Skip to main content

Advertisement

SpringerLink
Log in

Increased risk of periodontitis among patients with Crohn’s disease: a population-based matched-cohort study

  • Original Article
  • Published:
International Journal of Colorectal Disease Aims and scope Submit manuscript

Abstract

Background

Periodontitis is a frequently cited extraintestinal manifestation of Crohn’s disease (CD). Despite a plethora of investigations and a recent meta-analysis linking CD and periodontitis, no study has estimated the risk of periodontitis among CD patients with respect to a comparison group nor has any investigation analyzed the effect of CD-specific medications on the risk of periodontitis. The present cohort study compared CD patients and matched subjects without a history of inflammatory bowel disease (IBD) to estimate the effect of CD and CD-specific pharmaceutical prescriptions on the risk of developing periodontitis by leveraging a population-based dataset in Taiwan.

Methods

We sourced 6657 CD patients and 26,628 comparison subjects without a history of IBD from the Taiwan National Health Insurance Database. Cox proportional hazards regressions were used to estimate the risk of subsequent periodontitis by CD status and pharmaceutical prescription during the follow-up period.

Results

After adjusting for socioeconomic status (SES), urbanicity, selected medical co-morbidities, and CD-specific pharmaceutical prescriptions, the hazard ratio (HR) for subsequent periodontitis among patients with CD was 1.36 (95% CI = 1.25–1.48) that of comparison subjects. There was not a significant difference in risk between genders or across ages. Steroids (95% CI = 0.66–0.77) appeared to confer a protective effect and Aspirin, Plavix, and Licodin were marginally protective (95% CI = 0.76–0.95).

Conclusion

This is the first study to report an increased HR for subsequent periodontitis among CD patients when compared to matched comparison subjects without IBD. The protective effect of some pharmaceuticals may suggest that treatment of CD protects against periodontitis.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

References

  1. Molodecky NA, Soon IS, Rabi DM, Ghali WA, Ferris M, Chernoff G, Benchimol EI, Panaccione R, Ghosh S, Barkema HW, Kaplan GG (2012) Increasing incidence and prevalence of the inflammatory bowel diseases with time, based on systematic review. Gastroenterology 142:46–54.e42

    Article  PubMed  Google Scholar 

  2. Knowles SR, Graff LA, Wilding H et al (2018) Qu ality of life in inflammatory bowel disease: a systematic review and meta-analyses—part I. Inflamm Bowel Dis 19(24):742–751

    Article  Google Scholar 

  3. Everhart JE, Ruhl CE (2009) Burden of digestive diseases in the United States. Part I: overall and upper gastrointestinal diseases. Gastroenterology 136:376–386

    Article  PubMed  Google Scholar 

  4. Jostins L, Ripke S, Weersma RK et al (2012) Host-microbe interactions have shaped the genetic architecture of inflammatory bowel disease. Nature 491:119–124

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  5. Chandan JS, Thomas T et al (2017) The impact of inflammatory bowel disease on oral health. Br Dent J 222:549–553

    Article  PubMed  CAS  Google Scholar 

  6. Williams H, Walker D, Orchard TR (2008) Extraintestinal manifestations of inflammatory bowel disease. Curr Gastroenterol Rep 10:597–605

    Article  PubMed  Google Scholar 

  7. Papageorgiou SN, Hagner M, Nogueira AV et al (2017) Inflammatory bowel disease and oral health: systematic review and a meta-analysis. J Clin Periodontol 44:382–393

    Article  PubMed  Google Scholar 

  8. Brandtzaeg P (2001) Inflammatory bowel disease: clinics and pathology. Do inflammatory bowel disease and periodontal disease have similar immunopathogeneses? Acta Odontol Scand 59:235–243

    Article  PubMed  CAS  Google Scholar 

  9. Kinane DF, Bartold PM (2007) Clinical relevance of the host responses of periodontitis. Periodontology 2000(43):278–293

    Article  Google Scholar 

  10. Indriolo A, Greco S, Ravelli P, Fagiuoli S (2011) What can we learn about biofilm/host interactions from the study of inflammatory bowel disease. J Clin Periodontol 38:36–43

    Article  PubMed  Google Scholar 

  11. Pischon N, Pischon T, Gülmez E et al (2010) Periodontal disease in patients with ankylosing spondylitis. Ann Rheum Dis 69:34–38

    Article  PubMed  CAS  Google Scholar 

  12. Preus HR, Khanifam P, Kolltveit K et al (2010) Periodontitis in psoriasis patients. A blinded, case-controlled study. Acta Odontol Scand 68:165–170

