Skip to main content

Advertisement

SpringerLink
Log in

Association between Periodontitis and Diabetes Mellitus in the General Population

  • Research article
  • Published:
Journal of Diabetes & Metabolic Disorders Aims and scope Submit manuscript

Abstract

Purpose-

This study aimed to examine the association between periodontitis and diabetes mellitus.

Methods

Participants with natural teeth in one jaw from the Third United States National Health and Nutrition Examination Survey (1988–1994) were included in this analysis. Participants with moderate (> 4mm attachment loss in ≥ 2 mesial sites or 5mm pocket depth in ≥ 2 mesial sites) or severe (> 6mm attachment loss in ≥ 2 mesial sites and > 5mm pocket depth in ≥ 1 mesial site) periodontitis were classified as having periodontal disease. The rest of the participants were considered without periodontal disease. Diabetes mellitus was defined as fasting glucose ≥ 126mg/dL, hemoglobin A1c ≥ 6.5% or the use of antihyperglycemic medications. Multivariable logistic regression was used to examine the association between periodontitis and diabetes mellitus in all study population and subgroups stratified by demographics and comorbidities.

Results

This analysis included 13,000 participants [mean age 43.8 ± 19.1 years, 47.5% male, 30% whites]. About 12.7% (n = 1,656) of the study population had periodontitis, and 9.2% (n = 1,200) had diabetes. In a multivariable-adjusted model, presence (vs. absence) of periodontitis was associated with 66% increased odds of diabetes (OR (95% CI):1.66 (1.43–1.94); p < 0.001). Compared to those without periodontitis, the odds of diabetes among those with severe periodontitis was much higher (OR (95% CI): 2.31(1.72–3.11); p < 0.001) than in those with moderate periodontitis (OR (95% CI): 1.54(1.30–1.82); p < 0.001).

Conclusions

Periodontitis is associated with prevalent diabetes in a dose-response fashion, suggesting a bidirectional relationship between those two diseases. Patients with periodontal disease should be counseled regarding their elevated risk of diabetes.

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

Similar content being viewed by others

Data Availability

and Codes: The dataset that supports this study are openly available at the National Center for Health Statisticshttps://www.cdc.gov/nchs/nhanes/nh3data.htm.

References

  1. Wild S, Roglic G, Green A, Sicree M, King H. Global prevalence of diabetes. Diabetes Care. 2004;27:1047–53.

    Article  PubMed  Google Scholar 

  2. Vos T, Lim SS, Abbafati C, Abbas KM, Abbasi M, Abbasifard M, Kangevari MA, Abbastabar H, Abd-Allah F, Abdelalim A, Abdollahi M, Abdollahpour I, Abolhassani H, Aboyans V, Abrams EM, Abreu LG, Abrigo MRM, Abu-Raddad LJ, Abushouk AI, Murray CLJ. Global burden of 369 diseases and injuries in 204 countries and territories, 1990–2019: A systematic analysis for the global burden of disease study 2019. Lancet. 2020;396:1204–22.

    Article  Google Scholar 

  3. Kassebaum NJ, Smith AGC, Bernabé E, Fleming TD, Reynolds AE, Vos T, Murray CJL, Marcenes W. GBD 2015 Oral Health Collaborators. Global, Regional, and National Prevalence, Incidence, and Disability-Adjusted Life Years for Oral Conditions for 195 Countries, 1990–2015: A systematic analysis for the global burden of diseases, injuries, and risk factors. J Dent Res. 2017;96[4]:380–7.

    Article  Google Scholar 

  4. Nishimura F, Takahashi K, Kurihara M, Takashiba S, Murayama Y. Periodontal disease as a complication of diabetes mellitus. Ann Periodontol. 1998;3:20–9.

    Article  CAS  PubMed  Google Scholar 

  5. Emrich LJ, Shlossman M, Genco RJ. Periodontal disease in non-insulin-dependent diabetes mellitus. J Periodontol. 1991;62(2):123–31.

    Article  CAS  PubMed  Google Scholar 

  6. Taylor GW, Burt BA, Becker MP, Genco RJ, Shlossman M. Glycemic control and alveolar bone loss progression in type 2 diabetes. Ann Periodontol. 1998;3:30–9.

    Article  CAS  PubMed  Google Scholar 

  7. Taylor GW. Bidirectional interrelationships between diabetes and periodontal diseases: an epidemiologic perspective. Ann Periodontol. 2001;6:99–112.

    Article  CAS  PubMed  Google Scholar 

  8. D’Aiuto F, Parkar M, Andreou G, Suvan J, Brett P, Ready D. & Tonetti M. periodontitis and systemic inflammation: Control of the Local Infection is Associated with a Reduction in Serum Inflammatory Markers. J Dent Res. 2004;83:156–60.

