Gefitinib plus chemotherapy versus placebo plus chemotherapy in EGFR-mutation-positive non-small-cell lung cancer after progression on first-line gefitinib (IMPRESS): a phase 3 randomised trial

Soria, Jean-Charles; Wu, Yi-Long; Nakagawa, Kazuhiko; Kim, Sang-We; Yang, Jin-Ji; Ahn, Myung-Ju; Wang, Jie; Yang, James Chih-Hsin; Lu, You; Atagi, Shinji; Ponce, Santiago; Lee, Dae Ho; Liu, Yunpeng; Yoh, Kiyotaka; Zhou, Jian-Ying; Shi, Xiaojin; Webster, Alan; Jiang, Haiyi; Mok, Tony S K

doi:10.1016/s1470-2045(15)00121-7

Cited by 413Lung Cancer Treatments and MutationsLung Cancer Diagnosis and TreatmentHER2/EGFR in Cancer Research

Gefitinib plus chemotherapy versus placebo plus chemotherapy in EGFR-mutation-positive non-small-cell lung cancer after progression on first-line gefitinib (IMPRESS): a phase 3 randomised trial

Soria, Jean-Charles, Wu, Yi-Long, Nakagawa, Kazuhiko, Kim, Sang-We, Yang, Jin-Ji, Ahn, Myung-Ju, Wang, Jie, Yang, James Chih-Hsin +11 more·2015·The Lancet Oncology

DOI 10.1016/s1470-2045(15)00121-7

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Abstract

Background Optimum management strategies for patients with advanced non-small-cell lung cancer (NSCLC) with acquired resistance to EGFR tyrosine-kinase inhibitors are undefined. We aimed to assess the efficacy and safety of continuing gefitinib combined with chemotherapy versus chemotherapy alone in patients with EGFR-mutation-positive advanced NSCLC with acquired resistance to first-line gefitinib.Methods The randomised, phase 3, multicentre IMPRESS study was done in 71 centres in 11 countries in Europe and the Asia-Pacific region. Eligible patients were aged at least 18 years with histologically confirmed, chemotherapy-naive, stage IIIB-IV EGFR-mutation-positive advanced NSCLC with previous disease control with first-line gefitinib and recent disease progression (Response Evaluation Criteria in Solid Tumors version 1.1). Participants were randomly assigned (1:1) by central block randomisation to oral gefitinib 250 mg or placebo once daily in tablet form; randomisation did not include stratification factors. All patients also received the platinum-based doublet chemotherapy cisplatin 75 mg/m(2) plus pemetrexed 500 mg/m(2) on the first day of each cycle. After completion of a maximum of six chemotherapy cycles, patients continued their randomly assigned treatment until disease progression or another discontinuation criterion was met. All study investigators and participants were masked to treatment allocation. The primary endpoint was progression-free survival in the intention-to-treat population. Safety was assessed in patients who received at least one dose of study treatment. The study has completed enrolment, but patients are still in follow-up for overall survival. This trial is registered with ClinicalTrials.gov, number NCT01544179.Findings Between March 29, 2012, and Dec 20, 2013, 265 patients were randomly assigned: 133 to the gefitinib group and 132 to the placebo group. At the time of data cutoff (May 5, 2014), 98 (74%) patients had disease progression in the gefitinib group compared with 107 (81%) in the placebo group (hazard ratio 0·86, 95% CI 0·65-1·13; p=0·27; median progression-free survival 5·4 months in both groups [95% CI 4·5-5·7 in the gefitinib group and 4·6-5·5 in the placebo group]). The most common adverse events of any grade were nausea (85 [64%] of 132 patients in the gefitinib group and 81 [61%] of 132 patients in the placebo group) and decreased appetite (65 [49%] and 45 [34%]). The most common adverse events of grade 3 or worse were anaemia (11 [8%] of 132 patients in the gefitinib group and five [4%] of 132 patients in the placebo group) and neutropenia (nine [7%] and seven [5%]). 37 (28%) of 132 patients in the gefitinib group and 28 (21%) of 132 patients in the placebo group reported serious adverse events.Interpretation Continuation of gefitinib after radiological disease progression on first-line gefitinib did not prolong progression-free survival in patients who received platinum-based doublet chemotherapy as subsequent line of treatment. Platinum-based doublet chemotherapy remains the standard of care in this setting.Funding AstraZeneca.

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In the IMPRESS study, adding gefitinib to pemetrexed-cisplatin after progression on a first-line EGFR TKI produced no difference in response rates (32% versus 34%) or median PFS (5.4 months in both groups).
“No difference in response rates (32% versus 34%) or median PFS (5.4 months in both groups) was demonstrated.”
From The International Association for the Study of Lung Cancer Consensus Statement on Optimizing Management of EGFR Mutation–Positive Non–Small Cell Lung Cancer: Status in 2016 (2016) · cites this paper as [90]
A subgroup analysis of IMPRESS stratifying by plasma T790M status at progression suggested a role for continuing gefitinib in T790M-negative patients.
“However, a subsequent subgroup analysis stratifying patients according to plasma T790M status at time of progression suggested a role for continuing gefitinib in those who are T790M negative.”
