Journal of Gastric Cancer

The Korean Gastric Cancer Association (대한위암학회)
권호 표지
DOI QR코드

DOI QR Code

Neoadjuvant Chemotherapy in Asian Patients With Locally Advanced Gastric Cancer

  • Xie Tong (Department of Gastrointestinal Oncology, Key Laboratory of Carcinogenesis and Translational Research (Ministry of Education), Peking University Cancer Hospital and Institute) ;
  • Peng Zhi (Department of Gastrointestinal Oncology, Key Laboratory of Carcinogenesis and Translational Research (Ministry of Education), Peking University Cancer Hospital and Institute) ;
  • Shen Lin (Department of Gastrointestinal Oncology, Key Laboratory of Carcinogenesis and Translational Research (Ministry of Education), Peking University Cancer Hospital and Institute)
  • Received : 2022.10.25
  • Accepted : 2023.01.03
  • Published : 2023.01.31
Download PDF
⟨ Previous Next ⟩

Abstract

Presently, surgery is the only treatment approach for gastric cancer and improving the prognosis of locally advanced gastric cancer is one of the key factors in promoting gastric cancer survival benefit. The MAGIC study was the first to demonstrate the efficacy of neoadjuvant chemotherapy (NAC) in European countries. In recent years, several clinical trials have provided evidence for the use of NAC in Asian patients with locally advanced gastric cancer. However, clinical practice guidelines vary between Asian and non-Asian populations. Optimal NAC regimens, proper target populations, and predictors of NAC outcomes in Asian patients are still under investigation. Herein, we summarized the current progress in the administration of NAC in Asian patients with gastric cancer.

Keywords

Acknowledgement

This work was supported by the National Natural Science Foundation of China (General Program, No.82272764), the Key Program of Beijing Natural Science Foundation (No. Z210015), Clinical Medicine Plus X-Young Scholars Project of Peking University (PKU2019LCXQ020, PKU2018LCXQ018) and Peking University Medicine Fund of Fostering Young Scholars' Scientific & Technological Innovation (BMU2022PYB026).

