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Article

Prevalence and Diagnostic Comparison of Helicobacter pylori and Non-Helicobacter pylori Helicobacter Infections in Patients Undergoing Upper Gastrointestinal Endoscopy with Gastric Biopsy in Algarve, Portugal

by
Francisco Cortez Nunes
1,
Teresa Letra Mateus
2,3,4,*,
Catarina Aguieiras
5,
Ricardo Louro
6,
Bruno Peixe
5,6,
Mauro Calhindro
7,
Patrícia Queirós
1,6,8,† and
Pedro Castelo-Branco
1,9,†
1
Faculty of Medicine and Biomedical Sciences, University of Algarve, 8005-139 Faro, Portugal
2
CISAS—Center for Research and Development in Agrifood Systems and Sustainability, Escola Superior Agrária, Instituto Politécnico de Viana do Castelo, 4900-367 Viana do Castelo, Portugal
3
EpiUnit ITR, Instituto de Saúde Pública, Universidade do Porto, 4050-091 Porto, Portugal
4
Veterinary and Animal Research Centre (CECAV), Associate Laboratory for Animal and Veterinary Sciences (AL4AnimalS), Universidade de Trás-os-Montes e Alto Douro, 5000-801 Vila Real, Portugal
5
Serviço de Gastroenterologia, Unidade Local de Saúde do Algarve—Hospital de Faro, 8000-386 Faro, Portugal
6
Hospital Particular do Algarve—Unidade de Alvor, 8500-322 Portimão, Portugal
7
Serviço de Medicina Interna, Unidade Local de Saúde do Algarve—Hospital de Portimão, 8500-338 Portimão, Portugal
8
Serviço de Gastroenterologia, Unidade Local de Saúde do Algarve—Hospital de Portimão, 8500-338 Portimão, Portugal
9
Algarve Biomedical Center Research Institute (ABC Ri), University of Algarve, 8005-139 Faro, Portugal
*
Author to whom correspondence should be addressed.
These authors contributed equally to this work.
Microorganisms 2025, 13(7), 1684; https://doi.org/10.3390/microorganisms13071684
Submission received: 25 June 2025 / Revised: 12 July 2025 / Accepted: 15 July 2025 / Published: 17 July 2025
(This article belongs to the Section Public Health Microbiology)

Abstract

H. pylori infects over half of the global population and is associated with various gastric and extra-gastric diseases. Other species, such as zoonotic non-Helicobacter pylori Helicobacters (NHPHs), have shown similar associations with gastritis and MALT lymphoma and H. pylori-negative cases with gastric disease have been identified, including gastric MALT lymphoma, chronic gastritis, and gastroduodenal ulcers. Accurate identification of these species is of great relevance but remains challenging using conventional diagnostic methods. This cross-sectional study aimed to determine the prevalence of H. pylori and NHPH infections, comparing standard histological protocols with molecular techniques. Between December 2024 and February 2025, 54 adult patients undergoing upper gastrointestinal endoscopy (UGE) with gastric biopsy in three hospitals in Algarve, Portugal were recruited. Endoscopic assessment was performed, and gastric biopsies were collected for histological and molecular analysis. DNA was extracted from antral biopsies and analyzed by conventional PCR to detect H. pylori and NHPH. H. pylori diagnostic techniques were compared, descriptive plus statistical analysis was performed, and p-values < 0.05 were considered to be statistically significant. Fifty-four patients were included in the study, with 51.9% of them presenting symptoms. Endoscopic gastritis was observed in 66.7% of patients, while histological gastritis was present in 88.9%, with statistically significant differences between the two diagnostic techniques (p = 0.004). Helicobacter spp. were identified in 44.4% (24/54) of the patients. H. pylori was detected in 42.6% of the patients by Modified Giemsa stain and in 33.3% by PCR. H. bizzozeronii was found in 35.9% of the patients, with 22.2% showing mixed infections. This study reveals a significant prevalence of Helicobacter spp. in patients from the Algarve region, with both H. pylori and zoonotic H. bizzozeronii detected. This is the first report of H. bizzozeronii DNA detection in gastric biopsies via PCR from patients undergoing UGE in Portugal, highlighting the need to consider NHPH in clinical diagnosis. It is important to include molecular methods in routine diagnostics and the need for broader studies to assess regional and national trends in Helicobacter infections besides H. pylori.

