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. 2020 Oct 21;69(5):392–399. doi: 10.1111/idj.12484

Periodontal treatment is more effective in gastric Helicobacter pylori eradication in those patients who maintain good oral hygiene#

Selin Yuksel Sert 1, Ayla Ozturk 1,†,*, Ahmet Bektas 2, Murat I Cengiz 2,‡
PMCID: PMC9379070  PMID: 31038210

Abstract

Objectives: This study aimed to investigate the effect of periodontal treatment and oral hygiene on the eradication of gastric Helicobacter pylori. Materials and methods: In this clinical trial, the 98 patients with gastric H. pylori infection that were enrolled received either triple-therapy regimen only or triple-therapy regimen plus periodontal treatment given during triple therapy. Eradication of H. pylori was checked at 3 months, and then after therapy using the urea breath test. Results: The triple-therapy plus periodontal treatment regime resulted in a 64.7% eradication rate, and the triple-therapy regime alone resulted in a 51.1% eradication rate (P = 0.17). Additionally, subgroup analysis indicated that the beneficial effect of periodontal treatment on the gastric H. pylori eradication rate improved if adequate plaque control was maintained (P = 0.02). Multivariate logistic regression analysis showed that post-treatment oral hygiene status [as indicated by the Oral Hygiene Index (OHI)] was associated with H. pylori eradication (P = 0.02), but not with pretreatment oral hygiene status (P = 0.24). Oral hygiene measures without periodontal treatment appear to have a limited impact on H. pylori eradication. Post-treatment oral hygiene level (OHI ≤ 1.25) had a positive effect on H. pylori eradication, increased the gastric eradication rate, with an OR of 3.19, and the oral H. pylori eradication rate, with an OR of 4.57. Furthermore, if periodontal treatment was unsuccessful in eliminating oral H. pylori, as tested using the Campylobacter-like organism test, the OR for the unsuccessful gastric eradication increased 64-fold. Conclusion: This result illustrates that the key factors for achieving successful gastric H. pylori eradication are professional periodontal treatment and the patients’ later adherence to an oral hygiene regimen.

Key words: Periodontal medicine, Helicobacter infections, rapid urease test, Campylobacter-like organism test, extragastric reservoir

INTRODUCTION

As one of the most common bacterial pathogens in humans, Helicobacter pylori infection affects approximately half of the world’s population1. Primarily residing in the stomach, H. pylori can lead to a variety of gastrointestinal diseases, including chronic gastritis, peptic ulcers, gastric cancers and mucosa-associated lymphoid tissue lymphoma1. Moreover, this type I carcinogen (definite carcinogen)2., 3. is responsible for the second most common type of fatal cancer, gastric cancer, worldwide. Besides gastrointestinal diseases, the bacterium has now been implicated in extragastric diseases, such as iron deficiency anaemia1., 4., vitamin B12 deficiency5, stroke6 and coronary artery disease7.

As with other infectious diseases, systemic antibiotic therapy is employed to eradicate H. pylori. The standard eradication treatment for H. pylori is a 10- to 14-day triple-therapy regimen composed of a proton pump inhibitor (PPI) with two antibiotics (clarithromycin and either amoxicillin or metronidazole)8. Other choices include sequential therapy and quadruple therapy1. However, with the rising resistance of H. pylori to antibiotics, the efficiency of triple-therapy regimens has been challenged9, and drugs are gradually becoming less effective with a failure rate ranging from 10% to 45%10., 11..

Increases in the H. pylori eradication failure rates and the high recurrence rate of infection9., 12. have led researchers to investigate the possible transmission routes of the microorganism, and to identify factors contributing to the recrudescence of this bacterium. Isolation of H. pylori by culture in the dental plaque13 of patients with gastritis drew attention to the fact that the oral cavity may be a secondary reservoir for this bacterium. Many researchers have also reported on the presence of H. pylori in the oral environment and dental plaque using a variety of methods14., 15., 16., 17.. While it is possible to eliminate the bacteria from the stomach with antibiotic treatment, these microorganisms cannot be eliminated from the mouth because of the inability of antibiotics to penetrate the biofilm structure of the dental plaque18; thus, the oral environment becomes the source of focal infection for the recurrence of H. pylori infection. In fact, studies that assessed the effect of systemic H. pylori eradication on oral H. pylori found that although it is effective in gastric eradication, it has little to no effect on oral H. pylori19., 20., 21., 22..

