ESMO 2024: Invited Discussant: A Randomized Phase 3 Trial of Neoadjuvant Durvalumab plus Chemotherapy Followed by Radical Cystectomy and Adjuvant Durvalumab in Muscle-Invasive Bladder Cancer (NIAGARA)

(UroToday.com) The 2024 European Society of Medical Oncology (ESMO) Annual Congress held in Barcelona, Spain between September 13th and 17th was host to the session Presidential Symposium II: Practice-changing trials. Dr. Petros Grivas discussed the presentation by Dr. Thomas B. Powles who presented the results of the NIAGARA trial, a randomized phase 3 trial of neoadjuvant durvalumab plus chemotherapy followed by radical cystectomy and adjuvant durvalumab in muscle-invasive bladder cancer.


Dr. Grivas began by emphasizing that neoadjuvant cisplatin-based chemotherapy (NAC) is currently the standard of care for patients with muscle-invasive bladder cancer before radical cystectomy (RC). NAC significantly prolongs overall survival (OS) in phase 3 trials and is supported by Level I evidence.The goal of NAC is to eradicate micrometastases early and maximize its impact on oncological outcomes. Despite its benefits and broad availability in most cancer centers and that it does not require recovery time after RC, NAC has historically been underutilized.
Dr. Grivas also highlighted that the response to neoadjuvant therapy, based on pathological stage, has prognostic value. This response can provide insights into tumor biology and help with risk stratification, thereby enabling more informed decisions about adjuvant therapy.

Multiple clinical trials have explored combinations of immunotherapy (IO) and chemotherapy in the neoadjuvant setting for muscle-invasive bladder cancer (MIBC). Trials have investigated various combinations, including Gemcitabine + Cisplatin (GC) + Atezolizumab for 4 cycles, GC + Nivolumab for 4 cycles, GC + Durvalumab for 4 cycles, and GC (3-4 cycles) + Pembrolizumab. There is notable heterogeneity among the patient populations included in these trials. However, the rates of ypT0 or pathological complete response (pCR) are consistently reported, ranging from 33% to 45%, as illustrated in the figure below:

The SAKK06/17 was an investigator-initiated, open-label, single-arm phase II study that included cisplatin-eligible patients with stage cT2-T4a cN0-1. Patients received four cycles of neoadjuvant GC in combination with four cycles of durvalumab, followed by radical cystectomy (RC) and adjuvant durvalumab. The trial showed a ypT2N0 response in 60% of patients, a 24-month event-free survival rate of 76%, and 85% of participants were alive. The pathological complete response (pCR) rate was 33%.2
pT2N0 response in 60% of patients, a 24-month event-free survival rate of 76%, and 85% of participants were alive. The pathological complete response (pCR) rate was 33%
Dr. Grivas reviewed the NIAGARA study design and highlighted that the study included some patients with cN1 disease at baseline. The endpoint of event-free survival (EFS) was defined to include the date of expected surgery for patients who did not undergo radical cystectomy (RC). Additionally, the study's strength lies in its inclusion of patients with UC, as well as those with UC and divergent differentiation or histologic subtypes. The definition of cisplatin eligibility was adjusted to include patients with a CrCl of ≥40 mL/min. For patients with a CrCl ≥ 40 and <60 mL/min, a split-dose cisplatin regimen (35 mg/m² + gemcitabine 1000 mg/m² Days 1 and 8, Q3W for 4 cycles) was used instead of full-dose cisplatin.
NIAGARA study design
A critical appraisal of the statistical analysis plan was made by Dr Grivas, he mentioned that pCR is a reasonable primary endpoint in phase Il trials helping to decide if we should move on to phase III trials. However, pCR can be impacted by number and completeness or extent of prior TURBTs and whether pCR is a surrogate for EFS/OS is not yet proven for neoadjuvant-ICI therapy. Lastly, pCR would not be adequate or sufficient for regulatory guidance. The study design said the study would be considered positive if any of the primary dual endpoints is met (pCR/EFS).

Furthermore, while EFS is a very relevant endpoint, it can be influenced by patient preferences to avoid RC/PLND, which was observed in approximately 6% of the NIAGARA cohort. Additionally, in real-world practice, the percentage of patients who might receive adjuvant anti-PD1 therapy in the GC arm could also affect the trial results. The OS endpoint is crucial but can be impacted by the access to and effectiveness of salvage therapies in the recurrent/metastatic setting for both arms. Dr. Grivas noted that Dr. Powles and his team are diligently working to capture data on subsequent therapies administered across the trial.

A total of 19% of patients in each arm had a CrCl of ≥40 mL/min and received split-dose cisplatin-based chemotherapy. Additionally, 14% of patients in the durvalumab arm and 17% in the comparator arm had divergent histologies and approximately half had squamous features.
NIAGARA baseline characteristics
Toxicity was as expected, with no new safety signals, and the combination of GC + Durvalumab was feasible with no detrimental impact on RC/PLND. The percentage of patients who underwent RC was relatively similar between the arms. Dr. Grivas noted that it would be interesting to capture data on postoperative complications, readmission rates, and healthcare utilization. However, there were no concerning signals from the SAKK06/17 trial.

