85
Views
5
CrossRef citations to date
0
Altmetric
Review

Management of neuroendocrine tumors: current and future therapies

Pages 49-62 | Published online: 10 Jan 2014

References

  • 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.26(18), 3063–3072 (2008).
  • Hauso O, Gustafsson BI, Kidd M et al. Neuroendocrine tumor epidemiology: contrasting Norway and North America. Cancer113(10), 2655–2664 (2008).
  • Maggard MA, O’Connell JB, Ko CY. Updated population-based review of carcinoid tumors. Ann. Surg.240(1), 117–122 (2004).
  • Modlin IM, Lye KD, Kidd M. A 5-decade analysis of 13,715 carcinoid tumors. Cancer97(4), 934–959 (2003).
  • Metz DC, Jensen RT. Gastrointestinal neuroendocrine tumors: pancreatic endocrine tumors. Gastroenterology135(5), 1469–1492 (2008).
  • Ramage JK, Davies AH, Ardill J et al. Guidelines for the management of gastroenteropancreatic neuroendocrine (including carcinoid) tumours. Gut54(Suppl. 4), iv1–iv16 (2005).
  • Pirker RA, Pont J, Pohnl R, Schutz W, Griesmacher A, Muller MM. Usefulness of chromogranin A as a marker for detection of relapses of carcinoid tumours. Clin. Chem. Lab. Med.36(11), 837–840 (1998).
  • Korse CM, Bonfrer JM, Aaronson NK, Hart AA, Taal BG. Chromogranin A as an alternative to 5-hydroxyindoleacetic acid in the evaluation of symptoms during treatment of patients with neuroendocrine tumors. Neuroendocrinology89(3), 296–301 (2009).
  • Bajetta E, Ferrari L, Martinetti A et al. Chromogranin A. Neuron specific enolase, carcinoembryonic antigen, and hydroxyindole acetic acid evaluation in patients with neuroendocrine tumors. Cancer86(5), 858–865 (1999).
  • Yao JC, Lombard-Bohas C, Baudin E et al. Daily oral everolimus activity in patients with metastatic pancreatic neuroendocrine tumors after failure of cytotoxic chemotherapy: a Phase II trial. J. Clin. Oncol.28(1), 69–76 (2009).
  • Schnirer, II, Yao JC, Ajani JA. Carcinoid – a comprehensive review. Acta Oncol.42(7), 672–692 (2003).
  • Eriksson B, Kloppel G, Krenning E et al. Consensus guidelines for the management of patients with digestive neuroendocrine tumors – well-differentiated jejunal-ileal tumor/carcinoma. Neuroendocrinology87(1), 8–19 (2008).
  • Pape UF, Berndt U, Muller-Nordhorn J et al. Prognostic factors of long-term outcome in gastroenteropancreatic neuroendocrine tumours. Endocr. Relat. Cancer15(4), 1083–1097 (2008).
  • Falconi M, Plockinger U, Kwekkeboom DJ et al. Well-differentiated pancreatic nonfunctioning tumors/carcinoma. Neuroendocrinology84(3), 196–211 (2006).
  • Ricke J, Klose KJ, Mignon M, Öberg K, Wiedenmann B. Standardisation of imaging in neuroendocrine tumours: results of a European delphi process. Eur. J. Radiol.37(1), 8–17 (2001).
  • Gabriel M, Decristoforo C, Kendler D et al. 68Ga-DOTA-Tyr3-octreotide PET in neuroendocrine tumors: comparison with somatostatin receptor scintigraphy and CT. J. Nucl. Med.48(4), 508–518 (2007).
  • Sundin A, Garske U, Orlefors H. Nuclear imaging of neuroendocrine tumours. Best Pract. Res. Clin. Endocrinol. Metab.21(1), 69–85 (2007).
  • Oberndorfer S. Karzenoide Tumoren des Dünndarms. Frankf. Zschr. Path.1, 426–430 (1907).
  • Williams ED, Sandler M. The classification of carcinoid tumours. Lancet1, 238–239 (1963).
  • Kloppel G, Perren A, Heitz PU. The gastroenteropancreatic neuroendocrine cell system and its tumors: the WHO classification. Ann. NY Acad. Sci.1014, 13–27 (2004).
  • Rindi G, Kloppel G, Alhman H et al. TNM staging of foregut (neuro)endocrine tumors: a consensus proposal including a grading system. Virchows Arch.449(4), 395–401 (2006).
