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Cystic renal masses: A reevaluation of the usefulness of the Bosniak classification system
Cystic Renal Masses:
A Reevaluation of the Usefulness of the Bosniak Classification System Todd E. Wilson, MD 1 , Eric A. Doelle, MD 1, Richard H. Cohan, MD 1, Kirk Wojno, MD 2, Melvyn Korobkin, MD 1
Rationale and Objectives. We evaluated the utility of the Bosniak system for classifying cystic renal masses on computed tomography (CT) scans. Methods. The CT scans of 20 patients with 24 cystic renal masses that were subsequently surgically removed or biopsied were reviewed retrospectively. Masses were categorized using the Bosniak system and were correlated with the pathology results. Results. The final pathology results of the cystic renal masses were as follows: Seven of seven category I lesions were benign, one of five category II lesions was benign, zero of four category III lesions were benign, and zero of six category IV lesions were benign. Neither of two unclassifiable cystic lesions were benign. The average enhancement of lesions in categories II, III, and IV was 6.3, 2.3, and 27.6 Hounsfield units (H), respectively. The two uncategorizable lesions had a mean enhancement of 26.8 H. Conclusion. The results of our study serve to underscore some limitations of the Bosniak classification system because most of our category II and all of our category IIl lesions were malignant, suggesting that minireally complex cystic renal masses may contain malignant cells. Contrast enhancement of less than 10 H was demonstrated in lesions in categories II and III. Key Words. Bosniak classification system; renal masses; complex cysts; computed tomography scanning. omputed tomography (CT) scanning is frequently used to direct the clinical management of renal masses because most of these masses have a relatively characteristic CT appearance. The majority of renal masses are simple cysts, all of which are benign and require no treatment unless they are symptomatic [1]. Solid renal masses with CT-detected fat almost always are benign angiomyolipomas and require no treatment if they are small [2]. Other solid renal masses without fatty content should be surgically removed because the majority represent renal adenocarcinomas [3]. Complex cystic renal masses, however, are a diagnostic challenge. Although many are benign, some represent cystic renal adenocarcinomas or renal cancers arising
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From the Departments of 1Radiology and 2pathology, University of Michigan, Ann Arbor, MI. Address reprint requests to R. H. Cohan, MD, Department of Radiology, University of Michigan, BID502, Box 0030, 1500 East Medical Center Dr., Ann Arbor, MI 48109-0030. Received December 4, 1995, and accepted for publication after revision March 22, 1996.
Acad Radio11996;3:564-570 © 1996, Association of University Radiologists
Vol. 3, No. 7, July 1996
in cysts. Appropriate imaging, and clinical management of these cases can be difficult. To assist in the m a n a g e m e n t of patients with cystic renal masses, Bosniak [4] p r o p o s e d a CT classification system in which cystic renal masses were assigned to one of four different categories on the basis of their imaging characteristics. The greater the complexity of the findings, the higher the category n u m b e r and the more likely the lesion is malignant. In 1986, Bosniak stated that all category I and category II lesions can be considered benign, whereas 50% of category III and all category IV lesions will be found to be malignant. Thus, Bosniak p r o p o s e d that all category I and II lesions do not need additional imaging or surgical intervention but that all category III and category IV lesions should be surgically removed. More recently, Bosniak revised this system to include a category IIF. Category IIF lesions are those with some areas of complexity that do require imaging follow-up but that are still most likely to be benign [5, 6]. To our knowledge, only Aronson et al. [7] have attempted to assess the accuracy of the Bosniak classification system. Their results supported Bosniak's predictions with 16 surgically confirmed cystic renal masses. All four of the category II lesions were benign, but four of seven category III lesions and all five category IV lesions were malignant. We recently encountered several category II cystic renal masses that subsequently were proved to be renal adenocarcinomas at surgery. Because this experience was contrary to Bosniak's predictions, we decided to evaluate our o w n experience with the Bosniak classification system. We also assessed the value of the presence or absence of contrast agent enhancement of a cystic renal mass in predicting the likelihood that a lesion will be malignant or benign. We also correlated the CT appearance of a cystic renal mass with its pathologic appearance, grade, and the stage of the cancer at the time of diagnosis.
