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Evaluation of Pseudoenhancement of Renal Cysts During Contrast-Enhanced CT

¹ All authors: Department of Radiology, Duke University Medical Center, Box 3808, Durham, NC 27710.

Received June 17, 1999; accepted after revision July 15, 1999.

 
Address correspondence to D. H. Sheafor.

Presented at the annual meeting of the American Roentgen Ray Society, New Orleans, May 1999.

Abstract

Top Abstract Introduction Materials and Methods Results Discussion References

 
OBJECTIVE. The purpose of our study was to evaluate renal cyst pseudoenhancement during helical CT in a phantom model and in patients.

MATERIALS AND METHODS. Iodine baths containing water-filled spheres and cylinders were constructed to simulate cysts in enhancing renal parenchyma. Iodine concentration, cyst size and location, collimation, and peak kilovoltage were varied and cyst attenuation was measured. Data were analyzed with the mixed linear models and Mantel-Haenszel tests. Subsequently, a paired t test compared CT attenuation values before and after contrast material enhancement in 40 patients with 68 renal cysts (radiographic stability >3 months).

RESULTS. The attenuation values of phantom cysts increased when placed in a contrast media bath (p = 0.001). The increase in attenuation values became more pronounced with increasing iodine concentrations, decreasing peak kilovoltage, and smaller sphere sizes. In patients, mean cyst attenuation increased 3.4 ± 6.2 H after administration of contrast material (p = 0.00002). The attenuation did not increase more than 10 H in any of the 37 cysts larger than 2 cm found in patients. Eight (26%) of the 31 cysts smaller than 2 cm found in patients increased by at least 10 H.

CONCLUSION. In a phantom model, at simulated physiologic levels of renal enhancement, cysts may pseudoenhance by more than 10 H. Similarly, in patients, cysts may also pseudoenhance; however, most pseudoenhancement does not exceed 10 H. In patients, pseudoenhancement of at least 10 H is more likely in cysts smaller than 2 cm.

Introduction

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Benign renal cysts are common incidental findings and may be seen on CT in up to 27% of patients more than 50 years old [1]. Uncommonly, primary renal neoplasms can be cystic, requiring differentiation from a simple cyst. CT criteria for the diagnosis of simple cysts have been well established and include an imperceptible wall, absence of internal septations, unenhanced attenuation of less than 20 H, and no enhancement or enhancement of less than 10 H after administration of IV contrast material [2, 3, 4]. A threshold of 10 H is generally considered significant for determination of nonenhancement. Unfortunately, many variables can affect CT attenuation measurements, falsely elevating or decreasing the attenuation of a lesion [5, 6]. Volume averaging is a well-known cause of evation of attenuation measurements. In phantom cysts, beam hardening has been shown to alter attenuation values [7, 8]. Pseudoenhancement refers to increases in lesion attenuation after administration of contrast material as a result of the beam-hardening artifact. If pseudoenhancement of simple renal cysts can occur with modern CT techniques, a benign simple cyst may potentially be misclassified as an enhancing mass that requires surgery. The purpose of our study was to evaluate pseudoenhancement in a renal phantom and to determine the degree to which beam hardening affects renal cyst attenuation values in patients.

Materials and Methods

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The initial phantom study was performed using a commercially available unit (Deluxe ECT phantom; Data Spectrum, Hillsborough, NC). The phantom consisted of a 20-cm-diameter acrylic cylinder housing attachable polycarbonate spheres suspended in a contrast bath (Fig. 1A). Neither the cylinder nor the spheres contained any high-atomic-number material that would cause significant X-ray beam attenuation. The spheres were filled with water to simulate simple cysts. The contrast bath consisted of an aqueous iodine solution comprised of various dilutions of iopamidol (Isovue 200; Bracco Diagnostics, Princeton, NJ). Iodine dilutions included 0, 6.5, 13, and 26 mg/ml, which corresponded to CT attenuations of -1.8, 129, 228, and 378 H, respectively. These dilutions were chosen to include the range of renal parenchymal attenuation values expected during the nephrographic phase of enhancement. All images were obtained during a single session using the same helical CT scanner (CT/i; General Electric Medical Systems, Milwaukee, WI). Sequential CT of the phantom was performed with iodine concentrations of 0, 3.25, 6.5, 13, and 26 mg/ml. Sphere sizes of 6, 10, 16, and 28 mm were used. Scanning was performed axially and helically (pitch = 1:1), using 200 mA with 3- and 5-mm collimation and reconstruction intervals, and using four different X-ray beam energies (80, 100, 120, and 140 kVp). Energy levels were selected to include the peak kilovoltage range used in routine clinical practice. Care was taken to calibrate the scanner at all four energy levels immediately before the experiment. Only 3-mm collimation was used for these lesions because of the predicted effects of volume averaging with 5-mm collimation in 6-mm simulated cysts. The scanning levels were selected so that the center image was scanned through the equator of the sphere. The spheres were positioned both centrally and peripherally in the phantom. Spheres and contrast bath attenuation values were obtained by placing circular region-of-interest (ROI) markers. In the case of the spheres, each ROI was placed centrally and did not contact the wall. The data were analyzed with both the mixed linear models and Mantel-Haenszel tests of association to adjust for the batched acquisition of phantom data.

