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Chemotherapy in Advanced Gastric Cancer: A Systematic Review and Meta-Analysis Based on Aggregate Data
Open accessAbstract
Purpose: This systematic review and meta-analysis were performed to assess the efficacy and tolerability of chemotherapy in patients with advanced gastric cancer. Methods: Randomized phase II and III clinical trials on first-line chemotherapy in advanced gastric cancer were identified by electronic searches of Medline, Embase, the Cochrane Controlled Trials Register, and Cancerlit; hand searches of relevant abstract books and reference lists; and contact to experts. Meta-analysis was performed using the fixed-effect model. Overall survival, reported as hazard ratio (HR) with 95% CI, was the primary outcome measure. Results: Analysis of chemotherapy versus best supportive care (HR = 0.39; 95% CI, 0.28 to 0.52) and combination versus single agent, mainly fluorouracil (FU) -based chemotherapy (HR = 0.83; 95% CI = 0.74 to 0.93) showed significant overall survival benefits in favor of chemotherapy and combination chemotherapy, respectively. In addition, comparisons of FU/cisplatin-containing regimens with versus without anthracyclines (HR = 0.77; 95% CI, 0.62 to 0.95) and FU/anthracycline-containing combinations with versus without cisplatin (HR = 0.83; 95% CI, 0.76 to 0.91) both demonstrated a significant survival benefit for the three-drug combination. Comparing irinotecan-containing versus nonirinotecan-containing combinations (mainly FU/cisplatin) resulted in a nonsignificant survival benefit in favor of the irinotecan-containing regimens (HR = 0.88; 95% CI, 0.73 to 1.06), but they have never been compared against a three-drug combination. Conclusion: Best survival results are achieved with three-drug regimens containing FU, an anthracycline, and cisplatin. Among these, regimens including FU as bolus exhibit a higher rate of toxic deaths than regimens using a continuous infusion of FU, such as epirubicin, cisplatin, and continuous-infusion FU.
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“The pyrimidine analogue 5-fluorouracil (5-FU) is a synthetic analogue of uracil that inhibits thymidylate synthase, limiting the availability of thymidine nucleotides for DNA synthesis (Figure 1b, Figure 2c). 5-FU and the related 5-FU-prodrug capecitabine remain widely used chemotherapies today and are an important treatment for gastrointestinal cancers (Heidelberger et al., 1957; Wagner et al., 2”
From Targeting Metabolism for Cancer Therapy (2017) · cites this paper as Wagner et al., 2006
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“…these regimens are not entirely satisfactory because mean average survival can only be extended ~6 months compared to best supportive care only (3). poor therapy efficacy may be successful chemotherapy of gastric cancers, unfortunately, to date, clinical tests for predicting cancer…”
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Teker, F., Yılmaz, B., Kemal, Y., Kut, E., & Yücel, İ. (2014) · Asian Pacific Journal of Cancer Prevention · doi:10.7314/apjcp.2014.15.16.6727 · Cited by 9
“Despite recent advances in the treatment of AGC, patients treated with first line chemotherapy have median OS rarely exceeding 12 months (Wagner et al., 2006).”
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“Regimens include doublet or triplet-combination chemotherapy agents, usually platinum- or 5-fluorouracil (5FU)–based, with response rates ranging from 15% to 50% (2).”
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Pterostilbene enhances sorafenib’s anticancer effects on gastric adenocarcinoma
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BackgroundZNF280B promotes the growth of gastric cancer in�vitro and in�vivo
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“Although advances in surgical treatment and chemotherapy have improved GC outcomes in recent decades, the prognosis is still unsatisfactory [7-9].”
BackgroundlncRNA RMST is associated with the progression and prognosis of gastric cancer via miR-204-5p
Cai, H., Li, C., & Zhou, W. (2024) · Cell Division · doi:10.1186/s13008-024-00117-x · Cited by 7
Zhong, J., Yang, L., Liu, N., Zheng, J., & Lin, C. (2013) · Digestive Diseases and Sciences · doi:10.1007/s10620-013-2796-5 · Cited by 7
Zhu, X., Zhao, X., Peng, W. J., Sun, S., Cao, J., Ji, D., Liu, X., Wang, C., Huang, M., Yu, H., et al. (2014) · Journal of Cancer Research and Clinical Oncology · doi:10.1007/s00432-014-1754-8 · Cited by 7
“In 2006, Wagner published a review supporting ECF as the standard of care for MGC, but this opinion was challenged by other oncologists (Wagner et al. 2006; Ajani 2006; Al-Batran et al. 2007).”
