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Pattern, timing and predictors of recurrence after surgical resection of chromophobe renal cell carcinoma

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Abstract

Purpose

Currently there are no specific guidelines for the post-operative follow-up of chromophobe renal cell carcinoma (chRCC). We aimed to evaluate the pattern, location and timing of recurrence after surgery for non-metastatic chRCC and establish predictors of recurrence and cancer-specific death.

Methods

Retrospective analysis of consecutive surgically treated non-metastatic chRCC cases from the Royal Free London NHS Foundation Trust (UK, 2015–2019) and the international collaborative database RECUR (15 institutes, 2006–2011). Kaplan–Meier curves were plotted. The association between variables of interest and outcomes were analysed using univariate and multivariate Cox proportional hazards regression models with shared frailty for data source.

Results

295 patients were identified. Median follow-up was 58 months. The five and ten-year recurrence-free survival rates were 94.3% and 89.2%. Seventeen patients (5.7%) developed recurrent disease, 13 (76.5%) with distant metastases. 54% of metastatic disease diagnoses involved a single organ, most commonly the bone. Early recurrence (< 24 months) was observed in 8 cases, all staged ≥ pT2b. 30 deaths occurred, of which 11 were attributed to chRCC. Sarcomatoid differentiation was rare (n = 4) but associated with recurrence and cancer-specific death on univariate analysis. On multivariate analysis, UICC/AJCC T-stage ≥ pT2b, presence of coagulative necrosis, and positive surgical margins were predictors of recurrence and cancer-specific death.

Conclusion

Recurrence and death after surgically resected chRCC are rare. For completely excised lesions ≤ pT2a without coagulative necrosis or sarcomatoid features, prognosis is excellent. These patients should be reassured and follow-up intensity curtailed.

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References

  1. Bray F, Ferlay J, Soerjomataram I, Siegel RL, Torre LA, Jemal A (2018) Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin 68(6):394–424. https://doi.org/10.3322/caac.21492

    Article  PubMed  Google Scholar 

  2. Moch H, Cubilla AL, Humphrey PA, Reuter VE, Ulbright TM (2016) The 2016 WHO classification of tumours of the urinary system and male genital organs-part A: renal, penile, and testicular tumours. Eur Urol 70(1):93–105. https://doi.org/10.1016/j.eururo.2016.02.029

