An evaluation of nivolumab for the treatment of metastatic renal cell carcinoma

References

• Reuter VE, Presti JC Jr. Contemporary approach to the classification of renal epithelial tumors. Semin Oncol. 2000;27:124–137.
   PubMed Web of Science ®Google Scholar
• Rini BI, Campbell SC, Escudier B. Renal cell carcinoma. Lancet. 2009;373:1119–1132.
   PubMed Web of Science ®Google Scholar
• Miller KD, Siegel RL, Lin CC, et al. Cancer treatment and survivorship statistics, 2016. CA Cancer J Clin. 2016;66:271–289.
   PubMed Web of Science ®Google Scholar
• Hammers HJ, Plimack ER, Infante JR, et al. Safety and efficacy of nivolumab in combination with ipilimumab in metastatic renal cell carcinoma: the CheckMate 016 study. J Clin Oncol. 2017;35:3851–3858.
   PubMed Web of Science ®Google Scholar
• Zarrabi K, Fang C, Wu S. New treatment options for metastatic renal cell carcinoma with prior anti-angiogenesis therapy. J Hematol Oncol. 2017;10:38.
   PubMed Web of Science ®Google Scholar
• Mazza C, Escudier B, Albiges L. Nivolumab in renal cell carcinoma: latest evidence and clinical potential. Ther Adv Med Oncol. 2017;9:171–181.
   PubMed Web of Science ®Google Scholar
• Stewart SB, Thompson RH, Psutka SP, et al. Evaluation of the National Comprehensive Cancer Network and American Urological Association renal cell carcinoma surveillance guidelines. J Clin Oncol. 2014;32:4059–4065.
   PubMed Web of Science ®Google Scholar
• Ross K, Jones RJ. Immune checkpoint inhibitors in renal cell carcinoma. Clin Sci (Lond). 2017;131:2627–2642.
   PubMed Web of Science ®Google Scholar
• Massari F, Di Nunno V, Ciccarese C, et al. Adjuvant therapy in renal cell carcinoma. Cancer Treat Rev. 2017;60:152–157.
   PubMed Web of Science ®Google Scholar
• Molina AM, Motzer RJ, Heng DY. Systemic treatment options for untreated patients with metastatic clear cell renal cancer. Semin Oncol. 2013;40:436–443.
   PubMed Web of Science ®Google Scholar
• Bedke J, Stühler V, Stenzl A, et al. Immunotherapy for kidney cancer: status quo and the future. Curr Opin Urol. 2018 Jan;28(1):8-14.
   Web of Science ®Google Scholar
• Kabaria R, Klaassen Z, Terris MK. Renal cell carcinoma: links and risks. Int J Nephrol Renovasc Dis. 2016;9:45–52.
   PubMed Web of Science ®Google Scholar
• Nickerson ML, Jaeger E, Shi Y, et al. Improved identification of von Hippel-Lindau gene alterations in clear cell renal tumors. Clin Cancer Res. 2008;14:4726–4734.
   PubMed Web of Science ®Google Scholar
• Rini BI, Atkins MB. Resistance to targeted therapy in renal-cell carcinoma. Lancet Oncol. 2009;10:992–1000.
   PubMed Web of Science ®Google Scholar
• Venur VA, Joshi M, Nepple KG, et al. Spotlight on nivolumab in the treatment of renal cell carcinoma: design, development, and place in therapy. Drug Des Devel Ther. 2017;11:1175–1182.
   PubMed Web of Science ®Google Scholar
• Choueiri TK, Figueroa DJ, Fay AP, et al. Correlation of PD-L1 tumor expression and treatment outcomes in patients with renal cell carcinoma receiving sunitinib or pazopanib: results from COMPARZ, a randomized controlled trial. Clin Cancer Res. 2015;21:1071–1077.
   PubMed Web of Science ®Google Scholar
• Atkins MB, Clark JI, Quinn DI. Immune checkpoint inhibitors in advanced renal cell carcinoma: experience to date and future directions. Ann Oncol. 2017;28:1484–1494.