From The International Association for the Study of Lung Cancer Consensus Statement on Optimizing Management of EGFR Mutation–Positive Non–Small Cell Lung Cancer: Status in 2016 (2016) · cites this paper as [90]
When rebiopsy is not feasible or T790M is not detected, platinum-based chemotherapy alone is standard, and no data support continuing the EGFR TKI with platinum-based chemotherapy.
“At the present time, when rebiopsy is not feasible or when the EGFR T790M mutation is not detected as a resistance mechanism, the standard of care is represented by platinum-based chemotherapy alone.There is no data to support continuation of the EGFR TKI with platinum-based chemotherapy [I, A] [125].”
From Metastatic non-small-cell lung cancer: ESMO Clinical Practice Guidelines for diagnosis, treatment and follow-up (2016) · cites this paper as [125]

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Background
Lung cancer in never smokers—the East Asian experience
Zhou, F., & Zhou, C. (2018) · Translational Lung Cancer Research · doi:10.21037/tlcr.2018.05.14 · Cited by 208 · see citing works
“com in patients with EGFR mutation-positive advanced NSCLC after failure of first-line gefitinib (56).”
Background
The International Association for the Study of Lung Cancer Consensus Statement on Optimizing Management of EGFR Mutation–Positive Non–Small Cell Lung Cancer: Status in 2016
Tan, D. S. W., Yom, S. S., Tsao, M. S., Pass, H. I., Kelly, K., Peled, N., Yung, R. C., Wistuba, I. I., Yatabe, Y., Unger, M., et al. (2016) · Journal of Thoracic Oncology · doi:10.1016/j.jtho.2016.05.008 · Cited by 201 · see citing works
“The question of whether a EGFR TKI should be continued beyond progression when switching to platinum-based chemotherapy was addressed in the IMPRESS study, in which patients received up to six cycles of pemetrexed-cisplatin, with or without gefitinib, after progression from a firstline EGFR TKI.90 No difference in res…”
BackgroundInfluentialSelf-citation
A New Approach to Predict Progression-free Survival in Stage IV EGFR-mutant NSCLC Patients with EGFR-TKI Therapy
Song, J., Shi, J., Dong, D., Fang, M., Zhong, W., Wang, K., Wu, N., Huang, Y., Liu, Z., Cheng, Y., et al. (2018) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-17-2507 · Cited by 187 · see citing works
“Consistent with previous randomized trails (4, 6, 7) and meta-analysis (8), EGFR-TKI therapy showed an overall longer PFS compared with chemotherapy in our multicenter study.”
Result
Emerging Treatment Paradigms for EGFR-Mutant Lung Cancers Progressing on Osimertinib: A Review
Piper‐Vallillo, A. J., Sequist, L. V. D., & Piotrowska, Z. (2020) · Journal of Clinical Oncology · doi:10.1200/jco.19.03123 · Cited by 189 · see citing works
“The phase III IMPRESS study assessed the benefit of continuing gefitinib or placebo in combination with second-line, platinum-based chemotherapy and showed no improvement in PFS or OS.69 However, results from 3 more recent phase III studies have suggested there could be significant OS benefits to combining chemotherap…”
Background
Randomized Phase II Trial of Gefitinib With and Without Pemetrexed as First-Line Therapy in Patients With Advanced Nonsquamous Non–Small-Cell Lung Cancer With Activating Epidermal Growth Factor Receptor Mutations
Cheng, Y., Murakami, H., Yang, P., He, J., Nakagawa, K., Kang, J. H., Kim, J.-H., Wang, X., Enatsu, S., Puri, T., et al. (2016) · Journal of Clinical Oncology · doi:10.1200/jco.2016.66.9218 · Cited by 181 · see citing works
Self-citation
Nivolumab Plus Erlotinib in Patients With EGFR-Mutant Advanced NSCLC
Gettinger, S. N., Hellmann, M. D., Chow, L. Q. M., Borghaei, H., Antonia, S. J., Brahmer, J. R., Goldman, J. W., Gerber, D. E., Juergens, R. A., Shepherd, F. A., et al. (2018) · Journal of Thoracic Oncology · doi:10.1016/j.jtho.2018.05.015 · Cited by 180 · see citing works
Gefitinib Plus Chemotherapy Versus Chemotherapy in Epidermal Growth Factor Receptor Mutation–Positive Non–Small-Cell Lung Cancer Resistant to First-Line Gefitinib (IMPRESS): Overall Survival and Biomarker Analyses
Mok, T. S. K., Kim, S., Wu, Y.-L. L. C., Nakagawa, K., Yang, J., Ahn, M., Wang, J., Yang, J. C., Lü, Y., Atagi, S., et al. (2017) · Journal of Clinical Oncology · doi:10.1200/jco.2017.73.9250 · Cited by 179 · see citing works
Self-citation
Nivolumab Plus Chemotherapy in Epidermal Growth Factor Receptor–Mutated Metastatic Non–Small-Cell Lung Cancer After Disease Progression on Epidermal Growth Factor Receptor Tyrosine Kinase Inhibitors: Final Results of CheckMate 722
