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1
Department of Radiology, Medical University of South Carolina, 169 Ashley
Ave., Main Hospital, Rm. 297, Box 250322, Charleston, SC 29425.
2
Department of Radiology, UCLA School of Medicine, 10833 Le Conte Ave., Los
Angeles, CA 90095-1721.
3
Department of Urology, Medical University of South Carolina, Charleston, SC
29425.
Received October 22, 1999;
accepted after revision January 4, 2000.
Presented at the annual meeting of the American Roentgen Ray Society, New
Orleans, May 1999.
Abstract
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MATERIALS AND METHODS. The scans of 109 patients were gathered from two large teaching institutions both prospectively and retrospectively, yielding a total of 116 analyzable renal cystic lesions. Eighty-two masses were resected from 77 of these patients, retrospectively categorized by two experienced uroradiologists using the Bosniak classification system, and correlated with pathology reports. A second group of 34 lesions in 32 patients with atypical cysts was followed up prospectively for periods ranging from 3 months to 10 years.
RESULTS. The results were similar for the two institutions: 15 resected categories I and II lesions were correctly identified as benign, and all 18 category IV lesions were malignant. Twenty-nine (59%) of 49 pooled category III masses were malignant. No malignancies have been identified in the prospectively monitored group of patients.
CONCLUSION. Our results are compared with earlier, smaller series and support those that show that the Bosniak classification system is useful in separating lesions requiring surgery from those that can be safely followed up, provided proper CT techniques are used.
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Eighty (73%) of the 109 patients underwent dedicated renal CT studies with imaging of the kidneys performed both before and after the IV injection of contrast material. Fifty-one (88%) of the 58 categories II and III patients were examined with dedicated renal studies. Hounsfield unit measurements were obtained on the lesions on both sets of scans. Section thickness varied from 3 to 10 mm, and collimation was 7 mm or less in 54% of the patients examined. A variety of scanners, both helical and conventional, from different manufacturers were used, but all provided shorter than 2-sec scan acquisition times. The types and amounts of injected water-soluble contrast material also varied, but all patients received IV contrast material.
Of the 116 cystic masses analyzed, 82 were resected from 77 patients, 25% of whom were female patients. The age range was 3.5-81 years. Excluding the single pediatric patient, the mean age was 60 years. Masses ranged in diameter from 1.5 to 11 cm, with 29 lesions (35%) measuring 3 cm or less in diameter (Table 1). The masses were retrospectively characterized using the Bosniak classification system and were correlated with pathology reports (Table 2).
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Thirty-four lesions in 32 patients who underwent follow-up CT rather than surgery were also identified prospectively. Five of these masses were needle-aspirated or biopsied. The lesions ranged in size from 1 to 12 cm, with 47% measuring 3 cm or less in diameter. These patients were observed for periods ranging from 3 months to 10 years, as follows: nine lesions were observed for less than 1 year, eight for 1-2 years, six for 2-3 years, and nine for 4-10 years. Ten of the patients (31%) were female.
Exclusion Criteria
Fifteen of the examinations were eliminated from consideration because the
imaging studies were not adequate to apply the classification system. Masses
were not included that showed more than half their volume to be solid. Lesions
were also excluded when the section thickness was greater than one half the
largest diameter of the lesion.
Bosniak Classification
All lesions were retrospectively assigned a Bosniak classification number
by consensus of the two radiologist authors on the basis of the following
criteria
[1,2,3,4].
Category I.—Category I lesions are simple benign cysts showing homogeneity, water content, and a sharp interface with adjacent renal parenchyma, with no wall thickening, calcification, or enhancement.
Category II.—This category consists of cystic lesions with
one or two thin (
1 mm thick) septations or thin, fine calcification in
their walls or septa (wall thickening > 1 mm advances the lesion into
surgical category III) and hyperdense benign cysts with all the features of
category I cysts except for homogeneously high attenuation. A benign category
II lesion must be 3 cm or less in diameter, have one quarter of its wall
extending outside the kidney so the wall can be assessed, and be nonenhancing
after contrast material is administered.
