Journal of Gastrointestinal Surgery

, Volume 22, Issue 4, pp 569–577 | Cite as

Incidence, Survival, and Predictors of Lymph Node Involvement in Early-Stage Gastric Signet Ring Cell Carcinoma in the US

  • Sridevi K. Pokala
  • Chao Zhang
  • Zhengjia Chen
  • Anthony M. Gamboa
  • Sarah L. Cristofaro
  • Steven A. Keilin
  • Qiang Cai
  • Field F. Willingham
2017 SSAT Plenary Presentation



The incidence, survival, and propensity for nodal metastasis in early-stage gastric signet ring cell carcinoma have not been defined in the United States. These data are critical determinants for treatment allocation.


Cases of gastric signet ring cell carcinoma were extracted from the national SEER database for the years 2004–2013. Age-standardized incidence was derived. Survival was calculated using the Kaplan-Meier method. Univariate and multivariate analyses were performed to identify predictors of nodal metastasis. Exclusion criteria included neoadjuvant radiotherapy and lack of histologic or nodal data.


A total of 10,624 cases were initially identified. The analysis cohort included 506 cases with early T-stage N0M0 disease following exclusions. The incidence was 0.094 per 100,000 person-years. The 5-year survival rate was 82.8%. Tumor stage (p < 0.001) and size (p < 0.001) were independent predictors of nodal metastasis. The incidence of nodal involvement for T1a tumors <2 cm was 5.4% (p < 0.004).


The incidence of potentially resectable signet ring gastric carcinoma has not changed significantly over the past decade. While presenting with predominantly high-grade histology, early T-stage disease has a high survival rate. Small T1a tumors have low rates of nodal metastasis, suggesting that an endoscopic resection could be considered in this subset.


Gastric cancer Endoscopic submucosal dissection Gastric signet ring carcinoma Gastrectomy Endoscopic mucosal resection 



This manuscript was supported in part by a development grant from the Department of Medicine at Emory University School of Medicine. Research reported in this publication was supported in part by the Biostatistics and Bioinformatics Shared Resource of Winship Cancer Institute of Emory University and NIH/NCI under award number P30CA138292. The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Institutes of Health.

Author Contributions

Sridevi K. Pokala contributed study concept and design, acquisition of data, statistical analysis and interpretation of data, and drafting of the manuscript. Chao Zhang and Zhengjia Chen contributed statistical analysis. Anthony M. Gamboa contributed acquisition of data and statistical analysis. Sarah L. Cristofaro contributed acquisition of the data. Steven A. Keilin and Qiang Cai contributed interpretation of the data. Field F. Willingham contributed study concept and design, statistical analysis, interpretation of the data, and drafting of the manuscript. All authors contributed to critical manuscript revision.


