Activity of bacteriophages in removing biofilms of pseudomonas aeruginosa isolates from chronic rhinosinusitis patients

Frontiers in Cellular and Infection Microbiology

Volumn 7, Issue SEP, 2017, Pages

  Fong, Stephanie A ^a   Drilling, Amanda ^a   Morales, Sandra ^b   Cornet, Marjolein E ^c   Woodworth, Bradford A ^d   Fokkens, Wytske J ^c   Psaltis, Alkis J ^a   Vreugde, Sarah ^a   Wormald, Peter John ^a  

^a QUEEN ELIZABETH HOSPITAL   (Australia)

^b AmpliPhi Australia   (Australia)

^c UNIVERSITY OF AMSTERDAM   (Netherlands)

^d UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

Author keywords

Bacteriophage; Biofilm; Chronic rhinosinusitis; Cystic fibrosis; Multidrug resistant; Pseudomonas aeruginosa

Indexed keywords

CRYSTAL VIOLET; ANTIINFECTIVE AGENT;

ANTIBIOTIC RESISTANCE; ARTICLE; BACTERIOPHAGE; BIOFILM; BIOMASS DISTRIBUTION; CHRONIC RHINOSINUSITIS; CLINICAL ARTICLE; CONTROLLED STUDY; CYSTIC FIBROSIS; ENDOSCOPIC BIOPSY; HUMAN; MINIMUM INHIBITORY CONCENTRATION; MULTIDRUG RESISTANCE; MULTILOCUS SEQUENCE TYPING; NONHUMAN; NOSE POLYP; PHYLOGENY; PSEUDOMONAS AERUGINOSA; PSEUDOMONAS INFECTION; RANDOMIZED CONTROLLED TRIAL (TOPIC); SENSITIVITY ANALYSIS; STRUCTURAL BIOINFORMATICS; TREATMENT FAILURE; AUSTRALIA; COMPLICATION; DRUG EFFECTS; GENETICS; ISOLATION AND PURIFICATION; MICROBIAL SENSITIVITY TEST; MICROBIOLOGY; PHAGE THERAPY; PHYSIOLOGY; SINUSITIS; VIROLOGY;

ANTI-BACTERIAL AGENTS; AUSTRALIA; BACTERIOPHAGES; BIOFILMS; CYSTIC FIBROSIS; DRUG RESISTANCE, MULTIPLE, BACTERIAL; HUMANS; MICROBIAL SENSITIVITY TESTS; MULTILOCUS SEQUENCE TYPING; PHAGE THERAPY; PHYLOGENY; PSEUDOMONAS AERUGINOSA; PSEUDOMONAS INFECTIONS; SINUSITIS;

EID: 85031398269     PISSN: None     EISSN: 22352988     Source Type: Journal    
DOI: 10.3389/fcimb.2017.00418     Document Type: Article

References (63)

