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Long-Term Outcomes of Open Versus Laparoscopic Distal Gastrectomy for T4a Gastric Cancer: A Propensity Score-Matched Cohort Study

  • Gastrointestinal Oncology
  • Published:
Annals of Surgical Oncology Aims and scope Submit manuscript

Abstract

Background

Laparoscopic gastrectomy for advanced gastric cancer (GC) has been applied more frequently worldwide but is still controversial for patients with serosal invasion (T4a). This study compared short- and long-term outcomes of laparoscopic distal radical gastrectomy (LDG) with open distal gastrectomy (ODG) for T4a GC.

Patients and Methods

We retrospectively studied 472 patients with T4a gastric adenocarcinoma in the lower or middle third of the stomach: 231 underwent LDG and 241 underwent ODG between 2013 and 2020. Short-term outcomes included operative characteristics and complications. Long-term outcomes included overall survival (OS) and disease-free survival (DFS). Propensity score-matched (PSM) analysis was used to adjust for imbalances in baseline characteristics between groups.

Results

The PSM strategy resulted in 294 patients (147 in each group). The LDG group had a significantly longer operating time (mean: 200 vs 190 min, p = 0.001) but reduced blood loss (mean: 50 vs 100 ml, p = 0.001). The LDG group had a higher rate of any postoperative complication (23.1% vs 12.2%, p = 0.021) but most were classified as grades I–II according to Clavien–Dindo classification. Grade III–V complications were similar between groups. Five-year OS was 69% versus 60% (p = 0.109) and 5-year DFS was 58% vs 53% (p = 0.3) in LDG and ODG groups, respectively. For tumor size < 5 cm, LDG was better in reduction of blood loss, postoperative hospital length of stay, and OS.

Conclusions

LDG is feasible and safe for patients with T4a GC and is comparable to ODG regarding short- and long-term outcomes. Furthermore, LDG can be a favorable option for T4a GC smaller than 5 cm.

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Data Availability

The data presented in this study are available on request from the corresponding author.

References

  1. Bray F, Ferlay J, Soerjomataram I, Siegel RL, Torre LA, Jemal A. Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin. 2018;68(6):394–424. https://doi.org/10.3322/caac.21492.

    Article  PubMed  Google Scholar 

  2. Kitano S, Iso Y, Moriyama M, Sugimachi K. Laparoscopy-assisted Billroth I gastrectomy. Surgical Laparosc Endosc. 1994;4(2):146–8.

    CAS  Google Scholar 

  3. Kim HH, Han SU, Kim MC, et al. Effect of laparoscopic distal gastrectomy vs open distal gastrectomy on long-term survival among patients with stage i gastric cancer: the KLASS-01 randomized clinical trial. JAMA Oncol. 2019;5(4):506–13. https://doi.org/10.1001/jamaoncol.2018.6727.

    Article  PubMed  PubMed Central  Google Scholar 

  4. Liu F, Huang C, Xu Z, et al. Morbidity and mortality of laparoscopic vs open total gastrectomy for clinical stage I gastric cancer: the CLASS02 multicenter randomized clinical trial. JAMA Oncol. 2020;6(10):1590–7. https://doi.org/10.1001/jamaoncol.2020.3152.

    Article  PubMed  Google Scholar 

  5. Katai H, Mizusawa J, Katayama H, et al. Short-term surgical outcomes from a phase III study of laparoscopy-assisted versus open distal gastrectomy with nodal dissection for clinical stage IA/IB gastric cancer: Japan Clinical Oncology Group Study JCOG0912. Gastric Cancer. 2017;20(4):699–708. https://doi.org/10.1007/s10120-016-0646-9.

    Article  PubMed  Google Scholar 

  6. Hyung WJ, Yang HK, Park YK, et al. Long-term outcomes of laparoscopic distal gastrectomy for locally advanced gastric cancer: the KLASS-02-RCT randomized clinical trial. J Clin Oncol. 2020;38(28):3304–13. https://doi.org/10.1200/jco.20.01210.

