Skip to main content

Advertisement

Log in

Periodontal disease and Helicobacter pylori infection in oral cavity: a meta-analysis of 2727 participants mainly based on Asian studies

  • Review
  • Published:
Clinical Oral Investigations Aims and scope Submit manuscript

Abstract

Objectives

To assess the association between periodontal disease and Helicobacter pylori (H. pylori) infection in oral cavity.

Materials and methods

We searched PubMed, Embase, Web of Science, Cochrane library, Gray literature, and clinicaltrials.gov for eligible studies up to September 25, 2019. Odds ratios (ORs) and 95% confidence intervals (CIs) were calculated. The random-effects model was used with the software STATA 13.0. The Newcastle-Ottawa-Scale was used for quality evaluation.

Results

Twelve observational studies (eight from Asia, one from Europe, and three from the South America) involving 2727 participants were included in the meta-analysis. The overall pooled results showed that H. pylori infection in oral cavity was associated with periodontal disease (OR 2.53, 95% CI 1.86–3.44, P < 0.05). No significant heterogeneity among the articles was observed (I2 = 44.3%, P < 0.05). The sensitivity analysis indicated that the result of our meta-analysis was generally stable. The Begg test and the Egger test both showed no publication bias was observed (P = 0.45 and P = 0.18 respectively).

Conclusions

Based on current available evidence, it seemed there was a correlation between oral H. pylori infection and the occurrence of periodontal disease. However, since most of the data comes from Asia, more large-scale investigations with high quality from all over the world are needed to confirm the association.

Clinical relevance

H. pylori infection in oral may have a positive association with the prevalence of periodontal disease mainly in Asian populations.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  1. Pihlstrom BL, Michalowicz BS, Johnson NW (2005) Periodontal diseases. Lancet 366:1809–1820. https://doi.org/10.1016/S0140-6736(05)67728-8

    Article  PubMed  Google Scholar 

  2. Babay N, Alshehri F, Al Rowis R (2019) Majors highlights of the new 2017 classification of periodontal and peri-implant diseases and conditions. Saudi Dent J 31:303–305. https://doi.org/10.1016/j.sdentj.2019.04.006

    Article  PubMed  PubMed Central  Google Scholar 

  3. Hegde R, Awan KH (2019) Effects of periodontal disease on systemic health. Disease-a-Month 65:185–192. https://doi.org/10.1016/j.disamonth.2018.09.011

    Article  PubMed  Google Scholar 

  4. Lafon A, Pereira B, Dufour T, Rigouby V, Giroud M, Béjot Y, Tubert-Jeannin S (2014) Periodontal disease and stroke: a meta-analysis of cohort studies. Eur J Neurol 21:1155–1167. https://doi.org/10.1067/moe.2003.107

    Article  PubMed  Google Scholar 

  5. Zeng X-T, Deng A-P, Cheng L, Xia L-Y, Niu Y-M, Leng W-D (2013) Periodontal disease and risk of head and neck cancer: a meta-analysis of observational studies. PLoS One 8:e79017. https://doi.org/10.1371/journal.pone.0079017

    Article  PubMed  PubMed Central  Google Scholar 

  6. Zahedi L, Jafari E, Parizi MT, Shafieipour S, Abbasi MHB, Moghadam SD, Zahedi MJ (2017) The association between oral hygiene and gastric pathology in patients with dyspepsia: a cross-sectional study in Southeast Iran. Middle East J Dig Dis 9:33–38. https://doi.org/10.15171/mejdd.2016.49

    Article  PubMed  PubMed Central  Google Scholar 

  7. Slots J (2010) Bacterial specificity in adult periodontitis. A summary of recent work. J Clin Periodontol 13:912–917. https://doi.org/10.1111/1600-051X.ep13487220

    Article  Google Scholar 

  8. Salama NR, Hartung ML, Müller A (2013) Life in the human stomach: persistence strategies of the bacterial pathogen Helicobacter pylori. Nat Rev Microbiol 11:385–399. https://doi.org/10.1038/nrmicro3016

    Article  PubMed  PubMed Central  Google Scholar 

  9. Wroblewski LE, Peek RM, Wilson KT (2010) Helicobacter pylori and gastric cancer: factors that modulate disease risk. Clin Microbiol Rev 23:713–739

    Article  PubMed  PubMed Central  Google Scholar 

  10. Correa P (1992) Human gastric carcinogenesis: a multistep and multifactorial process. First American Cancer Society award lecture on cancer epidemiology and prevention. Cancer Res 52:6735–6740

