246
Views
0
CrossRef citations to date
0
Altmetric
Review

Immunotherapy for Non-Muscle-Invasive Bladder Cancer: from the Origins of BCG to Novel Therapies

ORCID Icon, ORCID Icon & ORCID Icon
Pages 105-115 | Received 24 Jun 2021, Accepted 30 Sep 2021, Published online: 12 Nov 2021

References

  • Antoni S , FerlayJ, SoerjomataramIet al. Bladder cancer incidence and mortality: a global overview and recent trends. Eur. Urol.71(1), 96–108 (2017).
  • Knowles MA , HurstCD. Molecular biology of bladder cancer: new insights into pathogenesis and clinical diversity. Nat. Rev. Cancer.15(1), 25–41 (2015).
  • Bryan RT , ZeegersMP, van RoekelEHet al. A comparison of patient and tumour characteristics in two UK bladder cancer cohorts separated by 20 years. BJU Int.112(2), 169–75 (2013).
  • van Rhijn BW , BurgerM, LotanYet al. Recurrence and progression of disease in non-muscle-invasive bladder cancer: from epidemiology to treatment strategy. Eur Urol.56(3), 430–42 (2009).
  • Riley GF , PotoskyAL, LubitzJD, KesslerLG. Medicare payments from diagnosis to death for elderly cancer patients by stage at diagnosis. Med. Care.33(8), 828–41 (1995).
  • Advanced Bladder Cancer (ABC) Meta-analysis Collaboration . Neoadjuvant chemotherapy in invasive bladder cancer: update of a systematic review and meta-analysis of individual patient data advanced bladder cancer (ABC) meta-analysis collaboration. Eur. Urol.48(2), 202–205 (2005).
  • Wallace DM , BryanRT, DunnJAet al. Delay and survival in bladder cancer. BJU Int.89(9), 868–78 (2002).
  • Babjuk M , BurgerM, ComperatEet al. EAU guidelines on non-muscle-invasive bladder cancer (TaT1 and CIS) (2020). https://uroweb.org/wp-content/uploads/EAU-Guidelines-on-Non-muscle-Invasive-Bladder-Cancer-2020.pdf
  • Cherry T . Cancer and acquired resistance to tuberculosis. Med. J. Australia1(23), 372–374 (1925).
  • Pearl R . Cancer and tuberculosis. Am. J. Epidemiol.9(1), 97–159 (1929).
  • Murray JF . A century of tuberculosis. Am. J. Resp. Crit. Care Med.169(11), 1181–1186 (2004).
  • Meyer J-P , PersadR, GillattDA. Use of bacille Calmette-Guérin in superficial bladder cancer. Postgrad. Med. J.78(922), 449–454 (2002).
  • Old LJ , ClarkeDA, BenacerrafB. Effect of Bacillus Calmette-Guérin infection on transplanted tumours in the mouse. Nature.184, 291–292 (1959).
  • Coe JE , FeldmanJD. Extracutaneous delayed hypersensitivity, particularly in the guinea-pig bladder. Immunology10(2), 127–36 (1966).
  • Zbar B , TanakaT. Immunotherapy of cancer: regression of tumours after intralesional injection of living Mycobacterium bovis. Am. Assoc. Adv. Sci.172, 271–273 (1971).
  • deKernion JB , GolubSH, GuptaRKet al. Successful transurethral intralesional BCG therapy of a bladder melanoma. Cancer36(5), 1662–1667 (1975).
  • Morales A , EidingerD, BruceAW. Intracavitary Bacillus Calmette-Guérin in the treatment of superficial bladder tumors. J. Urol.116(2), 180–3 (1976).
  • Herr HW , MoralesA. History of Bacillus Calmette-Guérin and bladder cancer: an immunotherapy success story. J. Urol.179(1), 53–56 (2008).
  • Sylvester RJ , VanDer Meijden AP, LammDL. Intravesical Bacillus Calmette-Guérin reduces the risk of progression in patients with superficial bladder cancer: a meta-analysis of the published results of randomized clinical trials. J. Urol.168(5), 1964–1970 (2002).
