Optimal Choice of Adjuvant Treatment for Renal Cell Carcinoma Following Nephrectomy

References

• Sung H, Ferlay J, Siegel RL, et al. Global cancer statistics 2020: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA a Cancer J Clin. 2021;71(3):209–249. doi:10.3322/caac.21660
   PubMed Web of Science ®Google Scholar
• AIOM, AIRTUM. NUMBERS OF CANCER IN ITALY. EDITION; 2021. Available from: https://www.aiom.it/wp-content/uploads/2021/11/2021_NDC.pdf. Accessed October 13, 2022.
   Google Scholar
• 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. doi:10.1056/NEJMoa1803675
   PubMed Web of Science ®Google Scholar
• Stellato M, Santini D, Verzoni E, et al. Impact of previous nephrectomy on clinical outcome of metastatic renal carcinoma treated with immune-oncology: a real-world study on behalf of Meet-URO Group (MeetUro-7b). Front Oncol. 2021;11:682449. doi:10.3389/fonc.2021.682449
   PubMed Web of Science ®Google Scholar
• 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. 2019;5(2):164. doi:10.1001/jamaoncol.2018.5543
   PubMed Web of Science ®Google Scholar
• The American Cancer Society medical and editorial content team. Kidney cancer early detection, diagnosis, and staging; 2020. Available from: https://www.cancer.org/content/dam/CRC/PDF/Public/8661.00.pdf. Accessed July 3, 2022.
   Google Scholar
• Gebrosky NP, Koukol S, Nseyo UO, Carpenter C, Lamm DL, Novick AC. Treatment of renal cell carcinoma with 5-fluorouracil and alfa-interferon. Urology. 1997;50(6):863–868. doi:10.1016/S0090-4295(97)00542-6
   PubMed Web of Science ®Google Scholar
• Fosså SD, Droz JP, Pavone-Macaluso MM, Debruyne FJJ, Vermeylen K, Sylvester R. Vinblastine in metastatic renal cell carcinoma: EORTC Phase II Trial 30882. Eur J Cancer. 1992;28(4–5):878–880. doi:10.1016/0959-8049(92)90139-S
   Web of Science ®Google Scholar
• Galligioni E, Quaia M, Merlo A, et al. Adjuvant immunotherapy treatment of renal carcinoma patients with autologous tumor cells and bacillus Calmette-Guèrin: five-year results of a prospective randomized study. Cancer. 1996;77(12):2560–2566. doi:10.1002/(SICI)1097-0142(19960615)77:12<2560::AID-CNCR20>3.0.CO;2-P
   PubMed Web of Science ®Google Scholar
• 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. doi:10.1016/S0140-6736(16)00559-6
   PubMed Web of Science ®Google Scholar
• 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. doi:10.1001/jamaoncol.2017.0076
   PubMed Web of Science ®Google Scholar
• Ravaud A, Motzer RJ, Pandha HS, et al. Adjuvant sunitinib in high-risk renal-cell carcinoma after nephrectomy. N Engl J Med. 2016;375(23):2246–2254. doi:10.1056/NEJMoa1611406
   PubMed Web of Science ®Google Scholar
• Motzer RJ, Ravaud A, Patard JJ, et al. Adjuvant sunitinib for high-risk renal cell carcinoma after nephrectomy: subgroup analyses and updated overall survival results. Eur Urol. 2018;73(1):62–68. doi:10.1016/j.eururo.2017.09.008
   PubMed Web of Science ®Google Scholar
• Food and Drug Administration. FDA approves sunitinib malate for adjuvant treatment of renal cell carcinoma; 2018. Available from: https://www.fda.gov/drugs/resources-information-approved-drugs/fda-approves-sunitinib-malate-adjuvant-treatment-renal-cell-carcinoma. Accessed July 3, 2022.
   Google Scholar
• Ljungberg B, Albiges L, Bedke J, et al. EAU guidelines. Edn. Presented at the EAU annual congress Amsterdam; 2022. Available from: https://d56bochluxqnz.cloudfront.net/documents/full-guideline/EAU-Guidelines-on-Renal-Cell-Carinoma-2022.pdf. Accessed October 13, 2022.