1. Introduction

The Helicobacter genus comprises Gram-negative spiral-shaped bacteria, including more than 70 different species that can colonize the gastrointestinal tract of humans and animals and may be associated with both gastric and extra-gastric diseases [1,2,3,4]. H. pylori infects over half the global population, causing gastritis, gastroduodenal ulcers, gastric adenocarcinoma, and mucosa-associated lymphoid tissue (MALT) lymphoma [5,6]. H. pylori is the most well-known and extensively studied species within this genus. Other gastric helicobacters, collectively referred to as non-Helicobacter pylori helicobacters (NHPHs), are also associated with gastrointestinal diseases in humans [3,7,8,9,10] and have gained increasing attention. The most common gastric NHPH in humans are H. bizzozeronii, H. felis, H. suis, H. heilmannii, and H. salomonis, all of which have zoonotic potential [7,11]. NHPH infections in humans are less frequent than H. pylori infections. Among the NHPH species, H. bizzozeronii, H. felis, and H. suis are the most prevalent [7]. Although NHPH infections are often associated with milder forms of gastritis, they have been linked to a higher risk of developing low-grade MALT lymphoma compared to H. pylori [8,11,12,13]. The primary source of NHPH infections in humans is most likely direct or indirect contact with infected animals and consumption of contaminated food or water [14,15]. H. bizzozeronii is considered one of the most frequently detected NHPH species in humans [7,11]. Originally isolated from dogs, H. bizzozeronii can colonize the gastric mucosa and is believed to be transmitted primarily through close contact with pets [2,14]. Studies have demonstrated its ability to adhere to human gastric epithelial cells and elicit an inflammatory response similar to H. pylori, contributing to chronic gastritis and MALT lymphoma development [7,8,12]. Unlike H. pylori, which predominantly affects humans, H. bizzozeronii has a broad host range, increasing the risk of zoonotic transmission [2,3]. Clinical differentiation from H. pylori is difficult due to overlapping symptoms and histological features, emphasizing the need for targeted molecular diagnostics [11,13]. Recent reports suggest that H. bizzozeronii may be underdiagnosed and underreported [9,14].
Several Portuguese studies provide valuable insight into the national epidemiology of Helicobacter spp. Bastos et al., 2013 report a very high prevalence of H. pylori infection in Portuguese adults, reaching 84.2%, with strong associations to low socioeconomic status, advanced age, and low educational level [16]. Morais et al., 2016 observed a declining trend in H. pylori prevalence, particularly among younger age groups, attributing this to improved hygiene, antibiotic use, and healthcare access [17]. In more recent work, Matos et al., 2022 conducted molecular investigations revealing that NHPHs were present in gastric tissue samples from Portuguese patients with a prevalence of 2.5%, as well as emphasized the role of glycan-mediated adhesion mechanisms in colonization of the human gastric mucosa by NHPH, which may contribute to chronic gastritis or even lymphoid tissue activation in H. pylori-negative patients [11,12].
Epidemiological studies have shown that NHPH infections are more common than previously thought, with some reports citing prevalence rates as high as 29.1% in symptomatic patients in Europe, as described by Taillieu et al., 2023 [7].
The accurate diagnosis of Helicobacter infections requires a combination of clinical suspicion and diagnostic tools, as no single method ensures complete sensitivity and specificity [18]. The clinical diagnosis of H. pylori can be conducted using different diagnostic techniques, either noninvasive or invasive [18]. Regarding the most commonly used noninvasive techniques in a clinical setting, the urea breath test (UBT), serological assays, and the stool antigen test can be used, while invasive techniques most commonly used include endoscopy for biopsy-based diagnosis such as histology, culture, and molecular methods and the rapid urease test (RUT) [18]. In patients who undergo upper gastrointestinal endoscopy with gastric biopsy, the diagnosis is routinely based on histological examination often using hematoxylin and eosin or modified Giemsa stain, and immunohistochemical techniques, which are the most widely used invasive methods and serve as the current diagnostic gold standard [19]. However, traditional histological methods may fall short in detecting and distinguishing between H. pylori and NHPH due to morphological similarities and low bacterial load. These result in differences regarding the sensitivity of these diagnostic techniques, and they may not allow the identification of the species [7,11], which can result in false-negative and or false-positive results, mainly when using modified Giemsa stain [20]. Molecular methods such as PCR have become increasingly valuable in detecting Helicobacter spp. DNA and differentiating between species offering enhanced sensitivity and specificity [7,11]. Recent European studies recommend integrating PCR into diagnostic algorithms, particularly when standard stains are inconclusive or when patients are H. pylori-negative despite clinical symptoms [7,11].
From a public health standpoint, understanding the burden of zoonotic Helicobacter infections is crucial, particularly in regions where contact with domestic animals or agricultural practices increases exposure risk [9,14]. There is also growing recognition that NHPH infections may contribute to gastric malignancies, especially in patients who test negative for H. pylori using conventional diagnostic methods but still present with gastric pathology [8,13]. As such, integrating molecular diagnosis into standard clinical workflows could enhance detection, enable better epidemiological surveillance, and allow more tailored therapeutic approaches [7,21].
Therefore, this study aimed to identify, diagnose, and characterize H. pylori and/or NHPH infections to determine the prevalence of H. pylori and NHPH infections and to compare the standard protocol for diagnose of H. pylori in gastric biopsies using histology and modified Giemsa stain with molecular diagnosis, specifically PCR using species-specific primers for the detection of Helicobacter species in patients undergoing upper gastrointestinal endoscopy with gastric biopsy in Algarve, Portugal.

