Advertisement

Pathology & Oncology Research

, Volume 23, Issue 3, pp 689–698 | Cite as

Prognostic Factors for Renal Cell Carcinoma Subtypes Diagnosed According to the 2016 WHO Renal Tumor Classification: a Study Involving 928 Patients

  • Levente Kuthi
  • Alex Jenei
  • Adrienn Hajdu
  • István Németh
  • Zoltán Varga
  • Zoltán Bajory
  • László Pajor
  • Béla Iványi
Original Article

Abstract

The morphotype and grade of renal cell carcinoma (RCC) in 928 nephrectomies were reclassified according to the 2016 WHO classification in order to analyze the distribution and outcomes of RCC subtypes in Hungary, to assess whether microscopic tumor necrosis is an independent prognostic factor in clear cell RCC, and to study whether a two-tiered grading (low/high) for clear cell and papillary RCC provides similar prognostic information to that of the four-tiered ISUP grading system. 83.4% of the cohort were clear cell, 6.9% papillary, 4.5% chromophobe, 2.3% unclassified, 1.1% Xp11 translocation, 1.1% clear cell papillary, 0.3% collecting duct and 0.1% mucinous tubular and spindle cell RCCs. RCC occurred in 16 patients with end-stage kidney disease and none of them displayed features of acquired cystic kidney disease-associated RCC. The 5-year survival rates were as follows: chromophobe 100%, clear cell papillary 100%, clear cell low-grade 96%, papillary type 1 92%, clear cell high-grade 63%, papillary type 2 65%, unclassified 46%, Xp11 translocation 20%, and collecting duct 0%. The 5-year survival rates in low-grade and high-grade papillary RCC were 95% and 59%, respectively. In clear cell RCC, only the grade, the stage and the positive surgical margin proved to be independent prognostic factors statistically. Overall, papillary RCC occurred relatively infrequently; microscopic tumor necrosis in clear cell RCC did not predict the outcome independently of the tumor grading; and the assignment of clear cell and papillary RCCs into low-grade or high-grade tumors was in terms of survival no worse than the ISUP grading.

Keywords

Renal cell carcinoma ISUP grading Microscopic tumor necrosis Survival rates Prognostic factors 

Notes

Acknowledgment

This study was supported by TÁMOP-4.2.2. A-11/1/KONV-2012-0. Earlier, some findings of the study were presented in a shortened form at the European Congress of Pathology, in Belgrade, Serbia, 2015

