Research Article
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Determination of Oxidative Stress Parameters and Tissue Factor Activity in the Saliva of Patients with Periodontitis

Year 2019, Volume: 78 Issue: 2, 63 - 68, 06.12.2019

Abstract

Objective: Periodontitis, an inflammatory disease, leads to the destruction of the periodontium and results in tooth loss. Reactive oxygen species are involved in the destruction of periodontal tissues and systemic inflammation. The aim of the study was to evaluate and compare the oxidative status in different kinds of periodontal disease and whether the treatment amends these effects. Materials and Methods: Whole saliva was collected from 30 patients with chronic marginal gingivitis, chronic periodontitis and generalized aggressive periodontitis at baseline and after non-surgical periodontal therapy and 10 healthy control subjects. Lipid peroxidation (LPO) and glutathione (GSH) levels and glutathione-s-transferase, superoxide dismutase catalase and tissue factor (TF) activities were determined in the whole saliva. Results: Antioxidant enzyme activities were significantly higher in periodontitis groups before non-surgical periodontal therapy and also increased LPO levels and decreased TF activities were found in these groups. Significant decreases in antioxidant enzymes and LPO levels, and increases in TF activities were detected after treatment. GSH levels increased after treatment. Conclusion: Increased antioxidant enzyme activities and LPO levels indicate destruction of periodontal tissues due to excessive radical production. Treatment of periodontitis and restoring the balance of oxidant-antioxidants ameliorates tissue damage caused by oxygen species and inflammation. 