Mok, T. S. K., Nakagawa, K., Park, K., Ohe, Y., Girard, N., Kim, H. R., Wu, Y.-L. L. C., Gainor, J. F., Lee, S., Chiu, C., et al. (2024) · Journal of Clinical Oncology · doi:10.1200/jco.23.01017 · Cited by 166 · see citing works
Self-citation
Management of advanced non-small cell lung cancers with known mutations or rearrangements: latest evidence and treatment approaches
Shea, M., Costa, D. B., & Rangachari, D. (2015) · Therapeutic Advances in Respiratory Disease · doi:10.1177/1753465815617871 · Cited by 157 · see citing works
Intrinsic resistance to EGFR tyrosine kinase inhibitors in advanced non-small-cell lung cancer with activating EGFR mutations
Wang, J., Wang, B., Chu, H., & Yao, Y. (2016) · OncoTargets and Therapy · doi:10.2147/ott.s106399 · Cited by 141 · see citing works
“A Phase III IMPRESS study showed no significant improvement in PFS with continued use of gefitinib plus pemetrexed/cisplatin doublet chemotherapy compared to chemotherapy alone in 265 EGFR mutationpositive patients who progressed on first-line treatment with EGFR TKIs.(94) However, a recent Phase II study showed that…”
Self-citation
Treatments for EGFR-mutant non-small cell lung cancer (NSCLC): The road to a success, paved with failures
Lee, K. H. (2017) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2017.02.001 · Cited by 142 · see citing works
Therapeutic advances in non‐small cell lung cancer: Focus on clinical development of targeted therapy and immunotherapy
Cheng, Y., Zhang, T., & Xu, Q. (2021) · MedComm · doi:10.1002/mco2.105 · Cited by 125 · see citing works
Molecular Mechanisms and Targeted Therapies Including Immunotherapy for Non-Small Cell Lung Cancer
Nagano, T., TACHIHARA, M. Y., & Nishimura, Y. (2018) · Current Cancer Drug Targets · doi:10.2174/1568009619666181210114559 · Cited by 118 · see citing works
Tepotinib plus osimertinib in patients with EGFR-mutated non-small-cell lung cancer with MET amplification following progression on first-line osimertinib (INSIGHT 2): a multicentre, open-label, phase 2 trial
Wu, Y.-L. L. C., Guarneri, V., Voon, P. J., Lim, B. K., Yang, J., Wislez, M., Huang, C., Liam, C. K., Mazières, J., Tho, L. M., et al. (2024) · The Lancet Oncology · doi:10.1016/s1470-2045(24)00270-5 · Cited by 114 · see citing works
Self-citation
Next-Generation EGFR Tyrosine Kinase Inhibitors for Treating EGFR-Mutant Lung Cancer beyond First Line
Sullivan, I., & Planchard, D. (2017) · Frontiers in Medicine · doi:10.3389/fmed.2016.00076 · Cited by 113 · see citing works
“The trial did not confirm a benefit of maintaining the EGFR TKI, with comparable RRs and PFS in the two arms (18).”
Result
Strategies to overcome acquired resistance to EGFR TKI in the treatment of non-small cell lung cancer
Gao, J., Li, H.-R., Jin, C., Jiang, J., & Ding, J. (2019) · Clinical & Translational Oncology · doi:10.1007/s12094-019-02075-1 · Cited by 112 · see citing works
EGFR exon 20 insertion mutations in Chinese advanced non-small cell lung cancer patients: Molecular heterogeneity and treatment outcome from nationwide real-world study
Yang, G., Li, J., Xu, H., Yang, Y., Yang, L., Xu, F., Xia, B., Zhu, V. W., Nagasaka, M., Yang, Y., et al. (2020) · Lung Cancer · doi:10.1016/j.lungcan.2020.03.014 · Cited by 113 · see citing works
Targeting EGFR in Lung Cancer: Current Standards and Developments
Díaz-Serrano, A., Gella, P., Jiménez, E., Zugazagoitia, J., & Paz-Ares Rodríguez, L. (2018) · Drugs · doi:10.1007/s40265-018-0916-4 · Cited by 108 · see citing works
“This explored gefitinib treatment beyond progression in addition to platinum-based doublet chemotherapy versus chemotherapy alone after disease progression to gefitinib in 265 patients not previously exposed to chemotherapy [119].”
Epidermal Growth Factor Receptor (EGFR)-Mutated Non-Small-Cell Lung Cancer (NSCLC)
O’Leary, C. G., Gasper, H. M., Sahin, K. B., Tang, M., Kulasinghe, A., Adams, M. N., Richard, D. J., & O'Byrne, K. J. (2020) · Pharmaceuticals · doi:10.3390/ph13100273 · Cited by 105 · see citing works
Efficacy and safety of osimertinib in treating EGFR‐mutated advanced NSCLC: A meta‐analysis
Yi, L., Fan, J., Qian, R., Luo, P., & Zhang, J. (2019) · International Journal of Cancer · doi:10.1002/ijc.32097 · Cited by 102 · see citing works
“Several RCTs showed that EGFR-TKIs combined with chemotherapy had no clinical benefit for patients whose disease progressed after first-generation EGFR-TKI therapy.(40,41) Additionally, the effect of alternating with other firstgeneration EGFR-TKIs was unsatisfactory in these patients.”
