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Published in: EJNMMI Research 1/2021

Open Access 01-12-2021 | Prostate Cancer | Original research

Potential synergy between PSMA uptake and tumour blood flow for prediction of human prostate cancer aggressiveness

Authors: Mads Ryø Jochumsen, Jens Sörensen, Lars Poulsen Tolbod, Bodil Ginnerup Pedersen, Jørgen Frøkiær, Michael Borre, Kirsten Bouchelouche

Published in: EJNMMI Research | Issue 1/2021

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Abstract

Background

Both prostate-specific membrane antigen (PSMA) uptake and tumour blood flow (TBF) correlate with International Society of Urological Pathology (ISUP) Grade Group (GG) and hence prostate cancer (PCa) aggressiveness. The aim of the present study was to evaluate the potential synergistic benefit of combining the two physiologic parameters for separating significant PCa from insignificant findings.

Methods

From previous studies of [82Rb]Rb positron emission tomography (PET) TBF in PCa, the 43 patients that underwent clinical [68Ga]Ga-PSMA-11 PET were selected for this retrospective study. Tumours were delineated on [68Ga]Ga-PSMA-11 PET or magnetic resonance imaging. ISUP GG was recorded from 52 lesions.

Results

[68Ga]Ga-PSMA-11 maximum standardized uptake value (SUVmax) and [82Rb]Rb SUVmax correlated moderately with ISUP GG (rho = 0.59 and rho = 0.56, both p < 0.001) and with each other (r = 0.65, p < 0.001). A combined model of [68Ga]Ga-PSMA-11 and [82Rb]Rb SUVmax separated ISUP GG > 2 from ISUP GG 1–2 and benign with an area-under-the-curve of 0.85, 96% sensitivity, 74% specificity, and 95% negative predictive value. The combined model performed significantly better than either tracer alone did (p < 0.001), primarily by reducing false negatives from five or six to one (p ≤ 0.025).

Conclusion

PSMA uptake and TBF provide complementary information about tumour aggressiveness. We suggest that a combined analysis of PSMA uptake and TBF could significantly improve the negative predictive value and allow non-invasive separation of significant from insignificant PCa.
Literature
1.
go back to reference Attard G, Parker C, Eeles RA, Schroder F, Tomlins SA, Tannock I, et al. Prostate cancer. Lancet (London, England). 2016;387(10013):70–82.CrossRef Attard G, Parker C, Eeles RA, Schroder F, Tomlins SA, Tannock I, et al. Prostate cancer. Lancet (London, England). 2016;387(10013):70–82.CrossRef
2.
go back to reference Hanahan D, Weinberg RA. Hallmarks of cancer: the next generation. Cell. 2011;144(5):646–74.CrossRef Hanahan D, Weinberg RA. Hallmarks of cancer: the next generation. Cell. 2011;144(5):646–74.CrossRef
3.
go back to reference Johnson GB, Harms HJ, Johnson DR, Jacobson MS. PET Imaging of Tumor Perfusion: A Potential Cancer Biomarker? Semin Nucl Med. 2020;50(6):549–61.CrossRef Johnson GB, Harms HJ, Johnson DR, Jacobson MS. PET Imaging of Tumor Perfusion: A Potential Cancer Biomarker? Semin Nucl Med. 2020;50(6):549–61.CrossRef
4.
go back to reference Hofman MS, Lawrentschuk N, Francis RJ, Tang C, Vela I, Thomas P, et al. Prostate-specific membrane antigen PET-CT in patients with high-risk prostate cancer before curative-intent surgery or radiotherapy (proPSMA): a prospective, randomised, multicentre study. The Lancet. 2020;395(10231):1208–16.CrossRef Hofman MS, Lawrentschuk N, Francis RJ, Tang C, Vela I, Thomas P, et al. Prostate-specific membrane antigen PET-CT in patients with high-risk prostate cancer before curative-intent surgery or radiotherapy (proPSMA): a prospective, randomised, multicentre study. The Lancet. 2020;395(10231):1208–16.CrossRef
5.
