, Volume 94, Issue 1, pp 10–21 | Cite as

Periodontal disease and systemic conditions: a bidirectional relationship

  • Jemin Kim
  • Salomon AmarEmail author


For decades, physicians and dentists have paid close attention to their own respective fields, specializing in medicine pertaining to the body and the oral cavity, respectively. However, recent findings have strongly suggested that oral health may be indicative of systemic health. Currently, this gap between allopathic medicine and dental medicine is quickly closing, due to significant findings supporting the association between periodontal disease and systemic conditions such as cardiovascular disease, type 2 diabetes mellitus, adverse pregnancy outcomes, and osteoporosis. Significant effort has brought numerous advances in revealing the etiological and pathological links between this chronic inflammatory dental disease and these other conditions. Therefore, there is reason to hope that the strong evidence from these studies may guide researchers towards greatly improved treatment of periodontal infection that would also ameliorate these systemic illnesses. Hence, researchers must continue not only to uncover more information about the correlations between periodontal and systemic diseases but also to focus on positive associations that may result from treating periodontal disease as a means of ameliorating systemic diseases.

Key words

Periodontal diseases Systemic diseases Cardiovascular diseases Diabetes Adverse pregnancy outcomes Osteoporosis 


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  1. 1.
    Loesche, WJ, Grossman, NS 2001Periodontal disease as a specific, albeit chronic, infection: diagnosis and treatmentClin Microbiol Rev1472752PubMedCrossRefGoogle Scholar
  2. 2.
    Amar, S, Gokce, N, Morgan, S, Loukideli, M, Van Dyke, TE, Vita, JA 2003Periodontal disease is associated with brachial artery endothelial dysfunction and systemic inflammationArterioscler Thromb Vasc Biol2312459PubMedCrossRefGoogle Scholar
  3. 3.
    Genco, RJ, Grossi, SG 1998Is estrogen deficiency a risk factor for periodontal disease?Compend Contin Educ Dent Suppl22S239PubMedGoogle Scholar
  4. 4.
    Fuster, V, Badimon, L, Badimon, JJ,  et al. 1992The pathogenesis of coronary artery disease and the acute coronary syndromesN Engl J Med32624250PubMedCrossRefGoogle Scholar
  5. 5.
    Angeli, F, Verdecchia, P, Pellegrino, C, Pellegrino, RG, Pellegrino, G, Prosciutti, L, Giannoni, C, Cianetti, S, Bentivoglio, M 2003Association between periodontal disease and left ventricle mass in essential hypertensionHypertension4148892PubMedCrossRefGoogle Scholar
  6. 6.
    Elter, JR, Champagne, CME, Offenbacher, S, Beck, JD 2004Relationship of periodontal disease and tooth loss to prevalence of coronary heart diseaseJ Periodontol7578290PubMedCrossRefGoogle Scholar
  7. 7.
    Hujoel, PP, Drangsholt, MT, Spiekerman, C, Derouen, TA 2002Periodontitis-systemic disease associations in the presence of smoking: causal or coincidental?J Periodontol 2000305160CrossRefGoogle Scholar
  8. 8.
    Ebersole, JL, Capelli, D, Steffen, MJ 1995Longitudinal dynamics of infection and serum antibody in A. actinomycetemcomitans periodontitisOral Dis112938PubMedCrossRefGoogle Scholar
  9. 9.
    Hayes, C, Antezak-Bouckoms, A, Burdick, E 1992Quality assessment and meta-analysis of systemic tetracycline use in chronic adult periodontitisJ Clin Periodontol191648PubMedCrossRefGoogle Scholar
  10. 10.
    Van Winkelhoff, AJ, Tijhof, CJ, de Graaff, J 1992Microbiological and clinical results of metronidazole plus amoxicillin therapy in Actinobacillus actinomycetemcomitans-associated periodontitisJ Periodontol63527PubMedGoogle Scholar
  11. 11.
    Sorsa, T, Ingman, T, Suomalainen, K, Haapasalo, M, Konttinen, YT, Lindy, O, Saari, H, Uitto, VJ 1992Identification of proteases from periodontopathogenic bacteria as activators of latent human neutrophil and fibroblast-type interstitial collagenasesInfect Immun6044915PubMedGoogle Scholar
  12. 12.
