Abstract
Purpose
The purpose of the study is to provide an update on the imaging evaluation of cystic renal masses, to review benign and malignant etiologies of cystic renal masses, and to review current controversies and future directions in the management of these lesions.
Conclusions
Cystic renal masses are relatively common in daily practice. The Bosniak classification is a time-proven method for the imaging classification and management of these lesions. Knowledge of the pathognomonic features of certain benign Bosniak 2F/3 lesions is important to avoid surgery on these lesions (e.g., localized cystic disease, renal abscess). For traditionally surgical Bosniak lesions (Classes 3 and 4), there are evolving data that risk stratification based on patient demographics, imaging size, and appearance may allow for expanded management options including tailored surveillance or ablation, along with the traditional surgical approach.
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Cystic renal masses include both benign and malignant etiologies. The term “cystic” refers to a lesion that, on imaging, has a mostly fluid-filled growth pattern with a solid portion occupying a maximum of 25% of the tumor [1–3] or a mass that is predominantly composed of spaces filled with fluid [4]. Benign cystic renal masses include the very common simple renal cyst, seen on imaging in up to 17%–41% of patients imaged for other reasons [5, 6]. Benign simple cysts can be accurately diagnosed and need no further evaluation [7], therefore these simple cysts are typically accurately diagnosed and ignored on the initial imaging study which detected them. The primary clinical concern is accurately differentiating benign complex cystic renal masses from malignant complex cystic masses. The Bosniak classification system, introduced in 1986, provides an imaging framework for the differentiation of benign and malignant cystic renal masses, and the utility of the system has been repeatedly validated to date by the international urologic and radiologic communities [8–14].
This article will review the imaging evaluation of cystic renal masses, review benign/benign-behaving lesions that may fall into the Bosniak 2F, 3 ,or 4 category (but which have features that allow for accurate suggestion of benignity, such as localized cystic renal disease or a renal abscess), and will discuss malignant cystic renal masses and associated controversies around their diagnosis and management.
The Bosniak classification
Renal cystic lesions are typically classified by the Bosniak classification system, which is based on CT findings and classifies a cystic renal mass into one of the five categories (1, 2, 2F, 3, and 4) on the basis of imaging features (Table 1; Fig. 1). In the Bosniak classification system, Bosniak 1 and 2 cystic lesions are benign and therefore, non-surgical. Bosniak category 2F (“F” for imaging follow-up), 3, and 4 lesions can have both benign and malignant etiologies, with malignancy rates increasing with increasing category. For example, malignancy rates have been reported (approximately) as 11% (range 5%–38%) for 2F lesions, 50% (range 25%–100%) for Bosniak 3 lesions, and 80% (range 67%–100%) for Bosniak 4 lesions [9, 15–19]. These rates are variable, likely secondary to different practice patterns of radiologists characterizing these lesions and urologists treating these lesions at different institutions [16, 17, 19]. Bosniak 2F lesions are typically managed by surveillance imaging. Traditionally, because of the high risk of malignancy of complex renal masses which fall in the Bosniak 3 and 4 categories, these two categories are considered best managed by surgical resection although imaging surveillance has been considered an acceptable alternative management approach in patients with a short-life expectancy or comorbidities.
Categories 1 and 2 cysts are typically straightforward to diagnose and are benign, therefore do not require follow-up. Category 4 lesions (generally cystic neoplasms) are also typically readily diagnosed as malignant, and, by conservative standards, typically require surgery. Bosniak category 2F (“F” for follow-up) and 3 cystic masses can be difficult to differentiate. Category 2F lesions are more complicated than lesions in category 2, but without frank solid enhancing component (enhancement of a thickened septation or wall) as seen in category 3. Category 2F lesions require follow-up imaging (up to 4 years in one series [14]) to prove benignity, whereas Bosniak 3 lesions have more worrisome features which conventionally require surgery.
