Advances of Oxidative Stress Impact in Periodontitis: Biomarkers and Effective Targeting Options


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Abstract

:Periodontitis is the most common inflammatory oral disease that affects around 15% of adults and contributes to severe periodontal tissue destruction with subsequent tooth loosening and loss. Among the main pathogenic mechanisms underlying periodontitis, excessive reactive oxygen species production and oxidative stress play a predominant role in inducing both local and systemic damage. Current therapeutic approaches have expanded the conventional methods combined with herbal antioxidant compounds to free radical-scavenging nanomaterials and infrared laser therapy, offering promising pre-clinical evidence in periodontitis management. Herein, we review the pathogenic mechanisms of reactive oxygen species tissue damage, along with recent advances in oxidative stress biomarkers and novel targeting options.

About the authors

Chrysi Pouliou

Dental School, National and Kapodistrian University of Athens

Email: info@benthamscience.net

Christina Piperi

Dental School, National and Kapodistrian University of Athens

Author for correspondence.
Email: info@benthamscience.net

References

  1. Nazir, M.A. Prevalence of periodontal disease, its association with systemic diseases and prevention. Int. J. Health Sci., 2017, 11(2), 72-80. PMID: 28539867
  2. Benjamin, R.M. Oral health: the silent epidemic. Public Health Rep., 2010, 125(2), 158-159. doi: 10.1177/003335491012500202 PMID: 20297740
  3. Sies, H.; Berndt, C.; Jones, D.P. Oxidative stress. Annu. Rev. Biochem., 2017, 86(1), 715-748. doi: 10.1146/annurev-biochem-061516-045037 PMID: 28441057
  4. Jones, D.P. Radical-free biology of oxidative stress. Am. J. Physiol. Cell Physiol., 2008, 295(4), C849-C868. doi: 10.1152/ajpcell.00283.2008 PMID: 18684987
  5. Battino, M.; Bullon, P.; Wilson, M.; Newman, H. Oxidative injury and inflammatory periodontal diseases: the challenge of anti-oxidants to free radicals and reactive oxygen species. Crit. Rev. Oral Biol. Med., 1999, 10(4), 458-476. doi: 10.1177/10454411990100040301 PMID: 10634583
  6. Halliwell, B. Biochemistry of oxidative stress. Biochem. Soc. Trans., 2007, 35(5), 1147-1150. doi: 10.1042/BST0351147 PMID: 17956298
  7. Frijhoff, J.; Winyard, P.G.; Zarkovic, N.; Davies, S.S.; Stocker, R.; Cheng, D.; Knight, A.R.; Taylor, E.L.; Oettrich, J.; Ruskovska, T.; Gasparovic, A.C.; Cuadrado, A.; Weber, D.; Poulsen, H.E.; Grune, T.; Schmidt, H.H.H.W.; Ghezzi, P. Clinical relevance of biomarkers of oxidative stress. Antioxid. Redox Signal., 2015, 23(14), 1144-1170. doi: 10.1089/ars.2015.6317 PMID: 26415143
  8. Franco, R.; Vargas, M.R. Redox biology in neurological function, dysfunction, and aging. Antioxid. Redox Signal., 2018, 28(18), 1583-1586. doi: 10.1089/ars.2018.7509 PMID: 29634346
  9. Sadasivam, N.; Kim, Y.J.; Radhakrishnan, K.; Kim, D.K. Oxidative stress, genomic integrity, and liver diseases. Molecules, 2022, 27(10), 3159. doi: 10.3390/molecules27103159 PMID: 35630636
  10. Turrens, J.F. Mitochondrial formation of reactive oxygen species. J. Physiol., 2003, 552(2), 335-344. doi: 10.1113/jphysiol.2003.049478 PMID: 14561818
  11. Phaniendra, A.; Jestadi, D.B.; Periyasamy, L. Free radicals: properties, sources, targets, and their implication in various diseases. Indian J. Clin. Biochem., 2015, 30(1), 11-26. doi: 10.1007/s12291-014-0446-0 PMID: 25646037
  12. Espinosa-Diez, C.; Miguel, V.; Mennerich, D.; Kietzmann, T.; Sánchez-Pérez, P.; Cadenas, S.; Lamas, S. Antioxidant responses and cellular adjustments to oxidative stress. Redox Biol., 2015, 6, 183-197. doi: 10.1016/j.redox.2015.07.008 PMID: 26233704
  13. Russell, E.G.; Cotter, T.G. New insight into the role of reactive oxygen species (ROS) in cellular signal-transduction processes. Int. Rev. Cell Mol. Biol., 2015, 319, 221-254. doi: 10.1016/bs.ircmb.2015.07.004 PMID: 26404470
  14. Finkel, T. Signal transduction by reactive oxygen species. J. Cell Biol., 2011, 194(1), 7-15. doi: 10.1083/jcb.201102095 PMID: 21746850
  15. Weidinger, A.; Kozlov, A. Biological activities of reactive oxygen and nitrogen species: oxidative stress versus signal transduction. Biomolecules, 2015, 5(2), 472-484. doi: 10.3390/biom5020472 PMID: 25884116
  16. Obeng-Gyasi, E. Lead exposure and oxidative stress-a life course approach in U.S. adults. Toxics, 2018, 6(3), 42. doi: 10.3390/toxics6030042 PMID: 30071602
  17. Besednova, N.N.; Andryukov, B.G.; Zaporozhets, T.S.; Kuznetsova, T.A.; Kryzhanovsky, S.P.; Ermakova, S.P.; Galkina, I.V.; Shchelkanov, M.Y. Molecular targets of brown algae phlorotannins for the therapy of inflammatory processes of various origins. Mar. Drugs, 2022, 20(4), 243. doi: 10.3390/md20040243 PMID: 35447916
  18. Perera, W.P.T.D.; Dissanayake, R.K.; Ranatunga, U.I.; Hettiarachchi, N.M.; Perera, K.D.C.; Unagolla, J.M.; De Silva, R.T.; Pahalagedara, L.R. Curcumin loaded zinc oxide nanoparticles for activity-enhanced antibacterial and anticancer applications. RSC Advances, 2020, 10(51), 30785-30795. doi: 10.1039/D0RA05755J PMID: 35516060
  19. Zhu, Y.; Luo, M.; Bai, X.; Li, J.; Nie, P.; Li, B.; Luo, P. SS-31, a mitochondria-targeting peptide, ameliorates kidney disease. Oxid. Med. Cell. Longev., 2022, 2022, 1-13. doi: 10.1155/2022/1295509 PMID: 35707274
  20. Su, L.J.; Zhang, J.H.; Gomez, H.; Murugan, R.; Hong, X.; Xu, D.; Jiang, F.; Peng, Z.Y. Reactive oxygen species-induced lipid peroxidation in apoptosis, autophagy, and ferroptosis. Oxid. Med. Cell. Longev., 2019, 2019, 1-13. doi: 10.1155/2019/5080843 PMID: 31737171
  21. Ruan, Y.; Jiang, S.; Gericke, A. Age-related macular degeneration: role of oxidative stress and blood vessels. Int. J. Mol. Sci., 2021, 22(3), 1296. doi: 10.3390/ijms22031296 PMID: 33525498
  22. Chen, Z.; Gan, J.; Zhang, M.; Du, Y.; Zhao, H. Ferroptosis and its emerging role in pre-eclampsia. Antioxidants, 2022, 11(7), 1282. doi: 10.3390/antiox11071282 PMID: 35883776
  23. Caliri, A.W.; Tommasi, S.; Besaratinia, A. Relationships among smoking, oxidative stress, inflammation, macromolecular damage, and cancer. Mutat. Res. Rev. Mutat. Res., 2021, 787, 108365. doi: 10.1016/j.mrrev.2021.108365 PMID: 34083039
  24. Fu, Z.; Zhang, J.; Zhang, Y. Role of molecular hydrogen in ageing and ageing-related diseases. Oxid. Med. Cell. Longev., 2022, 2022, 1-17. doi: 10.1155/2022/2249749 PMID: 35340218
  25. Matsuo, K.; Hosoda, K.; Tanaka, J.; Yamamoto, Y.; Imahori, T.; Nakai, T.; Irino, Y.; Shinohara, M.; Sasayama, T.; Kohmura, E. Geranylgeranylacetone attenuates cerebral ischemia–reperfusion injury in rats through the augmentation of HSP 27 phosphorylation: a preliminary study. BMC Neurosci., 2021, 22(1), 9. doi: 10.1186/s12868-021-00614-7 PMID: 33557752
  26. Sologova, S.S.; Zavadskiy, S.P.; Mokhosoev, I.M.; Moldogazieva, N.T. Short linear motifs orchestrate functioning of human proteins during embryonic development, redox regulation, and cancer. Metabolites, 2022, 12(5), 464. doi: 10.3390/metabo12050464 PMID: 35629968
  27. Khan, S.N.; Kumar, S.; Iqbal, S.; Joy, M.T.; Ramaprabha, G. Oxidative stress, antioxidants and periodontitis: how are they linked? Int. J. Oral Care Res., 2018, 6(2), 107-112.
