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Research ArticleBRIEF COMMUNICATION
Open Access

Safety and Survival Outcomes of 177Lu-Prostate-Specific Membrane Antigen Therapy in Patients with Metastatic Castration-Resistant Prostate Cancer with Prior 223Ra treatment: The RALU Study

Kambiz Rahbar, Markus Essler, Kim M. Pabst, Matthias Eiber, Christian la Fougère, Vikas Prasad, Philipp Rassek, Ergela Hasa, Helmut Dittmann, Ralph A. Bundschuh, Wolfgang P. Fendler, Milena Kurtinecz, Anja Schmall, Frank Verholen and Oliver Sartor
Journal of Nuclear Medicine April 2023, 64 (4) 574-578; DOI: https://doi.org/10.2967/jnumed.122.264456
Kambiz Rahbar
1Department of Nuclear Medicine, University of Münster Medical Center, Münster, Germany;
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Markus Essler
2Department of Nuclear Medicine, University Hospital Bonn, Bonn, Germany;
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Kim M. Pabst
3Department of Nuclear Medicine, German Cancer Consortium (DKTK) University Hospital Essen, Essen, Germany;
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Matthias Eiber
4Department of Nuclear Medicine, Technical University of Munich, Munich, Germany;
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Christian la Fougère
5Department of Nuclear Medicine and Clinical Molecular Imaging, University Hospital Tübingen, Tübingen, Germany;
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Vikas Prasad
6Department of Nuclear Medicine, University of Ulm, Ulm, Germany;
7International Centers for Precision Oncology Foundation, Ravensburg, Germany;
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Philipp Rassek
1Department of Nuclear Medicine, University of Münster Medical Center, Münster, Germany;
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Ergela Hasa
4Department of Nuclear Medicine, Technical University of Munich, Munich, Germany;
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Helmut Dittmann
5Department of Nuclear Medicine and Clinical Molecular Imaging, University Hospital Tübingen, Tübingen, Germany;
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Ralph A. Bundschuh
8Department of Nuclear Medicine, Medical Faculty, University of Augsburg, Augsburg, Germany;
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Wolfgang P. Fendler
3Department of Nuclear Medicine, German Cancer Consortium (DKTK) University Hospital Essen, Essen, Germany;
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Milena Kurtinecz
9Bayer HealthCare Pharmaceuticals, Whippany, New Jersey;
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Anja Schmall
10Bayer Consumer Care, Basel, Switzerland; and
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Frank Verholen
10Bayer Consumer Care, Basel, Switzerland; and
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Oliver Sartor
11Tulane Cancer Center, Tulane Medical School, New Orleans, Louisiana
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Abstract

The radium lutetium (RALU) study evaluated the feasibility of sequential α- and β-emitter use in patients with bone-predominant metastatic castration-resistant prostate cancer. Methods: This preplanned interim retrospective analysis investigated safety and survival outcomes with 177Lu-PSMA in patients treated with prior 223Ra. Results: Forty-nine patients were evaluated. Patients received a median of 6 223Ra injections; 59% of patients received at least 4 177Lu-PSMA cycles. Most (69%) patients received at least 4 life-prolonging therapies before 177Lu-PSMA. Common Terminology Criteria for Adverse Events grade 3–4 treatment-emergent adverse events during 177Lu-PSMA therapy and a 30-d follow-up period included anemia (18%) and thrombocytopenia (2%). Median overall survival was 12.6 mo (95% CI, 8.8–16.1 mo) and 31.4 mo (95% CI, 25.7–37.6 mo) from starting 177Lu-PSMA or 223Ra, respectively. Conclusion: 177Lu-PSMA treatment was well tolerated in patients who had received prior 223Ra. 223Ra use before 177Lu-PSMA is feasible and can be considered for future assessment of the optimal treatment sequence.

