Neuroendocrine tumours of the small intestine

Best Practice and Research: Clinical Gastroenterology

Volumn 26, Issue 6, 2012, Pages 755-773

  Strosberg, Jonathan ^a  

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

Author keywords

Carcinoid; Carcinoid syndrome; Duodenum; Ileum; Jejunum; Midgut; Neuroendocrine tumour

Indexed keywords

5 HYDROXYINDOLEACETIC ACID; 5 HYDROXYTRYPTOPHAN; ALPHA INTERFERON; ANGIOPEPTIN; BEVACIZUMAB; CHROMOGRANIN A; CHROMOGRANIN B; CISPLATIN; DOPAMINE; DOXORUBICIN; ENOLASE; EVEROLIMUS; HISTAMINE; KALLIKREIN; NEUROKININ A; OCTREOTIDE; PANCREASTATIN; PAZOPANIB; PEGINTERFERON ALPHA; PENTETREOTIDE IN 111; PLACEBO; PROSTAGLANDIN; SECRETOGRANIN II; SUBSTANCE P; SUNITINIB; TEMOZOLOMIDE; THALIDOMIDE; TUMOR MARKER;

ABDOMINAL PAIN; ADD ON THERAPY; ANTIPROLIFERATIVE ACTIVITY; APHTHOUS ULCER; ARTICLE; BONE MARROW SUPPRESSION; CANCER CHEMOTHERAPY; CANCER CLASSIFICATION; CANCER GRADING; CANCER INCIDENCE; CANCER PROGNOSIS; CANCER STAGING; CANCER SURVIVAL; CARCINOID SYNDROME; CHEMOEMBOLIZATION; CHOLESTASIS; CLINICAL FEATURE; COMPUTER ASSISTED TOMOGRAPHY; CYTOPENIA; DEPRESSION; DISEASE SPECIFIC SURVIVAL; DNA REPLICATION; DRUG TOLERABILITY; DUODENUM OBSTRUCTION; ENDOSCOPIC SURGERY; FAMILY HISTORY; FLU LIKE SYNDROME; G1 PHASE CELL CYCLE CHECKPOINT; GENE OVEREXPRESSION; HEMICOLECTOMY; HUMAN; HYPERGLYCEMIA; LIFE EXPECTANCY; LIVER TRANSPLANTATION; LOW DRUG DOSE; MESENTERIC ISCHEMIA; MONOTHERAPY; MULTICENTER STUDY (TOPIC); MYALGIA; NEUROENDOCRINE TUMOR; NUCLEAR MAGNETIC RESONANCE IMAGING; OVERALL SURVIVAL; PANCREATICODUODENECTOMY; PHASE 2 CLINICAL TRIAL (TOPIC); PHASE 3 CLINICAL TRIAL (TOPIC); PNEUMONIA; PRACTICE GUIDELINE; PROGRESSION FREE SURVIVAL; PROTEIN PROCESSING; RADIOFREQUENCY ABLATION; RANDOMIZED CONTROLLED TRIAL (TOPIC); RASH; RECURRENCE FREE SURVIVAL; SEROTONIN BLOOD LEVEL; SINGLE PHOTON EMISSION COMPUTER TOMOGRAPHY; SMALL INTESTINE OBSTRUCTION; SMALL INTESTINE RESECTION; SMALL INTESTINE TUMOR; STATISTICAL SIGNIFICANCE; SURVIVAL RATE; SYSTEMIC THERAPY; TREATMENT DURATION;

EID: 84876134206     PISSN: 15216918     EISSN: 15321916     Source Type: Journal    
DOI: 10.1016/j.bpg.2012.12.002     Document Type: Review

References (118)

1. F. Feyrter Über diffuse endocrine epitheliale Organe 1938 Barth Leipzig
2. I.M. Modlin, M.C. Champaneria, J. Bornschein, and M. Kidd Evolution of the diffuse neuroendocrine system-clear cells and cloudy origins Neuroendocrinology 84 2 2006 69 82
3. S. Oberndorfer Karzinoide Tumoren des Dünndarms Frankf Z Pathol 1 1907 425 429
4. E.D. Williams, and M. Sandler The classification of carcinoid tum ours Lancet 1 Feb 2 1963 238 239
5. M.A. Maggard, J.B. O'Connell, and C.Y. Ko Updated population-based review of carcinoid tumors Ann Surg 240 1 Jul 2004 117 122
6. J.C. Yao, M. Hassan, A. Phan, C. Dagohoy, C. Leary, and J.E. Mares 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 Jun 20 2008 3063 3072
7. S.K. Chuah, T.H. Hu, C.M. Kuo, K.W. Chiu, C.H. Kuo, and K.L. Wu Upper gastrointestinal carcinoid tumors incidentally found by endoscopic examinations World J Gastroenterol 11 44 Nov 28 2005 7028 7032
