DOI QR코드

DOI QR Code

Postoperative Radiotherapy Improves Survival in Gastric Signet-Ring Cell Carcinoma: a SEER Database Analysis

  • Wei, Feng (Department of Gastroenterology, The Fifth People's Hospital of Shanghai Fudan University) ;
  • Lyu, Hongwei (Department of Gastroenterology, The Fifth People's Hospital of Shanghai Fudan University) ;
  • Wang, Shuoer (Central Laboratory, The Fifth People's Hospital of Shanghai Fudan University) ;
  • Chu, Yan (Department of Gastroenterology, The Fifth People's Hospital of Shanghai Fudan University) ;
  • Chen, Fengyuan (Department of Gastroenterology, The Fifth People's Hospital of Shanghai Fudan University)
  • Received : 2019.07.06
  • Accepted : 2019.09.26
  • Published : 2019.12.31

Abstract

Purpose: To identify the potential therapeutic role of postoperative radiotherapy (RT) in patients with locally advanced (stage II and stage III) gastric signet ring cell carcinoma (SRC). Materials and methods: Patients with locally advanced gastric SRC from the Surveillance, Epidemiology, and End Results program database between 2004 and 2012 were included in our study. Univariate and multivariate Cox proportional models were performed, and survival curves were generated to evaluate the prognostic effect of postoperative RT and surgery alone on SRC patients. Propensity score matching (PSM) was used to avoid selection bias among the study cohorts. Results: We found that patients with postoperative RT had better probability of survival compared with those who did not receive RT (overall survival [OS], P<0.001; cancer-specific survival [CSS], P<0.001). After PSM, analysis of both overall and CSS showed that patients who underwent postoperative RT had better prognosis than those receiving surgery alone in the matched cohort (OS, P=0.00079; CSS, P=0.0036). Multivariate Cox proportional model indicated that postoperative RT had better effect on prognosis compared with surgery alone with respect to both overall (hazard ratio [HR], 0.716; 95% confidence interval [95% CI], 0.590-0.87; P=0.001) and CSS (HR, 0.713; 95% CI, 0.570-0.890; P=0.003). Conclusions: Postoperative RT had better prognosis compared with surgery alone for both overall and CSS for patients with locally advanced gastric SRC.

