Renal hybrid oncocytic/chromophobe tumors - A review

Histology and Histopathology

Volumn 28, Issue 10, 2013, Pages 1257-1264

  Hes, Ondrej ^a   Petersson, Fredrik ^b   Kuroda, Naoto ^c   Hora, Milan ^a   Michal, Michal ^a  

^a CHARLES UNIVERSITY   (Czech Republic)

^b NATIONAL UNIVERSITY HEALTH SYSTEM   (Singapore)

^c KOCHI RED CROSS HOSPITAL   (Japan)

Author keywords

Birt hogg dub ; Chromophobe renal cell carcinoma; Kidney; Oncocytoma; Oncocytosis; Sporadic hybrid tumor; Syndrome

Indexed keywords

STEM CELL FACTOR RECEPTOR;

BIRT HOGG DUBE SYNDROME; CHEMISTRY; CHROMOSOME ABERRATION; CYTOLOGY; DIFFERENTIAL DIAGNOSIS; DISEASE COURSE; EOSINOPHIL; HUMAN; IMMUNOHISTOCHEMISTRY; KIDNEY; KIDNEY CARCINOMA; KIDNEY TUMOR; MUTATION; ONCOCYTOMA; PATHOLOGY; PROGNOSIS; REVIEW;

ADENOMA, OXYPHILIC; BIRT-HOGG-DUBE SYNDROME; CARCINOMA, RENAL CELL; CHROMOSOME ABERRATIONS; DIAGNOSIS, DIFFERENTIAL; DISEASE PROGRESSION; EOSINOPHILS; HUMANS; IMMUNOHISTOCHEMISTRY; KIDNEY; KIDNEY NEOPLASMS; MUTATION; PROGNOSIS; PROTO-ONCOGENE PROTEINS C-KIT;

EID: 84885347572     PISSN: 02133911     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Review

References (58)

