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Anti-Cancer Agents in Medicinal Chemistry

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ISSN (Print): 1871-5206
ISSN (Online): 1875-5992

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Systematic Review Article

Long-Term Outcomes of Neoadjuvant Chemotherapy in Locally Advanced Gastric Cancer/Esophagogastric Junction Cancer: A Systematic Review and Meta-Analysis

Author(s): Feng Wu, Jiaze Hong, Nannan Du, Yiran Wang, Juan Chen, Yuanfang He and Ping Chen*

Volume 22, Issue 1, 2022

Published on: 15 March, 2021

Page: [143 - 151] Pages: 9

DOI: 10.2174/1871520621666210315091932

Price: $65

Abstract

Background: Neoadjuvant chemotherapy (NAC) has been defined as any preoperative chemotherapy scheme aiming to reduce tumor staging and to control preoperative micrometastasis, which has been extensively used as a treatment for resectable gastric cancer. However, its effect on the long-term survival of patients with locally advanced gastric cancer (AGC) or esophagogastric junction cancer (EGC) remains unknown.

Objective: This study aimed at investigating the long-term efficacy of NAC in locally AGC/EGC.

Methods: The following databases were searched for articles published from their inception to April 2020: PubMed, Web of Science, EBSCO, and Cochrane library. The primary outcomes were overall survival (OS) and progression-free survival (PFS).

Results: A total of 19 articles were included in this meta-analysis, with a total of 4,446 patients. The results showed that NAC increased the patients’ 3-year OS (HR: 0.56, 95% CI, 0.21 - 0.91, p < 0.001), 3-year PFS (HR: 0.76, 95% CI, 0.66 - 0.87, p < 0.001), 5-year OS (HR: 0.71, 95% CI, 0.64 - 0.78, p < 0.001), and 5-year PFS (HR: 0.70, 95% CI, 0.61 - 0.79, p < 0.001). Besides, subgroup analysis showed that Asian countries have benefited significantly from NAC (HR: 0.65, 95% CI, 0.55 - 0.74, p < 0.001), and other countries have also benefited (HR: 0.79, 95% CI, 0.68 - 0.89, p < 0.001).

Conclusion: Compared with adjuvant chemotherapy and surgery alone, NAC can improve the long-term survival outcomes (OS and PFS) of patients with resectable AGC or EGC.

Keywords: Neoadjuvant chemotherapy, advanced gastric cancer, esophagogastric junction cancer, long-term survival, meta-analysis, progression-free survival.