    Lee, W, Aitken, S, Sodek, J, McCulloch, CA 1995Evidence of a direct relationship between neutrophil collagenase activity and periodontal tissue destruction in vivo: role of active enzyme in human periodontitisJ Periodontal Res302333PubMedCrossRefGoogle Scholar
  13. 13.
    Geerts, SO, Legrand, V, Charpentier, J, Albert, A, Rompen, EH 2004Further evidence of the association between periodontal conditions and coronary artery diseaseJ Periodontol75127480PubMedCrossRefGoogle Scholar
  14. 14.
    Page, RC 1991The role of inflammatory mediators in the pathogenesis of periodontal diseaseJ Periodontal Res2623042PubMedCrossRefGoogle Scholar
  15. 15.
    Loesche, WJ, Gusberti, F, Mettraux, G, Higgins, T, Syed, S 1983Relationship between oxygen tension and subgingival bacterial flora in untreated human periodontal pocketsInfect Immun4265967PubMedGoogle Scholar
  16. 16.
    Amar, S, Han, X 2003The impact of periodontal infection on systemic diseasesMed Sci Monit9RA2919PubMedGoogle Scholar
  17. 17.
    Socransky, SS, Haffajee, AD, Cugini, MA, Smith, C, Kent, RL,Jr 1998Microbial complexes in subgingival plaqueJ Clin Periodontol2513444PubMedCrossRefGoogle Scholar
  18. 18.
    Slots, J, Kamma, JJ, Sugar, C 2003The herpesvirus-Porphyromonas gingivalis-periodontitis axisJ Periodont Res3831223Google Scholar
  19. 19.
    Leivadaros, E, van der Velden, U, Bizzarro, S, ten Heggeler, JM, Gerdes, VE, Hoek, FJ, Nagy, TO, Scholma, J, Bakker, SJ, Gans, RO, Ten Cate, H, Loos, BG 2005A pilot study into measurements of markers of atherosclerosis periodontitisJ Periodontol761218PubMedCrossRefGoogle Scholar
  20. 20.
    Prabhu, A, Michalowicz, BS, Mathur, A 1996Detection of local and systemic cytokines in adult periodontitisJ Periodontol6751522PubMedGoogle Scholar
  21. 21.
    Lusis, AJ 2000AtherosclerosisNature40723341PubMedCrossRefGoogle Scholar
  22. 22.
    Beck, J, Garcia, R, Heiss, G, Vokonas, PS, Offenbacher, S 1996Periodontal disease and cardiovascular diseaseJ Periodontol67112337PubMedGoogle Scholar
  23. 23.
    Haraszthy, VI, Zambon, JJ, Trevisan, M, Zeid, M, Genco, RJ 2000Identification of periodontal pathogens in atheromatous plaquesJ Periodontol71155460PubMedCrossRefGoogle Scholar
  24. 24.
    Cairo, F, Gaeta, C, Dorigo, W, Oggioni, MR, Pratesi, C, Pini Prato, GP, Pozzi, G 2004Periodontal pathogens in atheromatous plaques. A controlled clinical and laboratory trialJ Periodontal Res394426PubMedCrossRefGoogle Scholar
  25. 25.
    Iwai, T, Inoue, Y, Umeda, M, Huang, Y, Kurihara, N, Koike, M, Ishikawa, I 2005Oral bacteria in the occluded arteries of patients with Buerger diseaseJ Vasc Surg4210715PubMedCrossRefGoogle Scholar
  26. 26.
    Chun, YH, Chun, KR, Olguin, D, Wang, HL 2005Biological foundation for periodontitis as a potential risk factor for atherosclerosisJ Periodontal Res408795PubMedCrossRefGoogle Scholar
  27. 27.
    Zhang, SH, Reddick, RL, Piedrahita, JA,  et al. 1992Spontaneous hypercholesterolemia and arterial lesions in mice lacking apolipoprotein EScience25846871PubMedGoogle Scholar
  28. 28.