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References

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  • 2. Silva N, Abusleme L, Bravo D, Dutzan N, Garcia-Sesnich J, Vernal R, et al. Host response mechanisms in periodontal diseases. J Appl Oral Sci 2015; 23(3):329-55.
  • 3. Armitage GC. Development of a classification system for periodontal diseases and conditions. Ann Periodontol 1999; 4(1): 1-6.
  • 4. Lamont RJ, Hajishengallis G. Polymicrobial synergy and dysbiosis in inflammatory disease. Trends Mol Med 2015; 21(3): 172-83.
  • 5. Liu G, Luan Q, Chen F, Chen Z, Zhang Q, Yu X. Shift in the subgingival microbiome following scaling and root planing in generalized aggressive periodontitis. J Clin Periodontol 2018; 45(4): 440-52.
  • 6. Waddington RJ, Moseley R, Embery G. Reactive oxygen species: A potential role in the pathogenesis of periodontal diseases. Oral Dis 2000; 6: 138-51.
  • 7. Piedrafta G, Keller M, Ralser M. The impact of non-enzymatic reactions and enzyme promiscuity on cellular metabolism during (oxidative) stress conditions. Biomolecules 2015; 5(3): 2101-122.
  • 8. Sculley DV, Langley-Evans SC. Periodontal disease is associated with lower antioxidant capacity in whole saliva and evidence of increased protein oxidation. Clin Sci (Lond) 2003; 105: 167-72.
  • 9. Spiekerman CF, Hujoel PP, DeRouen TA. Bias induced by selfreported smoking on periodontitis-systemic disease associations. J Dent Res 2003;82(5) : 345-49.
  • 10. Kuboniwa M, Sakanaka A, Hashino E, Bamba T, Fukusaki E, Amano A. Prediction of periodontal inflammation via metabolic profiling of saliva. J Dent Res 2016; 95(12): 1381-86.
  • 11. Löe H. and Silness J. Periodontal disease in pregnancy. Prevalance and severity. Acta Odontol Scand 1963; 21(6): 533-55.
  • 12. Silnes J and Löe H. Periodontal disease in pregnancy II. Correlation between oral hygiene and periodontal condition. Acta Odontol Scand 1964; 22(1): 121-35.
  • 13. Beutler E. Glutathione: red cell metabolism. A manual biochemical methods 1975; pp. 72-136, Grune and Stratton, New York.
  • 14. Yagi K. Assay for blood plasma or serum. Methods Enzymol 1984; 105: 328-37.
  • 15. Habig WH, Jacopy WB. Assays for differentiation of glutathione-Stransferases. Method Enzymol 1981; 77: 398-405.
  • 16. Aebi H. Catalase in vitro. In (Ed. Bergmeye HU) Methods of enzymatic analysis 1974; pp. 673-7, New York.
  • 17. Mylroie AA, Collins H, Umbles C, Kyle J. Erythrocyte superoxide dismutase activity and other parameters of copper status in rats ingesting lead acetate. Toxicol Appl Pharmacol 1986; 82: 512-20.
  • 18. Ingram GIC, Hills M. Reference method for the one stage prothrombin time test on human blood. Thromb Haemostas 1976; 36: 237-38.
  • 19. Dave S, Balista EL Jr, Thomas E, Van D. Cardiovascular disease and periodontal disease: commonality and causation. Compendium 2004; 25(7): 26-37.
  • 20. D’Aiuto F, Nibali L, Parkar M, Patel K, Suvan J, Donos N. Oxidative stress, systemic inflammation, and severe periodontitis. J Dent Res 2010; 89: 1241-46.
  • 21. Panjamurthy K, Manoharan S, Ramachandran CR. Lipid peroxidation and antioxidant status in patients with periodontitis. Cell Mol Biol Lett 2005; 10: 255-64.
  • 22. Patel SP, Pradeep AR, Chowdhry S. Crevicular fluid levels of plasma glutathione peroxidase (eGPx) in periodontal health and disease. Arch Oral Biol 2009; 54: 543-48.
  • 23. Amarnath K, Nellore J. Antioxidant potential of phytonanoparticles in an emerging biofluid (saliva) of periodontitis patients. In Nanoscience, Engineering and Technology (ICONSET), 2011 International Conference, 2011; pp. 401-407.IEEE.
  • 24. Akalin FA, Baltacioglu E, Alver A, Karabulut E. Lipid peroxidation levels and total oxidant status in serum, saliva and gingival crevicular fluid in patients with chronic periodontitis. J Clin Periodontol 2007; 34: 558-65.
  • 25. Yagan A, Kesim S, Liman N. Effect of low-dose doxycycline on serum oxidative status, gingival antioxidant levels and alveolar bone loss in experimental periodontitis in rats. J Periodontol 2014; 85(3): 478-89.
  • 26. Tsai CC, Chen HS, Chen SL, Ho YP, Ho KY, Wu YM, et al. Lipid peroxidation: a possible role in the induction and progression of chronic periodontitis. J Periodontal Res 2005; 40(5): 378-84.
  • 27. Tonguc MO, Ozturk O, Sutcu R, Ceyhan BM, Kılınc G, Sonmez Y, et al. The impact of smoking status on antioxidant enzyme activity and malondialdehyde levels in chronic periodontitis. J Periodontol 2011; 82(9): 1320-28.
  • 28. Oktay S, Chukkapalli SS, Rivera-Kweh MF, Velsko IM, Holliday LS, Kesavalu L. Periodontitis in rats induces systemic oxidative stress that is controlled by bone-targeted antiresorptives. J Periodontol 2015; 86(1): 137-45.
  • 29. Fabrini R, Bocedi A, Camerini S, Fusetti M, Ottaviani F, Passali FM et al. Inactivation of human salivary glutathione transferase p1-1 by hypothiocyanite: A post-translational control system in search of a role. Ed. Fernando Rodrigues-Lima.PLoS ONE 2014; 9(11): e112797.
  • 30. Borges I, Moreira EAM, Filho DW, Tiago Oliveira TB, Silva MBS, Frode TS.Proinflammatory and oxidative stress markers in patients with periodontal disease. Mediators Inflamm 2007; 2007: 1-5.
  • 31. Akalin FA, Toklu E, Renda N. Analysis of superoxide dismutase activity levels in gingiva and gingival crevicular fluid in patients with chronic periodontitis and periodontally healthy controls. J Clin Periodontol 2005; 32:238-43.
  • 32. Wei D, Zhang X-L, Wang Y-Z, Yang C-X, Chen G. Lipid peroxidation levels, total oxidant status and superoxide dismutase in serum, saliva and gingival crevicular fluid in chronic periodontitis patients before and after periodontal therapy. Australian Dent J 2010; 55: 70-8.
  • 33. Aziz AS, Kalekar MG, Benjamin T, Suryakar AN, Prakashan MM. Effect of nonsurgical periodontal therapy an some oxidative stress markers in patients with chronic periodontitis: A biochemical study. World J Dent 2013; 4: 17-23. 34. Roth GA, Moser B, Roth-Walter E GiacoDa MD, Harja E, Papapanou PN, et al. Infection with a periodontal pathogen increases mononuclear cell adhesion to human aortic endothelial cells. Atherosclerosis 2007; 190: 271-81.
  • 35. Buhlin K, Gustafsson A, Hakansson J, Klinge B. Oral health and cardiovascular disease in Sweden. J CIin Periodontol 2002; 291: 254-59.
  • 36. 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: 1777-82.
  • 37. Emekli Alturfan E, Basar I, Malali E, Elemek E, Oktay S, Ayan F, et al. Plasma tissue factor levels and salivary tissue factor activities of periodontitis patients with and without cardiovascular disease. Pathophysiol Haemost Thromb 2010; 37(2-4): 77-81.
  • 38. Caton JG, Armitage G, Berglundh T, Chapple IL, Jepsen S, Kornman KS, Sanz M, Tonetti MS, Mealey BL, Papapanou PN, Sa Tonetti MS. A new classification scheme for periodontal and peri‐implant diseases and conditions–Introduction and key changes from the 1999 classification. J Periodontol 2018; 89: 1-8.
Year 2019, Volume: 78 Issue: 2, 63 - 68, 06.12.2019

