Periodontal disease: Associations with diabetes, glycemic control and complications

Oral Diseases

Volumn 14, Issue 3, 2008, Pages 191-203

  Taylor, G W ^a   Borgnakke, W S ^a  

^a UNIVERSITY OF MICHIGAN   (United States)

Author keywords

Diabetes; Epidemiology; Periodontal disease; Periodontal treatment

Indexed keywords

DIABETES MELLITUS; DISEASE ASSOCIATION; DISEASE SEVERITY; GLYCEMIC CONTROL; HUMAN; LONGITUDINAL STUDY; MEDLINE; OBSERVATIONAL STUDY; PERIODONTAL DISEASE; PREVALENCE; PRIORITY JOURNAL; REVIEW;

BLOOD GLUCOSE; DIABETES COMPLICATIONS; DIABETES MELLITUS; GLUCOSE; GLYCOSYLATION END PRODUCTS, ADVANCED; HUMANS; INFLAMMATION MEDIATORS; OXIDATIVE STRESS; PERIODONTAL DISEASES;

EID: 40749099407     PISSN: 1354523X     EISSN: 16010825     Source Type: Journal    
DOI: 10.1111/j.1601-0825.2008.01442.x     Document Type: Review

References (103)

1. Albandar JM, Kingman A (1999). Gingival recession, gingival bleeding, and dental calculus in adults 30 years of age and older in the United States, 1988-1994. J Periodontol 70:30 43.
2. Albandar JM, Brunelle JA, Kingman A (1999). Destructive periodontal disease in adults 30 years of age and older in the United States, 1988-1994. J Periodontol 70:13 29.
3. Aldridge JP, Lester V, Watts TL, Collins A, Viberti G, Wilson RF (1995). Single-blind studies of the effects of improved periodontal health on metabolic control in type 1 diabetes mellitus. J Clin Periodontol 22:271 275.
4. Anonymous (1993). The effect of intensive treatment of diabetes on the development and progression of long-term complications in insulin-dependent diabetes mellitus. The Diabetes Control and Complications Trial Research Group [see comments]. N Engl J Med 329:977 986.
5. Anonymous (1998a). 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.[see comment][erratum appears in Lancet 1999 Aug 14;354(9178):602]. Lancet 352:837 853.
6. Anonymous (1998b). Effect of intensive blood-glucose control with metformin on complications in overweight patients with type 2 diabetes (UKPDS 34). UK Prospective Diabetes Study (UKPDS) Group.[see comment][erratum appears in Lancet 1998 Nov 7;352(9139):1558]. Lancet 352:854 865.
7. Arrieta-Blanco JJ, Bartolome-Villar B, Jimenez-Martinez E, Saavedra-Vallejo P, Arrieta-Blanco FJ (2003). Dental problems in patients with diabetes mellitus (II): gingival index and periodontal disease. Medicina Oral 8:233 247.
8. Baeuerle PA (1991). The inducible transcription activator NF-kappa B: regulation by distinct protein subunits. Biochim Biophys Acta 1072:63 80.
9. Borges-Yáñez SA, Irigoyen-Camacho ME, Maupome G (2006). Risk factors and prevalence of periodontitis in community-dwelling elders in Mexico. J Clin Periodontol 33:184 194.
10. Bouillon R (1991). Diabetic bone disease. Calcif Tissue Int 49:155 160.
11. Brett J, Schmidt AM, Yan SD et al (1993). Survey of the distribution of a newly characterized receptor for advanced glycation end products in tissues. Am J Pathol 143:1699 1712.
12. Brownlee M (1994). Lilly Lecture 1993. Glycation and diabetic complications. Diabetes 43:836 841.
13. Burt BA (2005). Position paper: epidemiology of periodontal diseases. J Periodontol 76:1406 1419.
14. Campus G, Salem A, Uzzau S, Baldoni E, Tonolo G (2005). Diabetes and periodontal disease: a case-control study. J Periodontol 76:418 425.
15. Christgau M, Palitzsch KD, Schmalz G, Kreiner U, Frenzel S (1998). Healing response to non-surgical periodontal therapy in patients with diabetes mellitus: clinical, microbiological, and immunologic results. J Clin Periodontol 25:112 124.
16. Chuang SF, Sung JM, Kuo SC, Huang JJ, Lee SY (2005). Oral and dental manifestations in diabetic and nondiabetic uremic patients receiving hemodialysis. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 99:689 695.
