The Korean journal of internal medicine

The Korean Association of Internal Medicine (대한내과학회)
권호 표지
DOI QR코드

DOI QR Code

Is screening and surveillance for early detection of gastric cancer needed in Korean Americans?

  • Kim, Gwang Ha (Department of Internal Medicine, Pusan National University School of Medicine) ;
  • Bang, Sung Jo (Department of Internal Medicine, Ulsan University Hospital) ;
  • Ende, Alexander R. (Division of Gastroenterology, Department of Medicine, University of Washington) ;
  • Hwang, Joo Ha (Division of Gastroenterology, Department of Medicine, University of Washington)
  • Received : 2015.04.29
  • Accepted : 2015.05.04
  • Published : 2015.11.01
⟨ Previous Next ⟩

Abstract

The incidence rate of gastric cancer in Korean Americans is over five times higher than that in non-Hispanic whites, and is similar to the incidence of colorectal cancer in the overall United States population. In Korea, the National Cancer Screening Program recommends endoscopy or upper gastrointestinal series for people aged 40 years and older every 2 years. However, the benefit of gastric cancer screening in Korean Americans has not been evaluated. Based on epidemiologic studies, Korean Americans appear to have more similar gastric cancer risk factors to Koreans as opposed to Americans of European descent, though the risk of gastric cancer appears to decrease for subsequent generations. Therefore, in accordance with recent recommendations regarding screening for gastric cancer in Korea, endoscopic screening for gastric cancer in Korean Americans should be considered, especially in those with known atrophic gastritis/intestinal metaplasia or a family history of gastric cancer. In the future, additional studies will needed to assess whether a screening program for gastric cancer in Korean Americans will result in a survival benefit.

Keywords

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. Ferlay J, Soerjomataram I, Ervik M, et al. GLOBOCAN 2012 v1.0, Cancer Incidence and Mortality Worldwide: IARC Cancer Base No. 11 [Internet]. Lyon (FR): International Agency for Research on Cancer, c2015 [cited 2015 Aug 24]. Available from: http://globocan.iarc.fr.
  3. Anderson WF, Camargo MC, Fraumeni JF Jr, Correa P, Rosenberg PS, Rabkin CS. Age-specific trends in incidence of noncardia gastric cancer in US adults. JAMA 2010;303:1723-1728. https://doi.org/10.1001/jama.2010.496
  4. Jung KW, Won YJ, Kong HJ, Oh CM, Lee DH, Lee JS. Cancer statistics in Korea: incidence, mortality, survival, and prevalence in 2011. Cancer Res Treat 2014;46:109-123. https://doi.org/10.4143/crt.2014.46.2.109
  5. Hoeffel EM, Rastogi S, Kim MO, Shahid H. The Asian population: 2010 [Internet]. Washington (DC): U.S. Department of Commerce, Economics and Statistics Administration, U.S. Census Bureau, 2012 [cited 2015 Aug 24]. Available from: http://www.census.gov/prod/cen2010/briefs/c2010br-11.pdf.
