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DOI:10.2214/AJR.05.0172
AJR 2007; 188:W256-W261
© American Roentgen Ray Society

Clinical Observations

Gadolinium-Enhanced Fat-Suppressed T1-Weighted Imaging for Staging Ureteral Carcinoma: Correlation with Histopathology

Masao Obuchi1,2, Kousei Ishigami3, Koji Takahashi4, Minoru Honda5, Toshiyuki Mitsuya6, David M. Kuehn2, Alan H. Stolpen2, Bruce P. Brown2 and Akihiro Nishie3

1 Present address: Department of Radiology, Showa University Fujigaoka Hospital, 1-30 Fujigaoka, Aoba-ku, Yokohama, Kanagawa 227-0043, Japan.
2 Department of Radiology, University of Iowa Hospitals and Clinics, Iowa City, IA 52242.
3 Department of Clinical Radiology, Graduate School of Medical Sciences, Kyushu University, Higashi-ku, Fukuoka, Japan.
4 Department of Radiology, Asahikawa Medical College, Midorigaoka, Asahikawa, Japan.
5 Department of Radiology, Showa University Hospital, Shinagawa-ku, Tokyo, Japan.
6 Department of Pathology, Showa University Fujigaoka Hospital, Aoba-ku, Yokohama, Japan.

Received February 1, 2005; accepted after revision September 15, 2005.

 
Address correspondence to M. Obuchi (m-obuchi{at}showa-university-fujigaoka.gr.jp).

WEB This is a Web exclusive article.


Abstract
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 Abstract
Introduction
 Materials and Methods
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OBJECTIVE. The purpose of this study was to retrospectively compare contrast-enhanced fat-suppressed T1-weighted images with histopathologic findings in ureteral carcinoma to develop accurate preoperative MR criteria for T staging.

CONCLUSION. Contrast-enhanced fat-suppressed T1-weighted images can be used to distinguish thickened noncarcinomatous ureteral walls, which occur due to the proliferation of fibrous tissue, from ureteral carcinoma because fibrous tissue enhances more intensely on MRI than ureteral carcinoma. We also observed that when ureteral carcinomas had invaded periureteral fat tissue, a disruption or fragmentation of the intensely enhancing ureteral wall was seen. Using the MR criteria for T staging that we developed on the basis of these findings, we were able to accurately determine whether a carcinoma had invaded periureteral fat tissue in all of our patients.

Keywords: genitourinary tract imaging • imaging-histopathologic correlation • MRI • oncologic imaging • T1-weighted imaging • ureteral carcinoma


Introduction
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 Abstract
 Introduction
Materials and Methods
 Results
 Discussion
 References
 
The accurate determination of tumor extent in patients with ureteral carcinoma plays an important role in therapeutic planning. Although nephroureterectomy with a bladder cuff is a standard treatment for ureteral carcinoma, adjuvant or neoadjuvant chemotherapy may also be considered for downstaging locally advanced (more than T3) ureteral carcinoma. Chemotherapeutic downstaging and subsequent management decisions are dependent on accurate initial and secondary clinical staging. Furthermore, it may be possible to consider organ-sparing treatments when ureteral carcinoma is superficial.

Although CT and MRI both provide information about intraluminal lesions, the ureteral wall, and associated extraluminal tissues, previous reports have indicated that the accuracy of T staging using CT is limited [1-5]. A few reports evaluate staging ureteral carcinomas using MRI [6-8], but these reports include both renal pelvis and ureteral tumors, and none, to our knowledge, includes more than four ureteral tumors. In addition, these reports evaluated only the morphologic changes—not the density, signal intensity, or enhancement pattern. We found that using gadolinium-enhanced fat-suppressed T1-weighted images for staging ureteral carcinoma improves the accuracy of T staging.

The purpose of this study was to compare gadolinium-enhanced fat-suppressed T1-weighted images with histopathologic findings in ureteral carcinoma to develop accurate preoperative MR criteria for T staging.


Materials and Methods
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 Abstract
 Introduction
 Materials and Methods
Results
 Discussion
 References
 
Patients
This was a retrospective single-institution study. The institutional review board approved all aspects of this study and did not require informed consent from the patients whose records were used.

