Periodontal disease: associations with diabetes, glycemic control and complications.

OBJECTIVE This report reviews the evidence for adverse effects of diabetes on periodontal health and periodontal disease on glycemic control and complications of diabetes. DESIGN MEDLINE search of the English language literature identified primary research reports published on (a) relationships between diabetes and periodontal diseases since 2000 and (b) effects of periodontal infection on glycemic control and diabetes complications since 1960. RESULTS Observational studies provided consistent evidence of greater prevalence, severity, extent, or progression of at least one manifestation of periodontal disease in 13/17 reports reviewed. Treatment and longitudinal observational studies provided evidence to support periodontal infection having an adverse effect on glycemic control, although not all investigations reported an improvement in glycemic control after periodontal treatment. Additionally, evidence from three observational studies supported periodontal disease increasing the risk for diabetes complications and no published reports refuted the findings. CONCLUSION The evidence reviewed supports diabetes having an adverse effect on periodontal health and periodontal infection having an adverse effect on glycemic control and incidence of diabetes complications. Further rigorous study is necessary to establish unequivocally that treating periodontal infections can contribute to glycemic control management and to the reduction of the burden of diabetes complications.

[1]  P. Baeuerle,et al.  Reactive oxygen intermediates as apparently widely used messengers in the activation of the NF‐kappa B transcription factor and HIV‐1. , 1991, The EMBO journal.

[2]  A. Baird,et al.  Does Periodontal Treatment Improve Glycemic Control in Diabetic Patients? A Meta-analysis of Intervention Studies , 2005, Journal of dental research.

[3]  C. Greenbaum,et al.  Short-term responses to periodontal therapy in insulin-dependent diabetic patients. , 1996, Journal of periodontology.

[4]  J. Beck,et al.  Periodontal Infection as a Possible Risk Factor for Preterm Low Birth Weight. , 1996, Journal of periodontology.

[5]  Y. Khader,et al.  Periodontal status of diabetics compared with nondiabetics: a meta-analysis. , 2006, Journal of diabetes and its complications.

[6]  A. Bascones,et al.  Clinical and metabolic changes after conventional treatment of type 2 diabetic patients with chronic periodontitis. , 2006, Journal of periodontology.

[7]  K. Roberts-Thomson,et al.  Anangu oral health: the status of the Indigenous population of the Anangu Pitjantjatjara lands. , 2004, The Australian journal of rural health.

[8]  A. Schmidt,et al.  The biology of the receptor for advanced glycation end products and its ligands. , 2000, Biochimica et biophysica acta.

[9]  A. Kingman,et al.  Gingival recession, gingival bleeding, and dental calculus in adults 30 years of age and older in the United States, 1988-1994. , 1999, Journal of periodontology.

[10]  G. Maupomé,et al.  Risk factors and prevalence of periodontitis in community-dwelling elders in Mexico. , 2006, Journal of clinical periodontology.

[11]  M. Taba,et al.  Effect of non-surgical periodontal therapy on glycemic control in patients with type 2 diabetes mellitus. , 2003, Journal of periodontology.

[12]  T. Kislinger,et al.  Blockade of receptor for advanced glycation end-products restores effective wound healing in diabetic mice. , 2001, The American journal of pathology.

[13]  U. Skalerič,et al.  Periodontal disease and diabetes metabolic control: a full-mouth disinfection approach. , 2006, Journal of the International Academy of Periodontology.

[14]  J. Lindhe,et al.  The effect of periodontal therapy in diabetics. Results after 5 years. , 1996, Journal of clinical periodontology.

[15]  Brian Burt,et al.  Position paper: epidemiology of periodontal diseases. , 2005, Journal of periodontology.

[16]  P. Papapanou,et al.  Periodontal diseases: epidemiology. , 1996, Annals of periodontology.

[17]  P. Baeuerle The inducible transcription activator NF-κB: regulation by distinct protein subunits , 1991 .