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[1]
Kawazoe, A.; Fukuoka, S.; Nakamura, Y.; Kuboki, Y.; Wakabayashi, M.; Nomura, S.; Mikamoto, Y.; Shima, H.; Fujishiro, N.; Higuchi, T.; Sato, A.; Kuwata, T.; Shitara, K. Lenvatinib plus pembrolizumab in patients with advanced gastric cancer in the first-line or second-line setting (EPOC1706): an open-label, single-arm, phase 2 trial. Lancet Oncol., 2020, 21(8), 1057-1065.
[http://dx.doi.org/10.1016/S1470-2045(20)30271-0] [PMID: 32589866]
[2]
Allemani, C.; Matsuda, T.; Di Carlo, V.; Harewood, R.; Matz, M.; Nikšić, M.; Bonaventure, A.; Valkov, M.; Johnson, C.J.; Estève, J.; Ogunbiyi, O.J.; Azevedo, E. Silva, G.; Chen, W.Q.; Eser, S.; Engholm, G.; Stiller, C.A.; Monnereau, A.; Woods, R.R.; Visser, O.; Lim, G.H.; Aitken, J.; Weir, H.K.; Coleman, M.P. CONCORD Working Group. Global surveillance of trends in cancer survival 2000-14 (CONCORD-3): analysis of individual records for 37 513 025 patients diagnosed with one of 18 cancers from 322 population-based registries in 71 countries. Lancet, 2018, 391(10125), 1023-1075.
[http://dx.doi.org/10.1016/S0140-6736(17)33326-3] [PMID: 29395269]
[3]
Wang, K.; Ren, Y.; Ma, Z.; Li, F.; Cheng, X.; Xiao, J.; Zhang, S.; Yu, Z.; Yang, H.; Zhou, H.; Li, Y.; Liu, H.; Jiao, Z.Y. Docetaxel, oxaliplatin, leucovorin, and 5-fluorouracil (FLOT) as preoperative and postoperative chemotherapy compared with surgery followed by chemotherapy for patients with locally advanced gastric cancer: a propensity score-based analysis. Cancer Manag. Res., 2019, 11, 3009-3020.
[http://dx.doi.org/10.2147/CMAR.S200883] [PMID: 31114348]
[4]
Gee, D.W.; Rattner, D.W. Management of gastroesophageal tumors. Oncologist, 2007, 12(2), 175-185.
[http://dx.doi.org/10.1634/theoncologist.12-2-175] [PMID: 17296813]
[5]
Yoshida, K.; Kodera, Y.; Kochi, M.; Ichikawa, W.; Kakeji, Y.; Sano, T.; Nagao, N.; Takahashi, M.; Takagane, A.; Watanabe, T.; Kaji, M.; Okitsu, H.; Nomura, T.; Matsui, T.; Yoshikawa, T.; Matsuyama, J.; Yamada, M.; Ito, S.; Takeuchi, M.; Fujii, M. Addition of Docetaxel to Oral Fluoropyrimidine Improves Efficacy in Patients With Stage III Gastric Cancer: Interim Analysis of JACCRO GC-07, a Randomized Controlled Trial. J. Clin. Oncol., 2019, 37(15), 1296-1304.
[http://dx.doi.org/10.1200/JCO.18.01138] [PMID: 30925125]
[6]
Miao, Z.F.; Liu, X.Y.; Wang, Z.N.; Zhao, T.T.; Xu, Y.Y.; Song, Y.X.; Huang, J.Y.; Xu, H.; Xu, H.M. Effect of neoadjuvant chemotherapy in patients with gastric cancer: a PRISMA-compliant systematic review and meta-analysis. BMC Cancer, 2018, 18(1), 118.
[http://dx.doi.org/10.1186/s12885-018-4027-0] [PMID: 29385994]
[7]
Yu, J.; Huang, C.; Sun, Y.; Su, X.; Cao, H.; Hu, J.; Wang, K.; Suo, J.; Tao, K.; He, X.; Wei, H.; Ying, M.; Hu, W.; Du, X.; Hu, Y.; Liu, H.; Zheng, C.; Li, P.; Xie, J.; Liu, F.; Li, Z.; Zhao, G.; Yang, K.; Liu, C.; Li, H.; Chen, P.; Ji, J.; Li, G. Chinese Laparoscopic Gastrointestinal Surgery Study (CLASS) Group. Effect of Laparoscopic vs Open Distal Gastrectomy on 3-Year Disease-Free Survival in Patients With Locally Advanced Gastric Cancer: The CLASS-01 Randomized Clinical Trial. JAMA, 2019, 321(20), 1983-1992.
