Ultrastructural characteristics of primary renal epithelial tumours with granular oncocytic cytoplasm

  • Sandra Trivunić Dajko University of Novi Sad, Faculty of Medicine, Department of Pathology, Novi Sad, Serbia
  • Jovo Bogdanović University of Novi Sad, Faculty of Medicine, Department of Surgery, Novi Sad, Serbia;
  • Bojana Andrejić Višnjić University of Novi Sad, Faculty of Medicine, Department of Histology and Embriology, Novi Sad, Serbia
  • Milan Popović University of Novi Sad, Faculty of Medicine, Department of Histology and Embriology, Novi Sad, Serbia
  • Ondrej Hes Charles University Hospital, Department of Pathology, Plzen, Czech Republic
Keywords: kidney neoplasms, microscopy, electron, diagnosis, differential, mitochondria, cytoplasmic granules

Abstract


Abstract

 

Background/Aim. Ultrastructural analysis of tumours has shown many common characteristics of certain neoplasms, as well as their specificities. Primary renal epithelial tumours with granular oncocytic cytoplasm is a very heterogeneous group in their histological origin and biological behaviour, which results in a difference in treatment and prognosis of the disease, making accurate morphological diagnosis neces­sary. The aim of this study was to determine ultrastructural similarities and differences among primary renal epithelial tumours with granular oncocytic cytoplasm. Methods. The analysis of archival and routine material in the archives of the Department of Pathology, University Hospital in Plzen, Czech Republic, as well as archival and routine material in the Centre for Pathology and Histology, Clinical Centre of Vojvodina in Novi Sad, discovered 346 primary renal epithelial tumours with granular oncocytic cytoplasm and divided them into 5 groups: 1) renal oncocytoma (RO) (234 tumours), 2) oncocytic papillary renal cell carcinoma (O-PRCC) (12 tumours), 3. sporadic renal hybrid onco­cytic/chromophobe tumour (HOCT) without evidence of Birt Hogg Dubé syndrome (BHD) (14 tumours), 4) chro­mophobe renal cell carcinoma (ChRCC) (21 tumours) and 5) granular renal cell carcinoma (RCC) [64 tumours + 1 clear cell RCC (CRCC) with hyaline globules]. Ultrastruc­tural analysis of tumour cells at the subcellular level was done using electron microscope (Philips electron micro­scope TEM 208) at the Department of Pathology, Univer­sity Hospital in Plzen, Czech Republic. Cellular organelles and pigments were evaluated in 5 tumours from each group according to the simple random sample principle with a total of 30 analysed tumours. Results. In all analysed pri­mary renal epithelial tumours with granular oncocytic, cyto­plasm dominant organelles were mitochondria. Specific ul­trastructural characteristics of RO were round mitochondria with lamellar cristae, whereas ChRCC had numerous typical cytoplasmic microvesicles 100–700 nm large and mitochon­dria with tubulovesicular, lamellar and circular cristae. Ultra­structural specificity of hybrid tumours were rare microvesi­cles and numerous mitochondria of O-PRCC mitochondria with lamellar cristae and small intracytoplasmic vesicles, 100–200 nm large, and of granular RCC, in addition to mi­tochondria, also glassy hyaline globules (GHG). Conclu­sion. Ultrastructural analysis indicates mitochondria as the dominant organelle in the analysed tumours. Electron mi­croscopy showed specificities, i.e., differences in appearance of cristae, presence and size of vesicles as well as deposition of pigment in and out of cytoplasm and glassy hyaline glob­ules.

References

REFERENCES

Severus L, Johannessen JV. Embedding. Sectioning and Staning. In: Johannessen JV, editor. Electron Microscopy in Human Medicine: Instrumentation and Techniques. New York: McGraw-Hill Intrenational Book Company; 1978. p. 116–84.

Laschi R, Govani E. Staining Methods for Semithin Sections. In: Johannessen JV, editor. Electron Microscopy in Human Medicine: Instrumentation and Techniques. New York: McGraw-Hill Intrenational Book Company; 1978. p. 187–98.

McKenney JK, Tickoo SK, Paner GP. Diagnostic Pathology: Geni-tourinary. 1st ed. Salt Lake City: Amirsys; 2010.

Bostwick DG, Cheng L. Urologic Surgical Pathology. 2nd ed. Philadelhia: Mosby, Elsevier. 2008.

Merino MJ, Eccles DM, Linehan WM, Eble IN, Sauter G, Epstein JI, et al. Tumours of the Urinary System and Male Genital Or-gans. Lyon, France: IARC Press; 2004.

