Alpha-Emitters and Targeted Alpha Therapy in Oncology: from Basic Science to Clinical Investigations

Makvandi, Mehran; Dupis, Edouard; Engle, Jonathan W.; Nortier, F. Meiring; Fassbender, Michael E.; Simon, Sam; Birnbaum, Eva R.; Atcher, Robert W.; John, Kevin D.; Rixe, Olivier; Norenberg, Jeffrey P.

doi:10.1007/s11523-018-0550-9

Alpha-Emitters and Targeted Alpha Therapy in Oncology: from Basic Science to Clinical Investigations

Journal Article · Thu Feb 08 00:00:00 EST 2018 · Targeted Oncology

DOI:https://doi.org/10.1007/s11523-018-0550-9· OSTI ID:1459839

Makvandi, Mehran ^[1]; Dupis, Edouard ^[2]; Engle, Jonathan W. ^[3]; Nortier, F. Meiring ^[3]; Fassbender, Michael E. ^[3]; Simon, Sam ^[1]; Birnbaum, Eva R. ^[3]; Atcher, Robert W. ^[4]; John, Kevin D. ^[3]; Rixe, Olivier ^[2]; Norenberg, Jeffrey P. ^[1]

Univ. of New Mexico, Albuquerque, NM (United States). Radiopharmaceutical Sciences Program. College of Pharmacy. Health Sciences Center
Univ. of New Mexico Comprehensive Cancer Center, Albuquerque, NM (United States). Experimental Therapeutics Unit
Los Alamos National Lab. (LANL), Los Alamos, NM (United States)
Univ. of New Mexico, Albuquerque, NM (United States). Radiopharmaceutical Sciences Program. College of Pharmacy. Health Sciences Center; Los Alamos National Lab. (LANL), Los Alamos, NM (United States)

Alpha-emitters are radionuclides that decay through the emission of high linear energy transfer α-particles and possess favorable pharmacologic profiles for cancer treatment. When coupled with monoclonal antibodies, peptides, small molecules, or nanoparticles, the excellent cytotoxic capability of α-particle emissions has generated a strong interest in exploring targeted α-therapy in the pre-clinical setting and more recently in clinical trials in oncology. Multiple obstacles have been overcome by researchers and clinicians to accelerate the development of targeted α-therapies, especially with the recent improvement in isotope production and purification, but also with the development of innovative strategies for optimized targeting. Numerous studies have demonstrated the in vitro and in vivo efficacy of the targeted α-therapy. Radium-223 (²²³Ra) dichloride (Xofigo®) is the first α-emitter to have received FDA approval for the treatment of prostate cancer with metastatic bone lesions. There is a significant increase in the number of clinical trials in oncology using several radionuclides such as Actinium-225 (²²⁵Ac), Bismuth-213 (²¹³Bi), Lead-212 (²¹²Pb), Astatine (²¹¹At) or Radium-223 (²²³Ra) assessing their safety and preliminary activity. Finally, this review will cover their therapeutic application as well as summarize the investigations that provide the foundation for further clinical development.

View Accepted Manuscript (DOE)

Research Organization:: Los Alamos National Lab. (LANL), Los Alamos, NM (United States); Univ. of New Mexico, Albuquerque, NM (United States)

Sponsoring Organization:: USDOE

Grant/Contract Number:: AC52-06NA25396

OSTI ID:: 1459839

Report Number(s):: LA-UR--16-27976

Journal Information:: Targeted Oncology, Journal Name: Targeted Oncology Journal Issue: 2 Vol. 13; ISSN 1776-2596

Publisher:: SpringerCopyright Statement

Country of Publication:: United States

Language:: English

References (84)

