AJR 2003; 180:771-777
© American Roentgen Ray Society
MR Imaging Features of Transitional Cell Carcinoma of the Urinary Bladder
Aylin Tekes1,
Ihab R. Kamel1,
Khursheed Imam1,
Theresa Y. Chan2,
Mark P. Schoenberg3 and
David A. Bluemke1
1 Russell H. Morgan Department of Radiology and Radiological Sciences, Johns
Hopkins Hospital, Rm. 100, 600 N. Wolfe St., Baltimore, MD 21287.
2 Department of Pathology, Johns Hopkins Hospital, Weinberg Bldg., Baltimore, MD
21287.
3 James Buchanan Brady Urological Institute, Johns Hopkins University Medical
Institutions, Marburg 150, Baltimore, MD 21287-2101.
Received March 7, 2002;
accepted after revision August 6, 2002.
Presented at the annual meeting of the American Roentgen Ray Society,
Atlanta, April—May 2002.
Address correspondence to I. R. Kamel.
Introduction
Bladder cancer is a common tumor of the urinary tract, accounting for 6-8%
of malignancies in men and 2-3% of malignancies in women
[1]. Transitional cell
carcinoma constitutes approximately 90% of all primary tumors of the urinary
bladder. Development of transitional cell carcinoma seems to be related to
both genetic and environmental factors. Among the latter, chemical exposure is
thought to be of great importance. Bladder tumors are more common in
industrial areas, and their incidence is increased with exposure to cigarette
smoke and arylamines [2].
Cystitis and chronic urinary tract infection predispose patients to bladder
cancer, and 7% of bladder tumors occur within diverticula
[1]. Noninvasive imaging aids
in determining the tumor stage, including detection of local extension of the
tumor, lymph node involvement, and distant metastasis
[3]. MR imaging is superior to
CT for staging carcinoma of the urinary bladder and offers several advantages
over CT and sonography. The multiplanar imaging capability and excellent
tissue contrast allow improved evaluation of the location and extent of the
tumor, as well as improved characterization of the lesion
[4].
The purpose of this pictorial essay is to present different manifestations
of transitional cell carcinoma of the bladder as depicted on state-of-the-art
MR imaging in a large series of surgically and pathologically proven
cases.
Technique
MR images were obtained on a 1.5-T MR scanner (Signa; General Electric
Medical Systems, Milwaukee, WI) with a phased array pelvic coil. Conventional
T1-weighted spin-echo images (TR/TE, 550/9; matrix, 512 x 192; field of
view, 20 cm; section thickness, 6 mm; intersection gap, 2 mm; signals
acquired, 4) and T2-weighted fast spin-echo images (TR range/TE range,
4000-5500/80-120; matrix, 256 x 256; field of view, 24 cm; section
thickness, 6 mm; intersection gap, 2 mm; signals acquired, 4) with fat
suppression were obtained. Subsequently, fast multiplanar spoiled
gradient-echo images (180-300/1.7-4.2; flip angle, 70°; matrix, 512
x 192; slice thickness, 6 mm; intersection gap, 2 mm; signals acquired,
2) with fat suppression were obtained in the axial plane before, at 20 sec
(arterial phase), and at 70 sec (venous phase) after injection of
gadopentetate dimeglumine (0.1 mmol/kg). Sagittal and coronal
gadolinium-enhanced images were added if the tumor was located in the base or
the dome of the bladder. In each patient, histologic sections were obtained
from cystectomy or transurethral resection specimens and correlated with the
MR imaging findings.
Staging
MR imaging is the first modality of choice in imaging of urinary bladder
cancer, with an accuracy of 73-96%. TNM staging, updated in 1997, was used in
this study [5]. Tumor staging
includes T0, no tumor; Tis, in situ carcinoma (flat tumor)
(Fig. 1); Ta, noninvasive
papillary carcinoma (Fig.
