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ORIGINAL ARTICLE
Year : 2021  |  Volume : 17  |  Issue : 2  |  Page : 372-378

Can combined multiparametric magnetic resonance imaging of the prostate and prostate-specific antigen density improve the detection of clinically significant prostate cancer: A prospective single-center cross-sectional study


1 Department of Diagnostic and Interventional Radiology, All India Institute of Medical Sciences, Jodhpur, Rajasthan, India
2 Department of Pathology and Lab Medicine, All India Institute of Medical Sciences, Jodhpur, Rajasthan, India
3 Department of Urology, All India Institute of Medical Sciences, Jodhpur, Rajasthan, India

Date of Submission24-Feb-2020
Date of Decision30-May-2020
Date of Acceptance12-Aug-2020
Date of Web Publication28-May-2021

Correspondence Address:
Binit Sureka
Department of Diagnostic and Interventional Radiology, All India Institute of Medical Sciences, Jodhpur - 342 005, Rajasthan
India
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/jcrt.JCRT_216_20

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 > Abstract 


Objective: The objective of the study was to validate PIRADS v2 on 3T MRI with secondary assessment if combination of the PIRADS v2 and PSA density improves detection of clinically significant prostate cancer.
Materials and Methods: We conducted a prospective study evaluating 58 patients with PSA value of >4 ng/ml from July 2017 to December 2019. Transrectal ultrasonography (TRUS) guided targeted biopsy was performed via cognitive targeting followed by systemic 12 core biopsy. Two cognitive fusion-targeted biopsy cores were added for each lesion in patients who had suspicious or equivocal lesions on mpMRI. The PI-RADS scoring system version 2.0 (PI-RADS v2) was used to describe the MRI findings.
Results: Total of 112 lesions of 58 patients were assessed via mpMRI followed by TRUS guided biopsy. A PI-RADS v2 score of ≥4 irrespective of PSA density categories and a PI-RADS v2 score of 3 with PSA density of ≥0.15 ng/mL/cc, yielded the highest overall prostate cancer and clinically significant prostate cancer detection rate. Contrary to, a PI-RADS v2 score of ≤3 and a PSA densitay of <0.15 ng/ mL/mL(low risk group), which yielded no clinically significant prostate cancer.
Conclusion: Both PIRADS v2 score and PSA density are eminently sensitive and specific in the detection of clinically significant prostate cancers individually. However the combination of PIRADS v2 and PSA density significantly improved the accuracy of clinically significant prostate cancer detection. Patients with combination of PIRADS v2 score 33 and PSA density 30.15 ng/ml/cc should undergo prostate biopsy.

Keywords: PIRADS, prostate-specific antigen, prostate-specific antigen density, prostate


How to cite this article:
Yadav K, Sureka B, Elhence P, Choudhary GR, Pandey H, Garg PK, Yadav T, Khera PS. Can combined multiparametric magnetic resonance imaging of the prostate and prostate-specific antigen density improve the detection of clinically significant prostate cancer: A prospective single-center cross-sectional study. J Can Res Ther 2021;17:372-8

How to cite this URL:
Yadav K, Sureka B, Elhence P, Choudhary GR, Pandey H, Garg PK, Yadav T, Khera PS. Can combined multiparametric magnetic resonance imaging of the prostate and prostate-specific antigen density improve the detection of clinically significant prostate cancer: A prospective single-center cross-sectional study. J Can Res Ther [serial online] 2021 [cited 2021 Sep 23];17:372-8. Available from: https://www.cancerjournal.net/text.asp?2021/17/2/372/317070




 > Introduction Top


Prostate cancer is the fourth most commonly occurring cancer overall and the second most cancer in men.[1] It is the fifth-leading cause of cancer deaths in men.[2] The peak age at presentation in the Indian population is above 65 years, indicating that prostate cancer as a cancer of the elderly.[3],[4] The combination of serum prostate-specific antigen (PSA) as a screening tool for prostate cancer with digital rectal examination has resulted in a significant reduction in stage at the diagnosis.[5] The risk of cancer rises directly with PSA levels as a continuum.[6],[7] However, the lack of specificity and a high inherent variability of these screening tests lead to over-diagnosis, the discovery of incidental, clinically insignificant cancers, which often leads to overtreatment with accompanying morbidities (incontinence, impotence, etc.).[8],[9] Therefore, PSA density was introduced by Benson et al. in 1992, as a method to increase the PSA screening specificity. PSA density is used in the updated Epstein criteria for predicting clinically insignificant prostate cancer; the criteria is as PSA density of <0.15 ng/mL/mL, Gleason score ≤6, fewer than three positive cores, and <50% cancer involvement in any core.[10]

