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1 Both authors: NYU Medical Center, Ste. HW 202, 560 First Ave., New York, NY 10016.
Received January 24, 2003;
accepted after revision March 28, 2003.
Address correspondence to G. M. Israel
(gary.israel{at}med.nyu.edu).
Abstract
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MATERIALS AND METHODS. The CT scans of 42 moderately complex cystic renal masses (Bosniak category IIF) with follow-up examinations for 2 years or greater or with pathology correlation (n = 3) were retrospectively analyzed by the authors in consensus. The complexity of each lesion was assessed on the basis of the number and appearance of the septa, wall thickness, interface with the kidney parenchyma, presence and amount of calcification, and contrast enhancement characteristics. Lesion size was measured in two dimensions. Follow-up examinations were evaluated for any interval change.
RESULTS. The average size of the lesions was 3.9 x 3.6 cm, and the average follow-up time was 5.8 years (range, 2 years-18 years 4 months; median, 5.0 years). Eighteen lesions had fewer than five septa, 16 lesions had between five and nine septa, and eight lesions had more than nine septa. In 39 lesions, the wall or septa or both were slightly thickened, and in a single lesion, the wall and septa were hairline thin. The two remaining lesions were of uniformly high attenuation and completely intrarenal. Forty-one lesions had a sharp interface with the kidney, whereas one had an indistinct interface. Twenty lesions contained calcium. Enhancement was not shown in any lesions except for minimal enhancement of smooth walls or septa of some lesions. Follow-up examinations showed that three lesions had developed more calcification, one lesion had increased in overall size but appeared less complex, and three lesions had decreased in size. In addition, two lesions had become more complex and developed thicker septa, and these lesions proved to be cystic neoplasms.
CONCLUSION. Follow-up CT studies are an effective way of managing patients with moderately complex cystic lesions of the kidney (Bosniak category IIF) because the absence of change supports benignity and progression indicates neoplasm.
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There is a group of cystic lesions that are not complex enough to be characterized as category III but that are more complex than category II lesions. These cysts, referred to as category IIF (F for follow-up), are thought to likely be benign but because of their complexity require follow-up studies to prove their benignity [2-5]. They may contain an increased number of septa or have minimal thickening of the wall or septa, and whether there is measurable enhancement of these structures is often uncertain. These lesions do not need surgical exploration, as would a more complex category III lesion, because they are thought to be benign. They can be managed with follow-up examinations to show their stability over time, thereby proving their benignity and saving the patient from undergoing an unnecessary surgical intervention. The purpose of this study is to show the use of follow-up CT studies in the management of these moderately complex cystic lesions of the kidney (Bosniak category IIF).
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The study group consisted of 25 men and 16 women with an average age of 57.8 years (range, 30-86 years). We attempted to obtain all subsequent CT examinations for each patient to ensure the longest possible follow-up interval. Pathologic correlation was available in three patients who underwent surgery after the follow-up studies. This study was approved by the institutional board of research associates at our institution.
Because our study was retrospective and the cases were collected over approximately 10 years, the examinations were performed on a variety of helical and conventional CT scanners using different slice collimations (range, 3-10 mm). In addition, the type and amount of IV contrast material also varied. However, all examinations were performed before and after IV contrast administration.
Image Analysis
Each case was retrospectively analyzed by the authors in consensus. The
complexity of each lesion was assessed on the basis of the number and
appearance of the septa, wall thickness, interface with the kidney parenchyma,
presence and amount of calcification, and contrast enhancement
characteristics. The diameter of each lesion was measured in two dimensions
using handheld calipers. The follow-up examinations were analyzed for any
interval change.
The number of septa in each lesion was determined, and each lesion was placed in one of three categories: fewer than five septa, between five and nine septa, and more than nine septa. In addition, the thicknesses of the septa and the wall of each lesion were subjectively determined to be either hairline thin or slightly thickened. If either a single septum or the wall of a lesion was determined to be slightly thickened, this finding was recorded as a slightly thickened septum or wall for the entire lesion. The interface of the lesion with the surrounding renal parenchyma was determined to be either sharp or indistinct. Contrast enhancement was evaluated using multiple region-of-interest measurements performed at the time of each examination.
For the lesions that contained calcium (17 calcified lesions were reported as part of a previous study [6]), a subjective scoring system of 1-4 was used. A score of 1 was given for minimal calcification, which was defined as hairline-thin smooth strands of calcium. A score of 2 was given for mild calcification, which indicated some thickness and minimal nodularity of the calcification. A score of 3 denoted moderate calcification, which was defined as further thickness of the calcification or grossly nodular calcification (or both). A score of 4 represented grossly thickened, nodular, and extensive calcification.
