Log in

Temporal sequence of the bidirectional relationship between hyperglycemia and periodontal disease: a community-based study of 5,885 Taiwanese aged 35–44 years (KCIS No. 32)

  • Original Article
  • Published:
Acta Diabetologica Aims and scope Submit manuscript

Abstract

The relationship between hyperglycemia (including diabetes) and periodontal disease (PD) has been noted previously, but its temporal sequence in the same study based on a population-based study has been barely addressed. Our study sought to clarify temporal bidirectional relationships between both diseases among Taiwanese aged 35–44 years. A prospective follow-up cohort study was designed by following over time the two normal cohorts (PD-free or hyperglycemia-free) derived from 5,885 subjects aged 35–44 years who were periodically attending a screening program. We ascertained both incident cases of PD (defined by Community Periodontal Index score ≧ 3) and hyperglycemia [fasting plasma glucose (FPG) ≧100 mg/dL] or type 2 diabetes (FPG ≧ 126 mg/dL) with 5-year follow-up. Cox proportional hazards regression model was used to assess the effect of PD on hyperglycemia and vice versa with adjustment for other confounding factors. Participants with PD presented a 33 % increase in their risk of incident hyperglycemia (including diabetes) [adjusted hazard ratio (aHR) = 1.33 (95 % CI 1.09–1.63)] after controlling for potential confounding factors. Conversely, prediabetes and type 2 diabetes mellitus led to a significant elevated risk for PD [aHR = 1.25 (95 % CI 1.00–1.57) and aHR = 1.95 (95 % CI 1.22–3.13)] after adjustment for other confounding factors. In conclusion, a significant bidirectional relationships was found between hyperglycemia and PD, suggesting that both diseases may share common latent traits and pathways that are worthy of being further elucidated by continuing a long-term follow-up of this cohort.

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

Access this article

Price includes VAT (Germany)

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

Abbreviations

KCIS:

Keelung community-based integrated screening

CPI:

Community Periodontal Index

PD:

Periodontal disease

References

  1. Taylor GW, Burt BA, Becker MP, Genco RJ, Shlossman M, Knowler WC, Pettitt DJ (1996) Severe periodontitis and risk for poor glycemic control in patients with non-insulin-dependent diabetes mellitus. J Periodontal 67(Suppl):1085–1093

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  3. Teeuw WJ, Gerdes VE, Loos BG (2010) Effect of periodontal treatment on glycemic control of diabetic patients: a systematic review and meta-analysis. Diabetes Care 33:421–427

    Article  PubMed Central  PubMed  Google Scholar 

  4. Mealey BL, Rose LF (2008) Diabetes mellitus and inflammatory periodontal diseases. Curr Opin Endocrinol Diabetes Obes 15:135–141

    Article  PubMed  Google Scholar 

  5. Bascones-Martínez A, Arias-Herrera S, Criado-Cámara E, Bascones-Ilundáin J, Bascones-Ilundáin C (2012) Periodontal disease and diabetes. Adv Exp Med 771:76–87

    Google Scholar 

  6. Merchant AT, Pitiphat W (2007) Researching periodontitis: challenges and opportunities. J Clin Periodontol 34:1007–1015

    Article  PubMed  Google Scholar 

  7. Seymour GJ, Ford PJ, Cullinan MP, Leishman S, Yamazaki K (2007) Relationship between periodontal infections and systemic disease. Clin Microbiol Infect 13(Suppl):3–10

    Article  CAS  PubMed  Google Scholar 

  8. Preshaw PM, Foster N, Taylor JJ (2007) Cross-susceptibility between periodontal disease and type 2 diabetes mellitus: an immunobiological perspective. Periodontol 2000 45:138–157

    Article  PubMed  Google Scholar 

  9. Demmer RT, Desvarieux M, Holtfreter B, Jacobs DR Jr, Wallaschofski H, Nauck M, Völzke H, Kocher T (2010) Periodontal status and A1C change: longitudinal results from the study of health in Pomerania (SHIP). Diabetes Care 33:1037–1043

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  10. Arora N, Papapanou PN, Rosenbaum M, Jacobs DR Jr, Desvarieux M, Demmer RT (2014) Periodontal infection, impaired fasting glucose and impaired glucose tolerance: results from the continuous national health and nutrition examination survey 2009–2010. J Clin Periodontol. doi:10.1111/jcpe.12258

    PubMed  Google Scholar 

  11. Demmer RT, Squillaro A, Papapanou PN, Rosenbaum M, Friedewald WT, Jacobs DR Jr, Desvarieux M (2012) Periodontal infection, systemic inflammation, and insulin resistance: results from the continuous National Health and Nutrition Examination Survey (NHANES) 1999–2004. Diabetes Care 35:2235–2242