Improved efficacy of α-particle-targeted radiation therapy: Dual targeting of human epidermal growth factor receptor-2 and tumor-associated glycoprotein 72 Milenic, Diane E.; Brady, Erik D.; Garmestani, Kayhan Cancer, Vol. 116, Issue S4 https://doi.org/10.1002/cncr.24793	journal	February 2010
Design and evaluation of an external high-current target for production of ²¹¹ At Gagnon, K.; Risler, R.; Pal, S. Journal of Labelled Compounds and Radiopharmaceuticals, Vol. 55, Issue 12 https://doi.org/10.1002/jlcr.2968	journal	October 2012
Targeted alpha-radionuclide therapy of functionally critically located gliomas with 213Bi-DOTA-[Thi8,Met(O2)11]-substance P: a pilot trial Cordier, D.; Forrer, F.; Bruchertseifer, F. European Journal of Nuclear Medicine and Molecular Imaging, Vol. 37, Issue 7 https://doi.org/10.1007/s00259-010-1385-5	journal	February 2010
213Bi-DOTATOC receptor-targeted alpha-radionuclide therapy induces remission in neuroendocrine tumours refractory to beta radiation: a first-in-human experience Kratochwil, C.; Giesel, F. L.; Bruchertseifer, F. European Journal of Nuclear Medicine and Molecular Imaging, Vol. 41, Issue 11 https://doi.org/10.1007/s00259-014-2857-9	journal	July 2014
213Bi-PSMA-617 targeted alpha-radionuclide therapy in metastatic castration-resistant prostate cancer Sathekge, Mike; Knoesen, Otto; Meckel, Marian European Journal of Nuclear Medicine and Molecular Imaging, Vol. 44, Issue 6 https://doi.org/10.1007/s00259-017-3657-9	journal	March 2017
Radioimmunotherapy with alpha-emitting nuclides McDevitt, Michael R.; Sgouros, George; Finn, Ronald D. European Journal of Nuclear Medicine and Molecular Imaging, Vol. 25, Issue 9 https://doi.org/10.1007/s002590050306	journal	September 1998
An overview of targeted alpha therapy Kim, Young-Seung; Brechbiel, Martin W. Tumor Biology, Vol. 33, Issue 3 https://doi.org/10.1007/s13277-011-0286-y	journal	December 2011
Evaluation of an internal cyclotron target for the production of 211At via the 209Bi (α,2n)211At reaction Larsen, Roy H.; Wieland, Bruce W.; Zalutsky, Michael R. Applied Radiation and Isotopes, Vol. 47, Issue 2 https://doi.org/10.1016/0969-8043(95)00285-5	journal	February 1996
Dry-distillation of astatine-211 from irradiated bismuth targets: a time-saving procedure with high recovery yields Lindegren, Sture; Bäck, Tom; Jensen, Holger J. Applied Radiation and Isotopes, Vol. 55, Issue 2 https://doi.org/10.1016/S0969-8043(01)00044-6	journal	August 2001
An²²⁵Ac/²¹³Bi generator system for therapeutic clinical applications: construction and operation McDevitt, Michael R.; Finn, Ronald D.; Sgouros, George Applied Radiation and Isotopes, Vol. 50, Issue 5, p. 895-904 https://doi.org/10.1016/S0969-8043(98)00151-1	journal	May 1999
New insights on cell death from radiation exposure Prise, Kevin M.; Schettino, Giuseppe; Folkard, Melvyn The Lancet Oncology, Vol. 6, Issue 7 https://doi.org/10.1016/S1470-2045(05)70246-1	journal	July 2005
A new internal target system for production of 211At on the cyclotron U-120M Lebeda, O.; Jiran, R.; Ráliš, J. Applied Radiation and Isotopes, Vol. 63, Issue 1 https://doi.org/10.1016/j.apradiso.2005.02.006	journal	July 2005
Proton-induced cross sections relevant to production of 225Ac and 223Ra in natural thorium targets below 200MeV Weidner, J. W.; Mashnik, S. G.; John, K. D. Applied Radiation and Isotopes, Vol. 70, Issue 11 https://doi.org/10.1016/j.apradiso.2012.07.006	journal	November 2012