   PubMed Web of Science ®Google Scholar
• Atkins MB, Larkin J. Immunotherapy combined or sequenced with targeted therapy in the treatment of solid tumors: current perspectives. J Natl Cancer Inst. 2016;108:djv414.
   PubMedGoogle Scholar
• NCCN clinical practice guidelines in oncology. [web page] [2016 2017]. Accessed on 9 March 2017. Available from: https://www.nccn.org/professionals/physician_gls/f_guidelines.asp
   Google Scholar
• Motzer RJ, Tannir NM, McDermott DF, et al. Nivolumab plus ipilimumab versus sunitinib in advanced renal-cell carcinoma. N Engl J Med. 2018;378:1277–1290.
   PubMed Web of Science ®Google Scholar
• Fischer S, Gillessen S, Rothermundt C. Sequence of treatment in locally advanced and metastatic renal cell carcinoma. Transl Androl Urol. 2015;4:310–325.
   PubMed Web of Science ®Google Scholar
• Zibelman M, Plimack ER. Integrating immunotherapy into the management of renal cell carcinoma. J Natl Compr Canc Netw. 2017;15:841–847.
   PubMed Web of Science ®Google Scholar
• Joseph RW, Chatta G, Vaishampayan U. Nivolumab treatment for advanced renal cell carcinoma: considerations for clinical practice. Urol Oncol. 2017;35:142–148.
   PubMed Web of Science ®Google Scholar
• Disis ML. Mechanism of action of immunotherapy. Semin Oncol. 2014;41(Suppl 5):S3–13.
   PubMed Web of Science ®Google Scholar
• Finn OJ. Immuno-oncology: understanding the function and dysfunction of the immune system in cancer. Ann Oncol. 2012;23(Suppl 8):viii6–9.
   PubMed Web of Science ®Google Scholar
• Parry RV, Chemnitz JM, Frauwirth KA, et al. CTLA-4 and PD-1 receptors inhibit T-cell activation by distinct mechanisms. Mol Cell Biol. 2005;25:9543–9553.
   PubMed Web of Science ®Google Scholar
• Liu Y, Cheng Y, Xu Y, et al. Increased expression of programmed cell death protein 1 on NK cells inhibits NK-cell-mediated anti-tumor function and indicates poor prognosis in digestive cancers. Oncogene. 2017;36:6143–6153.
   PubMed Web of Science ®Google Scholar
• Francisco LM, Sage PT, Sharpe AH. The PD-1 pathway in tolerance and autoimmunity. Immunol Rev. 2010;236:219–242.
   PubMed Web of Science ®Google Scholar
• Thompson RH, Gillett MD, Cheville JC, et al. Costimulatory molecule B7-H1 in primary and metastatic clear cell renal cell carcinoma. Cancer. 2005;104:2084–2091.
   PubMed Web of Science ®Google Scholar
• Thompson RH, Dong H, Kwon ED. Implications of B7-H1 expression in clear cell carcinoma of the kidney for prognostication and therapy. Clin Cancer Res. 2007;13:709s–15s.
   PubMed Web of Science ®Google Scholar
• Hakenberg OW. Nivolumab for the treatment of bladder cancer. Expert Opin Biol Ther. 2017;17:1309–1315.
   PubMed Web of Science ®Google Scholar
• Lee JY, Lee HT, Shin W, et al. Structural basis of checkpoint blockade by monoclonal antibodies in cancer immunotherapy. Nat Commun. 2016;7:13354.
   PubMed Web of Science ®Google Scholar
• Blank C, Kuball J, Voelkl S, et al. Blockade of PD-L1 (B7-H1) augments human tumor-specific T cell responses in vitro. Int J Cancer. 2006;119:317–327.
   PubMed Web of Science ®Google Scholar
• Schmidinger M. Clinical decision-making for immunotherapy in metastatic renal cell carcinoma. Curr Opin Urol. 2018;28:29–34.
   PubMed Web of Science ®Google Scholar
• Garrido G, Rabasa A, Garrido C, et al. Preclinical modeling of EGFR-specific antibody resistance: oncogenic and immune-associated escape mechanisms. Oncogene. 2014;33:3129–3139.
