Application of probes for targeting prostate-specific membrane antigen molecular in diagnosis and treatment of prostate cancer_West China Medical Journal

Authors：

XU Xiaoyu , LI Xingchang , LÜ Shijian , XU Lingling ,  LAI Jianping

Department of Nuclear Medicine, the People’s Hospital of Three Gorge University, the First People’s Hospital of Yichang, Yichang, Hubei 443000, P. R. China;

Corresponding author：

LAI Jianping, Email: LJP2116@163.com

Keywords：

Positron emission tomography; Computed tomography; Prostate-specific membrane antigen; Prostate cancer

DOI：

10.7507/1002-0179.201911075

Video：

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Prostate cancer ranks second among the causes of death of malignant tumors in middle-aged and elderly men. A considerable number of patients are not easily detected in early-stage prostate cancer. Although traditional imaging examinations are of high value in the diagnosis and staging of prostate cancer, they also have certain limitations. With the development of nuclear medicine instruments and molecular probes, molecular imaging is playing an increasingly important role in the diagnosis and treatment of prostate cancer. Positron emission tomography and computed tomography (PET/CT) using prostate-specific membrane antigen (PSMA) as a probe has gained increasing recognition. This article will review the latest progress in the application of PET/CT using probes for targeting PSMA to imaging and treatment of prostate cancer, in order to provide a theoretical basis for the application of probes for targeting PSMA in the diagnosis and treatment of prostate cancer.

Citation： XU Xiaoyu, LI Xingchang, LÜ Shijian, XU Lingling, LAI Jianping. Application of probes for targeting prostate-specific membrane antigen molecular in diagnosis and treatment of prostate cancer. West China Medical Journal, 2020, 35(1): 98-102. doi: 10.7507/1002-0179.201911075 Copy

