Plasma biomarkers for afatinib monotherapy in EGFR-mutated non-small cell lung cancer: Novel insights from companion genomics analysis of the EXTRA study

Objectives: Plasma-based testing with circulating cell-free DNA (cfDNA) is an active area of biomarker exploratory studies in patients with non-small cell lung cancer (NSCLC) harboring EGFR mutations. The Exosome-focused Translational Research for Afatinib study prospectively explored novel plasma b...

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Main Authors: Tomonori Makiguchi, Hisashi Tanaka, Kei Morikawa, Aya Hirata, Hidetoshi Itani, Shigeru Tanzawa, Kageaki Watanabe, Hiroyuki Yasuda, Kazuya Horiuchi, Hideyuki Nakagawa, Yoshitaka Seki, Yoshiro Nakahara, Kentaro Hayashi, Nobumasa Takahashi, Takeo Endo, Akihiro Bessho, Tetsuya Okano, Kiyoshi Takeyama, Akikazu Kawase, Makoto Endo, Toshiya Maekura, Kenji Nemoto, Nagio Takigawa, Kazuma Kishi, Kenzo Soejima, Yusuke Okuma, Akira Togashi, Noriyuki Matsutani, Hiroki Shinchi, Koji Ueda, Nobuhiko Seki
Format: Article
Language:English
Published: Elsevier 2025-01-01
Series:Cancer Treatment and Research Communications
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Online Access:http://www.sciencedirect.com/science/article/pii/S2468294225000887
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author Tomonori Makiguchi
Hisashi Tanaka
Kei Morikawa
Aya Hirata
Hidetoshi Itani
Shigeru Tanzawa
Kageaki Watanabe
Hiroyuki Yasuda
Kazuya Horiuchi
Hideyuki Nakagawa
Yoshitaka Seki
Yoshiro Nakahara
Kentaro Hayashi
Nobumasa Takahashi
Takeo Endo
Akihiro Bessho
Tetsuya Okano
Kiyoshi Takeyama
Akikazu Kawase
Makoto Endo
Toshiya Maekura
Kenji Nemoto
Nagio Takigawa
Kazuma Kishi
Kenzo Soejima
Yusuke Okuma
Akira Togashi
Noriyuki Matsutani
Hiroki Shinchi
Koji Ueda
Nobuhiko Seki
author_facet Tomonori Makiguchi
Hisashi Tanaka
Kei Morikawa
Aya Hirata
Hidetoshi Itani
Shigeru Tanzawa
Kageaki Watanabe
Hiroyuki Yasuda
Kazuya Horiuchi
Hideyuki Nakagawa
Yoshitaka Seki
Yoshiro Nakahara
Kentaro Hayashi
Nobumasa Takahashi
Takeo Endo
Akihiro Bessho
Tetsuya Okano
Kiyoshi Takeyama
Akikazu Kawase
Makoto Endo
Toshiya Maekura
Kenji Nemoto
Nagio Takigawa
Kazuma Kishi
Kenzo Soejima
Yusuke Okuma
Akira Togashi
Noriyuki Matsutani
Hiroki Shinchi
Koji Ueda
Nobuhiko Seki
author_sort Tomonori Makiguchi
collection DOAJ
description Objectives: Plasma-based testing with circulating cell-free DNA (cfDNA) is an active area of biomarker exploratory studies in patients with non-small cell lung cancer (NSCLC) harboring EGFR mutations. The Exosome-focused Translational Research for Afatinib study prospectively explored novel plasma biomarkers for afatinib monotherapy in patients with NSCLC harboring EGFR mutations using genomics, proteomics, epigenomics, and metabolomics. Herein, we present the results of the genomics part. Materials and Methods: Clinical data of afatinib were matched with next generation sequencing (NGS)-based genomics data of cfDNA (n = 101) and extracellular vesicle DNA (evDNA) (n = 99) from pretreatment plasma samples. Results: The detection sensitivity of cfDNA and evDNA mutations was 86 % (87/101) and 37 % (37/99), respectively. When cfDNA mutations were classified into tissue-matched (any EGFR mutations consistent with those identified in tissue) (n = 28), tissue-unmatched (n = 59), and mutation-undetected (n = 14) groups, cfDNA mutation status was a predictor of progression-free survival (PFS) (p < 0.01) and overall survival (OS) (p < 0.01). EvDNA mutation status was a predictor of OS (p < 0.01) rather than PFS (p = 0.48). When the tissue-unmatched cfDNA group was subclassified into EGFR-related (n = 49) and EGFR-unrelated (n = 10) groups, the EGFR-unrelated group had a median PFS and 3-year OS rate of 31.2 months and 80.0 %, respectively. EGFR-unrelated and mutation-undetected cfDNA groups (n = 24) exhibited a median PFS and 3-year OS rate of >30 months and >80 %, respectively, with afatinib monotherapy. Conclusion: This is the first large-scale prospective study of NGS-based concurrent testing for plasma cfDNA and evDNA mutations. The findings suggest that cfDNA mutation status is a promising plasma biomarker for afatinib monotherapy.
