Multiparametric Magnetic Resonance Imaging for Bladder Cancer: Development of VI-RADS (Vesical Imaging-Reporting And Data System)

European Urology

Volumn 74, Issue 3, 2018, Pages 294-306

  Panebianco, Valeria ^a   Narumi, Yoshifumi ^b   Altun, Ersan ^c   Bochner, Bernard H ^d   Efstathiou, Jason A ^e   Hafeez, Shaista ^f,g   Huddart, Robert ^f,g   Kennish, Steve ^h   Lerner, Seth ⁱ   Montironi, Rodolfo ^j   Muglia, Valdair F ^k   Salomon, Georg ^l   Thomas, Stephen ^m   Vargas, Hebert Alberto ^d   Witjes, J Alfred ⁿ   Takeuchi, Mitsuru ^o   Barentsz, Jelle ⁿ   Catto, James W F ^p  

^a SAPIENZA UNIVERSITY OF ROME   (Italy)

^b OSAKA MEDICAL COLLEGE   (Japan)

^c UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^d MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^e MASSACHUSETTS GENERAL HOSPITAL   (United States)

^f INSTITUTE OF CANCER RESEARCH   (United Kingdom)

^g INSTITUTE OF CANCER RESEARCH   (United Kingdom)

^h SHEFFIELD TEACHING HOSPITALS NHS FOUNDATION TRUST   (United Kingdom)

ⁱ BAYLOR COLLEGE OF MEDICINE   (United States)

^j UNIVERSITÀ POLITECNICA DELLE MARCHE   (Italy)

^k UNIVERSITY OF SÃO PAULO   (Brazil)

^l UNIVERSITY MEDICAL CENTER HAMBURG EPPENDORF   (Germany)

^m UNIVERSITY OF CHICAGO   (United States)

ⁿ RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

^o Radiolonet Tokai ^*  (Japan)

^p UNIVERSITY OF SHEFFIELD   (United Kingdom)

more..

Author keywords

Bladder cancer; Multiparametric magnetic resonance imaging; RADS; Scoring; Staging

Indexed keywords

BLADDER CANCER; CANCER DIAGNOSIS; CANCER PROGNOSIS; DIAGNOSTIC ACCURACY; DIAGNOSTIC IMAGING; DIFFUSION WEIGHTED IMAGING; DYNAMIC CONTRAST-ENHANCED MAGNETIC RESONANCE IMAGING; HUMAN; IMAGE ANALYSIS; INFORMATION RETRIEVAL; MULTIPARAMETRIC MAGNETIC RESONANCE IMAGING; MUSCLE INVASIVE BLADDER CANCER; PRIORITY JOURNAL; REVIEW; TRANSURETHRAL RESECTION; BLADDER TUMOR; CANCER STAGING; COMPUTER ASSISTED DIAGNOSIS; CONSENSUS; INFORMATION PROCESSING; OBSERVER VARIATION; PATHOLOGY; PREDICTIVE VALUE; PROCEDURES; REPRODUCIBILITY; STANDARDS;

CONTRAST MEDIUM;

CONSENSUS; CONTRAST MEDIA; DATA SYSTEMS; DIFFUSION MAGNETIC RESONANCE IMAGING; HUMANS; IMAGE INTERPRETATION, COMPUTER-ASSISTED; NEOPLASM STAGING; OBSERVER VARIATION; PREDICTIVE VALUE OF TESTS; REPRODUCIBILITY OF RESULTS; URINARY BLADDER NEOPLASMS;

EID: 85046821608     PISSN: 03022838     EISSN: 18737560     Source Type: Journal    
DOI: 10.1016/j.eururo.2018.04.029     Document Type: Review

References (86)