Background
Overcoming microenvironmental resistance to PD-1 blockade in genetically engineered lung cancer models
Martínez-Usatorre, A., Kadioglu, E., Boivin, G., Cianciaruso, C., Guichard, A., Torchia, B., Zangger, N., Nassiri, S., Keklikoglou, I., Schmittnaegel, M., et al. (2021) · Science Translational Medicine · doi:10.1126/scitranslmed.abd1616 · Cited by 103 · see citing works
Association of EGFR Exon 19 Deletion and EGFR-TKI Treatment Duration with Frequency of T790M Mutation in EGFR-Mutant Lung Cancer Patients
Matsuo, N., Azuma, K., Sakai, K., Hattori, S., Kawahara, A., Ishii, H., Tokito, T., Kinoshita, T., Yamada, K., Nishio, K., et al. (2016) · Scientific Reports · doi:10.1038/srep36458 · Cited by 96 · see citing works
Mechanisms of resistance to third-generation EGFR tyrosine kinase inhibitors
Wang, S., Song, Y., Yan, F., & Liu, D. (2016) · Frontiers of Medicine · doi:10.1007/s11684-016-0488-1 · Cited by 96 · see citing works
The APPLE Trial: Feasibility and Activity of AZD9291 (Osimertinib) Treatment on Positive PLasma T790M in EGFR-mutant NSCLC Patients. EORTC 1613
Remón, J., Menis, J., Hasan, B., Peric, A., Maio, E. D., Novello, S., Reck, M., Berghmans, T., Wasąg, B., Besse, B., et al. (2017) · Clinical Lung Cancer · doi:10.1016/j.cllc.2017.02.005 · Cited by 95 · see citing works
Osimertinib in the treatment of non-small-cell lung cancer: design, development and place in therapy
Santarpía, M., Liguori, A., Karachaliou, N., González‐Cao, M., Daffinà, M. G., D’Aveni, A., Marabello, G., Altavilla, G., & Rosell, R. (2017) · Lung Cancer Targets and Therapy · doi:10.2147/lctt.s119644 · Cited by 100 · see citing works
“A Phase III randomized trial failed to demonstrate the superiority of gefitinib plus cisplatin and pemetrexed compared with chemotherapy and placebo after progression on first-line gefitinib.(51) In addition, the combination of gefitinib and chemotherapy had a detrimental effect on OS, mainly driven by T790M-positive…”
Patient Experience Captured by Quality-of-Life Measurement in Oncology Clinical Trials
Haslam, A., Herrera-Perez, D., Gill, J., & Prasad, V. K. (2020) · JAMA Network Open · doi:10.1001/jamanetworkopen.2020.0363 · Cited by 96 · see citing works
Development of EGFR TKIs and Options to Manage Resistance of Third-Generation EGFR TKI Osimertinib: Conventional Ways and Immune Checkpoint Inhibitors
Wu, L., Ke, L., Zhang, Z., Yu, J., & Meng, X. (2020) · Frontiers in Oncology · doi:10.3389/fonc.2020.602762 · Cited by 97 · see citing works
A Comparison of ddPCR and ARMS for detecting EGFR T790M status in ctDNA from advanced NSCLC patients with acquired EGFR‐TKI resistance
Wang, W., Song, Z., & Zhang, Y. (2016) · Cancer Medicine · doi:10.1002/cam4.978 · Cited by 93 · see citing works
“Trials including ASPIRATION [41] and IMPRESS [42] explored the treatment strategies for EGFRTKI failure.”
MethodInfluential
Toripalimab plus chemotherapy as second-line treatment in previously EGFR-TKI treated patients with EGFR-mutant-advanced NSCLC: a multicenter phase-II trial
Jiang, T., Wang, P., Zhang, J., Zhao, Y., Zhou, J., Fan, Y., Shu, Y., Liu, X., Zhang, H., He, J., et al. (2021) · Signal Transduction and Targeted Therapy · doi:10.1038/s41392-021-00751-9 · Cited by 92 · see citing works
Self-citation
Current treatment strategies for EGFR -mutated non-small cell lung cancer: from first line to beyond osimertinib resistance
Araki, T., Kanda, S., Horinouchi, H., & Ohe, Y. (2023) · Japanese Journal of Clinical Oncology · doi:10.1093/jjco/hyad052 · Cited by 100 · see citing works
“13)] (23), and OS was inferior in the continuing group [median OS, 13.”
