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Stage-Stratified Prognosis of Signet Ring Cell Histology in Patients Undergoing Curative Resection for Gastric Adenocarcinoma

Abstract

Background

The prognosis of signet ring cell (SRC) gastric adenocarcinoma is regarded as poor, although studies addressing outcomes in relation to non-SRC tumors are conflicting. Our objective was to compare the survival of SRC tumors with stage-matched intestinal-type tumors in a cohort of Western patients.

Methods

Review of a prospectively maintained database identified 569 patients undergoing curative resection (R0) from 1990 to 2009. Patients were divided into three histologic groups on the basis of the Lauren classification: SRC (n = 210), intestinal well- or moderately differentiated (WMD, n = 242) disease, and intestinal poorly differentiated (PD, n = 117) disease. Patient demographics, clinicopathologic features, and postoperative outcomes were determined. Stage-stratified disease-specific mortality was calculated and multivariate analysis performed.

Results

When compared with WMD and PD tumors, SRC tumors were associated with younger age (63 years SRC vs. 71 years WMD and 72 years PD, p < 0.0001) and with female sex (58 % SRC vs. 40 % WMD and 40 % PD, p = 0.0003). Median follow-up was 115 months. Patients with stage Ia SRC lesions had a better 5-year disease-specific mortality compared with stage-matched intestinal-type tumors (0 % SRC vs. 8 % WMD and 24 % PD, p = 0.001). In contrast, SRC patients with stage III disease fared significantly worse (78 % SRC vs. 54 % WMD and 72 % PD, p = 0.001). On multivariate analysis, the risk of death from gastric cancer comparing all three groups was lowest for SRC in stage I and highest for SRC in stage III disease (stage III hazard ratio: SRC 1 vs. 0.47 WMD and 0.85 PD).

Conclusions

When compared with intestinal-type tumors, SRC tumors at early stages are not necessarily associated with poor outcomes.

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References

  1. Antonioli DA, Goldman H. Changes in the location and type of gastric adenocarcinoma. Cancer. 1982;50:775–81.

    CAS  PubMed  Article  Google Scholar 

  2. Henson DE, Dittus C, Younes M, Nguyen H, Albores-Saavedra J. Differential trends in the intestinal and diffuse types of gastric carcinoma in the United States, 1973–2000: increase in the signet ring cell type. Arch Pathol Lab Med. 2004;128:765–70.

    PubMed  Google Scholar 

  3. Kim JP, Kim SC, Yang HK. Prognostic significance of signet ring cell carcinoma of the stomach. Surg Oncol. 1994;3:221–7.

    CAS  PubMed  Article  Google Scholar 

  4. Li C, Kim S, Lai JF, Hyung WJ, Choi WH, Choi SH, et al. Advanced gastric carcinoma with signet ring cell histology. Oncology. 2007;72:64–8.

    PubMed  Article  Google Scholar 

  5. Park JM, Jang YJ, Kim JH, Park SS, Park SH, Kim SJ, et al. Gastric cancer histology: clinicopathologic characteristics and prognostic value. J Surg Oncol. 2008;98:520–5.

    PubMed  Article  Google Scholar 

  6. Piessen G, Messager M, Leteurtre E, Jean-Pierre T, Mariette C. Signet ring cell histology is an independent predictor of poor prognosis in gastric adenocarcinoma regardless of tumoral clinical presentation. Ann Surg. 2009;250:878–87.

    PubMed  Article  Google Scholar 

  7. Yokota T, Kunii Y, Teshima S, Yamada Y, Saito T, Kikuchi S, et al. Signet ring cell carcinoma of the stomach: a clinicopathological comparison with the other histological types. Tohoku J Exp Med. 1998;186:121–30.

    CAS  PubMed  Article  Google Scholar 

  8. Kim DY, Park YK, Joo JK, Ryu SY, Kim YJ, Kim SK, et al. Clinicopathological characteristics of signet ring cell carcinoma of the stomach. ANZ J Surg. 2004;74:1060–4.

    PubMed  Article  Google Scholar 

  9. Kunisaki C, Shimada H, Nomura M, Matsuda G, Otsuka Y, Akiyama H. Therapeutic strategy for signet ring cell carcinoma of the stomach. Br J Surg. 2004;91:1319–24.