8. K. Hemminki, and X. Li Incidence trends and risk factors of carcinoid tumors: a nationwide epidemiologic study from Sweden Cancer 92 8 Oct 15 2001 2204 2210
9. I.M. Modlin, K.D. Lye, and M.A. Kidd 5-decade analysis of 13,715 carcinoid tumors Cancer 97 4 Feb 15 2003 934 959
10. C.G. Moertel Karnofsky memorial lecture. An odyssey in the land of small tumors J Clin Oncol 5 10 Oct 1987 1502 1522
11. C. Makridis, K. Oberg, C. Juhlin, J. Rastad, H. Johansson, and L.E. Lörelius Surgical treatment of mid-gut carcinoid tumors World J Surg 14 3 May-Jun 1990 377 383 [discussion 384-375]
12. C.G. Moertel, W.G. Sauer, M.B. Dockerty, and A.H. Baggenstoss Life history of the carcinoid tumor of the small intestine Cancer 14 Sep-Oct 1961 901 912
13. M.H. Kulke, and R.J. Mayer Carcinoid tumors N Engl J Med 340 11 Mar 18 1999 858 868
14. F.E. Eckhauser, L.C. Argenta, W.E. Strodel, R.H. Wheeler, F.E. Bull, and H.D. Appelman Mesenteric angiopathy, intestinal gangrene, and midgut carcinoids Surgery 90 4 Oct 1981 720 728
15. O. Rorstad Prognostic indicators for carcinoid neuroendocrine tumors of the gastrointestinal tract J Surg Oncol 89 3 Mar 1 2005 151 160
16. J. Strosberg, N. Gardner, and L. Kvols Survival and prognostic factor analysis of 146 metastatic neuroendocrine tumors of the mid-gut Neuroendocrinology 89 4 2009 471 476
17. J. Strosberg, A. Nasir, J. Cragun, N. Gardner, and L. Kvols Metastatic carcinoid tumor to the ovary: a clinicopathologic analysis of seventeen cases Gynecol Oncol 106 1 Jul 2007 65 68
18. A. Thorson, G. Biorck, G. Bjorkman, and J. Waldenstrom Malignant carcinoid of the small intestine with metastases to the liver, valvular disease of the right side of the heart (pulmonary stenosis and tricuspid regurgitation without septal defects), peripheral vasomotor symptoms, bronchoconstriction, and an unusual type of cyanosis; a clinical and pathologic syndrome Am Heart J 47 5 Jun 1954 795 817
19. W.B. Bean, D. Olch, and H.B. Weinberg The syndrome of carcinoid and acquired valve lesions of the right side of the heart Circulation 12 1 Jul 1955 1 6
20. F. Lembeck Detection of 5-hydroxytryptamine in carcinoid metastases Naunyn Schmiedebergs Arch Exp Pathol Pharmakol 221 1 1954 50 66
21. V. Erspamer, and B. Asero Identification of enteramine, the specific hormone of the enterochromaffin cell system, as 5-hydroxytryptamine Nature 169 4306 May 10 1952 800 801
22. A.I. Vinik, M.P. Silva, E.A. Woltering, V.L. Go, R. Warner, and M. Caplin Biochemical testing for neuroendocrine tumors Pancreas 38 8 Nov 2009 876 889
23. Z. Davis, C.G. Moertel, and D.C. McIlrath The malignant carcinoid syndrome Surg Gynecol Obstet 137 4 Oct 1973 637 644
24. M.R. von der Ohe, M. Camilleri, L.K. Kvols, and G.M. Thomforde Motor dysfunction of the small bowel and colon in patients with the carcinoid syndrome and diarrhea N Engl J Med 329 15 Oct 7 1993 1073 1078
25. J.M. Feldman Carcinoid tumors and syndrome Semin Oncol 14 3 Sep 1987 237 246
26. J.L. Cunningham, E.T. Janson, S. Agarwal, L. Grimelius, and M. Stridsberg Tachykinins in endocrine tumors and the carcinoid syndrome Eur J Endocrinol 159 3 Sep 2008 275 282