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Twenty lesions contained calcium with an average calcification score of 2.7 (Fig. 5). At initial presentation, the calcification score of each lesion was as follows: a calcification score of 1 in two lesions, a calcification score of 2 in five lesions, a calcification score of 3 in 10 lesions, and a calcification score of 4 in three lesions. Three lesions were shown to have developed more calcification on follow-up examinations, two of which increased by one calcification score over an average of 6.8 years (range, 6 years 6 months-7 years). One of these two lesions was pathologically proven to be a benign multilocular cyst, and the patient underwent surgery at the discretion of the referring physician. The third lesion increased by two calcification scores over 18 years 4 months.
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Follow-up examinations showed that three lesions had decreased in diameter (range, 1-3 cm; average, 1.8 cm), and two lesions had grown. The first of these two lesions, which increased from 2 to 2.5 cm over 4 years 7 months, initially contained septa that were slightly thickened (Figs. 6A, and 6B). On the follow-up examinations, the septa were less apparent and the lesion appeared less complex. The second lesion that had grown was a case from an outside institution which was sent to one of the authors for consultation. Initially, a 2-cm moderately complex cystic mass was identified. Follow-up examinations were recommended and were performed at the outside institution. A 1-year follow-up examination showed no change in the lesion. The next follow-up examination was performed 2 years later (3 years after the initial examination), and it showed that the lesion had grown to 4 cm and that the septa had become thicker and nodular. This lesion proved to be a cystic renal cell carcinoma. One final lesion that had not increased in size over a follow-up period of 1 year 4 months had become more complex and developed thicker septa; this lesion proved to be a cystic neoplasm (Figs. 7A, and 7B). This lesion was included in our series because it was originally interpreted as category IIF, even though it could be consistent with a category III lesion.
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Category I (simple cysts) and category II (mildly complex cysts) lesions (Appendix 1) are considered benign and do not require treatment. Their diagnosis and differentiation are usually straightforward and without difficulty or disagreement between observers. The differentiation of category III and IV lesions can occasionally cause difficulty but is not essential because both require surgery, although the surgical approach may be different. However, differentiating more complex category II lesions (nonsurgical) from some less complex category III lesions (surgical) is important because their recommended management is different, and these cases cause the most difficulty in diagnosis and the most interobserver variation [11].
In 1993, Bosniak revised the original classification system [2] to include a subset of category II lesions, category IIF lesions ("F" for follow-up) [5]. These lesions do not fall neatly into category II because they are more complex. They do not require surgical exploration because they are thought to be benign, but they do require follow-up examinations to prove they are benign by showing no substantial change in appearance. Category IIF lesions may contain increased numbers of thin septa or a slightly thickened but smooth septum or wall. They may also contain calcification that may be thick and nodular, but they do not contain any associated enhancing soft-tissue elements [6]. Completely intrarenal high-attenuation cysts 3 cm or larger fall into this group (category IIF) as well (Appendix 1).
Unfortunately, quantifying the number of hairline-thin septa that would upgrade a lesion from category II to category IIF is not possible. This number depends on many factors including the size of the lesion. For example, a 10-cm thin-walled cystic lesion containing a few hairline-thin septa would not be a worrisome finding and would be placed in category II. However, a 4-cm thin-walled cystic lesion containing the same number of hairline-thin septa would appear more complex. In this smaller lesion, the septa would be closer to each other and have less surrounding fluid, giving the lesion a more troublesome appearance. In this situation, the smaller lesion might warrant a follow-up examination and might be placed in category IIF, whereas the larger lesion might not. The 24 lesions in this cohort that contained more than five septa had an average size of 4.4 x 4.7 cm. Furthermore, 23 of these lesions also contained a slightly thickened septum or wall. In only a single 8-cm lesion, which contained more than nine septa, were all septa hairline thin.
Quantifying the thickness of the septa or wall that would place a lesion in category IIF is also not possible. However, any thickness to the septum or wall that is greater than hairline thin would upgrade a lesion from category II to category IIF. In our series, 39 of the 42 lesions contained either a septum or wall that was slightly thicker than hairline thin. It is this slight thickening that requires that these lesions be studied further. However, the septal or wall thickening that may occur in category IIF lesions is mild and smooth and is not the gross irregular wall or septal thickening present in category III lesions.
In some cases, a cluster of small simple cysts may superficially appear as a large, more complex lesion. The walls of these small cysts lie adjacent to each other, giving the appearance of slightly thickened septations in a large mass. Often, a small portion of normal renal parenchyma may insinuate itself between cysts, mimicking enhancing soft tissue in the wall of the lesion. In this instance, it is important to verify that the tissue between the cysts enhances identically to the renal parenchyma and does not exhibit enhancement characteristics typical of abnormal tissue associated with a cystic neoplasm. In recent cases and with the advent of multidetector CT (MDCT) scanners, we find that scrolling through thin-section images in succession on a workstation helps establish the relationship of the cysts to each other and to the renal parenchyma that has been incorporated between the cysts. As more studies are performed with MDCT scanners, this technique may prove helpful in evaluating some of these cases.
