de la Chapelle, A.; Koshiji, M.; Bhaijee, F.; Huebner, T.; Hruban, R.H.; Wood, L.D.; Cuka, N.; Pardoll, D.M.; Papadopoulos, N.; Kinzler, K.W.; Zhou, S.; Cornish, T.C.; Taube, J.M.; Anders, R.A.; Eshleman, J.R.; Vogelstein, B.; Diaz, L.A., Jr PD-1 blockade in tumors with mismatch-repair deficiency. N. Engl. J. Med., 2015, 372(26), 2509-2520.
[http://dx.doi.org/10.1056/NEJMoa1500596] [PMID: 26028255]
[23]
Shitara, K.; Van Cutsem, E.; Bang, Y.J.; Fuchs, C.; Wyrwicz, L.; Lee, K.W.; Kudaba, I.; Garrido, M.; Chung, H.C.; Lee, J.; Castro, H.R.; Mansoor, W.; Braghiroli, M.I.; Karaseva, N.; Caglevic, C.; Villanueva, L.; Goekkurt, E.; Satake, H.; Enzinger, P.; Alsina, M.; Benson, A.; Chao, J.; Ko, A.H.; Wainberg, Z.A.; Kher, U.; Shah, S.; Kang, S.P.; Tabernero, J. Efficacy and safety of pembrolizumab or pembrolizumab plus chemotherapy vs chemotherapy alone for patients with first-line, advanced gastric cancer: The KEYNOTE-062 phase 3 randomized clinical trial. JAMA Oncol., 2020, 6(10), 1571-1580.
[http://dx.doi.org/10.1001/jamaoncol.2020.3370] [PMID: 32880601]
[24]
Shitara, K.; Van Cutsem, E.; Bang, Y.J.; Fuchs, C.S.; Wyrwicz, L.; Lee, K.W. LBA44 - Pembrolizumab with or without chemotherapy vs chemotherapy in patients with advanced G/GEJ cancer (GC) including outcomes according to Microsatellite Instability-High (MSI-H) status in KEYNOTE-062. Ann. Oncol., 2019, 30, v878-v9.
[http://dx.doi.org/10.1093/annonc/mdz394.035]
[25]
Van Cutsem, E.; Valderrama, A.; Bang, Y.J.; Fuchs, C.; Shitara, K.; Janjigian, Y.Y. Health-related quality of life (HRQoL) impact of pembrolizumab (P) versus chemotherapy (C) as first-line (1L) treatment in PD-L1–positive advanced gastric or gastroesophageal junction (G/GEJ) adenocarcinoma. Ann. Oncol., 2019, 30, v879.
[http://dx.doi.org/10.1093/annonc/mdz394.036]
[26]
Results of the JAVELIN Gastric 100 phase 3 trial: avelumab maintenance following first-line (1L) chemotherapy (CTx) vs continuation of CTx for HER2− advanced gastric or gastroesophageal junction cancer. Gastrointestinal Cancers Symposium: American Society of Clinical Oncology, 2020.
[27]
Moehler, M.T.A.P.S. Phase III JAVELIN Gastric 100 Trial Finds No Survival Benefit for Maintenance Avelumab. Available from: https://ascopost.com/issues/march-25-2020-supplement-conference-highlights-gi-cancers/phase-iii-javelin-gastric-100-trial-finds-no-survival-benefit-for-maintenance-avelumab/ (Accessed 24/09/2020).
[28]
Moehler, M.H.; Janjigian, Y.Y.; Adenis, A.; Aucoin, J.-S.; Boku, N.; Chau, I. CheckMate 649: A randomized, multicenter, open-label, phase III study of nivolumab (NIVO) + ipilimumab (IPI) or nivo + chemotherapy (CTX) versus CTX alone in patients with previously untreated advanced (Adv) gastric (G) or gastroesophageal junction (GEJ) cancer. J. Clin. Oncol., 2018, 36(4_suppl), TPS192-TPS.
[http://dx.doi.org/10.1200/JCO.2018.36.4_suppl.TPS192]
[29]
Kato, K.; Shah, M.A.; Enzinger, P.C.; Bennouna, J.; Shen, L.; Adenis, A. Phase III KEYNOTE-590 study of chemotherapy + pembrolizumab versus chemotherapy + placebo as first-line therapy for patients (Pts) with advanced esophageal or esophagogastric junction (E/EGJ) cancer. Ann. Oncol., 2018, 29, viii- 268-viii269.
[http://dx.doi.org/10.1093/annonc/mdy282.168]
[30]
Moehler, M.; Shitara, K.; Garrido, M.; Salman, P.; Shen, L.; Wyrwicz, L. LBA6_PR Nivolumab (nivo) plus chemotherapy (chemo) versus chemo as first-line (1L) treatment for advanced gastric cancer/gastroesophageal junction cancer (GC/GEJC)/esophageal adenocarcinoma (EAC): First results of the CheckMate 649 study. Ann. Oncol., 2020, 31, S1191.
[http://dx.doi.org/10.1016/j.annonc.2020.08.2296]
[31]
Kato, K.; Sun, J.M.; Shah, M.A.; Enzinger, P.C.; Adenis, A.; Doi, T. LBA8_PR Pembrolizumab plus chemotherapy versus chemotherapy as first-line therapy in patients with advanced esophageal cancer: The phase 3 KEYNOTE-590 study. Ann. Oncol., 2020, 31, S1192-S3.
