LBA6_PR Nivolumab (nivo) plus chemotherapy (chemo) versus chemo as first-line (1L) treatment for advanced gastric cancer/gastroesophageal junction cancer (GC/GEJC)/esophageal adenocarcinoma (EAC): First results of the CheckMate 649 study

Moehler, M.; Shitara, K.; Garrido, M.; Salman, P.; Shen, L.; Wyrwicz, L.; Yamaguchi, K.; Skoczylas, T.; Campos Bragagnoli, A.; Liu, T.; Schenker, M.; Yanez, P.; Tehfe, M.; Poulart, V.; Cullen, D.; Lei, M.; Kondo, K.; Li, M.; Ajani, J.A.; Janjigian, Y.Y.

doi:10.1016/j.annonc.2020.08.2296

Cited by 208Gastric Cancer Management and OutcomesCancer Immunotherapy and BiomarkersEsophageal Cancer Research and Treatment

LBA6_PR Nivolumab (nivo) plus chemotherapy (chemo) versus chemo as first-line (1L) treatment for advanced gastric cancer/gastroesophageal junction cancer (GC/GEJC)/esophageal adenocarcinoma (EAC): First results of the CheckMate 649 study

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Moehler, M., Shitara, K., Garrido, M., Salman, P., Shen, L., Wyrwicz, L., Yamaguchi, K., Skoczylas, T. +12 more·2020·Annals of Oncology

DOI 10.1016/j.annonc.2020.08.2296

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The FDA rarely approves chemoimmunotherapeutic strategies with other α-PD-1 drugs, except for nivolumab combined with chemotherapy for gastric cancer and GEJC.
“The FDA rarely approves chemoimmunotherapeutic strategies with other α-PD-1 drugs (except for nivolumab combined with chemotherapy for gastric cancer and GEJC) [58].”
From Combination strategies with PD-1/PD-L1 blockade: current advances and future directions (2022) · cites this paper as [58]

