Log in

A Nomogram for Predicting Overall Survival of Gastric Cancer Patients with Insufficient Lymph Nodes Examined

  • Original Article
  • Published:
Journal of Gastrointestinal Surgery

Abstract

Insufficient number of examined lymph nodes (eLNs) was considered to increase significantly the risk of stage migration in gastric cancer patients. The aim of our study is to establish a nomogram predicting the overall survival (OS) for patients with an insufficient number of eLNs. A total of 872 gastric cancer patients with extended lymphadenectomies were assigned randomly (2:1) to the development cohort and the validation cohort. The nomogram was established based on the Cox regression model using the development cohort. The concordance index (C-index) was used to evaluate the discriminative ability. We also compared our model with two other staging systems. Using multivariate analysis, age, sex, tumor location, depth of invasion, macroscopic type, lymphovascular invasion, the number of eLNs, and metastatic lymph nodes were selected and incorporated into the nomogram. The C-index of the nomogram was 0.742 and 0.743 in development and validation cohorts, respectively, which were significantly superior to the C-indices (range 0.705–0.712, all P < 0.001) of American Joint Committee on Cancer (AJCC) seventh edition and lymph node ratio staging systems in both cohorts. We established a nomogram which could predict accurately OS for gastric cancer patients with insufficient number of eLNs.

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

References

Author names in bold designate shared co-first authorship

  1. Edge SB, Byrd DR, Compton CC, Fritz AG, Greene FL, Trotti A. AJCC cancer staging manual. 7th ed. New York: Springer-Verlag; 2010.

    Google Scholar 

  2. 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: 7114–7124.

    Article  PubMed  Google Scholar 

  3. Coburn NG, Swallow CJ, Kiss A, Law C. Significant regional variation in adequacy of lymph node assessment and survival in gastric cancer. Cancer 2006; 107: 2143–2151.

    Article  PubMed  Google Scholar 

  4. Baxter NN, Tuttle TM. Inadequacy of lymph node staging in gastric cancer patients: a population-based study. Ann Surg Oncol 2005; 12: 981–987.

    Article  PubMed  Google Scholar 

  5. Inoue K, Nakane Y, Iiyama H, Sato M, Kanbara T, Nakai K, Okumura S, Yamamichi K, Hioki K. The superiority of ratio-based lymph node staging in gastric carcinoma. Ann Surg Oncol 2002; 9: 27–34.

    Article  PubMed  Google Scholar 

  6. Kong SH, Lee HJ, Ahn HS, Kim JW, Kim WH, Lee KU, Yang HK. Stage migration effect on survival in gastric cancer surgery with extended lymphadenectomy: the reappraisal of positive lymph node ratio as a proper N-staging. Ann Surg 2012; 255: 50–58.

    Article  PubMed  Google Scholar 

  7. 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: 775–784.

    Article  PubMed  Google Scholar 

  8. Son T, Hyung WJ, Lee JH, Kim YM, Kim HI, An JY, Cheong JH, Noh SH. Clinical implication of an insufficient number of examined lymph nodes after curative resection for gastric cancer. Cancer 2012; 118: 4687–4693.

    Article  PubMed  Google Scholar 

  9. Sun Z, Zhu GL, Lu C, Guo PT, Huang BJ, Li K, Xu Y, Li DM, Wang ZN, Xu HM. The impact of N-ratio in minimizing stage migration phenomenon in gastric cancer patients with insufficient number or level of lymph node retrieved: results from a Chinese mono-institutional study in 2159 patients. Ann Oncol 2009; 20: 897–905.

    Article  CAS  PubMed  Google Scholar 

  10. Maduekwe UN, Lauwers GY, Fernandez-Del-Castillo C, Berger DL, Ferguson CM, Rattner DW, Yoon SS. New metastatic lymph node ratio system reduces stage migration in patients undergoing D1 lymphadenectomy for gastric adenocarcinoma. Ann Surg Oncol 2010; 17: 1267–1277.

    Article  PubMed  PubMed Central  Google Scholar 

  11. Wang J, Dang P, Raut CP, Pandalai PK, Maduekwe UN, Rattner DW, Lauwers GY, Yoon SS. Comparison of a lymph node ratio-based staging system with the 7th AJCC system for gastric cancer: analysis of 18,043 patients from the SEER database. Ann Surg 2012; 255: 478–485.

