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Theranostics in oncology: What radiologists want to know

      Highlights

      • Theranostics enable improved patient selection by functional imaging to identify those benefitting most.
      • Appropriate criteria and timing for response assessment is yet to be standardised.
      • Both SSTR and PSMA are established targets in nuclear medicine theranostics. Many more are underway.

      Abstract

      Combination of radioligand imaging and therapy, so called radiotheranostics, is a novel tool of precision oncology with proven clinical value. In-depth knowledge of functional imaging nuances is critically needed for precise prognostication and guidance of management. Here, we review theranostic applications with up to Phase III type evidence for outcome improvement: Imaging and therapy of neuroendocrine neoplasms (NEN) exploiting high levels of somatostatin receptor (SSTR) expression and radiotheranostics of prostate cancer targeting the prostate specific membrane antigen (PSMA). This narrative review focusses on these two applications and elucidates patient selection and response assessment by radioligand scintigraphy and/or positron emission tomography. Furthermore, we provide a brief outlook on future applications for novel targets outside of NEN and prostate cancer.

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      References

        • Hertz S.
        • Roberts A.
        Radioactive iodine in the study of thyroid physiology; the use of radioactive iodine therapy in hyperthyroidism.
        J Am Med Assoc. 1946; 131: 81-86
        • Strosberg J.
        • El-Haddad G.
        • Wolin E.
        • Hendifar A.
        • Yao J.
        • Chasen B.
        • Mittra E.
        • Kunz P.L.
        • Kulke M.H.
        • Jacene H.
        • Bushnell D.
        • O'Dorisio T.M.
        • Baum R.P.
        • Kulkarni H.R.
        • Caplin M.
        • Lebtahi R.
        • Hobday T.
        • Delpassand E.
        • Van Cutsem E.
        • Benson A.
        • Srirajaskanthan R.
        • Pavel M.
        • Mora J.
        • Berlin J.
        • Grande E.
        • Reed N.
        • Seregni E.
        • Oberg K.
        • Lopera Sierra M.
        • Santoro P.
        • Thevenet T.
        • Erion J.L.
        • Ruszniewski P.
        • Kwekkeboom D.
        • Krenning E.
        • Investigators N.-T.
        Phase 3 Trial of (177)Lu-Dotatate for Midgut Neuroendocrine Tumors.
        N Engl J Med. 2017; 376: 125-135
        • Hofman M.S.
        • Violet J.
        • Hicks R.J.
        • Ferdinandus J.
        • Thang S.P.
        • Akhurst T.
        • Iravani A.
        • Kong G.
        • Ravi Kumar A.
        • Murphy D.G.
        • Eu P.
        • Jackson P.
        • Scalzo M.
        • Williams S.G.
        • Sandhu S.
        [(177)Lu]-PSMA-617 radionuclide treatment in patients with metastatic castration-resistant prostate cancer (LuPSMA trial): a single-centre, single-arm, phase 2 study.
        Lancet Oncol. 2018; 19: 825-833
        • Kulke M.H.
        • Mayer R.J.
        Carcinoid tumors.
        N Engl J Med. 1999; 340: 858-868
        • Strosberg J.R.
        • Weber J.M.
        • Feldman M.
        • Coppola D.
        • Meredith K.
        • Kvols L.K.
        Prognostic validity of the American Joint Committee on Cancer staging classification for midgut neuroendocrine tumors.
        J Clin Oncol. 2013; 31: 420-425
        • Yao J.C.
        • Hassan M.
        • Phan A.
        • Dagohoy C.
        • Leary C.
        • Mares J.E.
        • Abdalla E.K.
        • Fleming J.B.
        • Vauthey J.N.
        • Rashid A.
        • Evans D.B.
        One hundred years after “carcinoid”: epidemiology of and prognostic factors for neuroendocrine tumors in 35,825 cases in the United States.
        J Clin Oncol. 2008; 26: 3063-3072
      1. A. Rinke, H.H. Muller, C. Schade-Brittinger, K.J. Klose, P. Barth, M. Wied, C. Mayer, B. Aminossadati, U.F. Pape, M. Blaker, J. Harder, C. Arnold, T. Gress, R. Arnold, P.S. Group, Placebo-controlled, double-blind, prospective, randomized study on the effect of octreotide LAR in the control of tumor growth in patients with metastatic neuroendocrine midgut tumors: a report from the PROMID Study Group, J Clin Oncol 27(28) (2009) 4656-63.

      2. G. Delle Fave, D. O'Toole, A. Sundin, B. Taal, P. Ferolla, J.K. Ramage, D. Ferone, T. Ito, W. Weber, Z. Zheng-Pei, W.W. De Herder, A. Pascher, P. Ruszniewski, p. Vienna Consensus Conference, ENETS Consensus Guidelines Update for Gastroduodenal Neuroendocrine Neoplasms, Neuroendocrinology 103(2) (2016) 119-24.