The gold standard of surgical resection for Bosniak 3 and 4 cystic renal masses has recently come under question for a number of reasons, including analysis of data from the Surveillance, Epidemiology, and End Results database which shows that despite the earlier detection and treatment of renal cancers, most of which are detected incidentally, the mortality rates from renal cell carcinoma (RCC) have steadily risen over the past 20 years [20–22]. This suggests that imaging detects many renal lesions that will not kill the patient, which in turn suggests that there is overdiagnosis and overtreatment of renal lesions. Cystic renal mass lesions, which represent 15% of all renal mass lesions [23, 24], are a minimal contributor to this mortality rate [1, 25–28] which is predominately mediated by the solid (or solid with necrosis), large, aggressive renal mass lesion, most of which are not cured by surgery, thus leaving the overall mortality rates of RCC unaffected by surgical intervention [21]. These studies also note that resection of renal masses is not without risk, especially since the greatest incidence of renal masses (cystic and solid) occur in patients 70 years old and older, in whom medical comorbidities (cardiovascular disease, pulmonary disease, renal disease, etc.) may increase the risks of radical or partial nephrectomy [29–31].
The ongoing clinical challenge therefore lies in the ability to definitively differentiate the benign (or benign-behaving) Bosniak 2F, 3, and 4 lesions from the malignant Bosniak 2F, 3, and 4 lesions, and to further evaluate which malignant cystic masses are amenable to more conservative management, in order to tailor treatment accurately [32–37].
Imaging evaluation of cystic renal masses (the Bosniak classification)
Computed tomography
Prior articles have described the appropriate imaging technique for adequate characterization of cystic renal masses [4, 9, 38, 39], and this is beyond the scope of this article. If the initial examination that detects the cystic renal mass is inadequate for characterization, then a dedicated renal mass CT or MRI can be performed, with gray-scale sonography reserved only for the characterization of specific lesions (described in detail below). The Bosniak classification is a CT-defined classification system [7, 40], and imaging performed on a multidetector CT scanner, using renal mass technique (non-contrast images through the kidneys, followed by post-contrast imaging in the nephrographic phase [41]) will characterize most renal cystic lesions. Known challenges in using CT for lesion characterization include the phenomenon of pseudoenhancement (the artifactual increase in attenuation on contrast-enhanced CT image by 10 Hounsfield units or more, thought to be secondary to beam hardening artifact) and the pitfall of partial volume averaging in small lesions (which occurs when the size of the lesion is less than twice the slice thickness used to scan) [42]. Mileto et al. recently demonstrated that virtual monochromatic imaging in dual energy MDCT may completely eliminate renal cyst pseudoenhancement in cysts larger than 1.5 cm [43].
Magnetic resonance imaging
Several papers have shown that renal mass MR imaging is equivalent to renal mass CT for the classification of cystic renal masses in the Bosniak classification system [16, 44, 45]. For detection of internal enhancement, particularly in hemorrhagic or calcified lesions, subtraction imaging can be used [39, 46, 47]. Known pitfalls with subtraction imaging in MRI include problems with image alignment (misregistration) and with discriminating signal from true internal enhancement from signal resulting from the additive noise on subtraction images [48]. An additional problem with MR imaging is secondary to its increased sensitivity for detection of subtle internal septations and wall thickening, particularly on T2-weighted images [44], as well as its superior contrast resolution compared to CT, both of which may cause less experienced readers of MRI to erroneously upgrade cystic renal lesions [16, 44, 49]. However, morphology alone (increased depiction of septations or apparent wall thickening) without associated enhancement does not upgrade a lesion in the Bosniak classification system; the morphologic change must be associated with enhancement. Advances in MR imaging with new sequences utilizing high-resolution free-breathing 3D fat-suppressed T1 gradient echo [50] allow improved detection and clarification of internal enhancement in small cystic renal masses. Diffusion-weighted imaging techniques cannot yet accurately differentiate a cystic renal mass from a simple renal cyst; however, preliminary studies have shown promising results [32, 37, 51–54]. Characterization of cystic renal masses can be challenging; for indeterminate CT scans, our institution tends to use contrast-enhanced MRI.
