Public Health
Volume 122, Issue 4 , Pages 417-433 , April 2008

Associations between periodontal diseases and systemic diseases: A review of the inter-relationships and interactions with diabetes, respiratory diseases, cardiovascular diseases and osteoporosis

Received 24 May 2006 ,Revised 30 May 2007 ,Accepted 12 July 2007.

References 

  1. Mealey BL, Rethman MP. Periodontal disease and diabetes mellitus. Bidirectional relationship. Dent Today. 2003;22:107–113
  2. Harmel AP, Mathur R. Davidson's diabetes mellitus: diagnosis and treatment. 5th ed. Philadelphia: Saunders; 2004;p. 1–22, 365–460
  3. Mokdad AH, Ford ES, Bowman BA, Nelson DE, Engelgau MM, Vinicor F, et al. Diabetes trends in the US: 1990–1998. Diabetes Care. 2000;23:1278–1283
  4. Loe H. Periodontal disease. The sixth complication of diabetes mellitus. Diabetes Care. 1993;16:329–334
  5. American Diabetes Association position statement. Diagnosis and classification of diabetes mellitus. Diabetes Care. 2007;30:S42–S47
  6. Rayburn WF. Diagnosis and classification of diabetes mellitus: highlights from the American Diabetes Association. J Reprod Med. 1997;42:585–586
  7. Soskolne WA, Klinger A. The relationship between periodontal diseases and diabetes: an overview. Ann Periodontol. 2001;6:91–98
  8. American Academy of Periodontology position paper. Diabetes and periodontal diseases. Committee on Research, Science and Therapy. J Periodontol. 2000;71:664–678
  9. Stegeman CA. Oral manifestations of diabetes. Home Healthcare Nurse. 2005;23:233–240[quiz 241–32]
  10. Grossi SG, Genco RJ. Periodontal disease and diabetes mellitus: a two-way relationship. Ann Periodontol. 1998;3:51–61
  11. Mealey BL, Moritz AJ. Hormonal influences: effects of diabetes mellitus and endogenous female sex steroid hormones on the periodontium. Periodontology 2000. 2003;32:59–81
  12. Taylor GW. Bidirectional interrelationships between diabetes and periodontal diseases: an epidemiologic perspective. Ann Periodontol. 2001;6:99–112
  13. Grossi SG, Zambon JJ, Ho AW, Koch G, Dunford RG, Machtei EE, et al. Assessment of risk for periodontal disease: I. Risk indicators for attachment loss. J Periodontol. 1994;65:260–267
  14. Dolan TA, Gilbert GH, Ringelberg ML, Legler DW, Antonson DE, Foerster U, et al. Behavioral risk indicators of attachment loss in adult Floridians. J Clin Periodontol. 1997;24:223–232
  15. 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;104:653–660
  16. Bacic M, Plancak D, Granic M. CPITN assessment of periodontal disease in diabetic patients. J Periodontol. 1988;59:816–822
  17. Oliver RC, Tervonen T. Periodontitis and tooth loss: comparing diabetics with the general population. J Am Dent Assoc. 1993;124:71–76
  18. Ringelberg ML, Dixon DO, Francis AO, Plummer RW. Comparison of gingival health and gingival cervicular fluid flow in children with and without diabetes. J Dent Res. 1977;56:108–111
  19. Tervonen T, Oliver RC. Long-term control of diabetes mellitus and periodontitis. J Clin Periodontol. 1993;20:431–435
  20. Sammalkorpi K. Glucose intolerance in acute infections. J Intern Med. 1989;225:15–19
  21. Yki-Jarvinen H, Sammalkorpi K, Koivisto VA, Nikkila EA. Severity, duration, and mechanisms of insulin resistance during acute infections. J Clin Endocrinol Metab. 1989;69:317–323
  22. 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;67:1085–1093