[18]  T. Collins Endothelial nuclear factor-kappa B and the initiation of the atherosclerotic lesion. , 1993, Laboratory investigation; a journal of technical methods and pathology.

[19]  P. Guillausseau,et al.  Rapid Publication , 1971, Nature.

[20]  Nicollerat Ja Implications of the United Kingdom Prospective Diabetes Study , 1998, Diabetes Care.

[21]  H. Murtomaa,et al.  Periodontal treatment needs in a follow-up study among adults with diabetes in Finland , 2003, Acta odontologica Scandinavica.

[22]  R. Holman,et al.  Effect of intensive blood-glucose control with metformin on complications in overweight patients with type 2 diabetes (UKPDS 34) , 1998, The Lancet.

[23]  J M Albandar,et al.  Destructive periodontal disease in adults 30 years of age and older in the United States, 1988-1994. , 1999, Journal of periodontology.

[24]  K. Wikblad,et al.  Type 2 diabetes and oral health: a comparison between diabetic and non-diabetic subjects. , 2000, Diabetes research and clinical practice.

[25]  J. Beck,et al.  PGE2, IL-1 beta, and TNF-alpha responses in diabetics as modifiers of periodontal disease expression. , 1998, Annals of periodontology.

[26]  E. Ogata,et al.  Stimulation of fracture repair by recombinant human basic fibroblast growth factor in normal and streptozotocin-diabetic rats. , 1994, Endocrinology.

[27]  S. Vannucci,et al.  Advanced glycation end products and RAGE: a common thread in aging, diabetes, neurodegeneration, and inflammation. , 2005, Glycobiology.

[28]  W. Knowler,et al.  Severe Periodontitis and Risk for Poor Glycemic Control in Patients with Non-Insulin-Dependent Diabetes Mellitus. , 1996, Journal of periodontology.

[29]  D. Graves,et al.  Diabetes-enhanced Inflammation and Apoptosis—Impact on Periodontal Pathology , 2006, Journal of dental research.

[30]  L. Forman,et al.  Oral health in the elderly with non-insulin-dependent diabetes mellitus. , 2002, Special care in dentistry : official publication of the American Association of Hospital Dentists, the Academy of Dentistry for the Handicapped, and the American Society for Geriatric Dentistry.

[31]  A. Hanlon,et al.  Periodontal treatment by Arestin and its effects on glycemic control in type 1 diabetes patients. , 2004, Journal of the International Academy of Periodontology.

[32]  Hsein-Kun Lu,et al.  Cross-sectional analysis of different variables of patients with non-insulin dependent diabetes and their periodontal status. , 2004, The International journal of periodontics & restorative dentistry.

[33]  E. Baldoni,et al.  Diabetes and periodontal disease: a case-control study. , 2005, Journal of periodontology.

[34]  M. Brownlee Lilly Lecture 1993. Glycation and diabetic complications. , 1994, Diabetes.

[35]  C. Deerochanawong,et al.  The Effect of Periodontal Therapy on Uncontrolled Type 2 Diabetes Mellitus in Older Subjects , 2005 .

[36]  F. Nishimura,et al.  The Periodontal Host Response with Diabetes Pathogenesis of Periodontal Disease in Diabetic Subjects , 2022 .

[37]  D. Barrio,et al.  Advanced glycation end-products (AGEs) induce concerted changes in the osteoblastic expression of their receptor RAGE and in the activation of extracellular signal-regulated kinases (ERK) , 2003, Molecular and Cellular Biochemistry.

[38]  O. Fatusi,et al.  Oral health status in a population of Nigerian diabetics. , 2005, The journal of contemporary dental practice.

[39]  G. Schmalz,et al.  Healing response to non-surgical periodontal therapy in patients with diabetes mellitus: clinical, microbiological, and immunologic results. , 1998, Journal of clinical periodontology.

[40]  W. Knowler,et al.  Effect of Periodontitis on Overt Nephropathy and End-Stage Renal Disease in Type 2 Diabetes , 2007, Diabetes Care.