View larger version (32K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 1A. —Diagrams of two renal phantoms. Two-dimensional diagram shows large cylindric phantom that houses attachable water-filled spheres suspended in contrast bath.

A second phantom was designed to simulate a kidney with both intraparenchymal and exophytic renal cysts because the commercially available phantom was larger than a kidney and could simulate only cysts completely surrounded by enhancing parenchyma. This second phantom consisted of a small basin (cross-section, 6 x 4 cm) filled with a contrast bath (I = 26 mg/ml) and 14-mm-diameter plastic cylinders filled with water. The use of cylinders negated the possibility of volume averaging effects. The phantom was scanned with an X-ray beam energy of 140 kVp, the value used in routine clinical practice at our institution. To evaluate the effect of cyst location in the kidney, a cylinder was suspended in the contrast bath at various heights above and below the bath surface (-17, -1, 6, and 17 mm from cylinder center to bath surface). In two of the positions (-1 and 6 mm), the cylinder was crossing the surface of the contrast bath, mimicking an exophytic renal cyst (Fig. 1B).

View larger version (33K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 1B. —Diagrams of two renal phantoms. Two-dimensional diagram shows small phantom containing 1.4-mm-diameter cylinders in contrast bath. Cylinders were positioned to simulate exophytic and intraparenchymal lesions.

The spheres and cylinders used in both phantom experiments were scanned in a water bath both before and after their submersion in contrast material, documenting impermeability to iodine.

A retrospective clinical study of renal cysts was also performed to assess the impact of pseudoenhancement in patients. Patient selection was based on a retrospective review of abdominal CT reports dated May 1996 through July 1998. The reports of CT performed both with and without the IV administration of iodinated contrast material were reviewed for the presence of renal cysts or low-attenuation lesions. Only lesions with radiographic stability for a minimum of 3 months were included in the study. All examinations with reported renal cysts or low-attenuation lesions were downloaded from optical disks and reviewed on a workstation monitor (SPARC station 10; Sun Workstations, Palo Alto, CA).

To meet inclusion criteria, all lesions were homogeneous, well defined, round or oval, lacking septations or mural nodularity; and all measured water attenuation (<20 H) on the unenhanced scan. Lesions not seen on at least three contiguous images were excluded from the study because of their small size and the inability to exclude the effects of partial volume averaging. To avoid patient bias, no more than two cysts per kidney were selected. If a kidney contained multiple cysts, two were selected at random. A total of 68 cysts in 48 kidneys in 40 patients were identified that met these criteria, and these cysts constituted our study group. Either multiphase liver imaging to evaluate for hepatic malignancy (n = 20) or dedicated renal imaging for characterization of a renal mass (n = 20) had been performed in all patients included in the study. All CT was performed as breath-hold helical acquisitions on one of four helical CT scanners (CT/i or HiSpeed Advantage; General Electric Medical Systems). X-ray beam energy was 140 kVp in all cases. Collimation was either 5 mm (n = 23) or 7 mm (n = 17), with a pitch of either 1.5 (n = 23) or 1.0 (n = 17), and a reconstruction interval of 5-7 mm. Patients received either 150 or 175 ml of nonionic contrast material.

Lesion attenuation was measured with a centrally placed ROI, avoiding the cyst wall. When the lesion was present on exactly three slices, the middle slice was selected for obtaining attenuation values. The neighboring renal parenchyma attenuation value was also obtained. Measurements were made on scans both before and during the portal venous phase (65-sec scan delay) or nephrographic phase (80-sec scan delay) of IV contrast material administration. A paired t test was performed to evaluate statistical differences comparing the attenuation values of the cysts before and after contrast material administration.

