Clinical Endoscopy

The Korean Society of Gastrointestinal Endoscopy (대한소화기내시경학회)
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Metachronous Gastric Cancer Following Curative Endoscopic Resection of Early Gastric Cancer

  • Received : 2017.06.29
  • Accepted : 2017.07.27
  • Published : 2018.05.30
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Abstract

This review article summarizes knowledge about metachronous gastric cancer (MGC) occurring after curative endoscopic resection (ER) of early gastric cancer (EGC), treatment outcomes of patients who developed MGC, and efficacy of Helicobacter pylori eradication to prevent MGC. The incidence of MGC following curative ER increases over time and is higher than in patients undergoing gastrectomy. Increasing age and multifocal EGC are independent risk factors for developing MGC. An MGC following curative ER is usually a small (<20 mm) and differentiated intramucosal cancer. Most MGC lesions are found at an early stage on semiannual or annual surveillance endoscopy and are successfully treated by further ER, with excellent long-term outcomes. Eradication of H. pylori may reduce the risk of MGC following ER of EGC, but further prospective studies with long-term outcomes are required. Surveillance endoscopy following gastric ER should be continued indefinitely, due to the risk of MGC even after successful H. pylori eradication. Risk stratification and tailored endoscopic surveillance schedules need to be developed.

Keywords

Acknowledgement

Supported by : National Cancer Center

References

  1. Ferlay J, Soerjomataram I, Dikshit R, et al. Cancer incidence and mortality worldwide: sources, methods and major patterns in GLOBOCAN 2012. Int J Cancer 2015;136:E359-E386. https://doi.org/10.1002/ijc.29210
  2. Nashimoto A, Akazawa K, Isobe Y, et al. Gastric cancer treated in 2002 in Japan: 2009 annual report of the JGCA nationwide registry. Gastric Cancer 2013;16:1-27. https://doi.org/10.1007/s10120-012-0163-4
  3. Gotoda T, Yanagisawa A, Sasako M, et al. Incidence of lymph node metastasis from early gastric cancer: estimation with a large number of cases at two large centers. Gastric Cancer 2000;3:219-225. https://doi.org/10.1007/PL00011720
  4. Hirasawa T, Gotoda T, Miyata S, et al. Incidence of lymph node metastasis and the feasibility of endoscopic resection for undifferentiated-type early gastric cancer. Gastric Cancer 2009;12:148-152. https://doi.org/10.1007/s10120-009-0515-x
  5. Japanese Gastric Cancer Association. Japanese gastric cancer treatment guidelines 2010 (ver. 3). Gastric Cancer 2011;14:113-123. https://doi.org/10.1007/s10120-011-0042-4
  6. Ono H, Yao K, Fujishiro M, et al. Guidelines for endoscopic submucosal dissection and endoscopic mucosal resection for early gastric cancer. Dig Endosc 2016;28:3-15. https://doi.org/10.1111/den.12518
  7. Oda I, Saito D, Tada M, et al. A multicenter retrospective study of endoscopic resection for early gastric cancer. Gastric Cancer 2006;9:262-270. https://doi.org/10.1007/s10120-006-0389-0
  8. Isomoto H, Shikuwa S, Yamaguchi N, et al. Endoscopic submucosal dissection for early gastric cancer: a large-scale feasibility study. Gut 2009;58:331-336. https://doi.org/10.1136/gut.2008.165381
  9. Goto O, Fujishiro M, Kodashima S, Ono S, Omata M. Outcomes of endoscopic submucosal dissection for early gastric cancer with special reference to validation for curability criteria. Endoscopy 2009;41:118-122. https://doi.org/10.1055/s-0028-1119452