  • Rindi G, Kloppel G, Couvelard A et al. TNM staging of midgut and hindgut (neuro) endocrine tumors: a consensus proposal including a grading system. Virchows Arch.451(4), 757–762 (2007).
  • Kaltsas GA, Besser GM, Grossman AB. The diagnosis and medical management of advanced neuroendocrine tumors. Endocr. Rev.25(3), 458–511 (2004).
  • Rubin J, Ajani J, Schirmer W et al. Octreotide acetate long-acting formulation versus open-label subcutaneous octreotide acetate in malignant carcinoid syndrome. J. Clin. Oncol.17(2), 600–606 (1999).
  • Beaumont J, Zhimei L, Choi S. et al. Health-related quality of life of patients with neuroendocrine tumor compared to the United States general population. Presented at: 2nd Annual Meeting of the North American NeuroEndocrine Tumor Society. Charlotte, North Carolina, USA, 2–3 October 2009.
  • Basson MD, Ahlman H, Wangberg B, Modlin IM. Biology and management of the midgut carcinoid. Am. J. Surg.165(2), 288–297 (1993).
  • Modlin IM, Öberg K, Chung DC et al. Gastroenteropancreatic neuroendocrine tumours. Lancet Oncol. 9(1), 61–72 (2008).
  • Kulke MH, Mayer RJ. Carcinoid tumors. N. Engl. J. Med.340(11), 858–868 (1999).
  • Plockinger U, Rindi G, Arnold R et al. Guidelines for the diagnosis and treatment of neuroendocrine gastrointestinal tumours. A consensus statement on behalf of the European Neuroendocrine Tumour Society (ENETS). Neuroendocrinology80(6), 394–424 (2004).
  • Öberg K, Jelic S. Neuroendocrine gastroenteropancreatic tumors: ESMO clinical recommendations for diagnosis, treatment and follow-up. Ann. Oncol.19(Suppl. 2), ii104–ii105 (2008).
  • Modlin IM, Latich I, Kidd M, Zikusoka M, Eick G. Therapeutic options for gastrointestinal carcinoids. Clin. Gastroenterol. Hepatol.4(5), 526–547 (2006).
  • McEntee GP, Nagorney DM, Kvols LK, Moertel CG, Grant CS. Cytoreductive hepatic surgery for neuroendocrine tumors. Surgery108(6), 1091–1096 (1990).
  • Moller LN, Stidsen CE, Hartmann B, Holst JJ. Somatostatin receptors. Biochim. Biophys. Acta1616(1), 1–84 (2003).
  • Susini C, Buscail L. Rationale for the use of somatostatin analogs as antitumor agents. Ann. Oncol.17(12), 1733–1742 (2006).
  • Schmid HA, Schoeffter P. Functional activity of the multiligand analog SOM230 at human recombinant somatostatin receptor subtypes supports its usefulness in neuroendocrine tumors. Neuroendocrinology80(Suppl. 1), 47–50 (2004).
  • Schmid HA. Pasireotide (SOM230), development, mechanism of action and potential applications. Mol. Cell. Endocrinol.286(1–2), 69–74 (2008).
  • Kvols LK, Moertel CG, O’Connell MJ, Schutt AJ, Rubin J, Hahn RG. Treatment of the malignant carcinoid syndrome. Evaluation of a long-acting somatostatin analogue. N. Engl. J. Med.315(11), 663–666 (1986).
  • Kvols LK, Martin JK, Marsh HM, Moertel CG. Rapid reversal of carcinoid crisis with a somatostatin analogue. N. Engl. J. Med.313(19), 1229–1230 (1985).
  • Garland J, Buscombe JR, Bouvier C et al. Sandostatin LAR (long-acting octreotide acetate) for malignant carcinoid syndrome: a 3-year experience. Aliment. Pharmacol. Ther.17(3), 437–444 (2003).
  • Welin SV, Janson ET, Sundin A et al. High-dose treatment with a long-acting somatostatin analogue in patients with advanced midgut carcinoid tumours. Eur. J. Endocrinol.151(1), 107–112 (2004).
  • Battershill PE, Clissold SP. Octreotide. A review of its pharmacodynamic and pharmacokinetic properties, and therapeutic potential in conditions associated with excessive peptide secretion. Drugs38(5), 658–702 (1989).
  • Maton PN, O’Dorisio TM, Howe BA et al. Effect of a long-acting somatostatin analogue (SMS 201–995) in a patient with pancreatic cholera. N. Engl. J. Med.312(1), 17–21 (1985).