1.	王跃, 戴波. 中国抗癌协会2017版《前列腺癌筛查专家共识》解读. 临床外科杂志, 2018, 26(1): 15-18.
2.	Stephenson SK, Chang EK, Marks LS. Screening and detection advances in magnetic resonance image-guided prostate biopsy. Urol Clin North Am, 2014, 41(2): 315-326.
3.	Siddiqui MM, Rais-Bahrami S, Turkbey B, et al. Comparison of MR/ultrasound fusion-guided biopsy with ultrasound-guided biopsy for the diagnosis of prostate cancer. JAMA, 2015, 313(4): 390-397.
4.	Maurer T, Gschwend JE, Rauscher I, et al. Diagnostic efficacy of (68)gallium-PSMA positron emission tomography compared to conventional imaging for lymph node staging of 130 consecutive patients with intermediate to high risk prostate cancer. J Urol, 2016, 195(5): 1436-1443.
5.	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): 1185-1190.
6.	Maurer T, Weirich G, Schottelius M, et al. Prostate-specific membrane antigen-radioguided surgery for metastatic lymph nodes in prostate cancer. Eur Urol, 2015, 68(3): 530-534.
7.	Perera M, Papa N, Christidis D, 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(6): 926-937.
8.	朱华, 程震, 杨志. 核医学分子探针在前列腺癌诊断中的临床研究进展. 中华核医学与分子影像杂志, 2017, 37(2): 103-107.
9.	Banerjee SR, Pullambhatla M, Byun Y, et al. ⁶⁸Ga-labeled inhibitors of prostate-specific membrane antigen (PSMA) for imaging prostate cancer. J Med Chem, 2010, 53(14): 5333-5341.
10.	Beijing Institute for Cancer Research. Chinese guidelines for diagnosis and treatment of prostate cancer 2018 (English version). Chin J Cancer Re, 2019, 31(1): 67-83.
11.	Torre LA, Bray F, Siegel RL, et al. Global cancer statistics, 2012. CA Cancer J Clin, 2015, 65(2): 87-108.
12.	Demirci E, Sahin OE, Ocak M, et al. Normal distribution pattern and physiological variants of ⁶⁸Ga-PSMA-11 PET/CT imaging. Nucl Med Commun, 2016, 37(11): 1169-1179.
13.	Reisæter LA, Fütterer JJ, Halvorsen OJ, et al. 1.5-T multiparametric MRI using PI-RADS: a region by region analysis to localize the index-tumor of prostate cancer in patients undergoing prostatectomy. Acta Radiol, 2015, 56(4): 500-511.
14.	王利伟, 王峰, 殷信道, 等. ⁶⁸Ga-PSMA-11 PET/CT显像SUVmax联合MRI ADC诊断前列腺癌的价值. 中华核医学与分子影像杂志, 2019, 39(5): 257-261.
15.	Herlemann A, Wenter V, Kretschmer A, et al. ⁶⁸Ga-PSMA positron emission tomography/computed tomography provides accurate staging of lymph node regions prior to lymph node dissection in patients with prostate cancer. Eur Urol, 2016, 70(4): 553-557.
16.	Hijazi S, Meller B, Leitsmann C, et al. Pelvic lymph node dissection for nodal oligometastatic prostate cancer detected by ⁶⁸Ga-PSMA-positron emission tomography/computerized tomography. Prostate, 2015, 75(16): 1934-1940.
17.	van Leeuwen PJ, Emmett L, Ho B, et al. Prospective evaluation of ⁶⁸Gallium-prostate-specific membrane antigen positron emission tomography/computed tomography for preoperative lymph node staging in prostate cancer. BJU Int, 2017, 119(2): 209-215.
18.	Bouchelouche K, Turkbey B, Choyke PL. PSMA PET and radionuclide therapy in prostate cancer. Semin Nucl Med, 2016, 46(6): 522-535.
19.	李周雷, 龙亚丽, 张祥松. PSMA-PET在前列腺癌诊断中的最新进展. 影像诊断与介入放射学, 2018, 27(6): 481-486.
20.	Rauscher I, Horn T, Eiber M, et al. Novel technology of molecular radio-guidance for lymph node dissection in recurrent prostate cancer by PSMA-ligands. World J Urol, 2018, 36(4): 603-608.
21.	Bandini M, Fossati N, Briganti A. Salvage surgery for nodal recurrent prostate cancer. Curr Opin Urol, 2017, 27(6): 604-611.
22.	Yu CY, Desai B, Ji L, et al. Comparative performance of PET tracers in biochemical recurrence of prostate cancer: a critical analysis of literature. Am J Nucl Med Mol Imaging, 2014, 4(6): 580-601.
23.	Pfister D, Porres D, Heidenreich A, et al. Detection of recurrent prostate cancer lesions before salvage lymphadenectomy is more accurate with ⁶⁸Ga-PSMA-HBED-CC than with ¹⁸F-Fluoroethylcholine PET/CT. Eur J Nucl Med Mol Imaging, 2016, 43(8): 1410-1417.
