Oral Cavity as an Extragastric Reservoir of Helicobacter pylori
Background. Several studies were reported on the prevalence, and relationship between the existence of Helicobacter pylori (H. pylori) in oral cavity and in stomach of patients. The purpose of this study was to systematically review the existing literature on the presence of H. pylori in the oral cavity and its link to gastric infection, the existence of coinfection, and the impact of anti-H. pylori therapy on the dental plaque and vice versa. Method. Two authors independently searched the Medline, EMBASE, Cochrane Library, Web of Science, Google Scholar, and Scopus databases for relevant studies. The articles were analyzed critically and all qualified studies were included. The search was carried out by using a combined text and the MeSH search strategies: using the key words Helicobacter, Helicobacter pylori, and H. pylori in combination with dental plaque, periodontitis, and oral hygiene. Results. The data was presented in 8 tables and each topic separately discussed. Conclusion. Based on the systematic review of the available literature on H. pylori infection and its presence in the oral cavity, it can be concluded that dental plaque can act as a reservoir, and proper oral hygiene maintenance is essential to prevent reinfection. Due to the diversified methods and population groups involved in the available literature, no concrete evidence can be laid down. Further studies are necessary to establish the role of H. pylori in the oral cavity and its eradication on preventing the gastroduodenal infection.
Helicobacter pylori (H. pylori) is one of the most common bacterial infections in humans . The presence of the organism H. pylori (initially termed Campylobacter pyloridis) in the antral mucosa of humans was first reported in 1983 . H. pylori has been closely linked to chronic gastritis, peptic ulcer, gastric cancer, and mucosa-associated lymphoid tissue (MALT) lymphoma [3, 4]. The International Agency for Research on Cancer of the World Health Organization (WHO) has designated H. pylori as a Group 1 carcinogen . Besides gastrointestinal diseases, recent data seems to suggest a possible association of this microorganism with other conditions such as anemia , altered serum levels of lipoproteins , and coronary atherosclerosis . Although H. pylori is present in the stomach of about half of the world’s population, we do not yet clearly understand its transmission. Available data suggests that oral-oral and fecal-oral routes are the most likely routes of transmission of this organism [9, 10]. However, no extragastric reservoirs of H. pylori have been clearly demonstrated. A recent study has reported the detection of the organisms in soil samples in public playgrounds suggesting the role of the abovementioned routes in the transmission of the organism . However, the likelihood of transmission of infection through contaminated soil needs to be clarified. Although organisms resembling H. pylori may be detected in other animals, none, except non-human primates  and cats , harbor H. pylori. Infections by Helicobacter species (H. heilmannii and H. felis) have been reported in dogs and cats [14, 15]. It has been suggested that the microorganism may be transmitted orally and has been detected in dental plaque and saliva [16–18]. But whether the oral cavity serves as an extragastric reservoir for H. pylori or harbors the organism only transiently, is not yet clear (the organism being only a transient inhabitant of this ecological niche or not). If the oral cavity is an extragastric reservoir of the H. pylori, it may be clinically significant from the treatment aspect as the microorganisms residing in the dental plaque are afforded protection from systemically administered antimicrobial agents. Treatment of H. pylori infection usually involves a combination of antibiotics, acid suppressors, and stomach protectors. Despite the current treatment regimens that lead to successful management of H. pylori—positive chronic gastritis, the reinfection rate is relatively high . One of the suggested mechanisms of reinfection is the possible recolonization from the dental plaque . A large number of studies have been carried out among various populations to determine whether dental plaque and periodontal disease are associated with H. pylori infection. This paper attempts to review the current evidence regarding the role of oral cavity as an extragastric reservoir of H. pylori.
2. Materials and Methods
2.1. Literature Search
A systematic review was conducted in January 2013. All relevant studies published between January 1990 and December 2012 were identified and included in the systematic analysis. Two authors independently searched the Medline, EMBASE, Cochrane Library, Web of Science, Google Scholar, and Scopus databases for relevant studies. The search was carried out by using a combined text and the MeSH search strategies: using the key words Helicobacter, Helicobacter pylori, and H. pylori in combination with dental plaque, periodontitis, and oral hygiene. We also examined the bibliographies from identified studies, reviews, and gray literature. The last search was conducted on December 31, 2012.
