Change of management by using hybrid imaging with radiolabelled choline in biochemical recurrent prostate cancer: a systematic review and a meta-analysis

Abstract

Background

Hybrid imaging with radiolabelled choline has been extensively used in patients with biochemical recurrent prostate cancer (BRPCa). A useful information for the clinicians could be the change of management that can be obtained by using these imaging modalities in BRPCa. Therefore, we aimed to perform a systematic review and meta-analysis to add evidence-based data in this setting.

Methods

A comprehensive computer literature search of studies listed in PubMed/MEDLINE, EMBASE and Cochrane library databases through February 2020 and regarding the change of management by using hybrid imaging with radiolabelled choline in BRPCa was performed. A pooled analysis evaluating the percentage of change of management performing hybrid imaging with radiolabelled choline in BRPCa patients was carried out.

Results

Nineteen studies on the change of management by using radiolabelled choline PET/CT or PET/MRI in 1931 BRPCa patients were included in the meta-analysis. Overall, a change of management by using radiolabelled choline PET/CT or PET/MRI was demonstrated in 45.8% (95% confidence interval 39.9–51.6%) of BRPCa patients. Significant heterogeneity among the selected studies was found, whereas a significant publication bias was excluded.

Conclusions

Our meta-analysis demonstrated that hybrid imaging with radiolabelled choline may change the management in about half of BRPCa patients. However, as for other PET radiopharmaceuticals, large-scale prospective multicentric studies are needed to investigate whether BRPCa patients can benefit from PET-related treatment changes.

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References

  1. 1.

    Fanti S, Minozzi S, Antoch G, Banks I, Briganti A, Carrio I, Chiti A, Clarke N, Eiber M, De Bono J, Fizazi K, Gillessen S, Gledhill S, Haberkorn U, Herrmann K, Hicks RJ, Lecouvet F, Montironi R, Ost P, O’Sullivan JM, Padhani AR, Schalken JA, Scher HI, Tombal B, van Moorselaar RJA, Van Poppel H, Vargas HA, Walz J, Weber WA, Wester HJ, Oyen WJG (2018) Consensus on molecular imaging and theranostics in prostate cancer. Lancet Oncol 19(12):e696–e708

    Article  Google Scholar 

  2. 2.

    De Visschere PJL, Standaert C, Fütterer JJ, Villeirs GM, Panebianco V, Walz J, Maurer T, Hadaschik BA, Lecouvet FE, Giannarini G, Fanti S (2019) A systematic review on the role of imaging in early recurrent prostate cancer. Eur Urol Oncol 2(1):47–76

    Article  Google Scholar 

  3. 3.

    Annunziata S, Pizzuto DA, Treglia G (2020) Diagnostic performance of PET imaging using different radiopharmaceuticals in prostate cancer according to published meta-analyses. Cancers 12(8):2153. https://doi.org/10.3390/cancers12082153

    CAS  Article  PubMed Central  Google Scholar 

  4. 4.

    Treglia G, Pereira Mestre R, Ferrari M, Bosetti DG, Pascale M, Oikonomou E, De Dosso S, Jermini F, Prior JO, Roggero E, Giovanella L (2019) Radiolabelled choline versus PSMA PET/CT in prostate cancer restaging: a meta-analysis. Am J Nucl Med Mol Imaging 9(2):127–139

    PubMed  PubMed Central  Google Scholar 

  5. 5.

    Giovacchini G, Giovannini E, Leoncini R, Riondato M, Ciarmiello A (2017) PET and PET/CT with radiolabeled choline in prostate cancer: a critical reappraisal of 20 years of clinical studies. Eur J Nucl Med Mol Imaging 44(10):1751–1776

    CAS  Article  Google Scholar 

  6. 6.

    Evangelista L, Cuppari L, Zattoni F, Mansi L, Bombardieri E (2019) The future of choline PET in the era of prostate specific membrane antigen. Q J Nucl Med Mol Imaging 63(1):19–28

    Article  Google Scholar 

  7. 7.

    Treglia G, Ceriani L, Sadeghi R, Giovacchini G, Giovanella L (2014) Relationship between prostate-specific antigen kinetics and detection rate of radiolabelled choline PET/CT in restaging prostate cancer patients: a meta-analysis. Clin Chem Lab Med 52(5):725–733

    CAS  Article  Google Scholar 

  8. 8.

