Generic placeholder image

Current Radiopharmaceuticals

Editor-in-Chief

ISSN (Print): 1874-4710
ISSN (Online): 1874-4729

Review Article

State of the Art and Recent Developments of Radiopharmaceuticals for Pancreatic Neuroendocrine Tumors Imaging

Author(s): Angela Carollo*, Stefano Papi, Chiara M. Grana, Luigi Mansi and Marco Chinol

Volume 12, Issue 2, 2019

Page: [107 - 125] Pages: 19

DOI: 10.2174/1874471012666190306104450

Price: $65

Abstract

Background: Neuroendocrine Tumors (NETs) are relatively rare tumors, mainly originating from the digestive system, that tend to grow slowly and are often diagnosed when metastasised. Surgery is the sole curative option but is feasible only in a minority of patients. Among them, pancreatic neuroendocrine tumors (pancreatic NETs or pNETs) account for less than 5% of all pancreatic tumors. Viable therapeutic options include medical treatments such as biotherapies and more recently Peptide Receptor Radionuclide Therapies (PRRT) with radiolabeled somatostatin analogues. Molecular imaging, with main reference to PET/CT, has a major role in patients with pNETs.

Objective: The overexpression of specific membrane receptors, as well as the ability of cells to take up amine precursors in NET, have been exploited for the development of specific targeting imaging agents.

Methods: SPECT/CT and PET/CT with specific isotopes such as [68Ga]-1,4,7,10-tetra-azacyclododecane- N,N’,N’’,N’’’-tetra-acetic acid (DOTA)-somatostatin analogs, [18F]-FDG and [18F]-fluorodopa have been clinically explored.

Results: To overcome the limitations of SSTR imaging, interesting improvements are connected with the availability of new radiotracers, activating with different mechanisms compared to somatostatin analogues, such as glucagon-like peptide 1 receptor (GLP-1 R) agonists or antagonists.

Conclusion: This paper shows an overview of the RPs used so far in the imaging of pNETs with insight on potential new radiopharmaceuticals currently under clinical evaluation.

Keywords: Neuroendocrine tumors, radionuclide therapies, PET/CT, pancreas, imaging, radiopharmaceuticals.

