DOI QR코드

DOI QR Code

Epidemiology of Gastroesophageal Junction Adenocarcinoma in Korea

  • Kim, Jin-Jo (Division of Gastrointestinal Surgery, Department of Surgery, Incheon St. Mary's Hospital, College of Medicine, The Catholic University of Korea)
  • Received : 2018.09.07
  • Accepted : 2018.12.04
  • Published : 2018.12.31

Abstract

The incidence of gastroesophageal junction adenocarcinoma (GEJAC) in Western countries has increased in recent decades, in addition to a rise in the incidence of esophageal adenocarcinoma (EAC). Gastroesophageal reflux disease (GERD), obesity, smoking, alcohol consumption, and low Helicobacter pylori (HP) infection rate have been nominated as risk factors for such cancers. Among these risk factors, the increased prevalence of GERD and obesity and the decreased prevalence of HP infection are of special interest owing to the currently increasing prevalence of GEJAC in Western countries. Although similar trends in the prevalence of GERD, obesity, and HP infection are observed in Asian countries after a time lag from Western countries, it is still uncertain if the prevalence of GEJAC in Asian countries is increasing, especially in Korea. The incidence of GERD in Korea is currently increasing; it was below 3% in the 1990s. The incidence of obesity in the Korean population is increasing owing to the adoption of westernized lifestyles, including food preferences, and the HP infection rate in Korea is known to be decreasing. Therefore, based on logical extrapolation of observations of Western countries, the incidence of GEJAC will increase in Korea. However, the proportion of GEJAC among other upper gastrointestinal malignancies in Korea appears to be currently unchanged compared with that in the 1990s. Presently, there is a lack of epidemiologic studies on this issue in this region; therefore, more studies are needed to clarify the characteristics of these tumors and to improve clinical outcomes for patients with these tumors.