References

  1. Sung H, Ferlay J, Siegel RL, Laversanne M, Soerjomataram I, Jemal A, et al. Global cancer statistics 2020: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin 2021;71:209-249.  https://doi.org/10.3322/caac.21660
  2. Chaft JE, Shyr Y, Sepesi B, Forde PM. Preoperative and postoperative systemic therapy for operable non-small-cell lung cancer. J Clin Oncol 2022;40:546-555.  https://doi.org/10.1200/JCO.21.01589
  3. Cascone T, William WN Jr, Weissferdt A, Leung CH, Lin HY, Pataer A, et al. Neoadjuvant nivolumab or nivolumab plus ipilimumab in operable non-small cell lung cancer: the phase 2 randomized NEOSTAR trial. Nat Med 2021;27:504-514.  https://doi.org/10.1038/s41591-020-01224-2
  4. Yang H, Liu H, Chen Y, Zhu C, Fang W, Yu Z, et al. Neoadjuvant chemoradiotherapy followed by surgery versus surgery alone for locally advanced squamous cell carcinoma of the esophagus (NEOCRTEC5010): a phase III multicenter, randomized, open-label clinical trial. J Clin Oncol 2018;36:2796-2803.  https://doi.org/10.1200/jco.2018.79.1483
  5. Cunningham D, Allum WH, Stenning SP, Thompson JN, Van de Velde CJ, Nicolson M, et al. Perioperative chemotherapy versus surgery alone for resectable gastroesophageal cancer. N Engl J Med 2006;355:11-20.  https://doi.org/10.1056/NEJMoa055531
  6. Al-Batran SE, Homann N, Pauligk C, Goetze TO, Meiler J, Kasper S, et al. Perioperative chemotherapy with fluorouracil plus leucovorin, oxaliplatin, and docetaxel versus fluorouracil or capecitabine plus cisplatin and epirubicin for locally advanced, resectable gastric or gastro-oesophageal junction adenocarcinoma (FLOT4): a randomised, phase 2/3 trial. Lancet 2019;393:1948-1957.  https://doi.org/10.1016/S0140-6736(18)32557-1
  7. van Hagen P, Hulshof MC, van Lanschot JJ, Steyerberg EW, van Berge Henegouwen MI, Wijnhoven BP, et al. Preoperative chemoradiotherapy for esophageal or junctional cancer. N Engl J Med 2012;366:2074-2084.  https://doi.org/10.1056/NEJMoa1112088
  8. Kang YK, Yook JH, Park YK, Lee JS, Kim YW, Kim JY, et al. PRODIGY: a phase III study of neoadjuvant docetaxel, oxaliplatin, and S-1 plus surgery and adjuvant S-1 versus surgery and adjuvant S-1 for resectable advanced gastric cancer. J Clin Oncol 2021;39:2903-2913.  https://doi.org/10.1200/JCO.20.02914
  9. Zhang X, Liang H, Li Z, Xue Y, Wang Y, Zhou Z, et al. Perioperative or postoperative adjuvant oxaliplatin with S-1 versus adjuvant oxaliplatin with capecitabine in patients with locally advanced gastric or gastro-oesophageal junction adenocarcinoma undergoing D2 gastrectomy (RESOLVE): an open-label, superiority and non-inferiority, phase 3 randomised controlled trial. Lancet Oncol 2021;22:1081-1092.  https://doi.org/10.1016/S1470-2045(21)00297-7
  10. Iwatsuki M, Orita H, Kobayashi K, Hidaka S, Arigami T, Kusumoto T, et al. Phase II study of S-1 and oxaliplatin as neoadjuvant chemotherapy for locally advanced adenocarcinoma of the gastric or esophagogastric junction: KSCC1601. Gastric Cancer 2022;25:180-187.  https://doi.org/10.1007/s10120-021-01218-0
  11. Terazawa T, Matsuyama J, Goto M, Kawabata R, Endo S, Imano M, et al. A phase II study of perioperative capecitabine plus oxaliplatin therapy for clinical SS/SE N1-3 M0 gastric cancer (OGSG 1601). Oncologist 2020;25:119-e208. 
  12. Xinxin Wang SL, Xie Tianyu, Lu Yixun, Guo Xin, Lin Chen. Early results of the randomized, multicenter, controlled evaluation of S-1 and oxaliplatin as neoadjuvant chemotherapy for Chinese advanced gastric cancer patients (RESONANCE Trial). J Clin Oncol 2020;38 Suppl 4:280.
  13. Xue K, Ying X, Bu Z, Wu A, Li Z, Tang L, et al. 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;30:516-525.  https://doi.org/10.21147/j.issn.1000-9604.2018.05.05
  14. Sah BK, Zhang B, Zhang H, Li J, Yuan F, Ma T, et al. Neoadjuvant FLOT versus SOX phase II randomized clinical trial for patients with locally advanced gastric cancer. Nat Commun 2020;11:6093. 
  15. Zhao Q, Lian C, Huo Z, Li M, Liu Y, Fan L, et al. The efficacy and safety of neoadjuvant chemotherapy on patients with advanced gastric cancer: a multicenter randomized clinical trial. Cancer Med 2020;9:5731-5745.  https://doi.org/10.1002/cam4.3224
