First results on survival from a large Phase 3 clinical trial of an autologous dendritic cell vaccine in newly diagnosed glioblastoma

doi:10.1186/s12967-018-1507-6

Clinical Trial

. 2018 May 29;16(1):142.

doi: 10.1186/s12967-018-1507-6.

First results on survival from a large Phase 3 clinical trial of an autologous dendritic cell vaccine in newly diagnosed glioblastoma

Linda M Liau¹, Keyoumars Ashkan², David D Tran³, Jian L Campian⁴, John E Trusheim⁵, Charles S Cobbs⁶, Jason A Heth⁷, Michael Salacz⁸, Sarah Taylor⁸, Stacy D D'Andre⁹, Fabio M Iwamoto¹⁰, Edward J Dropcho¹¹, Yaron A Moshel¹², Kevin A Walter¹³, Clement P Pillainayagam¹⁴, Robert Aiken¹⁵, Rekha Chaudhary¹⁶, Samuel A Goldlust¹⁷, Daniela A Bota¹⁸, Paul Duic¹⁹, Jai Grewal²⁰, Heinrich Elinzano²¹, Steven A Toms²¹, Kevin O Lillehei²², Tom Mikkelsen²³, Tobias Walbert²³, Steven R Abram²⁴, Andrew J Brenner²⁵, Steven Brem²⁶, Matthew G Ewend²⁷, Simon Khagi²⁷, Jana Portnow²⁸, Lyndon J Kim²⁹, William G Loudon³⁰, Reid C Thompson³¹, David E Avigan³², Karen L Fink³³, Francois J Geoffroy³⁴, Scott Lindhorst³⁵, Jose Lutzky³⁶, Andrew E Sloan³⁷, Gabriele Schackert³⁸, Dietmar Krex³⁸, Hans-Jorg Meisel³⁹, Julian Wu⁴⁰, Raphael P Davis⁴¹, Christopher Duma⁴², Arnold B Etame⁴³, David Mathieu⁴⁴, Santosh Kesari⁴⁵, David Piccioni⁴⁵, Manfred Westphal⁴⁶, David S Baskin⁴⁷, Pamela Z New⁴⁷, Michel Lacroix⁴⁸, Sven-Axel May⁴⁹, Timothy J Pluard⁵⁰, Victor Tse⁵¹, Richard M Green⁵², John L Villano⁵³, Michael Pearlman⁵⁴, Kevin Petrecca⁵⁵, Michael Schulder⁵⁶, Lynne P Taylor⁵⁷, Anthony E Maida⁵⁸, Robert M Prins⁵⁹, Timothy F Cloughesy⁵⁹, Paul Mulholland⁶⁰, Marnix L Bosch⁶¹