  • Gyr KE, Meier R. Pharmacodynamic effects of Sandostatin in the gastrointestinal tract. Digestion54(Suppl. 1), 14–19 (1993).
  • Dueno MI, Bai JC, Santangelo WC, Krejs GJ. Effect of somatostatin analog on water and electrolyte transport and transit time in human small bowel. Dig. Dis. Sci.32(10), 1092–1096 (1987).
  • Anthony LB, Martin W, Delbeke D, Sandler M. Somatostatin receptor imaging: predictive and prognostic considerations. Digestion57(Suppl. 1), 50–53 (1996).
  • Ruszniewski P, Ish-Shalom S, Wymenga M et al. Rapid and sustained relief from the symptoms of carcinoid syndrome: results from an open 6-month study of the 28-day prolonged-release formulation of lanreotide. Neuroendocrinology80(4), 244–251 (2004).
  • Modlin IM, Pavel M, Kidd M, Gustafsson BI. Review article: somatostatin analogues in the treatment of gastroenteropancreatic neuroendocrine (carcinoid) tumours. Aliment. Pharmacol. Ther.31(2), 169–188 (2010).
  • Ricci S, Antonuzzo A, Galli L et al. Long-acting depot lanreotide in the treatment of patients with advanced neuroendocrine tumors. Am. J. Clin. Oncol.23(4), 412–415 (2000).
  • Wynick D, Anderson JV, Williams SJ, Bloom SR. Resistance of metastatic pancreatic endocrine tumours after long-term treatment with the somatostatin analogue octreotide (SMS 201–995). Clin. Endocrinol.30(4), 385–388 (1989).
  • Wynick D, Bloom SR. Clinical review 23: The use of the long-acting somatostatin analog octreotide in the treatment of gut neuroendocrine tumors. J. Clin. Endocrinol. Metab.73(1), 1–3 (1991).
  • Hofland LJ, van der Hoek J, Feelders R, van der Lely AJ, de Herder W, Lamberts SW. Pre-clinical and clinical experiences with novel somatostatin ligands: advantages, disadvantages and new prospects. J. Endocrinol. Invest.28(11 Suppl. International), 36–42 (2005).
  • van Vugt HH, Smid HA, Sailer AW. Ligand-dependent internalization of somatostatin receptors. Endocrine Abstracts16, P659 (2008).
  • Kvols L, Wiedenmann B, Öberg K et al. Safety and efficacy of pasireotide (SOM230) in patients with metastatic carcinoid tumors refractory or resistant to octreotide LAR: results of a Phase II study. Presented at: ASCO GI Cancers Symposium. San Francisco, CA, USA, 26–28 January 2006 (Abstract 171).
  • Grozinsky-Glasberg S, Shimon I, Korbonits M, Grossman AB. Somatostatin analogues in the control of neuroendocrine tumours: efficacy and mechanisms. Endocr. Relat. Cancer15(3), 701–720 (2008).
  • Arnold R, Trautmann ME, Creutzfeldt W et al. Somatostatin analogue octreotide and inhibition of tumour growth in metastatic endocrine gastroenteropancreatic tumours. Gut38(3), 430–438 (1996).
  • Panzuto F, Di Fonzo M, Iannicelli E et al. Long-term clinical outcome of somatostatin analogues for treatment of progressive, metastatic, well-differentiated entero-pancreatic endocrine carcinoma. Ann. Oncol.17(3), 461–466 (2006).
  • Shojamanesh H, Gibril F, Louie A et al. Prospective study of the antitumor efficacy of long-term octreotide treatment in patients with progressive metastatic gastrinoma. Cancer94(2), 331–343 (2002).
  • di Bartolomeo M, Bajetta E, Buzzoni R et al. Clinical efficacy of octreotide in the treatment of metastatic neuroendocrine tumors. A study by the Italian Trials in Medical Oncology Group. Cancer77(2), 402–408 (1996).
  • Saltz L, Trochanowski B, Buckley M et al. Octreotide as an antineoplastic agent in the treatment of functional and nonfunctional neuroendocrine tumors. Cancer72(1), 244–248 (1993).
  • Rinke A, Muller HH, Schade-Brittinger C et al. Placebo-controlled, double-blind, prospective, randomized study on the effect of octreotide LAR in the control of tumor growth in patients with metastatic neuroendocrine midgut tumors: a report from the PROMID Study Group. J. Clin. Oncol.27(28), 4656–4663 (2009).