[41]  David Haber,et al.  Guide to clinical preventive services: a challenge to physician resourcefulness , 1993 .

[42]  Y. Zou,et al.  Survey of the distribution of a newly characterized receptor for advanced glycation end products in tissues. , 1993, The American journal of pathology.

[43]  Jeng-Jong Huang,et al.  Oral and dental manifestations in diabetic and nondiabetic uremic patients receiving hemodialysis. , 2005, Oral surgery, oral medicine, oral pathology, oral radiology, and endodontics.

[44]  D. Bourgeois,et al.  Type 2 diabetes and periodontal indicators : epidemiology in France 2002-2003 , 2006 .

[45]  H. Michie,et al.  Metabolism of Sepsis and Multiple Organ Failure , 1996, World Journal of Surgery.

[46]  R. Bouillon,et al.  Diabetic bone disease , 2007, Calcified Tissue International.

[47]  F. A. Blanco,et al.  Problemas bucodentales en pacientes con diabetes mellitus (II): indice gingival y enfermedad periodontal , 2003 .

[48]  A. Schmidt,et al.  Enhanced interaction of advanced glycation end products with their cellular receptor RAGE: implications for the pathogenesis of accelerated periodontal disease in diabetes. , 1998, Annals of periodontology.

[49]  Plamen Nikolov,et al.  Economic Costs of Diabetes in the U.S. in 2002 , 2003, Diabetes care.

[50]  G. Taylor,et al.  Glycemic control of type 2 diabetes and severe periodontal disease in the US adult population. , 2002, Community dentistry and oral epidemiology.

[51]  G. Taylor Periodontal treatment and its effects on glycemic control: a review of the evidence. , 1999, Oral surgery, oral medicine, oral pathology, oral radiology, and endodontics.

[52]  H. Vlassara Recent progress on the biologic and clinical significance of advanced glycosylation end products. , 1994, The Journal of laboratory and clinical medicine.

[53]  K. Wager,et al.  The effect of periodontal treatment on glycemic control in patients with type 2 diabetes mellitus. , 2001, Journal of clinical periodontology.

[54]  Simon Smyth,et al.  Diabetes and obesity: the twin epidemics , 2006, Nature Medicine.

[55]  D. Graves,et al.  A role for advanced glycation end products in diminished bone healing in type 1 diabetes. , 2003, Diabetes.

[56]  S. Takashiba,et al.  Assessment of interleukin-6 in the pathogenesis of periodontal disease. , 1994, Journal of periodontology.

[57]  D. Graves,et al.  Diabetes interferes with the bone formation by affecting the expression of transcription factors that regulate osteoblast differentiation. , 2003, Endocrinology.

[58]  P. Buekens,et al.  Periodontal disease and gestational diabetes mellitus. , 2005, American journal of obstetrics and gynecology.

[59]  D. Rogers,et al.  The effect of intensive treatment of diabetes on the development and progression of long-term complications in insulin-dependent diabetes mellitus , 1994 .

[60]  J. J. Arrieta-Blanco,et al.  Dental problems in patients with diabetes mellitus (II): gingival index and periodontal disease. , 2003, Medicina oral : organo oficial de la Sociedad Espanola de Medicina Oral y de la Academia Iberoamericana de Patologia y Medicina Bucal.

[61]  G. Taylor,et al.  Periodontitis and gestational diabetes mellitus: exploring the link in NHANES III. , 2006, Journal of public health dentistry.

[62]  M. Matsumoto,et al.  Rage: A Novel Cellular Receptor for Advanced Glycation End Products , 1996, Diabetes.

[63]  James A Rothendler,et al.  Does periodontal care improve glycemic control? The Department of Veterans Affairs Dental Diabetes Study. , 2007, Journal of clinical periodontology.

[64]  G. Taylor Bidirectional interrelationships between diabetes and periodontal diseases: an epidemiologic perspective. , 2001, Annals of periodontology.

