August 2013, VOLUME 201
NUMBER 2

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August 2013, Volume 201, Number 2

Genitourinary Imaging

Original Research

Cystic Renal Cell Carcinomas: Do They Grow, Metastasize, or Recur?

+ Affiliations:
1 Joint Department of Medical Imaging, University Health Network–Mount Sinai Hospital and Women's College Hospital, University of Toronto, 3-957, 610 University Ave, Toronto, ON M5G 2M9, Canada.

2 Division of Abdominal Imaging and Interventional Radiology, Massachusetts General Hospital, Harvard Medical School, Boston, MA.

3 Department of Pathology, University Health Network, University of Toronto, Toronto, ON, Canada.

4 Division of Urology, Department of Surgical Oncology, University Health Network–Princess Margaret Hospital, University of Toronto, Toronto, ON, Canada.

Citation: American Journal of Roentgenology. 2013;201: W292-W296. 10.2214/AJR.12.9414

ABSTRACT
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OBJECTIVE. The purpose of this study is to evaluate the interval growth, tumor recurrence, and metastatic disease occurrence of cystic renal cell carcinoma (RCC).

MATERIALS AND METHODS. Pre-and posttreatment imaging of 47 histologically proven cystic RCCs, with at least 6 months of pretreatment imaging monitoring or at least 2 years of posttreatment imaging follow-up, or both, was retrospectively reviewed. Tumor morphologic features, preoperative growth, histologic typing and grading, and the incidence of tumor recurrence or metastasis were evaluated. Growth rate of tumors were compared among various histologic subtypes and Fuhrman grades.

RESULTS. Of 47 tumors, 27 (57.5%) were clear cell RCCs, 12 (25.5%) were multilocular RCCs, and eight (17%) were papillary cystic RCCs. Overall, 26 (55.3%) tumors were graded as Fuhrman grade 2, 17 (36.1%) were Fuhrman grade 1, and one tumor was Fuhrman grade 3. Of the 26 tumors with a minimum of 6 months of pretreatment imaging monitoring, 19 (73%) did not show a significant increase in tumor size. The differences in mean growth among the Fuhrman grades and different subtypes were not statistically significant. The average duration of posttreatment follow-up was 51 months. There were no local recurrences among the 43 patients who underwent posttreatment imaging, except for one patient who had metastasis at preoperative clinical presentation.

CONCLUSION. Cystic RCCs exhibit slow indolent growth, if any, and show no significant metastatic or recurrence potential, with excellent clinical outcomes. We raise the need for revisiting current imaging protocols that may involve frequent pre-and posttreatment imaging in cystic RCCs.

Keywords: CT, cystic renal cell carcinoma, growth patterns, imaging, MRI

Renal cell carcinoma (RCC) accounts for 3–5% of cancers [1, 2]. Imaging plays a key role in the diagnosis, staging, and follow-up of RCCs. There is growing interest in better characterization of renal tumors preoperatively. This would be important for treatment individualization based on the tumor profile. Cystic RCCs can represent up to 3–14% of all RCCs and comprise a wide category of renal cancers, including multilocular cystic RCCs, unilocular cystic RCCs, RCCs with extensive cystic necrosis, and unilocular cysts with mural tumor nodules [3, 4]. Among these subtypes, multilocular cystic RCC has been shown to be a low-grade neoplasm with an excellent prognosis compared with other subtypes of RCC, both cystic and solid [5]. The 2004 World Health Organization classification of kidney tumors recognizes multilocular cystic RCCs as a variant of clear cell RCC [6, 7]. Because cystic RCCs occur infrequently, the natural history, clinical outcomes, optimal treatment strategy, and prognosis for this type of renal malignancy remain controversial. Minimally invasive procedures have been recommended in small retrospective studies [8]; however, there is no consensus about the overall course of these malignancies and the proper management strategy of each subtype. The aim of our study was to evaluate interval growth, tumor recurrence, and metastatic disease occurrence in patients with cystic RCC.