    Article  PubMed  Google Scholar 

  3. Davis Caleb F, Ricketts CJ, Wang M, Yang L, Cherniack Andrew D, Shen H, Buhay C, Kang H, Kim Sang C, Fahey Catherine C, Hacker Kathryn E, Bhanot G, Gordenin Dmitry A, Chu A, Gunaratne Preethi H, Biehl M, Seth S, Kaipparettu Benny A, Bristow Christopher A, Donehower Lawrence A, Wallen Eric M, Smith Angela B, Tickoo Satish K, Tamboli P, Reuter V, Schmidt Laura S, Hsieh James J, Choueiri Toni K, Hakimi AA, Creighton Chad J, Davis Caleb F, Morgan M, Gunaratne Preethi H, Donehower Lawrence A, Kaipparettu Benny A, Wheeler David A, Gibbs Richard A, Signoretti S, Cherniack Andrew D, Robertson AG, Chu A, Choueiri Toni K, Henske Elizabeth P, Kwiatkowski David J, Reuter V, Hsieh James J, Hakimi AA, Tickoo Satish K, Ricketts C, Linehan WM, Schmidt Laura S, Gordenin Dmitry A, Bhanot G, Seiler M, Tamboli P, Rathmell WK, Fahey Catherine C, Hacker Kathryn E, Smith Angela B, Wallen Eric M, Shen H, Laird Peter W, Shuch B, Muzny D, Buhay C, Wang M, Chao H, Dahdouli M, Xi L, Kakkar N, Reid Jeffrey G, Downs B, Drummond J, Morton D, Doddapaneni H, Lewis L, English A, Meng Q, Kovar C, Wang Q, Hale W, Hawes A, Kalra D, Walker K, Murray Bradley A, Sougnez C, Saksena G, Carter Scott L, Schumacher Steven E, Tabak B, Zack Travis I, Getz G, Beroukhim R, Gabriel Stacey B, Meyerson M, Ally A, Balasundaram M, Birol I, Brooks D, Butterfield Yaron SN, Chuah E, Clarke A, Dhalla N, Guin R, Holt Robert A, Kasaian K, Lee D, Li Haiyan I, Lim E, Ma Y, Mayo M, Moore Richard A, Mungall Andrew J, Schein Jacqueline E, Sipahimalani P, Tam A, Thiessen N, Wong T, Jones Steven JM, Marra Marco A, Auman JT, Tan D, Meng S, Jones Corbin D, Hoadley Katherine A, Mieczkowski Piotr A, Mose Lisle E, Jefferys Stuart R, Roach J, Veluvolu U, Wilkerson Matthew D, Waring S, Buda E, Wu J, Bodenheimer T, Hoyle Alan P, Simons Janae V, Soloway Mathew G, Balu S, Parker Joel S, Hayes DN, Perou Charles M, Weisenberger Daniel J, Bootwalla Moiz S, Triche T Jr, Lai Phillip H, Van Den Berg DJ, Baylin Stephen B, Chen F, Coarfa C, Noble Michael S, DiCara D, Zhang H, Cho J, Heiman David I, Gehlenborg N, Voet D, Lin P, Frazer S, Stojanov P, Liu Y, Zou L, Kim J, Lawrence Michael S, Chin L, Yang L, Seth S, Bristow Christopher A, Protopopov A, Song X, Zhang J, Pantazi A, Hadjipanayis A, Lee E, Luquette Lovelace J, Lee S, Parfenov M, Santoso N, Seidman J, Xu Andrew W, Kucherlapati R, Park Peter J, Kang H, Lee J, Roberts Steven A, Klimczak Leszek J, Fargo D, Lang M, Choi Y-L, Kim Sang C, Lee J-K, Park W-Y, Wang W, Fan Y, Ahn J, Akbani R, Weinstein John N, Haussler D, Ma S, Radenbaugh A, Zhul J, Biehl M, Lichtenberg Tara M, Zmuda E, Black Aaron D, Hanf B, Ramirez Nilsa C, Wise L, Bowen J, Leraas Kristen M, Hall Tracy M, Gastier-Foster Julie M, Kaelin William G, Thorne L, Boice L, Huang M, Vocke C, Peterson J, Worrell R, Merino M, Czerniak Bogdan A, Aldape Kenneth D, Wood Christopher G, Spellman Paul T, Atkins Michael B, Cheville J, Thompson RH, Jensen Mark A, Pihl T, Wan Y, Ayala B, Baboud J, Velaga S, Walton J, Liu J, Chudamani S, Wu Y, Sheth M, Mills Shaw Kenna R, Demchok John A, Davidsen T, Yang L, Wang Z, Tarnuzzer Roy W, Zhang J, Eley G, Felau I, Zenklusen Jean C, Hutter Carolyn M, Guyer Mark S, Ozenberger Bradley A, Sofia Heidi J, Chin L, Meyerson M, Kucherlapati R, Park W-Y, Robertson AG, Laird PW, Henske EP, Kwiatkowski DJ, Park PJ, Morgan M, Shuch B, Muzny D, Wheeler DA, Linehan WM, Gibbs RA, Rathmell WK, Creighton CJ (2014) The somatic genomic landscape of chromophobe renal cell carcinoma. Cancer Cell 26(3):319–330. https://doi.org/10.1016/j.ccr.2014.07.014

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Leibovich BC, Blute ML, Cheville JC, Lohse CM, Frank I, Kwon ED, Weaver AL, Parker AS, Zincke H (2003) Prediction of progression after radical nephrectomy for patients with clear cell renal cell carcinoma: a stratification tool for prospective clinical trials. Cancer 97(7):1663–1671. https://doi.org/10.1002/cncr.11234

    Article  PubMed  Google Scholar 

  5. Zisman A, Pantuck AJ, Wieder J, Chao DH, Dorey F, Said JW, deKernion JB, Figlin RA, Belldegrun AS (2002) Risk group assessment and clinical outcome algorithm to predict the natural history of patients with surgically resected renal cell carcinoma. J Clin Oncol 20(23):4559–4566. https://doi.org/10.1200/jco.2002.05.111

    Article  PubMed  Google Scholar 

  6. Meskawi M, Sun M, Ismail S, Bianchi M, Hansen J, Tian Z, Hanna N, Trinh QD, Graefen M, Montorsi F, Perrotte P, Karakiewicz PI (2013) Fuhrman grade [corrected] has no added value in prediction of mortality after partial or [corrected] radical nephrectomy for chromophobe renal cell carcinoma patients. Mod Pathol 26(8):1144–1149. https://doi.org/10.1038/modpathol.2012.230

    Article  PubMed  Google Scholar 

  7. Delahunt B, Cheville JC, Martignoni G, Humphrey PA, Magi-Galluzzi C, McKenney J, Egevad L, Algaba F, Moch H, Grignon DJ, Montironi R, Srigley JR (2013) The international society of urological pathology (ISUP) grading system for renal cell carcinoma and other prognostic parameters. Am J Surg Pathol 37(10):1490–1504. https://doi.org/10.1097/PAS.0b013e318299f0fb