  6. Kong SH, Park DJ, Lee HJ, et al. Clinicopathologic features of asymptomatic gastric adenocarcinoma patients in Korea. Jpn J Clin Oncol 2004;34:1-7. https://doi.org/10.1093/jjco/hyh009
  7. Choi IJ. Gastric cancer screening and diagnosis. Korean J Gastroenterol 2009;54:67-76. https://doi.org/10.4166/kjg.2009.54.2.67
  8. Kim YG, Kong SH, Oh SY, et al. Effects of screening on gastric cancer management: comparative analysis of the results in 2006 and in 2011. J Gastric Cancer 2014;14:129-134. https://doi.org/10.5230/jgc.2014.14.2.129
  9. Everett SM, Axon AT. Early gastric cancer in Europe. Gut 1997;41:142-150. https://doi.org/10.1136/gut.41.2.142
  10. Oh KM, Jun J, Zhou Q, Kreps G. Korean American women's perceptions about physical examinations and cancer screening services offered in Korea: the influences of medical tourism on Korean Americans. J Community Health 2014;39:221-229. https://doi.org/10.1007/s10900-013-9800-z
  11. Lui FH, Tuan B, Swenson SL, Wong RJ. Ethnic disparities in gastric cancer incidence and survival in the USA: an updated analysis of 1992-2009 SEER data. Dig Dis Sci 2014;59:3027-3034. https://doi.org/10.1007/s10620-014-3275-3
  12. Miller BA, Chu KC, Hankey BF, Ries LA. Cancer incidence and mortality patterns among specific Asian and Pacific Islander populations in the U.S. Cancer Causes Control 2008;19:227-256. https://doi.org/10.1007/s10552-007-9088-3
  13. McCracken M, Olsen M, Chen MS Jr, et al. Cancer incidence, mortality, and associated risk factors among Asian Americans of Chinese, Filipino, Vietnamese, Korean, and Japanese ethnicities. CA Cancer J Clin 2007;57:190-205. https://doi.org/10.3322/canjclin.57.4.190
  14. Gomez SL, Noone AM, Lichtensztajn DY, et al. Cancer incidence trends among Asian American populations in the United States, 1990-2008. J Natl Cancer Inst 2013;105:1096-1110. https://doi.org/10.1093/jnci/djt157
  15. Maskarinec G, Noh JJ. The effect of migration on cancer incidence among Japanese in Hawaii. Ethn Dis 2004;14:431-439.
  16. Park SY, Murphy SP, Sharma S, Kolonel LN. Dietary intakes and health-related behaviours of Korean American women born in the USA and Korea: the Multiethnic Cohort Study. Public Health Nutr 2005;8:904-911.
  17. Lee J, Demissie K, Lu SE, Rhoads GG. Cancer incidence among Korean-American immigrants in the United States and native Koreans in South Korea. Cancer Control 2007;14:78-85. https://doi.org/10.1177/107327480701400111
  18. Correa P. A human model of gastric carcinogenesis. Cancer Res 1988;48:3554-3560.
  19. 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.
  20. Helicobacter and Cancer Collaborative Group. Gastric cancer and Helicobacter pylori: a combined analysis of 12 case control studies nested within prospective cohorts. Gut 2001;49:347-353. https://doi.org/10.1136/gut.49.3.347
  21. Yim JY, Kim N, Choi SH, et al. Seroprevalence of Helicobacter pylori in South Korea. Helicobacter 2007;12:333-340. https://doi.org/10.1111/j.1523-5378.2007.00504.x
  22. Everhart JE, Kruszon-Moran D, Perez-Perez GI, Tralka TS, McQuillan G. Seroprevalence and ethnic differences in Helicobacter pylori infection among adults in the United States. J Infect Dis 2000;181:1359-1363. https://doi.org/10.1086/315384
  23. La Torre G, Chiaradia G, Gianfagna F, et al. Smoking status and gastric cancer risk: an updated meta-analysis of case-control studies published in the past ten years. Tumori 2009;95:13-22. https://doi.org/10.1177/030089160909500103
  24. IARC Working Group on the Evaluation of Carcinogenic Risks to Humans; International Agency for Research on Cancer (Lyon) Working Group on the Evaluation of Carcinogenic Risks to Humans. Tobacco smoke and involuntary smoking. Lyon: IARC Press, 2004. (International Agency for Research on Cancer, ed. IARC Monographs on the Evaluation of Carcinogenic Risks to Humans; vol. 83).
  25. Ladeiras-Lopes R, Pereira AK, Nogueira A, et al. Smoking and gastric cancer: systematic review and meta-analysis of cohort studies. Cancer Causes Control 2008;19:689-701. https://doi.org/10.1007/s10552-008-9132-y
  26. Tramacere I, Negri E, Pelucchi C, et al. A meta-analysis on alcohol drinking and gastric cancer risk. Ann Oncol 2012;23:28-36. https://doi.org/10.1093/annonc/mdr135
  27. IARC Working Group on the Evaluation of Carcinogenic Risks to Humans. Alcohol consumption and ethyl carbamate. IARC Monogr Eval Carcinog Risks Hum 2010;96:3-1383.
