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Oncology

Long-term Efficacy of Neoadjuvant Chemoradiotherapy Plus Surgery for the Treatment of Locally Advanced Esophageal Squamous Cell CarcinomaThe NEOCRTEC5010 Randomized Clinical Trial

Educational Objective
To compare the treatment efficacy of neoadjuvant chemoradiotherapy plus surgery with surgery alone for long-term survival among patients with locally advanced esophageal squamous cell carcinoma.
1 Credit CME
JAMA Surgery
Published Online: June 23, 2021
Original Investigation
Hong Yang, MD1;
Hui Liu, MD2;
Yuping Chen, MD3;
Chengchu Zhu, MD4;
Wentao Fang, MD5;
Zhentao Yu, MD6,7;
Weimin Mao, MD8;
Jiaqing Xiang, MD9;
Yongtao Han, MD10;
Zhijian Chen, MD11,12;
Haihua Yang, MD13;
Jiaming Wang, MD14;
Qingsong Pang, MD15;
Xiao Zheng, MD16;
Huanjun Yang, MD17;
Tao Li, MD18;
Xu Zhang, MD1;
Qun Li, MD2;
Geng Wang, MD3;
Baofu Chen, MD4;
Teng Mao, MD5;
Min Kong, MD4;
Xufeng Guo, MD5;
Ting Lin, MD1;
Mengzhong Liu, MD2;
Jianhua Fu, MD, PhD1
Author Affiliations
  • 1Department of Thoracic Surgery, Sun Yat-sen University Cancer Center, State Key Laboratory of Oncology in South China, Guangdong Esophageal Cancer Institute, Collaborative Innovation Center for Cancer Medicine, Guangzhou, China
  • 2Department of Radiation Oncology, Sun Yat-sen University Cancer Center, State Key Laboratory of Oncology in South China, Guangdong Esophageal Cancer Institute, Collaborative Innovation Center for Cancer Medicine, Guangzhou, China
  • 3Department of Thoracic Surgery, Cancer Hospital of Shantou University Medical College, Shantou, China
  • 4Department of Thoracic Surgery, Taizhou Hospital, Wenzhou Medical University, Linhai, China
  • 5Department of Thoracic Surgery, Shanghai Chest Hospital, Shanghai Jiaotong University, Shanghai, China
  • 6Department of Thoracic Surgery, National Cancer Center, National Clinical Research Center for Cancer, Cancer Hospital and Shenzhen Hospital, Chinese Academy of Medical Sciences and Peking Union Medical College, Shenzhen, China
  • 7Tianjin Medical University Cancer Hospital, Tianjin, China
  • 8Department of Thoracic Surgery, Zhejiang Cancer Hospital, Hangzhou, China
  • 9Department of Thoracic Surgery, Fudan University Shanghai Cancer Center, Shanghai, China
  • 10Department of Thoracic Surgery, Sichuan Cancer Hospital, Chengdu, China
  • 11Department of Radiation Oncology, Cancer Hospital of Shantou University Medical College, Shantou, China
  • 12The University of Hong Kong–Shenzhen Hospital, Shenzhen, China
  • 13Department of Radiation Oncology, Taizhou Hospital, Wenzhou Medical University, Linhai, China
  • 14Department of Radiation Oncology, Shanghai Chest Hospital, Shanghai Jiaotong University, Shanghai, China
  • 15Department of Radiation Oncology, Tianjin Medical University Cancer Hospital, Tianjin, China
  • 16Department of Radiation Oncology, Zhejiang Cancer Hospital, Hangzhou, China
  • 17Department of Radiation Oncology, Fudan University Shanghai Cancer Center, Shanghai, China
  • 18Department of Radiation Oncology, Sichuan Cancer Hospital, Chengdu, China
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Key Points

Question  Does treatment with neoadjuvant chemoradiotherapy plus surgery improve the long-term survival of patients with locally advanced esophageal squamous cell carcinoma (ESCC) compared with surgery alone?

Findings  In this randomized clinical trial of 451 patients with locally advanced ESCC, treatment with neoadjuvant chemoradiotherapy plus surgery showed significantly improved 5-year overall survival of 59.9% compared with 49.1% for surgery alone, as well as improved disease-free survival.

Meaning  In this study, long-term outcomes demonstrated a survival benefit from neoadjuvant chemoradiotherapy followed by surgery compared with surgery alone for the treatment of patients with locally advanced ESCC, indicating that this combination may be considered a standard of care in this patient population.

