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1
Department of Radiology, SS Annunziata Hospital, via Bruno, 74100 Taranto,
Italy.
2
Department of Nephrology, SS. Annunziata Hospital, 74100 Taranto, Italy.
3
Department of Radiology, University Hospital, Piazza Giulio Cesare, 70124
Bari, Italy.
Received August 16, 1999;
accepted after revision February 8, 2000.
Address correspondence to M. Scialpi, via Solito 83, 74100 Taranto, Italy
(michelescialpi{at}libero.it
).
Abstract
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MATERIALS AND METHODS. We retrospectively reviewed the MR imaging examinations of 35 patients (20 with renal cell carcinoma, eight with angiomyolipoma, and seven with complicated cysts) who were studied with spin-echo and dynamic fat-suppressed gradient-recalled echo MR sequences, before and after the administration of gadopentetate dimeglumine. Every 30 sec after contrast injection, we measured the lesion percentage of enhancement and the ratio of contrast (lesion—renal cortex signal intensity difference) to noise.
RESULTS. Ten renal cell carcinomas were classified as hypervascular (enhancement greater than that of renal cortex) and 10 as hypovascular. The percentage of enhancement of hypervascular carcinomas was similar to that of renal cortex until 150 sec and greater in the late sequences (180-210 sec, p < 0.01). Hypovascular carcinomas had a lower percentage of enhancement than hypervascular carcinomas (60-210 sec, p < 0.005). Angiomyolipomas, after an early enhancement peak, showed values similar to those of hypovascular carcinomas. Complicated cysts had very low enhancement (p < 0.001). The baseline contrast-to-noise ratio was negative for all lesions (hypointensity with respect to renal cortex). After gadolinium injection, the contrast-to-noise ratio of hypervascular carcinomas rose, becoming positive after 150 sec. Until 60 sec, the contrast-to-noise ratio of hypovascular carcinomas declined slightly, whereas that of angiomyolipomas and cysts fell sharply; then the three curves remained stable (60-210 sec, p < 0.05 for all matches except angiomyolipomas versus cysts).
CONCLUSION. Quantitative analysis of signal intensity variations during dynamic contrast-enhanced MR imaging with fat suppression can be useful in the characterization of small renal lesions.
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Conventional spin-echo MR imaging does not offer any advantage over CT in the evaluation of small renal masses; the spatial resolution of MR imaging is inferior, and inherent tissue relaxation parameters are not specific or are even misleading [2]. MR imaging with contrast enhancement and fat suppression has proven more sensitive in detecting and characterizing small renal lesions than unenhanced spin-echo sequences [3, 4]. Detection and characterization of small renal lesions has been further improved with breath-hold gradient-echo sequences (fast low-angle shot [FLASH]), before and after an IV bolus injection of a paramagnetic contrast agent (dynamic MR imaging), with enhancement resulting from vascularity of the lesion as a criterion[5,6,7].
We performed this study to evaluate the usefulness of dynamic gadolinium-enhanced MR imaging with fat suppression for the detection and characterization of small renal masses and the assessment of their vascularity.
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3.0 cm) renal lesion who had undergone an identical protocol of
conventional and dynamic contrast-enhanced fat-suppressed MR imaging. The 26
men and nine women had a mean age of 56.7 ± 15.2 years (range, 38-71
years). The size of the lesions ranged from 1 to 3 cm (mean, 2.44 ±
0.56 cm). The final diagnoses were renal cell carcinoma in 20 patients (16 clear cell, alveolar, or trabecular carcinomas and four papillary carcinomas) and benign lesions in 15 patients (eight angiomyolipomas and seven complicated cysts). Renal cell carcinomas had been diagnosed by histologic examination after surgery. Angiomyolipomas had been diagnosed on the basis of fat recognition on CT scans and an unchanged sonographic pattern after a 2-year follow-up in seven patients, and by histology after surgery in one equivocal case. All complicated benign cystic lesions had been diagnosed by examination of the aspirate after fine-needle aspiration, and all were confirmed after a 2-year sonographic follow-up that showed no lesion growth.
No patients had venous thrombosis, regional adenopathy, or distant metastases. No cases of oncocytoma, renal metastasis, focal nephritic lesion, or multiple carcinomas were involved in this study.
At time of the MR imaging, all 35 patients had normal overall renal function and symmetric kidneys; the 70 kidneys were free from medical or surgical disease, were of normal size, and were not obstructed.
