Pharmacotherapy for metastatic esophageal cancer: where do we need to improve?

References

• Ferlay J, Soerjomataram I, Dikshit R, et al. Cancer incidence and mortality worldwide: sources, methods and major patterns in GLOBOCAN 2012. Int J Cancer. 2014;136(5):E359—E386.
   PubMed Web of Science ®Google Scholar
• Siegel RL, Miller KD, Jemal A. Cancer statistics, 2018. CA Cancer J Clin. 2018;68(1):7–30.
   PubMed Web of Science ®Google Scholar
• Cancer stat facts: esophageal cancer [Internet]. Surveillance, epidemiology, and end results program. [cited 2018 Jun 29]. Available from: https://seer.cancer.gov/statfacts/html/esoph.html
   Google Scholar
• Wheeler JB, Reed CE. Epidemiology of esophageal cancer. Surg Clin North Am. 2012;92(5):1077–1087.
   PubMed Web of Science ®Google Scholar
• Rustgi AK, El-Serag HB. Esophageal carcinoma. NEJM. 2014;371(26):2499–2509.
   PubMed Web of Science ®Google Scholar
• Testa U, Castelli G, Pelosi E. Esophageal cancer: genomic and molecular characterization, stem cell compartment and clonal evolution. Medicines (Basel). 2017;4(3):67.
   Google Scholar
• The Cancer Genome Atlas Research Network. Integrated genomic characterization of oesophageal carcinoma. Nature. 2017;541(7636):169–175.
   PubMed Web of Science ®Google Scholar
• Dulak AM, Stojanov P, Peng S, et al. Exome and whole-genome sequencing of esophageal adenocarcinoma identifies recurrent driver events and mutational complexity. Nat Genet. 2013;45(5):478–486.
   PubMed Web of Science ®Google Scholar
• Secrier M, Li X, Silva ND, et al. Mutational signatures in esophageal adenocarcinoma define etiologically distinct subgroups with therapeutic relevance. Nat Genet. 2016 May;48(10):1131–1141.
   PubMed Web of Science ®Google Scholar
• Chau I, Norman AR, Cunningham D, et al. The impact of primary tumour origins in patients with advanced oesophageal, oesophago-gastric junction and gastric adenocarcinoma–individual patient data from 1775 patients in four randomised controlled trials. Ann Oncol. 2009;20(5):885–891.
   PubMed Web of Science ®Google Scholar
• Ezdinli EZ, Gelber R, Desai DV, et al. Chemotherapy of advanced esophageal carcinoma: eastern cooperative oncology group experience. Cancer. 1980;46(10):2149–2153.
   PubMed Web of Science ®Google Scholar
• Kantarjian H, Ajani JA, Karlin DA. Cis-Diaminodichloroplatinum (II) Chemotherapy for advanced adenocarcinoma of the upper gastrointestinal tract. Oncology. 1985;42(2):69–71.
   PubMed Web of Science ®Google Scholar
• Davis S, Shanmugathasa M, Kessler W. cis-Dichlorodiammineplatinum(II) in the treatment of esophageal carcinoma. Cancer Treat Rep. 1980 Apr;64(4–5):709–711.
   PubMedGoogle Scholar
• Ilson D, Wadleigh R, Leichman L, et al. Paclitaxel given by a weekly 1-h infusion in advanced esophageal cancer. Ann Oncol. 2007;18(5):898–902.
   PubMed Web of Science ®Google Scholar
• Ajani JA, Ilson DH, Daugherty K, et al. Activity of taxol in patients with squamous cell carcinoma and adenocarcinoma of the esophagus. J Natl Cancer Inst. 1994;86(14):1086–1091.
   PubMedGoogle Scholar
• Muro K. A phase II study of single-agent docetaxel in patients with metastatic esophageal cancer. Ann Oncol. 2004 Jan;15(6):955–959.
   PubMed Web of Science ®Google Scholar
• Enzinger PC, Kulke MH, Clark JW, et al. A Phase II trial of irinotecan in patients with previously untreated advanced esophageal and gastric adenocarcinoma. Dig Dis Sci. 2005;50(12):2218–2223.
   PubMed Web of Science ®Google Scholar
• Bleiberg H, Conroy T, Paillot B, et al. Randomised phase II study of cisplatin and 5-fluorouracil (5-FU) versus cisplatin alone in advanced squamous cell oesophageal cancer. Eur J Cancer. 1997;33(8):1216–1220.
