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Published online before print November 7, 2006, 10.1148/radiol.2421051254
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(Radiology 2007;242:182-188.)
© RSNA, 2006

Genitourinary Imaging

Prediction of Seminal Vesicle Invasion in Prostate Cancer: Incremental Value of Adding Endorectal MR Imaging to the Kattan Nomogram1

Liang Wang, MD, Hedvig Hricak, MD, PhD, Michael W. Kattan, PhD, Hui Ni Chen, MS, Kentaro Kuroiwa, MD, PhD, Halley F. Eisenberg, BS and Peter T. Scardino, MD

1 From the Departments of Radiology (L.W., H.H., H.N.C., H.F.E.) and Urology (K.K., P.T.S.), Memorial Sloan-Kettering Cancer Center, 1275 York Ave, New York, NY 10021; and Department of Quantitative Health Sciences, Cleveland Clinic Foundation, Cleveland, Ohio (M.W.K.). Received July 26, 2005; revision requested September 13; revision received January 23, 2006; accepted February 13; final version accepted May 19. Supported by National Institutes of Health grant R01 CA76423. Address correspondence to L.W. (e-mail: wang6{at}mskcc.org).


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 ADVANCES IN KNOWLEDGE
 References
 
Purpose: To retrospectively determine whether endorectal magnetic resonance (MR) imaging findings contribute incremental value to the Kattan nomogram for predicting seminal vesicle invasion (SVI) in patients with prostate cancer.

Materials and Methods: The institutional review board issued a waiver of authorization, which included a waiver of informed consent, for this HIPAA-compliant study. From October 2000 through January 2005, 573 patients (mean age, 58.3 years; age range, 36–86 years) underwent endorectal MR imaging before prostate cancer surgery. The endorectal MR imaging results had been prospectively interpreted by seven radiologists, and the likelihood of SVI was retrospectively scored on the basis of radiologists' written reports. MR imaging findings, individual clinical variables (serum prostate-specific antigen [PSA] level, Gleason grade, clinical stage, greatest percentage of cancer in all biopsy cores, percentage of positive cores in all biopsy cores, and perineural invasion), and the Kattan nomogram were evaluated with respect to SVI prediction; surgical pathologic analysis was used as the reference standard. Logistic regression and receiver operating characteristic (ROC) curve analyses were performed.

Results: At pathologic analysis, 28 (4.9%) of 573 patients had SVI. At univariate analysis, endorectal MR imaging results and all clinical variables except the percentage of positive biopsy cores were significantly associated with SVI (P < .02); endorectal MR imaging (0.76) had a larger area under the ROC curve (AUC) than any clinical variable (0.62–0.73). At multivariate analysis, endorectal MR imaging results, Gleason grade, PSA level, and the percentage of cancer in all biopsy cores were significantly associated with SVI (P ≤ .02). The Kattan nomogram plus endorectal MR imaging (0.87) had a significantly larger (P < .05) AUC than either endorectal MR imaging alone (0.76) or the Kattan nomogram alone (0.80).

Conclusion: The addition of endorectal MR imaging contributes significant incremental value to the Kattan nomogram for predicting SVI.

© RSNA, 2006


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 ADVANCES IN KNOWLEDGE
 References
 
Prostate cancer has the highest incidence of any noncutaneous cancer in the United States and is the third leading cause of cancer death in American men (1). The American Cancer Society has estimated that in 2006 in the United States, 234 460 new cases of prostate cancer will be diagnosed and 27 350 men will die of the disease (1). The prevalence of seminal vesicle invasion (SVI) in contemporary surgical series (ie, those series performed in the past 10 years) is 5%–23% (2–16). Preoperative identification of SVI is an important factor for staging and prognosis and may modify treatment selection and treatment planning (4,12,17).

The prognosis, however, depends on the status of other tumor prognostic variables and is not always poor. In a recent study (4), the 5-year biochemical progression-free rate for patients with SVI was 71.9% when surgical margins and nodes were negative, 36.6% when surgical margins were positive and nodes were negative, and 25.9% when surgical margins and nodes were positive.