2. Materials and Methods

2.1. Study Design

A cross-sectional study was carried out at the endoscopy units of three hospitals in Algarve, Portugal (Unidade Local de Saúde do Algarve—Hospital de Faro, Hospital de Portimão, and the Hospital Particular do Algarve—Unidade de Alvor) between December 2024 and February 2025. Patients aged 18 years and older who presented with an indication for upper gastrointestinal endoscopy with gastric biopsy were considered for recruitment. To be included in the study, all patients had to sign a consent form and had to be off proton pump inhibitors and antimicrobials for at least 14 days and 30 days before the procedure, respectively. Informed written consent was obtained from all the participants.

2.2. Upper Gastrointestinal Endoscopy and Histological and Molecular Analysis

An upper gastrointestinal endoscopy was performed by a gastroenterologist assisted by a nurse using endoscopes (Olympus® GIF-Q165/185 (Olympus®, Tokyo, Japan), Fujifilm® EG-760R (Fujifilm® (Tokyo, Japan)). During the procedure, pictures were taken of the significant findings. Biopsies were taken from the antrum and corpus for histological analysis and one extra biopsy of the antrum was taken for DNA extraction and molecular analysis.
The collected biopsies followed the standard intrahospital diagnostic procedure for histological analysis and H. pylori diagnosis with standard modified Giemsa stain. The extra biopsies taken for DNA extraction and molecular analysis were labeled and stored at −20 °C until sent to the Institute for Research and Innovation in Health (i3S)—Porto University for processing and molecular diagnostics.
At the Cell Culture and Genotyping Platform of i3S, DNA was extracted from the frozen biopsies using the conventional salting out protocol. All samples were tested for the presence of H. pylori, H. bizzozeronii, H. felis, H. suis, H. heilmannii, and H. salomonis DNA through conventional PCR using species-specific primers and pre-established protocols as previously described in other studies used in human and animal samples (Table S1).
The amplicons of each PCR-positive sample underwent bidirectional sequencing using the Sanger method at the Genomics Core facility of the Institute of Molecular Pathology and Immunology of the University of Porto, Portugal. Sequence editing and multiple alignments were performed with the MegaX Molecular Evolutionary Genetic Analysis version 10.1.8 [22]. The sequences obtained were subject to BLAST analysis using the non-redundant nucleotide database (http://blast.ncbi.nlm.nih.gov/Blast.cgi (accessed on 24 April 2025)) [23,24].

