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 Table of Contents  
ORIGINAL ARTICLE
Year : 2022  |  Volume : 8  |  Issue : 1  |  Page : 20

Diagnostic performance of reduced field-of-view diffusion-weighted imaging-targeted biopsy in suspected prostate cancer patients: A comparison with systematic biopsy


Department of Ultrasound, Medical Imaging Center, Affiliated Hospital of Yangzhou University, Yangzhou University, Yangzhou, Jiangsu, China

Date of Submission16-Jan-2022
Date of Decision08-Apr-2022
Date of Acceptance07-May-2022
Date of Web Publication27-Sep-2022

Correspondence Address:
Tingyue Qi
Department of Ultrasound, Medical Imaging Center, Affiliated Hospital of Yangzhou University, Yangzhou University, Yangzhou
China
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/digm.digm_3_22

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  Abstract 


Purpose: To clarify the diagnostic performance of reduced field-of-view (rFOV) diffusion-weighted imaging (DWI) and compare prostate cancer (PCa) detection rates of rFOV DWI-targeted biopsy (rFOV DWI-TB) with systemic biopsy (SB). Materials and Methods: Ninety-eight consecutive patients with suspected PCa (mean prostate-specific antigen [PSA]: 17.85 ng/mL, range, 4–28 ng/mL) were prospectively enrolled in this study. All rFOV DWI data were carried out using PI-RADS V 2.0 assessment category. All patients underwent a 10-core SB and a further 2–4 cores of rFOV DWI-TB. The performance of rFOV DWI was analyzed, and the cancer detection rates between two methods were compared. Results: The sensitivity, specificity, positive predictive value, and negative predictive value for detecting PCa with rFOV DWI were 85.11%, 92.16%, 90.91%, and 87.04%, respectively. Area under curve for rFOV DWI was 0.886. In the digital rectal examination (DRE) normal and PSA ≥ 10 ng/mL subgroups, the PCa detection rates were statistically greater for rFOV DWI-TB than for SB (both P < 0.05). The mean Gleason score of cancers detected by rFOV DWI-TB was significantly higher than that detected by SB (P < 0.05). In addition, the detection rate for rFOV DWI-TB cores was significantly better than for SB cores (P < 0.001). Conclusion: RFOV DWI allowed for good diagnostic performance in patients suspected of PCa. It may be useful for clinically significant PCa detecting.

Keywords: Diffusion-weighted imaging, Magnetic resonance imaging, Prostate cancer, Reduced field of view, Transrectal ultrasonography


How to cite this article:
Qi T, Cao H, Sun H, Du F, Feng H, Rong X, Fan Q, Wang L. Diagnostic performance of reduced field-of-view diffusion-weighted imaging-targeted biopsy in suspected prostate cancer patients: A comparison with systematic biopsy. Digit Med 2022;8:20

How to cite this URL:
Qi T, Cao H, Sun H, Du F, Feng H, Rong X, Fan Q, Wang L. Diagnostic performance of reduced field-of-view diffusion-weighted imaging-targeted biopsy in suspected prostate cancer patients: A comparison with systematic biopsy. Digit Med [serial online] 2022 [cited 2022 Dec 2];8:20. Available from: http://www.digitmedicine.com/text.asp?2022/8/1/20/357208




  Introduction Top


Prostate cancer (PCa) was the most common cancer found in men in the United States in 2019.[1] Similarly, resulting from the widespread use of testing for prostate-specific antigen (PSA), the incidence of PCa has also steadily accelerated in recent years in China. Early diagnosis and staging are crucial for optimal management in attempts to improve the survival rate and the quality of life for PCa patients. In recent years, multiparametric magnetic resonance imaging (mp-MRI) has been widely used in PCa detection,[2],[3],[4] and diffusion-weighted imaging (DWI) has been generally recognized as 1 of the essential techniques in mp-MRI.[5] However, conventional DWI is prone to distortion and other artifacts due to field changes in magnetic susceptibility at the air–tissue boundary;[6] thus, the diagnostic value of DWI can be diminished by these artifacts.

