Top

Acta Diabetologica

Published in:

01-07-2018 | Review Article

Does diabetes increase the risk of periodontitis? A systematic review and meta-regression analysis of longitudinal prospective studies

Authors: Gustavo G. Nascimento, Fábio R. M. Leite, Peter Vestergaard, Flemming Scheutz, Rodrigo López

Published in: Acta Diabetologica | Issue 7/2018

Abstract

Aim

Even though the association between diabetes and periodontitis is taken for granted, results on this association are conflicting within the literature. This systematic review assessed whether poorly controlled diabetes was associated with periodontitis onset or progression.

Methods

Electronic searches were performed in PubMed, Scopus and Embase databases. Hand search was carried out in the reference list of all articles included. Gray literature was investigated with a Google Scholar search. Prospective longitudinal studies on the association between diabetes and periodontitis were considered for this review. Studies should have presented at least two measurements of periodontal conditions over time. Data on study design, crude and adjusted estimates were collected. We used meta-analysis to estimate the pooled effect of hyperglycemia in people with diabetes on periodontitis onset or progression. Meta-regression and subgroup analyses were employed to investigate potential sources of heterogeneity between studies.

Results

Thirteen studies matched the inclusion criteria, comprising 49,262 individuals, including 3197 diagnosed with diabetes. Meta-analyses of adjusted estimates showed that diabetes increased the risk of incidence or progression of periodontitis by 86% (RR 1.86 [95% CI 1.3–2.8]). However, there is scarce information on the association between diabetes and periodontal destruction.

Conclusions

This study provides evidence that diabetes is associated with increased risk of periodontitis onset and progression in adults. Upcoming prospective longitudinal studies ought to overcome methodological caveats identified in this review.

Available only for authorised users

American Diabetes Association (2014) Diagnosis and classification of diabetes mellitus. Diabetes Care 37(Suppl 1):S81–S90. https://doi.org/10.2337/dc14-S081 CrossRef

Internation Diabetes Federation (2015) International Diabetes Federation Diabetes Atlas, 7th edn, vol 144. http://www.diabetesatlas.org/. Accessed 14 Jun 2017

Fox CS, Coady S, Sorlie PD et al (2007) Increasing cardiovascular disease burden due to diabetes mellitus: the Framingham Heart Study. Circulation 115(12):1544–1550. https://doi.org/10.1161/CIRCULATIONAHA.106.658948 CrossRefPubMed

Smith NL, Barzilay JI, Kronmal R et al (2006) New-onset diabetes and risk of all-cause and cardiovascular mortality: the Cardiovascular Health Study. Diabetes Care 29(9):2012–2017. https://doi.org/10.2337/dc06-0574 CrossRefPubMed

Lu J, Hou X, Zhang L et al (2015) Association between body mass index and diabetic retinopathy in Chinese patients with type 2 diabetes. Acta Diabetol 52(4):701–708. https://doi.org/10.1007/s00592-014-0711-y CrossRefPubMed

Tasci I, Basgoz BB, Saglam K (2016) Glycemic control and the risk of microvascular complications in people with diabetes mellitus. Acta Diabetol 53(1):129–130. https://doi.org/10.1007/s00592-015-0778-0 CrossRefPubMed

Tadic M, Cuspidi C, Vukomanovic V et al (2016) The influence of type 2 diabetes and arterial hypertension on right ventricular layer-specific mechanics. Acta Diabetol 53(5):791–797. https://doi.org/10.1007/s00592-016-0874-9 CrossRefPubMed

Giacco F, Brownlee M (2010) Oxidative stress and diabetic complications. Circ Res 107(9):1058–1070. https://doi.org/10.1161/CIRCRESAHA.110.223545 CrossRefPubMedPubMedCentral

Löe H (1993) Periodontal disease. The sixth complication of diabetes mellitus. Diabetes Care 16(1):329–334CrossRefPubMed

10.