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Bordry, N., Astaras, C., Ongaro, M., Goossens, N., Frossard, J., & Koessler, T. (2021) · World Journal of Gastroenterology · doi:10.3748/wjg.v27.i28.4493 · Cited by 28 · see citing works
Immune Checkpoint Inhibition in Oesophago-Gastric Carcinoma
Högner, A., & Thuss-Patience, P. C. (2021) · Pharmaceuticals · doi:10.3390/ph14020151 · Cited by 27 · see citing works
“[22] Checkmate-649 III Nivo + XELOX/ FOLFOX vs.”
Perioperative treatment in resectable gastric cancer with spartalizumab in combination with fluorouracil, leucovorin, oxaliplatin and docetaxel (FLOT): a phase II study (GASPAR)
Santos, M. D., Lequesne, J., Leconte, A., Corbinais, S., Parzy, A., Guilloit, J., Varatharajah, S., Brachet, P.-E., Dorbeau, M., Vaur, D., et al. (2022) · BMC Cancer · doi:10.1186/s12885-022-09623-z · Cited by 27 · see citing works
“The CheckMate 649 trial recently showed that nivolumab and chemotherapy versus chemotherapy alone improved OS and progression-free survival (PFS) as first-line treatment in patients with non-HER-2-positive advanced gastric, GEJ or oesophageal cancer [15].”
Method
Targeted and immunotherapy in the era of personalised gastric cancer treatment
Catanese, S., & Lordick, F. (2021) · Best Practice & Research Clinical Gastroenterology · doi:10.1016/j.bpg.2021.101738 · Cited by 26 · see citing works
Claudin 18.2—a FAST-moving target in gastric cancer?
Athauda, A., & Chau, I. (2021) · Annals of Oncology · doi:10.1016/j.annonc.2021.02.021 · Cited by 26 · see citing works
Outcomes on anti‐VEGFR ‐2/paclitaxel treatment after progression on immune checkpoint inhibition in patients with metastatic gastroesophageal adenocarcinoma
Fonkoua, L. A. K., Chakrabarti, S., Sonbol, M. B., et al. (2021) · International Journal of Cancer · doi:10.1002/ijc.33559 · Cited by 26 · see citing works
“Moving forward, understanding the impact of prior ICI may have more relevance given that more patients will receive upfront ICI in this disease.(24,25)”
Background
Distinct genomic landscapes of gastroesophageal adenocarcinoma depending on PD-L1 expression identify mutations in RAS–MAPK pathway and TP53 as potential predictors of immunotherapy efficacy
Wang, J., Xiu, J., Baca, Y., Arai, H., Battaglin, F., Kawanishi, N. K., Soni, S., Zhang, W., Millstein, J., Shields, A. F., et al. (2021) · Annals of Oncology · doi:10.1016/j.annonc.2021.03.203 · Cited by 27 · see citing works
Self-citation
Immunotherapy Predictive Molecular Markers in Advanced Gastroesophageal Cancer: MSI and Beyond
Park, R., da Silva, L. L., & Saeed, A. (2021) · Cancers · doi:10.3390/cancers13071715 · Cited by 26 · see citing works
“The PD-L1 CPS is the most common method to assess PD-L1 expression in gastric cancers [6,18,33,50].”
BackgroundMethodResultInfluential
Advances in the treatment of gastric cancer: 2020–2021
Ilson, D. H. (2021) · Current Opinion in Gastroenterology · doi:10.1097/mog.0000000000000776 · Cited by 26 · see citing works
Association of inflammatory markers with survival in patients with advanced gastric cancer treated with immune checkpoint inhibitors combined with chemotherapy as first line treatment
Wan, M., Ding, Y., Mao, C., Ma, X., Li, N., Cheng, X., Qian, J., Jiang, H., Zheng, Y., Wu, L., et al. (2022) · Frontiers in Oncology · doi:10.3389/fonc.2022.1029960 · Cited by 26 · see citing works
T cells, B cells, and PD-L1 expression in esophageal and gastric adenocarcinoma before and after neoadjuvant chemotherapy: relationship with histopathological response and survival
Svensson, M. C., Lindén, A., Nygaard, J., et al. (2021) · OncoImmunology · doi:10.1080/2162402x.2021.1921443 · Cited by 26 · see citing works
Clinical relevance of PD-1 positive CD8 T-cells in gastric cancer
Choo, J. R. E., Kua, L. F., Soe, M. Y., et al. (2023) · Gastric Cancer · doi:10.1007/s10120-023-01364-7 · Cited by 25 · see citing works
Immunotherapy in Gastroesophageal Cancers: Current Evidence and Ongoing Trials
Huynh, J. C., Patel, K. G., Gong, J., Cho, M. T., Malla, M., Parikh, A. R., & Klempner, S. J. (2021) · Current Treatment Options in Oncology · doi:10.1007/s11864-021-00893-6 · Cited by 21 · see citing works
Molecular Landscapes of Gastric Pre-Neoplastic and Pre-Invasive Lesions
Businello, G., Angerilli, V., Parente, P., et al. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22189950 · Cited by 23 · see citing works
“PD-1/PD-L1 Nivolumab (CHECKMATE-649 [29]) (ATTRACTION-4 [30]) (ATTRACTION-2 [31]) First line First line Third or later line”
Background
Pazopanib with 5‐FU and oxaliplatin as first line therapy in advanced gastric cancer: A randomized phase‐II study—The PaFLO trial. A study of the Arbeitsgemeinschaft Internistische Onkologie AIO‐STO ‐0510
