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Journal of Translational Medicine
Published in: Journal of Translational Medicine 1/2024

Open Access 01-12-2024 | Gastric Cancer | Review

Chronic atrophic gastritis and risk of incident upper gastrointestinal cancers: a systematic review and meta-analysis

Authors: Junqiu Li, Jielu Pan, Dinghong Xiao, Nan Shen, Ruiqing Wang, Hongyv Miao, Peimin Pu, Haiyan Zhang, Xiao Yv, Lianjun Xing

Published in: Journal of Translational Medicine | Issue 1/2024

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Abstract

Background

Previous literature has explored the relationship between chronic atrophic gastritis (CAG) and isolated cancers within the upper gastrointestinal cancers; However, an integrative synthesis across the totality of upper gastrointestinal cancers was conspicuously absent. The research objective was to assess the relationship between CAG and the risk of incident upper gastrointestinal cancers, specifically including gastric cancer, oesophageal cancer, and oesophagogastric junction cancer.

Methods

Rigorous systematic searches were conducted across three major databases, namely PubMed, Embase and Web of Science, encompassing the timeline from database inception until August 10, 2023. We extracted the necessary odds ratio (OR) and their corresponding 95% confidence interval (CI) for subsequent meta-analysis. Statistical analyses were conducted using Stata 17.0 software.

Results

This meta-analysis included a total of 23 articles encompassing 5858 patients diagnosed with upper gastrointestinal cancers. CAG resulted in a statistically significant 4.12-fold elevated risk of incident gastric cancer (OR = 4.12, 95% CI 3.20–5.30). Likewise, CAG was linked to a 2.08-fold increased risk of incident oesophageal cancer (OR = 2.08, 95%CI 1.60–2.72). Intriguingly, a specific correlation was found between CAG and the risk of incident oesophageal squamous cell carcinoma (OR = 2.29, 95%CI 1.77–2.95), while no significant association was detected for oesophageal adenocarcinoma (OR = 0.62, 95%CI 0.17–2.26). Moreover, CAG was correlated with a 2.77-fold heightened risk of oesophagogastric junction cancer (OR = 2.77, 95%CI 2.21–3.46). Notably, for the same type of upper gastrointestinal cancer, it was observed that diagnosing CAG through histological methods was linked to a 33–77% higher risk of developing cancer compared to diagnosing CAG through serological methods.

