Evaluation of bacteriophage as an adjunct therapy for treatment of peri-prosthetic joint infection caused by Staphylococcus aureus
Autoři:
Jodie L. Morris aff001; Hayley L. Letson aff002; Lisa Elliott aff003; Andrea L. Grant aff001; Matthew Wilkinson aff001; Kaushik Hazratwala aff001; Peter McEwen aff001
Působiště autorů:
Orthopaedic Research Institute of Queensland, Townsville, Queensland, Australia
aff001; College of Medicine and Dentistry, James Cook University, Queensland, Australia
aff002; AusPhage Pty Ltd, Townsville, Queensland, Australia
aff003
Vyšlo v časopise:
PLoS ONE 14(12)
Kategorie:
Research Article
doi:
https://doi.org/10.1371/journal.pone.0226574
Souhrn
Phage therapy offers a potential alternate strategy for the treatment of peri-prosthetic joint infection (PJI), particularly where limited effective antibiotics are available. We undertook preclinical trials to investigate the therapeutic efficacy of a phage cocktail, alone and in combination with vancomycin, to reduce bacterial numbers within the infected joint using a clinically-relevant model of Staphylococcus aureus-induced PJI. Infected animals were randomised to 4 treatment groups, with treatment commencing 21-days post-surgery: bacteriophage alone, vancomycin alone, bacteriophage and vancomycin, and sham. At day 28 post-surgery, animals were euthanised for microbiological and immunological assessment of implanted joints. Treatment with phage alone or vancomycin alone, led to 5-fold and 6.2-fold reductions, respectively in bacterial load within peri-implant tissue compared to sham-treated animals. Compared to sham-treated animals, a 22.5-fold reduction in S. aureus burden was observed within joint tissue of animals that were administered phage in combination with vancomycin, corresponding with decreased swelling in the implanted knee. Microbiological data were supported by evidence of decreased inflammation within the joints of animals administered phage in combination with vancomycin, compared to sham-treated animals. Our findings provide further support for phage therapy as a tolerable and effective adjunct treatment for PJI.
Klíčová slova:
Bacteriophages – Inflammation – Knee joints – Skeletal joints – Staphylococcus aureus – Titanium implants – Vancomycin
Zdroje
1. Cisek AA, Dabrowska I, Gregorczyk KP, Wyzewski Z. Phage therapy in bacterial infections treatment: One hundred years after the discovery of bacteriophages. Curr Microbiol. 2017;74: 277–283. doi: 10.1007/s00284-016-1166-x 27896482
2. Akanda ZZ, Taha M, Abdelbary H. Current review—The rise of bacteriophage as a unique therapeutic platform in treating peri-prosthetic joint infections. J Orthop Res. 2018;36: 1051–1060. doi: 10.1002/jor.23755 28971508
3. Schmidt C. Phage therapy’s latest makeover. Nat Biotechnol. 2019;37: 581–586. doi: 10.1038/s41587-019-0133-z 31068679
4. Lu TK, Koeris MS. The next generation of bacteriophage therapy. Curr Opin Microbiol. 2011;14: 524–531. doi: 10.1016/j.mib.2011.07.028 21868281
5. World Health Organisation (WHO). No time to wait: Securing the future from drug-resistant infections. Report to the Secretary-General of the United Nations. Geneva, Switzerland; 2019 April, 2019. www.who.int/antimicrobial-resistance/interagency-coordination-group/final-report/en/
6. Ferry T, Boucher F, Fevre C, Perpoint T, Chateau J, Petitjean C, et al. Innovations for the treatment of a complex bone and joint infection due to XDR Pseudomonas aeruginosa including local application of a selected cocktail of bacteriophages. J Antimicrob Chemother. 2018;73: 2901–2903. doi: 10.1093/jac/dky263 30060002
7. Patey O, McCallin S, Mazure H, Liddle M, Smithyman A, Dublanchet A. Clinical indications and compassionate use of phage therapy: Personal experience and literature review with a focus on osteoarticular infections. Viruses. 2018;11: 18. doi: 10.3390/v11010018 30597868
