Prevalence of chronic atrophic gastritis worldwide from 2010 to 2020: an updated systematic review and meta-analysis
Original Article

Prevalence of chronic atrophic gastritis worldwide from 2010 to 2020: an updated systematic review and meta-analysis

Yuan Yin, Hongliang Liang, Na Wei, Zhiqiang Zheng

Department of Gastroenterology, 363 Hospital, Chengdu, China

Contributions: (I) Conception and design: H Liang; (II) Administrative support: H Liang; (III) Provision of study materials or patients: N Wei; (IV) Collection and assembly of data: Y Yin; (V) Data analysis and interpretation: Z Zheng; (VI) Manuscript writing: All authors; (VII) Final approval of manuscript: All authors.

Correspondence to: Prof. Zhiqiang Zheng. Department of Gastroenterology, 363 Hospital, No. 108 Daosangshu Street, Wuhou District, Chengdu 610041, China. Email: 2467350937@qq.com.

Background: Gastric cancer ranks 4th in cancer incidence and ranks 2nd in leading to cancer-related deaths worldwide. The present study aimed to provide an updated overview of the prevalence of chronic atrophic gastritis (CAG), one of the precancerous lesions of gastric cancer, in the recent 10 years and its association with Helicobacter pylori (HP) infection.

Methods: A meta-analysis of follow-up studies worldwide in the recent 10 years was performed by systematically searching in Web of Science, PubMed, Cochrane, and Embase.

Results: A total of 14 studies were finally enrolled in the present meta-analysis. The pooled results showed that the prevalence of CAG was about 25% in the study population, and the risk of CAG was about 2.4-fold higher in HP-positive patients than in those who were HP negative. Subgroup analyses showed that both the prevalence of CAG and the risk of CAG in HP-positive patients were higher when infection was diagnosed by histology than by serology.

Conclusions: The worldwide prevalence of CAG is still high, and HP infection remains an important risk factor for CAG. Future studies of large-scale are still in urgent need to further control the prevalence of CAG, so as to reduce the burden of gastric cancer.

Keywords: Chronic atrophic gastritis (CAG); prevalence; meta-analysis

Submitted Mar 16, 2022. Accepted for publication Jun 29, 2022.

doi: 10.21037/apm-21-1464

Introduction

Gastric cancer ranks 4th in cancer incidence and ranks 2nd in leading to cancer-related deaths worldwide (1). The public health burden of gastric cancer is still very high even though its incidence has declined in recent years (2).

Chronic atrophic gastritis (CAG) is one of a series of precancerous lesions that occurs in the gastric mucosa before the appearance of the intestinal subtype of gastric cancer. In general, the process is from non-atrophic gastritis to CAG, then to intestinal metaplasia, dysplasia and finally to adenocarcinoma (3). To understand the occurrence of this cancer and to determine the risk factors for its incidence, it is important to study the precursor lesions and the risk factors related to their incidence.

Helicobacter pylori (HP) infection is such a risk factor that was shown to be strongly associated with the incidence of CAG in a previous meta-analysis (4). Marques-Silva et al. also performed a meta-analysis regarding the prevalence of CAG, however, that analysis only included studies published before March, 2013 (5). Now eight years has passed, and we believed that an updated meta-analysis with more recent relevant studies included will provide more accurate data on the incidence of CAG. Therefore, we performed the present analysis of follow-up studies to further prove the causal role of HP infection in the development of CAG. The present meta-analysis aimed to provide an updated overview of the prevalence of CAG in the recent 10 years and its association with HP infection. We present the following article in accordance with the PRISMA reporting checklist (available at https://apm.amegroups.com/article/view/10.21037/apm-21-1464/rc). This study has been registered in PROSPERO, and the registration number is “CRD42021250872”.

Methods

Search strategy

This study followed the PRISMA Statement (Preferred Reporting Items for Systematic Reviews and Meta-Analysis) (6). A systemic search was performed in Web of Science, PubMed, Cochrane, and Embase for articles from 2010 to 2020. No language restrictions were set, and the search strategy was as follows: ((prevalence) or (rate)) and ((chronic atrophic gastritis) or (atrophic chronic gastritis)) and ((endoscopy) or (biopsy) or (histology) or (serology)).

Selection criteria

Inclusion criteria were articles addressing atrophic gastritis conditions, published in indexed journals from January 1, 2010 to December 1, 2020, including cross-sectional or retrospective articles. Reasons for exclusion included opinion articles or case reports, studies of experimental design, participants selected according to their previous conditions, and studies not reporting the relevant data clearly.

