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Rindopepimut with Temozolomide for Patients with Newly Diagnosed, Egfrviii-Expressing Glioblastoma (ACT IV): a Randomised, Double-Blind, International Phase 3 Trial

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Rindopepimut with Temozolomide for Patients with Newly Diagnosed, Egfrviii-Expressing Glioblastoma (ACT IV): a Randomised, Double-Blind, International Phase 3 Trial Zurich Open Repository and Archive University of Zurich Main Library Strickhofstrasse 39 CH-8057 Zurich www.zora.uzh.ch Year: 2017 Rindopepimut with temozolomide for patients with newly diagnosed, EGFRvIII-expressing glioblastoma (ACT IV): a randomised, double-blind, international phase 3 trial Weller, Michael ; Butowski, Nicholas ; Tran, David D ; Recht, Lawrence D ; Lim, Michael ; Hirte, Hal ; Ashby, Lynn ; Mechtler, Laszlo ; Goldlust, Samuel A ; Iwamoto, Fabio ; Drappatz, Jan ; O’Rourke, Donald M ; Wong, Mark ; Hamilton, Mark G ; Finocchiaro, Gaetano ; Perry, James ; Wick, Wolfgang ; Green, Jennifer ; He, Yi ; Turner, Christopher D ; Yellin, Michael J ; Keler, Tibor ; Davis, Thomas A ; Stupp, Roger ; Sampson, John H ; ACT IV trial investigators DOI: https://doi.org/10.1016/S1470-2045(17)30517-X Posted at the Zurich Open Repository and Archive, University of Zurich ZORA URL: https://doi.org/10.5167/uzh-141081 Journal Article Accepted Version The following work is licensed under a Creative Commons: Attribution-NonCommercial-NoDerivatives 4.0 International (CC BY-NC-ND 4.0) License. Originally published at: Weller, Michael; Butowski, Nicholas; Tran, David D; Recht, Lawrence D; Lim, Michael; Hirte, Hal; Ashby, Lynn; Mechtler, Laszlo; Goldlust, Samuel A; Iwamoto, Fabio; Drappatz, Jan; O’Rourke, Donald M; Wong, Mark; Hamilton, Mark G; Finocchiaro, Gaetano; Perry, James; Wick, Wolfgang; Green, Jennifer; He, Yi; Turner, Christopher D; Yellin, Michael J; Keler, Tibor; Davis, Thomas A; Stupp, Roger; Sampson, John H; ACT IV trial investigators (2017). Rindopepimut with temozolomide for patients with newly diagnosed, EGFRvIII-expressing glioblastoma (ACT IV): a randomised, double-blind, international phase 3 trial. Lancet Oncology, 18(10):1373-1385. DOI: https://doi.org/10.1016/S1470-2045(17)30517-X TITLE PAGE Title: Rindopepimut with temozolomide for patients with newly diagnosed, EGFRvIII- expressing glioblastoma (ACT IV): results of a randomized, double-blind, international phase 3 trial Authors: Michael Weller, Nicholas Butowski, David D. Tran, Lawrence D. Recht, Michael Lim, Hal Hirte, Lynn Ashby, Lazlo Mechtler, Samuel A. Goldlust, Fabio Iwamoto, Jan Drappatz, Donald M. O'Rourke, Mark Wong, Mark G. Hamilton, Gaetano Finocchiaro, James Perry, Wolfgang Wick, Jennifer Green, Yi He, Christopher D. Turner, Michael J. Yellin, Tibor Keler, Thomas A. Davis, Roger Stupp, and John H. Sampson, for the ACT IV trial investigators* *Additional ACT IV trial investigators who participated in this trial are listed in the appendix. Affiliations: Departments of Neurology (Prof M. Weller, MD) and Oncology (Prof R. Stupp, MD), University Hospital and University of Zurich, Zurich, Switzerland; Department of Neurological Surgery, University of California, San Francisco, CA (N. Butowski, MD); Washington University, St. Louis, MO (D Tran, MD); Stanford University Medical Center, Palo Alto, CA (L.D. Recht, MD); The Johns Hopkins Hospital, Baltimore, MD (M. Lim, MD); Juravinski Cancer Centre, Hamilton, ON, Canada (H. Hirte, MD); Barrow Neurological Institute, Phoenix, AZ (L. Ashby, MD); Dent Neurologic Institute, Buffalo, NY (L. Mechtler, MD); John Theurer Cancer Center, Hackensack, NJ (S. Goldlust, MD); Columbia University Medical Center, New York, NY (F. Iwamoto, MD); University of Pittsburgh Medical Center, Pittsburgh, PA (Jan Drappatz); Department of Neurosurgery, Perelman School of Medicine, University of 1 Pennsylvania, Philadelphia, PA (D. O’Rourke, MD); Westmead Hospital, Westmead, Australia (M. Wong, MD); University of Calgary, Department of Clinical Neurosciences, Division of Neurosurgery, Foothills Hospital, Calgary, Alberta, Canada (Prof M. Hamilton, MD); Fondazione IRCCS Istituto Neurologico Carlo Besta, Milan, Italy (G. Finocchiaro, MD); Sunnybrook Health Sciences Centre, Toronto, ON, Canada (Prof J. Perry, MD); The University of Heidelberg and German Cancer Research Center, Heidelberg, Germany (Prof. W. Wick, MD); Celldex Therapeutics, Inc., Hampton, NJ (J. Green, Y. He, PhD, C. Turner, MD, M. Yellin, MD, T. Keler, PhD, T. Davis, MD); The Preston Robert Tisch Brain Tumor Center, Duke University Medical Center, Durham, NC (Prof J. H. Sampson, MD) Corresponding author: Michael Weller, MD Department of Neurology, University Hospital and University of Zurich Frauenklinikstrasse 26, 8091 Zurich, Switzerland, Tel. +41 44 255 55 00 [email protected] 2 SUMMARY Background Rindopepimut, a vaccine targeting the EGFR deletion mutation EGFRvIII, consists of a EGFRvIII-specific peptide conjugated to keyhole limpet hemocyanin (KLH). Single-arm studies