  • targeted α-therapy
  • 223Ra
  • 177Lu-PSMA
  • metastatic castration-resistant prostate cancer
  • real-world practice

Overall survival and quality of life in patients with bone-predominant metastatic castration-resistant prostate cancer (mCRPC) was improved by 223Ra-dichloride, a targeted α-therapy with a good safety profile (1). 223Ra therapy results in low myelosuppression rates, and recent preclinical data demonstrated its transient effect on the bone marrow without long-term effects (1,2). Therefore, earlier incorporation of 223Ra in the treatment sequence may facilitate optimal build-in of life-prolonging therapies to improve survival outcomes.

The VISION study investigated a β-emitter, 177Lu-PSMA-617, targeting PSMA-expressing cells and found prolonged overall survival and acceptable safety in heavily pretreated patients with mCRPC (3). Another 177Lu-PSMA radioligand (177Lu-PSMA-I&T) was also well tolerated, with few hematologic adverse events (AEs) of grade 3 or higher (4).

223Ra and 177Lu-PSMA regulatory approval (in some countries) for patients with mCRPC, albeit in different patient populations, prompted us to investigate the safety and survival outcomes of sequential 223Ra and 177Lu-PSMA. In VISION, 17.4% of patients received 223Ra therapy before 177Lu-PSMA without adversely affecting efficacy, but safety has not been reported for this subgroup (5). However, retrospective studies have shown that using 223Ra before 177Lu-PSMA is feasible, with acceptable safety (6,7). Moreover, 177Lu-PSMA-617 initiation at no more than 8 wk after 223Ra in patients with progressive bone-metastatic disease was effective, with acceptable safety (8). We analyzed interim data from the observational radium lutetium (RALU) study to further evaluate safety and survival for sequential 223Ra and 177Lu-PSMA therapy in patients with mCRPC.

MATERIALS AND METHODS

The RALU study was a retrospective, multicenter medical chart review investigating the safety of 177Lu-PSMA in patients with mCRPC previously treated with 223Ra. This analysis includes patients treated in Germany. Patients were at least 18 y old with mCRPC and received at least 1 223Ra injection and subsequently at least 1 177Lu-PSMA cycle.

The retrospective observation period started at mCRPC diagnosis and ended either at the last available visit or death, whichever occurred first. Prebaseline, baseline, and follow-up period definitions are shown in Figure 1.

FIGURE 1.
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FIGURE 1.

RALU study design. *From 177Lu-PSMA start to 90 d after last dose. †From 177Lu-PSMA start to 30 d after last dose. ALP = alkaline phosphatase; OS = overall survival; PSA = prostate-specific antigen; SAEs = serious AEs.

The primary endpoint was the safety of 177Lu-PSMA after 223Ra therapy. AEs used Common Terminology Criteria for Adverse Events grading. Secondary endpoints included OS, time to next treatment, and change from baseline in serum prostate-specific antigen and alkaline phosphatase levels. AEs and grade 3–4 laboratory abnormalities were recorded as per Figure 1.

The study was conducted in accordance with relevant guidelines and regulations (supplemental methods).

RESULTS

This preplanned interim analysis included medical records from 49 patients (data cutoff, January 31, 2022) (Table 1). Before 177Lu-PSMA initiation, 31% (15/49) of patients had visceral metastases, and median prostate-specific antigen and alkaline phosphatase values were 287.0 ng/mL and 142.5 U/L, respectively (Table 1). At least 1 line of taxane-based chemotherapy was received by 92% (45/49) of patients before 177Lu-PSMA initiation, with 51% (25/49) receiving taxane-based chemotherapy between 223Ra and 177Lu-PSMA (Table 1). Before starting 177Lu-PSMA, 63% (30/49) of patients received at least 4 life-prolonging therapies (docetaxel, cabazitaxel, abiraterone, enzalutamide, and 223Ra; Table 1; Fig. 2). Most patients received chemotherapy before 177Lu-PSMA; 92% received docetaxel, and 18% received cabazitaxel (Fig. 2).

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TABLE 1.

Baseline Characteristics Before Starting 177Lu-PSMA

FIGURE 2.
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FIGURE 2.

