Skip to main content
Top
Published in: Lasers in Medical Science 3/2018

Open Access 01-04-2018 | Original Article

Antimicrobial photodynamic therapy—a promising treatment for prosthetic joint infections

Authors: Timothy Briggs, Gordon Blunn, Simon Hislop, Rita Ramalhete, Caroline Bagley, David McKenna, Melanie Coathup

Published in: Lasers in Medical Science | Issue 3/2018

Login to get access

Abstract

Periprosthetic joint infection (PJI) is associated with high patient morbidity and a large financial cost. This study investigated Photodynamic Therapy (PDT) as a means of eradicating bacteria that cause PJI, using a laser with a 665-nm wavelength and methylene blue (MB) as the photosensitizer. The effectiveness of MB concentration on the growth inhibition of methicillin-sensitive Staphylococcus aureus (MSSA), methicillin-resistant Staphylococcus aureus (MRSA), Staphylococcus epidermidis, Pseudomonas aeruginosa and Acinetobacter baumannii was investigated. The effect of laser dose was also investigated and the optimized PDT method was used to investigate its bactericidal effect on species within planktonic culture and following the formation of a biofilm on polished titanium and hydroxyapatite coated titanium discs. Results showed that Staphylococci were eradicated at the lowest concentration of 0.1 mM methylene blue (MB). With P. aeruginosa and A. baumannii, increasing the MB concentration improved the bactericidal effect. When the laser dose was increased, results showed that the higher the power of the laser the more bacteria were eradicated with a laser power ≥ 35 J/cm2 and an irradiance of 35 mW/cm2, eradicating all S. epidermidis. The optimized PDT method had a significant bactericidal effect against planktonic MRSA and S. epidermidis compared to MB alone, laser alone, or control (no treatment). When biofilms were formed, PDT treatment had a significantly higher bactericidal effect than MB alone and laser alone for all species of bacteria investigated on the polished disc surfaces. P. aeruginosa grown in a biofilm was shown to be less sensitive to PDT when compared to Staphylococci, and a HA-coated surface reduced the effectiveness of PDT. This study demonstrated that PDT is effective for killing bacteria that cause PJI.
Literature
1.
2.
go back to reference Phillips JE, Crane TP, Noy M, Elliott TS, Grimer RJ (2006) The incidence of deep prosthetic infections in a specialist orthopaedic hospital: a 15-year prospective survey. J Bone Joint Surg Br 88:943–948CrossRefPubMed Phillips JE, Crane TP, Noy M, Elliott TS, Grimer RJ (2006) The incidence of deep prosthetic infections in a specialist orthopaedic hospital: a 15-year prospective survey. J Bone Joint Surg Br 88:943–948CrossRefPubMed
3.
go back to reference Blom AW, Taylor AH, Pattison G, Whitehouse S, Bannister GC (2003) Infection after total hip arthroplasty. The Avon experience. J Bone Joint Surg Br 85:956–959CrossRefPubMed Blom AW, Taylor AH, Pattison G, Whitehouse S, Bannister GC (2003) Infection after total hip arthroplasty. The Avon experience. J Bone Joint Surg Br 85:956–959CrossRefPubMed
4.
go back to reference Toms AD, Davidson D, Masri BA, Duncan CP (2006) The management of peri-prosthetic infection in total joint arthroplasty. J Bone Joint Surg Br 88:149–155CrossRefPubMed Toms AD, Davidson D, Masri BA, Duncan CP (2006) The management of peri-prosthetic infection in total joint arthroplasty. J Bone Joint Surg Br 88:149–155CrossRefPubMed
5.
go back to reference Schroer WC, Berend KR, Lombardi AV, Barnes CL, Bolognesi MP, Berend ME, Ritter MA, Nunley RM (2013) Why are total knees failing today? Etiology of total knee revision in 2010 and 2011. J Arthroplast 28:116–119CrossRef Schroer WC, Berend KR, Lombardi AV, Barnes CL, Bolognesi MP, Berend ME, Ritter MA, Nunley RM (2013) Why are total knees failing today? Etiology of total knee revision in 2010 and 2011. J Arthroplast 28:116–119CrossRef
7.
