229
Views
7
CrossRef citations to date
0
Altmetric
Review

Developments in the use of tyrosine kinase inhibitors in the treatment of renal cell carcinoma

, &
Pages 259-271 | Received 28 Nov 2018, Accepted 21 Jan 2019, Published online: 04 Feb 2019

References

  • “Cancer stat facts: kidney and renal pelvis cancer.” SEER, Available from: seer.cancer.gov/statfacts/html/kidrp.html.
  • American Cancer Society, Kidney Cancer (adult)– renal cell carcinoma. Available from: (http://www.cancer.org/cancer/kidneycancer/detailedguide/).
  • Latif F, Tory K, Gnarra J, et al. Identification of the von Hippel-Lindau disease tumor suppressor gene. Science. 1993;260(5112):1317–1320.
  • Sufan RI, Jewett MA, Ohh M. The role of von Hippel-Lindau tumor suppressor protein and hypoxia in renal clear cell carcinoma. Am J Physiol Renal Physiol. 2004;287(1):F1–F6.
  • Beroukhim R, Brunet JP, Di Napoli A, et al. Patterns of gene expression and copy-number alterations in von-hippel lindau disease-associated and sporadic clear cell carcinoma of the kidney. Cancer Res. 2009;69(11):4674–4681.
  • Cancer Genome Atlas Research Network. Comprehensive molecular characterization of clear cell renal cell carcinoma. Nature. 2013;499(7456):43–49.
  • U.S. Food and Drug Administration, Center for Drug Evaluation and Research. Sorafenib NDA 21-923 approval letter, 12/ 20/2005. cited 2018 Oct 10 Available from: http://www.accessdata.fda.gov/drugsatfda_docs/nda/2005/021923_s000_Nexavar_Approv.pdf
  • Escudier B, Eisen T, Stadler WM, et al. Sorafenib in advanced clear-cell renal-cell carcinoma. N Engl J Med. 2007;356(2):125–134.
  • U.S. Food and Drug Administration, Center for Drug Evaluation and Research. Sorafenib NDA 21-968 approval letter, [ updated 2006 Jan 26; cited 2018 Oct 10]. Available from: http://www.accessdata.fda.gov/drugsatfda_docs/nda/2006/021938_S000_Sutent_Approv.pdf
  • Motzer RJ, Hutson TE, Tomczak P, et al. Sunitinib versus interferon alfa in metastatic renal-cell carcinoma. N Engl J Med. 2007;356(2):115–124.
  • Motzer RJ, Hutson TE, Tomczak P, et al. Overall survival and updated results for sunitinib compared with interferon alfa in patients with metastatic renal cell carcinoma. J Clin Oncol. 2009;27(22):3584–3590.
  • Schmidinger M, Zielinski CC, Vogl UM, et al. Cardiac toxicity of sunitinib and sorafenib in patients with metastatic renal cell carcinoma. J Clin Oncol. 2008;26(32):5204–5212.
  • Hall PS, Harshman LC, Srinivas S, et al. The frequency and severity of cardiovascular toxicity from targeted therapy in advanced renal cell carcinoma patients. JACC Heart Fail. 2013;1(1):72–78.
  • Najjar YG, Mittal K, Elson P, et al. A 2 weeks on and 1 week off schedule of sunitinib is associated with decreased toxicity in metastatic renal cell carcinoma. Eur J Cancer. 2014;50(6):1084–1089.
  • Sternberg CN, Davis ID, Mardiak J, et al. Pazopanib in locally advanced or metastatic renal cell carcinoma: results of a randomized phase III trial. J Clin Oncol. 2010;28(6):1061–1068.
  • Motzer RJ, Hutson TE, Cella D, et al. Pazopanib versus sunitinib in metastatic renal-cell carcinoma. N Engl J Med. 2013;369(8):722–731.
  • U.S. Food and Drug Administration, Center for Drug Evaluation and Research. Pazopanib NDA 022465 approval letter. Available from: https://www.accessdata.fda.gov/drugsatfda_docs/nda/2009/022465s000_Approv.pdf
  • Rini BI, Escudier B, Tomczak P, et al. Comparative effectiveness of axitinib versus sorafenib in advanced renal cell carcinoma (AXIS): a randomised phase 3 trial. Lancet. 2011;378(9807): 1931–1939. Phase 3 AXIS trial showing axitinib was superior to sorafenib for treatment of advanced RCC in the second-line setting.
  • Motzer RJ, Escudier B, Tomczak P, et al. Axitinib versus sorafenib as second-line treatment for advanced renal cell carcinoma: overall survival analysis and updated results from a randomised phase 3 trial. Lancet Oncol. 2013;14(6):552–562.