  28. Jones, D.P. Redefining oxidative stress. Antioxid. Redox Signal., 2006, 8(9-10), 1865-1879. doi: 10.1089/ars.2006.8.1865 PMID: 16987039
  29. Trivedi, S.; Lal, N. Oxidative stress and periodontitis: cause or effect. J. Nepal Dent. Assoc., 2015, 15, 87.
  30. Jia, L.; Han, N.; Du, J.; Guo, L.; Luo, Z.; Liu, Y. Pathogenesis of important virulence factors of Porphyromonas gingivalis via toll-like receptors. Front. Cell. Infect. Microbiol., 2019, 9, 262. doi: 10.3389/fcimb.2019.00262 PMID: 31380305
  31. Sidhu, P.; Shankargouda, S.; Rath, A.; Hesarghatta Ramamurthy, P.; Fernandes, B.; Kumar Singh, A. Therapeutic benefits of liquorice in dentistry. J. Ayurveda Integr. Med., 2020, 11(1), 82-88. doi: 10.1016/j.jaim.2017.12.004 PMID: 30391123
  32. Miyasaki, K.T. The neutrophil: mechanisms of controlling periodontal bacteria. J. Periodontol., 1991, 62(12), 761-774. doi: 10.1902/jop.1991.62.12.761 PMID: 1765939
  33. Gustafsson, A.; Ito, H.; Åsman, B.; Bergström, K. Hyper-reactive mononuclear cells and neutrophils in chronic periodontitis. J. Clin. Periodontol., 2006, 33(2), 126-129. doi: 10.1111/j.1600-051X.2005.00883.x PMID: 16441737
  34. Matthews, J.B.; Wright, H.J.; Roberts, A.; Cooper, P.R.; Chapple, I.L.C. Hyperactivity and reactivity of peripheral blood neutrophils in chronic periodontitis. Clin. Exp. Immunol., 2007, 147(2), 255-264. doi: 10.1111/j.1365-2249.2006.03276.x PMID: 17223966
  35. Ling, M.R.; Chapple, I.L.C.; Matthews, J.B. Neutrophil superoxide release and plasma C-reactive protein levels pre- and post-periodontal therapy. J. Clin. Periodontol., 2016, 43(8), 652-658. doi: 10.1111/jcpe.12575 PMID: 27168055
  36. Chapple, I. L.; Matthews, J. B. The role of reactive oxygen and antioxidant species in periodontal tissue destruction. Periodontol, 2007, 43, 160-232. doi: 10.1111/j.1600-0757.2006.00178.x
  37. Gustafsson, A.; Åsman, B. Increased release of free oxygen radicals from peripheral neutrophils in adult periodontitis after Feγ-receptor stimulation. J. Clin. Periodontol., 1996, 23(1), 38-44. doi: 10.1111/j.1600-051X.1996.tb00502.x PMID: 8636455
  38. Fredriksson, M.; Gustafsson, A.; Åsman, B.; Bergström, K. Hyper-reactive peripheral neutrophils in adult periodontitis: generation of chemiluminescence and intracellular hydrogen peroxide after in vitro priming and FcγR-stimulation. J. Clin. Periodontol., 1998, 25(5), 394-398. doi: 10.1111/j.1600-051X.1998.tb02461.x PMID: 9650876
  39. Fredriksson, M.I.; Gustafsson, A.K.; Bergström, K.G.; Åsman, B.E. Constitutionally hyperreactive neutrophils in periodontitis. J. Periodontol., 2003, 74(2), 219-224. doi: 10.1902/jop.2003.74.2.219 PMID: 12666711
  40. Guarnieri, C.; Zucchelli, G.; Bernardi, F.; Scheda, M.; Valentini, A.F.; Calandriello, M. Enhanced superoxide production with no change of the antioxidant activity in gingival fluid of patients with chronic adult periodontitis. Free Radic. Res. Commun., 1991, 15(1), 11-16. doi: 10.3109/10715769109049120 PMID: 1663065
  41. Kimura, S.; Yonemura, T.; Kaya, H. Increased oxidative product formation by peripheral blood polymorphonuclear leukocytes in human periodontal diseases. J. Periodontal Res., 1993, 28(3), 197-203. doi: 10.1111/j.1600-0765.1993.tb01069.x PMID: 8496783
  42. Bullon, P.; Cordero, M.D.; Quiles, J.L.; Morillo, J.M.; Ramirez-Tortosa, M.C.; Battino, M. Mitochondrial dysfunction promoted by Porphyromonas gingivalis lip- opolysaccharide as a possible link between cardiovascular disease and periodontitis. Free Radic. Biol. Med., 2011, 50(10), 1336-1343. doi: 10.1016/j.freeradbiomed.2011.02.018 PMID: 21354301
  43. Gölz, L.; Memmert, S.; Rath-Deschner, B.; Jäger, A.; Appel, T.; Baumgarten, G.; Götz, W.; Frede, S. LPS from P. gingivalis and hypoxia increases oxidative stress in periodontal ligament fibroblasts and contributes to periodontitis. Mediators Inflamm., 2014, 2014, 1-13. doi: 10.1155/2014/986264 PMID: 25374447
  44. Govindaraj, P.; Khan, N.A.; Gopalakrishna, P.; Chandra, R.V.; Vanniarajan, A.; Reddy, A.A.; Singh, S.; Kumaresan, R.; Srinivas, G.; Singh, L.; Thangaraj, K. Mitochondrial dysfunction and genetic heterogeneity in chronic periodontitis. Mitochondrion, 2011, 11(3), 504-512. doi: 10.1016/j.mito.2011.01.009 PMID: 21296687
  45. Sui, L.; Wang, J.; Xiao, Z.; Yang, Y.; Yang, Z.; Ai, K. ROS-scavenging nanomaterials to treat periodontitis. Front Chem., 2020, 8, 595530. doi: 10.3389/fchem.2020.595530 PMID: 33330384
  46. Tottoli, E.M.; Dorati, R.; Genta, I.; Chiesa, E.; Pisani, S.; Conti, B. Skin wound healing process and new emerging technologies for skin wound care and regeneration. Pharmaceutics, 2020, 12(8), 735. doi: 10.3390/pharmaceutics12080735 PMID: 32764269
  47. Cordani, M.; Resines-Urien, E.; Gamonal, A.; Milán-Rois, P.; Salmon, L.; Bousseksou, A.; Costa, J.S.; Somoza, Á. Water soluble iron-based coordination trimers as synergistic adjuvants for pancreatic cancer. Antioxidants, 2021, 10(1), 66. doi: 10.3390/antiox10010066 PMID: 33430324