2.2. Study Selection Criteria
Studies reporting the identification of Helicobacter pylori in dental plaque, coinfection of periodontitis and H. pylori, effect of periodontal therapy on H. pylori, and effect of treatment of H. pylori infection on periodontal problems were included in the review. The types of studies included were cross-sectional, experimental studies and interventional studies. Patients in all age groups were included. Studies presented solely in the form of abstracts in scientific conferences and studies published in languages other than English were not considered in this review.
2.3. Data Extraction Considerations
Data extracted from each of the included studies was referred to the study design, the method used to study the presence of H. pylori, and the type of association between the periodontal problems and H. pylori infection. The data was presented in a tabular form with the variables in quantitative and qualitative format.
The papers were grouped according to the content of the study and presented in 8 tables based on the date of publication of the study. Tables 1–4 depict the presence of H. pylori in dental plaque. Tables 5 and 6 enumerate the coinfection and association studies between H. pylori infection and periodontal disease. Table 7 shows the effect of anti-H. pylori therapy on its presence in dental plaque. Studies on the effects of periodontal treatment on H. pylori presence in dental plaque and gastric infection are listed are Table 8.
2.4. Methods of Detection of H. pylori
Various methods have been employed to detect the presence of the bacterium H. pylori in the gastrointestinal mucosa. These include histology, culture, urease test, serologic tests, urea breath test, and polymerase chain reaction targeting specific nuclear material of the microorganism . Histological methods using conventional hematoxylin and eosin staining can be used to visualize H. pylori while use of special stains such Warthin-Starry and Giemsa staining can enhance the histologic identification of the microorganism. By employing culture methods, antimicrobial susceptibility tests can be performed. Urease tests and urea breath tests are based on the fact that the microorganisms are associated with large amounts of urease activity while serologic tests detect the levels of antibodies such as IgG and IgA in the serum that is elevated in response to an infection by H. pylori. Several different polymerase chain reaction (PCR) methods which differ in their target DNA have been developed for the diagnosis of H. pylori infection and these can help to differentiate between H. pylori strains.
2.5. H. pylori in Dental Plaque
The prevalence of H. pylori in the dental plaque has been studied by several investigators. The results of these studies showed wide variation and this seems to depend at least in part on the method employed to detect the bacterium in the dental plaque. As mentioned earlier, investigators have used several methods to detect the presence of the bacterium in the dental plaque and these include urease tests (rapid urease/CLO test), PCR, histology, culture, and immunoassays.
2.6. Prevalence Data as Reported in Studies Utilizing Urease Tests
The prevalence of H. Pylori in the dental plaque of study participants reported by investigators using urease tests is given in Table 1. The prevalence of H. pylori in dental plaque in these studies generally ranged from 50% to 100% except in 3 studies. In 2 of these studies the prevalence rates reported were 44.8%  and 43%  while the lowest rate reported was 18.2% .
2.7. Prevalence Data as Reported in Studies Utilizing PCR
The prevalence of H. pylori in the dental plaque of study participants reported by investigators using PCR is given in Table 2. The prevalence rates reported in these studies ranged from 0-100% and were generally lower than those reported in studies in which urease tests were used to detect the presence of H. pylori in dental plaque. However, out of the 34 studies reviewed in this category, only 7 studies reported a prevalence rate exceeding 50%. Of these 7 studies, 6 were conducted amongst Asian populations.
2.8. Prevalence Data as Reported in Studies Utilizing Culture
The prevalence of H. pylori in the dental plaque reported by investigators using culture method is given in Table 3. The prevalence rates reported in these studies were generally below 50% with about half studies reported less than 10% prevalence. In 2 of these studies [24, 25], the microorganism could not be cultured from the dental plaque.
2.9. Prevalence Data as Reported in Studies Utilizing Immunoassays
The prevalence of H. pylori in the dental plaque reported by investigators using immunoassays is given in Table 4. Using this method for detection of H. pylori in dental plaque, 2 studies [26, 27] reported a high prevalence (>65%) of the microorganism in dental plaque while other 2 studies [28, 29] reported a very low prevalence (0 and 11%).
