The impact of neoadjuvant immune checkpoint inhibitors on kidney cancer and bladder cancer surgeries: a systematic review
Main Article Content
Abstract
Background: the neoadjuvant use of immune checkpoint inhibitors (ICIs) in patients with kidney cancer and bladder cancer is controversial, and there are reports suggesting increased difficulties in surgeries in these settings.
Aims: we performed a systematic review using PRISMA guidelines methodology to analyze pertinent literature available up to January 05, 2024 in PubMed, updating our previously published systematic review on the subject.
Results: we have selected 25 publications for the neoadjuvant use of different immune checkpoint inhibitors before nephrectomies for kidney cancer and seven publications concerning the neoadjuvant use of immune checkpoint inhibitors before cystectomies for bladder cancer. Reports of additional surgical difficulties were noted in 6/25 reports for kidney cancer and 0/7 reports for bladder cancer.
Conclusions: in the setting of neoadjuvant immune checkpoint inhibitors, a minority of cases of nephrectomies may be challenging due to inflammatory changes to the surrounding tissues, which may require more experienced surgeons. Neoadjuvant immune checkpoint inhibitors do not seem to pose additional surgical difficulties in cystectomies for the treatment of bladder cancer.
Article Details
How to Cite
NASPOLINI, Gabriel Zanette et al.
The impact of neoadjuvant immune checkpoint inhibitors on kidney cancer and bladder cancer surgeries: a systematic review.
Medical Research Archives, [S.l.], v. 12, n. 6, june 2024.
ISSN 2375-1924.
Available at: <https://esmed.org/MRA/mra/article/view/5376>. Date accessed: 02 july 2024.
doi: https://doi.org/10.18103/mra.v12i6.5376.
Section
Review Articles
The Medical Research Archives grants authors the right to publish and reproduce the unrevised contribution in whole or in part at any time and in any form for any scholarly non-commercial purpose with the condition that all publications of the contribution include a full citation to the journal as published by the Medical Research Archives.
References
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5. Shapiro DD, Karam JA, Zemp L, et al. Cytoreductive Nephrectomy Following Immune Checkpoint Inhibitor Therapy Is Safe and Facilitates Treatment-free Intervals. Eur Urol Open Sci. 2023;50:43-46. doi:10.1016/j. euros.2023.01.016
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7. Singla N, Elias R, Ghandour RA, et al. Pathologic response and surgical outcomes in patients undergoing nephrectomy following receipt of immune checkpoint inhibitors for renal cell carcinoma. Urol Oncol. 2019;37 :924–931. doi:10.1016/ j.urolonc.2019.08.012.
8. Merseburger AS, Apolo AB, Chowdhury S, et al. SIU-ICUD recommendations on bladder cancer: systemic therapy for metastatic bladder cancer. World J Urol. 2019;37(1):95-105. doi:10.1007/s00345-018-2486-1
9. Petzold AP, Lubianca FN, Passos LG, et al. The impact of preoperative immune checkpoint inhibitors on kidney and bladder cancer surgeries: a systematic review. Curr Probl Cancer 2022; 46(1):100765. 10.1016/j.currpro blcancer.2021.100765
10. Ouzzani, Mourad, Hossam Hammady, Zbys Fedorowicz, and Ahmed Elmagarmid. 2016. “Rayyan-a Web and Mobile App for Systematic Reviews.” Systematic Reviews 5 (1): 210.
11. Page MJ, McKenzie JE, Bossuyt PM, Boutron I, Hoffmann TC, Mulrow CD, et al. The PRISMA 2020 statement: an updated guideline for reporting systematic reviews. BMJ 2021;372:n71
12. Woldu SL, Brugarolas J, Kapur P, Margulis V. What is the role of nephrectomy following complete response to check- point inhibitors? Urol case rep. 2018;18:60–63. doi:10.1016/j.eucr.2018.02.016.
13. Ikarashi D, Kato Y, Katagiri H, et al. Case of complete response to neoadjuvant therapy using nivolumab in a patient with metastatic renal cell carcinoma. Int J Urol. 2018;25:630–632. doi:10.1111/iju.13590.
