Advertisement

Diabetes and Periodontal Disease

  • Thomas W. Oates
  • Namita Khandelwal
Reference work entry
Part of the Endocrinology book series (ENDOCR)

Abstract

Periodontal disease represents an inflammation-driven insult to the supporting tissues of the dentition. It is a chronic, complex disease developing from an altered inflammatory response in association with a pathogenically evolving polymicrobial infection. This complex inflammatory state has a direct impact on the supporting tissues of the dentition along with the potential for systemic sequelae with diabetes. This review explores our current understanding of the impact of diabetes on periodontal disease and dental impalnt therapy as well as the potential impact of periodontal disease on diabetes.

Keywords

Periodontal Diabetes mellitus Dental implant Inflammation Pathogenesis 

References

  1. Abdulwassie H, Dhanrajani PJ. Diabetes mellitus and dental implants: a clinical study. Implant Dent. 2002;11:83–6.CrossRefGoogle Scholar
  2. Amir G, Rosenmann E, Sherman Y, Greenfeld Z, Ne’eman Z, Cohen AM. Osteoporosis in the Cohen diabetic rat: correlation between histomorphometric changes in bone and microangiopathy. Lab Invest. 2002;82(10):1399–405.CrossRefGoogle Scholar
  3. Balshi TJ, Wolfinger GJ. Dental implants in the diabetic patient: a retrospective study. Implant Dent. 1999;8:355–9.CrossRefGoogle Scholar
  4. Barewal RM, Oates TW, Meredith N, Cochran DL. Resonance frequency measurement of implant stability in vivo on implants with a sandblasted and acid-etched surface. Int J Oral Maxillofac Implants. 2003;18(5):641–51.PubMedGoogle Scholar
  5. Beck J, Garcia R, Heiss G, Vokonas PS, Offenbacher S. Periodontal disease and cardiovascular disease. J Periodontol. 1996;67(10 Suppl):1123–37.CrossRefGoogle Scholar
  6. Botero JE, González AM, Mercado RA, Olave G, Contreras A. Subgingival microbiota in peri-implant mucosa lesions and adjacent teeth in partially edentulous patients. J Periodontol. 2005;76(9):1490–5.CrossRefGoogle Scholar
  7. Botero JE, Yepes FL, Roldán N, et al. Tooth and periodontal clinical attachment loss are associated with hyperglycemia in patients with diabetes. J Periodontol. 2012;83:1245–50.CrossRefGoogle Scholar
  8. Botero JE, Rodríguez C, Agudelo-Suarez AA. Periodontal treatment and glycaemic control in patients with diabetes and periodontitis: an umbrella review. Aust Dent J. 2016;61(2):134–48.CrossRefGoogle Scholar
  9. Casap N, Nimri S, Ziv E, Sela J, Samuni Y. Type 2 diabetes has minimal effect on osseointegration of titanium implants in psammomys obesus. Clin Oral Implants Res. 2008;19:458–64.CrossRefGoogle Scholar
  10. Chávarry NG, Vettore MV, Sansone C, Sheiham A. The relationship between diabetes mellitus and destructive periodontal disease: a meta-analysis. Oral Health Prev Dent. 2009;7:107–27.PubMedGoogle Scholar
  11. Cohen A, Horton ES. Progress in the treatment of type 2 diabetes: new pharmacologic approaches to improve glycemic control. Curr Med Res Opin. 2007;23:905–17.CrossRefGoogle Scholar
  12. Corbella S, Francetti L, Taschieri S, De Siena F, Fabbro MD. Effect of periodontal treatment on glycemic control of patients with diabetes: a systematic review and meta-analysis. J Diabetes Investig. 2013;4(5):502–9.CrossRefGoogle Scholar