Abstract

Importance  The prognosis of patients with locally advanced esophageal squamous cell carcinoma (ESCC) remains poor after surgery. Neoadjuvant chemoradiotherapy (NCRT) has been shown to potentially improve survival.

Objective  To compare the treatment efficacy of NCRT plus surgery with surgery alone for long-term survival among patients with locally advanced ESCC.

Design, Setting, and Participants  The Neoadjuvant Chemoradiotherapy for Esophageal Cancer 5010 study was a multicenter open-label randomized phase 3 clinical trial that enrolled patients between June 1, 2007, and December 31, 2014. Follow-up ended on December 31, 2019. The study was conducted at 8 centers in China. A total of 451 patients aged 18 to 70 years with thoracic ESCC stage T1-4N1M0/T4N0M0 were enrolled and randomized. Data were analyzed from December 1, 2019, to June 30, 2020.

Interventions  Patients randomized to receive NCRT plus surgery (NCRT group) received preoperative chemotherapy (25 mg/m2 of vinorelbine on days 1 and 8 and 75 mg/m2 of cisplatin on day 1 or 25 mg/m2 of cisplatin on days 1 to 4) every 3 weeks for 2 cycles and concurrent radiotherapy (40.0 Gy, administered in 20 fractions of 2.0 Gy for 5 days per week) followed by surgery. Patients randomized to receive surgery alone (surgery group) underwent surgery after randomization.

Main Outcomes and Measures  The primary end point was overall survival in the intention-to-treat population. The secondary end point was disease-free survival.

Results  A total of 451 patients (mean [SD] age, 56.5 [7.0] years; 367 men [81.4%]) were randomized to the NCRT (n = 224) and surgery (n = 227) groups and were eligible for the intention-to-treat analysis. By December 31, 2019, 224 deaths had occurred. The median follow-up was 53.5 months (interquartile range, 18.2-87.4 months). Patients receiving NCRT plus surgery had prolonged overall survival compared with those receiving surgery alone (hazard ratio, 0.74; 95% CI, 0.57-0.97; P = .03), with a 5-year survival rate of 59.9% (95% CI, 52.9%-66.1%) vs 49.1% (95% CI, 42.3%-55.6%), respectively. Patients in the NCRT group compared with the surgery group also had prolonged disease-free survival (hazard ratio, 0.60; 95% CI, 0.45-0.80; P < .001), with a 5-year survival rate of 63.6% (95% CI, 56.0%-70.2%) vs 43.0% (95% CI, 36.0%-49.7%), respectively.

Conclusions and Relevance  In this randomized clinical trial, treatment with NCRT plus surgery significantly improved long-term overall survival and disease-free survival and therefore may be considered a standard of care for patients with locally advanced ESCC.

Trial Registration  ClinicalTrials.gov Identifier: NCT01216527

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CME Disclosure Statement: Unless noted, all individuals in control of content reported no relevant financial relationships. If applicable, all relevant financial relationships have been mitigated.

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Esophageal Cancer Esophageal Disease Gastroenterology Gastrointestinal Cancer Oncology Radiation Oncology Surgery Surgical Oncology Gastroenterology and Hepatology
Article Information

Accepted for Publication: March 13, 2021.

Published Online: June 23, 2021. doi:10.1001/jamasurg.2021.2373

Correction: This article was corrected on August 3, 2022, to amend data in a figure.

Corresponding Author: Jianhua Fu, MD, PhD, Department of Thoracic Surgery, Sun Yat-sen University Cancer Center, State Key Laboratory of Oncology in South China, Guangdong Esophageal Cancer Institute, Collaborative Innovation Center for Cancer Medicine, Guangzhou City, Guangdong Province 510060, China (fujh@sysucc.org.cn).

Open Access: This is an open access article distributed under the terms of the CC-BY License. © 2021 Yang H et al. JAMA Surgery.

Author Contributions: Drs Fu and M. Liu (senior coauthors) had full access to all of the data in the study and take responsibility for the integrity of the data and the accuracy of the data analysis. Drs Hong Yang, H. Liu, Y. Chen, Zhu, Fang, and Yu contributed equally and should be considered first coauthors.

Concept and design: Hong Yang, H. Liu, Zhu, Fang, Yu, Xiang, Han, Z. Chen, Zhang, Fu.