  28. Elliott P, Brown I. Sodium Intakes around the World. Geneva: World Health Organization, 2007.
  29. Tsugane S. Salt, salted food intake, and risk of gastric cancer: epidemiologic evidence. Cancer Sci 2005;96:1-6. https://doi.org/10.1111/j.1349-7006.2005.00006.x
  30. Ge S, Feng X, Shen L, Wei Z, Zhu Q, Sun J. Association between habitual dietary salt intake and risk of gastric cancer: a systematic review of observational studies. Gastroenterol Res Pract 2012;2012:808120.
  31. D'Elia L, Rossi G, Ippolito R, Cappuccio FP, Strazzullo P. Habitual salt intake and risk of gastric cancer: a meta-analysis of prospective studies. Clin Nutr 2012;31:489-498. https://doi.org/10.1016/j.clnu.2012.01.003
  32. Chen Y, Liu L, Wang X, et al. Body mass index and risk of gastric cancer: a meta-analysis of a population with more than ten million from 24 prospective studies. Cancer Epidemiol Biomarkers Prev 2013;22:1395-1408. https://doi.org/10.1158/1055-9965.EPI-13-0042
  33. Hoyo C, Cook MB, Kamangar F, et al. Body mass index in relation to oesophageal and oesophagogastric junction adenocarcinomas: a pooled analysis from the International BEACON Consortium. Int J Epidemiol 2012;41:1706-1718. https://doi.org/10.1093/ije/dys176
  34. Lin XJ, Wang CP, Liu XD, et al. Body mass index and risk of gastric cancer: a meta-analysis. Jpn J Clin Oncol 2014;44:783-791. https://doi.org/10.1093/jjco/hyu082
  35. Correa P. Human gastric carcinogenesis: a multistep and multifactorial process. First American Cancer Society Award Lecture on Cancer Epidemiology and Prevention. Cancer Res 1992;52:6735-6740.
  36. de Vries AC, van Grieken NC, Looman CW, et al. Gastric cancer risk in patients with premalignant gastric lesions: a nationwide cohort study in the Netherlands. Gastroenterology 2008;134:945-952. https://doi.org/10.1053/j.gastro.2008.01.071
  37. Tatsuta M, Iishi H, Nakaizumi A, et al. Fundal atrophic gastritis as a risk factor for gastric cancer. Int J Cancer 1993;53:70-74. https://doi.org/10.1002/ijc.2910530114
  38. Busuttil RA, Boussioutas A. Intestinal metaplasia: a premalignant lesion involved in gastric carcinogenesis. J Gastroenterol Hepatol 2009;24:193-201. https://doi.org/10.1111/j.1440-1746.2008.05774.x
  39. Gonzalez CA, Sanz-Anquela JM, Gisbert JP, Correa P. Utility of subtyping intestinal metaplasia as marker of gastric cancer risk: a review of the evidence. Int J Cancer 2013;133:1023-1032. https://doi.org/10.1002/ijc.28003
  40. 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
  41. Shin CM, Kim N, Yang HJ, et al. Stomach cancer risk in gastric cancer relatives: interaction between Helicobacter pylori infection and family history of gastric cancer for the risk of stomach cancer. J Clin Gastroenterol 2010;44:e34-e39. https://doi.org/10.1097/MCG.0b013e3181a159c4
  42. Rokkas T, Sechopoulos P, Pistiolas D, Margantinis G, Koukoulis G. Helicobacter pylori infection and gastric histology in first-degree relatives of gastric cancer patients: a meta-analysis. Eur J Gastroenterol Hepatol 2010;22:1128-1133. https://doi.org/10.1097/MEG.0b013e3283398d37
  43. Ley C, Mohar A, Guarner J, et al. Screening markers for chronic atrophic gastritis in Chiapas, Mexico. Cancer Epidemiol Biomarkers Prev 2001;10:107-112.
  44. Samloff IM. Cellular localization of group I pepsinogens in human gastric mucosa by immunofluorescence. Gastroenterology 1971;61:185-188.
  45. Samloff IM, Liebman WM. Cellular localization of the group II pepsinogens in human stomach and duodenum by immunofluorescence. Gastroenterology 1973;65:36-42.