Reduced field-of-view (rFOV) DWI is a recently introduced approach that offers improved image quality for DWI of the prostate with reduced anatomic warping and other artifacts, and several clinical studies have confirmed the ability of rFOV DWI of the prostate to achieve such an anatomic warping reduction with improved image quality.[7],[8],[9] However, to the best of our knowledge, this technique has not been specifically evaluated in the setting of patients with suspected PCa scheduled for transrectal ultrasonography (TRUS)-guided biopsy.

Therefore, patients suspected of PCa were included in this study, and rFOV DWI sequences of all patients' lesions were scored according to PI-RADS V 2.0 scoring criteria. The diagnostic performance of rFOV DWI was evaluated and the cancer detection rate of rFOV DWI-targeted biopsy (rFOV DWI-TB) and systemic biopsy (SB) in TRUS-guided transperineal prostate biopsy was further compared.


  Materials and Methods Top


Patients

This prospective study was approved by our institutional review board, and written informed consent was obtained from all patients. We obtained study data between September 2016 and October 2019. In this prospective, single-center study analysis, a total of 150 consecutive patients undergoing MRI examinations of the prostate prior to TRUS-guided transperineal prostate biopsy for the first time were studied. Inclusion criteria were as follows: (1) MRI examination using rFOV DWI 1 week before biopsy; (2) PSA >4 ng/mL; and (3) no prior history of PCa or other malignancy. Exclusion criteria were (1) MRI examination using conventional DWI; (2) poor image quality; and (3) a combination of other malignant tumors or serious diseases. Ultimately, we enrolled a total of 98 patients in the study.

Magnetic resonance imaging protocol and interpretation

All images were acquired using a 3.0 T MRI unit (Discovery MR750, GE Healthcare, Milwaukee, WI, USA) with a 16-channel, receive-only, phased-array torso coil. We acquired a fast spin-echo (FSE) T1-weighted sequence and, subsequently, an FSE T2-weighted sequence in the transverse and coronal planes. T2-weighted images were acquired with the following scan parameters: repetition time (TR) =3861 ms, echo time (TE) =109 ms, matrix = 256 × 256, FOV = 18 cm × 9 cm, slice thickness (ST) =3 mm, intersection gap = 1 mm, and acceleration factor = 4.

RFOV DWI was performed using two-dimensional single-shot EPI (ss-EPI) with multiple b values (500, 750, and 1000 s/mm2) in all diffusion directions. Imaging parameters were the following: TR = 2500 ms, TE = 73.4 ms, matrix = 256 × 256, FOV = 18 cm × 9 cm, ST = 3 mm, intersection gap = 1 mm, and acceleration factor = 2. The acquisition time for the entire MRI examination ranged from 10 to 15 min. Consequently, we obtained the apparent diffusion coefficient maps on a dedicated workstation (Advantage Windows 4.5, GE Healthcare, Milwaukee, WI, USA).

Two radiologists, one with more than 10 years of experience and the other with 7 years of experience in urogenital radiology, reviewed all the MR sequences including rFOV-DWI together, consensually identified suspicious lesions, and were blinded to the clinical details. We used prostate imaging reporting and data system version 2 (PI-RADS™ V2) scoring for DWI.[10] A PI-RADS score of 1–3 was considered negative, and a PI-RADS score of 4 or 5 was considered positive.

Biopsy protocol and pathologic analysis

Two investigators (with 8 and 5 years of experience in TRUS-guided prostate biopsy, respectively) performed biopsy of the prostate after the MRI examination. A MyLab Twice System (Esaote SpA, Genoa, Italy), with a 3–13 MHz endorectal biplane probe (TRT33), was used transperineally, and we used an 18-G needle for the biopsy. All patients underwent a 10-core SB via the perineum as described in our previous study.[11] The biopsy operator also reviewed the rFOV DWI data, and thus a further 2–4 cores of rFOV DWI-TB were taken from each suspicious lesion using visual registration.[12] Each sample was labeled separately and sent to the pathology laboratory for analysis, and each biopsy core was reviewed by a pathologist and reported as cancer with an assigned Gleason score, or as prostatitis, atrophia, benign prostate hyperplasia (BPH), or normal prostatic tissue.

We defined the area over the urethral plane as the anterior region and the remaining area as the posterior region, as described previously.[13] This definition resulted in four anterior cores and six posterior cores for SB, and each rFOV DWI-TB core was taken according to its actual location and consonant with the urethral plane.