Affiliations

¹ University of California Los Angeles (UCLA) David Geffen School of Medicine & Jonsson Comprehensive Cancer Center, Los Angeles, CA, USA. lliau@mednet.ucla.edu.
² King's College London School of Medical Education, London, UK.
³ University of Florida, Gainesville, FL, USA.
⁴ Washington University, St. Louis, MO, USA.
⁵ Abbott Northwestern Hospital, Minneapolis, MN, USA.
⁶ Swedish Medical Center, Swedish Neuroscience Institute, Seattle, WA, USA.
⁷ University of Michigan Medical School, Ann Arbor, MI, USA.
⁸ University of Kansas Cancer Center, Kansas City, KS, USA.
⁹ Sutter Institute for Medical Research, Sacramento, CA, USA.
¹⁰ Columbia University Medical Center, New York, NY, USA.
¹¹ Indiana University Simon Cancer Center, Indianapolis, IN, USA.
¹² Overlook Medical Center, Summit, NJ, USA.
¹³ University of Rochester Medical Center, Rochester, NY, USA.
¹⁴ Rush University Medical Center, Rochester, USA.
¹⁵ Rutgers Cancer Institute, New Brunswick, NJ, USA.
¹⁶ University of Cincinnati Medical Center, Cincinnati, OH, USA.
¹⁷ Hackensack University Medical Center, Hackensack, NJ, USA.
¹⁸ UC Irvine Medical Center, Irvine, CA, USA.
¹⁹ Winthrop-University Hospital, Mineola, NY, USA.
²⁰ NYU Winthrop Hospital, Mineola, NY, USA.
²¹ Rhode Island Hospital, Providence, RI, USA.
²² University of Colorado Hospital, Aurora, CO, USA.
²³ Henry Ford Health System, Detroit, MI, USA.
²⁴ St. Thomas Research Institute, Nashville, TN, USA.
²⁵ University of Texas Health Science Center, San Antonio, TX, USA.
²⁶ University of Pennsylvania Perelman School of Medicine, Philadelphia, PA, USA.
²⁷ University of North Carolina, Chapel Hill, NC, USA.
²⁸ City of Hope National Medical Center, Duarte, CA, USA.
²⁹ Thomas Jefferson University, Philadelphia, PA, USA.
³⁰ St. Joseph Hospital, Newport Beach, CA, USA.
³¹ Vanderbilt University, Nashville, TN, USA.
³² Beth Israel Deaconess Medical Center, Boston, MA, USA.
³³ Baylor University Medical Center, Dallas, TX, USA.
³⁴ Illinois CancerCare, Peoria, IL, USA.
³⁵ Medical University of South Carolina, Charleston, SC, USA.
³⁶ Mount Sinai Comprehensive Cancer Center, Miami, FL, USA.
³⁷ University Hospitals Case Medical Center, Cleveland, OH, USA.
³⁸ University Hospital Carl-Gustav-Carus of Technical University, Dresden, Germany.
³⁹ BG-Klinikum Bergmannstrost, Halle, Germany.
⁴⁰ Tufts University School of Medicine, Boston, MA, USA.
⁴¹ Stony Brook University, Stony Brook, NY, USA.
⁴² Hoag Cancer Center, Newport Beach, CA, USA.
⁴³ H. Lee Moffit Cancer Center and Research Institute, Tampa, FL, USA.
⁴⁴ CHUS-Hopital Fleurimont, Sherbrooke University, Sherbrooke, QC, Canada.
⁴⁵ UCSD Health System, UC San Diego, San Diego, CA, USA.
⁴⁶ Neurochirurgische Klinik University Clinic Hamburg-Eppendorf, Hamburg, Germany.
⁴⁷ Houston Methodist, Houston, TX, USA.
⁴⁸ Geisinger Health System, Danville, PA, USA.
⁴⁹ Klinikum Chemnitz GGMBH, Chemnitz, Germany.
⁵⁰ Saint Luke's Cancer Institute, Kansas City, MO, USA.
⁵¹ Kaiser Permanente Northern California, Redwood City, CA, USA.
⁵² Kaiser Permanente Southern California, Los Angeles, CA, USA.
⁵³ University of Kentucky College of Medicine, Lexington, KY, USA.
⁵⁴ Colorado Neurological Institute, Englewood, CO, USA.
⁵⁵ Montreal Neurological Institute and Hospital, McGill University, Montreal, Canada.
⁵⁶ Northwell Hofstra School of Medicine, Lake Success, NY, USA.
⁵⁷ Department of Neurology, Alvord Brain Tumor Center, University of Washington, Seattle, WA, USA.
⁵⁸ Northwest Biotherapeutics Inc., Bethesda, MD, USA.
⁵⁹ University of California Los Angeles (UCLA) David Geffen School of Medicine & Jonsson Comprehensive Cancer Center, Los Angeles, CA, USA.
⁶⁰ University College Hospitals, London, UK.
⁶¹ Northwest Biotherapeutics Inc., Bethesda, MD, USA. marnix@nwbio.com.

PMID: 29843811
PMCID: PMC5975654
DOI: 10.1186/s12967-018-1507-6

Clinical Trial

First results on survival from a large Phase 3 clinical trial of an autologous dendritic cell vaccine in newly diagnosed glioblastoma

Linda M Liau et al. J Transl Med. 2018.

. 2018 May 29;16(1):142.

doi: 10.1186/s12967-018-1507-6.