[http://dx.doi.org/10.1016/j.annonc.2020.08.2298]
[32]
Ochoa de Olza, M.; Navarro Rodrigo, B.; Zimmermann, S.; Coukos, G. Turning up the heat on non-immunoreactive tumours: Opportunities for clinical development. Lancet Oncol., 2020, 21(9), e419-e430.
[http://dx.doi.org/10.1016/S1470-2045(20)30234-5] [PMID: 32888471]
[33]
Li, J.; Byrne, K.T.; Yan, F.; Yamazoe, T.; Chen, Z.; Baslan, T.; Richman, L.P.; Lin, J.H.; Sun, Y.H.; Rech, A.J.; Balli, D.; Hay, C.A.; Sela, Y.; Merrell, A.J.; Liudahl, S.M.; Gordon, N.; Norgard, R.J.; Yuan, S.; Yu, S.; Chao, T.; Ye, S.; Eisinger-Mathason, T.S.K.; Faryabi, R.B.; Tobias, J.W.; Lowe, S.W.; Coussens, L.M.; Wherry, E.J.; Vonderheide, R.H.; Stanger, B.Z. Tumor cell-intrinsic factors underlie heterogeneity of immune cell infiltration and response to immunotherapy. Immunity, 2018, 49(1), 178-193.e7.
[http://dx.doi.org/10.1016/j.immuni.2018.06.006] [PMID: 29958801]
[34]
Sato, H.; Okonogi, N.; Nakano, T. Rationale of combination of anti-PD-1/PD-L1 antibody therapy and radiotherapy for cancer treatment. Int. J. Clin. Oncol., 2020, 25(5), 801-809.
[http://dx.doi.org/10.1007/s10147-020-01666-1] [PMID: 32246277]
[35]
Mamdani, H.; Schneider, B.J.; Kasi, P.M.; Abushahin, L.I.; Birdas, T.J.; Kesler, K. Durvalumab following multimodality therapy for locally advanced esophageal and GEJ adenocarcinoma: Updated survival and early translational results from Big Ten Cancer Research Consortium Study. J. Clin. Oncol., 2020, 38(15-suppl), 4572.
[http://dx.doi.org/10.1200/JCO.2020.38.15_suppl.4572]
[36]
Hong, M.H.; Kim, H.; Park, S.Y.; Kim, D.J.; Lee, C.G.; Cho, J. A phase II trial of preoperative chemoradiotherapy and pembrolizumab for locally advanced esophageal squamous cell carcinoma (ESCC). J. Clin. Oncol., 2019, 37(15_suppl), 4027.
[http://dx.doi.org/10.1200/JCO.2019.37.15_suppl.4027]
[37]
Uboha, N.V.; Maloney, J.D.; McCarthy, D.; Deming, D.A.; LoConte, N.K.; Matkowskyj, K. Safety of neoadjuvant chemoradiation (CRT) in combination with avelumab (A) in the treatment of resectable esophageal and gastroesophageal junction (E/GEJ) cancer. J. Clin. Oncol., 2019, 37(15_suppl), 4041.
[http://dx.doi.org/10.1200/JCO.2019.37.15_suppl.4041]
[38]
van den Ende, T.; de Clercq, N.C.; van Berge Henegouwen, M.I.; Gisbertz, S.S.; Meijer, S.L.; Schokker, S. A phase II feasibility trial of neoadjuvant chemoradiotherapy combined with atezolizumab for resectable esophageal adenocarcinoma: The PERFECT trial. J. Clin. Oncol., 2019, 37(15_suppl), 4045.
[http://dx.doi.org/10.1200/JCO.2019.37.15_suppl.4045]
[39]
Kelly, R.J.; Ajani, J.A.; Kuzdzal, J.; Zander, T.; Van Cutsem, E.; Piessen, G. LBA9_PR Adjuvant nivolumab in resected esophageal or gastroesophageal junction cancer (EC/GEJC) following neoadjuvant chemoradiation therapy (CRT): First results of the CheckMate 577 study. Ann. Oncol., 2020, 31, S1193-S4.
[http://dx.doi.org/10.1016/j.annonc.2020.08.2299]
[40]
Fukumura, D.; Kloepper, J.; Amoozgar, Z.; Duda, D.G.; Jain, R.K. Enhancing cancer immunotherapy using antiangiogenics: Opportunities and challenges. Nat. Rev. Clin. Oncol., 2018, 15(5), 325-340.
[http://dx.doi.org/10.1038/nrclinonc.2018.29] [PMID: 29508855]
[41]
Smyth, E.C. Regorafenib in gastric cancer. Transl. Gastroenterol. Hepatol., 2017, 2(3), 16.
[http://dx.doi.org/10.21037/tgh.2017.01.07]
[42]
Fukuoka, S.; Hara, H.; Takahashi, N.; Kojima, T.; Kawazoe, A.; Asayama, M.; Yoshii, T.; Kotani, D.; Tamura, H.; Mikamoto, Y.; Hirano, N.; Wakabayashi, M.; Nomura, S.; Sato, A.; Kuwata, T.; Togashi, Y.; Nishikawa, H.; Shitara, K. Regorafenib plus nivolumab in patients with advanced gastric or colorectal cancer: an open-label, dose-escalation, and dose-expansion phase Ib Trial (REGONIVO, EPOC1603). J. Clin. Oncol., 2020, 38(18), 2053-2061.
