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Review Article
The Current Evidence and Future Direction of Adjuvant Treatment for Gastric Cancer in the Era of Precision Medicine
Jong Hyuk Yun, Yoon Young Choi, Jae-Ho Cheong
Received December 18, 2024  Accepted January 22, 2025  Published online January 23, 2025  
DOI: https://doi.org/10.4143/crt.2024.1222    [Accepted]
AbstractAbstract PDF
Although gastric cancer remains a significant global health burden, its treatment strategies vary across different geographical regions, leading to distinct guidelines. In Asia, particularly in Korea, D2 gastrectomy followed by adjuvant chemotherapy has been established as the standard treatment for stage II/III gastric cancer based on landmark clinical trials. However, this "one-size-fits-all" approach requires refinement as emerging evidence suggests heterogeneous outcomes even within the same stage. This review discusses the evolving landscape of adjuvant treatment in gastric cancer, emphasizing the transition towards precision medicine. Recent molecular characterization of gastric cancer has revealed distinct subtypes with varying prognoses and chemotherapy responses, exemplified by the favorable outcomes of microsatellite instability-high tumors without adjuvant chemotherapy. Additionally, clinical factors including sub-stages within stage II/III, patient performance status, comorbidities, and personal preferences should be considered in treatment decisions. The integration of these molecular and clinical factors, along with shared decision-making between physicians and patients, represents a crucial step toward personalized treatment approaches. Looking ahead, the field is poised for further evolution with the emergence of immune checkpoint inhibitors, growing evidence for neoadjuvant chemotherapy in selected cases, and the potential of circulating tumor DNA as a biomarker for minimal residual disease. This comprehensive approach to treatment decision-making, considering both tumor biology and patient factors, will be essential for realizing precision medicine in gastric cancer care.
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Original Articles
Gastrointestinal cancer
A Multi-cohort Study of the Prognostic Significance of Microsatellite Instability or Mismatch Repair Status after Recurrence of Resectable Gastric Cancer
Ji Yeong An, Yoon Young Choi, Jeeyun Lee, Woo Jin Hyung, Kyoung-Mee Kim, Sung Hoon Noh, Min-Gew Choi, Jae-Ho Cheong
Cancer Res Treat. 2020;52(4):1153-1161.   Published online May 4, 2020
DOI: https://doi.org/10.4143/crt.2020.173
AbstractAbstract PDFSupplementary MaterialPubReaderePub
Purpose
High microsatellite instability (MSI) is related to good prognosis in gastric cancer. We aimed to identify the prognostic factors of patients with recurrent gastric cancer and investigate the role of MSI as a prognostic and predictive biomarker of survival after tumor recurrence.
Materials and Methods
This retrospective cohort study enrolled patients treated for stage II/III gastric cancer who developed tumor recurrence and in whom the MSI status or mismatch repair (MMR) status of the tumor was known. MSI status and the expression of MMR proteins were evaluated using polymerase chain reaction and immunohistochemical analysis, respectively.
Results
Of the 790 patients included, 64 (8.1%) had high MSI status or MMR deficiency. The tumor-node-metastasis stage, type of recurrence, Lauren classification, chemotherapy after recurrence, and interval to recurrence were independently associated with survival after tumor recurrence. The MSI/MMR status and receiving adjuvant chemotherapy were not associated with survival after recurrence. In a subgroup analysis of patients with high MSI or MMR-deficient gastric cancer, those who did not receive adjuvant chemotherapy had better treatment response to chemotherapy after recurrence than those who received adjuvant chemotherapy.
Conclusion
Patients with high MSI/MMR-deficient gastric cancer should be spared from adjuvant chemotherapy after surgery, but aggressive chemotherapy after recurrence should be considered. Higher tumor-node-metastasis stage, Lauren classification, interval to recurrence, and type of recurrence are associated with survival after tumor recurrence and should thus be considered when establishing a treatment plan and designing clinical trials targeting recurrent gastric cancer.

