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Original Articles
Genomic Insights into Innate Resistance in Early-Stage EGFR-Mutant Non-Small Cell Lung Cancer: A Comprehensive Analysis of Next-Generation Sequencing Data
Hayoung Seong, Soo Han Kim, Mi-Hyun Kim, Ahrong Kim, Ju Sun Song, Jung Seop Eom
Received January 28, 2025  Accepted August 19, 2025  Published online August 25, 2025  
DOI: https://doi.org/10.4143/crt.2025.114    [Epub ahead of print]
AbstractAbstract PDFSupplementary MaterialPubReaderePub
Purpose
Comprehensive genomic profiling of early-stage non-small cell lung cancer (NSCLC) with epidermal growth factor receptor (EGFR) mutations remains limited. This study aimed to investigate genomic profiles of early- and advanced-stage EGFR-mutant NSCLC and identify potential innate resistance mechanisms to EGFR-tyrosine kinase inhibitors (TKIs) using targeted next-generation sequencing (NGS).
Materials and Methods
This retrospective observational study analyzed genomic profiles of patients with early-stage (IA-IIIA) and advanced-stage (IIIB-IV) EGFR-mutant NSCLC from the Lung Cancer NGS registry. Targeted NGS was performed to assess concurrent genetic alterations (GAs), tumor mutational burden (TMB), and variant allele frequency (VAF) of EGFR mutations.
Results
Overall, 160 patients (100 early-stage and 60 advanced-stage) were analyzed. The proportion of patients with concurrent GAs was not significantly different between stages (82.0% vs. 91.7%, p=0.092). Median TMB was 3.8 mutations/Mb in both stages, with no significant difference (p=0.206). However, the median VAF of EGFR mutations was significantly lower in early-stage compared to that in advanced-stage (19.3% vs. 29.6%, p=0.002). While TMB remained unchanged with disease progression (p=0.192), VAF of EGFR mutations increased significantly (p < 0.001). Moreover, the frequencies of concurrent single nucleotide variants and copy number variants were significantly lower in early-stage NSCLC.
Conclusion
Genomic heterogeneity in EGFR-mutant NSCLC arises early in tumorigenesis. The comparable TMB and lower VAF of EGFR mutations in early-stage disease suggest that innate resistance to EGFR-TKIs may be driven by concurrent GAs, supporting the consideration of combination therapies even in early-stage EGFR-mutant NSCLC.
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Lung and Thoracic cancer
Novel Bronchoscopy Method for Molecular Profiling of Lung Cancer: Targeted Washing Technique
Mi-Hyun Kim, Hayoung Seong, Hyojin Jang, Saerom Kim, Wanho Yoo, Soo Han Kim, Jeongha Mok, Kwangha Lee, Ki Uk Kim, Min Ki Lee, Jung Seop Eom
Cancer Res Treat. 2026;58(1):107-114.   Published online February 26, 2025
DOI: https://doi.org/10.4143/crt.2024.1128
AbstractAbstract PDFSupplementary MaterialPubReaderePub
Purpose
There have been efforts to find alternative samples other than standard samples of tissue or plasma for mutational analyses for lung cancer patients. However, no other sample or technique has replaced the mutational analyses using standard samples. In this prospective study, we assessed a novel bronchoscopy method, named as targeted washing technique, for detecting the epidermal growth factor receptor (EGFR) mutation.
Materials and Methods
A 3.0-mm ultrathin bronchoscope was precisely navigated to the target lung lesion with the assistance of virtual bronchoscopic navigation and fluoroscopy. Once the bronchoscope is placed in front of target lung lesion, 0.9% normal saline was instilled for targeted washing. EGFR testing using targeted washing fluid (TWF) was compared to standard methods using plasma or tumor tissue.