    Plump, AS, Smith, JD, Hayek, T,  et al. 1992Severe hypercholester-olemia and atherosclerosis in apolipoprotein E-deficient mice created by homologous recombination in ES cellsCell7134353PubMedCrossRefGoogle Scholar
  29. 29.
    Gibson, FC,3rd, Hong, C, Chou, HH, Yumoto, H, Chen, J, Lien, E, Wong, J, Genco, CA 2004Innate immune recognition of invasive bacteria accelerates atherosclerosis in apolipoprotein E-deficient miceCirculation10928016Epub 2004 May 3PubMedCrossRefGoogle Scholar
  30. 30.
    Loos, BG, Craandijk, J, Hoek, FJ, Wertheim-van Dillen, PM, van der Velden, U 2000Elevation of systemic markers related to cardiovascular diseases in the peripheral blood of periodontitis patientsJ Periodontol71152834PubMedCrossRefGoogle Scholar
  31. 31.
    Khlgatian, M, Nassar, H, Chou, HH, Gibson, FC,3rd, Genco, CA 2002Fimbria-dependent activation of cell adhesion molecule expression in Porphyromonas gingivalis-infected endothelial cellsInfect Immun7025767PubMedCrossRefGoogle Scholar
  32. 32.
    Schachinger, V, Britten, MB, Zeiher, AM 2000Prognostic impact of coronary vasodilator dysfunction on adverse long-term outcome of coronary heart diseaseCirculation1011899906PubMedGoogle Scholar
  33. 33.
    Firatli, E 1997The relationship between clinical periodontal status and insulin-dependent diabetes mellitus. Results after 5 yearsJ Periodontol6813640PubMedGoogle Scholar
  34. 34.
    Hung, HC, Willett, W, Merchant, A, Rosner, BA, Acherio, A, Joshipura, KJ 2003Oral health and peripheral arterial diseaseCirculation10711527PubMedCrossRefGoogle Scholar
  35. 35.
    Joshipura, KJ, Wand, HC, Merchant, AT, Rimm, EB 2004Periodontal disease and biomarkers related to cardiovascular diseaseJ Dent Res831515PubMedGoogle Scholar
  36. 36.
    Sinisalo, J, Paronen, J, Mattila, KJ, Syrjala, M, Alfthan, G, Palosuo, T, Nieminen, MS, Vaarala, O 2000Relation of inflammation to vascular function in patients with coronary heart diseaseAtherosclerosis14940311PubMedCrossRefGoogle Scholar
  37. 37.
    Thompson, SG, Kienast, J, Pyke, SD, Haverkate, F, van de Loo, JC 1995Hemostatic factors and the risk of myocardial infarction or sudden death in patients with angina pectorisN Engl J Med33263541PubMedCrossRefGoogle Scholar
  38. 38.
    Skoog, T, Dichtl, W, Boquist, S, Skoglund-Andersson, C, Karpe, F, Tang, ,  et al. 2002Plasma tumour necrosis factor-alpha and early carotid atherosclerosis in healthy middle-aged menEur Heart J2337683PubMedCrossRefGoogle Scholar
  39. 39.
    Desvarieux, M, Demmer, RT, Rundek, T, Boden-Albala, B, Jacobs, DR,Jr, Papapanou, PN, Sacco, RL 2003Relationship between periodontal disease, tooth loss, and carotid artery plaque: the Oral Infections and Vascular Disease Epidemiology Study (INVEST)Stroke3421205PubMedCrossRefGoogle Scholar
  40. 40.
    Wang, CH, Li, SH, Weisel, RD,  et al. 2003C-reactive protein upregulates angiotensin type 1 receptors in vascular smooth muscleCirculation107178390PubMedCrossRefGoogle Scholar
  41. 41.
    Fichtlscherer, S, Breuer, S, Schachinger, V, Dimmeler, S, Zeiher, AM 2004C-reactive protein levels determine systemic nitric oxide bioavailability in patients with coronary artery diseaseEur Heart J2514128PubMedCrossRefGoogle Scholar
  42. 42.
