Abstract
Periodontitis is bacterial infection characterized by persistent inflammation, damages connective tissue and alveolar bone destruction. The present study performed to investigate that the salivary levels could be associated with progression of periodontitis so that they used as biological markers of this disease. In this study, Twenty-nine periodontitis patients were recruited from periodontology service. Control groups are consisting of twenty-eight subjects. Total antioxidant capacity (TAC), catalase activity (CAT), reduced glutathione (GSH), uric acid, malondialdehyde (MDA) and carbonyl proteins (CP), as well as inflammatory TNF-α, IL-1β, and immune IgA biomarkers were measured in saliva. Our results revealed that salivary MDA and carbonyls levels were significantly greater (P < 0.001), while TAC, GSH and uric acid were attenuated in periodontitis patients as compared to controls (P < 0.001). Moreover, high TNF-α, Il1-β and IgA levels (P < 0.001) were observed. Positive and significant correlations were noticed between probing pocket depth (PPD), clinical attachment level (CAL) and gingival index (GI) and assessed biomarkers. Whereas, negative correlations were observed between TAC, CAT and GSH and clinical assessments. Therefore, MDA and CP were positive and significantly correlated with TNF-α, Il1-β. In conclusion, our results show positive association between oxidative stress and pro-inflammatory cytokines, which are major modulators of the inflammatory response in stage III and grade C periodontitis. Moreover, these salivary biomarkers could be utilized as a major asset for early diagnosis and their relation with severe periodontitis.
Similar content being viewed by others
Abbreviations
- CAL:
-
Clinical Attachment Level
- CAT:
-
Catalase activity
- CP:
-
Carbonyl Proteins
- GSH:
-
Reduced Glutathione
- IgA:
-
Immunoglobulin A
- IL-1β:
-
Interleukin-1β
- MDA:
-
Malondialdehyde
- NADPH:
-
Nicotinamide Adenine Dinucleotide Phosphate
- NF-κB:
-
Nuclear Factor kappa B
- PMN:
-
Polymorph Nuclear Leukocytes
- PPD:
-
Probing Pocket Depth
- ROS:
-
reactive oxygen species
- TAC`:
-
Total Antioxidant Capacity
- TNF-α:
-
Tumor necrosis factor-α
References
Ahmadi-motamayel F, Goodarzi MT, Jamshidi Z, Kebriaei R (2017) Evaluation of salivary and serum antioxidant and oxidative stress status in patients with chronic periodontitis: a case-control study. Front Physiol 8:189. https://doi.org/10.3389/fphys.2017.00189
Altinkaynak K, Varoglu AO, Aksoy H, Deniz O, Aksoy (2009) Serum uric acid levels in patients with relapsing-remitting multiple sclerosis. Eur J Gen Med 6:166–169. https://doi.org/10.29333/ejgm/82663
Baltacioğlu E, Yuva P, Aydin G, Alver A, Kahraman C, Karabulut E, Akalın FA (2014) 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 85:1432–1441. https://doi.org/10.1902/jop.2014.130654
Baser U, Gamsiz-isik H, Cifcibasi E, Ademoglu E, Yalcin F (2015) Plasma and salivary total antioxidant capacity in healthy controls compared with aggressive and chronic periodontitis patients. Saudi Med J 36:856–861. https://doi.org/10.15537/smj.2015.7.11954
Blaser H, Dostert C, Mak TW, Brenner D (2016) TNF and ROS crosstalk in inflammation. Trends Cell Biol 26:249–261. https://doi.org/10.1016/j.tcb.2015.12.002
Borges IJR, Moreira EA, Filho DW, de Oliveira TB, da Silva MBS, Fröde TS (2007) Pro inflammatory and oxidative stress markers in patients with periodontal disease. Mediat Inflamm 2007:45794. https://doi.org/10.1155/2007/45794
Branco-de-almeida ACM, Lopes FF, Vasconcelos Pereira AF (2011) Salivary IgA and periodontal treatment needs in diabetic patients. Braz Oral Res 25:550–555. https://doi.org/10.1590/S1806-83242011000600013
Brandtzaeg P (2013) Secretory immunity with special reference to the oral cavity. J Oral Microbiol 5:340. https://doi.org/10.3402/jom.v5i0.20401
Bullon P, Newman HN, Battino M (2014) Obesity, diabetes mellitus, atherosclerosis and chronic periodontitis: a shared pathology via oxidative stress and mitochondrial dysfunction? Periodontol 2000 64:139–153. https://doi.org/10.1111/j.1600-0757.2012.00455.x
Cheng R, Wu Z, Li M, Shao M, Hu T (2020) Interleukin-1β is a potential therapeutic target for periodontitis: a narrative review. Int J Oral Sci 12:2. https://doi.org/10.1038/s41368-019-0068-8
