6655Revista Românæ de Urologie

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eePrivire de ansamblu asupra tehnicilor øi semiologieiIRM øi uro-RM ale tractului urinar superior

în carcinoamele uroteliale

Ioana G. Lupescu, Cristina Nicolae, R. Al. Capsa, I.Sinescu1, R. Hinaut2, N. Al. Câmpeanu3

Department of Radiology and Imaging, Fundeni Clinical Institute, Bucharest1Department of Urology Hemodialysis and Renal Transplantation, Fundeni Clinical

Institute, Bucharest2 Service de Radiologie et Imagerie Medicale-Centre Hospitalier Lagny Marne La Vallee3 UMF Carol Davila, Radiologie Fundeni /Service de Radiologie et Imagerie

Medicale, Centre Hospitalier Lagny Marne La Vallee

Corespondenflæ: Dr. Ioana G. LupescuDepartment of Radiology and ImagingFundeni Clinical Institute, BucharestE-mail: ilupescu@gmail.com

Abstract

The purpose of this article is to present the MRI technique and also the current and particular MR aspects of the upperurinary tract carcinomas. Specific MR techniques for suspected upper tract urothelial carcinomas are coronal T2-weighted hydrographic and coronal gadolinium-enhanced T1- weighted 3D-spoiled gradient-recalled echo innephrographic and pyelographic phases. Upper tract urothelial carcinomas can be classified into papillary tumor, flattumor, and infiltrative tumor. Papillary lesions appear as filling defects of soft tissue signal on T2-weightedhydrographic (MR urography) and T1-weighted pyelographic phase images. On nephrographic phase images, thelesions show moderately homogeneous enhancement. Flat tumors appear as a segmental area of diffuse thickeningand enhancement of the affected urinary tract wall on nephrographic phase images. Infiltrative tumor appears as alarge heterogeneously enhancing mass.

MRI, with MR urography sequences, represents actually an optimal and totally noninvasive imaging method toevaluate carcinomas of the upper urinary tract.

Key words: MRI. MR urography. Upper tract urothelial carcinomas.

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IntroductionMagnetic resonance imaging (MRI) is a useful tool

for the characterization and presurgical staging ofrenal masses. Transitional cell carcinomas (TCC) of theupper tract accounts for 5% of all urothelial carcinomasand 10% of renal tumors (1,2). Patients with a history ofupper or lower tract urothelial carcinoma are at highrisk of developing synchronous or metachronousurothelial carcinoma in the upper tract (1). Patientswith history of urothelial carcinoma and patients withhematuria, require imaging evaluation of the urinarytract (3, 4, 5, 6). MRI and MR urography (MRU) arealternative noninvasive methods for CT urography inthe evaluation of upper tract urothelial carcinoma,especially when the patient has a contraindication toiodinated contrast material (7,8,9). In this article, wedescribe the technique of MRI evaluation for detectingupper tract urothelial carcinoma and screening ofhigh-risk populations. We illustrate also the differentMRI findings of upper tract tumors, differentialdiagnoses, and pitfalls.

IndicationsThe urinary tract is depicted using MR urography

entirely, including the complete ureters and ureterove-sical junctions. Multiplanar MRI is indicate for suspec-ted upper tract urothelial carcinomas, in patients athigh risk (hematuria, history of urothelial carcinoma, orabnormal urine cytology) or to evaluate and characte-rize other imaging findings such as hydronephrosis orsoft tissue in the urinary tract on unenhanced CT orultrasound (3,4, 9,10). MRI and MRU are recommendedin patients with contraindication for CTU or excretoryurography (history of previous reaction to iodinatedcontrast material or renal insufficiency. Also MRI isindicated in pediatric population.

MRI protocolMR imaging examinations are performed with a

phased-array body coil with the patient in supine posi-tion. Our standard imaging MRI protocol, performedon 1.5-T systems, include coronal half-Fourier single-shot fast (or turbo) spin-echo images (SSFSE: short andlong TE- Fig. 1), axial dual-echo in-phase and opposed-phase gradient-echo (GRE) T1-weighted images, andcoronal three-dimensional (3D) fat-suppressed GRE T1-weighted images obtained following the intravenousadministration of contrast material. The best sequen-

ces to evaluate the urinary tract are coronal T2-weigh-ted hydrographic sequences. obtained using thin-sliceor thick-slab coronal single-shot fast spin-echo similarto the sequences used in MR cholangiopancreato-graphy (7). Respiratory triggered T2-weighted was alsoused. Coronal gadolinium-enhanced T1-weighted 3D-spoiled gradient-recalled echo (GRE) in nephrographic(Fig. 2) and pyelographic (Fig. 3) phases with ivcontrast agent were used to better delineate thetumor infiltration and enhancement characteristics (8).A 10 mg dose of furosemide was given intravenouslyto achieve distention of urinary tract and dilution ofgadolinium contrast material to avoid T2* artifact. Theoptimal time window for MR imaging after furosemidewas between 5 and 20 min.

