Skip to main content
Top
Published in: BMC Cancer 1/2016

Open Access 01-12-2016 | Research article

Which is better for gastric cancer patients, perioperative or adjuvant chemotherapy: a meta-analysis

Authors: Jun-hua Zhao, Peng Gao, Yong-xi Song, Jing-xu Sun, Xiao-wan Chen, Bin Ma, Yu-chong Yang, Zhen-ning Wang

Published in: BMC Cancer | Issue 1/2016

Login to get access

Abstract

Background

The preferred chemotherapy method for gastric cancer continues to be matter of debate. We performed a meta-analysis to comparing prognosis and safety between perioperative chemotherapy and adjuvant chemotherapy to identify the better chemotherapy option for gastric cancer.

Methods

We searched the PubMed, EMBASE, Cochrane Library, and Ovid databases for eligible studies until February 2016. The main endpoints were prognostic value (hazard ratio [HR] for overall survival [OS] and 1-, 2-, 3-, and 5-year survival rate), response rate of chemotherapy, radical resection rate, post-operative complication rate, and adverse effects of chemotherapy.

Results

Five randomized controlled trials and six clinical controlled trials involving 1,240 patients were eligible for analysis. Compared with the adjuvant chemotherapy group, the perioperative chemotherapy group had significantly better prognosis (HR, 0.74; 95 % CI, 0.61 to 0.89; P < 0.01). The difference between the two groups remained significant in the studies that used combination chemotherapy as the neoadjuvant chemotherapy regimen (HR, 0.59; 95 % CI, 0.46 to 0.76; P < 0.01) but were not significant in the studies that used fluoropyrimidine monotherapy (HR, 0.93; 95 % CI, 0.56 to 1.55; P = 0.84). Furthermore, the two groups showed no significant differences in the post-operative complication rates (relative risk, 0.98; 95 % CI, 0.63 to 1.51; P = 0.91) or adverse effects of chemotherapy (P > 0.05 for all adverse effects).

