Novel fluoropyrimidine-based chemotherapy for advanced well-differentiated neuroendocrine tumors: a clinical update

References

• Toumpanakis CG, Caplin ME. Molecular genetics of gastroenteropancreatic neuroendocrine tumors. Am J Gastroenterol. 2008;103:729–732.
   PubMed Web of Science ®Google Scholar
• Modlin IM, Oberg K, Chung DC, et al. Gastroenteropancreatic neuroendocrine tumours. Lancet Oncol. 2008;9:61–72.
   PubMed Web of Science ®Google Scholar
• Bosman FT, Carneiro F, Hruban RH, et al. WHO classification of tumours of the digestive system 4th ed. Lyon, France: International Agency for Research on Cancer; 2010.
   Google Scholar
• Travis WD, Brambilla E, Burke AP, et al. WHO classification of tumours of the lung, pleura, thymus and heart. Lyon: IARC; 2015.
   Google Scholar
• Lloyd RV, Osamura RY, Kloppel G, et al. WHO classifiation of tumours of endocrine organs. Lyon, France: IARC Press; 2017.
   Google Scholar
• R F DW, B H E, R H H, et al. Well-differentiated pancreatic neuroendocrine tumors: from genetics to therapy[J]. Nat Rev Gastroenterol Hepatol. 2012;9(4):199.
   PubMed Web of Science ®Google Scholar
• Yao JC, Hassan M, Phan A, et al. One hundred years after “carcinoid”: epidemiology of and prognostic factors for neuroendocrine tumors in 35,825 cases in the United States. J Clin Oncol. 2008;26:3063–3072.
   PubMed Web of Science ®Google Scholar
• Kunz PL. Carcinoid and neuroendocrine tumors: building on success. J Clin Oncol. 2015;33:1855–1863.
   PubMed Web of Science ®Google Scholar
• Yao JC, Fazio N, Singh S, et al. Everolimus for the treatment of advanced, non-functional neuroendocrine tumours of the lung or gastrointestinal tract (RADIANT-4): a randomised, placebo-controlled, phase 3 study. Lancet. 2016;387:968–977.
   PubMed Web of Science ®Google Scholar
• Kulke M, Shah M, Benson AB, et al. National comprehensive cancer network neuroendocrine tumors guidelines. Version 1. 2017, 2017.
   Google Scholar
• Kunz PL, Reidy-Lagunes D, Anthony LB, et al. Consensus guidelines for the management and treatment of neuroendocrine tumors. Pancreas. 2013;42:557–577.
   PubMed Web of Science ®Google Scholar
• Pavel M, O’Toole D, Costa F, et al. Enets consensus guidelines update for the management of distant metastatic disease of intestinal, pancreatic, bronchial neuroendocrine neoplasms (nen) and nen of unknown primary site. Neuroendocrinology. 2016;103:172–185.
   PubMed Web of Science ®Google Scholar
• Gustavsson B, Carlsson G, Machover D, et al. A review of the evolution of systemic chemotherapy in the management of colorectal cancer. Clin Colorectal Cancer. 2015;14:1–10.
   PubMed Web of Science ®Google Scholar
• Grem JL, Nguyen D, Monahan BP, et al. Sequence-dependent antagonism between fluorouracil and paclitaxel in human breast cancer cells. Biochem Pharmacol. 1999;58:477–486.
   PubMed Web of Science ®Google Scholar
• Marchal JA, Boulaiz H, Suárez I, et al. Growth inhibition, G(1)-arrest, and apoptosis in MCF-7 human breast cancer cells by novel highly lipophilic 5-fluorouracil derivatives. Invest New Drugs. 2004;22:379–389.
   PubMed Web of Science ®Google Scholar
• Silvestris N, Maiello E, De Vita F, et al. Update on capecitabine alone and in combination regimens in colorectal cancer patients. Cancer Treat Rev. 2010;36(Suppl 3):S46S55.
   Google Scholar
• Shirasaka T, Nakano K, Takechi T, et al. Antitumor activity of 1 M tegafur-0.4 M 5-chloro-2,4-dihydroxypyridine-1 M potassium oxonate (S-1) against human colon carcinoma orthotopically implanted into nude rats. Cancer Res. 1996;56:2602–2606.
