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Perioperative toripalimab and chemotherapy in locally advanced gastric or gastro-esophageal junction cancer: a randomized phase 2 trial

Nature Medicine volume 30, pages 552–559 (2024)Cite this article

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Abstract

Perioperative chemotherapy is the standard treatment for locally advanced gastric or gastro-esophageal junction cancer, and the addition of programmed cell death 1 (PD-1) inhibitor is under investigation. In this randomized, open-label, phase 2 study (NEOSUMMIT-01), patients with resectable gastric or gastro-esophageal junction cancer clinically staged as cT3-4aN + M0 were randomized (1:1) to receive either three preoperative and five postoperative 3-week cycles of SOX/XELOX (chemotherapy group, n = 54) or PD-1 inhibitor toripalimab plus SOX/XELOX, followed by toripalimab monotherapy for up to 6 months (toripalimab plus chemotherapy group, n = 54). The primary endpoint was pathological complete response or near-complete response rate (tumor regression grade (TRG) 0/1). The results showed that patients in the toripalimab plus chemotherapy group achieved a higher proportion of TRG 0/1 than those in the chemotherapy group (44.4% (24 of 54, 95% confidence interval (CI): 30.9%–58.6%) versus 20.4% (11 of 54, 95% CI: 10.6%–33.5%)), and the risk difference of TRG 0/1 between toripalimab plus chemotherapy group and chemotherapy group was 22.7% (95% CI: 5.8%–39.6%; P = 0.009), meeting a prespecified endpoint. In addition, a higher pathological complete response rate (ypT0N0) was observed in the toripalimab plus chemotherapy group (22.2% (12 of 54, 95% CI: 12.0%–35.6%) versus 7.4% (4 of 54, 95% CI: 2.1%–17.9%); P = 0.030), and surgical morbidity (11.8% in the toripalimab plus chemotherapy group versus 13.5% in the chemotherapy group) and mortality (1.9% versus 0%), and treatment-related grade 3–4 adverse events (35.2% versus 29.6%) were comparable between the treatment groups. In conclusion, the addition of toripalimab to chemotherapy significantly increased the proportion of patients achieving TRG 0/1 compared to chemotherapy alone and showed a manageable safety profile. ClinicalTrials.gov registration: NCT04250948.

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Fig. 1: CONSORT diagram.
Fig. 2: Histopathological tumor regression by tumor location and Lauren’s classification.

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Data availability

All requests for data will be reviewed by the leading clinical site, Sun Yat-Sen University Cancer Center, to verify whether the request is subject to any intellectual property or confidentiality obligations. Requests for access to the patient-level data from this study can be submitted via email to wangfeng@sysucc.org.cn with detailed proposals for approval and will be responded to in two weeks. A signed data access agreement with the sponsor is required before accessing shared data.

Code availability

No custom code was used for statistical analysis in this study.

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Acknowledgements

This study is sponsored by Shanghai Junshi Biosciences. We thank the patients who participated in this study and their families. We thank S. R. Seeruttun (Sun Yat-sen University Cancer Center) for assistance in writing and revising the contents of this work. This research was supported by the National Natural Science Foundation of China (81930065, 82173128, to R.H.X.), CAMS Innovation Fund for Medical Sciences (CIFMS) (2019-I2M-5-036, to R.H.X.), International Cooperation and Exchanges National Natural Science Foundation of China (82061160373, to F.W.), Science and Technology Program of Guangzhou (202206080011, to F.W.), the Fundamental Research Funds for the Central Universities,Sun Yat-sen University (84000-31620003, to F.W.), Young Talents Program of Sun Yat-sen University Cancer Center(YTP-SYSUCC-0018, to F.W.) and Guangdong Esophageal Cancer Institute Science and Technology Program (M02210, to S.Q.Y.). The funders played no role in the study’s design, conduct or reporting.

