Diagnostic Value of Multiparametric Transrectal Ultrasound in Patients with Suspected Carcinoma of Prostate: A Tertiary Care Centre Experience

Abstract

Objectives

To establish the role of grayscale ultrasonography, shear wave elastography (SWE), and contrast-enhanced ultrasound (CEUS) independently and in combination with multiparametric transrectal ultrasound (mp-TRUS) in detecting peripheral zone prostate cancer (PCa) and to compare the performance of mp-TRUS with multiparametric MRI (mp-MRI), keeping biopsy as the gold standard.

Materials and Methods

Thirty men with clinically suspected PCa were enrolled in this single-center-based prospective study conducted over a period of 1.5 years. All patients underwent mp-MRI, mp-TRUS, and guided biopsy. The mp-MRI and mp-TRUS were conducted and interpreted by two different observers who were blinded to each other's findings. In all patients, biopsy cores were taken from a minimum of 12 predetermined sites with extra cores taken from lesions suspicious on either grayscale ultrasonography, SWE, or CEUS.

Results

Malignancy was detected in 19 of our patients on mp-TRUS-guided biopsy. A total of 386 cores were obtained with a positive biopsy rate of 38%. mp-TRUS gave a sensitivity, specificity, PPV, NPV, and diagnostic accuracy of 100, 63.63, 82.61, 100, and 86.67%, respectively, while the values for mp-MRI were 94.74, 45.45, 75.00, 83.33, and 76.67%, respectively. The area under the ROC curve for mp-TRUS was 0.818 ± 0.076. This value was higher than that for mp-MRI (0.701 ± 0.083).

Conclusion

Performance of mp-TRUS is comparable to that of mp-MRI in diagnosing peripheral zone PCa. By improving the diagnostic yield of grayscale ultrasonography, mp-TRUS also acts as a great guiding tool for targeted biopsies, especially in patients where no lesions are seen on grayscale imaging.

 

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Keywords

prostatic neoplasms - multiparametric magnetic resonance imaging - biopsy - ultrasonography

Introduction

Prostate cancer (PCa) is now second in order of the most frequently diagnosed malignancies among men and also the fifth most frequent cause of cancer-related mortality in men worldwide.[1] The major clinical concern with PCa is that early disease is often asymptomatic, and it is only when the patient has advanced local cancer or metastatic disease that he presents with symptoms like those of bladder outlet obstruction, pelvic pain, hematuria, and/or bone pain. Survival rates depend on various factors, the most important of which is the tumor's extent at the time of diagnosis. The 5-year survival rate among patients with localized PCa is almost 100% versus just 29.3% among those diagnosed at a stage with distant metastases.[2]

As far as radiology is concerned, multiparametric MRI (mp-MRI)—an amalgamation of T2 weighted imaging (T2WI) with at least two functional MRI sequences—is currently the imaging gold standard for the prostate.[3] While mp-MRI has shown good performance in diagnosing, staging, and even monitoring patients with PCa, its utility is restricted by certain limitations such as low specificity, high cost, limited availability, and moderate inter-reader reproducibility.[4] [5] It is therefore not appropriate and presently not recommended as a screening modality for diagnosing PCa.[6] [7] [8] [9]

Consequently, a need was felt to explore a modality that could do away with these limitations while maintaining similar diagnostic performance. Therefore, as part of our research, we evaluated the diagnostic performances of grayscale imaging, shear wave elastography (SWE), and contrast-enhanced ultrasound (CEUS) independently and in combination with multiparametric transrectal ultrasound (mp-TRUS) and compared this performance with that of mp-MRI in patients with clinically suspected PCa keeping biopsy as our gold standard. Besides being widely available, portable, and relatively cheap, ultrasonography provides the added advantage of real-time imaging and allows biopsy needle tracking.[10] Over the years, several studies have been conducted to assess the diagnostic capabilities of the individual components of mp-TRUS.[11] [12] [13] [14] [15] [16] [17] [18] [19] [20] However, there are very few studies that have assessed the combined performance of these modalities and that have compared mp-TRUS with mp-MRI.

 

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Materials and Methods

Ours was a single-center-based prospective study conducted over a period of 1.5 years. Based on the previously done studies with a similar design and in accordance with the concept of convenience sampling, we included a total of 30 men who met the selection criteria of the study ([Table 1]). The study was duly approved by the Institutional Ethics Committee (vide application number: INT/IEC/2019/000564 dated March 16, 2019). Written informed consent was obtained from all participants who were then taken up for mp-MRI, mp-TRUS, and guided biopsy (in that order). The mp-MRI and mp-TRUS were conducted and interpreted by two different observers who were blinded to each other's findings.

