Urological Science

REVIEW ARTICLE
Year
: 2018  |  Volume : 29  |  Issue : 6  |  Page : 266--276

Multiparametric magnetic resonance imaging of prostate cancer


Siu-Wan Hung1, Yen-Ting Lin2, Ming-Cheng Liu2,  
1 Department of Radiology, Taichung Veterans General Hospital; Department of Veterinary Medicine, National Chung Hsing University; School of Medical Imaging and Radiological Sciences, Chung Shan Medical University, Taichung, Taiwan
2 Department of Radiology, Taichung Veterans General Hospital, Taichung, Taiwan

Correspondence Address:
Siu-Wan Hung
Department of Radiology, Taichung Veterans General Hospital; Department of Veterinary Medicine, National Chung Hsing University; School of Medical Imaging and Radiological Sciences, Chung Shan Medical University, Taichung
Taiwan

Abstract

As the number of elderly population increase, prostate cancer (CaP) becomes the most common cause of urological cancer of men in Taiwan. Multiparametric MRI (mp-MRI) combines standard pulse sequences and Functional Imaging, is a promising tool for CaP detection. Its role has changed from detection to preoperative staging. A consensus scoring system, PI-RAD™, is developed for interpretation and reporting.



How to cite this article:
Hung SW, Lin YT, Liu MC. Multiparametric magnetic resonance imaging of prostate cancer.Urol Sci 2018;29:266-276


How to cite this URL:
Hung SW, Lin YT, Liu MC. Multiparametric magnetic resonance imaging of prostate cancer. Urol Sci [serial online] 2018 [cited 2022 Sep 26 ];29:266-276
Available from: https://www.e-urol-sci.com/text.asp?2018/29/6/266/237604


Full Text

 Introduction



As the number of elderly population increases, prostate cancer (CaP) becomes the most common cause of urologic cancer in men in Taiwan.[1],[2] Although the incidence of CaP in Asian-Pacific countries is lower than Western countries.[3] Its annual incidence has increased over the last three decades. From 1980 to 2013, standardized incidence and mortality rates (per million population) are increasing from 2.57–29.22 to 1.88–6.52 [Figure 1].[1] This may be due to new developing techniques and modalities for screening and diagnosis of CaP.{Figure 1}

 Diagnostic Tools of Prostate Cancer



Urologists use prostatic-specific antigen (PSA) for screening and monitoring CaP. However, PSA is not a cancer-specific marker. It has the lead time or overdiagnosis bias for early detection of CaP. Urologists also use digital rectum examination (DRE) for the diagnosis of CaP. Combine using PSA and DRE may improve the early diagnostic rate in men with low PSA level. With elevated PSA or/with abnormal DRE, urologists use transrectal ultrasound (TRUS) for assessment of the prostate size and guidance for biopsy. Pathologists category different histopathological findings of CaP into Gleason score. We then use risk stratification to provide care decisions and a better allocation of resources to manage localized CaP base on PSA elevation, DRE stage, and Gleason score. We divide localized CaP into three groups: (a) Low-risk: PSA <10 ng/mL, and Gleason score ≤6, and clinical stage T1-T2a; (b) intermediate-risk: PSA 10–20 ng/mL, or biopsy Gleason score 7, or clinical stage T2b or T2c; and (c) high-risk: PSA >20 ng/mL, or Gleason score 8–10, or clinical stage >T2c.[4] Computed tomography (CT) is poor in soft-tissue resolution and no good at the prostatic zonal definition. Therefore, CT is not used for initial CaP evaluation. However, CT is good for the wide range of coverage. We use CT for preoperative staging and organs metastasis. Steyn and Smith used magnetic resonance imaging (MRI) for CaP detection after 1982.[5] Since DRE and TRUS biopsy have their own limitations,[6],[7] the role of MRI is used for localization and preoperative staging of a patient with biopsy-proven CaP.