    PubMed  Google Scholar 

  11. Yu HC, Chen TP, Wei CY (2018) Association between peptic ulcer disease and periodontitis: a nationwide population-based case-control study in Taiwan. Int J Environ Res Public Health 15:912. https://doi.org/10.3390/ijerph15050912

    Article  PubMed Central  Google Scholar 

  12. Bouziane A, Ahid S, Abouqal R, Ennibi O (2012) Effect of periodontal therapy on prevention of gastric Helicobacter pylori recurrence: a systematic review and meta-analysis. J Clin Periodontol 39:1166–1173. https://doi.org/10.1111/jcpe.12015

    Article  PubMed  Google Scholar 

  13. Krajden S, Fuksa M, Anderson J, Kempston J, Boccia A, Petrea C, Babida C, Karmali M, Penner JL (1989) Examination of human stomach biopsies, saliva, and dental plaque for campylobacter pylori. J Clin Microbiol 27:1397–1398

    Article  PubMed  PubMed Central  Google Scholar 

  14. Al Sayed A, Anand PS, Kamath KP, Patil S, Preethanath RS, Anil S (2014) Oral cavity as an extragastric reservoir of helicobacter pylori. Isrn Gastroenterol 2014:261369–261316. https://doi.org/10.1155/2014/261369

    Article  PubMed  PubMed Central  Google Scholar 

  15. Gao J, Li Y, Wang Q, Qi C, Zhu S (2011) Correlation between distribution of Helicobacter pylori in oral cavity and chronic stomach conditions. J Huazhong Univ Sci Technol Med Sci 31:409–412

    Article  Google Scholar 

  16. Al Asqah M, Al Hamoudi N, Anil S, Al Jebreen A, Al-Hamoudi WK (2009) Is the presence of Helicobacter pylori in dental plaque of patients with chronic periodontitis a risk factor for gastric infection? Can J Gastroenterol 23:177–179. https://doi.org/10.1155/2009/950527

    Article  PubMed  PubMed Central  Google Scholar 

  17. Veerman EC, Bank CM, Namavar F, Appelmelk BJ, Bolscher JG, Nieuw Amerongen AV (1997) Sulfated glycans on oral mucin as receptors for Helicobacter pylori. Glycobiology 7:737–743. https://doi.org/10.1093/glycob/7.6.737

    Article  PubMed  Google Scholar 

  18. Fritscher AM, Cherubini K, Chies J, Dias AC (2004) Association between Helicobacter pylori and recurrent aphthous stomatitis in children and adolescents. J Oral Pathol Med 33:129–132. https://doi.org/10.1111/j.0904-2512.2004.00074.x

    Article  PubMed  Google Scholar 

  19. Alm RA, Bina J, Andrews BM, Doig P, Hancock REW, Trust TJ (2000) Comparative genomics of Helicobacter pylori: analysis of the outer membrane protein families. Infect Immun 68:4155–4168. https://doi.org/10.1128/IAI.68.7.4155-4168.2000

    Article  PubMed  PubMed Central  Google Scholar 

  20. Zou QH, Li RQ (2011) Helicobacter pylori in the oral cavity and gastric mucosa: a meta-analysis. J Oral Pathol Med 40:317–324. https://doi.org/10.1111/j.1600-0714.2011.01006.x

    Article  PubMed  Google Scholar 

  21. Nisha KJ, Nandakumar K, Shenoy KT, Janam P (2016) Periodontal disease and Helicobacter pylori infection: a community-based study using serology and rapid urease test. J Investig Clin Dent 7:37–45

    Article  PubMed  Google Scholar 

  22. Riggio MP, Lennon A (1999) Identification by PCR of Helicobacter pylori in subgingival plaque of adult periodontitis patients. J Med Microbiol 48:317–322. https://doi.org/10.1099/00222615-48-3-317

    Article  PubMed  Google Scholar 

  23. Umeda M, Kobayashi H, Takeuchi Y, Hayashi J, Morotome-Hayashi Y, Yano K, Aoki A, Ohkusa T, Ishikawa I (2003) High prevalence of Helicobacter pylori detected by PCR in the oral cavities of periodontitis patients. J Periodontol 74:129–134. https://doi.org/10.1902/jop.2003_74_1_129

