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The Tumor Entity Denominated “clear cell-papillary renal cell carcinoma” According to the WHO 2016 new Classification, have the Clinical Characters of a Renal Cell Adenoma as does Harbor a Benign Outcome

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Pathology & Oncology Research

Abstract

The new WHO 2016 classification of renal neoplasia encounters the new entity called “clear cell papillary renal cell carcinoma” (ccpRCC). The ccpRCC has been long included as a subtype of clear cell RCC histotype and it actually ranges from 2 to 9% in different routinely available cohort of renal carcinomas. Of important note, ccpRCC does not show any recurrences or metastases or lymph-node invasion and the outcome is always good. We reviewed twenty-four publications with available follow-up for patients (no. 362) affected by clear cell papillary RCCs/renal adenomatoid tumours and notably ccpRCC harbors an indolent clinical behavior after a mean of 38 months (3,5 years) of follow-up. This paper reviews the histological, molecular and clinical features characterizing ccpRCC, with the goal of focusing the knowledge of the benign fashion of this new tumour entity, supporting the idea of a new renal cell adenoma recruited morphologically from ex conventional clear cell RCC tumours.

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References

  1. Moch H, Humphrey PA, Ulbright TM, Reuter VE (2016) WHO classification of Tumours of the urinary system and male genital organs (IARC WHO classification of Tumours). IARC, Lyon

    Google Scholar 

  2. Srigley JR, Delahunt B, Eble JN, Egevad L, Epstein JI, Grignon D, Hes O, Moch H, Montironi R, Tickoo SK, Zhou M, Argani P (2013) The International Society of Urological Pathology (ISUP) Vancouver classification of renal Neoplasia. Am J Surg Pathol 37(10):1469–1489. doi:10.1097/PAS.0b013e318299f2d1

    Article  PubMed  Google Scholar 

  3. Tickoo SK, dePeralta-Venturina MN, Harik LR, Worcester HD, Salama ME, Young AN, Moch H, Amin MB (2006) Spectrum of epithelial neoplasms in end-stage renal disease: an experience from 66 tumor-bearing kidneys with emphasis on histologic patterns distinct from those in sporadic adult renal neoplasia. Am J Surg Pathol 30(2):141–153

    Article  PubMed  Google Scholar 

  4. Aron M, Chang E, Herrera L, Hes O, Hirsch MS, Comperat E, Camparo P, Rao P, Picken M, Michal M, Montironi R, Tamboli P, Monzon F, Amin MB (2015) Clear cell-papillary renal cell carcinoma of the kidney not associated with end-stage renal disease: clinicopathologic correlation with expanded immunophenotypic and molecular characterization of a large cohort with emphasis on relationship with renal angiomyoadenomatous tumor. Am J Surg Pathol 39(7):873–888. doi:10.1097/PAS.0000000000000446

    Article  PubMed  Google Scholar 

  5. Adam J, Couturier J, Molinie V, Vieillefond A, Sibony M (2011) Clear-cell papillary renal cell carcinoma: 24 cases of a distinct low-grade renal tumour and a comparative genomic hybridization array study of seven cases. Histopathology 58(7):1064–1071. doi:10.1111/j.1365-2559.2011.03857.x

    Article  PubMed  Google Scholar 

  6. Gobbo S, Eble JN, Grignon DJ, Martignoni G, MacLennan GT, Shah RB, Zhang S, Brunelli M, Cheng L (2008) Clear cell papillary renal cell carcinoma: a distinct histopathologic and molecular genetic entity. Am J Surg Pathol 32(8):1239–1245. doi:10.1097/PAS.0b013e318164bcbb

    Article  PubMed  Google Scholar 

  7. Williamson SR, Zhang S, Eble JN, Grignon DJ, Martignoni G, Brunelli M, Wang M, Gobbo S, Baldridge LA, Cheng L (2013) Clear cell papillary renal cell carcinoma-like tumors in patients with von Hippel-Lindau disease are unrelated to sporadic clear cell papillary renal cell carcinoma. Am J Surg Pathol 37(8):1131–1139. doi:10.1097/PAS.0b013e318282dab8

