Research ArticleClinical Studies
Open Access

Histopathology Features of H. pylori Gastritis Associated With Altered Lipid Profile: An Observational Study from a Tertiary Healthcare Center in North West Romania

IOANA ALEXANDRA CARDOS, CATALINA DANILA, TIMEA CLAUDIA GHITEA, OVIDIU POP, ANDREI PASCALAU and SIMONA CAVALU
In Vivo May 2024, 38 (3) 1421-1428; DOI: https://doi.org/10.21873/invivo.13584

Abstract

Background/Aim: H. pylori infection can promote a systemic inflammatory syndrome, eventually leading to intestinal metaplasia and gastric cancer. The aim of our study was to investigate the possible association between dyslipidemia and histopathological features of H. pylori gastritis. Patients and Methods: An observational, retrospective study was conducted over the period 2017-2022 on symptomatic patients with a positive rapid urease test. A total of 121 patients who underwent upper gastrointestinal endoscopy with stomach biopsy were enrolled in this study. Based on the updated Sydney System, we investigated the association between neutrophils, mononuclear cells, intestinal metaplasia, or gastric atrophy and altered lipid profiles. Results: A high prevalence of H. pylori infection was noticed in the studied group upon the application of the rapid urease test, being associated with dyslipidemia regardless of patient sex. All the endoscopic diagnoses (acute, chronic, or atrophic chronic gastritis, metaplasia) correlated with the histopathological features. Mononuclear cells and metaplasia were more likely to be found in H. pylori-positive patients with dyslipidemia, which is consistent with acute and chronic inflammation caused by H. pylori in the gastric mucosa. Conclusion: Although our study was conducted on a small scale, it offers new insights and details regarding H. pylori infection and histopathological features. Mononuclear cells and metaplasia were associated with an altered lipid profile in H. pylori-positive patients. These findings warrant future investigation, such as the evolution of gastric biopsies and lipid profiles before and after eradication.

Key Words:

H. pylori is a genetically diversified pathogen with a constrained host and target organ range (1). It is estimated that 50% of the world’s population is infected with H. pylori (2). The percentage is lower in developed countries and higher in developing ones, and it is more frequent in men than in women (3). It is a gram-negative bacterium that causes chronic gastritis, peptic ulcers, and stomach cancer (4, 5). Chronic and ongoing inflammation caused by H. pylori infection leads to the production of cytokines, such as tumor necrosis factor, interleukin (IL)-6, and IL-8 (6, 7). Consequently, a chronic inflammatory syndrome and extra-gastric diseases may develop, including non-alcoholic fatty liver disease, dyslipidemia, and coronary heart disease (8-11). By preventing the release of pro-inflammatory cytokines, H. pylori eradication therapy may improve lipid profiles in patients with dyslipidemia (12-14). In addition, H. pylori chronic inflammation may prevent proper lipid absorption (15). Furthermore, more changes in the metabolism of lipids and lipoproteins, induced by this infection, may allow transfer of nutrients to cells, which is crucial for tissue healing or host defense (16). Since H. pylori cannot produce cholesterol on its own, it must obtain exogenous cholesterol from the host (17). Glycosylated cholesterol (8), a significant constituent of H. pylori’s cell wall, is necessary for the bacteria to proliferate (18).

Previous studies evaluating the relationship between H. pylori infection and the serum lipid profile emphasized a negative correlation with high levels of HDL-cholesterol and a positive correlation with high levels of LDL-cholesterol, total cholesterol, and triglycerides. According to these studies, H. pylori infection has a major impact on serum lipid levels, which may result in abnormalities in the lipid profile (19).

However, there are few studies focused on the relationship between the histological features of gastritis and the lipid profile of H. pylori-infected patients (20). One study from South Korea evaluated the histological features of gastritis based on the Updated Sydney System and found an association between H. pylori infection, systemic inflammation response, and dyslipidemia (21).

In this context, the aim of this study was to assess whether there is any relation between H. pylori gastritis, more specifically histopathology features evaluated using the Updated Sydney System, and the lipid profile of the patients. Such a study has not yet been conducted in Eastern Europe, implicitly in Romania. Our results might contribute to the update of knowledge already reported in the literature by providing additional information on the influence of H. pylori infection on lipid profile alteration.

Patients and Methods

This is an observational, retrospective study conducted from 2017 to 2022 at the Emergency Clinical Hospital Oradea, Bihor County, Romania. A total of 121 dyspeptic patients aged over 18, registered in the Digestive Endoscopy Department, and underwent upper gastrointestinal endoscopy with stomach biopsy, were enrolled in this study. All patients were tested for H. pylori infection using the rapid urease test (RUT), and lipid profiles were assessed.