  • Hudson MA , RatliffTL, GillenDPet al. Single course versus maintenance Bacillus Calmette-Guérin therapy for superficial bladder tumors: a prospective, randomized trial. J. Urol.138(2), 295–298 (1987).
  • Badalament RA , HerrHW, WongGYet al. A prospective randomized trial of maintenance versus nonmaintenance intravesical Bacillus Calmette-Guérin therapy of superficial bladder cancer. J. Clin. Oncol.5(3), 441–449 (1987).
  • Lamm DL , BlumensteinBA, CrissmanJDet al. Maintenance Bacillus Calmette-Guérin immunotherapy for recurrent TA, T1 and carcinoma in situ transitional cell carcinoma of the bladder: a randomized Southwest Oncology Group Study. J. Urol.163(4), 1124–1129 (2000).
  • Böhle A , JochamD, BockPR. Intravesical Bacillus Calmette-Guérin versus mitomycin C for superficial bladder cancer: a formal meta-analysis of comparative studies on recurrence and toxicity. J. Urol.169(1), 90–95 (2003).
  • Babjuk M , BurgerM, ComperatE. EAU guidelines on non-muscle-invasive bladder cancer (TaT1 and CIS) (2018). https://uroweb.org/wp-content/uploads/EAU-Guidelines-Non-muscle-invasive-Bladder-Cancer-TaT1-CIS-2018.pdf
  • Boehm BE , CornellJE, WangHet al. Efficacy of Bacillus Calmette-Guérin strains for treatment of nonmuscle invasive bladder cancer: a systematic review and network meta-analysis. J. Urol.198(3), 503–510 (2017).
  • D’Andrea D , GonteroP, ShariatSFet al. Intravesical Bacillus Calmette-Guérin for bladder cancer: are all the strains equal? Transl. Androl. Urol. 8(1), 85–93 (2019).
  • Meeks JJ , LernerSP, SvatekRS. Bacillus Calmette-Guérin manufacturing and SWOG S1602 intergroup clinical trial. J. Urol.197(3), 538–540 (2017).
  • Rentsch CA , BirkhäuserFD, BiotCet al. Bacillus Calmette-Guérin strain differences have an impact on clinical outcome in bladder cancer immunotherapy. Eur. Urol.66(4), 677–688 (2014).
  • Inamoto T , UbaiT, NishidaTet al. Comparable effect with minimal morbidity of low-dose Tokyo 172 strain compared with regular dose Connaught strain as an intravesical Bacillus Calmette-Guérin prophylaxis in nonmuscle invasive bladder cancer: results of a randomized prospective comparison. Urol. Ann.5(1), 7–12 (2013).
  • Hofbauer SL , ShariatSF, ChaseDCet al. The moreau strain of Bacillus Calmette-Guérin (BCG) for high-risk non-muscle invasive bladder cancer: an alternative during Worldwide BCG shortage? Urol. Int. 96(1), 46–50 (2016).
  • D’Andrea D , SoriaF, AbufarajMet al. Comparative effectiveness of intravesical BCG-Tice and BCG-Moreau in patients with non-muscle-invasive bladder cancer. Clin. Genitourin. Cancer.18(1), 20–25 (2020).
  • Svatek RS , TangenC, DelacroixSet al. Background and update for S1602 “A Phase III Randomized Trial to Evaluate the Influence of BCG Strain Differences and T Cell Priming with Intradermal BCG Before Intravesical Therapy for BCG-naïve High-grade Non-muscle-invasive Bladder Cancer.” Eur. Urol. Focus. 4(4), 522–524 (2018).
  • Balar AV . Faced with BCG shortages, oncologists move to rationing of care (2019). www.targetedonc.com/view/faced-with-bcg-shortages-oncologists-move-to-rationing-of-care
  • Mostafid HA , RedortaJP, SylvesterR, WitjesJA. Therapeutic options in high-risk non–muscle-invasive bladder cancer during the current worldwide shortage of bacille Calmette-Guérin. Eur. Urol.67(3), 359–360 (2015).
  • Liu X , DowellAC, PatelPet al. Cytokines as effectors and predictors of responses in the treatment of bladder cancer by Bacillus Calmette-Guérin. Future Oncol.10(8), 1443–1456 (2014).