  13. Costa FO, Miranda Cota LO, Pereira Lages EJ, Soares Dutra Oliveira AM, Dutra Oliveira PA, Cyrino RM, Medeiros Lorentz TC, Cortelli SC, Cortelli JR. Progression of periodontitis and tooth loss associated with glycemic control in individuals undergoing periodontal maintenance therapy: a 5-year follow-up study. J Periodontol. 2013;84(5):595–605.CrossRefGoogle Scholar
  14. Delamaire M, Maugendre D, Moreno M, Le Goff MC, Allannic H, Genetet B. Impaired leucocyte functions in diabetic patients. Diabet Med. 1997;14(1):29–34.CrossRefGoogle Scholar
  15. Demmer RT, Papapanou PN. Epidemiologic patterns of chronic and aggressive periodontitis. Periodontol 2000. 2010;53:28–44.CrossRefGoogle Scholar
  16. Dowell S, Oates TW, Robinson M. Implant success in people with type 2 diabetes mellitus with varying glycemic control: a pilot study. J Am Dent Assoc. 2007;138:355–61.CrossRefGoogle Scholar
  17. Emrich LJ, Shlossman M, Genco RJ. Periodontal disease in non-insulin-dependent diabetes mellitus. J Periodontol. 1991;62(2):123–31.CrossRefGoogle Scholar
  18. Faggion CM Jr, Cullinan MP, Atieh M. An overview of systematic reviews on the effectiveness of periodontal treatment to improve glycaemic control. J Periodontal Res. 2016;51(6):716–25.CrossRefGoogle Scholar
  19. Farzad P, Andersson L, Nyberg J. Dental implant treatment in diabetic patients. Implant Dent. 2002;11:262–7.CrossRefGoogle Scholar
  20. Fiorellini JP, Chen PK, Nevins M, Nevins ML. A retrospective study of dental implants in diabetic patients. Int J Periodontics Restorative Dent. 2000;20:366–73.PubMedGoogle Scholar
  21. Funk JR, Hale JE, Carmines D, Gooch HL, Hurwitz SR. Biomechanical evaluation of early fracture healing in normal and diabetic rats. J Orthop Res. 2000;18(1):126–32.CrossRefGoogle Scholar
  22. Gallacher SJ, Thomson G, Fraser WD, Fisher BM, Gemmell CG, MacCuish AC. Neutrophil bactericidal function in diabetes mellitus: evidence for association with blood glucose control. Diabet Med. 1995;12(10):916–20.CrossRefGoogle Scholar
  23. Ghiraldini B, Conte A, Casarin RC, Casati MZ, Pimentel SP, Cirano FR, Ribeiro FV. Influence of glycemic control on peri-implant bone healing: 12-month outcomes of local release of bone-related factors and implant stabilization in type 2 diabetics. Clin Implant Dent Relat Res. 2016;18(4):801–9.CrossRefGoogle Scholar
  24. Glossary of Periodontal Terms, 4th ed, Copyright 2001 by The American Academy of Periodontology, Suite 800, 737 North Michigan Avenue, Chicago, Illinois 60611-2690.Google Scholar
  25. Hajishengallis G. Immunomicrobial pathogenesis of periodontitis: keystones, pathobionts, and host response. Trends Immunol. 2014;35(1):3–11.CrossRefGoogle Scholar
  26. Jiao Y, Hasegawa M, Inohara N. The role of oral pathobionts in dysbiosis during periodontitis development. J Dent Res. 2014;93(6):539–46.CrossRefGoogle Scholar
  27. Kapp JM, Boren SA, Yun S, LeMaster J. Diabetes and tooth loss in a national sample of dentate adults reporting annual dental visits. Prev Chronic Dis. 2007;4(3):A59.PubMedPubMedCentralGoogle Scholar
  28. Kapur KK, Garrett NR, Hamada MO, et al. Randomized clinical trial comparing the efficacy of mandibular implant-supported overdentures and conventional dentures in diabetic patients. Part III: comparisons of patient satisfaction. J Prosthet Dent. 1999;82(4):416–27.CrossRefGoogle Scholar