The study was conducted in accordance with the ethical principles of the Declaration of Helsinki and received approval from the institutional board of the Emergency Clinical Hospital Oradea, Bihor County, Romania (Approval No. CEFMF 01/28.11.2022). Informed consent was obtained from all subjects involved in the study. Written informed consent has been obtained from the patient(s) to publish this paper.

Endoscopy. The Olympus Exera II CV 165 endoscope (Olympus Medical System Corporation, Tokyo, Japan) was utilized for upper digestive tract endoscopy, with the same specialist performing the instrumentation. The assessment considered the following endoscopic findings: chronic and acute gastritis, and atrophic gastritis with or without metaplasia. Special attention was given to the evaluation of intestinal metaplasia and atrophic gastritis. Due to the mucosal thinning in atrophic gastritis, the submucosal vasculature is easily visible. The endoscopist evaluated the gastric mucosa for intestinal metaplasia, focusing on a pale color change with plaques, patches, or homogeneous discoloration (22). The endoscopist obtained a minimum of two samples (biopsies), one from the antrum and one from the corpus, to enhance the sensitivity of the test (23-25).

Rapid urease test for the diagnosis of Helicobacter pylori. The patients were diagnosed using the RUT (AMA Co Ltd., Lehmuskatu, Finland), which serves as the first-line indication for H. pylori. According to the literature, the rapid urease test has a sensitivity of 90% and specificity ranging from 95% to 100% (26).

Lipid profile. All blood samples were analyzed in the same laboratory, utilizing the Abbott Alinity™ s System equipment (Abbott Gmhb, Wiesbaden, Germany). The cut-off values used were as follows: 200 mg/dl for total cholesterol, 50 mg/dl for HDL cholesterol, 100 mg/dl for LDL cholesterol, and 150 mg/dl for triglycerides. All samples were collected from fasting patients, as this is an essential condition for accurate analysis, given that triglyceride values remain elevated for several hours after a meal (27).

Histopathology. The antrum served as the primary site for biopsy, which was subsequently fixed in 10% neutral formalin until histopathological analysis. The Pathology Department of the County Emergency Clinical Hospital of Oradea received all collected biopsies and embedded them in paraffin blocks. For histological investigation, two sets of tissue sections were assessed: one set was stained with Giemsa stain (Epredia-USA; Portsmouth, NH, USA), and the other with hematoxylin and eosin (H&E). Each tissue sample underwent a double-blind examination by two independent pathologists, evaluating the presence or absence of inflammatory mononuclear cellular infiltrates, inflammation activity (neutrophilic infiltrations), glandular atrophy, metaplasia, reparative atypia, and dysplasia (27, 28).

The results were assessed utilizing the Houston-updated Sydney system, which categorizes inflammation into absent (Grade 0), mild (Grade 1), moderate (Grade 2), and severe (Grade 3). The evaluation was conducted based on the following features: neutrophil infiltration, mononuclear-cell infiltration, glandular atrophy, intestinal metaplasia, and H. pylori density.

Statistical analysis. The data analysis was performed using the Statistical Product and Service Solutions (version 20; IBM, Armonk, NY, USA) computer software program. Means, frequency ranges, standard deviations, and statistical significance were calculated using Student’s t-test and the chi-square test. The relationship between two variables was assessed using the Bravais-Pearson correlation coefficient. Statistical significance was deemed at a level of p<0.05, with p<0.01 indicating high-level statistical significance. For further subgroup analysis to explore differences between groups, post-hoc analysis (Bonferroni) was conducted (29).

Results

Socio-demographic features of patients included in the study. The descriptive data of the patients are outlined in Table I. The majority of patients were female, from urban backgrounds, with a mean age of 62.9 years. Initially, our goal was to outline the prevalence of the infection among the tested subjects, revealing that H. pylori was present in 87% of the tested patients. Patients from urban environments were more likely to be infected, with a prevalence of 87% compared to 81% in rural areas.

View this table:
Table I.

Descriptive statistics on socio-demographic parameters.

Endoscopic diagnostics. As depicted in Figure 1, the most prevalent diagnosis was chronic gastritis (76%), primarily attributed to H. pylori (83%), establishing an association between chronic gastritis and H. pylori. Although less common, acute gastritis (22.3%) was predominantly associated with H. pylori as the causative factor (88.8%). A robust association between H. pylori and endoscopic diagnoses was also observed in atrophic gastritis (9.9%, with 91.6% being H. pylori positive) and intestinal metaplasia (20.6%, with 92% attributed to H. pylori infection). The chi-squared test yielded p-values <0.05, affirming an association between H. pylori infection and the investigated endoscopic diagnostics.

Figure 1.
Figure 1.

Endoscopy diagnostics according to the rapid urease test.

Lipid profile. We investigated whether H. pylori-positive patients were more likely to suffer from dyslipidemia and if this condition was more prevalent in a specific sex. The results yielded statistically significant values for both males and females (Table II).

View this table:
Table II.