  16. Saito T, Kurokawa Y, Takahashi T, Yamamoto K, Yamashita K, Tanaka K, et al. Neoadjuvant docetaxel, oxaliplatin and S\xe2\x80\x911 (DOS) combination chemotherapy for patients with resectable adenocarcinoma of esophagogastric junction. Gastric Cancer 2022;25:966-972.  https://doi.org/10.1007/s10120-022-01300-1
  17. Zhang X, Huang H, Wei Z, Zhu Z, Yang D, Fu H, et al. Comparison of docetaxel + oxaliplatin + S-1 vs oxalipatin + S-1 as neoadjuvant chemotherapy for locally advanced gastric cancer: a propensity score matched analysis. Cancer Manag Res 2020;12:6641-6653.  https://doi.org/10.2147/CMAR.S258360
  18. Chen Y, He J, Liu D, Xiao J, Chen X, Tang H, et al. Triplet versus doublet neoadjuvant chemotherapy regimens for locally advanced gastric cancer: a propensity score matching analysis. BMC Cancer 2021;21:1328. 
  19. Tu RH, Lin JX, Xie JW, Wang JB, Lu J, Chen QY, et al. Assessment of the short-term outcomes of laparoscopic gastrectomy after neoadjuvant chemotherapy for locally advanced gastric cancer: a prospective single-armed clinical trial. Surgery 2022;172:160-168.  https://doi.org/10.1016/j.surg.2022.01.015
  20. Yu JH, Wang ZZ, Fan YC, Liu MX, Xu K, Zhang N, et al. Comparison of neoadjuvant chemotherapy followed by surgery vs. surgery alone for locally advanced gastric cancer: a meta-analysis. Chin Med J (Engl) 2021;134:1669-1680.  https://doi.org/10.1097/CM9.0000000000001603
  21. Fu T, Bu ZD, Li ZY, Zhang LH, Wu XJ, Wu AW, et al. Neoadjuvant chemoradiation therapy for resectable esophago-gastric adenocarcinoma: a meta-analysis of randomized clinical trials. BMC Cancer 2015;15:322. 
  22. Meng X, Wang L, Zhao Y, Zhu B, Sun T, Zhang T, et al. Neoadjuvant chemoradiation treatment for resectable esophago-gastric cancer: a systematic review and meta-analysis. J Cancer 2019;10:192-204.  https://doi.org/10.7150/jca.25915
  23. Wang T, Chen Y, Zhao L, Zhou H, Wu C, Zhang X, et al. The effect of neoadjuvant therapies for patients with locally advanced gastric cancer: a propensity score matching study. J Cancer 2021;12:379-386.  https://doi.org/10.7150/jca.46847
  24. Lee J, Lim DH, Kim S, Park SH, Park JO, Park YS, et al. Phase III trial comparing capecitabine plus cisplatin versus capecitabine plus cisplatin with concurrent capecitabine radiotherapy in completely resected gastric cancer with D2 lymph node dissection: the ARTIST trial. J Clin Oncol 2012;30:268-273.  https://doi.org/10.1200/JCO.2011.39.1953
  25. Park SH, Lim DH, Sohn TS, Lee J, Zang DY, Kim ST, et al. A randomized phase III trial comparing adjuvant single-agent S1, S-1 with oxaliplatin, and postoperative chemoradiation with S-1 and oxaliplatin in patients with node-positive gastric cancer after D2 resection: the ARTIST 2 trial . Ann Oncol 2021;32:368-374.  https://doi.org/10.1016/j.annonc.2020.11.017
  26. Hu Y, Huang C, Sun Y, Su X, Cao H, Hu J, et al. Morbidity and mortality of laparoscopic versus open D2 distal gastrectomy for advanced gastric cancer: a randomized controlled trial. J Clin Oncol 2016;34:1350-1357.  https://doi.org/10.1200/JCO.2015.63.7215
  27. Yu J, Huang C, Sun Y, Su X, Cao H, Hu J, et al. 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;321:1983-1992.  https://doi.org/10.1001/jama.2019.5359
  28. Furuta S, Uyama I, Morise Z. Propensity-score-matching-based analysis of laparoscopic gastrectomy with neoadjuvant chemotherapy for gastric carcinoma. Fujian Med J 2021;7:50-53.
  29. Hu HT, Ma FH, Xiong JP, Li Y, Jin P, Liu H, et al. Laparoscopic vs open total gastrectomy for advanced gastric cancer following neoadjuvant therapy: a propensity score matching analysis. World J Gastrointest Surg 2022;14:161-173.  https://doi.org/10.4240/wjgs.v14.i2.161
  30. Li Z, Shan F, Ying X, Zhang Y, e JY, Wang Y, et al. Assessment of laparoscopic distal gastrectomy after neoadjuvant chemotherapy for locally advanced gastric cancer: a randomized clinical trial. JAMA Surg 2019;154:1093-1101.  https://doi.org/10.1001/jamasurg.2019.3473
  31. Yoshida K, Yamaguchi K, Okumura N, Tanahashi T, Kodera Y. Is conversion therapy possible in stage IV gastric cancer: the proposal of new biological categories of classification. Gastric Cancer 2016;19:329-338.  https://doi.org/10.1007/s10120-015-0575-z
  32. Sasako M, Sano T, Yamamoto S, Kurokawa Y, Nashimoto A, Kurita A, et al. D2 lymphadenectomy alone or with para-aortic nodal dissection for gastric cancer. N Engl J Med 2008;359:453-462.  https://doi.org/10.1056/NEJMoa0707035
