Evolving treatment strategies for management of carcinoid tumors

Current Treatment Options in Oncology

Volumn 14, Issue 3, 2013, Pages 374-388

  Strosberg, Jonathan ^a  

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

Author keywords

Carcinoid tumor; Neuroendocrine tumor; Treatment

Indexed keywords

ANGIOGENESIS INHIBITOR; ANGIOPEPTIN; AXITINIB; BEVACIZUMAB; CISPLATIN; DOXORUBICIN; EDOTREOTIDE; EDOTREOTIDE Y 90; ETOPOSIDE; EVEROLIMUS; GADOLINIUM PENTETATE; INDIUM 111; IRINOTECAN; LUTETIUM 177; MAMMALIAN TARGET OF RAPAMYCIN INHIBITOR; OCTREOTIDE; OCTREOTIDE IN 11; PASIREOTIDE; PAZOPANIB; PEGINTERFERON ALPHA; PLACEBO; PLATINUM; PROTEIN TYROSINE KINASE INHIBITOR; SOMATOSTATIN DERIVATIVE; SUNITINIB; TETRAXETAN; UNCLASSIFIED DRUG; UNINDEXED DRUG; VASCULOTROPIN ANTIBODY; VASCULOTROPIN INHIBITOR; YTTRIUM 90;

ANTIPROLIFERATIVE ACTIVITY; APHTHOUS ULCER; BINDING AFFINITY; BLOATING; BLOOD FLOW; CANCER CELL; CANCER COMBINATION CHEMOTHERAPY; CANCER GROWTH; CANCER INHIBITION; CANCER SURVIVAL; CARCINOID; CHEMOEMBOLIZATION; CHEMOSENSITIVITY; DIARRHEA; DRUG EFFICACY; DRUG HALF LIFE; DRUG MECHANISM; DRUG MEGADOSE; DRUG RECEPTOR BINDING; DRUG RESPONSE; DRUG TARGETING; FATIGUE; GALLSTONE; HAND FOOT SYNDROME; HEMATOLOGIC DISEASE; HUMAN; HYPERGLYCEMIA; HYPERTENSION; INFECTION; ISOTOPE LABELING; KIDNEY FAILURE; LIVER METASTASIS; MULTIPLE CYCLE TREATMENT; NAUSEA; NEUROENDOCRINE TUMOR; OVERALL SURVIVAL; PANCREATIC NEUROENDOCRINE TUMOR; PNEUMONIA; POSTOPERATIVE NAUSEA AND VOMITING; PROGRESSION FREE SURVIVAL; QUALITY OF LIFE; RADIOFREQUENCY ABLATION; RASH; REVIEW; SALVAGE THERAPY; SINGLE DRUG DOSE; STEATORRHEA; STOMACH CARCINOID; THROMBOCYTOPENIA; TREATMENT DURATION; TUMOR GROWTH;

CARCINOID TUMOR; CELL PROLIFERATION; GASTROINTESTINAL TRACT; HUMANS; LUNG NEOPLASMS; NEOPLASM STAGING; NEUROENDOCRINE TUMORS; SIGNAL TRANSDUCTION; SOMATOSTATIN; TOR SERINE-THREONINE KINASES; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 84884204951     PISSN: 15272729     EISSN: 15346277     Source Type: Journal    
DOI: 10.1007/s11864-013-0246-4     Document Type: Review

References (76)

