International Scholarly Research Notices

International Scholarly Research Notices / 2014 / Article

Review Article | Open Access

Volume 2014 |Article ID 261369 | 16 pages | https://doi.org/10.1155/2014/261369

Oral Cavity as an Extragastric Reservoir of Helicobacter pylori

Academic Editor: T. Tsukamoto
Received11 Nov 2013
Accepted24 Dec 2013
Published20 Feb 2014

Abstract

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.

1. Introduction

Helicobacter pylori (H. pylori) is one of the most common bacterial infections in humans [1]. The presence of the organism H. pylori (initially termed Campylobacter pyloridis) in the antral mucosa of humans was first reported in 1983 [2]. 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 [5]. Besides gastrointestinal diseases, recent data seems to suggest a possible association of this microorganism with other conditions such as anemia [6], altered serum levels of lipoproteins [7], and coronary atherosclerosis [8]. 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 [11]. 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 [12] and cats [13], 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 [1618]. 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 [19]. One of the suggested mechanisms of reinfection is the possible recolonization from the dental plaque [20]. 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 14 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.


No.Author(s)YearSample sizePrevalence of
H. pylori

1 Assumpção et al. [48]201099 adult patients who underwent upper gastrointestinal endoscopy52%
2Al Asqah et al. [35] 2009Sixty-two dyspeptic patients with periodontitis and 39 dyspeptic patients without periodontitisOverall-65%; 79% in periodontitis group and 43% in nonperiodontitis group
3Anand et al. [38]2006Sixty-five dyspeptic patients with H. pylori infection (cases) and 69 dyspeptic patients without H. pylori infection (control)Overall-79.9%; 89% among cases and 71% among controls
4Chitsazi et al. [23]200688 dyspeptic patients-44 with H. pylori infection and 44 without H. Pylori infectionOverall 18.2%; 36.4% in HP positive group
5Choudhury et al. [22]2003124 patients with dyspepsia43%
6 Gürbüz et al. [30]200375 dyspeptic patients91.7%
7Suk et al. [45] 2002Sixty-five patients with dyspeptic symptoms 100%
8Avcu et al. [21]2001241 H. pylori positive patients with gastric histologic changes44.8%
9 Özdemir et al. [49]200181 dyspeptic patients79%
10Qureshi et al. [50]199960 dyspeptic patients50%
11Contractor et al. [51]1998100 healthy subjects81%