Clinical factors associated with an increased incidence of SVI include a high prostate-specific antigen (PSA) level, a high Gleason grade, the presence of tumor at the base of the prostate gland, and lymph node metastasis (3,4,18,19). To replace somewhat arbitrary combinations of individual clinical variables, nomograms have been introduced to help predict the stage of prostate cancer and to aid in the choice of treatment (3,20–22). The Kattan staging nomogram, which is based on presurgical clinical variables (serum PSA level, Gleason grade at biopsy, clinical stage, and systematic needle biopsy cores from the base of the prostate), is a validated predictive instrument that is widely used to help direct adjuvant therapy and to guide postoperative counseling for patients with clinical data suggestive of SVI (3,23). However, the Kattan staging nomogram cannot predict the location of SVI. Of the modern diagnostic imaging modalities, endorectal magnetic resonance (MR) imaging has shown the most promise in the detection of prostate cancer SVI, with high specificity (81%–99%) but widely varying sensitivity (23%–80%) (6–9,14–16,24).

In historical studies on the detection of SVI with MR imaging, the disease was often relatively advanced, and the contribution of MR findings to clinical nomograms was not assessed (5–9,14–16,24). Thus, the purpose of our study was to retrospectively determine whether endorectal MR imaging findings contribute incremental value to the Kattan nomogram for predicting SVI in patients with prostate cancer.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 ADVANCES IN KNOWLEDGE
 References
 
Patients
A total of 592 consecutive patients with prostate cancer were referred from the urology department to undergo MR imaging before radical retropubic prostatectomy and pelvic lymphadenectomy, which were performed at our institution by one of six attending surgeons, one of whom was an author (P.T.S.) (Table 1). For the six attending surgeons, the range of experience in prostate surgery was 10–35 years. From October 2000 through June 2003, imaging was performed as part of an ongoing National Institutes of Health study investigating the use of MR imaging in patients with prostate cancer; all patients gave informed consent before enrollment in the prospective institutional review board–approved National Institutes of Health study, which was compliant with the Health Insurance Portability and Accountability Act. From July 2003 to January 2005, imaging was performed as part of our accepted clinical practice for patient evaluation. The institutional review board of the Memorial Sloan-Kettering Cancer Center issued a waiver of authorization (which includes a waiver of informed consent) for retrospective review of the MR imaging reports and clinical data; this review was also compliant with the Health Insurance Portability and Accountability Act.


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  		Table 1. Distribution of Preoperative Clinical Variables

 
For 19 of 592 patients, no needle biopsy cores from the base of the prostate were available, and thus the likelihood of SVI on the basis of the Kattan nomogram could not be calculated (3). Therefore, data analysis was based on the remaining 573 patients (mean age, 58.3 years; age range, 36–86 years). None of the 573 patients underwent neoadjuvant hormonal therapy or radiation therapy prior to surgery. The average time between biopsy and MR imaging was 71.73 days (range, 1042 days before MR imaging to 114 days after MR imaging), and the average time from MR imaging to surgery was 38.40 days (range, 1–185 days).

In all patients, prostate cancer was diagnosed by means of biopsy specimens. Clinical serum PSA levels, Gleason grade at biopsy, clinical stage, the greatest percentage of cancer in all biopsy cores, the percentage of positive cores in all biopsy cores, and perineural invasion (PNI) were recorded from the patients' medical records (K.K.). A portion of the patient population has been reported on previously (25–28).

Kattan Staging Nomogram
For all 573 patients, the likelihood of SVI according to the Kattan nomogram was recorded by two authors (L.W. and K.K. working together) on the basis of serum PSA levels, Gleason grade at biopsy, clinical stage, and systematic needle biopsy cores from the base of the prostate (3).

MR Data Acquisition and Interpretation
MR imaging was performed with a 1.5-T whole-body MR imager (Signa Horizon; GE Medical Systems, Milwaukee, Wis). Patients were examined in the supine position by using the body coil for excitation and a pelvic phased-array coil (GE Medical Systems) in combination with a commercially available balloon-covered expandable endorectal coil (Medrad, Pittsburgh, Pa) for signal reception. T1-weighted transverse and spin-echo MR images were obtained from the aortic bifurcation to the symphysis pubis by using the following parameters: repetition time, 700 msec; echo time, 8 msec; section thickness, 5 mm; intersection gap, 1 mm; field of view, 24 cm; matrix, 256 x 192; transverse frequency direction (to prevent obstruction of the pelvic node by endorectal coil motion artifact); and one signal acquired. Thin-section high-spatial-resolution transverse and coronal T2-weighted fast spin-echo MR images of the prostate and seminal vesicles were obtained by using the following parameters: repetition time, 5000 msec; effective echo time, 96 msec; echo train length, 16; section thickness, 3 mm; no intersection gap; field of view, 14 cm; matrix, 256 x 192; anteroposterior frequency direction (to prevent obstruction of the prostate by endorectal coil motion artifact); and four signals acquired.

