Diabetes, periodontitis, and the subgingival microbiota

Journal of Oral Microbiology

Volumn 2, Issue 2010, 2010, Pages

  Ohlrich, Edward J ^a   Cullinan, Mary P ^a   Leichter, Jonathan W ^a  

^a UNIVERSITY OF OTAGO   (New Zealand)

Author keywords

Diabetes; Metabolic control; Periodontitis; Subgingival microbiota

Indexed keywords

EID: 80052198878     PISSN: None     EISSN: 20002297     Source Type: Journal    
DOI: 10.3402/jom.v2i0.5818     Document Type: Article

References (87)

1. Wild S, Roglic G, Green A, Sicree R, King H. Global prevalence of diabetes: estimates for the year 2000 and projections for 2030. Diabetes Care 2004; 27: 1047-53.
2. Lamster IB, Lalla E, Borgnakke WS, Taylor GW. The relationship between oral health and diabetes mellitus. JAm Dent Assoc 2008; 139: 19S-24S.
3. Loe H. Periodontal disease. The sixth complication of diabetes mellitus. Diabetes Care 1993; 16: 329-34.
4. Nelson RG, Shlossman M, Budding LM, Pettitt DJ, Saad MF, Genco RJ, et al. Periodontal disease and NIDDM in Pima Indians. Diabetes Care 1990; 13: 836-40.
5. Khader YS, Dauod AS, El-Qaderi SS, Alkafajei A, Batayha WQ. Periodontal status of diabetics compared with nondiabetics: a meta-analysis. J Diabetes Complications 2006; 20: 59-68.
6. Cullinan MP, Westerman B, Hamlet SM, Palmer JE, Faddy MJ, Lang NP, et al. A longitudinal study of interleukin-1 gene polymorphisms and periodontal disease in a general adult population. J Clin Periodontol 2001; 28: 1137-44.
7. Rylander H, Ramberg P, Blohme G, Lindhe J. Prevalence of periodontal disease in young diabetics. J Clin Periodontol 1986; 14: 38-43.
8. Cianciola LJ, Park BH, Bruck E, Mosovich L, Genco RJ. Prevalence of periodontal disease in insulin-dependent diabetes mellitus (juvenile diabetes). J Am Dent Assoc 1982; 104: 653-60.
9. Thorstensson H, Hugoson A. Periodontal disease experience in adult long-duration insulin-dependent diabetics. J Clin Periodontol 1993; 20: 352-8.
10. Emrich LJ, Shlossman M, Genco RJ. Periodontal disease in non-insulin-dependent diabetes mellitus. J Periodontol 1991; 62: 123-31.
11. Taylor GW, Burt BA, Becker MP, Genco RJ, Shlossman M. Glycemic control and alveolar bone loss progression in type 2 diabetes. Ann Periodontol 1998; 3: 30-9.
12. Tervonen T, Oliver RC. Long-term control of diabetes mellitus and periodontitis. J Clin Periodontol 1993; 20: 431-5.
13. Tervonen T, Karjalainen K, Knuuttila M, Huumonen S. Alveolar bone loss in type 1 diabetic subjects. J Clin Periodontol 2000; 27: 567-71.
14. Seppala B, Ainamo J. A site-by-site follow-up study on the effect of controlled versus poorly controlled insulin-dependent diabetes mellitus. J Clin Periodontol 1994; 21: 161-5.
15. Seppala B, Seppala M, Ainamo J. A longitudinal study on insulin-dependent diabetes mellitus and periodontal disease. J Clin Periodontol 1993; 20: 161-5.
16. Loe H, Theilade E, Jensen SB. Experimental gingivitis in man. J Periodontol 1965; 36: 177-87.
17. Lindhe J, Nyman S. Scaling and granulation tissue removal in periodontal therapy. J Clin Periodontol 1985; 12: 374-88.
18. Axelsson P, Lindhe J. The significance of maintenance care in the treatment of periodontal disease. J Clin Periodontol 1981; 8: 281-94.
19. Rosling B, Nyman S, Lindhe J. The effect of systematic plaque control on bone regeneration in infrabony pockets. J Clin Periodontol 1976; 3: 38-53.