1. AURA (2016). AURA 2016: First Australian Report on Antimicrobial Use and Resistance in Human Health. Sydney, NSW: Australian Commission on Safety and Quality in Health Care (ACSQHC)
2. Aanaes, K. (2013). Bacterial sinusitis can be a focus for initial lung colonisation and chronic lung infection in patients with cystic fibrosis. J. Cyst. Fibros. 12(Suppl. 2), S1-S20. doi: 10.1016/S1569-1993(13)00150-1
3. Aanaes, K., von Buchwald, C., Hjuler, T., Skov, M., Alanin, M., and Johansen, H. K. (2013). The effect of sinus surgery with intensive follow-up on pathogenic sinus bacteria in patients with cystic fibrosis. Am. J. Rhinol. Allergy 27, e1-e4. doi: 10.2500/ajra.2013.27.3829
4. Abedon, S. (2011). "Phage therapy pharmacology: calculating phage dosing," in Advances in Applied Microbiology, Vol. 77, eds I. Allen, S. S. Laskin, and M. G. Geoffrey (San Diego, CA: Academic Press), 1-40.
5. Alemayehu, D., Casey, P. G., McAuliffe, O., Guinane, C. M., Martin, J. G., Shanahan, F., et al. (2012). Bacteriophages phiMR299-2 and phiNH-4 can eliminate Pseudomonas aeruginosa in the murine lung and on cystic fibrosis lung airway cells. MBio 3, e00029-e00012. doi: 10.1128/mBio.00029-12
6. Beeton, M. L., Alves, D. R., Enright, M. C., and Jenkins, A. T. A. (2015). Assessing phage therapy against Pseudomonas aeruginosa using a Galleria mellonella infection model. Int. J. Antimicrob. Agents 46, 196-200. doi: 10.1016/j.ijantimicag.2015.04.005
7. Bendouah, Z., Barbeau, J., Hamad, W. A., and Desrosiers, M. (2006). Biofilm formation by Staphylococcus aureus and Pseudomonas aeruginosa is associated with an unfavorable evolution after surgery for chronic sinusitis and nasal polyposis. Otolaryngol. Head Neck Surg. 134, 991-996. doi: 10.1016/j.otohns.2006.03.001
8. Chan, B. K., and Abedon, S. T. (2012). "Phage therapy pharmacology: phage cocktails," in Advances in Applied Microbiology, Vol. 78, eds I. Allen, S. S. Laskin, and M. G. Geoffrey (San Diego, CA: Academic Press), 1-23.
9. Chen, H.-H., Liu, X., Ni, C., Lu, Y.-P., Xiong, G.-Y., Lu, Y.-Y., et al. (2012). Bacterial biofilms in chronic rhinosinusitis and their relationship with inflammation severity. Auris Nasus Larynx 39, 169-174. doi: 10.1016/j.anl.2011.04.014
10. Ciofu, O., Johansen, H. K., Aanaes, K., Wassermann, T., Alhede, M., von Buchwald, C., et al. (2013). P. aeruginosa in the paranasal sinuses and transplanted lungs have similar adaptive mutations as isolates from chronically infected CF lungs. J. Cyst. Fibros. 12, 729-736. doi: 10.1016/j.jcf.2013.02.004
11. Cleland, E. J., Bassiouni, A., Vreugde, S., and Wormald, P. J. (2016). The bacterial microbiome in chronic rhinosinusitis: richness, diversity, postoperative changes, and patient outcomes. Am. J. Rhinol. Allergy 30, 37-43. doi: 10.2500/ajra.2016.30.4261
12. Cleland, E. J., Bassiouni, A., and Wormald, P. J. (2013). The bacteriology of chronic rhinosinusitis and the pre-eminence of Staphylococcus aureus in revision patients. Int. Forum Allergy Rhinol. 3, 642-646. doi: 10.1002/alr.21159
13. Cramer, N., Wiehlmann, L., Ciofu, O., Tamm, S., Høiby, N., and Tümmler, B. (2012). Molecular epidemiology of chronic Pseudomonas aeruginosa airway infections in cystic fibrosis. PLoS ONE 7:e50731. doi: 10.1371/journal.pone.0050731
14. Curran, B., Jonas, D., Crundmann, H., Pitt, T., and Dowson, C. (2004). Development of a multilocus sequence typing scheme for the opportunistic pathogen Pseudomonas aeruginosa. J. Clin. Microbiol. 42, 5644-5649. doi: 10.1128/JCM.42.12.5644-5649.2004
15. Debarbieux, L., Leduc, D., Maura, D., Morello, E., Criscuolo, A., Grossi, O., et al. (2010). Bacteriophages can treat and prevent Pseudomonas aeruginosa lung infections. J. Infect. Dis. 201, 1096-1104. doi: 10.1086/651135
16. de la Fuente-Nú-ez, C., Reffuveille, F., Fernández, L., and Hancock, R. E. W. (2013). Bacterial biofilm development as a multicellular adaptation: antibiotic resistance and new therapeutic strategies. Curr. Opin. Microbiol. 16, 580-589. doi: 10.1016/j.mib.2013.06.013
17. Doring, G., Conway, S. P., Heijerman, H. G., Hodson, M. E., Hoiby, N., Smyth, A., et al. (2000). Antibiotic therapy against Pseudomonas aeruginosa in cystic fibrosis: a European consensus. Eur. Respir. J. 16, 749-767. doi: 10.1034/j.1399-3003.2000.16d30.x
