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Biphasic papillary (biphasic squamoid alveolar) renal cell carcinoma: a clinicopathologic and molecular study of 17 renal cell carcinomas including 10 papillary adenomas

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Abstract

Biphasic papillary renal cell carcinoma (synonymous with biphasic squamoid alveolar renal cell carcinoma) is considered within the spectrum of papillary renal cell carcinoma (PRCC). With < 70 reported cases of biphasic PRCC, there is limited data on the pathologic spectrum and clinical course. Seventeen biphasic PRCC cases and 10 papillary adenomas with similar biphasic morphology were assessed. The mean age of the biphasic PRCC patients was 62 years (male to female ratio of 1.8:1), from 10 partial nephrectomies, 6 radical nephrectomies, and 1 biopsy. The mean tumor size was 3.6 cm (range 1.6-8 cm), with 24% showing multifocality. Fifteen out of 17 cases were limited to the kidney (one of which was staged as pT2a but had lung metastases at diagnosis) and 2/17 cases were staged as T3a. All tumors showed typical biphasic morphology with an extent of squamoid foci widely variable from 10 to 95%. Emperipolesis was identified in 88% of cases. All biphasic PRCC tested exhibited positivity for PAX8 (16/16), keratin 7 (17/17), EMA (15/15), AMACR (17/17), and vimentin (12/12) in both large and small cells; cyclin D1 was only expressed in the large cells (16/16). The 10 papillary adenomas showed a similar immunoprofile to biphasic PRCC. NGS testing performed on 13 biphasic PRCC revealed 4 (31%) harboring MET SNVs. In 1/5 (20%) papillary adenomas, a pathogenic MET SNV was identified. Biphasic PRCC is rare with a generally similar immunoprofile to “type 1” PRCC but with notable strong positivity for cyclin D1 in the large cell component. Although most of the biphasic PRCC cases were of small size, low stage, and with an indolent behavior, one patient had metastatic disease and one patient died of the disease.

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Data availability

The data generated in this study are available from the corresponding author upon request.

References

  1. Amin MB, Gill AJ, Hartmann A et al (2022) Tumours of the kidney. In: WHO Classification of Tumours Editorial Board (ed) Urinary and Male Genital Tumours, 5th edn. International Agency for Research on Cancer. Lyon, France, pp 31–129

  2. Trpkov K, Hes O (2019) New and emerging renal entities: a perspective post-WHO 2016 classification. Histopathology 74:31–59

    Article  PubMed  Google Scholar 

  3. Trpkov K, Hes O, Williamson SR et al (2021) New developments in existing WHO entities and evolving molecular concepts: The genitourinary pathology society (GUPS) update on renal neoplasia. Mod Pathol 34:1392–1424

    Article  PubMed  Google Scholar 

  4. Hes O, Condom Mundo E, Peckova K et al (2016) Biphasic squamoid alveolar renal cell carcinoma: a distinctive subtype of papillary renal cell carcinoma? Am J Surg Pathol 40:664–675

    Article  PubMed  Google Scholar 

  5. Petersson F, Bulimbasic S, Hes O et al (2012) Biphasic alveolosquamoid renal carcinoma: a histomorphological, immunohistochemical, molecular genetic, and ultrastructural study of a distinctive morphologic variant of renal cell carcinoma. Ann Diagn Pathol 16:459–469

    Article  PubMed  Google Scholar 

  6. Zhou L, Xu H, Zhou Y et al (2019) Biphasic squamoid alveolar renal carcinoma with positive CD57 expression: A clinicopathologic study of three cases. Pathol Int 69:519–525

    Article  CAS  PubMed  Google Scholar 

  7. Chartier S, Méjean A, Richard S, Thiounn N, Vasiliu V, Verkarre V (2017) Biphasic squamoid alveolar renal cell carcinoma: 2 cases in a family supporting a continuous spectrum with papillary type I renal cell carcinoma. Am J Surg Pathol 41:1011–1012

    Article  PubMed  Google Scholar 

  8. Zhang X, Tretiakova M (2021) Biphasic squamoid alveolar renal cell carcinoma of the kidney involved by atypical CD5-positive B-cells. Int J Surg Pathol 29:427–432

