Advertisement

Risk Factors Associated with Lymph Node Metastasis for Early Gastric Cancer Patients Who Underwent Non-curative Endoscopic Resection: a Systematic Review and Meta-analysis

  • Bochao Zhao
  • Jingting Zhang
  • Jiale Zhang
  • Rui Luo
  • Zhenning Wang
  • Huimian Xu
  • Baojun HuangEmail author
Original Article
  • 197 Downloads

Abstract

Background

Recently, increased evidence indicated that additional surgery should be performed in highly selected patients with non-curative endoscopic resection. In this study, we performed a systematic review and meta-analysis to evaluate the risk factors associated with lymph node metastasis for the patients with non-curative endoscopic resection of early gastric cancer.

Methods

The related studies were identified by searching PubMed and Embase databases. According to the status of lymph node metastasis, all patients were classified into node-negative group and node-positive group. The relevant clinicopathologic factors were extracted, and the pooled odds ratio (OR) and 95% confidence interval (CIs) were assessed using a fixed effects model or random effects model.

Results

A total of nine relevant studies involving 1720 early gastric cancer patients who underwent additional surgery following the non-curative endoscopic resection were included in this meta-analysis. The results indicated that deeper submucosal invasion (SM2) (OR 3.44, 95% CI 1.94–6.10, P < 0.001; I2 = 0%), positive vertical margin (OR 2.35, 95% CI 1.57–3.53, P < 0.001; I2 = 0%), lymphatic invasion (OR 11.06, 95% CI 5.47–22.36, P < 0.001; I2 = 0%), and vascular invasion (OR 2.79, 95% CI 1.68–4.64, P < 0.001; I2 = 0%) were significantly associated with lymph node metastasis for these patients. However, horizontal margin, tumor size, differentiation type, and ulceration were not identified as risk factors associated with lymph node metastasis.

Conclusion

Lymphatic invasion, vascular invasion, deeper submucosal invasion (SM2), and positive vertical margin should be strongly considered in selecting the candidates for additional surgery treatment.

Keywords

Early gastric cancer Endoscopic submucosal dissection (ESD) Non-curative endoscopic resection Lymph node metastasis Additional surgery 

Notes

Author Contributions

Study conception and design: Bochao Zhao and Baojun Huang; collection and acquisition of data: Bochao Zhao, Jiale Zhang, and Rui Luo; analysis and interpretation of data: Bochao Zhao, Jingting Zhang, and Jiale Zhang; drafting of manuscript: Bochao Zhao and Jingting Zhang; critical revision: Zhenning Wang, Huimian Xu, and Baojun Huang.

Compliance with Ethical Standards

Conflict of Interest

The authors declare that they have no conflict of interest.