    Article  PubMed Central  PubMed  Google Scholar 

  12. Borgnakke WS, Ylöstalo PV, Taylor GW, Genco RJ (2013) Effect of periodontal disease on diabetes: systematic review of epidemiologic observational evidence. J Clin Periodontol 40(Suppl):S135–S152

    PubMed  Google Scholar 

  13. Chen THH, Chiu YH, Luh DL, Taiwan Community-Based Integrated Screening Group et al (2004) Community-Based Integrated Screening Group Community-based multiple screening model: design, implementation, and analysis of 42,387 participants. Cancer 100:1734–1743

    Article  PubMed  Google Scholar 

  14. Wang PE, Wang TT, Chiu YH, Yen AM, Chen THH (2006) Evolution of multiple disease screening in Keelung: a model for community involvement in health interventions? J Med Screen 13(Suppl 1):S54–S58

    PubMed  Google Scholar 

  15. Chiu YH, Chen LS, Chan CC, Liou DM, Wu SC, Kuo HS, Chang HJ, Chen TH (2006) Health information system for community, based multiple screening in Keelung, Taiwan (Keelung Community based Integrated Screening No 3). Int J Med Inform 75:369–383

    Article  PubMed  Google Scholar 

  16. Chiu YH, Wu SC, Tseng CD, Yen MF, Chen THH (2006) Progression of pre, hypertension, stage 1 and 2 hypertension (JNC 7): a population, based study in Keelung, Taiwan (Keelung Community, based Integrated Screening No 9). J Hypertens 24:821–828

    Article  CAS  PubMed  Google Scholar 

  17. Lai H, Lo MT, Wang PE, Wang TT, Chen TH, Wu GH (2007) A community-based epidemiological study of periodontal disease in Keelung, Taiwan: a model from Keelung community-based integrated screening programme (KCIS No 18). J Clin Periodontol 34:851–859

    Article  PubMed  Google Scholar 

  18. American Diabetes Association (2008) Diagnosis and classification of diabetes mellitus. Diabetes Care 31(Suppl):s55–s60

    Article  Google Scholar 

  19. Wang TT, Chen TH, Wang PE, Lai H, Lo MT, Chen PY, Chiu SY (2009) A population-based study on the association between type 2 diabetes and periodontal disease in 12,123 middle-aged Taiwanese (KCIS No 21). J Clin Periodontol 36:372–379

    Article  PubMed  Google Scholar 

  20. Expert Panel on Detection, Evaluation, and Treatment of High Blood Cholesterol in Adults (2001) Executive Summary of The Third Report of The National Cholesterol Education Program (NCEP) Expert Panel on Detection, Evaluation, And Treatment of High Blood Cholesterol In Adults (Adult Treatment Panel III). JAMA 285:2486–97

  21. World Health Organization (2000) Obesity: preventing and managing the global epidemic. World Health Organization, Geneva

    Google Scholar 

  22. Demmer RT, Jacobs DR Jr, Desvarieux M (2008) Periodontal disease and incident type 2 diabetes mellitus: results from the first National Health and Nutrition Examination Survey and its epidemiologic follow-up study. Diabetes Care 31:1373–1379

    Article  PubMed Central  PubMed  Google Scholar 

  23. Ide R, Hoshuyama T, Wilson D, Takahashi K, Higashi T (2011) Periodontal disease and incident diabetes: a seven-year study. J Dent Res 90:41–46

    Article  CAS  PubMed  Google Scholar 

  24. Pontes Andersen CC, Flyvbjergc A, Buschard K, Holmstrup P (2007) Periodontitis is associated with aggravation of prediabetes in Zucker fatty rats. J Periodontol 78:559–565

    Article  PubMed  Google Scholar 

  25. Chapple IL, Genco R (2013) Working group 2 of joint EFP/AAP workshop. Diabetes and periodontal diseases: consensus report of the Joint EFP/AAP Workshop on Periodontitis and Systemic Diseases. J Clin Periodontol 40(Suppl):S106–S112

    PubMed  Google Scholar 

  26. Taylor JJ, Preshaw PM, Lalla E (2013) A review of the evidence for pathogenic mechanisms that may link periodontitis and diabetes. J Clin Periodontol 40(Suppl):S113–S134

    PubMed  Google Scholar 

  27. Lakschevitz F, Aboodi G, Tenenbaum H, Glogauer M (2011) Diabetes and periodontal diseases: interplay and links. Curr Diabetes Rev 7:433–439

