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Arquivos de Gastroenterologia

Print version ISSN 0004-2803On-line version ISSN 1678-4219

Arq. Gastroenterol. vol.54 no.3 São Paulo July/Sept. 2017  Epub July 13, 2017 

Original Articles

Correlation between virulence markers of Helicobacter pylori in the oral cavity and gastric biopsies

Correlação entre marcadores de virulência de Helicobacter pylori na cavidade oral e em biópsias gástricas

Myriam Lucrecia MEDINA 1  

Marcelo Gabriel MEDINA 2  

Luis Antonio MERINO 3  

1Unidad de Investigación, Hospital Pediátrico Dr. Avelino Castelán, Resistencia, Argentina

2Area de Medicina Tropical, Instituto de Medicina Regional, Universidad Nacional del Nordeste, Resistencia, Argentina

3Area de Bacteriología, Instituto de Medicina Regional, Universidad Nacional del Nordeste, Resistencia, Argentina



The clinical outcome of Helicobacter pylori infection has been associated with virulence factors. The presence of these factors is useful as molecular markers in the identification of the high risk for developing severe gastric pathologies.


To correlate the presence of virulence markers cagA and bab2A of H. pylori in oral and gastric biopsy samples.


An observational, prospective, descriptive, and cross-sectional study was carried out between September 2011 and September 2012. Patients suffering dyspepsia with indication for upper gastrointestinal video endoscopy who attended the Gastroenterology Service of the Hospital Dr. Julio C. Perrando were included. Epidemiological investigation was completed. To detect the bacteria and their virulence genes, samples of saliva, dental plaque and gastric biopsy were taken and processed by PCR.


Sixty-one patients were selected for this study (30 women and 31 men). H. pylori was detected in 31 gastric biopsies and 31 oral samples. Significant difference between oral and gastric samples was found in cagA genotype. Agreement between oral and gastric genotypes was found in 38.7% of samples from the same patient.


This study is the first in provide information about the genotypes of the Argentinean Northeast H. pylori strains. Despite the high prevalence of H. pylori infection, the most of patients had less virulent genotypes in oral cavity and gastric tissue. The cagA / babA2 combination was not frequent in the samples studied. There was not a statistical correlation between the virulence genes and gastroduodenal or oral diseases. Although in some patients the same genotype was found both in oral and gastric samples, it cannot be ensure that they corresponding to the same strain because a DNA sequencing was not performed.

HEADINGS: Helicobacter pylori, genetics; Helicobacter infections, diagnosis; Gastric mucosa, microbiology; Saliva, microbiology



O resultado clínico da infecção por Helicobacter pylori tem sido associado com fatores de virulência. A presença desses fatores como marcadores moleculares é útil na identificação do risco elevado para o desenvolvimento de graves patologias gástricas.


Correlacionar a presença de marcadores de virulência cagA e bab2A do H. pylori em amostras de biópsias gástricas e orais.


Um estudo observacional, prospectivo, descritivo e transversal foi realizado entre setembro de 2011 e setembro de 2012. Foram incluídos pacientes com sintomas de dispepsia com indicação de endoscopia gastrointestinal que compareceram ao Serviço de Gastroenterologia do Hospital Dr. Julio C. Perrando . Investigação epidemiológica foi concluída. Para detectar a bactéria e seus genes de virulência, amostras de saliva, placa dentária e biópsia gástrica foram tomadas e processadas pelo PCR.


Sessenta e um pacientes foram selecionados para este estudo (30 mulheres e 31 homens). H. pylori foi detectado em 31 biópsias gástricas e 31 amostras orais. Foi encontrada diferença significativa entre as amostras orais e gástricas no genótipo cagA . A ocorrência simultânea entre genótipos orais e gástricos do mesmo paciente foi encontrada em 38,7% das amostras.


Este é o primeiro estudo a fornecer informações sobre os genótipos das cepas do H. pylori no Nordeste Argentino. Apesar da alta prevalência da infecção pelo H. pylori , a maioria dos pacientes tinha genótipos menos virulentos na cavidade oral e tecido gástrico. A combinação cagA / babA2 não foi frequente nas amostras estudadas. Não houve correlação estatística entre os genes de virulência e doenças gastroduodenais ou orais. Embora em alguns pacientes o mesmo genótipo tenha sido encontrado tanto nas amostras orais quanto gástricas, não se pode garantir que correspondam à mesma variação, pois um sequenciamento de DNA não foi realizado.