Production of 211 At by a vertical beam irradiation method Nagatsu, Kotaro; Minegishi, Katsuyuki; Fukada, Masami Applied Radiation and Isotopes, Vol. 94 https://doi.org/10.1016/j.apradiso.2014.09.012	journal	December 2014
Large scale accelerator production of 225Ac: Effective cross sections for 78–192 MeV protons incident on 232Th targets Griswold, J. R.; Medvedev, D. G.; Engle, J. W. Applied Radiation and Isotopes, Vol. 118 https://doi.org/10.1016/j.apradiso.2016.09.026	journal	December 2016
A kit method for the high level synthesis of [211At]MABG Vaidyanathan, Ganesan; Affleck, Donna J.; Alston, Kevin L. Bioorganic & Medicinal Chemistry, Vol. 15, Issue 10 https://doi.org/10.1016/j.bmc.2007.03.016	journal	May 2007
A randomized, dose–response, multicenter phase II study of radium-223 chloride for the palliation of painful bone metastases in patients with castration-resistant prostate cancer Nilsson, S.; Strang, P.; Aksnes, A. K. European Journal of Cancer, Vol. 48, Issue 5 https://doi.org/10.1016/j.ejca.2011.12.023	journal	March 2012
Mitigation of radiation nephropathy after internal α-particle irradiation of kidneys Jaggi, Jaspreet Singh; Seshan, Surya V.; McDevitt, Michael R. International Journal of Radiation OncologyBiologyPhysics, Vol. 64, Issue 5 https://doi.org/10.1016/j.ijrobp.2005.11.036	journal	April 2006
Absorbed Doses and Risk Estimates of 211At-MX35 F(ab')2 in Intraperitoneal Therapy of Ovarian Cancer Patients Cederkrantz, Elin; Andersson, Håkan; Bernhardt, Peter International Journal of Radiation OncologyBiologyPhysics, Vol. 93, Issue 3 https://doi.org/10.1016/j.ijrobp.2015.07.005	journal	November 2015
Targeted α-particle radiotherapy with ²¹¹At-labeled monoclonal antibodies Zalutsky, Michael R.; Reardon, David A.; Pozzi, Oscar R. Nuclear Medicine and Biology, Vol. 34, Issue 7, p. 779-785 https://doi.org/10.1016/j.nucmedbio.2007.03.007	journal	October 2007
Preparation and evaluation of an astatine-211-labeled sigma receptor ligand for alpha radionuclide therapy Ogawa, Kazuma; Mizuno, Yoshiaki; Washiyama, Kohshin Nuclear Medicine and Biology, Vol. 42, Issue 11 https://doi.org/10.1016/j.nucmedbio.2015.07.001	journal	November 2015
The pre-clinical characterization of an alpha-emitting sigma-2 receptor targeted radiotherapeutic Makvandi, Mehran; Lieberman, Brian P.; LeGeyt, Ben Nuclear Medicine and Biology, Vol. 43, Issue 1 https://doi.org/10.1016/j.nucmedbio.2015.10.001	journal	January 2016
B7-H3-targeted 212Pb radioimmunotherapy of ovarian cancer in preclinical models Kasten, Benjamin B.; Arend, Rebecca C.; Katre, Ashwini A. Nuclear Medicine and Biology, Vol. 47 https://doi.org/10.1016/j.nucmedbio.2017.01.003	journal	April 2017
Bystander effects and radiotherapy Marín, Alicia; Martín, Margarita; Liñán, Olga Reports of Practical Oncology & Radiotherapy, Vol. 20, Issue 1 https://doi.org/10.1016/j.rpor.2014.08.004	journal	January 2015
Enhanced Retention of the α-Particle-Emitting Daughters of Actinium-225 by Liposome Carriers Sofou, Stavroula; Kappel, Barry J.; Jaggi, Jaspreet S. Bioconjugate Chemistry, Vol. 18, Issue 6 https://doi.org/10.1021/bc070075t	journal	November 2007
LaPO ₄ Nanoparticles Doped with Actinium-225 that Partially Sequester Daughter Radionuclides Woodward, Jonathan; Kennel, Stephen J.; Stuckey, Alan Bioconjugate Chemistry, Vol. 22, Issue 4 https://doi.org/10.1021/bc100574f	journal	April 2011
Enhanced Loading Efficiency and Retention of ²²⁵ Ac in Rigid Liposomes for Potential Targeted Therapy of Micrometastases Chang, Min-Yuan; Seideman, Jonathan; Sofou, Stavroula Bioconjugate Chemistry, Vol. 19, Issue 6 https://doi.org/10.1021/bc700440a	journal	June 2008