Multiparametric magnetic resonance imaging (MRI) has good sensitivity for clinically significant prostate cancer, with a specificity of 80%–90%_.[11] The European Society of Urogenital Radiology drew guidelines, including the PIRADS v2 scoring system, that allows risk stratification in patients with suspected cancer in treatment naive prostate glands.[12],[31],[14] Combination of targeted biopsies with prior MRI imaging in biopsy naïve patients results in higher clinically significant prostate cancer detection rates than standard systemic transrectal ultrasound (TRUS) biopsy alone.[15],[16],[17],[18],[19],[20],[21],[22] Considering the previous literature, we hypothesized that combination of mp-MRI PI-RADS v2 and PSA density can further improve diagnostic accuracy and risk assessment of patients with prostate cancer.


 > Material and Methods Top


Patients

The Institutional Ethics Committee approved this prospective study which was conducted at a tertiary care referral hospital in Western Rajasthan. Fifty-eight patients with PSA value of >4 ng/ml, referred from the department of urology for prostate magnetic resonance from July 2017 to December 2019 were enrolled in the study cohort. We excluded patients with a history of previous prostate biopsy (within 6 weeks) (n = 8), previous prostate surgery and patients who had incomplete or non-diagnostic MRI (n = 3).

Magnetic resonance protocol

Patient preparation: Patients were advised to take a low residue diet one night before the mpMRI examination. MRI was performed on 3T clinical MRI systems (GE Discovery MR 750 w 3T SYSTEM USA) using a 32-channel abdominal array coil. The detailed MR protocol is listed in [Table 1].
Table 1: Technical specifications for multiparametric magnetic resonance imaging

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Magnetic resonance imaging interpretation

Interpretation was performed by two radiologists (BS, KY with 15 and 2 years of experience respectively) in prostate mpMRI. The radiologists were aware of each patient's clinical findings before and during the PI-RADS scoring, which was based on PI-RADS version 2. PI-RADS version 2 utilizes a 5-point scoring scale based on the probability of the presence of clinically significant prostate cancer. Clinically, significant prostate cancer is defined on the basis of Gleason score ≥7 (including 3 + 4 with a prominent but not predominant 4 component) at histological examination, or volume >0.5 cm3, or extra prostatic extension.[23] The segmentation model in PI-RADS v2 consists 39 sectors/regions: thirty-six for the prostate, two for the seminal vesicles, and one for the external urethral sphincter.[24]

Assessment of clinically significant cancer

MR imaging analysis was performed using PI-RADS v2, a 5-point scale based on the likelihood (probability) that a combination of mpMRI findings on T2W, DWI, and DCE correlates with the presence of a clinically significant cancer for each lesion in the prostate gland We grouped patients into three categories according to mpMRI PI-RADS score and PSA density. Patients were considered in green zone whose PI-RADS v2 score was ≤3 and PSA density <0.15 ng/mL/mL, orange zone whose PI-RADS v2 score of ≥3 with PSA density ≥0.30 ng/mL/mL and yellow zone for remaining patients.

Transrectal ultrasound-guided 12 core prostate biopsy protocol

TRUS guided 12 core prostate biopsy was performed on PHILIPS Clear Vue 550 ultrasound machine. Biopsy was done using 18G × 25 cm automated biopsy gun. Sterile urine culture was mandatory prior to biopsy. Patients were advised to take a low residue diet one night before and are given a light soap water enema on the morning of the examination. Preprocedural antibiotic prophylaxis was given as injection Amikacin 750 mg intravenous 30 min before the biopsy and combination tablet of Ofloxacin (200 mg) and Ornidazole (500 mg) BD for 5 days. First, target biopsy was performed by a radiologist through cognitive targeting; the target lesion determined by multiparametric MRI according to PIRADS v2 criteria. The target biopsy consisted of two cores from each target lesion. If more than two target lesions were identified on MR images, target biopsies were performed on the two lesions with the highest PI-RADS score. Then standardized 12-core transrectal ultrasound-guided systematic biopsy (six in the peripheral zone and six in the transitional zone) was performed by another radiologist obtaining samples in 12 sample containers. The pathologist was blinded about the specimen obtained by cognitive targeting.