Chengcheng L, Longyi M, Yulong N, Xin L, Xuedong Z, Xin X (2017) The role of reactive oxygen species and autophagy in periodontitis and their potential linkage. Front Physiol 8:439. https://doi.org/10.3389/fphys.2017.00439
De lima CL, Acevedo AC, Grisi DC, MJr T, Guerra E, De Luca Canto G (2016) Host-derived salivary biomarkers in diagnosing periodontal disease: systematic review and meta- analysis. J Clin Periodontol 43:492–502. https://doi.org/10.1111/jcpe.12538
Ebersole JL, Nagarajan R, Akers D, Mille CS (2015) Targeted salivary biomarkers for discrimination of periodontal health and disease(s). Front Cell Infect Microbiol 5:62. https://doi.org/10.3389/fcimb.2015.00062
Giannopoulou C, Krause K-H, Müller F (2008) The NADPH oxidase NOX2 plays a role in periodontal pathologies. Semin Immunopathol 30:273–278. https://doi.org/10.1007/s00281−008-0128-1
Gomes FIF, Aragão MG, Barbosa FC, Bezerra MM, de Paulo Teixeira Pinto V, Chaves HV (2016) Inflammatory cytokines interleukin-1β and tumour necrosis factor-α-novel biomarkers for the detection of periodontal diseases: a literature review. J Oral Maxillofac Res 7:e2. https://doi.org/10.5037/jomr.2016.7202
Hadwan MH, Abed HN (2015) Data supporting the spectrophotometric method for the estimation of catalase activity. Data Brief 6:194–199. https://doi.org/10.1016/j.dib.2015.12.012
Jaedicke KM, Presshaw PM, Taylor RJ (2016) Salivary cytokines as biomarkers of periodontal diseases. Periodontol 2000 70:164–183. https://doi.org/10.1111/prd.12117
Kerboua KE, Haiba F, Boumediene A (2015) The plasmatic oxygen radical antioxidant capacity (ORAC) index but not the neutrophil enzyme Lcn2 level may predict high levels of serum malondialdehyde in male idiopathic infertility. Ann Biol Res 6:16–24
Kundalić J, Pavlović D, Jevtović-stoimenov T, Obradović R, Kesić L, Kundalić B, Stošić N (2016) Oxidative stress in the pathogenesis of periodontal disease. Acta Medica Medianae 55:66–72. https://doi.org/10.5633/AMM.2016.0409
Levine RL, Garlan D, Oliver CN, Amici A, Climent I, Lenz AG, Ahn BW, Shaltiel S, Stadtman ER (1990) Determination of carbonyl content in oxidativelymodified proteins. Methods Enzymol 186:464–478. https://doi.org/10.1016/0076-6879(90)86141-H
Lingappan K (2018) NF-κB in oxidative stress. Curr Opin Toxicol 7:81–86. https://doi.org/10.1016/j.cotox.2017.11.002
Liu T, Zhang L, Joo D, Sun SC (2017) NF-κB signaling in inflammation. Signal Transduct Target Ther 2:17023. https://doi.org/10.1038/sigtrans.2017.23
Marcotte H, Lavoie MC (1998) Oral microbial ecology and the role of salivary immunoglobulin a. Microbiol Mol Biol Rev 62:71–109
Mashayekhi F, Aghahoseini F, Rezaie A, Zamani MJ, Khorasani R, Abdollahi M (2005) Alteration of cyclic nucleotides levels and oxidative stress in saliva of human subjects with periodontitis. J Contemp Dent Pract 6:46–53
Mathur A, Mathur L, Manohar B, Mathur H, Shankarapillai R, Shetty N, Bhatia A (2013) Antioxidant therapy as monotherapy or as an adjunct to treatment of periodontal diseases. J Indian Soc Periodontol 17:21–24. https://doi.org/10.5005/jcdp-6-4-46
Meyle J, Chapple I (2015) Molecular aspects of the pathogenesis of periodontitis. Periodontol 2000 69:7–17. https://doi.org/10.1111/prd.12104
Miricescu D, Totan A, Calenic B, Mocanu B, Didilescu A, Mohora M et al (2014) Salivary biomarkers: relationship between oxidative stress and alveolar bone loss in chronic periodontitis. Acta Odontol Scand 72:42–47. https://doi.org/10.3109/00016357.2013.795659
Morgan MJ, Liu ZG (2011) Crosstalk of reactive oxygen species and NF-kappaB signaling. Cell Res 21:103–115. https://doi.org/10.1038/cr.2010.178
Navazesh Mahvash (1993) Methods for Collecting Saliva. Annals of the New York Academy of Sciences 694(1 Saliva as a D):72–77
Pfaffe T, Cooper-White J, Beyerlein P, Kostner K, Punyadeera C (2011) Diagnostic potential of saliva: current state and future applications. Clin Chem 57:675–687. https://doi.org/10.1373/clinchem.2010.153767
Pradeep A, Ramchandraprasad M, Bajaj P, Rao NS, Agarwal E (2013) Protein carbonyl: an oxidative stress marker in gingival crevicular fluid in healthy, gingivitis, and chronic periodontitis subjects. Contemp Clin Dent 4:27–31. https://doi.org/10.4103/0976-237X.111589
