Inhibition of Porphyromonas gingivalis by hydrophilic titanium surface modified with cinnamaldehyde

doi:10.12337/zgkqzzxzz.2023.12.004

Abstract

Abstract: Objective Mechanical debridement exhibits a poor prognosis in the treatment of peri-implantitis, necessitating the adjunctive use of local antimicrobial agents. Cinnamaldehyde (CA) possesses antimicrobial properties, yet its application in peri-implantitis remains unclear. This study aimed to investigate the inhibitory effects of cinnamaldehyde on the primary pathogen, Porphyromonas gingivalis (P.gingivalis), in peri-implantitis. Furthermore, the study explored the loading of cinnamaldehyde onto titanium surfaces through plasma plus alkali and heat treatment for potential in vivo applications. Methods The minimum inhibitory concentration (MIC) and minimum bactericidal concentration (MBC) of cinnamaldehyde on P.gingivalis were determined by serial dilution. Its impact on gingipain activity of P.gingivalis was evaluated. Subsequently, titanium surfaces were subjected to alkali and heat treatment combined with or without plasma treatment to assess its hydrophilicity, drug-loading capacity, and sustained release of cinnamaldehyde. P.gingivalis cultures on differently treated titanium surfaces were examined for antimicrobial properties. Results The MIC and MBC of cinnamaldehyde on P.gingivalis were found to be 21.12 μg/mL and 42.24 μg/mL, respectively. Cinnamaldehyde at 1/2 and 1/4 MIC significantly inhibited the gingipain produced by P.gingivalis. Alkali and heat treatment with or without plasma treatment significantly enhanced the hydrophilicity of titanium surfaces and facilitated cinnamaldehyde loading, exerting inhibitory effects on the adhesion and growth of P.gingivalis. The composite treatment outperformed the alkali and heat treatment alone in terms of loading capacity and antimicrobial efficacy on P.gingivalis. Conclusion Cinnamaldehyde effectively inhibits the growth and virulence of P.gingivalis. Plasma-alkali composite treatment enables successful loading of cinnamaldehyde, augmenting the antibacterial properties of titanium surfaces and offering promise for peri-implantitis prevention and therapy.

Key words: Peri-implantitis, Cinnamaldehyde, Alkali and heat treatment, Plasma, Porphyromonas gingivalis

Ou Yanjing, Lu Jie, Chen Jiang. Inhibition of Porphyromonas gingivalis by hydrophilic titanium surface modified with cinnamaldehyde[J]. Chinese Journal of Oral Implantology, 2023, 28(6): 410-416.

