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1 Department of Radiology, Klinikum rechts der Isar der Technischen
Universität München, Ismaninger Str. 22, D-81675 Munich,
Germany.
2 Present address: Division of Diagnostic Radiology, Mallinckrodt Institute of
Radiology, Washington University School of Medicine, 510 S. Kingshighway
Blvd., St. Louis, MO 63110.
3 Department of Urology, Klinikum rechts der Isar der Technischen
Universität München, D-81675 Munich, Germany.
Received June 4, 2001;
accepted after revision December 7, 2001.
Address correspondence to M. Lämmle.
Abstract
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SUBJECTS AND METHODS. Twenty-five patients with urinary bladder cancer diagnosed on conventional cystoscopy underwent MR imaging of the pelvis. Patients were examined without external bladder filling or administration of IV contrast medium. No medications were administered. The data obtained by MR imaging were reconstructed for virtual endoscopy on a workstation. The locations and sizes of tumors were individually determined and compared with results of conventional cystoscopy.
RESULTS. Twenty-four patients were evaluated; one patient's examination was excluded from analysis because of metallic artifacts. Seventeen patients were diagnosed with a single bladder tumor. Five patients had two tumors each, and two patients had three tumors. Tumor diameter ranged from 0.4 to 6.4 cm. Thirty (90.9%) of 33 tumors detected on cystoscopy were visualized with virtual endoscopy. The detection rate for 23 tumors of 1 cm or greater was 100%. Difficult conditions for conventional cystoscopy, including hematuria, anterior wall involvement, and urethral strictures, had no deleterious impact on virtual cystoscopy. Difficulties in detection on virtual endoscopy were associated with flat bladder tumors with minimal surface elevation.
CONCLUSION. The results of this study suggest a high reliability in the diagnosis of urinary bladder cancer by MR imaging—based virtual cystoscopy—a noninvasive method, independent of medication or contrast enhancement, that may be of value for screening, primary diagnosis, and surveillance. Virtual MR cystoscopy may be indicated when conventional cystoscopy cannot be performed or is ineffective.
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Urinary bladder cancer is a frequently occuring malignancy with a high rate of recurrence and multifocal manifestations, and therefore it requires reliable diagnostic techniques [8,9,10,11]. The purpose of this study was to evaluate MR imaging—based virtual endoscopy in patients with urinary bladder cancer compared with the gold standard—that is, conventional cystoscopy—and to determine the modality's detection rate and positive predictive value. In addition, we wanted to discover the advantages and disadvantages of the new method and to determine whether suspected urinary bladder cancer is a good indication for virtual endoscopy.
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The patients' clinical histories varied. Twenty-one patients presented with painless hematuria or with dysuria, and a primary tumor was found in each patient. Four patients with a history of transurethral resection had recurrent tumor disease that was detected on follow-up cystoscopy.
Of the 25 patients studied, one patient's examination was not acceptable for reconstruction because of strong artifacts from a hip prosthesis. That patient was excluded from analysis. The other 24 patients had examinations of satisfactory image quality and were evaluated.
Cystoscopy
Details regarding estimated size, location, and number of tumors found on
cystoscopy were obtained from the cystoscopic reports provided by the
Department of Urology. Techniques used for conventional cystoscopy included,
in 21 patients, rigid cystoscopy with a field of view of 30-45° and, in
three patients, flexible fiberoptic cystoscopy with a 90° field of view.
Number, location, and size of the tumors were individually determined and
noted after cystoscopy for later comparison with the results of MR
imaging—based virtual endoscopy.
MR Technique
MR imaging was performed without external bladder filling or administration
of IV contrast medium. No medications were given. The patients were instructed
to start drinking water 1 hr before the MR imaging study and to present with a
full bladder.
All examinations were performed on a 1.5-T scanner (Gyroscan ACS-NT; Philips Medical Systems, Best, The Netherlands) using a five-element phased array coil. We performed a T2-weighted three-dimensional turbo spin-echo sequence for data acquisition with the following parameters: TR/TE, 2911/650; echo train, 128 (effective train length, 100); matrix, 128 x 256; reconstruction matrix, 256 x 256; flip angle, 90°; field of view, 350 mm; excitations, 2; signal averages, 2; voxel size, 1.4 (x) x 1.9 (y) x 2.0 (z) mm3; number of slices, 100; and interpolated slice thickness, 1.0 mm. The acquisition time of the sequence was 4 min 8 sec.