18. Drilling, A. J., Ooi, M. L., Miljkovic, D., James, C., Speck, P., Vreugde, S., et al. (2017). Long-term safety of topical Bacteriophage application to the frontal sinus region. Front. Cell. Infect. Microbiol. 7:49. doi: 10.3389/fcimb.2017.00049
19. Drilling, A., Morales, S., Boase, S., Jervis-Bardy, J., James, C., Jardeleza, C., et al. (2014a). Safety and efficacy of topical bacteriophage and ethylenediaminetetraacetic acid treatment of Staphylococcus aureus infection in a sheep model of sinusitis. Int. Forum Allergy Rhinol. 4, 176-186. doi: 10.1002/alr.21270
20. Drilling, A., Morales, S., Jardeleza, C., Vreugde, S., Speck, P., and Wormald, P.-J. (2014b). Bacteriophage reduces biofilm of Staphylococcus aureus ex vivo isolates from chronic rhinosinusitis patients. Am. J. Rhinol. Allergy 28, 3-11. doi: 10.2500/ajra.2014.28.4001
21. Edgar, R. C. (2004). MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32, 1792-1797. doi: 10.1093/nar/gkh340
22. Feil, E. J., Li, B. C., Aanensen, D. M., Hanage, W. P., and Spratt, B. G. (2004). eBURST: inferring patterns of evolutionary descent among clusters of related bacterial genotypes from multilocus sequence typing data. J. Bacteriol. 186, 1518-1530. doi: 10.1128/JB.186.5.1518-1530.2004
23. Felsenstein, J. (1985). Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39, 783-791. doi: 10.1111/j.1558-5646.1985.tb00420.x
24. Fokkens, W. J., Lund, V. J., Mullol, J., Bachert, C., Alobid, I., Baroody, F., et al. (2012). EPOS 2012: European position paper on rhinosinusitis and nasal polyps 2012. A summary for otorhinolaryngologists. Rhinology 50, 1-12. doi: 10.4193/Rhino50E2
25. Fukuda, K., Ishida, W., Uchiyama, J., Rashel, M., Kato, S., Morita, T., et al. (2012). Pseudomonas aeruginosa keratitis in mice: effects of topical bacteriophage KPP12 administration. PLoS ONE 7:e47742. doi: 10.1371/journal.pone.0047742
26. Govan, J. R., and Deretic, V. (1996). Microbial pathogenesis in cystic fibrosis: mucoid Pseudomonas aeruginosa and Burkholderia cepacia. Microbiol. Rev. 60, 539-574.
27. Grobler, A., Weitzel, E. K., Buele, A., Jardeleza, C., Cheong, Y. C., Field, J., et al. (2008). Pre- and postoperative sinus penetration of nasal irrigation. Laryngoscope 118, 2078-2081. doi: 10.1097/MLG.0b013e31818208c1
28. Guss, J., Abuzeid, W. M., Doghramji, L., Edelstein, P. H., and Chiu, A. G. (2009). Fluoroquinolone-resistant Pseudomonas aeruginosa in chronic rhinosinusitis. ORL. J. Otorhinolaryngol. Relat. Spec. 71, 263-267. doi: 10.1159/000242428
29. Guttman, B., Raya, R., and Kutter, E. (2004). "Basic phage biology," in Bacteriophages: Biology and Applications, eds E. Kutter and A. Sulakvelidze (Boca Raton, FL: CRC Press), 30-63.
30. Hall, A. R., Vos, D., Friman, V. P., Pirnay, J. P., and Buckling, A. (2012). Effects of sequential and simultaneous application of bacteriophages on populations of Pseudomonas aeruginosa in vitro and in waxmoth larvae. Appl. Environ. Microbiol. 78, 5646-5652. doi: 10.1128/AEM.00757-12.
31. Hanlon, G. W. (2007). Bacteriophages: an appraisal of their role in the treatment of bacterial infections. Int. J. Antimicrob. Agents 30, 118-128. doi: 10.1016/j.ijantimicag.2007.04.006
32. Hansen, S. K., Rau, M. H., Johansen, H. K., Ciofu, O., Jelsbak, L., Yang, L., et al. (2012). Evolution and diversification of Pseudomonas aeruginosa in the paranasal sinuses of cystic fibrosis children have implications for chronic lung infection. ISME J. 6, 31-45. doi: 10.1038/ismej.2011.83
33. Haussler, S., Tummler, B., Weissbrodt, H., Rohde, M., and Steinmetz, I. (1999). Small-colony variants of Pseudomonas aeruginosa in cystic fibrosis. Clin. Infect. Dis. 29, 621-625. doi: 10.1086/598644
34. Hawkins, C., Harper, D., Burch, D., Anggard, E., and Soothill, J. (2010). Topical treatment of Pseudomonas aeruginosa otitis of dogs with a bacteriophage mixture: a before/after clinical trial. Vet. Microbiol. 146, 309-313. doi: 10.1016/j.vetmic.2010.05.014
35. Henwood, C. J., Livermore, D. M., James, D., and Warner, M. (2001). Pseudomonas Study Group t. Antimicrobial susceptibility of Pseudomonas aeruginosa: results of a UK survey and evaluation of the British Society for Antimicrobial Chemotherapy disc susceptibility test. J. Antimicrob. Chemother. 47, 789-799. doi: 10.1093/jac/47.6.789
