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Dynamic Gadolinium-Enhanced Magnetic Resonance Imaging in Staging of Superficial Bladder Cancer
0022-6347/96/1556-1594$03.W/0
Vol. 155. 1594-1599, May 1996 Printed in U.S.A.
"KE JOUBNAL OF uR0uX;U Copyright 8 1996 by AMEIUCAN UROLOCICAL AS~OCUTION,h c .
DYNAMIC GADOLINIUM-ENHANCED MAGNETIC RESONANCE IMAGING IN STAGING OF SUPERFICIAL BLADDER CANCER VINCENZO SCATTONI, LUIGI F. DA POZZO, RENZO COLOMBO, LUCIAN0 NAVA, PATRIZIO RIGATTI, FRANCESCO DE COBELLI, ANGEL0 VANZULLI AND ALESSANDRO DEL MASCHIO From the Departments of Urology and Radiology, Scientific Institute H San Raffade, Milan, Italy
ABSTRACT
Purpose: We evaluated the usefulness of dynamic enhanced magnetic resonance imaging (MRI) in the staging of superficial tumors following a bolus administration of gadopentetate dimeglumine. Materials and Methods: In 48 patients with proved bladder tumors the results of preoperative plain spin echo T1 (repetition timelecho time 500120 msec.) and T2 (repetition timelecho time 2,000/40 to 100 msec.)-weighted MRI, dynamic gadolinium-enhanced MRI (repetition timelecho time 200/15 msec.) and late gadolinium-enhanced MRI (repetition timelecho time 500/20 msec.) were compared and correlated with the histopathological findings. Results: Unenhanced spin echo T1 and T2-weighted MRI sequences were able to stage correctly 14 (56%) and 17 (68%)of 25 superficial bladder cancers, respectively. Muscular infiltration (stages pT2 and pT3a) was correctly depicted in 3 (27%)and 6 (54%)of 11cases respectively, with over staging being the most frequent error. On the basis of the dynamic gadolinium-enhanced T1-weighted MRI appearance, superficial involvement of the bladder wall was correctly assessed in 21 of 25 cases (84%) and muscular infiltration (stages pT2 to pT3a) in 7 of 11 (63%).Delayed enhanced T1-weighted sequences showed a low accuracy rate in staging superficial tumors (44%). The overall accuracy of T1 and T2-weighted, dynamic T1-weighted and delayed T1-weighted MRI in staging bladder cancer was 58, 71, 81 and 56%, respectively. Conclusions: The use of gadolinium improved the accuracy of dynamic enhanced MFtI in staging superficial bladder cancer. On the contrary, delayed enhanced MRI was not useful for staging superficial bladder cancer. The degree of bladder distension was a determinant factor in staging superficial tumors. KEY WORDS: bladder neoplasms, magnetic resonance imaging, gadolinium, neoplasm staging
The ability of computerized tomography (CT) to stage bladder cancer and particularly to distinguish superficial from invasive disease has proved to be relatively limited. The accuracy of staging tumors using CT ranges from 33 to 96%.13 When using CT 67% of superficial tumors are incorrectly staged, while pathological invasive tumors present a staging error ranging from 30% under staging to 20% over The primary function of CT is to distinguish tumors confined to the bladder from those with extravesical extension.' CT is unable to differentiate superficial bladder cancer from infiltrating muscular wall tumors due to the fact that the density of bladder neoplasms is similar to that of the normal bladder. Compared to CT, magnetic resonance imaging (MRI), with its multiplanar capability and excellent tissue contrast, presents some advantages in staging bladder tumors. Tumors of the bladder base or dome, which cannot be readily appreciated in the transaxial plane, may be staged more easily with MRI in the sagittal or coronal plane. Moreover, the signal intensity of tumors on MRI differs from that of the normal bladder wall, thus allowing for differentiation between the 2 types.6-9 The high tissue contrast on MRI provides better demonstration of perivesical fat planes, prostate and seminal vesicles, thus allowing assessment of infiltration of the tumor beyond the bladder wall. Despite these unique features, due to chemical shift artifacts and motion induced phase artifacts, MRI appears to have only 1 slight advantage over CT in terms of sensitivity Accepted for publication October 27, 1995.
and specificity.' In some studies the recent use of gadopentetate dimeglumine (gadolinium) in bladder tumor staging has shown improved sensitivity in detecting intramural tumor growth,10,11although other studies have reported contrasting results.12.13 We evaluated the accuracy of dynamic enhanced MRI in the staging of superficial and advanced bladder tumors following a bolus administration of gadolinium. MATERIALS AND METHODS
From July 1993 to December 1994,36 men and 12 women 37 to 85 years old (average age 62.3 years) with histologically proved bladder neoplasms were included in this prospective study. Patients with a history of bladder tumors treated with transurethral resection, adjuvant intravesical chemotherapy andor neoadjuvant systemic chemotherapy or radiotherapy were excluded. To avoid artifacts and edema of the bladder wall, all patients underwent diagnostic cystoscopy and cold cup biopsy at least 2 weeks before MRI. Within 3 weeks after MRI all patients underwent transurethral resection or cystectomy. Preoperative CT was available in 41 patients. MRI technique. MRI was performed with a 0.5 Tesla superconductive magnet system. To keep the bladder moderately distended during the study all patients were prohibited from urinating until 2 hours before examination. At first, conventional spin echo T1-weighted sequences (repetition timelecho time 500/20 msec.) and spin echo T2-weighted (repetition time/echo time 2,000/40 to 100 msec.) sequences were acquired. The field of view ranged from 30 to 35 cm. and
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DYNAMIC ENHANCED MAGNETIC RESONANCE IMAGING IN BLADDER CANCER STAGING
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matrix size was 256 X 256 and 256 X 192 for spin echo T1 after transurethral resection in 25 patients and radical cysand "2-weighted sequences, respectively. Imaging planes kctomy in 23. Tumors were classified according to the TNM perpendicular to the tumor base were acquired according to system.14 Patients with suspected superficial bladder tumors ~~stoscopy, CT (if available) and plain MRI sequences. After routinely underwent transurethral resection of the tumor conventional spin echo MRI sequences short spin echo T1- and the muscular layer in each case following biopsies of the weighted images (repetition timdecho time 200/15 msec.) base of the reeected area. Superficial tumors were considered were acquired. Three sections were obtained during 1study on the basis of tumor absence in the r e d muecular tissue with a 20-second breath hold, a section thickness of 7.5 mm. after transurethral resection. and an intersection gap of 1.5 mm. Dynamic MRI consisted of short (repetition timdecho time RESULTS 200/15 msec.) spin echo T1-weighted sequencesbefore and 20 seconds after an intravenous bolus injection of 0.1 mmolflrg. Of the 48 tumors evaluated the presence of cancer was gadolinium-pentetic acid (DTPA), which took less than 10 correctly identified in all cases by MFU. Tumor size ranged seconds using an 18 gauge catheter positioned in an antecu- from 0.7 to 8.6 cm.