20. Gemmell E, Marshall RI, Seymour GJ. Cytokines and prostaglandins in immune homeostasis and tissue destruction in periodontal disease. Periodontol 2000 1997; 14: 112-43.
21. Loesche WJ. Clinical and microbiological aspects of chemotherapeutic agents used according to the specific plaque hypothesis. J Dent Res 1979; 58: 2404-12.
22. Hamlet SM, Cullinan MP, Westerman B, Lindeman M, Bird PS, Palmer J, et al. Distribution of Actinobacillus actinomycetemcomitans, Porphyromonas gingivalis and Prevotella intermedia in an Australian population. J Clin Periodontol 2001; 28: 1163-71.
23. Marsh PD. Are dental diseases examples of ecological catastrophes? Microbiology 2003; 149: 279-94.
24. Mandell RL, Dirienzo J, Kent R, Joshipura K, Haber J. Microbiology of healthy and diseased periodontal sites in poorly controlled insulin dependent diabetics. J Periodontol 1992; 63: 274-9.
25. Mashimo PA, Yamamoto Y, Slots J, Park BH, Genco RJ. The periodontal microflora of juvenile diabetics. Culture, immunofluorescence, and serum antibody studies. J Periodontol 1983; 54: 420-30.
26. Thorstensson H, Dahlen G, Hugoson A. Some suspected periodontopathogens and serum antibody response in adult long-duration insulin-dependent diabetics. J Clin Periodontol 1995; 22: 449-58.
27. Sastrowijoto SH, Hillemans P, van Steenbergen TJ, Abraham-Inpijn L, de Graaff J. Periodontal condition and microbiology of healthy and diseased periodontal pockets in type 1 diabetes mellitus patients. J Clin Periodontol 1989; 16: 316-22.
28. Sastrowijoto SH, van der Velden U, van Steenbergen TJ, Hillemans P, Hart AA, de Graaff J, et al. Improved metabolic control, clinical periodontal status and subgingival microbiology in insulin-dependent diabetes mellitus. A prospective study. J Clin Periodontol 1990; 17: 233-42.
29. Sbordone L, Ramaglia L, Barone A, Ciaglia RN, Iacono VJ. Periodontal status and subgingival microbiota of insulin-dependent juvenile diabetics: a 3-year longitudinal study. J Periodontol 1998; 69: 120-8.
30. Sbordone L, Ramaglia L, Barone A, Ciaglia RN, Tenore A, Iacono VJ. Periodontal status and selected cultivable anaerobic microflora of insulin-dependent juvenile diabetics. J Periodontol 1995; 66: 452-61.
31. Hintao J, Teanpaisan R, Chongsuvivatwong V, Ratarasan C, Dahlen G. The microbiological profiles of saliva, supragingival and subgingival plaque and dental caries in adults with and without type 2 diabetes mellitus. Oral Microbiol Immunol 2007; 22: 175-81.
32. Lalla E, Kaplan S, Chang SM, Roth GA, Celenti R, Hinckley K, et al. Periodontal infection profiles in type 1 diabetes. J Clin Periodontol 2006; 33: 855-62.
33. Ebersole JL, Holt SC, Hansard R, Novak MJ. Microbiologic and immunologic characteristics of periodontal disease in Hispanic Americans with type 2 diabetes. J Periodontol 2008; 79: 637-46.
34. Campus G, Salem A, Uzzau S, Baldoni E, Tonolo G. Diabetes and periodontal disease: a case-control study. J Periodontol 2005; 76: 418-25.
35. Ojima M, Takeda M, Yoshioka H, Nomura M, Tanaka N, Kato T, et al. Relationship of periodontal bacterium genotypic variations with periodontitis in type 2 diabetic patients. Diabetes Care 2005; 28: 433-4.
