Advances in neoadjuvant immunotherapy for bladder cancer_West China Medical Journal

Authors：

WU Han ¹ , SHI Yanxiang ² ,  SHEN Yali ³

1. Department of oncology, the People’s Hospital of Shifang, Shifang, Sichuan 618400, P. R. China;
2. Department of Outpatient, West China Hospital, Sichuan University, Chengdu, Sichuan 610041, P. R. China;
3. Abdominal Oncology Ward, Division of Radiation Oncology, Cancer Center, State Key Laboratory of Biological Therapy, West China Hospital, Sichuan University, Chengdu, Sichuan 610041, P. R. China;

Corresponding author：

SHEN Yali, Email: sylprecious123@163.com

Keywords：

Muscular-invasive bladder cancer; neoadjuvant therapy; immunotherapy; biomarker

DOI：

10.7507/1002-0179.202304126

Video：

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Bladder cancer is one of the most common cancers of the urinary system. Baesd on the involvement of the blandder muscle or not, bladder cancer can be generally classified into muscule-invasive bladder cancer (MIBC) and non-MIBC. Cisplatin-based neoadjuvant chemotherapy followed by radical cystectomy is the standard treament recommended by current guidelines for MIBC. Based on the good efficacy of immunocheckpoint inhibitors in advanced bladder cancer. More and more studies have explored the safety and efficacy of immunotherapy in MIBC neoadjuvant therapy, and analyzed biomarkers to explore the benefit groups. This article reviews the latest progress of various neoadjuvant immunomonotherapy in MIBC, and prospect the future direction of development.

Citation： WU Han, SHI Yanxiang, SHEN Yali. Advances in neoadjuvant immunotherapy for bladder cancer. West China Medical Journal, 2023, 38(12): 1934-1939. doi: 10.7507/1002-0179.202304126 Copy