Statistical analysis

Statistical analyses were performed using the SPSS software for Windows (version 22.0, SPSS, IBM Corp, Armonk, NY, USA), and differences were considered significant when P < 0.05. The factors evaluated for the risk of a positive biopsy included age, PSA level, prostate volume, PSA density, and PI-RADS v2 score. The best-fit ROC curve was calculated with AUC estimates and 95% CIs. The sensitivity, specificity, positive, and negative predictive value were calculated for PSA density. Diagnostic accuracies for all PI-RADS categories, PSA density and combined PI-RADS and PSA density were also calculated. The cutoff values for the PSA density were calculated using the Youden index.


 > Results Top


Patient data

Flow of the patients in study is shown in [Figure 1]. Study population included 58 patients (mean age [standard deviation]: 68[9] years; range: 43–85 years). PSA density in malignant patients was higher than the benign group (median PSA density for malignant patients and for benign patients was 0.38 ng/ml/cc with IQR: 0.96 ng/ml/cc and 0.15 ng/ml/cc with IQR: 0.27 ng/ml/cc, respectively; P < 0.05). Malignant patients mean combined cases with clinically significant and clinically nonsignificant prostate cancer patients.
Figure 1: Flow of patients through the study

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PSA density in clinically significant prostate cancer patients was higher than the clinically non-significant prostate cancer patients (median PSA density for clinically significant prostate cancer patients and for clinically nonsignificant prostate cancer patients was 0.7 ng/ml/cc with IQR: 0.9 ng/ml/cc and 0.16 ng/ml/cc with IQR: 0.26 ng/ml/cc, respectively).

Tumor characteristics and distribution

There was total of 112 lesions suspicious for malignancy on MR imaging. 696 sectors of 58 patients (58 × 12 = 696) were evaluated histopathologically. Of the 696 sectors, 132 sectors were positive for cancer on histopathology. 108 sectors (16%) were positive for clinically significant prostate cancer and 24 sectors (3%) were positive for clinically non-significant prostate cancer.

Location of lesions

Of the 112 lesions in 58 patients which were assessed via mpMRI, a total of 84 lesions (84.75%) were detected in the central gland, whereas 20 lesions (20.18%) were detected in the peripheral zone. However, 8 (8.7%) lesions could not be localized into either peripheral zone or central gland, thereby categorizing them as mixed category. The ROC curve analysis for predicting prostate cancer showed that the AUC values of PSA density is 0.718 (95%CI: [0.601–0.836]), P = 0.001 suggesting that PSA density is a good marker for the diagnosis of prostate cancer. The ideal cutoff as per Youden's index method was found to be 0.23 where sensitivity and specificity were 70.4% and 67.1%, respectively [Figure 2] and [Figure 3].
Figure 2: Box plots showing comparison of prostate specific antigen density (ng/ml/cc) with patients having significant prostate cancer

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Figure 3: ROC curve analysis for predicting prostate cancer

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Isolated multiparametric magnetic resonance assessment in detecting prostate cancer

The histological outcomes stratified by PI-RADS v2 score is outlined by the bar diagram [Figure 4]. When a PI-RADS v2 score of ≥3 was considered positive, the sensitivity, specificity, PPV, and NPV for the detection of clinically significant prostate cancer were 94.1%, 68.4%, 34.8%, and 98.5%, respectively [Figure 5]. However, when a PI-RADS v2 score of ≥4 was considered positive, the sensitivity, specificity, PPV, and NPV for the detection of clinically significant prostate cancer were 82.4%, 89.5%, 58.3%, and 96.6%, respectively. [Table 2] shows the patients distribution according to PI-RADS and histopathological grading. The comparative statistics for overall prostate cancer detection and clinically significant prostate cancer are illustrated in [Table 3].
Figure 4: Bar diagrams showing distribution of lesions in each PIRADS category 2, 3, 4, 5 for benign and clinically significant prostate cancer and clinically non-significant prostate cancer