References

  1. 1.
    Moch H, Humphrey PA, Ulbright TM, Reuter VE (2016) WHO classification Tumours of the urinary system and male genital organs. International Agency for Research on Cancer, LyonGoogle Scholar
  2. 2.
    Srigley JR, Delahunt B, Eble JN et al (2013) The International Society of Urological Pathology (ISUP) Vancouver classification of renal neoplasia. Am J Surg Pathol 37:1469–1489CrossRefPubMedGoogle Scholar
  3. 3.
    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 37:1490–1504CrossRefPubMedGoogle Scholar
  4. 4.
    Reuter VE, Argani P, Zhou M, Delahunt B, Members of the ISUP Immunohistochemistry in Diagnostic Urologic Pathology Group (2014) Best practices recommendations in the application of immunohistochemistry in the kidney tumors: report from the International Society of Urologic Pathology consensus conference. Am J Surg Pathol 38:e35–e49PubMedGoogle Scholar
  5. 5.
    Steffens S, Janssen M, Ross FC et al (2014) The Fuhrman grading system has no prognostic value in patients with nonsarcomatoid chromophobe renal cell carcinoma. Hum Pathol 45:2411–2416CrossRefPubMedGoogle Scholar
  6. 6.
    Delahunt B, McKenney JK, Lohse CM, Leibovich BC, Thompson RH, Boorjian SA, Cheville JC (2013) A novel grading system for clear cell renal cell carcinoma incorporating tumor necrosis. Am J Surg Pathol 37:311–322CrossRefPubMedGoogle Scholar
  7. 7.
    Tan PH, Cheng L, Rioux-Leclercq N et al (2013) Renal tumors: diagnostic and prognostic biomarkers. Am J Surg Pathol 37:1518–1531CrossRefPubMedPubMedCentralGoogle Scholar
  8. 8.
    Genega EM, Ghebremichael M, Najarian R et al (2010) Carbonic anhydrase IX expression in renal neoplasms: correlation with tumor type and grade. Am J Clin Pathol 134:873–879CrossRefPubMedPubMedCentralGoogle Scholar
  9. 9.
    Gupta R, Billis A, Shah RB et al (2012) Carcinoma of the collecting ducts of Bellini and renal medullary carcinoma: clinicopathologic analysis of 52 cases of rare aggressive subtypes of renal cell carcinoma with a focus on their interrelationship. Am J Surg Pathol 36:1265–1278CrossRefPubMedGoogle Scholar
  10. 10.
    Williamson SR, Cheng L (2016) Clear cell renal cell tumors: not all that is “clear” is cancer. Urol Oncol 34:292.e17–292.e22CrossRefGoogle Scholar
  11. 11.
    Sobin LH, Gospodarowicz MK, Wittekind C (2009) TNM classification of malignant tumors, 7th edn. Wiley-Blackwell, OxfordGoogle Scholar
  12. 12.
    Tarabeia J, Kaluski DN, Barchana M, Dichtiar R, Green MS (2010) Renal cell cancer in Israel: sex and ethnic differences in incidence and mortality, 1980-2004. Cancer Epidemiol 34:226–231CrossRefPubMedGoogle Scholar
  13. 13.
    Lipworth L, Morgans AK, Edwards TL et al (2016) Renal cell cancer histologic subtype distribution differs by race and sex. BJU Int 117:260–265CrossRefPubMedGoogle Scholar
  14. 14.
    Pichler M, Hutterer GC, Chromecki TF, Jesche J, Kampel-Kettner K, Pummer K, Zigeuner R (2012) Renal cell carcinoma stage migration in a single European Centre over 25 years: effects on 5- and 10-year metastasis-free survival. Int Urol Nephrol 44:997–1004CrossRefPubMedGoogle Scholar
  15. 15.
    Steffens S, Junker K, Roos FC et al (2014) Small renal cell carcinomas--how dangerous are they really? Results of a large multicenter study. Eur J Cancer 50:739–745CrossRefPubMedGoogle Scholar
  16. 16.
    Novara G, Ficarra V, Antonelli A et al (2010) Validation of the 2009 TNM version in a large multi-institutional cohort of patients treated for renal cell carcinoma: are further improvements needed? Eur Urol 58:588–595CrossRefPubMedGoogle Scholar
  17. 17.
    Moch H, Gasser T, Amin MB, Torhorst J, Sauter G, Mihatsch MJ (2000) Prognostic utility of the recently recommended histologic classification and revised TNM staging system of renal cell carcinoma: a Swiss experience with 588 tumors. Cancer 89:604–614CrossRefPubMedGoogle Scholar
  18. 18.
    Rabjerg M, Mikkelsen MN, Walter S, Marcussen N (2014) Incidental renal neoplasms: is there a need for routine screening? A Danish single-center epidemiological study. APMIS 122:708–714CrossRefPubMedGoogle Scholar
  19. 19.
    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 45:59–64CrossRefPubMedGoogle Scholar
  20. 20.
    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 40:141–154CrossRefPubMedGoogle Scholar
  21. 21.
    Tickoo SK, dePeralta-Venturina MN, Harik LR et al (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 30:141–153CrossRefPubMedGoogle Scholar
  22. 22.
    Végső G, Toronyi E, Hajdu M et al (2011) Renal cell carcinoma of the native kidney: a frequent tumor after kidney transplantation with favorable prognosis in case of early diagnosis. Transplant Proc 43:1261–1264CrossRefPubMedGoogle Scholar
  23. 23.