    Article  CAS  PubMed  Google Scholar 

  9. Zhang Y, Xu Y, Yu T, Chen J, Zhao M, Lin C (2022) Biphasic squamoid alveolar renal cell carcinoma: description of a rare case and a literature analysis. Quant Imaging Med Surg 12:3987–3994

    Article  PubMed  PubMed Central  Google Scholar 

  10. Sherin SB, Gunabooshanam B, Sundaram S, D’ Cruze L (2023) Biphasic squamoid alveolar renal cell carcinoma: A rare entity with an even rarer presentation as cutaneous metastases - A case report. Indian J Pathol Microbiol 66:174–176

    Article  PubMed  Google Scholar 

  11. Lopez JI (2016) Case Report: Multifocal biphasic squamoid alveolar renal cell carcinoma. F1000Research 5:607

    Article  PubMed  PubMed Central  Google Scholar 

  12. Troxell ML, Higgins JP (2016) Renal cell carcinoma in kidney allografts: histologic types, including biphasic papillary carcinoma. Hum Pathol 57:28–36

    Article  CAS  PubMed  Google Scholar 

  13. Suárez-Vilela D, Izquierdo FM, Méndez-Álvarez JR, Velasco-Alonso J (2018) The squamoid cells in biphasic squamoid alveolar renal carcinoma present cytophagocytosis (Not Emperipolesis) of apoptotic neutrophilic granulocytes. Am J Surg Pathol 42:420–422

    Article  PubMed  Google Scholar 

  14. Trpkov K, Athanazio D, Magi-Galluzzi C et al (2018) Biphasic papillary renal cell carcinoma is a rare morphological variant with frequent multifocality: a study of 28 cases. Histopathology 72:777–785

    Article  PubMed  Google Scholar 

  15. Denize T, Just PA, Sibony M et al (2021) MET alterations in biphasic squamoid alveolar papillary renal cell carcinomas and clinicopathological features. Mod Pathol 34:647–659

    Article  CAS  PubMed  Google Scholar 

  16. Lobo J, Ohashi R, Amin MB et al (2022) WHO 2022 landscape of papillary and chromophobe renal cell carcinoma. Histopathology 81:426–438

    Article  PubMed  Google Scholar 

  17. Rini BI, McKiernan JM, Chang SS et al (2017) Kidney. In: Amin MB, Edge SB, Greene FL et al (eds) AJCC Cancer Staging Manual, 8th edn. Springer, Chicago, IL, pp 747–756

    Google Scholar 

  18. Delahunt B, Cheville JC, Martignoni G et al (2013) The International Society of Urological Pathology (ISUP) grading system for renal cell carcinoma and other prognostic parameters. Am J Surg Pathol 37:1490–1504

    Article  PubMed  Google Scholar 

  19. Albiges L, Guegan J, Le Formal A et al (2014) MET is a potential target across all papillary renal cell carcinomas: result from a large molecular study of pRCC with CGH array and matching gene expression array. Clin Cancer Res 20:3411–3421

    Article  CAS  PubMed  Google Scholar 

  20. Durinck S, Stawiski EW, Pavía-Jiménez A et al (2015) Spectrum of diverse genomic alterations define non-clear cell renal carcinoma subtypes. Nat Genet 47:13–21

    Article  CAS  PubMed  Google Scholar 

  21. Mantoan Padilha M, Billis A, Allende D, Zhou M, Magi-Galluzzi C (2013) Metanephric adenoma and solid variant of papillary renal cell carcinoma: common and distinctive features. Histopathology 62:941–953

    Article  PubMed  Google Scholar 

  22. Ulamec M, Skenderi F, Trpkov K et al (2016) Solid papillary renal cell carcinoma: clinicopathologic, morphologic, and immunohistochemical analysis of 10 cases and review of the literature. Ann Diagn Pathol 23:51–57

    Article  PubMed  Google Scholar 

  23. Renshaw AA, Zhang H, Corless CL, Fletcher JA, Pins MR (1997) Solid variants of papillary (chromophil) renal cell carcinoma: clinicopathologic and genetic features. Am J Surg Pathol 21:1203–1209