1. Svatek, R.S., Hollenbeck, B.K., Holmang, S., et al. The economics of bladder cancer: costs and considerations of caring for this disease. Eur Urol 66 (2014), 253–262.
2. Antoni, S., Ferlay, J., Soerjomataram, I., Znaor, A., Jemal, A., Bray, F., Bladder cancer incidence and mortality: a global overview and recent trends. Eur Urol 71 (2017), 96–108.
3. Leow, J.J., Cole, A.P., Seisen, T., et al. Variations in the costs of radical cystectomy for bladder cancer in the USA. Eur Urol 73 (2018), 374–382.
4. Soukup, V., Capoun, O., Cohen, D., et al. Prognostic performance and reproducibility of the 1973 and 2004/2016 World Health Organization grading classification systems in non-muscle-invasive bladder cancer: a European Association of Urology Non-muscle Invasive Bladder Cancer Guidelines Panel systematic review. Eur Urol 72 (2017), 801–813.
5. Linton, K.D., Rosario, D.J., Thomas, F., et al. Disease specific mortality in patients with low risk bladder cancer and the impact of cystoscopic surveillance. J Urol 189 (2013), 828–833.
6. Babjuk, M., Bohle, A., Burger, M., et al. EAU guidelines on non-muscle-invasive urothelial carcinoma of the bladder: update 2016. Eur Urol 71 (2017), 447–461.
7. Sylvester, R.J., van der Meijden, A.P., Oosterlinck, W., et al. Predicting recurrence and progression in individual patients with stage Ta T1 bladder cancer using EORTC risk tables: a combined analysis of 2596 patients from seven EORTC trials. Eur Urol 49 (2006), 466–475 discussion 75–7.
8. Kluth, L.A., Black, P.C., Bochner, B.H., et al. Prognostic and prediction tools in bladder cancer: a comprehensive review of the literature. Eur Urol 68 (2015), 238–253.
9. Gontero, P., Sylvester, R., Pisano, F., et al. Prognostic factors and risk groups in T1G3 non-muscle-invasive bladder cancer patients initially treated with Bacillus Calmette-Guerin: results of a retrospective multicenter study of 2451 patients. Eur Urol 67 (2015), 74–82.
10. Witjes, J.A., Comperat, E., Cowan, N.C., et al. EAU guidelines on muscle-invasive and metastatic bladder cancer: summary of the 2013 guidelines. Eur Urol 65 (2014), 778–792.
11. Fonteyne, V., Ost, P., Bellmunt, J., et al. Curative treatment for muscle invasive bladder cancer in elderly patients: a systematic review. Eur Urol 73 (2018), 40–50.
12. Noon, A.P., Albertsen, P.C., Thomas, F., Rosario, D.J., Catto, J., Competing mortality in patients diagnosed with bladder cancer: Evidence of under-treatment in the elderly and females. Br J Cancer 108 (2013), 1534–1540.
13. Stein, J.P., Lieskovsky, G., Cote, R., et al. Radical cystectomy in the treatment of invasive bladder cancer: long-term results in 1,054 patients. J Clin Oncol 19 (2001), 666–675.
14. James, N.D., Hussain, S.A., Hall, E., et al. Radiotherapy with or without chemotherapy in muscle-invasive bladder cancer. N Engl J Med 366 (2012), 1477–1488.
15. Giacalone, N.J., Shipley, W.U., Clayman, R.H., et al. Long-term outcomes after bladder-preserving tri-modality therapy for patients with muscle-invasive bladder cancer: an updated analysis of the Massachusetts General Hospital experience. Eur Urol 71 (2017), 952–960.
16. Eylert, M.F., Hounsome, L.S., Persad, R., et al. Falling bladder cancer incidence from 1990 to 2009 is not producing universal mortality improvements. J Clin Urol 7 (2014), 90–98.
17. Saunders, C.L., Abel, G.A., Lyratzopoulos, G., Inequalities in reported cancer patient experience by socio-demographic characteristic and cancer site: evidence from respondents to the English Cancer Patient Experience Survey. Eur J Cancer Care (Engl) 24 (2015), 85–98.
18. Kulkarni, G.S., Hakenberg, O.W., Gschwend, J.E., et al. An updated critical analysis of the treatment strategy for newly diagnosed high-grade T1 (previously T1G3) bladder cancer. Eur Urol 57 (2010), 60–70.