2.10. Prevalence of Coinfection of Gastric Mucosa and Dental Plaque by H. pylori
The summary of studies which have evaluated the prevalence of coinfection of gastric mucosa and dental plaque by H. pylori among the study participants is given in Table 5. The prevalence rate of coinfection among the respective study populations reported by different investigators ranged from as low as 1% to as high as 82.1%. This wide variation in the prevalence rates of coinfection may be partly due to the difference in the diagnostic tests employed by various investigators to detect the bacterium in the dental plaque. Studies utilizing urease tests to detect the presence of the microorganism in the dental plaque have reported very high prevalence rates. Except for one study which reported a 25.2% prevalence of coinfection, all the other studies utilizing urease tests have reported a coinfection rate in excess of 32%, with one study reporting a prevalence rate of 81.3% . In studies involving PCR, the prevalence rates have ranged between 0% and 47.6% with only 5 out of the 11 studies reporting a prevalence rate above 30%. Low rates of prevalence of coinfection were reported when microbial culture was employed to detect H. pylori from the dental plaque. Out of the 5 studies reviewed which employed microbial culture, the rates of prevalence reported were 1%, 1.4%, 6.9%, 14.6%, and 18%, respectively [16, 31–33]. In the 2 studies reviewed which used immunoassays for detection of pathogen in dental plaque samples, the prevalence rates reported were 23.6% and 47.6% . Among patients with gastrointestinal colonization by H. pylori, the prevalence of coinfection in dental plaque was reported to be in the range of 25.2% to 100%. In studies involving the use of urease test only 2 out of the 8 studies reported a prevalence rate of less than 50%; 0% to 100% in PCR studies with 5 out of the 11 studies reviewed reported a prevalence rate above 50%; 1.7% to 30% in the 5 studies using microbial culture; and 23.6% to 82.1% in studies using immunoassays.
2.11. H. pylori and Periodontal Disease
Few studies have evaluated the relationship between gingival and periodontal disease and H. pylori infection. While some investigators [34, 35] have reported a positive association between the two conditions, others have reported that there was no association between H. pylori infection and periodontal diseases [18, 36]. Table 6 shows the studies which have evaluated the relationship between periodontal disease and H. pylori infection.
A large-scale epidemiological study which evaluated the relationship between H. pylori infection and abnormal periodontal conditions by Dye et al.  utilized the data from the first phase of the third National Health and Nutrition Examination Survey. A total of 4504 participants aged 20 to 59 years who completed a periodontal examination and tested positive for H. pylori antibodies were examined. Periodontal pockets with a depth of 5 mm or more were associated with increased odds of H. pylori seropositivity after adjustment for sociodemographic factors. The authors reported that this association is comparable to the independent effects of poverty on H. pylori and concluded that poor periodontal health, characterized by advanced periodontal pockets, may be associated with H. pylori infection in adults, independent of poverty status.
Nested polymerase chain reaction (PCR) was employed by Umeda et al.  to clarify whether the oral cavity acts as a reservoir for H. pylori. The existence of H. pylori in the oral cavity was determined by nested PCR in 57 subjects and by culture method in 18 subjects. The presence of periodontopathic bacteria was also determined by 16S rRNA-based PCR method. Although H. pylori was rarely detected in the oral cavity by culture technique, it was frequently detected (35.1%) by nested PCR, especially among periodontitis patients who had the bacterium in the gastrointestinal tract (46.4%). Among the subjects who harbored H. pylori in the stomach or duodenum, 41.2% of patients with periodontal pockets ≥4 mm and 9.1% of subjects without periodontal pockets showed H. pylori in dental plaque. They also reported that one patient who had periodontal pockets retained H. pylori in the oral cavity even after eradication of the bacterium from the stomach and duodenum. Most (8/10) of the patients who had H. pylori in dental plaque harbored Bacteroides forsythus in their oral cavities. Based on the previously mentioned findings, the authors concluded that close attention should be given to periodontitis patients who harbor H. pylori in the oral cavity.
