Lymph Node Noncompliance Affects the Long-Term Prognosis of Patients with Gastric Cancer after Laparoscopic Total Gastrectomy



Our study investigated the effect of lymph node (LN) noncompliance on the long-term prognosis of patients after laparoscopic total gastrectomy (LTG) and explored the risk factors of LN noncompliance.


The clinicopathological data of gastric cancer (GC) patients who underwent LTG with D2 lymphadenectomy from June 2007 to December 2013 were prospectively collected and retrospectively analyzed. The effects of LN noncompliance on the long-term prognosis of patients with GC after LTG were explored.


The overall LN noncompliance rate was 51.9%. The survival rate of patients after LTG with LN compliance was significantly superior to that of patients with LN noncompliance (p = 0.013). The stratified analysis of TNM stage indicated that there was no difference between the OS of stage I patients with LN compliance and those with LN noncompliance; OS of stage II/III patients with LN compliance was significantly better than that of those with LN noncompliance. Cox regression analyses showed that LN noncompliance was an independent risk factor for OS. Logistic regression analysis showed that high BMI (≥ 25 kg/m2) was an independent risk factor for preoperative prediction of LN noncompliance in cStage II/III patients. Patients with a high BMI were more likely to have LN noncompliance during surgery, especially during the dissections of #6, #8a, and #12a LN stations.


LN noncompliance was an independent risk factor for poor prognosis in patients with advanced gastric cancer (AGC) after LTG. Patients with high BMI were more likely to have LN noncompliance, especially during the dissections of #6, #8a, and #12a LN stations. LN tracing was recommended for these patients to reduce the rate of LN noncompliance.

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  1. 1.

    Torre L, Bray F, Siegel R, Ferlay J, Lortettieulent J, Jemal A. Global cancer statistics, 2012: Global Cancer Statistics, 2012. CA Cancer J Clin. 2015;65:87–108.

    Google Scholar 

  2. 2.

    Bunt AM, Hermans J, Boon MC, Cj VDV, Sasako M, Fleuren GJ, Bruijn JA. Evaluation of the extent of lymphadenectomy in a randomized trial of Western- versus Japanese-type surgery in gastric cancer. J Clin Oncol Off J Am Soc Clin Oncol. 1994;12:417–422.

    CAS  Article  Google Scholar 

  3. 3.

    Cuschieri A, Weeden S, Fielding J, Bancewicz J, Craven J, Joypaul V, Sydes M, Fayers P. Patient survival after D 1 and D 2 resections for gastric cancer: long-term results of the MRC randomized surgical trial. Br J Cancer. 1999;79:1522–1530.

    CAS  Article  Google Scholar 

  4. 4.

    Feinstein AR, Sosin DM, Wells CK. The Will Rogers phenomenon. Stage migration and new diagnostic techniques as a source of misleading statistics for survival in cancer. N Engl J Med. 1985;312:1604–1608.

    CAS  Article  Google Scholar 

  5. 5.

    Glynne-Jones R, Northover JM, Cervantes A, Group EGW. Gastric cancer: ESMO Clinical Practice Guidelines for diagnosis, treatment and follow-up. Ann Oncol Off J Eur Soc Med Oncol. 2010;21(Suppl 5(5)):v50.

    Google Scholar 

  6. 6.

    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. Extended lymph node dissection for gastric cancer: who may benefit? Final results of the randomized Dutch gastric cancer group trial. J Clin Oncol. 2004;22:2069–2077.

    CAS  Article  Google Scholar 

  7. 7.

    Songun I, Putter H, Kranenbarg EM, Sasako M, Van CDV. Surgical treatment of gastric cancer: 15-year follow-up results of the randomised nationwide Dutch D1D2 trial. Lancet Oncol. 2010;11:439–449.

    Article  Google Scholar 

  8. 8.

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

    CAS  PubMed  Google Scholar 

  9. 9.

    Lee JH, Han HS, Lee JH. A prospective randomized study comparing open vs laparoscopy-assisted distal gastrectomy in early gastric cancer: early results. Surg Endosc. 2005;19:168.

    Article  Google Scholar 

  10. 10.

    Han HS, Kim YW, Yi NJ, Fleischer GD. Laparoscopy-assisted D2 subtotal gastrectomy in early gastric cancer. Surg Laparosc Endosc Percutan Tech. 2003;13(6), 361–365.

    Article  Google Scholar 

  11. 11.

    Lee JH, Yom CK, Han HS. Comparison of long-term outcomes of laparoscopy-assisted and open distal gastrectomy for early gastric cancer. Surg Endosc. 2009;23:1759–1763.

    Article  Google Scholar 

  12. 12.