17. Collin HL, Uusitupa M, Niskanen L et al (1998). Periodontal findings in elderly patients with non-insulin dependent diabetes mellitus. J Periodontol 69:962 966.
18. Collins T (1993). Endothelial nuclear factor-kappa B and the initiation of the atherosclerotic lesion. Lab Invest 68:499 508.
19. Cortizo AM, Lettieri MG, Barrio DA, Mercer N, Etcheverry SB, McCarthy AD (2003). 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). Mol Cell Biochem 250:1 10.
20. Endean C, Roberts-Thomson K, Wooley S (2004). Anangu oral health: the status of the Indigenous population of the Anangu Pitjantjatjara lands. Australian Journal of Rural Health 12:99 103.
21. Faria-Almeida R, Navarro A, Bascones A (2006). Clinical and metabolic changes after conventional treatment of type 2 diabetic patients with chronic periodontitis. J Periodontol 77:591 598.
22. Feingold KR, Grunfeld C (1992). Role of cytokines in inducing hyperlipidemia. Diabetes 41:97 101.
23. Feingold KR, Soued M, Serio MK, Moser AH, Dinarello CA, Grunfeld C (1989). Multiple cytokines stimulate hepatic lipid synthesis in vivo. Endocrinology 125:267 274.
24. Genuth S, Eastman R, Kahn R et al (2003). Implications of the United Kingdom prospective diabetes study. Diabetes Care 26 (Suppl. 1 S28 S32.
25. Goova MT, Li J, Kislinger T et al (2001). Blockade of receptor for advanced glycation end-products restores effective wound healing in diabetic mice [see comment]. Am J Pathol 159:513 525.
26. Graves DT, Liu R, Alikhani M, Al-Mashat H, Trackman PC (2006). Diabetes-enhanced inflammation and apoptosis - impact on periodontal pathology. J Dent Res 85:15 21.
27. Grossi SG, Genco RJ (1998). Periodontal disease and diabetes mellitus: a two-way relationship. Ann Periodontol 3:51 61.
28. Grossi SG, Skrepcinski FB, DeCaro T, Zambon JJ, Cummins D, Genco RJ (1996). Response to periodontal therapy in diabetics and smokers. Journal of Periodontology 67:1094 1102.
29. Grossi SG, Skrepcinski FB, DeCaro T et al (1997). Treatment of periodontal disease in diabetics reduces glycated hemoglobin. J Periodontol 68:713 719.
30. Grunfeld C, Soued M, Adi S, Moser AH, Dinarello CA, Feingold KR (1990). Evidence for two classes of cytokines that stimulate hepatic lipogenesis: relationships among tumor necrosis factor, interleukin-1 and interferon-alpha. Endocrinology 127:46 54.
31. Guzman S, Karima M, Wang H-Y, Van Dyke TE (2003). Association between interleukin-1 genotype and periodontal disease in a diabetic population. J Periodontol 74:1183 1190.
32. Harris MI (1995). Summary National Diabetes Data Group. Diabetes in America. 2nd ed. Washington DC:Government Printing Office, pp. 1 13. NIH Publication no. 95-1468 Edition.
33. Hogan P, Dall T, Nikolov P, American Diabetes A (2003). Economic costs of diabetes in the US in 2002. Diabetes Care 26:917 932.
34. Iwamoto Y, Nishimura F, Nakagawa M et al (2001). The effect of antimicrobial periodontal treatment on circulating tumor necrosis factor-alpha and glycated hemoglobin level in patients with type 2 diabetes. J Periodontol 72:774 778.
35. Janket SJ, Wightman A, Baird AE, Van Dyke TE, Jones JA (2005). Does periodontal treatment improve glycemic control in diabetic patients? A meta-analysis of intervention studies [see comment]. J Dent Res 84:1154 1159.
36. Jansson H, Lindholm E, Lindh C, Groop L, Bratthall G (2006). Type 2 diabetes and risk for periodontal disease: a role for dental health awareness. J Clin Periodontol 33:408 414.
37. Jones JA, Miller DR, Wehler CJ et al (2007). Does periodontal care improve glycemic control? The Department of Veterans Affairs Dental Diabetes Study. J Clin Periodontol 34:46 52.
38. Karikoski A, Murtomaa H (2003). Periodontal treatment needs in a follow-up study among adults with diabetes in Finland. Acta Odontol Scand 61:6 10.
