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http://dx.doi.org/10.3348/kjr.2015.16.1.99

Imaging Findings of Common Benign Renal Tumors in the Era of Small Renal Masses: Differential Diagnosis from Small Renal Cell Carcinoma - Current Status and Future Perspectives  

Woo, Sungmin (Department of Radiology, Seoul National University College of Medicine)
Cho, Jeong Yeon (Department of Radiology, Seoul National University College of Medicine)
Publication Information
Korean Journal of Radiology / v.16, no.1, 2015 , pp. 99-113 More about this Journal
Abstract
The prevalence of small renal masses (SRM) has risen, paralleling the increased usage of cross-sectional imaging. A large proportion of these SRMs are not malignant, and do not require invasive treatment such as nephrectomy. Therefore, differentation between early renal cell carcinoma (RCC) and benign SRM is critical to achieve proper management. This article reviews the radiological features of benign SRMs, with focus on two of the most common benign entities, angiomyolipoma and oncocytoma, in terms of their common imaging findings and differential features from RCC. Furthermore, the role of percutaneous biopsy is discussed as imaging is yet imperfect, therefore necessitating biopsy in certain circumstances to confirm the benignity of SRMs.
Keywords
Small renal mass; Angiomyolipoma; Oncocytoma; Renal cell carcinoma;
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1 Silverman SG, Israel GM, Herts BR, Richie JP. Management of the incidental renal mass. Radiology 2008;249:16-31   DOI
2 Gill IS, Aron M, Gervais DA, Jewett MA. Clinical practice. Small renal mass. N Engl J Med 2010;362:624-634   DOI
3 Chow WH, Dong LM, Devesa SS. Epidemiology and risk factors for kidney cancer. Nat Rev Urol 2010;7:245-257   DOI
4 Reis LAG, Melbert D, Krapcho M, Stinchcomb DG, Howlader N, Horner MJ, et al. SEER Cancer Statistics Review, 1975-2007. Bethesda, MD: National Cancer Institute, 2008
5 Rioux-Leclercq N, Karakiewicz PI, Trinh QD, Ficarra V, Cindolo L, de la Taille A, et al. Prognostic ability of simplified nuclear grading of renal cell carcinoma. Cancer 2007;109:868-874   DOI
6 Frank I, Blute ML, Cheville JC, Lohse CM, Weaver AL, Zincke H. Solid renal tumors: an analysis of pathological features related to tumor size. J Urol 2003;170(6 Pt 1):2217-2220   DOI
7 Thompson RH, Kurta JM, Kaag M, Tickoo SK, Kundu S, Katz D, et al. Tumor size is associated with malignant potential in renal cell carcinoma cases. J Urol 2009;181:2033-2036   DOI
8 Sivalingam S, Nakada SY. Contemporary minimally invasive treatment options for renal angiomyolipomas. Curr Urol Rep 2013;14:147-153   DOI
9 Lane BR, Aydin H, Danforth TL, Zhou M, Remer EM, Novick AC, et al. Clinical correlates of renal angiomyolipoma subtypes in 209 patients: classic, fat poor, tuberous sclerosis associated and epithelioid. J Urol 2008;180:836-843   DOI
10 Siegel CL, Middleton WD, Teefey SA, McClennan BL. Angiomyolipoma and renal cell carcinoma: US differentiation. Radiology 1996;198:789-793   DOI
11 Jinzaki M, Ohkuma K, Tanimoto A, Mukai M, Hiramatsu K, Murai M, et al. Small solid renal lesions: usefulness of power Doppler US. Radiology 1998;209:543-550   DOI
12 Bosniak MA, Megibow AJ, Hulnick DH, Horii S, Raghavendra BN. CT diagnosis of renal angiomyolipoma: the importance of detecting small amounts of fat. AJR Am J Roentgenol 1988;151:497-501   DOI