 Morphological Imaging



Conventional MRI pulse sequences including T1-weighted imaging (T1WI) and T2-weighted imaging (T2WI). With their high spatial resolution, they highlight the zonal anatomy of the prostate gland. After Hricak et al.,[8] we divide prostate into four regions: The central zone (CZ), transition zone (TZ), peripheral zone (PZ), and fibromuscular zone (FMZ) [Figure 2]. They are just like a baseball glove holding a baseball. We combined the CZ and TZ to call it as central gland (CG, the baseball).[9] The CZ locates at the base of prostate just superoposteriorly to the proximal urethra. It surrounds the ejaculatory ducts from the prostatic base to verumontanum where ejaculatory ducts enter the urethra [Figure 2]c. In a normal person, the PZ comprises about 70% of the glandular tissue. It is just like a baseball glove running from base to apex of the gland and surrounds the distal urethra.[10] Urologists using DRE to palpate PZ. In T1WI, both CG and PZ are isointense signal intensity (SI). In T2WI, the PZ becomes high in SI where the CG is still iso and heterogeneous SI. The FMZ comprises stromal tissue has low SI on both T1WI and T2WI. T2WI depicts prostatic zonal anatomy and surgical capsule. We consider it as morphology MRI. Untreated CaP shows a mass effect to adjacent normal prostate tissue or surgical capsule invasion. They have homogenous low SI and ill-defined margin, so-called erased charcoal sign on T2WI [Figure 3]. Intraglandular hemorrhage is common in prostate MRI (90%–95%).[11] We found over 81.5% of hemorrhage in the PZ of the prostate (range 7–58 days, not published data in our center). Prostate hemorrhage is present with high SI, without or with fat suppression T1WI, so we use T1WI to look for postbiopsy hemorrhage in the prostate. However, hemorrhage has a low SI on T2WI. Therefore, it affects the staging interpretation of CaP in T2WI [Figure 4]. We recommend the optimal timing to get a post-biopsy prostate MRI to be at least over 6-8 weeks.[1],[9]{Figure 2}{Figure 3}{Figure 4}

 Functional Magnetic Resonance Imaging



TRUS biopsy[7] and DRE[6] have their limitations in CaP diagnosis. As the development of functional and metabolic techniques, the role of MRI is no more only for detection and localization of CaP. In a high-risk patient with a negative biopsy, MRI acts as a guidance for repeated TRUS biopsy. MRI is also used for follow-up on postprostatectomy and active surveillance on the result of treatment.[12] We are now using multiparametric MRI (mp-MRI) for diagnosis of CaP. mp-MRI consists of Morphology MRI (T2WI) and two or more other modern functional MRI sequences. They include MR spectroscopic imaging (MRSI), dynamic contrasted-enhanced (DCE)-MRI, and diffusion-weighted imaging (DWI). MRSI measures metabolites concentrations. DCE-MRI presents angiogenesis and DWI reflects cell density within the prostate. mp-MRI using different protocols according to a patient's risk of tumor spreading, the severity of abnormal PSA, clinical stage, and Gleason score.[4]

 Magnetic Resonance Spectroscopic Imaging



MRSI is a promising tool and can provide biochemical information of cellular metabolites. CaP tissue reduces the area of the cell lumen and increases nuclei. Such morphology changing shows relating to primary Gleason score pattern.[13] As a result, cellular metabolites such as choline (Cho), creatine (Cr), citrate (Cit), and spermine (Spm) will change.

We measure the metabolite ratio of Cho/(Cr + Spm) or (Cho + Cr)/Cit in CaP. These ratios show positively correlating with the percentage area of nuclei lesion[14] and Gleason score[15] [Figure 3]. However, MRSI requires endorectal coil (ERC) on 1.5T MRI scanner.[16] It is easily affected by homogenous electromagnetic field,[17] requires additional software expertise, training, support, and time-consuming.[18],[19] One study on “MRSI and accuracy of 3T mp-MRI” shows that MRSI failure to provide added value for sextant localization of CaP.[20] These make both urologists and radiologists drawback to MRSI usage. Therefore, the published guidelines of ACR have omitted its routine usage.[9]

 Dynamic Contrast-Enhanced Magnetic Resonance Imaging



CaP pronounced angiogenesis because of vascular growth factors secretion induced by local hypoxia or lack of nutrients during tumor progression. The neogrowth vessels with defects or pores in the endothelial wall have higher permeability and causing leakage of small molecules to extracellular space. DCE-MRI needs a rapid acquisition lesser than 15s per acquisition. By injecting low molecular weight contrast media and using this rapid acquisition pulse sequence, CaP has a pattern of an earlier peak of enhancement (wash-in) and rapid washout of contrast agent than those of the normal surrounding tissue.[21] This special enhancing pattern (DCE I/O) presents three kinds of curve form, types I, II, and III [Figure 5]. These curves relate to the aggressiveness of CaP. By looking for these curves, DCE-MRI can also help to monitor treatment effects.[22] In one recent study on the current role of mp-MRI shows that DEC is less used than other functional techniques.[23] However, DCE-MRI is most helpful when the T2W-MRI and DWI are equivocal[24] [Figure 6].{Figure 5}{Figure 6}

