Erlotinib versus chemotherapy as first-line treatment for patients with advanced EGFR mutation-positive non-small-cell lung cancer (OPTIMAL, CTONG-0802): a multicentre, open-label, randomised, phase 3 study

Zhou, Caicun; Wu, Yi-Long; Chen, Gongyan; Feng, Jifeng; Liu, Xiao-Qing; Wang, Changli; Zhang, Shucai; Wang, Jie; Zhou, Songwen; Ren, Shengxiang; Lu, Shun; Zhang, Li; Hu, Chengping; Hu, Chunhong; Luo, Yi; Chen, Lei; Ye, Ming; Huang, Jianan; Zhi, Xiuyi; Zhang, Yiping; Xiu, Qingyu; Ma, Jun; Zhang, Li; You, Changxuan

doi:10.1016/s1470-2045(11)70184-x

Cited by 4,081Lung Cancer Treatments and MutationsLung Cancer Diagnosis and TreatmentLung Cancer Research Studies

Erlotinib versus chemotherapy as first-line treatment for patients with advanced EGFR mutation-positive non-small-cell lung cancer (OPTIMAL, CTONG-0802): a multicentre, open-label, randomised, phase 3 study

Zhou, Caicun, Wu, Yi-Long, Chen, Gongyan, Feng, Jifeng, Liu, Xiao-Qing, Wang, Changli, Zhang, Shucai, Wang, Jie +16 more·2011·The Lancet Oncology

DOI 10.1016/s1470-2045(11)70184-x

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Abstract

Background Activating mutations in EGFR are important markers of response to tyrosine kinase inhibitor (TKI) therapy in non-small-cell lung cancer (NSCLC). The OPTIMAL study compared efficacy and tolerability of the TKI erlotinib versus standard chemotherapy in the first-line treatment of patients with advanced EGFR mutation-positive NSCLC.Methods We undertook an open-label, randomised, phase 3 trial at 22 centres in China. Patients older than 18 years with histologically confirmed stage IIIB or IV NSCLC and a confirmed activating mutation of EGFR (exon 19 deletion or exon 21 L858R point mutation) received either oral erlotinib (150 mg/day) until disease progression or unacceptable toxic effects, or up to four cycles of gemcitabine plus carboplatin. Patients were randomly assigned (1:1) with a minimisation procedure and were stratified according to EGFR mutation type, histological subtype (adenocarcinoma vs non-adenocarcinoma), and smoking status. The primary outcome was progression-free survival, analysed in patients with confirmed disease who received at least one dose of study treatment. The trial is registered at ClinicalTrials.gov, number NCT00874419, and has completed enrolment; patients are still in follow-up.Findings 83 patients were randomly assigned to receive erlotinib and 82 to receive gemcitabine plus carboplatin; 82 in the erlotinib group and 72 in the chemotherapy group were included in analysis of the primary endpoint. Median progression-free survival was significantly longer in erlotinib-treated patients than in those on chemotherapy (13.1 [95% CI 10.58-16.53] vs 4.6 [4.21-5.42] months; hazard ratio 0.16, 95% CI 0.10-0.26; p<0.0001). Chemotherapy was associated with more grade 3 or 4 toxic effects than was erlotinib (including neutropenia in 30 [42%] of 72 patients and thrombocytopenia in 29 [40%] patients on chemotherapy vs no patients with either event on erlotinib); the most common grade 3 or 4 toxic effects with erlotinib were increased alanine aminotransferase concentrations (three [4%] of 83 patients) and skin rash (two [2%] patients). Chemotherapy was also associated with increased treatment-related serious adverse events (ten [14%] of 72 patients [decreased platelet count, n=8; decreased neutrophil count, n=1; hepatic dysfunction, n=1] vs two [2%] of 83 patients [both hepatic dysfunction]).Interpretation Compared with standard chemotherapy, erlotinib conferred a significant progression-free survival benefit in patients with advanced EGFR mutation-positive NSCLC and was associated with more favourable tolerability. These findings suggest that erlotinib is important for first-line treatment of patients with advanced EGFR mutation-positive NSCLC.Funding F Hoffmann-La Roche Ltd (China); Science and Technology Commission of Shanghai Municipality.