Treatment of Metastatic Bone Disease and the Emerging Role of Radium-223 Coleman, Robert Seminars in Nuclear Medicine, Vol. 46, Issue 2 https://doi.org/10.1053/j.semnuclmed.2015.10.012	journal	March 2016
Production of α-particle emitting ²¹¹ At using 45 MeV α-beam Kim, Gyehong; Chun, Kwonsoo; Park, Sung Ho Physics in Medicine and Biology, Vol. 59, Issue 11 https://doi.org/10.1088/0031-9155/59/11/2849	journal	May 2014
Evaluation of ²²⁵ Ac for Vascular Targeted Radioimmunotherapy of Lung Tumors Kennel, Stephen J.; Chappell, Lara L.; Dadachova, Kate Cancer Biotherapy and Radiopharmaceuticals, Vol. 15, Issue 3 https://doi.org/10.1089/108497800414329	journal	June 2000
α-Particle Radioimmunotherapy of Disseminated Peritoneal Disease Using a ²¹² Pb-Labeled Radioimmunoconjugate Targeting HER2 Milenic, Diane E.; Garmestani, Kayhan; Brady, Erik D. Cancer Biotherapy and Radiopharmaceuticals, Vol. 20, Issue 5 https://doi.org/10.1089/cbr.2005.20.557	journal	October 2005
Pharmacokinetics and Imaging of ²¹² Pb-TCMC-Trastuzumab After Intraperitoneal Administration in Ovarian Cancer Patients Meredith, Ruby F.; Torgue, Julien; Azure, Michael T. Cancer Biotherapy and Radiopharmaceuticals, Vol. 29, Issue 1 https://doi.org/10.1089/cbr.2013.1531	journal	February 2014
Patient-reported quality-of-life analysis of radium-223 dichloride from the phase III ALSYMPCA study Nilsson, S.; Cislo, P.; Sartor, O. Annals of Oncology, Vol. 27, Issue 5 https://doi.org/10.1093/annonc/mdw065	journal	February 2016
Metabolic Characteristics Within a Chemical Family Durbin, Patricia W. Health Physics, Vol. 2, Issue 3 https://doi.org/10.1097/00004032-195907000-00001	journal	January 1959
The Metabolism of Actinium in the Rat Taylor, D. M. Health Physics, Vol. 19, Issue 3 https://doi.org/10.1097/00004032-197009000-00004	journal	January 1970
Cytotoxicity of 213Bi- and 225Ac-immunoconjugates Kaspersen, F. M.; Bos, E.; Doornmalen, A. V. Nuclear Medicine Communications, Vol. 16, Issue 6 https://doi.org/10.1097/00006231-199506000-00009	journal	January 1995
Radioimmunotherapy with Bismuth-213 as Conditioning for Nonmyeloablative Allogeneic Hematopoietic Cell Transplantation in Dogs: A Dose Deescalation Study Bethge, Wolfgang A.; Wilbur, D. Scott; Storb, Rainer Transplantation, Vol. 78, Issue 3 https://doi.org/10.1097/01.TP.0000128853.62545.B2	journal	January 2004
Safety and Outcome Measures of First-in-Human Intraperitoneal α Radioimmunotherapy With 212Pb-TCMC-Trastuzumab Meredith, Ruby F.; Torgue, Julien J.; Rozgaja, Tania A. American Journal of Clinical Oncology, Vol. 41, Issue 7 https://doi.org/10.1097/COC.0000000000000353	journal	January 2018
Preliminary Production of 211At at the Texas A&M University Cyclotron Institute Martin, Thomas Michael; Bhakta, Vihar; Al-Harbi, Abeer Health Physics, Vol. 107, Issue 1 https://doi.org/10.1097/HP.0000000000000042	journal	January 2014
Modification of Radiation Damage by Fractionation of the Dose, Anoxia, and Chemical Protectors in Relation to let Barendsen, G. W. Annals of the New York Academy of Sciences, Vol. 114, Issue 1 https://doi.org/10.1111/j.1749-6632.1964.tb53565.x	journal	March 1964
Theoretical estimation of absorbed dose to organs in radioimmunotherapy using radionuclides with multiple unstable daughters Hamacher, K. A.; Sgouros, G. Medical Physics, Vol. 28, Issue 9 https://doi.org/10.1118/1.1395026	journal	September 2001
A schema for estimating absorbed dose to organs following the administration of radionuclides with multiple unstable daughters: A matrix approach Hamacher, K. A.; Sgouros, G. Medical Physics, Vol. 26, Issue 12 https://doi.org/10.1118/1.598788	journal	December 1999