19. Gordon PC, Thomas F, Noon AP, Rosario DJ, Catto JWF. Long-term outcomes from re-resection for high-risk non-muscle invasive bladder cancer: a potential to rationalize use. Eur Urol Focus. In press. https://doi.org/10.1016/j.euf.2017.10.004.
20. Ark, J.T., Keegan, K.A., Barocas, D.A., et al. Incidence and predictors of understaging in patients with clinical T1 urothelial carcinoma undergoing radical cystectomy. BJU Int 113 (2014), 894–899.
21. Brausi, M., Collette, L., Kurth, K., et al. Variability in the recurrence rate at first follow-up cystoscopy after TUR in stage Ta T1 transitional cell carcinoma of the bladder: a combined analysis of seven EORTC studies. Eur Urol 41 (2002), 523–531.
22. Hall, M.C., Chang, S.S., Dalbagni, G., et al. Guideline for the management of nonmuscle invasive bladder cancer (stages Ta, T1, and Tis): 2007 update. J Urol 178 (2007), 2314–2330.
23. Burger, M., Oosterlinck, W., Konety, B., et al. ICUD-EAU international consultation on bladder cancer 2012: non-muscle-invasive urothelial carcinoma of the bladder. Eur Urol 63 (2013), 36–44.
24. Witjes, J.A., Babjuk, M., Gontero, P., et al. Clinical and cost effectiveness of hexaminolevulinate-guided blue-light cystoscopy: evidence review and updated expert recommendations. Eur Urol 66 (2014), 863–871.
25. Mari, A., Abufaraj, M., Gust, K.M., Shariat, S.F., Novel endoscopic visualization techniques for bladder cancer detection: a review of the contemporary literature. Curr Opin Urol 28 (2018), 214–218.
26. Engilbertsson, H., Aaltonen, K.E., Bjornsson, S., et al. Transurethral bladder tumor resection can cause seeding of cancer cells into the bloodstream. J Urol 193 (2015), 53–57.
27. Mydlo, J.H., Weinstein, R., Shah, S., Solliday, M., Macchia, R.J., Long-term consequences from bladder perforation and/or violation in the presence of transitional cell carcinoma: results of a small series and a review of the literature. J Urol 161 (1999), 1128–1132.
28. Humphrey, P.A., Moch, H., Cubilla, A.L., Ulbright, T.M., Reuter, V.E., The 2016 WHO classification of tumours of the urinary system and male genital organs—part B: prostate and bladder tumours. Eur Urol 70 (2016), 106–119.
29. Ficarra, V., Dalpiaz, O., Alrabi, N., Novara, G., Galfano, A., Artibani, W., Correlation between clinical and pathological staging in a series of radical cystectomies for bladder carcinoma. BJU Int 95 (2005), 786–790.
30. Kim, J.K., Park, S.Y., Ahn, H.J., Kim, C.S., Cho, K.S., Bladder cancer: analysis of multi-detector row helical CT enhancement pattern and accuracy in tumor detection and perivesical staging. Radiology 231 (2004), 725–731.
31. Paner, G.P., Montironi, R., Amin, M.B., Challenges in pathologic staging of bladder cancer: proposals for fresh approaches of assessing pathologic stage in light of recent studies and observations pertaining to bladder histoanatomic variances. Adv Anat Pathol 24 (2017), 113–127.
32. Tritschler, S., Mosler, C., Straub, J., et al. Staging of muscle-invasive bladder cancer: can computerized tomography help us to decide on local treatment?. World J Urol 30 (2012), 827–831.
33. Woo, S., Suh, C.H., Kim, S.Y., Cho, J.Y., Kim, S.H., Diagnostic performance of MRI for prediction of muscle-invasiveness of bladder cancer: a systematic review and meta-analysis. Eur J Radiol 95 (2017), 46–55.
34. Huang, L., Kong, Q., Liu, Z., Wang, J., Kang, Z., Zhu, Y., The Diagnostic value of MR imaging in differentiating T staging of bladder cancer: a meta-analysis. Radiology 286 (2018), 502–511.
35. Kim, B., Semelka, R.C., Ascher, S.M., Chalpin, D.B., Carroll, P.R., Hricak, H., Bladder tumor staging: comparison of contrast-enhanced CT, T1- and T2-weighted MR imaging, dynamic gadolinium-enhanced imaging, and late gadolinium-enhanced imaging. Radiology 193 (1994), 239–245.