24.	Eiber M, Maurer T, Souvatzoglou M, et al. Evaluation of hybrid ⁶⁸Ga-PSMA ligand PET/CT in 248 patients with biochemical recurrence after radical prostatectomy. J Nucl Med, 2015, 56(5): 668-674.
25.	Afshar-Oromieh A, Holland-Letz T, Giesel FL, et al. Diagnostic performance of ⁶⁸Ga-PSMA-11(HBED-CC) PET/CT in patients with recurrent prostate cancer: evaluation in 1007 patients. EurJ Nucl Med Mol Imaging, 2017, 44(8): 1258-1268.
26.	Schwenck J, Rempp H, Reischl G, et al. Comparison of ⁶⁸Ga-labelled PSMA-11 and ¹¹C-choline in the detection of prostate cancer metastases by PET/CT. Eur J Nucl Med Mol Imaging, 2017, 44(1): 92-101.
27.	Bluemel C, Krebs M, Polat B, et al. ⁶⁸Ga-PSMA-PET/CT in patients with biochemical prostate cancer recurrence and negative 18F-choline-PET/CT. Clin Nucl Med, 2016, 41(7): 515-521.
28.	Montorsi F, Gandaglia G, Fossati N, et al. Robot-assisted salvage lymph node dissection for clinically recurrent prostate cancer. Eur Urol, 2017, 72(3): 432-438.
29.	Siriwardana A, Thompson J, van Leeuwen PJ, et al. Initial multicentre experience of ⁶⁸gallium-PSMA PET/CT guided robot-assisted salvage lymphadenectomy: acceptable safety profile but oncological benefit appears limited. BJU Int, 2017, 120(5): 673-681.
30.	Herlemann A, Kretschmer A, Buchner A, et al. Salvage lymph node dissection after ⁶⁸Ga-PSMA or ¹⁸F-FEC PET/CT for nodal recurrence in prostate cancer patients. Oncotarget, 2017, 8(48): 84180-84192.
31.	Tilki D, Mandel P, Seeliger F, et al. Salvage lymph node dissection for nodal recurrence of prostate cancer after radical prostatectomy. J Urol, 2015, 193(2): 484-490.
32.	Wu CT, Chen WC, Chen MF. The response of prostate cancer to androgen deprivation and irradiation due to immune modulation. Cancers (Basel), 2018, 11(1): 20.
33.	Rahbar K, Bögeman M, Yordanova A, et al. Delayed response after repeated ¹⁷⁷Lu-PSMA-617 radioligand therapy in patients with metastatic castration resistant prostate cancer. Eur J Nucl Med Mol Imaging, 2018, 45(2): 243-246.
34.	Ahmadzadehfar H, Wegen S, Yordanova A, 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(9): 1448-1454.
35.	Rahbar K, Ahmadzadehfar H, Kratochwil C, et al. German multicenter study investigating ¹⁷⁷Lu-PSMA-617 radioligand therapy in advanced prostate cancer patients. J Nucl Med, 2017, 58(1): 85-90.
36.	Wei X, Schlenkhoff C, Schwarz B, et al. 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(9): 704-706.
37.	Bradley CA. [¹⁷⁷Lu]PSMA-617 radionuclide therapy shows promise. Nat Rev Urol, 2018, 15(8): 468.
38.	Gafita A, Rauscher I, Retz M, et al. Early experience of rechallenge ¹⁷⁷Lu-PSMA radioligand therapy after an initial good response in patients with advanced prostate cancer. J Nucl Med, 2019, 60(5): 644-648.
39.	Evangelista L, Bertoldo F, Boccardo F, et al. Diagnostic imaging to detect and evaluate response to therapy in bone metastases from prostate cancer: current modalities and new horizons. Eur J Nucl Med Mol Imaging, 2016, 43(8): 1546-1562.
40.	Heinzel A, Boghos D, Mottaghy FM, et al. ⁶⁸Ga-PSMA PET/CT for monitoring response to ¹⁷⁷Lu-PSMA-617 radioligand therapy in patients with metastatic castration-resistant prostate cancer. EurJ Nucl Med Mol Imaging, 2019, 46(5): 1054-1062.
41.	O JH, Lodge MA, Wahl RL. Practical PERCIST: a simplified guide to PET response criteria in solid tumors 1.0. Radiology, 2016, 280(2): 576-584.
42.	Kulkarni HR, Singh A, Schuchardt C, et al. PSMA-based radioligand therapy for metastatic castration-resistant prostate cancer: the bad berka experience since 2013. J Nucl Med, 2016, 57(Suppl 3): 97S-104S.
43.	Giesel FL, Hadaschik B, Cardinale J, et al. F-18 labelled PSMA-1007: biodistribution, radiation dosimetry and histopathological validation of tumor lesions in prostate cancer patients. Eur J Nucl Med Mol Imaging, 2017, 44(4): 678-688.