MR images were prospectively interpreted by seven attending MR body radiologists, one of whom was an author (H.H.); images were interpreted independently during the regular clinical assignment of each radiologist to the MR service. Six of the readers had performed a fellowship in body imaging that included MR imaging. The experience of each radiologist in reading MR images since fellowship ranged from 1 to 13 years, with one reader having more than 20 years of experience interpreting MR images. All of the readers had experience in prostate imaging and were members of the institution's prostate cancer disease management team. As per regular clinical practice, the readers were not blinded to clinical data, such as PSA level and biopsy results; however, the amount of clinical data that was available varied. Each radiologist made his or her determination regarding the presence of SVI on the basis of his or her own continuous medical training and knowledge of previously described MR features of SVI.

The main diagnostic criteria used by the radiologists to determine the presence of SVI on MR images were the disruption or loss of the normal architecture of the seminal vesicle, focal or diffuse areas of low signal intensity within the seminal vesicle, low signal intensity within the seminal vesicle causing mass effect, enlarged ejaculatory ducts with low signal intensity, and direct extension of the low signal intensity of tumor from the base of the prostate to the seminal vesicle (24). On the basis of the radiologists' written reports, one author (L.W.) independently and retrospectively scored the likelihood of SVI on a scale of 1–5, with a score of 1 indicating no SVI; 2, probably no SVI (ie, SVI cannot be ruled out, although there is no clear evidence); 3, possible SVI (lesion is suspicious for SVI); 4, probable SVI (lesion is highly suspicious for SVI); and 5, definite SVI.

Histopathologic Analysis
Pretreatment sextant biopsy reports provided the following clinical parameters, which were used for prediction of SVI: Gleason grade, the greatest percentage of cancer in all biopsy cores, the percentage of positive cores in all biopsy cores, and PNI. Radical prostatectomy specimens had been examined by the institutional pathology department. Prostatectomy specimens were inked with tattoo dye (green dye on the right side and blue dye on the left side), and the specimens were fixed in 10% formalin for 36 hours. The distal 5 mm of the apex was amputated and coned. The remainder of the gland was serially sectioned from the apex to the base at 3–4-mm intervals and was entirely submitted for paraffin embedding as whole-mount sections. The seminal vesicles were amputated and submitted separately. After paraffin embedding, microsections were placed on glass slides and were stained with hematoxylin and eosin. One uropathologist (K.K.) subsequently reviewed all the specimens, mapped each tumor area with a marker (green for a Gleason grade of 3 and black for a Gleason grade of 4 or a mixture of Gleason grades 4 and 5), and recorded the presence and location of SVI (Fig 1).


Figure 1
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  		Figure 1a: pT4 prostate cancer (clinical stage T2b with PSA level of 12.42 ng/mL) and bilateral seminal vesicle involvement in a 63-year-old man. Sextant biopsy results showed Gleason grade 4 + 3 tumors involving 50% of the total submitted tissue on both sides (94% of total submitted cores were positive) and PNI in left peripheral and transition zones. According to the Kattan staging nomogram, the likelihood of SVI was 18%. (a) Transverse T2-weighted fast spin-echo 3-mm-thick MR image (4900/118 [repetition time msec/effective echo time msec]) and (b) coronal T2-weighted fast spin-echo 3-mm-thick MR image (4666/96) show bilateral SVI (arrows). (c) Whole-mount pathologic step section shows prostate cancer with bilateral seminal vesicle involvement. The green circle represents the area with a Gleason grade of 3, and the black circle represents the area with a Gleason grade of 4 or a mixture of Gleason grades 4 and 5. LSV = left seminal vesicle, RSV = right seminal vesicle.

