How Should We Measure the Quality of Lymphadenectomy for Gastric Cancer? Anatomical Versus Numerical Criterion

  • Stefano Rausei
  • Federica Galli
  • Georgios LianosEmail author
  • Fausto Rosa
  • Andrea Cossu
  • Alberto Biondi
  • Francesco Martignoni
  • Ferdinando Carlo Maria Cananzi
  • Uberto Fumagalli
  • Sergio Alfieri
  • Roberto Persiani
  • Vittorio Quagliuolo
  • Domenico D’Ugo
  • Riccardo Rosati
Original Research



To compare anatomical with numerical criterion to measure the quality of lymphadenectomy for gastric cancer.

Patients and Methods

We analyzed 447 gastric cancer patients with resectable tumor stage (R0 resection) with at least 16 examined lymph nodes.


Of 447 patients, 82.6% underwent D2 lymphadenectomy for a median of total examined lymph nodes of 28. The 7-year disease-specific survival rate for the whole sample was 71.4%. Survival was significantly different between patients treated with D2 and D1 lymphadenectomy (77.4% versus 44.3%; p < 0.001) and between patients with total examined lymph nodes ≥ 28 and < 28 (74.5% versus 62.3%; p = 0.041). Anatomical criterion significantly differentiated 7-year survival in patients stratified according to a numerical parameter.


We should still consider the anatomical criterion as the best item to measure the quality of lymphadenectomy for gastric cancer.


Locally advanced gastric cancer Lymphadenectomy Number of removed lymph nodes Cancer-related survival 


Compliance with Ethical Standards

Conflict of Interest

The authors declare that they have no conflict of interest.