1.	Lenis AT, Lec PM, Chamie K. Bladder cancer: a review. JAMA, 2020, 324(19): 1980-1991.
2.	Funt SA, Rosenberg JE. Systemic, perioperative management of muscle-invasive bladder cancer and future horizons. Nat Rev Clin Oncol, 2017, 14(4): 221-234.
3.	Edge SB, Compton CC. The American joint committee on cancer: the 7th edition of the AJCC cancer staging manual and the future of TNM. Ann Surg Oncol, 2010, 17(6): 1471-1474.
4.	Alfred Witjes J, Lebret T, Compérat EM, et al. Updated 2016 EAU guidelines on muscle-invasive and metastatic bladder cancer. Eur Urol, 2017, 71(3): 462-475.
5.	Grossman HB, Natale RB, Tangen CM, et al. Neoadjuvant chemotherapy plus cystectomy compared with cystectomy alone for locally advanced bladder cancer. N Engl J Med, 2003, 349(9): 859-866.
6.	Hanna N, Trinh QD, Seisen T, et al. Effectiveness of neoadjuvant chemotherapy for muscle-invasive bladder cancer in the current real world setting in the USA. Eur Urol Oncol, 2018, 1(1): 83-90.
7.	Necchi A, Joseph RW, Loriot Y, et al. Atezolizumab in platinum-treated locally advanced or metastatic urothelial carcinoma: post-progression outcomes from the phase Ⅱ IMvigor210 study. Ann Oncol, 2017, 28(12): 3044-3050.
8.	Powles T, Durán I, van der Heijden MS, et al. Atezolizumab versus chemotherapy in patients with platinum-treated locally advanced or metastatic urothelial carcinoma (IMvigor211): a multicentre, open-label, phase 3 randomised controlled trial. Lancet, 2018, 391(10122): 748-757.
9.	Witjes JA, Bruins HM, Cathomas R, et al. European Association of Urology guidelines on muscle-invasive and meta-static bladder cancer: summary of the 2020 guidelines. Eur Urol, 2021, 79(1): 82-104.
10.	Flaig TW, Spiess PE, Agarwal N, et al. Bladder cancer, version 3. 2020, NCCN clinical practice guidelines in oncology. J Natl Compr Canc Netw, 2020, 18(3): 329-354.
11.	Basile G, Bandini M, Gibb EA, et al. Neoadjuvant pembrolizumab and radical cystectomy in patients with muscle-invasive urothelial bladder cancer: 3-year median follow-up update of PURE-01 Trial. Clin Cancer Res, 2022, 28(23): 5107-5114.
12.	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(11): 1706-1714.
13.	Szabados B, Kockx M, Assaf ZJ, et al. Final results of neoadjuvant atezolizumab in cisplatin-ineligible patients with muscle-invasive urothelial cancer of the bladder. Eur Urol, 2022, 82(2): 212-222.
14.	Gupta S, Gibb E, Sonpavde GP, et al. Biomarker analysis and updated clinical follow-up from BLASST-1 (Bladder cancer signal seeking trial) of nivolumab, gemcitabine, and cisplatin in patients with muscle-invasive bladder cancer (MIBC) undergoing cystectomy. J Clin Oncol, 2022, 40(Suppl 6): 528.
15.	Kim H, Jeong BC, Hong J, et al. Neoadjuvant nivolumab plus gemcitabine/cisplatin chemotherapy in muscle-invasive urothelial carcinoma of the bladder. Cancer Res Treat, 2022, 55(2): 636-642.
16.	Lin Tianxin, Li Kaiwen, Fan Jinhai, et al. Interim results from a multicenter clinical study of tislelizumab combined with gemcitabine and cisplatin as neoadjuvant therapy for patients with cT2-T4aN0M0 MIBC. J Clin Oncol, 2022, 40(Suppl 16): S4580.
17.	Goubet AG, Lordello L, Alves Costa Silva C, et al. Escherichia coli-specific CXCL13-producing TFH are associated with clinical efficacy of neoadjuvant PD-1 blockade against muscle-invasive bladder cancer. Cancer Discov, 2022, 12(10): 2280-2307.