1. Abbosh P.H., Grubb R.L., Cao D. and Humphrey P.A. (2011). Hybrid renal tumors in Birt-Hogg-Dube syndrome. J. Urol. 186, 2413-2414.
2. Adamy A., Lowrance W.T., Yee D.S., Chong K.T., Bernstein M., Tickoo S.K., Coleman J.A. and Russo P. (2011). Renal oncocytosis: Management and clinical outcomes. J. Urol. 185, 795-801.
3. Adley B.P., Smith N.D., Nayar R. and Yang X.J. (2006). Birt-Hogg-Dube syndrome: clinicopathologic findings and genetic alterations. Arch. Pathol. Lab. Med. 130, 1865-1870.
4. Al-Saleem T., Cairns P., Dulaimi E. A., Feder M, Testa J.R. and Uzzo R.G. (2004). The genetics of renal oncocytosis: a possible model for neoplastic progression. Cancer Genet. Cytogenet. 152, 23-28.
5. Amin M.B., Paner G.P., Alvarado-Cabrero I., Young A.N., Stricker H.J., Lyles R.H. and Moch H. (2008). Chromophobe renal cell carcinoma: histomorphologic characteristics and evaluation of conventional pathologic prognostic parameters in 145 cases. Am. J. Surg. Pathol. 32, 1822-1834.
6. Barcena C., Martinez M.A., Ortega P., Munoz G. and Usera Sarraga G. (2010). Mitochondria with tubulovesicular cristae in renal oncocytomas. Ultrastruct. Pathol. 34, 315-320.
7. Brunelli M., Eble J.N., Zhang S., Martignoni G., Delahunt B. and Cheng L. (2005). Eosinophilic and classic chromophobe renal cell carcinomas have similar frequent losses of multiple chromosomes from among chromosomes 1, 2, 6, 10, and 17, and this pattern of genetic abnormality is not present in renal oncocytoma. Mod. Pathol. 18, 161-169.
8. Caamano V., Gonzalez M., Perez A., Cerda A., Coromias A., Muniz G., Gaafar A. and Lopez J. I. (2012). Renal cell carcinoma with papillary and chromophobe features: An example of hybrid tumor. Virchows Arch. 461 (1), S280-S281.
9. Chen T.S., McNally M., Hulbert W., Agnese P.A. and Huang J. (2003). Renal oncocytosis presenting in childhood: A case report. Int. J. Surg. Pathol. 11, 325-329.
10. Cossu-Rocca P., Brunelli M., Gobbo S., Eccher A., Bragantini E., Mina M.M., Ficarra V., Zattoni F., Zamò A., Pea M., Scarpa A., Chilosi M., Menestrina F., Bonetti F., Eble J.N. and Martignoni G. (2007). Diagnostic utility of S100A1 expression in renal cell neoplasms: an immunohistochemical and quantitative RT-PCR study. Mod. Pathol. 20, 722-728.
11. Cossu-Rocca P., Eble J.N., Zhang S., Bonsib S.M., Martignoni G., Brunelli M., and Cheng L. (2008). Interphase cytogenetic analysis with centromeric probes for chromosomes 1, 2, 6, 10, and 17 in 11 tumors from a patient with bilateral renal oncocytosis. Mod. Pathol. 21, 498-504.
12. Delongchamps N.B., Galmiche L. and Eiss D. (2009). Hybrid tumour 'oncocytoma-chromophobe renal cell carcinoma' of the kidney: a report of seven sporadic cases. BJU Int. 103, 1381-1384.
13. Erlandson R.A., Shek T.W.H. and Reuter V.E. (1997) Diagnostic significance of mitochondria in four types of renal epithelial neoplasms: an ultrastructural study of 60 cases. Ultrastruct. Pathol. 21, 409-417.
14. Furuya M., Tanaka R., Koga S., Yatabe Y., Gotoda H., Takagi S., Hsu Y.H., Fujii T., Okada A., Kuroda N., Moritani S., Mizuno H., Nagashima Y., Nagahama K., Hiroshima K., Yoshino I., Nomura F., Aoki I. and Nakatani Y. (2012). Pulmonary cysts of Birt-Hogg-Dubé syndrome: a clinicopathologic and immunohistochemical study of 9 families. Am. J. Surg. Pathol. 36, 589-600.
15. Gatalica Z., Lilleberg S.L., Vranic S., Eyzaguirre E., Orihuela E. and Velagaleti G. (2009). Novel intronic germ-line FLCN gene mutation in a patient with multiple ipsilateral renal neoplasms. Hum. Pathol. 40, 1813-1819.
