Antimicrobial photodynamic therapy combined with conventional endodontic treatment to eliminate root canal biofilm infection
Aguinaldo S. Garcez DDS
Center for Lasers and Applications, IPEN-CNEN/SP, São Paulo, SP, Brazil
Search for more papers by this authorMartha S. Ribeiro PhD
Center for Lasers and Applications, IPEN-CNEN/SP, São Paulo, SP, Brazil
Search for more papers by this authorGeorge P. Tegos PhD
Wellman Center for Photomedicine, Massachusetts General Hospital, Boston, Massachusetts
Department of Dermatology, Harvard Medical School, Boston, Massachusetts
Search for more papers by this authorSilvia C. Núñez DDS
Center for Lasers and Applications, IPEN-CNEN/SP, São Paulo, SP, Brazil
Search for more papers by this authorAntonio O.C. Jorge PhD
School of Dentistry, Universidade de Taubaté, Taubaté, São Paulo, SP, Brazil
Search for more papers by this authorCorresponding Author
Michael R. Hamblin PhD
Wellman Center for Photomedicine, Massachusetts General Hospital, Boston, Massachusetts
Department of Dermatology, Harvard Medical School, Boston, Massachusetts
Harvard-MIT Division of Health Sciences and Technology, Cambridge, Massachusetts
BAR414, Wellman Center for Photomedicine, Massachusetts General Hospital, 40 Blossom Street, Boston, MA 02114.Search for more papers by this authorAguinaldo S. Garcez DDS
Center for Lasers and Applications, IPEN-CNEN/SP, São Paulo, SP, Brazil
Search for more papers by this authorMartha S. Ribeiro PhD
Center for Lasers and Applications, IPEN-CNEN/SP, São Paulo, SP, Brazil
Search for more papers by this authorGeorge P. Tegos PhD
Wellman Center for Photomedicine, Massachusetts General Hospital, Boston, Massachusetts
Department of Dermatology, Harvard Medical School, Boston, Massachusetts
Search for more papers by this authorSilvia C. Núñez DDS
Center for Lasers and Applications, IPEN-CNEN/SP, São Paulo, SP, Brazil
Search for more papers by this authorAntonio O.C. Jorge PhD
School of Dentistry, Universidade de Taubaté, Taubaté, São Paulo, SP, Brazil
Search for more papers by this authorCorresponding Author
Michael R. Hamblin PhD
Wellman Center for Photomedicine, Massachusetts General Hospital, Boston, Massachusetts
Department of Dermatology, Harvard Medical School, Boston, Massachusetts
Harvard-MIT Division of Health Sciences and Technology, Cambridge, Massachusetts
BAR414, Wellman Center for Photomedicine, Massachusetts General Hospital, 40 Blossom Street, Boston, MA 02114.Search for more papers by this authorAbstract
Background and Objective
To compare the effectiveness of antimicrobial photodynamic therapy (PDT), standard endodontic treatment and the combined treatment to eliminate bacterial biofilms present in infected root canals.
Study Design/Materials and Methods
Ten single-rooted freshly extracted human teeth were inoculated with stable bioluminescent Gram-negative bacteria, Proteus mirabilis and Pseudomonas aeruginosa to form 3-day biofilms in prepared root canals. Bioluminescence imaging was used to serially quantify bacterial burdens. PDT employed a conjugate between polyethylenimine and chlorin(e6) as the photosensitizer (PS) and 660-nm diode laser light delivered into the root canal via a 200-µ fiber, and this was compared and combined with standard endodontic treatment using mechanical debridement and antiseptic irrigation.
Results
Endodontic therapy alone reduced bacterial bioluminescence by 90% while PDT alone reduced bioluminescence by 95%. The combination reduced bioluminescence by >98%, and importantly the bacterial regrowth observed 24 hours after treatment was much less for the combination (P<0.0005) than for either single treatment.
Conclusions
Bioluminescence imaging is an efficient way to monitor endodontic therapy. Antimicrobial PDT may have a role to play in optimized endodontic therapy. Lasers Surg. Med. © 2006 Wiley-Liss, Inc.
REFERENCES
- 1 Siqueira JF, Jr. Endodontic infections: Concepts, paradigms, and perspectives. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 2002; 94(3): 281–293.
- 2 Bahcall JK, Barss JT. Understanding and evaluating the endodontic file. Gen Dent 2000; 48(6): 690–692.
- 3 Sedgley C. Root canal irrigation—a historical perspective. J Hist Dent 2004; 52(2): 61–65.
- 4 Ching BB. Common causes of endodontic failure. Hawaii Dent J 2003; 34(4): 13–16.
- 5 Wong R. Conventional endodontic failure and retreatment. Dent Clin North Am 2004; 48(1): 265–289.
- 6 Reynaud Af Geijersstam AH, Ellington MJ, Warner M, Woodford N, Haapasalo M. Antimicrobial susceptibility and molecular analysis of Enterococcus faecalis originating from endodontic infections in Finland and Lithuania. Oral Microbiol Immunol 2006; 21(3): 164–168.