27. C. Matuchansky, and J.M. Launay Serotonin, catecholamines, and spontaneous midgut carcinoid flush: plasma studies from flushing and nonflushing sites Gastroenterology 108 3 Mar 1995 743 751
28. A.G. Smith, and M.W. Greaves Blood prostaglandin activity associated with noradrenaline-provoked flush in the carcinoid syndrome Br J Dermatol 90 5 May 1974 547 551
29. L.K. Kvols Metastatic carcinoid tumors and the malignant carcinoid syndrome Ann N Y Acad Sci 733 Sep 15 1994 464 470
30. M.E. Kahil, H. Brown, and H.L. Fred The carcinoid crisis Arch Intern Med 114 Jul 1964 26 28
31. L.K. Kvols, J.K. Martin, H.M. Marsh, and C.G. Moertel Rapid reversal of carcinoid crisis with a somatostatin analogue N Engl J Med 313 19 Nov 7 1985 1229 1230
32. P.A. Robiolio, V.H. Rigolin, J.S. Wilson, J.K. Harrison, L.L. Sanders, and T.M. Bashore Carcinoid heart disease. Correlation of high serotonin levels with valvular abnormalities detected by cardiac catheterization and echocardiography Circulation 92 4 Aug 15 1995 790 795
33. L. Lundin, I. Norheim, J. Landelius, K. Oberg, and E. Theodorsson-Norheim Carcinoid heart disease: relationship of circulating vasoactive substances to ultrasound-detectable cardiac abnormalities Circulation 77 2 Feb 1988 264 269
34. J.M. Zuetenhorst, J.M. Bonfrer, C.M. Korse, R. Bakker, H. van Tinteren, and B.G. Taal Carcinoid heart disease: the role of urinary 5-hydroxyindoleacetic acid excretion and plasma levels of atrial natriuretic peptide, transforming growth factor-beta and fibroblast growth factor Cancer 97 7 Apr 1 2003 1609 1615
35. H.M. Connolly, H.V. Schaff, C.J. Mullany, J. Rubin, M.D. Abel, and P.A. Pellikka Surgical management of left-sided carcinoid heart disease Circulation 104 12 Suppl. 1 Sep 18 2001 I36 I40
36. U.F. Pape, A. Perren, B. Niederle, D. Gross, T. Gress, and F. Costa ENETS Consensus Guidelines for the management of patients with neuroendocrine neoplasms from the jejuno-ileum and the appendix including goblet cell carcinomas Neuroendocrinology 95 2 2012 135 156
37. M.H. Kulke, A.B. Benson 3rd, E. Bergsland, J.D. Berlin, L.S. Blaszkowsky, and M.A. Choti Neuroendocrine tumors J Natl Compr Canc Netw 10 6 Jun 1 2012 724 764
38. J. Strosberg, A. Nasir, D. Coppola, M. Wick, and L. Kvols Correlation between grade and prognosis in metastatic gastroenteropancreatic neuroendocrine tumors Hum Pathol 40 9 Sep 2009 1262 1268
39. D.S. Klimstra, I.R. Modlin, D. Coppola, R.V. Lloyd, and S. Suster The pathologic classification of neuroendocrine tumors: a review of nomenclature, grading, and staging systems Pancreas 39 6 2010 Aug 707 712
40. J.R. Strosberg, J.M. Weber, M. Feldman, D. Coppola, K. Meredith, and L.K. Kvols Prognostic validity of the American Joint Committee on Cancer (AJCC) staging classification for midgut neuroendocrine tumros J Clin Oncol 31 4 2013 Feb 420 425
41. G. Rindi, G. Klöppel, A. Couvelard, P. Komminoth, M. Körner, and J.M. Lopes TNM staging of midgut and hindgut (neuro) endocrine tumors: a consensus proposal including a grading system Virchows Arch 451 4 Oct 2007 757 762
42. AJCC cancer staging manual 7th ed. 2010 Springer Chicago
