Endodontic biofilms: contemporary and future treatment options |
Yoo, Yeon-Jee
(Department of Conservative Dentistry, Dental Research Institute, School of Dentistry, Seoul National University)
Perinpanayagam, Hiran (Division of Restorative Dentistry, Schulich School of Medicine & Dentistry, University of Western Ontario) Oh, Soram (Department of Conservative Dentistry, School of Dentistry, Kyung Hee University) Kim, A-Reum (Department of Oral Microbiology and Immunology, Dental Research Institute and BK21 Plus Program, School of Dentistry, Seoul National University) Han, Seung-Hyun (Department of Oral Microbiology and Immunology, Dental Research Institute and BK21 Plus Program, School of Dentistry, Seoul National University) Kum, Kee-Yeon (Department of Conservative Dentistry, Dental Research Institute, School of Dentistry, Seoul National University) |
1 | Dai T, Huang YY, Hamblin MR. Photodynamic therapy for localized infections--state of the art. Photodiagnosis Photodyn Ther 2009;6:170-188. DOI |
2 | Meire MA, De Prijck K, Coenye T, Nelis HJ, De Moor RJ. Effectiveness of different laser systems to kill Enterococcus faecalis in aqueous suspension and in an infected tooth model. Int Endod J 2009;42:351-359. DOI |
3 | George S, Kishen A. Photophysical, photochemical, and photobiological characterization of methylene blue formulations for light-activated root canal disinfection. J Biomed Opt 2007;12:034029. DOI |
4 | Basrani B, Santos JM, Tjaderhane L, Grad H, Gorduysus O, Huang J, Lawrence HP, Friedman S. Substantive antimicrobial activity in chlorhexidine-treated human root dentin. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 2002;94:240-245. DOI |
5 | Baca P, Junco P, Arias-Moliz MT, Castillo F, Rodriguez-Archilla A, Ferrer-Luque CM. Antimicrobial substantivity over time of chlorhexidine and cetrimide. J Endod 2012;38:927-930. DOI |
6 | Mohammadi Z, Abbott PV. The properties and applications of chlorhexidine in endodontics. Int Endod J 2009;42:288-302. DOI |
7 | Gomes BP, Ferraz CC, Vianna ME, Berber VB, Teixeira FB, Souza-Filho FJ. In vitro antimicrobial activity of several concentrations of sodium hypochlorite and chlorhexidine gluconate in the elimination of Enterococcus faecalis. Int Endod J 2001;34:424-428. DOI |
8 | Lee JK, Baik JE, Yun CH, Lee K, Han SH, Lee W, Bae KS, Baek SH, Lee Y, Son WJ, Kum KY. Chlorhexidine gluconate attenuates the ability of lipoteichoic acid from Enterococcus faecalis to stimulate toll-like receptor 2. J Endod 2009;35:212-215. DOI |
9 | Kim HS, Woo Chang S, Baek SH, Han SH, Lee Y, Zhu Q, Kum KY. Antimicrobial effect of alexidine and chlorhexidine against Enterococcus faecalis infection. Int J Oral Sci 2013;5:26-31. DOI |
10 | Ozdemir HO, Buzoglu HD, Calt S, Stabholz A, Steinberg D. Effect of ethylenediaminetetraacetic acid and sodium hypochlorite irrigation on Enterococcus faecalis biofilm colonization in young and old human root canal dentin: in vitro study. J Endod 2010;36:842-846. DOI |
11 | Azarpazhooh A, Limeback H. The application of ozone in dentistry: a systematic review of literature. J Dent 2008;36:104-116. DOI |
12 | Soares JA, Roque de Carvalho MA, Cunha Santos SM, Mendonca RM, Ribeiro-Sobrinho AP, Brito-Junior M, Magalhaes PP, Santos MH, de Macedo Farias L. Effectiveness of chemomechanical preparation with alternating use of sodium hypochlorite and EDTA in eliminating intracanal Enterococcus faecalis biofilm. J Endod 2010;36:894-898. DOI |