Next »
Graphical Abstract
[1]
Falconi, M.; Eriksson, B. Kaltsa,s G.; Bartsch, D.K.; Capdevila, J.; Caplin, M.; Kos-Kudla, B.; Kwekkeboom, D.; Rindi, G.; Klöppel, G.; Reed, N.; Kianmanesh, R.; Jensen, R.T. ENETS consensus guidelines update for the management of patients with functional pancreatic neuroendocrine tumors and nonfunctional pancreatic neuroendocrine tumors. Neuroendocrinology, 2016, 103, 153-171.
[2]
Klimstra, D.S.; Modlin, I.R.; Coppola, D.; Lloyd, R.V.; Suster, S. The pathologic classification of neuroendocrine tumors: A review of nomenclature, grading, and staging systems. Pancreas, 2010, 39(6), 707-712.
[3]
Li, X.; Gou, S.; Liu, Z.; Ye, Z.; Wang, C. Assessment of the American Joint commission on cancer 8th edition staging system for patients with pancreatic neuroendocrine tumors: A surveillance, epidemiology, and end results analysis.Cancer Med; , 2018, 7, pp. (3)626-634.
[4]
Halfdanarson, T.R.; Rabe, K.G.; Rubin, J.; Petersen, G.M. Pancreatic neuroendocrine tumors (PNETs): Incidence, prognosis and recent trend toward improved survival. Ann. Oncol., 2008, 19, 1727-1733.
[5]
ENETS consensus guidelines for the standards of care in neuroendocrine tumors: Radiological, nuclear medicine & hybrid imaging. Neuroendocrinology, 2017, 105(3), 212-244.
[6]
Lloyd, R.V.; Osamura, R.Y.; Klöppel, G.; Rosai, J. WHO classification of tumours of endocrine organs. WHO Classification of Tumours, (4th Edition. ) Volume 10
[7]
Ahlstrom, H.; Eriksson, B.; Bergstrom, M.; Bjurling, P.; Langstrom, B.; Oberg, K. Pancreatic neuroendocrine tumors: Diagnosis with PET. Radiology, 1995, 195(2), 333-337.
[8]
Baumann, T.; Rottenburger, C.; Nicolas, G.; Wild, D. Gastroenteropancreatic neuroendocrine tumors (GEP-NET)- Imaging and staging. Best Pract. Res. Clin. Endocrinol. Metab., 2016, 45-57.
[9]
Fani, M. Kolenc, Peitl, P.; Velikyan, I. Current status of radiopharmaceuticals for the theranostics of neuroendocrine neoplasms. Pharmaceuticals, 2017, 10, 30.
[10]
Deroose, C.M.; Hindié, E.; Kebebew, E.; Goichot, B.; Pacak, K.; Taïeb, D.; Imperiale, A. Molecular imaging of gastroenteropancreatic neuroendocrine tumors: Current status and future directions. J. Nucl. Med., 2016, 57, 1949-1956.
[11]
Fani, M. Current and future radiopharmaceuticals in neuroendocrine tumor imaging.Chapter 7; 141-162, in: K. Pacak, D. Taïeb (eds.) . Diagnostic and Therapeutic Nuclear Medicine for Neuroendocrine Tumors.Contemporary Endocrinology; Springer, 2017.
[12]
D’Herbomez, M.; Coppin, L.; Bauters, C.; Rouaix-Emery, N.; Carnaille, B.; Do Cao, C. Biomarkers of neuroendocrine tumors. Ann. Biol. Clin. (Paris), 2016, 74(6), 669-679.
[13]
Liu, I.H.; Kunz, P.L. Biologics in gastrointestinal and pancreatic neuroendocrine tumors. J. Gastrointest. Oncol., 2017, 8(3), 457-465.
[14]
Reubi, J.C.; Waser, B.; Schaer, J.C.; Laissue, J.A. Somatostatin receptor sst1-sst5 expression in normal and neoplastic human tissues using receptor autoradiography with subtype-selective ligands. Eur. J. Nucl. Med., 2001, 28(7), 836-846.
[15]
