Oxidative stress and peri-implantitis: The role of oxidants and antioxidants

Document Type : Original Article

Authors

1 Department of Periodontology, Gulhane Faculty of Dentistry, University of Health Sciences, Ankara, Turkey

2 Department of Oral and Maxillofacial Surgery, Faculty of Dentistry, Bolu Abant Izzet Baysal University, Bolu, Turkey

3 Department of Biochemistry, Gulhane Faculty of Pharmacy, University of Health Sciences, Ankara, Turkey

Abstract

Background: Peri-implantitis is the main cause of implant failure and is associated with augmented oxidative stress or tissue destruction. In this study, it was aimed to investigate the oxidant-antioxidant balance parameters in individuals with peri-implantitis, considering the clinical findings and the control group.
Methods: Peri-implantitis (n = 30) and healthy (n = 30) individuals participated in the study. Peri-implant clinical parameters, including probing depth (PD), gingival index (GI), plaque index (PI), bleeding on probing (BoP), and keratinized mucosa width (KMW), were recorded. The levels of total antioxidant capacity (TAC), total oxidant capacity (TOC), oxidative stress index (OSI), and arylesterase (ARE) in saliva were examined. To identify the relationship between oxidative stress biomarkers and clinical parameters was used Spearman’s correlation coefficient.
Results: TOC values were higher in peri-implantitis, and they correlated with BoP, GI, PD, and PI (P = 0.004, r = 0.370; P = 0.010, r = 0.328; P = 0.038, r = 0.268; P = 0.007, r = 0.342, respectively). TAC values were higher in healthy and correlated with PI, BoP, and GI (P = 0.021, r = -0.297; P = 0.035, r = -0.273; P = 0.012, r = -0.321, respectively). OSI showed a negative correlation with the KMW (mm) (P = 0.046, r = -0.259).
Conclusion: Increased TOC and decreased TAC and ARE activity could be predictors of peri-implantitis development. Adequate KMW is important in the production of antioxidants.

