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1 Russell H. Morgan Department of Radiology, Johns Hopkins School of Medicine,
601 N Caroline St., Ste. 3235A, Baltimore, MD 21287.
2 Department of Urology, Brady Urological Institute, Johns Hopkins School of
Medicine, Baltimore, MD 21287.
3 Johns Hopkins School of Public Health, Baltimore, MD 21287.
4 Department of Cardiology, Johns Hopkins School of Medicine, Baltimore, MD
21287.
Received February 24, 2004;
accepted after revision June 14, 2004.
Address correspondence to I. Kamel
(ikamel{at}jhmi.edu).
Abstract
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MATERIALS AND 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. Agreement 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. Although overall staging accuracy was only moderate, the accuracy for differentiating superficial versus invasive disease and organ-confined versus non-organ-confined disease was high.
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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-organ-confined disease, which is the main objective of imaging these patients.
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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; 512 x 192 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; 256 x 256
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 (180–300/1.7–4.2;
70° flip angle; 512 x 92 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, Berlex)
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 52–86 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].
An 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].
All 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 Analysis
Data were analyzed using STATA software (version 7, Stata). Continuous
variables were expressed as means ± SD. Interobserver agreement between
the two MRI reviewers was calculated using kappa statistics. Agreement between
observers was characterized by weighted kappa values and correlation
coefficients. Kappa scores between 0.41 and 0.6 were considered moderate
agreement; 0.61–0.80, 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 Against 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.
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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 0.05.
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All 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 Appearance
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 invasive
tumors, and they received intravesical chemotherapy. MRI was indicated to
stage their disease. After 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.
All 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). 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.
1A,
1B,
2A,
2B,
3A, and
3B), overstaged in 23 patients
(32%) (Figs. 4A and
4B), 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).
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Staging accuracy was evaluated several ways to reflect clinical utility. Despite the good interobserver agreement, we used the scores of both reviewers to perform additional statistical analysis. All 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-confined tumors. Of the 62 cases, 51 were correctly classified, seven were overstaged, and four were understaged, yielding an overall accuracy of 82%.
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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 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).
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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 transitional 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. Among 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). Both 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%.
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Clinical management primarily is based on distinguishing superficial (Figs. 1A and 1B) from muscle-invasive (Figs. 2A and 2B) disease. Approximately 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. 3A, 3B, 4A, and 4B). Although 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-organ-confined 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 Buy 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 organ-confined 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]. All 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 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-organ-confined
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. Overall, staging accuracy of MRI is 85% and 82% in differentiating superficial tumors from invasive disease and organ-confined tumors from non-organ-confined disease, respectively. Continued improvements in MR hardware, such as the advent of higher-magnetic-field-strength MR scanners and higher-resolution imaging techniques may aid in improving staging accuracy further.
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