Recommendations for management of patients with neuroendocrine liver metastases

The Lancet Oncology

Volumn 15, Issue 1, 2014, Pages

  Frilling, Andrea ^a   Modlin, Irvin M ^b   Kidd, Mark ^b   Russell, Christopher ^c   Breitenstein, Stefan ^d   Salem, Riad ^e   Kwekkeboom, Dik ^f   Lau, Wan yee ^g   Klersy, Catherine ^h   Vilgrain, Valerie ⁱ   Davidson, Brian ^c   Siegler, Mark ^j   Caplin, Martyn ^c,k   Solcia, Enrico ^h   Schilsky, Richard ^l  

^a IMPERIAL COLLEGE LONDON   (United Kingdom)

^b YALE UNIVERSITY   (United States)

^c UNIVERSITY COLLEGE LONDON   (United Kingdom)

^d UNIVERSITY HOSPITAL ZURICH   (Switzerland)

^e NORTHWESTERN UNIVERSITY   (United States)

^f ERASMUS MEDICAL CENTER   (Netherlands)

^g CHINESE UNIVERSITY OF HONG KONG   (Hong Kong)

^h FONDAZIONE IRCCS POLICLINICO SAN MATTEO   (Italy)

ⁱ BEAUJON HOSPITAL   (France)

^j UNIVERSITY OF CHICAGO   (United States)

^k ROYAL FREE HOSPITAL   (United Kingdom)

^l AMERICAN SOCIETY OF CLINICAL ONCOLOGY   (United States)

more..

Author keywords

[No Author keywords available]

Indexed keywords

CHROMOGRANIN A; COPPER 64; DOXORUBICIN; EVEROLIMUS; FLUORODEOXYGLUCOSE F 18; FLUOROURACIL; GADOTERIC ACID; GALLIUM 68; KI 67 ANTIGEN; LUTETIUM 177; SOMATOSTATIN RECEPTOR; STREPTOZOCIN; SUNITINIB;

CANCER DIAGNOSIS; CANCER INCIDENCE; CANCER LOCALIZATION; CANCER REGISTRY; CANCER SURVIVAL; CHEMOEMBOLIZATION; CIRCULATING TUMOR CELL; CLINICAL RESEARCH; COMPUTER ASSISTED TOMOGRAPHY; CONTRAST ENHANCEMENT; ECHOGRAPHY; ENTEROCHROMAFFIN CELL; EVIDENCE BASED PRACTICE; FATIGUE; GASTRITIS; GASTROENTEROPANCREATIC NEUROENDOCRINE TUMOR; HUMAN; LIVER BIOPSY; LIVER LOBECTOMY; LIVER METASTASIS; LIVER SURGERY; LIVER TRANSPLANTATION; MEDICAL SOCIETY; MICROWAVE THERAPY; NAUSEA; NEUROENDOCRINE TUMOR; NUCLEAR MAGNETIC RESONANCE IMAGING; OVERALL SURVIVAL; PREVALENCE; PRIORITY JOURNAL; PROGNOSIS; PROTEIN EXPRESSION; REVIEW; SCINTISCANNING; SENSITIVITY AND SPECIFICITY; SURVIVAL TIME; TREATMENT RESPONSE; TUMOR VOLUME;

EID: 84891369262     PISSN: 14702045     EISSN: 14745488     Source Type: Journal    
DOI: 10.1016/S1470-2045(13)70362-0     Document Type: Review

References (85)