  • Motzer RJ, Hutson TE, Glen H, et al. Lenvatinib, everolimus, and the combination in patients with metastatic renal cell carcinoma: a randomised, phase 2, open-label, multicentre trial. Lancet Oncol. 2015;16(15):1473–1482.
  • Choueiri TK, Escudier B, Powles T, et al. Cabozantinib versus everolimus in advanced renal cell carcinoma (METEOR): final results from a randomised, open-label, phase 3 trial. Lancet Oncol. 2016;17(7):917–927.
  • Zhou L, Liu XD, Sun M, et al. Targeting MET and AXL overcomes resistance to sunitinib therapy in renal cell carcinoma. Oncogene. 2016;35(21):2687–2697.
  • Choueiri TK, Halabi S, Sanford BL, et al. Cabozantinib versus sunitinib as initial targeted therapy for patients with metastatic renal cell carcinoma of poor or intermediate risk: the alliance A031203 CABOSUN trial. J Clin Oncol. 2017;35(6):591–597.
  • Buti S, Bersanelli M. Is cabozantinib really better than sunitinib as first-line treatment of metastatic renal cell Carcinoma? J Clin Oncol. 2017;35(16):1858–1859.
  • Choueiri TK, Hessel C, Halabi S, et al. Cabozantinib versus sunitinib as initial therapy for metastatic renal cell carcinoma of intermediate or poor risk (Alliance A031203 CABOSUN randomised trial): progression-free survival by independent review and overall survival update. Eur J Cancer. 2018;94:115–125.
  • U.S. Food and Drug Administration, Center for Drug Evaluation and Research. Cabozantinib NDA 208692 approval letter. Available from: https://www.accessdata.fda.gov/drugsatfda_docs/nda/2016/208692Orig1s000TOC.cfm
  • Motzer RJ, Nosov D, Eisen T, et al. Tivozanib versus sorafenib as initial targeted therapy for patients with metastatic renal cell carcinoma: results from a phase III trial. J Clin Oncol. 2013;31(30):3791–3799.
  • Molina AM, Hutson TE, Nosov D, et al. Efficacy of tivozanib treatment after sorafenib in patients with advanced renal cell carcinoma: crossover of a phase 3 study. Eur J Cancer. 2018;94:87–94.
  • Fotivda. (n.d.). [cited 2018 Oct 10], from https://www.ema.europa.eu/medicines/human/EPAR/fotivda
  • Jamil MO, Hathaway A, Mehta A. Tivozanib: status of development. Curr Oncol Rep. 2015;17(6):24.
  • U.S. Food and Drug Administration, Center for Drug Evaluation and Research. Lenvatinib NDA 206947/S-003 approval letter. Available from: https://www.accessdata.fda.gov/drugsatfda_docs/nda/2016/208692Orig1s000TOC.cfm
  • Choueiri TK, Fay AP, Gray KP, et al. PD-L1 expression in nonclear-cell renal cell carcinoma. Ann Oncol. 2014;25(11):2178–2184.
  • Thompson RH, Dong H, Lohse CM, et al. PD-1 is expressed by tumor-infiltrating immune cells and is associated with poor outcome for patients with renal cell carcinoma. Clin Cancer Res. 2007;13(6):1757–1761.
  • Motzer RJ, Tannir NM, McDermott DF, et al. Nivolumab plus ipilimumab versus sunitinib in advanced renal-cell Carcinoma. N Engl J Med. 2018;378(14):1277–1290.
  • Amin A, Plimack ER, Ernstoff MS, et al. Safety and efficacy of nivolumab in combination with sunitinib or pazopanib in advanced or metastatic renal cell carcinoma: the checkmate 016 study. J Immunother Cancer. 2018;6(1):109.
  • Motzer RJ, Powles T, Atkins MB, et al. IMmotion151: a randomized phase III study of atezolizumab plus bevacizumab vs sunitinib in untreated metastatic renal cell Carcinoma (mRCC). J clin oncol. 2018;36(6_suppl):578.
  • Kelsey R. Kidney cancer: PDL1 as a biomarker in high-risk RCC. Nat Rev Urol. 2018;15(4):202.
  • Choueiri TK, Larkin J, Oya M, et al. Preliminary results for avelumab plus axitinib as first-line therapy in patients with advanced clear-cell renal-cell carcinoma (JAVELIN renal 100): an open-label, dose-finding and dose-expansion, phase 1b trial. Lancet Oncol. 2018;19(4):451–460.
  • Motzer et al. Abstract LBA6_PR ‘JAVELIN Renal 101: A randomized, phase III study of avelumab + axitinib vs sunitinib as first-line treatment of advanced renal cell carcinoma (aRCC)’ will be presented by Robert Motzer during Presidential Symposium 2 on Sunday 21 October, 16:30 to 18: 10(CEST) in room 18 - hall A2. Ann Oncol. 8 October 2018; 29 Supplement.
