Radiol Oncol 2005; 39(1): 23-35. review The MR imaging as a one-way shopping tool for detecting and staging renal tumours Galina Kirova Department of Radiology, University Hospital Lozenetz, Sofia, Bulgaria Background. Magnetic resonance imaging is one of the most attractive approaches: the technology is wide-ly available, it is not associated with the exposure to ionizing radiation, and does not require the injection of iodinated contrast agent. High-field strength clinical magnets, high-performance gradient hardware, and ul-trafast pulse sequence technology are rapidly making the vision of a comprehensive »one-stop shop« uro-logic MR imaging examination a reality. Conclusions. Difficulties that remain are related to the variable protocols of the examination and, therefore, it is mandatory to standardize as much as possible the techniques that are used in order to obtain repro-ducible information. Key words: kidney neoplasms - diagnosis; magnetic resonance imaging; neoplasms staging Introduction Since the only successful curative treatment of renal tumours is surgery, accurate radio-logical information is crucial during the initial tumour staging for an optimal operative plan-ning. The preoperative assessment of renal carcinoma includes tumour size, tumour ex-tent, in particular capsule invasion with tu-mour spread to perinephric fat with or with-out direct invasion of adjacent organs outside Received 5 July 2004 Accepted 10 September 2004 Correspondence to: Galina Kirova, MD. PhD, Department of Radiology, University Hospital Lozenetz, 1 Koziak st, 1407 Sofia, Bulgaria; Phone: +359 888 401 678; E-mail: kirovag@yahoo.com Gerota’s fascia, regional lymph node metasta-sis, venous tumour thrombosis, and distant metastases.1 Intravenous urography, angiog-raphy and ultrasound have been the main in-vestigations for a long period of time. All these methods are complementary and each has advantages and disadvantages. None of these single methods are sufficient for the evaluation of all aspects involved in oncolog-ic urologic pathology. Nowadays the prether-apeutic planning of renal carcinoma has dra-matically improved in the use of cross-sec-tional imaging, in particular CT and MRI. Magnetic resonance imaging is one of the most attractive approaches: the technology is widely available, it is not associated with the exposure to ionizing radiation, and does not require the injection of iodinated contrast agent.2 24 Kirova G / MR imaging and renal tumours In recent years a number of reports on dynamic MRI have evaluated renal functioning and morphological changes. Dynamic MRI has proven able to integrate renal scintigra-phy in documenting functional impairment and to supplement the information acquired by other imaging techniques on the morphol-ogy of the kidney.3 Stimulated by the philos-ophy and results of the all-in-one examina-tion for pancreatic neoplastic disease, Verswijvel et al invade a similar approach for the evaluation of urologic disease. Cross-sec-tional sequences, MR angiography in the ar-terial and venous phase, evaluation of the re-nal parenchymal and lesional perfusion, and contrast-enhanced MR urography were com-bined in one imaging session.4 The method gained a widespread acceptance as a standard for patients in which several conven- tional complementary modalities must be performed and is fairly well illustrated for pa-tients with neoplasms of the renal parenchy-ma or urothelium. The aim of the paper is to describe an all-in-one approach protocol for MR examination of patients with suspected or proved renal tu-mours in order to achieve all necessary pre-operative (pretreatment) information. Some explications of the possibilities and clinical usefulness of each one MR series will be done. Paramagnetic contrast materials Advances in the application of MRI in kid-ney’s pathology depend predominantly on the use of magnetic resonance contrast Table 1. Example of order of the sequences for an all-in-one approach protocol 1. AX T1 WI 2. AX T2 FSE WI 3. COR T2 FSE WI double echo half-Fourier acquisition single-shot turbo spin echo + FAT SAT + IN/OUT Phase T1 4. Furosemide+Gd (Gd-DTPA 0,2mmol/kg body weight, injection rate 2,5ml/s and Furosemide 0,1mg/kg body weight) Breath-hold 3D gradient echo MRA Breath-hold 3D gradient echo MRU 5. Postprocessing Table 2. Parameters of the MR sequences (for GE 1.5T Signa). Phased-array torso coil. (TE-echo time, TR-repetition time, FA-flip angle, ST-slice thickness, FOV-field of view) Pulse sequence TR(ms) TE(ms) FA(’) ST(mm) FOV(mm) Matrix(mm) orientation