(mean 1.8).The bladder cancer was at the bital vein. Images were repeated 4 times at the same section base and trigone in 17 of 48 cases (35%), at the lateral after 20,50,80 and 110 seconds. Total imaging time for the bladder wall in 19 (39%), at the posterior wall in 8 (16%)and dynamic study was less than 2 minutes. Matrix size was at the dome in 4 (8%). The final stage of disease confirmed histologically was T1 in 25 patients (52%)after transurethral 128 X 128. Delayed spin echo T1-weighted (repetition timdecho time resection, and pT2 in 2 (4%), pT3a in 9 (19%), pT3b in 11 500/20 msec.) images were also obtained when the bladder (23%) and pT4a in 1 (2%) after cyetectomy. In no case was was filled with contrast medium. Two studies were used for transitional cell carcinoma in situ found in the pathological spin echo T1 and spin echo T2-weighted sequences, and im- specimen. On T1-weighted images the signal intensity of the bladder aging times were 4.3 minutes and 11.4 minutes, respectively. tumor was slightly hypointense and similar to that of the No motion artifact reduction techniques were used. Diagnostic criteria MRI images were prospectively inter- bladder wall, which contrasted with the hyper-intensity of preted by 2 radiologists (A. V. and F. DC.) and reviewed for the perivesical fat. On T2-weighted images the bladder canconsensus by 1urologist (V. S.)without any knowledge of the cer showed a higher signal intensity than the normal bladder pathological findings obtained after surgery. The actual CT wall but a lower intensity than that of the urine or perivesical reports were not available to the reviewers, and no direct fat. The correlation between MRI and postoperative staging is comparison between CT and MRI examinations was made in detailed in table 1. The comparison of plain spin echo T1this study. Clinical stage of the bladder tumor on plain and enhanced weighted MRI and histopathological findings demonstrated MRI was determined according to the TNM classification of that the overall staging accuracy was 58% (28 of 48 cases), bladder cancer (see Appendix).14 Our staging criteria were over staging ocmrred in 38% (18 of 48) and under staging similar to those reported previously.13 Spin echo T2-weighted occurred in 4% (2 of 48, table 2). While spin echo T1-weighted sequences were useful in terms of evaluating the neoplastic MRI correctly staged 909b of bladder tumors with extravesiinfiltration of the bladder wall, which appeared as a low cal fat invasion (stage T3b), muscular infiltration(stagea pT2 signal intensity line, and disruption of the hypointense line and pT3a) was correctly detected in only 3 of 11caaea (27%). was considered as a sign of neoplastic infiltration.8. l6.l* Plain Spin echo plain Tl-we@ted MRI sequences were only able TI-weighted sequences were useful to detect extravesical to demonstrate superficialinfiltration in 14 of 25 cases (56%). tumor involvement, since in case of infiltration the low signal with 11 (44%) being over staged (fig. 1). Plain spin echo intensity of the tumor replaced the normal high signal inten- T2-weighted MRI accurately staged 17 of 25 supeficial bladsity of the perivesical fat.17-20 Spin echo T2-weighted images der cancers (68%)and in 6 of 11 cases (54%) it correctly were also used to detect seminal vesicle invasion due to the depicted muscular infiltration by the tumor. Disruption of fact that they showed the highest contrast between the hy- the low m p a l line of the muBcul8f bladder wall was not pointensity of bladder cancer and the hyper-intensity of the evident in only 1case (9%) due to chemical shift artifacts, normal seminal vesicle.15 On dynamic spin echo T1-weighted while over staging din 4 (36%). T2-weighted MRI with MRI tumor, mucosa and submucosa showed an earlier en- staging proved to be correct in 10 of 11patients (90%) hancement than the muscular bladder wall, which remained tumor spread beyond the bladder wall. The overall accurflcy hypointense immediately after injection of gadolinium-DTPA rate for staging was 71% (34of 48 cases),while over stagmg (within the first 2 minutes).21.22 On the contrary, the bladder din 25% (12 of 48) and under staging occurred in 4% tumor and muscular bladder wall showed the same signal (2 of 48). On the basis of the dynamic gadoliniumenhanced T1intensity aRer contrast enhancement with no possibility of differentiation between the neoplastic lesion and muscular weighted MRI appearance, superficial involvement of the wal1.21 The gold standard of the study was postoperative bladder wall was correctly staged in 21 cases (84%. &. 1). (transurethral resection of bladder tumors or cystectomy) Muscular infiltration was accurately aeeeseed in 7 of 11cases (6396,fig. 2) and extravesical spread was noted in 90%.Durhistological evaluation (48 of 48 cases). Pathological staging. Histological stage was determined ing the early phase of contrast enhanced T1-weighted MRI
TABLE1. LXagnostic accumcy ofplain and gaddinium-enhanced MRI in 48patient8 with bladder colz~er No. Pb.(%I
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DYNAMIC ENHANCED MAGNETIC RESONANCE IMAGING IN BLADDER CANCER STAGING
ntensity line indicates deep muscular invasion, while the xesence of a regular and sharp hypointense line implies a wperficial bladder cancer.8 On T1-weighted sequences MRI :an correctly demonstrate extravesical tumor spread because Staging Dynamic Late it provides high tissue contrast between the hypointensity of Accuracy T1-Weighted "%Weighted Gadolinium- Gadoliniumthe lesion and hyper-intensity of the pelvic fat.23 Moreover, MRI MRI Enhanced Enhanced with its multiplanar display capabilities, particularly sagitMRI MRI 1tal and coronal imaging, and its excellent tissue contrast, 39 (81) 27 (56) 34 (71) Correct 28 (58) MRI can detect and stage tumors of the bladder base or dome Under stagmg 2 (4) 2 (4) 1 (2) 1 (2) that cannot be readily appreciated in the transaxial plane 8(17) 20 (42) 18 (38) 12 (25) Over staging 44 (92) 34 (71) 39 (81) 36 (75) Ta-T1 versus T2-T4 more accurately than CT. Studies in the literature show that MRI has a staging accuracy rate of 72 to 96%,s,15-17.19."3 which is slightly better than CT.17.24 Despite these potential advantages of MRI over CT, the tumor enhancement was early and high in all cases, and reduced spatial resolution and signal-to-noise ratio on T2signal intensity was similar to that of the perivesical fat. weighted sequences, as well as chemical shift artifacts, image Bladder lesions showed the highest contrast compared to the degradation caused by breathing artifacts, suboptimal lesion surrounding structure (bladder wall, bladder lumen, prostate conspicuity, cost-effectiveness and availability have limited and seminal vesicles), which remained hypointense during the overall use of MRI. There is the common impression that the first minutes following injection of gadolinium. On dy- plain MRI suffers the same limitations as CT in staging namic MRI 39 of 48 cases (81%) were correctly staged, 8 small and superficial tumors (less than 1cm.), and that the 2 (17%)were over staged and 1 (2%) was under staged. techniques are comparable and accurate with regard to the Delayed T1-weighted sequences showed a low accuracy evaluation of perivesical tumor extension. lo,12-13. 