P- Reviewer: Zhou LY S- Editor: Ji FF L- Editor: A E- Editor: Wang CH
Published online Feb 6, 2016. doi: 10.4292/wjgpt.v7.i1.126
Peer-review started: April 30, 2015
First decision: July 25, 2015
Revised: October 16, 2015
Accepted: November 10, 2015
Article in press: November 11, 2015
Published online: February 6, 2016
Helicobacter pylori (H. pylori) has long been found to cause gastric diseases such as gastritis, gastric ulcers and gastric cancer. The transmission medium of this bacterium has yet to be determined, though several studies have speculated that the oral cavity is a reservoir for H. pylori. Others have also reported that the oral cavity may be a source of both transmission and gastric reinfection; however, such results are controversial. We reviewed the literature and selected studies that report an association among H. pylori detections in the oral cavity (dental plaque, saliva, tongue, tonsil tissue, root canals, oral mucosa) in humans and in animals, as well as in the human stomach. The oral cavity may be considered the main reservoir for H. pylori. There are a correlations between H. pylori infection in the oral cavity and periodontal disease, oral tissue inflammation, H. pylori transmission, and gastric reinfection. We believe that the mouth is a reservoir and that it plays a crucial role in both H. pylori transmission and gastric infection.
Core tip: This review focuses on some aspects of infection and reinfection by Helicobacter pylori (H. pylori), particularly in the possible reservoirs of this bacterium. It also explores the association between gastric infection and these reservoirs. In addition, this review highlights possible reservoirs in animals and some routes of infection, and it considers the techniques used to diagnose this bacterium in different environments. The difficulty in accessing bacteria in reservoirs is a problem for H. pylori eradication in particular, and new discoveries in this field will contribute to the understanding of H. pylori infection mechanisms.
- Citation: Payão SLM, Rasmussen LT. Helicobacter pylori and its reservoirs: A correlation with the gastric infection. World J Gastrointest Pharmacol Ther 2016; 7(1): 126-132
- URL: https://www.wjgnet.com/2150-5349/full/v7/i1/126.htm
- DOI: https://dx.doi.org/10.4292/wjgpt.v7.i1.126
Helicobacter pylori (H. pylori) is a gram-negative and microaerophilic bacterium that has been associated with some certain diseases, including chronic gastritis, peptic ulcers, gastric cancer, and mucosa-associated lymphoid tissue (MALT) lymphoma. In 1994, the International Agency for Research on Cancer of the World Health Organization defined H. pylori as a Group 1 carcinogen[1,2].
It is estimated that the H. pylori is present in the stomachs of 50% of the world’s population, but despite this high prevalence, we do not yet clearly understand its transmission. Possible routes are oral-oral and fecal-oral, but no consensus has been reached.
Currently, the main area of research into natural reservoirs for H. pylori has included oral H. pylori with gastric infection and the presence of H. pylori in the stomach[1,4]. Many studies have suggested that the primary reservoir for H. pylori is the oral cavity, but overall, the results have been very inconsistent[1-7].
Several previous studies reported success in diagnosing H. pylori from oral samples from dental plaque, saliva, tongue, tonsil tissue and root canals. These other researchers have raised the question of whether the mouth is a common source of stomach reinfection, even after treatment is received[4-8].
Miyabayashi et al were the first to investigate the influence of oral H. pylori on the stomach. In short, their patients with oral H. pylori were found to be at a significantly higher risk for gastric reinfection after having received successful treatment. The authors also determined that drugs recommended for the eradication of the H. pylori from the stomach seem to have no effect on oral H. pylori.
At this stage of research, the crucial questions are whether the oral cavity is a reservoir and whether it plays a role in H. pylori transmission. Therefore, this review includes all relevant studies that report the detection of H. pylori in a reservoir and the possible relationship between gastric and extra-gastric infection.
Krajden et al were the first authors to perform H. pylori isolation in H. pylori-positive patients with gastric symptoms of infection. Twenty-six years later, researchers have yet to reach a conclusion about the role of the oral cavity in gastric infection by H. pylori.
