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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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“Although various new therapeutic innovations such as gene therapy and Immunotherapy are being developed, chemotherapy remains the primary choice of treatment for a variety of cancers [1].”
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“Many patients, however, present a primary refractory disease or eventually progress [4], and their median overall survival only occasionally surpasses 12 months.”
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Kim, H. S., Kim, J. H., Jang, H. J., Han, B., & Zang, D. Y. (2018) · Journal of Cancer · doi:10.7150/jca.28204 · Cited by 49
“For patients with recurrent or metastatic diseases, systemic chemotherapy can prolong median overall survival (OS) from 3-4 months to approximately 10-13 months [5,6].”
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“Oncogenic KRAS promotes EMT and acquisition of CSC phenotypes in gastric epithelial cells We next examined the functional consequences of (1) oncogenic KRAS activation in human gastric epithelial cells and (2) KRAS inhibition in gastric adenocarcinoma cell lines.”
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“The median survival time for those with advanced GC is less than 1 year [2].”
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“None-theless, they translate into only modest progression-free survival (PFS) and overall survival (OS), which rarely exceed 7 and 12 months, respectively, in HER2-negative tumours (Wagner et al , 2006).”
BackgroundArtificial intelligence in gastric cancer: applications and challenges
Cao, R., Tang, L., Fang, M., Zhong, L., Wang, S., Gong, L., Li, J., Dong, D., & Tian, J. (2022) · Gastroenterology report · doi:10.1093/gastro/goac064 · Cited by 49
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Update on treatment of gastric cancer
Kuo, C., Chao, Y., & Li, C. (2014) · Journal of the Chinese Medical Association · doi:10.1016/j.jcma.2014.04.006 · Cited by 47
“The meta-analysis showed significant benefits from adding an anthracycline to a platinum and fluoropyrimidine doublet, and ECF (epirubicin plus cisplatin plus protracted infusion 5fluorouracil) is among the most active and well-tolerated regimens.(65) The combination of docetaxel, cisplatin, and 5fluorouracil (DCF) wa…”
BackgroundHER 2 Expression in Gastric and Gastro-esophageal Junction (GEJ) Adenocarcinomas
Rajagopal, I. (2015) · JOURNAL OF CLINICAL AND DIAGNOSTIC RESEARCH · doi:10.7860/jcdr/2015/12581.5630 · Cited by 47
“uncertainty regarding the choice of the chemotherapy regimen [6].”
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“Cisplatin and fluorpyrimidine combination regimens are widely accepted as standard therapy for this disease (Wagner et al, 2006).”
BackgroundMultidisciplinary management for esophageal and gastric cancer
Boniface, M., Wani, S. B., Schefter, T. E., Koo, P. J., Meguid, C. L., Leong, S., Kaplan, J., Wingrove, L. J., & McCarter, M. D. (2016) · Cancer Management and Research · doi:10.2147/cmar.s101169 · Cited by 47
“Here a multimodality approach is often beneficial since surgical, endoscopic, or radiation therapies may be used for symptom control in addition to systemic chemotherapy.(24) The palliative care team is available for both esophageal and gastric cancer patients seen in the EGMDC upon request.”
Li, Q., Jiang, H., Li, H., Xu, R., Shen, L., Yu, Y., Wang, Y., Cui, Y., Li, W., Yu, S., et al. (2016) · Oncotarget · doi:10.18632/oncotarget.10456 · Cited by 47
Multimodal treatment of gastric cancer
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microRNAs in gastric cancer invasion and metastasis
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Chemotherapy for advanced gastric cancer: across the years for a standard of care
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“analysed randomised Phase II and III trials in order to assess the efficacy and tolerability of chemotherapy in patients with AGC [75].”
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“To patients, these complications and side effects cause not only discomforts but also fatalities [37].”
BackgroundThe power of microRNAs as diagnostic and prognostic biomarkers in liquid biopsies
Quirico, L., & Orso, F. (2020) · Cancer Drug Resistance · doi:10.20517/cdr.2019.103 · Cited by 46
“Gastric cancer (GC) diagnosis at an early stage is difficult since its symptoms may be mild or absent, resulting in a seven-month median survival([57]).”
