DOI: 10.1148/radiol.2431051924
(Radiology 2007;243:158-165.)
© RSNA, 2007
Complex Cystic Renal Masses: Characterization with Contrast-enhanced US1
Giorgio Ascenti, MD,
Silvio Mazziotti, MD,
Giovanni Zimbaro, MD,
Nicola Settineri, MD,
Carlo Magno, MD,
Darwin Melloni, MD,
Rosario Caruso, MD and
Emanuele Scribano, MD
1 From the Department of Radiological Sciences (G.A., S.M., G.Z., N.S., E.S.), Clinic of Urology (C.M., D.M.), and Department of Pathology (R.C.), University of Messina, via Consolare Valeria-Gazzi, 98100 Messina, Italy. Received November 26, 2005; revision requested January 19, 2006; revision received February 22; accepted March 10; final version accepted August 23.
Address correspondence to S.M. (e-mail: smazziotti{at}unime.it).
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ABSTRACT
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Purpose: To prospectively compare contrast material–enhanced ultrasonography (US) with computed tomography (CT) in the classification of complex cystic renal masses with the Bosniak system.
Materials and Methods: Ethics committee approval and written informed consent were obtained. Forty patients (17 women, 23 men; age range, 31–77 years) with 44 complex cystic renal masses detected with conventional US were prospectively examined by using second-harmonic US with a second-generation contrast agent and multiphasic helical CT. Thirty-six patients had one lesion, and four patients had two lesions. Surgical resection in nine patients and imaging follow-up in 31 patients were used to determine the outcome.
Results: On contrast-enhanced US images, masses were classified as Bosniak category II (n = 18), IIF (ie, lesions were classified as category II and follow-up was needed) (n = 16), III (n = 7), or IV (n = 3) lesions. On CT images, masses were classified as Bosniak category II (n = 24), IIF (n = 10), III (n = 7), or IV (n = 3) lesions. Interobserver agreement was high (
= 0.86, P < .001) for classification with US. Complete concordance between the readers was found for classification with CT. Complete concordance between contrast-enhanced US and CT was observed in the differentiation of surgical and nonsurgical complex cysts. Complete concordance among the three readers in the assessment of vascularity with contrast-enhanced US was found. Interobserver agreement in the evaluation of enhancement on CT images was high ( = 0.88, P < .001). Concordance between contrast-enhanced US and CT in the evaluation of vascularization was high ( = 0.77, P < .001).
Conclusion: The study data suggest that contrast-enhanced second-harmonic US is appropriate for renal cyst classification with the Bosniak system.
© RSNA, 2007
Approximately 10% of all renal cell carcinomas appear as complex cystic lesions on images. On the other hand, nonmalignant renal cysts can have a complex appearance, usually as a result of hemorrhage, infection, inflammation, or ischemia (1,2).
Differentiating between complex cystic renal masses that require surgery and those that do not remains a common and difficult diagnostic problem (3). The Bosniak system for classification of renal cysts evolved over time, and on the basis of computed tomographic (CT) criteria, it has been largely accepted. It has been used by urologists and radiologists as an effective tool in the characterization of cystic renal masses (4–9).
Although renal cysts are usually discovered during an ultrasonographic (US) abdominal examination, one should not rely on US when differentiating between surgical and nonsurgical complex cystic renal masses, and further examination with contrast material–enhanced CT or magnetic resonance (MR) imaging is required (8–11). This lack of diagnostic accuracy is mainly due to the absence of contrast material, considering that the enhancement of the solid components of a cyst represents a crucial factor in the decision to remove or follow up a lesion (1,7,12).
Today, harmonic US performed with second-generation contrast agents has revealed promising perspectives in the diagnosis of renal masses (13–16). Thus, the purpose of our study was to prospectively compare contrast-enhanced US with CT in the classification of complex cystic renal masses with the Bosniak system.
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MATERIALS AND METHODS
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Patients
Between March 2001 and January 2004, all patients referred to our institution with a complex cystic renal mass were prospectively examined with contrast-enhanced US and triple-phase helical CT. Patients were enrolled in this study on the basis of conventional US findings. Patients with simple cysts that had a hairline-thin wall and anechoic content without septa or calcifications (Bosniak category I cysts) were excluded.