Image Analysis
A coronal scout image was obtained to localize the urinary bladder and to
visualize filling status and size of the bladder of patients undergoing MR
imaging. Coronal imaging was performed as a standard scanning plane.
Data were reconstructed on a postprocessing workstation (Easy Vision; Philips Medical Systems). The hardware consisted of a workstation (Sun Microsystems, Palo Alto, CA). The data were transferred via intranet using DICOM (Digital Imaging and COmmunications in Medicine) standards. Surface rendering was used to generate a standardized three-dimensional interactive intraluminal image of the urinary bladder.
The region of interest was chosen from the data, and surrounding structures were segmented out. For reconstruction of a urinary bladder that presented with high signal intensity in comparison with the surrounding tissue, an upper threshold was selected on a scale with a range from 1 to 1000 units. The upper threshold was set at approximately 450 (420-480) units for three-dimensional reconstruction. Using multiplanar reformation from source images, a central observation point was defined in the middle of the lumen of the bladder. The obtained reconstruction was visualized in two standard-perspective projections, rotated horizontally and vertically. In this manner, reconstruction was standardized to view internal bladder surfaces in all areas.
First we created an overall view by spinning from the central observation point. A field of view of 120° was applied to the vertical and horizontal planes, so that we could visualize the bladder neck; the vesical trigone with the ureteric orifices and the internal urethral orifice; the right, posterior, left, and anterior bladder wall; and the vesical dome. Then we used a field of view of 90° and the zoom function to scan the mucosa for small tumors. This search pattern was followed in all patients.
Virtual endoscopy was performed and analyzed by one radiologist who was unaware of the other findings. The number, location, and size of the tumors were individually determined and noted after standardized virtual endoscopy for later comparison with the results of conventional cystoscopy.
Statistical Analysis
Findings from both methods—conventional cystoscopy and virtual
endoscopy—were analyzed to determine the detection rate and positive
predictive value of MR imaging—based virtual endoscopy in the diagnosis
of urinary bladder tumors.
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Evaluation of the results of tumor detection by cystoscopy and MR imaging—based virtual endoscopy is shown in Figures 1 and 2. On conventional cystoscopy, 33 tumors were found in 24 patients. Among those, 17 patients (70.8%) were diagnosed with a single bladder tumor. Five patients (20.8%) had two tumor locations, and two patients (8.3%) had three tumors. One or more tumors were found on virtual endoscopy in all patients, and all known single tumors were identified. In two patients with two known tumors each, only one tumor was detected; in one patient with three tumor locations, only two were identified by virtual endoscopy. Thus, in total, 30 of 33 known tumors were identified by virtual MR cystoscopy (Fig. 1).
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Two tumors that were not identified on initial cystoscopy were detected by virtual endoscopy. In one patient, the tumor was very small (0.5 cm in maximum diameter) and was located on the anterior bladder wall. Additionally, cystoscopy was complicated by moderate hematuria in this patient. In the second patient, a 2.1-cm tumor located at the dome of the bladder was not seen on initial cystoscopy because vision was restricted by the presence of marked hematuria. These findings were confirmed by repeated conventional cystoscopy after coagulation of bleeding tumors and bladder washings at the time of transurethral resection.
Tumor size ranged from 0.4 to 6.4 cm in diameter (mean size, 2.1 cm). Virtual endoscopy depicted all 23 known tumors with a diameter of 1 cm or greater and seven of 10 known tumors smaller than 1 cm (Fig. 2). Thus the detection rate for those small tumors was 70%. Detection rate for tumors larger than 1 cm was 100%. Thirty of 33 tumors detected on conventional cystoscopy were identified with virtual endoscopy, corresponding to an overall detection rate of 90.9%. Virtual endoscopy revealed two tumors that were not seen on cystoscopy, which represented our gold standard. Therefore, per definition, the positive predictive value of virtual endoscopy is 93.8%. However, the positive predictive value is 100% if we consider the fact that the two tumors revealed on virtual endoscopy were confirmed later intraoperatively, and, therefore, no false-positive findings resulted from virtual endoscopy.
Difficult conditions for conventional cystoscopy, including hematuria, anterior wall involvement, and urethral strictures, had no impact on virtual endoscopy. Standardized reconstruction of data sets guaranteed a complete examination of all areas of the mucosa of the bladder. Even very small tumors were easily identified in virtual endoscopic reconstruction using the zoom function in the software tools. Difficulties in detection were associated with small, flat bladder tumors that caused only a slight elevation of surface structure. Three masses smaller than 1 cm in diameter and without significant contour elevation from the bladder wall into the lumen were not found on virtual endoscopy. The three undetected tumors were histologically superficial tumors. Two of the tumors were staged pTa, G1 and one was staged pT1(is), G3 on histology after transurethral resection.