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Multidisciplinary management of gastric and gastroesophageal cancers
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A phase I/Ib study of OTSGC-A24 combined peptide vaccine in advanced gastric cancer
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“The 5-year overall survival (OS) for patients with unresectable GC due to locally advanced disease or metastatic spread ranges from 5 to 15% [1, 2].”
Pang, W., Lou, N., Jin, C., Hu, C., Chandoo, A., Zhu, G., & Shen, X. (2016) · European Journal of Gastroenterology & Hepatology · doi:10.1097/meg.0000000000000563 · Cited by 45
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“Table 2 shows the univariate analysis of clinicopathologic factors for the different recurrence patterns in patients with node-negative advanced GC.”
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Prognostic Value of the Preoperative Neutrophil to Lymphocyte Ratio in Resectable Gastric Cancer
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“Although there have been advances in diagnosis and management, most GC patients present with locally advanced or metastatic disease with a 5-year survival rate of <10%.(2,3) The tumor-node-metastasis (TNM) staging mainly focuses on the tumor itself, that is, its biological behavior, and is the most important prognosti…”
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Biswas, P., Kaium, M. A., Tareq, M. M. I., Tauhida, S. J., Hossain, M. R., Siam, L. S., Parvez, A., Bibi, S., Hasan, M. H., Rahman, M. M., et al. (2024) · Biomedicine & Pharmacotherapy · doi:10.1016/j.biopha.2024.116860 · Cited by 43
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“Although chemotherapy, radiotherapy and targeted therapy have improved the response rate in advanced gastric cancer patients, metastasis remains the most common cause of mortality (4).”
Palliative management of gastric cancer
Cunningham, S. C., & Schulick, R. D. (2007) · Surgical Oncology · doi:10.1016/j.suronc.2007.08.004 · Cited by 43
“Chemotherapy for advanced gastric cancer was recently reviewed [52–54], and need not be rereviewed here.”
BackgroundTrastuzumab for gastric cancer
Meza–Junco, J., Au, H., & Sawyer, M. B. (2009) · Expert Opinion on Biological Therapy · doi:10.1517/14712590903439702 · Cited by 43
“Singleagent versus combination chemotherapy has also been addressed [12,13].”
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“However, most gastric cancers are diagnosed at advanced or metastatic stages when the tumor is considered unresectable [3, 4], especially in many endemic areas where programs for early detection is limited.”
BackgroundGeographic differences in approach to advanced gastric cancer: Is there a standard approach?
Kim, R. D., Tan, A., Choi, M., & El‐Rayes, B. F. (2013) · Critical Reviews in Oncology/Hematology · doi:10.1016/j.critrevonc.2013.05.007 · Cited by 42
Systemic Therapy for Advanced Gastric Cancer: A Clinical Practice Guideline
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Cutsem, E. V., Muro, K., Cunningham, D., Bodoky, G., Sobrero, A. F., Cascinu, S., Ajani, J. A., Oh, S. C., Al-Batran, S. E., Wainberg, Z. A., et al. (2020) · European Journal of Cancer · doi:10.1016/j.ejca.2019.10.026 · Cited by 42
“Patients receiving initial treatment with first-line platinum/fluoropyrimidine chemotherapy, with or without docetaxel or epirubicin, may initially respond to treatment but relapse over time [3].”
BackgroundMulazzani, G., Corti, F., Valle, S. D., & Bartolomeo, M. D. (2021) · Nutrients · doi:10.3390/nu13082766 · Cited by 42
“In the setting of advanced unresectable or metastatic GC, chemotherapy should be offered to patients with adequate performance status and organ function, as it improves QoL and survival outcomes over the best supportive care (BSC) alone [88,89].”
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“Furthermore, cetuximab preclinical anti-tumour activity was not predicted by relative total or activated EGFR tumour expression levels (Wild et al. 2006).”
