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Published online before print December 12, 2005, 10.1148/radiol.2382041905

(Radiology 2005;238:597.)

A more recent version of this article appeared on December 1, 2005
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© RSNA, 2005

Genitourinary Imaging

Prediction of Organ-confined Prostate Cancer: Incremental Value of MR Imaging and MR Spectroscopic Imaging to Staging Nomograms1

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

1 From the Departments of Radiology (L.W., H.H., H.N.C.) and Urology (M.W.K., P.T.S., K.K.), Memorial Sloan-Kettering Cancer Center, 1275 York Ave, New York, NY 10021. From the 2004 RSNA Annual Meeting. Received November 10, 2004; revision requested December 16; revision received May 9, 2005; accepted May 19; final version accepted June 17. 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
 References
 
Purpose: To assess retrospectively the incremental value of endorectal coil magnetic resonance (MR) imaging and combined endorectal MR imaging–MR spectroscopic imaging to the staging nomograms for predicting organ-confined prostate cancer (OCPC).

Materials and Methods: The institutional review board approved this HIPAA-compliant study and issued a waiver of informed consent for review of the MR reports and clinical data. Between November 1, 1999, and November 1, 2004, 229 patients underwent endorectal MR imaging and 383 underwent combined endorectal MR imaging–MR spectroscopic imaging before radical prostatectomy. Mean patient age was 58 years (range, 32–74 years). MR studies were interpreted prospectively by 12 radiologists who were informed of patients' clinical data. On the basis of the MR reports, the risks of extracapsular extension, seminal vesicle invasion, and lymph node metastasis were scored retrospectively from 1 to 5; the highest score was subtracted from 6 to determine a score (from 1 to 5) for the likelihood of OCPC on MR studies. The staging nomograms were used to calculate the likelihood of OCPC on the basis of serum prostate-specific antigen level, Gleason grade at biopsy, and clinical stage. Histopathologic findings constituted the reference standard. Logistic regression was used to estimate the multivariable relations between OCPC and MR findings. The area under the receiver operator characteristic curve was calculated for each model. The jackknife method was used for bias correction.

Results: MR findings contributed significant incremental value (P ≤ .02) to the nomograms in the overall study population. The contribution of MR findings was significant in all risk groups but was greatest in the intermediate- and high-risk groups (P < .01 for both). Accuracy in the prediction of OCPC with MR was higher when MR spectroscopic imaging was used, but the difference was not significant.

Conclusion: Endorectal MR imaging and combined endorectal MR imaging–MR spectroscopic imaging contribute significant incremental value to the staging nomograms in predicting OCPC.

© RSNA, 2005


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
Materials and Methods
 Results
 Discussion
 References
 
Today, with the widespread use of screening of prostate-specific antigen (PSA) levels and with better methods for diagnosis at biopsy, 90% of newly diagnosed cases of prostate cancer are considered to be of a local or regional stage (1). When clinically localized cancers are confined to the prostate pathologically, more than 85% are curable with radical prostatectomy (2,3).

Effective treatment planning, whether for radiation treatment or surgery, requires accurate prediction of the pathologic stage of the cancer. Various methods have been proposed for predicting that a clinically localized prostate cancer is, in fact, pathologically confined to the prostate (4–8). An important advance in accurate prediction was the development of nomograms that combined clinical stage (determined by means of digital rectal examination), serum PSA levels, and the Gleason grade in the biopsy specimen to predict the pathologic stage of the cancer (9,10). These "Partin Tables" are a validated predictive tool widely used for patient counseling (11–13). However, as a treatment-planning tool they are limited because they do not incorporate anatomic data that could guide interventions to control local disease. If cancer extends outside the prostate, the chances of cure are substantially diminished, and the surgical or radiation treatment planning must be adapted to ensure complete eradication of the cancer. The role of endorectal magnetic resonance (MR) imaging in prostate cancer management has been emerging with improved MR techniques, such as MR spectroscopic imaging, and with better interpretation of MR images of the prostate by experienced radiologists (14–19). The present study was designed to assess retrospectively the incremental value of endorectal coil MR imaging and combined endorectal MR imaging–MR spectroscopic imaging to the staging nomograms for predicting organ-confined prostate cancer (OCPC).