A review of the database of MR examinations collected over a 5-year period (1998-2002) revealed that 232 examinations using gadolinium-enhanced fat-suppressed T1-weighted imaging were performed to assess urinary obstruction. Among these cases were 12 patients with surgically proven ureteral carcinoma (five men, seven women; age range, 54-80 years; mean age, 71.3 years) who had also undergone MRI within 2 months before surgery (Table 1). The postsurgical pathologic diagnoses were seven transitional cell carcinomas (TCCs) and five squamous cell carcinomas (SCCs). The postsurgical T staging (pT) system used is as follows: pT1, tumor is confined to the submucosa; pT2, tumor invades into, but not through, the muscularis; pT3, tumor invades the periureteral fat; and pT4, tumor extends to distant organs [9]. There were three patients with pT1, one with pT2, six with pT3, and two with pT4 tumors.


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  		TABLE 1: Patient Characteristics, Pathologic Diagnosis, and T Staging

 

MRI
MR examinations were performed on a 1.0-T scanner (Signa Horizon, GE Healthcare) with a torso phased-array coil. All pulse sequences were breath-holding acquisitions, including T1-weighted, T2-weighted, and dynamic gadolinium-enhanced MRI, through the abdomen and pelvis.

Coronal and axial T1-weighted fast spoiled gradient-echo localizer images were obtained. The imaging parameters included a TR range/TE of 150-200/2.3, 256 x 128 matrix, 10-mm slice thickness, and 5-mm slice gap. Ten slices were obtained during one 19-second breath-hold. A coronal breath-hold fat-suppressed heavily T2-weighted single-shot fast spin-echo image was obtained with a TR/TE of infinite/1,164, 256 x 256 matrix, one-half signal acquired, 50-mm slice thickness, and receiver bandwidth of 20.8 kHz. Coronal and axial non-fat-suppressed T2-weighted single-shot fast spin-echo images were obtained with a TR/TE of infinite/93, 256 x 160-192 matrix, one-half signal acquired, 5-mm slice thickness, 0-mm slice gap, and receiver bandwidth of 62.5 kHz.

Coronal breath-hold 3D fast spoiled gradient-echo images with fat saturation were obtained before and 30 and 90 seconds after the IV administration of 0.1 mmol/kg of gadolinium chelate (gadopentetate dimeglumine [Magnevist, Schering]). The injection rate was 1 mL/s, and the contrast injection was followed by a 20-mL saline chaser administered at the same injection rate. Imaging parameters included 6.4/1.4, an inversion time of 27 milliseconds, a flip angle of 20°, 256 x 192 matrix, 1 signal acquired, 8-mm slice thickness, and 96-mm slab thickness. Using the same imaging parameters, axial gadolinium-enhanced fat-suppressed T1-weighted images were obtained 180-210 seconds after gadolinium chelate was administered IV at the site of obstruction shown on the T2-weighted images.

Review of MR Images
Delayed phase gadolinium-enhanced fat-suppressed T1-weighted images obtained 90 seconds, 180-210 seconds, or both 90 and 180-210 seconds after IV administration of gadolinium were retrospectively reviewed. First, a comparison was made between the gadolinium-enhanced fat-suppressed T1-weighted images and the pathologic findings by a radiologist in conjunction with a pathologist. Next, the relationship between gadolinium-enhanced fat-suppressed T1-weighted images and pT staging was evaluated, and the radiologist developed MR staging criteria based on gadolinium-enhanced fat-suppressed T1-weighted images. The staging criteria were then used to determine whether a tumor had invaded periureteral fat tissue (T3 or T4) or not (T2 or lower). The radiologic findings of an intensely enhancing rim seen at the tumor region on delayed phase gadolinium-enhanced fat-suppressed T1-weighted images were divided into three categories: smooth; irregular, disrupted, or fragmented (or a combination thereof); and not detected.

Two other radiologists, having 9 and 22 years of experience with body imaging, respectively, evaluated the criteria separately. Both were blinded to the pT staging but were informed about the patients' diagnoses and site of the tumors. Each observer reviewed only the delayed phase gadolinium-enhanced fat-suppressed T1-weighted images of each patient and evaluated the MR images for morphologic changes of the intensely enhancing rim. A checklist was used for the evaluation, which included a description of the intensely enhancing rim (seen or not; smooth, irregular, disrupted, or fragmented), and whether the tumor had invaded periureteral fat tissue (T3 or T4) or not (T2 or lower).


Results
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 Abstract
 Introduction
 Materials and Methods
 Results
Discussion
 References
 
Comparison of Imaging Findings and Pathologic Results
In the segments of ureters involved with tumors, three kinds of structures could be seen: first, an intensely enhancing rim, which corresponded to thickening of the ureteral wall due to marked proliferation of fibrous tissue with little or no invasion of cancer cells; second, moderately enhancing mass, which corresponded to cancer cells (both TCC and SCC); and, third, poorly or nonenhancing structures, which corresponded to necrotic tissue (Figs. 1A, 1B, 1C and 2A, 2B, 2C).