  • Aparicio T, Ducreux M, Baudin E et al. Antitumour activity of somatostatin analogues in progressive metastatic neuroendocrine tumours. Eur. J. Cancer.37(8), 1014–1019 (2001).
  • Kulke MH. Neuroendocrine tumors: is there a standard treatment? Gastrointest. Cancer Res.2(3), 152–153 (2008).
  • Pavel M, Heuck F, Plockinger U et al. Prospective randomized trial: biotherapy versus chemotherapy in malignant nonfunctional neuroendocrine tumors of the pancreas and bronchial tract (ENET-1). Presented at: ASCO GI Cancers Symposium. Orlando, FL, USA, 25–27 January 2008 (Abstract 202).
  • Faiss S, Pape UF, Bohmig M et al. Prospective, randomized, multicenter trial on the antiproliferative effect of lanreotide, interferon a, and their combination for therapy of metastatic neuroendocrine gastroenteropancreatic tumors – the International Lanreotide and Interferon Alfa Study Group. J. Clin. Oncol.21(14), 2689–2696 (2003).
  • Strosberg J, Kvols L. Antiproliferative effect of somatostatin analogs in gastroenteropancreatic neuroendocrine tumors. World J. Gastroenterol.16(24), 2963–2970 (2010).
  • Öberg K, Kvols L, Caplin M et al. Consensus report on the use of somatostatin analogs for the management of neuroendocrine tumors of the gastroenteropancreatic system. Ann. Oncol.15(6), 966–973 (2004).
  • Arnold R, Rinke A, Klose KJ et al. Octreotide versus octreotide plus interferon-a in endocrine gastroenteropancreatic tumors: a randomized trial. Clin. Gastroenterol. Hepatol.3(8), 761–771 (2005).
  • Kolby L, Persson G, Franzen S, Ahren B. Randomized clinical trial of the effect of interferon alpha on survival in patients with disseminated midgut carcinoid tumours. Br. J. Surg.90(6), 687–693 (2003).
  • Bondanelli M, Ambrosio MR, Zatelli MC, Cavazzini L, Al Jandali Rifa’y L, Degli Uberti EC. Regression of liver metastases of occult carcinoid tumor with slow release lanreotide therapy. World J. Gastroenterol.11(13), 2041–2044 (2005).
  • Jensen RT, Berna MJ, Bingham DB, Norton JA. Inherited pancreatic endocrine tumor syndromes: advances in molecular pathogenesis, diagnosis, management, and controversies. Cancer113(7 Suppl.), 1807–1843 (2008).
  • Boulay A, Zumstein-Mecker S, Stephan C et al. Antitumor efficacy of intermittent treatment schedules with the rapamycin derivative RAD001 correlates with prolonged inactivation of ribosomal protein S6 kinase 1 in peripheral blood mononuclear cells. Cancer Res.64(1), 252–261 (2004).
  • Horsch D, Tielke S, Schrader J. Expression and activation of mTOR in neuroendocrine tumors: effects of mTOR inhibition by RAD001 upon growth, call cycle regulation and signaling in neuroendocrine cell lines. J. Clin. Oncol.25(Suppl. 18), 10570 (2007).
  • Cejka D, Preusser M, Fuereder T et al. mTOR inhibition sensitizes gastric cancer to alkylating chemotherapy in vivo. Anticancer Res.28(6A), 3801–3808 (2008).
  • Chollet P, Abrial C, Tacca O et al. Mammalian target of rapamycin inhibitors in combination with letrozole in breast cancer. Clin. Breast Cancer7(4), 336–338 (2006).
  • Yao JC, Phan AT, Chang DZ et al. Efficacy of RAD001 (everolimus) and octreotide LAR in advanced low- to intermediate-grade neuroendocrine tumors: results of a Phase II study. J. Clin. Oncol.26(26), 4311–4318 (2008).
  • Meric-Bernstam F, Gonzalez-Angulo AM. Targeting the mTOR signaling network for cancer therapy. J. Clin. Oncol.27(13), 2278–2287 (2009).
  • Pavel M. RADIANT-2 – No. LBA8. A randomized, double-blind, placebo controlled, multicentre Phase 3 trial of everolimus plus octreotide LAR vs. placebo plus octreotide LAR in patients with advanced neuroendocrine tumors (NET) (RADIANT-2). Presented at: European Society for Medical Oncology. Milan, Italy, 8–12 October 2010.