    Bonenkamp JJ, Songun I, Hermans J, Sasako M, Welvaart K, Plukker JT, Van EP, Obertop H, Gouma DJ, Taat CW. Randomised comparison of morbidity after D1 and D2 dissection for gastric cancer in 996 Dutch patients. Lancet. 1995;345(8952):745–748.

    CAS  Article  Google Scholar 

  13. 13.

    Bonenkamp JJ, Hermans J, Sasako M, Welvaart K, Songun I, Meyer S, Plukker JTM, Van Elk P, Obertop H, Gouma DJ. Extended Lymph-Node Dissection for Gastric Cancer. N Engl J Med. 1999;340:908–914.

    CAS  Article  Google Scholar 

  14. 14.

    Bonenkamp JJ, Hermans J, Sasako M, van De Velde CJ. Quality control of lymph node dissection in the Dutch randomized trial of D1 and D2 lymph node dissection for gastric cancer. Gastric Cancer. 1998;1:152–159.

    Article  Google Scholar 

  15. 15.

    de Steur WO, Hartgrink HH, Dikken JL, Putter H, van de Velde CJ. Quality control of lymph node dissection in the Dutch Gastric Cancer Trial. Br J Surg. 2015;102:1388–1393.

    Article  Google Scholar 

  16. 16.

    Claassen YHM, De Steur WO, Hartgrink HH, Dikken JL, Van Sandick JW, Van Grieken NCT, et al. Surgicopathological quality control and protocol adherence to lymphadenectomy in the critics gastric cancer trial. Ann Surg. 2018;268:1008–1013.

    Article  Google Scholar 

  17. 17.

    Claassen YHM, van Sandick JW, Hartgrink HH, Dikken JL, De Steur WO, van Grieken NCT, Boot H, Cats A, Trip AK, Jansen EPM, Meershoek-Klein Kranenbarg WM, Braak J, Putter H, van Berge Henegouwen MI, Verheij M, van de Velde CJH. Association between hospital volume and quality of gastric cancer surgery in the CRITICS trial. Br J Surg. 2018;105:728–735.

    CAS  Article  Google Scholar 

  18. 18.

    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, Group C. 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;267:638–645.

    Article  Google Scholar 

  19. 19.

    Sano T, Aiko T. New Japanese classifications and treatment guidelines for gastric cancer: revision concepts and major revised points. Gastric Cancer. 2011;14:97–100.

    Article  Google Scholar 

  20. 20.

    Lin JX, Huang CM, Zheng CH, Li P, Xie JW, Wang JB, Jun L, Chen QY, Lin M, Tu R. Evaluation of laparoscopic total gastrectomy for advanced gastric cancer: results of a comparison with laparoscopic distal gastrectomy. Surg Endosc. 2016;30:1988–1998.

    Article  Google Scholar 

  21. 21.

    Lu J, Wang W, Zheng CH, Fang C, Li P, Xie JW, Wang JB, Lin JX, Chen QY, Cao LL. 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;24:1–8.

    Google Scholar 

  22. 22.

    Tu RH, Lin JX, Zheng CH, Li P, Xie JW, Wang JB, Lu J, Chen QY, Cao LL, Lin M. Development of a nomogram for predicting the risk of anastomotic leakage after a gastrectomy for gastric cancer. Eur J Surg Oncol (EJSO). 2016;43(2);485–492.

    Article  Google Scholar 

  23. 23.

    Grambsch PM, Therneau TM. Proportional hazards tests and diagnostics based on weighted residuals. Biometrika. 1994;81:515–526.

    Article  Google Scholar 

  24. 24.

    Asoglu O, Matlim T, Kurt A, Onder SY, Kunduz E, Karanlik H, Sam B, Kapran Y, Bugra D. Guidelines for extended lymphadenectomy in gastric cancer: a prospective comparative study. Ann Surg Oncol. 2013;20:218–225.

    Article  Google Scholar 

  25. 25.

    Wagner PK, Ramaswamy A, Rüschoff J, Schmitz-Moormann P, Rothmund M. Lymph node counts in the upper abdomen: Anatomical basis for lymphadenectomy in gastric cancer. Br J Surg. 2010;78:825–827.

    Article  Google Scholar 

  26. 26.

    Maruyama K, Okabayashi K, Kinoshita T. Progress in gastric cancer surgery in Japan and its limits of radicality. World J Surg. 1987;11:418–425.

    CAS  Article  Google Scholar 

  27. 27.

    Kajitani T. The general rules for the gastric cancer study in surgery and pathology. Jpn J Surg. 1981;11:140–145.

    Article  Google Scholar 

  28. 28.

