European Journal of Epidemiology

, Volume 25, Issue 7, pp 439–448

Incidence of chronic atrophic gastritis: systematic review and meta-analysis of follow-up studies

  • Mariam Abdullahi Adamu
  • Melanie Nicole Weck
  • Lei Gao
  • Hermann Brenner
Review

Abstract

Chronic atrophic gastritis (CAG) is an important precursor lesion of intestinal gastric cancer. As it is typically asymptomatic, epidemiological data on the incidence of CAG are sparse. We aimed to provide an overview of published data on CAG incidence (overall and according to risk factors) from follow-up studies. Articles with information on incidence of CAG published in English until 26th of July 2009 were identified through a systematic MEDLINE and EMBASE search. Data extracted include study characteristics and key findings regarding the incidence of CAG. A meta-analysis was performed on the association between Helicobacter pylori infection and CAG incidence. Overall, data on CAG incidence were available from 14 studies, in 7 studies incidence could be estimated according to H. pylori infection. Most studies were conducted in symptomatic or high risk populations and the maximum number of incident cases was 284. Incidence estimates ranged from 0 to 11% per year and were consistently below 1% in patients not infected with H. pylori. The highest incidence was observed in a special study conducted on ulcer patients treated by proximal gastric vagotomy. Rate ratios for the association between H. pylori infection and CAG incidence ranged from 2.4 to 7.6 with a summary estimate of 5.0 (95% confidence interval: 3.1–8.3). Incidence of CAG is very low in the absence of H. pylori infection. There is a need for more population-based studies to provide comparable estimates of incidence and the impact of risk factors in the development of CAG.