1. Lawrence B, Gustafsson BI, Chan A, Svejda B, Kidd M, Modlin IM The epidemiology of gastroenteropancreatic neuroendocrine tumors. Endocrinol Metab Clin North Am 2011, 40:1-18.
2. Modlin IM, Oberg K, Chung DC, et al. Gastroenteropancreatic neuroendocrine tumours. Lancet Oncol 2008, 9:61-72.
3. Saxena A, Chua TC, Sarkar A, et al. Progression and survival results after radical hepatic metastasectomy of indolent advanced neuroendocrine neoplasms (NENs) supports an aggressive surgical approach. Surgery 2011, 149:209-220.
4. Pape UF, Berndt U, Muller-Nordhorn J, et al. Prognostic factors of long-term outcome in gastroenteropancreatic neuroendocrine tumours. Endocr Relat Cancer 2008, 15:1083-1097.
5. McDermott EW, Guduric B, Brennan MF Prognostic variables in patients with gastrointestinal carcinoid tumours. Br J Surg 1994, 81:1007-1009.
6. Rindi G, D'Adda T, Froio E, Fellegara G, Bordi C Prognostic factors in gastrointestinal endocrine tumors. Endocr Pathol 2007, 18:145-149.
7. Pavel M, Baudin E, Couvelard A, et al. ENETS Consensus Guidelines for the management of patients with liver and other distant metastases from neuroendocrine neoplasms of foregut, midgut, hindgut, and unknown primary. Neuroendocrinology 2012, 95:157-176.
8. Grundahl J The Danish consensus conference model. Public participation in science: the role of consensus conferences in Europe 1995, 31-41. Science Museum, London. S. Joss, J. Durant (Eds.).
9. Guyatt G, Oxman AD, Akl EA, et al. GRADE guidelines: 1. Introduction-GRADE evidence profiles and summary of findings tables. J Clin Epidemiol 2011, 64:383-394.
10. Yao JC, Hassan M, Phan A, et al. One hundred years after "carcinoid": epidemiology of and prognostic factors for neuroendocrine tumors in 35825 cases in the United States. J Clin Oncol 2008, 26:3063-3072.
11. Lepage C, Ciccolallo L, De Angelis R, Bouvier AM, Faivre J, Gatta G European disparities in malignant digestive endocrine tumours survival. Int J Cancer 2010, 126:2928-2934.
12. Guyatt GH, Oxman AD, Kunz R, et al. Going from evidence to recommendations. BMJ 2008, 336:1049-1051.
13. Jamali M, Chetty R Predicting prognosis in gastroentero-pancreatic neuroendocrine tumors: an overview and the value of Ki-67 immunostaining. Endocr Pathol 2008, 19:282-288.
14. Jann H, Roll S, Couvelard A, et al. Neuroendocrine tumors of midgut and hindgut origin: tumor-node-metastasis classification determines clinical outcome. Cancer 2011, 117:3332-3341.
15. Norlen O, Stalberg P, Oberg K, et al. Long-term results of surgery for small intestinal neuroendocrine tumors at a tertiary referral center. World J Surg 2012, 36:1419-1431.
16. Landerholm K, Zar N, Andersson RE, Falkmer SE, Jarhult J Survival and prognostic factors in patients with small bowel carcinoid tumour. Br J Surg 2011, 98:1617-1624.
17. 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 2007, 451:757-762.
18. Modlin I, Drozdov I, Kidd M The identification of gut neuroendocrine tumor disease by multiple synchronous transcript analysis in blood. PLoS One 2013, 8:e63364.
19. Kidd M, Modlin IM, Mane SM, Camp RL, Eick G, Latich I The role of genetic markers-NAP1L1, MAGE-D2, and MTA1 in defining small-intestinal carcinoid neoplasia. Ann Surg Oncol 2006, 13:253-262.
20. Leja J, Essaghir A, Essand M, et al. Novel markers for enterochromaffin cells and gastrointestinal neuroendocrine carcinomas. Mod Pathol 2009, 22:261-272.
21. Edfeldt K, Bjorklund P, Akerstrom G, Westin G, Hellman P, Stalberg P Different gene expression profiles in metastasizing midgut carcinoid tumors. Endocr Relat Cancer 2011, 18:479-489.
22. Posorski N, Kaemmerer D, Ernst G, et al. Localization of sporadic neuroendocrine tumors by gene expression analysis of their metastases. Clin Exp Metastasis 2011, 28:637-647.