Fig. 1 T2 weighted MR-urography. ssFSE short TE (a) and long TE (b).Left hydronephrosis in a case of transitional cell

carcinoma-papillary form (arrows).

Fig. 2 T1 weighted afterGadolinium injection-nephrographic phase.Left hydronephrosis in

a case of transitional cell carcinoma-flat tumoralform- of the uretero-pyelicjunction (arrows)

Fig. 3 T1 weighted afterGadolinium injection-pyelographic phase- fillingdefect into the pyelic region(arrow)

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Staging of urothelial carcinomaThe classification applies only for carcinoma (Table

I). Anatomical sites are the renal plvis and the ureter.Regional lymph nodes are the hilar, para-/peri-/preaor-tic, interaortocaval, retrocaval and retroaortic nodes,and for the ureter, intrapelvic nodes. Laterality doesnot affect the N classification (11).

TN ClassificationTx – Primary tumor cannot be assessedT0 – No evidence of primary tumorTa – Noninvasive papillary carcinomaTis – Carcinoma in situ

Table I. T (Tumor) staging of transitional cell carcinoma

T (tumor) InvasionT1 INVASION OF SUBEPITHELIAL CONNECTIVE TISSUET2 INVASION OF MUSCULARIST3 INVASION THRU MUSCULARIS INTO

– PERIPELVIC FAT OR KIDNEY PARENCHYMA BY PELVIC LESION

– INVASION OF PERIURETERIC FAT BY URETERAL LESION

T4 INVASION INTO PERINEPHRIC FAT OR ADJACENT ORGANS

N – Regional lymph nodesNx – regional lymph nodes cannot be assessedN0 –no regional lymph node metastasisN1 –metastasis in a single lymph node 2 cm or less in

greatest dimensionN2 –metastasis in a single lymph node more than 2 cm

but not more than 5 cm in greatest dimension, ormultiple lymph node, none more than 5 cm ingreatest dimension

N3 –Metastasis in a lymph node more than 5 cm ingreatest dimension

MRI appearances of upper tract urothelialcarcinomas. Imaging interpretation

A papillary lesion appears as a small filling defect ofsoft tissue signal on T2-weighted hydrographic imagesand pyelographic phase images. On nephrographicphase images, the lesion shows homogeneous enhan-cement, which is essential for differentiating fromother causes of filling defects. Flat tumor grows alongthe surface of urothelium without forming a papillarynodule.

Gadolinium-enhanced nephrographic and pyelo-graphic phase images are the most important sequen-

ces of MRI for detection of small urothelial carcinomas.Small urothelial carcinomas appear as focal areas ofenhancement on nephrographic phase images andfocal filling defects on pyelographic phase images.According to the appearances of upper tract urothelialcarcinoma, differential diagnoses of MRU findings canbe categorized into three patterns: (1) filling defect(Fig. 4) or focal enhancing lesion, (2) diffuseenhancement or thickening of the urinary tract wall(Fig. 5), and (3) infiltrative mass (Fig. 6).

Fig. 4 Papillary tumor type ofTCC : mass (arrows) in the right renal collectingsystem- T2 weighted (a,b), T1 weighted after Gd innephrographic phase (c) and pyelographic phase (d,e)

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Differential diagnosesPapillary urothelial carcinoma should be differen-

tiate from other causes of filling defects, including po-lyp, stone, blood clot or debris, fungus ball, sloughedpapilla, and gas. Flow-related artifact is often seen onT2-weighted hydrographic images. Blood vessels mayalso appear as a filling defect.

Diffuse thickening or enhancement of the urinarytract wall of urothelial carcinoma should be differen-tiate from inflammatory changes, recent instrumenta-tion, presence of a ureteral stent, reflux, artifact due tobreathing motion or ureteral peristalsis.

Infiltrative mass of urothelial carcinoma should bedifferentiate lymphoma, renal cell carcinoma, otherneoplasms, inflammatory mass.