   PubMed Web of Science ®Google Scholar
• Kadowaki N. Combination of targeted therapy and immunotherapy for cancer. Gan To Kagaku Ryoho. 2015;42:1046–1049.
   PubMedGoogle Scholar
• Motzer RJ, Escudier B, McDermott DF, et al. Nivolumab versus everolimus in advanced renal-cell carcinoma. N Engl J Med. 2015;373:1803–1813.
   PubMed Web of Science ®Google Scholar
• Ascierto ML, McMiller TL, Berger AE, et al. The intratumoral balance between metabolic and immunologic gene expression is associated with anti-PD-1 response in patients with renal cell carcinoma. Cancer Immunol Res. 2016;4:726–733.
   PubMed Web of Science ®Google Scholar
• Iacovelli R, Nolè F, Verri E, et al. Prognostic role of PD-L1 expression in renal cell carcinoma: a systematic review and meta-analysis. Target Oncol. 2016;11:143–148.
   PubMed Web of Science ®Google Scholar
• Lolli C, Basso U, Derosa L, et al. Systemic immune-inflammation index predicts the clinical outcome in patients with metastatic renal cell cancer treated with sunitinib. Oncotarget. 2016;7:54564–54571.
   PubMedGoogle Scholar
• Das R, Verma R, Sznol M, et al. Combination therapy with anti-CTLA-4 and anti-PD-1 leads to distinct immunologic changes in vivo. J Immunol. 2015;194:950–959.
   PubMed Web of Science ®Google Scholar
• Choueiri TK, Fishman MN, Escudier B, et al. Immunomodulatory activity of nivolumab in metastatic renal cell carcinoma. Clin Cancer Res. 2016;22:5461–5471.
   PubMed Web of Science ®Google Scholar
• Sodji Q, Klein K, Sravan K, et al. Predictive role of PD-L1 expression in the response of renal medullary carcinoma to PD-1 inhibition. J Immunother Cancer. 2017;5:62.
   PubMed Web of Science ®Google Scholar
• Topalian SL, Hodi FS, Brahmer JR, et al. Safety, activity, and immune correlates of anti-PD-1 antibody in cancer. N Engl J Med. 2012;366:2443–2454.
   PubMed Web of Science ®Google Scholar
• Brahmer JR, Drake CG, Wollner I, et al. Phase I study of single-agent anti-programmed death-1 (MDX-1106) in refractory solid tumors: safety, clinical activity, pharmacodynamics, and immunologic correlates. J Clin Oncol. 2010;28:3167–3175.
   PubMed Web of Science ®Google Scholar
• Agrawal S, Feng Y, Roy A, et al. Nivolumab dose selection: challenges, opportunities, and lessons learned for cancer immunotherapy. J Immunother Cancer. 2016;4:72.
   PubMed Web of Science ®Google Scholar
• Guo L, Zhang H, Chen B. Nivolumab as programmed death-1 (PD-1) inhibitor for targeted immunotherapy in tumor. J Cancer. 2017;8:410–416.
   PubMed Web of Science ®Google Scholar
• Wang C, Thudium KB, Han M, et al. In vitro characterization of the anti-PD-1 antibody nivolumab, BMS-936558, and in vivo toxicology in non-human primates. Cancer Immunol Res. 2014;2:846–856.
   PubMed Web of Science ®Google Scholar
• Glassman PM, Balthasar JP. Mechanistic considerations for the use of monoclonal antibodies for cancer therapy. Cancer Biol Med. 2014;11:20–33.
   PubMedGoogle Scholar
• Kuenen B, Witteveen PO, Ruijter R, et al. A phase I pharmacologic study of necitumumab (IMC-11F8), a fully human IgG1 monoclonal antibody directed against EGFR in patients with advanced solid malignancies. Clin Cancer Res. 2010;16:1915–1923.
   PubMed Web of Science ®Google Scholar
• Liu C, Yu J, Li H, et al. Association of time-varying clearance of nivolumab with disease dynamics and its implications on exposure response analysis. Clin Pharmacol Ther. 2017;101:657–666.
