Abstract
Background
In Japan, the incidence of esophageal adenocarcinoma (EAC) and esophagogastric junction (EGJ) adenocarcinoma is expected to increase and that of gastric adenocarcinoma (GAC) is expected to decrease due to Westernization of the diet and the decreasing prevalence of Helicobacter pylori infection. However, few reports about these trends have included the latest data, and no reports about the time trend in the incidence of EGJ adenocarcinoma have focused on the etiologies (gastric cardia adenocarcinoma or EAC, including Barrett’s adenocarcinoma). We therefore investigated the time trends in the incidence of these cancers by including the latest data.
Methods
First, we investigated the time trends in EAC and GAC using population-based cancer registry data in Osaka Prefecture (1985–2014). We then investigated the time trend in superficial EGJ adenocarcinoma with clinicopathological features at Osaka International Cancer Institute (2006–2017).
Results
From 1985 to 2014 in Osaka Prefecture, the incidence of EAC gradually increased in both sexes, while that of GAC in men did not significantly change and that in women decreased. The ratio of the EAC/GAC incidence increased 3.5 times in men and 1.8 times in women. In the secondary time trend survey for EGJ adenocarcinoma, the numbers of patients with endoscopic Barrett’s esophagus and those without gastric mucosal atrophy increased, and the number of patients with lesions located above the EGJ line and histologically diagnosed as Barrett’s adenocarcinoma increased.
Conclusions
The incidence of EAC and superficial EGJ adenocarcinoma with characteristics similar to those of EAC, including Barrett’s adenocarcinoma, might be increasing.
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References
Ferlay J, Colombet M, Soerjomataram I, et al. Estimating the global cancer incidence and mortality in 2018: GLOBOCAN sources and methods. Int J Cancer. 2019;144(8):1941–53.
Devesa SS, Blot WJ, Fraumeni JF Jr. Changing patterns in the incidence of esophageal and gastric carcinoma in the United States. Cancer. 1998;83(10):2049–53.
Bytzer P, Christensen PB, Damkier P, et al. Adenocarcinoma of the esophagus and Barrett’s esophagus: a population-based study. Am J Gastroenterol. 1999;94(1):86–91.
Thrift AP, Whiteman DC. The incidence of esophageal adenocarcinoma continues to rise: analysis of period and birth cohort effects on recent trends. Ann Oncol. 2012;23(12):3155–62.
Drahos J, Wu M, Anderson WF, et al. Regional variations in esophageal cancer rates by census region in the United States, 1999–2008. PLoS ONE. 2013;8(7):e67913.
Lagergren J, Bergstrom R, Lindgren A, et al. Symptomatic gastroesophageal reflux as a risk factor for esophageal adenocarcinoma. N Engl J Med. 1999;340(11):825–31.
Corley DA, Kubo A, Levin TR, et al. Abdominal obesity and body mass index as risk factors for Barrett’s esophagus. Gastroenterology. 2007;133(1):34–41 (quiz 311).
Lauby-Secretan B, Scoccianti C, Loomis D, et al. Body fatness and cancer-viewpoint of the IARC Working Group. N Engl J Med. 2016;375(8):794–8.
Wang Z, Shaheen NJ, Whiteman DC, et al. Helicobacter pylori infection is associated with reduced risk of Barrett’s esophagus: an analysis of the Barrett’s and esophageal adenocarcinoma consortium. Am J Gastroenterol. 2018;113(8):1148–55.
Fujiwara Y, Arakawa T. Epidemiology and clinical characteristics of GERD in the Japanese population. J Gastroenterol. 2009;44(6):518–34.
Kinoshita Y, Adachi K, Hongo M, et al. Systematic review of the epidemiology of gastroesophageal reflux disease in Japan. J Gastroenterol. 2011;46(9):1092–103.
Yoshiike N, Seino F, Tajima S, et al. Twenty-year changes in the prevalence of overweight in Japanese adults: the National Nutrition Survey 1976–1995. Obes Rev. 2002;3(3):183–90.
Matsushita Y, Takahashi Y, Mizoue T, et al. Overweight and obesity trends among Japanese adults: a 10-year follow-up of the JPHC Study. Int J Obes (Lond). 2008;32(12):1861–7.
Hirayama Y, Kawai T, Otaki J, et al. Prevalence of Helicobacter pylori infection with healthy subjects in Japan. J Gastroenterol Hepatol. 2014;29(Suppl 4):16–9.
Watanabe M, Ito H, Hosono S, et al. Declining trends in prevalence of Helicobacter pylori infection by birth-year in a Japanese population. Cancer Sci. 2015;106(12):1738–43.
Miyamoto M, Haruma K, Kuwabara M, et al. High incidence of newly-developed gastroesophageal reflux disease in the Japanese community: a 6-year follow-up study. J Gastroenterol Hepatol. 2008;23(3):393–7.
Shibata A, Matsuda T, Ajiki W, et al. Trend in incidence of adenocarcinoma of the esophagus in Japan, 1993–2001. Jpn J Clin Oncol. 2008;38(7):464–8.
Hasegawa S, Yoshikawa T, Cho H, et al. 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(1):95–103.
Hansen S, Vollset SE, Derakhshan MH, et al. Two distinct aetiologies of cardia cancer; evidence from premorbid serological markers of gastric atrophy and Helicobacter pylori status. Gut. 2007;56(7):918–25.
Derakhshan MH, Malekzadeh R, Watabe H, et al. Combination of gastric atrophy, reflux symptoms and histological subtype indicates two distinct aetiologies of gastric cardia cancer. Gut. 2008;57(3):298–305.
Hatta W, Tong D, Lee YY, et al. Different time trend and management of esophagogastric junction adenocarcinoma in three Asian countries. Dig Endosc. 2017;29(Suppl 2):18–25.