    Article  PubMed  Google Scholar 

  8. Siddiqui SA, Frank I, Cheville JC, Lohse CM, Leibovich BC, Blute ML (2009) Postoperative surveillance for renal cell carcinoma: a multifactorial histological subtype specific protocol. BJU Int 104(6):778–785. https://doi.org/10.1111/j.1464-410X.2009.08499.x

    Article  PubMed  Google Scholar 

  9. Leibovich BC, Lohse CM, Cheville JC, Zaid HB, Boorjian SA, Frank I, Thompson RH, Parker WP (2018) Predicting oncologic outcomes in renal cell carcinoma after surgery. Eur Urol 73(5):772–780. https://doi.org/10.1016/j.eururo.2018.01.005

    Article  PubMed  Google Scholar 

  10. Volpe A, Novara G, Antonelli A, Bertini R, Billia M, Carmignani G, Cunico SC, Longo N, Martignoni G, Minervini A, Mirone V, Simonato A, Terrone C, Zattoni F, Ficarra V (2012) Chromophobe renal cell carcinoma (RCC): oncological outcomes and prognostic factors in a large multicentre series. BJU Int 110(1):76–83. https://doi.org/10.1111/j.1464-410X.2011.10690.x

    Article  PubMed  Google Scholar 

  11. Frees S, Kamal MM, Knoechlein L, Bell R, Ziesel C, Neisius A, Thomas C, Brenner W, Jager W, Thuroff JW, Roos FC (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 98:81–87. https://doi.org/10.1016/j.urology.2016.05.048

    Article  PubMed  Google Scholar 

  12. Daugherty M, Sedaghatpour D, Shapiro O, Vourganti S, Kutikov A, Bratslavsky G (2017) The metastatic potential of renal tumors: influence of histologic subtypes on definition of small renal masses, risk stratification, and future active surveillance protocols. Urol Oncol 35(4):153.e115-153.e120. https://doi.org/10.1016/j.urolonc.2016.11.009

    Article  Google Scholar 

  13. Dabestani S, Beisland C, Stewart GD, Bensalah K, Gudmundsson E, Lam TB, Gietzmann W, Zakikhani P, Marconi L, Fernandez-Pello S, Monagas S, Williams SP, Torbrand C, Powles T, Van Werkhoven E, Meijer R, Volpe A, Staehler M, Ljungberg B, Bex A (2019) Intensive imaging-based follow-up of surgically treated localised renal cell carcinoma does not improve post-recurrence survival: results from a european multicentre database (RECUR). Eur Urol 75(2):261–264. https://doi.org/10.1016/j.eururo.2018.10.007

    Article  PubMed  Google Scholar 

  14. Sobin LH, Gospodarowicz MK, Wittekind C (2009) TNM classification of malignant tumours UICC International Union Against Cancer, 7th edn. Wiley-Blackwell, Hoboken

    Google Scholar 

  15. Edge S, Byrd DR, Compton CC, Fritz AG, Greene FL, Trotti A (2011) AJCC cancer staging manual, 7th edn. Springer, Berlin

    Google Scholar 

  16. Dabestani S, Beisland C, Stewart GD, Bensalah K, Gudmundsson E, Lam TB, Gietzmann W, Zakikhani P, Marconi L, Fernandez-Pello S, Monagas S, Williams SP, Torbrand C, Powles T, Van Werkhoven E, Meijer R, Volpe A, Staehler M, Ljungberg B, Bex A (2019) Long-term outcomes of follow-up for initially localised clear cell renal cell carcinoma: RECUR database analysis. Eur Urol Focus 5(5):857–866. https://doi.org/10.1016/j.euf.2018.02.010

    Article  PubMed  Google Scholar 

  17. Casuscelli J, Becerra MF, Seier K, Manley BJ, Benfante N, Redzematovic A, Stief CG, Hsieh JJ, Tickoo SK, Reuter VE, Coleman JA, Russo P, Ostrovnaya I, Hakimi AA (2019) Chromophobe renal cell carcinoma: results from a large single-institution series. Clin Genitourin Cancer 17(5):373-379.e374. https://doi.org/10.1016/j.clgc.2019.06.011

    Article  PubMed  PubMed Central  Google Scholar 

  18. Jiang HM, Wei JH, Zhang ZL, Fang Y, Zhou BF, Chen ZH, Lu J, Liao B, Zhou FJ, Luo JH, Chen W (2016) Does chromophobe renal cell carcinoma have better survival than clear cell renal cell carcinoma? A clinical-based cohort study and meta-analysis. Int Urol Nephrol 48(2):191–199. https://doi.org/10.1007/s11255-015-1161-3

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

The authors would like to thank the members of the RECUR consortium. JBN is funded by a UK Medical Research Council (MRC) Clinical Research Training Fellowship.