18.	Wei XX, McGregor BA, Lee RJ, et al. Durvalumab as neoadjuvant therapy for muscle-invasive bladder cancer: preliminary results from the bladder cancer signal seeking trial (BLASST)-2. J Clin Oncol, 2020, 38(Suppl 6): 507.
19.	van Dijk N, Gil-Jimenez A, Silina K, et al. Preoperative ipilimumab plus nivolumab in locoregionally advanced urothelial cancer: the NABUCCO trial. Nat Med, 2020, 26(12): 1839-1844.
20.	Van Dorp J, Suelmann BBM, Mehra N, et al. LBA31 high- vs low-dose pre-operative ipilimumab andnivolumab in locoregionally advanced urothelial cancer (NABUCCO cohort 2). Ann Oncol, 2021, 32(Suppl 5): S1305-S1306.
21.	Gao J, Navai N, Alhalabi O, et al. Neoadjuvant PD-L1 plus CTLA-4 blockade in patients with cisplatin-ineligible operable high-risk urothelial carcinoma. Nat Med, 2020, 26(12): 1845-1851.
22.	Grande E, Guerrero F, Puente J, et al. DUTRENEO trial: a randomized phaseⅡtrial of Durvalumab and tremelimumab versus chemotherapy as a neoadjuvant approach to muscle-invasive urothelial bladder cancer (MIBC) patients (pts) prospectively selected by an interferon (INF)-gamma immune signature. J Clin Oncol, 2020, 38(Suppl 15): S5012.
23.	Gupta S, Sonpavde G, Weight CJ, et al. Results from BLASST-1 (Blandder Cancer Signal Seeking Trial) of nivolumab, gemcitabine, and cisplatin in muscle-invasive bladder cancer (MIBC) undergoing cystectomy. J Clin Oncol, 2020, 38(Suppl 6): S439.
24.	Martinez Chanza N, Carnot A, Barthelemy P, et al. 659MO Avelumab (A) as the basis of neoadjuvant chemotherapy (NAC) regimen in platinum eligible and ineligible patients (pts) with non-metastatic muscle invasive bladder cancer (NM-MIBC). Ann Oncol, 2021, 32(Suppl 5): S683.
25.	Funt SA, Lattanzi M, Whiting K, et al. Neoadjuvant atezolizumab with gemcitabine and cisplatin in patients with muscle-invasive bladder cancer: a multicenter, single-arm, phaseⅡtrial. J Clin Oncol, 2022, 40(12): 1312-1322.
26.	Cathomas R, Rothschild SI, Hayoz S, et al. Perioperative chemoimmunotherapy with durvalumab for muscle-invasive urothelial carcinoma: primary analysis of the single-arm phaseⅡtrial SAKK 06/17. J Clin Oncol, 2023, 41(33): 5131-5139.
27.	Shen Y, Wen F, Zhang P, et al. Real-world study of chemotherapy plus immunotherapy versus chemotherapy alone as neoadjuvant treatment guided bladder-sparing therapy for localized muscle-invasive bladder cancer. J Clin Oncol, 2022, 40(Suppl 6): S499.
28.	Shen Yali, Wen Feng, et al. HOPE-02: a phase 2, open-label study of neoadjuvant chemotherapy plus tislelizumab followed by radiotherapy based bladder-preserving treatment for high risk/locally advanced muscle invasive urothelial bladder cancer. ASCO-GU, 2023: abstract 516.
29.	Hu J, Chen J, Ou Z, et al. Neoadjuvant immunotherapy, chemotherapy, and combination therapy in muscle-invasive bladder cancer: a multi-center real-world retrospective study. Cell Rep Med, 2022, 3(11): 100785.
30.	Wen F, Lin T, Tan P, et al. 135O A multi-center phase Ⅰb/Ⅱ study of RC48-ADC combined with tislelizumab as neoadjuvant treatment in patients with HER2 positive locally advanced MIBC. Ann Oncol, 2022, 33(Suppl 9): S1485.
31.	Petrylak DP, Flaig TW, Mar N, et al. Study EV-103 cohort H: antitumor activity of neoadjuvant treatment with enfortumab vedotin monotherapy in patients (pts) with muscle invasive bladder cancer (MIBC) who are cisplatin-ineligible. J Clin Oncol, 2022, 40(Suppl 6): S435.