Statistical analysis

We performed statistical analysis using SPSS 22.0 software (SPSS, Chicago, IL, USA) with P < 0.05 considered to be statistically significant. The distribution of qualitative variables was expressed as the relative frequency of the various modalities under observation, while the distribution of quantitative variables was expressed as means ± 1 standard deviation. Differences in parametric data were assessed using the independent samples t-test. Cancer detection rates were compared in the two groups using McNemar's, Fisher's exact, or Wilcoxon rank-sum test. Area under the receiver operating characteristic (ROC) curve (AUC) was calculated to assess the diagnostic efficiency of rFOV DWI. It is important to point out that if one core of SB was located in the target of the rFOV DWI, this core would be counted both in SB and rFOV DWI-TB for analysis.


  Results Top


Patient characteristics

Patient age ranged from 37 to 86 years, with a mean of 68.3 years. The mean PSA level was 17.85 ng/mL, with a range of 4–28 ng/mL; overall, 47 of the 98 patients (47.96%) had histologically confirmed PCa. Clinical characteristics of all patients are summarized [Table 1]. Patients with PCa exhibited significantly greater age, PSA, PSA density, and PSA transition-zone density, and a significantly lower free-to-total PSA ratio compared to patients without PCa (by independent-samples t-test, all P < 0.05). In addition, we observed no significant difference in free PSA between the two groups (independent-sample t-test, P > 0.05).
Table 1: Patient characteristics.

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Diagnostic performance of reduced field-of-view diffusion-weighted imaging

Overall, 30, 18, 6, 33, and 11 patients had scores of 1, 2, 3, 4, and 5 on PI-RADS scoring for rFOV DWI, respectively. In patients with a score of 1-5-2, 2, 3, 29, and 11 patients were confirmed to have PCa by rFOV DWI-TB, respectively [Figure 1]. The sensitivity, specificity, positive predictive value (PPV), and negative predictive value (NPV) for detecting PCa with rFOV DWI were 85.11% (40/47), 92.16% (47/51), 90.91% (40/44), and 87.04% (47/54), respectively. ROC curve analysis revealed an AUC for rFOV DWI of 0.886 [Figure 2].
Figure 1: Patient with a PI-RADS score of 5 on rFOV DWI. 65 years, PSA 15.6 ng/mL. (a) rFOV DWI demonstrated a markedly hyperintense area in anterior region of the prostate (white arrow); (b) ADC map showed a focal markedly hypointense area with a maximum diameter of 21 mm (white arrow); (c) TRUS-guided rFOV DWI-TB demonstrated the biopsy site was located in the lesion (white arrow). (d) Pathologic examination revealed Gleason 4 + 3 adenocarcinoma (H and E, ×100). rFOV: Reduced field-of-view, DWI: Diffusion-weighted imaging, PSA: Prostate-specific antigen, ADC: Apparent diffusion coefficient, TRUS-guided: transrectal ultrasonography-guided.

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Figure 2: ROC curve of rFOV DWI. ROC: Receiver operating characteristic, rFOV: Reduced field-of-view, DWI: Diffusion-weighted imaging.

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Patient-based cancer detection rates

Of the 47 patients with PCa, cancers were independently detected by SB and rFOV DWI-TB in seven patients (14.9%) and 13 patients (27.7%), respectively. RFOV DWI-TB identified PCa in 40 of the 98 patients (40.8%), compared with 34 of the 98 patients (34.7%) by SB. A patient-based analysis revealed no statistically significant difference in the overall cancer detection rate between rFOV DWI-TB and SB (using McNemar's test, P > 0.05).

Comparison of cancer detection rates by rFOV DWI-TB and SB between subgroups according to DRE, PSA, and age is shown [Table 2]. By patient, in the DRE normal and PSA ≥ 10 ng/mL subgroups, the PCa detection rates were statistically greater for rFOV DWI-TB than for SB (Pearson Chi-square test, both P < 0.05). There was no significant difference between the two techniques in the age subgroups.
Table 2: Comparison of cancer detection rate by reduced field-of-view diffusion-weighted imaging-targeted biopsy and systemic biopsy between subgroups according to digital rectal examination, prostate-specific antigen and age.

