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Comparison of PSMA-PET/CT, choline-PET/CT, NaF-PET/CT, MRI, and bone scintigraphy in the diagnosis of bone metastases in patients with prostate cancer: a systematic review and meta-analysis

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Abstract

Objective

A systematic review and meta-analysis to compare the diagnostic performance of prostate-specific membrane antigen (PSMA)-PET/CT, choline-PET/CT, Sodium Fluoride (NaF) PET/CT, MRI, and bone scintigraphy (BS) in detecting bone metastases in patients with prostate cancer.

Methods

We searched PubMed and Embase for articles published between January 1990 and September 2018. Two evaluators independently extracted the sensitivity, specificity, the numbers of true and false positives, and true and false negatives. We calculated the pooled sensitivity, specificity, and 95% confidence intervals (CI) for each method. We calculated the tests’ diagnostic odds ratios (DOR); drew the summary receiver operating characteristic (SROC) curves; and obtained the areas under the curves (AUC), Q* values, and 95% CIs.

Results

The per-patient pooled sensitivities of PSMA-PET/CT, choline-PET/CT, NaF-PET/CT, MRI, and BS were 0.97, 0.87, 0.96, 0.91, and 0.86, respectively. The pooled specificities were 1.00, 0.99, 0.97, 0.96, and 0.95, respectively. The pooled DOR values were 504.16, 673.67, 242.63, and 114.44, respectively. The AUC were 1.00, 0.99, 0.99, 0.98, and 0.95, respectively. The per-lesion pooled sensitivities of PSMA-PET/CT, choline-PET/CT, NaF-PET/CT, MRI, and bone imaging were 0.88, 0.80, 0.97, 0.81 and 0.68, respectively.

Conclusions

According to the meta-analysis, PSMA-PET/CT had the highest per-patient sensitivity and specificity in detecting bone metastases with prostate cancer. The sensitivities of NaF-PET/CT and MRI were better than those for choline-PET/CT and BS. The specificity of PSMA-PET/CT was significantly better than BS. Others were similar. For per-lesion, NaF-PET/CT had the highest sensitivity, PSMA-PET/CT had higher sensitivity than choline-PET/CT and MRI, and BS had the lowest sensitivity.

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References

  1. Bray F, Ferlay J, Soerjomataram I, Siegel RL, Torre LA, Jemal A. Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin. 2018;0:3–31.

    Google Scholar 

  2. Bubendorf L, Schöpfer A, Wagner U, et al. Metastatic patterns of prostate cancer: an autopsy study of 1,589 patients. Hum Pathol. 2000;31(5):578–83.

    CAS  PubMed  Google Scholar 

  3. Langsteger W, Rezaee A, Pirich C, Beheshti M. (18)F-NaF-PET/CT and (99m)Tc-MDP bone scintigraphy in the detection of bone metastases in prostate cancer. Semin Nucl Med. 2016;46(6):491–501.

    PubMed  Google Scholar 

  4. Even-Sapir E, Metser U, Mishani E, Lievshitz G, Lerman H, Leibovitch I. The detection of bone metastases in patients with high-risk prostate cancer: 99mTc-MDP planar bone scintigraphy, single- and multi-field-of-view SPECT, 18F-fluoride PET, and 18F-fluoride PET/CT. J Nucl Med. 2006;47:287–97.

    Google Scholar 

  5. Giovanella L, Castellani M, Suriano S, et al. Multi-field-of-view SPECT is superior to whole-body scanning for assessing metastatic bone disease in patients with prostate cancer. Tumori. 2011;97(5):629–33.

    CAS  PubMed  Google Scholar 

  6. Lecouvet FE, El Mouedden J, Collette L, et al. Can whole-body magnetic resonance imaging with diffusion-weighted imaging replace Tc 99m bone scanning and computed tomography for single-step detection of metastases in patients with high-risk prostate cancer? Eur Urol. 2012;62(1):68–75.

    PubMed  Google Scholar 

  7. Lecouvet FE, Geukens D, Stainier A, et al. Magnetic resonance imaging of the axial skeleton for detecting bone metastases in patients with high-risk prostate cancer: diagnostic and cost-effectiveness and comparison with current detection strategies. J Clin Oncol. 2007;25(22):3281–7.

    PubMed  Google Scholar 

  8. Woo S, Kim SY, Kim SH, Cho JY. JOURNAL CLUB: identification of bone metastasis with routine prostate MRI: a study of patients with newly diagnosed prostate cancer. AJR Am J Roentgenol. 2016;206(6):1156–63.

    PubMed  Google Scholar 

  9. Woo S, Suh CH, Kim SY, Cho JY, Kim SH. Diagnostic performance of magnetic resonance imaging for the detection of bone metastasis in prostate cancer: a systematic review and meta-analysis. Eur Urol. 2018;73(1):81–91.