of rindopepimut in patients with newly diagnosed, EGFRvIII+ glioblastoma and minimal residual disease (MRD) resulted in median survival of 20-22 months, compared to ~16 months for matched contemporary datasets. The ACT IV study was conducted to demonstrate prolongation of survival by rindopepimut when added to standard chemotherapy. Methods This pivotal, randomized, double-blind, phase 3 trial was conducted at 165 hospitals in 22 countries. Eligible patients had newly diagnosed glioblastoma confirmed to express EGFRvIII by central analysis, and had undergone maximal surgical resection and completion of standard chemoradiation without progression. Patients were stratified by RPA class, MGMT promoter methylation, and geographic region, and randomized (1:1) to receive rindopepimut (500 µg admixed with 150 µg GM CSF) or control (100 µg KLH) via monthly intradermal injection until progression or intolerance, concurrent with standard temozolomide (150-200 mg/m2 for 5/28 days) for 6-12 cycles or longer. Patients, investigators, and the trial sponsor were blinded to treatment allocation. Randomization and preparation of blinded treatment were managed via interactive response technology by designated pharmacists otherwise uninvolved in study conduct. Primary endpoint was intention-to-treat analysis of overall survival for MRD patients (enhancing tumor <2 cm2 post-chemoradiation by central review) aiming to detect a log-rank hazard ratio (HR) ≤0·71 with 80% power and alpha=0·05. The trial is registered with ClinicalTrials.gov (NCT01480479). 3 Findings Between April 12, 2012 and December 15, 2014, 745 patients were enrolled (405 MRD; 338 SRD; 2 unevaluable). The study was terminated for futility after a preplanned interim analysis. At final analysis, there was no significant difference in overall survival for the MRD (HR 1·01, 95% CI 0·79-1·30; p=0·93) population. Rindopepimut was well tolerated with robust anti- EGFRvIII immune response. Most common grade 3-4 adverse events for all 369 treated patients in the rindopepimut group vs 372 treated patients in the control group included: thrombocytopenia (33 [9%] vs 23 [6%]), fatigue (6 [2%] vs 19 [5%]), brain edema (8 [2%] vs 11 [3%]), seizure (9 [2%] vs 8 [2%]), and headache (6 [2%] vs 10 [3%]). Serious adverse events included seizure (18 [5%] vs 22 [6%]) and brain edema (7 [2%] vs 12 [3%]). Interpretation Despite consistent rindopepimut-induced humoral responses, rindopepimut did not prolong survival in patients with newly diagnostic glioblastoma. Combination approaches potentially including rindopepimut may be required to demonstrate efficacy of immunotherapy in glioblastoma. Funding Celldex Therapeutics, Inc. 4 RESEARCH IN CONTEXT Evidence before this study Using PubMed, we performed a systematic review of the scientific literature published prior to August 1, 2011 using the search terms “glioblastoma” and publication type "randomized controlled trial" or “clinical trial, phase III”. The standard of care for newly diagnosed glioblastoma established in 2005, maximum feasible surgical resection followed by radiotherapy and temozolomide chemotherapy, is associated with median overall survival of approximately 15 months. Despite the introduction of a number of investigational approaches in the subsequent years, no treatment had successfully demonstrated further improvement in survival. The addition of the search term “EGFRvIII” and expansion of our search to any clinical trial did not identify any other agents specifically targeting EGFRvIII. Finally, a search including “glioblastoma”, “EGFRvIII” and “survival” produced a few retrospective studies showing similar or worse median and long-term survival for patients whose tumor expressed EGFRvIII. Three prior studies of rindopepimut had been conducted in patients with newly diagnosed, EGFRvIII- expressing glioblastoma and minimal residual disease. In these studies, rindopepimut was associated with a strong anti-EGFRvIII humoral immune response, marked reduction in EGFRvIII expression in available recurrent tumor samples, and a median survival of 20-22 months, as compared to ~12 months for a small matched contemporary dataset and 15 months for the small subset of patients with newly diagnosed EGFRvIII-expressing glioblastoma randomized to receive standard of care therapy in the ACT III study. 5 Added value of this study To our knowledge, the ACT IV study is the first randomized trial evaluating the efficacy of an EGFRvIII-targeted therapy for newly diagnosed glioblastoma. Despite the strong anti-EGFRvIII immune response generated in patients, the primary study analysis did not demonstrate a survival benefit for patients with minimal residual disease who received rindopepimut with temozolomide. A potential long-term survival benefit was observed in exploratory analyses of a subset of patients with significant residual disease, which may challenge the view that minimal tumor burden is required for immunotherapy to
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