Figure 1
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  		Fig. 1A —Stage pT1 transitional cell carcinoma (TCC) of left ureteropelvic junction. Coronal gadolinium-enhanced fat-suppressed T1-weighted image (A) obtained 90 seconds after IV administration of gadolinium in 79-year-old man (case 1 in Table 1) and schema (B) corresponding to circled region in A show intensely enhancing rim (arrows) and moderately enhancing mass (arrowheads).

 

Figure 2
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  		Fig. 1B —Stage pT1 transitional cell carcinoma (TCC) of left ureteropelvic junction. Coronal gadolinium-enhanced fat-suppressed T1-weighted image (A) obtained 90 seconds after IV administration of gadolinium in 79-year-old man (case 1 in Table 1) and schema (B) corresponding to circled region in A show intensely enhancing rim (arrows) and moderately enhancing mass (arrowheads).

 

Figure 3
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  		Fig. 1C —Stage pT1 transitional cell carcinoma (TCC) of left ureteropelvic junction. Photograph of pathologic specimen from patient in A shows TCC (arrowheads) that is confined to submucosa and thickened muscularis or adventitia due to proliferation of fibrous tissue (arrows). Intensely enhancing rim corresponds to thickened muscularis or adventitia due to proliferation of fibrous tissue. Moderately enhancing mass corresponds to TCC. (H and E, loupe)

 

Figure 4
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  		Fig. 2A —Stage pT3 squamous cell carcinoma (SCC) of right distal ureter. Axial gadolinium-enhanced fat-suppressed T1-weighted image (A) obtained 210 seconds after IV administration of gadolinium in 78-year-old woman (case 9 in Table 1) and schema (B) corresponding to circled region in A show intensely enhancing rim (white arrows), relatively moderate enhancing ill-defined mass (arrowheads), and poorly enhancing region (curved arrow). Intensely enhancing rim is disrupted in its left to posterior aspect (straight black arrow, B), and relatively moderate enhancing ill-defined mass is spread inside and outside of disrupted portion.

 

Figure 5
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  		Fig. 2B —Stage pT3 squamous cell carcinoma (SCC) of right distal ureter. Axial gadolinium-enhanced fat-suppressed T1-weighted image (A) obtained 210 seconds after IV administration of gadolinium in 78-year-old woman (case 9 in Table 1) and schema (B) corresponding to circled region in A show intensely enhancing rim (white arrows), relatively moderate enhancing ill-defined mass (arrowheads), and poorly enhancing region (curved arrow). Intensely enhancing rim is disrupted in its left to posterior aspect (straight black arrow, B), and relatively moderate enhancing ill-defined mass is spread inside and outside of disrupted portion.

 

Figure 6
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  		Fig. 2C —Stage pT3 squamous cell carcinoma (SCC) of right distal ureter. Photograph of pathologic specimen shows SCC (white arrowheads) and thickening of both muscularis and adventitia (white arrows) due to marked proliferation of fibrous tissue that is partially invaded by SCC. Necrotic change is also depicted in tumor (curved arrow). Tumor invaded into periureteral fat tissue through area in thickened muscularis, and adventitia (black arrow) was disrupted. Intensely enhancing rim corresponds to thickened muscularis and adventitia due to proliferation of fibrous tissue. Relatively moderate enhancing ill-defined mass corresponds to SCC. Poorly enhancing region corresponds to necrotic tissue in tumor. (H and E, loupe)

 
Relationship Between pT Staging and Imaging Findings
In the cases of pT1 (n = 3) and pT2 (n =1) tumors, gadolinium-enhanced fat-suppressed T1-weighted images clearly depicted an intensely enhancing rim with smooth margins in all four cases. In two of the pT1 cases, no moderately enhancing mass suggesting carcinoma was seen (Fig. 3A, 3B). In four pT3 tumors (n =6), an intensely enhancing rim was seen but was disrupted, and a moderately enhancing mass spread around the disrupted region was noted (Fig. 2A, 2B, 2C). In the other two pT3 tumors, the intensely enhancing rim fragmented into many tiny segments and was surrounded by a moderately enhancing mass (Fig. 4A, 4B). In one of the pT4 tumors (n = 2), a heterogeneous ill-defined mass extended to the left iliac vessels with no definite rim of intense enhancement. In the other pT4 tumor, the intensely enhancing rim was seen but was disrupted, and a moderately enhancing mass that spread around the disrupted region was noted.