    PubMed  Google Scholar 

  10. Shen G, Deng H, Hu S, Jia Z. Comparison of choline-PET/CT, MRI, SPECT, and bone scintigraphy in the diagnosis of bone metastases in patients with prostate cancer: a meta-analysis. Skelet Radiol. 2014;43(11):1503–13.

    Google Scholar 

  11. Richter JA, Rodriguez M, Rioja J, et al. Dual tracer 11C-choline and FDG-PET in the diagnosis of biochemical prostate cancer relapse after radical treatment. Mol Imaging Biol. 2010;12(2):210–7.

    PubMed  Google Scholar 

  12. Cimitan M, Bortolus R, Morassut S, et al. [18F]fluorocholine PET/CT imaging for the detection of recurrent prostate cancer at PSA relapse: experience in 100 consecutive patients. Eur J Nucl Med Mol Imaging. 2006;33(12):1387–98.

    PubMed  Google Scholar 

  13. Fuccio C, Castellucci P, Schiavina R, et al. Role of 11C-choline PET/CT in the restaging of prostate cancer patients showing a single lesion on bone scintigraphy. Ann Nucl Med. 2010;24(6):485–92.

    CAS  PubMed  Google Scholar 

  14. Picchio M, Spinapolice EG, Fallanca F, et al. [11C]choline PET/CT detection of bone metastases in patients with PSA progression after primary treatment for prostate cancer: comparison with bone scintigraphy. Eur J Nucl Med Mol Imaging. 2012;39(1):13–26.

    CAS  PubMed  Google Scholar 

  15. Corfield J, Perera M, Bolton D, Lawrentschuk N. (68)Ga-prostate specific membrane antigen (PSMA) positron emission tomography (PET) for primary staging of high-risk prostate cancer: a systematic review. World J Urol. 2018;36(4):519–27.

    PubMed  Google Scholar 

  16. Perera M, Papa N, Christidis D, et al. Sensitivity, specificity, and predictors of positive (68)Ga-prostate-specific membrane antigen positron emission tomography in advanced prostate cancer: a systematic review and meta-analysis. Eur Urol. 2016;70(6):926–37.

    PubMed  Google Scholar 

  17. Kitajima K, Fukushima K, Yamamoto S, et al. Diagnostic performance of (11)C-choline PET/CT and bone scintigraphy in the detection of bone metastases in patients with prostate cancer. Nagoya J Med Sci. 2017;79(3):387–99.

    CAS  PubMed  PubMed Central  Google Scholar 

  18. Lengana T, Lawal IO, Boshomane TG, et al. (68)Ga-PSMA PET/CT replacing bone scan in the initial staging of skeletal metastasis in prostate cancer: a fait accompli? Clin Genitourin Cancer. 2018;16(5):392–401.

    PubMed  Google Scholar 

  19. Uprimny C, Svirydenka A, Fritz J, et al. Comparison of [(68)Ga]Ga-PSMA-11 PET/CT with [(18)F]NaF PET/CT in the evaluation of bone metastases in metastatic prostate cancer patients prior to radionuclide therapy. Eur J Nucl Med Mol Imaging. 2018;45(11):1873–83.

    CAS  PubMed  Google Scholar 

  20. Schwenck J, Rempp H, Reischl G, et al. Comparison of (68)Ga-labelled PSMA-11 and (11)C-choline in the detection of prostate cancer metastases by PET/CT. Eur J Nucl Med Mol Imaging. 2017;44(1):92–101.

    CAS  PubMed  Google Scholar 

  21. Janssen JC, Meissner S, Woythal N, et al. Comparison of hybrid (68)Ga-PSMA-PET/CT and (99m)Tc-DPD-SPECT/CT for the detection of bone metastases in prostate cancer patients: additional value of morphologic information from low dose CT. Eur Radiol. 2018;28(2):610–9.

    PubMed  Google Scholar 

  22. Zacho HD, Nielsen JB, Afshar-Oromieh A, et al. Prospective comparison of (68)Ga-PSMA PET/CT, (18)F-sodium fluoride PET/CT and diffusion weighted-MRI at for the detection of bone metastases in biochemically recurrent prostate cancer. Eur J Nucl Med Mol Imaging. 2018;45(11):1884–97.

    CAS  PubMed  Google Scholar 

  23. Wondergem M, van der Zant FM, Knol RJJ, et al. (99m)Tc-HDP bone scintigraphy and (18)F-sodiumfluoride PET/CT in primary staging of patients with prostate cancer. World J Urol. 2018;36(1):27–34.

    PubMed  Google Scholar 

  24. Kawanaka Y, Kitajima KD, Yamamoto S, et al. Comparison of 11C-choline positron emission tomography/computed tomography (PET/CT) and conventional imaging for detection of recurrent prostate cancer. Cureus. 2018;10(7):e2966.