MATERIALS AND METHODS
A retrospective search of our computerized pathology and radiology databases b e t w e e n 1986 and 1994 provided 20 consecutive patients with 24 pathologically confirmed cystic renal masses. Twenty-two of these masses also were seen as cystic renal masses on diagnostic CT examinations and could be classified b y the Bosniak system. The remaining two patients had pathologically proved cystic lesions that had CT characteris-
BOSNIAK CLASSIFICATION SYSTEM AND RENAL MASSES
tics not included in the Bosniak classification system. Overall, these 20 patients included 14 m e n and six w o m e n aged 17-78 years (M = 60 years). CT scanning was performed on a General Electric CT/T 9800, CT/T 9800 High-Speed Advantage, or CT/T 9800 HiLight scanner (General Electric Medical Systems, Milwaukee, WI). Nine patients had dedicated renal CT examinations with contiguous 5-ram collimated scans obtained both before and after dynamic intravenous (IV) contrast agent administration (two of which were performed spirally, 1:1 pitch, 5 mm/sec table feed). One patient had 10ram-thick collimated images before and 5-ram collimated images after 1V contrast medium was injected. Two patients had incremental contiguous axial 10-ram CT scans done before and after IV contrast medium injection, and the remaining eight patients had incremental 10-mm collimated scans only after IV infusion of the contrast agent. Contrast material was administered as a dynamic bolus injection of 150 rrfl iohexol-300 (Omnipaque; Nycomed, Collegeville, PA) or sodium meglumine diatrizoate-60 (Hypaque; Nycomed). One patient received a 75ml bolus of iohexol-300 because of an elevated serum creatinine level. Bolus infusion of contrast material was delivered by either a Mark IV CT power injector (Medrad, Pittsburgh, PA) or an Angiomat digital CT power injector (Liebel-Flarsheim, Cincinnati, OH). The CT scans were reviewed by three radiologists. The cystic masses were categorized by consensus according to the Bosniak system [1, 4-7]. All cystic masses having all features of a simple cyst (i.e., smooth contour, imperceptible wall, water attenuation, nonenhancement, and absence of nodularity or septations) were classified as category I lesions. Hyperdense cysts or water attenuation masses having one or two thin septations, peripheral calcifications, or both were classified as category II cysts. Water attenuation masses having multiple loculations, nonenhancing nodules, thick uniform walls, or thick irregular calcifications were considered to be category III cysts. Category IV lesions contained large nodules or any other enhancing solid component with a contrast agent-enhanced attenuation increase of at least 10 Hounsfield units (H). There were two masses in two patients that were subsequently proved to be cystic renal masses that could not be classified according to the Bosniak system because they had CT characteristics that min:icked solid renal adenocarcinomas after contrast agent enhancement (Table 1). Region-of-interest (ROD measurements were obtained in 11 patients with 11 cystic renal masses (nine had contiguous 5-mm collimated images and two had contigu565
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ET AL.
TABLE 1: Bosniak Classification System Bosniak Category
No.
I II
7 5
III
4
IV
6
No category
2
Features Leading Categorization
MalignantTotal for Each Feature
Simple cyst Thin septation (<1 mm) Thin, fine calcifications Hyperdense Thick, irregular calcifications Multilocular Nodularity (nonenhancing) Thick wall uniform Indeterminant hyperdense Nodularity Thick wall Solid component Enhancement
0/7 2/3 1/1 2/3 0/0 1/1 0/O 2/2 1/1 2/2 4/4 4/4 2/2
ous 10-mm collimated images). Three ROIs of each mass were measured on both enhanced and unenhanced scans, and the region with the greatest difference in Hounsfield units was selected. The area of the ROI was placed to include the entire mass, the cystic component, and a prominent solid component depending on which features were present. All measurements of attenuation change were done by standard ROI techniques, with the ROI being the largest possible for the area being sampled [8, 9] (Table 2). Histologic sections of 22 surgical specimens and the cytology preparations of one percutaneous and one
intraoperative aspiration were reviewed by a pathologist w h o had no knowledge of the CT findings. The cystic renal masses were categorized as renal cysts, renal cell carcinomas, or other malignancy. Renal cell carcinomas were histologically subtyped as clear cell, mixed clear cell and granular, granular, sarcomatoid, papillary, or oncocytic [101. The overall growth pattern was classified as cystic if more than 75% of the tumor was c o m p o s e d of macroscopic cysts (>2 mm). Tumors were considered to be mixed cystic and solid w h e n the cystic c o m p o n e n t made up 25-75% of the area and solid w h e n cystic central areas were felt to be caused by tumor necrosis. The degree of cellular atypia of the renal adenocarcinomas was determined according to the Fuhrman classification system [11]. The pathologic stage of the renal carcinomas was determined according to the Robson system [121.
RESULTS B o s n i a k Classification
Twenty-two of the 24 cystic lesions could be classified according to the Bosniak system (Table 1). There were seven category I, five category- II (Figs. 1 and 2), four category III (Fig. 3), and six category IV (Fig. 4) cysts (Table 1). On histopathologic analysis, all category I masses were confirmed to be simple cysts. All but one of the other 17 cystic masses were found to be malignant. This included four of the five cysts considered to
TABLE 2: Region-of-Interest Measurements Patient No.
Precontrast (H) Postcontrast (H)
Category II 1 2 3 M Category III 1 2 3 M Category IV 1 2 3 M Indeterminants 1 2 M H = Hounsfield units.
566
Change
14 32 21 22.3
20 41 25 28.7
6 9 4 6.3
20 8 12 13.3
26 8 13 15.6
6 -1 2.3
16 15 14 15
37 66 25 42.6
21 51 11 27.6
16 38.8 22.4
50 58.4 54.2
34 19.6 26.8
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BOSNIAK
CLASSIFICATION
SYSTEM
AND RENAL MASSES
FIGURE 1. Category II lesion. This contrast-enhanced computed tomography scan from a 62-year-old woman shows a cystic mass with thin septations in the right upper pole. The mass was pathologically proved to be a cystic renal adenocarcinoma.
FIGURE 3. Category III lesion. This contrast-enhanced computed tomography scan from a a 43-year-old man shows a multilocular cystic mass in the upper pole of the left kidney. The mass was pathologically proved to be a cystic renal adenocarcinoma.
