Safety evaluation of immune-based combinations in patients with advanced renal cell carcinoma: a systematic review and meta-analysis

References

• Siegel RL, Miller KD, Jemal A. Cancer statistics, 2020. CA Cancer J Clin. 2020;70:7–30.
   PubMed Web of Science ®Google Scholar
• Capitanio U, Montorsi F. Renal cancer. Lancet. 2016;387:894–906.
   PubMed Web of Science ®Google Scholar
• 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;30:843–852.
   PubMed Web of Science ®Google Scholar
• Huang JJ, Hsieh JJ. The therapeutic landscape of renal cell carcinoma: from the dark age to the golden age. Semin Nephrol. 2020;40:28–41.
   PubMed Web of Science ®Google Scholar
• [ cited 2020 Apr 14]. Available from: https://www.esmo.org/guidelines/genitourinary-cancers/renal-cell-carcinoma/eupdate-renal-cell-carcinoma-treatment-recommendations
   Google Scholar
• Albiges L, Powles T, Staehler M, et al. Updated European association of urology guidelines on renal cell carcinoma: immune checkpoint inhibition is the new backbone in first-line treatment of metastatic clear-cell renal cell carcinoma. Eur Urol. 2019;76:151–156.
   PubMed Web of Science ®Google Scholar
• Motzer RJ, Jonasch E, Michaelson MD, et al. NCCN guidelines insights: kidney cancer, version 2.2020. J Natl Compr Canc Netw. 2019;17:1278–1285.
   PubMed Web of Science ®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
• Rini BI, Plimack ER, Stus V, et al. Pembrolizumab plus axitinib versus sunitinib for advanced renal-cell carcinoma. N Eng J Med. 2019;380:1116–1127.
   PubMed Web of Science ®Google Scholar
• Heng DY, Xie W, Regan MM, et al. External validation and comparison with other models of the international metastatic renal-cell carcinoma database consortium prognostic model: a population-based study. Lancet Oncol. 2013;14:141–148.
   PubMed Web of Science ®Google Scholar
• Motzer RJ, Rini BI, McDermott DF, et al. Nivolumab plus ipilimumab versus sunitinib in first-line treatment for advanced renal cell carcinoma: extended follow-up of efficacy and safety results from a randomised, controlled, phase 3 trial. Lancet Oncol. 2019;20:1370–1385.
   PubMed Web of Science ®Google Scholar
• Escudier B, Motzer RJ, Tannir NM, et al. Efficacy of nivolumab plus ipilimumab according to number of IMDC risk factors in CheckMate 214. Eur Urol. 2020;77:449–453.
   PubMed Web of Science ®Google Scholar
• Rini BI, Powles T, Atkins MB, et al. Atezolizumab plus bevacizumab versus sunitinib in patients with previously untreated metastatic renal cell carcinoma (IMmotion-151): a multicentre, open-label, phase 3, randomised controlled trial. Lancet. 2019;393:2404–2415.
   PubMed Web of Science ®Google Scholar
• Motzer RJ, Penkov K, Haanen J, et al. Avelumab plus axitinib versus sunitinib for advanced renal-cell carcinoma. N Engl J Med. 2019;380:1103–1115.
   PubMed Web of Science ®Google Scholar
• Park R, Lopes L, Cristancho CR, et al. Treatment-related adverse events of combination immune checkpoint inhibitors: systematic review and meta-analysis. Front Oncol. 2020;10:258.
   PubMed Web of Science ®Google Scholar
• Moher D, Liberati A, Tetzlaff J, et al., PRISMA Group. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. PLoS Med. 2009;6(7):e10000097.
   Web of Science ®Google Scholar
• Higgins JPT, Thomas J, Chandler J, et al., editors. Cochrane handbook for systematic reviews of interventions. 2nd ed. Chichester (UK): John Wiley & Sons; 2019.
   Google Scholar
• [ cited 2020 Apr 14]. Available from: https://ctep.cancer.gov/protocolDevelopment/electronic_applications/docs/ctcaev3.pdf
   Google Scholar
• [ cited 2020 Apr 14]. Available from: https://www.eortc.be/services/doc/ctc/CTCAE_4.03_2010-06-14_QuickReference_5x7.pdf
   Google Scholar
• McDermott DF, Huseni MA, Atkins MB, et al. Clinical activity and molecular correlates of response to atezolizumab alone or in combination with bevacizumab versus sunitinib in renal cell carcinoma. Nat Med. 2018;24:749–757.
