Helicobacter pylori (H. pylori) is a well-recognized pathogen associated primarily with type B gastritis and peptic ulcers (1) usually associated with dyspepsia and disorders of food intake (2, 3). It has been also designated as a type I carcinogen, predisposing to gastric cancer or gastric mucosa associated lymphoid tissue (MALT) lymphoma (4). The occurrence of H. pylori gastric infection is high all over the world and reaches 80% and 40% in developing and developed countries, respectively (5). Despite of numerous investigations, the modes of its transmission in the population remains still unclear. It has been shown that both oral-oral and fecal-oral transmission occurs in humans (6). Humans appear to be the main reservoir of H. pylori in nature. Therefore, the transfer of H. pylori between individuals via infected saliva or contaminated food and eating devices appear to be the major routes of spreading of the bacteria (7, 8). Taking all these into account it could be reasonable to assume that the oral cavity should plays a critical role in the process of H. pylori transmission and infection in humans. However, the exact role of oral cavity in this transmission as well as eating disorders remains under discussion and the subject of controversy.

It is likely that oral cavity may represent an important reservoir of H. pylori infection for gastric infections and contributes to alteration in food intake and its controlling mechanisms originating in the upper gastrointestinal tract (GI) due to the activation of various oral receptors and afferent nerves signaling to the feeding centers in hypothalamus involved in the control of food intake (9).

The contribution of H. pylori in the pathogenesis of periodontal disease, recurrent aphthous stomatitis, glossitis, burning mouth syndrome and mucosa lesions remains unclear. It is, however, possible, that H. pylori is transiently present in oral cavity and leads to a disbalance of the residual flora of oral cavity. Furthermore, there is the possibility that the bacteria is a part of normal oral microenvironment and belongs to a normal bacteria-film that is not pathogenic reservoir of H. pylori for the stomach, remaining in normal immunological balance with the host or even protecting host against dangerous pathogens. In addition, the numbers of H. pylori colonizing the oral cavity could be too small to cause the gastric infection provided that the host immunity remains appropriate. However, when host immunological defense becomes impaired, bacteria’s role as commensal is changed and it becomes pathogen.

The occurrence of oral colonization by H. pylori, its relation to oral health and food intake or dyspeptic symptoms as well as its relationships to gastric H. pylori infection remain unclear. Accordingly, the objectives of the present study were to evaluate the presence of H. pylori in the oral cavity and to investigate its environmental niche. Additionally, we aimed to determine if the presence of H. pylori in oral cavity is reflected in the change of the selected parameters of the immune system including IgG anti-Hp, IgG anti-CagA, anti-VacA in blood and IgA anti-H. pylori in saliva as well as plasma levels of cytokines like TNF-alpha, and IL-8. We also decided to analyze the relationship between the occurrence of H. pylori in the oral cavity and the presence of gingivitis and priodontitis in examined individuals. Eventually, we investigated the prevalence of gastric H. pylori in oral cavity of H. pylori positive and negative patients and the serum levels of ghrelin (major appetite stimulating hormone) and gastrin (the major gastric acid secretagogue) in all these subjects tested with confirmed by 13C-urea breath test (UBT) to detect gastric H. pylori infection of accompanied by dyspeptic symptoms and alterations in feeding behavior.


MATERIAL AND METHODS
Study population

One hundred female subjects aged 20-52 (mean 41 ± 16 were included into a study. Detailed oral clinical examination and collection of saliva (2 ml) and supragingival dental plaque samples, as well as UBT and blood collection were performed. Study was approved by the Institutional Research Ethics Committee of the Jagiellonian University and informed consent was obtained from all individuals before the study. Patients who had taken antisecretory drugs or antibiotics, bismuth salts or antisecretory agents within previous 2 months, were excluded from the study. Oral clinical parameters including probing depth, bleeding on probing and clinical attachment level were collected by the same investigator. Patients presenting 3 probing depth within at least four sites and exhibiting bleeding on probing were diagnozed as gingivitis and the patients presenting 5 probing depth at least four teeth and bleeding were allocated to periodontitis group. The rest of individuals were considered as healthy oral cavity status subjects. The samples of the supragingival plaques were collected with a periodontal curette from two different front teeth, or in the case of tooth loss, from premolars and molars.