   PubMed Web of Science ®Google Scholar
• Fine RL, Fogelman DR, Schreibman SM. Effective treatment of neuroendocrine tumors with temozolomide and capecitabine. J Clin Oncol. 2005;23(Suppl 16):S4216.
   Web of Science ®Google Scholar
• Cohen AL, Colman H. Glioma biology and molecular markers. Cancer Treat Res. 2015;163:15–30.
   PubMedGoogle Scholar
• Van Cutsem E, Twelves C, Cassidy J, et al. Oral capecitabine compared with intravenous fluorouracil plus leucovorin in patients with metastatic colorectal cancer: results of a large phase III study. J Clin Oncol. 2001;19:4097–4106.
   PubMed Web of Science ®Google Scholar
• Moertel CG, Hanley JA. Combination chemotherapy trials in metastatic carcinoid tumor and the malignant carcinoid syndrome. Cancer Clin Trials. 1979;2:327–334.
   PubMedGoogle Scholar
• Moertel CG, Hanley JA, Johnson LA. Streptozocin alone compared with streptozocin plus fluorouracil in the treatment of advanced islet-cell carcinoma. N Engl J Med. 1980;303:1189–1194.
   PubMed Web of Science ®Google Scholar
• Engstrom PF, Lavin PT, Moertel CG, et al. Streptozocin plus fluorouracil versus doxorubicin therapy for metastatic carcinoid tumor. J Clin Oncol. 1984;2:1255–1259.
   PubMed Web of Science ®Google Scholar
• Moertel CG, Lefkopoulo M, Lipsitz S, et al. Streptozocin-doxorubicin, streptozocin-fluorouracil or chlorozotocin in the treatment of advanced islet-cell carcinoma. N Engl J Med. 1992;326:519–523.
   PubMed Web of Science ®Google Scholar
• Oberg K, Norheim I, Alm G. Treatment of malignant carcinoid tumors: a randomized controlled study of streptozocin plus 5-FU and human leukocyte interferon. Eur J Cancer Clin Oncol. 1989;25:1475–1479.
   PubMedGoogle Scholar
• Rougier JP, Oliveira J, Ducreux M, et al. Metastatic carcinoid and islet cell tumours of the pancreas: a phase II trial of the efficacy of combination chemotherapy with 5-fluorouracil, doxorubicin and cisplatin. Eur J Cancer. 1991;27:1380–1382.
   PubMed Web of Science ®Google Scholar
• Hughes MJ, Kerr DJ, Cassidy J, et al. A pilot study of combination therapy with interferon-alpha-2a and 5-fluorouracil in metastatic carcinoid and malignant endocrine pancreatic tumours. Ann Oncol. 1996;7:208–210.
   PubMed Web of Science ®Google Scholar
• Andreyev HJ, Scott-Mackie P, Cunningham D, et al. Phase II study of continuous infusion fluorouracil and interferon alfa-2b in the palliation of malignant neuroendocrine tumors. J Clin Oncol. 1995;13:1486–1492.
   PubMed Web of Science ®Google Scholar
• Di BM, Bajetta E, Bochicchio AM, et al. A phase II trial of dacarbazine, fluorouracil and epirubicin in patients with neuroendocrine tumours A study by the Italian Trials in Medical Oncology (I.T.M.O.) Group. Ann Oncol. 1995;6:77–79.
   PubMed Web of Science ®Google Scholar
• Lamarca A, Elliott E, Barriuso J, et al. Chemotherapy for advanced non-pancreatic well-differentiated neuroendocrine tumours of the gastrointestinal tract, a systematic review and meta-analysis: a lost cause. Cancer Treat Rev. 2016;44:26–41.
   PubMed Web of Science ®Google Scholar
• Peixoto RD, Noonan KL, Pavlovich P, et al. Outcomes of patients treated with capecitabine and temozolamide for advanced pancreatic neuroendocrine tumors (PNETs) and non-PNETs. J Gastrointest Oncol. 2014;5:247–252.
   PubMedGoogle Scholar
• Ramirez RA, Beyer DT, Chauhan A, et al. The role of capecitabine/temozolomide in metastatic neuroendocrine tumors. Oncologist. 2016;21:671–675.
