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Combined Endorectal and Phased-Array MRI in the Prediction of Pelvic Lymph Node Metastasis in Prostate Cancer

¹ Department of Radiology, Memorial Sloan-Kettering Cancer Center, 1275 York Ave., Rm. C-278, New York, NY 10021.
² Department of Urology, Sidney Kimmel Center for Prostate and Urologic Cancers, Memorial Sloan-Kettering Cancer Center, New York, NY 10021.
³ Present address: Department of Quantitative Health Sciences, Cleveland Clinic Foundation, Cleveland, OH 44195.
⁴ Present address: Department of Radiology, University of New Mexico Health Sciences Center, Albuquerque, NM 87131.

Received October 28, 2004; accepted after revision February 3, 2005.

 
Supported by the National Institutes of Health (grant IRGICA76423-0IRI).

Presented at the 2004 American Roentgen Ray Society annual meeting, Miami Beach, FL.

Address correspondence to H. Hricak.

Abstract

Top Abstract Introduction Subjects and Methods Results Discussion References

 
OBJECTIVE. The objectives of our study were to evaluate the accuracy of combined endorectal and phased-array MRI in detecting pelvic lymph node metastasis (LNM) in patients with prostate cancer and to determine whether radiologists' predictions of LNM improve with the incorporation of Partin nomogram or MRI findings (or both) regarding extracapsular extension or seminal vesicle invasion.

SUBJECTS AND METHODS. Between May 1999 and September 2003, 411 consecutive patients with clinically localized prostate cancer underwent MRI before surgery. Serum prostate-specific antigen (PSA) level, Gleason grade, clinical stage, greatest percentage of cancer and percentage of positive cores in all biopsy cores, presence of perineural invasion on biopsy, and likelihood of LNM based on the Partin tables (2001 version) were recorded. MRI studies were interpreted prospectively, but the risks of LNM, extracapsular extension, and seminal vesicle invasion were scored retrospectively on the basis of the MRI reports. Surgical pathology constituted the standard of reference. The accuracy of LNM prediction was assessed using areas under receiver operating characteristic curves (AUCs) and univariate and multivariate logistic regression analyses. For multivariate models, the jackknife method was used for bias correction. A p value below 0.05 denoted statistical significance.

RESULTS. At surgical pathology, LNM was present in 22 (5%) of 411 patients. MRI was an independent statistically significant predictor of LNM (p = 0.002), with positive and negative predictive values of 50% and 96.36%, respectively. On multivariate analysis, prediction of lymph node status using the model that included all MRI variables (extracapsular extension, seminal vesicle invasion, and LNM) along with the Partin nomogram results had a significantly greater AUC than the univariate model that included only MRI LNM findings (AUC = 0.892 vs 0.633, respectively; p < 0.01).

CONCLUSION. Incorporation of the Partin nomogram results and MRI findings regarding both extracapsular extension and seminal vesicle invasion improves the MR prediction of LNM in patients with prostate cancer.

Keywords: biopsy • genitourinary tract imaging • MRI • oncologic imaging • prostate • prostate cancer

Introduction

Top Abstract Introduction Subjects and Methods Results Discussion References

 
Prostate cancer is the most common cancer and the second leading cause of cancer death in American men. The American Cancer Society estimated that in 2005 in the United States, 232,090 new cases of prostate cancer would be diagnosed and 39,350 men would die of the disease [1]. In a patient with newly diagnosed prostate cancer, the presence of lymphatic metastases is an important prognostic factor, indicating great risk for progression to established distant metastases and death [2-5]. The risk of metastatic disease at 10 years is 31% ± 7% (mean ± SD) for patients with negative nodes compared with 83% ± 7% for patients with positive nodes at the time of initial treatment. The risk of dying of prostate cancer is 17% ± 6% at 10 years for patients with negative nodes compared with 57% ± 11% for patients with positive nodes [4]. Accurate diagnosis of lymph node metastasis (LNM) is essential in treatment selection and planning.