Atanacković M, Bačetić D, Basta-Jovanović G, Begić-Janeva A, Boričić I, Brašanac D, et al. Pathology. Belgrade: Faculty of Medicine, University of Belgrade; 2003. (Serbian)

Kumar V, Abbas AK, Fausto N . Robbins pathologic basis of disease. 7th ed. Philadelphia, Pa: Elsevier Saunders; 2005.

Imada K, Dainichi T, Yokomizo A, Tsunoda T, Song YH, Nagasaki A, et al. Birt-Hogg-Dubé syndrome with clear-cell and onco-cytic renal tumour and trichoblastoma associated with a novel FLCN mutation. Br J Dermatol 2009; 160(6): 1350–3.

Kluijt I, de Jong D, Teertstra HJ, Axwijk PH, Gille JJ, Bell K, et al. Early onset of renal cancer in a family with Birt-Hogg-Dubé syndrome. Clin Genet 2009; 75(6): 537–43.

Murakami T, Sano F, Huang Y, Komiya A, Baba M, Osada Y, et al. Identification and characterization of Birt-Hogg-Dubé as-sociated renal carcinoma. J Pathol 2007; 211(5): 524–31.

Murphy WM, Grignon DJ, Perlman EJ. Tumors of the kidney, bladder and related urinary structures. (AFIP Atlas of Tumor Pathology 4th Series). Washington DC: American Registry of Pathology; 2004.

Delahunt B, Eble JN. Papillary renal cell carcinoma: a clinicopathologic and immunohistochemical study of 105 tumors. Mod Pathol 1997; 10(6): 537–44.

Brunelli M, Eble JN, Zhang S, Martignoni G, Cheng L. Gains of chromosomes 7, 17, 12, 16, and 20 and loss of Y occur early in the evolution of papillary renal cell neoplasia: a fluorescent in situ hybridization study. Mod Pathol 2003; 16(10): 1053–9.

Allory Y, Ouazana D, Boucher E, Thiounn N, Vieillefond A. Papillary renal cell carcinoma. Prognostic value of morphological subtypes in a clinicopathologic study of 43 cases. Virchows Arch 2003; 442(4): 336–42.

Kattar MM, Grignon DJ, Wallis T, Haas GP, Sakr WA, Pontes JE, et al. Clinicopathologic and interphase cytogenetic analysis of papillary (chromophilic) renal cell carcinoma. Mod Pathol 1997; 10(11): 1143–50.

Thoenes W, Störkel S, Rumpelt HJ. Histopathology and classifi-cation of renal cell tumors (adenomas, oncocytomas and carcinomas). The basic cytological and histopathological ele-ments and their use for diagnostics. Pathol Res Pract 1986; 181(2): 125–43.

Pradhan D, Kakkar N, Bal A, Singh S, Joshi K. Sub-typing of renal cell tumours; contribution of ancillary techniques. Diagn Pathol 2009; 4: 21.

Thoenes W, Störkel S, Rumpelt HJ. Human chromophobe cell renal carcinoma. Virchows Arch B Cell Pathol Incl Mol Pathol 1985; 48(3): 207–17.

Michal M, Hes O, Svec A, Ludvíková M. Pigmented microcystic chromophobe cell carcinoma: a unique variant of renal cell carcinoma. Ann Diagn Pathol 1998; 2(3): 149–53.

Hes O, Vanecek T, Perez-Montiel DM, Alvarado Cabrero I, Hora M, Suster S, et al. 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 2005; 446(4): 383–93.

Amin MB, Crotty TB, Tickoo SK, Farrow GM. Renal oncocytoma: a reappraisal of morphologic features with clinicopathologic findings in 80 cases. Am J Surg Pathol 1997; 21(1): 1–12.

Davis CJ, Jr, Sesterhenn IA, Mostofi FK, Ho CK. Renal oncocytoma. Clinicopathological study of 166 patients. J Urogen Pathol 1999; 1: 41–52.

Crotty TB, Farrow GM, Lieber MM. Chromophobe Cell Renal Carcinoma: Clinicopathological Features of 50 Cases. J Urol 1995; 154(3): 964–7

Fuhrman SA, Lasky LC, Limas C. Prognostic significance of morphologic parameters in renal cell carcinoma. Am J Surg Pathol 1982; 6(7): 655–63.

Eble JN, Hull MT. Morphologic features of renal oncocytoma: A light and electron microscopic study. Hum Pathol 1984; 15(11): 1054–61.

Tickoo SK, Lee MW, Eble JN, Amin M, Christopherson T, Zarbo RJ, et al. Ultrastructural Observations on Mitochondria and Microvesicles in Renal Oncocytoma, Chromophobe Renal Cell Carcinoma, and Eosinophilic Variant of Conventional (Clear Cell) Renal Cell Carcinoma. Am J Surg Pathol 2000; 24(9): 1247–56.