Association between periodontal disease and H. pylori infection was tested in a case-control study among 134 dyspeptic patients reporting for upper gastrointestinal endoscopy . The periodontal status of the patients was examined as a dichotomous variable with patients being described as being either diseased or healthy depending on their periodontal status. Among the cases, 30 subjects out of 65 (46.2%) had periodontal disease compared to only 20 out of 69 (29%) in comparison to the controls. Although the univariate analysis suggested that the relationship was significant, when analyzed by logistic regression, the difference was found to be not significant.
Lack of association between H. pylori infection and periodontal disease was reported by Berroteran et al.  based on the results from their study of a Venezuelan population. Gingival and Plaque indices were used to assess the gingival and oral hygiene status of the 32 dyspeptic patients and 20 asymptomatic subjects. It was found that patients with poor oral hygiene and periodontal status had a similar prevalence of H. pylori to patients with good-to-moderate dental hygiene.
To elucidate the possible sources of H. pylori infection in an isolated, rural population in Guatemala, Dowsett et al.  examined 242 subjects in family units. Periodontal status, H. pylori antibody status, and presence of H. pylori in the dental plaque, dorsum of tongue, and fingernails were recorded. PCR based on 16S rRNA gene of H. pylori were employed for the detection of the microorganism in the plaque, tongue, and finger nail samples. It was found that there was no statistically significant relationship between H. pylori status and periodontal disease. A high rate of oral carriage was found irrespective of periodontal status, showing no association with pocket depth.
Al Asqah et al.  reported that 60% (37/62) of the periodontitis patients in their study harbored H. pylori in their stomach compared to only 33% (13/39) of the patients without periodontitis. Furthermore, they reported that the prevalence of H. pylori in the dental plaque was higher among periodontitis patients (79%, 49/62) than in patients without periodontitis (43%, 17/39). They also reported that the presence of the bacterium in both locations was higher among periodontitis patients (46.8%, 29/62) than in patients without periodontitis (10.3%, 4/39).
2.12. Effects of Systemic Anti-H. pylori Therapy on Dental Plaque
A total of 8 studies [30, 40–46] were reviewed in which the effect of anti-H. pylori therapy on its presence in the dental plaque was evaluated. The summary of these studies are given in Table 7. In 6 of these 8 studies, PCR was used to detect H. pylori in dental plaque while in one study  urease test was used and in the other  smear cytology was used. In their study on 82 H. pylori positive patients, Butt et al.  treated 27 of these patients with anti-H. pylori therapy (triple therapy-2 antibiotics and 1 proton pump inhibitor) alone and reported 100% prevalence of H. pylori in the dental plaque of these 27 patients after 10 days of treatment. Gürbüz et al.  conducted a study among 75 dyspeptic patients in which H. pylori positive patients were treated with anti-H. pylori therapy. In this study, initially 68 (91%) patients were positive for H. pylori in dental plaque and 65 (87%) were positive for H. pylori in the gastric mucosa. When the procedures were repeated after 1 month following treatment, the authors reported that all the dental plaque samples were positive for H. pylori although they had not mentioned the number of patients treated with anti-H. pylori therapy. Among the studies in which PCR was employed for pathogen detection, Gao et al.  reported that, among 37 H. pylori positive patients, the prevalence of plaque colonization was 29.7% and 43.2%, respectively, at 4 weeks and 1 year after anti-H. pylori therapy. Gebara et al. , in their study on 30 dental patients with periodontitis and H. pylori infection, reported an increase in the prevalence of plaque colonization from 20% to 30% in supragingival plaque and from 26.6% to 46.7% in subgingival plaque. Suk et al.  reported that, after anti-H. pylori therapy, the microorganism persisted in the dental plaque of 92.9% () of the 28 patients who harbored the organism in the dental plaque before anti-H. pylori therapy. Zaric et al.  reported that, after anti-H. pylori therapy, the pathogen could be detected in the dental plaque of 66.7% () of the 21 patients who were positive for the microorganism both in the subgingival plaque and gastric mucosa before the intervention. Miyabayashi et al.  in their study on 47 dyspeptic patients reported 48.9% () positive for oral H. pylori and 38.3% () had H. pylori in plaque before anti-H. pylori treatment. At 4 weeks after treatment, they reported that 31.9% of the patients were positive for oral H. pylori. However, they did not specify how many patients were positive for the microorganism in the dental plaque. Contrary to these studies, Bago et al. , reported that 21 patients were positive for H. pylori in the dental plaque in a study on 56 chronic periodontitis patients who harbored H. pylori in the gastric mucosa. They reported complete eradication of H. pylori from dental plaque in all of the 21 patients following anti-H. pylori therapy consisting of 2 antibiotic and 1 proton pump inhibitor (PPI).