13 Lemaitre L, Claudon M, Dubrulle F, Mazeman E. Imaging of angiomyolipomas. Semin Ultrasound CT MR 1997;18:100-114   DOI
14 Israel GM, Hindman N, Hecht E, Krinsky G. The use of opposed-phase chemical shift MRI in the diagnosis of renal angiomyolipomas. AJR Am J Roentgenol 2005;184:1868-1872   DOI
15 Takahashi K, Honda M, Okubo RS, Hyodo H, Takakusaki H, Yokoyama H, et al. CT pixel mapping in the diagnosis of small angiomyolipomas of the kidneys. J Comput Assist Tomogr 1993;17:98-101   DOI
16 Kurosaki Y, Tanaka Y, Kuramoto K, Itai Y. Improved CT fat detection in small kidney angiomyolipomas using thin sections and single voxel measurements. J Comput Assist Tomogr 1993;17:745-748   DOI
17 Hafron J, Fogarty JD, Hoenig DM, Li M, Berkenblit R, Ghavamian R. Imaging characteristics of minimal fat renal angiomyolipoma with histologic correlations. Urology 2005;66:1155-1159   DOI
18 Jinzaki M, Tanimoto A, Narimatsu Y, Ohkuma K, Kurata T, Shinmoto H, et al. Angiomyolipoma: imaging findings in lesions with minimal fat. Radiology 1997;205:497-502   DOI
19 Trigaux JP, Pauls C, Van Beers B. Atypical renal hamartomas: ultrasonography, computed tomography, and angiographic findings. J Clin Ultrasound 1993;21:41-44   DOI
20 Jinzaki M, Silverman SG, Akita H, Nagashima Y, Mikami S, Oya M. Renal angiomyolipoma: a radiological classification and update on recent developments in diagnosis and management. Abdom Imaging 2014;39:588-604   DOI
21 Lee MS, Cho JY, Kim SH. Ultrasonographic differentiation of small angiomyolipoma from renal cell carcinoma by measuring relative echogenicity on PACS. J Korean Soc Ultrasound Med 2010;29:105-113   DOI
22 Kim JK, Park SY, Shon JH, Cho KS. Angiomyolipoma with minimal fat: differentiation from renal cell carcinoma at biphasic helical CT. Radiology 2004;230:677-684   DOI
23 Yang CW, Shen SH, Chang YH, Chung HJ, Wang JH, Lin AT, et al. Are there useful CT features to differentiate renal cell carcinoma from lipid-poor renal angiomyolipoma? AJR Am J Roentgenol 2013;201:1017-1028   DOI
24 Kim MH, Lee J, Cho G, Cho KS, Kim J, Kim JK. MDCT-based scoring system for differentiating angiomyolipoma with minimal fat from renal cell carcinoma. Acta Radiol 2013;54:1201-1209   DOI
25 Simpfendorfer C, Herts BR, Motta-Ramirez GA, Lockwood DS, Zhou M, Leiber M, et al. Angiomyolipoma with minimal fat on MDCT: can counts of negative-attenuation pixels aid diagnosis? AJR Am J Roentgenol 2009;192:438-443   DOI
26 Chaudhry HS, Davenport MS, Nieman CM, Ho LM, Neville AM. Histogram analysis of small solid renal masses: differentiating minimal fat angiomyolipoma from renal cell carcinoma. AJR Am J Roentgenol 2012;198:377-383   DOI
27 Catalano OA, Samir AE, Sahani DV, Hahn PF. Pixel distribution analysis: can it be used to distinguish clear cell carcinomas from angiomyolipomas with minimal fat? Radiology 2008;247:738-746   DOI
28 Choi HJ, Kim JK, Ahn H, Kim CS, Kim MH, Cho KS. Value of T2-weighted MR imaging in differentiating low-fat renal angiomyolipomas from other renal tumors. Acta Radiol 2011;52:349-353   DOI
29 Chung MS, Choi HJ, Kim MH, Cho KS. Comparison of T2-weighted MRI with and without fat suppression for differentiating renal angiomyolipomas without visible fat from other renal tumors. AJR Am J Roentgenol 2014;202:765-771   DOI