Authors

Affiliations

¹ University of California Los Angeles (UCLA) David Geffen School of Medicine & Jonsson Comprehensive Cancer Center, Los Angeles, CA, USA. lliau@mednet.ucla.edu.
² King's College London School of Medical Education, London, UK.
³ University of Florida, Gainesville, FL, USA.
⁴ Washington University, St. Louis, MO, USA.
⁵ Abbott Northwestern Hospital, Minneapolis, MN, USA.
⁶ Swedish Medical Center, Swedish Neuroscience Institute, Seattle, WA, USA.
⁷ University of Michigan Medical School, Ann Arbor, MI, USA.
⁸ University of Kansas Cancer Center, Kansas City, KS, USA.
⁹ Sutter Institute for Medical Research, Sacramento, CA, USA.
¹⁰ Columbia University Medical Center, New York, NY, USA.
¹¹ Indiana University Simon Cancer Center, Indianapolis, IN, USA.
¹² Overlook Medical Center, Summit, NJ, USA.
¹³ University of Rochester Medical Center, Rochester, NY, USA.
¹⁴ Rush University Medical Center, Rochester, USA.
¹⁵ Rutgers Cancer Institute, New Brunswick, NJ, USA.
¹⁶ University of Cincinnati Medical Center, Cincinnati, OH, USA.
¹⁷ Hackensack University Medical Center, Hackensack, NJ, USA.
¹⁸ UC Irvine Medical Center, Irvine, CA, USA.
¹⁹ Winthrop-University Hospital, Mineola, NY, USA.
²⁰ NYU Winthrop Hospital, Mineola, NY, USA.
²¹ Rhode Island Hospital, Providence, RI, USA.
²² University of Colorado Hospital, Aurora, CO, USA.
²³ Henry Ford Health System, Detroit, MI, USA.
²⁴ St. Thomas Research Institute, Nashville, TN, USA.
²⁵ University of Texas Health Science Center, San Antonio, TX, USA.
²⁶ University of Pennsylvania Perelman School of Medicine, Philadelphia, PA, USA.
²⁷ University of North Carolina, Chapel Hill, NC, USA.
²⁸ City of Hope National Medical Center, Duarte, CA, USA.
²⁹ Thomas Jefferson University, Philadelphia, PA, USA.
³⁰ St. Joseph Hospital, Newport Beach, CA, USA.
³¹ Vanderbilt University, Nashville, TN, USA.
³² Beth Israel Deaconess Medical Center, Boston, MA, USA.
³³ Baylor University Medical Center, Dallas, TX, USA.
³⁴ Illinois CancerCare, Peoria, IL, USA.
³⁵ Medical University of South Carolina, Charleston, SC, USA.
³⁶ Mount Sinai Comprehensive Cancer Center, Miami, FL, USA.
³⁷ University Hospitals Case Medical Center, Cleveland, OH, USA.
³⁸ University Hospital Carl-Gustav-Carus of Technical University, Dresden, Germany.
³⁹ BG-Klinikum Bergmannstrost, Halle, Germany.
⁴⁰ Tufts University School of Medicine, Boston, MA, USA.
⁴¹ Stony Brook University, Stony Brook, NY, USA.
⁴² Hoag Cancer Center, Newport Beach, CA, USA.
⁴³ H. Lee Moffit Cancer Center and Research Institute, Tampa, FL, USA.
⁴⁴ CHUS-Hopital Fleurimont, Sherbrooke University, Sherbrooke, QC, Canada.
⁴⁵ UCSD Health System, UC San Diego, San Diego, CA, USA.
⁴⁶ Neurochirurgische Klinik University Clinic Hamburg-Eppendorf, Hamburg, Germany.
⁴⁷ Houston Methodist, Houston, TX, USA.
⁴⁸ Geisinger Health System, Danville, PA, USA.
⁴⁹ Klinikum Chemnitz GGMBH, Chemnitz, Germany.
⁵⁰ Saint Luke's Cancer Institute, Kansas City, MO, USA.
⁵¹ Kaiser Permanente Northern California, Redwood City, CA, USA.
⁵² Kaiser Permanente Southern California, Los Angeles, CA, USA.
⁵³ University of Kentucky College of Medicine, Lexington, KY, USA.
⁵⁴ Colorado Neurological Institute, Englewood, CO, USA.
⁵⁵ Montreal Neurological Institute and Hospital, McGill University, Montreal, Canada.
⁵⁶ Northwell Hofstra School of Medicine, Lake Success, NY, USA.
⁵⁷ Department of Neurology, Alvord Brain Tumor Center, University of Washington, Seattle, WA, USA.
⁵⁸ Northwest Biotherapeutics Inc., Bethesda, MD, USA.
⁵⁹ University of California Los Angeles (UCLA) David Geffen School of Medicine & Jonsson Comprehensive Cancer Center, Los Angeles, CA, USA.
⁶⁰ University College Hospitals, London, UK.
⁶¹ Northwest Biotherapeutics Inc., Bethesda, MD, USA. marnix@nwbio.com.