    Breda A, Luccarelli G, Rodriguez-Faba O et al (2015) Clinical and pathological outcomes of renal cell carcinoma (RCC) in native kidneys of patients with end-stage renal disease: a long-term comparative retrospective study with RCC diagnosed in the general population. World J Urol 33:1–7CrossRefPubMedGoogle Scholar
  24. 24.
    Song C, Hong SH, Chung JS, Byun SS, Kwak C, Jeong CW, Seo SI, Jeon HG, Seo IY (2016) Renal cell carcinoma in end-stage disease: multi-institutional comparative analysis of survival. Int J Urol 23:465–471CrossRefPubMedGoogle Scholar
  25. 25.
    Patard JJ, Leray E, Rioux-Leclercq N, Cindolo L et al (2005) Prognostic value of histologic subtypes in renal cell carcinoma: a multicenter experience. J Clin Oncol 23:2763–2771CrossRefPubMedGoogle Scholar
  26. 26.
    Leibovich BC, Lohse CM, Crispen PL, Boorjian SA, Thompson RH, Blute ML, Cheville JC (2010) Histological subtype is an independent predictor of outcome for patients with renal cell carcinoma. J Urol 183:1309–1315CrossRefPubMedGoogle Scholar
  27. 27.
    Capitanio U, Cloutier V, Zini L et al (2009) A critical assessment of the prognostic value of clear cell, papillary and chromophobe histological subtypes in renal cell carcinoma: a population-based study. BJUI 103:1496–1500CrossRefGoogle Scholar
  28. 28.
    Volpe A, Novara G, Antonelli A et al (2012) Chromophobe renal cell carcinoma (RCC): oncological outcomes and prognostic factors in a large multicentre series. BJU Int 110:76–83CrossRefPubMedGoogle Scholar
  29. 29.
    Frees S, Kamal MM, Knoechlein L et al (2016) Differences in overall and cancer-specific survival of patients presenting with chromophobe versus clear cell renal cell carcinoma: a propensity score matched analysis. Urology. doi: 10.1016/j.urology.2016.05.048 Google Scholar
  30. 30.
    Amin MB, Paner GP, Alvarado-Cabrero I, Young AN, Stricker HJ, Lyles RH, Moch H (2008) Chromophobe renal cell carcinoma: histomorphologic characteristics and evaluation of conventional pathologic prognostic parameters in 145 cases. Am J Surg Pathol 32:1822–1834CrossRefPubMedGoogle Scholar
  31. 31.
    Diolombi ML, Cheng L, Argani P, Epstein JI (2015) Do clear cell papillary renal cell carcinomas have malignant potential? Am J Surg Pathol 39:1621–1634CrossRefPubMedGoogle Scholar
  32. 32.
    Cornejo KM, Dong F, Zhou AG et al (2015) Papillary renal cell carcinoma: correlation of tumor grade and histologic characteristics with clinical outcome. Hum Pathol 46:1411–1417CrossRefPubMedGoogle Scholar
  33. 33.
    Warrick JI, Tsodikov A, Kunju LP et al (2012) Papillary renal cell carcinoma revisited: a comprehensive histomorphologic study with outcome correlations. Hum Pathol 45:1139–1146CrossRefGoogle Scholar
  34. 34.
    Pichler M, Hutterer GC, Chromecki TF, Pummer K, Mannweiler S, Zigeuner R (2013) Presence and extent of histological tumour necrosis is an adverse prognostic factor in papillary type 1 but not in papillary type 2 renal cell carcinoma. Histopathology 62:219–228CrossRefPubMedGoogle Scholar
  35. 35.
    Frank I, Blute ML, Cheville JC, Lohse CM, Weaver AL, Zincke H (2002) An outcome prediction model for patients with clear cell renal cell carcinoma treated with radical nephrectomy based on tumor stage, size, grade and necrosis: the SSIGN score. J Urol 168:2395–2400CrossRefPubMedGoogle Scholar
  36. 36.
    Lam JS, Shvarts O, Said JW et al (2005) Clinicopathologic and molecular correlations of necrosis in the primary tumor of patients with renal cell carcinoma. Cancer 103:2517–2525CrossRefPubMedGoogle Scholar
  37. 37.
    The Cancer Genom Atlas Network (2016) Comprehensive molecular characterization of papillary renal-cell carcinoma. N Engl J Med 374:135–145CrossRefGoogle Scholar
  38. 38.
    Becker A, Hickmann D, Hansen J et al (2016) Critical analysis of a simplified Fuhrman grading scheme for prediction of cancer specific mortality in patients with clear cell renal cell carcinoma--impact on prognosis. Eur J Surg Oncol 42:419–425CrossRefPubMedGoogle Scholar
  39. 39.
    Pierorazio PM, Johnson MH, Patel HD et al (2016) Management of Renal Masses and Localized Renal Cancer: systematic review and meta-analysis. J Urol. doi: 10.1016/j.juro.2016.04.081 Google Scholar
  40. 40.
    Chamie K, Donin NM, Klöpfer P et al (2016) Adjuvant weekly girentuximab following nephrectomy for high-risk renal cell carcinoma: the ARISER randomized clinical trial. JAMA Oncol. doi: 10.1001/jamaoncol.2016.4419 PubMedGoogle Scholar

Copyright information

© Arányi Lajos Foundation 2016

Authors and Affiliations

  1. 1.Department of PathologyUniversity of SzegedSzegedHungary
  2. 2.Department of Dermatology and AllergologyUniversity of SzegedSzegedHungary
  3. 3.Department of OncotherapyUniversity of SzegedSzegedHungary
  4. 4.Department of UrologyUniversity of SzegedSzegedHungary

Personalised recommendations