This study included 44 complex cystic renal masses in 40 consecutive patients (17 women, 23 men; age range, 31–77 years). Thirty-six patients had one lesion, and four patients had two lesions. Asymptomatic complex renal cysts were incidentally detected with abdominal US performed to assess other abdominal diseases in 39 of the patients. Microscopic hematuria, fever, and right flank pain were present in one patient. Approval of the ethics committee of our institution and written informed consent were obtained.
Imaging Technique
All US examinations were performed by two authors (G.A., G.Z.), who had 15 and 25 years of experience, respectively, in abdominal US, by using Esatune or Technos MPX scanners (Esaote, Genoa, Italy), which are dedicated second-generation contrast agent machines that were equipped with contrast-tuned imaging real-time contrast-specific software (CnTI; Esaote) that produces images on the basis of maintenance of microbubbles at low acoustic pressure and subtraction imaging techniques. A convex, phased-array 2–7-MHz transducer was used.
Harmonic US with real-time contrast-tuned imaging software was performed by switching the scanner to the contrast-specific mode with the press of a button on the console. The second-generation contrast agent (SonoVue; Bracco, Milan, Italy) consisted of an aqueous suspension of stabilized sulfur hexaflouride microbubbles with a phospholipidic shell and was approved for clinical radiologic use in Europe.
A 2.4-mL dose of contrast material was injected rapidly through an antecubital vein and immediately followed by a 10-mL flush of saline solution (0.9% NaCl). A double dose of contrast material was administered in 16 patients so that we could evaluate lesion perfusion in a different US study. Examination of renal mass perfusion was evaluated in real time during the corticomedullary and nephrographic phases until 3–4 minutes after the beginning of the injection. In the contrast-specific second-harmonic scanning mode, acoustic pressure ranged from 0.35 to 0.55 kPa to minimize breakage of microbubbles. A digital video clip of the entire examination was stored on the hard disk of the US scanner.
Within 1–7 days after contrast-enhanced US, all patients underwent multiphasic helical CT performed with either a single–detector row scanner (Somatom Plus 4; Siemens, Erlangen, Germany) (n = 9) or a multi–detector row scanner (Somatom Sensation 16; Siemens) (n = 31). A section collimation of 5 mm and a pitch factor of 1.5 were routinely used with the single–detector row scanner, and dedicated thinner sections of 3 mm were adopted for small masses. Multi–detector row CT data sets were acquired with a collimaton of 16 x 1.5 mm and were reconstructed to 4-mm-thick sections.
Unenhanced images were acquired first. Thereafter, contrast-enhanced images were obtained in the corticomedullary (25–30 seconds), nephrographic (85–100 seconds), and excretory (8–13 minutes) phases after the beginning of injection of 120–140 mL (300 mg of iodine per milliliter) of nonionic iodinated contrast material (Xenetix; Guerbet, Aulnay-sous-Bois, France) at a rate of 2–3 mL/sec.
Image Interpretation and Analysis
A digital video clip of the entire study, including the preliminary basal US images, was stored on the hard disk of the US scanner, and dynamic images were viewed on the US unit. All triple-phase helical CT images were evaluated on the computer console, with adjustment of the optimal window settings in each case.
All US and CT images were interpreted by three independent dedicated abdominal radiologists (S.M., E.S., N.S.) with 15, 25, and 10 years of experience in urologic imaging. These readers were blinded to clinical and laboratory findings and other imaging information. The US and CT images were reviewed in individual sessions separated by 3-week intervals. For both imaging techniques, each observer evaluated the (a) size of each focal lesion, (b) wall thickness, and (c) presence of septa (few or multiple septa), calcifications, and solid endocystic components.
The presence of contrast enhancement of the wall, septa, or solid endocystic components was assessed with side-by-side comparison of unenhanced and contrast-enhanced images. Moreover, enhancement of solid endocystic components was assessed by measuring the region of interest on CT images; when regions of interest were measured, enhancement was considered present when attenuation increased by more than 15 HU (1).