    McInnes MDF, Moher D, Thombs BD, McGrath TA, Bossuyt PM, The PRISMA-DTA Group, Clifford T, Cohen JF, Deeks JJ, Gatsonis C, Hooft L, Hunt HA, Hyde CJ, Korevaar DA, Leeflang MMG, Macaskill P, Reitsma JB, Rodin R, Rutjes AWS, Salameh JP, Stevens A, Takwoingi Y, Tonelli M, Weeks L, Whiting P, Willis BH (2018) Preferred reporting items for a systematic review and meta-analysis of diagnostic test accuracy studies: the PRISMA-DTA statement. JAMA 319(4):388–396

    Article  Google Scholar 

  9. 9.

    Sadeghi R, Treglia G (2017) Systematic reviews and meta-analyses of diagnostic studies: a practical guideline. Clin Transl Imaging 5:83–87

    Article  Google Scholar 

  10. 10.

    Whiting PF, Rutjes AW, Westwood ME, Mallett S, Deeks JJ, Reitsma JB, Leeflang MM, Sterne JA, Bossuyt PM, QUADAS-2 Group (2011) QUADAS-2: a revised tool for the quality assessment of diagnostic accuracy studies. Ann Intern Med 155(8):529–536

    Article  Google Scholar 

  11. 11.

    Higgins JP, Thompson SG (2002) Quantifying heterogeneity in a meta-analysis. Stat Med 21:1539–1558

    Article  Google Scholar 

  12. 12.

    Harbord RM, Egger M, Sterne JA (2006) A modified test for small-study effects in meta-analyses of controlled trials with binary endpoints. Stat Med 25:3443–3457

    Article  Google Scholar 

  13. 13.

    Achard V, Lamanna G, Denis A, De Perrot T, Mainta IC, Ratib O, Iselin C, Miralbell R, Garibotto V, Zilli T (2019) Recurrent prostate cancer after radical prostatectomy: restaging performance of 18F-choline hybrid PET/MRI. Med Oncol 36:67

    Article  Google Scholar 

  14. 14.

    Alongi F, Comito T, Villa E, Lopci E, Iftode C, Mancosu P, Navarria P, Rocco L, Tomatis S, Chiti A, Scorsetti M (2014) What is the role of [11C]choline PET/CT in decision making strategy before postoperative salvage radiation therapy in prostate cancer patients? Acta Oncol 53:990–992

    Article  Google Scholar 

  15. 15.

    Ceci F, Herrmann K, Castellucci P, Graziani T, Bluemel C, Schiavina R, Vollmer C, Droll S, Brunocilla E, Mazzarotto R, Buck AK, Fanti S (2014) Impact of 11C-choline PET/CT on clinical decision making in recurrent prostate cancer: results from a retrospective two-centre trial. Eur J Nucl Med Mol Imaging 41:2222–2231

    Article  Google Scholar 

  16. 16.

    Colombié M, Campion L, Bailly C, Rusu D, Rousseau T, Mathieu C, Ferrer L, Rousseau N, Kraeber-Bodéré F, Rousseau C (2015) Prognostic value of metabolic parameters and clinical impact of 18F-fluorocholine PET/CT in biochemical recurrent prostate cancer. Eur J Nucl Med Mol Imaging 42:1784–1793

    Article  Google Scholar 

  17. 17.

    Couñago F, Recio M, Maldonado A, Del Cerro E, Díaz-Gavela AA, Thuissard IJ, Sanz-Rosa D, Marcos FJ, Olaciregui K, Mateo M, Cerezo L (2016) Evaluation of tumor recurrences after radical prostatectomy using 18F-Choline PET/CT and 3T multiparametric MRI without endorectal coil: a single center experience. Cancer Imaging 16:42

    Article  Google Scholar 

  18. 18.

    D’Agostino GR, Lopci E, Di Brina L, Franzese C, Tomatis S, Castello A, Franceschini D, Navarria P, Chiti A, Scorsetti M (2018) Role of 11C-choline PET/CT in radiation therapy planning of patients with prostate cancer. Nucl Med Commun 39:951–956

    Article  Google Scholar 

  19. 19.

    Emmett L, Metser U, Bauman G, Hicks RJ, Weickhardt A, Davis ID, Punwani S, Pond G, Chua S, Ho B, Johnston E, Pouliot F, Scott AM (2019) Prospective, Multisite, International Comparison of 18F-fluoromethylcholine PET/CT, multiparametric MRI, and 68Ga-HBED-CC PSMA-11 PET/CT in men with high-risk features and biochemical failure after radical prostatectomy: clinical performance and patient outcomes. J Nucl Med 60:794–800

    CAS  Article  Google Scholar 

  20. 20.

    Gauthé M, Aveline C, Lecouvet F, Michaud L, Rousseau C, Tassart M, Cussenot O, Talbot JN, Durand-Zaleski I (2019) Impact of sodium 18F-fluoride PET/CT, 18F-fluorocholine PET/CT and whole-body diffusion-weighted MRI on the management of patients with prostate cancer suspicious for metastasis: a prospective multicentre study. World J Urol 37:1587–1595

    Article  Google Scholar 

  21. 21.