Descriptive statistics on lipid profile.

We further explored whether the lipid profile was more altered in H. pylori-positive patients compared to negative ones. H. pylori-positive patients were more likely to develop dyslipidemia compared to the negative patients, without considering sex. We also observed more frequent occurrences of HDL-cholesterol values falling below the normal range and triglycerides exceeding the normal range in H. pylori-positive patients (Table III).

View this table:
Table III.

H. pylori prevalence and lipid profile of the patients (chi-squared test).

In Figure 2, a noticeable distinction of 48.6% is evident in total cholesterol, which is higher in individuals testing positive for H. pylori. Conversely, HDL cholesterol shows a decrease of 15.27% in those with a positive H. pylori status. Additionally, LDL cholesterol exhibits a 31.68% increase in individuals with H. pylori, and triglyceride levels rise by 28.28% in the presence of H. pylori.

Figure 2.
Figure 2.

Graphical presentation of H. pylori prevalence and lipid profile of the patients in our study. HDL-C: High density lipoprotein cholesterol; LDL-C: low density lipoprotein cholesterol; RUT: Rapid urease test.

Correlations between RUT and histological features (Updated Sydney System). As shown in Table IV, there were not many correlations between the results of the RUT test and the histopathology findings. Moderate neutrophil cell infiltration, characteristic of acute gastritis, was correlated with a negative RUT test, while positive RUT tests were associated with intestinal metaplasia (specific for H. pylori infection).

View this table:
Table IV.

H. pylori prevalence, and histopathology diagnostics of the patients in our study (chi-squared test).

Figure 3 presents relevant histopathological results. Using Hematoxylin-Eosin staining, Figure 3A features aspects of chronic gastritis, while Figure 3C presents the normal appearance of the antral gastric mucosa. Using Giemsa staining, Figure 3B identifies the presence of H. pylori, in contrast to Figure 3C, which depicts a normal gastric mucosa.

Figure 3.
Figure 3.

Histopathology aspects of the gastric mucosa using HE and Giemsa staining. A) Antral gastric mucosa showing aspects of mucus hypersecretion at the level of the lumen (yellow arrow). Edema and lymphocytic inflammatory infiltrate can be noted in the chorion (blue arrow). B) Antral gastric mucosa showing aspects of mucus hypersecretion at the level of the lumen (yellow arrow). In Giemsa staining, the presence of H. pylori is identified in contact with the gastric glands (red arrow). C) Antral gastric mucosa showing normal aspects at the level of the lumen (yellow arrow). The chorion is edematous with the presence of rare lymphocytes. D) Microorganisms are not identified in Giemsa staining.

Pearson correlation on research parameters features. Table V presents the Pearson correlation coefficient for the histopathology results and positive RUT test, respectively, as well as for the histopathology results and endoscopic diagnostics. It also presents the Pearson correlation coefficient for the modified lipid profile (total cholesterol, HDL, LDL, and triglyceride values) with the RUT test and, respectively, with the endoscopic diagnostics. In almost all cases, the endoscopic diagnosis correlated with the histopathological diagnosis.

View this table:
Table V.

Pearson correlation on research parameters.

Association between lipid profile and histopathology results. In our study, dyslipidemia was predominantly associated with mononuclear cells, followed by neutrophil cells. This finding held true for both positive and negative patients, with a more pronounced association observed in the H. pylori positive group, as indicated in Table VI.

View this table:
Table VI.

Lipid profile and histopathology results according to the rapid urease test, using Chi-square test.

Discussion

Worldwide, H. pylori is an infection with a high prevalence rate, and influenced by various factors, such as sex, age, socio-economic status, geographic area, diet, and lifestyle (30). In Romania, the prevalence of H. pylori infection remains largely unexplored, and comprehensive data are lacking. Our study revealed a high prevalence of H. pylori infection (87%), significantly surpassing percentages reported in a previous study conducted in the North-West part of Romania (31). Moreover, our figure exceeded that reported by Zamani et al. in 2018 (3) encompassing a comprehensive study across 73 countries and 6 continents, which found an overall prevalence of 44.3% [95% confidence interval (CI)=40.9-47.7], exhibiting considerable variation between geographic areas. A plausible explanation lies in the fact that our study focused on dyspeptic patients, diagnosed with acute gastritis, chronic gastritis, atrophic gastritis, and metaplasia, conditions predominantly caused by H. pylori infection (32, 33).

In current practice, when there is a clear indication for digestive endoscopy, the rapid urease test is the first-line diagnostic tool. To enhance the sensitivity of rapid urease tests, it is recommended to obtain at least two biopsy specimens from the stomach body and antrum during gastroscopy (26).

H. pylori is associated with various extra-digestive manifestations, including cardiovascular disease, hematological diseases, metabolic syndrome, and neurodegenerative diseases (34, 35). Although previous studies have reported on the extraintestinal manifestations of the disease, including alterations in lipid profiles, further investigation into the histopathological features of gastritis associated with dyslipidemia is warranted.