Since the late 1980s, studies have consistently shown that MRI has limited value in the assessment of LNM in patients with prostate cancer [6-14] (Table 1). Although MRI provides images with excellent anatomic detail for the evaluation of locoregional disease and has high specificity for LNM, the sensitivity of MRI for the detection of LNM is relatively low [15-17]. Furthermore, the National Cancer Institute's Surveillance, Epidemiology, and End Results Program has shown that there has been a dramatic downstaging of prostate cancer at the time of diagnosis [1, 18]. This change has made the MRI evaluation of lymph nodes even more difficult. Not only has the incidence of LNM declined steeply (in a study by Soh et al. [19], it decreased from 23% in 1984 to 2% in 1995), but cancerous nodes, when present, are likely to be smaller [1, 2, 18, 19]. A recent study by Harisinghani et al. [14] showed that high-resolution MRI with lymphotropic superparamagnetic nanoparticles allows the detection of small and otherwise undetectable LNMs in patients with prostate cancer. Although these results are excellent and promising, the low incidence of LNM raises the question of whether lymphotropic superparamagnetic nanoparticles should be used routinely. Although the U.S. Food and Drug Administration (FDA) is expected to approve the clinical use of lymphotropic superparamagnetic nanoparticles, the question of patient selection remains unanswered.

In part, the limitations of imaging in the evaluation of LNM in patients with prostate cancer have been offset by the development of Partin staging nomograms or tables (available online as supplemental data), which predict the final pathologic stage, including the presence of LNM, on the basis of clinical stage, serum prostate-specific antigen (PSA) level, and Gleason grade [20, 21]. The Partin staging nomograms are a validated predictive instrument widely used for patient counseling [22-25]. However, as a treatment planning tool, they are limited by the fact that they do not incorporate anatomic data that could assist in interventions aimed to control the disease.

We undertook this study to investigate the role of combined endorectal and phased-array MRI in nodal metastasis detection in a representative sample of the current prostate cancer patient population, with its low incidence of LNM. Our goal was to assess the accuracy of MRI in predicting prostate cancer LNM. In addition, we aimed to determine whether the prediction of LNM improved with the inclusion of MRI findings regarding extracapsular extension or seminal vesicle invasion (or both) or with the use of the Partin nomograms.

Subjects and Methods

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Patients
Between November 1999 and September 2003, 411 consecutive patients with clinically localized prostate cancer underwent MRI before radical retropubic prostatectomy and pelvic lymphadenectomy (Table 2). For all patients, the surgery was performed at our institution. The mean patient age was 57.6 years (range, 32-74 years). None of the patients received neoadjuvant hormonal or radiation therapy before surgery. All patients had tissue diagnosis of prostate cancer on biopsy specimens. The approval of the institutional review board was obtained, and all patients gave informed consent. Patient accrual was done as part of an ongoing National Cancer Institute trial, and some of the cases have been previously reported in studies on the locoregional evaluation of prostate cancer by MRI [26-28].

The following clinical variables were recorded for each patient: clinical stage, pretreatment serum PSA, biopsy Gleason sum, greatest percentage of cancer in all biopsy cores, percentage of positive cores in all biopsy cores, and presence of perineural invasion. Clinical stage was assigned using the 1992 American Joint Committee on Cancer (AJCC) and the Union Internationale Contre le Cancer (UICC) TNM guidelines based on digital rectal examination regardless of the results of sonography or other imaging techniques. Serum PSA was measured using a Hybritech assay (Hybritech Tandem-R, Beckman Coulter). Central pathologic review was not performed, but all specimens were analyzed by dedicated genitourinary pathologists at our institution.

Combined Endorectal and Phased-Array MRI Data Acquisition and Interpretation
MRI was performed at 1.5 T with state-of-the-art imaging systems (Signa Horizon, GE Healthcare) and pelvic phased-array and endorectal coils. Images of the pelvis, extending from the pubic symphysis to the level of the aortic bifurcation, were obtained. The MR pulse sequences consisted of axial spin-echo T1-weighted images with the following parameters: TR/TE, 700/8; slice thickness, 5 mm; interslice gap, 1 mm; field of view, 24 cm; matrix, 256 x 192; and 1 excitation. Thin-section high-spatial-resolution axial, coronal, and sagittal T2-weighted fast spin-echo images of the prostate and seminal vesicles were obtained with the following parameters: TR/TE, 5,000/96; echo-train length, 16; slice thickness, 3 mm; interslice gap, 0 mm; field of view, 14-20 cm; matrix, 256 x 192; and 3 excitations. Axial T2-weighted images were postprocessed to correct for the reception profile of the endorectal coil.