Efforts to Control the Errant Products of a Targeted In vivo Generator Singh Jaggi, Jaspreet; Kappel, Barry J.; McDevitt, Michael R. Cancer Research, Vol. 65, Issue 11 https://doi.org/10.1158/0008-5472.CAN-04-3096	journal	June 2005
Breaking Chemoresistance and Radioresistance with [ ²¹³ Bi]anti-CD45 Antibodies in Leukemia Cells Friesen, Claudia; Glatting, Gerhard; Koop, Bernd Cancer Research, Vol. 67, Issue 5 https://doi.org/10.1158/0008-5472.CAN-06-3569	journal	March 2007
Radioimmunotherapy of Breast Cancer Metastases with -Particle Emitter 225Ac: Comparing Efficacy with 213Bi and 90Y Song, H.; Hobbs, R. F.; Vajravelu, R. Cancer Research, Vol. 69, Issue 23 https://doi.org/10.1158/0008-5472.CAN-09-1828	journal	November 2009
Selective Killing of Tumor Neovasculature Paradoxically Improves Chemotherapy Delivery to Tumors Escorcia, F. E.; Henke, E.; McDevitt, M. R. Cancer Research, Vol. 70, Issue 22 https://doi.org/10.1158/0008-5472.CAN-10-2029	journal	November 2010
First Clinical Experience with -Emitting Radium-223 in the Treatment of Skeletal Metastases Nilsson, S. Clinical Cancer Research, Vol. 11, Issue 12 https://doi.org/10.1158/1078-0432.CCR-04-2244	journal	June 2005
Melanoma Therapy via Peptide-Targeted -Radiation Miao, Y. Clinical Cancer Research, Vol. 11, Issue 15 https://doi.org/10.1158/1078-0432.CCR-05-0619	journal	August 2005
213Bi-[DOTA0, Tyr3]Octreotide Peptide Receptor Radionuclide Therapy of Pancreatic Tumors in a Preclinical Animal Model Norenberg, J. P. Clinical Cancer Research, Vol. 12, Issue 3 https://doi.org/10.1158/1078-0432.CCR-05-1264	journal	February 2006
Preclinical Evaluation of the α-Particle Generator Nuclide ²²⁵Ac for Somatostatin Receptor Radiotherapy of Neuroendocrine Tumors Miederer, M.; Henriksen, G.; Alke, A. Clinical Cancer Research, Vol. 14, Issue 11, p. 3555-3561 https://doi.org/10.1158/1078-0432.CCR-07-4647	journal	June 2008
Sequential Cytarabine and α-Particle Immunotherapy with Bismuth-213–Lintuzumab (HuM195) for Acute Myeloid Leukemia Rosenblat, Todd L.; McDevitt, Michael R.; Mulford, Deborah A. Clinical Cancer Research, Vol. 16, Issue 21 https://doi.org/10.1158/1078-0432.CCR-10-0382	journal	September 2010
Radium Ra 223 Dichloride Injection: U.S. Food and Drug Administration Drug Approval Summary Kluetz, P. G.; Pierce, W.; Maher, V. E. Clinical Cancer Research, Vol. 20, Issue 1 https://doi.org/10.1158/1078-0432.CCR-13-2665	journal	November 2013
Improved tumor imaging and therapy via i.v. IgG–mediated time-sequential modulation of neonatal Fc receptor Singh Jaggi, Jaspreet; Carrasquillo, Jorge A.; Seshan, Surya V. Journal of Clinical Investigation, Vol. 117, Issue 9 https://doi.org/10.1172/JCI32226	journal	September 2007
Targeted deletion of T-cell clones using alpha-emitting suicide MHC tetramers Yuan, Rui Rong; Wong, Phillip; McDevitt, Michael R. Blood, Vol. 104, Issue 8 https://doi.org/10.1182/blood-2004-01-0324	journal	October 2004
Astatine-211 conjugated to an anti-CD20 monoclonal antibody eradicates disseminated B-cell lymphoma in a mouse model Green, Damian J.; Shadman, Mazyar; Jones, Jon C. Blood, Vol. 125, Issue 13 https://doi.org/10.1182/blood-2014-11-612770	journal	March 2015
Targeted α particle immunotherapy for myeloid leukemia Jurcic, Joseph G.; Larson, Steven M.; Sgouros, George Blood, Vol. 100, Issue 4 https://doi.org/10.1182/blood.V100.4.1233.h81602001233_1233_1239	journal	August 2002