    Article  CAS  PubMed  Google Scholar 

  24. Tickoo SK (2016) Papillary renal cell carcinoma. In: Tickoo SK, Chen Y-B, Zynger DL (eds) Biopsy interpretation of the kidney and adrenal gland. Wolters Kluwer, Philadelphia, PA, pp 43–55

    Google Scholar 

  25. Williamson SR, Kum JB, Goheen MP, Cheng L, Grignon DJ, Idrees MT (2014) Clear cell renal cell carcinoma with a syncytial-type multinucleated giant tumor cell component: implications for differential diagnosis. Hum Pathol 45:735–744

    Article  CAS  PubMed  Google Scholar 

  26. Nova-Camacho LM, Sangoi AR (2023) Clear cell renal cell carcinoma with syncytial-type multinucleated giant tumor cells: A clinicopathologic study of 14 cases [published online ahead of print, 2023 Jul 31]. Int J Surg Pathol. https://doi.org/10.1177/10668969231189798

    Article  PubMed  Google Scholar 

  27. Balint I, Szponar A, Jauch A, Kovacs G (2009) Trisomy 7 and 17 mark papillary renal cell tumours irrespectively of variation of the phenotype. J Clin Pathol 62:892–895

    Article  CAS  PubMed  Google Scholar 

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Authors and Affiliations

  1. Department of Pathology, Donostia University Hospital, San Sebastian, Spain

    Luiz M. Nova-Camacho, Andrea Val-Carreres, Maialen Martin-Arruti & Irune Ruiz

  2. Department of Pathology, Indiana University, Indianapolis, IN, USA

    Andres M. Acosta

  3. Department of Pathology and Laboratory Medicine, Albany Medical Center, Albany, NY, USA

    Mahmut Akgul

  4. Department of Pathology, University Hospital of Navarra, Pamplona, Spain

    Angel Panizo & David Guerrero-Setas

  5. Department of Anatomical Pathology, Sonic Healthcare, Melbourne PathologyVictoria, Australia

    Laurence A. Galea

  6. Department of Internal Medicine, Diagnósticos da America DASA, Sao Paulo, Brazil

    Juan A. Talavera

  7. Laboratory of Molecular Pathology and Therapeutic Targets, Donostia University Hospital, San Sebastian, Spain

    Maialen Martin-Arruti & Irune Ruiz

  8. Department of Pathology, Gregorio Marañon University Hospital, Madrid, Spain

    María García-Martos

  9. Department of Pathology, Stanford University, Stanford, CA, USA

    Ankur R. Sangoi

  10. Gainesville, USA

    Luiz M. Nova-Camacho

Authors
  1. Luiz M. Nova-Camacho
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  12. Ankur R. Sangoi
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Contributions

Concept, design, and coordination: L.M.N.C., A.R.S.; contribution of cases: L.M.N.C., M.A., A.P., L.A.G., M.G.M., and A.R.S.; histopathological evaluation: L.M.N.C., M.A., A.P., L.A.G., A.V.C., M.G.M., and A.R.S.; molecular evaluation: D.G.S., M.M.A., and I.R.; analysis of clinical, histopathologic, and molecular data: L.M.N.C., A.M.A., D.G.S., J.A.T., M.M.A., and A.R.S.; manuscript draft: L.M.N.C., A.M.A., A.R.S.; intellectual contributions: all authors; editing and approval of the manuscript: all authors.

Corresponding author

Correspondence to Luiz M. Nova-Camacho.

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Retrospective study not interfering with diagnosis and patient management.

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Nova-Camacho, L.M., Acosta, A.M., Akgul, M. et al. Biphasic papillary (biphasic squamoid alveolar) renal cell carcinoma: a clinicopathologic and molecular study of 17 renal cell carcinomas including 10 papillary adenomas. Virchows Arch 484, 441–449 (2024). https://doi.org/10.1007/s00428-024-03768-x

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  • DOI: https://doi.org/10.1007/s00428-024-03768-x

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