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Keywords:

  • 3D reconstruction;
  • diagnostics;
  • power Doppler;
  • prostate cancer;
  • ultrasound

Abstract

  1. Top of page
  2. Abstract
  3. Introduction
  4. Patients and methods
  5. Results
  6. Discussion
  7. Conclusion
  8. Acknowledgments
  9. References

Aim:  The aim of the study is to investigate the value of preoperative power Doppler sonography with 3D reconstruction (3D-PDS) for diagnostics of extraprostatic extension of prostate cancer.

Patients and Methods:  In the prospective study we examined 146 patients with clinically localized prostate cancer who underwent radical prostatectomy. Prior to surgery, each patient underwent 3D-PDS, transrectal ultrasound (TRUS), and digital rectal examination (DRE). Furthermore, we determined the prostate volume, prostate specific antigen (PSA) level, PSA density (PSAD), and Gleason score. The risk of locally advanced cancer was assessed using Partin tables. We determined the sensitivity, specificity, and predictive values of these diagnostic procedures. We plotted the receiver operating characteristic (ROC) curves and calculated the areas under the curves (AUC). Multivariate logistic regression was used to identify the significant predictors of extraprostatic tumor extension. Based on this we developed diagnostic nomograms maximizing the probability of accurate diagnosis.

Results:  The significant differences between patients with organ confined and locally advanced tumor (based on the postoperative assessment) were observed in the PSA levels (P < 0.014), PSAD (P < 0.004), DRE (P < 0.037), TRUS (P < 0.003), and 3D-PDS (P < 0.000). The highest AUC value of 0.776 (P < 0.000) was found for 3D-PDS. The observed AUC value for TRUS was 0.670 (P < 0.000) and for PSAD 0.639 (P < 0.004). In multivariate regression analysis, the PSAD, preoperative Gleason score, and 3D-PDS finding were identified as significant preoperative predictors of extraprostatic tumor extension.

Conclusion:  Our data suggest that the 3D-PDS is a valuable preoperative diagnostic examination to identify locally advanced prostate cancer. Therefore, it can be used to maximize the probability of the accurate diagnosis of extraprostatic tumor extension.


Introduction

  1. Top of page
  2. Abstract
  3. Introduction
  4. Patients and methods
  5. Results
  6. Discussion
  7. Conclusion
  8. Acknowledgments
  9. References

With steadily growing incidence, prostate cancer represents the third most frequent cancer in men in the Czech Republic and the second in the European Union.1 The increasing number of men undergoing examination of prostate specific antigen (PSA) enables the detection of tumors with more favorable characteristics (earlier stage, lower tumor grade) and in younger patients.2,3 The current trend in localized prostate cancer therapy therefore aims at lowering treatment aggressiveness, leading to less frequent late complications and the associated undesirable impact on the quality of life. The preservation of neuro-vascular bundles lowers the occurrence of erectile dysfunction after surgery4 and according to some authors, the nerve-sparing technique also represents a protective factor for continence after radical prostatectomy.5,6 Nerve-sparing radical prostatectomy is indicated in cases of prostate cancer without signs of extraprostatic extension.7 Accurate preoperative assessment of tumor extent is therefore a key factor in determining the therapy and prognosis. Unfortunately, in 22–63% of cases of clinically localized prostate cancer, later histological examination of the radical prostatectomy specimen reveals locally advanced cancer.8 The accuracy of preoperative diagnostics of prostate cancer is therefore still limited.

Extraprostatic tumor extension is currently most often assessed by nomograms evaluating its probability based on a few parameters obtained by preoperative examination, e.g. digital rectal examination (DRE), PSA, and prostate biopsy. The Partin 1997 tables and their more recent version of 2001 are an example of nomograms commonly used in clinical practice.9,10 Imaging methods represent another possibility of preoperative extraprostatic tumor extension diagnostics. However, CT examination is inadequate for local assessment of prostate cancer and not used routinely.11 A more suitable imaging method is endorectal MRI; however, it is costly and in many facilities unavailable. The most commonly used imaging method is therefore transrectal ultrasound, even though its results in determining minimal T3 disease are poor.11

Recently, the optimistic results of Doppler sonography, particularly power Doppler sonography with 3D reconstruction (3D-PDS), in diagnostics of the extraprostatic tumor extension were reported.12 Therefore, we designed the present study to evaluate the reliability of 3D-PDS in preoperative diagnostics of localized and locally advanced prostate cancer. This evaluation is based on a comparison of performance between 3D-PDS and other diagnostic methods commonly used for the preoperative diagnostics of prostate tumor extension and the postoperative examination of the tumor extent in the definitive histological examination of the radical prostatectomy specimen.

