Systemic treatment of gastroenteropancreatic neuroendocrine tumors (GEP-NETs): Cuirrent approaches and future options

Endocrine Practice

Volumn 20, Issue 2, 2014, Pages 167-175

  Strosberg, Jonathan R ^a  

^a H LEE MOFFITT CANCER CENTER AND RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTINEOPLASTIC AGENT; RADIOPHARMACEUTICAL AGENT; SOMATOSTATIN;

ANALOGS AND DERIVATIVES; HUMAN; INTESTINAL NEOPLASMS; NEUROENDOCRINE TUMORS; PANCREATIC NEOPLASMS; STOMACH NEOPLASMS;

ANTINEOPLASTIC AGENTS; HUMANS; INTESTINAL NEOPLASMS; NEUROENDOCRINE TUMORS; PANCREATIC NEOPLASMS; RADIOPHARMACEUTICALS; SOMATOSTATIN; STOMACH NEOPLASMS;

EID: 84894118346     PISSN: 1530891X     EISSN: 19342403     Source Type: Journal    
DOI: 10.4158/EP13262.RA     Document Type: Review

References (74)

1. Reichlin S. Somatostatin. N Engl J Med. 1983;309:1495-1501.
2. Evers BM, Parekh D, Townsend CM Jr, Thompson JC. Somatostatin and analogues in the treatment of cancer. A review. Ann Surg. 1991;213:190-198.
3. Maurer R, Reubi JC. Somatostatin receptors. JAMA. 1985;253:2741.
4. Reubi JC, Schär JC, Waser B, et al. Affinity profiles for human somatostatin receptor subtypes SST1-SST5 of somatostatin radiotracers selected for scintigraphic and radiotherapeutic use. Eur J Nucl Med. 2000;27:273-282.
5. Bauer W, Briner U, Doepfner W, et al. SMS 201-995: a very potent and selective octapeptide analogue of somatostatin with prolonged action. Life Sci. 1982;31:1133-1140.
6. 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. 1986;315:663-666.
7. O'Toole D, Ducreux M, Bommelaer G, et al. Treatment of carcinoid syndrome: a prospective crossover evaluation of lanreotide versus octreotide in terms of efficacy, patient acceptability, and tolerance. Cancer. 2000;88:770-776.
8. O'Dorisio TM, Gaginella TS, Mekhjian HS, Rao B, O'Dorisio MS. Somatostatin and analogues in the treatment of VIPoma. Ann N Y Acad Sci. 1988;527:528-535.
9. Maton PN. Use of octreotide acetate for control of symptoms in patients with islet cell tumors. World J Surg. 1993;17:504-510.
10. Jensen RT. Gastrinomas: advances in diagnosis and management. Neuroendocrinology. 2004;80 Suppl 1:23-27.
11. 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. 1999;17:600-606.
12. Wymenga AN, Eriksson B, Salmela PI, et al. Efficacy and safety of prolonged-release lanreotide in patients with gastrointestinal neuroendocrine tumors and hormone-related symptoms. J Clin Oncol. 1999;17:1111.
13. Ruszniewski P, Ducreux M, Chayvialle JA, et al. Treatment of the carcinoid syndrome with the longacting somatostatin analogue lanreotide: a prospective study in 39 patients. Gut. 1996;39:279-283.
14. Bronstein M, Musolino N, Jallad R, et al. Pharmacokinetic profile of lanreotide Autogel in patients with acromegaly after four deep subcutaneous injections of 60, 90 or 120 mg every 28 days. Clin Endocrinol (Oxf). 2005;63:514-519.
15. Eriksson B, Klöppel G, Krenning E, et al. Consensus guidelines for the management of patients with digestive neuroendocrine tumors-well- differentiated jejunal-ileal tumor/carcinoma. Neuroendocrinology. 2008;87:8-19.
16. Strosberg J, Weber J, Feldman M, Goldman J, Almhanna K, Kvols L. Above-label doses of octreotide LAR in patients with metastatic small-intestinal carcinoid tumors. Gastrointest Cancer Res. 2013;6:81-85.