[http://dx.doi.org/10.1200/JCO.19.03296] [PMID: 32343640]
[43]
Hironaka, S.; Kadowaki, S.; Izawa, N.; Nishina, T.; Yamanaka, T.; Minashi, K A phase I/II study of nivolumab, paclitaxel, and ramucirumab as second-line in advanced gastric cancer. J. Clin. Oncol., 2020, 38(4_suppl), 352.
[http://dx.doi.org/10.1200/JCO.2020.38.4_suppl.352]
[44]
Kawazoe, A.; Fukuoka, S.; Nakamura, Y.; Kuboki, Y.; Wakabayashi, M.; Nomura, S.; Mikamoto, Y.; Shima, H.; Fujishiro, N.; Higuchi, T.; Sato, A.; Kuwata, T.; Shitara, K. Lenvatinib plus pembrolizumab in patients with advanced gastric cancer in the first-line or second-line setting (EPOC1706): an open-label, single-arm, phase 2 trial. Lancet Oncol., 2020, 21(8), 1057-1065.
[http://dx.doi.org/10.1016/S1470-2045(20)30271-0] [PMID: 32589866]
[45]
Saeed, A.; Koestler, D.; Williamson, S.K.; Baranda, J.C.; Sun, W.; Al-Rajabi, R.M.d.T A phase Ib trial of cabozantinib in combination with durvalumab (MEDI4736) in previously treated patients with advanced gastroesophageal cancer and other gastrointestinal (GI) malignancies (CAMILLA). J. Clin. Oncol., 2019, 37(8_suppl), TPS56-TPS.
[http://dx.doi.org/10.1200/JCO.2019.37.8_suppl.TPS56]
[46]
Bang, Y-J.; Golan, T.; Lin, C-C.; Dahan, L.; Fu, S.; Moreno, V. Ramucirumab (Ram) and durvalumab (Durva) treatment of metastatic non-small cell lung cancer (NSCLC), gastric/gastroesophageal junction (G/GEJ) adenocarcinoma, and hepatocellular carcinoma (HCC) following progression on systemic treatment(s). Journal of Clinical Oncology, 2019, 37(15_suppl), 2528.
[http://dx.doi.org/10.1200/JCO.2019.37.15_suppl.2528]
[47]
Fonkoua, L.A.K.; Chakrabarti, S.; Sonbol, M.B.; Kasi, P.M.; Starr, J.S.; Liu, A.J. Enhanced efficacy of anti-VEGFR2/taxane therapy after progression on immune checkpoint inhibition (ICI) in patients (pts) with metastatic gastroesophageal adenocarcinoma (mGEA). J. Clin. Oncol., 2020, 38(15-suppl), 4541.
[http://dx.doi.org/10.1200/JCO.2020.38.15_suppl.4541]
[48]
Szabados, B.; van Dijk, N.; Tang, Y.Z.; van der Heijden, M.S.; Wimalasingham, A.; Gomez de Liano, A.; Chowdhury, S.; Hughes, S.; Rudman, S.; Linch, M.; Powles, T. Response rate to chemotherapy after immune checkpoint inhibition in metastatic urothelial cancer. Eur. Urol., 2018, 73(2), 149-152.
[http://dx.doi.org/10.1016/j.eururo.2017.08.022] [PMID: 28917596]
[49]
Shiono, A.; Kaira, K.; Mouri, A.; Yamaguchi, O.; Hashimoto, K.; Uchida, T.; Miura, Y.; Nishihara, F.; Murayama, Y.; Kobayashi, K.; Kagamu, H. Improved efficacy of ramucirumab plus docetaxel after nivolumab failure in previously treated non-small cell lung cancer patients. Thorac. Cancer, 2019, 10(4), 775-781.
[http://dx.doi.org/10.1111/1759-7714.12998] [PMID: 30809973]
[50]
Bang, Y.J.; Van Cutsem, E.; Feyereislova, A.; Chung, H.C.; Shen, L.; Sawaki, A.; Lordick, F.; Ohtsu, A.; Omuro, Y.; Satoh, T.; Aprile, G.; Kulikov, E.; Hill, J.; Lehle, M.; Rüschoff, J.; Kang, Y.K. ToGA Trial Investigators. Trastuzumab in combination with chemotherapy versus chemotherapy alone for treatment of HER2- positive advanced gastric or gastro-oesophageal junction cancer (ToGA): A phase 3, open-label, randomised controlled trial. Lancet, 2010, 376(9742), 687-697.
[http://dx.doi.org/10.1016/S0140-6736(10)61121-X] [PMID: 20728210]
[51]
Shen, J.Y.C.; Usher, J.; Samberg, D.; Ishiba, T.; Danenberg, K.; Lenz, H.-J. PD-L1 and HER2 expression in gastric cancer (GC) patients (pts) using cell-free RNA (cfRNA). J. Clin. Oncol., 2016, 34(15_suppl), e15539-e.
