Ultrasonographic Features of Renal Oncocytoma with Histopathologic Correlation Li Lou, PhD,1 Jianbo Teng, MD,1 Xiaoyan Lin, PhD,2 Hui Zhang, PhD3 1

Department of Ultrasound, Shandong Medical Imaging Research Institute, Shandong University, Jinan, 250021, P.R. China 2 Department of Histopathology, Shandong Provincial Hospital, Shandong University, Jinan, 250021, P.R. China 3 Department of Urology, Shandong Provincial Hospital, Shandong University, Jinan, 250021, P.R. China Received 27 March 2013; accepted 5 December 2013

ABSTRACT: Background. To analyze the sonographic (US) features of renal oncocytoma and correlate them with histopathologic findings. Methods. The medical records of 12 patients with a histologic diagnosis of renal oncocytomas were reviewed. The location, size, shape, margin, echogenicity, homogeneity, and blood flow distribution of the lesions were analyzed, and the US features were compared with histopathologic findings. Results. Oncocytomas appeared as solid, solitary, well-marginated, unencapsulated, fairly homogeneous renal cortical masses (n 5 10), with regular shape, relatively isoechoic (n 5 5) or slightly hyperechoic (n 5 7) to the adjacent renal parenchyma, and an exophytic growth pattern was exhibited in most cases (n 5 9). Two larger masses (9 cm) demonstrated a central stellate scar and a characteristic of spokewheel vascular pattern. The tumors with a low percentage of stroma (20%) were slightly hyperechoic. Conclusions. Although the US features are not pathognomonic, their presence should alert to the possible C 2014 Wiley Periodidiagnosis of renal oncocytoma. V cals, Inc. J Clin Ultrasound 42:129–133, 2014; Published online in Wiley Online Library (wileyonlinelibrary.com). DOI: 10.1002/jcu.22128 Keywords: ultrasonography; renal oncocytoma; renal; neoplasms

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enal oncocytoma is a rare benign renal cell neoplasm, which accounts for approximately 5% of all adult primary renal epithelial neoCorrespondence to: L. Lou C 2014 Wiley Periodicals, Inc. V

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plasms in surgical series.1 Unlike renal cell carcinoma, oncocytoma is not associated with vascular invasion, local recurrence after surgery, or distant metastases. Preoperative diagnosis would be valuable as the oncocytoma is treated through local resection or heminephrectomy and requires no chemotherapy after surgery. Several studies have evaluated the features of renal oncocytoma on CT, angiography, and MRI.1–5 To our knowledge, little emphasis has been placed on the ultrasound (US) features of oncocytoma,6,7 and correlation between US features and pathologic findings has not been reported. US is usually the firstline diagnostic examination used for patients with abdominal conditions. US is also a means for the detection of asymptomatic renal oncocytoma during physical examination. In the present study, we evaluate the US features of 12 histologically confirmed renal oncocytomas and correlate them with histopathologic findings.

MATERIALS AND METHODS

The medical records of all patients between 2008 and 2012 with a histologic diagnosis of renal oncocytoma were reviewed at our institution. Twelve cases diagnosed as oncocytomas according to World Health Organization 2004 criteria were included. Medical records, sonograms, and histopathological slides were retrospectively reviewed for each patient. Institutional Review Board approval was obtained. A waiver of informed consent was granted for this retrospective study. 129

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US was performed preoperatively with various scanners (GE LOGIQ 9; GE Healthcare, Milwaukee, WI; and Aloka ProSound Alpha10; Aloka, Tokyo, Japan), using 3.5- to 5-MHz convex array transducers. Color Doppler US was performed with optimized color Doppler parameters. Two sonographers who specialized in genitourinary US with knowledge of the diagnosis evaluated the US findings by means of consensus. The US appearances were evaluated for features such as tumor site, size, shape, margin, echogenicity, homogeneity, and presence of central scar. Color Doppler imaging was evaluated for the presence of a spoke-wheel pattern of vessels extending into the tumor from the periphery, and the location (internal or peripheral) of the vessels was recorded. All histologic and cytologic slides of these patients were retrieved and reviewed by the pathologist without knowledge of the US findings. Histopathologic specimens were reviewed to confirm the diagnosis of oncocytoma. The percentage by volume of extracellular stroma was calculated in each tumor mass. Each case was correlated with US features with histopathologic findings.

