Oxidative Stress Markers Analysis in Sites with Healthy Conditions and with Periodontal and Peri-Implant Diseases

Guarnieri, Renzo; Reda, Rodolfo; Zanza, Alessio; Bramucci, Chiara; Testarelli, Luca; Di Nardo, Dario

doi:10.15517/9g5pw090

Authors

Renzo Guarnieri Private Practice, Treviso, Italy. Author https://orcid.org/0000-0003-1449-8340
Rodolfo Reda Fondazione Policlinico Universitario Campus Bio-Medico, Rome, Italy. Author https://orcid.org/0000-0003-1532-6524
Alessio Zanza Fondazione Policlinico Universitario Campus Bio-Medico, Rome, Italy. Author https://orcid.org/0000-0002-2062-8140
Chiara Bramucci Fondazione Policlinico Universitario Campus Bio-Medico, Rome, Italy. Author https://orcid.org/0009-0008-3270-9301
Luca Testarelli Department of Oral and Maxillo-Facial Sciences, Sapienza Univerisity of Rome, Italy. Author https://orcid.org/0000-0003-3904-3000
Dario Di Nardo Department of Oral and Maxillo-Facial Science, Sapienza University of Rome, Italy. Author https://orcid.org/0000-0002-5054-0828

DOI:

https://doi.org/10.15517/9g5pw090

Keywords:

Perimplantitis; Periodontitis; Oxidative stress markers.

Abstract

To evaluate the gingival crevicular fluid (GCF) and the peri- implant crevicular fluid (PICF) concentration of oxidative stress markers, such as malondialdehyde (MDA) and superoxide dismutase (SOD) in healthy sites and in those affected by periodontitis (PER) and peri-implantitis (PIM). Sites in periodontal (PH) and peri-implant (PIH) healthy conditions and sites with PER and PIM were investigated in 120 subjects. Clinical parameters including plaque index (PI), gingival index (GI), probing pocket depth (PPD), and bleeding on probing (BOP) were recorded. Levels of MDA and SOD in GCF and PICF were determined using commercially available enzyme-linked immunosorbent assay (ELISA) kits and statistically correlated with PI, GI PPD and BOP. No statistically significant differences (p>0.05) in level of MDA and SOD were found in PH vs. PIH sites with. Compared to PH sites, PER sites presented a higher level of MDA and SOD, but the difference was not statistically significant (p>0.05). Statistically significant higher concentrations of MDA (p=0.009) and SOD (p= 0.004) were found in PIM sites compared to PIH. Moreover, PIM sites showed also statistically higher levels of MDA (p=0.012) and SOD (p=0.013) than PER sites. MDA and SOD concentrations were found positively correlated with PD and BOP. The measured oxidative stress markers were statistically higher in diseased peri-implant sites than in diseased periodontal sites.

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References

Berglundh T., Armitage G., Araujo M.G., Avila-Ortiz G., Blanco J., Camargo P.M., 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 Clin Periodontol. 2018; 45 Suppl 20: S286-91.

Heitz-Mayfield L.J. Peri-implant diseases: diagnosis and risk indicators. J Clin Periodontol. 2008; 35 (8 Suppl): 292-304.

Lang N.P., Berglundh T. Periimplant diseases: where are we now?--Consensus of the Seventh European Workshop on Periodontology. J Clin Periodontol. 2011; 38 Suppl 11: 178-81.

Guarnieri R., Testarelli L., Galindo-Moreno P., Del Fabbro M., Testori T. Current Emerging Concepts on the Pathogenesis of Periimplant Diseases: A Narrative Review. Int J Oral Maxillofac Implants. 2024 Oct 16; 39 (5): 674-683.

Carcuac O., Berglundh T. Composition of human peri-implantitis and periodontitis lesions. J Dent Res. 2014 Nov; 93 (11): 1083-8.

Galárraga-Vinueza M.E., Tangl S., Bianchini M., Magini R., Obreja K., Gruber R., Schwarz F. Histological characteristics of advanced peri-implantitis bone defects in humans. Int J Implant Dent. 2020 Mar 25; 6 (1): 12.

Maruyama N., Maruyama F., Takeuchi Y., Aikawa C., Izumi Y., Nakagawa I. Intraindividual variation in core microbiota in peri-implantitis and periodontitis. Sci Rep. 2014; 4: 6602.

Venza I., Visalli M., Cucinotta M., De Grazia G., Teti D., Venza M. Proinflammatory gene expression at chronic periodontitis and peri-implantitis sites in patients with or without type 2 diabetes. J Periodontol. 2010; 81: 99-108.

Becker S.T., Beck-Broichsitter B.E., Graetz C., Dörfer C.E., Wiltfang J., Häsler R. Peri-implantitis versus periodontitis: functional differences indicated by transcriptome profiling. Clin Implant Dent Relat Res. 2014 Jun;16 (3): 401-11.