8. Davis J. Prosthetic joint infections in Australia and New Zealand: The first 275 patients from the PIANO (Prosthetic Joint Infection in Australia and New Zealand Observational) study. Orthop Proc. 2016;98-B:58. www.online.boneandjoint.org.uk/doi/abs/10.1302/1358-992X.98BSUPP_23.EBJIS2016-058
9. Springer BD, Cahue S, Etkin CD, Lewallen DG, McGrory BJ. Infection burden in total hip and knee arthroplasties: an international registry-based perspective. Arthroplast Today. 2017;3: 137–140. doi: 10.1016/j.artd.2017.05.003 28695187
10. Tande AJ, Gomez-Urena EO, Berbari EF, Osmon DR. Management of prosthetic joint infection. Infect Dis Clin North Am. 2017;31: 237–52. doi: 10.1016/j.idc.2017.01.009 28366224
11. Kostakioti M, Hadjifrangiskou M, Hultgren SJ. Bacterial biofilms: development, dispersal, and therapeutic strategies in the dawn of the postantibiotic era. Cold Spring Harb Perspect Med. 2013;3: a010306. doi: 10.1101/cshperspect.a010306 23545571
12. Ricciardi BF, Muthukrishnan G, Masters E, Ninomiya M, Lee CC, Schwarz EM. Staphylococcus aureus Evasion of Host Immunity in the Setting of Prosthetic Joint Infection: Biofilm and Beyond. Curr Rev Musculoskelet Med. 2018;11: 389–400. doi: 10.1007/s12178-018-9501-4 29987645
13. Arciola CR, Campoccia D, Montanaro L. Implant infections: adhesion, biofilm formation and immune evasion. Nat Rev Microbiol. 2018;16: 397–409. doi: 10.1038/s41579-018-0019-y 29720707
14. Josse J, Velard F, Gangloff SC. Staphylococcus aureus vs. Osteoblast: relationship and consequences in osteomyelitis. Front Cell Infect Microbiol. 2015;5:85. doi: 10.3389/fcimb.2015.00085 26636047
15. Parvizi J, Gehrke T, Chen AF. Proceedings of the International Consensus on Periprosthetic Joint Infection. Bone Joint J. 2013;95-b: 1450–1452. doi: 10.1302/0301-620X.95B11.33135 24151261
16. Ma C-Y, Lu Y-D, Bell KL, Wang J-W, Ko J-Y, Wang C-J, et al. Predictors of treatment failure after 2-stage reimplantation for infected total knee arthroplasty: a 2- to 10-year follow-up. J Arthroplasty. 2018;33: 2234–2239. doi: 10.1016/j.arth.2018.02.007 29572036
17. Tan TL, Goswami K, Kheir MM, Xu C, Wang Q, Parvizi J. Surgical treatment of chronic periprosthetic joint infection: fate of spacer exchanges. J Arthroplasty. 2019;34: 2085–2090. doi: 10.1016/j.arth.2019.04.016 31182410
18. Dublanchet A, Patey O. Phage therapy for bone and joint infections: Report of French cases. Orthop Proc. 2017;99-B(SUPP_22):35. www.online.boneandjoint.org.uk/doi/abs/10.1302/1358-992X.2017.22.035
19. Kishor C, Mishra RR, Saraf SK, Kumar M, Srivastav AK, Nath G. Phage therapy of Staphylococcal chronic osteomyelitis in experimental animal model. Indian J Med Res. 2016;143:87–94. doi: 10.4103/0971-5916.178615 26997019
20. Morris J, Kelly N, Elliott L, Grant A, Wilkinson M, Hazratwala K, et al. Evaluation of bacteriophage anti-biofilm activity for potential control of orthopedic implant-related infections caused by Staphylococcus aureus. Surg Infect (Larchmt). 2018;20: 16–24. doi: 10.1089/sur.2018.135 30207891
21. Morris J, Letson H, Grant A, Wilkinson M, Hazratwala K, McEwen P. Experimental model of experimental peri-prosthetic joint infection of the knee caused by Staphylococcus aureus using biomaterials representative of modern TKA. Biol Open. 2019;8: bio045203. doi: 10.1242/bio.045203 31533935
22. Poeppl W, Lingscheid T, Bernitzky D, Schwarze UY, Donath O, Perkmann T, et al. Efficacy of fosfomycin compared to vancomycin in treatment of implant-associated chronic methicillin-resistant Staphylococcus aureus osteomyelitis in rats. Antimicrob Agents Chemother. 2014;58: 5111–5116. doi: 10.1128/AAC.02720-13 24936591
23. Rouse MS, Piper KE, Jacobson M, Jacofsky DJ, Steckelberg JM, Patel R. Daptomycin treatment of Staphylococcus aureus experimental chronic osteomyelitis. J Antimicrob Chemother. 2006;57: 301–305. doi: 10.1093/jac/dki435 16361330
24. Vergidis P, Schmidt-Malan SM, Mandrekar JN, Steckelberg JM, Patel R. Comparative activities of vancomycin, tigecycline and rifampin in a rat model of methicillin-resistant Staphylococcus aureus osteomyelitis. J Infect. 2015;70: 609–615. doi: 10.1016/j.jinf.2014.12.016 25576292
