Log in

The short- and long-term outcomes of laparoscopic D2 lymphadenectomy plus complete mesogastrium excision for lymph node-negative gastric cancer

  • Dynamic Manuscript
  • Published:
Surgical Endoscopy Aims and scope Submit manuscript

Abstract

Background

Patients with T1-3N0M0 gastric cancer (GC) who undergo radical gastrectomy maintain a high recurrence rate. The free cancer cells in the mesogastric adipose connective tissue (Metastasis V) maybe the reason for recurrence in these individuals. We aimed to evaluate whether D2 lymphadenectomy plus complete mesogastrium excision (D2 + CME) was superior to D2 lymphadenectomy with regard to safety and oncological efficacy for T1-3N0M0 GC.

Methods

Patients with T1-3N0M0 GC who underwent radical resection from January 2014 to July 2018 were retrospectively analyzed; there were 323 patients, of whom 185 were in the D2 + CME group and 138 in the D2 group. The primary endpoint was 5-year disease-free survival (DFS). Secondary endpoints include the 5-year overall survival (OS), recurrence pattern, morbidity, mortality, and surgical outcomes.

Results

D2 + CME was associated with less intraoperative bleeding loss, a greater number of lymph nodes harvested, and less time to first postoperative flatus, but the postoperative morbidity was similar. The 5-year DFS was 95.6% (95% CI 92.7–98.5%) and 90.4% (95% CI 85.5–95.3%) in the D2 + CME group and the D2 group, respectively, with a hazard ratio (HR) of 0.455 (95% CI 0.188–1.097; p = 0.071). In terms of recurrence patterns, local recurrence was more prone to occur in the D2 group (p = 0.031). Subgroup analysis indicated that for patients with T1b-3N0M0 GC, the 5-year DFS in the D2 + CME group was considerably greater than that in the D2 group (95.3% [95% CI 91.6–99.0%] vs. 87.6% [95% CI 80.7–94.5%], HR 0.369, 95% CI 0.138–0.983; log-rank p = 0.043).

Conclusion

Laparoscopic D2 + CME for T1-3N0M0 GC is safe and feasible. Furthermore, it not only reduces the local recurrence rate but also improves the 5-year DFS in cases of T1b-3N0M0 GC.

Graphical abstract

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

Access this article

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

Data availability

The data sets used or analyzed in this study are available from the corresponding author on reasonable request.

References

  1. Sung H, Ferlay J, Siegel RL, Laversanne M, Soerjomataram I, Jemal A, Bray F (2021) Global cancer statistics 2020: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin 71(3):209–249

    Article  PubMed  Google Scholar 

  2. Sasako M, Saka M, Fukagawa T, Katai H, Sano T (2007) Surgical treatment of advanced gastric cancer: Japanese perspective. Dig Surg 24(2):101–107

    Article  CAS  PubMed  Google Scholar 

  3. Sano T, Sasako M, Yamamoto S, Nashimoto A, Kurita A, Hiratsuka M, Tsu**aka T, Kinoshita T, Arai K, Yamamura Y, Okajima K (2004) Gastric cancer surgery: morbidity and mortality results from a prospective randomized controlled trial comparing D2 and extended para-aortic lymphadenectomy—Japan Clinical Oncology Group study 9501. J Clin Oncol 22(14):2767–2773

    Article  PubMed  Google Scholar 

  4. Schwarz RE, Smith DD (2007) Clinical impact of lymphadenectomy extent in resectable gastric cancer of advanced stage. Ann Surg Oncol 14(2):317–328

    Article  PubMed  Google Scholar 

  5. Sasako M, Sano T, Yamamoto S, Kurokawa Y, Nashimoto A, Kurita A, Hiratsuka M, Tsu**aka T, Kinoshita T, Arai K, Yamamura Y, Okajima K, Japan Clinical Oncology Group (2008) D2 lymphadenectomy alone or with para-aortic nodal dissection for gastric cancer. N Engl J Med 359(5):453–462

    Article  CAS  PubMed  Google Scholar 

  6. Yang SH, Zhang YC, Yang KH, Li YP, He XD, Tian JH, Lv TH, Hui YH, Sharma N (2009) An evidence-based medicine review of lymphadenectomy extent for gastric cancer. Am J Surg 197(2):246–251

    Article  PubMed  Google Scholar 

  7. Kooby DA, Suriawinata A, Klimstra DS, Brennan MF, Karpeh MS (2003) Biologic predictors of survival in node-negative gastric cancer. Ann Surg 237(6):828–835 (discussion 835–837)

    Article  PubMed  PubMed Central  Google Scholar 

  8. Jeong JY, Kim MG, Ha TK, Kwon SJ (2012) Prognostic factors on overall survival in lymph node negative gastric cancer patients who underwent curative resection. J Gastric Cancer 12(4):210–216

    Article  PubMed  PubMed Central  Google Scholar 

  9. Dittmar Y, Schüle S, Koch A, Rauchfuss F, Scheuerlein H, Settmacher U (2015) Predictive factors for survival and recurrence rate in patients with node-negative gastric cancer—a European single-centre experience. Langenbecks Arch Surg 400(1):27–35