  33. Tsuburaya A, Mizusawa J, Tanaka Y, Fukushima N, Nashimoto A, Sasako M, et al. Neoadjuvant chemotherapy with S-1 and cisplatin followed by D2 gastrectomy with para-aortic lymph node dissection for gastric cancer with extensive lymph node metastasis. Br J Surg 2014;101:653-660.  https://doi.org/10.1002/bjs.9484
  34. Ito S, Sano T, Mizusawa J, Takahari D, Katayama H, Katai H, et al. A phase II study of preoperative chemotherapy with docetaxel, cisplatin, and S-1 followed by gastrectomy with D2 plus para-aortic lymph node dissection for gastric cancer with extensive lymph node metastasis: JCOG1002. Gastric Cancer 2017;20:322-331.  https://doi.org/10.1007/s10120-016-0619-z
  35. Takahari D, Ito S, Mizusawa J, Katayama H, Terashima M, Sasako M, et al. Long-term outcomes of preoperative docetaxel with cisplatin plus S-1 therapy for gastric cancer with extensive nodal metastasis (JCOG1002). Gastric Cancer 2020;23:293-299.  https://doi.org/10.1007/s10120-019-01007-w
  36. Ri M, Ohashi M, Eto K, Ishizuka N, Atsumi S, Makuuchi R, et al. Favorable outcomes of neoadjuvant chemotherapy and limited para-aortic lymph node dissection for advanced gastric cancer with para-aortic lymph node metastasis. World J Surg 2021;45:2849-2859.  https://doi.org/10.1007/s00268-021-06184-3
  37. Liang H. Extent of lymphadenectomy for local advanced gastric cancer in the era of perioperative treatment and minimally invasive surgery. Zhonghua Wei Chang Wai Ke Za Zhi 2022;25:284-289. 
  38. Iwasaki Y, Terashima M, Mizusawa J, Katayama H, Nakamura K, Katai H, et al. Gastrectomy with or without neoadjuvant S-1 plus cisplatin for type 4 or large type 3 gastric cancer (JCOG0501): an open-label, phase 3, randomized controlled trial. Gastric Cancer 2021;24:492-502.  https://doi.org/10.1007/s10120-020-01136-7
  39. Sakuramoto S, Sasako M, Yamaguchi T, Kinoshita T, Fujii M, Nashimoto A, et al. Adjuvant chemotherapy for gastric cancer with S-1, an oral fluoropyrimidine. N Engl J Med 2007;357:1810-1820.  https://doi.org/10.1056/NEJMoa072252
  40. Bang YJ, Kim YW, Yang HK, Chung HC, Park YK, Lee KH, et al. Adjuvant capecitabine and oxaliplatin for gastric cancer after D2 gastrectomy (CLASSIC): a phase 3 open-label, randomised controlled trial. Lancet 2012;379:315-321. 
  41. Cho H, Nakamura J, Asaumi Y, Yabusaki H, Sakon M, Takasu N, et al. Long-term survival outcomes of advanced gastric cancer patients who achieved a pathological complete response with neoadjuvant chemotherapy: a systematic review of the literature. Ann Surg Oncol 2015;22:787-792.  https://doi.org/10.1245/s10434-014-4084-9
  42. Li Z, Shan F, Wang Y, Zhang Y, Zhang L, Li S, et al. Correlation of pathological complete response with survival after neoadjuvant chemotherapy in gastric or gastroesophageal junction cancer treated with radical surgery: a meta-analysis. PLoS One 2018;13:e0189294. 
  43. Xie JW, Lu J, Xu BB, Zheng CH, Li P, Wang JB, et al. Prognostic value of tumor regression grading in patients treated with neoadjuvant chemotherapy plus surgery for gastric cancer. Front Oncol 2021;11:587856. 
  44. Lin JX, Tang YH, Lin GJ, Ma YB, Desiderio J, Li P, et al. Association of adjuvant chemotherapy with overall survival among patients with locally advanced gastric cancer after neoadjuvant chemotherapy. JAMA Netw Open 2022;5:e225557.
  45. Mokdad AA, Yopp AC, Polanco PM, Mansour JC, Reznik SI, Heitjan DF, et al. Adjuvant chemotherapy vs postoperative observation following preoperative chemoradiotherapy and resection in gastroesophageal cancer: a propensity score-matched analysis. JAMA Oncol 2018;4:31-38.  https://doi.org/10.1001/jamaoncol.2017.2805
  46. Kang WZ, Wang BZ, Li DF, Jiang ZC, Xiong JP, Li Y, et al. Can gastric cancer patients with high mandard score benefit from neoadjuvant chemotherapy? Can J Gastroenterol Hepatol 2022;2022:8178184. 
  47. Xie K, Cui Y, Zhang D, He W, He Y, Gao D, et al. Pretreatment contrast-enhanced computed tomography radiomics for prediction of pathological regression following neoadjuvant chemotherapy in locally advanced gastric cancer: a preliminary multicenter study. Front Oncol 2022;11:770758. 
  48. Chen Y, Xu W, Li YL, Liu W, Sah BK, Wang L, et al. CT-based radiomics showing generalization to predict tumor regression grade for advanced gastric cancer treated with neoadjuvant chemotherapy. Front Oncol 2022;12:758863. 