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The Gleason score in the 40 patients as diagnosed by rFOV DWI-TB varied between 6 and 10, and the Gleason score in the 34 patients as diagnosed by SB varied between 5 and 9. The mean Gleason score of cancers detected by rFOV DWI-TB was significantly higher than the score for cancers detected by SB (7.1 vs. 6.8, Wilcoxon rank-sum test, Z = −2.268; P < 0.05) [Table 3]. The detection rate of cancers with Gleason score ≥ 7 by rFOV DWI-TB (63.8% or 30 of 47 patients) was significantly higher than that by SB (36.2% or 17 of 47 patients) (Pearson Chi-square test, P < 0.01).
Table 3: Gleason score distribution.

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Biopsy core-based cancer detection rates

We obtained 1076 cores from 98 patients, 206 of which (19.1%) were found to contain evidence of PCa in the 47 patients. The detection rate for rFOV DWI-TB cores (55.2% or 80 of 145 cores) was significantly better than for SB cores (13.7% or 134 of 980 cores) (Pearson Chi-square test, P < 0.001). However, the cancer core rate in the anterior region of the prostate (18.7% or 83 of 445 cores) was not found to be significantly different (P > 0.05) from that of the posterior region (19.5% or 123 of 631 cores).


  Discussion Top


TRUS-guided prostate biopsy is the current standard for PCa detection. However, due to the difficulty in using TRUS to identify isoechoic PCa lesions or cancers located in the transition zone and the low sensitivity of conventional TRUS-guided prostate biopsy, other imaging-guided biopsy methods have been used in an attempt to increase the cancer detection rate. In addition, previous studies had suggested that TRUS was not used diagnostically but solely to target lesions found on Mp-MRI.[14] For mp-MRI, a key advantage of DWI is that it provides additional insights into the biologic activity of intraprostatic lesions that are not observable with anatomical T2 sequences.[15] However, because the prostate is located near the adjacent air-filled rectum, conventional DWI is prone to distortion and susceptibility artifacts, especially at 3T.[8] Several recent studies[7],[8],[9] have fortunately demonstrated that rFOV DWI technology can overcome these limitations. Compared with conventional DWI, rFOV DWI technology may be more valuable in the diagnosis of prostate diseases. On the one hand, the rFOV-DWI scans are small and narrow, which fits well into a small organ such as the prostate, and on the other hand, the rFOV-DWI scans enable a focused excitation of small field of views, resulting in reduced artifacts in surrounding tissues and reduced distortion in target organ.

In the present study, the sensitivity, specificity, PPV, and NPV for PCa detection with rFOV DWI were 85.11%, 92.16%, 90.91%, and 87.04%, respectively; and the resulting AUC was 0.886. Chen et al.[16] evaluated the diagnostic performance of solely conventional DWI in PCa detection using a meta-analysis that included 21 studies and concluded that conventional DWI had a pooled sensitivity and specificity with a corresponding 95% confidence interval (CI) of 0.62 (95% CI, 0.61–0.64) and 0.90 (95% CI, 0.89–0.90), respectively; the AUC was 0.90. Our results confirmed these findings, with a specificity and AUC of solely conventional DWI similar to those of rFOV DWI (92.16% vs. 90.00% and 0.886 vs. 0.900, respectively); however, in comparison, the sensitivity of rFOV DWI in our study was much higher than that of DWI in previous studies (85.11% vs. 62.00%). Therefore, rFOV DWI improves the PCa detection rate without increasing false-positive rates. However, Brendle et al.[8] published a comparable study with conventional and rFOV DWI and concluded that sensitivity and specificity of rFOV and conventional DWI were not significantly different and that rFOV DWI had a slightly higher AUC compared to conventional DWI (but not significantly different, 0.82 vs. 0.78; P = 0.0576). The Brendel study, however, entailed only 15 patients with 29 histology-proven PCa lesions.

Although our study showed that there was no significant difference in the PCa detection rate by the patient between SB and rFOV DWI-TB, several investigators[17],[18],[19] have concluded that a TRUS-guided TB approach cannot completely replace SB under the present circumstances. In our study, PCa was detected in only 7 (14.9%) patients by SB, and thus, at present, the combination of SB and TB is still the standard scheme to be used in TRUS-guided prostate biopsy. However, one important issue in the present study was that the PCa detection rates were significantly greater for rFOV DWI-TB than for SB in DRE normal and PSA ≥10 ng/mL subgroups. This suggests that rFOV DWI is beneficial in the detection of cancers not located in the peripheral zone.