   PubMed Web of Science ®Google Scholar
• Christensen H, Hermann M. Immunological response as a source to variability in drug metabolism and transport. Front Pharmacol. 2012;3:8.
   PubMed Web of Science ®Google Scholar
• Thompson RH, Kuntz SM, Leibovich BC, et al. Tumor B7-H1 is associated with poor prognosis in renal cell carcinoma patients with long-term follow-up. Cancer Res. 2006;66:3381–3385.
   PubMed Web of Science ®Google Scholar
• McDermott DF, Drake CG, Sznol M, et al. Survival, durable response, and long-term safety in patients with previously treated advanced renal cell carcinoma receiving nivolumab. J Clin Oncol. 2015;33:2013–2020.
   PubMed Web of Science ®Google Scholar
• McDermott DF, Michael RJM, Atkins B, et al. Long-term overall survival (OS) with nivolumab in previously treated patients with advanced renal cell carcinoma (aRCC) from phase I and II studies. in ASCO. J Clin Oncol. 2016;34:15suppl, 4507-4507.
   Google Scholar
• Motzer RJ, Rini BI, McDermott DF, et al. Nivolumab for metastatic renal cell carcinoma: results of a randomized phase II trial. J Clin Oncol. 2015;33:1430–1437.
   PubMed Web of Science ®Google Scholar
• Borghaei H, Paz-Ares L, Horn L, et al. Nivolumab versus docetaxel in advanced nonsquamous non-small-cell lung cancer. N Engl J Med. 2015;373:1627–1639.
   PubMed Web of Science ®Google Scholar
• Brahmer J, Reckamp KL, Baas P, et al. Nivolumab versus docetaxel in advanced squamous-cell non-small-cell lung cancer. N Engl J Med. 2015;373:123–135.
   PubMed Web of Science ®Google Scholar
• Robert C, Long GV, Brady B, et al. Nivolumab in previously untreated melanoma without BRAF mutation. N Engl J Med. 2015;372:320–330.
   PubMed Web of Science ®Google Scholar
• B. Escudier, N. Tannir, D.F. McDermott et al. CheckMate 214: efficacy and safety of nivolumab + ipilimumab (N+I) v sunitinib (S) for treatment-naive advanced or metastatic renal cell carcinoma (mRCC), including IMDC risk and PD-L1 expression subgroups. In: ESMO. Madrid, Spain: Annual Congress of the European Society for Medical Oncology; 2017.
   Google Scholar
• FDA approves nivolumab plus ipilimumab combination for intermediate or poor-risk advanced renal cell carcinoma. US FDA. 2018.
   Google Scholar
• Powles, T., et al. Updated European Association of Urology guidelines recommendations for the treatment of first-line metastatic clear cell renal cancer. Eur Urol. 2018.
   Google Scholar
• Plimack E.R, J.R. Motzer, Escudier Bernard. Two-year efficacy and safety update: phase III CheckMate 025 STUDY of nivolumab vs everolimus in patients with advanced renal cell carcinoma (aRCC). In: ESMO 2016. Copenhagen, Denmark; 2016.
   Google Scholar
• Escudier B, Sharma P, McDermott DF, et al. CheckMate 025 randomized phase 3 study: outcomes by key baseline factors and prior therapy for nivolumab versus everolimus in advanced renal cell carcinoma. Eur Urol. 2017;72:962–971.
   PubMed Web of Science ®Google Scholar
• Cella D, Yount S, Brucker PS, et al. Development and validation of a scale to measure disease-related symptoms of kidney cancer. Value Health. 2007;10:285–293.
   PubMed Web of Science ®Google Scholar
• Cella D, Grünwald V, Nathan P, et al. Quality of life in patients with advanced renal cell carcinoma given nivolumab versus everolimus in CheckMate 025: a randomised, open-label, phase 3 trial. Lancet Oncol. 2016;17:994–1003.
   PubMed Web of Science ®Google Scholar
• Yerushalmi R, Gelmon K. Treatment beyond progression: is it moving from belief to evidence? Oncologist. 2010;15:796–798.