In 2015, two relevant studies were published on this topic. In the first, Ismail et al developed a new nested-PCR assay that can be used to identify H. pylori DNA in dental plaque samples. These authors report that this new nested PCR is as sensitive as tests that rely on histology, and also that it may be useful when patients must be tested for H. pylori but are unable to undergo endoscopic examinations. In the second study, Amiri et al analyzed 45 samples of dental plaque and detected H. pylori in 44% (20/45), 66.67% (30/45) and 77.78% (35/45) using PCR, LAMP reaction, and positivity for both the PCR test and the LAMP test, respectively. In addition to their reports of a high frequency of H. pylori in the dental plaque samples, they also determined that dental plaque may be one of the main causes of reinfection, as well as the cause of oral-oral transmission.
Ahmed et al used PCR for 16S rRNA to establish the presence of H. pylori. They analyzed saliva and gastric biopsy samples from 400 symptomatic subjects and detected H. pylori in 246 (61.5%) and 240 (60%) samples from gastric biopsies and saliva, respectively. They also found that H. pylori prevalence in both samples was higher in older populations, and their report highlighted the oral-oral transmission.
Liu et al analyzed 443 symptomatic patients and verified the presence of H. pylori in 59.4% (263/443) of their dental plaque samples and in 61.6% (273/443) of their stomach samples. These results corroborate the findings reported by Liu et al, who found 126 (58.9%) of 214 children’s dental plaque samples to be H. pylori positive and who also reported a statistically significant correlation between the H. pylori infection and dental caries.
In addition, Souto and Colombo studied 225 adult subjects who sought dental treatment and detected H. pylori in 24% of the samples. More sub-gingival biofilm samples (33.3%) than saliva samples (20%) tested positive for H. pylori. The same authors also offered the theory that “periodontal pocketing and inflammation may favor the colonization by (H. pylori)”.
Rasmussen et al used southern blots on DNA extracts from saliva and dental plaque samples in order to detect H. pylori in 78 patients with gastric disease. A total of 33 saliva samples (42%) were found to be positive for H. pylori, and 37 dental plaque samples (47.4%) were found to be positive. In another study by our group, Rasmussen et al reported significant genotypic diversity among H. pylori cytotoxins that had been found in stomach, saliva, and dental plaque samples. The study revealed the strains from the stomach to be more virulent than those from the oral cavity.
Results described by Silva et al are more convincing. They detected H. pylori in 30/30 (100%) of their patients’ gastric biopsies, in 16/30 (53.3%) of their saliva samples, and in 11/30 (36.6%) of their dental plaque samples. These researchers also detected the cagA gene in 13/30 (43.3%) of their patients’ gastric biopsies, in 7/16 (43.8%) of their saliva samples, and in 3/11 (27.3%) of their dental plaque samples. Similar results found by Assumpção et al who found that 96% of their patients’ gastric mucosa samples and 72% of their dental plaque samples were positive for H. pylori. Furthermore, they determined 63/71 (89%) of their patients’ dental plaque samples to be both positive for H. pylori and to possess identical vacA and cagA genotypes in gastric mucosa.
All authors mentioned above suggest that dental plaque and saliva may be an important reservoir for H. pylori and that the presence of H. pylori in the oral cavity may contribute to oral diseases, oral transmission, gastric reinfection, and also virulence strains.
Meanwhile, Silva Rossi-Aguiar et al analyzed saliva, tongue dorsum, and supra gingival dental plaque samples from 43 patients with gastric disease and did not detect H. pylori in these oral samples. Their results that consistent with those of Olivier et al, who also failed to detect H. pylori in dental samples. Both studies question the theory of the oral cavity serving as a reservoir for H. pylori in patients with symptoms of gastric disease.