Another important issue is the detection of PCa with clinical significance. Clinically significant cancer is surgically defined as having a Gleason score of 7 or greater, tumor volume of 0.5 cm3 or greater, or tumor category T3 or greater;[20] this definition is also used to detect clinically significant cancer with PI-RADS V2.[10] In the present study, the Gleason score in the 40 patients diagnosed by rFOV DWI-TB (range, 6–10) was significantly greater than in the 34 patients diagnosed by SB (range, 5–9), with means of 7.1 and 6.8, respectively (P < 0.05). More importantly, the detection rate of cancers with Gleason score ≥ 7 by rFOV DWI-TB (63.8%) was significantly higher than that by SB (36.2%) (P < 0.01). Thus, it appears that with respect to determining the treatment plan, rFOV DWI may have utility in providing an accurate preoperative awareness of the Gleason score or the presence of clinically significant cancer.

In the present study, the detection rate for rFOV DWI-TB cores was significantly better than for SB cores (55.2% vs. 13.7%, respectively; P < 0.001). However, we found no significant difference in the detection rates for the anterior and posterior zones (18.7% vs. 19.5%, respectively; P > 0.05). Furuno et al.[13] used extensive transperineal ultrasound-guided template prostate biopsy and also reported the cancer core rate in the anterior region (18.7%) was not different from that in the posterior region (8.6%) (P = 0.7111) in 86 men without previous biopsy history and with PSA levels between 4.0 and 10.0 ng/mL. Our results therefore further confirmed these investigators' findings.

Our study did have some limitations. First, diagnosis and histologic grading of PCa were not achieved using whole-mount radical prostatectomy specimens. Second, we used visual registration for TRUS-guided rFOV DWI-TB in our study, and this procedure may influence the accuracy of TB, although the real-time TRUS/MRI fusion prostate biopsy system may overcome this limitation in future studies. The final limitation of our study was that the sample size was inadequate, such that a prospective study based on a larger sample size is needed to confirm our findings in the future.


  Conclusion Top


rFOV DWI allowed for good diagnostic performance in patients suspected of PCa. Moreover, compared with SB, rFOV DWI-TB not only significantly improved PCa detection rates in subgroups of normal DRE or PSA ≥ 10 ng/mL but also detected more clinically significant cancers. These initial results should be validated by subsequent future studies on larger patient groups.

Statement of ethics

All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki Declaration and its later amendments or comparable ethical standards. Informed consent was obtained from all individual participants included in the study.

Acknowledgments

Nil.

Financial support and sponsorship

This study was supported by the Instructional Research Project of Jiangsu Commission of Health (Z2019046) and the Key Research and Development Foundation of Yangzhou Science and Technology Bureau (Grant No.YZ2020099).

Conflicts of interest

There are no conflicts of interest.



 
  References Top

1.
Siegel RL, Miller KD, Fuchs HE, Jemal A. Cancer statistics, 2022. CA Cancer J Clin 2022;72:7-33.  Back to cited text no. 1
    
2.
Costa DN. Multiparametric MRI of the prostate: Beyond cancer detection and staging. Radiology 2021;299:624-5.  Back to cited text no. 2
    
3.
Kowa JY, Soneji N, Sohaib SA, Mayer E, Hazell S, Butterfield N, et al. Detection and staging of radio-recurrent prostate cancer using multiparametric MRI. Br J Radiol 2021;94:20201423.  Back to cited text no. 3
    
4.
Rouvière O, Puech P, Renard-Penna R, Claudon M, Roy C, Mège-Lechevallier F, et al. Use of prostate systematic and targeted biopsy on the basis of multiparametric MRI in biopsy-naive patients (MRI-FIRST): A prospective, multicentre, paired diagnostic study. Lancet Oncol 2019;20:100-9.  Back to cited text no. 4
    
5.
Tamada T, Ueda Y, Ueno Y, Kojima Y, Kido A, Yamamoto A. Diffusion-weighted imaging in prostate cancer. Magn Reson Mater Phy 2022;35:533-47.  Back to cited text no. 5
    
