Rhenium-188 Labeled Radiopharmaceuticals: Current Clinical Applications in Oncology and Promising Perspectives

Lepareur, Nicolas; Lacœuille, Franck; Bouvry, Christelle; Hindré, François; Garcion, Emmanuel; Chérel, Michel; Noiret, Nicolas; Garin, Etienne; Knapp, F. F.  Russ

doi:10.3389/fmed.2019.00132

Title: Rhenium-188 Labeled Radiopharmaceuticals: Current Clinical Applications in Oncology and Promising Perspectives

Journal Article · 14 June 2019 · Frontiers in Medicine

DOI: https://doi.org/10.3389/fmed.2019.00132 · OSTI ID:1628049

Lepareur, Nicolas ^[1]; Lacœuille, Franck ^[2]; Bouvry, Christelle ^[3]; Hindré, François ^[4]; Garcion, Emmanuel ^[4]; Chérel, Michel ^[5]; Noiret, Nicolas ^[6]; Garin, Etienne ^[1]; Knapp, F. F. Russ ^[7]

Comprehensive Cancer Center Eugène Marquis, Rennes (France); Univ. Rennes (France). Inst. NUMECAN (Nutrition, Métabolismes et Cancer)
Angers Univ. Hospital, Angers (France); Angers Univ. (France). Univ. Nantes. CRCINA (Centre de Recherche en Cancérologie et Immunologie Nantes—Angers)
Comprehensive Cancer Center Eugène Marquis, Rennes (France); Univ Rennes, Rennes (France). CNRS, ISCR (Institut des Sciences Chimiques de Rennes)
Univ. Angers (France). Univ. Nantes. CRCINA (Centre de Recherche en Cancérologie et Immunologie Nantes—Angers); Univ.Angers (France). PRIMEX (Plateforme de Radiobiologie et d’Imagerie EXperimentale)
Univ. Angers (France). Univ. Nantes. CRCINA (Centre de Recherche en Cancérologie et Immunologie Nantes—Angers); ICO (Institut de Cancérologie de l’Ouest), Comprehensive Cancer Center René Gauducheau, Saint-Herblain (France)
Univ Rennes, Rennes (France). CNRS, ISCR (Institut des Sciences Chimiques de Rennes); ENSCR (Ecole Nationale Supérieure de Chimie de Rennes), Rennes (France)
Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Medical Radioisotopes Program

Rhenium-188 (¹⁸⁸Re) is a high energy beta-emitting radioisotope with a short 16.9 h physical half-life, which has been shown to be a very attractive candidate for use in therapeutic nuclear medicine. The high beta emission has an average energy of 784 keV and a maximum energy of 2.12 MeV, sufficient to penetrate and destroy targeted abnormal tissues. In addition, the low-abundant gamma emission of 155 keV (15%) is efficient for imaging and for dosimetric calculations. These key characteristics identify ¹⁸⁸Re as an important therapeutic radioisotope for routine clinical use. Moreover, the highly reproducible on-demand availability of ¹⁸⁸Re from the ¹⁸⁸W/¹⁸⁸Re generator system is an important feature and permits installation in hospital-based or central radiopharmacies for cost-effective availability of no-carrier-added (NCA) ¹⁸⁸Re. Rhenium-188 and technetium-99 m exhibit similar chemical properties and represent a “theranostic pair.” Thus, preparation and targeting of ¹⁸⁸Re agents for therapy is similar to imaging agents prepared with ^99mTc, the most commonly used diagnostic radionuclide. Over the last three decades, radiopharmaceuticals based on ¹⁸⁸Re-labeled small molecules, including peptides, antibodies, Lipiodol and particulates have been reported. The successful application of these ¹⁸⁸Re-labeled therapeutic radiopharmaceuticals has been reported in multiple early phase clinical trials for the management of various primary tumors, bone metastasis, rheumatoid arthritis, and endocoronary interventions. This article reviews the use of ¹⁸⁸Re-radiopharmaceuticals which have been investigated in patients for cancer treatment, demonstrating that 188Re represents a cost effective alternative for routine clinical use in comparison to more expensive and/or less readily available therapeutic radioisotopes.