    Article  PubMed  Google Scholar 

  9. Artese HPC, Foz AM, Rabelo MDS, Gomes GH, Orlandi M, Suvan J, D’Aiuto F, Romito GA. Periodontal therapy and systemic inflammation in type 2 diabetes mellitus: A meta-analysis. PLoS ONE. 2015;10: https://doi.org/10.1371/JOURNAL.PONE.0128344.

  10. Esteves Lima RP, Astanzio ARS, Costa FO, Cunha FA, Abreu LG. Impact of non-surgical periodontal treatment on serum TNF-α levels in individuals with type 2 diabetes. A systematic review and meta-analysis. J Evid Based Dent Prac. 2021;21:101546.

    Article  Google Scholar 

  11. Teeuw WJ, Gerdes VEA, Loos BG. Effect of periodontal treatment on glycemic control of diabetic patients: A systematic review and meta-analysis. Diabetes Care. 2010;33:421.

    Article  PubMed  PubMed Central  Google Scholar 

  12. Wang X, Han X, Guo X, Luo X, Wang D. The effect of periodontal treatment on hemoglobin A1c levels of diabetic patients: A systematic review and Meta-Analysis. PLoS ONE. 2014; 9: https://doi.org/10.1371/JOURNAL.PONE.0108412.

  13. Center for Disease Control [n.d.]. National Health and Examination Survey NHANES III [1988–1994], National Center of Health Statistics. Retrieved 4/9/2021 https://wwwn.cdc.gov/nchs/nhanes/nhanes3/default.aspx.

  14. Ricardo AA, Chen J, Hampol H, Garside D, Marucha PP, Lash J. Periodontal disease, chronic kidney disease and mortality: results from the third national health and nutrition examination survey. BMC Nephro. 2015;16:97.

    Article  Google Scholar 

  15. Cecoro G, Annunziata M, Iuorio MT, Nastri L, Guida L. Periodontitis. Low-Grade inflammation and systemic health: A scoping review. Medicina. 2020;56:272.

    Article  PubMed Central  Google Scholar 

  16. Araya AV, Pavez V, Perez C, Gonzalez F, Colombo A, Aguirre A, Schiattino I, Aguillón JC. Ex vivo lipopolysaccharide (LPS)-induced TNF‐alpha, IL‐1beta, IL‐6 and PGE2 secretion in whole blood from type 1 diabetes mellitus patients with or without aggressive periodontitis. Eur Cytokine Netw. 2003;14:128‐33.

    PubMed  Google Scholar 

  17. Pejcic A, Kesic LJ, Milasin J. C-reactive protein as a systemic marker of inflammation in periodontitis. Eur J Clin Microbiol Infect Dis. 2011;30:407–14.

    Article  CAS  PubMed  Google Scholar 

  18. Tunes SR, Freitas MCF, Filho NR. Impact of periodontitis on the diabetes-related inflammatory status. J Can Dent Assoc. 2010;76:a35.

    Google Scholar 

  19. Preshaw PM, Bissett SM. Periodontitis: oral complication of diabetes. Endocrinol Metab Clin North Am. 2013;42:849–67.

    Article  PubMed  Google Scholar 

  20. Chávarry NGVM, Sansone C, Sheiham A. The relationship between diabetes mellitus and destructive periodontal disease: a meta-analysis. Oral Health Prev Dent. 2009;7:107–27.

    PubMed  Google Scholar 

  21. Nascimento GG, Leite FRM, Vestergaard P, Scheutz F, Lopez R. Does diabetes increase the risk of periodontitis? A systematic review and meta-regression analysis of longitudinal prospective studies. Acta diabetol. 2018;55:653–67.

    Article  PubMed  Google Scholar 

  22. Takeda M, Ojima M, Yoshioka H, Inaba H, Kogo M, Shizukuishi S, et al. Relationship of serum advanced glycation end products with deterioration of periodontitis in type 2 diabetes patients. J Periodontol. 2005;77:15–20.

    Article  Google Scholar 

  23. Kalaitzoglou E, Popescu I, Bunn RC, Fowlkes JL, Thrailkill KM. Effects of Type 1 Diabetes on Osteoblasts, Osteocytes, and Osteoclasts. Curr Osteoporos Rep. 2016;14:310–9.

    Article  PubMed  PubMed Central  Google Scholar 

  24. Wu C, Yuan Y, Liu H, Li SS, Zhang B, Chen W, An Z, Chen S, Wu Y, Han B, Li C, Li L. Epidemiologic relationship between periodontitis and type 2 diabetes mellitus. BMC Oral Health. 2020;20:1.

    Article  Google Scholar 

  25. Kocher T, König J, Borgnakke WS, Pink C, Meisel P. Periodontal complications of hyperglycemia/diabetes mellitus: Epidemiologic complexity and clinical challenge. Periodontology 2000. 2018; 78:59–97.

  26. Darling-Fisher CS, Kanjirath PP, Peters MC, Borgnakke WS. Oral Health: An untapped resource in managing glycemic control in diabetes and promoting overall health. J N Pract. 2015;11:889–96.