Results
In 41 TWF samples, the T790M mutation was detected in tissue, plasma, and TWF samples at rates of 22.0%, 9.8%, and 29.3%, respectively. The overall EGFR T790M detection rate using tissue, plasma, or TWF samples was 36.6%, with TWF samples increasing the T790M mutation detection rate by up to 10%. The accuracy of T790M mutation detection using TWF sample was 82.9% compared with standard samples. Four patients were found to have the EGFR T790M mutation solely through EGFR testing using TWF, which repeated rebiopsies using either plasma or tissue finally confirmed to have the T790M mutation.
Conclusion
We demonstrated the clinical potential of targeted washing technique for molecular testing, which can be a good option to overcome spatial heterogeneity, low sensitivity of plasma sample or technical limitations in collecting tumor tissues.

Citations

Citations to this article as recorded by  
  • Comparison of the safety and efficacy of remimazolam for sedation during bronchoscopy: a meta-analysis of randomized controlled trials
    Yupei Yuan, Chunlei Chang, Jing Zhang, Liang Liang
    PeerJ.2026; 14: e20552.     CrossRef
  • 3,102 View
  • 131 Download
  • 2 Web of Science
  • 1 Crossref
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Development of the Korean Association for Lung Cancer Clinical Practice Guidelines: Recommendations on Radial Probe Endobronchial Ultrasound for Diagnosing Lung Cancer - An Updated Meta-Analysis
Soo Han Kim, Hyun Sung Chung, Jinmi Kim, Mi-Hyun Kim, Min Ki Lee, Insu Kim, Jung Seop Eom
Cancer Res Treat. 2024;56(2):464-483.   Published online November 29, 2023
DOI: https://doi.org/10.4143/crt.2023.749
AbstractAbstract PDFSupplementary MaterialPubReaderePub
Purpose
Radial probe endobronchial ultrasound (RP-EBUS) accurately locates peripheral lung lesions (PLLs) during transbronchial biopsy (TBB). We performed an updated meta-analysis of the diagnostic yield of TBB for PLLs using RP-EBUS to generate recommendations for the development of the Korean Association of Lung Cancer guidelines.
Materials and Methods
We systematically searched MEDLINE and EMBASE (from January 2013 to December 2022), and performed a meta-analysis using R software. The diagnostic yield was evaluated by dividing the number of successful diagnoses by the total lesion number. Subgroup analysis was performed to identify related factors.
Results
Forty-one studies with a total of 13,133 PLLs were included. The pooled diagnostic yield of RP-EBUS was 0.72 (95% confidence interval [CI], 0.70 to 0.75). Significant heterogeneity was observed among studies (χ2=292.38, p < 0.01, I2=86.4%). In a subgroup analysis, there was a significant difference in diagnostic yield based on RP-EBUS findings (within, adjacent to, invisible), with a risk ratio of 1.45 (95% CI, 1.23 to 1.72) between within and adjacent to, 4.20 (95% CI, 1.89 to 9.32) between within and invisible, and 2.59 (95% CI, 1.32 to 5.01) between adjacent to and invisible. There was a significant difference in diagnostic yield based on lesion size, histologic diagnosis, computed tomography (CT) bronchus sign, lesion character, and location from the hilum. The overall complication rate of TBB with RP-EBUS was 6.8% (bleeding, 4.5%; pneumothorax, 1.4%).
Conclusion
Our study showed that TBB with RP-EBUS is an accurate diagnostic tool for PLLs with good safety profiles, especially for PLLs with within orientation on RP-EBUS or positive CT bronchus sign.

Citations

Citations to this article as recorded by  
  • Peripheral bronchoscopy: back to basics
    Pipetius Quah, Pyng Lee
    Current Opinion in Pulmonary Medicine.2026; 32(1): 8.     CrossRef
  • Efficacy and safety of radial probe endobronchial ultrasound–transbronchial lung biopsy in peripheral pulmonary lesions without guide sheath and fluoroscopy
    Cong Nguyen Hai, The Nguyen Minh, Toan Hoang Thanh, Loi Trinh Duc, Cuong Hoang Xuan
    Therapeutic Advances in Respiratory Disease.2026;[Epub]     CrossRef
  • Can intraoperative improvement of radial endobronchial ultrasound imaging enhance the diagnostic yield in peripheral pulmonary lesions?