Keywords

References

  1. Pohl H, Welch HG. The role of overdiagnosis and reclassification in the marked increase of esophageal adenocarcinoma incidence. J Natl Cancer Inst 2005;97:142-146. https://doi.org/10.1093/jnci/dji024
  2. Walther C, Zilling T, Perfekt R, Moller T. Increasing prevalence of adenocarcinoma of the oesophagus and gastro-oesophageal junction: a study of the Swedish population between 1970 and 1997. Eur J Surg 2001;167:748-757. https://doi.org/10.1080/11024150152707725
  3. Chow WH, Finkle WD, McLaughlin JK, Frankl H, Ziel HK, Fraumeni JF Jr. The relation of gastroesophageal reflux disease and its treatment to adenocarcinomas of the esophagus and gastric cardia. JAMA 1995;274:474-477. https://doi.org/10.1001/jama.1995.03530060048032
  4. Lagergren J, Bergstrom R, Lindgren A, Nyren O. Symptomatic gastroesophageal reflux as a risk factor for esophageal adenocarcinoma. N Engl J Med 1999;340:825-831. https://doi.org/10.1056/NEJM199903183401101
  5. Wu AH, Tseng CC, Bernstein L. Hiatal hernia, reflux symptoms, body size, and risk of esophageal and gastric adenocarcinoma. Cancer 2003;98:940-948. https://doi.org/10.1002/cncr.11568
  6. Lubin JH, Cook MB, Pandeya N, Vaughan TL, Abnet CC, Giffen C, et al. The importance of exposure rate on odds ratios by cigarette smoking and alcohol consumption for esophageal adenocarcinoma and squamous cell carcinoma in the Barrett's Esophagus and Esophageal Adenocarcinoma Consortium. Cancer Epidemiol 2012;36:306-316. https://doi.org/10.1016/j.canep.2012.03.001
  7. Hoyo C, Cook MB, Kamangar F, Freedman ND, Whiteman DC, Bernstein L, 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
  8. Pohl H, Wrobel K, Bojarski C, Voderholzer W, Sonnenberg A, Rosch T, et al. Risk factors in the development of esophageal adenocarcinoma. Am J Gastroenterol 2013;108:200-207. https://doi.org/10.1038/ajg.2012.387
  9. Derakhshan MH, Malekzadeh R, Watabe H, Yazdanbod A, Fyfe V, Kazemi A, et al. Combination of gastric atrophy, reflux symptoms and histological subtype indicates two distinct aetiologies of gastric cardia cancer. Gut 2008;57:298-305. https://doi.org/10.1136/gut.2007.137364
  10. Nilsson M, Johnsen R, Ye W, Hveem K, Lagergren J. Prevalence of gastro-oesophageal reflux symptoms and the influence of age and sex. Scand J Gastroenterol 2004;39:1040-1045. https://doi.org/10.1080/00365520410003498
  11. Bollschweiler E, Knoppe K, Wolfgarten E, Holscher AH. Prevalence of reflux symptoms in the general population of Cologne. Z Gastroenterol 2007;45:177-181. https://doi.org/10.1055/s-2006-927402
  12. Goh KL. Emerging gastrointestinal and liver diseases in Asia Pacific: Implications to health care in the region (World Gastroenterology Organization: Asian Pacific Association of Gastroenterology Distinguished Global Lecture 2015). J Clin Gastroenterol 2017;51:479-485. https://doi.org/10.1097/MCG.0000000000000847
  13. Siewert JR, Stein HJ. Classification of adenocarcinoma of the oesophagogastric junction. Br J Surg 1998;85:1457-1459. https://doi.org/10.1046/j.1365-2168.1998.00940.x
  14. Hasegawa S, Yoshikawa T, Cho H, Tsuburaya A, Kobayashi O. Is adenocarcinoma of the esophagogastric junction different between Japan and western countries? The incidence and clinicopathological features at a Japanese high-volume cancer center. World J Surg 2009;33:95-103. https://doi.org/10.1007/s00268-008-9740-4
  15. Edge SB, Byrd DR, Compton CC, Fritz AG, Greene FL, Trotti A, eds. AJCC Cancer Staging Manual. 7th ed. New York: Springer, 2010.
  16. Amin MB, Edge SB, Brookland RK, Jessup JM, Brierly JD, Byrd DR, et al., eds. AJCC Cancer Staging Manual. 8th ed. New York: Springer, 2017.
  17. Hasegawa S, Yoshikawa T. Adenocarcinoma of the esophagogastric junction: incidence, characteristics, and treatment strategies. Gastric Cancer 2010;13:63-73. https://doi.org/10.1007/s10120-010-0555-2
  18. Yamashita H, Seto Y, Sano T, Makuuchi H, Ando N, Sasako M, et al. Results of a nation-wide retrospective study of lymphadenectomy for esophagogastric junction carcinoma. Gastric Cancer 2017;20:69-83. https://doi.org/10.1007/s10120-016-0663-8
  19. Buas MF, Vaughan TL. Epidemiology and risk factors for gastroesophageal junction tumors: understanding the rising incidence of this disease. Semin Radiat Oncol 2013;23:3-9. https://doi.org/10.1016/j.semradonc.2012.09.008
