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Current Medicinal Chemistry

Editor-in-Chief

ISSN (Print): 0929-8673
ISSN (Online): 1875-533X

Review Article

Clinical and Translational Research Challenges in Neuroendocrine Tumours

Author(s): Jorge Barriuso* and Angela Lamarca

Volume 27, Issue 29, 2020

Page: [4823 - 4839] Pages: 17

DOI: 10.2174/0929867327666200207120725

open access plus

Abstract

Neuroendocrine tumours (NETs) represent a range of neoplasms that may arise from any (neuro)endocrine cell situated in any part of the human body. As any other rare diseases, NETs face several difficulties in relation to research. This review will describe some of the main challenges and proposed solutions faced by researchers with expertise in rare malignancies.

Some of the most common challenges in clinical and translational research are enumerated in this review, covering aspects from clinical, translational and basic research. NETs being a heterogeneous group of diseases and a limited sample size of clinical and translational research projects are the main challenges.

Challenges with NETs lay over the disparities between healthcare models to tackle rare diseases. NETs add an extra layer of complexity due to a numerous group of different entities.

Prospective real-world data trials are an opportunity for rare cancers with the revolution of electronic health technologies. This review explores potential solutions to these challenges that could be useful not only to the NET community but also to other rare tumours researchers.

Keywords: Neuroendocrine tumours, neoplasms, foregut, midgut, hindgut, translational research.