    Article  PubMed  Google Scholar 

  28. Preshaw PM, Alba AL, Herrera D, Jepsen S, Konstantinidis A, Makrilakis K, Taylor R (2012) Periodontitis and diabetes: a two-way relationship. Diabetologia 55:21–31

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  29. Taylor GW, Borgnakk WS (2008) Periodontal disease: associations with diabetes, glycemic control and complications. Oral Dis 14:191–203

    Article  CAS  PubMed  Google Scholar 

  30. Willi G, Bodenmann P, Ghali WA, Faris PD, Cornuz J (2007) Active smoking and the risk of type 2 diabetes: a systematic review and meta-analysis. JAMA 298:2654–2664

    Article  CAS  PubMed  Google Scholar 

  31. Okamoto Y, Tsuboi S, Suzuki S, Nakagaki H, Ogura Y, Maeda K, Tokudome S (2006) Effects of smoking and drinking habits on the incidence of periodontal disease and tooth loss among Japanese males: a 4-yr longitudinal study. J Periodontal Res 41:560–566

    Article  CAS  PubMed  Google Scholar 

  32. Shimazaki Y, Saito T, Yonemoto K, Kiyohara Y, Iida M, Yamashita Y (2007) Relationship of metabolic syndrome to periodontal disease in Japanese women: the Hisayama study. J Dent Res 86:271–275

    Article  CAS  PubMed  Google Scholar 

  33. Neely AL, Holford TR, Löe H, Anerud A, Boysen H (2005) The natural history of periodontal disease in humans: risk factors for tooth loss in caries-free subjects receiving no oral health care. J Clin Periodontol 32:984–993

    Article  PubMed  Google Scholar 

  34. Nishida M, Grossi SG, Dunford RG, Ho AW, Trevisan M, Genco RJ (2000) Dietary vitamin C and the risk for periodontal disease. J Periodontol 71:1215–1223

    Article  CAS  PubMed  Google Scholar 

  35. Dinneen SF, Maldonado D 3rd, Leibson CL, Klee GG, Li H, Melton LJ 3rd, Rizza RA (1998) Effects of changing diagnostic criteria on the risk of develo** diabetes. Diabetes Care 21:1408–1413

    Article  CAS  PubMed  Google Scholar 

  36. Wilson PW, Meigs JB, Sullivan L, Fox CS, Nathan DM, D’Agostino RB Sr (2007) Prediction of incident diabetes mellitus in middle-aged adults: the Framingham offspring study. Arch Intern Med 167:1068–1074

    Article  PubMed  Google Scholar 

  37. American Diabetes Association and National Institute of Diabetes, Digestive and Kidney Diseases (2002) The Prevention or delay of type 2 diabetes. Diabetes Care 25:742–749

    Article  Google Scholar 

  38. Davey Smith G, Bracha Y, Svendsen KH, Neaton JD, Haffner SM, Kuller LH (2005) Multiple risk factor intervention trial research group incidence of type 2 diabetes in the randomized multiple risk factor intervention trial. Ann Intern Med 142:313–322

    Article  PubMed  Google Scholar 

  39. Li G, Zhang P, Wang J, Gregg EW, Yang W, Gong Q, Li H, Li H, Jiang Y, An Y, Shuai Y, Zhang B, Zhang J, Thompson TJ, Gerzoff RB, Roglic G, Hu Y, Bennett PH (2008) The long-term effect of lifestyle interventions to prevent diabetes in the China Da Qing Diabetes Prevention Study: a 20-year follow-up study. Lancet 371:1783–1789

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

We thank all faculty of the Public Health Center and Division of Health Promotion, Health Bureau of Keelung City, Keelung City, Taiwan for their contribution to the Keelung Community-based Integrated Screening (KCIS).

Conflict of interest

The authors declare that there are no conflicts of interest in this study.

Human and animal rights

All procedures followed were in accordance with the ethical standards of the responsible committee on human experimentation (institutional and national) and with the Helsinki Declaration of 1975, as revised in 2008.

Informed consent

Informed consent was obtained from all subjects for being included in this study, which was governed by Health Bureau.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Hsiu-Hsi Chen.

Additional information

Managed by Massimo Porta.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Chiu, S.YH., Lai, H., Yen, A.MF. et al. Temporal sequence of the bidirectional relationship between hyperglycemia and periodontal disease: a community-based study of 5,885 Taiwanese aged 35–44 years (KCIS No. 32). Acta Diabetol 52, 123–131 (2015). https://doi.org/10.1007/s00592-014-0612-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00592-014-0612-0

Keywords

Navigation