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Endorectal MR Imaging in the Evaluation of Seminal Vesicle Invasion: Diagnostic Accuracy and Multivariate Feature Analysis¹

¹ From the Departments of Radiology (E.S., O.A., H.F.E., B.R., H.H.), Epidemiology and Biostatistics (C.S.M., N.M.I.), Pathology (K.K.), and Urology (P.T.S.), Memorial Sloan-Kettering Cancer Center, 1275 York Ave, New York, NY 10021. From the 2005 RSNA Annual Meeting. Received April 20, 2005; revision requested June 16; revision received July 5; final version accepted July 28. Supported by grant R01-CA76423 from the National Institutes of Health. Address correspondence to H.H.

	ABSTRACT

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION ADVANCES IN KNOWLEDGE References

 
Purpose: To retrospectively determine the accuracy of endorectal magnetic resonance (MR) imaging in demonstrating seminal vesicle invasion (SVI) and to investigate the MR imaging features that can predict SVI.

Materials and Methods: The Institutional Review Board granted exempt status for this retrospective study, with waiver of informed consent; patient data were collected and handled in accordance with HIPAA regulations. Fifty-one men (age range, 44–73 years) with SVI and 303 men (age range, 40–76 years) without SVI who underwent endorectal MR imaging before radical prostatectomy between January 2000 and October 2004 were included in the study. Endorectal MR images were retrospectively and independently analyzed by two radiologists for SVI, tumor at prostate base, extracapsular extension, and other features considered indicative of SVI. Areas under the receiver operating characteristic curves (AUCs) were used to assess the accuracy of detecting SVI at endorectal MR imaging. A multiple logistic regression was used to explore the combinations of MR imaging features that might facilitate the detection of SVI.

Results: Readers 1 and 2 had an AUC of 0.93 and 0.81, respectively, for the detection of SVI. For both readers, the features that had the highest sensitivity and specificity were low signal intensity within the seminal vesicle and lack of preservation of seminal vesicle architecture. At multiple regression analysis, tumor at the prostate base that extended beyond the capsule and low signal intensity within a seminal vesicle that has lost its normal architecture were highly predictive of SVI.

Conclusion: Endorectal MR imaging is accurate in demonstrating SVI prior to radical prostatectomy, and recognition of the most predictive features may facilitate the use of this modality.

© RSNA, 2006

	INTRODUCTION

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION ADVANCES IN KNOWLEDGE References

 
In patients with newly diagnosed prostate cancer, the presence of seminal vesicle invasion (SVI) is associated with high rates of treatment failure and tumor recurrence (1–5). Reported progression rates in these patients range from 40% to 95% (1,3,6). Factors associated with an increased incidence of SVI are a high prostate-specific antigen (PSA) level, a high Gleason score, the presence of tumor at the base of the prostate gland, and lymph node metastasis (7–9). The prevalence of SVI, as reported in current surgical series, is 4%–12% (5,10,11).

For patients with prostate cancer, the preoperative identification of SVI is an important factor in staging and prognosis and affects treatment decisions and planning (5,9). Enthusiasm for performing seminal vesicle biopsy during routine preoperative work-up has been limited by the low prevalence of SVI in patients with prostate cancer, the low sensitivity of the test, and the high rate of false-positive results (12,13).

Clinical staging nomograms that are based on preoperative clinical variables are routinely used to predict SVI in patients with prostate cancer; these nomograms assist in directing adjuvant therapy and in guiding postoperative counseling (14,15). The use of additional preoperative variables (ie, imaging findings) to enhance the specificity and sensitivity of the present models is of great interest. Moreover, unlike imaging findings, nomograms do not provide anatomic data that can assist in surgical interventions.

Endorectal magnetic resonance (MR) imaging is useful in demonstrating SVI in patients with prostate cancer; the sensitivities and specificities that are reported in the literature, however, vary widely (16–22). To the best of our knowledge, no study has been performed to identify the endorectal MR imaging features that are indicative of SVI. The purpose of our study was to retrospectively determine the accuracy of endorectal MR imaging in demonstrating SVI and to investigate the MR imaging features that can help predict SVI.