17. Woltering EA, Mamikunian PM, Zietz S, et al. Effect of octreotide LAR dose and weight on octreotide blood levels in patients with neuroendocrine tumors. Pancreas. 2005;31:392-400.
18. Kahil ME, Brown H, Fred HL. The Carcinoid Crisis. Arch Intern Med. 1964;114:26-28.
19. Kvols LK, Martin JK, Marsh HM, Moertel CG. Rapid reversal of carcinoid crisis with a somatostatin analogue. N Engl J Med. 1985;313:1229-1230.
20. Strosberg J, Kvols L. Antiproliferative effect of somatostatin analogs in gastroenteropancreatic neuroendocrine tumors. World J Gastroenterol. 2010;16:2963-2970.
21. Ducreux M, Ruszniewski P, Chayvialle JA, et al. The antitumoral effect of the long-acting somatostatin analog lanreotide in neuroendocrine tumors. Am J Gastroenterol. 2000;95:3276-3281.
22. Reardon DB, Dent P, Wood SL, Kong T, Sturgill TW. Activation in vitro of somatostatin receptor subtypes 2, 3, or 4 stimulates protein tyrosine phosphatase activity in membranes from transfected Ras-transformed NIH 3T3 cells: coexpression with catalytically inactive SHP-2 blocks responsiveness. Mol Endocrinol. 1997;11:1062-1069.
23. Weckbecker G, Lewis I, Albert R, Schmid HA, Hoyer D, Bruns C. Opportunities in somatostatin research: biological, chemical and therapeutic aspects. Nat Rev Drug Discov. 2003;2:999-1017.
24. Ambler GR, Butler AA, Padmanabhan J, Breier BH, Gluckman PD. The effects of octreotide on GH receptor and IGF-I expression in the GH-deficient rat. J Endocrinol. 1996;149:223-231.
25. Woltering EA, Watson JC, Alperin-Lea RC, et al. Somatostatin analogs: angiogenesis inhibitors with novel mechanisms of action. Invest New Drugs. 1997;15:77-86.
26. Florio T, Morini M, Villa V, et al. Somatostatin inhibits tumor angiogenesis and growth via somatostatin receptor-3-mediated regulation of endothelial nitric oxide synthase and mitogen-activated protein kinase activities. Endocrinology. 2003;144:1574-1584.
27. Tomassetti P, Migliori M, Corinaldesi R, Gullo L. Treatment of gastroenteropancreatic neuroendocrine tumours with octreotide LAR. Aliment Pharmacol Ther. 2000;14:557-560.
28. 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. 2000;23:412-415.
29. Rinke A, Müller 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. 2009;27:4656-4663.
30. Kulke MH, Benson AB 3rd, Bergsland E, et al. Neuroendocrine tumors. J Natl Compr Canc Netw. 2012. 10:724-764.
31. Kunz PL, Reidy-Lagunes D, Anthony LB, et al. Consensus guidelines for the management and treatment of neuroendocrine tumors. Pancreas. 2013;42:557-577.
32. Oberg K. Interferons in the management of neuroendocrine tumors and their possible mechanism of action. Yale J Biol Med. 1992;65:519-29; discussion 531-536.
33. Detjen KM, Welzel M, Farwig K, et al. Molecular mechanism of interferon alfa-mediated growth inhibition in human neuroendocrine tumor cells. Gastroenterology. 2000;118:735-748.
34. Oberg K, Funa K, Alm G. Effects of leukocyte interferon on clinical symptoms and hormone levels in patients with mid-gut carcinoid tumors and carcinoid syndrome. N Engl J Med. 1983;309:129-133.
35. Janson ET, Oberg K. Long-term management of the carcinoid syndrome. Treatment with octreotide alone and in combination with alpha-interferon. Acta Oncol. 1993;32:225-229.