17 rate in the staging of superficial (44%) and locally advanced Subsequent studies on the use of contrast material (gado(69%)bladder cancer due to the fact that the contrast me- linium-DTPA) demonstrated that assessment of intramural dium and consequent enhancement decreased the contrast neoplastic infiltration was possible following administration among the bladder lesion, bladder wall and perivesical fat. of gadolinium,l1,25,26although other studies have reported Most of the useful details acquired by dynamic sequences opposite results.12.13 On pre-contrast spin echo T1-weighted were not obtained. The hypointense line of the muscular sequences small bladder tumors are hypointense and isoinbladder wall was not evident in 8 cases with proved supefi- tense in relation to the bladder wall and, if not prominent, cia1 bladder cancer. On the contrary, dynamic MRI was able they are difficult to stage correctly. As a rule, following adto show the %lack line" in 22 of 25 patients (88%). Muscular ministration of gadolinium the tumor is immediately eninfiltration was correctly depicted by late gadolinium en- hanced and shows the highest signal intensity during the hanced MRI in only 5 of 11cases (45%). On delayed MRI 27 early phase (during the first 2 minutes). It also contrasts of 48 tumors (56%) were correctly staged, 20 (42%) were over sharply with the low bladder lumen signal as well as with the staged and 1 (2%)was under staged. When the stages were normal bladder wall, which shows a later gradual signal grouped as Ta to T1 versus T2 to T4, staging accuracy im- intensity increase during the post-contrast sequences. proved. T1-weighted MRI accurately staged 36 of the 48 Our overall accuracy rate in staging bladder cancer on tumors (75%),T2-weighted MRI 39 of 48 (81%), dynamic MRI dynamic gadolinium-enhanced MRI was 81%, that is higher 44 of 48 (92%)and late enhanced MFtI 34 of 48 (71%, table 2). than the 71% obtained with spin echo T2-weighted MRI and higher than the 56% obtained with the post-contrast seDISCUSSION quences. More importantly, the overall staging accuracy of Since detection of a bladder tumor is easily assessed by stage Ta to T1 as a group versus T2 or greater on dynamic cystoscopic biopsy, staging bladder cancer is the main clinical MRI was 92%. Recently, similar results have been reported problem. Today accurate staging is becoming imperative in with a staging accuracy of 83, 78 and 61% for dynamic, new therapeutic strategies, such as in conservative surgery delayed and conventional MRI, respectively."' Even if most of the investigators agree that tumor enwhereby selecting patients by tumor stage is of great clinical significance. The same applies to the neoadjuvant systemic hancement is higher than that of the bladder muschemotherapy for which accurate staging of bladder cancer cle,l1.21922,27 differentiation of the tumor from the bladder wall on post-contrast MRI is not always possible.l"i3 In our remains critical. Until now CT has been considered the primary imaging study the maximum difference in intensity between the tumodality and the most widely used technique to stage blad- mor and bladder wall was only achieved during the early der cancer. However, CT staging accuracy rates have vaned phase of the bolus injection, while on the delayed images the widely from 33 to 96%, partly due to the inclusion of patients intensity contrast of the lesion versus bladder wall became with superficial bladder In fact, while CT has been less evident. Dynamic MRI provided more detailed informashown to be a n effective method of depicting tumors that tion concerning differentiation between superficial and mushave spread beyond the bladder wall, CT is unable to assess cle-invasive bladder tumor than late gadolinium-enhanced whether a lesion with focal or diffuse thickening of the blad- MRI. Moreover, dynamic MRI was able to show the low der wall is an infiltrating or superficial tumor.2 Since the signal intensity muscle layer, and the differential enhancebladder tumor density on CT is similar to that of the nor- ment of the mucosal lining and bladder wall more often than mal bladder wall, the major and most well recognized limi- late gadolinium-enhanced MRI. Thus, the use of gadolinium tation of CT is its inability to depict correctly the intramural only improved the accuracy of dynamic enhanced MRI in neoplastic extent. In a recent report 67% of superficial blad- staging superficial bladder cancer. On the contrary, late gader tumors had been incorrectly staged with CT.* dolinium-enhanced MRI was not useful in staging superficial Due to the fact that MRI has some potential advantages bladder cancer due to the less evident signal intensity differover CT, MRI has a n increasingly important role in staging ence between the lesion and bladder wall. Today gadolinium bladder cancer. On T2-weighted sequences MRI can often enhanced MRI is not able to differentiate stage Ta from T1 differentiate superficial tumors from those invading deep bladder tumors and it is unable to detect the presence of muscle because the signal intensity of the bladder lesion is carcinoma in situ, since it is too small for current resolution. higher than that of the normal or hypertrophied wall, which More powerful magnets, further improvements in scanning A disruption of the low techniques, phased array coils and new contrast materials appears as a hypointense TABLE2. Staging accuracy of plain spin echo TI and T2-weighted, dvnamic ,?adolinium-enhanced and delayed MRl in 48 patients No.Pts.(%)
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FIG. 1. Stage T1 transitional cell carcinoma of bladder. A, axial plain spin echo T1-weighted sequence (repetition timdecho delay time 500/20 msec.) shows low intensity lesion arising from left lateral wall of bladder. Note that signal is similar to one from bladder wall, which appears as irregular and disrupted line in region of tumor. B,axial plain spin echo T2-weighted se uence (repetition timdecho delay time 2,000/40 msec.) reveals high signal tumor disrupting low signal intensity muscle layer of bladder wJ1 and suggesting that it has infiltrated bladder wall. C, transverse dynamic gadolinium-enhanced MRI (re etition timdecho delay time 200/15 msec.) 30 seconds after contrast material injection demonstrates differential enhancement between gladder tumor and muscle layer, which appears as uninterru ted low intensity line. Su erficial infiltration from bladder tumor was correctly assessed. D, on delayed sequence (repetition timdecho defay time 500120 msec.) different enhancement between lesion and bladder wall is not visible. Dynamic MRI provides more detailed information concerning differentiation between superficial and muscle-invasive bladder tumor than late gadoliniumenhanced MRI.