Table 1 Patient selection criteria

Inclusion criteria • Patients ≥ 18 years old • Abnormal digital rectal examination and/or raised S. PSA (≥4 ng/mL) • Patients undergoing mp-MRI of the prostate • Signed informed consent

Exclusion criteria • Proven cases of prostate cancer • Patients who are not able to undergo TRUS • Clinically T3 or higher rectal examination • Any prior focal therapy for any prostate-related condition • Any kind of hormonal or androgen deprivation therapy in the last 6 months • Patients who cannot be administered UCA due to one or more contraindications for the same • Any condition (or circumstance) which could hinder any aspect of the study

Abbreviations: S. PSA, serum prostate-specific antigen; UCA, ultrasound contrast agent.

mp-MRI was conducted using a 3-T system (MAGNETOM Verio; Siemens Medical Solutions, Erlanger, Germany) with a pelvic phased array coil. Turbo spin-echo sequences were used to attain T2WIs of the gland and the seminal vesicles in three planes (axial, sagittal, and coronal). All measurements were taken on T2WIs. Echoplanar imaging sequences were used to attain the diffusion-weighted images in the axial plane at multiple b-values (50, 400, 800, 1,000, and 1,400 second mm²). Following DWI, dynamic contrast-enhanced MRI was done using fast T1-weighted “Volumetric Interpolated Breath-Hold Examination (VIBE)” gradient echo sequences, and axial sections were obtained during continuous intravenous injection of a gadolinium-based contrast agent. The findings were reported on the basis of the guidelines laid down by PI-RADS version 2.1 and scores ≥ 4 were considered as malignant.

mp-TRUS was performed using the Aixplorer clinical ultrasound scanner (Supersonic Imagine, Aix-en-Provence, France) by using the Super Endocavity SE 12–3 end-firing endoluminal probe. SonoVue (Bracco, Switzerland) was the intravenous ultrasound contrast agent (UCA) used for CEUS examinations. Since the biopsy was conducted in the same sitting, it was ensured before starting the procedure that the patient's urine culture was sterile and that the coagulogram was normal. Also, patients were asked to start tablet ciprofloxacin 500 mg BD 1 day before the procedure and to continue it for 3 days post procedure. All patients who were constipated were prescribed laxatives, to be taken the night before the procedure. The examination was begun following the proper establishment of an intravenous access line and placement of the patient in the left lateral position.

Grayscale imaging: We started by measuring the anteroposterior, transverse, and cranio-caudal dimensions of the prostate and then calculated the volume using the ellipsoid formula. The entire gland was assessed in both axial and sagittal planes and images were stored at the level of the base, mid, and apical transverse planes. For each suspicious lesion, we noted its echogenicity (hypoechoic/isoechoic), shape (regular/irregular), and margins (clear/unclear). The prostate capsule and seminal vesicles were evaluated to look for any evidence of breach or invasion, respectively.

SWE: In the SWE mode, the prostate was scanned in the transverse plane keeping minimal transducer pressure over the gland. Proper optimization of the settings was done to ensure maximum penetration and set a scale of 70 kPa. The right and left sides of the peripheral zone were analyzed from base to apex and still images were saved. Before capturing the images, the transducer was kept still for 3 to 5 seconds to ensure stable acquisition. Once acquired, two measurements per sextant were taken by placing a circular ROI in the lateral and paramedian portions of the sextant. This way, a total of 12 readings were taken. In cases where a suspicious area was identified outside the predetermined imaging planes, that too was brought into view, assessed, and recorded. The diameter of the ROI was fixed at 3 mm for all stiffness measurements.

CEUS: Before scanning, settings such as focus zone, dynamic range, and mechanical index were optimized for each patient. While performing the scan, a rapid bolus of SonoVue UCA was administered intravenously which was followed by a 10 mL normal saline flush. In patients who had suspicious lesions on grayscale ultrasound, CEUS was performed keeping those lesions under focus. For patients who had a normal grayscale study but had suspicious areas on SWE, CEUS was performed at the corresponding sites of increased stiffness. For patients who had no suspicious lesions on both grayscale and SWE, CEUS was performed in three planes by giving three separate UCA boluses—at the level of the base, mid-gland, and apex to look for suspicious enhancement patterns. Continuous evaluation was performed immediately after UCA administration and video clips of 3 minutes were recorded in the “Digital Imaging and Communications in Medicine (DICOM)” format which was evaluated and analyzed. The parameters we assessed included wash-in time (early/synchronous/late), wash-out time (early/synchronous/late), and enhancement intensity (high/equal/low).