Scan time COR T2 SSFSF 2300 80 - 8 36 256/256 coronal 48s COR T2 SSFSE 1300 200 - 3 36 256/160 obl 16s AX T1 BH dual 160 2,2/4,4 80 8 36 256/128 axial 33s echo AX T2 FRFSE 3000 85 - 8 36 256/256 axial 4,07min AX 3D SPGR 4,6 1,8 15 5 36 256/160 axial 20sec/phase Dyn+CM URO COR 3D SPGR 150 6 80 8 36 256/128 coronal 20s Radiol Oncol 2005; 39(1): 23-35. Kirova G / MR imaging and renal tumours 25 agents to enhance both parenchyma and tu-mours. The most widely used contrast agents are chelates of gadolinium (Gd). Its chemical structure comprises a Gd-ion with a triple positive charge combined with a DTPA derivate, forming a very stable complex. The strongly paramagnetic gadolinium has sever-al effects. It can change (relax) the magnetic state of hydrogen atoms in water molecules; this markedly changes the appearance of tis-sues, with a high contrast agent uptake in T1-weighted images, causing tissues to appear bright. High concentrations of gadolinium chelates can also induce local changes in the magnetic field (magnetic susceptibility). This is most apparent during the first pass of a bo-lus of contrast agent after the rapid intra-venous injection. On gradient echo T2*-weighted images, this effect is apparent as a darkening of the image in well-perfused areas of tissue. Gadolinium-DTPA is eliminated rapidly and completely by the renal excretion with-out tubular reabsorbtion. The half-time of Gd-DTPA in blood is 90 minutes. More than ~ 91% of the administrated dose is eliminated after 24 hours. The elimination depends only upon the glomerular filtration rate. The renal insufficiency is not a contraindication for the contrast material administration. The recommended contrast dosage for magnetic resonance imaging of the kidneys is 0.1 mmol Gd-DTPA/kg BW. The administration of contrast material should be mechani-cal with the use of automatic injector after the correct timing of the bolus injection in order to synchronize the moment of the peak renal artery enhancement with the acquisition of central k-space data.5 The intravenous administration of an ex-tracellular paramagnetic contrast material provides a means for imaging the circulation. Dynamic measurements, in which the uptake and washout of contrast in tissues is moni-tored with time, can assist in the diagnosis and can provide information on vascular per- meability and perfusion, by quantifying and analyzing image intensity changes, and fit-ting these to analytical or model functions. Dynamic information shows the rate at which tissue enhances, and subsequently the rate at which contrast agent washes out. This de-pends on the delivery of the agent (perfusion), the ability of the agent to leak out of the vasculature (vascular permeability), and the extracellular volume. Usually, a region of in-terest (ROI) is selected within the tumour, and the software that is provided with the magnetic resonance scanner is used to evalu-ate the change in signal intensity with time in that ROI. Technique of MR imaging of the kidneys Patient positioning and coils The patient is examined in supine position with both arms lying flat against the body, us-ing a phased-array torso coil to optimize sig-nal-to-noise ratio. Prior the examination pa-tients would be informed about the necessity of breath-holding in some sequences. Field strength Presently recommended systems for the performance of MRI of the kidneys with contrast material have the field strength of 0.5 to 1.5T and most published studies using fast GE se-quences have been performed on higher field strength systems. The advantage is that the paramagnetic contrast material has a greater effect on the signal due to the increased T1 relaxation time of enhancing tissues at higher field strengths. At the same time the high-field strength machines allow to perform fast techniques, required for the angiographic and dynamic studies. Radiol Oncol 2005; 39(1): 23-35. 