  10. Gotoda T, Iwasaki M, Kusano C, Seewald S, Oda I. Endoscopic resection of early gastric cancer treated by guideline and expanded National Cancer Centre criteria. Br J Surg 2010;97:868-871. https://doi.org/10.1002/bjs.7033
  11. Abe S, Oda I, Suzuki H, et al. Short- and long-term outcomes of endoscopic submucosal dissection for undifferentiated early gastric cancer. Endoscopy 2013;45:703-707. https://doi.org/10.1055/s-0033-1344396
  12. Kosaka T, Endo M, Toya Y, et al. Long-term outcomes of endoscopic submucosal dissection for early gastric cancer: a single-center retrospective study. Dig Endosc 2014;26:183-191. https://doi.org/10.1111/den.12099
  13. Tanabe S, Ishido K, Higuchi K, et al. Long-term outcomes of endoscopic submucosal dissection for early gastric cancer: a retrospective comparison with conventional endoscopic resection in a single center. Gastric Cancer 2014;17:130-136. https://doi.org/10.1007/s10120-013-0241-2
  14. 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;26:214-219. https://doi.org/10.1111/den.12141
  15. Ohnita K, Isomoto H, Shikuwa S, et al. Early and long-term outcomes of endoscopic submucosal dissection for early gastric cancer in a large patient series. Exp Ther Med 2014;7:594-598. https://doi.org/10.3892/etm.2014.1488
  16. 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. https://doi.org/10.1007/s10120-015-0469-0
  17. Choi JH, Kim ES, Lee YJ, et al. Comparison of quality of life and worry of cancer recurrence between endoscopic and surgical treatment for early gastric cancer. Gastrointest Endosc 2015;82:299-307. https://doi.org/10.1016/j.gie.2015.01.019
  18. Moertel CG, Bargen JA, Soule EH. Multiple gastric cancers; review of the literature and study of 42 cases. Gastroenterology 1957;32:1095-1103.
  19. Uemura N, Okamoto S. Effect of Helicobacter pylori eradication on subsequent development of cancer after endoscopic resection of early gastric cancer in Japan. Gastroenterol Clin North Am 2000;29:819-827. https://doi.org/10.1016/S0889-8553(05)70149-7
  20. Arima N, Adachi K, Katsube T, et al. Predictive factors for metachronous recurrence of early gastric cancer after endoscopic treatment. J Clin Gastroenterol 1999;29:44-47. https://doi.org/10.1097/00004836-199907000-00011
  21. Nishida T, Tsujii M, Kato M, et al. Endoscopic surveillance strategy after endoscopic resection for early gastric cancer. World J Gastrointest Pathophysiol 2014;5:100-106. https://doi.org/10.4291/wjgp.v5.i2.100
  22. Kim JJ, Lee JH, Jung HY, et al. EMR for early gastric cancer in Korea: a multicenter retrospective study. Gastrointest Endosc 2007;66:693-700. https://doi.org/10.1016/j.gie.2007.04.013
  23. Lee H, Yun WK, Min BH, et al. A feasibility study on the expanded indication for endoscopic submucosal dissection of early gastric cancer. Surg Endosc 2011;25:1985-1993. https://doi.org/10.1007/s00464-010-1499-7
  24. Kato M, Nishida T, Yamamoto K, et al. Scheduled endoscopic surveillance controls secondary cancer after curative endoscopic resection for early gastric cancer: a multicentre retrospective cohort study by Osaka University ESD study group. Gut 2013;62:1425-1432. https://doi.org/10.1136/gutjnl-2011-301647
  25. Hahn KY, Park JC, Kim EH, et al. Incidence and impact of scheduled endoscopic surveillance on recurrence after curative endoscopic resection for early gastric cancer. Gastrointest Endosc 2016;84:628-638.e1. https://doi.org/10.1016/j.gie.2016.03.1404