Keywords

Chronic atrophic gastritis Incidence Follow-up studies 

Abbreviations

CAG

Chronic atrophic gastritis

cagA

Cytotoxin associated gene A

H. pylori

Helicobacter pylori

PG

Pepsinogen

Supplementary material

References

  1. 1.
    Ohata H, Kitauchi S, Yoshimura N, Mugitani K, Iwane M, Nakamura H, Yoshikawa A, Yanaoka K, Arii K, Tamai H, Shimizu Y, Takeshita T, Mohara O, Ichinose M. Progression of chronic atrophic gastritis associated with Helicobacter pylori infection increases risk of gastric cancer. Int J Cancer. 2004;109:138–43.CrossRefPubMedGoogle Scholar
  2. 2.
    Parkin DM, Bray F, Ferlay J, Pisani P. Global cancer statistics, 2002. CA Cancer J Clin. 2005;55:74–108.CrossRefPubMedGoogle Scholar
  3. 3.
    Kuipers EJ. Review article: exploring the link between Helicobacter pylori and gastric cancer. Aliment Pharmacol Ther. 1999;13(Suppl 1):3–11.CrossRefPubMedGoogle Scholar
  4. 4.
    Weck MN, Brenner H. Prevalence of chronic atrophic gastritis in different parts of the world. Cancer Epidemiol Biomarkers Prev. 2006;15:1083–94.CrossRefPubMedGoogle Scholar
  5. 5.
    Weck MN, Brenner H. Association of Helicobacter pylori infection with chronic atrophic gastritis: meta-analyses according to type of disease definition. Int J Cancer. 2008;123:874–81.CrossRefPubMedGoogle Scholar
  6. 6.
    Cochran WG. The combination of estimates from different experiments. Biometrics. 1954;10:101–29.CrossRefGoogle Scholar
  7. 7.
    Higgins JP, Thompson SG, Deeks JJ, Altman DG. Measuring inconsistency in meta-analyses. BMJ. 2003;327:557–60.CrossRefPubMedGoogle Scholar
  8. 8.
    Egger M, Davey Smith G, Schneider M, Minder C. Bias in meta-analysis detected by a simple, graphical test. BMJ. 1997;315:629–34.PubMedGoogle Scholar
  9. 9.
    Begg CB, Mazumdar M. Operating characteristics of a rank correlation test for publication bias. Biometrics. 1994;50:1088–101.CrossRefPubMedGoogle Scholar
  10. 10.
    Jonsson KA, Strom M, Bodemar G, Norrby K. Histologic changes in the gastroduodenal mucosa after long-term medical treatment with cimetidine or parietal cell vagotomy in patients with juxtapyloric ulcer disease. Scand J Gastroenterol. 1988;23:433–41.CrossRefPubMedGoogle Scholar
  11. 11.
    Correa P, Haenszel W, Cuello C, Zavala D, Fontham E, Zarama G, Tannenbaum S, Collazos T, Ruiz B. Gastric precancerous process in a high risk population: cohort follow-up. Cancer Res. 1990;50:4737–40.PubMedGoogle Scholar
  12. 12.
    Kuipers EJ, Perez-Perez GI, Meuwissen SG, Blaser MJ. Helicobacter pylori and atrophic gastritis: importance of the cagA status. J Natl Cancer Inst. 1995;87:1777–80.CrossRefPubMedGoogle Scholar
  13. 13.
    Kuipers EJ, Uyterlinde AM, Pena AS, Roosendaal R, Pals G, Nelis GF, Festen HPM, Meuwissen SGM. Long-term sequelae of Helicobacter pylori gastritis. Lancet. 1995;345:1525–8.CrossRefPubMedGoogle Scholar
  14. 14.
    Kuipers EJ, Lundell L, Klinkenberg-Knol EC, Havu N, Festen HP, Liedman B, Lamers CB, Jansen JB, Dalenback J, Snel P, Nelis GF, Meuwissen SG. Atrophic gastritis and Helicobacter pylori infection in patients with reflux esophagitis treated with omeprazole or fundoplication. N Engl J Med. 1996;334:1018–22.CrossRefPubMedGoogle Scholar
  15. 15.
    Valle J, Kekki M, Sipponen P, Ihamaki T, Siurala M. Long-term course and consequences of Helicobacter pylori gastritis. Results of a 32-year follow-up study. Scand J Gastroenterol. 1996;31:546–50.CrossRefPubMedGoogle Scholar
  16. 16.
    Maaroos HI, Havu N, Sipponen P. Follow-up of Helicobacter pylori positive gastritis and argyrophil cells pattern during the natural course of gastric ulcer. Helicobacter. 1998;3:39–44.CrossRefPubMedGoogle Scholar
  17. 17.
    Ozasa K, Kurata JH, Higashi A, Hayashi K, Inokuchi H, Miki K, Tada M, Kawai K, Watanabe Y. Helicobacter pylori infection and atrophic gastritis: a nested case-control study in a rural town in Japan. Dig Dis Sci. 1999;44:253–6.CrossRefPubMedGoogle Scholar
  18. 18.