6.
Stocker D, Manoliu A, Becker AS, Barth BK, Nanz D, Klarhöfer M, et al. Image quality and geometric distortion of modern diffusion-weighted imaging sequences in magnetic resonance imaging of the prostate. Invest Radiol 2018;53:200-6.  Back to cited text no. 6
    
7.
Rosenkrantz AB, Taneja SS. Use of reduced field-of-view acquisition to improve prostate cancer visualization on diffusion-weighted magnetic resonance imaging in the presence of hip implants: Report of 2 cases. Curr Probl Diagn Radiol 2018;47:125-7.  Back to cited text no. 7
    
8.
Brendle C, Martirosian P, Schwenzer NF, Kaufmann S, Kruck S, Kramer U, et al. Diffusion-weighted imaging in the assessment of prostate cancer: Comparison of zoomed imaging and conventional technique. Eur J Radiol 2016;85:893-900.  Back to cited text no. 8
    
9.
Korn N, Kurhanewicz J, Banerjee S, Starobinets O, Saritas E, Noworolski S. Reduced-FOV excitation decreases susceptibility artifact in diffusion-weighted MRI with endorectal coil for prostate cancer detection. Magn Reson Imaging 2015;33:56-62.  Back to cited text no. 9
    
10.
Weinreb 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.  Back to cited text no. 10
    
11.
Qi TY, Sun HG, Li NF, Feng H, Ding YL, Wang XX. Value of three-section contrast-enhanced transrectal ultrasonography in the detection of prostate cancer. J Clin Ultrasound 2017;45:304-9.  Back to cited text no. 11
    
12.
Moore CM, Kasivisvanathan V, Eggener S, Emberton M, Fütterer JJ, Gill IS, et al. Standards of reporting for MRI-targeted biopsy studies (START) of the prostate: Recommendations from an International Working Group. Eur Urol 2013;64:544-52.  Back to cited text no. 12
    
13.
Furuno T, Demura T, Kaneta T, Gotoda H, Muraoka S, Sato T, et al. Difference of cancer core distribution between first and repeat biopsy: In patients diagnosed by extensive transperineal ultrasound guided template prostate biopsy. Prostate 2004;58:76-81.  Back to cited text no. 13
    
14.
Rosoff JS, Prasad SM, Savage SJ. Ultrasonography in prostate cancer: Current roles and potential applications in radiorecurrent disease. World J Urol 2013;31:1353-9.  Back to cited text no. 14
    
15.
Moghanaki D, Turkbey B, Vapiwala N, Ehdaie B, Frank SJ, McLaughlin PW, et al. Advances in prostate cancer magnetic resonance imaging and positron emission tomography-computed tomography for staging and radiotherapy treatment planning. Semin Radiat Oncol 2017;27:21-33.  Back to cited text no. 15
    
16.
Chen J, Liu RB, Tan P. The value of diffusion-weighted imaging in the detection of prostate cancer: A meta-analysis. Eur Radiol 2014;24:1929-41.  Back to cited text no. 16
    
17.
Kratzenberg J, Salomon G, Tennstedt P, Dell'Oglio P, Tilki D, Haferkamp A, et al. Prostate cancer rates in patients with initially negative elastography-targeted biopsy vs. systematic biopsy. World J Urol 2018;36:623-8.  Back to cited text no. 17
    
18.
Albisinni S, Aoun F, Noel A, El Rassy E, Lemort M, Paesmans M, et al. Are concurrent systematic cores needed at the time of targeted biopsy in patients with prior negative prostate biopsies? Prog Urol 2018;28:18-24.  Back to cited text no. 18
    
19.
Fulco A, Chiaradia F, Ascalone L, Andracchio V, Greco A, Cappa M, et al. Multiparametric magnetic resonance imaging-ultrasound fusion transperineal prostate biopsy: Diagnostic accuracy from a single center retrospective study. Cancers (Basel) 2021;13:4833.  Back to cited text no. 19
    
20.
Ploussard G, Epstein JI, Montironi R, Carroll PR, Wirth M, Grimm MO, et al. The contemporary concept of significant versus insignificant prostate cancer. Eur Urol 2011;60:291-303.  Back to cited text no. 20
    


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