Treatment of Neuroendocrine Neoplasms with Radiolabeled Peptides—Where Are We Now
Abstract
:Simple Summary
Abstract
1. Introduction
2. Somatostatin Receptor Imaging
3. Peptide Receptor Radiotherapy: From 111In to 177Lu
4. Current Therapeutic Considerations with 177Lu-DOTATATE
5. Future Directions for PRRT
6. Conclusions
Author Contributions
Funding
Conflicts of Interest
References
- Rosai, J. The origin of neuroendocrine tumors and the neural crest saga. Mod. Pathol. 2011, 24 (Suppl. S2), S53–S57. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Oronsky, B.; Ma, P.C.; Morgensztern, D.; Carter, C.A. Nothing But NET: A Review of Neuroendocrine Tumors and Carcinomas. Neoplasia 2017, 19, 991–1002. [Google Scholar] [CrossRef] [PubMed]
- Sackstein, P.E.; O’Neil, D.S.; Neugut, A.I.; Chabot, J.; Fojo, T. Epidemiologic trends in neuroendocrine tumors: An examination of incidence rates and survival of specific patient subgroups over the past 20 years. Semin. Oncol. 2018, 45, 249–258. [Google Scholar] [CrossRef]
- Walenkamp, A.; Crespo, G.; Fierro Maya, F.; Fossmark, R.; Igaz, P.; Rinke, A.; Tamagno, G.; Vitale, G.; Öberg, K.; Meyer, T. Hallmarks of gastrointestinal neuroendocrine tumours: Implications for treatment. Endocr. Relat. Cancer 2014, 21, R445–R4460. [Google Scholar] [CrossRef] [PubMed]
- Capella, C.; Heitz, P.U.; Höfler, H.; Solcia, E.; Klöppel, G. Revised classification of neuroendocrine tumours of the lung, pancreas and gut. Virchows Arch. 1995, 425, 547–560. [Google Scholar] [CrossRef]
- Williams, E.D.; Sandler, M. The classification of carcinoid tum ours. Lancet 1963, 1, 238–239. [Google Scholar] [CrossRef]
- 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, 707–712. [Google Scholar] [CrossRef]
- Rindi, G.; Klöppel, G.; Alhman, H.; Caplin, M.; Couvelard, A.; de Herder, W.W.; Erikssson, B.; Falchetti, A.; Falconi, M.; Komminoth, P.; et al. TNM staging of foregut (neuro)endocrine tumors: A consensus proposal including a grading system. Virchows Arch. 2006, 449, 395–401. [Google Scholar] [CrossRef] [Green Version]
- Cavalcanti, M.S.; Gönen, M.; Klimstra, D.S. The ENETS/WHO grading system for neuroendocrine neoplasms of the gastroenteropancreatic system: A review of the current state, limitations and proposals for modifications. Int. J. Endocr. Oncol. 2016, 3, 203–219. [Google Scholar] [CrossRef]
- Amin, M.; Edge, S.; Greene, F.; Byrd, D.; Brookland, R.; Washington, K.M.; Gershenwald, J.; Compton, C.; Hess, K.; Sullivan, D.; et al. AJCC Cancer Staging Manual, 8th ed.; Springer International Publishing: Berlin/Heidelberg, Germany, 2017; ISBN 978-3-319-40617-6. [Google Scholar]
- Papotti, M.; Bongiovanni, M.; Volante, M.; Allìa, E.; Landolfi, S.; Helboe, L.; Schindler, M.; Cole, S.; Bussolati, G. Expression of somatostatin receptor types 1–5 in 81 cases of gastrointestinal and pancreatic endocrine tumors. Virchows Arch. 2002, 440, 461–475. [Google Scholar] [CrossRef]
- Kulaksiz, H.; Eissele, R.; Rössler, D.; Schulz, S.; Höllt, V.; Cetin, Y.; Arnold, R. Identification of somatostatin receptor subtypes 1, 2A, 3, and 5 in neuroendocrine tumours with subtype specific antibodies. Gut 2002, 50, 52–60. [Google Scholar] [CrossRef] [PubMed]
- Cakir, M.; Dworakowska, D.; Grossman, A. Somatostatin receptor biology in neuroendocrine and pituitary tumours: Part 1—Molecular pathways. J. Cell. Mol. Med. 2010, 14, 2570–2584. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Stueven, A.K.; Kayser, A.; Wetz, C.; Amthauer, H.; Wree, A.; Tacke, F.; Wiedenmann, B.; Roderburg, C.; Jann, H. Somatostatin Analogues in the Treatment of Neuroendocrine Tumors: Past, Present and Future. Int. J. Mol. Sci. 2019, 20, 49. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Caplin, M.E.; Pavel, M.; Ćwikła, J.B.; Phan, A.T.; Raderer, M.; Sedláčková, E.; Cadiot, G.; Wolin, E.M.; Capdevila, J.; Wall, L.; et al. Lanreotide in metastatic enteropancreatic neuroendocrine tumors. N. Engl. J. Med. 2014, 371, 224–233. [Google Scholar] [CrossRef] [PubMed]
- Reubi, J.C.; Landolt, A.M. High density of somatostatin receptors in pituitary tumors from acromegalic patients. J. Clin. Endocrinol. Metab. 1984, 59, 1148–1151. [Google Scholar] [CrossRef]
- Reubi, J.C.; Kvols, L.K.; Waser, B.; Nagorney, D.M.; Heitz, P.U.; Charboneau, J.W.; Reading, C.C.; Moertel, C. Detection of somatostatin receptors in surgical and percutaneous needle biopsy samples of carcinoids and islet cell carcinomas. Cancer Res. 1990, 50, 5969–5977. [Google Scholar]
- Krenning, E.P.; Breeman, W.A.P.; Kooij, P.P.M.; Lameris, J.S.; Bakker, W.H.; Koper, J.W.; Ausema, L.; Reubi, J.C.; Lamberts, S.W.J. Localisation of endocrine-related tumours with radioiodinated analogue of somatostatin. Lancet 1989, 333, 242–244. [Google Scholar] [CrossRef]
- Lamberts, S.W.J.; Hofland, L.E.O.J.; Van Koetsveld, P.M.; Reubi, J.-C.; Bruining, H.A.; Barker, W.H.; Krenning, E.P. Parallel in Vivo and in Vitro Detection of Functional Somatostatin Receptors in Human Endocrine Pancreatic Tumors: Consequences with Regard to Diagnosis, Localization, and Therapy. J. Clin. Endocrinol. Metab. 1990, 71, 566–574. [Google Scholar] [CrossRef]
- Lamberts, S.W.; Bakker, W.H.; Reubi, J.C.; Krenning, E.P. Somatostatin-receptor imaging in the localization of endocrine tumors. N. Engl. J. Med. 1990, 323, 1246–1249. [Google Scholar] [CrossRef]
- Lamberts, S.W.; Chayvialle, J.A.; Krenning, E.P. The visualization of gastroenteropancreatic endocrine tumors. Digestion 1993, 54 (Suppl. S1), 92–97. [Google Scholar] [CrossRef]
- 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.; et al. 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. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Al-Nahhas, A. Nuclear medicine imaging of neuroendocrine tumours. Clin. Med. 2012, 12, 377–380. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Hofmann, M.; Maecke, H.; Börner, A.; Weckesser, E.; Schöffski, P.; Oei, M.; Schumacher, J.; Henze, M.; Heppeler, A.; Meyer, G.; et al. Biokinetics and imaging with the somatostatin receptor PET radioligand 68Ga-DOTATOC: Preliminary data. Eur. J. Nucl. Med. 2001, 28, 1751–1757. [Google Scholar] [CrossRef] [PubMed]
- Gabriel, M.; Decristoforo, C.; Kendler, D.; Dobrozemsky, G.; Heute, D.; Uprimny, C.; Kovacs, P.; Von Guggenberg, E.; Bale, R.; Virgolini, I.J. 68Ga-DOTA-Tyr3-octreotide PET in neuroendocrine tumors: Comparison with somatostatin receptor scintigraphy and CT. J. Nucl. Med. 2007, 48, 508–518. [Google Scholar] [CrossRef] [PubMed]
- Johnbeck, C.B.; Knigge, U.; Kjær, A. PET tracers for somatostatin receptor imaging of neuroendocrine tumors: Current status and review of the literature. Future Oncol. 2014, 10, 2259–2277. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Antunes, P.; Ginj, M.; Zhang, H.; Waser, B.; Baum, R.P.; Reubi, J.C.; Maecke, H. Are radiogallium-labelled DOTA-conjugated somatostatin analogues superior to those labelled with other radiometals? Eur. J. Nucl. Med. Mol. Imaging 2007, 34, 982–993. [Google Scholar] [CrossRef] [Green Version]