    Gauvin S, Cerantola Y, Haberer E, Pelsser V, Probst S, Bladou F, Anidjar M (2017) Initial single-centre Canadian experience with 18F-fluoromethylcholinepositron emission tomography-computed tomography (18F-FCH PET/CT) for biochemical recurrence in prostate cancer patients initiallytreated with curative intent. Can Urol Assoc J 11:47–52

    Article  Google Scholar 

  22. 22.

    Gillebert Q, Huchet V, Rousseau C, Cochet A, Olivier P, Courbon F, Gontier E, Nataf V, Balogova S, Talbot JN, Other ICHOROPRO investigators (2018) 18F-fluorocholine PET/CT in patients with occult biochemical recurrence of prostate cancer: Detection rate, impact on management and adequacy of impact. A prospective multicentre study. PLoS ONE 13:e0191487

    Article  Google Scholar 

  23. 23.

    Goldstein J, Even-Sapir E, Ben-Haim S, Saad A, Spieler B, Davidson T, Berger R, Weiss I, Appel S, Lawrence YR, Symon Z (2017) Does choline PET/CT change the management of prostate cancer patients with biochemical failure? Am J Clin Oncol 40:256–259

    CAS  Article  Google Scholar 

  24. 24.

    Gómez-de la Fuente FJ, Martínez-Rodríguez I, De Arcocha-Torres M, Quirce R, Jiménez-Bonilla J, Martínez-Amador N, Sánchez-Salmón A, Lucas-Velázquez B, Cuenca-Vera O, Banzo I (2019) Effect of positive carbon-11-choline PET/CT results in the therapeutic management of prostate cancer biochemical relapse. Nucl Med Commun 40:79–85

    Article  Google Scholar 

  25. 25.

    Jereczek-Fossa BA, Rodari M, Bonora M, Fanti P, Fodor C, Pepe G, Lopci E, Zerini D, Vischioni B, Baroni G, Matei DV, De Cobelli O, Chiti A, Orecchia R (2014) [11C]choline PET/CT impacts treatment decision making in patients with prostate cancer referred for radiotherapy. Clin Genitourin Cancer 12:155–159

    Article  Google Scholar 

  26. 26.

    Lamanna G, Tabouret-Viaud C, Rager O, Jorcano S, Vees HJ, Seimbille Y, Zaidi H, Ratib O, Buchegger F, Miralbell R, Zilli T, Garibotto V (2017) Long-term results of a comparative PET/CT and PET/MRI study of 11C-acetate and 18F-fluorocholine for restaging of early recurrent prostate cancer. Clin Nucl Med 42:e242–e246

    Article  Google Scholar 

  27. 27.

    Mitchell CR, Lowe VJ, Rangel LJ, Hung JC, Kwon ED, Karnes RJ (2013) Operational characteristics of 11C-choline positron emission tomography/computerized tomography for prostate cancer with biochemical recurrence after initial treatment. J Urol 189:1308–1313

    Article  Google Scholar 

  28. 28.

    Morigi JJ, Stricker PD, van Leeuwen PJ, Tang R, Ho B, Nguyen Q, Hruby G, Fogarty G, Jagavkar R, Kneebone A, Hickey A, Fanti S, Tarlinton L, Emmett L (2015) Prospective comparison of 18F-fluoromethylcholine versus 68Ga-PSMA PET/CT in prostate cancer patients who have rising PSA after curative treatment and are being considered for targeted therapy. J Nucl Med 56:1185–1190

    CAS  Article  Google Scholar 

  29. 29.

    Niziers V, Boissier R, Borchiellini D, Deville JL, Khoury C, Durand M, Toledano H, Albert T, Branger N, Bandelier Q, Ouvrier MJ, Gabriel S, Hoch B, Gross E, Walz J, Brenot-Rossi I, Pignot G (2020) “Real-world” evaluation of 18F-Choline PET/CT practices in prostate cancer patients and impact on changes in therapeutic strategy. Urol Oncol 38:2.e1-2.e9

    Article  Google Scholar 

  30. 30.

    Samper Ots P, Luis Cardo A, Vallejo Ocaña C, Cabeza Rodríguez MA, Glaria Enríquez LA, Couselo Paniagua ML, Olivera Vegas J (2019) Diagnostic performance of 18F-choline PET-CT in prostate cancer. Clin Transl Oncol 21:766–773

    CAS  Article  Google Scholar 

  31. 31.

