Skip to main content

Advertisement

Log in

Short- and long-term outcomes of laparoscopic versus open gastrectomy for locally advanced gastric cancer following neoadjuvant chemotherapy

  • Published:
Surgical Endoscopy Aims and scope Submit manuscript

Abstract

Background

This study aimed to investigate the short- and long-term outcomes of laparoscopic gastrectomy (LG) in patients with advanced gastric cancer following neoadjuvant chemotherapy (NAC) to determine its safety and feasibility.

Methods

We retrospectively investigated 51 patients who underwent gastrectomy for locally advanced gastric cancer [cT3-4/N1-3 or macroscopic type 3 (> 80 mm) or type 4] following NAC between November 2009 and January 2018. After excluding two patients who underwent palliative surgery due to peritoneal dissemination, 49 patients were ultimately selected for this cohort study. The patients were then divided into the LG group and open gastrectomy (OG) group, after which the clinicopathological characteristics as well as short- and long-term outcomes were examined.

Results

Compared with the OG group, the LG group demonstrated a significantly lower amount of intraoperative blood loss and a shorter hospital stay. The overall complication rates were 10% (2 of 20 patients) and 24% (7 of 29 patients) in the LG and OG groups (P = 0.277), respectively. No significant differences in 5-year disease-free (LG 44.4% vs. OG 53.3%; P = 0.382) or overall survival rates (LG 46.9% vs. OG 54.0%; P = 0.422) were observed between the groups. Multivariate analysis revealed that the surgical procedure (LG vs. OG) was not an independent risk factor for disease-free (P = 0.645) or overall survival (P = 0.489).

Conclusions

LG may be a potential therapeutic option for patients with gastric cancer following NAC considering its high success rates and acceptable short- and long-term outcomes.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1

Similar content being viewed by others

References

  1. Torre LA, Bray F, Siegel RL, Ferlay J, Lortet-Tieulent J, Jemal A (2015) Global cancer statistics, 2012. CA Cancer J Clin 65:87–108

    PubMed  Google Scholar 

  2. Cunningham D, Allum WH, Stenning SP, Thompson JN, Van de Velde CJ, Nicolson M, Scarffe JH, Lofts FJ, Falk SJ, Iveson TJ, Smith DB, Langley RE, Verma M, Weeden S, Chua YJ, Trial Participants MAGIC (2006) Perioperative chemotherapy versus surgery alone for resectable gastroesophageal cancer. N Engl J Med 355:11–20

    Article  CAS  PubMed  Google Scholar 

  3. Al-Batran SE, Homann N, Pauligk C, Goetze TO, Meiler J, Kasper S, Kopp HG, Mayer F, Haag GM, Luley K, Lindig U, Schmiegel W, Pohl M, Stoehlmacher J, Folprecht G, Probst S, Prasnikar N, Fischbach W, Mahlberg R, Trojan J, Koenigsmann M, Martens UM, Thuss-Patience P, Egger M, Block A, Heinemann V, Illerhaus G, Moehler M, Schenk M, Kullmann F, Behringer DM, Heike M, Pink D, Teschendorf C, Löhr C, Bernhard H, Schuch G, Rethwisch V, von Weikersthal LF, Hartmann JT, Kneba M, Daum S, Schulmann K, Weniger J, Belle S, Gaiser T, Oduncu FS, Güntner M, Hozaeel W, Reichart A, Jäger E, Kraus T, Mönig S, ßBechstein WO, Schuler M, Schmalenberg H, Hofheinz RD, FLOT4-AIO Investigators (2019) 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 393:1948–1957

    Article  PubMed  Google Scholar 

  4. Kitano S, Iso Y, Moriyama M, Sugimachi K (1994) Laparoscopy-assisted Billroth I gastrectomy. Surg Laparosc Endosc 4:146–148

    CAS  PubMed  Google Scholar 

  5. Hu Y, Ying M, Huang C, Wei H, Jiang Z, Peng X, Hu J, Du X, Wang B, Lin F, Xu J, Dong G, Mou T, Li G, Chinese Laparoscopic Gastrointestinal Surgery Study (CLASS) Group (2014) Oncologic outcomes of laparoscopy-assisted gastrectomy for advanced gastric cancer: a large-scale multicenter retrospective cohort study from China. Surg Endsoc 28:2048–2056

    Article  Google Scholar 

  6. Lee JH, Lee CM, Son SY, Ahn SH, Park DJ, Kim HH (2014) Laparoscopic versus open gastrectomy for gastric cancer: long-term oncologic results. Surgery 155:154–164