[http://dx.doi.org/10.1200/JCO.2016.34.15_suppl.e15539]
[52]
Beer, A.; Taghizadeh, H.; Schiefer, A-I.; Puhr, H.C.; Karner, A.K.; Jomrich, G.; Schoppmann, S.F.; Kain, R.; Preusser, M.; Ilhan-Mutlu, A. PD-L1 and HER2 expression in gastroesophageal cancer: A matched case control study. Pathol. Oncol. Res., 2020, 26(4), 2225-2235.
[http://dx.doi.org/10.1007/s12253-020-00814-2] [PMID: 32372174]
[53]
Janjigian, Y.Y.; Maron, S.B.; Chatila, W.K.; Millang, B.; Chavan, S.S.; Alterman, C.; Chou, J.F.; Segal, M.F.; Simmons, M.Z.; Momtaz, P.; Shcherba, M.; Ku, G.Y.; Zervoudakis, A.; Won, E.S.; Kelsen, D.P.; Ilson, D.H.; Nagy, R.J.; Lanman, R.B.; Ptashkin, R.N.; Donoghue, M.T.A.; Capanu, M.; Taylor, B.S.; Solit, D.B.; Schultz, N.; Hechtman, J.F. First-line pembrolizumab and trastuzumab in HER2-positive oesophageal, gastric, or gastro-oesophageal junction cancer: An open-label, single-arm, phase 2 trial. Lancet Oncol., 2020, 21(6), 821-831.
[http://dx.doi.org/10.1016/S1470-2045(20)30169-8] [PMID: 32437664]
[54]
Janjigian, Y.Y.; Bang, Y.-J.; Fuchs, C.S.; Qin, S.; Satoh, T.; Shitara, K. KEYNOTE-811 pembrolizumab plus trastuzumab and chemotherapy for HER2+ metastatic gastric or gastroesophageal junction cancer (mG/GEJC): A double-blind, randomized, placebo- controlled phase 3 study. J. Clin. Oncol., 2019, 37(15_suppl), TPS4146-TPS.
[http://dx.doi.org/10.1200/JCO.2019.37.15_suppl.TPS4146]
[55]
Takahari, D.; Shoji, H.; Minashi, K.; Hara, H.; Chin, K.; Ooki, A. A phase Ib study of nivolumab plus trastuzumab with S-1/capecitabine plus oxaliplatin for HER2-positive advanced gastric cancer (Ni-HIGH study): Safety evaluation. J. Clin. Oncol., 2020, 38(15_suppl), 4525.
[http://dx.doi.org/10.1200/JCO.2020.38.15_suppl.4525]
[56]
Larkin, J.; Chiarion-Sileni, V.; Gonzalez, R.; Grob, J-J.; Rutkowski, P.; Lao, C.D.; Cowey, C.L.; Schadendorf, D.; Wagstaff, J.; Dummer, R.; Ferrucci, P.F.; Smylie, M.; Hogg, D.; Hill, A.; Márquez-Rodas, I.; Haanen, J.; Guidoboni, M.; Maio, M.; Schöffski, P.; Carlino, M.S.; Lebbé, C.; McArthur, G.; Ascierto, P.A.; Daniels, G.A.; Long, G.V.; Bastholt, L.; Rizzo, J.I.; Balogh, A.; Moshyk, A.; Hodi, F.S.; Wolchok, J.D. Five-year survival with combined nivolumab and ipilimumab in advanced melanoma. N. Engl. J. Med., 2019, 381(16), 1535-1546.
[http://dx.doi.org/10.1056/NEJMoa1910836] [PMID: 31562797]
[57]
Motzer, R.J.; Tannir, N.M.; McDermott, D.F.; Arén Frontera, O.; Melichar, B.; Choueiri, T.K.; Plimack, E.R.; Barthélémy, P.; Porta, C.; George, S.; Powles, T.; Donskov, F.; Neiman, V.; Kollmannsberger, C.K.; Salman, P.; Gurney, H.; Hawkins, R.; Ravaud, A.; Grimm, M.O.; Bracarda, S.; Barrios, C.H.; Tomita, Y.; Castellano, D.; Rini, B.I.; Chen, A.C.; Mekan, S.; McHenry, M.B.; Wind-Rotolo, M.; Doan, J.; Sharma, P.; Hammers, H.J.; Escudier, B. CheckMate 214 Investigators. Nivolumab plus Ipilimumab versus sunitinib in advanced renal-cell carcinoma. N. Engl. J. Med., 2018, 378(14), 1277-1290.
[http://dx.doi.org/10.1056/NEJMoa1712126] [PMID: 29562145]
[58]
Camacho, L.H. CTLA-4 blockade with ipilimumab: Biology, safety, efficacy, and future considerations. Cancer Med., 2015, 4(5), 661-672.
[http://dx.doi.org/10.1002/cam4.371] [PMID: 25619164]
[59]
Letendre, P.; Monga, V.; Milhem, M.; Zakharia, Y. Ipilimumab: From preclinical development to future clinical perspectives in melanoma. Future Oncol., 2017, 13(7), 625-636.
[http://dx.doi.org/10.2217/fon-2016-0385] [PMID: 27882779]
[60]
Janjigian, Y.Y.; Bendell, J.; Calvo, E.; Kim, J.W.; Ascierto, P.A.; Sharma, P.; Ott, P.A.; Peltola, K.; Jaeger, D.; Evans, J.; de Braud, F.; Chau, I.; Harbison, C.T.; Dorange, C.; Tschaika, M.; Le, D.T. CheckMate-032 study: Efficacy and safety of nivolumab and nivolumab plus ipilimumab in patients with metastatic esophagogastric cancer. J. Clin. Oncol., 2018, 36(28), 2836-2844.
