Profile of lanreotide autogel and its potential in the treatment of gastroenteropancreatic neuroendocrine tumors

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. 2008;26:3063–3072.
   PubMed Web of Science ®Google Scholar
• Hauso O, Gustafsson BI, Kidd M, et al. Neuroendocrine tumor epidemiology: contrasting Norway and North America. Cancer. 2008;113:2655–2664.
   PubMed Web of Science ®Google Scholar
• Pape UF, Berndt U, Müller-Nordhorn J, et al. Prognostic factors of long-term outcome in gastroenteropancreatic neuroendocrine tumours. Endocr Relat Cancer. 2008;15:1083–1097.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Rindi G, D’Adda T, Froio E, et al. Prognostic factors in gastrointestinal endocrine tumors. Endocr Pathol. 2007;18:145–149.
   PubMed Web of Science ®Google Scholar
• Rindi G, Falconi M, Klersy C, et al. TNM staging of neoplasms of the endocrine pancreas: results from a large international cohort study. J Natl Cancer Inst. 2012;104:764–777.
   PubMedGoogle Scholar
• Strosberg JR, Weber JM, Feldman M, et al. Prognostic validity of the American Joint Committee on Cancer staging classification for midgut neuroendocrine tumors. J Clin Oncol. 2013;31:420–425.
   PubMed Web of Science ®Google Scholar
• Rindi G, Arnold R, Bosman FT, et al. Nomenclature and classification of neuroendocrine neoplasms of the digestive system. In: WHO Classification of Tumors of the Digestive System. Geneva, Switzerland: WHO; 2010:13–14.
   Google Scholar
• Modlin IM, Oberg K, Chung DC, et al. Gastroenteropancreatic neuroendocrine tumours. Lancet Oncol. 2008;9:61–72.
   PubMed Web of Science ®Google Scholar
• Moertel CG, Lefkopoulo M, Lipsitz S, et al. Streptozocin-doxorubicin, streptozocin-fluorouracil or chlorozotocin in the treatment of advanced islet-cell carcinoma. N Engl J Med. 1992;326:519–523.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Yao JC, Shah MH, Ito T, et al. Everolimus for advanced pancreatic neuroendocrine tumors. N Engl J Med. 2011;364:514–523.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Kvols LK, Moertel CG, O’Connell MJ, et al. Treatment of the malignant carcinoid syndrome. Evaluation of a long-acting somatostatin analogue. N Engl J Med. 1986;315:663–666.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Caplin ME, Pavel M, Ćwikła JB, et al. Lanreotide in metastatic enteropancreatic neuroendocrine tumors. N Engl J Med. 2014;371:224–233.
   PubMed Web of Science ®Google Scholar
• Brazeau P, Vale W, Burgus R, et al. Hypothalamic polypeptide that inhibits the secretion of immunoreactive pituitary growth hormone. Science. 1973;179:77–79.
   PubMed Web of Science ®Google Scholar
• Modlin IM, Pavel M, Kidd M, et al. Review article: somatostatin analogues in the treatment of gastroenteropancreatic neuroendocrine (carcinoid) tumours. Aliment Pharmacol Ther. 2010;31:169–188.
   PubMed Web of Science ®Google Scholar
• Lichtenauer-Kaligis EG, Dalm VA, Oomen SP, et al. Differential expression of somatostatin receptor subtypes in human peripheral blood mononuclear cell subsets. Eur J Endocrinol. 2004;150:565–577.
   Web of Science ®Google Scholar
• Caplin M, Sundin A, Nillson O, et al. ENETS Consensus Guidelines for the management of patients with digestive neuroendocrine neoplasms: colorectal neuroendocrine neoplasms. Neuroendocrinology. 2012;95:88–97.
   PubMed Web of Science ®Google Scholar
• Kulaksiz H, Eissele R, Rössler D, et al. Identification of somatostatin receptor subtypes 1, 2A, 3, and 5 in neuroendocrine tumours with subtype specific antibodies. Gut. 2002;50:52–60.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Trocóniz IF, Cendrós JM, Peraire C, et al. Population pharmacokinetic analysis of lanreotide autogel in healthy subjects: evidence for injection interval of up to 2 months. Clin Pharmacokinet. 2009;48:51–62.
   PubMed Web of Science ®Google Scholar
• Buil-Bruna N, Garrido MJ, Dehez M, et al. Population pharmacokinetic (PK) analysis of lanreotide autogel/depot in the treatment of gastroenteropancreatic (GEP) neuroendocrine tumors (NETs): pooled analysis of four clinical trials. J Clin Oncol. 2015;33(Suppl 3):abstr 397. ASCO Meeting Abstracts.
   Web of Science ®Google Scholar
• Bajetta E, Procopio G, Catena L, et al. Lanreotide autogel every 6 weeks compared with Lanreotide microparticles every 3 weeks in patients with well differentiated neuroendocrine tumors: a Phase III Study. Cancer. 2006;107:2474–2481.
   PubMed Web of Science ®Google Scholar
• Betke KM, Wells CA, Hamm HE. GPCR mediated regulation of synaptic transmission. Prog Neurobiol. 2012;96:304–321.