Sato M, Nagata A, Maehara R, Endo J, Hinode D (1987) Salivary IgA antibody to bacteroides gingivalis and Actinobacillus actinomycetemcomitans in patients with adult marginal periodontitis. J Dent Health 37:244–249. https://doi.org/10.5834/jdh.37.244
Sczepanik FSC, Grossi ML, Casati M, Goldberg M, Glogaue M, Fine N, Tenenbaum HC (2020) Periodontitis is an inflammatory disease of oxidative stress: we should treat it that way. Periodontol 2000 84:45–68. https://doi.org/10.1111/prd.12342
Silva N, Dutzan N, Hernandez M, Dezerega A, Rivera O, Aguillon JC et al (2008) Characterization of progressive periodontal lesions in chronic periodontitis patients: levels of chemokines, cytokines, matrix metalloproteinase-13, periodontalpathogens and inflammatory cells. J Clin Periodontol 35:206–214. https://doi.org/10.1111/j.1600-051X.2007.01190.x
Srinivasan PC (2012) Immunoglobulin levels and periodontal diseases- a clinical immunological study. Open Access Sci Rep 1:254. https://doi.org/10.4172/scientificreports.254
Toczewska J, Maciejczyk M, Konopka T, Zalewska A (2020) Total oxidant and antioxidant capacity of gingival Crevicular fluid and saliva in patients with periodontitis: review and clinical study. Antioxidants 9:450. https://doi.org/10.3390/antiox9050450
Tonetti MS, Greenwell H, Kornman KS (2018) Staging and grading of periodontitis: framework and proposal of a new classification and case definition. J Clin Periodontol 89:S149–S161. https://doi.org/10.1002/JPER.18-0006
Torumtay G, Kirzioğlu FY, Öztürktonguç M, Kale B, Calapoğlu M, Orhan H (2016) Effects of periodontal treatment on inflammation and oxidative stress markers in patients with metabolic syndrome. J Periodontal Res 51:489–498. https://doi.org/10.1111/jre.12328
Tóthová L, Kamodyová N, Červenka T, Celec P (2015) Salivary markers of oxidative stress in oral diseases. Front Cell Infect Microbiol 5:73. https://doi.org/10.3389/fcimb.2015.00073
Tsai CC, Chen HS, Chen SL, Ho YP, Ho KY, Wu YM, Hung CC (2005) Lipid peroxidation: a possible role in the induction and progression of chronic periodontitis. J Periodontal Res 40:378–384. https://doi.org/10.1111/j.1600-0765.2005.00818.x
Varghese SS, Thomas H, Jayakumar ND, Sankari M, Lakshmanan R (2015) Estimation of salivary tumor necrosis factor-alpha in chronic and aggressive periodontitis patients. Contemp Clin Dent 6:S152–SS56. https://doi.org/10.4103/0976-237X.166816
Weckbecker G, Cory JG (1988) Ribonucleotide reductase activity and growth of glutathione- depleted mouse leukemia L1210 cells in vitro. Cancer Lett 40:257–264. https://doi.org/10.1016/0304-3835(88)90084-5
Yagi K (1976) A simple fluorometric assay for lipoperoxide in blood plasma. Biochem Med 15:212–216. https://doi.org/10.1016/0006-2944(76)90049-1
Zhang T, Andrukhov O, Haririan H, Müller-Kern M, Liu S, Liu Z, Rausch-Fan X (2016) Total antioxidant capacity and total oxidant status in saliva of periodontitis patients in relation to bacterial load. Front Cell Infect Microbiol 5:97. https://doi.org/10.3389/fcimb.2015.00097
Acknowledgments
We thank Dr. Benmahdi Lahcen, a head of department in central laboratory HMRUO, Algeria for having accepted me in his laboratory.
Funding
This work was supported by research laboratory of the University of Oran 1: Oral biology laboratory (Code W0900100).
Author information
Authors and Affiliations
Contributions
All authors declare that they have intellectually participated in this work and are solely responsible for its results.
Corresponding author
Ethics declarations
Ethics approval and consent to participate
The Ethics Committee of Research, Faculty of Medicine University of Oran1, approved this study. Information of consent and assent was received from each patient.
Conflict of interest
The authors have no conflict of interest to declare.
Additional information
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Senouci, S., Ait Yahia, D., Bouziane, D. et al. The diagnostic role of salivary biomarkers of oxidative stress and inflammatory status and their relationship in periodontitis stage III and grade C. Biologia 76, 1617–1625 (2021). https://doi.org/10.1007/s11756-021-00714-z
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11756-021-00714-z