    Article  PubMed  Google Scholar 

  7. Huang C, Liu H, Hu Y, et al. Laparoscopic vs open distal gastrectomy for locally advanced gastric cancer: five-year outcomes from the CLASS-01 randomized clinical trial. JAMA Surg. 2022;157(1):9–17. https://doi.org/10.1001/jamasurg.2021.5104.

    Article  PubMed  Google Scholar 

  8. Yu J, Huang C, Sun Y, 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(20):1983–92. https://doi.org/10.1001/jama.2019.5359.

    Article  PubMed  PubMed Central  Google Scholar 

  9. Uyama I, Sugioka A, Matsui H, Fujita J, Komori Y, Hasumi A. Laparoscopic D2 lymph node dissection for advanced gastric cancer located in the middle or lower third portion of the stomach. Gastric Cancer. 2000;3(1):50–5. https://doi.org/10.1007/pl00011690.

    Article  PubMed  Google Scholar 

  10. Nakauchi M, Suda K, Nakamura K, et al. Laparoscopic subtotal gastrectomy for advanced gastric cancer: technical aspects and surgical, nutritional and oncological outcomes. Surg Endosc. 2017;31(11):4631–40. https://doi.org/10.1007/s00464-017-5526-9.

    Article  PubMed  Google Scholar 

  11. Shibuya K, Kawamura H, Takahashi S, et al. Short-term and long-term outcomes following laparoscopic gastrectomy for advanced gastric cancer compared with open gastrectomy. Surg Laparosc Endosc Percutan Tech. 2019;29(4):297–303. https://doi.org/10.1097/sle.0000000000000660.

    Article  PubMed  Google Scholar 

  12. Quan Y, Huang A, Ye M, et al. Comparison of laparoscopic versus open gastrectomy for advanced gastric cancer: an updated meta-analysis. Gastric Cancer. 2016;19(3):939–50. https://doi.org/10.1007/s10120-015-0516-x.

    Article  PubMed  Google Scholar 

  13. Wong J. Effect of laparoscopic versus open distal gastrectomy on 3-year disease free survival in patients with locally advanced gastric cancer: commentary on the class-01 randomized clinical trial. Transl Gastroenterol Hepatol. 2019;4:78. https://doi.org/10.21037/tgh.2019.09.14.

    Article  PubMed  PubMed Central  Google Scholar 

  14. Garbarino GM, Costa G, Laracca GG, et al. Laparoscopic versus open distal gastrectomy for locally advanced gastric cancer in middle-low-volume centers in Western countries: a propensity score matching analysis. Langenbeck’s Arch Surg. 2020;405(6):797–807. https://doi.org/10.1007/s00423-020-01951-7.

    Article  Google Scholar 

  15. Shi Y, Xu X, Zhao Y, et al. Short-term surgical outcomes of a randomized controlled trial comparing laparoscopic versus open gastrectomy with D2 lymph node dissection for advanced gastric cancer. Surg Endosc. 2018;32(5):2427–33. https://doi.org/10.1007/s00464-017-5942-x.

    Article  PubMed  Google Scholar 

  16. Chan BYO, Yau KKW, Chan CKO. Totally laparoscopic versus open gastrectomy for advanced gastric cancer: a matched retrospective cohort study. HKMJ. 2019;25(1):30–7. https://doi.org/10.12809/hkmj177150.

    Article  CAS  PubMed  Google Scholar 

  17. Zhang F, Lan Y, Tang B, Hao Y, Shi Y, Yu P. Comparative study of laparoscopy-assisted and open radical gastrectomy for stage T4a gastric cancer. Int J Surg. 2017;41:23–7. https://doi.org/10.1016/j.ijsu.2017.01.116.

    Article  PubMed  Google Scholar 

  18. Son T, Hyung WJ, Lee JH, Kim YM, Noh SH. Minimally invasive surgery for serosa-positive gastric cancer (pT4a) in patients with preoperative diagnosis of cancer without serosal invasion. Surg Endosc. 2014;28(3):866–74. https://doi.org/10.1007/s00464-013-3236-5.