43. H. Jann, S. Roll, A. Couvelard, O. Hentic, M. Pavel, and J. Müller-Nordhorn Neuroendocrine tumors of midgut and hindgut origin: tumor-node-metastasis classification determines clinical outcome Cancer 117 15 Aug 1 2011 3332 3341
44. L.K. Kvols The carcinoid syndrome: a treatable malignant disease Oncology (Huntingt) 2 2 Feb 1988 33 41
45. V.T. Caldarola, R.J. Jackman, C.G. Moertel, and M.B. Dockerty Carcinoid tumors of the rectum Am J Surg 107 Jun 1964 844 849
46. K.R. Allen, T.J. Degg, D.A. Anthoney, and D. Fitzroy-Smith Monitoring the treatment of carcinoid disease using blood serotonin and plasma 5-hydroxyindoleacetic acid: three case examples Ann Clin Biochem 44 Pt 3 May 2007 300 307
47. R.S. Carling, T.J. Degg, K.R. Allen, N.D. Bax, and J.H. Barth Evaluation of whole blood serotonin and plasma and urine 5-hydroxyindole acetic acid in diagnosis of carcinoid disease Ann Clin Biochem 39 Pt 6 Nov 2002 577 582
48. D. Campana, F. Nori, L. Piscitelli, A.M. Morselli-Labate, R. Pezzilli, and R. Corinaldesi Chromogranin A: is it a useful marker of neuroendocrine tumors? J Clin Oncol 25 15 May 20 2007 1967 1973
49. J.M. Conlon Granin-derived peptides as diagnostic and prognostic markers for endocrine tumors Regul Pept 165 1 Nov 30 2010 5 11
50. S. Sanduleanu, A. De Bruïne, M. Stridsberg, D. Jonkers, I. Biemond, and W. Hameeteman Serum chromogranin A as a screening test for gastric enterochromaffin-like cell hyperplasia during acid-suppressive therapy Eur J Clin Invest 31 9 Sep 2001 802 811
51. E.H. Jensen, L. Kvols, J.M. McLoughlin, J.M. Lewis, M.D. Alvarado, and T. Yeatman Biomarkers predict outcomes following cytoreductive surgery for hepatic metastases from functional carcinoid tumors Ann Surg Oncol 14 2 Feb 2007 780 785
52. J.C. Yao, M. Pavel, A.T. Phan, M.H. Kulke, S. Hoosen, and J. St Peter Chromogranin A and neuron-specific enolase as prognostic markers in patients with advanced pNET treated with everolimus J Clin Endocrinol Metab 96 12 Dec 2011 3741 3749
53. E. Bajetta, L. Ferrari, A. Martinetti, L. Celio, G. Procopio, and S. Artale Chromogranin A, neuron specific enolase, carcinoembryonic antigen, and hydroxyindole acetic acid evaluation in patients with neuroendocrine tumors Cancer 86 5 Sep 1 1999 858 865
54. T. Ito, H. Igarashi, and R.T. Jensen Serum pancreastatin: the long sought universal, sensitive, specific tumor marker for neuroendocrine tumors? Pancreas 41 4 May 2012 505 507
55. E.K. Paulson, V.G. McDermott, M.T. Keogan, D.M. DeLong, M.G. Frederick, and R.C. Nelson Carcinoid metastases to the liver: role of triple-phase helical CT Radiology 206 1 Jan 1998 143 150
56. F.A. Hakim, J.A. Alexander, J.E. Huprich, M. Grover, and F.T. Enders CT-enterography may identify small bowel tumors not detected by capsule endoscopy: eight years experience at Mayo clinic Rochester Dig Dis Sci 56 10 Oct 2011 2914 2919
57. C. Dromain, T. de Baere, J. Lumbroso, H. Caillet, A. Laplanche, and V. Boige Detection of liver metastases from endocrine tumors: a prospective comparison of somatostatin receptor scintigraphy, computed tomography, and magnetic resonance imaging J Clin Oncol 23 1 Jan 1 2005 70 78