MR Imaging Protocol
MR imaging was performed with a 1.0-T super-conducting unit (Impact;
Siemens, Erlangen, Germany). Scout turboFLASH images (TR/TE, 8.5/4.0 msec;
flip angle, 8°; inversion time, 500 msec) were acquired in the coronal
plane. A T1-weighted spin-echo sequence (600/15) and a T2-weighted spin-echo
sequence (2000/80) in the axial plane were initially performed. For both
sequences the matrix size was 192 x 256, the section thickness was 7 mm,
and the intersection gap was 1 mm. These sequences were followed by a
T1-weighted spoiled gradient-recalled echo sequence with FLASH and the
fat-suppression technique (120/6.5), with a flip angle of 70°, a matrix
size of 134 x 256, a section thickness of 8 mm, and an intersection gap
of 2 mm. This pulse sequence enabled us to acquire four sections in 16 sec
during a single breath-hold. The optimal imaging plane was selected with
either sagittal or coronal references to unenhanced T1- and T2-weighted
spin-echo imaging. When the tumor location could not be identified because of
a similarity of the signal intensity of the tumor and renal parenchyma (in
four patients with renal cell carcinoma), CT was used as a reference. In two
additional patients with renal cell carcinoma, respiratory motion artifacts
caused poor image quality on unenhanced T1- and T2-weighted spin-echo
sequences, and we also used CT as a reference.
A paramagnetic contrast agent, gadopentetate dimeglumine (Magnevist; Schering, Berlin, Germany), was administered to all patients as a bolus injection (0.1 mmol/kg of body weight injected in 5-8 sec) through a 22-gauge cannula, which was initially placed in the antecubital vein and which was attached through a long connecting tube to a 20-mL syringe to avoid changing the patient's position during the examination. Immediately after the injection of the contrast agent, the connecting tube was flushed with saline. T1-weighted gradient-recalled echo sequences with FLASH and fat suppression were obtained before and repeatedly after the injection of the contrast agent. Considering the start of the bolus injection to be the zero point, imaging was performed at 30, 60, 90, 120, 150, 180, and 210 sec.
MR Image Analysis
Images were separately interpreted by two radiologists and were reviewed by
consensus. On the basis of visual inspection, the signal intensity enhancement
on dynamic FLASH sequences was graded as either greater than, equal to, or
less than that of the normal renal parenchyma, and subsequently the lesions
were categorized as hypervascular or hypovascular (avascular).
Quantitative Analysis and Calculations
All MR images were transferred from hard copy to a satellite console
(SIENET Magic View 1000; Siemens). The signal intensities of the lesion and of
the cortex and medulla were measured in operator-defined circular regions of
interest placed manually over the lesion, the cortex, and the medulla of the
kidney on unenhanced T1-weighted gradient-recalled echo images and on dynamic
gadolinium-enhanced gradient-recalled echo images obtained at each imaging
time. The region-of-interest size of the lesion was large enough to encompass
a representative area of the mass without being so large as to lead to
spurious values because of volume averaging with adjacent normal renal
parenchyma. The time of measurements on regions of interest for each patient
was approximately 10 min. Background noise was measured in the phase-encoding
direction.
We calculated two parameters for each lesion. First, we calculated the percentage of enhancement of signal intensity after the administration of gadolinium with respect to the value on unenhanced images, as follows: percentage of enhancement = (SIpost-SIpre) / SIprex(STDnoisepre/STDnoisepost), where SI stands for signal intensity, STDnoise for standard deviation of noise, and pre and post for unenhanced and contrast-enhanced, respectively. Second, we calculated the contrast-to-noise ratio as being equal to the ratio of the lesion-cortex signal intensity difference to noise. This parameter is a measure of the signal intensity of the lesion relative to that of the cortex—that is, a positive value indicates hyperintensity and a negative value indicates hypointensity with respect to renal cortex.
Statistical Analysis
Analysis of variance and the Newman-Keuls test were used for multiple
comparisons of quantitative data. A p value of less than 0.05 was
considered statistically significant.
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On dynamic MR sequences, angiomyolipomas, at visual inspection 30 sec after gadolinium injection, appeared hyperintense with respect to the renal cortex in three patients, hypointense in one patients, and isointense in four patients. From 60 to 210 sec, all angiomyolipomas showed a signal intensity enhancement lower than that of renal cortex (Fig. 3A,3B,3C,3D).
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On dynamic MR sequences, the complicated cysts showed no or minimal enhancement and were classified as avascular lesions (Fig. 4A,4B,4C,4D).
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Quantitative Analysis
The differentiation between hyper- and hypovascular renal cell carcinomas,
which emerged from the visual observations of the qualitative examination, was
used for the further analysis of quantitative data.