Keywords

References

  1. Flejou JF. WHO classification of digestive tumors: the fourth edition. Ann Pathol 2011;31:S27-S31. https://doi.org/10.1016/j.annpat.2011.08.001
  2. Hass HG, Smith U, Jager C, Schaffer M, Wellhauber U, Hehr T, et al. Signet ring cell carcinoma of the stomach is significantly associated with poor prognosis and diffuse gastric cancer (Lauren's): single-center experience of 160 cases. Onkologie 2011;34:682-686. https://doi.org/10.1159/000334545
  3. Torre LA, Bray F, Siegel RL, Ferlay J, Lortet-Tieulent J, Jemal A. Global cancer statistics, 2012. CA Cancer J Clin 2015;65:87-108. https://doi.org/10.3322/caac.21262
  4. 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;15:508-513. https://doi.org/10.1245/s10434-007-9660-9
  5. Kim JP, Kim SC, Yang HK. Prognostic significance of signet ring cell carcinoma of the stomach. Surg Oncol 1994;3:221-227. https://doi.org/10.1016/0960-7404(94)90037-X
  6. Li C, Kim S, Lai JF, Hyung WJ, Choi WH, Choi SH, et al. Advanced gastric carcinoma with signet ring cell histology. Oncology 2007;72:64-68. https://doi.org/10.1159/000111096
  7. Heger U, Blank S, Wiecha C, Langer R, Weichert W, Lordick F, et al. Is preoperative chemotherapy followed by surgery the appropriate treatment for signet ring cell containing adenocarcinomas of the esophagogastric junction and stomach? Ann Surg Oncol 2014;21:1739-1748. https://doi.org/10.1245/s10434-013-3462-z
  8. Ajani JA, D'Amico TA, Almhanna K, Bentrem DJ, Chao J, Das P, et al. Gastric cancer, version 3.2016, NCCN clinical practice guidelines in oncology. J Natl Compr Canc Netw 2016;14:1286-1312. https://doi.org/10.6004/jnccn.2016.0137
  9. Smyth EC, Verheij M, Allum W, Cunningham D, Cervantes A, Arnold D. Gastric cancer: ESMO clinical practice guidelines for diagnosis, treatment and follow-up. Ann Oncol 2016;27:v38-v49. https://doi.org/10.1093/annonc/mdw350
  10. Ling CR, Wang R, Wang MJ, Ping J, Zhuang W. Prognosis and value of preoperative radiotherapy in locally advanced rectal signet-ring cell carcinoma. Sci Rep 2017;7:45334. https://doi.org/10.1038/srep45334
  11. Wu SG, Zhang WW, Sun JY, He ZY, Su GQ, Li FY. Preoperative radiotherapy improves survival in rectal signet-ring cell carcinoma-a population-based study. Radiat Oncol 2017;12:141. https://doi.org/10.1186/s13014-017-0874-0
  12. Bratland A, Vetrhus T, Groholt KK, Ree AH. Preoperative radiotherapy in rectal signet-ring cell carcinoma - magnetic resonance imaging and treatment outcome: report of six cases. Acta Oncol 2010;49:42-49. https://doi.org/10.3109/02841860903081897
  13. Ren J, Niu G, Wang X, Song T, Hu Z, Ke C. Effect of age on prognosis of gastric signet-ring cell carcinoma: a SEER database analysis. Med Sci Monit 2018;24:8524-8532. https://doi.org/10.12659/MSM.911766
  14. Zhang X, Wang S, Zhao S, Sun Y, Yang G. Postoperative chemotherapy had no prognostic effect on early-staged young ovarian cancer with unilateral resection. Cancer Med 2018;7:5488-5496. https://doi.org/10.1002/cam4.1822
  15. Jiang H, Zhang H, Tian L, Zhang X, Xue Y. The difference in clinic-pathological features between signet ring cell carcinoma and gastric mucinous adenocarcinoma. Tumour Biol 2013;34:2625-31. https://doi.org/10.1007/s13277-013-0812-1
  16. Zhang Z. Propensity score method: a non-parametric technique to reduce model dependence. Ann Transl Med 2017;5:7. https://doi.org/10.21037/atm.2016.08.57
  17. 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;186:121-130. https://doi.org/10.1620/tjem.186.121
  18. Zhou R, Yan S, Li J. Influence of marital status on the survival of patients with gastric cancer. J Gastroenterol Hepatol 2016;31:768-775. https://doi.org/10.1111/jgh.13217
  19. 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;128:765-770. https://doi.org/10.5858/2004-128-765-DTITIA
  20. Bamboat ZM, Tang LH, Vinuela E, Kuk D, Gonen M, Shah MA, et al. Stage-stratified prognosis of signet ring cell histology in patients undergoing curative resection for gastric adenocarcinoma. Ann Surg Oncol 2014;21:1678-1685. https://doi.org/10.1245/s10434-013-3466-8
  21. Yashiro M, Chung YS, Nishimura S, Inoue T, Sowa M. Establishment of two new scirrhous gastric cancer cell lines: analysis of factors associated with disseminated metastasis. Br J Cancer 1995;72:1200-1210. https://doi.org/10.1038/bjc.1995.486
  22. Kunz PL, Gubens M, Fisher GA, Ford JM, Lichtensztajn DY, Clarke CA. Long-term survivors of gastric cancer: a California population-based study. J Clin Oncol 2012;30:3507-3515. https://doi.org/10.1200/JCO.2011.35.8028
  23. Chiurillo MA. Role of the Wnt/${\beta}$-catenin pathway in gastric cancer: an in-depth literature review. World J Exp Med 2015;5:84-102. https://doi.org/10.5493/wjem.v5.i2.84
  24. 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;250:878-887. https://doi.org/10.1097/SLA.0b013e3181b21c7b
  25. Liu X, Cai H, Sheng W, Yu L, Long Z, Shi Y, et al. Clinicopathological characteristics and survival outcomes of primary signet ring cell carcinoma in the stomach: retrospective analysis of single center database. PLoS One 2015;10:e0144420. https://doi.org/10.1371/journal.pone.0144420
  26. Kwon KJ, Shim KN, Song EM, Choi JY, Kim SE, Jung HK, et al. Clinicopathological characteristics and prognosis of signet ring cell carcinoma of the stomach. Gastric Cancer 2014;17:43-53. https://doi.org/10.1007/s10120-013-0234-1