13 | George S, Kishen A. Influence of photosensitizer solvent on the mechanisms of photoactivated killing of Enterococcus faecalis. Photochem Photobiol 2008;84:734-740. DOI |
14 | George S, Kishen A. Augmenting the antibiofilm efficacy of advanced noninvasive light activated disinfection with emulsified oxidizer and oxygen carrier. J Endod 2008;34:1119-1123. DOI |
15 | Soukos NS, Chen PS, Morris JT, Ruggiero K, Abernethy AD, Som S, Foschi F, Doucette S, Bammann LL, Fontana CR, Doukas AG, Stashenko PP. Photodynamic therapy for endodontic disinfection. J Endod 2006;32:979-984. DOI |
16 | Nagayoshi M, Kitamura C, Fukuizumi T, Nishihara T, Terashita M. Antimicrobial effect of ozonated water on bacteria invading dentinal tubules. J Endod 2004;30:778-781. DOI |
17 | Arita M, Nagayoshi M, Fukuizumi T, Okinaga T, Masumi S, Morikawa M, Kakinoki Y, Nishihara T. Microbicidal efficacy of ozonated water against Candida albicans adhering to acrylic denture plates. Oral Microbiol Immunol 2005;20:206-210. DOI |
18 | Hems RS, Gulabivala K, Ng YL, Ready D, Spratt DA. An in vitro evaluation of the ability of ozone to kill a strain of Enterococcus faecalis. Int Endod J 2005;38:22-29. DOI |
19 | Chai WL, Hamimah H, Cheng SC, Sallam AA, Abdullah M. Susceptibility of Enterococcus faecalis biofilm to antibiotics and calcium hydroxide. J Oral Sci 2007;49:161-166. DOI |
20 | Siqueira JF Jr, Lopes HP. Mechanisms of antimicrobial activity of calcium hydroxide: a critical review. Int Endod J 1999;32:361-369. DOI |
21 | Brandle N, Zehnder M, Weiger R, Waltimo T. Impact of growth conditions on susceptibility of five microbial species to alkaline stress. J Endod 2008;34:579-582. DOI |
22 | Baik JE, Jang KS, Kang SS, Yun CH, Lee K, Kim BG, Kum KY, Han SH. Calcium hydroxide inactivates lipoteichoic acid from Enterococcus faecalis through deacylation of the lipid moiety. J Endod 2011;37:191-196. DOI |
23 | Safavi KE, Nichols FC. Effect of calcium hydroxide on bacterial lipopolysaccharide. J Endod 1993;19:76-78. DOI |
24 | Barthel CR, Levin LG, Reisner HM, Trope M. TNF-alpha release in monocytes after exposure to calcium hydroxide treated Escherichia coli LPS. Int Endod J 1997;30:155-159. DOI |
25 | Siqueira JF Jr. Strategies to treat infected root canals. J Calif Dent Assoc 2001;29:825-837. |
26 | Jiang J, Zuo J, Chen SH, Holliday LS. Calcium hydroxide reduces lipopolysaccharide-stimulated osteoclast formation. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 2003;95:348-354. DOI |
27 | Buck RA, Cai J, Eleazer PD, Staat RH, Hurst HE. Detoxification of endotoxin by endodontic irrigants and calcium hydroxide. J Endod 2001;27:325-327. DOI |
28 | Bobichon H, Bouchet P. Action of chlorhexidine on budding Candida albicans: scanning and transmission electron microscopic study. Mycopathologia 1987;100:27-35. DOI |
29 | Krithikadatta J, Indira R, Dorothykalyani AL. Disinfection of dentinal tubules with 2% chlorhexidine, 2% metronidazole, bioactive glass when compared with calcium hydroxide as intracanal medicaments. J Endod 2007;33:1473-1476. DOI |
30 | Yoo YJ, Kwon I, Oh SR, Perinpanayagam H, Lim SM, Ahn KB, Lee Y, Han SH, Chang SW, Baek SH, Zhu Q, Kum KY. Antifungal effects of synthetic human beta-defensin-3-C15 peptide on Candida albicans-infected root dentin. J Endod 2017;43:1857-1861. DOI |
31 | Kara D, Luppens SB, van Marle J, Ozok R, ten Cate JM. Microstructural differences between single-species and dual-species biofilms of Streptococcus mutans and Veillonella parvula, before and after exposure to chlorhexidine. FEMS Microbiol Lett 2007;271:90-97. DOI |