- 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. [Google Scholar] [CrossRef] [Green Version]
- Sandström, M.; Velikyan, I.; Garske-Román, U.; Sörensen, J.; Eriksson, B.; Granberg, D.; Lundqvist, H.; Sundin, A.; Lubberink, M. Comparative biodistribution and radiation dosimetry of 68Ga-DOTATOC and 68Ga-DOTATATE in patients with neuroendocrine tumors. J. Nucl. Med. 2013, 54, 1755–1759. [Google Scholar] [CrossRef] [Green Version]
- Ambrosini, V.; Fani, M.; Fanti, S.; Forrer, F.; Maecke, H.R. Radiopeptide imaging and therapy in Europe. J. Nucl. Med. 2011, 52 (Suppl. S2), 42S–55S. [Google Scholar] [CrossRef] [Green Version]
- Reubi, J.C.; Schär, J.-C.; Waser, B.; Wenger, S.; 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. [Google Scholar] [CrossRef]
- Yang, J.; Kan, Y.; Ge, B.H.; Yuan, L.; Li, C.; Zhao, W. Diagnostic role of Gallium-68 DOTATOC and Gallium-68 DOTATATE PET in patients with neuroendocrine tumors: A meta-analysis. Acta Radiol. 2014, 55, 389–398. [Google Scholar] [CrossRef] [PubMed]
- Yu, J.; Li, N.; Li, J.; Lu, M.; Leal, J.P.; Tan, H.; Su, H.; Fan, Y.; Zhang, Y.; Zhao, W.; et al. The Correlation Between [68Ga]DOTATATE PET/CT and Cell Proliferation in Patients With GEP-NENs. Mol. Imaging Biol. 2019, 21, 984–990. [Google Scholar] [CrossRef] [PubMed]
- Partelli, S.; Rinzivillo, M.; Maurizi, A.; Panzuto, F.; Salgarello, M.; Polenta, V.; Delle Fave, G.; Falconi, M. The role of combined Ga-DOTANOC and 18FDG PET/CT in the management of patients with pancreatic neuroendocrine tumors. Neuroendocrinology 2014, 100, 293–299. [Google Scholar] [CrossRef]
- Werner, R.A.; Solnes, L.B.; Javadi, M.S.; Weich, A.; Gorin, M.A.; Pienta, K.J.; Higuchi, T.; Buck, A.K.; Pomper, M.G.; Rowe, S.P.; et al. SSTR-RADS Version 1.0 as a Reporting System for SSTR PET Imaging and Selection of Potential PRRT Candidates: A Proposed Standardization Framework. J. Nucl. Med. 2018, 59, 1085–1091. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Werner, R.A.; Derlin, T.; Rowe, S.P.; Bundschuh, L.; Sheikh, G.T.; Pomper, M.G.; Schulz, S.; Higuchi, T.; Buck, A.K.; Bengel, F.M.; et al. High Interobserver Agreement for the Standardized Reporting System SSTR-RADS 1.0 on Somatostatin Receptor PET/CT. J. Nucl. Med. 2021, 62, 514–520. [Google Scholar] [CrossRef]
- Adams, S.; Baum, R.; Rink, T.; Schumm-Dräger, P.M.; Usadel, K.H.; Hör, G. Limited value of fluorine-18 fluorodeoxyglucose positron emission tomography for the imaging of neuroendocrine tumours. Eur. J. Nucl. Med. 1998, 25, 79–83. [Google Scholar] [CrossRef]
- Belhocine, T.; Foidart, J.; Rigo, P.; Najjar, F.; Thiry, A.; Quatresooz, P.; Hustinx, R. Fluorodeoxyglucose positron emission tomography and somatostatin receptor scintigraphy for diagnosing and staging carcinoid tumours: Correlations with the pathological indexes p53 and Ki-67. Nucl. Med. Commun. 2002, 23, 727–734. [Google Scholar] [CrossRef] [PubMed]
- Binderup, T.; Knigge, U.; Loft, A.; Federspiel, B.; Kjaer, A. 18F-fluorodeoxyglucose positron emission tomography predicts survival of patients with neuroendocrine tumors. Clin. Cancer Res. Off. J. Am. Assoc. Cancer Res. 2010, 16, 978–985. [Google Scholar] [CrossRef] [Green Version]
- Bahri, H.; Laurence, L.; Edeline, J.; Leghzali, H.; Devillers, A.; Raoul, J.-L.; Cuggia, M.; Mesbah, H.; Clement, B.; Boucher, E.; et al. High prognostic value of 18F-FDG PET for metastatic gastroenteropancreatic neuroendocrine tumors: A long-term evaluation. J. Nucl. Med. 2014, 55, 1786–1790. [Google Scholar] [CrossRef] [Green Version]
- Panagiotidis, E.; Alshammari, A.; Michopoulou, S.; Skoura, E.; Naik, K.; Maragkoudakis, E.; Mohmaduvesh, M.; Al-Harbi, M.; Belda, M.; Caplin, M.E.; et al. Comparison of the impact of 68Ga-DOTATATE and 18F-FDG PET/CT on clinical management in patients with Neuroendocrine tumors. J. Nucl. Med. 2017, 58, 91–96. [Google Scholar] [CrossRef] [Green Version]
- Muffatti, F.; Partelli, S.; Cirocchi, R.; Andreasi, V.; Mapelli, P.; Picchio, M.; Gianolli, L.; Falconi, M. Combined 68Ga-DOTA-peptides and 18F-FDG PET in the diagnostic work-up of neuroendocrine neoplasms (NEN). Clin. Transl. Imaging 2019, 7, 181–188. [Google Scholar] [CrossRef]
- Niederle, B.; Pape, U.-F.; Costa, F.; Gross, D.; Kelestimur, F.; Knigge, U.; Öberg, K.; Pavel, M.; Perren, A.; Toumpanakis, C.; et al. ENETS Consensus Guidelines Update for Neuroendocrine Neoplasms of the Jejunum and Ileum. Neuroendocrinology 2016, 103, 125–138. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Falconi, M.; Eriksson, B.; Kaltsas, G.; Bartsch, D.K.; Capdevila, J.; Caplin, M.; Kos-Kudla, B.; Kwekkeboom, D.; Rindi, G.; Klöppel, G.; et al. ENETS Consensus Guidelines Update for the Management of Patients with Functional Pancreatic Neuroendocrine Tumors and Non-Functional Pancreatic Neuroendocrine Tumors. Neuroendocrinology 2016, 103, 153–171. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Abgral, R.; Leboulleux, S.; Déandreis, D.; Aupérin, A.; Lumbroso, J.; Dromain, C.; Duvillard, P.; Elias, D.; de Baere, T.; Guigay, J.; et al. Performance of 18fluorodeoxyglucose-positron emission tomography and somatostatin receptor scintigraphy for high Ki67 (≥10%) well-differentiated endocrine carcinoma staging. J. Clin. Endocrinol. Metab. 2011, 96, 665–671. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Oberg, K.; Krenning, E.; Sundin, A.; Bodei, L.; Kidd, M.; Tesselaar, M.; Ambrosini, V.; Baum, R.P.; Kulke, M.; Pavel, M.; et al. A Delphic consensus assessment: Imaging and biomarkers in gastroenteropancreatic neuroendocrine tumor disease management. Endocr. Connect. 2016, 5, 174–187. [Google Scholar] [CrossRef]
- Carideo, L.; Prosperi, D.; Panzuto, F.; Magi, L.; Pratesi, M.S.; Rinzivillo, M.; Annibale, B.; Signore, A. Role of Combined [68Ga]Ga-DOTA-SST Analogues and [18F]FDG PET/CT in the Management of GEP-NENs: A Systematic Review. J. Clin. Med. 2019, 8, 1032. [Google Scholar] [CrossRef] [Green Version]
- Krenning, E.P.; Kooij, P.P.; Bakker, W.H.; Breeman, W.A.; Postema, P.T.; Kwekkeboom, D.J.; Oei, H.Y.; de Jong, M.; Visser, T.J.; Reijs, A.E. Radiotherapy with a radiolabeled somatostatin analogue, [111In-DTPA-D-Phe1]-octreotide. A case history. Ann. N. Y. Acad. Sci. 1994, 733, 496–506. [Google Scholar] [CrossRef] [Green Version]
- Fjälling, M.; Andersson, P.; Forssell-Aronsson, E.; Grétarsdóttir, J.; Johansson, V.; Tisell, L.E.; Wängberg, B.; Nilsson, O.; Berg, G.; Michanek, A.; et al. Systemic radionuclide therapy using indium-111-DTPA-D-Phe1-octreotide in midgut carcinoid syndrome. J. Nucl. Med. 1996, 37, 1519–1521. [Google Scholar]
- Valkema, R.; De Jong, M.; Bakker, W.H.; Breeman, W.A.P.; Kooij, P.P.M.; Lugtenburg, P.J.; De Jong, F.H.; Christiansen, A.; Kam, B.L.R.; De Herder, W.W.; et al. Phase I study of peptide receptor radionuclide therapy with [In-DTPA]octreotide: The Rotterdam experience. Semin. Nucl. Med. 2002, 32, 110–122. [Google Scholar] [CrossRef]