 Diffusion-Weighted Imaging



CaP tissue increases the cell density and shows a significant positive association with the percentage area of a lumen, the lumen-to-nuclei ratio,[14] and tumor Gleason score at final pathology.[25] DWI is one of the functional MRI methods that work based on water molecules movements within a tissue. Therefore, DWI is enabling qualitative and quantitative assessment of CaP aggressiveness. DWI uses apparent diffusion coefficient (ADC) value to reflect cell density within the prostate tissue. Increases the cell density will cause water restriction at diffusion study and reduces ADC value. CaP shows a higher SI on DWI and a lower ADC value as compared with normal prostatic tissue [Figure 7].[26]{Figure 7}

 Staging of Prostate Cancer



Early detection or organ-confined CaP is curable. Local staging of CaP is important for differentiating organ-confined (stage T1 or T2) from early advanced disease with extraprostatic extension (EPE) or seminal vesicle invasion (Stage T3). Urologists also require exact localization of cancer for appropriate treatments. These choices of treatment include prostatectomy, minimally invasive therapy for organ-confined cases, and hormone ablation or radiation therapy for advanced extraprostatic-extended cases.[27] Minimally invasive treatments include cryoablation, radiofrequency ablation, brachytherapy, photodynamic therapy, or high-intensity focused ultrasonography. A 1.5T MRI image acquisition needs to use an ERC-combined pelvic phased-array coil to get high-quality images of the prostate. A 3T MRI scanner may have the benefits of better signal-to-noise ratio, a shorter time for acquisition and without the use of ERC.[28]

With advanced MRI techniques, mp-MRI is considered the best imaging tools for detection of multiple foci CaP. It is more accurate in differentiation between Stage T2 and T3 CaP than other imaging modalities. Its higher accuracy rate may let the urologists have a well preoperative planning to consider a nerve-sparing option. This may decrease the morbidities associated with radical prostatectomy (RRP). The stage distribution of CaP in Taiwan from 2004 to 2012 is: Stage 2 is 40%, Stage 3 is 11%, and Stage 4 is 29%.[1],[2] An equal portion of cases is between <= Stage 2 and >= Stage 3. This makes radiologists of Taiwan even more concern on specificity and sensitivity of mp-MRI for local staging of CaP. A meta-analysis report (2014) shows that mp-MRI has a specificity of 0.88 and a sensitivity of 0.74 for CaP detection. Its negative predictive values (NPVs) ranging from 0.65 to 0.94.[29] Another recent document reports that mp-MRI has an NPV and specificity of 93% and 90% on EPE detection. MRI can also predict index lesion (P = 0.012).[30]

There are multiple MRI findings for a diagnosis of EPE in CaP. They include broad capsular tumor contact (>10 mm) [Figure 8], contour deformity or retraction [Figure 9] and [Figure 10], focal capsular thickening or irregular and/or bulging of outer margin, direct extension of the tumor beyond the capsule [Figure 9], obliteration of the rectoprostatic angle [Figure 8], asymmetry of the neurovascular bundle [Figure 9], and change of seminal vesicles such as focal decrease in SI, T2 hypointense with enlarged seminal vesicle or ejaculatory duct or direct tumor extension from the prostatic base [Figure 8].[27]{Figure 8}{Figure 9}{Figure 10}

 Differentiation and Mimicking Lesions



mp-MRI combines morphologic and functional techniques. This gives promising accuracy in diagnosis, localization, risk stratification, and staging of significant CaP. Typical untreated CaP of mp-MRI as mentioned before has a lenticular appearance in CG, with mass effect to adjacent normal prostate tissue and/or surgical capsule in PZ. They are predominant to have homogenous low SI ill-defined (erased charcoal sign) and without capsule in T2WI in CG. They have diffusion restriction in DWI, asymmetric rapid DCE I/O, and increase Cho peak in MRSI [Figure 3] and [Figure 7].

The intrinsic prostate tissue composition[31],[32] and aggressiveness of CaP may affect the signal characteristics among different parameters of mp-MRI[31],[32],[33] [Figure 10]. Some literature reported missing or undetected CaP in MRI studies. Tan et al. reported that 53.3% missing CaP nodules in their 3T MRI studies. There has a higher sensitivity for lesion ≥1 cm and those missing lesions are likely to be low risk (75.2%, Gleason score of 6).[34],[35] One report on using b = 2000 s/mm2 DWI at 3T may even detect high-grade CaP in size of >5 mm[36] [Figure 11]. The missing detection rate is higher in the apex lesions.[34],[37],[38],[39] Urologists usually use DCE for following up treatment of CaP after RRP or radiation. A local recurrent CaP in RRP is a focal nodule adjacent musculature or crescentic subcapsular focus after radiation with losing zonal anatomy. It shows diffuse low SI but with higher SI than radiation patient in T2WI. It also presents diffusion restriction in DWI, gives early rapid washin and washout contrast in a DCE study and increased Cho peak in MRSI[40],[41] [Figure 12] and [Figure 13].{Figure 11}{Figure 12}{Figure 13}