  20. Hansen S, Vollset SE, Derakhshan MH, Fyfe V, Melby KK, Aase S, et al. Two distinct aetiologies of cardia cancer; evidence from premorbid serological markers of gastric atrophy and Helicobacter pylori status. Gut 2007;56:918-925. https://doi.org/10.1136/gut.2006.114504
  21. Blot WJ, Devesa SS, Kneller RW, Fraumeni JF Jr. Rising incidence of adenocarcinoma of the esophagus and gastric cardia. JAMA 1991;265:1287-1289. https://doi.org/10.1001/jama.1991.03460100089030
  22. Kubo A, Corley DA. Marked multi-ethnic variation of esophageal and gastric cardia carcinomas within the United States. Am J Gastroenterol 2004;99:582-588. https://doi.org/10.1111/j.1572-0241.2004.04131.x
  23. Pandeya N, Webb PM, Sadeghi S, Green AC, Whiteman DC; Australian Cancer Study. Gastro-oesophageal reflux symptoms and the risks of oesophageal cancer: are the effects modified by smoking, NSAIDs or acid suppressants? Gut 2010;59:31-38. https://doi.org/10.1136/gut.2009.190827
  24. Whiteman DC, Sadeghi S, Pandeya N, Smithers BM, Gotley DC, Bain CJ, et al. Combined effects of obesity, acid reflux and smoking on the risk of adenocarcinomas of the oesophagus. Gut 2008;57:173-180. https://doi.org/10.1136/gut.2007.131375
  25. Crane SJ, Locke GR 3rd, Harmsen WS, Diehl NN, Zinsmeister AR, Melton LJ 3rd, et al. Subsite-specific risk factors for esophageal and gastric adenocarcinoma. Am J Gastroenterol 2007;102:1596-1602. https://doi.org/10.1111/j.1572-0241.2007.01234.x
  26. Odze RD. Pathology of the gastroesophageal junction. Semin Diagn Pathol 2005;22:256-265. https://doi.org/10.1053/j.semdp.2006.04.007
  27. Goh KL, Chang CS, Fock KM, Ke M, Park HJ, Lam SK. Gastro-oesophageal reflux disease in Asia. J Gastroenterol Hepatol 2000;15:230-238. https://doi.org/10.1046/j.1440-1746.2000.02148.x
  28. Wang HY, Leena KB, Plymoth A, Hergens MP, Yin L, Shenoy KT, et al. Prevalence of gastro-esophageal reflux disease and its risk factors in a community-based population in southern India. BMC Gastroenterol 2016;16:36. https://doi.org/10.1186/s12876-016-0452-1
  29. Hung LJ, Hsu PI, Yang CY, Wang EM, Lai KH. Prevalence of gastroesophageal reflux disease in a general population in Taiwan. J Gastroenterol Hepatol 2011;26:1164-1168. https://doi.org/10.1111/j.1440-1746.2011.06750.x
  30. Fujiwara Y, Arakawa T. Epidemiology and clinical characteristics of GERD in the Japanese population. J Gastroenterol 2009;44:518-534. https://doi.org/10.1007/s00535-009-0047-5
  31. Murao T, Sakurai K, Mihara S, Marubayashi T, Murakami Y, Sasaki Y. Lifestyle change influences on GERD in Japan: a study of participants in a health examination program. Dig Dis Sci 2011;56:2857-2864. https://doi.org/10.1007/s10620-011-1679-x
  32. Jung HK. Epidemiology of gastroesophageal reflux disease in Asia: a systematic review. J Neurogastroenterol Motil 2011;17:14-27. https://doi.org/10.5056/jnm.2011.17.1.14
  33. Cho YS, Choi MG, Jeong JJ, Chung WC, Lee IS, Kim SW, et al. Prevalence and clinical spectrum of gastroesophageal reflux: a population-based study in Asan-si, Korea. Am J Gastroenterol 2005;100:747-753. https://doi.org/10.1111/j.1572-0241.2005.41245.x
  34. Kim KM, Cho YK, Bae SJ, Kim DS, Shim KN, Kim JH, et al. Prevalence of gastroesophageal reflux disease in Korea and associated health-care utilization: a national population-based study. J Gastroenterol Hepatol 2012;27:741-745. https://doi.org/10.1111/j.1440-1746.2011.06921.x
  35. Olefson S, Moss SF. Obesity and related risk factors in gastric cardia adenocarcinoma. Gastric Cancer 2015;18:23-32. https://doi.org/10.1007/s10120-014-0425-4
  36. Abnet CC, Freedman ND, Hollenbeck AR, Fraumeni JF Jr, Leitzmann M, Schatzkin A. A prospective study of BMI and risk of oesophageal and gastric adenocarcinoma. Eur J Cancer 2008;44:465-471. https://doi.org/10.1016/j.ejca.2007.12.009
  37. Lagergren J, Bergstrom R, Nyren O. Association between body mass and adenocarcinoma of the esophagus and gastric cardia. Ann Intern Med 1999;130:883-890. https://doi.org/10.7326/0003-4819-130-11-199906010-00003
  38. Kubo A, Corley DA. Body mass index and adenocarcinomas of the esophagus or gastric cardia: a systematic review and meta-analysis. Cancer Epidemiol Biomarkers Prev 2006;15:872-878. https://doi.org/10.1158/1055-9965.EPI-05-0860