  48. Lee, N.K.; Choi, Y.G.; Baik, J.Y.; Han, S.Y.; Jeong, D.; Bae, Y.S.; Kim, N.; Lee, S.Y. A crucial role for reactive oxygen species in RANKL-induced osteoclast differentiation. Blood, 2005, 106(3), 852-859. doi: 10.1182/blood-2004-09-3662 PMID: 15817678
  49. Cochran, D.L. Inflammation and bone loss in periodontal disease. J. Periodontol., 2008, 79(8S)(Suppl.), 1569-1576. doi: 10.1902/jop.2008.080233 PMID: 18673012
  50. Graves, D. Cytokines that promote periodontal tissue destruction. J. Periodontol., 2008, 79(8S)(Suppl.), 1585-1591. doi: 10.1902/jop.2008.080183 PMID: 18673014
  51. Garrett, I.R.; Boyce, B.F.; Oreffo, R.O.; Bonewald, L.; Poser, J.; Mundy, G.R. Oxygen-derived free radicals stimulate osteoclastic bone resorption in rodent bone in vitro and in vivo. J. Clin. Invest., 1990, 85(3), 632-639. doi: 10.1172/JCI114485 PMID: 2312718
  52. Fearon, I.M.; Phillips, G.; Carr, T.; Taylor, M.; Breheny, D.; Faux, S.P. The role of oxidative stress in smoking-related diseases. Mini Rev. Org. Chem., 2011, 8, 360-371. doi: 10.2174/157019311797440317
  53. Caley, M.P.; Martins, V.L.C.; O’Toole, E.A. Metalloproteinases and wound healing. Adv. Wound Care (New Rochelle), 2015, 4(4), 225-234. doi: 10.1089/wound.2014.0581 PMID: 25945285
  54. Stanisic, D.; Obradovic, R.; Vujovic, S.; Jovanovic, M.; Zivkovic, V. The connection of periodontal disease and diabetes mellitus: the role of matrix metalloproteinases and oxidative stress. Serbian J. Exp. Clin. Res., 1019, 2019, 1-10.
  55. Franco, C.; Patricia, H.R.; Timo, S.; Claudia, B.; Marcela, H. Matrix metalloproteinases as regulators of periodontal inflammation. Int. J. Mol. Sci., 2017, 18(2), 440. doi: 10.3390/ijms18020440 PMID: 28218665
  56. Cook-Mills, J.M. Hydrogen peroxide activation of endothelial cell-associated MMPs during VCAM-1-dependent leukocyte migration. Cell. Mol. Biol., 2006, 52(4), 8-16. PMID: 17543193
  57. Osorio, C.; Cavalla, F.; Paula-Lima, A.; Díaz-Araya, G.; Vernal, R.; Ahumada, P.; Gamonal, J.; Hernández, M. H2O2 activates matrix metalloproteinases through the nuclear factor kappa B pathway and Ca2+ signals in human periodontal fibroblasts. J. Periodontal Res., 2015, 50(6), 798-806. doi: 10.1111/jre.12267 PMID: 25824649
  58. Hernández-Ríos, P.; Pussinen, P.J.; Vernal, R.; Hernández, M. Oxidative stress in the local and systemic events of apical periodontitis. Front. Physiol., 2017, 8, 869. doi: 10.3389/fphys.2017.00869 PMID: 29163211
  59. Desarda, H.; Gaikwad, S. Matrix metalloproteinases & Implication in periodontitis- A short review. Journal of Dental and Allied Sciences, 2013, 2(2), 66. doi: 10.4103/2277-4696.159288
  60. Moseley, R.; Waddington, R.J.; Embery, G. Degradation of glycosaminoglycans by reactive oxygen species derived from stimulated polymorphonuclear leukocytes. Biochim. Biophys. Acta Mol. Basis Dis., 1997, 1362(2-3), 221-231. doi: 10.1016/S0925-4439(97)00083-5 PMID: 9540853
  61. Montemurro, N.; Perrini, P.; Rapone, B. Clinical risk and overall survival in patients with diabetes mellitus, hyperglycemia and glioblastoma multiforme. a review of the current literature. Int. J. Environ. Res. Public Health, 2020, 17(22), 8501. doi: 10.3390/ijerph17228501 PMID: 33212778
  62. Pham, V.H.; Gargiulo Isacco, C.; Nguyen, K.C.D.; Le, S.H.; Tran, D.K.; Nguyen, Q.V.; Pham, H.T.; Aityan, S.; Pham, S.T.; Cantore, S.; Inchingolo, A.M.; Inchingolo, A.D.; Dipalma, G.; Ballini, A.; Inchingolo, F. Rapid and sensitive diagnostic procedure for multiple detection of pandemic Coronaviridae family members SARS-CoV-2, SARS-CoV, MERS-CoV and HCoV: a translational research and cooperation between the Phan Chau Trinh University in Vietnam and University of Bari "Aldo Moro" in Italy. Eur. Rev. Med. Pharmacol. Sci., 2020, 24(12), 7173-7191. doi: 10.26355/eurrev_202006_21713 PMID: 32633414
  63. Rittié, L.; Monboisse, J.C.; Gorisse, M.C.; Gillery, P. Malondialdehyde binding to proteins dramatically alters fibroblast functions. J. Cell. Physiol., 2002, 191(2), 227-236. doi: 10.1002/jcp.10093 PMID: 12064466
  64. Żukowski, P.; Maciejczyk, M.; Waszkiel, D. Sources of free radicals and oxidative stress in the oral cavity. Arch. Oral Biol., 2018, 92, 8-17. doi: 10.1016/j.archoralbio.2018.04.018 PMID: 29729478
  65. Sam, C.H.; Lu, H.K. The role of hypochlorous acid as one of the reactive oxygen species in periodontal disease. J. Dent. Sci., 2009, 4(2), 45-54. doi: 10.1016/S1991-7902(09)60008-8
  66. Morgan, M.J.; Liu, Z. Crosstalk of reactive oxygen species and NF-κB signaling. Cell Res., 2011, 21(1), 103-115. doi: 10.1038/cr.2010.178 PMID: 21187859