  1. 1.
    Qiu MZ, Qiu HJ, Wang ZQ, Ren C, Wang DS, Zhang DS, et al. The tumor - log odds of positive lymph nodes-metastasis staging system, a promising new staging system for gastric cancer after D2 resection in China. PLoS One. 2012;7(2):e31736.CrossRefGoogle Scholar
  2. 2.
    Chen HN, Chen XZ, Zhang WH, et al. Necessity of harvesting at least 25 lymph nodes in patients with stage N2–N3 resectable gastric cancer. A 10-year, single-institution cohort study. Medicine. 2015;94(10):e620.CrossRefGoogle Scholar
  3. 3.
    Tanizawa Y, Terashima M. Lymph node dissection in the resection of gastric cancer: review of existing evidence. Gastric Cancer. 2010;13:137–48.CrossRefGoogle Scholar
  4. 4.
    Wu CW, Hsiung CA, Lo SS, Hsieh MC, Chen JH, Li AF, et al. Nodal dissection for patients with gastric cancer: a randomized controlled trial. Lancet Oncol. 2006;7:309–15.CrossRefGoogle Scholar
  5. 5.
    Wu CW, Hsiung CA, Lo SS. Randomized clinical trial of morbidity after D1 and D3 surgery for gastric cancer. Br J Surg. 2004;91:283–7.CrossRefGoogle Scholar
  6. 6.
    Lu J, Wang W, Zheng CH, et al. Influence of total lymph node count on staging and survival after gastrectomy for gastric cancer: an analysis from a two-institution database in China. Ann Surg Oncol. 2017;24:486–93.CrossRefGoogle Scholar
  7. 7.
    Japanese Gastric Cancer Association Japanese gastric cancer treatment guidelines 2014 (ver. 4). Gastric Cancer 2017; 20(1):1-19.Google Scholar
  8. 8.
    Giuliani A, Miccini M, Basso L. Extent of lymphadenectomy and perioperative therapies: two open issues in gastric cancer. World J Gastroenterol. 2014;20(14):3889–904.CrossRefGoogle Scholar
  9. 9.
    Deng J, Zhang R, Pan Y, Wang B, Wu L, Hao X, et al. N stages of the seventh edition of TNM classification are the most intensive variables for predictions of the overall survival of gastric cancer patients who underwent limited lymphadenectomy. Tumor Biol. 2014;35(4):3269–81.CrossRefGoogle Scholar
  10. 10.
    Karpeh MS, Leon L, Klimstra D, Brennan MF. Lymph node staging in gastric cancer: is location more important than number? An analysis of 1.038 patients. Ann Surg. 2000;232(3):362–71.CrossRefGoogle Scholar
  11. 11.
    Smith DD, Schwarz RR, Schwarz RE. Impact of total lymph node count on staging and survival after gastrectomy for gastric cancer: data from a large US-population database. J Clin Oncol. 2005;23:7114–24.CrossRefGoogle Scholar
  12. 12.
    Cuschieri A, Weeden S, Fielding J, Bancewicz J, Craven J, Joypaul V, et al. 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. 1999;79:1522–30.CrossRefGoogle Scholar
  13. 13.
    Rausei S, Dionigi G, Sano T, et al. Updates on surgical management of advanced gastric cancer: new evidence and trends. Insights from the first international course on upper gastrointestinal surgery--Varese (Italy), December 2, 2011. Ann Surg Oncol. 2013;20(12):3942–7.CrossRefGoogle Scholar
  14. 14.
    Degiuli M, Sasako M, Ponti A, et al. Morbidity and mortality after D2 gastrectomy for gastric cancer: results of the Italian Gastric Cancer Study Group prospective multicenter surgical study. J Clin Oncol. 1998;16:1490–3.CrossRefGoogle Scholar
  15. 15.
    Barreto SG, Sirohi B. Why should we perform a D2 lymphadenectomy in gastric cancer? Future Oncol. 2017;13(23):2009–12.CrossRefGoogle Scholar
  16. 16.
    Rausei S, Dionigi G, Boni L, Rovera F, Dionigi R. How does the 7th TNM edition fit in gastric cancer management? Ann Surg Oncol. 2011;18(5):1219–21.CrossRefGoogle Scholar
  17. 17.
    Ahn HS, Lee HJ, Hahn S, Kim WH, Lee KU, Sano T, et al. Evaluation of the seventh American Joint Committee on Cancer/International Union Against Cancer Classification of gastric adenocarcinoma in comparison with the sixth classification. Cancer. 2010;116(24):5592–8.CrossRefGoogle Scholar
  18. 18.
    Sobin LH, Wittekind CH, editors. TNM classification of malignant tumors. 6th ed. New York: Wiley; 2002.Google Scholar
  19. 19.
    Greene FL, Page DL, Fleming ID, et al., editors. AJCC cancer staging manual: TNM classification of malignant tumors. 6th ed. New York: Springer-Verlag; 2002.Google Scholar
  20. 20.
    In H, Solsky I, Palis B, et al. Validation of the 8th edition of the AJCC TNM staging system for gastric cancer using the national cancer database. Ann Surg Oncol. 2017;11:1–9.Google Scholar
  21. 21.
    Edge SB, Byrd DR, Compton CC, et al. AJCC cancer staging manual. 7th ed. New York: Springer; 2010.Google Scholar
  22. 22.
    Gholami S, Janson L, Worhunsky DJ, et al. Number of lymph nodes removed and survival after gastric cancer resection: an analysis from the US gastric cancer collaborative. J Am Coll Surg. 2015;21:291–9.CrossRefGoogle Scholar
  23. 23.
    Schwarz REI, Smith DD. Clinical impact of lymphadenectomy extent in resectable gastric cancer of advanced stage. Ann Surg Oncol. 2006;14:317–8.CrossRefGoogle Scholar
  24. 24.
    Bunt AM, Hermans J, Boon MC, van de Velde C, Sasako M, Fleuren GJ, et al. Evaluation of the extent of lymphadenectomy in a randomized trial of Western-versus Japanese-type surgery in gastric cancer. J Clin Oncol. 1994;12(2):417–22.CrossRefGoogle Scholar
  25. 25.
    Chen T, Yan D, Zheng Z, et al. Evolution in the surgical management of gastric cancer: is extended lymph node dissection back in vogue in the USA? World J Surg Oncol. 2017;15:135.CrossRefGoogle Scholar
  26. 26.
    Chon SH, Berlth F, Plum PS, et al. Gastric cancer treatment in the world: Germany. Transl Gastroenterol Hepatol. 2017;2:53.CrossRefGoogle Scholar
  27. 27.
    Bando E, Yonemura Y, Taniguchi K, Fushida S, Fujimura T, Miwa K. Outcome of ratio of lymph node metastasis in gastric carcinoma. Ann Surg Oncol. 2002;9(8):775–84.CrossRefGoogle Scholar
  28. 28.
    Nitti D, Marchet A, Olivieri M. Ratio between metastatic and examined lymph node is an independent prognostic factor after D2 resection for gastric cancer: analysis of a large European monoinstitution experience. Ann Surg Oncol. 2003;2(5):S54–7.Google Scholar
  29. 29.
    Marchet A, Mocellin S, Ambrosi A, Morgagni P, Garcea D, Marrelli D, et al. The ratio between metastatic and examined lymph nodes is an independent prognostic factor in gastric cancer regardless of the type of lymphadenectomy. Ann Surg. 2007;245:543–52.CrossRefGoogle Scholar
  30. 30.
    Xu D, Geng Q, Long Z, Zhan YQ, Li W, Zhou ZW, et al. Positive lymph node ratio is an independent prognostic factor in gastric cancer after D2 resection regardless of the examined number of lymph nodes. Ann Surg Oncol. 2009;16:319–26.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  • Stefano Rausei
    • 1
  • Federica Galli
    • 2
  • Georgios Lianos
    • 3
    Email author
  • Fausto Rosa
    • 4
  • Andrea Cossu
    • 5
  • Alberto Biondi
    • 6
  • Francesco Martignoni
    • 2
  • Ferdinando Carlo Maria Cananzi
    • 7
  • Uberto Fumagalli
    • 8
  • Sergio Alfieri
    • 4
  • Roberto Persiani
    • 6
  • Vittorio Quagliuolo
    • 7
  • Domenico D’Ugo
    • 6
  • Riccardo Rosati
    • 5
  1. 1.Department of SurgeryASST Valle OlonaGallarateItaly
  2. 2.Department of SurgeryUniversity of InsubriaVareseItaly
  3. 3.Department of SurgeryUniversity Hospital of IoanninaIoanninaGreece
  4. 4.Division of Digestive Surgery, Department of Surgical SciencesCatholic UniversityRomeItaly
  5. 5.Department of SurgeryVita-Salute San Raffaele UniversityMilanItaly
  6. 6.Division of General Surgery, Department of Surgical SciencesCatholic UniversityRomeItaly
  7. 7.Division of Surgical OncologyHumanitas Clinical and Research CenterRozzanoItaly
  8. 8.Department of SurgeryBrescia UniversityBresciaItaly

Personalised recommendations