   PubMed Web of Science ®Google Scholar
• Warner E, Jensen JL, Cripps C, et al. Outpatient 5-fluorouracil, folinic acid and cisplatin in patients with advanced esophageal carcinoma. Acta Oncol. 1999;38(2):255–259.
   PubMed Web of Science ®Google Scholar
• Lee SJ, Kim S, Kim M, et al. Capecitabine in combination with either cisplatin or weekly paclitaxel as a first-line treatment for metastatic esophageal squamous cell carcinoma; a randomized phase II study. BMC Cancer. 2015;15:693.
   PubMed Web of Science ®Google Scholar
• Ajani JA, Rodriguez W, Bodoky G, et al. Multicenter phase III comparison of cisplatin/S-1 with cisplatin/infusional fluorouracil in advanced gastric or gastroesophageal adenocarcinoma study: the FLAGS trial. J Clin Oncol. 2010;28(9):1547–1553.
   PubMed Web of Science ®Google Scholar
• Al-Batran S-E, Hartmann JT, Probst S, et al. Phase III trial in metastatic gastroesophageal adenocarcinoma with fluorouracil, leucovorin plus either oxaliplatin or cisplatin: a study of the arbeitsgemeinschaft internistische onkologie. J Clin Oncol. 2008;26(9):1435–1442.
   PubMed Web of Science ®Google Scholar
• Webb A, Cunningham D, Scarffe JH, et al. Randomized trial comparing epirubicin, cisplatin, and fluorouracil versus fluorouracil, doxorubicin, and methotrexate in advanced esophagogastric cancer. J Clin Oncol. 1997;15(1):261–267.
   PubMed Web of Science ®Google Scholar
• Cunningham D, Starling N, Rao S, et al. Capecitabine and oxaliplatin for advanced esophagogastric cancer. N Engl J Med. 2008 Mar;358(1):36–46.
   PubMed Web of Science ®Google Scholar
• Cutsem EV, Moiseyenko VM, Tjulandin S, et al. Phase III study of docetaxel and cisplatin plus fluorouracil compared with cisplatin and fluorouracil as first-line therapy for advanced gastric cancer: a report of the V325 Study Group. J Clin Oncol. 2006;24(31):4991–4997.
   PubMed Web of Science ®Google Scholar
• Veer ET, Mohammad NH, Valkenhoef GV, et al. The efficacy and safety of first-line chemotherapy in advanced esophagogastric cancer: a network meta-analysis. J Natl Cancer Inst. 2016;108(10):djw166.
   PubMedGoogle Scholar
• Guimbaud R, Louvet C, Ries P, et al. Prospective, randomized, multicenter, phase III study of fluorouracil, leucovorin, and irinotecan versus epirubicin, cisplatin, and capecitabine in advanced gastric adenocarcinoma: a French intergroup (Fédération Francophone de Cancérologie Digestive, Fédération Nationale des Centres de Lutte Contre le Cancer, and Groupe Coopérateur Multidisciplinaireen Oncologie) study. J Clin Oncol. 2014;32(31):3520–3526.
   PubMed Web of Science ®Google Scholar
• El-Rayes BF. A phase II study of carboplatin and paclitaxel in esophageal cancer. Ann Oncol. 2004 Jan;15(6):960–965.
   PubMed Web of Science ®Google Scholar
• Janmaat VT, Steyerberg EW, Gaast AVD, et al. Palliative chemotherapy and targeted therapies for esophageal and gastroesophageal junction cancer. Cochrane Database Syst Rev. 2017 Nov;11:CD004063.
   PubMed Web of Science ®Google Scholar
• Bang Y-J, Cutsem EV, Feyereislova A, et al. 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.
   PubMed Web of Science ®Google Scholar
• Prins MJD, Ruurda JP, Diest PJV, et al. The significance of the HER-2 status in esophageal adenocarcinoma for survival: an immunohistochemical and an in situ hybridization study†. Ann Oncol. 2013;24(5):1290–1297.
   PubMed Web of Science ®Google Scholar
• Tabernero J, Hoff P, Shen L, et al. Pertuzumab plus trastuzumab and chemotherapy for HER2-positive metastatic gastric or gastro-oesophageal junction cancer (JACOB): final analysis of a double-blind, randomised, placebo-controlled phase 3 study. Lancet Oncol. 2018 Oct;19(10):1372–1384.