The operative site is common to have a fibrotic scar and has a low SI in T2WI that mimics recurrence CaP. However, fibrotic scar shows no or delayed enhancement on contrast injection.[42],[43] Sometimes, subtraction MRI imaging technique may be helpful in case of equivocal findings between mp-MRI images.

In DWI, there are many benign entities that may show diffusion restriction and mimicking CaP.[44] DWI is using SE sequence for acquisition. Therefore, the SI of the study tissue depends on both the T2 signal and signal attenuation in between the two lobe gradients that are being applied. In lesions with a very long T2 relaxation time, such T2 effects may produce a high signal even using high b values in acquisitions. It will cause a wrong interpretation of diffusion restriction. We call it as T2 shine-through effect.[39],[45] If a tissue has a very short T2 relaxation time, complete loss of the signal may have indifferent to what b value is being promoted. We call this effect as T2 dark-through or blackout effect.[46] Many entities confound the detection or interpretation of mp-MRI on CaP.[38],[39] They include anterior hypertrophic fibromuscular stroma, chronic and granulomatous prostatitis, hypertrophic nodule or normal displaced of CG, focal changes after radiation, focal areas of atrophy, necrosis or calcification, hemorrhage or pseudolesion at the midline of PZ, surgical capsule, prominent periprostatic venous plexus, and ejaculatory ducts between seminal vesicles.[40],[42],[44],[47] We will discuss some of them in the following paragraph and summarize others in [Table 1].[37],[38],[39],[42],[47]{Table 1}

Benign prostatic hyperplasia (BPH) is usually present in a round or oval shape nodule with well-defined margin in MRI. It is commonly found in the TZ. They show heterogeneous and various SI appearance in T2WI according to their compositions of glandular and stromal tissue. The stromal BPH nodules may mimic TZ cancer that may show low SI on T2WI, diffusion restriction in DWI, early enhancement on DCE images and elevated choline peaks in MRSI. However, they are rounded in appearance and have a more well-defined low SI “capsule” in T2WI and have symmetric rapid contrast wash-in and wash-out at DCE. Sometimes, a stromal nodule presents in PZ and often with normal prostate tissue between the nodule and the surgical capsule[38],[40],[47] [Figure 14] and [Figure 15].{Figure 14}{Figure 15}

Chronic prostatitis appears ill-defined margin, band-like or wedge-shaped in morphology. It is not common to have contour deformity or mass effect on the adjacent normal prostate tissue or surgical capsule as seen with CaP. They are less to have low SI at T2WI and do not have elevated choline or decreased citrate in MRSI. It has only mild diffusion restriction on the ADC map but might have symmetric rapid contrast wash-in and wash-out at DCE[40],[42],[44],[47],[48] [Figure 11], [Figure 14] and [Figure 15]. Granulomatous prostatitis is more common to have a large area of nonenhancement due to necrosis. Sometimes, a low ADC value together with a low DCE score may suggest granulomatous prostatitis rather than CaP.[49]

 Prostate Imaging Reporting and Data System



The accuracy of morphologic MRI for detection, localization, and characterization of CaP is high. Although the mp-MRI is a promising tool in the diagnosis of CaP, its usefulness in clinical practice is not established. There are discrepancy and inconsistency between the conduct, interpretation, and reporting of prostate mp-MRI. A group of multidisciplinary experts considers improving MRI techniques for CaP diagnosis. A formal consensus on the above discrepancy and inconsistency was developed. In response to increasing the quality and diagnostic value of prostate MRI, the ESUR published the first version of the prostate imaging reporting and data system (PI-RADS™) in early 2011.[4]

The PI-RADS™ v1 counts on a Likert-like five-grade scaling systems on each of the MRI parameters. It gives each suspected lesion an overall score including T2W, DWI, and DCE ranged between 3 and 15 to predict the chance of being a clinically significant CaP. The score >9 is rated positively for malignancy independent of the zonal location of the lesion.