- 7 Pinheiro ET, Gomes BP, Drucker DB, Zaia AA, Ferraz CC, Souza-Filho FJ. Antimicrobial susceptibility of Enterococcus faecalis isolated from canals of root filled teeth with periapical lesions. Int Endod J 2004; 37(11): 756–763.
- 8 Figdor D. Microbial aetiology of endodontic treatment failure and pathogenic properties of selected species. Aust Endod J 2004; 30(1): 11–14.
- 9 Gomes BP, Lilley JD, Drucker DB. Variations in the susceptibilities of components of the endodontic microflora to biomechanical procedures. Int Endod J 1996; 29(4): 235–241.
- 10 Drucker DB, Lilley JD, Tucker D, Gibbs AC. The endodontic microflora revisited. Microbios 1992; 71(288–289): 225–234.
- 11 Sjogren U, Hagglund B, Sundqvist G, Wing K. Factors affecting the long-term results of endodontic treatment. J Endod 1990; 16(10): 498–504.
- 12 Friedman S, Mor C. The success of endodontic therapy—healing and functionality. J Calif Dent Assoc 2004; 32(6): 493–503.
- 13 Bahcall JK, Miserendino L, Walia H, Belardi DW. Scanning electron microscopic comparison of canal preparation with Nd:YAG laser and hand instrumentation: A preliminary study. Gen Dent 1993; 41(1): 45–47.
- 14 Lee MT, Bird PS, Walsh LJ. Photo-activated disinfection of the root canal: A new role for lasers in endodontics. Aust Endod J 2004; 30(3): 93–98.
- 15 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(3): 268–274.
- 16 Bahcall J, Howard P, Miserendino L, Walia H. Preliminary investigation of the histological effects of laser endodontic treatment on the periradicular tissues in dogs. J Endodont 1992; 18: 47–51.
- 17 Distel JW, Hatton JF, Gillespie MJ. Biofilm formation in medicated root canals. J Endod 2002; 28(10): 689–693.
- 18 Fux CA, Costerton JW, Stewart PS, Stoodley P. Survival strategies of infectious biofilms. Trends Microbiol 2005; 13(1): 34–40.
- 19 Lewis K. Riddle of biofilm resistance. Antimicrob Agents Chemother 2001; 45(4): 999–1007.
- 20 Hamblin MR, Hasan T. Photodynamic therapy: A new antimicrobial approach to infectious disease? Photochem Photobiol Sci 2004; 3(5): 436–450.
- 21 Demidova TN, Hamblin MR. Photodynamic therapy targeted to pathogens. Int J Immunopathol Pharmacol 2004; 17(3): 245–254.
- 22 Wainwright M. Photodynamic antimicrobial chemotherapy (PACT). J Antimicrob Chemother 1998; 42(1): 13–28.
- 23 Soukos NS, Ximenez-Fyvie LA, Hamblin MR, Socransky SS, Hasan T. Targeted antimicrobial photochemotherapy. Antimicrob Agents Chemother 1998; 42(10): 2595–2601.
- 24 Maisch T, Bosl C, Szeimies RM, Lehn N, Abels C. Photodynamic effects of novel XF porphyrin derivatives on prokaryotic and eukaryotic cells. Antimicrob Agents Chemother 2005; 49(4): 1542–1552.
- 25 Komerik N, Macrobert AJ. Photodynamic therapy as an alternative antimicrobial modality for oral infections. J Environ Pathol Toxicol Oncol 2006; 25(1–2): 487–504.
- 26 Wilson M. Lethal photosensitisation of oral bacteria and its potential application in the photodynamic therapy of oral infections. Photochem Photobiol Sci 2004; 3(5): 412–418.
- 27 Bonsor SJ, Nichol R, Reid TM, Pearson GJ. Microbiological evaluation of photo-activated disinfection in endodontics (an in vivo study). Br Dent J 2006; 200(6): 337–341, discussion 329.
- 28 Bonsor SJ, Pearson GJ. Current clinical applications of photo-activated disinfection in restorative dentistry. Dent Update 2006; 33(3): 143–144 , 147–150, 153.
- 29 Garcez AS, Núñez SC, Lage-Marques JL, Jorge AO, Ribeiro MS. Efficiency of NaOCl and laser-assisted photosensitization on the reduction of Enterococcus faecalis in vitro. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 2006; 12(4): e93–e98 (online).
- 30 Meisel P, Kocher T. Photodynamic therapy for periodontal diseases: State of the art. J Photochem Photobiol B 2005; 79(2): 159–170.
- 31 Hayek RR, Araujo NS, Gioso MA, Ferreira J, Baptista-Sobrinho CA, Yamada AM, Ribeiro MS. Comparative study between the effects of photodynamic therapy and conventional therapy on microbial reduction in ligature-induced peri-implantitis in dogs. J Periodontol 2005; 76(8): 1275–1281.
- 32 Walsh LJ. The current status of laser applications in dentistry. Aust Dent J 2003; 48(3): 146–155; quiz 198.
- 33 Wong TW, Wang YY, Sheu HM, Chuang YC. Bactericidal effects of toluidine blue-mediated photodynamic action on Vibrio vulnificus. Antimicrob Agents Chemother 2005; 49(3): 895–902.