2A,2B);
T1, tumor invading subepithelial connective tissue; T2a, tumor invading
superficial muscle layer; T2b, tumor invading deep muscle (Fig.
3A,3B);
T3a, tumor invading perivesical tissue microscopically (Fig.
4A,4B);
T3b, tumor invading perivesical fat macroscopically (Figs.
5A,5B,5C,5D
and
6A,6B);
T4a, tumor invading prostate, uterus, or vagina; and T4b, tumor invading
pelvic or abdominal wall (Fig.
7A,7B).
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Fig. 1. —64-year-old woman with bladder diverticulum and in situ
carcinoma. Axial arterial phase contrast-enhanced fast spoiled gradient-echo
MR image (TR/TE, 250/2.9) shows small diverticulum arising from left lateral
wall. Note submucosal enhancement of diverticulum (arrow). At
surgery, patient was found to have in situ transitional cell carcinoma.
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Fig. 2A. —60-year-old man with papillary (stage Ta) transitional cell
carcinoma of bladder. Axial T2-weighted MR image (TR/TE, 5000/120) shows
multiple, intermediate-signal-intensity papillary lesions arising from bladder
wall (straight arrows). Note that hypointense signal of bladder wall
is not disrupted (curved arrow), indicating that tumors are confined
to organ.
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Fig. 2B. —60-year-old man with papillary (stage Ta) transitional cell
carcinoma of bladder. Axial arterial phase gadolinium-enhanced MR image
(300/2.2) obtained at slightly higher level than A with more distended
bladder shows early homogeneous enhancement of tumors (straight
arrow), whereas bladder wall shows low signal (curved arrow)
with adjacent submucosal enhancement. Tumor on right bladder base was biopsied
and found to be stage Ta tumor. Patient was followed up for 2 years and
remains with treated stage Ta tumor.
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Fig. 3A. —68-year-old man with stage T2b transitional cell carcinoma of
bladder. Axial T2-weighted MR image (TR/TE, 4200/80) shows large diverticulum
(straight arrow) arising from right posterior wall of bladder. Note
large broad-based tumor of intermediate signal intensity that disrupts dark
signal intensity on right side of bladder wall (curved arrow). Mass
(M) protrudes into bladder lumen. Note also another focus of tumor in left
lateral wall (arrowhead).
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Fig. 3B. —68-year-old man with stage T2b transitional cell carcinoma of
bladder. Axial arterial phase gadolinium-enhanced fast spoiled gradient-echo
MR image (300/1.9) reveals extension of heterogeneously enhancing mass
(asterisk) into diverticulum (arrow). Note disruption of
normal signal in right bladder wall where tumor originates.
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Fig. 4A. —57-year-old man with stage T3a transitional cell carcinoma of
bladder. Axial T2-weighted MR image (TR/TE, 4000/80) shows slightly
hyperintense sessile mass infiltrating bladder wall posteriorly at site of
muscle disruption (arrow).
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Fig. 4B. —57-year-old man with stage T3a transitional cell carcinoma of
bladder. Axial arterial phase fast spoiled gradient-echo MR image (200/2.1)
obtained after administration of gadolinium shows strong homogeneous
enhancement of sessile mass (curved arrow) with minimal extension
into perivesical fat (straight arrow).
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Fig. 5A. —70-year-old man with stage T3b transitional cell carcinoma of
bladder. Axial T2-weighted MR image (TR/TE, 4200/80) shows hypointense sessile
mass arising from left posterolateral wall extending into perivesical fat
(straight arrows). Note that lower portion of left ureter is
surrounded by mass, resulting in hydroureter (curved arrow).
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Fig. 5B. —70-year-old man with stage T3b transitional cell carcinoma of
bladder. Axial arterial phase fast spoiled gradient-echo MR image (225/2.9)
obtained after administration of gadolinium reveals irregular inner contour
and prominent submucosal enhancement (curved arrow). Notice shaggy
outer contour of mass due to invasion of perivesical fat (straight
arrow).