   PubMed Web of Science ®Google Scholar
• Vogelzang NJ. Treatment options in metastatic renal carcinoma: an embarrassment of riches. J Clin Oncol. 2006;24:1–3.
   PubMed Web of Science ®Google Scholar
• Escudier B. Combination therapy as first-line treatment in metastatic renal-cell carcinoma. N Engl J Med. 2019;380:1176–1178.
   PubMed Web of Science ®Google Scholar
• Wan X, Zhang Y, Tan C, et al. First-line nivolumab plus ipilimumab vs sunitinib for metastatic renal cell carcinoma: a cost-effectiveness analysis. JAMA Oncol. 2019;5:491–496.
   PubMed Web of Science ®Google Scholar
• Bensimon AG, Zhong Y, Swami U, et al. Cost-effectiveness of pembrolizumab in combination with axitinib as first-line treatment for advanced renal cell carcinoma. J Clin Oncol. 2020;38(no.6_suppl):716.
   Web of Science ®Google Scholar
• Lu P, Liang W, Li J, et al. A cost-effectiveness analysis: first-line avelumab plus axitinib versus sunitinib for advanced renal-cell carcinoma. Front Pharmacol. 2020;11:619.
   PubMed Web of Science ®Google Scholar
• Esfahani K, Elkrief A, Calabrese C, et al. Moving towards personalized treatments of immune-related adverse events. Nat Rev Clin Oncol. 2020 published online ahead of print 2020 Apr 3. DOI:https://doi.org/10.1038/s41571-020-0352-8
   Google Scholar
• Oh DY, Cham J, Zhang L, et al. Immune toxicities elicited by CTLA-4 blockade in cancer patients are associated with early diversification of the T-cell repertoire. Cancer Res. 2017;77:1322–1330.
   PubMed Web of Science ®Google Scholar
• Subudhi SK, Aparicio A, Gao J, et al. Clonal expansion of CD8 T cells in the systemic circulation precedes development of ipilimumab-induced toxicities. Proc Natl Acad Sci USA. 2016;113:11919–11924.
   PubMed Web of Science ®Google Scholar
• Lim SY, Lee JH, Gide TN, et al. Circulating cytokines predict immune-related toxicity in melanoma patients receiving anti-PD-1-based immunotherapy. Clin Cancer Res. 2019;25:1557–1563.
   PubMed Web of Science ®Google Scholar
• Dudani S, Savard MF, Heng DYC. An update on predictive biomarkers in metastatic renal cell carcinoma. Eur Urol Focus. 2020;6:34–36.
   PubMedGoogle Scholar
• Beuselinck B, Verbiest A, Couchy G, et al. Tumor molecular characteristics in patients (pts) with international metastatic renal cell carcinoma database consortium (IMDC) good (G) and intermediate/poor (I/P) risk. Ann Oncol. 2018;29(Suppl.8):viii303–31.
   Google Scholar
• Beuselinck B, Job S, Becht E, et al. Molecular subtypes of clear cell renal cell carcinoma are associated with sunitinib response in the metastatic setting. Clin Cancer Res. 2015;21:1329–1339.
   PubMed Web of Science ®Google Scholar
• Hellmann MD, Paz-Ares L, Bernabe Caro R, et al. Nivolumab plus ipilimumab in advanced non-small-cell lung cancer. N Engl J Med. 2019;381:2020–2031.
   PubMed Web of Science ®Google Scholar
• Ready NE, Ott PA, Hellmann MD, et al. Nivolumab monotherapy and nivolumab plus ipilimumab in recurrent small cell lung cancer: results from the CheckMate-032 randomized cohort. J Thorac Oncol. 2020;15:426–435.
   PubMed Web of Science ®Google Scholar
• Sharma P, Siefker-Radtke A, de Braud F, et al. Nivolumab alone and with ipilimumab in previously treated metastatic urothelial carcinoma: checkMate-032 nivolumab 1 mg/kg plus ipilimumab 3 mg/kg expansion cohort results. J Clin Oncol. 2019;37:1608–1616.