    Article  CAS  PubMed  Google Scholar 

  19. Li Z, Liu Y, Hao Y, Bai B, Yu D, Zhao Q. Surgical and long-term oncologic outcomes of laparoscopic and open gastrectomy for serosa-positive (pT4a) gastric cancer: a propensity score-matched analysis. Surg Oncol. 2019;28:167–73. https://doi.org/10.1016/j.suronc.2019.01.003.

    Article  PubMed  Google Scholar 

  20. Japanese gastric cancer treatment guidelines 2010 (ver. 3). Gastric Cancer. 2011;14(2):113–23. https://doi.org/10.1007/s10120-011-0042-4.

  21. Japanese gastric cancer treatment guidelines 2014 (ver. 4). Gastric Cancer. 2017;20(1):1–19. https://doi.org/10.1007/s10120-016-0622-4.

  22. Clavien PA, Barkun J, de Oliveira ML, et al. The Clavien-Dindo classification of surgical complications: five-year experience. Ann Surg. 2009;250(2):187–96. https://doi.org/10.1097/SLA.0b013e3181b13ca2.

    Article  PubMed  Google Scholar 

  23. Team RC. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. Accessed 12 May 2022. https://www.R-project.org/.

  24. TM T. A Package for Survival Analysis in R. R package version 3.3-1. Accessed 12 May 2022. https://CRAN.R-project.org/package=survival.

  25. Stuart EA, King G, Imai K, Ho D. MatchIt: Nonparametric preprocessing for parametric causal inference. J Stat Softw. 2011;42(8):1–28. https://doi.org/10.18637/jss.v042.i08.

    Article  Google Scholar 

  26. Beyer K, Baukloh AK, Kamphues C, et al. Laparoscopic versus open gastrectomy for locally advanced gastric cancer: a systematic review and meta-analysis of randomized controlled studies. World J Surgl Oncol. 2019;17(1):68. https://doi.org/10.1186/s12957-019-1600-1.

    Article  Google Scholar 

  27. Park YK, Yoon HM, Kim YW, et al. Laparoscopy-assisted versus open D2 distal gastrectomy for advanced gastric cancer: results from a randomized phase ii multicenter clinical trial (COACT 1001). Ann Surg. 2018;267(4):638–45. https://doi.org/10.1097/sla.0000000000002168.

    Article  PubMed  Google Scholar 

  28. Huang ZN, Ma Y, Chen QY, et al. Potential survival benefits of open over laparoscopic radical gastrectomy for gastric cancer patients beyond three years after surgery: result from multicenter in-depth analysis based on propensity matching. Surg Endosc. 2022;36(2):1456–65. https://doi.org/10.1007/s00464-021-08430-0.

    Article  PubMed  Google Scholar 

  29. Zhang L, Zang L, Sun J, et al. Long-term outcomes of laparoscopy-assisted gastrectomy for T4a advanced gastric cancer: a single-center retrospective study. Surg Laparosc Endosc Percutan Tech. 2019;29(6):476–82. https://doi.org/10.1097/sle.0000000000000684.

    Article  PubMed  Google Scholar 

  30. Shi Y, Xu X, Zhao Y, et al. Long-term oncologic outcomes of a randomized controlled trial comparing laparoscopic versus open gastrectomy with D2 lymph node dissection for advanced gastric cancer. Surgery. 2019;165(6):1211–6. https://doi.org/10.1016/j.surg.2019.01.003.

    Article  PubMed  Google Scholar 

  31. Lee HJ, Hyung WJ, Yang HK, et al. Short-term outcomes of a multicenter randomized controlled trial comparing laparoscopic distal gastrectomy with D2 lymphadenectomy to open distal gastrectomy for locally advanced gastric cancer (KLASS-02-RCT). Ann Surg. 2019;270(6):983–91. https://doi.org/10.1097/sla.0000000000003217.

    Article  PubMed  Google Scholar 

  32. Wang Z, Xing J, Cai J, et al. 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. 2019;33(1):33–45. https://doi.org/10.1007/s00464-018-6391-x.