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Fig. 5C. —70-year-old man with stage T3b transitional cell carcinoma of
bladder. Axial arterial phase fast spoiled gradient-echo MR image (225/2.9)
obtained after administration of gadolinium shows urethral enhancement
(arrow), which is commonly seen in absence of urethral involvement
and could be physiologic or from previous transurethral resection.
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Fig. 5D. —70-year-old man with stage T3b transitional cell carcinoma of
bladder. Photomicrograph of cystectomy specimen shows invasive high-grade
urothelial carcinoma infiltrating muscularis propria muscle bundles
(straight arrows) and perivesical fat (curved arrow). (H and
E, x100)
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Fig. 6A. —58-year-old man with stage T3b transitional cell carcinoma of
bladder. Axial arterial phase contrast-enhanced fast spoiled gradient-echo MR
image (TR/TE, 180/1.9) reveals irregular, heterogeneously enhancing sessile
mass on left anterior and lateral wall (open arrow). Note left-sided
tumor implant (curved arrow) that is located in perivesical fat and
left external iliac lymph node that shows peripheral enhancement (straight
solid arrow).
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Fig. 6B. —58-year-old man with stage T3b transitional cell carcinoma of
bladder. Axial arterial phase contrast-enhanced fast spoiled gradient-echo MR
image (180/1.9) obtained at slightly higher level than A shows that
most of tumor is located in dome (arrows). Note three brightly
enhancing tumor implants (arrowheads) in perivesical fat located
anterior to main tumor mass.
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Fig. 7A. —66-year-old man with stage T4b transitional cell carcinoma of
bladder. Axial T2-weighted MR image (TR/TE, 4700/80) shows sessile mass
(straight arrow) of intermediate signal intensity located in anterior
wall of bladder with extension into perivesical fat on right side (curved
arrow). Surgery revealed involvement of posterior rectus sheath (not
shown).
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Fig. 7B. —66-year-old man with stage T4b transitional cell carcinoma of
bladder. Axial venous phase fast spoiled gradient-echo MR image (200/1.9)
obtained after administration of gadolinium shows bright enhancement of mass
(straight arrows) with extension into perivesical fat (curved
arrow).
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Metastasis in a single lymph node less than or equal to 2 cm in greatest
dimension is stage N1, metastasis in a single lymph node greater than 2 cm but
less than 5 cm in greatest dimension or multiple lymph nodes is stage N2
(Fig. 8), and metastasis in a
lymph node greater than 5 cm in greatest dimension is stage N3. Distant
metastasis is stage M1 [5].
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Fig. 8. —56-year-old woman with stage T3b transitional cell carcinoma
of bladder. Axial venous phase fast spoiled gradient-echo MR image (TR/TE,
200/1.9) obtained after administration of gadolinium shows intense enhancement
of sessile mass (straight arrows) arising from left lateral wall,
filling most of bladder lumen. Enlarged lymph node in left obturator chain
(curved arrow) shows heterogeneous enhancement consistent with tumor
involvement.
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Clinical Presentation
Gross or microscopic hematuria is the most common presentation of
transitional cell carcinoma, followed by symptoms related to associated
urinary infection. Most cases of transitional cell carcinoma of the bladder
present in patients more than 50 years old. Men are affected more often than
women, and whites more often than blacks
[2]. At the time of
presentation, 30% of the patients had multifocal disease (Fig.
2A,2B),
and widespread areas of squamous metaplasia and carcinoma in situ
[1] may have been present.
Morphologic Features
Transitional cell carcinoma can arise any-where in the bladder, but it is
most commonly located in the lateral wall (Figs.
3A,3B,
5A,5B,5C,5D,
and 8). When it is located
around the ureteral orifices, the tumor may produce partial or complete
blockage of one or both ureters, resulting in hydroureter and hydronephrosis
[2] (Figs.
5A,5B,5C,5D
and
9A,9B,9C,9D).