   Google Scholar
• 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. JCO. 2017;35(35):3916–3923. doi:10.1200/JCO.2017.73.5324
   PubMed Web of Science ®Google Scholar
• Motzer RJ, Russo P, Haas N, et al. Adjuvant pazopanib versus placebo after nephrectomy in patients with localized or locally advanced renal cell carcinoma: final overall survival analysis of the Phase 3 PROTECT trial. Eur Urol. 2021;79(3):334–338. doi:10.1016/j.eururo.2020.12.029
   PubMed Web of Science ®Google Scholar
• Gross-Goupil M, Kwon TG, Eto M, et al. Axitinib versus placebo as an adjuvant treatment of renal cell carcinoma: results from the phase III, randomized ATLAS trial. Ann Oncol. 2018;29(12):2371–2378. doi:10.1093/annonc/mdy454
   PubMed Web of Science ®Google Scholar
• Eisen T, Frangou E, Oza B, et al. Adjuvant sorafenib for renal cell carcinoma at intermediate or high risk of relapse: results from the SORCE randomized Phase III intergroup trial. JCO. 2020;38(34):4064–4075. doi:10.1200/JCO.20.01800
   PubMed Web of Science ®Google Scholar
• Ryan CW, Tangen C, Heath EI, et al. EVEREST: everolimus for renal cancer ensuing surgical therapy—A phase III study (SWOG S0931, NCT01120249). JCO. 2022;40(17_suppl):LBA4500. doi:10.1200/JCO.2022.40.17_suppl.LBA4500
   Web of Science ®Google Scholar
• Motzer RJ, Escudier B, McDermott DF, et al. Nivolumab versus everolimus in advanced renal-cell carcinoma. N Engl J Med. 2015;373(19):1803–1813. doi:10.1056/NEJMoa1510665
   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(14):1277–1290. doi:10.1056/NEJMoa1712126
   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 Engl J Med. 2019;380(12):1116–1127. doi:10.1056/NEJMoa1816714
   PubMed Web of Science ®Google Scholar
• Motzer R, Alekseev B, Rha SY, et al. Lenvatinib plus pembrolizumab or everolimus for advanced renal cell carcinoma. N Engl J Med. 2021;384(14):1289–1300. doi:10.1056/NEJMoa2035716
   PubMed Web of Science ®Google Scholar
• Thomas D, Bello DM. Adjuvant immunotherapy for melanoma. J Surg Oncol. 2021;123(3):789–797. doi:10.1002/jso.26329
   PubMed Web of Science ®Google Scholar
• Choueiri TK, Tomczak P, Park SH, et al. Adjuvant pembrolizumab after nephrectomy in renal-cell carcinoma. N Engl J Med. 2021;385(8):683–694. doi:10.1056/NEJMoa2106391
   PubMed Web of Science ®Google Scholar
• Choueiri TK, Tomczak P, Park SH, et al. Pembrolizumab as post nephrectomy adjuvant therapy for patients with renal cell carcinoma: results from 30-month follow-up of KEYNOTE-564. JCO. 2022;40(6_suppl):290. doi:10.1200/JCO.2022.40.6_suppl.290
   Web of Science ®Google Scholar
• European Medicines Agency. Assessment report – keytruda; 2021. Available from: https://www.ema.europa.eu/en/documents/variation-report/keytruda-h-c-003820-ii-0108-epar-assessment-report-variation_en.pdf. Accessed July 3, 2022.