58. C. Dromain, T. de Baere, E. Baudin, J. Galline, M. Ducreux, and V. Boige MR imaging of hepatic metastases caused by neuroendocrine tumors: comparing four techniques AJR Am J Roentgenol 180 1 Jan 2003 121 128
59. Y.K. Kim, M.W. Lee, W.J. Lee, S.H. Kim, H. Rhim, and J.H. Lim Diagnostic accuracy and sensitivity of diffusion-weighted and of gadoxetic acid-enhanced 3-T MR imaging alone or in combination in the detection of small liver metastasis (
60. E.P. Krenning, W.H. Bakker, P.P. Kooij, W.A. Breeman, H.Y. Oei, and M. de Jong Somatostatin receptor scintigraphy with indium-111-DTPA-D-Phe-1-octreotide in man: metabolism, dosimetry and comparison with iodine-123-Tyr-3-octreotide J Nucl Med 33 5 May 1992 652 658
61. Y. Krausz, Z. Keidar, I. Kogan, E. Even-Sapir, R. Bar-Shalom, and A. Engel SPECT/CT hybrid imaging with 111In-pentetreotide in assessment of neuroendocrine tumours Clin Endocrinol (Oxf) 59 5 Nov 2003 565 573
62. D.L. Reidy-Lagunes, M.J. Gollub, and L.B. Saltz Addition of octreotide functional imaging to cross-sectional computed tomography or magnetic resonance imaging for the detection of neuroendocrine tumors: added value or an anachronism? J Clin Oncol 29 3 Jan 20 2011 e74 e75
63. I. Buchmann, M. Henze, S. Engelbrecht, M. Eisenhut, A. Runz, and M. Schäfer Comparison of 68Ga-DOTATOC PET and 111In-DTPAOC (Octreoscan) SPECT in patients with neuroendocrine tumours Eur J Nucl Med Mol Imaging 34 10 Oct 2007 1617 1626
64. K.P. Koopmans, O.C. Neels, I.P. Kema, P.H. Elsinga, W.J. Sluiter, and K. Vanghillewe Improved staging of patients with carcinoid and islet cell tumors with 18F-dihydroxy-phenyl-alanine and 11C-5-hydroxy-tryptophan positron emission tomography J Clin Oncol 26 9 Mar 20 2008 1489 1495
65. B. Givi, S.J. Pommier, A.K. Thompson, B.S. Diggs, and R.F. Pommier Operative resection of primary carcinoid neoplasms in patients with liver metastases yields significantly better survival Surgery 140 6 Dec 2006 891 897 [discussion 897-898]
66. M. Jayant, R. Punia, R. Kaushik, R. Sharma, A. Sachdev, and N.K. Nadkarni Neuroendocrine tumors of the ampulla of vater: presentation, pathology and prognosis JOP 13 3 May 2012 263 267
67. S. Reichlin Somatostatin N Engl J Med 309 24 Dec 15 1983 1495 1501
68. R. Maurer, and J.C. Reubi Somatostatin receptors JAMA 253 18 May 10 1985 2741
69. S.W. Lamberts, A.J. van der Lely, W.W. de Herder, and L.J. Hofland Octreotide N Engl J Med 334 4 Jan 25 1996 246 254
70. L.K. Kvols, C.G. Moertel, M.J. O'Connell, A.J. Schutt, J. Rubin, and R.G. Hahn Treatment of the malignant carcinoid syndrome. Evaluation of a long-acting somatostatin analogue N Engl J Med 315 11 Sep 11 1986 663 666
71. D. O'Toole, M. Ducreux, G. Bommelaer, J.L. Wemeau, O. Bouché, and F. Catus Treatment of carcinoid syndrome: a prospective crossover evaluation of lanreotide versus octreotide in terms of efficacy, patient acceptability, and tolerance Cancer 88 4 Feb 15 2000 770 776
72. M. di Bartolomeo, E. Bajetta, R. Buzzoni, L. Mariani, C. Carnaghi, and L. Somma Clinical efficacy of octreotide in the treatment of metastatic neuroendocrine tumors. A study by the Italian Trials in Medical Oncology Group Cancer 77 2 Jan 15 1996 402 408