   Web of Science ®Google Scholar
• Weckbecker G, Lewis I, Albert R, et al. Opportunities in somatostatin research: biological, chemical and therapeutic aspects. Nat Rev Drug Discov. 2003;2:999–1017.
   PubMed Web of Science ®Google Scholar
• Guillermet J, Saint-Laurent N, Rochaix P, et al. Somatostatin receptor subtype 2 sensitizes human pancreatic cancer cells to death ligand-induced apoptosis. Proc Natl Acad Sci U S A. 2003;100:155–160.
   PubMed Web of Science ®Google Scholar
• Susini C, Buscail L. Rationale for the use of somatostatin analogs as antitumor agents. Ann Oncol. 2006;17:1733–1742.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• 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. Neuroendocrinology. 2004;80:244–251.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Khan MS, El-Khouly F, Davies P, et al. Long-term results of treatment of malignant carcinoid syndrome with prolonged release Lanreotide (Somatuline Autogel). Aliment Pharmacol Ther. 2011;34:235–242.
   PubMed Web of Science ®Google Scholar
• Vinik A, Wolin EM, Audry H, et al. ELECT: a phase 3 study of efficacy and safety of lanreotide autogel/depot (LAN) treatment for carcinoid syndrome in patients with neuroendocrine tumors (NETs). J Clin Oncol. 2014;32(Suppl 3):abstr 268. ASCO Meeting Abstracts.
   Web of Science ®Google Scholar
• Ruszniewski PB, Caplin ME, Valle JW, et al. Patient-reported satisfaction with symptom control during lanreotide autogel/depot (LAN) treatment for carcinoid syndrome (CS) in gastroenteropancreatic neuroendocrine tumor (GEP-NET) patients: symnet, a large multinational, cross-sectional, observational study. J Clin Oncol. 2014;32(Suppl 3): abstr 273. ASCO Meeting Abstracts.
   Web of Science ®Google Scholar
• Andries M, Glintborg D, Kvistborg A, et al. A 12-month randomized crossover study on the effects of lanreotide autogel and octreotide long-acting repeatable on GH and IGF-l in patients with acromegaly. Clin Endocrinol (Oxf). 2008;68:473–480.
   PubMed Web of Science ®Google Scholar
• 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. 2006;17:461–466.
   PubMed Web of Science ®Google Scholar
• Arnold R, Rinke A, Klose K, et al. Octreotide versus octreotide plus interferon-alpha in endocrine gastroenteropancreatic tumors: a randomized trial. Clin Gastroenterol Hepatol. 2005;3:761–771.
   PubMed Web of Science ®Google Scholar
• Martín-Richard M, Massutí B, Pineda E, et al. Antiproliferative effects of lanreotide autogel in patients with progressive, well-differentiated neuroendocrine tumours: a Spanish, multicentre, open-label, single arm phase II study. BMC Cancer. 2013;13:427.
   PubMed Web of Science ®Google Scholar
• Caplin ME, Pavel M, Ruszniewski P. Lanreotide in metastatic enteropancreatic neuroendocrine tumors. N Engl J Med. 2014;371:1556–1557.
   PubMedGoogle Scholar
• Caplin M, Ruszniewski P, Pavel M, et al. Progression-free survival (PFS) with lanreotide autogel/depot (LAN) in enteropancreatic NETs patients: the CLARINET extension study. J Clin Oncol. 2014;32(18 Suppl): abstr 4107.
   Google Scholar
• Faiss S, Räth U, Mansmann U, et al. Ultra-high-dose lanreotide treatment in patients with metastatic neuroendocrine gastroenteropancreatic tumors. Digestion. 1999;60:469–476.
   PubMed Web of Science ®Google Scholar
• Eriksson B, Renstrup J, Imam H, et al. High-dose treatment with lanreotide of patients with advanced neuroendocrine gastrointestinal tumors: clinical and biological effects. Ann Oncol. 1997;8:1041–1044.
   PubMed Web of Science ®Google Scholar
• Schmid HA. Pasireotide (SOM230): development, mechanism of action and potential applications. Mol Cell Endocrinol. 2008;286:69–74.
   Web of Science ®Google Scholar
• Anthony L, Johnson D, Hande K, et al. Somatostatin analogue phase I trials in neuroendocrine neoplasms. Acta Oncol. 1993;32:217–223.
   PubMed Web of Science ®Google Scholar
• Tomassetti P, Migliori M, Gullo L. Slow-release lanreotide treatment in endocrine gastrointestinal tumors. Am J Gastroenterol. 1998;93:1468–1471.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Aparicio T, Ducreux M, Baudin E, et al. Antitumour activity of somatostatin analogues in progressive metastatic neuroendocrine tumours. Eur J Cancer. 2001;37:1014–1019.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Bianchi A, De Marinis L, Fusco A, et al. The treatment of neuroendocrine tumors with long-acting somatostatin analogs: a single center experience with lanreotide autogel. J Endocrinol Invest. 2011;34:692–697.
   PubMed Web of Science ®Google Scholar