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The urinary bladder tumor has a high tendency toward multifocality (
50%
of all cases) [10] and recurs
after treatment—either at the initial tumor site or elsewhere throughout
the transitional epithelium—in 30-80% of patients
[8,
9,
11]. Considering the specific
features of the disease, it is important to apply diagnostic methods with a
maximum sensitivity and the capability to reliably visualize the entire
organ.
Virtual MR endoscopy is a recently developed noninvasive method to detect tumors protruding from the walls of hollow organs. A promising advantage of this imaging modality is that views not possible in conventional endoscopic examination can be created [1]. At present, it is important to gather information about the reliability of the new method compared with conventional cystoscopy, which is the gold standard for detection of bladder tumors. This pilot study contributes to the growing experience in this new field. Although further clinical trials must be performed to reach statistical significance, our study found a high overall detection rate (90.9%) for bladder tumors. The detection rate for tumors of 1 cm in diameter or greater was 100%.
Virtual endoscopy revealed two tumors that were not seen on cystoscopy, our gold standard. Therefore, per definition, the positive predictive value for virtual endoscopy is 93.8%. Considering the two tumors revealed by virtual endoscopy as true-positive because they were confirmed later intraoperatively, the positive predictive value is 100%. Given the detection rate and positive predictive value found in this study, a high sensitivity and specificity can be expected for the presented method.
The primary advantage of virtual endoscopy versus cystoscopy is that virtual MR cystoscopy is a noninvasive technique. Cystoscopy is an invasive and uncomfortable procedure for patients, and complications such as infections, perforation, scarring, and stricture of the urethra have been observed [13,14,15,16,17]. No complications resulted from MR imaging—based virtual endoscopy in our study.
Cystoscopy is often difficult to perform adequately when exploring the anterior bladder wall or the lumen of a diverticulum [18, 19]. The anterior bladder wall is a common location of bladder tumors [20]. Primary intradiverticular carcinomas are rare, but diagnosis is often difficult and prognosis is relatively poor. Therefore, imaging plays an important role in these cases [18, 19, 21,22,23]. Access to the anterior bladder wall (Fig. 3A,3B) or the lumen of a diverticulum is not restricted in virtual endoscopy because various software reconstruction tools can be used. A virtual observation point can be placed individually, and individual path tracking permits easy access to all areas of the hollow organ and visualization of the mucosa. Free choice of angle and the ability to magnify a focal point (zoom in) allow detection of small lesions (Fig. 4A,4B).
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In our study, at least two instances of neoplasm were not initially detected on conventional cystoscopy because of poor visibility related to hematuria. In distinction, visibility and detection of tumors on virtual endoscopy is not affected by hematuria.
The disadvantages of virtual MR cystoscopy versus cystoscopy include difficulties in detecting flat tumors, and the fact that it is not possible to visualize the lumen of the urethra as is routinely done with conventional cystoscopy. Differentiation between small tumors and inflammatory swelling of the mucosa may be difficult, especially in patients with unsatisfactory bladder filling in whom folding of the vesical mucosa occurs. Inflammatory swelling of the mucosa thus could be misdiagnosed as a tumor, or small tumors could be missed on virtual endoscopy. Another disadvantage is that patients with metal prostheses or implants cannot be adequately examined. Finally, in MR imaging—based virtual endoscopy, the scanning and reconstructing process is lengthy and costly. This factor, at present, limits the usefulness of this technique as a screening tool.
Raw data from MR imaging provide a sufficient basis for reconstruction. Patients do not need to undergo CT and the external bladder filling used in CT-based virtual endoscopy, which has been described by authors who report a tumor detection rate in their studies that is similar to the results of our MR imaging—based study [2,3,4]. Performing standardized reconstruction of our MR imaging raw data sets provided accurate and clinically useful visualization (Fig. 5A,5B,5C,5D).
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Our experience with virtual MR cystoscopy showed that once the operator becomes familiar with the intraluminal perspective, time needed for postprocessing could be reduced by establishing a routine in performing and analyzing endoscopic views. Postprocessing and evaluation of virtual cystoscopic views were performed in approximately 15-40 min, depending on reviewers' experience, hard disk usage of the workstation, zoom status, artifacts, mucosal morphology, and the number of tumors.