36. Griffiths GS. Formation, collection and significance of gingival crevice fluid. Periodontol 2000 2003; 31: 32-42.
37. Socransky SS, Haffajee AD. Periodontal microbial ecology. Periodontol 2000 2005; 31: 135-87.
38. Ficara AJ, Levin MP, Grower MF, Kramer GD. A comparison of the glucose and protein content of gingival fluid from diabetics and nondiabetics. J Periodontal Res 1975; 10: 171-5.
39. Socransky SS, Haffajee AD, Cugini MA, Smith C, Kent RL Jr. Microbial complexes in subgingival plaque. J Clin Periodontol 1998; 25: 134-44.
40. Kolenbrander PE, Andersen RN, Blehert DS, Egland PG, Foster JS, Palmer RJ Jr. Communication among oral bacteria. Microbiol Mol Biol Rev 2002; 66: 486-505.
41. Willershausen-Zonnchen B, Lemmen C, Hamm G. Influence of high glucose concentrations on glycosaminoglycan and collagen synthesis in cultured human gingival fibroblasts. J Clin Periodontol 1991; 18: 190-5.
42. Kent MJ, Light ND, Bailey AJ. Evidence for glucose-mediated covalent cross-linking of collagen after glycosylation in vitro. Biochem J 1985; 225: 745-52.
43. Schnider SL, Kohn RR. Effects of age and diabetes mellitus on the solubility and nonenzymatic glucosylation of human skin collagen. J Clin Invest 1981; 67: 1630-5.
44. Frantzis TG, Reeve CM, Brown AL Jr. The ultrastructure of capillary basement membranes in the attached gingiva of diabetic and nondiabetic patients with periodontal disease. J Periodontol 1971; 42: 406-11.
45. Listgarten MA, Ricker FH Jr, Laster L, Shapiro J, Cohen DW. Vascular basement lamina thickness in the normal and inflamed gingiva of diabetics and non-diabetics. J Periodontol 1974; 45: 676-84.
46. Johnson LL, Dyer R, Hupe DJ. Matrix metalloproteinases. Curr Opin Chem Biol 1998; 2: 466-71.
47. Ramamurthy NS, Golub LM. Diabetes increases collagenase activity in extracts of rat gingiva and skin. J Periodontal Res 1983; 18: 23-30.
48. Ramamurthy NS, Zebrowski EJ, Golub LM. Insulin reversal of alloxan-diabetes induced changes in gingival collagen metabolism of the rat. J Periodontal Res 1974; 9: 199-206.
49. Hart TC, Shapira L, Van Dyke TE. Neutrophil defects as risk factors for periodontal diseases. J Periodontol 1994; 65: 521-9.
50. Bissada NF, Manouchehr-Pour M, Haddow M, Spagnuolo PJ. Neutrophil functional activity in juvenile and adult onset diabetic patients with mild and severe periodontitis. J Periodontal Res 1982; 17: 500-2.
51. Manouchehr-Pour M, Spagnuolo PJ, Rodman HM, Bissada NF. Comparison of neutrophil chemotactic response in diabetic patients with mild and severe periodontal disease. J Periodontol 1981; 52: 410-5.
52. Manouchehr-Pour M, Spagnuolo PJ, Rodman HM, Bissada NF. Impaired neutrophil chemotaxis in diabetic patients with severe periodontitis. J Dent Res 1981; 60: 729-30.
53. Salvi GE, Collins JG, Yalda B, Arnold RR, Lang NP, Offenbacher S. Monocytic TNF alpha secretion patterns in IDDM patients with periodontal diseases. J Clin Periodontol 1997; 24: 8-16.
54. Salvi GE, Yalda B, Collins JG, Jones BH, Smith FW, Arnold RR, et al. Inflammatory mediator response as a potential risk marker for periodontal diseases in insulin-dependent diabetes mellitus patients. J Periodontol 1997; 68: 127-35.
55. Reynolds JJ, Meikle MC. Mechanisms of connective tissue matrix destruction in periodontitis. Periodontol 2000 1997; 14: 144-57.