Background
EGFR tyrosine kinase inhibitor (TKI) in patients with advanced non-small cell lung cancer (NSCLC) harboring uncommon EGFR mutations: A real-world study in China
Xu, J., Jin, B., Chu, T., Dong, X., Yang, H., Zhang, Y., Wu, D., Lou, Y., Zhang, X., Wang, H., et al. (2016) · Lung Cancer · doi:10.1016/j.lungcan.2016.01.018 · Cited by 92 · see citing works
Epidermal growth factor receptor inhibition downregulatesHelicobacter pylori-induced epithelial inflammatory responses, DNA damage and gastric carcinogenesis
Sierra, J. C., Asim, M., Verriere, T. G., Piazuelo, M. B., Suárez, G., Romero–Gallo, J., Delgado, A. G., Wroblewski, L. E., Barry, D. P., Peek, R. M., et al. (2017) · Gut · doi:10.1136/gutjnl-2016-312888 · Cited by 81 · see citing works
Combination of EGFR-TKIs and chemotherapy in advanced EGFR mutated NSCLC: Review of the literature and future perspectives
Rebuzzi, S. E., Alfieri, R. R., Monica, S. L., Minari, R., Petronini, P. G., & Tiseo, M. (2019) · Critical Reviews in Oncology/Hematology · doi:10.1016/j.critrevonc.2019.102820 · Cited by 80 · see citing works
Osimertinib treatment based on plasma T790M monitoring in patients with EGFR-mutant non-small-cell lung cancer (NSCLC): EORTC Lung Cancer Group 1613 APPLE phase II randomized clinical trial
Remón, J., Besse, B., Ponce-Aix, S., Callejo, A., Al-Rabi, K., Bernabé, R., Greillier, L., Majem, M., Reguart, N., Monnet, I., et al. (2023) · Annals of Oncology · doi:10.1016/j.annonc.2023.02.012 · Cited by 79 · see citing works
Efficacy of Pemetrexed-Based Chemotherapy in Patients with ROS1 Fusion–Positive Lung Adenocarcinoma Compared with in Patients Harboring Other Driver Mutations in East Asian Populations
Chen, Y., Hsieh, M., Wu, S., Chang, Y., Yu, C., Yang, J. C., Yang, P., & Shih, J. (2016) · Journal of Thoracic Oncology · doi:10.1016/j.jtho.2016.03.022 · Cited by 79 · see citing works
Self-citation
Efficacy of Platinum/Pemetrexed Combination Chemotherapy in ALK-Positive NSCLC Refractory to Second-Generation ALK Inhibitors
Lin, J. J., Schoenfeld, A. J., Zhu, V. W., Yeap, B. Y., Chin, E. N., Rooney, M. M., Plodkowski, A. J., Digumarthy, S. R., Dagogo‐Jack, I., Gainor, J. F., et al. (2019) · Journal of Thoracic Oncology · doi:10.1016/j.jtho.2019.10.014 · Cited by 77 · see citing works
Gefitinib for advanced non-small cell lung cancer
Sim, E., Yang, I. A., Wood-Baker, R. R., Bowman, R., & Fong, K. M. (2018) · Cochrane Database of Systematic Reviews · doi:10.1002/14651858.cd006847.pub2 · Cited by 67 · see citing works
Osimertinib in Japanese patients with EGFR T790M mutation‐positive advanced non‐small‐cell lung cancer: AURA 3 trial
Akamatsu, H., Katakami, N., Okamoto, I., Kato, T., Kim, Y. H., Imamura, F., Shinkai, M., Hodge, R. A., Uchida, H., & Hida, T. (2018) · Cancer Science · doi:10.1111/cas.13623 · Cited by 66 · see citing works
Development and Validation of a Machine Learning Model to Explore Tyrosine Kinase Inhibitor Response in Patients With Stage IV EGFR Variant–Positive Non–Small Cell Lung Cancer
Song, J., Wang, L., Ng, N. N., Zhao, M., Shi, J., Wu, N., Li, W., Liu, Z., Yeom, K. W., & Tian, J. (2020) · JAMA Network Open · doi:10.1001/jamanetworkopen.2020.30442 · Cited by 68 · see citing works
First-line continual EGFR-TKI plus local ablative therapy demonstrated survival benefit in EGFR-mutant NSCLC patients with oligoprogressive disease
Xu, Q., Liu, H., Meng, S., Jiang, T., Li, X., Liang, S., Ren, S., & Zhou, C. (2019) · Journal of Cancer · doi:10.7150/jca.26494 · Cited by 68 · see citing works
The Role of Radiotherapy in Epidermal Growth Factor Receptor Mutation-positive Patients with Oligoprogression: A Matched-cohort Analysis
Chan, O. S. H., Lee, V. H.-F., Mok, T. S. K., Mo, F. K. F., Chang, A. T. Y., & Yeung, R. M. W. (2017) · Clinical Oncology · doi:10.1016/j.clon.2017.04.035 · Cited by 66 · see citing works
Self-citation
A systematic review of targeted agents for non-small cell lung cancer
Vestergaard, H. H., Christensen, M. R., & Lassen, U. (2017) · Acta Oncologica · doi:10.1080/0284186x.2017.1404634 · Cited by 66 · see citing works
“4 – [26] 2015 Phase III EGFR 133 (287) Gefitinibþ Standard chemotherapy 42 (32%) – – 5.”
