Safety and efficacy of topical bacteriophage and ethylenediaminetetraacetic acid treatment of Staphylococcus aureus infection in a sheep model of sinusitis

International Forum of Allergy and Rhinology

Volumn 4, Issue 3, 2014, Pages 176-186

  Drilling, Amanda ^a   Morales, Sandra ^b   Boase, Samuel ^a   Jervis Bardy, Joshua ^a   James, Craig ^c   Jardeleza, Camille ^a   Tan, Neil Cheng Wen ^a   Cleland, Edward ^a   Speck, Peter ^d   Vreugde, Sarah ^a   Wormald, Peter John ^a  

^a UNIVERSITY OF ADELAIDE   (Australia)

^b Special Phage Services   (Australia)

^c Adelaide Pathology Partners   (Australia)

^d FLINDERS UNIVERSITY   (Australia)

Author keywords

Antimicrobial therapy; Bacteriophage; Biofilm; EDTA; Ovine

Indexed keywords

ANTIBIOTIC AGENT; COCKTAIL OF STAPHYLOCOCCUS AUREUS SPECIFIC PHAGE; EDETIC ACID; TOPICAL AGENT; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIOPHAGE; BIOFILM; CONTROLLED STUDY; DRUG EFFICACY; DRUG SAFETY; FECES; FRONTAL SINUSITIS; HISTOLOGY; INFLAMMATION; INOCULATION; NONHUMAN; OVINE MODEL; PRIORITY JOURNAL; RISK ASSESSMENT; SCANNING ELECTRON MICROSCOPY; STAPHYLOCOCCUS INFECTION; TISSUE SECTION; TREATMENT DURATION;

ANTIMICROBIAL THERAPY; BACTERIOPHAGE; BIOFILM; EDTA; OVINE;

ANIMALS; BIOFILMS; CATTLE; DISEASE MODELS, ANIMAL; EDETIC ACID; FRONTAL SINUS; HUMANS; MICROSCOPY, CONFOCAL; SHEEP; STAPHYLOCOCCAL INFECTIONS; STAPHYLOCOCCUS AUREUS; STAPHYLOCOCCUS PHAGES;

EID: 84895452699     PISSN: 20426976     EISSN: 20426984     Source Type: Journal    
DOI: 10.1002/alr.21270     Document Type: Article

References (84)