PMID: 29843811
PMCID: PMC5975654
DOI: 10.1186/s12967-018-1507-6

Erratum in

Correction to: First results on survival from a large Phase 3 clinical trial of an autologous dendritic cell vaccine in newly diagnosed glioblastoma.
Liau LM, Ashkan K, Tran DD, Campian JL, Trusheim JE, Cobbs CS, Heth JA, Salacz M, Taylor S, D'Andre SD, Iwamoto FM, Dropcho EJ, Moshel YA, Walter KA, Pillainayagam CP, Aiken R, Chaudhary R, Goldlust SA, Bota DA, Duic P, Grewal J, Elinzano H, Toms SA, Lillehei KO, Mikkelsen T, Walbert T, Abram SR, Brenner AJ, Brem S, Ewend MG, Khagi S, Portnow J, Kim LJ, Loudon WG, Thompson RC, Avigan DE, Fink KL, Geoffroy FJ, Lindhorst S, Lutzky J, Sloan AE, Schackert G, Krex D, Meisel HJ, Wu J, Davis RP, Duma C, Etame AB, Mathieu D, Kesari S, Piccioni D, Westphal M, Baskin DS, New PZ, Lacroix M, May SA, Pluard TJ, Tse V, Green RM, Villano JL, Pearlman M, Petrecca K, Schulder M, Taylor LP, Maida AE, Prins RM, Cloughesy TF, Mulholland P, Bosch ML. Liau LM, et al. J Transl Med. 2018 Jun 29;16(1):179. doi: 10.1186/s12967-018-1552-1. J Transl Med. 2018. PMID: 29958537 Free PMC article.

Abstract

Background: Standard therapy for glioblastoma includes surgery, radiotherapy, and temozolomide. This Phase 3 trial evaluates the addition of an autologous tumor lysate-pulsed dendritic cell vaccine (DCVax^®-L) to standard therapy for newly diagnosed glioblastoma.

Methods: After surgery and chemoradiotherapy, patients were randomized (2:1) to receive temozolomide plus DCVax-L (n = 232) or temozolomide and placebo (n = 99). Following recurrence, all patients were allowed to receive DCVax-L, without unblinding. The primary endpoint was progression free survival (PFS); the secondary endpoint was overall survival (OS).

Results: For the intent-to-treat (ITT) population (n = 331), median OS (mOS) was 23.1 months from surgery. Because of the cross-over trial design, nearly 90% of the ITT population received DCVax-L. For patients with methylated MGMT (n = 131), mOS was 34.7 months from surgery, with a 3-year survival of 46.4%. As of this analysis, 223 patients are ≥ 30 months past their surgery date; 67 of these (30.0%) have lived ≥ 30 months and have a Kaplan-Meier (KM)-derived mOS of 46.5 months. 182 patients are ≥ 36 months past surgery; 44 of these (24.2%) have lived ≥ 36 months and have a KM-derived mOS of 88.2 months. A population of extended survivors (n = 100) with mOS of 40.5 months, not explained by known prognostic factors, will be analyzed further. Only 2.1% of ITT patients (n = 7) had a grade 3 or 4 adverse event that was deemed at least possibly related to the vaccine. Overall adverse events with DCVax were comparable to standard therapy alone.