Gray-scale ultrasound
Gray-scale ultrasound without contrast is limited in its utility in the diagnosis of complex renal masses, with specific exceptions. Ultrasound is useful in characterizing cystic renal masses that measure between 20 and 40 HU on CT, as these lesions typically contain internal proteinaceous material and will appear simple on ultrasound, allowing for definitive characterization. It is limited in its utility for detecting small renal lesions [55]. The poor sensitivity to vascular flow of color Doppler techniques limits the technique to only describing morphology, which in the absence of contrast enhancement is inadequate for the accurate characterization of renal mass lesions. Morphology alone cannot upgrade a lesion in the Bosniak classification system; enhancement of that morphologic finding is the key [7, 40]. Pitfalls in gray-scale ultrasound without contrast include the erroneous upgrading of cystic renal masses that appear solid or contain internal debris [56]. However, if a cystic lesion is seen on ultrasound and meets criteria for a simple cyst (i.e., is anechoic, with a well-defined border and with increased posterior through-transmission), no further follow-up is necessary [57]. Renal cystic masses with an attenuation greater than 40 HU on CT are more likely to be hemorrhagic cysts and will therefore appear complex (and thus, indeterminate) on ultrasound [4]. Multiple recent articles have evaluated the accuracy of contrast-enhanced ultrasound in evaluating cystic renal masses using the Bosniak classification, and the results have shown promise [58–61].
Size
Size is not a component of the Bosniak classification system, as small cystic renal masses can be malignant, and large cystic masses can be benign. However, size should arguably be considered an important consideration in the management of cystic renal lesions, as small renal lesions are more indolent than large renal lesions, just as cystic lesions are more indolent than solid lesions [21, 25, 62–67]. Small renal lesions smaller than 1.5 cm are overwhelmingly likely to be benign (excluding patients with a demographic/genetic predisposition to cancer) [68]. Incidental detection of a benign-appearing very small renal cystic mass in a patient with no risk factors for malignancy can be presumed benign and does not warrant further characterization [4].
Biopsy
Although some studies have suggested that biopsy of cystic renal masses is helpful in distinguishing benign from malignant etiologies [15], in general it is not a high-yield technique, secondary to the paucity of cells within cystic renal masses that limits a definitive sample and therefore, limits the likelihood of a definitive diagnosis from pathology. Biopsy/drainage is useful for cystic renal masses that are suspected to be renal abscesses, and may be useful in patients who are poor surgical candidates, with the caveat that frequently the sample may be insufficient to give a definitive diagnosis [21, 25, 62–68].
Benign/benign-behaving Bosniak 2F, 3, and 4 lesions
There are benign/benign-behaving lesions that may fall into the Bosniak 2F, 3, or 4 category but which have imaging features that may allow for the accurate suggestion of benignity. The benign lesions that can be confidently diagnosed as benign include localized cystic disease, pyelocalyceal diverticula/milk of calcium cysts, and calcified partially thrombosed pseudoaneurysms. Also included are the benign lesions where imaging may heavily suggest a benign diagnosis; however, tissue is ultimately needed to confirm the diagnosis. These lesions include the renal abscess, cystic nephroma (CN), and mixed epithelial stromal tumor (MEST).
Localized cystic disease is a benign process which is unilateral in all patients, and characterized by multiple cysts of various sizes separated by normal or atrophic renal tissue in a conglomerate mass that can be suggestive of a cystic neoplasm. The key to diagnosis is the ability to find a single cyst within the conglomerate mass, which is surrounded by normal renal parenchyma (Fig. 2).
Pyelocalyceal diverticula are outpouchings of the renal collecting system that project into the renal cortex. These diverticula may contain stones, and should communicate with the collecting system (best depicted on excretory urographic phase images; Fig. 3).