Thus, new strategies are needed to improve the overall H. pylori eradication rates. Therefore, the primary objective of this study was to determine whether periodontal therapy is a useful adjunct to triple therapy to eradicate gastric H. pylori infection. The secondary objective was to assess the effect of clinical variables on gastric H. pylori eradication, such as Oral Hygiene Index (OHI), clinical attachment levels (CALs), and bleeding on probing (BOP).

MATERIALS AND METHODS

From 2008 to 2011, patients who required H. pylori eradication therapy at the Department of Gastroenterology, Faculty of Medicine, OMU were enrolled in the clinical study (Figure 1). The nature and procedures of the study were explained to the patients, and written informed consent was obtained from all of the study participants. This study was approved by the Research Ethics Committee at Ondokuz Mayıs University (OMU Etik 2009/95), and the study was conducted in accordance with the principles of the Helsinki Declaration.

Figure 1.

Figure 1.

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Study design.

The presence of H. pylori was confirmed by histological examination with immunostaining and through the rapid urease test, also known as the Campylobacter-like organism (CLO) test, on gastric biopsy specimens obtained during gastrointestinal endoscopy. The presence of H. pylori in dental plaque was scanned using the CLO test. Plaque samples were collected from tooth surfaces with a sterile periodontal curette. They were then instantly impregnated into CLO test gel. Results were checked at 10 minutes, 30 minutes and 1 hour23., 24.. Only patients who tested positive for H. pylori in both the gastric biopsy specimens and the dental plaque samples were included in this study. Patients who had undergone treatment with antibiotics, PPIs, H2 blockers and bismuth derivatives within 6 months before the clinical protocol, as well as those that had undergone previous eradication therapy or previous periodontal therapy, or orthodontic therapy were excluded from the study. Subjects with diabetes, HIV-infection and autoimmune diseases or who were edentulous or pregnant or smokers were also excluded.

Clinical periodontal examination

Clinical and radiographic examinations were performed for each patient. Diagnosis and classification of chronic periodontitis were performed based on the 1999 American Academy of Periodontology classification criteria25. Subjects with radiographic evidence of alveolar bone loss and at least two interproximal sites with attachment loss ≥ 3 mm, not on the same tooth, were entered into the chronic periodontitis group. Subjects without a history of periodontitis and no sites with a CAL26, probing depth (PD) > 3 mm and the presence of BOP were diagnosed with gingivitis. All clinical parameters were evaluated by one calibrated investigator (S.Y.S.). Ten patients, not related to the study with varying degrees of periodontal disease, were used to calibrate the examiner. The examiner evaluated the subjects on two occasions 1 week apart. Calibration was validated if 90% of the recordings could be reproduced within a 1.0-mm difference. Patients were given a thorough clinical examination, including determination of periodontal PD, CAL, mobility, gingival index (GI)27, plaque index (PI)28, BOP, and simplified OHI29.

Treatment regimens

Patients were allocated to one of the eradication regimens: triple therapy only or triple therapy combined with periodontal treatment. The allocation to a treatment group was based on which day of the week they presented for examination to reduce selection bias in treatment assignment. The triple therapy consisted of a 10-day course of a PPI combined with amoxicillin (2 × 1 g daily) and clarithromycin (2 × 500 mg daily). Periodontal therapy involved scaling and, or combined with root planing and oral hygiene instructions on brushing with the modified Bass technique. The follow-up was done by a 14C-urea breath test at least 12 weeks after completion of treatment. A 14C urea breath test analyser (HUBT-20; Headway, Guangdong, China) was employed to diagnose H. pylori infection. Periodontal therapy for the control group was offered and performed at the end of the study, after monitoring for 3 months.

Outcome measures

The primary outcome measure of the study was the eradication of gastric H. pylori infection, and secondary outcomes were periodontal parameters, including PD, CAL, OHI, PI, GI, BOP and oral H. pylori infection.

Statistical analysis

Statistical analysis was performed with SPSS software version 16.0 (SPSS, Chicago, IL, USA). The χ2 test was used to analyse the eradication rate of gastric H. pylori. If the case number in one group was below 5, Fisher’s exact test was used and corrected for multiple comparisons. Individual data groups were tested for normality (Kolmogorov–Smirnov test). The paired t-test was used to compare pre- and post-treatment differences in continuous variables with normal distribution, and the Mann–Whitney test for non-parametric data (presence of pocket greater than 4 mm). The diagnostic abilities of OHI were assessed by receiver operating characteristic (ROC) curve analysis. To identify potential risk factors for gastric and oral H. pylori eradication, a univariate analysis was conducted. Variables with P < 0.2 in the univariate analysis or established risk factors such as age and gender were further analysed by performing multivariate analysis. The current study was designed to detect medium effect size differences (25%) between treatment groups with a power of 80% at 5% significance level.