  • Atkins MB, Plimack ER, Puzanov I, et al. Axitinib in combination with pembrolizumab in patients with advanced renal cell cancer: a non-randomised, open-label, dose-finding, and dose-expansion phase 1b trial. Lancet Oncol. 2018;19(3):405–415.
  • Rexer H, Bedke J. First-line therapy in advanced renal cell carcinoma: A randomized, open-label phase III study evaluating the efficacy and safety of pembrolizumab (MK-3475) in combination with axitinib compared to sunitinib monotherapy as first-line treatment for locally advanced or metastatic renal cell carcinoma (mRCC) (Keynote-426) - AN 39/16 of the AUO. Urologe A. 2017;56(3):385–386.
  • Merck’s KEYTRUDA® (pembrolizumab) in Combination with Pfizer’s Inlyta® (axitinib) Significantly Improved Overall Survival (OS) and Progression-free Survival (PFS) as First-Line Therapy for Advanced or Metastatic Renal Cell Carcinoma. (2018, Oct 18). [cited 2018 Oct 20]. Available from: https://investors.merck.com/news/press-release-details/2018/Mercks-KEYTRUDA-pembrolizumab-in-Combination-with-Pfizers-Inlyta-axitinib-Significantly-Improved-Overall-Survival-OS-and-Progression-free-Survival-PFS-as-First-Line-Therapy-for-Advanced-or-Metastatic-Renal-Cell-Carcinoma/default.aspx
  • Lee C, Makker V, Rasco DW, et al. Lenvatinib + pembrolizumab in patients with renal cell carcinoma: updated results. Jco. 2018;36(15_suppl):4560.
  • Motzer RJ, Grünwald V, Hutson TE, et al. A phase 3 trial to compare efficacy and safety of lenvatinib in combination with everolimus or pembrolizumab versus sunitinib alone in first-line treatment of patients with metastatic renal cell carcinoma. Jco. 2018;36(6_suppl):TPS706–TPS706.
  • Nadal RM, Mortazavi A, Stein M, et al. Results of phase I plus expansion cohorts of cabozantinib (Cabo) plus nivolumab (Nivo) and CaboNivo plus ipilimumab (Ipi) in patients (pts) with with metastatic urothelial carcinoma (mUC) and other genitourinary (GU) malignancies. Jco. 2018;36(6_suppl):515.
  • Choueiri TK, Apolo AB, Powles T, et al. A phase 3, randomized, open-label study of nivolumab combined with cabozantinib vs sunitinib in patients with previously untreated advanced or metastatic renal cell carcinoma (RCC; CheckMate 9ER). Jco. 2018;36(15_suppl):TPS4598–TPS4598.
  • Maia MC, Agarwal N, McGregor BA, et al. Phase 1b trial of cabozantinib in combination with atezolizumab in patients with locally advanced or metastatic urothelial carcinoma (UC) or renal cell carcinoma (RCC). JCO. 2018;36(5_suppl):TPS42–TPS42.
  • Thomas AA, Rini BI, Stephenson AJ, et al. Surgical resection of renal cell carcinoma after targeted therapy. J Urol. 2009;182(3):881–886.
  • Hellenthal NJ, Underwood W, Penetrante R, et al. Prospective clinical trial of preoperative sunitinib in patients with renal cell carcinoma. J Urol. 2010;184(3):859–864.
  • Cowey CL, Amin C, Pruthi RS, et al. Neoadjuvant clinical trial with sorafenib for patients with stage II or higher renal cell carcinoma. J Clin Oncol. 2010;28(9):1502–1507.
  • Rini BI, Plimack ER, Takagi T, et al. A phase II study of pazopanib in patients with localized renal cell carcinoma to optimize preservation of renal parenchyma. J Urol. 2015;194(2):297–303.
  • Silberstein JL, Millard F, Mehrazin R, et al. Feasibility and efficacy of neoadjuvant sunitinib before nephron-sparing surgery. BJU Int. 2010;106(9):1270–1276.
  • Karam JA, Devine CE, Urbauer DL, et al. Phase 2 trial of neoadjuvant axitinib in patients with locally advanced nonmetastatic clear cell renal cell carcinoma. Eur Urol. 2014;66(5):874–880.
  • Bindayi A, Hamilton ZA, Mcdonald ML, et al. Neoadjuvant therapy for localized and locally advanced renal cell carcinoma. Urol Oncol. 2018;36(1):31–37.
  • Janzen NK, Kim HL, Figlin RA, et al. Surveillance after radical or partial nephrectomy for localized renal cell carcinoma and management of recurrent disease. Urol Clin North Am. 2003;30(4):843–852.
