Advertisement

Gastric Cancer

, Volume 22, Issue 4, pp 853–863 | Cite as

Number of retrieved lymph nodes is an independent prognostic factor after total gastrectomy for patients with stage III gastric cancer: propensity score matching analysis of a multi-institution dataset

  • Shogo Hayashi
  • Mitsuro KandaEmail author
  • Seiji Ito
  • Yoshinari Mochizuki
  • Hitoshi Teramoto
  • Kiyoshi Ishigure
  • Toshifumi Murai
  • Takahiro Asada
  • Akiharu Ishiyama
  • Hidenobu Matsushita
  • Chie Tanaka
  • Daisuke Kobayashi
  • Michitaka Fujiwara
  • Kenta Murotani
  • Yasuhiro Kodera
Original Article

Abstract

Background

The prognostic significance of the number of retrieved lymph nodes (RLNs) in gastric cancer remains controversial. Therefore, we designed a multicenter collaborative database to investigate the correlation between the number of RLNs and prognosis of patients with advanced gastric cancer after curative resection.

Methods

We retrospectively analyzed 1103 patients who underwent gastrectomy for stage II/III gastric cancer between 2010 and 2014. Lymph nodes, which were retrieved by surgeons from surgically resected specimens, were validated by pathologists. A target population and the optimal cutoff were determined using receiver operating characteristic (ROC) curve analysis. After propensity score matching of eight variables, including splenectomy and adjuvant chemotherapy, the prognostic significance of RLNs was evaluated.

Results

According to ROC curve analysis, the optimum cutoff score for predicting postoperative survival was 40. After matching, the backgrounds of patients in the RLN < 40 and RLN ≥ 40 groups (n = 87 each) became well-balanced. The RLN < 40 group experienced significantly shorter relapse-free and overall survival. The prevalence of peritoneal recurrence was significantly increased in the RLN < 40 group. RLN < 40 was an independent prognostic factor in multivariable analysis, although pathological N status was not. A forest plot revealed that the RLN < 40 group was at greater risk of recurrence in most subgroups.

Conclusions

RLN < 40 was associated with an adverse prognosis of patients with stage III gastric cancer who underwent total gastrectomy.

Keywords

Gastric cancer Number of retrieved LNs Prognosis Total gastrectomy 

Notes

Acknowledgements

We thank Edanz Group (http://www.edanzediting.com/ac) for editing a draft of this manuscript.

Compliance with ethical standards

Ethical standards

All procedures followed were in accordance with the ethical standards of the responsible committee on human experimentation (institutional and national) and with the Helsinki Declaration of 1964 and later versions. Informed consent to be included in the study, or the equivalent, was obtained from all patients.

Conflict of interest

All Authors declare that they have no conflict of interest.

Supplementary material

10120_2018_902_MOESM1_ESM.tif (5.9 mb)
Supplemental Fig. 1. Receiver operating characteristic curve analysis of the numbers of RLNs associated with 2-year mortality after surgery in each category by type of gastrectomy and disease stage (TIF 6034 KB)
10120_2018_902_MOESM2_ESM.tif (5.9 mb)
Supplemental Fig. 2. Subgroup analyses of relapse-free survival associated with splenectomy (TIF 6033 KB)
10120_2018_902_MOESM3_ESM.tif (5.9 mb)
Supplemental Fig. 3. Subgroup analyses of relapse-free survival according to pathological N stage (TIF 6033 KB)
10120_2018_902_MOESM4_ESM.tif (5.9 mb)
Supplemental Fig. 4. Subgroup analyses of relapse-free survival according to the administration of postoperative adjuvant chemotherapy (TIF 6033 KB)
10120_2018_902_MOESM5_ESM.docx (14 kb)
Supplementary material 5 (DOCX 14 KB)