MethodYu, C., Wang, R.-T., Chiang, L., & Lee, M. (2007) · Tetrahedron Letters · doi:10.1016/j.tetlet.2007.03.002 · Cited by 7
Berglund, Å., Byström, P., Johansson, B., Nygren, P., Frödin, J., Pedersen, D., Letocha, H., & Glimelius, B. L. G. (2009) · Medical Oncology · doi:10.1007/s12032-009-9173-4 · Cited by 7
Zhang, J., Cuiping, X., Xie, J. W., Liang, N., Wang, J., Qiao, L., Luo, H., & Zhang, J. (2014) · Journal of Cancer Research and Therapeutics · doi:10.4103/0973-1482.151487 · Cited by 7
Yao, Z., Hongqiang, G., Yuan, Y., Zhao, Y., Yao, S., Xu, Y.-J., Liu, L., Liu, T., Liu, Y., & Yang, S. (2013) · Journal of Chemotherapy · doi:10.1179/1973947813y.0000000120 · Cited by 7
Evolving treatments for advanced gastric cancer: appraisal of the survival trend
Roberto, M., Romiti, A., Onesti, C. E., Zullo, A., Falcone, R., & Marchetti, P. (2016) · Expert Review of Anticancer Therapy · doi:10.1080/14737140.2016.1184979 · Cited by 7
“Combination therapy as compared with single-drug chemotherapy has demonstrated higher efficacy, and its superiority was also confirmed in a meta-analysis [4].”
BackgroundDai, X., Zhang, X., Wang, C., Jiang, J., & Wu, C. (2016) · Oncotarget · doi:10.18632/oncotarget.13721 · Cited by 7
“Local recurrence and distant metastasis occur in 60% of mGC patients even with a radical stomach surgery [9] Chemotherapy is the most effective treatment option for patients with advanced gastric cancer who can’t be operated on [10-12].”
BackgroundKim, B. J., Kim, J. H., Jang, H. J., & Kim, H. S. (2017) · Oncotarget · doi:10.18632/oncotarget.20958 · Cited by 7
“For patients with advanced or metastatic diseases, combination chemotherapy can prolong median overall survival (OS) from 3–4 months to approximately 10–13 months with best supportive care [5, 6].”
BackgroundYen, C., Bai, L., Cheng, R., Hsiao, F., & Orlando, M. (2018) · Journal of Cancer Research and Practice · doi:10.1016/j.jcrpr.2018.03.001 · Cited by 7
Nigro, O., Chini, C., & Proserpio, I. (2021) · Anti-Cancer Drugs · doi:10.1097/cad.0000000000001071 · Cited by 7
Adjuvant chemoradiotherapy after D2 resection in gastric cancer: a single-center observational study
Saglam, E. K., Yücel, S., Balık, E., Sağlam, S., Asoğlu, O., Yamaner, S., Buğra, D., Oral, E. N., Kızır, A., Kapran, Y., et al. (2014) · Journal of Cancer Research and Clinical Oncology · doi:10.1007/s00432-014-1816-y · Cited by 7
“A meta-analysis showed better survival rates with three-drug regimen in patient with metastatic gastric cancer (Wagner et al. 2006).”
BackgroundNeoadjuvant treatment in upper gastrointestinal adenocarcinomas: new paradigms from old concepts?