	MATERIALS AND METHODS

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION ADVANCES IN KNOWLEDGE References

 
This was a retrospective, single-institution cross-sectional study. The Institutional Review Board granted exempt status for the study, with a waiver of informed consent. Patient data were collected and handled in accordance with the Health Insurance Portability and Accountability Act regulations.

Between January 1, 2000, and October 31, 2004, 612 patients with histologically diagnosed prostate carcinoma who were enrolled in an ongoing National Institutes of Health study were referred for combined endorectal and phased-array coil MR imaging of the prostate gland before radical prostatectomy. Patient charts and MR images were subsequently reviewed to determine if the patients met the following inclusion criteria for this retrospective study: (a) SVI at step-section histopathologic examination (70 patients), (b) no radiation, chemo-, or hormone therapy prior to surgery (54 patients), and (c) complete endorectal coil transverse T1-weighted and T2-weighted MR images that were retrievable for review (51 patients). Fifty-one patients met all the inclusion criteria. On the basis of sample size calculations, which took into account the fact that SVI prevalence in current surgical series is around 14%, 303 consecutive patients with no SVI at step-section histopathologic examination were selected from the same database. These patients had not undergone radiation, chemo-, or hormone therapy prior to surgery but had undergone complete endorectal MR imaging of the prostate. Patient characteristics are presented in Table 1.

MR Imaging Analysis
Images were retrospectively and independently analyzed by two radiologists (E.S., O.A.) who were unaware of the clinical, surgical, and histologic findings. Each radiologist had completed a body MR imaging fellowship and had read more than 500 MR images of the prostate. Prior to image interpretation, the readers met with other coauthors to agree on which MR features would be used in the diagnosis of SVI and to design the data collection form. Each reader independently completed a data collection form for each case.

For each patient, the radiologists assigned scores for the presence or absence of (a) SVI, (b) tumor at the base of the prostate gland, and (c) extracapsular extension (ECE). Scores were assigned on a scale of 1–5 (score of 1, definitely absent; score of 2, probably absent; score of 3, possibly present; score of 4, probably present; and score of 5, definitely present). For each feature, the left and right sides of the prostate were scored separately.

The radiologists also evaluated each seminal vesicle for several imaging features that were considered to be associated with SVI, as described in the MR imaging, ultrasonography, and pathology literature (15,23–25).

The first feature was lack of preservation of normal architecture in the seminal vesicle. On T2-weighted MR images, normal seminal vesicles demonstrate a grapelike configuration, with high-signal-intensity fluid and a low-signal-intensity wall. When seminal vesicles are invaded by tumor, they display an area of homogeneous low signal intensity that is indistinguishable from that of the adjacent wall. The presence of hemorrhage can also result in low signal intensity. With hemorrhage, however, the lower signal intensity of the wall is preserved.

The second feature was the presence of focal or diffuse low signal intensity within the seminal vesicle. This feature should not be confused with the low signal intensity commonly found in the area of the ductus deferens, which is caused by the presence of blood in the fluid after biopsy. Hemospermia is a common complication of prostate biopsy and can persist for 6–8 weeks. Hemospermia is often seen as a region of low signal intensity on T2-weighted MR images. In patients with hemospermia (unlike those with tumor), the normal architecture of the seminal vesicle is preserved.

Other features that are associated with SVI included low signal intensity within the seminal vesicle, which causes mass effect; thickening of the ductus deferens; expanded low-signal-intensity ejaculatory ducts; obliteration of the angle between the prostate and seminal vesicle on sagittal MR images; and noncontinuous areas of low signal intensity within the seminal vesicle (metastatic).

All features were recorded by each reader as being either present or absent (Figs 1, 2). The presence or absence of hemorrhage and/or calcifications within the seminal vesicles was also recorded, although such findings were not considered features of SVI.

