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Increasing the Number of Examined Lymph Nodes is a Prerequisite for Improvement in the Accurate Evaluation of Overall Survival of Node-Negative Gastric Cancer Patients

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

Abstract

Background

This study aims to elucidate whether increasing the number of examined lymph nodes (NELN) is mandatory for the accurate prognosis of node-negative gastric cancer (GC) patients after curative gastrectomy in Eastern countries (China and Japan).

Methods

The clinicopathological data of 2455 GC patients (including 1137 node-negative cases) were included to demonstrate whether a minimum NELN is inevitable for guaranteeing the accurate prognosis of node-negative GC patients after curative gastrectomy.

Results

Survival analyses revealed that the NELN significantly positively correlated with overall survival (p < 0.001) and was an independent prognostic predictor (hazard ratio 0.447; p = 0.025) of 1137 node-negative GC patients. Stratum analysis within the Kaplan–Meier method showed that sex, tumor size, and extent of lymphadenectomy did not affect the NELN in predicting the prognosis of all node-negative GC patients. Stage migration was mainly detected in the subgroup of node-negative GC Chinese patients who presented considerably lower mean NELN and more advanced staging than patients from Japan. The NELN was identified as the most intensively independent predictor of prognosis of 600 node-negative GC patients from China, with the smallest Akaike information criterion (176.964) and Bayesian information criterion values (194.552). These findings indicate that increasing the NELN is a prerequisite to guaranteeing precise TNM classification.

Conclusions

The NELN should be considered a mandatory requirement for improving the accuracy of prognostic evaluation of GC patients, especially for advanced-stage patients.

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References

  1. Deng J, Zhang R, Pan Y, Wang B, Wu L, Jiao X, et al. Comparison of the staging of regional lymph nodes using the sixth and seventh editions of the tumor-node-metastasis (TNM) classification system for the evaluation of overall survival in gastric cancer patients: findings of a case-control analysis involving a single institution in China. Surgery. 2014;56:64–74.

    Article  Google Scholar 

  2. Marrelli D, Morgagni P, de Manzoni G, Coniglio A, Marchet A, Saragoni L, et al. Prognostic value of the 7th AJCC/UICC TNM classification of noncardia gastric cancer: analysis of a large series from specialized Western centers. Ann Surg. 2012;255:486–91.

    Article  PubMed  Google Scholar 

  3. de Manzoni G, Verlato G, Roviello F, Morgagni P, Di Leo A, Saragoni L, et al. The new TNM classification of lymph node metastasis minimises stage migration problems in gastric cancer patients. Br J Cancer. 2002;87:171–4.

    Article  PubMed  PubMed Central  Google Scholar 

  4. Bouvier AM, Haas O, Piard F, Roignot P, Bonithon-Kopp C, Faivre J. How many nodes must be examined to accurately stage gastric carcinomas? Results from a population based study. Cancer. 2002;94:2862–6.

    Article  PubMed  Google Scholar 

  5. Biffi R, Botteri E, Cenciarelli S, Luca F, Pozzi S, Valvo M, et al. Impact on survival of the number of lymph nodes removed in patients with node-negative gastric cancer submitted to extended lymph node dissection. Eur J Surg Oncol. 2011;37:305–11.

    Article  CAS  PubMed  Google Scholar 

  6. Li Y, Du P, Zhou Y, Cheng Q, Chen D, Wang D, et al. Lymph node micrometastases is a poor prognostic factor for patients in pN0 gastric cancer: a meta-analysis of observational studies. J Surg Res. 2014;191:413–22.

    Article  PubMed  Google Scholar 

  7. Huang JY, Xu YY, Li M, Sun Z, Zhu Z, Song YX, et al. The prognostic impact of occult lymph node metastasis in node-negative gastric cancer: a systematic review and meta-analysis. Ann Surg Oncol. 2013;20:3927–34.

    Article  PubMed  Google Scholar 

  8. Song W, Yuan Y, Wang L, He W, Zhang X, Chen C, et al. The prognostic value of lymph nodes dissection number on survival of patients with lymph node-negative gastric cancer. Gastroenterol Res Pract. 2014;2014:603194.