Improved safety and efficacy of 213Bi-DOTATATE-targeted alpha therapy of somatostatin receptor-expressing neuroendocrine tumors in mice pre-treated with l-lysine Chan, Ho Sze; Konijnenberg, Mark W.; Daniels, Tamara EJNMMI Research, Vol. 6, Issue 1 https://doi.org/10.1186/s13550-016-0240-5	journal	November 2016
Phase I trial of α-particle therapy with actinium-225 ( ²²⁵ Ac)-lintuzumab (anti-CD33) and low-dose cytarabine (LDAC) in older patients with untreated acute myeloid leukemia (AML. Jurcic, Joseph G.; Ravandi, Farhad; Pagel, John M. Journal of Clinical Oncology, Vol. 33, Issue 15_suppl https://doi.org/10.1200/jco.2015.33.15_suppl.7050	journal	May 2015
Selective Alpha-Particle Mediated Depletion of Tumor Vasculature with Vascular Normalization Jaggi, Jaspreet Singh; Henke, Erik; Seshan, Surya V. PLoS ONE, Vol. 2, Issue 3 https://doi.org/10.1371/journal.pone.0000267	journal	March 2007
Treatment of Peritoneal Carcinomatosis by Targeted Delivery of the Radio-Labeled Tumor Homing Peptide 213Bi-DTPA-[F3]2 into the Nucleus of Tumor Cells Drecoll, Enken; Gaertner, Florian C.; Miederer, Matthias PLoS ONE, Vol. 4, Issue 5 https://doi.org/10.1371/journal.pone.0005715	journal	May 2009
Gold Coated Lanthanide Phosphate Nanoparticles for Targeted Alpha Generator Radiotherapy McLaughlin, Mark F.; Woodward, Jonathan; Boll, Rose A. PLoS ONE, Vol. 8, Issue 1 https://doi.org/10.1371/journal.pone.0054531	journal	January 2013
Long-Term Toxicity of 213Bi-Labelled BSA in Mice Dorso, Laëtitia; Bigot-Corbel, Edith; Abadie, Jérôme PLOS ONE, Vol. 11, Issue 3 https://doi.org/10.1371/journal.pone.0151330	journal	March 2016
Targeted Alpha-Particle Immunotherapy for Acute Myeloid Leukemia Jurcic, Joseph G.; Rosenblat, Todd L. American Society of Clinical Oncology Educational Book, Issue 34 https://doi.org/10.14694/EdBook_AM.2014.34.e126	journal	May 2014
Renal Tubulointerstitial Changes after Internal Irradiation with α-Particle–Emitting Actinium Daughters Jaggi, Jaspreet Singh; Seshan, Surya V.; McDevitt, Michael R. Journal of the American Society of Nephrology, Vol. 16, Issue 9 https://doi.org/10.1681/ASN.2004110945	journal	June 2005
Effective treatment of ductal carcinoma in situ with a HER-2- targeted alpha-particle emitting radionuclide in a preclinical model of human breast cancer Yoshida, Takahiro; Jin, Kideok; Song, Hong Oncotarget, Vol. 7, Issue 22 https://doi.org/10.18632/oncotarget.8949	journal	April 2016
Astatine-211: Production and Availability R. Zalutsky, Michael; Pruszynski, Marek Current Radiopharmaceuticalse, Vol. 4, Issue 3 https://doi.org/10.2174/1874471011104030177	journal	July 2011
Targeted Alpha Therapy with 213Bi Morgenstern, Alfred; Bruchertseifer, Frank; Apostolidis, Christos Current Radiopharmaceuticalse, Vol. 4, Issue 4 https://doi.org/10.2174/1874471011104040295	journal	October 2011
Bismuth-213 and Actinium-225 – Generator Performance and Evolving Therapeutic Applications of Two Generator-Derived Alpha-Emitting Radioisotopes Morgenstern, Alfred; Bruchertseifer, Frank; Apostolidis, Christos Current Radiopharmaceuticals, Vol. 5, Issue 3 https://doi.org/10.2174/1874471011205030221	journal	June 2012
Analysis of patient survival in a Phase I trial of systemic targeted α-therapy for metastatic melanoma Allen, Barry J.; Singla, Apresh A.; Rizvi, Syed M. Abbas Immunotherapy, Vol. 3, Issue 9 https://doi.org/10.2217/imt.11.97	journal	September 2011
The Relative Radiosensitivity of the Nucleus and Cytoplasm of Chinese Hamster Fibroblasts Munro, T. R. Radiation Research, Vol. 42, Issue 3 https://doi.org/10.2307/3572962	journal	June 1970