    Article  PubMed  Google Scholar 

  10. Etoh T, Sasako M, Ishikawa K, Katai H, Sano T, Shimoda T (2006) Extranodal metastasis is an indicator of poor prognosis in patients with gastric carcinoma. Br J Surg 93(3):369–373

    Article  CAS  PubMed  Google Scholar 

  11. **e D, Liu L, Osaiweran H, Yu C, Sheng F, Gao C, Hu J, Gong J (2015) Detection and characterization of metastatic cancer cells in the mesogastrium of gastric cancer patients. PLoS ONE 10(11):e0142970

    Article  PubMed  PubMed Central  Google Scholar 

  12. **e D, Osaiweran H, Liu L, Wang X, Yu C, Tong Y, Hu J, Gong J (2013) Mesogastrium: a fifth route of metastasis in gastric cancer? Med Hypotheses 80(4):498–500

    Article  PubMed  Google Scholar 

  13. Heald RJ, Husband EM, Ryall RD (1982) The mesorectum in rectal cancer surgery—the clue to pelvic recurrence? Br J Surg 69(10):613–616

    Article  CAS  PubMed  Google Scholar 

  14. Hohenberger W, Weber K, Matzel K, Papadopoulos T, Merkel S (2009) Standardized surgery for colonic cancer: complete mesocolic excision and central ligation—technical notes and outcome. Colorectal Dis 11(4):354–364 (discussion 364–365)

    Article  CAS  PubMed  Google Scholar 

  15. Maurer CA, Renzulli P, Kull C, Käser SA, Mazzucchelli L, Ulrich A, Büchler MW (2011) The impact of the introduction of total mesorectal excision on local recurrence rate and survival in rectal cancer: long-term results. Ann Surg Oncol 18(7):1899–1906

    Article  CAS  PubMed  Google Scholar 

  16. Shinohara H, Kurahashi Y, Haruta S, Ishida Y, Sasako M (2017) Universalization of the operative strategy by systematic mesogastric excision for stomach cancer with that for total mesorectal excision and complete mesocolic excision colorectal counterparts. Ann Gastroenterol Surg 2(1):28–36

    Article  PubMed  PubMed Central  Google Scholar 

  17. **e D, Yu C, Liu L, Osaiweran H, Gao C, Hu J, Gong J (2016) Short-term outcomes of laparoscopic D2 lymphadenectomy with complete mesogastrium excision for advanced gastric cancer. Surg Endosc 30(11):5138–5139

    Article  PubMed  Google Scholar 

  18. **e D, Shen J, Liu L, Cao B, Wang Y, Qin J, Wu J, Yan Q, Hu Y, Yang C, Cao Z, Hu J, Yin P, Gong J (2021) Complete mesogastric excision for locally advanced gastric cancer: short-term outcomes of a randomized clinical trial. Cell Rep Med 2(3):100217

    Article  PubMed  PubMed Central  Google Scholar 

  19. Zhao D, Deng J, Cao B, Shen J, Liu L, **ao A, Yin P, **e D, Gong J (2022) Short-term outcomes of D2 lymphadenectomy plus complete mesogastric excision for gastric cancer: a propensity score matching analysis. Surg Endosc 36(8):5921–5929

    Article  PubMed  Google Scholar 

  20. Li Z, Wu H, Lin H, Li J, Guo Z, Pan G, Guo Y, Zheng P, Cai Z, Ren J, Zhou J, Ye J, Xu Y (2023) The short- and long-term effect of membrane anatomy-guided laparoscopic D2 lymphadenectomy plus regional complete mesogastrium excision for locally advanced gastric cancer. Surg Endosc 37(6):4990–5003

    Article  PubMed  Google Scholar 

  21. **e D, Wang Y, Shen J, Hu J, Yin P, Gong J (2018) Detection of carcinoembryonic antigen in peritoneal fluid of patients undergoing laparoscopic distal gastrectomy with complete mesogastric excision. Br J Surg 105(11):1471–1479

    Article  CAS  PubMed  Google Scholar 

  22. Japanese Gastric Cancer Association (2011) Japanese classification of gastric carcinoma: 3rd English edition. Gastric Cancer 14(2):101–112

    Article  Google Scholar 

  23. American Joint Committee on Cancer (AJCC) (2010) AJCC cancer staging manual, 7th edn. Springer, New York

    Book  Google Scholar 

  24. Japanese Gastric Cancer Association (2011) Japanese gastric cancer treatment guidelines 2010 (ver. 3). Gastric Cancer 14(2):113–123

    Article  Google Scholar 

  25. Songun I, Putter H, Kranenbarg EM, Sasako M, van de Velde CJ (2010) Surgical treatment of gastric cancer: 15-year follow-up results of the randomised nationwide Dutch D1D2 trial. Lancet Oncol 11(5):439–449

    Article  PubMed  Google Scholar 

  26. Eom BW, Joo J, Kim YW, Bae JM, Park KB, Lee JH, Ryu KW, Kook MC (2013) Role of bursectomy for advanced gastric cancer: result of a case-control study from a large volume hospital. Eur J Surg Oncol 39(12):1407–1414