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First-generation EGFR TKIs gefitinib and erlotinib have shown improved efficacy and tolerability compared with chemotherapy in phase III trials.
“have shown improved efficacy and tolerability compared with chemotherapy in numerous phase III trials”
From Afatinib for the treatment of EGFR mutation-positive NSCLC: A review of clinical findings (2020) · cites this paper as [34]
Eight randomised controlled phase III trials have demonstrated that first-generation or second-generation EGFR-TKIs represent the best first-line treatment option in patients with advanced NSCLC whose tumours harbour EGFR mutations, when compared with chemotherapy, because they significantly improved the RR and PFS.
“Eight randomised controlled phase III trials (table 1) have demonstrated that first-generation or second-generation EGFR-TKIs represent the best first-line treatment option in patients with advanced NSCLC whose tumours harbour EGFR mutations, when compared with chemotherapy, because they significantly improved the RR and progression-free survival (PFS).4–11”
From Mechanisms of resistance to EGFR-targeted drugs: lung cancer (2016) · cites this paper as [7]
Patients with EGFR-mutant NSCLC usually respond to first-generation TKIs but most progress after about 9-14 months.
“Unfortunately, whilst patients with EGFRm+ tumors typically show good initial responses to first generation TKIs, most patients who respond to therapy ultimately develop disease progression after about 9-14 months of treatment (7-11).”
From AZD9291, an Irreversible EGFR TKI, Overcomes T790M-Mediated Resistance to EGFR Inhibitors in Lung Cancer (2014) · cites this paper as [11]
In first-line targeted therapy trials for oncogene-addicted NSCLC, objective response rates typically range from 50% to 83%, complete responses are rare, and some patients show de novo resistance.
“Across clinical trials of first-line targeted therapy for oncogene-addicted subgroups of NSCLC, rates of objective response [G] typically range between 50% and 83% and complete responses [G] are rare; in addition, some patients exhibit de novo resistance16–26, 28–32, 35.”
From Co-occurring genomic alterations in non-small-cell lung cancer biology and therapy (2019) · cites this paper as [17]
Duration of response, progression-free survival, and overall survival are even more variable across these trials.
“Even more variable are duration of response to targeted therapy, progression-free survival and overall survival16–26, 28–32, 35.”
From Co-occurring genomic alterations in non-small-cell lung cancer biology and therapy (2019) · cites this paper as [17]