Dr. Grivas mentioned that he favors aMVAC (+ G-CSF) in the neoadjuvant setting but acknowledges that GC is a reasonable and commonly used control arm regimen. He noted that the performance of GC in this trial regarding OS seems comparable to historical controls such as the SWOG 8710 trial.1

The pCR rate in NIAGARA was similar to that in the phase II SAKK 06/17 trial (37.3% vs. 30%). Dr. Grivas questioned whether this ~10% difference in pCR rate alone could explain the significant differences in EFS and OS, considering data from the CheckMate 274 and AMBASSADOR trials.3,4 He was uncertain based on the NIAGARA trial design, which is the first study assessing perioperative therapy for MIBC.

Notably, the Kaplan-Meier curves in NIAGARA separate early and remain distinct, suggesting a possible tail in the curve. However, Dr. Grivas reiterated that results might have been different with adjuvant nivolumab and depending on rescue therapies in the metastatic/recurrent setting. He emphasized that while the NIAGARA trial is practice-changing due to its EFS/OS benefit and is the first to demonstrate an OS benefit in the perioperative setting for MIBC, the design cannot differentiate the impact of neoadjuvant versus adjuvant therapy. The key question remains whether either or both therapies are needed.
NIAGARA pathologic complete response
How does NIAGARA fit in the context of adjuvant trials? The CheckMate 274 trial assessed adjuvant Nivolumab (353 patients) versus placebo (356 patients) in high-risk muscle-invasive urothelial carcinoma (MIBC). Patients in this trial had either ypT2-ypT4a or ypN+ after neoadjuvant cisplatin chemotherapy, or pT3-pT4a or pN+ without prior neoadjuvant cisplatin chemotherapy. Although direct comparisons between trials should be avoided, in the NIAGARA trial, the median EFS was not reached in the Durvalumab arm, while it was 21 months in the adjuvant Nivolumab arm of CheckMate 274. For overall survival, the median OS was not reached in the NIAGARA trial, with 82.2% of patients alive at 24 months, compared to 76.1% alive at 24 months in CheckMate 274.How does NIAGARA fit in the context of adjuvant trials
Dr. Grivas emphasized that to build on the practice-changing findings of the NIAGARA trial, future trials should aim to dissect the contribution of each therapy phase (neoadjuvant vs. adjuvant). However, considerations such as operational, logistical, sample size, time, and budget constraints are crucial. Ideally, such a trial would involve a 3-4 arm design to comprehensively evaluate the impact of different treatment phases.

Dr. Grivas’s wish list for additional analyses in the NIAGARA trial includes several key areas for exploration. He suggested conducting ad-hoc exploratory analyses of EFS and OS for pCR, <ypT2N0, and ≥ ypT2N0 subgroups in each arm. This would help in understanding how these subgroups respond to treatment and provide more granular insights into the trial outcomes.

Additionally, he emphasized the importance of recording and reporting hospitalizations and systemic steroid use for managing adverse events. These factors can significantly impact patient experience and overall treatment burden. Assessing the quality of life and patient-reported outcomes using validated tools is also crucial for understanding the broader implications of the treatment.

Dr. Grivas also highlighted the need to evaluate the cost of the perioperative treatment strategy and assess financial toxicity. Understanding the economic impact of the treatment approach can guide future decisions and inform healthcare policies. 

In terms of biomarkers, he suggested investigating molecular markers such as ctDNA, DDR genes, RNA-based signatures, and spatial transcriptomics. Incorporating AI-based pathology and imaging biomarkers like MRI/VI-RADS could provide additional insights. Moreover, exploring the association between histology subtypes and outcomes could help tailor treatments more effectively.

Lastly, examining subsequent therapies in both the adjuvant (GC arm) and metastatic (both arms) settings would offer valuable information on the long-term management of patients following the initial treatment.

This trial leaves us with several important unanswered questions that impact clinical practice. First, the effect of prior immune checkpoint inhibitor (ICI) therapy given for non-muscle invasive bladder cancer (NMIBC) on neoadjuvant therapy selection remains uncertain, particularly regarding the use of Pembrolizumab for BCG-unresponsive disease. Additionally, there is uncertainty about whether adjuvant Durvalumab should be continued in patients with ypT0/N0, ypTa/Tis/T1N0, or ≥ ypT2N0, and whether ctDNA or other biomarkers could guide decisions on de-intensification of therapy. The applicability of these findings to upper tract urothelial carcinoma also needs further exploration. Another consideration is whether aMVAC with or without Durvalumab could be used for cisplatin-fit patients, or if Durvalumab plus Gemcitabine is suitable for cisplatin-unfit patients. Finally, there is the question of whether rechallenging with ICI is beneficial for patients who were treated with Durvalumab in the perioperative setting but subsequently experience disease progression in the metastatic setting.