There is a large variability in the oral cavity H. pylori frequency rates described in the literature. These differences could be explained by variations in sample demographics, the use of different sampling procedures or detection methods, the patients’ oral health statuses, differences in H. pylori infection statuses, the type and number of clinical samples used, and varying complexities among the oral microbiota samples used across the studies[7,15-17,21].
Gastric heterotopia (GH) can occur throughout the digestive tract; however, the involvement of the tongue is rare, and fewer than 40 cases have been reported to date. When GH is found in the head and neck region, it is frequently in cases of children or young adults, and it is more prominent among males[22,23].
A histologic evaluation was given to a 21-year-old man who reported the growth of a mass on his tongue 4 years prior to the exam and who presented ulcerations in the last 3 mo. The evaluation revealed the presence of gastric tissue that extended into the striated muscle layer of the tongue. There were scattered intestinal metaplasia foci containing Goblet cells. Toluidine-blue-stained sections suggested the presence of H. pylori in the lumina of the glandular epithelium. Colonization by H. pylori was determined by the immunohistochemical method using polyclonal H. pylori antibody, and the finding was confirmed using the PCR method.
There is also a great diversity in the different biological surfaces of the oral cavity that are subject to colonization by different bacterial species. Different studies have isolated H. pylori from samples taken from oral cavities, dental plaque (supragingival and subgingival plaque), dorsa of tongue, and salivary secretions. H. pylori findings in oral cavities and dental plaque are conflicting. The differing results of tests to determine the prevalence of H. pylori in oral cavities are partly due to the use of different detection methods[25,26].
Clinical presentation varies depending on the site considered and on the extent of the lesion. An GH issue of note is the colonization by H. pylori and its association with complications. In their study, Berber et al reports the first case of a peptic ulcer and intestinal metaplasia associated with the colonization of H. pylori in a case of GH of the tongue.
Although the oral cavity has been suggested as a reservoir for H. pylori infection, the findings have not been definitive. Some authors have proposed the theory that in cases of gastroesophageal reflux disease (GERD), gastric fluid that is contaminated with H. pylori enters the nasopharyngeal cavity, thus allowing the bacterium to colonize in dental plaque and adenotonsillar tissue. Other researchers have also recently offered evidence of H. pylori in gastric mucosa that was bound to MALT. Because of these findings, more efforts have recently been placed on detecting H. pylori in adenotonsillar tissue.
Nártová et al detected and genotyped H. pylori and found data supporting the possible role played by H. pylori in the etiologies of both chronic tonsillitis and sleep apnoea syndrome (SAS). H. pylori was detected through the use of real-time polymerase chain reaction. A total of 89 patients were tested, 60 of whom had received a diagnosis of chronic tonsillitis and 29 of whom had SAS. In the chronic tonsillitis group, H. pylori was detected in 48 (80%) of the samples, the cagA gene was detected in 12 samples (25%), and 12 samples were negative. In the SAS group, H. pylori was found in 24 samples (82.76%), cagA gene was detected in 5 samples (20.83%), and 5 samples (17.24%) were negative.
Nártová et al’s study shows that the oropharynx represents a reservoir for H. pylori infection that could be an etiopathogenetic factor in chronic tonsillitis and tonsillar hyperplasia caused by SAS. No conclusion has been drawn regarding the mechanisms of the process.
In another study, Abdel-Monem et al tested 30 adenotonsillectomy specimens (20 tonsils and 10 adenoids). RUT results were positive in 16 of their samples (12 tonsils and 4 adenoids; 53.3%). The authors report that, “according to the ‘gold standard’, 11/16 were considered a false positive, yielding a sensitivity of 100% and specificity of 56%”. The authors also used PCR, and the ureC gene sequence was detected in 5 specimens (3 tonsils and 2 adenoids; 16.6%), all of which also tested positive when RUT was used. In these cases, the patients were considered to be infected by H. pylori. For this reason, the authors reported PCR sensitivity and specificity to be 100%. Serology testing results were positive for H. pylori IgG antibodies in 4/20 patients (20%), only two of whom were found to have H. pylori-infected adenotonsillar tissue.