  67. Souza, J.A.C.; Junior, C.R.; Garlet, G.P.; Nogueira, A.V.B.; Cirelli, J.A. Modulation of host cell signaling pathways as a therapeutic approach in periodontal disease. J. Appl. Oral Sci., 2012, 20(2), 128-138. doi: 10.1590/S1678-77572012000200002 PMID: 22666826
  68. Nakano, H.; Nakajima, A.; Sakon-Komazawa, S.; Piao, J-H.; Xue, X.; Okumura, K. Reactive oxygen species mediate crosstalk between NF-κB and JNK. Cell Death Differ., 2006, 13(5), 730-737. doi: 10.1038/sj.cdd.4401830 PMID: 16341124
  69. Kang, S.W.; Park, H.J.; Ban, J.Y.; Chung, J.H.; Chun, G.S.; Cho, J.O. Effects of nicotine on apoptosis in human gingival fibroblasts. Arch. Oral Biol., 2011, 56(10), 1091-1097. doi: 10.1016/j.archoralbio.2011.03.016 PMID: 21497792
  70. Oben, K.Z.; Alhakeem, S.S.; McKenna, M.K.; Brandon, J.A.; Mani, R.; Noothi, S.K.; Jinpeng, L.; Akunuru, S.; Dhar, S.K.; Singh, I.P.; Liang, Y.; Wang, C.; Abdel-Latif, A.; Stills, H.F., Jr; St Clair, D.K.; Geiger, H.; Muthusamy, N.; Tohyama, K.; Gupta, R.C.; Bondada, S. Oxidative stress-induced JNK/AP-1 signaling is a major pathway involved in selective apoptosis of myelodysplastic syndrome cells by Withaferin-A. Oncotarget, 2017, 8(44), 77436-77452. doi: 10.18632/oncotarget.20497 PMID: 29100399
  71. Guo, H.; Callaway, J.B.; Ting, J.P.Y. Inflammasomes: mechanism of action, role in disease, and therapeutics. Nat. Med., 2015, 21(7), 677-687. doi: 10.1038/nm.3893 PMID: 26121197
  72. Ding, P.H.; Yang, M.X.; Wang, N.N.; Jin, L.J.; Dong, Y.; Cai, X.; Chen, L.L. Porphyromonas gingivalis-induced NLRP3 inflammasome activation and its downstream interleukin-1β release depend on caspase-4. Front. Microbiol., 2020, 11, 1881. doi: 10.3389/fmicb.2020.01881 PMID: 32903638
  73. Marchesan, J.T.; Girnary, M.S.; Moss, K.; Monaghan, E.T.; Egnatz, G.J.; Jiao, Y.; Zhang, S.; Beck, J.; Swanson, K.V. Role of inflammasomes in the pathogenesis of periodontal disease and therapeutics. Periodontol. 2000, 2020, 82(1), 93-114. doi: 10.1111/prd.12269 PMID: 31850638
  74. Niture, S.K.; Khatri, R.; Jaiswal, A.K. Regulation of Nrf2-an update. Free Radic. Biol. Med., 2014, 66, 36-44. doi: 10.1016/j.freeradbiomed.2013.02.008 PMID: 23434765
  75. Yamaguchi, Y.; Kurita-Ochiai, T.; Kobayashi, R.; Suzuki, T.; Ando, T. Regulation of the NLRP3 inflammasome in Porphyromonas gingivalis-accelerated periodontal disease. Inflamm. Res., 2017, 66(1), 59-65. doi: 10.1007/s00011-016-0992-4 PMID: 27665233
  76. Franchi, L.; Eigenbrod, T.; Muñoz-Planillo, R.; Nuñez, G. The inflammasome: a caspase-1-activation platform that regulates immune responses and disease pathogenesis. Nat. Immunol., 2009, 10(3), 241-247. doi: 10.1038/ni.1703 PMID: 19221555
  77. Sima, C.; Aboodi, G.M.; Lakschevitz, F.S.; Sun, C.; Goldberg, M.B.; Glogauer, M. Nuclear Factor Erythroid 2-Related Factor 2 Down-Regulation in oral neutrophils is associated with periodontal oxidative damage and severe chronic periodontitis. Am. J. Pathol., 2016, 186(6), 1417-1426. doi: 10.1016/j.ajpath.2016.01.013 PMID: 27070823
  78. Hyeon, S.; Lee, H.; Yang, Y.; Jeong, W. Nrf2 deficiency induces oxidative stress and promotes RANKL-induced osteoclast differentiation. Free Radic. Biol. Med., 2013, 65, 789-799. doi: 10.1016/j.freeradbiomed.2013.08.005 PMID: 23954472
  79. Kataoka, K.; Ekuni, D.; Tomofuji, T.; Irie, K.; Kunitomo, M.; Uchida, Y.; Fukuhara, D.; Morita, M. Visualization of oxidative stress induced by experimental periodontitis in Keap1-dependent oxidative stress detector- luciferase mice. Int. J. Mol. Sci., 2016, 17(11), 1907. doi: 10.3390/ijms17111907 PMID: 27854327
  80. Ahmadi-Motamayel, F.; Goodarzi, M.T.; Jamshidi, Z.; Kebriaei, R. Evaluation of salivary and serum antioxidant and oxidative stress statuses in patients with chronic periodontitis: A case-control study. Front. Physiol., 2017, 8, 189. doi: 10.3389/fphys.2017.00189 PMID: 28408887
  81. Yagi, K. A simple fluorometric assay for lipoperoxide in blood plasma. Biochem. Med., 1976, 15(2), 212-216. doi: 10.1016/0006-2944(76)90049-1 PMID: 962904
  82. Panjamurthy, K.; Manoharan, S.; Ramachandran, C.R. Lipid peroxidation and antioxidant status in patients with periodontitis. Cell. Mol. Biol. Lett., 2005, 10(2), 255-264. PMID: 16010291
  83. Tonguç, M.Ö.; Öztürk, Ö.; Sütçü, R.; Ceyhan, B.M.; Kılınç, G.; Sönmez, Y.; Yetkin Ay, Z.; Şahin, Ü.; Baltacıoğlu, E.; Kırzıoğlu, F.Y. The impact of smoking status on antioxidant enzyme activity and malondialdehyde levels in chronic periodontitis. J. Periodontol., 2011, 82(9), 1320-1328. doi: 10.1902/jop.2011.100618 PMID: 21219099
  84. Ghallab, N.A.; Hamdy, E.; Shaker, O.G. Malondialdehyde, superoxide, dismutase and melatonin levels in GFC of aggressive and chronic periodontitis patients. Aust. Dent. J., 2016, 61, 53-61. doi: 10.1111/adj.12294 PMID: 25581300
  85. Dakovic, D. Malondialdehyde as an indicator of local oxidative cell damage in periodontitis patients. Master's thesis, Military Medical Academy, Sofia, Bulgaria, 2005.