    Pussinen, PJ, Viluna-Rautiainen, T, Alfthan, G, Palosuo, T, Jauhiainen, M, Sundvall, J, Vesanen, M, Mattila, K, Asikainen, S 2004Severe periodontitis enhances macrophage activation via increased serum lipopolysaccharideArterioscler Thromb Vasc Biol24217480PubMedCrossRefGoogle Scholar
  43. 43.
    Zwaka, TP, Hombach, V, Torzewski, J 2001C-reactive protein-mediated low density lipoprotein uptake by macrophages: implications for atherosclerosisCirculation10311947PubMedGoogle Scholar
  44. 44.
    Mattila, KJ, Pussinen, PJ, Paju, S 2005Dental infections and cardiovascular diseases: a reviewJ Periodontol7620858PubMedCrossRefGoogle Scholar
  45. 45.
    Pussinen, PJ, Jauhiainen, M, Vilkuna-Rautiainen, T, Sundvall, J, Vesanen, M, Mattila, K, Palosuo, T, Alfthan, G, Asikainen, S 2004Periodontitis decreases the antiatherogenic potency of high density lipoproteinJ Lipid Res4513947PubMedCrossRefGoogle Scholar
  46. 46.
    Pearson, TA, Mensah, GA, Alexander, RW, Anderson, JL, Cannon, RO,3rd, Criqui, M,  et al. 2003Markers of inflammation and cardiovascular disease: application to clinical and public health practice: a statement for healthcare professionals from the Centers for Disease Control and Prevention and the American Heart AssociationCirculation107499511PubMedCrossRefGoogle Scholar
  47. 47.
    Pussinen, PJ, Jousilahti, P, Alfthan, G, Palosuo, T, Asikainen, S, Salomaa, V 2003Antibodies to periodontal pathogens are associated with coronary heart diseaseArterioscler Thromb Vasc Biol2312504PubMedCrossRefGoogle Scholar
  48. 48.
    Pussinen, PJ, Nyysonen, K, Alfthan, G, Salonen, R, Laukkanen, JA, Salonen, JT 2005Serum antibody levels to Actinobacillus actinomycetemcomitans predict the risk for coronary heart diseaseArterioscler Thromb Vasc Biol258338PubMedCrossRefGoogle Scholar
  49. 49.
    Gilbert, GH, Miller, MK, Duncan, RP, Ringelberg, ML, Dolan, TA, Foerster, U 1999Tooth-specific and person-level predictors of 24-month tooth loss among older adultsCommunity Dent Oral Epidemiol2737285PubMedGoogle Scholar
  50. 50.
    Chi, H, Messas, E, Levine, RA, Graves, DT, Amar, S 2004Interleukin-1 receptor signaling mediates atherosclerosis associated with bacterial exposure and/or a high-fat diet in a murine apolipoprotein E heterozygote model: pharmacotherapeutic implicationsCirculation110167885PubMedCrossRefGoogle Scholar
  51. 51.
    Li, L, Messas, E, Batista, EL,Jr,  et al. 2002Porphyromonas gingivalis infection accelerates the progression of atherosclerosis in a heterozygous apolipoprotein E-deficient murine modelCirculation1058617PubMedCrossRefGoogle Scholar
  52. 52.
    Skyler, J, Oddo, C 2002Diabetes trends in the USADiabetes Metab Res Rev18S216PubMedCrossRefGoogle Scholar
  53. 53.
    King, H, Aubert, RE, Herman, WH 1998Global burden of diabetes, 1995–2025: prevalence, numerical estimates, and projectionsDiabetes Care21141431PubMedGoogle Scholar
  54. 54.
    Matthews, DC 2002The relationship between diabetes and periodontal diseaseJ Can Dent Assoc681614PubMedGoogle Scholar
  55. 55.
    Tervonen, T, Oliver, RC, Wolff, LF, Bereuter, J, Anderson, LA, Aeppli, DM 1994Prevalence of periodontal pathogens with varying metabolic control of diabetes mellitusJ Clin Periodontol213759PubMedCrossRefGoogle Scholar
  56. 56.
