Skip to main content
Log in

Current standards of lymphadenectomy in gastric cancer

  • Review Article
  • Published:
Updates in Surgery Aims and scope Submit manuscript

Abstract

Gastric cancer remains the 5th most common cancer and the 3rd most common cause of cancer mortality. Most patients diagnosed with gastric cancer still have a poor prognosis due to its advanced presentation at diagnosis, even in countries with developed screening programs. Surgery is the cornerstone of the treatment for gastric cancer, often combined with perioperative chemotherapy. Lymph node dissection is a crucial component of the surgical treatment of gastric cancer. D1 lymphadenectomy is currently recommended for early stage tumors. The extent of lymphadenectomy in advanced gastric cancer, however, is still a matter of debate between Eastern and Western surgeons. Although a D2 dissection is the current standard recommended by most guidelines, there might be a place for more limited dissections such as D1 + in selected cases. This evidence-based review will help defining the optimal lymphadenectomy for patients with gastric cancer.

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

Availability of data and material

Not applicable.

Code availability

Not applicable.

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. https://doi.org/10.3322/caac.21660

    Article  PubMed  Google Scholar 

  2. Ning FL, Lyu J, Pei JP, Gu WJ, Zhang NN, Cao SY, Zeng YJ, Abe M, Nishiyama K, Zhang CD (2022) The burden and trend of gastric cancer and possible risk factors in five Asian countries from 1990 to 2019. Sci Rep 12(1):5980. https://doi.org/10.1038/s41598-022-10014-4

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  3. Lordick F, Carneiro F, Cascinu S, Fleitas T, Haustermans K, Piessen G, Vogel A, Smyth EC; ESMO Guidelines Committee. Electronic address: clinicalguidelines@esmo.org (2022) Gastric cancer: ESMO clinical practice guideline for diagnosis, treatment and follow-up. Ann Oncol 33(10):1005-1020. DOI: https://doi.org/10.1016/j.annonc.2022.07.004.

  4. NCCN Clinical Practice Guidelines in Oncology (NCCN Guidelines®) for Gastric Cancer 01.11.2022. p MS2, MS5-MS7, MS11-MS16. Accessed 15 Jan 2023

  5. Smyth EC, Nilsson M, Grabsch HI, van Grieken NC, Lordick F (2020) Gastric cancer. Lancet 396(10251):635–648. https://doi.org/10.1016/S0140-6736(20)31288-5

    Article  PubMed  CAS  Google Scholar 

  6. Tan Z (2019) Recent advances in the surgical treatment of advanced gastric cancer: a review. Med Sci Monit 25:3537–3541. https://doi.org/10.12659/MSM.916475

    Article  PubMed  PubMed Central  Google Scholar 

  7. Li GZ, Doherty GM, Wang J (2022) Surgical management of gastric cancer: a review. JAMA Surg 157(5):446–454. https://doi.org/10.1001/jamasurg.2022.0182

    Article  PubMed  Google Scholar 

  8. Japanese Gastric Cancer Association (2023) Japanese gastric cancer treatment guidelines 2021 (6th edition). Gastric Cancer 26(1):1–25. https://doi.org/10.1007/s10120-022-01331-8

    Article  Google Scholar 

  9. Kinami S, Nakamura N, Tomita Y, Miyata T, Fujita H, Ueda N, Kosaka T (2019) Precision surgical approach with lymph-node dissection in early gastric cancer. World J Gastroenterol 25(14):1640–1652. https://doi.org/10.3748/wjg.v25.i14.1640

    Article  PubMed  PubMed Central  Google Scholar 

  10. Degiuli M, De Manzoni G, Di Leo A, D’Ugo D, Galasso E, Marrelli D, Petrioli R, Polom K, Roviello F, Santullo F, Morino M (2016) Gastric cancer: current status of lymph node dissection. World J Gastroenterol 22(10):2875–2893. https://doi.org/10.3748/wjg.v22.i10.2875