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Research Organization:: Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States)

Sponsoring Organization:: USDOE Office of Science (SC)

Grant/Contract Number:: AC05-00OR22725

OSTI ID:: 1628049

Journal Information:: Frontiers in Medicine, Vol. 6; ISSN 2296-858X

Publisher:: Frontiers Media S.A.Copyright Statement

Country of Publication:: United States

Language:: English

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Preliminary results of the Phase 1 Lip-Re I clinical trial: biodistribution and dosimetry assessments in hepatocellular carcinoma patients treated with 188Re-SSS Lipiodol radioembolization Delaunay, Kostas; Edeline, Julien; Rolland, Yan European Journal of Nuclear Medicine and Molecular Imaging, Vol. 46, Issue 7 https://doi.org/10.1007/s00259-019-04277-9	journal	February 2019
99mTc(V)DMSA quantitatively predicts 188Re(V)DMSA distribution in patients with prostate cancer metastatic to bone Blower, P. J.; Kettle, A. G.; O'Doherty, M. J. European Journal of Nuclear Medicine, Vol. 27, Issue 9 https://doi.org/10.1007/s002590000307	journal	July 2000
Preparation and evaluation of the rhenium-188-labelled anti-NCA antigen monoclonal antibody BW 250/183 for radioimmunotherapy of leukaemia Seitz, Ulrike; Neumaier, Bernd; Glatting, Gerhard European Journal of Nuclear Medicine and Molecular Imaging, Vol. 26, Issue 10 https://doi.org/10.1007/s002590050582	journal	October 1999
The benefit of bone-seeking radiopharmaceuticals in the treatment of metastatic bone pain Liepe, Knut; Runge, Roswitha; Kotzerke, J�rg Journal of Cancer Research and Clinical Oncology, Vol. 131, Issue 1 https://doi.org/10.1007/s00432-004-0625-0	journal	September 2004
Radiopharmaceuticals for metastatic bone pain palliation: available options in the clinical domain and their comparisons Das, Tapas; Banerjee, Sharmila Clinical & Experimental Metastasis, Vol. 34, Issue 1 https://doi.org/10.1007/s10585-016-9831-9	journal	December 2016
Characterization of the distribution, retention, and efficacy of internal radiation of 188Re-lipid nanocapsules in an immunocompromised human glioblastoma model Cikankowitz, Annabelle; Clavreul, Anne; Tétaud, Clément Journal of Neuro-Oncology, Vol. 131, Issue 1 https://doi.org/10.1007/s11060-016-2289-4	journal	October 2016
Radiosynovectomy using yttrium-90, phosphorus-32 or rhenium-188 radiocolloids versus corticoid instillation for rheumatoid arthritis of the knee Liepe, Knut; Zaknun, John J.; Padhy, Ajit Annals of Nuclear Medicine, Vol. 25, Issue 5 https://doi.org/10.1007/s12149-011-0467-1	journal	February 2011
Preparation of rhenium-186 labelled EHDP and its possible use in the treatment of osseous neoplasms Mathieu, L.; Chevalier, P.; Galy, G. The International Journal of Applied Radiation and Isotopes, Vol. 30, Issue 12 https://doi.org/10.1016/0020-708x(79)90150-9	journal	December 1979
Labeling and biodistribution of different particle materials for radioembolization therapy with 188Re Wunderlich, Gerd; Pinkert, Jörg; Stintz, Michael Applied Radiation and Isotopes, Vol. 62, Issue 5 https://doi.org/10.1016/j.apradiso.2004.11.003	journal	May 2005
Development of semi-automated system for preparation of 188Re aqueous solutions of high and reproducible activity concentrations Jäckel, B.; Cripps, R.; Güntay, S. Applied Radiation and Isotopes, Vol. 63, Issue 3 https://doi.org/10.1016/j.apradiso.2005.04.009	journal	September 2005