No.AuthorsYearTarget geneSample sizePrevalence of H. pylori

1Momtaz et al. [52]2012ureC, cagA, and vacA300 patients with gastroduodenal diseasesNone of the plaque samples showed presence of H. pylori
2Agarwal and Jithendra [31]201216S rRNA30 H. pylori positive and 20 H. pylori negative patientsOverall-42%; in H. pylori positive group-60%; in H. pylori negative group-15%.
3Bago et al. [41]201116S rDNA56 patients with chronic periodontitis and gastric H. pylori positive37.5%
4Chaudhry et al. [53]201116srRNA and 860 bp DNA region89 dyspeptic patients reporting for endoscopy51.6% for both genes; 62.9% for 16srRNA; 61% for 860 bp DNA region and 73% if either of the 2 regions are considered
5Gao et al. [44]2011ureC and cagA genes96 patients with H. pylori infection82.3%
6Wichelhaus et al. [54]2011860bp DNA11 orthodontic patients36%
7 Assumpção et al. [48]2010vacA and cagA99 adult patients who underwent upper gastrointestinal endoscopy72% samples were positive for H. pylori. 63 of 71 positive dental plaque samples were positive for vacA and cagA. 58/71 were positive for cagA while vacA genotypes had a prevalence ranging from 13–59%
8Rasmussen et al. [55]2010Genomic DNA78 dyspeptic patients47.4%
9Eskandari et al. [56]201016S rRNA67 patients with chronic periodontitis-23 with H. pylori positive gastritis5.97%
10 Silva et al. [57]2010vacA and 16S rDNA30 dyspeptic patients20% by 16S rDNA and 6.7% by vacA
11Silva et al. [58]201016S rRNA115 patients11.3%
12Silva et al. [59]200916s ribosomal and cagA genes32 with H. pylori positive with gastric disease and 32 with H. pylori positive with no gastric disease Overall-17.7%. Among cases, H. pylori DNA detected in 36.6% and cagA gene detected in 3 out of 11 (27.3%) samples. In control group 0%
13 Gonçalves
et al. [60]
2009JW22 and JW23 primers/16S rRNA23, HIV seropositive individuals of whom 13 with chronic periodontitis and 10 with periodontally healthy and 31 HIV seronegative individuals of whom 17 had chronic periodontitis and 14 were periodontally healthyNot specified
14Liu et al. [61]2009860 bp fragment443 dyspeptic patients59.4%
15 Bürgers et al. [36]200816S rDNA94 patients who underwent upper gastrointestinal endoscopy5.4%
16Liu et al. [62]2008860 bp fragment214 children58.9%
17Teoman et al. [25]2007Urease A67 dyspeptic patients28.3%
18Olivier et al. [63]2006urease AB gene; phosphoglucosamine
mutase (glmM) gene; and 860 bp DNA region
74 healthy members of a rural community0
19Kignel et al. [64]200516S rRNA49 dyspeptic patients2%
20Fritscher et al. [65]2004860 bp fragment53 patients with recurrent aphthous stomatitis and 52 patients without RASOverall-3.8%; 5.7% in cases and 1.9% among controls
21Gebara et al. [66]200416S rDNA30 dentate patients with gingivitis/periodontitis and H. pylori infection20% in supra-gingival plaque and 26.6% in subgingival plaque
22Umeda et al. [37]200316S rRNA56 dental patients25%
23Goosen et al. [67]2002
24Berroteran et al. [39]2002Urease genes32 dyspeptic patients and 20 asymptomatic controlsOverall-28.9%; 37.5% among dyspeptic patients and 15% among controls
25Suk et al. [45] 2002cagASixty-five patients with dyspeptic symptoms 43.1%
26Miyabayashi et al. [43]2000ureA47 patients with chronic gastritis or peptic ulcer38.3%
27Song et al. [68]2000860 bp fragmentForty-two patients who underwent upper gastrointestinal endoscopyOverall 97% (82% in molar region, 64% in premolar region and 59% in incisor region)
28Song et al. [69]2000860 bp fragment20 dyspeptic patientsNot specified
29Song et al. [70]2000860 bp fragment21 patients100%
30Song et al. [71]1999Urease A, 16S rRNA, and 860 bp fragment40 dental patients
31Dowsett et al. [18]1999Not specified
32Oshowo et al. [32]199816S rRNA208 dyspeptic patients-116 H. pylori positive and 92 H. pylori negativeOverall 6.25% all in H. pylori positive
33Hardo et al. [24]199516S rRNA62 dyspeptic patients1.6%
34Mapstone et al. [72]199316S rRNA21 dyspeptic patients-13 with H. pylori associated gastritis and 8 who had normal histologyOverall-9.5%; 15.4% in gastritis group and 0 in histologically normal group-overall prevalence-9.5%
35Nguyen et al. [73]199316S rRNA25 dyspeptic patientsOverall 28% all in H. pylori positive; among H. pylori positive individuals 38.8%.


No.AuthorsYearSample sizePrevalence of
H. pylori

1Agarwal and Jithendra [31]201230 H. pylori positive and 20 H. pylori negative patientsOverall-18%; in H. pylori positive group-30%; in H. pylori negative group-0
2Loster et al. [74]2009Forty six dentists without known co-morbidities48%
3Teoman et al. [25]200767 dyspeptic patients0
4Czesnikiewicz-Guzik et al. [75]2005100 female patients48.3%
5 Cze nikiewicz-Guzik et al. [33]2004100 female patients48.3%
6Umeda et al. [37]200318 dental patients5.6%
7Goosen et al. [67]200258 clinically healthy volunteers13.8% of which only 5.2% were positive in PCR analysis
8Checchi et al. [28]200035 patients from a Periodontology clinic8.6%
9Oshowo et al. [32]1998208 dyspeptic patients-116 H. pylori positive and 92 H. pylori negativeOverall 1% all in H. pylori positive
10Hardo et al. [24]199562 dyspeptic patients0
11Krajden et al. [16]198971 patients undergoing endoscopy1.4%


No.AuthorsYearSample sizePrevalence of H. pylori

1Namiot et al. [26]2010155 patients65.6%
2Leszczyńska et al. [27]2009164 dyspeptic patients referred for endoscopy-95 H. pylori infected and 69 noninfected82.1% in H. pylori positive subjects and 17.7% in H. pylori negative subjects
3Checchi et al. [28]200035 patients from a Periodontology clinic11%
4Savoldi et al. [29]199880 dyspeptic patients0


No.AuthorsYearMethod used to detect H. pylori Sample sizePrevalence of coinfection of H. pylori