References

  1. 1.
    Leung WK, Wu MS, Kakugawa Y, Kim JJ, Yeoh KG, Goh KL, et al. Screening for gastric cancer in Asia: current evidence and practice. Lancet Oncol. 2008;9:279–87.CrossRefGoogle Scholar
  2. 2.
    Gonzalez CA, Agudo A. Carcinogenesis, prevention and early detection of gastric cancer: where we are and where we should go. Int J Cancer. 2012;130:745–53.CrossRefGoogle Scholar
  3. 3.
    Van Cutsem E, Sagaert X, Topal B, Haustermans K, Prenen H. Gastric cancer. Lancet. 2016;388:2654–64.CrossRefGoogle Scholar
  4. 4.
    Foo M, Leong T. Adjuvant therapy for gastric cancer: current and future directions. World J Gastroenterol. 2014;20:13718–27.CrossRefGoogle Scholar
  5. 5.
    Kanda M, Kodera Y, Sakamoto J. Updated evidence on adjuvant treatments for gastric cancer. Expert Rev Gastroenterol Hepatol. 2015;9:1–12.CrossRefGoogle Scholar
  6. 6.
    Sasako M, Sano T, Yamamoto S, Kurokawa Y, Nashimoto A, Kurita A, et al. D2 lymphadenectomy alone or with para-aortic nodal dissection for gastric cancer. N Engl J Med. 2008;359:453–62.CrossRefGoogle Scholar
  7. 7.
    Japanese Gastric Cancer Association. Japanese gastric cancer treatment guidelines 2014 (ver. 4). Gastric Cancer. 2017;20:1–19.Google Scholar
  8. 8.
    Eom BW, Joo J, Kim YW, Reim D, Park JY, Yoon HM, et al. Improved survival after adding dissection of the superior mesenteric vein lymph node (14v) to standard D2 gastrectomy for advanced distal gastric cancer. Surgery. 2014;155:408–16.CrossRefGoogle Scholar
  9. 9.
    Li F, Hong X, Hou L, Lin F, Chen P, Pang S, et al. A greater number of dissected lymph nodes is associated with more favorable outcomes in bladder cancer treated by radical cystectomy: a meta-analysis. Oncotarget. 2016;7:61284–94.Google Scholar
  10. 10.
    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
  11. 11.
    Jiang L, Yao Z, Zhang Y, Hu J, Zhao D, Zhai H, et al. Comparison of lymph node number and prognosis in gastric cancer patients with perigastric lymph nodes retrieved by surgeons and pathologists. Chin J Cancer Res. 2016;28:511–8.CrossRefGoogle Scholar
  12. 12.
    Liu JY, Peng CW, Yang XJ, Huang CQ, Li Y. The prognosis role of AJCC/UICC 8(th) edition staging system in gastric cancer, a retrospective analysis. Am J Transl Res. 2018;10:292–303.Google Scholar
  13. 13.
    Kanda M, Shimizu D, Tanaka H, Tanaka C, Kobayashi D, Hayashi M, et al. Significance of SYT8 for the detection, prediction, and treatment of peritoneal metastasis from gastric cancer. Ann Surg. 2018;267:495–503.CrossRefGoogle Scholar
  14. 14.
    Miki Y, Tokunaga M, Tanizawa Y, Bando E, Kawamura T, Terashima M. Perioperative risk assessment for gastrectomy by surgical apgar score. Ann Surg Oncol. 2014;21:2601–7.CrossRefGoogle Scholar
  15. 15.
    Zhou J, Zhang WW, Wu SG, He ZY, Sun JY, Wang Y, et al. The impact of examined lymph node count on survival in squamous cell carcinoma and adenocarcinoma of the uterine cervix. Cancer Manag Res. 2017;9:315–22.CrossRefGoogle Scholar
  16. 16.
    Degiuli M, Arolfo S, Evangelista A, Lorenzon L, Reddavid R, Staudacher C, et al. Number of lymph nodes assessed has no prognostic impact in node-negative rectal cancers after neoadjuvant therapy. Results of the “Italian Society of Surgical Oncology (S.I.C.O.) Colorectal Cancer Network” (SICO-CCN) multicentre collaborative study. Eur J Surg Oncol. 2018;44:1233–40.CrossRefGoogle Scholar
  17. 17.
    Kanda M, Murotani K, Kobayashi D, Tanaka C, Yamada S, Fujii T, et al. Postoperative adjuvant chemotherapy with S-1 alters recurrence patterns and prognostic factors among patients with stage II/III gastric cancer: a propensity score matching analysis. Surgery. 2015;158:1573–80.CrossRefGoogle Scholar
  18. 18.
    Okajima W, Komatsu S, Ichikawa D, Kosuga T, Kubota T, Okamoto K, et al. Prognostic impact of the number of retrieved lymph nodes in patients with gastric cancer. J Gastroenterol Hepatol. 2016;31:1566–71.CrossRefGoogle Scholar
  19. 19.
    Zhao B, Zhang J, Chen X, Sun T, Wang Z, Xu H, et al. The retrieval of at least 25 lymph nodes should be essential for advanced gastric cancer patients with lymph node metastasis: a retrospective analysis of single-institution database study design: Cohort study. Int J Surg. 2017;48:291–9.CrossRefGoogle Scholar
  20. 20.
    Hall MD, Schultheiss TE, Smith DD, Fakih MG, Kim J, Wong JY, et al. Impact of total lymph node count on staging and survival after neoadjuvant chemoradiation therapy for rectal cancer. Ann Surg Oncol. 2015;22(Suppl 3):580–7.CrossRefGoogle Scholar
  21. 21.
    Wu CW, Hsieh MC, Lo SS, Shen KH, Lui WY, P’Eng FK. Comparison of the UICC/AJCC 1992 and 1997 pN categories for gastric cancer patients after surgery. Hepatogastroenterology. 2001;48:279–84.Google Scholar
  22. 22.
    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.CrossRefGoogle Scholar
  23. 23.
    Hartgrink HH, van de Velde CJ, Putter H, Bonenkamp JJ, Klein Kranenbarg E, Songun I, et al. Extended lymph node dissection for gastric cancer: who may benefit? Final results of the randomized Dutch gastric cancer group trial. J Clin Oncol. 2004;22:2069–77.CrossRefGoogle Scholar
  24. 24.
    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.CrossRefGoogle Scholar
  25. 25.
    Woo Y, Goldner B, Ituarte P, Lee B, Melstrom L, Son T, et al. Lymphadenectomy with optimum of 29 lymph nodes retrieved associated with improved survival in advanced gastric cancer: a 25,000-Patient International Database Study. J Am Coll Surg. 2017;224:546–55.CrossRefGoogle Scholar
  26. 26.
    Chen T, Yan D, Zheng Z, Yang J, Dong XDE. 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
  27. 27.
    Lu J, Wang W, Zheng CH, Fang C, Li P, Xie JW, 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
  28. 28.
    Ashraf N, Hoffe S, Kim R. Adjuvant treatment for gastric cancer: chemotherapy versus radiation. Oncologist. 2013;18:1013–21.CrossRefGoogle Scholar
  29. 29.
    Macdonald JS, Smalley SR, Benedetti J, Hundahl SA, Estes NC, Stemmermann GN, et al. Chemoradiotherapy after surgery compared with surgery alone for adenocarcinoma of the stomach or gastroesophageal junction. N Engl J Med. 2001;345:725–30.CrossRefGoogle Scholar
  30. 30.
    Wong RK, Jang R, Darling G. Postoperative chemoradiotherapy vs. preoperative chemoradiotherapy for locally advanced (operable) gastric cancer: clarifying the role and technique of radiotherapy. J Gastrointest Oncol. 2015;6:89–107.Google Scholar