    PubMed  PubMed Central  Google Scholar 

  25. Kitajima K, Murphy RC, Nathan MA, et al. Detection of recurrent prostate cancer after radical prostatectomy: comparison of 11C-choline PET/CT with pelvic multiparametric MR imaging with endorectal coil. J Nucl Med. 2014;55(2):223–32.

    CAS  PubMed  Google Scholar 

  26. Takesh M, Odat Allh K, Adams S, Zechmann C. Diagnostic role of (18)F-FECH-PET/CT compared with bone scan in evaluating the prostate cancer patients referring with biochemical recurrence. ISRN Oncol. 2012;2012:815234.

    PubMed  PubMed Central  Google Scholar 

  27. Fonager RF, Zacho HD, Langkilde NC, et al. Diagnostic test accuracy study of 18F-sodium fluoride PET_CT, 99mTc-labelled diphosphonate SPECT_CT, and planar bone scintigraphy for diagnosis of bone metastases in newly diagnosed, high-risk prostate cancer. Am J Nucl Med Mol Imaging. 2017;7(5):218–27.

    PubMed  PubMed Central  Google Scholar 

  28. Beheshti M, Vali R, Waldenberger P, et al. Detection of bone metastases in patients with prostate cancer by 18F fluorocholine and 18F fluoride PET-CT: a comparative study. Eur J Nucl Med Mol Imaging. 2008;35(10):1766–74.

    PubMed  Google Scholar 

  29. Venkitaraman R, Cook GJ, Dearnaley DP, et al. Does magnetic resonance imaging of the spine have a role in the staging of prostate cancer? Clin Oncol (R Coll Radiol). 2009;21(1):39–42.

    CAS  Google Scholar 

  30. Huysse W, Lecouvet F, Castellucci P, et al. Prospective comparison of F-18 choline PET/CT scan versus axial MRI for detecting bone metastasis in biochemically relapsed prostate cancer patients. Diagnostics (Basel). 2017;7:56.

    Google Scholar 

  31. Poulsen MH, Petersen H, Hoilund-Carlsen PF, et al. Spine metastases in prostate cancer: comparison of technetium-99m-MDP whole-body bone scintigraphy, [(18) F]choline positron emission tomography(PET)/computed tomography (CT) and [(18) F]NaF PET/CT. BJU Int. 2014;114(6):818–23.

    CAS  PubMed  Google Scholar 

  32. Mosavi F, Johansson S, Sandberg DT, Turesson I, Sörensen J, Ahlström H. Whole-body diffusion-weighted MRI compared with 18F-NaF PET/CT for detection of bone metastases in patients with high-risk prostate carcinoma. Am J Roentgenol. 2012;199(5):1114–20.

    Google Scholar 

  33. Venkitaraman R, Cook GJR, Dearnaley DP, et al. Whole-body magnetic resonance imaging in the detection of skeletal metastases in patients with prostate cancer. J Med Imaging Radiat Oncol. 2009;53:241–7.

    CAS  PubMed  Google Scholar 

  34. Wieder H, Maurer T, Beer AJ, et al. 11C-choline PET_CT and whole-body MRI including diffusion-weighted imaging for patients with recurrent prostate cancer. Oncotarget. 2017;8(39):66516–27.

    PubMed  PubMed Central  Google Scholar 

  35. Dyrberg E, Hendel HW, Huynh THV, et al. (68)Ga-PSMA-PET/CT in comparison with (18)F-fluoride-PET/CT and whole-body MRI for the detection of bone metastases in patients with prostate cancer: a prospective diagnostic accuracy study. Eur Radiol. 2018. https://doi.org/10.1007/s00330-018-5682-x.

    PubMed  Google Scholar 

  36. Nozaki T, Yasuda K, Akashi T, Fuse H. Usefulness of single photon emission computed tomography imaging in the detection of lumbar vertebral metastases from prostate cancer. Int J Urol. 2008;15(6):516–9.

    PubMed  Google Scholar 

  37. Lecouvet FE, Simon M, Tombal B, Jamart J, Vande Berg BC, Simoni P. Whole-body MRI (WB-MRI) versus axial skeleton MRI (AS-MRI) to detect and measure bone metastases in prostate cancer (PCa). Eur Radiol. 2010;20(12):2973–82.

    CAS  PubMed  Google Scholar 

  38. Harmon SA, Perk T, Lin C, et al. Quantitative assessment of early [18F]sodium fluoride positron emission tomography/computed tomography response to treatment in men with metastatic prostate cancer to bone. J Clin Oncol. 2017;35:24.

    Google Scholar 

  39. Beheshti M, Mottaghy FM, Paycha F, et al. 18F-NaF PET/CT: EANM procedure guidelines for bone imaging. Eur J Nucl Med Mol Imaging. 2015;42(11):1767–77.