- 34 Komerik N, Nakanishi H, MacRobert AJ, Henderson B, Speight P, Wilson M. In vivo killing of Porphyromonas gingivalis by toluidine blue-mediated photosensitization in an animal model. Antimicrob Agents Chemother 2003; 47(3): 932–940.
- 35 Contag CH, Contag PR, Mullins JI, Spilman SD, Stevenson DK, Benaron DA. Photonic detection of bacterial pathogens in living hosts. Mol Microbiol 1995; 18(4): 593–603.
- 36 Burns SM, Joh D, Francis KP, Shortliffe LD, Gruber CA, Contag PR, Contag CH. Revealing the spatiotemporal patterns of bacterial infectious diseases using bioluminescent pathogens and whole body imaging. Contrib Microbiol 2001; 9: 71–88.
- 37 Doyle TC, Burns SM, Contag CH. In vivo bioluminescence imaging for integrated studies of infection. Cell microbiol 2004; 6(4): 303–317.
- 38 Demidova TN, Gad F, Zahra T, Francis KP, Hamblin MR. Monitoring photodynamic therapy of localized infections by bioluminescence imaging of genetically engineered bacteria. J Photochem Photobiol B 2005; 81: 15–25.
- 39 Hamblin MR, O'Donnell DA, Murthy N, Contag CH, Hasan T. Rapid control of wound infections by targeted photodynamic therapy monitored by in vivo bioluminescence imaging. Photochem Photobiol 2002; 75(1): 51–57.
- 40 Hamblin MR, Zahra T, Contag CH, McManus AT, Hasan T. Optical monitoring and treatment of potentially lethal wound infections in vivo. J Infect Dis 2003; 187(11): 1717–1726.
- 41 Lambrechts SA, Demidova TN, Aalders MC, Hasan T, Hamblin MR. Photodynamic therapy for Staphylococcus aureus infected burn wounds in mice. Photochem Photobiol Sci 2005; 4(7): 503–509.
- 42 Gad F, Zahra T, Francis KP, Hasan T, Hamblin MR. Targeted photodynamic therapy of established soft-tissue infections in mice. Photochem Photobiol Sci 2004; 3(5): 451–458.
- 43 Tegos GP, Anbe M, Yang C, Demidova TN, Satti M, Mroz P, Janjua S, Gad F, Hamblin MR. Protease-stable polycationic photosensitizer conjugates between polyethyleneimine and chlorin(e6) for broad-spectrum antimicrobial photoinactivation. Antimicrob Agents Chemother 2006; 50(4): 1402–1410.
- 44 Haapasalo M, Orstavik D. In vitro infection and disinfection of dentinal tubules. J Dent Res 1987; 66(8): 1375–1379.
- 45 Maoz A, Mayr R, Bresolin G, Neuhaus K, Francis KP, Scherer S. Sensitive in situ monitoring of a recombinant bioluminescent Yersinia enterocolitica reporter mutant in real time on Camembert cheese. Appl Environ Microbiol 2002; 68(11): 5737–5740.
- 46 Jett BD, Hatter KL, Huycke MM, Gilmore MS. Simplified agar plate method for quantifying viable bacteria. Biotechniques 1997; 23(4): 648–650.
- 47 Gutknecht N, van Gogswaardt D, Conrads G, Apel C, Schubert C, Lampert F. Diode laser radiation and its bactericidal effect in root canal wall dentin. J Clin Laser Med Surg 2000; 18(2): 57–60.
- 48 Peciuliene V, Reynaud AH, Balciuniene I, Haapasalo M. Isolation of yeasts and enteric bacteria in root-filled teeth with chronic apical periodontitis. Int Endod J 2001; 34(6): 429–434.
- 49 Ranta K, Haapasalo M, Ranta H. Monoinfection of root canal with Pseudomonas aeruginosa. Endod Dent Traumatol 1988; 4(6): 269–272.
- 50 Haapasalo M, Ranta H, Ranta KT. Facultative gram-negative enteric rods in persistent periapical infections. Acta Odontol Scand 1983; 41(1): 19–22.
- 51 Sedgley C, Applegate B, Nagel A, Hall D. Real-time imaging and quantification of bioluminescent bacteria in root canals in vitro. J Endod 2004; 30(12): 893–898.
- 52 Sedgley CM, Nagel AC, Hall D, Applegate B. Influence of irrigant needle depth in removing bioluminescent bacteria inoculated into instrumented root canals using real-time imaging in vitro. Int Endod J 2005; 38(2): 97–104.
- 53 Foley JW, Song X, Demidova TN, Jilal F, Hamblin MR. Synthesis and properties of benzo[a]phenoxazinium chalcogen analogs as novel broad-spectrum antimicrobial photosensitizers. J Med Chem 2006; 49: 5291–5299.
- 54 Seal GJ, Ng YL, Spratt D, Bhatti M, Gulabivala K. An in vitro comparison of the bactericidal efficacy of lethal photosensitization or sodium hydrochlorite irrigation on Streptococcus intermedius biofilms in root canals. Int Endod J 2002; 35(3): 268–274.