FIGURE 2. Category II lesion. This contrast-enhanced computed tomography scan from a 64-year-old man shows a cystic mass with a thin septation in the posterior right kidney. The mass was pathologically proved to be a cystic renal adenocarcinoma.
be category II masses (Figs. 1 and 2) and all of the category III and IV masses. Two cystic masses could not be classified using Bosniak's system. One was a homogeneous near-water attenuation mass on unenhanced scans (16 H) that enhanced to soft-tissue attenuation values (50 H) after contrast agent injection (Fig. 5). We were concerned because this was a small lesion that could have had an element of volume averaging. The other mass measured 38.8 H prior to contrast agent administration and enhanced to 58.4 H after IV contrast material was injected, mimicking a solid mass on the CT scan (Fig. 6). On review of the pathologic specimens, the 15 categorized cystic cancers included eight cystic renal cell carci-
FIGURE 4. Category IV lesion. This contrast-enhanced computed tomography scan from a 46-year-old woman shows a thick walled cystic renal mass. The mass proved to be a solid necrotic renal adenocarcinoma on pathologic specimen.
nomas, four solid necrotic renal cell carcinomas, two solid tumors, and one lymphoma. The case of lymphoma was proved by percutaneous biopsy. On CT scans, this lesion had what appeared to be an enhancing periphery and a central area of lower attenuation. This 567
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FIGURE 5. Unclassifiable lesion. This contrast-enhanced computed tomography scan from an obese 54-year-old woman shows a small, low-attenuation lesion in the posterior area of the mid-right kidney. This measured 16 Hounsfield units (H) on precontrast imaging and 50 H on postcontrast imaging. This was resected and proved to be a cystic renal adenocarcinoma having prominent papillary histology.
was assumed to be an area of necrosis. One of the uncategorized cystic cancers was an enhancing cystic renal neoplasm, of which a considerable portion exhibited papillary histology. The other undefinable cystic renal cell carcinoma was found on pathologic examination to be a multisegmented cystic cavity filled with blood. This was the patient whose CT scan mimicked a solid renal cell carcinoma with 20-H enhancement (Table 2). Of the remaining 14 renal adenocarcinomas, 12 were clear-cell tumors and two had papillary architecture. Measured
Enhancement
ROI measurements were obtained during the initial evaluation of six classifiable and the two nonclassifiable cystic renal masses. The RO1 data for these eight masses were reviewed. In addition, ROI measurements were obtained retrospectively in another three patients (Table 2). Of these 11 masses, nine were scanned at 5m m intervals and two at contiguous 10-mm intervals. The measured lesions included three category II, three category III, three category IV masses, and two unclas-
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FIGURE 6. Unclassifiable lesion. This contrast-enhanced computed tomography scan of a 57-year-old man shows a solid-appearing mass in the lower pole of the left kidney.This enhanced postcontrast and was prospectively diagnosed as a solid renal cancer. On pathology, this proved to be a hemorrhagic cystic renal adenocarcinoma.
sifted cystic neoplasms. The category II lesions had a mean attenuation increase of 6.3 H (range = 4-9 H), the category III lesions had a mean attenuation increase of 2.3 H (range = 0-6 H), and the category IV lesions had a mean attenuation increase of 27.6 H (range = 11-51 H). Both of the unclassified lesions enhanced 20+ H. Pathologic
Grading
Fuhrman nuclear grading [11] was performed on 13 cystic renal carcinomas, including the two unclassified masses (Table 3). Of the classified masses, one category II lesion and one category IV lesion had Fuhrman grade 1 nuclear atypia. Three Bosniak category II, two category III, and two category IV lesions had Fuhrman grade 2 nuclear atypia. The two lesions not classified by the Bosniak system also were assigned a Fuhrman grade of 2. The two Fuhrman grade 3 lesions were Bosniak category IV neoplasms. One necrotic category III lesion could not be classified because of extensive cellular lysis, one category IV lesion had only
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BOSNIAK CLASSIFICATION SYSTEM AND RENAL MASSES
TABLE 3: Robson Stages and Fuhrman Grades Category
Fuhrman Grade
II
1/4 grade I 3/4 grade II 1/4 necrotic 1/4 l y m p h o m a 2/4 grade II 1/6 grade I 1/6 grade II 1/6 grade III 1/6 grade II 1/6 grade III 1/6 aspiration and therefore no grade or stage 2/2 grade II
III
IV
Unclassified
Robson Stage I I I NA IIIc, I I I I II II
I
cytopathology results available, and o n e category III lesion was a l y m p h o m a . Pathologic S t a g i n g
Pathologic staging was available for 14 cystic renal adenocarcinomas, including the two unclassified masses (Table 3). Eleven of the 14 cystic masses were confined to the kidney at surgery (Robson stage I [12]). These included all four malignant Bosniak category II, two category III, three category IV, and the two unclassified masses. T w o category IV cystic malignancies had invaded the capsule at the time of surgery but were confined to the perinephric space (Robson stage II). Only one patient had advanced disease not amenable to simple surgical extirpation. This patient had a 9-cm Bosniak category III mass that was a Robson stage IIIc tumor with renal vein invasion and perirenal lymphadenopathy detected at surgery. DISCUSSION
The results of our study are discordant with Bosniak's [4] predictions as well as the supportive findings of Aronson et al. [7], primarily because four of the five category II lesions as classified b y the Bosniak system were malignant. It might be argued that our different results reflect the inaccurate use of Bosniak's system. Certainly, difficulty in classifying category II and category III lesions is expected and has b e e n reported [5, 6, 13, 14]. In one of our'patients, there was disagreement about whether a lesion should have b e e n considered a category II or III lesion. Furthermore, one may argue that the nondedicated CT technique could contribute to difficulty in classifying category II and category III
