Analysis of Changes in Attenuation of Proven Renal Cysts on Different Scanning Phases of Triphasic MDCT

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1 Eugene P. Chung 1 Brian R. Herts 1,2 Grant Linnell 1 Andrew C. Novick 2 Nancy Obuchowski 1,3 Deirdre M. Coll 1,4 Mark E. Baker 1 Received June 24, 2003; accepted after revision August 28, Presented at the 2000 annual meeting of the American Roentgen Ray Society, Washington, DC. 1 Department of Radiology HB6, The Cleveland Clinic Foundation, 9500 Euclid Ave., Cleveland, OH Address correspondence to B. R. Herts (hertsb@ccf.org). 2 The Glickman Urological Institute, The Cleveland Clinic Foundation, Cleveland, OH Department of Biostatistics, The Cleveland Clinic Foundation, Cleveland, OH Present address: Department of Radiology, Weill Hospital, Cornell University Medical Center, New York, NY. AJR 2004;182: X/04/ American Roentgen Ray Society Analysis of Changes in Attenuation of Proven Renal Cysts on Different Scanning Phases of Triphasic MDCT OBJECTIVE. The purpose of this study is to document changes in attenuation values on triphasic MDCT of histologically or surgically proven cystic renal lesions. 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 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. D ifferentiating benign cystic lesions of the kidney from those that require surveillance or surgical exploration remains a common problem. The introduction of the Bosniak classification [1] in 1986 provided radiologists with a practical method of analyzing these lesions, and its usefulness has been confirmed in subsequent studies [2, 3]. This classification system is widely used by radiologists and urologists because of its simplicity and practicality. For the most part, this classification system has withstood the test of time. However, it has also been modified and updated since its original description, which is further evidence of the difficulty characterizing some complex cystic renal lesions [4, 5]. 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 ( 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 pop- AJR:182, February

2 Chung et al. ulation, 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. Materials and Methods Patient Population Three radiologists, in a blinded and retrospective fashion, measured Hounsfield unit attenuation and SD on all lesions (cystic or solid-appearing at CT) having a diameter greater than 1 cm in 90 consecutive patients who underwent three-phase renal MDCT during a 9-month period at our institution. Institutional review board approval was obtained for medical chart review. These scans were obtained as a preoperative evaluation before potential partial nephrectomy, and this study was performed in conjunction with a previously reported study [11]. The operative notes were reviewed for mention of any cystic lesion and its location if more than one such lesion was present. Pathology reports were reviewed for histologic confirmation of cystic lesions and final pathology findings. CT findings were correlated with the operative notes and pathology reports. Only those lesions at CT that were homogeneous, had no septations or calcifications (meeting CT criteria for Bosniak classification I or II hyperdense cysts), and had histologic and surgical confirmation as a cystic (fluid-containing) lesion were included in the final study group. 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 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 (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 We assessed the interreviewer variability by computing the absolute value of the difference among reviewers measurements of the changes in attenuation between scanning phases. Results Cyst Population Thirty-eight (88%) of the 43 lesions had histologic confirmation as cystic lesions. Of these 38 lesions, 31 were benign epithelial cysts, and seven had either incipient renal cell carcinoma in the cyst wall (n = 4) or scattered clear cells, suspicious for carcinoma in the cyst wall (n = 3). Only one report provided a size measurement of 0.3 mm for the suspected tumor; none had gross tumor at pathology. These seven lesions are discussed in more de- 406 AJR:182, February 2004

3 CT of Renal Cysts tail in the following text. The remaining five (12%) of 43 lesions had confirmation as cysts (fluid-containing) in the operative report but no histologic confirmation. The mean diameter of all lesions was 2.9 cm (SD, ± 1.7 cm; range, 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. Fig. 1. Attenuation change from unenhanced to parenchymal phase. Bar graph shows percentage of all cysts with respective attenuation changes between these phases. Ninety-five percent (vertical line) of all attenuation changes were less than 7 H. Fig. 2. Attenuation change from unenhanced to corticomedullary phase. Bar graph shows percentage of all cysts with respective attenuation changes between these phases. Ninety-five percent (vertical line) of all attenuation changes were less than 5 H. 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. Ninetyfive percent of the cysts showed a change of less than 7 H (Fig. 1). 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 Cysts (%) Cysts (%) H. Ninety-five percent of the cysts showed a change of less than 5 H (Fig. 2). 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. To assess interobserver variability, we calculated the average difference among reviewers for all three scanning phases. These Change in Attenuation (H) Change in Attenuation (H) AJR:182, February