    Kazuki Nishida, Takayasu Ito, Shingo Iwano, Shotaro Okachi, Shota Nakamura, Basile Chrétien, Toyofumi Fengshi Chen-Yoshikawa, Makoto Ishii
    BMC Pulmonary Medicine.2025;[Epub]     CrossRef
  • Transbronchial Cryobiopsy under Simultaneous Confocal Laser Endomicroscopy Guidance for Peripheral Pulmonary Lesions: A Pilot Study
    Daniela Gompelmann, Anastasia Papaporfyriou, Christina Bal, Yasmin Merza, Berta Mosleh, Felicitas Oberndorfer, Edda Tschernko, Mir Alireza Hoda, Marco Idzko
    Respiration.2025; 105(2): 305.     CrossRef
  • A predictive model for diagnosing peripheral pulmonary lesions using radial probe endobronchial ultrasound images
    Minlong Zhang, Cuiping Yang, Yinghua Guo
    Scientific Reports.2025;[Epub]     CrossRef
  • 7,013 View
  • 188 Download
  • 6 Web of Science
  • 5 Crossref
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Should We Perform Repeated Re-biopsy for the Detection of T790M Mutation?
Saerom Kim, Soo Han Kim, Jinmi Kim, Mi-Hyun Kim, Min Ki Lee, Jung Seop Eom
Cancer Res Treat. 2023;55(4):1190-1197.   Published online April 17, 2023
DOI: https://doi.org/10.4143/crt.2023.320
AbstractAbstract PDFPubReaderePub
Purpose
Epidermal growth factor receptor (EGFR) T790M mutations have been detected in the second or third rebiopsy, even if the T790M mutation was not identified in the first rebiopsy. This meta-analysis investigated the EGFR T790M mutation detection rates and its additional advantages with repeated rebiopsies.
Materials and Methods
We searched through the PubMed and EMBASE databases up to June 2022. Studies reporting rebiopsy to identify the EGFR T790M mutation in case of disease progression among patients with advanced non-small cell lung cancer and multiple rebiopsies were included. The quality of the included studies was checked using the Quality Assessment of Diagnostic Accuracy Studies-2 (QUADAS-2) tool.
Results
Eight studies meeting the eligibility criteria, reporting 1,031 EGFR mutation–positive patients were selected. The pooled EGFR T790M mutation detection rate of the first and repeated rebiopsies were 0.442 (95% confidence interval [CI], 0.411 to 0.473; I2=84%; p < 0.01) and 0.465 (95% CI, 0.400 to 0.530; I2=69%; p < 0.01), respectively. Overall, the pooled detection rate of EGFR T790M mutation was 0.545 (95% CI, 0.513 to 0.576), which increased by 10.3% with repeated rebiopsies.
Conclusion
This meta-analysis identified that repeated rebiopsy increases the detection rate of EGFR T790M mutation by 10.3%, even if EGFR T790M mutation is not detected in the first rebiopsy. Our results indicate that the spatiotemporal T790M heterogeneity can be overcome with repeated rebiopsy.