    Yuan, K, Chang, CJ, Hsu, PC, Sun, HS, Tseng, CC, Wang, JR 2001Detection of putative periodontal pathogens in non-insulin-dependent diabetes mellitus and non-diabetes mellitus by polymerase chain reactionJ Periodontal Res361824PubMedCrossRefGoogle Scholar
  57. 57.
    Teng, YT, Taylor, GW, Scannapieco, F, Kinane, DF, Curtis, M, Beck, JD, Kogon, S 2002Periodontal health and systemic disordersJ Can Dent Assoc6818892PubMedGoogle Scholar
  58. 58.
    Pradhan, AD, Ridker, PM 2002Do atherosclerosis and type 2 diabetes share a common inflammatory basis?Eur Heart J238314PubMedCrossRefGoogle Scholar
  59. 59.
    Yudkin, JS, Stehouwer, CD, Emeis, JJ, Coppack, SW 1999C-reactive protein in healthy subjects: associations with obesity, insulin resistance, and endothelial dysfunction: a potential role for cytokines originating from adipose tissue?Arterioscler Thromb Vasc Biol199728PubMedGoogle Scholar
  60. 60.
    Bluher, M, Fasshauer, M, Tonjes, A, Kratzsch, J, Schon, MR, Paschke, R 2005Association of interleukin-6, C-reactive protein, interleukin-10 and adiponectin plasma concentrations with measures of obesity, insulin sensitivity and glucose metabolismExp Clin Endocrinol Diabetes1135347PubMedCrossRefGoogle Scholar
  61. 61.
    Thorand, B, Kolb, H, Baumert, J, Koenig, W, Chambless, L, Meisinger, C, Illig, T, Martin, S, Herder, C 2005Elevated levels of interleukin-18 predict the development of type 2 diabetes: results from the MONICA/KORA Augsburg Study, 1984–2002Diabetes5429328PubMedGoogle Scholar
  62. 62.
    Grossi, SG, Zambon, JJ, Ho, AW, Koch, G, Dunford, RG, Machtel, EE,  et al. 1994Assessment of risk for periodontal disease. I. Risk indicators for attachment lossJ Periodontol652607PubMedGoogle Scholar
  63. 63.
    Christgau, M, Palitzsch, KD, Schmalz, G, Kreiner, U, Frenzel, S 1998Healing response to nonsurgical periodontal therapy in patients with diabetes mellitus: clinical, microbiological, and immunologic resultsJ Clin Periodontol2511224PubMedCrossRefGoogle Scholar
  64. 64.
    Stewart, JE, Wager, KA, Friedlander, AH, Zadeh, HH 2001The effect of periodontal treatment on glycemic control in patients with type 2 diabetes mellitusJ Clin Periodontol2830610PubMedCrossRefGoogle Scholar
  65. 65.
    Offenbacher, S, Salvi, GE 1999Induction of prostaglandin release from macrophages by bacterial endotoxinClin Infect Dis2850513PubMedGoogle Scholar
  66. 66.
    Lalla, RV, D'Ambrosio, JA 2001Dental management considerations for the patient with diabetes mellitusJ Am Dent Assoc132142532PubMedGoogle Scholar
  67. 67.
    Westfelt, E, Rylander, H, Blohme, G, Jonasson, P, Lindhe, J 1996The effect of periodontal therapy in diabetics. Results after 5 yearsJ Clin Periodontol2392100PubMedCrossRefGoogle Scholar
  68. 68.
    Strommer, L, Wickbom, M, Wang, F, Herrington, MK, Ostenson, CG, Arnelo, U, Permert, J 2002Early impairment of insulin secretion in rats after surgical traumaEur J Endocrinol14782533PubMedCrossRefGoogle Scholar
  69. 69.
    Tsigos, C, Papanicolaou, DA, Kyrou, I, Defensor, R, Mitsiadis, CS, Chrousos, GP 1997Dose-dependent effects of recombinant human interleukin-6 on glucose regulationJ Clin Endocrinol Metab82416770PubMedCrossRefGoogle Scholar
  70. 70.