The resistance mechanisms and treatment strategies for EGFR -mutant advanced non-small-cell lung cancer
Zhong, W., Zhou, Q. H., & Wu, Y.-L. L. C. (2017) · Oncotarget · doi:10.18632/oncotarget.20311 · Cited by 65 · see citing works
“, [78] Post TKI HM61713 62% 91% − − − − − −”
BackgroundSelf-citation
HERTHENA-Lung02: phase III study of patritumab deruxtecan in advanced EGFR -mutated NSCLC after a third-generation EGFR TKI
Mok, T. S. K., Janne, P. A., Nishio, M., Novello, S., Reck, M., Steuer, C. E., Wu, Y.-L., Fougeray, R., Fan, P., Meng, J., et al. (2023) · Future Oncology · doi:10.2217/fon-2023-0602 · Cited by 65 · see citing works
Self-citation
Bridging the divide: preclinical research discrepancies between triple-negative breast cancer cell lines and patient tumors
Sulaiman, A., & Wang, L. (2017) · Oncotarget · doi:10.18632/oncotarget.22916 · Cited by 63 · see citing works
Third-Generation Tyrosine Kinase Inhibitors Targeting Epidermal Growth Factor Receptor Mutations in Non-Small Cell Lung Cancer
Barnes, T. A., O'Kane, G. M., Vincent, M. D., & Leighl, N. B. (2017) · Frontiers in Oncology · doi:10.3389/fonc.2017.00113 · Cited by 61 · see citing works
Savolitinib plus osimertinib in epidermal growth factor receptor (EGFR)-mutated advanced non-small cell lung cancer with MET overexpression and/or amplification following disease progression on osimertinib: primary results from the phase II SAVANNAH study
de Marinis, F., Kim, T. M., Bonanno, L., Cheng, S., Kim, S.-W., Tiseo, M., Chu, Q. S.-C., Proto, C., Sacher, A. G., Luo, Y.-H., et al. (2025) · Annals of Oncology · doi:10.1016/j.annonc.2025.04.003 · Cited by 64 · see citing works
Self-citation
Continuous sc infusion of narcotics using a portable disposable device in patients with advanced cancer.
Bruera, E. D., Brenneis, C., Michaud, M., Chadwick, S., & MacDonald, R. N. (1987) · PubMed · Cited by 59 · see citing works
RETRACTED ARTICLE: The lncRNA RHPN1-AS1 downregulation promotes gefitinib resistance by targeting miR-299-3p/TNFSF12 pathway in NSCLC
Li, X., Zhang, X., Yang, C., Cui, S., Shen, Q., & Xu, S. (2018) · Cell Cycle · doi:10.1080/15384101.2018.1496745 · Cited by 58 · see citing works
“While the mechanism of gefitinib resistance is complex and heterogeneous [18].”
Background
Retracted
Frequency of EGFR T790M mutation and multimutational profiles of rebiopsy samples from non-small cell lung cancer developing acquired resistance to EGFR tyrosine kinase inhibitors in Japanese patients
Ko, R., Kenmotsu, H., Serizawa, M., Koh, Y., Wakuda, K., Ono, A., Taira, T., Naito, T., Murakami, H., Isaka, M., et al. (2016) · BMC Cancer · doi:10.1186/s12885-016-2902-0 · Cited by 59 · see citing works
SBRT for oligoprogressive oncogene addicted NSCLC
Basler, L., Kroeze, S. G. C., & Gückenberger, M. (2017) · Lung Cancer · doi:10.1016/j.lungcan.2017.02.007 · Cited by 59 · see citing works
Advances in the Development of Molecularly Targeted Agents in Non-Small-Cell Lung Cancer
Dolly, S. O., Collins, D. C., Sundar, R., Popat, S., & Yap, T. A. (2017) · Drugs · doi:10.1007/s40265-017-0732-2 · Cited by 57 · see citing works
“Last, accelerated disease progression on cessation of EGFR or ALK inhibitors has been reported [88, 89], raising questions such as should TKIs be continued until commencing or continuing with chemotherapy [10, 90, 91].”
Background
INSIGHT 2: a Phase II Study of Tepotinib Plus Osimertinib in MET -Amplified NSCLC and First-Line Osimertinib Resistance
Smit, E. F., Dooms, C., Raskin, J., Nadal, E., Tho, L. M., Le, X., Mazières, J., Hin, H. S., Morise, M., Zhu, V. W., et al. (2021) · Future Oncology · doi:10.2217/fon-2021-1406 · Cited by 56 · see citing works
Self-citation
The Resistance to EGFR-TKIs in Non-Small Cell Lung Cancer: From Molecular Mechanisms to Clinical Application of New Therapeutic Strategies
Laface, C., Maselli, F. M., Santoro, A. N., Iaia, M. L., Ambrogio, F., Laterza, M., Guarini, C., Santis, P. D., Perrone, M., & Fedele, P. (2023) · Pharmaceutics · doi:10.3390/pharmaceutics15061604 · Cited by 57 · see citing works
SEOM clinical guidelines for the treatment of non-small cell lung cancer (NSCLC) 2015
García‐Campelo, R., Bernabé, R., Cobo, M., Corral, J., Coves, J., Dómine, M., Nadal, E., Rodríguez‐Abreu, D., Viñolas, N., & Massutí, B. (2015) · Clinical & Translational Oncology · doi:10.1007/s12094-015-1455-z · Cited by 54 · see citing works
“• Continuing EGFR TKI in combination with platinumbased chemotherapy beyond progression has failed to demonstrate a significant benefit and should not be recommended [43].”