Category IIF.—This category consists of minimally complicated cysts that need follow-up. This is a group not well defined by Bosniak but consists of lesions that do not neatly fall into category II. These lesions have some suspicious features that deserve follow-up to detect any change in character.
Category III.—Category III consists of true indeterminate cystic masses that need surgical evaluation, although many prove to be benign. They may show uniform wall thickening, nodularity, thick or irregular peripheral calcification, or a multilocular nature with multiple enhancing septa. Hyperdense lesions that do not fulfill category II criteria are included in this group.
Category IV.—These are lesions with a nonuniform or enhancing thick wall, enhancing or large nodules in the wall, or clearly solid components in the cystic lesion. Enhancement was considered present when lesion components increased by at least 10 H.
Data recorded included the patient name, age, sex, hospital number, short medical history, date of initial scan and any follow-up scans, slice thickness, and Hounsfield attenuation before and after contrast enhancement. Ancillary studies such as sonography, fine-needle aspiration, biopsy, angiography, and MR imaging were noted. Lesion characteristics such as enhancement, homogeneity, wall thickening, septations, calcifications, and size were recorded, as was the Bosniak classification assigned by the investigators on the basis of these features. Surgical findings from pathology reports, fine-needle aspirations, and biopsies were obtained.
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Table 2 depicts the surgical outcome for the two institutions correlated with the Bosniak categorization. The classification scheme accurately predicted outcome for categories I, II, and IV. The 15 pooled categories I (n = 4) and II (n = 11) lesions all proved to be benign, and the 18 category IV lesions were all malignant. Twenty (65%) of 31 category III lesions at the first institution were malignant versus nine (50%) of 18 at the second institution. Using the Fisher-Halton-Freeman two-sided exact test, these results were not significantly different between the two institutions. Twenty-nine (59%) of the 49 pooled lesions in category III, those considered truly indeterminate by Bosniak, were malignant.
Nonsurgical Group
Thirty-two patients with complex lesions from both institutions were
followed up for periods ranging from 3 months to 10 years. Sixteen (47%) of
these lesions were 3 cm or smaller in diameter. Nine of these patients had
follow-up imaging of less than 1 year, and 23 were followed up for 1-10 years.
Needle aspiration of three of these lesions yielded diagnoses of hemorrhagic
cysts and one abscess. No malignancies have been identified in this
prospectively monitored group. Most were classified into category II or IIF
except for two category I lesions, three category III lesions, and two
category IV lesions, described in the following text.
Category I.—A patient with an incidental 2-cm-diameter hyperdense cyst was found to have a prior CT scan 7 years earlier that showed the lesion to be a simple cyst. No further change was noted after an observation period of 1 year 4 months. Another patient with a 1-cm simple cyst had a second CT performed (5 months after the first) that showed questionable medial wall enhancement. The lesion was aspirated and yielded serosanguineous fluid and "rare, atypical renal cells" but no definite evidence of malignancy. No further follow-up took place.
Category III.—An elderly male patient with a category III multiloculated lesion refused surgery or other intervention. Follow-up CT 4 months later showed slightly decreased lesion size. No further imaging was performed, but the patient was alive and well 6 years later. A patient with acquired uremic cystic disease had a 6-cm heterogeneous cystic mass (category III) without enhancement. On CT scans obtained 6 months earlier, the lesion showed simple cystic characteristics. It was aspirated, yielding bloody fluid with negative findings on cytology. A second scan 3 years later showed complete resolution of this lesion. A third category III lesion in an elderly woman had not changed over 3 months; it may have been a cluster of adjacent cysts.
Category IV.—A category IV mass in a patient with clinical signs of infection proved to be an abscess at aspiration. On follow-up imaging it was decreased in size. Another patient had a category IV cystic mass with a thickened, slightly irregular wall and internal heterogeneity that was reported at an outside hospital to be "a complex cystic mass not compatible with simple cyst." For unknown reason, the patient underwent no further evaluation. Ten years later he presented with solidification of the mass and contralateral metastases. He died within a year.