- Bodei, L.; Kwekkeboom, D.J.; Kidd, M.; Modlin, I.M.; Krenning, E.P. Radiolabeled Somatostatin Analogue Therapy Of Gastroenteropancreatic Cancer. Semin. Nucl. Med. 2016, 46, 225–238. [Google Scholar] [CrossRef]
- Anthony, L.B.; Woltering, E.A.; Espenan, G.D.; Cronin, M.D.; Maloney, T.J.; McCarthy, K.E. Indium-111-pentetreotide prolongs survival in gastroenteropancreatic malignancies. Semin. Nucl. Med. 2002, 32, 123–132. [Google Scholar] [CrossRef] [PubMed]
- De Jong, M.; Bakker, W.H.; Breeman, W.A.; Bernard, B.F.; Hofland, L.J.; Visser, T.J.; Srinivasan, A.; Schmidt, M.; Béhé, M.; Mäcke, H.R.; et al. Pre-clinical comparison of [DTPA0] octreotide, [DTPA0,Tyr3] octreotide and [DOTA0,Tyr3] octreotide as carriers for somatostatin receptor-targeted scintigraphy and radionuclide therapy. Int. J. Cancer 1998, 75, 406–411. [Google Scholar] [CrossRef]
- Otte, A.; Jermann, E.; Behe, M.; Goetze, M.; Bucher, H.C.; Roser, H.W.; Heppeler, A.; Mueller-Brand, J.; Maecke, H.R. DOTATOC: A powerful new tool for receptor-mediated radionuclide therapy. Eur. J. Nucl. Med. 1997, 24, 792–795. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Otte, A.; Mueller-Brand, J.; Dellas, S.; Nitzsche, E.U.; Herrmann, R.; Maecke, H.R. Yttrium-90-labelled somatostatin-analogue for cancer treatment. Lancet 1998, 351, 417–418. [Google Scholar] [CrossRef]
- Cremonesi, M.; Ferrari, M.; Zoboli, S.; Chinol, M.; Stabin, M.G.; Orsi, F.; Maecke, H.R.; Jermann, E.; Robertson, C.; Fiorenza, M.; et al. Biokinetics and dosimetry in patients administered with (111)In-DOTA-Tyr(3)-octreotide: Implications for internal radiotherapy with (90)Y-DOTATOC. Eur. J. Nucl. Med. 1999, 26, 877–886. [Google Scholar] [CrossRef]
- De Jong, M.; Rolleman, E.J.; Bernard, B.F.; Visser, T.J.; Bakker, W.H.; Breeman, W.A.; Krenning, E.P. Inhibition of renal uptake of indium-111-DTPA-octreotide in vivo. J. Nucl. Med. 1996, 37, 1388–1392. [Google Scholar]
- Waldherr, C.; Pless, M.; Maecke, H.R.; Haldemann, A.; Mueller-Brand, J. The clinical value of [90Y-DOTA]-D-Phe1-Tyr3-octreotide (90Y-DOTATOC) in the treatment of neuroendocrine tumours: A clinical phase II study. Ann. Oncol. Off. J. Eur. Soc. Med. Oncol. 2001, 12, 941–945. [Google Scholar] [CrossRef]
- Paganelli, G.; Zoboli, S.; Cremonesi, M.; Bodei, L.; Ferrari, M.; Grana, C.; Bartolomei, M.; Orsi, F.; De Cicco, C.; Mäcke, H.R.; et al. Receptor-mediated radiotherapy with 90Y-DOTA-D-Phe1-Tyr3-octreotide. Eur. J. Nucl. Med. 2001, 28, 426–434. [Google Scholar] [CrossRef]
- 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. Off. J. Am. Soc. Clin. Oncol. 2011, 29, 2416–2423. [Google Scholar] [CrossRef]
- Cwikla, J.B.; Sankowski, A.; Seklecka, N.; Buscombe, J.R.; Nasierowska-Guttmejer, A.; Jeziorski, K.G.; Mikolajczak, R.; Pawlak, D.; Stepien, K.; Walecki, J. Efficacy of radionuclide treatment DOTATATE Y-90 in patients with progressive metastatic gastroenteropancreatic neuroendocrine carcinomas (GEP-NETs): A phase II study. Ann. Oncol. 2009, 21, 787–794. [Google Scholar] [CrossRef]
- Valkema, R.; Pauwels, S.A.; Kvols, L.K.; Kwekkeboom, D.J.; Jamar, F.; de Jong, M.; Barone, R.; Walrand, S.; Kooij, P.P.M.; Bakker, W.H.; et al. Long-term follow-up of renal function after peptide receptor radiation therapy with 90Y-DOTA0,Tyr3-octreotide and 177Lu-DOTA0, Tyr3-octreotate. J. Nucl. Med. 2005, 46 (Suppl. S1), 83S–91S. [Google Scholar] [PubMed]
- Wright, C.L.; Zhang, J.; Tweedle, M.F.; Knopp, M.V.; Hall, N.C. Theranostic Imaging of Yttrium-90. BioMed Res. Int. 2015, 2015, 481279. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Lee, S.T.; Kulkarni, H.R.; Singh, A.; Baum, R.P. Theranostics of Neuroendocrine Tumors. Visc. Med. 2017, 33, 358–366. [Google Scholar] [CrossRef] [PubMed]
- Walrand, S.; Flux, G.D.; Konijnenberg, M.W.; Valkema, R.; Krenning, E.P.; Lhommel, R.; Pauwels, S.; Jamar, F. Dosimetry of yttrium-labelled radiopharmaceuticals for internal therapy: 86Y or 90Y imaging? Eur. J. Nucl. Med. Mol. Imaging 2011, 38 (Suppl. S1), S57–S68. [Google Scholar] [CrossRef] [PubMed]
- Kwekkeboom, D.J.; Kam, B.L.; Van Essen, M.; Teunissen, J.J.M.; Van Eijck, C.H.J.; Valkema, R.; De Jong, M.; De Herder, W.W.; Krenning, E.P. Somatostatin receptor-based imaging and therapy of gastroenteropancreatic neuroendocrine tumors. Endocr. Relat. Cancer 2010, 17, R53. [Google Scholar] [CrossRef] [Green Version]
- Kwekkeboom, D.J.; Teunissen, J.J.; Bakker, W.H.; Kooij, P.P.; De Herder, W.W.; Feelders, R.A.; Van Eijck, C.H.; Esser, J.P.; Kam, B.L.; Krenning, E.P. Radiolabeled somatostatin analog [177Lu-DOTA0, Tyr3]octreotate in patients with endocrine gastroenteropancreatic tumors. J. Clin. Oncol. 2005, 23, 2754–2762. [Google Scholar] [CrossRef] [Green Version]
- Levine, R.; Krenning, E.P. Clinical History of the Theranostic Radionuclide Approach to Neuroendocrine Tumors and Other Types of Cancer: Historical Review Based on an Interview of Eric P. Krenning by Rachel Levine. J. Nucl. Med. 2017, 58, 3S–9S. [Google Scholar] [CrossRef] [Green Version]
- De Jong, M.; Breeman, W.A.P.; Bernard, B.F.; Bakker, W.H.; Schaar, M.; van Gameren, A.; Bugaj, J.E.; Erion, J.; Schmidt, M.; Srinivasan, A.; et al. [177Lu-DOTA0,Tyr3]octreotate for somatostatin receptor-targeted radionuclide therapy. Int. J. Cancer 2001, 92, 628–633. [Google Scholar] [CrossRef]
- Kwekkeboom, D.J.; Bakker, W.H.; Kooij, P.P.; Konijnenberg, M.W.; Srinivasan, A.; Erion, J.L.; Schmidt, M.A.; Bugaj, J.L.; de Jong, M.; Krenning, E.P. [177Lu-DOTAOTyr3]octreotate: Comparison with [111In-DTPAo]octreotide in patients. Eur. J. Nucl. Med. 2001, 28, 1319–1325. [Google Scholar] [CrossRef]
- Kwekkeboom, D.J.; Bakker, W.H.; Kam, B.L.; Teunissen, J.J.M.; Kooij, P.P.M.; de Herder, W.W.; Feelders, R.A.; van Eijck, C.H.J.; de Jong, M.; Srinivasan, A.; et al. Treatment of patients with gastro-entero-pancreatic (GEP) tumours with the novel radiolabelled somatostatin analogue [177Lu-DOTA0,Tyr3]octreotate. Eur. J. Nucl. Med. Mol. Imaging 2003, 30, 417–422. [Google Scholar] [CrossRef] [Green Version]
- Kwekkeboom, D.J.; de Herder, W.W.; Kam, B.L.; van Eijck, C.H.; van Essen, M.; Kooij, P.P.; Feelders, R.A.; van Aken, M.O.; Krenning, E.P. Treatment with the radiolabeled somatostatin analog [177Lu-DOTA0,Tyr3]octreotate: Toxicity, efficacy, and survival. J. Clin. Oncol. Off. J. Am. Soc. Clin. Oncol. 2008, 26, 2124–2130. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Khan, S.; Krenning, E.P.; van Essen, M.; Kam, B.L.; Teunissen, J.J.; Kwekkeboom, D.J. Quality of life in 265 patients with gastroenteropancreatic or bronchial neuroendocrine tumors treated with [177Lu-DOTA0,Tyr3]octreotate. J. Nucl. Med. 2011, 52, 1361–1368. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Strosberg, J.; El-Haddad, G.; Wolin, E.; Hendifar, A.; Yao, J.; Chasen, B.; Mittra, E.; Kunz, P.L.; Kulke, M.H.; Jacene, H.; et al. Phase 3 Trial of 177Lu-Dotatate for Midgut Neuroendocrine Tumors. N. Engl. J. Med. 2017, 376, 125–135. [Google Scholar] [CrossRef] [PubMed]