Erlandson RA, Shek TW, Reuter VE. Diagnostic Significance of Mitochondria in Four Types of Renal Epithelial Neoplasms: An Ultrastructural Study of 60 Tumors. Ultrastruct Pathol 1997; 21(5): 409–17.

Bugert P, Kovacs G. Molecular differential diagnosis of renal cell carcinomas by microsatellite analysis. Am J Pathol 1996; 149(6): 2081–8.

Bonsib SM, Bray C, Timmerman TG. Renal chromophobe cell carcinoma: limitations of paraffin-embedded tissue. Ultrastruct Pathol 1993; 17(5): 529–36.

Perez-Ordonez B, Hamed G, Campbell S, Erlandson RA, Russo P, Gaudin PB, et al. Renal oncocytoma: a clinicopathologic study of 70 cases. Am J Surg Pathol 1997; 21(8): 871–83.

Maj MN. Hyaline globules. Arch Pathol 1973; 96: 144.

Dekker A, Kraus JR. Hyline globules in human neoplasms. Arch Pathol 1973; 95: 178–81.

Michal M, Havlicek F. Corticomedullary Tumors of the Adrenal Glands: Report of two cases. Assotiation with spindle cell sar-coma. Pathol Res Pract 1996; 192(11): 1082–9.

Ulbright TM, Gersell DJ. Rete testis hyperplasia with hyaline globule formation. A lesion simulating yolk sac tumor. Am J Surg Pathol 1991; 15(1): 66–74.

Jagirdar J, Irie T, French SW, Patil J, Schwarz R, Paronetto F. Glo-bular mallory-like bodies in renal cell carcinoma: Report of a case and review of cytoplasmic eosinophilic globules. Hum Pa-thol 1985; 16(9): 949–52.

Datta BN. Hylineintracytoplasmatic globules in renal carcino-ma. Arch Pathol Lab Med 1977; 101(7): 391.

Barnes CA, Beckman EN. Renal Oncocytoma and Its Congen-ers. Am J Clin Pathol 1983; 79(3): 312–18.

Bonsib SM, Bromley C, Lager D. Renal oncocytoma: diagnostic utility of cytokeratin-containing globular filamentous bodies. Mod Pathol 1991; 4(1): 16–23.

Ghadially FN. Globular filamentous bodies. In: Ghadially FN, editor. Ultrastructural Pathology of the Cell and Matrix. Bos-ton, MA: Butterworth-Heinemann; 1988. p. 906–11.

Gatalica Z, Miettinen M, Kovatich A, McCue PA. Hyaline globules in renal cell carcinomas and oncocytomas. Hum Pathol 1997; 28(4): 400–3.

Michal M, Skálova A. Collagenous Spherulosis: A comment on its histogenesis. Pathol Res Pract 1990; 186(3): 365–70.

Yamaguchi T, Kuroda N, Imamura Y, Hes O, Michal M, Sima R, et al. Imprint cytologic features of chromophobe renal cell carcinoma morphologically resembling renal oncocytoma: Is this an oncocytic variant of chromophobe renal cell carcinoma? Diagn Cytopathol 2010; 38(7): 509–13.

Petersson F, Síma R, Grossmann P, Michal M, Kuroda N, Hora M, et al. Renal small cell oncocytoma with pseudorosettes: A his-tomorphologic, immunohistochemical and molecular genetic study of 10 cases. Hum Pathol 2011; 42(11): 1751–60.

Kuroda N, Tanaka A, Yamaguchi T, Kasahara K, Naruse K, Yama-da Y, et al. Chromophobe renal cell carcinoma, oncocytic va-riant: a proposal of a new variant giving a critical diagnostic pitfall in diagnosing renal oncocytic tumors. Med Mol Mor-phol 2013; 46(1): 49–55.

Bárcena C, Martínez MA, Ortega MP, Muñoz HG, Sárraga GU. Mitochondria with Tubulovesicular Cristae in Renal Oncocy-tomas. Ultrastruct Pathol 2010; 34(6): 315–20.

Kryvenko ON, Jorda M, Argani P, Epstein JI. Diagnostic Ap-proach to Eosinophilic Renal Neoplasms. Arch Pathol Lab Med 2014; 38(11): 1531–41.

Yamaguchi T, Hirota E, Kuroda N. Chromophobe renal cell car-cinoma, oncocytic variant: Cytological and ultrastructural ob-servations. J Cytol 2015; 32(3): 184.

Published
2021/04/21
Section
Original Paper