73. J. Rubin, J. Ajani, W. Schirmer, A.P. Venook, R. Bukowski, and R. Pommier Octreotide acetate long-acting formulation versus open-label subcutaneous octreotide acetate in malignant carcinoid syndrome J Clin Oncol 17 2 Feb 1999 600 606
74. P. Ruszniewski, M. Ducreux, J.A. Chayvialle, J. Blumberg, D. Cloarec, and H. Michel Treatment of the carcinoid syndrome with the longacting somatostatin analogue lanreotide: a prospective study in 39 patients Gut 39 2 Aug 1996 279 283
75. M.H. Kulke, L.B. Anthony, D.L. Bushnell, W.W. de Herder, S.J. Goldsmith, and D.S. Klimstra NANETS treatment guidelines: well-differentiated neuroendocrine tumors of the stomach and pancreas Pancreas 39 6 2010 Aug 735 752
76. K. Oberg, L. Kvols, M. Caplin, G. Delle Fave, W. de Herder, and G. Rindi Consensus report on the use of somatostatin analogs for the management of neuroendocrine tumors of the gastroenteropancreatic system Ann Oncol 15 6 Jun 2004 966 973
77. J. Strosberg, and L. Kvols Antiproliferative effect of somatostatin analogs in gastroenteropancreatic neuroendocrine tumors World J Gastroenterol 16 24 Jun 28 2010 2963 2970
78. G. Weckbecker, I. Lewis, R. Albert, H.A. Schmid, D. Hoyer, and C. Bruns Opportunities in somatostatin research: biological, chemical and therapeutic aspects Nat Rev Drug Discov 2 12 Dec 2003 999 1017
79. E.A. Woltering, J.C. Watson, R.C. Alperin-Lea, C. Sharma, E. Keenan, and D. Kurozawa Somatostatin analogs: angiogenesis inhibitors with novel mechanisms of action Invest New Drugs 15 1 1997 77 86
80. O. Serri, P. Brazeau, Z. Kachra, and B. Posner Octreotide inhibits insulin-like growth factor-I hepatic gene expression in the hypophysectomized rat: evidence for a direct and indirect mechanism of action Endocrinology 130 4 Apr 1992 1816 1821
81. A. Rinke, H.H. Müller, C. Schade-Brittinger, K.J. Klose, P. Barth, and M. Wied 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 Oct 1 2009 4656 4663
82. K.M. Detjen, M. Welzel, K. Farwig, F.H. Brembeck, A. Kaiser, and E.O. Riecken Molecular mechanism of interferon alfa-mediated growth inhibition in human neuroendocrine tumor cells Gastroenterology 118 4 Apr 2000 735 748
83. K. Oberg, K. Funa, and G. Alm Effects of leukocyte interferon on clinical symptoms and hormone levels in patients with mid-gut carcinoid tumors and carcinoid syndrome N Engl J Med 309 3 Jul 21 1983 129 133
84. E.T. Janson, and K. Oberg Long-term management of the carcinoid syndrome. Treatment with octreotide alone and in combination with alpha-interferon Acta Oncol 32 2 1993 225 229
85. L. Kolby, G. Persson, S. Franzen, and B. Ahren Randomized clinical trial of the effect of interferon alpha on survival in patients with disseminated midgut carcinoid tumours Br J Surg 90 6 Jun 2003 687 693
86. S. Faiss, U.F. Pape, M. Böhmig, Y. Dörffel, U. Mansmann, and W. Golder 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 21 14 Jul 15 2003 2689 2696