Conclusion

Perioperative chemotherapy showed improved survival compared to adjuvant chemotherapy for gastric cancer. In addition, combination chemotherapy resulted in better survival compared to monotherapy in the neoadjuvant chemotherapy regimens.
Appendix
Available only for authorised users
Literature
1.
go back to reference Jemal A, Bray F, Center MM, Ferlay J, Ward E, Forman D. Global cancer statistics. CA Cancer J Clin. 2011;61(2):69–90.CrossRefPubMed Jemal A, Bray F, Center MM, Ferlay J, Ward E, Forman D. Global cancer statistics. CA Cancer J Clin. 2011;61(2):69–90.CrossRefPubMed
2.
go back to reference Herszenyi L, Tulassay Z. Epidemiology of gastrointestinal and liver tumors. Eur Rev Med Pharmacol Sci. 2010;14(4):249–58.PubMed Herszenyi L, Tulassay Z. Epidemiology of gastrointestinal and liver tumors. Eur Rev Med Pharmacol Sci. 2010;14(4):249–58.PubMed
3.
go back to reference Sant M, Allemani C, Santaquilani M, Knijn A, Marchesi F, Capocaccia R, Group EW. EUROCARE-4. Survival of cancer patients diagnosed in 1995–1999. Results and commentary. Eur J Cancer. 2009;45(6):931–91.CrossRefPubMed Sant M, Allemani C, Santaquilani M, Knijn A, Marchesi F, Capocaccia R, Group EW. EUROCARE-4. Survival of cancer patients diagnosed in 1995–1999. Results and commentary. Eur J Cancer. 2009;45(6):931–91.CrossRefPubMed
4.
go back to reference Cunningham D, Allum WH, Stenning SP, Thompson JN, Van de Velde CJ, Nicolson M, Scarffe JH, Lofts FJ, Falk SJ, Iveson TJ, et al. Perioperative chemotherapy versus surgery alone for resectable gastroesophageal cancer. N Engl J Med. 2006;355(1):11–20.CrossRefPubMed Cunningham D, Allum WH, Stenning SP, Thompson JN, Van de Velde CJ, Nicolson M, Scarffe JH, Lofts FJ, Falk SJ, Iveson TJ, et al. Perioperative chemotherapy versus surgery alone for resectable gastroesophageal cancer. N Engl J Med. 2006;355(1):11–20.CrossRefPubMed
5.
go back to reference Bang YJ, Kim YW, Yang HK, Chung HC, Park YK, Lee KH, Lee KW, Kim YH, Noh SI, Cho JY, et al. Adjuvant capecitabine and oxaliplatin for gastric cancer after D2 gastrectomy (CLASSIC): a phase 3 open-label, randomised controlled trial. Lancet. 2012;379(9813):315–21.CrossRefPubMed Bang YJ, Kim YW, Yang HK, Chung HC, Park YK, Lee KH, Lee KW, Kim YH, Noh SI, Cho JY, et al. Adjuvant capecitabine and oxaliplatin for gastric cancer after D2 gastrectomy (CLASSIC): a phase 3 open-label, randomised controlled trial. Lancet. 2012;379(9813):315–21.CrossRefPubMed
7.
8.
go back to reference Frei 3rd E, Miller D, Clark JR, Fallon BG, Ervin TJ. Clinical and scientific considerations in preoperative (neoadjuvant) chemotherapy. Recent Results Cancer Res. 1986;103:1–5.CrossRefPubMed Frei 3rd E, Miller D, Clark JR, Fallon BG, Ervin TJ. Clinical and scientific considerations in preoperative (neoadjuvant) chemotherapy. Recent Results Cancer Res. 1986;103:1–5.CrossRefPubMed
9.
go back to reference Li ZY, Koh CE, Bu ZD, Wu AW, Zhang LH, Wu XJ, Wu Q, Zong XL, Ren H, Tang L, et al. Neoadjuvant chemotherapy with FOLFOX: improved outcomes in Chinese patients with locally advanced gastric cancer. J Surg Oncol. 2012;105(8):793–9.CrossRefPubMed Li ZY, Koh CE, Bu ZD, Wu AW, Zhang LH, Wu XJ, Wu Q, Zong XL, Ren H, Tang L, et al. Neoadjuvant chemotherapy with FOLFOX: improved outcomes in Chinese patients with locally advanced gastric cancer. J Surg Oncol. 2012;105(8):793–9.CrossRefPubMed
10.