Schaer, J.C.; Waser, B.; Mengod, G.; Reubi, J.C. Somatostatin receptor subtypes sst1, sst2, sst3 and sst5 expression in human pituitary, gastroentero-pancreatic and mammary tumors: Comparison of mRNA analysis with receptor autoradiography. Int. J. Cancer, 1997, 70(5), 530-537.
[16]
Riesen, A.; Zehnder, M. Kaden, T.A. Metal complexes of Macrocyclic Ligands. Institut fur anorganische Chemie der Universitat Basel, Basel, 1986. Helvetica Chimica ACTA, 1986, 69, 2067-2073.
[17]
Korner, M.; Christ, E.; Wild, D.; Reubi, J.C. Glucagon-like peptide-1 receptor overexpression in cancer and its impact on clinical applications. Front. Endocrinol. (Lausanne), 2012, 3, 158.
[18]
Korner, M.; Stockli, M.; Waser, B.; Reubi, J.C. GLP-1 receptor expression in human tumors and human normal tissues: Potential for in vivo targeting. J. Nucl. Med., 2007, 48, 736-743.
[19]
Wild, D.; Christ, E.; Caplin, M.E.; Kurzawinski, T.R.; Forrer, F.; Brändle, M.; Seufert, J.; Weber, W.A.; Bomanji, J.; Perren, A.; Ell, P.J.; Reubi, J.C. Glucagon-like peptide-1 versus somatostatin receptor targeting reveals 2 distinct forms of malignant insulinomas. J. Nucl. Med., 2011, 52, 1073-1078.
[20]
Deroose, C.M.; Hindié, E.; Kebebew, E.; Goichot, B.; Pacak, K.; Taïeb, D.; Imperiale, A. Molecular imaging of gastroenteropancreatic neuroendocrine tumors: Current status and future directions. J. Nucl. Med., 2016, 57, 1949-1956.
[21]
Krenning, E.P.; Kwekkeboom, D.J.; Bakker, W.H.; Breeman, W.A.P.; Kooij, P.P.M.; Oei, H.Y.; van Hagen, M.; Postema, P.T.E.; de Jong, M.; Reubi, J.C.; Visser, T.J.; Reijs, A.E.M.; Hofland, L.J.; Koper, J.W.; Lamberts, S.W.J. Somatostatin receptor scintigraphy with [111In-DTPA-D-Phe1]- and [123I-Tyr3]-octreotide: the Rotterdam experience with more than 1000 patients. Eur. J. Nucl. Med., 1993, 20, 716-731.
[22]
Bakker, W.H.; Krenning, E.P.; Breeman, W.A.R.; Kooij, P.P.M.; Reubi, J-C.; Koper, J.W.; de Jong, M.; Lameris, J.S.; Visser, T.J.; Lamberts, S.W.J. In vivo use of a radioiodinated somatostatin analogue: dynamics, metabolism and binding to somatostatin receptor-positive turnouts in man. J. Nucl. Med., 1991, 32, 1184-1189.
[23]
Krenning, E.P.; Bakker, W.H.; Kooij, P.P.M.; Breeman, W.A.R.; Oei, H.Y.; de Jong, M.; Reubi, J-C.; Visser, T.J.; Bruns, C.; Kwekkeboom, D.J.; Reijs, A.E.M.; van Hagen, P.M.; Koper, J.W.; Lamberts, S.W.J. Somatostatin receptor scintigraphy with [111In-DTPA-D-PHE1] - octreotide in man: metabolism, dosimetry and comparison with [123I-Tyr-3-]-octreotide. J. Nucl. Med., 1992, 33, 652-658.
[24]
Forrer, F.; Uusijarvi, H.; Waldherr, C.; Cremonesi, M.; Bernhardt, P.; Mueller-Brand, J.; Maecke, H.R. A comparison of (111)In-DOTATOC and (111)In-DOTATATE: biodistribution and dosimetry in the same patients with metastatic neuroendocrine tumours. Eur. J. Nucl. Med. Mol. Imaging, 2004, 31(9), 1257-1262.
[25]
Kjaer, A.; Knigge, U. Use of radioactive substances in diagnosis and treatment of neuroendocrine tumors. Scand. J. Gastroenterol., 2015, 50(6), 740-747.
[26]