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spelling doaj-art-37cf6f9bd73e4c85a420e1686511e0ce2025-08-20T03:24:52ZengElsevierCancer Treatment and Research Communications2468-29422025-01-014410095210.1016/j.ctarc.2025.100952Plasma biomarkers for afatinib monotherapy in EGFR-mutated non-small cell lung cancer: Novel insights from companion genomics analysis of the EXTRA studyTomonori Makiguchi0Hisashi Tanaka1Kei Morikawa2Aya Hirata3Hidetoshi Itani4Shigeru Tanzawa5Kageaki Watanabe6Hiroyuki Yasuda7Kazuya Horiuchi8Hideyuki Nakagawa9Yoshitaka Seki10Yoshiro Nakahara11Kentaro Hayashi12Nobumasa Takahashi13Takeo Endo14Akihiro Bessho15Tetsuya Okano16Kiyoshi Takeyama17Akikazu Kawase18Makoto Endo19Toshiya Maekura20Kenji Nemoto21Nagio Takigawa22Kazuma Kishi23Kenzo Soejima24Yusuke Okuma25Akira Togashi26Noriyuki Matsutani27Hiroki Shinchi28Koji Ueda29Nobuhiko Seki30Department of Respiratory Medicine, Hirosaki University Graduate School of Medicine, Aomori, JapanDepartment of Respiratory Medicine, Hirosaki University Graduate School of Medicine, Aomori, JapanDivision of Respiratory Medicine, Department of Internal Medicine, St. Marianna University School of Medicine, Kanagawa, JapanDepartment of Respiratory Medicine, Kyorin University School of Medicine, Tokyo, JapanDepartment of Respiratory Medicine, Japanese Red Cross Ise Hospital, Mie, JapanDivision of Medical Oncology, Department of Internal Medicine, Teikyo University School of Medicine, Tokyo, JapanDepartment of Respiratory Medicine, Tokyo Metropolitan Cancer and Infectious Diseases Center Komagome Hospital, Tokyo, JapanDivision of Pulmonary Medicine, Department of Medicine, Keio University School of Medicine, Tokyo, JapanRespiratory Disease Center, Showa University Northern Yokohama Hospital, Kanagawa, JapanDepartment of Respiratory Medicine, National Hospital, Organization Hirosaki, Hospital, Aomori, JapanDivision of Respirology, Department of Internal Medicine, The Jikei Daisan Hospital, Tokyo, JapanDepartment of Respiratory Medicine, Kitasato University School of Medicine, Kanagawa, JapanDivision of Respiratory Medicine, Department of Internal Medicine, Nihon University School of Medicine, Tokyo, JapanDepartment of Thoracic Surgery, Saitama Cardiovascular, and Respiratory Center, Saitama, JapanDepartment of Respiratory Medicine, NHO Mito Medical Center, Ibaraki, JapanDepartment of Respiratory Medicine, Japanese Red Cross Okayama Hospital, Okayama, JapanDepartment of Surgery, Tokyo Medical University, Tokyo, JapanDepartment of Respiratory Medicine, Tokyo Women’s Medical University, Tokyo, JapanFirst Department of Surgery, Hamamatsu University School of Medicine, Shizuoka, JapanDepartment of Thoracic Surgery, Yamagata Prefectural Central Hospital, Yamagata, JapanDepartment of Respiratory Medicine, Japan Community Health care Organization, Hoshigaoka Medical Center, Osaka, JapanDepartment of Respiratory Medicine, National Hospital Organization, Ibarakihigashi National Hospital, Ibaraki, JapanDepartment of General Internal Medicine 4, Kawasaki Medical School, Okayama, JapanDepartment of Respiratory Medicine, Respiratory Center, Toranomon Hospital, Tokyo, JapanClinical and Translational Research Center, Keio University Hospital, Tokyo, JapanDepartment of Thoracic Oncology and Respiratory Medicine, Tokyo Metropolitan Cancer and Infectious Diseases Center, Komagome Hospital, Tokyo, JapanNippon Boehringer Ingelheim Co., Ltd., Tokyo, JapanDepartment of Surgery, Teikyo University Mizoguchi Hospital, Tokyo, JapanCancer Precision Medicine Center, Japanese Foundation for Cancer Research, Koto-ku, Tokyo, JapanCancer Precision Medicine Center, Japanese Foundation for Cancer Research, Koto-ku, Tokyo, JapanDivision of Medical Oncology, Department of Internal Medicine, Teikyo University School of Medicine, Tokyo, Japan; Corresponding author at: Division of Medical Oncology, Department of Internal Medicine, Teikyo University School of Medicine, 2-11-1, Kaga, Itabashi-ku, Tokyo, Japan.Objectives: Plasma-based