Durvalumab and tremelimumab with or without stereotactic body radiation therapy in relapsed small cell lung cancer: a randomized phase II study

Background Immune checkpoint blockade (ICB) targeting programmed cell death protein 1 and cytotoxic T lymphocyte-associated protein 4 has achieved modest clinical activity as salvage therapy in relapsed small cell lung cancer (SCLC). We conducted this signal-finding study to assess the efficacy of I...

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Main Authors: Chao Zhang, Shuhua Wang, Suresh Ramalingam, Sagar Lonial, Walter Curran, Edmund K Waller, Bassel Nazha, Taofeek K Owonikoko, Conor Steuer, Suchita Pakkala, Kristin Higgins, Zhengjia Chen, Gabriel Sica, Guojing Zhang, Mohammad S Hossain, Tyler Beardslee, Fadlo R Khuri
Format: Article
Language:English
Published: BMJ Publishing Group 2020-10-01
Series:Journal for ImmunoTherapy of Cancer
Online Access:https://jitc.bmj.com/content/8/2/e001302.full
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author Chao Zhang
Shuhua Wang
Suresh Ramalingam
Sagar Lonial
Walter Curran
Edmund K Waller
Bassel Nazha
Taofeek K Owonikoko
Conor Steuer
Suchita Pakkala
Kristin Higgins
Zhengjia Chen
Gabriel Sica
Guojing Zhang
Mohammad S Hossain
Tyler Beardslee
Fadlo R Khuri
author_facet Chao Zhang
Shuhua Wang
Suresh Ramalingam
Sagar Lonial
Walter Curran
Edmund K Waller
Bassel Nazha
Taofeek K Owonikoko
Conor Steuer
Suchita Pakkala
Kristin Higgins
Zhengjia Chen
Gabriel Sica
Guojing Zhang
Mohammad S Hossain
Tyler Beardslee
Fadlo R Khuri
author_sort Chao Zhang
collection DOAJ
description Background Immune checkpoint blockade (ICB) targeting programmed cell death protein 1 and cytotoxic T lymphocyte-associated protein 4 has achieved modest clinical activity as salvage therapy in relapsed small cell lung cancer (SCLC). We conducted this signal-finding study to assess the efficacy of ICB with or without radiation in relapsed SCLC.Methods Patients with relapsed SCLC and ≤2 previous lines of therapy were randomized to (1) arm A: durvalumab (D) 1500 mg/tremelimumab (T) 75 mg (intravenously every 4 weeks without stereotactic body radiation therapy (SBRT)) or (2) arm B: immune-sensitizing SBRT to one selected tumor site (9 Gy × 3 fractions) followed by D/T. Treatment continued until progression or a maximum of 12 months. The co-primary endpoints of the study were overall response rate (ORR) and progression-free survival (PFS). We evaluated circulating lymphocyte repertoire in serial peripheral blood samples and tumor infiltrating lymphocytes (TILs) from on-treatment biopsies as pharmacodynamic markers.Results Eighteen patients were randomized to arms A and B (n=9 each): median age 70 years; 41.2% women. The median PFS and ORR were 2.1 months and 0% in arm A and 3.3 months and 28.6% in arm B. The median overall survival (OS) was 2.8 months in arm A and 5.7 months in arm B (p=0.3772). Pooled efficacy of D/T±SBRT in 15 Response evaluation criteria in solid tumors (RECIST) evaluable patients across both arms showed the best ORR in terms of partial response in 13.3%, stable disease in 26.6% and progressive disease in 60.0%; the overall median PFS and OS were 2.76 and 3.9 months. The most common adverse events were grade 1 fatigue (66%) and grade 1 elevated amylase (56%) in arm A, and grade 1 fatigue (56%) and pain (44%) in arm B. There was a significant increase in activated CD8(+)ICOS+ T cells (p=0.048) and a reduction in naïve T cells (p=0.0454) in peripheral blood following treatment, along with a significant amount of activated CD8+ICOS+ T cells in TILs from responders.Conclusions The D/T combination with and without SBRT was safe but did not show sufficient efficacy signal in relapsed SCLC. Changes in peripheral blood lymphocyte and TILs were consistent with an immunologic response.Trial registration number NCT02701400.