Conclusion

This meta-analysis indicated a two- to fourfold increased risk of gastric cancer, oesophageal cancer, and oesophagogastric junction cancer in patients with CAG. Importantly, for the same upper gastrointestinal cancer, the risk of incident cancer was higher when CAG was diagnosed histologically compared to serological diagnosis. Further rigorous study designs are required to explore the impact of CAG diagnosed through both diagnostic methods on the risk of upper gastrointestinal cancers.
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Literature
1.
Kocarnik JM, Compton K, Dean FE, Fu W, Gaw BL, Harvey JD, Henrikson HJ, Lu D, Pennini A, Xu R, et al. Cancer incidence, mortality, years of life lost, years lived with disability, and disability-adjusted life years for 29 cancer groups from 2010 to 2019: a systematic analysis for the global burden of disease study 2019. JAMA Oncol. 2022;8:420–44.PubMedCrossRef
2.
Yang H, Wang X-K, Wang J-B, Zhao F-H, Fan J-H, Qiao Y-L, Taylor PR, Abnet CC. Combined risk factors and risk of upper gastrointestinal cancer mortality in the Linxian general population. Int J Cancer. 2022;151:1462–73.PubMedCrossRef
3.
Abnet CC, Corley DA, Freedman ND, Kamangar F. Diet and upper gastrointestinal malignancies. Gastroenterology. 2015;148:1234.PubMedCrossRef
4.
5.
Mantovani A, Allavena P, Sica A, Balkwill F. Cancer-related inflammation. Nature. 2008;454:436–44.PubMedCrossRef
6.
González CA, Figueiredo C, Lic CB, Ferreira RM, Pardo ML, Ruiz Liso JM, Alonso P, Sala N, Capella G, Sanz-Anquela JM. Helicobacter pylori cagA and vacA genotypes as predictors of progression of gastric preneoplastic lesions: a long-term follow-up in a high-risk area in Spain. Am J Gastroenterol. 2011;106:867–74.PubMedCrossRef
7.
Ohata H, Kitauchi S, Yoshimura N, Mugitani K, Iwane M, Nakamura H, Yoshikawa A, Yanaoka K, Arii K, Tamai H, et al. Progression of chronic atrophic gastritis associated with Helicobacter pylori infection increases risk of gastric cancer. Int J Cancer. 2004;109:138–43.PubMedCrossRef
8.
Sharma PK, Suri TM, Venigalla PM, Garg SK, Mohammad G, Das P, Sood S, Saraya A, Ahuja V. Atrophic gastritis with high prevalence of Helicobacter pylori is a predominant feature in patients with dyspepsia in a high altitude area. Trop Gastroenterol. 2014;35:246–51.PubMedCrossRef
9.
Plummer M, van Doorn L-J, Franceschi S, Kleter B, Canzian F, Vivas J, Lopez G, Colin D, Muñoz N, Kato I. Helicobacter pylori cytotoxin-associated genotype and gastric precancerous lesions. J Natl Cancer Inst. 2007;99:1328–34.PubMedCrossRef
10.
Akbari M, Tabrizi R, Kardeh S, Lankarani KB. Gastric cancer in patients with gastric atrophy and intestinal metaplasia: a systematic review and meta-analysis. PLoS ONE. 2019;14: e0219865.PubMedPubMedCentralCrossRef
11.
Spence AD, Cardwell CR, McMenamin ÚC, Hicks BM, Johnston BT, Murray LJ, Coleman HG. Adenocarcinoma risk in gastric atrophy and intestinal metaplasia: a systematic review. BMC Gastroenterol. 2017;17:157.PubMedPubMedCentralCrossRef
12.
Islami F, Sheikhattari P, Ren JS, Kamangar F. Gastric atrophy and risk of oesophageal cancer and gastric cardia adenocarcinoma—a systematic review and meta-analysis. Ann Oncol. 2011;22:754–60.PubMedCrossRef
13.
Page MJ, McKenzie JE, Bossuyt PM, Boutron I, Hoffmann TC, Mulrow CD, Shamseer L, Tetzlaff JM, Akl EA, Brennan SE, et al. The PRISMA 2020 statement: an updated guideline for reporting systematic reviews. BMJ (Clin Res Ed). 2021;372: n71.
14.
Taylor KS, Mahtani KR, Aronson JK. Summarising good practice guidelines for data extraction for systematic reviews and meta-analysis. BMJ Evid Based Med. 2021;26:88–90.PubMedCrossRef
15.