go back to reference Yang Y, Yin X, Sheng L, Xu S, Dong L, Liu L. Perioperative chemotherapy more of a benefit for overall survival than adjuvant chemotherapy for operable gastric cancer: an updated Meta-analysis. Sci Reports. 2015;5:12850.CrossRef Yang Y, Yin X, Sheng L, Xu S, Dong L, Liu L. Perioperative chemotherapy more of a benefit for overall survival than adjuvant chemotherapy for operable gastric cancer: an updated Meta-analysis. Sci Reports. 2015;5:12850.CrossRef
11.
go back to reference Feng D, Leong M, Li T, Chen L, Li T. Surgical outcomes in patients with locally advanced gastric cancer treated with S-1 and oxaliplatin as neoadjuvant chemotherapy. World J Surg Oncol. 2015;13:11.CrossRefPubMedPubMedCentral Feng D, Leong M, Li T, Chen L, Li T. Surgical outcomes in patients with locally advanced gastric cancer treated with S-1 and oxaliplatin as neoadjuvant chemotherapy. World J Surg Oncol. 2015;13:11.CrossRefPubMedPubMedCentral
12.
go back to reference Fujiwara Y, Takiguchi S, Nakajima K, Miyata H, Yamasaki M, Kurokawa Y, Okada K, Mori M, Doki Y. Neoadjuvant intraperitoneal and systemic chemotherapy for gastric cancer patients with peritoneal dissemination. Ann Surg Oncol. 2011;18(13):3726–31.CrossRefPubMed Fujiwara Y, Takiguchi S, Nakajima K, Miyata H, Yamasaki M, Kurokawa Y, Okada K, Mori M, Doki Y. Neoadjuvant intraperitoneal and systemic chemotherapy for gastric cancer patients with peritoneal dissemination. Ann Surg Oncol. 2011;18(13):3726–31.CrossRefPubMed
13.
go back to reference Macdonald JS, Smalley SR, Benedetti J, Hundahl SA, Estes NC, Stemmermann GN, Haller DG, Ajani JA, Gunderson LL, Jessup JM, et al. Chemoradiotherapy after surgery compared with surgery alone for adenocarcinoma of the stomach or gastroesophageal junction. N Engl J Med. 2001;345(10):725–30.CrossRefPubMed Macdonald JS, Smalley SR, Benedetti J, Hundahl SA, Estes NC, Stemmermann GN, Haller DG, Ajani JA, Gunderson LL, Jessup JM, et al. Chemoradiotherapy after surgery compared with surgery alone for adenocarcinoma of the stomach or gastroesophageal junction. N Engl J Med. 2001;345(10):725–30.CrossRefPubMed
14.
go back to reference Grobmyer SR, Pieracci FM, Allen PJ, Brennan MF, Jaques DP. Defining morbidity after pancreaticoduodenectomy: use of a prospective complication grading system. J Am Coll Surg. 2007;204(3):356–64.CrossRefPubMed Grobmyer SR, Pieracci FM, Allen PJ, Brennan MF, Jaques DP. Defining morbidity after pancreaticoduodenectomy: use of a prospective complication grading system. J Am Coll Surg. 2007;204(3):356–64.CrossRefPubMed
15.
go back to reference Stang A. Critical evaluation of the Newcastle-Ottawa scale for the assessment of the quality of nonrandomized studies in meta-analyses. Eur J Epidemiol. 2010;25(9):603–5.CrossRefPubMed Stang A. Critical evaluation of the Newcastle-Ottawa scale for the assessment of the quality of nonrandomized studies in meta-analyses. Eur J Epidemiol. 2010;25(9):603–5.CrossRefPubMed
16.
go back to reference Tierney JF, Stewart LA, Ghersi D, Burdett S, Sydes MR. Practical methods for incorporating summary time-to-event data into meta-analysis. Trials. 2007;8:16.CrossRefPubMedPubMedCentral Tierney JF, Stewart LA, Ghersi D, Burdett S, Sydes MR. Practical methods for incorporating summary time-to-event data into meta-analysis. Trials. 2007;8:16.CrossRefPubMedPubMedCentral
17.