  29. Kaur G, Holtfreter B, Rathmann W, Schwahn C, Wallaschofski H, Schipf S, Nauck M, Kocher T. Association between type 1 and type 2 diabetes with periodontal disease and tooth loss. J Clin Periodontol. 2009;36(9):765–74.CrossRefGoogle Scholar
  30. Khader YS, Dauod AS, El-Qaderi SS, Alkafajei A, Batayha WQ. Periodontal status of diabetics compared with nondiabetics: a meta-analysis. J Diabet Complications. 2006;20:59–68.CrossRefGoogle Scholar
  31. Khandelwal N, Oates TW, Vargas A, Alexander PP, Schoolfield JD, Alex McMahan C. Conventional SLA and chemically modified SLA implants in patients with poorly controlled type 2 Diabetes mellitus – a randomized controlled trial. Clin Oral Implants Res. 2013;24:13–9.CrossRefGoogle Scholar
  32. Knight ET, Leichter JW, Tawse-Smith A, Thomson WM. Quantifying the association between self-reported diabetes and periodontitis in the New Zealand population. J Periodontol. 2015;86(8):945–54.CrossRefGoogle Scholar
  33. Koenig RJ, Peterson CM, Jones RL, Saudek C, Lehrman M, Cerami A. Correlation of glucose regulation and hemoglobin A1c in diabetes mellitus. N Engl J Med. 1976;295:417–20.CrossRefGoogle Scholar
  34. Kowall B, Holtfreter B, Völzke H, Schipf S, Mundt T, Rathmann W, Kocher T. Pre-diabetes and well-controlled diabetes are not associated with periodontal disease: the SHIP Trend Study. J Clin Periodontol. 2015;42(5):422–30.CrossRefGoogle Scholar
  35. Lalla E, Papapanou PN. Diabetes mellitus and periodontitis: a tale of two common interrelated diseases. Nat Rev Endocrinol. 2011;7(12):738–48.CrossRefGoogle Scholar
  36. Lalla E, et al. Periodontal changes in children and adolescents with diabetes: a case–control study. Diabetes Care. 2006;29:295–9.CrossRefGoogle Scholar
  37. Lalla E, et al. Diabetes mellitus promotes periodontal destruction in children. J Clin Periodontol. 2007;34:294–8.CrossRefGoogle Scholar
  38. Lamont RJ, Hajishengallis G. Polymicrobial synergy and dysbiosis in inflammatory disease. Trends Mol Med. 2015;21(3):172–83.CrossRefGoogle Scholar
  39. Li Q, Hao S, Fang J, Xie J, Kong XH, Yang JX. Effect of non-surgical periodontal treatment on glycemic control of patients with diabetes: a meta-analysis of randomized controlled trials. Trials. 2015;16:291.CrossRefGoogle Scholar
  40. López NJ, Uribe S, Martinez B. Effect of periodontal treatment on preterm birth rate: a systematic review of metaanalyses. Periodontol 2000. 2015;67(1):87–130.CrossRefGoogle Scholar
  41. Lu H, Kraut D, Gerstenfeld LC, Graves DT. Diabetes interferes with the bone formation by affecting the expression of transcription factors that regulate osteoblast differentiation. Endocrinology. 2003;144(1):346–52.CrossRefGoogle Scholar
  42. Maruyama N, Maruyama F, Takeuchi Y, Aikawa C, Izumi Y, Nakagawa I. Intraindividual variation in core microbiota in peri-implantitis and periodontitis. Sci Rep. 2014;13(4):6602.Google Scholar
  43. McMahon MM, Bistrian BR. Host defenses and susceptibility to infection in patients with diabetes mellitus. Infect Dis Clin North Am. 1995;9(1):1–9.PubMedGoogle Scholar
