DOI QR코드

DOI QR Code

Effect of Sub-minimal Inhibitory Concentration of Chlorhexidine on Biofilm Formation and Coaggregation of Early Colonizers, Streptococci and Actinomycetes

  • Lee, So Yeon (Department of Oral Microbiology, College of Dentistry, Research Institute of Oral Science, Gangneung-Wonju National University) ;
  • Lee, Si Young (Department of Oral Microbiology, College of Dentistry, Research Institute of Oral Science, Gangneung-Wonju National University)
  • Received : 2016.10.14
  • Accepted : 2016.11.19
  • Published : 2016.12.31

Abstract

Chlorhexidine has long been used in mouth washes for the control of dental caries, gingivitis and dental plaque. Minimal inhibitory concentration (MIC) is the lowest concentration of an antimicrobial substance to inhibit the growth of bacteria. Concentrations lower than the MIC are called sub minimal inhibitory concentrations (sub-MICs). Many studies have reported that sub-MICs of antimicrobial substances can affect the virulence of bacteria. The aim of this study was to investigate the effect of sub-MIC chlorhexidine on biofilm formation and coaggregation of oral early colonizers, such as Streptococcus gordonii, Actinomyces naeslundii and Actinomyces odontolyticus. The biofilm formation of S. gordonii, A. naeslundii and A. odontolyticus was not affected by sub-MIC chlorhexidine. However, the biofilm formation of S. mutans increased after incubation with sub-MIC chlorhexidine. In addition, cell surface hydrophobicity of S. mutans treated with sub-MIC of chlorhexidine, decreased when compared with the group not treated with chlorhexidine. However, significant differences were seen with other bacteria. Coaggregation of A. naeslundii with A. odontolyticus reduced by sub-MIC chlorhexidine, whereas the coaggreagation of A. naeslundii with S. gordonii remained unaffected. These results indicate that sub-MIC chlorhexidine could influence the binding properties, such as biofilm formation, hydrophobicity and coaggregation, in early colonizing streptococci and actinomycetes.