Citations

Citations to this article as recorded by  
  • Novel Bronchoscopy Method for Molecular Profiling of Lung Cancer: Targeted Washing Technique
    Mi-Hyun Kim, Hayoung Seong, Hyojin Jang, Saerom Kim, Wanho Yoo, Soo Han Kim, Jeongha Mok, Kwangha Lee, Ki Uk Kim, Min Ki Lee, Jung Seop Eom
    Cancer Research and Treatment.2026; 58(1): 107.     CrossRef
  • Enhanced Detection of Druggable Mutations in Non–Small Cell Lung Cancer Using Targeted Collection of Bronchial Washing Fluid Compared With Plasma and Tumor Tissue
    Mi-Hyun Kim, Soo Han Kim, Hayoung Seong, Jung Seop Eom
    JCO Precision Oncology.2025;[Epub]     CrossRef
  • A Multicenter Study on Unnecessary Rebiopsies in CT‐Guided Percutaneous Transthoracic Needle Biopsy of Pulmonary Lesions
    Yangfan He, Huanhuan He, Yubo Cai, Shanshan Lyu, Zhengyi Zhou, Chengyou Zheng, Xinke Zhang, Jinling Duan, Jierong Chen, Jiewei Chen
    Cancer Medicine.2025;[Epub]     CrossRef
  • Clinical utility of repeated rebiopsy for EGFR T790M mutation detection in non-small cell lung cancer
    Eun Hye Lee, Se Hyun Kwak, Kyeong Yeon Kim, Chi Young Kim, Sang Hoon Lee, Seok-Jae Heo, Yoon Soo Chang, Eun Young Kim
    Frontiers in Oncology.2024;[Epub]     CrossRef
  • Repeated rebiopsy for detection of EGFR T790M mutation in patients with advanced-stage lung adenocarcinoma: Associated factors and treatment outcomes of Osimertinib
    Taeyun Kim, Junsu Choe, Sun Hye Shin, Byeong-Ho Jeong, Kyungjong Lee, Hojoong Kim, Se-Hoon Lee, Sang-Won Um, Hamidreza Montazeri Aliabadi
    PLOS ONE.2024; 19(9): e0310079.     CrossRef
  • Rebiopsie tumorale : quand ? pour qui ? pourquoi ? comment ?
    V. Fallet
    Revue des Maladies Respiratoires Actualités.2023; 15(2): 2S121.     CrossRef
  • 5,356 View
  • 208 Download
  • 5 Web of Science
  • 6 Crossref
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The Additive Impact of Transbronchial Cryobiopsy Using a 1.1-mm Diameter Cryoprobe on Conventional Biopsy for Peripheral Lung Nodules
Soo Han Kim, Jeongha Mok, Eun-Jung Jo, Mi-Hyun Kim, Kwangha Lee, Ki Uk Kim, Hye-Kyung Park, Min Ki Lee, Jung Seop Eom
Cancer Res Treat. 2023;55(2):506-512.   Published online November 1, 2022
DOI: https://doi.org/10.4143/crt.2022.1008
AbstractAbstract PDFSupplementary MaterialPubReaderePub
Purpose
The diagnostic yield of transbronchial biopsy (TBB) using radial probe endobronchial ultrasound (RP-EBUS) is 71%, which is lower than that of transthoracic needle biopsy. We investigated the performance and safety of sequential transbronchial cryobiopsy (TBC) using a novel 1.1-mm diameter cryoprobe, after conventional TBB using RP-EBUS for the diagnosis of peripheral lung lesions (PLLs).
Materials and Methods
From April 2021 to November 2021, 110 patients who underwent bronchoscopy using RP-EBUS for the diagnosis of PLL ≤ 30 mm were retrospectively included in our study. All records were followed until June 2022.
Results
The overall diagnostic yield of combined TBB and TBC was 79.1%, which was higher than 60.9% of TBB alone (p=0.005). The diagnostic yield of sequential TBC was 65.5%, which increased the overall diagnostic yield by 18.2%. The surface area of tissues by TBC (mean area, 18.5 mm2) was significantly larger than those of TBB by 1.5-mm forceps (3.4 mm2, p < 0.001) and 1.9-mm forceps (3.7 mm2, p=0.011). In the multivariate analysis, PLLs with the longest diameter of ≤ 22 mm were found to be related to additional diagnostic benefits from sequential TBC (odds ratio, 3.51; 95% confidence interval, 1.043 to 11.775; p=0.042). Complications were found in 10.5% of the patients: pneumothorax (1.0%), infection (1.0%), and significant bleeding (8.6%). None of the patients developed any life-threatening complications.
Conclusion
Sequential TBC with a 1.1-mm cryoprobe improved the performance of conventional TBB using RP-EBUS without serious complications.