56. Kardesler L, Biyikoglu B, Cetinkalp S, Pitkala M, Sorsa T, Buduneli N. Crevicular fluid matrix metalloproteinase-8, -13, and TIMP-1 levels in type 2 diabetics. Oral Dis 2010; 16: 476-81.
57. Lalla E, Lamster IB, Drury S, Fu C, Schmidt AM. Hyperglycemia, glycoxidation and receptor for advanced glycation endproducts: potential mechanisms underlying diabetic complications, including diabetes-associated periodontitis. Periodontol 2000 2000; 23: 50-62.
58. Taylor GW, Burt BA, Becker MP, Genco RJ, Shlossman M, Knowler WC, et al. Severe periodontitis and risk for poor glycemic control in patients with non-insulin-dependent diabetes mellitus. J Periodontol 1996; 67: 1085-93.
59. Skaleric U, Schara R, Medvescek M, Hanlon A, Doherty F, Lessem J. Periodontal treatment by Arestin and its effects on glycemic control in type 1 diabetes patients. J Int Acad Periodontol 2004; 6: 160-5.
60. Kiran M, Arpak N, Unsal E, Erdogan MF. The effect of improved periodontal health on metabolic control in type 2 diabetes mellitus. J Clin Periodontol 2005; 32: 266-72.
61. Rodrigues DC, Taba MJ, Novaes AB, Souza SL, Grisi MF. Effect of non-surgical periodontal therapy on glycemic control in patients with type 2 diabetes mellitus. J Periodontol 2003; 74: 1361-7.
62. Aldridge JP, Lester V, Watts TL, Collins A, Viberti G, Wilson RF. Single-blind studies of the effects of improved periodontal health on metabolic control in type 1 diabetes mellitus. J Clin Periodontol 1995; 22: 271-5.
63. Tervonen T, Lamminsalo S, Hiltunen L, Raunio T, Knuuttila M. Resolution of periodontal inflammation does not guarantee improved glycemic control in type 1 diabetic subjects. J Clin Periodontol 2009; 36: 51-7.
64. Jones JA, Miller DR, Wehler CJ, Rich SE, Krall-Kaye EA, McCoy LC, et al. Does periodontal care improve glycemic control? The Department of Veterans Affairs Dental Diabetes Study. J Clin Periodontol 2007; 34: 46-52.
65. Grossi SG, Skrepcinski FB, DeCaro T, Robertson DC, Ho AW, Dunford RG, et al. Treatment of periodontal disease in diabetics reduces glycated hemoglobin. J Periodontol 1997; 68: 713-9.
66. Janket SJ, Wightman A, Baird AE, Van Dyke TE, Jones JA. Does periodontal treatment improve glycemic control in diabetic patients? A meta-analysis of intervention studies. J Dent Res 2005; 84: 1154-9.
67. Simpson TC, Needleman I, Wild SH, Moles DR, Mills EJ. Treatment of periodontal disease for glycaemic control in people with diabetes. Cochrane Database Syst Rev 2010; 5: CD004714.
68. Teeuw WJ, Gerdes VE, Loos BG. Effect of periodontal treatment on glycemic control of diabetic patients: a systematic review and meta-analysis. Diabetes Care 2010; 33: 421-7.
69. Khaw KT, Wareham N, Luben R, Bingham S, Oakes S, Welch A, et al. Glycated haemoglobin, diabetes, and mortality in men in Norfolk cohort of European prospective investigation of cancer and nutrition (EPIC-Norfolk). BMJ 2001; 322: 15-8.
70. Preshaw PM, Foster N, Taylor JJ. Cross-susceptibility between periodontal disease and type 2 diabetes mellitus: an immunobiological perspective. Periodontol 2000 2007; 45: 138-57.
71. Nesse W, Linde A, Abbas F, Spijkervet FK, Dijkstra PU, de Brabander EC, et al. Dose-response relationship between periodontal inflamed surface area and HbA1c in type 2 diabetics. J Clin Periodontol 2009; 36: 295-300.