[1]
Dasari, A.; Shen, C.; Halperin, D.; Zhao, B.; Zhou, S.; Xu, Y.; Shih, T.; Yao, J.C. Trends in the incidence, prevalence, and survival outcomes in patients with neuroendocrine tumors in the United States. JAMA Oncol., 2017, 3(10), 1335-1342.
[http://dx.doi.org/10.1001/jamaoncol.2017.0589] [PMID: 28448665]
[2]
Klimstra, D.S.; Kloppell, G.; La Rosa, S.; Rindi, G. Classification of neuroendocrine neoplasms of the digestive system.WHO Classification of Tumours: Digestive System Tumours; 5th ed; WHO Classification of Tumours Editorial Board (Ed), International Agency for Research on Cancer: Lyon, 2019, p. 16.
[3]
Caplin, M.E.; Pavel, M.; Ćwikła, J.B.; Phan, A.T.; Raderer, M.; Sedláčková, E.; Cadiot, G.; Wolin, E.M.; Capdevila, J.; Wall, L.; Rindi, G.; Langley, A.; Martinez, S.; Gomez-Panzani, E.; Ruszniewski, P. CLARINET Investigators. Anti-tumour effects of lanreotide for pancreatic and intestinal neuroendocrine tumours: the CLARINET open-label extension study. Endocr. Relat. Cancer, 2016, 23(3), 191-199.
[http://dx.doi.org/10.1530/ERC-15-0490] [PMID: 26743120]
[4]
Raymond, E.; Dahan, L.; Raoul, J.L.; Bang, Y.J.; Borbath, I.; Lombard-Bohas, C.; Valle, J.; Metrakos, P.; Smith, D.; Vinik, A.; Chen, J.S.; Hörsch, D.; Hammel, P.; Wiedenmann, B.; Van Cutsem, E.; Patyna, S.; Lu, D.R.; Blanckmeister, C.; Chao, R.; Ruszniewski, P. Sunitinib malate for the treatment of pancreatic neuroendocrine tumors. N. Engl. J. Med., 2011, 364(6), 501-513.
[http://dx.doi.org/10.1056/NEJMoa1003825] [PMID: 21306237]
[5]
Yao, J.C.; Shah, M.H.; Ito, T.; Bohas, C.L.; Wolin, E.M.; Van Cutsem, E.; Hobday, T.J.; Okusaka, T.; Capdevila, J.; de Vries, E.G.; Tomassetti, P.; Pavel, M.E.; Hoosen, S.; Haas, T.; Lincy, J.; Lebwohl, D.; Öberg, K. RAD001 in Advanced Neuroendocrine Tumors, Third Trial (RADIANT-3) Study Group. Everolimus for advanced pancreatic neuroendocrine tumors. N. Engl. J. Med., 2011, 364(6), 514-523.
[http://dx.doi.org/10.1056/NEJMoa1009290] [PMID: 21306238]
[6]
Strosberg, J.; El-Haddad, G.; Wolin, E.; Hendifar, A.; Yao, J.; Chasen, B.; Mittra, E.; Kunz, P.L.; Kulke, M.H.; Jacene, H.; Bushnell, D.; O’Dorisio, T.M.; Baum, R.P.; Kulkarni, H.R.; Caplin, M.; Lebtahi, R.; Hobday, T.; Delpassand, E.; Van Cutsem, E.; Benson, A.; Srirajaskanthan, R.; Pavel, M.; Mora, J.; Berlin, J.; Grande, E.; Reed, N.; Seregni, E.; Öberg, K.; Lopera Sierra, M.; Santoro, P.; Thevenet, T.; Erion, J.L.; Ruszniewski, P.; Kwekkeboom, D.; Krenning, E. NETTER-1 Trial Investigators. Phase 3 Trial of 177Lu-Dotatate for Midgut Neuroendocrine Tumors. N. Engl. J. Med., 2017, 376(2), 125-135.
[http://dx.doi.org/10.1056/NEJMoa1607427] [PMID: 28076709]
[7]
Kulke, M.H.; O’Dorisio, T.; Phan, A.; Bergsland, E.; Law, L.; Banks, P.; Freiman, J.; Frazier, K.; Jackson, J.; Yao, J.C.; Kvols, L.; Lapuerta, P.; Zambrowicz, B.; Fleming, D.; Sands, A. Telotristat etiprate, a novel serotonin synthesis inhibitor, in patients with carcinoid syndrome and diarrhea not adequately controlled by octreotide. Endocr. Relat. Cancer, 2014, 21(5), 705-714.
[http://dx.doi.org/10.1530/ERC-14-0173] [PMID: 25012985]
[8]
Yao, J.C.; Fazio, N.; Singh, S.; Buzzoni, R.; Carnaghi, C.; Wolin, E.; Tomasek, J.; Raderer, M.; Lahner, H.; Voi, M.; Pacaud, L.B.; Rouyrre, N.; Sachs, C.; Valle, J.W.; Fave, G.D.; Van Cutsem, E.; Tesselaar, M.; Shimada, Y.; Oh, D.Y.; Strosberg, J.; Kulke, M.H.; Pavel, M.E. RAD001 in Advanced Neuroendocrine Tumours, Fourth Trial (RADIANT-4) Study Group. Everolimus for the treatment of advanced, non-functional neuroendocrine tumours of the lung or gastrointestinal tract (RADIANT-4): a randomised, placebo-controlled, phase 3 study. Lancet, 2016, 387(10022), 968-977.
[http://dx.doi.org/10.1016/S0140-6736(15)00817-X] [PMID: 26703889]
[9]