FIG.2. Stage pT3a bladder tumor. Axial plain spin echo T1-weighted MRI sequence (repetition timdecho delay time 500/20 msec.) shows low signal intensity bladder tumor that is indistinguishable from signal intensit of bladder wall. A, assessment of depth of tumor infiltration is critical on plain s in echo T1-weighted MRI. €3, on dynamic MRI enhanced gladder tumor contrasts with hypointense muscle layer and correct depth of infifkation can be assessed.
might probably provide better results. In any case, in our opinion diagnostic techniques that are able to differentiate stage T1 from T2 tumors are of greater value than those that differentiate stage Ta from T1 cancer because a more aggressive and more radical treatment is necessary only in the presence of a bladder lesion that infiltrates the muscular layer of the bladder wall. The degree of bladder distension was a determinant factor in staging superficial tumors. With an over distended bladder, the thickness of the bladder wall became too thin to distinguish superficial invasion from deep muscular invasion. On the contrary, when the bladder was not distended in some cases the collapsed bladder mucosa mimicked tumor infiltration. Our patients were asked to present for examination with a moderately distended bladder and to drink 2 or more glasses of water when this was not considered full enough. Except for these considerations, over staging remained the most frequent error due to the presence of an
inflammatory reaction around the tumor, which with current diagnostic techniques cannot be distinguished from a tumor. Gadolinium enhancement in the dynamic and late enhanced MRI was also useful in staging bladder tumor with invasion of the seminal vesicles and prostate. Tumor enhancement allowed us to distinguish between the hypointense seminal vesicles and hyper-intense neoplastic tissue. On the contrary, staging bladder tumors with perivesical infiltration (stage pT3b) by dynamic and delayed enhanced MRI was not accurate due to the gadolinium enhancement of the bladder tumor, which decreased the signal intensity contrast between pelvic fat and tumor. Another diagnostic technique that has provided highly accurate results in the assessment of early lesions is transvesical u l t r a s o ~ n dAlthough . ~ ~ ~ ~Schuller ~ ~ ~ ~et al reported a 92% staging accuracy rate28 and Pavone et a1 concluded that transurethral ultrasonography was superior to CT and plain MRI,30 others did not confirm these good results.11 Cumula-
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DYNAMIC ENHANCED MAGNETIC RESONANCE IMAGING IN BLADDER CANCER STAGING
tive results of studies on accuracy of transurethral ultrasonography showed an over staging error of 24% for stage T1 disease or less and an under staging error of 10%for stage T2 cancer or greater.' This method allows the bladder m u w a to be separately visualized f h m the muscular layer, thus, enabling early superficial tumors to be Werentiated from those with deeper invasion of the bladder wall. Unfortunately, transurethral ultrasonography is less accurate in staging locally advanced bladder cancer because the tumor extends beyond the penetration depth of the ultrasound beam.= Its major disadvantage and limitation are the need to perform the examination with the patient under general, spinal or epidural anesthesia. Furthermore, the equipment for transurethral sonography,which requires a special transducer, is not widely available. Presently, this technique is not considered the method of choice for staging superficial bladder cancer. Most authors agree that conventional clinical techniques, such as excretory urography, cyt~logy,b i m a n d examination, cystoscopy and biopsy, are a m a t e in staging superficial tumors while they are less accurate in cases of locally advanced disease.31 These techniques are considered to be capable of staging correctly superficial tumor (carcinoma in situ to T1) in 50 to 80% of cases.20 More importantly,cumulative results of studies on the accuracy of clinical staging
before the era of cross-sectional imaging showed that the overall sensitivity for pathologicalstage T2 or greater disease was 95%.1 Nevertheless, the overall staging accuracy rate was low at 354Rb.l The majority of these studies, similarly to ours, have used a combination of cystectomy and transurethral resection of the tumor for pathological staging. From these considerations, dynamic enhanced MRI seems equally effective to conventional clinical staging in differentiating superficial disease as a group from muscle-invasive disease but with a higher overall staging accuracy. A large prospective blinded study comparing dynamic enhanced MRI, CT, transurethral ultrasonography and conventional techniques is needed to define the ultimate applicability of gadoliniumenhanced MRI in staging superficial bladder cancer. CONCLUSIONS
Dynamic MRI has provided more detailed information on differentiationbetween superficial and muscle-invasivebladder tumor than late gadolinium-enhancedMRI. Even if dynamic MRI were superior to =-weighted sequences in demonstrating the presence of the unbroken hypointense line of the muscular wall, over staging remained the most frequent error in superficial bladder cancer.
APPENDIX: CRITERIA ESTABLISHED TO ASSESS CLINICAL STAGE OF BLADDER CANCER ON PLAIN SPIN ECHO T1-WEIGHTED AND T2-WEIGHTED MRI, AND GADOLINIUM-ENHANCED MRI
TNM stage
Ta-T1
T2 T3a
T3b
T4a
Plain T1-Weighted MRI N e ~ ~ l a ~lesion t i c with normal &ter bladder wall seen as low intensity band Same findings as for stage T1 Bladder tumor with thickening of adjacent bladder wall, interface between bladder wall and perivesical fat regular Hypointense bladder lesion with irregular interface showing hyper-intense perivesical fat Strands of soft tissue contiguous with the primary tumor in extravesical organ
REFERENCES
Plain T2-Weighted MRI
Dynamic Gadolinium-Enhanced MRI
Enhanced tumor and adjacent mucosa with unbroken hypointense muscular layer Wall Irregularity of hypointense muscular Bladder tumor with focally diswall due to presence of enhanced rupted low intensity band of bladder Ca bladder wall Interruption of hypointense line of Bladder tumor with completely muscular layer showing regular disrupted low intensity band of interface between enhanced lesion bladder wall and perivesical fat Lesion showing abnormal intenEnhanced bladder Ca extending into sity in perivesical fat with comhyper-intense perivesical fat pletely disrupted low intensity band of bladder wall Hypointense large bladder tumor Interrupted perivesical fat-bladder that replaces hyper-intense wall plane with evidence of enseminal vesicle, or infiltrates hanced tumor in adjacent organs, prostate or uterus (sagittal and which display with abnormal archicoronal scans) tecture
NGplasticTesion &owing unbroken hypointense line of bladder
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22. Narumi, Y.,Kadota, T., Inoue, E., Kuriyama, K., Fujita, M., Hosomi, N., Sawai, Y.,Kuroda, M.,Kotake, T. and Kuroda, C.: Bladder tumora: staging with gadoliniumedmnced oblique M R imaging. Radiology, 181: 145, 1993. 23. Bryan, P. J., Butler, H. E., LiPuma, J. P.,Resniclr, M. I. and Kursh, E. D.: CT and MR imaging in staging bladder neoplasms. J. Comput. Assist. Tomogr.. 11: 96,1987. 24. Lee,J. K T.and Rholl, K S.: MRI of the bladder and prostate. AJR, 141: 732,1986. 25. Barentsz, J. O., Ruijs, S. H. and Strijk, S. P.: The role of M R imaai~ in carcinoma of the urinary bladder. AJR, 160: 937, 1993. 26. Hawnaur, J. M.,Johnson, R. J., Read, C. and Isherwood, I.: Magnetic resonance imaging with gadolinium-DTPA for aseeasment of bladder carcinoma and its reeponse to treatment. Clin. Rad., 41:302,1993. 27. Kim, B.,S e m e h , R. C., Ascher, S. M.. Chalpin, D. B., Carroll, P. R. and Hricak, H.:Bladder tumor.-s comparison of contrastenhanced CT,T1- and T2-weighted M R imaging, dynamic gadolinium-enhanced imaging, and late gadoliniumenhanced imaging. Radiology, IS% 239,1994. 28. Schiiller, J., Walther, V., Schmiedt, E., Staehler, G., Bauer, H.W. and Schilling,A: Intravesical ultrasound tomography in staging bladder carcinoma.J. Urol., 128:264, 1982. 29. Resnik, M. I. and Kursh. E. D.:Transurethral ultrasonography in bladder cancer. J. Urol., 1% 263, 1986. 30. Pavone, C., Di Trapani, D.,Serretta, V., Filoato, L.. Cacciatore, M., Caramin, G. and Pavone-Macalm. M.: Transurethral ultraeonography, CT scan, nuclear magnetic resonance (NMR) imaging and pathological control in staging and follow up of invasive bladder carcinoma. Prop. Clin. Biol. Res., 260: 251, 1988. 31. Cumyings, K. B., Barone, J. G. and Ward, W.S.:Diagnosis and stagmg of bladder cancer. Urol. Clin. N. Amer., 19: 465,1992.
