Study design

It was a multicenter, retrospective study in which 2099 patients underwent a complete diagnostic gastroscopy between March 2018 and October 2019, with biopsy samples taken for histopathological evaluation of gastritis. The patients whose examination was incomplete due to previous surgeries, intolerance, inappropriate preparation, or particular anatomical conditions were excluded. In 3 separate endoscopy units, the collected data included the patient’s age and sex, the endoscope type, sedation, inpatient or outpatient setting of the endoscopy, and indication for this examination. Imaging endoscopic data included the presence of gastritis, mucosal atrophy, gastric intestinal metaplasia, and their extent, as well as the location of the biopsies. In addition, data on the presence of a gastric ulcer, polyp, or tumor were recorded. Helicobacter pylori infection was diagnosed when a rapid urease test was positive or detected during a histopathological examination. All examinations were performed with the Olympus Exera III system using GIF‑Q165, GIF‑Q180, GIF‑H180J, and GIF‑HQ190 endoscopes (Hamburg, Germany).

Gastric specimens from all endoscopy units were sent to 3 different histopathological laboratories. Data on the presence and severity of AG, IM, and dysplasia were collected based on histopathological work‑up. Operative links for gastritis assessment (OLGA) and IM assessment (OLGIM) were calculated based on the histopathological reports.^14,15 AG of at least a moderate degree in both the corpus and antrum, and IM in both the corpus and antrum, OLGA/OLGIM III/IV were considered advanced stages of AG according to MAPS II guidelines.¹³ To assess the advanced stages of AG, only examinations with biopsies obtained from the corpus and antrum to separate the containers were evaluated. The gastroscopies with the biopsies obtained from the corpus and antrum to the same container were only evaluated for global IM and AG detection performance. The procedures in which the samples were taken from the corpus or antrum were evaluated for global AG and IM detection and their detection in the corpus or antrum, respectively. The study was conducted with the ethical review board approval (PCN/022/KB/40/21).

Statistical analysis

Qualitative features were presented as frequencies and percentages. Quantitative features were characterized with the mean value and SD. Median and interquartile range (IQR) were applied if a nonparametric test was performed to compare quantitative features in each group. The Shapiro–Wilk test determined, if the quantitative data were normally distributed. The Levene test was used to verify the homogeneity of variance. The ANOVA or the Kruskal–Wallis test with multiple comparisons compared features between more than 2 groups.

Multivariable logistic regression models were computed to determine how selected risk factors, such as age, male sex, use of a HD instrument, outpatient procedure setting, use of sedation, the occurrence of gastritis, gastric polyps, gastric ulcer, influence the odds of occurrence of AG, IM, dysplasia, and advanced stage of AG. The results were reported as odds ratio (OR) with 95% CI.

The efficiency of endoscopic diagnosis of GPC and advanced stage of AG were reported as sensitivity, specificity, accuracy, positive / negative likelihood ratio, and positive / negative predictive value. Receiver operating characteristic (ROC) curves and area under the curves were derived. The association between age and corresponding sensitivity, as well as specificity values of advanced stages of atrophic gastritis and dysplasia was generated. The sensitivity of detection of advanced stages of atrophic gastritis and dysplasia was calculated for age groups of 40, 45, 50, and 55 years with or without endoscopic detection of gastritis during the procedure. A potential reduction in the number of biopsies was calculated as the number of the patients in the study from whom the biopsies would not be obtained due to age or age and endoscopic detection of gastritis criteria that were not met.

A P value below 0.05 was considered significant. The collected data were grouped on Microsoft Excel spreadsheets and analyzed with STATISTICA v.13.1 (StatSoft Inc., Tulsa, Oklahoma, United States) for Windows.

General data

Based on histopathological reports of 2099 patients, AG, IM, and dysplasia were diagnosed in 262 (12.5%), 660 (31.4%), and 85 (4%) patients, respectively. The mean age of the patients was 59 years, and 59% were women. Seventy percent of EGDs were conducted as outpatient procedures, and 31.6% were performed under sedation. HD endoscopes were used in 47.6% of the procedures. The endoscopic data are summarized in Table 1. Of 85 patients identified with dysplasia, 79 were classified as low‑grade dysplasia, 1 as high‑grade dysplasia, and 5 as indefinite dysplasia.