MRI studies were prospectively interpreted by 11 MR body radiologists during their regular clinical assignment to the MR service. Each radiologist made his or her determination regarding the presence of LNM based on his or her practice pattern and knowledge of previously described MRI features of LNM. As a basic clinical guideline, the radiologists classified lymph nodes on MRI as malignant if the short-axis diameter was elongated and exceeded 10 mm or was rounded and exceeded 8 mm, according to the standard accepted criteria [10]. On the basis of the radiologists' written reports, a single observer retrospectively and separately scored the probabilities of LNM, extracapsular extension, and seminal vesicle invasion using the following rating scale: 5, definite yes; 4, probable yes; 3, possible yes; 2, probable no; and 1, definite no [14].

Partin Staging Nomogram
Based on serum PSA, biopsy Gleason grade, and clinical staging, the likelihood of LNM according to the 2001 version of the Partin staging nomograms was recorded [21].

Histology
The histology reports from the core biopsies were all recorded at our institution and included the following: Gleason grade, greatest percentage of cancer in all biopsy cores, percentage of positive cores in all biopsy cores, and presence of perineural invasion. Radical prostatectomy specimens were examined as previously described by Yossepowitch et al. [29]. Standard template pelvic lymph node dissection was performed, encompassing all nodal tissue from the medial inferior margin of the external iliac vein down to the internal iliac and obturator vessels. Step-section histopathology findings were used as the standard of reference for extracapsular extension, seminal vesicle invasion, and LNM. Surgical margin status, pelvic lymph node status, presence of seminal vesicle invasion, and extracapsular extension were recorded.

Statistical Analysis
Both univariate and multivariate analyses were performed for all clinical and imaging variables to predict LNM. We evaluated the area under the receiver operating characteristic (ROC) curve for each variable. A model combining extracapsular extension and seminal vesicle invasion on MRI with the prediction of nodal disease and a model for the addition of the Partin nomogram to MRI were constructed; the areas under the ROC curves (AUCs) were calculated and compared [30]. For the multivariate models, the jackknife method, a form of resampling that reduces the optimistic bias, was used to obtain the bias-corrected probabilities and construct the ROC curves. A p value of less than 0.05 was considered significant. The sensitivity, specificity, negative predictive value, positive predictive value, and accuracy of MRI for the detection of LNM were determined, with positive LNM on MRI defined by a score of 3-5. Software programs used for data analysis were SAS, version 8.2 (SAS Institute), and S-PLUS, version 2000 (Insightful).

Results

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On surgical histopathology, positive lymph nodes were found in 22 (5%) of 411 patients. Table 2 summarizes the preoperative distribution of the clinical variables, and Table 3 shows the distribution of final pathologic staging [31]. Performance characteristics for each variable are listed in Table 4. In the evaluation of LNM, MRI had sensitivity and specificity of 27.27% and 98.46%, respectively, and positive predictive value and negative predictive value of 50% and 95.99%, respectively.

Univariate analysis (Table 5) showed that all variables were associated with LNM. In the prediction of LNM, the AUC for MRI was 0.633. In multivariate analysis, MRI (p = 0.002), Gleason score (p = 0.007), greatest percentage of cancer in all biopsy cores (p = 0.007), and PSA (p = 0.004) were significant predictors of LNM (Table 6).

In the prediction of LNM, each of the multivariate models that incorporated MRI findings regarding extracapsular extension and seminal vesicle invasion with MRI LNM findings had a greater AUC than the univariate model that included only MRI LNM findings (Fig. 1). The model that included all MRI variables (extracapsular extension, seminal vesicle invasion, and LNM) along with the Partin nomogram results had a significantly greater AUC than the univariate model that included only MRI LNM findings (Fig. 1; Table 7: model I vs model A, 0.892 vs 0.633, respectively; p < 0.01).

View larger version (27K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 1 —Graph shows that each multivariate model had greater area under receiver operating characteristic curve (AUC) than model A (green) (Table 7), which included only MRI findings for lymph node metastasis (LMN). Model combining MRI findings for seminal vesicle invasion and LNM (model F) (red) had greater AUC than model A: 0.714 vs 0.633, respectively (p = 0.08). Model combining MRI findings for extracapsular extension and LNM (model G) (blue) had greater AUC than model A: 0.798 vs 0.633, respectively (p = 0.15). Model combining MRI findings for extracapsular extension, seminal vesicle invasion, and LNM (model H) (yellow) had greater AUC than model A: 0.813 vs 0.633, respectively (p = 0.11). Model combining MRI findings for extracapsular extension, seminal vesicle invasion, and LNM and Partin tomogram prediction of LNM (model I) (black) had significantly greater AUC than model A: 0.892 vs 0.633, respectively (p < 0.01).