Following radiological evaluation, a US-guided biopsy was performed in the same sitting. Biopsy cores were taken from 12 predefined sites corresponding to the sites of SWE measurements. Additional cores were taken from areas suspicious on SWE and /or CEUS by a targeted approach in cases where grayscale imaging showed no suspicious lesion. All specimens were then assessed by an experienced uropathologist and Gleason scores were assigned for the positive cores. Clinically significant disease was defined as Gleason score ≥ 3 + 4 = 7 with a tumor volume > 0.5 cm³. A patient was labeled as having PCa if at least one of the cores came out positive for clinically significant malignancy.

The grayscale data was correlated with the final diagnosis as per biopsy. Statistical analysis was performed to evaluate if a significant difference existed between the grayscale characteristics of benign and malignant lesions. A patient was then classified as having PCa (as per the grayscale US) if ≥ 3 malignant characteristics were present. The CEUS data was similarly correlated with the biopsy results. A patient was classified as having PCa (as per CEUS) if ≥ 2 malignant characteristics were present. For the data pertaining to SWE, analysis was done at the level of each core. The stiffness value of each core was compared with its respective biopsy result. The data was then assessed to see if the difference in stiffness values of malignant and benign lesions was statistically significant or not.

 

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Results

As per biopsy results, 19 (63.33%) of our patients had PCa. A total of 386 cores were obtained with a positivity rate of 38%. No major complications were encountered while performing the mp-TRUS examinations and biopsies. Comparison between the median values of serum prostate-specific antigen (PSA) levels of the benign (7.70 ng/mL) and malignant (9.72 ng/mL) groups showed no significant difference in our study (p = 0.287).

On mp-MRI, 24 (80%) patients had a PIRADS score of 4 or 5 while the other 6 (20%) had a score of either 1, 2, or 3. Based on the final biopsy result, mp-MRI had a sensitivity, specificity, PPV, NPV, and accuracy of 94.74, 45.45, 75.00, 83.33, and 76.67%, respectively, for diagnosing PCa.

On grayscale US, 14 (46.67%) patients showed a suspicious lesion. “Hypoechoic” echogenicity, “irregular” shape, and “unclear” margins showed statistically significant differences from their counter-characters (p-value of 0.0003 each) and were considered to be malignant characteristics. By applying the criteria described, 13 patients were labeled as having PCa on grayscale US and the modality gave a sensitivity, specificity, PPV, NPV, and accuracy of 68.42, 100, 100, 64.71, and 80%, respectively.

On CEUS, 18 (60%) patients showed suspicious lesions. Nonsynchronous wash-in and washout times along with unequal enhancement intensity were categorized as malignant characteristics. Lesions that met ≥ 2 malignant characteristics (n = 17) were labeled to be diagnostic of PCa by CEUS. With CEUS, we got a sensitivity, specificity, PPV, NPV, and accuracy of 89.47, 100, 100, 84.62, and 93.33%, respectively.

On SWE evaluation, the overall mean elasticity value of the 386 cores was 63.88 ± 32.08 kPa (range: 3.70–168.10 kPa) with a median of 51.25 kPa. A total of 147 cores were malignant out of 386. The mean stiffness value of the malignant cores was 92.36 ± 27.75 kPa with a median value of 88.50 kPa. The benign cores had a mean elasticity value of 46.37 ± 19.61 kPa. The median value was 42.00 kPa. Applying the Mann–Whitney U test, a p-value of <0.0001 was attained suggesting that the difference was statistically significant. Also, a rising trend was observed for the elasticity values with increasing Gleason scores. Thus, Spearman rank correlation was used to compute the correlation between adenocarcinoma stiffness and Gleason score, and a box-and-whisker plot for the same was plotted ([Fig. 1]). A correlation coefficient (r) of 0.33 was attained suggesting a weak positive linear correlation. A ROC curve ([Fig. 2]) was plotted for the elasticity values and the AUC was calculated with 95% confidence intervals. A maximum Youden Index of 72.90% was attained and the application of a cut-off value of 51.6 kPa for differentiating malignant cores from benign ones resulted in an AUC of 91.4%. The diagnostic performance of SWE keeping an optimal cut-off of 56.1 kPa was calculated which gave a sensitivity, specificity, PPV, NPV, and accuracy of 94.74, 63.63, 81.82, 87.50, and 83.33%, respectively.

Fig. 1 Box-and-whisker plot showing elasticity values for malignant cores with Gleason scores of 6 to 10.