RESULTS

There were 12 patients (five men and seven women, age range 30–63 years, mean age 57 years) with 12 histologically proven renal oncocytomas. The lesions were found incidentally during US evaluation for an unrelated condition in nine patients, for flank pain in two patients, and for macroscopic hematuria in one patient. Seven masses were found in the right kidney and five in the left kidney. All cases were single and unilateral. Eight masses were found to involve the mid zone of the kidney; two were in the upper pole, and two were in the lower pole. Eight patients underwent partial nephrectomy; the remaining four patients underwent radical nephrectomy. All patients are free of evidence of venous invasion or distant spread on follow-up evaluation. Lesions ranged from 1.5 to 11 cm in diameter (mean, 5.4 cm). Of the 12 lesions, 5 were 3 cm in diameter or less, 5 were between 4 and 7 cm in diameter, and 2 were between 9 and 11 cm in diameter. All lesions showed smooth contours and distinct delineation from surrounding renal parenchyma. The smaller tumors were round, whereas the larger tumors tended to be ovoid. All were solid masses; five were relatively isoe130

FIGURE 1. A 37-year-old woman with oncocytoma of the right kidney. (A) Longitudinal sonogram shows a 4-cm, solid, well-defined, homogeneous mass, isoechoic to the adjacent renal parenchyma. (B) Photomicrograph (HES, 3100) shows low percentage of stroma correlated with isoechoic mass.

choic and seven were slightly hyperechoic to the adjacent renal parenchyma (Figure 1). None had cystic regions. Ten of 12 masses were homogeneous, and two demonstrated a central scar (Figure 2) but were otherwise homogeneous. Most of the masses located in the renal cortex and an exophytic growth pattern (Figure 3) was noted in nine cases. A stellate central scar was present in two larger masses (9 cm). On color Doppler US, the two masses demonstrated a spoke-wheel pattern (Figure 4), that is, the vessel branches extended from the periphery to the central portion of the mass and supplied the mass centripetally. Among the other 10 masses, 4 presented both internal and peripheral blood flow distribution, 3 presented only peripheral blood flow, while the remaining 3 presented no blood flow. JOURNAL OF CLINICAL ULTRASOUND

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FIGURE 2. A 47-year-old man with oncocytoma of the left kidney. (A) Sonogram shows a stellate central scar within an otherwise homogeneous mass, which measures 11 cm in diameter. Gross pathologic (B) and microscopic (C, HES, 3100) specimen demonstrates corresponding fibrotic scar in the center of the tumor.

On gross examination, the lesions were uniformly solid and tan-brown in color, without areas of necrosis or hemorrhage. Central fibrotic scars were identified grossly (Figure 2B) in three lesions, which were all larger than 7 cm VOL. 42, NO. 3, MARCH/APRIL 2014

FIGURE 3. A 40-year-old woman with oncocytoma of the left kidney. Both sonogram (A) and contrast-enhanced CT (B) show a 1.5-cm mass (black arrow) located in the renal cortex and exhibiting an exophytic growth pattern. (C) Photomicrograph (HES, 3200) shows a higher percentage of stroma correlated with slightly hyperechoic mass.

in diameter. Microscopically, all tumors were typically well-circumscribed masses, which compressed adjacent renal parenchyma and lacked a true capsule. The tumors were composed solely of oncocytes. The cells were arranged in nests or cords embedded in loose myxoid or 131

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FIGURE 4. A 31-year-old woman with oncocytoma of the left kidney. Color Doppler sonogram shows the characteristic spoke-wheel vascular pattern.

hyalinized stroma. Nuclear pleomorphism was present only focally in one case, but mitotic figures were not seen. Histopathological intratumoral contents were correlated with the lesion’s echogenicity. The tumors with a low percentage of stroma (20%) were slightly hyperechoic (Figure 3C). Neither perirenal fat invasion nor vascular invasion was detected in any case.

DISCUSSION

Renal oncocytomas originate from intercalated cells of the cortical collecting duct.8,9 They were reported as benign tumors with eosinophilic cytoplasm and abundant mitochondria.10 Most tumors occur sporadically in asymptomatic patients. They are usually single and unilateral, although 4–5% are bilateral and 13% are multifocal.11,12 Oncocytomas occur in both sexes at a similar rate, and most patients are over 50 years old at the time of presentation.1,2,11 Our series consists of five men and seven women with a mean age of 57 years. The clinical presentations of oncocytomas are variable according to their size and site. As oncocytomas usually involve the cortical portion of the collecting duct, they have a propensity for exophytic growth. The cortical origin and tendency for exophytic growth mean that oncocytomas rarely cause hydronephrosis and hematuria even when of large size, so the majority of 132

oncocytomas are incidental findings and present with nonspecific clinical symptoms. Oncocytomas can be incidentally found on US, CT, or MRI performed for other reasons. Patients frequently present with nonspecific abdominal symptoms such as pain, discomfort, or palpable mass. In our series, all 12 cases were detected and located accurately with US. Only four cases were diagnosed correctly prior to surgery. Preoperative diagnosis is difficult owing to the nonspecific presentation and the overlap of the imaging appearances of oncocytomas and other renal neoplasms. However, we found that some US features can point the radiologist to the diagnosis of oncocytoma. In this series, oncocytomas appeared as solid, solitary, well-demarcated, unencapsulated, fairly homogeneous renal cortical tumors, with regular shape (round, or ovoid), relatively isoechoic (5/12) or slightly hyperechoic (7/12) to the adjacent renal parenchyma, and an exophytic growth pattern was exhibited in most cases (9/ 12). This was in concordance with previous reports.1,4,6,7 Their circumscribed appearance resulted from their compression by the surrounding renal parenchyma into a pseudocapsule, which with smooth contour and distinct interface with surrounding renal parenchyma. The presence of a stellate central scar is a characteristic feature of oncocytomas. It appears as a discrete branching hypoechoic area within an otherwise homogeneous mass on US. The central stellate scar corresponds pathologically to fibrous connective tissue. It is reported as one of the most important imaging findings that may suggest the diagnosis of oncocytoma by either CT or US.4 In our series, this scar was present only in the larger masses. In two masses that were 9 cm or more in diameter, the central scar was identified on both US and gross specimen; in one mass that was 7 cm in diameter, the central scar was identified pathologically, but not on US. Possibly as the mass enlarges, it may outgrow its blood supply with concomitant ischemia; eventually, the ischemic tumor is replaced by a fibrotic scar. Because the blood supply comes from the periphery to the central portion of the mass, the fibrotic scar is more likely to develop in the central region of the mass. Although the central scar is not specific,2,5 it is helpful when present and can aid the radiologist in narrowing the differential diagnosis. The homogeneous echogenicity is another useful distinguishing imaging feature of oncocytomas,1,4,7 which was seen in 10 of the 12 cases JOURNAL OF CLINICAL ULTRASOUND