Tumor Targeting with Antibody-Functionalized, Radiolabeled Carbon Nanotubes McDevitt, M. R.; Chattopadhyay, D.; Kappel, B. J. Journal of Nuclear Medicine, Vol. 48, Issue 7 https://doi.org/10.2967/jnumed.106.039131	journal	July 2007
Clinical Experience with -Particle Emitting 211At: Treatment of Recurrent Brain Tumor Patients with 211At-Labeled Chimeric Antitenascin Monoclonal Antibody 81C6 Zalutsky, M. R.; Reardon, D. A.; Akabani, G. Journal of Nuclear Medicine, Vol. 49, Issue 1 https://doi.org/10.2967/jnumed.107.046938	journal	December 2007
MIRD Pamphlet No. 22 (Abridged): Radiobiology and Dosimetry of -Particle Emitters for Targeted Radionuclide Therapy Sgouros, G.; Roeske, J. C.; McDevitt, M. R. Journal of Nuclear Medicine, Vol. 51, Issue 2 https://doi.org/10.2967/jnumed.108.058651	journal	January 2010
Intraperitoneal -Particle Radioimmunotherapy of Ovarian Cancer Patients: Pharmacokinetics and Dosimetry of 211At-MX35 F(ab')2--A Phase I Study Andersson, H.; Cederkrantz, E.; Back, T. Journal of Nuclear Medicine, Vol. 50, Issue 7 https://doi.org/10.2967/jnumed.109.062604	journal	June 2009
Remodeling the Vascular Microenvironment of Glioblastoma with -Particles Behling, K.; Maguire, W. F.; Di Gialleonardo, V. Journal of Nuclear Medicine, Vol. 57, Issue 11 https://doi.org/10.2967/jnumed.116.173559	journal	June 2016
(2S)-2-(3-(1-Carboxy-5-(4-211At-Astatobenzamido)Pentyl)Ureido)-Pentanedioic Acid for PSMA-Targeted -Particle Radiopharmaceutical Therapy Kiess, A. P.; Minn, I.; Vaidyanathan, G. Journal of Nuclear Medicine, Vol. 57, Issue 10 https://doi.org/10.2967/jnumed.116.174300	journal	May 2016
225Ac-PSMA-617 for PSMA-Targeted -Radiation Therapy of Metastatic Castration-Resistant Prostate Cancer Kratochwil, C.; Bruchertseifer, F.; Giesel, F. L. Journal of Nuclear Medicine, Vol. 57, Issue 12 https://doi.org/10.2967/jnumed.116.178673	journal	July 2016
What is the Role of the Bystander Response in Radionuclide Therapies? Brady, Darren; O’Sullivan, Joe M.; Prise, Kevin M. Frontiers in Oncology, Vol. 3 https://doi.org/10.3389/fonc.2013.00215	journal	January 2013
Significant systemic therapeutic effects of high-LET immunoradiation by 212Pb-trastuzumab against prostatic tumors of androgen-independent human prostate cancer in mice Dong, Zhongyun International Journal of Oncology https://doi.org/10.3892/ijo.2012.1357	journal	February 2012
Different ways to improve the clinical effectiveness of radioimmunotherapy in solid tumors Chatal, Jean-Francois; Davodeau, Francois; Cherel, Michel Journal of Cancer Research and Therapeutics, Vol. 5, Issue 9 https://doi.org/10.4103/0973-1482.55139	journal	January 2009
Targeting of Radio-Isotopes for Cancer Therapy Milenic, Diane E.; Brechbiel, Martin W. Cancer Biology & Therapy, Vol. 3, Issue 4 https://doi.org/10.4161/cbt.3.4.790	journal	April 2004
Intralesional targeted alpha therapy for metastatic melanoma Allen, Barry J.; Raja, Chand; Rizvi, Syed Cancer Biology & Therapy, Vol. 4, Issue 12 https://doi.org/10.4161/cbt.4.12.2251	journal	December 2005
Interim analysis of toxicity and response in phase 1 trial of systemic targeted alpha therapy for metastatic melanoma Raja, Chand; Graham, Peter; Rizvi, Syed Cancer Biology & Therapy, Vol. 6, Issue 6 https://doi.org/10.4161/cbt.6.6.4089	journal	June 2007
Pharmacokinetics and toxicity of 213Bi-labeled PAI2 in preclinical targeted alpha therapy for cancer Song, Emma Y.; Rizvi, Syed M. A.; Qu, Chang F. Cancer Biology & Therapy, Vol. 6, Issue 6 https://doi.org/10.4161/cbt.6.6.4097	journal	June 2007