View larger version (158K): [in this window] [in a new window] [Download PPT slide]   Figure 1a: Clinical stage T2a prostate cancer in 61-year-old man with Gleason score of 9 and PSA level of 8.45 ng/mL. (a, b) Transverse, (c) coronal, and (d) sagittal T2-weighted fast spin-echo (5800/100) MR images show tumor (T) and ECE (arrow in a and c) at right side of prostate base. Seminal vesicles demonstrate low signal intensity, mass effect, and loss of normal architecture (b–d). Angle obliteration (arrow in d) is noted. (e, f) Corresponding whole-mount sections confirm tumor (T) and bilateral SVI. RSV = right seminal vesicle, LSV = left seminal vesicle.

View larger version (146K): [in this window] [in a new window] [Download PPT slide]   Figure 1b: Clinical stage T2a prostate cancer in 61-year-old man with Gleason score of 9 and PSA level of 8.45 ng/mL. (a, b) Transverse, (c) coronal, and (d) sagittal T2-weighted fast spin-echo (5800/100) MR images show tumor (T) and ECE (arrow in a and c) at right side of prostate base. Seminal vesicles demonstrate low signal intensity, mass effect, and loss of normal architecture (b–d). Angle obliteration (arrow in d) is noted. (e, f) Corresponding whole-mount sections confirm tumor (T) and bilateral SVI. RSV = right seminal vesicle, LSV = left seminal vesicle.

View larger version (154K): [in this window] [in a new window] [Download PPT slide]   Figure 1c: Clinical stage T2a prostate cancer in 61-year-old man with Gleason score of 9 and PSA level of 8.45 ng/mL. (a, b) Transverse, (c) coronal, and (d) sagittal T2-weighted fast spin-echo (5800/100) MR images show tumor (T) and ECE (arrow in a and c) at right side of prostate base. Seminal vesicles demonstrate low signal intensity, mass effect, and loss of normal architecture (b–d). Angle obliteration (arrow in d) is noted. (e, f) Corresponding whole-mount sections confirm tumor (T) and bilateral SVI. RSV = right seminal vesicle, LSV = left seminal vesicle.

View larger version (144K): [in this window] [in a new window] [Download PPT slide]   Figure 1d: Clinical stage T2a prostate cancer in 61-year-old man with Gleason score of 9 and PSA level of 8.45 ng/mL. (a, b) Transverse, (c) coronal, and (d) sagittal T2-weighted fast spin-echo (5800/100) MR images show tumor (T) and ECE (arrow in a and c) at right side of prostate base. Seminal vesicles demonstrate low signal intensity, mass effect, and loss of normal architecture (b–d). Angle obliteration (arrow in d) is noted. (e, f) Corresponding whole-mount sections confirm tumor (T) and bilateral SVI. RSV = right seminal vesicle, LSV = left seminal vesicle.

View larger version (105K): [in this window] [in a new window] [Download PPT slide]   Figure 1e: Clinical stage T2a prostate cancer in 61-year-old man with Gleason score of 9 and PSA level of 8.45 ng/mL. (a, b) Transverse, (c) coronal, and (d) sagittal T2-weighted fast spin-echo (5800/100) MR images show tumor (T) and ECE (arrow in a and c) at right side of prostate base. Seminal vesicles demonstrate low signal intensity, mass effect, and loss of normal architecture (b–d). Angle obliteration (arrow in d) is noted. (e, f) Corresponding whole-mount sections confirm tumor (T) and bilateral SVI. RSV = right seminal vesicle, LSV = left seminal vesicle.

View larger version (82K): [in this window] [in a new window] [Download PPT slide]   Figure 1f: Clinical stage T2a prostate cancer in 61-year-old man with Gleason score of 9 and PSA level of 8.45 ng/mL. (a, b) Transverse, (c) coronal, and (d) sagittal T2-weighted fast spin-echo (5800/100) MR images show tumor (T) and ECE (arrow in a and c) at right side of prostate base. Seminal vesicles demonstrate low signal intensity, mass effect, and loss of normal architecture (b–d). Angle obliteration (arrow in d) is noted. (e, f) Corresponding whole-mount sections confirm tumor (T) and bilateral SVI. RSV = right seminal vesicle, LSV = left seminal vesicle.