2.3. Data Collection

Each patient was questioned regarding the indication to be admitted for upper gastrointestinal endoscopy and major symptoms at the time of the procedure. For each patient, age, sex, the upper gastrointestinal endoscopy report, and the histology report were consulted, and data were collected regarding endoscopic gastritis classification and diagnosis and histological gastritis classification according to the Updated Sydney System.

2.4. Statistical Analysis

The data were analyzed using IBM SPSS® Statistics v30 (IBM Corp., Armonk, NY, USA). Frequencies and descriptive statistics were calculated. For bivariate analysis, Chi-square was applied to verify the statistical significance between groups of data, and Cramer’s V (cv) was used to measure the strength of association between two categorical variables. The McNemar test was applied to dichotomous categorical data. p-values < 0.05 were considered to be statistically significant.

3. Results

3.1. Patients’ Data

A total of 54 patients were included in this study, with a mean age of 51.8 years; 27 of them were males with a mean age of 55.5 years, and 27 were females with a mean age of 48.1 years, as shown in Table 1. All patients were asked about current symptoms at the time of the upper gastrointestinal endoscopy. Most of the patients (51.9%) were symptomatic and the most frequent symptom was epigastralgia (18.5%) followed by dyspepsia (16.7%) and heartburn (11.1%); the most frequent indication for upper gastrointestinal endoscopy was gastric cancer opportunistic screening (38.9%), dyspepsia (16.7%), and heartburn (14.8%), as shown in Table 1.

3.2. Upper Gastrointestinal Endoscopic Findings

Of the 54 patients who underwent upper gastrointestinal endoscopy, only 18 (33.3%) presented normal gastric mucosa. Of the 36 patients with endoscopic gastritis, atrophy was the most frequent finding in both male and female patients; however, females presented a higher prevalence of erosion (22.2%) and ulceration (11.1%), as shown in Table 2.

3.3. Histology Results

Regarding the histological findings of the analyzed biopsies, there were a total of 48 patients with gastritis. There was a higher prevalence of mild gastritis in both male (74.1%) and female (51.9%) patients, with only one female (3.7%) patient with severe gastritis (shown in Table 3). On histological analysis, there was no dysplasia. Atrophy and intestinal metaplasia ranged from mild to moderate, and activity ranged from mild to severe.
Comparing the endoscopic and histological findings, there were normal endoscopy and histology in 4 patients, endoscopic and histological gastritis in 34 patients, endoscopic gastritis with normal histology in 2 patients, and normal endoscopy with histological gastritis in 14 patients. There was a statistically significant difference (p = 0.004) when comparing the endoscopic (36/54) and the histological (48/54) diagnosis of gastritis, with higher diagnosis of gastritis using histological diagnosis.