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  11. Son SY, Hur H, Hyung WJ, Park YK, Lee HJ, An JY, Kim W, Kim HI, Kim HH, Ryu SW, Kim MC, Kong SH, Cho GS, Kim JJ, Park DJ, Ryu KW, Kim YW, Kim JW, Lee JH, Yang HK, Han SU, Korean Laparoendoscopic Gastrointestinal Surgery Study (KLASS) Group (2022) Laparoscopic vs open distal gastrectomy for locally advanced gastric cancer: 5-year outcomes of the KLASS-02 randomized clinical trial. JAMA Surg 157(10):879–886. https://doi.org/10.1001/jamasurg.2022.2749

    Article  PubMed  PubMed Central  Google Scholar 

  12. 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, ChineseLaparoscopic Gastrointestinal SurgeryStudy (CLASS) Group (2019) 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 321(20):1983–1992. https://doi.org/10.1001/jama.2019.5359

    Article  PubMed  PubMed Central  Google Scholar 

  13. 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, Xing 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. https://doi.org/10.1200/JCO.2015.63.7215

    Article  PubMed  Google Scholar 

  14. 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, KoreanLaparo-endoscopic Gastrointestinal SurgeryStudy (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. https://doi.org/10.1097/SLA.0000000000003217

    Article  PubMed  Google Scholar 

  15. Sun T, Wang Y, Liu Y, Wang Z (2022) Perioperative outcomes of robotic versus laparoscopic distal gastrectomy for gastric cancer: a meta-analysis of propensity score-matched studies and randomized controlled trials. BMC Surg 22(1):427. https://doi.org/10.1186/s12893-022-01881-9

    Article  PubMed  PubMed Central  Google Scholar 

  16. Lu J, Zheng CH, Cao LL, Li P, Xie JW, Wang JB, Lin JX, Chen QY, Lin M, Huang CM (2017) The effectiveness of the 8th American Joint Committee on Cancer TNM classification in the prognosis evaluation of gastric cancer patients: a comparative study between the 7th and 8th editions. Eur J Surg Oncol 43(12):2349–2356. https://doi.org/10.1016/j.ejso.2017.09.001

    Article  PubMed  Google Scholar 

  17. Japanese Gastric Cancer Association (2011) Japanese classification of gastric carcinoma: 3rd English edition. Gastric Cancer 14(2):101–112. https://doi.org/10.1007/s10120-011-0041-5

    Article  Google Scholar 

  18. Japanese Research Society for Gastric Cancer, Murakami T (1973) The general rules for the gastric cancer study in surgery. Jpn J Surg 3(1):61–71. https://doi.org/10.1007/BF02469463

  19. Memon MA, Subramanya MS, Khan S, Hossain MB, Osland E, Memon B (2011) Meta-analysis of D1 versus D2 gastrectomy for gastric adenocarcinoma. Ann Surg 253(5):900–911. https://doi.org/10.1097/SLA.0b013e318212bff6

    Article  PubMed  Google Scholar 

  20. Hartgrink HH, van de Velde CJ, Putter H, Bonenkamp JJ, Klein Kranenbarg E, Songun I, Welvaart K, van Krieken JH, Meijer S, Plukker JT, van Elk PJ, Obertop H, Gouma DJ, van Lanschot JJ, Taat CW, de Graaf PW, von Meyenfeldt MF, Tilanus H, Sasako M (2004) Extended lymph node dissection for gastric cancer: who may benefit? Final results of the randomized Dutch gastric cancer group trial. J Clin Oncol 22(11):2069–2077. https://doi.org/10.1200/JCO.2004.08.026

    Article  PubMed  CAS  Google Scholar 

  21. 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. https://doi.org/10.1016/S1470-2045(10)70070-X

