Have a personal or library account? Click to login
The Connection of Periodontal Disease and Diabetes Mellitus: The Role of Matrix Metalloproteinases and Oxidative Stress Cover

The Connection of Periodontal Disease and Diabetes Mellitus: The Role of Matrix Metalloproteinases and Oxidative Stress

Open Access
|Nov 2019

References

  1. 1. Slots J. Periodontitis: facts, fallacies and the future. Periodontol 2000. 2017;75(1):7-23.10.1111/prd.1222128758294
  2. 2. Pihlstrom, BL. Periodontal risk assessment, diagnosis and treatment planning. Periodontology 2000. 2001;25:37-58.10.1034/j.1600-0757.2001.22250104.x11155181
  3. 3. Grenier, G, Gagnon, G, Grenier, D. Detection of herpetic viruses in gingival crevicular fluid of patients suffering from periodontal diseases: prevalence and effect of treatment. Oral Microbiology and Immunology 2009;24:506-9.10.1111/j.1399-302X.2009.00542.x19832804
  4. 4. Järvensivu, A, Hietanen, J, Rautemaa, R, Sorsa, T, Richardson, M. Candida yeasts in chronic periodontitis tissues and subgingival microbial biofilms in vivo. Oral Diseases 2004;10:106-12.10.1046/j.1354-523X.2003.00978.x14996281
  5. 5. Hajishengallis, G, Lamont, RJ. Beyond the red complex and into more complexity: the polymicrobial synergy and dysbiosis (PSD) model of periodontal disease etiology. Molecular oral microbiology 2012;27:409-19.10.1111/j.2041-1014.2012.00663.x365331723134607
  6. 6. Mahajan, A, Singh, B, Kashyap, D, Kumar, A, Mahajan, P. Interspecies communication and periodontal disease. The Scientific World Journal 2013;2013:10.1155/2013/765434387430924396307
  7. 7. Gupta S, Maharjan A, Dhami B, Amgain P, Katwal S, Adhikari B, Shukla A. Status of Tobacco Smoking and Diabetes with Periodontal Disease. JNMA J Nepal Med Assoc. 2018;56(213):818-824.10.31729/jnma.3610
  8. 8. Preshaw, PM, Taylor, JJ. How has research into cytokine interactions and their role in driving immune responses impacted our understanding of periodontitis? Journal of clinical periodontology 2011;38:60-84.
  9. 9. Kinane, DF, Preshaw, PM, Loos, BG, on Behalf of Working Group 2 of the Seventh European Workshop on, P. Host-response: understanding the cellular and molecular mechanisms of host-microbial interactions – Consensus of the Seventh European Workshop on Periodontology. Journal of Clinical Periodontology 2011;38:44-8.10.1111/j.1600-051X.2010.01682.x21323703
  10. 10. Garlet, G. Destructive and protective roles of cytokines in periodontitis: a re-appraisal from host defense and tissue destruction viewpoints. Journal of dental research 2010;89:1349-63.10.1177/002203451037640220739705
  11. 11. McInnes, IB, Schett, G. Cytokines in the pathogenesis of rheumatoid arthritis. Nature Reviews Immunology 2007;7:429-42.10.1038/nri209417525752
  12. 12. Page, RC. The pathobiology of periodontal diseases may affect systemic diseases: inversion of a paradigm. Annals of periodontology 1998;3:108-20.10.1902/annals.1998.3.1.1089722695
  13. 13. Lamster, IB, Lalla, E, Borgnakke, WS, Taylor, GW. The relationship between oral health and diabetes mellitus. The Journal of the American Dental Association 2008;139:19S-24S.10.14219/jada.archive.2008.036318809650
  14. 14. Murrah, V, Crosson, J, Sauk, J. Parotid gland basement membrane variation in diabetes mellitus. Journal of Oral Pathology & Medicine 1985;14:236-46.10.1111/j.1600-0714.1985.tb00487.x3921679
  15. 15. Ship, JA. Diabetes and oral health: an overview. The Journal of the American Dental Association 2003;134:4S-10S.10.14219/jada.archive.2003.036718196667