25. Roach DR, Debarbieux L. Phage therapy: awakening a sleeping giant. Emerging Topics in Life Sciences. 2017;1: 93–103. doi: 10.1042/ETLS20170002
26. Marre R, Schulz E, Anders T, Sack K. Renal tolerance and pharmacokinetics of vancomycin in rats. J Antimicrob Chemother. 1984;14: 253–260. doi: 10.1093/jac/14.3.253 6490570
27. Yilmaz C, Colak M, Yilmaz BC, Ersoz G, Kutateladze M, Gozlugol M. Bacteriophage therapy in implant-related infections: an experimental study. J Bone Joint Surg Am. 2013;95: 117–125. doi: 10.2106/JBJS.K.01135 23324958
28. Kutateladze M, Adamia R. Bacteriophages as potential new therapeutics to replace or supplement antibiotics. Trends Biotechnol. 2010;28: 591–595. doi: 10.1016/j.tibtech.2010.08.001 20810181
29. Barakat A, Schilling WHK, Sharma S, Guryel E, Freeman R. Chronic osteomyelitis: a review on current concepts and trends in treatment. Orthop Trauma. 2019;33: 181–187. doi: 10.1016/j.mporth.2019.03.005
30. Thabit AK, Fatani DF, Bamakhrama MS, Barnawi OA, Basudan LO, Alhejaili SF. Antibiotic penetration into bone and joints: An updated review. Int J Infect Dis. 2019;81: 128–136. doi: 10.1016/j.ijid.2019.02.005 30772469
31. Torres-Barcelo C, Gurney J, Gougat-Barbera C, Vasse M, Hochberg ME. Transient negative effects of antibiotics on phages do not jeopardise the advantages of combination therapies. FEMS Microbiol Ecol. 2018;94: doi: 10.1093/femsec/fiy107 29878184
32. Champagne CP, Gardner N. The spot test method for the in-plant enumeration of bacteriophages with paired cultures of Lactobacillus delbrueckii subsp. bulgaricus and Streptococcus salivarius subsp. thermophilus. Intern Dairy J. 1995;5: 417–425.
33. Speck P, Smithyman A. Safety and efficacy of phage therapy via the intravenous route. FEMS Microbiol Lett. 2016;363: pii: fnv242. doi: 10.1093/femsle/fnv242 26691737
34. Van Belleghem JD, Dabrowska K, Vaneechoutte M, Barr JJ, Bollyky PL. Interactions between bacteriophage, bacteria, and the mammalian immune system. Viruses. 2018;11: pii: E10. doi: 10.3390/v11010010 30585199
35. Krut O, Bekeredjian-Ding I. Contribution of the immune response to phage therapy. J Immunol. 2018;200: 3037–344. doi: 10.4049/jimmunol.1701745 29685950
36. Dąbrowska K. Phage therapy: What factors shape phage pharmacokinetics and bioavailability? Systematic and critical review. Med Res Rev. 2019;39: 2000–2025. doi: 10.1002/med.21572 30887551
37. Seed KD. Battling phages: how bacteria defend against viral attack. PLoS Pathogens. 2015;11: e1004847. doi: 10.1371/journal.ppat.1004847 26066799
38. Oechslin F. Resistance development to bacteriophages occurring during bacteriophage therapy. Viruses. 2018;10:351. doi: 10.3390/v10070351 29966329
39. Clinical and Laboratory Standards Institute (CLSI). CLSI M100-ED29:2019 Performance Standards for Antimicrobial Susceptibility Testing. Pennsylvannia, USA; 2019. www.clsi.org/standards/products/free-resources/access-our-free-resources/
40. Dhand A, Sakoulas G. Reduced vancomycin susceptibility among clinical Staphylococcus aureus isolates ('the MIC Creep'): implications for therapy. F1000 Med Rep. 2012;4: 4. doi: 10.3410/M4-4 22312414
41. Kok EY, Vallejo JG, Sommer LM, Rosas L, Kaplan SL, Hulten KG, et al. Association of vancomycin MIC and molecular characteristics with clinical outcomes in methicillin-susceptible Staphylococcus aureus acute hematogenous osteoarticular infections in children. Antimicrob Agents Chemother. 2018;62: e00084–18. doi: 10.1128/AAC.00084-18 29530845
42. Srivastava K, Bozic KJ, Silverton C, Nelson AJ, Makhni EC, Davis JJ. Reconsidering strategies for managing chronic periprosthetic joint infection in total knee Arthroplasty: using decision analytics to find the optimal strategy between one-stage and two-stage total knee revision. J Bone Joint Surg Am. 2019;101: 14–24. doi: 10.2106/JBJS.17.00874 30601412
Článek vyšel v časopise
PLOS One
2019 Číslo 12
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