    Park SH, Sohn TS, Lee J, Lim DH, Hong ME, Kim KM, Sohn I, Jung SH, Choi MG, Lee JH. Phase III Trial to Compare Adjuvant Chemotherapy With Capecitabine and Cisplatin Versus Concurrent Chemoradiotherapy in Gastric Cancer: Final Report of the Adjuvant Chemoradiotherapy in Stomach Tumors Trial, Including Survival and Subset Analyses. J Clin Oncol. 2015;33:3130–3136.

    CAS  Article  Google Scholar 

  29. 29.

    Kim MG, Kim KC, Kim BS, Kim TH, Kim HS, Yook JH, Kim BS. A totally laparoscopic distal gastrectomy can be an effective way of performing laparoscopic gastrectomy in obese patients (body mass index>/=30). World J Surg. 2011;35:1327–1332.

    Article  Google Scholar 

  30. 30.

    Miyaki A, Imamura K, Kobayashi R, Takami M, Matsumoto J. Impact of visceral fat on laparoscopy-assisted distal gastrectomy. Surgeon. 2013;11:76–81.

    Article  Google Scholar 

  31. 31.

    Sugimoto M, Kinoshita T, Shibasaki H, Kato Y, Gotohda N, Takahashi S, Konishi M. Short-term outcome of total laparoscopic distal gastrectomy for overweight and obese patients with gastric cancer. Surg Endosc. 2013;27:4291–4296.

    Article  Google Scholar 

  32. 32.

    Lee HJ, Kim HH, Kim MC, Ryu SY, Kim W, Song KY, Cho GS, Han SU, Hyung WJ, Ryu SW. The impact of a high body mass index on laparoscopy assisted gastrectomy for gastric cancer. Surg Endosc. 2009;23:2473–2479.

    Article  Google Scholar 

  33. 33.

    Ueda J, Ichimiya H, Okido M, Kato M. The impact of visceral fat accumulation on laparoscopy-assisted distal gastrectomy for early gastric cancer. J Laparoendosc Adv Surg Tech. 2009;19(2), 157–162.

    Article  Google Scholar 

  34. 34.

    Cabanas RM. An approach for the treatment of the penile carcinoma. Cancer. 1977;39(2):456–466.

    CAS  Article  Google Scholar 

  35. 35.

    Giuliano AE, Kirgan DM, Guenther JM, Morton DL. Lymphatic mapping and sentinel lymphadenectomy for breast cancer. Ann Surg. 1994;220:391–398. Ann Surg. 188:391–398.

    CAS  Article  Google Scholar 

  36. 36.

    Morton DL, Wen DR, Wong JH, Economou JS, Cagle LA, Storm FK, Foshag LJ, Cochran AJ. Technical Details of Intraoperative Lymphatic Mapping for Early Stage Melanoma. Arch Surg. 1992;27:392–399.

    Article  Google Scholar 

  37. 37.

    Joosten JJA, Strobbe LJA, Wauters CAP, Pruszczynski M, Ruers TJM. Intraoperative lymphatic mapping and the sentinel node concept in colorectal carcinoma. Br J Surg. 1999;86:482–486

    CAS  Article  Google Scholar 

  38. 38.

    Yano K, Mitsumori N, Takahashi N, Kashiwagi H, Yanaga K. The efficiency of micrometastasis by sentinel node navigation surgery using indocyanine green and infrared ray laparoscopy system for gastric cancer. Gastric Cancer. 2012;15:287–291.

    Article  Google Scholar 

  39. 39.

    Samorani D, Fogacci T, Panzini I, Frisoni G, Accardi FG, Ricci M, Fabbri E, Nicoletti S, Flenghi L, Tamburini E. The use of indocyanine green to detect sentinel nodes in breast cancer: a prospective study. Eur J Surg Oncol. 2015;41:64–70.

    CAS  Article  Google Scholar 

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This work was supported by scientific and technological innovation joint capital projects of Fujian Province, China (No.2016Y9031). Minimally invasive medical center of Fujian Province (No. [2017]171). National key clinical specialty discipline construction program of China (No. [2012]649).

Author information




GTL, CMH, and CHZ conceived and designed the study. QYC, PL, JWX, JBW, and JXL performed the study. GTL and QYC analyzed the data. ZNH, LLC, ML, RHT, and JLL contributed the reagents/materials/analysis tools. GTL wrote the manuscript. All authors read and approved the final manuscript.

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Correspondence to Chang-Ming Huang.

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Lin, G., Chen, Q., Zheng, C. et al. Lymph Node Noncompliance Affects the Long-Term Prognosis of Patients with Gastric Cancer after Laparoscopic Total Gastrectomy. J Gastrointest Surg 24, 540–550 (2020).

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  • gastric carcinoma
  • laparoscopic total gastrectomy
  • D2 lymphadenectomy
  • LN noncompliance
  • prognosis