Japanese Gastric Cancer A. A Japanese classification of gastric carcinoma: 3rd English edition. Gastric Cancer. 2011;14(2):101–12.
Siewert JR, Stein HJ. Classification of adenocarcinoma of the oesophagogastric junction. Br J Surg. 1998;85(11):1457–9.
Kuwano H, Nishimura Y, Oyama T, et al. Guidelines for diagnosis and treatment of carcinoma of the esophagus April 2012 edited by the Japan Esophageal Society. Esophagus. 2015;12:1–30.
Kimura K, Takemoto T. An endoscopic recognition of the atrophic border and its significance in chronic gastritis. Endoscopy. 1969;1(03):87–97.
Redeen S, Petersson F, Jonsson KA, et al. Relationship of gastroscopic features to histological findings in gastritis and Helicobacter pylori infection in a general population sample. Endoscopy. 2003;35(11):946–50.
Sharma P, Dent J, Armstrong D, et al. The development and validation of an endoscopic grading system for Barrett’s esophagus: the Prague C & M criteria. Gastroenterology. 2006;131(5):1392–9.
Chandrasoma P, Makarewicz K, Wickramasinghe K, et al. A proposal for a new validated histological definition of the gastroesophageal junction. Hum Pathol. 2006;37(1):40–7.
Drahos J, Xiao Q, Risch HA, et al. Age-specific risk factor profiles of adenocarcinomas of the esophagus: a pooled analysis from the international BEACON consortium. Int J Cancer. 2016;138(1):55–64.
Armitage P, Doll R. The age distribution of cancer and a multi-stage theory of carcinogenesis. Br J Cancer. 1954;8(1):1–12.
Kim HJ, Fay MP, Feuer EJ, et al. Permutation tests for joinpoint regression with applications to cancer rates. Stat Med. 2000;19(3):335–51.
Kanda Y. Investigation of the freely available easy-to-use software ‘EZR’ for medical statistics. Bone Marrow Transplant. 2013;48(3):452–8.
Koizumi S, Motoyama S, Iijima K. Is the incidence of esophageal adenocarcinoma increasing in Japan? Trends from the data of a hospital-based registration system in Akita Prefecture, Japan. J Gastroenterol. 2018;53(7):827–33.
Okita K, Amano Y, Takahashi Y, et al. Barrett’s esophagus in Japanese patients: its prevalence, form, and elongation. J Gastroenterol. 2008;43(12):928–34.
Akiyama T, Inamori M, Akimoto K, et al. Risk factors for the progression of endoscopic Barrett’s epithelium in Japan: a multivariate analysis based on the Prague C & M Criteria. Dig Dis Sci. 2009;54(8):1702–7.
Watari J, Hori K, Toyoshima F, et al. Association between obesity and Barrett’s esophagus in a Japanese population: a hospital-based, cross-sectional study. BMC Gastroenterol. 2013;13:143.
Akiyama T, Yoneda M, Inamori M, et al. Visceral obesity and the risk of Barrett’s esophagus in Japanese patients with non-alcoholic fatty liver disease. BMC Gastroenterol. 2009;9:56.
Correa P. Chronic gastritis as a cancer precursor. Scand J Gastroenterol Suppl. 1984;104:131–6.
Tatsuta M, Iishi H, Nakaizumi A, et al. Fundal atrophic gastritis as a risk factor for gastric cancer. Int J Cancer. 1993;53(1):70–4.
Uemura N, Okamoto S, Yamamoto S, et al. Helicobacter pylori infection and the development of gastric cancer. N Engl J Med. 2001;345(11):784–9.
Hanaoka N, Uedo N, Shiotani A, et al. Autofluorescence imaging for predicting development of metachronous gastric cancer after Helicobacter pylori eradication. J Gastroenterol Hepatol. 2010;25(12):1844–9.
Nomura S, Ida K, Terao S, et al. Endoscopic diagnosis of gastric mucosal atrophy: multicenter prospective study. Dig Endosc. 2014;26(6):709–19.
Kaji K, Hashiba A, Uotani C, et al. Grading of atrophic gastritis is useful for risk stratification in endoscopic screening for gastric cancer. Am J Gastroenterol. 2018. https://doi.org/10.1038/s41395-018-0259-5.
Hamashima C, Shabana M, Okada K, et al. Mortality reduction from gastric cancer by endoscopic and radiographic screening. Cancer Sci. 2015;106(12):1744–9.
Ono H, Kondo H, Gotoda T, et al. Endoscopic mucosal resection for treatment of early gastric cancer. Gut. 2001;48(2):225–9.
Yao K, Oishi T, Matsui T, et al. Novel magnified endoscopic findings of microvascular architecture in intramucosal gastric cancer. Gastrointest Endosc. 2002;56(2):279–84.
Gono K, Obi T, Yamaguchi M, et al. Appearance of enhanced tissue features in narrow-band endoscopic imaging. J Biomed Opt. 2004;9(3):568–77.
Katanoda K, Hori M, Matsuda T, et al. An updated report on the trends in cancer incidence and mortality in Japan, 1958–2013. Jpn J Clin Oncol. 2015;45(4):390–401.
Acknowledgements
We thank Angela Morben, DVM, and ELS from Edanz Group (www.edanzediting.com/ac) for editing a draft of this manuscript.
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Matsuno, K., Ishihara, R., Ohmori, M. et al. Time trends in the incidence of esophageal adenocarcinoma, gastric adenocarcinoma, and superficial esophagogastric junction adenocarcinoma. J Gastroenterol 54, 784–791 (2019). https://doi.org/10.1007/s00535-019-01577-7
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DOI: https://doi.org/10.1007/s00535-019-01577-7