   Materials and Methods
TOP
 ABSTRACT
 INTRODUCTION
 Materials and Methods
Results
 Discussion
 References
 
Patients
Between November 1, 1999, and November 1, 2004, 612 consecutive patients with prostate cancer were referred from the urology department (P.T.S.) for MR imaging before radical retropubic prostatectomy and pelvic lymphadenectomy. Three hundred eighty-three patients underwent endorectal MR imaging combined with MR spectroscopic imaging, and 229 underwent endorectal MR imaging alone. From November 1999 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 National Institutes of Health study, which was compliant with the Health Insurance Portability and Accountability Act, or HIPAA. Subsequent to June 2003, imaging was performed as part of our accepted practice for patient evaluation. Our institutional review board issued a waiver of informed consent for the review of the MR reports and clinical data for this retrospective study, which was also HIPAA compliant. Mean patient age was 58 years (range, 32–74 years). None of the patients received neoadjuvant hormonal or radiation therapy prior to surgery. A tissue diagnosis of prostate cancer was made at biopsy in all patients. Clinical stage (determined by means of digital rectal examination), serum PSA level, and Gleason grade in the biopsy specimen, as well as MR data, were recorded retrospectively from the patients' medical records by two coauthors (L.W. and K.K.). A segment of the study population (371 of 612 patients) has been included in previous publications (14,16,17).

Staging Nomograms and Risk Groups
The likelihood of OCPC according to the 2001 version of the Partin Tables was recorded on the basis of the serum PSA level, Gleason grade, and clinical staging (L.W. and K.K.) (10). Furthermore, the same coauthors divided the patients into three categories: low, intermediate, or high risk for cancer spread outside the prostate. The low-risk group had clinical stage T1 or T2 prostate cancer, with a Gleason score of 6 or less and a PSA level lower than 10 ng/mL. The intermediate-risk group had clinical stage T1 or T2 prostate cancer, with a Gleason score of 7 and/or a PSA level of 10.1–20 ng/mL. The high-risk group had clinical stage T3 or T4 prostate cancer or a Gleason score greater than 7 or a PSA level greater than 20 ng/mL (20–22).

Imaging and Interpretation
Endorectal MR imaging and hydrogen 1 MR spectroscopic imaging had been performed by using 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 msec/echo time msec, 700/8; section thickness, 5 mm; intersection gap, 1 mm; field of view, 24 cm; matrix, 256 x 192; frequency direction, transverse (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 msec/effective echo time msec, 5000/96; echo train length, 16; section thickness, 3 mm; intersection gap, 0 mm; field of view, 14 cm; matrix, 256 x 192; frequency direction, anteroposterior (to prevent obstruction of the prostate by endorectal coil motion artifact); and three signals acquired. MR spectroscopic imaging was performed by using point-resolved spectroscopy voxel excitation, with band-selective inversion with gradient dephasing water and lipid suppression (23) and spatial encoding by means of chemical shift imaging (24) at 6.25-mm resolution in all three dimensions. Timing parameters were 1000/130, and imaging time was 17 minutes.

Data processing was performed at a workstation (Sun Ultra 10; Sun Microsystems, Mountain View, Calif) and included 2-Hz Lorentzian spectral apodization, four-dimensional Fourier transform, and automated frequency, phase, and baseline correction. Spectral data were zero filled to 3.1-mm resolution in the superior-inferior dimension and overlaid on corresponding transverse T2-weighted MR images. Peak areas were calculated by using numeric integration. To provide a noise measurement, we calculated the standard deviation of the MR signal intensity in a region of the spectrum containing only noise. Metabolite peak areas were then normalized with respect to the noise standard deviation to yield an approximate signal-to-noise ratio.

MR studies had been interpreted prospectively by 12 MR radiologists during their regular clinical assignment to the MR imaging service. All of the readers were trained in body MR imaging (nine had an MR imaging fellowship and the others had been involved with MR imaging since it was introduced to clinical practice). The level of experience reading MR images since fellowship ranged from 4 to 17 years among the readers. Each radiologist made his or her determination of MR prostate findings on the basis of his or her own continuous medical training and knowledge of previously described MR imaging features of extracapsular extension (ECE), seminal vesicle invasion (SVI), and lymph node metastasis (LNM) (16,25–31). All readers had access to the patients' medical records, including PSA level and biopsy findings as per their regular clinical practice. In addition, all readers had access to MR spectroscopic imaging data when available. The use of MR spectroscopic imaging data consisted of the evaluation of the location and number of abnormal voxels (voxels classified as suspicious or definitive for cancer by a spectroscopist). As described by Yu et al (25), when there are more than 4 voxels of cancer per section present at spectroscopy, the probability of ECE increases. Spectroscopy does not play a role in the assessment of the probability of SVI or LNM.