    Article  PubMed  Google Scholar 

  33. Caruso S, Giudicissi R, Mariatti M, Cantafio S, Paroli GM, Scatizzi M. Laparoscopic versus open gastrectomy for locally advanced gastric cancer: a propensity score-matched retrospective case-control study. Curr Oncol. 2022;29(3):1840–65. https://doi.org/10.3390/curroncol29030151.

    Article  PubMed  PubMed Central  Google Scholar 

  34. Kim SH, Chung Y, Kim YH, Choi SI. Oncologic outcomes after laparoscopic and open distal gastrectomy for advanced gastric cancer: propensity score matching analysis. J Gastric Cancer. 2019;19(1):83–91. https://doi.org/10.5230/jgc.2019.19.e4.

    Article  PubMed  PubMed Central  Google Scholar 

  35. Katai H, Ishikawa T, Akazawa K, et al. Five-year survival analysis of surgically resected gastric cancer cases in Japan: a retrospective analysis of more than 100,000 patients from the nationwide registry of the Japanese Gastric Cancer Association (2001–2007). Gastric Cancer. 2018;21(1):144–54. https://doi.org/10.1007/s10120-017-0716-7.

    Article  PubMed  Google Scholar 

  36. Trastulli S, Desiderio J, Lin JX, et al. Laparoscopic compared with open D2 gastrectomy on perioperative and long-term, stage-stratified oncological outcomes for gastric cancer: a propensity score-matched analysis of the IMIGASTRIC database. Cancers. 2021. https://doi.org/10.3390/cancers13184526.

    Article  PubMed  PubMed Central  Google Scholar 

  37. Kinoshita T, Uyama I, Terashima M, et al. 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. 2019;269(5):887–94. https://doi.org/10.1097/sla.0000000000002768.

    Article  PubMed  Google Scholar 

  38. Ahn SH, Kang SH, Lee Y, et al. Long-term survival outcomes of laparoscopic gastrectomy for advanced gastric cancer: five-year results of a phase II prospective clinical trial. J Gastric Cancer. 2019;19(1):102–10. https://doi.org/10.5230/jgc.2019.19.e6.

    Article  PubMed  PubMed Central  Google Scholar 

  39. Kano Y, Ohashi M, Muneoka Y, et al. Different risk factors for three major recurrence patterns of pathological stage II or III gastric cancer patients who completed adjuvant S-1 monotherapy. EJSO. 2021;47(12):3097–104. https://doi.org/10.1016/j.ejso.2021.04.018.

    Article  PubMed  Google Scholar 

  40. Nakanishi Y, Ohara M, Domen H, Shichinohe T, Hirano S, Ishizaka M. Differences in risk factors between patterns of recurrence in patients after curative resection for advanced gastric carcinoma. World J Surg Oncol. 2013;11:98. https://doi.org/10.1186/1477-7819-11-98.

    Article  PubMed  PubMed Central  Google Scholar 

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Correspondence to Vo Duy Long MD, PhD or Nguyen Lam Vuong MD.

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Disclosure

Drs. Vo Duy Long, Tran Quang Dat, Dang Quang Thong, Nguyen Viet Hai, Ho Le Minh Quoc, Doan Thuy Nguyen, Tran Anh Minh, Nguyen Vu Tuan Anh, Nguyen Lam Vuong, Jimmy So, Masanori Terashima, and Nguyen Hoang Bac disclose any potential or actual personal, political or financial conflict of interest in the material, information or techniques described in the paper.

Ethical Approval

This study was conducted according to the guidelines of the Declaration of Helsinki and approved by Institutional Review Board, University Medical Center Ho Chi Minh city. Approval to perform research on human subjects in this study was provided by the Institutional Review Board, University Medical Center Ho Chi Minh city (registration number: 76/GCN-HDDD).

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Long, V.D., Dat, T.Q., Thong, D.Q. et al. Long-Term Outcomes of Open Versus Laparoscopic Distal Gastrectomy for T4a Gastric Cancer: A Propensity Score-Matched Cohort Study. Ann Surg Oncol 30, 2278–2289 (2023). https://doi.org/10.1245/s10434-022-12897-z

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