Skip to main content

Advertisement

SpringerLink
Log in

Periodontitis predicts HbA1c levels and glucose variability in type 1 diabetic patients: the PARODIA Florence Project study

  • Original Article
  • Published:
Clinical Oral Investigations Aims and scope Submit manuscript

Abstract

Objective

The aim of the present study was to assess the extent and severity of periodontal disease among type 1 diabetic patients (T1DM) and to investigate the possible association with systemic markers of glucose control and variability.

Material and methods

Patients were consecutively enrolled in a Diabetic Unit. A full-mouth periodontal evaluation was performed, and data on systemic markers of diabetes were collected. Descriptive statistics and logistic and linear models were performed.

Results

A total of 136 T1DM patients (mean age: 45.5 ± 14.6 years) were examined. Periodontitis was detected in 62% of cases (mean CAL: 3.0 ± 0.9 mm): stage III periodontitis was diagnosed in 32% of patients while stage IV in 8%. Mean level of glycated hemoglobin (HbA1c) was 7.5% ± 1.4. Among the investigated factors, mean CAL (p=0.040) was associated with HbA1c ≥ 7%; 93% of patients with mean CAL > 6 mm showed HbA1c ≥ 7%. Mean CAL (p=0.004), mean PPD (p=0.005), mean FMPS (p=0.030), and stage III/IV periodontitis (p=0.018) predict glucose coefficient of variation (CV).

Conclusions

Periodontitis showed a relevant prevalence in the present, well-controlled T1DM population and predicts poor glycemic control (HbA1c ≥7%) and higher glucose variability. The present findings suggest that periodontal infection may have systemic effects also in T1DM patients.

Clinical relevance

The extent and severity of periodontitis and its possible systemic effects in T1DM patients could be underestimated.

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

References

  1. Sanz M, Quirynen M, European Workshop in Periodontology Group A (2005) Advances in the aetiology of periodontitis. Group A: consensus report of the 5th European Workshop in Periodontology. J Clin Periodontol 32(Suppl. 6):54–56. https://doi.org/10.1111/j.1600-051X.2005.00827.x

    Article  PubMed  Google Scholar 

  2. Kassebaum NJ, Bernab E, Dahiya M, Bhandari B, Murray CJ, Marcenes W (2014) Global burden of severe periodontitis in 1990-2010: a systematic review and meta-regression. J Dental Re 93(11):1045–1053. https://doi.org/10.1177/0022034514552491

    Article  Google Scholar 

  3. Chapple IL, Genco R, Working group 2 of the joint EFP/AAP workshop (2013) Diabetes and periodontal diseases: consensus report of the Joint EFP/AAP Workshop on Periodontitis and Systemic Diseases. J Periodontol 84(4 Suppl):S106–S112. https://doi.org/10.1902/jop.2013.1340011

    Article  PubMed  Google Scholar 

  4. Kapila YL (2021) Oral health’s inextricable connection to systemic health: special populations bring to bear multimodal relationships and factors connecting periodontal disease to systemic diseases and conditions. Periodontol 87(1):11–16. https://doi.org/10.1111/prd.12398

    Article  Google Scholar 

  5. Cairo F, Castellani S, Gori AM, Nieri M, Baldelli G, Abbate R, Pini-Prato GP (2008) Severe periodontitis in young adults is associated with sub-clinical atherosclerosis. J Clin Periodontol 35(6):465–472. https://doi.org/10.1111/j.1600-051X.2008.01228.x

    Article  PubMed  Google Scholar 

  6. Cairo F, Castellani S, Gori AM, Nieri M, Abbate R, Pini-Prato GP (2009) Periodontol variables predict sub-clinical atherosclerosis and systemic inflammation in young adults. Eur J Oral Implant 2:125–133

    Google Scholar 

  7. D’Aiuto F, Gkranias N, Bhowruth D, Khan T, Orlandi M, Suvan J, Masi S, Tsakos G, Hurel S, Hingorani AD, Donos N, Deanfield JE, TASTE Group (2018) Systemic effects of periodontitis treatment in patients with type 2 diabetes: a 12 month, single-centre, investigator-masked, randomised trial. Lancet Diabetes Endocrinol 6(12):954–965. https://doi.org/10.1016/S2213-8587(18)30038-X

    Article  PubMed  Google Scholar 

  8. Cairo F, Gaeta C, Dorigo W, Oggioni MR, Pratesi C, Pini Prato GP, Pozzi G (2004) Periodontal pathogens in atheromatous plaques. A controlled clinical and laboratory plaques. J Periodontal Res 39:442–446. https://doi.org/10.1111/j.1600-0765.2004.00761.x