3.4. Presence of Helicobacter spp.

Despite the diagnostic technique used, Helicobacter species were identified in 24 of the 54 analyzed samples, and there was a statistically significant mild association between sex and the identification of Helicobacter species (as shown in Table 4).
Regarding the presence of H. pylori using modified Giemsa stain, there was a total of 23 positive samples, with a statistically significant moderate association between female sex and the identification of the presence of H. pylori using modified Giemsa stain (p = 0.013, cv = 0.337) (as shown in Table 4).
Considering the presence of Helicobacter species through PCR analysis, 20/54 (37.0%) patients were PCR-positive for Helicobacter spp. DNA, 18/54 (33.3%) patients were PCR-positive for H. pylori DNA, and 14/54 (35.9%) were PCR-positive for H. bizzozeronii DNA, as shown in Table 4. Mixed infections with PCR-positive H. pylori DNA plus H. bizzozeronii DNA were detected in 12/54 (22.2%) patients, 6/54 (11.1%) were PCR-positive just for H. pylori DNA, and 2/54 (3.7%) of the patients were PCR-positive only for H. bizzozeronii DNA. No amplification of DNA was achieved for the remaining NHPH-tested species, as presented in Table 4.
Regarding the endoscopic findings, histological findings, and the presence of Helicobacter spp. (Table 5), there was a statistically significant association between them, as presented in Table 6.

4. Discussion

It is known that Helicobacter spp. may be associated with gastric disease in humans, and it is well-known that H. pylori is associated with gastritis, gastroduodenal ulcers, gastric adenocarcinoma, and MALT lymphoma [6].
At the time of the upper gastrointestinal endoscopy, 51.9% of the patients were symptomatic, with the most frequent symptom being epigastralgia (18.5%), followed by dyspepsia (16.7%) and heartburn (11.1%). Our results showed that 66.7% (36/54) of the patients had endoscopic gastritis; however, 88.9% (48/54) had histological gastritis with a statistically significant difference between these two methods (p = 0.004), as shown in Table 2 and Table 3, suggesting that endoscopic and histological results are not equivalent. These results corroborate the use of histology as the gold standard method for the diagnosis of antral gastritis, and biopsies should always be performed, regardless of the endoscopic findings, as stated by Bertges et al., 2018 [25].
This study reports a prevalence of Helicobacter spp. infection of 44.4% (24 of 54 patients), a lower prevalence compared with the Portuguese prevalence of 84.2% to 90% reported by Bastos et al., 2013 and Morais et al., 2016 [16,17]; however, it is similar to the worldwide studies’ prevalence of 43.1–44.3% [26,27]. The discrepancy with older Portuguese data could reflect improved hygiene, antibiotic usage, and public health measures or may results from sample size limitation since our study reports regional prevalence with a small study population.
Interestingly, the prevalence had a statistically significant moderate association with sex (p = 0.028, cv = 0.298), with females presenting a prevalence of Helicobacter infections of 59.3% compared to 29.6% in male patients. Although the mechanism underlying sex differences in infection prevalence are unclear, previous studies suggest that horminal, immunological and behavioral factors may contribute [27,28,29,30]. No direct comparison can be made, since our study refers to prevalence of H. pylori and H. bizzozeronii; however, there are some studies referring to prevalences of H. pylori infection ranging from 29.2 to 42.7% in females and 36.6–46.3% in males [27,28,29,30], although these studies included a higher number of male than female participants. Further studies must be conducted to determine how sex influences the acquisition of Helicobacter spp. infections.
Regarding the presence of NHPH, only DNA of the zoonotic H. bizzozeronii was detected, with a prevalence of 25.9% (14/54). The prevalence was also higher in females (37.0%, 10/27) than in males (14.8%, 4/27). To the best of the authors’ knowledge, this finding is significant as it represents the first report of H. bizzozeronii DNA detection in gastric biopsies from patients undergoing upper gastrointestinal endoscopy in Portugal. The fact that only H. bizzozeronii DNA was detected goes along with previous reports that state that this is one of the most common NHPHs to infect humans [7].
When comparing the diagnostic techniques to diagnose H. pylori infection, namely histology using modified Giemsa (23/54) vs. PCR (18/54), there was a statistically significant strong association between the two techniques (p < 0.001, cv = 0.741). These findings are consistent with the literature, suggesting that while modified Giemsa is a reliable method, it lacks the species-level specificity and sensitivity of molecular methods, particularly in the context of NHPH detection [30,31]. Moalla et al., 2024 report 81.5% sensitivity and 56.3% specificity of the modified Giemsa stain; however, Matos et al., 2022 and Taillieu et al., 2023 explain that despite gastric bacterial load, PCR is more sensitive and more specific since it allows for species differentiation. Despite these reports suggesting differences in histology diagnosis compared to molecular techniques [7,11,21,31], our study suggests that histology can be considered an efficient test compared to PCR in H. pylori detection, as reported by Moalla et al., 2024 [21]; however, it cannot identify the species and is dependent on the expertise of the pathologist and awareness for morphological differences between H. pylori and NHPHs.
When analyzing the presence of gastritis (48/54) with the presence of Helicobacter spp. (24/54), there were 25 patients with histological gastritis who were negative for Helicobacter, 23 patients with histological gastritis who were positive for Helicobacter, and only one patient who was negative for histological gastritis and PCR-positive for Helicobacter. Nonetheless, no statistically significant association was found between these two variables (p = 0.146). This may suggest that gastritis can have multifactorial etiologies and may occur independently of detectable Helicobacter infections. Yet, there was a statistically significant moderate association between the presence of Helicobacter spp. and ulceration on endoscopy (p = 0.042, cv= 0.280) and a statistically significant strong association between the presence of Helicobacter spp. and the severity of gastritis according to the Updated Sydney System Classification (p < 0.001, cv = 0.582), as shown in Table 5, as previous reports suggest [32,33].