      3. J.C. Yao, N. Fazio, S. Singh, R. Buzzoni, C. Carnaghi, E. Wolin, J. Tomasek, M. Raderer, H. Lahner, M. Voi, L.B. Pacaud, N. Rouyrre, C. Sachs, J.W. Valle, G.D. Fave, E. Van Cutsem, M. Tesselaar, Y. Shimada, D.Y. Oh, J. Strosberg, M.H. Kulke, M.E. Pavel, F.T.S.G. Rad001 in Advanced Neuroendocrine Tumours, 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 387(10022) (2016) 968-977.

        • Valkema Roelf
        • Pauwels Stanislas
        • Kvols Larry K.
        • Barone Raffaella
        • Jamar Francois
        • Bakker Willem H.
        • Kwekkeboom Dik J.
        • Bouterfa Hakim
        • Krenning Eric P.
        Survival and response after peptide receptor radionuclide therapy with [90Y-DOTA0, Tyr3]octreotide in patients with advanced gastroenteropancreatic neuroendocrine tumors.
        Semin Nucl Med. 2006; 36: 147-156
        • Krenning E.P.
        • de Jong M.
        • Kooij P.P.
        • Breeman W.A.
        • Bakker W.H.
        • de Herder W.W.
        • van Eijck C.H.
        • Kwekkeboom D.J.
        • Jamar F.
        • Pauwels S.
        • Valkema R.
        Radiolabelled somatostatin analogue(s) for peptide receptor scintigraphy and radionuclide therapy.
        Ann Oncol. 1999; 10: S23-S29
      4. D.J. Kwekkeboom, E.P. Krenning, K. Scheidhauer, V. Lewington, R. Lebtahi, A. Grossman, P. Vitek, A. Sundin, U. Plockinger, p. Mallorca Consensus Conference, S. European Neuroendocrine Tumor, ENETS Consensus Guidelines for the Standards of Care in Neuroendocrine Tumors: somatostatin receptor imaging with (111)In-pentetreotide, Neuroendocrinology 90(2) (2009) 184-9.

