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REVIEW

Experimental and New Approaches for Bladder Preservation in Intermediate and High-Risk Non-Muscle-Invasive Bladder Cancer (NMIBC)

, & ORCID Icon
Pages 89-113 | Received 29 Nov 2023, Accepted 08 Feb 2024, Published online: 05 Apr 2024

References

  • IARC, Cancer Today. Estimated number of new cases in 2020, worldwide, both sexes, all ages; 2021. Available from: https://gco.iarc.fr/today/en. Accessed March, 2022.
  • Compérat E, Larré S, Roupret M, et al. Clinicopathological characteristics of urothelial bladder cancer in patients less than 40 years old. Virchows Arch. 2015;466:589–594. doi:10.1007/s00428-015-1739-2
  • Sylvester RJ, Rodríguez O, Hernández V, et al. European Association of Urology (EAU) Prognostic Factor Risk Groups for Non-muscle-invasive Bladder Cancer (NMIBC) incorporating the WHO 2004/2016 and WHO 1973 classification systems for grade: an update from the EAU NMIBC guidelines panel. Eur Urol. 2021;79:480–488. doi:10.1016/j.eururo.2020.12.033
  • Psutka SP, Barocas DA, Catto JWF, et al. Staging the host: personalizing risk assessment for radical cystectomy patients. Eur Urol Oncol. 2018;1:292–304. doi:10.1016/j.euo.2018.05.010
  • Tse J, Singla N, Ghandour R, Lotan Y, Margulis V. Current advances in BCG-unresponsive non-muscle invasive bladder cancer. Expert Opin Investig Drugs. 2019;28:757–770. doi:10.1080/13543784.2019.1655730
  • Meghani K, Cooley LF, Choy B, et al. First in-human intravesical delivery of pembrolizumab identifies immune activation in bladder cancer unresponsive to Bacillus Calmette-Guérin. Eur Urol. 2022;82:602–610. doi:10.1016/j.eururo.2022.08.004
  • Moe A, Liow E, Redfern A, et al. A phase I open label dose-escalation study to evaluate the tolerability, safety and immunological efficacy of sub-urothelial durvalumab injection in adults with muscle-invasive or high-risk non-muscle-invasive bladder cancer (SUBDUE-1, SUB-urothelial DUrvalumab injection-1 study): clinical trial protocol. BJU Int. 2021;128(Suppl 1):9–17. doi:10.1111/bju.15365
  • Balar AV, Kamat AM, Kulkarni GS, et al. Pembrolizumab monotherapy for the treatment of high-risk non-muscle-invasive bladder cancer unresponsive to BCG (KEYNOTE-057): an open-label, single-arm, multicentre, Phase 2 study. Lancet Oncol. 2021;22:919–930. doi:10.1016/S1470-2045(21)00147-9
  • Black PC, Tangen C, Singh P, et al. Phase II trial of atezolizumab in BCG-unresponsive non-muscle invasive bladder cancer: SWOG S1605 (NCT #02844816). J Clin Oncol. 2020;38(15 Suppl):5022. doi:10.1200/JCO.2020.38.15_suppl.5022
  • Vonderheide RH, Flaherty KT, Khalil M, et al. Clinical activity and immune modulation in cancer patients treated with CP-870,893, a novel CD40 agonist monoclonal antibody. J Clin Oncol. 2007;25:876–883. doi:10.1200/JCO.2006.08.3311
  • Mangsbo SM, Broos S, Fletcher E, et al. The human agonistic CD40 antibody ADC-1013 eradicates bladder tumors and generates T-cell–dependent tumor immunity. Clin Cancer Res. 2015;21:1115–1126. doi:10.1158/1078-0432.CCR-14-0913
  • Bennett SR, Carbone FR, Karamalis F, Flavell RA, Miller JF, Heath WR. Help for cytotoxic-T-cell responses is mediated by CD40 signalling. Nature. 1998;393:478–480. doi:10.1038/30996
