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Original Report |
1 Department of Radiology, University Hospital Graz, Auenbruggerplatz 9, Graz,
Styria A-8036, Austria.
2 Department of Radiology, Hospital of Leoben, A-8700 Leoben, Austria.
3 D2K-Solutions, A-8410 Wildon, Austria.
Received November 26, 2003;
accepted after revision February 17, 2004.
Address correspondence to A. J. Ruppert-Kohlmayr
(andrea.ruppert{at}lkh-leoben.at).
Abstract
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CONCLUSION. The new correction method is a simple tool for excluding intrinsic influences on the enhancement of lesions. Quantitative enhancement evaluation with this method of the influence of intrinsic factors enables accurate differentiation between renal clear cell carcinoma and renal papillary carcinoma.
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Enhancement measurement is accurate for differentiating renal lesions, but a large number of intrinsic and extrinsic factors can affect organ perfusion and the quantity, time, and rate of delivery of contrast material to organs such as the kidneys, influencing the attenuation values and contrast enhancement of lesions in contrast phases. The intrinsic factors are anatomic and physiologic characteristics that vary from patient to patient and temporally within the same patient. They include, for example, the patient's weight, cardiac function, state of hydration, and renal function [8, 9]. Extrinsic factors are mechanical variables that are dictated by the CT protocol. They include the quantity, rate, and length of injection of contrast material [8, 9] and the delay from the injection of contrast material to the beginning of image acquisition. All these factors influence enhancement dynamics of organs or lesions after contrast administration and make attenuation measurements variable [10].
The influence of the CT protocol parameters [8, 10] can be excluded when they are equalized for all patients using a standard CT protocol, but the exclusion of the intrinsic factors is not possible under natural conditions.
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Helical CT Protocol
A helical CT scanner (LightSpeed, GE Healthcare) and a uniform examination
protocol were used in all patients. One hundred twenty milliliters of contrast
material with a concentration of 300 mg I/mL (Ultravist 300 [iopromide],
Schering) was administered with a flow rate of 4 mL/sec using an automatic
injector (Medrad). The contrast agent was injected via a 19-gauge venous line
into the right antecubital vein during each examination. The patient was
placed in the supine position, and each examination phase was performed during
expiration.
CT of the kidney consisted of a triphasic helical CT study: an unenhanced phase of the upper abdomen from the diaphragm to the iliac crest, a corticomedullary phase (30-sec delay) covering the whole kidneys, and a nephrographic or pyelographic phase (180-sec delay) from the diaphragm to the symphysis. A section collimation of 2.5 mm, a pitch of 1.5, and a reconstruction interval of 2 mm were applied in all kidney studies.
All examinations were evaluated on a Sparc 10 CT/MR Workstation (Sienet Magic View 1100, Siemens) by two experienced radiologists.
Standardized Attenuation Measurements
Three attenuation values within the lesions
(Lx; L = lesion, x = scanning
phase) were obtained in each phase. Therefore, three regions of interest
(ROIs) were identified in different positions of one lesion in one examination
phase. Each of the three ROIs was put in the corresponding position in the
other phases. We did not use a standard ROI size, but we used an ROI that
included approximately one third of the lesion. We paid attention to ROI
placement in hypervascular lesions that often have cystic or necrotic parts to
ensure this ROI was placed only in the hypervascular region and not in the
cystic or necrotic regions or in healthy renal tissue. From the measured
attenuation values, mean values with single SDs were calculated.
To eliminate the influence of intrinsic factors on the measured attenuation
values, a formula was created to obtain attenuation values that are corrected
to a certain standard in the aorta at the level of the organ-supplying vessel,
considering the pathway of contrast media flow through the body. Contrast
media initially reach the kidneys via the renal arteries. Therefore, we
measured the attenuation of the aorta at the origin level
(Ax) of this vessel. As a standard value for
sAx we took a constant value for each phase. We
took a randomized value that lay within our measured aortic values. For the
corticomedullary phase, this constant value was 250 H; for the nephrographic
phase, 120 H. A standardizing factor (Fx) that
characterized the discrepancy between the measured aortic value in a certain
patient and the standard value in the aorta at the level of the supplying
vessel was created as follows:
 | (1) |
Fx was then multiplied by the measured attenuation value in the lesion (Lx) and a corrected lesion attenuation value (cLx) resulted.
The formula was as follows:
 | (2) |
where cLx equals the corrected lesion attenuation value in any scanning phase (cLcm in the corticomedullary phase and cLng in the nephrographic phase). Lx equals the measured lesion attenuation value in any scanning phase (Lcm in corticomedullary phase and Lng in nephrographic phase).
An example explains the method: A patient has a renal lesion showing a measured attenuation value Lcm of 130 H and aortic attenuation Acm of 280 H in the corticomedullary phase. As described earlier, the standard aortic attenuation value in the corticomedullary phase (sAcm) is 250 H. The standardizing factor Fcm is then 250 H/280 H = 0.89. The corrected attenuation of the lesion in the corticomedullary phase cLcm is 130 H x 0.89 = 116.1 H. Standardized attenuation measurements are shown in Figure 1.