36. Johnson, W., Taylor, M.B., Carrington, B.M., Bonington, S.C., Swindell, R., The value of hyoscine butylbromide in pelvic MRI. Clin Radiol 62 (2007), 1087–1093.
37. Barentsz, J.O., Ruijs, S.H., Strijk, S.P., The role of MR imaging in carcinoma of the urinary bladder. AJR Am J Roentgenol 160 (1993), 937–947.
38. Panebianco, V., Barchetti, F., de Haas, R.J., et al. Improving staging in bladder cancer: the increasing role of multiparametric magnetic resonance imaging. Eur Urol Focus 2 (2016), 113–121.
39. Takeuchi, M., Sasaki, S., Ito, M., et al. Urinary bladder cancer: diffusion-weighted MR imaging–accuracy for diagnosing T stage and estimating histologic grade. Radiology 251 (2009), 112–121.
40. Takeuchi, M., Sasaki, S., Naiki, T., et al. MR imaging of urinary bladder cancer for T-staging: a review and a pictorial essay of diffusion-weighted imaging. J Magn Reson Imaging 38 (2013), 1299–1309.
41. Donaldson, S.B., Bonington, S.C., Kershaw, L.E., et al. Dynamic contrast-enhanced MRI in patients with muscle-invasive transitional cell carcinoma of the bladder can distinguish between residual tumour and post-chemotherapy effect. Eur J Radiol 82 (2013), 2161–2168.
42. Narumi, Y., Kadota, T., Inoue, E., et al. Bladder tumors: staging with gadolinium-enhanced oblique MR imaging. Radiology 187 (1993), 145–150.
43. Hayashi, N., Tochigi, H., Shiraishi, T., Takeda, K., Kawamura, J., A new staging criterion for bladder carcinoma using gadolinium-enhanced magnetic resonance imaging with an endorectal surface coil: a comparison with ultrasonography. BJU Int 85 (2000), 32–36.
44. Zhou, G., Chen, X., Zhang, J., Zhu, J., Zong, G., Wang, Z., Contrast-enhanced dynamic and diffusion-weighted MR imaging at 3.0T to assess aggressiveness of bladder cancer. Eur J Radiol 83 (2014), 2013–2018.
45. Naish, J.H., McGrath, D.M., Bains, L.J., et al. Comparison of dynamic contrast-enhanced MRI and dynamic contrast-enhanced CT biomarkers in bladder cancer. Magn Reson Med 66 (2011), 219–226.
46. Panebianco, V., De Berardinis, E., Barchetti, G., et al. An evaluation of morphological and functional multi-parametric MRI sequences in classifying non-muscle and muscle invasive bladder cancer. Eur Radiol 27 (2017), 3759–3766.
47. Cheong, J.J.W., Woodward, P.J., Maria, A., Davis, C.J., From the archives of the AFIP inflammatory and nonneoplastic bladder masses: radiologic-pathologic objectives. RadioGraphics 1595 (2006), 1847–1869.
48. Ma, W., Kang, S.K., Hricak, H., Gerst, S.R., Zhang, J., Imaging appearance of granulomatous disease after intravesical Bacille Calmette-Guerin (BCG) treatment of bladder carcinoma. AJR Am J Roentgenol 192 (2009), 1494–1500.
49. El-Assmy, A., Abou-El-Ghar, M.E., Refaie, H.F., Mosbah, A., El-Diasty, T., Diffusion-weighted magnetic resonance imaging in follow-up of superficial urinary bladder carcinoma after transurethral resection: initial experience. BJU Int 110 (2012), E622–E627.
50. Wang, H.J., Pui, M.H., Guo, Y., Yang, D., Pan, B.T., Zhou, X.H., Diffusion-weighted MRI in bladder carcinoma: the differentiation between tumor recurrence and benign changes after resection. Abdom Imaging 39 (2014), 135–141.
51. Narumi, Y., Kadota, T., Inoue, E., et al. Bladder wall morphology: in vitro MR imaging-histopathologic correlation. Radiology 187 (1993), 151–155.
52. Xiao, G.Q., Rashid, H., Bladder neck urothelial carcinoma: a urinary bladder subsite carcinoma with distinct clinicopathology. Int J Surg Pathol 23 (2015), 517–523.
53. Wang, H.J., Pui, M.H., Guan, J., et al. Comparison of early submucosal enhancement and tumor stalk in staging bladder urothelial carcinoma. AJR Am J Roentgenol 207 (2016), 797–803.