  • Skinner EC, Goldman B, Sakr WA, et al. SWOG S0353: phase II trial of intravesical gemcitabine in patients with nonmuscle invasive bladder cancer and recurrence after 2 prior courses of intravesical Bacillus Calmette-Guérin. J Urol. 2013;190:1200–1204. doi:10.1016/j.juro.2013.04.031
  • Sternberg IA, Dalbagni G, Chen LY, Donat SM, Bochner BH, Herr HW. Intravesical gemcitabine for high risk, nonmuscle invasive bladder cancer after Bacillus Calmette-Guérin treatment failure. J Urol. 2013;190:1686–1691. doi:10.1016/j.juro.2013.04.120
  • Steinberg GD, Smith ND, Ryder K, Strangman NM, Slater SJ. Factors Affecting valrubicin response in patients with Bacillus Calmette-Guérin-refractory bladder carcinoma in situ. Postgrad Med. 2011;123:28–34. doi:10.3810/pgm.2011.05.2281
  • McKiernan JM, Barlow LJ, Laudano MA, Mann MJ, Petrylak DP, Benson MC. A phase I trial of intravesical nanoparticle albumin-bound paclitaxel in the treatment of Bacillus Calmette-Guérin refractory nonmuscle invasive bladder cancer. J Urol. 2011;186:448–451. doi:10.1016/j.juro.2011.03.129
  • Bassi PF, Volpe A, D’Agostino D, et al. Paclitaxel-hyaluronic acid for intravesical therapy of Bacillus Calmette-Guérin refractory carcinoma in situ of the bladder: results of a phase I study. J Urol. 2011;185:445–449. doi:10.1016/j.juro.2010.09.073
  • Di Lorenzo G, Perdonà S, Damiano R, et al. Gemcitabine versus bacille Calmette-Guérin after initial bacille Calmette-Guérin failure in non-muscle-invasive bladder cancer: a multicenter prospective randomized trial. Cancer. 2010;116:1893–1900. doi:10.1002/cncr.24914
  • Perdonà S, Di Lorenzo G, Cantiello F, et al. Is gemcitabine an option in BCG-refractory nonmuscle-invasive bladder cancer? A single-arm prospective trial. Anticancer Drugs. 2010;21:101–106. doi:10.1097/CAD.0b013e3283324d83
  • Laudano MA, Barlow LJ, Murphy AM, et al. Long-term clinical outcomes of a phase I trial of intravesical docetaxel in the management of non-muscle-invasive bladder cancer refractory to standard intravesical therapy. Urology. 2010;75:134–137. doi:10.1016/j.urology.2009.06.112
  • Addeo R, Caraglia M, Bellini S, et al. Randomized phase III trial on gemcitabine versus mytomicin in recurrent superficial bladder cancer: evaluation of efficacy and tolerance. J Clin Oncol. 2010;28:543–548. doi:10.1200/JCO.2008.20.8199
  • Ignatoff JM, Chen YH, Greenberg RE, Pow-Sang JM, Messing EM, Wilding G. Phase II study of intravesical therapy with AD32 in patients with papillary urothelial carcinoma or Carcinoma In Situ (CIS) refractory to prior therapy with Bacillus Calmette-Guerin (E3897): a trial of the Eastern Cooperative Oncology Group. Urol Oncol. 2009;27:496–501. doi:10.1016/j.urolonc.2008.05.004
  • Mohanty NK, Nayak RL, Vasudeva P, Arora RP. Intravesicle gemcitabine in management of BCG refractory superficial TCC of urinary bladder-our experience. Urol Oncol. 2008;26:616–619. doi:10.1016/j.urolonc.2007.10.016
  • Gunelli R, Bercovich E, Nanni O, et al. Activity of endovesical gemcitabine in BCG-refractory bladder cancer patients: a Translational Study. Br J Cancer. 2007;97:1499–1504. doi:10.1038/sj.bjc.6604074
  • Dalbagni G, Russo P, Bochner B, et al. Phase II trial of intravesical gemcitabine in bacille Calmette-Guérin-refractory transitional cell carcinoma of the bladder. J Clin Oncol. 2006;24:2729–2734. doi:10.1200/JCO.2005.05.2720