    Article  PubMed  Google Scholar 

  8. Aydin H, Chen L, Cheng L, Vaziri S, He H, Ganapathi R, Delahunt B, Magi-Galluzzi C, Zhou M (2010) Clear cell tubulopapillary renal cell carcinoma: a study of 36 distinctive low-grade epithelial tumors of the kidney. Am J Surg Pathol 34(11):1608–1621. doi:10.1097/PAS.0b013e3181f2ee0b

    Article  PubMed  Google Scholar 

  9. Park JH, Lee C, Suh JH, Moon KC (2012) Clear cell papillary renal cell carcinoma: a report of 15 cases including three cases of concurrent other-type renal cell carcinomas. Korean J of Pathol 46(6):541–547. doi:10.4132/Korean JPathol.2012.46.6.541

    Article  Google Scholar 

  10. Williamson SR, Eble JN, Cheng L, Grignon DJ (2013) Clear cell papillary renal cell carcinoma: differential diagnosis and extended immunohistochemical profile. Mod Pathol: Official J of the United States Canadian Acad Pathol Inc 26(5):697–708. doi:10.1038/modpathol.2012.204

    Article  CAS  Google Scholar 

  11. Mai KT, Kohler DM, Belanger EC, Robertson SJ, Wang D (2008) Sporadic clear cell renal cell carcinoma with diffuse cytokeratin 7 immunoreactivity. Pathology 40(5):481–486. doi:10.1080/00313020802197962

    Article  PubMed  CAS  Google Scholar 

  12. Zhou H, Zheng S, Truong LD, Ro JY, Ayala AG, Shen SS (2014) Clear cell papillary renal cell carcinoma is the fourth most common histologic type of renal cell carcinoma in 290 consecutive nephrectomies for renal cell carcinoma. Hum Pathol 45(1):59–64. doi:10.1016/j.humpath.2013.08.004

    Article  PubMed  Google Scholar 

  13. Gill S, Kauffman EC, Kandel S, George S, Schwaab T, Xu B (2015) Incidence of clear cell papillary renal cell carcinoma in low-grade renal cell carcinoma cases: a 12-year retrospective Clinicopathologic study from a single cancer center. Int J Surg Pathol. doi:10.1177/1066896915613432

  14. Alexiev BA, Thomas C, Zou YS (2014) Clear cell papillary renal cell carcinoma with angiomyomatous stroma: a histological, immunohistochemical, and fluorescence in situ hybridization study. Virchows Archiv: Intern J Pathol 464(6):709–716. doi:10.1007/s00428-014-1581-y

    Article  CAS  Google Scholar 

  15. Bhatnagar R, Alexiev BA (2012) Renal-cell carcinomas in end-stage kidneys: a clinicopathological study with emphasis on clear-cell papillary renal-cell carcinoma and acquired cystic kidney disease-associated carcinoma. Int J Surg Pathol 20(1):19–28. doi:10.1177/1066896911414273

    Article  PubMed  Google Scholar 

  16. Alexiev BA, Drachenberg CB (2014) Clear cell papillary renal cell carcinoma: incidence, morphological features, immunohistochemical profile, and biologic behavior: a single institution study. Pathol Res Pract 210(4):234–241. doi:10.1016/j.prp.2013.12.009

    Article  PubMed  CAS  Google Scholar 

  17. Shi SS, Shen Q, Xia QY, Tu P, Shi QL, Zhou XJ, Rao Q (2013) Clear cell papillary renal cell carcinoma: a clinicopathological study emphasizing ultrastructural features and cytogenetic heterogeneity. Int J Clin Exp Pathol 6(12):2936–2942

    PubMed  PubMed Central  Google Scholar 

  18. Behdad A, Monzon F, Hes O, Michal M, Comperat E, Camparo P, Rao P, Picken M, Montironi R, Annaiah C, Herrera L, Arora K, Westfall DE, Tamboli P, Amin M (2011) Relationship between sporadic clear cell-papillary renal cell carcinoma (CP-RCC) and renal angiomyoadenomatous tumor (RAT) of the kidney: analysis by virtual karyotyping, fluorescent in situ analysis and immunohistochemistry (IHC). Modern pathology: an official journal of the United States and Canadian Academy of Pathology, Inc 24(Suppl):179A