1Agarwal and Jithendra [31]2012PCR-16S rRNA30 H. pylori positive and 20 H. pylori negative patientsOverall-36%; in H. pylori positive group-60%
2Agarwal and Jithendra [31]2012Culture30 H. pylori positive and 20 H. pylori patientsOverall-18%; in H. pylori positive group-30%
3Bago et al. [41]2011PCR-16S rDNA56 patients with chronic periodontitis and gastric H. pylori positive37.5%
4Silva et al. [58]2010PCR-16S rRNA115 patientsOverall-8.7%; among H. pylori positive group-14.93%
5Eskandari et al. [56]2010PCR-16S rRNA67 patients with chronic periodontitis-23 with H. pylori positive gastritisOverall-5.97%; among H. pylori positive group-17.39%
6Al Asqah et al. [35]2009RUT62 dyspeptic patients with periodontitis and 39 dyspeptic patients without periodontitisOverall-32.7%; 66% among H. pylori positive patients
7Liu et al. [61]2009PCR-860-bp fragment443 dyspeptic patientsOverall-42.7%; among H. pylori positive subjects-69.2% (75.5% in 18–29 years; 61.7% in 30–39 years; 79.7% in 40–49 years; 76.6% in ≥50 years)
8Leszczyńska
et al. [27]
2009EIA164 dyspeptic patients referred for endoscopy-95 H. pylori positive and 69 noninfectedOverall-47.6%; 82.1% in H. pylori positive
9Silva et al. [59]2009PCR-16s ribosomal and cagA genes30 with H. pylori positive with gastric disease and 32 with H. pylori positive with no gastric diseaseOverall-17.7%. Among cases, H. pylori DNA detected in 36.6%, and cagA gene detected in 3 out of 11 samples. In control group-0%
10Bürgers et al. [36]2008PCR-16S rDNA94 patients who underwent upper gastrointestinal endoscopyOverall-1.1% 3.5% of H. pylori positive subjects
11Teoman et al. [25]2007PCR-Urease A67 dyspeptic patientsOverall-25.4%; among H. pylori positive group-36.2%
12Anand et al. [38]2006RUTSixty-five dyspeptic patients with H. pylori infection and 69 dyspeptic patients without H. pylori infection Overall-43.3%; 89.2% among cases
13 Chitsazi et al. [23]2006RUT88 dyspeptic patients-44 with H. pylori infection and 44 without H. pylori infectionOverall 34.1%; 36.4% in H. pylori positive group
14Agüloğlu et al. [76]2006CLO test468 patients who were H. pylori positive by CLO test25.2%
15Agüloğlu et al. [76]2006EIA318 patients who were H. pylori positive by EIA23.6%
16Agüloğlu et al. [76]2006Culture295 patients who were H. pylori positive by culture14.6%
17Czesnikiewicz-Guzik et al. [75]2005Culture100 female patients6.9%
18 Kignel et al. [64]2005PCR-16S rRNA49 dyspeptic patients2% of the total population and 5% of H. pylori positive subjects
19Umeda et al. [37]2003PCR-16S rRNA56 dental patientsOverall-14.3%; among H. pylori positive group-28.6%.
20 Gürbüz et al. [30]2003RUT75 dyspeptic patientsOverall-81.3%; among H. pylori positive subjects-93.9%
21Berroteran et al. [39]2002PCR-Urease genes32 dyspeptic patients and 20 asymptomatic controlsOverall-13.5%; 58% among dyspeptic patients
22Suk et al. [45] 2002PCR-cagA65 patients with dyspeptic symptoms Overall-43.1%, 73.7% among H. pylori positive patients
23Suk et al. [45] 2002RUT65 patients with dyspeptic symptoms Overall-58.5%, 100% among H. pylori positive patients
24Özdemir et al. [49]2001CLO test81 dyspeptic patientsOverall-64.2%; among H. pylori positive group-82.5%.
25Song et al. [70]2000PCR-860-bp fragment21 patientsOverall-47.6%; among H. pylori positive group-100%
26Qureshi et al. [50]1999CLO test60 dyspeptic patientsOverall 33.3%; in H. pylori positive 55.6%
27Oshowo et al. [32]1998PCR-16S rRNA and culture208 dyspeptic patients-116 H. pylori positive and 92 H. pylori negativeBy PCR-Overall 6.25%; in H. pylori positive-11.2%
By culture-Overall 1%; in H. pylori positive-1.7% By both methods-Overall 7.2% in H. pylori positive-12.9%.
28Hardo et al. [24]199516S rRNA62 dyspeptic patients0
29Mapstone et al. [72]1993PCR-16S rRNA21 dyspeptic patients-13 with H. pylori associated gastritis and 8 who had normal histology15.4% in gastritis group-overall prevalence 9.5%
30 Nguyen et al. [73]1993PCR-16S rRNA25 dyspeptic patientsOverall 28%, among H. pylori positive individuals 38.8%
31Krajden et al. [16]1989Culture71 patients undergoing endoscopy1.4% of the total population and 3.5% of H. pylori positive subjects