RESULTS

Study population characteristics

Initially, 120 patients were recruited for this study (Figure 1). Of these, 22 participants dropped out because they did not attend follow-up appointments. The distribution of patients with respect to gender (P = 0.07) and age (P = 0.27) was not significantly different for the study groups. The subject cohort comprised 24 (47.1%) females in the combined therapy group and 31 (65.9%) in the triple therapy-only group. The mean age of the combined therapy group was 50.88 ± 12.9 years, and that of the triple-therapy group was 46.32 ± 11.9 years. The combined group comprised of 6 (11%) gingivitis patients, and the triple therapy-only group comprised of 8 (17%) gingivitis patients (P = 0.46). Table 1 displays the periodontal variables of the study groups.

Table 1.

Comparison of periodontal variables at baseline between treatment groups

Periodontal parameters Combined therapy (n = 51) Triple therapy only (n = 47) P-value
OHI 1.95 ± 1.34 2.50 ± 1.70 0.08
PI 1.33 ± 0.81 1.53 ± 0.92 0.25
GI 1.53 ± 0.74 1.83 ± 0.83 0.06
Clinical PD 2.36 ± 0.53 2.57 ± 1.02 0.21
CAL 2.76 ± 1.08 2.74 ± 1.07 0.93
Periodontal status [gingivitis n (%)] 6 (11%) 8 (17%) 0.46
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CAL, clinical attachment level; GI, gingival index; OHI, Oral Hygiene Index; PD, probing depth; PI, plaque index.

Gastric Helicobacter pylori eradication

At least 3 months after completion of gastric H. pylori eradication therapy, the13C-UBT test showed that 33 (64.71%) of the 51 combined therapy group subjects were negative for gastric H. pylori, whereas 24 (51.06%) of the 47 triple-therapy patients were negative. The difference between the treatment groups was not statistically significant (P = 0.17; Table 2).

Table 2.

(a) Comparison of gastric Helicobacter pylori eradication rates between treatment groups; (b) comparison of gastric H. pylori eradication rates based on oral hygiene status after periodontal treatment

(a) Gastric H. pylori negative(−) n Gastric H. pylori positive(+) n Percent eradication n P-value
Triple therapy with periodontal treatment 33 18 64.71% 51 0.17
Triple therapy only 24 23 51.06% 47
(b) OR (95% CI; P-value)
Good OHI Perio triple 30 9 76.92%
3.19 (1.25–8.17; P = 0.02)
3.73 (1.37–10.16; P = 0.01)†
Triple therapy only 24 23 51.06%
3.13 (0.75–13.03; P = 0.12)
2.73 (0.64–11.66; P = 0.17)†
Poor OHI Perio triple 3 9 25%
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CI, confidence interval; n, number.

‘Good OHI’: “OHI ≤ 1.25”.

†

Age- and sex-adjusted odds ratio (OR).OHI, Oral Hygiene Index.

P < 0.05 (in bold)

A multiple logistic regression analysis showed that H. pylori eradication was associated with post-treatment OHI (P = 0.023), but none of the other tested variables [pre-treatment OHI (P = 0.24), the post-treatment levels of PI (P = 0.13), GI (P = 0.13), BOP (P = 0.87), CAL (P = 0.51) and PD (P = 0.78), a pocket greater than 4 mm (P = 0.44)] displayed a significant statistical association with the treatment outcome. The mean OHI for the successful group was lower than that of patients with an unsuccessful outcome [gastric H. pylori (+) patient; 0.68 vs. 1.17, respectively; P = 0.023]. Controlling for the effects of other potential confounding factors such as age and gender did not seem to influence our results (P = 0.024).

The discriminative ability of the OHI was further tested via ROC and area under the curve (AUC) analyses. We used ROC analysis to identify the optimal cut-off points that maximise the probability of correct classification, using OHI as a continuous variable in detecting possible differences between successful and unsuccessful therapy. As shown in Figure 2, this analysis revealed that the post-treatment OHI predicted treatment outcome (P < 0.0001). The AUC associated with the OHI was 0.73 ± 0.05 [95% confidence interval (CI): 0.628, 0.837; P < 0.0001]. At a cut-off value of 1.25 for OHI, the sensitivity was 71.4% and specificity 62.8% for discriminating the outcome.