5. Conclusions

This was the first study, at the national level, to compare the standard diagnostic protocol for H. pylori with molecular diagnostics, as well as the first to detect H. bizzozeronii DNA in gastric samples of patients undergoing UGE with gastric biopsy. The study concludes that NHPHs, in this case, H. bizzozeronii, are often associated with gastritis along with H. pylori, underlining the clinical importance of considering NHPHs in routine diagnostic workflows and contributing to the emerging epidemiological picture of zoonotic Helicobacter infections in Southern Portugal. These findings support the inclusion of PCR-based methods into standard diagnostic algorithms to enhance sensitivity and allow for species-level identification, which is crucial for appropriate clinical management. Ideally, this study should be replicated with a larger number of participants and in other regions of Portugal to determine whether regional differences exist in the prevalence of H. pylori and NHPH infections. Moreover, longitudinal studies could provide insight into the chronic outcomes of NHPH infections and their role in gastric disease.

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/microorganisms13071684/s1. Table S1: Primer sequences and thermocycling conditions for H. pylori and NHPH.

Author Contributions

Conceptualization: F.C.N.; methodology: F.C.N.; formal analysis: F.C.N.; investigation: F.C.N., T.L.M., C.A., P.Q., B.P. and R.L.; resources: F.C.N. and T.L.M.; data curation: F.C.N., M.C. and T.L.M.; writing—original draft preparation: F.C.N.; writing—review and editing: F.C.N., T.L.M., M.C., C.A., P.Q. and P.C.-B.; supervision: P.Q. and P.C.-B. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by national funds through FCT—Fundação para a Ciência e a Tecnologia, I.P., within the scope of project UIDB/05937/2020 with DOI identifier 10.54499/UIDB/05937/2020 and UIDP/05937/2020 with DOI identifier 10.54499/UIDP/05937/2020.

Institutional Review Board Statement

The study was conducted in accordance with the Declaration of Helsinki and approved by the Ethics Committee for Health—ULS Algarve (approval number 292/24; approval date 19 December 2024) and the Ethics Committee for Health—Hospital Particular do Algarve (approval number 13/2024; approval date 18 November 2024).

Informed Consent Statement

Informed consent was obtained from all subjects involved in the study.

Data Availability Statement

The original contributions presented in this study are included in the article/Supplementary Materials. Further inquiries can be directed to the corresponding author.

Acknowledgments

The authors would like to acknowledge Paula Magalhães, Cell Culture and Genotyping Platform of i3S-UP, as well as Freddy Haesebrouck and Frank Pasmans from Ghent University, for kindly providing the Helicobacter species positive controls to be used in this study.