[http://dx.doi.org/10.1001/jama.2019.5359] [PMID: 31135850]
[8]
Coccolini, F.; Nardi, M.; Montori, G.; Ceresoli, M.; Celotti, A.; Cascinu, S.; Fugazzola, P.; Tomasoni, M.; Glehen, O.; Catena, F.; Yonemura, Y.; Ansaloni, L. Neoadjuvant chemotherapy in advanced gastric and esophago-gastric cancer. Meta-analysis of randomized trials. Int. J. Surg., 2018, 51, 120-127.
[http://dx.doi.org/10.1016/j.ijsu.2018.01.008] [PMID: 29413875]
[9]
Cunningham, D.; Allum, W.H.; Stenning, S.P.; Thompson, J.N.; Van de Velde, C.J.; Nicolson, M.; Scarffe, J.H.; Lofts, F.J.; Falk, S.J.; Iveson, T.J.; Smith, D.B.; Langley, R.E.; Verma, M.; Weeden, S.; Chua, Y.J. MAGIC Trial Participants. Perioperative chemotherapy versus surgery alone for resectable gastroesophageal cancer. N. Engl. J. Med., 2006, 355(1), 11-20.
[http://dx.doi.org/10.1056/NEJMoa055531] [PMID: 16822992]
[10]
Li, Z. Shan, F.; Ying, X.; Zhang, Y.; e, J.Y.; Wang, Y.; Ren, H.; Su, X.; Ji, J. Assessment of Laparoscopic Distal Gastrectomy After Neoadjuvant Chemotherapy for Locally Advanced Gastric Cancer: A Randomized Clinical Trial. JAMA Surg., 2019, 154(12), 1093-1101.
[http://dx.doi.org/10.1001/jamasurg.2019.3473] [PMID: 31553463]
[11]
Zhao, Q.; Li, Y.; Huang, J.; Fan, L.; Tan, B.; Tian, Y.; Yang, P.; Jiao, Z.; Zhao, X.; Zhang, Z.; Wang, D.; Liu, Y. Short-term curative effect of S-1 plus oxaliplatin as perioperative chemotherapy for locally advanced gastric cancer: a prospective comparison study. Pharmazie, 2017, 72(4), 236-240.
[PMID: 29441995]
[12]
Luo, H.; Wu, L.; Huang, M.; Jin, Q.; Qin, Y.; Chen, J. Postoperative morbidity and mortality in patients receiving neoadjuvant chemotherapy for locally advanced gastric cancers: A systematic review and meta-analysis. Medicine (Baltimore), 2018, 97(43)e12932
[http://dx.doi.org/10.1097/MD.0000000000012932] [PMID: 30412102]
[13]
Zhao, J.H.; Gao, P.; Song, Y.X.; Sun, J.X.; Chen, X.W.; Ma, B.; Yang, Y.C.; Wang, Z.N. Which is better for gastric cancer patients, perioperative or adjuvant chemotherapy: a meta-analysis. BMC Cancer, 2016, 16, 631.
[http://dx.doi.org/10.1186/s12885-016-2667-5] [PMID: 27519527]
[14]
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. Rep., 2015, 5, 12850.
[http://dx.doi.org/10.1038/srep12850] [PMID: 26242393]
[15]
Biondi, A.; Agnes, A.; Del Coco, F.; Pozzo, C.; Strippoli, A.; D’Ugo, D.; Persiani, R. Preoperative therapy and long-term survival in gastric cancer: One size does not fit all. Surg. Oncol., 2018, 27(3), 575-583.
[http://dx.doi.org/10.1016/j.suronc.2018.07.006] [PMID: 30217321]
[16]
Parry, K.; van Rossum, P.S.; Haj Mohammad, N.; Ruurda, J.P.; van Hillegersberg, R. The effect of perioperative chemotherapy for patients with an adenocarcinoma of the gastroesophageal junction: A propensity score matched analysis. Eur. J. Surg. Oncol., 2017, 43(1), 226-233.
[http://dx.doi.org/10.1016/j.ejso.2016.06.393] [PMID: 27424786]
[17]