  19. Rohan SM, Xiao Y, Liang Y, Dudas ME, Al-Ahmadie HA, Fine SW, Gopalan A, Reuter VE, Rosenblum MK, Russo P, Tickoo SK (2011) Clear-cell papillary renal cell carcinoma: molecular and immunohistochemical analysis with emphasis on the von Hippel-Lindau gene and hypoxia-inducible factor pathway-related proteins. Mod Pathol: Official J of the United States Canadian Acad Pathol Inc 24(9):1207–1220. doi:10.1038/modpathol.2011.80

    Article  CAS  Google Scholar 

  20. Leroy X, Camparo P, Gnemmi V, Aubert S, Flamand V, Roupret M, Fantoni JC, Comperat E (2014) Clear cell papillary renal cell carcinoma is an indolent and low-grade neoplasm with overexpression of cyclin-D1. Histopathology 64(7):1032–1036. doi:10.1111/his.12359

    Article  PubMed  Google Scholar 

  21. Yan WX, Cao WR, Zhao J, Zhang W, Wang XL, Yuan Q, Dang SQ (2015) Clear cell papillary renal cell carcinoma: a clinicopathologic analysis of 6 cases. Int J Clin Exp Pathol 8(5):4595–4599

    PubMed  PubMed Central  CAS  Google Scholar 

  22. Michal M, Hes O, Havlicek F (2000) Benign renal angiomyoadenomatous tumor: a previously unreported renal tumor. Ann Diagn Pathol 4(5):311–315. doi:10.1053/adpa.2000.17890

    Article  PubMed  CAS  Google Scholar 

  23. Singh C, Kendi AT, Manivel JC, Pambuccian SE (2012) Renal angiomyoadenomatous tumor. Ann Diagn Pathol 16(6):470–476. doi:10.1016/j.anndiagpath.2012.01.006

    Article  PubMed  Google Scholar 

  24. Kuroda N, Michal M, Hes O, Taguchi T, Tominaga A, Mizobuchi K, Ohe C, Sakaida N, Uemura Y, Shuin T, Lee GH (2009) Renal angiomyoadenomatous tumor: fluorescence in situ hybridization. Pathol Int 59(9):689–691. doi:10.1111/j.1440-1827.2009.02429.x

    Article  PubMed  Google Scholar 

  25. Michal M, Hes O, Nemcova J, Sima R, Kuroda N, Bulimbasic S, Franco M, Sakaida N, Danis D, Kazakov DV, Ohe C, Hora M (2009) Renal angiomyoadenomatous tumor: morphologic, immunohistochemical, and molecular genetic study of a distinct entity. Virchows Archiv: Intern J Pathol 454(1):89–99. doi:10.1007/s00428-008-0697-3

    Article  CAS  Google Scholar 

  26. Deml KF, Schildhaus HU, Comperat E, von Teichman A, Storz M, Schraml P, Bonventre JV, Fend F, Fleige B, Nerlich A, Gabbert HE, GaBler N, Grobholz R, Hailemariam S, Hinze R, Knuchel R, Lhermitte B, Nesi G, Rudiger T, Sauter G, Moch H (2015) Clear cell papillary renal cell carcinoma and renal angiomyoadenomatous tumor: two variants of a morphologic, immunohistochemical, and genetic distinct entity of renal cell carcinoma. Am J Surg Pathol 39(7):889–901. doi:10.1097/PAS.0000000000000456

    Article  PubMed  PubMed Central  Google Scholar 

  27. Fisher KE, Yin-Goen Q, Alexis D, Sirintrapun JS, Harrison W, Benjamin Isett R, Rossi MR, Moreno CS, Young AN, Osunkoya AO (2014) Gene expression profiling of clear cell papillary renal cell carcinoma: comparison with clear cell renal cell carcinoma and papillary renal cell carcinoma. Mod Pathol 27(2):222–230. doi:10.1038/modpathol.2013.140