On the other hand, Aliakbari et al reported that neither gastrointestinal symptoms nor H. pylori seropositivity were correlated with the presence of H. pylori or H. hepaticus in adenotonsillar tissues. The findings did not support the idea that adenotonsills is a reservoir for H. pylori or H. hepaticus. The study included 90 patients (36% female and 64% male) who had been diagnosed with chronic tonsillitis and adenoid hypertrophy; the average age of the study group was 36 ± 22 years. In their study, Aliakbari et al detected H. pylori and H. hepaticus using glmM gene and 16S rRNA-specific primers, respectively. Out of all of their patients, 58 (65%) were found to be seropositive for the H. pylori IgG, though only 7 (8%) patients presented any gastrointestinal symptoms and all 7 were cases of gastritis. According to the authors, neither H. pylori nor H. hepaticus was detected in any of the patients when PCR was used.
In conclusion, there are inconsistent results regarding the detection of H. pylori in the tonsils and adenoids; however, we believe that there is enough evidence to support the theory that such tissues can be considered a reservoir of such bacteria.
Most of the studies considered in this review analyzed dental plaque, saliva, and/or oral mucosa samples. In these studies, several H. pylori markers were identified through the use of various tests, including the urea breath test, the rapid urease test, the Campylobacter-like organism test, and/or polymerase chain reaction (PCR). Some PCR studies found H. pylori DNA in samples from oral cavities, but overall, reports of live H. pylori are very rare and inconclusive.
In light of this literature review, we agree with Zou and Li and their report that H. pylori can be identified unequivocally only through the use of direct cultures. This limitation exists because erroneous PCR results can result from the presence of transient H. pylori in the mouth. This transient presence occurs in cases of interference from food or from acid that includes H. pylori or its DNA that reaches the mouth via reflux from the stomach[33,35,36]. Hirsch et al “erroneous results can also arise from the misclassification of other urease-producing microorganisms. Thus, it is still unclear whether H. pylori can indeed survive in the oral environment”.
In another study by Hirsch et al, electron microscopy, selective growth techniques, urease assays, 16S rRNA PCR, and western blotting were used to determine whether live H. pylori were present in 10 root canal and corresponding plaque samples taken from endodontic-infected deciduous teeth from three children. In their study, they report that PCR was able to identifiy H. pylori DNA in several plaque and root canal samples. However, bacterial colonies were successfully grown from two root canals, but not from plaque. As the authors report, “these colonies were unequivocally identified as H. pylori by microscopic, genetic, and biochemical approaches”. The authors showed that root canals performed on endodontic-infected teeth may create a reservoir for live H. pylori, and that this reservoir may serve as a potential source of transmission.
Genomic DNA was isolated from samples taken during 25 root canals of teeth from patients with asymptomatic and chronic apical periodontitis and from 25 patients with aspirates from acute apical abscess. These DNA samples were first amplified using the multiple displacement amplification approach and were then used as a template in species-specific PCR in order to determine whether H. pylori and C. pneumoniae were present. Neither H. pylori nor C. pneumoniae were found in samples from primary endodontic infections. These findings suggest that these species are not possible endodontic pathogens and that the necrotic root canal does not serve as a reservoir for these human pathogens in healthy patients.
In another study by Correia-Silva Jde et al, many H. pylori-positive results were found in the oral mucosa of 46 haematopoietic stem cell transplantation (HSCT) patients. The authors report that their findings may be due to the patients’ poor oral hygiene during the transplantation and/or immunosuppression procedures involved in HSCT therapy. Other authors note that, because “the oral cavity is a frequent site of local infections and an important port of entry for systemic infections in HSCT recipients..., the presence of H. pylori in the oral cavity may be a risk factor for infection or reinfection of the stomach of these patients”[9,38]. Though this literature review shows that the exact role played by H. pylori in oral cavity infections has not been confirmed, these findings may be relevant to the gastrointestinal pathology of HSCT patients.