  27. 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;91:1319-1324. https://doi.org/10.1002/bjs.4637
  28. Kwon KJ, Shim KN, Song EM, Choi JY, Kim SE, Jung HK, et al. Clinicopathological characteristics and prognosis of signet ring cell carcinoma of the stomach. Gastric Cancer 2014;17:43-53. https://doi.org/10.1007/s10120-013-0234-1
  29. Ajani JA, Winter K, Okawara GS, Donohue JH, Pisters PW, Crane CH, et al. Phase II trial of preoperative chemoradiation in patients with localized gastric adenocarcinoma (RTOG 9904): quality of combined modality therapy and pathologic response. J Clin Oncol 2006;24:3953-3958. https://doi.org/10.1200/JCO.2006.06.4840
  30. 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. https://doi.org/10.1200/JCO.2005.14.621
  31. Lu M, Yang Z, Feng Q, Yu M, Zhang Y, Mao C, et al. The characteristics and prognostic value of signet ring cell histology in gastric cancer: a retrospective cohort study of 2199 consecutive patients. Medicine (Baltimore) 2016;95:e4052. https://doi.org/10.1097/MD.0000000000004052
  32. Liu X, Cai H, Sheng W, Yu L, Long Z, Shi Y, et al. Clinicopathological characteristics and survival outcomes of primary signet ring cell carcinoma in the stomach: retrospective analysis of single center database. PLoS One 2015;10:e0144420. https://doi.org/10.1371/journal.pone.0144420
  33. Smalley SR, Benedetti JK, Haller DG, Hundahl SA, Estes NC, Ajani JA, et al. Updated analysis of SWOG-directed intergroup study 0116: a phase III trial of adjuvant radiochemotherapy versus observation after curative gastric cancer resection. J Clin Oncol 2012;30:2327-2333. https://doi.org/10.1200/JCO.2011.36.7136
  34. Cunningham D, Allum WH, Stenning SP, Thompson JN, Van de Velde CJ, Nicolson M, et al. Perioperative chemotherapy versus surgery alone for resectable gastroesophageal cancer. N Engl J Med 2006;355:11-20. https://doi.org/10.1056/NEJMoa055531
  35. Kim S, Lim DH, Lee J, Kang WK, MacDonald JS, Park CH, et al. An observational study suggesting clinical benefit for adjuvant postoperative chemoradiation in a population of over 500 cases after gastric resection with D2 nodal dissection for adenocarcinoma of the stomach. Int J Radiat Oncol Biol Phys 2005;63:1279-1285. https://doi.org/10.1016/j.ijrobp.2005.05.005
  36. Ohri N, Garg MK, Aparo S, Kaubisch A, Tome W, Kennedy TJ, et al. Who benefits from adjuvant radiation therapy for gastric cancer? A meta-analysis. Int J Radiat Oncol Biol Phys 2013;86:330-335. https://doi.org/10.1016/j.ijrobp.2013.02.008
  37. Park SH, Sohn TS, Lee J, Lim DH, Hong ME, Kim KM, et al. Phase III trial to compare adjuvant chemotherapy with capecitabine and cisplatin versus concurrent chemoradiotherapy in gastric cancer: final report of the adjuvant chemoradiotherapy in stomach tumors trial, including survival and subset analyses. J Clin Oncol 2015;33:3130-3136. https://doi.org/10.1200/JCO.2014.58.3930
  38. Kamat AM. Commentary on "Phase II trial of cetuximab with or without paclitaxel in patients with advanced urothelial tract carcinoma." Wong YN, Litwin S, Vaughn D, Cohen S, Plimack ER, Lee J, Song W, Dabrow M, Brody M, Tuttle H, Hudes G, University of Pennsylvania, Philadelphia, PA: J Clin Oncol 2012;30(28):3545-51 [Epub 2012 Aug 27]. Urol Oncol 2013;31:719. https://doi.org/10.1200/JCO.2012.41.9572
  39. Park SH, Zang DY, Han B, Ji JH, Kim TG, Oh SY, et al. ARTIST 2: interim results of a phase III trial involving adjuvant chemotherapy and/or chemoradiotherapy after D2-gastrectomy in stage II/III gastric cancer (GC). J Clin Oncol 2019;37:4001. https://doi.org/10.1200/JCO.2019.37.15_suppl.4001
  40. Asano N, Iijima K, Terai S, Uno K, Endo H, Koike T, et al. Signet ring cell gastric cancer occurring after radiation therapy for Helicobacter pylori-uninfected mucosa-associated lymphoid tissue lymphoma. Case Rep Gastroenterol 2011;5:325-329. https://doi.org/10.1159/000329559
  41. Skoropad VIu, Berdov BA, Loktionova OV, Mardynskii IuS, Titova LN. Comparative analysis of long-term results of combined and surgical treatment at the patients with signet ring cell carcinoma of stomach. Khirurgiia (Mosk) 2008:13-17.
  42. Gee JM, Nicholson RI. Expanding the therapeutic repertoire of epidermal growth factor receptor blockade: radiosensitization. Breast Cancer Res 2003;5:126-129. https://doi.org/10.1186/bcr584
  43. Foda AA, Aziz AA, Mohamed MA. Colorectal signet ring cell carcinoma: influence of EGFR, E-cadherin and MMP-13 expression on clinicopathological features and prognosis. Ann Diagn Pathol 2018;32:41-46. https://doi.org/10.1016/j.anndiagpath.2017.10.003

Cited by

  1. Gastric Signet Ring Cell Carcinoma: Current Management and Future Challenges vol.12, 2019, https://doi.org/10.2147/cmar.s268032
  2. Superior survival in right-sided versus left-sided colon signet ring cell carcinoma vol.10, pp.1, 2019, https://doi.org/10.1038/s41598-020-74926-9
  3. A Prognostic Model for Patients With Gastric Signet Ring Cell Carcinoma vol.20, 2019, https://doi.org/10.1177/15330338211027912
  4. Development and Validation of a Prognostic Nomogram for Gastric Signet Ring Cell Carcinoma: A Multicenter Population-Based Study vol.11, 2021, https://doi.org/10.3389/fonc.2021.603031
  5. Construction and validation a nomogram to predict overall survival for colorectal signet ring cell carcinoma vol.11, pp.1, 2019, https://doi.org/10.1038/s41598-021-82978-8