go back to reference Murdoch DR, Roberts SA, Fowler VG Jr, Shah MA, Taylor SL, Morris AJ, Corey GR (2001) Infection of orthopedic prostheses after Staphylococcus aureus bacteremia. Clin Infect Dis 32(4):647–649CrossRefPubMed Murdoch DR, Roberts SA, Fowler VG Jr, Shah MA, Taylor SL, Morris AJ, Corey GR (2001) Infection of orthopedic prostheses after Staphylococcus aureus bacteremia. Clin Infect Dis 32(4):647–649CrossRefPubMed
8.
go back to reference Jamsen E, Nevalainen P, Eskelinen A, Huotari K, Kalliovalkama J, Moilanen T (2012) Obesity, diabetes, and preoperative hyperglycemia as predictors of periprosthetic joint infection: a single-center analysis of 7181 primary hip and knee replacements for osteoarthritis. J Bone Joint Surg Am 94(14):e101CrossRefPubMed Jamsen E, Nevalainen P, Eskelinen A, Huotari K, Kalliovalkama J, Moilanen T (2012) Obesity, diabetes, and preoperative hyperglycemia as predictors of periprosthetic joint infection: a single-center analysis of 7181 primary hip and knee replacements for osteoarthritis. J Bone Joint Surg Am 94(14):e101CrossRefPubMed
9.
go back to reference Dowsey MM, Choong PF (2008) Obesity is a major risk factor for prosthetic infection after primary hip arthroplasty. Clin Orthop Relat Res 466:153–158CrossRefPubMedPubMedCentral Dowsey MM, Choong PF (2008) Obesity is a major risk factor for prosthetic infection after primary hip arthroplasty. Clin Orthop Relat Res 466:153–158CrossRefPubMedPubMedCentral
10.
go back to reference Bozic KJ, Ries MD (2005) The impact of infection after total hip arthroplasty on hospital and surgeon resource utilization. J Bone Joint Surg Am 87:1746–1751PubMed Bozic KJ, Ries MD (2005) The impact of infection after total hip arthroplasty on hospital and surgeon resource utilization. J Bone Joint Surg Am 87:1746–1751PubMed
11.
go back to reference Choong PF, Dowsey MM, Carr D, Daffy J, Stanley P (2007) Risk factorsassociated with acute hip prosthetic joint infections and outcome of treatment with a rifampinbased regimen. Acta Orthop 78:755–765CrossRefPubMed Choong PF, Dowsey MM, Carr D, Daffy J, Stanley P (2007) Risk factorsassociated with acute hip prosthetic joint infections and outcome of treatment with a rifampinbased regimen. Acta Orthop 78:755–765CrossRefPubMed
12.
go back to reference Kurtz SM, Lau E, Watson H, Schmier JK, Parvizi J (2012) Economic burden of periprosthetic joint infection in the United States. J Arthroplast 27:61–65CrossRef Kurtz SM, Lau E, Watson H, Schmier JK, Parvizi J (2012) Economic burden of periprosthetic joint infection in the United States. J Arthroplast 27:61–65CrossRef
13.
go back to reference Klouche S, Sariali E, Mamoudy P (2010) Total hip arthroplasty revision due to infection: a cost analysis approach. Orthop Traumatol Surg Res 96:124–132CrossRefPubMed Klouche S, Sariali E, Mamoudy P (2010) Total hip arthroplasty revision due to infection: a cost analysis approach. Orthop Traumatol Surg Res 96:124–132CrossRefPubMed
14.
go back to reference Costerton JW, Stewart PS, Greenberg EP (1999) Bacterial biofilms: a common cause of persistent infections. Science 284:1318–1322CrossRefPubMed Costerton JW, Stewart PS, Greenberg EP (1999) Bacterial biofilms: a common cause of persistent infections. Science 284:1318–1322CrossRefPubMed
15.
go back to reference Fu XJ, Fang Y, Yao M (2013) Antimicrobial photodynamic therapy for methicillin-resistant Staphylococcus aureus infection. Biomed Res Int 2013:159157PubMedPubMedCentral Fu XJ, Fang Y, Yao M (2013) Antimicrobial photodynamic therapy for methicillin-resistant Staphylococcus aureus infection. Biomed Res Int 2013:159157PubMedPubMedCentral
16.
go back to reference O'connor AE, Gallagher WM, Byrne AT (2009) Porphyrin and nonporphyrin photosensitizers in oncology: preclinical and clinical advances in photodynamic therapy. Photochem Photobiol 85:1053–1074CrossRefPubMed O'connor AE, Gallagher WM, Byrne AT (2009) Porphyrin and nonporphyrin photosensitizers in oncology: preclinical and clinical advances in photodynamic therapy. Photochem Photobiol 85:1053–1074CrossRefPubMed
17.