References

  1. 1.
    Torre LA, Bray F, Siegel RL, et al. Global cancer statistics, 2012. CA Cancer J Clin 2015;65:87–108.CrossRefPubMedGoogle Scholar
  2. 2.
    Maehara Y, Kakeji Y, Oda S, et al. Time trends of surgical treatment and the prognosis for Japanese patients with gastric cancer. Br J Cancer 2000;83:986–91.CrossRefPubMedPubMedCentralGoogle Scholar
  3. 3.
    Oda I, Oyama T, Abe S, et al. Preliminary results of multicenter questionnaire study on long-term outcomes of curative endoscopic submucosal dissection for early gastric cancer. Dig Endosc 2014;26:214–9.CrossRefPubMedGoogle Scholar
  4. 4.
    Park CH, Shin S, Park JC, et al. Long-term outcome of early gastric cancer after endoscopic submucosal dissection: expanded indication is comparable to absolute indication. Dig Liver Dis 2013;45:651–6.CrossRefPubMedGoogle Scholar
  5. 5.
    Petruzziello L, Campanale M, Spada C, et al. Endoscopic submucosal dissection of gastric superficial neoplastic lesions: a single Western center experience. United European Gastroenterol J 2018;6:203–212.CrossRefPubMedPubMedCentralGoogle Scholar
  6. 6.
    Hatta W, Gotoda T, Oyama T, et al. Is radical surgery necessary in all patients who do not meet the curative criteria for endoscopic submucosal dissection in early gastric cancer? A multi-center retrospective study in Japan. J Gastroenterol 2017;52:175–184.CrossRefPubMedGoogle Scholar
  7. 7.
    Han JP, Hong SJ, Kim HK, et al. Risk stratification and management of non-curative resection after endoscopic submucosal dissection for early gastric cancer. Surg Endosc 2016;30:184–9.CrossRefPubMedGoogle Scholar
  8. 8.
    Choi JY, Jeon SW, Cho KB, et al. Non-curative endoscopic resection does not always lead to grave outcomes in submucosal invasive early gastric cancer. Surg Endosc 2015;29:1842–9.CrossRefPubMedGoogle Scholar
  9. 9.
    Japanese gastric cancer treatment guidelines 2010 (ver. 3). Gastric Cancer 2011;14:113–23.Google Scholar
  10. 10.
    Eom BW, Kim YI, Kim KH, et al. Survival benefit of additional surgery after noncurative endoscopic resection in patients with early gastric cancer. Gastrointest Endosc 2017;85:155–163.e3.CrossRefPubMedGoogle Scholar
  11. 11.
    Suzuki S, Gotoda T, Hatta W, et al. Survival benefit of additional surgery after non-curative endoscopic submucosal dissection for early gastric cancer: a propensity score matching analysis. Ann Surg Oncol 2017;24:3353–3360.CrossRefPubMedGoogle Scholar
  12. 12.
    Son SY, Park JY, Ryu KW, et al. The risk factors for lymph node metastasis in early gastric cancer patients who underwent endoscopic resection: is the minimal lymph node dissection applicable? A retrospective study. Surg Endosc 2013;27:3247–53.CrossRefPubMedGoogle Scholar
  13. 13.
    Kawata N, Kakushima N, Takizawa K, et al. Risk factors for lymph node metastasis and long-term outcomes of patients with early gastric cancer after non-curative endoscopic submucosal dissection. Surg Endosc 2017;31:1607–1616.CrossRefPubMedGoogle Scholar
  14. 14.
    Sunagawa H, Kinoshita T, Kaito A, et al. Additional surgery for non-curative resection after endoscopic submucosal dissection for gastric cancer: a retrospective analysis of 200 cases. Surg Today 2017;47:202–209.CrossRefPubMedGoogle Scholar
  15. 15.
    Ito H, Inoue H, Ikeda H, et al. Surgical outcomes and clinicopathological characteristics of patients who underwent potentially noncurative endoscopic resection for gastric cancer: a report of a single-center experience. Gastroenterol Res Pract 2013;2013:427405.CrossRefPubMedPubMedCentralGoogle Scholar
  16. 16.
    Kim ER, Lee H, Min BH, et al. Effect of rescue surgery after non-curative endoscopic resection of early gastric cancer. Br J Surg 2015;102:1394–401.CrossRefPubMedGoogle Scholar
  17. 17.
    Toyokawa T, Ohira M, Tanaka H, et al. Optimal management for patients not meeting the inclusion criteria after endoscopic submucosal dissection for gastric cancer. Surg Endosc 2016;30:2404–14.CrossRefPubMedGoogle Scholar
  18. 18.
    Suzuki H, Oda I, Abe S, et al. Clinical outcomes of early gastric cancer patients after noncurative endoscopic submucosal dissection in a large consecutive patient series. Gastric Cancer 2017;20:679–689.CrossRefPubMedGoogle Scholar
  19. 19.
    Kikuchi S, Kuroda S, Nishizaki M, et al. Management of early gastric cancer that meet the indication for radical lymph node dissection following endoscopic resection: a retrospective cohort analysis. BMC Surg 2017;17:72.CrossRefPubMedPubMedCentralGoogle Scholar
  20. 20.
    Jung DH, Huh CW, Kim JH, et al. Risk-stratification model based on lymph node metastasis after noncurative endoscopic resection for early gastric cancer. Ann Surg Oncol 2017;24:1643–1649.CrossRefPubMedGoogle Scholar
  21. 21.