Scarpa, A.; Chang, D.K.; Nones, K.; Corbo, V.; Patch, A.M.; Bailey, P.; Lawlor, R.T.; Johns, A.L.; Miller, D.K.; Mafficini, A.; Rusev, B.; Scardoni, M.; Antonello, D.; Barbi, S.; Sikora, K.O.; Cingarlini, S.; Vicentini, C.; McKay, S.; Quinn, M.C.; Bruxner, T.J.; Christ, A.N.; Harliwong, I.; Idrisoglu, S.; McLean, S.; Nourse, C.; Nourbakhsh, E.; Wilson, P.J.; Anderson, M.J.; Fink, J.L.; Newell, F.; Waddell, N.; Holmes, O.; Kazakoff, S.H.; Leonard, C.; Wood, S.; Xu, Q.; Nagaraj, S.H.; Amato, E.; Dalai, I.; Bersani, S.; Cataldo, I.; Dei Tos, A.P.; Capelli, P.; Davì, M.V.; Landoni, L.; Malpaga, A.; Miotto, M.; Whitehall, V.L.; Leggett, B.A.; Harris, J.L.; Harris, J.; Jones, M.D.; Humphris, J.; Chantrill, L.A.; Chin, V.; Nagrial, A.M.; Pajic, M.; Scarlett, C.J.; Pinho, A.; Rooman, I.; Toon, C.; Wu, J.; Pinese, M.; Cowley, M.; Barbour, A.; Mawson, A.; Humphrey, E.S.; Colvin, E.K.; Chou, A.; Lovell, J.A.; Jamieson, N.B.; Duthie, F.; Gingras, M.C.; Fisher, W.E.; Dagg, R.A.; Lau, L.M.; Lee, M.; Pickett, H.A.; Reddel, R.R.; Samra, J.S.; Kench, J.G.; Merrett, N.D.; Epari, K.; Nguyen, N.Q.; Zeps, N.; Falconi, M.; Simbolo, M.; Butturini, G.; Van Buren, G.; Partelli, S.; Fassan, M.; Khanna, K.K.; Gill, A.J.; Wheeler, D.A.; Gibbs, R.A.; Musgrove, E.A.; Bassi, C.; Tortora, G.; Pederzoli, P.; Pearson, J.V.; Waddell, N.; Biankin, A.V.; Grimmond, S.M. Australian Pancreatic Cancer Genome Initiative. Whole-genome landscape of pancreatic neuroendocrine tumours. Nature, 2017, 543(7643), 65-71.
[http://dx.doi.org/10.1038/nature21063] [PMID: 28199314]
[10]
Francis, J.M.; Kiezun, A.; Ramos, A.H.; Serra, S.; Pedamallu, C.S.; Qian, Z.R.; Banck, M.S.; Kanwar, R.; Kulkarni, A.A.; Karpathakis, A.; Manzo, V.; Contractor, T.; Philips, J.; Nickerson, E.; Pho, N.; Hooshmand, S.M.; Brais, L.K.; Lawrence, M.S.; Pugh, T.; McKenna, A.; Sivachenko, A.; Cibulskis, K.; Carter, S.L.; Ojesina, A.I.; Freeman, S.; Jones, R.T.; Voet, D.; Saksena, G.; Auclair, D.; Onofrio, R.; Shefler, E.; Sougnez, C.; Grimsby, J.; Green, L.; Lennon, N.; Meyer, T.; Caplin, M.; Chung, D.C.; Beutler, A.S.; Ogino, S.; Thirlwell, C.; Shivdasani, R.; Asa, S.L.; Harris, C.R.; Getz, G.; Kulke, M.; Meyerson, M. Somatic mutation of CDKN1B in small intestine neuroendocrine tumors. Nat. Genet., 2013, 45(12), 1483-1486.
[http://dx.doi.org/10.1038/ng.2821] [PMID: 24185511]
[11]
Busico, A.; Maisonneuve, P.; Prinzi, N.; Pusceddu, S.; Centonze, G.; Garzone, G.; Pelligrinelli, A.; Giacomelli, L.; Mangogna, A.; Paolino, C.; Belfiore, A.; Kankava, K.; Perrone, F.; Tamborini, E.; Pruneri, G.; Fazio, N.; Milione, M. Gastroenteropancreatic High-Grade Neuroendocrine Neoplasms (H-NENs): histology and molecular analysis, two sides of the same coin. Neuroendocrinology, 2020, 110(7-8), 616-629.
[http://dx.doi.org/10.1159/000503722] [PMID: 31557757]
[12]
Lamarca, A.; Nonaka, D.; Breitwieser, W.; Ashton, G.; Barriuso, J.; McNamara, M.G.; Moghadam, S.; Rogan, J.; Mansoor, W.; Hubner, R.A.; Clark, C.; Chakrabarty, B.; Valle, J.W. PD-L1 expression and presence of TILs in small intestinal neuroendocrine tumours. Oncotarget, 2018, 9(19), 14922-14938.
[http://dx.doi.org/10.18632/oncotarget.24464] [PMID: 29599916]
[13]
Demetri, G.D.; von Mehren, M.; Blanke, C.D.; Van den Abbeele, A.D.; Eisenberg, B.; Roberts, P.J.; Heinrich, M.C.; Tuveson, D.A.; Singer, S.; Janicek, M.; Fletcher, J.A.; Silverman, S.G.; Silberman, S.L.; Capdeville, R.; Kiese, B.; Peng, B.; Dimitrijevic, S.; Druker, B.J.; Corless, C.; Fletcher, C.D.; Joensuu, H. Efficacy and safety of imatinib mesylate in advanced gastrointestinal stromal tumors. N. Engl. J. Med., 2002, 347(7), 472-480.
[http://dx.doi.org/10.1056/NEJMoa020461] [PMID: 12181401]
[14]
Mathoulin-Pélissier, S.; Pritchard-Jones, K. Evidence-based data and rare cancers: The need for a new methodological approach in research and investigation. Eur. J. Surg. Oncol., 2019, 45(1), 22-30.
[http://dx.doi.org/10.1016/j.ejso.2018.02.015] [PMID: 29526369]
[15]
Tran, B.; Kopetz, S.; Tie, J.; Gibbs, P.; Jiang, Z.Q.; Lieu, C.H.; Agarwal, A.; Maru, D.M.; Sieber, O.; Desai, J. Impact of BRAF mutation and microsatellite instability on the pattern of metastatic spread and prognosis in metastatic colorectal cancer. Cancer, 2011, 117(20), 4623-4632.