        • Krenning E.P.
        • Valkema R.
        • Kooij P.P.
        • Breeman W.A.
        • Bakker W.H.
        • deHerder W.W.
        • vanEijck C.H.
        • Kwekkeboom D.J.
        • deJong M.
        • Pauwels S.
        Scintigraphy and radionuclide therapy with [indium-111-labelled-diethyl triamine penta-acetic acid-D-Phe1]-octreotide.
        Ital J Gastroenterol Hepatol. 1999; 31: S219-S223
        • Hope T.A.
        • Calais J.
        • Zhang L.
        • Dieckmann W.
        • Millo C.
        (111)In-Pentetreotide Scintigraphy Versus (68)Ga-DOTATATE PET: Impact on Krenning Scores and Effect of Tumor Burden.
        J Nucl Med. 2019; 60: 1266-1269
        • 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 [177 Lu-DOTA 0, Tyr3]octreotate: toxicity, efficacy, and survival.
        J Clin Oncol. 2008; 26: 2124-2130
        • Bodei L.
        • Kidd M.
        • Modlin I.M.
        • Severi S.
        • Drozdov I.
        • Nicolini S.
        • Kwekkeboom D.J.
        • Krenning E.P.
        • Baum R.P.
        • Paganelli G.
        Measurement of circulating transcripts and gene cluster analysis predicts and defines therapeutic efficacy of peptide receptor radionuclide therapy (PRRT) in neuroendocrine tumors.
        Eur J Nucl Med Mol Imaging. 2016; 43: 839-851
        • Bodei Lisa
        • Kidd Mark S.
        • Singh Aviral
        • van der Zwan Wouter A.
        • Severi Stefano
        • Drozdov Ignat A.
        • Cwikla Jaroslaw
        • Baum Richard P.
        • Kwekkeboom Dik J.
        • Paganelli Giovanni
        • Krenning Eric P.
        • Modlin Irvin M.
        PRRT genomic signature in blood for prediction of (177)Lu-octreotate efficacy.
        Eur J Nucl Med Mol Imaging. 2018; 45: 1155-1169
        • Deb N.
        • Goris M.
        • Trisler K.
        • Fowler S.
        • Saal J.
        • Ning S.
        • Becker M.
        • Marquez C.
        • Knox S.
        Treatment of hormone-refractory prostate cancer with 90Y-CYT-356 monoclonal antibody.
        Clin Cancer Res. 1996; 2: 1289-1297
        • Milowsky Matthew I.
        • Nanus David M.
        • Kostakoglu Lale
        • Vallabhajosula Shankar
        • Goldsmith Stanley J.
        • Bander Neil H.
        Phase I trial of yttrium-90-labeled anti-prostate-specific membrane antigen monoclonal antibody J591 for androgen-independent prostate cancer.
        J Clin Oncol. 2004; 22: 2522-2531
        • Bander Neil H.
        • Milowsky Matthew I.
        • Nanus David M.
        • Kostakoglu Lale
        • Vallabhajosula Shankar
        • Goldsmith Stanley J.
        Phase I trial of 177lutetium-labeled J591, a monoclonal antibody to prostate-specific membrane antigen, in patients with androgen-independent prostate cancer.
        J Clin Oncol. 2005; 23: 4591-4601
        • Benešová Martina
        • Schäfer Martin
        • Bauder-Wüst Ulrike
        • Afshar-Oromieh Ali
        • Kratochwil Clemens
        • Mier Walter
        • Haberkorn Uwe
        • Kopka Klaus
        • Eder Matthias
        Preclinical Evaluation of a Tailor-Made DOTA-Conjugated PSMA Inhibitor with Optimized Linker Moiety for Imaging and Endoradiotherapy of Prostate Cancer.
        J Nucl Med. 2015; 56: 914-920
        • Fendler W.P.
        • Calais J.
        • Eiber M.
        • Flavell R.R.
        • Mishoe A.
        • Feng F.Y.
        • Nguyen H.G.
        • Reiter R.E.
        • Rettig M.B.
        • Okamoto S.
        • Emmett L.
        • Zacho H.D.
        • Ilhan H.
        • Wetter A.
        • Rischpler C.
        • Schoder H.
        • Burger I.A.
        • Gartmann J.
        • Smith R.
        • Small E.J.
        • Slavik R.
        • Carroll P.R.
        • Herrmann K.
        • Czernin J.
        • Hope T.A.
        Assessment of 68Ga-PSMA-11 PET Accuracy in Localizing Recurrent Prostate Cancer: A Prospective Single-Arm Clinical Trial.
        JAMA Oncol. 2019; 5: 856-863
        • Calais J.
        • Ceci F.
        • Eiber M.
        • Hope T.A.
        • Hofman M.S.
        • Rischpler C.
        • Bach-Gansmo T.
        • Nanni C.
        • Savir-Baruch B.
        • Elashoff D.
        • Grogan T.
        • Dahlbom M.
        • Slavik R.
        • Gartmann J.
        • Nguyen K.
        • Lok V.
        • Jadvar H.
        • Kishan A.U.
        • Rettig M.B.
        • Reiter R.E.
        • Fendler W.P.
        • Czernin J.
        (18)F-fluciclovine PET-CT and (68)Ga-PSMA-11 PET-CT in patients with early biochemical recurrence after prostatectomy: a prospective, single-centre, single-arm, comparative imaging trial.
        Lancet Oncol. 2019; 20: 1286-1294
        • Rauscher I.
        • Kronke M.
        • Konig M.
        • Gafita A.
        • Maurer T.
        • Horn T.
        • Schiller K.
        • Weber W.
        • Eiber M.
        Matched-Pair Comparison of (68)Ga-PSMA-11 PET/CT and (18)F-PSMA-1007 PET/CT: Frequency of Pitfalls and Detection Efficacy in Biochemical Recurrence After Radical Prostatectomy.
        J Nucl Med. 2020; 61: 51-57
      5. A.O. Sartor, M.J. Morris, B.J. Krause, VISION: An international, prospective, open-label, multicenter, randomized phase 3 study of 177Lu-PSMA-617 in the treatment of patients with progressive PSMA-positive metastatic castration-resistant prostate cancer (mCRPC), Journal of Clinical Oncology 37(15_suppl) (2019) TPS5099-TPS5099.

      6. M.S. Hofman, L. Emmett, J. Violet, Y.Z. A, N.J. Lawrence, M. Stockler, R.J. Francis, A. Iravani, S. Williams, A. Azad, A. Martin, M. McJannett, A.T. team, I.D. Davis, TheraP: a randomized phase 2 trial of (177) Lu-PSMA-617 theranostic treatment vs cabazitaxel in progressive metastatic castration-resistant prostate cancer (Clinical Trial Protocol ANZUP 1603), BJU Int 124 Suppl 1 (2019) 5-13.