  • Bartoletti R, Cai T, Gacci M, et al. Intravesical gemcitabine therapy for superficial transitional cell carcinoma: results of a phase II Prospective Multicenter Study. Urology. 2005;66:726–731. doi:10.1016/j.urology.2005.04.062
  • Bassi P, De Marco V, Tavolini IM, et al. Pharmacokinetic study of intravesical gemcitabine in carcinoma in situ of the bladder refractory to Bacillus Calmette-Guérin therapy. Urol Int. 2005;75:309–313. doi:10.1159/000089164
  • Chevuru PT, McElree IM, Mott SL, Steinberg RL, O’Donnell MA, Packiam VT. Long-term follow-up of sequential intravesical gemcitabine and docetaxel salvage therapy for non-muscle invasive bladder cancer. Urol Oncol. 2023;41:148.e1–148.e7. doi:10.1016/j.urolonc.2022.10.030
  • Steinberg RL, Thomas LJ, Brooks N, et al. Multi-institution evaluation of sequential gemcitabine and docetaxel as rescue therapy for nonmuscle invasive bladder cancer. J Urol. 2020;203:902–908. doi:10.1097/JU.0000000000000688
  • DeCastro GJ, Sui W, Pak JS, et al. A Phase I trial of intravesical cabazitaxel, gemcitabine and cisplatin for the treatment of nonmuscle invasive Bacillus Calmette-Guérin unresponsive or recurrent/relapsing urothelial carcinoma of the bladder. J Urol. 2020;204:247–253. doi:10.1097/JU.0000000000000919
  • Dalbagni G, Benfante N, Sjoberg DD, et al. Single Arm Phase I/II Study of everolimus and intravesical gemcitabine in patients with primary or secondary carcinoma in situ of the bladder who failed Bacillus Calmette Guerin (NCT01259063). Bladder Cancer. 2017;3:113–119. doi:10.3233/BLC-170095
  • Cockerill PA, Knoedler JJ, Frank I, Tarrell R, Karnes RJ. Intravesical gemcitabine in combination with mitomycin C as salvage treatment in recurrent non-muscle-invasive bladder cancer. BJU Int. 2016;117:456–462. doi:10.1111/bju.13088
  • Lightfoot AJ, Breyer BN, Rosevear HM, Erickson BA, Konety BR, O’Donnell MA. Multi-institutional analysis of sequential intravesical gemcitabine and mitomycin C chemotherapy for non-muscle invasive bladder cancer. Urol Oncol. 2014;32:35.e15–35.e19. doi:10.1016/j.urolonc.2013.01.009
  • Hurle R, Casale P, Morenghi E, et al. Intravesical gemcitabine as bladder-preserving treatment for BCG unresponsive non-muscle-invasive bladder cancer. Results from a Single-Arm, Open-Label Study. BJUI Compass. 2020;1:126–132. doi:10.1002/bco2.28
  • Milbar N, Kates M, Chappidi MR, et al. Oncological outcomes of sequential intravesical gemcitabine and docetaxel in patients with non-muscle invasive bladder cancer. Bladder Cancer. 2017;3:293–303. doi:10.3233/BLC-170126
  • Robins DJ, Sui W, Matulay JT, et al. Long-term survival outcomes with intravesical nanoparticle albumin-bound paclitaxel for recurrent non-muscle-invasive bladder cancer after previous Bacillus Calmette-guérin therapy. Urology. 2017;103:149–153. doi:10.1016/j.urology.2017.01.018
  • Barlow LJ, McKiernan JM, Benson MC. Long-term survival outcomes with intravesical docetaxel for recurrent nonmuscle invasive bladder cancer after previous Bacillus Calmette-Guérin therapy. J Urol. 2013;189:834–839. doi:10.1016/j.juro.2012.10.068
  • Hendricksen K. Device-assisted intravesical therapy for non-muscle invasive bladder cancer. Transl Androl Urol. 2019;8:94–100. doi:10.21037/tau.2018.09.09