DiscussionDiagnosis of urothelial carcinoma requires imaging

evaluation of the entire urothelium. Between 30% and75% of patients with urothelial carcinoma of the uppertract will have synchronous bladder tumors (15) and2% to 4% of patients with bladder TCC will have synch-ronous upper tract disease (Fig. 7). Transitional cellcarcinoma tend to be multicentric (Fig. 8) and bilateralwith synchronous or metachronous tumors (Fig. 9).

Fig. 5 Flat tumor type of TCC: focal thickening involving the uretero-pyelic junction- T2W MR urography (a)

and T1W after Gd injection nephrographic phase

Fig. 6 Infiltrative masstype of TCC located into

the left renal collectingsystem with extension

into the adjacent renalparenchyma- T1w

after Gd injection innephrographic

phase (a,b) andin pyelographic

phase (c.d).

Fig. 7 Synchronous tumors- TCC papillary form of the urinary bladder and the pelvic left ureters- T2 w image

Fig. 8 Multiple filling defects of the left ureter using a T2w MRurography- TCC papillary form

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Imaging evaluation of suspected upper urinarytract TCC was initially performed with intravenous uro-graphy and retrograde pyelography, both with a verygood spatial resolution for detection of small urothelialabnormalities. In our days cross-sectional imaging mo-dalities are used to detect TCC of the upper tracts. Themost common MRI techniques used to display the uri-nary tract can be divided into two categories: (a) static-fluid MR urography (also known as static MR urogra-phy, T2-weighted MR urography, or MR hydrography),and (b) excretory MR urography (also known as T1-weighted MR urography). Heavily T2-W MR hydro-graphy can evaluate dilated collecting systems even inthe absence of renal function. Additionally, MRI canstage upper tract TCC by showing distant metastasesor tumor involvement of the renal parenchyma, peri-nephric fat, or periureteral fat. More than 40% of casesof carcinoma of the transitional cell epithelium arise inthe renal pelvis; they account for 8% of all renal tumors(9). Men are three times more frequently affected thanwomen (15). The transitional cell cancer of the renalpelvis infiltrates early into the renal parenchyma andinto the peripelvine tissue. The signal intensity of tran-sitional cell carcinomas is mainly isointense to the re-nal parenchyma on T1-weighted images and T2-weighted images. Transitional cell carcinomas of therenal pelvis or renal collecting system are generallyvisualized on MRU or on T2-WI as filling defects, with orwithout proximal hydronephrosis. TCC is hypointenseto urine on T2-WI. MRU with heavily T2- weightedimages after the administration of furosemide mayalso demonstrate narrowing of the ureters in case oftransitional cell carcinoma involvement. Contrast-en-hanced T1-weighted images often show a narrowing

of the ureter at the side of the tumor or a bulging of thetumor into the renal pelvis (12,13). Transitional cellcarcinomas of the renal pelvis and ureter must bedifferentiated from stones Transitional cell carcinomasare mainly hypovascularized and appear hypointensecompared to the kidney on postcotrast examination.which do not reveal any changes of the signal intensityafter Gadolinium injection, and from blood clots,which are rather hyperintense in T1w images (14,15).

Accuracy of MRI for detecting upper tract urothelial carcinoma

When the lesions are obstructive, MRU can detectupper tract urothelial carcinoma with an accuracy of96% or higher using gadolinium-enhanced pyelogra-phic phase or T2-weighted single-shot fast spin-echoMRU (9,12). The accuracy of MRI is probably similar orslightly inferior to that of multislice CTU (4). Extensionof tumor outside the wall of the urinary tract (T3)appears as an irregularity of the tumor border ordisruption of the intensely enhancing rim of theureteral wall on 2–3 min delayed T1-weighted images.However, MR has a limited role in accurately staginglow-volume tumor (Ta, T1, T2), which may be impor-tant in deciding the treatment option (nephrourete-rectomy versus endoscopic treatment). The maindrawbacks of MRU are lower spatial resolution, highersusceptibility to motion artifact, and lower accuracy fordetecting small urinary stones (15).

ConclusionMRI using MR urography can be a valuable means

of noninvasively assessing the urinary tract. Static-fluidand excretory MR urography can be combined withconventional MR imaging to provide a comprehensiveevaluation of the kidneys, ureters, bladder, vascula-ture, and soft tissues in patients with symptoms sug-gestive for transitional cell carcinoma of the uppertract. MR urography represents a good alternative forCT urography in the evaluation of upper tract, especial-ly in young population and when the patient has acontraindication to iodinated contrast agents.