Milk of calcium cysts are thought to arise from pyelocalyceal diverticula which have internal precipitations of calcium salts. Typically these cysts have lost communication with the adjacent collecting system. On imaging, the internal precipitation will layer, and often will have a horizontal sharp upper border, and will not enhance post-contrast (Fig. 4).
Although not a cystic renal mass, vascular etiologies should be considered in the diagnosis of a peripherally calcified renal cystic mass. When a peripherally calcified lesion is seen in the kidney, either Doppler ultrasound imaging or arterial phase CT or MR imaging should be performed to demonstrate internal signal/attenuation that follows the aortic signal/attenuation (Fig. 5).
Renal abscesses typically have a thickened peripheral rim with perilesional edema within the kidney. There is frequently mild stranding in the perirenal fat adjacent to the renal abscess (Fig. 6). In the setting of a lesion with this appearance, correlation with patient’s clinical symptoms (flank pain, urine analysis, urine cultures), imaging follow-up and/or tissue aspiration may be considered.
Benign or benign-behaving renal neoplasms that cannot be confidently diagnosed on pre-operative imaging studies, and therefore may require surgical excision
Cystic Nephroma (CN) is a rare, non-familial tumor which has a bimodal age and sex distribution. In the pediatric population, it has a male predilection, whereas it affects middle-aged females in the adult population. CN herniates into the sinus and occasionally extends into the collecting system (Fig. 7).
A Mixed Epithelial Stromal Tumor (MEST) is currently thought to be a lesion on the same spectrum as the CN, with the vast majority of these lesions in middle-aged women, also occasionally demonstrating “herniation” in the collecting system [69, 70]. CN has a greater proportion of fluid and cysts within them, while MEST has a greater ovarian stromal component [71] (Fig. 8). Some pathologists have recommended use of the term renal epithelial and stromal tumor to refer to both CN and MEST [72].
The multilocular cystic renal cell carcinoma (MLCRCC) is a low-grade neoplasm of excellent prognosis. This lesion has a male predominance, with a male–female ratio of 3:1 [73]. Some pathologists suspect it is essentially benign as there are no cases of progression or metastases in reported series [26]. This lesion can range in appearance from a Bosniak 2F to a Bosniak 4 lesion, and it resembles a CN on gross pathology. It lacks solid nodules of carcinoma histologically. It is important to emphasize that there is no classic imaging feature that can suggest this benign-behaving neoplasm prior to surgical excision, and other malignant lesions (such as the cystic clear cell RCC) can have an identical appearance, therefore it is still considered a surgical lesion (Fig. 9).
Malignant Bosniak 2F, 3, and 4 lesions
Malignant cystic RCCs are all rare compared with solid RCCs. These malignant cystic lesions include cystic clear cell carcinoma, the clear cell (tubulo) papillary RCC, tubulocystic carcinomas, and the benign-behaving MLCRCC.
Cystic cell carcinoma is a cystic mass with an irregularly thickened wall with large areas of solid nodularity within the wall. The demographic for this cystic tumor is identical to that of the clear cell solid RCC, with a male predominance (male:female ratio of 2:1), predominantly occurring in the sixth–seventh decades [74]. These cancers show extensive cystic change not resulting from necrosis, and are usually multiloculated. When there is no necrosis (based on careful analysis by the pathologist), these neoplasms are typically cured with resection [75] (Fig. 9).
The clear cell (tubulo) papillary RCC is composed of clear cells of low nuclear grade, with variable papillary tubular/acinar and cystic architecture. This tumor has no sex predilection, occurs at a mean age of 61 years, and usually presents at a low stage with indolent behavior and no metastases reported [76, 77].
Tubulocystic carcinoma is a mixture of tubules with micro- and macrocysts with low-grade nuclear features lined by a single layer of cuboidal or columnar cells with distinct nuclei that have a hobnail appearance. This lesion is also termed low-grade collecting duct carcinoma and Bellini duct carcinoma; this occurs mostly in men (85% male, 15% female) with a mean age of 54 years. The prognosis is excellent, with rare metastases [77, 78].