  • Van der Heijden AG, Verhaegh G, Jansen CF, et al. Effect of hyperthermia on the cytotoxicity of 4 chemotherapeutic agents currently used for the treatment of transitional cell carcinoma of the bladder: an in vitro study. J Urol. 2005;173:1375–1380. doi:10.1097/01.ju.0000146274.85012.e1
  • Paroni R, Salonia A, Lev A, et al. Effect of local hyperthermia of the bladder on mitomycin C pharmacokinetics during intravesical chemotherapy for the treatment of superficial transitional cell carcinoma. Br J Clin Pharmacol. 2001;52:273–278. doi:10.1046/j.0306-5251.2001.01449.x
  • Liem EIML, Crezee H, de la Rosette JJ, de Reijke TM. Chemohyperthermia in non-muscle-invasive bladder cancer: an overview of the literature and recommendations. Int J Hyperth. 2016;32:363–373. doi:10.3109/02656736.2016.1155760
  • Longo TA, Gopalakrishna A, Tsivian M, et al. A systematic review of regional hyperthermia therapy in bladder cancer. Int J Hyperthermia. 2016;32:381–389. doi:10.3109/02656736.2016.1157903
  • Colombo R, Da Pozzo LF, Salonia A, et al. Multicentric study comparing intravesical chemotherapy alone and with local microwave hyperthermia for prophylaxis of recurrence of superficial transitional cell carcinoma. J Clin Oncol. 2003;21(23):4270–4276. doi:10.1200/JCO.2003.01.089
  • Colombo R, Salonia A, Leib Z, et al. Long-term outcomes of a randomized controlled trial comparing thermochemotherapy with mitomycin-C alone as adjuvant treatment for non-muscle-invasive bladder cancer (NMIBC). BJU Int. 2011;107(6):912–918. doi:10.1111/j.1464-410X.2010.09654.x
  • Arends TJ, Nativ O, Maffezzini M, et al. Results of a Randomised controlled trial comparing intravesical chemohyperthermia with Mitomycin C versus Bacillus Calmette-Guerin for adjuvant treatment of patients with intermediate- and high-risk non-muscle-invasive bladder cancer. Eur Urol. 2016;69:1046–1052. doi:10.1016/j.eururo.2016.01.006
  • Nativ O, Witjes JA, Hendricksen K, et al. Combined thermo-chemotherapy for recurrent bladder cancer after Bacillus Calmette-Guerin. J Urol. 2009;182(4):1313–1317. doi:10.1016/j.juro.2009.06.017
  • Di Stasi SM, Giannantoni A, Stephen RL, et al. Intravesical electromotive mitomycin C versus passive transport mitomycin C for high-risk superficial bladder cancer: a prospective randomized study. J Urol. 2003;170(3):777–782. doi:10.1097/01.ju.0000080568.91703.18
  • Zahoor H, Mir MC, Barata PC, et al. Phase II trial of continuous treatment with sunitinib in patients with high-risk (BCG-refractory) non-muscle invasive bladder cancer. Investig New Drugs. 2019;37:1231–1238. doi:10.1007/s10637-018-00716-w
  • Hahn NM, Bivalacqua TJ, Ross AE, et al. A Phase II trial of dovitinib in BCG-unresponsive urothelial carcinoma with FGFR3 mutations or overexpression: Hoosier cancer research network trial HCRN 12-157. Clin Cancer Res. 2017;23:3003–3011. doi:10.1158/1078-0432.CCR-16-2267
  • Boorjian SA, Alemozaffar M, Konety BR, et al. Intravesical nadofaragene firadenovec gene therapy for BCG-unresponsive non-muscle-invasive bladder cancer: a single-arm, open-label, repeat-dose clinical trial. Lancet Oncol. 2021;22:107–117. doi:10.1016/S1470-2045(20)30540-4