   Google Scholar
• Uzzo R, Bex A, Rini BI, et al. A phase III study of atezolizumab (atezo) vs placebo as adjuvant therapy in renal cell carcinoma (RCC) patients (pts) at high risk of recurrence following resection (IMmotion010). JCO. 2017;35(15_suppl):TPS4598. doi:10.1200/JCO.2017.35.15_suppl.TPS4598
   Web of Science ®Google Scholar
• Bex A, Russo P, Tomita Y, et al. A phase III, randomized, placebo-controlled trial of nivolumab or nivolumab plus ipilimumab in patients with localized renal cell carcinoma at high-risk of relapse after radical or partial nephrectomy (CheckMate 914). JCO. 2020;38(15_suppl):TPS5099. doi:10.1200/JCO.2020.38.15_suppl.TPS5099
   Google Scholar
• Oza B, Frangou E, Smith B, et al. RAMPART: a phase III multi-arm multi-stage trial of adjuvant checkpoint inhibitors in patients with resected primary renal cell carcinoma (RCC) at high or intermediate risk of relapse. Contemp Clin Trials. 2021;108:106482. doi:10.1016/j.cct.2021.106482
   PubMed Web of Science ®Google Scholar
• Choueiri TK, Bedke J, Karam JA, et al. LITESPARK-022: a phase 3 study of pembrolizumab + belzutifan as adjuvant treatment of clear cell renal cell carcinoma (ccRCC). JCO. 2022;40(16_suppl):TPS4602. doi:10.1200/JCO.2022.40.16_suppl.TPS4602
   Web of Science ®Google Scholar
• Ahrens M, Scheich S, Hartmann A, Bergmann L; IAG-N Interdisciplinary Working Group Kidney Cancer of the German Cancer Society. Non-clear cell renal cell carcinoma - pathology and treatment options. Oncol Res Treat. 2019;42(3):128–135. doi:10.1159/000495366
   PubMed Web of Science ®Google Scholar
• Dutcher JP, de Souza P, McDermott D, et al. Effect of temsirolimus versus interferon-α on outcome of patients with advanced renal cell carcinoma of different tumor histologies. Med Oncol. 2009;26(2):202–209. doi:10.1007/s12032-009-9177-0
   PubMed Web of Science ®Google Scholar
• Motzer RJ, Barrios CH, Kim TM, et al. Phase II randomized trial comparing sequential first-line everolimus and second-line sunitinib versus first-line sunitinib and second-line everolimus in patients with metastatic renal cell carcinoma. JCO. 2014;32(25):2765–2772. doi:10.1200/JCO.2013.54.6911
   PubMed Web of Science ®Google Scholar
• Armstrong AJ, Halabi S, Eisen T, et al. Everolimus versus sunitinib for patients with metastatic non-clear cell renal cell carcinoma (ASPEN): a multicentre, open-label, randomised Phase 2 trial. Lancet Oncol. 2016;17(3):378–388. doi:10.1016/S1470-2045(15)00515-X
   PubMed Web of Science ®Google Scholar
• Escudier B, Molinie V, Bracarda S, et al. Open-label phase 2 trial of first-line everolimus monotherapy in patients with papillary metastatic renal cell carcinoma: RAPTOR final analysis. Eur J Cancer. 2016;69:226–235. doi:10.1016/j.ejca.2016.08.004
   PubMed Web of Science ®Google Scholar
• Koh Y, Lim HY, Ahn JH, et al. Phase II trial of everolimus for the treatment of nonclear-cell renal cell carcinoma. Ann Oncol. 2013;24(4):1026–1031. doi:10.1093/annonc/mds582
   PubMed Web of Science ®Google Scholar
• Buti S, Bersanelli M, Maines F, et al. First-line PAzopanib in NOn–clear-cell renal cArcinoMA: the Italian Retrospective Multicenter PANORAMA Study. Clin Genitourin Cancer. 2017;15(4):e609–e614. doi:10.1016/j.clgc.2016.12.024
   PubMed Web of Science ®Google Scholar
• Matrana MR, Duran C, Shetty A, et al. Outcomes of patients with metastatic clear-cell renal cell carcinoma treated with pazopanib after disease progression with other targeted therapies. Eur J Cancer. 2013;49(15):3169–3175. doi:10.1016/j.ejca.2013.06.003
   PubMed Web of Science ®Google Scholar
