Dynamic MRI of Bladder Cancer: Evaluation of Staging Accuracy

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1 Genitourinary Imaging Tekes et al. MRI of ladder Cancer ylin Tekes 1 Ihab Kamel 1 Khursheed Imam 1 Gilberto Szarf 1 Mark Schoenberg 2 Khurram Nasir 3 Richard Thompson 4 David luemke 1 Tekes, Kamel I, Imam K, et al. Received February 24, 2004; accepted after revision June 14, Russell H. Morgan Department of Radiology, Johns Hopkins School of Medicine, 601 N Caroline St., Ste. 3235, altimore, MD ddress correspondence to I. Kamel (ikamel@jhmi.edu). 2 Department of Urology, rady Urological Institute, Johns Hopkins School of Medicine, altimore, MD Johns Hopkins School of Public Health, altimore, MD Department of Cardiology, Johns Hopkins School of Medicine, altimore, MD JR 2005;184: X/05/ merican Roentgen Ray Society Dynamic MRI of ladder Cancer: Evaluation of Staging ccuracy OJECTIVE. The purpose of this study was to evaluate the accuracy of gadoliniumenhanced MRI in staging bladder cancer in a series of patients with surgically proven bladder cancer. MTERILS ND METHODS. Seventy-one patients with biopsy-proven bladder cancer underwent MRI on a 1.5-T scanner with a phased-array pelvic coil. Conventional T1- weighted spin-echo, T2-weighted spin-echo, and unenhanced and enhanced (0.1 mmol/kg gadolinium) fast spoiled gradient-echo images with fat suppression were obtained. Two blinded reviewers evaluated the MR images and assigned a stage that was compared with the pathologic stage (n = 67) or with clinical follow-up for at least 2 years after MRI (n = 4). RESULTS. greement among the reviewers was good in assigning a radiologic stage for bladder cancer (kappa = 0.80). On a stage-by-stage basis, MRI accuracy was 62%, and overstaging was the most common error (32%). Staging accuracy improved to 85% and 82% in differentiating superficial from invasive tumors and organ-confined from non-organ-confined tumors, respectively. The time interval between MRI and transurethral resection ( 60 days and 61 days) was not a statistically significant factor in differentiating superficial from invasive and organ-confined from non-organ-confined tumors (p > 0.05). MRI accuracy in staging transitional cell carcinoma was not significantly different from that obtained in staging non transitional cell carcinoma (p > 0.05). CONCLUSION. MRI shows good reproducibility between reviewers for staging bladder cancer. lthough overall staging accuracy was only moderate, the accuracy for differentiating superficial versus invasive disease and organ-confined versus non-organ-confined disease was high. arcinoma of the urinary bladder is C one of the more common malignant tumors of the urinary tract in both male and female patients [1]. ccurate preoperative staging is the most important factor in determining the appropriate management of bladder carcinoma because the therapeutic method chosen and prognosis depend on the clinical and radiologic stage at presentation [2]. Superficial tumors can be treated by local endoscopic resection with or without adjuvant installation of chemotherapeutic agents, whereas invasive tumors are treated by curative cystectomy or by palliative chemotherapy or radiation therapy. Clinical staging can differentiate superficial tumors from invasive tumors [3]. However, clinical staging is not reliable for determining tumor extension beyond the bladder wall; therefore, imaging of the urinary bladder and the extravesical pelvis is needed [3]. Patients with extravesical tumors show significantly higher recurrence rates and worse survival than those with organ-confined tumors [4]. Therefore, distinguishing between organ-confined and non-organ-confined tumors is essential. Prior studies have reported that CT was a valuable tool in staging bladder carcinoma [5, 6]. MRI with dynamic contrast administration has been shown to be superior to CT, particularly in detecting superficial and multiple tumors and in detecting extravesical tumor extension and surrounding organ invasion [1, 5, 7 12]. The purposes of this study were to evaluate the overall accuracy of state-of-the-art dynamic gadolinium-enhanced MRI in staging bladder cancer on a stage-by-stage basis and to determine the usefulness of MRI in determining organ-confined versus non-organconfined disease, which is the main objective of imaging these patients. JR:184, January