go back to reference Ferdinandus J, Fendler WP, Hadaschik B, Herrmann K. Prostate-specific membrane antigen targeted PET imaging for prostate cancer recurrence. Curr Opin Urol. 2020;30(5):635–40.PubMed Ferdinandus J, Fendler WP, Hadaschik B, Herrmann K. Prostate-specific membrane antigen targeted PET imaging for prostate cancer recurrence. Curr Opin Urol. 2020;30(5):635–40.PubMed
6.
go back to reference Demirci E, Kabasakal L, Sahin OE, Akgun E, Gultekin MH, Doganca T, et al. Can SUVmax values ofGa-68-PSMA PET/CT scan predict the clinically significant prostate cancer? Nucl Med Commun. 2019;40(1):86–91.CrossRef Demirci E, Kabasakal L, Sahin OE, Akgun E, Gultekin MH, Doganca T, et al. Can SUVmax values ofGa-68-PSMA PET/CT scan predict the clinically significant prostate cancer? Nucl Med Commun. 2019;40(1):86–91.CrossRef
7.
go back to reference Uprimny C, Kroiss AS, Decristoforo C, Fritz J, von Guggenberg E, Kendler D, et al. (68)Ga-PSMA-11 PET/CT in primary staging of prostate cancer: PSA and Gleason score predict the intensity of tracer accumulation in the primary tumour. Eur J Nucl Med Mol Imaging. 2017;44(6):941–9.CrossRef Uprimny C, Kroiss AS, Decristoforo C, Fritz J, von Guggenberg E, Kendler D, et al. (68)Ga-PSMA-11 PET/CT in primary staging of prostate cancer: PSA and Gleason score predict the intensity of tracer accumulation in the primary tumour. Eur J Nucl Med Mol Imaging. 2017;44(6):941–9.CrossRef
8.
go back to reference Chen M, Qiu X, Zhang Q, Zhang C, Zhou Y, Zhao X, et al. PSMA uptake on [68Ga]-PSMA-11-PET/CT positively corrects with prostate cancer aggressiveness. The quarterly journal of nuclear medicine and molecular imaging : official publication of the Italian Association of Nuclear Medicine (AIMN) [and] the International Association of Radiopharmacology (IAR), [and] Section of the So. 2019. Chen M, Qiu X, Zhang Q, Zhang C, Zhou Y, Zhao X, et al. PSMA uptake on [68Ga]-PSMA-11-PET/CT positively corrects with prostate cancer aggressiveness. The quarterly journal of nuclear medicine and molecular imaging : official publication of the Italian Association of Nuclear Medicine (AIMN) [and] the International Association of Radiopharmacology (IAR), [and] Section of the So. 2019.
9.
go back to reference Cytawa W, Seitz AK, Kircher S, Fukushima K, Tran-Gia J, Schirbel A, et al. (68)Ga-PSMA I&T PET/CT for primary staging of prostate cancer. Eur J Nucl Med Mol Imaging. 2020;47(1):168–77.CrossRef Cytawa W, Seitz AK, Kircher S, Fukushima K, Tran-Gia J, Schirbel A, et al. (68)Ga-PSMA I&T PET/CT for primary staging of prostate cancer. Eur J Nucl Med Mol Imaging. 2020;47(1):168–77.CrossRef
10.
go back to reference Klingenberg S, Jochumsen MR, Ulhøi BP, Fredsøe J, Sørensen KD, Borre M, et al. (68)Ga-PSMA PET/CT for primary NM staging of high-risk prostate cancer. Journal of nuclear medicine : official publication, Society of Nuclear Medicine. 2020. Klingenberg S, Jochumsen MR, Ulhøi BP, Fredsøe J, Sørensen KD, Borre M, et al. (68)Ga-PSMA PET/CT for primary NM staging of high-risk prostate cancer. Journal of nuclear medicine : official publication, Society of Nuclear Medicine. 2020.