1. Feyrter F. Über diffuse endocrine epitheliale Organe. Leipzig: Barth; 1938.
2. Oberndorfer S. Karzinoide Tumoren des Dünndarms. Frankf Z Pathol. 1907;1:425-9.
3. Williams ED, Sandler M. The classification of carcinoid tum ours. Lancet. 1963;1:238-9.
4. Strosberg JR, Nasir A, Hodul P, Kvols L. Biology and treatment of metastatic gastrointestinal neuroendocrine tumors. Gastrointest Cancer Res. 2008;2(3):113-25.
5. 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;26:3063-72.
6. Strosberg JR, Weber JM, Feldman M, Coppola D, Meredith K, Kvols LK. Prognostic validity of the American Joint Committee on Cancer staging classification for midgut neuroendocrine tumors. J Clin Oncol. 2013;31:420-5.
7. Brazeau P, Vale W, Burgus R, et al. Hypothalamic polypeptide that inhibits the secretion of immunoreactive pituitary growth hormone. Science. 1973;179:77-9.
8. Reichlin S. Somatostatin. N Engl J Med. 1983;309:1495-501.
9. Maurer R, Reubi JC. Somatostatin receptors. JAMA. 1985;253:2741.
10. Lamberts SW, van der Lely AJ, de Herder WW, Hofland LJ. Octreotide. N Engl J Med. 1996;334:246-54.
11. 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;315:663-6.
12. 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;39:279-83.
13. O'Toole D, Ducreux M, Bommelaer G, et al. Treatment of carcinoid syndrome: a prospective crossover evaluation of lanreotide vs octreotide in terms of efficacy, patient acceptability, and tolerance. Cancer. 2000;88:770-6.
14. Rubin J, Ajani J, Schirmer W, et al. Octreotide acetate long-acting formulation vs open-label subcutaneous octreotide acetate in malignant carcinoid syndrome. J Clin Oncol. 1999;17:600-6.
15. Strosberg J, Kvols L. Antiproliferative effect of somatostatin analogs in gastroenteropancreatic neuroendocrine tumors. World J Gastroenterol. 2010;16:2963-70.
16. Florio T. Somatostatin/somatostatin receptor signalling: phosphotyrosine phosphatases. Mol Cell Endocrinol. 2008;286:40-8.
17. Florio T, Yao H, Carey KD, Dillon TJ, Stork PJ. Somatostatin activation of mitogen-activated protein kinase via somatostatin receptor 1 (SSTR1). Mol Endocrinol. 1999;13:24-37.
18. Serri O, Brazeau P, Kachra Z, Posner B. Octreotide inhibits insulin-like growth factor-I hepatic gene expression in the hypophysectomized rat: evidence for a direct and indirect mechanism of action. Endocrinology. 1992;130:1816-21.
19. 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.
20. 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. 2009;27:4656-63.
21. Kulke MH, Benson III AB, Bergsland E, et al. Neuroendocrine tumors. J Natl Compr Canc Netw. 2012;10:724-64.
22. Study of lanreotide autogel in nonfunctioning entero-pancreatic endocrine tumours. ClinicalTrials.gov Identifier: NCT00326469. 2006.
23. Pritchard KI, Shepherd LE, Chapman JA, et al. Randomized trial of tamoxifen vs combined tamoxifen and octreotide LAR Therapy in the adjuvant treatment of early-stage breast cancer in postmenopausal women: NCIC CTG MA.14. J Clin Oncol. 2011;29:3869-76.
24. Strosberg J, Bobiak S, Zornosa C, et al. Dosing patterns for octreotide LAR in neuroendocrine tumor patients. Paper presented at the American Society of Clinical Oncology conference, Chicago, May 31-June 4, 2013.
25. Weber J, Feldman M, Kvols L, Strosberg J. Above-label doses of octreotide LAR in patients with metastatic small-intestinal carcinoid tumors. J Clin Oncol. 2012;(Suppl):Abstract e14579.
26. Schmid HA. Pasireotide (SOM230): development, mechanism of action and potential applications. Mol Cell Endocrinol. 2008;286:69-74.
27. Kvols LK, Oberg KE, O'Dorisio TM, et al. Pasireotide (SOM230) shows efficacy and tolerability in the treatment of patients with advanced neuroendocrine tumors refractory or resistant to octreotide LAR: results from a phase II study. Endocr Relat Cancer. 2012;19:657-66.
28. van Vliet EI, Teunissen JJ, Kam BL, de Jong M, Krenning EP, Kwekkeboom DJ. Treatment of gastroenteropancreatic neuroendocrine tumors with peptide receptor radionuclide therapy. Neuroendocrinology. 2013;97:74-85.