Ezziddin, S.; Logvinski, T.; Yong-Hing, C.; Ahmadzadehfar, H.; Fischer, H.P.; Palmedo, H.; Bucerius, J.; Reinhardt, M.J.; Biersack, H.J. Factors Predicting Tracer Uptake in Somatostatin Receptor and MIBG Scintigraphy of Metastatic Gastroenteropancreatic Neuroendocrine Tumors. J. Nucl. Med., 2006, 47, 223-233.
[27]
Decristoforo, C.; Mather, S.J.; Cholewinski, W.; Donnemiller, E.; Riccabona, G.; Moncayo, R. 99mTc-EDDA/HYNIC-TOC: a new 99mTc-labelled radiopharmaceutical for imaging somatostatin receptor-positive tumors; first clinical results and intra-patient comparison with 111In-labelled octreotide derivatives. Eur. J. Nucl. Med., 2000, 27(9), 1318-1325.
[28]
Qiao, Z.; Zhang, J.; Jin, X.; Huo, L.; Zhu, Z.; Xing, H.; Li, F. 99mTc-HYNIC-TOC imaging in the evaluation of pancreatic masses which are potential neuroendocrine tumor. Clin. Nucl. Med., 2015, 40(5), 397-400.
[29]
Gabriel, M.; Decristoforo, C.; Donnemiller, E.; Ulmer, H.; Watfah Rychlinski, C.; Mather, S.J.; Moncayo, R. An Intrapatient Comparison of 99mTc-EDDA/HYNIC-TOC with 111In-DTPA-Octreotide for diagnosis of somatostatin receptor-expressing tumors. J. Nucl. Med., 2003, 44, 708-716.
[30]
Frilling, A.; Sotiropoulos, G.C.; Radtke, A.; Malago, M.; Bockisch, A.; Kuehl, H.; Li, J.; Broelsch, C.E. 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.
[31]
Reubi, J.C.; Schar, J.C.; Waser, B.; Heppeler, A.; Schmitt, J.S.; Mäcke, H.R. Affinity profiles for human somatostatin receptor subtypes SST1-SST5 of somatostatin radiotracers selected for scintigraphic and radiotherapeutic use. Eur. J. Nucl. Med., 2000, 27, 273-282.
[32]
Bodei, L.; Ambrosini, V.; Herrmann, K.; Modlin, I. Current concepts in 68Ga-DOTATATE imagin of neuroendocrine neoplasms: Interpretation, biodistribution, dosimetry and molecular strategies. J. Nucl. Med., 2017, 58, 1718-1726.
[33]
Kabasakal, L.; Demirci, E.; Ocak, M.; Decristoforo, C.; Araman, A.; Ozsoy, Y.; Uslu, I.; Kanmaz, B. Comparison of 68Ga-DOTATATE and 68Ga-DOTANOC PET/CT imaging in the same patient group with neuroendocrine tumours. Eur. J. Nucl. Med. Mol. Imaging, 2012, 39, 1271-1277.
[34]
Poeppel, T.D.; Binse, I.; Petersenn, S.; Lahner, H.; Schott, M.; Antoch, G.; Brandau, W.; Bockisch, A.; Boy, C. 68Ga-DOTATOC versus 68Ga-DOTATATE PET/CT in functional imaging of neuroendocrine tumors. J. Nucl. Med., 2011, 52, 1864-1870.
[35]
Buchmann, I.; Henze, M.; Engelbrecht, S.; Eisenhut, M.; Runz, A.; Schäfer, M.; Schilling, T.; Haufe, S.; Herrmann, T.; Haberkorn, U. Comparison of 68Ga-DOTATOC PET and 111In-DTPAOC (Octreoscan) SPECT in patients with neuroendocrine tumors. Eur. J. Nucl. Med. Mol. Imaging, 2007, 34, 1617-1626.
[36]
Ruf, J.; Heuck, F.; Schiefer, J.; Denecke, T.; Elgeti, F.; Pascher, A.; Pavel, M.; Stelter, L.; Kropf, S.; Wiedenmann, B.; Amthauer, H. Impact of multiphase 68Ga-DOTATOC-PET/CT on therapy management in patients with neuroendocrine tumors. Neuroendocrinology, 2010, 91, 101-109.
[37]
Naswa, N.; Sharma, P.; Gupta, S.K.; Karunanithi, S.; Reddy, R.M.; Patnecha, P.; Lata, S.; Kumar, R. Dual tracer functional imaging of gastroenteropancreatic neuroendocrine tumors using 68Ga-DOTA-NOC PET-CT and 18F-FDG PET-CT: Competitive or complementary? Clin. Nucl. Med., 2014, 39, e27-e34.