go back to reference Bertoloni G, Lauro FM, Cortella G, Merchat M (2000) Photosensitizingactivity of hematoporphyrin on Staphylococcus aureus cells. Biochim Biophys Acta 1475:169–174CrossRefPubMed Bertoloni G, Lauro FM, Cortella G, Merchat M (2000) Photosensitizingactivity of hematoporphyrin on Staphylococcus aureus cells. Biochim Biophys Acta 1475:169–174CrossRefPubMed
19.
go back to reference Tanaka M, Kinoshita M, Yoshihara Y, Shinomiya N, Seki S, Nemoto K, Hirayama T, Dai T, Huang L, Hamblin MR, Morimoto Y (2012) Optimal photosensitizers for photodynamic therapy of infections should kill bacteria but spare neutrophils. Photochem Photobiol 88:227–232CrossRefPubMed Tanaka M, Kinoshita M, Yoshihara Y, Shinomiya N, Seki S, Nemoto K, Hirayama T, Dai T, Huang L, Hamblin MR, Morimoto Y (2012) Optimal photosensitizers for photodynamic therapy of infections should kill bacteria but spare neutrophils. Photochem Photobiol 88:227–232CrossRefPubMed
20.
go back to reference Rolim JP, De-Melo MA, Guedes SF, Albuquerque-Filho FB, De Souza JR, Nogueira NA, Zanin IC, Rodrigues LK (2012) The antimicrobial activity of photodynamic therapy against Streptococcus mutans using different photosensitizers. J Photochem Photobiol B 106:40–46CrossRefPubMed Rolim JP, De-Melo MA, Guedes SF, Albuquerque-Filho FB, De Souza JR, Nogueira NA, Zanin IC, Rodrigues LK (2012) The antimicrobial activity of photodynamic therapy against Streptococcus mutans using different photosensitizers. J Photochem Photobiol B 106:40–46CrossRefPubMed
21.
go back to reference Klepac-Ceraj V, Patel N, Song X, Holewa C, Patel C, Kent R, Amiji MM, Soukos NS (2011) Photodynamic effects of methylene blue-loaded polymeric nanoparticles on dental plaque bacteria. Lasers Surg Med 43:600–606CrossRefPubMedPubMedCentral Klepac-Ceraj V, Patel N, Song X, Holewa C, Patel C, Kent R, Amiji MM, Soukos NS (2011) Photodynamic effects of methylene blue-loaded polymeric nanoparticles on dental plaque bacteria. Lasers Surg Med 43:600–606CrossRefPubMedPubMedCentral
22.
go back to reference Jerjes WTH, Hopper C, Giannoudis PV (2012) Surgical site infections subjected to photodynamnic therapy: a potential application in orthopaedic surgery. Hard Tissue 1(1):9 Jerjes WTH, Hopper C, Giannoudis PV (2012) Surgical site infections subjected to photodynamnic therapy: a potential application in orthopaedic surgery. Hard Tissue 1(1):9
23.
go back to reference Sperandio FF, Huang YY, Hamblin MR (2013) Antimicrobial photodynamic therapy to kill Gram-negative bacteria. Recent Pat Antiinfect Drug Discov 8:108–120CrossRefPubMedPubMedCentral Sperandio FF, Huang YY, Hamblin MR (2013) Antimicrobial photodynamic therapy to kill Gram-negative bacteria. Recent Pat Antiinfect Drug Discov 8:108–120CrossRefPubMedPubMedCentral
24.
go back to reference Usacheva MN, Teichert MC, Biel MA (2001) Comparison of the methylene blue and toluidine blue photobactericidal efficacy against gram-positive and gram-negative microorganisms. Lasers Surg Med 29:165–173CrossRefPubMed Usacheva MN, Teichert MC, Biel MA (2001) Comparison of the methylene blue and toluidine blue photobactericidal efficacy against gram-positive and gram-negative microorganisms. Lasers Surg Med 29:165–173CrossRefPubMed
25.
go back to reference Xhevdet A, Stubljar D, Kriznar I, Jukic T, Skvarc M, Veranic P, Ihan A (2014) The disinfecting efficacy of root canals with laser photodynamic therapy. J Lasers Med Sci 5:19–26PubMedPubMedCentral Xhevdet A, Stubljar D, Kriznar I, Jukic T, Skvarc M, Veranic P, Ihan A (2014) The disinfecting efficacy of root canals with laser photodynamic therapy. J Lasers Med Sci 5:19–26PubMedPubMedCentral
26.
go back to reference Gois MM, Kurachi C, Santana EJ, Mima EG, Spolidorio DM, Pelino JE, Salvador Bagnato V (2010) Susceptibility of Staphylococcus aureus to porphyrin- mediated photodynamic antimicrobial chemotherapy: an in vitro study. Lasers Med Sci 25:391–395CrossRefPubMed Gois MM, Kurachi C, Santana EJ, Mima EG, Spolidorio DM, Pelino JE, Salvador Bagnato V (2010) Susceptibility of Staphylococcus aureus to porphyrin- mediated photodynamic antimicrobial chemotherapy: an in vitro study. Lasers Med Sci 25:391–395CrossRefPubMed