  23. Collin HL, Uusitupa M, Niskanen L, Kontturi-Narhi V, Markkanen H, Koivisto AM, et al. Periodontal findings in elderly patients with non-insulin dependent diabetes mellitus. J Periodontol. 1998;69:962–966
  24. Grossi SG. Treatment of periodontal disease and control of diabetes: an assessment of the evidence and need for future research. Ann Periodontol. 2001;6:138–145
  25. Lamster IB, Lalla E. Periodontal disease and diabetes mellitus: discussion, conclusions, and recommendations. Ann Periodontol. 2001;6:146–149
  26. Murray CJ, Lopez AD. Mortality by cause for eight regions of the world: global burden of disease study. Lancet. 1997;349:1269–1276
  27. Craven DE, Steger KA, Barber TW. Preventing nosocomial pneumonia: state of the art and perspectives for the 1990s. Am J Med. 1991;91:44S–53S
  28. Scannapieco FA, Mylotte JM. Relationships between periodontal disease and bacterial pneumonia. J Periodontol. 1996;67:1114–1122
  29. Toews GB. Nosocomial pneumonia. Am J Med Sci. 1986;291:355–367
  30. Wenzel RP. Manual of clinical microbiology. Epidemiology of hospital-acquired infection. Washington DC: American Society for Microbiology; 1991;
  31. Wenzel RP. Hospital-acquired pneumonia: overview of the current state of the art for prevention and control. Eur J Clin Microbiol Infect Dis. 1989;8:56–60
  32. Scannapieco FA. Role of oral bacteria in respiratory infection. J Periodontol. 1999;70:793–802
  33. Sandford AJ, Joos L, Pare PD. Genetic risk factors for chronic obstructive pulmonary disease. Curr Opin Pulm Med. 2002;8:87–94
  34. Scannapieco FA, Wang B, Shiau HJ. Oral bacteria and respiratory infection: effects on respiratory pathogen adhesion and epithelial cell proinflammatory cytokine production. Ann Periodontol. 2001;6:78–86
  35. Scannapieco FA, Papandonatos GD, Dunford RG. Associations between oral conditions and respiratory disease in a national sample survey population. Ann Periodontol. 1998;3:251–256
  36. Hayes C, Sparrow D, Cohen M, Vokonas PS, Garcia RI. The association between alveolar bone loss and pulmonary function: the VA Dental Longitudinal Study. Ann Periodontol. 1998;3:257–261
  37. Travis J, Pike R, Imamura T, Potempa J. The role of proteolytic enzymes in the development of pulmonary emphysema and periodontal disease. Am J Respir Crit Care Med. 1994;150:S143–S146
  38. Garcia RI, Nunn ME, Vokonas PS. Epidemiologic associations between periodontal disease and chronic obstructive pulmonary disease. Ann Periodontol. 2001;6:71–77
  39. Page RC. Periodontitis and respiratory diseases: discussion, conclusions, and recommendations. Ann Periodontol. 2001;6:87–90
  40. Libby P, Geng YJ, Sukhova GK, Simon DI, Lee RT. Molecular determinants of atherosclerotic plaque vulnerability. Ann N Y Acad Sci. 1997;811:134–142[discussion 142–35]
  41. The World Health Report. Conquering suffering, enriching humanity. World Health Forum. 1997;18:248–260
  42. American Heart Association. Heart disease and stroke statistics—2004 update. 2004.
  43. Mattila KJ, Nieminen MS, Valtonen VV, Rasi VP, Kesaniemi YA, Syrjala SL, et al. Association between dental health and acute myocardial infarction. BMJ. 1989;298:779–781
  44. American Academy of Periodontology academy report. Periodontal management of patients with cardiovascular diseases. J Periodontol. 2002;73:954–968