Conclusions: Addition of DCVax-L to standard therapy is feasible and safe in glioblastoma patients, and may extend survival. Trial registration Funded by Northwest Biotherapeutics; Clinicaltrials.gov number: NCT00045968; https://clinicaltrials.gov/ct2/show/NCT00045968?term=NCT00045968&rank=1 ; initially registered 19 September 2002.

Keywords: Dendritic cell; Glioblastoma; Immunotherapy; Vaccine.

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Figures

**Fig. 1**
Recruitment, inclusion, and randomization of patients in the study. (1) Patients are screened prior to surgery, so glioblastoma (GBM) determination is made from pathological diagnosis after surgery. (2) Insufficient tumor lysate generated to meet threshold. (3) Progressive disease or pseudo-progression (which are indistinguishable at this point) based on central review of MRI imaging at baseline post-chemoradiation. (4) Patients who consented to tumor donation but then declined participation in trial prior to leukapheresis. (5) Includes deviations from standard chemoradiation protocol, history of prior malignancy, inadequate renal or bone marrow function, etc. (6) Includes drug product failure or insufficient drug or placebo manufactured to meet release criteria. (7) Includes clinical deterioration, declining Karnofsky performance status, or patient deaths. (8) Includes biopsy only, surgery canceled, or tumor tissue not processed after surgery

**Fig. 2**
Overall survival curves for patients in the intent-to-treat population. Overall survival analyses of time from date of surgery until death or last follow-up according to the Kaplan–Meier method for all patients in the intent-to-treat (ITT) population (a), and the ITT population stratified by MGMT gene promoter methylation status (b). Censored patients are annotated by a small vertical line

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References

1. Ostrom QT, Gittleman H, Xu J, Kromer C, Wolinsky Y, Kruchko C, Barnholtz-Sloan JS. CBTRUS statistical report: primary brain and other central nervous system tumors diagnosed in the United States in 2009–2013. Neuro-oncology. 2016;18(suppl_5):v1–v75. doi: 10.1093/neuonc/now207. - DOI - PMC - PubMed
1. Stupp R, Mason WP, van den Bent MJ, Weller M, Fisher B, Taphoorn MJ, Belanger K, Brandes AA, Marosi C, Bogdahn U, et al. Radiotherapy plus concomitant and adjuvant temozolomide for glioblastoma. N Engl J Med. 2005;352(10):987–996. doi: 10.1056/NEJMoa043330. - DOI - PubMed
1. Stupp R, Hegi ME, Mason WP, van den Bent MJ, Taphoorn MJ, Janzer RC, Ludwin SK, Allgeier A, Fisher B, Belanger K, et al. Effects of radiotherapy with concomitant and adjuvant temozolomide versus radiotherapy alone on survival in glioblastoma in a randomised phase III study: 5-year analysis of the EORTC-NCIC trial. Lancet Oncol. 2009;10(5):459–466. doi: 10.1016/S1470-2045(09)70025-7. - DOI - PubMed
1. Stupp R, Taillibert S, Kanner AA, Kesari S, Steinberg DM, Toms SA, Taylor LP, Lieberman F, Silvani A, Fink KL, et al. Maintenance therapy with tumor-treating fields plus temozolomide vs temozolomide alone for glioblastoma: a randomized clinical trial. JAMA. 2015;314(23):2535–2543. doi: 10.1001/jama.2015.16669. - DOI - PubMed
1. Wick W, Puduvalli VK, Chamberlain MC, van den Bent MJ, Carpentier AF, Cher LM, Mason W, Weller M, Hong S, Musib L, et al. Phase III study of enzastaurin compared with lomustine in the treatment of recurrent intracranial glioblastoma. J Clin Oncol. 2010;28(7):1168–1174. doi: 10.1200/JCO.2009.23.2595. - DOI - PMC - PubMed

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[1] Ostrom QT, Gittleman H, Xu J, Kromer C, Wolinsky Y, Kruchko C, Barnholtz-Sloan JS. CBTRUS statistical report: primary brain and other central nervous system tumors diagnosed in the United States in 2009–2013. Neuro-oncology. 2016;18(suppl_5):v1–v75. doi: 10.1093/neuonc/now207. - DOI - PMC - PubMed