    Article  PubMed  PubMed Central  Google Scholar 

  9. Bunt AM, Hermans J, van de Velde CJ, Sasako M, Hoefsloot FA, Fleuren G, et al. Lymph node retrieval in a randomized trial on Western-type versus Japanese-type surgery in gastric cancer. J Clin Oncol. 1996;14:2289–94.

    CAS  PubMed  Google Scholar 

  10. Candela FC, Urmacher C, Brennan MF. Comparison of the conventional method of lymph node staging with a comprehensive fat-clearing method for gastric adenocarcinoma. Cancer. 1990;66:1828–32.

    Article  CAS  PubMed  Google Scholar 

  11. Sobin LH, Fleming ID. TNM classification of malignant tumors. Cancer. 1997;80:1803–4.

    CAS  PubMed  Google Scholar 

  12. Karpeh MS, Leon L, Klimstra D, Brennan MF. Lymph node staging in gastric cancer: is location more important than number? An analysis of 1038 patients. Ann Surg. 2000;232:362–71.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Deng JY, Liang H, Sun D, Pan Y, Zhang RP, Wang BG, et al. Outcome in relation to numbers of nodes harvested in lymph node-positive gastric cancer. Eur J Surg Oncol. 2009;35:814–9.

    Article  CAS  PubMed  Google Scholar 

  14. Sobin L, Gospodarowicz M, Wittekind C. TNM classification of malignant tumours. 7th ed. New York: Wiley; 2009.

    Google Scholar 

  15. 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;18:1219–21.

    Article  PubMed  Google Scholar 

  16. Baiocchi GL, Tiberio GA, Minicozzi AM, Morgagni P, Marrelli D, Bruno L, et al. A multicentric Western analysis of prognostic factors in advanced, node-negative gastric cancer patients. Ann Surg. 2010;252:70–3.

    Article  PubMed  Google Scholar 

  17. He H, Shen Z, Wang X, Qin J, Sun Y, Qin X. Survival benefit of greater number of lymph nodes dissection for advanced node-negative gastric cancer patients following radical gastrectomy. Jpn J Clin Oncol. 2016;46:63–70.

    Article  PubMed  Google Scholar 

  18. Jiao XG, Deng JY, Zhang RP, Wu LL, Wang L, Liu HG, et al. Prognostic value of number of examined lymph nodes in patients with node-negative gastric cancer. World J Gastroenterol. 2014;20:3640–8.

    Article  PubMed  PubMed Central  Google Scholar 

  19. Li B, Li Y, Wang W, Qiu H, Seeruttun SR, Fang C, et al. Incorporation of N0 stage with insufficient numbers of lymph nodes into N1 stage in the seventh edition of the TNM classification improves prediction of prognosis in gastric cancer: results of a single-institution study of 1258 Chinese patients. Ann Surg Oncol. 2016;23:142–8.

    Article  PubMed  Google Scholar 

  20. Jaehne J, Meyer HJ, Maschek H, Geerlings H, Burns E, Pichlmayr R. Lymphadenectomy in gastric adenocarcinoma: a prospective and prognostic study. Arch Surg. 1992;127:290–4.

    Article  CAS  PubMed  Google Scholar 

  21. Nakajima T. Gastric cancer treatment guidelines in Japan. Gastric Cancer. 2002;5:1–5.

    Article  PubMed  Google Scholar 

  22. Smith DD, Schwarz RR, Schwartz 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.

    Article  PubMed  Google Scholar 

  23. Nitsche U, Maak M, Schuster T, Künzli B, Langer R, Slotta-Huspenina J, et al. Prediction of prognosis is not improved by the seventh and latest edition of the TNM classification for colorectal cancer in a single-center collective. Ann Surg. 2011;254:793–800.

    Article  PubMed  Google Scholar 

  24. Cho YK, Chung JW, Kim JK, Ahn YS, Kim MY, Park YO, et al. Comparison of 7 staging systems for patients with hepatocellular carcinoma undergoing transarterial chemoembolization. Cancer. 2008;112:352–61.