Post-elution concentration of 188Re by an electrochemical method Chakravarty, Rubel; Dash, Ashutosh; Pillai, M. R. A. Applied Radiation and Isotopes, Vol. 68, Issue 12 https://doi.org/10.1016/j.apradiso.2010.06.022	journal	December 2010
Preparation and first biological evaluation of novel Re-188/Tc-99m peptide conjugates with substance-P Smilkov, Katarina; Janevik, Emilija; Guerrini, Remo Applied Radiation and Isotopes, Vol. 92 https://doi.org/10.1016/j.apradiso.2014.06.003	journal	September 2014
Structure-based optimization of GRP78-binding peptides that enhances efficacy in cancer imaging and therapy Wang, Sheng-Hung; Lee, Andy Chi-Lung; Chen, I-Ju Biomaterials, Vol. 94 https://doi.org/10.1016/j.biomaterials.2016.03.050	journal	July 2016
Re(VII) and Tc(VII) trioxo complexes stabilized by tridentate ligands and their potential use as radiopharmaceuticals Hahn, Eva M.; Casini, Angela; Kühn, Fritz E. Coordination Chemistry Reviews, Vol. 276 https://doi.org/10.1016/j.ccr.2014.05.021	journal	September 2014
Bone-Targeting Radiopharmaceuticals as Monotherapy or Combined With Chemotherapy in Patients With Castration-Resistant Prostate Cancer Metastatic to Bone Bouman-Wammes, Esther W.; de Klerk, John M. H.; Bloemendal, Haiko J. Clinical Genitourinary Cancer, Vol. 17, Issue 2 https://doi.org/10.1016/j.clgc.2018.11.014	journal	April 2019
Fibrin glue system for adjuvant brachytherapy of brain tumors with 188Re and 186Re-labeled microspheres Häfeli, Urs O.; Pauer, Gayle J.; Unnithan, Jaya European Journal of Pharmaceutics and Biopharmaceutics, Vol. 65, Issue 3 https://doi.org/10.1016/j.ejpb.2006.10.016	journal	March 2007
Transarterial radionuclide therapy with Re-188-HDD-lipiodol in case of unresectable hepatocellular carcinoma with extensive portal vein thrombosis Kumar, Ajay; Bal, Chandrashekhar; Srivastava, Deep Narayan European Journal of Radiology Extra, Vol. 56, Issue 2 https://doi.org/10.1016/j.ejrex.2005.07.016	journal	November 2005
Rhenium and technetium based radiopharmaceuticals: Development and recent advances Jürgens, Sophie; Herrmann, Wolfgang A.; Kühn, Fritz E. Journal of Organometallic Chemistry, Vol. 751 https://doi.org/10.1016/j.jorganchem.2013.07.042	journal	February 2014
Treatment with rhenium-188-perrhenate and iodine-131 of NIS-expressing mammary cancer in a mouse model remarkably inhibited tumor growth Dadachova, Ekaterina; Nguyen, Andrew; Lin, Elaine Y. Nuclear Medicine and Biology, Vol. 32, Issue 7 https://doi.org/10.1016/j.nucmedbio.2005.05.007	journal	October 2005
Evaluating the potential of 188Re-SOCTA–trastuzumab as a new radioimmunoagent for breast cancer treatment Luo, Tsai-Yueh; Tang, I-Chang; Wu, Yu-Long Nuclear Medicine and Biology, Vol. 36, Issue 1 https://doi.org/10.1016/j.nucmedbio.2008.10.014	journal	January 2009
Measurements of 186Re production cross section induced by deuterons on natW target at ARRONAX facility Guertin, Arnaud; Duchemin, Charlotte; Haddad, Ferid Nuclear Medicine and Biology, Vol. 41 https://doi.org/10.1016/j.nucmedbio.2013.11.003	journal	May 2014
Drug composition matters: the influence of carrier concentration on the radiochemical purity, hydroxyapatite affinity and in-vivo bone accumulation of the therapeutic radiopharmaceutical 188 Rhenium-HEDP Lange, R.; de Klerk, J. M. H.; Bloemendal, H. J. Nuclear Medicine and Biology, Vol. 42, Issue 5 https://doi.org/10.1016/j.nucmedbio.2015.01.007	journal	May 2015