    Article  PubMed  CAS  Google Scholar 

  28. Wolfe A, Dobin SM, Grossmann P, Michal M, Donner LR (2011) Clonal trisomies 7,10 and 12, normal 3p and absence of VHL gene mutation in a clear cell tubulopapillary carcinoma of the kidney. Virchows Archiv: Intern J Pathol 459(4):457–463. doi:10.1007/s00428-011-1137-3

    Article  Google Scholar 

  29. Rao P, Monzon F, Jonasch E, Matin SF, Tamboli P (2014) Clear cell papillary renal cell carcinoma in patients with von Hippel-Lindau syndrome--clinicopathological features and comparative genomic analysis of 3 cases. Hum Pathol 45(9):1966–1972. doi:10.1016/j.humpath.2014.06.004

    Article  PubMed  CAS  Google Scholar 

  30. Lawrie CH, Larrea E, Larrinaga G, Goicoechea I, Arestin M, Fernandez-Mercado M, Hes O, Caceres F, Manterola L, Lopez JI (2014) Targeted next-generation sequencing and non-coding RNA expression analysis of clear cell papillary renal cell carcinoma suggests distinct pathological mechanisms from other renal tumour subtypes. J Pathol 232(1):32–42. doi:10.1002/path.4296

    Article  PubMed  CAS  Google Scholar 

  31. Raspollini MR, Castiglione F, Cheng L, Montironi R, Lopez-Beltran A (2016) Genetic mutations in accordance with a low malignant potential tumour are not demonstrated in clear cell papillary renal cell carcinoma. J Clin Pathol. doi:10.1136/jclinpath-2015-203565

  32. Munari E, Marchionni L, Chitre A, Hayashi M, Martignoni G, Brunelli M, Gobbo S, Argani P, Allaf M, Hoque MO, Netto GJ (2014) Clear cell papillary renal cell carcinoma: micro-RNA expression profiling and comparison with clear cell renal cell carcinoma and papillary renal cell carcinoma. Hum Pathol 45(6):1130–1138. doi:10.1016/j.humpath.2014.01.013

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  33. Dhakal HP, McKenney JK, Khor LY, Reynolds JP, Magi-Galluzzi C, Przybycin CG (2016) Renal neoplasms with overlapping features of clear cell renal cell carcinoma and clear cell papillary renal cell carcinoma: a Clinicopathologic study of 37 cases from a single institution. Am J Surg Pathol 40(2):141–154. doi:10.1097/PAS.0000000000000583

    Article  PubMed  Google Scholar 

  34. Gobbo S, Eble JN, Maclennan GT, Grignon DJ, Shah RB, Zhang S, Martignoni G, Brunelli M, Cheng L (2008) Renal cell carcinomas with papillary architecture and clear cell components: the utility of immunohistochemical and cytogenetical analyses in differential diagnosis. Am J Surg Pathol 32(12):1780–1786. doi:10.1097/PAS.0b013e31818649ed

    Article  PubMed  Google Scholar 

  35. Kuhn E, De Anda J, Manoni S, Netto G, Rosai J (2006) Renal cell carcinoma associated with prominent angioleiomyoma-like proliferation: report of 5 cases and review of the literature. Am J Surg Pathol 30(11):1372–1381. doi:10.1097/01.pas.0000213277.45715.82

    Article  PubMed  Google Scholar 

  36. Shannon BA, Cohen RJ, Segal A, Baker EG, Murch AR (2009) Clear cell renal cell carcinoma with smooth muscle stroma. Hum Pathol 40(3):425–429. doi:10.1016/j.humpath.2008.05.021

    Article  PubMed  Google Scholar 

  37. Iczkowski KA, Shanks JH, Burdge AH, Cheng L (2013) Renal cell carcinoma with clear cells, smooth muscle stroma, and negative for 3p deletion: a variant of renal angiomyoadenomatous tumour? A case report. Histopathology 62(3):522–524. doi:10.1111/his.12040

    Article  PubMed  Google Scholar 

  38. Martignoni G, Brunelli M, Segala D, Gobbo S, Borze I, Atanesyan L, Savola S, Barzon L, Masi G, Tardanico R, Zhang S, Eble JN, Chilosi M, Bohling T, Cheng L, Delahunt B, Knuutila S (2014) Renal cell carcinoma with smooth muscle stroma lacks chromosome 3p and VHL alterations. Mod Pathol: Official J of the United States Canadian Acad Pathol Inc 27(5):765–774. doi:10.1038/modpathol.2013.180