54. Kulkarni, G.S., Alibhai, S.M., Finelli, A., et al. Cost-effectiveness analysis of immediate radical cystectomy versus intravesical Bacillus Calmette-Guerin therapy for high-risk, high-grade (T1G3) bladder cancer. Cancer 115 (2009), 5450–5459.
55. Lammle, M., Beer, A., Settles, M., Hannig, C., Schwaibold, H., Drews, C., Reliability of MR imaging-based virtual cystoscopy in the diagnosis of cancer of the urinary bladder. AJR Am J Roentgenol 178 (2002), 1483–1488.
56. Gore, J.L., Lai, J., Setodji, C.M., Litwin, M.S., Saigal, C.S., Urologic Diseases in America Project. Mortality increases when radical cystectomy is delayed more than 12 weeks: results from a Surveillance, Epidemiology, and End Results-Medicare analysis. Cancer 115 (2009), 988–996.
57. van den Bosch, S., Alfred Witjes, J., Long-term cancer-specific survival in patients with high-risk, non-muscle-invasive bladder cancer and tumour progression: a systematic review. Eur Urol 60 (2011), 493–500.
58. Oughton, J.B., Poad, H., Twiddy, M., et al. Radical cystectomy (bladder removal) against intravesical BCG immunotherapy for high-risk non-muscle invasive bladder cancer (BRAVO): a protocol for a randomised controlled feasibility study. BMJ Open, 7, 2017, e017913.
59. Wang, F., Wu, L.M., Hua, X.L., Zhao, Z.Z., Chen, X.X., Xu, J.R., Intravoxel incoherent motion diffusion-weighted imaging in assessing bladder cancer invasiveness and cell proliferation. J Magn Reson Imaging 47 (2018), 1054–1060.
60. Thomas, F., Noon, A.P., Rubin, N., Goepel, J.R., Catto, J.W., Comparative outcomes of primary, recurrent, and progressive high-risk non-muscle-invasive bladder cancer. Eur Urol 63 (2013), 145–154.
61. International Collaboration of Trialists, Medical Research Council Advanced Bladder Cancer Working Party (now the National Cancer Research Institute Bladder Cancer Clinical Studies Group), European Organisation for Research and Treatment of Cancer Genito-urinary Tract Cancer Group, et al. International phase III trial assessing neoadjuvant cisplatin, methotrexate, and vinblastine chemotherapy for muscle-invasive bladder cancer: long-term results of the BA06 30894 trial. J Clin Oncol 29 (2011), 2171–2177.
62. Seisen, T., Sun, M., Lipsitz, S.R., et al. Comparative effectiveness of trimodal therapy versus radical cystectomy for localized muscle-invasive urothelial carcinoma of the bladder. Eur Urol. 72 (2017), 483–487.
63. Schrier, B.P., Peters, M., Barentsz, J.O., Witjes, J.A., Evaluation of chemotherapy with magnetic resonance imaging in patients with regionally metastatic or unresectable bladder cancer. Eur Urol 49 (2006), 698–703.
64. Barentsz, J.O., Berger-Hartog, O., Witjes, J.A., et al. Evaluation of chemotherapy in advanced urinary bladder cancer with fast dynamic contrast-enhanced MR imaging. Radiology 207 (1998), 791–797.
65. Nguyen, H.T., Jia, G., Shah, Z.K., et al. Prediction of chemotherapeutic response in bladder cancer using K-means clustering of dynamic contrast-enhanced (DCE)-MRI pharmacokinetic parameters. J Magn Reson Imaging 41 (2015), 1374–1382.
66. Eisenhauer, E.A., Therasse, P., Bogaerts, J., et al. New response evaluation criteria in solid tumours: revised RECIST guideline (version 1.1). Eur J Cancer 45 (2009), 228–247.
67. Yoshida, S., Koga, F., Kawakami, S., et al. Initial experience of diffusion-weighted magnetic resonance imaging to assess therapeutic response to induction chemoradiotherapy against muscle-invasive bladder cancer. Urology 75 (2010), 387–391.
68. Johnson, R.J., Carrington, B.M., Jenkins, J.P., Barnard, R.J., Read, G., Isherwood, I., Accuracy in staging carcinoma of the bladder by magnetic resonance imaging. Clin Radiol 41 (1990), 258–263.
69. Barentsz, J.O., Jager, G.J., van Vierzen, P.B., et al. Staging urinary bladder cancer after transurethral biopsy: value of fast dynamic contrast-enhanced MR imaging. Radiology 201 (1996), 185–193.