   PubMed Web of Science ®Google Scholar
• Fine RL, Gulati AP, Krantz BA, et al. Capecitabine and temozolomide (CAPTEM) for metastatic, well-differentiated neuroendocrine cancers: the Pancreas Center at Columbia University experience. Cancer Chemother Pharmacol. 2013;71:663–670.
   PubMed Web of Science ®Google Scholar
• Cives M, Ghayouri M, Morse B, et al. Analysis of potential response predictors to capecitabine/temozolomide in metastatic pancreatic neuroendocrine tumors. Endocr Relat Cancer. 2016;23:759–767.
   PubMed Web of Science ®Google Scholar
• Saif MW, Kaley K, Brennan M, et al. A retrospective study of capecitabine/temozolomide (CAPTEM) regimen in the treatment of metastatic pancreatic neuroendocrine tumors (pNETs) after failing previous therapy. JOP. 2013;14:498–501.
   PubMedGoogle Scholar
• Strosberg JR, Fine RL, Choi J, et al. First-line chemotherapy with capecitabine and temozolomide in patients with metastatic pancreatic endocrine carcinomas. Cancer. 2011;117:268–275.
   PubMed Web of Science ®Google Scholar
• Abbasi S, Kashashna A, Albaba H. Efficacy of capecitabine and temozolomide combination in well-differentiated neuroendocrine tumors: jordan experience. Pancreas. 2014;43:1303–1305.
   PubMed Web of Science ®Google Scholar
• Kotteas EA, Syrigos KN, Saif MW. Profile of capecitabine/temozolomide combination in the treatment of well-differentiated neuroendocrine tumors. Onco Targets Ther. 2016;9:699–704.
   PubMed Web of Science ®Google Scholar
• Twelves C, Scheithauer W, McKendrick J, et al. Capecitabine versus 5-fluorouracil/folinic acid as adjuvant therapy for stage III colon cancer: final results from the X-ACT trial with analysis by age and preliminary evidence of a pharmacodynamic marker of efficacy. Ann Oncol. 2012;23:1190–1197.
   PubMed Web of Science ®Google Scholar
• Cassidy J, Clarke S, Díaz-Rubio E, et al. Randomized phase III study of capecitabine plus oxaliplatin compared with fluorouracil/folinic acid plus oxaliplatin as first-line therapy for metastatic colorectal cancer. J Clin Oncol. 2008;26:2006–2012.
   PubMed Web of Science ®Google Scholar
• Cassidy J, Tabernero J, Twelves C, et al. XELOX (capecitabine plus oxaliplatin): active first-line therapy for patients with metastatic colorectal cancer. J Clin Oncol. 2004;22:2084–2091.
   PubMed Web of Science ®Google Scholar
• Porschen R, Arkenau HT, Kubicka S, et al. Phase III study of capecitabine plus oxaliplatin compared with fluorouracil and leucovorin plus oxaliplatin in metastatic colorectal cancer: a final report of the AIO Colorectal Study Group. J Clin Oncol. 2007;25:4217–4223.
   PubMed Web of Science ®Google Scholar
• Cassidy J, Clarke S, Díaz-Rubio E, et al. XELOX vs FOLFOX-4 as first-line therapy for metastatic colorectal cancer: NO16966 updated results. Br J Cancer. 2011;105:58–64.
   PubMed Web of Science ®Google Scholar
• Ducreux M, Bennouna J, Hebbar M, et al. Capecitabine plus oxaliplatin (XELOX) versus 5-fluorouracil/leucovorin plus oxaliplatin (FOLFOX-6) as first-line treatment for metastatic colorectal cancer. Int J Cancer. 2011;128:682–690.
   PubMed Web of Science ®Google Scholar
• Spada F, Antonuzzo L, Marconcini R, et al. Oxaliplatin-based chemotherapy in advanced neuroendocrine tumors: clinical outcomes and preliminary correlation with biological factors. Neuroendocrinology. 2016;103:806–814.
   PubMed Web of Science ®Google Scholar
• Bajetta E, Catena L, Procopio G, et al. Are capecitabine and oxaliplatin (XELOX) suitable treatments for progressing low-grade and high-grade neuroendocrine tumours. Cancer Chemother Pharmacol. 2007;59:637–642.