Multilocular cystic renal cell carcinoma
This is a benign-behaving neoplasm (also termed a neoplasm of low-malignant potential), which is almost entirely cystic, with the septa between the cystic components containing small clusters of clear cells without solid expansile nodules of clear cell carcinoma [79]. This lesion has a variable imaging appearance, ranging from a Bosniak 2F lesion to a Bosniak 4 lesion, with the Bosniak category corresponding to the degree of vascularized fibrosis within the lesion [26] (Fig. 9).
Solid renal neoplasms mimicking cystic renal cell carcinomas
Solid RCCs may mimic a cystic RCC; this either occurs secondary to a nearly absent internal enhancement in a hypovascular solid papillary RCC or an extensively necrotic solid RCC with a thickened rind of residual non-necrotic tumor [22]. Necrosis in a solid lesion can be, and has been, mistaken for an intrinsically cystic lesion (Fig. 10). In the Smith et al. article investigating the outcomes of cystic renal masses, 1 of the lesions prospectively read as a Bosniak 3 lesion (out of 113 total Bosniak 3 lesions) was a sarcomatoid RCC (presumably extensively necrotic), and while the patient had a history of a surgically resected solid papillary tumor, presumably the subsequent rapid tumor progression of the category 3 lesion and associated pulmonary metastases were secondary to this sarcomatoid tumor [18]. Similarly, in the same paper, a lesion prospectively classified as a Bosniak 4 lesion was a necrotic solid papillary RCC on pathology, and that patient eventually died of metastases from this lesion. The problem is, therefore, that solid necrotic tumors can be mistaken for cystic benign-behaving renal neoplasms on imaging. Solid papillary RCC without internal necrosis has been mistaken for a cystic lesion on imaging. This is because papillary carcinomas may have a partially cystic arrangement with papillae that variably fill a cystic space. For solid papillary renal lesions with a low density of papillae, the lesion will appear more cystic on pathology. Additionally, the solid variant of papillary RCC, composed of cells in tightly packed tubules can also mimic a cystic lesion on imaging, depending on the density of internal tissue [26, 80, 81]. It is also known that papillary RCCs are commonly hypovascular on imaging (such that they may not demonstrate internal contrast uptake to reach the threshold needed to suggest true enhancement within a lesion, i.e., typically an increase by ≥20 HU between pre and post-contrast CT, or solid internal enhancement on subtraction MR images; Fig. 11). In this way, these lesions may mimic a cystic non-enhancing renal lesion on imaging [82, 83]. Therefore, an overlap exists in imaging appearance between truly cystic lesions on histopathology (e.g., cystic clear cell RCC, MLCRCC, complicated hemorrhagic cysts, infected cysts) and solid papillary hypovascular tumors. Huber et al. suggested that a cystic appearance on imaging, regardless of the true pathology (i.e., cystic or solid) is associated with a lower-malignant potential in these lesions [2].
Of course, these articles assume that a necrotic solid aggressive tumor is not placed into this category of cystic renal mass. Several articles offer guides to accurately diagnosing necrosis in a solid tumor and in better predicting true cystic pathology from cystic imaging appearance [2, 33]. For example, necrosis is typically centrally located in larger renal mass lesions. If a lesion with a thickened solid peripheral rind is seen, with non-enhancement centrally (Fig. 10), then necrosis in a solid tumor should be favored, and this lesion should not be categorized with the Bosniak classification as a Bosniak 4 lesion, but instead termed a solid necrotic mass [26, 80–84].
Demographics with increased risk
Several recent studies have described demographic features that are associated with an increased risk for malignancy in cystic renal lesions [85]. Smith et al. found an increased risk of malignancy in Bosniak categories 2F and 3 lesions in patients with a history of a primary renal malignancy, with a coexisting Bosniak category 4 cystic renal lesion or a solid renal mass (or both), and with multiple Bosniak category 3 renal lesions [19]. Similarly, we reported a trend toward increased risk for malignancy in Bosniak category 2F cysts in men more than 50 years old with a prior solid RCC [16]. Therefore, on the basis of these studies, in men over 50 years old with a history of a prior RCC (cystic or solid), the risk of malignancy in a cystic renal lesion appears to be increased relative to that of the general population. Larger studies of this subgroup of patients need to be performed to confirm this association.