Background
Trastuzumab and paclitaxel in patients with EGFR mutated NSCLC that express HER2 after progression on EGFR TKI treatment
de Langen, A. J., Jebbink, M., Hashemi, S. M. S., Kuiper, J. L., de Bruin-Visser, J., Monkhorst, K., Thunnissen, E., & Smit, E. F. (2018) · British Journal of Cancer · doi:10.1038/s41416-018-0194-7 · Cited by 51 · see citing works
Deep Learning to Predict EGFR Mutation and PD-L1 Expression Status in Non-Small-Cell Lung Cancer on Computed Tomography Images
Wang, C., Xu, X., Shao, J., Zhou, K., Zhao, K., He, Y., Li, J., Guo, J., Zhang, Y., & Li, W. (2021) · Journal of Oncology · doi:10.1155/2021/5499385 · Cited by 50 · see citing works
“Tyrosine kinase inhibitors (TKIs) targeted to epidermal growth factor receptor (EGFR) could lead to extend progression-free survival (PFS) compared with conventional chemotherapy in EGFR-mutated NSCLC patients [4, 5].”
Background
Targeting the Epidermal Growth Factor Receptor with Molecular Degraders: State-of-the-Art and Future Opportunities
Maity, P., Chatterjee, J., Patil, K. T., Arora, S., Katiyar, M. K., Kumar, M., Samarbakhsh, A., Joshi, G., Bhutani, P., Chugh, M., et al. (2023) · Journal of Medicinal Chemistry · doi:10.1021/acs.jmedchem.2c01242 · Cited by 51 · see citing works
RECIST progression patterns during EGFR tyrosine kinase inhibitor treatment of advanced non-small cell lung cancer patients harboring an EGFR mutation
Yoshida, T., Yoh, K., Niho, S., Umemura, S., Matsumoto, S., Ohmatsu, H., Ohe, Y., & Goto, K. (2015) · Lung Cancer · doi:10.1016/j.lungcan.2015.09.025 · Cited by 50 · see citing works
Self-citation
Cost-effectiveness analysis of the first-line EGFR-TKIs in patients with non-small cell lung cancer harbouring EGFR mutations
Holleman, M. S., Al, M., Zaim, R., Groen, H. J. M., & Groot, C. A. U. (2019) · The European Journal of Health Economics · doi:10.1007/s10198-019-01117-3 · Cited by 51 · see citing works
Resistance mechanisms to osimertinib and emerging therapeutic strategies in nonsmall cell lung cancer
Zeng, Y., Yu, D., Tian, W., & Wu, F. (2021) · Current Opinion in Oncology · doi:10.1097/cco.0000000000000805 · Cited by 49 · see citing works
“Results from the IMMUNOTARGET registry showed a low ORR of 12% to ICIs in 125 EGFR-mutant patients with mPFS of 2.1 months [123].”
MethodInfluential
Mechanisms of resistance to irreversible epidermal growth factor receptor tyrosine kinase inhibitors and therapeutic strategies in non-small cell lung cancer
Xu, J., Wang, J., & Zhang, S. (2017) · Oncotarget · doi:10.18632/oncotarget.21164 · Cited by 48 · see citing works
“Another phase III IMPRESS study (NCT01544179) [168] evaluated whether it was beneficial for continuing gefitinib combined with chemotherapy beyond PD in the patients treated with first-line gefitinib.”
BackgroundSelf-citation
Advanced Non–Small Cell Lung Cancer: Sequencing Agents in the EGFR-Mutated/ALK-Rearranged Populations
Singhi, E. K., Horn, L., Sequist, L. V. D., Heymach, J. V., & Langer, C. J. (2019) · American Society of Clinical Oncology Educational Book · doi:10.1200/edbk_237821 · Cited by 45 · see citing works
Treatment Strategies for Non-Small Cell Lung Cancer with Common EGFR Mutations: A Review of the History of EGFR TKIs Approval and Emerging Data
Marin-Acevedo, J. A., Pellini, B., Kimbrough, E. O., Hicks, J. K., & Chiappori, A. (2023) · Cancers · doi:10.3390/cancers15030629 · Cited by 49 · see citing works
Optimal management of EGFR -mutant non-small cell lung cancer with disease progression on first-line tyrosine kinase inhibitor therapy
Liao, B.-C., Lin, C., Lee, J., & Yang, J. C. (2017) · Lung Cancer · doi:10.1016/j.lungcan.2017.05.009 · Cited by 48 · see citing works
Self-citation
Microwave ablation as local consolidative therapy for patients with extracranial oligometastatic EGFR-mutant non-small cell lung cancer without progression after first-line EGFR-TKIs treatment
Ni, Y., Ye, X., Yang, X., Huang, G., Li, W., Wang, J., Han, X., Wei, Z., & Meng, M. (2019) · Journal of Cancer Research and Clinical Oncology · doi:10.1007/s00432-019-03043-6 · Cited by 47 · see citing works
Self-citation
Metastatic EML4-ALK fusion detected by circulating DNA genotyping in an EGFR-mutated NSCLC patient and successful management by adding ALK inhibitors: a case report
Liang, W., He, Q., Chen, Y., Chuai, S., Yin, W., Wang, W., Peng, G., Zhou, C., & He, J. (2016) · BMC Cancer · doi:10.1186/s12885-016-2088-5 · Cited by 45 · see citing works
“In this case, switching to chemotherapy is suggested according to what IMPRESS trial indicated [12].”