23. Matsuoka S, Huang M, Elledge S Linkage of ATM to cell cycle regulation by the Chk2 protein kinase. Science 1998, 282:1893-1897.
24. Lee J, Sung CO, Lee EJ, et al. Metastasis of neuroendocrine tumors are characterized by increased cell proliferation and reduced expression of the ATM gene. PLoS One 2012, 7:e34456.
25. Ruebel K, Leontovich AA, Stilling GA, et al. MicroRNA expression in ileal carcinoid tumors: downregulation of microRNA-133a with tumor progression. Mod Pathol 2010, 23:367-375.
26. Modlin IM, Gustafsson BI, Drozdov I, Nadler B, Pfragner R, Kidd M Principal component analysis, hierarchical clustering, and decision tree assessment of plasma mRNA and hormone levels as an early detection strategy for small intestinal neuroendocrine (carcinoid) tumors. Ann Surg Oncol 2009, 16:487-498.
27. Couce ME, Bautista D, Costa J, Carter D Analysis of K-ras, N-ras, H-ras, and p53 in lung neuroendocrine neoplasms. Diagn Mol Pathol 1999, 8:71-79.
28. Kidd M, Schimmack S, Lawrence B, Alaimo D, Modlin IM EGFR/TGFalpha and TGFbeta/CTGF signaling in neuroendocrine neoplasia: theoretical therapeutic targets. Neuroendocrinology 2013, 97:35-44.
29. 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.
30. Khan MS, Kirkwood A, Tsigani T, et al. Circulating tumor cells as prognostic markers in neuroendocrine tumors. J Clin Oncol 2013, 31:365-372.
31. 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.
32. Olausson M, Friman S, Herlenius G, et al. Orthotopic liver or multivisceral transplantation as treatment of metastatic neuroendocrine tumors. Liver Transpl 2007, 13:327-333.
33. Jensen EH, Kvols L, McLoughlin JM, et al. Biomarkers predict outcomes following cytoreductive surgery for hepatic metastases from functional carcinoid tumors. Ann Surg Oncol 2007, 14:780-785.
34. Modlin IM, Gustafsson BI, Moss SF, Pavel M, Tsolakis AV, Kidd M Chromogranin A-biological function and clinical utility in neuro endocrine tumor disease. Ann Surg Oncol 2010, 17:2427-2443.
35. Rickes S, Ocran KW, Gerstenhauer G, Neye H, Wermke W Evaluation of diagnostic criteria for liver metastases of adenocarcinomas and neuroendocrine tumours at conventional ultrasound, unenhanced power Doppler sonography and echo-enhanced ultrasound. Dig Dis 2004, 22:81-86.
36. Jung EM, Ross CJ, Rennert J, et al. Characterization of microvascularization of liver tumor lesions with high resolution linear ultrasound and contrast enhanced ultrasound (CEUS) during surgery: first results. Clin Hemorheol Microcirc 2010, 46:89-99.
37. d'Assignies G, Fina P, Bruno O, et al. High sensitivity of diffusion-weighted MR imaging for the detection of liver metastases from neuroendocrine tumors: comparison with T2-weighted and dynamic gadolinium-enhanced MR imaging. Radiology 2013, 268:390-399.
38. Elias D, Lefevre JH, Duvillard P, et al. Hepatic metastases from neuroendocrine tumors with a "thin slice" pathological examination: they are many more than you think. Ann Surg 2010, 251:307-310.
39. Frilling A, Sotiropoulos GC, Radtke A, et al. The impact of 68Ga-DOTATOC positron emission tomography/computed tomography on the multimodal management of patients with neuroendocrine tumors. Ann Surg 2010, 252:850-856.
40. Ruf J, Heuck F, Schiefer J, et al. Impact of multiphase 68Ga-DOTATOC-PET/CT on therapy management in patients with neuroendocrine tumors. Neuroendocrinology 2010, 91:101-109.
41. Schreiter NF, Brenner W, Nogami M, et al. Cost comparison of 111In-DTPA-octreotide scintigraphy and 68Ga-DOTATOC PET/CT for staging enteropancreatic neuroendocrine tumours. Eur J Nucl Med Mol Imaging 2012, 39:72-82.
42. Pfeifer A, Knigge U, Mortensen J, et al. Clinical PET of neuroendocrine tumors using 64Cu-DOTATATE: first-in-humans study. J Nucl Med 2012, 53:1207-1215.