    Article  PubMed  Google Scholar 

  9. Genco RJ, Borgnakke WS (2013) Diabetes as a potential risk for periodontitis: association studies. Periodontol 83(1):40–45. https://doi.org/10.1111/prd.12270

    Article  Google Scholar 

  10. Genco RJ, Borgnakke WS (2020) Diabetes as a potential risk for periodontitis: association studies. Periodontol 83(1):40–45. https://doi.org/10.1111/prd.12270

    Article  Google Scholar 

  11. Polak D, Sanui T, Nishimura F, Shapira L (2020) Diabetes as a risk factor for periodontal disease-plausible mechanisms. Periodontol 83(1):46–58. https://doi.org/10.1111/prd.12298

    Article  Google Scholar 

  12. Golub LM, Schneir M, Ramamurthy NS (1978) Enhanced collagenase activity in diabetic rat gingiva: in vitro and in vivo evidence. J Dent Res 57(3):520–525. https://doi.org/10.1177/00220345780570032101

    Article  PubMed  Google Scholar 

  13. Federoff HJ, Lawrence D, Brownlee M (1993) Nonenzymatic glycosylation of laminin and the laminin peptide CIKVAVS inhibits neurite outgrowth. Diabetes 42(4):509–513. https://doi.org/10.2337/diab.42.4.509

    Article  PubMed  Google Scholar 

  14. Zambon JJ, Reynolds H, Fisher JG, Shlossman M, Dunford R, Genco RJ (1988) Microbiological and immunological studies of adult periodontitis in patients with noninsulin-dependent diabetes mellitus. J Periodontol 59(1):23–31. https://doi.org/10.1902/jop.1988.59.1.23

    Article  PubMed  Google Scholar 

  15. Salvi GE, Lawrence HP, Offenbacher S, Beck JD (1997) Influence of risk factors on the pathogenesis of periodontitis. Periodontol 14:173–201. https://doi.org/10.1111/j.1600-0757.1997.tb00197.x

    Article  Google Scholar 

  16. Ko KI, Sculean A, Graves DT (2021) Diabetic wound healing in soft and hard oral tissues. Transl Res 236:72–86. https://doi.org/10.1016/j.trsl.2021.05.001

    Article  PubMed  Google Scholar 

  17. Sanz M, Ceriello A, Buysschaert M, Chapple I, Demmer RT, Graziani F, Herrera D, Jepsen S, Lione L, Madianos P, Mathur M, Montanya E, Shapira L, Tonetti M, Vegh D (2018) Scientific evidence on the links between periodontal diseases and diabetes: consensus report and guidelines of the joint workshop on periodontal diseases and diabetes by the International Diabetes Federation and the European Federation of Periodontology. J Clin Periodontol 45(2):138–149. https://doi.org/10.1111/jcpe.12808

    Article  PubMed  Google Scholar 

  18. Genco RJ, Graziani F, Hasturk H (2020) Effects of periodontal disease on glycemic control, complications, and incidence of diabetes mellitus. Periodontol 83(1):59–65. https://doi.org/10.1111/prd.12271

    Article  Google Scholar 

  19. Graziani F, Gennai S, Solini A, Petrini M (2018) A systematic review and meta-analysis of epidemiologic observational evidence on the effect of periodontitis on diabetes An update of the EFP-AAP review. J Clin Periodontol 45(2):167–187. https://doi.org/10.1111/jcpe.12837

    Article  PubMed  Google Scholar 

  20. Engebretson S, Kocher T (2013) Evidence that periodontal treatment improves diabetes outcomes: a systematic review and meta-analysis. J Periodontol 84(Suppl 4):S153–S169. https://doi.org/10.1902/jop.2013.1340017

    Article  PubMed  PubMed Central  Google Scholar 

  21. Dicembrini I, Serni L, Monami M, Caliri M, Barbato L, Cairo F, Mannucci E (2020) Type 1 diabetes and periodontitis: prevalence and periodontal destruction-a systematic review. Acta Diabetol 57(12):1405–1412. https://doi.org/10.1007/s00592-020-01531-7

    Article  PubMed  Google Scholar 

  22. Dicembrini I, Barbato L, Serni L, Caliri M, Pala L, Cairo F, Mannucci E (2021) Glucose variability and periodontal disease in type 1 diabetes: a cross-sectional study-the “PAROdontopatia e DIAbete” (PARODIA) project. Acta Diabetol 58(10):1367–1371. https://doi.org/10.1007/s00592-021-01720-y