Citations

Citations to this article as recorded by  
  • HIGD1B, as a novel prognostic biomarker, is involved in regulating the tumor microenvironment and immune cell infiltration; its overexpression leads to poor prognosis in gastric cancer patients
    Shibo Wang, Siyi Zhang, Xiaoxuan Li, Xiangxue Li, Shufen Zhao, Jing Guo, Shasha Wang, Rui Wang, Mengqi Zhang, Wensheng Qiu
    Frontiers in Immunology.2024;[Epub]     CrossRef
  • Proteomic signatures of infiltrative gastric cancer by proteomic and bioinformatic analysis
    Li-Hua Zhang, Hui-Qin Zhuo, Jing-Jing Hou, Yang Zhou, Jia Cheng, Jian-Chun Cai
    World Journal of Gastrointestinal Oncology.2022; 14(11): 2097.     CrossRef
  • The distinct clinical trajectory, metastatic sites, and immunobiology of microsatellite-instability-high cancers
    Shuting Han, Aik Yong Chok, Daniel Yang Yao Peh, Joshua Zhi-Ming Ho, Emile Kwong Wei Tan, Si-Lin Koo, Iain Bee-Huat Tan, Johnny Chin-Ann Ong
    Frontiers in Genetics.2022;[Epub]     CrossRef
  • Mismatch Repair Status Characterization in Oncologic Pathology: Taking Stock of the Real-World Possibilities
    Roberto Piciotti, Konstantinos Venetis, Elham Sajjadi, Nicola Fusco
    Journal of Molecular Pathology.2021; 2(2): 93.     CrossRef
  • The Impact of Mismatch Repair Status on Prognosis of Patients With Gastric Cancer: A Multicenter Analysis
    Wen-Long Guan, Yue Ma, Yue-Hong Cui, Tian-Shu Liu, Yan-Qiao Zhang, Zhi-Wei Zhou, Jian-Ying Xu, Li-Qiong Yang, Jia-Yu Li, Yu-Ting Sun, Rui-Hua Xu, Feng-Hua Wang, Miao-Zhen Qiu
    Frontiers in Oncology.2021;[Epub]     CrossRef
  • Establishment of a 5-gene risk model related to regulatory T cells for predicting gastric cancer prognosis
    Gang Hu, Ningjie Sun, Jiansong Jiang, Xiansheng Chen
    Cancer Cell International.2020;[Epub]     CrossRef
  • Mismatch Repair System Genomic Scars in Gastroesophageal Cancers: Biology and Clinical Testing
    Gianluca Lopez, Konstantinos Venetis, Elham Sajjadi, Nicola Fusco
    Gastrointestinal Disorders.2020; 2(4): 341.     CrossRef
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  • 15 Web of Science
  • 7 Crossref
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Immunohistochemistry Biomarkers Predict Survival in Stage II/III Gastric Cancer Patients: From a Prospective Clinical Trial
Min Hwan Kim, Xianglan Zhang, Minkyu Jung, Inkyung Jung, Hyung Soon Park, Seung-Hoon Beom, Hyo Song Kim, Sun Young Rha, Hyunki Kim, Yoon Young Choi, Taeil Son, Hyoung-Il Kim, Jae-Ho Cheong, Woo Jin Hyung, Sung Hoon Noh, Hyun Cheol Chung
Cancer Res Treat. 2019;51(2):819-831.   Published online September 27, 2018
DOI: https://doi.org/10.4143/crt.2018.331
AbstractAbstract PDFSupplementary MaterialPubReaderePub
Purpose
Identification of biomarkers to predict recurrence risk is essential to improve adjuvant treatment strategies in stage II/III gastric cancer patients. This study evaluated biomarkers for predicting survival after surgical resection.
Materials and Methods
This post-hoc analysis evaluated patients from the CLASSIC trial who underwent D2 gastrectomy with or without adjuvant chemotherapy (capecitabine plus oxaliplatin) at the Yonsei Cancer Center. Tumor expressions of thymidylate synthase (TS), excision repair cross-complementation group 1 (ERCC1), and programmed death-ligand 1 (PD-L1) were evaluated by immunohistochemical (IHC) staining to determine their predictive values.
Results
Among 139 patients, IHC analysis revealed high tumor expression of TS (n=22, 15.8%), ERCC1 (n=23, 16.5%), and PD-L1 (n=42, 30.2%) in the subset of patients. Among all patients, high TS expression tended to predict poor disease-free survival (DFS; hazard ratio [HR], 1.80; p=0.053), whereas PD-L1 positivity was associated with favorable DFS (HR, 0.33; p=0.001) and overall survival (OS; HR, 0.38; p=0.009) in multivariate Cox analysis. In the subgroup analysis, poor DFS was independently predicted by high TS expression (HR, 2.51; p=0.022) in the adjuvant chemotherapy subgroup (n=66). High PD-L1 expression was associated with favorable DFS (HR, 0.25; p=0.011) and OS (HR, 0.22; p=0.015) only in the surgery-alone subgroup (n=73). The prognostic impact of high ERCC1 expression was not significant in the multivariate Cox analysis.