14. Fallah J, Diaz-Montero CM, Rayman PA, et al. Neoadjuvant durvalumab +/- tremelimumab affects the expression of immune checkpoint (IC) molecules on myeloid derived suppressor cells (MDSC) in patients (pts) with locally advanced renal cell carcinoma (RCC). J Clin Oncol. 2019;37(7_suppl):587 -587. doi:10.1200/JCO.2019.37.7_suppl.587.
15. Labbate C, Hatogai K, Werntz R, et al. Complete response of renal cell carcinoma vena cava tumour thrombus to neoadjuvant immunotherapy. J Immunother Cancer. 2019;7:66. doi:10.1186/s40425-019-0546-8.
16. Shepherd A, Joshi R, Tan CP, Cohen P, Brook NR. Inferior vena cava thrombectomy following complete response to nivolumab/ ipilimumab for metastatic renal cell carcinoma. ANZ J Surg. 2020;90:1517–1519. doi:10.1111/ans.15608.
17. Okada T, Hamamoto S, Etani T, et al. Complete response of renal cell carcinoma with an inferior vena cava tumour thrombus and lung metastases after treatment with nivolumab plus ipilimumab. Int cancer conferen J. 2020;9:88–91.doi:10.1007/s13691-020-00403-9.
18. Singla N, Hutchinson RC, Ghandour RA, et al. Improved survival after cytoreductive nephrectomy for metastatic renal cell carcinoma in the contemporary immunotherapy era: An analysis of the national cancer database. Urol Oncol.2020;38:604 e9–604.e17. doi:10.1016/ j.urolonc.2020.02.029.
19. Shapiro D, Westerman M, Tannir N, et al. Preoperative checkpoint inhibitors are not associated with increased surgical complications compared to preoperative tyrosine kinase inhibitors or upfront cytoreductive nephrectomy. J Urol.2020;203(4_suppl):811–812. doi:10.1097/JU.0000000000000918.08.
20. de Joode K, de Ruig-Spakman JI, Baktawar SS, van Leenders G, Verhagen P, van der Veldt A. Nivolumab plus ipilimumab as neoadjuvant treatment in primary advanced renal cell tumors: Cutting edges for cutting-edge surgery.Urol Oncol. 2020;38:553–554. doi:10.1016/j.urolonc.2020.01.009.
21. Nishimura K, Miura N, Sugihara N, et al. Sequential immune-targeted surgical therapy resulted in disease-free survival in a case with advanced renal cell carcinoma. BMC Urol. 2021;21(1):124. doi:10.1186/s12894-021-008 91-8
22. Sazuka T, Fujimoto A, Sato H, et al. Expression of tertiary lymphoid structure in deferred cytoreductive nephrectomy of metastatic renal cell carcinoma treated with nivolumab plus ipilimumab. IJU Case Rep. 2021;4(6):355-358. doi:10.1002/iju5.12347
23. Zhuang TZ, Harik L, Force S, et al. Durable complete response for oligometastatic renal cell carcinoma with immune checkpoint inhibition and cytoreductive nephrectomy in a Jehovah's witness: A case report. Front Oncol. 2022;12:949400. Published 2022 Dec 2. doi:10.3389/fonc.2022.949400
24. Uematsu T, Kijima T, Takada-Owada A, Nishihara D, Ishida K, Kamai T. Presurgical avelumab plus axitinib in an immunosenescent octogenarian with renal cell carcinoma invading the vena cava. Urol Case Rep. 2022;45:102205. doi:10.1016/j.eucr.2022.102205
25. Mebroukine S, Yacoub M, Michiels C, Ravaud A, Gross-Goupil M, Bernhard JC. Feasibility of robotic-assisted partial nephrectomy for complete remission of metastatic renal cell carcinoma after long exposure to immune checkpoint inhibitors (UroCCR-106). J Surg Case Rep. 2022;2022 (12):rjac560. doi:10.1093/jscr/rjac560