Fig. 2 ROC curve for elasticity values showing an AUC of 91.4.

Finally, on mp-TRUS, a patient was diagnosed as having PCa if any of the three components was suggestive of malignancy by the criteria described above. In this way, mp-TRUS gave a sensitivity, specificity, PPV, NPV, and accuracy of 100, 63.63, 82.61, 100, and 86.67%, respectively. The diagnostic performances of mp-TRUS and mp-MRI were compared by ROC curve analysis. The AUC for mp-TRUS was 0.818 ± 0.076 while the AUC for mp-MRI was lower at 0.701 ± 0.083. A pairwise comparison of the two ROC curves revealed a p-value of 0.2155 suggesting comparable performance of the two modalities. [Table 2] summarizes the diagnostic performance of all the modalities that we tested.

Table 2 Diagnostic performance of grayscale US, SWE, CEUS, mp-TRUS, and mp-MRI

Modality	Sensitivity (%)	Specificity (%)	PPV (%)	NPV (%)	Accuracy (%)
Grayscale US	68.42	100	100	64.71	80
SWE	94.74	63.63	81.82	87.50	83.33
CEUS	89.47	100	100	84.62	93.33
mp-TRUS (grayscale, SWE, or CEUS)	100	63.63	82.61	100	86.67
mp-TRUS (grayscale + SWE + CEUS)	57.89	100	100	57.89	73.33
mp-MRI	94.74	45.45	75	83.33	76.67

Abbreviations: CEUS, contrast-enhanced ultrasound; mp-MRI, multiparametric magnetic resonance imaging; mp-TRUS, multiparametric transrectal ultrasound; SWE, shear wave elastography; US, ultrasound.

 

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Discussion

Starting with mp-MRI, we observed in our study that while the modality performed very well in picking up almost all patients with PCa (18 out of 19; sensitivity of 94.74%), it also gave false positive results in 26.31% of the patients (n = 5) thereby reducing the overall specificity to 45.45%. These results are in line with those of the PROMIS trial conducted by Ahmed et al[4] who reported a sensitivity and specificity of 93 and 41%, respectively.

Grayscale US (when considered independently) missed 31.6% (n = 6) of the lesions that were actually malignant. These results are in line with those attained by Zhang et al[12] who showed that 28.9% of their PCa patients had no visible lesions on grayscale US. These results reflect the known sonographic properties of PCa[13] [14] that around 30 to 40% of tumors are isoechoic, thus limiting the diagnostic capability of grayscale US.

The basis for SWE is that malignant disease is characterized by hardening of tissue which can be picked up in the form of raised elasticity values. Based on the conclusions made by Barr et al[21] and Correas et al[11] on the inaccuracy of SWE's performance in the transition zone due to inevitably high elasticity values, we decided to limit our study to the peripheral zone of the prostate only. In our study, a statistically significant difference was noted between the median elasticity values of benign (42.00 kPa) and malignant (88.50 kPa) regions with a p-value of <0.0001. This result is in agreement with the multiple other studies done on SWE of the prostate such as those conducted by Ahmad et al,[22] Barr et al,[20] Boehm et al,[19] Correas et al,[11] and Woo et al[23]—all of which concluded that SWE values are significantly different between benign and malignant regions. As for the elasticity values, there is heterogeneity in the literature regarding the cut-off with different studies recommending different cut-offs. Studies done by Barr et al,[20] Boehm et al,[19] Correas et al,[11] Rouviere et al,[24] Woo et al,[23] and Ji et al.[18] reported cut-offs of 37, 50, 35, 45, 43.9, and 62.27 kPa, respectively. There could be several reasons for the slightly higher cut-off attained in our study. One, the study was conducted in patients with suspected PCa. Therefore, many benign entities such as prostatitis which are known to increase stiffness values may have contributed to the overall higher values. Second, the benign prostates included in our study had a significantly higher mean volume (60.29 ± 27.73 cc vs. 30.18 ± 14.58 cc) than the malignant ones (predominantly due to changes in benign prostatic hyperplasia). Enlargement of the transition zone can exert pressure over the peripheral zone leading to falsely high elasticity values. The heterogeneity with respect to cut-off values can also be explained to some extent by the variable pressure exerted onto the gland while performing the elastography. Even though it has been documented in the literature that SWE does not require additional extrinsic compression, it is not possible to carry out SWE examination without applying any pressure at all to the gland.[22] This implies that the prostate size and the operator's technique may lead to some variability in the elasticity values even if the least possible pressure is applied while performing the examination.