29. Reubi JC, Schar 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;27:273-82.
30. Anthony LB, Woltering EA, Espenan GD, Cronin MD, Maloney TJ, McCarthy KE. Indium-111-pentetreotide prolongs survival in gastroenteropancreatic malignancies. Semin Nucl Med. 2002;32:123-32.
31. 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;32:110-22.
32. Paganelli G, Bodei L, Handkiewicz Junak D, et al. 90Y-DOTA-D-Phe1-Try3- octreotide in therapy of neuroendocrine malignancies. Biopolymers. 2002;66:393-8.
33. 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;36:147-56.
34. Bushnell DL Jr, O'Dorisio TM, O'Dorisio MS, et al. 90Y-edotreotide for metastatic carcinoid refractory to octreotide. J Clin Oncol. 2010;28:1652-9.
35. 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;29:2416-23.
36. 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;26:2124-30.
37. 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. http://clinicaltrials.gov. Accessed April 15, 2013.
38. Meric-Bernstam F, Gonzalez-Angulo AM. Targeting the mTOR signaling network for cancer therapy. J Clin Oncol. 2009;27:2278-87.
39. Vignot S, Faivre S, Aguirre D, Raymond E. mTOR-targeted therapy of cancer with rapamycin derivatives. Ann Oncol. 2005;16:525-37.
40. Jiao Y, Shi C, Edil BH, et al. DAXX/ATRX, MEN1, and mTOR pathway genes are frequently altered in pancreatic neuroendocrine tumors. Science. 2011;331:1199-203.
41. Yao JC, Shah MH, Ito T, et al. Everolimus for advanced pancreatic neuroendocrine tumors. N Engl J Med. 2011;364:514-23.
42. 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 randomized, placebo-controlled, phase 3 study. Lancet. 2011;378:2005-12. Randomized phase III study of 429 patients demonstrating an improvement of PFS with everolimus vs placebo, which fell just short of statistical significance on central radiographic review. Thus, the role of everolimus in carcinoid tumors remains controversial.
43. Scoazec JY. Angiogenesis in neuroendocrine tumors: therapeutic applications. Neuroendocrinology. 2013;97:45-56.
44. La Rosa S, Uccella S, Finzi G, Albarello L, Sessa F, Capella C. Localization of vascular endothelial growth factor and its receptors in digestive endocrine tumors: correlation with microvessel density and clinicopathologic features. Hum Pathol. 2003;34:18-27.
45. 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;26:1316-23.
46. Kulke MH, Lenz HJ, Meropol NJ, et al. Activity of sunitinib in patients with advanced neuroendocrine tumors. J Clin Oncol. 2008;26:3403-10.
47. Phan A, Yao J, Fogelman D, et al. A prospective multi-institutional phase II study of GW786034 (pazopanib) and depot octreotide (Sandostatin LAR) in advanced low-grade neuroendocrine carcinoma (LGNEC). J Clin Oncol. 2010;28 Suppl 15.
48. 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;68:227-32.
49. Sorbye H, Welin S, Langer SW, et al. Predictive and prognostic factors for treatment and survival in 305 patients with advanced gastrointestinal neuroendocrine carcinoma (WHO G3): the NORDIC NEC study. Ann Oncol. 2013;24:152-60. Large multi-institutional series of high-grade neuroendocrine cancers demonstrating that only patients with very high ki-67 proliferative index (>55%) are likely to respond to platinum/etoposide based therapy.
50. 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;24:401-6.
51. Chan JA, Stuart K, Earle CC, et al. Prospective study of bevacizumab plus temozolomide in patients with advanced neuroendocrine tumors. J Clin Oncol. 2012;30:2963-8.
52. 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;15:338-45.
53. Crona J, Bjorklund P, Welin S, Kozlovacki G, Oberg K, Granberg D. Treatment, prognostic markers and survival in thymic neuroendocrine tumour: a study from a single tertiary referral centre. Lung Cancer. 2013;79:289-93.
54. Saranga-Perry V, Morse B, Centeno B, Kvols L, Strosberg J. Treatment of metastatic neuroendocrine tumors of the thymus with capecitabine and temozolomide: a case series. Neuroendocrinology. 2013;97(4):318-21.