References

[1] Sailer I, Karasan D, Todorovic A, et al.Prosthetic failures in dental implant therapy[J]. Periodontol 2000, 2022,88(1):130-144. DOI: 10.1111/prd.12416.
[2] Fu JH, Wang HL.Breaking the wave of peri-implantitis[J]. Periodontol 2000, 2020,84(1):145-160. DOI: 10.1111/prd.12335.
[3] Yan Y, Orlandi M, Suvan J, et al.Association between peri-implantitis and systemic inflammation: a systematic review[J]. Front Immunol, 2023,14:1235155. DOI: 10.3389/fimmu.2023.1235155.
[4] Zheng S, Yu S, Fan X, et al.Porphyromonas gingivalis survival skills: immune evasion[J]. J Periodontal Res, 2021,56(6):1007-1018. DOI: 10.1111/jre.12915.
[5] Zhu R, Liu H, Liu C, et al.Cinnamaldehyde in diabetes: a review of pharmacology, pharmacokinetics and safety[J]. Pharmacol Res, 2017,122:78-89. DOI: 10.1016/j.phrs.2017.05.019.
[6] He Z, Jiang W, Jiang Y, et al.Anti-biofilm activities of coumarin as quorum sensing inhibitor for Porphyromonas gingivalis[J]. J Oral Microbiol, 2022,14(1):2055523. DOI: 10.1080/20002297.2022.2055523.
[7] He Z, Zhang X, Song Z, et al.Quercetin inhibits virulence properties of Porphyromas gingivalis in periodontal disease[J]. Sci Rep, 2020,10(1):18313. DOI: 10.1038/s41598-020-74977-y.
[8] Jun HK, An SJ, Kim HY, et al.Inflammatory response of uric acid produced by Porphyromonas gingivalis gingipains[J]. Mol Oral Microbiol, 2020,35(5):222-230. DOI: 10.1111/omi.12309.
[9] Koyanagi T, Sakamoto M, Takeuchi Y, et al.Comprehensive microbiological findings in peri-implantitis and periodontitis[J]. J Clin Periodontol, 2013,40(3):218-226. DOI: 10.1111/jcpe.12047.
[10] He Z, Huang Z, Jiang W, et al.Antimicrobial activity of cinnamaldehyde on Streptococcus mutans biofilms[J]. Front Microbiol, 2019,10:2241. DOI: 10.3389/fmicb.2019.02241.
[11] Gill AO, Holley RA.Mechanisms of bactericidal action of cinnamaldehyde against Listeria monocytogenes and of eugenol against L. monocytogenes and Lactobacillus sakei[J]. Appl Environ Microbiol, 2004,70(10):5750-5755. DOI: 10.1128/AEM.70.10.5750-5755.2004.
[12] Abdelhamid SM, Edris AE, Sadek Z.Novel approach for the inhibition of Helicobacter pylori contamination in yogurt using selected probiotics combined with eugenol and cinnamaldehyde nanoemulsions[J]. Food Chem, 2023,417:135877. DOI: 10.1016/j.foodchem.2023.135877.
[13] Shreaz S, Wani WA, Behbehani JM, et al.Cinnamaldehyde and its derivatives, a novel class of antifungal agents[J]. Fitoterapia, 2016,112:116-131. DOI: 10.1016/j.fitote.2016.05.016.
[14] Wang Y, Zhang Y, Shi YQ, et al.Antibacterial effects of cinnamon (Cinnamomum zeylanicum) bark essential oil on Porphyromonas gingivalis[J]. Microb Pathog, 2018,116:26-32. DOI: 10.1016/j.micpath.2018.01.009.
[15] Guggenheim B. Oral microbiology and general immunology. Elaboration of principles of the etiology of common diseases of the mouth. Conversation with Prof. Dr. B. Guggenheim[J]. Swiss Dent, 1983,4(5):6-8, 11, 14-16.
[16] Vasconcelos NG, Croda J, Simionatto S.Antibacterial mechanisms of cinnamon and its constituents: a review[J]. Microb Pathog, 2018,120:198-203. DOI: 10.1016/j.micpath.2018.04.036.
[17] Popadiak K, Potempa J, Riesbeck K, et al.Biphasic effect of gingipains from Porphyromonas gingivalis on the human complement system[J]. J Immunol, 2007,178(11):7242-7250. DOI: 10.4049/jimmunol.178.11.7242.
[18] Sabbagh MN, Decourt B.COR388 (atuzaginstat): an investigational gingipain inhibitor for the treatment of Alzheimer disease[J]. Expert Opin Investig Drugs, 2022,31(10):987-993. DOI: 10.1080/13543784.2022.2117605.
[19] Potineni RV, Peterson DG.Mechanisms of flavor release in chewing gum: cinnamaldehyde[J]. J Agric Food Chem, 2008,56(9):3260-3267. DOI: 10.1021/jf0727847.
[20] Wang CX, Wang M, Zhou X.Nucleation and growth of apatite on chemically treated titanium alloy: an electrochemical impedance spectroscopy study[J]. Biomaterials, 2003,24(18):3069-3077. DOI: 10.1016/s0142-9612(03)00154-6.
[21] Camargo WA, Takemoto S, Hoekstra JW, et al.Effect of surface alkali-based treatment of titanium implants on ability to promote in vitro mineralization and in vivo bone formation[J]. Acta Biomater, 2017,57:511-523. DOI: 10.1016/j.actbio.2017.05.016.
[22] Abdelrahim RA, Badr NA, Baroudi K.Effect of anodization and alkali-heat treatment on the bioactivity of titanium implant material (an in vitro study)[J]. J Int Soc Prev Community Dent, 2016,6(3):189-195. DOI: 10.4103/2231-0762.183107.
[23] Snoeckx R, Bogaerts A.Plasma technology-a novel solution for CO₂ conversion?[J]. Chem Soc Rev, 2017,46(19):5805-5863. DOI: 10.1039/c6cs00066e.
[24] Henningsen A, Smeets R, Hartjen P, et al.Photofunctionalization and non-thermal plasma activation of titanium surfaces[J]. Clin Oral Investig, 2018,22(2):1045-1054. DOI: 10.1007/s00784-017-2186-z.
[25] Jeong WS, Kwon JS, Choi EH, et al.The effects of non-thermal atmospheric pressure plasma treated Titanium surface on behaviors of oral soft tissue cells[J]. Sci Rep, 2018,8(1):15963. DOI: 10.1038/s41598-018-34402-x.
[26] Liu H, Xiao J, Zhong W, et al.“In vitro”behavior of bacteria on fluoride ion-corted titanium: with special regands on Porphyromonas gingivalis[J]. Journal of Hard Tissue Biology, 2011,20(1):47-52.DOI:10.2485/jhtb.20.47.