On contrast-enhanced US images, the presence of vascularization was based on visual impressions because with our instrumentation it was impossible to perform quantitative analysis. Vascularization was considered present when hyperechoic signals became evident in the lesion during real-time observation (13–15). On the basis of morphologic findings and characteristics of enhancement, the readers classified each lesion with the Bosniak classification system (Table 1) (8,9,12).
Outcome
Surgical resection and imaging follow-up were used to determine outcome. Nine patients underwent surgery, and 31 underwent follow-up; 16 patients were followed up with CT alone, and the remaining 15 were followed up with conventional US and CT for a minimum of 12 months and a maximum of 24 months. All follow-up examinations were performed with the same technique used in the initial study. Follow-up images were reviewed by the same readers in consensus. The criteria used to assess stability were the lack of an increase in the size of the mass (measured on transverse CT images) and the absence of morphologic and contrast-enhanced modifications. Histologic diagnosis was obtained for each surgical specimen.
Statistical Analysis
The Cohen statistic was used to analyze agreement between the diagnostic procedures. Interobserver agreement among the three dedicated abdominal radiologists was also evaluated with the Cohen statistic (17). Agreement was considered fair to good if values were between 0.40 and 0.75 and high if values were greater than 0.75 (18).
The Genmod procedure (SAS Institute, Cary, NC) with repeated statement generalized estimating equations was used as the standard method to exclude any interaction in the four patients with two lesions.
Sample size was determined with the assumption of an estimated accuracy of 85% and a 95% confidence interval of ± 10% (19). All statistical analyses were performed with SPSS, version 10.0, software (SPSS, Chicago, Ill). A P value of less than .05 was considered to indicate a statistically significant difference.
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RESULTS
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The maximum diameter of the 44 complex cystic renal masses ranged from 1 to 7 cm (mean diameter, 3.5 cm). Wall thickness was clearly evaluated with CT and contrast-enhanced US. More intracystic septa were identified with US than with CT in six lesions. No calcifications were identified with either technique.
Bosniak Category
Lesions seen on contrast-enhanced US images were classified as Bosniak category II (n = 18), IIF (n = 16), III (n = 7), or IV (n = 3, Table 2). Lesions seen on CT images were classified as Bosniak category II (n = 24), IIF (n = 10), III (n = 7), or IV (n = 3).
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Table 2. Comparison between Contrast-enhanced US and Triple-Phase Helical CT in Bosniak Classification Category and Depiction of Contrast Enhancement of 44 Complex Cystic Renal Masses
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The final diagnoses of nine renal masses (six category III lesions and three category IV lesions) in which pathologic diagnosis was made at surgery were as follows: Five masses were cystic renal cell carcinomas, two were inflammatory cysts, one was xanthogranulomatous pyelonephritis, and one was multilocular cystic renal cell carcinoma. One patient with an indeterminate complex cyst (classified as a Bosniak category III lesion) refused to undergo surgery and remained stable at 18-month follow-up.
In the remaining 34 cystic masses (classified as Bosniak category II or IIF lesions) in 30 patients in whom diagnosis was obtained by means of follow-up, no malignancies were identified for 12–24 months.
Agreement
Regarding classification with the Bosniak system, interobserver agreement was high when US was used ( = 0.86, P < .001); however, complete concordance between the three readers was found when CT was used ( = 1.00, P < .001).
A disagreement with regard to Bosniak classification between contrast-enhanced US and triple-phase spiral CT occurred in six (14%) of the 44 lesions. All of these lesions demonstrated more intracystic septa at US than at CT. All of the lesions were considered category IIF lesions at US; however, at CT four lesions were considered category I and two were considered category II (Fig 1).
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Figure 1a: Complicated benign cystic renal mass (stable at 18-month follow-up) in a 64-year-old man. (a) Transverse baseline US image of the left kidney shows well-defined, 2-cm multiloculated cystic mass (*) with several thin septa. (b) Transverse contrast-enhanced US image obtained in the contrast-specific mode with contrast-tuned imaging. The software suppresses tissue background, with almost complete cancellation of intracystic septa. Absence of enhancement is seen during the nephrographic phase. This cyst was classified as a Bosniak IIF lesion. Note the presence of a large endosinusal simple cyst (C). (c) Transverse contrast-enhanced CT image obtained during the nephrographic phase. Both endosinusal and cortical masses appear as simple cysts (Bosniak category I lesions).