Van Dyke TE (2014) Commentary: periodontitis is characterized by an immuno-inflammatory host-mediated destruction of bone and connective tissues that support the teeth. J Periodontol 85(4):509–511. https://doi.org/10.1902/jop.2014.130701 CrossRefPubMed

11.

Hyvarinen K, Salminen A, Salomaa V, Pussinen PJ (2015) Systemic exposure to a common periodontal pathogen and missing teeth are associated with metabolic syndrome. Acta Diabetol 52(1):179–182. https://doi.org/10.1007/s00592-014-0586-y CrossRefPubMed

12.

Brennan DS, Spencer AJ, Roberts-Thomson KF (2007) Quality of life and disability weights associated with periodontal disease. J Dent Res 86(8):713–717. https://doi.org/10.1177/154405910708600805 CrossRefPubMed

13.

Kassebaum NJ, Bernabe 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 Dent Res 93(11):1045–1053. https://doi.org/10.1177/0022034514552491 CrossRefPubMedPubMedCentral

14.

Corbella S, Francetti L, Taschieri S, De Siena F, Fabbro MD (2013) Effect of periodontal treatment on glycemic control of patients with diabetes: a systematic review and meta-analysis. J Diabetes Invest 4(5):502–509. https://doi.org/10.1111/jdi.12088 CrossRef

15.

Pink C, Kocher T, Meisel P et al (2015) Longitudinal effects of systemic inflammation markers on periodontitis. J Clin Periodontol 42(11):988–997. https://doi.org/10.1111/jcpe.12473 CrossRefPubMed

16.

Hujoel PP, Stott-Miller M (2011) Retinal and gingival hemorrhaging and chronic hyperglycemia. Diabetes Care 34(1):181–183. https://doi.org/10.2337/dc10-0901 CrossRefPubMed

17.

Vandenbroucke JP, von Elm E, Altman DG et al (2007) Strengthening the Reporting of Observational Studies in Epidemiology (STROBE): explanation and elaboration. Epidemiology 18(6):805–835. https://doi.org/10.1097/EDE.0b013e3181577511 CrossRefPubMed

18.

Chavarry NG, Vettore MV, Sansone C, Sheiham A (2009) The relationship between diabetes mellitus and destructive periodontal disease: a meta-analysis. Oral Health Prev Dent 7(2):107–127PubMed

19.

Moher D, Liberati A, Tetzlaff J, Altman DG, PRISMA Group (2009) Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. PLoS Med 6(7):e1000097. https://doi.org/10.1371/journal.pmed.1000097 CrossRefPubMedPubMedCentral

20.

The Joanna Briggs Institute (2017) Registered topics in the JBI database. http://joannabriggs.org/research/registered_titles.aspx. Accessed 08 Oct 2017

21.

Wells GA, Shea B, O’Connell D, Peterson J, Welch V, Losos M, Tugwell P (2014) The Newcastle–Ottawa Scale (NOS) for assessing the quality if nonrandomised studies in meta-analyses. http://www.ohri.ca/programs/clinical_epidemiology/nosgen.pdf. Accessed 08 June 2017

22.

Higgins JP, Thompson SG, Deeks JJ, Altman DG (2003) Measuring inconsistency in meta-analyses. BMJ 327(7414):557–560. https://doi.org/10.1136/bmj.327.7414.557 CrossRefPubMedPubMedCentral

23.

Zhang J, Yu KF (1998) What’s the relative risk? A method of correcting the odds ratio in cohort studies of common outcomes. JAMA 280(19):1690–1691CrossRefPubMed

24.

World Bank Group (2017) Country and lending groups. http://data.worldbank.org/about/country-and-lending-groups. Accessed 08 June 2017

25.

Bandyopadhyay D, Marlow NM, Fernandes JK, Leite RS (2010) Periodontal disease progression and glycaemic control among Gullah African Americans with type-2 diabetes. J Clin Periodontol 37(6):501–509. https://doi.org/10.1111/j.1600-051X.2010.01564.x CrossRefPubMedPubMedCentral

26.

