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 retro- spectively. 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 fol- lows: 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 limita- tions of the Bosniak classification system because most of our category II and all of our category IIl lesions were malignant, suggesting that mini- really complex cystic renal masses may contain malignant cells. Contrast enhancement of less than 10 H was demonstrated in lesions in categories II and III.
C 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
From the Departments of 1 Radiology and 2pathology, University of Michigan, Ann Arbor, MI.
Address reprint requests to R. H. Cohan, MD, De- partment 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.
Vol. 3, No. 7, July 1996 BOSNIAK CLASSIFICATION SYSTEM AND RENAL MASSES
in cysts. Appropriate imaging, and clinical management
of these cases can be difficult.
To assist in the management of patients with cystic
renal masses, Bosniak [4] proposed 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 number 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 proposed that all category I and II lesions do not need additional imaging or surgical inter- vention 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 classifi- cation system. Their results supported Bosniak's predic- tions 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 own experience with the Bosniak classifi-
cation 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 pathol- ogy and radiology databases be tween 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 diag- nostic CT examinations and could be classified by the
Bosniak system. The remaining two patients had patho- logically proved cystic lesions that had CT characteris-
tics not included in the Bosniak classification system. Overall, these 20 patients included 14 men 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, Mil-
waukee, WI). Nine patients had dedicated renal CT exam- inations with contiguous 5-ram collimated scans obtained
both before and after dynamic intravenous (IV) contrast agent administration (two of which were performed spi- rally, 1:1 pitch, 5 mm/sec table feed). One patient had 10-
ram-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 diatri-
zoate-60 (Hypaque; Nycomed). One patient received a 75- ml bolus of iohexol-300 because of an elevated serum cre- atinine level. Bolus infusion of contrast material was deliv- ered 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, impercepti- ble wall, water attenuation, nonenhancement, and absence of nodularity or septations) were classified as category I lesions. Hyperdense cysts or water attenuation masses hav- ing one or two thin septations, peripheral calcifications, or both were classified as category II cysts. Water attenuation masses having multiple loculations, nonenhancing nod- ules, 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 attenua- tion increase of at least 10 Hounsfield units (H).
There were two masses in two patients that were sub- sequently 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 con- tiguous 5-mm collimated images and two had contigu-
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WILSON ET AL. Vol. 3, No. 7, July 1996
TABLE 1: Bosniak Classification System
Bosniak No. Features Leading MalignantTotal for Category Categorization Each Feature
I 7 Simple cyst 0/7 II 5 Thin septation (<1 mm) 2/3
IV 6 Nodularity 2/2 Thick wall 4/4 Solid component 4/4
No 2 Enhancement 2/2 category
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 sam-
pled [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 patholo- gist who 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 composed of macroscopic cysts (>2 mm). Tumors were considered to be mixed cystic and solid when the cystic componen t made up 25-75% of the area and solid when 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 accord- ing to the Robson system [121.
RESULTS
Bosniak Classif ication
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 malig-
nant. This included four of the five cysts considered to
Vol. 3, No. 7, July 1996 B O S N I A K C L A S S I F I C A T I O N S Y S T E M A N D R E N A L M A S S E S
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 cate-
gory III and IV masses. Two cystic masses could not be classified using Bos-
niak's system. One was a homogeneous near-water atten- uation 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 con-
trast 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 catego-
rized 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 lym-
phoma 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
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W I L S O N ET AL . VoL 3, No. 7, July 1996
FIGURE 5. Unclassifiable lesion. This contrast-enhanced computed tomogra- phy scan from an obese 54-year-old woman shows a small, low-attenuation le- sion 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 exhib-
ited papillary histology. The other undefinable cystic renal cell carcinoma was found on pathologic examina-
tion 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.
M e a s u r e d E n h a n c e m e n t
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 5- mm 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-
FIGURE 6. Unclassifiable lesion. This contrast-enhanced computed tomogra- phy 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.
P a t h o l o g i c G r a d i n g
Fuhrman nuclear grading [11] was performed on 13
cystic renal carcinomas, including the two unclassified
masses (Table 3). Of the classified masses, one cate-
gory II lesion and one category IV lesion had Fuhr- man 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 cate-
gory III lesion could not be classified because of exten-
sive cellular lysis, one category IV lesion had only
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Vol. 3, No. 7, July 1996 B O S N I A K C L A S S I F I C A T I O N S Y S T E M A N D RENAL M A S S E S
TABLE 3: Robson Stages and Fuhrman Grades
Robson Category Fuhrman Grade Stage
II 1/4 g rade I I 3/4 g rade II I
III 1/4 necrot ic I 1/4 l y m p h o m a NA
2/4 g rade II IIIc, I IV 1/6 g rade I I
1/6 g rade II I 1/6 g rade III I 1/6 g rade II II 1/6 g rade III II
1/6 aspiration and therefore no grade or stage
Unclassified 2/2 grade II I
cytopathology results available, and one category III lesion was a lymphoma.
Pathologic Stag ing
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 unclas- sified masses. Two 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 lymphade-
nopathy detected at surgery.
D I S C U S S I O N
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 cat-
egory II lesions as classified by 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 cate- gory III lesions is expected and has been reported [5, 6,
13, 14]. In one of our 'patients, there was disagreement about whether a lesion should have been 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 nar- row 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 aspira- tion biopsy was performed on these patients because of ongoing symptoms and a strong clinical suspicion of malignancy, despite the relatively benign CT appear- ance 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 suspi-
cious clinical or imaging changes in all cases: paraneo- plastic 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 who had a concurrent ,contralateral renal cell carcinoma.
It is likely that some truly benign nonoperative cate- gory 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 demon- strated 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 cate- gory, 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 con-
firms that the diagnosis of a simple renal cyst cannot be made with complete certainty when a small homoge-
neous water attenuation mass is identified only on unen- hanced 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 sur- gical removal is required in both instances, but it is inter-
esting. To our knowledge, this is the first reported example of an enhancing cystic renal adenocarcinoma that had these CT characteristics and the second reported
5 6 9
W I L S O N E T AL. vol. 3, No. 7, July 1996
example of a cystic renal adenoca rc inoma mimicking a
solid tumor [14]. It has been shown that some small cys-
tic renal carcinomas can contain enough solid cellular material to mimic more typical solid renal cell carcino- mas [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 can- cers [9]. Conversely, a lack of contrast enhancement has been accepted as an indicator of the absence of vascular- ity 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 identi- fied 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 charac- teristics parallel those in recent reports of cystic renal car- cinomas [13, 14]. This series serves to underscore the difficulties that can be encountered when 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. Tumor 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
number of cystic renal cell carcinomas in our series was small, our results suggest that higher category lesions may have higher Fuhrman pathologic grades, whereas
lower category lesions have a variety of grades. The results of our study also suggest that less complex cys-
tic renal malignancies tend to be low Robson stage [12] when 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 by
radical or partial nephrectomy.
In summary, our experience provides evidence that although the Bosniak CT classification system is valu-
able, it does have limitations. A larger percentage of cat- egory 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 many cystic renal cancers do
not have the contrast enhancement patterns often associ- ated 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 progno- sis 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 con- firmation. Certainly, additional experience is needed to
help direct the clinical management of category II cystic renal masses.
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