Targeted therapy of osteosarcoma with radiolabeled monoclonal antibody to an insulin-like growth factor-2 receptor (IGF2R) Geller, David S.; Morris, Jonathan; Revskaya, Ekaterina Nuclear Medicine and Biology, Vol. 43, Issue 12 https://doi.org/10.1016/j.nucmedbio.2016.07.008	journal	December 2016
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Uptake of the 188Re(V)-DMSA complex by cervical carcinoma cells in nude mice: pharmacokinetics and dosimetry Garcı́a-Salinas, Laura; Ferro-Flores, Guillermina; Arteaga-Murphy, Consuelo Applied Radiation and Isotopes, Vol. 54, Issue 3 https://doi.org/10.1016/s0969-8043(00)00278-5	journal	March 2001
Preparation of 188Re-labeled paper for treating skin cancer Jeong, Jae Min; Lee, Yong Jin; Kim, Eun-Hee Applied Radiation and Isotopes, Vol. 58, Issue 5 https://doi.org/10.1016/s0969-8043(03)00063-0	journal	May 2003
Preparation of 188Re-RC-160 somatostatin analog: a peptide for local/regional radiotherapy Zamora, P. O.; Marek, M. J.; (Russ) Knapp, F. F. Applied Radiation and Isotopes, Vol. 48, Issue 3 https://doi.org/10.1016/s0969-8043(96)00226-6	journal	March 1997
An alternative approach to the preparation of 188Re radiopharmaceuticals from generator-produced [188ReO4]−: efficient synthesis of 188Re(V)-meso-2,3-dimercaptosuccinic acid Bolzati, Cristina; Boschi, Alessandra; Uccelli, Licia Nuclear Medicine and Biology, Vol. 27, Issue 3 https://doi.org/10.1016/s0969-8051(00)00079-2	journal	April 2000
Effect of reaction conditions on preparations of rhenium-188 hydroxyethylidene diphosphonate complexes Lin, Wan-Yu; Hsieh, Jih-Fang; Lin, Chih-Phoon Nuclear Medicine and Biology, Vol. 26, Issue 4 https://doi.org/10.1016/s0969-8051(99)00007-4	journal	May 1999
Comparison of various rhenium-188-labeled diphosphonates for the treatment of bone metastases Hsieh, Bor-Tsung; Hsieh, Jih-Fang; Tsai, Shih-Chuan Nuclear Medicine and Biology, Vol. 26, Issue 8 https://doi.org/10.1016/s0969-8051(99)00075-x	journal	November 1999
Phage Display Library Derived Peptides that Bind to Human Tumor Melanin as Potential Vehicles for Targeted Radionuclide Therapy of Metastatic Melanoma Howell, Robertha C.; Revskaya, Ekaterina; Pazo, Valeria Bioconjugate Chemistry, Vol. 18, Issue 6 https://doi.org/10.1021/bc060330u	journal	November 2007
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Investigation of SP94 Peptide as a Specific Probe for Hepatocellular Carcinoma Imaging and Therapy Li, Yanli; Hu, Yan; Xiao, Jie Scientific Reports, Vol. 6, Issue 1 https://doi.org/10.1038/srep33511	journal	September 2016
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The role of coordination chemistry in the development of copper and rhenium radiopharmaceuticals Donnelly, Paul S. Dalton Transactions, Vol. 40, Issue 5 https://doi.org/10.1039/c0dt01075h	journal	January 2011
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International Atomic Energy Agency-Sponsored Multination Study of Intra-Arterial Rhenium-188-Labeled Lipiodol in the Treatment of Inoperable Hepatocellular Carcinoma: Results With Special Emphasis on Prognostic Value of Dosimetric Study Bernal, Patricia; Raoul, Jean-Luc; Stare, Janez Seminars in Nuclear Medicine, Vol. 38, Issue 2 https://doi.org/10.1053/j.semnuclmed.2007.10.006	journal	March 2008
Dead cells in melanoma tumors provide abundant antigen for targeted delivery of ionizing radiation by a mAb to melanin Dadachova, E.; Nosanchuk, J. D.; Shi, L. Proceedings of the National Academy of Sciences, Vol. 101, Issue 41 https://doi.org/10.1073/pnas.0406180101	journal	October 2004