[65]  T. Fukuda,et al.  The effect of antimicrobial periodontal treatment on circulating tumor necrosis factor-alpha and glycated hemoglobin level in patients with type 2 diabetes. , 2001, Journal of periodontology.

[66]  C Lindh,et al.  Type 2 diabetes and risk for periodontal disease: a role for dental health awareness. , 2006, Journal of clinical periodontology.

[67]  L. Niskanen,et al.  Periodontal findings in elderly patients with non-insulin dependent diabetes mellitus. , 1998, Journal of periodontology.

[68]  Y. Zou,et al.  Enhanced cellular oxidant stress by the interaction of advanced glycation end products with their receptors/binding proteins. , 1994, The Journal of biological chemistry.

[69]  Jennifer L. Talbert,et al.  The effect of periodontal therapy on TNF-alpha, IL-6 and metabolic control in type 2 diabetics. , 2006, Journal of dental hygiene : JDH.

[70]  A. Schmidt,et al.  Advanced glycation endproducts interacting with their endothelial receptor induce expression of vascular cell adhesion molecule-1 (VCAM-1) in cultured human endothelial cells and in mice. A potential mechanism for the accelerated vasculopathy of diabetes. , 1995, The Journal of clinical investigation.

[71]  R. Holman,et al.  Intensive blood-glucose control with sulphonylureas or insulin compared with conventional treatment and risk of complications in patients with type 2 diabetes (UKPDS 33). UK Prospective Diabetes Study (UKPDS) Group. , 1998 .

[72]  M. Kawanami,et al.  Effect of lifestyle on periodontal disease status in diabetic patients. , 2004, Journal of the International Academy of Periodontology.

[73]  T. Kislinger,et al.  Blockade of RAGE suppresses periodontitis-associated bone loss in diabetic mice. , 2000, The Journal of clinical investigation.

[74]  Robert L Hanson,et al.  Periodontal disease and mortality in type 2 diabetes. , 2005, Diabetes care.

[75]  J. Hood American Academy of Periodontology , 1921 .

[76]  M. Brownlee Glycation and Diabetic Complications , 1994, Diabetes.

[77]  J. Wolf Dental and periodontal conditions in diabetes mellitus. A clinical and radiographic study. , 1977, Proceedings of the Finnish Dental Society. Suomen Hammaslaakariseuran toimituksia.

[78]  V. Çanakçi,et al.  The Influence of Smoking and Non-Insulin-Dependent Diabetes Mellitus on Periodontal Disease , 2002, The Journal of international medical research.

[79]  M. Thornhill,et al.  Endothelial cell leukocyte adhesion molecule-1 (ELAM-1) and intercellular adhesion molecule-1 (ICAM-1) expression in gingival tissue during health and experimentally-induced gingivitis. , 1992, Journal of periodontal research.

[80]  M. Reding,et al.  The relationship between reduction in periodontal inflammation and diabetes control: a report of 9 cases. , 1992, Journal of periodontology.

[81]  R. Schmidt,et al.  Effect of Aminoguanidine on the Frequency of Neuroaxonal Dystrophy in the Superior Mesenteric Sympathetic Autonomic Ganglia of Rats With Streptozocin-Induced Diabetes , 1996, Diabetes.

[82]  N. Istfan,et al.  Differential effects of interleukin-1 receptor antagonist in cytokine- and endotoxin-treated rats. , 1995, The American journal of physiology.

[83]  S. Genuth,et al.  The effect of intensive treatment of diabetes on the development and progression of long-term complications in insulin-dependent diabetes mellitus. , 1993, The New England journal of medicine.

[84]  A. Schmidt,et al.  A murine model of accelerated periodontal disease in diabetes. , 2010, Journal of periodontal research.

[85]  K. Feingold,et al.  Evidence for two classes of cytokines that stimulate hepatic lipogenesis: relationships among tumor necrosis factor, interleukin-1 and interferon-alpha. , 1990, Endocrinology.