Patients and methods

  1. Top of page
  2. Abstract
  3. Introduction
  4. Patients and methods
  5. Results
  6. Discussion
  7. Conclusion
  8. Acknowledgments
  9. References

This prospective study is based on the comparison of different preoperative diagnostic methods used for the diagnostics of prostate cancer extension, including 3D-PDS, with the postoperative evaluation of the tumor extent in the definitive histological examination of the radical prostatectomy specimen.

Patients

In the years 2003–2005, 173 patients were admitted to the Department of Urology of the 3rd Medical School of Charles University to undergo radical prostatectomy due to prostate cancer. This department represents a tertiary urology center where patients are transferred from a large catchment area.

The study enrolled 146 patients with clinically localized cancer according to DRE and with a PSA value lower than 20 ng/mL, who underwent radical prostatectomy. Their mean age at the time of surgery was 63.9 years (51–79 years), the mean PSA value was 8.45 ng/mL (0.8–18.87 ng/mL) and the mean Gleason score was 4.5. The mean prostate volume was 36.6 mL (15–140 mL). The mean PSA density value (PSAD) calculated as a ratio of PSA value and prostate volume measured by transrectal sonography was 0.27. Written informed consent was obtained from all participants.

Diagnostic methods

Prior to radical prostatectomy, each patient underwent DRE, TRUS and 3D-PDS. Both sonography tests were done using ultrasonography detector B-K Hawk by one examiner only (M.Z.). At the time of examination, the examiner was kept blind regarding the tumor characteristics determined by the urologist committing the patient (PSA, prostate biopsy histology, TRUS).

Transrectal ultrasonography was performed using a biplanar rectal probe 7.5 MHz BK 8808 with crystals in transversal and sagittal planes. Patients were examined lying on the left side. A tumor extending beyond the prostate or invading the seminal vesicles was considered in cases of apparent hypoechogenic or anisoechogenic focus distinctly extending the prostate outline or penetrating seminal vesicles.

Doppler imaging was then performed using power Doppler mapping in transversal and sagittal planes. The Doppler gain was adjusted according to the Rubin technique.13 Other parameters were preset and used in the same manner at every examination (PRF 1500 Hz, persistence was preset to grade 3 of a 6-degree scale and filtering was preset to grade 16 of a 32-degree scale). Transversal prostate sections directed from the base to the apex were then recorded in 0.25 mm intervals and 3D reconstruction was done based on the findings. Vascularization of the prostate obtained in the power Doppler mode was analyzed on 3D images. The finding of apparent hypervascular focus extending beyond the prostatic capsule was taken as a prostate-extending tumor (Fig. 1); the invasion of seminal vesicles was considered when finding a hypervascular focus extending from the prostate to the seminal vesicles (Fig. 2).

image

Figure 1. Power Doppler sign of extraprostatic extension of prostate cancer. The finding of apparent hypervascular focus extending beyond the prostatic capsule was taken as a prostate-extending tumor.

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image

Figure 2. Power Doppler sign of the invasion of the seminal vesicle. Invasion of the seminal vesicle was considered when finding a hypervascular focus extending from the prostate to the seminal vesicles.

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The risk of extraprostatic tumor extension was also evaluated using Partin tables (versions 1997 and 2001).9,10

The local cancer extent was then assessed by histological examination of the radical prostatectomy specimen (Table 1).

Table 1.  Tumor extent according to the results of histological examination of the radical prostatectomy specimen
pT03pT032.05%
pT1b0pT100.00%
pT1c0   
pT2a20pT28155.48%
pT2b13   
pT2c48   
pT3a41pT36141.78%
pT3b20   
pT4a1pT410.68%
Total146 146100.00%

Statistical evaluation

Based on the agreement between preoperative findings and postoperative findings we calculated Cohen kappa coefficient, sensitivity, specificity, negative predictive value (NPV), positive predictive value (PPV), and the accuracy of all diagnostic tests of interest.

The differences between the groups with organ confined cancer and extraprostatic tumors determined by postoperative histological examination were evaluated by means of the Mann–Whitney U-test and the χ2 -test.