Results

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Phantom Study
The attenuation values of water spheres increased significantly when placed in the contrast baths (p = 0.001). Attenuation values of the spheres increased in a stepwise fashion as the iodine concentration in the bath increased. The effect was more pronounced with decreasing X-ray beam energies (p = 0.001) (Fig. 2) and in smaller spheres (p = 0.001) (Fig. 3). Whereas both centrally and peripherally located spheres had pseudoenhancement, the peripherally located spheres increased in attenuation more than the centrally located spheres (p = 0.001). The results did not vary between axial and helical technique (p = 0.473).

View larger version (21K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 2. —Bar graph shows effect of beam energy (peak kilovoltage) on pseudoenhancement of 28-mm water sphere. Lower peak kilovoltage settings produced more pronounced pseudoenhancement. White = 80 kVp, lightly shaded = 100 kVp, darkly shaded = 120 kVp, black = 140 kVp.

View larger version (19K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 3. —Bar graph shows effect of sphere size on pseudoenhancement at 140 kVp. Small spheres tend to pseudoenhance more than large spheres. White = 6 mm, lightly shaded = 10 mm, darkly shaded = 16 mm, black = 28 mm.

In the exophytic cyst phantom study, an increase from the baseline attenuation value was observed with the cylinder completely submerged in the contrast bath. As the cylinder was raised toward the surface, attenuation values increased. As the cylinder was elevated out of the bath, the attenuation value decreased to baseline (Fig. 4). At contrast bath iodine concentrations simulating physiologic levels of enhancement (150-250 H), cyst pseudoenhancement was 8 H (range, 5-10 H).

View larger version (17K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 4. —Bar graph shows effect of distance from contrast bath surface on pseudoenhancement at 140 kVp in 14-mm cylinder. Attenuation increases as cylinder approaches bath surface, then decreases as cylinder is raised out of contrast bath. White = -17 mm, lightly shaded = -1 mm, darkly shaded = 6 mm, black = 17 mm.

Clinical Study
The 68 renal cysts had a mean attenuation value of 6.2 ± 6.2 H (range, -10.5 to 17.7 H) before contrast material administration, and a mean attenuation value of 10.0 ± 8.5 H (range, -8.0 to 35.1 H) after contrast material administration, resulting in a mean increase of 3.4 ± 6.2 H (range, -12.2 to 19.7 H) after contrast material administration. This increase was statistically significant (p = 0.00002; 95% confidence interval, 1.97-4.89). Mean unenhanced renal parenchyma attenuation was 27.4 ± 5.8 H (range, 15.4-36.4 H). Mean renal parenchyma attenuation during the portal venous and nephrographic phases of contrast material enhancement was 162.1 ± 40.7 H (range, 97.3-232.4 H). This resulted in a mean renal parenchyma enhancement of 134.7 ± 40.2 H (range, 73.2-206.1 H).

Eight (12%) of the 68 cysts "enhanced" more than 10 H, but none by more than 20 H (range, 10.3-19.7 H; mean, 14.5 H). These eight cysts were all smaller than 2 cm in diameter. These cases were rereviewed, and none had other imaging features of malignancy (Fig. 5A, 5B, 5C, 5D). The mean interval of stability on follow-up of these eight lesions was 39.6 months (range, 10-78 months; median, 32 months). Seven of the eight lesions were located predominately in the renal margin. In the group of 60 cysts that did not increase in attenuation by more than 10 H, the mean increase in attenuation above baseline was 2.0 ± 4.8 H (p = 0.002).

View larger version (144K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 5A. —32-year-old woman with dysmenorrhea. Unenhanced CT image (collimation, 5 mm) shows 2-cm low-density intraparenchymal lesion measuring 18 H in right kidney.

View larger version (157K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 5B. —32-year-old woman with dysmenorrhea. Three contiguous nephrographic-phase CT images (collimation, 5 mm; pitch, 1.5:1) of same lesion as in A. Unenhanced attenuation was 35 H (pseudoenhancement, 17 H). Lesion was stable for more than 3 years of radiographic follow-up (not shown) and is presumed to represent simple cyst. Note circular regions of interest labeled "1" on A and C.

View larger version (165K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 5C. —32-year-old woman with dysmenorrhea. Three contiguous nephrographic-phase CT images (collimation, 5 mm; pitch, 1.5:1) of same lesion as in A. Unenhanced attenuation was 35 H (pseudoenhancement, 17 H). Lesion was stable for more than 3 years of radiographic follow-up (not shown) and is presumed to represent simple cyst. Note circular regions of interest labeled "1" on A and C.