The current diagnostic approach of testing only for common exon 19 and 21 mutations, as done in EURTAC or OPTIMAL, might miss identifying a number of patients who could have some benefit from EGFR TKI treatment.
“One potential limitation of the current diagnostic approach of testing only for common exon 19 and 21 mutations, as was done in the EURTAC or OPTIMAL studies, 4,5 is that such an approach might miss identifying a number of patients who could have some benefit from EGFR TKI treatment.”
From Examining Treatment Outcomes with Erlotinib in Patients with Advanced Non–Small Cell Lung Cancer Whose Tumors Harbor Uncommon EGFR Mutations (2016) · cites this paper as [4]
Most patients with exon 19 deletions or L858R have radiographic responses to gefitinib, erlotinib, and afatinib.
“Most patients whose tumors harbor exon 19 deletions or L858R EGFR activating mutations have radiographic responses to monotherapy with the reversible adenosine triphosphate (ATP)-competitive EGFR tyrosine kinase inhibitors (TKIs) gefitinib and erlotinib 17–23 and the irreversible EGFR TKI afatinib 24.”
From Structural, Biochemical, and Clinical Characterization of Epidermal Growth Factor Receptor (EGFR) Exon 20 Insertion Mutations in Lung Cancer (2013) · cites this paper as [23]
Randomized trials show that EGFR TKIs improve response rate and progression-free survival compared with chemotherapy as initial systemic therapy for advanced EGFR-mutant NSCLC.
“Several randomized clinical trials have demonstrated that EGFR TKIs are more effective, as measured by response rate (RR) and progression free survival (PFS), than chemotherapy when used as initial systemic treatment for advanced EGFR mutant NSCLC (1, 4–9).”
From EGFR Mutations and Resistance to Irreversible Pyrimidine-Based EGFR Inhibitors (2015) · cites this paper as [8]
The extension of approval of Erlotinib for patients harboring EGFR mutations was obtained after two large phase III trials conducted in Asia and Europe provided definitive demonstration of superiority of an EGFR TKI over standard first-line chemotherapy in molecularly selected patients.
“The extension of approval of Erlotinib for patients harboring EGFR mutations, in addition to the previous indication for unselected patients with NSCLC after at least one chemotherapeutic line, was obtained after the publication of two large phase III trials conducted in Asia [65] and Europe [66], providing the definitive demonstration of superiority of an EGFR TKI over standard first-line”
From A decade of EGFR inhibition in EGFR-mutated non small cell lung cancer (NSCLC): Old successes and future perspectives (2015) · cites this paper as [65]
Targeted therapies for EGFR-mutant lung cancers were established based on 7 phase III randomized trials.
“Targeted therapies for these lung cancers were established based on 7 phase III randomized trials.5, 6, 7, 8, 9, 10, 11”
From Not all epidermal growth factor receptor mutations in lung cancer are created equal: Perspectives for individualized treatment strategy (2016) · cites this paper as [7]
In prospective trials of common EGFR mutations, gefitinib, erlotinib and afatinib showed objective response rates of approximately 60% and progression-free survival of 9-13 months.
“Evidence of these common mutations has been developed in prospective trials: gefitinib, erlotinib and afatinib showed ORR of approximately 60% and PFS of 9–13 months.5, 6, 7, 8, 9, 10, 11”
From Not all epidermal growth factor receptor mutations in lung cancer are created equal: Perspectives for individualized treatment strategy (2016) · cites this paper as [7]
Since the publication of the ASCO 2009 guideline and the ASCO EGFR provisional clinical opinion, results from seven trials of first-line EGFR TKIs for patients with EGFR mutations have been published.
“Since the publication of the ASCO 2009 guideline and the ASCO EGFR provisional clinical opinion,59 results from seven trials of first-line EGFR TKIs for patients with EGFR mutations have been published.11,13,29,31,34,36,40”
From Systemic Therapy for Stage IV Non–Small-Cell Lung Cancer: American Society of Clinical Oncology Clinical Practice Guideline Update (2015) · cites this paper as [13]
In a second small study comparing first-line erlotinib with chemotherapy, there was a longer PFS (erlotinib: 13.7 months; 95% CI, 10.6 to 15.3; control: 4.6 months; 95% CI, 4.2 to 5.4; HR, 0.164; 95% CI, 0.11 to 0.26; P < .001).
“In the second small study, which was a publication of an abstract in the provisional clinical opinion, there was a longer PFS (erlotinib: 13.7 months; 95% CI, 10.6 to 15.3; control: 4.6 months; 95% CI, 4.2 to 5.4; HR, 0.164; 95% CI, 0.11 to 0.26; P < .001); OS had not yet been reached.13,14”
From Systemic Therapy for Stage IV Non–Small-Cell Lung Cancer: American Society of Clinical Oncology Clinical Practice Guideline Update (2015) · cites this paper as [13]
Final results of OS have not been reported for most studies of first-line EGFR TKI versus cytotoxic chemotherapy in EGFR-mutant patients, so outcomes of patients who crossed over to chemotherapy have not been analyzed.
“However, final results of OS have not been reported for most studies; therefore, the outcomes of those patients who crossed over to chemotherapy have not been yet analyzed.11,13,20,29,94”
From Systemic Therapy for Stage IV Non–Small-Cell Lung Cancer: American Society of Clinical Oncology Clinical Practice Guideline Update (2015) · cites this paper as [13]
Other studies have randomly assigned patients with EGFR mutations to a first-line EGFR TKI or cytotoxic chemotherapy and found that PFS was improved in those who received the EGFR TKI.
“Other studies have randomly assigned patients with EGFR mutations to a first-line EGFR TKI or cytotoxic chemotherapy and found that PFS was improved in those who received the EGFR TKI.”
From Systemic Therapy for Stage IV Non–Small-Cell Lung Cancer: American Society of Clinical Oncology Clinical Practice Guideline Update (2015) · cites this paper as [13]