30 Sasiwimonphan K, Takahashi N, Leibovich BC, Carter RE, Atwell TD, Kawashima A. Small (<4 cm) renal mass: differentiation of angiomyolipoma without visible fat from renal cell carcinoma utilizing MR imaging. Radiology 2012;263:160-168   DOI
31 Kido T, Yamashita Y, Sumi S, Baba Y, Takahashi M, Ootsuka Y, et al. Chemical shift GRE MRI of renal angiomyolipoma. J Comput Assist Tomogr 1997;21:268-270   DOI
32 Kim JK, Kim SH, Jang YJ, Ahn H, Kim CS, Park H, et al. Renal angiomyolipoma with minimal fat: differentiation from other neoplasms at double-echo chemical shift FLASH MR imaging. Radiology 2006;239:174-180   DOI
33 Hindman N, Ngo L, Genega EM, Melamed J, Wei J, Braza JM, et al. Angiomyolipoma with minimal fat: can it be differentiated from clear cell renal cell carcinoma by using standard MR techniques? Radiology 2012;265:468-477   DOI
34 Verma SK, Mitchell DG, Yang R, Roth CG, O'Kane P, Verma M, et al. Exophytic renal masses: angular interface with renal parenchyma for distinguishing benign from malignant lesions at MR imaging. Radiology 2010;255:501-507   DOI
35 Kim KH, Yun BH, Jung SI, Hwang IS, Hwang EC, Kang TW, et al. Usefulness of the ice-cream cone pattern in computed tomography for prediction of angiomyolipoma in patients with a small renal mass. Korean J Urol 2013;54:504-509   DOI
36 van den Berg E, Dijkhuizen T, Oosterhuis JW, Geurts van Kessel A, de Jong B, Storkel S. Cytogenetic classification of renal cell cancer. Cancer Genet Cytogenet 1997;95:103-107   DOI
37 Agnello F, Roy C, Bazille G, Galia M, Midiri M, Charles T, et al. Small solid renal masses: characterization by diffusion-weighted MRI at 3 T. Clin Radiol 2013;68:e301-e308   DOI
38 Tan S, Ozcan MF, Tezcan F, Balci S, Karaog˘lanog˘lu M, Huddam B, et al. Real-time elastography for distinguishing angiomyolipoma from renal cell carcinoma: preliminary observations. AJR Am J Roentgenol 2013;200:W369-W375   DOI
39 Tanaka H, Yoshida S, Fujii Y, Ishii C, Tanaka H, Koga F, et al. Diffusion-weighted magnetic resonance imaging in the differentiation of angiomyolipoma with minimal fat from clear cell renal cell carcinoma. Int J Urol 2011;18:727-730   DOI
40 Sasamori H, Saiki M, Suyama J, Ohgiya Y, Hirose M, Gokan T. Utility of apparent diffusion coefficients in the evaluation of solid renal tumors at 3T. Magn Reson Med Sci 2014;13:89-95   DOI
41 Geramizadeh B, Ravanshad M, Rahsaz M. Useful markers for differential diagnosis of oncocytoma, chromophobe renal cell carcinoma and conventional renal cell carcinoma. Indian J Pathol Microbiol 2008;51:167-171   DOI
42 Kurup AN, Thompson RH, Leibovich BC, Harmsen WS, Sebo TJ, Callstrom MR, et al. Renal oncocytoma growth rates before intervention. BJU Int 2012;110:1444-1448   DOI
43 Goiney RC, Goldenberg L, Cooperberg PL, Charboneau JW, Rosenfield AT, Russin LD, et al. Renal oncocytoma: sonographic analysis of 14 cases. AJR Am J Roentgenol 1984;143:1001-1004   DOI
44 Charboneau JW, Hattery RR, Ernst EC 3rd, James EM, Williamson B Jr, Hartman GW. Spectrum of sonographic findings in 125 renal masses other than benign simple cyst. AJR Am J Roentgenol 1983;140:87-94   DOI
45 Quinn MJ, Hartman DS, Friedman AC, Sherman JL, Lautin EM, Pyatt RS, et al. Renal oncocytoma: new observations. Radiology 1984;153:49-53   DOI
46 Woo S, Cho JY, Kim SH, Kim SY, Lee HJ, Hwang SI, et al. Segmental enhancement inversion of small renal oncocytoma: differences in prevalence according to tumor size. AJR Am J Roentgenol 2013;200:1054-1059   DOI