View larger version (152K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 5D. —32-year-old woman with dysmenorrhea. Three contiguous nephrographic-phase CT images (collimation, 5 mm; pitch, 1.5:1) of same lesion as in A. Unenhanced attenuation was 35 H (pseudoenhancement, 17 H). Lesion was stable for more than 3 years of radiographic follow-up (not shown) and is presumed to represent simple cyst. Note circular regions of interest labeled "1" on A and C.

The mean attenuation increase in the 37 cysts larger than 2 cm was 1.6 ± 3.5 H (range, -8.8 to 8.4, p = 0.009). The mean attenuation increase in the 31 cysts smaller than 2 cm was 5.6 ± 7.8 H (range, -12.2 to 19.7; p = 0.0003). Overall, the group of cysts smaller than 2 cm pseudoenhanced significantly more than the group of cysts larger than 2 cm (p = 0.01).

Data were also analyzed with cysts categorized as either exophytic or nonexophytic. Cysts with greater than or equal to 50% of their volume bulging outside the confines of the renal margin were arbitrarily considered exophytic. By this criterion, 30 cysts were grouped as exophytic and 38 as nonexophytic. Mean attenuation increase of the exophytic group after the administration of IV contrast material was 1.2 ± 5.0 H (range, -12.2 to 11.8 H), which was not statistically significant (p = 0.20). Only one (3.3%) of 30 cysts in this group pseudoenhanced by more than 10 H. Mean attenuation increase of the nonexophytic cyst group was 5.2 ± 6.5 H (range, -7.8 to 19.7 H), which was statistically significant (p = 0.00002). The difference in enhancement between exophytic and nonexophytic cysts was also statistically different (p = 0.005).

Discussion

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Renal cystic pseudoenhancement refers to the artifactual increase in CT attenuation value of a simple cyst after the administration of iodinated contrast material. Theoretically, a phenomenon similar to that depicted on CT imaging of the brain (when the high-attenuation calvaria causes artifactual increases in cerebral attenuation values) could occur in renal cystic lesions [9]. This pseudoenhancement has been reported in a phantom model; however, to our knowledge it has not been described in patients [7]. Enhancement of 10 H has been widely accepted as the threshold value below which a lesion may be considered nonenhancing. If a cystic lesion enhances more than 10 H, it may be considered indeterminate and potentially require additional imaging, follow-up, or, in more complicated lesions, surgical resection; therefore, a complete understanding of potential pitfalls is critical. Maki et al. [10] reported pseudoenhancement in phantom renal cysts of greater than 10 H. This effect was seen in both spherical and elliptical simulated cysts, the latter nullifying any possibility of volume averaging effect [10]. If similar findings were noted in the clinical setting, there could be wide-ranging implications in the interpretation of renal cystic lesions.

Pseudoenhancement is thought to be a result of beam-hardening effects in conjunction with the image-reconstruction algorithm [7, 9, 10, 11]. This type of beam-hardening artifact has also been referred to as the environmental density artifact. Falsely elevated attenuation values are assigned to an ROI that is surrounded by material that attenuates a polychromatic X-ray beam to a greater degree than that of water. When the lower energy photons of the beam are preferentially attenuated, beam hardening results. CT scanners reconstruct an image from raw data using an algorithm that compensates for the beam hardening that would occur if the body were of uniform water density. Prior studies have shown the environmental density artifact in the brain and in a concentric cylinder model [7, 9]. In the brain, this effect is a result of beam hardening from the calcium-rich calvaria [9]. The effect is larger when close to the inner table and less pronounced in the center of the brain. This latter finding is explained by "cupping," a well-documented artifact relating beam hardening to the increased attenuation of an object near the periphery [12].

Our study confirms the initial report of Maki et al. [10]. Pseudoenhancement of cysts in a contrast bath increases as a function of surrounding iodine concentration. Pseudoenhancement is more pronounced with lower CT beam energies, in smaller spheres, and in peripherally located spheres. Because the phantom is a fixed volume, the larger spheres occupy more room and are proportionately less surrounded by aqueous iodine. The aqueous iodine is responsible for the beam-hardening effect; therefore, larger spheres pseudoenhance less than smaller spheres.