27.
go back to reference Lopez-Jimenez L, Fuste E, Martinez-Garriga B, Arnabat-Dominguez J, Vinuesa T, Vinas M (2015) Effects of photodynamic therapy on enterococcus faecalis biofilms. Lasers Med Sci 30:1519–1526CrossRefPubMedPubMedCentral Lopez-Jimenez L, Fuste E, Martinez-Garriga B, Arnabat-Dominguez J, Vinuesa T, Vinas M (2015) Effects of photodynamic therapy on enterococcus faecalis biofilms. Lasers Med Sci 30:1519–1526CrossRefPubMedPubMedCentral
28.
go back to reference Simonetti O, Cirioni O, Orlando F, Alongi C, Lucarini G, Silvestri C, Zizzi A, Fantetti L, Roncucci G, Giacometti A, Offidani A, Provinciali M (2011) Effectiveness of antimicrobial photodynamic therapy with a single treatment of RLP068/Cl in an experimental model of Staphylococcus aureus wound infection. Br J Dermatol 164:987–995CrossRefPubMed Simonetti O, Cirioni O, Orlando F, Alongi C, Lucarini G, Silvestri C, Zizzi A, Fantetti L, Roncucci G, Giacometti A, Offidani A, Provinciali M (2011) Effectiveness of antimicrobial photodynamic therapy with a single treatment of RLP068/Cl in an experimental model of Staphylococcus aureus wound infection. Br J Dermatol 164:987–995CrossRefPubMed
29.
go back to reference Percival SL, Suleman L, Francolini I, Donelli G (2014) The effectiveness ofphotodynamic therapy on planktonic cells and biofilms and its role in wound healing. Future Microbiol 9:1083–1094CrossRefPubMed Percival SL, Suleman L, Francolini I, Donelli G (2014) The effectiveness ofphotodynamic therapy on planktonic cells and biofilms and its role in wound healing. Future Microbiol 9:1083–1094CrossRefPubMed
30.
go back to reference Biel MA, Sievert C, Usacheva M, Teichert M, Wedell E, Loebel N, Rose A, Zimmermann R (2011) Reduction of endotracheal tube biofilms using antimicrobial photodynamic therapy. Lasers Surg Med 43:586–590CrossRefPubMedPubMedCentral Biel MA, Sievert C, Usacheva M, Teichert M, Wedell E, Loebel N, Rose A, Zimmermann R (2011) Reduction of endotracheal tube biofilms using antimicrobial photodynamic therapy. Lasers Surg Med 43:586–590CrossRefPubMedPubMedCentral
31.
go back to reference Gristina AG, Costerton JW (1985) Bacterial adherence to biomaterials and tissue. The significance of its role in clinical sepsis. J Bone Joint Surg Am 67:264–273CrossRefPubMed Gristina AG, Costerton JW (1985) Bacterial adherence to biomaterials and tissue. The significance of its role in clinical sepsis. J Bone Joint Surg Am 67:264–273CrossRefPubMed
32.
go back to reference Cordero J, Munuera L, Folgueira MD (1996) The influence of the chemical composition and surface of the implant on infection. Injury 27(Suppl 3):SC34–SC37PubMed Cordero J, Munuera L, Folgueira MD (1996) The influence of the chemical composition and surface of the implant on infection. Injury 27(Suppl 3):SC34–SC37PubMed
33.
go back to reference Laure B, Besnier JM, Bergemer-Fouquet AM, Marquet-Van Der Mee N, Damie F, Quentin R, Favard L, Rosset P (2008) Effect of hydroxyapatite coating and polymethylmethacrylate on stainless steel implant-site infection with Staphylococcus epidermidis in a sheep model. J Biomed Mater Res A 84:92–98CrossRefPubMed Laure B, Besnier JM, Bergemer-Fouquet AM, Marquet-Van Der Mee N, Damie F, Quentin R, Favard L, Rosset P (2008) Effect of hydroxyapatite coating and polymethylmethacrylate on stainless steel implant-site infection with Staphylococcus epidermidis in a sheep model. J Biomed Mater Res A 84:92–98CrossRefPubMed
Metadata
Title
Antimicrobial photodynamic therapy—a promising treatment for prosthetic joint infections
Authors
Timothy Briggs
Gordon Blunn
Simon Hislop
Rita Ramalhete
Caroline Bagley
David McKenna
Melanie Coathup
Publication date
01-04-2018
Publisher
Springer London
Published in
Lasers in Medical Science / Issue 3/2018
Print ISSN: 0268-8921
Electronic ISSN: 1435-604X
DOI
https://doi.org/10.1007/s10103-017-2394-4

Other articles of this Issue 3/2018

Lasers in Medical Science 3/2018 Go to the issue