- Strosberg, J.R.; Wolin, E.M.; Chasen, B.A.; Kulke, M.H.; Bushnell, D.L.; Caplin, M.E.; Baum, R.P.; Hobday, T.J.; Hendifar, A.E.; Lopera Sierra, M.; et al. First update on overall survival, progression-free survival, and health-related time-to-deterioration quality of life from the NETTER-1 study: 177Lu-Dotatate vs. high dose octreotide in progressive midgut neuroendocrine tumors. J. Clin. Oncol. 2018, 36, 4099. [Google Scholar] [CrossRef]
- Strosberg, J.R.; Caplin, M.E.; Kunz, P.L.; Ruszniewski, P.B.; Bodei, L.; Hendifar, A.E.; Mittra, E.; Wolin, E.M.; Yao, J.C.; Pavel, M.E.; et al. Final overall survival in the phase 3 NETTER-1 study of lutetium-177-DOTATATE in patients with midgut neuroendocrine tumors. J. Clin. Oncol. 2021, 39, 4112. [Google Scholar] [CrossRef]
- Brabander, T.; Van Der Zwan, W.A.; Teunissen, J.J.M.; Kam, B.L.R.; Feelders, R.A.; De Herder, W.W.; Van Eijck, C.H.J.; Franssen, G.J.H.; Krenning, E.P.; Kwekkeboom, D.J. Long-term efficacy, survival, and safety of [177Lu-DOTA0,Tyr3]octreotate in patients with gastroenteropancreatic and bronchial neuroendocrine tumors. Clin. Cancer Res. 2017, 23, 4617–4624. [Google Scholar] [CrossRef] [Green Version]
- Hennrich, U.; Kopka, K. Lutathera(®): The First FDA- and EMA-Approved Radiopharmaceutical for Peptide Receptor Radionuclide Therapy. Pharmaceuticals 2019, 12, 114. [Google Scholar] [CrossRef] [Green Version]
- Kim, S.J.; Pak, K.; Koo, P.J.; Kwak, J.J.; Chang, S. The efficacy of 177Lu-labelled peptide receptor radionuclide therapy in patients with neuroendocrine tumours: A meta-analysis. Eur. J. Nucl. Med. Mol. Imaging 2015, 42, 1964–1970. [Google Scholar] [CrossRef]
- Zhang, J.; Kulkarni, H.R.; Singh, A.; Niepsch, K.; Müller, D.; Baum, R.P. Peptide Receptor Radionuclide Therapy in Grade 3 Neuroendocrine Neoplasms: Safety and Survival Analysis in 69 Patients. J. Nucl. Med. 2019, 60, 377–385. [Google Scholar] [CrossRef]
- Thang, S.P.; Lung, M.S.; Kong, G.; Hofman, M.S.; Callahan, J.; Michael, M.; Hicks, R.J. Peptide receptor radionuclide therapy (PRRT) in European Neuroendocrine Tumour Society (ENETS) grade 3 (G3) neuroendocrine neoplasia (NEN)—A single-institution retrospective analysis. Eur. J. Nucl. Med. Mol. Imaging 2018, 45, 262–277. [Google Scholar] [CrossRef]
- Carlsen, E.A.; Fazio, N.; Granberg, D.; Grozinsky-Glasberg, S.; Ahmadzadehfar, H.; Grana, C.M.; Zandee, W.T.; Cwikla, J.; Walter, M.A.; Oturai, P.S.; et al. Peptide receptor radionuclide therapy in gastroenteropancreatic NEN G3: A multicenter cohort study. Endocr. Relat. Cancer 2019, 26, 227–239. [Google Scholar] [CrossRef] [PubMed]
- Sorbye, H.; Kong, G.; Grozinsky-Glasberg, S. PRRT in high-grade gastroenteropancreatic neuroendocrine neoplasms (WHO G3). Endocr. Relat. Cancer 2020, 27, R67–R77. [Google Scholar] [CrossRef] [PubMed]
- Graf, J.; Pape, U.-F.; Jann, H.; Denecke, T.; Arsenic, R.; Brenner, W.; Pavel, M.; Prasad, V. Prognostic Significance of Somatostatin Receptor Heterogeneity in Progressive Neuroendocrine Tumor Treated with Lu-177 DOTATOC or Lu-177 DOTATATE. Eur. J. Nucl. Med. Mol. Imaging 2020, 47, 881–894. [Google Scholar] [CrossRef] [PubMed]
- Chan, D.L.; Pavlakis, N.; Schembri, G.P.; Bernard, E.J.; Hsiao, E.; Hayes, A.; Barnes, T.; Diakos, C.; Khasraw, M.; Samra, J.; et al. Dual Somatostatin Receptor/FDG PET/CT Imaging in Metastatic Neuroendocrine Tumours: Proposal for a Novel Grading Scheme with Prognostic Significance. Theranostics 2017, 7, 1149–1158. [Google Scholar] [CrossRef]
- Alevroudis, E.; Spei, M.-E.; Chatziioannou, S.N.; Tsoli, M.; Wallin, G.; Kaltsas, G.; Daskalakis, K. Clinical Utility of 18F-FDG PET in Neuroendocrine Tumors Prior to Peptide Receptor Radionuclide Therapy: A Systematic Review and Meta-Analysis. Cancers 2021, 13, 1813. [Google Scholar] [CrossRef]
- Hindié, E. The netpet score: Combining FDG and somatostatin receptor imaging for optimal management of patients with metastatic well-differentiated neuroendocrine tumors. Theranostics 2017, 7, 1159–1163. [Google Scholar] [CrossRef]
- Hope, T.A.; Bodei, L.; Chan, J.A.; El-Haddad, G.; Fidelman, N.; Kunz, P.L.; Mailman, J.; Menda, Y.; Metz, D.C.; Mittra, E.S.; et al. NANETS/SNMMI Consensus Statement on Patient Selection and Appropriate Use of 177Lu-DOTATATE Peptide Receptor Radionuclide Therapy. J. Nucl. Med. 2020, 61, 222–227. [Google Scholar] [CrossRef]
- Pavel, M.; Öberg, K.; Falconi, M.; Krenning, E.P.; Sundin, A.; Perren, A.; Berruti, A. Gastroenteropancreatic neuroendocrine neoplasms: ESMO Clinical Practice Guidelines for diagnosis, treatment and follow-up. Ann. Oncol. Off. J. Eur. Soc. Med. Oncol. 2020, 31, 844–860. [Google Scholar] [CrossRef]
- Pavel, M.; O’Toole, D.; Costa, F.; Capdevila, J.; Gross, D.; Kianmanesh, R.; Krenning, E.; Knigge, U.; Salazar, R.; Pape, U.-F.; et al. ENETS Consensus Guidelines Update for the Management of Distant Metastatic Disease of Intestinal, Pancreatic, Bronchial Neuroendocrine Neoplasms (NEN) and NEN of Unknown Primary Site. Neuroendocrinology 2016, 103, 172–185. [Google Scholar] [CrossRef]
- Raymond, E.; Dahan, L.; Raoul, J.-L.; Bang, Y.-J.; Borbath, I.; Lombard-Bohas, C.; Valle, J.; Metrakos, P.; Smith, D.; Vinik, A.; et al. Sunitinib malate for the treatment of pancreatic neuroendocrine tumors. N. Engl. J. Med. 2011, 364, 501–513. [Google Scholar] [CrossRef] [Green Version]
- 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.E.; et al. Everolimus for advanced pancreatic neuroendocrine tumors. N. Engl. J. Med. 2011, 364, 514–523. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Yao, J.C.; Fazio, N.; Singh, S.; Buzzoni, R.; Carnaghi, C.; Wolin, E.; Tomasek, J.; Raderer, M.; Lahner, H.; Voi, M.; et al. 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, 968–977. [Google Scholar] [CrossRef]
- Pavel, M.E.; Baudin, E.; Öberg, K.E.; Hainsworth, J.D.; Voi, M.; Rouyrre, N.; Peeters, M.; Gross, D.J.; Yao, J.C. Efficacy of everolimus plus octreotide LAR in patients with advanced neuroendocrine tumor and carcinoid syndrome: Final overall survival from the randomized, placebo-controlled phase 3 RADIANT-2 study. Ann. Oncol. Off. J. Eur. Soc. Med. Oncol. 2017, 28, 1569–1575. [Google Scholar] [CrossRef] [PubMed]
- Satapathy, S.; Mittal, B.R. 177Lu-DOTATATE peptide receptor radionuclide therapy versus Everolimus in advanced pancreatic neuroendocrine tumors: A systematic review and meta-analysis. Nucl. Med. Commun. 2019, 40, 1195–1203. [Google Scholar] [CrossRef] [PubMed]
- De Baere, T.; Deschamps, F.; Tselikas, L.; Ducreux, M.; Planchard, D.; Pearson, E.; Berdelou, A.; Leboulleux, S.; Elias, D.; Baudin, E. GEP-NETS update: Interventional radiology: Role in the treatment of liver metastases from GEP-NETs. Eur. J. Endocrinol. 2015, 172, R151–R166. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Agency, E.M. Lutathera Summary of Product Characteristics. Available online: https://www.ema.europa.eu/en/documents/product-information/lutathera-epar-product-information_en.pdf (accessed on 22 May 2021).