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Figure 5: 69-year-old male with prostate specific antigen = 20 ng/ml, prostate volume = 57 cc, prostate specific antigen Density = 0.35 ng/ml/cc, MR PIRADS score 3, HPE proven prostate carcinoma (a) T2W image demonstrate irregular moderate hypointense lesion in right TZa. (b) DWI sequence at high b value shows perilesional moderately hyperintensity (c) ADC maps show markedly hypointense confirming true restriction (d and e) DCE MRI reveals early enhancement with type 3 kinetic curve. (f) HPE (H and E stain, ×40) showing prostatic acini with prominent nucleoli, Gleason score 3 + 3 = 6

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Table 2: Patient characteristics, Prostate Imaging–Reporting and Data System score and Gleason score grading

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Table 3: Performance of Prostate Imaging–Reporting and Data System v2 score for the detection of prostate cancer

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Isolated prostate-specific antigen density assessment in detecting prostate cancer

PSA density was grouped into four categories <0.15, 0.15–0.29, 0.30–0.44, ≥0.45 ng/ml/cc [Table 4]. PSA density more than 0.30 ng/ml/cc has a higher specificity (71.8%) for the detection of prostate cancer as compared to PSA density of 0.15. ng/ml/cc (49.4%). The comparative statistics for overall prostate cancer detection and clinically significant prostate cancer are illustrated in [Table 5].
Table 4: Distribution of lesions in each prostate specific antigen density category

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Table 5: Performance of prostate specific antigen density using≥0.15 and≥0.30 ng/ml/cc as cut offs for the detection of prostate cancer

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Combined detection rate of overall prostate cancer using categories classified according to PSA density (<0.15, 0.15-0.29 or ≥0.30 ng/mL/mL) and PI-RADS v2 score

(2, 3 or ≥4).

A PI-RADS v2 score of ≥4 with all PSA density categories and a PI-RADS v2 score of 3 with a PSA density of ≥0.30 ng/mL/mL (orange zone), provided the highest number of overall prostate cancers (24) thereby assorted as high-risk group. On the contrary, a PI-RADS v2 score of ≤3 and PSA density of <0.15 ng/mL/mL (green zone), yielded no prostate cancer hence deemed as the low-risk group. Other group (yellow zone) shows overall prostate cancer detection rate of approximately 5% to 12.5%, assorted as moderate risk group [Table 6]. Sensitivity and NPV for the detection of prostate cancer after combining PSA density and PI-RADS increased to 96.3% and 97.8% from 92.6% and 97% for PI-RADS alone with a cutoff for PSA density of 0.3 ng/ml/cc.
Table 6: Prostate cancer detection by combination of Prostate Imaging–Reporting and Data System v2 score and prostate specific antigen density

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 > Discussion Top


Our study prospectively assessed PI-RADS version 2 and PSA density to test its performance in the diagnosis of overall prostate cancer and clinically significant prostate cancers. Our results showed that, in general, higher PI-RADS score positively correlate with higher diagnostic yield of clinically significant prostate cancer. The highest diagnostic accuracy of clinically significant prostate cancer was obtained with a PI-RADS score of 5. The present study shows superior diagnostic accuracy of clinically significant prostate cancer with an overall score of ≥4 compared to that of ≤3.

We assessed the accuracy of PI-RADS v2, (currently the most popular standardized reporting system among radiologists), for the detection and localization of prostate cancer. A cutoff ≥4 showed a higher specificity, PPV (97.6%, 91.7% for overall prostate cancer and 89.5%, 58.3% for CSPCa) than a cutoff ≥3 (75.3% and 54.3% for overall prostate cancer and 68.4%, 34.8% for CSPCa), and a lower sensitivity, NPV (81.5%, 94.3% for overall prostate cancer and 82.4%, 96.6% for CSPCa) than a cutoff ≥3 (92.6%, and 97.0% for overall prostate cancer and 94.1%, 98.5% for CSPCa). Hence, we concluded that a score ≥4 would be an optimal cutoff to detect overall prostate cancer and clinically significant prostate cancer with good sensitivity and specificity. However, a cutoff ≥3 in keeping with the greater sensitivity will aid in the detection of higher number of overall prostate cancer and clinically significant prostate cancers. Various other studies using radical prostatectomy/systematic biopsies as reference standards showed a wide range of sensitivities and specificities for the detection of clinically significant prostate cancer.[25],[26],[27],[28],[29],[30],[31],[32],[33],[34] The wide variation in sensitivity and specificity can be explained by the different cutoffs, differences in MRI machines, MRI acquisition protocols, variability of PI-RADS scoring, biopsy protocol, differences in patient characteristics, and user experience with the PI-RADS v2 system. With the relatively recent genesis of this system, the existing inter-observer variability can be regarded as part of a learning curve which is expected to improve with larger and more variable studies. To the best of our knowledge, we prospectively evaluated PI-RADS v2, strictly adhering to their imaging protocols.