[http://dx.doi.org/10.1002/cncr.26086] [PMID: 21456008]
[16]
Strosberg, J.R.; Kvols, L.K. A review of the current clinical trials for gastroenteropancreatic neuroendocrine tumours. Expert Opin. Investig. Drugs, 2007, 16(2), 219-224.
[http://dx.doi.org/10.1517/13543784.16.2.219] [PMID: 17243941]
[17]
Strosberg, J.R.; Fine, R.L.; Choi, J.; Nasir, A.; Coppola, D.; Chen, D.T.; Helm, J.; Kvols, L. First-line chemotherapy with capecitabine and temozolomide in patients with metastatic pancreatic endocrine carcinomas. Cancer, 2011, 117(2), 268-275.
[http://dx.doi.org/10.1002/cncr.25425] [PMID: 20824724]
[18]
Strosberg, J.R.; Cheema, A.; Kvols, L.K. A review of systemic and liver-directed therapies for metastatic neuroendocrine tumors of the gastroenteropancreatic tract. Cancer Contr., 2011, 18(2), 127-137.
[http://dx.doi.org/10.1177/107327481101800207] [PMID: 21451455]
[19]
Kunz, PL; Catalano, PJ; Nimeiri, H; Fisher, GA; Longacre, TA; Suarez, C.J. A randomized study of temozolomide or temozolomide and capecitabine in patients with advanced pancreatic neuroendocrine tumors: A trial of the ECOGACRIN Cancer Research Group (E2211). Journal of Clinical Oncology, 2018, 36((15_suppl)), 4004.
[20]
Grande, E.; Capdevila, J.; Castellano, D.; Teulé, A.; Durán, I.; Fuster, J.; Sevilla, I.; Escudero, P.; Sastre, J.; García-Donas, J.; Casanovas, O.; Earl, J.; Ortega, L.; Apellaniz-Ruiz, M.; Rodriguez-Antona, C.; Alonso-Gordoa, T.; Díez, J.J.; Carrato, A.; García-Carbonero, R. Pazopanib in pretreated advanced neuroendocrine tumors: a phase II, open-label trial of the Spanish Task Force Group for Neuroendocrine Tumors (GETNE). Ann. Oncol., 2015, 26(9), 1987-1993.
[http://dx.doi.org/10.1093/annonc/mdv252] [PMID: 26063633]
[21]
Castellano, D.; Capdevila, J.; Sastre, J.; Alonso, V.; Llanos, M.; García-Carbonero, R.; Manzano Mozo, J.L.; Sevilla, I.; Durán, I.; Salazar, R. Sorafenib and bevacizumab combination targeted therapy in advanced neuroendocrine tumour: a phase II study of Spanish Neuroendocrine Tumour Group (GETNE0801). Eur. J. Cancer, 2013, 49(18), 3780-3787.
[http://dx.doi.org/10.1016/j.ejca.2013.06.042] [PMID: 24012098]
[22]
Capdevila, J.; Teule, A.; Barriuso, J.; Castellano, D.; Lopez, C.; Manzano, J.L.; Phase, I.I. Study of Everolimus and Octreotide LAR in Patients with Nonfunctioning Gastrointestinal Neuroendocrine Tumors: The GETNE1003_EVERLAR study. Oncologist, 2019, 24(1), 38-46.
[PMID: 29794066]
[23]
Yao, J.C.; Lagunes, D.R.; Kulke, M.H. Targeted therapies in neuroendocrine tumors (NET): clinical trial challenges and lessons learned. Oncologist, 2013, 18(5), 525-532.
[http://dx.doi.org/10.1634/theoncologist.2012-0434] [PMID: 23615698]
[24]
Eisenhauer, E.A.; Therasse, P.; Bogaerts, J.; Schwartz, L.H.; Sargent, D.; Ford, R.; Dancey, J.; Arbuck, S.; Gwyther, S.; Mooney, M.; Rubinstein, L.; Shankar, L.; Dodd, L.; Kaplan, R.; Lacombe, D.; Verweij, J. New response evaluation criteria in solid tumours: revised RECIST guideline (version 1.1). Eur. J. Cancer, 2009, 45(2), 228-247.
[http://dx.doi.org/10.1016/j.ejca.2008.10.026] [PMID: 19097774]
[25]
Therasse, P.; Eisenhauer, E.A.; Verweij, J. RECIST revisited: a review of validation studies on tumour assessment. Eur. J. Cancer, 2006, 42(8), 1031-1039.
[http://dx.doi.org/10.1016/j.ejca.2006.01.026] [PMID: 16616487]
[26]
Eisenhauer, E.A. Response evaluation: beyond RECIST. Ann. Oncol., 2007, 18(Suppl. 9), ix29-ix32.
[http://dx.doi.org/10.1093/annonc/mdm290] [PMID: 17631592]
[27]
Lamarca, A.; Barriuso, J.; Kulke, M.; Borbath, I.; Lenz, H.J.; Raoul, J.L.; Meropol, N.J.; Lombard-Bohas, C.; Posey, J.; Faivre, S.; Raymond, E.; Valle, J.W. Determination of an optimal response cut-off able to predict progression-free survival in patients with well-differentiated advanced pancreatic neuroendocrine tumours treated with sunitinib: an alternative to the current RECIST-defined response. Br. J. Cancer, 2018, 118(2), 181-188.