testing with circulating cell-free DNA (cfDNA) is an active area of biomarker exploratory studies in patients with non-small cell lung cancer (NSCLC) harboring EGFR mutations. The Exosome-focused Translational Research for Afatinib study prospectively explored novel plasma biomarkers for afatinib monotherapy in patients with NSCLC harboring EGFR mutations using genomics, proteomics, epigenomics, and metabolomics. Herein, we present the results of the genomics part. Materials and Methods: Clinical data of afatinib were matched with next generation sequencing (NGS)-based genomics data of cfDNA (n = 101) and extracellular vesicle DNA (evDNA) (n = 99) from pretreatment plasma samples. Results: The detection sensitivity of cfDNA and evDNA mutations was 86 % (87/101) and 37 % (37/99), respectively. When cfDNA mutations were classified into tissue-matched (any EGFR mutations consistent with those identified in tissue) (n = 28), tissue-unmatched (n = 59), and mutation-undetected (n = 14) groups, cfDNA mutation status was a predictor of progression-free survival (PFS) (p < 0.01) and overall survival (OS) (p < 0.01). EvDNA mutation status was a predictor of OS (p < 0.01) rather than PFS (p = 0.48). When the tissue-unmatched cfDNA group was subclassified into EGFR-related (n = 49) and EGFR-unrelated (n = 10) groups, the EGFR-unrelated group had a median PFS and 3-year OS rate of 31.2 months and 80.0 %, respectively. EGFR-unrelated and mutation-undetected cfDNA groups (n = 24) exhibited a median PFS and 3-year OS rate of >30 months and >80 %, respectively, with afatinib monotherapy. Conclusion: This is the first large-scale prospective study of NGS-based concurrent testing for plasma cfDNA and evDNA mutations. The findings suggest that cfDNA mutation status is a promising plasma biomarker for afatinib monotherapy.http://www.sciencedirect.com/science/article/pii/S2468294225000887Plasma biomarkerCell-free DNAExtracellular vesicle-derived DNANon-small cell lung cancerAfatinib
spellingShingle Tomonori Makiguchi
Hisashi Tanaka
Kei Morikawa
Aya Hirata
Hidetoshi Itani
Shigeru Tanzawa
Kageaki Watanabe
Hiroyuki Yasuda
Kazuya Horiuchi
Hideyuki Nakagawa
Yoshitaka Seki
Yoshiro Nakahara
Kentaro Hayashi
Nobumasa Takahashi
Takeo Endo
Akihiro Bessho
Tetsuya Okano
Kiyoshi Takeyama
Akikazu Kawase
Makoto Endo
Toshiya Maekura
Kenji Nemoto
Nagio Takigawa
Kazuma Kishi
Kenzo Soejima
Yusuke Okuma
Akira Togashi
Noriyuki Matsutani
Hiroki Shinchi
Koji Ueda
Nobuhiko Seki
Plasma biomarkers for afatinib monotherapy in EGFR-mutated non-small cell lung cancer: Novel insights from companion genomics analysis of the EXTRA study
Cancer Treatment and Research Communications
Plasma biomarker
Cell-free DNA
Extracellular vesicle-derived DNA
Non-small cell lung cancer
Afatinib
title Plasma biomarkers for afatinib monotherapy in EGFR-mutated non-small cell lung cancer: Novel insights from companion genomics analysis of the EXTRA study
title_full Plasma biomarkers for afatinib monotherapy in EGFR-mutated non-small cell lung cancer: Novel insights from companion genomics analysis of the EXTRA study
title_fullStr Plasma biomarkers for afatinib monotherapy in EGFR-mutated non-small cell lung cancer: Novel insights from companion genomics analysis of the EXTRA study
title_full_unstemmed Plasma biomarkers for afatinib monotherapy in EGFR-mutated non-small cell lung cancer: Novel insights from companion genomics analysis of the EXTRA study
title_short Plasma biomarkers for afatinib monotherapy in EGFR-mutated non-small cell lung cancer: Novel insights from companion genomics analysis of the EXTRA study
title_sort plasma biomarkers for afatinib monotherapy in egfr mutated non small cell lung cancer novel insights from companion genomics analysis of the extra study
topic Plasma biomarker
Cell-free DNA
Extracellular vesicle-derived DNA
Non-small cell lung cancer
Afatinib
url http://www.sciencedirect.com/science/article/pii/S2468294225000887
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