Conclusion
This study shows that high TS expression is a predictive factor for worse outcomes on capecitabine plus oxaliplatin adjuvant chemotherapy, whereas PD-L1 expression is a favorable prognostic factor in locally advanced gastric cancer patients.

Citations

Citations to this article as recorded by  
  • Utility of TMPRSS4 as a Prognostic Biomarker and Potential Therapeutic Target in Patients with Gastric Cancer
    Hirofumi Tazawa, Takahisa Suzuki, Akihisa Saito, Akira Ishikawa, Toshiaki Komo, Haruki Sada, Norimitsu Shimada, Naoto Hadano, Takashi Onoe, Takeshi Sudo, Yosuke Shimizu, Kazuya Kuraoka, Hirotaka Tashiro
    Journal of Gastrointestinal Surgery.2022; 26(2): 305.     CrossRef
  • Scoring systems for PD-L1 expression and their prognostic impact in patients with resectable gastric cancer
    Marina Alessandra Pereira, Marcus Fernando Kodama Pertille Ramos, André Roncon Dias, Renan Ribeiro, Leonardo Cardili, Bruno Zilberstein, Ivan Cecconello, Ulysses Ribeiro, Evandro Sobroza de Mello, Tiago Biachi de Castria
    Virchows Archiv.2021; 478(6): 1039.     CrossRef
  • Epstein–Barr Virus Positive Gastric Cancer: A Distinct Subtype Candidate for Immunotherapy
    Marina Alessandra Pereira, Daniel Amadeus Molon Batista, Marcus Fernando Kodama Pertille Ramos, Leonardo Cardili, Renan Ribeiro e Ribeiro, Andre Roncon Dias, Bruno Zilberstein, Ulysses Ribeiro Jr, Ivan Cecconello, Venâncio Avancini Ferreira Alves, Evandro
    Journal of Surgical Research.2021; 261: 130.     CrossRef
  • Cytotoxic T‐lymphocyte‐associated protein 4 in gastric cancer: Prognosis and association with PD‐L1 expression
    Marina Alessandra Pereira, Tiago Biachi de Castria, Marcus Fernando Kodama Pertille Ramos, André Roncon Dias, Leonardo Cardili, Rafael Dyer Rodrigues de Moraes, Bruno Zilberstein, Sergio Carlos Nahas, Ulysses Ribeiro, Evandro Sobroza de Mello
    Journal of Surgical Oncology.2021; 124(7): 1040.     CrossRef
  • Remnant gastric cancer: a neglected group with high potential for immunotherapy
    Marcus Fernando Kodama Pertille Ramos, Marina Alessandra Pereira, Tiago Biachi de Castria, Renan Ribeiro e Ribeiro, Leonardo Cardili, Evandro Sobroza de Mello, Bruno Zilberstein, Ulysses Ribeiro-Júnior, Ivan Cecconello
    Journal of Cancer Research and Clinical Oncology.2020; 146(12): 3373.     CrossRef
  • Molecular Bases of Mechanisms Accounting for Drug Resistance in Gastric Adenocarcinoma
    Jose J. G. Marin, Laura Perez-Silva, Rocio I. R. Macias, Maitane Asensio, Ana Peleteiro-Vigil, Anabel Sanchez-Martin, Candela Cives-Losada, Paula Sanchon-Sanchez, Beatriz Sanchez De Blas, Elisa Herraez, Oscar Briz, Elisa Lozano
    Cancers.2020; 12(8): 2116.     CrossRef
  • Clinical Significance of CLDN18.2 Expression in Metastatic Diffuse-Type Gastric Cancer
    Seo Ree Kim, Kabsoo Shin, Jae Myung Park, Han Hong Lee, Kyo Yong Song, Sung Hak Lee, Bohyun Kim, Sang-Yeob Kim, Junyoung Seo, Jeong-Oh Kim, Sang-Young Roh, In-Ho Kim
    Journal of Gastric Cancer.2020; 20(4): 408.     CrossRef
  • Prognostic and Predictive Factors for the Curative Treatment of Esophageal and Gastric Cancer in Randomized Controlled Trials: A Systematic Review and Meta-Analysis
    van den Ende, ter Veer, Mali, van Berge Henegouwen, Hulshof, van Oijen, van Laarhoven
    Cancers.2019; 11(4): 530.     CrossRef
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S-1 Based Doublet as an Adjuvant Chemotherapy for Curatively Resected Stage III Gastric Cancer: Results from the Randomized Phase III POST Trial
Choong-kun Lee, Minkyu Jung, Hyo Song Kim, Inkyung Jung, Dong Bok Shin, Seok Yun Kang, Dae Young Zang, Ki Hyang Kim, Moon Hee Lee, Bong-Seog Kim, Kyung Hee Lee, Jae-Ho Cheong, Woo Jin Hyung, Sung Hoon Noh, Hyun Cheol Chung, Sun Young Rha
Cancer Res Treat. 2019;51(1):1-11.   Published online February 5, 2018
DOI: https://doi.org/10.4143/crt.2018.028
AbstractAbstract PDFSupplementary MaterialPubReaderePub
Purpose
We conducted a randomized, multicenter, phase III trial to compare S-1 plus docetaxel (DS) with S-1 plus cisplatin (SP) as adjuvant chemotherapy for stage III gastric cancer patients.