 

Figure 1
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  		Figure 1b: pT4 prostate cancer (clinical stage T2b with PSA level of 12.42 ng/mL) and bilateral seminal vesicle involvement in a 63-year-old man. Sextant biopsy results showed Gleason grade 4 + 3 tumors involving 50% of the total submitted tissue on both sides (94% of total submitted cores were positive) and PNI in left peripheral and transition zones. According to the Kattan staging nomogram, the likelihood of SVI was 18%. (a) Transverse T2-weighted fast spin-echo 3-mm-thick MR image (4900/118 [repetition time msec/effective echo time msec]) and (b) coronal T2-weighted fast spin-echo 3-mm-thick MR image (4666/96) show bilateral SVI (arrows). (c) Whole-mount pathologic step section shows prostate cancer with bilateral seminal vesicle involvement. The green circle represents the area with a Gleason grade of 3, and the black circle represents the area with a Gleason grade of 4 or a mixture of Gleason grades 4 and 5. LSV = left seminal vesicle, RSV = right seminal vesicle.

 

Figure 1
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  		Figure 1c: pT4 prostate cancer (clinical stage T2b with PSA level of 12.42 ng/mL) and bilateral seminal vesicle involvement in a 63-year-old man. Sextant biopsy results showed Gleason grade 4 + 3 tumors involving 50% of the total submitted tissue on both sides (94% of total submitted cores were positive) and PNI in left peripheral and transition zones. According to the Kattan staging nomogram, the likelihood of SVI was 18%. (a) Transverse T2-weighted fast spin-echo 3-mm-thick MR image (4900/118 [repetition time msec/effective echo time msec]) and (b) coronal T2-weighted fast spin-echo 3-mm-thick MR image (4666/96) show bilateral SVI (arrows). (c) Whole-mount pathologic step section shows prostate cancer with bilateral seminal vesicle involvement. The green circle represents the area with a Gleason grade of 3, and the black circle represents the area with a Gleason grade of 4 or a mixture of Gleason grades 4 and 5. LSV = left seminal vesicle, RSV = right seminal vesicle.

 
Statistical Analysis
Univariate and multivariate logistic regression and receiver operating characteristic (ROC) curve analyses were performed for all clinical and imaging variables to predict SVI (H.N.C., M.W.K.). Univariate logistic regression was used to compare the characteristics of patients with SVI with the characteristics of patients without SVI. The area under the ROC curve (AUC) was evaluated for models of SVI prediction on the basis of the Kattan nomogram alone and MR imaging alone. In addition, a model was constructed for the prediction of SVI on the basis of the Kattan nomogram and MR imaging combined. AUC was bias-corrected by using the leave-one-out cross validation method (29). A P value of less than .05 was considered to indicate a statistically significant difference. The software programs that were used for data analysis included SAS (version 8.2; SAS Institute, Cary, NC) and S-PLUS (version 2000; Insightful, Seattle, Wash).


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 ADVANCES IN KNOWLEDGE
 References
 
At surgical histopathologic analysis, 28 (4.9%) of 573 patients had evidence of SVI. Unilateral SVI was present in 22 (3.8%) of 573 patients, and bilateral SVI was present in six (1.0%) of 573 patients (Table 2).


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  		Table 2. Prevalence of SVI in Final Pathologic Specimens

 
MR imaging was associated with SVI at both univariate and multivariate analysis (P < .001 in both cases) (Table 3).


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  		Table 3. Strength of Clinical Variables and MR Findings for the Prediction of SVI

 
At univariate analysis, MR findings (P < .001), PSA level (P = .014), Gleason grade (P = .01), clinical stage (P < .001), the greatest percentage of cancer in all biopsy cores (P < .001), and PNI (P = .005) were significantly associated with SVI; the percentage of positive cores was the only clinical variable that was not significantly associated with SVI (P = .30). AUC was larger for MR imaging (0.76) than for any of the clinical variables (0.62–0.73) (Table 3).

At multivariate analysis, MR findings (P < .001), PSA level (P = .012), Gleason grade (P < .001), and the greatest percentage of cancer in all biopsy cores (P = .02) were significantly associated with SVI. The AUC for the Kattan nomogram plus MR imaging (0.87) was significantly larger than the AUC for the Kattan nomogram alone (0.80) or for MR imaging alone (0.76) (P < .05 in both cases) (Table 4, Figs 1, 2).


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  		Table 4. AUC Values for Models Predicting SVI on the Basis of MR Imaging and the Kattan Nomogram

 

Figure 2
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  		Figure 2: Graph shows ROC curves for jackknife predicted probabilities of SVI on the basis of endorectal MR imaging and the Kattan nomogram plus MR imaging. The model containing the Kattan nomogram plus MR imaging (0.87) has a significantly greater AUC than the model containing only the Kattan nomogram (0.80; P = .04) or the model containing only MR imaging (0.76; P < .01).