43. Binderup T, Knigge U, Loft A, et al. Functional imaging of neuroendocrine tumors: a head-to-head comparison of somatostatin receptor scintigraphy, 123I-MIBG scintigraphy, and 18F-FDG PET. J Nucl Med 2010, 51:704-712.
44. Bodei L, Kidd M, Modlin I, Paganelli G Nuclear medicine in the diagnosis and therapy of neuroendocrine tumors. Nuclear oncology 2013, Wolters Kluwer Health. C. Akotlun, S. Goldsmith (Eds.).
45. John BJ, Davidson BR Treatment options for unresectable neuroendocrine liver metastases. Expert Rev Gastroenterol Hepatol 2012, 6:357-369.
46. Kulke MH, Benson AB, Bergsland E, et al. Neuroendocrine tumors. J Natl Compr Canc Netw 2012, 10:724-764.
47. Oberg K, Knigge U, Kwekkeboom D, Perren A Neuroendocrine gastro-entero-pancreatic tumors: ESMO Clinical Practice Guidelines for diagnosis, treatment and follow-up. Ann Oncol 2012, 23(suppl 7):vii124-vii130.
48. Dhall D, Mertens R, Bresee C, et al. Ki-67 proliferative index predicts progression-free survival of patients with well-differentiated ileal neuroendocrine tumors. Hum Pathol 2012, 43:489-495.
49. Yang Z, Tang LH, Klimstra DS Effect of tumor heterogeneity on the assessment of Ki-67 labeling index in well-differentiated neuroendocrine tumors metastatic to the liver: implications for prognostic stratification. Am J Surg Pathol 2011, 35:853-860.
50. Dhall D, Mertens R, Bresee C, et al. Ki-67 proliferative index predicts progression-free survival of patients with well-differentiated ileal neuroendocrine tumors. Hum Pathol 2012, 43:489-495.
51. Sarmiento JM, Heywood G, Rubin J, Ilstrup DM, Nagorney DM, Que FG Surgical treatment of neuroendocrine metastases to the liver: a plea for resection to increase survival. J Am Coll Surg 2003, 197:29-37.
52. Elias D, Lasser P, Ducreux M, et al. Liver resection (and associated extrahepatic resections) for metastatic well-differentiated endocrine tumors: a 15-year single center prospective study. Surgery 2003, 133:375-382.
53. Glazer ES, Tseng JF, Al-Refaie W, et al. Long-term survival after surgical management of neuroendocrine hepatic metastases. HPB (Oxford) 2010, 12:427-433.
54. Mayo SC, de Jong MC, Pulitano C, et al. Surgical management of hepatic neuroendocrine tumor metastasis: results from an international multi-institutional analysis. Ann Surg Oncol 2010, 17:3129-3136.
55. Frilling A, Li J, Malamutmann E, Schmid KW, Bockisch A, Broelsch CE Treatment of liver metastases from neuroendocrine tumours in relation to the extent of hepatic disease. Br J Surg 2009, 96:175-184.
56. Demirkan BH, Eriksson B Systemic treatment of neuroendocrine tumors with hepatic metastases. Turk J Gastroenterol 2012, 23:427-437.
57. Capurso G, Rinzivillo M, Bettini R, Boninsegna L, Delle Fave G, Falconi M Systematic review of resection of primary midgut carcinoid tumour in patients with unresectable liver metastases. Br J Surg 2012, 99:1480-1486.
58. Gedaly R, Daily MF, Davenport D, et al. Liver transplantation for the treatment of liver metastases from neuroendocrine tumors: an analysis of the UNOS database. Arch Surg 2011, 146:953-958.
59. Maire F, Hammel P, Kianmanesh R, et al. Is adjuvant therapy with streptozotocin and 5-fluorouracil useful after resection of liver metastases from digestive endocrine tumors?. Surgery 2009, 145:69-75.
60. Sowa-Staszczak A, Pach D, Chrzan R, et al. Peptide receptor radionuclide therapy as a potential tool for neoadjuvant therapy in patients with inoperable neuroendocrine tumours (NETs). Eur J Nucl Med Mol Imaging 2011, 38:1669-1674.
61. Stoeltzing O, Loss M, Huber E, et al. Staged surgery with neoadjuvant 90Y-DOTATOC therapy for down-sizing synchronous bilobular hepatic metastases from a neuroendocrine pancreatic tumor. Langenbecks Arch Surg 2010, 395:185-192.
62. Kaemmerer D, Prasad V, Daffner W, et al. Neoadjuvant peptide receptor radionuclide therapy for an inoperable neuroendocrine pancreatic tumor. World J Gastroenterol 2009, 15:5867-5870.
