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

Acta Diabetologica - Tập 55 Số 7 - Trang 653-667 - 2018
Gustavo G. Nascimento1, Fábio Renato Manzolli Leite1, Peter Vestergaard2, Flemming Scheutz1, Rodrigo López1
1Section of Periodontology, Department of Dentistry and Oral Health, Aarhus University, Vennelyst Boulevard 9, 8000, Aarhus C, Denmark
2Department of Clinical Medicine, Aalborg University Hospital, Aalborg, Denmark

Tóm tắt

Từ khóa


Tài liệu tham khảo

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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):107–127

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

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

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

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

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):1690–1691

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

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

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

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

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

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

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):328–334

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

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

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

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

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

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

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

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):1119–1129

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

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

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

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):171–178

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):146–152

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):56–61

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

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):2008–2012

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

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

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

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

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

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

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

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):15–21

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

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):7250–7256

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

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

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):65–73

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

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

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

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

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

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

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