[http://dx.doi.org/10.1200/JCO.2017.76.6212] [PMID: 30110194]
[61]
Al-Batran, S.-E.; Pauligk, C.; Goetze, T.O.; Riera-Knorrenschild, J.; Goekkurt, E.; Angermeier, S. Modified FOLFOX versus modified FOLFOX plus nivolumab and ipilimumab in patients with previously untreated advanced or metastatic adenocarcinoma of the stomach or gastroesophageal junction: Moonlight, a randomized phase 2 trial of the German Gastric Group of the AIO. J. Clin. Oncol., 2019, 37(15_suppl), TPS4144-TPS.
[http://dx.doi.org/10.1200/JCO.2019.37.15_suppl.TPS4144]
[62]
Puhr, H.C.; Ilhan-Mutlu, A. New emerging targets in cancer immunotherapy: the role of LAG3. ESMO Open, 2019, 4(2), e000482.
[http://dx.doi.org/10.1136/esmoopen-2018-000482] [PMID: 31231559]
[63]
Andrews, L.P.; Marciscano, A.E.; Drake, C.G.; Vignali, D.A.A. LAG3 (CD223) as a cancer immunotherapy target. Immunol. Rev., 2017, 276(1), 80-96.
[http://dx.doi.org/10.1111/imr.12519] [PMID: 28258692]
[64]
Woo, S.R.; Turnis, M.E.; Goldberg, M.V.; Bankoti, J.; Selby, M.; Nirschl, C.J.; Bettini, M.L.; Gravano, D.M.; Vogel, P.; Liu, C.L.; Tangsombatvisit, S.; Grosso, J.F.; Netto, G.; Smeltzer, M.P.; Chaux, A.; Utz, P.J.; Workman, C.J.; Pardoll, D.M.; Korman, A.J.; Drake, C.G.; Vignali, D.A. Immune inhibitory molecules LAG-3 and PD-1 synergistically regulate T-cell function to promote tumoral immune escape. Cancer Res., 2012, 72(4), 917-927.
[http://dx.doi.org/10.1158/0008-5472.CAN-11-1620] [PMID: 22186141]
[65]
Feeney, K.; Kelly, R.; Lipton, L.R.; Chao, J.; Acosta-Rivera, M.; Earle, D. CA224-060: A randomized, open label, phase II trial of relatlimab (anti-LAG-3) and nivolumab with chemotherapy versus nivolumab with chemotherapy as first-line treatment in patients with gastric or gastroesophageal junction adenocarcinoma. J. Clin. Oncol., 2019, 37(15_suppl), TPS4143-TPS.
[http://dx.doi.org/10.1200/JCO.2019.37.15_suppl.TPS4143]
[66]
Aanur, P.; Gutierrez, M.; Kelly, R.J.; Ajani, J.A.; Ku, G.Y.; Denlinger, C.S. FRACTION (Fast Real-time Assessment of Combination Therapies in Immuno-Oncology)-Gastric Cancer (GC): A randomized, open-label, adaptive, phase 2 study of nivolumab in combination with other Immuno-Oncology (IO) agents in patients with advanced GC. J. Clin. Oncol., 2017, 35(15_suppl), TPS4137-TPS.
[http://dx.doi.org/10.1200/JCO.2017.35.15_suppl.TPS4137]
[67]
Qin, S.; Xu, L.; Yi, M.; Yu, S.; Wu, K.; Luo, S. Novel immune checkpoint targets: Moving beyond PD-1 and CTLA-4. Mol. Cancer, 2019, 18(1), 155.
[http://dx.doi.org/10.1186/s12943-019-1091-2]
[68]
Alves Costa Silva, C.; Facchinetti, F.; Routy, B.; Derosa, L. New pathways in immune stimulation: targeting OX40. ESMO Open, 2020, 5(1), e000573.
[http://dx.doi.org/10.1136/esmoopen-2019-000573] [PMID: 32392177]
[69]
Al-Batran, S.-E.; Pauligk, C.; Hofheinz, R.; Lorenzen, S.; Wicki, A.; Siebenhuener, A.R. Perioperative atezolizumab in combination with FLOT versus FLOT alone in patients with resectable esophagogastric adenocarcinoma: DANTE, a randomized, open-label phase II trial of the German Gastric Group of the AIO and the SAKK. J. Clin. Oncol., 2019, 37(15_suppl), TPS4142-TPS.
[http://dx.doi.org/10.1200/JCO.2019.37.15_suppl.TPS4142]
[70]
Homann, N.; Lorenzen, S.; Schenk, M.; Thuss-Patience, P.C.; Goekkurt, E.; Hofheinz, R.D. Interim safety analysis of the DANTE trial: Perioperative atezolizumab in combination with FLOT versus FLOT alone in patients with resectable esophagogastric adenocarcinoma-A randomized, open-label phase II trial of the German Gastric Group at the AIO and SAKK. J. Clin. Oncol., 2020, 38(15_suppl), 4549.