  16. 16. Löe, H. Periodontal disease: the sixth complication of diabetes mellitus. Diabetes care 1993;16:329-34.10.2337/diacare.16.1.329
  17. 17. Tsai, C, Hayes, C, Taylor, GW. Glycemic control of type 2 diabetes and severe periodontal disease in the US adult population. Community dentistry and oral epidemiology 2002;30:182-92.10.1034/j.1600-0528.2002.300304.x12000341
  18. 18. Lalla, E, Cheng, B, Lal, S, Kaplan, S, Softness, B, Greenberg, E, et al. Diabetes mellitus promotes periodontal destruction in children. Journal of clinical periodontology 2007;34:294-8.10.1111/j.1600-051X.2007.01054.x17378885
  19. 19. Yoshida, T, Flegler, A, Kozlov, A, Stern, PH. Direct inhibitory and indirect stimulatory effects of RAGE ligand S100 on sRANKL-induced osteoclastogenesis. Journal of cellular biochemistry 2009;107:917-25.10.1002/jcb.2219219415676
  20. 20. Nishimura, F, Takahashi, K, Kurihara, M, Takashiba, S, Murayama, Y. Periodontal Disease as a Complication of Diabetes Mellitus*. Annals of periodontology 1998;3:20-9.10.1902/annals.1998.3.1.209722687
  21. 21. Esposito, K, Nappo, F, Marfella, R, Giugliano, G, Giugliano, F, Ciotola, M, et al. Inflammatory cytokine concentrations are acutely increased by hyperglycemia in humans role of oxidative stress. Circulation 2002;106:2067-72.10.1161/01.CIR.0000034509.14906.AE12379575
  22. 22. Kobayashi, K, Takahashi, N, Jimi, E, Udagawa, N, Takami, M, Kotake, S, et al. Tumor necrosis factor α stimulates osteoclast differentiation by a mechanism independent of the ODF/RANKL–RANK interaction. The Journal of experimental medicine 2000;191:275-86.10.1084/jem.191.2.275219574610637272
  23. 23. Pan Z, Guzeldemir E, Toygar HU, Bal N, Bulut S. Nitric oxide synthase in gingival tissues of patients with chronic periodontitis and with and without diabetes. J Periodontol. 2010;81(1):109-20.10.1902/jop.2009.09045420059423
  24. 24. Collin, H-L, Uusitupa, M, Niskanen, L, Kontturi-Närhi, V, Markkanen, H, Koivisto, A-M, et al. Periodontal Findings in Elderly Patients with Non-Insulin Dependent Diabetes Mellitus. Journal of Periodontology 1998;69:962-6.10.1902/jop.1998.69.9.9629776023
  25. 25. 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. Journal of Periodontology 1996;67:1085-93.10.1902/jop.1996.67.10s.10858910827
  26. 26. Kıran, M, Arpak, N, Ünsal, E, Erdoğan, MF. The effect of improved periodontal health on metabolic control in type 2 diabetes mellitus. Journal of Clinical Periodontology 2005;32:266-72.10.1111/j.1600-051X.2005.00658.x15766369
  27. 27. Singh, S, Kumar, V, Kumar, S, Subbappa, A. The effect of periodontal therapy on the improvement of glycemic control in patients with type 2 diabetes mellitus: A randomized controlled clinical trial. International Journal of Diabetes in Developing Countries 2008;28:38-44.10.4103/0973-3930.43097277201019902046
  28. 28. Katagiri, S, Nitta, H, Nagasawa, T, Uchimura, I, Izumiyama, H, Inagaki, K, et al. Multi-center intervention study on glycohemoglobin (HbA1c) and serum, high-sensitivity CRP (hs-CRP) after local anti-infectious periodontal treatment in type 2 diabetic patients with periodontal disease. Diabetes Research and Clinical Practice 2009;83:308-15.10.1016/j.diabres.2008.10.01619168253
  29. 29. Koromantzos, PA, Makrilakis, K, Dereka, X, Katsilambros, N, Vrotsos, IA, Madianos, PN. A randomized, controlled trial on the effect of non-surgical periodontal therapy in patients with type 2 diabetes. Part I: effect on periodontal status and glycaemic control. Journal of Clinical Periodontology 2011;38:142-7.10.1111/j.1600-051X.2010.01652.x21114680