Figure 7
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  		Fig. 3A —Stage pT1 transitional cell carcinoma (TCC) of right distal ureter. Axial gadolinium-enhanced fat-suppressed T1-weighted image (A) obtained 210 seconds after IV administration of gadolinium in 70-year-old woman (case 2 in Table 1) and schema (B) corresponding to circled region in A show that intensely enhancing rim is clearly visible and that smooth margin (arrow) is not disrupted. Pathologically, carcinoma is confined to submucosa, and marked fibrous proliferation is noted in adventitia of ureteral wall and in periureteral fat tissue.

 

Figure 8
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  		Fig. 3B —Stage pT1 transitional cell carcinoma (TCC) of right distal ureter. Axial gadolinium-enhanced fat-suppressed T1-weighted image (A) obtained 210 seconds after IV administration of gadolinium in 70-year-old woman (case 2 in Table 1) and schema (B) corresponding to circled region in A show that intensely enhancing rim is clearly visible and that smooth margin (arrow) is not disrupted. Pathologically, carcinoma is confined to submucosa, and marked fibrous proliferation is noted in adventitia of ureteral wall and in periureteral fat tissue.

 

Figure 9
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  		Fig. 4A —Stage pT3 transitional cell carcinoma of right distal ureter. Axial gadolinium-enhanced fat-suppressed T1-weighted image (A) obtained 210 seconds after IV administration of gadolinium in 73-year-old man (case 8 in Table 1) and schema (B) corresponding to circled region in A show intensely enhanced bandlike structure (arrows) that is irregular and disrupted. Moderately enhancing, irregular-shaped mass is depicted, and it invades periureteral tissue (arrowheads). Pathologically, carcinoma invaded periureteral fat tissue.

 

Figure 10
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  		Fig. 4B —Stage pT3 transitional cell carcinoma of right distal ureter. Axial gadolinium-enhanced fat-suppressed T1-weighted image (A) obtained 210 seconds after IV administration of gadolinium in 73-year-old man (case 8 in Table 1) and schema (B) corresponding to circled region in A show intensely enhanced bandlike structure (arrows) that is irregular and disrupted. Moderately enhancing, irregular-shaped mass is depicted, and it invades periureteral tissue (arrowheads). Pathologically, carcinoma invaded periureteral fat tissue.

 
MRI Staging Criteria Using Gadolinium-Enhanced Fat-Suppressed T1-Weighted Images
Figure 5A, 5B shows a schema of the proposed MR T staging criteria based on our results. When an intensely enhancing rim appears smooth, the tumor does not invade the periureteral tissue, which is pT1 or pT2 (Fig. 5A). When an intensely enhancing rim is irregular, disrupted, or fragmented, our study results indicate that the tumor has invaded the periureteral tissue and is pT3 or pT4 (Fig. 5B).


Figure 11
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  		Fig. 5A —Schemas show proposed MR criteria in T staging of ureteral carcinoma based on our results. When intensely enhancing rim (arrow) is clearly visible and its smooth margin is not disrupted, tumor does not invade into periureteral tissue and is less than stage pT2.

 

Figure 12
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  		Fig. 5B —Schemas show proposed MR criteria in T staging of ureteral carcinoma based on our results. When intensely enhancing rim (arrows) is disrupted or fragmented, findings indicate that tumor does invade periureteral tissue and is stage pT3 or pT4.

 
Evaluation by Two Radiologists Using the Staging Criteria
One observer indicated that two cases had no intensely enhancing rim, whereas the other observer indicated that an intensely enhancing rim existed in all cases. The two cases in which the first observer noted no intensely enhancing rim were pT3 and pT4. In both cases, the tumors had invaded the entire circumference of the ureter and extended beyond the ureteral wall. Both observers noted a smooth, intensely enhancing rim in the same four cases: three pT1 tumors and one pT2 tumor. In the other eight cases, the first observer indicated that six had an irregular, disrupted, and fragmented intensely enhancing rim and that two had no intensely enhancing rim. The second observer indicated that all eight cases had an irregular, disrupted, or fragmented intensely enhancing rim. Of these eight cases, six were pT3 and two were pT4. Both observers indicated T2 or lower in the same four cases and T3 or T4 in the other eight cases, which was consistent with pT staging. Using the proposed MRI criteria, the observers diagnosed all cases correctly as to whether the tumor had invaded periureteral fat tissue (T3 or T4) or not (T2 or lower).