26 Kirova G / MR imaging and renal tumours Imaging protocol The imaging protocol should be designed for the evaluation of the kidney and the entire upper urinary tract and should include unen-hanced and enhanced phases. Morphological assessment The imaging protocol for renal tumour stag-ing should include conventional or fast-spin echo sequences in axial and coronal projec-tions for assessing the morphology of both kidney and tumour parenchyma.6 T2-weighted sequences In T2-weighted sequences, hydrous or oede-matous structures emit an intense signal. Spin-echo (SE) or fast-spin-echo (FSE) se-quences are the T2-weighted sequences most commonly used in MR imaging of the abdomen. COR T2 weighted images using the half-Fourier acquisition single-shot turbo spin echo technique permits in a very short exam-ination time to visualize kidneys, ureters and urinary bladder, giving the possibility for the rough orientation. Usually they are acquired before performing contrast enhanced dynamic measurements (Figures 1, 2a, 2b, 2c). T2-weighted images are useful in recogniz-ing small cysts only a few millimetres in diameter with high sensitivity.7 This is an ad-vantage of MR imaging compared with the CT, where the partial volume effect leads to confusion in such kind lesion characteriza-tion. T1-weighted images The axial T1WI focused at the kidney gives an excellent T1 contrast independent of patient breathing. If »bright« spots (hyperintense lesions in T1) are detected, breath-hold T1 fat suppressed gradient echo pulse sequences should Radiol Oncol 2005; 39(1): 23-35. be obtained to exclude or confirm the pres-ence of fat lesion. This technique is especial-ly useful in cases of the suspected intratu-moural haemorrhage or fat-containing le-sions.8 Chemical shift can be used as a tool for delin-eating structures that are surrounded by fat. Out-of phase images can aid in the demarca-tion of the renal contour, the margin of the adrenal glands, and the liver edge. Gradientecho images that use out-of phase chemical shift demonstrate dark lines around organs embedded in fat. Those dark lines are created by the phase cancellation of the fat and water signals that exist within the voxels of the lipid-water interface. The width of the dark lines can be accentuated by increasing the field of view. The use of a narrower band-width will also increase the chemical sift banding seen on the images (Figures 3a, 3b, 3c).9 Chemical shift MR imaging has become a popular technique for diagnosing adrenal adenomas. Benign adrenal adenomas, which are typically composed of approximately 16% lipid based on in vivo studies,10 can demon- Figure 1. COR T2WI of a female patient with transi-tional cell renal cancer (arrow) of the left kidney. Note high-intensity bilobulated mass, obstructing the pelvi-caliceal system of the kidney. Kirova G / MR imaging and renal tumours 27 strate measurable differences in signal inten-sity when their appearance on in-phase gradient-echo images is compared with that on the Figures 2a, 2b, 2c. 2WI (a), T1WI (b) and contrast en-hanced T1WI (c) in a patient with relapsing Wilm’s tu-mour demonstrating definite spread into the perirenal space (arrow). The structure of the tumour is nonho-mogeniuos, highly vascularized with large areas of necrosis. Figures 3a, 3b, 3c. COR and Ax T2WI of a 34 years old man with renal cancer demonstrate round high-inten-sity renal tumour, protruding the renal contours and invading the perirenal space (arrow in a and b). AX out-of phase T1 image of the same patient shows a mass invading into the inferior aspect of the liver, as evidenced by the interruption of the dark cortical line (arrow in c.) that demarcates the liver margin (c). Radiol Oncol 2005; 39(1): 23-35. 28 Kirova G / MR imaging and renal tumours out-of-phase counterparts. A decrease in the signal intensity of greater than 20% within an adrenal mass on out-of-phase images helps to confirm the diagnosis of an adrenal adeno-ma.11 Adrenal metastases, on the other hand, typically do not contain any significant lipid elements and will not demonstrate an appre-ciable change in the signal intensity with inphase and out-of-phase chemical shift imag-ing (Figures 4a, 4b). Combined morphological and functional assessment Contrast-enhanced MRI Multi-phase breath-hold 3D volume acquisi-tion is the technique of choice for evaluating renal vessels and dynamic changes in renal parenchyma.12,13 Two technical developments are essential to the successful use of fast 3D MR sequence: the availability of high-performance gradient systems as well as dedicated surface coils. The implementation of high-performance gradient has enabled the acquisition of complex 3D sets with ultrashort repetition (TR) and echo (TE) times within a comfortable breath-hold period. The ultrashort TR in conjunction with a relatively high flip angle minimizes the signal of all abdominal tissues. Against this background, structures containing T1-short-ening contrast agents can be made selectively visible.14 In the 3D technique, the entire part of the body is exited as a volume. This volume can be divided into the so-called partitions, or slices of variable thickness, in any desired plane. 