Samalin, E., & Ychou, M. (2007) · Current Opinion in Oncology · doi:10.1097/cco.0b013e3281a73674 · Cited by 7
Barrett Esophagus and Esophageal Adenocarcinoma
Spechler, S. J., & Souza, R. F. (2008) · Wiley eBooks · doi:10.1002/9781444303254.ch35 · Cited by 7
An Analytics Approach to Designing Clinical Trials for Cancer
Relyea, S. L. (2013) · DSpace@MIT (Massachusetts Institute of Technology) · Cited by 7
Türkoğlu, E., Akdağ, G., Yıldırım, S., Kınıkoğlu, O., Busery, N. S., Kaya, T., Yıldız, H. Ş., Turkoglu, F., Tatar, C., Sakin, A., et al. (2025) · Medicina · doi:10.3390/medicina61061075 · Cited by 6
“These findings are consistent with previously reported survival outcomes in patients with metastatic gastric cancer [35,36].”
Wu, Z., Wang, H., Chu, X., Chen, J., & Fang, S. (2013) · Tumor Biology · doi:10.1007/s13277-013-0747-6 · Cited by 6
“In Asians, it is predicted to rank as the third most common cancer and causes serious damages to the public health [2–4].”
BackgroundThe combination of docetaxel, cisplatin, and 5-fluorouracil in advanced gastric cancer
Aharon, I. B., Purim, O., Kundel, Y., Brenner, R. M., Gordon, N., Sulkes, A., & Brenner, B. (2012) · Anti-Cancer Drugs · doi:10.1097/cad.0b013e32834fd780 · Cited by 6
Wen, F., Zheng, H., Wu, Y., Wheeler, J. R. C., Zeng, X., Fu, P., & Li, Q. (2016) · Scientific Reports · doi:10.1038/srep36060 · Cited by 6
Lim, K., Lee, H.-Y., Park, S. B., & Song, S. (2017) · Oncology · doi:10.1159/000471767 · Cited by 6
Eastern Canadian Colorectal Cancer Consensus Conference 2017
McGee, S. F., Alghareeb, W. A., Ahmad, C. H., Armstrong, D. E., Babak, S., Berry, S. R., Biagi, J. J., Booth, C. M., Bossé, D., Champion, P., et al. (2018) · Current Oncology · doi:10.3747/co.25.4083 · Cited by 6
Zarei, S., Reza, J. Z., Jaliani, H. Z., Hajizadeh, M. R., Sargazi, S., & Hosseinian, H. (2019) · Bratislavské lekárske listy/Bratislava medical journal · doi:10.4149/bll_2019_075 · Cited by 6
“Although various studies have established that the use alkylating agents as chemotherapeutic therapy substantially improved overall survival compared to single-agent therapy in vitro and in vivo (31, 32), the prognosis of advanced ovarian cancer remains poor, and novel treatments demonstrating favorable toxicity profi…”
Mahvi, D. M., & Krantz, S. B. (2012) · Elsevier eBooks · doi:10.1016/b978-1-4377-1560-6.00049-4 · Cited by 6
Liao, P., Cheng, S., Chou, C., Lin, H., Lin, C., Chen, T., Hsu, C., Teng, C. J., & Shih, Y. (2022) · Clinical Medicine Insights Oncology · doi:10.1177/11795549221123617 · Cited by 6
Ünek, İ. T., Akman, T., Öztop, İ., Ünal, O. Ü., Salman, T., & Yılmaz, U. (2012) · Gastric Cancer · doi:10.1007/s10120-012-0206-x · Cited by 6
“Cisplatin plus 5-fluorouracil (CF) and epirubicin plus CF (ECF) regimens have been investigated widely in clinical studies and were, until recently, presented as the reference regimens [2–12].”
BackgroundLoupakis, F., Masi, G., Fornaro, L., Vasile, E., Allegrini, G., Fontana, E., Granetto, C., Salvatore, L., Mentuccia, L., Andreuccetti, M., et al. (2010) · Cancer Chemotherapy and Pharmacology · doi:10.1007/s00280-009-1196-1 · Cited by 6
“A meta-analysis of studies comparing polychemotherapy to single-agent treatment showed a significant gain in median survival with combination therapy establishing its role in the palliative setting [4].”