Discussion
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 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
References
 
Primary carcinoma of the ureter is rare, accounting for only 1% of all cancers of the upper urinary tract. When urothelial carcinoma of the urinary tract is found, it is essential to conduct a thorough investigation of the entire urinary tract for additional lesions. Determination of tumor extent is also important for therapeutic planning. The recent development of MDCT, especially CT urography, looks to be a promising approach in detecting wall thickening, masses, and filling defects because it has higher spatial resolution than single-detector CT [10, 11]. However, there has been little discussion about the usefulness of CT for determining local tumor extension or about the contrast resolution of CT in terms of accuracy for local tumor staging. In previous reports, researchers using single-detector CT discuss only morphologic changes to determine tumor extent, including wall thickening, filling defects, and periureteral stranding or streaking [1-6]. Periureteral stranding is a cause of false-positive findings for periureteral involvement because it can occur as a result of either tumor involvement or periureteral inflammatory change [6]. Caoili et al. [10] reported that CT urography using MDCT made it difficult to distinguish benign from malignant wall thickening. Because of the results of previous reports, we believe that using only morphologic changes to assess local tumor extent might be insufficient and may be the reason the accuracy of T staging based on CT in previous reports was limited.

Although the ureteral wall is normally thin and mildly enhancing after IV contrast administration, both on CT and MRI, our results showed that the wall at the site of the tumor was thicker and was intensely enhancing on contrast-enhanced MRI. Pathologic correlation showed that proliferating fibrous tissue made the ureteral wall thicker and intensely enhancing at the site of the tumor after IV administration of gadolinium. Consequently, the ureteral wall at the site of the tumor was seen as an intensely enhancing rim and became distinct from a tumor that was relatively less enhancing. To our knowledge, no previous reports about fibrous proliferation in response to ureteral carcinoma have been published in the literature.

Based on the results of the relationship between gadolinium-enhanced fat-suppressed T1-weighted images and pathologic findings, we propose using the MR T staging criteria with gadolinium-enhanced fat-suppressed T1-weighted images and evaluating not only morphologic changes, but also signal intensity changes. We believe that a major advantage of these criteria is the use of MR contrast resolution after IV contrast administration, which provides a signal intensity difference between a carcinoma and the surrounding tissues. To accurately determine the local extent of a carcinoma, we believe that it is important to conduct a detailed analysis of both morphologic changes and signal intensity changes with IV contrast material.

TCC is the most common type of ureteral carcinoma. SCC is the second most common type of tumor originating in the uroepithelium after TCC, but it is still relatively rare. Narumi et al. [12] reported that SCC had a predominantly extraluminal extension with invasion into adjacent organs. In our study, there were five patients with SCC; however, we observed no significant differences in findings or staging between cases of TCC and SCC.

One of the limitations of our study was spatial resolution. Voxel size in our study, when the field of view was 32 x 32 cm, was 1.3 x 1.7 x 8.0 mm. This spatial resolution might be relatively insufficient for evaluating ureteral lesions, and mild periureteral involvement could be misdiagnosed. Recently, parallel imaging techniques have been developed that can improve spatial resolution during the same acquisition time. Another limitation of this study is the small number of subjects. Because ureteral carcinoma is relatively rare, we used the same group of patients to develop and subsequently test the criteria for staging. As a result, the study design is not ideal. The number of subjects in previous reports is also relatively small, ranging from four to 31 cases with a mean of 11.8 cases; thus, the number of subjects in our study (n = 12) is average. A multiinstitution study, therefore, may be necessary to generate a larger number of subjects.


References
Top
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 References
 

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  6. Milestone B, Radecki PD, Friedman AC, Lev-Toaff AS, Seidmon EJ, Caroline DF. Staging of ureteral transitional cell carcinoma by CT and MRI. Urology 1990; 36:346 -349[CrossRef][Medline]
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  8. Weeks SM, Brown ED, Adamis MK, Eisenberg LB, Semelka RC. Transitional cell carcinoma of the upper urinary tract: staging by MRI. Abdom Imaging 1995;20 : 365-367[CrossRef][Medline]
  9. Greene FL, Balch CM, Fleming ID, et al. AJCC cancer staging manual, 6th ed. New York, NY: Springer,2002 : 329-334
  10. Caoili EM, Cohan RH, Korobkin M, et al. Urinary tract abnormalities: initial experience with multi-detector row CT urography. Radiology 2002;222 : 353-360[Abstract/Free Full Text]
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