1. Benninger MS, Ferguson BJ, Hadley JA, et al. Adult chronic rhinosinusitis: definitions, diagnosis, epidemiology, and pathophysiology. Otolaryngol Head Neck Surg. 2003;129(3 Suppl):S1-S32.
2. Mccaig LF, Hughes JM. Trends in antimicrobial drug prescribing among office-based physicians in the United States. JAMA. 1995;273:214-219.
3. Costerton JW, Stewart PS, Greenberg EP. Bacterial biofilms: a common cause of persistent infections. Science. May 21 1999;284(5418):1318-1322.
4. Foreman A, Wormald PJ. Different biofilms, different disease? A clinical outcomes study. Laryngoscope. 2010;120:1701-1706.
5. Nickel JC, Ruseska I, Wright JB, Costerton JW. Tobramycin resistance of Pseudomonas aeruginosa cells growing as a biofilm on urinary catheter material. Antimicrob Agents Chemother. 1985;27:619-624.
6. Briandet R, Lacroix-Gueu P, Renault M, et al. Fluorescence correlation spectroscopy to study diffusion and reaction of bacteriophages inside biofilms. Appl Environ Microbiol. 2008;74:2135-2143.
7. Corbin BD, McLean RJ, Aron GM. Bacteriophage T4 multiplication in a glucose-limited Escherichia coli biofilm. Can J Microbiol. 2001;47:680-684.
8. Sillankorva S, Oliveira R, Vieira MJ, Sutherland IW, Azeredo J. Bacteriophage Phi S1 infection of Pseudomonas fluorescens planktonic cells versus biofilms. Biofouling. 2004;20:133-138.
9. Fu W, Forster T, Mayer O, Curtin JJ, Lehman SM, Donlan RM. Bacteriophage cocktail for the prevention of biofilm formation by Pseudomonas aeruginosa on catheters in an in vitro model system. Antimicrob Agents Chemother. 2010;54:397-404.
10. Carson L, Gorman SP, Gilmore BF. The use of lytic bacteriophages in the prevention and eradication of biofilms of Proteus mirabilis and Escherichia coli. FEMS Immunol Med Microbiol. 2010;59:447-455.
11. Siringan P, Connerton PL, Payne RJ, Connerton IF. Bacteriophage-mediated dispersal of Campylobacter jejuni biofilms. Appl Environ Microbiol. 2011;77:3320-3326.
12. Cerca N, Oliveira R, Azeredo J. Susceptibility of Staphylococcus epidermidis planktonic cells and biofilms to the lytic action of staphylococcus bacteriophage K. Lett Appl Microbiol. 2007;45:313-317.
13. Curtin JJ, Donlan RM. Using bacteriophages to reduce formation of catheter-associated biofilms by Staphylococcus epidermidis. Antimicrob Agents Chemother. 2006;50:1268-1275.
14. Lu TK, Collins JJ. Dispersing biofilms with engineered enzymatic bacteriophage. Proc Natl Acad Sci U S A. 2007;104:11197-11202.
15. Rahman M, Kim S, Kim SM, Seol SY, Kim J. Characterization of induced Staphylococcus aureus bacteriophage SAP-26 and its anti-biofilm activity with rifampicin. Biofouling. 2011;27:1087-1093.
16. Drilling A, Jardeleza C, Morales S, Smithyman T, Vreugde S, Speck P, et al. Bacteriophage reduces biofilm of Staphylococcus aureus ex vivo isolates from chronic rhinosinusitis patients. Presented October 12, 2012, Basil Hetzel Institute for Translational Health Research, University of South Australia, Adelaide, SA, Australia.
17. Bruttin A, Brussow H. Human volunteers receiving Escherichia coli phage T4 orally: a safety test of phage therapy. Antimicrob Agents Chemother. 2005;49:2874-2878.
18. McCallin S, Alam Sarker S, Barretto C, et al. Safety analysis of a Russian phage cocktail: from metagenomic analysis to oral application in healthy human subjects. Virology. 2013;443:187-196.
19. Wright A, Hawkins CH, Anggard EE, Harper DR. A controlled clinical trial of a therapeutic bacteriophage preparation in chronic otitis due to antibiotic-resistant Pseudomonas aeruginosa; a preliminary report of efficacy. Clin Otolaryngol. 2009;34:349-357.
20. Markoishvili K, Tsitlanadze G, Katsarava R, Morris JG Jr, Sulakvelidze A. A novel sustained-release matrix based on biodegradable poly(ester amide)s and impregnated with bacteriophages and an antibiotic shows promise in management of infected venous stasis ulcers and other poorly healing wounds. Int J Dermatol. 2002;41:453-458.