Figure 2.

Figure 2.

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The area under the receiver operating characteristic (ROC) curve associated with Oral Hygiene Index (OHI) was 0.73 ± 0.05 [95% confidence interval (CI): 0.628-0.837; P = 0 < 0.0001]. At cut-off values of 1.25 for OHI, sensitivity was 71.4% and specificity was 62.8%.

Based on this reference cut-off point, our analysis showed that, when the patient achieved optimum oral hygiene levels (OHI ≤ 1.25), the odds of having successful gastric H. pylori eradication were 3.19 (95% CI: 1.25–8.17; P = 0.02) times greater than the odds of having an unsuccessful outcome (adjusted OR: 3.73; 95% CI: 1.37–10.16; P = 0.01; Table 2b).

Effect of oral hygiene status on oral Helicobacter pylori eradication rate

Similar to gastric H. pylori, based on the same reference cut-off point, our results showed that poor oral hygiene was associated with a 4.57-fold (95% CI: 1.13–18.47; P = 0.02) increase in the odds of unsuccessful oral H. pylori treatment. The adjustment for age and sex did not alter this association (Table 3a).

Table 3.

(a) Oral Helicobacter pylori eradication rates based on oral hygiene status; (b) gastric H. pylori eradication rates based on the persistence of oral H. pylori after periodontal treatment

(a) Oral H. pylori (−) n Oral H. pylori (+) n Percent eradication OR(95% CI; P-value)
Optimal OH (OHI ≤ 1.25) 32 7 82.05% 4.57 (95% CI: 1.13–18.47; P = 0.02)
4.30 (95% CI: 1.04–17.76; P < 0.04)†
Poor OH 6 6 50%
(b) Gastric H. pylori (−)
n 		Gastric H. pylori (+)
n 		Percent eradication OR (95% CI; P-value)
Oral H. pylori (−)† 32 6 84.21% 64.00 (95% CI: 6.96–588.4; P < 0.0001)
Oral H. pylori (+)† 1 12 7.69% 72.62 (95% CI: 7.19–733.6; P = 0.0002)†
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†

Presence of oral H. pylori tested by CLO test. OHI, Oral Hygiene Index, Green and Vermillion (1964).29

Effect of periodontal therapy outcome on oral Helicobacter pylori eradication rate

The eradication rate of the combined therapy group was 74.5%. Within the combined treatment group, the gastric eradication rate was higher when oral eradication was successful (P < 0.0001). The odds of having a successful gastric H. pylori eradication outcome for oral H. pylori-negative cases was 64 times (95% CI: 6.96–588.4; P < 0.0001; Table 3b) greater than the odds of having a successful gastric H. pylori eradication outcome for oral H. pylori-positive cases. Indeed, only one subject of the 13 with oral H. pylori had gastric H. pylori eradication (Table 3b). Adjustment for potential confounders, including gender and age, yielded similar findings (OR: 72.62; 95% CI: 7.19–733.6; P = 0.0002).

DISCUSSION

The goal of this investigation was to assess the effect of non-surgical periodontal therapy and oral hygiene status on gastric H. pylori eradication. Our results showed that 64.71% of patients who subjected to both systemic triple therapy and periodontal therapy displayed gastric eradication compared with 51.06% of patients who were subjected to systemic triple therapy only. Although there was improvement in the clinical outcome of the combined therapy group, the difference was not statistically significant (Table 2a). A detailed analysis of the data revealed that the greatest decrease in gastric H. pylori was seen in patients who maintained good oral hygiene after receiving combined triple and periodontal therapy (Table 2b). If oral hygiene had deteriorated after periodontal treatment, the contribution of such treatment to conventional triple treatment was reduced.

Moreover, patients who had undergone successful eradication therapy had better oral hygiene status (mean OHI = 0.68) compared with those who had failed eradication therapy (mean OHI = 1.17). In our study, while the baseline oral hygiene status was not associated with H. pylori eradication, maintenance of good oral hygiene after periodontal treatment improved gastric H. pylori eradication with odds of 3.19. While oral hygiene measures are indispensable to periodontal treatment, hygiene measures alone have a limited effect on established periodontitis30. To the best of our knowledge, no study has assessed the influence of oral hygiene in the success of periodontal therapy on H. pylori eradication outcomes. These results illustrate that the beneficial effect of periodontal treatment on the gastric H. pylori eradication rate is improved if adequate plaque control is maintained.