Copyright information

© The International Gastric Cancer Association and The Japanese Gastric Cancer Association 2018

Authors and Affiliations

  • Shogo Hayashi
    • 1
  • Mitsuro Kanda
    • 2
    Email author
  • Seiji Ito
    • 3
  • Yoshinari Mochizuki
    • 4
  • Hitoshi Teramoto
    • 5
  • Kiyoshi Ishigure
    • 6
  • Toshifumi Murai
    • 7
  • Takahiro Asada
    • 8
  • Akiharu Ishiyama
    • 9
  • Hidenobu Matsushita
    • 1
  • Chie Tanaka
    • 2
  • Daisuke Kobayashi
    • 2
  • Michitaka Fujiwara
    • 2
  • Kenta Murotani
    • 10
  • Yasuhiro Kodera
    • 2
  1. 1.Department of SurgeryTosei General HospitalSetoJapan
  2. 2.Department of Gastroenterological Surgery (Surgery II)Nagoya University Graduate School of MedicineNagoyaJapan
  3. 3.Department of Gastroenterological SurgeryAichi Cancer CenterNagoyaJapan
  4. 4.Department of SurgeryKomaki Municipal HospitalKomakiJapan
  5. 5.Department of SurgeryYokkaichi Municipal HospitalYokkaichiJapan
  6. 6.Department of SurgeryKonan Kosei HospitalKonanJapan
  7. 7.Department of SurgeryIchinomiya Municipal HospitalIchinomiyaJapan
  8. 8.Department of SurgeryGifu Prefectural Tajimi HospitalTajimiJapan
  9. 9.Department of SurgeryOkazaki City HospitalOkazakiJapan
  10. 10.Biostatistics Center, Graduate School of MedicineKurume UniversityKurumeJapan

Personalised recommendations