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Relative Enhancement
The relative enhancement in a contrast phase
(relEx) of the lesions was defined as the ratio
between the corrected attenuation in a contrast phase
(cLx) and the measured attenuation in an
unenhanced phase (Lu), resulting in the following
formula:
 | (3) |
Statistical Analysis
For all parameters, such as corrected attenuation of the lesion and
relative enhancement of each contrast phase, a cutoff value was defined, and
the sensitivity, specificity, and accuracy for differentiating renal clear
cell carcinoma from renal papillary carcinoma were calculated.
Kolmogorov-Smirnov tests of the attenuation parameters of each phase were
carried out. A p value less than 0.05 was considered statistically
significant at the 95% confidence level.
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In the unenhanced phase, the mean attenuation value was 39.9 H (SD ± 11 H; range, 17.4-73.8 H) in renal clear cell carcinoma and 38.5 H (± 5.4 H; range, 27.8-46.6 H) in renal papillary carcinoma.
In the corticomedullary and nephrographic phases, all attenuation values were calculated according to the previously mentioned formulas. In the corticomedullary phase, attenuation values (cLcm) of renal clear cell carcinoma were significantly higher than those of renal papillary carcinoma (p < 0.05). In renal clear cell carcinoma, the mean arterial attenuation value was 152.6 H (± 35.4 H; range, 90.5-276.1 H); in renal papillary carcinoma, the value was 61.8 H (± 24.4 H; range, 37.7-123.8 H). The accuracy of Lcm was 95.7%; the sensitivity, 98.3%; and the specificity, 92%, when using 100 H as the cutoff value.
The nephrographic phase had a significant difference of attenuation (Lng) between renal clear cell carcinoma and renal papillary carcinoma (p < 0.05). In renal clear cell carcinoma, the mean nephrographic attenuation value was 105.1 H (± 17.5 H; range, 88.4-120.1 H); in renal papillary carcinoma, it was 67.3 H (± 14.4 H; range, 36.1-88.7 H). The accuracy of Lng was 94.8%; the sensitivity, 95.2%; and the specificity, 92.3%, when using 85 H as the cutoff value.
Relative Enhancement
The relative enhancement in the corticomedullary and nephrographic phases
showed significant differences between renal clear cell carcinoma and renal
papillary carcinoma (p < 0.05).
The relative enhancement in the corticomedullary phase (relEcm) was higher than the cutoff value of 2.0 in most renal clear cell carcinomas (mean value, 4.07; SD, 1.73; range, 1.51-10.98) and lower than 2.0 in renal papillary carcinomas (mean value, 1.66; SD, 0.55; range, 1.13-2.82), with accuracy of 90%, sensitivity of 94.7%, and specificity of 75%.
In the nephrographic phase, relEng was higher than the cutoff value of 1.8 in most renal clear cell carcinomas (mean value, 2.88; SD, 1.2; range, 1.19-7.99) and lower than 1.8 in renal papillary carcinomas (mean value, 1.72; SD, 0.28; range, 1.3-2.34), with accuracy of 88%, sensitivity of 92%, and specificity of 69%.
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If absolute enhancement measurements are used for quantitative studies to differentiate lesions by means of enhancement patterns, an exact quantitative evaluation of enhancement is important. For this reason, the influence of external and intrinsic factors is important because enhancement depends on the amount of contrast material reaching the organ at the specific time of measurement.
In a previous study [11], we quantitatively differentiated two benign liver lesions—focal nodular hyperplasia and hepatocellular adenoma. To raise the accuracy of differentiation, especially in small lesions in which morphologic and vascular patterns often are inconclusive, a quantitative evaluation of enhancement measurements should improve the results. Perfusion of an organ and subsequently of lesions is essentially dependent on intrinsic factors—such as cardiac function, IV access, a patient's weight and size, and blood viscosity—but also on factors concerning the CT protocol parameters [8-10].
The idea of this standardizing method is that in each patient, different amounts of contrast material are present in the supplying vessel at the time of scanning because of external factors, especially cardiac function and patient weight [8]. Therefore, the blood, as well as the contrast material supply to the organ and a lesion in that organ, is different in each patient, a fact that influences organ and lesion attenuation. The simplest way to equalize these conditions is to mathematically equalize the attenuation in the aorta at the level of the supplying vessels in the different phases for each patient. The consequence was that we obtained attenuation values in the lesions nearly exactly at the same contrast material levels in the supplying vessel. When this method is used, the external factor has no influence on enhancement. If all patients have the same attenuation in the supplying vessel, the contrast-enhancement conditions in the organ and in lesions are the same for each patient. Because this condition is not always present, the attenuation value in the organ or lesion that could be measured if the attenuation value in the aorta at the level of the supplying vessel had a certain standard value has been calculated. This standard aortic attenuation value (sAx) was randomly assumed to be values within the measured range of our patient cohort—250 H in the corticomedullary phase and 120 H in the nephrographic phase. The choice of sAx is not obligatory; any other consistently used value could be taken as the standard value.