In our study, mp-TRUS gave a sensitivity of 100% with a specificity of 63.63% and PPV and NPV of 82.61 and 100%, respectively, with an overall accuracy of 86.67%. Although mp-MRI showed good sensitivity (94.74%), the specificity, PPV, and NPV (45.54, 75, and 83.33%, respectively) were lower than mp-TRUS (63.63 82.61, and 100%, respectively). The overall accuracy of mp-MRI was also lower than that of mp-TRUS (76.67% vs. 86.67%). The AUC for mp-TRUS was 0.818 ± 0.076 while that for mp-MRI was lower at 0.701 ± 0.083. Our results are similar to those attained by Zhang et al[12] who reported a sensitivity, specificity, PPV, NPV, and accuracy of 97.4, 77.5, 80.4, 96.9, and 87.2%, respectively, for mp-TRUS. The AUC for mp-TRUS in their study was 0.874, which was higher than that of mp-MRI (0.774).

Our results imply the fact that since the performance of mp-TRUS in diagnosing peripheral zone PCa is comparable to that of mp-MRI, mp-TRUS may be appropriate as an independent modality for highlighting and selecting targets during guided biopsies without the need for prior MR imaging. Also, with the use of mp-TRUS, unnecessary biopsies could well be avoided (attributable to the high NPV); thereby resulting in an overall reduction in the related medical costs and complications. In addition, the fact that mp-TRUS significantly improved the sensitivity of grayscale US signifies that mp-TRUS can act as a great guiding tool for targeted biopsies, especially in patients in whom grayscale imaging is unable to pick up suspicious lesions ([Fig. 3]). [Fig. 4] shows the comparable performance of mp-MRI and mp-TRUS in highlighting a suspicious lesion in the peripheral zone of the prostate.

Fig. 3 Images at the level of the base and mid-gland of a patient with clinically suspected PCa. (A–D) No definite lesion was seen on the grayscale images. (E, F) SWE in the same patient shows significantly elevated stiffness in the left peripheral zone at the level of the base and mid part of the gland. (G, H) CEUS images showing early nonsynchronous enhancement (arrow) and washout in the corresponding area. Biopsy revealed adenocarcinoma.

Fig. 4 (A–D) mp-MRI prostate showing PIRADS 5 lesion. (A) T2WI shows a circumscribed, moderately hypointense lesion in the left peripheral zone (arrow) at the level of the base of the gland measuring >1.5 cm in the greatest dimension. (B) Dynamic contrast-enhanced MRI showing early enhancement of the lesion. (C) Hyperintense signal of lesion on DWI (b-value = 1,400 second mm²). (D) Corresponding ADC map showing hypointensity, confirming restricted diffusion. (E–H) mp-TRUS in the same patient (E) Grayscale image appears grossly normal except for subtle hypoechogenicity in the left peripheral zone. (F) SWE at the same level shows the nodular area of elevated tissue stiffness. (G, H) CEUS at the same level shows early wash-in and wash-out of contrast. Biopsy from this suspicious lesion revealed adenocarcinoma with a Gleason score of 3 + 4.

Our study had a few limitations. First, we used image-guided biopsy as our gold standard and not radical prostatectomy specimens. This could have led to the missing out of some of the cancerous lesions, resulting in a higher number of false positives on SWE, thereby negatively influencing the modality's diagnostic performance. Second, the sample size of our study was small. Third, this study was restricted to the detection and characterization of lesions located in just the peripheral zone of the prostate. And lastly, CEUS data was analyzed qualitatively in our study. A quantitative analysis, however, would have helped extract blood flow parameters from the CEUS data and would've helped predict better whether a particular lesion was malignant or not.

In conclusion, our results and observations suggest that mp-TRUS is comparable in its diagnostic performance to mp-MRI in patients with clinically suspected peripheral zone PCa. mp-TRUS also significantly improves the diagnostic yield of conventional grayscale ultrasound and can act as a great guiding tool for targeted biopsies, especially in patients where no lesions are seen on grayscale imaging. The results imply that mp-TRUS may be appropriate as an independent modality for highlighting and selecting targets during guided biopsies without the need for prior MR imaging. Also, with the use of mp-TRUS, unnecessary biopsies could well be avoided, thereby resulting in an overall reduction in the related medical costs and complications.

 

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Conflict of Interest

None declared.

Note

This work was previously presented at the ARRS 2021 Annual Conference.

Ethical Approval

Ethical approval was obtained from the Institutional Ethics Committee.

Patients' Consent

Written informed consent was obtained from all patients for this study.

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Publication History

Article published online:
04 June 2025