2 Tekes et al. Materials and Methods Patient Selection Inclusion criteria for this study were that patients had undergone state-of-the art dynamic enhanced MRI examination, with bladder carcinoma pathologically documented within 6 months of imaging. search of our database identified MRI examinations of 71 consecutive patients with histologically proven bladder cancer who underwent imaging between January 1998 and June Permission to review these clinical MRI examinations and medical records for scientific research was granted before the study. MRI Technique Patients were imaged using a 1.5-T MR scanner (Signa, GE Healthcare) with a phased-array pelvic coil. Conventional T1-weighted spin-echo images (TR/TE, 550/9; matrix; 20-cm field of view; 6-mm section thickness; 2-mm intersection gap; 4 signals acquired) and T2-weighted fast spinecho images (TR range/te range, 4,000 5,500/80 120; matrix; 24-cm field of view; 6-mm section thickness; 2-mm intersection gap; 4 signals acquired) were obtained. Subsequently, fast multiplanar spoiled gradient-echo images with fat suppression ( / ; 70 flip angle; matrix; 20-cm field of view; 6-mm slice thickness; 2-mm intersection gap; 2 signals acquired) were obtained in the axial plane before and after gadopentetate dimeglumine (Magnevist, erlex) injection (0.1 mmol/kg). Enhanced images were acquired during the arterial phase (20 sec), which was immediately followed by the venous phase. The acquisition time was sec for each phase. Sagittal and coronal gadolinium-enhanced images were added if the tumor was located in the base or the dome of the bladder. These additional images were acquired in nine patients. Diagnostic MRI Criteria MR images were interpreted independently by two MR radiologists with special interest in urologic imaging without prior knowledge of the final staging obtained at transurethral resection, cystectomy, or clinical follow-up. Each reviewer assigned a radiologic stage using criteria similar to those previously described in the literature. On T2-weighted images, the normal bladder wall was identified as a hypointense line outlining the bladder lumen [5 7, 10, 13, 14]. On dynamic contrast-enhanced MR images, bladder tumors, mucosa, and submucosa (lamina propria) enhanced early, but the muscle layer maintained its hypointensity [9, 15]. n intact, hypointense line (muscle layer) at the base of the tumor was classified as stage T1; an irregular inner margin of hypointense line, stage T2a; a disrupted hypointense line without perivesical fat infiltration, stage T2b; a lesion with an irregular, shaggy outer border and streaky areas of the same signal intensity of the tumor in perivesical fat, stage T3b; and a lesion extending into an adjacent organ or abdominal and pelvic side walls with the same signal intensity of the primary tumor, stage T4a or T4b, respectively [8]. Lymph nodes were considered abnormal if the long axis was 10 mm or more [8]. ll patients included in our study were found to be free of distant metastasis before they were referred for MRI. Their workup for distant metastasis included chest CT, abdominal MRI, and bone scanning. Data nalysis Data were analyzed using STT software (version 7, Stata). Continuous variables were expressed as means ± SD. Interobserver agreement between the two MRI reviewers was calculated using kappa statistics. greement between observers was characterized by weighted kappa values and correlation coefficients. Kappa scores between 0.41 and 0.6 were considered moderate agreement; , good agreement; and greater than 0.80, excellent agreement [16]. Sensitivity, specificity, and accuracy of MRI were assessed on a stage-by-stage basis, and the gold standard was pathologic confirmation in all cases. Pathologic staging conformed to the updated TNM system of the International Union gainst Cancer [17] (Table 1). In addition, the data were regrouped to evaluate the accuracy of MRI staging in distinguishing superficial ( T1) from invasive ( T2) tumors and organ-confined ( T2b) from non-organ-confined ( T3) tumors. To analyze the effect of the time interval between MRI and prior transurethral resection on staging accuracy, we classified patients into two