  30. 30. Moeintaghavi, A, Arab, HR, Bozorgnia, Y, Kianoush, K, Alizadeh, M. Non-surgical periodontal therapy affects metabolic control in diabetics: a randomized controlled clinical trial. Australian Dental Journal 2012;57:31-7.10.1111/j.1834-7819.2011.01652.x22369555
  31. 31. Wang, X, Han, X, Guo, X, Luo, X, Wang, D. The Effect of Periodontal Treatment on Hemoglobin A1c Levels of Diabetic Patients: A Systematic Review and Meta-Analysis. PLoS ONE 2014;9:e108412.10.1371/journal.pone.0108412417791425255331
  32. 32. Southerland JH, Taylor GW, Moss K, Beck JD, Offenbacher S. Commonality in chronic inflammatory diseases: periodontitis, diabetes, and coronary artery disease. Periodontol 2000. 2006;40:130-43.10.1111/j.1600-0757.2005.00138.x
  33. 33. Chen, L, Luo, G, Xuan, D, Wei, B, Liu, F, Li, J, et al. Effects of non-surgical periodontal treatment on clinical response, serum inflammatory parameters, and metabolic control in patients with type 2 diabetes: a randomized study. Journal of periodontology 2012;83:435-43.10.1902/jop.2011.110327
  34. 34. Rodrigues, DC, Taba, M, Novaes, AB, Souza, SLS, Grisi, MFM. Effect of Non-Surgical Periodontal Therapy on Glycemic Control in Patients with Type 2 Diabetes Mellitus. Journal of Periodontology 2003;74:1361-7.10.1902/jop.2003.74.9.1361
  35. 35. Nishimura, F, Iwamoto, Y, Mineshiba, J, Shimizu, A, Soga, Y, Murayama, Y. Periodontal Disease and Diabetes Mellitus: The Role of Tumor Necrosis Factor-α in a 2-Way Relationship. Journal of Periodontology 2003;74:97-102.10.1902/jop.2003.74.1.97
  36. 36. Baud, V, Karin, M. Signal transduction by tumor necrosis factor and its relatives. Trends in cell biology 2001;11:372-7.10.1016/S0962-8924(01)02064-5
  37. 37. Aderka, D. The potential biological and clinical significance of the soluble tumor necrosis factor receptors. Cytokine & growth factor reviews 1996;7:231-40.10.1016/S1359-6101(96)00026-3
  38. 38. Franco C, Patricia H, Timo S, Claudia B, Marcela H. Matrix Metalloproteinases as Regulators of Periodontal Inflammation. Int J Mol Sci. 2017;18(2).10.3390/ijms18020440534397428218665
  39. 39. Romanelli, R, Mancini, S, Laschinger, C, Overall, CM, Sodek, J, McCulloch, CA. Activation of neutrophil collagenase in periodontitis. Infection and immunity 1999;67:2319-26.10.1128/IAI.67.5.2319-2326.199911597310225890
  40. 40. Bhavsar, A.P.; Guttman, J.A.; Finlay, B.B. Manipulation of host-cell pathways by bacterial pathogens. Nature. 2007, 449, 827–834.10.1038/nature06247
  41. 41. Graves, D. Cytokines that promote periodontal tissue destruction. J. Periodontol. 2008, 79, 1585–1591.10.1902/jop.2008.080183
  42. 42. Houri-Haddad, Y.; Wilensky, A.; Shapira, L. T-cell phenotype as a risk factor for periodontal disease. Periodontol. 2000 2007, 45, 67–75.10.1111/j.1600-0757.2007.00227.x
  43. 43. Nitta, H.; Katagiri, S.; Nagasawa, T.; Izumi, Y.; Ishikawa, I.; Izumiyama, H.; Uchimura, I.; Kanazawa, M.; Chiba, H.; Matsuo, A.; et al. The number of microvascular complications is associated with an increased risk for severity of periodontitis in type 2 diabetic patients: Results of a multicenter hospital-based cross-sectional 1. study. J. Diabetes Investig. 2017;8(5):677-68610.1111/jdi.12633558395828129466
  44. 44. Leppilahti, J, Ahonen, MM, Hernández, M, Munjal, S, Netuschil, L, Uitto, VJ, et al. Oral rinse MMP-8 point-of-care immuno test identifies patients with strong periodontal inflammatory burden. Oral diseases 2011;17:115-22.10.1111/j.1601-0825.2010.01716.x20659259