  46. Samloff IM, Stemmermann GN, Heilbrun LK, Nomura A. Elevated serum pepsinogen I and II levels differ as risk factors for duodenal ulcer and gastric ulcer. Gastroenterology 1986;90:570-576. https://doi.org/10.1016/0016-5085(86)91110-8
  47. Miki K, Ichinose M, Shimizu A, et al. Serum pepsinogens as a screening test of extensive chronic gastritis. Gastroenterol Jpn 1987;22:133-141.
  48. Kato M, Asaka M. Recent development of gastric cancer prevention. Jpn J Clin Oncol 2012;42:987-994. https://doi.org/10.1093/jjco/hys151
  49. Borch K, Axelsson CK, Halgreen H, et al. The ratio of pepsinogen A to pepsinogen C: a sensitive test for atrophic gastritis. Scand J Gastroenterol 1989;24:870-876. https://doi.org/10.3109/00365528909089228
  50. Asaka M, Kato M, Kudo M, et al. Relationship between Helicobacter pylori infection, atrophic gastritis and gastric carcinoma in a Japanese population. Eur J Gastroenterol Hepatol 1995;7 Suppl 1:S7-S10.
  51. Yanaoka K, Oka M, Mukoubayashi C, et al. Cancer highrisk subjects identified by serum pepsinogen tests: outcomes after 10-year follow-up in asymptomatic middle-aged males. Cancer Epidemiol Biomarkers Prev 2008;17:838-845. https://doi.org/10.1158/1055-9965.EPI-07-2762
  52. Watabe H, Mitsushima T, Yamaji Y, et al. Predicting the development of gastric cancer from combining Helicobacter pylori antibodies and serum pepsinogen status: a prospective endoscopic cohort study. Gut 2005;54:764-768. https://doi.org/10.1136/gut.2004.055400
  53. Oishi Y, Kiyohara Y, Kubo M, et al. The serum pepsinogen test as a predictor of gastric cancer: the Hisayama study. Am J Epidemiol 2006;163:629-637. https://doi.org/10.1093/aje/kwj088
  54. Yoshihara M, Hiyama T, Yoshida S, et al. Reduction in gastric cancer mortality by screening based on serum pepsinogen concentration: a case-control study. Scand J Gastroenterol 2007;42:760-764. https://doi.org/10.1080/00365520601097351
  55. Dinis-Ribeiro M, da Costa-Pereira A, Lopes C, et al. Validity of serum pepsinogen I/II ratio for the diagnosis of gastric epithelial dysplasia and intestinal metaplasia during the follow-up of patients at risk for intestinal-type gastric adenocarcinoma. Neoplasia 2004;6:449-456. https://doi.org/10.1593/neo.03505
  56. Hisamichi S, Sugawara N. Mass screening for gastric cancer by X-ray examination. Jpn J Clin Oncol 1984;14:211-223.
  57. Asaka M, Kato M, Takahashi S, et al. Guidelines for the management of Helicobacter pylori infection in Japan: 2009 revised edition. Helicobacter 2010;15:1-20.
  58. Abe Y, Mitsushima T, Nagatani K, Ikuma H, Minamihara Y. Epidemiological evaluation of the protective effect for dying of stomach cancer by screening programme for stomach cancer with applying a method of case-control study: a study of a efficient screening programme for stomach cancer. Nihon Shokakibyo Gakkai Zasshi 1995;92:836-845.
  59. Inaba S, Hirayama H, Nagata C, et al. Evaluation of a screening program on reduction of gastric cancer mortality in Japan: preliminary results from a cohort study. Prev Med 1999;29:102-106. https://doi.org/10.1006/pmed.1999.0507
  60. Fukao A, Tsubono Y, Tsuji I, Hisamichi S, Sugahara N, Takano A. The evaluation of screening for gastric cancer in Miyagi Prefecture, Japan: a population-based case-control study. Int J Cancer 1995;60:45-48. https://doi.org/10.1002/ijc.2910600106
  61. Compare D, Rocco A, Nardone G. Screening for and surveillance of gastric cancer. World J Gastroenterol 2014;20:13681-13691. https://doi.org/10.3748/wjg.v20.i38.13681
  62. Tashiro A, Sano M, Kinameri K, Fujita K, Takeuchi Y. Comparing mass screening techniques for gastric cancer in Japan. World J Gastroenterol 2006;12:4873-4874.