Moher, D.; Shamseer, L.; Clarke, M.; Ghersi, D.; Liberati, A.; Petticrew, M.; Shekelle, P.; Stewart, L.A. PRISMA-P Group. Preferred reporting items for systematic review and meta-analysis protocols (PRISMA-P) 2015 statement. Syst. Rev., 2015, 4(1), 1.
[http://dx.doi.org/10.1186/2046-4053-4-1] [PMID: 25554246]
[18]
Parmar, M.K.; Torri, V.; Stewart, L. Extracting summary statistics to perform meta-analyses of the published literature for survival endpoints. Stat. Med., 1998, 17(24), 2815-2834.
[http://dx.doi.org/10.1002/(SICI)1097-0258(19981230)17:24<2815:AID-SIM110>3.0.CO;2-8] [PMID: 9921604]
[19]
Gu, L.; Chen, M.; Khadaroo, P.A.; Ma, X.; Kong, L.; Li, X.; Zhu, H.; Zhong, X.; Pan, J.; Wang, X. A Risk-Scoring Model for Predicting Lymph Node Metastasis in Early Gastric Cancer Patients: a Retrospective Study and External Validation. J. Gastrointest. Surg., 2018, 22(9), 1508-1515.
[http://dx.doi.org/10.1007/s11605-018-3816-8] [PMID: 29845571]
[20]
Kuhnle, P.J.; Israel, K.F.; Menges, M. Real-life data on improvement of survival after perioperative chemotherapy versus surgery alone on resectable adenocarcinoma of the stomach - a single-center study. Z. Gastroenterol., 2019, 57(5), 606-610.
[http://dx.doi.org/10.1055/a-0841-3513] [PMID: 31083749]
[21]
Kano, M.; Hayano, K.; Hayashi, H.; Hanari, N.; Gunji, H.; Toyozumi, T.; Murakami, K.; Uesato, M.; Ota, S.; Matsubara, H. Survival Benefit of Neoadjuvant Chemotherapy with S-1 Plus Docetaxel for Locally Advanced Gastric Cancer: A Propensity Score-Matched Analysis. Ann. Surg. Oncol., 2019, 26(6), 1805-1813.
[http://dx.doi.org/10.1245/s10434-019-07299-7] [PMID: 30977014]
[22]
Xue, K.; Ying, X.; Bu, Z.; Wu, A.; Li, Z.; Tang, L.; Zhang, L.; Zhang, Y.; Li, Z.; Ji, J. Oxaliplatin plus S-1 or capecitabine as neoadjuvant or adjuvant chemotherapy for locally advanced gastric cancer with D2 lymphadenectomy: 5-year follow-up results of a phase II-III randomized trial. Chin. J. Cancer Res., 2018, 30(5), 516-525.
[http://dx.doi.org/10.21147/j.issn.1000-9604.2018.05.05] [PMID: 30510363]
[23]
Yang, B.; Shi, C.; Lin, X.; Wang, X.; Chen, Q. Retrospective study on efficacy of a paclitaxel combined with a leucovorin and fluorouracil regimen for advanced gastric cancer. Tumori, 2019, 105(6), 509-515.
[http://dx.doi.org/10.1177/0300891618792481] [PMID: 30157713]
[24]
Gabriel, E.; Attwood, K.; Narayanan, S.; Brady, M.; Nurkin, S.; Hochwald, S.; Kukar, M. Does neoadjuvant/perioperative chemotherapy improve overall survival for T2N0 gastric adenocarcinoma? J. Surg. Oncol., 2018, 117(4), 659-670.
[http://dx.doi.org/10.1002/jso.24894] [PMID: 29127704]
[25]
Fiteni, F.; Paget-Bailly, S.; Messager, M.; N’Guyen, T.; Lakkis, Z.; Mathieu, P.; Lamfichekh, N.; Picard, A.; Benzidane, B.; Cléau, D.; Bonnetain, F.; Borg, C.; Mariette, C.; Kim, S. Docetaxel, Cisplatin, and 5-Fluorouracil as perioperative chemotherapy compared with surgery alone for resectable gastroesophageal adenocarcinoma. Cancer Med., 2016, 5(11), 3085-3093.
[http://dx.doi.org/10.1002/cam4.885] [PMID: 27726290]
[26]