   PubMed Web of Science ®Google Scholar
• Hecht JR, Bang Y-J, Qin SK, et al. Lapatinib in combination with capecitabine plus oxaliplatin in human epidermal growth factor receptor 2–positive advanced or metastatic gastric, esophageal, or gastroesophageal adenocarcinoma: TRIO-013/LOGiC—a randomized phase III trial. J Clin Oncol. 2016 Oct;34(5):443–451.
   PubMed Web of Science ®Google Scholar
• Thuss-Patience PC, Shah MA, Ohtsu A, et al. Trastuzumab emtansine versus taxane use for previously treated HER2-positive locally advanced or metastatic gastric or gastro-oesophageal junction adenocarcinoma (GATSBY): an international randomised, open-label, adaptive, phase 2/3 study. Lancet Oncol. 2017;18(5):640–653.
   PubMed Web of Science ®Google Scholar
• Pavlidis ET. Role of bevacizumab in colorectal cancer growth and its adverse effects: a review. World J Gastroenterol. 2013;19(31):5051–5060.
   PubMed Web of Science ®Google Scholar
• Fuchs CS, Tomasek J, Yong CJ, et al. Ramucirumab monotherapy for previously treated advanced gastric or gastro-oesophageal junction adenocarcinoma (REGARD): an international, randomised, multicentre, placebo-controlled, phase 3 trial. Lancet. 2014;383(9911):31–39.
   PubMed Web of Science ®Google Scholar
• Wilke H, Muro K, Cutsem EV, et al. Ramucirumab plus paclitaxel versus placebo plus paclitaxel in patients with previously treated advanced gastric or gastro-oesophageal junction adenocarcinoma (RAINBOW): a double-blind, randomised phase 3 trial. Lancet Oncol. 2014;15(11):1224–1235.
   PubMed Web of Science ®Google Scholar
• Ohtsu A, Shah MA, Cutsem EV, et al. Bevacizumab in combination with chemotherapy as first-line therapy in advanced gastric cancer: a randomized, double-blind, placebo-controlled phase III study. J Clin Oncol. 2011;29(30):3968–3976.
   PubMed Web of Science ®Google Scholar
• Lin SJ, Gagnon-Bartsch JA, Tan IB, et al. Signatures of tumour immunity distinguish Asian and non-Asian gastric adenocarcinomas. Gut. 2014 Oct;64(11):1721–1731.
   PubMed Web of Science ®Google Scholar
• Li J, Qin S, Xu J, et al. Randomized, double-blind, placebo-controlled phase III trial of apatinib in patients with chemotherapy-refractory advanced or metastatic adenocarcinoma of the stomach or gastroesophageal junction. J Clin Oncol. 2016;34(13):1448–1454.
   PubMed Web of Science ®Google Scholar
• Pavlakis N, Sjoquist KM, Martin AJ, et al. Regorafenib for the treatment of advanced gastric cancer (INTEGRATE): a multinational placebo-controlled phase II trial. J Clin Oncol. 2016 Oct;34(23):2728–2735.
   PubMed Web of Science ®Google Scholar
• Yi JH, Lee J, Lee J, et al. Randomised phase II trial of docetaxel and sunitinib in patients with metastatic gastric cancer who were previously treated with fluoropyrimidine and platinum. Br J Cancer. 2012;106(9):1469–1474.
   PubMed Web of Science ®Google Scholar
• Enzinger PC, Mccleary NJ, Zheng H, et al. Multicenter double-blind randomized phase II: FOLFOX ziv-aflibercept/placebo for patients (pts) with chemo-naive metastatic esophagogastric adenocarcinoma (MEGA). J Clin Oncol. 2016;34:4.
   Web of Science ®Google Scholar
• Drake CG, Lipson EJ, Brahmer JR. Breathing new life into immunotherapy: review of melanoma, lung and kidney cancer. Nat Rev Clin Oncol. 2013;11(1):24–37.
   PubMed Web of Science ®Google Scholar
• Pardoll DM. The blockade of immune checkpoints in cancer immunotherapy. Nat Rev Cancer. 2012;12(4):252–264.