21. Kutter E, De Vos D, Gvasalia G, et al. Phage therapy in clinical practice: treatment of human infections. Curr Pharm Biotechnol. 2010;11:69-86.
22. Lamas GA, Goertz C, Boineau R, et al. Effect of disodium EDTA chelation regimen on cardiovascular events in patients with previous myocardial infarction: the TACT randomized trial. JAMA. 2013;309:1241-1250.
23. Chauhan A, Lebeaux D, Ghigo JM, Beloin C. Full and broad-spectrum in vivo eradication of catheter-associated biofilms using gentamicin-EDTA antibiotic lock therapy. Antimicrob Agents Chemother. 2012;56:6310-6318.
24. Ballal NV, Yegneswaran PP, Mala K, Bhat KS. In vitro antimicrobial activity of maleic acid and ethylenediaminetetraacetic acid on endodontic pathogens. Oral Surg Oral Med Oral Pathol Oral Radiol Endod. 2011;112:696-700.
25. Raad I, Chatzinikolaou I, Chaiban G, et al. In vitro and ex vivo activities of minocycline and EDTA against microorganisms embedded in biofilm on catheter surfaces. Antimicrob Agents Chemother. 2003;47:3580-3585.
26. Shanks RM, Sargent JL, Martinez RM, Graber ML, O'Toole GA. Catheter lock solutions influence staphylococcal biofilm formation on abiotic surfaces. Nephrol Dial Transplant. 2006;21:2247-2255.
27. Lin MH, Shu JC, Huang HY, Cheng YC. Involvement of iron in biofilm formation by Staphylococcus aureus. PLoS One. 2012;7:e34388.
28. Dass CL, Walsh MF, Seo S, Shiratsuchi H, Craig DH, Basson MD. Irrigant divalent cation concentrations influence bacterial adhesion. J Surg Res. 2009;156:57-63.
29. Bjarnsholt T, Alhede M, Alhede M, et al. The in vivo biofilm. Trends Microbiol. 2013;21:466-474.
30. Fanning S, Xu W, Solis N, Woolford CA, Filler SG, Mitchell AP. Divergent targets of Candida albicans biofilm regulator Bcr1 in vitro and in vivo. Eukaryot Cell. 2012;11:896-904.
31. Jepson CD, March JB. Bacteriophage lambda is a highly stable DNA vaccine delivery vehicle. Vaccine. 2004;22:2413-2419.
32. Valentine R, Jervis-Bardy J, Psaltis A, Tan LW, Wormald PJ. Efficacy of using a hydrodebrider and of citric acid/zwitterionic surfactant on a Staphylococcus aureus bacterial biofilm in the sheep model of rhinosinusitis. Am J Rhinol Allergy. 2011;25:323-326.
33. Singhal D, Jekle A, Debabov D, et al. Efficacy of NVC-422 against Staphylococcus aureus biofilms in a sheep biofilm model of sinusitis. Int Forum Allergy Rhinol. 2012;2:309-315.
34. Ha KR, Psaltis AJ, Tan L, Wormald PJ. A sheep model for the study of biofilms in rhinosinusitis. Am J Rhinol. 2007;21:339-345.
35. Le T, Psaltis A, Tan LW, Wormald PJ. The efficacy of topical antibiofilm agents in a sheep model of rhinosinusitis. Am J Rhinol. 2008;22:560-567.
36. Fischer AH, Jacobson KA, Rose J, Zeller R. Hematoxylin and eosin staining of tissue and cell sections. CSH Protoc. 2008;2008:pdb.prot4986.
37. Adams M. Bacteriophages. New York: Interscience Publishers; 1959.
38. Ramesh V, Fralick JA, Rolfe RD. Prevention of Clostridium difficile-induced ileocecitis with bacteriophage. Anaerobe. 1999;5:69-78.
39. Barrow P, Lovell M, Berchieri A Jr. Use of lytic bacteriophage for control of experimental Escherichia coli septicemia and meningitis in chickens and calves. Clin Diagn Lab Immunol. 1998;5:294-298.
40. Matsuzaki S, Yasuda M, Nishikawa H, et al. Experimental protection of mice against lethal Staphylococcus aureus infection by novel bacteriophage phi MR11. J Infect Dis. 2003;187:613-624.
41. Wills QF, Kerrigan C, Soothill JS. Experimental bacteriophage protection against Staphylococcus aureus abscesses in a rabbit model. Antimicrob Agents Chemother. 2005;49:1220-1221.
42. McVay CS, Velasquez M, Fralick JA. Phage therapy of Pseudomonas aeruginosa infection in a mouse burn wound model. Antimicrob Agents Chemother. 2007;51:1934-1938.