87. R. Arnold, A. Rinke, K.J. Klose, H.H. Müller, M. Wied, and K. Zamzow Octreotide versus octreotide plus interferon-alpha in endocrine gastroenteropancreatic tumors: a randomized trial Clin Gastroenterol Hepatol 3 8 Aug 2005 761 771
88. S. Vignot, S. Faivre, D. Aguirre, and E. Raymond mTOR-targeted therapy of cancer with rapamycin derivatives Ann Oncol 16 4 Apr 2005 525 537
89. Y. Jiao, C. Shi, B.H. Edil, R.F. de Wilde, D.S. Klimstra, and A. Maitra DAXX/ATRX, MEN1, and mTOR pathway genes are frequently altered in pancreatic neuroendocrine tumors Science 331 6021 Mar 4 2011 1199 1203
90. M.E. Pavel, J.D. Hainsworth, E. Baudin, M. Peeters, D. Hörsch, and R.E. Winkler 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 378 9808 Dec 10 2011 2005 2012
91. B. Terris, J.Y. Scoazec, L. Rubbia, L. Bregeaud, M.S. Pepper, and P. Ruszniewski Expression of vascular endothelial growth factor in digestive neuroendocrine tumours Histopathology 32 2 Feb 1998 133 138
92. J.C. Yao, A. Phan, P.M. Hoff, H.X. Chen, C. Charnsangavej, and S.C. Yeung 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 26 8 Mar 10 2008 1316 1323
93. M.H. Kulke, H.J. Lenz, N.J. Meropol, J. Posey, D.P. Ryan, and J. Picus Activity of sunitinib in patients with advanced neuroendocrine tumors J Clin Oncol 26 20 Jul 10 2008 3403 3410
94. A.T. Phan, J.C. Yao, D.R. Fogelman, K.R. Hess, C.S. Ng, and S.A. Bullock A prospective, multi-institutional phase II study of GW786034 (pazopanib) and depot octreotide in advanced low-grade neuroendocrine carcinoma J Clin Oncol 28 15s 2010 [suppl; abstr 4001]
95. M.H. Kulke, K. Stuart, P.C. Enzinger, D.P. Ryan, J.W. Clark, and A. Muzikansky Phase II study of temozolomide and thalidomide in patients with metastatic neuroendocrine tumors J Clin Oncol 24 3 Jan 20 2006 401 406
96. J.A. Chan, K. Stuart, C.C. Earle, J.W. Clark, P. Bhargava, and R. Miksad Prospective study of bevacizumab plus temozolomide in patients with advanced neuroendocrine tumors J Clin Oncol 30 24 Aug 20 2012 2963 2968
97. M.H. Kulke, J.L. Hornick, C. Frauenhoffer, S. Hooshmand, D.P. Ryan, and P.C. Enzinger O6-methylguanine DNA methyltransferase deficiency and response to temozolomide-based therapy in patients with neuroendocrine tumors Clin Cancer Res 15 1 Jan 1 2009 338 345
98. D.J. Kwekkeboom, J. Mueller-Brand, G. Paganelli, L.B. Anthony, S. Pauwels, and L.K. Kvols Overview of results of peptide receptor radionuclide therapy with 3 radiolabeled somatostatin analogs J Nucl Med 46 Suppl. 1 Jan 2005 62S 66S
99. R. Valkema, M. De Jong, W.H. Bakker, W.A. Breeman, P.P. Kooij, and P.J. Lugtenburg Phase I study of peptide receptor radionuclide therapy with [In-DTPA]octreotide: the Rotterdam experience Semin Nucl Med 32 2 Apr 2002 110 122
100. 90Y-DOTA0, Tyr3]octreotide in patients with advanced gastroenteropancreatic neuroendocrine tumors Semin Nucl Med 36 2 Apr 2006 147 156
101. 90Y-edotreotide for metastatic carcinoid refractory to octreotide J Clin Oncol 28 10 Apr 1 2010 1652 1659
102. 177Lu-DOTA 0, Tyr3]octreotate: toxicity, efficacy, and survival J Clin Oncol 26 13 May 1 2008 2124 2130
103. J.M. Sarmiento, G. Heywood, J. Rubin, D.M. Ilstrup, D.M. Nagorney, and F.G. Que Surgical treatment of neuroendocrine metastases to the liver: a plea for resection to increase survival J Am Coll Surg 197 1 Jul 2003 29 37