Cohen DW, Friedman LA, Shapiro J, Kyle GC, Franklin S (1970) Diabetes mellitus and periodontal disease: two-year longitudinal observations. I. J Periodontol 41(12):709–712. https://doi.org/10.1902/jop.1970.41.12.709 CrossRefPubMed

27.

Iwasaki M, Sato M, Minagawa K, Manz MC, Yoshihara A, Miyazaki H (2015) Longitudinal relationship between metabolic syndrome and periodontal disease among Japanese adults aged ≥70 years: the Niigata Study. J Periodontol 86(4):491–498. https://doi.org/10.1902/jop.2015.140398 CrossRefPubMed

28.

Karikoski A, Murtomaa H (2003) Periodontal treatment needs in a follow-up study among adults with diabetes in Finland. Acta Odontol Scand 61(1):6–10CrossRefPubMed

29.

Sbordone L, Ramaglia L, Barone A, Ciaglia RN, Iacono VJ (1998) Periodontal status and subgingival microbiota of insulin-dependent juvenile diabetics: a 3-year longitudinal study. J Periodontol 69(2):120–128. https://doi.org/10.1902/jop.1998.69.2.120 CrossRefPubMed

30.

Novaes AB Jr., Silva MAP, Batista EL Jr, Dos Anjos BA, Novaes AB, Pereira ALA (1997) Manifestations of insulin-dependent diabetes mellitus in the periodontium of young Brazilian patients. A 10-year follow-up study. J Periodontol 68(4):328–334CrossRefPubMed

31.

Firatli E (1997) The relationship between clinical periodontal status and insulin-dependent diabetes mellitus. Results after 5 years. J Periodontol 68(2):136–140. https://doi.org/10.1902/jop.1997.68.2.136 CrossRefPubMed

32.

Jimenez M, Hu FB, Marino M, Li Y, Joshipura KJ (2012) Type 2 diabetes mellitus and 20 year incidence of periodontitis and tooth loss. Diabetes Res Clin Pract 98(3):494–500. https://doi.org/10.1016/j.diabres.2012.09.039 CrossRefPubMedPubMedCentral

33.

Demmer RT, Kerner W, Holtfreter B et al (2012) The influence of type 1 and type 2 diabetes on periodontal disease progression: prospective results from the Study of Health in Pomerania (SHIP). Diabetes Care 35(10):2036–2042. https://doi.org/10.2337/dc11-2453 CrossRefPubMedPubMedCentral

34.

Morita I, Inagaki K, Nakamura F et al (2012) Relationship between periodontal status and levels of glycated hemoglobin. J Dent Res 91(2):161–166. https://doi.org/10.1177/0022034511431583 CrossRefPubMed

35.

Taylor GW, Burt BA, Becker MP, Genco RJ, Shlossman M (1998) Glycemic control and alveolar bone loss progression in type 2 diabetes. Ann Periodontol 3(1):30–39. https://doi.org/10.1902/annals.1998.3.1.30 CrossRefPubMed

36.

Chiu SYH, Lai H, Yen AMF, Fann JCY, Chen LS, Chen HH (2015) Temporal sequence of the bidirectional relationship between hyperglycemia and periodontal disease: a community-based study of 5885 Taiwanese aged 35–44 years (KCIS No. 32). Acta Diabetol 52(1):123–131. https://doi.org/10.1007/s00592-014-0612-0 CrossRefPubMed

37.

Lee KS, Kim EK, Kim JW et al (2014) The relationship between metabolic conditions and prevalence of periodontal disease in rural Korean elderly. Arch Gerontol Geriatr 58(1):125–129. https://doi.org/10.1016/j.archger.2013.08.011 CrossRefPubMed

38.

Sterne JA, Gavaghan D, Egger M (2000) Publication and related bias in meta-analysis: power of statistical tests and prevalence in the literature. J Clin Epidemiol 53(11):1119–1129CrossRefPubMed

39.