Citations

Citations to this article as recorded by  
  • A refined diagnostic approach for interstitial lung disease: efficient and safe transbronchial cryobiopsy using a 1.1-mm cryoprobe
    Qinghua Zhang, Jinyan Yu, Xiaohao Zhang, Tiangang Ma, Yan Wang
    Frontiers in Medicine.2026;[Epub]     CrossRef
  • Comparative study of transbronchial cryobiopsy and transbronchial biopsy for diagnostic yield in peripheral pulmonary lesions
    Hao-Chun Chang, Ching-Kai Lin, Lun‑Che Chen, Ling‑Kai Chang, Shun‑Mao Yang, Li-Ta Keng, Chong‑Jen Yu
    Annals of Medicine.2026;[Epub]     CrossRef
  • Clinical applications of cryobiopsy in the diagnosis of thoracic malignancies: a comprehensive review
    Miwa Kamatani, Nobuyasu Awano, Takehiro Izumo
    Japanese Journal of Clinical Oncology.2026; 56(4): 373.     CrossRef
  • Complete resolution of non-tuberculous mycobacterial pulmonary nodule following cryobiopsy: The first case report
    Sung Joon Han, Chaeuk Chung, Dongil Park
    Diagnostic Pathology.2025;[Epub]     CrossRef
  • Feasibility of a Modified Bronchoscopic Transparenchymal Nodule Access Technique (‘Essen Tunnel’) for Improving the Diagnosis of Intraparenchymal Pulmonary Lesions
    Erik Büscher, Faustina Funke, Jane Winantea, Hanna Zellerhoff, Johannes Wienker, Marcel Opitz, Christian Taube, Kaid Darwiche
    Respirology.2025; 30(9): 851.     CrossRef
  • Enhanced Detection of Druggable Mutations in Non–Small Cell Lung Cancer Using Targeted Collection of Bronchial Washing Fluid Compared With Plasma and Tumor Tissue
    Mi-Hyun Kim, Soo Han Kim, Hayoung Seong, Jung Seop Eom
    JCO Precision Oncology.2025;[Epub]     CrossRef
  • Comparison of sequential cryoprobe and biopsy forceps in endobronchial ultrasound-guided transbronchial needle aspiration for mediastinal and hilar lesions: a prospective observational study
    Ching-Kai Lin, Sheng-Yuan Ruan, Hung-Jen Fan, Hao-Chun Chang, Yen-Ting Lin, Chao-Chi Ho
    Annals of Medicine.2025;[Epub]     CrossRef
  • Numerical simulation of bioheat transfer during bronchial cryobiopsy using cryoprobes of different diameters
    Junhong Tang, Yudong Bao, Wenqing Du, Wen Wei
    Cryobiology.2025; 121: 105320.     CrossRef
  • American Association for Bronchology and Interventional Pulmonology (AABIP) Evidence-Based Guidelines on Bronchoscopic Diagnosis and Staging of Lung Cancer
    Russell J. Miller, Ara A. Chrissian, Fayez Kheir, Majid Shafiq, Abigail T. Chua, Neal Navani, Francisco A. Almeida, Abdul H. Alraiyes, Paul A. Bain, Christina R. Bellinger, Cherng H. Chao, George Z. Cheng, Rebecca Cloyes, Javier Diaz-Mendoza, David M. DiB
    Journal of Bronchology & Interventional Pulmonology.2025;[Epub]     CrossRef
  • Transbronchial cryobiopsy for diagnosing pulmonary hyalinizing granuloma: a case report
    Akihiko Amano, Takashi Niwa, Masamitsu Hamakawa, Yasushi Fukuda, Toshihide Yokoyama, Tadashi Ishida
    BMC Pulmonary Medicine.2025;[Epub]     CrossRef
  • Advances in Invasive Diagnostics in Lung Cancer
    Pascalin Roy, Sara Shadchehr, Anne V. Gonzalez
    Seminars in Respiratory and Critical Care Medicine.2025; 46(05): 530.     CrossRef
  • The role of bronchoscopy in the diagnosis of solitary pulmonary nodules in 2025