[http://dx.doi.org/10.1200/JCO.2020.38.15_suppl.4549]
[71]
Davidson, M.; Mansukhani, S.; Starling, N.; Chau, I.; Watkins, D.; Cunningham, D. 674PD - Perioperative FLOT + anti-PD-L1 avelumab (FLOT-A) chemo-immunotherapy in resectable oesophagogastric adenocarcinoma (OGA): Safety and biomarker data from the ICONIC trial safety run-in. Ann. Oncol., 2019, 30, v254.
[http://dx.doi.org/10.1093/annonc/mdz247.002]
[72]
Bang, Y.J.; Van Cutsem, E.; Fuchs, C.S.; Ohtsu, A.; Tabernero, J.; Ilson, D.H. Phase III KEYNOTE-585 study of chemotherapy (Chemo) + pembrolizumab (Pembro) vs chemo + placebo as neoadjuvant/adjuvant treatment for patients (Pts) with gastric or gastroesophageal junction (G/GEJ) cancer. Ann. Oncol., 2018, 29, viii268.
[http://dx.doi.org/10.1093/annonc/mdy282.167]
[73]
Smyth, E.; Knödler, M.; Giraut, A.; Mauer, M.; Nilsson, M.; Van Grieken, N.; Wagner, A.D.; Moehler, M.; Lordick, F. VESTIGE: Adjuvant immunotherapy in patients with resected esophageal, gastroesophageal junction and gastric cancer following preoperative chemotherapy with high risk for recurrence (N+ and/or R1): An open label randomized controlled phase-2-study. Front. Oncol., 2020, 9, 1320.
[http://dx.doi.org/10.3389/fonc.2019.01320] [PMID: 32083013]
[74]
Wei, J.; Liu, Q.; Sha, H.; Qian, H.; Shao, J.; Zhu, L. Personalized neoantigen/cancer testis antigen nanovaccine (PVAC) in combination with PD-1 monoclonal antibody and/or antiangiogenic treatment in patients with metastatic solid tumors. J. Clin. Oncol., 2020, 38(15_suppl), 3134.
[http://dx.doi.org/10.1200/JCO.2020.38.15_suppl.3134]
[75]
Zhan, X.; Wang, B.; Li, Z.; Li, J.; Wang, H.; Chen, L. Phase I trial of Claudin 18.2-specific chimeric antigen receptor T cells for advanced gastric and pancreatic adenocarcinoma. J. Clin. Oncol., 2019, 37(15_suppl), 2509.
[http://dx.doi.org/10.1200/JCO.2019.37.15_suppl.2509]
[76]
Puhr, H.; Ilhan-Mutlu, A. Molecular profiling in gastroesophageal cancer-clinical routine and future perspective. memo -. Mag. Eur. Med. Oncol., 2020, 13, 440-444.
[http://dx.doi.org/10.1007/s12254-019-00534-7]
[77]
Kulangara, K.; Hanks, D.A.; Waldroup, S.; Peltz, L.; Shah, S.; Roach, C. Development of the Combined Positive Score (CPS) for the evaluation of PD-L1 in solid tumors with the immunohistochemistry assay PD-L1 IHC 22C3 pharmDx. J. Clin. Oncol., 2017, 35(15_suppl), e14589-e.
[http://dx.doi.org/10.1200/JCO.2017.35.15_suppl.e14589]
[78]
Yamashita, K.; Iwatsuki, M.; Harada, K.; Eto, K.; Hiyoshi, Y.; Ishimoto, T. Prognostic impacts of the combined positive score and the tumor proportion score for programmed death ligand-1 expression by double immunohistochemical staining in patients with advanced gastric cancer. Gastric Cancer, 2020, 23(1), 95-104.
[http://dx.doi.org/10.1007/s10120-019-00999-9]
[79]
Tabernero, J. Pembrolizumab with or without chemotherapy versus chemotherapy for advanced gastric or gastroesophageal junction (G/GEJ) adenocarcinoma: The phase III KEYNOTE-062 study. ASCO Annual Meeting: American Society of Clinical Oncology, 2019.
[80]
Humphries, M.P. A digital pathology demonstration of an "immune hot" ICOS+/CD45RO+ immunephenotype and the impact on survival in patients with esophageal adenocarcinoma. ASCO Annual Meeting: American Society of Clinical Oncology, 2019.
[81]
Nishikawa, J.; Iizasa, H.; Yoshiyama, H.; Shimokuri, K.; Kobayashi, Y.; Sasaki, S.; Nakamura, M.; Yanai, H.; Sakai, K.; Suehiro, Y.; Yamasaki, T.; Sakaida, I. Clinical importance of Epstein-Barr virus-associated gastric cancer. Cancers (Basel), 2018, 10(6), 167.
[http://dx.doi.org/10.3390/cancers10060167] [PMID: 29843478]
[82]
Camargo, M.C.; Murphy, G.; Koriyama, C.; Pfeiffer, R.M.; Kim, W.H.; Herrera-Goepfert, R.; Corvalan, A.H.; Carrascal, E.; Abdirad, A.; Anwar, M.; Hao, Z.; Kattoor, J.; Yoshiwara-Wakabayashi, E.; Eizuru, Y.; Rabkin, C.S.; Akiba, S. Determinants of Epstein-Barr virus-positive gastric cancer: An international pooled analysis. Br. J. Cancer, 2011, 105(1), 38-43.