BackgroundCurrent status of targeted therapies in advanced gastric cancer
Vita, F. D., Giuliani, F., Silvestris, N., Rossetti, S., Pizzolorusso, A., Santabarbara, G., Galizia, G., Colucci, G., Ciardiello, F., & Orditura, M. (2012) · Expert Opinion on Therapeutic Targets · doi:10.1517/14728222.2011.652616 · Cited by 42
“Metastatic gastric cancer (GC) has a poor outcome [1,2]; in this setting, chemotherapy improves quality of life (QoL) and prolongs survival when compared to best supportive care (BSC) alone [3].”
BackgroundHe, H., Wang, C., Shen, Z., Fang, Y., Wang, X., Chen, W., Liu, F., Qin, X., & Sun, Y. (2013) · PLoS ONE · doi:10.1371/journal.pone.0071864 · Cited by 41
“Chemotherapy is an indispensable element of treatment for gastric cancer patients, and fluoropyrimidines, platinumcontaining agents, alone or in combinations, are the most effective and commonly used chemotherapy regimens [23].”
BackgroundMoon, J. Y., Cho, M., Ahn, K. S., & Cho, S. K. (2013) · Nutrition and Cancer · doi:10.1080/01635581.2013.756529 · Cited by 42
“Currently, chemotherapy regimens represent the primary treatment option for patients with gastric cancer (3).”
BackgroundA Phase I–II Study of Postoperative Capecitabine-Based Chemoradiotherapy in Gastric Cancer
Jansen, E. P. M., Boot, H., Saunders, M. P., Crosby, T. D. L., Dubbelman, R., Bartelink, H. G. M. M., Verheij, M., & Cats, A. (2007) · International Journal of Radiation Oncology*Biology*Physics · doi:10.1016/j.ijrobp.2007.05.004 · Cited by 41
“In patients with advanced gastric cancer, 5-FU–based regimens were reported to be effective (24).”
BackgroundTargeting the fibroblast growth factor receptor 2 in gastric cancer: promise or pitfall?
Hierro, C., Alsina, M., Sánchez-Guixé, M., Serra, V., Rodon, J. A., & Tabernero, J. M. (2017) · Annals of Oncology · doi:10.1093/annonc/mdx081 · Cited by 41
“Over the last 20 years, efforts have been made in order to improve the results of initial chemotherapeutic regimens, using combinations of platinum salts and fluoropyrimidines as the more frequent backbone strategy with or without a third drug [3].”
BackgroundLee, M. S., Cha, E. Y., Thương, P. T., Kim, J. Y., Ahn, M., & Sul, J. Y. (2010) · Biological and Pharmaceutical Bulletin · doi:10.1248/bpb.33.931 · Cited by 41
CD2AP inhibits metastasis in gastric cancer by promoting cellular adhesion and cytoskeleton assembly
Xie, W., Chen, C., Han, Z., Huang, J., Liu, X., Chen, H., Zhang, T., Chen, S., Chen, C., Lu, M., et al. (2020) · Molecular Carcinogenesis · doi:10.1002/mc.23158 · Cited by 40
Yoshida, S., Watabe, H., Isayama, H., Kogure, H., Nakai, Y., Yamamoto, N., Sasaki, T., Kawakubo, K., Hamada, T., Ito, Y., et al. (2012) · Digestive Endoscopy · doi:10.1111/j.1443-1661.2012.01353.x · Cited by 40
Menges, M., & Hoehler, T. (2008) · Journal of Cancer Research and Clinical Oncology · doi:10.1007/s00432-008-0425-z · Cited by 40
“In a meta-analysis, the comparison of irinotecan versus non-irinotecan-based regimens (mainly 5-FU/cisplatin) resulted in a nonstatistically signiWcant trend toward better survival with irinotecan (HR for death 0.88) (Wagner et al. 2006).”