Management recommendations
Recent review articles have outlined reasonable approaches to the management of both solid and cystic renal masses [4, 65, 86]. In sum, these recommendations generally follow the Bosniak categorization, with surgery recommended for Bosniak 3 and 4 lesions, and follow-up surveillance for Bosniak 2F lesions. Malignant cystic renal lesions are traditionally managed surgically (with partial nephrectomy as opposed to radical nephrectomy now considered the standard of care). However, there is an interest in more conservative management for these lesions in selected cases. Malignancy rates in Bosniak 2F, 3, and 4 lesions range from around 5% for Bosniak 2F lesions (lowest reported percentage in the literature) up to 100% for Bosniak 4 lesions. Some investigators are challenging whether, even in the case of true malignancy, cystic renal mass lesions are optimally treated by surgical removal. Data supporting this include reports that cystic RCCs have lower malignant potential than solid RCCs [16, 17, 20, 21], as long as extensively necrotic solid RCCs are not mistaken for cystic renal lesions [22]. The reports that show that cystic renal lesions are benign-behaving rely on the accurate diagnosis of these lesions as cystic on both imaging and on pathology (e.g., Bosniak 3 and 4 lesions that on surgical resection prove to be MLCRCC, cystic clear cell RCC, or cystic papillary RCC). These favorable prognostic reports do not account for highly aggressive solid necrotic lesions that are mistakenly rarely placed into the “cystic” category [18].
Size is becoming a factor in management, with some recommendations now more liberally allowing for the incidentally (in an otherwise healthy individual) very small cystic renal lesion (less than 2 or 1.5 cm in size, depending on the paper) which is benign-appearing (within limitations of the imaging modality) to be definitively called a simple cyst and be ignored [14, 68]. Surveillance imaging is cautiously being used even for solid tumors (mean size 7.1 cm in the Mues et al. series) in selected (elderly patients with comorbidities) patient populations, with most patients not progressing to metastases even in these high-risk large tumors (progression to metastatic disease seen in 2/36 patients (5.6%)) [14, 87, 88]. If extrapolated to cystic renal masses, which are more indolent than solid tumors, then selected patients with Bosniak 3 and 4 lesions are candidates for surveillance imaging. Almost all series to date report the absence of recurrence or metastases after surgical resection of Bosniak 2F and 3 lesions, with favorable outcomes after surgical resection of Bosniak 4 lesions [16, 19, 89–91]. It will require further study to see if observation of these lesions will prove safe.
The role of ablation in the treatment of cystic renal masses has not yet been delineated. Smith et al. has suggested that there are less complications and lower cost associated with cystic renal mass ablation, as opposed to surgery [18]. However, ablation is only selectively utilized for cystic renal masses, depending on the size and location of the cystic lesion [92, 93].
Summary
In conclusion, cystic renal masses are relatively common in daily practice. The Bosniak classification is a time-proven method for the imaging classification and management of these lesions. Knowledge of the pathognomonic features of certain benign Bosniak 2F/3 lesions is important to avoid surgery on these lesions (e.g., localized cystic disease, renal abscess). For traditionally surgical Bosniak lesions (Bosniak categories 3 and 4), there are evolving data that risk stratification based on patient demographics, imaging size, and appearance may allow for expanded management options, including tailored surveillance ablation, along with the traditional surgical approach.
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Nicole M. Hindman has no funding nor any conflicts of interest to declare.
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Hindman, N.M. Cystic renal masses. Abdom Radiol 41, 1020–1034 (2016). https://doi.org/10.1007/s00261-016-0761-4
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DOI: https://doi.org/10.1007/s00261-016-0761-4