Materials and Methods
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Patient Population

This was a retrospective single-center longitudinal study undertaken in compliance with HIPAA. Institutional review board approval was obtained for this study, and the need for informed patient consent was waived. We retrospectively reviewed our institutional database to identify patients with cystic renal tumor or “Bosniak cyst III or IV” between 2000 and 2010. Pathologic reports of these patients were reviewed, and patients with histologic diagnosis of cystic renal cancer (either by core biopsy or surgical histopathologic analysis) were identified. After reviewing the radiologic reports, we included in the study patients who had undergone at least 6 months of pretreatment imaging monitoring or at least 2 years of posttreatment imaging follow-up, or both.

Imaging

All available imaging for these tumors was retrieved from the institutional radiology archival system, including 172 CT, 150 ultrasound, and 75 MRI examinations. CT examinations were performed on 4-MDCT (Light-Speed QX/I, GE Healthcare), 8-MDCT (LightSpeed Ultra, GE Healthcare), or 64-MDCT (Aquilion, Toshiba Medical Systems) units, using a standard triphasic renal CT protocol that included an unenhanced arterial phase at 30 seconds and a venous phase at 100 seconds (5mm slice thickness and 2.5-mm reconstruction interval). All patients were administered IV contrast agent, which included a nonionic contrast medium, either 2 mL/kg of iohexol (Omnipaque 300, Amersham Health) or iodixanol (Visipaque 270, GE Healthcare), to a maximum of 200 mL. Injection flow rate was 5 mL/s into an antecubital vein. All MRI examinations were performed on a 1.5-T system (Genesis Sigma and Sigma Excite, GE Healthcare) using a phased-array coil and requisite renal MRI protocol that included T2-weighted localizer sequences, followed by T2-weighted axial and coronal fast spin-echo, T1-weighted in and opposed phase gradient-echo, unenhanced, and contrast-enhanced fatsaturated 3D T1-weighted gradient-echo pulse sequences. IV gadolinium-based contrast agent (gadodiamide; Omniscan, GE Healthcare) was injected with a pressure injector at flow rate of 2 mL/s and dose of 0.1 mmol/kg body weight. Sonography was performed using Acuson Sequoia (Siemens Healthcare), iU22 (Philips Healthcare), HDI5000 (ATL), or Aplio80 (Toshiba) units with a 2–5-MHz curvilinear probe. All patients underwent CT (n = 34) or MRI (n = 13), or both, in addition to ultrasound. Imaging studies were reviewed independently initially by two abdominal radiologists who were blinded to final histopathologic diagnoses. A consensus read between the two readers was later reached for each of the 47 tumors, and no significant interobserver discrepancies were present.

Image Analysis

Any well-defined focal renal lesion with predominantly low attenuation (≤ 20 HU) in the unenhanced phase on CT or that was diffusely or predominantly T1 hypointense and T2 hyperintense on MRI with no contrast enhancement was defined as a “cyst.” On ultrasound, cysts were defined as predominantly anechoic lesions with posterior acoustic enhancement. On CT, if the lesion was predominantly cystic with areas of high attenuation (20–70 HU), it was considered proteinaceous or hemorrhagic. In cysts with solid components, only those for which less than 25% of the total volume was solid were included, and the lesion was called “solid cystic” [6, 9]. Enhancement pattern was also evaluated both on CT and MRI. On CT, an incremental attenuation of greater than 15 HU was considered to be positive. On MRI, unenhanced and contrast-enhanced T1-weighted subtraction sequences were analyzed.

Histopathologic Examination

The histopathology report was reviewed for each patient, and pathologic typing and Fuhrman grading of the tumors were evaluated.

Clinical and Demographic Data

Relevant data, including age, sex, and underlying syndromes (e.g., von Hippel-Lindau syndrome), were recorded. All available outcomes and follow-up imaging were examined until a minimum period of at least 2 years after treatment. Any clinical, pathologic, or imaging evidence of recurrence or metastases over the follow-up period was also recorded.

Statistical Analysis

Statistical analysis was performed to compare the growth rate of tumors for various histologic subtypes of cystic RCC as well as for different Fuhrman grades, as determined by pathologic assessment, using the Kruskal-Wallis test. Analysis was done using the statistical software SPSS (version 20, SPSS), and a p value of less than 0.05 was considered as statistically significant.