    Article  PubMed  Google Scholar 

  12. Wang J, Hassett JM, Dayton MT, Kulaylat MN. The prognostic superiority of log odds of positive lymph nodes in stage III colon cancer. J Gastrointest Surg 2008; 12: 1790–1796.

    Article  PubMed  Google Scholar 

  13. Sun Z, Xu Y, Li de M, Wang ZN, Zhu GL, Huang BJ, Li K, Xu HM. Log odds of positive lymph nodes: a novel prognostic indicator superior to the number-based and the ratio-based N category for gastric cancer patients with R0 resection. Cancer 2010; 116: 2571–2580.

    Article  PubMed  Google Scholar 

  14. Deng J, Zhang R, Wu L, Zhang L, Wang X, Liu Y, Hao X, Liang H. Superiority of the ratio between negative and positive lymph nodes for predicting the prognosis for patients with gastric cancer. Ann Surg Oncol 2015; 22: 1258–1266.

    Article  PubMed  Google Scholar 

  15. Iasonos A, Schrag D, Raj GV, Panageas KS. How to build and interpret a nomogram for cancer prognosis. J Clin Oncol 2008; 26: 1364–1370.

    Article  PubMed  Google Scholar 

  16. Han DS, Suh YS, Kong SH, Lee HJ, Choi Y, Aikou S, Sano T, Park BJ, Kim WH, Yang HK. Nomogram predicting long-term survival after d2 gastrectomy for gastric cancer. J Clin Oncol 2012; 30: 3834–3840.

    Article  PubMed  Google Scholar 

  17. Song KY, Park YG, Jeon HM, Park CH. A nomogram for predicting individual survival of patients with gastric cancer who underwent radical surgery with extended lymph node dissection. Gastric Cancer 2014; 17: 287–293.

    Article  PubMed  Google Scholar 

  18. Eom BW, Ryu KW, Nam BH, Park Y, Lee HJ, Kim MC, Cho GS, Kim CY, Ryu SW, Shin DW, Hyung WJ, Lee JH. Survival nomogram for curatively resected Korean gastric cancer patients: multicenter retrospective analysis with external validation. PLoS One 2015; 10: e0119671.

    Article  PubMed  PubMed Central  Google Scholar 

  19. Hirabayashi S, Kosugi S, Isobe Y, Nashimoto A, Oda I, Hayashi K, Miyashiro I, Tsujitani S, Kodera Y, Seto Y, Furukawa H, Ono H, Tanabe S, Kaminishi M, Nunobe S, Fukagawa T, Matsuo R, Nagai T, Katai H, Wakai T, Akazawa K. Development and external validation of a nomogram for overall survival after curative resection in serosa-negative, locally advanced gastric cancer. Ann Oncol 2014; 25: 1179–1184.

    Article  CAS  PubMed  Google Scholar 

  20. Kattan MW, Karpeh MS, Mazumdar M, Brennan MF. Postoperative nomogram for disease-specific survival after an R0 resection for gastric carcinoma. J Clin Oncol 2003; 21: 3647–3650.

    Article  PubMed  Google Scholar 

  21. 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: 439–449.

    Article  PubMed  Google Scholar 

  22. Okines A, Verheij M, Allum W, Cunningham D, Cervantes A, Group EGW. Gastric cancer: ESMO Clinical Practice Guidelines for diagnosis, treatment and follow-up. Ann Oncol 2010; 21 Suppl 5: v50–54.

    Article  PubMed  Google Scholar 

  23. Memon MA, Subramanya MS, Khan S, Hossain MB, Osland E, Memon B. Meta-analysis of D1 versus D2 gastrectomy for gastric adenocarcinoma. Ann Surg 2011; 253: 900–911.

    Article  PubMed  Google Scholar 

  24. Balachandran VP, Gonen M, Smith JJ, DeMatteo RP. Nomograms in oncology: more than meets the eye. The Lancet Oncology 2015; 16: e173-e180.

    Article  PubMed  PubMed Central  Google Scholar 

  25. Harrell FE, Jr., Lee KL, Mark DB. Multivariable prognostic models: issues in develo** models, evaluating assumptions and adequacy, and measuring and reducing errors. Stat Med 1996; 15: 361–387.