Discussion

Top Abstract Introduction Subjects and Methods Results Discussion References

 
Pretreatment knowledge of prostate cancer LNM is important for patient counseling and appropriate treatment selection and planning. The presence of LNMs at the time of prostate cancer diagnosis is associated with a high probability of progression after treatment and a poor prognosis [2, 4, 32].

Over the years, studies examining the association between a number of clinical variables and the prediction of LNM have been performed. The variables studied included serum PSA, Gleason grade, clinical stage, greatest percentage of cancer in all biopsy cores, percentage of positive cores in all biopsy cores, and perineural invasion [21, 33, 34]. Since the introduction of the Partin staging nomograms in 1993, investigators have repeatedly validated their capacity to predict LNM of clinically localized prostate cancer [22, 24, 25]. In a study by Cagiannos et al. [2] the overall predictive accuracy of the Partin tables as measured by AUC was 0.74, while the AUCs for the three- and four-variable nomograms developed by Cagiannos et al. were 0.76 and 0.78, respectively [2, 20]. In our study, the Partin nomograms-derived probability of LNM had an AUC of 0.899.

Given the strength of the Partin nomograms, what place, if any, does MRI have in the presurgical evaluation of prostate cancer and in lymph node staging in particular? The routine use of MRI for presurgical evaluation of prostate cancer is controversial because the high cost of the test might place a substantial burden on the health care system unless its use prevents unnecessary surgery or improves treatment planning and outcomes [35]. MRI has been shown to have incremental value in prostate cancer staging and treatment planning [26, 27]. MRI has also shown high specificity for LNM detection; however, the low sensitivity of MRI (0-69%) in detecting LNMs has been an obstacle to its widespread use. Table 1 is a summary of the results of the major studies on the use of MRI for prostate cancer LNM staging that have used surgical pathology as the standard of reference [6, 12].

The low sensitivity of MRI has been attributed mainly to the inability of cross-sectional imaging to detect metastases in normal-sized nodes [13, 14]. This limitation is especially important to consider in deciding when to use MRI in the current patient population because the incidence of LNM at diagnosis of prostate cancer has declined steeply and nodal metastases, when present, are often within normal-sized nodes. Tables 2 and 3 reflect the effects of prostate cancer downstaging on our study population, which was greater than the patient populations of all the other studies that used surgical pathology as the standard of reference (Table 1). Our overall positive lymph node rate of 5% confirms the decreasing incidence of LNM in prostate cancer patients [1, 2]. Therefore, our study should permit a contemporary assessment of the potential role of MRI in the current patient population.

Our study shows that the sensitivity of MRI for nodal metastases (27.27%) has not improved compared with the historical results [6, 12] (Table 1). However, we have also shown that in the prediction of LNM, a model that included the Partin nomograms with MRI findings regarding LNM, extracapsular extension, and seminal vesicle invasion had a significantly greater AUC (0.892) than a model that included only MRI LNM findings (AUC = 0.633; p < 0.01).

A study by Harisinghani et al. [14] showed that MRI with lymphotropic superparamagnetic nanoparticles has both high sensitivity (100%) and high specificity (95.7%) in detecting LNM. Although these findings are promising, it would be helpful to have a means of determining which patients are most likely to benefit from the use of nanoparticles, because the incidence of LNM at the time of radical prostatectomy in current studies is only 5% or less [2, 27, 28, 36]. Our data confirm that MRI has high negative predictive value for LNM and indicate that a combination of endorectal and phased-array MRI with the Partin tables has high accuracy in predicting LNM. Furthermore, MRI provides anatomic information that is useful for treatment planning. We therefore suggest that combined endorectal and phased-array MRI be used in conjunction with the Partin tables in determining whether imaging with lymphotropic superparamagnetic nanoparticles is warranted.

Summary
The combination of Partin nomograms and MRI findings regarding extracapsular extension, seminal vesicle invasion, and LNM offers high predictive value for LNM. Combined endorectal and phased-array MRI supplemented by the Partin nomograms could potentially be used to determine whether additional imaging with lymphotropic superparamagnetic nanoparticles is indicated.

Acknowledgments
 
We thank Filip Claus for productive discussions, Chinyere Onyebuchi for helping prepare the figures and legends, and Ada Muellner for editing the manuscript.

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