[2] Ostrom QT, Gittleman H, Xu J, Kromer C, Wolinsky Y, Kruchko C, Barnholtz-Sloan JS. CBTRUS statistical report: primary brain and other central nervous system tumors diagnosed in the United States in 2009–2013. Neuro-oncology. 2016;18(suppl_5):v1–v75. doi: 10.1093/neuonc/now207. - DOI - PMC - PubMed

[3] Stupp R, Mason WP, van den Bent MJ, Weller M, Fisher B, Taphoorn MJ, Belanger K, Brandes AA, Marosi C, Bogdahn U, et al. Radiotherapy plus concomitant and adjuvant temozolomide for glioblastoma. N Engl J Med. 2005;352(10):987–996. doi: 10.1056/NEJMoa043330. - DOI - PubMed

[4] Stupp R, Mason WP, van den Bent MJ, Weller M, Fisher B, Taphoorn MJ, Belanger K, Brandes AA, Marosi C, Bogdahn U, et al. Radiotherapy plus concomitant and adjuvant temozolomide for glioblastoma. N Engl J Med. 2005;352(10):987–996. doi: 10.1056/NEJMoa043330. - DOI - PubMed

[5] Stupp R, Hegi ME, Mason WP, van den Bent MJ, Taphoorn MJ, Janzer RC, Ludwin SK, Allgeier A, Fisher B, Belanger K, et al. Effects of radiotherapy with concomitant and adjuvant temozolomide versus radiotherapy alone on survival in glioblastoma in a randomised phase III study: 5-year analysis of the EORTC-NCIC trial. Lancet Oncol. 2009;10(5):459–466. doi: 10.1016/S1470-2045(09)70025-7. - DOI - PubMed

[6] Stupp R, Hegi ME, Mason WP, van den Bent MJ, Taphoorn MJ, Janzer RC, Ludwin SK, Allgeier A, Fisher B, Belanger K, et al. Effects of radiotherapy with concomitant and adjuvant temozolomide versus radiotherapy alone on survival in glioblastoma in a randomised phase III study: 5-year analysis of the EORTC-NCIC trial. Lancet Oncol. 2009;10(5):459–466. doi: 10.1016/S1470-2045(09)70025-7. - DOI - PubMed

[7] Stupp R, Taillibert S, Kanner AA, Kesari S, Steinberg DM, Toms SA, Taylor LP, Lieberman F, Silvani A, Fink KL, et al. Maintenance therapy with tumor-treating fields plus temozolomide vs temozolomide alone for glioblastoma: a randomized clinical trial. JAMA. 2015;314(23):2535–2543. doi: 10.1001/jama.2015.16669. - DOI - PubMed

[8] Stupp R, Taillibert S, Kanner AA, Kesari S, Steinberg DM, Toms SA, Taylor LP, Lieberman F, Silvani A, Fink KL, et al. Maintenance therapy with tumor-treating fields plus temozolomide vs temozolomide alone for glioblastoma: a randomized clinical trial. JAMA. 2015;314(23):2535–2543. doi: 10.1001/jama.2015.16669. - DOI - PubMed

[9] Wick W, Puduvalli VK, Chamberlain MC, van den Bent MJ, Carpentier AF, Cher LM, Mason W, Weller M, Hong S, Musib L, et al. Phase III study of enzastaurin compared with lomustine in the treatment of recurrent intracranial glioblastoma. J Clin Oncol. 2010;28(7):1168–1174. doi: 10.1200/JCO.2009.23.2595. - DOI - PMC - PubMed

[10] Wick W, Puduvalli VK, Chamberlain MC, van den Bent MJ, Carpentier AF, Cher LM, Mason W, Weller M, Hong S, Musib L, et al. Phase III study of enzastaurin compared with lomustine in the treatment of recurrent intracranial glioblastoma. J Clin Oncol. 2010;28(7):1168–1174. doi: 10.1200/JCO.2009.23.2595. - DOI - PMC - PubMed

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First results on survival from a large Phase 3 clinical trial of an autologous dendritic cell vaccine in newly diagnosed glioblastoma

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First results on survival from a large Phase 3 clinical trial of an autologous dendritic cell vaccine in newly diagnosed glioblastoma

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