    Article  PubMed  PubMed Central  Google Scholar 

  23. Tonetti MS, Greenwell H, Kornman KS (2018) Staging and grading of periodontitis: framework and proposal of a new classification and case definition. J Clin Periodontol 45(Suppl 20):S149–S161. https://doi.org/10.1111/jcpe.12945

    Article  PubMed  Google Scholar 

  24. Hsieh FY (1989) Sample size tables for logistic regression. Stat Med 8(7):795–802. https://doi.org/10.1002/sim.4780080704

    Article  PubMed  Google Scholar 

  25. Hugoson A, Norderyd O, Slotte C, Thorstensson H (1998) Distribution of periodontal disease in a Swedish adult population 1973, 1983 and 1993. J Clin Periodontol 25:542–548. https://doi.org/10.1111/j.1600-051x.1998.tb02485.x

    Article  PubMed  Google Scholar 

  26. Tonetti MS, Jepsen S, Jin L, Otomo-Corgel J (2017) Impact of the global burden of periodontal diseases on health, nutrition and wellbeing of mankind: a call for global action. J Clin Periodontol 44:456–462. https://doi.org/10.1111/jcpe.12732

    Article  PubMed  Google Scholar 

  27. Preshaw PM, Alba AL, Herrera D, Jepsen S, Kostantinidis A, Makrilakis K, Taylor R (2012) Periodontitis and diabetes: a two-way relationship. Diabetologia 55(1):21–31. https://doi.org/10.1007/s00125-011-2342-y

    Article  PubMed  Google Scholar 

  28. Taylor GW (2001) Bidirectional interrelationships between diabetes and periodontal diseases: an epidemiologic perspective. Ann Periodontol 6:99–112. https://doi.org/10.1902/annals.2001.6.1.99

    Article  PubMed  Google Scholar 

  29. Lalla E, Cheng B, Lal S, Kaplan S, Softness B, Greenberg E, Goland RS, Lamster I (2007) Diabetes mellitus promotes periodontal destruction in children. J Clin Periodontol 34:294–298. https://doi.org/10.1111/j.1600-051X.2007.01054.x

    Article  PubMed  Google Scholar 

Download references

Funding

This study was self-funded.

Author information

Authors and Affiliations

  1. Research Unit in Periodontology and Periodontal Medicine, Department of Experimental and Clinical Medicine, University of Florence, Florence, Italy

    Francesco Cairo, Lapo Serni, Michele Nieri, Guido Bettarini & Luigi Barbato

  2. Department of Experimental and Clinical Biomedical Sciences, University of Florence, viale Morgagni 50, 50134, Florence, Italy

    Ilaria Dicembrini, Mariasmeralda Caliri, Laura Pala & Edoardo Mannucci

  3. Diabetes Unit, Careggi Teaching Hospital, Largo Brambilla 3, 50127, Florence, Italy

    Ilaria Dicembrini, Mariasmeralda Caliri, Laura Pala & Edoardo Mannucci

Authors
  1. Francesco Cairo
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ilaria Dicembrini
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Lapo Serni
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Michele Nieri
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Guido Bettarini
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Mariasmeralda Caliri
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Laura Pala
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Edoardo Mannucci
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Luigi Barbato
    View author publications

    You can also search for this author in PubMed Google Scholar

Ethics declarations

Ethical approval

The study protocol was approved by the Ethical Board (PARODIA Project, approval number: CEAVC 30952/2019).

Conflict of interest

Francesco Cairo has received consultancy fees and grants from Straumann and Geistlich Biomaterials. Ilaria Dicembrini has received speaking fees from Merck, Novartis, AstraZeneca, Bristol Myers Squibb, Boehringer-Ingelheim, Eli-Lilly, Novo Nordisk, Sanofi, and Novartis. Edoardo Mannucci has received consultancy fees from Merck and Novartis; speaking fees from AstraZeneca, Bristol Myers Squibb, Boehringer-Ingelheim, Eli-Lilly, Merck, Novo Nordisk, Sanofi; and Novartis, and research grants from Merck, Novartis, and Takeda. Other authors have nothing to disclose.

Informed consent

Informed consent was obtained from all subjects included in the study.

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

Cairo, F., Dicembrini, I., Serni, L. et al. Periodontitis predicts HbA1c levels and glucose variability in type 1 diabetic patients: the PARODIA Florence Project study. Clin Oral Invest 26, 3585–3591 (2022). https://doi.org/10.1007/s00784-021-04326-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00784-021-04326-4

Keywords

Search

Navigation