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Figure 1b: Complicated benign cystic renal mass (stable at 18-month follow-up) in a 64-year-old man. (a) Transverse baseline US image of the left kidney shows well-defined, 2-cm multiloculated cystic mass (*) with several thin septa. (b) Transverse contrast-enhanced US image obtained in the contrast-specific mode with contrast-tuned imaging. The software suppresses tissue background, with almost complete cancellation of intracystic septa. Absence of enhancement is seen during the nephrographic phase. This cyst was classified as a Bosniak IIF lesion. Note the presence of a large endosinusal simple cyst (C). (c) Transverse contrast-enhanced CT image obtained during the nephrographic phase. Both endosinusal and cortical masses appear as simple cysts (Bosniak category I lesions).
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Figure 1c: Complicated benign cystic renal mass (stable at 18-month follow-up) in a 64-year-old man. (a) Transverse baseline US image of the left kidney shows well-defined, 2-cm multiloculated cystic mass (*) with several thin septa. (b) Transverse contrast-enhanced US image obtained in the contrast-specific mode with contrast-tuned imaging. The software suppresses tissue background, with almost complete cancellation of intracystic septa. Absence of enhancement is seen during the nephrographic phase. This cyst was classified as a Bosniak IIF lesion. Note the presence of a large endosinusal simple cyst (C). (c) Transverse contrast-enhanced CT image obtained during the nephrographic phase. Both endosinusal and cortical masses appear as simple cysts (Bosniak category I lesions).
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Concordance between contrast-enhanced US and triple-phase helical CT was high ( = 0.79; range, 0.73–0.86). Complete concordance in Bosniak grading was observed in the differentiation of surgical and nonsurgical complex cysts ( = 1.00, P < .001).
Contrast-enhanced US depicted vascularization in 14 (32%) of 44 lesions (four category IIF lesions, seven category III lesions, and three category IV lesions). These findings were confirmed with CT in 10 (23%) of the lesions (one category IIF lesion, six category III lesions, and three category IV lesions) and were considered doubtful (attenuation increase <15 HU after contrast agent administration) in two lesions (one category IIF lesion and one category III lesion) (Fig 2). In two category IIF cysts, vascularization of a thin and regular endocystic septum, which was clearly depicted with contrast-enhanced US, was not depicted with CT (Fig 3).
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Figure 2a: Complicated benign cystic renal mass (stable at 12-month follow-up) in a 66-year-old woman. (a) Oblique US image obtained in the contrast-specific mode before contrast agent administration shows a large cystic renal mass. Thin endocystic septa (arrows) are almost completely suppressed by the software. (b) Oblique contrast-enhanced US image obtained in the contrast-specific mode during the nephrographic phase with the same technical parameters used in a. The endocystic septa appear strongly hyperechoic due to the presence of microbubbles (arrows). Expanding endocystic nodules are not seen. This cyst was classified as a Bosniak II lesion. (c) Transverse contrast-enhanced CT image of the right kidney obtained during the nephrographic phase shows a large renal cyst (C) with perceived thin enhancing septa (arrows) (Bosniak category II lesion).
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Figure 2b: Complicated benign cystic renal mass (stable at 12-month follow-up) in a 66-year-old woman. (a) Oblique US image obtained in the contrast-specific mode before contrast agent administration shows a large cystic renal mass. Thin endocystic septa (arrows) are almost completely suppressed by the software. (b) Oblique contrast-enhanced US image obtained in the contrast-specific mode during the nephrographic phase with the same technical parameters used in a. The endocystic septa appear strongly hyperechoic due to the presence of microbubbles (arrows). Expanding endocystic nodules are not seen. This cyst was classified as a Bosniak II lesion. (c) Transverse contrast-enhanced CT image of the right kidney obtained during the nephrographic phase shows a large renal cyst (C) with perceived thin enhancing septa (arrows) (Bosniak category II lesion).