In 2014, to make PI-RADS™ standardization and more globally acceptable, a joint steering committee has formed by the AdMeTech Foundation. The ACR and the ESUR released an updated version of PI-RADS™ v2 to overcome limitations of PI-RADS™ v1.[9],[50],[51] PI-RADS™ v2 improves detection, localization, characterization, and risk stratification in patients with suspected cancer in treatment naïve prostate glands. PI-RADS™ v2 uses a 5-point scale based on the likelihood (probability) for each lesion in the prostate gland. It combines mp-MRI findings on T2W, DWI, and DCE correlates with “the presence of a clinically significant cancer.”

PI-RADS™ v2 categories into PIRADS-1: Very low (clinically significant cancer is highly unlikely to be present), PIRADS-2: Low (clinically significant cancer is unlikely to be present), PIRADS-3: Intermediate (the presence of clinically significant cancer is equivocal), PIRADS-4: High (clinically significant cancer is likely to be present), and PIRADS-5: Very high clinically significant cancer is highly likely to be present). The timing of MRI following prostate biopsy is addressed to at least 6 weeks or longer for a staging patient. Recent PSA level, DRE findings, biopsy results, Gleason scores, and medications of hormones should be available to the radiologist at the time of MRI examination performance and interpretation.

As compared to PI-RADS™ v1, PI-RADS™ v2 proposes just one protocol for MRI of the prostate without separate parameters offered. PI-RADS™ v2 considering the location and the size (should be ≥0.5 cc) of a lesion at T2WI and DWI. Then, using the dichotomized score (positive or negative) for DCE findings. We use a specific sequence for point scoring depending on the zonal location of the evaluated lesion. The PZ lesion will use DWI, whereas TZ lesion will use T2WI for assessment. Index lesion should be identified and the EPE should be the first priority to be addressed. The highest RADS™ v2 Assessment Categories are the second consideration criteria. A final 5-point score for each lesion is assigned to the decision process. As CaP is usually multifocal, in PI-RADS™ v2, only the four highest PIRADS score will be reported. There is also have a strong recommendation that the imaging plane angle, location, and section thickness (3 mm) are identical for all sequences.[50],[51],[52] A sector map is recommended to use for defined localization in a report in case of extreme changing prostate anatomy in CaP [Figure 16].[50] A report on using PI-RADS™ v2 reveal very excellent interreader agreement (0.85). Using PI-RADS v2 may help preoperatively diagnose on the clinically significant CaP.[53] Another report shows that general body radiologists and prostate specialists can detect high-grade index CaP lesions with high sensitivity (79% to 90%) and agreement (88% to 95%).[54]{Figure 16}

 Future Role of mp-MRI



The RADS™ v2 has removed the MRSI and reduced the role of DCE in PIRADS assessment category. DCE has a limitation in specificity. For cost-down consideration, expertise pointed out that biparametric MRI (bp-MRI: T2WI + DWI) may be the next coming modified edition for PI-RADS™ v2. Our experience considers that DWI is the dominant sequence in intermediate- or high-risk CaP detection[33] both in CG and PZ.[55],[56] The recent reports show that the overall accuracy of CaP detection in bp-MRI was 79%.[57] The combined usage of bp-MRI and PSA or PSA density resulted in improved accuracy for detecting clinically significant CaP.[58]

mp-MRI is a promising noninvasive imaging tool for CaP screening. It helps detect primary cancer, recurrent cancer, localize, and staging a locally advanced disease. It has high accuracy and reliability in the diagnosis of index CaP lesion. RADS™ v2 considered that the detection of index lesion is important,[50] for it may change further CaP management pathway to focal therapy.[59]

Other research tools are also working for CaP detection. They are MRI-guided biopsy, MRSI at 7T, diffusion tensor imaging, diffusional kurtosis imaging, multiple b value assessments of fractional ADC, intravoxel incoherent motion, blood oxygenation level dependent imaging, intravenous ultra-small superparamagnetic iron oxide agents, and MR-positron emission tomography. With the advancement and adding usage of these novel tools, it may further improve the clinical practice of CaP treatment in the coming future.[50]

Declaration of patient consent

The authors certify that they have obtained all appropriate patient consent forms. In the form the patient(s) has/have given his/her/their consent for his/her/their images and other clinical information to be reported in the journal. The patients understand that their names and initials will not be published and due efforts will be made to conceal their identity, but anonymity cannot be guaranteed.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.