11.
go back to reference Zhou J, Neale JH, Pomper MG, Kozikowski AP. NAAG peptidase inhibitors and their potential for diagnosis and therapy. Nat Rev Drug Discovery. 2005;4(12):1015–26.CrossRef Zhou J, Neale JH, Pomper MG, Kozikowski AP. NAAG peptidase inhibitors and their potential for diagnosis and therapy. Nat Rev Drug Discovery. 2005;4(12):1015–26.CrossRef
12.
go back to reference Yao V, Bacich DJ. Prostate specific membrane antigen (PSMA) expression gives prostate cancer cells a growth advantage in a physiologically relevant folate environment in vitro. 2006;66(8):867–75. Yao V, Bacich DJ. Prostate specific membrane antigen (PSMA) expression gives prostate cancer cells a growth advantage in a physiologically relevant folate environment in vitro. 2006;66(8):867–75.
13.
go back to reference Yao V, Berkman CE, Choi JK, O'Keefe DS, Bacich DJ. Expression of prostate-specific membrane antigen (PSMA), increases cell folate uptake and proliferation and suggests a novel role for PSMA in the uptake of the non-polyglutamated folate, folic acid. 2009:n/a-n/a. Yao V, Berkman CE, Choi JK, O'Keefe DS, Bacich DJ. Expression of prostate-specific membrane antigen (PSMA), increases cell folate uptake and proliferation and suggests a novel role for PSMA in the uptake of the non-polyglutamated folate, folic acid. 2009:n/a-n/a.
14.
go back to reference Ghosh A, Wang X, Klein E, Heston WD. Novel role of prostate-specific membrane antigen in suppressing prostate cancer invasiveness. Can Res. 2005;65(3):727–31. Ghosh A, Wang X, Klein E, Heston WD. Novel role of prostate-specific membrane antigen in suppressing prostate cancer invasiveness. Can Res. 2005;65(3):727–31.
15.
go back to reference Kurdziel KA, Figg WD, Carrasquillo JA, Huebsch S, Whatley M, Sellers D, et al. Using positron emission tomography 2-deoxy-2-[18F]fluoro-D-glucose, 11CO, and 15O-water for monitoring androgen independent prostate cancer. MIB. 2003;5(2):86–93.PubMed Kurdziel KA, Figg WD, Carrasquillo JA, Huebsch S, Whatley M, Sellers D, et al. Using positron emission tomography 2-deoxy-2-[18F]fluoro-D-glucose, 11CO, and 15O-water for monitoring androgen independent prostate cancer. MIB. 2003;5(2):86–93.PubMed
16.
go back to reference Inaba T. Quantitative measurements of prostatic blood flow and blood volume by positron emission tomography. J Urol. 1992;148(5):1457–60.CrossRef Inaba T. Quantitative measurements of prostatic blood flow and blood volume by positron emission tomography. J Urol. 1992;148(5):1457–60.CrossRef
17.
go back to reference Tolbod LP, Nielsen MM, Pedersen BG, Hoyer S, Harms HJ, Borre M, et al. Non-invasive quantification of tumor blood flow in prostate cancer using (15)O-H2O PET/CT. Am J Nucl Med Mol Imaging. 2018;8(5):292–302.PubMedPubMedCentral Tolbod LP, Nielsen MM, Pedersen BG, Hoyer S, Harms HJ, Borre M, et al. Non-invasive quantification of tumor blood flow in prostate cancer using (15)O-H2O PET/CT. Am J Nucl Med Mol Imaging. 2018;8(5):292–302.PubMedPubMedCentral
18.
go back to reference de Langen AJ, van den Boogaart V, Lubberink M, Backes WH, Marcus JT, van Tinteren H, et al. Monitoring response to antiangiogenic therapy in non-small cell lung cancer using imaging markers derived from PET and dynamic contrast-enhanced MRI. J Nucl Med. 2011;52(1):48–55.CrossRef de Langen AJ, van den Boogaart V, Lubberink M, Backes WH, Marcus JT, van Tinteren H, et al. Monitoring response to antiangiogenic therapy in non-small cell lung cancer using imaging markers derived from PET and dynamic contrast-enhanced MRI. J Nucl Med. 2011;52(1):48–55.CrossRef
19.