lesions because small septations or small mural nodules may not be apparent without narrow collimation or precontrast scanning. However, nine of our 20 patients had dedicated renal CT examinations that included narrow collimation scans obtained both before and after the IV injection of contrast material. This included two patients with category II lesions, one of which was malignant, as well as three category III masses. Also, both of the malignant uncategorizable lesions were scanned using the dedicated renal protocol. Another variable that may account for the high rate of malignancy found in our patients is case selection bias. Only patients having pathologically proved cystic renal masses were included. Presumably, surgery or aspiration biopsy was performed on these patients because of ongoing symptoms and a strong clinical suspicion of malignancy, despite the relatively benign CT appearance of some of these cystic renal masses. Chart reviews of the patients having the four malignant category II masses revealed that surgery was precipitated by suspicious clinical or imaging changes in all cases: paraneoplastic syndrome (one of four), interval change on imaging studies (two of four), hematuria (four of four), or flank pain (two of four). The benign category II lesion was resected in a patient w h o had a concurrent ,contralateral renal cell carcinoma. It is likely that some truly benign nonoperative category II lesions were detected over the course of this study and were not surgically removed. These lesions would not have been included in this study. Therefore, we suspect that the actual malignancy rate of category II lesions is considerably lower than the 80% rate demonstrated in this study. Nonetheless, our results suggest that at least some category II lesions may be malignant. Of the two cystic masses not assigned a Bosniak category, one was of water attenuation on unenhanced scans but of heterogeneous soft-tissue attenuation on enhanced scans, whereas the other appeared to be solid and enhancing. The former is a disturbing case and confirms that the diagnosis of a simple renal cyst cannot be made with complete certainty w h e n a small homogeneous water attenuation mass is identified only on unenhanced scans. Confusion of a cystic neoplasm with a solid mass, as was the case in our other nonclassifiable lesion, is not likely to be clinically relevant because surgical removal is required in both instances, but it is interesting. To our knowledge, this is the first reported example of an enhancing cystic renal adenocarcinoma that had these CT characteristics and the second reported
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example of a cystic renal a d e n o c a r c i n o m a mimicking a solid tumor [14]. It has b e e n shown that some small cystic renal carcinomas can contain enough solid cellular material to mimic more typical solid renal cell carcinomas [14]. Presumably, the enhancement characteristics of at least one, if not both, nonclassifiable lesions can be attributed to the septations or papillary projections of tumor within the wall of these complex renal masses that were detected pathologically. It generally has been accepted that renal mass enhancement in excess of 10-15 H after IV contrast media injection indicates malignant tumor vascularity. Such enhancing masses are usually surgically removed (unless they contain fat) because they often are renal cancers [9]. Conversely, a lack of contrast enhancement has been accepted as an indicator of the absence of vascularity and of lesion benignity. It is therefore of concern that seven of the nine classifiable malignant cystic renal masses in which attenuation coefficients were measured in this series had demonstrable contrast enhancement of no more than 10 H. Even on detailed retrospective review, no suspiciously enhancing areas could be identified in these cases. We suspect that this was primarily due to the small sizes and relative hypovascularity of the solid components of the lower category lesions. These characteristics parallel those in recent reports of cystic renal carcinomas [13, 14]. This series serves to underscore the difficulties that can be encountered w h e n obtaining enhancement measurements in cystic renal masses and certainly indicates that lack of enhancement by 10-15 H does not eliminate the possibility of malignancy. T u m o r grading with the Fuhrman system [11] is thought to have prognostic significance. The Fuhrman classification pertains to cytologic characteristics of tumor aggressiveness (i.e., nucleoli and mitotic figures) and thus its likelihood for metastasis.. Although the n u m b e r of cystic renal cell carcinomas in our series was small, our results suggest that higher category lesions m a y have higher Fuhrman pathologic grades, whereas lower category lesions have a variety of grades. The results of our study also suggest that less complex cystic renal malignancies tend to be low Robson stage [12] w h e n detected. In fact, all Bosniak category II tumors were Fuhrman grade I or II and Robson stage I renal cell carcinomas. These tumors usually are curable b y radical or partial nephrectomy.
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In summary, our experience provides evidence that although the Bosniak CT classification system is valuable, it does have limitations. A larger percentage of category II and category III lesions may in fact be malignant than was predicted by Bosniak [4] and found by Aronson et al. [7]. We also show that m a n y cystic renal cancers do not have the contrast enhancement patterns often associated with solid renal cell carcinomas and therefore lack of demonstrable enhancement cannot be relied on to differentiate benign complex cysts from cystic renal malignancies in at least some instances. Because most of these cystic cancers are of low Fuhrman nuclear grade and low Robson stage, they should have a good prognosis if detected early and surgically extirpated. Perhaps all category II cystic renal masses should be followed with imaging studies (IIF) to confirm long-term stability unless clinical circumstances dictate immediate pathologic confirmation. Certainly, additional experience is needed to help direct the clinical management of category II cystic renal masses.