   PubMed Web of Science ®Google Scholar
• Harris SJ, Brown J, Lopez J, et al. Immuno-oncology combinations: raising the tail of the survival curve. Cancer Biol Med. 2016;13:171–193.
   PubMed Web of Science ®Google Scholar
• Wolchok JD, Hoos A, O’Day S, et al. Guidelines for the evaluation of immune therapy activity in solid tumors: immune-related response criteria. Clin Cancer Res. 2009;15:7412–7420.
   PubMed Web of Science ®Google Scholar
• Chiou VL, Burotto M. Pseudoprogression and immune-related response in solid tumors. J Clin Oncol. 2015;33:3541–3543.
   PubMed Web of Science ®Google Scholar
• Mendiratta P, Rini BI, Ornstein MC. Emerging immunotherapy in advanced renal cell carcinoma. Urol Oncol. 2017;35:687–693.
   PubMed Web of Science ®Google Scholar
• George S, Motzer RJ, Hammers HJ, et al. Safety and efficacy of nivolumab in patients with metastatic renal cell carcinoma treated beyond progression: a subgroup analysis of a randomized clinical trial. JAMA Oncol. 2016;2:1179–1186.
   PubMed Web of Science ®Google Scholar
• Escudier B, Motzer RJ, Sharma P, et al. Treatment beyond progression in patients with advanced renal cell carcinoma treated with nivolumab in CheckMate 025. Eur Urol. 2017;72:368–376.
   PubMed Web of Science ®Google Scholar
• Amin A, Plimack E.R, Infante J.R. Nivolumab (anti-PD-1; BMS-936558, ONO-4538) in combination with sunitinib or pazopanib in patients (pts) with metastatic renal cell carcinoma (mRCC), in ASCO. J Clin Oncol. 2014.
   Google Scholar
• Farolfi A, Schepisi G, Conteduca V, et al. Pharmacokinetics, pharmacodynamics and clinical efficacy of nivolumab in the treatment of metastatic renal cell carcinoma. Expert Opin Drug Metab Toxicol. 2016;12:1089–1096.
   PubMed Web of Science ®Google Scholar
• Zimmer L, Goldinger SM, Hofmann L, et al. Neurological, respiratory, musculoskeletal, cardiac and ocular side-effects of anti-PD-1 therapy. Eur J Cancer. 2016;60:210–225.
   PubMed Web of Science ®Google Scholar
• Choueiri TK, Escudier B, Powles T, et al. Cabozantinib versus everolimus in advanced renal-cell carcinoma. N Engl J Med. 2015;373:1814–1823.
   PubMed Web of Science ®Google Scholar
• Motzer, R.J, Huston, E.H, Glen H. Lenvatinib, everolimus, and the combination in patients with metastatic renal cell carcinoma: a randomised, phase 2, open-label, multicentre trial. Lancet Oncol. 2015;16:1473–1482.
   PubMed Web of Science ®Google Scholar
• Eigentler TK, Hassel JC, Berking C, et al. Diagnosis, monitoring and management of immune-related adverse drug reactions of anti-PD-1 antibody therapy. Cancer Treat Rev. 2016;45:7–18.
   PubMed Web of Science ®Google Scholar
• Abdel-Wahab N, Shah M, Suarez-Almazor ME. Adverse events associated with immune checkpoint blockade in patients with cancer: a systematic review of case reports. PLoS One. 2016;11:e0160221.
   PubMed Web of Science ®Google Scholar
• Weber JS, Dummer R, De Pril V, et al. Patterns of onset and resolution of immune-related adverse events of special interest with ipilimumab: detailed safety analysis from a phase 3 trial in patients with advanced melanoma. Cancer. 2013;119:1675–1682.
   PubMed Web of Science ®Google Scholar
• Champiat S, Lambotte O, Barreau E, et al. Management of immune checkpoint blockade dysimmune toxicities: a collaborative position paper. Ann Oncol. 2016;2:559–574.