Abstract

References

  • 1. Ridgeway EE. Periodontal disease: diagnosis and management. J Am Acad Nurse Pract 2000; 12: 79-83.
  • 2. Silva N, Abusleme L, Bravo D, Dutzan N, Garcia-Sesnich J, Vernal R, et al. Host response mechanisms in periodontal diseases. J Appl Oral Sci 2015; 23(3):329-55.
  • 3. Armitage GC. Development of a classification system for periodontal diseases and conditions. Ann Periodontol 1999; 4(1): 1-6.
  • 4. Lamont RJ, Hajishengallis G. Polymicrobial synergy and dysbiosis in inflammatory disease. Trends Mol Med 2015; 21(3): 172-83.
  • 5. Liu G, Luan Q, Chen F, Chen Z, Zhang Q, Yu X. Shift in the subgingival microbiome following scaling and root planing in generalized aggressive periodontitis. J Clin Periodontol 2018; 45(4): 440-52.
  • 6. Waddington RJ, Moseley R, Embery G. Reactive oxygen species: A potential role in the pathogenesis of periodontal diseases. Oral Dis 2000; 6: 138-51.
  • 7. Piedrafta G, Keller M, Ralser M. The impact of non-enzymatic reactions and enzyme promiscuity on cellular metabolism during (oxidative) stress conditions. Biomolecules 2015; 5(3): 2101-122.
  • 8. Sculley DV, Langley-Evans SC. Periodontal disease is associated with lower antioxidant capacity in whole saliva and evidence of increased protein oxidation. Clin Sci (Lond) 2003; 105: 167-72.
  • 9. Spiekerman CF, Hujoel PP, DeRouen TA. Bias induced by selfreported smoking on periodontitis-systemic disease associations. J Dent Res 2003;82(5) : 345-49.
  • 10. Kuboniwa M, Sakanaka A, Hashino E, Bamba T, Fukusaki E, Amano A. Prediction of periodontal inflammation via metabolic profiling of saliva. J Dent Res 2016; 95(12): 1381-86.
  • 11. Löe H. and Silness J. Periodontal disease in pregnancy. Prevalance and severity. Acta Odontol Scand 1963; 21(6): 533-55.
  • 12. Silnes J and Löe H. Periodontal disease in pregnancy II. Correlation between oral hygiene and periodontal condition. Acta Odontol Scand 1964; 22(1): 121-35.
  • 13. Beutler E. Glutathione: red cell metabolism. A manual biochemical methods 1975; pp. 72-136, Grune and Stratton, New York.
  • 14. Yagi K. Assay for blood plasma or serum. Methods Enzymol 1984; 105: 328-37.
  • 15. Habig WH, Jacopy WB. Assays for differentiation of glutathione-Stransferases. Method Enzymol 1981; 77: 398-405.
  • 16. Aebi H. Catalase in vitro. In (Ed. Bergmeye HU) Methods of enzymatic analysis 1974; pp. 673-7, New York.
  • 17. Mylroie AA, Collins H, Umbles C, Kyle J. Erythrocyte superoxide dismutase activity and other parameters of copper status in rats ingesting lead acetate. Toxicol Appl Pharmacol 1986; 82: 512-20.
  • 18. Ingram GIC, Hills M. Reference method for the one stage prothrombin time test on human blood. Thromb Haemostas 1976; 36: 237-38.
  • 19. Dave S, Balista EL Jr, Thomas E, Van D. Cardiovascular disease and periodontal disease: commonality and causation. Compendium 2004; 25(7): 26-37.
  • 20. D’Aiuto F, Nibali L, Parkar M, Patel K, Suvan J, Donos N. Oxidative stress, systemic inflammation, and severe periodontitis. J Dent Res 2010; 89: 1241-46.
  • 21. Panjamurthy K, Manoharan S, Ramachandran CR. Lipid peroxidation and antioxidant status in patients with periodontitis. Cell Mol Biol Lett 2005; 10: 255-64.
  • 22. Patel SP, Pradeep AR, Chowdhry S. Crevicular fluid levels of plasma glutathione peroxidase (eGPx) in periodontal health and disease. Arch Oral Biol 2009; 54: 543-48.
  • 23. Amarnath K, Nellore J. Antioxidant potential of phytonanoparticles in an emerging biofluid (saliva) of periodontitis patients. In Nanoscience, Engineering and Technology (ICONSET), 2011 International Conference, 2011; pp. 401-407.IEEE.
  • 24. Akalin FA, Baltacioglu E, Alver A, Karabulut E. Lipid peroxidation levels and total oxidant status in serum, saliva and gingival crevicular fluid in patients with chronic periodontitis. J Clin Periodontol 2007; 34: 558-65.