go back to reference Scott AM, Mitchell PL, O’Keefe G, Saunder T, Hicks RJ, Poon A, et al. Pharmacodynamic analysis of tumour perfusion assessed by 15O-water-PET imaging during treatment with sunitinib malate in patients with advanced malignancies. EJNMMI Res. 2012;2(1):31.CrossRef Scott AM, Mitchell PL, O’Keefe G, Saunder T, Hicks RJ, Poon A, et al. Pharmacodynamic analysis of tumour perfusion assessed by 15O-water-PET imaging during treatment with sunitinib malate in patients with advanced malignancies. EJNMMI Res. 2012;2(1):31.CrossRef
20.
go back to reference Krak N, van der Hoeven J, Hoekstra O, Twisk J, van der Wall E, Lammertsma A. Blood flow and glucose metabolism in stage IV breast cancer: heterogeneity of response during chemotherapy. MIB. 2008;10(6):356–63.PubMed Krak N, van der Hoeven J, Hoekstra O, Twisk J, van der Wall E, Lammertsma A. Blood flow and glucose metabolism in stage IV breast cancer: heterogeneity of response during chemotherapy. MIB. 2008;10(6):356–63.PubMed
21.
go back to reference Mankoff DA, Dunnwald LK, Gralow JR, Ellis GK, Schubert EK, Tseng J, et al. Changes in blood flow and metabolism in locally advanced breast cancer treated with neoadjuvant chemotherapy. J Nucl Med . 2003;44(11):1806–14.PubMed Mankoff DA, Dunnwald LK, Gralow JR, Ellis GK, Schubert EK, Tseng J, et al. Changes in blood flow and metabolism in locally advanced breast cancer treated with neoadjuvant chemotherapy. J Nucl Med . 2003;44(11):1806–14.PubMed
22.
go back to reference Specht JM, Kurland BF, Montgomery SK, Dunnwald LK, Doot RK, Gralow JR, et al. Tumor metabolism and blood flow as assessed by positron emission tomography varies by tumor subtype in locally advanced breast cancer. Clin Cancer Res. 2010;16(10):2803–10.CrossRef Specht JM, Kurland BF, Montgomery SK, Dunnwald LK, Doot RK, Gralow JR, et al. Tumor metabolism and blood flow as assessed by positron emission tomography varies by tumor subtype in locally advanced breast cancer. Clin Cancer Res. 2010;16(10):2803–10.CrossRef
23.
go back to reference Dunnwald LK, Gralow JR, Ellis GK, Livingston RB, Linden HM, Specht JM, et al. Tumor metabolism and blood flow changes by positron emission tomography: relation to survival in patients treated with neoadjuvant chemotherapy for locally advanced breast cancer. J Clin Oncol. 2008;26(27):4449–57.CrossRef Dunnwald LK, Gralow JR, Ellis GK, Livingston RB, Linden HM, Specht JM, et al. Tumor metabolism and blood flow changes by positron emission tomography: relation to survival in patients treated with neoadjuvant chemotherapy for locally advanced breast cancer. J Clin Oncol. 2008;26(27):4449–57.CrossRef
24.
go back to reference Lehtio K, Oikonen V, Gronroos T, Eskola O, Kalliokoski K, Bergman J, et al. Imaging of blood flow and hypoxia in head and neck cancer: initial evaluation with [(15)O]H(2)O and [(18)F]fluoroerythronitroimidazole PET. J Nucl Med. 2001;42(11):1643–52.PubMed Lehtio K, Oikonen V, Gronroos T, Eskola O, Kalliokoski K, Bergman J, et al. Imaging of blood flow and hypoxia in head and neck cancer: initial evaluation with [(15)O]H(2)O and [(18)F]fluoroerythronitroimidazole PET. J Nucl Med. 2001;42(11):1643–52.PubMed
25.
go back to reference Lubberink M, Golla SS, Jonasson M, Rubin K, Glimelius B, Sorensen J, et al. (15)O-Water PET Study of the Effect of Imatinib, a Selective Platelet-Derived Growth Factor Receptor Inhibitor, Versus Anakinra, an IL-1R Antagonist, on Water-Perfusable Tissue Fraction in Colorectal Cancer Metastases. J Nucl Med. 2015;56(8):1144–9.CrossRef Lubberink M, Golla SS, Jonasson M, Rubin K, Glimelius B, Sorensen J, et al. (15)O-Water PET Study of the Effect of Imatinib, a Selective Platelet-Derived Growth Factor Receptor Inhibitor, Versus Anakinra, an IL-1R Antagonist, on Water-Perfusable Tissue Fraction in Colorectal Cancer Metastases. J Nucl Med. 2015;56(8):1144–9.CrossRef
26.