    Article  Google Scholar 

  27. Eke PI, Thornton-Evans GO, Wei L, Borgnakke WS, Dye BA. Accuracy of NHANES Periodontal Examination Protocols. J Dent Res. 2018;89:1208–13.

    Article  Google Scholar 

  28. National Diabetes Statistics Report. 2020. https://www.cdc.gov/diabetes/pdfs/data/statistics/national-diabetes-statistics-report.pdf.

  29. Madianos PN, Koromantzos PA. An update of the evidence on the potential impact of periodontal therapy on diabetes outcomes. J Clin Periodontol. 2018;45:188–95.

    Article  CAS  PubMed  Google Scholar 

  30. Engebretson SP, Hyman LG, Michalowicz BS, Schoenfeld ER, Gelato MC, Hou W, Seaquist ER, Reddy MS, Lewis CE, Oates TW, Tripathy D, Katancik JA, Orlander PR, Paquette DW, Hanson NQ, Tsai MY. The effect of nonsurgical periodontal therapy on hemoglobin A1c levels in persons with type 2 diabetes and chronic periodontitis: a randomized clinical trial. JAMA. 2013;310:2523–32.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Sgolastra F, Severino M, Pietropaoli D, Gatto R, Monaco A. Effectiveness of periodontal treatment to improve metabolic control in patients with chronic periodontitis and type 2 diabetes: a meta-analysis of randomized clinical trials. J Periodontol. 2013;84:958–73.

    Article  PubMed  Google Scholar 

  32. Teshome A, Yitayeh A. The effect of periodontal therapy on glycemic control and fasting plasma glucose level in type 2 diabetic patients: systematic review and meta-analysis. BMC Oral Health. 2016;30:17:31.

    Google Scholar 

  33. Mauri-Obradors E, Merlos A, Estrugo-Devesa A, Jané-Salas E, López-López J, Viñas M. Benefits of non-surgical periodontal treatment in patients with type 2 diabetes mellitus and chronic periodontitis: A randomized controlled trial. J Clin Periodontol. 2018;45:345–53.

    Article  CAS  PubMed  Google Scholar 

  34. Janket SJ. Scaling and root-planing (SRP) may improve glycemic control and lipid profile in patients with chronic periodontitis (CP) and type 2 diabetes (DM2) in a specific subgroup: a meta-analysis of randomized clinical trials. J Evid Based Dent Pract. 2014;14:31–3.

    Article  PubMed  Google Scholar 

  35. Li Q, Hao S, Fang J, Xie J, Kong XH, Yang JX. Effect of non-surgical periodontal treatment on glycemic control of patients with diabetes: a meta-analysis of randomized controlled trials. Trials. 2015;16:291.

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

Research reported in this publication was supported by the National Center for Advancing Translational Sciences of the National Institutes of Health under Award Number UL1TR001420. The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Institutes of Health.

Funding

Research reported in this publication was supported by the National Center for Advancing Translational Sciences of the National Institutes of Health under Award Number UL1TR001420. The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Institutes of Health.

Author information

Authors and Affiliations

  1. Institute of Global Health and Human Ecology, School of Sciences and Engineering, American University in Cairo, New Cairo, Cairo, Egypt

    Basant M. Mehriz & Mirna A. Atteya

  2. Department of Internal Medicine, Wake Forest School of Medicine, Winston Salem, North Carolina, United States

    Travis M. Skipina

  3. Epidemiological Cardiology Research Center, Department of Internal Medicine, Section on Cardiovascular Medicine, Wake Forest School of Medicine, Winston Salem, North Carolina, United States

    Mohamed A. Mostafa & Elsayed Z. Soliman

Authors
  1. Basant M. Mehriz
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Mirna A. Atteya
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Travis M. Skipina
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Mohamed A. Mostafa
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Elsayed Z. Soliman
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

EZS and TMS were responsible for the study concept; TMS was responsible for statistical analyses; EZS, BMM, TMS, and MAA were responsible for the interpretation of results; BMM and MAA were responsible for drafting the manuscript; EZS and TMS were responsible for review and supervision of the manuscript writing.

Corresponding author

Correspondence to Elsayed Z. Soliman.

Ethics declarations

Conflict of interest

The authors have no relevant financial or non-financial interests to disclose.

Compliance with ethical standards

NHANES-III protocol was approved by the National Center for Health Statistics (NCHS) of the Centers for Disease Control and Prevention (CDC) Research Ethics Review Board, and all participants provided written informed consent.

Additional information

Publisher’s Note

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

Electronic Supplementary Material

Below is the link to the electronic supplementary material.

Supplementary Material 1

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Mehriz, B.M., Atteya, M.A., Skipina, T.M. et al. Association between Periodontitis and Diabetes Mellitus in the General Population. J Diabetes Metab Disord 21, 1249–1254 (2022). https://doi.org/10.1007/s40200-022-01010-6

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s40200-022-01010-6

Keywords

Search

Navigation