  44. Mealey BL, Rethman MP. Periodontal disease and diabetes mellitus. Bidirectional relationship. Dent Today. 2003;22(4):107–13.PubMedGoogle Scholar
  45. Michaeli E, Weinberg I, Nahlieli O. Dental implants in the diabetic patient: systemic and rehabilitative considerations. Quintessence Int. 2009;40(8):639–45.PubMedGoogle Scholar
  46. Morris HF, Ochi S, Winkler S. Implant survival in patients with type 2 diabetes: placement to 36 months. Ann Periodontol. 2000;5:157–65.CrossRefGoogle Scholar
  47. Moy PK, Medina D, Shetty V, Aghaloo TL. Dental implant failure rates and associated risk factors. Int J Oral Maxillofac Implants. 2005;20(4):569–77.PubMedGoogle Scholar
  48. Nelson RG, Shlossman M, Budding LM, Pettitt DJ, Saad MF, Genco RJ, Knowler WC. Periodontal disease and NIDDM in Pima Indians. Diabetes Care. 1990;13(8):836–40.CrossRefGoogle Scholar
  49. Oates TW, Dowell S, Robinson M, McMahan CA. Glycemic control and implant stabilization in type 2 diabetes mellitus. J Dent Res. 2009;88:367–71.CrossRefGoogle Scholar
  50. Oates TW, Huynh-Ba G, Vargas A, Alexander P, Feine J. A critical review of diabetes, glycemic control, and dental implant therapy. Clin Oral Implants Res. 2013;24(2):117–27.CrossRefGoogle Scholar
  51. Oates TW, Galloway P, Alexander P, Vargas Green A, Huynh-Ba G, Feine J, McMahan CA. The effects of elevated hemoglobin A(1c) in patients with type 2 diabetes mellitus on dental implants: survival and stability at one year. J Am Dent Assoc. 2014;145(12):1218–26.CrossRefGoogle Scholar
  52. Offenbacher S, Katz V, Fertik G, Collins J, Boyd D, Maynor G, McKaig R, Beck J. Periodontal infection as a possible risk factor for preterm low birth weight. J Periodontol. 1996;67(10 Suppl):1103–13.CrossRefGoogle Scholar
  53. Oliver RC, Tervonen T. Periodontitis and tooth loss: comparing diabetics with the general population. J Am Dent Assoc. 1993;124(12):71–6.CrossRefGoogle Scholar
  54. Olson JW, Shernoff F, Tarlow JL, Colwell JA, Scheetz JP, Bingham SF. Dental endosseous implant assessments in a type 2 diabetic population: A prospective study. Int J Oral Maxillofac Implants. 2000;15:811–21.PubMedGoogle Scholar
  55. Pearl SH, Kanat IO. Diabetes and healing: a review of the literature. J Foot Surg. 1988;27(3):268–70.PubMedGoogle Scholar
  56. Peled M, Ardekian L, Tagger-Green N, Gutmacher Z, Machtei EE. Dental implants in patients with type 2 diabetes mellitus: a clinical study. Implant Dent. 2003;12:116–22.CrossRefGoogle Scholar
  57. Polyzos NP, Polyzos IP, Zavos A, Valachis A, Mauri D, Papanikolaou EG, Tzioras S, Weber D, Messinis IE. Obstetric outcomes after treatment of periodontal disease during pregnancy: systematic review and meta-analysis. BMJ. 2010;341:c7017. (need approval to use figure 6 from publication)CrossRefGoogle Scholar
  58. Pranckeviciene A, Siudikiene J, Ostrauskas R, Machiulskiene V. Severity of periodontal disease in adult patients with diabetes mellitus in relation to the type of diabetes. Biomed Pap Med Fac Univ Palacky Olomouc Czech Repub. 2014;158(1):117–23.CrossRefGoogle Scholar
  59. Preshaw PM, Alba AL, Herrera D, Jepsen S, Konstantinidis A, Makrilakis K, Taylor R. Periodontitis and diabetes: a two-way relationship. Diabetologia. 2012;55(1):21–31.CrossRefGoogle Scholar