   Google Scholar
• Naidoo J, Page DB, Li BT, et al. Toxicities of the anti-PD-1 and anti-PD-L1 immune checkpoint antibodies. Ann Oncol. 2016;27:1362.
   PubMed Web of Science ®Google Scholar
• Wan XM, Peng LB, Ma JA, et al. Economic evaluation of nivolumab as a second-line treatment for advanced renal cell carcinoma from US and Chinese perspectives. Cancer. 2017;123:2634–2641.
   PubMed Web of Science ®Google Scholar
• Sarfaty M, Leshno M, Gordon N. Cost effectiveness of nivolumab in advanced renal cell carcinoma. Eur Urol. 2017;4:628-634.
   PubMed Web of Science ®Google Scholar
• Bach PB. New math on drug cost-effectiveness. N Engl J Med. 2015;373:1797–1799.
   PubMed Web of Science ®Google Scholar
• Wiecek W, Karcher H. Nivolumab versus cabozantinib: comparing overall survival in metastatic renal cell carcinoma. PLoS One. 2016;11:e0155389.
   PubMed Web of Science ®Google Scholar
• Guislain A, Gadiot J, Kaiser A, et al. Sunitinib pretreatment improves tumor-infiltrating lymphocyte expansion by reduction in intratumoral content of myeloid-derived suppressor cells in human renal cell carcinoma. Cancer Immunol Immunother. 2015;64:1241–1250.
   PubMed Web of Science ®Google Scholar
• Huillard O, Alexandre J, Goldwasser F. Treatment of advanced renal-cell carcinoma. N Engl J Med. 2016;374:888.
   PubMed Web of Science ®Google Scholar
• Linehan WM, Srinivasan R, Garcia JA. Non-clear cell renal cancer: disease-based management and opportunities for targeted therapeutic approaches. Semin Oncol. 2013;40:511–520.
   PubMed Web of Science ®Google Scholar
• Xu KY, Wu S. Update on the treatment of metastatic clear cell and non-clear cell renal cell carcinoma. Biomark Res. 2015;3:5.
   PubMed Web of Science ®Google Scholar
• Motzer RJ, Bacik J, Mariani T, et al. Treatment outcome and survival associated with metastatic renal cell carcinoma of non-clear-cell histology. J Clin Oncol. 2002;20:2376–2381.
   PubMed Web of Science ®Google Scholar
• Kroeger N, Xie W, Lee J-L, et al. Metastatic non-clear cell renal cell carcinoma treated with targeted therapy agents: characterization of survival outcome and application of the International mRCC Database Consortium criteria. Cancer. 2013;119:2999–3006.
   PubMed Web of Science ®Google Scholar
• Beckermann KE, Jolly PC, Kim JY, et al. Clinical and immunologic correlates of response to PD-1 blockade in a patient with metastatic renal medullary carcinoma. J Immunother Cancer. 2017;5:1.
   PubMed Web of Science ®Google Scholar
• Koshkin VS, Barata PC, Zhang T, et al. Clinical activity of nivolumab in patients with non-clear cell renal cell carcinoma. J Immunother Cancer. 2018;6:9.
   PubMed Web of Science ®Google Scholar
• NIH. clinicaltrials.gov. US National Library of Medicine, Bethesda, MD 20894 ; 2017.
   Google Scholar
• Lalani AA, Bossé D, McGregor BA, et al. Immunotherapy in the elderly. Eur Urol Focus. 2017;3:403–412.
   PubMedGoogle Scholar
• Powles T, Staehler M, Ljungberg B, et al. Updated EAU guidelines for clear cell renal cancer patients who fail VEGF targeted therapy. Eur Urol. 2016;69:4–6.
   PubMed Web of Science ®Google Scholar
• Weber JS, Kudchadkar RR, Yu B, et al. Safety, efficacy, and biomarkers of nivolumab with vaccine in ipilimumab-refractory or -naive melanoma. J Clin Oncol. 2013;31:4311–4318.
   PubMed Web of Science ®Google Scholar
• Hammers HJ. Hammers recommends revisiting vaccines in renal cell carcinoma, A. Welch, editor. Target Oncol. 2017.
   Google Scholar