Data collection

Two authors independently collected the data from the enrolled studies using a data collection sheet. Information collected included first author, year of publication, diagnostic methods of CAG, demographic characteristics of the study population (country, population type, sample size, age, sex ratios of study participants). Data on the status of HP was also collected if the relevant data were reported. Discrepancies were resolved by a third reviewer.

Statistical analysis

A meta-analysis of the prevalence of CAG and the correlation between HP infection and the prevalence of CAG was performed using a random effects model. For the latter analysis, the relative efficacy was measured using risk ratios (RRs) with their corresponding 95% confidence intervals (CIs). The heterogeneity between studies was evaluated using a Q test, in which I2<50% and P>0.05 indicated no significant heterogeneity (7,8). The robustness of the results was tested using sensitivity analysis by omitting studies sequentially. Also, we performed subgroup analyses to address the diagnostic methods of CAG and population type. STATA (version 15.0, STATA MP) was used to perform all analyses.

Results

Baseline characteristics

The final number of studies enrolled in this meta-analysis was 14. Figure 1 shows the detailed selection process (9-22), and the baseline characteristics of the studies are summarized in Table 1. The studies were conducted in 11 countries including China, Italy, Canada, Columbia and so on, and were distributed in Asia, Europe, and North and South America. Sample sizes ranged from 93 to 5,284, and the age of the participants ranged from 1 to 83 years, with the proportion of female ranging from 37.7% to 70.4%. A total of 10 studies used histological methods to diagnose CAG, and the remaining 4 used serological methods.

Figure 1 Flowchart for the selection of studies to be included in the meta-analysis.

Table 1

Baseline characteristics of enrolled studies

Study Country Sample size Population type Age (years), median [range] Women, n (%) Determination of CAG HP+ HP–
CAG Non-CAG CAG Non-CAG
Emura et al. 2010 Columbia 650 General NR [49–70] 390 (60.0) Histology NR NR NR NR
Cam et al. 2014 Turkey 750 General 10.1 [1–18] 362 (48.3) Histology 24 366 1 359
Song et al. 2015 Sweden 5,284 General NR [35–64] 2,420 (45.8) Serology NR NR NR NR
Roman et al. 2016 Russia 918 General 51.8 [26–83] 646 (70.4) Serology NR NR NR NR
Bas et al. 2020 Turkey 2,214 General NR [18–69] 929 (42.0) Histology 493 924 84 713
Fagan-Garcia et al. 2019 Canada 308 General NR [0–96] 171 (55.5) Histology 96 128 0 84
Muhsen et al. 2019 Israel 1,644 General NR [25–78] 774 (47.1) Serology 75 1,144 50 375
Kikuchi et al. 2011 Japan 300 Selected NR [22–87] 113 (37.7) Histology NR NR NR NR
Eshmuratov et al. 2010 Korea 1,330 Selected NR 551 (41.4) Histology 679 428 81 142
Lombardo et al. 2010 Italy 1,387 Selected 40 [18–80] 704 (50.8) Serology NR NR NR NR
Rugge et al. 2010 Italy 93 Selected 55 [22–73] 45 (48.4) Histology NR NR NR NR
Alina et al. 2011 Israel 1,651 Selected NR 834 (50.5) Histology 234 506 60 851
Liu et al. 2010 China 1,179 Selected 52.5 [35–85] 621 (52.7) Histology NR NR NR NR
Haziri et al. 2010 Kosova 802 Selected NR 369 (46.0) Histology 93 386 48 275

CAG, chronic atrophic gastritis; HP, Helicobacter pylori; NR, not reported.

Prevalence of CAG

As shown in Figure 2, the pooled results of all 14 studies indicated that the prevalence of CAG worldwide was 25% (95% CI: 18–32%). However, a significant heterogeneity was observed in this analysis, as I2=99.5% and P<0.001. No significant change in the results was found when sensitivity analyses were performed by omitting each study sequentially. The results of subgroup analysis by population type are shown in Figure S1. We found that the prevalence of CAG was 16% (95% CI: 10–22%) in the general population and 35% (95% CI: 21–48%) in the selected population. We also found that the prevalence of CAG was generally higher when diagnosed by histology [32% (95% CI: 20–43%)] than by serology [10% (95% CI: 6–13%)], as shown in Figure S2. The heterogeneity was still significant in these subgroup analyses.

Figure 2 Forest plot for the prevalence of chronic atrophic gastritis worldwide from 2010 to 2020. CI, confidence interval; ES, effect size.