  26. Nakajima T, Oda I, Gotoda T, et al. Metachronous gastric cancers after endoscopic resection: how effective is annual endoscopic surveillance? Gastric Cancer 2006;9:93-98. https://doi.org/10.1007/s10120-006-0372-9
  27. Nasu J, Doi T, Endo H, Nishina T, Hirasaki S, Hyodo I. Characteristics of metachronous multiple early gastric cancers after endoscopic mucosal resection. Endoscopy 2005;37:990-993. https://doi.org/10.1055/s-2005-870198
  28. Kobayashi M, Narisawa R, Sato Y, Takeuchi M, Aoyagi Y. Self-limiting risk of metachronous gastric cancers after endoscopic resection. Dig Endosc 2010;22:169-173. https://doi.org/10.1111/j.1443-1661.2010.00987.x
  29. Min BH, Kim ER, Kim KM, et al. Surveillance strategy based on the incidence and patterns of recurrence after curative endoscopic submucosal dissection for early gastric cancer. Endoscopy 2015;47:784-793. https://doi.org/10.1055/s-0034-1392249
  30. Abe S, Oda I, Suzuki H, et al. Long-term surveillance and treatment outcomes of metachronous gastric cancer occurring after curative endoscopic submucosal dissection. Endoscopy 2015;47:1113-1118. https://doi.org/10.1055/s-0034-1392484
  31. Onodera H, Tokunaga A, Yoshiyuki T, et al. Surgical outcome of 483 patients with early gastric cancer: prognosis, postoperative morbidity and mortality, and gastric remnant cancer. Hepatogastroenterology 2004;51:82-85.
  32. Hosokawa O, Kaizaki Y, Watanabe K, et al. Endoscopic surveillance for gastric remnant cancer after early cancer surgery. Endoscopy 2002;34:469-473. https://doi.org/10.1055/s-2002-32007
  33. Ikeda Y, Saku M, Kishihara F, Maehara Y. Effective follow-up for recurrence or a second primary cancer in patients with early gastric cancer. Br J Surg 2005;92:235-239. https://doi.org/10.1002/bjs.4758
  34. Nozaki I, Hato S, Kobatake T, et al. Incidence of metachronous gastric cancer in the remnant stomach after synchronous multiple cancer surgery. Gastric Cancer 2014;17:61-66. https://doi.org/10.1007/s10120-013-0261-y
  35. Maehata Y, Nakamura S, Fujisawa K, et al. Long-term effect of Helicobacter pylori eradication on the development of metachronous gastric cancer after endoscopic resection of early gastric cancer. Gastrointest Endosc 2012;75:39-46. https://doi.org/10.1016/j.gie.2011.08.030
  36. Kwon YH, Heo J, Lee HS, Cho CM, Jeon SW. Failure of Helicobacter pylori eradication and age are independent risk factors for recurrent neoplasia after endoscopic resection of early gastric cancer in 283 patients. Aliment Pharmacol Ther 2014;39:609-618. https://doi.org/10.1111/apt.12633
  37. Kim YI, Choi IJ, Kook MC, et al. The association between Helicobacter pylori status and incidence of metachronous gastric cancer after endoscopic resection of early gastric cancer. Helicobacter 2014;19:194-201. https://doi.org/10.1111/hel.12116
  38. Lim JH, Kim SG, Choi J, Im JP, Kim JS, Jung HC. Risk factors for synchronous or metachronous tumor development after endoscopic resection of gastric neoplasms. Gastric Cancer 2015;18:817-823. https://doi.org/10.1007/s10120-014-0438-z
  39. Venerito M, Malfertheiner P. Preneoplastic conditions in the stomach: always a point of no return? Dig Dis 2015;33:5-10. https://doi.org/10.1159/000369185
  40. Zaky AH, Watari J, Tanabe H, et al. Clinicopathologic implications of genetic instability in intestinal-type gastric cancer and intestinal metaplasia as a precancerous lesion: proof of field cancerization in the stomach. Am J Clin Pathol 2008;129:613-621. https://doi.org/10.1309/DFLELPGPNV5LK6B1