16. Gobbo S., Eble J.N., Delahunt B., Grignon D.J., Samaratunga H., Martignoni G., Zhang S., Wang M., Brunelli M., Cossu-Rocca P. and Cheng L. (2010). Renal cell neoplasms of oncocytosis have distinct morphologic, immunohistochemical, and cytogenetic profile. Am. J. Surg. Pathol. 34, 620-626.
17. Hagenkord J.M., Gatalica Z., Jonasch E. and Monzon F.A. (2011). Clinical genomics of renal epithelial tumors. Cancer Genet. 204, 285-297.
18. Haudebourg J., Hoch B., Fabas T., Cardot-Leccia N., Burel-Vandenbos F., Vieillefond A., Amiel J., Michiels J.F. and Pedeutour F. (2010). Strength of molecular cytogenetic analyses for adjusting the diagnosis of renal cell carcinomas with both clear cells and papillary features: a study of three cases. Virchows Arch. 457,397-404.
19. Hes O., Michal M., Boudova L., Mukensnabl P., Kinkor Z. and Miculka P. (2001). Small cell variant of renal oncocytoma-a rare and misleading type of benign renal tumor. Int. J. Surg. Pathol. 9, 215-222.
20. Hes O., Vanecek T., Perez-Montiel D.M., Alvarado Cabrero I., Hora M., Suster S., Lamovec J., Curik R., Mandys V. and Michal M. (2005). Chromophobe renal cell carcinoma with microcystic and adenomatous arrangement and pigmentation--a diagnostic pitfall. Morphological, immunohistochemical, ultrastructural and molecular genetic report of 20 cases. Virchows Arch. 446, 383-393.
21. Hes O., Brunelli M., Michal M., Cossu Rocca P., Hora M., Chilosi M., Mina M., Boudova L., Menestrina F. and Martignoni G. (2006). Oncocytic papillary renal cell carcinoma: a clinicopathologic, immunohistochemical, ultrastructural, and interphase cytogenetic study of 12 cases. Ann. Diagn. Pathol. 10, 133-139
22. Hes O., Michal M., Síma R., Vanecek T., Brunelli M., Martignoni G., Kuroda N., Alvarado Cabrero I., Perez-Montiel D., Hora M., Urge T., Dvorák M., Jarosova M. and Yang X. (2008). Renal oncocytoma with and without intravascular extension into the branches of renal vein have the same morphological, immunohistochemical, and genetic features. Virchows Arch. 452, 193-200.
23. Herbers J., Schullerus D., Chudek J., Bugert P., Kanamaru H., Zeisler J., Ljungberg B., Akhtar M. and Kovacs G. (1998). Lack of genetic changes at specific genomic sites separates renal oncocytomas from renal cell carcinomas. J. Pathol. 184, 58-62.
24. Houweling A.C., Gijezen L.M., Jonker M.A., van Doorn M.B.A., Oldenburg R.A., van Spaendonck-Zwarts K.Y., Leter E.M., van Os T.A., van Grieken N.C.T., Jaspars E.H., deJong M.M., Bongers E.M.H.F., Johanesma P.C., Postmus P.E., van Moorselaar J.-H.T.M., Starink T.M., van Steensel M.A.M., Gille J.J.P, Menko F.H. (2011). Renal cancer and pneumothorax risk in Birt-Hogg-Dubé syndrome; an analysis of 115 FLCN mutation carriers from 35 BHD families. Br. J. Cancer 105, 1912-1919.
25. Imada K., Dainichi T., Yokomizo A., Tsunoda T., Song Y.H., Nagasaki A., Sawamura D., Nishie W., Shimizu H., Fukagawa S., Urabe K., Furue M., Hashimoto T. and Naito S. (2009). Birt-Hogg-Dube syndrome with clear-cell and oncocytic renal tumour and trichoblastoma associated with a novel FLCN mutation. Br. J. Dermatol. 160, 1350-1353.
26. Kesik V., Yalcin B., Akcoren Z., Senocak M.E., Talim B. and Buyukpamukcu M. (2010). A rare type of renal cell carcinoma in a girl: Hybrid renal cell carcioma. Ped. Hematol. Oncol. 27, 228-232.
27. Klomp J.A., Petillo D., Niemi N.M., Dykema K.J., Chen J., Yang X.J., Sääf A., Zickert P., Aly M., Bergerheim U., Nordenskjöld M., Gad S., Giraud S., Denoux Y., Yonneau L., Méjean A., Vasiliu V., Richard S., MacKeigan J.P., Teh B.T. and Furge K.A. (2010). Birt-Hogg-Dube renal tumors are genetically distinct from other renal neoplasias and are associated with up-regulation of mitochondrial gene expression. BMC Med. Genom. 3, 59.