  49. Song R, Cui Y, Ren J, Zhang J, Yang Z, Li D, et al. CT-based radiomics analysis in the prediction of response to neoadjuvant chemotherapy in locally advanced gastric cancer: a dual-center study. Radiother Oncol 2022;171:155-163.  https://doi.org/10.1016/j.radonc.2022.04.023
  50. Zhu Y, Jiang Z, Wang B, Li Y, Jiang J, Zhong Y, et al. Quantitative dynamic-enhanced MRI and intravoxel incoherent motion diffusion-weighted imaging for prediction of the pathological response to neoadjuvant chemotherapy and the prognosis in locally advanced gastric cancer. Front Oncol 2022;12:841460. 
  51. Cancer Genome Atlas Research Network. Comprehensive molecular characterization of gastric adenocarcinoma. Nature 2014;513:202-209.  https://doi.org/10.1038/nature13480
  52. Smyth EC, Wotherspoon A, Peckitt C, Gonzalez D, Hulkki-Wilson S, Eltahir Z, et al. Mismatch repair deficiency, microsatellite instability, and survival: an exploratory analysis of the medical research council adjuvant gastric infusional chemotherapy (MAGIC) trial. JAMA Oncol 2017;3:1197-1203.  https://doi.org/10.1001/jamaoncol.2016.6762
  53. Pietrantonio F, Miceli R, Raimondi A, Kim YW, Kang WK, Langley RE, et al. Individual patient data meta-analysis of the value of microsatellite instability as a biomarker in gastric cancer. J Clin Oncol 2019;37:3392-3400.  https://doi.org/10.1200/JCO.19.01124
  54. Xie T, Peng Z, Liu Y, Zhang Z, Zhang X, Li J, et al. Clinicopathological characteristics and response to chemotherapy in treatment-naive epstein-barr virus associated gastric cancer: a retrospective study. Front Oncol 2021;11:611676. 
  55. Zhou K, Wang A, Wei J, Ji K, Li Z, Ji X, et al. The value of perioperative chemotherapy for patients with hepatoid adenocarcinoma of the stomach undergoing radical gastrectomy. Front Oncol 2022;11:789104. 
  56. Stahl M, Maderer A, Lordick F, Mihaljevic AL, Kanzler S, Hoehler T, et al. Perioperative chemotherapy with or without epidermal growth factor receptor blockade in unselected patients with locally advanced oesophagogastric adenocarcinoma: Randomized phase II study with advanced biomarker program of the German Cancer Society (AIO/CAO STO-0801). Eur J Cancer 2018;93:119-126.  https://doi.org/10.1016/j.ejca.2018.01.079
  57. Li Z, Gao X, Peng X, May Chen MJ, Li Z, Wei B, et al. Multi-omics characterization of molecular features of gastric cancer correlated with response to neoadjuvant chemotherapy. Sci Adv 2020;6:eaay4211. 
  58. Kleo K, Jovanovic VM, Arndold A, Lehmann A, Lammert H, Berg E, et al. Response prediction in patients with gastric and esophagogastric adenocarcinoma under neoadjuvant chemotherapy using targeted gene expression analysis and next-generation sequencing in pre-therapeutic biopsies. J Cancer Res Clin Oncol 2022. 
  59. Christina Svensson M, Linden A, Nygaard J, Borg D, Hedner C, Nodin B, et al. T cells, B cells, and PD-L1 expression in esophageal and gastric adenocarcinoma before and after neoadjuvant chemotherapy: relationship with histopathological response and survival. OncoImmunology 2021;10:1921443. 
  60. Shitara K, Ajani JA, Moehler M, Garrido M, Gallardo C, Shen L, et al. Nivolumab plus chemotherapy or ipilimumab in gastro-oesophageal cancer. Nature 2022;603:942-948. https://doi.org/10.1038/s41586-022-04508-4
  61. Hasegawa H, Shitara K, Takiguchi S, Takiguchi N, Ito S, Kochi M, et al. A multicenter, open-label, single-arm phase I trial of neoadjuvant nivolumab monotherapy for resectable gastric cancer. Gastric Cancer 2022;25:619-628.  https://doi.org/10.1007/s10120-022-01286-w
  62. Jiang H, Yu X, Li N, Kong M, Ma Z, Zhou D, et al. Efficacy and safety of neoadjuvant sintilimab, oxaliplatin and capecitabine in patients with locally advanced, resectable gastric or gastroesophageal junction adenocarcinoma: early results of a phase 2 study. J Immunother Cancer 2022;10:e003635. 
  63. Andre T, Tougeron D, Piessen G, de la Fouchardiere C, Louvet C, Adenis A, et al. Neoadjuvant nivolumab plus ipilimumab and adjuvant nivolumab in localized deficient mismatch repair/microsatellite instability-high gastric or esophagogastric junction adenocarcinoma: the GERCOR NEONIPIGA phase II study. J Clin Oncol 2023;41:255-265. https://doi.org/10.1200/JCO.22.00686