[http://dx.doi.org/10.1038/bjc.2017.402] [PMID: 29161241]
[28]
Raymond, E.; Kulke, M.H.; Qin, S.; Yu, X.; Schenker, M.; Cubillo, A.; Lou, W.; Tomasek, J.; Thiis-Evensen, E.; Xu, J.M.; Croitoru, A.E.; Khasraw, M.; Sedlackova, E.; Borbath, I.; Ruff, P.; Oberstein, P.E.; Ito, T.; Jia, L.; Hammel, P.; Shen, L.; Shrikhande, S.V.; Shen, Y.; Sufliarsky, J.; Khan, G.N.; Morizane, C.; Galdy, S.; Khosravan, R.; Fernandez, K.C.; Rosbrook, B.; Fazio, N. Efficacy and safety of sunitinib in patients with well-differentiated pancreatic neuroendocrine tumours. Neuroendocrinology, 2018, 107(3), 237-245.
[http://dx.doi.org/10.1159/000491999] [PMID: 29991024]
[29]
Faivre, S.; Ronot, M.; Dreyer, C.; Serrate, C.; Hentic, O.; Bouattour, M.; Bruno, O.; Couvelard, A.; Vilgrain, V.; Raymond, E. Imaging response in neuroendocrine tumors treated with targeted therapies: the experience of sunitinib. Target. Oncol., 2012, 7(2), 127-133.
[http://dx.doi.org/10.1007/s11523-012-0216-y] [PMID: 22585430]
[30]
Oberg, K.E. The management of neuroendocrine tumours: current and future medical therapy options. Clin. Oncol. (R. Coll. Radiol.), 2012, 24(4), 282-293.
[http://dx.doi.org/10.1016/j.clon.2011.08.006] [PMID: 21907552]
[31]
Rinke, A.; Müller, H.H.; Schade-Brittinger, C.; Klose, K.J.; Barth, P.; Wied, M.; Mayer, C.; Aminossadati, B.; Pape, U.F.; Bläker, M.; Harder, J.; Arnold, C.; Gress, T.; Arnold, R. PROMID Study Group. 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(28), 4656-4663.
[http://dx.doi.org/10.1200/JCO.2009.22.8510] [PMID: 19704057]
[32]
Blumenthal, G.M.; Cortazar, P.; Zhang, J.J.; Tang, S.; Sridhara, R.; Murgo, A.; Justice, R.; Pazdur, R. FDA approval summary: sunitinib for the treatment of progressive well-differentiated locally advanced or metastatic pancreatic neuroendocrine tumors. Oncologist, 2012, 17(8), 1108-1113.
[http://dx.doi.org/10.1634/theoncologist.2012-0044] [PMID: 22836448]
[33]
Hendifar, A.E.; Dhall, D.; Strosberg, J.R. The evolving treatment algorithm for advanced neuroendocrine neoplasms: diversity and commonalities across tumor types. Oncologist, 2019, 24(1), 54-61.
[http://dx.doi.org/10.1634/theoncologist.2018-0187] [PMID: 30104288]
[34]
Kulke, M.H.; Siu, L.L.; Tepper, J.E.; Fisher, G.; Jaffe, D.; Haller, D.G.; Ellis, L.M.; Benedetti, J.K.; Bergsland, E.K.; Hobday, T.J.; Van Cutsem, E.; Pingpank, J.; Oberg, K.; Cohen, S.J.; Posner, M.C.; Yao, J.C. Future directions in the treatment of neuroendocrine tumors: consensus report of the National Cancer Institute Neuroendocrine Tumor clinical trials planning meeting. J. Clin. Oncol., 2011, 29(7), 934-943.
[http://dx.doi.org/10.1200/JCO.2010.33.2056] [PMID: 21263089]
[35]
Rinke, A.; Wittenberg, M.; Schade-Brittinger, C.; Aminossadati, B.; Ronicke, E.; Gress, T.M.; Müller, H.H.; Arnold, R. PROMID Study Group. 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 (PROMID): results of long-term survival. Neuroendocrinology, 2017, 104(1), 26-32.
[http://dx.doi.org/10.1159/000443612] [PMID: 26731483]
[36]
Kulke, M.H.; Ruszniewski, P.; Van Cutsem, E.; Lombard-Bohas, C.; Valle, J.W.; De Herder, W.W.; Pavel, M.; Degtyarev, E.; Brase, J.C.; Bubuteishvili-Pacaud, L.; Voi, M.; Salazar, R.; Borbath, I.; Fazio, N.; Smith, D.; Capdevila, J.; Riechelmann, R.P.; Yao, J.C. A randomized, open-label, phase 2 study of everolimus in combination with pasireotide LAR or everolimus alone in advanced, well-differentiated, progressive pancreatic neuroendocrine tumors: COOPERATE-2 trial. Ann. Oncol., 2017, 28(6), 1309-1315.
[http://dx.doi.org/10.1093/annonc/mdx078] [PMID: 28327907]
[37]
Ferolla, P.; Brizzi, M.P.; Meyer, T.; Mansoor, W.; Mazieres, J.; Do Cao, C.; Léna, H.; Berruti, A.; Damiano, V.; Buikhuisen, W.; Grønbæk, H.; Lombard-Bohas, C.; Grohé, C.; Minotti, V.; Tiseo, M.; De Castro, J.; Reed, N.; Gislimberti, G.; Singh, N.; Stankovic, M.; Öberg, K.; Baudin, E. Efficacy and safety of long-acting pasireotide or everolimus alone or in combination in patients with advanced carcinoids of the lung and thymus (LUNA): an open-label, multicentre, randomised, phase 2 trial. Lancet Oncol., 2017, 18(12), 1652-1664.