32 | Zasloff M. Antimicrobial peptides of multicellular organisms. Nature 2002;415:389-395. DOI |
33 | Lee SH, Baek DH. Antibacterial and neutralizing effect of human -defensins on Enterococcus faecalis and Enterococcus faecalis lipoteichoic acid. J Endod 2012;38:351-356. DOI |
34 | Selsted ME, Ouellette AJ. Mammalian defensins in the antimicrobial immune response. Nat Immunol 2005;6:551-557. DOI |
35 | Schneider JJ, Unholzer A, Schaller M, Schafer-Korting M, Korting HC. Human defensins. J Mol Med (Berl) 2005;83:587-595. DOI |
36 | Lee SH, Jun HK, Lee HR, Chung CP, Choi BK. Antibacterial and lipopolysaccharide (LPS)-neutralising activity of human cationic antimicrobial peptides against periodontopathogens. Int J Antimicrob Agents 2010;35:138-145. DOI |
37 | Yamaguchi Y, Nagase T, Makita R, Fukuhara S, Tomita T, Tominaga T, Kurihara H, Ouchi Y. Identification of multiple novel epididymis-specific beta-defensin isoforms in humans and mice. J Immunol 2002;169:2516-2523. DOI |
38 | Svensater G, Bergenholtz G. Biofilms in endodontic infections. Endod Topics 2004;9:27-36. DOI |
39 | Siqueira JF Jr, Rocas IN. Clinical implications and microbiology of bacterial persistence after treatment procedures. J Endod 2008;34:1291-1301.e3. DOI |
40 | Chavez de Paz LE. Redefining the persistent infection in root canals: possible role of biofilm communities. J Endod 2007;33:652-662. DOI |
41 | Ingle JI, Bakland LK, Baumgartner JC. Ingle's Endodontics. 6th ed. Lewiston, PA: PMPH-USA; 2008. p268-285. |
42 | Mohammadi Z, Palazzi F, Giardino L, Shalavi S. Microbial biofilms in endodontic infections: an update review. Biomed J 2013;36:59-70. DOI |
43 | Grenier D, Mayrand D. Nutritional relationships between oral bacteria. Infect Immun 1986;53:616-620. DOI |
44 | Costerton JW, Stewart PS, Greenberg EP. Bacterial biofilms: a common cause of persistent infections. Science 1999;284:1318-1322. DOI |
45 | Cowan MM, Taylor KG, Doyle RJ. Energetics of the initial phase of adhesion of Streptococcus sanguis to hydroxylapatite. J Bacteriol 1987;169:2995-3000. DOI |
46 | Nair PN, Henry S, Cano V, Vera J. Microbial status of apical root canal system of human mandibular first molars with primary apical periodontitis after "one-visit" endodontic treatment. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 2005;99:231-252. DOI |
47 | Lim SM, Ahn KB, Kim C, Kum JW, Perinpanayagam H, Gu Y, Yoo YJ, Chang SW, Han SH, Shon WJ, Lee W, Baek SH, Zhu Q, Kum KY. Antifungal effects of synthetic human -defensin 3-C15 peptide. Restor Dent Endod 2016;41:91-97. DOI |
48 | Paris S, Wolgin M, Kielbassa AM, Pries A, Zakrzewicz A. Gene expression of human beta-defensins in healthy and inflamed human dental pulps. J Endod 2009;35:520-523. DOI |
49 | Giacometti A, Cirioni O, Ghiselli R, Mocchegiani F, Del Prete MS, Viticchi C, Kamysz W, LEmpicka E, Saba V, Scalise G. Potential therapeutic role of cationic peptides in three experimental models of septic shock. Antimicrob Agents Chemother 2002;46:2132-2136. DOI |
50 | Ahn KB, Kim AR, Kum KY, Yun CH, Han SH. The synthetic human beta-defensin-3 C15 peptide exhibits antimicrobial activity against Streptococcus mutans, both alone and in combination with dental disinfectants. J Microbiol 2017;55:830-836. DOI |
51 | Windley W 3rd, Teixeira F, Levin L, Sigurdsson A, Trope M. Disinfection of immature teeth with a triple antibiotic paste. J Endod 2005;31:439-443. DOI |