On the basis of the radiologists' written reports, the likelihood of ECE, SVI, and LNM was scored retrospectively by a single observer (L.W., 4 years of experience with research on MR imaging of the prostate). Three separate scores were assigned (one for ECE, one for SVI, and one for LNM) by using the following rating scale: score of 5, definite yes; score of 4, probable yes; score of 3, possible yes; score of 2, probable no; and score of 1, definite no. The greatest of the three scores was then used to calculate the likelihood of OCPC at MR evaluation with the following formula: OCPC = 6 – maximal score (ie, the ECE, SVI, or LNM score). The rating scale for the likelihood of OCPC at MR evaluation was as follows: score of 1, definitely no OCPC; score of 2, probably no OCPC; score of 3, possible OCPC; score of 4, probable OCPC; and score of 5, definite OCPC. Thus, if the scores for ECE, SVI, and LNM were 1 (definitely no ECE), 1 (definitely no SVI), and 1 (definitely no LNM), respectively, the score for the likelihood of OCPC was 5 (definite OCPC). The formula is an attempt to assess one minus the probability of the patient's highest risk factor, though on a five-point ordinal scale. It was designed and validated by a statistician (M.W.K.) with extensive experience in prostate cancer outcome research.

Histologic Evaluation
Core biopsies had been evaluated for Gleason grade, greatest percentage of cancer in all biopsy cores, percentage of positive cores in all biopsy cores, and perineural invasion. Histology reports were reviewed by one author (L.W.). Radical prostatectomy specimens were examined by the institutional pathology department, as previously described by Yossepowitch et al (32). Specimens were fixed in formalin, with the external surface of the right and left sides dyed in two colors. The apical prostate was truncated perpendicular to the prostatic urethra and subsequently sectioned as slices parallel to the prostatic urethra. The bladder neck margin was obtained by sampling portions of soft tissue at the junction of the rough prostatic capsule and smooth bladder neck or most proximal portion of the submitted specimen corresponding to the anatomic bladder neck. The remaining prostate was completely transected at 3–5-mm intervals in a plane perpendicular to the urethra. The final pathology report following surgery was used to determine the presence of OCPC. OCPC was defined as the absence of cancer cells beyond the prostate capsule. Patients with LNM were considered not to have OCPC regardless of whether there was penetration through the prostate capsule.

Statistical Analysis
Logistic regression was used to estimate the relations between clinical variables and MR findings and the prediction of OCPC. Model discrimination was assessed by using the receiver operator characteristic (ROC) curves, which were plotted, calculated, and compared. When the staging nomograms were combined with MR results in the model, the jackknife method, a form of resampling that reduces the optimistic bias, was used to obtain the bias-corrected predicted probabilities and construct the ROC curves (33). The areas under the ROC curves were evaluated for models of OCPC prediction on the basis of the staging nomograms alone, MR findings alone (from endorectal MR imaging or combined endorectal MR imaging–MR spectroscopic imaging), and the staging nomograms plus MR findings (H.N.C., M.W.K.). To assess the incremental value of MR findings to the staging nomograms, the model for the prediction of OCPC based on the staging nomograms plus MR findings was compared with the model of prediction based on the staging nomograms alone. P < .05 was considered to indicate a statistically significant difference. Software programs used for data analysis were 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
 References
 
At surgical histopathologic evaluation, 445 (73%) of 612 patients had evidence of OCPC (Fig 1). Table 1 summarizes the distribution of the preoperative clinical variables, Table 2 shows the predicted probabilities of OCPC (derived from the 2001 Partin Tables) according to risk group, and Table 3 demonstrates the distribution of final pathologic staging.



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  		Figure 1a: Images in a 55-year-old man with a small palpable clinical stage T2 prostate nodule and PSA level of 0.80 ng/mL. Sextant biopsy results showed Gleason grade 3 + 3 cancer involving 10% of submitted tissue from the right side (50% of the cores) and no perineural invasion. By using staging nomograms, the likelihood of OCPC was determined to be 81%. (a–c) T2-weighted fast spin-echo MR images. (a) Transverse 3-mm-thick MR (4900/118) image shows OCPC (arrow) in the right apex. (b) Sagittal 4-mm-thick MR (6000/97) image shows a focus of cancer (arrow) in the right apex and midgland. (c) Coronal 3-mm-thick MR (4666/96) image shows cancer (arrow) in the right apex and midgland. (d) Whole-mount serial section of the removed prostate shows organ-confined cancer (arrow) involving the right posterior quadrant of the prostate.