3D imaging allows the depiction of thin slices without gaps in a defined slice profile. Generally a volume block of 150mm with, for example, 30 partitions is used for an examination with axial angulation. The re-sulting slice thickness is 5mm. The coronal angulation permits the use of a rectangular FOV. The resulting time gain allows the ac-quisition of a greater number of partitions, optimizing the spatial resolution. For the purpose of tumor staging MRA is performed in the axial plane, with the top of the volume at the diaphragmatic level and the base below the level of lower renal poles. The volume should extend posteriorly to encom-pass both kidneys. This large field of view combined with an acquisition matrix of 512 Figures 4a, 4b. AX in-phase (a) and out-of phase (b) T1 images of a 56-years-old man with metastatic clear cell re-nal carcinoma in the left adrenal glad. No differences in signal are seen on the two images. Metastases generally do not contain fat and do not exhibit the signal loss by chemical shift effects. Radiol Oncol 2005; 39(1): 23-35. Kirova G / MR imaging and renal tumours 29 in frequency and 128-256 in phase-encoding direction is typically used. The use of multiphase sequence gives the possibility to repeat the series from three to ten times, depending on the suspected pathology.5 Angiography for preoperative arterial and venous mapping The determination of the extent of intra-venous tumour growth is of paramount im-portance, since it affects the operative ap-proach in many cases. Venous involvement is one of the cornerstones of the surgical plan-ning in renal tumours. A few studies have re-ported the usefulness of MR angiography in the preoperative assessment of venous in-volvement in patient with renal cell carcino-ma, as well in tumour characterization. In the study of J.P. Laissay et al venous diameter en-largement was the hallmark of tumour thrombus, with a sensitivity of 84% and a specifici-ty of 94%. At the same time the use of Gd-en-hanced imaging improved the diagnostic yield of morphological data by additional information upon the thrombus enhancement (Figures 5, 6, 7a, 7b).15 Serial MR imaging for evaluation of renal parenchyma and tumour vascularity Regarding the functional evaluation, the ki-netics of gadolinium chelates during passage through the kidneys has been described in many reports. In the normal kidney four phases can be distinguished in the transit of the paramagnetic contrast agent through the parenchyma: the cortical, corticomedullary, medullary and excretory phases. For these reasons, the generally accepted guidelines re-quire that dynamic measurements (at least five measurements after CM administration) have a temporal resolution of 20-25sec per se-quence. This makes possible the discrimina-tion between pathological processes and sur-rounding parenchyma, as well as the acquisi- Figure 5. MR angiography in the arterial phase demonstrating gradual compression of the right exter-nal iliac artery from enlarged parailiac lymph nodes (arrow). Figure 6. Parasagital T1 contrast-enhanced image of a retroperitoneal tumour in a 17 years-old male showing compression of the vena cava (arrow) and upper right renal pole (punctuate arrow) without invading or ob-structing the vein. tion of a sufficiently accurate dynamic curve. Researches in this field have established the way in which changes in the kinetics of the Radiol Oncol 2005; 39(1): 23-35. 30 Kirova G / MR imaging and renal tumours Figures 7a, 7b. Postcontrast MR imaging of a patient with large left renal cell carcinoma with thrombus within the left renal vein and IVC. Ax image shows thrombus within IVC (arrow in a.) resulting in a filling defect. Reconstructive image in coronal plane in the same patient shows the large thrombus extending in-to the vena cava up to the level of hepatic veins (punc-tuate arrow in b.). contrast agents in the kidney reflect alterations in the renal function.16-19 Administration of gadolinium compounds is not con-traindicated in patients with the impaired re-nal function, and it is therefore possible to study renal perfusion and excretion in pa-tients with a chronic renal failure by dynamic MRI.20 Radiol Oncol 2005; 39(1): 23-35. Assessing the corticomedullary phase alone may result in clinically significant er-rors, since small hypovascular tumours of the renal medulla may be missed since they are not sufficiently enhanced and hypervascular cortical renal cell carcinomas may enhance to the same degree