36. Frank M, Klose KJ, Wied M, Ishaque N, Schade-Brittinger C, Arnold R. Combination therapy with octreotide and alpha-interferon: effect on tumor growth in metastatic endocrine gastroenteropancreatic tumors. Am J Gastroenterol. 1999;94:1381-1387.
37. Kölby L, Persson G, Franzén S, Ahrén B. Randomized clinical trial of the effect of interferon alpha on survival in patients with disseminated midgut carcinoid tumours. Br J Surg. 2003. 90:687-693.
38. Arnold R, Rinke A, Klose KJ, et al. Octreotide versus octreotide plus interferon-alpha in endocrine gastroenteropancreatic tumors: a randomized trial. Clin Gastroenterol Hepatol. 2005;3:761-771.
39. Faiss S, Pape UF, Böhmig M, et al. Prospective, randomized, multicenter trial on the antiproliferative effect of lanreotide, interferon alfa, and their combination for therapy of metastatic neuroendocrine gastroenteropancreatic tumors-the International Lanreotide and Interferon Alfa Study Group. J Clin Oncol. 2003;21:2689-2696.
40. Meric-Bernstam F, Gonzalez-Angulo AM. Targeting the mTOR signaling network for cancer therapy. J Clin Oncol. 2009;27:2278-2287.
41. Verhoef S, van Diemen-Steenvoorde R, Akkersdijk WL, et al. Malignant pancreatic tumour within the spectrum of tuberous sclerosis complex in childhood. Eur J Pediatr. 1999;158:284-287.
42. Jiao Y, Shi C, Edil BH, et al. DAXX/ATRX, MEN1, and mTOR pathway genes are frequently altered in pancreatic neuroendocrine tumors. Science. 2011;331:1199-1203.
43. Banck MS, Kanwar R, Kulkarni AA, et al. The genomic landscape of small intestine neuroendocrine tumors. J Clin Invest. 2013;123:2502-2508.
44. 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. 2010;28:69-76.
45. Pavel ME, Hainsworth JD, Baudin E, et al. Everolimus plus octreotide long-acting repeatable for the treatment of advanced neuroendocrine tumours associated with carcinoid syndrome (RADIANT-2): a randomised, placebo-controlled, phase 3 study. Lancet. 2011;378:2005-2012.
46. Yao JC, Shah MH, Ito T, et al. Everolimus for advanced pancreatic neuroendocrine tumors. N Engl J Med. 2011;364:514-523.
47. Terris B, Scoazec JY, Rubbia L, et al. Expression of vascular endothelial growth factor in digestive neuroendocrine tumours. Histopathology. 1998;32:133-138.
48. Yao JC, Phan A, Hoff PM, et al. Targeting vascular endothelial growth factor in advanced carcinoid tumor: a random assignment phase II study of depot octreotide with bevacizumab and pegylated interferon alpha-2b. J Clin Oncol. 2008;26:1316-1323.
49. Kulke MH, Lenz HJ, Meropol NJ, et al. Activity of sunitinib in patients with advanced neuroendocrine tumors. J Clin Oncol. 2008;26:3403-3410.
50. Raymond E, Dahan L, Raoul JL, et al. Sunitinib malate for the treatment of pancreatic neuroendocrine tumors. N Engl J Med. 2011;364:501-513.
51. Vinik A, Bang Y, Raoul J, et al. Patient-reported outcomes (PROs) in patients with pancreatic neuroendocrine tumors receiving sunitinib in a phase III trial. J Clin Oncol. 2010;28:15s, 2010.
52. Klimstra DS, Modlin IR, Coppola D, Lloyd RV, Suster S. The pathologic classification of neuroendocrine tumors: a review of nomenclature, grading, and staging systems. Pancreas. 2010;39:707-712.
53. Moertel CG, Kvols LK, O'Connell MJ, Rubin J. Treatment of neuroendocrine carcinomas with combined etoposide and cisplatin. Evidence of major therapeutic activity in the anaplastic variants of these neoplasms. Cancer. 1991;68:227-232.