28. Kluijt I., de Jong D., Teertsra H.J., Axwijk P.H., Gille J.J.P., Bell K., van Rens A., van der Velden A.W.G., Middelton L, Horenblas S. (2009). Early onset of renal cancer in a family with Birt-Hogg-Dube syndrome. Clin. Genet. 75, 537-543.
29. Kovacs G., Szucs S., Eichner W., Maschek H.J., Wahnschaffe U. and De Riese W. (1987) Renal oncocytoma. A cytogenetic and morphologic study. Cancer 59, 2071-2077.
30. Kovacs G., Welter C., Wilkens L., Blin N. and De Riese W. (1989). Renal oncocytoma. A phenotypic and genotypic entity of renal parenchymal tumors. Am. J. Pathol. 134, 967-971.
31. Kuroda N. (2003). Renal oncocytomatosis in a long-term hemodialysis patient treated by laparoscopic surgery. Int. J. Urol. 10, 510.
32. Kuroda N., Tanaka A., Ohe C., Mikami S., Nagashima Y., Sasaki T., Inoue K., Hes O., Michal M., Brunelli M. and Martignoni G.(2012). Review of renal oncocytosis (multiple oncocytic lesions) with focus on clinical and pathobiological aspects. Histol. Histopathol. 27, 1407-1412.
33. Lefevre M., Couturier J., Sibony M., Bazille C., Boyer K., Callard P., Vieillefond A. and Allory Y. (2005). Adult papillary renal tumor with oncocytic cells: clinicopathologic, immunohistochemical, and cytogenetic features of 10 cases. Am. J. Surg. Pathol. 29, 1576-1581.
34. Leroy X., Lemaitre L., De La Taille A., Hazzan M., Delepaul B., Couturier J. and Gosselin B. (2001). Bilateral renal oncocytosis with renal failure: Immunohistochemical and cytogenetic study of a case associated with a papillary renal cell carcinoma. Arch. Pathol. Lab. Med. 125, 683-685.
35. Lhermitte B, Leval de L. (2012). Review and Perspectives. Interpretation of needle biopsies of the kidney for investigation of renal masses. Virchows Arch. 461, 13-26.
36. Mai K.T., Dhamanaskar P., Belanger E. and Stinson W.A. (2005). Hybrid chromophobe renal cell neoplasm. Pathol. Res. Pract. 201, 385-389.
37. Mai K.T., Kohler D.M., Roustan Delatour N.L. and Veinot J.P. (2006). Cytohistopathologic hybrid renal cell carcinoma with papillary and clear cell features. Pathol. Res. Pract. 202, 863-8.
38. Mazzucchelli R., Cheng L., Lopez-Beltran A., Scarpelli M. and Montironi R. (2008). Renal oncocytosis and multiple papillary adenomas with renal oncocytoma as dominant nodules coexisting with papillary carcinoma in a patient with diabetic glomerulosclerosis, acquired renal cystic disease and B cell lymphoma. APMIS 116, 934-938.
39. Murakami T., Sano F., Huang Y., Komiya A., Baba M., Osada Y., Nagashima Y., Kondo K., Nakaigawa N., Miura T., Kubota Y., Yao M. and Kishida T. (2007). Identification and characterization of Birt-Hogg-Dube associated renal carcinoma. J. Pathol. 211, 524-531.
40. Nagashima Y., Mitsuya T., Shioi K., Noguchi S., Kishida T., Hamano A., Ohgo Y., Tsuura Y., Ogawa T., Aoki I. and Yao M. (2005). Renal oncocytosis. Pathol. Int. 55, 210-215.
41. Nagashima Y., Furuya M., Gotohda H., Takagi S., Hes O., Michal M., Grossmann P., Tanaka R., Nakatani Y. and Kuroda N. (2012). FLCN gene-mutated renal cell neoplasms: mother and daughter cases with a novel germline mutation. Int. J. Urol. 19:468-470.
42. Ohe C., Kuroda N., Takasu K., Senzaki H., Shikata N., Yamaguchi T., Miyasaka C., Nakano Y., Sakaida N. and Uemura Y. (2012). Utility of immunohistochemical analysis of KAI1, epithelial-specific antigen, and epithelial-related antigen for distinction of chromophobe renal cell carcinoma, an eosinophilic variant from renal oncocytoma. Med. Mol. Morphol. 45, 98-104.