References1. Hall MC, Womack S, Sagalowsky AI, Carmody T, Erickstad MD,

Roehrborn CG. Prognostic factors, recurrence, and survival intransitional cell carcinoma of the upper urinary tract: a 30-yearexperience in 252 patients. Urology 1998, 52:594–601

2. Kirkali Z, Tuzel E. Transitional cell carcinoma of the ureter and

Fig. 9 Synchronous tumors in a patients with history of urinary bladderurothelial carcinoma- filling defect into the right ureter lumen

and at the junction of the ureter and the neobladder.

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ee renal pelvis. Crit Rev Oncol Hematol 2003, 47:155–1693. Caoili EM, Cohan RH, Inampudi P et al. MDCT urography of upper

tract urothelial neoplasms. AJR Am J Roentgenol 2005,184:1873–1881

4. Fritz GA, Schoellnast H, Deutschmann HA, Quehenberger F,Tillich M. Multiphasic multidetector-row CT (MDCT) in detectionand staging of transitional cell carcinomas of the upper urinarytract. Eur Radiol 2006, 16:1244–1252

5. Szopinski K, Szopinska M, Borowka A, Jakubowski W. Magneticresonance urography: initial experience of a low-dose Gd-DTPA-enhanced technique. Eur Radiol 2000, 10:1158–1164

6. Hughes J, Jan W, Goodie J, Lund R, Rankin S () MR urography:evaluation of different techniques in nondilated tracts. Clin Radiol2002, 57:989–994

7. Leyendecker JR, Barnes CE, Zagoria RJ. MR urography: tech-niques and clinical applications. Radiographics 2008, 28:23–46

8. Ergen FB, Hussain HK, Carlos RC et al. 3D excretory MR urogra-phy: improved image quality with intravenous saline and diureticadministration. J Magn Reson Imaging 2007, 25:783–789

9. Takahashi N, Kawashima A, Glockner JF, Hartman RP, Kim B,King BF. MR urography for suspected upper tract urothelial carci-noma Eur Radiol 2009, 19: 912–923

10. Shokeir AA, El-Diasty T, Eassa Wet al. Diagnosis of noncalcareoushydronephrosis: role of magnetic resonance urography and non-contrast computed tomography. Urology 2004, 63:225–229

11. Wittekind C, Greene FL, Hutter RVP et al. TNM Atlas, 5th edition,Springer-Verlag 2005, 315-321.

12. Obuchi M, Ishigami K, Takahashi K et al. Gadolinium-enhancedfatsuppressed T1-weighted imaging for staging ureteral carcino-ma: correlation with histopathology. AJR Am J Roentgenol 2007,188:W256–W261

13. Obuchi M, Takahara T, Takahashi M et al. Breath-hold 3D MR uro-graphy with 2 ml Gd-DTPA injection. Nippon Igaku HoshasenGakkai Zasshi 1998, 58:163–165

14. Chahal R, Taylor K, Eardley I, Lloyd SN, Spencer JA. Patients athigh risk for upper tract urothelial cancer: evaluation of hydro-nephrosis using high resolution magnetic resonance urography. JUrol 2005, 174:478–482

15. Hamm B, Asbach P, Beyersdorff D, Hein P, Lemke U. UrogenitalImaging, Thieme, 2008, 124-126.

Rezumat

Obiectivul acestui articol este de a prezenta tehnica IRM precum si aspectele RM curente si particulare alecarcinoamelor cu localizare la nivelul cailor urinare superioare. Tehnicile RM specifice utilizate in evaluareacarcinoamelor uroteliale cuprind secventele ponderate T2, de tip hidrografic, in plan coronal si secventele 3D T1postinjectare de Gadolinium in faza nefrografica si pielografica, realizate in plan coronal. Carcinoamele tractuluiurinar superior pot fi clasificate in tumori papilare, tumori plate si tumori infiltrative. Leziunile papilare apar sub formade defecte de umplere (lacune) cu semnal tisular in secventele ponderate T2 tip urografie-RM si T1 in fazapielografica. Postcontrast, in faza nefrografica leziunile se incarca moderat si omogen. Tumorile plate apar sub formaunor ingrosari segmentare sau difuze cu incarcarea peretelui tractului urinar afectat in faza nefrografica. Tumorileinfiltrative apar sub forma de mase heterogene la examinarea postcontrast. IRM, cu secvente de urografia RM,reprezinta actualmente o metoda optima, total neinvaziva, pentru evaluarea carcinoamelor tractului urinar superior.

Cuvinte cheie: IRM, urografie MR, carcinoamele tractului urinar superior