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Figure 2c: Complicated benign cystic renal mass (stable at 12-month follow-up) in a 66-year-old woman. (a) Oblique US image obtained in the contrast-specific mode before contrast agent administration shows a large cystic renal mass. Thin endocystic septa (arrows) are almost completely suppressed by the software. (b) Oblique contrast-enhanced US image obtained in the contrast-specific mode during the nephrographic phase with the same technical parameters used in a. The endocystic septa appear strongly hyperechoic due to the presence of microbubbles (arrows). Expanding endocystic nodules are not seen. This cyst was classified as a Bosniak II lesion. (c) Transverse contrast-enhanced CT image of the right kidney obtained during the nephrographic phase shows a large renal cyst (C) with perceived thin enhancing septa (arrows) (Bosniak category II lesion).
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Figure 3a: Complicated hemorragic cyst (stable at 24-month follow-up) in a 56-year-old man. (a) Sagittal baseline US image of the left kidney shows a well-defined 1.5-cm-diameter exophytic cystic mass (*) with several septa and slightly hypoechoic content. (b) Oblique contrast-enhanced US image obtained in the contrast-specific mode with contrast-tuned imaging shows subtle endocystic enhancing septa (arrow). No enhancement of the endocystic solid component is seen. This cyst was classified as a Bosniak II lesion. (c) Transverse unenhanced and (d) contrast-enhanced CT images of the left kidney obtained in the nephrographic phase show an exophytic complex hemorragic cyst. The lesion has a high-attenuation nonenhancing hemorrhagic component (large region of interest) and a small low-attenuation component (small region of interest) with pseudoenhancement in the basal (attenuation, 31.7 HU) and nephrographic (attenuation, 40.8 HU) phases (Bosniak category IIF lesion).
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Figure 3b: Complicated hemorragic cyst (stable at 24-month follow-up) in a 56-year-old man. (a) Sagittal baseline US image of the left kidney shows a well-defined 1.5-cm-diameter exophytic cystic mass (*) with several septa and slightly hypoechoic content. (b) Oblique contrast-enhanced US image obtained in the contrast-specific mode with contrast-tuned imaging shows subtle endocystic enhancing septa (arrow). No enhancement of the endocystic solid component is seen. This cyst was classified as a Bosniak II lesion. (c) Transverse unenhanced and (d) contrast-enhanced CT images of the left kidney obtained in the nephrographic phase show an exophytic complex hemorragic cyst. The lesion has a high-attenuation nonenhancing hemorrhagic component (large region of interest) and a small low-attenuation component (small region of interest) with pseudoenhancement in the basal (attenuation, 31.7 HU) and nephrographic (attenuation, 40.8 HU) phases (Bosniak category IIF lesion).
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Figure 3c: Complicated hemorragic cyst (stable at 24-month follow-up) in a 56-year-old man. (a) Sagittal baseline US image of the left kidney shows a well-defined 1.5-cm-diameter exophytic cystic mass (*) with several septa and slightly hypoechoic content. (b) Oblique contrast-enhanced US image obtained in the contrast-specific mode with contrast-tuned imaging shows subtle endocystic enhancing septa (arrow). No enhancement of the endocystic solid component is seen. This cyst was classified as a Bosniak II lesion. (c) Transverse unenhanced and (d) contrast-enhanced CT images of the left kidney obtained in the nephrographic phase show an exophytic complex hemorragic cyst. The lesion has a high-attenuation nonenhancing hemorrhagic component (large region of interest) and a small low-attenuation component (small region of interest) with pseudoenhancement in the basal (attenuation, 31.7 HU) and nephrographic (attenuation, 40.8 HU) phases (Bosniak category IIF lesion).
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Figure 3d: Complicated hemorragic cyst (stable at 24-month follow-up) in a 56-year-old man. (a) Sagittal baseline US image of the left kidney shows a well-defined 1.5-cm-diameter exophytic cystic mass (*) with several septa and slightly hypoechoic content. (b) Oblique contrast-enhanced US image obtained in the contrast-specific mode with contrast-tuned imaging shows subtle endocystic enhancing septa (arrow). No enhancement of the endocystic solid component is seen. This cyst was classified as a Bosniak II lesion. (c) Transverse unenhanced and (d) contrast-enhanced CT images of the left kidney obtained in the nephrographic phase show an exophytic complex hemorragic cyst. The lesion has a high-attenuation nonenhancing hemorrhagic component (large region of interest) and a small low-attenuation component (small region of interest) with pseudoenhancement in the basal (attenuation, 31.7 HU) and nephrographic (attenuation, 40.8 HU) phases (Bosniak category IIF lesion).