Vol. 155. 1594-1599, May 1996 Printed in U.S.A.
"KE JOUBNAL OF uR0uX;U Copyright 8 1996 by AMEIUCAN UROLOCICAL AS~OCUTION,h c .
DYNAMIC GADOLINIUM-ENHANCED MAGNETIC RESONANCE IMAGING IN STAGING OF SUPERFICIAL BLADDER CANCER VINCENZO SCATTONI, LUIGI F. DA POZZO, RENZO COLOMBO, LUCIAN0 NAVA, PATRIZIO RIGATTI, FRANCESCO DE COBELLI, ANGEL0 VANZULLI AND ALESSANDRO DEL MASCHIO From the Departments of Urology and Radiology, Scientific Institute H San Raffade, Milan, Italy
ABSTRACT
Purpose: We evaluated the usefulness of dynamic enhanced magnetic resonance imaging (MRI) in the staging of superficial tumors following a bolus administration of gadopentetate dimeglumine. Materials and Methods: In 48 patients with proved bladder tumors the results of preoperative plain spin echo T1 (repetition timelecho time 500120 msec.) and T2 (repetition timelecho time 2,000/40 to 100 msec.)-weighted MRI, dynamic gadolinium-enhanced MRI (repetition timelecho time 200/15 msec.) and late gadolinium-enhanced MRI (repetition timelecho time 500/20 msec.) were compared and correlated with the histopathological findings. Results: Unenhanced spin echo T1 and T2-weighted MRI sequences were able to stage correctly 14 (56%) and 17 (68%)of 25 superficial bladder cancers, respectively. Muscular infiltration (stages pT2 and pT3a) was correctly depicted in 3 (27%)and 6 (54%)of 11cases respectively, with over staging being the most frequent error. On the basis of the dynamic gadolinium-enhanced T1-weighted MRI appearance, superficial involvement of the bladder wall was correctly assessed in 21 of 25 cases (84%) and muscular infiltration (stages pT2 to pT3a) in 7 of 11 (63%).Delayed enhanced T1-weighted sequences showed a low accuracy rate in staging superficial tumors (44%). The overall accuracy of T1 and T2-weighted, dynamic T1-weighted and delayed T1-weighted MRI in staging bladder cancer was 58, 71, 81 and 56%, respectively. Conclusions: The use of gadolinium improved the accuracy of dynamic enhanced MFtI in staging superficial bladder cancer. On the contrary, delayed enhanced MRI was not useful for staging superficial bladder cancer. The degree of bladder distension was a determinant factor in staging superficial tumors. KEY WORDS: bladder neoplasms, magnetic resonance imaging, gadolinium, neoplasm staging
The ability of computerized tomography (CT) to stage bladder cancer and particularly to distinguish superficial from invasive disease has proved to be relatively limited. The accuracy of staging tumors using CT ranges from 33 to 96%.13 When using CT 67% of superficial tumors are incorrectly staged, while pathological invasive tumors present a staging error ranging from 30% under staging to 20% over The primary function of CT is to distinguish tumors confined to the bladder from those with extravesical extension.' CT is unable to differentiate superficial bladder cancer from infiltrating muscular wall tumors due to the fact that the density of bladder neoplasms is similar to that of the normal bladder. Compared to CT, magnetic resonance imaging (MRI), with its multiplanar capability and excellent tissue contrast, presents some advantages in staging bladder tumors. Tumors of the bladder base or dome, which cannot be readily appreciated in the transaxial plane, may be staged more easily with MRI in the sagittal or coronal plane. Moreover, the signal intensity of tumors on MRI differs from that of the normal bladder wall, thus allowing for differentiation between the 2 types.6-9 The high tissue contrast on MRI provides better demonstration of perivesical fat planes, prostate and seminal vesicles, thus allowing assessment of infiltration of the tumor beyond the bladder wall. Despite these unique features, due to chemical shift artifacts and motion induced phase artifacts, MRI appears to have only 1 slight advantage over CT in terms of sensitivity Accepted for publication October 27, 1995.