        • Rahbar Kambiz
        • Ahmadzadehfar Hojjat
        • Kratochwil Clemens
        • Haberkorn Uwe
        • Schäfers Michael
        • Essler Markus
        • Baum Richard P.
        • Kulkarni Harshad R.
        • Schmidt Matthias
        • Drzezga Alexander
        • Bartenstein Peter
        • Pfestroff Andreas
        • Luster Markus
        • Lützen Ulf
        • Marx Marlies
        • Prasad Vikas
        • Brenner Winfried
        • Heinzel Alexander
        • Mottaghy Felix M.
        • Ruf Juri
        • Meyer Philipp Tobias
        • Heuschkel Martin
        • Eveslage Maria
        • Bögemann Martin
        • Fendler Wolfgang Peter
        • Krause Bernd Joachim
        German Multicenter Study Investigating 177Lu-PSMA-617 Radioligand Therapy in Advanced Prostate Cancer Patients.
        J Nucl Med. 2017; 58: 85-90
        • Kratochwil Clemens
        • Fendler Wolfgang Peter
        • Eiber Matthias
        • Baum Richard
        • Bozkurt Murat Fani
        • Czernin Johannes
        • Delgado Bolton Roberto C.
        • Ezziddin Samer
        • Forrer Flavio
        • Hicks Rodney J.
        • Hope Thomas A.
        • Kabasakal Levant
        • Konijnenberg Mark
        • Kopka Klaus
        • Lassmann Michael
        • Mottaghy Felix M.
        • Oyen Wim
        • Rahbar Kambiz
        • Schöder Heiko
        • Virgolini Irene
        • Wester Hans-Jürgen
        • Bodei Lisa
        • Fanti Stefano
        • Haberkorn Uwe
        • Herrmann Ken
        EANM procedure guidelines for radionuclide therapy with (177)Lu-labelled PSMA-ligands ((177)Lu-PSMA-RLT).
        Eur J Nucl Med Mol Imaging. 2019; 46: 2536-2544
        • Violet J.
        • Jackson P.
        • Ferdinandus J.
        • Sandhu S.
        • Akhurst T.
        • Iravani A.
        • Kong G.
        • Kumar A.R.
        • Thang S.P.
        • Eu P.
        • Scalzo M.
        • Murphy D.
        • Williams S.
        • Hicks R.J.
        • Hofman M.S.
        Dosimetry of (177)Lu-PSMA-617 in Metastatic Castration-Resistant Prostate Cancer: Correlations Between Pretherapeutic Imaging and Whole-Body Tumor Dosimetry with Treatment Outcomes.
        J Nucl Med. 2019; 60: 517-523
        • Ferdinandus Justin
        • Eppard Elisabeth
        • Gaertner Florian C.
        • Kürpig Stefan
        • Fimmers Rolf
        • Yordanova Anna
        • Hauser Stefan
        • Feldmann Georg
        • Essler Markus
        • Ahmadzadehfar Hojjat
        Predictors of Response to Radioligand Therapy of Metastatic Castrate-Resistant Prostate Cancer with 177Lu-PSMA-617.
        J Nucl Med. 2017; 58: 312-319
        • Seifert Robert
        • Kessel Katharina
        • Schlack Katrin
        • Weber Manuel
        • Herrmann Ken
        • Spanke Maximilian
        • Fendler Wolfgang P.
        • Hadaschik Boris
        • Kleesiek Jens
        • Schäfers Michael
        • Weckesser Matthias
        • Boegemann Martin
        • Rahbar Kambiz
        PSMA PET total tumor volume predicts outcome of patients with advanced prostate cancer receiving [(177)Lu]Lu-PSMA-617 radioligand therapy in a bicentric analysis.
        Eur J Nucl Med Mol Imaging. 2021; 48: 1200-1210
        • Ferdinandus Justin
        • Violet John
        • Sandhu Shahneen
        • Hicks Rodney J.
        • Ravi Kumar Aravind S.
        • Iravani Amir
        • Kong Grace
        • Akhurst Tim
        • Thang Sue Ping
        • Murphy Declan G.
        • Williams Scott
        • Hofman Michael S.
        Prognostic biomarkers in men with metastatic castration-resistant prostate cancer receiving [177Lu]-PSMA-617.
        Eur J Nucl Med Mol Imaging. 2020; 47: 2322-2327
        • Suman S.
        • Parghane R.V.
        • Joshi A.
        • Prabhash K.
        • Bakshi G.
        • Talole S.
        • Banerjee S.
        • Basu S.
        Therapeutic efficacy, prognostic variables and clinical outcome of (177)Lu-PSMA-617 PRLT in progressive mCRPC following multiple lines of treatment: prognostic implications of high FDG uptake on dual tracer PET-CT vis-a-vis Gleason score in such cohort.
        Br J Radiol. 2019; 92: 20190380
        • Eisenhauer E.A.
        • Therasse P.
        • Bogaerts J.
        • Schwartz L.H.
        • Sargent D.
        • Ford R.
        • Dancey J.
        • Arbuck S.
        • Gwyther S.
        • Mooney M.
        • Rubinstein L.
        • Shankar L.
        • Dodd L.
        • Kaplan R.
        • Lacombe D.
        • Verweij J.
        New response evaluation criteria in solid tumours: revised RECIST guideline (version 1.1).
        Eur J Cancer. 2009; 45: 228-247
        • Choi H.
        • Charnsangavej C.
        • Faria S.C.
        • Macapinlac H.A.
        • Burgess M.A.
        • Patel S.R.
        • Chen L.L.
        • Podoloff D.A.
        • Benjamin R.S.
        Correlation of computed tomography and positron emission tomography in patients with metastatic gastrointestinal stromal tumor treated at a single institution with imatinib mesylate: proposal of new computed tomography response criteria.
        J Clin Oncol. 2007; 25: 1753-1759
      7. D.M.V. Huizing, E.A. Aalbersberg, M.W.J. Versleijen, M.E.T. Tesselaar, I. Walraven, M.J. Lahaye, B.J. de Wit-van der Veen, M.P.M. Stokkel, Early response assessment and prediction of overall survival after peptide receptor radionuclide therapy, Cancer Imaging 20(1) (2020) 57.