Association between HP and the prevalence of CAG

As shown in Figure 3, HP infection was associated with a significant higher risk of CAG, with an RR of 2.40 (95% CI: 2.16–2.67). A significant heterogeneity was also observed as I2=96.0% and P<0.001. Similarly, there was no significant change in the results when performing sensitivity analyses by omitting each study sequentially. The results of subgroup analysis by population type are shown in Figure S3; the RR of 2.56 (95% CI: 2.16–3.03) in the general population was found to be similar to the RR of 2.28 (95% CI: 2.00–2.60) in the selected population. As shown in Figure S4, subgroup analysis by diagnostic methods showed that RR of 2.78 (95% CI: 2.49–3.12) was higher when diagnosed by histology. However, only one study used serology to diagnose CAG, so this subgroup analysis was not available. The heterogeneity remained significant when performing these analyses.

Figure 3 Forest plot for the association between Helicobacter pylori infection and the incidence of chronic atrophic gastritis. CI, confidence interval; RR, risk ratio.

Discussion

The present study is the most recent meta-analysis of the related topic. It aimed to provide the updated prevalence of CAG and explore changes over the past 10 years, in order to provide some guidance for future clinical decision making. In total, 14 studies with data on the prevalence of CAG were identified, among which the prevalence rates ranged from 6% to 66%. Our pooled results showed that 25% of people worldwide may have CAG, which is lower than previously reported in a meta-analysis published in 2014 (5). Most of the literature enrolled in that meta-analysis was from 1990 to 2010, and the lower prevalence observed in our results might reflect improvements in people's lifestyles and more efforts being made on the screening and treatment of precancerous gastric diseases.

It has been reported that HP infection is strongly associated with the occurrence of CAG (4). The increase in the prevalence of CAG in HP-positive patients was expected and was confirmed by our study. The prevalence of CAG was found to be 2.4-fold higher in HP-positive patients compared with those who were HP negative. This ratio was similar to the result from the previous meta-analysis described above (5), but s lower than reported in another meta-analysis published in 2010 (23). Most of the studies enrolled in the 2010 meta-analysis were published in the 1990s. One potential explanation for the decreased risk of CAG over time in HP-positive patients might be the development of tolerance to the virulence of HP.

Another important finding of our study was that both the population type and the diagnostic method used could affect the prevalence of CAG. People with upper gastrointestinal symptoms were naturally more likely to have CAG than those without symptoms, which is also why the prevalence of CAG in our study was higher in the selected population than in the general population. Both the prevalence of CAG and the risk of CAG in HP-positive patients were found to be higher when diagnosed by histology than by serology, and one possible reason for this might be the low sensitivity of serology to diagnose CAG.

However, there are some limitations of this analysis that should be kept in mind. First, there was a huge heterogeneity in the existing literature. For example, the diagnostic criteria of CAG varied among different studies, and different methods were used in different studies to assess HP infection. Second, the number of studies that reported the status of HP infection and the corresponding sample sizes were small, which might affect the statistical results. Third, because only one author collected the data, mistakes are more likely. Finally, because of a lack of data, we failed to analyze the many potential risk factors for CAG other than HP infection.

Generally speaking, the worldwide prevalence of CAG is still high, and HP infection remains an important risk factor for CAG Future studies of large-scale are still in urgent need to further control the prevalence of CAG, so as to reduce the burden of gastric cancer. We believe that eradication of HP infection will effectively reduce the incidence rate of CAG. Other measures to prevent CAG include improving eating habits and enhancing physical exercise.

Conclusions

This is the most recent meta-analysis to investigate the prevalence of CAG, which was found to be ~25% in the general population, and the risk of CAG was ~2.4-fold higher in HP-positive patients than in those who were HP negative. Further analyses involving more studies with more participants are still needed to investigate the future prevalence of CAG and its risk factors.

Acknowledgments

Funding: None.

Footnote

Reporting Checklist: The authors have completed the PRISMA reporting checklist. Available at https://apm.amegroups.com/article/view/10.21037/apm-21-1464/rc

Conflicts of Interest: All authors have completed the ICMJE uniform disclosure form (available at https://apm.amegroups.com/article/view/10.21037/apm-21-1464/coif). The authors have no conflicts of interest to declare.

Ethical Statement: The authors are accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved.

Open Access Statement: This is an Open Access article distributed in accordance with the Creative Commons Attribution-NonCommercial-NoDerivs 4.0 International License (CC BY-NC-ND 4.0), which permits the non-commercial replication and distribution of the article with the strict proviso that no changes or edits are made and the original work is properly cited (including links to both the formal publication through the relevant DOI and the license). See: https://creativecommons.org/licenses/by-nc-nd/4.0/.

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(English Language Editor: K. Brown)

Cite this article as: Yin Y, Liang H, Wei N, Zheng Z. Prevalence of chronic atrophic gastritis worldwide from 2010 to 2020: an updated systematic review and meta-analysis. Ann Palliat Med 2022;11(12):3697-3703. doi: 10.21037/apm-21-1464

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