In assessing virtual endoscopic images, we observed striping and wrap-around artifacts. The causes are probably related to motion artifacts resulting from long TE. Possible causes of motion artifacts are scanner vibration and detrusor contractions. The artifacts possibly interfere with detection of small lesions and thus may affect the detection rate and positive predictive value of the method. Breath-triggered examinations were not successful in preventing artifacts; therefore, it seems that breathing motion may not affect image quality.
Postprocessed images must be established from cross-sectional source data that can be used as a tool for the assessment of virtual endoscopic images. For interpretation of the reconstructed virtual endoscopic image, using the coronal T2-weighted source images is recommended for spatial orientation and quick assessment of the dimensions of a tumor that is already visible in cross-sectional imaging.
Source images were used to provide a first overview. However, cross-sectional imaging for tumor detection is often confusing and is, therefore, not recommended (Fig. 6A,6B). In patients with diverticula, it is often impossible to differentiate between wall segments of diverticula and small tumors.
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It is useful, in assessing the intravesical image, to focus first on the vesical trigone with the ureteric orifices and the internal urethral orifice in anteroposterior orientation—similar to the generally practiced standard in conventional cystoscopy (Figs. 3A, 5D, and 6B). From this position, it is possible to proceed to successively visualize all areas of the mucosa of the bladder and perform a standardized reconstruction. Standardizing reconstruction allows easy orientation inside the lumen of the bladder and identification of the exact tumor position on the internal bladder wall. Therefore, mapping of the internal surface of the bladder wall is possible. This technique allows examination of the complete organ and provides accurate and reproducible results. These characteristics are important to fulfill the requirements of diagnosing urinary bladder cancer, which has a high rate of multifocality and recurrence.
When MR imaging is used as the basis for virtual endoscopic reconstruction, there is an obvious interest in simultaneous contribution of the MR images to clinical staging of the bladder tumors by revealing information about depth of invasion, metastasis of lymph nodes, and infiltration of pelvic organs. Barentsz et al. [24] compared accuracy of different staging techniques for bladder carcinoma and showed the potential use of MR imaging in this field. Beyersdorff et al. [25] identified even small tumors with a T2-weighted turbo spin-echo sequence after intravesical administration of superparamagnetic iron oxide particles, but they found it was not possible to reliably differentiate the layers of the bladder wall. However, MR imaging can provide only indicative information for staging of bladder cancer. Staging of bladder cancer and the deduced prognosis and therapeutic strategies depend primarily on histologic analysis; staging; and grading of a specimen from transurethral resection, biopsies, or cytology [8, 9, 11, 26]. MR imaging cannot yet provide differentiation of histologic layers of the urinary bladder wall or provide a definitive diagnosis without histopathologic confirmation [24, 25, 27].
On the basis of the results of this study and our experience with conventional cystoscopy and virtual endoscopy, we propose that virtual cystoscopy is indicated when conventional cystoscopy is difficult to perform, restricted in feasibility, unsatisfactory in interpretation, or contraindicated. Contraindications for cystoscopy are bacteriuria, acute cystitis, urethritis, prostatitis, obstructive prostatic hypertrophy, and stricture or rupture of the urethra. Factors that limit the technical success of cystoscopy, thereby decreasing its reliability, include marked hematuria, bladder diverticula, and poor visibility of the anterior urinary bladder wall. Occasionally, after cystoscopy, there are no pathologic findings in spite of a strong clinical suspicion of bladder cancer. In these patients, virtual cystoscopy can be used complementary to conventional cystoscopy to enhance diagnostic performance. MR imaging—based virtual endoscopy is also indicated for patients who are at risk of complications such as hemorrhage, perforation, infection, or pain, and for the examination of young patients. The modality may also be used at the patient's request.
In the future, we expect improved detection rate and sensitivity for even very small tumors through continued development and advancement of hardware and software, with the possible use of virtual MR cystoscopy for screening and follow-up of bladder cancer, and in the clinical setting in which cystoscopy cannot be performed or is ineffective.
In conclusion, the results of our study suggest a high reliability in the diagnosis of urinary bladder cancer by MR imaging—based virtual cystoscopy. This noninvasive method, independent of any medication or contrast enhancement, can be of value for screening, primary diagnosis, and surveillance of bladder cancer, which is a frequent malignancy with a high rate of recurrence and multifocal manifestations. At this time, virtual MR cystoscopy may be indicated as a clinical routine when conventional cystoscopy is contraindicated or restricted in feasibility or interpretation; when there is risk of hemorrhage, perforation, or pain; for young patients; or if a patient wishes a noninvasive assessment of bladder mucosa.
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