- Hope, T.A.; Abbott, A.; Colucci, K.; Bushnell, D.L.; Gardner, L.; Graham, W.S.; Lindsay, S.; Metz, D.C.; Pryma, D.A.; Stabin, M.G.; et al. NANETS/SNMMI procedure standard for somatostatin receptor-based peptide receptor radionuclide therapy with 177Lu-DOTATATE. J. Nucl. Med. 2019, 60, 937–943. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Bodei, L.; Mueller-Brand, J.; Baum, R.P.; Pavel, M.E.; Hörsch, D.; O’Dorisio, M.S.; O’Dorisio, T.M.; Howe, J.R.; Cremonesi, M.; Kwekkeboom, D.J.; et al. The joint IAEA, EANM, and SNMMI practical guidance on peptide receptor radionuclide therapy (PRRNT) in neuroendocrine tumours. Eur. J. Nucl. Med. Mol. Imaging 2013, 40, 800–816. [Google Scholar] [CrossRef]
- De Keizer, B.; Van Aken, M.O.; Feelders, R.A.; De Herder, W.W.; Kam, B.L.R.; Van Essen, M.; Krenning, E.P.; Kwekkeboom, D.J. Hormonal crises following receptor radionuclide therapy with the radiolabeled somatostatin analogue [177Lu-DOTA0,Tyr3]octreotate. Eur. J. Nucl. Med. Mol. Imaging 2008, 35, 749–755. [Google Scholar] [CrossRef] [Green Version]
- Condron, M.E.; Jameson, N.E.; Limbach, K.E.; Bingham, A.E.; Sera, V.A.; Anderson, R.B.; Schenning, K.J.; Yockelson, S.; Harukuni, I.; Kahl, E.A.; et al. A prospective study of the pathophysiology of carcinoid crisis. Surgery 2019, 165, 158–165. [Google Scholar] [CrossRef]
- Del Olmo-García, M.I.; Muros, M.A.; López-de-la-Torre, M.; Agudelo, M.; Bello, P.; Soriano, J.M.; Merino-Torres, J.-F. Prevention and Management of Hormonal Crisis during Theragnosis with LU-DOTA-TATE in Neuroendocrine Tumors. A Systematic Review and Approach Proposal. J. Clin. Med. 2020, 9, 2203. [Google Scholar] [CrossRef]
- Tapia Rico, G.; Li, M.; Pavlakis, N.; Cehic, G.; Price, T.J. Prevention and management of carcinoid crises in patients with high-risk neuroendocrine tumours undergoing peptide receptor radionuclide therapy (PRRT): Literature review and case series from two Australian tertiary medical institutions. Cancer Treat. Rev. 2018, 66, 1–6. [Google Scholar] [CrossRef] [PubMed]
- Zandee, W.T.; Brabander, T.; Blažević, A.; Kam, B.L.R.; Teunissen, J.J.M.; Feelders, R.A.; Hofland, J.; de Herder, W.W. Symptomatic and Radiological Response to 177Lu-DOTATATE for the Treatment of Functioning Pancreatic Neuroendocrine Tumors. J. Clin. Endocrinol. Metab. 2019, 104, 1336–1344. [Google Scholar] [CrossRef] [PubMed]
- Kendi, A.T.; Halfdanarson, T.R.; Packard, A.; Dundar, A.; Subramaniam, R.M. Therapy with 177Lu-DOTATATE: Clinical implementation and impact on care of patients with neuroendocrine tumors. Am. J. Roentgenol. 2019, 213, 309–317. [Google Scholar] [CrossRef] [PubMed]
- Strosberg, J.; Kunz, P.L.; Hendifar, A.; Yao, J.; Bushnell, D.; Kulke, M.H.; Baum, R.P.; Caplin, M.; Ruszniewski, P.; Delpassand, E.; et al. Impact of liver tumour burden, alkaline phosphatase elevation, and target lesion size on treatment outcomes with 177Lu-Dotatate: An analysis of the NETTER-1 study. Eur. J. Nucl. Med. Mol. Imaging 2020, 47, 2372–2382. [Google Scholar] [CrossRef] [Green Version]
- Sabet, A.; Khalaf, F.; Yong-Hing, C.J.; Sabet, A.; Haslerud, T.; Ahmadzadehfar, H.; Guhlke, S.; Grünwald, F.; Biersack, H.-J.; Ezziddin, S. Can peptide receptor radionuclide therapy be safely applied in florid bone metastases? A pilot analysis of late stage osseous involvement. Nuklearmedizin 2014, 53, 54–59. [Google Scholar] [CrossRef]
- Huizing, D.M.V.; de Wit-van der Veen, B.J.; Verheij, M.; Stokkel, M.P.M. Dosimetry methods and clinical applications in peptide receptor radionuclide therapy for neuroendocrine tumours: A literature review. EJNMMI Res. 2018, 8, 89. [Google Scholar] [CrossRef]
- Stokke, C.; Gabiña, P.M.; Solný, P.; Cicone, F.; Sandström, M.; Gleisner, K.S.; Chiesa, C.; Spezi, E.; Paphiti, M.; Konijnenberg, M.; et al. Dosimetry-based treatment planning for molecular radiotherapy: A summary of the 2017 report from the Internal Dosimetry Task Force. EJNMMI Phys. 2017, 4, 27. [Google Scholar] [CrossRef]
- Sandström, M.; Ilan, E.; Karlberg, A.; Johansson, S.; Freedman, N.; Garske-Román, U. Method dependence, observer variability and kidney volumes in radiation dosimetry of 177Lu-DOTATATE therapy in patients with neuroendocrine tumours. EJNMMI Phys. 2015, 2, 24. [Google Scholar] [CrossRef] [Green Version]
- Del Prete, M.; Buteau, F.-A.; Beauregard, J.-M. Personalized 177Lu-octreotate peptide receptor radionuclide therapy of neuroendocrine tumours: A simulation study. Eur. J. Nucl. Med. Mol. Imaging 2017, 44, 1490–1500. [Google Scholar] [CrossRef]
- Sabet, A.; Haslerud, T.; Pape, U.-F.; Sabet, A.; Ahmadzadehfar, H.; Grünwald, F.; Guhlke, S.; Biersack, H.-J.; Ezziddin, S. Outcome and toxicity of salvage therapy with 177Lu-octreotate in patients with metastatic gastroenteropancreatic neuroendocrine tumours. Eur. J. Nucl. Med. Mol. Imaging 2014, 41, 205–210. [Google Scholar] [CrossRef]
- Van der Zwan, W.A.; Brabander, T.; Kam, B.L.R.; Teunissen, J.J.M.; Feelders, R.A.; Hofland, J.; Krenning, E.P.; de Herder, W.W. Salvage peptide receptor radionuclide therapy with [177Lu-DOTA,Tyr3]octreotate in patients with bronchial and gastroenteropancreatic neuroendocrine tumours. Eur. J. Nucl. Med. Mol. Imaging 2019, 46, 704–717. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Modlin, I.M.; Kidd, M.; Malczewska, A.; Drozdov, I.; Bodei, L.; Matar, S.; Chung, K.-M. The NETest: The Clinical Utility of Multigene Blood Analysis in the Diagnosis and Management of Neuroendocrine Tumors. Endocrinol. Metab. Clin. N. Am. 2018, 47, 485–504. [Google Scholar] [CrossRef] [PubMed]
- Öberg, K.; Califano, A.; Strosberg, J.R.; Ma, S.; Pape, U.; Bodei, L.; Kaltsas, G.; Toumpanakis, C.; Goldenring, J.R.; Frilling, A.; et al. A meta-analysis of the accuracy of a neuroendocrine tumor mRNA genomic biomarker (NETest) in blood. Ann. Oncol. Off. J. Eur. Soc. Med. Oncol. 2020, 31, 202–212. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- ClinicalTrials.gov. Study to Evaluate the Efficacy and Safety of Lutathera in Patients With Grade 2 and Grade 3 Advanced GEP-NET. Available online: https://clinicaltrials.gov/ct2/show/NCT03972488 (accessed on 22 May 2021).