Determination of H. pylori status in stomach

The infection of the stomach was estimated using UBT as described before (10). After obtaining 2 baseline breath samples for registering baseline 13CO2 /12CO2 level, gelatin capsule containing 38 mg of 13C-urea was swallowed with 25 ml of water by each subject. Then, breath samples were collected into testing vials after 10 and 20 minutes following 13C-urea administration. Final results of 13CO2/ 12CO2 ratios were measured with the use of isotope ratio mass-spectometry (IRMS, Heliview, Medichems Seoul, Korea) and were expressed as 13CO2 (per mil) values. A change of mean 13CO2 value over baseline (DOB) after urea capsule administration, of more than 2.5 was considered as positive result.

Detection of oral H. pylori

The presence of H. pylori in the oral cavity was determined using microbiological culture. The samples of saliva and supragingival dental plaque were obtained into sterile vials. Aliquots (100 µl) of the samples were cultured on solid selective, enriched medium (H. pylori agar, Becton Dicinson) containing 5% horse blood and incubated microaerophilically at 37°C for 5-7 days. Colonies were confirmed as Helicobacter pylori by Gram staining to show the presence of gram-negative spiral bacteria and by using the tests for bacterial urease, catalase and oxidase. The API-Campy test (BioMerieux) was performed to confirm diagnosis.

Serological tests

Five ml of vein blood was obtained from each subject. The blood was centrifuged for 10 min at 2000g and serum was saved for the further investigation. To measure the level of anti-Hp IgG, we used Captia TM H. pylori IgG (Trinity Biotech) test based on enzyme linked immunosorbent assay. Levels of TNF-alpha, IL-8 were determined using EASIA test (Biosource) based on solid phase enzyme amplified sensitivity immunoassay. We detected the presence of anti-CagA IgG and anti-VacA IgG using MarDx H. pylori Marblot strip System. The level of gastrin and progastrin in serum was studied by specific radioimmunoassay (RIA) described previously. Salivary anti-Hp IgA was determined using ELISA kit (EIAGEN HP, Clone System) as described before (11). Levels of anti-Hp IgA> 1.0 OD were considered positive, based on previous population study (12, 13).

Patients were asked about their appetite behavior and dyspeptic symptoms such as upper abdominal pain and discomfort in the abdomen that are considered as dyspeptic symptoms (14).

Statistical analysis

The data were expressed as means ± standard error of the mean (SEM). Statistical analysis was performed using Student t or Tukey test after analysis of variance. A P value of less than 0.05 was condired statistically significant.


RESULTS
H. pylori in the oral cavity

H. pylori was found in saliva in 54.1 % and in dental pockets in 48.3% examined individuals. Simultaneously IgA anti-H. pylori IgA antibodies were detectable at high levels in saliva of 84.5% indicating significantly higher exposure to H. pylori (Fig. 1).

Fig. 1. The comparison between the presence of H. pylori in saliva and supragingival (sg) plaque with amount of the patients with elevated anti-H. pylori IgA in saliva.

Environmental niche for H. pylori in the oral cavity

We also investigated, the relationships between environmental niches of H. pylori and its presence was detected in the oral cavity, namely supragingival plaques and saliva. H. pylori presence was detected in supragingival plaques in 70% of individuals who showed the H. pylori in saliva, while 69% of saliva of H. pylori negative patients were negative in supragingival plaque too (Table 1). These results indicate that these two environmental niches: saliva and dental plaque are connected and H. pylori does not seem to have a preferential niche for the oral cavity habituation. Moreover, we observed that H. pylori was present in saliva in 63.7% of toothless subjects indicating that the presence of teeth and gingival pockets are not critical for oral H. pylori colonization.