and specificity.' In some studies the recent use of gadopentetate dimeglumine (gadolinium) in bladder tumor staging has shown improved sensitivity in detecting intramural tumor growth,10,11although other studies have reported contrasting results.12.13 We evaluated the accuracy of dynamic enhanced MRI in the staging of superficial and advanced bladder tumors following a bolus administration of gadolinium. MATERIALS AND METHODS
From July 1993 to December 1994,36 men and 12 women 37 to 85 years old (average age 62.3 years) with histologically proved bladder neoplasms were included in this prospective study. Patients with a history of bladder tumors treated with transurethral resection, adjuvant intravesical chemotherapy andor neoadjuvant systemic chemotherapy or radiotherapy were excluded. To avoid artifacts and edema of the bladder wall, all patients underwent diagnostic cystoscopy and cold cup biopsy at least 2 weeks before MRI. Within 3 weeks after MRI all patients underwent transurethral resection or cystectomy. Preoperative CT was available in 41 patients. MRI technique. MRI was performed with a 0.5 Tesla superconductive magnet system. To keep the bladder moderately distended during the study all patients were prohibited from urinating until 2 hours before examination. At first, conventional spin echo T1-weighted sequences (repetition timelecho time 500/20 msec.) and spin echo T2-weighted (repetition time/echo time 2,000/40 to 100 msec.) sequences were acquired. The field of view ranged from 30 to 35 cm. and
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DYNAMIC ENHANCED MAGNETIC RESONANCE IMAGING IN BLADDER CANCER STAGING
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matrix size was 256 X 256 and 256 X 192 for spin echo T1 after transurethral resection in 25 patients and radical cysand "2-weighted sequences, respectively. Imaging planes kctomy in 23. Tumors were classified according to the TNM perpendicular to the tumor base were acquired according to system.14 Patients with suspected superficial bladder tumors ~~stoscopy, CT (if available) and plain MRI sequences. After routinely underwent transurethral resection of the tumor conventional spin echo MRI sequences short spin echo T1- and the muscular layer in each case following biopsies of the weighted images (repetition timdecho time 200/15 msec.) base of the reeected area. Superficial tumors were considered were acquired. Three sections were obtained during 1study on the basis of tumor absence in the r e d muecular tissue with a 20-second breath hold, a section thickness of 7.5 mm. after transurethral resection. and an intersection gap of 1.5 mm. Dynamic MRI consisted of short (repetition timdecho time RESULTS 200/15 msec.) spin echo T1-weighted sequencesbefore and 20 seconds after an intravenous bolus injection of 0.1 mmolflrg. Of the 48 tumors evaluated the presence of cancer was gadolinium-pentetic acid (DTPA), which took less than 10 correctly identified in all cases by MFU. Tumor size ranged seconds using an 18 gauge catheter positioned in an antecu- from 0.7 to 8.6 cm.(mean 1.8).The bladder cancer was at the bital vein. Images were repeated 4 times at the same section base and trigone in 17 of 48 cases (35%), at the lateral after 20,50,80 and 110 seconds. Total imaging time for the bladder wall in 19 (39%), at the posterior wall in 8 (16%)and dynamic study was less than 2 minutes. Matrix size was at the dome in 4 (8%). The final stage of disease confirmed histologically was T1 in 25 patients (52%)after transurethral 128 X 128. Delayed spin echo T1-weighted (repetition timdecho time resection, and pT2 in 2 (4%), pT3a in 9 (19%), pT3b in 11 500/20 msec.) images were also obtained when the bladder (23%) and pT4a in 1 (2%) after cyetectomy. In no case was was filled with contrast medium. Two studies were used for transitional cell carcinoma in situ found in the pathological spin echo T1 and spin echo T2-weighted sequences, and im- specimen. On T1-weighted images the signal intensity of the bladder aging times were 4.3 minutes and 11.4 minutes, respectively. tumor was slightly hypointense and similar to that of the No motion artifact reduction techniques were used. Diagnostic criteria MRI images were prospectively inter- bladder wall, which contrasted with the hyper-intensity of preted by 2 radiologists (A. V. and F. DC.) and reviewed for the perivesical fat. On T2-weighted images the bladder canconsensus by 1urologist (V. S.)without any knowledge of the cer showed a higher signal intensity than the normal bladder pathological findings obtained after surgery. The actual CT wall but a lower intensity than that of the urine or perivesical reports were not available to the reviewers, and no direct fat. The correlation between MRI and postoperative staging is comparison between CT and MRI examinations was made in detailed in table 1. The comparison of plain spin echo T1this study. Clinical stage of the bladder tumor on plain and enhanced weighted MRI and histopathological findings demonstrated MRI was determined according to the TNM classification of that the overall staging accuracy was 58% (28 of 48 cases), bladder cancer (see Appendix).14 Our staging criteria were over staging ocmrred in 38% (18 of 48) and under staging similar to those reported previously.13 Spin echo T2-weighted occurred in 4% (2 of 48, table 2). While spin echo T1-weighted sequences were useful in terms of evaluating the neoplastic MRI correctly staged 909b of bladder tumors with extravesiinfiltration of the bladder wall, which appeared as a low cal fat invasion (stage T3b), muscular infiltration(stagea pT2 signal intensity line, and disruption of the hypointense line and pT3a) was correctly detected in only 3 of 11caaea (27%). was considered as a sign of neoplastic infiltration.8. l6.l* Plain Spin echo plain Tl-we@ted MRI sequences were only able TI-weighted sequences were useful to detect extravesical to demonstrate superficialinfiltration in 14 of 25 cases (56%). tumor involvement, since in case of infiltration the low signal with 11 (44%) being over staged (fig. 1). Plain spin echo intensity of the tumor replaced the normal high signal inten- T2-weighted MRI accurately staged 17 of 25 supeficial bladsity of the perivesical fat.17-20 Spin echo T2-weighted images der cancers (68%)and in 6 of 11 cases (54%) it correctly were also used to detect seminal vesicle invasion due to the depicted muscular infiltration by the tumor. Disruption of fact that they showed the highest contrast between the hy- the low m p a l line of the muBcul8f bladder wall was not pointensity of bladder cancer and the hyper-intensity of the evident in only 1case (9%) due to chemical shift artifacts, normal seminal vesicle.15 On dynamic spin echo T1-weighted while over staging din 4 (36%). T2-weighted MRI with MRI tumor, mucosa and submucosa showed an earlier en- staging proved to be correct in 10 of 11patients (90%) hancement than the muscular bladder wall, which remained tumor spread beyond the bladder wall. The overall accurflcy hypointense immediately after injection of gadolinium-DTPA rate for staging was 71% (34of 48 cases),while over stagmg (within the first 2 minutes).21.22 On the contrary, the bladder din 25% (12 of 48) and under staging occurred in 4% tumor and muscular bladder wall showed the same signal (2 of 48). On the basis of the dynamic gadoliniumenhanced T1intensity aRer contrast enhancement with no possibility of differentiation between the neoplastic lesion and muscular weighted MRI appearance, superficial involvement of the wal1.21 The gold standard of the study was postoperative bladder wall was correctly staged in 21 cases (84%. &. 1). (transurethral resection of bladder tumors or cystectomy) Muscular infiltration was accurately aeeeseed in 7 of 11cases (6396,fig. 2) and extravesical spread was noted in 90%.Durhistological evaluation (48 of 48 cases). Pathological staging. Histological stage was determined ing the early phase of contrast enhanced T1-weighted MRI
TABLE1. LXagnostic accumcy ofplain and gaddinium-enhanced MRI in 48patient8 with bladder colz~er No. Pb.(%I
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DYNAMIC ENHANCED MAGNETIC RESONANCE IMAGING IN BLADDER CANCER STAGING