BackgroundInfluentialYu, P., Huang, L., Cheng, G., Yang, L., Dai, G., Ying, J., & Du, Y. (2017) · Oncotarget · doi:10.18632/oncotarget.19759 · Cited by 40
“Chemotherapy is another main treatment for these patients, and improves quality of life and OS [17].”
BackgroundIizumi, S., Takashima, A., Sakamaki, K., Morita, S., & Boku, N. (2018) · Cancer Chemotherapy and Pharmacology · doi:10.1007/s00280-018-3569-9 · Cited by 40
Curran, D., Pozzo, C., Załuski, J., Dank, M., Barone, C., Valvere, V., Yalçın, Ş., Peschel, C., Wenczl, M., Göker, E., et al. (2009) · Quality of Life Research · doi:10.1007/s11136-009-9493-z · Cited by 40
“QoL assessment should be incorporated as a prominent objective in phase III studies in advanced gastric cancer to help both patients and physicians to discuss treatment choices and aid decision making [6, 7].”
BackgroundCurrent and Future Therapies for Advanced Gastric Cancer
Davidson, M., Okines, A. F. C., & Starling, N. (2015) · Clinical Colorectal Cancer · doi:10.1016/j.clcc.2015.05.013 · Cited by 39
Kim, K. H., Kwon, H.-C., Oh, S. Y., Kim, S. H., Lee, S., Kwon, K. A., Jang, J. S., Kim, M. C., Kim, S.-J., & Kim, H. (2010) · Biomarkers · doi:10.3109/1354750x.2010.533284 · Cited by 39
“In fact, the combination of 5-FU and cisplatin (FP) is regarded as a standard chemotherapeutic protocol for metastatic gastric cancer(Wagner et al., 2006).”
BackgroundMedical management of gastric cancer: A 2014 update
Elimova, E. C. (2014) · World Journal of Gastroenterology · doi:10.3748/wjg.v20.i38.13637 · Cited by 39
Efficacy and safety for Apatinib treatment in advanced gastric cancer: a real world study
Zhang, Y., Han, C., Li, J., Zhang, L., Wang, L., Ye, S., Hu, Y., & Bai, L. (2017) · Scientific Reports · doi:10.1038/s41598-017-13192-8 · Cited by 39
Zhang, Y., Liu, S., Qin, F., Huang, X., Wang, X., Peng, Y., Zhao, Z., & Liu, Z. (2018) · Journal of Cellular Biochemistry · doi:10.1002/jcb.27491 · Cited by 41
“Unfortunately, the resistance to chemotherapeutic agents is easily developed within a short period of symptom control.(3,4) To combat the dismal mortality rates, some new drugs and therapeutics strategies are needed.”
BackgroundChen, J., Li, T., Liang, J., Huang, Q., Huang, J., Ke, Y., & Sun, H. (2021) · Biomedicine & Pharmacotherapy · doi:10.1016/j.biopha.2021.112443 · Cited by 40
Chen, S., Tian, W., Zhang, L., Kim, S., Ding, W., & Tong, Y. (2014) · Drug Design Development and Therapy · doi:10.2147/dddt.s74379 · Cited by 39
“receive palliative chemotherapy is barely 5% to 10%.(5,6) Therefore, a new strategy for the treatment of gastric cancer is urgently needed.”
Koopman, T., Smits, M. M., Louwen, M., Hage, M., Boot, H., & Imholz, A. L. T. (2014) · Journal of Cancer Research and Clinical Oncology · doi:10.1007/s00432-014-1900-3 · Cited by 38
“Advanced cancer patients have a poor prognosis with median survival of months rather than years, even if treated with chemotherapy (Chau et al. 2009; Chua and Merrett 2012; Wagner et al. 2006).”