go back to reference Yonemura Y, Sawa T, Kinoshita K, Matsuki N, Fushida S, Tanaka S, Ohoyama S, Takashima T, Kimura H, Kamata T, et al. Neoadjuvant chemotherapy for high-grade advanced gastric cancer. World J Surg. 1993;17(2):256–61. discussion 261–252.CrossRefPubMed Yonemura Y, Sawa T, Kinoshita K, Matsuki N, Fushida S, Tanaka S, Ohoyama S, Takashima T, Kimura H, Kamata T, et al. Neoadjuvant chemotherapy for high-grade advanced gastric cancer. World J Surg. 1993;17(2):256–61. discussion 261–252.CrossRefPubMed
18.
go back to reference Sun XC, Lin J, Ju AH. Treatment of Borrmann type IV gastric cancer with a neoadjuvant chemotherapy combination of docetaxel, cisplatin and 5-fluorouracil/leucovorin. J Int Med Res. 2011;39(6):2096–102.CrossRefPubMed Sun XC, Lin J, Ju AH. Treatment of Borrmann type IV gastric cancer with a neoadjuvant chemotherapy combination of docetaxel, cisplatin and 5-fluorouracil/leucovorin. J Int Med Res. 2011;39(6):2096–102.CrossRefPubMed
19.
go back to reference Qu JJ, Shi YR, Liu FR, Ma SQ, Ma FY. A clinical study of paclitaxel combined with FOLFOX4 regimen as neoadjuvant chemotherapy for advanced gastric cancer. Chin J Gastrointestinal Surg. 2010;13(9):664–7. Qu JJ, Shi YR, Liu FR, Ma SQ, Ma FY. A clinical study of paclitaxel combined with FOLFOX4 regimen as neoadjuvant chemotherapy for advanced gastric cancer. Chin J Gastrointestinal Surg. 2010;13(9):664–7.
20.
go back to reference Nio Y, Koike M, Omori H, Hashimoto K, Itakura M, Yano S, Higami T, Maruyama R. A randomized consent design trial of neoadjuvant chemotherapy with tegafur plus uracil (UFT) for gastric cancer--a single institute study. Anticancer Res. 2004;24(3b):1879–87.PubMed Nio Y, Koike M, Omori H, Hashimoto K, Itakura M, Yano S, Higami T, Maruyama R. A randomized consent design trial of neoadjuvant chemotherapy with tegafur plus uracil (UFT) for gastric cancer--a single institute study. Anticancer Res. 2004;24(3b):1879–87.PubMed
21.
go back to reference Kobayashi T, Kimura T. Long-term outcome of preoperative chemotherapy with 5′-deoxy-5-fluorouridine (5′-DFUR) for gastric cancer. Gan Kagaku ryoho Cancer Chemotherapy. 2000;27(10):1521–6.PubMed Kobayashi T, Kimura T. Long-term outcome of preoperative chemotherapy with 5′-deoxy-5-fluorouridine (5′-DFUR) for gastric cancer. Gan Kagaku ryoho Cancer Chemotherapy. 2000;27(10):1521–6.PubMed
22.
go back to reference Zhang J, Chen RX, Zhang J, Cai J, Meng H, Wu GC, Zhang ZT, Wang Y, Wang KL. Efficacy and safety of neoadjuvant chemotherapy with modified FOLFOX7 regimen on the treatment of advanced gastric cancer. Chin Med J. 2012;125(12):2144–50.PubMed Zhang J, Chen RX, Zhang J, Cai J, Meng H, Wu GC, Zhang ZT, Wang Y, Wang KL. Efficacy and safety of neoadjuvant chemotherapy with modified FOLFOX7 regimen on the treatment of advanced gastric cancer. Chin Med J. 2012;125(12):2144–50.PubMed
23.
go back to reference Zhang CW, Zou SC, Shi D, Zhao DJ. Clinical significance of preoperative regional intra-arterial infusion chemotherapy for advanced gastric cancer. World J Gastroenterol. 2004;10(20):3070–2.CrossRefPubMedPubMedCentral Zhang CW, Zou SC, Shi D, Zhao DJ. Clinical significance of preoperative regional intra-arterial infusion chemotherapy for advanced gastric cancer. World J Gastroenterol. 2004;10(20):3070–2.CrossRefPubMedPubMedCentral
24.