Zhang Z, Xu X, Ni H (2013) Small studies may overestimate the effect sizes in critical care meta-analyses: a meta-epidemiological study. Crit Care 17(1):R2. https://doi.org/10.1186/cc11919 CrossRefPubMedPubMedCentral

40.

Dechartres A, Trinquart L, Boutron I, Ravaud P (2013) Influence of trial sample size on treatment effect estimates: meta-epidemiological study. BMJ 346:f2304. https://doi.org/10.1136/bmj.f2304 CrossRefPubMedPubMedCentral

41.

Nascimento GG, Leite FR, Conceicao DA, Ferrua CP, Singh A, Demarco FF (2016) Is there a relationship between obesity and tooth loss and edentulism? A systematic review and meta-analysis. Obes Rev 17(7):587–598. https://doi.org/10.1111/obr.12418 CrossRefPubMed

42.

Michalowicz BS, Hodges JS, Pihlstrom BL (2013) Is change in probing depth a reliable predictor of change in clinical attachment loss? J Am Dent Assoc 144(2):171–178CrossRefPubMed

43.

Baelum V, Manji F, Wanzala P, Fejerskov O (1995) Relationship between CPITN and periodontal attachment loss findings in an adult population. J Clin Periodontol 22(2):146–152CrossRefPubMed

44.

Agerholm DM, Ashley FP (1996) Clinical assessment of periodontitis in young adults—evaluation of probing depth and partial recording methods. Commun Dent Oral Epidemiol 24(1):56–61CrossRef

45.

Mdala I, Olsen I, Haffajee AD, Socransky SS, Thoresen M, de Blasio BF (2014) Comparing clinical attachment level and pocket depth for predicting periodontal disease progression in healthy sites of patients with chronic periodontitis using multi-state Markov models. J Clin Periodontol 41(9):837–845. https://doi.org/10.1111/jcpe.12278 CrossRefPubMedPubMedCentral

46.

Stroup DF, Berlin JA, Morton SC et al (2000) Meta-analysis of observational studies in epidemiology: a proposal for reporting. Meta-analysis Of Observational Studies in Epidemiology (MOOSE) group. JAMA 283(15):2008–2012CrossRefPubMed

47.

Shrier I, Boivin JF, Steele RJ et al (2007) Should meta-analyses of interventions include observational studies in addition to randomized controlled trials? A critical examination of underlying principles. Am J Epidemiol 166(10):1203–1209. https://doi.org/10.1093/aje/kwm189 CrossRefPubMed

48.

Nascimento GG, Peres MA, Mittinty MN et al (2017) Diet-induced overweight and obesity and periodontitis risk: an application of the parametric G-formula in the 1982 Pelotas Birth Cohort. Am J Epidemiol 185(6):442–451. https://doi.org/10.1093/aje/kww187 CrossRefPubMed

49.

Leung MY, Carlsson NP, Colditz GA, Chang SH (2017) The burden of obesity on diabetes in the United States: Medical Expenditure Panel Survey, 2008 to 2012. Value Health 20(1):77–84. https://doi.org/10.1016/j.jval.2016.08.735 CrossRefPubMed

50.

Pogue J, Yusuf S (1998) Overcoming the limitations of current meta-analysis of randomised controlled trials. Lancet 351(9095):47–52. https://doi.org/10.1016/S0140-6736(97)08461-4 CrossRefPubMed

51.

Bian Z, Guo Y, Ha B, Zen K, Liu Y (2012) Regulation of the inflammatory response: enhancing neutrophil infiltration under chronic inflammatory conditions. J Immunol 188(2):844–853. https://doi.org/10.4049/jimmunol.1101736 CrossRefPubMed

52.

Chapple IL, Matthews JB (2000) The role of reactive oxygen and antioxidant species in periodontal tissue destruction. Periodontol 43:160–232. https://doi.org/10.1111/j.1600-0757.2006.00178.x CrossRef

53.