ntensity line indicates deep muscular invasion, while the xesence of a regular and sharp hypointense line implies a wperficial bladder cancer.8 On T1-weighted sequences MRI :an correctly demonstrate extravesical tumor spread because Staging Dynamic Late it provides high tissue contrast between the hypointensity of Accuracy T1-Weighted "%Weighted Gadolinium- Gadoliniumthe lesion and hyper-intensity of the pelvic fat.23 Moreover, MRI MRI Enhanced Enhanced with its multiplanar display capabilities, particularly sagitMRI MRI 1tal and coronal imaging, and its excellent tissue contrast, 39 (81) 27 (56) 34 (71) Correct 28 (58) MRI can detect and stage tumors of the bladder base or dome Under stagmg 2 (4) 2 (4) 1 (2) 1 (2) that cannot be readily appreciated in the transaxial plane 8(17) 20 (42) 18 (38) 12 (25) Over staging 44 (92) 34 (71) 39 (81) 36 (75) Ta-T1 versus T2-T4 more accurately than CT. Studies in the literature show that MRI has a staging accuracy rate of 72 to 96%,s,15-17.19."3 which is slightly better than CT.17.24 Despite these potential advantages of MRI over CT, the tumor enhancement was early and high in all cases, and reduced spatial resolution and signal-to-noise ratio on T2signal intensity was similar to that of the perivesical fat. weighted sequences, as well as chemical shift artifacts, image Bladder lesions showed the highest contrast compared to the degradation caused by breathing artifacts, suboptimal lesion surrounding structure (bladder wall, bladder lumen, prostate conspicuity, cost-effectiveness and availability have limited and seminal vesicles), which remained hypointense during the overall use of MRI. There is the common impression that the first minutes following injection of gadolinium. On dy- plain MRI suffers the same limitations as CT in staging namic MRI 39 of 48 cases (81%) were correctly staged, 8 small and superficial tumors (less than 1cm.), and that the 2 (17%)were over staged and 1 (2%) was under staged. techniques are comparable and accurate with regard to the Delayed T1-weighted sequences showed a low accuracy evaluation of perivesical tumor extension. lo,12-13. 17 rate in the staging of superficial (44%) and locally advanced Subsequent studies on the use of contrast material (gado(69%)bladder cancer due to the fact that the contrast me- linium-DTPA) demonstrated that assessment of intramural dium and consequent enhancement decreased the contrast neoplastic infiltration was possible following administration among the bladder lesion, bladder wall and perivesical fat. of gadolinium,l1,25,26although other studies have reported Most of the useful details acquired by dynamic sequences opposite results.12.13 On pre-contrast spin echo T1-weighted were not obtained. The hypointense line of the muscular sequences small bladder tumors are hypointense and isoinbladder wall was not evident in 8 cases with proved supefi- tense in relation to the bladder wall and, if not prominent, cia1 bladder cancer. On the contrary, dynamic MRI was able they are difficult to stage correctly. As a rule, following adto show the %lack line" in 22 of 25 patients (88%). Muscular ministration of gadolinium the tumor is immediately eninfiltration was correctly depicted by late gadolinium en- hanced and shows the highest signal intensity during the hanced MRI in only 5 of 11cases (45%). On delayed MRI 27 early phase (during the first 2 minutes). It also contrasts of 48 tumors (56%) were correctly staged, 20 (42%) were over sharply with the low bladder lumen signal as well as with the staged and 1 (2%)was under staged. When the stages were normal bladder wall, which shows a later gradual signal grouped as Ta to T1 versus T2 to T4, staging accuracy im- intensity increase during the post-contrast sequences. proved. T1-weighted MRI accurately staged 36 of the 48 Our overall accuracy rate in staging bladder cancer on tumors (75%),T2-weighted MRI 39 of 48 (81%), dynamic MRI dynamic gadolinium-enhanced MRI was 81%, that is higher 44 of 48 (92%)and late enhanced MFtI 34 of 48 (71%, table 2). than the 71% obtained with spin echo T2-weighted MRI and higher than the 56% obtained with the post-contrast seDISCUSSION quences. More importantly, the overall staging accuracy of Since detection of a bladder tumor is easily assessed by stage Ta to T1 as a group versus T2 or greater on dynamic cystoscopic biopsy, staging bladder cancer is the main clinical MRI was 92%. Recently, similar results have been reported problem. Today accurate staging is becoming imperative in with a staging accuracy of 83, 78 and 61% for dynamic, new therapeutic strategies, such as in conservative surgery delayed and conventional MRI, respectively."' Even if most of the investigators agree that tumor enwhereby selecting patients by tumor stage is of great clinical significance. The same applies to the neoadjuvant systemic hancement is higher than that of the bladder muschemotherapy for which accurate staging of bladder cancer cle,l1.21922,27 differentiation of the tumor from the bladder wall on post-contrast MRI is not always possible.l"i3 In our remains critical. Until now CT has been considered the primary imaging study the maximum difference in intensity between the tumodality and the most widely used technique to stage blad- mor and bladder wall was only achieved during the early der cancer. However, CT staging accuracy rates have vaned phase of the bolus injection, while on the delayed images the widely from 33 to 96%, partly due to the inclusion of patients intensity contrast of the lesion versus bladder wall became with superficial bladder In fact, while CT has been less evident. Dynamic MRI provided more detailed informashown to be a n effective method of depicting tumors that tion concerning differentiation between superficial and mushave spread beyond the bladder wall, CT is unable to assess cle-invasive bladder tumor than late gadolinium-enhanced whether a lesion with focal or diffuse thickening of the blad- MRI. Moreover, dynamic MRI was able to show the low der wall is an infiltrating or superficial tumor.2 Since the signal intensity muscle layer, and the differential enhancebladder tumor density on CT is similar to that of the nor- ment of the mucosal lining and bladder wall more often than mal bladder wall, the major and most well recognized limi- late gadolinium-enhanced MRI. Thus, the use of gadolinium tation of CT is its inability to depict correctly the intramural only improved the accuracy of dynamic enhanced MRI in neoplastic extent. In a recent report 67% of superficial blad- staging superficial bladder cancer. On the contrary, late gader tumors had been incorrectly staged with CT.* dolinium-enhanced MRI was not useful in staging superficial Due to the fact that MRI has some potential advantages bladder cancer due to the less evident signal intensity differover CT, MRI has a n increasingly important role in staging ence between the lesion and bladder wall. Today gadolinium bladder cancer. On T2-weighted sequences MRI can often enhanced MRI is not able to differentiate stage Ta from T1 differentiate superficial tumors from those invading deep bladder tumors and it is unable to detect the presence of muscle because the signal intensity of the bladder lesion is carcinoma in situ, since it is too small for current resolution. higher than that of the normal or hypertrophied wall, which More powerful magnets, further improvements in scanning A disruption of the low techniques, phased array coils and new contrast materials appears as a hypointense TABLE2. Staging accuracy of plain spin echo TI and T2-weighted, dvnamic ,?adolinium-enhanced and delayed MRl in 48 patients No.Pts.(%)
~~~
~
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DYNAMIC ENHANCED MAGNETIC RESONANCE IMAGING IN BLADDER CANCER STAGING
1597
FIG. 1. Stage T1 transitional cell carcinoma of bladder. A, axial plain spin echo T1-weighted sequence (repetition timdecho delay time 500/20 msec.) shows low intensity lesion arising from left lateral wall of bladder. Note that signal is similar to one from bladder wall, which appears as irregular and disrupted line in region of tumor. B,axial plain spin echo T2-weighted se uence (repetition timdecho delay time 2,000/40 msec.) reveals high signal tumor disrupting low signal intensity muscle layer of bladder wJ1 and suggesting that it has infiltrated bladder wall. C, transverse dynamic gadolinium-enhanced MRI (re etition timdecho delay time 200/15 msec.) 30 seconds after contrast material injection demonstrates differential enhancement between gladder tumor and muscle layer, which appears as uninterru ted low intensity line. Su erficial infiltration from bladder tumor was correctly assessed. D, on delayed sequence (repetition timdecho defay time 500120 msec.) different enhancement between lesion and bladder wall is not visible. Dynamic MRI provides more detailed information concerning differentiation between superficial and muscle-invasive bladder tumor than late gadoliniumenhanced MRI.