104. J.A. Norton, R.S. Warren, M.G. Kelly, M.B. Zuraek, and R.T. Jensen Aggressive surgery for metastatic liver neuroendocrine tumors Surgery 134 6 Dec 2003 1057 1063 [discussion 1063-1055]
105. A.R. Henn, E.A. Levine, W. McNulty, and R.J. Zagoria Percutaneous radiofrequency ablation of hepatic metastases for symptomatic relief of neuroendocrine syndromes AJR Am J Roentgenol 181 4 Oct 2003 1005 1010
106. G.P. McEntee, D.M. Nagorney, L.K. Kvols, C.G. Moertel, and C.S. Grant Cytoreductive hepatic surgery for neuroendocrine tumors Surgery 108 6 Dec 1990 1091 1096
107. F.G. Que, D.M. Nagorney, K.P. Batts, L.J. Linz, and L.K. Kvols Hepatic resection for metastatic neuroendocrine carcinomas Am J Surg 169 1 Jan 1995 36 42 [discussion 42-33]
108. P. Ruszniewski, P. Rougier, A. Roche, P. Legmann, A. Sibert, and S. Hochlaf Hepatic arterial chemoembolization in patients with liver metastases of endocrine tumors. A prospective phase II study in 24 patients Cancer 71 8 Apr 15 1993 2624 2630
109. B.K. Eriksson, E.G. Larsson, B.M. Skogseid, A.M. Lofberg, L.E. Lorelius, and K.E. Oberg Liver embolizations of patients with malignant neuroendocrine gastrointestinal tumors Cancer 83 11 Dec 1 1998 2293 2301
110. S. Gupta, J.C. Yao, K. Ahrar, M.J. Wallace, F.A. Morello, and D.C. Madoff Hepatic artery embolization and chemoembolization for treatment of patients with metastatic carcinoid tumors: the M.D. Anderson experience Cancer J 9 4 Jul-Aug 2003 261 267
111. J.R. Strosberg, J. Choi, A.B. Cantor, and L.K. Kvols Selective hepatic artery embolization for treatment of patients with metastatic carcinoid and pancreatic endocrine tumors Cancer Control 13 1 Jan 2006 72 78
112. C. Loewe, M. Schindl, M. Cejna, B. Niederle, J. Lammer, and S. Thurnher Permanent transarterial embolization of neuroendocrine metastases of the liver using cyanoacrylate and lipiodol: assessment of mid- and long-term results AJR Am J Roentgenol 180 5 May 2003 1379 1384
113. E. Therasse, F. Breittmayer, A. Roche, T. De Baere, S. Indushekar, and M. Ducreux Transcatheter chemoembolization of progressive carcinoid liver metastasis Radiology 189 2 Nov 1993 541 547
114. J.R. Strosberg, J.M. Weber, J. Choi, T.L. Campos, T.L. Valone, and G. Han A phase II clinical trial of sunitinib following hepatic transarterial embolization for metastatic neuroendocrine tumors Ann Oncol 23 9 Sep 2012 2335 2341
115. 90Y-microspheres: early results in 148 patients Am J Clin Oncol 31 3 Jun 2008 271 279
116. 90Y Radioembolization for metastatic neuroendocrine liver tumors: preliminary results from a multi-institutional experience Ann Surg 247 6 Jun 2008 1029 1035
117. T. Lehnert Liver transplantation for metastatic neuroendocrine carcinoma: an analysis of 103 patients Transplantation 66 10 Nov 27 1998 1307 1312
118. Y.P. Le Treut, E. Grégoire, J. Belghiti, O. Boillot, O. Soubrane, and G. Mantion Predictors of long-term survival after liver transplantation for metastatic endocrine tumors: an 85-case French multicentric report Am J Transpl 8 6 Jun 2008 1205 1213