Nontoxic radioactive Listeriaat is a highly effective therapy against metastatic pancreatic cancer Quispe-Tintaya, W.; Chandra, D.; Jahangir, A. Proceedings of the National Academy of Sciences, Vol. 110, Issue 21 https://doi.org/10.1073/pnas.1211287110	journal	April 2013
188 Re-labeled Anti-CD66 Monoclonal Antibody in Stem Cell Transplantation for Patients with High-risk Acute Myeloid Leukemia Bunjes, Donald Leukemia & Lymphoma, Vol. 43, Issue 11 https://doi.org/10.1080/1042819021000033015	journal	January 2002
Radiobiological characterization of post-lumpectomy focal brachytherapy with lipid nanoparticle-carried radionuclides Hrycushko, Brian A.; Gutierrez, Alonso N.; Goins, Beth Physics in Medicine and Biology, Vol. 56, Issue 3 https://doi.org/10.1088/0031-9155/56/3/011	journal	January 2011
Rhenium-188-HEDP in the Palliative Treatment of Bone Metastases Liepe, Knut; Hliscs, Reiner; Kropp, Joachim Cancer Biotherapy and Radiopharmaceuticals, Vol. 15, Issue 3 https://doi.org/10.1089/108497800414356	journal	June 2000
Rhenium-188-HEDP Therapy for the Palliation of Pain Due to Osseous Metastases in Lung Cancer Patients Zhang, Hong; Tian, Mei; Li, Sijing Cancer Biotherapy and Radiopharmaceuticals, Vol. 18, Issue 5 https://doi.org/10.1089/108497803770418265	journal	October 2003
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The Tolerance and Therapeutic Efficacy of Rhenium-188 Hydroxyethylidene Diphosphonate in Advanced Cancer Patients with Painful Osseous Metastases Cheng, Aiping; Chen, Shaoliang; Zhang, Ying Cancer Biotherapy and Radiopharmaceuticals, Vol. 26, Issue 2 https://doi.org/10.1089/cbr.2010.0873	journal	April 2011
Targeted therapy in nuclear medicine current status and future prospects Oyen, W. J. G.; Bodei, L.; Giammarile, F. Annals of Oncology, Vol. 18, Issue 11 https://doi.org/10.1093/annonc/mdm111	journal	April 2007
Significant Reduction of the Mass of Bone Metastasis 1 Year After Rhenium-186 HEDP Pain Palliation Therapy Liepe, Knut; Kropp, Joachim; Hliscs, Rainer Clinical Nuclear Medicine, Vol. 25, Issue 11 https://doi.org/10.1097/00003072-200011000-00009	journal	January 2000
188Re(V)-DMSA revisited: Preparation and biodistribution of a potential radiotherapeutic agent with low kidney uptake Dadachova, E.; Chapman, J. Nuclear Medicine Communications, Vol. 19, Issue 2 https://doi.org/10.1097/00006231-199802000-00012	journal	January 1998
Management of multiple intrahepatic recurrences after radiofrequency ablation of hepatocellular carcinoma with rhenium-188???HDD-lipiodol Kumar, Ajay; Bal, Chandrasekhar; Srivastava, Deep Narayan European Journal of Gastroenterology & Hepatology, Vol. 18, Issue 2 https://doi.org/10.1097/00042737-200602000-00016	journal	January 2006
Management of Postsurgical Recurrence of Hepatocellular Carcinoma with Rhenium 188–HDD Labeled Iodized Oil Kumar, Ajay; Srivastava, Deep N.; Bal, Chandrasekhar Journal of Vascular and Interventional Radiology, Vol. 17, Issue 1 https://doi.org/10.1097/01.rvi.0000195321.20579.f2	journal	January 2006
A comparative study of 188Re-HEDP, 186Re-HEDP, 153Sm-EDTMP and 89Sr in the treatment of painful skeletal metastases Liepe, Knut; Kotzerke, Joerg Nuclear Medicine Communications, Vol. 28, Issue 8 https://doi.org/10.1097/mnm.0b013e32825a6adc	journal	January 2007