[38]
Ginj, M.; Zhang, H.; Waser, B.; Cescato, R.; Wild, D.; Wang, X.; Erchegyi, J.; Rivier, J.; Mäcke, H.R.; Reubi, J.C. Radiolabeled somatostatin receptor antagonists are preferable to agonists for in vivo peptide receptor targeting of tumors. PNAS, 2006, 103 16436±41
[39]
Abiraj, K.; Mansi, R.; Tamma, M.L.; Fani, M.; Forrer, F.; Nicolas, G.; Cescato, R.; Reubi, J.C.; Maecke, H.R. Bombesin antagonist-based radioligands for translational nuclear imaging of gastrin-releasing peptide receptor-positive tumors. J. Nucl. Med., 2011, 52, 1970-1978.
[40]
Fani, M.; Nicolas, G.P.; Wild, D. Somatostatin receptor antagonists for imaging and therapy. J. Nucl. Med., 2017, 58, 61S-66S.
[41]
Wild, D.; Fani, M.; Fischer, R.; Del Pozzo, L.; Kaul, F.; Krebs, S.; Fischer, R.; Rivier, J.E.; Reubi, J.C.; Maecke, H.R.; Weber, W.A. Comparison of somatostatin receptor agonist and antagonist for peptide receptor radionuclide therapy: A pilot study. J. Nucl. Med., 2014, 55, 1248-1252.
[42]
Wild, D.; Fani, M.; Behe, M.; Brink, I.; Rivier, J.E.; Reubi, J.C.; Maecke, H.R.; Weber, W.A. First clinical evidence that imaging with somatostatin receptor antagonists is feasible. J. Nucl. Med., 2011, 52, 1412-1417.
[43]
Garin, E.; Le Jeune, F.; Devillers, A.; Cuggia, M.; de Lajarte-Thirouard, A.S.; Bouriel, C.; Boucher, E.; Raoul, J.L. Predictive value of 18F-FDG PET and somatostatin receptor scintigraphy in patients with metastatic endocrine tumors. J. Nucl. Med., 2009, 50, 858-864.
[44]
Has Simsek, D.; Kuyumcu, S.; Turkmen, C.; Sanlı, Y.; Aykan, F.; Unal, S.; Adalet, I. Can complementary 68Ga-DOTATATE and 18F-FDG PET/CT establish the missing link between histopathology and therapeutic approach in gastroenteropancreatic neuroendocrine tumors? J. Nucl. Med., 2014, 55, 1811-1817.
[45]
Heiss, W.D.; Wienhard, K.; Wagner, R.; Lanfermann, H.; Thiel, A.; Herholz, K.; Pietrzyk, U. F-Dopa as an amino acid tracer to detect brain tumors. J. Nucl. Med., 1996, 37(7), 1180-1182.
[46]
Tessonnier, L.; Sebag, F.; Ghander, C.; De Micco, C.; Reynaud, R.; Palazzo, F.F.; Conte-Devolx, B.; Henry, J.F.; Mundler, O.; Taïeb, D. Limited value of 18F-F-DOPA PET to localize pancreatic insulin-secreting tumors in adults with hyperinsulinemic hypoglycemia. J. Clin. Endocrinol. Metab., 2010, 95, 303-307.
[47]
Schiesser, M.; Veit-Haibach, P.; Muller, M.K.; Weber, M.; Bauerfeind, P.; Hany, T.; Clavien, P.A. Value of combined 6-[18F]fluorodihydroxyphenylalanine PET/CT for imaging of neuroendocrine tumours. Br. J. Surg., 2010, 97(5), 691-697.
[48]
Ambrosini, V.; Tomassetti, P.; Castellucci, P.; Campana, D.; Montini, G.; Rubello, D.; Nanni, C.; Rizzello, A.; Franchi, R.; Fanti, S. Comparison between 68Ga-DOTA-NOC and 18F-DOPA PET for the detection of gastro-entero-pancreatic and lung neuro-endocrine tumours. Eur. J. Nucl. Med. Mol. Imaging, 2008, 35(8), 1431-1438.
[49]