Fazio, N.; Biffi, R.; Maibach, R.; Hayoz, S.; Thierstein, S.; Brauchli, P.; Bernhard, J.; Stupp, R.; Andreoni, B.; Renne, G.; Crosta, C.; Morant, R.; Chiappa, A.; Luca, F.; Zampino, M.G.; Huber, O.; Goldhirsch, A.; de Braud, F.; Roth, A.D. Swiss Group for Clinical Cancer Research SAKK; European Institute of Oncology, Milan, Italy. Preoperative versus postoperative docetaxel-cisplatin-fluorouracil (TCF) chemotherapy in locally advanced resectable gastric carcinoma: 10-year follow-up of the SAKK 43/99 phase III trial. Ann. Oncol., 2016, 27(4), 668-673.
[http://dx.doi.org/10.1093/annonc/mdv620] [PMID: 26712905]
[27]
Tian, S.B.; Yu, J.C.; Kang, W.M.; Ma, Z.Q.; Ye, X.; Yan, C.; Huang, Y.K. Effect of Neoadjuvant Chemotherapy Treatment on Prognosis of Patients with Advanced Gastric Cancer: a Retrospective Study. Chin. Med. Sci. J., 2015, 30(2), 84-89.
[http://dx.doi.org/10.1016/S1001-9294(15)30017-1] [PMID: 26148998]
[28]
Zheng, C.H.; Lu, J.; Huang, C.M.; Li, P.; Xie, J.W.; Wang, J.B.; Lin, J.X. Treatment of locally advanced gastric cancer with the XELOX program of neoadjuvantchemotherapy combined with laparoscopic surgery: the experience in China. Hepatogastroenterology, 2014, 61(135), 1876-1882.
[PMID: 25713882]
[29]
Sun, Z.; Zhu, R.J.; Yang, G.F.; 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. ScientificWorldJournal, 2014, 2014418694
[http://dx.doi.org/10.1155/2014/418694] [PMID: 25136668]
[30]
Ruf, C.; Thomusch, O.; Goos, M.; Makowiec, F.; Illerhaus, G.; Ruf, G. Impact of neoadjuvant chemotherapy with PELF-protocoll versus surgery alone in the treatment of advanced gastric carcinoma. BMC Surg., 2014, 14, 5.
[http://dx.doi.org/10.1186/1471-2482-14-5] [PMID: 24461063]
[31]
Ychou, M.; Boige, V.; Pignon, J.P.; Conroy, T.; Bouché, O.; Lebreton, G.; Ducourtieux, M.; Bedenne, L.; Fabre, J.M.; Saint-Aubert, B.; Genève, J.; Lasser, P.; Rougier, P. Perioperative chemotherapy compared with surgery alone for resectable gastroesophageal adenocarcinoma: an FNCLCC and FFCD multicenter phase III trial. J. Clin. Oncol., 2011, 29(13), 1715-1721.
[http://dx.doi.org/10.1200/JCO.2010.33.0597] [PMID: 21444866]
[32]
Schuhmacher, C.; Gretschel, S.; Lordick, F.; Reichardt, P.; Hohenberger, W.; Eisenberger, C.F.; Haag, C.; Mauer, M.E.; Hasan, B.; Welch, J.; Ott, K.; Hoelscher, A.; Schneider, P.M.; Bechstein, W.; Wilke, H.; Lutz, M.P.; Nordlinger, B.; Van Cutsem, E.; Siewert, J.R.; Schlag, P.M. Neoadjuvant chemotherapy compared with surgery alone for locally advanced cancer of the stomach and cardia: European Organisation for Research and Treatment of Cancer randomized trial 40954. J. Clin. Oncol., 2010, 28(35), 5210-5218.
[http://dx.doi.org/10.1200/JCO.2009.26.6114] [PMID: 21060024]
[33]
Hartgrink, H.H.; van de Velde, C.J.; Putter, H.; Songun, I.; Tesselaar, M.E.; Kranenbarg, E.K.; de Vries, J.E.; Wils, J.A.; van der Bijl, J.; van Krieken, J.H. Cooperating Investigators of The Dutch Gastric Cancer Group. Neo-adjuvant chemotherapy for operable gastric cancer: long term results of the Dutch randomised FAMTX trial. Eur. J. Surg. Oncol., 2004, 30(6), 643-649.