Conflicts of Interest

The authors declare no conflicts of interest.

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Table 1. Clinical characteristics of patients per sex.
Table 1. Clinical characteristics of patients per sex.
TotalMaleFemale
N5427 (50%)27 (50%)
n (%)n (%)n (%)
Age
Mean (± SD)51.81 (±15.80)55.52 (±13.75)48.11 (±17.08)
Median [IQR]51.00 [25.75]57.00 [18.00]48.00 [28.00]
Indication for UGE
Gastric cancer opportunistic screening21 (38.9%)12 (44.4%)9 (33.3%)
Dyspepsia9 (16.7%)3 (11.1%)6 (22.2%)
Heartburn8 (14.8%)2 (7.4%)6 (22.2%)
Pre surgical assessment7 (13.0%)3 (11.1%)4 (14.8%)
Epigastralgia6 (11.1%)4 (14.8%)2 (7.4%)
Nausea1 (1.9%)1 (3.7%)0 (0.0%)
Dysphagia1 (1.9%)1 (3.7%)0 (0.0%)
Diarrhea1 (1.9%)1 (3.7%)0 (0.0%)
Symptomatic28 (51.9%)11 (40.7%)17 (63.0%)
Symptoms
Epigastralgia10 (18.5%)4 (14.8%)6 (22.2%)
Dyspepsia9 (16.7%)3 (11.1%)6 (22.2%)
Heartburn6 (11.1%)1 (3.7%)5 (18.5%)
Nausea1 (1.9%)1 (3.7%)0 (0.0%)
Dysphagia1 (1.9%)1 (3.7%)0 (0.0%)
Bloating1 (1.9%)1 (3.7%)0 (0.0%)
Endoscopic gastritis36 (66.7%)18 (66.7%)18 (66.7%)
Histological gastritis48 (88.9%)24 (88.9%)24 (88.9%)
Helicobacter-positive24 (44.4%)8 (29.6%)16 (59.3%)
H. pylori-positive on Modified Giemsa stain23 (42.6%)7 (25.9%)16 (59.3%)
H. pylori
PCR-positive
18 (33.3%)7 (25.9%)11 (40.7%)
NHPH
PCR-positive
14 (25.9%)4 (14.8%)10 (37.0%)
Table 2. Endoscopic findings per sex.
Table 2. Endoscopic findings per sex.
TotalMaleFemale
N542727
n (%)n (%)n (%)
Endoscopic findings
Gastritis36 (66.7%)18 (66.7%)18 (66.7%)
Atrophy10 (18.5%)5 (18.5%)5 (18.5%)
Erosion9 (16.7%)3 (11.1%)6 (22.2%)
Ulceration3 (5.6%)0 (0.0%)3 (11.1%)
Marble appearance3 (5.6%)2 (7.4%)1 (3.7%)
Table 3. Histological findings per sex.
Table 3. Histological findings per sex.
TotalMaleFemale
N542727
n (%)n (%)n (%)
Histological gastritis48 (88.9%)24 (88.9%)24 (88.9%)
Updated Sydney System Classification and grading of gastritis
Absent6 (11.1%)3 (11.1%)3 (11.1%)
Mild34 (63.0%)20 (74.1%)14 (51.9%)
Moderate13 (24.1%)4 (14.8%)9 (33.3%)
Severe1 (1.9%)0 (0.0%)1 (3.7%)
Helicobacter spp.
Modified Giemsa- or PCR-Positive
24 (44.4%)8 (29.6%)16 (59.3%)
Table 4. Helicobacter spp.-positive samples per sex and diagnostic technique.
Table 4. Helicobacter spp.-positive samples per sex and diagnostic technique.
TotalMaleFemale
N542727
n (%)n (%)n (%)
Helicobacter spp.
Modified Giemsa- and PCR-Positive
24 (44.4%)8 (29.6%)16 (59.3%)p = 0.028
cv = 0.298
H. pylori
Modified Giemsa-Positive
23 (42.6%)7 (25.9%)16 (59.3%)p = 0.013
cv = 0.337
H. pylori
PCR-positive
18 (33.3%)7 (25.9%)11 (40.7%)
NHPH
PCR-positive
14 (25.9%)4 (14.8%)10 (37.0%)
H. bizzozeronii
PCR-positive
14 (25.9%)4 (14.8%)10 (37.0%)
H. felis
PCR-positive
0 (0.0%)0 (0.0%)0 (0.0%)
H. suis
PCR-positive
0 (0.0%)0 (0.0%)0 (0.0%)
H. heilmannii
PCR-positive
0 (0.0%)0 (0.0%)0 (0.0%)
H. salomonis
PCR-positive
0 (0.0%)0 (0.0%)0 (0.0%)
Table 5. Percentage of gastritis and presence of Helicobacter spp. per diagnostic technique.
Table 5. Percentage of gastritis and presence of Helicobacter spp. per diagnostic technique.
GastritisHelicobacter spp.
Endoscopic DiagnosisHistological DiagnosisH. pylori-Positive
Modified Giemsa Stain
H. pylori-Positive
PCR
H. bizzozeronii-Positive
PCR
Nn   (%)n   (%)n   (%)n   (%)n   (%)
Total5448 (88.9%)36 (66.7%)23 (42.6%)18 (33.3%)14 (25.9%)
Table 6. Association between presence of Helicobacter spp. and endoscopic and histological findings.
Table 6. Association between presence of Helicobacter spp. and endoscopic and histological findings.
Ulceration on EndoscopyUpdated Sydney System
Classification and Grading of Gastritis
Helicobacter spp.p = 0.042 cv = 0.280p < 0.001 cv = 0.582
H. bizzozeronii p < 0.001 cv = 0.627
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Cortez Nunes, F.; Mateus, T.L.; Aguieiras, C.; Louro, R.; Peixe, B.; Calhindro, M.; Queirós, P.; Castelo-Branco, P. Prevalence and Diagnostic Comparison of Helicobacter pylori and Non-Helicobacter pylori Helicobacter Infections in Patients Undergoing Upper Gastrointestinal Endoscopy with Gastric Biopsy in Algarve, Portugal. Microorganisms 2025, 13, 1684. https://doi.org/10.3390/microorganisms13071684