as the normal cortex. During the early nephrographic phase inhomoge-neous enhancement of the medulla may be also misinterpreted as a mass lesion. This arti-fact disappears later in the nephrographic phase.21 Advantages of the corticomedullary phase include the differentiation of the normal variants of renal parenchyma from renal masses and the better depiction of tumour hypervascularity improving the characteriza-tion of solid renal mass lesions.22 The nephrographic phase is considered the optimal phase for the detection and charac-terization of renal masses, in particular of small renal masses, providing both homoge-neous enhancement of cortex and medulla and lesion enhancement (Figures 8a, 8b). In principle, it is possible to perform MRI examinations at any angulation. For dynamic MRU, the coronal slice orientation is general-ly preferred. The main advantage of the coro-nal slice orientation is that it permits the se-lection of a rectangular FOV, which makes to allow the reduction of the slice thickness and the optimization of the spatial resolution to 2mm. The disadvantages are that the whole ~ volume of the slab is reduced and it is not al-ways possible to visualize the whole abdomen. This is very important in cases of abundant collateral vessels (after CVI throm-bosis) or in cases of tumour staging, when the condition of the liver is crucial. The axial slice orientation is that it makes a good assessment of the whole abdomen, which is of great importance in case of onco-logic disease. The sagittal and parasagittal orientation is not routinely recommended for use. They are, however, employed in the examination of pyelo-ureteral junction pathology and ob- Kirova G / MR imaging and renal tumours 31 Figures 8a, 8b. Angiographic phase in a patient with relapsed Wilm’s tumour (the same patient as in pic-ture 2) showing a strengthed and displaced right renal artery (arrow in a.). Axial image of the same patient in the parenchymal phase, demonstrating the possibility of comparing the signal intensity levels in different tumor levels and the spared part of the kidney (b). tained for each individual excretory system having the major advantage of data acquisi-tion of nearly isovolumetric voxels. This is due to the fact that the effective slice thick-ness can significantly be reduced which in-creases the image resolution both in the na-tive and MIP images. MRU for evaluation of collecting system The term MRU is used for a MR examination which combines different techniques for vi-sualizing the urinary tract.23 This can be per-formed with the so-called heavy T2 tech-niques receiving a signal from fluid-field structures or at the end of contrast-enhanced MR of the kidneys.24,25 Later the collecting system and the ureters are visualized during the excretory phase as reformatted 3D images. MRU in the excretory phase provides the volume scanning of the kidney and the upper urinary tract within one breath hold. The visualization of the renal collecting system and ureter is significantly improved due to the avoidance of respiratory data misregis-tration improved resolution and data sets suitable for 2D and 3D reconstructions. The multiplanar reformation creates images simi-lar in appearance to IVU. For this purpose the measurement volume should extend as far posteriorly as possible to encompass the pelvic segment of the ureters and anteriorly to encompass the anterior bladder wall. The top of the coronal volume should be set above the upper pole of the kidneys at the one end and just inferior of the bladder base at the other. In particular cases sagitally oriented images for each kidney could be performed using smaller field of view, reduced effective slice thickness and respective generating, more detailed images. The latter is obtained for each individual excretory system and has the major advantage of data acquisition of nearly isovolumetric voxels, which has a major benefit in the MIP images. The lumen, the wall, the structures adja-cent to the collecting system and ureter as well as the contrast enhancement are assessed on axial and MPR views. When pathology is depicted on axial images the re-formatted images are of additional diagnostic value to the axial ones being not only a means to present an abnormality in an easily under-standable manner. MRU has the potential to Radiol Oncol 2005; 39(1): 23-35. 