Shah SC, Piazuelo MB, Kuipers EJ, Li D. AGA clinical practice update on the diagnosis and management of atrophic gastritis: expert review. Gastroenterology. 2021;161:1325.PubMedCrossRef
16.
Sjs HJ. Classification of adenocarcinoma of the oesophagogastric junction. Br J Surg. 1998;85:1457–9.
17.
18.
Localio AR, Margolis DJ, Berlin JA. Relative risks and confidence intervals were easily computed indirectly from multivariable logistic regression. J Clin Epidemiol. 2007;60:874–82.PubMedCrossRef
19.
Akiyama T, Inamori M, Iida H, Endo H, Hosono K, Yoneda K, Fujita K, Yoneda M, Takahashi H, Goto A, et al. Macroscopic extent of gastric mucosal atrophy: increased risk factor for esophageal squamous cell carcinoma in Japan. BMC Gastroenterol. 2009;9:34.PubMedPubMedCentralCrossRef
20.
Almodova EdC, De Oliveira WK, Machado LFA, Grejo JR, Da Cunha TR, Colaiacovo W, Ortolan EVP. Atrophic gastritis: risk factor for esophageal squamous cell carcinoma in a Latin-American population. World J Gastroenterol. 2013;19:2060–4.PubMedPubMedCentralCrossRef
21.
Anderson LA, Murphy SJ, Johnston BT, Watson RGP, Ferguson HR, Bamford KB, Ghazy A, McCarron P, McGuigan J, Reynolds JV, et al. Relationship between Helicobacter pylori infection and gastric atrophy and the stages of the oesophageal inflammation, metaplasia, adenocarcinoma sequence: results from the FINBAR case–control study. Gut. 2008;57:734–9.PubMedCrossRef
22.
Aromaa A, Kosunen TU, Knekt P, Maatela J, Teppo L, Heinonen OP, Härkönen M, Hakama MK. Circulating anti-Helicobacter pylori immunoglobulin A antibodies and low serum pepsinogen I level are associated with increased risk of gastric cancer. Am J Epidemiol. 1996;144:142–9.PubMedCrossRef
23.
Cook MB, Dawsey SM, Diaw L, Blaser MJ, Perez-Perez GI, Abnet CC, Taylor PR, Albanes D, Virtamo J, Kamangar F. Serum pepsinogens and Helicobacter pylori in relation to the risk of esophageal squamous cell carcinoma in the alpha-tocopherol, beta-carotene cancer prevention study. Cancer Epidemiol Biomarkers Prev. 2010;19:1966–75.PubMedPubMedCentralCrossRef
24.
de Vries AC, Capelle LG, Looman CWN, van Blankenstein M, van Grieken NCT, Casparie MK, Meijer GA, Kuipers EJ. Increased risk of esophageal squamous cell carcinoma in patients with gastric atrophy: independent of the severity of atrophic changes. Int J Cancer. 2009;124:2135–8.PubMedCrossRef
25.
Ekheden I, Yang X, Chen H, Chen X, Yuan Z, Jin L, Lu M, Ye W. Associations between gastric atrophy and its interaction with poor oral health and the risk for esophageal squamous cell carcinoma in a high-risk region of China: a population-based case–control study. Am J Epidemiol. 2020;189:931–41.PubMedPubMedCentralCrossRef
26.
Fukuda H, Saito D, Hayashi S, Hisai H, Ono H, Yoshida S, Oguro Y, Noda T, Sato T, Katoh M. Helicobacter pylori infection, serum pepsinogen level and gastric cancer: a case–control study in Japan. Jpn J Cancer Res Gann. 1995;86:64–71.PubMedCrossRef
27.
Gao P, Cai N, Yang X, Yuan Z, Zhang T, Lu M, Jin L, Ye W, Suo C, Chen X. Association of Helicobacter pylori and gastric atrophy with adenocarcinoma of the esophagogastric junction in Taixing, China. Int J Cancer. 2022;150:243–52.PubMedCrossRef
28.
Hansen S, Vollset SE, Derakhshan MH, Fyfe V, Melby KK, Aase S, Jellum E, McColl KEL. Two distinct aetiologies of cardia cancer; evidence from premorbid serological markers of gastric atrophy and Helicobacter pylori status. Gut. 2007;56:918–25.PubMedPubMedCentralCrossRef
29.
Holleczek B, Schöttker B, Brenner H. Helicobacter pylori infection, chronic atrophic gastritis and risk of stomach and esophagus cancer: results from the prospective population-based ESTHER cohort study. Int J Cancer. 2020;146:2773–83.PubMedCrossRef
30.