   PubMed Web of Science ®Google Scholar
• Faure M, Niccoli P, Autret A, et al. Systemic chemotherapy with FOLFOX in metastatic grade 1/2 neuroendocrine cancer. Mol Clin Oncol. 2017;6:44–48.
   PubMed Web of Science ®Google Scholar
• Sasako M, Sakuramoto S, Katai H, et al. Five-year outcomes of a randomized phase III trial comparing adjuvant chemotherapy with S-1 versus surgery alone in stage II or III gastric cancer. J Clin Oncol. 2011;29:4387–4393.
   PubMed Web of Science ®Google Scholar
• Ajani JA, Buyse M, Lichinitser M, et al. Combination of cisplatin/S-1 in the treatment of patients with advanced gastric or gastroesophageal adenocarcinoma: results of noninferiority and safety analyses compared with cisplatin/5-fluorouracil in the First-Line Advanced Gastric Cancer Study. Eur J Cancer. 2013;49:3616–3624.
   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;28:1547–1553.
   PubMed Web of Science ®Google Scholar
• Zhao J, Zhao H, Chi Y. Safety and efficacy of the S-1/Temozolomide regimen in patients with metastatic neuroendocrine tumors. Neuroendocrinology. 2017. Epub ahead of print.
   PubMed Web of Science ®Google Scholar
• Rindi G, Klöppel G, Alhman H, et al. TNM staging of foregut (neuro)endocrine tumors: a consensus proposal including a grading system. Virchows Arch. 2006;449:395–401.
   PubMed Web of Science ®Google Scholar
• Meyer T, Qian W, Caplin ME, et al. Capecitabine and streptozocin ± cisplatin in advanced gastroenteropancreatic neuroendocrine tumours. Eur J Cancer. 2014;50:902–911.
   PubMed Web of Science ®Google Scholar
• Medley L, Morel AN, Farrugia D, et al. Phase II study of single agent capecitabine in the treatment of metastatic non-pancreatic neuroendocrine tumours. Br J Cancer. 2011;104:1067–1070.
   PubMed Web of Science ®Google Scholar
• Heppeler A, Froidevaux S, Eberle AN, et al. Receptor targeting for tumor localisation and therapy with radiopeptides. Curr Med Chem. 2000;7:971–994.
   PubMed Web of Science ®Google Scholar
• Strosberg J, Wolin E, Chasen B, et al. 177-Lu-Dotatate significantly improves progression-free survival in patients with midgut neuroendocrine tumours: results of the phase III NETTER-1 trial. Proceedings of the 2015 European Cancer Congress; 2015 Sep 25–29;Vienna.
   Google Scholar
• Childs A, Kirkwood A, Edeline J, et al. Ki-67 index and response to chemotherapy in patients with neuroendocrine tumours. Endocr Relat Cancer. 2016;23:563–570.
   PubMed Web of Science ®Google Scholar
• P G C, R A P, Turner JH. Phase I-II study of radiopeptide 177Lu-octreotate in combination with capecitabine and temozolomide in advanced low-grade neuroendocrine tumors[J]. Cancer Biother Radiopharm. 2012;27(9):561–569.
   PubMed Web of Science ®Google Scholar
• Lambrescu I, Fica S, Martins D, et al. Metronomic and metronomic-like therapies in neuroendocrine tumors - Rationale and clinical perspectives. Cancer Treat Rev. 2017;55:46–56.
   PubMed Web of Science ®Google Scholar
• Brizzi MP, Berruti A, Ferrero A, et al. Continuous 5-fluorouracil infusion plus long acting octreotide in advanced well-differentiated neuroendocrine carcinomas A phase II trial of the Piemonte oncology network. BMC Cancer. 2009;9:388.
   PubMed Web of Science ®Google Scholar
• Squadroni M, Meglio GD, Spada F, et al. Metronomic capecitabine in advanced well or moderately differentiated neuroendocrine carcinomas. DOI:10.1200/jco.2010.28.15_suppl.e13130
   Google Scholar
• Bongiovanni A, Riva N, Calpona S, et al. Metronomic capecitabine in gastroenteropancreatic neuroendrocrine tumors: a suitable regimen and review of the literature. Onco Targets Ther. 2014;7:1919–1926.