Galarraga-Vinueza M.E., Obreja K., Ramanauskaite A, Magini R, Begic A, Sader R., Schwarz F. Macrophage polarization in peri-implantitis lesions. Clin Oral Investig. 2021 Apr; 25 (4): 2335-2344.

Emecen-Huja P., Eubank T.D., Shapiro V., Yildiz V., Tatakis D.N., Leblebicioglu B. Peri-implant versus periodontal wound healing. J Clin Periodontol. 2013; 40: 816-824.

Mittal, M., Siddiqui, M. R., Tran, K., Reddy, S. P., and Malik, A. B. (2014). Reactive oxygen species in inflammation and tissue injury. Antioxid. Redox Sig 2014; 20, 1126-1167.

Tóthová L., Kamodyová N., Červenka T., Celec P. Salivary markers of oxidative stress in oral diseases. Front Cell Infect Microbiol. 2015 Oct 20; 5: 73.

Buczko P., Zalewska A., Szarmach I. Saliva and oxidative stress in oral cavity and in some systemic disorders. J Physiol Pharmacol. 2015 Feb; 66 (1): 3-9. PMID: 25716960.

Chen M., Cai W., Zhao S., Shi L., Chen Y., Li X., Sun X., Mao Y., He B., Hou Y., Zhou Y., Zhou Q., Ma J., Huang S. Oxidative stress-related biomarkers in saliva and gingival crevicular fluid associated with chronic periodontitis: A systematic review and meta-analysis. J Clin Periodontol. 2019 Jun; 46 (6): 608-622.

Wang J., Hu C., Ma X., Zhang Y., Zhang X., Hong X., Chen L., Wang Y., Wang J., Chen S., Zhang Q., Wu Y., Wu M., Chen Y., Song Z., Sun X., Zhao S., Huang S. The role of oxidative stress biomarkers in the development of peri-implant disease: A systematic review and meta-analysis. J Dent. 2024 Jul; 146: 105026.

Halliwell B., Gutteridge J.M.C. Free radicals in biology and medicine Oxford university press, Oxford, UK: 198: 96-98.

Chapple I.L.C., Matthews J.B. The role of reactive oxygen and antioxidant species in periodontal tissue destruction. Periodontol 2000 2007; 43: 160-232.

Akalin F.A., Baltaciog!lu 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: 558-565.

Waddington R.J., Moseley R., Embery G. Reactive oxygen species: A potential role in the pathogenesis of periodontal diseases. Oral Dis 2000; 6: 138-151.

Halliwell, B.; Gutteridge, J.M. The definition and measurement of antioxidants in biological systems. Free Radic. Biol. Med. 1995, 18, 125-126.

Binder C.J., Papac-Milicevic N., Witztum J.L. Innate sensing of oxidation-specific epitopes in health and disease. Nat Rev Immunol. (2016) 8: 485-97.

Kimura, S.; Yonemura, T.; Kaya, H. Increased oxidative product formation by peripheral blood polymorphonuclear leukocytes in human periodontal diseases. J. Periodontal. Res. 1993, 28: 197-203.

Mijiritsky E., Ferroni L., Gardin C., Peleg O., Gultekin A., Saglanmak A., Delogu L.G., Mitrecic D., Piattelli A., Tatullo M., Zavan B. Presence of ROS in Inflammatory Environment of Peri-Implantitis Tissue: In Vitro and In Vivo Human Evidence. J Clin Med. 2019 Dec 23; 9 (1): 38.

Mittal M., Siddiqui M.R., Tran K., Reddy S.P., Malik A.B. Reactive oxygen species in inflammation and tissue injury. Antioxid Redox Signal. 2014; 20 (7): 1126-67.

Kinane D.F., Preshaw P.M., Loos B.G., Working Group 2 of 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. J Clin Periodontol. 2011; 38 Suppl 11: 44-8.

Kimura, S.; Yonemura, T.; Kaya, H. Increased oxidative product formation by peripheral blood polymorphonuclear leukocytes in human periodontal diseases. J. Periodontal. Res. 1993, 28: 197-203.

Tóthová, L.; Celec, P. Oxidative Stress and Antioxidants in the Diagnosis and Therapy of Periodontitis. Front. Physiol. 2017, 8: 1055.

Del Rio D., Serafini M., Pellegrini N. Selected methodologies to assess oxidative ⁄ antioxidant status in vivo: a critical review. Nutr Metab Cardiovasc Dis. 2002 Dec; 12 (6): 343-51.

Del Rio D., Stewart A.J., Pellegrini N. A review of recent studies on malondialdehyde as toxic molecule and biological marker of oxidative stress. Nutr Metab Cardiovasc Dis. 2005 Aug; 15 (4): 316-28.