  86. 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(1), 70-78. doi: 10.1111/j.1834-7819.2009.01123.x PMID: 20415915
  87. Petersen, D.R.; Doorn, J.A. Reactions of 4-hydroxynonenal with proteins and cellular targets. Free Radic. Biol. Med., 2004, 37(7), 937-945. doi: 10.1016/j.freeradbiomed.2004.06.012 PMID: 15336309
  88. Altıngöz, S.M.; Kurgan, Ş.; Önder, C.; Serdar, M.A.; Ünlütürk, U.; Uyanık, M.; Başkal, N.; Tatakis, D.N.; Günhan, M. Salivary and serum oxidative stress biomarkers and advanced glycation end products in periodontitis patients with or without diabetes: A cross-sectional study. J. Periodontol., 2021, 92(9), 1274-1285. doi: 10.1002/JPER.20-0406 PMID: 33277933
  89. Roberts, L.J., II; Morrow, J.D. Products of the isoprostane pathway: unique bioactive compounds and markers of lipid peroxidation. Cell. Mol. Life Sci., 2002, 59(5), 808-820. doi: 10.1007/s00018-002-8469-8 PMID: 12088281
  90. Su, H.; Gornitsky, M.; Velly, A.M.; Yu, H.; Benarroch, M.; Schipper, H.M. Salivary DNA, lipid, and protein oxidation in nonsmokers with periodontal disease. Free Radic. Biol. Med., 2009, 46(7), 914-921. doi: 10.1016/j.freeradbiomed.2009.01.008 PMID: 19280702
  91. Pradeep, A.R.; Rao, N.S.; Bajaj, P.; Agarwal, E. 8-Isoprostane: A lipid peroxidation product in gingival crevicular fluid in healthy, gingivitis and chronic periodontitis subjects. Arch. Oral Biol., 2013, 58(5), 500-504. doi: 10.1016/j.archoralbio.2013.01.011 PMID: 23453083
  92. Nguyen, T.T.; Ngo, L.Q.; Promsudthi, A.; Surarit, R. Salivary oxidative stress biomarkers in chronic periodontitis and acute coronary syndrome. Clin. Oral Investig., 2017, 21(7), 2345-2353. doi: 10.1007/s00784-016-2029-3 PMID: 27987039
  93. Halliwell, B. Why and how should we measure oxidative DNA damage in nutritional studies? How far have we come? Am. J. Clin. Nutr., 2000, 72(5), 1082-1087. doi: 10.1093/ajcn/72.5.1082 PMID: 11063432
  94. Ekuni, D.; Tomofuji, T.; Tamaki, N.; Sanbe, T.; Azuma, T.; Yamanaka, R.; Yamamoto, T.; Watanabe, T. Mechanical stimulation of gingiva reduces plasma 8-OHdG level in rat periodontitis. Arch. Oral Biol., 2008, 53(4), 324-329. doi: 10.1016/j.archoralbio.2007.10.005 PMID: 18031711
  95. Yang, X.; Li, C.; Pan, Y. The influences of periodontal status and periodontal pathogen quantity on salivary 8-hydroxydeoxyguanosine and interleukin-17 levels. J. Periodontol., 2016, 87(5), 591-600. doi: 10.1902/jop.2015.150390 PMID: 26654345
  96. Önder, C.; Kurgan, Ş.; Altıngöz, S.M.; Bağış, N.; Uyanık, M.; Serdar, M.A.; Kantarcı, A.; Günhan, M. Impact of non-surgical periodontal therapy on saliva and serum levels of markers of oxidative stress. Clin. Oral Investig., 2017, 21(6), 1961-1969. doi: 10.1007/s00784-016-1984-z PMID: 27807715
  97. Zamora-Perez, A.L.; Ortiz-García, Y.M.; Lazalde-Ramos, B.P.; Guerrero-Velázquez, C.; Gómez-Meda, B.C.; Ramírez-Aguilar, M.Á.; Zúñiga-González, G.M. Increased micronuclei and nuclear abnormalities in buccal mucosa and oxidative damage in saliva from patients with chronic and aggressive periodontal diseases. J. Periodontal Res., 2015, 50(1), 28-36. doi: 10.1111/jre.12175 PMID: 24666368
  98. Çanakçı, C.F.; Tatar, A.; Çanakçı, V.; Cicek, Y.; Oztas, S.; Orbak, R. New evidence of premature oxidative DNA damage: mitochondrial DNA deletion in gingival tissue of patients with periodontitis. J. Periodontol., 2006, 77(11), 1894-1900. doi: 10.1902/jop.2006.060108 PMID: 17076616
  99. Masi, S.; Salpea, K.D.; Li, K.; Parkar, M.; Nibali, L.; Donos, N.; Patel, K.; Taddei, S.; Deanfield, J.E.; D’Aiuto, F.; Humphries, S.E. Oxidative stress, chronic inflammation, and telomere length in patients with periodontitis. Free Radic. Biol. Med., 2011, 50(6), 730-735. doi: 10.1016/j.freeradbiomed.2010.12.031 PMID: 21195167
  100. Vo, T.T.T.; Chu, P.M.; Tuan, V.P.; Te, J.S.L.; Lee, I.T. The promising role of antioxidant phytochemicals in the prevention and preatment of periodontal disease via the inhibition of oxidative stress pathways: updated insights. Antioxidants, 2020, 9(12), 1211. doi: 10.3390/antiox9121211 PMID: 33271934
  101. Bouayed, J.; Bohn, T. Exogenous antioxidants-double-edged swords in cellular redox state: Health beneficial effects at physiologic doses versus deleterious effects at high doses. Oxid. Med. Cell. Longev., 2010, 3(4), 228-237. doi: 10.4161/oxim.3.4.12858 PMID: 20972369
  102. J Mbah, C.; Orabueze, I.; H Okorie, N. Antioxidants properties of natural and synthetic chemical compounds: Therapeutic effects on biological system. Acta Scientific Pharmaceutical Sciences, 2019, 3(6), 28-42. doi: 10.31080/ASPS.2019.03.0273
  103. Jindal, M.; Tripathi, P.; Blaggana, V.; Upadhyay, P.; Gupta, S.; Nishat, S. Antioxidant therapy (lycopene and green tea extract) in periodontal disease: A promising paradigm. J. Indian Soc. Periodontol., 2019, 23(1), 25-30. doi: 10.4103/jisp.jisp_277_18 PMID: 30692739
  104. Kaur, G.; Kathariya, R.; Bansal, S.; Singh, A.; Shahakar, D. Dietary antioxidants and their indispensable role in periodontal health. J. Food Drug Anal., 2016, 24(2), 239-246. doi: 10.1016/j.jfda.2015.11.003 PMID: 28911576
  105. Toraman, A.; Arabaci, T.; Aytekin, Z.; Albayrak, M.; Bayir, Y. Effects of vitamin C local application on ligature-induced periodontitis in diabetic rats. J. Appl. Oral Sci., 2020, 28, e20200444. doi: 10.1590/1678-7757-2020-0444 PMID: 33263670
  106. Li, L.; Zhang, Y.L.; Liu, X.Y.; Meng, X.; Zhao, R.Q.; Ou, L.L.; Li, B.Z.; Xing, T. Periodontitis exacerbates and promotes the progression of chronic kidney disease through oral flora, cytokines, and oxidative stress. Front. Microbiol., 2021, 12, 656372. doi: 10.3389/fmicb.2021.656372 PMID: 34211440