DESCRITORES: Helicobacter pylori, genética; Infecções por Helicobacter, diagnóstico; Mucosa gástrica, microbiologia;; Saliva, microbiologia


At least half the world’s population is infected by Helicobacter pylori , making it the most widespread infection in the world. Actual infection rates vary from nation to nation, the people in under developed countries has much higher infection rates than the developed countries 20 .

The clinical course of H. pylori infection is highly variable depending on bacterial and host (genetic and immune) factors 9 .

It has been established that some genes differentially expressed between strains could be used as virulence markers in H. pylori7 .

All identified H. pylori strains possess the vacA gene which codifies for the VacA toxin; this toxin has a vast array of functions that span induction of apoptosis to modulation of the immune system 13,26 .

Additionally, disruption of epithelial cell polarity by CagA protein, codified by the cagA gene, is thought to be an indispensable role in the development of gastric carcinoma 23 and the strains cagA+ are more associated with severe inflammation that those cagA - strains 15 .

The first identified and probably the best characterized adhesin of H. pylori is a 78 KDa protein termed BabA (blood group antigen binding adhesion) 14 . Carriage of the babA2 + strains was associated with more intense chronic inflammation, and presence of glandular gastric atrophy and intestinal metaplasia in the gastric antrum 40 .

The presence of H. pylori in the oral cavity of patients suffering digestive pathologies has been published and it is more frequent in those patients harboring a periodontal disease 19,35 .

Some authors indicate that gastric reflux is not the only route by which H. pylori reaches the mouth and its detection and the genotyping in mouth and in stomach are complementary tests to understand some epidemiological issues 21 .

Therefore, any information about cagA and babA2 genotypes prevalence among different H. pylori -infected clinical groups in the country can help public health authorities to plan preventive policies to reduce the prevalence of diseases associated with H. pylori infection 32 .

The aim of this work was to detect and correlate the virulence markers cagA and babaA2 of H. pylori in gastric biopsies and oral cavity samples.


An observational, descriptive, prospective, and cross-sectional study was carried out between September 2010 and September 2012. Patients with dyspeptic symptomatology and indication for upper gastrointestinal video endoscopy (UGVE) were studied.

We included all patients of both sexes, aged between 18 and 80 years attended to the Service of Gastroenterology of the Hospital Dr. Julio C. Perrando in Resistencia, Argentina.

Patients that denied participating, with a history of gastric endoscopy, who had received antibiotics, proton pump inhibitors, histamine receptors antagonists or bismuth compounds in the last four weeks, were excluded.

The selection of patients was non-probabilistic and intentional type. The size of sample was defined on base to the total number of patients annually attending to the Service of Gastroenterology and the prevalence of H. pylori in patients suffering dyspepsia according data from literature.

The institutional Bioethical Committee approved all procedures and those patients that accepted to participate provided a written informed consent prior to sampling. Demographic, epidemiological, and clinical data were recorded.

Without oral hygiene, dental plaque and saliva, were sampled. All samples were stored at -20ºC until their further processing by molecular methods.

After oral clinical examination and collection of the oral samples, the patients were subjected to UGVE examination. UGVE has carried out using an endoscope OlimpusRCV-100 GIF-130. Two gastric samples were taken at 2 or 3 cm from the pylorus and were stored at -20ºC to further processing.

DNA was isolated from all samples using the CTAB method and was immediately subjected to conventional PCR.

Purified DNA was carried out for detection of H. pylori by conventional PCR using primers derived from the ureA gene 18).

In the samples positives for H. pylori , the virulence markers were studied, amplifying the cagA and babA2 genes according to the protocols previously published 8).

In all protocols, positive and negative controls supplied by a colleague from the University of Concepción (Chile) were included.


During the period of study, 61 dyspeptic patients with digestive diseases and indication for UGVE were selected, 30 females and 31 males. Patients ranged in age from 18 to 69 years (Average 45 years).

H. pylori was detected in 31/61 gastric samples and in 31/61 oral samples ( Figure 1 ), indicating a prevalence of 50.8% in both body sites.

FIGURE 1 Agarose gel electrophoresis of H. pylori detection in gastric samples. Lines 2 to 5: positive samples. The molecular weight of the amplicon corresponding to the ureA gene is 411 bp. Line 8: 100 bp weight marker. 

Due to insufficient quantity or bad quality of DNA obtained, genotyping was performed in 31 positive gastric samples but only in 16 dental plaques and 1 saliva sample ( Figure 2 ).