Receiver operating characteristic (ROC) curves were plotted with the sensitivity on the y-axis vs 1 minus the specificity on the x-axis for each diagnostic test, and the areas under the curves (AUC) were compared as the best marker of diagnostic value of the tests.

The best independent predictors of extraprostatic tumors were identified by a stepwise logistic regression analysis (probability for entry of the variable was set to be less than 5%, the probability for removal more than 10%). The resulting model was used to predict the risk of locally advanced cancer, according to the following formula: risk of extraprostatic cancer = 1/(1 + e–(b0+b1X1+b2X2+b3X3)), where b's are the regression coefficients for risk factors and X's are the values of risk factors.

The results with P < 0.05 were considered statistically significant.

Results

  1. Top of page
  2. Abstract
  3. Introduction
  4. Patients and methods
  5. Results
  6. Discussion
  7. Conclusion
  8. Acknowledgments
  9. References

Results of sonographic methods

The values of basic diagnostic parameters of TRUS and 3D-PDS and its comparison with histological examination of the radical prostatectomy are presented in Table 2.

Table 2.  Evaluation of preoperative imaging methods (n = 146)
 TRUS3D-PDS
  1. 3D-PDS, power Doppler sonography with 3D reconstruction; NPV, negative predictive value; PPV, positive predictive value; TRUS, transrectal ultrasound.

Sensitivity0.080.62
Specificity0.990.79
PPV§0.830.72
NPV¶0.590.70
Accuracy0.600.71
Kappa0.078 (P < 0.039)0.416 (P < 0.000)

In 41 out of 146 patients (28.08%), TRUS showed isoechogenic prostate tumor without any signs of abnormalities allowing sonographic diagnostics of prostate cancer. Of these cases, 33 patients (80.49%) were diagnosed postoperatively with localized prostate cancer.

Twenty-nine out of 146 patients (19.86%) displayed no abnormalities suggesting the presence of prostate tumor in 3D-PDS. In 26 of them (89.66%) the prostate tumor was limited to the prostate according to the histological examination of the radical prostatectomy specimen. Only two patients showed tumor invasion through the prostatic capsule and one had invaded seminal vesicles.

On DRE, 81 patients (55.5%) had unpalpable prostate tumors. In this subgroup, 38 patients (46.9%) had no apparent tumor in TRUS and in 29 cases (35.8%) the tumor was not apparent even on 3D-PDS.

A total of 65 patients (45.5%) had palpable prostate tumors, and in 17 patients (11.6%) the tumor was palpable bilaterally. In this subgroup only three patients (4.6%) had no apparent tumor according to TRUS; using 3D-PDS the tumor was visible in all patients.

Potential preoperative estimation of seminal vesicle invasion (SVI) using TRUS and 3D-PDS was then evaluated. The invasion of seminal vesicles in the radical prostatectomy specimen was found in 20 patients (13.7%). The sensitivity of SVI detection by TRUS was 0.05, specificity 1.00, and the kappa value 0.083 (P < 0.012). The sensitivity of SVI detection by 3D-PDS was 0.35, specificity 0.93, and the kappa value was 0.304 (P < 0.000).

Comparison of preoperative findings in patients with localized and locally advanced tumors and ROC analysis of preoperative diagnostic methods

Histological examination of the radical prostatectomy specimen showed the presence of localized tumors in 84 patients and of locally advanced tumors in 62 patients. In both subgroups the continuous preoperative parameters were compared and evaluated using the Mann–Whitney U-test (Table 3). A statistically significant difference between patients with localized and locally advanced tumor was found in the PSA values (P < 0.014) and PSAD (P < 0.004). Other parameters such as age, prostate volume and risk of locally advanced prostate tumor according to Partin tables were not significantly statistically different. Categorical preoperative parameters were evaluated using the χ2-test (Table 4). Statistically significant differences between the group of localized cancer and the group of locally advanced cancer were found in the case of DRE (P < 0.037), TRUS (P < 0.003) and 3D-PDS (P < 0.000). The Gleason score obtained by prostate biopsy was not significantly statistically different in either group.

Table 3.  Comparison of preoperative parameters in patients with localized and locally advanced prostate carcinoma
  Localized prostate cancer n = 84Locally advanced prostate cancer n = 62Mann–Whitney (P)
  • Prostatic specific antigen transrectal ultrasound.

