Third-line treatment and 177Lu-PSMA radioligand therapy of metastatic castration-resistant prostate cancer: a systematic review

European Journal of Nuclear Medicine and Molecular Imaging

Volumn 45, Issue 3, 2018, Pages 496-508

  von Eyben, Finn Edler ^a   Roviello, Giandomenico ^b,c   Kiljunen, Timo ^d   Uprimny, Christian ^e   Virgolini, Irene ^e   Kairemo, Kalevi ^d   Joensuu, Timo ^d  

^a Center of Tobacco Control Research   (Denmark)

^b IRCCS POLICLINICO SAN DONATO   (Italy)

^c UNIVERSITY OF TRIESTE   (Italy)

^d Docrates Oncology Clinic   (Finland)

^e UNIVERSITY HOSPITAL INNSBRUCK   (Austria)

Author keywords

177Lu PSMA radioligand therapy; Abiraterone; Cabazitaxel; Docetaxel; Enzalutamide; Prostate cancer; Systematic review

Indexed keywords

ABIRATERONE; CABAZITAXEL; ENZALUTAMIDE; MONOCLONAL ANTIBODY J591 LU 177; PROSTATE SPECIFIC MEMBRANE ANTIGEN LU 177; RADIOLIGAND; UNCLASSIFIED DRUG; FOLH1 PROTEIN, HUMAN; GLUTAMATE CARBOXYPEPTIDASE II; LIGAND; LUTETIUM; LUTETIUM-177; MEMBRANE ANTIGEN; RADIOISOTOPE;

BODY SURFACE; CANCER COMBINATION CHEMOTHERAPY; CANCER DIAGNOSIS; CANCER GRADING; CANCER REGRESSION; CANCER STAGING; CANCER SURVIVAL; CANCER THERAPY; CASTRATION RESISTANT PROSTATE CANCER; DRUG EFFICACY; DRUG WITHDRAWAL; EMBASE; FOLLOW UP; HUMAN; LONG TERM CARE; MALE; MEDLINE; META ANALYSIS; OVERALL SURVIVAL; REVIEW; SYSTEMATIC REVIEW; THROMBOCYTOPENIA; UNSPECIFIED SIDE EFFECT; METABOLISM; METASTASIS; PATHOLOGY;

ANTIGENS, SURFACE; GLUTAMATE CARBOXYPEPTIDASE II; HUMANS; LIGANDS; LUTETIUM; MALE; NEOPLASM METASTASIS; PROSTATIC NEOPLASMS, CASTRATION-RESISTANT; RADIOISOTOPES;

EID: 85038074814     PISSN: 16197070     EISSN: 16197089     Source Type: Journal    
DOI: 10.1007/s00259-017-3895-x     Document Type: Review

References (67)