References

1Registry TC. Cancer Registry Information System of Health Promotion Administration in Taiwan; 2016. Available from: https://iiqsw.mohw.gov.tw/olap/pivot.aspx?TID=FB1CD658AE193736&MTID=7A44D15FB9355B34&strGuid=06acf6ae-6269-4203-90e4-e3c90b23c067.
2Hung CF, Yang CK, Ou YC. Urologic cancer in Taiwan. Jpn J Clin Oncol 2016;46:605-9.
3Baade PD, Youlden DR, Cramb SM, Dunn J, Gardiner RA. Epidemiology of prostate cancer in the Asia-Pacific region. Prostate Int 2013;1:47-58.
4Barentsz JO, Richenberg J, Clements R, Choyke P, Verma S, Villeirs G, et al. ESUR prostate MR guidelines 2012. Eur Radiol 2012;22:746-57.
5Steyn JH, Smith FW. Nuclear magnetic resonance imaging of the prostate. Br J Urol 1982;54:726-8.
6Obek C, Louis P, Civantos F, Soloway MS. Comparison of digital rectal examination and biopsy results with the radical prostatectomy specimen. J Urol 1999;161:494-8.
7Presti JC. Prostate biopsy: Current status and limitations. Rev Urol 2007;9:93-8.
8Hricak H, Dooms GC, McNeal JE, Mark AS, Marotti M, Avallone A, et al. MR imaging of the prostate gland: Normal anatomy. AJR Am J Roentgenol 1987;148:51-8.
9Weinreb JC, Barentsz JO, Choyke PL, Cornud F, Haider MA, Macura KJ, et al. PI-RADS prostate imaging - Reporting and data system: 2015, version 2. Eur Urol 2016;69:16-40.
10Bhavsar A, Verma S. Anatomic imaging of the prostate. Biomed Res Int 2014;2014:728539.
11Tamada T, Sone T, Jo Y, Yamamoto A, Yamashita T, Egashira N, et al. Prostate cancer: Relationships between post-biopsy hemorrhage and tumor detectability at MR diagnosis. Radiology 2008;248:531-9.
12Mullerad M, Hricak H, Kuroiwa K, Pucar D, Chen HN, Kattan MW, et al. Comparison of endorectal magnetic resonance imaging, guided prostate biopsy and digital rectal examination in the preoperative anatomical localization of prostate cancer. J Urol 2005;174:2158-63.
13Venkataraman G, Rycyna K, Rabanser A, Heinze G, Baesens BM, Ananthanarayanan V, et al. Morphometric signature differences in nuclei of Gleason pattern 4 areas in Gleason 7 prostate cancer with differing primary grades on needle biopsy. J Urol 2009;181:88-93.
14Kobus T, van der Laak JA, Maas MC, Hambrock T, Bruggink CC, Hulsbergen-van de Kaa CA, et al. Contribution of histopathologic tissue composition to quantitative MR spectroscopy and diffusion-weighted imaging of the prostate. Radiology 2016;278:801-11.
15Wang XZ, Wang B, Gao ZQ, Liu JG, Liu ZQ, Niu QL, et al. 1H-MRSI of prostate cancer: The relationship between metabolite ratio and tumor proliferation. Eur J Radiol 2010;73:345-51.
16Verma S, Rajesh A, Fütterer JJ, Turkbey B, Scheenen TW, Pang Y, et al. Prostate MRI and 3D MR spectroscopy: How we do it. AJR Am J Roentgenol 2010;194:1414-26.
17Nayyar R, Kumar R, Kumar V, Jagannathan NR, Gupta NP, Hemal AK, et al. Magnetic resonance spectroscopic imaging: Current status in the management of prostate cancer. BJU Int 2009;103:1614-20.
18Loffroy R, Chevallier O, Moulin M, Favelier S, Genson PY, Pottecher P, et al. Current role of multiparametric magnetic resonance imaging for prostate cancer. Quant Imaging Med Surg 2015;5:754-64.
19Yoo S, Kim JK, Jeong IG. Multiparametric magnetic resonance imaging for prostate cancer: A review and update for urologists. Korean J Urol 2015;56:487-97.
20Platzek I, Borkowetz A, Toma M, Brauer T, Meissner C, Dietel K, et al. Multiparametric prostate magnetic resonance imaging at 3 T: Failure of magnetic resonance spectroscopy to provide added value. J Comput Assist Tomogr 2015;39:674-80.
21Verma S, Turkbey B, Muradyan N, Rajesh A, Cornud F, Haider MA, et al. Overview of dynamic contrast-enhanced MRI in prostate cancer diagnosis and management. AJR Am J Roentgenol 2012;198:1277-88.