55. Ekeblad S, Sundin A, Janson ET, et al. Temozolomide as monotherapy is effective in treatment of advanced malignant neuroendocrine tumors. Clin Cancer Res. 2007;13:2986-91.
56. Proye C. Natural history of liver metastasis of gastroenteropancreatic neuroendocrine tumors: place for chemoembolization. World J Surg. 2001;25:685-8.
57. Strosberg JR, Choi J, Cantor AB, Kvols LK. Selective hepatic artery embolization for treatment of patients with metastatic carcinoid and pancreatic endocrine tumors. Cancer Control. 2006;13:72-8.
58. Eriksson BK, Larsson EG, Skogseid BM, Lofberg AM, Lorelius LE, Oberg KE. Liver embolizations of patients with malignant neuroendocrine gastrointestinal tumors. Cancer. 1998;83:2293-301.
59. Ruszniewski P, Malka D. Hepatic arterial chemoembolization in the management of advanced digestive endocrine tumors. Digestion. 2000;62 Suppl 1:79-83.
60. Gupta S, Yao JC, Ahrar K, et al. Hepatic artery embolization and chemoembolization for treatment of patients with metastatic carcinoid tumors: the M.D. Anderson experience. Cancer J. 2003;9:261-7.
61. Loewe C, Schindl M, Cejna M, Niederle B, Lammer J, Thurnher S. Permanent transarterial embolization of neuroendocrine metastases of the liver using cyanoacrylate and lipiodol: assessment of mid- and long-term results. Am J Roentgenol. 2003;180:1379-84.
62. Therasse E, Breittmayer F, Roche A, et al. Transcatheter chemoembolization of progressive carcinoid liver metastasis. Radiology. 1993;189:541-7.
63. Andrews JC, Walker SC, Ackermann RJ, Cotton LA, Ensminger WD, Shapiro B. Hepatic radioembolization with yttrium-90 containing glass microspheres: preliminary results and clinical follow-up. J Nucl Med. 1994;35:1637-44.
64. Sato K, Lewandowski RJ, Bui JT, et al. Treatment of unresectable primary and metastatic liver cancer with yttrium-90 microspheres (TheraSphere): assessment of hepatic arterial embolization. Cardiovasc Intervent Radiol. 2006;29:522-9.
65. Rhee TK, Lewandowski RJ, Liu DM, et al. 90Y Radioembolization for metastatic neuroendocrine liver tumors: preliminary results from a multi-institutional experience. Ann Surg. 2008;247:1029-35.
66. Kennedy AS, Dezarn WA, McNeillie P, et al. Radioembolization for unresectable neuroendocrine hepatic metastases using resin 90Y-microspheres: early results in 148 patients. Am J Clin Oncol. 2008;31:271-9.
67. Giovannini M. Percutaneous alcohol ablation for liver metastasis. Semin Oncol. 2002;29:192-5.
68. Cozzi PJ, Englund R, Morris DL. Cryotherapy treatment of patients with hepatic metastases from neuroendocrine tumors. Cancer. 1995;76:501-9.
69. Siperstein AE, Rogers SJ, Hansen PD, Gitomirsky A. Laparoscopic thermal ablation of hepatic neuroendocrine tumor metastases. Surgery. 1997;122:1147-54. discussion 1154-45.
70. Lounsberry W, Goldschmidt V, Linke CA, Walder HJ, Chrzan D. The early histologic changes following electrocoagulation. J Urol. 1961;86:321-9.
71. Berber E, Flesher N, Siperstein AE. Laparoscopic radiofrequency ablation of neuroendocrine liver metastases. World J Surg. 2002;26:985-90.
72. O'Toole D, Maire F, Ruszniewski P. Ablative therapies for liver metastases of digestive endocrine tumours. Endocr Relat Cancer. 2003;10:463-8.
73. Henn AR, Levine EA, McNulty W, Zagoria RJ. Percutaneous radiofrequency ablation of hepatic metastases for symptomatic relief of neuroendocrine syndromes. Am J Roentgenol. 2003;181:1005-10.
74. Gillams A, Cassoni A, Conway G, Lees W. Radiofrequency ablation of neuroendocrine liver metastases-the Middlesex experience. Abdom Imaging. 2005;30(4):435-41.
75. Strosberg JR, Weber JM, Choi J, et al. A phase II clinical trial of sunitinib following hepatic transarterial embolization for metastatic neuroendocrine tumors. Ann Oncol. 2012;23:2335-41.
76. Yao J, Phan A, Fogelman D, et al. Randomized run-in study of bevacizumab and everolimus in low- to intermediate-grade neuroendocrine tumors (LGNETs) using perfusion CT as functional biomarker. J Clin Oncol. 2010;28. Suppl 15.