No.AuthorsYearDefinition of gingival/periodontal diseaseSample sizeAssociation with oral H. pylori Association with gastric H. pylori

1Silva et al. [58]2010At least 4 teeth with PD ≥ 5 mm and CAL > 3 mm115 dyspeptic patientsSignificant Not evaluated
2Namiot et al. [26]2010Russell’s periodontal index155 dyspeptic patientsNonsignificantNot evaluated
3Gonçalves et al. [60]2009At least 3 sites with PD ≥ 5 mm and/or CAL ≥ 4 mm and BOP23 HIV seropositive patients of whom 13 had periodontitis and 10 were periodontally healthy; 31 HIV seronegative patients of 17 had periodontitis and 14 were periodontally healthySignificant
4Al Asqah et al. [35]2009BOP + PD ≥ 3 mm on at least 4 teethDyspeptic patients-62 patients with periodontitis and 39 without periodontitisSignificantSignificant
5Liu et al. [61]2009Gingival index443 dyspeptic patientsSignificant Not evaluated
6Zaric et al. [40]2009Mean PD, CAL, and gingival index scores66 dyspeptic patients with H. pylori infection of gastric mucosaSignificant for mean PD and CAL; not significant for gingival index scoresNot evaluated
7Bürgers et al. [36]2008Periodontal Screening Index 94 dyspeptic patientsNonsignificantNonsignificant
8Namiot et al. [77]2007Russell’s periodontal index137 H. pylori positive patients with peptic ulcerOutcome variable was efficacy of HP eradicationNonsignificant (outcome variable was efficacy of H. pylori eradication)
9Anand et al. [38]2006Patients with one or more sites with a PD ≥ 3 mm and CAL ≥ 3 mm at the same siteSixty-five dyspeptic patients with H. Pylori infection and 69 dyspeptic patients without H. pylori infectionNot evaluatedNonsignificant
10Gebara et al. [66]2004Gingivitis group-patients with PD ≤ 3 mm and BOP on at least 4 sites; periodontitis group-BOP + PD ≥ 5 mm on at least 4 teeth15 gingivitis and 15 periodontitis patients-All were H. pylori positive in antral mucosaNonsignificant
11Umeda et al. [37]2003Presence of periodontal pockets ≥ 4 mm28 patients who harbored H. pylori in stomach/duodenumSignificant Not evaluated
12Choudhury et al. [22]2003CPI124 dyspeptic patientsSignificantNot evaluated
13Dye et al. [34]2002Presence of 1 dental site with PD ≥ 5 mmData from 4504 participants of NHANES III SurveyNot evaluatedSignificant
14Berroteran et al. [39]2002Gingival index-scoring 0–332 dyspeptic patients and 20 asymptomatic controlsNonsignificantNonsignificant
15Dowsett et al. [18]1999Full mouth periodontal examination242 subjectsNonsignificantNonsignificant
16Savoldi et al. [29]1998Gingival index80 dyspeptic patientsNonsignificant-None of the plaque samples were positive for HPNonsignificant
17Hardo et al. [24]1995CPITN62 dyspeptic patientsNonsignificantNonsignificant
18Nguyen et al. [73]1993Gingival index25 dyspeptic patientsNonsignificantNonsignificant


No.AuthorsYearMethod used to detect H. pylori Sample sizePrevalence of H. pylori Prevalence after anti-H. pylori therapyEffect on H. pylori infection

