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Neoadjuvant Atezolizumab With Gemcitabine and Cisplatin in Patients With Muscle-Invasive Bladder Cancer: A Multicenter, Single-Arm, Phase II Trial

  • Samuel A. Funt,
  • Michael Lattanzi,
  • Karissa Whiting,
  • Hikmat Al-Ahmadie,
  • Colleen Quinlan,
  • Min Yuen Teo,
  • Chung-Han Lee,
  • David Aggen,
  • Danielle Zimmerman,
  • Deaglan McHugh,
  • Arlyn Apollo,
  • Trey D. Durdin,
  • Hong Truong,
  • Jeffrey Kamradt,
  • Maged Khalil,
  • Bradley Lash,
  • Irina Ostrovnaya,
  • Asia S. McCoy,
  • Grace Hettich,
  • Ashley Regazzi,
  • Marwah Jihad,
  • Neha Ratna,
  • Abigail Boswell,
  • Kaitlyn Francese,
  • Yuanquan Yang,
  • Edmund Folefac,
  • Harry W. Herr,
  • Machele Donat,
  • Eugene Pietzak,
  • Eugene K. Cha,
  • Timothy F. Donahue,
  • Alvin C. Goh,
  • William C. Huang,
  • Dean F. Bajorin,
  • Gopa Iyer,
  • Bernard H. Bochner,
  • Arjun V. Balar,
  • Amir Mortazavi,
  • Jonathan E. Rosenberg

Publication: Journal of Clinical Oncology, January 2022

Purpose

Neoadjuvant gemcitabine and cisplatin (GC) followed by radical cystectomy (RC) is standard for patients with muscle-invasive bladder cancer (MIBC). On the basis of the activity of atezolizumab (A) in metastatic BC, we tested neoadjuvant GC plus A for MIBC.

Methods

Eligible patients with MIBC (cT2-T4aN0M0) received a dose of A, followed 2 weeks later by GC plus A every 21 days for four cycles followed 3 weeks later by a dose of A before RC. The primary end point was non–muscle-invasive downstaging to < pT2N0.

Results

Of 44 enrolled patients, 39 were evaluable. The primary end point was met, with 27 of 39 patients (69%) < pT2N0, including 16 (41%) pT0N0. No patient with < pT2N0 relapsed and four (11%) with ≥ pT2N0 relapsed with a median follow-up of 16.5 months (range: 7.0-33.7 months). One patient refused RC and two developed metastatic disease before RC; all were considered nonresponders. The most common grade 3-4 adverse event (AE) was neutropenia (n = 16; 36%). Grade 3 immune-related AEs occurred in five (11%) patients with two (5%) requiring systemic steroids. The median time from last dose of chemotherapy to surgery was 7.8 weeks (range: 5.1-17 weeks), and no patient failed to undergo RC because of AEs. Four of 39 (10%) patients had programmed death-ligand 1 (PD-L1)–positive tumors and were all < pT2N0. Of the patients with PD-L1 low or negative tumors, 23 of 34 (68%) achieved < pT2N0 and 11 of 34 (32%) were ≥ pT2N0 (P = .3 for association between PD-L1 and < pT2N0).

Conclusion

Neoadjuvant GC plus A is a promising regimen for MIBC and warrants further study. Patients with < pT2N0 experienced improved relapse-free survival. The PD-L1 positivity rate was low compared with published data, which limits conclusions regarding PD-L1 as a predictive biomarker.

Dr. Benjamin Pradere

Neoadjuvant cisplatin-based chemotherapy prior to radical cystectomy (RC) and pelvic lymph node dissection (PLND) improves survival compared to RC-PLND alone for patients with muscle-invasive bladder cancer (MIBC).

Neoadjuvant gemcitabine-cisplatin is standard for patients with MIBC and can result in pathologic downstaging to NMIBC (< pT2N0) at RC, which correlates with improved survival. Based on the known activity of atezolizumab in metastatic bladder cancer (mBCa), it is reasonable to assess the efficacy of combination gemcitabine-cisplatin + atezolizumab as neoadjuvant therapy. 

This study is a U.S. multicenter trial that included 39 evaluable patients with MIBC (cT2–T4aN0M0) enrolled between 2018 and 2020. Patients received a lead-in dose of atezolizumab followed at two weeks by four cycles of gemcitabine/cisplatin plus atezolizumab every 21 days and another dose of atezolizumab three weeks later, prior to RC-PLND.

Atezolizumab was given at 1,200 mg, gemcitabine at 1,000 mg/m2 once on days 1 and 8, and cisplatin at either 70 mg/m2 once on day 1 or as a split dose at 35 mg/m2 once on days 1 and 8.

The primary endpoint was pathological downstaging to < pT2N0 (pDS) at time of RC; the combination of atezolizumab with GemCis was to be considered promising if a pDS occurred in 19 or more of the 39 evaluable patients.

At time of surgery, pDS was achieved in 27 (69%, 95% confidence interval [CI] = 55%–79%) of 39 patients, including pathologic complete response (pT0N0) (pCR) in 16 (41%). Among the remaining 12 patients: 2 (5%) had pT2N0 disease and 7 (18%) were non-responders with N+ disease; 2 patients (5%) developed metastatic disease prior to surgery and were considered non-responders.

Over a median follow-up of 16.5 months (range = 7.0–33.7 months), relapse was observed in none of the patients with pDS and in 4 (11%) with ≥ pT2N0.

PD-L1–positive status was defined as expression on ≥ 5% of tumour-infiltrating immune cells. Among four PD-L1–positive patients, all achieved pDS. Among 34 with PD-L1 expression of < 5%, 23 (68%) achieved pDS and 11 (32%) were ≥ pT2N0

At a median follow-up of 23.6 months, median RFS and median OS were not reached. Patients who achieved pDS had significantly better RFS vs those with ≥ pT2N0 (P < .001).

The most common treatment-related adverse events of any grade in 44 patients evaluated for safety were neutropenia (59%), fatigue (55%), anaemia (55%), and nausea (50%). Grade 3 or 4 AEs occurred in 59% of patients, most commonly neutropenia (36%, no febrile neutropenia) and lymphopenia (16%). Grade 3 immune-related adverse events occurred in five patients (11%), with two requiring systemic steroids. 

Overall, this study has shown that neoadjuvant gemcitabine/cisplatin plus atezolizumab seems to be promising for MIBC, achieving a downstaging to < pT2N0 in 69% of patients despite a low PDL1 positivity in the cohort. Moreover, it is interesting to see that patients who experienced pDS had no relapse during the median follow-up of 16.5 months. No patients failed to undergo timely radical cystectomy because of toxicity, and no unexpected safety signals were observed during treatment or postoperatively

Interestingly, the PD-L1 positivity rate was low compared with published data and was not correlated to pDS. These results limit again any conclusions regarding PD-L1 as a predictive biomarker in this setting. The genomic and host immune factors mediating response and resistance to GemCis + atezolizumab still remain unknown and need more investigations.