  45. Loesche WJ. Association of the oral flora with important medical diseases. Curr Opin Periodontol. 1997;4:21–28
  46. Pussinen PJ, Mattila K. Periodontal infections and atherosclerosis: mere associations?. Curr Opin Lipidol. 2004;15:583–588
  47. Silver JG, Martin AW, McBride BC. Experimental transient bacteraemias in human subjects with varying degrees of plaque accumulation and gingival inflammation. J Clin Periodontol. 1977;4:92–99
  48. Dave S, Batista EL, Van Dyke TE. Cardiovascular disease and periodontal diseases: commonality and causation. Compend Contin Educ Dent. 2004;25:26–37
  49. Craig RG. Inflammation, cardiovascular disease and destructive periodontal diseases. The evolving role of the dental profession. N Y State Dent J. 2004;70:22–26
  50. Muhlestein JB, Anderson JL. Chronic infection and coronary artery disease. Cardiol Clin. 2003;21:333–362
  51. Roivainen M, Viik-Kajander M, Palosuo T, Toivanen P, Leinonen M, Saikku P, et al. Infections, inflammation, and the risk of coronary heart disease. Circulation. 2000;101:252–257
  52. Paquette DW. The periodontal–cardiovascular link. Compend Contin Educ Dent. 2004;25:681–692[quiz 694]
  53. Herzberg MC, Meyer MW. Effects of oral flora on platelets: possible consequences in cardiovascular disease. J Periodontol. 1996;67:1138–1142
  54. Herzberg MC, Meyer MW. Dental plaque, platelets, and cardiovascular diseases. Ann Periodontol. 1998;3:151–160
  55. Beck JD, Offenbacher S. The association between periodontal diseases and cardiovascular diseases: a state-of-the-science review. Ann Periodontol. 2001;6:9–15
  56. DeStefano F, Anda RF, Kahn HS, Williamson DF, Russell CM. Dental disease and risk of coronary heart disease and mortality. BMJ. 1993;306:688–691
  57. Arbes SJ, Slade GD, Beck JD. Association between extent of periodontal attachment loss and self-reported history of heart attack: an analysis of NHANES III data. J Dent Res. 1999;78:1777–1782
  58. Wu T, Trevisan M, Genco RJ, Dorn JP, Falkner KL, Sempos CT. Periodontal disease and risk of cerebrovascular disease: the first national health and nutrition examination survey and its follow-up study. Arch Intern Med. 2000;160:2749–2755
  59. Scannapieco FA, Bush RB, Paju S. Associations between periodontal disease and risk for atherosclerosis, cardiovascular disease, and stroke. A systematic review. Ann Periodontol. 2003;8:38–53
  60. Joshipura KJ, Rimm EB, Douglass CW, Trichopoulos D, Ascherio A, Willett WC. Poor oral health and coronary heart disease. J Dent Res. 1996;75:1631–1636
  61. Hujoel PP, Drangsholt M, Spiekerman C, DeRouen TA. Pre-existing cardiovascular disease and periodontitis: a follow-up study. J Dent Res. 2002;81:186–191
  62. Meurman JH, Janket SJ, Qvarnstrom M, Nuutinen P. Dental infections and serum inflammatory markers in patients with and without severe heart disease. Oral Surg Oral Med Oral Pathol Oral Radiol Endod. 2003;96:695–700
  63. D’Aiuto F, Parkar M, Andreaou G, Brett PM, Ready D, Tonetti MS. Periodontitis and atherosclerosis: causal association or simple coincidence? A pilot intervention study. J Clin Periodontol. 2004;31:401–411
  64. D’Aiuto F, Parkar M, Tonetti MS. Acute effects of periodontal therapy on bio-markers of vascular health. J Clin Periodontol. 2007;34:124–129
  65. Montebugnoli L, Servidio D, Miaton RA, Prati C, Tricoci P, Melloni C, et al. Periodontal health improves systemic inflammatory and haemostatic status in subjects with coronary heart disease. J Clin Periodontol. 2005;32:188–192