Use of life-prolonging therapies. *Chemotherapy was not used concomitantly with 177Lu-PSMA.

The median time from the first 223Ra and 177Lu-PSMA dose to the end of observation was 28.0 mo (range, 11.0–68.2 mo) and 8.9 mo (range, 1.4–63.9 mo), respectively. A median of 6 223Ra injections was administered, and 71% (35/49) of patients received 5–6 223Ra injections. The median 223Ra therapy duration was 4.7 mo (range, 1.0–7.0 mo). All patients received 177Lu-PSMA (177Lu-PSMA-617 [67%] or 177Lu-PSMA-I&T [33%]), and 59% (29/49) received at least 4 177Lu-PSMA cycles. The median 177Lu-PSMA therapy duration was 4.9 mo (range, 0–57.1 mo). The median time from the last 223Ra injection to the first 177Lu-PSMA dose was 9.3 mo (range, 0.9–41.9 mo). Overall, 51% (25/59) of patients received taxane-based chemotherapy during or after 223Ra and until 60 d before 177Lu-PSMA.

During 177Lu-PSMA, 92% (45/49) of patients experienced any grade of treatment-emergent AEs and 41% (20/49) experienced grade 3–4 (Supplemental Table 1). Grade 3–4 anemia and thrombocytopenia occurred in 18% (9/49) and 2% (1/49) of patients, respectively. Grade 1–2 dry mouth occurred in 27% (13/49) of patients; none had grade 3–4 dry mouth. One patient (2%) had grade 1–2 dry eye. The incidence of grade 3–4 laboratory abnormalities was highest for anemia (35% [17/49]) and thrombocytopenia (13% [6/49]) (Table 2). No grade 5 toxicities occurred.

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TABLE 2.

Incidence of Grade 3–4 Laboratory Abnormalities Measured from 177Lu-PSMA Start to 90 Days After Last Dose

Median overall survival was 12.6 mo (95% CI, 8.8–16.1 mo) and 31.4 mo (95% CI, 25.7–37.6 mo) from the first dose of 177Lu-PSMA and 223Ra, respectively (Fig. 3). During 177Lu-PSMA, 39% and 29% of patients had at least a 30% or 50% decline in prostate-specific antigen (best response), respectively; corresponding alkaline phosphatase declines were 6% and 4%.

FIGURE 3.
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FIGURE 3.

Kaplan–Meier plots for overall survival calculated from first 177Lu-PSMA (A) and 223Ra (B) dose.

DISCUSSION

Randomized trials have demonstrated low myelosuppression rates in patients with mCRPC receiving 223Ra or 177Lu-PSMA (1,3,9). However, chemotherapy and advanced disease affecting bone marrow function can increase myelosuppression rates in this setting (10–12). Therefore, in real-world practice, radiopharmaceutical therapy after prior chemotherapy may result in more serious hematologic AEs.

177Lu-PSMA after 223Ra treatment had an acceptable safety profile. Notably, this was despite the heavy pretreatment of the patient population, with more than 90% of patients having received chemotherapy in addition to 223Ra and 177Lu-PSMA. Grade 3–4 anemia and thrombocytopenia incidences were 18% and 2%, respectively, consistent with the retrospective analysis of patients receiving the 223Ra and 177Lu-PSMA sequence in the real-world REASSURE study (15% and 4%, respectively) (6). When 177Lu-PSMA was given within 8 wk of 223Ra, the incidence of anemia of at least grade 3 was similar (18%), but the rates of leukopenia and thrombocytopenia of at least grade 3 were higher than reported here (14% vs. 0 and 21% vs. 2%, respectively) (8).

The median overall survival from the start of 177Lu-PSMA or 223Ra therapy (12.6 and 31.4 mo, respectively) corresponded to that reported in REASSURE (13.2 and 28.0 mo, respectively) (6). In patients with mCRPC who underwent 177Lu-PSMA therapy in the WARMTH study, overall survival was longer in patients with bone metastases receiving prior 223Ra than in those who did not (16 vs. 12 mo in patients with 6–20 bone lesions, P = 0.038, and 11 vs. 7 mo in patients with diffuse involvement, P = 0.034) (12).