According to Momtaz et al, there is a possibility that zoonotic transmission of H. pylori occurred, but this transmission has not been proven in non-primate reservoirs.
In the first report of infection by H. pylori in animals in 1990, Jones and Elridge isolated a strain of H. pylori from a pig stomach and suggested that pigs may be a possible reservoir for this bacterium. Eaton et al and Engstrand et al supported this hypothesis; both authors have succeeded in infecting pigs, specimens which subsequently developed gastritis. However, De Groote et al more recently sequenced the 16S of rDNA of H. pylori and then named the bacterium Helicobacter suis. Mégraud and Broutet analyzed all of these studies and concluded that pigs are not a reservoir for H. pylori. They suggest the bacterium isolated by Jones and Elridge was probably acquired from human beings.
Four years later, Jones and Elridge detected H. pylori in a pig stomach sample. Handt et al diagnosed the H. pylori in six cats - their identification was confirmed through the use of 16S rDNA sequencing. However, no other studies confirm these results. These studies argue that cats serve as a reservoir for H. pylori, but additional studies are necessary to determine whether cats are actually an important route of transmission. Based on the overall data available, having a cat as a pet does not put owners at risk of acquiring H. pylori infection.
More recently, Momtaz et al analyzed 800 samples, 200 of which were from human beings and 600 of which came from healthy animals (200 cows, 200 sheep and 200 goats). They detected H. pylori and main virulence markers (gene cagA and vacA) using PCR and selected 6 H. pylori-positive samples (3 samples from cows and 3 samples from sheep) for DNA sequencing analysis.
They reported that the H. pylori was detected in 0/200 goat samples, 6/200 (3%) cow samples and in 32/200 (16%) sheep samples. Out of 200 human samples, 164 (82%) were infected with the bacterium. They also considered the virulence markers: A high prevalence of the cagA gene and of s1/m1 genotypes of the vacA gene were found in all of the samples. When the sequences of H. pylori isolates of sheep and humans were compared, 3.4%-8.4% variability and a 92.9%-98.5% homology were found. However, the greatest sequence similarity (98.5%) was found between the H. pylori isolates from Iranian sheep and those from German humans (FN598874), while the weakest relationship observed (91.6%) was between the Iranian cow and the South African population (NC017361).
According to Momtaz et al, cows and sheep were found to have H. pylori in their gastric tissue. The authors also theorize that sheep may be the natural reservoir for the bacteria and may be the source of H. pylori in human populations.
This literature review provides information to help determine the relevance of the several H. pylori reservoirs wherein each one possesses specific characteristics that favor or hinder the presence of H. pylori. Failure to eradicate and detection of H. pylori in reservoirs, may suggests an important route of reinfection and transmission, in additional to increase a risk of gastrointestinal disease.