Acquisition, analysis, or interpretation of data: Hong Yang, H. Liu, Y. Chen, Fang, W. Mao, Xiang, Han, Z. Chen, Haihua Yang, J. Wang, Pang, Zheng, Huanjun Yang, T. Li, Q. Li, G. Wang, B. Chen, T. Mao, Kong, Guo, Lin, M. Liu, Fu.

Drafting of the manuscript: Hong Yang, H. Liu, Fang, Xiang, Han, Z. Chen, J. Wang, T. Mao, Lin, Fu.

Critical revision of the manuscript for important intellectual content: Hong Yang, H. Liu, Y. Chen, Zhu, Fang, Yu, W. Mao, Xiang, Han, Haihua Yang, Pang, Zheng, Huanjun Yang, T. Li, Zhang, Q. Li, G. Wang, B. Chen, Kong, Guo, M. Liu, Fu.

Statistical analysis: Hong Yang, Fang, Xiang, Han, Lin, M. Liu, Fu.

Obtained funding: Xiang, Fu.

Administrative, technical, or material support: Y. Chen, Zhu, Yu, W. Mao, Xiang, Han, Z. Chen, Haihua Yang, Huanjun Yang, T. Li, Q. Li, G. Wang, B. Chen, T. Mao, Kong, Guo, Lin, Fu.

Supervision: H. Liu, Y. Chen, Xiang, Han, Pang, Zhang, Lin, Fu.

Conflict of Interest Disclosures: None reported.

Funding/Support: This clinical trial was supported by grant 179 from the Health Ministry of China (Dr Fu), grant 2007048 from the Sun Yat-sen University Clinical Research 5010 Program (Dr Fu), grant 81272635 from the National Science Foundation of China (Dr Fu), grant 2012A030400007 from the Science and Technology Fund for Projects of Guangdong Province (Dr Fu), and grant 2011C13039-2 from the Major Science and Technology Special Fund for Projects of Zhejiang Province (Dr Zhu).

Role of the Funder/Sponsor: The funding organizations had no role in the design and conduct of the study; collection, management, analysis, and interpretation of the data; preparation, review, or approval of the manuscript; and decision to submit the manuscript for publication.

Group Information: Nonauthor investigators in the Neoadjuvant Chemoradiotherapy for Esophageal Cancer 5010 (NEOCRTEC5010) Randomized Clinical Trial Group: Yonghong Hu, MD, Qiaoqiao Li, MD, Mian Xi, MD, Liru He, MD, Bo Qiu, MD, and Shiliang Liu, MD, Department of Radiation Oncology, Sun Yat-sen University Cancer Center; Xiaodong Li, MD, Kongjia Luo, MD, Junying Chen, MD, Yihuai Hu, MD, Jiyang Chen, BS, and Caiyan Fang, MD, Department of Thoracic Surgery, Sun Yat-sen University Cancer Center; Wenfeng Ye, MD, Department of Clinical Nutrition, Sun Yat-sen University Cancer Center; Jing Wen, PhD, State Key Laboratory of Oncology in South China, Collaborative Innovation Center for Cancer Medicine; Ruiqi Wang, MD, Department of Pancreatic and Biliary Surgery, Sun Yat-sen University Cancer Center; Xuan Xie, MD, Department of Thoracic Surgery, Sun Yat-sen Memorial Hospital, Sun Yat-sen University; Fu Yang, MD, Department of Thoracic Surgery, Shanghai General Hospital; Feixiang Wang, MD, Department of Thoracic Surgery, Cancer Center of Guangzhou Medical University; Shihua Yao, MD, Department of Thoracic Surgery, Changhai Hospital; Peng Tang, MD, Zhao Ma, MD, Department of Esophageal Cancer, Tianjin Medical University Cancer Institute and Hospital; Longlong Shao, MD, Department of Thoracic Surgery, Fudan University Shanghai Cancer Center; and Lin Peng, Department of Thoracic Surgery, Sichuan Cancer Hospital and Institute.

Meeting Presentations: The results of this study were presented in part at the annual meeting of the European Society for Medical Oncology; October 8, 2016; Copenhagen, Denmark and the 25th annual meeting of the European Society of Thoracic Surgeons; May 30, 2017; Innsbruck, Austria.

Data Sharing Statement: See Supplement 3.

Additional Contributions: We thank the members of the independent data monitoring committee, Tiehua Rong, MD, Qing Liu, PhD, and Yuhong Li, MD, of the Sun Yat-sen University Cancer Center. We also thank Jibin Li, PhD, of the Sun Yat-sen University Cancer Center, for his assistance with the statistical analysis. None of the contributors received compensation.

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