   PubMed Web of Science ®Google Scholar
• Terris B, Scoazec JY, Rubbia L, et al. Expression of vascular endothelial growth factor in digestive neuroendocrine tumours. Histopathology. 1998;32:133–138.
   PubMed Web of Science ®Google Scholar
• Zhang J, Jia Z, Li Q, et al. Elevated expression of vascular endothelial growth factor correlates with increased angiogenesis and decreased progression-free survival among patients with low-grade neuroendocrine tumors. Cancer. 2007;109:1478–1486.
   PubMed Web of Science ®Google Scholar
• Jubb AM, Harris AL. Biomarkers to predict the clinical efficacy of bevacizumab in cancer. Lancet Oncol. 2010;11:1172–1183.
   PubMed Web of Science ®Google Scholar
• Chan JA, Stuart K, Earle CC, et al. Prospective study of bevacizumab plus temozolomide in patients with advanced neuroendocrine tumors. J Clin Oncol. 2012;30:2963–2968.
   PubMed Web of Science ®Google Scholar
• Mitry E, Walter T, Baudin E, et al. Bevacizumab plus capecitabine in patients with progressive advanced well-differentiated neuroendocrine tumors of the gastro-intestinal (GI-NETs) tract (BETTER trial)–a phase II non-randomised trial. Eur J Cancer. 2014;50:3107–3115.
   PubMed Web of Science ®Google Scholar
• Kunz PL, Balise RR, Fehrenbacher L, et al. Oxaliplatin-fluoropyrimidine chemotherapy plus bevacizumab in advanced neuroendocrine tumors: an analysis of 2 phase ii trials. Pancreas. 2016;45:1394–1400.
   PubMed Web of Science ®Google Scholar
• Berruti A, Fazio N, Ferrero A, et al. Bevacizumab plus octreotide and metronomic capecitabine in patients with metastatic well-to-moderately differentiated neuroendocrine tumors: the XELBEVOCT study. BMC Cancer. 2014;14:184.
   PubMed Web of Science ®Google Scholar
• Kulke MH, Hornick JL, Frauenhoffer C, et al. O6-methylguanine DNA methyltransferase deficiency and response to temozolomide-based therapy in patients with neuroendocrine tumors. Clin Cancer Res. 2009;15:338–345.
   PubMed Web of Science ®Google Scholar
• Liu L, Gerson SL. Targeted modulation of MGMT: clinical implications. Clin Cancer Res. 2006;12:328–331.
   PubMed Web of Science ®Google Scholar
• Gerson SL. Clinical relevance of MGMT in the treatment of cancer. J Clin Oncol. 2002;20:2388–2399.
   PubMed Web of Science ®Google Scholar
• Walter T, van Brakel B, Vercherat C, et al. O6-Methylguanine-DNA methyltransferase status in neuroendocrine tumours: prognostic relevance and association with response to alkylating agents. Br J Cancer. 2015;112:523–531.
   PubMed Web of Science ®Google Scholar
• Schmitt AM, Pavel M, Rudolph T, et al. Prognostic and predictive roles of MGMT protein expression and promoter methylation in sporadic pancreatic neuroendocrine neoplasms. Neuroendocrinology. 2014;100:35–44.
   PubMed Web of Science ®Google Scholar
• Ekeblad S, Sundin A, Janson ET, et al. Temozolomide as monotherapy is effective in treatment of advanced malignant neuroendocrine tumors. Clin Cancer Res. 2007;13:2986–2991.
   PubMed Web of Science ®Google Scholar
• L E S, N E D, D S W, et al. American Society of Clinical Oncology statement: a conceptual framework to assess the value of cancer treatment options. J Clin Oncol. 2015;33(23):2563–2577.
   PubMed Web of Science ®Google Scholar
• Turner NC, Strauss SJ, Sarker D, et al. Chemotherapy with 5-fluorouracil, cisplatin and streptozocin for neuroendocrine tumours. Br J Cancer. 2010;102:1106–1112.
   PubMed Web of Science ®Google Scholar
• Oberg K. Neuroendocrine tumors of the gastrointestinal tract: recent advances in molecular genetics, diagnosis, and treatment. Curr Opin Oncol. 2005;17:386–391.