26. Yoshino M, Ishihara H, Nemoto Y, et al. Therapeutic role of deferred cytoreductive nephrectomy in patients with metastatic renal cell carcinoma treated with nivolumab plus ipilimumab. Jpn J Clin Oncol. 2022;52(10): 1208-1214. doi:10.1093/jjco/hyac099
27. Yoshida K, Hata K, Iizuka J, et al. Immune Checkpoint Inhibitor Combination Therapy for Renal Cell Carcinomas With Concomitant Inferior Vena Cava Thrombi. In Vivo. 2022;36 (2):1030-1034. doi:10.21873/invivo.12798
28. Pignot G, Thiery-Vuillemin A, Albigès L, et al. Oncological Outcomes of Delayed Nephrectomy After Optimal Response to Immune Checkpoint Inhibitors for Metastatic Renal Cell Carcinoma. Eur Urol Oncol. 2022;5 (5):577-584. doi:10.1016/j.euo.2022.07.002
29. Otsuka H, Masui K, Hosomi T, Makino Y, Shibasaki N, Shichiri Y. Preoperative ipilimumab/nivolumab combination therapy reduced operation risk by downstaging the inferior vena cava tumor thrombus extending to the right atrium in a metastatic renal cell carcinoma: A case report. Urol Case Rep. 2021;40:101912. Published 2021 Oct 23.
30. Carlo MI, Attalla K, Mazaheri Y, et al. Phase II Study of Neoadjuvant Nivolumab in Patients with Locally Advanced Clear Cell Renal Cell Carcinoma Undergoing Nephrectomy. Eur Urol. 2022;81(6):570-573. doi:10.1016/j.eururo.2022.01.043
31. Karam JA, Msaouel P, Haymaker CL, et al. Phase II trial of neoadjuvant sitravatinib plus nivolumab in patients undergoing nephrectomy for locally advanced clear cell renal cell carcinoma. Nat Commun. 2023;14 (1):2684. doi:10.1038/s41467-023-38342-7
32. Machida A, Ikarashi D, Yanagawa N, et al. Pathological Complete Response to Preoperative Nivolumab Plus Cabozantinib for Renal Cell Carcinoma With Inferior Vena Cava Thrombus: A Case Report. Cancer Diagn Progn. 2023;3(1):124-129. doi:10.21873/cdp .10189
33. Reese SW, Eismann L, White C, et al. Surgical outcomes of cytoreductive nephrectomy in patients receiving systemic immunotherapy for advanced renal cell carcinoma. Urol Oncol. 2024;42(2):32.e9-32.e16. doi:10.1016/j.urolonc.2023.12.003
34. Bhanji Y, Baraban E, Antonucci B, Ged Y, Singla N. Robotic-assisted cytoreductive partial nephrectomy for metastatic sarcomatoid renal cell carcinoma following dramatic response to combination immunotherapy in a young female. Kidney Cancer J. 2023;21(2):15-18.v.
35. Scuderi S, Gandaglia G, Fossati N, et al. Comparison of peri-operative complications according to surgical approach and urinary diversion in patients treated with neoadjuvant pembrolizumab (pure-01) and radical cystectomy for mibc. J Urol. 2019;201(4_suppl). doi:10.1097/01.JU.0000557161.13435.f6.
36. Gao J, Siefker-Radtke AO, Navai N, et al. A pilot presurgical study evaluating anti-PD-L1 durvalumab (durva) plus anti- CTLA-4 tremelimumab (treme) in patients (pts) with high-risk muscle-invasive bladder carcinoma (MIBC) who are ineligible for cisplatin-based neoadjuvant chemotherapy (NAC). J Clin Oncol. 2019;37(15_suppl (May 20, 2019)): 4551 -4551. doi:10.1200/JCO.2019.37.15_s uppl.4551.
37. Powles T, Kockx M, Rodriguez-Vida A, et al. Clinical efficacy and biomarker analysis of neoadjuvant atezolizumab in operable urothelial carcinoma in the ABACUS trial. Nat Med. 2019;25:1706–1714. doi:10.1038/s415 91-019-0628-7.