View larger version (127K): [in this window] [in a new window] [Download PPT slide]   Figure 2a: Clinical stage T2c prostate cancer in 63-year-old man with Gleason score of 8 and PSA level of 56.24 ng/mL. (a) Transverse T1-weighted (500/10) MR image and (b) transverse, (c) coronal, and (d) sagittal T2-weighted fast spin-echo (5800/100) MR images show right SVI (T). Note the presence of extensive hemorrhage in both seminal vesicles (high signal intensity in a). In b–d, a focal area of low signal intensity (T) is seen in the right seminal vesicle. This area causes mass effect and distortion of the normal architecture of the seminal vesicle, which are both indicative of SVI.

View larger version (174K): [in this window] [in a new window] [Download PPT slide]   Figure 2b: Clinical stage T2c prostate cancer in 63-year-old man with Gleason score of 8 and PSA level of 56.24 ng/mL. (a) Transverse T1-weighted (500/10) MR image and (b) transverse, (c) coronal, and (d) sagittal T2-weighted fast spin-echo (5800/100) MR images show right SVI (T). Note the presence of extensive hemorrhage in both seminal vesicles (high signal intensity in a). In b–d, a focal area of low signal intensity (T) is seen in the right seminal vesicle. This area causes mass effect and distortion of the normal architecture of the seminal vesicle, which are both indicative of SVI.

View larger version (176K): [in this window] [in a new window] [Download PPT slide]   Figure 2c: Clinical stage T2c prostate cancer in 63-year-old man with Gleason score of 8 and PSA level of 56.24 ng/mL. (a) Transverse T1-weighted (500/10) MR image and (b) transverse, (c) coronal, and (d) sagittal T2-weighted fast spin-echo (5800/100) MR images show right SVI (T). Note the presence of extensive hemorrhage in both seminal vesicles (high signal intensity in a). In b–d, a focal area of low signal intensity (T) is seen in the right seminal vesicle. This area causes mass effect and distortion of the normal architecture of the seminal vesicle, which are both indicative of SVI.

View larger version (158K): [in this window] [in a new window] [Download PPT slide]   Figure 2d: Clinical stage T2c prostate cancer in 63-year-old man with Gleason score of 8 and PSA level of 56.24 ng/mL. (a) Transverse T1-weighted (500/10) MR image and (b) transverse, (c) coronal, and (d) sagittal T2-weighted fast spin-echo (5800/100) MR images show right SVI (T). Note the presence of extensive hemorrhage in both seminal vesicles (high signal intensity in a). In b–d, a focal area of low signal intensity (T) is seen in the right seminal vesicle. This area causes mass effect and distortion of the normal architecture of the seminal vesicle, which are both indicative of SVI.

Statistical Analysis
The Fisher exact test was used to compare the distribution of tumor presence at the prostate base, ECE, and Gleason score between patients with and those without SVI. The Wilcoxon rank sum test was used to compare the distribution of PSA levels between these two groups of patients. We used a receiver operating characteristic (ROC) curve analysis to evaluate each radiologist's accuracy in using MR imaging to detect SVI, tumor at the prostate base, and ECE. For this analysis, the side (right versus left) of the prostate was used as the unit of analysis. The area under the ROC curve (AUC) and the corresponding confidence intervals were estimated by using the methods described by Obuchowski (26), which accounted for correlations owing to multiple observations per patient. To assess the interrater variability in determining tumor location, we used a weighted statistic with weights 1–|i–j|/(5–1), where i, j = 1,...,5 denote the rating categories for the first and second readers, respectively (27,28).

A multiple logistic regression analysis was used to explore which combinations of MR imaging features might be helpful in predicting SVI. Scores for tumor at the base of the prostate and ECE were dichotomized, with a score of 3 or more indicating the presence of tumor at the prostate base or ECE. The choice of a threshold score of 3 was based on the results of prior ROC curve analyses. Stepwise methods were used to generate the final model. Parameters and standard errors were estimated by using generalized estimating equations (29), with an independence working covariance matrix to account for the multiple observations per subject. For model validation, the predicted probabilities were calculated for each patient by using the testing data, and an ROC curve analysis was used to assess the accuracy of the predicted probabilities.