groups: patients who had transurethral resection 60 or fewer days before MRI and patients who had transurethral resection 61 or more days after MRI. Staging accuracy was evaluated separately for transitional cell carcinomas versus non transitional cell carcinomas. Significant differences were declared for p values less than Results total of 71 patients were included in the study: 62 men and nine women ranging in age between 38 and 88 years (mean, 64 years). efore MRI, all patients underwent clinical staging including cystoscopy and bimanual examination. In addition, 62 patients underwent transurethral resection days (mean, 61 days) before MRI. fter MRI, treatment was radical cystectomy (n = 39), partial cystectomy (n = 2), transurethral tumor resection (n = 26), or palliative radiation therapy (n = 3). The remaining patient had a history of in situ tumor and received intravesical chemotherapy before MRI. fter MRI, the patient had urine analysis and cystoscopy and was found to be disease-free. Therefore, no additional treatment was necessary. ll patients received treatment within 150 days (mean, 31 days) after MRI. Forty-one (58%) of the 71 patients had pelvic lymphadenectomy. For the remaining 30 patients (42%), the absence of lymph node involvement was established by clinical follow-up and MRI studies at 6-month intervals for at least 2 years. Histologic diagnoses were transitional cell carcinoma (n = 60), squamous cell carcinoma (n = 1), adenocarcinoma (n = 6), small cell carcinoma (n = 1), and carcinosarcoma (n = 3). Tumor ppearance The final pathologic staging revealed 24 patients with stage Ta T1 disease, 10 with stage T2b, 21 with stage T3a b, five with T4a, and two with stage T4b. None of the patients had stage T2a tumor. Nine patients were stage T0. These patients initially had in situ or lamina propria in- TLE 1 Stage Ta Tis T1 T2a T2b T3a T3b T4a T4b N0 N1 N2 N3 M0 M1 TNM Classification for ladder Cancer (1997) [17] Characteristics Noninvasive papillary carcinoma Carcinoma in situ: flat tumor Tumor invades subepithelial connective tissue Tumor invades superficial muscle (inner half) Tumor invades deep muscle (outer half) Tumor invades perivesical tissue microscopically Tumor invades perivesical tissue macroscopically Tumor invades prostate or uterus or vagina Tumor invades pelvic wall or abdominal wall No regional lymph node metastasis Metastasis in a single lymph node 2 cm in greatest dimension Metastasis in a single lymph node > 2 cm but 5 cm in greatest dimension, or multiple lymph nodes Metastasis in lymph node > 5 cm in greatest dimension No distant metastasis Distant metastasis 122 JR:184, January 2005

3 MRI of ladder Cancer vasive tumors, and they received intravesical chemotherapy. MRI was indicated to stage their disease. fter MRI, biopsy confirmed the absence of disease. These patients were followed up every 6 months for 2 years, and none of the follow-up examinations revealed tumor recurrence. Tumors were detected in 62 (87%) of the 71 patients on pathologic confirmation. Of these patients, 45 patients (63%) had mass lesions, whereas 17 (24%) had diffuse wall thickening. Of the mass lesions, 20 were papillary and 25 were sessile. Tumor size ranged from 0.5 to 7.3 cm (mean, 2.5 cm). Twelve patients had multiple tumors; in such cases, the highest tumor stage present was used for the analysis. ll 62 detected tumors were isointense relative to bladder wall muscle on T1-weighted images. On T2-weighted images, 50 tumors (81%) were isointense and 12 (19%) were slightly hyperintense relative to muscle. On dynamic contrast-enhanced MR images, all tumors had increased enhancement compared with uninvolved bladder. Fifty-three tumors (85%) showed early, intense enhancement on images obtained beginning 20 sec after gadolinium administration. Eight tumors showed heterogeneous enhancement at 20 sec, whereas one of the tumors showed superficial enhancement on the delayed images. Tumor Staging Interobserver agreement was good in assigning a radiologic stage (kappa = 0.80). TLE 2 Staging Results in 71 Patients on Stage-by-Stage asis (Reviewer 1) MRI Stage Sixty-two tumors that were present at the time of imaging were detected correctly (sensitivity of 100%). On a stage-by-stage basis, tumors were staged correctly in 44 (62%) of 71 patients (Figs. 1 3), overstaged in 23 patients (32%) (Fig. 4), and understaged in four patients (6%) for reviewer 1 (Table 2). Reviewer 2 correctly staged on a stage-by-stage basis 37 (52%) of 71 tumors, overstaged tumors in 26 patients (37%), and understaged tumors in eight patients (11%) (Table 3). Staging accuracy was evaluated several ways to reflect clinical utility. Despite the good interobserver agreement, we used the Histopathology Stage T0 Ta T1 T2a T2b T3a T3b T4a T4b Total T Ta T T2a T2b T3a T3b T4a T4b Total Note. Numbers in boldface indicate number of correctly staged patients in each row. Sum of numbers under each bold number represents overstaged cases; sum of numbers above each bold number represents understaged cases. scores of both reviewers to perform additional statistical analysis. ll T0 tumors (n = 9) were excluded from further analysis because they were found to be tumor-free after stage-by-stage analysis. We evaluated the ability of MRI to distinguish between superficial (those without muscle invasion) and invasive tumors (Tables 4 and 5). Of the 62 tumors, 53 were staged correctly, eight were overstaged, and one was understaged, yielding an overall accuracy of 85%. We also evaluated the accuracy of MRI in classifying organ-confined (those within the bladder) versus non-organ-con- Fig. 1. Images in 58-year-old man with correctly staged papillary (Ta) transitional cell carcinoma of bladder., xial T2-weighted image (TR/TE, 4,000/80) shows polypoid mass (arrow) arising from right posterolateral wall with homogeneous low signal intensity. Note that low-signal muscular layer is intact., xial arterial phase gadolinium-enhanced image (200/2.9) shows bright, homogeneous enhancement of mass (arrow). JR:184, January

4 Tekes et al. fined tumors. Of the 62 cases, 51 were correctly classified, seven were overstaged, and four were understaged, yielding an overall accuracy of 82%. The effect of the time interval between MRI and biopsy on staging accuracy was assessed. One group included patients who underwent transurethral resection 60 or fewer Fig. 2. Images in 70-year-old man with correctly staged T2b transitional cell carcinoma of bladder., xial T2-weighted image (TR/TE, 4,000/80) shows that sessile mass arising from right lateral wall (arrow) disrupts low-signal-intensity muscle layer., xial arterial phase gadolinium-enhanced image (200/2.9) shows early enhancement of sessile mass (arrow). days (mean, 33 days) before MRI (n = 34), and the second group (n = 28) included patients who had transurethral resection 61 or more days (mean, 95 days) before MRI. Staging accuracy between the two groups was not statistically different in classifying superficial tumors from invasive tumors or in differentiating organ-confined tumors from non-organ-confined ones (p > 0.05) (Tables 6 and 7). Eleven patients (15%) had non transitional cell carcinoma, and 60 patients (85%) had transitional cell carcinoma. Seven (64%) of the 11 cases of non transitional cell carcinoma were staged correctly, and 37 (62%) of the 60 cases with transi- Fig. 3. Images in 68-year-old man with correctly staged T4a transitional cell carcinoma of bladder., xial T2-weighted image (TR/TE, 4,000/80) obtained above level of mass shows two diverticula arising from ureterovesical junction bilaterally (white arrows) and left hydroureter (arrowhead). Note enlarged left external iliac lymph nodes (black arrows)., xial arterial phase gadolinium-enhanced image (200/2.9) obtained slightly lower than shows polypoid tumor with homogeneous enhancement arising from left base of bladder (small short arrow) and extending into perivesical fat (arrowheads). Note that asymmetric enhancement in left seminal vesicle (large short arrow) correlates with organ invasion at radical cystectomy. Enlarged right inguinal lymph node (long arrow) also can be seen. 124 JR:184, January 2005