[86]  P. Baeuerle The inducible transcription activator NF-kappa B: regulation by distinct protein subunits. , 1991, Biochimica et biophysica acta.

[87]  K. Feingold,et al.  Role of Cytokines in Inducing Hyperlipidemia , 1992, Diabetes.

[88]  J. Ainamo,et al.  A longitudinal study on insulin-dependent diabetes mellitus and periodontal disease. , 1993, Journal of clinical periodontology.

[89]  J. Ainamo,et al.  A site-by-site follow-up study on the effect of controlled versus poorly controlled insulin-dependent diabetes mellitus. , 1994, Journal of clinical periodontology.

[90]  E. Sato,et al.  [Reactive oxygen]. , 2002, Nihon eiseigaku zasshi. Japanese journal of hygiene.

[91]  R. Genco,et al.  Periodontal disease and diabetes mellitus: a two-way relationship. , 1998, Annals of periodontology.

[92]  T. Watts Diabetes mellitus promotes periodontal destruction in children , 2007, BDJ.

[93]  A. Dedić,et al.  [Diabetes mellitus and periodontal diseases]. , 1998, Medicinski arhiv.

[94]  E. Koumantakis,et al.  Gingival condition of women with gestational diabetes on a Greek island. , 2006, Special care in dentistry : official publication of the American Association of Hospital Dentists, the Academy of Dentistry for the Handicapped, and the American Society for Geriatric Dentistry.

[95]  M. Serio,et al.  Multiple cytokines stimulate hepatic lipid synthesis in vivo. , 1989, Endocrinology.

[96]  K. Kuwabara,et al.  Receptor for advanced glycation end products (AGEs) has a central role in vessel wall interactions and gene activation in response to circulating AGE proteins. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[97]  G. Gill,et al.  Oral health in rural South African type 2 diabetic patients , 2006, Tropical doctor.

[98]  S. Etcheverry,et al.  Effect of advanced glycation endproducts on the secretion of insulin-like growth factor-I and its binding proteins: role in osteoblast development , 2001, Acta Diabetologica.

[99]  J. Pickup,et al.  NIDDM as a disease of the innate immune system: association of acute-phase reactants and interleukin-6 with metabolic syndrome X , 1997, Diabetologia.

[100]  S. Genuth Lowering the criterion for impaired fasting glucose is in order. , 2003, Diabetes care.

[101]  A. Schmidt,et al.  Advanced glycation endproducts (AGEs) induce oxidant stress in the gingiva: a potential mechanism underlying accelerated periodontal disease associated with diabetes. , 1996, Journal of periodontal research.

[102]  R. Williams,et al.  Periodontal disease and diabetes in young adults. , 1960, Journal of the American Medical Association.

[103]  S. Huumonen,et al.  Alveolar bone loss in type 1 diabetic subjects. , 2000, Journal of clinical periodontology.

[104]  T. V. Van Dyke,et al.  Association between interleukin-1 genotype and periodontal disease in a diabetic population. , 2003, Journal of periodontology.

[105]  G. Viberti,et al.  Single-blind studies of the effects of improved periodontal health on metabolic control in type 1 diabetes mellitus. , 1995, Journal of clinical periodontology.

[106]  G. Taylor,et al.  Commonality in chronic inflammatory diseases: periodontitis, diabetes, and coronary artery disease. , 2006, Periodontology 2000.

[107]  R. Genco,et al.  Treatment of periodontal disease in diabetics reduces glycated hemoglobin. , 1997, Journal of periodontology.

[108]  M. Erdoğan,et al.  The effect of improved periodontal health on metabolic control in type 2 diabetes mellitus. , 2005, Journal of clinical periodontology.

[109]  A. Hugoson,et al.  Medical status and complications in relation to periodontal disease experience in insulin-dependent diabetics. , 1996, Journal of clinical periodontology.

[110]  R. Genco,et al.  Response to Periodontal Therapy in Diabetics and Smokers. , 1996, Journal of periodontology.