        • Gabriel Michael
        • Oberauer Andreas
        • Dobrozemsky Georg
        • Decristoforo Clemens
        • Putzer Daniel
        • Kendler Dorota
        • Uprimny Christian
        • Kovacs Peter
        • Bale Reto
        • Virgolini Irene J.
        68Ga-DOTA-Tyr3-octreotide PET for assessing response to somatostatin-receptor-mediated radionuclide therapy.
        J Nucl Med. 2009; 50: 1427-1434
        • Bodei L.
        • Kidd M.S.
        • Singh A.
        • van der Zwan W.A.
        • Severi S.
        • Drozdov I.A.
        • Malczewska A.
        • Baum R.P.
        • Kwekkeboom D.J.
        • Paganelli G.
        • Krenning E.P.
        • Modlin I.M.
        PRRT neuroendocrine tumor response monitored using circulating transcript analysis: the NETest.
        Eur J Nucl Med Mol Imaging. 2020; 47: 895-906
        • Ortega C.
        • Wong R.K.
        • Schaefferkoetter J.
        • Veit-Haibach P.
        • Myrehaug S.
        • Juergens R.
        • Laidley D.
        • Anconina R.
        • Liu Z.A.
        • Metser U.
        Quantitative (68)Ga-DOTATATE PET/CT parameters for the prediction of therapy response in patients with progressive metastatic neuroendocrine tumors treated with (177)Lu-DOTATATE.
        J Nucl Med. 2021;
      8. H.I. Scher, M.J. Morris, W.M. Stadler, C. Higano, E. Basch, K. Fizazi, E.S. Antonarakis, T.M. Beer, M.A. Carducci, K.N. Chi, P.G. Corn, J.S. de Bono, R. Dreicer, D.J. George, E.I. Heath, M. Hussain, W.K. Kelly, G. Liu, C. Logothetis, D. Nanus, M.N. Stein, D.E. Rathkopf, S.F. Slovin, C.J. Ryan, O. Sartor, E.J. Small, M.R. Smith, C.N. Sternberg, M.E. Taplin, G. Wilding, P.S. Nelson, L.H. Schwartz, S. Halabi, P.W. Kantoff, A.J. Armstrong, G. Prostate Cancer Clinical Trials Working, Trial Design and Objectives for Castration-Resistant Prostate Cancer: Updated Recommendations From the Prostate Cancer Clinical Trials Working Group 3, J Clin Oncol 34(12) (2016) 1402-18.