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Background
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“The objective response rates to these agents in randomized clinical trials range from 56-74%, and the median time to progression is 9-13 months (5,6,7).”
Background

Authors: Zhou, C., Wu, Y.-L., Chen, G., Feng, J., Liu, X.-Q., Wang, C., Zhang, S., Wang, J., Zhou, S., Ren, S., Lu, S., Zhang, L., Hu, C., Hu, C., Luo, Y., Chen, L., Ye, M., Huang, J., Zhi, X., Zhang, Y., Xiu, Q., Ma, J., Zhang, L., & You, C.
Affiliations: Tongji University (CN)
Guangdong General Hospital (CN)
Harbin Medical University (CN)
Jiangsu Cancer Hospital (CN)
Academy of Military Medical Sciences (CN)
Tianjin Medical University Cancer Institute and Hospital (CN)
Capital Medical University (CN)
Peking University Cancer Hospital (CN)
Central South University (CN)
Hunan Cancer Hospital (CN)
Cancer Hospital of Shantou University Medical College (CN)
Shanghai Jiao Tong University (CN)
First Affiliated Hospital of Soochow University (CN)
Zhejiang Cancer Hospital (CN)
Second Military Medical University (CN)
Nanfang Hospital (CN)
Corresponding author: Zhou, Caicun
ORCID: Zhou, Caicun
Wu, Yi-Long
Chen, Gongyan
Feng, Jifeng
Wang, Changli
Zhang, Shucai
Wang, Jie
Zhou, Songwen
Ren, Shengxiang
Hu, Chengping
Hu, Chunhong
Luo, Yi
Ye, Ming
Huang, Jianan
Zhang, Yiping
Ma, Jun
You, Changxuan
Venue: The Lancet Oncology
Publisher: Elsevier BV
Published: 2011-08
Volume: 12
Issue: 8
Pages: 735-742
ISSN: 1470-2045 (ISSN-L)
DOI: 10.1016/s1470-2045(11)70184-x
OpenAlex: W2160982674
Cited by: 4,081
References: 1
Citations by year: 2026: 56 · 2025: 116 · 2024: 143 · 2023: 198 · 2022: 238 · 2021: 301 · 2020: 272 · 2019: 310 · 2018: 360 · 2017: 383 · 2016: 364 · 2015: 412 · 2014: 351 · 2013: 325 · 2012: 218
FWCI: 250.56
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)
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 › Lung Cancer Research Studies
Keywords: erlotinib, EGFR-mutant non-small cell lung cancer, tyrosine kinase inhibitors, first-line therapy, progression-free survival, exon 19 deletion, L858R mutation, chemotherapy toxicity, OPTIMAL trial, Chinese patients, adenocarcinoma
MeSH terms: Erlotinib Hydrochloride, Gemcitabine, Administration, Oral, Adult, Aged, Antineoplastic Combined Chemotherapy Protocols, Carcinoma, Non-Small-Cell Lung, China, Deoxycytidine, Female, Humans, Lung Neoplasms, Male, Middle Aged, Mutation, Neoplasm Staging, Quinazolines, Carboplatin, Gene Deletion, Disease-Free Survival, Protein Kinase Inhibitors, ErbB Receptors

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Erlotinib versus chemotherapy as first-line treatment for patients with advanced EGFR mutation-positive non-small-cell lung cancer (OPTIMAL, CTONG-0802): a multicentre, open-label, randomised, phase 3 study

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