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spelling doaj-art-1972602b33d841d1980a59a671248fb62024-11-10T15:00:07ZengBMJ Publishing GroupJournal for ImmunoTherapy of Cancer2051-14262020-10-018210.1136/jitc-2020-001302Durvalumab and tremelimumab with or without stereotactic body radiation therapy in relapsed small cell lung cancer: a randomized phase II studyChao Zhang0Shuhua Wang1Suresh Ramalingam2Sagar Lonial3Walter Curran4Edmund K Waller5Bassel Nazha6Taofeek K Owonikoko7Conor Steuer8Suchita Pakkala9Kristin Higgins10Zhengjia Chen11Gabriel Sica12Guojing Zhang13Mohammad S Hossain14Tyler Beardslee15Fadlo R Khuri16Department of Pharmacy, Beijing Tongren Hospital, Capital Medical University, Beijing, China1 Hematology and Medical Oncology, Emory University Winship Cancer Institute, Atlanta, Georgia, USAWinship Cancer Institute, Emory University, Atlanta, Georgia, USA1 Hematology and Medical Oncology, Emory University Winship Cancer Institute, Atlanta, Georgia, USADepartment of Radiation Oncology, Emory University, Atlanta, Georgia, USA1 Hematology and Medical Oncology, Emory University Winship Cancer Institute, Atlanta, Georgia, USAWinship Cancer Institute of Emory University, Atlanta, Georgia, USA4 Department of Hematology and Medical Oncology, Emory University Winship Cancer Institute, Atlanta, Georgia, USA8Winship Cancer Institute of Emory University, Atlanta, GA, USA1 Hematology and Medical Oncology, Emory University Winship Cancer Institute, Atlanta, Georgia, USA2 Department of Radiation Oncology, Emory University, Atlanta, Georgia, USADepartment of Epidemiology and Biostatics, University of Illinois Chicago, Chicago, Illinois, USA3 Pathology, Emory University Winship Cancer Institute, Atlanta, Georgia, USA1 Hematology and Medical Oncology, Emory University Winship Cancer Institute, Atlanta, Georgia, USA1 Hematology and Medical Oncology, Emory University Winship Cancer Institute, Atlanta, Georgia, USA1 Hematology and Medical Oncology, Emory University Winship Cancer Institute, Atlanta, Georgia, USA1 Hematology and Medical Oncology, Emory University Winship Cancer Institute, Atlanta, Georgia, USABackground Immune checkpoint blockade (ICB) targeting programmed cell death protein 1 and cytotoxic T lymphocyte-associated protein 4 has achieved modest clinical activity as salvage therapy in relapsed small cell lung cancer (SCLC). We conducted this signal-finding study to assess the efficacy of ICB with or without radiation in relapsed SCLC.Methods Patients with relapsed SCLC and ≤2 previous lines of therapy were randomized to (1) arm A: durvalumab (D) 1500 mg/tremelimumab (T) 75 mg (intravenously every 4 weeks without stereotactic body radiation therapy (SBRT)) or (2) arm B: immune-sensitizing SBRT to one selected tumor site (9 Gy × 3 fractions) followed by D/T. Treatment continued until progression or a maximum of 12 months. The co-primary endpoints of the study were overall response rate (ORR) and progression-free survival (PFS). We evaluated circulating lymphocyte repertoire in serial peripheral blood samples and tumor infiltrating lymphocytes (TILs) from on-treatment biopsies as pharmacodynamic markers.Results Eighteen patients were randomized to arms A and B (n=9 each): median age 70 years; 41.2% women. The median PFS and ORR were 2.1 months and 0% in arm A and 3.3 months and 28.6% in arm B. The median overall survival (OS) was 2.8 months in arm A and 5.7 months in arm B (p=0.3772). Pooled efficacy of D/T±SBRT in 15 Response evaluation criteria in solid tumors (RECIST) evaluable patients across both arms showed the best ORR in terms of partial response in 13.3%, stable disease in 26.6% and progressive disease in 60.0%; the overall median PFS and OS were 2.76 and 3.9 months. The most common adverse events were grade 1 fatigue (66%) and grade 1 elevated amylase (56%) in arm A, and grade 1 fatigue (56%) and pain (44%) in arm B. There was a significant increase in activated CD8(+)ICOS+ T cells (p=0.048) and a reduction in naïve T cells (p=0.0454) in peripheral blood following treatment, along with a significant amount of activated CD8+ICOS+ T cells in TILs from responders.Conclusions The D/T combination with and without SBRT was safe but did not show sufficient efficacy signal in relapsed SCLC. Changes in peripheral blood lymphocyte and TILs were consistent with an immunologic response.Trial registration number NCT02701400.https://jitc.bmj.com/content/8/2/e001302.full
spellingShingle Chao Zhang
Shuhua Wang
Suresh Ramalingam
Sagar Lonial
Walter Curran
Edmund K Waller
Bassel Nazha
Taofeek K Owonikoko
Conor Steuer
Suchita Pakkala
Kristin Higgins
Zhengjia Chen
Gabriel Sica
Guojing Zhang
Mohammad S Hossain
Tyler Beardslee
Fadlo R Khuri
Durvalumab and tremelimumab with or without stereotactic body radiation therapy in relapsed small cell lung cancer: a randomized phase II study
Journal for ImmunoTherapy of Cancer
title Durvalumab and tremelimumab with or without stereotactic body radiation therapy in relapsed small cell lung cancer: a randomized phase II study
title_full Durvalumab and tremelimumab with or without stereotactic body radiation therapy in relapsed small cell lung cancer: a randomized phase II study
title_fullStr Durvalumab and tremelimumab with or without stereotactic body radiation therapy in relapsed small cell lung cancer: a randomized phase II study
title_full_unstemmed Durvalumab and tremelimumab with or without stereotactic body radiation therapy in relapsed small cell lung cancer: a randomized phase II study
title_short Durvalumab and tremelimumab with or without stereotactic body radiation therapy in relapsed small cell lung cancer: a randomized phase II study
title_sort durvalumab and tremelimumab with or without stereotactic body radiation therapy in relapsed small cell lung cancer a randomized phase ii study
url https://jitc.bmj.com/content/8/2/e001302.full
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