  63. Hosokawa O, Hattori M, Takeda T, Watanabe K, Fujita M. Accuracy of endoscopy in detecting gastric cancer. J Gastroenterol Mass Surv 2004;42:33-39.
  64. Otsuji M, Kouno Y, Otsuji A, Tokushige J, Shimotatara K, Arimura K. Assessment of small diameter panendoscopy for diagnosis of gastric cancer: comparative study with follow-up survey date. Stomach Intest 1989;24:1291-1297.
  65. Choi KS, Kwak MS, Lee HY, Jun JK, Hahm MI, Park EC. Screening for gastric cancer in Korea: population-based preferences for endoscopy versus upper gastrointestinal series. Cancer Epidemiol Biomarkers Prev 2009;18:1390-1398. https://doi.org/10.1158/1055-9965.EPI-08-0940
  66. Kim Y, Jun JK, Choi KS, Lee HY, Park EC. Overview of the National Cancer screening programme and the cancer screening status in Korea. Asian Pac J Cancer Prev 2011;12:725-730.
  67. Jung M. National Cancer Screening Programs and evidence- based healthcare policy in South Korea. Health Policy 2015;119:26-32. https://doi.org/10.1016/j.healthpol.2014.08.012
  68. National Cancer Center. Cancer Facts & Figures 2014. Goyang (KR): National Cancer Center, 2014.
  69. Choi KS, Jun JK, Lee HY, et al. Performance of gastric cancer screening by endoscopy testing through the National Cancer Screening Program of Korea. Cancer Sci 2011;102:1559-1564. https://doi.org/10.1111/j.1349-7006.2011.01982.x
  70. Choi KS, Jun JK, Park EC, et al. Performance of different gastric cancer screening methods in Korea: a population- based study. PLoS One 2012;7:e50041. https://doi.org/10.1371/journal.pone.0050041
  71. Cho E, Kang MH, Choi KS, Suh M, Jun JK, Park EC. Cost-effectiveness outcomes of the national gastric cancer screening program in South Korea. Asian Pac J Cancer Prev 2013;14:2533-2540. https://doi.org/10.7314/APJCP.2013.14.5.2533
  72. Lee HY, Park EC, Jun JK, Choi KS, Hahm MI. Comparing upper gastrointestinal X-ray and endoscopy for gastric cancer diagnosis in Korea. World J Gastroenterol 2010;16:245-250. https://doi.org/10.3748/wjg.v16.i2.245
  73. Chang HS, Park EC, Chung W, et al. Comparing endoscopy and upper gastrointestinal X-ray for gastric cancer screening in South Korea: a cost-utility analysis. Asian Pac J Cancer Prev 2012;13:2721-2728. https://doi.org/10.7314/APJCP.2012.13.6.2721
  74. Tava F, Luinetti O, Ghigna MR, et al. Type or extension of intestinal metaplasia and immature/atypical "indefinite- for-dysplasia" lesions as predictors of gastric neoplasia. Hum Pathol 2006;37:1489-1497. https://doi.org/10.1016/j.humpath.2006.05.012
  75. Dinis-Ribeiro M, Areia M, de Vries AC, et al. Management of precancerous conditions and lesions in the stomach (MAPS): guideline from the European Society of Gastrointestinal Endoscopy (ESGE), European Helicobacter Study Group (EHSG), European Society of Pathology (ESP), and the Sociedade Portuguesa de Endoscopia Digestiva (SPED). Endoscopy 2012;44:74-94. https://doi.org/10.1055/s-0031-1291491
  76. Szaloki T, Toth V, Nemeth I, Tiszlavicz L, Lonovics J, Czako L. Endoscopic mucosal resection: not only therapeutic, but a diagnostic procedure for sessile gastric polyps. J Gastroenterol Hepatol 2008;23:551-555. https://doi.org/10.1111/j.1440-1746.2007.05247.x