RECUR consortium members and affiliations: Karim Bensalah (Department of Urology, University of Rennes, France), Eirikur Gudmundsson (Department of Urology, Landspitali University Hospital, Iceland), Thomas B. Lam (Academic Urology Unit, University of Aberdeen, United Kingdom; Department of Urology, Aberdeen Royal Infirmary, United Kingdom), Lorenzo Marconi (Department of Urology, Coimbra University Hospital, Portugal), Sergio Fernandéz-Pello (Department of Urology, Cabueñes University Hospital, Spain), Thomas Powles (Barts Cancer Institute, Queen Mary University of London, United Kingdom), Richard Meijer (Department of Urology, University Medical Center Utrecht , Utrecht , The Netherlands), Alessandro Volpe (Department of Urology , University of Eastern Piedmont , Novara , Italy).

Funding

No funding was required for this study.

Author information

Author notes

  1. Joana B. Neves and Leyre Vanaclocha Saiz joint first authors.

  2. Saeed Dabestani, Maxine G. B. Tran and Axel Bex joint last authors.

Authors and Affiliations

  1. Division of Surgery and Interventional Science, University College London, London, UK

    Joana B. Neves, Maxine G. B. Tran & Axel Bex

  2. Specialist Centre for Kidney Cancer, Royal Free London NHS Foundation Trust, Royal Free Hospital, Pond street, London, NW3 2QG, UK

    Joana B. Neves, Yasmin Abu-Ghanem, Marta Marchetti, Ravi Barod, David Cullen, Faiz Mumtaz, Prasad Patki, Maxine G. B. Tran & Axel Bex

  3. Faculty of Medical Sciences, University College London, London, UK

    Leyre Vanaclocha Saiz

  4. Department of Pathology, Royal Free London NHS Foundation Trust, London, UK

    My-Anh Tran-Dang & Soha El-Sheikh

  5. Department of Clinical Medicine, University of Bergen, Bergen, Norway

    Christian Beisland

  6. Department of Urology, Haukeland University Hospital, Bergen, Norway

    Christian Beisland

  7. Department of Urology and Division of Experimental Oncology, Urological Research Institute, IRCCS San Raffaele Scientific Institute, Milan, Italy

    Umberto Capitanio

  8. Department of Urology, Royal Bournemouth Hospital, Bournemouth, UK

    Tobias Klatte

  9. Department of Surgery, University of Cambridge, Cambridge, UK

    Tobias Klatte & Grant D. Stewart

  10. Department of Surgical and Perioperative Sciences, Urology and Andrology, Umeå University, Umeå, Sweden

    Börje Ljungberg

  11. Department of Clinical Sciences Lund, Lund University, Skåne University Hospital, Malmö, Sweden

    Saeed Dabestani

Authors
  1. Joana B. Neves
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  2. Leyre Vanaclocha Saiz
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  3. Yasmin Abu-Ghanem
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  18. Axel Bex
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Consortia

the RECUR consortium

Contributions

Project development—JBN, MBGT, SD, AB. Data collection—JBN, LVS, MM, MAT, SE, SD. Data analysis—JBN, MBGT, SD, AB. Data interpretation—all authors. Manuscript writing/editing—JBN, MBGT, SD, AB. Critical revision of the manuscript—all authors. Manuscript submission approval—all authors. JBN, LVS joint first authors. SD, MGBT, AB joint last authors.

Corresponding author

Correspondence to Axel Bex.

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Conflict of interest

GDS has received educational grants from Pfizer, AstraZeneca and Intuitive Surgical, consultancy fees from Merck, Pfizer, EUSA Pharma and CMR Surgical, travel expenses from Pfizer and speaker fees from Pfizer. The remaining authors declare no conflicts of interest.

Ethics approval

The study was deemed exempt from research ethics committee approval (UK Health Research Authority decision tool). Informed consent was not sought. Only retrospectively collected clinical data was used for analysis. The study was performed in line with the principles of the Declaration of Helsinki.

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Members of the RECUR consortium are listed in the Acknowledgements section.

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Neves, J.B., Vanaclocha Saiz, L., Abu-Ghanem, Y. et al. Pattern, timing and predictors of recurrence after surgical resection of chromophobe renal cell carcinoma. World J Urol 39, 3823–3831 (2021). https://doi.org/10.1007/s00345-021-03683-9

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  • DOI: https://doi.org/10.1007/s00345-021-03683-9

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