    Article  PubMed  Google Scholar 

  7. Shinohara T, Satoh S, Kanaya S, Ishida Y, Taniguchi K, Isogaki J, Inaba K, Yanaga K, Uyama I (2013) Laparoscopic versus open D2 gastrectomy for advanced gastric cancer: a retrospective cohort study. Surg Endosc 27:286–294

    Article  PubMed  Google Scholar 

  8. Kinoshita T, Uyama I, Terashima M, Noshiro H, Nagai E, Obama K, Tamamori Y, Nabae T, Honda M, Abe T, LOC-A Study Group (2019) Long-term outcomes of laparoscopic versus open surgery for clinical Stage II/III gastric cancer: A multicenter cohort study in Japan (LOC-A study). Ann Surg 269:887–894

    Article  Google Scholar 

  9. Cai J, Wei D, Gao CF, Zhang CS, Zhang H, Zhao T (2011) A prospective randomized study comparing open versus laparoscopy-assisted D2 radical gastrectomy in advanced gastric cancer. Dig Surg 28:331–337

    Article  CAS  PubMed  Google Scholar 

  10. Park YK, Yoon HM, Kim YW, Park JY, Ryu KW, Lee YJ, Jeong O, Yoon KY, Lee JH, Lee SE, Yu W, Jeong SH, Kim T, Kim S, Nam BH, COACT group, (2018) Laparoscopy-assisted versus open D2 distal gastrectomy for advanced gastric cancer: results from a randomized phase II multicenter clinical trial (COACT 1001). Ann Surg 267:638–645

    Article  PubMed  Google Scholar 

  11. Inaki N, Etoh T, Ohyama T, Uchiyama K, Katada N, Koeda K, Yoshida K, Takagane A, Kojima K, Sakuramoto S, Shiraishi N, Kitano S (2015) A multi-institutional, prospective, Phase II feasibility study of laparoscopy-assisted distal gastrectomy with D2 lymph node dissection for locally advanced gastric cancer (JLSSG0901). World J Surg 39:2734–2741

    Article  PubMed  Google Scholar 

  12. Hur H, Lee HY, Lee HJ, Kim MC, Hyung WJ, Park YK, Kim W, Han SU (2015) Efficacy of laparoscopic subtotal gastrectomy with D2 lymphadenectomy for locally advanced gastric cancer: the protocol of the KLASS-02 multicenter randomized controlled clinical trial. BMC Cancer 15:355

    Article  PubMed  PubMed Central  Google Scholar 

  13. Japanese Gastric Cancer Association (2011) Japanese gastric cancer treatment guidelines 2010 (ver. 3). Gastric Cancer 14:113–123

    Article  Google Scholar 

  14. Japanese Gastric Cancer Association (2011) Japanese classification of gastric carcinoma: 3rd English edition. Gastric Cancer 14:101–112

  15. Kanaya S, Gomi T, Momoi H, Tamaki N, Isobe H, Katayama T, Wada Y, Ohtoshi M (2002) Delta-shaped anastomosis in totally laparoscopic Billroth I gastrectomy: new technique of intraab- dominal gastroduodenostomy. J Am Coll Surg 195:284–287

    Article  PubMed  Google Scholar 

  16. Inaba K, Satoh S, Ishida Y, Taniguchi K, Isogaki J, Kanaya S, Uyama I (2010) Overlap method: novel intracorporeal esophagojejunostomy after laparoscopic total gastrectomy. J Am Coll Surg 211:e25–e29

    Article  PubMed  Google Scholar 

  17. Eisenhauer EA, Therasse P, Bogaerts J, Schwartz LH, Sargent D, Ford R, Dancey J, Arbuck S, Gwyther S, Mooney M, Rubinstein L, Shankar L, Dodd L, Kaplan R, Lacombe D, Verweij J (2009) New response evaluation criteria in solid tumours: revised RECIST guideline (version 1.1). Eur J Cancer 45:228–247

    Article  CAS  PubMed  Google Scholar 

  18. Charlson ME, Pompei P, Ales KL, MacKenzie CR (1987) A new method of classifying prognostic comorbidity in longitudinal studies: development and validation. J Chronic Dis 40:373–383

    Article  CAS  PubMed  Google Scholar 

  19. Dindo D, Demartines N, Clavien PA (2004) Classification of surgical complications: a new proposal with evaluation in a cohort of 6336 patients and results of a survey. Ann Surg 240:205–213