No attempt was made to systematically identify and follow up all cysts encountered. The number of cases of complicated cysts we found is proportionally small compared with the number of surgical cases collected. The lesions were identified in the course of everyday practice by two radiologists at two institutions, and only those with CT follow-up to assess change were included, which excluded categories I and II lesions deemed benign at initial encounter by other radiologists at the same hospitals who were not participating in this study.
The length of time necessary to declare a stable lesion benign is currently unknown. Bosniak originally suggested that initial follow-up scans be performed at 3 months, 6 months, and 1 year [3]. In a later commentary, he advised the initial scan should be obtained at 6 months and repeated at 1-year intervals, although he did not specify how long this should be carried out [4]. It seems reasonable that imaging findings unchanged at 6 months, 18 months, and 3 years ought to suffice. All follow-up scans should be obtained as dedicated renal studies and should be compared with the original baseline images.
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In 1986, Bosniak [1] proposed a classification system designed to separate cystic renal masses into surgical and nonsurgical categories by analysis of specific CT features. He elaborated further on this topic in later publications and commentary [2,3,4]. Category I lesions are readily recognized as simple cortical cysts and rarely cause problems in diagnosis. Category II lesions are minimally complicated cysts that may be left alone provided they fulfill imaging criteria set out in the classification. Bosniak emphasized that clinical features should play a role in deciding whether some of these lesions should be followed up. Category III lesions are the truly "indeterminate" cystic masses that are as likely to be benign as malignant and must be evaluated surgically. Category IV lesions are usually obvious and are nearly always malignant. Clearly, the hardest distinction—and the most important to make—is between categories II and III, because this determines whether surgery is necessary. This classification system has been used with various degrees of acceptance and success. Several smaller studies have examined its usefulness with conflicting results (Table 3) [5,6,7,8,9].
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Aronson et al. [5] evaluated 20 lesions in 1991, including 13 problematic categories II and III lesions, and concluded that the classification was a useful management tool. They correctly identified all four category II lesions in their series as benign and all seven category IV masses as malignant. Half their category III lesions were malignant. Favorable results were also found in a similarly small series by Brown et al. [6], although fewer malignant lesions in categories III and IV were found.
Wilson et al. [7] in 1996 cast doubt on the classification scheme, finding four of five malignancies in their category II group. However, only two of these patients had a dedicated renal CT examination, including the one whose lesion was correctly identified as benign. This series appears to be flawed by the small number of problematic categories II and III lesions (n = 9), whereas seven of the surgically resected lesions were benign simple cysts.
Cloix et al. [8] also concluded that the Bosniak system was not useful in their evaluation of 32 surgically proven lesions because they found two malignant lesions in a group of nine categories I and II masses and 11 benign lesions in the 23 lesions in categories III and IV group. No information was provided about lesion sizes, however, and all their scans were obtained with 10-mm collimation. No mention is made of whether images of the kidneys were obtained before contrast administration to assess enhancement. Analysis of both these series, Wilson et al. [7] and Cloix et al. [8], suggests that inaccurate assignment to a category because of suboptimal CT technique may have led to failure of the classification.
To our knowledge, the most recent examination of the clinical usefulness of the system was by Siegel et al. [9], published in 1997. These researchers evaluated 70 lesions in 46 patients; many of the lesions were presumably benign simple cysts removed along with a more complex lesion. They studied only 19 categories II and III lesions. One of eight category II lesions was malignant and three of the 29 category IV lesions were benign. Forty-two (60%) of the lesions were evaluated with unenhanced and enhanced CT. Thin-section (5-mm) collimation was used in 38 lesions and 10-mm collimation in 27. Hounsfield attenuation was available in fewer than half the lesions, so objective evidence of enhancement was lacking in a significant number of lesions. Two of the three benign category IV masses were multilocular cystic nephromas, which are usually classified in category III because of their multilocular nature. Misclassification of a category III lesion as category IV may have some practical importance if nephron-sparing surgery might be undertaken in place of a radical nephrectomy.