 

   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
ADVANCES IN KNOWLEDGE
 References
 
In patients with prostate cancer, the presence of SVI is associated with an increased risk of lymph node metastasis and recurrence (4,17,23,30). The prediction of SVI before treatment may influence treatment selection in favor of radiation therapy instead of surgery. Furthermore, while resection of the seminal vesicles has been a standard component of radical prostatectomy, it has recently been suggested that if SVI can be confidently ruled out, the surgeon may prefer to spare the seminal vesicles during radical prostatectomy to prevent long-term loss of urinary continence (31).

In our patient population, 4.9% of patients had evidence of SVI at surgical histopathologic analysis. This result is consistent with the dramatic downstaging of prostate cancer at the time of diagnosis that has occurred over the past 2 decades, as demonstrated by the National Cancer Institute's Surveillance, Epidemiology, and End Results Program. Data from this program show that from 1995 to 2001, 91% of prostate cancer cases were of a local or regional stage at diagnosis compared with only 74% from 1981 to 1987 (1,32).

Because of the importance of SVI in patient prognosis and treatment choice, presurgical biopsy of the seminal vesicles has been suggested. Terris et al (33) performed biopsies of the seminal vesicles in 73 selected patients, 12 of whom had SVI in the radical prostatectomy specimens. They reported a negative predictive value of 97%, a positive predictive value of 80%, and a sensitivity of 67%. The low incidence of SVI overall, occasional false-positive results, and low sensitivity limit the enthusiasm for performing biopsy in the seminal vesicles (3,12,33).

In the literature, serum PSA level and Gleason grade are significantly associated with SVI for both univariate and multivariate analysis (3,34–36). In our study, MR imaging results, the greatest percentage of cancer in all biopsy cores, PSA level, clinical stage, Gleason grade, and PNI were all significantly associated with SVI at univariate analysis, while MR imaging results, Gleason grade, PSA level, and the greatest percentage of cancer in all biopsy cores were significantly associated with SVI at multivariate analysis. Koh et al (3) found that all prognostic factors, when combined in a model, predicted the pathologic stage more accurately than did any single parameter alone—a finding that is consistent with the findings of our study. Our results show that MR imaging can add significant incremental value to clinical variables for the prediction of SVI.

The role of modern MR imaging in prostate cancer management has been changing not only because of the development of new MR techniques, such as endorectal MR imaging, contrast material–enhanced endorectal MR imaging, and MR spectroscopic imaging, but also because of radiologists' increased experience with MR imaging of the prostate. The results of previous studies have shown that MR imaging findings, although subject to substantial interobserver variability, can add significant incremental value to clinical variables in predicting other features of prostate cancer that are relevant to staging, such as extracapsular extension and lymph node metastasis (26,27,37).

Our study was not designed to assess MR technology but to assess the value of MR imaging, as applied in the clinical setting during radiologists' regular clinical assignments. Accordingly, the readers had access to clinical data, such as PSA level and biopsy results when available, in the patient's medical record. Each study was evaluated only once, so we could not assess interobserver and intraobserver variability. Furthermore, we studied a consecutive cohort of patients who met eligibility requirements on the basis of pretreatment factors (not SVI outcome) and not a random sample. Thus, the estimates of accuracy might be biased.

In conclusion, our results show that endorectal MR imaging findings can contribute significant incremental value to the Kattan nomogram for predicting SVI. Although further multicenter confirmatory studies would be helpful, we suggest that MR imaging has an important role to play in the pretreatment evaluation of prostate cancer, including the prediction of SVI.


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


   ACKNOWLEDGMENTS
 
The authors thank Ada Muellner, BA, for editing the manuscript, Chinyere Onyebuchi, MPH, for preparing the figures, and Fernando P. Secin, MD, PhD, for helpful comments.


   FOOTNOTES
 

Abbreviations: AUC = area under the ROC curve • PNI = perineural invasion • PSA = prostate-specific antigen • ROC = receiver operating characteristic • SVI = seminal vesicle invasion

Author contributions: Guarantor of integrity of entire study, L.W.; study concepts/study design or data acquisition or data analysis/interpretation, all authors; manuscript drafting or manuscript revision for important intellectual content, all authors; manuscript final version approval, all authors; literature research, L.W.; clinical studies, H.H.; statistical analysis, M.W.K., H.N.C.; and manuscript editing, H.H.

Authors stated no financial relationship to disclose.


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

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