Lastly, Dr. Grivas briefly highlighted several ongoing phase III trials in the perioperative and adjuvant settings for muscle-invasive bladder cancer (MIBC). These include:

  • Keynote-866: Evaluating the combination of Gemcitabine and Cisplatin (GC) with Pembrolizumab.
  • CheckMate 976: Investigating GC combined with Nivolumab or Nivolumab plus the IDO-1 inhibitor Linrodostat.
  • EV-304/KEYNOTE B15: Comparing Enfortumab Vedotin (EV) plus Pembrolizumab (EV+P) versus EV plus Durvalumab in cisplatin-eligible patients.
  • A032103 MODERN: Exploring ctDNA biomarker-based randomization to Nivolumab versus Nivolumab plus Relatimab, or Nivolumab versus surveillance.

A summary of the trial designs and schemas is illustrated in the graphic below.
summary of the trial designs and schemas 

Dr. Grivas concluded his presentation with the following key takeaways:

  • NIAGARA is considered practice-changing due to its demonstrated benefits EFS and OS, and it is currently awaiting regulatory review for approval in the perioperative setting of MIBC
  • The contribution of the neoadjuvant versus adjuvant phases remains unclear, and future trial designs may be able to address this unmet need, potentially through multi-arm studies that separate and evaluate these phases.
  • Ongoing and upcoming perioperative and adjuvant trials are critical to defining the optimal therapy for localized MIBC. Continued research will help refine treatment strategies and identify the best approaches for patient management.
  • Future directions may include more emphasis on bladder preservation, and exploring whether systemic therapy alone could be sufficient to achieve a cure in some patients, potentially reducing the need for radical cystectomy.
  • The question of what to do after progression remains relevant, particularly regarding the potential for IO rechallenge after progression in mUC. Further research is needed to determine the efficacy and safety of IO rechallenge strategies.

Presented by: Petros Grivas MD, PhD, Professor, Division of Hematology and Oncology, University of Washington, Seattle, USA.

Written by: Julian Chavarriaga, MD – Urologic Oncologist at Cancer Treatment and Research Center (CTIC) Luis Carlos Sarmiento Angulo Foundation via Society of Urologic Oncology (SUO) Fellow at The University of Toronto. @chavarriagaj on Twitter during the 2024 European Society of Medical Oncology (ESMO) Annual Congress held in Barcelona, Spain between September 13th and 17th

References:
  1. Grossman HB, Natale RB, Tangen CM, Speights VO, Vogelzang NJ, Trump DL, deVere White RW, Sarosdy MF, Wood DP Jr, Raghavan D, Crawford ED. Neoadjuvant chemotherapy plus cystectomy compared with cystectomy alone for locally advanced bladder cancer. N Engl J Med. 2003 Aug 28;349(9):859-66. doi: 10.1056/NEJMoa022148. Erratum in: N Engl J Med. 2003 Nov 6;349(19):1880. PMID: 12944571.
  2. Cathomas R, Rothschild SI, Hayoz S, Bubendorf L, Özdemir BC, Kiss B, Erdmann A, Aeppli S, Mach N, Strebel RT, Hadaschik B, Berthold D, John H, Zihler D, Schmid M, Alborelli I, Schneider M, Musilova J, Spahn M, Petrausch U. Perioperative Chemoimmunotherapy With Durvalumab for Muscle-Invasive Urothelial Carcinoma: Primary Analysis of the Single-Arm Phase II Trial SAKK 06/17. J Clin Oncol. 2023 Nov 20;41(33):5131-5139. doi: 10.1200/JCO.23.00363. Epub 2023 Aug 17. PMID: 37590894; PMCID: PMC10666980.
  3. Bajorin DF, Witjes JA, Gschwend JE, Schenker M, Valderrama BP, Tomita Y, Bamias A, Lebret T, Shariat SF, Park SH, Ye D, Agerbaek M, Enting D, McDermott R, Gajate P, Peer A, Milowsky MI, Nosov A, Neif Antonio J Jr, Tupikowski K, Toms L, Fischer BS, Qureshi A, Collette S, Unsal-Kacmaz K, Broughton E, Zardavas D, Koon HB, Galsky MD. Adjuvant Nivolumab versus Placebo in Muscle-Invasive Urothelial Carcinoma. N Engl J Med. 2021 Jun 3;384(22):2102-2114. doi: 10.1056/NEJMoa2034442. Erratum in: N Engl J Med. 2021 Aug 26;385(9):864. doi: 10.1056/NEJMx210012. PMID: 34077643; PMCID: PMC8215888.
  4. Andrea B. Apolo et al. AMBASSADOR Alliance A031501: Phase III randomized adjuvant study of pembrolizumab in muscle-invasive and locally advanced urothelial carcinoma (MIUC) vs observation. JCO 42, LBA531-LBA531(2024).
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