47 Ambos MA, Bosniak MA, Valensi QJ, Madayag MA, Lefleur RS. Angiographic patterns in renal oncocytomas. Radiology 1978;129:615-622   DOI
48 Davidson AJ, Hayes WS, Hartman DS, McCarthy WF, Davis CJ Jr. Renal oncocytoma and carcinoma: failure of differentiation with CT. Radiology 1993;186:693-696   DOI
49 Kim JI, Cho JY, Moon KC, Lee HJ, Kim SH. Segmental enhancement inversion at biphasic multidetector CT: characteristic finding of small renal oncocytoma. Radiology 2009;252:441-448   DOI
50 McGahan JP, Lamba R, Fisher J, Starshak P, Ramsamooj R, Fitzgerald E, et al. Is segmental enhancement inversion on enhanced biphasic MDCT a reliable sign for the noninvasive diagnosis of renal oncocytomas? AJR Am J Roentgenol 2011;197:W674-W679   DOI
51 O'Malley ME, Tran P, Hanbidge A, Rogalla P. Small renal oncocytomas: is segmental enhancement inversion a characteristic finding at biphasic MDCT? AJR Am J Roentgenol 2012;199:1312-1315   DOI
52 Schieda N, McInnes MD, Cao L. Diagnostic accuracy of segmental enhancement inversion for diagnosis of renal oncocytoma at biphasic contrast enhanced CT: systematic review. Eur Radiol 2014;24:1421-1429   DOI
53 Alshumrani G, O'Malley M, Ghai S, Metser U, Kachura J, Finelli A, et al. Small (< or = 4 cm) cortical renal tumors: characterization with multidetector CT. Abdom Imaging 2010;35:488-493   DOI
54 Gakis G, Kramer U, Schilling D, Kruck S, Stenzl A, Schlemmer HP. Small renal oncocytomas: differentiation with multiphase CT. Eur J Radiol 2011;80:274-278   DOI
55 Lanzman RS, Robson PM, Sun MR, Patel AD, Mentore K, Wagner AA, et al. Arterial spin-labeling MR imaging of renal masses: correlation with histopathologic findings. Radiology 2012;265:799-808   DOI
56 Bird VG, Kanagarajah P, Morillo G, Caruso DJ, Ayyathurai R, Leveillee R, et al. Differentiation of oncocytoma and renal cell carcinoma in small renal masses (<4 cm): the role of 4-phase computerized tomography. World J Urol 2011;29:787-792   DOI
57 Rosenkrantz AB, Hindman N, Fitzgerald EF, Niver BE, Melamed J, Babb JS. MRI features of renal oncocytoma and chromophobe renal cell carcinoma. AJR Am J Roentgenol 2010;195:W421-W427   DOI
58 Cornelis F, Tricaud E, Lasserre AS, Petitpierre F, Bernhard JC, Le Bras Y, et al. Routinely performed multiparametric magnetic resonance imaging helps to differentiate common subtypes of renal tumours. Eur Radiol 2014;24:1068-1080   DOI
59 Lassel EA, Rao R, Schwenke C, Schoenberg SO, Michaely HJ. Diffusion-weighted imaging of focal renal lesions: a meta-analysis. Eur Radiol 2014;24:241-249   DOI
60 Choyke PL. Imaging of hereditary renal cancer. Radiol Clin North Am 2003;41:1037-1051   DOI
61 Rowsell C, Fleshner N, Marrano P, Squire J, Evans A. Papillary renal cell carcinoma within a renal oncocytoma: case report of an incidental finding of a tumour within a tumour. J Clin Pathol 2007;60:426-428
62 Davis CJ Jr, Barton JH, Sesterhenn IA, Mostofi FK. Metanephric adenoma. Clinicopathological study of fifty patients. Am J Surg Pathol 1995;19:1101-1114   DOI
63 Patankar T, Punekar S, Madiwale C, Prasad S, Hanchate V. Metanephric adenoma in a solitary kidney. Br J Radiol 1999;72:80-81   DOI
64 Katabathina VS, Vikram R, Nagar AM, Tamboli P, Menias CO, Prasad SR. Mesenchymal neoplasms of the kidney in adults: imaging spectrum with radiologic-pathologic correlation. Radiographics 2010;30:1525-1540   DOI