1. Center MM, Jemal A, Lortet-Tieulent J, Ward E, Ferlay J, Brawley O, et al. International variation in prostate cancer incidence and mortality rates. Eur Urol. 2012;61:1079–92.
2. Patrikidou A, Loriot Y, Eymard JC, Albiges L, Massard C, Ileana E, et al. Who dies from prostate cancer? Prostate Cancer Prostatic Dis. 2014;17:348–52.
3. Tannock IF, de Wit R, Berry WR, Horti J, Pluzanska A, Chi KN, et al. Docetaxel plus prednisone or mitoxantrone plus prednisone for advanced prostate cancer. N Engl J Med. 2004;351:1502–12.
4. de Bono JS, Oudard S, Ozguroglu M, Hansen S, Machiels JP, Kocak I, et al. Prednisone plus cabazitaxel or mitoxantrone for metastatic castration-resistant prostate cancer progressing after docetaxel treatment: a randomised open-label trial. Lancet. 2010;376:1147–54.
5. de Bono JS, Logothetis CJ, Molina A, Fizazi K, North S, Chu L, et al. Abiraterone and increased survival in metastatic prostate cancer. N Engl J Med. 2011;364:1995–2005.
6. Scher HI, Fizazi K, Saad F, Taplin ME, Sternberg CN, Miller K, et al. Increased survival with enzalutamide in prostate cancer after chemotherapy. N Engl J Med. 2012;367:1187–97.
7. Sartor O, Coleman R, Nilsson S, Heinrich D, Helle SI, O’Sullivan JM, et al. Effect of radium-223 dichloride on symptomatic skeletal events in patients with castration-resistant prostate cancer and bone metastases: results from a phase 3, double-blind, randomised trial. Lancet Oncol. 2014;15:738–46.
8. Kantoff PW, Higano CS, Shore ND, Berger ER, Small EJ, Penson DF, et al. Sipuleucel-T immunotherapy for castration-resistant prostate cancer. N Engl J Med. 2010;363:411–22.
9. Berthold DR, Pond GR, Soban F, de Wit R, Eisenberger M, Tannock IF. Docetaxel plus prednisone or mitoxantrone plus prednisone for advanced prostate cancer: updated survival in the TAX 327 study. J Clin Oncol. 2008;26:242–5.
10. Summers N, Vanderpuye-Orgle J, Reinhart M, Gallagher M, Sartor O. Efficacy and safety of post-docetaxel therapies in metastatic castration-resistant prostate cancer: a systematic review of the literature. Curr Med Res Opin. 2017:1–14.
11. Cornford P, Bellmunt J, Bolla M, Briers E, De Santis M, Gross T, et al. EAU-ESTRO-SIOG guidelines on prostate cancer. Part II: treatment of relapsing, metastatic, and castration-resistant prostate cancer. Eur Urol. 2017;71:630–42.
12. Gillessen S, Attard G, Beer TM, Beltran H, Bossi A, Bristow R, et al. Management of Patients with Advanced Prostate Cancer: The Report of the Advanced Prostate Cancer Consensus Conference APCCC 2017. Eur Urol 2017.
13. Kopka K, Benesova M, Barinka C, Haberkorn U, Babich J. Glu-Ureido-based inhibitors of prostate-specific membrane antigen: lessons learned during the development of a novel class of low-molecular-weight Theranostic radiotracers. J Nucl Med. 2017;58:17S–26S.
14. Perera M, Papa N, Christidis D, Wetherell D, Hofman MS, Murphy DG, et al. Sensitivity, specificity, and predictors of positive 68Ga-prostate-specific membrane antigen positron emission tomography in advanced prostate cancer: a systematic review and meta-analysis. Eur Urol. 2016;70:926–37.
15. von Eyben FE, Picchio M, von Eyben R, Rhee H, Bauman G. 68Ga-labeled prostate-specific membrane antigen ligand positron emission tomography/computed tomography for prostate cancer: a systematic review and meta-analysis. Eur Urol Focus 2016.
16. Calopedos RJS, Chalasani V, Asher R, Emmett L, Woo HH. Lutetium-177-labelled anti-prostate-specific membrane antigen antibody and ligands for the treatment of metastatic castrate-resistant prostate cancer: a systematic review and meta-analysis. Prostate Cancer Prostatic Dis. 2017;20:352–60.
17. Fendler WP, Rahbar K, Herrmann K, Kratochwil C, Eiber M. 177Lu-PSMA Radioligand therapy for prostate cancer. J Nucl Med. 2017;58:1196–200.
18. von Eyben FE, Kiljunen T, Joensuu T, Kairemo K, Uprimny C, Virgolini I. 177Lu-PSMA-617 radioligand therapy for a patient with lymph node metastatic prostate cancer. Oncotarget. 2017;8:66112–6.