Another consideration was the necessity of the standard aortic attenuation value in our formula. Some might believe that this value would not be necessary for the results, making the formula unnecessarily complicated. It would also be possible to divide the measured lesion attenuation value (Lx) by the measured aortic attenuation value (Ax), getting a factor describing the relationship between lesion attenuation and aortic attenuation at the point of measurement, as did Herts et al. [6] for the tumor-to-aorta enhancement ratio. An argument against this is that with this alternative calculation method, we would get a corrected attenuation factor the radiologist—who, used to working with attenuation values in Hounsfield units—could not work with because the resulting values are factors. That is why correction of certain attenuation in the aorta at the level of the supplying vessel is necessary.
The chosen standard CT protocol in our study with unenhanced, corticomedullary, and nephrographic phases was chosen because these phases are accurate for detection and characterization of parenchymal lesions in kidneys [12, 13].
Previous studies [7, 14-16] tried to describe and differentiate renal lesions according to morphologic criteria. Differentiation according to morphologic characteristics is possible in large lesions, but in small lesions it is often difficult. Using contrast enhancement on CT, we confirmed the high vascularization and perfusion of renal clear cell carcinoma compared with the low perfusion of renal papillary carcinoma, an observation that was made before the advent of CT in angiographic studies [17, 18].
In our study, the differentiation of renal clear cell carcinoma from renal papillary carcinoma, using the corrected attenuation in the corticomedullary phase, was accurate (95.7%). This was the most accurate and sensitive parameter of all four evaluated parameters that showed significant differences between renal clear cell carcinoma and renal papillary carcinoma. Renal clear cell carcinoma had cLcm values higher—and renal papillary carcinoma, lower—than 100 H, which was defined as the cutoff value. The nephrographic phase was also accurate (94.8%) in differentiating between renal clear cell carcinoma and renal papillary carcinoma. Renal clear cell carcinoma had cLng values higher—and renal papillary carcinoma, lower—than 85 H (cutoff value). Kim et al. [7] found lower cutoff values. These differences might be due to the inclusion of renal clear cell carcinoma, renal papillary carcinoma, and other lesions in their study, making no correction to the attenuation values.
The relative enhancement parameter indicates a feature that describes the increase of attenuation after contrast material application. For example, factor 2 means an increase of two times the attenuation between the unenhanced and contrast phases. In our study, relative enhancement in the corticomedullary and nephrographic phases showed significantly different values between renal clear cell carcinoma and renal papillary carcinoma. Relative enhancement in the corticomedullary phase was an accurate parameter (accuracy, 90%) for differentiating renal clear cell carcinoma from renal papillary carcinoma. Renal clear cell carcinoma had relEcm values higher—and renal papillary carcinoma, lower—than the cutoff value of 2.0. The relative enhancement in the nephrographic phase had an accuracy of 88%. Renal clear cell carcinoma had relEng values higher—and renal papillary carcinoma, lower—than the cutoff value of 1.8.
Knowing the histologic type of renal cell carcinoma might be interesting for two reasons that influence the preoperative and operative strategies. First, the better prognosis of renal papillary carcinoma might allow patients with higher surgical risks to wait and control the lesion or choose a minimally invasive strategy such as radiofrequency or cryotherapy [19]. A second reason is better operation planning. The type of tumor might be of interest to the surgeon because if he resects a hypervascular renal clear cell carcinoma, he must expect more bleeding than with hypovascular renal papillary carcinoma. The same information might be of interest for minimally invasive ablative approaches like radiofrequency or cryotherapy [19] for two reasons: It might be safer to perform an embolization in renal clear cell carcinoma—a palliative procedure—before the planned curative intervention to avoid bleeding. Radiofrequency ablation and cryotherapy are procedures that do not produce histologic material such as that produced during surgery so it is important to have a tool like CT that can accurately classify the histologic type of renal cell carcinoma before intervention.
One limitation of this study is the relatively small number of patients with renal papillary carcinoma. It might be necessary for further studies to prove these promising results and confirm observations made many years ago in angiographic studies [17, 18]. Our study includes only malignant lesions, but it might be interesting to compare the enhancement characteristics of hypovascular renal papillary carcinoma with those of hyperdense cysts to show the accuracy of CT in differentiating these two lesions. We plan to cover this interesting topic in a further study.
In conclusion, our enhancement correcting method is a simple way to deal with the influence of intrinsic factors on quantitative enhancement patterns in focal lesions. It can be applied not only to single-detector helical CT but also to other techniques in which dynamic studies are performed. The method can be applied not only to renal lesions but also to differentiate lesions in other organs. In this study, the introduced method can differentiate the most common malignant renal tumors accurately. Our study showed a high enhancement in the corticomedullary phase in renal clear cell carcinoma with a slight washout in the nephrographic phase; it showed a low enhancement in many renal papillary carcinomas—sometimes less than 12 H in the corticomedullary phase—but in the nephrographic phase, the enhancement of renal papillary carcinoma was clearly higher than 12 H.
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