- ClinicalTrials.gov. Efficacy and Safety of 177Lu-edotreotide PRRT in GEP-NET Patients (COMPETE). Available online: https://clinicaltrials.gov/ct2/show/NCT03049189 (accessed on 22 May 2021).
- Kaemmerer, D.; Prasad, V.; Daffner, W.; Hörsch, D.; Klöppel, G.; Hommann, M.; Baum, R.P. Neoadjuvant peptide receptor radionuclide therapy for an inoperable neuroendocrine pancreatic tumor. World J. Gastroenterol. 2009, 15, 5867–5870. [Google Scholar] [CrossRef]
- Stoeltzing, O.; Loss, M.; Huber, E.; Gross, V.; Eilles, C.; Mueller-Brand, J.; Schlitt, H.J. Staged surgery with neoadjuvant 90Y-DOTATOC therapy for down-sizing synchronous bilobular hepatic metastases from a neuroendocrine pancreatic tumor. Langenbeck’s Arch. Surg. 2010, 395, 185–192. [Google Scholar] [CrossRef]
- Partelli, S.; Bertani, E.; Bartolomei, M.; Perali, C.; Muffatti, F.; Grana, C.M.; Schiavo Lena, M.; Doglioni, C.; Crippa, S.; Fazio, N.; et al. Peptide receptor radionuclide therapy as neoadjuvant therapy for resectable or potentially resectable pancreatic neuroendocrine neoplasms. Surgery 2018, 163, 761–767. [Google Scholar] [CrossRef]
- Breeman, W.A.P.; Mearadji, A.; Capello, A.; Bernard, B.F.; van Eijck, C.H.J.; Krenning, E.P.; de Jong, M. Anti-tumor effect and increased survival after treatment with [177Lu-DOTA0,Tyr3]octreotate in a rat liver micrometastases model. Int. J. Cancer 2003, 104, 376–379. [Google Scholar] [CrossRef]
- Bertani, E.; Fazio, N.; Radice, D.; Zardini, C.; Grana, C.; Bodei, L.; Funicelli, L.; Ferrari, C.; Spada, F.; Partelli, S.; et al. Resection of the Primary Tumor Followed by Peptide Receptor Radionuclide Therapy as Upfront Strategy for the Treatment of G1-G2 Pancreatic Neuroendocrine Tumors with Unresectable Liver Metastases. Ann. Surg. Oncol. 2016, 23, 981–989. [Google Scholar] [CrossRef]
- Kratochwil, C.; Giesel, F.L.; López-Benítez, R.; Schimpfky, N.; Kunze, K.; Eisenhut, M.; Kauczor, H.-U.; Haberkorn, U. Intraindividual comparison of selective arterial versus venous 68Ga-DOTATOC PET/CT in patients with gastroenteropancreatic neuroendocrine tumors. Clin. Cancer Res. Off. J. Am. Assoc. Cancer Res. 2010, 16, 2899–2905. [Google Scholar] [CrossRef] [Green Version]
- Limouris, G.S.; Chatziioannou, A.; Kontogeorgakos, D.; Mourikis, D.; Lyra, M.; Dimitriou, P.; Stavraka, A.; Gouliamos, A.; Vlahos, L. Selective hepatic arterial infusion of In-111-DTPA-Phe1-octreotide in neuroendocrine liver metastases. Eur. J. Nucl. Med. Mol. Imaging 2008, 35, 1827–1837. [Google Scholar] [CrossRef]
- De Jong, M.; Breeman, W.A.P.; Valkema, R.; Bernard, B.F.; Krenning, E.P. Combination radionuclide therapy using 177Lu- and 90Y-labeled somatostatin analogs. J. Nucl. Med. 2005, 46 (Suppl. S1), 13S–17S. [Google Scholar] [PubMed]
- Werner, R.A.; Bluemel, C.; Allen-Auerbach, M.S.; Higuchi, T.; Herrmann, K. 68Gallium- and 90Yttrium-/ 177Lutetium: “Theranostic twins” for diagnosis and treatment of NETs. Ann. Nucl. Med. 2015, 29, 1–7. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Villard, L.; Romer, A.; Marincek, N.; Brunner, P.; Koller, M.T.; Schindler, C.; Ng, Q.K.T.; Mäcke, H.R.; Müller-Brand, J.; Rochlitz, C.; et al. Cohort study of somatostatin-based radiopeptide therapy with [90Y-DOTA]-TOC versus [90Y-DOTA]-TOC plus [177Lu-DOTA]-TOC in neuroendocrine cancers. J. Clin. Oncol. Off. J. Am. Soc. Clin. Oncol. 2012, 30, 1100–1106. [Google Scholar] [CrossRef] [PubMed]
- Gabriel, M.; Andergassen, U.; Putzer, D.; Kroiss, A.; Waitz, D.; Von Guggenberg, E.; Kendler, D.; Virgolini, I.J. Individualized peptide-related-radionuclide-therapy concept using different radiolabelled somatostatin analogs in advanced cancer patients. Q. J. Nucl. Med. Mol. Imaging. 2010, 54, 92–99. [Google Scholar]
- Yordanova, A.; Ahmadzadehfar, H. Combination Therapies with PRRT. Pharmaceuticals 2021, 14, 1005. [Google Scholar] [CrossRef]
- Bodei, L.; Kidd, M.; Paganelli, G.; Grana, C.M.; Drozdov, I.; Cremonesi, M.; Lepensky, C.; Kwekkeboom, D.J.; Baum, R.P.; Krenning, E.P.; et al. Long-term tolerability of PRRT in 807 patients with neuroendocrine tumours: The value and limitations of clinical factors. Eur. J. Nucl. Med. Mol. Imaging 2015, 42, 5–19. [Google Scholar] [CrossRef]
- Cives, M.; Strosberg, J. Radionuclide Therapy for Neuroendocrine Tumors. Curr. Oncol. Rep. 2017, 19, 9. [Google Scholar] [CrossRef]
- Chan, P.S.; Croasdale, J. Survey of current therapeutic radiopharmaceuticals. In Sampson’s Textbook of Radiopharmacy; Theobald, T., Ed.; Pharmaceutical Press: London, UK, 2011; p. 305. ISBN 978. [Google Scholar]
- Navalkissoor, S.; Grossman, A. Targeted Alpha Particle Therapy for Neuroendocrine Tumours: The Next Generation of Peptide Receptor Radionuclide Therapy. Neuroendocrinology 2019, 108, 256–264. [Google Scholar] [CrossRef]
- Kratochwil, C.; Giesel, F.L.; Bruchertseifer, F.; Mier, W.; Apostolidis, C.; Boll, R.; Murphy, K.; Haberkorn, U.; Morgenstern, A. 213Bi-DOTATOC receptor-targeted alpha-radionuclide therapy induces remission in neuroendocrine tumours refractory to beta radiation: A first-in-human experience. Eur. J. Nucl. Med. Mol. Imaging 2014, 41, 2106–2119. [Google Scholar] [CrossRef] [Green Version]
- Stallons, T.A.R.; Saidi, A.; Tworowska, I.; Delpassand, E.S.; Torgue, J.J. Preclinical Investigation of 212Pb-DOTAMTATE for Peptide Receptor Radionuclide Therapy in a Neuroendocrine Tumor Model. Mol. Cancer Ther. 2019, 18, 1012–1021. [Google Scholar] [CrossRef] [Green Version]
- Ezziddin, S.; Meyer, C.; Kahancova, S.; Haslerud, T.; Willinek, W.; Wilhelm, K.; Biersack, H.-J.; Ahmadzadehfar, H. 90Y Radioembolization after radiation exposure from peptide receptor radionuclide therapy. J. Nucl. Med. 2012, 53, 1663–1669. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Claringbold, P.G.; Turner, J.H. NeuroEndocrine Tumor Therapy with Lutetium-177-octreotate and Everolimus (NETTLE): A Phase I Study. Cancer Biother. Radiopharm. 2015, 30, 261–269. [Google Scholar] [CrossRef] [PubMed]
- Riff, B.P.; Yang, Y.-X.; Soulen, M.C.; Pryma, D.A.; Bennett, B.; Wild, D.; Nicolas, G.; Teitelbaum, U.R.; Metz, D.C. Peptide Receptor Radionuclide Therapy-Induced Hepatotoxicity in Patients With Metastatic Neuroendocrine Tumors. Clin. Nucl. Med. 2015, 40, 845–850. [Google Scholar] [CrossRef]
- Hubble, D.; Kong, G.; Michael, M.; Johnson, V.; Ramdave, S.; Hicks, R.J. 177Lu-octreotate, alone or with radiosensitising chemotherapy, is safe in neuroendocrine tumour patients previously treated with high-activity 111In-octreotide. Eur. J. Nucl. Med. Mol. Imaging 2010, 37, 1869–1875. [Google Scholar] [CrossRef]