Initially, the difference in the success of H. pylori eradication between the two treatment groups in our study was 13.65%. The practice of good oral hygiene further increased the difference between the test and control groups to 25.86%. These results suggest that the key factor in achieving successful gastric H. pylori eradication outcomes is not only professional periodontal treatment, but also patients’ later adherence to the oral hygiene regimen.

This observation is in agreement with results from previous studies31., 32., 33., which have shown that the effects of non-surgical periodontal treatment are short-lived in the absence of oral hygiene, as evidenced by the quick repopulation of subgingival sites with potential periodontal pathogens after treatment. Furthermore, classical clinical studies on oral health34., 35., 36. have demonstrated that the key to success in periodontal treatment is maintaining a high standard of oral hygiene. Indeed, earlier clinical trials were designed to meet stringent OHI rules to obtain higher gastric H. pylori eradication rates37., 38.. The rules are to exclude subjects who do not maintain good oral hygiene37 or to provide frequent (twice a month) periodontal treatment to compensate for poor oral hygiene38.

Several studies have examined the effect of periodontal therapy on gastric H. pylori eradication. However, none of these assessed the effect of oral hygiene status after periodontal treatment. Initial support for the potential benefit of periodontal therapy in gastric H. pylori eradication comes from Zaric et al39. A concurrent study by Jia et al. (2009)37 reinforced the role of periodontal therapy as an adjunct in gastric H. pylori eradication. Most of the relevant studies37., 38., 39., 40. supported the contribution of periodontal treatment to the success of H. pylori eradication, and two meta-analyses41., 42. gave further credence to the association.

In our study, the difference in H. pylori eradication success between the treatment groups was lower (13% difference) compared with previous studies (ranging from 17% to 63%). This could be because a majority of our study population consisted of patients with lower dental awareness who only seek treatment when a problem arises. This poor dental awareness was reflected in their poor performance in oral hygiene practices, which in turn affected periodontal treatment outcomes.

In the current study, the cut-off criterion for oral hygiene status that could best predict gastric H. pylori eradication outcome was determined using ROC curve analysis. This analysis revealed that the OHI of 1.25 appears to be a valid target for achieving successful H. pylori eradication (Figure 2). In our study, poor oral hygiene was associated with a 3.19-fold increase in the odds of unsuccessful gastric H. pylori eradication (Table 2b) and a 4.57-fold increase in the odds of unsuccessful oral H. pylori treatment (Table 3a).

Furthermore, our study revealed that the eradication of H. pylori from the oral cavity improved eradication from the stomach (Table 3b). Dental plaque is a natural reservoir of H. pylori13, which could account for the frequent relapses after gastric eradication therapy. Our results showed that failure of eradication of H. pylori from dental plaque (tested by CLO test) increased the odds of gastric failure almost 64-fold (Table 3b). Therefore, screening patients for H. pylori in the dental plaque may offer the clinician a cue about the outcome of eradication therapy, and may help to decrease the appearance of antibiotic resistance and reduce costs by eliminating a source of reinfection. This result is consistent with previous reports demonstrating that patients who showed eradication of oral H. pylori also showed eradication of the gastric organism39., 40..

Although systemic therapy was successful in gastric H. pylori eradication, bacteria present in dental plaque is protected from systemic antibiotic treatment by the nature of the biofilm. It can be removed efficiently only by professional and daily oral hygiene procedures22. If it is not removed mechanically, it is a potential source of reinfection of the stomach.

The strength of our study is that the follow-up for gastric H. pylori infection was conducted via a 14C urea breath test analyser, which allowed for an automated, unbiased assessment of infection status to be evaluated. On the other hand, the oral H. pylori assessment was provided by the dentist who carried out the clinical examination and thus knew the treatment groups. Nonetheless, as expected, the oral H. pylori and the gastric H. pylori eradication rates were highly correlated, suggesting that the non-blind assessment of oral H. pylori was not biased. Another limitation is that some patients in the control group did not return for follow-up dental re-evaluation and periodontal treatment. Therefore, we have limited information on the oral H. pylori compared with the gastric H. pylori results in the systemic triple therapy-only group.