    Article  PubMed  Google Scholar 

  24. Valadan Tahbaz S, Yadegar A, Amirmozafari N, Yaghoobee S, Ehsaniardekani MJ, Zojaji H (2017) Occurrence of Helicobacter pylori and its major virulence genotypes in dental plaque samples of patients with chronic periodontitis in Iran. Gastroenterol Hepatol Bed Bench 10:S70–S78

    PubMed  PubMed Central  Google Scholar 

  25. Moher D, Liberati A, Tetzlaff J, Altman DG, The PRISMA Group (2009) Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. Int J Surg 8:336–341. https://doi.org/10.1016/j.ijsu.2010.02.007

    Article  Google Scholar 

  26. Stroup DF, Berlin JA, Morton SC, Olkin I, Williamson GD, Rennie D, Moher D, Becker BJ, Sipe TA, Thacker SB (2000) Meta-analysis of observational studies in epidemiology: a proposal for reporting. J Am Med Assoc 283:2008–2012

    Article  Google Scholar 

  27. Armitage GC (2000) Development of a classification system for periodontal diseases and conditions. Northwest Dent 79:31–35

    PubMed  Google Scholar 

  28. Higgins JPT, Thomas J, Chandler J, Cumpston M, Li T, Page MJ, Welch VA (editors) (2019) Cochrane handbook for systematic reviews of interventions version 6.0 (updated July 2019). Cochrane, Available from https://training.cochrane.org/handbook/current

  29. Stang A (2010) Critical evaluation of the Newcastle-Ottawa scale for assessing the quality of nonrandomized studies in meta-analyses. Eur J Epidemiol 25:603–605. https://doi.org/10.1007/s10654-010-9491-z

    Article  PubMed  Google Scholar 

  30. De Souza GM, De Oliveira DWD, Lages FS, Fernandes IA, Falci SGM (2018) Relationship between bariatric surgery and periodontal status: a systematic review and meta-analysis. Surg Obes Relat Dis 14:1205–1216. https://doi.org/10.1016/j.soard.2018.04.018

    Article  Google Scholar 

  31. Higgins JPT, Thompson SG (2002) Quantifying heterogeneity in a meta-analysis. Stat Med 21:1539–1558

    Article  PubMed  Google Scholar 

  32. Souto R, Colombo AP (2008) Detection of Helicobacter pylori by polymerase chain reaction in the subgingival biofilm and saliva of non-dyspeptic periodontal patients. J Periodontol 79:97–103

    Article  PubMed  Google Scholar 

  33. Silva DG, Stevens RH, Macedo JMB, Albano RM, Falabella MEV, Fischer RG, Veerman EC, Tinoco EM (2010) Presence of Helicobacter pylori in supragingival dental plaque of individuals with periodontal disease and upper gastric diseases. Arch Oral Biol 55:896–901

    Article  PubMed  Google Scholar 

  34. Medina ML, Medina MG, Martin GT, Picón SO, Merino LA (2010) Molecular detection of Helicobacter pylori in oral samples from patients suffering digestive pathologies. Med Oral Patol Oral Cir Bucal 15:e38–e42. https://doi.org/10.4317/medoral.15.e38

    Article  PubMed  Google Scholar 

  35. Salehi MR, Shah Aboei MS, Naghsh N, Hajisadeghi S, Ajami E (2013) A comparison in prevalence of Helicobacter pylori in the gingival crevicular fluid from subjects with periodontitis and healthy individuals using polymerase chain reaction. J Dent Res Dental Clin Dent Prospect 7:238–243. https://doi.org/10.5681/joddd.2013.038

    Article  Google Scholar 

  36. Ding Y-J, Yan T-L, Hu X-L, Liu J-H, Yu C-H, Li Y-M, Wang Q-Y (2015) Association of salivary Helicobacter pylori infection with oral diseases: a cross-sectional study in a Chinese population. Int J Med Sci 12:742–747. https://doi.org/10.7150/ijms.11050

    Article  PubMed  PubMed Central  Google Scholar 

  37. Zheng P, Zhou W (2015) Relation between periodontitis and Helicobacter pylori infection. Int J Clin Exp Med 8:16741–16744

    PubMed  PubMed Central  Google Scholar 

  38. Yang J, Zhang Q, Chen M, Wu WZ, Tan HB (2016) Association between Helicobacter pylori infection and risk of periodontal diseases in Han Chinese: a case-control study. Med Sci Monit 22:121–126. https://doi.org/10.12659/MSM.894583