Ambrosini, V.; Rubello, D.; Nanni, C.; Al-Nahhas, A.; Fanti, S. 68Ga-DOTA-peptides versus 18F-DOPA PET for the assessment of NET patients. Nucl. Med. Commun., 2008, 29(5), 415-417.
[50]
Haug, A.; Auernhammer, C.J.; Wängler, B.; Tiling, R.; Schmidt, G.; Göke, B.; Bartenstein, P.; Pöpperl, G. Intraindividual comparison of 68Ga-DOTA-TATE and 18F-DOPA PET in patients with well-differentiated metastatic neuroendocrine tumours. Eur. J. Nucl. Med. Mol. Imaging, 2009, 36, 765-770.
[51]
Kratochwil, C.; Stefanova, M.; Mavriopoulou, E.; Holland-Letz, T.; Dimitrakopoulou-Strauss, A.; Afshar-Oromieh, A.; Mier, W.; Haberkorn, U.; Giesel, F.L. SUV of [68Ga]-DOTATOC PET/CT predicts response probability of PRRT in neuroendocrine tumors. Mol. Imaging Biol., 2015, 17, 313-318.
[52]
Haug, A.R.; Auernhammer, C.J.; Wängler, B.; Schmidt, G.P.; Uebleis, C.; Göke, B.; Cumming, P.; Bartenstein, P.; Tiling, R.; Hacker, M. 68Ga-DOTATATE PET/CT for the early prediction of response to somatostatin receptor-mediated radionuclide therapy in patients with well-differentiated neuroendocrine tumors. J. Nucl. Med., 2010, 51, 1349-1356.
[53]
Partelli, S.; Bertani, E.; Bartolomei, M.; Perali, C.; Muffatti, F.; Grana, C.M. Schiavo, Lena, M.; Doglioni, C.; Crippa, S.; Fazio, N.; Zamboni, G.; Falconi, M. Peptide receptor radionuclide therapy as neoadjuvant therapy for resectable or potentially resectable pancreatic neuroendocrine neoplasms. Surgery, 2018, 163(4), 761-767.
[54]
Wessels, B.W.; Meares, C.F. Physical and Chemical Properties of Radionuclide Therapy. Semin. Radiat. Oncol., 2000, 110(2), 115-122.
[55]
Gulenchyn, K.Y.; Yaoy, X.; Asa, S.L.; Singh, S.; Law, C. Radionuclide Therapy in Neuroendocrine Tumours: A Systematic Review. Clin. Oncol., 2012, 24, 294-308.
[56]
Krenning, E.P.; Kwekkeboom, D.J.; Bakker, W.H.; Breeman, W.A.; Kooij, P.P.; Oei, H.Y.; van Hagen, M.; Postema, P.T.; de Jong, M.; Reubi, J.C.; Visser, T.J.; Reijs, A.E.M.; Holland, L.J.; Koper, J.W.; Lamberts, S.W.J. Somatostatin receptor scintigraphy with [111In-DTPA-D-Phe1]- and [123I-Tyr3]-octreotide: the Rotterdam experience with more than 1000 patients. Eur. J. Nucl. Med., 1993, 20(8), 716-731.
[57]
Nicolas, G.; Giovacchini, G.; Müller-Brand, J.; Forrer, F. Targeted Radiotherapy with Radiolabeled Somatostatin Analogs. Endocrinol. Metab. Clin. North Am., 2011, 40, 187-204.
[58]
Limouris, G.S.; Poulantzas, V.; Trompoukis, N.; Karfis, I.; Chondrogiannis, S.; Triantafyllou, N.; Gennimata, V.; Moulopoulou, L.E.; Patsouris, E.; Nikou, G.; Michalaki, V.; Fragulidis, G.; Paphiti, M.; McCready, R.V.; Colletti, P.M.; Cook, G.J.; Rubello, D. Comparison of 111In-[DTPA0]Octreotide Versus Non Carrier Added 177Lu-[DOTA0,Tyr3]-Octreotate Efficacy in Patients With GEP-NET Treated Intra-arterially for Liver Metastases. Clin. Nucl. Med., 2016, 41(3), 194-200.
[59]
Ozkan, E.; Tokmak, E.; Kucuk, N.O. Efficacy of adding high-dose In-111 octreotide therapy during Sandostatin treatment in patients with disseminated neuroendocrine tumors: Clinical results of 14 patients. Ann. Nucl. Med., 2011, 25(6), 425-4231.
[60]