52 | Hoshino E, Kurihara-Ando N, Sato I, Uematsu H, Sato M, Kota K, Iwaku M. In-vitro antibacterial susceptibility of bacteria taken from infected root dentine to a mixture of ciprofloxacin, metronidazole and minocycline. Int Endod J 1996;29:125-130. DOI |
53 | Sato I, Ando-Kurihara N, Kota K, Iwaku M, Hoshino E. Sterilization of infected root-canal dentine by topical application of a mixture of ciprofloxacin, metronidazole and minocycline in situ. Int Endod J 1996;29:118-124. DOI |
54 | Ordinola-Zapata R, Bramante CM, Minotti PG, Cavenago BC, Garcia RB, Bernardineli N, Jaramillo DE, Hungaro Duarte MA. Antimicrobial activity of triantibiotic paste, 2% chlorhexidine gel, and calcium hydroxide on an intraoral-infected dentin biofilm model. J Endod 2013;39:115-118. DOI |
55 | Dunavant TR, Regan JD, Glickman GN, Solomon ES, Honeyman AL. Comparative evaluation of endodontic irrigants against Enterococcus faecalis biofilms. J Endod 2006;32:527-531. DOI |
56 | Ricucci D, Martorano M, Bate AL, Pascon EA. Calculus-like deposit on the apical external root surface of teeth with post-treatment apical periodontitis: report of two cases. Int Endod J 2005;38:262-271. DOI |
57 | Noiri Y, Ehara A, Kawahara T, Takemura N, Ebisu S. Participation of bacterial biofilms in refractory and chronic periapical periodontitis. J Endod 2002;28:679-683. DOI |
58 | Siqueira JF Jr. Periapical actinomycosis and infection with Propionobacterium propionicum. Endod Topics 2003;6:78-95. DOI |
59 | Figdor D, Sjogren U, Sorlin S, Sundqvist G, Nair PN. Pathogenicity of Actinomyces israelii and Arachnia propionica: experimental infection in guinea pigs and phagocytosis and intracellular killing by human polymorphonuclear leukocytes in vitro. Oral Microbiol Immunol 1992;7:129-136. DOI |
60 | Wilson M. Susceptibility of oral bacterial biofilms to antimicrobial agents. J Med Microbiol 1996;44:79-87. DOI |
61 | Larsen T. Susceptibility of Porphyromonas gingivalis in biofilms to amoxicillin, doxycycline and metronidazole. Oral Microbiol Immunol 2002;17:267-271. DOI |
62 | Portenier I, Waltimo TM, Haapasalo M. Enterococcus faecalis: the root canal survivor and 'star' in post-treatment disease. Endod Topics 2003;6:135-159. DOI |
63 | Athanassiadis B, Abbott PV, Walsh LJ. The use of calcium hydroxide, antibiotics and biocides as antimicrobial medicaments in endodontics. Aust Dent J 2007;52:S64-S82. DOI |
64 | Distel JW, Hatton JF, Gillespie MJ. Biofilm formation in medicated root canals. J Endod 2002;28:689-693. DOI |
65 | Noiri Y, Katsumoto T, Azakami H, Ebisu S. Effects of Er:YAG laser irradiation on biofilm-forming bacteria associated with endodontic pathogens in vitro. J Endod 2008;34:826-829. DOI |
66 | Seal GJ, Ng YL, Spratt D, Bhatti M, Gulabivala K. An in vitro comparison of the bactericidal efficacy of lethal photosensitization or sodium hyphochlorite irrigation on Streptococcus intermedius biofilms in root canals. Int Endod J 2002;35:268-274. DOI |
67 | Araki AT, Ibraki Y, Kawakami T, Lage-Marques JL. Er:Yag laser irradiation of the microbiological apical biofilm. Braz Dent J 2006;17:296-299. DOI |
68 | Bergmans L, Moisiadis P, Teughels W, Van Meerbeek B, Quirynen M, Lambrechts P. Bactericidal effect of Nd:YAG laser irradiation on some endodontic pathogens ex vivo. Int Endod J 2006;39:547-557. DOI |
69 | Isolauri E. Probiotics in human disease. Am J Clin Nutr 2001;73:1142S-1146S. DOI |
70 | Soderling EM, Marttinen AM, Haukioja AL. Probiotic lactobacilli interfere with Streptococcus mutans biofilm formation in vitro. Curr Microbiol 2011;62:618-622. DOI |