Beam hardening affects a larger percentage of polychromatic X-ray beam energies in a beam with a lower mean energy than in a beam with a higher mean energy; therefore, pseudoenhancement is noticeably greater with lower peak kilovoltage settings. These findings are predictable given past reports of the dependence of CT attenuation values on X-ray beam energy [13]. The cupping artifact could explain why peripherally located spheres pseudoenhance more than centrally located spheres. Cupping also explains the increased pseudoenhancement that occurs as the cyst approaches the periphery of the bath in the small phantom model.

Whereas pseudoenhancement clearly occurs in a phantom model, its clinical relevance cannot be assessed in vitro. However, pseudoenhancement in renal cysts was also found in our retrospective clinical evaluation of presumed simple renal cysts. The clinical study showed a statistically significant increase in cyst attenuation value (mean, 3.4 H) after IV contrast material enhancement. This increase in attenuation was clinically insignificant in most cases (88%), with pseudoenhancement of less than 10 H. However, the other cases did increase by more than 10 H, but none by more than 20 H. Considering that care was taken to avoid volume averaging effects, pseudoenhancement likely accounts for most of the observed attenuation increase. Cysts surrounded by enhancing renal parenchyma are akin to water spheres surrounded by aqueous iodine in the phantom model. Because pseudoenhancement occurs in a phantom model, it is reasonable to suggest that increased attenuation values in the eight renal cysts in our clinical study were a result of a pseudoenhancement component.

Pseudoenhancement requires enough enhancing renal parenchyma neighboring the cyst to produce beam hardening. Large renal cysts tend to displace renal parenchyma and bulge away from the renal surface. This may explain why larger, exophytic cysts do not pseudoenhance as much as smaller, internally located cysts. Our exophytic phantom showed that cysts with only a small area of contact with the contrast bath pseudoenhanced less than internal cysts. This correlates well with our clinical study, during which exophytic cysts pseudoenhanced less than cysts that were either intraparenchymal or only minimally exophytic.

Several limitations to our study should be discussed. First, histopathologic proof was not available for any of the cystic lesions in the clinical study, including the eight lesions with enhancement greater than 10 H. However, these eight lesions were stable on follow-up CT for a mean of 39 months (median, 32 months). Given their other radiographic features and size stability, it is unlikely that these lesions represented neoplasms [14, 15, 16]. Pathologic confirmation for the other 60 cysts was not possible because lesions that meet all criteria for simple cysts generally are not subject to surgical removal. A second potential limitation to our study is that partial volume averaging effects could not be entirely separated from pseudoenhancement effects on the patients' CT images. Our design theoretically precludes volume averaging because examinations were performed during breath-held helical acquisitions and included lesions seen on three contiguous images. Helical slice broadening and undulating contours of the cyst shape could also result in partial volume averaging with enhancing renal parenchyma [17, 18]; however, to avoid volume averaging with cyst margins, care was taken to place the ROI centrally. Furthermore, phantom models designed to completely exclude partial volume averaging still show the pseudoenhancement artifact. As a retrospective clinical study, we were limited by the collimation used in our patient population. Future investigation with the very thin collimation permitted by multislice helical CT scanners may clarify partial volume averaging issues.

In conclusion, pseudoenhancement occurs in both a phantom model and in patients. This effect is greatest when lesions are small or intraparenchymal and when they are imaged at low energies or at peak renal enhancement. Because small cysts are especially prone to both pseudoenhancement and volume averaging artifacts, lesions smaller than 2 cm in diameter should be scanned with narrow collimation and high beam energies. With multislice CT scanners it is possible to image the entire length of the kidneys with thin collimation (1.25-2.50 mm) during peak renal enhancement after the rapid IV administration of iodinated contrast material. Narrow slice profiles may help reduce volume averaging effects; however, the benefits of decreased volume averaging may be confounded by the increasing effects of pseudoenhancement seen in small lesions. If high volumes of contrast material in a tight bolus are used, increased parenchymal enhancement and increasing pseudoenhancement are expected; therefore, pseudoenhancement may preclude accurate characterization even with optimized imaging parameters for smaller, intraparenchymal lesions. Enhancement is only one feature used in the assessment of renal lesions. For example, heterogeneous or focal regions of enhancement in a cystic lesion cannot be dismissed as simple artifacts because these regions can be seen in cystic renal neoplasms. Pseudoenhancement applies only to lesions meeting all other criteria of simple cysts. In certain indeterminate cases, close follow-up or additional evaluation with sonography, MR imaging, or positron emission tomography may be warranted to distinguish these small renal cysts from renal neoplasms [19, 20, 21].

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