[http://dx.doi.org/10.1016/j.ejso.2004.04.013] [PMID: 15256239]
[34]
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), 1879-1887.
[PMID: 15274369]
[35]
Takiguchi, N.; Nunomura, M.; Koda, K.; Oda, K.; Suzuki, H.; Miyazaki, M. Neoadjuvant chemotherapy with CDDP and 5-fluorouracil for gastric cancer with serosal invasion. Oncol. Rep., 2003, 10(2), 433-438.
[http://dx.doi.org/10.3892/or.10.2.433] [PMID: 12579285]
[36]
Wang, X.L.; Wu, G.X.; Zhang, M.D.; Guo, M.; Zhang, H.; Sun, X.F. A favorable impact of preoperative FPLC chemotherapy on patients with gastric cardia cancer. Oncol. Rep., 2000, 7(2), 241-244.
[http://dx.doi.org/10.3892/or.7.2.241] [PMID: 10671664]
[37]
Tokunaga, M.; Sato, Y.; Nakagawa, M.; Aburatani, T.; Matsuyama, T.; Nakajima, Y.; Kinugasa, Y. Perioperative chemotherapy for locally advanced gastric cancer in Japan: current and future perspectives. Surg. Today, 2020, 50(1), 30-37.
[http://dx.doi.org/10.1007/s00595-019-01896-5] [PMID: 31612329]
[38]
Petrelli, F.; Ghidini, M.; Barni, S.; Sgroi, G.; Passalacqua, R.; Tomasello, G. Neoadjuvant chemoradiotherapy or chemotherapy for gastroesophageal junction adenocarcinoma: A systematic review and meta-analysis. Gastric Cancer, 2019, 22(2), 245-254.
[http://dx.doi.org/10.1007/s10120-018-0901-3] [PMID: 30483986]
[39]
Wilke, H.; Preusser, P.; Fink, U.; Gunzer, U.; Meyer, H.J.; Meyer, J.; Siewert, J.R.; Achterrath, W.; Lenaz, L.; Knipp, H. Preoperative chemotherapy in locally advanced and nonresectable gastric cancer: a phase II study with etoposide, doxorubicin, and cisplatin. J. Clin. Oncol., 1989, 7(9), 1318-1326.
[http://dx.doi.org/10.1200/JCO.1989.7.9.1318] [PMID: 2769330]
[40]
Kanaji, S.; Suzuki, S.; Matsuda, Y.; Hasegawa, H.; Yamamoto, M.; Yamashita, K.; Oshikiri, T.; Matsuda, T.; Nakamura, T.; Sumi, Y.; Kakeji, Y. Recent updates in perioperative chemotherapy and recurrence pattern of gastric cancer. Ann Gastroenterol Surg, 2018, 2(6), 400-405.
[http://dx.doi.org/10.1002/ags3.12199] [PMID: 30460342]
[41]
Bose, K.; Franck, C.; Müller, M.N.; Canbay, A.; Link, A.; Venerito, M. Perioperative Therapy of Oesophagogastric Adenocarcinoma: Mainstay and Future Directions. Gastroenterol. Res. Pract., 2017, 20175651903
[http://dx.doi.org/10.1155/2017/5651903] [PMID: 28785280]
[42]
Hartgrink, H.H.; Jansen, E.P.M.; van Grieken, N.C.T.; van de Velde, C.J.H. Gastric cancer. Lancet, 2009, 374(9688), 477-490.
[http://dx.doi.org/10.1016/S0140-6736(09)60617-6] [PMID: 19625077]
[43]
Russo, A.E.; Strong, V.E. Gastric Cancer Etiology and Management in Asia and the West. Annu. Rev. Med., 2019, 70, 353-367.
[http://dx.doi.org/10.1146/annurev-med-081117-043436] [PMID: 30355265]
[44]
Biffi, R.; Fazio, N.; Luca, F.; Chiappa, A.; Andreoni, B.; Zampino, M.G.; Roth, A.; Schuller, J.C.; Fiori, G.; Orsi, F.; Bonomo, G.; Crosta, C.; Huber, O. Surgical outcome after docetaxel-based neoadjuvant chemotherapy in locally-advanced gastric cancer. World J. Gastroenterol., 2010, 16(7), 868-874.
[PMID: 20143466]

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