This study’s strength is underlined by broad inclusion criteria and high-quality data with few missing datapoints. Accordingly, we could effectively evaluate 177Lu-PSMA safety in patients with a history of 223Ra therapy who received chemotherapy, before or after 223Ra treatment. Nevertheless, a retrospective study design may have contributed to a patient selection bias due to the preset outcomes of interest. Other limitations include retrospective AE grading, lack of ascertainment of 177Lu-PSMA doses and schedules, and a lack of comparison to patients who were not pretreated with 223Ra. Despite small patient numbers, patients were managed and treated in high-volume German nuclear medicine centers with extensive 223Ra and 177Lu-PSMA experience.

CONCLUSION

This retrospective cohort study demonstrated that, for patients with bone-predominant mCRPC who were receiving 223Ra in routine care, subsequent 177Lu-PSMA treatment was clinically feasible and well tolerated, with limited myelosuppression. Survival outcomes reflected those of previous reports. Therefore, in patients with bone-predominant mCRPC, 223Ra use before 177Lu-PSMA can be considered in future assessments of the optimal sequence for life-prolonging therapies.

DISCLOSURE

Cancer Communications and Consultancy Ltd., Cheshire, U.K., provided medical writing assistance (funded by Bayer). Dr. Lila Adnane (Bayer) provided editorial assistance. Kambiz Rahbar receives honoraria from Advanced Accelerator Applications (AAA) and Bayer and has a consultancy/advisory role with ABX GmbH, ABX-CRO, Bayer, and AAA. Markus Essler has a consultancy/advisory role with Bayer, AAA, and Ipsen and receives travel funds from Ipsen. Matthias Eiber owns stocks or has other ownership interests in Novartis and Telix Pharmaceuticals; has a consultancy/advisory role with Blue Earth Diagnostics, ABX Advanced Biochemical Compounds, Janssen Oncology, Telix Pharmaceuticals, and Novartis; receives research funding from Siemens, ABX Advanced Biochemical Compounds, Blue Earth Diagnostics, and Bayer; has a patent application for rhPSMA; and receives travel funds from Bayer Schering Pharma. Christian la Fougère has a consultancy/advisory role with Novartis, EUSA-Pharma, Ipsen, Oncodesign, and Sirtex Medical and receives research funding from Oncovision. Vikas Prasad receives honoraria from AAA; has a consultancy/advisory role with Bayer; and receives research funding from Ipsen. Wolfgang Fendler receives honoraria from Parexel and AAA; has a consultancy/advisory role with Janssen, Calyx, and Bayer; and receives research funding from SOFIE. Philipp Rassek is an employee of Porterhouse Group AG Paracelsus Kliniken. Helmut Dittmann has a consultancy/advisory role with Bayer, Ipsen, and Eisai AG. Ralph Bundschuh receives honoraria from Eisai AG and has a consultancy/advisory role with Bayer. Kim Pabst receives a Junior Clinician Scientist Stipend from the University Medicine Essen Clinician Scientist Academy (sponsor: Faculty of Medicine and Deutsche Forschungsgemeinschaft) and research funding from Bayer. Milena Kurtinecz, and Frank Verholen are employees of Bayer. Oliver Sartor has a consultancy/advisory role with Bayer, Sanofi, AstraZeneca, Dendreon, Constellation Pharmaceuticals, AAA, Pfizer, Bristol-Myers Squibb, Bavarian Nordic, EMD Serono, Astellas Pharma, Progenics, Blue Earth Diagnostics, Myovant Sciences, Myriad Genetics, Novartis, Clarity Pharmaceuticals, Fusion Pharmaceuticals, Isotopen Technologien, Janssen, Noxopharm, Clovis Oncology, Noria Therapeutics, Point Biopharma, TeneoBio, Telix Pharmaceuticals, and Theragnostics; receives travel funds from Bayer, Johnson & Johnson, Sanofi, AstraZeneca, and Progenics; provides expert testimony for Sanofi; owns stocks or has other ownership interests in Lilly, GlaxoSmithKline, Abbvie, Cardinal Health, United Health Group, PSMA Therapeutics, Clarity Pharmaceuticals, Noria Therapeutics, and Clovis Oncology; and receives research funding from Bayer, Sanofi, Endocyte, Merck, InVitae, Constellation Pharmaceuticals, AAA, AstraZeneca, Dendreon, SOTIO, Janssen, and Progenics. No other potential conflict of interest relevant to this article was reported.