Results
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Initially, 307 patients with cystic renal tumor or cancer were retrieved. After review of the radiologic database, 47 patients (30 men and 17 women; mean age, 58.25 years) were included in the study. Two patients with a history of von Hippel–Lindau syndrome had multiple tumors, and the largest and most complicated cyst was considered for the purpose of our study. Of the 47 patients, 43 (91.5%) had undergone both pre- and posttreatment CT or MRI, whereas four had undergone only preoperative imaging. The mean duration of follow-up was 51 months (range, 24–120 months).

Tumor Morphologic Features

Twenty-four (51.1%) patients had left-sided tumors, 20 (42.6%) patients had right-sided tumors, two (4.3%) patients had bilateral tumors, and one (2.2%) patient had a tumor in a right lower quadrant renal allograft. Of the 47 tumors, 14 (29.8%) were classified as Bosniak category III, followed closely by Bosniak categories IIF and IV (13 [27.7%] tumors each). The largest mean axial dimension at presentation was 46 mm, and the thickest septum was 7 mm. Calcification was noted in 16 (34%) tumors. Among the patients who received contrast agent, 14 (29.8%) had tumors that revealed nodular enhancement after administration of contrast agent, whereas 31 (66%) had tumors that showed only septal enhancement. Hemorrhagic or hyperdense cysts were reported in nine (19.1%) cases. In terms of tumoral spread, one patient had (2.2%) aortocaval lymphadenopathy and one patient (2.2%) had metastasis at the time of presentation. No vascular invasion or thrombosis was noted in the present cohort.

Tumor Pathologic Profiles

Surgical histopathology reports were present for 44 tumors, whereas for three tumors, core biopsy was performed, followed by radiofrequency ablation for conservative nonsurgical management. The tumors included 27 (57.5%) clear cell cystic RCCs, 12 (25.5%) multilocular RCCs, and eight (17%) papillary cystic RCCs. In the remaining two cases, the pathology report was suggestive of clear cell cystic RCC versus multilocular or benign epithelial lesion. Twenty-six tumors were Fuhrman grade 2, 17 were Fuhrman grade 1, and one tumor was Fuhrman grade 3, as confirmed by histopathologic analysis. Three tumors were not assigned a Fuhrman grade in the final pathology report.

Preoperative Growth

In 26 cases, preoperative cross-sectional imaging for at least 6 months before treatment was available. When an increase in the single largest axial dimension of at least 20% was regarded as significant, only seven (26.9%) tumors showed growth (range, 6–100%) (Fig. 1). The average increase in dimension was 10.5 mm (range, 0–24 mm) with a mean increase of 46%. Most of the tumors (73.1%) did not show a significant increase in size (Fig. 2). The difference in median growth between the three histologic subtypes was not statistically significant (p = 0.738) (Table 1). In addition, this difference was not statistically significant when we compared the two groups of Fuhrman grades (grade 1 vs grade 2) (p = 0.424).

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Fig. 1A —45-year-old man with slow-growing cystic renal cell carcinoma.

A, Axial contrast-enhanced CT shows left renal mid polar complex cystic 5.45-cm lesion (arrow).

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Fig. 1B —45-year-old man with slow-growing cystic renal cell carcinoma.

B, On CT obtained 5 years later, lesion (arrow) shows mild growth (< 20%).

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Fig. 2A —57-year-old woman with cystic renal cell carcinoma who declined surgical resection, opting instead for close surveillance. No growth was seen in cystic renal cell carcinoma over 8-year period.

A, Axial contrast-enhanced CT shows left renal mid polar complex cystic lesion at initial presentation.

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Fig. 2B —57-year-old woman with cystic renal cell carcinoma who declined surgical resection, opting instead for close surveillance. No growth was seen in cystic renal cell carcinoma over 8-year period.

B, Axial CT shows postbiopsy dimension 1 year later.

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Fig. 2C —57-year-old woman with cystic renal cell carcinoma who declined surgical resection, opting instead for close surveillance. No growth was seen in cystic renal cell carcinoma over 8-year period.

C, Follow-up appearance at 8 years shows no growth compared with baseline.

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Fig. 2D —57-year-old woman with cystic renal cell carcinoma who declined surgical resection, opting instead for close surveillance. No growth was seen in cystic renal cell carcinoma over 8-year period.

D, Histologic examination (H and E, ×100) shows multilocular cystic lesion. Cyst walls are lined by single layer of attenuated cuboidal epithelial cells with clear cytoplasm. Focally, septa between cysts contain proliferations of low-grade malignant epithelial cells with clear cytoplasm accompanied by delicate microvascular network.