   PubMed Web of Science ®Google Scholar
• Fuchs CS, Doi T, Jang RW, et al. Safety and efficacy of pembrolizumab monotherapy in patients with previously treated advanced gastric and gastroesophageal junction cancer. JAMA Oncol. 2018 Oct;4(5):e180013.
   PubMed Web of Science ®Google Scholar
• Shah MA, Takashi K, Enzinger P, 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;36:4049.
   Google Scholar
• Kang Y-K, Boku N, Satoh T, et al. 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.
   PubMed Web of Science ®Google Scholar
• Kitagawa Y, Doki Y, Kato K, et al. Two year survival and safety update for esophageal squamous cell carcinoma treated with nivolumab (ATTRACTION-01/ONO-4538-07). Annals of Oncology. 2017 Sep;28(suppl_5). doi:10.1093/annonc/mdx369.022.
   PubMedGoogle Scholar
• Janjigian YY, Ott PA, Calvo E, et al. 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 May;35:4014.
   Web of Science ®Google Scholar
• Le DT, Durham JN, Smith KN, et al. Mismatch repair deficiency predicts response of solid tumors to PD-1 blockade. Science. 2017 Aug;357(6349):409–413.
   PubMed Web of Science ®Google Scholar
• Center for drug evaluation and research. Approved drugs - FDA grants accelerated approval to pembrolizumab for first tissue/site agnostic indication [Internet]. U S Food and Drug Administration Home Page. Center for Biologics Evaluation and Research; [cited 2018 Jun 29]. Available from: https://www.fda.gov/Drugs/InformationOnDrugs/ApprovedDrugs/ucm560040.htm
   Google Scholar
• Falkenback D, Johansson J, Halvarsson B, et al. Defective mismatch-repair as a minor tumorigenic pathway in Barrett esophagus-associated adenocarcinoma. Cancer Genet Cytogenet. 2005;157(1):82–86.
   PubMedGoogle Scholar
• Muro K, Chung HC, Shankaran V, et al. Pembrolizumab for patients with PD-L1-positive advanced gastric cancer (KEYNOTE-012): a multicentre, open-label, phase 1b trial. Lancet Oncol. 2016;17(6):717–726.
   PubMed Web of Science ®Google Scholar
• Doi T, Piha-Paul SA, Jalal SI, et al. Safety and antitumor activity of the anti–programmed death-1 antibody pembrolizumab in patients with advanced esophageal carcinoma. J Clin Oncol. 2018;36(1):61–67.
   PubMed Web of Science ®Google Scholar
• Gopalakrishnan V, Spencer CN, Nezi L, et al. Gut microbiome modulates response to anti–PD-1 immunotherapy in melanoma patients. Science. 2017 Feb;359(6371):97–103.
   PubMed Web of Science ®Google Scholar
• Matson V, Fessler J, Bao R, et al. The commensal microbiome is associated with anti–PD-1 efficacy in metastatic melanoma patients. Science. 2018 Apr;359(6371):104–108.
   PubMed Web of Science ®Google Scholar
• Routy B, Chatelier EL, Derosa L, et al. Gut microbiome influences efficacy of PD-1–based immunotherapy against epithelial tumors. Science. 2017 Feb;359(6371):91–97.
   PubMed Web of Science ®Google Scholar
• Zaidi AH, Kelly LA, Kreft RE, et al. Associations of microbiota and toll-like receptor signaling pathway in esophageal adenocarcinoma. BMC Cancer. 2016 Feb;16:52.
   PubMed Web of Science ®Google Scholar
• Blackett KL, Siddhi SS, Cleary S, et al. Oesophageal bacterial biofilm changes in gastro-oesophageal reflux disease, Barretts and oesophageal carcinoma: association or causality? Aliment Pharmacol Ther. 2013;37(11):1084–1092.
   PubMed Web of Science ®Google Scholar
• Peters BA, Wu J, Pei Z, et al. Oral microbiome composition reflects prospective risk for esophageal cancers. Cancer Res. 2017;77(23):6777–6787.
   PubMed Web of Science ®Google Scholar
• Salem M, Xiu J, Weinberg A, et al. Characterization of tumor mutation burden (TMB) in gastrointestinal (GI) cancers. J Clin Oncol. 2017;35:530.