43. Capparelli R, Parlato M, Borriello G, Salvatore P, Iannelli D. Experimental phage therapy against Staphylococcus aureus in mice. Antimicrob Agents Chemother. 2007;51:2765-2773.
44. Cerveny KE, DePaola A, Duckworth DH, Gulig PA. Phage therapy of local and systemic disease caused by Vibrio vulnificus in iron-dextran-treated mice. Infect Immun. 2002;70:6251-6262.
45. Soothill JS. Bacteriophage prevents destruction of skin grafts by Pseudomonas aeruginosa. Burns. 1994;20:209-211.
46. Li H, Ma ML, Xie HJ, Kong J. Biosafety evaluation of bacteriophages for treatment of diarrhea due to intestinal pathogen Escherichia coli 3-2 infection of chickens. World J Microbiol Biotechnol. 2012;28:1-6.
47. Sulakvelidze A, Alavidze Z, Morris JG Jr. Bacteriophage therapy. Antimicrob Agents Chemother. 2001;45:649-659.
48. Brüssow H. Bacteriophage therapy: potential and problems. In: Moselio S, ed. Encyclopedia of Microbiology. Oxford: Academic Press; 2009:267-273.
49. Morello E, Saussereau E, Maura D, Huerre M, Touqui L, Debarbieux L. Pulmonary bacteriophage therapy on Pseudomonas aeruginosa cystic fibrosis strains: first steps towards treatment and prevention. PLoS One. 2011;6:e16963.
50. Royce S, Rosenberg J. Chelation therapy in workers with lead exposure. West J Med. 1993;158:372-375.
51. Born T, Kontoghiorghe CN, Spyrou A, Kolnagou A, Kontoghiorghes GJ. EDTA chelation reappraisal following new clinical trials and regular use in millions of patients: review of preliminary findings and risk/benefit assessment. Toxicol Mech Methods. 2013;23:11-17.
52. Guldager B, Jelnes R, Jorgensen SJ, et al. EDTA treatment of intermittent claudication-a double-blind, placebo-controlled study. J Intern Med. 1992;231:261-267.
53. Beck FW, Prasad AS, Kaplan J, Fitzgerald JT, Brewer GJ. Changes in cytokine production and T cell subpopulations in experimentally induced zinc-deficient humans. Am J Physiol. 1997;272(6 Pt 1):E1002-E1007.
54. Han JE, Kim JH, Hwang SY, et al. Isolation and characterization of a Myoviridae bacteriophage against Staphylococcus aureus isolated from dairy cows with mastitis. Res Vet Sci. 2013;95:758-763.
55. Sahin F, Karasartova D, Ozsan TM, Gerceker D, Kiyan M. [Identification of a novel lytic bacteriophage obtained from clinical MRSA isolates and evaluation of its antibacterial activity]. Mikrobiyol Bul. 2013;47:27-34. [Turkish]
56. Bueno E, García P, Martinez B, Rodríguez A. Phage inactivation of Staphylococcus aureus in fresh and hard-type cheeses. Int J Food Microbiol. 2012;158:23-27.
57. O'Flaherty S, Ross RP, Meaney W, Fitzgerald GF, Elbreki MF, Coffey A. Potential of the polyvalent anti-Staphylococcus bacteriophage K for control of antibiotic-resistant staphylococci from hospitals. Appl Environ Microbiol. 2005;71:1836-1842.
58. Kelly D, McAuliffe O, Ross RP, Coffey A. Prevention of Staphylococcus aureus biofilm formation and reduction in established biofilm density using a combination of phage K and modified derivatives. Lett Appl Microbiol. 2012;54:286-291.
59. Chhibber S, Kaur T, Kaur S. Co-therapy using lytic bacteriophage and linezolid: effective treatment in eliminating methicillin resistant Staphylococcus aureus (MRSA) from diabetic foot infections. PLoS One. 2013;8:e56022.
60. Hsieh SE, Lo HH, Chen ST, Lee MC, Tseng YH. Wide Host range and strong lytic activity of Staphylococcus aureus lytic phage Stau2. Appl Environ Microbiol. 2011;77:756-761.
61. Sunagar R, Patil SA, Chandrakanth RK. Bacteriophage therapy for Staphylococcus aureus bacteremia in streptozotocin-induced diabetic mice. Res Microbiol. 2010;161:854-860.
62. 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;95A:117-125.
63. Seth AK, Geringer MR, Nguyen KT, et al. Bacteriophage therapy for Staphylococcus aureus biofilm-infected wounds: a new approach to chronic wound care. Plast Reconstr Surg. 2013;131:225-234.