Materials and Methods
Stage III gastric cancer patients who had received curative gastrectomy with D2 lymphadenectomy were randomized into equal groups to receive adjuvant chemotherapy of eight cycles of DS (S-1 70 mg/m2 /day on days 1-14 plus docetaxel 35 mg/m2 on days 1 and 8) every 3 weeks or SP (S-1 70 mg/m2 /day on days 1-14 plus cisplatin 60 mg/m2 on day 1) every 3 weeks. The primary endpoint was 3-year disease-free survival (DFS) rate.
Results
Between November 2010 and July 2013, 153 patients (75 patients to DS and 78 patients to SP) were enrolled from 8 institutions in Korea. After the capecitabine plus oxaliplatin was approved based on the CLASSIC study, itwas decided to close the study early. With a median follow-up duration of 56.9 months, the 3-year DFS rate between two groups was not significantly different (49.14% in DS group vs. 52.5% in SP group). The most common grade 3-4 adverse event was neutropenia (42.7% in DS and 38.5% in SP, p=0.351). SP group had more grade 3-4 anemia (1.3% vs. 11.5%, p=0.037), whereas grade 3-4 hand-foot syndrome (4.1% vs. 0%, p=0.025) and mucositis (10.7% vs. 2.6%, p=0.001) were more common in DS group. Fifty-one patients (68%) in DS group and 52 (66.7%) in SP group finished planned treatment.
Conclusion
Our findings suggest that SP or DS is an effective and tolerable option for patients with curatively resected stage III gastric cancer.

Citations

Citations to this article as recorded by  
  • Efficacy and safety of docetaxel plus S-1-based therapy in gastric cancer: a quantitative evidence synthesis of randomized controlled trials
    Hui-Fen Lv, Li-Feng Qin, Rui-Zhi Ran, Xue-Ping Jiang, Fang-Yu Zhao, Bo Li
    Frontiers in Pharmacology.2024;[Epub]     CrossRef
  • A novel method of bedside hyperthermic intraperitoneal chemotherapy as adjuvant therapy for stage-III gastric cancer
    Lili Liu, Li Sun, Ning Zhang, Cheng-gong Liao, Haichuan Su, Jie Min, Yang Song, Xue Yang, Xiaofeng Huang, Dongxu Chen, Yu Chen, Hong-wei Zhang, Helong Zhang
    International Journal of Hyperthermia.2022; 39(1): 239.     CrossRef
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    Qiang Hu, Yuanshui Sun
    Clinical Nutrition.2021; 40(3): 1438.     CrossRef
  • THE ROLE OF ADJUVANT CHEMOTHERAPY IN THE TREATMENT OF LOCALLY ADVANCED GASTRIC CANCER
    A. A. Bobryshev, M. M. Davudov, M. N. Narimanov, S. B. Polycarpova, V. Y. Kirsanov, V. N. Blindar
    Siberian journal of oncology.2021; 20(1): 133.     CrossRef
  • Multidisciplinary treatment strategy for locally advanced gastric cancer: A systematic review
    Kotaro Sugawara, Yoshikuni Kawaguchi, Yasuyuki Seto, Jean-Nicolas Vauthey
    Surgical Oncology.2021; 38: 101599.     CrossRef
  • Surgery alone, adjuvant tegafur/gimeracil/octeracil (S-1), or platinum-based chemotherapies for resectable gastric cancer: real-world experience and a propensity score matching analysis
    Chih-Chieh Yen, Yan-Shen Shan, Ying-Jui Chao, Ting-Kai Liao, I-Shu Chen, Hsuan-Yi Huang, I-Ting Liu, Chia-Jui Yen
    BMC Cancer.2021;[Epub]     CrossRef
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    Expert Review of Gastroenterology & Hepatology.2018; 12(11): 1109.     CrossRef
  • 13,125 View
  • 591 Download
  • 23 Web of Science
  • 11 Crossref
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