go back to reference Sun Z, Zhu RJ, Yang GF, Li Y. Neoadjuvant chemotherapy with FOLFOX4 regimen to treat advanced gastric cancer improves survival without increasing adverse events: a retrospective cohort study from a Chinese center. Sci World J. 2014;2014:418694. Sun Z, Zhu RJ, Yang GF, Li Y. Neoadjuvant chemotherapy with FOLFOX4 regimen to treat advanced gastric cancer improves survival without increasing adverse events: a retrospective cohort study from a Chinese center. Sci World J. 2014;2014:418694.
25.
go back to reference Nishioka B, Ouchi T, Watanabe S, Umehara M, Yamane E, Yahata K, Muto F, Kojima O, Nomiyama S, Sakita M, et al. Follow-up study of preoperative oral administration of an antineoplastic agent as an adjuvant chemotherapy in stomach cancer. Gan Kagaku ryoho Cancer Chemotherapy. 1982;9(8):1427–32.PubMed Nishioka B, Ouchi T, Watanabe S, Umehara M, Yamane E, Yahata K, Muto F, Kojima O, Nomiyama S, Sakita M, et al. Follow-up study of preoperative oral administration of an antineoplastic agent as an adjuvant chemotherapy in stomach cancer. Gan Kagaku ryoho Cancer Chemotherapy. 1982;9(8):1427–32.PubMed
26.
go back to reference Fukushima M, Satake H, Uchida J, Shimamoto Y, Kato T, Takechi T, Okabe H, Fujioka A, Nakano K, Ohshimo H, et al. Preclinical antitumor efficacy of S-1: a new oral formulation of 5-fluorouracil on human tumor xenografts. Int J Oncol. 1998;13(4):693–8.PubMed Fukushima M, Satake H, Uchida J, Shimamoto Y, Kato T, Takechi T, Okabe H, Fujioka A, Nakano K, Ohshimo H, et al. Preclinical antitumor efficacy of S-1: a new oral formulation of 5-fluorouracil on human tumor xenografts. Int J Oncol. 1998;13(4):693–8.PubMed
27.
go back to reference Schoffski P. The modulated oral fluoropyrimidine prodrug S-1, and its use in gastrointestinal cancer and other solid tumors. Anti-Cancer Drugs. 2004;15(2):85–106.CrossRefPubMed Schoffski P. The modulated oral fluoropyrimidine prodrug S-1, and its use in gastrointestinal cancer and other solid tumors. Anti-Cancer Drugs. 2004;15(2):85–106.CrossRefPubMed
28.
29.
go back to reference Iacovelli R, Pietrantonio F, Maggi C, de Braud F, Di Bartolomeo M. Combination or single-agent chemotherapy as adjuvant treatment of gastric cancer: A systematic review and meta-analysis of published trials. Crit Rev Oncol/Hematol. 2015;98:24–8.CrossRef Iacovelli R, Pietrantonio F, Maggi C, de Braud F, Di Bartolomeo M. Combination or single-agent chemotherapy as adjuvant treatment of gastric cancer: A systematic review and meta-analysis of published trials. Crit Rev Oncol/Hematol. 2015;98:24–8.CrossRef
30.
go back to reference Koizumi W, Narahara H, Hara T, Takagane A, Akiya T, Takagi M, Miyashita K, Nishizaki T, Kobayashi O, Takiyama W, et al. S-1 plus cisplatin versus S-1 alone for first-line treatment of advanced gastric cancer (SPIRITS trial): a phase III trial. Lancet Oncol. 2008;9(3):215–21.CrossRefPubMed Koizumi W, Narahara H, Hara T, Takagane A, Akiya T, Takagi M, Miyashita K, Nishizaki T, Kobayashi O, Takiyama W, et al. S-1 plus cisplatin versus S-1 alone for first-line treatment of advanced gastric cancer (SPIRITS trial): a phase III trial. Lancet Oncol. 2008;9(3):215–21.CrossRefPubMed
31.
go back to reference Ajani JA, Moiseyenko VM, Tjulandin S, Majlis A, Constenla M, Boni C, Rodrigues A, Fodor M, Chao Y, Voznyi E, et al. Clinical benefit with docetaxel plus fluorouracil and cisplatin compared with cisplatin and fluorouracil in a phase III trial of advanced gastric or gastroesophageal cancer adenocarcinoma: the V-325 Study Group. J Clin Oncol. 2007;25(22):3205–9.CrossRefPubMed Ajani JA, Moiseyenko VM, Tjulandin S, Majlis A, Constenla M, Boni C, Rodrigues A, Fodor M, Chao Y, Voznyi E, et al. Clinical benefit with docetaxel plus fluorouracil and cisplatin compared with cisplatin and fluorouracil in a phase III trial of advanced gastric or gastroesophageal cancer adenocarcinoma: the V-325 Study Group. J Clin Oncol. 2007;25(22):3205–9.CrossRefPubMed
