Abstract
Aim: This study aimed to assess the effects of smoking on systemic and local oxidative stress markers in patients with periodontitis.
Methods: A total of 72 patients with periodontitis [38 smokers (S +P+), 34 non-smokers (S-P+)] and 54 periodontally healthy individuals [28 smokers (S+P-), 26 non-smokers (S-P-, control)] were included. After clinical measurements and samplings, the cotinine level, total antioxidant capacity (TAOC), total oxidative status (TOS), and malondialdehyde (MDA) level in the serum and saliva were determined, and the oxidative stress index (OSI) was calculated. Kruskal-Wallis and Mann-Whitney U tests were used for multiple and pairwise comparisons. Correlations were analyzed using Pearson correlation coefficient. P<0.05 was considered statistically significant.
Results: Smoking and periodontitis decreased the serum and salivary TAOCs and increased the TOS, MDA level, and OSI. The smokers with periodontitis had the lowest TAOC and the highest TOS, MDA level, and OSI, while the controls had the highest TAOC and the lowest TOS, MDA level, and OSI. The systemic and local effects of smoking seemed more pronounced than those of periodontitis in the oxidative stress study, but no significant difference was identified between the smoking (S+P-) and periodontitis (S-P+) groups. The clinical parameters and oxidative stress markers showed both substantial positive and negative relationships in all groups (p<0.01).
Conclusions: It can be concluded that smoking and periodontitis (S+P+) are associated with a decrease in serum and salivary TAOCs and an increase in TOS, MDA levels, and OSI. Smoking has a similar effect as periodontitis on local and systemic oxidative stress, and oxidative stress caused by smoking may be a significant factor in the pathophysiology of periodontitis.
Keywords: Smoking, lipid peroxidation, oxidative stress, periodontitis
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Copyright © 1970 The Author(s). This is an open-access article published by Bolu İzzet Baysal Training and Research Hospital under the terms of the Creative Commons Attribution License (CC BY) which permits unrestricted use, distribution, and reproduction in any medium or format, provided the original work is properly cited.
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References
- Chapple IL, Matthews JB. The role of reactive oxygen and antioxidant species in periodontal tissue destruction. Periodontol 2000. 2007; 43: 160-232. https://doi.org/10.1111/j.1600-0757.2006.00178.x
- Waddington RJ, Moseley R, Embery G. Reactive oxygen species: a potential role in the pathogenesis of periodontal diseases. Oral Dis. 2000; 6(3): 138-51. https://doi.org/10.1111/j.1601-0825.2000.tb00325.x
- Baltacıoğlu E, Kehribar MA, Yuva P, et al. Total oxidant status and bone resorption biomarkers in serum and gingival crevicular fluid of patients with periodontitis. J Periodontol. 2014; 85(2): 317-26. https://doi.org/10.1902/jop.2013.130012
- 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(11): 1241-6. https://doi.org/10.1177/0022034510375830
- Chen M, Cai W, Zhao S, et al. Oxidative stress-related biomarkers in saliva and gingival crevicular fluid associated with chronic periodontitis: A systematic review and meta-analysis. J Clin Periodontol. 2019; 46(6): 608-22. https://doi.org/10.1111/jcpe.13112
- Van Dyke TE, Sheilesh D. Risk factors for periodontitis. J Int Acad Periodontol. 2005; 7(1): 3-7.