Transitional cell carcinomas manifest a variety of patterns of tumor growth
including papillary (Figs.
2A,2B
and
9A,9B,9C,9D),
sessile (Figs.
7A,7B
and 8), infiltrating (Fig.
5A,5B,5C,5D),
nodular, mixed, and flat intraepithelial growth
(Fig. 1). Because the bladder
does not have a distinct basement membrane, it is difficult to show invasion
of the lamina propria [6].
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Fig. 9A. —58-year-old man with papillary (Ta) transitional cell
carcinoma of bladder. T2-weighted MR image (TR/TE, 4000/80) shows polypoid
mass (straight arrow) arising from right posterolateral wall,
obstructing right ureterovesical junction and causing hydroureter (curved
arrow).
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Fig. 9B. —58-year-old man with papillary (Ta) transitional cell
carcinoma of bladder. Axial arterial phase gadolinium-enhanced MR image
(200/2.9) shows bright homogeneous enhancement of mass (arrow).
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Fig. 9C. —58-year-old man with papillary (Ta) transitional cell
carcinoma of bladder. Photomicrograph of transurethral resection specimen
shows low magnification view of high-grade papillary urothelial carcinoma.
Tumor shows exophytic growth and is confined to surface urothelium (curved
arrows). Hyperchromasia of cells lining fibrovascular cores (straight
arrows) is noted even at this power. (H and E, x40)
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Fig. 9D. —58-year-old man with papillary (Ta) transitional cell
carcinoma of bladder. Photomicrograph of transurethral resection specimen
shows high magnification of high-grade papillary urothelial carcinoma. Note
disorganized, hyperchromatic, and pleomorphic cells with mitoses. (H and E,
x400)
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MR Imaging Features
Urinary carcinomas have an intermediate signal intensity, equal to that of
muscle on T1-weighted images. T1-weighted images are used to assess
perivesical fat invasion and lymph node involvement. T2-weighted images aid in
determining the depth of tumor infiltration in the bladder wall (Fig.
2A,2B).
On T2-weighted images, urine has high signal intensity, and the bladder wall
appears hypointense. Bladder tumors have the same or slightly higher signal
intensity as the bladder wall on T2-weighted images. An intact,
low-signal-intensity muscle layer at the base of the tumor is classified as
stage Ta or T1; a disrupted low-signal-intensity muscle layer without
infiltration of perivesical fat is classified as stage T2b (Fig.
3A,3B).
Urinary bladder carcinomas and their metastases develop neovascularization
[7]; therefore, these tumors
enhance earlier than the normal bladder wall
[8] (Figs.
2A,2B,
4A,4B,
and
5A,5B,5C,5D).
In the arterial phase of contrast enhancement, bladder tumors enhance more
than the muscle of the bladder. Superficial tumors (those without muscle
invasion stage T1 and lower) may be differentiated from muscle invasive tumors
on contrast-enhanced images (Fig.
2A,2B).
On contrast-enhanced studies, a lesion with an irregular, shaggy outer border,
and streaky areas of the same signal intensity of the tumor in perivesical fat
is classified as stage T3b (Fig.
5A,5B,5C,5D).
A tumor extending into an adjacent organ or abdominal and pelvic sidewall with
the same signal intensity as that of the primary tumor is classified as stage
T4a or T4b, respectively. With the current resolution of 1.5-T MR scanners, MR
imaging cannot differentiate stage Ta tumors from T1, and differentiation of
stage T2a tumors (superficial muscle invasion) from stage T2b (deep muscle
invasion) is problematic and can be better delineated on contrast-enhanced
studies [3].
Role of MR Imaging After Treatment
Restaging carcinoma of the urinary bladder after treatment is particularly
challenging. Intravesical therapy with chemotherapeutic agents is used to
treat low-stage tumors. Intravesical therapy may cause bright submucosal
enhancement after administration of gadolinium
(Fig. 10). Previous
transurethral resection or biopsy of the tumor may cause inflammation and
edema, which may result in overstaging (Figs.