    Article  CAS  Google Scholar 

  39. Canzonieri V, Volpe R, Gloghini A, Carbone A, Merlo A (1993) Mixed renal tumor with carcinomatous and fibroleiomyomatous components, associated with angiomyolipoma in the same kidney. Pathol Res Pract 189(8):951–956; discussion 957-959. doi:10.1016/S0344-0338(11)81110-6

    Article  PubMed  CAS  Google Scholar 

  40. Hakimi AA, Tickoo SK, Jacobsen A, Sarungbam J, Sfakianos JP, Sato Y, Morikawa T, Kume H, Fukayama M, Homma Y, Chen YB, Sankin AI, Mano R, Coleman JA, Russo P, Ogawa S, Sander C, Hsieh JJ, Reuter VE (2015) TCEB1-mutated renal cell carcinoma: a distinct genomic and morphological subtype. Mod Pathol: Official J of the United States Canadian Acad Pathol Inc 28(6):845–853. doi:10.1038/modpathol.2015.6

    Article  CAS  Google Scholar 

  41. Diolombi ML, Cheng L, Argani P, Epstein JI (2015) Do clear cell papillary renal cell carcinomas have malignant potential? Am J Surg Pathol 39(12):1621–1634. doi:10.1097/PAS.0000000000000513

    Article  PubMed  Google Scholar 

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Acknowledgements

This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.

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Authors and Affiliations

  1. Division of Oncology, S.Orsola-Malpighi Hospital, Bologna, Italy

    Francesco Massari & Andrea Ardizzoni

  2. Division of Oncology, AOUI, University of Verona, Verona, Italy

    Chiara Ciccarese, Roberto Iacovelli & Giampaolo Tortora

  3. Department of Pathology, Faculty of Medicine in Plzen, Charles University, Pilsen, Czech Republic

    Ondrej Hes & Michal Michal

  4. Department of Diagnostics and Public Health, AOUI, University of Verona, Verona, Italy

    Anna Caliò, Luca Cima, Guido Martignoni & Matteo Brunelli

  5. Department of Pathology, S.Orsola-Malpighi Hospital, Bologna, Italy

    Michelangelo Fiorentino & Francesca Giunchi

  6. Anatomic Pathology, Card. G. Panico Hospital, Tricase, Lecce, Italy

    Alessandro D’Amuri

  7. Department of Pathology, University of Foggia, Foggia, Italy

    Francesca Sanguedolce

  8. Department of Oncology, Hematology & Respiratory Diseases, University of Modena & Reggio Emilia, Modena, Italy

    Roberto Sabbatini & Annalisa Guida

  9. Division of Oncology, I.R.C.C.S. San Matteo University Hospital Foundation, Pavia, Italy

    Camillo Porta

  10. Division of Oncology, Institute for Cancer Research and Treatment, Asl Cn2 Alba-, Bra, Piemonte, Italy

    Cinzia Ortega

  11. Urology Clinic, Carreggi Hospital, University of Florence, Florence, Italy

    Alberto Lapini

  12. Anatomic Pathology, Pederzoli Hospital, Peschiera del Garda, Verona, Italy

    Guido Martignoni

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  1. Francesco Massari
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  2. Chiara Ciccarese
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  3. Ondrej Hes
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  4. Michal Michal
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Correspondence to Matteo Brunelli.

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Francesco Massari and Chiara Ciccarese co-authored as first.

Guido Martignoni and Matteo Brunelli are seniorship coauthor.

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Massari, F., Ciccarese, C., Hes, O. et al. The Tumor Entity Denominated “clear cell-papillary renal cell carcinoma” According to the WHO 2016 new Classification, have the Clinical Characters of a Renal Cell Adenoma as does Harbor a Benign Outcome. Pathol. Oncol. Res. 24, 447–456 (2018). https://doi.org/10.1007/s12253-017-0271-x

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