Our focus on the altered lipid profile stems from its crucial role in cardiovascular disease. The association between H. pylori and cardiovascular disease has been a subject of debate in several studies (36, 37). Our study concluded that patients with H. pylori exhibit an altered lipid profile compared to patients without H. pylori. Elevated total cholesterol values were observed in 43.8% of patients, 98% of whom tested positive for H. pylori. HDL cholesterol fell below the normal limit in 45.4% of cases, all of which were H. pylori-positive patients. Additionally, LDL and triglyceride levels exceeding the normal range were associated with H. pylori infection in 95% and 81% of cases, respectively. This observation may be attributed to the age of the studied population, mostly over 50 years old, which could be an independent risk factor for dyslipidemia (38). Our findings align with a recent study from Ethiopia, which reported that two-thirds of H. pylori seropositive patients presented dyslipidemia (39).

Histopathologically, our results showed that the most common cells found in dyslipidemic H. pylori-positive patients were mononuclear cells and neutrophil cells, consistent with acute and chronic inflammation caused by H. pylori in the gastric mucosa. Literature evidence suggests that chronic infection by gram-negative bacteria and the consequent secretion of inflammatory cytokines are linked to changes in lipid profiles (19, 40). These investigations indicate that H. pylori infection may contribute to alterations in lipid profiles through a systemic inflammatory response. The chronic inflammatory response associated with precancerous lesions, such as glandular atrophy and intestinal metaplasia has been extensively studied (41), indicating a probability of regression or persistence without progression in patients who undergo screening for gastric cancer. However, a recent study concluded that patients with intestinal metaplasia of the lesser curvature had a higher risk of developing gastric cancer even after eradication and need closer surveillance (42).

It is important to note that the infection induces an inflammatory response not only in the gastric mucosa but also in other organs (43). Further studies are warranted to assess the histopathological features after eradication and the evolution of lipid profiles in patients. A recent meta-analysis reported that H. pylori eradication did not alter lipid levels (44). However, the effect of H. pylori eradication on lipid levels remains unclear (45) although there is general consensus that abnormal lipid metabolism contributes to the development of cardiovascular diseases.

Given the positive association between H. pylori and cardiovascular disease (2, 3), understanding the relationship between H. pylori eradication and HDL-C (a protective factor for cardiovascular disease) among the evaluated lipids is of interest. Exploring overall changes in lipids following H. pylori eradication may also shed light on the connection between bacteria and lipid metabolism.

Our study has several limitations. First, the number of enrolled patients was small. It was challenging to recruit patients meeting all the inclusion criteria. Additionally, patient selection could be considered biased, as only symptomatic patients referred for gastroscopy were enrolled, rather than routine-examination patients. The diagnostic method for H. pylori is another limitation, as all patients were diagnosed using the RUT test. A more accurate approach might consider the specificities of additional diagnostic methods, such as stool antigen and serology.

Conclusion

In the realm of H. pylori exploration, our small-scale study serves as a fascinating window into uncharted territories. Delving into the intricate world of infection and histopathological intricacies, we uncovered an important connection. Mononuclear cells and metaplasia emerged as key players, correlating with an altered lipid profile in H. pylori-positive patients.

Consider our findings as an intriguing prologue, teasing the possibilities that lie ahead. In the future, it is important to unravel gastric biopsy evolution and lipid profile transformations pre and post-eradication.

Footnotes

  • Authors’ Contributions

    Conceptualization, I.A.C. and C.D.; methodology, S.C.; software, T.C.G.; validation, S.C.; formal analysis, O.P.; investigation, A.P.; resources, I.A.C.; data curation, C.D.; writing—original draft preparation, I.A.C.; writing—review and editing, C.D.; visualization, T.C.G.; supervision, S.C.; project administration, I.A.C.; funding acquisition, C.D. All Authors have read and agreed to the published version of the manuscript.

  • Funding

    The University of Oradea, Oradea, Romania funded this study.

  • Conflicts of Interest

    The Authors declare no conflicts of interest in relation to this study.

  • Received December 20, 2023.
  • Revision received February 4, 2024.
  • Accepted February 5, 2024.

This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY-NC-ND) 4.0 international license (https://creativecommons.org/licenses/by-nc-nd/4.0).

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Histopathology Features of H. pylori Gastritis Associated With Altered Lipid Profile: An Observational Study from a Tertiary Healthcare Center in North West Romania
IOANA ALEXANDRA CARDOS, CATALINA DANILA, TIMEA CLAUDIA GHITEA, OVIDIU POP, ANDREI PASCALAU, SIMONA CAVALU
In Vivo May 2024, 38 (3) 1421-1428; DOI: 10.21873/invivo.13584
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