go back to reference Bruehlmeier M, Roelcke U, Schubiger PA, Ametamey SM. Assessment of hypoxia and perfusion in human brain tumors using PET with 18F-fluoromisonidazole and 15O–H2O. J Nucl Med. 2004;45(11):1851–9.PubMed Bruehlmeier M, Roelcke U, Schubiger PA, Ametamey SM. Assessment of hypoxia and perfusion in human brain tumors using PET with 18F-fluoromisonidazole and 15O–H2O. J Nucl Med. 2004;45(11):1851–9.PubMed
27.
go back to reference Hasbak P, Enevoldsen LH, Fosbøl MØ, Skovgaard D, Knigge UP, Kjær A. Rubidium-82 uptake in metastases from neuroendocrine tumors: No flow response to adenosine. J Nucl Cardiol. 2016;23(4):840–2.CrossRef Hasbak P, Enevoldsen LH, Fosbøl MØ, Skovgaard D, Knigge UP, Kjær A. Rubidium-82 uptake in metastases from neuroendocrine tumors: No flow response to adenosine. J Nucl Cardiol. 2016;23(4):840–2.CrossRef
28.
go back to reference Lu Y. FDG and (82)Rb PET/MRI features of brain metastasis of breast cancer. Clin Nucl Med. 2015;40(6):494–5.CrossRef Lu Y. FDG and (82)Rb PET/MRI features of brain metastasis of breast cancer. Clin Nucl Med. 2015;40(6):494–5.CrossRef
29.
go back to reference Mirpour S, Khandani AH. Extracardiac abnormalities on rubidium-82 cardiac positron emission tomography/computed tomography. Nucl Med Commun. 2011;32(4):260–4.CrossRef Mirpour S, Khandani AH. Extracardiac abnormalities on rubidium-82 cardiac positron emission tomography/computed tomography. Nucl Med Commun. 2011;32(4):260–4.CrossRef
30.
go back to reference Murthy VL, Brown RK, Corbett JR. Metastatic renal cell carcinoma avid for 82Rb but not 18F-FDG. Clin Nucl Med. 2014;39(10):908–9.CrossRef Murthy VL, Brown RK, Corbett JR. Metastatic renal cell carcinoma avid for 82Rb but not 18F-FDG. Clin Nucl Med. 2014;39(10):908–9.CrossRef
31.
go back to reference Jochumsen MR, Tolbod LP, Pedersen BG, Nielsen MM, Hoyer S, Frokiaer J, et al. Quantitative tumor perfusion imaging with (82)Rb PET/CT in prostate cancer: analytic and clinical validation. J Nucl Med. 2019;60(8):1059–65.CrossRef Jochumsen MR, Tolbod LP, Pedersen BG, Nielsen MM, Hoyer S, Frokiaer J, et al. Quantitative tumor perfusion imaging with (82)Rb PET/CT in prostate cancer: analytic and clinical validation. J Nucl Med. 2019;60(8):1059–65.CrossRef
32.
go back to reference Jochumsen MR, Bouchelouche K, Nielsen KB, Frokiaer J, Borre M, Sorensen J, et al. Repeatability of tumor blood flow quantification with (82)Rubidium PET/CT in prostate cancer - a test-retest study. EJNMMI research. 2019;9(1):58.CrossRef Jochumsen MR, Bouchelouche K, Nielsen KB, Frokiaer J, Borre M, Sorensen J, et al. Repeatability of tumor blood flow quantification with (82)Rubidium PET/CT in prostate cancer - a test-retest study. EJNMMI research. 2019;9(1):58.CrossRef
33.
go back to reference Jochumsen MR, Sörensen J, Pedersen BG, Nyengaard JR, Krag SRP, Frøkiær J, et al. Tumour blood flow for prediction of human prostate cancer aggressiveness: a study with Rubidium-82 PET, MRI and Na(+)/K(+)-ATPase-density. Eur J Nucl Med Mol Imaging. 2020. Jochumsen MR, Sörensen J, Pedersen BG, Nyengaard JR, Krag SRP, Frøkiær J, et al. Tumour blood flow for prediction of human prostate cancer aggressiveness: a study with Rubidium-82 PET, MRI and Na(+)/K(+)-ATPase-density. Eur J Nucl Med Mol Imaging. 2020.