REFERENCES 1. Hartman DS. Cysts and cystic neoplasms. Urol Radio11993;12:7-10. 2. Bosniak MA, Megibow A J, Hulnick DH, Horii S, Raghavendra BN. CT diagnosis of renal angiomyolipoma: the importance of detecting small amounts of fat. AJR 1988;157:497-501. 3. Dunnick NR. Textbook of uroradiology. Baltimore: Williams & Wilkins, 1991:113-134. 4. Bosniak MA. The current radiological approach to renal cysts. Radiology
1986;158:1-10. 5. Hartman D, Davis CJ, Sanders RC, Johns TT, Smirniotopoulos J, Goldman SM. The multiloculated renal mass: considerations and differential features. RadioGraphics 1987;1:29-52. 6. Bosniak MA. Difficulties in classifying cystic lesions of the kidney. Urol Radiol 1991; 13:91-93. 7. Aronson S, Frazier HA, Balwah JD, Hartman DS, Christenson PPJ. Cystic renal masses: usefulness of the Bosniak classification. Urol Radiol
1988;13:83-93. 8. Amendola MA. Small renal cell carcinomas: resolving a diagnostic dilemma. Radiology 1988; 166:637-741. 9. Silverman SG, Lee BY, Seltzer SE, Bloom DA, Corless CL, Adams DR Small (<3 cm) renal masses: correlation of spiral CT features and pathologic findings. A JR 1994;163:597-605. 10. Fromowitz FB, Bard RH. Clinical implications of pathologic subtypes in renal cell carcinoma. Sem Uro11990;7:31-50. 11. Fuhrman SA, Lasky LC, Limas CR Prognostic significance of morphologic parameters in renal cell carcinoma. Am J Surg Path 1982;6:655-663. 12. Robson C J, Churchill RM, Anderson W. The results of radical nephrectomy for renal cell carcinoma. J Uro11969;101:297-301. 13. Hartman DS, Ellsworth W, Laskin WB, Brody JM, Corse W, Baluch JD. Cystic renal cell carcinoma: CT findings mimicking a benign hyperdense cyst. A JR 1992;159:1235-1236. 14. Yamashita Y, Watanabe O, Miyazaki T, Yamamoto M, Harada M, Takahashi M. Cystic renal cell carcinoma: imaging findings with pathologic correlation. Acta Radio11994; 35:19-24.
A Reevaluation of the Usefulness of the Bosniak Classification System Todd E. Wilson, MD 1 , Eric A. Doelle, MD 1, Richard H. Cohan, MD 1, Kirk Wojno, MD 2, Melvyn Korobkin, MD 1
Rationale and Objectives. We evaluated the utility of the Bosniak system for classifying cystic renal masses on computed tomography (CT) scans. Methods. The CT scans of 20 patients with 24 cystic renal masses that were subsequently surgically removed or biopsied were reviewed retrospectively. Masses were categorized using the Bosniak system and were correlated with the pathology results. Results. The final pathology results of the cystic renal masses were as follows: Seven of seven category I lesions were benign, one of five category II lesions was benign, zero of four category III lesions were benign, and zero of six category IV lesions were benign. Neither of two unclassifiable cystic lesions were benign. The average enhancement of lesions in categories II, III, and IV was 6.3, 2.3, and 27.6 Hounsfield units (H), respectively. The two uncategorizable lesions had a mean enhancement of 26.8 H. Conclusion. The results of our study serve to underscore some limitations of the Bosniak classification system because most of our category II and all of our category IIl lesions were malignant, suggesting that minireally complex cystic renal masses may contain malignant cells. Contrast enhancement of less than 10 H was demonstrated in lesions in categories II and III. Key Words. Bosniak classification system; renal masses; complex cysts; computed tomography scanning. omputed tomography (CT) scanning is frequently used to direct the clinical management of renal masses because most of these masses have a relatively characteristic CT appearance. The majority of renal masses are simple cysts, all of which are benign and require no treatment unless they are symptomatic [1]. Solid renal masses with CT-detected fat almost always are benign angiomyolipomas and require no treatment if they are small [2]. Other solid renal masses without fatty content should be surgically removed because the majority represent renal adenocarcinomas [3]. Complex cystic renal masses, however, are a diagnostic challenge. Although many are benign, some represent cystic renal adenocarcinomas or renal cancers arising
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564
From the Departments of 1Radiology and 2pathology, University of Michigan, Ann Arbor, MI. Address reprint requests to R. H. Cohan, MD, Department of Radiology, University of Michigan, BID502, Box 0030, 1500 East Medical Center Dr., Ann Arbor, MI 48109-0030. Received December 4, 1995, and accepted for publication after revision March 22, 1996.
Acad Radio11996;3:564-570 © 1996, Association of University Radiologists
Vol. 3, No. 7, July 1996
in cysts. Appropriate imaging, and clinical management of these cases can be difficult. To assist in the m a n a g e m e n t of patients with cystic renal masses, Bosniak [4] p r o p o s e d a CT classification system in which cystic renal masses were assigned to one of four different categories on the basis of their imaging characteristics. The greater the complexity of the findings, the higher the category n u m b e r and the more likely the lesion is malignant. In 1986, Bosniak stated that all category I and category II lesions can be considered benign, whereas 50% of category III and all category IV lesions will be found to be malignant. Thus, Bosniak p r o p o s e d that all category I and II lesions do not need additional imaging or surgical intervention but that all category III and category IV lesions should be surgically removed. More recently, Bosniak revised this system to include a category IIF. Category IIF lesions are those with some areas of complexity that do require imaging follow-up but that are still most likely to be benign [5, 6]. To our knowledge, only Aronson et al. [7] have attempted to assess the accuracy of the Bosniak classification system. Their results supported Bosniak's predictions with 16 surgically confirmed cystic renal masses. All four of the category II lesions were benign, but four of seven category III lesions and all five category IV lesions were malignant. We recently encountered several category II cystic renal masses that subsequently were proved to be renal adenocarcinomas at surgery. Because this experience was contrary to Bosniak's predictions, we decided to evaluate our o w n experience with the Bosniak classification system. We also assessed the value of the presence or absence of contrast agent enhancement of a cystic renal mass in predicting the likelihood that a lesion will be malignant or benign. We also correlated the CT appearance of a cystic renal mass with its pathologic appearance, grade, and the stage of the cancer at the time of diagnosis.