38. Briganti A, Gandaglia G, Scuderi S, et al. Surgical safety of radical cystectomy and pelvic lymph node dissection following neoadjuvant pembrolizumab in patients with bladder cancer: prospective assessment of perioperative out- comes from the PURE-01 Trial. Eur Urol. 2020;77:576–580. doi:10.1016 /j.eururo.2019.12.019.
39. Truong H, Hardacker T, Mark J, Lallas C, Gomella L, Trabulsi E. Surgical complications associated with pre- operative immunotherapy for muscle invasive bladder cancer. J Urol. 2020;203(4_suppl):354–355. doi:10.1097/JU. 0000000000000857.017.
40. Juan Francisco Rodriguez-Moreno et al., Impact of the combination of durvalumab (MEDI4736) plus olaparib (AZD2281) administered prior to surgery in the molecular profile of resectable urothelial bladder cancer: NEODURVARIB Trial.. JCO 38, 542-542(2020).doi:10.1200/JCO.2020.38.6_suppl.542
41. Szabados B, Rodriguez-Vida A, Durán I, et al. Toxicity and Surgical Complication Rates of Neoadjuvant Atezolizumab in Patients with Muscle-invasive Bladder Cancer Undergoing Radical Cystectomy: Updated Safety Results from the ABACUS Trial. Eur Urol Oncol. 2021; 4(3):456-463. doi:10.1016/j.euo.2020.11.010
42. Rini BI, Battle D, Figlin RA, et al. The society for immunotherapy of cancer consensus statement on immunotherapy for the treatment of advanced renal cell carcinoma (RCC). J Immunother Cancer. 2019;7(1):354. doi:10.1186/s40425-019-0813-8.
43. Motzer RJ, Jonasch E, Agarwal N, et al. NCCN Guidelines® Insights: Kidney Cancer, Version 2.2024. J Natl Compr Canc Netw. 2024;22(1):4-16. doi:10.6004/jnccn.2024.0008.
44. Choueiri TK, Tomczak P, Park SH, et al. Overall Survival with Adjuvant Pembrolizumab in Renal-Cell Carcinoma. N Engl J Med. 2024; 390(15):1359-1371. doi:10.1056/NEJMoa231 2695.
45. Powles T, Valderrama BP, Gupta S, et al. Enfortumab Vedotin and Pembrolizumab in Untreated Advanced Urothelial Cancer. N Engl J Med. 2024;390(10):875-888. doi:10.10 56/NEJMoa2312117.
2. Maggiore U, Pascual J. The bad and the good news on cancer immunotherapy: implications for organ transplant recipients. Adv Chronic Kidney Dis. 2016;23:312–316. doi:10.1053/j.ackd.2016.08.002.
3. Rathmell WK, Rumble RB, Van Veldhuizen PJ, et al. Management of Metastatic Clear Cell Renal Cell Carcinoma: ASCO Guideline. J Clin Oncol. 2022;40(25):2957-2995. doi:10.1200/J CO.22.00868
4. Marandino L, Raggi D, Necchi A, Capitanio U. Neoadjuvant Treatment in Renal Cell Carcinoma: Transforming Challenges into Opportunities. Eur Urol. 2022;81(6):574-575. doi:10.1016/j.eururo.2022.02.013
5. Shapiro DD, Karam JA, Zemp L, et al. Cytoreductive Nephrectomy Following Immune Checkpoint Inhibitor Therapy Is Safe and Facilitates Treatment-free Intervals. Eur Urol Open Sci. 2023;50:43-46. doi:10.1016/j. euros.2023.01.016
6. Pignot G, Thiery-Vuillemin A, Walz J, et al. Nephrectomy after complete response to immune checkpoint inhibitors for metastatic renal cell carcinoma: a new surgical challenge? Eur Urol. 2020;77:761–763. doi:10.1016/j.eur uro.2019.12.018.
7. Singla N, Elias R, Ghandour RA, et al. Pathologic response and surgical outcomes in patients undergoing nephrectomy following receipt of immune checkpoint inhibitors for renal cell carcinoma. Urol Oncol. 2019;37 :924–931. doi:10.1016/ j.urolonc.2019.08.012.