  107. Permuy, M.; López-Peña, M.; González-Cantalapiedra, A.; Muñoz, F. Melatonin: A review of its potential functions and effects on dental disease. Int. J. Mol. Sci., 2017, 18(4), 865. doi: 10.3390/ijms18040865 PMID: 28422058
  108. Ramesh, A.; Varghese, S.; Doraiswamy, J.; Malaiappan, S. Herbs as an antioxidant arsenal for periodontal diseases. J. Intercult. Ethnopharmacol., 2016, 5(1), 92-96. doi: 10.5455/jice.20160122065556 PMID: 27069730
  109. Stahl, W.; Sies, H. Antioxidant activity of carotenoids. Mol. Aspects Med., 2003, 24(6), 345-351. doi: 10.1016/S0098-2997(03)00030-X PMID: 14585305
  110. Kajiura, Y.; Nishikawa, Y.; Lew, J.H.; Kido, J.; Nagata, T.; Naruishi, K. β-carotene suppresses Porphyromonas gingivalis lipopolysaccharide-mediated cytokine production in THP-1 monocytes cultured with high glucose condition. Cell Biol. Int., 2018, 42(1), 105-111. doi: 10.1002/cbin.10873 PMID: 28906038
  111. Young, A.J.; Lowe, G.M. Antioxidant and prooxidant properties of carotenoids. Arch. Biochem. Biophys., 2001, 385(1), 20-27. doi: 10.1006/abbi.2000.2149 PMID: 11361018
  112. Nishigaki, M.; Yamamoto, T.; Ichioka, H.; Honjo, K.; Yamamoto, K.; Oseko, F.; Kita, M.; Mazda, O.; Kanamura, N. β-cryptoxanthin regulates bone resorption related-cytokine production in human periodontal ligament cells. Arch. Oral Biol., 2013, 58(7), 880-886. doi: 10.1016/j.archoralbio.2013.01.005 PMID: 23452546
  113. Balci Yuce, H.; Lektemur Alpan, A.; Gevrek, F.; Toker, H. Investigation of the effect of astaxanthin on alveolar bone loss in experimental periodontitis. J. Periodontal Res., 2018, 53(1), 131-138. doi: 10.1111/jre.12497 PMID: 29044575
  114. Martillanes, S.; Rocha-Pimienta, J.; Delgado-Adamez, J. Agrifood by-products as a source of phytochemical compounds. In: Descriptive food science; intechopen, 2018.
  115. Vuolo, M.M.; Lima, V.S.; Junior, M.R.M. Bioactive Compounds: Health Benefits and Potential Applications; Woodhead Publishing: Cambridge, UK, 2019, pp. 33-50. doi: 10.1016/B978-0-12-814774-0.00002-5
  116. Kumar, N.; Goel, N. Phenolic acids: Natural versatile molecules with promising therapeutic applications. Biotechnol. Rep. (Amst.), 2019, 24, e00370. doi: 10.1016/j.btre.2019.e00370 PMID: 31516850
  117. Nugala, B.; Namasi, A.; Emmadi, P.; Krishna, P.M. Role of green tea as an antioxidant in periodontal disease: The Asian paradox. J. Indian Soc. Periodontol., 2012, 16(3), 313-316. doi: 10.4103/0972-124X.100902 PMID: 23162321
  118. Cai, Y.; Chen, Z.; Liu, H.; Xuan, Y.; Wang, X.; Luan, Q. Green tea epigallocatechin-3-gallate alleviates Porphyromonas gingivalis -induced periodontitis in mice. Int. Immunopharmacol., 2015, 29(2), 839-845. doi: 10.1016/j.intimp.2015.08.033 PMID: 26359545
  119. Hrishi, T.S.; Kundapur, P.P.; Naha, A.; Thomas, B.S.; Kamath, S.; Bhat, G.S. Effect of adjunctive use of green tea dentifrice in periodontitis patients – A Randomized Controlled Pilot Study. Int. J. Dent. Hyg., 2016, 14(3), 178-183. doi: 10.1111/idh.12131 PMID: 25690541
  120. Carocho, M.; Ferreira, I.C.F.R. A review on antioxidants, prooxidants and related controversy: Natural and synthetic compounds, screening and analysis methodologies and future perspectives. Food Chem. Toxicol., 2013, 51, 15-25. doi: 10.1016/j.fct.2012.09.021 PMID: 23017782
  121. Gutiérrez-Venegas, G.; Kawasaki-Cárdenas, P.; Rita Arroyo-Cruz, S.; Maldonado-Frías, S. Luteolin inhibits lipopolysaccharide actions on human gingival fibroblasts. Eur. J. Pharmacol., 2006, 541(1-2), 95-105. doi: 10.1016/j.ejphar.2006.03.069 PMID: 16762341
  122. Ben Lagha, A.; Dudonné, S.; Desjardins, Y.; Grenier, D. Wild blueberry (Vaccinium angustifolium Ait.) polyphenols target Fisobacterium nucleatum and the host inflammatory response: Potential innovative molecules for treating periodontal disease. J. Agric. Food Chem., 2015, 63(31), 6999-7008. doi: 10.1021/acs.jafc.5b01525 PMID: 26207764
  123. Ben Lagha, A.; Haas, B.; Grenier, D. Tea polyphenols inhibit the growth and virulence properties of Fusobacterium nucleatum. Sci. Rep., 2017, 7(1), 44815. doi: 10.1038/srep44815 PMID: 28322293
  124. Bouarab-Chibane, L.; Forquet, V.; Lantéri, P.; Clément, Y.; Léonard-Akkari, L.; Oulahal, N.; Degraeve, P.; Bordes, C. Antibacterial properties of polyphenols: characterization and QSAR (quantitative structure activity relationship) models. Front. Microbiol., 2019, 10, 829. doi: 10.3389/fmicb.2019.00829 PMID: 31057527
  125. Batchu, S.N.; Chaudhary, K.R.; Wiebe, G.J.; Seubert, J.M. Bioactive compounds in heart disease. In: Bioactive Food as Dietary Interventions for Cardiovascular Disease; Watson, R.R.; Preedy, V.R., Eds.; Academic Press: San Diego, CA, USA, 2013; pp. 431-442. doi: 10.1016/B978-0-12-396485-4.00026-8
  126. Chan, J.Y.Y.; Yuen, A.C.Y.; Chan, R.Y.K.; Chan, S.W. A review of the cardiovascular benefits and antioxidant properties of allicin. Phytother. Res., 2013, 27(5), 637-646. doi: 10.1002/ptr.4796 PMID: 22888009
  127. Provinciali, M.; Pierpaoli, E.; Piacenza, F.; Giacconi, R.; Costarelli, L.; Basso, A.; Recchioni, R.; Marcheselli, F.; Bray, D.; Benlhassan, K. Nutritional modulators of cellular senescence in vitro. In: Molecular Basis of Nutrition and Aging; Academic Press.: London, UK., 2016. doi: 10.1016/B978-0-12-801816-3.00022-4
  128. Shahzad, M.; Millhouse, E.; Culshaw, S.; Edwards, C.A.; Ramage, G.; Combet, E. Selected dietary (poly)phenols inhibit periodontal pathogen growth and biofilm formation. Food Funct., 2015, 6(3), 719-729. doi: 10.1039/C4FO01087F PMID: 25585200