64. Anderson GG, Moreau-Marquis S, Stanton BA, O'Toole GA. In vitro analysis of tobramycin-treated Pseudomonas aeruginosa biofilms on cystic fibrosis-derived airway epithelial cells. Infect Immun. 2008;76:1423-1433.
65. Al-Azemi A, Fielder MD, Abuknesha RA, Price RG. Effects of chelating agent and environmental stresses on microbial biofilms: relevance to clinical microbiology. J Appl Microbiol. 2011;110:1307-1313.
66. Fidalgo TK, Barcelos R, Portela MB, Soares RM, Gleiser R, Silva-Filho FC. Inhibitory activity of root canal irrigants against Candida albicans, Enterococcus faecalis and Staphylococcus aureus. Braz Oral Res. 2010;24:406-412.
67. El-Sharif AA, Hussain MHM. Chitosan-EDTA new combination is a promising candidate for treatment of bacterial and fungal infections. Curr Microbiol. 2011;62:739-745.
68. Shukla SK, Rao TS. Effect of calcium on Staphylococcus aureus biofilm architecture: a confocal laser scanning microscopic study. Colloids Surf B Biointerfaces. 2013;103:448-454.
69. Chhibber S, Kaur S, Kumari S. Therapeutic potential of bacteriophage in treating Klebsiella pneumoniae B5055-mediated lobar pneumonia in mice. J Med Microbiol. 2008;57(Pt 12):1508-1513.
70. Carmody LA, Gill JJ, Summer EJ, et al. Efficacy of bacteriophage therapy in a model of Burkholderia cenocepacia pulmonary infection. J Infect Dis. 2010;201:264-271.
71. Fukuda K, Ishida W, Uchiyama J, et al. Pseudomonas aeruginosa keratitis in mice: effects of topical bacteriophage KPP12 administration. PLoS One. 2012;7:e47742.
72. Nungester WJ, Watrous RM. Accumulation of bacteriophage in spleen and liver following its intravenous inoculation. Exp Biol Med. 1934;31:901-905.
73. Lu TK, Koeris MS. The next generation of bacteriophage therapy. Curr Opin Microbiol. 2011;14:524-531.
74. Malik R, Chhibber S. Protection with bacteriophage KO1 against fatal Klebsiella pneumoniae-induced burn wound infection in mice. J Microbiol Immunol. 2009;42:134-140.
75. Ghelardi E, Celandroni F, Gueye SA, Salvetti S, Campa M, Senesi S. Antimicrobial activity of a new preservative for multiuse ophthalmic solutions. J Ocul Pharmacol Ther. 2013;29:586-590.
76. Lee YS, Han SH, Lee SH, et al. The mechanism of antibacterial activity of tetrandrine against Staphylococcus aureus. Foodborne Pathog Dis. 2012;9:686-691.
77. Bookstaver PB, Williamson JC, Tucker BK, Raad II, Sherertz RJ. Activity of novel antibiotic lock solutions in a model against isolates of catheter-related bloodstream infections. Ann Pharmacother. 2009;43:210-219.
78. Estes R, Theusch J, Beck A, Pitrak D, Mullane KM. Activity of daptomycin with or without 25 percent ethanol compared to combinations of minocycline, EDTA, and 25 percent ethanol against methicillin-resistant Staphylococcus aureus isolates embedded in biofilm. Antimicrob Agents Chemother. 2013;57:1998-2000.
79. Hamilton-Miller JM. Damaging effects of ethylenediaminetetra-acetate and penicillins on permeability barriers in Gram-negative bacteria. Biochem J. 1966;100:675-682.
80. Vaara M. Agents that increase the permeability of the outer membrane. Microbiol Rev. 1992;56:395-411.
81. Lodish H, Berk A, Zipursky SL, Matsudaira P, Baltimore D, Darnell J. Molecular Cell Biology. Vol 4. New York: W. H. Freeman; 2000.
82. Uehara Y, Nakama H, Agematsu K, et al. Bacterial interference among nasal inhabitants: eradication of Staphylococcus aureus from nasal cavities by artificial implantation of Corynebacterium sp. J Hosp Infect. 2000;44:127-133.
83. Banin E, Brady KM, Greenberg EP. Chelator-induced dispersal and killing of Pseudomonas aeruginosa cells in a biofilm. Appl Environ Microbiol. 2006;72:2064-2069.
84. Payne RJ, Phil D, Jansen VA. Phage therapy: the peculiar kinetics of self-replicating pharmaceuticals. Clin Pharmacol Ther. 2000;68:225-230.