Very few clinically significant prostate cancers were missed (PI-RADS score of 2) by MRI. Hence, PI-RADS v2, even in isolation, proved to be an accurate modality to diagnose overall prostate cancer and clinically significant disease. Despite the accuracy in determining biopsy outcome, the ambiguity of choice of whether to intervene by means of biopsy using solely this scoring system is questionable and therefore needs to be assisted using other parameters. If patients with a PI-RADS v2 score of 2 or 3 avoided a biopsy in the present study, 2.9% of the clinically significant prostate cancer would have been missed. We found that patients with a PI-RADS v2 score of 2 had fewer biopsy positive cores than those with PI-RADS v2 scores of 3,4 and 5. Furthermore, patients with PI-RADS v2 scores of 2 had no high-grade cancer in contrast to patients with PI-RADS v2 scores of 3, 4, and 5 which showed significant proportion of high-grade cancer.

The PSA density contributes significantly in predicting biopsy outcome. When the PSA density cut off value was set to 0.15 ng/mL/cc, sensitivity, specificity, PPV, NPV for detection of overall prostate cancer and clinically significant prostate cancers were 81.5%, 49.4%, 33.8%, 89.4% and 88.2%, 47.4%, 23.1%, 95.7%, respectively. However, when the PSA density cutoff value was set to 0.30 ng/mL/cc, sensitivity, specificity, PPV and NPV for detection of overall prostate cancer and clinically significant prostate cancers were 66.7%, 71.8%, 42.9%, 87.1% and 82.4%, 70.5%, 33.3%, and 95.7%, respectively. Various other studies using prostate biopsies as reference standards showed a wide range of sensitivities and specificities for the detection of clinically significant prostate cancer.[35],[36],[37],[38]

Despite the accuracy of PI-RADS v2 and PSA density in predicting biopsy outcomes individually, shortcomings of each of these entities are to be addressed. We found that a combination of the PI-RADS v2 score and PSA density recouped for these weak points and improved the predictive performance.

A PI-RADS v2 score of ≥4 irrespective of PSA density categories and a PI-RADS v2 score of 3 with PSA density of ≥0.15 ng/ml/cc yielded the highest overall prostate cancer and clinically significant prostate cancer detection rate. Contrary to, a PI-RADS v2 score of ≤3 and a PSA density of <0.15 ng/ml/ml (low-risk group), which yielded no clinically significant prostate cancer, inferring that this cohort of patients could have avoided unnecessary biopsies. Hence, a combination of PI-RADS v2 score and PSA density is weighed more effective in predicting biopsy outcome and thereby impelling further follow-up for patients with negative biopsy results.

The present study has some limitations. Prostate biopsies are subjected to the risk of inaccurate and inadequate sampling, making it less appropriate reference standard compared to radical prostatectomy specimen which was used as reference standard by many of the quoted studies. To the best of our knowledge, we were precise enough to sample the biopsy from the target lesion and 12 sectors, as quoted in methodology. Further, all the samples were appropriately labeled before transport and histopathological examination. However, even with appropriate sampling from the target lesion and biopsy sectors, there is still a chance that a prostate cancer can be missed. Biopsy accuracy could have been more accurate by using fusion imaging and shear wave elastography. The study was done taking TRUS-biopsy as the reference standard and not radical prostatectomy specimens. PSA density estimation and timing of biopsy varied in few cases, standardized protocol and reducing the time interval of patient biopsy could reduce variation and improve correlation.


 > Conclusion Top


Both PIRADS v2 score and PSA density are eminently sensitive and specific in the detection of clinically significant prostate cancers individually. However, the combination of PIRADS v2 and PSA density significantly improved the accuracy of clinically significant prostate cancer detection. Patients with combination of PIRADS v2 score ≥3 and PSA density ≥0.15 ng/ml/cc should definitely undergo prostate biopsy.

Acknowledgment

The authors would like to thank Dr Akhil Goel and Dr Ajay Chugh for helping in the statistical analysis.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.



 
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