63. Vogl TJ, Naguib NN, Zangos S, Eichler K, Hedayati A, Nour-Eldin NE Liver metastases of neuroendocrine carcinomas: interventional treatment via transarterial embolization, chemoembolization and thermal ablation. Eur J Radiol 2009, 72:517-528.
64. Gillams A, Cassoni A, Conway G, Lees W Radiofrequency ablation of neuroendocrine liver metastases: the Middlesex experience. Abdom Imaging 2005, 30:435-441.
65. Elias D, Goere D, Leroux G, et al. Combined liver surgery and RFA for patients with gastroenteropancreatic endocrine tumors presenting with more than 15 metastases to the liver. Eur J Surg Oncol 2009, 35:1092-1097.
66. Pitt SC, Knuth J, Keily JM, et al. Hepatic neuroendocrine metastases: chemo- or bland embolization?. J Gastrointest Surg 2008, 12:1951-1960.
67. Memon K, Lewandowski RJ, Riaz A, Salem R Chemoembolization and radioembolization for metastatic disease to the liver: available data and future studies. Curr Treat Options Oncol 2012, 13:403-415.
68. McStay MK, Maudgil D, Williams M, et al. Large-volume liver metastases from neuroendocrine tumors: hepatic intra-arterial 90Y-DOTA-lanreotide as effective palliative therapy. Radiology 2005, 237:718-726.
69. 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, 31:271-279.
70. Memon K, Lewandowski RJ, Mulcahy MF, et al. Radioembolization for neuroendocrine liver metastases: safety, imaging, and long-term outcomes. Int J Radiat Oncol Biol Phys 2012, 83:887-894.
71. Whitney R, Valek V, Fages JF, et al. Transarterial chemoembolization and selective internal radiation for the treatment of patients with metastatic neuroendocrine tumors: a comparison of efficacy and cost. Oncologist 2011, 16:594-601.
72. Crowder CD, Grabowski C, Inampudi S, Sielaff T, Sherman CA, Batts KP Selective internal radiation therapy-induced extrahepatic injury: an emerging cause of iatrogenic organ damage. Am J Surg Pathol 2009, 33:963-975.
73. Kalinowski M, Dressler M, Konig A, et al. Selective internal radiotherapy with Yttrium-90 microspheres for hepatic metastatic neuroendocrine tumors: a prospective single center study. Digestion 2009, 79:137-142.
74. Gulec SA, Pennington K, Hall M, Fong Y Preoperative Y-90 microsphere selective internal radiation treatment for tumor downsizing and future liver remnant recruitment: a novel approach to improving the safety of major hepatic resections. World J Surg Oncol 2009, 7:6.
75. 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.
76. Villard L, Romer A, Marincek N, et al. Cohort study of somatostatin-based radiopeptide therapy with [(90)Y-DOTA]-TOC versus [(90)Y-DOTA]-TOC plus [(177)Lu-DOTA]-TOC in neuroendocrine cancers. J Clin Oncol 2012, 30:1100-1106.
77. 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.
78. Horsch D, Ezziddin S, Haug A, et al. Peptide receptor radionuclide therapy for neuroendocrine tumors in Germany: first results of a multi-institutional cancer registry. Recent Results Cancer Res 2013, 194:457-465.
79. 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.
80. Delaunoit T, Ducreux M, Boige V, et al. The doxorubicin-streptozotocin combination for the treatment of advanced well-differentiated pancreatic endocrine carcinoma; a judicious option?. Eur J Cancer 2004, 40:515-520.
81. Yao JC, Shah MH, Ito T, et al. Everolimus for advanced pancreatic neuroendocrine tumors. N Engl J Med 2011, 364:514-523.
82. 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.
83. 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, 27:4656-4663.
84. Comprehensive molecular characterization of human colon and rectal cancer. Nature 2012, 487:330-337. Cancer Genome Atlas Network.
85. Maitland ML, Schilsky RL Clinical trials in the era of personalized oncology. CA Cancer J Clin 2011, 61:365-381.