34.
go back to reference Turkbey B, Rosenkrantz AB, Haider MA, Padhani AR, Villeirs G, Macura KJ, et al. Prostate Imaging Reporting and Data System Version 2.1: 2019 Update of Prostate Imaging Reporting and Data System Version 2. European urology. 2019;76(3):340–51. Turkbey B, Rosenkrantz AB, Haider MA, Padhani AR, Villeirs G, Macura KJ, et al. Prostate Imaging Reporting and Data System Version 2.1: 2019 Update of Prostate Imaging Reporting and Data System Version 2. European urology. 2019;76(3):340–51.
35.
go back to reference Harris PA, Taylor R, Thielke R, Payne J, Gonzalez N, Conde JG. Research electronic data capture (REDCap)–a metadata-driven methodology and workflow process for providing translational research informatics support. J Biomed Inform. 2009;42(2):377–81.CrossRef Harris PA, Taylor R, Thielke R, Payne J, Gonzalez N, Conde JG. Research electronic data capture (REDCap)–a metadata-driven methodology and workflow process for providing translational research informatics support. J Biomed Inform. 2009;42(2):377–81.CrossRef
36.
go back to reference Zamboglou C, Drendel V, Jilg CA, Rischke HC, Beck TI, Schultze-Seemann W, et al. Comparison of (68)Ga-HBED-CC PSMA-PET/CT and multiparametric MRI for gross tumour volume detection in patients with primary prostate cancer based on slice by slice comparison with histopathology. Theranostics. 2017;7(1):228–37.CrossRef Zamboglou C, Drendel V, Jilg CA, Rischke HC, Beck TI, Schultze-Seemann W, et al. Comparison of (68)Ga-HBED-CC PSMA-PET/CT and multiparametric MRI for gross tumour volume detection in patients with primary prostate cancer based on slice by slice comparison with histopathology. Theranostics. 2017;7(1):228–37.CrossRef
37.
go back to reference Donato P, Morton A, Yaxley J, Ranasinghe S, Teloken PE, Kyle S, et al. (68)Ga-PSMA PET/CT better characterises localised prostate cancer after MRI and transperineal prostate biopsy: Is (68)Ga-PSMA PET/CT guided biopsy the future? Eur J Nucl Med Mol Imaging. 2020;47(8):1843–51.CrossRef Donato P, Morton A, Yaxley J, Ranasinghe S, Teloken PE, Kyle S, et al. (68)Ga-PSMA PET/CT better characterises localised prostate cancer after MRI and transperineal prostate biopsy: Is (68)Ga-PSMA PET/CT guided biopsy the future? Eur J Nucl Med Mol Imaging. 2020;47(8):1843–51.CrossRef
38.
go back to reference Cristel G, Esposito A, Damascelli A, Briganti A, Ambrosi A, Brembilla G, et al. Can DCE-MRI reduce the number of PI-RADS vol 2 false positive findings? Role of quantitative pharmacokinetic parameters in prostate lesions characterization. Eur J Radiol. 2019;118:51–7.CrossRef Cristel G, Esposito A, Damascelli A, Briganti A, Ambrosi A, Brembilla G, et al. Can DCE-MRI reduce the number of PI-RADS vol 2 false positive findings? Role of quantitative pharmacokinetic parameters in prostate lesions characterization. Eur J Radiol. 2019;118:51–7.CrossRef
39.
go back to reference Vos EK, Litjens GJ, Kobus T, Hambrock T, Hulsbergen-van de Kaa CA, Barentsz JO, et al. Assessment of prostate cancer aggressiveness using dynamic contrast-enhanced magnetic resonance imaging at 3 T. European urology. 2013;64(3):448–55. Vos EK, Litjens GJ, Kobus T, Hambrock T, Hulsbergen-van de Kaa CA, Barentsz JO, et al. Assessment of prostate cancer aggressiveness using dynamic contrast-enhanced magnetic resonance imaging at 3 T. European urology. 2013;64(3):448–55.