FIG.2. Stage pT3a bladder tumor. Axial plain spin echo T1-weighted MRI sequence (repetition timdecho delay time 500/20 msec.) shows low signal intensity bladder tumor that is indistinguishable from signal intensit of bladder wall. A, assessment of depth of tumor infiltration is critical on plain s in echo T1-weighted MRI. €3, on dynamic MRI enhanced gladder tumor contrasts with hypointense muscle layer and correct depth of infifkation can be assessed.
might probably provide better results. In any case, in our opinion diagnostic techniques that are able to differentiate stage T1 from T2 tumors are of greater value than those that differentiate stage Ta from T1 cancer because a more aggressive and more radical treatment is necessary only in the presence of a bladder lesion that infiltrates the muscular layer of the bladder wall. The degree of bladder distension was a determinant factor in staging superficial tumors. With an over distended bladder, the thickness of the bladder wall became too thin to distinguish superficial invasion from deep muscular invasion. On the contrary, when the bladder was not distended in some cases the collapsed bladder mucosa mimicked tumor infiltration. Our patients were asked to present for examination with a moderately distended bladder and to drink 2 or more glasses of water when this was not considered full enough. Except for these considerations, over staging remained the most frequent error due to the presence of an
inflammatory reaction around the tumor, which with current diagnostic techniques cannot be distinguished from a tumor. Gadolinium enhancement in the dynamic and late enhanced MRI was also useful in staging bladder tumor with invasion of the seminal vesicles and prostate. Tumor enhancement allowed us to distinguish between the hypointense seminal vesicles and hyper-intense neoplastic tissue. On the contrary, staging bladder tumors with perivesical infiltration (stage pT3b) by dynamic and delayed enhanced MRI was not accurate due to the gadolinium enhancement of the bladder tumor, which decreased the signal intensity contrast between pelvic fat and tumor. Another diagnostic technique that has provided highly accurate results in the assessment of early lesions is transvesical u l t r a s o ~ n dAlthough . ~ ~ ~ ~Schuller ~ ~ ~ ~et al reported a 92% staging accuracy rate28 and Pavone et a1 concluded that transurethral ultrasonography was superior to CT and plain MRI,30 others did not confirm these good results.11 Cumula-
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DYNAMIC ENHANCED MAGNETIC RESONANCE IMAGING IN BLADDER CANCER STAGING
tive results of studies on accuracy of transurethral ultrasonography showed an over staging error of 24% for stage T1 disease or less and an under staging error of 10%for stage T2 cancer or greater.' This method allows the bladder m u w a to be separately visualized f h m the muscular layer, thus, enabling early superficial tumors to be Werentiated from those with deeper invasion of the bladder wall. Unfortunately, transurethral ultrasonography is less accurate in staging locally advanced bladder cancer because the tumor extends beyond the penetration depth of the ultrasound beam.= Its major disadvantage and limitation are the need to perform the examination with the patient under general, spinal or epidural anesthesia. Furthermore, the equipment for transurethral sonography,which requires a special transducer, is not widely available. Presently, this technique is not considered the method of choice for staging superficial bladder cancer. Most authors agree that conventional clinical techniques, such as excretory urography, cyt~logy,b i m a n d examination, cystoscopy and biopsy, are a m a t e in staging superficial tumors while they are less accurate in cases of locally advanced disease.31 These techniques are considered to be capable of staging correctly superficial tumor (carcinoma in situ to T1) in 50 to 80% of cases.20 More importantly,cumulative results of studies on the accuracy of clinical staging
before the era of cross-sectional imaging showed that the overall sensitivity for pathologicalstage T2 or greater disease was 95%.1 Nevertheless, the overall staging accuracy rate was low at 354Rb.l The majority of these studies, similarly to ours, have used a combination of cystectomy and transurethral resection of the tumor for pathological staging. From these considerations, dynamic enhanced MRI seems equally effective to conventional clinical staging in differentiating superficial disease as a group from muscle-invasive disease but with a higher overall staging accuracy. A large prospective blinded study comparing dynamic enhanced MRI, CT, transurethral ultrasonography and conventional techniques is needed to define the ultimate applicability of gadoliniumenhanced MRI in staging superficial bladder cancer. CONCLUSIONS
Dynamic MRI has provided more detailed information on differentiationbetween superficial and muscle-invasivebladder tumor than late gadolinium-enhancedMRI. Even if dynamic MRI were superior to =-weighted sequences in demonstrating the presence of the unbroken hypointense line of the muscular wall, over staging remained the most frequent error in superficial bladder cancer.
APPENDIX: CRITERIA ESTABLISHED TO ASSESS CLINICAL STAGE OF BLADDER CANCER ON PLAIN SPIN ECHO T1-WEIGHTED AND T2-WEIGHTED MRI, AND GADOLINIUM-ENHANCED MRI
TNM stage
Ta-T1
T2 T3a
T3b
T4a
Plain T1-Weighted MRI N e ~ ~ l a ~lesion t i c with normal &ter bladder wall seen as low intensity band Same findings as for stage T1 Bladder tumor with thickening of adjacent bladder wall, interface between bladder wall and perivesical fat regular Hypointense bladder lesion with irregular interface showing hyper-intense perivesical fat Strands of soft tissue contiguous with the primary tumor in extravesical organ
REFERENCES
Plain T2-Weighted MRI
Dynamic Gadolinium-Enhanced MRI
Enhanced tumor and adjacent mucosa with unbroken hypointense muscular layer Wall Irregularity of hypointense muscular Bladder tumor with focally diswall due to presence of enhanced rupted low intensity band of bladder Ca bladder wall Interruption of hypointense line of Bladder tumor with completely muscular layer showing regular disrupted low intensity band of interface between enhanced lesion bladder wall and perivesical fat Lesion showing abnormal intenEnhanced bladder Ca extending into sity in perivesical fat with comhyper-intense perivesical fat pletely disrupted low intensity band of bladder wall Hypointense large bladder tumor Interrupted perivesical fat-bladder that replaces hyper-intense wall plane with evidence of enseminal vesicle, or infiltrates hanced tumor in adjacent organs, prostate or uterus (sagittal and which display with abnormal archicoronal scans) tecture
NGplasticTesion &owing unbroken hypointense line of bladder
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