Halliwell B. Reactive oxygen species in living systems: source, biochemistry, and role in human disease. Am J Med. 1991 Sep 30; 91 (3C): 14S-22S.

Esterbauer H., Cheeseman K.H. Determination of aldehydic lipid peroxidation products: malonaldehyde and 4- hydroxynonenal. Methods Enzymol. 1990; 186: 407-21.

Paoletti F., Mocali A. Determination of superoxide dismutase activity by purely chemical system based on NAD(P)H oxidation. Methods Enzymol. 1990; 186: 209-20.

Guentsch A., Preshaw P.M., Bremer-Streck S., Klinger G., Glockmann E., Sigusch B.W. Lipid peroxidation and antioxidant activity in saliva of periodontitis patients: effect of smoking and periodontal treatment. Clin Oral Investig. 2008; 12 (4): 345-352.

Anwar S., Sarwar T., Khan A.A., Rahmani A.H. Therapeutic Applications and Mechanisms of Superoxide Dismutase (SOD) in Different Pathogenesis. Biomolecules. 2025 Aug 5;15 (8): 1130.

Ertugrul, A. S., Sahin, H., Dikilitas, A., Alpaslan, N., & Bozoglan, A. Comparison of CCL28, interleukin-8, interleukin-1ß and tumor ne- crosis factor-alpha in subjects with gingivitis, chronic periodonti- tis and generalized aggressive periodontitis. J Periodon Res 2013; 48: 44-51.

Nowzari, H., Botero, J. E., DeGiacomo, M., Villacres, M. C., & Rich, S. K. Microbiology and cytokine levels around healthy dental implants and teeth. Clin Impl Dent and Rel Res 2008; 10 (3): 166-173.

Emecen-Huja, P., Eubank, T. D., Shapiro, V., Yildiz, V., Tatakis, D. N., & Leblebicioglu, B. Peri-implant versus periodontal wound healing. J Clin Periodont 2013; 40 (8): 816-824.

Shee, F.; Pralhad, S.; Natarajan, S.; Manaktala, N.; Arun, S.; Marathe, A. Cellular and biochemical changes in different categories of periodontitis: A patient-based study. J. Int. Soc. Prev. Community Dent. 2020, 10: 341-349.

Baltacıoglu, E.; Yuva, P.; Aydin, G.; Alver, A.; Kahraman, C.; Karabulut, E.; Akalın, F.A. 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: 1432-1441.

Akaln, F.A.; Baltaoglu, 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: 558-565.

Tsai, C.C.; Chen, H.S.; Chen, S.L.; Ho, Y.P.; Ho, K.Y.; Wu, Y.M.; Hung, C.C. Lipid peroxidation: A possible role in the induction and progression of chronic periodontitis. J. Periodontal Res. 2005, 40: 378-384.

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. Aust. Dent. J. 2010, 55: 70-78.

Tonguç M.Ö., 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: 1320-8.

Özkan Karasu Y., Maden O., Çanakçı C.F. Oxidative damage biomarkers and antioxidant enzymes in saliva of patients with peri-implant diseases. Int J Implant Dent. 2024 Oct 14; 10 (1): 43.

Palsson-McDermott E.M., Curtis A.M., Goel G., Lauterbach M.A., Sheedy F.J., Gleeson L.E., et al. Pyruvate kinase M2 regulates Hif-1a activity and IL-1b induction and is a critical determinant of the warburg effect in LPS-activated macrophages. Cell Metab. (2015) 21: 65-80. doi: 10.1016/j.cmet.2014.12.005

Gordon S., Mantovani A. Diversity and plasticity of mononuclear phagocytes. Eur J Immunol. (2011) 41: 2470-2. doi: 10.1002/eji.201141988

Manoharan R.R., Prasad A., Pospíšil P., Kzhyshkowska J. ROS signaling in innate immunity via oxidative protein modifications. Front Immunol. 2024 Mar 7; 15: 1359600.

Ning Y., Li W., Zou L., Shen H., Su Z. Hypoxia-inducible Factor 1α Contributes to Matrix Metalloproteinases 2/9 and Inflammatory Responses in Periodontitis. Cell Biochem Biophys. 2025 Mar; 83 (1): 1159-1166. doi: 10.1007/s12013-024-01550-z. Epub 2024 Sep 28.

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 Feb; 18 (1): 27-33.

Mousavi Jazi M., Sadeghi Pour Rodsari H.R., Mirmiran F. Level of Oxidative Stress Markers in Peri-Implant Crevicular Fluid and Their Correlation with Clinical Parameters. J Dent (Tehran). 2015 May; 12 (5): 340-6.