22Ueno Y, Tamada T, Bist V, Reinhold C, Miyake H, Tanaka U, et al. Multiparametric magnetic resonance imaging: Current role in prostate cancer management. Int J Urol 2016;23:550-7.
23Quon J, Kielar AZ, Jain R, Schieda N. Assessing the utilization of functional imaging in multiparametric prostate MRI in routine clinical practice. Clin Radiol 2015;70:373-8.
24Turkbey B, Brown AM, Sankineni S, Wood BJ, Pinto PA, Choyke PL, et al. Multiparametric prostate magnetic resonance imaging in the evaluation of prostate cancer. CA Cancer J Clin 2016;66:326-36.
25Boesen L, Chabanova E, Løgager V, Balslev I, Thomsen HS. Apparent diffusion coefficient ratio correlates significantly with prostate cancer Gleason score at final pathology. J Magn Reson Imaging 2015;42:446-53.
26Tamada T, Sone T, Jo Y, Yamamoto A, Ito K. Diffusion-weighted MRI and its role in prostate cancer. NMR Biomed 2014;27:25-38.
27Bonekamp D, Jacobs MA, El-Khouli R, Stoianovici D, Macura KJ. Advancements in MR imaging of the prostate: From diagnosis to interventions. Radiographics 2011;31:677-703.
28Baur AD, Daqqaq T, Wagner M, Maxeiner A, Huppertz A, Renz D, et al. T2- and diffusion-weighted magnetic resonance imaging at 3T for the detection of prostate cancer with and without endorectal coil: An intraindividual comparison of image quality and diagnostic performance. Eur J Radiol 2016;85:1075-84.
29de Rooij M, Hamoen EH, Fütterer JJ, Barentsz JO, Rovers MM. Accuracy of multiparametric MRI for prostate cancer detection: A meta-analysis. AJR Am J Roentgenol 2014;202:343-51.
30Albisinni S, De Groote A, Deneft F, Thoma P, Catteau X, Roumeguère T, et al. Can preoperative prostate MRI before radical prostatectomy predict extracapsular extension and the side of the index lesion? Prog Urol 2016;26:281-6.
31Hegde JV, Mulkern RV, Panych LP, Fennessy FM, Fedorov A, Maier SE, et al. Multiparametric MRI of prostate cancer: An update on state of the art techniques and their performance in detecting and localizing prostate cancer. J Magn Reson Imaging 2013;37:1035-54.
32Langer DL, van der Kwast TH, Evans AJ, Sun L, Yaffe MJ, Trachtenberg J, et al. Intermixed normal tissue within prostate cancer: Effect on MR imaging measurements of apparent diffusion coefficient and T2 – Sparse versus dense cancers. Radiology 2008;249:900-8.
33Nowak J, Malzahn U, Baur AD, Reichelt U, Franiel T, Hamm B, et al. The value of ADC, T2 signal intensity, and a combination of both parameters to assess Gleason score and primary Gleason grades in patients with known prostate cancer. Acta Radiol 2016;57:107-14.
34Tan N, Margolis DJ, Lu DY, King KG, Huang J, Reiter RE, et al. Characteristics of detected and missed prostate cancer foci on 3-T multiparametric MRI using an endorectal coil correlated with whole-mount thin-section histopathology. AJR Am J Roentgenol 2015;205:W87-92.
35Shimizu T, Nishie A, Ro T, Tajima T, Yamaguchi A, Kono S, et al. Prostate cancer detection: The value of performing an MRI before a biopsy. Acta Radiol 2009;50:1080-8.
36Barral M, Cornud F, Neuzillet Y, Lonchampt E, Lassalle L, Delonchamp NB, et al. Characteristics of undetected prostate cancer on diffusion-weighted MR Imaging at 3-Tesla with a b-value of 2000 s/mm2: Imaging-pathologic correlation. Diagn Interv Imaging 2015;96:923-9.
37Rosenkrantz AB, Verma S, Turkbey B. Prostate cancer: Top places where tumors hide on multiparametric MRI. AJR Am J Roentgenol 2015;204:W449-56.
38Panebianco V, Barchetti F, Barentsz J, Ciardi A, Cornud F, Futterer J, et al. Pitfalls in interpreting mp-MRI of the prostate: A pictorial review with pathologic correlation. Insights Imaging 2015;6:611-30.
39Rosenkrantz AB, Taneja SS. Radiologist, be aware: Ten pitfalls that confound the interpretation of multiparametric prostate MRI. AJR Am J Roentgenol 2014;202:109-20.