Iijima K, Koike T, Abe Y, Inomata Y, Sekine H, Imatani A, Nakaya N, Ohara S, Shimosegawa T. Extensive gastric atrophy: an increased risk factor for superficial esophageal squamous cell carcinoma in Japan. Am J Gastroenterol. 2007;102:1603–9.PubMedCrossRef
31.
Ikeda F, Shikata K, Hata J, Fukuhara M, Hirakawa Y, Ohara T, Mukai N, Nagata M, Yoshida D, Yonemoto K, et al. Combination of Helicobacter pylori antibody and serum pepsinogen as a good predictive tool of gastric cancer incidence: 20-year prospective data from the hisayama study. J Epidemiol. 2016;26:629–36.PubMedCrossRef
32.
In H, Sarkar S, Ward J, Friedmann P, Parides M, Yang J, Epplein M. Serum pepsinogen as a biomarker for gastric cancer in the united states: a nested case-control study using the PLCO cancer screening trial data. Cancer Epidemiol Biomark Prev. 2022;31:1426–32.CrossRef
33.
Inoue M, Sawada N, Goto A, Shimazu T, Yamaji T, Iwasaki M, Tsugane S. High-negative anti-helicobacter pylori igg antibody titers and long-term risk of gastric cancer: results from a large-scale population-based cohort study in Japan. Cancer Epidemiol Biomark Prev. 2020;29:420–6.CrossRef
34.
Inoue M, Tajima K, Matsuura A, Suzuki T, Nakamura T, Ohashi K, Nakamura S, Tominaga S. Severity of chronic atrophic gastritis and subsequent gastric cancer occurrence: a 10-year prospective cohort study in Japan. Cancer Lett. 2000;161:105–12.PubMedCrossRef
35.
Nasrollahzadeh D, Malekzadeh R, Aghcheli K, Sotoudeh M, Merat S, Islami F, Kamangar F, Abnet CC, Shakeri R, Pourshams A, et al. Gastric atrophy and oesophageal squamous cell carcinoma: possible interaction with dental health and oral hygiene habit. Br J Cancer. 2012;107:888–94.PubMedPubMedCentralCrossRef
36.
Sasazuki S, Inoue M, Iwasaki M, Otani T, Yamamoto S, Ikeda S, Hanaoka T, Tsugane S. Effect of Helicobacter pylori infection combined with CagA and pepsinogen status on gastric cancer development among Japanese men and women: a nested case–control study. Cancer Epidemiol Biomark Prev. 2006;15:1341–7.CrossRef
37.
Song H, Ekheden IG, Zheng Z, Ericsson J, Nyrén O, Ye W. Incidence of gastric cancer among patients with gastric precancerous lesions: observational cohort study in a low risk Western population. BMJ (Clin Res Ed). 2015;351:h3867.
38.
Venerito M, Kohrs S, Wex T, Adolf D, Kuester D, Schubert D, Peitz U, Mönkemüller K, Malfertheiner P. Helicobacter pylori infection and fundic gastric atrophy are not associated with esophageal squamous cell carcinoma: a case–control study. Eur J Gastroenterol Hepatol. 2011;23:859–64.PubMedCrossRef
39.
Vohlonen I, Pukkala E, Malila N, Härkönen M, Hakama M, Koistinen V, Sipponen P. Risk of gastric cancer in Helicobacter pylori infection in a 15-year follow-up. Scand J Gastroenterol. 2016;51:1159–64.PubMedPubMedCentralCrossRef
40.
Watanabe Y, Kurata JH, Mizuno S, Mukai M, Inokuchi H, Miki K, Ozasa K, Kawai K. Helicobacter pylori infection and gastric cancer. A nested case–control study in a rural area of Japan. Digest Dis Sci. 1997;42:1383–7.PubMedCrossRef
41.
Ye W, Held M, Lagergren J, Engstrand L, Blot WJ, McLaughlin JK, Nyrén O. Helicobacter pylori infection and gastric atrophy: risk of adenocarcinoma and squamous-cell carcinoma of the esophagus and adenocarcinoma of the gastric cardia. J Natl Cancer Inst. 2004;96:388–96.PubMedCrossRef
42.
Shao L, Li P, Ye J, Chen J, Han Y, Cai J, Lu X. Risk of gastric cancer among patients with gastric intestinal metaplasia. Int J Cancer. 2018;143:1671–7.PubMedCrossRef
43.
Sui Z, Chen J, Li P, Shao L, Ye J, Lu X, Cai J. Risk for gastric cancer in patients with gastric atrophy: a systematic review and meta-analysis. Transl Cancer Res. 2020;9:1618–24.PubMedPubMedCentralCrossRef
44.