Age and oral H. pylori

As propensity to certain infections may be related to the age of patient, we have analyzed the relationship between the occurrence of H. pylori in the oral cavity in relation to subject’s age. Interestingly, no significant difference in age was found in relation to oral H. pylori occurrence in oral cavity (Fig. 2).

Fig.2. The levels of the cytokines (TNF-alpha and IL8) in the patients with and without presence of H. pylori in saliva (panel A) and with and without presence of this bacteria in supragingival (sg) plaque (panel B). The immunoreactive status ratio (ISR) estimated from the levels of anti-H.pylori IgA, IgA and CagA in saliva and material from supragingival plaque in oral cavity H. pylori positive and negative patients.

Relationship of selected immunological parameters with oral H. pylori

The mean level of TNF-alpha was 27.3±30.7 pg/ml. Anti-Hp IgG and anti-CagA IgG in plasma were elevated in 50.5% and in 20% of subjects, respectively. We compared levels of anti-Hp IgG (plasma), TNF-alpha, IL-8 and presence of anti-CagA, anti-VacA IgG in plasma and anti-Hp IgA in saliva between individuals who showed presence of H. pylori in the oral cavity (namely who were positive in saliva and/or dental plaque) with individuals who were Hp negative in culture from oral cavity (Fig. 3). We did not observe any significant differences in immunological parameters studied between these two groups.

Fig. 3. The mean age of the patients with and without H. pylori (H.p.) in saliva (panel A) and in supragingival plaque (panel B).

Relationships between serum ghrelin and gastrin levels with and without oral and gastric H. pylori

Serum ghrelin and gastrin levels were measured as indices of the association of H. pylori in oral cavity and in the stomach with appetitive behaviour and gastric secretion. The comparison of ghrelin and gastrin levels between H. pylori inoculation of oral cavity or gastric H. pylori infection shows that patients with the presence of H. pylori in the oral cavity but without gastric infection, showed no statistically significant difference in serum hormones as compared to those without gastric H. pylori infection (healthy controls) (Figs 4 and 5).

Fig. 4. Serum ghrelin and gastrin levels in patients with and without the presence of H. pylori (H.p.) in oral cavity in patients without gastric H. pylori infection.

Fig. 5. Serum ghrelin and gastrin levels in patients with and without gastric H. pylori (H.p.) infection but without the presence of the bacteria in oral cavity. Asterisk indicates significant change as compared to the levels recorded in patients without gastric H. pylori infection.

Relationships between oral H. pylori and gastric infection

The presence of H. pylori in oral cavity was detected in 54.1% of examined individuals, whereas the gastric H. pylori infection was found in 51% of these cases. However, the correlation analysis between those two showed that within in the group of patients with positive UBT (gastric infection) - 45.1% did not show the presence of H. pylori in saliva and 43.1% showed no H. pylori in supragingival plaque. In line with these findings patients, who did not have H. pylori gastric infection (UBT negative) 53.2 % showed presence of H. pylori in saliva and 42.9% in supragingival plaque. The overall X2 analysis showed no relationship between oral and gastric H. pylori in studied group (X2= 0.029; p>0.05).

Relationships between oral H. pylori and appetitive behavior and dyspeptic symptoms

Among patients without and with H. pylori colonization of the oral cavity, the appetite disorders and dyspeptic symptoms were similar and averaged about 25% and 36%, respectively. In patients with gastric H. pylori infection the reduction or loss of appetite and dyspeptic symptoms, mostly in the form of upper abdominal pain or discomfort was recorded in 45% and 63%, respectively, and the occurrence of these symptoms were found statistically significant in higher number of patients as when significant higher number of patients compared to those recorded in patients without gastric H. pylori infection, who showed the alterations in appetite in about 30% and 31%, respectively (Fig. 6).