19. Gillessen S, de Bono JS, Sartor O, Omlin AG. Reply to Finn E. von Eyben, Irene Virgolini and Giandomenico Roviello’s Letter to the Editor re: Silke Gillessen, Gerhardt Attard, Tomasz M. Beer, et al. Management of Patients with Advanced Prostate Cancer: The Report of the Advanced Prostate Cancer Consensus Conference APCCC 2017. Eur Urol. In press. https://doi.org/10.1016/j.eururo.2017.06.002. Eur Urol. 2017.
20. von Eyben FE, Virgolini I, Roviello G. Re: Silke Gillessen, Gerhardt Attard, Tomasz M. Beer, et al. Management of Patients with Advanced Prostate Cancer: The Report of the Advanced Prostate Cancer Consensus Conference APCCC 2017. Eur Urol. In press. https://doi.org/10.1016/j.eururo.2017.06.002. Eur Urol. 2017.
21. Liberati A, Altman DG, Tetzlaff J, Mulrow C, Gotzsche PC, Ioannidis JP, et al. The PRISMA statement for reporting systematic reviews and meta-analyses of studies that evaluate health care interventions: explanation and elaboration. Ann Intern Med. 2009;151:W65–94.
22. Maines F, Caffo O, Veccia A, Trentin C, Tortora G, Galligioni E, et al. Sequencing new agents after docetaxel in patients with metastatic castration-resistant prostate cancer. Crit Rev Oncol Hematol. 2015;96:498–506.
23. Roviello G, Petrioli R, Laera L, Francini E. The third line of treatment for metastatic prostate cancer patients: option or strategy? Crit Rev Oncol Hematol. 2015;95:265–71.
24. Caffo O, De Giorgi U, Fratino L, Alesini D, Zagonel V, Facchini G, et al. Clinical outcomes of castration-resistant prostate cancer treatments administered as third or fourth line following failure of docetaxel and other second-line treatment: results of an Italian multicentre study. Eur Urol. 2015;68:147–53.
25. Brasso K, Thomsen FB, Schrader AJ, Schmid SC, Lorente D, Retz M, et al. Enzalutamide antitumour activity against metastatic castration-resistant prostate cancer previously treated with docetaxel and Abiraterone: a multicentre analysis. Eur Urol. 2015;68:317–24.
26. Scher HI, Morris MJ, Basch E, Heller G. End points and outcomes in castration-resistant prostate cancer: from clinical trials to clinical practice. J Clin Oncol. 2011;29:3695–704.
27. Eisenhauer EA, Therasse P, Bogaerts J, Schwartz LH, Sargent D, Ford R, et al. New response evaluation criteria in solid tumours: revised RECIST guideline (version 1.1). Eur J Cancer. 2009;45:228–47.
28. Sterne JA, Sutton AJ, Ioannidis JP, Terrin N, Jones DR, Lau J, et al. Recommendations for examining and interpreting funnel plot asymmetry in meta-analyses of randomised controlled trials. BMJ. 2011;343:d4002.
29. Nyaga VN, Arbyn M, Aerts M. Metaprop: a Stata command to perform meta-analysis of binomial data. Arch Public Health. 2014;72:39.
30. Bander NH, Milowsky MI, Nanus DM, Kostakoglu L, Vallabhajosula S, Goldsmith SJ. 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;23:4591–601.
31. Tagawa ST, Milowsky MI, Morris M, Vallabhajosula S, Christos P, Akhtar NH, et al. Phase II study of Lutetium-177-labeled anti-prostate-specific membrane antigen monoclonal antibody J591 for metastatic castration-resistant prostate cancer. Clin Cancer Res. 2013;19:5182–91.
32. Heck MM, Retz M, D’Alessandria C, Rauscher I, Scheidhauer K, Maurer T, et al. Systemic Radioligand therapy with (177)Lu labeled prostate specific membrane antigen ligand for imaging and therapy in patients with metastatic castration resistant prostate cancer. J Urol. 2016;196:382–91.
33. Kratochwil C, Giesel FL, Stefanova M, Benesova M, Bronzel M, Afshar-Oromieh A, et al. PSMA-targeted radionuclide therapy of metastatic castration-resistant prostate cancer with 177Lu-labeled PSMA-617. J Nucl Med. 2016;57:1170–6.
34. Kulkarni HR, Singh A, Schuchardt C, Niepsch K, Sayeg M, Leshch Y, et al. PSMA-based Radioligand therapy for metastatic castration-resistant prostate cancer: the Bad Berka experience since 2013. J Nucl Med. 2016;57:97S–104S.