    Carter M, Katz DL, Haque S, DeLuca VA. Jr. Does acid suppression by antacids and H2 receptor antagonists increase the incidence of atrophic gastritis in patients with or without H. pylori gastritis? J Clin Gastroenterol. 1999;29:183–7.CrossRefPubMedGoogle Scholar
  19. 19.
    Tepes B, Kavcic B, Zaletel LK, Gubina M, Ihan A, Poljak M, Krizman I. Two- to four-year histological follow-up of gastric mucosa after Helicobacter pylori eradication. J Pathol. 1999;188:24–9.CrossRefPubMedGoogle Scholar
  20. 20.
    Klinkenberg-Knol EC, Nelis F, Dent J, Snel P, Mitchell B, Prichard P, Lloyd D, Havu N, Frame MH, Roman J, Walan A. Long-term omeprazole treatment in resistant gastroesophageal reflux disease: efficacy, safety, and influence on gastric mucosa. Gastroenterology. 2000;118:661–9.CrossRefPubMedGoogle Scholar
  21. 21.
    Lamberts R, Brunner G, Solcia E. Effects of very long (up to 10 years) proton pump blockade on human gastric mucosa. Digestion. 2001;64:205–13.CrossRefPubMedGoogle Scholar
  22. 22.
    Lundell L, Havu N, Miettinen P, Myrvold HE, Wallin L, Julkunen R, Levander K, Hatlebakk JG, Liedman B, Lamm M, Malm A, Walan A. Changes of gastric mucosal architecture during long-term omeprazole therapy: results of a randomized clinical trial. Aliment Pharmacol Ther. 2006;23:639–47.CrossRefPubMedGoogle Scholar
  23. 23.
    Xie XF, Ito M, Yoshihara M, Haruma K, Tanaka S, Chayama K. Serum pepsinogen levels in the Japanese population: prospective study of 9 years of follow-up. Hepatogastroenterology. 2007;54:1887–90.PubMedGoogle Scholar
  24. 24.
    Vorobjova T, Maaroos HI, Uibo R. Immune response to Helicobacter pylori and its association with the dynamics of chronic gastritis in the antrum and corpus. APMIS. 2008;116:465–76.CrossRefPubMedGoogle Scholar
  25. 25.
    Sidebotham RL, Worku ML, Karim QN, Dhir NK, Baron JH. How Helicobacter pylori urease may affect external pH and influence growth and motility in the mucus environment: evidence from in vitro studies. Eur J Gastroenterol Hepatol. 2003;15:395–401.CrossRefPubMedGoogle Scholar
  26. 26.
    Burne RA, Chen YY. Bacterial ureases in infectious diseases. Microbes Infect. 2000;2:533–42.CrossRefPubMedGoogle Scholar
  27. 27.
    Kuipers EJ, Nelis GF, Klinkenberg-Knol EC, Snel P, Goldfain D, Kolkman JJ, Festen HP, Dent J, Zeitoun P, Havu N, Lamm M, Walan A. Cure of Helicobacter pylori infection in patients with reflux oesophagitis treated with long term omeprazole reverses gastritis without exacerbation of reflux disease: results of a randomised controlled trial. Gut. 2004;53:12–20.CrossRefPubMedGoogle Scholar
  28. 28.
    Ihamaki T, Kekki M, Sipponen P, Siurala M. The sequelae and course of chronic gastritis during a 30- to 34-year bioptic follow-up study. Scand J Gastroenterol. 1985;20:485–91.CrossRefPubMedGoogle Scholar
  29. 29.
    El-Zimaity HM, Ota H, Graham DY, Akamatsu T, Katsuyama T. Patterns of gastric atrophy in intestinal type gastric carcinoma. Cancer. 2002;94:1428–36.CrossRefPubMedGoogle Scholar
  30. 30.
    Weck MN, Stegmaier C, Rothenbacher D, Brenner H. Epidemiology of chronic atrophic gastritis: population-based study among 9444 older adults from Germany. Aliment Pharmacol Ther. 2007;26:879–87.PubMedGoogle Scholar
  31. 31.
    Brenner H, Rothenbacher D, Weck MN. Epidemiologic findings on serologically defined chronic atrophic gastritis strongly depend on the choice of the cutoff-value. Int J Cancer. 2007;121:2782–6.CrossRefPubMedGoogle Scholar
  32. 32.
    Iijima K, Abe Y, Kikuchi R, Koike T, Ohara S, Sipponen P, Shimosegawa T. Serum biomarker tests are useful in delineating between patients with gastric atrophy and normal, healthy stomach. World J Gastroenterol. 2009;15:853–9.CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2010

Authors and Affiliations

  • Mariam Abdullahi Adamu
    • 1
  • Melanie Nicole Weck
    • 1
  • Lei Gao
    • 1
  • Hermann Brenner
    • 1
  1. 1.Division of Clinical Epidemiology and Aging ResearchGerman Cancer Research CenterHeidelbergGermany

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