  • 25. Yagan A, Kesim S, Liman N. Effect of low-dose doxycycline on serum oxidative status, gingival antioxidant levels and alveolar bone loss in experimental periodontitis in rats. J Periodontol 2014; 85(3): 478-89.
  • 26. Tsai CC, Chen HS, Chen SL, Ho YP, Ho KY, Wu YM, et al. Lipid peroxidation: a possible role in the induction and progression of chronic periodontitis. J Periodontal Res 2005; 40(5): 378-84.
  • 27. Tonguc MO, Ozturk O, Sutcu R, Ceyhan BM, Kılınc G, Sonmez Y, et al. The impact of smoking status on antioxidant enzyme activity and malondialdehyde levels in chronic periodontitis. J Periodontol 2011; 82(9): 1320-28.
  • 28. Oktay S, Chukkapalli SS, Rivera-Kweh MF, Velsko IM, Holliday LS, Kesavalu L. Periodontitis in rats induces systemic oxidative stress that is controlled by bone-targeted antiresorptives. J Periodontol 2015; 86(1): 137-45.
  • 29. Fabrini R, Bocedi A, Camerini S, Fusetti M, Ottaviani F, Passali FM et al. Inactivation of human salivary glutathione transferase p1-1 by hypothiocyanite: A post-translational control system in search of a role. Ed. Fernando Rodrigues-Lima.PLoS ONE 2014; 9(11): e112797.
  • 30. Borges I, Moreira EAM, Filho DW, Tiago Oliveira TB, Silva MBS, Frode TS.Proinflammatory and oxidative stress markers in patients with periodontal disease. Mediators Inflamm 2007; 2007: 1-5.
  • 31. Akalin FA, Toklu E, Renda N. Analysis of superoxide dismutase activity levels in gingiva and gingival crevicular fluid in patients with chronic periodontitis and periodontally healthy controls. J Clin Periodontol 2005; 32:238-43.
  • 32. Wei D, Zhang X-L, Wang Y-Z, Yang C-X, Chen G. Lipid peroxidation levels, total oxidant status and superoxide dismutase in serum, saliva and gingival crevicular fluid in chronic periodontitis patients before and after periodontal therapy. Australian Dent J 2010; 55: 70-8.
  • 33. Aziz AS, Kalekar MG, Benjamin T, Suryakar AN, Prakashan MM. Effect of nonsurgical periodontal therapy an some oxidative stress markers in patients with chronic periodontitis: A biochemical study. World J Dent 2013; 4: 17-23. 34. Roth GA, Moser B, Roth-Walter E GiacoDa MD, Harja E, Papapanou PN, et al. Infection with a periodontal pathogen increases mononuclear cell adhesion to human aortic endothelial cells. Atherosclerosis 2007; 190: 271-81.
  • 35. Buhlin K, Gustafsson A, Hakansson J, Klinge B. Oral health and cardiovascular disease in Sweden. J CIin Periodontol 2002; 291: 254-59.
  • 36. 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: 1777-82.
  • 37. Emekli Alturfan E, Basar I, Malali E, Elemek E, Oktay S, Ayan F, et al. Plasma tissue factor levels and salivary tissue factor activities of periodontitis patients with and without cardiovascular disease. Pathophysiol Haemost Thromb 2010; 37(2-4): 77-81.
  • 38. Caton JG, Armitage G, Berglundh T, Chapple IL, Jepsen S, Kornman KS, Sanz M, Tonetti MS, Mealey BL, Papapanou PN, Sa Tonetti MS. A new classification scheme for periodontal and peri‐implant diseases and conditions–Introduction and key changes from the 1999 classification. J Periodontol 2018; 89: 1-8.
There are 37 citations in total.

Details

Primary Language English
Journal Section Research Articles
Authors

Sehkar Oktay This is me 0000-0002-2878-288X

Ozge Ozoner This is me 0000-0001-8103-0700

Ebru Emekli Alturfan This is me 0000-0003-2419-8587

Ulku Noyan This is me 0000-0002-5489-9758

Publication Date December 6, 2019
Submission Date April 3, 2019
Published in Issue Year 2019 Volume: 78 Issue: 2

Cite

AMA Oktay S, Ozoner O, Emekli Alturfan E, Noyan U. Determination of Oxidative Stress Parameters and Tissue Factor Activity in the Saliva of Patients with Periodontitis. Eur J Biol. December 2019;78(2):63-68.