    Article  PubMed  PubMed Central  Google Scholar 

  20. Li Z, Shan F, Wang Y, Li S, Jia Y, Zhang L, Yin D, Ji J (2016) Laparoscopic versus open distal gastrectomy for locally advanced gastric cancer after neoadjuvant chemotherapy: safety and short-term oncologic results. Surg Endosc 30:4265–4278

    Article  PubMed  Google Scholar 

  21. Li Z, Shan F, Ying X, Zhang Y, Wang Y, Ren H, Su X, Ji J (2019) Assessment of laparoscopic distal gastrectomy after neoadjuvant chemotherapy for locally advanced gastric cancer: a randomized clinical trial. JAMA. https://doi.org/10.1001/jamasurg.2019.3473

    Article  PubMed  PubMed Central  Google Scholar 

  22. Wang X, Zhao L, Liu H, Zhong D, Liu W, Shan G, Dong F, Gao W, Bai C, Li X (2016) A phase II study of a modified FOLFOX6 regimen as neoadjuvant chemotherapy for locally advanced gastric cancer. Br J Cancer 114:1326–1333

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Tsuburaya A, Mizusawa J, Tanaka Y, Fukushima N, Nashimoto A, Sasako M, Stomach Cancer Study Group of the Japan Clinical Oncology Group (2014) 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 101:653–660

    Article  Google Scholar 

  24. Feng D, Leong M, Li T, Chen L, Li T (2015) Surgical outcomes in patients with locally advanced gastric cancer treated with S-1 and oxaliplatin as neoadjuvant chemotherapy. World J Surg Oncol 13:11

    Article  PubMed  PubMed Central  Google Scholar 

  25. Terazawa T, Matsuyama J, Goto M, Kawabata R, Endo S, Imano M, Fujita S, Akamura Y, Taniguchi H, Tatsumi M, Lee SW, Kurisu Y, Kawakami H, Kurokawa Y, Shimokawa T, Sakai D, Kato T, Fujitani K, Satoh T (2020) A phase II study of perioperative capecitabine plus oxaliplatin therapy for clinical SS/SE N1–3 M0 gastric cancer (OGSG1601). Oncologist 25:119–e208

    Article  CAS  PubMed  Google Scholar 

  26. Kochi M, Fujii M, Kanamori N, Mihara Y, Funada T, Tamegai H, Watanabe M, Takayama Y, Suda H, Takayama T (2017) Phase II study of neoadjuvant chemotherapy with S-1 and CDDP in patients with lymph node metastatic Stage II or III gastric cancer. Am J Clin Oncol 40:17–21

    Article  CAS  PubMed  Google Scholar 

  27. Tokunaga M, Sato Y, Nakagawa M, Aburatani T, Matsuyama T, Nakajima Y, Kinugasa Y (2020) Perioperative chemotherapy for locally advanced gastric cancer in Japan: current and future perspectives. Surg Today 50:30–37

    Article  PubMed  Google Scholar 

  28. Wang Z, Xing J, Cai J, Zhang Z, Li F, Zhang N, Wu J, Cui M, Liu Y, Chen L, Yang H, Zheng Z, WangX GC, Wang Z, Fan Q, Zhu Y, Ren S, Zhang C, Liu M, Ji J, Su X (2019) Short-term surgical outcomes of laparoscopy-assisted versus open D2 distal gastrectomy for locally advanced gastric cancer in North China: a multicenter randomized controlled trial. Surg Endosc 33:33–45

    Article  PubMed  Google Scholar 

  29. Mörner ME, Gunnarsson U, Jestin P, Svanfeldt M (2012) The importance of blood loss during colon cancer surgery for long- term survival: an epidemiological study based on a population based register. Ann Surg 255:1126–1128

    Article  PubMed  Google Scholar 

  30. Nagai S, Fujii T, Kodera Y, Kanda M, Sahin TT, Kanzaki A, Yamada S, Sugimoto H, Nomoto S, Takeda S, Morita S, Nakao A (2011) Impact of operative blood loss on survival in invasive ductal adenocarcinoma of the pancreas. Pancreas 40:3–9

    Article  PubMed  Google Scholar 

  31. Liang YX, Guo HH, Deng JY, Wang BG, Ding XW, Wang XN, Zhang L, Liang H (2013) Impact of intraoperative blood loss on survival after curative resection for gastric cancer. World J Gastroenterol 19:5542–5550

    Article  PubMed  PubMed Central  Google Scholar 

  32. Ahn HS, Jeong SH, Son YG, Lee HJ, Im SA, Bang YJ, Kim HH, Yang HK (2014) Effect of neoadjuvant chemotherapy on postoperative morbidity and mortality in patients with locally advanced gastric cancer. Br J Surg 101:1560–1565