  39. Olsen CM, Pandeya N, Green AC, Webb PM, Whiteman DC; Australian Cancer Study. Population attributable fractions of adenocarcinoma of the esophagus and gastroesophageal junction. Am J Epidemiol 2011;174:582-590. https://doi.org/10.1093/aje/kwr117
  40. Deepa M, Farooq S, Deepa R, Manjula D, Mohan V. Prevalence and significance of generalized and central body obesity in an urban Asian Indian population in Chennai, India (CURES: 47). Eur J Clin Nutr 2009;63:259-267. https://doi.org/10.1038/sj.ejcn.1602920
  41. Gu D, Reynolds K, Wu X, Chen J, Duan X, Reynolds RF, et al. Prevalence of the metabolic syndrome and overweight among adults in China. Lancet 2005;365:1398-1405. https://doi.org/10.1016/S0140-6736(05)66375-1
  42. Sasazuki S, Inoue M, Tsuji I, Sugawara Y, Tamakoshi A, Matsuo K, et al. Body mass index and mortality from all causes and major causes in Japanese: results of a pooled analysis of 7 large-scale cohort studies. J Epidemiol 2011;21:417-430. https://doi.org/10.2188/jea.JE20100180
  43. Berrington de Gonzalez A, Hartge P, Cerhan JR, Flint AJ, Hannan L, MacInnis RJ, et al. Body-mass index and mortality among 1.46 million white adults. N Engl J Med 2010;363:2211-2219. https://doi.org/10.1056/NEJMoa1000367
  44. Park S, Kim Y, Shin HR, Lee B, Shin A, Jung KW, et al. Population-attributable causes of cancer in Korea: obesity and physical inactivity. PLoS One 2014;9:e90871. https://doi.org/10.1371/journal.pone.0090871
  45. Peek RM Jr, Crabtree JE. Helicobacter infection and gastric neoplasia. J Pathol 2006;208:233-248. https://doi.org/10.1002/path.1868
  46. Chow WH, Blaser MJ, Blot WJ, Gammon MD, Vaughan TL, Risch HA, et al. An inverse relation between cagA+ strains of Helicobacter pylori infection and risk of esophageal and gastric cardia adenocarcinoma. Cancer Res 1998;58:588-590.
  47. Weston AP, Badr AS, Topalovski M, Cherian R, Dixon A, Hassanein RS. Prospective evaluation of the prevalence of gastric Helicobacter pylori infection in patients with GERD, Barrett's esophagus, Barrett's dysplasia, and Barrett's adenocarcinoma. Am J Gastroenterol 2000;95:387-394. https://doi.org/10.1111/j.1572-0241.2000.01758.x
  48. Islami F, Kamangar F. Helicobacter pylori and esophageal cancer risk: a meta-analysis. Cancer Prev Res (Phila) 2008;1:329-338. https://doi.org/10.1158/1940-6207.CAPR-08-0109
  49. Kamangar F, Dawsey SM, Blaser MJ, Perez-Perez GI, Pietinen P, Newschaffer CJ, et al. Opposing risks of gastric cardia and noncardia gastric adenocarcinomas associated with Helicobacter pylori seropositivity. J Natl Cancer Inst 2006;98:1445-1452. https://doi.org/10.1093/jnci/djj393
  50. Whiteman DC, Parmar P, Fahey P, Moore SP, Stark M, Zhao ZZ, et al. Association of Helicobacter pylori infection with reduced risk for esophageal cancer is independent of environmental and genetic modifiers. Gastroenterology 2010;139:73-83. https://doi.org/10.1053/j.gastro.2010.04.009
  51. Inomata Y, Koike T, Ohara S, Abe Y, Sekine H, Iijima K, et al. Preservation of gastric acid secretion may be important for the development of gastroesophageal junction adenocarcinoma in Japanese people, irrespective of the H. pylori infection status. Am J Gastroenterol 2006;101:926-933. https://doi.org/10.1111/j.1572-0241.2006.00497.x
  52. Hooi JK, Lai WY, Ng WK, Suen MM, Underwood FE, Tanyingoh D, et al. Global prevalence of Helicobacter pylori infection: systematic review and meta-analysis. Gastroenterology 2017;153:420-429. https://doi.org/10.1053/j.gastro.2017.04.022
  53. Haruma K, Okamoto S, Kawaguchi H, Gotoh T, Kamada T, Yoshihara M, et al. Reduced incidence of Helicobacter pylori infection in young Japanese persons between the 1970s and the 1990s. J Clin Gastroenterol 1997;25:583-586. https://doi.org/10.1097/00004836-199712000-00006
  54. Xia B, Xia HH, Ma CW, Wong KW, Fung FM, Hui CK, et al. Trends in the prevalence of peptic ulcer disease and Helicobacter pylori infection in family physician-referred uninvestigated dyspeptic patients in Hong Kong. Aliment Pharmacol Ther 2005;22:243-249. https://doi.org/10.1111/j.1365-2036.2005.02554.x
  55. Shimatani T, Inoue M, Iwamoto K, Hyogo H, Yokozaki M, Saeki T, et al. Prevalence of Helicobacter pylori infection, endoscopic gastric findings and dyspeptic symptoms among a young Japanese population born in the 1970s. J Gastroenterol Hepatol 2005;20:1352-1357. https://doi.org/10.1111/j.1440-1746.2005.03866.x