71 | Ahn KB, Baik JE, Yun CH, Han SH. Lipoteichoic acid inhibits Staphylococcus aureus biofilm formation. Front Microbiol 2018;9:327. DOI |
72 | Bryce G, O'Donnell D, Ready D, Ng YL, Pratten J, Gulabivala K. Contemporary root canal irrigants are able to disrupt and eradicate single- and dual-species biofilms. J Endod 2009;35:1243-1248. DOI |
73 | Hong SW, Baik JE, Kang SS, Kum KY, Yun CH, Han SH. Sodium hypochlorite inactivates lipoteichoic acid of Enterococcus faecalis by deacylation. J Endod 2016;42:1503-1508. DOI |
74 | Ahn KB, Baik JE, Park OJ, Yun CH, Han SH. Lactobacillus plantarum lipoteichoic acid inhibits biofilm formation of Streptococcus mutans. PLoS One 2018;13:e0192694. DOI |
75 | Jung S, Park OJ, Kim AR, Ahn KB, Lee D, Kum KY, Yun CH, Han SH. Lipoteichoic acids of lactobacilli inhibit Enterococcus faecalis biofilm formation and disrupt the preformed biofilm. J Microbiol 2019 Jan 22. doi: 10.1007/s12275-019-8538-4. [Epub ahead of print] DOI |
76 | Spratt DA, Pratten J, Wilson M, Gulabivala K. An in vitro evaluation of the antimicrobial efficacy of irrigants on biofilms of root canal isolates. Int Endod J 2001;34:300-307. DOI |
77 | Ozok AR, Wu MK, Luppens SB, Wesselink PR. Comparison of growth and susceptibility to sodium hypochlorite of mono- and dual-species biofilms of Fusobacterium nucleatum and Peptostreptococcus (micromonas) micros. J Endod 2007;33:819-822. DOI |
78 | Clegg MS, Vertucci FJ, Walker C, Belanger M, Britto LR. The effect of exposure to irrigant solutions on apical dentin biofilms in vitro. J Endod 2006;32:434-437. DOI |
79 | Giardino L, Ambu E, Savoldi E, Rimondini R, Cassanelli C, Debbia EA. Comparative evaluation of antimicrobial efficacy of sodium hypochlorite, MTAD, and Tetraclean against Enterococcus faecalis biofilm. J Endod 2007;33:852-855. DOI |
80 | Baca P, Junco P, Arias-Moliz MT, Gonzalez-Rodriguez MP, Ferrer-Luque CM. Residual and antimicrobial activity of final irrigation protocols on Enterococcus faecalis biofilm in dentin. J Endod 2011;37:363-366. DOI |
81 | Parsons GJ, Patterson SS, Miller CH, Katz S, Kafrawy AH, Newton CW. Uptake and release of chlorhexidine by bovine pulp and dentin specimens and their subsequent acquisition of antibacterial properties. Oral Surg Oral Med Oral Pathol 1980;49:455-459. DOI |
82 | Beard SJ, Hughes MN, Poole RK. Inhibition of the cytochrome bd-terminated NADH oxidase system in Escherichia coli K-12 by divalent metal cations. FEMS Microbiol Lett 1995;131:205-210. DOI |
83 | Kim AR, Ahn KB, Yoon SH, Yoo YJ, Perinpanayagam H, Kum KY, Han SH. Lactobacillus plantarum lipoteichoic acid inhibits oral multispecies biofilm. J Endod. 2019 Jan. doi: 10.1016/j.joen.2018.12.007. [accepted]. DOI |
84 | Kim JS, Kuk E, Yu KN, Kim JH, Park SJ, Lee HJ, Kim SH, Park YK, Park YH, Hwang CY, Kim YK, Lee YS, Jeong DH, Cho MH. Antimicrobial effects of silver nanoparticles. Nanomedicine (Lond) 2007;3:95-101. DOI |
85 | Sawai J. Quantitative evaluation of antibacterial activities of metallic oxide powders (ZnO, MgO and CaO) by conductimetric assay. J Microbiol Methods 2003;54:177-182. DOI |
86 | Feng QL, Wu J, Chen GQ, Cui FZ, Kim TN, Kim JO. A mechanistic study of the antibacterial effect of silver ions on Escherichia coli and Staphylococcus aureus. J Biomed Mater Res 2000;52:662-668. DOI |
87 | Kishen A, Sum CP, Mathew S, Lim CT. Influence of irrigation regimens on the adherence of Enterococcus faecalis to root canal dentin. J Endod 2008;34:850-854. DOI |