Biodistribution and internal dosimetry of the 188Re-labelled humanized monoclonal antibody anti-epidemal growth factor receptor, nimotuzumab, in the locoregional treatment of malignant gliomas Torres, Leonel A.; Coca, Marco A.; Batista, Juan F. Nuclear Medicine Communications, Vol. 29, Issue 1 https://doi.org/10.1097/mnm.0b013e3282f1bbce	journal	January 2008
188Re or 90Y-labelled anti-CD66 antibody as part of a dose-reduced conditioning regimen for patients with acute leukaemia or myelodysplastic syndrome over the age of 55: results of a phase I-II study Ringhoffer, Mark; Blumstein, Norbert; Neumaier, Bernd British Journal of Haematology, Vol. 130, Issue 4 https://doi.org/10.1111/j.1365-2141.2005.05663.x	journal	August 2005
¹⁸⁸ Re anti-CD66 radioimmunotherapy combined with reduced-intensity conditioning and in-vivo T cell depletion in elderly patients undergoing allogeneic haematopoietic cell transplantation Lauter, Anett; Strumpf, Annette; Platzbecker, Uwe British Journal of Haematology, Vol. 148, Issue 6 https://doi.org/10.1111/j.1365-2141.2009.08025.x	journal	March 2010
Dermatological high-dose-rate brachytherapy for the treatment of basal and squamous cell carcinoma Sedda, A. F.; Rossi, G.; Cipriani, C. Clinical and Experimental Dermatology, Vol. 33, Issue 6 https://doi.org/10.1111/j.1365-2230.2008.02852.x	journal	November 2008
Radiolabeled Antibodies to Bacillus anthracis Toxins Are Bactericidal and Partially Therapeutic in Experimental Murine Anthrax Rivera, Johanna; Nakouzi, Antonio S.; Morgenstern, Alfred Antimicrobial Agents and Chemotherapy, Vol. 53, Issue 11 https://doi.org/10.1128/aac.01269-08	journal	August 2009
Inoperable Hepatocellular Carcinoma: Transarterial ¹⁸⁸ Re HDD–Labeled Iodized Oil for Treatment—Prospective Multicenter Clinical Trial Kumar, Ajay; Srivastava, Deep Narayan; Chau, Trinh Thi Minh Radiology, Vol. 243, Issue 2 https://doi.org/10.1148/radiol.2432051246	journal	May 2007
Safety and Efficacy of 188-Rhenium-Labeled Antibody to Melanin in Patients with Metastatic Melanoma Klein, M.; Lotem, M.; Peretz, T. Journal of Skin Cancer, Vol. 2013 https://doi.org/10.1155/2013/828329	journal	January 2013
Monoclonal Antibodies Radiolabeling with Rhenium-188 for Radioimmunotherapy Uccelli, Licia; Martini, Petra; Pasquali, Micol BioMed Research International, Vol. 2017 https://doi.org/10.1155/2017/5923609	journal	January 2017
Studies on Neoplasms with the aid of Radioactive Phosphorus. i. the Total Phosphorus Metabolism of Normal and Leukemic mice 1 Lawrence, J. H.; Tuttle, L. W.; Scott, K. G. Journal of Clinical Investigation, Vol. 19, Issue 2 https://doi.org/10.1172/jci101129	journal	March 1940
Unrelated marrow transplantation for adult patients with poor-risk acute lymphoblastic leukemia: strong graft-versus-leukemia effect and risk factors determining outcome Cornelissen, Jan J.; Carston, Michael; Kollman, Craig Blood, Vol. 97, Issue 6 https://doi.org/10.1182/blood.v97.6.1572	journal	March 2001
Repeated Bone-Targeted Therapy for Hormone-Refractory Prostate Carcinoma: Randomized Phase II Trial With the New, High-Energy Radiopharmaceutical Rhenium-188 Hydroxyethylidenediphosphonate Palmedo, Holger; Manka-Waluch, Agnieska; Albers, Peter Journal of Clinical Oncology, Vol. 21, Issue 15 https://doi.org/10.1200/jco.2003.12.060	journal	August 2003
Initial Study of Radiological and Clinical Efficacy Radioembolization Using 188Re-Human Serum Albumin (HSA) Microspheres in Patients with Progressive, Unresectable Primary or Secondary Liver Cancers Pawlak, Dariusz Medical Science Monitor, Vol. 20 https://doi.org/10.12659/msm.890480	journal	January 2014