  45. 45. Sorsa, T.; Gursoy, U.K.; Nwhator, S.; Hernandez, M.; Tervahartiala, T.; Leppilahti, J.; Gursoy, M.; Könönen, E.; Emingil, G.; Pussinen, P.J.; et al. Analysis of matrix metalloproteinases, especially MMP-8, in gingival creviclular fluid, mouthrinse and saliva for monitoring periodontal diseases. Periodontol. 2000. 2016; 70(1):142-63.10.1111/prd.12101
  46. 46. Luo, K.W.; Wei, C.; Lung, W.Y.; Wei, X.Y.; Cheng, B.H.; Cai, Z.M.; Huang, W.R. EGCG inhibited bladder cancer SW780 cell proliferation and migration both in vitro and in vivo via down-regulation of NF-_B and MMP-9. J. Nutr. Biochem. 2016, 41, 56–64.10.1016/j.jnutbio.2016.12.004
  47. 47. Stawowczyk, M.;Wellenstein, M.D.; Lee, S.B.; Yomtoubian, S.; Durrans, A.; Choi, H.; Huang,W.R. Matrix Metalloproteinase 14 promotes lung cancer by cleavage of Heparin-Binding EGF-like Growth Factor. Neoplasia 2017; 19(2):55-64.10.1016/j.neo.2016.11.005519872828013056
  48. 48. Shintani, T.; Kusuhara, Y.; Daizumoto, K.; Dondoo, T.O.; Yamamoto, H.; Mori, H.; Fukawa, T.; Nakatsuji, H.; Fukumori, T.; Takahashi, M.; et al. The Involvement of Hepatocyte Growth Factor-MET-Matrix Metalloproteinase 1 Signaling in Bladder Cancer Invasiveness and Proliferation. Effect of the MET Inhibitor, Cabozantinib (XL184), on Bladder Cancer Cells. Urology. 2017; 101:169.e7-169.e13.10.1016/j.urology.2016.12.00628013036
  49. 49. Butler, G.S.; Overall, C.M. Updated biological roles for matrix metalloproteinases and new “intracellular” substrates revealed by degradomics. Biochemistry. 2009; 48(46):10830-45.10.1021/bi901656f19817485
  50. 50. Morrison CJ, Butler GS, Rodríguez D, Overall CM. Matrix metalloproteinase proteomics: substrates, targets, and therapy. Curr Opin Cell Biol. 2009;21(5):645-53.10.1016/j.ceb.2009.06.00619616423
  51. 51. Heikkinen, A.M.; Sorsa, T.; Pitkaniemi, J.; Tervahartiala, T.; Kari, K.; Broms, U.; Koskenvuo, M.; Meurman, J.H. Smoking affects diagnostic salivary periodontal disease biomarker levels in adolescents. J. Periodontol. 2010; 81(9):1299-30710.1902/jop.2010.09060820450405
  52. 52. Hernandez, M.; Valenzuela, M.A.; Lopez-Otin, C.; Alvarez, J.; Lopez, J.M.; Vernal, R.; Gamonal, J. Matrix metalloproteinase-13 is highly expressed in destructive periodontal disease activity. J. Periodontol. 2006; 77(11):1863-70.10.1902/jop.2006.05046117076612
  53. 53. Folgueras, A.R.; Pendas, A.M.; Sanchez, L.M.; Lopez-Otin, C. Matrix metalloproteinases in cancer: From new functions to improved inhibition strategies. Int. J. Dev. Biol. 2004; 48(5-6):411-24.10.1387/ijdb.041811af15349816
  54. 54. Overall, C.M. Molecular determinants of metalloproteinase substrate specificity: Matrix metalloproteinase substrate binding domains, modules, and exosites. Mol. Biotechnol. 2002; 22(1):51-86.10.1385/MB:22:1:051
  55. 55. Leppilahti, J.M.; Hernandez-Rios, P.A.; Gamonal, J.A.; Tervahartiala, T.; Brignardello-Petersen, R.; Mantyla, P.; Sorsa, T.; Hernández, M. Matrix metalloproteinases and myeloperoxidase in gingival crevicular fluid provide site-specific diagnostic value for chronic periodontitis. J. Clin. Periodontol. 2014, 41, 348–356.10.1111/jcpe.12223
  56. 56. Mori, K.; Shibanuma, M.; Nose, K. Invasive potential induced under long-term oxidative stress in mammary epithelial cells. Cancer Res. 2004, 64, 7464–7472.10.1158/0008-5472.CAN-04-1725
  57. 57. Yoon, S.O.; Park, S.J.; Yoon, S.Y.; Yun, C.H.; Chung, A.S. Sustained production of H2O2 activates pro-matrix metalloproteinase-2 through receptor tyrosine kinases/phosphatidylinositol 3-kinase/NF-_B pathway. J. Biol. Chem. 2002, 277, 30271–30282.10.1074/jbc.M202647200