MATERIALS AND METHODS
A retrospective search of our computerized pathology and radiology databases b e t w e e n 1986 and 1994 provided 20 consecutive patients with 24 pathologically confirmed cystic renal masses. Twenty-two of these masses also were seen as cystic renal masses on diagnostic CT examinations and could be classified b y the Bosniak system. The remaining two patients had pathologically proved cystic lesions that had CT characteris-
BOSNIAK CLASSIFICATION SYSTEM AND RENAL MASSES
tics not included in the Bosniak classification system. Overall, these 20 patients included 14 m e n and six w o m e n aged 17-78 years (M = 60 years). CT scanning was performed on a General Electric CT/T 9800, CT/T 9800 High-Speed Advantage, or CT/T 9800 HiLight scanner (General Electric Medical Systems, Milwaukee, WI). Nine patients had dedicated renal CT examinations with contiguous 5-ram collimated scans obtained both before and after dynamic intravenous (IV) contrast agent administration (two of which were performed spirally, 1:1 pitch, 5 mm/sec table feed). One patient had 10ram-thick collimated images before and 5-ram collimated images after 1V contrast medium was injected. Two patients had incremental contiguous axial 10-ram CT scans done before and after IV contrast medium injection, and the remaining eight patients had incremental 10-mm collimated scans only after IV infusion of the contrast agent. Contrast material was administered as a dynamic bolus injection of 150 rrfl iohexol-300 (Omnipaque; Nycomed, Collegeville, PA) or sodium meglumine diatrizoate-60 (Hypaque; Nycomed). One patient received a 75ml bolus of iohexol-300 because of an elevated serum creatinine level. Bolus infusion of contrast material was delivered by either a Mark IV CT power injector (Medrad, Pittsburgh, PA) or an Angiomat digital CT power injector (Liebel-Flarsheim, Cincinnati, OH). The CT scans were reviewed by three radiologists. The cystic masses were categorized by consensus according to the Bosniak system [1, 4-7]. All cystic masses having all features of a simple cyst (i.e., smooth contour, imperceptible wall, water attenuation, nonenhancement, and absence of nodularity or septations) were classified as category I lesions. Hyperdense cysts or water attenuation masses having one or two thin septations, peripheral calcifications, or both were classified as category II cysts. Water attenuation masses having multiple loculations, nonenhancing nodules, thick uniform walls, or thick irregular calcifications were considered to be category III cysts. Category IV lesions contained large nodules or any other enhancing solid component with a contrast agent-enhanced attenuation increase of at least 10 Hounsfield units (H). There were two masses in two patients that were subsequently proved to be cystic renal masses that could not be classified according to the Bosniak system because they had CT characteristics that min:icked solid renal adenocarcinomas after contrast agent enhancement (Table 1). Region-of-interest (ROD measurements were obtained in 11 patients with 11 cystic renal masses (nine had contiguous 5-mm collimated images and two had contigu565
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ET AL.
TABLE 1: Bosniak Classification System Bosniak Category
No.
I II
7 5
III
4
IV
6
No category
2
Features Leading Categorization
MalignantTotal for Each Feature
Simple cyst Thin septation (<1 mm) Thin, fine calcifications Hyperdense Thick, irregular calcifications Multilocular Nodularity (nonenhancing) Thick wall uniform Indeterminant hyperdense Nodularity Thick wall Solid component Enhancement
0/7 2/3 1/1 2/3 0/0 1/1 0/O 2/2 1/1 2/2 4/4 4/4 2/2
ous 10-mm collimated images). Three ROIs of each mass were measured on both enhanced and unenhanced scans, and the region with the greatest difference in Hounsfield units was selected. The area of the ROI was placed to include the entire mass, the cystic component, and a prominent solid component depending on which features were present. All measurements of attenuation change were done by standard ROI techniques, with the ROI being the largest possible for the area being sampled [8, 9] (Table 2). Histologic sections of 22 surgical specimens and the cytology preparations of one percutaneous and one
intraoperative aspiration were reviewed by a pathologist w h o had no knowledge of the CT findings. The cystic renal masses were categorized as renal cysts, renal cell carcinomas, or other malignancy. Renal cell carcinomas were histologically subtyped as clear cell, mixed clear cell and granular, granular, sarcomatoid, papillary, or oncocytic [101. The overall growth pattern was classified as cystic if more than 75% of the tumor was c o m p o s e d of macroscopic cysts (>2 mm). Tumors were considered to be mixed cystic and solid w h e n the cystic c o m p o n e n t made up 25-75% of the area and solid w h e n cystic central areas were felt to be caused by tumor necrosis. The degree of cellular atypia of the renal adenocarcinomas was determined according to the Fuhrman classification system [11]. The pathologic stage of the renal carcinomas was determined according to the Robson system [121.
RESULTS B o s n i a k Classification
Twenty-two of the 24 cystic lesions could be classified according to the Bosniak system (Table 1). There were seven category I, five category- II (Figs. 1 and 2), four category III (Fig. 3), and six category IV (Fig. 4) cysts (Table 1). On histopathologic analysis, all category I masses were confirmed to be simple cysts. All but one of the other 17 cystic masses were found to be malignant. This included four of the five cysts considered to
TABLE 2: Region-of-Interest Measurements Patient No.
Precontrast (H) Postcontrast (H)
Category II 1 2 3 M Category III 1 2 3 M Category IV 1 2 3 M Indeterminants 1 2 M H = Hounsfield units.
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Change
14 32 21 22.3
20 41 25 28.7
6 9 4 6.3
20 8 12 13.3
26 8 13 15.6
6 -1 2.3
16 15 14 15
37 66 25 42.6
21 51 11 27.6
16 38.8 22.4
50 58.4 54.2
34 19.6 26.8
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CLASSIFICATION
SYSTEM
AND RENAL MASSES
FIGURE 1. Category II lesion. This contrast-enhanced computed tomography scan from a 62-year-old woman shows a cystic mass with thin septations in the right upper pole. The mass was pathologically proved to be a cystic renal adenocarcinoma.