    Article  PubMed  Google Scholar 

  22. Cuschieri A, Fayers P, Fielding J, Craven J, Bancewicz J, Joypaul V, Cook P (1996) Postoperative morbidity and mortality after D1 and D2 resections for gastric cancer: preliminary results of the MRC randomised controlled surgical trial. The Surgical Cooperative Group. Lancet 347(9007):995–999. https://doi.org/10.1016/s0140-6736(96)90144-0

    Article  PubMed  CAS  Google Scholar 

  23. Cuschieri A, Weeden S, Fielding J, Bancewicz J, Craven J, Joypaul V, Sydes M, Fayers P (1999) Patient survival after D1 and D2 resections for gastric cancer: long-term results of the MRC randomized surgical trial. Surgical Co-operative Group. Br J Cancer 79(9–10):1522–1530. https://doi.org/10.1038/sj.bjc.6690243

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  24. Degiuli M, Sasako M, Ponti A, Italian Gastric Cancer Study Group (2010) Morbidity and mortality in the Italian Gastric Cancer Study Group randomized clinical trial of D1 versus D2 resection for gastric cancer. Br J Surg 97(5):643–9. https://doi.org/10.1002/bjs.6936

    Article  PubMed  CAS  Google Scholar 

  25. Degiuli M, Reddavid R, Tomatis M, Ponti A, Morino M, Sasako M, of the Italian Gastric Cancer Study Group (IGCSG) (2021) D2 dissection improves disease-specific survival in advanced gastric cancer patients: 15-year follow-up results of the Italian Gastric Cancer Study Group D1 versus D2 randomised controlled trial. Eur J Cancer 150:10–22. https://doi.org/10.1016/j.ejca.2021.03.031

    Article  PubMed  CAS  Google Scholar 

  26. El-Sedfy A, Dixon M, Seevaratnam R, Bocicariu A, Cardoso R, Mahar A, Kiss A, Helyer L, Law C, Coburn NG (2015) Personalized surgery for gastric adenocarcinoma: a meta-analysis of D1 versus D2 lymphadenectomy. Ann Surg Oncol 22(6):1820–1827. https://doi.org/10.1245/s10434-014-4168-6

    Article  PubMed  Google Scholar 

  27. Jiang L, Yang KH, Chen Y, Guan QL, Zhao P, Tian JH, Wang Q (2014) Systematic review and meta-analysis of the effectiveness and safety of extended lymphadenectomy in patients with resectable gastric cancer. Br J Surg 101(6):595–604. https://doi.org/10.1002/bjs.9497

    Article  PubMed  CAS  Google Scholar 

  28. De Manzoni G, Marrelli D, Baiocchi GL, Morgagni P, Saragoni L, Degiuli M, Donini A, Fumagalli U, Mazzei MA, Pacelli F, Tomezzoli A, Berselli M, Catalano F, Di Leo A, Framarini M, Giacopuzzi S, Graziosi L, Marchet A, Marini M, Milandri C, Mura G, Orsenigo E, Quagliuolo V, Rausei S, Ricci R, Rosa F, Roviello G, Sansonetti A, Sgroi G, Tiberio GA, Verlato G, Vindigni C, Rosati R, Roviello F (2017) The Italian Research Group for Gastric Cancer (GIRCG) guidelines for gastric cancer staging and treatment: 2015. Gastric Cancer 20(1):20–30. https://doi.org/10.1007/s10120-016-0615-3

    Article  PubMed  Google Scholar 

  29. Lee JH, Kim JG, Jung HK, Kim JH, Jeong WK, Jeon TJ, Kim JM, Kim YI, Ryu KW, Kong SH, Kim HI, Jung HY, Kim YS, Zang DY, Cho JY, Park JO, Lim DH, Jung ES, Ahn HS, Kim HJ (2014) Clinical practice guidelines for gastric cancer in Korea: an evidence-based approach. J Gastric Cancer 14(2):87–104. https://doi.org/10.5230/jgc.2014.14.2.87