43. Osunkoya A.O., Cohen C., Lawson D., Picken M.M., Amin M.B. and Young A.N. (2009). Claudin-7 and claudin-8: immunohistochemical markers for the differential diagnosis of chromophobe renal cell carcinoma and renal oncocytoma. Hum. Pathol.40, 206-210.
44. Pavlovich C.P., Walther M.M., Eyler R.A, Hewitt S.M., Zbar B., Linehan W.M, Merino M.J. (2002). Renal tumors in the Birt-Hogg-Dube syndrome. Am. J. Surg. Pathol. 26, 1542-1552.
45. Pavlovich C.P., Grubb R.L., Hurley K. Glenn G.M., Toro J., Schmidt L.S., Torres-Cabala C., Merino M.J., Zbar B., Choyke P., Walther M.M., Linehan W.M. (2005). Evaluation and management of renal tumors in the Birt-Hogg-Dube syndrome. J. Urol. 173, 1482-1486.
46. Petersson F., Gatalica Z., Grossmann P., Perez Montiel M.D., Alvarado Cabrero I., Bulimbasic S., Swatek A., Straka L., Tichy T., Hora M., Kuroda N., Legendre B., Michal M. and Hes O. (2010). Sporadic hybrid oncocytic/chromophobe tumor of the kidney: a clinicopathologic, histomorphologic, immunohistochemical, ultrastructural, and molecular cytogenetic study of 14 cases. Virchows Arch. 456, 355-365.
47. Petersson F., Síma R., Grossmann P., Michal M., Kuroda N., Hora M., Yang X., Kinkor Z., Trivunic S., Zalud R., Sperga M., Jaunmuktane Z., Branžovský J., Ferda J. and Hes O. (2011). Renal small cell oncocytoma with pseudorosettes A histomorphologic, immunohistochemical, and molecular genetic study of 10 cases. Hum. Pathol. 42, 1751-1760.
48. Picken M.M. (2010). Editorial comment from dr. Picken to Molecular pathology of renal oncocytoma: A review. In. J. Urol. 17:613-614.
49. Presti J.C. Jr, Moch H., Reuter V.E., Huynh D. and Waldman F.M. (1996) Comparative genomic hybridization for genetic analysis of renal oncocytomas. Genes Chromosom. Cancer 17, 199-204.
50. Shiga Y., Suzuki K., Tsutsumi M., Ishikawa S., Gotoh M., Shimokawa T. and Hattori K. (2002). Renal oncocytomatosis in a long-term hemodialysis patient treated by laparoscopic surgery. Int. J. Urol. 9, 646-649.
51. Sydor A., Sulowicz W., Stompor T., Plezia B., Wrona A. and Okon K. (2009). Two consecutive cases of renal oncocytomatosis in a single-center experience. Clin. Nephrol. 71, 433-440.
52. Tickoo S.K. and Amin M.B. (1998). Discriminant nuclear features of renal oncocytoma and chromophobe renal cell carcinoma. Analysis of their potential utility in the differential diagnosis. Am. J. Clin. Pathol. 110, 782-787.
53. Tickoo S.K., Reuter V.E., Amin M.B., Srigley J.R., Epstein J.I., Min K.W., Rubin M.A., Ro J.Y. (1999). Renal oncocytosis: a morphologic study of fourteen cases. Am. J. Surg. Pathol. 23, 1094-1101.
54. Waldert M., Klatte T., Haitel A., Ozsoy M., Schmidbauer J., Marberger M. and Remzi M. (2010). Hybrid renal cell carcinomas containing histopathologic features of chromophobe renal cell carcinomas and oncocytomas have excellent oncologic outcomes. Eur. Urol. 57, 661-665.
55. Warfel K.A. and Eble J.N. (1982). Renal oncocytomatosis. J. Urol. 127, 1179-1180.
56. Yamaguchi T., Kuroda N., Imamura Y., Hes O., Michal M., Sima R., Nakayama K. and Sato N. (2010). Imprint cytologic features of chromophobe renal cell carcinoma morphologically resembling renal oncocytoma: is this an oncocytic variant of chromophobe renal cell carcinoma? Diagn. Cytopathol. 38, 509-513.
57. Yusenko M.V. (2010). Molecular pathology of renal oncocytoma: A review. Int. J. Urol. 17, 602-12.
58. Yusenko M.V. and Kovacs G. (2009). Identifying CD82 (KAI1) as a marker for human chromophobe renal cell carcinoma. Histopathology 55, 687-695.