    Plomgaard, P, Bouzakri, K, Krogh-Madsen, R, Mittendorfer, B, Zierath, JR, Pedersen, BK 2005Tumor necrosis factor-alpha induces skeletal muscle insulin resistance in healthy human subjects via inhibition of Akt substrate 160 phosphorylationDiabetes54293945PubMedGoogle Scholar
  71. 71.
    Vendrell, J, Broch, M, Vilarrasa, N,  et al. 2004Resistin, adiponectin, ghrelin, leptin, and proinflammatory cytokines: relationships in obesityObes Res1296271PubMedCrossRefGoogle Scholar
  72. 72.
    Genco, RJ, Grossi, SG, Ho, A, Nishimura, F, Murayama, Y 2005A proposed model linking inflammation to obesity, diabetes, and periodontal infectionsJ Periodontol76207584PubMedCrossRefGoogle Scholar
  73. 73.
    Berkowitz, GS, Papeirnik, E 1993Epidemiology of preterm birthEpidemiol Rev1541443PubMedGoogle Scholar
  74. 74.
    Buduneli, N, Baylas, H, Buduneli, E, Turkoglu, O, Kose, T, Dahlen, G 2005Periodontal infections and pre-term low birth weight: a case-control studyJ Clin Periodontol3217481PubMedCrossRefGoogle Scholar
  75. 75.
    McCormick, MC 1985The contribution of low birth weight to infant mortality and childhood morbidityN Engl J Med3128290PubMedCrossRefGoogle Scholar
  76. 76.
    Davenport, ES, Williams, CE, Sterne, KA, Murad, S, Sivapathasundram, V, Curtis, MA 2002Maternal periodontal disease and preterm low birthweight: case-control studyJ Dent Res813138PubMedCrossRefGoogle Scholar
  77. 77.
    Offenbacher, S, Lieff, S, Boggess, K, Murtha, A, Madianos, P, Champagne, C,  et al. 2001Maternal periodontitis and prematurity. Part I: obstetric outcome of prematurity and growth restrictionAnn Periodontol616474PubMedCrossRefGoogle Scholar
  78. 78.
    Moreu, G, Tellez, L, Gonzalez-Jaranay, M 2005Relationship between maternal periodontal disease and low-birth-weight pre-term infantsJ Clin Periodontol326227PubMedCrossRefGoogle Scholar
  79. 79.
    Yeo, BK, Lim, LP, Paquette, DW, Williams, RC 2005Periodontal disease – the emergence of a risk for systemic conditions: pre-term low birth weightAnn Acad Med341116Google Scholar
  80. 80.
    Ventura, SJ, Martine, JA, Curtin, SC,  et al. 1999Births: final data for 1997Natl Vital Stat Rep47196Google Scholar
  81. 81.
    Skuldbol, T, Johansen, KH, Dahlen, G, Stoltze, K, Holmstrup, P 2006Is pre-term labour associated with periodontitis in a Danish maternity ward?J Clin Periodontol3317783PubMedCrossRefGoogle Scholar
  82. 82.
    Andrews, WW, Goldenberg, RL, Hauth, JC 1995Preterm labor: emerging role of genital tract infectionsInfect Agents Dis4196211PubMedGoogle Scholar
  83. 83.
    Gibbs, RS, Romero, R, Hillier, SL, Eschenbach, DA, Sweet, RL 1992A review of premature birth subclinical infectionAm J Obstet Gynecol166151526PubMedGoogle Scholar
  84. 84.
    Minkoff, H, Grunebaum, AN, Schwarz, RH, Feldman, J, Cummings, M, Crombleholme, W,  et al. 1984Risk factors for premature rupture of membranes: a prospective study of the vagina flora in pregnancyAm J Obstet Gynecol15096572PubMedGoogle Scholar
  85. 85.
    Offenbacher, S, Katz, V, Fertik, G,  et al. 1996Periodontal infection as a possible risk factor for preterm low birth weightJ Periodontol67110313PubMedGoogle Scholar
  86. 86.
    Slattery, MM, Morrison, JJ 2002Preterm deliveryLancet360148997PubMedCrossRefGoogle Scholar
  87. 87.