11A,11B,11C
and
12A,12B,12C).
Using MR imaging, we found that it is not possible to discriminate by signal
characteristics alone between edema as a result of treatment and tumor
recurrence, but the presence of a mass with signal characteristics typical of
tumor may enable the diagnosis of recurrence
[1].
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Fig. 10. —61-year-old man with in situ transitional cell carcinoma
after intravesical mitomycin therapy. Axial arterial phase contrast-enhanced
fast spoiled gradient-echo MR image (TR/TE, 125/4.2) shows minimal thickening
of anterior bladder wall and bright early submucosal enhancement of anterior
and lateral walls (arrow), which is commonly seen after intravesical
therapy.
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Fig. 11A. —74-year-old man with stage T1 transitional cell carcinoma of
bladder who underwent MR imaging 2 weeks after transurethral resection. Axial
T2-weighted MR image (TR/TE, 4500/120) shows papillary lesion located on left
at base of bladder (straight arrow). Note predominantly dark,
heterogeneous signal intensity on right in bladder lumen (curved
arrow).
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Fig. 11B. —74-year-old man with stage T1 transitional cell carcinoma of
bladder who underwent MR imaging 2 weeks after transurethral resection. Axial
fast spoiled gradient-echo unenhanced MR image (160/4.2) shows high signal
intensity on right side of bladder. Low signal intensity of same area shown in
A suggests presence of blood clot (arrow).
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Fig. 11C. —74-year-old man with stage T1 transitional cell carcinoma of
bladder who underwent MR imaging 2 weeks after transurethral resection. Axial
venous phase gadolinium-enhanced fast spoiled gradient-echo MR image (160/4.2)
shows intense homogeneous enhancement of papillary lesion on left side of
bladder (straight arrow). Contour deformity due to previous biopsy
and strong enhancement of bladder wall due to delayed phase of contrast
enhancement mimic stage T2b tumor. Note different signal characteristics of
blood products on right side, which do not show contrast enhancement
(curved arrow).
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Fig. 12A. —64-year-old man with suspected tumor who underwent MR imaging
3 months after biopsy of bladder was negative for tumor. Axial unenhanced fast
spoiled gradient-echo MR image (TR/TE, 275/4.2) shows left posterolateral
thickening of bladder wall (arrow). Wall thickening was due to edema
after biopsy. No neoplasm was found histologically.
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Fig. 12B. —64-year-old man with suspected tumor who underwent MR imaging
3 months after biopsy of bladder was negative for tumor. Axial arterial phase
fast spoiled gradient-echo MR image (275/4.2) obtained 60 sec after injection
of gadolinium shows bright and homogeneous enhancement of same area
(arrow). Bright and homogeneous enhancement was due to prior biopsy.
Histopathologic examination did not reveal transmural spread of tumor.
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Fig. 12C. —64-year-old man with suspected tumor who underwent MR imaging
3 months after biopsy of bladder was negative for tumor. Photomicrograph of
transurethral resection specimen shows urothelial mucosa with multiple cystic
(straight arrows) and glandular structures (curved arrows)
in lamina propria. Cystic structures are lined by benign flattened or cuboidal
urothelial cells. Glandular epithelium is columnar with apical cytoplasm
containing mucin vacuoles. No cytologic atypia is present to suggest
malignancy. (H and E, x100)
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Conclusion
MR imaging with dynamic gadolinium enhancement readily shows the extent of
bladder tumor and the involvement of adjacent organs. Clinical staging,
including transurethral resection, can assess involvement of deep muscle, but
staging is inaccurate in detecting extravesical disease. Patients with
extravesical tumors show significantly higher recurrence rates and lower
survival rates compared with those who have organ-confined tumors. MR imaging
thus plays a critical role in improving staging accuracy, determining
treatment methods, and assessing response to therapy.
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Introduction
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