|1.||Adler I, Muiño A, Aguas S, Harada L, Diaz M, Lence A, Labbrozzi M, Muiño JM, Elsner B, Avagnina A. Helicobacter pylori and oral pathology: relationship with the gastric infection. World J Gastroenterol. 2014;20:9922-9935. [PubMed] [DOI]|
|2.||Al Sayed A, Anand PS, Kamath KP, Patil S, Preethanath RS, Anil S. Oral Cavity as an Extragastric Reservoir of Helicobacter pylori. ISRN Gastroenterol. 2014;2014:261369. [PubMed] [DOI]|
|3.||García A, Salas-Jara MJ, Herrera C, González C. Biofilm and Helicobacter pylori: from environment to human host. World J Gastroenterol. 2014;20:5632-5638. [PubMed] [DOI]|
|4.||Liu Y, Yue H, Li A, Wang J, Jiang B, Zhang Y, Bai Y. An epidemiologic study on the correlation between oral Helicobacter pylori and gastric H. pylori. Curr Microbiol. 2009;58:449-453. [PubMed] [DOI]|
|5.||Ahmed KS, Khan AA, Ahmed I, Tiwari SK, Habeeb MA, Ali SM, Ahi JD, Abid Z, Alvi A, Hussain MA. Prevalence study to elucidate the transmission pathways of Helicobacter pylori at oral and gastroduodenal sites of a South Indian population. Singapore Med J. 2006;47:291-296. [PubMed]|
|6.||Lukes P, Astl J, Pavlík E, Potuzníková B, Sterzl I, Betka J. Helicobacter pylori in tonsillar and adenoid tissue and its possible role in oropharyngeal carcinogenesis. Folia Biol (Praha). 2008;54:33-39. [PubMed]|
|7.||Silva DG, Stevens RH, Macedo JM, Albano RM, Falabella ME, Veerman EC, Tinoco EM. Detection of cytotoxin genotypes of Helicobacter pylori in stomach, saliva and dental plaque. Arch Oral Biol. 2009;54:684-688. [PubMed] [DOI]|
|8.||Hirsch C, Tegtmeyer N, Rohde M, Rowland M, Oyarzabal OA, Backert S. Live Helicobacter pylori in the root canal of endodontic-infected deciduous teeth. J Gastroenterol. 2012;47:936-940. [PubMed] [DOI]|
|9.||Miyabayashi H, Furihata K, Shimizu T, Ueno I, Akamatsu T. Influence of oral Helicobacter pylori on the success of eradication therapy against gastric Helicobacter pylori. Helicobacter. 2000;5:30-37. [PubMed] [DOI]|
|10.||Loster BW, Majewski SW, Cześnikiewicz-Guzik M, Bielanski W, Pierzchalski P, Konturek SJ. The relationship between the presence of Helicobacter pylori in the oral cavity and gastric in the stomach. J Physiol Pharmacol. 2006;57 Suppl 3:91-100. [PubMed]|
|11.||Krajden S, Fuksa M, Anderson J, Kempston J, Boccia A, Petrea C, Babida C, Karmali M, Penner JL. Examination of human stomach biopsies, saliva, and dental plaque for Campylobacter pylori. J Clin Microbiol. 1989;27:1397-1398. [PubMed]|
|12.||Ismail H, Morgan C, Griffiths P, Williams J, Jenkins G. A Newly Developed Nested PCR Assay for the Detection of Helicobacter pylori in the Oral Cavity. J Clin Gastroenterol. 2016;50:17-22. [PubMed] [DOI]|
|13.||Amiri N, Abiri R, Eyvazi M, Zolfaghari MR, Alvandi A. The frequency of Helicobacter pylori in dental plaque is possibly underestimated. Arch Oral Biol. 2015;60:782-788. [PubMed] [DOI]|
|14.||Liu Y, Lin H, Bai Y, Qin X, Zheng X, Sun Y, Zhang Y. Study on the relationship between Helicobacter pylori in the dental plaque and the occurrence of dental caries or oral hygiene index. Helicobacter. 2008;13:256-260. [PubMed] [DOI]|
|15.||Souto R, Colombo AP. Detection of Helicobacter pylori by polymerase chain reaction in the subgingival biofilm and saliva of non-dyspeptic periodontal patients. J Periodontol. 2008;79:97-103. [PubMed] [DOI]|