35. Ahmadzadehfar H, Wegen S, Yordanova A, Fimmers R, Kurpig S, Eppard E, et al. Overall survival and response pattern of castration-resistant metastatic prostate cancer to multiple cycles of radioligand therapy using [177Lu]Lu-PSMA-617. Eur J Nucl Med Mol Imaging. 2017;44:1448–54.
36. Brauer A, Grubert LS, Roll W, Schrader AJ, Schafers M, Bogemann M, et al. 177Lu-PSMA-617 radioligand therapy and outcome in patients with metastasized castration-resistant prostate cancer. Eur J Nucl Med Mol Imaging. 2017;44:1663–70.
37. Fendler WP, Reinhardt S, Ilhan H, Delker A, Boning G, Gildehaus FJ, et al. Preliminary experience with dosimetry, response and patient reported outcome after 177Lu-PSMA-617 therapy for metastatic castration-resistant prostate cancer. Oncotarget. 2017;8:3581–90.
38. Rahbar K, Ahmadzadehfar H, Kratochwil C, Haberkorn U, Schafers M, Essler M, et al. German multicenter study investigating 177Lu-PSMA-617 Radioligand therapy in advanced prostate cancer patients. J Nucl Med. 2017;58:85–90.
39. Rahbar K, Boegemann M, Yordanova A, Eveslage M, Schafers M, Essler M, et al. PSMA targeted radioligandtherapy in metastatic castration resistant prostate cancer after chemotherapy, abiraterone and/or enzalutamide. A retrospective analysis of overall survival. Eur J Nucl Med Mol Imaging. 2018;45:12–9.
40. Scarpa L, Buxbaum S, Kendler D, Fink K, Bektic J, Gruber L, et al. The 68Ga/177Lu theragnostic concept in PSMA targeting of castration-resistant prostate cancer: correlation of SUVmax values and absorbed dose estimates. Eur J Nucl Med Mol Imaging. 2017;44:788–800.
41. Yadav MP, Ballal S, Tripathi M, Damle NA, Sahoo RK, Seth A, et al. 177Lu-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.
42. Loriot Y, Bianchini D, Ileana E, Sandhu S, Patrikidou A, Pezaro C, et al. Antitumour activity of abiraterone acetate against metastatic castration-resistant prostate cancer progressing after docetaxel and enzalutamide (MDV3100). Ann Oncol. 2013;24:1807–12.
43. Noonan KL, North S, Bitting RL, Armstrong AJ, Ellard SL, Chi KN. Clinical activity of abiraterone acetate in patients with metastatic castration-resistant prostate cancer progressing after enzalutamide. Ann Oncol. 2013;24:1802–7.
44. Pezaro CJ, Omlin AG, Altavilla A, Lorente D, Ferraldeschi R, Bianchini D, et al. Activity of cabazitaxel in castration-resistant prostate cancer progressing after docetaxel and next-generation endocrine agents. Eur Urol. 2014;66:459–65.
45. Sella A, Sella T, Peer A, Berger R, Frank SJ, Gez E, et al. Activity of cabazitaxel after docetaxel and abiraterone acetate therapy in patients with castration-resistant prostate cancer. Clin Genitourin Cancer. 2014;12:428–32.
46. Al Nakouzi N, Le Moulec S, Albiges L, Wang C, Beuzeboc P, Gross-Goupil M, et al. Cabazitaxel remains active in patients progressing after docetaxel followed by novel androgen receptor pathway targeted therapies. Eur Urol. 2015;68:228–35.
47. Azad AA, Eigl BJ, Murray RN, Kollmannsberger C, Chi KN. Efficacy of enzalutamide following abiraterone acetate in chemotherapy-naive metastatic castration-resistant prostate cancer patients. Eur Urol. 2015;67:23–9.
48. Cheng HH, Gulati R, Azad A, Nadal R, Twardowski P, Vaishampayan UN, et al. Activity of enzalutamide in men with metastatic castration-resistant prostate cancer is affected by prior treatment with abiraterone and/or docetaxel. Prostate Cancer Prostatic Dis. 2015;18:122–7.
49. Sonpavde G, Bhor M, Hennessy D, Bhowmik D, Shen L, Nicacio L, et al. Sequencing of Cabazitaxel and Abiraterone acetate after docetaxel in metastatic castration-resistant prostate cancer: treatment patterns and clinical outcomes in multicenter community-based US oncology practices. Clin Genitourin Cancer. 2015;13:309–18.
50. Wissing MD, Coenen JL, van den Berg P, Westgeest HM, van den Eertwegh AJ, van Oort IM, et al. CAST: a retrospective analysis of cabazitaxel and abiraterone acetate sequential treatment in patients with metastatic castrate-resistant prostate cancer previously treated with docetaxel. Int J Cancer. 2015;136:E760–72.