Overall, the classification was deemed useful by Siegel et al. [9], but that study also showed considerable disagreement among three radiologists in categorization. Not surprisingly, this discordance was greatest in the problematic categories II and III. This interobserver variability may be the result of differing levels of experience, but suboptimal CT technique may have played a role.
Our series represents the largest number of patients and lesions reported and the largest number of pathologically proven results. In addition, our series includes 32 patients with 34 cystic renal masses that were followed up for periods from 3 months to 10 years. Like its predecessors, our study can be criticized for case selection bias, small sample size, and incomplete adherence to optimal dedicated renal CT technique. Some patients were referred from other institutions at which a standard scan had already been obtained. Other patients were identified on scans obtained for evaluation of disorders unrelated to the kidneys. However, despite the fact that only 73% of our surgical group of patients had both unenhanced and enhanced images, 88% of the difficult subgroup of patients with categories II and III lesions were investigated appropriately.
Our results support the use of the Bosniak classification system as a guide for distinguishing which cystic renal masses require surgical intervention provided proper CT technique is used in evaluating these lesions. The two main sources of error in evaluating cystic renal masses have been difficulties with interobserver variation and improper CT technique [4, 9]. It is difficult to influence the former, which depends heavily on experience and expertise, and we have not attempted to address that issue in this paper.
When an appropriate dedicated renal CT technique is used, the Bosniak
classification system is a practical methodology that limits the number of
complex cystic renal masses requiring surgery and may influence the choice of
surgical technique. Both unenhanced and contrast-enhanced thin-section scans
should be obtained, preferably on a helical scanner that eliminates
respiratory misregistration. Collimation (ideally, 5 mm) must be less than
half the diameter of the lesion to allow adequate assessment.
The degree of enhancement of a lesion reflects its vascularity and is a critical factor in proper categorization. This requires an adequate bolus of contrast material (at least 100 mL of a contrast agent containing 300 mg I/mL) power-injected at a rate of 2-3 mL/sec. Timing of image acquisition is also critical. The contrast-enhanced images should be obtained in uniform nephrographic phases approximately 100 sec after the start of injection. Images obtained in the earlier corticomedullary differentiation phase may obscure the lesion or provide misleading information.
Measurements of regions of interest in comparable portions of the lesion should be obtained to evaluate enhancement, with all imaging parameters (i.e., field of view, position in gantry, collimation, pitch, kilovoltage, and milliamperage) held constant between the unenhanced and the contrast-enhanced scans [10]. Region-of-interest sampling in a cyst should be central and should include as much area as possible. Areas of nodulation should be measured if present.
Some concerns exist about the reliability of attenuation numbers obtained from helical scanners. Pseudoenhancement may be encountered because of beam hardening or broadening of the section sensitivity profile. A recent small study showed the degree of pseudoenhancement was not more than 10 H in lesions greater than 2 cm in diameter, although eight (26%) of 31 cysts smaller than 2 cm increased by at least 10 H [11]. Machines should be frequently calibrated, and internal comparisons made with known cystic structures such as the gallbladder and the nonopacified renal pelvis. Retrospective reconstruction over small intervals can be performed with helical scanners to more accurately sample a lesion exhibiting suspected partial volume effect. Incomplete or indeterminate studies should be repeated if necessary.
In the event of incidental discovery of a homogeneously high-attenuation (>30 H) renal mass in patients in whom no preliminary unenhanced scanning was performed, Macari and Bosniak [12] recently suggested that a delayed scan at 15 min may provide sufficient information to distinguish between a benign high-density cyst and a neoplasm. Deenhancement of the lesion suggests vascularity and the likelihood of neoplasm, whereas unchanging high attenuation is consistent with a high-density avascular cyst.
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