    Article  CAS  PubMed  Google Scholar 

  33. Okabe H, Hata H, Ueda S, Zaima M, Tokuka A, Yoshimura T, Ota S, Kinjo Y, Yoshimura K, Sakai Y, Kyoto University Surgical Oncology Group (KUSOG) (2016) A phase II study of neoadjuvant chemotherapy with S-1 and cisplatin for stage III gastric cancer: KUGC03. J Surg Oncol 113:36–41

    Article  Google Scholar 

  34. Wu L, Ge L, Qin Y, Huang M, Chen J, Yang Y, Zhong J (2019) Postoperative morbidity and mortality after neoadjuvant chemotherapy versus upfront surgery for locally advanced gastric cancer: a propensity score matching analysis. Cancer Manag Res 11:6011–6018

    Article  PubMed  PubMed Central  Google Scholar 

  35. Kosaka T, Akiyama H, Miyamoto H, Sato S, Tanaka Y, Sato K, Kunisaki C, Endo I (2019) Outcomes of preoperative S-1 and docetaxel combination chemotherapy in patients with locally advanced gastric cancer. Cancer Chemother Pharmacol 83:1047–1055

    Article  CAS  PubMed  Google Scholar 

  36. Kim MC, Kim W, Kim HH, Ryu SW, Ryu SY, Song KY, Lee HJ, Cho GS, Han SU, Hyung WJ, Korean Laparoscopic Gastrointestinal Surgery Study (KLASS) Group (2008) Risk factors associated with complication following laparoscopy-assisted gastrectomy for gastric cancer: a large-scale korean multicenter study. Ann Surg Oncol 15:2692–2700

    Article  Google Scholar 

  37. Ryu KW, Kim YW, Lee JH, Nam BH, Kook MC, Choi IJ, Bae JM (2008) Surgical complications and the risk factors of laparoscopy-assisted distal gastrectomy in early gastric cancer. Ann Surg Oncol 15:1625–1631

    Article  PubMed  Google Scholar 

  38. 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 MG, Huber O, Goldhirsch A, de Braud F, Roth AD, Swiss Group for Clinical Cancer Research SAKK, European Institute of Oncology, Milan, Italy (2016) 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 27:668–673

    Article  Google Scholar 

  39. Shoup M, Brennan MF, Karpeh MS, Gillern SM, McMahon RL, Conlon KC (2002) Port site metastasis after diagnostic laparoscopy for upper gastrointestinal tract malignancies: an uncommon entity. Ann Surg Oncol 9:632–636

    Article  PubMed  Google Scholar 

  40. Tokunaga M, Tanizawa Y, Bando E, Kawamura T, Terashima M (2013) Poor survival rate in patients with postoperative intra-abdominal infectious complicationsfollowing curative gastrectomy for gastric cancer. Ann Surg Oncol 20:1575–1583

    Article  PubMed  Google Scholar 

  41. Kubota T, Hiki N, Sano T, Nomura S, Nunobe S, Kumagai K, Aikou S, Watanabe R, Kosuga T, Yamaguchi T (2014) Prognostic significance of complications after curative surgery for gastric cancer. Ann Surg Oncol 21:891–898

    Article  PubMed  Google Scholar 

  42. Lagarde SM, Reitsma JB, Ten Kate FJ, Busch OR, Obertop H, Zwinderman AH, Moons J, van Lanschot JJ, Lerut T (2008) Predicting individual survival after potentially curative esophagectomy for adenocarcinoma of the esophagus or gastroesophageal junction. Ann Surg 248:1006–1013

    Article  PubMed  Google Scholar 

  43. Shimada H, Fukagawa T, Haga Y, Oba K (2017) Does postoperative morbidity worsen the oncological outcome after radical surgery for gastrointestinal cancers? A systematic review of the literature. Ann Gastroenterol Surg 1:11–23

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Muneharu Fujisaki.

Ethics declarations

Conflict of interest

Muneharu Fujisaki, Norio Mitsumori, Toshihiko Shinohara, Naoto Takahashi, Hiroaki Aoki, Yuya Nyumura, Seizo Kitazawa, and Katsuhiko Yanaga have no conflicts of interest or financial ties to disclose.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Fujisaki, M., Mitsumori, N., Shinohara, T. et al. Short- and long-term outcomes of laparoscopic versus open gastrectomy for locally advanced gastric cancer following neoadjuvant chemotherapy. Surg Endosc 35, 1682–1690 (2021). https://doi.org/10.1007/s00464-020-07552-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00464-020-07552-1

Keywords

Navigation