TABLE 1: Descriptive Statistics of Renal Tumor Growth, by Histologic Group
Postoperative Metastases or Recurrence

Twenty-two patients (46.8%) underwent partial nephrectomy, 22 patients (46.8%) had radical nephrectomy, and three patients (6.4%) were treated with radiofrequency ablation. Forty-three patients had posttreatment imaging follow-up over the course of 2 years or more, with an average follow-up duration of 51 months (range, 24–120 months). No clinical, imaging, or pathologic evidence of tumor recurrence was reported. No metastases were detected in any of the patients in the follow-up period after treatment. One patient had metastases (hepatic, nodal, and pulmonary) at the time of clinical presentation and died within 6 months of surgery.

Discussion
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With wider application of advanced imaging techniques, small incidental renal cysts needing further categorization are being increasingly detected in the adult population, with approximately half of patients older than 50 years having renal cysts [10]. The Bosniak system is widely followed for imaging classification of renal cysts, leading to further imaging and management protocols. Category I and II cysts do not warrant any further imaging follow-up [10]. Category IIF cysts are slightly more complicated than category II cysts, and some period of observation is recommended for these, through CT or MRI, to suggest benignity [11, 12]. Category III cysts are reported to have a variable prevalence of malignancy, 31–100% [13, 14], and are considered “surgical lesions” because of the probability of being malignant. Bosniak category IV cysts are renal cancers unless proven otherwise [12]. Bosniak recommended that, in otherwise healthy individuals, all lesions (cystic and solid) 1.0 cm or larger should be evaluated [15].

Cystic RCCs represent a mix of various pathologic entities, some of which are well classified (e.g., multilocular cystic RCCs), whereas others are cystic subtypes of common renal neoplasms. Up to 15% of clear cell RCCs may either have cysts as a dominant component or may arise within a cyst. Papillary cystic RCC can present as a large cyst containing hemorrhagic fluid or necrotic material surrounded by a thick pseudocapsule. Angiomyolipoma or oncocytoma may also have prominent cysts. In addition, uncommon renal neoplasms, such as cystic nephroma, stromal tumor, tubulocystic carcinoma, synovial sarcoma, and acquired cystic disease-associated RCC, may also have associated cysts [4]. The cystic appearance of RCCs may be due to intrinsic unilocular or multiloculated growth, cystic necrosis, or origin from the epithelial lining of a preexisting simple cyst [16].

Although Bosniak classification is helpful in determining malignant risk and required follow-up or treatment of lesions with cystic components, there is no guideline regarding imaging cystic renal neoplasms before or after treatment. Institutional protocols regarding imaging and follow-up of cystic RCCs vary greatly depending on local expertise and cumulative experience. However, no guidelines or management protocols are available for the treatment of the cystic RCCs. Accordingly, the current management and postsurgical surveillance protocols that are used typically for cystic RCCs are similar to those for their solid counterparts. However, various studies have described better clinical outcomes and survival rates for cystic RCCs. It has been shown that patients with cystic clear cell RCC are less likely to present with symptoms, have smaller tumors, and are well responsive to less-aggressive treatment strategies [17].

In our study of 26 tumors that were monitored with at least 6 months of pretreatment imaging, no significant tumor enlargement was noted in most cases, implying a probable indolent course of the disease. In addition, the 43 patients with at least 2 years of posttreatment imaging follow-up did not show evidence of recurrences or metastases, conferring 100% disease-free survival during the follow-up period. This finding is in agreement with those of previous reports on cystic RCCs. However, one patient in our series died within 6 months after presenting with nodal and pulmonary metastases from an aggressive hemorrhagic necrotic cystic papillary RCC. Many reasons can be postulated for improved clinical outcomes in this subset of RCCs.

Features of local invasiveness (e.g., perinephric fat invasion, microscopic vascular invasion, lymph node involvement, peritumoral invasion into healthy renal parenchyma, and distant metastasis at the time of diagnosis) are not commonly seen in cystic RCCs, conferring a favorable prognosis [18]. In our series, one patient (2.2%) had nodal metastasis (aortocaval lymphadenopathy), but no vascular invasion was noted. This provides further evidence for better prognostic profile of cystic RCCs.