    Article  PubMed  Google Scholar 

  13. Lira-Junior R, Figueredo CM (2016) Periodontal and inflammatory bowel diseases: is there evidence of complex pathogenic interactions? World J Gastroenterol 22:7963–7972

    Article  PubMed  PubMed Central  Google Scholar 

  14. Pihlstrom BL, Michalowicz BS, Johnson NW (2005) Periodontal diseases. Lancet 366:1809–1820

    Article  PubMed  Google Scholar 

  15. Listgarten MA (1986) Pathogenesis of periodontitis. J Clin Periodontol 13:418–430

    Article  PubMed  CAS  Google Scholar 

  16. Vavricka SR, Manser CN, Hediger S et al (2013) Periodontitis and gingivitis in inflammatory bowel disease: a case-control study. Inflamm Bowel Dis 19:2768–2777

    Article  PubMed  Google Scholar 

  17. Keller JJ, Wang J, Hwang YL, Chou CC, Wang LH, Hsu JL, Bai CH, Chiou HY (2015) Increased risk of stroke among patients with Crohn’s disease: a population-based matched cohort study. Int J Color Dis 30:645–653

    Article  Google Scholar 

  18. Keller JJ, Wang J, Huang YL, Chou CC, Wang LH, Hsu JL, Bai CH, Chiou HY (2014) Increased risk of stroke among patients with ulcerative colitis: a population-based matched cohort study. Int J Colorectal Dis Jul 29:805–812

    Article  Google Scholar 

  19. Yu HC, Su NY, Huang JY, Lee SS, Chang YC (2017) Trends in the prevalence of periodontitis in Taiwan from 1997 to 2013: a nationwide population-based retrospective study. Medicine (Baltimore) 96:e8585

    Article  Google Scholar 

  20. Dudeney TP (1969) Crohn’s disease of the mouth. Proc R Soc Med 62:1237

    PubMed  PubMed Central  CAS  Google Scholar 

  21. Ojha J, Cohen DM, Islam NM, Stewart CM, Katz J, Bhattacharyya I (2007) Gingival involvement in Crohn disease. J Am Dent Assoc 138:1574–1181 quiz 1574-181

    Article  PubMed  Google Scholar 

  22. Brito F, de Barros FC, Zaltman C et al (2008) Prevalence of periodontitis and DMFT index in patients with Crohn’s disease and ulcerative colitis. J Clin Periodontol 35:555–560

    Article  PubMed  Google Scholar 

  23. Ruiz-Roca JA, Berini-Aytés L, Gay-Escoda C, Pyostomatitis vegetans (2005) Report of two cases and review of the literature. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 99:447–454

    Article  PubMed  Google Scholar 

  24. Preshaw PM, Alba AL, Herrera D et al (2012) Periodontitis and diabetes: a two-way relationship. Diabetologia 55:21–31

    Article  PubMed  CAS  Google Scholar 

  25. Habashneh RA, Khader YS, Alhumouz MK, Jadallah K, Ajlouni Y (2012) The association between inflammatory bowel disease and periodontitis among Jordanians: a 27 case-control study. J Periodontal Res 47:293–298

    Article  PubMed  CAS  Google Scholar 

  26. Menegat JS, Lira-Junior R, Siqueira MA et al (2016) Cytokine expression in gingival and intestinal tissues of patients with periodontitis and inflammatory bowel disease: an exploratory study. Arch Oral Biol 66:141–146

    Article  PubMed  CAS  Google Scholar 

  27. Figueredo CM, Brito F, Barros FC, Menegat JSB, Pedreira RR, Fischer RG, Gustafsson A (2011) Expression of cytokines in the gingival crevicular fluid and serum from patients with inflammatory bowel disease and untreated chronic periodontitis. J Periodontal Res 46:141–146

    Article  PubMed  CAS  Google Scholar 

  28. Gao H, Hou J, Meng H, Zhang X, Zheng Y, Peng L (2017) Proinflammatory effects and mechanisms of calprotectin on human gingival fibroblasts. J Periodontal Res 52:975–983

    Article  PubMed  CAS  Google Scholar 

  29. Schmidt J, Weigert M, Leuschner C et al (2018) Active Matrixmetalloproteinase-8 and periodontal bacteria—interlink between periodontitis and inflammatory bowel disease? J Periodontol [Epub ahead of print]

  30. Haag L-M, Siegmund B (2015) Intestinal microbiota and the innate immune system—a crosstalk in Crohn’s disease pathogenesis. Front Immunol 6:489

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  31. Boylan MR, Khalili H, Huang ES, Michaud DS, Izard J, Joshipura KJ, Chan AT (2014) A prospective study of periodontal disease and risk of gastric and duodenal ulcer in male health professionals. Clinical and Translational Gastroenterology 5(2):e49