  41. McDonald SA, Greaves LC, Gutierrez-Gonzalez L, et al. Mechanisms of field cancerization in the human stomach: the expansion and spread of mutated gastric stem cells. Gastroenterology 2008;134:500-510. https://doi.org/10.1053/j.gastro.2007.11.035
  42. Feng XY, Chen YB, Wang W, et al. Time-varying pattern of recurrence risk for gastric cancer patients. Med Oncol 2013;30:514. https://doi.org/10.1007/s12032-013-0514-y
  43. Fuccio L, Zagari RM, Eusebi LH, et al. Meta-analysis: can Helicobacter pylori eradication treatment reduce the risk for gastric cancer? Ann Intern Med 2009;151:121-128. https://doi.org/10.7326/0003-4819-151-2-200907210-00009
  44. Sipponen P, Hyvarinen H. Role of Helicobacter pylori in the pathogenesis of gastritis, peptic ulcer and gastric cancer. Scand J Gastroenterol Suppl 1993;196:3-6.
  45. Huang JQ, Sridhar S, Chen Y, Hunt RH. Meta-analysis of the relationship between Helicobacter pylori seropositivity and gastric cancer. Gastroenterology 1998;114:1169-1179. https://doi.org/10.1016/S0016-5085(98)70422-6
  46. Eslick GD, Lim LL, Byles JE, Xia HH, Talley NJ. Association of Helicobacter pylori infection with gastric carcinoma: a meta-analysis. Am J Gastroenterol 1999;94:2373-2379. https://doi.org/10.1111/j.1572-0241.1999.01360.x
  47. Sipponen P, Kimura K. Intestinal metaplasia, atrophic gastritis and stomach cancer: trends over time. Eur J Gastroenterol Hepatol 1994;6 Suppl 1:S79-S83.
  48. Schistosomes, liver flukes and Helicobacter pylori. IARC Working Group on the Evaluation of Carcinogenic Risks to Humans. Lyon, 7-14 June 1994. IARC Monogr Eval Carcinog Risks Hum 1994;61:1-241.
  49. Uemura N, Okamoto S, Yamamoto S, et al. Helicobacter pylori infection and the development of gastric cancer. N Engl J Med 2001;345:784-789. https://doi.org/10.1056/NEJMoa001999
  50. Take S, Mizuno M, Ishiki K, et al. The effect of eradicating helicobacter pylori on the development of gastric cancer in patients with peptic ulcer disease. Am J Gastroenterol 2005;100:1037-1042. https://doi.org/10.1111/j.1572-0241.2005.41384.x
  51. Uemura N, Mukai T, Okamoto S, et al. Effect of Helicobacter pylori eradication on subsequent development of cancer after endoscopic resection of early gastric cancer. Cancer Epidemiol Biomarkers Prev 1997;6:639-642.
  52. Fukase K, Kato M, Kikuchi S, et al. Effect of eradication of Helicobacter pylori on incidence of metachronous gastric carcinoma after endoscopic resection of early gastric cancer: an open-label, randomised controlled trial. Lancet 2008;372:392-397. https://doi.org/10.1016/S0140-6736(08)61159-9
  53. Choi J, Kim SG, Yoon H, et al. Eradication of Helicobacter pylori after endoscopic resection of gastric tumors does not reduce incidence of metachronous gastric carcinoma. Clin Gastroenterol Hepatol 2014;12:793-800.e1. https://doi.org/10.1016/j.cgh.2013.09.057
  54. Shiotani A, Uedo N, Iishi H, et al. Predictive factors for metachronous gastric cancer in high-risk patients after successful Helicobacter pylori eradication. Digestion 2008;78:113-119. https://doi.org/10.1159/000173719
  55. Seo JY, Lee DH, Cho Y, et al. Eradication of Helicobacter pylori reduces metachronous gastric cancer after endoscopic resection of early gastric cancer. Hepatogastroenterology 2013;60:776-780.