A further limitation was that the sample size in the subgroup analysis for examining the effect of oral hygiene on oral H. pylori eradication was small; therefore, caution is needed in the interpretation of this finding. However, this result was consistent with the other findings that show the positive effect of oral hygiene on oral H. pylori eradication and in turn the positive effect of oral hygiene on the gastric H. pylori eradication. In addition, multiple logistic regression analysis revealed that post-treatment OHI levels were a strong predictor of H. pylori eradication. The consistency of these findings further supports this association. In addition, these results are clinically plausible.

In view of our findings, we suggest that combining mechanical periodontal treatment with systemic triple therapy could enhance the success of gastric eradication. Additionally, maintaining good oral hygiene and controlling dental plaque are essential to gastric H. pylori eradication. Therefore, coordination between a dental professional and a gastroenterologist may be helpful in improving outcomes. Furthermore, our results suggest that utilisation of the CLO test for screening dental plaque-associated H. pylori may give physicians and dentists a cue regarding the outcome of periodontal therapy in eliminating oral H. pylori, and thus may increase the success of systemic gastric eradication therapy.

Acknowledgements

The authors thank Prof. Dr Soner Çankaya, Biostatistics Department, School of Medicine, Ordu University, for statistical support. This investigation is supported by the Scientific Research Foundation of Ondokuz Mayıs University.

Conflicts of interest

The authors report no conflicts of interest related to this study.