    Article  CAS  PubMed  Google Scholar 

  27. Hasegawa S, Kunisaki C, Ono H, Oshima T, Fujii S, Taguri M, Morita S, Sato T, Yamada R, Yukawa N, Rino Y, Masuda M (2013) Omentum-preserving gastrectomy for advanced gastric cancer: a propensity-matched retrospective cohort study. Gastric Cancer 16(3):383–388

    Article  PubMed  Google Scholar 

  28. Kurokawa Y, Doki Y, Mizusawa J, Terashima M, Katai H, Yoshikawa T, Kimura Y, Takiguchi S, Nishida Y, Fukushima N, Iwasaki Y, Kaji M, Hirao M, Katayama H, Sasako M (2018) Bursectomy versus omentectomy alone for resectable gastric cancer (JCOG1001): a phase 3, open-label, randomised controlled trial. Lancet Gastroenterol Hepatol 3(7):460–468

    Article  PubMed  Google Scholar 

  29. **e D, Gao C, Lu A, Liu L, Yu C, Hu J, Gong J (2015) Proximal segmentation of the dorsal mesogastrium reveals new anatomical implications for laparoscopic surgery. Sci Rep 6(5):16287

    Article  Google Scholar 

  30. Shinohara H, Kurahashi Y, Ishida Y (2021) Gastric equivalent of the “Holy Plane” to standardize the surgical concept of stomach cancer to mesogastric excision: updating Jamieson and Dobson’s historic schema. Gastric Cancer 24(2):273–282

    Article  PubMed  Google Scholar 

  31. Hu Y, Huang C, Sun Y, Su X, Cao H, Hu J, Xue Y, Suo J, Tao K, He X, Wei H, Ying M, Hu W, Du X, Chen P, Liu H, Zheng C, Liu F, Yu J, Li Z, Zhao G, Chen X, Wang K, Li P, **ng J, Li G (2016) Morbidity and mortality of laparoscopic versus open D2 distal gastrectomy for advanced gastric cancer: a randomized controlled trial. J Clin Oncol 34(12):1350–1357

    Article  PubMed  Google Scholar 

  32. 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(11):2734–2741

    Article  PubMed  Google Scholar 

  33. Lee HJ, Hyung WJ, Yang HK, Han SU, Park YK, An JY, Kim W, Kim HI, Kim HH, Ryu SW, Hur H, Kong SH, Cho GS, Kim JJ, Park DJ, Ryu KW, Kim YW, Kim JW, Lee JH, Kim MC, Korean Laparo-endoscopic Gastrointestinal Surgery Study (KLASS) Group (2019) 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 270(6):983–991

    Article  PubMed  Google Scholar 

  34. Shinohara H, Haruta S, Ohkura Y, Udagawa H, Sakai Y (2015) Tracing dissectable layers of mesenteries overcomes embryologic restrictions when performing infrapyloric lymphadenectomy in laparoscopic gastric cancer surgery. J Am Coll Surg 220(6):e81–e87

    Article  PubMed  Google Scholar 

  35. Kumamoto T, Kurahashi Y, Haruta S, Niwa H, Nakanishi Y, Ozawa R, Okumura K, Ishida Y, Shinohara H (2019) Laparoscopic modified lymphadenectomy in gastric cancer surgery using systematic mesogastric excision: a novel technique based on a concept. Langenbecks Arch Surg 404(3):369–374

    Article  PubMed  Google Scholar 

  36. Whiting J, Sano T, Saka M, Fukagawa T, Katai H, Sasako M (2006) Follow-up of gastric cancer: a review. Gastric Cancer 9(2):74–81

    Article  PubMed  Google Scholar 

  37. Lee IS, Yook JH, Kim TH, Kim HS, Kim KC, Oh ST, Kim BS (2013) Prognostic factors and recurrence pattern in node-negative advanced gastric cancer. Eur J Surg Oncol 39(2):136–140

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

Thank American Journal Experts (AJE) for proofreading the English grammar and spelling of our paper.

Funding

None.

Author information

Authors and Affiliations

Authors

Contributions

Conception and design: ZMC, YCX. Performed the research and acquired the data: ZMC, HML, ZXL, JFZ, WXC, FL, HRZ, YCX. Analyzed the data: ZMC, HML. Manuscript writing: ZMC, HML, YCX. Final approval of manuscript: All authors.

Corresponding author

Correspondence to Yanchang Xu.

Ethics declarations

Disclosures

Zhiming Cai, Huimei Lin, Zhixiong Li, **feng Zhou, Weixiang Chen, Feng Liu, Hongrui Zhao and Yanchang Xu 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.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 25.7 kb)

Supplementary file2 (MP4 472340 kb)

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Cai, Z., Lin, H., Li, Z. et al. The short- and long-term outcomes of laparoscopic D2 lymphadenectomy plus complete mesogastrium excision for lymph node-negative gastric cancer. Surg Endosc 38, 1059–1068 (2024). https://doi.org/10.1007/s00464-023-10621-w

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00464-023-10621-w

Keywords

Navigation