BackgroundCritical appraisal of trastuzumab in treatment of advanced stomach cancer
Meza–Junco, J., Au, H., & Sawyer, M. B. (2011) · Cancer Management and Research · doi:10.2147/cmar.s12698 · Cited by 38
Matt, P., van Zwieten‐Boot, B., Calvo, G., ter Hofstede, H. J. M., García‐Carbonero, R., Camarero, J., Abadie, E., & Pignatti, F. (2011) · The Oncologist · doi:10.1634/theoncologist.2011-0224 · Cited by 38
Palle, J., Tougeron, D., Pozet, A., Soularue, É., Artru, P., Leroy, F., Dubreuil, O., Sarabi, M., Williet, N., Manfrédi, S., et al. (2017) · Oncotarget · doi:10.18632/oncotarget.20711 · Cited by 38
“For patients with inoperable locally advanced or metastatic disease, systemic chemotherapy improves survival and quality of life compared with best supportive care alone [2].”
BackgroundLocally Advanced and Metastatic Gastric Cancer
Field, K. M., Michael, M., & Leong, T. (2008) · Drugs · doi:10.2165/00003495-200868030-00004 · Cited by 38
Metachronous Ovarian Metastases Following Resection of the Primary Gastric Cancer
Jun, S.-Y., & Park, J. K. (2011) · Journal of the Korean Gastric Cancer Association · doi:10.5230/jgc.2011.11.1.31 · Cited by 38
New perspectives in the treatment of advanced or metastatic gastric cancer
Rosati, G., Ferrara, D., & Manzione, L. (2009) · World Journal of Gastroenterology · doi:10.3748/wjg.15.2689 · Cited by 38
Pharmacokinetics and pharmacogenomics in gastric cancer chemotherapy
Nishiyama, M., & Eguchi, H. (2008) · Advanced Drug Delivery Reviews · doi:10.1016/j.addr.2008.09.004 · Cited by 38
“001) and an advantage of cisplatin based on OS [14].”
BackgroundKim, S. T., Jang, H.-L., Lee, S. J., Lee, J., Choi, Y., Kim, K., Cho, J., Park, S. H., Park, Y. S., Lim, H. Y., et al. (2014) · Molecular Cancer Therapeutics · doi:10.1158/1535-7163.mct-14-0255 · Cited by 38
“with advanced gastric cancer (AGC) and have substantially improved outcomes compared with single-agent chemotherapy or best supportive care (4).”
BackgroundThe progress of targeted therapy in advanced gastric cancer
Qiu, M., & Xu, R. (2013) · Biomarker Research · doi:10.1186/2050-7771-1-32 · Cited by 37
“The median survival of advanced gastric cancer patients who received palliative chemotherapy is approximately 7 to 11 months [4-8].”
BackgroundNishimura, T., Mitsunaga, M., Ito, K., Kobayashi, H., & Saruta, M. (2019) · Gastric Cancer · doi:10.1007/s10120-019-00988-y · Cited by 37
Guo, X., Zhao, F., Ma, X., Shen, G., Ren, D., Zheng, F., Du, F., Wang, Z., Ahmad, R., Yuan, X., et al. (2019) · BMC Cancer · doi:10.1186/s12885-019-6294-9 · Cited by 38
“An early meta-analysis confirmed that anthracycline-based triplet regimens could improve OS [41].”
BackgroundResultGenetic variant of cyclooxygenase-2 in gastric cancer: More inflammation and susceptibility
Ji, X.-K., Madhurapantula, S. V., He, G., Wang, K., Song, C., Zhang, J., & Wang, K.-J. (2021) · World Journal of Gastroenterology · doi:10.3748/wjg.v27.i28.4653 · Cited by 37
Cabalag, C. S., Chan, S. T. F., Kaneko, Y., & Duong, C. P. (2014) · Gastric Cancer · doi:10.1007/s10120-014-0388-5 · Cited by 37
“measured quality of life-adjusted survival as a major outcome [27].”
BackgroundTreatment Options for Surgically Resectable Gastric Cancer
Rajdev, L. N. (2010) · Current Treatment Options in Oncology · doi:10.1007/s11864-010-0117-1 · Cited by 37
“5-FU as a single agent is less active than ECF in advanced gastric cancer [ 31 ], and therefore may be less effective at eliminating micrometastatic disease in patients with apparently localized disease.”
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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