KEY POINTS

QUESTION: Is it safe to use 177Lu-PSMA to treat patients with mCRPC if they have previously received 223Ra?

PERTINENT FINDINGS: Low rates of overall and hematologic AEs indicated an acceptable safety profile for this treatment sequence. Median OS was 12.6 and 31.4 mo from the first dose of 177Lu-PSMA and 223Ra, respectively, and 39% of patients had at least a 30% decline in prostate-specific antigen.

IMPLICATIONS FOR PATIENT CARE: Introduction of 223Ra early in the treatment sequence in patients with bone-predominant mCRPC and subsequent treatment with 177Lu-PSMA is feasible, well tolerated, and effective.

Footnotes

  • Published online Oct. 27, 2022.

  • © 2023 by the Society of Nuclear Medicine and Molecular Imaging.

Immediate Open Access: Creative Commons Attribution 4.0 International License (CC BY) allows users to share and adapt with attribution, excluding materials credited to previous publications. License: https://creativecommons.org/licenses/by/4.0/. Details: http://jnm.snmjournals.org/site/misc/permission.xhtml.

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  • Received for publication July 1, 2022.
  • Revision received October 12, 2022.
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Journal of Nuclear Medicine: 64 (4)
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Safety and Survival Outcomes of 177Lu-Prostate-Specific Membrane Antigen Therapy in Patients with Metastatic Castration-Resistant Prostate Cancer with Prior 223Ra treatment: The RALU Study
Kambiz Rahbar, Markus Essler, Kim M. Pabst, Matthias Eiber, Christian la Fougère, Vikas Prasad, Philipp Rassek, Ergela Hasa, Helmut Dittmann, Ralph A. Bundschuh, Wolfgang P. Fendler, Milena Kurtinecz, Anja Schmall, Frank Verholen, Oliver Sartor
Journal of Nuclear Medicine Apr 2023, 64 (4) 574-578; DOI: 10.2967/jnumed.122.264456

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Safety and Survival Outcomes of 177Lu-Prostate-Specific Membrane Antigen Therapy in Patients with Metastatic Castration-Resistant Prostate Cancer with Prior 223Ra treatment: The RALU Study
Kambiz Rahbar, Markus Essler, Kim M. Pabst, Matthias Eiber, Christian la Fougère, Vikas Prasad, Philipp Rassek, Ergela Hasa, Helmut Dittmann, Ralph A. Bundschuh, Wolfgang P. Fendler, Milena Kurtinecz, Anja Schmall, Frank Verholen, Oliver Sartor
Journal of Nuclear Medicine Apr 2023, 64 (4) 574-578; DOI: 10.2967/jnumed.122.264456
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  • Clinical Management of Advanced Prostate Cancer: Where Does Radiopharmaceutical Therapy Fit in the Treatment Algorithm?
  • Sequential and Combination Therapies of 223RaCl2 and Prostate-Specific Membrane Antigen Radioligand Therapy
  • 177Lu-Prostate-Specific Membrane Antigen Therapy in Patients with Metastatic Castration-Resistant Prostate Cancer and Prior 223Ra (RALU Study)
  • SNMMI Consensus Statement on Patient Selection and Appropriate Use of 177Lu-PSMA-617 Radionuclide Therapy
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Keywords

  • targeted α-therapy
  • 223Ra
  • 177Lu-PSMA
  • metastatic castration-resistant prostate cancer
  • real-world practice
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