FIGURE 2 Agarose gel electrophoresis of H. pylori genotyping products in gastric samples.a The molecular weights of the different amplicons are: cagA 400 bp, vacA 259 and babA2 831 bp. Line 7: 100 bp weight marker. 

Table 1 shows the correlation between different genotypes of H. pylori in the studied samples. As it was expected, the vacA gene was detected in 100% of oral and gastric samples. The cagA + was significantly more frequent in gastric biopsies tan in oral cavity.

TABLE 1 Distribution of genotypes among different samples 

Genotypes Biopsies (n=31) Oral (n=17)
vacA 31 (100%) 17 (100%)
cagA 22 (71%) 5 (29%)
babA2 3 (9.7%) 3 (17.6%)

In 12/31 (38.7%) patients concordance between the genotypes found in their oral and gastric samples was found.

Table 2 and Table 3 show the distribution of genotypes according the different oral and gastroduodenal diseases. No significant differences were found among pathological groups regarding the genotypes studied ( P value >0.05).

TABLE 2 Relationship between genotypes and digestive diseases 

Genotypes Gastroduodenal diseases
ACG ACGFM CGND Total P value
n=18 n=8 n=5 n=31
vacA 18 8 5 31
cagA 13 4 5 22 0.25
babA2 2 0 1 3 0.60

ACG: H. pylori associated active chronic gastritis; ACGFM: H. pylori associated active chronic gastritis with focus of metaplasia; CGND: chronic gastritis with non-specific duodenitis.

TABLE 3 Relationship between genotypes and oral status 

Genotypes Oral status
Gingivitis Periodontitis Normal Total P value
n=10 n=5 n=2 n=17
vacA 10 5 2 17 -
cagA 2 0 2 5 0.25
babA2 0 2 1 3 0.60


It has become increasingly clear that populations in humans are highly diverse and this heterogeneity can be analyzed at two different levels: genotypic variation among strains and variations in H. pylori populations within an individual host 5 .

The presence of multiple organisms within a host may occur as a result of recombination events leading to genetic shift, whereas ongoing mutation within a strain can lead to the formation of quasispecies by genetic drift 5 .

In the oral cavity there exists a live H. pylori that has negative influences on the eradication of stomach infection and as long as physicians agree with the idea of a second colonized site within the oral cavity, the rate for successful eradication of H. pylori will increase 39 .

From 1989 to date, many researchers worldwide have identified H. pylori in plaque and saliva with varying results 1 .

H. pylori was found in saliva of 33 (42.3%) patients and in dental plaque samples of 37 (47.4%) patients 38 . In dental plaque 60% of the patients with chronic periodontitis were found to be positive for H. pylori2 . In the present work, H. pylori was detected in 50.8% of oral samples.

The H. pylori DNA was found with variable frequencies in gastric samples from patients suffering gastroduodenal disorders, ranging from 48 to 63% 17,25,27 .

The percentages of positivity for H. pylori in gastric samples were lower than previously found in symptomatic patients in Argentina. Medina et al. reported 88.3% of positivity in gastric samples in patients suffering digestive pathologies 19 , meanwhile Jimenez et al. published 91% of H. pylori - positive gastric samples 11 .

Not always H. pylori is found simultaneously in oral cavity and in gastric samples. Román-Román et al. found H. pylori DNA in saliva and in biopsy in 24% of patients,52.5% were saliva negative/biopsy positive and 6.6% were saliva positive/biopsy negative 31 .

Berroteran et al. investigated H. pylori presence in dental plaque from dyspeptic patients 4 . They found that 75% of patients presented H. pylori -positive gastric pathology, and 38% presented H. pylori in the dental plaque, assuming this organism in the dental plaque could be a risk factor for gastrointestinal reinfection.

As published for Trevizani Rasmussen et al., of the 66 patients who were H. pylori positive in their gastric biopsies, 19 (28.8%) were found not to have H. pylori in the oral cavity. In other hand, of the 12 patients whose gastric biopsies were negative for H. pylori , six (50%) were found not to have H. pylori in the oral cavity 38 .

In gastric biopsies, it was found a higher prevalence than reported by other authors.

The prevalence of cagA gene was 48.7% among the positive samples and was not significantly associated with the gastroduodenal diseases 17 . Among patients with chronic gastritis, 39.2% were cagA + 27 . The cagA gene was detected in 42 (56.0%) strains in Cuban patients with upper gastrointestinal diseases 10 .