Differentiating a complex benign multilocular cyst from a multiloculated cystic neoplasm is usually impossible with imaging studies. These lesions appear as category III lesions and will be removed. However, there does exist a small percentage of less complex multiloculated cystic neoplasms that can appear as category IIF lesions. Nevertheless, these lesions will appear more complex on follow-up examinations, and their true nature will become apparent. This scenario occurred in two cases in our series. In one of these cases, which is shown in Figures 7A, and 7B, one could argue that the initial interpretation of category IIF was faulty and that, in fact, the lesion should have been placed in category III initially. However, the follow-up examination did clearly indicate increased septal and wall thickening, and its malignant nature became obvious. In the second case, the malignant nature of the lesion also became apparent on the follow-up examination, which showed a gross soft-tissue thickening in a previously moderately complex cyst.
Calcification is common in cystic lesions of the kidneys and can be seen in both benign and malignant lesions [12]. Hairline-thin calcification or a short segment of slightly thickened but smooth calcification may be present in the septum or wall of minimally complex renal cysts (category II), whereas either large or small amounts of calcification may be present in more complex lesions (categories IIF, III, and IV). Category IIF renal cysts may contain irregular, thick, and nodular calcification as long as no associated enhancing soft-tissue components are present [6]. Furthermore, the amount of calcification can increase over time without indicating malignancy. This finding occurred in three of the 20 calcified lesions in this series. However, if the septum or wall becomes thicker or irregular with any sign of an increase in the soft-tissue component, the lesion should be considered category III (or IV) and approached surgically.
Hyperdense (or high-attenuation) renal cysts are difficult cystic lesions to evaluate: the thickness of the wall or the internal composition of the lesion cannot be assessed because the homogeneous high-attenuation fluid inside the lesion masks these structures. Therefore, the major diagnostic criterion used in evaluating these cysts is the presence or absence of enhancement. The highest quality examination needs to be performed when characterizing these masses, and numerous region-of-interest measurements need to be obtained from all parts of the lesion on the unenhanced and contrast-enhanced examinations to ensure that there are no enhancing components. Hyperdense cysts are commonly seen. When they measure less than 3 cm, are round and sharply marginated with at least one quarter of the lesion extending outside the renal parenchyma, and most importantly do not enhance, a diagnosis of a benign hyperdense cyst (category II) can be made. These criteria and this approach have been accepted by most radiologists and are used in general practice. However, when hyperdense cysts are completely intrarenal and measure 3 cm or larger, the diagnosis of a benign lesion cannot be made with as much confidence. In this case, a portion of the lesion does not extend outside the renal parenchyma, so the morphology and smoothness of the wall cannot be accessed. These lesions may appear to have a slightly indistinct interface with the surrounding renal parenchyma (as did one of the two intrarenal high-density lesions in this series). They must be considered category IIF, and follow-up examinations need to be performed to show their stability over time. Alternatively, MRI may prove helpful in the characterization of these troublesome lesions and may possibly avoid the need for follow-up examinations in these cases [13].
When a complex cystic lesion considered to be category IIF is encountered, the radiologist must be certain that the referring physician clearly understands that the lesion in question is likely benign but that it does have some worrisome features and that follow-up examinations are necessary to prove stability and, therefore, benignity. Some patients, particularly those who are young, may not want to use a follow-up approach and may want surgical intervention for a definitive immediate diagnosis. However, if the follow-up approach is taken, we recommend the first follow-up examination occur 6 months after the initial examination. If the lesion is unchanged, additional follow-up examinations should be performed at yearly intervals for at least 5 years, although the optimal follow-up period has not yet been determined. The length of follow-up depends on a number of factors including the patient's age as well as the size and complexity of the lesion. In general, we think that a 5-year follow-up period in patients older than 50-60 years is adequate to show that a complex cystic lesion is stable. However, in younger patients, a longer follow-up period may be necessary. Many patients (and physicians) do not want additional follow-up studies to continue after 3 years (which may be adequate in less complex category IIF lesions). This follow-up protocol should be used to follow up these patients when possible. Obviously, further experience is necessary to come to a definitive conclusion regarding the proper interval and length of follow-up necessary in these cases. In this series, many patients had long-term follow-up examinations. These examinations were performed either because the patient or the physician requested them or, more often, because the patient was imaged for a different reason and those examinations became available for comparison. Longer follow-up periods may be appropriate in the more complex category IIF lesions and in young patients because no data that describe long-term follow-up of these cystic lesions are available.