    Souvatzoglou M, Krause BJ, Pürschel A, Thamm R, Schuster T, Buck AK, Zimmermann F, Molls M, Schwaiger M, Geinitz H (2011) Influence of 11C-choline PET/CT on the treatment planning for salvage radiation therapy in patients with biochemical recurrence of prostate cancer. Radiother Oncol 99:193–200

    Article  Google Scholar 

  32. 32.

    Soyka JD, Muster MA, Schmid DT, Seifert B, Schick U, Miralbell R, Jorcano S, Zaugg K, Seifert HH, Veit-Haibach P, Strobel K, Schaefer NG, Husarik DB, Hany TF (2012) Clinical impact of 18F-choline PET/CT in patients with recurrent prostate cancer. Eur J Nucl Med Mol Imaging 39:936–943

    CAS  Article  Google Scholar 

  33. 33.

    Tuncel M, Souvatzoglou M, Herrmann K, Stollfuss J, Schuster T, Weirich G, Wester HJ, Schwaiger M, Krause BJ (2008) [(11)C]Choline positron emission tomography/computed tomography for staging and restaging of patients with advanced prostate cancer. Nucl Med Biol 35:689–695

    CAS  Article  Google Scholar 

  34. 34.

    Fuchs S, Grössmann N, Ferch M, Busse R, Wild C (2019) Evidence-based indications for the planning of PET or PET/CT capacities are needed. Clin Transl Imaging 7:65–81

    Article  Google Scholar 

  35. 35.

    Treglia G (2013) Sadeghi R (2013) Meta-analyses and systematic reviews on PET and PET/CT in oncology: the state of the art. Clin Transl Imaging 1:73–75

    Article  Google Scholar 

  36. 36.

    Fanti S, Giammarile F (2016) Molecular imaging and prostate cancer: unmet clinical needs and future perspectives. Clin Transl Imaging 4:421–422

    Article  Google Scholar 

  37. 37.

    Omlin A, Mueller J, Gillessen S (2016) The oncologists’ unmet clinical needs for imaging in advanced prostate cancer. Clin Transl Imaging 4:423–431

    Article  Google Scholar 

  38. 38.

    Han S, Woo S, Kim YJ, Suh CH (2018) Impact of 68Ga-PSMA PET on the management of patients with prostate cancer: a systematic review and meta-analysis. Eur Urol 74(2):179–190

    CAS  Article  Google Scholar 

  39. 39.

    Diao W, Cao Y, Su D, Jia Z (2020) 68Ga-prostate-specific membrane antigen tracers can alter the management of more than half of prostate cancer patients with biochemical recurrence. BJU Int. https://doi.org/10.1111/bju.15257

    Article  PubMed  Google Scholar 

  40. 40.

    Ceci F, Castellucci P, Polverari G, Iagaru A (2020) Clinical application of fluciclovine PET, choline PET and gastrin-releasing polypeptide receptor (bombesin) targeting PET in prostate cancer. Curr Opin Urol 30(5):641–648

    PubMed  Google Scholar 

  41. 41.

    De Bruycker A, Spiessens A, Dirix P, Koutsouvelis N, Semac I, Liefhooghe N, Gomez-Iturriaga A, Everaerts W, Otte F, Papachristofilou A, Scorsetti M, Shelan M, Siva S, Ameye F, Guckenberger M, Heikkilä R, Putora PM, Zapatero A, Conde-Moreno A, Couñago F, Vanhoutte F, Goetghebeur E, Reynders D, Zilli T, Ost P (2020) PEACE V—salvage treatment of OligoRecurrent nodal prostate cancer metastases (STORM): a study protocol for a randomized controlled phase II trial. BMC Cancer 20(1):406

    Article  Google Scholar 

  42. 42.

    Decaestecker K, De Meerleer G, Ameye F, Fonteyne V, Lambert B, Joniau S, Delrue L, Billiet I, Duthoy W, Junius S, Huysse W, Lumen N, Ost P (2014) Surveillance or metastasis-directed Therapy for OligoMetastatic Prostate cancer recurrence (STOMP): study protocol for a randomized phase II trial. BMC Cancer 14:671

    Article  Google Scholar 

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Funding

This study was performed with a grant received by the Advisory Board of Research of Ente Ospedaliero Cantonale (ABREOC).

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Correspondence to Giorgio Treglia.

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Ferrari, M., Renard, J., Pereira Mestre, R. et al. Change of management by using hybrid imaging with radiolabelled choline in biochemical recurrent prostate cancer: a systematic review and a meta-analysis. Clin Transl Imaging 9, 57–71 (2021). https://doi.org/10.1007/s40336-020-00407-8

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Keywords

  • Prostate cancer
  • Management
  • PET
  • Choline
  • Multimodal imaging
  • Hybrid imaging
  • Meta-analysis