In one study the prevalence of cagA gene was 48.7%, lower than other reports in African countries 17 and was present in 73.3% of isolates 6 .

In patient positives for H. pylori in gastric biopsies, the cagA gene was detected in 43.3% of gastric biopsies, in 43.8% of saliva samples, and in 27.3% of dental plaque samples, noting that dental plaque and saliva can serve as temporary storage for the cagA variant H. pylori in individuals with gastric disease 34 . In other study, the cagA gene was present in gastric biopsies from 84% of patients with gastroduodenal disorders 25 .

In saliva samples and in dental plaque the prevalence of cagA gene found in the present work was like that reported previously. The cagA gene was found in 27 (45%) of the 60 samples of H. pylori -positive saliva samples 28 . In a previous study, 14 from 18 patients harbored the cagA+ genotype of H. pylori , but only 9 of them presented this genotype in stomach 33 . These studies suggest that the genotyping must be performed simultaneously in oral cavity and in stomach.

Some authors, in agreement with the findings here presented, reported about a low correlation between the gastric infection and the presence of cagA + genotype in oral cavity 31 .

Although there are several genes associated with adhesion of the bacteria, the babA2 gene is associated with successful colonization 21 .

In the present work, the babA2 + genotype was the less frequent, in agreement with previous reports. In patients with chronic gastritis 12 . Nevertheless, a recent study reported that babA2 prevalence was significantly higher in gastric biopsies obtained from chronic gastritis patients (95%) when compared with duodenal ulcer patients (18.1%) and non-ulcer dyspepsia subjects (26.1%) 30 .

Arévalo et al. found that 57% of the gastric isolates were babA2 + 3 , which coincides with other South American studies that reported gene frequencies ranging from 40.4% to 82.3% in stomach samples 16,27,29,37 .

When babA2 and cagA are coexpressed in the same H. pylori strain, they work synergistically in worsening inflammation and may be a potential risk of intestinal metaplasia 30 .

Taking into account the genes association, it was found the cagA +/ babA2 + combination in 9.7% of gastric biopsies and in 17.6% of oral samples. Similarly, this association was observed in 13.3% of gastric samples from patients suffering chronic gastritis as reported by Paniagua et al. 27 . Regarding the coincidence between the same genotype in oral cavity and gastric mucosa, the genotypes found in saliva and biopsy of the same patient had 51.1% agreement 31 . Other studies show that people can be infected simultaneously by two or more genotypes of H. pylori22 , due to coinfection or genetic variation 24 . In the present work the same genotypes were found simultaneously in oral and gastric samples from the same patient in 38.7% of them. However, complete genomes of the detected strains should be sequenced, since this is the only way to demonstrate genetic identity.

Nevertheless, as published previously, we did not find a statistical correlation between the virulence genes and the gastroduodenal or oral diseases 17,36 . That could be due to the small number of patients with H. pylori harboring each virulence marker.

Additionally, further studies may be performed to correlate different digestive disorders with the presence of various virulence factors, including the iceA protein and the different alleles of vacA gen 10 .


This study is the first in provide information about the genotypes of the Argentinean Northeast H. pylori strains. Despite the high prevalence of H. pylori infection, the most of patients had less virulent genotypes in oral cavity and gastric tissue. The cagA / babA2 combination was not frequent in the samples studied. There was not a statistical correlation between the virulence genes and gastroduodenal or oral diseases.

Although in some patients the same genotype was found both in oral and gastric samples, it cannot be ensure that they corresponding to the same strain because a DNA sequencing was not performed.


To Dr. Apolinaria García Cancino (University of Concepción, Chile) for suppling the control strains and to the Staff of the Histocompatibility and Genetic Laboratory of the Hospital “Dr. Julio C. Perrando” (Resistencia, Argentina) for helping in genes detection.


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Disclosure of funding: The present work had the financial support of the “Alberto J. Roemmers” Foundation and the National Agency for Scientific and Technological Promotion (Ministry of Science, Technology and Productive Innovation, Argentina) through the grant PICTO-UNNE 2010.

Received: November 13, 2016; Accepted: March 27, 2017

Correspondence: Luis A. Merino. Chaco, 1163, 6°B - Corrientes, Argentina. E-mail:

Declared conflict of interest of all authors: none

Authors’ contributions: Medina ML: samples and data collection, survey execution, revision of text. Medina MG: survey execution, statistical analysis, revision of text. Merino LA: samples processing, survey execution, writing of text.

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