In general, we prefer to perform CT studies initially as the follow-up examination. This examination allows a precise and direct comparison of the thickness of the septa and wall of the lesion. MRI can be performed for follow-up, particularly in young patients, to reduce radiation exposure or in patients with renal insufficiency. Although CT and MRI examinations are often compatible in terms of assessing cystic renal lesions, at times they are not equivalent. In our experience, septa are more prominent and obvious on MRI studies, so comparing a CT scan with a subsequent MRI study may be difficult.
If a lesion grows slightly, this change should not be perceived as troublesome because even benign simple cysts grow. If the septa and wall of the lesion are unchanged, this finding supports benignity and continued follow-up is recommended. However, if an increase in the thickness or in the irregularity of the wall or septa is seen, surgical exploration is necessary because either finding indicates malignancy. In this series, only two of the 42 lesions were shown to have increased in size at the follow-up examination. One lesion grew from 2 to 2.5 cm over 4 years 7 months, became less complex, and was thought to be benign. The second lesion increased from 2 to 4 cm over 3 years and developed thicker and more complex septa; a cystic neoplasm was ultimately diagnosed at pathology. This case illustrates the value and importance of the follow-up approach to the management of these cases, in which a lesion initially thought to most likely be benign (even though complex) is shown to be a surgical lesion (most likely malignant) on a follow-up examination. It also shows that if this strategy is used, the follow-up studies must be performed on a timely basis.
One might argue that all category IIF lesions should be surgically removed. That assertion may be true in some young patients or in those uncomfortable with the follow-up approach, but this strategy does not seem appropriate for the general population. Because only two of the 42 category IIF lesions in our series were found to be malignant, a surgical approach does not seem justified. These malignant cystic lesions may represent a low-grade variant of renal cell carcinoma [14]. They are associated with a better prognosis than other renal malignancies [15] and have less tendency to metastasize [14-16]; in fact, some have "at most low malignant potential" [16]. Therefore, in those few cases in which a diagnosis of malignancy is delayed until follow-up examinations reveal the true nature of the lesion, the welfare of the patient does not appear to be compromised.
We recognize several limitations of this study. The cases in this series were reanalyzed in consensus, so interobserver variability could not be evaluated. Because the study lesions were complex, placement of some into category IIF might not be accepted by all radiologists and is open to a difference of opinion. Some of the category IIF lesions included in this group might well be considered category III by some observers. In general, we believe that if the complexity of a category II lesion is in question, the lesion should be placed in category IIF and followed up. Likewise, if there is a question as to whether a lesion belongs in category IIF or category III, the lesion should be placed in category III. Intervention could then be influenced by clinical parameters such as the patient's age and physical condition. Although the Bosniak classification system is based only on imaging findings, the incorporation of clinical parameters may lead to variability in the management of some cases.
Another limitation of the study is that the examinations were retrospectively collected. This factor introduces a case selection bias and our cohort is not all-inclusive. Also, some patients with a category IIF lesion were lost to follow-up because they relocated, changed physicians or hospitals, or did not heed the advice to undergo further follow-up. Next, the CT protocol was not standardized across all cases, although all examinations were performed before and after IV contrast administration.
Pathologic proof is available in three of the 42 cases. Because category IIF lesions are not usually surgically removed, follow-up studies need to be performed to document their stability and thereby confirm their benignity. As we discussed previously, the length of follow-up to prove benignity has not been established. However, on the basis of our experience gathered with this case material, we believe a lesion that is stable over a 5-year period certainly implies benignity. Because cystic lesions of the kidney have a slow growth pattern, longer follow-up periods may be prudent. This more cautious approach is especially prudent for more complex lesions, patients with multiple complex lesions, and young patients. The average follow-up in our series is 5.8 years. We included many cases with prolonged follow-up, not because we believe that follow-up for more than 5 years was needed in many of the cases, but because the data were available. These cases support the contention that follow-up of more than 5 years is not generally necessary. Finally, the sample size is relatively small, and additional studies with increased numbers of patients and longer follow-up would be of value.
In summary, differentiating complex cystic renal masses that require surgical intervention from those that do not remains a difficult and common problem. Evaluation of the number and appearance of the septa, wall thickness, interface with the kidney parenchyma, presence of calcification, and contrast enhancement characteristics of a lesion determines its nature and ultimate management. For patients with moderately complex cystic lesions of the kidney that fall into the Bosniak category IIF group, follow-up examinations have proven to be an effective management strategy. The stability of these lesions over time supports benignity and avoids unnecessary surgical intervention from being performed, whereas progression indicates neoplasm. However, if a complex cystic lesion is placed in category IIF, follow-up studies must be performed as outlined in this article to ensure that the lesion is benign and a nonsurgical approach is justified.
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