  • Yasuyo S , YoshihisaS, TakeshiI. Intravesical instillation therapy with Bacillus Calmette-Guérin for superficial bladder cancer: Study of the mechanism of Bacillus Calmette-Guérin immunotherapy. Int. J. Urol.14(2), 140–146 (2007).
  • Fankhauser CD , TeohJY, MostafidH. Treatment options and results of adjuvant treatment in nonmuscle-invasive bladder cancer (NMIBC) during the Bacillus Calmette-Guérin shortage. Curr. Opin. Urol.30(3), 365–369 (2020).
  • Tolley DA , HargreaveTB, SmithPHet al. Effect of intravesical mitomycin C on recurrence of newly diagnosed superficial bladder cancer: interim report from the Medical Research Council Subgroup on Superficial Bladder Cancer (Urological Cancer Working Party). Br. Med. J. (Clin. Res. Ed).296(6639), 1759–1761 (1988).
  • Verweij J , PinedoH. Mitomycin C: mechanism of action, usefulness and limitations. Anti-Cancer Drugs.1(1), 5–13 (1990).
  • Slater SE , PatelP, VineyRet al. The effects and effectiveness of electromotive drug administration and chemohyperthermia for treating non-muscle invasive bladder cancer. Ann. R. Coll. Surg. Engl.96(6), 415–419 (2014).
  • Clinicaltrial.gov . Electromotive mitomycin-C (EMDA-MMC) in preventing recurrences in high-risk non-muscle-invasive bladder cancer (FB10) (2018). https://clinicaltrials.gov/ct2/show/NCT03664869
  • Di Stasi SM , GiannantoniA, GiurioliAet al. Sequential BCG and electromotive mitomycin versus BCG alone for high-risk superficial bladder cancer: a randomised controlled trial. Lancet Oncol.7(1), 43–51 (2006).
  • Lamm DL . Efficacy and safety of bacille Calmette-Guérin immunotherapy in superficial bladder cancer. Clin. Infect. Dis.31(Suppl. 3), S86–90 (2000).
  • Oddens J , BrausiM, SylvesterRet al. Final results of an EORTC-GU cancers group randomized study of maintenance Bacillus Calmette-Guérin in intermediate- and high-risk Ta, T1 papillary carcinoma of the urinary bladder: one-third dose versus full dose and 1 year versus 3 years of maintenance. Eur Urol.63(3), 462–472 (2013).
  • Martinez-Pineiro L , PortilloJA, FernandoJMet al. Maintenance therapy with 3-monthly Bacillus Calmette-Guérin for 3 years is not superior to standard induction therapy in high-risk non-muscle-invasive urothelial bladder carcinoma: final results of randomised CUETO Study 98013. Eur Urol.68(2), 256–262 (2015).
  • Grimm MO , vander Heijden AG, ColombelMet al. Treatment of high-grade non-muscle-invasive bladder carcinoma by standard number and dose of BCG instillations versus reduced number and standard dose of bcg instillations: results of the European Association of Urology Research Foundation randomised phase iii clinical trial “NIMBUS”. Eur Urol.78(5), 690–698 (2020).
  • Ojea A , NogueiraJL, SolsonE. A multicentre, randomised prospective trial comparing three intravesical adjuvant therapies for intermediate-risk superficial bladder cancer: low-dose Bacillus Calmette-Guérin (27 mg) versus very low-dose Bacillus Calmette-Guérin (13.5 mg) versus mitomycin C. Eur Urol.52(5), 1398–1406 (2007).
  • US Food and Drug Administration . BCG-unresponsive nonmuscle invasive bladder cancer: developing drugs and biologics for treatment (2018). www.fda.gov/media/101468/download
  • Steinberg RL , ThomasLJ, O’DonnellMA, NeppleKG. Sequential intravesical gemcitabine and docetaxel for the salvage treatment of non-muscle invasive bladder cancer. Bladder Cancer1(1), 65–72 (2015).
  • Milbar N , KatesM, ChappidiMRet al. Oncological outcomes of sequential intravesical gemcitabine and docetaxel in patients with non-muscle invasive bladder cancer. Bladder Cancer3(4), 293–303 (2017).