72. Noack B, Genco RJ, Trevisan M, Grossi S, Zambon JJ, De Nardin E. Periodontal infections contribute to elevated systemic C-reactive protein level. J Periodontol 2001; 72: 1221-7.
73. Slade GD, Offenbacher S, Beck JD, Heiss G, Pankow JS. Acutephase inflammatory response to periodontal disease in the US population. J Dent Res 2000; 79: 49-57.
74. Loos BG, Craandijk J, Hoek FJ, Wertheim-van Dillen PM, van der Velden U. Elevation of systemic markers related to cardiovascular diseases in the peripheral blood of periodontitis patients. J Periodontol 2000; 71: 1528-34.
75. Yamazaki K, Honda T, Oda T, Ueki-Maruyama K, Nakajima T, Yoshie H, et al. Effect of periodontal treatment on the Creactive protein and proinflammatory cytokine levels in Japanese periodontitis patients. J Periodontal Res 2005; 40: 53-8.
76. Engebretson S, Chertog R, Nichols A, Hey-Hadavi J, Celenti R, Grbic J. Plasma levels of tumour necrosis factor-alpha in patients with chronic periodontitis and type 2 diabetes. J Clin Periodontol 2007; 34: 18-24.
77. Havemose-Poulsen A, Sorensen LK, Stoltze K, Bendtzen K, Holmstrup P. Cytokine profiles in peripheral blood and whole blood cell cultures associated with aggressive periodontitis, juvenile idiopathic arthritis, and rheumatoid arthritis. J Periodontol 2005; 76: 2276-85.
78. D'Aiuto F, Parkar M, Andreou G, Suvan J, Brett PM, Ready D, et al. Periodontitis and systemic inflammation: control of the local infection is associated with a reduction in serum inflammatory markers. J Dent Res 2004; 83: 156-60.
79. Papapanou P, Behle JH. Mechanisms linking periodontitis to systemic disease. In: Henderson B, Curtis MA, Seymour RM, Donos N, eds. Periodontal medicine and systems biology. Oxford: Blackwell Publishing; 2009. p. 97-116.
80. Crasta K, Daly CG, Mitchell D, Curtis B, Stewart D, Heitz-Mayfield LJ. Bacteraemia due to dental flossing. J Clin Periodontol 2009; 36: 323-32.
81. Forner L, Larsen T, Kilian M, Holmstrup P. Incidence of bacteremia after chewing, tooth brushing and scaling in individuals with periodontal inflammation. J Clin Periodontol 2006; 33: 401-7.
82. Mattila KJ, Nieminen MS, Valtonen VV, Rasi VP, Kesaniemi YA, Syrjala SL, et al. Association between dental health and acute myocardial infarction. BMJ 1989; 298: 779-81.
83. Offenbacher S, Katz V, Fertik G, Collins J, Boyd D, Maynor G, et al. Periodontal infection as a possible risk factor for preterm low birth weight. J Periodontol 1996; 67: 1103-13.
84. Ford PJ, Gemmell E, Hamlet SM, Hasan A, Walker PJ, West MJ, et al. Cross-reactivity of GroEL antibodies with human heat shock protein 60 and quantification of pathogens in atherosclerosis. Oral Microbiol Immunol 2005; 20: 296-302.
85. Yamazaki K, Ohsawa Y, Tabeta K, Ito H, Ueki K, Oda T, et al. Accumulation of human heat shock protein 60-reactive T cells in the gingival tissues of periodontitis patients. Infect Immun 2002; 70: 2492-501.
86. Seymour GJ, Ford PJ, Cullinan MP, Leishman S, West MJ, Yamazaki K. Infection or inflammation: the link between periodontal and cardiovascular diseases. Future Cardiol 2009; 5: 5-9.
87. Seymour GJ, Ford PJ, Cullinan MP, Leishman S, Yamazaki K. Relationship between periodontal infections and systemic disease. Clin Microbiol Infect 2007; 13: 3-10.