Keywords

Main Subjects


  1. Berglundh T, Armitage G, Araujo MG, Avila-Ortiz G, Blanco J, Camargo PM, et al. Peri-implant diseases and conditions: consensus report of workgroup 4 of the 2017 World Workshop on the Classification of Periodontal and Peri-Implant Diseases and Conditions. J Periodontol. 2018;89 Suppl 1:S313-S8. doi: 10.1002/jper.17-0739.
  2. Mousavi Jazi M, Sadeghi Pour Rodsari HR, Mirmiran F. Level of oxidative stress markers in peri-implant crevicular fluid and their correlation with clinical parameters. J Dent (Tehran). 2015;12(5):340-6.
  3. Young IS, Woodside JV. Antioxidants in health and disease. J Clin Pathol. 2001;54(3):176-86. doi: 10.1136/jcp.54.3.176.
  4. Zhang T, Andrukhov O, Haririan H, Müller-Kern M, Liu S, Liu Z, et al. Total antioxidant capacity and total oxidant status in saliva of periodontitis patients in relation to bacterial load. Front Cell Infect Microbiol. 2015;5:97. doi: 10.3389/fcimb.2015.00097.
  5. Erel O. A new automated colorimetric method for measuring total oxidant status. Clin Biochem. 2005;38(12):1103-11. doi: 10.1016/j.clinbiochem.2005.08.008.
  6. Baltacıoğlu E, Yuva P, Aydın G, Alver A, Kahraman C, Karabulut E, et al. Lipid peroxidation levels and total oxidant/antioxidant status in serum and saliva from patients with chronic and aggressive periodontitis. Oxidative stress index: a new biomarker for periodontal disease? J Periodontol. 2014;85(10):1432-41. doi: 10.1902/jop.2014.130654.
  7. Cebeci E, Alibaz-Oner F, Usta M, Yurdakul S, Erguney M. Evaluation of oxidative stress, the activities of paraoxonase and arylesterase in patients with subclinical hypothyroidism. J Investig Med. 2012;60(1):23-8. doi: 10.2310/JIM.0b013e31823581dd.
  8. Yesilova Y, Turan E, Ucmak D, Selek S, Halil Yavuz İ, Tanrıkulu O. Reduced serum paraoxonase-1 levels in vitiligo: further evidence of oxidative stress. Redox Rep. 2012;17(5):214-8. doi: 10.1179/1351000212y.0000000025.
  9. Kul A, Uzkeser H, Ozturk N. Paraoxonase and arylesterase levels in Behcet’s disease and their relations with the disease activity. Biochem Genet. 2017;55(4):335-44. doi: 10.1007/s10528-017-9800-2.
  10. Olama SM, Elarman MM. Evaluation of paraoxonase and arylesterase activities in Egyptian patients with ankylosing spondylitis. Rheumatol Int. 2013;33(6):1487-94. doi: 10.1007/s00296-012-2591-1.
  11. de la Iglesia R, Mansego ML, Sánchez-Muniz FJ, Zulet MA, Martinez JA. Arylesterase activity is associated with antioxidant intake and paraoxonase-1 (PON1) gene methylation in metabolic syndrome patients following an energy restricted diet. EXCLI J. 2014;13:416-26.
  12. Li C, Chen JW, Ding FH, Shen Y, Liu ZH, Wang F, et al. Relationship of high-density lipoprotein-associated arylesterase activity to systolic heart failure in patients with and without type 2 diabetes. Sci Rep. 2019;9(1):5979. doi: 10.1038/s41598-019-42518-x.
  13. Silness J, Loe H. Periodontal disease in pregnancy.II. Correlation between oral hygiene and periodontal condtion. Acta Odontol Scand. 1964;22:121-35. doi: 10.3109/00016356408993968.
  14. Löe H. The gingival index, the plaque index and the retention index systems. J Periodontol. 1967;38(6):610-6. doi: 10.1902/jop.1967.38.6.610.
  15. Erel O. A novel automated direct measurement method for total antioxidant capacity using a new generation, more stable ABTS radical cation. Clin Biochem. 2004;37(4):277-85. doi: 10.1016/j.clinbiochem.2003.11.015.
  16. Haagen L, Brock A. A new automated method for phenotyping arylesterase (EC 3.1.1.2) based upon inhibition of enzymatic hydrolysis of 4-nitrophenyl acetate by phenyl acetate. Eur J Clin Chem Clin Biochem. 1992;30(7):391-5. doi: 10.1515/cclm.1992.30.7.391.
  17. Harma M, Harma M, Erel O. Increased oxidative stress in patients with hydatidiform mole. Swiss Med Wkly. 2003;133(41-42):563-6. doi: 10.4414/smw.2003.10397.
  18. Choromańska M, Klimiuk A, Kostecka-Sochoń P, Wilczyńska K, Kwiatkowski M, Okuniewska N, et al. Antioxidant defence, oxidative stress and oxidative damage in saliva, plasma and erythrocytes of dementia patients. Can salivary AGE be a marker of dementia? Int J Mol Sci. 2017;18(10):2205. doi: 10.3390/ijms18102205.
  19. Sánchez GA, Miozza VA, Delgado A, Busch L. Total salivary nitrates and nitrites in oral health and periodontal disease. Nitric Oxide. 2014;36:31-5. doi: 10.1016/j.niox.2013.10.012.
  20. Kamodyová N, Tóthová L, Celec P. Salivary markers of oxidative stress and antioxidant status: influence of external factors. Dis Markers. 2013;34(5):313-21. doi: 10.3233/dma-130975.