References

  • 1.Malfertheiner P, Megraud F, O’Morain C, et al. Management of Helicobacter pylori infection—the Maastricht V/Florence consensus report. Gut. 2017;66:6–30. doi: 10.1136/gutjnl-2016-312288. [DOI] [PubMed] [Google Scholar]
  • 2.Wroblewski LE, Peek RM, Wilson KT. Helicobacter pylori and gastric cancer: factors that modulate disease risk. Clin Microbiol Rev. 2010;23:713–739. doi: 10.1128/CMR.00011-10. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 3.Forman D, Webb P, Parsonnet J. H. pylori and gastric cancer. Lancet. 1994;343:243–244. [PubMed] [Google Scholar]
  • 4.Fong T-L, Dooley CP, Dehesa M, et al. Helicobacter pylori infection in pernicious anemia: a prospective controlled study. Gastroenterology. 1991;100:328–332. doi: 10.1016/0016-5085(91)90199-u. [DOI] [PubMed] [Google Scholar]
  • 5.Kaptan K, Beyan C, Ural AU, et al. Helicobacter pylori–is it a novel causative agent in Vitamin B12 deficiency? Arch Intern Med. 2000;160:1349–1353. doi: 10.1001/archinte.160.9.1349. [DOI] [PubMed] [Google Scholar]
  • 6.Wang ZW, Li Y, Huang LY, et al. Helicobacter pylori infection contributes to high risk of ischemic stroke: evidence from a meta-analysis. J Neurol. 2012;259:2527–2537. doi: 10.1007/s00415-012-6558-7. [DOI] [PubMed] [Google Scholar]
  • 7.Vijayvergiya R, Vadivelu R. Role of Helicobacter pylori infection in pathogenesis of atherosclerosis. World J Cardiol. 2015;7:134. doi: 10.4330/wjc.v7.i3.134. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 8.Chey WD, Wong BC. American College of Gastroenterology guideline on the management of Helicobacter pylori infection. Am J Gastroenterol. 2007;102:1808. doi: 10.1111/j.1572-0241.2007.01393.x. [DOI] [PubMed] [Google Scholar]
  • 9.Vakil N. H. pylori treatment: new wine in old bottles? Am J Gastroenterol. 2009;104:26. doi: 10.1038/ajg.2008.91. [DOI] [PubMed] [Google Scholar]
  • 10.Megraud F. Helicobacter pylori and antibiotic resistance. Gut. 2007;56:1502. doi: 10.1136/gut.2007.132514. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 11.De Francesco V, Giorgio F, Hassan C, et al. Worldwide H. pylori antibiotic resistance: a systematic review. J Gastrointestin Liver Dis. 2010;19:409–414. [PubMed] [Google Scholar]
  • 12.Hsu P-I, Wu D-C, Chen W-C, et al. Randomized controlled trial comparing 7-day triple, 10-day sequential, and 7-day concomitant therapies for Helicobacter pylori infection. Antimicrob Agents Chemother. 2014;58:5936–5942. doi: 10.1128/AAC.02922-14. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 13.Krajden S, Fuksa M, Anderson J, et al. Examination of human stomach biopsies, saliva, and dental plaque for Campylobacter pylori. J Clin Microbiol. 1989;27:1397–1398. doi: 10.1128/jcm.27.6.1397-1398.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 14.Mapstone N, Lynch D, Lewis F, et al. Identification of Helicobacter pylori DNA in the mouths and stomachs of patients with gastritis using PCR. J Clin Pathol. 1993;46:540–543. doi: 10.1136/jcp.46.6.540. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 15.Birek C, Grandhi R, McNeill K, et al. Detection of Helicobacter pylori in oral aphthous ulcers. J Oral Pathol Med. 1999;28:197–203. doi: 10.1111/j.1600-0714.1999.tb02024.x. [DOI] [PubMed] [Google Scholar]
  • 16.Gebara E, Pannuti C, Faria C, et al. Prevalence of Helicobacter pylori detected by polymerase chain reaction in the oral cavity of periodontitis patients. Mol Oral Microbiol. 2004;19:277–280. doi: 10.1111/j.1399-302X.2004.00153.x. [DOI] [PubMed] [Google Scholar]
  • 17.Lauritano D, Cura F, Candotto V, et al. Periodontal pockets as a reservoir of Helicobacter pylori causing relapse of gastric ulcer: a review of the literature. J Biol Regul Homeost Agents. 2015;29:123–126. [PubMed] [Google Scholar]
  • 18.Socransky SS, Haffajee AD. Dental biofilms: difficult therapeutic targets. Periodontology 2000. 2002;28:12–55. doi: 10.1034/j.1600-0757.2002.280102.x. [DOI] [PubMed] [Google Scholar]
  • 19.Miyabayashi H, Furihata K, Shimizu T, et al. Influence of oral Helicobacter pylori on the success of eradication therapy against gastric Helicobacter pylori. Helicobacter. 2000;5:30–37. doi: 10.1046/j.1523-5378.2000.00004.x. [DOI] [PubMed] [Google Scholar]
  • 20.Gebara E, Faria C, Pannuti C, et al. Persistence of Helicobacter pylori in the oral cavity after systemic eradication therapy. J Clin Periodontol. 2006;33:329–333. doi: 10.1111/j.1600-051X.2006.00915.x. [DOI] [PubMed] [Google Scholar]
  • 21.Czesnikiewicz-Guzik M, Loster B, Bielanski W, et al. Implications of oral Helicobacter pylori for the outcome of its gastric eradication therapy. J Clin Gastroenterol. 2007;41:145–151. doi: 10.1097/01.mcg.0000225654.85060.3d. [DOI] [PubMed] [Google Scholar]