  66. Ide M, McPartlin D, Coward PY, Crook M, Lumb P, Wilson RF. Effect of treatment of chronic periodontitis on levels of serum markers of acute-phase inflammatory and vascular responses. J Clin Periodontol. 2003;30:334–340
  67. Tonetti MS, D’Aiuto F, Nibali L, Donald A, Storry C, Parkar M, et al. Treatment of periodontitis and endothelial function. N Engl J Med. 2007;356:911–920
  68. Wactawski-Wende J. Periodontal diseases and osteoporosis: association and mechanisms. Ann Periodontol. 2001;6:197–208
  69. Whyte JJ, Peraud P. Osteoporosis: diagnosis and treatment. CME Resource. 2005;123:11–30
  70. Iqbal MM. Osteoporosis: epidemiology, diagnosis, and treatment. South Med J. 2000;93:2–18
  71. Jeffcoat MK, Lewis CE, Reddy MS, Wang CY, Redford M. Post-menopausal bone loss and its relationship to oral bone loss. Periodontology 2000. 2000;23:94–102
  72. Payne JB, Reinhardt RA, Nummikoski PV, Dunning DG, Patil KD. The association of cigarette smoking with alveolar bone loss in postmenopausal females. J Clin Periodontol. 2000;27:658–664
  73. von Wowern N, Klausen B, Olgaard K. Steroid-induced mandibular bone loss in relation to marginal periodontal changes. J Clin Periodontol. 1992;19:182–186
  74. Wactawski-Wende J, Grossi SG, Trevisan M, Genco RJ, Tezal M, Dunford RG, et al. The role of osteopenia in oral bone loss and periodontal disease. J Periodontol. 1996;67:1076–1084
  75. Tezal M, Wactawski-Wende J, Grossi SG, Ho AW, Dunford R, Genco RJ. The relationship between bone mineral density and periodontitis in postmenopausal women. J Periodontol. 2000;71:1492–1498
  76. Hirai T, Ishijima T, Hashikawa Y, Yajima T. Osteoporosis and reduction of residual ridge in edentulous patients. J Prosthet Dent. 1993;69:49–56
  77. Klemetti E, Collin HL, Forss H, Markkanen H, Lassila V. Mineral status of skeleton and advanced periodontal disease. J Clin Periodontol. 1994;21:184–188
  78. Whalen JP, Krook L. Periodontal disease as the early manifestation of osteoporosis. Nutrition. 1996;12:53–54
  79. Reddy MS. Osteoporosis and periodontitis: discussion, conclusions, and recommendations. Ann Periodontol. 2001;6:214–217
  80. Ershler WB, Keller ET. Age-associated increased interleukin-6 gene expression, late-life diseases, and frailty. Annu Rev Med. 2000;51:245–270
  81. Jeffcoat MK, Reddy MS. Alveolar bone loss and osteoporosis: evidence for a common mode of therapy using the bisphosphonate alendronate. Biol Mech Tooth Movement Craniofac Adapt. 1996;1:365–373
  82. Rocha M, Nava LE, Vazquez de la Torre C, Sanchez-Marin F, Garay-Sevilla ME, Malacara JM. Clinical and radiological improvement of periodontal disease in patients with type 2 diabetes mellitus treated with alendronate: a randomized, placebo-controlled trial. J Periodontol. 2001;72:204–209
  83. Takaishi Y, Miki T, Nishizawa Y, Morii H. Clinical effect of etidronate on alveolar pyorrhoea associated with chronic marginal periodontitis: report of four cases. J Int Med Res. 2001;29:355–365
  84. Reddy MS, Geurs NC, Gunsolley JC. Periodontal host modulation with antiproteinase, anti-inflammatory, and bone-sparing agents. A systematic review. Ann Periodontol. 2003;8:12–37

PII: S0033-3506(07)00232-6

doi: 10.1016/j.puhe.2007.07.004

Public Health
Volume 122, Issue 4 , Pages 417-433 , April 2008