The time profiles of percentage of enhancement and contrast-to-noise ratio on dynamic FLASH gradient-recalled echo sequences are summarized in Tables 1 and 2, respectively, with statistical significance given. The time profile of percentage of enhancement of hypervascular renal cell carcinomas was similar to that of cortical tissue until 150 sec. In late sequences (180-210 sec) the percentage of enhancement became significantly greater than that of cortex and similar to that of renal medulla. Hypovascular renal cell carcinomas always showed lower values of percentage of enhancement than those of hypervascular renal cell carcinoma, the difference being significant from 60 to 210 sec.
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Angiomyolipomas had an early peak mean percentage of enhancement at 30 sec, even though they remained hypointense when compared with renal cortex (see contrast-to-noise ratio results). This was because of the shift from a low signal intensity on baseline fat-suppressed sequences to high signal intensity for lesion vascularity as soon as the contrast material was injected. Subsequently, a vascular washout of the gadolinium determined a decline in percentage of enhancement to values similar to that of hypovascular renal cell carcinomas from 90 to 210 sec.
Complicated cysts showed low mean percentage of enhancement values, significantly different from those of all other lesions at all times.
Contrast-to-noise ratio showed that all lesions were hypointense with respect to the renal cortex at baseline. Contrast-to-noise ratio values before the injection of gadolinium were similar for hypervascular and hypovascular renal cell carcinomas and complicated cysts; those of angiomyolipomas were significantly lower because of fat suppression. After the injection of gadolinium, the hypervascular renal cell carcinomas progressively became isointense and, from 150 to 210 sec, hyperintense with respect to renal cortex.
The other lesions remained hypointense, and the gap in signal intensity with the renal cortex increased in the first minute; until 60 sec, hypovascular renal cell carcinomas showed a slight decline in contrast-to-noise ratio, whereas angiomyolipomas and cysts had a sharper decrease, then the respective values for the three lesions remained almost stable until 210 sec.
With the values obtained from measurements of percentage of enhancement and contrast-to-noise ratio, it was possible to draw time curves that, when observed in combination, could shape a typical pattern for each kind of lesion (Figs. 5 and 6).
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MR imaging of small renal lesions has been limited, not only because of the higher costs and the lower availability of this technique but also because, with conventional spin-echo sequences, small renal cell carcinomas often show a relative regularity or sharpness of margins and appear as homogeneous lesions. On conventional MR imaging, these cases have no specific signal intensity that is diagnostic of renal cell carcinoma. Their signal intensity varies on T1-weighted images from hypo- to hyperintense when compared with the surrounding renal parenchyma, and it increases on T2-weighted images. However, hypointensity on both T1-and T2-weighted images has been described [16,17,18]. Thus, on unenhanced MR imaging, the signal intensity of solid renal tumors can be similar to that of renal parenchyma on both T1- and T2-weighted images, resulting, according to Semelka et al. [6], in only a 63% tumor detection rate when the lesion measures less than 3 cm in diameter.
Indications for the use of MR imaging in the study of small renal lesions include allergy to iodine contrast agents, renal failure, and suboptimal or equivocal CT or sonography studies [4, 5]. The possibility of obtaining sections that are not only transverse but also multiplanar makes MR imaging indicated over conventional CT in patients with a renal mass at either pole of the kidney, for identification of which coronal or sagittal imaging may be useful [16]. Recent developments, including the technique we used in the present study—namely, breath-hold gradient-recalled echo FLASH sequences with fat suppression, before and after the IV administration of gadolinium (dynamic MR imaging)—help to shorten examination times, reduce respiratory motion artifacts, increase the conspicuity of renal lesions, and improve MR imaging in detecting and characterizing renal masses [1, 4, 7, 19,20,21].
In our study we performed a quantitative analysis of signal intensity on MR images. Although transferring MR images to a MagicView workstation is not widely available to practicing radiologists, it is a feasible method for rapidly calculating the percentage of enhancement of renal lesions and their contrast-to-noise ratio with respect to renal cortex.
The degree of vascularity of tissue lesions correlates with the degree of enhancement on contrast-enhanced images [22]. Early enhancement of a renal lesion during the distribution phase of gadolinium reflects blood delivery (capillary phase imaging), depending on tumor vascularity and its blood supply; subsequent enhancement reflects capillary permeability (interstitial imaging) [23]. Becuase gadolinium rapidly equilibrates from the intravascular space into the extracellular space, there is a potential for the signal intensity of the lesion to became isointense relative to the normal parenchyma. Therefore, it is important to perform MR imaging in the first minutes after injection of contrast material [19], as we did with the dynamic sequences in the first 210 sec after contrast injection.