  21. Sánchez-Siles M, Lucas-Azorin J, Salazar-Sánchez N, Carbonell-Meseguer L, Camacho-Alonso F. Salivary concentration of oxidative stress biomarkers in a group of patients with peri-implantitis: a transversal study. Clin Implant Dent Relat Res. 2016;18(5):1015-22. doi: 10.1111/cid.12367.
  22. Mijiritsky E, Ferroni L, Gardin C, Peleg O, Gultekin A, Saglanmak A, et al. Presence of ROS in inflammatory environment of peri-implantitis tissue: in vitro and in vivo human evidence. J Clin Med. 2019;9(1):38. doi: 10.3390/jcm9010038.
  23. Brock GR, Butterworth CJ, Matthews JB, Chapple IL. Local and systemic total antioxidant capacity in periodontitis and health. J Clin Periodontol. 2004;31(7):515-21. doi: 10.1111/j.1600-051X.2004.00509.x.
  24. Sezer U, Ciçek Y, Canakçi CF. Increased salivary levels of 8-hydroxydeoxyguanosine may be a marker for disease activity for periodontitis. Dis Markers. 2012;32(3):165-72. doi: 10.3233/dma-2011-0876.
  25. Liskmann S, Vihalemm T, Salum O, Zilmer K, Fischer K, Zilmer M. Characterization of the antioxidant profile of human saliva in peri-implant health and disease. Clin Oral Implants Res. 2007;18(1):27-33. doi: 10.1111/j.1600-0501.2006.01296.x.
  26. Shapira L, Gordon B, Warbington M, Van Dyke TE. Priming effect of Porphyromonas gingivalis lipopolysaccharide on superoxide production by neutrophils from healthy and rapidly progressive periodontitis subjects. J Periodontol. 1994;65(2):129-33. doi: 10.1902/jop.1994.65.2.129.
  27. Brock G, Matthews J, Butterworth C, Chapple I. Effect of Periodontal Therapy on Local and Peripheral Antioxidant Capacity. University of Birmingham; 2002.
  28. Saita M, Kaneko J, Sato T, Takahashi SS, Wada-Takahashi S, Kawamata R, et al. Novel antioxidative nanotherapeutics in a rat periodontitis model: reactive oxygen species scavenging by redox injectable gel suppresses alveolar bone resorption. Biomaterials. 2016;76:292-301. doi: 10.1016/j.biomaterials.2015.10.077.
  29. Lim HC, Wiedemeier DB, Hämmerle CHF, Thoma DS. The amount of keratinized mucosa may not influence periimplant health in compliant patients: a retrospective 5-year analysis. J Clin Periodontol. 2019;46(3):354-62. doi: 10.1111/jcpe.13078.
  30. Romanos G, Grizas E, Nentwig GH. Association of keratinized mucosa and periimplant soft tissue stability around implants with platform switching. Implant Dent. 2015;24(4):422-6. doi: 10.1097/id.0000000000000274.
  31. Monje A, Blasi G. Significance of keratinized mucosa/gingiva on peri-implant and adjacent periodontal conditions in erratic maintenance compliers. J Periodontol. 2019;90(5):445-53. doi: 10.1002/jper.18-0471.
  32. Schrott AR, Jimenez M, Hwang JW, Fiorellini J, Weber HP. Five-year evaluation of the influence of keratinized mucosa on peri-implant soft-tissue health and stability around implants supporting full-arch mandibular fixed prostheses. Clin Oral Implants Res. 2009;20(10):1170-7. doi: 10.1111/j.1600-0501.2009.01795.x.
  33. Ueno D, Nagano T, Watanabe T, Shirakawa S, Yashima A, Gomi K. Effect of the keratinized mucosa width on the health status of periimplant and contralateral periodontal tissues: a cross-sectional study. Implant Dent. 2016;25(6):796-801. doi: 10.1097/id.0000000000000483.
  34. Grischke J, Karch A, Wenzlaff A, Foitzik MM, Stiesch M, Eberhard J. Keratinized mucosa width is associated with severity of peri-implant mucositis. A cross-sectional study. Clin Oral Implants Res. 2019;30(5):457-65. doi: 10.1111/clr.13432.
  35. Shokri Y, Variji A, Nosrati M, Khonakdar-Tarsi A, Kianmehr A, Kashi Z, et al. Importance of paraoxonase 1 (PON1) as an antioxidant and antiatherogenic enzyme in the cardiovascular complications of type 2 diabetes: genotypic and phenotypic evaluation. Diabetes Res Clin Pract. 2020;161:108067. doi: 10.1016/j.diabres.2020.108067.
  36. Astashina NB, Plyukhin DV, Sosnin DY, Mudrova OA. [Salivary level of lipid peroxidation products as a predictor of dental implantation complications]. Stomatologiia (Mosk). 2019;98(3):31-4. doi: 10.17116/stomat20199803131.[Russian].
  37. Tekin Koruk S, Aksoy N, Hamidanoglu M, Karsen H, Unlu S, Bilinc H. The activity of paraoxonase and arylesterase in patients with osteomyelitis. Scand J Clin Lab Invest. 2012;72(7):513-7. doi: 10.3109/00365513.2012.700058.
  38. Li Y, Zhai R, Li H, Mei X, Qiu G. Prognostic value of serum paraoxonase and arylesterase activity in patients with sepsis. J Int Med Res. 2013;41(3):681-7. doi: 10.1177/0300060513483412.