39. Kawaguchi H, Kurokawa T, Hanada K et al (1994). Stimulation of fracture repair by recombinant human basic fibroblast growth factor in normal and streptozotocin-diabetic rats. Endocrinology 135:774 781.
40. Khader YS, Dauod AS, El-Qaderi SS, Alkafajei A, Batayha WQ (2006). Periodontal status of diabetics compared with nondiabetics: a meta-analysis [see comment in: Evid Based Dent. 2006;7(2):45; PMID: 16858380]. J Diabetes Complications 20:59 68.
41. Kiran M, Arpak N, Unsal E, Erdoan MF (2005). The effect of improved periodontal health on metabolic control in type 2 diabetes mellitus. J Clin Periodontol 32:266 272.
42. Lalla E, Lamster IB, Feit M, Huang L, Schmidt AM (1998a). A murine model of accelerated periodontal disease in diabetes. J Periodontal Res 33:387 399.
43. Lalla E, Lamster IB, Schmidt AM (1998b). Enhanced interaction of advanced glycation end products with their cellular receptor RAGE: implications for the pathogenesis of accelerated periodontal disease in diabetes. Ann Periodontol 3:13 19.
44. Lalla E, Lamster IB, Feit M et al (2000). Blockade of RAGE suppresses periodontitis-associated bone loss in diabetic mice. J Clin Invest 105:1117 1124.
45. Lalla E, Cheng B, Lal S et al (2007). Diabetes mellitus promotes periodontal destruction in children. J Clin Periodontol 34:294 298.
46. Ling PR, Istfan NW, colon E, Bistrian BR (1995). Differential effects of interleukin-1 receptor antagonist in cytokine- and endotoxin-treated rats. Am J Physiol 268:E255 E261.
47. Lu HK, Yang PC (2004). Cross-sectional analysis of different variables of patients with non-insulin dependent diabetes and their periodontal status. Int J Periodontics Restorative Dent 24:71 79.
48. Lu H, Kraut D, Gerstenfeld LC, Graves DT (2003). Diabetes interferes with the bone formation by affecting the expression of transcription factors that regulate osteoblast differentiation. Endocrinology 144:346 352.
49. Mattout C, Bourgeois D, Bouchard P (2006). Type 2 diabetes and periodontal indicators: epidemiology in France 2002-2003. J Periodontal Res 41:253 258.
50. McCarthy AD, Etcheverry SB, Cortizo AM (2001). Effect of advanced glycation endproducts on the secretion of insulin-like growth factor-I and its binding proteins: role in osteoblast development. Acta Diabetol 38:113 122.
51. Mealey BL, Oates TW, American Academy of Periodontology (2006). Diabetes mellitus and periodontal diseases. J Periodontol 77:1289 1303.
52. Michie HR (1996). Metabolism of sepsis and multiple organ failure. World J Surg 20:460 464.
53. Miller LS, Manwell MA, Newbold D et al (1992). The relationship between reduction in periodontal inflammation and diabetes control: a report of 9 cases. J Periodontol 63:843 848.
54. Mittas E, Erevnidou K, Koumantakis E, Papavasileiou S, Helidonis E (2006). Gingival condition of women with gestational diabetes on a Greek island. Spec Care Dentist 26:214 219.
55. Moughal NA, Adonogianaki E, Thornhill MH, Kinane DF (1992). 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. J Periodontal Res 27:623 630.
56. Negishi J, Kawanami M, Terada Y et al (2004). Effect of lifestyle on periodontal disease status in diabetic patients. J Int Acad Periodontol 6:120 124.
57. Nishimura F, Iwamoto Y, Soga Y (2007). The periodontal host response with diabetes. Periodontol 2000 43:245 253.
58. Novak KF, Taylor GW, Dawson DR, Ferguson JE II., Novak MJ (2006). Periodontitis and gestational diabetes mellitus: exploring the link in NHANES III. J Public Health Dent 66:163 168.
59. Offenbacher S, Katz V, Fertik G et al (1996). Periodontal infection as a possible risk factor for preterm low birth weight. J Periodontol 67:1103 1113.