Moreover, cell arrangement with regard to tumor vascularity can correlate with radiologic appearances on gadolinium-enhanced dynamic MR images. In tumors with solid architecture (the most common type of renal cell carcinoma), a large nest of tumor cells is separated by a stroma endowed with prominent sinusoidlike vessels, whereas in tumors with papillary architecture (which were found in four of our 10 patients with hypovascular renal cell carcinoma), neoplastic cells line thin connective tissue stalks with very small vessels [24].
In our patients, on basal, unenhanced gradient-recalled echo sequences, renal cell carcinomas and complicated cysts could be almost indistinguishable because of their similar degree of hypointensity with respect to the renal cortex. Benign, complicated cysts can be difficult to differentiate from malignancies [8]. These cysts have high attenuation on CT scans and can appear as medium- or high-signal-intensity lesions on spin-echo and unenhanced gradient-recalled echo FLASH MR sequences, depending on the age of the blood break-down products or depending on protein concentration. Even though complicated cysts do not enhance, their signal intensity remains higher than that of simple cysts, and they are identified only by comparing unenhanced and contrast-enhanced images [5, 7, 16, 18].
Our results show that, after the administration of gadolinium, hypervascular renal cell carcinoma can be easily differentiated because of the percentage of enhancement and contrast-to-noise ratio curve, which are significantly higher than those of hypovascular renal cell carcinoma and benign lesions (angiomyolipomas and complicated cysts). This can be explained by the fact that all our cases of hypervascular renal cell carcinoma were solid clear cell tumors with alveolar or trabecular architecture and a profuse blood supply.
On the other side, hypovascular renal cell carcinomas, angiomyolipomas, and complicated cysts enhanced significantly less than did cortical and medullary tissue. A simple qualitative or visual observation of the images, at a determinate time after contrast injection, could be confusing by not allowing a correct characterization of the hypointense lesion (Figs. 2A,2B,2C,2D,3A,3B,3C,3D,4A,4B,4C,4D). This is a critical factor, considering the importance of differentiating a malignant (hypovascular renal cell carcinoma) from a benign (angiomyolipoma or cyst) lesion. Quantitative evaluation can be helpful in these cases, providing different signal intensity profiles or time curves for each kind of lesion. In fact, hypovascular renal cell carcinomas, from the first minute after gadolinium injection, showed significantly greater enhancement than complicated cysts. Moreover, hypovascular carcinomas showed mean values of contrast-to-noise-ratio that were always lower than those of hypervascular carcinomas and always greater than those of benign lesions, the latter decreasing and remaining at a significantly lower level.
Renal cell carcinoma can have a cystic aspect, even though such an appearance is rare with small carcinoma. In the patients we studied, all the pathology studies proved renal cell carcinomas were solid and all the cysts had no pathologic proof for true benignity, although we found no malignant cells in the cystic aspiration fluid and, after a 2-year follow-up, no mass enlargement was present. Thus, although complicated cysts show no or minimal enhancement, the possibility exists that they could be difficult to differentiate from minimally enhancing cystic renal cell carcinoma on rare occasions [5].
With our dynamic technique, angiomyolipomas showed a peculiar pattern, with a brisk early (30 sec) percentage of enhancement of signal intensity compared with the basal low intensity caused by fat suppression, and a gradual decrease in intensity (washout) during the remainder of the imaging period. These data agree with the data of other researchers [4]. Of course, the radiologic diagnosis of angiomyolipoma depends on the visualization of fat on unenhanced images (either CT or MR images), and contrast enhancement has a limited diagnostic role.
Our study is limited because it does not include the entire spectrum of renal masses (no cases of oncocytoma, renal metastasis, or focal nephritic lesion). Moreover, the dynamic breath-hold technique we used in this study limits the MR imaging to four slices. For this reason, it is not useful for the screening of renal masses and has a limited value in patients with multiple lesions, some of which can be missed if located on different planes. Rather, this technique can be used for the assessment of single established renal masses.
In conclusion, the potential for lesion characterization is an important benefit of dynamic breath-hold gradient-recalled echo FLASH MR imaging with fat suppression and the IV administration of gadolinium. When a lesion of low signal intensity before the injection of contrast material shows no perceptual enhancement (cystic) after the injection, or a definitive enhancement (solid), no quantitative signal intensity measurements are needed. However, for complicated lesions that show medium or high signal intensity on unenhanced images, quantitative measurements on contrast-enhanced images can be essential.
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| HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
), medulla (
), and different lesions.
Note that after 60 sec from contrast injection, hypervascular renal cell
carcinoma (
) enhances more than cortex. Hypovascular renal cell
carcinoma ([UNK]) has much lower enhancement. Angiomyolipoma (
), after
early peak, has enhancement curve similar to that of hypovascular carcinoma.
Enhancement of complicated cyst (
) is negligible.