    Ishii S, Yamashita K, Kato H, et al. Predictive factors for lymph node metastasis in additional gastrectomy after endoscopic resection of cT1aN0 gastric cancer. Surg Today 2016;46:1031–8.CrossRefPubMedGoogle Scholar
  22. 22.
    Noh GY, Ku HR, Kim YJ, et al. Clinical outcomes of early gastric cancer with lymphovascular invasion or positive vertical resection margin after endoscopic submucosal dissection. Surg Endosc 2015;29:2583–9.CrossRefPubMedGoogle Scholar
  23. 23.
    Toya Y, Endo M, Nakamura S, et al. Clinical outcomes of non-curative endoscopic submucosal dissection with negative resected margins for gastric cancer. Gastrointest Endosc 2017;85:1218–1224.CrossRefPubMedGoogle Scholar
  24. 24.
    Yamanouchi K, Ogata S, Sakata Y, et al. Effect of additional surgery after noncurative endoscopic submucosal dissection for early gastric cancer. Endosc Int Open 2016;4:E24–9.PubMedGoogle Scholar
  25. 25.
    Yang HJ, Kim SG, Lim JH, et al. Predictors of lymph node metastasis in patients with non-curative endoscopic resection of early gastric cancer. Surg Endosc 2015;29:1145–55.CrossRefPubMedGoogle Scholar
  26. 26.
    Stang A. Critical evaluation of the Newcastle-Ottawa scale for the assessment of the quality of nonrandomized studies in meta-analyses. Eur J Epidemiol 2010;25:603–5.CrossRefPubMedGoogle Scholar
  27. 27.
    Suzuki H, Oda I, Abe S, et al. High rate of 5-year survival among patients with early gastric cancer undergoing curative endoscopic submucosal dissection. Gastric Cancer 2016;19:198–205.CrossRefPubMedGoogle Scholar
  28. 28.
    Choi J, Kim SG, Im JP, et al. Is endoscopic ultrasonography indispensable in patients with early gastric cancer prior to endoscopic resection? Surg Endosc 2010;24:3177–85.CrossRefPubMedGoogle Scholar
  29. 29.
    Jeon MY, Park JC, Hahn KY, et al. Long-term outcomes after noncurative endoscopic resection of early gastric cancer: the optimal time for additional endoscopic treatment. Gastrointest Endosc 2018;87:1003–1013.e2.CrossRefPubMedGoogle Scholar
  30. 30.
    Jung DH, Lee YC, Kim JH, et al. Additive treatment improves survival in elderly patients after non-curative endoscopic resection for early gastric cancer. Surg Endosc 2017;31:1376–1382.CrossRefPubMedGoogle Scholar
  31. 31.
    Kusano C, Iwasaki M, Kaltenbach T, et al. Should elderly patients undergo additional surgery after non-curative endoscopic resection for early gastric cancer? Long-term comparative outcomes. Am J Gastroenterol 2011;106:1064–9.CrossRefPubMedGoogle Scholar
  32. 32.
    Kim H, Kim JH, Park JC, et al. Lymphovascular invasion is an important predictor of lymph node metastasis in endoscopically resected early gastric cancers. Oncol Rep 2011;25:1589–95.PubMedGoogle Scholar
  33. 33.
    Sako A, Kitayama J, Ishikawa M, et al. Impact of immunohistochemically identified lymphatic invasion on nodal metastasis in early gastric cancer. Gastric Cancer 2006;9:295–302.CrossRefPubMedGoogle Scholar
  34. 34.
    Yoon H, Kim SG, Choi J, et al. Risk factors of residual or recurrent tumor in patients with a tumor-positive resection margin after endoscopic resection of early gastric cancer. Surg Endosc 2013;27:1561–8.CrossRefPubMedGoogle Scholar
  35. 35.
    Kim TK, Kim GH, Park DY, et al. Risk factors for local recurrence in patients with positive lateral resection margins after endoscopic submucosal dissection for early gastric cancer. Surg Endosc 2015;29:2891–8.CrossRefPubMedGoogle Scholar
  36. 36.
    Oda I, Gotoda T, Sasako M, et al. Treatment strategy after non-curative endoscopic resection of early gastric cancer. Br J Surg 2008;95:1495–500.CrossRefPubMedGoogle Scholar
  37. 37.
    Kikuchi D, Iizuka T, Hoteya S, et al. Safety and efficacy of secondary endoscopic submucosal dissection for residual gastric carcinoma after primary endoscopic submucosal dissection. Digestion 2012;86:288–93.CrossRefPubMedGoogle Scholar
  38. 38.
    Bae SY, Jang TH, Min BH, et al. Early additional endoscopic submucosal dissection in patients with positive lateral resection margins after initial endoscopic submucosal dissection for early gastric cancer. Gastrointest Endosc 2012;75:432–6.CrossRefPubMedGoogle Scholar
  39. 39.
    Abe N, Takeuchi H, Ohki A, et al. Long-term outcomes of combination of endoscopic submucosal dissection and laparoscopic lymph node dissection without gastrectomy for early gastric cancer patients who have a potential risk of lymph node metastasis. Gastrointest Endosc 2011;74:792–7.CrossRefPubMedGoogle Scholar

Copyright information

© The Society for Surgery of the Alimentary Tract 2018

Authors and Affiliations

  1. 1.Department of Surgical OncologyFirst Affiliated Hospital of China Medical UniversityShenyangPeople’s Republic of China

Personalised recommendations