  • Packiam VT, Lamm DL, Barocas DA, et al. An open label, single-arm, phase II Multicenter Study of the Safety and Efficacy of CG0070 oncolytic vector regimen in patients with BCG-unresponsive non-muscle-invasive bladder cancer: interim results. Urol Oncol. 2018;36:440–447. doi:10.1016/j.urolonc.2017.07.005
  • Shore ND, Boorjian SA, Canter DJ, et al. Intravesical RAd-IFNα/Syn3 for patients with high-grade, Bacillus Calmette-Guerin-refractory or relapsed non-muscle-invasive bladder cancer: a Phase II Randomized Study. J Clin Oncol. 2017;35:3410–3416. doi:10.1200/JCO.2017.72.3064
  • Navai N, Benedict WF, Zhang G, et al. Phase 1b trial to evaluate tissue response to a second dose of intravesical recombinant adenoviral interferon A2b formulated in Syn3 for failures of Bacillus Calmette-Guerin (BCG) therapy in nonmuscle invasive bladder cancer. Ann Surg Oncol. 2016;23:4110–4114. doi:10.1245/s10434-016-5300-6
  • Dinney CPN, Fisher MB, Navai N, et al. Phase I trial of intravesical recombinant adenovirus mediated interferon-A2b formulated in syn3 for Bacillus Calmette-Guérin failures in nonmuscle invasive bladder cancer. J Urol. 2013;190:850–856. doi:10.1016/j.juro.2013.03.030
  • Benedict WF, Tao Z, Kim CS, et al. Intravesical Ad-IFNalpha causes marked regression of human bladder cancer growing orthotopically in nude mice and overcomes resistance to IFN-alpha protein. Mol Ther. 2004;10:525–532. doi:10.1016/j.ymthe.2004.05.027
  • Connor RJ, Anderson JM, Machemer T, Maneval DC, Engler H. Sustained intravesical interferon protein exposure is achieved using an adenoviral-mediated gene delivery system: a study in rats evaluating dosing regimens. Urology. 2005;66:224–229. doi:10.1016/j.urology.2005.02.015
  • Yamashita M, Rosser CJ, Zhou JH, et al. Syn3 provides high levels of intravesical adenoviral-mediated gene transfer for gene therapy of genetically altered urothelium and superficial bladder cancer. Cancer Gene Ther. 2002;9:687–691. doi:10.1038/sj.cgt.7700488
  • Chu C, Pietzak E. Immune mechanisms and molecular therapeutic strategies to enhance immunotherapy in non-muscle invasive bladder cancer: invited review for special issue ”seminar: treatment advances and molecular biology insights in urothelial carcinoma”. Urol Oncol. 2023;41:398–409. doi:10.1016/j.urolonc.2022.05.013
  • Chang SS, Chamie K, Gonzalgo ML, et al. Positive efficacy and safety Phase 3 results in both CIS and papillary cohorts BCG-unresponsive nonmuscle invasive bladder cancer (NMIBC) after IL-15RFc superagonist N-803 (Anktiva) and BCG infusion. J clin oncol. 2022;40:431. doi:10.1200/JCO.2022.40.6_suppl.431
  • Morales A, Herr H, Steinberg G, et al. Efficacy and safety of MCNA in patients with nonmuscle invasive bladder cancer at high risk for recurrence and progression after failed treatment with Bacillus Calmette-Guérin. J Urol. 2015;193:1135–1143. doi:10.1016/j.juro.2014.09.109
  • Kowalski M, Guindon J, Brazas L, et al. A phase II study of oportuzumab monatox: an immunotoxin therapy for patients with noninvasive urothelial carcinoma in situ previously treated with Bacillus Calmette-Guérin. J Urol. 2012;188:1712–1718. doi:10.1016/j.juro.2012.07.020
  • Morales A, Phadke K, Steinhoff G. Intravesical mycobacterial cell wall-DNA complex in the treatment of carcinoma in situ of the bladder after standard intravesical therapy has failed. J Urol. 2009;181:1040–1045. doi:10.1016/j.juro.2008.11.019.