  • Risk of locally advanced tumor according to Partin 1997 tables.9

  • §

    Risk of locally advanced tumor according to Partin 2001 tables.10 PSA, prostatic specific antigen.

Age (years)Mean63.6164.400.433
Median64.0064.00 
Minimum51.0056.00 
Maximum79.0073.00 
PSA (ng/mL)Mean7.719.460.014
Median7.108.25 
Minimum0.803.20 
Maximum14.7018.87 
PSA densityMean0.230.330.004
Median0.220.26 
Minimum0.030.07 
Maximum0.691.00 
Partin 1997 (%)Mean35.4541.080.067
Median33.539.5 
Minimum1111 
Maximum8685 
Partin 2001§ (%)Mean29.1934.480.125
Median2531 
Minimum58 
Maximum7989 
Prostate volume (cm3)Mean37.3835.570.108
Median35.0029.00 
Minimum15.0015.00 
Maximum95.00140.00 
Table 4.  Contingent table for preoperative categorical parameters with the χ2-test evaluation
 Preoperative categorical parametersLocalized prostate cancer (n)Locally advanced prostate cancer (n)Total (n)Sig. (P)
  1. 3D-PDS, power Doppler sonography with 3D reconstruction; DRE, digital rectal examination; TRUS, transrectal ultrasound.

Biopsy Gleason score2107170.118
39716 
4301343 
5231538 
6101222 
7156 
8112 
9022 
Total 8462146 
DRE†T1b2020.037
T1c522779 
T2a639 
T2b152439 
T2c9817 
Total 8462146 
TRUS‡T1b2020.003
T1c31839 
T2a221638 
T2b142034 
T2c141327 
T3a145 
T3b011 
Total 8462146 
3D-PDS§T1b2020.000
T1c24327 
T2a21930 
T2b13821 
T2c10212 
T3a112738 
T3b31316 
Total 8462146 

For all preoperative parameters, ROC curves were generated and areas under the curve (AUC) were calculated (Table 5). The highest AUC value was for 3D-PDS 0.776 (P < 0.000), TRUS 0.67 (P < 0.000) and PSA density 0.639 (P < 0.004). Figure 3 shows ROC curves for PSA density and Gleason score values and for 3D-PDS findings.

Table 5.  Area under the curve (AUC) of individual preoperative parameters and their statistical significance
 AreaSig. (P)95% Confidence Interval
Lower boundUpper bound
  • Risk of locally advanced tumor according to Partin 2001 tables.10

  • Risk of locally advanced tumor according to Partin 1997 tables.9 3D-PDS, power Doppler sonography with 3D reconstruction; DRE, digital rectal examination; PSA, prostatic specific antigen; TRUS, transrectal ultrasound.

Prostate volume0.4240.1160.3270.520
Partin 20010.5740.1260.4800.668
Partin 19970.5880.0680.4950.682
Biopsy Gleason score0.5900.0630.4940.686
DRE0.6110.0220.5190.704
PSA0.6180.0150.5250.711
PSA density0.6390.0040.5480.731
TRUS0.6700.0000.5830.757
3D-PDS0.7760.0000.6990.852
image

Figure 3. Receiver operating characteristic (ROC) curve for values of prostate specific antigen (PSA) density and Gleason score and power Doppler sonography with 3D reconstruction (3D-PDS) findings.

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Multivariate analysis and prediction plots determining the risk of extraprostatic tumor extension

Looking for the clinically most important preoperative predictors of locally advanced prostate cancer, we carried out a multivariate logistic regression analysis. Its results are presented in Table 6. To fit the model, we used a set of variables describing age, prostate volume, PSA, PSA density, Gleason score, DRE, TRUS, and 3D-PDS. Only PSA density, a preoperative Gleason score ≥7, and 3D-PDS finding were statistically significant preoperative predictors of extraprostatic tumor extension.

Table 6.  Statistically significant preoperative predictors of extraprostatic tumor extension given by the model of multivariate logistic regression
 Odds ratio95.0% CI for odds ratioSig.
LowerUpper
  1. 3D-PDS, power Doppler sonography with 3D reconstruction; PSA, prostatic specific antigen.