Endoscopic diagnosis of atrophic gastritis and intestinal metaplasia

While atrophy was diagnosed during EGD in 35.4% of all patients, in the histopathological examination AG was diagnosed in 12.5% of all patients. Out of 262 patients with histopathological diagnosis of AG, endoscopy detected this pathology in 182 patients. Contrary to that, IM was endoscopically diagnosed in 7.6% of all patients, while it was found in 31.4% of all patients on the histopathological examination. Of 660 patients with histopathologically diagnosed IM, in only 128 it could be detected by the endoscopy. Both the sensitivity and specificity of endoscopic diagnosis of AG were 69.5%, while the sensitivity of endoscopy to detect IM was much lower, that is, 19.4% with a high specificity of 97.9% (Table 2). The diagnostic accuracy of AG and IM detection in the antrum was higher than in the corpus of the stomach. The sensitivity, specificity, and accuracy of GPC was 55%, 76.9%, and 68.5% in the examinations performed with non‑HD instruments, and 61.5%, 65.3%, and 64% with HD endoscopes.

Accuracy of endoscopic diagnosis of gastric precancerous conditions in patients with histologically proven advanced stage of atrophic gastritis

Ninety‑one of the patients were diagnosed with an advanced stage of AG (13.9% of patients whose biopsies were obtained from both the corpus and the antrum). Among them, gastritis was diagnosed during endoscopy in 89 patients, and AG or IM was suspected in 64 patients (70% sensitivity, 55.9% specificity) (Table 2).

Risk factors for histopathological diagnosis of gastric precancerous conditions and dysplasia

Dysplastic foci were found in the histopathological specimens in 85 patients. Based on the endoscopy, 82 patients were diagnosed with gastritis, and AG or IM was recognized in 55 patients.

In the multivariable logistic regression, the patient’s age and endoscopic diagnosis of gastritis were the risk factors for the occurrence of both AG and IM. The outpatient procedure was a risk factor for AG diagnosis but at the same time an opposite risk factor for IM diagnosis. Sedation during the procedure was an opposite risk factor for AG and IM diagnosis. Performing EGD with a HD endoscope was a risk factor for AG diagnosis without any influence on the detection of IM, dysplasia, and advanced stage of AG. Age was the only risk factor for an advanced stage of AG and dysplasia (Table 3).

Age and endoscopic diagnosis of gastritis as conditions for biopsy to evaluate gastric precancerous conditions

Patients with biopsies obtained from the corpus and antrum were divided into 5 groups: (1) advanced stage of AG, (2) dysplasia, (3) GPC in the corpus and antrum classified as nonadvanced AG, (4) GPC in the corpus or antrum, (5) patients without GPC and dysplasia. The median (IQR) age of patients was 66 (60–73), 70 (62–78), 67 (60–79), 63 (53–71), and 58 (49–68) years for groups 1 to 5, respectively. The age of the patients in the group 5 was significantly lower than in the other groups, and the age of the patients in the group 4 was significantly lower than in group 2 (P <⁠0.05).

The ROC curve analysis was performed to assess the targeted age group for a biopsy to evaluate GPC. The area under the ROC curve for age according to advanced stages of gastritis was 0.647 and 0.663, including patients with dysplasia (Figure 1). The highest Youden score for advanced stages of AG was achieved for patients aged 56 years (0.254), and for advanced stages of AG or dysplasia for patients aged 62 years (0.266).

As endoscopically diagnosed gastritis was another risk factor for detecting AG and IM, we analyzed the diagnostic significance of the combination of age and gastritis. The age threshold of 45 or 40 years and finding of gastritis resulted in at least 95% sensitivity for the diagnosis of advanced stage of AG or dysplasia, with a 20% reduction in the number of patients with biopsies. These data are summarized in Table 4.

Limitations and conclusions

The main limitation of our study is its retrospective design. For this reason, we could not evaluate AG and IM in relation to clinical data and family history. We were also unable to evaluate the significance of using NBI for the diagnostic performance of endoscopy. Also, we could not evaluate either the exact anatomical locations where the biopsies were collected or the number of specimens.

In conclusion, the endoscopic diagnosis of GPC is still not adequate and insufficient to replace histology in a real‑life scenario, as it provides too many false positive and negative results. However, the number of mapping biopsies may be reduced in patients younger than 45 years or younger than 40 years and without an endoscopic diagnosis of gastritis.