Nassar H, Kantarci A, van Dyke TE (2000) Diabetic periodontitis: a model for activated innate immunity and impaired resolution of inflammation. Periodontology 2000 43:233–244. https://doi.org/10.1111/j.1600-0757.2006.00168.x CrossRef

54.

Graves DT, Liu R, Alikhani M, Al-Mashat H, Trackman PC (2006) Diabetes-enhanced inflammation and apoptosis—impact on periodontal pathology. J Dent Res 85(1):15–21CrossRefPubMed

55.

Ding Y, Kantarci A, Hasturk H, Trackman PC, Malabanan A, Van Dyke TE (2007) Activation of RAGE induces elevated O₂-generation by mononuclear phagocytes in diabetes. J Leukoc Biol 81(2):520–527. https://doi.org/10.1189/jlb.0406262 CrossRefPubMed

56.

Gyurko R, Siqueira CC, Caldon N, Gao L, Kantarci A, Van Dyke TE (2006) Chronic hyperglycemia predisposes to exaggerated inflammatory response and leukocyte dysfunction in Akita mice. J Immunol 177(10):7250–7256CrossRefPubMedPubMedCentral

57.

Seppälä B, Seppälä M, Ainamo J (1993) A longitudinal study on insulin-dependent diabetes mellitus and periodontal disease. J Clin Periodontol 20(3):161–165. https://doi.org/10.1111/j.1600-051X.1993.tb00338.x CrossRefPubMed

58.

Seppälä B, Ainamo J (1994) A site-by-site follow-up study on the effect of controlled versus poorly controlled insulin-dependent diabetes mellitus. J Clin Periodontol 21(3):161–165. https://doi.org/10.1111/j.1600-051X.1994.tb00297.x CrossRefPubMed

59.

Novaes AB Jr, Gutierrez FG, Novaes AB (1996) Periodontal disease progression in type II non-insulin-dependent diabetes mellitus patients (NIDDM). Part I-Probing pocket depth and clinical attachment. Braz Dent J 7(2):65–73PubMed

60.

Taylor GW, Burt BA, Becker MP, Genco RJ, Shlossman M, Knowler WC, Pettitt DJ (1998) Non-insulin dependent diabetes mellitus and alveolar bone loss progression over 2 years. J Periodontol 69(1):76–83. https://doi.org/10.1902/jop.1998.69.1.76 CrossRefPubMed

61.

Thomson WM, Slade GD, Beck JD, Elter JR, Spencer AJ, Chalmers JM (2004) Incidence of periodontal attachment loss over 5 years among older South Australians. J Clin Periodontol 31(2):119–125. https://doi.org/10.1111/j.0303-6979.2004.00460.x CrossRefPubMed

62.

Morita I, Okamoto Y, Yoshii S, Nakagaki H, Mizuno K, Sheiham A, Sabbah W (2011) Five-year incidence of periodontal disease is related to body mass index. J Dent Res 90(2):199–202. https://doi.org/10.1177/0022034510382548 CrossRefPubMed

63.

Timonen P, Saxlin T, Knuuttila M, Suominen AL, Jula A, Tervonen T, Ylöstalo P (2013) Role of insulin sensitivity and beta cell function in the development of periodontal disease in adults without diabetes. J Clin Periodontol 40(12):1079–1086. https://doi.org/10.1111/jcpe.12162 CrossRefPubMed

64.

Knight ET, Leichter JW, Tawse-Smith A, Thomson WM (2015) Quantifying the association between self-reported diabetes and periodontitis in the New Zealand population. J Periodontol 86(8):945–954. https://doi.org/10.1902/jop.2015.150048 CrossRefPubMed

65.

Chang JS, Tsai CR, Chen LT, Shan YS (2016) Investigating the association between periodontal disease and risk of pancreatic cancer. Pancreas 45(1):134–141. https://doi.org/10.1097/MPA.0000000000000419 CrossRefPubMed

66.