40Yu J, Fulcher AS, Turner MA, Cockrell CH, Cote EP, Wallace TJ, et al. Prostate cancer and its mimics at multiparametric prostate MRI. Br J Radiol 2014;87:20130659.
41Li Y, Mongan J, Behr SC, Sud S, Coakley FV, Simko J, et al. Beyond prostate adenocarcinoma: Expanding the differential diagnosis in prostate pathologic conditions. Radiographics 2016;36:1055-75.
42Notley M, Yu J, Fulcher AS, Turner MA, Cockrell CH, Nguyen D, et al. Pictorial review. Diagnosis of recurrent prostate cancer and its mimics at multiparametric prostate MRI. Br J Radiol 2015;88:20150362.
43Oppenheimer DC, Weinberg EP, Hollenberg GM, Meyers SP. Multiparametric magnetic resonance imaging of recurrent prostate cancer. J Clin Imaging Sci 2016;6:18.
44Bhowmik NM, Yu J, Fulcher AS, Turner MA. Benign causes of diffusion restriction foci in the peripheral zone of the prostate: Diagnosis and differential diagnosis. Abdom Radiol (NY) 2016;41:910-8.
45Malayeri AA, El Khouli RH, Zaheer A, Jacobs MA, Corona-Villalobos CP, Kamel IR, et al. Principles and applications of diffusion-weighted imaging in cancer detection, staging, and treatment follow-up. Radiographics 2011;31:1773-91.
46Andreou A, Whitten C, MacVicar D, Fisher C, Sohaib A. Imaging appearance of sarcomas of the prostate. Cancer Imaging 2013;13:228-37.
47Kitzing YX, Prando A, Varol C, Karczmar GS, Maclean F, Oto A, et al. Benign conditions that mimic prostate carcinoma: MR imaging features with histopathologic correlation. Radiographics 2016;36:162-75.
48Meier-Schroers M, Kukuk G, Wolter K, Decker G, Fischer S, Marx C, et al. Differentiation of prostatitis and prostate cancer using the prostate imaging-reporting and data system (PI-RADS). Eur J Radiol 2016;85:1304-11.
49Bour L, Schull A, Delongchamps NB, Beuvon F, Muradyan N, Legmann P, et al. Multiparametric MRI features of granulomatous prostatitis and tubercular prostate abscess. Diagn Interv Imaging 2013;94:84-90.
50Radiology ACo: PI-RADS V2. 2015. Available from: https://www.acr.org/-/media/ACR/Files/RADS/Pi-RADS/PIRADS-V2.pdf.
51Polanec S, Helbich TH, Bickel H, Pinker-Domenig K, Georg D, Shariat SF, et al. Head-to-head comparison of PI-RADS v2 and PI-RADS v1. Eur J Radiol 2016;85:1125-31.
52Barrett T, Turkbey B, Choyke PL: PI-RADS version 2: What you need to know. Clin Radiol 2015, 70:1165-76.
53Park SY, Jung DC, Oh YT, Cho NH, Choi YD, Rha KH, et al. Prostate cancer: PI-RADS version 2 helps preoperatively predict clinically significant cancers. Radiology 2016;280:108-16.
54Greer MD, Brown AM, Shih JH, Summers RM, Marko J, Law YM, et al. Accuracy and agreement of PIRADSv2 for prostate cancer mpMRI: A multireader study. J Magn Reson Imaging 2017;45:579-85.
55Scialpi M, Falcone G, Scialpi P, D'Andrea A. Biparametric MRI: A further improvement to PIRADS 2.0? Diagn Interv Radiol 2016;22:297-8.
56Radtke JP, Boxler S, Kuru TH, Wolf MB, Alt CD, Popeneciu IV, et al. Improved detection of anterior fibromuscular stroma and transition zone prostate cancer using biparametric and multiparametric MRI with MRI-targeted biopsy and MRI-US fusion guidance. Prostate Cancer Prostatic Dis 2015;18:288-96.
57Rais-Bahrami S, Siddiqui MM, Vourganti S, Turkbey B, Rastinehad AR, Stamatakis L, et al. Diagnostic value of biparametric magnetic resonance imaging (MRI) as an adjunct to prostate-specific antigen (PSA)-based detection of prostate cancer in men without prior biopsies. BJU Int 2015;115:381-8.
58Fascelli M, Rais-Bahrami S, Sankineni S, Brown AM, George AK, Ho R, et al. Combined biparametric prostate magnetic resonance imaging and prostate-specific antigen in the detection of prostate cancer: A validation study in a biopsy-naive patient population. Urology 2016;88:125-34.
59Marra G, Gontero P, Valerio M. Changing the prostate cancer management pathway: Why focal therapy is a step forward. Arch Esp Urol 2016;69:271-80.