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Complete concordance between the three readers in the assessment of vascularity with contrast-enhanced US was found ( = 1.00, P < .001). Interobserver agreement in the evaluation of enhancement on CT images was high ( = 0.88; range, 0.88–1.00; P < .001). Concordance between contrast-enhanced US and CT in the evaluation of vascularization was also high ( = 0.77, P < .001) (Fig 4).
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Figure 4a: Cystic renal cell carcinoma in a 69-year-old man. (a) Coronal baseline US image of the right kidney shows a well-defined 5-cm-diameter exophytic complex cystic mass (arrow). A round hyperechoic structure (*) is present in the mass. (b) Coronal contrast-enhanced US image obtained with the contrast-specific mode during the early arterial phase. The cystic mass (arrow) appears almost completely anechoic due to the suppression of fundamental signals by the software. Initial enhancement of hepatic arterial vessels and renal cortical parenchyma is seen. (c) Coronal contrast-enhanced US image obtained with the contrast-specific mode during the nephrographic phase. Enhancement of a solid endocystic nodule (*) with irregular contours is demonstrated. This complex cystic renal mass was classified as a Bosniak IV lesion. (d) Transverse unenhanced CT image of the right kidney shows an exophytic high-attenuation hemorrhagic cyst (*) with a small low-attenuation endocystic component. (e) Transverse contrast-enhanced CT image of the right kidney obtained during the nephrographic phase shows enhancement of an intracystic nodule that became isoattenuated with hemorrhagic fluid (Bosniak category IV lesion). Microscopic examination of the resected specimen (not shown) revealed cystic clear cell carcinoma.
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Figure 4b: Cystic renal cell carcinoma in a 69-year-old man. (a) Coronal baseline US image of the right kidney shows a well-defined 5-cm-diameter exophytic complex cystic mass (arrow). A round hyperechoic structure (*) is present in the mass. (b) Coronal contrast-enhanced US image obtained with the contrast-specific mode during the early arterial phase. The cystic mass (arrow) appears almost completely anechoic due to the suppression of fundamental signals by the software. Initial enhancement of hepatic arterial vessels and renal cortical parenchyma is seen. (c) Coronal contrast-enhanced US image obtained with the contrast-specific mode during the nephrographic phase. Enhancement of a solid endocystic nodule (*) with irregular contours is demonstrated. This complex cystic renal mass was classified as a Bosniak IV lesion. (d) Transverse unenhanced CT image of the right kidney shows an exophytic high-attenuation hemorrhagic cyst (*) with a small low-attenuation endocystic component. (e) Transverse contrast-enhanced CT image of the right kidney obtained during the nephrographic phase shows enhancement of an intracystic nodule that became isoattenuated with hemorrhagic fluid (Bosniak category IV lesion). Microscopic examination of the resected specimen (not shown) revealed cystic clear cell carcinoma.
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Figure 4c: Cystic renal cell carcinoma in a 69-year-old man. (a) Coronal baseline US image of the right kidney shows a well-defined 5-cm-diameter exophytic complex cystic mass (arrow). A round hyperechoic structure (*) is present in the mass. (b) Coronal contrast-enhanced US image obtained with the contrast-specific mode during the early arterial phase. The cystic mass (arrow) appears almost completely anechoic due to the suppression of fundamental signals by the software. Initial enhancement of hepatic arterial vessels and renal cortical parenchyma is seen. (c) Coronal contrast-enhanced US image obtained with the contrast-specific mode during the nephrographic phase. Enhancement of a solid endocystic nodule (*) with irregular contours is demonstrated. This complex cystic renal mass was classified as a Bosniak IV lesion. (d) Transverse unenhanced CT image of the right kidney shows an exophytic high-attenuation hemorrhagic cyst (*) with a small low-attenuation endocystic component. (e) Transverse contrast-enhanced CT image of the right kidney obtained during the nephrographic phase shows enhancement of an intracystic nodule that became isoattenuated with hemorrhagic fluid (Bosniak category IV lesion). Microscopic examination of the resected specimen (not shown) revealed cystic clear cell carcinoma.
