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1 Department of Radiology – HB6, The Cleveland Clinic Foundation, 9500
Euclid Ave., Cleveland, OH 44195.
2 The Glickman Urological Institute, The Cleveland Clinic Foundation, Cleveland,
OH 44195.
3 Department of Biostatistics, The Cleveland Clinic Foundation, Cleveland, OH
44195.
4 Present address: Department of Radiology, Weill Hospital, Cornell University
Medical Center, New York, NY.
Received June 24, 2003;
accepted after revision August 28, 2003.
Presented at the 2000 annual meeting of the American Roentgen Ray Society,
Washington, DC.
Abstract
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MATERIALS AND METHODS. A retrospective study of all renal lesions greater than 1 cm that underwent triphasic MDCT was performed in 90 patients before partial nephrectomy. Three reviewers independently measured the mean attenuation of all lesions in three phases (unenhanced, corticomedullary, and parenchymal) in a blinded retrospective fashion. Forty-three lesions identified at CT in 27 patients had pathologic or surgical confirmation as cysts (fluid-filled lesions). Mean change in attenuation between phases was calculated and correlated with size, unenhanced density, and percentage of the lesion exophytic from renal parenchyma. All scans were obtained after 150 mL of nonionic contrast material was injected at 3 mL/sec. Scanning delays were 30–40 sec (corticomedullary phase) and 120 sec (parenchymal phase).
RESULTS. The mean change in attenuation coefficient of the cysts from the unenhanced to the parenchymal phase was –1.8 H (SD, ± 4.4 H); from the unenhanced to the corticomedullary phase was –2.3 H (± 3.9 H); and from the corticomedullary to the parenchymal phase was 0.6 H (± 4.2 H). No cyst increased more than 10 H between the unenhanced and the parenchymal phases; more than 95% of cysts increased less than 8 H between any scanning phases. No significant difference was seen in enhancement related to lesion size (p > 0.054), unenhanced attenuation (p > 0.255), or percentage of the lesion that was exophytic (p > 0.124).
CONCLUSION. The attenuation coefficient of a cystic renal lesion increased by no more than 10 H among the unenhanced, corticomedullary, and parenchymal phase scans.
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One of the fundamental suppositions in this classification system is that a clear delineation exists between lesions that enhance and those that do not enhance (cystic vs solid). Bosniak [1] reported that 10 H was a useful divider at which enhancement can be reliably determined. However, some studies have shown that cysts may in fact change by more than 10 H between unenhanced and early or delayed phases of enhancement [6, 7]. The studies reported that these attenuation changes are more pronounced in small or intrarenal cysts [6–9]. Even with strict numeric criteria for enhancement, disagreement about enhancement of renal lesions still occurs, particularly in the case of small (1.0–1.5 cm) cysts [10].
No study, to our knowledge, has defined a normal range of attenuation change on triphasic (unenhanced, vascular, and nephrographic phases) renal MDCT using only histologically or surgically proven cystic lesions. Without defining the "normal" population, it is difficult to establish whether a given numeric change in Hounsfield units may be the result of enhancement or of other factors such as volume averaging artifacts or pseudoenhancement [6–9]. Such uncertainty could result in the mischaracterization of a simple renal cyst as an enhancing mass and lead to further studies or unnecessary surgery. Conversely, a stricter criterion for enhancement of more than 10 H may result in hypovascular tumors being mistakenly characterized as cysts. The purpose of this study is to document the range of normal attenuation changes among all three scanning phases using only histologically or surgically proven renal cystic lesions. Any change in attenuation value above the "normal" should be therefore viewed with concern as representing true enhancement and therefore a solid hypovascular mass (after assessing for factors that may lead to pseudoenhancement). Statistical analysis was also used to determine whether any correlation exists among the measured attenuation changes and cyst size, baseline attenuation, or percentage of the lesion that is exophytic from the kidney.
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Thirty-three (37%) of 90 patients had at least one such cystic benign-appearing lesion on CT that was measured in the kidney at surgery (cystic masses seen at CT on the nonsurgical side were not included in the study). Two patients with von Hippel-Lindau disease were eliminated from this group of 33 because all cystic and solid lesions in patients with von Hippel-Lindau disease should be treated as potentially malignant regardless of size and appearance. No calcified or septate lesions were identified at CT in the remaining group of 31 patients.