Fig.6. Schematic presentation of H. pylori (H.p.) infection and its effects on serum gastrin and ghrelin release. This infection enhances gastrin release while reduced ghrelin release and results in appetite disorders and dyspeptic symptoms.

DISCUSSION
The results of this study revealed that H. pylori is relatively commonly present in the oral cavity, although the character of this oral colonization remains unclear and its relation to appetite behavior and dyspeptic symptoms is uncertain. Our results indicate that the presence of H. pylori in oral cavity does not seem to be significantly associated with either gastric infections or periodontal health status or to serum levels of ghrelin and gastrin. In addition, the comparisons shows that oral H. pylori does not seem to evoke significant changes in major inflammatory cytokine production or in specific antibodies directed against H. pylori proteins, apart from salivary IgA. Moreover, much higher occurrence of the latter antibodies than the presence of bacteria itself may suggest that H. pylori in the oral cavity is transient, possibly dependent on other regulatory factors.

Numerous conflicting studies regarding oral localization of H. pylori have been reported. Some authors showed that the occurrence of H. pylori is relatively low and equals about 38% (15), while others find it in nearly 90% (16) or even in 100% of subjects (17, 18). The major differences in study populations, sample collection and laboratory procedure for bacteria detection between studies described above make it difficult to compare results obtained in these studies. There are two main methods currently accepted for the H. pylori detection in oral cavity that is culture and PCR (19, 20), but each of them has disadvantages. Culture is not that sensitive as PCR and H. pylori, because a microaerophilic bacteria, may not be able in some cases to survive the sampling process before being transferred into the medium. This could particularly refer to cases in which numbers of colonizing bacteria are low. PCR detection in turn, although highly sensitive, could result in false positive results. More importantly, PCR detects bacteria’s DNA, which is not a viable organism but potentially just a part of dead bacteria genome. Finally, PCR allows to detect very small numbers of bacteria which may have no significant influence on oral cavity and stomach infection. Therefore, while accepting the limitations of culture as a method for H. pylori identification, we assumed that it reflects the presence of clinically relevant inoculation.

The major question which is related to the presence of H. pylori in the oral cavity is whether this is a residual bacteria, composing part of biofilm of the oral cavity, or whether it plays a pathogenic role. Some investigators suggested that H. pylori can contribute to the etiology of recurrent aphthous stomatitis (21). Our study was limited to analyzing the presence of periodontitis and gingivitis and did not find an evidence linking H. pylori to either of these clinical conditions and this is in keeping with Okuda et al. (22) who concluded that H. pylori has only a transient presence in oral cavity.

Fritscher et al. (23) who examined 105 individuals with recurrent aphthous stomatitis did not find significant difference in H. pylori PCR detection between stomatitis and control groups. Some other authors postulated that H. pylori may be important in atrophic glossitis or cancer lesions (22, 24). Despite, H. pylori being found in a few samples, it was only a minority of the examined individuals. These authors concluded that H. pylori does not contribute to lesions, but, conversely, it is mucosal lesion that makes mucosa more prone for H. pylori colonization (22, 24). The role of H. pylori in periodontal diseases and upper gastrointestinal symptoms in gastrin and ghrelin release is still unclear. Some authors show evident association of H. pylori presence in supra- and sub-gingival plaques and periodontal disease (25-27), while others (28, 29), similarly to us, were unable to confirm this relationship (30). Okuda et al. (22) discovered that Porphyromonas gingivalis and Fusobacterium nucleatum, both periodontal disease bacteria, are able to adhere to H. pylori bacteria and to trap them. It is possible, that although H. pylori may not directly contribute to periodontal disease, it may accompany the pathogenic bacteria causing periodontal diseases. This could explain why H. pylori is often detected in periodontal disease patients. Okuda et al. (22) established also that bacteria composing normal biofilm like Streptococcus mutans and Prevotella intermedia, may produce bacteriocin-like inhibitory protein, thus inhibiting growth of H. pylori strains. This fact supports the idea that H. pylori occurs transiently in the oral cavity, because it could be quickly removed by other bacteria within a biofilm (22). Moreover, it is possible, that despite of H. pylori being directly harmless for gingival tissue, may also contribute to periodontal disease indirectly. It has been found H. pylori antibody that is cross-reactive with antibody of Campylobacter rectus. H. pylori stomach infection can create complexes of antigen-antibody, which infiltrate gingival tissue and initiates inflammation. We did not, however, find features of systemic inflammation in relation to the presence of oral H. pylori.