PSA density17.671.38226.680.027
Gleason score
 ≥7 vs≤65.250.8034.310.084
3D-PDS
 T2 vs T1c3.270.8612.490.083
3D-PDS
 T3 vs T1c20.165.1479.080.000

The results of the multivariate analysis were used to derive prediction plots for the probability of locally advanced prostate cancer, when PSAD, Gleason score, and 3D-PDS findings are considered (Fig. 4). For example, a patient with a PSA density of 4.5 (i.e. preoperative PSA value 11.25 and prostate volume 25 mL determined by TRUS), with a prostate biopsy Gleason score of 5 and with a 3D-PDS finding of a visible tumor without signs of extracapsular penetration and seminal vesicle invasion (category cT2) has, according to plot 4B, a 40% probability of a locally advanced tumor in the definitive histological finding (Fig. 4B). Similarly, the risk of a locally advanced tumor can be assessed in patients with category cT1c established by 3D-PDS (Fig. 4A) or cT3 (Fig. 4C).

image

Figure 4. Probability plots for predicting locally advanced prostate carcinoma determined by the prostate specific antigen (PSA) density value, Gleason score, and power Doppler sonography with 3D reconstruction (3D-PDS) findings. Plot A is designated for patients with category cT1c established by 3D-PDS, plot B is designated for patients with category cT2 established by 3D-PDS, and plot C for patients with category cT3 established by 3D-PDS.

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Discussion

  1. Top of page
  2. Abstract
  3. Introduction
  4. Patients and methods
  5. Results
  6. Discussion
  7. Conclusion
  8. Acknowledgments
  9. References

Standard preoperative PSA, DRE, TRUS, and prostate biopsy examination misclassify the local tumor extent in 22–63% of cases.8 However, accurate preoperative estimation of the tumor extent is crucial both for the selection of definitive treatment strategy and for the indication of nerve sparing radical prostatectomy.

Our results show that 3D-PDS provides the best parameters of all of the compared diagnostic methods for extracapsular extension (ECE). The area under the ROC curve in 3D-PDS was 0.776 (P < 0.000) (Table 5).

Transrectal sonography (TRUS), due to its low sensitivity, is not an adequate tool for preoperative ECE prediction. Sonographic signs of ECE, irregular prostate outline in the area of the hypoechogenic finding of a prostate tumor, are usually used in TRUS. When using these ECE criteria, the sensitivity is about 20% and specificity 95%.14 Other studies report sensitivity in the range 23–66% and specificity 46–88%.11 The ECE criterion of a 23-mm long contact of a hypoechogenic tumor with a fibromuscular prostate capsule was used by Ukimura et al.15 With this criterion, they achieved 65% sensitivity and 88% specificity. Such results are undoubtedly dependent on the patient selection and histological characteristics of the tested prostate tumors. Utilization of this criterion is probably hindered by the fact that 40% of prostate tumors have no characteristic hypogenic lesions and are therefore undetectable by TRUS.16 In our study, there was 28% of such patients. The major contribution of transrectal sonography is therefore its role in prostate biopsy; its role in preoperative estimation of minimal ECE is rather negligible.

Doppler imaging provides essential information on tumor vascularization and vascular extension through the prostatic capsule to the standard TRUS. The results of color-Doppler mapping in ECE diagnostics are not very promising. Utilization of Power Doppler mapping, sensitive for the imaging of slow vascular flows, probably represents the main contribution. 3D reconstruction enables easier ECE assessment in the otherwise less accessible plane, and to our knowledge also markedly reduces the time of examination with the introduced transrectal probe in the rectum, which is usually negatively perceived by the patients. Sauvain et al.12 determined ECE by 3D-PDS in a group of 63 patients and obtained a sensitivity of 59.3%, a specificity of 94.4%, and an accuracy of 79.3%. They created three subgroups of a vascular pattern of prostate cancer and they analyzed an extraprostatic spread of the cancer in each subgroup. We did not create criteria that would allow us to make three subtypes of sonographic images, because we wanted to make clear and easy-to-follow criterion for discrimination in the ultrasound image. The criterion differentiating between these two types is the presence or absence of vascularization beyond the prostatic capsule (as is shown in Figs 1,5). Statistical evaluation of our study proved that the application of our criterion in the discrimination of T2 and T3 in 3D-PDS was statistically significant. With respect to the findings obtained in our study and the above-mentioned findings, we consider power Doppler sonography with 3D reconstruction the most adequate imaging method for the preoperative assessment of the local tumor extent (Tables 2,5). In the modern ultrasound era, a 3D module could be added to ultrasound equipment. In comparison to the purchase cost of MRI or other imaging modalities the purchase cost is low.

image

Figure 5. Power Doppler image of a localized prostate cancer.