    Jiří Votruba
    Vnitřní lékařství.2025; 71(5): E6.     CrossRef
  • Transbronchial lung cryobiopsy for peripheral pulmonary lesions. A narrative review
    Y. Tang, S. Tian, H. Chen, X. Li, X. Pu, X. Zhang, Y. Zheng, Y. Li, H. Huang, C. Bai
    Pulmonology.2024; 30(5): 475.     CrossRef
  • Transbronchial Tumor Ablation
    Russell Miller, George Cheng
    Current Pulmonology Reports.2024; 13(1): 103.     CrossRef
  • Using cryoprobes of different sizes combined with cone-beam computed tomography-derived augmented fluoroscopy and endobronchial ultrasound to diagnose peripheral pulmonary lesions: a propensity-matched study
    Ching-Kai Lin, Sheng-Yuan Ruan, Hung-Jen Fan, Hao-Chun Chang, Yen-Ting Lin, Chao-Chi Ho
    Respiratory Research.2024;[Epub]     CrossRef
  • Next‐generation sequencing using tissue specimen collected with a 1.1 mm‐diameter cryoprobe in patients with lung cancer
    Mi‐Hyun Kim, Soo Han Kim, Geewon Lee, Jeongha Mok, Min Ki Lee, Ju Sun Song, Jung Seop Eom
    Respirology.2024; 29(4): 333.     CrossRef
  • Development of the Korean Association for Lung Cancer Clinical Practice Guidelines: Recommendations on Radial Probe Endobronchial Ultrasound for Diagnosing Lung Cancer - An Updated Meta-Analysis
    Soo Han Kim, Hyun Sung Chung, Jinmi Kim, Mi-Hyun Kim, Min Ki Lee, Insu Kim, Jung Seop Eom
    Cancer Research and Treatment.2024; 56(2): 464.     CrossRef
  • Navigational bronchoscopy with tranbronchial cryobiopsy in differential diagnosis of peripheral pulmonary lesions
    Ya.O. Chesalina, I.Yu. Shabalina, L.A. Semenova, I.V. Sivokozov
    Pirogov Russian Journal of Surgery.2024; (6): 36.     CrossRef
  • Advanced Bronchoscopic Diagnostic Techniques in Lung Cancer
    Dongil Park
    Tuberculosis and Respiratory Diseases.2024; 87(3): 282.     CrossRef
  • Clinical utility of rapid on-site evaluation of brush cytology during bronchoscopy using endobronchial ultrasound with a guide sheath
    Kazuhiro Nishiyama, Kei Morikawa, Shotaro Kaneko, Makoto Nishida, Aya Matsushima, Yoshihiro Nishi, Yu Numata, Yusuke Shinozaki, Hajime Tsuruoka, Hirotaka Kida, Hiroshi Handa, Naoki Shimada, Chie Okawa, Nobuyuki Ohike, Junki Koike, Masamichi Mineshita
    Scientific Reports.2024;[Epub]     CrossRef
  • Bronchial branch tracing navigation in ultrathin bronchoscopy-guided radial endobronchial ultrasound for peripheral pulmonary nodule
    Sze Shyang Kho, Shirin Hui Tan, Swee Kim Chan, Chan Sin Chai, Siew Teck Tie
    BMC Pulmonary Medicine.2024;[Epub]     CrossRef
  • The diagnosis of peripheral lung lesions: transbronchial biopsy using a radial probe endobronchial ultrasound
    Jung Seop Eom
    Journal of the Korean Medical Association.2023; 66(3): 166.     CrossRef
  • Clinical outcomes of transbronchial cryobiopsy using a 1.1-mm diameter cryoprobe for peripheral lung lesions - A prospective pilot study
    Soo Han Kim, Jeongha Mok, Saerom Kim, Wan Ho Yoo, Eun-Jung Jo, Mi-Hyun Kim, Kwangha Lee, Ki Uk Kim, Hye-Kyung Park, Min Ki Lee, Jung Seop Eom
    Respiratory Medicine.2023; 217: 107338.     CrossRef
  • 8,222 View
  • 271 Download
  • 29 Web of Science
  • 23 Crossref
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