1Gao et al. [44]2011PCR-ureC and cagA genes80 patients with H. pylori infection-37 treated with anti-H. pylori therapy and 43 treated with anti-H. pylori therapy and periodontal therapy After 4 weeks-29.7% in gp A and 4.7% in gp B; after 1 year-43.2% in gp A and 18.6% in gp BEradication rate of gastric H. pylori. After 4 weeks-73% in gp A and 81.4% in gp B
After 1 year-32.4% in gp A and 62.8% in gp B
2Bago et al. [41]2011PCR-16S rDNA56 patients with chronic periodontitis and gastric H. pylori positive37.5% ( )0Eradication rate in stomach was 76.2%
3Zaric et al. [40]2009PCR44 patients: 21 patients positive for H. pylori in subgingival dental plaque and gastric mucosa and 23 patients who were positive for H. pylori only in gastric mucosa-all 44 received only for H. pylori (triple) therapyIn G+O+t-66.7% In the G+O+t group, only 47.6%
showed eradication of gastric H. pylori compared to 87.4% in G+Ot
4Gebara et al. [42]2006PCR-16S rDNA30 dentate patients with gingivitis/periodontitis and H. pylori infection who received anti-H. pylori therapy20% ( ) in supra-gingival plaque and 26.6% ( ) in sub-gingival plaque30% in supra-gingival plaque and 46.7% in sub-gingival plaque
5Gürbüz et al. [30]2003CLO test75 dyspeptic patients of which 61 were H. pylori positive and also had H. pylori in dental plaque90.7% ( ); 81.3% ( ) had co-infection100%
6Suk et al. [45] 2002PCR-cagASixty-five patients with dyspeptic symptoms Overall-43.1% ( ), 73.7% (28/38) among H. pylori positive patients92.9%
7Butt et al. [46]2001Smear cytology82 patients positive for H. pylori in dental plaque: 27 received only anti-H. pylori therapy (gp 1); 25 received anti-HP therapy + periodontal therapy (gp 2); 30 received only periodontal therapy (gp 3)100%100% in gp 1; 16% in gp 2; 10% in gp 3
8Miyabayashi et al. [43]2000PCR-ureA47 patients with chronic gastritis or peptic ulcer-48.9% ( ) were positive for oral HP and 38.3% ( ) had HP in plaqueOral prevalence at 4 weeks-31.9 At 4 weeks-91.6% of subjects negative for oral H. pylori were successfully eradicated of HP infection compared to 52.2% in oral H. pylori positive patients. At 2 years-95.8% of subjects negative for oral H. pylori were successfully eradicated of H. pylori infection compared to 69.5% in oral H. pylori positive patients


No.AuthorsYearMethod used to detect H. pylori Sample sizePrevalence of H. pylori Prevalence after anti-H. pylori therapyEffect on H. pylori infection

1Gao et al. [44]2011PCR-ureC and cagA genes80 patients with H. pylori infection-37 treated with anti-HP therapy (gp A) and 43 treated with anti-H. pylori therapy and periodontal therapy (gp B)After 4 weeks-29.7% in gp A and 4.7% in gp B; after 1 year-43.2% in gp A and 18.6% in gp BEradication rate of gastric H. pylori. After 4 weeks-73% in gp A and 81.4% in gp B, After 1 year-32.4% in gp A and 62.8% in gp B
2Zaric et al. [40]2009PCR43 patients positive for H. pylori in sub gingival dental plaque and gastric mucosa: 21 received only anti-H. pylori triple therapy (G+O+t); 22 received anti-H. pylori triple therapy + periodontal therapy (G+O+tp)In G+O+t-66.7%; in G+O+tp-27.3% In the G+O+tp group, 77.3% showed eradication of gastric H. pylori compared to 47.6% in G+O+t. H. pylori eradication in the stomach and the oral cavity coincided—that is, all 16 of the individuals negative for oral H. pylori were also negative for gastric H. pylori. Five of the participants positive for oral samples were positive for gastric H. pylori as well.
3Jia et al. [47]2009107 dyspeptic patients-56 received dental plaque control (test) and 51 did not (control)Prevalence of H. pylori in gastric mucosa was 19.64% in test group and 84.31% in control group
4Butt et al. [46]2001Smear cytology82 patients positive for H. pylori in dental plaque: 27 received only anti-H. pylori therapy (gp 1); 25 received anti-H. pylori therapy + periodontal therapy (gp 2); 30 received only periodontal therapy (gp 3)100%100% in gp 1; 16% in gp 2; 10% in gp 3

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 [3]. 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% [21] and 43% [22] while the lowest rate reported was 18.2% [23].

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% [30]. 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, 3133]. 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% [27]. 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. [34] 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. [37] 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 [38]. 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. [39] 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. [18] 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. [35] 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, 4046] 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 [30] urease test was used and in the other [46] smear cytology was used. In their study on 82 H. pylori positive patients, Butt et al. [46] 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. [30] 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. [44] 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. [42], 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. [45] 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. [40] 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. [43] 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. [41], 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. [46] 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. [40] 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. [44], 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. [44] 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. [40] 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. [47], 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.

3. Conclusion

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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Copyright © 2014 Arwa Al Sayed et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.


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