68Ga and 188Re Starch-Based Microparticles as Theranostic Tool for the Hepatocellular Carcinoma: Radiolabeling and Preliminary In Vivo Rat Studies Verger, Elise; Drion, Pierre; Meffre, Geneviève PLOS ONE, Vol. 11, Issue 10 https://doi.org/10.1371/journal.pone.0164626	journal	October 2016
Burn-up Cross-Section of 188W Mirzadeh, Saed; Knapp, F. F. (Russ); Lambrecht, Richard M. Radiochimica Acta, Vol. 77, Issue 1-2 https://doi.org/10.1524/ract.1997.77.12.99	journal	January 1997
A perspective view of sodium iodide symporter research and its clinical implications Riesco-Eizaguirre, Garcilaso; Santisteban, Pilar European Journal of Endocrinology, Vol. 155, Issue 4 https://doi.org/10.1530/eje.1.02257	journal	October 2006
Rhenium-188 Radiochemistry: Challenges and Prospects Blower, Philip International Journal of Nuclear Medicine Research, Issue Special - 2017 https://doi.org/10.15379/2408-9788.2017.04	journal	July 2017
Transarterial Radionuclide Therapy with 188Re-Labelled Lipiodol Lepareur, N. International Journal of Nuclear Medicine Research, Issue Special - 2017 https://doi.org/10.15379/2408-9788.2017.07	journal	July 2017
188 Re Zoledronic Acid in the Palliative Treatment of Painful Bone Metastases Kochetova, Tatiana International Journal of Nuclear Medicine Research, Issue Special - 2017 https://doi.org/10.15379/2408-9788.2017.08	journal	July 2017
Personalized High-Dose-Rate Brachytherapy with Non-Sealed Rhenium-188 in Non-Melanoma Skin Cancer Cipriani, Cesidio International Journal of Nuclear Medicine Research, Issue Special - 2017 https://doi.org/10.15379/2408-9788.2017.11	journal	July 2017
Radiovirotherapy: Principles and Prospects in Oncology Touchefeu, Y.; Franken, P.; J. Harrington, K. Current Pharmaceutical Design, Vol. 18, Issue 22 https://doi.org/10.2174/1381612811209023313	journal	May 2012
Rhenium-188: Availability from the 188W/188Re Generator and Status of Current Applications R. A. Pillai, M.; Dash, Ashutosh; F. Knapp, F. Current Radiopharmaceuticals, Vol. 5, Issue 3 https://doi.org/10.2174/1874471011205030228	journal	June 2012
Radiolabeling, Characteristics and NanoSPECT/CT Imaging of 188Re-cetuximab in NCI-H292 Human Lung Cancer Xenografts Kuo, Wan-I; Cheng, Kai-Hung; Chang, Ya-Jen Anticancer Research, Vol. 39, Issue 1 https://doi.org/10.21873/anticanres.13096	journal	December 2018
Inhibitory effects of Rhenium-188-labeled Herceptin on prostate cancer cell growth: A possible radioimmunotherapy to prostate carcinoma Wang, Hsin-Yi; Lin, Wan-Yu; Chen, Mei-Chih International Journal of Radiation Biology, Vol. 89, Issue 5 https://doi.org/10.3109/09553002.2013.762136	journal	February 2013
The Potential and Hurdles of Targeted Alpha Therapy – Clinical Trials and Beyond Elgqvist, Jörgen; Frost, Sofia; Pouget, Jean-Pierre Frontiers in Oncology, Vol. 3 https://doi.org/10.3389/fonc.2013.00324	journal	January 2014
Re-188 Enhances the Inhibitory Effect of Bevacizumab in Non-Small-Cell Lung Cancer Xiao, Jie; Xu, Xiaobo; Li, Xiao Molecules, Vol. 21, Issue 10 https://doi.org/10.3390/molecules21101308	journal	September 2016
Treatment of painful bone metastases in prostate and breast cancer patients with the therapeutic radiopharmaceutical rhenium-188-HEDP: Clinical benefit in a real-world study Lange, Rogier; Overbeek, Floor; de Klerk, John Nuklearmedizin, Vol. 55, Issue 05 https://doi.org/10.3413/nukmed-0828-16-05	journal	January 2016

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