   PubMed Web of Science ®Google Scholar
• Larkin J, Chiarion-Sileni V, Gonzalez R, et al. Five-year survival with combined nivolumab and ipilimumab in advanced melanoma. N Engl J Med. 2019;381:1535–1546.
   PubMed Web of Science ®Google Scholar
• Larkin J, Chiarion Sileni V, Gonzalez R, et al. Combined nivolumab and ipilimumab or monotherapy in untreated melanoma. N Engl J Med. 2015;373:23–34.
   PubMed Web of Science ®Google Scholar
• Hodi FS, Chesney J, Pavlick AC, et al. Two-year overall survival rates from a randomised phase 2 trial evaluating the combination of nivolumab and ipilimumab versus ipilimumab alone in patients with advanced melanoma. Lancet Oncol. 2016;17:1558–1568.
   PubMed Web of Science ®Google Scholar
• Long GV, Atkinson V, Lo S, et al. Combination nivolumab and ipilimumab or nivolumab alone in melanoma brain metastases: a multicenter randomised phase 2 study. Lancet Oncol. 2018;19:672–681.
   PubMed Web of Science ®Google Scholar
• Omuro A, Vlahovic G, Lim M, et al. Nivolumab with or without ipilimumab in patients with recurrent glioblastoma: results from exploratory phase I cohorts of CheckMate-143. Neuro Oncol. 2018;20:674–686.
   PubMed Web of Science ®Google Scholar
• D’Angelo SP, Mahoney MR, Van Tine BA, et al. Nivolumab with or without ipilimumab treatment for metastatic sarcoma (Alliance A091401): two open-label, non-comparative, randomised, phase 2 trials. Lancet Oncol. 2018;19:416–426.
   PubMed Web of Science ®Google Scholar
• Janjigian YY, Bendell J, Calvo E, et al. CheckMate-032 study: efficacy and safety of nivolumab and nivolumab plus ipilimumab in patients with metastatic esophagogastric cancer. J Clin Oncol. 2018;36:2836–2844.
   PubMed Web of Science ®Google Scholar
• Scherpereel A, Mazieres J, Greillier L, et al. Nivolumab or nivolumab plus ipilimumab in patients with relapsed malignant pleural mesothelioma (IFCT-1501 MAPS2): a multicentre, open-label, randomised, non-comparative, phase 2 trial. Lancet Oncol. 2019;20:239–253.
   PubMed Web of Science ®Google Scholar
• Haanen JBAG, Carbonnel F, Robert C, et al. Management of toxicities from immunotherapy: ESMO clinical practice guidelines for diagnosis, treatment and follow-up. Ann Oncol. 2018:29(Suppl. 4): iv264–6.
   PubMed Web of Science ®Google Scholar
• Boutros C, Tarhini A, Routier E, et al. Safety profiles of anti-CTLA-4 and anti-PD-1 antibodies alone and in combination. Nat Rev Clin Oncol. 2016;13:473–486.
   PubMed Web of Science ®Google Scholar
• Gu L, Khadaroo PA, Su H, et al. The safety and tolerability of combined immune checkpoint inhibitors (anti-PD-1/PD-L1 plus anti-CTLA-4): a systematic review and meta-analysis. BMC Cancer. 2019;19:559.
   PubMed Web of Science ®Google Scholar
• Gupta A, De Felice KM, Loftus EV Jr, et al. Systematic review: colitis associated with anti-CTLA-4 therapy. Aliment Pharmacol Ther. 2015;42:406–417.
   PubMed Web of Science ®Google Scholar
• Cella D, Grünwald V, Escudier B, et al. Patient-reported outcomes of patients with advanced renal cell carcinoma treated with nivolumab plus ipilimumab versus sunitinib (CheckMate-214): a randomised, phase 3 trial. Lancet Oncol. 2019;20:297–310.
   PubMed Web of Science ®Google Scholar
• Atkins MB, Rini BI, Motzer RJ, et al. Patient-reported outcomes from the phase 3 randomized IMmotion-151 trial: atezolizumab + bevacizumab vs sunitinib in treatment-naive metastatic renal cell carcinoma. Clin Cancer Res. 2020;clincanres.2838:2019. [published online ahead of print 2020 Mar 3].
   Google Scholar