60. Ogunbodede EO, Fatusi OA, Akintomide A, Kolawole K, Ajayi A (2005). Oral health status in a population of Nigerian diabetics. J Contemp Dent Pract 6:75 84.
61. Orbak R, Tezel A, Canakci V, Demir T (2002). The influence of smoking and non-insulin-dependent diabetes mellitus on periodontal disease. J Int Med Res 30:116 125.
62. Papapanou PN (1996). Periodontal diseases: epidemiology. Ann Periodontol 1:1 36.
63. Peck T, Price C, English P, Gill G (2006). Oral health in rural South African type 2 diabetic patients. Trop Doct 36:111 112.
64. Pickup JC, Mattock MB, Chusney GD, Burt D (1997). NIDDM as a disease of the innate immune system: association of acute-phase reactants and interleukin-6 with metabolic syndrome X. Diabetologia 40:1286 1292.
65. Promsudthi A, Pimapansri S, Deerochanawong C, Kanchanavasita W (2005). The effect of periodontal therapy on uncontrolled type 2 diabetes mellitus in older subjects. Oral Dis 11:293 298.
66. Ramasamy R, Vannucci SJ, Yan SSD, Herold K, Yan SF, Schmidt AM (2005). Advanced glycation end products and RAGE: a common thread in aging, diabetes, neurodegeneration, and inflammation. Glycobiology 15:16R 28R.
67. Rodrigues DC, Taba MJ, Novaes ABJ, Souza SLS, Grisi MFM (2003). Effect of non-surgical periodontal therapy on glycemic control in patients with type 2 diabetes mellitus.[erratum appears in J Periodontol. 2004 May;75(5):780]. J Periodontol 74:1361 1367.
68. Salvi GE, Beck JD, Offenbacher S (1998). PGE2, IL-1 beta, and TNF-alpha responses in diabetics as modifiers of periodontal disease expression. Ann Periodontol 3:40 50.
69. Sandberg GE, Sundberg HE, Fjellstrom CA, Wikblad KF (2000). Type 2 diabetes and oral health: a comparison between diabetic and non-diabetic subjects. Diabetes Res Clin Pract 50:27 34.
70. Santana RB, Xu L, Chase HB, Amar S, Graves DT, Trackman PC (2003). A role for advanced glycation end products in diminished bone healing in type 1 diabetes. Diabetes 52:1502 1510.
71. Saremi A, Nelson RG, Tulloch-Reid M et al (2005). Periodontal disease and mortality in type 2 diabetes. Diabetes Care 28:27 32.
72. Schara R, Medvescek M, Skaleric U (2006). Periodontal disease and diabetes metabolic control: a full-mouth disinfection approach. J Int Acad Periodontol 8:61 66.
73. Schmidt AM, Hasu M, Popov D et al (1994). Receptor for advanced glycation end products (AGEs) has a central role in vessel wall interactions and gene activation in response to circulating AGE proteins. Proc Natl Acad Sci U S A 91:8807 8811.
74. Schmidt AM, Hori O, Chen JX et al (1995). 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. J Clin Invest 96:1395 1403.
75. Schmidt AM, Weidman E, Lalla E et al (1996a). Advanced glycation endproducts (AGEs) induce oxidant stress in the gingiva: a potential mechanism underlying accelerated periodontal disease associated with diabetes. J Periodontal Res 31:508 515.
76. Schmidt AM, Hori O, Cao R et al (1996b). RAGE: a novel cellular receptor for advanced glycation end products. Diabetes 45:S77 S80.
77. Schmidt AM, Yan SD, Yan SF, Stern DM (2000). The biology of the receptor for advanced glycation end products and its ligands. Biochim Biophys Acta 1498:99 111.
78. Schreck R, Rieber P, Baeuerle PA (1991). Reactive oxygen intermediates as apparently widely used messengers in the activation of the NF-kappa B transcription factor and HIV-1. EMBO J 10:2247 2258.
79. Seppala 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 21:161 165.
80. Seppala B, Seppala M, Ainamo J (1993). A longitudinal study on insulin-dependent diabetes mellitus and periodontal disease. J Clin Periodontol 20:161 165.
81. Shultis WA, Weil EJ, Looker HC et al (2007). Effect of periodontitis on overt nephropathy and end-stage renal disease in type 2 diabetes. Diabetes Care 30:306 311.