    Article  PubMed  Google Scholar 

  26. Harrell FE, Jr., Califf RM, Pryor DB, Lee KL, Rosati RA. Evaluating the yield of medical tests. JAMA 1982; 247: 2543–2546.

    Article  PubMed  Google Scholar 

  27. Huitzil-Melendez FD, Capanu M, O’Reilly EM, Duffy A, Gansukh B, Saltz LL, Abou-Alfa GK. Advanced hepatocellular carcinoma: which staging systems best predict prognosis? J Clin Oncol 2010; 28: 2889–2895.

    Article  PubMed  PubMed Central  Google Scholar 

  28. Siewert JR, Bottcher K, Stein HJ, Roder JD. Relevant prognostic factors in gastric cancer: ten-year results of the German Gastric Cancer Study. Ann Surg 1998; 228: 449–461.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Dicken BJ, Bigam DL, Cass C, Mackey JR, Joy AA, Hamilton SM. Gastric adenocarcinoma: review and considerations for future directions. Ann Surg 2005; 241: 27–39.

    PubMed  PubMed Central  Google Scholar 

  30. Kim JP, Lee JH, Kim SJ, Yu HJ, Yang HK. Clinicopathologic characteristics and prognostic factors in 10 783 patients with gastric cancer. Gastric Cancer 1998; 1: 125–133.

    Article  PubMed  Google Scholar 

  31. Greene FL, Page DL, Fleming ID, Fritz AG, Balch CM, Haller DG, Morrow M. AJCC cancer staging manual. 6th ed. New York: Springer-Verlag; 2002.

    Book  Google Scholar 

  32. Fleming ID, Cooper JS, Henson DE, Hutter RVP, Kennedy BJ, Murphy GP, O’Sullivan B, Sobin LH, Yarbro JW. AJCC cancer staging manual. 5th ed. Philadelphia: Lippincott-Raven; 1997.

    Google Scholar 

  33. 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: 2862–2866.

    Article  PubMed  Google Scholar 

  34. Lee HK, Yang HK, Kim WH, Lee KU, Choe KJ, Kim JP. Influence of the number of lymph nodes examined on staging of gastric cancer. Br J Surg 2001; 88: 1408–1412.

    Article  CAS  PubMed  Google Scholar 

  35. 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.

    Article  CAS  PubMed  Google Scholar 

  36. Bunt AM, Hermans J, van de Velde CJ, Sasako M, Hoefsloot FA, Fleuren G, Bruijn JA. Lymph node retrieval in a randomized trial on western-type versus Japanese-type surgery in gastric cancer. J Clin Oncol 1996; 14: 2289–2294.

    Article  CAS  PubMed  Google Scholar 

  37. Dhar DK, Kubota H, Tachibana M, Kotoh T, Tabara H, Masunaga R, Kohno H, Nagasue N. Body mass index determines the success of lymph node dissection and predicts the outcome of gastric carcinoma patients. Oncology 2000; 59: 18–23.

    Article  CAS  PubMed  Google Scholar 

  38. Dudeja V, Habermann EB, Zhong W, Tuttle TM, Vickers SM, Jensen EH, Al-Refaie WB. Guideline recommended gastric cancer care in the elderly: insights into the applicability of cancer trials to real world. Ann Surg Oncol 2011; 18: 26–33.

    Article  PubMed  Google Scholar 

  39. Marchet A, Mocellin S, Ambrosi A, Morgagni P, Garcea D, Marrelli D, Roviello F, de Manzoni G, Minicozzi A, Natalini G, De Santis F, Baiocchi L, Coniglio A, Nitti D, Italian Research Group for Gastric C. The ratio between metastatic and examined lymph nodes (N ratio) is an independent prognostic factor in gastric cancer regardless of the type of lymphadenectomy: results from an Italian multicentric study in 1853 patients. Ann Surg 2007; 245: 543–552.

    Article  PubMed  PubMed Central  Google Scholar 

  40. Nitti D, Marchet A, Olivieri M, Ambrosi A, Mencarelli R, Belluco C, Lise M. Ratio Between Metastatic and Examined Lymph Nodes Is an Independent Prognostic Factor After D2 Resection for Gastric Cancer: Analysis of a Large European Monoinstitutional Experience. Annals of Surgical Oncology 2003; 10: 1077–1085.