32 Kirova G / MR imaging and renal tumours become a primary investigation in the evaluation on the upper urinary tract; however, its sensitivity for the diagnosis of subtle urothe-lial lesions is unknown and needs to be eval-uated by clinical validation studies (Figures 9, 10). The evaluation of the images could be done on the original images (a), or on the edited MIP images (b) (Figures 11a, 11b, 11c). Figure 9. Late pyelographic phase in the patient with relapsing Wilm’s tumour showing the invasion of the collecting system and the level of displacement. Figure 10. Picture in the late pyelographic phase in the patient with retroperitoneal tumour and the caudal displacement of the pelvi-caliceal system. Figures 11a, 11b, 11c. Coronal and axial images in a patient with left renal cell carcinoma and retroperi-toneal lymph nodes, leading to an obstruction of the right pyelo-ureteral system (arrow in a). Note the necrotic parailiac lymph node on the right side (arrow in b). Edited maximum intensity projection (MIP) of the MR urogram of the same patient (c). Radiol Oncol 2005; 39(1): 23-35. Kirova G / MR imaging and renal tumours 33 Post processing Postprocedure processing of the MRA and MRU data could be supplementary obtained by means of a maximum intensity projection algorithm. MIP technique yields a three-di-mensional comprehensive view of both kid-neys and their vessels. Based on post processed subtraction images in which only image pixels having at least a certain signal intensity are taken into account (threshold value algorithm), the representation of image information gives the impression of a real 3-dimensional angiographic or urographic views.26 The resultant MIP images with sub-traction techniques allow the adequate visu-alization of the renal vessels - renal arteries, renal veins and inferior vena cava. This form of imaging allows a simpler spatial orienta-tion and is especially suitable for the presen-tation of suspicious findings. MPR images allow the three-dimensional view of partial volumes within the abdomen. These are also based on postprocessed sub-traction images. In special cases, these clarify the topographic relationship between a suspi-cious lesion and defined anatomical struc-tures. 3D imaging of tumours using VRT and 3D data sets allow the ascertainment of the size (T1 and T2 staging) and the precise location of the tumour within the kidney as well of relation to the major vessels and the renal col-lecting system. This influences the decision as to whether nephron-sparing surgery can be performed. In case of tumour resection, the depth of incision can be calculated, the con-servation of normal renal parenchyma is en-sured and complications are minimized.27,28 In case of tumoural lesion, the time-re-solved perfusion of the cortex of the lesion could be compared in a curve to the perfusion of the normal cortical parenchyma of the same kidney. Conclusions The concept of a comprehensive imaging evaluation has been an evolving theme dur-ing the past decade, with the vision of a com-plete examination that could be performed in a relatively short time. Advances in the rapid MRI technology and its application to oncolo-gy imaging have shown that MRI has a tremendous potential for the evaluation of re-nal tumours and renal disease in general. A comprehensive MR examination including CE 3D MRA, MRU and MR nephrogram offers several potential advantages compared with conventional X-ray studies. By combin-ing all three techniques into an all in one pro-tocol the same information can be obtained as with conventional studies; however, the patient convenience will be improved, the potential morbidity is lower and the substantial costs decrease. The use of contrast-enhanced dynamically collected multiplanar acquisi-tions permits local, lymph node, and hepatic staging, all within the same examination. At the same time the use of Gadolinium chelates are considered to be safe and can be per-formed in patients with the impaired renal function. The combination of different MR tech-niques in one examination with the simulta-neous morphologic and functional analysis appears to be the »Holly Grail« of Magnetic Resonance Imaging. Such kind of technique has several advantages: 1. The duration of the combined MR exami-nation is approximately 30-40min. 2. The all-in one approach examination based on MR imaging provides the good visuali-zation of the renal parenchyma, the renal vascular supply and the collecting system, irrespective of the renal function. 3. The combination of nonenhanced and en-hanced MRU gives the possibility of the evaluation of both dilated and nondilated collecting systems. 4. 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