  77. Lee CK, Chung IK, Lee SH, et al. Is endoscopic forceps biopsy enough for a definitive diagnosis of gastric epithelial neoplasia? J Gastroenterol Hepatol 2010;25:1507-1513. https://doi.org/10.1111/j.1440-1746.2010.006367.x
  78. Lim H, Jung HY, Park YS, et al. Discrepancy between endoscopic forceps biopsy and endoscopic resection in gastric epithelial neoplasia. Surg Endosc 2014;28:1256-1262. https://doi.org/10.1007/s00464-013-3316-6
  79. Gupta N, Bansal A, Wani SB, Gaddam S, Rastogi A, Sharma P. Endoscopy for upper GI cancer screening in the general population: a cost-utility analysis. Gastrointest Endosc 2011;74:610-624.e2. https://doi.org/10.1016/j.gie.2011.05.001
  80. Yeh JM, Hur C, Kuntz KM, Ezzati M, Goldie SJ. Cost-effectiveness of treatment and endoscopic surveillance of precancerous lesions to prevent gastric cancer. Cancer 2010;116:2941-2953. https://doi.org/10.1002/cncr.25030
  81. Cash BD, Banerjee S, Anderson MA, et al. Ethnic issues in endoscopy. Gastrointest Endosc 2010;71:1108-1112. https://doi.org/10.1016/j.gie.2010.03.001
  82. Lin JT. Screening of gastric cancer: who, when, and how. Clin Gastroenterol Hepatol 2014;12:135-138. https://doi.org/10.1016/j.cgh.2013.09.064
  83. Brenner H, Arndt V, Sturmer T, Stegmaier C, Ziegler H, Dhom G. Individual and joint contribution of family history and Helicobacter pylori infection to the risk of gastric carcinoma. Cancer 2000;88:274-279. https://doi.org/10.1002/(SICI)1097-0142(20000115)88:2<274::AID-CNCR5>3.0.CO;2-9

Cited by

  1. Massive Endoscopic Screening for Esophageal and Gastric Cancers in a High-Risk Area of China vol.10, pp.12, 2015, https://doi.org/10.1371/journal.pone.0145097
  2. How Do We Manage Gastric Intestinal Metaplasia? A Survey of Clinical Practice Trends for Gastrointestinal Endoscopists in the United States vol.61, pp.7, 2015, https://doi.org/10.1007/s10620-016-4107-4
  3. Gastric cancer and family history vol.31, pp.6, 2016, https://doi.org/10.3904/kjim.2016.147
  4. Endoscopic gastritis, serum pepsinogen assay, and Helicobacter pylori infection vol.31, pp.5, 2015, https://doi.org/10.3904/kjim.2016.166
  5. Association of gastric intestinal metaplasia and East Asian ethnicity with the risk of gastric adenocarcinoma in a U.S. population vol.87, pp.4, 2018, https://doi.org/10.1016/j.gie.2017.11.010
  6. Occurrence of gastric cancer in patients with atrophic gastritis during long-term follow-up vol.53, pp.7, 2015, https://doi.org/10.1080/00365521.2018.1477987
  7. Predictive Factors for Improvement of Atrophic Gastritis and Intestinal Metaplasia: A Long-term Prospective Clinical Study vol.18, pp.3, 2018, https://doi.org/10.7704/kjhugr.2018.18.3.186
  8. A Chance to Cut Is a Chance to Cure: Endoscopic Submucosal Dissection for Early Gastric Cancer vol.64, pp.5, 2019, https://doi.org/10.1007/s10620-018-5317-8
  9. Evaluation of serum markers for gastric cancer and its precursor diseases among high incidence and mortality rate of gastric cancer area vol.22, pp.1, 2015, https://doi.org/10.1007/s10120-018-0844-8
  10. Quantification of the sensitivity of early detection surveillance vol.67, pp.6, 2015, https://doi.org/10.1111/tbed.13598
  11. A Novel Six-Gene-Based Prognostic Model Predicts Survival and Clinical Risk Score for Gastric Cancer vol.12, pp.None, 2021, https://doi.org/10.3389/fgene.2021.615834