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in our series, the remaining 2 demonstrating a central scar but being otherwise homogeneous. Homogeneity on US correlated with the absence of hemorrhage and necrosis at pathologic examination. Oncocytomas tended to be more often isoechoic than hyperechoic masses in previous studies.1,4,6,7 Our series consisted of five isoechoic and seven slightly hyperechoic masses, but this difference may be related to differences in the patient populations. We found that histopathological intratumoral structure was correlated with internal echo pattern. The tumors with a low percentage of stroma (20%) were slightly hyperechoic. Oncocytomas have a distinctive appearance on angiography, showing a characteristic of spoke-wheel vascular pattern, that is, the vessel branches extended from the periphery to the central portion of the mass.4 Angiography is no longer performed for renal tumors. However, color Doppler US can show the blood flow distribution of the oncocytomas. In our study, two larger masses (9 cm) demonstrated the characteristic spoke-wheel pattern; three masses presented no blood flow, and the other masses presented either internal and peripheral blood flow distribution (4/12) or only peripheral blood flow (3/12). This series also demonstrated that as the tumor increases, the blood supply is gradually increasing, suggesting that the blood flow increases with the tumor size. Our study was limited by its retrospective design and a small population, which could have created biases. However, these problems were unavoidable because of the rarity of oncocytomas. Despite these limitations, we believe that some US features can orientate the radiologist toward the diagnosis of oncocytoma and possibly prevent unnecessary nephrectomy. However, not all oncocytomas have such suggestive US features and the final diagnosis will be established at histopathologic evaluation.

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ACKNOWLEDGMENT This work was supported by grant 2013WS0183 from the Medical Science and Technology Development Program of Shandong Province. This work was supported by grant from the Natural Science Foundation of Shandong Province (ZR2011HL054).

REFERENCES 1. Prasad SR, Surabhi VR, Menias CO, et al. Benign renal neoplasms in adults: cross-sectional imaging findings. AJR Am J Roentgenol 2008;190:158. 2. Choudhary S, Rajesh A, Mayer NJ, et al. Renal oncocytoma: CT features cannot reliably distinguish oncocytoma from other renal neoplasms. Clin Radiol 2009;64:517. 3. Harmon WJ, King BF, Lieber MM. Renal oncocytoma: magnetic resonance imaging characteristics. J Urol 1996;155:863. 4. Quinn MJ, Hartman DS, Friedman AC, et al. Renal oncocytoma: new observations. Radiology 1984;153:49. 5. Davidson AJ, Hayes WS, Hartman DS, et al. Renal oncocytoma and carcinoma: failure of differentiation with CT. Radiology 1993;186:693. 6. Wu Y, Du LF, Li F, et al. Renal oncocytoma contrast-enhanced sonographic features. J Ultrasound Med 2013;32:441. 7. Goiney R, Goldenberg L, Cooperberg PL. Renal oncocytoma: sonographic analysis of 14 cases. AJR Am J Roentgenol 1984;143:1001. 8. Storkel S, Pannen B, Thoenes W, et al. Intercalated cells as a probable source for the development of renal oncocytoma. Virchows Arch B Cell Pathol Incl Mol Pathol 1988;56:185. 9. Prasad SR, Narra VR, Shah R, et al. Segmental disorders of the nephron: histopathological and imaging perspective. Br J Radiol 2007;80:593. 10. Lindgren V, Panner GP, Omeroglu A, et al. Cytogenetic analysis of a series of 13 renal oncocytomas. J Urol 2004;171:602. 11. Perez-Ordonez B, Hamed G, Campbell S, et al. Renal oncocytoma: a clinicopathologic study of 70 cases. Am J Surg Pathol 1997;21:871. 12. Villanueva PA, Roca EA, De Diego RE, et al. Bilateral multiple renal oncocytoma. Case report and review of the literature. Prog Urol 2007;17:997.

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Ultrasonographic features of renal oncocytoma with histopathologic correlation.

To analyze the sonographic (US) features of renal oncocytoma and correlate them with histopathologic findings...
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