  • Joudi FN, Smith BJ, O’Donnell MA. Final results from a national multicenter Phase II trial of combination Bacillus Calmette-Guérin plus interferon alpha-2B for reducing recurrence of superficial bladder cancer. Urol Oncol. 2006;24:344–348. doi:10.1016/j.urolonc.2005.11.026
  • O’Donnell MA, Lilli K, Leopold C. Interim results from a national multicenter Phase II trial of combination Bacillus Calmette-Guerin plus interferon Alfa-2b for superficial bladder cancer. J Urol. 2004;172:888–893. doi:10.1097/01.ju.0000136446.37840.0a
  • Chu CE, Sjöström M, Egusa EA, et al. Heterogeneity in NECTIN4 expression across molecular subtypes of urothelial cancer mediates sensitivity to enfortumab vedotin. Clin Cancer Res. 2021;27:5123–5130. doi:10.1158/1078-0432.CCR-20-4175
  • Kamat AM, Steinberg GD, Inman BA, et al. Study EV-104: phase 1 study of intravesical enfortumab vedotin for treatment of patients with Non-Muscle Invasive Bladder Cancer (NMIBC)—trial in progress. J Clin Oncol. 2023;41:TPS582. doi:10.1200/JCO.2023.41.6_suppl.TPS582
  • Lee JY, Diaz RR, Cho KS, et al. Efficacy and safety of photodynamic therapy for recurrent, high grade nonmuscle invasive bladder cancer refractory or intolerant to bacille Calmette-Guerin immunotherapy. J Urol. 2013;190:1192–1199.
  • Waidelich R, Stepp H, Baumgartner R, et al. Clinical experience with 5-aminolevulinic acid and photodynamic therapy for refractory superficial bladder cancer. J Urol. 2001;165:1904–1907. doi:10.1016/S0022-5347(05)66239-8
  • Ritch CR, Velasquez MC, Kwon D, et al. Use and validation of the AUA/SUO risk grouping for nonmuscle invasive bladder cancer in a contemporary cohort. J Urol. 2020;203(3):505–511. doi:10.1097/JU.0000000000000593
  • Zuiverloon TCM, Zwarthoff EC. Predicting response to intravesical Bacillus Calmette-Güerin immunotherapy: are we moving forward? Eur Urol. 2016;69:201–202. doi:10.1016/j.eururo.2015.07.010
  • Kamat AM, Sylvester RJ, B€ohle A, et al. Definitions, end points, and clinical trial designs for non-muscle-invasive bladder cancer: recommendations from the International Bladder Cancer Group. J Clin Oncol. 2016;34:1935–1944. doi:10.1200/JCO.2015.64.4070
  • Lerner SP, Dinney C, Kamat A, et al. Clarification of bladder cancer disease states following treatment of patients with intravesical BCG. Bladder Cancer. 2015;1:29–30.
  • Cui J, Wang W, Chen S, et al. Combination of intravesical chemotherapy and Bacillus Calmette-Guerin versus Bacillus Calmette-Guerin monotherapy in intermediate- and high-risk nonmuscle invasive bladder cancer: a systematic review and meta-analysis. Medicine. 2016;95:e2572. doi:10.1097/MD.0000000000002572
  • Arends TJ, van der Heijden AG, Witjes JA. Combined chemohyperthermia: 10-year single center experience in 160 patients with nonmuscle invasive bladder cancer. J Urol. 2014;192:708–713. doi:10.1016/j.juro.2014.03.101