8. Merseburger AS, Apolo AB, Chowdhury S, et al. SIU-ICUD recommendations on bladder cancer: systemic therapy for metastatic bladder cancer. World J Urol. 2019;37(1):95-105. doi:10.1007/s00345-018-2486-1
9. Petzold AP, Lubianca FN, Passos LG, et al. The impact of preoperative immune checkpoint inhibitors on kidney and bladder cancer surgeries: a systematic review. Curr Probl Cancer 2022; 46(1):100765. 10.1016/j.currpro blcancer.2021.100765
10. Ouzzani, Mourad, Hossam Hammady, Zbys Fedorowicz, and Ahmed Elmagarmid. 2016. “Rayyan-a Web and Mobile App for Systematic Reviews.” Systematic Reviews 5 (1): 210.
11. Page MJ, McKenzie JE, Bossuyt PM, Boutron I, Hoffmann TC, Mulrow CD, et al. The PRISMA 2020 statement: an updated guideline for reporting systematic reviews. BMJ 2021;372:n71
12. Woldu SL, Brugarolas J, Kapur P, Margulis V. What is the role of nephrectomy following complete response to check- point inhibitors? Urol case rep. 2018;18:60–63. doi:10.1016/j.eucr.2018.02.016.
13. Ikarashi D, Kato Y, Katagiri H, et al. Case of complete response to neoadjuvant therapy using nivolumab in a patient with metastatic renal cell carcinoma. Int J Urol. 2018;25:630–632. doi:10.1111/iju.13590.
14. Fallah J, Diaz-Montero CM, Rayman PA, et al. Neoadjuvant durvalumab +/- tremelimumab affects the expression of immune checkpoint (IC) molecules on myeloid derived suppressor cells (MDSC) in patients (pts) with locally advanced renal cell carcinoma (RCC). J Clin Oncol. 2019;37(7_suppl):587 -587. doi:10.1200/JCO.2019.37.7_suppl.587.
15. Labbate C, Hatogai K, Werntz R, et al. Complete response of renal cell carcinoma vena cava tumour thrombus to neoadjuvant immunotherapy. J Immunother Cancer. 2019;7:66. doi:10.1186/s40425-019-0546-8.
16. Shepherd A, Joshi R, Tan CP, Cohen P, Brook NR. Inferior vena cava thrombectomy following complete response to nivolumab/ ipilimumab for metastatic renal cell carcinoma. ANZ J Surg. 2020;90:1517–1519. doi:10.1111/ans.15608.
17. Okada T, Hamamoto S, Etani T, et al. Complete response of renal cell carcinoma with an inferior vena cava tumour thrombus and lung metastases after treatment with nivolumab plus ipilimumab. Int cancer conferen J. 2020;9:88–91.doi:10.1007/s13691-020-00403-9.
18. Singla N, Hutchinson RC, Ghandour RA, et al. Improved survival after cytoreductive nephrectomy for metastatic renal cell carcinoma in the contemporary immunotherapy era: An analysis of the national cancer database. Urol Oncol.2020;38:604 e9–604.e17. doi:10.1016/ j.urolonc.2020.02.029.
19. Shapiro D, Westerman M, Tannir N, et al. Preoperative checkpoint inhibitors are not associated with increased surgical complications compared to preoperative tyrosine kinase inhibitors or upfront cytoreductive nephrectomy. J Urol.2020;203(4_suppl):811–812. doi:10.1097/JU.0000000000000918.08.
20. de Joode K, de Ruig-Spakman JI, Baktawar SS, van Leenders G, Verhagen P, van der Veldt A. Nivolumab plus ipilimumab as neoadjuvant treatment in primary advanced renal cell tumors: Cutting edges for cutting-edge surgery.Urol Oncol. 2020;38:553–554. doi:10.1016/j.urolonc.2020.01.009.