[http://dx.doi.org/10.1038/bjc.2011.215] [PMID: 21654677]
[83]
Tavakoli, A.; Monavari, S.H.; Solaymani Mohammadi, F.; Kiani, S.J.; Armat, S.; Farahmand, M. Association between Epstein-Barr virus infection and gastric cancer: a systematic review and meta-analysis. BMC Cancer, 2020, 20(1), 493.
[http://dx.doi.org/10.1186/s12885-020-07013-x] [PMID: 32487043]
[84]
Cancer Genome Atlas Research Network. Comprehensive molecular characterization of gastric adenocarcinoma. Nature, 2014, 513(7517), 202-209.
[http://dx.doi.org/10.1038/nature13480] [PMID: 25079317]
[85]
Cho, J.; Kang, M.S.; Kim, K.M. Epstein-Barr virus-associated gastric carcinoma and specific features of the accompanying immune response. J. Gastric Cancer, 2016, 16(1), 1-7.
[http://dx.doi.org/10.5230/jgc.2016.16.1.1] [PMID: 27104020]
[86]
Ma, C.; Patel, K.; Singhi, A.D.; Ren, B.; Zhu, B.; Shaikh, F.; Sun, W. Programmed death-ligand 1 expression is common in gastric cancer associated with Epstein-Barr virus or microsatellite instability. Am. J. Surg. Pathol., 2016, 40(11), 1496-1506.
[http://dx.doi.org/10.1097/PAS.0000000000000698] [PMID: 27465786]
[87]
Derks, S.; Liao, X.; Chiaravalli, A.M.; Xu, X.; Camargo, M.C.; Solcia, E.; Sessa, F.; Fleitas, T.; Freeman, G.J.; Rodig, S.J.; Rabkin, C.S.; Bass, A.J. Abundant PD-L1 expression in Epstein-Barr Virus-infected gastric cancers. Oncotarget, 2016, 7(22), 32925-32932.
[http://dx.doi.org/10.18632/oncotarget.9076] [PMID: 27147580]
[88]
Kim, S.T.; Cristescu, R.; Bass, A.J.; Kim, K.M.; Odegaard, J.I.; Kim, K.; Liu, X.Q.; Sher, X.; Jung, H.; Lee, M.; Lee, S.; Park, S.H.; Park, J.O.; Park, Y.S.; Lim, H.Y.; Lee, H.; Choi, M.; Talasaz, A.; Kang, P.S.; Cheng, J.; Loboda, A.; Lee, J.; Kang, W.K. Comprehensive molecular characterization of clinical responses to PD-1 inhibition in metastatic gastric cancer. Nat. Med., 2018, 24(9), 1449-1458.
[http://dx.doi.org/10.1038/s41591-018-0101-z] [PMID: 30013197]
[89]
Xie, T.; Liu, Y.; Zhang, Z.; Zhang, X.; Gong, J.; Qi, C.; Li, J.; Shen, L.; Peng, Z. Positive status of epstein-barr virus as a biomarker for gastric cancer immunotherapy: A prospective observational study. J. Immunother., 2020, 43(4), 139-144.
[http://dx.doi.org/10.1097/CJI.0000000000000316] [PMID: 32134806]
[90]
Engstrand, L.; Graham, D.Y. Microbiome and gastric cancer. Dig. Dis. Sci., 2020, 65(3), 865-873.
[http://dx.doi.org/10.1007/s10620-020-06101-z] [PMID: 32040665]
[91]
Brawner, K.M.; Morrow, C.D.; Smith, P.D. Gastric microbiome and gastric cancer. Cancer J., 2014, 20(3), 211-216.
[http://dx.doi.org/10.1097/PPO.0000000000000043] [PMID: 24855010]
[92]
Fessler, J; Matson, V; Gajewski, TF Exploring the emerging role of the microbiome in cancer immunotherapy. J. Immunother. Cancer, 2019, 7(1), 108.
[http://dx.doi.org/10.1186/s40425-019-0574-4]
[93]
Maron, S.B.; Vanderbilt, C.; Sabwa, S.; Bowman, A.; Chatila, W.K.; Tang, L.H. PD-L1 positive esophagogastric (EG) cancer is associated with distinct bacteria. J. Clin. Oncol., 2020, 38(15_suppl), 4568.
[http://dx.doi.org/10.1200/JCO.2020.38.15_suppl.4568]
[94]
Pinato, D.J.; Howlett, S.; Ottaviani, D.; Urus, H.; Patel, A.; Mineo, T.; Brock, C.; Power, D.; Hatcher, O.; Falconer, A.; Ingle, M.; Brown, A.; Gujral, D.; Partridge, S.; Sarwar, N.; Gonzalez, M.; Bendle, M.; Lewanski, C.; Newsom-Davis, T.; Allara, E.; Bower, M. Association of prior antibiotic treatment with survival and response to immune checkpoint inhibitor therapy in patients with cancer. JAMA Oncol., 2019, 5(12), 1774-1778.
[http://dx.doi.org/10.1001/jamaoncol.2019.2785] [PMID: 31513236]
[95]
Rizvi, N.A.; Hellmann, M.D.; Snyder, A.; Kvistborg, P.; Makarov, V.; Havel, J.J.; Lee, W.; Yuan, J.; Wong, P.; Ho, T.S.; Miller, M.L.; Rekhtman, N.; Moreira, A.L.; Ibrahim, F.; Bruggeman, C.; Gasmi, B.; Zappasodi, R.; Maeda, Y.; Sander, C.; Garon, E.B.; Merghoub, T.; Wolchok, J.D.; Schumacher, T.N.; Chan, T.A. Cancer immunology. Mutational landscape determines sensitivity to PD-1 blockade in non-small cell lung cancer. Science, 2015, 348(6230), 124-128.