    Romero, R, Mazor, M 1988Infection and preterm laborClin Obstet Gynecol3155384PubMedCrossRefGoogle Scholar
  88. 88.
    Madianos, PN, Lieff, S, Murtha, AP, Boggess, KA, Auten, RL,Jr, Beck, JD, Offenbacher, S 2001Maternal periodontitis and prematurity. Part II: maternal infection and fetal exposureAnn Periodontol617582PubMedCrossRefGoogle Scholar
  89. 89.
    Offenbacher, S, Riche, EL, Barros, SP, Bobetsis, Lin D, Beck, JD 2005Effects of maternal Campylobacter rectus infection on murine placenta, fetal and neonatal survival, and brain developmentJ Periodontol76213343PubMedCrossRefGoogle Scholar
  90. 90.
    Han, YW, Redline, RW, Li, M, Yin, L, Hill, GB, McCormick, TS 2004Fusobacterium nucleatum induces premature and term stillbirths in pregnant mice: implication of oral bacteria in preterm birthInfect Immun7222729PubMedCrossRefGoogle Scholar
  91. 91.
    Boggess, KA, Moss, K, Madianos, P, Murtha, AP, Beck, J, Offenbacher, S 2005Fetal immune response to oral pathogens and risk of preterm birthAm J Obstet Gynecol19311216PubMedCrossRefGoogle Scholar
  92. 92.
    Lopez, NJ, Silva, ID, Ipinza, J, Gutierrez, J 2005Periodontal therapy reduces the rate of preterm low birth weight in women with pregnancy-associated gingivitisJ Periodontol76214453PubMedCrossRefGoogle Scholar
  93. 93.
    Wactawski-Wende, J, Grossi, SG, Trevisan, M, Genco, RJ, Tezal, M, Dunford, RG, Ho, AW, Hausmann, E, Hreshchyshyn, MM 1996The role of osteopenia in oral bone loss and periodontal diseaseJ Periodontol67107684PubMedGoogle Scholar
  94. 94.
    Garnero, P 2000Markers of bone turnover for the prediction of fracture riskOsteoporos Int11S5565PubMedCrossRefGoogle Scholar
  95. 95.
    Jeffcoat, MK, Chestnut, CH,3rd 1993Systemic osteoporosis and oral bone loss: evidence shows increased risk factorsJ Am Dent Assoc1244956PubMedGoogle Scholar
  96. 96.
    Page, RC, Sims, TJ, Geissler, F, Altman, LC, Baab, DA 1985Defective neutrophil and monocyte motility in patients with early-onset periodontitisInfect Immun4716975PubMedGoogle Scholar
  97. 97.
    Lerner, UH 2000Osteoclast formation and resorptionMatrix Biol1910720PubMedCrossRefGoogle Scholar
  98. 98.
    Manabe, H, Kawaguchi, H, Chikuda, H, Miyaura, C, Inada, M, Nagai, R,  et al. 2001Connection between B lymphocyte and ostoclast differentiation pathwaysJ Immunol167262531PubMedGoogle Scholar
  99. 99.
    Taubman, MA, Kawai, T 2001Involvement of T-lymphocytes in periodontal disease and in direct and indirect induction of bone resoprtionCrit Rev Oral Biol Med1212535PubMedCrossRefGoogle Scholar
  100. 100.
    Liu, D, Xu, JK, Figliomeni, L, Huang, L, Pavlos, NJ, Rogers, M,  et al. 2003Expression of RANKL and OPG mRnNA in periodontal disease. Possible involvement in bone destructionInt J Mol Med111721PubMedGoogle Scholar
  101. 101.
    Nagasawa, T, Kobayashi, H, Kiji, M, Aramaki, M, Mahanoda, R, Kojima, T,  et al. 2002LPS-stimulated human gingival fibroblast inhibits the differentiation of monocytes into osteoclasts through the production of osteoprotegerinClin Exp Immunol13033844PubMedCrossRefGoogle Scholar
  102. 102.
    Teng, YTA, Nguyen, H, Gao, X, Kong, YY, Gorczynski, RM, Singh, B,  et al. 2000Functional human T-cell immunity and osteoprotegerin ligand control alveolar bone destruction in periodontal infectionJ Clin Invest106R5967PubMedGoogle Scholar
  103. 103.