Keywords

References

  1. Addy M, Slayne MA, Wade WG. The formation and control of dental plaque--an overview. J Appl Bacteriol. 1992;73:269-278. https://doi.org/10.1111/j.1365-2672.1992.tb04977.x
  2. Braga PC, Sasso MD, Sala MT. Sub-MIC concentrations of cefodizime interfere with various factors affecting bacterial virulence. J Antimicrob Chemother. 2000;45:15-25. doi: 10.1093/jac/45.1.15
  3. Lorian V. Medical relevance of low concentrations of antibiotics. J Antimicrob Chemother. 1993;31 Suppl D:137-148. doi: 10.1093/jac/31.suppl_D.137
  4. Fonseca AP, Extremina C, Fonseca AF, Sousa JC. Effect of subinhibitory concentration of piperacillin/tazobactam on Pseudomonas aeruginosa. J Med Microbiol. 2004;53:903-910. doi: 10.1099/jmm.0.45637-0
  5. Lorian V, Atkinson B. Abnormal forms of bacteria produced by antibiotics. Am J Clin Pathol. 1975;64:678-688. https://doi.org/10.1093/ajcp/64.5.678
  6. Raponi G, Keller N, Overbeek BP, Rozenberg-Arska M, van Kessel KP, Verhoef J. Enhanced phagocytosis of encapsulated Escherichia coli strains after exposure to sub-MICs of antibiotics is correlated to changes of the bacterial cell surface. Antimicrob Agents Chemother. 1990;34:332-336. doi: 10.1128/AAC.34.2.332
  7. Chopra I, Linton A. The antibacterial effects of low concentrations of antibiotics. Adv Microb Physiol. 1986;28:211-259.
  8. Marsh PD. Microbiological aspects of the chemical control of plaque and gingivitis. J Dent Res. 1992;71:1431-1438. doi: 10.1177/00220345920710071501
  9. Mandel ID. Chemotherapeutic agents for controlling plaque and gingivitis. J Clin Periodontol. 1988;15:488-498. doi: 10.1111/j.1600-051X.1988.tb01020.x
  10. Hjeljord LG, Rolla G, Bonesvoll P. Chlorhexidine-protein interactions. J Periodontal Res Suppl. 1973;12:11-16.
  11. Hugo WB, Longworth AR. Some aspects of the mode of action of chlorhexidine. J Pharm Pharmacol. 1964;16:655-662. doi: 10.1111/j.2042-7158.1964.tb07384.x
  12. Freitas LB, Rundegren J, Arnebrant T. The binding of delmopinol and chlorhexidine to Streptococcus mutans and Actinobacillus actinomycetemcomitans strains with varying degrees of surface hydrophobicity. Oral Microbiol Immunol. 1993;8:355-360. doi: 10.1111/j.1399-302X.1993.tb00611.x
  13. Freitas LB, Vassilakos N, Arnebrant T. Interactions of chlorhexidine with salivary films adsorbed at solid/liquid and air/liquid interfaces. J Periodontal Res. 1993;28:92-97. doi: 10.1111/j.1600-0765.1993.tb01055.x
  14. Gisselsson H, Birkhed D, Bjorn AL. Effect of professional flossing with chlorhexidine gel on approximal caries in 12- to 15-year-old schoolchildren. Caries Res. 1988;22:187-192. https://doi.org/10.1159/000261104
  15. Freitas LB, Vassilakos N, Arnebrant T. Interactions of chlorhexidine with salivary films adsorbed at solid/liquid and air/liquid interfaces. J Periodontal Res. 1993;28:92-97. doi: 10.1111/j.1600-0765.1993.tb01055.x
  16. Hope CK, Wilson M. Analysis of the effects of chlorhexidine on oral biofilm vitality and structure based on viability profiling and an indicator of membrane integrity. Antimicrob Agents Chemother. 2004;48:1461-1468. doi: 10.1128/AAC.48.5.1461-1468.2004
  17. Meurman JH. Ultrastructure, growth, and adherence of Streptococcus mutans after treatment with chlorhexidine and fluoride. Caries Res. 1988;22:283-287. https://doi.org/10.1159/000261122
  18. Dong L, Tong Z, Linghu D, Lin Y, Tao R, Liu J, Tian Y, Ni L. Effects of sub-minimum inhibitory concentrations of antimicrobial agents on Streptococcus mutans biofilm formation. Int J Antimicrob Agents. 2012;39:390-395. doi: 10.1016/j.ijantimicag.2012.01.009.
  19. Kolenbrander PE, London J. Adhere today, here tomorrow: Oral bacterial adherence. J Bacteriol. 1993;175:3247-3252. https://doi.org/10.1128/jb.175.11.3247-3252.1993
  20. Gibbons RJ, Nygaard M. Interbacterial aggregation of plaque bacteria. Arch Oral Biol. 1970;15:1397-1400. https://doi.org/10.1016/0003-9969(70)90031-2
  21. Ledder RG, Timperley AS, Friswell MK, Macfarlane S, McBain AJ. Coaggregation between and among human intestinal and oral bacteria. FEMS Microbiol Ecol. 2008;66:630-636. doi: 10.1111/j.1574-6941.2008.00525.x.
  22. Smith RN, Andersen RN, Kolenbrander PE. Inhibition of intergeneric coaggregation among oral bacteria by cetylpyridinium chloride, chlorhexidine digluconate and octenidine dihydrochloride. J Periodontal Res. 1991;26:422-428. doi: 10.1111/j.1600-0765.1991.tb01732.x
  23. Clinical and Laboratory Standards Institute. Methods for dilution antimicrobial susceptibility tests for bacteria that grow aerobically, M07-A8, vol.29, no.2, 8th ed., CLSI. Wayne, PA, 2009.
  24. Park JH, Lee JK, Um HS, Chang BS, Lee SY. A periodontitis-associated multispecies model of an oral biofilm. J Periodontal Implant Sci. 2014;44:79-84. doi: 10.5051/jpis.2014.44.2.79.
  25. Lee SY, Kim YJ, Kim KK, Choe SJ. Effects of subinhibitory antibiotic concentrations on Porphyromonas gingivalis fibrinogen and hemin binding. Intern J Oral Biol. 1999;24:121-127.
  26. Hamada N, Watanabe K, Sasakawa C, Yoshikawa M, Yoshimura F, Umemoto T. Construction and characterization of a fimA mutant of Porphyromonas gingivalis. Infect Immun. 1994;62:1696-1704.
  27. Lee SY, Lee SY. Effect of sub-minimal inhibitory concentrations of antibiotics on biofilm formation and coaggregation of streptococci and actinomycetes. Intern J Oral Biol. 2015;40:189-196. https://doi.org/10.11620/IJOB.2015.40.4.189
  28. Lee SY. Effects of chlorhexidine digluconate and hydrogen peroxide on Porphyromonas gingivalis hemin binding and coaggregation with oral streptococci. J Oral Sci. 2001;43:1-7. https://doi.org/10.2334/josnusd.43.1
  29. Cisar JO, Kolenbrander PE, McIntire FC. Specificity of coaggregation reactions between human oral streptococci and strains of Actinomyces viscosus or Actinomyces naeslundii. Infect Immun. 1979;24:742-752.
  30. Kara D, Luppens SB, Cate JM. Differences between single- and dual-species biofilms of Streptococcus mutans and Veillonella parvula in growth, acidogenicity and susceptibility to chlorhexidine. Eur J Oral Sci. 2006;114:58-63. doi: 10.1111/j.1600-0722.2006.00262.x
  31. Jones CG. Chlorhexidine: Is it still the gold standard? Periodontol 2000. 1997;15:55-62. https://doi.org/10.1111/j.1600-0757.1997.tb00105.x
  32. Bonesvoll P, Lokken P, Rolla G, Paus PN. Retention of chlorhexidine in the human oral cavity after mouth rinses. Arch Oral Biol. 1974;19:209-212. https://doi.org/10.1016/0003-9969(74)90263-5
  33. Ellepola AN, Samaranayake LP. The effect of limited exposure to Antimycotics on the relative cell-surface hydrophobicity and the adhesion of oral Candida albicans to buccal epithelial cells. Arch Oral Biol. 1998;43:879-887. https://doi.org/10.1016/S0003-9969(98)00064-8
  34. Gibbons RJ, Etherden I. Comparative hydrophobicities of oral bacteria and their adherence to salivary pellicles. Infect Immun. 1983;41:1190-1196.
  35. Ana C. Okamoto, Elerson Gaetti-Jardim Jr., Victor E. Arana-Chavez, Mario J. Avila-Campos. Influence of subinhibitory concentrations of antimicrobials on hydrophobicity, adherence and ultra-structure of Fusobacterium nucleatum. Braz J Microbiol. 2002;33:178-184. https://doi.org/10.1590/S1517-83822002000200017
  36. Cai S, Simionato MR, Mayer MP, Novo NF, Zelante F. Effects of subinhibitory concentrations of chemical agents on hydrophobicity and in vitro adherence of Streptococcus mutans and Streptococcus sanguis. Caries Res. 1994;28:335-341. https://doi.org/10.1159/000261998
  37. Kolenbrander, P. E., London, J. Ecological significance of coaggregation among oral bacteria. Adv Microb Ecol. 1992;12:183-217.