1. Lenis AT, Lec PM, Chamie K. Bladder cancer: a review. JAMA, 2020, 324(19): 1980-1991.
2. Funt SA, Rosenberg JE. Systemic, perioperative management of muscle-invasive bladder cancer and future horizons. Nat Rev Clin Oncol, 2017, 14(4): 221-234.
3. Edge SB, Compton CC. The American joint committee on cancer: the 7th edition of the AJCC cancer staging manual and the future of TNM. Ann Surg Oncol, 2010, 17(6): 1471-1474.
4. Alfred Witjes J, Lebret T, Compérat EM, et al. Updated 2016 EAU guidelines on muscle-invasive and metastatic bladder cancer. Eur Urol, 2017, 71(3): 462-475.
5. Grossman HB, Natale RB, Tangen CM, et al. Neoadjuvant chemotherapy plus cystectomy compared with cystectomy alone for locally advanced bladder cancer. N Engl J Med, 2003, 349(9): 859-866.
6. Hanna N, Trinh QD, Seisen T, et al. Effectiveness of neoadjuvant chemotherapy for muscle-invasive bladder cancer in the current real world setting in the USA. Eur Urol Oncol, 2018, 1(1): 83-90.
7. Necchi A, Joseph RW, Loriot Y, et al. Atezolizumab in platinum-treated locally advanced or metastatic urothelial carcinoma: post-progression outcomes from the phase Ⅱ IMvigor210 study. Ann Oncol, 2017, 28(12): 3044-3050.
8. Powles T, Durán I, van der Heijden MS, et al. Atezolizumab versus chemotherapy in patients with platinum-treated locally advanced or metastatic urothelial carcinoma (IMvigor211): a multicentre, open-label, phase 3 randomised controlled trial. Lancet, 2018, 391(10122): 748-757.
9. Witjes JA, Bruins HM, Cathomas R, et al. European Association of Urology guidelines on muscle-invasive and meta-static bladder cancer: summary of the 2020 guidelines. Eur Urol, 2021, 79(1): 82-104.
10. Flaig TW, Spiess PE, Agarwal N, et al. Bladder cancer, version 3. 2020, NCCN clinical practice guidelines in oncology. J Natl Compr Canc Netw, 2020, 18(3): 329-354.
11. Basile G, Bandini M, Gibb EA, et al. Neoadjuvant pembrolizumab and radical cystectomy in patients with muscle-invasive urothelial bladder cancer: 3-year median follow-up update of PURE-01 Trial. Clin Cancer Res, 2022, 28(23): 5107-5114.
12. 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(11): 1706-1714.
13. Szabados B, Kockx M, Assaf ZJ, et al. Final results of neoadjuvant atezolizumab in cisplatin-ineligible patients with muscle-invasive urothelial cancer of the bladder. Eur Urol, 2022, 82(2): 212-222.
14. Gupta S, Gibb E, Sonpavde GP, et al. Biomarker analysis and updated clinical follow-up from BLASST-1 (Bladder cancer signal seeking trial) of nivolumab, gemcitabine, and cisplatin in patients with muscle-invasive bladder cancer (MIBC) undergoing cystectomy. J Clin Oncol, 2022, 40(Suppl 6): 528.
15. Kim H, Jeong BC, Hong J, et al. Neoadjuvant nivolumab plus gemcitabine/cisplatin chemotherapy in muscle-invasive urothelial carcinoma of the bladder. Cancer Res Treat, 2022, 55(2): 636-642.
16. Lin Tianxin, Li Kaiwen, Fan Jinhai, et al. Interim results from a multicenter clinical study of tislelizumab combined with gemcitabine and cisplatin as neoadjuvant therapy for patients with cT2-T4aN0M0 MIBC. J Clin Oncol, 2022, 40(Suppl 16): S4580.
17. Goubet AG, Lordello L, Alves Costa Silva C, et al. Escherichia coli-specific CXCL13-producing TFH are associated with clinical efficacy of neoadjuvant PD-1 blockade against muscle-invasive bladder cancer. Cancer Discov, 2022, 12(10): 2280-2307.
18. Wei XX, McGregor BA, Lee RJ, et al. Durvalumab as neoadjuvant therapy for muscle-invasive bladder cancer: preliminary results from the bladder cancer signal seeking trial (BLASST)-2. J Clin Oncol, 2020, 38(Suppl 6): 507.
19. van Dijk N, Gil-Jimenez A, Silina K, et al. Preoperative ipilimumab plus nivolumab in locoregionally advanced urothelial cancer: the NABUCCO trial. Nat Med, 2020, 26(12): 1839-1844.
20. Van Dorp J, Suelmann BBM, Mehra N, et al. LBA31 high- vs low-dose pre-operative ipilimumab andnivolumab in locoregionally advanced urothelial cancer (NABUCCO cohort 2). Ann Oncol, 2021, 32(Suppl 5): S1305-S1306.
21. Gao J, Navai N, Alhalabi O, et al. Neoadjuvant PD-L1 plus CTLA-4 blockade in patients with cisplatin-ineligible operable high-risk urothelial carcinoma. Nat Med, 2020, 26(12): 1845-1851.
22. Grande E, Guerrero F, Puente J, et al. DUTRENEO trial: a randomized phaseⅡtrial of Durvalumab and tremelimumab versus chemotherapy as a neoadjuvant approach to muscle-invasive urothelial bladder cancer (MIBC) patients (pts) prospectively selected by an interferon (INF)-gamma immune signature. J Clin Oncol, 2020, 38(Suppl 15): S5012.
23. Gupta S, Sonpavde G, Weight CJ, et al. Results from BLASST-1 (Blandder Cancer Signal Seeking Trial) of nivolumab, gemcitabine, and cisplatin in muscle-invasive bladder cancer (MIBC) undergoing cystectomy. J Clin Oncol, 2020, 38(Suppl 6): S439.
24. Martinez Chanza N, Carnot A, Barthelemy P, et al. 659MO Avelumab (A) as the basis of neoadjuvant chemotherapy (NAC) regimen in platinum eligible and ineligible patients (pts) with non-metastatic muscle invasive bladder cancer (NM-MIBC). Ann Oncol, 2021, 32(Suppl 5): S683.
25. Funt SA, Lattanzi M, Whiting K, et al. Neoadjuvant atezolizumab with gemcitabine and cisplatin in patients with muscle-invasive bladder cancer: a multicenter, single-arm, phaseⅡtrial. J Clin Oncol, 2022, 40(12): 1312-1322.
26. Cathomas R, Rothschild SI, Hayoz S, et al. Perioperative chemoimmunotherapy with durvalumab for muscle-invasive urothelial carcinoma: primary analysis of the single-arm phaseⅡtrial SAKK 06/17. J Clin Oncol, 2023, 41(33): 5131-5139.
27. Shen Y, Wen F, Zhang P, et al. Real-world study of chemotherapy plus immunotherapy versus chemotherapy alone as neoadjuvant treatment guided bladder-sparing therapy for localized muscle-invasive bladder cancer. J Clin Oncol, 2022, 40(Suppl 6): S499.
28. Shen Yali, Wen Feng, et al. HOPE-02: a phase 2, open-label study of neoadjuvant chemotherapy plus tislelizumab followed by radiotherapy based bladder-preserving treatment for high risk/locally advanced muscle invasive urothelial bladder cancer. ASCO-GU, 2023: abstract 516.
29. Hu J, Chen J, Ou Z, et al. Neoadjuvant immunotherapy, chemotherapy, and combination therapy in muscle-invasive bladder cancer: a multi-center real-world retrospective study. Cell Rep Med, 2022, 3(11): 100785.
30. Wen F, Lin T, Tan P, et al. 135O A multi-center phase Ⅰb/Ⅱ study of RC48-ADC combined with tislelizumab as neoadjuvant treatment in patients with HER2 positive locally advanced MIBC. Ann Oncol, 2022, 33(Suppl 9): S1485.
31. Petrylak DP, Flaig TW, Mar N, et al. Study EV-103 cohort H: antitumor activity of neoadjuvant treatment with enfortumab vedotin monotherapy in patients (pts) with muscle invasive bladder cancer (MIBC) who are cisplatin-ineligible. J Clin Oncol, 2022, 40(Suppl 6): S435.

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