Högner, A., Al‐Batran, S., Siveke, J. T., et al. (2021) · International Journal of Cancer · doi:10.1002/ijc.33864 · Cited by 21 · see citing works
Current Progress on Predictive Biomarkers for Response to Immune Checkpoint Inhibitors in Gastric Cancer: How to Maximize the Immunotherapeutic Benefit?
Liu, Y., Hu, P., Xu, L., et al. (2023) · Cancers · doi:10.3390/cancers15082273 · Cited by 21 · see citing works
“This correlation was also confirmed by the Checkmate-649 study [30,38,39].”
Result
A Signature-Based Classification of Gastric Cancer That Stratifies Tumor Immunity and Predicts Responses to PD-1 Inhibitors
Li, S., Gao, J., Xu, Q., Zhang, X., Huang, M., Dai, X., Huang, K., & Liu, L. (2021) · Frontiers in Immunology · doi:10.3389/fimmu.2021.693314 · Cited by 21 · see citing works
miRNA-Based Therapeutics in the Era of Immune-Checkpoint Inhibitors
Huemer, F., Leisch, M., Geisberger, R., Zaborsky, N., & Greil, R. (2021) · Pharmaceuticals · doi:10.3390/ph14020089 · Cited by 20 · see citing works
“data from the Checkmate-649 study [58] as well as the Keynote-590 study [59] demonstrated”
Method
An Investigator-Initiated Phase 2 Study of Nivolumab Plus Low-Dose Ipilimumab as First-Line Therapy for Microsatellite Instability—High Advanced Gastric or Esophagogastric Junction Cancer (NO LIMIT, WJOG13320G/CA209-7W7)
Kawakami, H., Hironaka, S., Esaki, T., Chayama, K., Tsuda, M., Sugimoto, N., Kadowaki, S., Makiyama, A., Machida, N., Hirano, H., et al. (2021) · Cancers · doi:10.3390/cancers13040805 · Cited by 20 · see citing works
“A global phase 3 trial (CheckMate-649) recently found that the combination of nivolumab and chemotherapy (FOLFOX or capecitabine plus oxaliplatin) conferred a significant survival benefit in previously untreated patients with advanced GC in a manner dependent on PD-L1 expression level [37].”
Background
The predictive value of tumor mutation burden on survival of gastric cancer patients treated with immune checkpoint inhibitors: A systematic review and meta-analysis
Ke, L., Su, L., & Huang, D. (2023) · International Immunopharmacology · doi:10.1016/j.intimp.2023.110986 · Cited by 21 · see citing works
Multimodal radiopathomics signature for prediction of response to immunotherapy-based combination therapy in gastric cancer using interpretable machine learning
Huang, W., Wang, X., Zhong, R., Li, Z., Zhou, K., Lyu, Q., Han, J., Chen, T., Islam, M. T., Yuan, Q., et al. (2025) · Cancer Letters · doi:10.1016/j.canlet.2025.217930 · Cited by 20 · see citing works
Self-citation
Patterns of recurrence following definitive chemoradiation for patients with proximal esophageal cancer
de Vos‐Geelen, J., Geurts, S. M. E., Nieuwenhuijzen, G. A. P., et al. (2021) · European Journal of Surgical Oncology · doi:10.1016/j.ejso.2021.02.001 · Cited by 19 · see citing works
Claudin-9 (CLDN9) promotes gastric cancer progression by enhancing the glycolysis pathway and facilitating PD-L1 lactylation to suppress CD8+ T cell anti-tumor immunity
Hu, X., Ouyang, W., Chen, H., Liu, Z., Lai, Z., & Yao, H. (2024) · Cancer Pathogenesis and Therapy · doi:10.1016/j.cpt.2024.09.006 · Cited by 20 · see citing works
CACA guidelines for holistic integrative management of gastric cancer
Society of Gastric Cancer of China Anti-Cancer Association (2022) · Holistic Integrative Oncology · doi:10.1007/s44178-022-00004-x · Cited by 19 · see citing works
Bone Metastases from Gastric Cancer: What We Know and How to Deal with Them
Petrillo, A., Giunta, E. F., Pappalardo, A., et al. (2021) · Journal of Clinical Medicine · doi:10.3390/jcm10081777 · Cited by 18 · see citing works
“CHECKMATE 649, 2020 [6] III First line 1581 NR (only abstract available) NR (only abstract available) Folfox/Xelox± nivolumab; PD-1 NR (only abstract available)”
Background
Tumor-Specific and Tumor-Agnostic Molecular Signatures Associated With Response to Immune Checkpoint Inhibitors
Schlauch, D., Fu, X., Jones, S. F., Burris, H. A., Spigel, D. R., Reeves, J. A., & McKenzie, A. J. (2021) · JCO Precision Oncology · doi:10.1200/po.21.00008 · Cited by 18 · see citing works
“Although our data cannot be directly compared with previously published CPI response data (our data are line of therapy and agent-agnostic, are from a standard-of-care patient population, and span various histologies), the TTF and OS rates fall within the general range of what has been previously published (Fig 2D).(2…”
Result
Radiation and Immunotherapy in Upper Gastrointestinal Cancers: The Current State of Play
Donlon, N. E., Power, R. F., Hayes, C., Davern, M., Reynolds, J. V., & Lysaght, J. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22031071 · Cited by 15 · see citing works
“0001) to first line chemotherapy in metastatic UGI cancers can prolong overall survival [55,56].”