|16.||Rasmussen LT, Labio RW, Gatti LL, Silva LC, Queiroz VF, Smith Mde A, Payão SL. Helicobacter pylori detection in gastric biopsies, saliva and dental plaque of Brazilian dyspeptic patients. Mem Inst Oswaldo Cruz. 2010;105:326-330. [PubMed] [DOI]|
|17.||Rasmussen LT, de Labio RW, Neto AC, Silva LC, Queiroz VF, Smith MAC, Payão SLM. Detection of Helicobacter pylori in gastric biopsies, saliva and dental plaques of dyspeptic patients from Marília, São Paulo, Brazil: presence of vacA and cagA genes. JVATiTD. 2012;18:7. [DOI]|
|18.||Assumpção MB, Martins LC, Melo Barbosa HP, Barile KA, de Almeida SS, Assumpção PP, Corvelo TC. Helicobacter pylori in dental plaque and stomach of patients from Northern Brazil. World J Gastroenterol. 2010;16:3033-3039. [PubMed] [DOI]|
|19.||Silva Rossi-Aguiar VP, Navarro-Rodriguez T, Mattar R, Siqueira de Melo Peres MP, Correa Barbuti R, Silva FM, Carrilho FJ, Eisig JN. Oral cavity is not a reservoir for Helicobacter pylori in infected patients with functional dyspepsia. Oral Microbiol Immunol. 2009;24:255-259. [PubMed] [DOI]|
|20.||Olivier BJ, Bond RP, van Zyl WB, Delport M, Slavik T, Ziady C, Terhaar Sive Droste JS, Lastovica A, van der Merwe SW. Absence of Helicobacter pylori within the oral cavities of members of a healthy South African community. J Clin Microbiol. 2006;44:635-636. [PubMed] [DOI]|
|21.||Graham DY. Helicobacter pylori update: gastric cancer, reliable therapy, and possible benefits. Gastroenterology. 2015;148:719-731.e3. [PubMed] [DOI]|
|22.||Erdem E, Tüz HH, Günhan O. Gastric mucosal choristoma of the tongue and floor of the mouth. J Oral Maxillofac Surg. 2001;59:210-212. [PubMed] [DOI]|
|23.||Berber U, Yılmaz İ, Erkul BE, Kaplan M. Peptic ulcer and intestinal metaplasia associated with Helicobacter pylori colonization in gastric heterotopia of the tongue. Turk J Gastroenterol. 2014;25:224-225. [PubMed] [DOI]|
|24.||Mager DL, Haffajee AD, Socransky SS. Effects of periodontitis and smoking on the microbiota of oral mucous membranes and saliva in systemically healthy subjects. J Clin Periodontol. 2003;30:1031-1037. [PubMed] [DOI]|
|25.||Czesnikiewicz-Guzik M, Bielanski W, Guzik TJ, Loster B, Konturek SJ. Helicobacter pylori in the oral cavity and its implications for gastric infection, periodontal health, immunology and dyspepsia. J Physiol Pharmacol. 2005;56 Suppl 6:77-89. [PubMed]|
|26.||Gebara EC, Pannuti C, Faria CM, Chehter L, Mayer MP, Lima LA. Prevalence of Helicobacter pylori detected by polymerase chain reaction in the oral cavity of periodontitis patients. Oral Microbiol Immunol. 2004;19:277-280. [PubMed] [DOI]|
|27.||Kurtaran H, Uyar ME, Kasapoglu B, Turkay C, Yilmaz T, Akcay A, Kanbay M. Role of Helicobacter pylori in pathogenesis of upper respiratory system diseases. J Natl Med Assoc. 2008;100:1224-1230. [PubMed]|
|28.||Abdel-Monem MH, Magdy EA, Nour YA, Harfoush RA, Ibreak A. Detection of Helicobacter pylori in adenotonsillar tissue of children with chronic adenotonsillitis using rapid urease test, PCR and blood serology: a prospective study. Int J Pediatr Otorhinolaryngol. 2011;75:568-572. [PubMed] [DOI]|
|29.||Cirak MY, Ozdek A, Yilmaz D, Bayiz U, Samim E, Turet S. Detection of Helicobacter pylori and its CagA gene in tonsil and adenoid tissues by PCR. Arch Otolaryngol Head Neck Surg. 2003;129:1225-1229. [PubMed] [DOI]|