[http://dx.doi.org/10.1016/S1470-2045(17)30681-2] [PMID: 29074099]
[38]
Seymour, L.; Ivy, S.P.; Sargent, D.; Spriggs, D.; Baker, L.; Rubinstein, L.; Ratain, M.J.; Le Blanc, M.; Stewart, D.; Crowley, J.; Groshen, S.; Humphrey, J.S.; West, P.; Berry, D. The design of phase II clinical trials testing cancer therapeutics: consensus recommendations from the clinical trial design task force of the national cancer institute investigational drug steering committee. Clin. Cancer Res., 2010, 16(6), 1764-1769.
[http://dx.doi.org/10.1158/1078-0432.CCR-09-3287] [PMID: 20215557]
[39]
Cives, M.; Strosberg, J. An update on gastroenteropancreatic neuroendocrine tumors. Oncology (Williston Park), 2014, 28(9), 749-758.
[PMID: 25224471]
[40]
Cives, M.; Soares, H.P.; Strosberg, J. Will clinical heterogeneity of neuroendocrine tumors impact their management in the future? Lessons from recent trials. Curr. Opin. Oncol., 2016, 28(4), 359-366.
[http://dx.doi.org/10.1097/CCO.0000000000000299] [PMID: 27138571]
[41]
Yachida, S.; Vakiani, E.; White, C.M.; Zhong, Y.; Saunders, T.; Morgan, R.; de Wilde, R.F.; Maitra, A.; Hicks, J.; Demarzo, A.M.; Shi, C.; Sharma, R.; Laheru, D.; Edil, B.H.; Wolfgang, C.L.; Schulick, R.D.; Hruban, R.H.; Tang, L.H.; Klimstra, D.S.; Iacobuzio-Donahue, C.A. Small cell and large cell neuroendocrine carcinomas of the pancreas are genetically similar and distinct from well-differentiated pancreatic neuroendocrine tumors. Am. J. Surg. Pathol., 2012, 36(2), 173-184.
[http://dx.doi.org/10.1097/PAS.0b013e3182417d36] [PMID: 22251937]
[42]
Takizawa, N.; Ohishi, Y.; Hirahashi, M.; Takahashi, S.; Nakamura, K.; Tanaka, M.; Oki, E.; Takayanagi, R.; Oda, Y. Molecular characteristics of colorectal neuroendocrine carcinoma; similarities with adenocarcinoma rather than neuroendocrine tumor. Hum. Pathol., 2015, 46(12), 1890-1900.
[http://dx.doi.org/10.1016/j.humpath.2015.08.006] [PMID: 26434631]
[43]
Fernandez-Cuesta, L.; Peifer, M.; Lu, X.; Sun, R.; Ozretić, L.; Seidal, D.; Zander, T.; Leenders, F.; George, J.; Müller, C.; Dahmen, I.; Pinther, B.; Bosco, G.; Konrad, K.; Altmüller, J.; Nürnberg, P.; Achter, V.; Lang, U.; Schneider, P.M.; Bogus, M.; Soltermann, A.; Brustugun, O.T.; Helland, Å.; Solberg, S.; Lund-Iversen, M.; Ansén, S.; Stoelben, E.; Wright, G.M.; Russell, P.; Wainer, Z.; Solomon, B.; Field, J.K.; Hyde, R.; Davies, M.P.; Heukamp, L.C.; Petersen, I.; Perner, S.; Lovly, C.; Cappuzzo, F.; Travis, W.D.; Wolf, J.; Vingron, M.; Brambilla, E.; Haas, S.A.; Buettner, R.; Thomas, R.K. Frequent mutations in chromatin-remodelling genes in pulmonary carcinoids. Nat. Commun., 2014, 5, 3518.
[http://dx.doi.org/10.1038/ncomms4518] [PMID: 24670920]
[44]
Jiao, Y.; Shi, C.; Edil, B.H.; de Wilde, R.F.; Klimstra, D.S.; Maitra, A.; Schulick, R.D.; Tang, L.H.; Wolfgang, C.L.; Choti, M.A.; Velculescu, V.E.; Diaz, L.A., Jr; Vogelstein, B.; Kinzler, K.W.; Hruban, R.H.; Papadopoulos, N. DAXX/ATRX, MEN1, and mTOR pathway genes are frequently altered in pancreatic neuroendocrine tumors. Science, 2011, 331(6021), 1199-1203.
[http://dx.doi.org/10.1126/science.1200609] [PMID: 21252315]
[45]
Karpathakis, A.; Dibra, H.; Pipinikas, C.; Feber, A.; Morris, T.; Francis, J.; Oukrif, D.; Mandair, D.; Pericleous, M.; Mohmaduvesh, M.; Serra, S.; Ogunbiyi, O.; Novelli, M.; Luong, T.; Asa, S.L.; Kulke, M.; Toumpanakis, C.; Meyer, T.; Caplin, M.; Meyerson, M.; Beck, S.; Thirlwell, C. Prognostic impact of novel molecular subtypes of small intestinal neuroendocrine tumor. Clin. Cancer Res., 2016, 22(1), 250-258.
[http://dx.doi.org/10.1158/1078-0432.CCR-15-0373] [PMID: 26169971]
[46]