  58. 58. Siwik, D.A.; Pagano, P.J.; Colucci, W.S. Oxidative stress regulates collagen synthesis and matrix metalloproteinase activity in cardiac fibroblasts. Am. J. Physiol. Cell Physiol. 2001, 280, C53–C60.10.1152/ajpcell.2001.280.1.C53
  59. 59. Tiranathanagul, S.; Yongchaitrakul, T.; Pattamapun, K.; Pavasant, P. Actinobacillus actinomycetemcomitans lipopolysaccharide activates matrix metalloproteinase-2 and increases receptor activator of nuclear factor-_B ligand expression in human periodontal ligament cells. J. Periodontol. 2004, 75, 1647–1654.10.1902/jop.2004.75.12.1647
  60. 60. Osorio, C.; Cavalla, F.; Paula-Lima, A.; Diaz-Araya, G.; Vernal, R.; Ahumada, P.; Gamonal, J.; Hernández, M. H2O2 activates matrix metalloproteinases through the nuclear factor _B pathway and Ca2+ signals in human periodontal fibroblasts. J. Periodontal Res. 2015, 50, 798–806.10.1111/jre.12267
  61. 61. Astrom, P.; Pirila, E.; Lithovius, R.; Heikkola, H.; Korpi, J.T.; Hernandez, M.; Sorsa, T.; Salo, T. Matrix metalloproteinase-8 regulates transforming growth factor-_1 levels in mouse tongue wounds and fibroblasts in vitro. Exp. Cell Res. 2014, 328, 217–227.10.1016/j.yexcr.2014.07.010
  62. 62. Eguchi, T.; Kubota, S.; Kawata, K.; Mukudai, Y.; Uehara, J.; Ohgawara, T.; Ibaragi, S.; Sasaki, A.; Kuboki, T.; Takigawa, M. Novel transcription-factor-like function of human matrix metalloproteinase 3 regulating the CTGF/CCN2 gene. Mol. Cell. Biol. 2008, 28, 2391–2413.10.1128/MCB.01288-07
  63. 63. Goncxalves FM, Jacob-Ferreira AL, Gomes VA, et al. Increased circulating levels of matrix metalloproteinase (MMP)-8, MMP-9, and pro-inflammatory markersin patients with metabolic syndrome. Clinica Chimica Acta.2009;403:173-177.10.1016/j.cca.2009.02.01319254704
  64. 64. Kadoglou NP, Daskalopoulou SS, Perrea D, Liapis CD.Matrix metalloproteinases and diabetic vascular complications. Angiology. 2005;56:173-189.10.1177/00033197050560020815793607
  65. 65. Thrailkill KM, Clay Bunn R, Fowlkes JL. Matrix metal-loproteinases: Their potential role in the pathogenesisof diabetic nephropathy. International Journal of Basic and Clinical Endocrinology. 2009;35:1-10.10.1007/s12020-008-9114-6
  66. 66. Koromantzos PA, Makrilakis K, Dereka X, Offenbacher S, Katsilambros N, Vrotsos IA, Madianos PN.Effect of non-surgical periodontal therapy on C-reactive protein, oxidative stress, and matrix metalloproteinase (MMP)-9 and MMP-2 levels in patients with type 2 diabetes: a randomized controlled study. Journal of Periodontology. 2012;83(1):3-10.10.1902/jop.2011.11014821627458
  67. 67. Kumar MS, Vamsi G, Sripriya R, Sehgal PK.Expression of matrix metalloproteinases (MMP-8 and -9) in chronic periodontitis patients with and without diabetes mellitus. Journal of Periodontology. 2006;77(11):1803-8.10.1902/jop.2006.050293
  68. 68. Halliwell B. Free radicals, antioxidants and human disease: Curiosity, cause or consequence. Lancet. 1994; 344:721-724.10.1016/S0140-6736(94)92211-X
  69. 69. Page RC, Kornman K. The pathogenesis of human periodontitis:an introduction. Periodontol 2000 1997;14:9-11.10.1111/j.1600-0757.1997.tb00189.x
  70. 70. Cesaratto L, Vascotto C, Calligaris S, Tell G. The importance of redox state in liver damage. Ann Hepatol 2004;3:86-92.10.1016/S1665-2681(19)32099-X
  71. 71. Jozanov-Stankov О, Dobutović DB, Djuric J, Isenović ER. Okidativni stres kao činilac kod oboljevanja i patoloških poremećaja ljudi. Apoll Med Aescul 2007;5:31-6.