    Article  PubMed  PubMed Central  Google Scholar 

  30. Meyer HJ, Hölscher AH, Lordick F, Messmann H, Mönig S, Schumacher C, Stahl M, Wilke H, Möhler M (2012) Aktuelle S3-Leitlinie zur Chirurgie des Magenkarzinoms [Current S3 guidelines on surgical treatment of gastric carcinoma]. Chirurg 83(1):31–37. https://doi.org/10.1007/s00104-011-2149-x

    Article  PubMed  Google Scholar 

  31. Bickenbach K, Strong VE (2012) Comparisons of gastric cancer treatments: east vs. west. J Gastric Cancer 12(2):55–62. https://doi.org/10.5230/jgc.2012.12.2.55

    Article  PubMed  PubMed Central  Google Scholar 

  32. Yamamoto M, Rashid OM, Wong J (2015) Surgical management of gastric cancer: the east vs. west perspective. J Gastrointest Oncol 6(1):79–88. https://doi.org/10.3978/j.issn.2078-6891.2014.097

    Article  PubMed  PubMed Central  Google Scholar 

  33. Kang JH, Ryu SY, Jung MR, Jeong O (2020) Comparison of long term survival outcomes between D1+ and D2 lymph node dissection for ≥ pT2 or pN+ gastric carcinoma: a large scale case-control study using propensity score matching. Eur J Surg Oncol 46(7):1239–1246. https://doi.org/10.1016/j.ejso.2020.04.013

    Article  PubMed  Google Scholar 

  34. Kimura A, Ogata K, Kogure N, Yanoma T, Suzuki M, Toyomasu Y, Ohno T, Mochiki E, Kuwano H (2016) Outcome of laparoscopic gastrectomy with D1 plus lymph node dissection in gastric cancer patients postoperatively diagnosed with locally advanced disease or lymph node metastasis. Surg Endosc 30(5):2090–2096. https://doi.org/10.1007/s00464-015-4462-9

    Article  PubMed  Google Scholar 

  35. Lorenzon L, Giudicissi R, Scatizzi M, Balducci G, Cantafio S, Biondi A, Persiani R, Mercantini P, D’Ugo D (2020) D1-plus vs D2 nodal dissection in gastric cancer: a propensity score matched comparison and review of published literature. BMC Surg 20(1):126. https://doi.org/10.1186/s12893-020-00714-x

    Article  PubMed  PubMed Central  Google Scholar 

  36. Kota I, Makoto H, Satoshi K, Yutaka T, Etsuro B, Masanori T (2021) Oncologic feasibility of D1+ gastrectomy for patients with cT1N1, cT2N0-1, or cT3N0 gastric cancer. Eur J Surg Oncol 47(2):456–462. https://doi.org/10.1016/j.ejso.2020.07.031

    Article  PubMed  Google Scholar 

  37. Kim J, Eom BW, Nam BH (2014) ADDICT—A multicenter 11 randomized clinical trial of D1+ versus D2 distal gastrectomy for stage IB & II 12 advanced gastric cancer: Design and rationale. Eur J Surg Oncol 40(S162):13

    CAS  Google Scholar 

  38. Wu CW, Hsiung CA, Lo SS, Hsieh MC, Chen JH, Li AF, Lui WY, Whang-Peng J (2006) Nodal dissection for patients with gastric cancer: a randomised controlled trial. Lancet Oncol 7(4):309–315. https://doi.org/10.1016/S1470-2045(06)70623-4

    Article  PubMed  CAS  Google Scholar 

  39. Sasako M, Sano T, Yamamoto S, Kurokawa Y, Nashimoto A, Kurita A, Hiratsuka M, Tsujinaka T, Kinoshita T, Arai K, Yamamura Y, Okajima K, JapanClinicalOncologyGroup (2008) D2 lymphadenectomy alone or with para-aortic nodal dissection for gastric cancer. N Engl J Med 359(5):453–62. https://doi.org/10.1056/NEJMoa0707035