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Another imaging method used for preoperative assessment of local tumor extent is endorectal MRI. In a set of 77 patients Yu et al. obtained 30% sensitivity and 95% specificity.17 Due to its low sensitivity, endorectal MRI does not fulfill criteria to be used for preoperative diagnostics of the local tumor extent. Another disadvantage of this method is its high cost and low accessibility.

The routinely used method for preoperative assessment of the risk of locally advanced tumors is based on nomograms estimating the ECE risk from the preoperative PSA, the Gleason score determined by prostate biopsy, and DRE. The accuracy of assessment of isolated extracapsular tumor penetration according to Partin tables is, however, lower than 60%.8 According to statistical evaluation in our study Partin tables failed to predict clinically localized prostate cancer. Partin tables were originally created according to the statistical evaluation of American men. We supposed that our group of patients could have been different to the study group of Partin. We think that PSA pre-testing was more prominent in the American population than in the Czech population. This could be a reason for such a high rate of pT3 tumors in our group of patients with clinically localized prostate cancer (42.46%). These differences in study groups could explain the failure of the Partin tables in our study group. For ECE prediction, particularly with regard to the indication of nerve sparing radical prostatectomy, several other types of nomograms have been proposed and validated. Ohori et al.18 increased its predictive value by adding the information obtained by prostate biopsy (the percentage of positive samples and the percentage of tumor occurrence in the entire bioptic material) to the routinely used standard ECE parameters (PSA, palpable tumor, Gleason score). To establish the specific ECE risk, Graefen et al.19 generated a side specific prediction nomogram evaluating the number of positive high-grade prostate biopsy cores, the total number of positive biopsy cores, and the preoperative PSA. None of these nomograms, however, uses an imaging technique that would estimate the local tumor extent with adequate reliability.

Multivariate analysis of our set of patients has shown that the PSAD, Gleason score, and 3D-PDS finding represent the most powerful predictors of ECE. PSA density has shown to be a better predictor than PSA. In accordance with other authors we have shown that PSA density is a statistically significant predictor of ECE.20,21 Although studies investigating the contribution of PSA density to prostate biopsy indications are controversial,22 PSA density as an ECE predictor belongs to significant parameters.

The Gleason score established by preoperative prostate biopsy also represents a good ECE predictor.8,20 According to our analysis, the presence of a histologically aggressive tumor (Gleason score ≥7) is a prognostically significant factor of ECE.

The multivariate analysis of our observed group has shown that the 3D-PDS imaging modality is one of the most powerful predictors of ECE occurrence. These results suggest that the sonographic findings of ECE in 3D-PDS are reliable signs of ECE presence in the radical prostatectomy specimen. Newly generated prediction plots (Fig. 4a–c) more accurately define the risk of locally advanced prostate cancer using three important predictors of extracapsular extension; that is, PSA density, the presence of cancer, a Gleason score ≥7 at biopsy, and 3D-PDS findings.

Conclusion

  1. Top of page
  2. Abstract
  3. Introduction
  4. Patients and methods
  5. Results
  6. Discussion
  7. Conclusion
  8. Acknowledgments
  9. References

According to the analysis of our study group, prostate imaging by power Doppler sonography with 3D reconstruction represents the most reliable preoperative diagnostic tool to establish extracapsular tumor extension and seminal vesicle invasion. Together with PSA density and the presence of an aggressive tumor (Gleason score ≥7) in prostate biopsy, it belongs to statistically and clinically significant predictors of locally advanced prostate cancer. The inclusion of the 3D-PDS findings, instead of DRE or TRUS into newly generated prediction plots contributes significantly to the greater accuracy of preoperative diagnostics of the local extent of prostate cancer.

Acknowledgments

  1. Top of page
  2. Abstract
  3. Introduction
  4. Patients and methods
  5. Results
  6. Discussion
  7. Conclusion
  8. Acknowledgments
  9. References

There was no financial support or relationships that may pose conflict of interest.

References

  1. Top of page
  2. Abstract
  3. Introduction
  4. Patients and methods
  5. Results
  6. Discussion
  7. Conclusion
  8. Acknowledgments
  9. References
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