    Article  PubMed  Google Scholar 

  41. Yang Y, Zhang YJ, Zhu Y, Cao JZ, Yuan ZY, Xu LM, Wu JX, Wang W, Wu T, Lu B, Zhu SY, Qian LT, Zhang FQ, Hou XR, Liu QF, Li YX. Prognostic nomogram for overall survival in previously untreated patients with extranodal NK/T-cell lymphoma, nasal-type: a multicenter study. Leukemia 2015; 29: 1571–1577.

    Article  CAS  PubMed  Google Scholar 

  42. Wang Y, Li J, **a Y, Gong R, Wang K, Yan Z, Wan X, Liu G, Wu D, Shi L, Lau W, Wu M, Shen F. Prognostic nomogram for intrahepatic cholangiocarcinoma after partial hepatectomy. J Clin Oncol 2013; 31: 1188–1195.

    Article  PubMed  Google Scholar 

  43. Kattan MW, Leung DH, Brennan MF. Postoperative nomogram for 12-year sarcoma-specific death. J Clin Oncol 2002; 20: 791–796.

    Article  PubMed  Google Scholar 

  44. Kim Y, Spolverato G, Ejaz A, Squires MH, Poultsides G, Fields RC, Bloomston M, Weber SM, Votanopoulos K, Acher AW, ** LX, Hawkins WG, Schmidt C, Kooby D, Worhunsky D, Saunders N, Levine EA, Cho CS, Maithel SK, Pawlik TM. A nomogram to predict overall survival and disease-free survival after curative resection of gastric adenocarcinoma. Ann Surg Oncol 2015; 22: 1828–1835.

    Article  PubMed  Google Scholar 

  45. Sasako M, Sakuramoto S, Katai H, Kinoshita T, Furukawa H, Yamaguchi T, Nashimoto A, Fujii M, Nakajima T, Ohashi Y. Five-year outcomes of a randomized phase III trial comparing adjuvant chemotherapy with S-1 versus surgery alone in stage II or III gastric cancer. J Clin Oncol 2011; 29: 4387–4393.

    Article  CAS  PubMed  Google Scholar 

  46. Bang YJ, Kim YW, Yang HK, Chung HC, Park YK, Lee KH, Lee KW, Kim YH, Noh SI, Cho JY, Mok YJ, Kim YH, Ji J, Yeh TS, Button P, Sirzen F, Noh SH. Adjuvant capecitabine and oxaliplatin for gastric cancer after D2 gastrectomy (CLASSIC): a phase 3 open-label, randomised controlled trial. Lancet 2012; 379: 315–321.

    Article  CAS  PubMed  Google Scholar 

  47. Kim DH, Kim SM, Hyun JK, Choi MG, Noh JH, Sohn TS, Bae JM, Kim S. Changes in postoperative recurrence and prognostic risk factors for patients with gastric cancer who underwent curative gastric resection during different time periods. Ann Surg Oncol 2013; 20: 2317–2327.

    Article  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Contributions

Research idea and study design: LFN, XHM, and WPL; data analysis/interpretation: WPL, XFT, and GBC; statistical analysis: WPL and LFN; supervision or mentorship: LFN and XHM. All the authors contributed important intellectual content for the overall work. LFN and XHM take responsibility for the honesty and accuracy of the present study.

Corresponding authors

Correspondence to Fu-nan Liu MD, PhD or Hui-mian Xu MD, PhD.

Ethics declarations

This study was approved by the Institutional Ethics Committee of China Medical University.

Grant Support

This work was supported by the National Natural Science Foundation of China (No. 81001092) and the Natural Science Foundation of Liaoning Province of China (No. 2013021097).

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Wang, Pl., **ao, Ft., Gong, Bc. et al. A Nomogram for Predicting Overall Survival of Gastric Cancer Patients with Insufficient Lymph Nodes Examined. J Gastrointest Surg 21, 947–956 (2017). https://doi.org/10.1007/s11605-017-3401-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11605-017-3401-6

Keywords

Navigation