1. 王跃, 戴波. 中国抗癌协会2017版《前列腺癌筛查专家共识》解读. 临床外科杂志, 2018, 26(1): 15-18.
2. Stephenson SK, Chang EK, Marks LS. Screening and detection advances in magnetic resonance image-guided prostate biopsy. Urol Clin North Am, 2014, 41(2): 315-326.
3. Siddiqui MM, Rais-Bahrami S, Turkbey B, et al. Comparison of MR/ultrasound fusion-guided biopsy with ultrasound-guided biopsy for the diagnosis of prostate cancer. JAMA, 2015, 313(4): 390-397.
4. Maurer T, Gschwend JE, Rauscher I, et al. Diagnostic efficacy of (68)gallium-PSMA positron emission tomography compared to conventional imaging for lymph node staging of 130 consecutive patients with intermediate to high risk prostate cancer. J Urol, 2016, 195(5): 1436-1443.
5. 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): 1185-1190.
6. Maurer T, Weirich G, Schottelius M, et al. Prostate-specific membrane antigen-radioguided surgery for metastatic lymph nodes in prostate cancer. Eur Urol, 2015, 68(3): 530-534.
7. Perera M, Papa N, Christidis D, 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(6): 926-937.
8. 朱华, 程震, 杨志. 核医学分子探针在前列腺癌诊断中的临床研究进展. 中华核医学与分子影像杂志, 2017, 37(2): 103-107.
9. Banerjee SR, Pullambhatla M, Byun Y, et al. ⁶⁸Ga-labeled inhibitors of prostate-specific membrane antigen (PSMA) for imaging prostate cancer. J Med Chem, 2010, 53(14): 5333-5341.
10. Beijing Institute for Cancer Research. Chinese guidelines for diagnosis and treatment of prostate cancer 2018 (English version). Chin J Cancer Re, 2019, 31(1): 67-83.
11. Torre LA, Bray F, Siegel RL, et al. Global cancer statistics, 2012. CA Cancer J Clin, 2015, 65(2): 87-108.
12. Demirci E, Sahin OE, Ocak M, et al. Normal distribution pattern and physiological variants of ⁶⁸Ga-PSMA-11 PET/CT imaging. Nucl Med Commun, 2016, 37(11): 1169-1179.
13. Reisæter LA, Fütterer JJ, Halvorsen OJ, et al. 1.5-T multiparametric MRI using PI-RADS: a region by region analysis to localize the index-tumor of prostate cancer in patients undergoing prostatectomy. Acta Radiol, 2015, 56(4): 500-511.
14. 王利伟, 王峰, 殷信道, 等. ⁶⁸Ga-PSMA-11 PET/CT显像SUVmax联合MRI ADC诊断前列腺癌的价值. 中华核医学与分子影像杂志, 2019, 39(5): 257-261.
15. Herlemann A, Wenter V, Kretschmer A, et al. ⁶⁸Ga-PSMA positron emission tomography/computed tomography provides accurate staging of lymph node regions prior to lymph node dissection in patients with prostate cancer. Eur Urol, 2016, 70(4): 553-557.
16. Hijazi S, Meller B, Leitsmann C, et al. Pelvic lymph node dissection for nodal oligometastatic prostate cancer detected by ⁶⁸Ga-PSMA-positron emission tomography/computerized tomography. Prostate, 2015, 75(16): 1934-1940.
17. van Leeuwen PJ, Emmett L, Ho B, et al. Prospective evaluation of ⁶⁸Gallium-prostate-specific membrane antigen positron emission tomography/computed tomography for preoperative lymph node staging in prostate cancer. BJU Int, 2017, 119(2): 209-215.
18. Bouchelouche K, Turkbey B, Choyke PL. PSMA PET and radionuclide therapy in prostate cancer. Semin Nucl Med, 2016, 46(6): 522-535.
19. 李周雷, 龙亚丽, 张祥松. PSMA-PET在前列腺癌诊断中的最新进展. 影像诊断与介入放射学, 2018, 27(6): 481-486.
20. Rauscher I, Horn T, Eiber M, et al. Novel technology of molecular radio-guidance for lymph node dissection in recurrent prostate cancer by PSMA-ligands. World J Urol, 2018, 36(4): 603-608.
21. Bandini M, Fossati N, Briganti A. Salvage surgery for nodal recurrent prostate cancer. Curr Opin Urol, 2017, 27(6): 604-611.
22. Yu CY, Desai B, Ji L, et al. Comparative performance of PET tracers in biochemical recurrence of prostate cancer: a critical analysis of literature. Am J Nucl Med Mol Imaging, 2014, 4(6): 580-601.
23. Pfister D, Porres D, Heidenreich A, et al. Detection of recurrent prostate cancer lesions before salvage lymphadenectomy is more accurate with ⁶⁸Ga-PSMA-HBED-CC than with ¹⁸F-Fluoroethylcholine PET/CT. Eur J Nucl Med Mol Imaging, 2016, 43(8): 1410-1417.
24. Eiber M, Maurer T, Souvatzoglou M, et al. Evaluation of hybrid ⁶⁸Ga-PSMA ligand PET/CT in 248 patients with biochemical recurrence after radical prostatectomy. J Nucl Med, 2015, 56(5): 668-674.