  72. 72. Halliwell B, Whiteman M. Measuring reactive species and oxidative damage in vivo and in cell cultures: how should you do it and what do the results mean? Brit J Pharmacol 2004;142:231-55.10.1038/sj.bjp.0705776
  73. 73. Canakci CF, Ciceki Y, Canakci V. Reactive oxygen species and human inflammatory periodontal diseases. Biochem (Mosc) 2005;70:619-28.10.1007/s10541-005-0161-916038603
  74. 74. Waddington RJ, Moseley R, Embery G. Reactive oxygen species: a potential role in the pathogenesis of periodontal diseases. Oral Dis 2000;6:138-51.10.1111/j.1601-0825.2000.tb00325.x10822357
  75. 75. Giannobile WV. C-telopeptide pyridinolone cross-links. Sensitive indicators of periodontal tissue destruction. Ann NY Acad Sci 1999;30:404–12.10.1111/j.1749-6632.1999.tb07698.x258693010415744
  76. 76. Mahajan, A, Singh, B, Kashyap, D, Kumar, A, Mahajan, P. Interspecies communication and periodontal disease. The Scientific World Journal 2013;2013:10.1155/2013/765434387430924396307
  77. 77. Johnson, GK, Slach, NA. Impact of tobacco use on periodontal status. Journal of Dental Education 2001;65:313-21.10.1002/j.0022-0337.2001.65.4.tb03401.x
  78. 78. Preshaw, PM, Taylor, JJ. How has research into cytokine interactions and their role in driving immune responses impacted our understanding of periodontitis? Journal of clinical periodontology 2011;38:60-84.10.1111/j.1600-051X.2010.01671.x
  79. 79. Mukhopadhyay CK, Chatterjee IB. Free metal iondependent oxidative damage of collagen. Protection by ascorbic acid. J Biol Chem 1994;269:30200–5.10.1016/S0021-9258(18)43797-0
  80. 80. Garrett IR, Boyce BF, Oreffo ROC, Bonewald L, Poser J, Mundy GR. Oxygen-derived free radicals stimulate osteoclastic bone resorption in rodent bone in vitro and in vivo. J Clin Invest 1990;85:632–9.10.1172/JCI1144852964762312718
  81. 81. Bax BE, Alam AS, Banerji B, Bax CM, Bevis PJ, Stevens CR et al. Stimulation of osteoclastic bone resorption by hydrogen peroxide. Biochem Biophys Res Commun 1992;183:1153–8.10.1016/S0006-291X(05)80311-0
  82. 82. Hall TJ, Schaeublin M, Jeker H, Fuller K, Chambers TJ. The role of reactive oxygen intermediates in osteoclastic bone resorption. Biochem Biophys Res Commun 1995;207:280–7.10.1006/bbrc.1995.11847857277
  83. 83. Moseley R, Waddington RJ, Embery G. The modification of alveolar bone proteoglycans by reactive species in vitro. Connect Tissue Res 1998;37:13–28.10.3109/030082098090288979643644
  84. 84. Chapple ILC, Matthews JB. The role of reactive oxygen and antioxidant species in periodontal tissue destruction. Periodontol 2000. 2007;43:160-232.10.1111/j.1600-0757.2006.00178.x17214840
  85. 85. Tamaki N, Tomofuji T, Ekuni D, Yamanaka R, Yamamoto T, Morita M. Short-term effects on non-surgical periodontal treatment on plasma level of reactive oxygen metabolites in patients with chronic periodontitis. J Periodontol 2009;80:901-6.10.1902/jop.2009.08064019485819
  86. 86. Ekuni D, Tomofuji T, Tamaki N, Sanbe T, Azuma T, Yamanaka R, et al. Mechanical stimulation of gingiva reduces plasma 8-OHdG level in rat periodontitis. Arch Oral Biol 2008;53:324-9.10.1016/j.archoralbio.2007.10.00518031711
  87. 87. Tomofuji T, Sanbe T, Ekuni D, Azuma T, Irie K, Maruyama T, et al. Oxidative damage of rat liver induced by ligature-induced periodontitis and chronic ethanol consumption. Arch Oral Biol 2008;53:1113-8.10.1016/j.archoralbio.2008.05.01518603227