   Web of Science ®Google Scholar
• Gabitass R, Annels N, Stocken D, et al. Elevated myeloid-derived suppressor cells in pancreatic, esophageal and gastric cancer are an independent prognostic factor and are associated with significant elevation of the Th2 cytokine interleukin-13. Cancer Immunol Immunother. 2011;60:1419–1430.
   PubMed Web of Science ®Google Scholar
• Yagi T, Baba Y, Ishimoto T, et al. PD-L1 expression, tumor-infiltrating lymphocytes, and clinical outcome in patients with surgically resected esophageal cancer. Ann Surg. 2017 Dec 4. doi:10.1097/SLA.0000000000002616. [Epub ahead of print]
   Google Scholar
• Gandhi L, Rodríguez-Abreu D, Gadgeel S, et al. Pembrolizumab plus chemotherapy in metastatic non–small-cell lung cancer. N Engl J Med. 2018;378(22):2078–2092.
   PubMed Web of Science ®Google Scholar
• Apetoh L, Ladoire S, Coukos G, et al. Combining immunotherapy and anticancer agents: the right path to achieve cancer cure? Ann Oncol. 2015;26(9):1813–1823.
   PubMed Web of Science ®Google Scholar
• Bang YJ, Muro K, Fuchs CS, et al. KEYNOTE-059 cohort 2: safety and efficacy of pembrolizumab (pembro) plus 5-fluorouracil (5-FU) and cisplatin for first-line (1L) treatment of advanced gastric cancer. J Clin Oncol. 2017 May;35:4012.
   PubMed Web of Science ®Google Scholar
• Stagg J, Loi S, Divisekera U, et al. Anti-ErbB-2 mAb therapy requires type I and II interferons and synergizes with anti-PD-1 or anti-CD137 mAb therapy. Proc Natl Acad Sci. 2011 Nov;108(17):7142–7147.
   PubMed Web of Science ®Google Scholar
• Suh KJ, Sung JH, Kim JW, et al. EGFR or HER2 inhibition modulates the tumor microenvironment by suppression of PD-L1 and cytokines release. Oncotarget. 2017 Dec;8(38):63901–63910.
   PubMedGoogle Scholar
• Catenacci DV, Park H, Lockhart AC, et al. Phase 1b/2 study of margetuximab (M) plus pembrolizumab (P) in advanced HER2 gastroesophageal junction (GEJ) or gastric (G) adenocarcinoma (GEA). J Clin Oncol. 2018 Feb;36:140.
   Web of Science ®Google Scholar
• Ott PA, Hodi FS, Buchbinder EI. Inhibition of immune checkpoints and vascular endothelial growth factor as combination therapy for metastatic melanoma: an overview of rationale, preclinical evidence, and initial clinical data. Front Oncol. 2015;5:202.
   PubMed Web of Science ®Google Scholar
• Chau I, Penel N, Arkenau HT, et al. Safety and antitumor activity of ramucirumab plus pembrolizumab in treatment naïve advanced gastric or gastroesophageal junction (G/GEJ) adenocarcinoma: preliminary results from a multi-disease phase I study (JVDF). J Clin Oncol. 2018 Feb;36:101.
   PubMed Web of Science ®Google Scholar
• Jiang W, Chan CK, Weissman IL, et al. Immune priming of the tumor microenvironment by radiation. Trends Cancer. 2016;2(11):638–645.
   PubMed Web of Science ®Google Scholar
• Neelapu SS, Locke FL, Bartlett NL, et al. Axicabtageneciloleucel CAR T-cell therapy in refractory large B-cell lymphoma. N Engl J Med. 2017;377(26):2531–2544.
   PubMed Web of Science ®Google Scholar
• Maude SL, Laetsch TW, Buechner J, et al. Tisagenlecleucel in children and young adults with B-cell lymphoblastic leukemia. N Engl J Med. 2018;378(5):439–448.
   PubMed Web of Science ®Google Scholar
• Lu Y-C, Parker LL, Lu T, et al. Treatment of patients with metastatic cancer using a major histocompatibility complex class II–restricted T-cell receptor targeting the cancer germline antigen MAGE-A3. J Clin Oncol. 2017 Oct;35(29):3322–3329.
   PubMed Web of Science ®Google Scholar
• Hahn AW, Gill DM, Pal SK, et al. The future of immune checkpoint cancer therapy after PD-1 and CTLA-4. Immunotherapy. 2017;9(8):681–692.
   PubMed Web of Science ®Google Scholar