    Article  PubMed  PubMed Central  Google Scholar 

  32. Kaneto C, Toyokawa S, Inoue K, Inoue M, Senba T, Suyama Y, Miyoshi Y, Kobayashi Y (2012) Association between periodontal disease and peptic ulcers among Japanese workers: MY health up study. Glob J Health Sci 4:42–49

    Article  PubMed  PubMed Central  Google Scholar 

  33. Liu Y, Lin H, Bai Y, Qin X, Zheng X, Sun Y, Zhang Y (2008) Study on the relationship between Helicobacter pylori in the dental plaque and the occurrence of dental caries or oral hygiene index. Helicobacter 13:256–260

    Article  PubMed  CAS  Google Scholar 

  34. Riggio MP, Lennon A (1999) Identification by PCR of Helicobacter pylori in subgingival plaque of adult periodontitis patients. J Med Microbiol 48:317–322

    Article  PubMed  CAS  Google Scholar 

  35. Suzuki N, Yoneda M, Naito T, Iwamoto T, Masuo Y, Yamada K, Hisama K, Okada I, Hirofuji T (2008) Detection of Helicobacter pylori DNA in the saliva of patients complaining of halitosis. J Med Microbiol 57:1553–1559

    Article  PubMed  CAS  Google Scholar 

  36. Al Asqah M, Al Hamoudi N, Anil S et al (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

    Article  PubMed  PubMed Central  Google Scholar 

  37. Chen J, He X, Wu L et al (2011) The correlation between oral colonization of Helicobacter pylori and gastrointestinal disease. Hua Xi Kou Qiang Yi XueZaZhi 29:351–354

    Google Scholar 

  38. Liu Y, Yue H, Li A, Wang J, Jiang B, Zhang Y, Bai Y (2009) An epidemiologic study on the correlation between oral Helicobacter pylori and gastric H. pylori. Curr Microbiol 58:449–453

    Article  PubMed  CAS  Google Scholar 

  39. 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 

  40. Zaric S, Bojic B, Lj J et al (2009) Periodontal therapy improves gastric Helicobacter pylori eradication. J Dent Res 88:946–950

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This study is based in part on data from the National Health Insurance Research Database. The authors are grateful to the members of the Research Office for Health Data, Department of Education and Research, Taipei City Hospital, Taiwan for their valuable contributions in data management and statistical analysis.

Author information

Authors and Affiliations

  1. Department of Healthcare Information and Management, Ming Chuan University, Taoyuan, Taiwan

    Ying-Chen Chi & Koyin Chang

  2. Department of Education & Research, Taipei City Hospital, Taipei City, Taiwan

    Ying-Chen Chi & Shu-Yi Lin

  3. Department of Ophthalmology, Kaohsiung Veterans General Hospital, Kaohsiung, Taiwan

    Jiunn-Liang Chen

  4. Department of Optometry, Shu-Zen Junior College of Medicine and Management, Kaohsiung, Taiwan

    Jiunn-Liang Chen

  5. Institute of Public Health and Department of Public Health, National Yang-Ming University, Taipei, Taiwan

    Jiunn-Liang Chen

  6. School of Pharmacy, College of Pharmacy, Taipei Medical University, Taipei, Taiwan

    Li-Hsuan Wang

  7. Department of Pediatrics, Landseed Hospital, Taoyuan, Taiwan

    Chen-Long Wu

  8. Department of Pediatrics, Landseed Hospital, Shanghai, China

    Chen-Long Wu

  9. School of Public Health, College of Medicine, College of Public Health and Nutrition, Taipei Medical University, 250 Wu-Hsing St, Taipei, 110, Taiwan

    Joseph Jordan Keller

  10. International Master’s Program, College of Health Technology, National Taipei University of Nursing and Health Sciences, Taipei, Taiwan

    Joseph Jordan Keller & Chyi-Huey Bai

  11. Department of Public Health, College of Medicine, Taipei Medical University, Taipei, Taiwan

    Chyi-Huey Bai

Authors
  1. Ying-Chen Chi
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jiunn-Liang Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Li-Hsuan Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Koyin Chang
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Chen-Long Wu
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Shu-Yi Lin
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Joseph Jordan Keller
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Chyi-Huey Bai
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Joseph Jordan Keller.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Chi, YC., Chen, JL., Wang, LH. et al. Increased risk of periodontitis among patients with Crohn’s disease: a population-based matched-cohort study. Int J Colorectal Dis 33, 1437–1444 (2018). https://doi.org/10.1007/s00384-018-3117-4

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00384-018-3117-4

Keywords

Search

Navigation