65 Fielding JR, Visweswaran A, Silverman SG, Granter SR, Renshaw AA. CT and ultrasound features of metanephric adenoma in adults with pathologic correlation. J Comput Assist Tomogr 1999;23:441-444   DOI
66 Araki T, Hata H, Asakawa E, Araki T. MRI of metanephric adenoma. J Comput Assist Tomogr 1998;22:87-90   DOI
67 Prasad SR, Surabhi VR, Menias CO, Raut AA, Chintapalli KN. Benign renal neoplasms in adults: cross-sectional imaging findings. AJR Am J Roentgenol 2008;190:158-164   DOI
68 Steiner M, Quinlan D, Goldman SM, Millmond S, Hallowell MJ, Stutzman RE, et al. Leiomyoma of the kidney: presentation of 4 new cases and the role of computerized tomography. J Urol 1990;143:994-998   DOI
69 Radvany MG, Shanley DJ, Gagliardi JA. Magnetic resonance imaging with computed tomography of a renal leiomyoma. Abdom Imaging 1994;19:67-69   DOI
70 Conn JW, Cohen EL, Lucas CP, McDonald WJ, Mayor GH, Blough WM Jr, et al. Primary reninism. Hypertension, hyperreninemia, and secondary aldosteronism due to renin-producing juxtaglomerular cell tumors. Arch Intern Med 1972;130:682-696   DOI
71 Prasad SR, Narra VR, Shah R, Humphrey PA, Jagirdar J, Catena JR, et al. Segmental disorders of the nephron: histopathological and imaging perspective. Br J Radiol 2007;80:593-602   DOI
72 Dunnick NR, Hartman DS, Ford KK, Davis CJ Jr, Amis ES Jr. The radiology of juxtaglomerular tumors. Radiology 1983;147:321-326   DOI
73 Herts BR, Baker ME. The current role of percutaneous biopsy in the evaluation of renal masses. Semin Urol Oncol 1995;13:254-261
74 Remzi M, Katzenbeisser D, Waldert M, Klingler HC, Susani M, Memarsadeghi M, et al. Renal tumour size measured radiologically before surgery is an unreliable variable for predicting histopathological features: benign tumours are not necessarily small. BJU Int 2007;99:1002-1006   DOI
75 Duchene DA, Lotan Y, Cadeddu JA, Sagalowsky AI, Koeneman KS. Histopathology of surgically managed renal tumors: analysis of a contemporary series. Urology 2003;62:827-830   DOI
76 Silver DA, Morash C, Brenner P, Campbell S, Russo P. Pathologic findings at the time of nephrectomy for renal mass. Ann Surg Oncol 1997;4:570-574   DOI
77 Sahni VA, Silverman SG. Biopsy of renal masses: when and why. Cancer Imaging 2009;9:44-55   DOI
78 Helm CW, Burwood RJ, Harrison NW, Melcher DH. Aspiration cytology of solid renal tumours. Br J Urol 1983;55:249-253   DOI
79 Murphy WM, Zambroni BR, Emerson LD, Moinuddin S, Lee LH. Aspiration biopsy of the kidney. Simultaneous collection of cytologic and histologic specimens. Cancer 1985;56:200-205   DOI
80 Bonzanini M, Pea M, Martignoni G, Zamboni G, Capelli P, Bernardello F, et al. Preoperative diagnosis of renal angiomyolipoma: fine needle aspiration cytology and immunocytochemical characterization. Pathology 1994;26:170-175   DOI
81 Gupta RK, Nowitz M, Wakefield SJ. Fine-needle aspiration cytology of renal angiomyolipoma: report of a case with immunocytochemical and electron microscopic findings. Diagn Cytopathol 1998;18:297-300   DOI
82 Renshaw AA, Lee KR, Madge R, Granter SR. Accuracy of fine needle aspiration in distinguishing subtypes of renal cell carcinoma. Acta Cytol 1997;41:987-994   DOI
83 Wehle MJ, Grabstald H. Contraindications to needle aspiration of a solid renal mass: tumor dissemination by renal needle aspiration. J Urol 1986;136:446-448   DOI