AMA Style

Cortez Nunes F, Mateus TL, Aguieiras C, Louro R, Peixe B, Calhindro M, Queirós P, Castelo-Branco P. Prevalence and Diagnostic Comparison of Helicobacter pylori and Non-Helicobacter pylori Helicobacter Infections in Patients Undergoing Upper Gastrointestinal Endoscopy with Gastric Biopsy in Algarve, Portugal. Microorganisms. 2025; 13(7):1684. https://doi.org/10.3390/microorganisms13071684

Chicago/Turabian Style

Cortez Nunes, Francisco, Teresa Letra Mateus, Catarina Aguieiras, Ricardo Louro, Bruno Peixe, Mauro Calhindro, Patrícia Queirós, and Pedro Castelo-Branco. 2025. "Prevalence and Diagnostic Comparison of Helicobacter pylori and Non-Helicobacter pylori Helicobacter Infections in Patients Undergoing Upper Gastrointestinal Endoscopy with Gastric Biopsy in Algarve, Portugal" Microorganisms 13, no. 7: 1684. https://doi.org/10.3390/microorganisms13071684

APA Style

Cortez Nunes, F., Mateus, T. L., Aguieiras, C., Louro, R., Peixe, B., Calhindro, M., Queirós, P., & Castelo-Branco, P. (2025). Prevalence and Diagnostic Comparison of Helicobacter pylori and Non-Helicobacter pylori Helicobacter Infections in Patients Undergoing Upper Gastrointestinal Endoscopy with Gastric Biopsy in Algarve, Portugal. Microorganisms, 13(7), 1684. https://doi.org/10.3390/microorganisms13071684

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