    Article  PubMed  CAS  Google Scholar 

  40. Yonemura Y, Wu CC, Fukushima N, Honda I, Bandou E, Kawamura T, Kamata T, Kim BS, Matsuki N, Sawa T, Noh SH, East Asia SurgicalOncologyGroup (2008) Randomized clinical trial of D2 and extended paraaortic lymphadenectomy in patients with gastric cancer. Int J Clin Oncol 13(2):132–7. https://doi.org/10.1007/s10147-007-0727-1

    Article  PubMed  Google Scholar 

  41. Mocellin S, McCulloch P, Kazi H, Gama-Rodrigues JJ, Yuan Y, Nitti D (2015) Extent of lymph node dissection for adenocarcinoma of the stomach. Cochrane Database Syst Rev 2015(8):CD001964. https://doi.org/10.1002/14651858.CD001964.pub4

    Article  PubMed  PubMed Central  Google Scholar 

  42. Smyth EC, Verheij M, Allum W, Cunningham D, Cervantes A, Arnold D, ESMO Guidelines Committee (2016) Gastric cancer: ESMO clinical practice guidelines for diagnosis, treatment and follow-up. Ann Oncol 27(suppl 5):v38–v49. https://doi.org/10.1093/annonc/mdw350

    Article  PubMed  CAS  Google Scholar 

  43. Wu ZM, Teng RY, Shen JG, Xie SD, Xu CY, Wang LB (2011) Reduced lymph node harvest after neoadjuvant chemotherapy in gastric cancer. J Int Med Res 39(6):2086–2095. https://doi.org/10.1177/147323001103900604

    Article  PubMed  CAS  Google Scholar 

  44. Mariette C, Piessen G, Briez N, Triboulet JP (2008) The number of metastatic lymph nodes and the ratio between metastatic and examined lymph nodes are independent prognostic factors in esophageal cancer regardless of neoadjuvant chemoradiation or lymphadenectomy extent. Ann Surg 247(2):365–371. https://doi.org/10.1097/SLA.0b013e31815aaadf

    Article  PubMed  Google Scholar 

  45. Kauppila JH, Wahlin K, Lagergren P, Lagergren J (2018) Neoadjuvant therapy in relation to lymphadenectomy and resection margins during surgery for oesophageal cancer. Sci Rep 8(1):446. https://doi.org/10.1038/s41598-017-18879-6

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  46. Yeung JC, Bains MS, Barbetta A, Nobel T, DeMeester SR, Louie BE, Orringer MB, Martin LW, Reddy RM, Schlottmann F, Molena D (2020) How many nodes need to be removed to make esophagectomy an adequate cancer operation, and does the number change when a patient has chemoradiotherapy before surgery? Ann Surg Oncol 27(4):1227–1232. https://doi.org/10.1245/s10434-019-07870-2

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

Dr. Agustin Valinoti for his artwork on the figure showing gastric lymph node stations.

Funding

None.

Author information

Authors and Affiliations

Authors

Contributions

All authors contributed on data collection, study design, data analysis and writing.

Corresponding author

Correspondence to Francisco Schlottmann.

Ethics declarations

Conflict of interest

Manuela Monrabal Lezama, Nicholas S. Murdoch Duncan, Sofia Bertona, and Francisco Schlottmann have no conflicts of interest/Competing interest to disclose.

Ethical approval

Not applicable.

Consent to participate

The written informed consent was waived by the IRB owing to the study’s retrospective nature.

Consent for publication

The written informed consent was waived by the IRB owing to the study’s retrospective nature.

Additional information

Publisher's Note

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

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

Monrabal Lezama, M., Murdoch Duncan, N.S., Bertona, S. et al. Current standards of lymphadenectomy in gastric cancer. Updates Surg 75, 1751–1758 (2023). https://doi.org/10.1007/s13304-023-01576-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13304-023-01576-7

Keywords

Navigation