Method
A deep learning-based system for survival benefit prediction of tyrosine kinase inhibitors and immune checkpoint inhibitors in stage IV non-small cell lung cancer patients: A multicenter, prognostic study
Deng, K., Wang, L., Liu, Y., Li, X., Hou, Q., Cao, M., Ng, N. N., Wang, H., Chen, H., Yeom, K. W., et al. (2022) · EClinicalMedicine · doi:10.1016/j.eclinm.2022.101541 · Cited by 45 · see citing works
Self-citation
Continuous targeted kinase inhibitors treatment induces upregulation of PD-L1 in resistant NSCLC
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“placebo plus chemotherapy in EGFR mutation-positive nonsmall cell lung cancer after progression on first-line gefitinib (IMPRESS) trial of patients treated with first-line gefitinib plus cisplatin/pemetrexed, no benefit was observed with continuation of gefitinib plus the doublet chemotherapy regimen at progression ve…”
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Gefitinib/Chemotherapy Versus Chemotherapy in EGFR Mutation-Positive NSCLC after Progression on First-Line Gefitinib: Impress Study Design
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Gefitinib improves outcome in patients with advanced non-small cell lung cancer compared with standard chemotherapy.
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Phase II study of gefitinib and inserted cisplatin plus docetaxel as a first-line treatment for advanced non-small cell lung cancer haboring an epidermal growth factor receptor activating mutation.
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Authors: Soria, J.-C., Wu, Y.-L., Nakagawa, K., Kim, S.-W., Yang, J.-J., Ahn, M.-J., Wang, J., Yang, J. C.-H., Lu, Y., Atagi, S., Ponce, S., Lee, D. H., Liu, Y., Yoh, K., Zhou, J.-Y., Shi, X., Webster, A., Jiang, H., & Mok, T. S. K.
Affiliations: Institut Gustave Roussy (FR)
Guangdong General Hospital (CN)
Kindai University (JP)
Asan Medical Center (KR)
National Taiwan University (TW)
Samsung Medical Center (KR)
Peking University Cancer Hospital (CN)
NHO Kinki Chuo Chest Medical Center (JP)
Hospital Universitario 12 De Octubre (ES)
First Hospital of China Medical University (CN)
National Cancer Center Hospital East (JP)
AstraZeneca (United Kingdom) (GB)
Chinese University of Hong Kong (HK)
Corresponding author: Mok, Tony S K
ORCID: Soria, Jean-Charles
Wu, Yi-Long
Nakagawa, Kazuhiko
Yang, Jin-Ji
Ahn, Myung-Ju
Wang, Jie
Yang, James Chih-Hsin
Atagi, Shinji
Ponce, Santiago
Liu, Yunpeng
Yoh, Kiyotaka
Shi, Xiaojin
Jiang, Haiyi
Mok, Tony S K
Venue: The Lancet Oncology
Publisher: Elsevier BV
Published: 2015-08
Volume: 16
Issue: 8
Pages: 990-998
ISSN: 1470-2045 (ISSN-L)
DOI: 10.1016/s1470-2045(15)00121-7
OpenAlex: W2152481222
Semantic Scholar: 8a3893572a340f3e2e3dc31440e3947d55eb0893
Cited by: 413
References: 30
Citations by year: 2026: 13 · 2025: 22 · 2024: 21 · 2023: 28 · 2022: 28 · 2021: 34 · 2020: 36 · 2019: 35 · 2018: 53 · 2017: 66 · 2016: 61 · 2015: 15
FWCI: 51.33
Type: journal article
Language: en
Open access: closed
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
www.elsevier.com/legal/tdmrep-license (tdm)
Locations: The Lancet Oncology (publishedVersion)
PubMed (publishedVersion)
Funders: AstraZeneca
Topics: Health Sciences › Medicine › Pulmonary and Respiratory Medicine › Lung Cancer Treatments and Mutations
Health Sciences › Medicine › Pulmonary and Respiratory Medicine › Lung Cancer Diagnosis and Treatment
Health Sciences › Medicine › Oncology › HER2/EGFR in Cancer Research
Keywords: gefitinib, EGFR mutation, non-small cell lung cancer, acquired resistance, EGFR tyrosine kinase inhibitors, cisplatin, pemetrexed, platinum-based chemotherapy, progression-free survival, second-line therapy, treatment safety, overall survival, quality of life, patient-reported outcomes, adverse events
MeSH terms: Pemetrexed, Gefitinib, Administration, Oral, Adult, Aged, Antineoplastic Combined Chemotherapy Protocols, Asia, Carcinoma, Non-Small-Cell Lung, Cisplatin, Drug Administration Schedule, Europe, Female, Glutamates, Guanine, Humans, Infusions, Intravenous, Lung Neoplasms, Male, Middle Aged, Mutation, Phenotype, Prospective Studies, Quinazolines, Time Factors, Biomarkers, Tumor, Proportional Hazards Models, Treatment Outcome, Disease Progression, Disease-Free Survival, Genetic Predisposition to Disease, Protein Kinase Inhibitors, Kaplan-Meier Estimate, ErbB Receptors

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Gefitinib plus chemotherapy versus placebo plus chemotherapy in EGFR-mutation-positive non-small-cell lung cancer after progression on first-line gefitinib (IMPRESS): a phase 3 randomised trial

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