• Jay R, McKay R, Werner L, et al. Phase 2 trial of sunitinib and gemcitabine in patients with sarcomatoid and/or poor-risk metastatic renal cell carcinoma. Michaelson MD, McKay RR, Werner L, Atkins MB, Van Allen EM, Olivier KM, Song J, Signoretti S, McDermott DF, Choueiri TK.Cancer. 2015 Oct 1;121(19):3435–3443. [Epub 2015 Jun 8]. Urol Oncol. 2017;35(3):117–118. doi:10.1016/j.urolonc.2016.12.023
   Google Scholar
• Twardowski PW, Tangen CM, Wu X, et al. Parallel (randomized) Phase II evaluation of tivantinib (ARQ197) and tivantinib in combination with erlotinib in papillary renal cell carcinoma: SWOG S1107. KCA. 2017;1(2):123–132. doi:10.3233/KCA-170018
   Google Scholar
• Procopio G, Apollonio G, Cognetti F, et al. Sorafenib versus observation following radical metastasectomy for clear-cell renal cell carcinoma: results from the Phase 2 randomized open-label RESORT Study. Eur Urol Oncol. 2019;2(6):699–707. doi:10.1016/j.euo.2019.08.011
   PubMed Web of Science ®Google Scholar
• Harshman LC, Puligandla M, Haas NB, et al. PROSPER: a phase III randomized study comparing perioperative nivolumab (nivo) versus observation in patients with localized renal cell carcinoma (RCC) undergoing nephrectomy (ECOG-ACRIN 8143). JCO. 2019;37(7_suppl):TPS684. doi:10.1200/JCO.2019.37.7_suppl.TPS684
   Web of Science ®Google Scholar
• Shen C, Kaelin WG. The VHL/HIF axis in clear cell renal carcinoma. Semin Cancer Biol. 2013;23(1):18–25. doi:10.1016/j.semcancer.2012.06.001
   PubMed Web of Science ®Google Scholar
• Courtney KD, Infante JR, Lam ET, et al. Phase I dose-escalation trial of pt2385, a first-in-class hypoxia-inducible factor-2α antagonist in patients with previously treated advanced clear cell renal cell carcinoma. JCO. 2018;36(9):867–874. doi:10.1200/JCO.2017.74.2627
   PubMed Web of Science ®Google Scholar
• Choueiri TK, Bauer TM, Papadopoulos KP, et al. Inhibition of hypoxia-inducible factor-2α in renal cell carcinoma with belzutifan: a Phase 1 trial and biomarker analysis. Nat Med. 2021;27(5):802–805. doi:10.1038/s41591-021-01324-7
   PubMed Web of Science ®Google Scholar
• Han G, Stevens C, Cao Z, et al. Abstract 4022: PT2385, a novel HIF-2α antagonist, combines with checkpoint inhibitor antibodies to inhibit tumor growth in preclinical models by modulating myeloid cells and enhancing T cell infiltration. Cancer Res. 2016;76(14_Supplement):4022. doi:10.1158/1538-7445.AM2016-4022
   Web of Science ®Google Scholar
• Alt AL, Boorjian SA, Lohse CM, Costello BA, Leibovich BC, Blute ML. Survival after complete surgical resection of multiple metastases from renal cell carcinoma. Cancer. 2011;117(13):2873–2882. doi:10.1002/cncr.25836
   PubMed Web of Science ®Google Scholar
• Kavolius JP, Mastorakos DP, Pavlovich C, Russo P, Burt ME, Brady MS. Resection of metastatic renal cell carcinoma. JCO. 1998;16(6):2261–2266. doi:10.1200/JCO.1998.16.6.2261
   PubMed Web of Science ®Google Scholar
• Vogl UM, Zehetgruber H, Dominkus M, et al. Prognostic factors in metastatic renal cell carcinoma: metastasectomy as independent prognostic variable. Br J Cancer. 2006;95(6):691–698. doi:10.1038/sj.bjc.6603327
   PubMed Web of Science ®Google Scholar
• Tang C, Msaouel P, Hara K, et al. Definitive radiotherapy in lieu of systemic therapy for oligometastatic renal cell carcinoma: a single-arm, single-centre, feasibility, phase 2 trial. Lancet Oncol. 2021;22(12):1732–1739. doi:10.1016/S1470-2045(21)00528-3
   PubMed Web of Science ®Google Scholar
• Mennitto A, Verzoni E, Cognetti F, et al. Radical metastasectomy followed by sorafenib versus observation in patients with clear cell renal cell carcinoma: extended follow -up of efficacy results from the randomized phase II RESORT trial. Expert Rev Clin Pharmacol. 2021;14(2):261–268. doi:10.1080/17512433.2021.1879639