- Toczewska J, Maciejczyk M, Konopka T, Zalewska A. Total oxidant and antioxidant capacity of gingival crevicular fluid and saliva in patients with periodontitis: review and clinical study. Antioxidants (Basel). 2020; 9(5): 450. https://doi.org/10.3390/antiox9050450
- Chapple IL, Milward MR, Dietrich T. The prevalence of inflammatory periodontitis is negatively associated with serum antioxidant concentrations. J Nutr. 2007; 137(3): 657-64. https://doi.org/10.1093/jn/137.3.657
- Baltacıoğlu E, Yuva P, Aydın G, 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. https://doi.org/10.1902/jop.2014.130654
- Guentsch A, Preshaw PM, Bremer-Streck S, Klinger G, Glockmann E, Sigusch BW. Lipid peroxidation and antioxidant activity in saliva of periodontitis patients: effect of smoking and periodontal treatment. Clin Oral Investig. 2008; 12(4): 345-52. https://doi.org/10.1007/s00784-008-0202-z
- Buduneli N, Kardeşler L, Işık H, et al. Effects of smoking and gingival inflammation on salivary antioxidant capacity. J Clin Periodontol. 2006; 33(3): 159-64. https://doi.org/10.1111/j.1600-051X.2006.00892.x
- Johnson GK, Guthmiller JM. The impact of cigarette smoking on periodontal disease and treatment. Periodontol 2000. 2007; 44: 178-94. https://doi.org/10.1111/j.1600-0757.2007.00212.x
- Tonguç MÖ, Öztürk O, Sütçü R, et al. The impact of smoking status on antioxidant enzyme activity and malondialdehyde levels in chronic periodontitis. J Periodontol. 2011; 82(9): 1320-8. https://doi.org/10.1902/jop.2011.100618
- Chen X, Wolff L, Aeppli D, et al. Cigarette smoking, salivary/gingival crevicular fluid cotinine and periodontal status. A 10-year longitudinal study. J Clin Periodontol. 2001; 28(4): 331-9. https://doi.org/10.1034/j.1600-051x.2001.028004331.x
- Sato J, Takahashi I, Umeda T, et al. Effect of alcohol drinking and cigarette smoking on neutrophil functions in adults. Luminescence. 2011; 26(6): 557-64. https://doi.org/10.1002/bio.1270
- Matthews JB, Chen FM, Milward MR, et al. Effect of nicotine, cotinine and cigarette smoke extract on the neutrophil respiratory burst. J Clin Periodontol. 2011; 38(3): 208-18. https://doi.org/10.1111/j.1600-051X.2010.01676.x
- Yamamoto Y, Nishida N, Tanaka M, et al. Association between passive and active smoking evaluated by salivary cotinine and periodontitis. J Clin Periodontol. 2005; 32(10): 1041-6. https://doi.org/10.1111/j.1600-051X.2005.00819.x
- Istvan JA, Nides MA, Buist AS, Greene P, Voelker H. Salivary cotinine, frequency of cigarette smoking, and body mass index: findings at baseline in the Lung Health Study. Am J Epidemiol. 1994; 139(6): 628-36. https://doi.org/10.1093/oxfordjournals.aje.a117052
- Erel O. A novel automated method to measure total antioxidant response against potent free radical reactions. Clin Biochem. 2004; 37(2): 112-9. https://doi.org/10.1016/j.clinbiochem.2003.10.014
- Erel O. A new automated colorimetric method for measuring total oxidant status. Clin Biochem. 2005; 38(12): 1103-11. https://doi.org/10.1016/j.clinbiochem.2005.08.008
- Young IS, Trimble ER. Measurement of malondialdehyde in plasma by high performance liquid chromatography with fluorimetric detection. Ann Clin Biochem. 1991; 28 (Pt 5): 504-8. https://doi.org/10.1177/000456329102800514
- Cohen J. Statistical power analysis. Current Directions in Psychological Science. 1992; 1(3): 98-101. https://doi.org/10.1111/1467-8721.ep10768783
- Erdemir EO, Duran I, Haliloglu S. Effects of smoking on clinical parameters and the gingival crevicular fluid levels of IL-6 and TNF-alpha in patients with chronic periodontitis. J Clin Periodontol. 2004; 31(2): 99-104. https://doi.org/10.1111/j.0303-6979.2004.00454.x
- Caton JG, Armitage G, Berglundh T, et al. A new classification scheme for periodontal and peri-implant diseases and conditions - Introduction and key changes from the 1999 classification. J Clin Periodontol. 2018; 45(Suppl 20): S1-8. https://doi.org/10.1111/jcpe.12935
- Machacek DA, Jiang NS. Quantification of cotinine in plasma and saliva by liquid chromatography. Clin Chem. 1986; 32(6): 979-82.
- Agnihotri R, Pandurang P, Kamath SU, et al. Association of cigarette smoking with superoxide dismutase enzyme levels in subjects with chronic periodontitis. J Periodontol. 2009; 80(4): 657-62. https://doi.org/10.1902/jop.2009.080545
- Zappacosta B, Persichilli S, De Sole P, Mordente A, Giardina B. Effect of smoking one cigarette on antioxidant metabolites in the saliva of healthy smokers. Arch Oral Biol. 1999; 44(6): 485-8. https://doi.org/10.1016/s0003-9969(99)00025-4
- Noh JW, Jang JH, Yoon HS, et al. Evaluation of Salivary Biomarkers of Periodontal Disease Based on Smoking Status: A Systematic Review. Int J Environ Res Public Health. 2022; 19(21): 14619. https://doi.org/10.3390/ijerph192114619
- Canakci CF, Cicek Y, Yildirim A, Sezer U, Canakci V. Increased levels of 8-hydroxydeoxyguanosine and malondialdehyde and its relationship with antioxidant enzymes in saliva of periodontitis patients. Eur J Dent. 2009; 3(2): 100-6.