To determine whether a radiologist's assessment of the presence of hemorrhage affected his or her accuracy, we modeled the effect of this assessment on the ROC curve by using methods described by Pepe (30). We fit the model logit ROC(t) = ₀ + ₁(logit t) + ß₀(reader) + ß₁(hemorrhage). By testing this model with a ß₁ value of 0, one can determine whether hemorrhage significantly affected a radiologist's accuracy. All analyses were performed with Windows-based software programs (Stata 8.0, Stata, College Station, Tex; S-Plus 6.2, Insightful, Seattle, Wash).

	RESULTS

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Surgical and Histopathologic Findings
Seventeen patients had invasion of both seminal vesicles, 20 had invasion of the left seminal vesicle, and 14 had invasion of the right seminal vesicle. The median baseline serum PSA level was 7.3 ng/mL (range, 3.3–72.0 ng/mL) for patients with SVI and 5.7 ng/mL (range, 0.15–28.0 ng/mL) for patients without SVI (Table 1); the difference between these two groups was statistically significant (P < .001). The median Gleason score for patients with SVI was 3 + 4, while the median Gleason score for patients without SVI was 3 + 3. There was a significant difference in the distribution of Gleason scores between patients with and those without SVI (P < .001) (Table 1).

At pathologic examination, all patients with SVI had tumor at the base of the prostate, whereas only 114 (38%) of 303 patients without SVI had tumor at the base of the prostate; the difference was statistically significant (P < .001). Of the 51 patients with pathologically confirmed SVI, 47 (92%) had ECE. Of the 303 patients without SVI, only 57 (19%) had ECE. This difference was statistically significant (P < .001).

MR Imaging Findings
Detection of SVI.—For readers 1 and 2, ROC curves for the detection and localization of SVI (Fig 3) showed that reader 1 had an AUC of 0.93 (95% confidence interval: 0.89, 0.97) and reader 2 had an AUC of 0.81 (95% confidence interval: 0.74, 0.88). The weighted statistic was 0.62, which indicated moderate agreement between readers. The identification of hemorrhage within the seminal vesicle had no significant effect on the ability of the readers to accurately detect SVI (P = .30). An AUC of 1.00 was noted when reader 1 found hemorrhage, and an AUC of 0.86 was noted when reader 1 did not find hemorrhage. Likewise, an AUC of 0.92 was noted when reader 2 found hemorrhage, and an AUC of 0.81 was noted when reader 2 did not find hemorrhage.

View larger version (30K): [in this window] [in a new window] [Download PPT slide]   Figure 3: ROC curves summarize the accuracy of endorectal MR imaging in demonstrating and localizing SVI.

View larger version (30K): [in this window] [in a new window] [Download PPT slide]   Figure 4a: ROC curves summarize the accuracy of endorectal MR imaging in demonstrating and localizing (a) tumor at the base of prostate and (b) ECE in patients with SVI.

View larger version (31K): [in this window] [in a new window] [Download PPT slide]   Figure 4b: ROC curves summarize the accuracy of endorectal MR imaging in demonstrating and localizing (a) tumor at the base of prostate and (b) ECE in patients with SVI.

The three different models are summarized in Table 6. In model 1, reader 1 had an AUC of 0.55, and reader 2 had an AUC of 0.48. In model 2, AUC increased from 0.55 to 0.93 (P < .01) for reader 1 and from 0.48 to 0.55 (P = .02) for reader 2. In model 3, AUC further increased from 0.93 to 0.97 (P = .02) for reader 1 and from 0.55 to 0.67 (P = .03) for reader 2. Figure 5 shows the ROC curves of the three multivariate models for reader 1 only.

View larger version (35K): [in this window] [in a new window] [Download PPT slide]   Figure 5: ROC curves summarize the accuracy of three multivariate models in detecting and localizing SVI for reader 1.