FIGURE 3. Category III lesion. This contrast-enhanced computed tomography scan from a a 43-year-old man shows a multilocular cystic mass in the upper pole of the left kidney. The mass was pathologically proved to be a cystic renal adenocarcinoma.
FIGURE 2. Category II lesion. This contrast-enhanced computed tomography scan from a 64-year-old man shows a cystic mass with a thin septation in the posterior right kidney. The mass was pathologically proved to be a cystic renal adenocarcinoma.
be category II masses (Figs. 1 and 2) and all of the category III and IV masses. Two cystic masses could not be classified using Bosniak's system. One was a homogeneous near-water attenuation mass on unenhanced scans (16 H) that enhanced to soft-tissue attenuation values (50 H) after contrast agent injection (Fig. 5). We were concerned because this was a small lesion that could have had an element of volume averaging. The other mass measured 38.8 H prior to contrast agent administration and enhanced to 58.4 H after IV contrast material was injected, mimicking a solid mass on the CT scan (Fig. 6). On review of the pathologic specimens, the 15 categorized cystic cancers included eight cystic renal cell carci-
FIGURE 4. Category IV lesion. This contrast-enhanced computed tomography scan from a 46-year-old woman shows a thick walled cystic renal mass. The mass proved to be a solid necrotic renal adenocarcinoma on pathologic specimen.
nomas, four solid necrotic renal cell carcinomas, two solid tumors, and one lymphoma. The case of lymphoma was proved by percutaneous biopsy. On CT scans, this lesion had what appeared to be an enhancing periphery and a central area of lower attenuation. This 567
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FIGURE 5. Unclassifiable lesion. This contrast-enhanced computed tomography scan from an obese 54-year-old woman shows a small, low-attenuation lesion in the posterior area of the mid-right kidney. This measured 16 Hounsfield units (H) on precontrast imaging and 50 H on postcontrast imaging. This was resected and proved to be a cystic renal adenocarcinoma having prominent papillary histology.
was assumed to be an area of necrosis. One of the uncategorized cystic cancers was an enhancing cystic renal neoplasm, of which a considerable portion exhibited papillary histology. The other undefinable cystic renal cell carcinoma was found on pathologic examination to be a multisegmented cystic cavity filled with blood. This was the patient whose CT scan mimicked a solid renal cell carcinoma with 20-H enhancement (Table 2). Of the remaining 14 renal adenocarcinomas, 12 were clear-cell tumors and two had papillary architecture. Measured
Enhancement
ROI measurements were obtained during the initial evaluation of six classifiable and the two nonclassifiable cystic renal masses. The RO1 data for these eight masses were reviewed. In addition, ROI measurements were obtained retrospectively in another three patients (Table 2). Of these 11 masses, nine were scanned at 5m m intervals and two at contiguous 10-mm intervals. The measured lesions included three category II, three category III, three category IV masses, and two unclas-
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FIGURE 6. Unclassifiable lesion. This contrast-enhanced computed tomography scan of a 57-year-old man shows a solid-appearing mass in the lower pole of the left kidney.This enhanced postcontrast and was prospectively diagnosed as a solid renal cancer. On pathology, this proved to be a hemorrhagic cystic renal adenocarcinoma.
sifted cystic neoplasms. The category II lesions had a mean attenuation increase of 6.3 H (range = 4-9 H), the category III lesions had a mean attenuation increase of 2.3 H (range = 0-6 H), and the category IV lesions had a mean attenuation increase of 27.6 H (range = 11-51 H). Both of the unclassified lesions enhanced 20+ H. Pathologic
Grading
Fuhrman nuclear grading [11] was performed on 13 cystic renal carcinomas, including the two unclassified masses (Table 3). Of the classified masses, one category II lesion and one category IV lesion had Fuhrman grade 1 nuclear atypia. Three Bosniak category II, two category III, and two category IV lesions had Fuhrman grade 2 nuclear atypia. The two lesions not classified by the Bosniak system also were assigned a Fuhrman grade of 2. The two Fuhrman grade 3 lesions were Bosniak category IV neoplasms. One necrotic category III lesion could not be classified because of extensive cellular lysis, one category IV lesion had only
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BOSNIAK CLASSIFICATION SYSTEM AND RENAL MASSES
TABLE 3: Robson Stages and Fuhrman Grades Category
Fuhrman Grade
II
1/4 grade I 3/4 grade II 1/4 necrotic 1/4 l y m p h o m a 2/4 grade II 1/6 grade I 1/6 grade II 1/6 grade III 1/6 grade II 1/6 grade III 1/6 aspiration and therefore no grade or stage 2/2 grade II
III
IV
Unclassified
Robson Stage I I I NA IIIc, I I I I II II
I
cytopathology results available, and o n e category III lesion was a l y m p h o m a . Pathologic S t a g i n g
Pathologic staging was available for 14 cystic renal adenocarcinomas, including the two unclassified masses (Table 3). Eleven of the 14 cystic masses were confined to the kidney at surgery (Robson stage I [12]). These included all four malignant Bosniak category II, two category III, three category IV, and the two unclassified masses. T w o category IV cystic malignancies had invaded the capsule at the time of surgery but were confined to the perinephric space (Robson stage II). Only one patient had advanced disease not amenable to simple surgical extirpation. This patient had a 9-cm Bosniak category III mass that was a Robson stage IIIc tumor with renal vein invasion and perirenal lymphadenopathy detected at surgery. DISCUSSION
The results of our study are discordant with Bosniak's [4] predictions as well as the supportive findings of Aronson et al. [7], primarily because four of the five category II lesions as classified b y the Bosniak system were malignant. It might be argued that our different results reflect the inaccurate use of Bosniak's system. Certainly, difficulty in classifying category II and category III lesions is expected and has b e e n reported [5, 6, 13, 14]. In one of our'patients, there was disagreement about whether a lesion should have b e e n considered a category II or III lesion. Furthermore, one may argue that the nondedicated CT technique could contribute to difficulty in classifying category II and category III