Sadanandam, A.; Wullschleger, S.; Lyssiotis, C.A.; Grötzinger, C.; Barbi, S.; Bersani, S.; Körner, J.; Wafy, I.; Mafficini, A.; Lawlor, R.T.; Simbolo, M.; Asara, J.M.; Bläker, H.; Cantley, L.C.; Wiedenmann, B.; Scarpa, A.; Hanahan, D. A cross-species analysis in pancreatic neuroendocrine tumors reveals molecular subtypes with distinctive clinical, metastatic, developmental, and metabolic characteristics. Cancer Discov., 2015, 5(12), 1296-1313.
[http://dx.doi.org/10.1158/2159-8290.CD-15-0068] [PMID: 26446169]
[47]
Carrick, D.M.; Mehaffey, M.G.; Sachs, M.C.; Altekruse, S.; Camalier, C.; Chuaqui, R.; Cozen, W.; Das, B.; Hernandez, B.Y.; Lih, C.J.; Lynch, C.F.; Makhlouf, H.; McGregor, P.; McShane, L.M.; Phillips Rohan, J.; Walsh, W.D.; Williams, P.M.; Gillanders, E.M.; Mechanic, L.E.; Schully, S.D. Robustness of next generation sequencing on older formalin-fixed paraffin-embedded tissue. PLoS One, 2015, 10(7)e0127353
[http://dx.doi.org/10.1371/journal.pone.0127353]] [PMID: 26222067]
[48]
Adiconis, X.; Haber, A.L.; Simmons, S.K.; Levy Moonshine, A.; Ji, Z.; Busby, M.A.; Shi, X.; Jacques, J.; Lancaster, M.A.; Pan, J.Q.; Regev, A.; Levin, J.Z. Comprehensive comparative analysis of 5′-end RNA-sequencing methods. Nat. Methods, 2018, 15(7), 505-511.
[http://dx.doi.org/10.1038/s41592-018-0014-2] [PMID: 29867192]
[49]
Gagne, J.J.; Thompson, L.; O’Keefe, K.; Kesselheim, A.S. Innovative research methods for studying treatments for rare diseases: methodological review. BMJ, 2014, 349, g6802.
[http://dx.doi.org/10.1136/bmj.g6802] [PMID: 25422272]
[50]
Shurin, S.; Krischer, J.; Groft, S.C. Clinical trials In BMT: ensuring that rare diseases and rarer therapies are well done. Biol. Blood Marrow Transplant., 2012, 18(1)(Suppl.), S8-S11.
[http://dx.doi.org/10.1016/j.bbmt.2011.10.030] [PMID: 22226117]
[51]
Whitehead, J.; Tishkovskaya, S.; O’Connor, J.; Damato, B. Devising two-stage and multistage phase II studies on systemic adjuvant therapy for uveal melanoma. Invest. Ophthalmol. Vis. Sci., 2012, 53(8), 4986-4989.
[http://dx.doi.org/10.1167/iovs.12-9858] [PMID: 22743326]
[52]
Stone, E.M. Challenges in genetic testing for clinical trials of inherited and orphan retinal diseases. Retina, 2005, 25(8)(Suppl.), S72-S73.
[http://dx.doi.org/10.1097/00006982-200512001-00034] [PMID: 16374347]
[53]
Buckley, B.M. Clinical trials of orphan medicines. Lancet, 2008, 371(9629), 2051-2055.
[http://dx.doi.org/10.1016/S0140-6736(08)60876-4] [PMID: 18555919]
[54]
van der Lee, J.H.; Wesseling, J.; Tanck, M.W.; Offringa, M. Efficient ways exist to obtain the optimal sample size in clinical trials in rare diseases. J. Clin. Epidemiol., 2008, 61(4), 324-330.
[http://dx.doi.org/10.1016/j.jclinepi.2007.07.008] [PMID: 18313556]
[55]
Kinder, B.; McCormack, F.X. Clinical trials for rare lung diseases: lessons from lymphangioleiomyomatosis. Lymphat. Res. Biol., 2010, 8(1), 71-79.
[http://dx.doi.org/10.1089/lrb.2009.0027] [PMID: 20235889]
[56]
Chow, S.C.; Chang, M. Adaptive design methods in clinical trials - a review. Orphanet J. Rare Dis., 2008, 3, 11.
[http://dx.doi.org/10.1186/1750-1172-3-11] [PMID: 18454853]
[57]
Gupta, S.; Faughnan, M.E.; Tomlinson, G.A.; Bayoumi, A.M. A framework for applying unfamiliar trial designs in studies of rare diseases. J. Clin. Epidemiol., 2011, 64(10), 1085-1094.
[http://dx.doi.org/10.1016/j.jclinepi.2010.12.019] [PMID: 21530171]
[58]
Cornu, C.; Kassai, B.; Fisch, R.; Chiron, C.; Alberti, C.; Guerrini, R.; Rosati, A.; Pons, G.; Tiddens, H.; Chabaud, S.; Caudri, D.; Ballot, C.; Kurbatova, P.; Castellan, A.C.; Bajard, A.; Nony, P.; Aarons, L.; Bajard, A.; Ballot, C.; Bertrand, Y.; Bretz, F.; Caudri, D.; Castellan, C.; Chabaud, S.; Cornu, C.; Dufour, F.; Dunger-Baldauf, C.; Dupont, J.M.; Fisch, R.; Guerrini, R.; Jullien, V.; Kassaï, B.; Nony, P.; Ogungbenro, K.; Pérol, D.; Pons, G.; Tiddens, H.; Rosati, A.; Alberti, C.; Chiron, C.; Kurbatova, P.; Nabbout, R. CRESim & Epi-CRESim Project Groups. Experimental designs for small randomised clinical trials: an algorithm for choice. Orphanet J. Rare Dis., 2013, 8, 48.
[http://dx.doi.org/10.1186/1750-1172-8-48] [PMID: 23531234]
[59]