51. Badrising SK, van der Noort V, van den Eertwegh AJ, Hamberg P, van Oort IM, van den Berg HP, et al. Prognostic parameters for response to enzalutamide after docetaxel and abiraterone treatment in metastatic castration-resistant prostate cancer patients; a possible time relation. Prostate. 2016;76:32–40.
52. Davies RS, Smith C, Lester JF. Third-line enzalutamide following docetaxel and Abiraterone in metastatic castrate-resistant prostate cancer. Anticancer Res. 2016;36:1799–803.
53. Kongsted P, Svane IM, Lindberg H, Bisbjerg R, Daugaard G, Sengelov L. Cabazitaxel as second-line or third-line therapy in patients with metastatic castration-resistant prostate cancer. Anti-Cancer Drugs. 2016;27:695–701.
54. Bando Y, Hinata N, Terakawa T, Furukawa J, Harada KI, Nakano Y, et al. Activity of cabazitaxel in patients with metastatic castration-resistant prostate cancer after treatment with single or dual regimens of novel androgen receptor-targeting agents. Med Oncol. 2017;34:163.
55. de Bono JS, Chowdhury S, Feyerabend S, Elliott T, Grande E, Melhem-Bertrandt A, et al. Antitumour activity and safety of enzalutamide in patients with metastatic castration-resistant prostate cancer previously treated with Abiraterone acetate plus prednisone for >/=24 weeks in Europe. Eur Urol 2017.
56. Emmett L, Willowson K, Violet J, Shin J, Blanksby A, Lee J. Lutetium 177 PSMA radionuclide therapy for men with prostate cancer: a review of the current literature and discussion of practical aspects of therapy. J Med Radiat Sci. 2017;64:52–60.
57. Fendler WP, Kratochwil C, Ahmadzadehfar H, Rahbar K, Baum RP, Schmidt M, et al. 177Lu-PSMA-617 therapy, dosimetry and follow-up in patients with metastatic castration-resistant prostate cancer. Nuklearmedizin. 2016;55:123–8.
58. Rathke H, Giesel FL, Flechsig P, Kopka K, Mier W, Hohenfellner M, et al. Repeated Lu-177-PSMA-617 radioligand therapy using treatment activities up to 9.3 GBq. J Nucl Med. 2017.
59. Eisenberger M, Hardy-Bessard AC, Kim CS, Geczi L, Ford D, Mourey L, et al. Phase III Study Comparing a Reduced Dose of Cabazitaxel (20 mg/m2) and the Currently Approved Dose (25 mg/m2) in Postdocetaxel Patients With Metastatic Castration-Resistant Prostate Cancer-PROSELICA. J Clin Oncol. 2017;135:3198–206.
60. Wei X, Schlenkhoff C, Schwarz B, Essler M, Ahmadzadehfar H. Combination of 177Lu-PSMA-617 and external radiotherapy for the treatment of cerebral metastases in patients with castration-resistant metastatic prostate cancer. Clin Nucl Med. 2017;42:704–6.
61. Fizazi K. Biennial report on genitourinary cancers. Eur J Cancer. 2016;66:125–30.
62. Estevez SV, Herranz UA, Calvo OF, Afonso Afonso FJ, Couto LS, Quintela ML, et al. Prostate cancer perspectives after chaarted: optimizing treatment sequence. Crit Rev Oncol Hematol. 2016;107:119–27.
63. Ryan CJ, Smith MR, de Bono JS, Molina A, Logothetis CJ, de Souza P, et al. Abiraterone in metastatic prostate cancer without previous chemotherapy. N Engl J Med. 2013;368:138–48.
64. Taplin ME, Armstrong AJ, Lin P, Krivoshik A, Phung, Parli T, et al. Clinical Outcomes of Chemotherapy-Naive Men with Metastatic Castration-Resistant Prostate Cancer and Low Baseline PSA Treated with Enzalutamide vs Placebo. J Urol. 2017;198:1324–32.
65. Fizazi K, Tran N, Fein L, Matsubara N, Rodriguez-Antolin A, Alekseev BY, et al. Abiraterone plus prednisone in metastatic, castration-sensitive prostate cancer. N Engl J Med. 2017;377:352–60.
66. Sweeney CJ, Chen YH, Carducci M, Liu G, Jarrard DF, Eisenberger M, et al. Chemohormonal therapy in metastatic hormone-sensitive prostate cancer. N Engl J Med. 2015;373:737–46.
67. Poorthuis MHF, Vernooij RWM, van Moorselaar RJA, de Reijke TM. First-line non-cytotoxic therapy in chemotherapy-naive patients with metastatic castration-resistant prostate cancer: a systematic review of 10 randomised clinical trials. BJU Int. 2017;119:831–45.