40.
go back to reference Hotker AM, Mazaheri Y, Aras O, Zheng J, Moskowitz CS, Gondo T, et al. Assessment of prostate cancer aggressiveness by use of the combination of quantitative DWI and dynamic contrast-enhanced MRI. AJR Am J Roentgenol. 2016;206(4):756–63.CrossRef Hotker AM, Mazaheri Y, Aras O, Zheng J, Moskowitz CS, Gondo T, et al. Assessment of prostate cancer aggressiveness by use of the combination of quantitative DWI and dynamic contrast-enhanced MRI. AJR Am J Roentgenol. 2016;206(4):756–63.CrossRef
41.
go back to reference Chen YJ, Chu WC, Pu YS, Chueh SC, Shun CT, Tseng WY. Washout gradient in dynamic contrast-enhanced MRI is associated with tumor aggressiveness of prostate cancer. J Magn Reson Imaging. 2012;36(4):912–9.CrossRef Chen YJ, Chu WC, Pu YS, Chueh SC, Shun CT, Tseng WY. Washout gradient in dynamic contrast-enhanced MRI is associated with tumor aggressiveness of prostate cancer. J Magn Reson Imaging. 2012;36(4):912–9.CrossRef
42.
go back to reference Stabile A, Giganti F, Kasivisvanathan V, Giannarini G, Moore CM, Padhani AR, et al. Factors Influencing Variability in the Performance of Multiparametric Magnetic Resonance Imaging in Detecting Clinically Significant Prostate Cancer: A Systematic Literature Review. European Urology Oncology. 2020. Stabile A, Giganti F, Kasivisvanathan V, Giannarini G, Moore CM, Padhani AR, et al. Factors Influencing Variability in the Performance of Multiparametric Magnetic Resonance Imaging in Detecting Clinically Significant Prostate Cancer: A Systematic Literature Review. European Urology Oncology. 2020.
43.
go back to reference Apostolova I, Hofheinz F, Buchert R, Steffen IG, Michel R, Rosner C, et al. Combined measurement of tumor perfusion and glucose metabolism for improved tumor characterization in advanced cervical carcinoma. A PET/CT pilot study using [15O]water and [18F]fluorodeoxyglucose. Strahlentherapie und Onkologie : Organ der Deutschen Rontgengesellschaft [et al]. 2014;190(6):575–81. Apostolova I, Hofheinz F, Buchert R, Steffen IG, Michel R, Rosner C, et al. Combined measurement of tumor perfusion and glucose metabolism for improved tumor characterization in advanced cervical carcinoma. A PET/CT pilot study using [15O]water and [18F]fluorodeoxyglucose. Strahlentherapie und Onkologie : Organ der Deutschen Rontgengesellschaft [et al]. 2014;190(6):575–81.
44.
go back to reference Komar G, Kauhanen S, Liukko K, Seppänen M, Kajander S, Ovaska J, et al. Decreased blood flow with increased metabolic activity: a novel sign of pancreatic tumor aggressiveness. Clin Cancer Res. 2009;15(17):5511–7.CrossRef Komar G, Kauhanen S, Liukko K, Seppänen M, Kajander S, Ovaska J, et al. Decreased blood flow with increased metabolic activity: a novel sign of pancreatic tumor aggressiveness. Clin Cancer Res. 2009;15(17):5511–7.CrossRef
45.
go back to reference Mankoff DA, Dunnwald LK, Gralow JR, Ellis GK, Charlop A, Lawton TJ, et al. Blood flow and metabolism in locally advanced breast cancer: relationship to response to therapy. J Nucl Med. 2002;43(4):500–9.PubMed Mankoff DA, Dunnwald LK, Gralow JR, Ellis GK, Charlop A, Lawton TJ, et al. Blood flow and metabolism in locally advanced breast cancer: relationship to response to therapy. J Nucl Med. 2002;43(4):500–9.PubMed
46.