54. Mitry E, Baudin E, Ducreux M, et al. Treatment of poorly differentiated neuroendocrine tumours with etoposide and cisplatin. Br J Cancer. 1999;81:1351-1355.
55. Broder LE, Carter SK. Pancreatic islet cell carcinoma. II. Results of therapy with streptozotocin in 52 patients. Ann Intern Med. 1973;79:108-118.
56. 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.
57. Moertel CG, Lefkopoulo M, Lipsitz S, Hahn RG, Klaassen D. Streptozocin-doxorubicin, streptozocin-fluorouracil or chlorozotocin in the treatment of advanced islet-cell carcinoma. N Engl J Med. 1992;326:519-523.
58. McCollum AD, Kulke MH, Ryan DP, et al. Lack of efficacy of streptozocin and doxorubicin in patients with advanced pancreatic endocrine tumors. Am J Clin Oncol. 2004;27:485-488.
59. Kouvaraki MA, Ajani JA, Hoff P, et al. Fluorouracil, doxorubicin, and streptozocin in the treatment of patients with locally advanced and metastatic pancreatic endocrine carcinomas. J Clin Oncol. 2004;22:4762-4771.
60. Kulke MH, Stuart K, Enzinger PC, et al. Phase II study of temozolomide and thalidomide in patients with metastatic neuroendocrine tumors. J Clin Oncol. 2006;24:401-406.
61. 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.
62. 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.
63. Sun W, Lipsitz S, Catalano P, et al. Phase II/III study of doxorubicin with fluorouracil compared with streptozocin with fluorouracil or dacarbazine in the treatment of advanced carcinoid tumors: Eastern Cooperative Oncology Group Study E1281. J Clin Oncol. 2005;23:4897-4904.
64. 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.
65. Krenning EP, Valkema R, Kooij PP, et al. The role of radioactive somatostatin and its analogues in the control of tumor growth. Recent Results Cancer Res. 2000;153:1-13.
66. Valkema R, De Jong M, Bakker WH, et al. Phase I study of peptide receptor radionuclide therapy with (In-DTPA) octreotide: the Rotterdam experience. Semin Nucl Med. 2002;32:110-122.
67. Kwekkeboom DJ, Mueller-Brand J, Paganelli G, et al. Overview of results of peptide receptor radionuclide therapy with 3 radiolabeled somatostatin analogs. J Nucl Med. 2005;46 Suppl 1:62S-66S.
68. Paganelli G, Bodei L, Handkiewicz Junak D, et al. 90Y-DOTA-D-Phe1-Try3- octreotide in therapy of neuroendocrine malignancies. Biopolymers. 2002;66:393-398.
69. 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. 2006;36:147-156.
70. Bushnell DL Jr, O'Dorisio TM, O'Dorisio MS, et al. 90Y-edotreotide for metastatic carcinoid refractory to octreotide. J Clin Oncol. 2010;28:1652-1659.
71. Imhof A, Brunner P, Marincek N, et al. Response, survival, and long-term toxicity after therapy with the radiolabeled somatostatin analogue [90Y-DOTA]-TOC in metastasized neuroendocrine cancers. J Clin Oncol. 2011:29:2416-2423.
72. 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. 2008;26:2124-2130.
73. A Study Comparing Treatment With 177Lu-DOTA0-Tyr3-Octreotate to Octreotide LAR in Patients With Inoperable, Progressive, Somatostatin Receptor Positive Midgut Carcinoid Tumours (NETTER-1): ClinicalTrials. gov Identifier NCT015782139. 2013.
74. Casciano R, Wang X, Stern L, et al. International practice patterns and resource utilization in the treatment of neuroendocrine tumors. Pancreas. 2013;42:339-347.