5 MRI of ladder Cancer tional cell carcinoma were staged correctly. Staging accuracy was not statistically different between transitional and non transitional cell carcinoma (p > 0.05). Of the 71 patients, 10 had pathologic lymph node involvement. mong the findings for the 61 patients who were free of lymph node involvement, there was one false-positive MR interpretation by both reviewers. The false-positive lymph node was benign at pathology, but on MRI it exceeded 10 mm in the long axis (14 mm). oth reviewers correctly detected lymph node involvement in seven of 10 patients on MRI, resulting in an accuracy of 96%, sensitivity of 78%, and specificity of 98%. Discussion Our study was performed on a large group of patients with pathologically proven bladder carcinoma who underwent state-of-theart MRI for preoperative staging. We have shown that MRI staging of bladder cancer is highly reproducible among experienced reviewers with pathologic confirmation of the disease stage in all cases (kappa = 0.80). Our overall accuracy of dynamic MRI on a stageby-stage basis was 62%. Overstaging was the most common error (32%) in the current study (Tables 2 and 3), contrary to the findings of a prior study by uy et al. [10] who used a 0.5-T MR scanner without contrast ad- Fig. 4. Images in 56-year-old woman with stage T3b transitional cell carcinoma of bladder. Tumor was overstaged by both reviewers., xial T2-weighted image (TR/TE, 4,000/80) shows tumor with heterogeneous signal intensity disrupting bladder wall and causing left hydroureter (large arrow). Note lymph node in left obturator chain (arrowhead). No clear fat plane (small arrows) is visible between uterus and tumor, suggesting uterine invasion. No uterine invasion was detected at pathology., xial venous phase fast spoiled gradient-echo image (200/1.9) obtained after administration of gadolinium shows intense enhancement of sessile mass arising from left lateral wall and filling most of bladder lumen. Note loss of fat plane (arrows) between uterus (arrowhead) and mass. TLE 3 Staging Results in 71 Patients on Stage-by-Stage asis (Reviewer 2) MRI Stage Histopathology Stage T0 Ta T1 T2a T2b T3a T3b T4a T4b Total T Ta T T2a T2b T3a T3b T4a T4b Total Note. Numbers in boldface indicate number of correctly staged patients in each row. Sum of numbers under each bold number represents overstaged cases; sum of numbers above each bold number represents understaged cases. TLE 4 ccuracy of MRI in Differentiating Superficial ( T1) from Invasive ( T2) and Organ-Confined ( T2b) from Non Organ-Confined ( T3) Disease (Reviewer 1) T1 vs T (74 92) T2b vs T (77 94) JR:184, January

6 Tekes et al. TLE 5 ccuracy of MRI in Differentiating Superficial ( T1) from Invasive ( T2) and Organ-Confined ( T2b) from Non Organ-Confined ( T3) Disease (Reviewer 2) T1 vs T (66 86) T2b vs T (69 89) TLE 6 Effect of Time Interval etween MRI and Transurethral Resection in Staging ccuracy (Reviewer 1) 60 days (n =39) T1 vs T (69 95) a T2b vs T (66 93) b 61 days (n =32) T1 vs T (71 98) a T2b vs T (80 100) b a For differentiating T1 vs T2 between 60 days and 61 days, p > b For differentiating T2b vs T3 between 60 days and 61 days, p > TLE 7 Effect of Time Interval etween MRI and Transurethral Resection in Staging ccuracy (Reviewer 2) 60 days (n = 39) T1 vs T (66 93) a T2b vs T (63 91) b 61 days (n = 32) T1 vs T (55 88) a T2b vs T (67 96) b a For differentiating T1 vs T2 between 60 days and 61 days, p > b For differentiating T2b vs T3 between 60 days and 61 days, p > ministration and reported an accuracy of 60%. The most common staging error reported in that study was underestimation (33%) of tumor extent. The improvement of image resolution in our study likely led to improved detection of perivesical fat stranding, which was frequently reactive or inflammatory rather than metastatic but was thought by our reviewers, on occasion, to represent extravesical spread of tumor. Our staging accuracy was lower than those previously reported, which ranged between 72% and 95%. However, those studies were performed using lowfield-strength scanners without dynamic contrast administration and a small sample size [5, 7, 13]. Clinical management primarily is based on distinguishing superficial (Fig. 1) from muscle-invasive (Fig. 2) disease. pproximately two thirds of all bladder cancers are superficial, and treatment options differ dramatically between superficial and invasive disease. Superficial tumors are treated with local endoscopic resection with or without adjuvant intravesical installations of chemotherapeutic agents, whereas invasive tumors are treated by curative cystectomy and palliative chemotherapy, radiation