go back to reference Zhao K, Wang C, Mao Q, Shang D, Huang Y, Ma L, et al. The flow-metabolism ratio might predict treatment response and survival in patients with locally advanced esophageal squamous cell carcinoma. EJNMMI Res. 2020;10(1):57.CrossRef Zhao K, Wang C, Mao Q, Shang D, Huang Y, Ma L, et al. The flow-metabolism ratio might predict treatment response and survival in patients with locally advanced esophageal squamous cell carcinoma. EJNMMI Res. 2020;10(1):57.CrossRef
47.
go back to reference Paschalis A, Sheehan B, Riisnaes R, Rodrigues DN, Gurel B, Bertan C, et al. Prostate-specific membrane antigen heterogeneity and DNA repair defects in prostate cancer. Eur Urol. 2019;76(4):469–78.CrossRef Paschalis A, Sheehan B, Riisnaes R, Rodrigues DN, Gurel B, Bertan C, et al. Prostate-specific membrane antigen heterogeneity and DNA repair defects in prostate cancer. Eur Urol. 2019;76(4):469–78.CrossRef
48.
go back to reference Palard-Novello X, Blin AL, Bourhis D, rin E, Salaun PY, Devillers A, et al. Comparison of choline influx from dynamic (18)F-Choline PET/CT and clinicopathological parameters in prostate cancer initial assessment. Ann Nucl Med. 2018;32(4):281–7.CrossRef Palard-Novello X, Blin AL, Bourhis D, rin E, Salaun PY, Devillers A, et al. Comparison of choline influx from dynamic (18)F-Choline PET/CT and clinicopathological parameters in prostate cancer initial assessment. Ann Nucl Med. 2018;32(4):281–7.CrossRef
49.
go back to reference Schaefferkoetter JD, Wang Z, Stephenson MC, Roy S, Conti M, Eriksson L, et al. Quantitative 18F-fluorocholine positron emission tomography for prostate cancer: correlation between kinetic parameters and Gleason scoring. EJNMMI research. 2017;7(1). Schaefferkoetter JD, Wang Z, Stephenson MC, Roy S, Conti M, Eriksson L, et al. Quantitative 18F-fluorocholine positron emission tomography for prostate cancer: correlation between kinetic parameters and Gleason scoring. EJNMMI research. 2017;7(1).
50.
go back to reference Nielsen MM, Tolbod LP, Borre M, Hoyer S, Harms HJ, Sorensen J, et al. The relationship between tumor aggressiveness and cholinergic PET imaging in prostate cancer tissue. A proof-of-concept study. American journal of nuclear medicine and molecular imaging. 2019;9(3):185–92. Nielsen MM, Tolbod LP, Borre M, Hoyer S, Harms HJ, Sorensen J, et al. The relationship between tumor aggressiveness and cholinergic PET imaging in prostate cancer tissue. A proof-of-concept study. American journal of nuclear medicine and molecular imaging. 2019;9(3):185–92.
51.
go back to reference Regula N, Honarvar H, Lubberink M, Jorulf H, Ladjevardi S, Haggman M, et al. Carbon flux as a measure of prostate cancer aggressiveness: [(11)C]-acetate PET/CT. Int J Med Sci. 2020;17(2):214–23.CrossRef Regula N, Honarvar H, Lubberink M, Jorulf H, Ladjevardi S, Haggman M, et al. Carbon flux as a measure of prostate cancer aggressiveness: [(11)C]-acetate PET/CT. Int J Med Sci. 2020;17(2):214–23.CrossRef
Metadata
Title
Potential synergy between PSMA uptake and tumour blood flow for prediction of human prostate cancer aggressiveness
Authors
Mads Ryø Jochumsen
Jens Sörensen
Lars Poulsen Tolbod
Bodil Ginnerup Pedersen
Jørgen Frøkiær
Michael Borre
Kirsten Bouchelouche
Publication date
01-12-2021
Publisher
Springer Berlin Heidelberg
Published in
EJNMMI Research / Issue 1/2021
Electronic ISSN: 2191-219X
DOI
https://doi.org/10.1186/s13550-021-00757-y

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