Background
PRODIGE 59-DURIGAST trial: A randomised phase II study evaluating FOLFIRI + Durvalumab ± Tremelimumab in second-line of patients with advanced gastric cancer
Evrard, C., Louvet, C., Hajbi, F. E., et al. (2021) · Digestive and Liver Disease · doi:10.1016/j.dld.2020.11.036 · Cited by 16 · see citing works
Construction of a nomogram to predict the survival of metastatic gastric cancer patients that received immunotherapy
Gou, M., Qian, N., Zhang, Y., Wei, L., Fan, Q., Wang, Z., & Dai, G. (2022) · Frontiers in Immunology · doi:10.3389/fimmu.2022.950868 · Cited by 15 · see citing works
“The outcomes of CheckMate 649 (26) and ATTRACTION-4 (27) paved the way for immunotherapy for MGC patients, especially with PD-L1 CPS ≥5.”
Background
Progress and Prospects of Immune Checkpoint Inhibitors in Advanced Gastric Cancer
Zeng, Z., Yang, B., & Liao, Z. (2021) · Future Oncology · doi:10.2217/fon-2020-0829 · Cited by 16 · see citing works
Nivolumab for the treatment of esophageal cancer
Mikuni, H., Yamamoto, S., & Kato, K. (2021) · Expert Opinion on Biological Therapy · doi:10.1080/14712598.2021.1904887 · Cited by 16 · see citing works
First-in-Human Phase 1 Study of a B Cell– and Monocyte-Based Immunotherapeutic Vaccine against HER2-Positive Advanced Gastric Cancer
Jung, M., Lee, J. B., Kim, H. S., et al. (2023) · Cancer Research and Treatment · doi:10.4143/crt.2022.1328 · Cited by 15 · see citing works
“first-line treatment in HER2-negative gastric cancer patients showed promising results with overall survival (OS) benefits [9].”
Background
Advances in Systemic Therapy for Gastric Cancer
Hsu, A., & Raufi, A. G. (2021) · Gastrointestinal Endoscopy Clinics of North America · doi:10.1016/j.giec.2021.03.009 · Cited by 15 · see citing works
PD-1 inhibition in patient derived tissue cultures of human gastric and gastroesophageal adenocarcinoma
Hußtegge, M., Hoang, N. A., Rebstock, J., Monecke, A., Gockel, I., Weimann, A., Schumacher, G., Bechmann, I., Lordick, F., Kallendrusch, S., et al. (2021) · OncoImmunology · doi:10.1080/2162402x.2021.1960729 · Cited by 15 · see citing works
The Efficacy and Safety of Sintilimab Combined With Nab-Paclitaxel as a Second-Line Treatment for Advanced or Metastatic Gastric Cancer and Gastroesophageal Junction Cancer
Wang, J., He, Y., Zhang, B., Lv, H., Nie, C., Chen, B., Xu, W., Zhao, J., Cheng, X., Li, Q., et al. (2022) · Frontiers in Oncology · doi:10.3389/fonc.2022.924149 · Cited by 15 · see citing works
PD-L1 testing in advanced gastric cancer—what physicians who treat this disease must know—a literature review
Peixoto, R. D., Mathias-Machado, M. C., Jacome, A. A. D. A., et al. (2023) · Journal of Gastrointestinal Oncology · doi:10.21037/jgo-22-1133 · Cited by 15 · see citing works
“Considering the clinical trials which have addressed the efficacy of ICIs, PD-L1 expression emerges as a predictive biomarker of clinical benefit, despite some limitations (2,6,8,50,91-97) ( Table 2 ).”
Distribution of tumor-infiltrating-T-lymphocytes and possible tumor-escape mechanisms avoiding immune cell attack in locally advanced adenocarcinomas of the esophagus
Schoemmel, M., Loeser, H., Kraemer, M., et al. (2021) · Clinical & Translational Oncology · doi:10.1007/s12094-021-02556-2 · Cited by 14 · see citing works
Patient and Caregiver Socioeconomic Burden of First-Line Systemic Therapy for Advanced Gastroesophageal Adenocarcinoma
Xiao, H., Bertwistle, D., Khela, K., Middleton‐Dalby, C., & Hall, J. (2022) · Future Oncology · doi:10.2217/fon-2021-1449 · Cited by 13 · see citing works
Comparative Efficacy and Safety of Programmed Death-1 Pathway Inhibitors in Advanced Gastroesophageal Cancers: A Systematic Review and Network Meta-Analysis of Phase III Clinical Trials
da Silva, L. L., Aguiar, P. N., Park, R., Saul, E. E., Haaland, B. A., & Lopes, G. D. L., Jr. (2021) · Cancers · doi:10.3390/cancers13112614 · Cited by 13 · see citing works
“CheckMate 649 (Moehler, 2020 [18]) NA nivolumab 360 mg Q3W or 240 mg Q2W (789) XELOX Q3W or FOLFOX Q2W (792) NA Cancers 2021, 13, x FOR PEER REVIEW 5 of 14”
BackgroundResult
Gemcitabine Plus Nab-Paclitaxel Induces PD-L1 mRNA Expression in Plasma-Derived Microvesicles in Pancreatic Cancer
Re, M. D., Vivaldi, C., Rofi, E., Salani, F., Crucitta, S., Catanese, S., Fontanelli, L., Massa, V., Cucchiara, F., Fornaro, L., et al. (2021) · Cancers · doi:10.3390/cancers13153738 · Cited by 13 · see citing works
“7 trial, which compared the doublet standard chemotherapy with the addition of durvalumab and tremelimumab; no significant differences were seen neither in OS nor in PFS, in spite of a slightly non-significantly higher efficacy of the experimental arm [38].”
Background