   PubMed Web of Science ®Google Scholar
• Oberg K. Management of neuroendocrine tumors. American Society of Clinical Oncology (ASCO) 2002 Educational Book, 38th Annual Meeting. J Clin Oncol. 2008;401–405.
   Google Scholar
• Lawrence B, Gustafsson BI, Kidd M, et al. clinical relevance of chromogranin A as a biomarker for gastroenteropancreatic neuroendocrine tumors. Endocrinol Metab Clin North Am. 2011;40:111–134, viii
   PubMed Web of Science ®Google Scholar
• Arnold R, Wilke A, Rinke A, et al. Plasma chromogranin A as marker for survival in patients with metastatic endocrine gastroenteropancreatic tumors. Clin Gastroenterol Hepatol. 2008;6:820–827.
   PubMed Web of Science ®Google Scholar
• Durante C, Boukheris H, Dromain C, et al. Prognostic factors influencing survival from metastatic (stage IV) gastroenteropancreatic well-differentiated endocrine carcinoma. Endocr Relat Cancer. 2009;16:585–597.
   PubMed Web of Science ®Google Scholar
• Rabik CA, Dolan ME. Molecular mechanisms of resistance and toxicity associated with platinating agents. Cancer Treat Rev. 2007;33:9–23.
   PubMed Web of Science ®Google Scholar
• Martin LP, Hamilton TC, Schilder RJ. Platinum resistance: the role of DNA repair pathways. Clin Cancer Res. 2008;14:1291–1295.
   PubMed Web of Science ®Google Scholar
• Ceppi P, Volante M, Ferrero A, et al. Thymidylate synthase expression in gastroenteropancreatic and pulmonary neuroendocrine tumors[J]. Clinical Cancer Research. 2008;14(4):1059–1064.
   PubMed Web of Science ®Google Scholar
• Paulson AS, Bergsland EK. Systemic therapy for advanced carcinoid tumors: where do we go from here. J Natl Compr Canc Netw. 2012;10:785–793.
   PubMed Web of Science ®Google Scholar
• Ajani JA, Faust J, Ikeda K, et al. Phase I pharmacokinetic study of S-1 plus cisplatin in patients with advanced gastric carcinoma. J Clin Oncol. 2005;23:6957–6965.
   PubMed Web of Science ®Google Scholar
• Chuah B, Goh BC, Lee SC, et al. Comparison of the pharmacokinetics and pharmacodynamics of S-1 between Caucasian and East Asian patients. Cancer Sci. 2011;102:478–483.
   PubMed Web of Science ®Google Scholar
• C M A, Nguyen P, B A C, et al. Multimodality management of “Borderline Resectable” pancreatic neuroendocrine tumors: report of a single-institution experience[J]. Cancer Control. 2017;24(5):1073274817729076.
   Web of Science ®Google Scholar
• Devata S, Kim EJ. Neoadjuvant chemotherapy with capecitabine and temozolomide for unresectable pancreatic neuroendocrine tumor. Case Rep Oncol. 2012;5:622–626.
   PubMedGoogle Scholar
• Chuang CC, Bhurke S, Chen SY, et al. Clinical characteristics, treatment patterns, and economic burden in patients treated for neuroendocrine tumors in the United States: a retrospective cohort study. J Med Econ. 2015;18:126–136.
   PubMed Web of Science ®Google Scholar
• André N, Banavali S, Snihur Y, et al. Has the time come for metronomics in low-income and middle-income countries. Lancet Oncol. 2013;14:e239e248.
   Web of Science ®Google Scholar
• A E H, A M M, Tuli R. Neuroendocrine tumors of the lung: current challenges and advances in the diagnosis and management of well-differentiated disease. J Thorac Oncol. 2017;12(3):425–436.
   PubMed Web of Science ®Google Scholar
• Partelli S, Cirocchi R, Crippa S, et al. Systematic review of active surveillance versus surgical management of asymptomatic small non‐functioning pancreatic neuroendocrine neoplasms. Br J Surg. 2017;104(1):34–41.
   PubMed Web of Science ®Google Scholar
• Singh S, S L A, Dey C, et al. Diagnosis and management of gastrointestinal neuroendocrine tumors: an evidence-based Canadian consensus. Cancer Treat Rev. 2016;47:32–45.
   PubMed Web of Science ®Google Scholar