  60. Quandt SA, Bell RA, Snively BM, et al. Dietary fat reduction behaviors among African American, American Indian, and white older adults with diabetes. J Nutr Elder. 2009;28(2):143–57.CrossRefGoogle Scholar
  61. Renvert S, Polyzois I. Risk indicators for peri-implant mucositis: a systematic literature review. J Clin Periodontol. 2015;42(Suppl 16):S172–86.  https://doi.org/10.1111/jcpe.12346.CrossRefPubMedGoogle Scholar
  62. Renvert S, Roos-Jansåker A-M, Lindahl C, Renvert H, Rutger Persson G. Infection at titanium implants with or without a clinical diagnosis of inflammation. Clin Oral Implants Res. 2007;18:509–16.CrossRefGoogle Scholar
  63. Roos-Jansåker AM, Lindahl C, Renvert H, Renvert S. Nine- to fourteen- year follow-up of implant treatment. Part II: presence of peri-implant lesions. J Clin Periodontol. 2006;33(4):290–5.CrossRefGoogle Scholar
  64. Schwartz AV, Sellmeyer DE, Ensrud KE, Cauley JA, Tabor HK, Schreiner PJ, Jamal SA, Black DM, Cummings SR. Older women with diabetes have an increased risk of fracture: a prospective study. J Clin Endocrinol Metab. 2001;86:32–8.CrossRefGoogle Scholar
  65. Shernoff AF, Colwell JA, Bingham SF. Implants for type II diabetic patients: interim report. VA implants in diabetes study group. Implant Dent. 1994;3:183–5.CrossRefGoogle Scholar
  66. Shurtz-Swirski R, Sela S, Herskovits AT, Shasha SM, Shapiro G, Nasser L, Kristal B. Involvement of peripheral polymorphonuclear leukocytes in oxidative stress and inflammation in type 2 diabetic patients. Diabetes Care. 2001;24(1):104–10.CrossRefGoogle Scholar
  67. Siqueira JT, Cavalher-Machado SC, Arana-Chavez VE, Sannomiya P. Bone formation around titanium implants in the rat tibia: role of insulin. Implant Dent. 2003;12:242–51.CrossRefGoogle Scholar
  68. Simpson TC, Weldon JC, Worthington HV, Needleman I, Wild SH, Moles DR, Stevenson B, Furness S, Iheozor-Ejiofor Z. Treatment of periodontal disease for glycaemic control in people with diabetes mellitus. Cochrane Database Syst Rev. 2015;11:CD004714.Google Scholar
  69. Starup-Linde J, Eriksen SA, Lykkeboe S, Handberg A, Vestergaard P. Biochemical markers of bone turnover in diabetes patients – a meta-analysis, and a methodological study on the effects of glucose on bone markers. Osteoporos Int. 2014;25(6):1697–708.CrossRefGoogle Scholar
  70. Stern MP. Diabetes and cardiovascular disease. The “common soil” hypothesis. Diabetes. 1995;44(4):369–74.CrossRefGoogle Scholar
  71. Tawil G, Younan R, Azar P, Sleilati G. Conventional and advanced implant treatment in the type II diabetic patient: surgical protocol and long-term clinical results. Int J Oral Maxillofac Implants. 2008;23(4):744–52.PubMedGoogle Scholar
  72. Turkyilmaz I. One-year clinical outcome of dental implants placed in patients with type 2 diabetes mellitus: a case series. Implant Dent. 2010;19(4):323–9.CrossRefGoogle Scholar
  73. van Steenberghe D, Jacobs R, Desnyder M, Maffei G, Quirynen M. The relative impact of local and endogenous patient-related factors on implant failure up to the abutment stage. Clin Oral Implants Res. 2002;13(6):617–22.CrossRefGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Department of Advanced Oral Sciences and TherapeuticsUniversity of MarylandBaltimoreUSA
  2. 2.College of Dental MedicineUniversity of New EnglandPortlandUSA

Personalised recommendations