  • 22.Czesnikiewicz-Guzik M, Bielanski W, Guzik T, et al. Helicobacter pylori in the oral cavity and its implications for gastric infection, periodontal health, immunology and dyspepsia. J Physiol Pharmacol. 2005;56:77. [PubMed] [Google Scholar]
  • 23.Gurbuz AK, Ozel AM, Yazgan Y, et al. Oral colonization of Helicobacter pylori: risk factors and response to eracizication therapy. South Med J. 2003;96:244–248. doi: 10.1097/01.SMJ.0000051069.50950.2B. [DOI] [PubMed] [Google Scholar]
  • 24.Vaira D, Holton J, Cairns S, et al. Urease tests for Campylobacter pylori: care in interpretation. J Clin Pathol. 1988;41:812. doi: 10.1136/jcp.41.7.812. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 25.Periodontology AAo 1999 International International Workshop for a classification of periodontal diseases and conditions. Papers. Oak Brook, Illinois, October 30-November 2, 1999. Ann Periodontol. 1999;4:1–112. doi: 10.1902/annals.1999.4.1.i. i. [DOI] [PubMed] [Google Scholar]
  • 26.Calvet X, Ramírez Lázaro MJ, Lehours P, et al. Diagnosis and epidemiology of Helicobacter pylori infection. Helicobacter. 2013;18:5–11. doi: 10.1111/hel.12071. [DOI] [PubMed] [Google Scholar]
  • 27.Löe H, Silness J. Periodontal disease in pregnancy I. Prevalence and severity. Acta Odontol Scand. 1963;21:533–551. doi: 10.3109/00016356309011240. [DOI] [PubMed] [Google Scholar]
  • 28.Silness J, Löe H. Periodontal disease in pregnancy II. Correlation between oral hygiene and periodontal condition. Acta Odontol Scand. 1964;22:121–135. doi: 10.3109/00016356408993968. [DOI] [PubMed] [Google Scholar]
  • 29.Greene JG, Vermillion JR. The simplified oral hygiene index. J Am Dent Assoc. 1964;68:7–13. doi: 10.14219/jada.archive.1964.0034. [DOI] [PubMed] [Google Scholar]
  • 30.Westfelt E. Rationale of mechanical plaque control. J Clin Periodontol. 1996;23:263–267. doi: 10.1111/j.1600-051x.1996.tb02086.x. [DOI] [PubMed] [Google Scholar]
  • 31.Magnusson I, Lindhe J, Yoneyama T, et al. Recolonization of a subgingival microbiota following scaling in deep pockets. J Clin Periodontol. 1984;11:193–207. doi: 10.1111/j.1600-051x.1984.tb01323.x. [DOI] [PubMed] [Google Scholar]
  • 32.Sbordone L, Ramaglia L, Gulletta E, et al. Recolonization of the subgingival microflora after scaling and root planing in human periodontitis. J Periodontol. 1990;61:579–584. doi: 10.1902/jop.1990.61.9.579. [DOI] [PubMed] [Google Scholar]
  • 33.Winkelhof A, Velden U, Graaff J. Microbial succession in recolonizing deep periodontal pockets after a single course of supra-and subgingival debridement. J Clin Periodontol. 1988;15:116–122. doi: 10.1111/j.1600-051x.1988.tb01004.x. [DOI] [PubMed] [Google Scholar]
  • 34.Axelsson P, Lindhe J. Effect of controlled oral hygiene procedures on caries and periodontal disease in adults. J Clin Periodontol. 1978;5:133–151. doi: 10.1111/j.1600-051x.1978.tb01914.x. [DOI] [PubMed] [Google Scholar]
  • 35.Axelsson P, Nyström B, Lindhe J. The long-term effect of a plaque control program on tooth mortality, caries and periodontal disease in adults. J Clin Periodontol. 2004;31:749–757. doi: 10.1111/j.1600-051X.2004.00563.x. [DOI] [PubMed] [Google Scholar]
  • 36.Nyman S, Rosling B, Lindhe J. Effect of professional tooth cleaning on healing after periodontal surgery. J Clin Periodontol. 1975;2:80–86. doi: 10.1111/j.1600-051x.1975.tb01728.x. [DOI] [PubMed] [Google Scholar]
  • 37.Jia C-L, Jiang G-S, Li C-H, et al. Effect of dental plaque control on infection of Helicobacter pylori in gastric mucosa. J Periodontol. 2009;80:1606–1609. doi: 10.1902/jop.2009.090029. [DOI] [PubMed] [Google Scholar]
  • 38.Song H-Y, Li Y. Can eradication rate of gastric Helicobacter pylori be improved by killing oral Helicobacter pylori? World J Gastroenterol. 2013;19:6645. doi: 10.3748/wjg.v19.i39.6645. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 39.Zarić S, Bojić B, Janković L, et al. Periodontal therapy improves gastric Helicobacter pylori eradication. J Dent Res. 2009;88:946–950. doi: 10.1177/0022034509344559. [DOI] [PubMed] [Google Scholar]
  • 40.Gao J, Li Y, Wang Q, et al. Correlation between distribution of Helicobacter pylori in oral cavity and chronic stomach conditions. J Huazhong Univ Sci Technolog Med Sci. 2011;31:409–412. doi: 10.1007/s11596-011-0391-6. [DOI] [PubMed] [Google Scholar]
  • 41.Bouziane A, Ahid S, Abouqal R, et al. Effect of periodontal therapy on prevention of gastric Rhizoma Coptidis recurrence: a systematic review and meta-analysis. J Clin Periodontol. 2012;39:1166–1173. doi: 10.1111/jcpe.12015. [DOI] [PubMed] [Google Scholar]
  • 42.Ren Q, Yan X, Zhou Y, et al. Periodontal therapy as adjunctive treatment for gastric Rhizoma Coptidis infection. Cochrane Database Syst Rev. 2016;(2):CD009477. doi: 10.1002/14651858.CD009477.pub2. [DOI] [PMC free article] [PubMed] [Google Scholar]

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