Cited By (6)

Towards elucidating the radiochemistry of astatine – Behavior in chloroform Aneheim, Emma; Palm, Stig; Jensen, Holger Scientific Reports, Vol. 9, Issue 1 https://doi.org/10.1038/s41598-019-52365-5	journal	November 2019
Rhenium-188 Labeled Radiopharmaceuticals: Current Clinical Applications in Oncology and Promising Perspectives Lepareur, Nicolas; Lacœuille, Franck; Bouvry, Christelle Frontiers in Medicine, Vol. 6 https://doi.org/10.3389/fmed.2019.00132	journal	June 2019
Ion acceleration by an ultrashort laser pulse interacting with a near-critical-density gas jet Ehret, M.; Salgado-Lopez, C.; Ospina-Bohorquez, V. arXiv https://doi.org/10.48550/arxiv.2012.09455	preprint	January 2020
Measurement of Ac227 Impurity in Ac225 using Decay Energy Spectroscopy Tollefson, Aidan D.; Smith, Chandler M.; Carpenter, Matthew H. arXiv https://doi.org/10.48550/arxiv.2102.02813	preprint	January 2021
Production of 149Tb, 152Tb, 155Tb and 161Tb from gadolinium using different light-particle beams Rahman, A. K. M. Rezaur; Awal, Abdul Journal of Radioanalytical and Nuclear Chemistry, Vol. 323, Issue 2 https://doi.org/10.1007/s10967-019-06973-0	journal	December 2019
Targeting the Tetraspanins with Monoclonal Antibodies in Oncology: Focus on Tspan8/Co-029 Bonnet, Mathilde; Maisonial-Besset, Aurélie; Zhu, Yingying Cancers, Vol. 11, Issue 2 https://doi.org/10.3390/cancers11020179	journal	February 2019