- Kong, G.; Thompson, M.; Collins, M.; Herschtal, A.; Hofman, M.S.; Johnston, V.; Eu, P.; Michael, M.; Hicks, R.J. Assessment of predictors of response and long-term survival of patients with neuroendocrine tumour treated with peptide receptor chemoradionuclide therapy (PRCRT). Eur. J. Nucl. Med. Mol. Imaging 2014, 41, 1831–1844. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Nicolini, S.; Bodei, L.; Bongiovanni, A.; Sansovini, M.; Grassi, I.; Ibrahim, T.; Monti, M.; Caroli, P.; Sarnelli, A.; Diano, D.; et al. Combined use of 177Lu-DOTATATE and metronomic capecitabine (Lu-X) in FDG-positive gastro-entero-pancreatic neuroendocrine tumors. Eur. J. Nucl. Med. Mol. Imaging 2021, 48, 3260–3267. [Google Scholar] [CrossRef]
- Goncalves, I.; Burbury, K.; Michael, M.; Iravani, A.; Ravi Kumar, A.S.; Akhurst, T.; Tiong, I.S.; Blombery, P.; Hofman, M.S.; Westerman, D.; et al. Characteristics and outcomes of therapy-related myeloid neoplasms after peptide receptor radionuclide/chemoradionuclide therapy (PRRT/PRCRT) for metastatic neuroendocrine neoplasia: A single-institution series. Eur. J. Nucl. Med. Mol. Imaging 2019, 46, 1902–1910. [Google Scholar] [CrossRef]
- Nonnekens, J.; van Kranenburg, M.; Beerens, C.E.M.T.; Suker, M.; Doukas, M.; van Eijck, C.H.J.; de Jong, M.; van Gent, D.C. Potentiation of Peptide Receptor Radionuclide Therapy by the PARP Inhibitor Olaparib. Theranostics 2016, 6, 1821–1832. [Google Scholar] [CrossRef] [Green Version]
- Demaria, S.; Bhardwaj, N.; McBride, W.H.; Formenti, S.C. Combining radiotherapy and immunotherapy: A revived partnership. Int. J. Radiat. Oncol. Biol. Phys. 2005, 63, 655–666. [Google Scholar] [CrossRef] [Green Version]
- Wu, Y.; Pfeifer, A.K.; Myschetzky, R.; Garbyal, R.S.; Rasmussen, P.; Knigge, U.; Bzorek, M.; Kristensen, M.H.; Kjaer, A. Induction of Anti-Tumor Immune Responses by Peptide Receptor Radionuclide Therapy with 177Lu-DOTATATE in a Murine Model of a Human Neuroendocrine Tumor. Diagnostics 2013, 3, 344–355. [Google Scholar] [CrossRef]
- Cavalcanti, E.; Armentano, R.; Valentini, A.M.; Chieppa, M.; Caruso, M.L. Role of PD-L1 expression as a biomarker for GEP neuroendocrine neoplasm grading. Cell Death Dis. 2017, 8, e3004. [Google Scholar] [CrossRef] [PubMed]
- Wild, D.; Fani, M.; Fischer, R.; Del Pozzo, L.; Kaul, F.; Krebs, S.; Fischer, R.; Rivier, J.E.F.; Reubi, J.C.; Maecke, H.R.; et al. Comparison of somatostatin receptor agonist and antagonist for peptide receptor radionuclide therapy: A pilot study. J. Nucl. Med. 2014, 55, 1248–1252. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Krebs, S.; Pandit-Taskar, N.; Reidy, D.; Beattie, B.J.; Lyashchenko, S.K.; Lewis, J.S.; Bodei, L.; Weber, W.A.; O’Donoghue, J.A. Biodistribution and radiation dose estimates for 68Ga-DOTA-JR11 in patients with metastatic neuroendocrine tumors. Eur. J. Nucl. Med. Mol. Imaging 2019, 46, 677–685. [Google Scholar] [CrossRef] [PubMed]
- Reidy-Lagunes, D.; Pandit-Taskar, N.; O’Donoghue, J.A.; Krebs, S.; Staton, K.D.; Lyashchenko, S.K.; Lewis, J.S.; Raj, N.; Gönen, M.; Lohrmann, C.; et al. Phase I Trial of Well-Differentiated Neuroendocrine Tumors (NETs) with Radiolabeled Somatostatin Antagonist 177Lu-Satoreotide Tetraxetan. Clin. Cancer Res. Off. J. Am. Assoc. Cancer Res. 2019, 25, 6939–6947. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Roosenburg, S.; Laverman, P.; van Delft, F.L.; Boerman, O.C. Radiolabeled CCK/gastrin peptides for imaging and therapy of CCK2 receptor-expressing tumors. Amino Acids 2011, 41, 1049–1058. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Gotthardt, M.; Béhé, M.P.; Grass, J.; Bauhofer, A.; Rinke, A.; Schipper, M.L.; Kalinowski, M.; Arnold, R.; Oyen, W.J.G.; Behr, T.M. Added value of gastrin receptor scintigraphy in comparison to somatostatin receptor scintigraphy in patients with carcinoids and other neuroendocrine tumours. Endocr. Relat. Cancer 2006, 13, 1203–1211. [Google Scholar] [CrossRef] [Green Version]
- Béhé, M.; Behr, T.M. Cholecystokinin-B (CCK-B)/gastrin receptor targeting peptides for staging and therapy of medullary thyroid cancer and other CCK-B receptor expressing malignancies. Biopolymers 2002, 66, 399–418. [Google Scholar] [CrossRef]
- White, B.H.; Whalen, K.; Kriksciukaite, K.; Alargova, R.; Au Yeung, T.; Bazinet, P.; Brockman, A.; DuPont, M.; Oller, H.; Lemelin, C.-A.; et al. Discovery of an SSTR2-Targeting Maytansinoid Conjugate (PEN-221) with Potent Activity in Vitro and in Vivo. J. Med. Chem. 2019, 62, 2708–2719. [Google Scholar] [CrossRef]
- Johnson, M.L.; Meyer, T.; Halperin, D.M.; Fojo, A.T.; Cook, N.; Blaszkowsky, L.S.; Schlechter, B.L.; Yao, J.C.; Jemiai, Y.; Kriksciukaite, K.; et al. First in human phase 1/2a study of PEN-221 somatostatin analog (SSA)-DM1 conjugate for patients (PTS) with advanced neuroendocrine tumor (NET) or small cell lung cancer (SCLC): Phase 1 results. J. Clin. Oncol. 2018, 36, 4097. [Google Scholar] [CrossRef]
- Halperin, D.M.; Johnson, M.L.; Chan, J.A.; Hart, L.L.; Cook, N.; Patel, V.M.; Schlechter, B.L.; Cave, J.; Dowlati, A.; Blaszkowsky, L.S.; et al. The safety and efficacy of PEN-221 somatostatin analog (SSA)-DM1 conjugate in patients (PTS) with advanced GI mid-gut neuroendocrine tumor (NET): Phase 2 results. J. Clin. Oncol. 2021, 39, 4110. [Google Scholar] [CrossRef]
- Kong, G.; Grozinsky-Glasberg, S.; Hofman, M.S.; Callahan, J.; Meirovitz, A.; Maimon, O.; Pattison, D.A.; Gross, D.J.; Hicks, R.J. Efficacy of Peptide Receptor Radionuclide Therapy for Functional Metastatic Paraganglioma and Pheochromocytoma. J. Clin. Endocrinol. Metab. 2017, 102, 3278–3287. [Google Scholar] [CrossRef] [Green Version]
- Zandee, W.T.; Feelders, R.A.; Smit Duijzentkunst, D.A.; Hofland, J.; Metselaar, R.M.; Oldenburg, R.A.; van Linge, A.; Kam, B.L.R.; Teunissen, J.J.M.; Korpershoek, E.; et al. Treatment of inoperable or metastatic paragangliomas and pheochromocytomas with peptide receptor radionuclide therapy using 177Lu-DOTATATE. Eur. J. Endocrinol. 2019, 181, 45–53. [Google Scholar] [CrossRef] [PubMed]
- Yadav, M.P.; Ballal, S.; Bal, C. Concomitant 177Lu-DOTATATE and capecitabine therapy in malignant paragangliomas. EJNMMI Res. 2019, 9, 13. [Google Scholar] [CrossRef] [PubMed]
- Lin, F.; Del Rivero, J.; Carrasquillo, J.A.; Jha, A.; Gonzales, M.K.; Lindenberg, L.; Turkbey, B.; Lin, E.; Mena, E.; Millo, C.; et al. Phase 2 trial of Lu-177-DOTATATE in inoperable pheochromocytoma/paraganglioma. J. Clin. Oncol. 2019, 37, TPS4159. [Google Scholar] [CrossRef]