Dimichele, D.M.; Blanchette, V.; Berntorp, E. Clinical trial design in haemophilia. Haemophilia, 2012, 18(Suppl. 4), 18-23.
[http://dx.doi.org/10.1111/j.1365-2516.2012.02824.x] [PMID: 22726077]
[60]
Gallin, J.I.; Alling, D.W.; Malech, H.L.; Wesley, R.; Koziol, D.; Marciano, B.; Eisenstein, E.M.; Turner, M.L.; DeCarlo, E.S.; Starling, J.M.; Holland, S.M. Itraconazole to prevent fungal infections in chronic granulomatous disease. N. Engl. J. Med., 2003, 348(24), 2416-2422.
[http://dx.doi.org/10.1056/NEJMoa021931] [PMID: 12802027]
[61]
Puopolo, M.; Pocchiari, M.; Petrini, C. Clinical trials and methodological problems in prion diseases. Lancet Neurol., 2009, 8(9), 782.
[http://dx.doi.org/10.1016/S1474-4422(09)70214-5] [PMID: 19679270]
[62]
Halpern, S.D.; Karlawish, J.H.; Berlin, J.A. The continuing unethical conduct of underpowered clinical trials. JAMA, 2002, 288(3), 358-362.
[http://dx.doi.org/10.1001/jama.288.3.358] [PMID: 12117401]
[63]
Lilford, R.J.; Thornton, J.G.; Braunholtz, D. Clinical trials and rare diseases: a way out of a conundrum. BMJ, 1995, 311(7020), 1621-1625.
[http://dx.doi.org/10.1136/bmj.311.7020.1621] [PMID: 8555809]
[64]
Tan, S.B.; Dear, K.B.; Bruzzi, P.; Machin, D. Strategy for randomised clinical trials in rare cancers. BMJ, 2003, 327(7405), 47-49.
[http://dx.doi.org/10.1136/bmj.327.7405.47] [PMID: 12842959]
[65]
Lagakos, S.W. Clinical trials and rare diseases. N. Engl. J. Med., 2003, 348(24), 2455-2456.
[http://dx.doi.org/10.1056/NEJMe030024] [PMID: 12802033]
[66]
Hyman, L. Design of phase III clinical trials for treatments of orphan retinal diseases: an overview of considerations. Retina, 2005, 25(8)(Suppl.), S69-S71.
[http://dx.doi.org/10.1097/00006982-200512001-00033] [PMID: 16374346]
[67]
Berlin, J.A. N-of-1 clinical trials should be incorporated into clinical practice. J. Clin. Epidemiol., 2010, 63(12), 1283-1284.
[http://dx.doi.org/10.1016/j.jclinepi.2010.05.006] [PMID: 20800449]
[68]
Weinreich, S.S.; Vrinten, C.; Kuijpers, M.R.; Lipka, A.F.; Schimmel, K.J.M.; van Zwet, E.W.; Gispen-de Wied, C.; Hekster, Y.A.; Verschuuren, J.J.G.M.; Cornel, M.C. Aggregated N-of-1 trials for unlicensed medicines for small populations: an assessment of a trial with ephedrine for myasthenia gravis. Orphanet J. Rare Dis., 2017, 12(1), 88.
[http://dx.doi.org/10.1186/s13023-017-0636-y] [PMID: 28494776]
[69]
Lillie, E.O.; Patay, B.; Diamant, J.; Issell, B.; Topol, E.J.; Schork, N.J. The n-of-1 clinical trial: the ultimate strategy for individualizing medicine? Per. Med., 2011, 8(2), 161-173.
[http://dx.doi.org/10.2217/pme.11.7] [PMID: 21695041]
[70]
Khozin, S.; Blumenthal, G.M.; Pazdur, R. Real-world data for clinical evidence generation in oncology. J. Natl. Cancer Inst., 2017, 109(11)
[http://dx.doi.org/10.1093/jnci/djx187] [PMID: 29059439]
[71]
Mandair, D.; Vesely, C.; Ensell, L.; Lowe, H.; Spanswick, V.; Hartley, J.A.; Caplin, M.E.; Meyer, T. A comparison of CellCollector with CellSearch in patients with neuroendocrine tumours. Endocr. Relat. Cancer, 2016, 23(10), L29-L32.
[http://dx.doi.org/10.1530/ERC-16-0201] [PMID: 27521132]
[72]
Childs, A.; Vesely, C.; Ensell, L.; Lowe, H.; Luong, T.V.; Caplin, M.E.; Toumpanakis, C.; Thirlwell, C.; Hartley, J.A.; Meyer, T. Expression of somatostatin receptors 2 and 5 in circulating tumour cells from patients with neuroendocrine tumours. Br. J. Cancer, 2016, 115(12), 1540-1547.
[http://dx.doi.org/10.1038/bjc.2016.377] [PMID: 27875519]
[73]
Carter, L.; Rothwell, D.G.; Mesquita, B.; Smowton, C.; Leong, H.S.; Fernandez-Gutierrez, F.; Li, Y.; Burt, D.J.; Antonello, J.; Morrow, C.J.; Hodgkinson, C.L.; Morris, K.; Priest, L.; Carter, M.; Miller, C.; Hughes, A.; Blackhall, F.; Dive, C.; Brady, G. Molecular analysis of circulating tumor cells identifies distinct copy-number profiles in patients with chemosensitive and chemorefractory small-cell lung cancer. Nat. Med., 2017, 23(1), 114-119.
[http://dx.doi.org/10.1038/nm.4239] [PMID: 27869802]

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