  129. Elburki, M.S.; Moore, D.D.; Terezakis, N.G.; Zhang, Y.; Lee, H.M.; Johnson, F.; Golub, L.M. A novel chemically modified curcumin reduces inflammation-mediated connective tissue breakdown in a rat model of diabetes: periodontal and systemic effects. J. Periodontal Res., 2017, 52(2), 186-200. doi: 10.1111/jre.12381 PMID: 27038334
  130. Guimarães, M.R.; Coimbra, L.S.; de Aquino, S.G.; Spolidorio, L.C.; Kirkwood, K.L.; Rossa, C., Jr. Potent anti-inflammatory effects of systemically administered curcumin modulate periodontal disease in vivo. J. Periodontal Res., 2011, 46(2), 269-279. doi: 10.1111/j.1600-0765.2010.01342.x PMID: 21306385
  131. Elburki, M.S.; Rossa, C., Jr; Guimarães-Stabili, M.R.; Lee, H.M.; Curylofo-Zotti, F.A.; Johnson, F.; Golub, L.M. A chemically modified curcumin (CMC 2.24) inhibits nuclear factor kappaB activation and inflammatory bone loss in murine models of LPS-induced experimental periodontitis and diabetes-associated natural periodontitis. Inflammation, 2017, 40(4), 1436-1449. doi: 10.1007/s10753-017-0587-4 PMID: 28534138
  132. Guru, S.; Kothiwale, S.; Saroch, N.; Guru, R. Comparative evaluation of inhibitory effect of curcumin and doxycycline on matrix metalloproteinase-9 activity in chronic periodontitis. Indian J. Dent. Res., 2017, 28(5), 560-565. doi: 10.4103/ijdr.IJDR_461_16 PMID: 29072221
  133. Martins, C.A.; Leyhausen, G.; Volk, J.; Geurtsen, W. Curcumin in combination with piperine suppresses osteoclastogenesis in vitro. J. Endod., 2015, 41(10), 1638-1645. doi: 10.1016/j.joen.2015.05.009 PMID: 26300429
  134. de Almeida Brandão, D.; Spolidorio, L.C.; Johnson, F.; Golub, L.M.; Guimarães-Stabili, M.R.; Rossa, C., Jr Dose-response assessment of chemically modified curcumin in experimental periodontitis. J. Periodontol., 2019, 90(5), 535-545. doi: 10.1002/JPER.18-0392 PMID: 30394523
  135. Guimarães, M.R.; de Aquino, S.G.; Coimbra, L.S.; Spolidorio, L.C.; Kirkwood, K.L.; Rossa, C., Jr. Curcumin modulates the immune response associated with LPS-induced periodontal disease in rats. Innate Immun., 2012, 18(1), 155-163. doi: 10.1177/1753425910392935 PMID: 21242275
  136. Curylofo-Zotti, F.A.; Elburki, M.S.; Oliveira, P.A.; Cerri, P.S.; Santos, L.A.; Lee, H.M.; Johnson, F.; Golub, L.M.; Rossa, C.; Guimarães-Stabili, M.R. Differential effects of natural Curcumin and chemically modified curcumin on inflammation and bone resorption in model of experimental periodontitis. Arch. Oral Biol., 2018, 91, 42-50. doi: 10.1016/j.archoralbio.2018.04.007 PMID: 29669267
  137. Zambrano, L.M.G.; Brandao, D.A.; Rocha, F.R.G.; Marsiglio, R.P.; Longo, I.B.; Primo, F.L.; Tedesco, A.C.; Guimaraes-Stabili, M.R.; Rossa Junior, C. Local administration of curcumin-loaded nanoparticles effectively inhibits inflammation and bone resorption associated with experimental periodontal disease. Sci. Rep., 2018, 8(1), 6652. doi: 10.1038/s41598-018-24866-2 PMID: 29703905
  138. Mazzarino, L.; Borsali, R.; Lemos-Senna, E. Mucoadhesive films containing chitosan-coated nanoparticles: a new strategy for buccal curcumin release. J. Pharm. Sci., 2014, 103(11), 3764-3771. doi: 10.1002/jps.24142 PMID: 25187001
  139. Carbinatto, F.M.; Ribeiro, T.S.; Colnago, L.A.; Evangelista, R.C.; Cury, B.S.F. Preparation and characterization of amylose inclusion complexes for drug delivery applications. J. Pharm. Sci., 2016, 105(1), 231-241. doi: 10.1002/jps.24702 PMID: 26579874
  140. Nasra, M.M.A.; Khiri, H.M.; Hazzah, H.A.; Abdallah, O.Y. Formulation, in-vitro characterization and clinical evaluation of curcumin in-situ gel for treatment of periodontitis. Drug Deliv., 2017, 24(1), 133-142. doi: 10.1080/10717544.2016.1233591 PMID: 28156166
  141. Franck, F.C.; Benatti, B.B.; Andia, D.C.; Cirano, F.R.; Casarin, R.C.; Corrêa, M.G.; Ribeiro, F.V. Impact of resveratrol on bone repair in rats exposed to cigarette smoke inhalation: histomorphometric and bone-related gene expression analysis. Int. J. Oral Maxillofac. Surg., 2018, 47(4), 541-548. doi: 10.1016/j.ijom.2017.08.004 PMID: 28927744
  142. Ikeda, E.; Ikeda, Y.; Wang, Y.; Fine, N.; Sheikh, Z.; Viniegra, A.; Barzilay, O.; Ganss, B.; Tenenbaum, H.C.; Glogauer, M. Resveratrol derivative-rich melinjo seed extract induces healing in a murine model of established periodontitis. J. Periodontol., 2018, 89(5), 586-595. doi: 10.1002/JPER.17-0352 PMID: 29856488
  143. Orihuela-Campos, R.C.; Tamaki, N.; Mukai, R.; Fukui, M.; Miki, K.; Terao, J.; Ito, H.O. Biological impacts of resveratrol, quercetin, and N-acetylcysteine on oxidative stress in human gingival fibroblasts. J. Clin. Biochem. Nutr., 2015, 56(3), 220-227. doi: 10.3164/jcbn.14-129 PMID: 26060353
  144. Bhattarai, G.; Poudel, S.B.; Kook, S.H.; Lee, J.C. Resveratrol prevents alveolar bone loss in an experimental rat model of periodontitis. Acta Biomater., 2016, 29, 398-408. doi: 10.1016/j.actbio.2015.10.031 PMID: 26497626
  145. Rizzo, A.; Bevilacqua, N.; Guida, L.; Annunziata, M.; Romano Carratelli, C.; Paolillo, R. Effect of resveratrol and modulation of cytokine production on human periodontal ligament cells. Cytokine, 2012, 60(1), 197-204. doi: 10.1016/j.cyto.2012.06.004 PMID: 22749236
  146. Wadhwa, D.; Bey, A.; Hasija, M.; Moin, S.; Kumar, A.; Aman, S.; Sharma, V.K. Determination of levels of nitric oxide in smoker and nonsmoker patients with chronic periodontitis. J. Periodontal Implant Sci., 2013, 43(5), 215-220. doi: 10.5051/jpis.2013.43.5.215 PMID: 24236243