2.13. Effects of Periodontal Therapy on Dental Plaque-Associated H. pylori
Three studies have evaluated the effects of nonsurgical periodontal therapy on H. pylori residing in the dental plaque (Table 8). Butt et al.  categorized 82 patients who harbored H. pylori in their dental plaque into 3 groups based on the type of intervention—Group 1 which received only anti-H. pylori therapy (), Group 2 which received anti-H. pylori therapy plus periodontal therapy (), and Group 3 which received only periodontal therapy (). Ten days after treatment, the prevalence of H. pylori in dental plaque for Groups 1, 2, and 3 were 100%, 16%, and 10%, respectively. In a study on 43 patients who harbored H. pylori both in the subgingival plaque and gastric mucosa, Zaric et al.  reported that, among 22 patients who received both anti-H. pylori therapy and periodontal therapy, H. pylori was detected in the dental plaque of only 6 patients 3 months after completion of treatment compared to 21 patients who received only anti-H. pylori therapy among whom the prevalence after intervention was 66.7%. Gao et al. , in their study to evaluate the effects of combination of anti-H. pylori therapy (triple therapy) and periodontal therapy for the management of H. pylori infection, treated 37 patients with anti-H. pylori therapy alone and 43 patients with a combination of anti-H. pylori therapy and periodontal therapy. The detection rates of H. pylori in the dental plaque for both groups at 4 weeks after intervention were 29.7% and 4.7%, respectively, and 43.2% and 18.6%, respectively, one year after intervention.
2.14. Effects of Periodontal Therapy on Gastric H. pylori Infection
Three studies have evaluated the effects of periodontal therapy on gastric H. pylori infection. Gao et al.  reported that, among 43 H. pylori positive patients who received both anti-H. pylori therapy and periodontal therapy, the gastric eradication rate at 4 weeks and 1 year after intervention was 81.4% and 62.8%, respectively, while the eradication rates at same time periods among 37 H. pylori positive patients who received only anti-H. pylori therapy were 73% and 32.4%. Zaric et al.  conducted a study among 43 patients who were positive for H. pylori in both subgingival plaque and gastric mucosa in which 21 patients received only anti-H. pylori therapy while 22 received anti-H. pylori therapy along with periodontal therapy. Three months after completion of treatment, 77.3% of the patients who received both anti-H. pylori therapy and periodontal therapy showed gastric eradication compared to only 47.6% of the patients who received only anti-H. pylori therapy. The authors also reported that eradication in the stomach coincided with eradication from the oral cavity; that is, all 16 of the individuals who received both forms of therapy and showed eradication of oral H. pylori, also showed eradication of gastric H. pylori. Five of the participants in this group who were positive for oral samples were positive for gastric H. pylori as well. Jia et al. , in a study on 107 H. pylori positive dyspeptic patient, reported that, 6 months after complete eradication of H. pylori from gastric mucosa, reinfection of the gastric mucosa by the bacterium was observed in 84.31% of the patients who did not receive any form of dental plaque control compared to only 19.64% of the patients who received dental plaque control and full-mouth scaling and root planing.
H. pylori is a major etiologic factor in the development of gastritis and peptic ulcer disease. There is sufficient evidence on the presence of H. pylori in the subgingival oral biofilm which could act as a reservoir for harboring H. pylori, leading to gastric reinfection. Hence, it is imperative to adapt a multidisciplinary clinical management protocol, merging the triple therapy to periodontal mechanical treatment and chemical antiseptic disinfection. Further research that may be directed towards controlled randomized clinical trials are necessary for testing the efficacy of the multidisciplinary therapeutic regimen.
Conflict of Interests
The authors declare that there is no conflict of interests regarding the publication of this paper.
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