    Jiang, Y, Mehta, CK, Hsu, TY, Alsulaimani, FFH 2002Bacteria induce osteoclastogenesis via an osteoblast-independent pathwayInfect Immun7031438PubMedCrossRefGoogle Scholar
  104. 104.
    Jacobs, R, Ghyselen, J, Konincks, P, van Steeberghe, D 1996Long-term bone mass evaluation of mandible and lumbar spine in a group of women receiving hormone replacement therapyEur J Oral Sci104106PubMedGoogle Scholar
  105. 105.
    Pacifici, R 1998Cytokines, estrogen, and postmenopausal osteoporosis – the second decadeEndocrinology139265961PubMedCrossRefGoogle Scholar
  106. 106.
    Gemmell, E, Marshall, RI, Seymour, GJ 1997Cytokines and prostaglandins in immune homeostasis and tissue destruction in periodontal diseaseJ Periodontol 20001411243Google Scholar
  107. 107.
    Baker, PJ 2000The role of immune responses in bone loss during periodontal diseaseMicrobes Infect2118192PubMedCrossRefGoogle Scholar
  108. 108.
    Tezal, M, Wactawaki-Wende, J, Grossi, SG, Ho, AW, Dunford, R, Genco, RJ 2000The relationship between bone mineral density and periodontitis in postmenopausal womenJ Periodontol7114928PubMedCrossRefGoogle Scholar
  109. 109.
    Inagaki, K, Kurosu, Y, Yoshinari, N, Noguchi, T, Krall, EA, Garcia, RI 2005Efficacy of periodontal disease and tooth loss to screen for low bone mineral density in Japanese womenCalcif Tissue Int77914Epub 2005 Jul 14PubMedCrossRefGoogle Scholar
  110. 110.
    Wactawski-Wende, J, Hausmann, E, Hovey, K, Trevisan, M, Grossi, S, Genco, RJ 2005The association between osteoporosis and alveolar crestal height in postmenopausal womenJ Periodontol76211624PubMedCrossRefGoogle Scholar
  111. 111.
    Marques, MR, da Silva, MAD, Manzi, FR, Cesar-Neto, JB, Nociti, FH,Jr, Barros, SP 2005Effect of intermittent PTH administration in the periodontitis-associated bone loss in ovariectomized ratsArch Oral Biol504219PubMedCrossRefGoogle Scholar
  112. 112.
    Jeffcoat, M 2005The association between osteoporosis and oral bone lossJ Periodontol76212532PubMedCrossRefGoogle Scholar
  113. 113.
    Brandi, ML, Hukkanen, M, Umeda, T,  et al. 1995Bidirectional regulation of osteoclast function by nitric oxide synthase isoformsProc Natl Acad Sci USA9229548PubMedCrossRefGoogle Scholar
  114. 114.
    Lohinai, Z, Stachlewitz, R, Virag, L, Szekely, AD, Hasko, G, Szabo, C 2001Evidence for reactive nitrogen species formation in gingivomucosal tissueJ Dent Res804705PubMedGoogle Scholar
  115. 115.
    Gyurko, R, Boustany, G, Huang, PL,  et al. 2003Mice lacking inducible nitric oxide synthase demonstrate impaired killing of Porphyromonas gingivalis Infect Immun183946Google Scholar
  116. 116.
    Leitao, RFC, Rocha, FAC, Chaves, HV, Lima, V, Cunha, FQ, Ribeiro, RA, Brito, GAC 2004Locally applied isosorbide decreases bone resorption in experimental periodontitis in ratsJ Periodontol75122732PubMedCrossRefGoogle Scholar
  117. 117.
    American Academy of Periodontology1996Systemic antibiotics in peridonticsJ Periodontol678318Google Scholar

Copyright information

© The Society of The Nippon Dental University 2006

Authors and Affiliations

  1. 1.Department of Periodontology and Oral BiologyBoston University Goldman School of Dental MedicineBostonUSA
  2. 2.Boston University Medical CenterBostonUSA

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