Combined effect of ipilimumab and nivolumab improves oncology endpoints in metastatic melanoma patients
Wahid, M., Mandal, R. K., Jawed, A., Alsulimani, A., Hashem, A. M., Harakeh, S., Hussain, A., Fagoonee, S., Pellicano, R., & Haque, S. (2023) · Biotechnology and Genetic Engineering Reviews · doi:10.1080/02648725.2022.2147683
Five-Year Survival with Combined Nivolumab and Ipilimumab in Advanced Melanoma
Larkin, J., Chiarion-Sileni, V., Gonzalez, R., Grob, J.-J., Rutkowski, P., Lao, C. D., Cowey, C. L., Schadendorf, D., Wagstaff, J., Dummer, R., et al. (2019) · New England Journal of Medicine · doi:10.1056/nejmoa1910836 · Cited by 3,723 · see citing works
Utility Values Across Lines of Therapy in Immuno-Oncology Treatments: An Example from Advanced Melanoma
Tilden, D., Sierakowski, W., Cottrell, S., et al. (2017) · Value in Health · doi:10.1016/j.jval.2017.08.289
Risks and benefits of reinduction ipilimumab/nivolumab in melanoma patients previously treated with ipilimumab/nivolumab
Chapman, P. B., Jayaprakasam, V. S., Panageas, K. S., et al. (2021) · Journal for ImmunoTherapy of Cancer · doi:10.1136/jitc-2021-003395 · Cited by 15 · see citing works
TNFSF9 is associated with favor tumor immune microenvironment in patients with renal cell carcinoma who are treated with the combination therapy of nivolumab and ipilimumabPreprint
Isoda, B., Kandori, S., Sazuka, T., et al. (2024) · Research Square · doi:10.21203/rs.3.rs-4161771/v1