lesions because small septations or small mural nodules may not be apparent without narrow collimation or precontrast scanning. However, nine of our 20 patients had dedicated renal CT examinations that included narrow collimation scans obtained both before and after the IV injection of contrast material. This included two patients with category II lesions, one of which was malignant, as well as three category III masses. Also, both of the malignant uncategorizable lesions were scanned using the dedicated renal protocol. Another variable that may account for the high rate of malignancy found in our patients is case selection bias. Only patients having pathologically proved cystic renal masses were included. Presumably, surgery or aspiration biopsy was performed on these patients because of ongoing symptoms and a strong clinical suspicion of malignancy, despite the relatively benign CT appearance of some of these cystic renal masses. Chart reviews of the patients having the four malignant category II masses revealed that surgery was precipitated by suspicious clinical or imaging changes in all cases: paraneoplastic syndrome (one of four), interval change on imaging studies (two of four), hematuria (four of four), or flank pain (two of four). The benign category II lesion was resected in a patient w h o had a concurrent ,contralateral renal cell carcinoma. It is likely that some truly benign nonoperative category II lesions were detected over the course of this study and were not surgically removed. These lesions would not have been included in this study. Therefore, we suspect that the actual malignancy rate of category II lesions is considerably lower than the 80% rate demonstrated in this study. Nonetheless, our results suggest that at least some category II lesions may be malignant. Of the two cystic masses not assigned a Bosniak category, one was of water attenuation on unenhanced scans but of heterogeneous soft-tissue attenuation on enhanced scans, whereas the other appeared to be solid and enhancing. The former is a disturbing case and confirms that the diagnosis of a simple renal cyst cannot be made with complete certainty w h e n a small homogeneous water attenuation mass is identified only on unenhanced scans. Confusion of a cystic neoplasm with a solid mass, as was the case in our other nonclassifiable lesion, is not likely to be clinically relevant because surgical removal is required in both instances, but it is interesting. To our knowledge, this is the first reported example of an enhancing cystic renal adenocarcinoma that had these CT characteristics and the second reported
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example of a cystic renal a d e n o c a r c i n o m a mimicking a solid tumor [14]. It has b e e n shown that some small cystic renal carcinomas can contain enough solid cellular material to mimic more typical solid renal cell carcinomas [14]. Presumably, the enhancement characteristics of at least one, if not both, nonclassifiable lesions can be attributed to the septations or papillary projections of tumor within the wall of these complex renal masses that were detected pathologically. It generally has been accepted that renal mass enhancement in excess of 10-15 H after IV contrast media injection indicates malignant tumor vascularity. Such enhancing masses are usually surgically removed (unless they contain fat) because they often are renal cancers [9]. Conversely, a lack of contrast enhancement has been accepted as an indicator of the absence of vascularity and of lesion benignity. It is therefore of concern that seven of the nine classifiable malignant cystic renal masses in which attenuation coefficients were measured in this series had demonstrable contrast enhancement of no more than 10 H. Even on detailed retrospective review, no suspiciously enhancing areas could be identified in these cases. We suspect that this was primarily due to the small sizes and relative hypovascularity of the solid components of the lower category lesions. These characteristics parallel those in recent reports of cystic renal carcinomas [13, 14]. This series serves to underscore the difficulties that can be encountered w h e n obtaining enhancement measurements in cystic renal masses and certainly indicates that lack of enhancement by 10-15 H does not eliminate the possibility of malignancy. T u m o r grading with the Fuhrman system [11] is thought to have prognostic significance. The Fuhrman classification pertains to cytologic characteristics of tumor aggressiveness (i.e., nucleoli and mitotic figures) and thus its likelihood for metastasis.. Although the n u m b e r of cystic renal cell carcinomas in our series was small, our results suggest that higher category lesions m a y have higher Fuhrman pathologic grades, whereas lower category lesions have a variety of grades. The results of our study also suggest that less complex cystic renal malignancies tend to be low Robson stage [12] w h e n detected. In fact, all Bosniak category II tumors were Fuhrman grade I or II and Robson stage I renal cell carcinomas. These tumors usually are curable b y radical or partial nephrectomy.
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In summary, our experience provides evidence that although the Bosniak CT classification system is valuable, it does have limitations. A larger percentage of category II and category III lesions may in fact be malignant than was predicted by Bosniak [4] and found by Aronson et al. [7]. We also show that m a n y cystic renal cancers do not have the contrast enhancement patterns often associated with solid renal cell carcinomas and therefore lack of demonstrable enhancement cannot be relied on to differentiate benign complex cysts from cystic renal malignancies in at least some instances. Because most of these cystic cancers are of low Fuhrman nuclear grade and low Robson stage, they should have a good prognosis if detected early and surgically extirpated. Perhaps all category II cystic renal masses should be followed with imaging studies (IIF) to confirm long-term stability unless clinical circumstances dictate immediate pathologic confirmation. Certainly, additional experience is needed to help direct the clinical management of category II cystic renal masses.
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