4 Chung et al. 12 Fig. 3. Attenuation change from corticomedullary to parenchymal phase. Bar graph shows percentage of all cysts with respective attenuation changes between these phases. Ninety-five percent (vertical line) of all attenuation changes were less than 8 H. 10 Cysts (%) 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). TABLE 1 Change in Attenuation (H) Note. Data are mean changes in attenuation given in Hounsfield units. a No significant difference was seen in attenuation between groups (significant at p < 0.05). 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%, Change in Attenuation (H) Correlated with Percentage of Cyst Exophytic from Renal Parenchyma Scanning Phases 0 25 (n = 15) (n = 4) % Exophytic (n = 10) (n = 13) Unenhanced to parenchymal Unenhanced to corticomedullary Corticomedullary to parenchymal p a 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). 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, 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. Discussion In 1986, Bosniak [1] introduced a classification system that separated cystic renal lesions into benign, likely benign, indeterminate, and malignant categories based on specific CT features. The system has since been updated and revised [4, 5]. The basic classification system is well known and need not be restated here. However, we reiterate that Bosniak suggested a cutoff of 10 H for distinguishing nonenhancing and therefore cystic lesions from enhancing and therefore solid lesions. This cutoff has been supported by several observational studies that used few or no patho- 408 AJR:182, February 2004

5 CT of Renal Cysts logically proven cysts, instead using stability or sonographic features as confirmation of a cystic nature [12, 13]. 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 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 H in cysts smaller than 1 cm and of 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 TABLE 2 Characteristics of Seven Cysts in Four Patients with Suspicious Findings at Pathology or Microscopic Tumor in Cyst Wall Patient Cyst Size (cm) Unenhanced Attenuation (H) Largest Change (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 stateof-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. AJR:182, February

6 Chung et al. References 1. Bosniak MA. The current radiological approach to renal cysts. Radiology 1986;158: Siegel CL, McFarland EG, Brink JA, Fisher AJ, Humphrey P, Heiken JP. CT of cystic renal masses: analysis of diagnostic performance and interobserver variation. AJR 1997;169: Curry NS, Cochran ST, Bissada NK. Cystic renal masses: accurate Bosniak classification requires adequate renal CT. AJR 2000;175: Bosniak MA. Difficulties in classifying cystic lesions of the kidney. Urol Radiol 1991;13: Bosniak MA. Problems in the radiologic diagnosis of renal parenchymal tumors. Urol Clin North Am 1993:20: Coulam CH, Sheafor DH, Leder RA, Paulson EK, DeLong DM, Nelson RC. Evaluation of pseudoenhancement of renal cysts during contrast-enhanced CT. AJR 2000;174: Maki DD, Birnbaum BA, Chakraborty DP, Jacobs JE, Carvalho BM, Herman GJ. Renal cyst pseudoenhancement: beam-hardening effects on CT numbers. Radiology 1999;213: Bosniak MA. The small (<3.0 cm) renal parenchymal tumor: detection, diagnosis, and controversies. Radiology 1991;179: Bosniak MA, Rofsky NM. Problems in the detection and characterization of small renal masses. Radiology 1996;198: Siegel CL, Fisher AJ, Bennett HF. Interobserver variability in determining enhancement of renal masses on helical CT. AJR 1999;172: Herts BR, Coll DM, Novick AC, et al. Enhancement characteristics of papillary renal neoplasms revealed on triphasic helical CT of the kidneys. AJR 2002;178: Coleman BG, Arger PH, Mintz MC, Pollack HM, Banner MP. Hyperdense renal masses: a computed tomographic dilemma. AJR 1984;143: Zirinsky K, Auh YH, Rubenstein WA, Williams JJ, Pasmantier MW, Kazem E. CT of the hyperdense renal cyst: sonographic correlation. AJR 1984;143: Rao PS, Alfidi RJ. The environmental density artifact: a beam-hardening effect in computed tomography. Radiology 1981;141: Bae KT, Heiken JP, Siegel CL, Bennett HF. Renal cysts: is attenuation artifactually increased on contrast-enhanced CT images? Radiology 2000; 216: AJR:182, February 2004

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