25. Afshar-Oromieh A, Holland-Letz T, Giesel FL, et al. Diagnostic performance of ⁶⁸Ga-PSMA-11(HBED-CC) PET/CT in patients with recurrent prostate cancer: evaluation in 1007 patients. EurJ Nucl Med Mol Imaging, 2017, 44(8): 1258-1268.
26. Schwenck J, Rempp H, Reischl G, et al. Comparison of ⁶⁸Ga-labelled PSMA-11 and ¹¹C-choline in the detection of prostate cancer metastases by PET/CT. Eur J Nucl Med Mol Imaging, 2017, 44(1): 92-101.
27. Bluemel C, Krebs M, Polat B, et al. ⁶⁸Ga-PSMA-PET/CT in patients with biochemical prostate cancer recurrence and negative 18F-choline-PET/CT. Clin Nucl Med, 2016, 41(7): 515-521.
28. Montorsi F, Gandaglia G, Fossati N, et al. Robot-assisted salvage lymph node dissection for clinically recurrent prostate cancer. Eur Urol, 2017, 72(3): 432-438.
29. Siriwardana A, Thompson J, van Leeuwen PJ, et al. Initial multicentre experience of ⁶⁸gallium-PSMA PET/CT guided robot-assisted salvage lymphadenectomy: acceptable safety profile but oncological benefit appears limited. BJU Int, 2017, 120(5): 673-681.
30. Herlemann A, Kretschmer A, Buchner A, et al. Salvage lymph node dissection after ⁶⁸Ga-PSMA or ¹⁸F-FEC PET/CT for nodal recurrence in prostate cancer patients. Oncotarget, 2017, 8(48): 84180-84192.
31. Tilki D, Mandel P, Seeliger F, et al. Salvage lymph node dissection for nodal recurrence of prostate cancer after radical prostatectomy. J Urol, 2015, 193(2): 484-490.
32. Wu CT, Chen WC, Chen MF. The response of prostate cancer to androgen deprivation and irradiation due to immune modulation. Cancers (Basel), 2018, 11(1): 20.
33. Rahbar K, Bögeman M, Yordanova A, et al. Delayed response after repeated ¹⁷⁷Lu-PSMA-617 radioligand therapy in patients with metastatic castration resistant prostate cancer. Eur J Nucl Med Mol Imaging, 2018, 45(2): 243-246.
34. Ahmadzadehfar H, Wegen S, Yordanova A, 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(9): 1448-1454.
35. Rahbar K, Ahmadzadehfar H, Kratochwil C, et al. German multicenter study investigating ¹⁷⁷Lu-PSMA-617 radioligand therapy in advanced prostate cancer patients. J Nucl Med, 2017, 58(1): 85-90.
36. Wei X, Schlenkhoff C, Schwarz B, et al. 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(9): 704-706.
37. Bradley CA. [¹⁷⁷Lu]PSMA-617 radionuclide therapy shows promise. Nat Rev Urol, 2018, 15(8): 468.
38. Gafita A, Rauscher I, Retz M, et al. Early experience of rechallenge ¹⁷⁷Lu-PSMA radioligand therapy after an initial good response in patients with advanced prostate cancer. J Nucl Med, 2019, 60(5): 644-648.
39. Evangelista L, Bertoldo F, Boccardo F, et al. Diagnostic imaging to detect and evaluate response to therapy in bone metastases from prostate cancer: current modalities and new horizons. Eur J Nucl Med Mol Imaging, 2016, 43(8): 1546-1562.
40. Heinzel A, Boghos D, Mottaghy FM, et al. ⁶⁸Ga-PSMA PET/CT for monitoring response to ¹⁷⁷Lu-PSMA-617 radioligand therapy in patients with metastatic castration-resistant prostate cancer. EurJ Nucl Med Mol Imaging, 2019, 46(5): 1054-1062.
41. O JH, Lodge MA, Wahl RL. Practical PERCIST: a simplified guide to PET response criteria in solid tumors 1.0. Radiology, 2016, 280(2): 576-584.
42. Kulkarni HR, Singh A, Schuchardt C, et al. PSMA-based radioligand therapy for metastatic castration-resistant prostate cancer: the bad berka experience since 2013. J Nucl Med, 2016, 57(Suppl 3): 97S-104S.
43. Giesel FL, Hadaschik B, Cardinale J, et al. F-18 labelled PSMA-1007: biodistribution, radiation dosimetry and histopathological validation of tumor lesions in prostate cancer patients. Eur J Nucl Med Mol Imaging, 2017, 44(4): 678-688.

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Application of probes for targeting prostate-specific membrane antigen molecular in diagnosis and treatment of prostate cancer

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