The three reviewers documented 52 cystic benign-appearing lesions in these 31 patients. Nine (17%) of these 52 lesions were eliminated for the following reasons: four lesions (in four patients) measured at CT had no mention of a renal cyst at surgery or in the pathology specimen. In four patients, five of 16 lesions seen on CT were not identified at surgery or histologically. Therefore, 43 cysts in 27 patients that were identified on CT and that had histologic (n = 38) or surgical (n = 5) correlation were included in the final study population. In one patient, two cysts were documented at histology, but only one was recorded on CT as being greater than 1 cm.
Of the 27 patients included in this study, 23 were referred for enhancing solid masses on CT. Twenty of these 23 patients had renal cell carcinoma at pathology, and three had oncocytoma. Three patients were referred for suspicious cystic lesions on CT, and all three had renal cell carcinoma at pathology. One patient was referred for a large angiomyolipoma on CT that was subsequently confirmed at pathology.
CT Protocol
All scans were obtained using a triphasic renal helical CT protocol on a
Somatom Plus 4 scanner (Siemens Medical Solutions, Forchheim, Germany) at 120
kVp and 0.75-sec revolution time. No oral contrast material was administered.
First, unenhanced CT of the kidneys was performed at 5-mm collimation and a
pitch of 1 (table speed, 5 mm per revolution) at 200–240 mAs.
Next, a test bolus of 20 mL nonionic contrast material (Ultravist 300 [iopromide], Berlex, Wayne, NJ) injected at 3 mL/sec was used to calculate the delay time for the corticomedullary phase. A single slice was obtained in the upper abdominal aorta, and images were obtained every second starting at 10 sec, for a total of 40 sec. A region of interest (ROI) was placed over the aorta and the time to peak enhancement was calculated. The delay for the corticomedullary phase was the time to peak aortic enhancement plus an additional 5 sec to allow venous opacification. The corticomedullary phase scan was obtained using the delay time calculated as stated after a 2-min delay to allow filling of the collecting system. One hundred twenty milliliters of contrast material was then injected at 3 mL/sec. The scan was obtained at 3-mm collimation and a pitch of 1.0–1.7 (table speed, 3–5 mm per revolution) at 240 mAs.
A parenchymal phase scan was then obtained using a 140-sec delay from the initiation of the bolus contrast injection. The scan was obtained at 5-mm collimation and a pitch of 1 (table speed, 5 mm per revolution). All scans were reconstructed with a 50% image overlap. All scans were reviewed on a PACS workstation (MagicView 1000, Siemens Medical Solutions).
Analysis of CT Lesions
Three radiologists who were unaware of final pathology and operative
reports independently and retrospectively recorded the largest diameter,
location, and Hounsfield unit attenuation (± SD) from an ROI in any
lesion greater than or equal to 1.0 cm in diameter. The reviewers were
instructed to maximize the ROI and to keep the ROI size and location the same
among all three scanning phases. Lesion location (anterior, posterior, or
apical; interpolar or basilar; medial or lateral) was recorded to assist in
identification of all lesions among reviewers and with the operative reports.
One reviewer retrospectively at a later review recorded the component of each
lesion that was exophytic from the kidney (qualitatively recorded as
0–25%, 25–50%, 50–75%, or 75–99%).
Statistical Methods
A total of 129 measures of lesion attenuation were made from the three
scanning phases by the three reviewers, who each measured 43 lesions. The mean
change in attenuation among the three phases was computed and averaged over
the three reviewers. The SDs of the change between phases were estimated from
a fitted analysis of variance model using software (SAS, Cary, NC) that
treated cysts as units nested within patients. When repeated measures analysis
of variance was used, the attenuation change between phases was examined for
trends, with unenhanced attenuation categorized as less than or equal to 20 H
and greater than 20 H (Bosniak classification I and II cysts), lesion size
(
or > 2 cm), and lesion location within or exophytic from the kidney
as already described. We took the average of the three reviewers' size
measurements as the estimate of the size of each cyst. The significance level
used was a p value of less than 0.05. We assessed the interreviewer
variability by computing the absolute value of the difference among reviewers'
measurements of the changes in attenuation between scanning phases.
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The mean diameter of all lesions was 2.9 cm (SD, ± 1.7 cm; range, 1.0–6.6 cm). Twenty-five lesions had an average density of less than or equal to 20 H on the unenhanced CT scans (Bosniak classification I); the remaining 18 lesions had densities greater than 20 H (hyperdense cysts, Bosniak classification II). Twenty-three (53%) of 43 cysts were at least 50% exophytic from the kidney.