    CAS  PubMed  Google Scholar 

  40. Ceci F, Herrmann K, Castellucci P, et al. 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. 2014;41(12):2222–31.

    PubMed  Google Scholar 

  41. Ceci F, Castellucci P, Graziani T, et al. 11C-choline PET/CT detects the site of relapse in the majority of prostate cancer patients showing biochemical recurrence after EBRT. Eur J Nucl Med Mol Imaging. 2014;41(5):878–86.

    CAS  PubMed  Google Scholar 

  42. Ceci F, Castellucci P, Mamede M, et al. 11C-choline PET/CT in patients with hormone-resistant prostate cancer showing biochemical relapse after radical prostatectomy. Eur J Nucl Med Mol Imaging. 2013;40(2):149–55.

    CAS  PubMed  Google Scholar 

  43. Dyrberg E, Larsen EL, Hendel HW, Thomsen HS. Diagnostic bone imaging in patients with prostate cancer: patient experience and acceptance of NaF-PET/CT, choline-PET/CT, whole-body MRI, and bone SPECT/CT. Acta Radiol. 2018;59(9):1119–25.

    PubMed  Google Scholar 

  44. Afshar-Oromieh A, Zechmann CM, Malcher A, et al. Comparison of PET imaging with a 68Ga-labelled PSMA ligand and 18F-choline-based PET/CT for the diagnosis of recurrent prostate cancer. Eur J Nucl Med Mol Imaging. 2014;41:11–20.

    CAS  PubMed  Google Scholar 

  45. Afshar-Oromieh A, Haberkorn U, Schlemmer H, et al. Comparison of PET/CTand PET/MRI hybrid systems using a 68Ga-labelled PSMA ligand for the diagnosis of recurrent prostate cancer: initial experience. Eur J Nucl Med Mol Imaging. 2013. https://doi.org/10.1007/s00259-013-2660-z.

    PubMed  Google Scholar 

  46. Freitag MT, Radtke JP, Hadaschik BA, et al. Comparison of hybrid (68)Ga-PSMA PET/MRI and (68)Ga-PSMA PET/CT in the evaluation of lymph node and bone metastases of prostate cancer. Eur J Nucl Med Mol Imaging. 2016;43(1):70–83.

    CAS  PubMed  Google Scholar 

  47. Afshar-Oromieh A, Avtzi E, Giesel FL, et al. The diagnostic value of PET/CT imaging with the 68Ga-labelled PSMA ligand HBED-CC in the diagnosis of recurrent prostate cancer. Eur J Nucl Med Mol Imaging. 2014. https://doi.org/10.1007/s00259-014-2949-6.

    PubMed  PubMed Central  Google Scholar 

  48. Morigi JJ, Stricker PD, van Leeuwen PJ, et al. 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. 2015;56(8):1185–90.

    CAS  PubMed  Google Scholar 

  49. Pyka T, Okamoto S, Dahlbender M, et al. Comparison of bone scintigraphy and (68)Ga-PSMA PET for skeletal staging in prostate cancer. Eur J Nucl Med Mol Imaging. 2016;43(12):2114–21.

    CAS  PubMed  Google Scholar 

  50. Iagaru A, Mittra E, Dick DW, Gambhir SS. Prospective evaluation of (99m)Tc MDP scintigraphy, (18)F NaF PET/CT, and (18)F FDG PET/CT for detection of skeletal metastases. Mol Imaging Biol. 2012;14(2):252–9.

    PubMed  Google Scholar 

  51. Apolo AB, Lindenberg L, Shih JH, et al. Prospective study evaluating Na18F PET/CT in predicting clinical outcomes and survival in advanced prostate cancer. J Nucl Med. 2016;57(6):886–92.

    CAS  PubMed  PubMed Central  Google Scholar 

  52. Jambor I, Kuisma A, Ramadan S, et al. Prospective evaluation of planar bone scintigraphy, SPECT, SPECT/CT, 18F-NaF PET/CT and whole body 1.5T MRI, including DWI, for the detection of bone metastases in high risk breast and prostate cancer patients: SKELETA clinical trial. Acta Oncol. 2016;55(1):59–67.

    PubMed  Google Scholar 

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Correspondence to Zhengxing Gou.

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The scientific guarantor of this publication is Jing Zhou.

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Zhou, J., Gou, Z., Wu, R. et al. Comparison of PSMA-PET/CT, choline-PET/CT, NaF-PET/CT, MRI, and bone scintigraphy in the diagnosis of bone metastases in patients with prostate cancer: a systematic review and meta-analysis. Skeletal Radiol 48, 1915–1924 (2019). https://doi.org/10.1007/s00256-019-03230-z

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