The Fuhrman nuclear grade is considered an important prognostic predictor in RCC [7, 19]. Suzigan et al. [16] hypothesized that favorable outcome for cystic RCCs may be attributable to fewer malignant cells proliferating at a slower rate and to the majority of these tumors being Fuhrman grade 1 or 2. Han et al. [6] found in their series that 72% of cystic RCCs were low grade (Fuhrman 1 or 2), compared with the conventional RCCs. Accordingly, in our cohort of patients, 97% of tumors were low grade; 27 tumors (57.5%) were Fuhrman grade 2 and 17 (36.1%) were Fuhrman grade 1. Interestingly, Fuhrman grade 4 was not reported in our series. This implies a less-aggressive nature of cystic RCC tumor; however, there was no significant difference in patients with Fuhrman grade 1 tumors compared with patients with Fuhrman grade 2 tumors in terms of preoperative growth rate and survival.

At present, the use of nephron-sparing surgery is the established treatment for T1a tumors (< 4 cm) and an emerging standard treatment for T1b tumors (4–7 cm), provided that the tumor can be completely removed [20]. The choice of treatment for patients with localized RCC needs to be individualized. The key point is preservation of renal function without compromising the oncologic outcome. The small size of cystic RCCs, along with the lower nuclear grade of these tumors, has raised the possibility of considering nephronsparing surgery for these subtypes [5], particularly in multilocular cystic RCC, which seems to be one end of the spectrum of cystic RCCs composed exclusively of cysts with an excellent outcome. In our series, most of the patients underwent partial nephrectomy (46.8%), and we found excellent outcomes over 51 months of follow-up, similar to the findings from a previously reported study [21]. We propose that nephron-sparing procedures for patients with cystic RCC could be a viable option. The 100% survival of our patients (excluding the case with initial presentation with metastatic disease) was in agreement with a study by Koga et al. [22], who found a 5-year survival rate of 80–100% for these tumors, significantly better than the 55% for conventional solid RCCs. In addition, Onishi et al. [18] reported 27 cases of cyst-associated RCC in which there were only three deaths, with an overall 5-year survival rate of 88.6%, compared with 50–60% of conventional RCCs.

A recent study by Hindman et al. [23] has evaluated the correlation of the imaging and pathologic features of multilocular cystic RCC. Those authors found that higher Bosniak category corresponds to an increase in the volume of malignant cells lining the tumor and an increase in the presence of vascularized fibrous tissue. Clinical follow-up showed no evidence of recurrent or metastatic disease in these patients. Findings of long-term outcomes in that study are in line with the findings in our cohort of patients; however, the correlation between Bosniak category and pathologic feature was not evaluated in our patients.

Our study has some limitations. It is a retrospective study with a small group of patients and has an inclusion bias. We also do not have a significant number of Fuhrman grade 3 and 4 tumors, which may explain better outcomes in this group. It should also be noted that we did not compare the outcomes of our series with that of the stage-matched solid subtype RCC, and one may favor the predictive role of staging rather than the natural course of cystic RCC. However, because our institution is a large tertiary oncology referral site and the patient selection was consecutive over a decade, the results might be more reflective of the actual tumor biology of cystic RCCs, rather than reflecting a selection bias. We also have not performed a cost-benefit analysis, but, to our knowledge, ours is the largest imaging-based single-center series of cystic renal neoplasms. It also should be noted that, in this study, we considered a lesion as enhancing when the Hounsfield unit value was more than 15 HU on CT, which includes lesions in the 15-to 20-HU zone, which many radiologists still consider to be pseudoenhancement.

In conclusion, cystic RCCs mostly presented as low-stage or low-grade tumors, with good prognosis and a good clinical outcome in our series. Most tumors did not show significant presurgical increase in size, and none showed postsurgical recurrence or metastasis. Regarding growth and metastatic and recurrence potential, cystic renal cancers seem to be a distinct subset of RCC, with many differences from the conventional solid subtypes. They show excellent clinical outcomes, and it might be prudent to not image them as frequently, pre-or postoperatively, as is routinely done. This may also help reduce the cumulative radiation burden on patients and optimize health resource allocation.

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Address correspondence to K. Jhaveri.

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