        • Yordanova Anna
        • Linden Paula
        • Hauser Stefan
        • Meisenheimer Michael
        • Kürpig Stefan
        • Feldmann Georg
        • Gaertner Florian C.
        • Essler Markus
        • Ahmadzadehfar Hojjat
        Outcome and safety of rechallenge [(177)Lu]Lu-PSMA-617 in patients with metastatic prostate cancer.
        Eur J Nucl Med Mol Imaging. 2019; 46: 1073-1080
        • Yadav M.P.
        • Ballal S.
        • Tripathi M.
        • Damle N.A.
        • Sahoo R.K.
        • Seth A.
        • Bal C.
        (177)Lu-DKFZ-PSMA-617 therapy in metastatic castration resistant prostate cancer: safety, efficacy, and quality of life assessment.
        Eur J Nucl Med Mol Imaging. 2017; 44: 81-91
        • Ahmadzadehfar Hojjat
        • Wegen Simone
        • Yordanova Anna
        • Fimmers Rolf
        • Kürpig Stefan
        • Eppard Elisabeth
        • Wei Xiao
        • Schlenkhoff Carl
        • Hauser Stefan
        • Essler Markus
        Overall survival and response pattern of castration-resistant metastatic prostate cancer to multiple cycles of radioligand therapy using [(177)Lu]Lu-PSMA-617.
        Eur J Nucl Med Mol Imaging. 2017; 44: 1448-1454
        • Armstrong A.J.
        • Anand A.
        • Edenbrandt L.
        • Bondesson E.
        • Bjartell A.
        • Widmark A.
        • Sternberg C.N.
        • Pili R.
        • Tuvesson H.
        • Nordle O.
        • Carducci M.A.
        • Morris M.J.
        Phase 3 Assessment of the Automated Bone Scan Index as a Prognostic Imaging Biomarker of Overall Survival in Men With Metastatic Castration-Resistant Prostate Cancer: A Secondary Analysis of a Randomized Clinical Trial.
        JAMA Oncol. 2018; 4: 944-951
        • Fendler W.P.
        • Eiber M.
        • Beheshti M.
        • Bomanji J.
        • Ceci F.
        • Cho S.
        • Giesel F.
        • Haberkorn U.
        • Hope T.A.
        • Kopka K.
        • Krause B.J.
        • Mottaghy F.M.
        • Schoder H.
        • Sunderland J.
        • Wan S.
        • Wester H.J.
        • Fanti S.
        • Herrmann K.
        (68)Ga-PSMA PET/CT: Joint EANM and SNMMI procedure guideline for prostate cancer imaging: version 1.0.
        Eur J Nucl Med Mol Imaging. 2017; 44: 1014-1024
        • Perera M.
        • Papa N.
        • Roberts M.
        • Williams M.
        • Udovicich C.
        • Vela I.
        • Christidis D.
        • Bolton D.
        • Hofman M.S.
        • Lawrentschuk N.
        • Murphy D.G.
        Gallium-68 Prostate-specific Membrane Antigen Positron Emission Tomography in Advanced Prostate Cancer-Updated Diagnostic Utility, Sensitivity, Specificity, and Distribution of Prostate-specific Membrane Antigen-avid Lesions: A Systematic Review and Meta-analysis.
        Eur Urol. 2020; 77: 403-417
        • Farolfi A.
        • Hirmas N.
        • Gafita A.
        • Weber M.
        • Barbato F.
        • Wetter A.
        • Mei R.
        • Pianori D.
        • Hadaschik B.
        • Herrmann K.
        • Castellucci P.
        • Fanti S.
        • Eiber M.
        • Fendler W.P.
        PSMA-PET identifies PCWG3 target populations with superior accuracy and reproducibility when compared to conventional imaging: a multicenter retrospective study.
        J Nucl Med. 2020;
        • Fendler Wolfgang P.
        • Weber Manuel
        • Iravani Amir
        • Hofman Michael S.
        • Calais Jérémie
        • Czernin Johannes
        • Ilhan Harun
        • Saad Fred
        • Small Eric J.
        • Smith Matthew R.
        • Perez Paola M.
        • Hope Thomas A.
        • Rauscher Isabel
        • Londhe Anil
        • Lopez-Gitlitz Angela
        • Cheng Shinta
        • Maurer Tobias
        • Herrmann Ken
        • Eiber Matthias
        • Hadaschik Boris
        Prostate-Specific Membrane Antigen Ligand Positron Emission Tomography in Men with Nonmetastatic Castration-Resistant Prostate Cancer.
        Clin Cancer Res. 2019; 25: 7448-7454
        • Kulkarni Harshad R.
        • Singh Aviral
        • Schuchardt Christiane
        • Niepsch Karin
        • Sayeg Manal
        • Leshch Yevgeniy
        • Wester Hans-Juergen
        • Baum Richard P.
        PSMA-Based Radioligand Therapy for Metastatic Castration-Resistant Prostate Cancer: The Bad Berka Experience Since 2013.
        J Nucl Med. 2016; 57: 97S-104S
        • Pollard Janet H.
        • Raman Caleb
        • Zakharia Yousef
        • Tracy Chad R.
        • Nepple Kenneth G.
        • Ginader Tim
        • Breheny Patrick
        • Sunderland John J.
        Quantitative Test-Retest Measurement of (68)Ga-PSMA-HBED-CC in Tumor and Normal Tissue.
        J Nucl Med. 2020; 61: 1145-1152
        • Heinzel Alexander
        • Boghos Dima
        • Mottaghy Felix M.
        • Gaertner Florian
        • Essler Markus
        • von Mallek Dirk
        • Ahmadzadehfar Hojjat
        (68)Ga-PSMA PET/CT for monitoring response to (177)Lu-PSMA-617 radioligand therapy in patients with metastatic castration-resistant prostate cancer.
        Eur J Nucl Med Mol Imaging. 2019; 46: 1054-1062
        • Fanti Stefano
        • Goffin Karolien
        • Hadaschik Boris A
        • Herrmann Ken
        • Maurer Tobias
        • MacLennan Steven
        • Oprea-Lager Daniela E.
        • Oyen Wim JG
        • Rouvière Olivier
        • Mottet Nicolas
        • Bjartell Anders
        Consensus statements on PSMA PET/CT response assessment criteria in prostate cancer.
        Eur J Nucl Med Mol Imaging. 2021; 48: 469-476
        • Grubmüller Bernhard
        • Senn Daniela
        • Kramer Gero
        • Baltzer Pascal
        • D’Andrea David
        • Grubmüller Karl Hermann
        • Mitterhauser Markus
        • Eidherr Harald
        • Haug Alexander R.
        • Wadsak Wolfgang
        • Pfaff Sarah
        • Shariat Shahrokh F.
        • Hacker Marcus
        • Hartenbach Markus
        Response assessment using (68)Ga-PSMA ligand PET in patients undergoing (177)Lu-PSMA radioligand therapy for metastatic castration-resistant prostate cancer.
        Eur J Nucl Med Mol Imaging. 2019; 46: 1063-1072
        • Fanti S.
        • Hadaschik B.
        • Herrmann K.
        Proposal for Systemic-Therapy Response-Assessment Criteria at the Time of PSMA PET/CT Imaging: The PSMA PET Progression Criteria.
        J Nucl Med. 2020; 61: 678-682
        • Hänscheid Heribert
        • Lapa Constantin
        • Buck Andreas K.
        • Lassmann Michael
        • Werner Rudolf A.
        Dose Mapping After Endoradiotherapy with (177)Lu-DOTATATE/DOTATOC by a Single Measurement After 4 Days.
        J Nucl Med. 2018; 59: 75-81
        • Marincek N.
        • Radojewski P.
        • Dumont R.A.
        • Brunner P.
        • Muller-Brand J.
        • Maecke H.R.
        • Briel M.
        • Walter M.A.
        Somatostatin receptor-targeted radiopeptide therapy with 90Y-DOTATOC and 177Lu-DOTATOC in progressive meningioma: long-term results of a phase II clinical trial.
        J Nucl Med. 2015; 56: 171-176
        • Gerster-Gilliéron Karine
        • Forrer Flavio
        • Maecke Helmut
        • Mueller-Brand Jan
        • Merlo Adrian
        • Cordier Dominik
        90Y-DOTATOC as a Therapeutic Option for Complex Recurrent or Progressive Meningiomas.
        J Nucl Med. 2015; 56: 1748-1751
        • Seystahl K.
        • Stoecklein V.
        • Schuller U.
        • Rushing E.
        • Nicolas G.
        • Schafer N.
        • Ilhan H.
        • Pangalu A.
        • Weller M.
        • Tonn J.C.
        • Sommerauer M.
        • Albert N.L.
        Somatostatin receptor-targeted radionuclide therapy for progressive meningioma: benefit linked to 68Ga-DOTATATE/-TOC uptake.
        Neuro Oncol. 2016; 18: 1538-1547
        • Hartrampf Philipp E.
        • Hänscheid Heribert
        • Kertels Olivia
        • Schirbel Andreas
        • Kreissl Michael C.
        • Flentje Michael
        • Sweeney Reinhart A.
        • Buck Andreas K.
        • Polat Bülent
        • Lapa Constantin
        Long-term results of multimodal peptide receptor radionuclide therapy and fractionated external beam radiotherapy for treatment of advanced symptomatic meningioma.
        Clin Transl Radiat Oncol. 2020; 22: 29-32
        • Kreissl M.C.
        • Hanscheid H.
        • Lohr M.
        • Verburg F.A.
        • Schiller M.
        • Lassmann M.
        • Reiners C.
        • Samnick S.S.
        • Buck A.K.
        • Flentje M.
        • Sweeney R.A.
        Combination of peptide receptor radionuclide therapy with fractionated external beam radiotherapy for treatment of advanced symptomatic meningioma.
        Radiat Oncol. 2012; 7: 99
      9. A. Braat, T.J. Snijders, T. Seute, E.P.A. Vonken, Will (177)Lu-DOTATATE Treatment Become More Effective in Salvage Meningioma Patients, When Boosting Somatostatin Receptor Saturation? A Promising Case on Intra-arterial Administration, Cardiovasc Intervent Radiol 42(11) (2019) 1649-1652.