84 Zhou M, Roma A, Magi-Galluzzi C. The usefulness of immunohistochemical markers in the differential diagnosis of renal neoplasms. Clin Lab Med 2005;25:247-257   DOI
85 Smith EH. Complications of percutaneous abdominal fine-needle biopsy. Review. Radiology 1991;178:253-258   DOI
86 Silverman SG, Gan YU, Mortele KJ, Tuncali K, Cibas ES. Renal masses in the adult patient: the role of percutaneous biopsy. Radiology 2006;240:6-22   DOI
87 Slywotzky C, Maya M. Needle tract seeding of transitional cell carcinoma following fine-needle aspiration of a renal mass. Abdom Imaging 1994;19:174-176   DOI
88 Woo S, Cho JY, Kim SH, Kim SY. Angiomyolipoma with minimal fat and non-clear cell renal cell carcinoma: differentiation on MDCT using classification and regression tree analysis-based algorithm. Acta Radiol 2014;55:1258-1269   DOI
89 Eble JN, Sauter G, Epstein JI, Sesterhenn IA. World Health Organization Classification of Tumors. Pathology and genetics of tumors of the Urinary System and Male Genital Organs. Lyon: IARC Press, 2004:65-66
90 Tamboli P, Ro JY, Amin MB, Ligato S, Ayala AG. Benign tumors and tumor-like lesions of the adult kidney. Part II: benign mesenchymal and mixed neoplasms, and tumor-like lesions. Adv Anat Pathol 2000;7:47-66   DOI
91 Oliva MR, Glickman JN, Zou KH, Teo SY, Mortele KJ, Rocha MS, et al. Renal cell carcinoma: t1 and t2 signal intensity characteristics of papillary and clear cell types correlated with pathology. AJR Am J Roentgenol 2009;192:1524-1530   DOI
92 Storkel S, Pannen B, Thoenes W, Steart PV, Wagner S, Drenckhahn D. Intercalated cells as a probable source for the development of renal oncocytoma. Virchows Arch B Cell Pathol Incl Mol Pathol 1988;56:185-189   DOI
93 Rybicki FJ, Shu KM, Cibas ES, Fielding JR, vanSonnenberg E, Silverman SG. Percutaneous biopsy of renal masses: sensitivity and negative predictive value stratified by clinical setting and size of masses. AJR Am J Roentgenol 2003;180:1281-1287   DOI
94 Woo S, Cho JY, Kim SH, Kim SY. Comparison of segmental enhancement inversion on biphasic MDCT between small renal oncocytomas and chromophobe renal cell carcinomas. AJR Am J Roentgenol 2013;201:598-604   DOI
95 Cornelis F, Lasserre AS, Tourdias T, Deminiere C, Ferriere JM, Le Bras Y, et al. Combined late gadolinium-enhanced and double-echo chemical-shift MRI help to differentiate renal oncocytomas with high central T2 signal intensity from renal cell carcinomas. AJR Am J Roentgenol 2013;200:830-838   DOI
96 Martin SA, Mynderse LA, Lager DJ, Cheville JC. Juxtaglomerular cell tumor: a clinicopathologic study of four cases and review of the literature. Am J Clin Pathol 2001;116:854-863   DOI
97 Liu J, Fanning CV. Can renal oncocytomas be distinguished from renal cell carcinoma on fine-needle aspiration specimens? A study of conventional smears in conjunction with ancillary studies. Cancer 2001;93:390-397   DOI
98 Jasinski RW, Amendola MA, Glazer GM, Bree RL, Gikas PW. Computed tomography of renal oncocytomas. Comput Radiol 1985;9:307-314   DOI
99 Amin MB, Corless CL, Renshaw AA, Tickoo SK, Kubus J, Schultz DS. Papillary (chromophil) renal cell carcinoma: histomorphologic characteristics and evaluation of conventional pathologic prognostic parameters in 62 cases. Am J Surg Pathol 1997;21:621-635   DOI