32.
go back to reference Ychou M, Boige V, Pignon JP, Conroy T, Bouche O, Lebreton G, Ducourtieux M, Bedenne L, Fabre JM, Saint-Aubert B, et al. Perioperative chemotherapy compared with surgery alone for resectable gastroesophageal adenocarcinoma: an FNCLCC and FFCD multicenter phase III trial. J Clin Oncol. 2011;29(13):1715–21.CrossRefPubMed Ychou M, Boige V, Pignon JP, Conroy T, Bouche O, Lebreton G, Ducourtieux M, Bedenne L, Fabre JM, Saint-Aubert B, et al. Perioperative chemotherapy compared with surgery alone for resectable gastroesophageal adenocarcinoma: an FNCLCC and FFCD multicenter phase III trial. J Clin Oncol. 2011;29(13):1715–21.CrossRefPubMed
33.
go back to reference Friedman MA, Ogawa M, Carter SK, Sakurai Y, Kimura K, Hannigan J. Chemotherapy of disseminated gastric cancer. A joint effort of the Northern California Oncology Group and the Japanese Gastric Cancer Chemotherapy Group. Cancer. 1983;52(10):1771–7.CrossRefPubMed Friedman MA, Ogawa M, Carter SK, Sakurai Y, Kimura K, Hannigan J. Chemotherapy of disseminated gastric cancer. A joint effort of the Northern California Oncology Group and the Japanese Gastric Cancer Chemotherapy Group. Cancer. 1983;52(10):1771–7.CrossRefPubMed
34.
go back to reference Xu AM, Huang L, Liu W, Gao S, Han WX, Wei ZJ. Neoadjuvant chemotherapy followed by surgery versus surgery alone for gastric carcinoma: systematic review and meta-analysis of randomized controlled trials. PLoS One. 2014;9(1):e86941.CrossRefPubMedPubMedCentral Xu AM, Huang L, Liu W, Gao S, Han WX, Wei ZJ. Neoadjuvant chemotherapy followed by surgery versus surgery alone for gastric carcinoma: systematic review and meta-analysis of randomized controlled trials. PLoS One. 2014;9(1):e86941.CrossRefPubMedPubMedCentral
35.
go back to reference Xiong BH, Cheng Y, Ma L, Zhang CQ. An updated meta-analysis of randomized controlled trial assessing the effect of neoadjuvant chemotherapy in advanced gastric cancer. Cancer Investig. 2014;32(6):272–84.CrossRef Xiong BH, Cheng Y, Ma L, Zhang CQ. An updated meta-analysis of randomized controlled trial assessing the effect of neoadjuvant chemotherapy in advanced gastric cancer. Cancer Investig. 2014;32(6):272–84.CrossRef
36.
Metadata
Title
Which is better for gastric cancer patients, perioperative or adjuvant chemotherapy: a meta-analysis
Authors
Jun-hua Zhao
Peng Gao
Yong-xi Song
Jing-xu Sun
Xiao-wan Chen
Bin Ma
Yu-chong Yang
Zhen-ning Wang
Publication date
01-12-2016
Publisher
BioMed Central
Published in
BMC Cancer / Issue 1/2016
Electronic ISSN: 1471-2407
DOI
https://doi.org/10.1186/s12885-016-2667-5

Other articles of this Issue 1/2016

BMC Cancer 1/2016 Go to the issue
Webinar | 19-02-2024 | 17:30 (CET)

Keynote webinar | Spotlight on antibody–drug conjugates in cancer

Antibody–drug conjugates (ADCs) are novel agents that have shown promise across multiple tumor types. Explore the current landscape of ADCs in breast and lung cancer with our experts, and gain insights into the mechanism of action, key clinical trials data, existing challenges, and future directions.

Dr. Véronique Diéras
Prof. Fabrice Barlesi
Developed by: Springer Medicine