  • Raymond E, Niccoli P, Raoul J et al. Cox proportional hazard analysis of sunitinib (SU) efficacy across subgroups of patients (pts) with progressive pancreatic neuroendocrine tumors (NET). Presented at: ASCO Annual Meeting. Chicago, IL, USA, 4–8 June 2010 (Abstract 4031).
  • Yao J. RADIANT-3 – No. LBA9. A randomized, double-blind, placebo controlled, multicentre phase 3 trial of everolimus in patients with advanced pancreatic NETs. Presented at: European Society for Medical Oncology. Milan, Italy, 8–12 October 2010.
  • Moertel CG. Treatment of the carcinoid tumor and the malignant carcinoid syndrome. J. Clin. Oncol.1(11), 727–740 (1983).
  • Janson ET, Ronnblom L, Ahlstrom H et al. Treatment with alpha-interferon versus alpha-interferon in combination with streptozocin and doxorubicin in patients with malignant carcinoid tumors: a randomized trial. Ann. Oncol.3(8), 635–638 (1992).
  • Biesma B, Willemse PH, Mulder NH et al. Recombinant interferon alpha-2b in patients with metastatic apudomas: effect on tumours and tumour markers. Br. J. Cancer66(5), 850–855 (1992).
  • Turner HE, Lindsell DR, Vadivale A, Thillainayagam AV, Wass JA. Differing effects on gall-bladder motility of lanreotide SR and octreotide LAR for treatment of acromegaly. Eur. J. Endocrinol.141(6), 590–594 (1999).
  • Ekeblad S, Sundin A, Janson ET et al. Temozolomide as monotherapy is effective in treatment of advanced malignant neuroendocrine tumors. Clin. Cancer Res.13(10), 2986–2991 (2007).
  • Kulke MH, Stuart K, Enzinger PC et al. Phase II study of temozolomide and thalidomide in patients with metastatic neuroendocrine tumors. J. Clin. Oncol.24(3), 401–406 (2006).
  • Strosberg JR, Fine RL, Choi J et al. First-line chemotherapy with capecitabine and temozolomide in patients with metastatic pancreatic endocrine carcinomas. Cancer DOI: 10.1002/cncr.25425 (2010) (Epub ahead of print).
  • Forrer F, Valkema R, Kwekkeboom DJ, de Jong M, Krenning EP. Neuroendocrine tumors. Peptide receptor radionuclide therapy. Best Pract. Res. Clin. Endocrinol. Metab.21(1), 111–129 (2007).
  • Comaru-Schally AM, Schally AV. A clinical overview of carcinoid tumors: perspectives for improvement in treatment using peptide analogs (review). Int. J. Cancer26(2), 301–309 (2005).
  • Valkema R, Pauwels S, Kvols LK et al. Survival and response after peptide receptor radionuclide therapy with [90Y-DOTA0,Tyr3]octreotide in patients with advanced gastroenteropancreatic neuroendocrine tumors. Semin. Nucl. Med. 36(2), 147–156 (2006).
  • Kwekkeboom DJ, de Herder WW, Kam BL et al. Treatment with the radiolabeled somatostatin analog [177 Lu-DOTA 0,Tyr3]octreotate: toxicity, efficacy, and survival. J. Clin. Oncol.26(13), 2124–2130 (2008).
  • Wolin E, Kvols L, Ezzat S et al. Pasireotide LAR in patients with metastatic carcinoid tumors: pharmacokinetics (PK) and safety results from a randomized, multicenter, Phase I study. Presented at: ASCO GI Cancers Symposium. San Francisco, CA, USA, 15–17 Januray 2009 (Abstract 93).
  • Pasquali D, Rossi V, Conzo G et al. Effects of somatostatin analog SOM230 on cell proliferation, apoptosis, and catecholamine levels in cultured pheochromocytoma cells. J. Mol. Endocrinol.40(6), 263–271 (2008).
  • Pavel M, Hassler G, Schmid HA, van Vugt HH, Hahn EG, Schuppan DS. Pasireotide strongly inhibits migration and proliferation of human micro- and macrovascular endothelial cells mainly via somatostatin receptor subtype 5 and FAK, ERK1/2 and p38 pathways. ENDO Abstract 1, P2–352 (2006).
  • Strosberg JR, Nasir A, Hodul P, Kvols L. Biology and treatment of metastatic gastrointestinal neuroendocrine tumors. Gastrointest. Cancer Res.2(3), 113–125 (2008).

Websites

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.