Authors: Moehler, M., Shitara, K., Garrido, M., Salman, P., Shen, L., Wyrwicz, L., Yamaguchi, K., Skoczylas, T., Campos Bragagnoli, A., Liu, T., Schenker, M., Yanez, P., Tehfe, M., Poulart, V., Cullen, D., Lei, M., Kondo, K., Li, M., Ajani, J. A., & Janjigian, Y. Y.
Affiliations: University Medical Center of the Johannes Gutenberg University Mainz (DE)
National Cancer Center Hospital East (JP)
Fundación Arturo López Pérez (CL)
Peking University Cancer Hospital (CN)
The Maria Sklodowska-Curie National Research Institute of Oncology (PL)
The Cancer Institute Hospital (JP)
Medical University of Lublin (PL)
Fudan University (CN)
Universidad de La Frontera (CL)
Centre Hospitalier de l’Université de Montréal (CA)
Bristol-Myers Squibb (United States) (US)
The University of Texas MD Anderson Cancer Center (US)
Memorial Sloan Kettering Cancer Center (US)
ORCID: Shitara, K.
Salman, P.
Shen, L.
Wyrwicz, L.
Yamaguchi, K.
Skoczylas, T.
Schenker, M.
Yanez, P.
Tehfe, M.
Lei, M.
Kondo, K.
Ajani, J.A.
Janjigian, Y.Y.
Venue: Annals of Oncology
Publisher: Elsevier BV
Published: 2020-09
Volume: 31
Pages: S1191
ISSN: 0923-7534 (ISSN-L)
DOI: 10.1016/j.annonc.2020.08.2296
OpenAlex: W3088611248
Cited by: 208
References: 0
Citations by year: 2026: 5 · 2025: 6 · 2024: 7 · 2023: 19 · 2022: 53 · 2021: 107 · 2020: 11
FWCI: 26.78
Type: journal article
Language: en
Open access: bronze
doi.org
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
www.elsevier.com/legal/tdmrep-license (tdm)
www.elsevier.com/open-access/userlicense/1.0/ (vor, 365 d)
Locations: Annals of Oncology (publishedVersion)
Funders: Bristol-Myers Squibb
Topics: Health Sciences › Medicine › Pulmonary and Respiratory Medicine › Gastric Cancer Management and Outcomes
Health Sciences › Medicine › Oncology › Cancer Immunotherapy and Biomarkers
Health Sciences › Medicine › Surgery › Esophageal Cancer Research and Treatment
Keywords: nivolumab, PD-1 inhibitors, advanced gastric cancer, gastroesophageal junction cancer, esophageal adenocarcinoma, first-line chemotherapy, PD-L1 combined positive score, overall survival, progression-free survival

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LBA6_PR Nivolumab (nivo) plus chemotherapy (chemo) versus chemo as first-line (1L) treatment for advanced gastric cancer/gastroesophageal junction cancer (GC/GEJC)/esophageal adenocarcinoma (EAC): First results of the CheckMate 649 study

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