  1. 1.
    Voron, T, Messager, M, Duhamel A, Lefevre J, Mabrut J, Goere D, Meunier B, Brigand C, Hamy A, Glehen O, Mariette C, Paye F. Is signet-ring cell carcinoma a specific entity amongst gastric cancers? Gastric Cancer. 2016;19:1027. Scholar
  2. 2.
    Ha TK, An JY, Youn HK, Noh JH, Sohn TS, Kim S. Indication for endoscopic mucosal resection in early signet-ring cell gastric cancer. Ann Surg Oncol. 2008;15(2):508–13.CrossRefPubMedGoogle Scholar
  3. 3.
    Zhang M, Zhu G, Zhang H, Gao H, Xue Y. Clinicopathologic features of gastric carcinoma with signet-ring cell histology. J Gastrointest Surg. 2010;14(4):601–6. Scholar
  4. 4.
    Li C, Kim S, Lai JF, Hyung WJ, Choi WH, Choi SH, Noh SH. Advanced gastric carcinoma with signet-ring cell histology. Oncology. 2007;72(1–2):64–8.CrossRefPubMedGoogle Scholar
  5. 5.
    Kim BS, Oh ST, Yook JH, Kim BS. Signet-ring cell type and other histologic types: differing clinical course and prognosis in T1 gastric cancer. Surgery. 2014 Jun;155(6):1030–5. Scholar
  6. 6.
    Hyung WJ, Noh SH, Lee JH, Huh JJ, Lah KH, Choi SH, Min JS. Early gastric carcinoma with signet-ring cell histology. Cancer. 2002;94(1):78–83.CrossRefPubMedGoogle Scholar
  7. 7.
    Lee SH, Jee SR, Kim JH, Seol SY. Intramucosal gastric cancer: the rate of lymph node metastasis in signet-ring cell carcinoma is as low as that in well-differentiated adenocarcinoma. Eur J Gastroenterol Hepatol. 2015;27(2):170–4. Scholar
  8. 8.
    Chon HJ, Hyung WJ, Kim C, Park S, Kim JH, Park CH, Ahn JB, Kim H, Chung HC, Rha SY, Noh SH, Jeung HC. Differential prognostic implications of gastric signet-ring cell carcinoma: stage adjusted analysis from a single high-volume center in Asia. Ann Surg. 2016.
  9. 9.
    Wang Z, Zhang X, Hu J, Zeng W, Zhou Z. Clinicopathological features and outcomes in patients undergoing radical resection for early gastric cancer with signet-ring cell histology. J Visc Surg. 2015;152(6):357–61. Scholar
  10. 10.
    Liu X, Cai H, Sheng W, Yu L, Long Z, Shi Y, Wang Y. Clinicopathological characteristics and survival outcomes of primary signet-ring cell carcinoma in the stomach: retrospective analysis of single center database. PLoS One. 2015 7;10(12):e0144420. eCollection 2015.
  11. 11.
    Yang XF, Yang L, Mao XY, Wu DY, Zhang SM, Xin Y. Pathobiological behavior and molecular mechanism of signet-ring cell carcinoma and mucinous adenocarcinoma of the stomach: a comparative study. World J Gastroenterol 2004; 10:750–754.CrossRefPubMedPubMedCentralGoogle Scholar
  12. 12.
    Taghavi S, Jayarajan SN, Davey A, Willis AI. Prognostic significance of signet-ring gastric cancer. J Clin Oncol. 2012;30(28):3493–8.
  13. 13.
    Wang Z, Zhang X, Hu J, Zeng W, Liang J, Zhou H, Zhou Z. Predictive factors for lymph node metastasis in early gastric cancer with signet-ring cell histology and their impact on the surgical strategy: analysis of single institutional experience. J Surg Res. 2014;191(1):130–3. Scholar
  14. 14.
    Park JM, Kim SW, Nam KW, Cho YK, Lee IS, Choi MG, Chung IS, Song KY, Park CH, Jung CK. Is it reasonable to treat early gastric cancer with signet-ring cell histology by endoscopic resection? Analysis of factors related to lymph-node metastasis. Eur J Gastroenterol Hepatol. 2009;21(10):1132–5. Scholar
  15. 15.
    Kim MN, Kim HK, Shim CN, Lee HJ, Lee H, Park JC, Shin SK, Lee SK, Lee YC. Tumour size is related to the curability of signet-ring cell early gastric cancer with endoscopic submucosal dissection: a retrospective single centre study. Dig Liver Dis. 2014;46(10):898–902. Scholar
  16. 16.
    Pokala SK, Chen Z, Mekaroonkamol P, Gamboa A, Keilin S, Cai Q, Willingham FF. 471 predictors of lymph node involvement in early stage gastric adenocarcinoma in the United States. Gastrointestinal Endosc. 2017;85(5): AB73-AB74. Scholar
  17. 17.
    Pokala SK, Chen Z, Mekaroonkamol P, Gamboa A, Keilin S, Cai Q, Willingham FF. Mo1071 incidence, survival, and predictors of lymph node metastasis in early stage gastric cardia adenocarcinomas in the United States. Gastrointestinal Endoscop. 2017;85(5): AB415. Scholar
  18. 18.
    Ahmad R, Setia N, Schmidt BH, Hong TS, Wo JY, Kwak EL, Rattner DW, Lauwers GY, Mullen JT. Predictors of lymph node metastasis in western early gastric cancer. J Gastrointest Surg. 2016;20(3):531–8. Scholar
  19. 19.
    Choi AH, Nelson RA, Merchant SJ, Kim JY, Chao J, Kim J. Rates of lymph node metastasis and survival in T1a gastric adenocarcinoma in Western populations. Gastrointestinal Endosc. 2016;83(6):1184–1192.e1. Scholar
  20. 20.
    Wong J, Jackson P. Gastric cancer surgery: an American perspective on the current options and standards. Curr Treat Options Oncol. 2011;12(1):72–84. Scholar
  21. 21.
    Willingham FF, Garud SS, Davis SS, Lewis MM, Maithel SK, Kooby DA. Human hybrid endoscopic and laparoscopic management of mass lesions of the foregut (with video). Gastrointest Endosc. 2012;75(4):905–12. Scholar
  22. 22.
    Garud SS, Keilin S, Cai Q, Willingham FF. Diagnosis and management of Barrett’s esophagus for the endoscopist. Therap Adv Gastroenterol. 2010;3(4):227–38. Scholar
  23. 23.
    Garud SS, Willingham FF. Natural orifice transluminal endoscopic surgery. Gastrointest Endosc. 2012;76(3):491–5. Scholar
  24. 24.
    Pernot S, Voron T, Perkins G, Lagorce-Pages C, Berger A, Taieb J. Signet-ring cell carcinoma of the stomach: impact on prognosis and specific therapeutic challenge. World Journal of Gastroenterology: WJG. 2015;21(40):11428–11438. Scholar

Copyright information

© The Society for Surgery of the Alimentary Tract 2018

Authors and Affiliations

  1. 1.Emory University School of MedicineAtlantaUSA
  2. 2.The Winship Cancer InstituteEmory UniversityAtlantaUSA
  3. 3.Department of Biostatistics and Bioinformatics, Rollins School of Public HealthEmory UniversityAtlantaUSA
  4. 4.Division of Gastroenterology, Department of MedicineVanderbilt University School of MedicineNashvilleUSA
  5. 5.Division of Digestive Diseases, Department of MedicineEmory University School of MedicineAtlantaUSA

Personalised recommendations