82. Skaleric U, Schara R, Medvescek M, Hanlon A, Doherty F, Lessem J (2004). Periodontal treatment by Arestin and its effects on glycemic control in type 1 diabetes patients. J Int Acad Periodontol 6:160 165.
83. Smith GT, Greenbaum CJ, Johnson BD, Persson GR (1996). Short-term responses to periodontal therapy in insulin-dependent diabetic patients [published erratum appears in J Periodontol 1996 Dec;67(12):1368]. J Periodontol 67:794 802.
84. Smyth S, Heron A (2006). Diabetes and obesity: the twin epidemics. Nat Med 12:75 80.
85. Southerland JH, Taylor GW, Moss K, Beck JD, Offenbacher S (2006). Commonality in chronic inflammatory diseases: periodontitis, diabetes, and coronary artery disease. Periodontol 2000 40:130 143.
86. Stewart JE, Wager KA, Friedlander AH, Zadeh HH (2001). The effect of periodontal treatment on glycemic control in patients with type 2 diabetes mellitus. J Clin Periodontol 28:306 310.
87. Takahashi K, Takashiba S, Nagai A et al (1994). Assessment of interleukin-6 in the pathogenesis of periodontal disease. J Periodontol 65:147 153.
88. Talbert J, Elter J, Jared HL, Offenbacher S, Southerland J, Wilder RS (2006). The effect of periodontal therapy on TNF-alpha, IL-6 and metabolic control in type 2 diabetics. J Dent Hyg 80:7.
89. Taylor GW (1999). Periodontal treatment and its effects on glycemic control: a review of the evidence. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 87:311 316.
90. Taylor GW (2001). Bidirectional interrelationships between diabetes and periodontal diseases: an epidemiologic perspective. Ann Periodontol 6:99 112.
91. Taylor GW, Burt BA, Becker MP et al (1996). Severe periodontitis and risk for poor glycemic control in patients with non-insulin-dependent diabetes mellitus. J Periodontol 67:1085 1093.
92. Tervonen T, Karjalainen K, Knuuttila M, Huumonen S (2000). Alveolar bone loss in type 1 diabetic subjects. J Clin Periodontol 27:567 571.
93. Thorstensson H, Kuylenstierna J, Hugoson A (1996). Medical status and complications in relation to periodontal disease experience in insulin-dependent diabetics. J Clin Periodontol 23:194 202.
94. Tsai C, Hayes C, Taylor GW (2002). Glycemic control of type 2 diabetes and severe periodontal disease in the US adult population. Community Dent Oral Epidemiol 30:182 192.
95. U.S. Preventive Services Task Force (1996). Guide to clinical preventive services, 2nd edn. Government Printing Office:Washington, DC.
96. Vlassara H (1994). Recent progress on the biologic and clinical significance of advanced glycosylation end products. J Lab Clin Med 124:19 30.
97. Wautier JL, Zoukourian C, Chappey O et al (1996). Receptor-mediated endothelial cell dysfunction in diabetic vasculopathy. Soluble receptor for advanced glycation end products blocks hyperpermeability in diabetic rats. J Clin Invest 97:238 243.
98. Westfelt E, Rylander H, Blohme G, Jonasson P, Lindhe J (1996). The effect of periodontal therapy in diabetics. Results after 5 years. J Clin Periodontol 23:92 100.
99. Williams RC Jr., Mahan CJ (1960). Periodontal disease and diabetes in young adults. JAMA 172:776 778.
100. Wolf J (1977). Dental and periodontal conditions in diabetes mellitus. A clinical and radiographic study. Proc Finn Dent Soc 73:1 56.
101. Xiong X, Buekens P, Vastardis S, Pridjian G (2006). Periodontal disease and gestational diabetes mellitus. Am J Obstet Gynecol 195:1086 1089.
102. Yan SD, Schmidt AM, Anderson GM et al (1994). Enhanced cellular oxidant stress by the interaction of advanced glycation end products with their receptors/binding proteins. J Biol Chem 269:9889 9897.
103. Zielinski MB, Fedele D, Forman LJ, Pomerantz SC (2002). Oral health in the elderly with non-insulin-dependent diabetes mellitus. Spec Care Dentist 22:94 98.