Kirikoshi H, Sekihara H, Katoh M. Up-regulation of WNT10A by tumor necrosis factor alpha and Helicobacter pylori in gastric cancer. Int J Oncol. 2001;19:533–6.PubMed
45.
Kirikoshi H, Inoue S, Sekihara H, Katoh M. Expression of WNT10A in human cancer. Int J Oncol. 2001;19:997.PubMed
46.
Long A, Giroux V, Whelan KA, Hamilton KE, Tétreault M-P, Tanaka K, Lee J-S, Klein-Szanto AJ, Nakagawa H, Rustgi AK. WNT10A promotes an invasive and self-renewing phenotype in esophageal squamous cell carcinoma. Carcinogenesis. 2015;36:598–606.PubMedPubMedCentralCrossRef
47.
Craddock VM. Aetiology of oesophageal cancer: some operative factors. Eur J Cancer Prev. 1992;1:89.PubMedCrossRef
48.
Derakhshan MH, El-Omar E, Oien K, Gillen D, Fyfe V, Crabtree JE, McColl KEL. Gastric histology, serological markers and age as predictors of gastric acid secretion in patients infected with Helicobacter pylori. J Clin Pathol. 2006;59:1293–9.PubMedPubMedCentralCrossRef
49.
Husebye E. The pathogenesis of gastrointestinal bacterial overgrowth. Chemotherapy. 2005;51(Suppl):1.PubMedCrossRef
50.
Lagergren J, Bergström R, Lindgren A, Nyrén O. Symptomatic gastroesophageal reflux as a risk factor for esophageal adenocarcinoma. N Engl J Med. 1999;340:825–31.PubMedCrossRef
51.
Brandt S, Kwok T, Hartig R, König W, Backert S. NF-kappaB activation and potentiation of proinflammatory responses by the Helicobacter pylori CagA protein. Proc Natl Acad Sci USA. 2005;102:9300–5.PubMedPubMedCentralCrossRef
52.
Sharma T, Gupta A, Chauhan R, Bhat AA, Nisar S, Hashem S, Akhtar S, Ahmad A, Haris M, Singh M, Uddin S. Cross-talk between the microbiome and chronic inflammation in esophageal cancer: potential driver of oncogenesis. Cancer Metastasis Rev. 2022;41:281–99.PubMedPubMedCentralCrossRef
53.
Pimentel-Nunes P, Libânio D, Marcos-Pinto R, Areia M, Leja M, Esposito G, Garrido M, Kikuste I, Megraud F, Matysiak-Budnik T, et al. Management of epithelial precancerous conditions and lesions in the stomach (MAPS II): European Society of Gastrointestinal Endoscopy (ESGE), European Helicobacter and Microbiota Study Group (EHMSG), European Society of Pathology (ESP), and Sociedade Portuguesa de Endoscopia Digestiva (SPED) guideline update 2019. Endoscopy. 2019;51:365–88.PubMedCrossRef
54.
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.PubMedPubMedCentralCrossRef
55.
Huang Y-K, Yu J-C, Kang W-M, Ma Z-Q, Ye X, Tian S-B, Yan C. Significance of serum pepsinogens as a biomarker for gastric cancer and atrophic gastritis screening: a systematic review and meta-analysis. PLoS ONE. 2015;10:e0142080.PubMedPubMedCentralCrossRef
Metadata
Title
Chronic atrophic gastritis and risk of incident upper gastrointestinal cancers: a systematic review and meta-analysis
Authors
Junqiu Li
Jielu Pan
Dinghong Xiao
Nan Shen
Ruiqing Wang
Hongyv Miao
Peimin Pu
Haiyan Zhang
Xiao Yv
Lianjun Xing
Publication date
01-12-2024
Publisher
BioMed Central
Published in
Journal of Translational Medicine / Issue 1/2024
Electronic ISSN: 1479-5876
DOI
https://doi.org/10.1186/s12967-023-04736-w

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Keynote webinar | Spotlight on medication adherence

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Live: Thursday 27th June 2024, 18:00-19:30 (CEST)

WHO estimates that half of all patients worldwide are non-adherent to their prescribed medication. The consequences of poor adherence can be catastrophic, on both the individual and population level.

Join our expert panel to discover why you need to understand the drivers of non-adherence in your patients, and how you can optimize medication adherence in your clinics to drastically improve patient outcomes.

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