 


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  		Figure 1b: Images in a 55-year-old man with a small palpable clinical stage T2 prostate nodule and PSA level of 0.80 ng/mL. Sextant biopsy results showed Gleason grade 3 + 3 cancer involving 10% of submitted tissue from the right side (50% of the cores) and no perineural invasion. By using staging nomograms, the likelihood of OCPC was determined to be 81%. (a–c) T2-weighted fast spin-echo MR images. (a) Transverse 3-mm-thick MR (4900/118) image shows OCPC (arrow) in the right apex. (b) Sagittal 4-mm-thick MR (6000/97) image shows a focus of cancer (arrow) in the right apex and midgland. (c) Coronal 3-mm-thick MR (4666/96) image shows cancer (arrow) in the right apex and midgland. (d) Whole-mount serial section of the removed prostate shows organ-confined cancer (arrow) involving the right posterior quadrant of the prostate.

 


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  		Figure 1c: Images in a 55-year-old man with a small palpable clinical stage T2 prostate nodule and PSA level of 0.80 ng/mL. Sextant biopsy results showed Gleason grade 3 + 3 cancer involving 10% of submitted tissue from the right side (50% of the cores) and no perineural invasion. By using staging nomograms, the likelihood of OCPC was determined to be 81%. (a–c) T2-weighted fast spin-echo MR images. (a) Transverse 3-mm-thick MR (4900/118) image shows OCPC (arrow) in the right apex. (b) Sagittal 4-mm-thick MR (6000/97) image shows a focus of cancer (arrow) in the right apex and midgland. (c) Coronal 3-mm-thick MR (4666/96) image shows cancer (arrow) in the right apex and midgland. (d) Whole-mount serial section of the removed prostate shows organ-confined cancer (arrow) involving the right posterior quadrant of the prostate.

 


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  		Figure 1d: Images in a 55-year-old man with a small palpable clinical stage T2 prostate nodule and PSA level of 0.80 ng/mL. Sextant biopsy results showed Gleason grade 3 + 3 cancer involving 10% of submitted tissue from the right side (50% of the cores) and no perineural invasion. By using staging nomograms, the likelihood of OCPC was determined to be 81%. (a–c) T2-weighted fast spin-echo MR images. (a) Transverse 3-mm-thick MR (4900/118) image shows OCPC (arrow) in the right apex. (b) Sagittal 4-mm-thick MR (6000/97) image shows a focus of cancer (arrow) in the right apex and midgland. (c) Coronal 3-mm-thick MR (4666/96) image shows cancer (arrow) in the right apex and midgland. (d) Whole-mount serial section of the removed prostate shows organ-confined cancer (arrow) involving the right posterior quadrant of the prostate.

 

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  		Table 1. Distribution of Preoperative Clinical Variables

 

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  		Table 2. Predicted Probability of OCPC according to the 2001 Partin Tables

 

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  		Table 3. Final Pathologic Stage

 
Overall, in the prediction of OCPC, the area under the ROC curve for the staging nomograms was 0.80, while the area under the ROC curve for the staging nomograms plus MR findings was 0.88; the difference was significant (P < .01) (Table 4) (Fig 2).


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  		Table 4. Areas under ROC Curves of OCPC Prediction Models

 


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  		Figure 2: Graph shows ROC curves for jackknife-predicted probabilities of OCPC for two models for the study population: one based only on clinical staging nomograms (Partin OCPC) and one based on staging nomograms plus MR findings (Partin OCPC + MR OCPC). The model with MR findings has a significantly greater area under the ROC curve (AUC) than does the model lacking MR findings (0.876 vs 0.80, P < .01).

 
Risk Groups
The incremental value of MR findings to the staging nomograms was significant in all three risk groups, although it was greater in the intermediate- and high-risk groups (P < .01 for both) than in the low-risk group (P = .02) (Table 4).

MR Spectroscopic Imaging and Endorectal MR Imaging
In the combined endorectal MR imaging–MR spectroscopic imaging group, the areas under the ROC curves were 0.81 for the staging nomograms and 0.90 for the staging nomograms plus MR findings; the difference was significant (P < .01) (Table 4).

Prediction of OCPC with MR findings plus the staging nomograms was better in the endorectal MR imaging–MR spectroscopic imaging group (area under the ROC curve, 0.84; 95% confidence interval: 0.79, 0.89) than in the endorectal MR imaging–only group (area under the ROC curve, 0.77; 95% confidence interval: 0.70, 0.84), but the difference was not significant (P > .05) (Table 4). The incremental value of MR spectroscopic imaging to endorectal MR imaging was slightly greater in the low- and intermediate-risk groups than in the high-risk group (Table 5), but the difference was not significant in any of the risk groups.