De Jong, M.; Valkema, R.; Jamar, F.; Kvols, L.K.; Kwekkeboom, D.J.; Breeman, W.A.; Bakker, W.H.; Smith, C.; Pauwels, S.; Krenning, E.P. Somatostatin receptor-targeted radionuclide therapy of tumors: preclinical and clinical findings. Semin. Nucl. Med., 2002, 32, 133-140.
[61]
Kwekkeboom, D.J.; Mueller-Brand, J.; Paganelli, G.; Anthony, L.B.; Pauwels, S.; Kvols, L.K.; O’dorisio, T.M.; Valkema, R.; Bodei, L.; Chinol, M.; Maecke, H.R.; Krenning, E.P. An overview of the results of peptide receptor radionuclide therapy with 3 different radiolabelled somatostatin analogues. J. Nucl. Med., 2005, 46, 62S-66S.
[62]
Cremonesi, M.; Botta, F.; Di Dia, A.; Ferrari, M.; Bodei, L.; De Cicco, C.; Rossi, A.; Bartolomei, M.; Mei, R.; Severi, S.; Salvatori, M.; Pedroli, G.; Paganelli, G. Dosimetry for treatment with radiolabelled somatostatin analogues. A review. Q. J. Nucl. Med. Mol. Imaging, 2010, 54, 37-51.
[63]
Valkema, R.; Pauwels, S.A.; Kvols, L.K.; Kwekkeboom, D.J. jamar, F. de Jong, M.; Barone, R.; Walrand, S.; Kooij, P.P.; Bakker, W.H.; Lasher, J.; Krenning, E.P. Long term follow-up of renal function after peptide receptor radiation therapy with (90)Y-DOTA(0),Tyr(3)-octreotide and (177)Lu-DOTA(0), Tyr(3)-octreotate. J. Nucl. Med., 2005, 46(Suppl. 1), 83S-91S.
[64]
Bodei, L.; Cremonesi, M.; Zoboli, S.; Grana, C.M.; Bartolomei, M.; Rocca, P.; Caracciolo, M.; Mäcke, H.R.; Chinol, M.; Paganelli, G. Receptor-mediated radionuclide therapy with 90Y-DOTATOCin association with amino acid infusion: A phase I study. Eur. J. Nucl. Med., 2003, 30, 207-216.
[65]
Bodei, L.; Cremonesi, M.; Ferrari, M.; Pacifici, M.; Grana, C.M.; Bartolomei, M.; Baio, S.M.; Sansovini, M.; Paganelli, G. Long term evaluation of renal toxicitiy after peptide receptor radionuclide therapy with 90Y-DOTATOC and 177Lu-DOTATATE: The role of associated risk factors. Eur. J. Nucl. Med. Mol. Imaging, 2008, 35(10), 1847-1856.
[66]
Imhof, A.; Brunner, P.; Marincek, N.; Briel, M.; Schindler, C.; Rasch, H.; Mäcke, H.R.; Rochlitz, C.; Müller-Brand, J.; Walter, M.A. 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.
[67]
Sansovini, M.; Severi, S.; Ambrosetti, A.; Monti, M.; Nanni, O.; Sarnelli, A.; Bodei, L.; Garaboldi, L.; Bartolomei, M.; Paganelli, G. Treatment with the radiolabelled somatostatin analog Lu-DOTATATE for advanced pancreatic neuroendocrine tumors. Neuroendocrinology, 2013, 97, 347-354.
[68]
Ezziddin, S.; Khalaf, F.; Vanezi, M.; Haslerud, T.; Mayer, K.; Al Zreiqat, A.; Willinek, W.; Biersack, H.J.; Sabet, A. Outcome of peptide receptor radionuclide therapy with 177Lu-octreotate in advanced grade 1/2 pancreatic neuroendocrine tumors. Eur. J. Nucl. Med. Mol. Imaging, 2014, 41, 925-933.
[69]
Eng, J.; Kleinman, W.A.; Singh, L.; Singh, G.; Raufman, J.P. Isolation and characterization of exendin-4, an exendin-3 analogue, from Heloderma suspectum venom. Further evidence for an exendin receptor on dispersed acini from guinea pig pancreas. J. Biol. Chem., 1992, 267(11), 7402-7405.
[70]
Kratochwil, C.; Giesel, F.L. Nuklearmedizinische therapie endokriner tumoren. Der Radiologe, 2014, 1-9.