According to our experience, the presence of H. pylori in oral cavity by itself does not induce important appetite alteration or dyspeptic symptoms or significant alterations in serum levels of ghrelin, representing a major, stomach originating hormone responsible for the appetitive behavior or that of gastrin known to act as the major gastric acid secretagogue. It seems reasonable to conclude, therefore, that highly complicated hormonal mechanisms involved in the control of appetitive behavior or gastric acid secretion may not be affected by the merely presence of H. pylori in oral cavity.

Similarly, despite of the claim of some investigators that oral H. pylori is the reservoir for stomach infection or reinfection, we did not find such a relationship in the studied population. Almost the same number individuals with and without H. pylori in oral cavity among those with gastric infection indicates that these bacteria in oral cavity may not represent the sanctuary of this germ for the stomach. This is confirmed by our finding that only about 53% of the patients, with confirmed by UBT gastric H. pylori infection, revealed the presence of bacteria in the oral cavity and these observations are consistent with findings of others (29, 30).

Our results appear to indicate that H. pylori could be as a transient microbe, which comes in oral cavity with food and vanishes after some time depending on some host factors as well as its interactions with the residual microflora of oral biofilm (22). We showed in our study that H. pylori in saliva and dental plaque is present in about 54% and 48%, respectively, while the elevation of IgA anti-Hp in saliva was registered in 84,5% cases. This indicates, that significantly more subjects have had contact with this bacterium in past and have eliminated it without recent antibiotic treatment, as patients who received antibiotics during 2 months prior to the study were excluded. This could also, at least in part, explain the fact of very varying occurrence of oral H. pylori in different studies.

On the other hand, it is possible that bacteria is constantly present in oral cavity in a small numbers, and its detection depends on sensitivity of the used method, reaching sufficient numbers to be detected by microbiological techniques in relation to some changes of oral and general health. Additionally, we did not notice the elevation of the markers of immunology defense like IgG anti-H. pylori, TNF-alpha, IL-8 and presence of IgG anti-CagA, anti-VacA in plasma. It would support the idea that oral bacterium is causing rathed negbligible immune reaction in the host.

In summary; the presence of H. pylori in oral cavity seems to be transient and it remains without causing any marked alterations in appetite and dyspeptic symptoms or hormonal changes that appear to be associated with gastric H. pylori infection. This does not exclude the possibility that the bacteria could still contribute to oral mucosal lesions and periodontal disease. It appears that oral cavity H. pylori in balanced immunological status of the host, may not be sufficient to be a source of infection and reinfection for the stomach. However, in changing environmental conditions, which would promote bacteria’s growth such as immunodeficiency or disturbed oral biofilm balance, like in patients with denture, the number of bacteria can increase and could possibly be sufficient for gastric infection. These problems require further investigation in those groups of patients. It seems obvious, however, that gastric H. pylori infection with chronic active gastritis is accompanied by enhanced serum gastrin release possibly related to the suppression of this germ of the D-cells and release of somatostatin (31, 32).

As oral cavity is equipped with myriad of various mechano- and chemoreceptors playing crucial role in the short-term control of food intake, further studies would be required to establish whether oral infection with more toxic H. pylori expressing various cytotoxins (CagA or VagA), especially in the mucosal area with histopathological changes and erosions could activate afferent cephalic pathways causing alteration in the neuronal mechanisms controlling of food intake.


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