|30.||Eyigor M, Eyigor H, Gultekin B, Aydin N. Detection of Helicobacter pylori in adenotonsiller tissue specimens by rapid urease test and polymerase chain reaction. Eur Arch Otorhinolaryngol. 2009;266:1611-1613. [PubMed] [DOI]|
|31.||Nártová E, Kraus J, Pavlík E, Lukeš P, Katra R, Plzák J, Kolářová L, Sterzl I, Betka J, Astl J. Presence of different genotypes of Helicobacter pylori in patients with chronic tonsillitis and sleep apnoea syndrome. Eur Arch Otorhinolaryngol. 2014;271:607-613. [PubMed] [DOI]|
|32.||Aliakbari I, Noohi S, Safavi SA, Tabrizi AG, Bolfion M, Razaghi M, Goudarzi H, Dabiri H. The role of adenotonsillar tissues as a reservoir for Helicobacter pylori and Helicobacter hepaticus. Gastroenterol Hepatol Bed Bench. 2011;4:153-158. [PubMed]|
|33.||Gharst G, Oyarzabal OA, Hussain SK. Review of current methodologies to isolate and identify Campylobacter spp. from foods. J Microbiol Methods. 2013;95:84-92. [PubMed]|
|34.||Zou QH, Li RQ. Helicobacter pylori in the oral cavity and gastric mucosa: a meta-analysis. J Oral Pathol Med. 2011;40:317-324. [PubMed] [DOI]|
|35.||Nguyen AM, el-Zaatari FA, Graham DY. Helicobacter pylori in the oral cavity. A critical review of the literature. Oral Surg Oral Med Oral Pathol Oral Radiol Endod. 1995;79:705-709. [PubMed]|
|36.||Nguyen AM, Engstrand L, Genta RM, Graham DY, el-Zaatari FA. Detection of Helicobacter pylori in dental plaque by reverse transcription-polymerase chain reaction. J Clin Microbiol. 1993;31:783-787. [PubMed]|
|37.||Rôças IN, Siqueira JF. Searching for Helicobacter pylori and Chlamydia pneumoniae in primary endodontic infections. Eur J Dent. 2012;6:158-162. [PubMed]|
|38.||Correia-Silva Jde F, Neto Victória JM, Guimarães AL, de Sá AR, Gomes CC, de Almeida HC, Gomez RS. Helicobacter pylori in the oral mucosa of patients submitted to allogeneic haematopoietic stem cell transplantation. Braz Oral Res. 2006;20:191-195. [PubMed]|
|39.||Momtaz H, Dabiri H, Souod N, Gholami M. Study of Helicobacter pylori genotype status in cows, sheep, goats and human beings. BMC Gastroenterol. 2014;14:61. [PubMed] [DOI]|
|40.||Jones DM, Elridge J. Gastric campylobacter-like organisms from man (C. pyloridis) compared with GCLO strains from the pig baboon and ferret. Göteborg, Sweden: University of Göteborg 1990; 44.|
|41.||Eaton KA, Morgan DR, Krakowka S. Persistence of Helicobacter pylori in conventionalized piglets. J Infect Dis. 1990;161:1299-1301. [PubMed]|
|42.||Engstrand L, Gustavsson S, Jörgensen A, Schwan A, Scheynius A. Inoculation of barrier-born pigs with Helicobacter pylori: a useful animal model for gastritis type B. Infect Immun. 1990;58:1763-1768. [PubMed]|
|43.||De Groote D, van Doorn LJ, Ducatelle R, Verschuuren A, Haesebrouck F, Quint WG, Jalava K, Vandamme P. ‘Candidatus Helicobacter suis’, a gastric helicobacter from pigs, and its phylogenetic relatedness to other gastrospirilla. Int J Syst Bacteriol. 1999;49 Pt 4:1769-1777. [PubMed]|
|44.||Mégraud F, Broutet N. Review article: have we found the source of Helicobacter pylori? Aliment Pharmacol Ther. 2000;14 Suppl 3:7-12. [PubMed]|
|45.||Handt LK, Fox JG, Dewhirst FE, Fraser GJ, Paster BJ, Yan LL, Rozmiarek H, Rufo R, Stalis IH. Helicobacter pylori isolated from the domestic cat: public health implications. Infect Immun. 1994;62:2367-2374. [PubMed]|