  56. Chon I, Choi C, Shin CM, Park YS, Kim N, Lee DH. Effect of Helicobacter pylori eradication on subsequent dysplasia development after endoscopic resection of gastric dysplasia. Korean J Gastroenterol 2013;61:307-312. https://doi.org/10.4166/kjg.2013.61.6.307
  57. Bae SE, Jung HY, Kang J, et al. Effect of Helicobacter pylori eradication on metachronous recurrence after endoscopic resection of gastric neoplasm. Am J Gastroenterol 2014;109:60-67. https://doi.org/10.1038/ajg.2013.404
  58. Jung DH, Kim JH, Lee YC, et al. Helicobacter pylori eradication reduces the metachronous recurrence of gastric neoplasms by attenuating the precancerous process. J Gastric Cancer 2015;15:246-255. https://doi.org/10.5230/jgc.2015.15.4.246
  59. Yoon SB, Park JM, Lim CH, Cho YK, Choi MG. Effect of Helicobacter pylori eradication on metachronous gastric cancer after endoscopic resection of gastric tumors: a meta-analysis. Helicobacter 2014;19:243-248. https://doi.org/10.1111/hel.12146
  60. Jung DH, Kim JH, Chung HS, et al. Helicobacter pylori eradication on the prevention of metachronous lesions after endoscopic resection of gastric neoplasm: a meta-analysis. PLoS One 2015;10:e0124725. https://doi.org/10.1371/journal.pone.0124725
  61. Mori G, Nakajima T, Asada K, et al. Incidence of and risk factors for metachronous gastric cancer after endoscopic resection and successful Helicobacter pylori eradication: results of a large-scale, multicenter cohort study in Japan. Gastric Cancer 2016;19:911-918. https://doi.org/10.1007/s10120-015-0544-6
  62. Ito M, Tanaka S, Takata S, et al. Morphological changes in human gastric tumours after eradication therapy of Helicobacter pylori in a shortterm follow-up. Aliment Pharmacol Ther 2005;21:559-566. https://doi.org/10.1111/j.1365-2036.2005.02360.x
  63. Kobayashi M, Hashimoto S, Nishikura K, et al. Magnifying narrow-band imaging of surface maturation in early differentiated-type gastric cancers after Helicobacter pylori eradication. J Gastroenterol 2013;48:1332-1342. https://doi.org/10.1007/s00535-013-0764-7
  64. Yamamoto K, Kato M, Takahashi M, et al. Clinicopathological analysis of early-stage gastric cancers detected after successful eradication of Helicobacter pylori. Helicobacter 2011;16:210-216. https://doi.org/10.1111/j.1523-5378.2011.00833.x
  65. Moribata K, Iguchi JK, Nakachi K, et al. Endoscopic features associated with development of metachronous gastric cancer in patients who underwent endoscopic resection followed by Helicobacter pylori eradication. Dig Endosc 2015 Dec 1 [Epub]. https://doi.org/10.1111/den.12581.
  66. National Comprehensive Cancer Network. NCCN clinical practice guidelines in oncology: gastric cancer version I. 2016 [Internet]. Fort Washington (PA): National Comprehensive Cancer Network; c2016 [cited 2016 Mar 31]. Available from: http://www.nccn.org/professionals/physician_gls/PDF/gastric.pdf
  67. Lieberman DA, Rex DK, Winawer SJ, Giardiello FM, Johnson DA, Levin TR. Guidelines for colonoscopy surveillance after screening and polypectomy: a consensus update by the US Multi-Society Task Force on Colorectal Cancer. Gastroenterology 2012;143:844-857. https://doi.org/10.1053/j.gastro.2012.06.001
  68. Asada K, Nakajima T, Shimazu T, et al. Demonstration of the usefulness of epigenetic cancer risk prediction by a multicentre prospective cohort study. Gut 2015;64:388-396. https://doi.org/10.1136/gutjnl-2014-307094

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