Shearer DM, Thomson WM, Broadbent JM, Mann J, Poulton R (2017) Periodontitis is not associated with metabolic risk during the fourth decade of life. J Clin Periodontol 44(1):22–30. https://doi.org/10.1111/jcpe.12641 CrossRefPubMed

Title: Does diabetes increase the risk of periodontitis? A systematic review and meta-regression analysis of longitudinal prospective studies
Authors: Gustavo G. Nascimento
Fábio R. M. Leite
Peter Vestergaard
Flemming Scheutz
Rodrigo López
Publication date: 01-07-2018
Publisher: Springer Milan
Published in: Acta Diabetologica / Issue 7/2018
Print ISSN: 0940-5429
Electronic ISSN: 1432-5233
DOI: https://doi.org/10.1007/s00592-018-1120-4

Obesity Clinical Trial Summary

At a glance: The STEP trials

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.

Developed by: Springer Medicine

Highlights from the ACC 2024 Congress

Year in Review: Pediatric cardiology

Pediatric Cardiology Video

Watch Dr. Anne Marie Valente present the last year's highlights in pediatric and congenital heart disease in the official ACC.24 Year in Review session.

Year in Review: Pulmonary vascular disease

Cardiopulmonary Comorbidity Video

The last year's highlights in pulmonary vascular disease are presented by Dr. Jane Leopold in this official video from ACC.24.

Year in Review: Valvular heart disease

Valvular Heart Disease Video

Watch Prof. William Zoghbi present the last year's highlights in valvular heart disease from the official ACC.24 Year in Review session.

Year in Review: Heart failure and cardiomyopathies

Heart Failure Video

Watch this official video from ACC.24. Dr. Biykem Bozkurt discuss last year's major advances in heart failure and cardiomyopathies.

ACC 2024 Congress Coverage

Heart Failure Video

Year in Review: Heart failure and cardiomyopathies

Watch now

Watch this official video from ACC.24. Dr. Biykem Bozkurt discuss last year's major advances in heart failure and cardiomyopathies.

Semaglutide benefits people with type 2 diabetes and obesity-related heart failure

16-04-2024 Type 2 Diabetes News

Incentivised to exercise

11-04-2024 Lifestyle Modifications News

New intervention for STEMI-related cardiogenic shock

10-04-2024 Myocardial Infarction News

» View more highlights on the ACC 2024 congress hub page

Image Credits

STEP AAG HeroTeaserCollection image/© Tarek / Generated with AI / Stock.adobe.com, ACC 2024 Pediatric and Congenital Heart Disease: Year in Review/© 2024 American College of Cardiology, ACC 2024 Pulmonary Vascular Disease: Year in Review/© 2024 American College of Cardiology, ACC 2024 Valvular Heart Disease: Year in Review/© 2024 American College of Cardiology, ACC 2024 HF and Cardiomyopathies: Year in Review/© 2024 American College of Cardiology, Woman out walking/© Seventyfour / stock.adobe.com (symbolic image with model), Woman checking smartwatch /© saltdium / stock.adobe.com (symbolic image with model), Cardiac catheterization/© Damian / stock.adobe.com

At a glance: The STEP trials

Springer Medicine

Abstract

Aim

Methods

Results

Conclusions

Please log in to get access to this content

Other articles of this Issue 7/2018

The relationship between the thickness of glomerular basement membrane and renal outcomes in patients with diabetic nephropathy

Relationship between serum apolipoproteins levels and retinopathy risk in subjects with type 2 diabetes mellitus

Reply to Letter to the Editor “The effects of resveratrol on markers of oxidative stress in patients with type 2 diabetes: a randomized, double-blind, placebo-controlled clinical trial”

Effect of resveratrol in type 2 diabetes oxidative stress markers: a reassessment

The effect of n-3 PUFAs on circulating adiponectin and leptin in patients with type 2 diabetes mellitus: a systematic review and meta-analysis of randomized controlled trials

An increased waist-to-hip ratio is a key determinant of atherosclerotic burden in overweight subjects

Highlights from the ACC 2024 Congress

ACC 2024 Congress Coverage