Change in Attenuation Between Scanning Phases
The mean change in attenuation from the unenhanced to the parenchymal phase
was –1.8 H (± 4.4 H). Only 32 (24.8%) of 129 measures of cyst
attenuation showed a positive change, none more than 10 H. Ninety-five percent
of the cysts showed a change of less than 7 H
(Fig. 1).
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The mean change in attenuation from the unenhanced to the corticomedullary phase was –2.3 H (± 3.9 H). Only 26 (20.2%) of 129 measures of cyst attenuation showed a positive change in attenuation, and none was more than 10 H. Ninety-five percent of the cysts showed a change of less than 5 H (Fig. 2).
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The mean change in attenuation from the corticomedullary to the parenchymal phase was 0.6 H (± 4.2 H), and 71 (56%) of 126 measures of cyst attenuation showed a positive change. Ninety-five percent of the cysts showed a change of less than 8 H (Fig. 3). Overall, two reviewers reported a change of greater than 10 H for two cysts.
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To assess interobserver variability, we calculated the average difference among reviewers for all three scanning phases. These differences were 4.1, 2.4, and 3.4 H for the unenhanced to the parenchymal, unenhanced to corticomedullary, and corticomedullary to parenchymal scanning phases, respectively. These changes in attenuation among reviewers were no larger than the differences measured between scanning phases for all reviewers.
Change in Attenuation Relative to Cyst Size
Attenuation changes were evaluated with respect to cyst size. The mean
changes in attenuation were small for cysts of 1–2 cm (n = 15)
and those greater than 2 cm (n = 28) in each respective phase. From
the unenhanced to the corticomedullary phase, the respective mean change was
–2.3 H for cysts of 1–2 cm versus –2.3 H for those greater
than 2 cm (p = 0.729); from the unenhanced to the parenchymal phase,
–2.8 H versus –1.2 H (p = 0.085); and from the
corticomedullary to the parenchymal phase, –0.5 versus 1.1 H (p
= 0.054).
Change in Attenuation Relative to Unenhanced Attenuation
Attenuation changes were evaluated with respect to baseline attenuation. No
significant difference was seen in the change of attenuation between scanning
phases among cysts with unenhanced attenuation of less than or equal to 20 H
(n = 25) compared with those having attenuation greater than 20 H
(n = 18) in each phase. From the unenhanced to the corticomedullary
phase, the respective mean change was –2.5 H for cysts having an
unenhanced attenuation value of less than or equal to 20 H, versus –2.0
H for cysts having an unenhanced attenuation value of greater than 20 H
(p = 0.903); from the unenhanced to the parenchymal phase, –2.2
H versus –1.2 H (p = 0.344); and from the corticomedullary to
the parenchymal phase, 0.4 versus 0.8 H (p = 0.255).
Change in Attenuation Relative to Lesion Location
Attenuation changes were evaluated with respect to lesion location of
0–25%, 25–50%, 51–75%, or 75–99% of the diameter being
exophytic from the kidney. No significant difference was seen in the change in
attenuation among categories between scanning phases (p > 0.081)
(Table 1).
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Characteristics of the Seven Potentially Neoplastic Cystic Lesions
As noted, seven cystic masses in four patients met Bosniak CT criteria for
benign (classification I or II) cysts but had microscopic evidence at
pathology that was suggestive of neoplasm in the wall of the cyst
(Table 2). All seven lesions
had unenhanced attenuation greater than 20 H (Bosniak classification II
cysts). The average size was 4.3 cm (range, 2.0–5.6 cm), the unenhanced
attenuations ranged from 25 to 58 H, and none increased by more than 9 H
between any of the scanning phases for any reviewer.
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However, the cutoff of 10 H has been recently challenged, with volume-averaging and beam-hardening compensatory mechanisms in the reconstruction algorithms frequently cited as causes of larger changes in attenuation measurements in small renal cysts. Changes in enhancement of more than 10 H in cysts has been termed "pseudoenhancement." This term refers to the artifactual increase in CT attenuation of a cyst after the administration of iodinated contrast material [6]. Briefly, pseudoenhancement is thought to be the result of beam-hardening effects in conjunction with corrections in the CT image reconstruction algorithm [14, 15]. Pseudoenhancement may in part be due to helical CT reconstruction algorithms, which may be the reason that pseudoenhancement was not reported with conventional CT scanners. Pseudoenhancement effects have been reported to increase with increasing background attenuation and decreasing cyst size and are usually more pronounced in intraparenchymal than in exophytic cysts [6].