21. Nishimura K, Miura N, Sugihara N, et al. Sequential immune-targeted surgical therapy resulted in disease-free survival in a case with advanced renal cell carcinoma. BMC Urol. 2021;21(1):124. doi:10.1186/s12894-021-008 91-8
22. Sazuka T, Fujimoto A, Sato H, et al. Expression of tertiary lymphoid structure in deferred cytoreductive nephrectomy of metastatic renal cell carcinoma treated with nivolumab plus ipilimumab. IJU Case Rep. 2021;4(6):355-358. doi:10.1002/iju5.12347
23. Zhuang TZ, Harik L, Force S, et al. Durable complete response for oligometastatic renal cell carcinoma with immune checkpoint inhibition and cytoreductive nephrectomy in a Jehovah's witness: A case report. Front Oncol. 2022;12:949400. Published 2022 Dec 2. doi:10.3389/fonc.2022.949400
24. Uematsu T, Kijima T, Takada-Owada A, Nishihara D, Ishida K, Kamai T. Presurgical avelumab plus axitinib in an immunosenescent octogenarian with renal cell carcinoma invading the vena cava. Urol Case Rep. 2022;45:102205. doi:10.1016/j.eucr.2022.102205
25. Mebroukine S, Yacoub M, Michiels C, Ravaud A, Gross-Goupil M, Bernhard JC. Feasibility of robotic-assisted partial nephrectomy for complete remission of metastatic renal cell carcinoma after long exposure to immune checkpoint inhibitors (UroCCR-106). J Surg Case Rep. 2022;2022 (12):rjac560. doi:10.1093/jscr/rjac560
26. Yoshino M, Ishihara H, Nemoto Y, et al. Therapeutic role of deferred cytoreductive nephrectomy in patients with metastatic renal cell carcinoma treated with nivolumab plus ipilimumab. Jpn J Clin Oncol. 2022;52(10): 1208-1214. doi:10.1093/jjco/hyac099
27. Yoshida K, Hata K, Iizuka J, et al. Immune Checkpoint Inhibitor Combination Therapy for Renal Cell Carcinomas With Concomitant Inferior Vena Cava Thrombi. In Vivo. 2022;36 (2):1030-1034. doi:10.21873/invivo.12798
28. Pignot G, Thiery-Vuillemin A, Albigès L, et al. Oncological Outcomes of Delayed Nephrectomy After Optimal Response to Immune Checkpoint Inhibitors for Metastatic Renal Cell Carcinoma. Eur Urol Oncol. 2022;5 (5):577-584. doi:10.1016/j.euo.2022.07.002
29. Otsuka H, Masui K, Hosomi T, Makino Y, Shibasaki N, Shichiri Y. Preoperative ipilimumab/nivolumab combination therapy reduced operation risk by downstaging the inferior vena cava tumor thrombus extending to the right atrium in a metastatic renal cell carcinoma: A case report. Urol Case Rep. 2021;40:101912. Published 2021 Oct 23.
30. Carlo MI, Attalla K, Mazaheri Y, et al. Phase II Study of Neoadjuvant Nivolumab in Patients with Locally Advanced Clear Cell Renal Cell Carcinoma Undergoing Nephrectomy. Eur Urol. 2022;81(6):570-573. doi:10.1016/j.eururo.2022.01.043
31. Karam JA, Msaouel P, Haymaker CL, et al. Phase II trial of neoadjuvant sitravatinib plus nivolumab in patients undergoing nephrectomy for locally advanced clear cell renal cell carcinoma. Nat Commun. 2023;14 (1):2684. doi:10.1038/s41467-023-38342-7
32. Machida A, Ikarashi D, Yanagawa N, et al. Pathological Complete Response to Preoperative Nivolumab Plus Cabozantinib for Renal Cell Carcinoma With Inferior Vena Cava Thrombus: A Case Report. Cancer Diagn Progn. 2023;3(1):124-129. doi:10.21873/cdp .10189
33. Reese SW, Eismann L, White C, et al. Surgical outcomes of cytoreductive nephrectomy in patients receiving systemic immunotherapy for advanced renal cell carcinoma. Urol Oncol. 2024;42(2):32.e9-32.e16. doi:10.1016/j.urolonc.2023.12.003
34. Bhanji Y, Baraban E, Antonucci B, Ged Y, Singla N. Robotic-assisted cytoreductive partial nephrectomy for metastatic sarcomatoid renal cell carcinoma following dramatic response to combination immunotherapy in a young female. Kidney Cancer J. 2023;21(2):15-18.v.