  147. Casati, M.Z.; Algayer, C.; Cardoso da Cruz, G.; Ribeiro, F.V.; Casarin, R.C.V.; Pimentel, S.P.; Cirano, F.R. Resveratrol decreases periodontal breakdown and modulates local levels of cytokines during periodontitis in rats. J. Periodontol., 2013, 84(10), e58-e64. doi: 10.1902/jop.2013.120746 PMID: 23489233
  148. Cirano, F.R.; Casarin, R.C.V.; Ribeiro, F.V.; Casati, M.Z.; Pimentel, S.P.; Taiete, T.; Bernardi, M.M. Effect of Resveratrol on periodontal pathogens during experimental periodontitis in rats. Braz. Oral Res., 2016, 30(1), e128. doi: 10.1590/1807-3107bor-2016.vol30.0128 PMID: 27901209
  149. Ornstrup, M.J.; Harsløf, T.; Sørensen, L.; Stenkjær, L.; Langdahl, B.L.; Pedersen, S.B. Resveratrol increases osteoblast differentiation in vitro independently of inflammation. Calcif. Tissue Int., 2016, 99(2), 155-163. doi: 10.1007/s00223-016-0130-x PMID: 27000750
  150. Tamaki, N.; Cristina Orihuela-Campos, R.; Inagaki, Y.; Fukui, M.; Nagata, T.; Ito, H.O. Resveratrol improves oxidative stress and prevents the progression of periodontitis via the activation of the Sirt1/AMPK and the Nrf2/antioxidant defense pathways in a rat periodontitis model. Free Radic. Biol. Med., 2014, 75, 222-229. doi: 10.1016/j.freeradbiomed.2014.07.034 PMID: 25091897
  151. Ribeiro, I.M.; de Souza Barroso, M.E.; Kampke, E.H.; Braga, L.T.F.; Campagnaro, B.P.; Meyrelles, S.S. Infrared laser therapy decreases systemic oxidative stress and inflammation in hypercholesterolemic mice with periodontitis. Lipids Health Dis., 2023, 22(1), 171. doi: 10.1186/s12944-023-01934-9 PMID: 37817126
  152. Bao, X.; Zhao, J.; Sun, J.; Hu, M.; Yang, X. Polydopamine nanoparticles as efficient scavengers for reactive oxygen species in periodontal disease. ACS Nano, 2018, 12(9), 8882-8892. doi: 10.1021/acsnano.8b04022 PMID: 30028940
  153. Higuchi, J.; Fortunato, G.; Woźniak, B.; Chodara, A.; Domaschke, S.; Męczyńska-Wielgosz, S.; Kruszewski, M.; Dommann, A.; Łojkowski, W. Polymer membranes sonocoated and electrosprayed with nano-hydroxyapatite for periodontal tissues regeneration. Nanomaterials (Basel), 2019, 9(11), 1625. doi: 10.3390/nano9111625 PMID: 31731775
  154. Kahraman, E.; ÿzhan, G.; ÿzsoy, Y.; Güngör, S. Polymeric micellar nanocarriers of benzoyl peroxide as potential follicular targeting approach for acne treatment. Colloids Surf. B Biointerfaces, 2016, 146, 692-699. doi: 10.1016/j.colsurfb.2016.07.029 PMID: 27434156
  155. Bhattarai, G.; Poudel, S.B.; Kook, S.H.; Lee, J.C. Anti-inflammatory, anti-osteoclastic, and antioxidant activities of genistein protect against alveolar bone loss and periodontal tissue degradation in a mouse model of periodontitis. J. Biomed. Mater. Res. A, 2017, 105(9), 2510-2521. doi: 10.1002/jbm.a.36109 PMID: 28509410
  156. Murgia, D.; Angellotti, G.; D’Agostino, F.; De Caro, V. Bioadhesive matrix tablets loaded with lipophilic nanoparticles as vehicles for drugs for periodontitis treatment: development and characterization. Polymers (Basel), 2019, 11(11), 1801. doi: 10.3390/polym11111801 PMID: 31684081
  157. Goyal, G.; Garg, T.; Rath, G.; Goyal, A.K. Current nanotechnological strategies for an effective delivery of drugs in treatment of periodontal disease. Crit. Rev. Ther. Drug Carrier Syst., 2014, 31(2), 89-119. doi: 10.1615/CritRevTherDrugCarrierSyst.2014008117 PMID: 24940625
  158. Shaheen, M.A.; Elmeadawy, S.H.; Bazeed, F.B.; Anees, M.M.; Saleh, N.M. Innovative coenzyme Q10-loaded nanoformulation as an adjunct approach for the management of moderate periodontitis: preparation, evaluation, and clinical study. Drug Deliv. Transl. Res., 2020, 10(2), 548-564. doi: 10.1007/s13346-019-00698-z PMID: 31953677
  159. Alvarez Echazú, M.I.; Olivetti, C.E.; Peralta, I.; Alonso, M.R.; Anesini, C.; Perez, C.J.; Alvarez, G.S.; Desimone, M.F. Development of pH-responsive biopolymer-silica composites loaded with Larrea divaricata Cav. extract with antioxidant activity. Colloids Surf. B Biointerfaces, 2018, 169, 82-91. doi: 10.1016/j.colsurfb.2018.05.015 PMID: 29751344
  160. Saita, M.; Kaneko, J.; Sato, T.; Takahashi, S.; Wada-Takahashi, S.; Kawamata, R.; Sakurai, T.; Lee, M.C.; Hamada, N.; Kimoto, K.; Nagasaki, Y. 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 PMID: 26559357
  161. Mills, M.P.; Rosen, P.S.; Chambrone, L.; Greenwell, H.; Kao, R.T.; Klokkevold, P.R.; McAllister, B.S.; Reynolds, M.A.; Romanos, G.E.; Wang, H.L. American Academy of Periodontology best evidence consensus statement on the efficacy of laser therapy used alone or as an adjunct to non-surgical and surgical treatment of periodontitis and peri-implant diseases. J. Periodontol., 2018, 89(7), 737-742. doi: 10.1002/JPER.17-0356 PMID: 29693260
  162. Santos, M.A.F.M.; Silva, D.N.; Rovaris, K.; Sousa, F.B.; Dantas, E.L.A.; Loureiro, L.A.; Pereira, T.M.C.; Meyrelles, S.S.; Bertollo, R.M.; Vasquez, E.C. Optimal parameters of laser therapy to improve critical calvarial defects. Front. Physiol., 2022, 13, 841146. doi: 10.3389/fphys.2022.841146 PMID: 35283760
  163. Marques, M.M.; Pereira, A.N.; Fujihara, N.A.; Nogueira, F.N.; Eduardo, C.P. Effect of low-power laser irradiation on protein synthesis and ultrastructure of human gingival fibroblasts. Lasers Surg. Med., 2004, 34(3), 260-265. doi: 10.1002/lsm.20008 PMID: 15022254
  164. R Hamblin, M. Mechanisms and applications of the anti-inflammatory effects of photobiomodulation. AIMS Biophys., 2017, 4(3), 337-361. doi: 10.3934/biophy.2017.3.337 PMID: 28748217
  165. Karu, T.I. Low-power laser therapy. In: Biomedical Photonics Handbook, 1st ed; Vo-Dinh, T., Ed.; CRC Press: Boca Raton, FL, 2003; pp. 1-25. doi: 10.1201/9780203008997.ch48

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