  • Haas NB, Manola J, Uzzo RG, et al. Adjuvant sunitinib or sorafenib for high-risk, non-metastatic renal-cell carcinoma (ECOG-ACRIN E2805): a double-blind, placebo-controlled, randomised, phase 3 trial. Lancet. 2016;387(10032):2008–2016.
  • Haas NB, Manola J, Dutcher JP, et al. Adjuvant treatment for high-risk clear cell renal cancer: updated results of a high-risk subset of the ASSURE randomized trial. JAMA Oncol. 2017;3(9):1249–1252.
  • Ravaud A, Rj M, Hs P, et al. Adjuvant sunitinib in high-risk renal-cell carcinoma after nephrectomy. N Engl J Med. 2016;375(23):2246–2254.
  • U.S. Food and Drug Administration, Center for Drug Evaluation and Research. Sunitinib NDA 21-938 and 21-968 approval letter. Available from: https://www.accessdata.fda.gov/drugsatfda_docs/nda/2006/021938_S000_Sutent_Approv.pdf
  • Motzer RJ, Haas NB, Donskov F, et al. Randomized phase III trial of adjuvant pazopanib versus placebo after nephrectomy in patients with localized or locally advanced renal cell carcinoma. J Clin Oncol. 2017;35(35):3916–3923.
  • Gross-Goupil M, Kwon TG, Eto M, et al. Axitinib versus placebo as an adjuvant treatment for renal cell carcinoma: results from the phase III, randomized ATLAS trial. Ann Oncol. 2018;29(12):2371-2378.
  • Figlin RA, Leibovich BC, Stewart GD, et al. Adjuvant therapy in renal cell carcinoma: does higher risk for recurrence improve the chance for success? Ann Oncol. 2018;29(2):324–331.
  • Casuscelli J, Hsieh JJ. Are we ready for adjuvant sunitinib in high-risk renal cell Carcinoma? Eur Urol. 2018;73(1):69–70.
  • Sun M, Marconi L, Eisen T, et al. Adjuvant vascular endothelial growth factor-targeted therapy in renal cell carcinoma: a systematic review and pooled analysis. Eur Urol. 2018;74(5):611–620.
  • Rini BI, Escudier B, Martini JF, et al. Validation of the 16-gene recurrence score in patients with locoregional, high-risk renal cell carcinoma from a phase iii trial of adjuvant sunitinib. Clin Cancer Res off J Am Assoc Cancer Res. 2018;24(18):4407–4415.
  • Flanigan RC, Mickisch G, Sylvester R, et al. Cytoreductive nephrectomy in patients with metastatic renal cancer: a combined analysis. J Urol. 2004;171(3):1071–1076.
  • National Comprehensive Cancer Center. Kidney Cancer, Version 2.2019. [cited Oct 20 2018]. Available from: https://www.nccn.org/professionals/physician_gls/pdf/kidney.pdf
  • You D, Jeong IG, Ahn JH, et al. The value of cytoreductive nephrectomy for metastatic renal cell carcinoma in the era of targeted therapy. J Urol. 2011;185(1):54–59.
  • Choueiri TK, Xie W, Kollmannsberger C, et al. The impact of cytoreductive nephrectomy on survival of patients with metastatic renal cell carcinoma receiving vascular endothelial growth factor targeted therapy. J Urol. 2011;185(1):60–66.
  • Psutka SP, Kim SP, Gross CP, et al. The impact of targeted therapy on management of metastatic renal cell carcinoma: trends in systemic therapy and cytoreductive nephrectomy utilization. Urology. 2015;85(2):442–450.
  • Méjean A, Ravaud A, Thezenas S, et al. Sunitinib alone or after nephrectomy in metastatic renal-cell carcinoma. N Engl J Med. 2018;379(5):417–427.
  • Motzer RJ, Russo P. Cytoreductive nephrectomy - patient selection is key. N Engl J Med. 2018;379(5):481–482.
  • Bex A, Mulders P, Jewett M, et al. Comparison of Immediate vs Deferred Cytoreductive Nephrectomy in Patients with Synchronous Metastatic Renal Cell Carcinoma Receiving Sunitinib: The SURTIME Randomized Clinical Trial. JAMA Oncol. 2018.
  • Macleod LC, Odisho AY, Tykodi SS, et al. Comparative effectiveness of initial surgery vs initial systemic therapy for metastatic kidney cancer in the targeted therapy era: analysis of a population-based Cohort. Urology. 2018;113:146–152.
  • Bhindi B, Habermann EB, Mason RJ, et al. Comparative Survival following Initial Cytoreductive Nephrectomy versus Initial Targeted Therapy for Metastatic Renal Cell Carcinoma. J Urol. 2018;200(3):528–534.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.