    CAS  PubMed  Article  Google Scholar 

  10. Zhang M, Zhu G, Zhang H, Gao H, Xue Y. Clinicopathologic features of gastric carcinoma with signet ring cell histology. J Gastrointest Surg. 2010;14:601–6.

    PubMed  Article  Google Scholar 

  11. Maehara Y, Sakaguchi Y, Moriguchi S, Orita H, Korenaga D, Kohnoe S, et al. Signet ring cell carcinoma of the stomach. Cancer. 1992;69:1645–50.

    CAS  PubMed  Article  Google Scholar 

  12. Otsuji E, Yamaguchi T, Sawai K, Takahashi T. Characterization of signet ring cell carcinoma of the stomach. J Surg Oncol. 1998;67:216–20.

    CAS  PubMed  Article  Google Scholar 

  13. Hyung WJ, Noh SH, Lee JH, Huh JJ, Lah KH, Choi SH, et al. Early gastric carcinoma with signet ring cell histology. Cancer. 2002;94:78–83.

    PubMed  Article  Google Scholar 

  14. 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;15:508–13.

    CAS  PubMed  Article  Google Scholar 

  15. Hohenberger P, Gretschel S. Gastric cancer. Lancet. 2003;362(9380):305–15.

    PubMed  Article  Google Scholar 

  16. Jass JR, Sobin LH, Watanabe H. The World Health Organization’s histologic classification of gastrointestinal tumors. A commentary on the second edition. Cancer. 1990;66:2162–7.

    CAS  PubMed  Article  Google Scholar 

  17. 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;21:3647–50.

    PubMed  Article  Google Scholar 

  18. Taghavi S, Jayarajan SN, Davey A, Willis AI. Prognostic significance of signet ring gastric cancer. J Clin Oncol. 2012;30:3493–8.

    PubMed Central  PubMed  Article  Google Scholar 

  19. Theuer CP, Nastanski F, Brewster WR, Butler JA, Anton-Culver H. Signet ring cell histology is associated with unique clinical features but does not affect gastric cancer survival. Am Surg. 1999;65:915–21.

    CAS  PubMed  Google Scholar 

  20. Shah MA, Khanin R, Tang L, Janjigian YY, Klimstra DS, Gerdes H, et al. Molecular classification of gastric cancer: a new paradigm. Clin Cancer Res. 2011;17:2693–701.

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  21. Tan IB, Ivanova T, Lim KH, Ong CW, Deng N, Lee J, et al. Intrinsic subtypes of gastric cancer, based on gene expression pattern, predict survival and respond differently to chemotherapy. Gastroenterology. 2011;141:476–85, 485 e1–11.

    PubMed Central  PubMed  Article  Google Scholar 

  22. Messager M, Lefevre JH, Pichot-Delahaye V, Souadka A, Piessen G, Mariette C, et al. The impact of perioperative chemotherapy on survival in patients with gastric signet ring cell adenocarcinoma: a multicenter comparative study. Ann Surg. 2011;254:684–93.

    PubMed  Article  Google Scholar 

  23. Dikken JL, van de Velde CJ, Gonen M, Verheij M, Brennan MF, Coit DG. The New American Joint Committee on Cancer/International Union against cancer staging system for adenocarcinoma of the stomach: increased complexity without clear improvement in predictive accuracy. Ann Surg Oncol. 2012;19:2443–51.

    PubMed Central  PubMed  Article  Google Scholar 

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Correspondence to Vivian E. Strong MD.

Additional information

Zubin M. Bamboat and Laura H. Tang have contributed equally to this study.

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Bamboat, Z.M., Tang, L.H., Vinuela, E. et al. Stage-Stratified Prognosis of Signet Ring Cell Histology in Patients Undergoing Curative Resection for Gastric Adenocarcinoma. Ann Surg Oncol 21, 1678–1685 (2014). https://doi.org/10.1245/s10434-013-3466-8

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  • DOI: https://doi.org/10.1245/s10434-013-3466-8

Keywords

  • Gastric Cancer
  • Signet Ring Cell
  • Hereditary Diffuse Gastric Cancer
  • Lauren Classification
  • Poorly Differentiate