therapy, or both. One of the most important reasons for performing preoperative imaging is distinction of organ-confined disease from tumor that has spread outside the bladder (Figs. 3 and 4). lthough clinical staging including transurethral resection or biopsy can distinguish superficial from invasive tumors, it is not capable of detecting extravesical disease. This distinction is important because patients with non-organconfined disease have higher recurrence rates and worse survival rates than patients with organ-confined disease [4]. Our staging accuracy was 85% for assessing superficial versus invasive disease and was slightly lower than that reported in the literature by Scattoni et al. [18], who reported an accuracy of 92% using a 0.5-T MR scanner with contrast administration. Our accuracy in differentiating organ-confined from non-organ-confined tumors was 82% and also was lower than that reported in a 1988 study by uy et al. [10]; those researchers reported an accuracy of 95% using a 0.5-T MR scanner without any contrast administration. However, our accuracy in differentiating organconfined from non-organ-confined tumors was higher than the 73% accuracy reported in a previous study that included patients who underwent transurethral resection 7 16 days before MRI [11]. Management of bladder carcinoma starts with cystoscopy, bimanual examination, and transurethral resection. The value of transurethral resection is to confirm the histology and to stage the tumor. In addition, transurethral resection alone or combined with intravesical chemotherapy may provide definitive therapy for superficial bladder tumors, which account for approximately two thirds of all bladder carcinomas. Transurethral resection before MRI has been suggested as a possible cause of overstaging bladder carcinoma [19], because the differentiation between acute edema or hyperemia due to transurethral resection and tumor is stated to be difficult, especially immediately after transurethral resection [12, 15, 20 23]. The differentiation is difficult on T2-weighted images and gadolinium-enhanced images [8, 15, 23, 24]. ll patients referred for MRI at our institution undergo transurethral resection or biopsy before MRI. Therefore, excluding these patients is not a practical approach before radiologic staging of bladder carcinoma. To evaluate the effect of the time interval between transurethral resection and MRI on 126 JR:184, January 2005

7 MRI of ladder Cancer staging accuracy, we classified the patients into two groups. Our analyses show that there is no statistically significant difference in staging accuracy between groups with a short ( 60 days) versus long ( 61 days) duration between MRI and transurethral resection or in differentiating superficial from invasive disease and organ-confined from non-organconfined disease. These findings are in agreement with a previous study that showed there was no statistically significant difference in staging 1 week (early) versus 4 weeks (late) after transurethral resection [1]. However, in that study, both time intervals between transurethral resection and MRI were within the short-duration group that we defined in the current study. Our study group consisted of 11 patients with non transitional cell carcinomas, including squamous cell carcinoma, adenocarcinoma, small cell carcinoma, and carcinosarcoma. Non transitional cell carcinoma is reported to differ from transitional cell carcinoma. These tumors are less common and generally are larger than transitional cell carcinomas. In addition, they are aggressive and usually extend beyond the bladder wall at the initial time of diagnosis [25 27]. Our results show that there is no statistically significant difference in the accuracy of MRI for staging transitional and non transitional cell carcinomas on a stage-by-stage basis and for differentiating superficial from invasive and organ-confined from non-organ-confined tumors. We conclude that MRI staging of bladder tumors is reproducible among reviewers. On a stage-by-stage basis, the accuracy of MRI is 62%, with overstaging being the most common error. However, when certain specific features of bladder cancers are assessed, MRI is considerably more accurate. 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