Chronic atrophic gastritis and risk of incident upper gastrointestinal cancers: a systematic review and meta-analysis.
Chronic atrophic gastritis
Gastric cancer
Meta-analysis
Oesophageal cancer
Oesophagogastric junction cancer
Upper gastrointestinal cancers
Journal
Journal of translational medicine
ISSN: 1479-5876
Titre abrégé: J Transl Med
Pays: England
ID NLM: 101190741
Informations de publication
Date de publication:
06 May 2024
06 May 2024
Historique:
received:
01
10
2023
accepted:
15
11
2023
medline:
7
5
2024
pubmed:
7
5
2024
entrez:
6
5
2024
Statut:
epublish
Résumé
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. 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. 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. 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.
Sections du résumé
BACKGROUND
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
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
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
CONCLUSIONS
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.
Identifiants
pubmed: 38711123
doi: 10.1186/s12967-023-04736-w
pii: 10.1186/s12967-023-04736-w
doi:
Types de publication
Meta-Analysis
Systematic Review
Journal Article
Research Support, Non-U.S. Gov't
Review
Langues
eng
Sous-ensembles de citation
IM
Pagination
429Subventions
Organisme : National Natural Science Foundation of China
ID : 82174240
Organisme : Shanghai Pudong New Area Health Commission
ID : PWRzm2020-03
Informations de copyright
© 2024. The Author(s).
Références
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.
pubmed: 34967848
doi: 10.1001/jamaoncol.2021.6987
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.
pubmed: 35689438
doi: 10.1002/ijc.34160
Abnet CC, Corley DA, Freedman ND, Kamangar F. Diet and upper gastrointestinal malignancies. Gastroenterology. 2015;148:1234.
pubmed: 25680671
doi: 10.1053/j.gastro.2015.02.007
Coussens LM, Werb Z. Inflammation and cancer. Nature. 2002;420:860–7.
pubmed: 12490959
pmcid: 2803035
doi: 10.1038/nature01322
Mantovani A, Allavena P, Sica A, Balkwill F. Cancer-related inflammation. Nature. 2008;454:436–44.
pubmed: 18650914
doi: 10.1038/nature07205
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.
pubmed: 21285949
doi: 10.1038/ajg.2011.1
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.
pubmed: 14735480
doi: 10.1002/ijc.11680
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.
pubmed: 26349170
doi: 10.7869/tg.224
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.
pubmed: 17728213
doi: 10.1093/jnci/djm120
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.
pubmed: 31348819
pmcid: 6660080
doi: 10.1371/journal.pone.0219865
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.
pubmed: 29228909
pmcid: 5725642
doi: 10.1186/s12876-017-0708-4
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.
pubmed: 20860989
doi: 10.1093/annonc/mdq411
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.
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.
pubmed: 33632720
doi: 10.1136/bmjebm-2020-111651
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.
pubmed: 34454714
doi: 10.1053/j.gastro.2021.06.078
Sjs HJ. Classification of adenocarcinoma of the oesophagogastric junction. Br J Surg. 1998;85:1457–9.
Lo CK-L, Mertz D, Loeb M. Newcastle–Ottawa Scale: comparing reviewers’ to authors’ assessments. BMC Med Res Methodol. 2014;14:45.
pubmed: 24690082
pmcid: 4021422
doi: 10.1186/1471-2288-14-45
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.
pubmed: 17689803
doi: 10.1016/j.jclinepi.2006.12.001
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.
pubmed: 19450276
pmcid: 2689248
doi: 10.1186/1471-230X-9-34
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.
pubmed: 23599625
pmcid: 3623983
doi: 10.3748/wjg.v19.i13.2060
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.
pubmed: 18025067
doi: 10.1136/gut.2007.132662
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.
pubmed: 8678045
doi: 10.1093/oxfordjournals.aje.a008901
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.
pubmed: 20647397
pmcid: 2919643
doi: 10.1158/1055-9965.EPI-10-0270
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.
pubmed: 19107937
doi: 10.1002/ijc.23955
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.
pubmed: 31899792
pmcid: 7443753
doi: 10.1093/aje/kwz283
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.
pubmed: 7737912
doi: 10.1111/j.1349-7006.1995.tb02989.x
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.
pubmed: 34498732
doi: 10.1002/ijc.33801
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.
pubmed: 17317788
pmcid: 1994366
doi: 10.1136/gut.2006.114504
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.
pubmed: 31376284
doi: 10.1002/ijc.32610
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.
pubmed: 17488251
doi: 10.1111/j.1572-0241.2007.01257.x
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.
pubmed: 27265836
doi: 10.2188/jea.JE20150258
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.
doi: 10.1158/1055-9965.EPI-21-1328
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.
doi: 10.1158/1055-9965.EPI-19-0993
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.
pubmed: 11078919
doi: 10.1016/S0304-3835(00)00603-0
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.
pubmed: 22814581
pmcid: 3425966
doi: 10.1038/bjc.2012.332
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.
doi: 10.1158/1055-9965.EPI-05-0901
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.
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.
pubmed: 21811162
doi: 10.1097/MEG.0b013e3283496469
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.
pubmed: 27338132
pmcid: 4960513
doi: 10.1080/00365521.2016.1183225
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.
pubmed: 9246033
doi: 10.1023/A:1018833819860
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.
pubmed: 14996860
doi: 10.1093/jnci/djh057
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.
pubmed: 29707766
doi: 10.1002/ijc.31571
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.
pubmed: 35117509
pmcid: 8798867
doi: 10.21037/tcr.2020.01.54
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: 11494032
Kirikoshi H, Inoue S, Sekihara H, Katoh M. Expression of WNT10A in human cancer. Int J Oncol. 2001;19:997.
pubmed: 11605000
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.
pubmed: 25795715
pmcid: 4498148
doi: 10.1093/carcin/bgv025
Craddock VM. Aetiology of oesophageal cancer: some operative factors. Eur J Cancer Prev. 1992;1:89.
pubmed: 1463984
doi: 10.1097/00008469-199202000-00002
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.
pubmed: 16644877
pmcid: 1860535
doi: 10.1136/jcp.2005.036111
Husebye E. The pathogenesis of gastrointestinal bacterial overgrowth. Chemotherapy. 2005;51(Suppl):1.
pubmed: 15855746
doi: 10.1159/000081988
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.
pubmed: 10080844
doi: 10.1056/NEJM199903183401101
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.
pubmed: 15972330
pmcid: 1166591
doi: 10.1073/pnas.0409873102
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.
pubmed: 35511379
pmcid: 9363391
doi: 10.1007/s10555-022-10026-6
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.
pubmed: 30841008
doi: 10.1055/a-0859-1883
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.
pubmed: 19230047
pmcid: 2653386
doi: 10.3748/wjg.15.853
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.
pubmed: 26556485
pmcid: 4640555
doi: 10.1371/journal.pone.0142080