	DISCUSSION

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Accurate pretreatment diagnosis of SVI has important implications in guiding therapy for prostate cancer (5). Of the available diagnostic imaging modalities, MR imaging has shown the most promise for accurate local staging because it has both high spatial and high contrast resolution. In our study, only 1% of patients with SVI had accurate clinical staging, whereas the presence or absence of SVI was accurately diagnosed at MR imaging in more than 90% of the patients. In previous studies, accuracy levels for the diagnosis of SVI were in the range of 85%, whereas sensitivities and specificities ranged from 50% to 71% and from 66% to 95%, respectively (16–21). In a previous meta-analysis on the local staging of prostate cancer by using MR imaging, the summary ROC curve for the detection of SVI had a joint maximum sensitivity and specificity of 80%. At a specificity of 95%, however, the sensitivity was 27% (22).

Low signal intensity within the seminal vesicle and lack of preservation of the normal architecture of the seminal vesicle were the two features that yielded the highest sensitivity and specificity for both readers. Expansion of the ejaculatory ducts and obliteration of the angle between the prostate gland and the seminal vesicle were not sensitive but were highly specific for SVI, indicating that when these features are confidently detected at MR imaging, they are highly suggestive of SVI. Based on the ROC curves for the three prediction models, it appears that the combination of tumor at the base of the prostate gland and ECE with SVI features is more helpful than any SVI feature alone in predicting SVI. The combinations of features that are predictive of SVI, however, will vary for different readers. Though both readers were considered experienced specialists in interpretation, we found a fair amount of interobserver variability, as is shown by statistics ranging from 0.42 to 0.62 for tumor detection and localization. The fact that MR image interpretation in the prostate is subject to considerable interobserver variability has been an ongoing issue.

In this study, we found significant relationships between SVI and the presence of tumor at the base of the prostate, Gleason score, and PSA level. These findings are in agreement with those described in the published literature (5,7,11,15,31). Previously, Koh et al (15) reported that PSA level, Gleason score, and the percentage of cancer at the base of the prostate were significant and independent predictors of SVI.

Although, to date, ours is the largest study to have evaluated SVI with preoperative endorectal MR imaging and pathologic correlation, our study was limited by its retrospective design and relatively small sample size. Another limitation of our study was the potential for verification bias because, for the past 2 years at our institution, endorectal MR imaging has been performed on every patient in whom radical prostatectomy is being considered. The results of endorectal MR imaging may therefore have contributed to the decision to either perform or cancel radical prostatectomy. This bias might have led to inflated estimates of AUC, sensitivity, and specificity and to better selection for organ-confined disease at surgery.

In summary, the results suggest that endorectal MR imaging is accurate in demonstrating SVI prior to radical prostatectomy. A combination of tumor at the base of the prostate that extends beyond the capsule and low signal intensity within a seminal vesicle that has lost its normal architecture is highly predictive of SVI. Information obtained at endorectal MR imaging should be incorporated into the criteria that are used to select patients for radical prostatectomy and may aid in surgical planning.

	ADVANCES IN KNOWLEDGE

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION ADVANCES IN KNOWLEDGE References

 

• Endorectal MR imaging is highly accurate in demonstrating seminal vesicle invasion prior to radical prostatectomy.
  
• On endorectal MR images, a combination of tumor at the base of the prostate that extends beyond the capsule and low signal intensity within a seminal vesicle that has lost its normal architecture is highly predictive of seminal vesicle invasion.
  

	ACKNOWLEDGMENTS

 
The authors thank Ada Muellner, BA, for her assistance in editing the manuscript.

	FOOTNOTES

 

Abbreviations: AUC = area under ROC curve • ECE = extracapsular extension • PSA = prostate-specific antigen • ROC = receiver operating characteristic • SVI = seminal vesicle invasion

Authors stated no financial relationship to disclose.

Author contributions: Guarantors of integrity of entire study, E.S., O.A., H.H.; study concepts/study design or data acquisition or data analysis/interpretation, all authors; manuscript drafting or manuscript revision for important intellectual content, all authors; approval of final version of submitted manuscript, all authors; literature research, E.S., O.A., B.R.; clinical studies, E.S., O.A., H.F.E., B.R.; statistical analysis, C.S.M., H.F.E., N.M.I.; and manuscript editing, E.S., O.A., N.M.I., H.H.

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TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION ADVANCES IN KNOWLEDGE References

 

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