  88. 88. Palasciano G, Moshetta A, Palmieri VO, Grattagliano I, Iacobellis G, Portincasa P. Non-alcoholic fatty liver disease in the metabolic syndrome. Curr Pharm Design 2007;13:2193-8.10.2174/13816120778103965217627552
  89. 89. Albano E. Oxidative mechanisms in the pathogenesis of alcoholic liver disease. Mol Aspects Med 2008;29:9-16.10.1016/j.mam.2007.09.00418045675
  90. 90. Ekuni D, Tomofuji T, Sanbe T, Irie K, Azuma T, Maruyama T, et al. Periodontitis-induced lipid peroxidation in rat descending aorta is involvedin initiation of atherosclerosis. J Periodontal Res 2009;44:434–4210.1111/j.1600-0765.2008.01122.x19210335
  91. 91. Valko M, Leibfritz D, Moncol J, Cronin MTD, Mazur M, Telser J. Free radicals and antioxidants in normal physiological functions and human disease. International Journal of Biochemistry and Cell Biology. 2007; 39(1):44–87.10.1016/j.biocel.2006.07.00116978905
  92. 92. Yamamoto Y, Hirose H, saito I, Nishikai K, Saruta T. Adiponectin, an adipocytederived protein, predicts future insulin resistance: two – year follow – up study in Japanese population. The Journal of Clinical Endocrinology and Metabolism. 2004; 89(1):87-90.10.1210/jc.2003-03116314715832
  93. 93. Liu Y, Zhang Q. Periodontitis aggravated pancreatic β-cell dysfunction in diabetic mice through interleukin-12 regulation on Klotho. J Diabetes Investig. 2016;7(3):303-11.10.1111/jdi.12410484788327330715
  94. 94. Monea A, Mezei T, Popsor S, Monea M. Oxidative Stress: A Link between Diabetes Mellitus and Periodontal Disease. International Journal of Endocrinology. 2014; 1–4.10.1155/2014/917631426569225525432
  95. 95. Vincent RR, Appukuttan D, Dhayanand JV, Balasundaram A. Oxidative stress in chronic periodontitis patients with type II diabetes mellitus. European Journal of Dentistry. 2018; 12(2): 225–231.10.4103/ejd.ejd_244_17600479329988233
  96. 96. Arana C, Moreno-Fernández AM, Gómez-Moreno G, Morales-Portillo C, Serrano-Olmedo I, de la Cuesta Mayor MC, Martín Hernández T. Increased salivary oxidative stress parameters in patients with type 2 diabetes: Relation with periodontal disease. Еndocrinologia, diabetes y nutricion. 2017;64(5):258-264.10.1016/j.endinu.2017.03.00528495321
  97. 97. Patil VS, Patil VP, Gokhale N, Acharya A, Kangokar P. Chronic Periodontitis in Type 2 Diabetes Mellitus: Oxidative Stress as a Common Factor in Periodontal Tissue Injury. Јournal of clinical and diagnostic research. 2016; 10(4):12-16.10.7860/JCDR/2016/17350.7542486608827190790
  98. 98. Blasco-Baque V, Garidou L, Pomié C, Escoula Q, Loubieres P, Le Gall-David S, Lemaitre M, Nicolas S, Klopp P, Waget A, Azalbert V, Colom A, Bonnaure-Mallet M, Kemoun P, Serino M, Burcelin R. Periodontitis induced by Porphyromonas gingivalis drives periodontal microbiota dysbiosis and insulin resistance via an impaired adaptive immune response. Gut. 2017;66(5):872-885.10.1136/gutjnl-2015-309897553122726838600
DOI: https://doi.org/10.2478/sjecr-2019-0051 | Journal eISSN: 2956-2090 | Journal ISSN: 2956-0454
Language: English
Submitted on: Sep 6, 2019
|
Accepted on: Oct 25, 2019
|
Published on: Nov 25, 2019
In partnership with: Paradigm Publishing Services
Publication frequency: 4 issues per year

© 2019 Dragana Stanisic, Radmila Obradovic, Sanja Vujovic, Milica Jovanovic, Vladimir Zivkovic, published by University of Kragujevac, Faculty of Medical Sciences
This work is licensed under the Creative Commons Attribution-NonCommercial-NoDerivatives 3.0 License.

AHEAD OF PRINT