        • Oddstig Jenny
        • Bernhardt Peter
        • Nilsson Ola
        • Ahlman Håkan
        • Forssell-Aronsson Eva
        Radiation induces up-regulation of somatostatin receptors 1, 2, and 5 in small cell lung cancer in vitro also at low absorbed doses.
        Cancer Biother Radiopharm. 2011; 26: 759-765
        • Chang S.S.
        • O'Keefe D.S.
        • Bacich D.J.
        • Reuter V.E.
        • Heston W.D.
        • Gaudin P.B.
        Prostate-specific membrane antigen is produced in tumor-associated neovasculature.
        Clin Cancer Res. 1999; 5: 2674-2681
        • Kunikowska Jolanta
        • Charzyńska Ingeborga
        • Kuliński Radosław
        • Pawlak Dariusz
        • Maurin Michał
        • Królicki Leszek
        Tumor uptake in glioblastoma multiforme after IV injection of [(177)Lu]Lu-PSMA-617.
        Eur J Nucl Med Mol Imaging. 2020; 47: 1605-1606
        • Kunikowska Jolanta
        • Cieślak Bartosz
        • Gierej Beata
        • Patkowski Waldemar
        • Kraj Leszek
        • Kotulski Marcin
        • Zieniewicz Krzysztof
        • Królicki Leszek
        [(68) Ga]Ga-Prostate-Specific Membrane Antigen PET/CT: a novel method for imaging patients with hepatocellular carcinoma.
        Eur J Nucl Med Mol Imaging. 2021; 48: 883-892
        • Sawicki L.M.
        • Buchbender C.
        • Boos J.
        • Giessing M.
        • Ermert J.
        • Antke C.
        • Antoch G.
        • Hautzel H.
        Diagnostic potential of PET/CT using a (68)Ga-labelled prostate-specific membrane antigen ligand in whole-body staging of renal cell carcinoma: initial experience.
        Eur J Nucl Med Mol Imaging. 2017; 44: 102-107
      10. W. van Boxtel, S. Lutje, I.C.H. van Engen-van Grunsven, G.W. Verhaegh, J.A. Schalken, M.A. Jonker, J. Nagarajah, M. Gotthardt, C.M.L. van Herpen, (68)Ga-PSMA-HBED-CC PET/CT imaging for adenoid cystic carcinoma and salivary duct carcinoma: a phase 2 imaging study, Theranostics 10(5) (2020) 2273-2283.