   PubMed Web of Science ®Google Scholar
• Appleman LJ, Puligandla M, Pal SK, et al. Randomized, double-blind phase III study of pazopanib versus placebo in patients with metastatic renal cell carcinoma who have no evidence of disease following metastasectomy: a trial of the ECOG-ACRIN cancer research group (E2810). JCO. 2019;37(15_suppl):4502. doi:10.1200/JCO.2019.37.15_suppl.4502
   Web of Science ®Google Scholar
• Naumov GN, Akslen LA, Folkman J. Role of angiogenesis in human tumor dormancy: animal models of the angiogenic switch. Cell Cycle. 2006;5(16):1779–1787. doi:10.4161/cc.5.16.3018
   PubMed Web of Science ®Google Scholar
• O’Donnell JS, Hoefsmit EP, Smyth MJ, Blank CU, Teng MWL. The Promise of Neoadjuvant Immunotherapy and Surgery for Cancer Treatment. Clin Cancer Res. 2019;25(19):5743–5751. doi:10.1158/1078-0432.CCR-18-2641
   PubMed Web of Science ®Google Scholar
• Choueiri TK, Kaelin WG. Targeting the HIF2–VEGF axis in renal cell carcinoma. Nat Med. 2020;26(10):1519–1530. doi:10.1038/s41591-020-1093-z
   PubMed Web of Science ®Google Scholar
• Food and Drug Administration. FDA approves pembrolizumab for adjuvant treatment of renal cell carcinoma; 2021. Available from: https://www.fda.gov/drugs/resources-information-approved-drugs/fda-approves-pembrolizumab-adjuvant-treatment-renal-cell-carcinoma. Accessed July 3, 2022.
   Google Scholar
• Harshman LC, Xie W, Moreira RB, et al. Evaluation of disease-free survival as an intermediate metric of overall survival in patients with localized renal cell carcinoma: a trial-level meta-analysis: DFS as a metric of overall survival in RCC. Cancer. 2018;124(5):925–933. doi:10.1002/cncr.31154
   PubMed Web of Science ®Google Scholar
• Swami U, Nussenzveig RH, Haaland B, Agarwal N. Revisiting AJCC TNM staging for renal cell carcinoma: quest for improvement. Ann Transl Med. 2019;7(S1):S18–S18. doi:10.21037/atm.2019.01.50
   PubMed Web of Science ®Google Scholar
• Zisman A, Pantuck AJ, Dorey F, et al. Improved prognostication of renal cell carcinoma using an integrated staging system. JCO. 2001;19(6):1649–1657. doi:10.1200/JCO.2001.19.6.1649
   PubMed Web of Science ®Google Scholar
• Patard JJ, Kim HL, Lam JS, et al. Use of the university of California los angeles integrated staging system to predict survival in renal cell carcinoma: an international multicenter study. JCO. 2004;22(16):3316–3322. doi:10.1200/JCO.2004.09.104
   PubMed Web of Science ®Google Scholar
• Leibovich BC, Blute ML, Cheville JC, et al. Prediction of progression after radical nephrectomy for patients with clear cell renal cell carcinoma: a stratification tool for prospective clinical trials. Cancer. 2003;97(7):1663–1671. doi:10.1002/cncr.11234
   PubMed Web of Science ®Google Scholar
• Frank I, Blute ML, Cheville JC, Lohse CM, Weaver AL, Zincke H. 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. 2002;168(6):2395–2400. doi:10.1097/01.ju.0000035885.91935.d5
   PubMed Web of Science ®Google Scholar
• Brooks SA, Brannon AR, Parker JS, et al. ClearCode34: a prognostic risk predictor for localized clear cell renal cell carcinoma. Eur Urol. 2014;66(1):77–84. doi:10.1016/j.eururo.2014.02.035
   PubMed Web of Science ®Google Scholar
• Rini B, Goddard A, Knezevic D, et al. A 16-gene assay to predict recurrence after surgery in localised renal cell carcinoma: development and validation studies. Lancet Oncol. 2015;16(6):676–685. doi:10.1016/S1470-2045(15)70167-1
   PubMed Web of Science ®Google Scholar
• 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. 2018;24(18):4407–4415. doi:10.1158/1078-0432.CCR-18-0323
   PubMed Web of Science ®Google Scholar