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Figure 4d: Cystic renal cell carcinoma in a 69-year-old man. (a) Coronal baseline US image of the right kidney shows a well-defined 5-cm-diameter exophytic complex cystic mass (arrow). A round hyperechoic structure (*) is present in the mass. (b) Coronal contrast-enhanced US image obtained with the contrast-specific mode during the early arterial phase. The cystic mass (arrow) appears almost completely anechoic due to the suppression of fundamental signals by the software. Initial enhancement of hepatic arterial vessels and renal cortical parenchyma is seen. (c) Coronal contrast-enhanced US image obtained with the contrast-specific mode during the nephrographic phase. Enhancement of a solid endocystic nodule (*) with irregular contours is demonstrated. This complex cystic renal mass was classified as a Bosniak IV lesion. (d) Transverse unenhanced CT image of the right kidney shows an exophytic high-attenuation hemorrhagic cyst (*) with a small low-attenuation endocystic component. (e) Transverse contrast-enhanced CT image of the right kidney obtained during the nephrographic phase shows enhancement of an intracystic nodule that became isoattenuated with hemorrhagic fluid (Bosniak category IV lesion). Microscopic examination of the resected specimen (not shown) revealed cystic clear cell carcinoma.
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Figure 4e: Cystic renal cell carcinoma in a 69-year-old man. (a) Coronal baseline US image of the right kidney shows a well-defined 5-cm-diameter exophytic complex cystic mass (arrow). A round hyperechoic structure (*) is present in the mass. (b) Coronal contrast-enhanced US image obtained with the contrast-specific mode during the early arterial phase. The cystic mass (arrow) appears almost completely anechoic due to the suppression of fundamental signals by the software. Initial enhancement of hepatic arterial vessels and renal cortical parenchyma is seen. (c) Coronal contrast-enhanced US image obtained with the contrast-specific mode during the nephrographic phase. Enhancement of a solid endocystic nodule (*) with irregular contours is demonstrated. This complex cystic renal mass was classified as a Bosniak IV lesion. (d) Transverse unenhanced CT image of the right kidney shows an exophytic high-attenuation hemorrhagic cyst (*) with a small low-attenuation endocystic component. (e) Transverse contrast-enhanced CT image of the right kidney obtained during the nephrographic phase shows enhancement of an intracystic nodule that became isoattenuated with hemorrhagic fluid (Bosniak category IV lesion). Microscopic examination of the resected specimen (not shown) revealed cystic clear cell carcinoma.
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Cystic renal masses in patients with multiple lesions were considered independent lesions. The generalized estimating equation, which was performed to assess the statistical significance of this assumption, yielded a P value greater than .1.
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DISCUSSION
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The differentiation of complex cystic renal masses that require surgery from those that do not represents a common clinical problem for radiologists. Since cystic renal cell carcinomas and benign complicated cysts can be indistinguishable at gross inspection and assigning a definitive diagnosis can require a histologic examination, an overlap in imaging findings might also be expected (1). This overlap provides the rationale for prolonged follow-up of low-risk malignant lesions and for removal of indeterminate cystic masses.
The role of US is usually limited to the evaluation of minimally complicated cysts to rule out a cystic tumor, while all other complex cystic masses should be considered suspicious and require evaluation with contrast-enhanced CT or MR imaging (10,11). According to Israel and Bosniak (8,9), one should not rely on US in the differentiation of surgical from nonsurgical complex cystic renal masses in most cases because US cannot be used to accurately evaluate the presence of contrast enhancement, which, despite its lack of absolute specificity, represents a crucial criterion in the choice of management options (surgical treatment vs follow-up) for a complex cystic renal mass with the Bosniak classification system (1,3,5,8,9,12).