- Trivedi S, Lal N, Mahdi AA, Mittal M, Singh B, Pandey S. Evaluation of antioxidant enzymes activity and malondialdehyde levels in patients with chronic periodontitis and diabetes mellitus. J Periodontol. 2014; 85(5): 713-20. https://doi.org/10.1902/jop.2013.130066
- Wei D, Zhang XL, Wang YZ, Yang CX, 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. Aust Dent J. 2010; 55(1): 70-8. https://doi.org/10.1111/j.1834-7819.2009.01123.x
- Akalın FA, Baltacıoğlu E, Alver A, Karabulut E. Total antioxidant capacity and superoxide dismutase activity levels in serum and gingival crevicular fluid in pregnant women with chronic periodontitis. J Periodontol. 2009; 80(3): 457-67. https://doi.org/10.1902/jop.2009.080218
- Panjamurthy K, Manoharan S, Ramachandran CR. Lipid peroxidation and antioxidant status in patients with periodontitis. Cell Mol Biol Lett. 2005; 10(2): 255-64.
- Akalın FA, Baltacıoğlu 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(7): 558-65. https://doi.org/10.1111/j.1600-051X.2007.01091.x
- Tsai CC, Chen HS, Chen SL, et al. Lipid peroxidation: a possible role in the induction and progression of chronic periodontitis. J Periodontal Res. 2005; 40(5): 378-84. https://doi.org/10.1111/j.1600-0765.2005.00818.x
- Su H, Gornitsky M, Velly AM, Yu H, Benarroch M, Schipper HM. Salivary DNA, lipid, and protein oxidation in nonsmokers with periodontal disease. Free Radic Biol Med. 2009; 46(7): 914-21. https://doi.org/10.1016/j.freeradbiomed.2009.01.008
- Celec P, Hodosy J, Celecová V, et al. Salivary thiobarbituric acid reacting substances and malondialdehyde-their relationship to reported smoking and to parodontal status described by the papillary bleeding index. Dis Markers. 2005; 21(3): 133-7. https://doi.org/10.1155/2005/693437
- Marton IJ, Balla G, Hegedus C, et al. The role of reactive oxygen intermediates in the pathogenesis of chronic apical periodontitis. Oral Microbiol Immunol. 1993; 8(4): 254-7. https://doi.org/10.1111/j.1399-302x.1993.tb00570.x
- Mashayekhi F, Aghahoseini F, Rezaie A, Zamani MJ, Khorasani R, Abdollahi M. Alteration of cyclic nucleotides levels and oxidative stress in saliva of human subjects with periodontitis. J Contemp Dent Pract. 2005; 6(4): 46-53.
- Sobaniec H, Sobaniec-Lotowska ME. Morphological examinations of hard tissues of periodontium and evaluation of selected processes of lipid peroxidation in blood serum of rats in the course of experimental periodontitis. Med Sci Monit. 2000; 6(5): 875-81.
- Sheikhi M, Bouhafs RK, Hammarström KJ, Jarstrand C. Lipid peroxidation caused by oxygen radicals from Fusobacterium-stimulated neutrophils as a possible model for the emergence of periodontitis. Oral Dis. 2001; 7(1): 41-6.
- Tüter G, Kurtiş B, Serdar M. Interleukin-1beta and thiobarbituric acid reactive substance (TBARS) levels after phase I periodontal therapy in patients with chronic periodontitis. J Periodontol. 2001; 72(7): 883-8. https://doi.org/10.1902/jop.2001.72.7.883
- Hendek MK, Erdemir EO, Kisa U, Ozcan G. Effect of initial periodontal therapy on oxidative stress markers in gingival crevicular fluid, saliva, and serum in smokers and non-smokers with chronic periodontitis. J Periodontol. 2015; 86(2): 273-82. https://doi.org/10.1902/jop.2014.140338
- Lütfioğlu M, Sakallıoğlu U, Sakallıoğlu EE, Özden FO, Ürkmez SS, Bilgici B. Effects of smoking on the gingival crevicular fluid levels of interleukin-17A, interleukin-17E, and oxidative stress following periodontal treatment process. J Periodontal Res. 2021; 56(2): 388-96. https://doi.org/10.1111/jre.12831