  • Steinberg RL , ThomasLJ, BrooksNet al. Multi-institution evaluation of sequential gemcitabine and docetaxel as rescue therapy for nonmuscle invasive bladder cancer. J. Urol.203(5), 902–909 (2020).
  • Liu X , DowellAC, PatelPet al. Cytokines as effectors and predictors of responses in the treatment of bladder cancer by Bacillus Calmette–Guérin. Future Oncol.10(8), 1443–1456 (2014).
  • Balar AV , KamatAM, KulkarniGSet 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).
  • Clinicaltrials.gov . Assessment of efficacy and safety of durvalumab plus BCG compared to the standard therapy with bcg in non-muscle invasive bladder cancer (POTOMAC) (2020). www.clinicaltrials.gov/ct2/show/NCT03528694
  • LaRue H , AyariC, BergeronA, FradetY. Toll-like receptors in urothelial cells-targets for cancer immunotherapy. Nat. Rev. Urol.10(9), 537–545 (2013).
  • Smith M , García-MartínezE, PitterMRet al. Trial watch: toll-like receptor agonists in cancer immunotherapy. Oncoimmunology.7(12), e1526250 (2018).
  • Fuge O , VasdevN, AllchorneP, GreenJA. Immunotherapy for bladder cancer. Res. Rep. Urol.4(7), 65–79 (2015).
  • Falke J , LammersRJ, ArentsenHCet al. Results of a phase 1 dose escalation study of intravesical TMX-101 in patients with nonmuscle invasive bladder cancer. J. Urol.189(6), 2077–2082 (2013).
  • Morales A , PhadkeK, SteinhoffG. Intravesical mycobacterial cell wall-DNA complex in the treatment of carcinoma in situ of the bladder after standard intravesical therapy has failed. J. Urol.181(3), 1040–1045 (2009).
  • Benedict WF , TaoZ, KimCSet 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.10(3), 525–532 (2004).
  • Tao Z , ConnorRJ, AshooriFet al. Efficacy of a single intravesical treatment with Ad-IFN/Syn 3 is dependent on dose and urine IFN concentration obtained: implications for clinical investigation. Cancer Gene Ther.13(2), 125–130 (2006).
  • Shore ND , BoorjianSA, CanterDJet al. Intravesical rAd-IFNα/Syn3 for patients with high-grade, Bacillus Calmette-Guérin-refractory or relapsed non-muscle-invasive bladder cancer: a Phase ii randomized study. J Clin Oncol.35(30), 3410–3416 (2017).
  • Boorjian SA , AlemozaffarM, KonetyBRet 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.22(1), 107–117 (2021).
  • Dickstein R , WuN, CowanBet al. VISTA phase 3 trial of vicinium, an EPCAM-targeted pseudomonas exotoxin, in BCG-unresponsive non-muscle invasive bladder cancer (2018). https://abstracts.mirrorsmed.org/abstracts/vista-phase-3-trial-vicinium-epcam-targeted-pseudomonas-exotoxin-bcg-unresponsive-non
  • Derre L , CessonV, LuccaI. Intravesical Bacillus Calmette Guérin combined with a cancer vaccine increases local T-cell responses in non-muscle-invasive bladder cancer Patients. Clin. Cancer Res.23(3), 717–725 (2017).
  • Kadri H , TaherTE, XuQet al. Aryloxy diester phosphonamidate prodrugs of phosphoantigens (ProPAgens) as potent activators of Vγ9/Vδ2 T-cell immune responses. J. Med. Chem.63(19), 11258–11270 (2020).
  • Alhunaidi O , ZlottaAR. The use of intravesical BCG in urothelial carcinoma of the bladder. Ecancermedicalscience13, 905 (2019).
  • Lammers RJ , WitjesJA, InmanBAet al. The role of a combined regimen with intravesical chemotherapy and hyperthermia in the management of non-muscle-invasive bladder cancer: a systematic review. Eur. Urol.60(1), 81–93 (2011).
  • Kleinmann N , MatinSF, PierorazioPMet al. Primary chemoablation of low-grade upper tract urothelial carcinoma using UGN-101, a mitomycin-containing reverse thermal gel (OLYMPUS): an open-label, single-arm, phase 3 trial. Lancet Oncol.21(6), 7767–85 (2020).

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.