70. Splinter, T.A., Scher, H.I., Denis, L., et al. The prognostic value of the pathological response to combination chemotherapy before cystectomy in patients with invasive bladder cancer. European Organization for Research on Treatment of Cancer—Genitourinary Group. J Urol 147 (1992), 606–608.
71. Grossman, H.B., Natale, R.B., Tangen, C.M., et al. Neoadjuvant chemotherapy plus cystectomy compared with cystectomy alone for locally advanced bladder cancer. N Engl J Med 349 (2003), 859–866.
72. Sternberg, C.N., Pansadoro, V., Calabro, F., et al. Can patient selection for bladder preservation be based on response to chemotherapy?. Cancer 97 (2003), 1644–1652.
73. Mak, R.H., Hunt, D., Shipley, W.U., et al. Long-term outcomes in patients with muscle-invasive bladder cancer after selective bladder-preserving combined-modality therapy: a pooled analysis of radiation therapy oncology group protocols 8802, 8903, 9506, 9706, 9906, and 0233. J Clin Oncol 32 (2014), 3801–3809.
74. Hafeez, S., Horwich, A., Omar, O., et al. Selective organ preservation with neo-adjuvant chemotherapy for the treatment of muscle invasive transitional cell carcinoma of the bladder. Br J Cancer 112 (2015), 1626–1635.
75. Efstathiou, J.A., Spiegel, D.Y., Shipley, W.U., et al. Long-term outcomes of selective bladder preservation by combined-modality therapy for invasive bladder cancer: the MGH experience. Eur Urol 61 (2012), 705–711.
76. Rosenblatt, R., Sherif, A., Rintala, E., et al. Pathologic downstaging is a surrogate marker for efficacy and increased survival following neoadjuvant chemotherapy and radical cystectomy for muscle-invasive urothelial bladder cancer. Eur Urol 61 (2012), 1229–1238.
77. Yoshida, S., Koga, F., Kobayashi, S., et al. Role of diffusion-weighted magnetic resonance imaging in predicting sensitivity to chemoradiotherapy in muscle-invasive bladder cancer. Int J Radiat Oncol Biol Phys 83 (2012), e21–e27.
78. Sevcenco, S., Haitel, A., Ponhold, L., et al. Quantitative apparent diffusion coefficient measurements obtained by 3-Tesla MRI are correlated with biomarkers of bladder cancer proliferative activity. PLoS One, 9, 2014, e106866.
79. Kobayashi, S., Koga, F., Kajino, K., et al. Apparent diffusion coefficient value reflects invasive and proliferative potential of bladder cancer. J Magn Reson Imaging 39 (2014), 172–178.
80. Alfred Witjes, J., Lebret, T., Comperat, E.M., et al. Updated 2016 EAU guidelines on muscle-invasive and metastatic bladder cancer. Eur Urol 71 (2017), 462–475.
81. Advanced Bladder Cancer (ABC) Meta-analysis Collaboration, Neoadjuvant chemotherapy in invasive bladder cancer: update of a systematic review and meta-analysis of individual patient data. Eur Urol 48 (2005), 202–205 discussion 5-6.
82. Hafeez, S., Koh, M.D., Sohaib, A., Huddart, R., Use of diffusion weighted-MRI (DW-MRI) as a prognostic biomarker of survival and time to cystectomy in muscle invasive bladder cancer (MIBC) following organ conserving treatment. Eur J Cancer, 72, 2017, S192.
83. Hafeez, S., Koh, M., Sohaib, A., Huddart, R., PD-0464: assessing response to chemotherapy with diffusion weighted MRI (DW-MRI) in muscle invasive bladder cancer (MIBC). Radiother Oncol 106:Suppl 2 (2013), S180–S181.
84. Nguyen, H.T., Mortazavi, A., Pohar, K.S., et al. Quantitative assessment of heterogeneity in bladder tumor MRI diffusivity: can response be predicted prior to neoadjuvant chemotherapy?. Bladder Cancer 3 (2017), 237–244.
85. O'Connor, J.P., Aboagye, E.O., Adams, J.E., et al. Imaging biomarker roadmap for cancer studies. Nat Rev Clin Oncol 14 (2017), 169–186.
86. Weinreb, J.C., Barentsz, J.O., Choyke, P.L., et al. PI-RADS Prostate Imaging—Reporting and Data System: 2015, version 2. Eur Urol 69 (2016), 16–40.