[71]
Wild, D.; Mäcke, H.; Gloor, B.; Reubi, J.C. Glucagon-like peptide 1-receptor scans to localize occult insulinomas. N. Engl. J. Med., 2008, 14, 359(7), 766-768.
[72]
Christ, E.; Wild, D.; Forrer, F.; Brandle, M.; Sahli, R.; Clerici, T.; Gloor, B.; Martius, F.; Maecke, H.; Reubi, J.C. Glucagon-like peptide-1 receptor imaging for localization of insulinomas. J. Clin. Endocrinol. Metab., 2009, 94(11), 4398-4405.
[73]
Christ, E.; Wild, D.; Ederer, S.; Behe, M.; Nicolas, G.; Caplin, M.E.; Brändle, M.; Clerici, T.; Fischli, S.; Stettler, C.; Ell, P.J.; Seufert, J.; Gloor, B.; Perren, A.; Reubi, J.C.; Forrer, F. Glucagon-like peptide-1 receptor imaging for the localisation of insulinomas: a prospective multicentre imaging study. Lancet Diabetes Endocrinol., 2013, 1(2), 115-122.
[74]
Sowa-Staszczak, A.; Pach, D.; Mikolajczak, R.; Mäcke, H.; Jabrocka-Hybel, A.; Stefańska, A.; Tomaszuk, M.; Janota, B.; Gilis-Januszewska, A.; Małecki, M.; Kamiński, G.; Kowalska, A.; Kulig, J.; Matyja, A.; Osuch, C.; Hubalewska-Dydejczyk, A. Glucagon-like peptide-1 receptor imaging with [Lys40(Ahx-HYNIC-99mTc/EDDA)NH2]-exendin-4 for the detection of insulinoma. Eur. J. Nucl. Med. Mol. Imaging, 2013, 40, 524-531.
[75]
Eriksson, O.; Velikyan, I.; Selvaraju, R.K.; Kandeel, F.; Johansson, L.; Antoni, G.; Eriksson, B.; Sörensen, J.; Korsgren, O. Detection of metastatic insulinoma by positron emission tomography with [(68)Ga]exendin-4. A case report. J. Clin. Endocrinol. Metab., 2014, 99, 1519-1524.
[76]
Antwi, K.; Fani, M.; Nicolas, G.; Rottenburger, C.; Heye, T.; Reubi, J.C.; Gloor, B.; Christ, E.; Wild, D. Localization of hidden insulinomas with 68Ga-DOTA-Exendin-4 PET/CT: A pilot study. J. Nucl. Med., 2015, 56, 1075-1078.
[77]
Antwi, K.; Fani, M.; Nicolas, G.; Rottenburger, C.; Heye, T.; Reubi, J.C.; Gloor, B.; Christ, E.; Wild, D. Localization of hidden insulinomas with (68)Ga-DOTA-Exendin-4 PET/CT: A Pilot Study. J. Nucl. Med., 2015, 56(7), 1075-1078.
[78]
Bauman, A. Valverde, I.E.; Fischer, C.A.; Vomstein, S.; Mindt T.L. Development of 68Ga- and 89Zr-Labeled Exendin-4 as Potential Radiotracers for the Imaging of Insulinomas by PET. J. Nucl. Med., 2015, 56, 1569-1574.
[79]
Goke, R.; Fehmann, H.C.; Linn, T.; Schmidt, H.; Krause, M.; Eng, J.; Göke, B. Exendin-4 is a high potency agonist and truncated exendin-(9±39)-amide an antagonist at the glucagon-like peptide 1-(7±36)-amide receptor of insulin-secreting beta-cells. J. Biol. Chem., 1993, 268, 19650-1965.
[80]
Vaidyanathan, G.; Zalutsky, M.R. Protein radiohalogenation: observations on the design of N-succinimidyl ester acylation agents. Bioconjug. Chem., 1990, 1, 269-273.
[81]
Lappchen, T.; Tonnesmann, R.; Eersels, J.; Meyer, P.T.; Maecke, H.R.; Rylova, S.N. Radioiodinated Exendin-4 Is Superior to the Radiometal-Labelled Glucagon-Like Peptide-1 Receptor Probes Overcoming Their High Kidney Uptake. PLoS One, 2017, 12(1), 1-16.

Rights & Permissions Print Cite
© 2024 Bentham Science Publishers | Privacy Policy