  56. Chen J, Bu XL, Wang QY, Hu PJ, Chen MH. Decreasing seroprevalence of Helicobacter pylori infection during 1993-2003 in Guangzhou, southern China. Helicobacter 2007;12:164-169. https://doi.org/10.1111/j.1523-5378.2007.00487.x
  57. Haruma K, Hamada H, Mihara M, Kamada T, Yoshihara M, Sumii K, et al. Negative association between Helicobacter pylori infection and reflux esophagitis in older patients: case-control study in Japan. Helicobacter 2000;5:24-29. https://doi.org/10.1046/j.1523-5378.2000.00003.x
  58. Chang SS, Lu CL, Chao JY, Chao Y, Yen SH, Wang SS, et al. Unchanging trend of adenocarcinoma of the esophagus and gastric cardia in Taiwan: a 15-year experience in a single center. Dig Dis Sci 2002;47:735-740. https://doi.org/10.1023/A:1014771429546
  59. Kusano C, Gotoda T, Khor CJ, Katai H, Kato H, Taniguchi H, et al. Changing trends in the proportion of adenocarcinoma of the esophagogastric junction in a large tertiary referral center in Japan. J Gastroenterol Hepatol 2008;23:1662-1665. https://doi.org/10.1111/j.1440-1746.2008.05572.x
  60. Chung JW, Lee GH, Choi KS, Kim DH, Jung KW, Song HJ, et al. Unchanging trend of esophagogastric junction adenocarcinoma in Korea: experience at a single institution based on Siewert's classification. Dis Esophagus 2009;22:676-681. https://doi.org/10.1111/j.1442-2050.2009.00946.x
  61. Hatta W, Tong D, Lee YY, Ichihara S, Uedo N, Gotoda T. Different time trend and management of esophagogastric junction adenocarcinoma in three Asian countries. Dig Endosc 2017;29 Suppl 2:18-25. https://doi.org/10.1111/den.12808
  62. Shin A, Kim J, Park S. Gastric cancer epidemiology in Korea. J Gastric Cancer 2011;11:135-140. https://doi.org/10.5230/jgc.2011.11.3.135
  63. Jemal A, Siegel R, Ward E, Hao Y, Xu J, Murray T, et al. Cancer statistics, 2008. CA Cancer J Clin 2008;58:71-96. https://doi.org/10.3322/CA.2007.0010
  64. Jeong O, Park YK. Clinicopathological features and surgical treatment of gastric cancer in South Korea: the results of 2009 nationwide survey on surgically treated gastric cancer patients. J Gastric Cancer 2011;11:69-77. https://doi.org/10.5230/jgc.2011.11.2.69
  65. Kim KT, Jeong O, Jung MR, Ryu SY, Park YK. Outcomes of abdominal total gastrectomy for type II and III gastroesophageal junction tumors: single center's experience in Korea. J Gastric Cancer 2012;12:36-42. https://doi.org/10.5230/jgc.2012.12.1.36
  66. Kim JY, Lee HS, Kim N, Shin CM, Lee SH, Park YS, et al. Prevalence and clinicopathologic characteristics of gastric cardia cancer in South Korea. Helicobacter 2012;17:358-368. https://doi.org/10.1111/j.1523-5378.2012.00958.x
  67. Suh YS, Han DS, Kong SH, Lee HJ, Kim YT, Kim WH, et al. Should adenocarcinoma of the esophagogastric junction be classified as esophageal cancer? A comparative analysis according to the seventh AJCC TNM classification. Ann Surg 2012;255:908-915. https://doi.org/10.1097/SLA.0b013e31824beb95
  68. Okabayashi T, Gotoda T, Kondo H, Inui T, Ono H, Saito D, et al. Early carcinoma of the gastric cardia in Japan: is it different from that in the West? Cancer 2000;89:2555-2559. https://doi.org/10.1002/1097-0142(20001215)89:12<2555::AID-CNCR6>3.0.CO;2-R
  69. Drewitz DJ, Sampliner RE, Garewal HS. The incidence of adenocarcinoma in Barrett's esophagus: a prospective study of 170 patients followed 4.8 years. Am J Gastroenterol 1997;92:212-215.
  70. Hameeteman W, Tytgat GN, Houthoff HJ, van den Tweel JG. Barrett's esophagus: development of dysplasia and adenocarcinoma. Gastroenterology 1989;96:1249-1256. https://doi.org/10.1016/S0016-5085(89)80011-3
  71. Tytgat GN, Hameeteman W, Onstenk R, Schotborg R. The spectrum of columnar-lined esophagus--Barrett's esophagus. Endoscopy 1989;21:177-185. https://doi.org/10.1055/s-2007-1012937
  72. Kim N, Lee SW, Cho SI, Park CG, Yang CH, Kim HS, et al. The prevalence of and risk factors for erosive oesophagitis and non-erosive reflux disease: a nationwide multicentre prospective study in Korea. Aliment Pharmacol Ther 2008;27:173-185.

Cited by

  1. Epidemiological Review of Gastroesophageal Junction Adenocarcinoma in Asian Countries vol.103, pp.1, 2018, https://doi.org/10.1159/000519602