        • Aide N.
        • Poulain L.
        • Elie N.
        • Briand M.
        • Giffard F.
        • Blanc-Fournier C.
        • Joly F.
        • Lasnon C.
        A PSMA-targeted theranostic approach is unlikely to be efficient in serous ovarian cancers.
        EJNMMI Res. 2021; 11: 11
        • Mittlmeier L.M.
        • Unterrainer M.
        • Rodler S.
        • Todica A.
        • Albert N.L.
        • Burgard C.
        • Cyran C.C.
        • Kunz W.G.
        • Ricke J.
        • Bartenstein P.
        • Stief C.G.
        • Ilhan H.
        • Staehler M.
        (18)F-PSMA-1007 PET/CT for response assessment in patients with metastatic renal cell carcinoma undergoing tyrosine kinase or checkpoint inhibitor therapy: preliminary results.
        Eur J Nucl Med Mol Imaging. 2021; 48: 2031-2037
        • Hamson E.J.
        • Keane F.M.
        • Tholen S.
        • Schilling O.
        • Gorrell M.D.
        Understanding fibroblast activation protein (FAP): substrates, activities, expression and targeting for cancer therapy.
        Proteomics Clin Appl. 2014; 8: 454-463
        • Kratochwil C.
        • Flechsig P.
        • Lindner T.
        • Abderrahim L.
        • Altmann A.
        • Mier W.
        • Adeberg S.
        • Rathke H.
        • Rohrich M.
        • Winter H.
        • Plinkert P.K.
        • Marme F.
        • Lang M.
        • Kauczor H.U.
        • Jager D.
        • Debus J.
        • Haberkorn U.
        • Giesel F.L.
        (68)Ga-FAPI PET/CT: Tracer Uptake in 28 Different Kinds of Cancer.
        J Nucl Med. 2019; 60: 801-805
        • Lindner Thomas
        • Loktev Anastasia
        • Altmann Annette
        • Giesel Frederik
        • Kratochwil Clemens
        • Debus Jürgen
        • Jäger Dirk
        • Mier Walter
        • Haberkorn Uwe
        Development of Quinoline-Based Theranostic Ligands for the Targeting of Fibroblast Activation Protein.
        J Nucl Med. 2018; 59: 1415-1422