    Article  CAS  PubMed  Google Scholar 

  25. Songun I, Putter H, Kranenbarg EM, Sasako M, van de Velde CJ. Surgical treatment of gastric cancer: 15-year follow-up results of the randomised nationwide Dutch D1D2 trial. Lancet Oncol. 2010;11:439–49.

    Article  PubMed  Google Scholar 

  26. Deng J, Liang H, Sun D, Zhang R, Zhan H, Wang X. Prognosis of gastric cancer patients with negative node metastasis following curative resection. Outcomes of the survival and recurrence. Can J Gastroenterol. 2008;22:835–9.

    Article  PubMed  PubMed Central  Google Scholar 

  27. Jeong JY, Kim MG, Ha TK, Kwon SJ. Prognostic factors on overall survival in lymph node negative gastric cancer patients who underwent curative resection. J Gastric Cancer. 2012;12:210–6.

    Article  PubMed  PubMed Central  Google Scholar 

  28. Chu X, Yang ZF. Impact on survival of the number of lymph nodes resected in patients with lymph node-negative gastric cancer. World J Surg Oncol. 2015;13:192.

    Article  PubMed  PubMed Central  Google Scholar 

  29. Xu D, Huang Y, Geng Q, Guan Y, Li Y, Wang W, et al. Effect of lymph node number on survival of patients with lymph node-negative gastric cancer according to the 7th edition UICC TNM system. PLoS One. 2012;7:e38681.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Deng J, Zhang R, Zhang L, Liu Y, Hao X, Liang H. Negative node count improvement prognostic prediction of the seventh edition of the TNM classification for gastric cancer. PLoS One. 2013;8:e80082.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Deng JY, Liang H, Wang DC, Sun D, Ding X, Pan Y, et al. Enhancement the prediction of postoperative survival in gastric cancer by combining the negative lymph node count with ratio between positive and examined lymph nodes. Ann Surg Oncol. 2010;17:1043–51.

    Article  PubMed  Google Scholar 

  32. Deng J, Sun D, Pan Y, Zhang L, Zhang R, Wang D, et al. Ratio between negative and positive lymph nodes is suitable for evaluation the prognosis of gastric cancer patients with positive node metastasis following curative surgery. PLoS One. 2012;7:e43925.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Deng J, Zhang R, Wu LL, Zhang L, Wang X, Liu Y, et al. Superiority of the ratio between negative and positive lymph nodes for predicting the prognosis for patients with gastric cancer. Ann Surg Oncol. 2015;22:1258–66.

    Article  PubMed  Google Scholar 

  34. Yonemura Y, Endo Y, Hayashi I, Kawamura T, Yun HY, Bandou E. Proliferative activity of micrometastases in the lymph nodes of patients with gastric cancer. Br J Surg. 2007;94:731–6.

    Article  CAS  PubMed  Google Scholar 

  35. Jeuck TL, Wittekind C. Gastric carcinoma: stage migration by immunohistochemically detected lymph node micrometastases. Gastric Cancer. 2015;18:100–8.

    Article  CAS  PubMed  Google Scholar 

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Funding

This study was supported in part by Grants from the Program of the National Natural Science Foundation of China (Number 81572372), the Application Foundation and Advanced Technology Program of Tianjin Municipal Science and Technology Commission (Number 15JCYBJC24800), and the National Key Clinical Specialist Construction Programs of China (Number 2013-544).

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Correspondence to Yasuyuki Seto or Han Liang.

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Additional information

Jingyu Deng and Hiroharu Yamashita contributed equally to this work and should be considered as co-first authors.

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Deng, J., Yamashita, H., Seto, Y. et al. Increasing the Number of Examined Lymph Nodes is a Prerequisite for Improvement in the Accurate Evaluation of Overall Survival of Node-Negative Gastric Cancer Patients. Ann Surg Oncol 24, 745–753 (2017). https://doi.org/10.1245/s10434-016-5513-8

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  • DOI: https://doi.org/10.1245/s10434-016-5513-8

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