Author information

Author notes

  1. These authors contributed equally: Shu-Qiang Yuan, Run-Cong Nie, Ying Jin, Cheng-Cai Liang, Yuan-Fang Li.

Authors and Affiliations

  1. Department of Gastric Surgery, Sun Yat-sen University Cancer Center, State Key Laboratory of Oncology in South China, Collaborative Innovation Center for Cancer Medicine, Guangzhou, P. R. China

    Shu-Qiang Yuan, Run-Cong Nie, Cheng-Cai Liang, Yuan-Fang Li, Rui Jian, Xiao-Wei Sun, Ying-Bo Chen, Hai-Bo Qiu, Wei Wang, Zhi-Min Liu, Yuan-Xiang Guan, Yong-Ming Chen & Zhi-Wei Zhou

  2. Department of Medical Oncology, Sun Yat-sen University Cancer Center, State Key Laboratory of Oncology in South China, Collaborative Innovation Center for Cancer Medicine, Sun Yat-sen University, Guangzhou, P. R. China

    Ying Jin, Wen-Long Guan, Zi-Xian Wang, Dong-Sheng Zhang, Rui-Hua Xu & Feng Wang

  3. Research Unit of Precision Diagnosis and Treatment for Gastrointestinal Cancer, Chinese Academy of Medical Sciences, Guangzhou, P. R. China

    Ying Jin, Wen-Long Guan, Zi-Xian Wang, Dong-Sheng Zhang, Rui-Hua Xu & Feng Wang

  4. Department of Gastric Surgery, The Sixth Affiliated Hospital, Sun Yat-sen University, Guangzhou, P. R. China

    Shi Chen & Jun-Sheng Peng

  5. Department of Pathology, Sun Yat-sen University Cancer Center, State Key Laboratory of Oncology in South China, Collaborative Innovation Center for Cancer Medicine, Guangzhou, P. R. China

    Yi-Hong Ling, Shao-Yan Xi & Mu-Yan Cai

  6. Department of Endoscopy, Sun Yat-sen University Cancer Center, State Key Laboratory of Oncology in South China, Collaborative Innovation Center for Cancer Medicine, Guangzhou, P. R. China

    Chun-Yu Huang

  7. Department of Medical Imaging, Sun Yat-sen University Cancer Center, State Key Laboratory of Oncology in South China, Collaborative Innovation Center for Cancer Medicine, Guangzhou, P. R. China

    Qiu-Xia Yang

  8. Department of Clinical Research, Sun Yat-Sen University Cancer Center, State Key Laboratory of Oncology in South China; Collaborative Innovation Center for Cancer Medicine, Guangzhou, P. R. China

    Ji-Bin Li

  9. Shanghai Junshi Biosciences, Shanghai, P. R. China

    Xiong-Wen Tang

  10. TopAlliance Biosciences, Rockville, MD, USA

    Xiong-Wen Tang

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  1. Shu-Qiang Yuan
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Contributions

R.-H.X., F.W., Z.-W.Z. and S.-Q.Y. conceived and designed the study. S.-Q.Y., R.-C.N., Y.J., C.-C.L., Y.-F.L., R.J., X.-W.S., Y.-B.C., W.-L.G., Z.-X.W., H.-B.Q., W.W., S.C., D.-S.Z., Y.-H.L., S.-Y.X., M.-Y.C., C.-Y.H., Q.-X.Y., Z.-M.L., Y.-X.G., Y.-M.C., J.-B.L., X.-W.T., J.-S.P., Z.-W.Z., F.W. and R.-H.X. conducted the provision of study materials and patients. R.-H.X., F.W., Z.-W.Z., S.-Q.Y. and R.-C.N. carried out data analysis and interpretation. All authors were involved in writing the manuscript and final approval.

Corresponding authors

Correspondence to Zhi-Wei Zhou, Rui-Hua Xu or Feng Wang.

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Extended data

Extended Data Table 1 Histopathological tumor regression according to chemotherapy regimen in the intention-to-treat population
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Extended Data Table 2 Histopathological tumor regression according to tumor location in the intention-to-treat population
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Extended Data Table 3 Histopathological tumor regression according to Lauren’s classification in the intention-to-treat population
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Extended Data Table 4 Histopathological tumor regression according to PD-L1 expression
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Extended Data Table 5 Histopathological tumor regression according to MMR status
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Extended Data Table 6 Summary of serious adverse events with perioperative morbidity
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Extended Data Table 7 Adverse events during preoperative treatment
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Extended Data Table 8 Adverse events during postoperative treatment
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Extended Data Table 9 Dose reduction in the intention-to-treat population
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Extended Data Table 10 Treatment discontinuation caused by treatment-related adverse events in the intention-to-treat population
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Yuan, SQ., Nie, RC., Jin, Y. et al. Perioperative toripalimab and chemotherapy in locally advanced gastric or gastro-esophageal junction cancer: a randomized phase 2 trial. Nat Med 30, 552–559 (2024). https://doi.org/10.1038/s41591-023-02721-w

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