The development of second-generation contrast agents that contain microbubbles of gas different than air (eg, sulfur hexaflouride), such as the contrast agent used in this study, has opened up new ways to perform US, as this modality is extremely sensitive in the detection of even a few small bubbles of contrast material traveling in a septum or cystic wall during a real-time examination (13,16,20–23).
Contrast-enhanced US may replace CT in complex renal cyst evaluation and follow-up, and some authors have proposed a diagnostic algorithm that involves use of the Bosniak classification system (13,23). Ko et al (24) compared the accuracy of contrast-enhanced US with that of CT in the diagnosis of 31 cystic renal masses. They found that the diagnostic accuracy for diagnosis of malignant lesions was 82% for both examinations. The accuracy for diagnosis of benign lesions was 75% with contrast-enhanced US and 100% with CT. In our series, complete concordance in Bosniak grading was observed in the differentiation of surgical and nonsurgical complex cysts.
In six (14%) of the 44 lesions, conventional US depicted more intracystic septa than did CT, and this led us to reclassify category I or II lesions as category IIF lesions. This was in agreement with data in the literature, which suggest that finer intracystic detail is seen and cyst contents typically appear more complex at conventional US than at CT.
Enhancement was seen in 14 (32%) of 44 complex cysts on contrast-enhanced US images, with high concordance with contrast-enhanced CT images. In four (9%) lesions, a minimal degree of vascularization that was considered absent in two cases and uncertain in the remaining two cases at CT imaging was demonstrated with contrast-enhanced US. This finding may indicate that US is more sensitive to contrast enhancement than is CT. Our findings agree with the results of Ko et al (24) who reported that contrast-enhanced US performed better than CT in the depiction of tumor vascularity in the septa of cystic renal masses. The presence of tiny capillaries that feed hairline-thin septa and walls and are well detected with contrast-enhanced US explains the minimal degree of perceived enhancement in some benign cysts on helical CT images (8,9,12,13). Increased detection of vascularity with contrast-enhanced US is not surprising because study results have shown that even a small amount of microbubbles can be detected with harmonic US. With CT or MR imaging, a higher concentration of contrast material needs to be used to yield detectable enhancement (20,25).
The incidence of hypersensitivity or adverse events appears to be much lower with the contrast agent used in our study than with uroangiographic contrast agents (26). Caution should be exercised in patients with severe chronic obstructive pulmonary disease, congestive heart failure (class IV according to the New York Heart Association classification), and recent cardiac infarction.
Our study did have some limitations. The number of lesions, especially category III and IV lesions, was small; additional studies with an increased number of patients may prove valuable. Another limitation was the short follow-up period. The slow growth rate for incidentally detected small renal cell carcinomas is well known; consequently, the follow-up period for complex cystic renal masses should be prolonged, even though the duration of follow-up is not definitely established in the literature. The lack of comparison of morphologic criteria with US and CT criteria and the enrollment of patients based on US findings could be further study limitations. Finally, pathologic comparison was unavailable in most cases (ie, almost all category IIF lesions).
On the basis of our initial experience, we believe that the use of contrast-enhanced second-harmonic US, as compared with triple-phase helical CT, is appropriate in the Bosniak classification of renal cysts. More studies are needed to confirm this finding. In our opinion, contrast-enhanced US may be helpful in patients who require follow-up to reduce the radiation dose.
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ADVANCES IN KNOWLEDGE
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- Contrast-enhanced US appears to be appropriate for use with the Bosniak renal cyst classification system.
- Concordance between contrast-enhanced US and triple-phase helical CT was high ( = 0.79; range, 0.73–0.86).
- Complete concordance in Bosniak grading was observed in the differentiation of surgical and nonsurgical complex cysts ( = 1.00, P < .001).
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FOOTNOTES
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Authors stated no financial relationship to disclose.
Author contributions: Guarantors of integrity of entire study, G.A., S.M., E.S.; study concepts/study design or data acquisition or data analysis/interpretation, all authors; manuscript drafting or manuscript revision for important intellectual content, all authors; manuscript final version approval, all authors; literature research, C.M., D.M., R.C.; clinical studies, G.A., S.M., G.Z., E.S.; statistical analysis, N.S.; and manuscript editing, G.Z., C.M., D.M., R.C.
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