    Article  PubMed  PubMed Central  Google Scholar 

  39. Ximénez-Fyvie LA, Haffajee AD, Som S, Thompson M, Torresyap G, Socransky SS (2000) The effect of repeated professional supragingival plaque removal on the composition of the supra - and subgingival microbiota. J Clin Periodontol 27:637–647. https://doi.org/10.1034/j.1600-051x.2000.027009637.x

    Article  PubMed  Google Scholar 

  40. Xime’nez-Fyvie LA, Haffajee AD, Socransky SS (2000) Comparison of the microbiota of supra- and subgingival plaque in health and periodontitis. J Clin Periodontol 27:648–657. https://doi.org/10.1034/j.1600-051x.2000.027009648.x

    Article  Google Scholar 

  41. Genco RJ (1998) Periodontal diseases: pathogenesis and microbial factors. J Am Dent Assoc 129:58S–62S. https://doi.org/10.1016/S0002-8177(15)30088-X

    Article  Google Scholar 

  42. Hu Z, Zhang Y, Li Z, Yu Y, Kang W, Han Y, Geng X, Ge S, Sun Y (2016) Effect of Helicobacter pylori infection on chronic periodontitis by the change of microecology and inflammation. Oncotarget 7:66700–66712. https://doi.org/10.18632/oncotarget.11449

    Article  PubMed  PubMed Central  Google Scholar 

  43. Nanbara H, Wara-aswapati N, Nagasawa T, Yoshida Y, Yashiro R, Bando Y, Kobayashi H, Khongcharoensuk J, Hormdee D, Pitiphat W, Boch JA, Izumi Y (2012) Modulation of Wnt5a expression by periodontopathic bacteria. PLoS One 7:e34434. https://doi.org/10.1371/journal.pone.0034434

    Article  PubMed  PubMed Central  Google Scholar 

  44. Ferreira RM, Pinto-Ribeiro I, Wen X, Marcos-Pinto R, Dinis-Ribeiro M, Carneiro F, Figueiredo C (2016) Helicobacter pylori cagA promoter region sequences influence CagA expression and interleukin 8 secretion. J Infect Dis 213:669–673

    Article  PubMed  Google Scholar 

  45. Reti KL, Tymensen LD, Davis SP, Amrein MW, Buret AG (2015) Campylobacter jejuni increases flagellar expression and adhesion of noninvasive Escherichia coli: effects on enterocytic toll-like receptor 4 and CXCL-8 expression. Infect Immun 83:4571–4581. https://doi.org/10.1128/IAI.00970-15

    Article  PubMed  PubMed Central  Google Scholar 

  46. Chen Z, Cai J, Chen YM, Wei J, Chen XL (2019) A meta-analysis of the association between the presence of Helicobacter pylori and periodontal diseases. Medicine 98:e15922. https://doi.org/10.1097/MD.0000000000015922

    Article  PubMed  PubMed Central  Google Scholar 

  47. Anand PS, Nandakumar K, Shenoy KT (2006) Are dental plaque, poor oral hygiene, and periodontal disease associated with Helicobacter pylori infection? J Periodontol 77:692–698

    Article  PubMed  Google Scholar 

  48. Dye BA, Kruszon-Moran D, McQuillan G (2002) The relationship between periodontal disease attributes and Helicobacter pylori infection among adults in the United States. Am J Public Health 92:1809–1815

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Funding

This study was supported by grants from Provincial Natural Science Foundation of Liaoning, China (201800506).

Author information

Authors and Affiliations

Authors

Contributions

Yanqing Liu and Rong Li contributed to the study selection and drafting the article. Yuxiao Luo and Qin Dong identified eligible studies for possible inclusion in the meta-analysis. Xiaomeng Xue and Tong Xu contributed to the data extraction. Junchao Liu and Jingbo Liu contributed to the literature quality assessment. Yaping Pan and Dongmei Zhang contributed to resolving disagreements and critically revising the manuscript. All authors have read and approved the final article.

Corresponding author

Correspondence to Dongmei Zhang.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

This article does not contain any studies with human participants or animals performed by any of the authors.

Informed consent

For this type of study, formal consent is not required.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Liu, Y., Li, R., Xue, X. et al. Periodontal disease and Helicobacter pylori infection in oral cavity: a meta-analysis of 2727 participants mainly based on Asian studies. Clin Oral Invest 24, 2175–2188 (2020). https://doi.org/10.1007/s00784-020-03330-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00784-020-03330-4

Keywords

Navigation