Several studies have assessed pseudoenhancement. Siegel et al. [10] reported observer disagreement on whether enhancement was present in cases of 1.0- to 1.5-cm lesions despite using 15 H as a minimum for defining enhancement. Coulam et al. [6] studied both phantom and patient cysts and reported that eight of 31 cysts smaller than 2 cm in the patient group increased by 10–20 H but none larger than 2 cm increased by more than 10 H. This phenomenon did not occur in our study for cysts smaller than 2 cm. Coulam et al. reported that only one of the 30 exophytic cysts studied showed pseudoenhancement of more than 10 H. In other studies of pseudoenhancement, Maki et al. [7] reported pseudoenhancement in phantom renal cysts of as much as 18–28 H in cysts smaller than 1 cm and of 10–15 H in cysts larger than 1 cm. Bae et al. [15] studied 48 cysts in 24 patients with sonographic documentation of simple cysts and found that none of the cysts larger than 1.0 cm showed an attenuation increase of more than 10 H.
To our knowledge, ours is the first study to use only pathologically and surgically proven cysts in evaluating these normal attenuation changes on triphasic renal helical CT. The attenuation of most (95%) of the cysts in our study increased by less than 8 H between scanning phases. In fact, many cysts in our study decreased in attenuation after the administration of contrast material, possibly as a result of beam hardening from adjacent enhanced renal tissue. Therefore, our study supports the use of 10 H as a threshold for lack of enhancement. It confirms the findings of Coulam et al. [6] in exophytic cysts and cysts larger than 2 cm, and the findings of Bae et al. [15] for cysts larger than 1 cm. We also found no difference in attenuation changes between cystic lesions that were intrarenal or exophytic, lesions that were less than or greater than 20 H on the unenhanced phase, or lesions that were greater than 2 cm and those of 1–2 cm.
Our study has several limitations. First, the study does not provide a value for what determines enhancement but rather determines "normal" behavior for cystic lesions at CT and thereby sets a threshold above which enhancement must be considered a likely possibility. Other limitations are our small sample size and the lack of assessment of intraobserver variation. We found no significant interobserver variation, however, and these limitations are similar to those of other reports [2, 15]. Another limitation is that CT techniques have changed with the introduction of MDCT scanners, particularly eight- and 16-row scanners. Most institutions, including ours, currently scan at a collimation of 2.5 mm or less and reconstruct at 1- or 3-mm slice thickness. The attenuation of small lesions may also depend on image reconstruction algorithms; thus, our results do not necessarily apply to all CT scanners and current state-of-the-art CT protocols.
Finally, our study included four patients with seven cystic masses that met Bosniak CT criteria for benign (classification I or II) cysts but had pathologic evidence suggestive of neoplasm in the wall of the cyst. We chose to include those masses in the study because they were surgically and pathologically cysts, filled with fluid, not solid tissue, and therefore were truly cystic lesions with microscopic findings. In fact, the pathologic identification of clusters of clear cells in the cyst wall does not necessarily imply malignancy. Three of the four patients, encompassing six of the seven cystic tumors, had multiple partially cystic or necrotic tumors, including the primary lesion at surgery; these patients may need to be followed up more closely. The finding of potential malignancy in hyperdense cysts also underscores the need to follow up hyperdense renal cysts at least initially and supports Siegel et al. [2] in confirming that a small percentage of Bosniak classification II lesions are neoplastic. One limitation of our study is that one or more of the five cysts that were reported as benign at surgery may have also had a microscopic tumor in the wall. We cannot explain why some surgeons did not send the cyst wall to pathology in these patients but did in others.
This study shows that cystic lesions typically reveal a change in attenuation of less than 10 H between the scanning phases of a triphasic MDCT, affirming Bosniak's initial assertion that 10 H is a reasonable cutoff for determining enhancement in renal lesions. We found this to be true regardless of cyst size, location, or baseline attenuation. If a lesion shows a change in attenuation of more than 10 H after the lesion size and location are considered for the possibility of volume averaging and pseudoenhancement, the lesion should be viewed with suspicion and thought likely to be a hypovascular but enhancing and therefore solid renal neoplasm. Further work needs to be done using current state-of-the-art protocols on MDCT scanners and MDCT reconstruction algorithms.
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