BackgroundClinical management of gastric cancer: results of a multicentre survey
Zhang, X., Li, N., Wen, W., Yao, W., Xie, K., Hu, J., Shen, L., Ji, W., Lü, Y., Wen, F., et al. (2011) · BMC Cancer · doi:10.1186/1471-2407-11-369 · Cited by 6
“Second, is there an ideal setting or regimen that predicts whether chemotherapy and/or radiotherapy should be provided before and/or after surgery as (neo) adjuvant treatment in patients with localized disease? Finally, there is no internationally accepted standard of care for patients with metastatic and advanced can…”
Yang, G., Ma, F., Zhong, M., Fang, L., Peng, Y., Xin, X., Zhong, J., Zhu, W., & Zhang, Y. (2015) · Molecular Medicine Reports · doi:10.3892/mmr.2015.4107 · Cited by 6
RetractedYıldız, R., Kalender, M., Dane, F., Sevinç, A., Gümüş, M., Camcı, C., Alıcı, S., Ali Osman, K. A. Y. A., Yaman, E., Öztürk, B., et al. (2009) · Journal of Oncology Pharmacy Practice · doi:10.1177/1078155209347402 · Cited by 6
Zeng, C., Zhou, H., Yang, W., Wang, L., Xie, H. Q., & Yao, W. (2014) · Chinese Medical Journal · doi:10.3760/cma.j.issn.0366-6999.20131490 · Cited by 6
“Although surgery and appropriate adjuvant chemotherapy have resulted in superior overall survival as compared to other cancer-related death of the world,(3) the prognosis of unresectable or recurrent gastric cancer remains dismal and it is necessary to develop more effective chemotherapeutic regimens.(4,5)”
BackgroundTreatment of Gastric and Gastroesophageal Cancers—Do We Really Need Anthracyclines?
Ashraf, N., & Kim, R. D. (2016) · JAMA Oncology · doi:10.1001/jamaoncol.2016.3064 · Cited by 6
Zhu, C., Wang, Y., Wang, X., Bai, C., Su, D., Cao, B., & Xu, J. (2017) · Journal of Cancer · doi:10.7150/jca.17847 · Cited by 6
“Currently doublet and triplet regimens have been widely used in the treatment for gastric cancer [3,4,5].”
Background
Metadata
- Authors
- Wagner, A. D., Grothe, W., Haerting, J., Kleber, G., Grothey, A., & Fleig, W. E.
- Affiliations
- From the First Department of Medicine, Coordinating Centre for Clinical Trials, Department of Medicine IV, and Institute of Medical Epidemiology, Biostatistics and Informatics, Martin-Luther-University Halle-Wittenberg, Halle/Saale, Germany; and Mayo Clinic College of Medicine, Rochester, MN
- Mayo Clinic (US)
- Venue
- Journal of Clinical Oncology
- Published
- 2006-06-20
- Volume
- 24
- Issue
- 18
- Pages
- 2903-2909
- ISSN
- 0732-183X (ISSN-L)
- 1527-7755
- OpenAlex
- W2145390243
- Cited by
- 1,171
- References
- 51
- Citations by year
- 2026: 7 · 2025: 15 · 2024: 26 · 2023: 28 · 2022: 34 · 2021: 64 · 2020: 55 · 2019: 54 · 2018: 69 · 2017: 89 · 2016: 72 · 2015: 84 · 2014: 105 · 2013: 92 · 2012: 77
- FWCI
- 9.54
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Journal of Clinical Oncology (publishedVersion)
- PubMed (publishedVersion)
- Funders
- American Society of Clinical Oncology
- Bundesministerium für Bildung und Forschung (01GH0105)
- Topics
- Health Sciences › Medicine › Oncology › Gastric Cancer Management and Outcomes
- Health Sciences › Medicine › Oncology › Colorectal Cancer Treatments and Studies
- Health Sciences › Medicine › Surgery › Intraperitoneal and Appendiceal Malignancies
- Keywords
- advanced gastric cancer, first-line chemotherapy, 5-fluorouracil, cisplatin, anthracyclines, irinotecan, combination chemotherapy, overall survival, best supportive care, epirubicin, chemotherapy toxicity
- MeSH terms
- Antineoplastic Combined Chemotherapy Protocols, Humans, Stomach Neoplasms
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