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  		Table 5. Accuracy of MR Imaging Prediction of Prostate Cancer with and without MR Spectroscopic Imaging

 

   Discussion
TOP
 ABSTRACT
 INTRODUCTION
 Materials and Methods
 Results
 Discussion
References
 
Pretreatment knowledge of OCPC is important for treatment selection and planning, regardless of whether the treatment method ultimately chosen is watchful waiting, surgery, or radiation therapy. Radical prostatectomy in patients with pathologically organ-confined cancer results in a survival rate comparable with that of age-matched controls without prostate cancer (34–39). Since the introduction of the Partin Tables in 1997, investigators have repeatedly validated the nomograms' capacity to help predict the pathologic stage of clinically localized prostate cancer (11–13). In 2001, the nomograms were updated based on a more contemporary cohort of disease features (10). The accuracy of the staging nomograms in predicting OCPC is high, with reports of the area under the ROC curve ranging from 0.79 to 0.82 (12,13). Our study results demonstrated similar accuracy for the staging nomograms in predicting OCPC, with an overall area under the ROC curve of 0.80. Despite the strong predictive ability and the cost-effectiveness of the staging nomograms, there is room for improved accuracy of prediction, particularly since clinical staging in the staging nomograms is based only on digital rectal examination. Moreover, the staging nomograms cannot assist in the localization of ECE, which is critical for optimal treatment planning (5,9).

Debate persists regarding whether MR imaging should be used routinely for presurgical evaluation of prostate cancer. Because of the high incidence of prostate cancer and the high cost of MR examinations, it has been stated that routine use of endorectal MR imaging alone or in combination with MR spectroscopic imaging might merely add a financial burden to the health care system unless it prevents unnecessary surgery or improves treatment planning and outcomes (40). It has been shown that endorectal MR imaging adds value in all risk groups (5,41); in the prediction of ECE, the greatest incremental value of endorectal MR imaging to the Partin Tables has been found in high-risk patients (14,16). In our study, the addition of MR findings to the Partin Tables (2001 version) significantly improved the prediction of OCPC for the overall patient population (P < .01). The addition of MR findings also increased the area under the ROC curve significantly in the low-risk group (P = .02) and in the intermediate- and high-risk groups (P < .01 for both).

The contribution of MR spectroscopic imaging findings to endorectal MR imaging in the prediction of OCPC was also assessed in our study. The magnitude and extent of metabolic abnormality on MR spectroscopic images is indicative of tumor aggressiveness, volume, and stage (42,43). Yu et al (25) demonstrated that the combined use of endorectal MR imaging and MR spectroscopic imaging decreased interobserver variability and, for less experienced radiologists, significantly improved the detection of ECE. In our study, the accuracy of radiologists' predictions of OCPC was higher in the combined MR group than in the endorectal MR imaging–only group, but the difference was not significant; MR findings contributed significant incremental value to the staging nomograms in the prediction of OCPC in both of these groups.

Our study was limited by the fact that it was designed to assess the value of MR readings as used in clinical practice; the readers were not blinded to clinical data such as PSA level and biopsy results. Furthermore, only one reader evaluated each case once, so we could not assess interobserver and intraobserver variability. With respect to the assessment of the incremental value of MR spectroscopic imaging, separate readings with and without MR spectroscopic imaging were not performed and therefore the true incremental value of MR spectroscopic imaging needs further analysis.

In conclusion, although further multicenter confirmatory studies would be helpful, our results show that MR findings (from endorectal MR imaging or combined endorectal MR imaging–MR spectroscopic imaging) contribute significant incremental value to clinical staging nomograms in the prediction of OCPC. The incorporation of endorectal MR imaging into future staging nomograms for the prediction of OCPC may therefore be warranted.


   ACKNOWLEDGMENTS
 
The authors thank Ada Muellner, BA, and Chinyere Onyebuchi, MPH, for editorial assistance, Lachlan Smith, BS, and Halley Eisenberg, BS, for helping to prepare the figures, and Anne K. Robbins, MLS, for reference assistance.


   FOOTNOTES
 

Abbreviations: ECE = extracapsular extension • LNM = lymph node metastasis • OCPC = organ-confined prostate cancer • 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, L.W., 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, L.W.; clinical studies, L.W., H.H.; statistical analysis, M.W.K., H.N.C.; and manuscript editing, H.H.


   References
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 ABSTRACT
 INTRODUCTION
 Materials and Methods
 Results
 Discussion
 References
 

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