35. Scuderi S, Gandaglia G, Fossati N, et al. Comparison of peri-operative complications according to surgical approach and urinary diversion in patients treated with neoadjuvant pembrolizumab (pure-01) and radical cystectomy for mibc. J Urol. 2019;201(4_suppl). doi:10.1097/01.JU.0000557161.13435.f6.
36. Gao J, Siefker-Radtke AO, Navai N, et al. A pilot presurgical study evaluating anti-PD-L1 durvalumab (durva) plus anti- CTLA-4 tremelimumab (treme) in patients (pts) with high-risk muscle-invasive bladder carcinoma (MIBC) who are ineligible for cisplatin-based neoadjuvant chemotherapy (NAC). J Clin Oncol. 2019;37(15_suppl (May 20, 2019)): 4551 -4551. doi:10.1200/JCO.2019.37.15_s uppl.4551.
37. Powles T, Kockx M, Rodriguez-Vida A, et al. Clinical efficacy and biomarker analysis of neoadjuvant atezolizumab in operable urothelial carcinoma in the ABACUS trial. Nat Med. 2019;25:1706–1714. doi:10.1038/s415 91-019-0628-7.
38. Briganti A, Gandaglia G, Scuderi S, et al. Surgical safety of radical cystectomy and pelvic lymph node dissection following neoadjuvant pembrolizumab in patients with bladder cancer: prospective assessment of perioperative out- comes from the PURE-01 Trial. Eur Urol. 2020;77:576–580. doi:10.1016 /j.eururo.2019.12.019.
39. Truong H, Hardacker T, Mark J, Lallas C, Gomella L, Trabulsi E. Surgical complications associated with pre- operative immunotherapy for muscle invasive bladder cancer. J Urol. 2020;203(4_suppl):354–355. doi:10.1097/JU. 0000000000000857.017.
40. Juan Francisco Rodriguez-Moreno et al., Impact of the combination of durvalumab (MEDI4736) plus olaparib (AZD2281) administered prior to surgery in the molecular profile of resectable urothelial bladder cancer: NEODURVARIB Trial.. JCO 38, 542-542(2020).doi:10.1200/JCO.2020.38.6_suppl.542
41. Szabados B, Rodriguez-Vida A, Durán I, et al. Toxicity and Surgical Complication Rates of Neoadjuvant Atezolizumab in Patients with Muscle-invasive Bladder Cancer Undergoing Radical Cystectomy: Updated Safety Results from the ABACUS Trial. Eur Urol Oncol. 2021; 4(3):456-463. doi:10.1016/j.euo.2020.11.010
42. Rini BI, Battle D, Figlin RA, et al. The society for immunotherapy of cancer consensus statement on immunotherapy for the treatment of advanced renal cell carcinoma (RCC). J Immunother Cancer. 2019;7(1):354. doi:10.1186/s40425-019-0813-8.
43. Motzer RJ, Jonasch E, Agarwal N, et al. NCCN Guidelines® Insights: Kidney Cancer, Version 2.2024. J Natl Compr Canc Netw. 2024;22(1):4-16. doi:10.6004/jnccn.2024.0008.
44. Choueiri TK, Tomczak P, Park SH, et al. Overall Survival with Adjuvant Pembrolizumab in Renal-Cell Carcinoma. N Engl J Med. 2024; 390(15):1359-1371. doi:10.1056/NEJMoa231 2695.
45. Powles T, Valderrama BP, Gupta S, et al. Enfortumab Vedotin and Pembrolizumab in Untreated Advanced Urothelial Cancer. N Engl J Med. 2024;390(10):875-888. doi:10.10 56/NEJMoa2312117.