- Gains, J.E.; Bomanji, J.B.; Fersht, N.L.; Sullivan, T.; D’Souza, D.; Sullivan, K.P.; Aldridge, M.; Waddington, W.; Gaze, M.N. 177Lu-DOTATATE molecular radiotherapy for childhood neuroblastoma. J. Nucl. Med. 2011, 52, 1041–1047. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Kong, G.; Hofman, M.S.; Murray, W.K.; Wilson, S.; Wood, P.; Downie, P.; Super, L.; Hogg, A.; Eu, P.; Hicks, R.J. Initial Experience With Gallium-68 DOTA-Octreotate PET/CT and Peptide Receptor Radionuclide Therapy for Pediatric Patients With Refractory Metastatic Neuroblastoma. J. Pediatr. Hematol. Oncol. 2016, 38, 87–96. [Google Scholar] [CrossRef] [Green Version]
- Menda, Y.; O’Dorisio, M.S.; Kao, S.; Khanna, G.; Michael, S.; Connolly, M.; Babich, J.; O’Dorisio, T.; Bushnell, D.; Madsen, M. Phase I trial of 90Y-DOTATOC therapy in children and young adults with refractory solid tumors that express somatostatin receptors. J. Nucl. Med. 2010, 51, 1524–1531. [Google Scholar] [CrossRef] [Green Version]
- Gains, J.E.; Moroz, V.; Aldridge, M.D.; Wan, S.; Wheatley, K.; Laidler, J.; Peet, C.; Bomanji, J.B.; Gaze, M.N. A phase IIa trial of molecular radiotherapy with 177-lutetium DOTATATE in children with primary refractory or relapsed high-risk neuroblastoma. Eur. J. Nucl. Med. Mol. Imaging 2020, 47, 2348–2357. [Google Scholar] [CrossRef]
- Cullinane, C.; Jeffery, C.M.; Roselt, P.D.; van Dam, E.M.; Jackson, S.; Kuan, K.; Jackson, P.; Binns, D.; van Zuylekom, J.; Harris, M.J.; et al. Peptide Receptor Radionuclide Therapy with 67Cu-CuSarTATE Is Highly Efficacious Against a Somatostatin-Positive Neuroendocrine Tumor Model. J. Nucl. Med. 2020, 61, 1800–1805. [Google Scholar] [CrossRef]
- Dearling, J.L.J.; van Dam, E.M.; Harris, M.J.; Packard, A.B. Detection and therapy of neuroblastoma minimal residual disease using [(64/67)Cu]Cu-SARTATE in a preclinical model of hepatic metastases. EJNMMI Res. 2021, 11, 20. [Google Scholar] [CrossRef]
- Mirvis, E.; Toumpanakis, C.; Mandair, D.; Gnanasegaran, G.; Caplin, M.; Navalkissoor, S. Efficacy and tolerability of peptide receptor radionuclide therapy (PRRT) in advanced metastatic bronchial neuroendocrine tumours (NETs). Lung Cancer 2020, 150, 70–75. [Google Scholar] [CrossRef] [PubMed]
- Naraev, B.G.; Ramirez, R.A.; Kendi, A.T.; Halfdanarson, T.R. Peptide Receptor Radionuclide Therapy for Patients With Advanced Lung Carcinoids. Clin. Lung Cancer 2019, 20, e376–e392. [Google Scholar] [CrossRef] [Green Version]
- ClinicalTrials.gov. Testing Lutetium Lu 177 Dotatate in Patients with Somatostatin Receptor Positive Advanced Bronchial Neuroendocrine Tumors. Available online: https://clinicaltrials.gov/ct2/show/NCT04665739 (accessed on 22 May 2021).
- Lewin, J.; Cullinane, C.; Akhurst, T.; Waldeck, K.; Watkins, D.N.; Rao, A.; Eu, P.; Mileshkin, L.; Hicks, R.J. Peptide receptor chemoradionuclide therapy in small cell carcinoma: From bench to bedside. Eur. J. Nucl. Med. Mol. Imaging 2015, 42, 25–32. [Google Scholar] [CrossRef] [PubMed]
- Kim, C.; Liu, S.V.; Subramaniam, D.S.; Torres, T.; Loda, M.; Esposito, G.; Giaccone, G. Phase I study of the 177Lu-DOTA0-Tyr3-Octreotate (lutathera) in combination with nivolumab in patients with neuroendocrine tumors of the lung. J. Immunother. Cancer 2020, 8, e000980. [Google Scholar] [CrossRef]
- Maghsoomi, Z.; Emami, Z.; Malboosbaf, R.; Malek, M.; Khamseh, M.E. Efficacy and safety of peptide receptor radionuclide therapy in advanced radioiodine-refractory differentiated thyroid cancer and metastatic medullary thyroid cancer: A systematic review. BMC Cancer 2021, 21, 579. [Google Scholar] [CrossRef] [PubMed]
- Grossrubatscher, E.; Fanciulli, G.; Pes, L.; Sesti, F.; Dolci, C.; de Cicco, F.; Colao, A.; Faggiano, A.; Group, N. Advances in the Management of Medullary Thyroid Carcinoma: Focus on Peptide Receptor Radionuclide Therapy. J. Clin. Med. 2020, 9, 3507. [Google Scholar] [CrossRef]
WHO 2019 Gastrointestinal NEN Classification | WHO 2017 Pancreatic NEN Classification | WHO 2010 Gastroenteropancreatic NEN Classification |
---|---|---|
Well-differentiated NETs: • NET G1 • NET G2 • NET G3 | Well-differentiated NETs: • NET G1 • NET G2 • NET G3 | Well-differentiated NETs: • NET G1 • NET G2 |
Poorly differentiated NECs: • NEC (large cell or small cell NEC) | Poorly differentiated NECs: • NEC G3 (large cell or small cell NEC) | Poorly differentiated NECs: • NEC G3 (large cell or small cell NEC) |
Tumor-Related Factors | |
Imaging | SSTR positive, metastatic or inoperable NET with disease progression |
Lesion uptake should exceed background hepatic activity | |
Histology | G1/2 NET ideally * Ki-67 ≤20% ideally * |
Patient-Related Factors | |
Clinical | Increasing symptoms or disease progression |
ECOG performance status 0–2 or Karnofsy/Lansky performance status above 60% New York Heart Association grade <III Able to comply with radiation protection advice Discontinuation of long-acting ‘cold’ somatostatin analogues for 4–6 weeks Functioning syndromes—consider inpatient treatment | |
Renal function | Creatinine clearance >40 mL/min |
Liver function | Bilirubin <3 x upper limit of normal # |
Albumin >30 g/L # | |
Full blood count | Hb >8 g/dL WCC >3000/mm 3 Platelets >75,000/mm 3 |
90Y (Yttrium-90) | 177Lu (Lutetium-177) | |
---|---|---|
Emission spectrum | β− | β− and γ-emitter |
Physical half-life (days) | 2.7 | 6.7 |
Maximum beta energy (MeV) | 2.28 | 0.50 |
Particle penetration (mm) | 11.3 | 1.8 |
Imaging ability | Bremsstrahlung | γ emission |
α Particles | β Particles | |
---|---|---|
Particle type | 4He nucleus | Energetic electron |
Particle energy | 5–9 MeV | 50–2300 keV |
Particle path length | 50–100 μm | 0.05–12 mm |
Linear energy transfer | ~80 keV/μm | ~0.2 keV/μm |
Oxygenation | Effective in hypoxic tumors | Less effective in hypoxic tumors |
Bystander effect | Yes | Yes |
Tumor crossfire | Low | Yes |
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Naik, M.; Al-Nahhas, A.; Khan, S.R. Treatment of Neuroendocrine Neoplasms with Radiolabeled Peptides—Where Are We Now. Cancers 2022, 14, 761. https://doi.org/10.3390/cancers14030761
Naik M, Al-Nahhas A, Khan SR. Treatment of Neuroendocrine Neoplasms with Radiolabeled Peptides—Where Are We Now. Cancers. 2022; 14(3):761. https://doi.org/10.3390/cancers14030761
Chicago/Turabian StyleNaik, Mitesh, Adil Al-Nahhas, and Sairah R. Khan. 2022. "Treatment of Neuroendocrine Neoplasms with Radiolabeled Peptides—Where Are We Now" Cancers 14, no. 3: 761. https://doi.org/10.3390/cancers14030761