[http://dx.doi.org/10.1126/science.aaa1348] [PMID: 25765070]
[96]
Kim, J.Y.; Kronbichler, A.; Eisenhut, M.; Hong, S.H.; van der Vliet, H.J.; Kang, J.; Shin, J.I.; Gamerith, G. Tumor mutational burden and efficacy of immune checkpoint inhibitors: A systematic review and meta-analysis. Cancers (Basel), 2019, 11(11), 1798.
[http://dx.doi.org/10.3390/cancers11111798] [PMID: 31731749]
[97]
Fuchs, C.S.; Özgüroğlu, M.; Bang, Y.-J.; Di Bartolomeo, M.; Mandalà, M.; Ryu, M.-h. The association of molecular biomarkers with efficacy of pembrolizumab versus paclitaxel in patients with gastric cancer (GC) from KEYNOTE-061. J. Clin. Oncol., 2020, 38(15_suppl), 4512.
[http://dx.doi.org/10.1200/JCO.2020.38.15_suppl.4512]
[98]
Shitara, K.; Özgüroğlu, M.; Bang, Y.-J.; Bartolomeo, M.D.; Mandalà, M.; Ryu, M.-h. The association of tissue tumor mutational burden (tTMB) using the Foundation Medicine genomic platform with efficacy of pembrolizumab versus paclitaxel in patients (pts) with gastric cancer (GC) from KEYNOTE-061. J. Clin. Oncol., 2020, 38(15_suppl), 4537.
[http://dx.doi.org/10.1200/JCO.2020.38.15_suppl.4537]
[99]
Administration FaD. FDA approves pembrolizumab for adults and children with TMB-H solid tumors. 2020. Available from: https://www.fda.gov/drugs/drug-approvals-and-databases/fda-approves-pembrolizumab-adults-and-children-tmb-h-solid-tumors (Accessed 01/11/2020).
[100]
Grenader, T.; Waddell, T.; Peckitt, C.; Oates, J.; Starling, N.; Cunningham, D.; Bridgewater, J. Prognostic value of neutrophil-to- lymphocyte ratio in advanced oesophago-gastric cancer: Exploratory analysis of the REAL-2 trial. Ann. Oncol., 2016, 27(4), 687-692.
[http://dx.doi.org/10.1093/annonc/mdw012] [PMID: 26787231]
[101]
Zhou, D.; Wu, Y.; Zhu, Y.; Lin, Z.; Yu, D.; Zhang, T. The prognostic value of neutrophil-to-lymphocyte ratio and monocyte-to- lymphocyte ratio in metastatic gastric cancer treated with systemic chemotherapy. J. Cancer, 2020, 11(14), 4205-4212.
[http://dx.doi.org/10.7150/jca.39575] [PMID: 32368303]
[102]
Hirahara, T.; Arigami, T.; Yanagita, S.; Matsushita, D.; Uchikado, Y.; Kita, Y.; Mori, S.; Sasaki, K.; Omoto, I.; Kurahara, H.; Maemura, K.; Okubo, K.; Uenosono, Y.; Ishigami, S.; Natsugoe, S. Combined neutrophil-lymphocyte ratio and platelet-lymphocyte ratio predicts chemotherapy response and prognosis in patients with advanced gastric cancer. BMC Cancer, 2019, 19(1), 672.
[http://dx.doi.org/10.1186/s12885-019-5903-y] [PMID: 31286873]
[103]
Ogata, T.; Satake, H.; Ogata, M.; Hatachi, Y.; Inoue, K.; Hamada, M.; Yasui, H. Neutrophil-to-lymphocyte ratio as a predictive or prognostic factor for gastric cancer treated with nivolumab: A multicenter retrospective study. Oncotarget, 2018, 9(77), 34520-34527.
[http://dx.doi.org/10.18632/oncotarget.26145] [PMID: 30349646]
[104]
Morelli, C.; Formica, V.; Patrikidou, A.; Murias, C.; Butt, S.-U.-R.; Nardecchia, A. Gastric inflammatory prognostic index (GIPI) to predict efficacy of PD-1/PD-L1 immune checkpoint inhibitors in metastatic Gastroesophageal Junction (GOJ)/Gastric Cancer (GC) patients. J. Clin. Oncol., 2020, 38(15-suppl), 4530.
[http://dx.doi.org/10.1200/JCO.2020.38.15_suppl.4530]
[105]
Formica, V.; Morelli, C.; Patrikidou, A.; Murias, C.; Butt, S.; Nardecchia, A.; Lucchetti, J.; Renzi, N.; Shiu, K.K.; Roselli, M.; Arkenau, H.T. Gastric Inflammatory Prognostic Index (GIPI) in patients with metastatic gastro-esophageal junction/gastric cancer treated with PD-1/PD-L1 immune checkpoint inhibitors. Target. Oncol., 2020, 15(3), 327-336.
[http://dx.doi.org/10.1007/s11523-020-00723-z] [PMID: 32449030]

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