36. Heo, Y. J., Lee, Y. R., Jung, H. H., Lee, J., Ko, G., and Cho, Y. H. (2009). Antibacterial efficacy of phages against Pseudomonas aeruginosa infections in mice and Drosophila melanogaster. Antimicrob. Agents Chemother. 53, 2469. doi: 10.1128/AAC.01646-08
37. Johansen, H. K., Aanaes, K., Pressler, T., Nielsen, K. G., Fisker, J., Skov, M., et al. (2012). Colonisation and infection of the paranasal sinuses in cystic fibrosis patients is accompanied by a reduced PMN response. J. Cyst. Fibros. 11, 525-531. doi: 10.1016/j.jcf.2012.04.011
38. Kiewitz, C., and Tümmler, B. (2000). Sequence diversity of Pseudomonas aeruginosa: impact on population structure and Genome evolution. J. Bacteriol. 182, 3125-3135. doi: 10.1128/JB.182.11.3125-3135.2000
39. Kingdom, T. T., and Swain, R. E. (2004). The microbiology and antimicrobial resistance patterns in chronic rhinosinusitis. Am. J. Otolaryngol. 25, 323-328. doi: 10.1016/j.amjoto.2004.03.003
40. Knezevic, P., Obreht, D., Curcin, S., Petrusic, M., Aleksic, V., Kostanjsek, R., et al. (2011). Phages of Pseudomonas aeruginosa: response to environmental factors and in vitro ability to inhibit bacterial growth and biofilm formation. J. Appl. Microbiol. 111, 245-254. doi: 10.1111/j.1365-2672.2011.05043.x
41. Kutateladze, M. (2015). Experience of the Eliava Institute in bacteriophage therapy. Virol. Sin. 30, 80-81. doi: 10.1007/s12250-014-3557-0
42. Li, Z., Kosorok, M. R., Farrell, P. M., Laxova, A., West, S. E. H., Green, C. G., et al. (2005). Longitudinal development of mucoid Pseudomonas aeruginosa infection and lung disease progression in children with cystic fibrosis. JAMA 293, 581-588. doi: 10.1001/jama.293.5.581
43. Magiorakos, A. P., Srinivasan, A., Carey, R. B., Carmeli, Y., Falagas, M. E., Giske, C. G., et al. (2012). Multidrug-resistant, extensively drug-resistant and pandrug-resistant bacteria: an international expert proposal for interim standard definitions for acquired resistance. Clin. Microbiol. Infect. 18, 268-281. doi: 10.1111/j.1469-0691.2011.03570.x
44. Mastella, G., Hodson, M. E., Koch, C., Navarro, J., Rainisio, M., Harms, H. K., et al. (1999). Factors affecting velocity of lung function deterioration in ERCF cystic fibrosis patients over 2-4 years follow-up. Neth. J. Med. 54:S22. doi: 10.1016/S0300-2977(99)90050-5
45. Mazzocco, A., Waddell, T. E., Lingohr, E., and Johnson, R. P. (2009). "Enumeration of Bacteriophages Using the Small Drop Plaque Assay System," in Bacteriophages: Methods and Protocols, Vol. 1, Isolation, Characterization, and Interactions, eds M. R. J. Clokie and A. M. Kropinski (Totowa, NJ: Humana Press), 81-85.
46. Miedzybrodzki, R., Borysowski, J., Weber-Dabrowska, B., Fortuna, W., Letkiewicz, S., Szufnarowski, K., et al. (2012). "Clinical aspects of phage therapy," in Advances in Virus Research, Vol. 83, eds. Malgorzata, and S. Waclaw (San Diego, CA: Academic Press), 73-121.
47. Nichols, W. W., Dorrington, S. M., Slack, M. P., and Walmsley, H. L. (1988). Inhibition of tobramycin diffusion by binding to alginate. Antimicrob. Agents Chemother. 32, 518-523. doi: 10.1128/AAC.32.4.518
48. O'Toole, G. A. (2011). Microtiter dish biofilm formation assay. J. Vis. Exp. e2437. doi: 10.3791/2437
49. Psaltis, A. J., Ha, K. R., Beule, A. G., Tan, L. W., and Wormald, P. J. (2007). Confocal scanning laser microscopy evidence of biofilms in patients with chronic rhinosinusitis. Laryngoscope 117, 1302-1306. doi: 10.1097/MLG.0b013e31806009b0
50. Rasmussen, J., Aanaes, K., Norling, R., Nielsen, K. G., Johansen, H. K., and von Buchwald, C. (2012). CT of the paranasal sinuses is not a valid indicator for sinus surgery in CF patients. J. Cyst. Fibros. 11, 93-99. doi: 10.1016/j.jcf.2011.09.009
51. Rhoads, D. D., Wolcott, R. D., Kuskowski, M. A., Wolcott, B. M., Ward, L. S., and Sulakvelidze, A. (2009). Bacteriophage therapy of venous leg ulcers in humans: results of a phase I safety trial. J. Wound Care 18, 237-243. doi: 10.12968/jowc.2009.18.6.42801
52. Roby, B. B., McNamara, J., Finkelstein, M., and Sidman, J. (2008). Sinus surgery in cystic fibrosis patients: comparison of sinus and lower airway cultures. Int. J. Pediatr. Otorhinolaryngol. 72, 1365-1369. doi: 10.1016/j.ijporl.2008.05.011
53. Rose, T., Verbeken, G., de Vos, D., Merabishvili, M., Vaneechoutte, M., Lavigne, R., et al. (2014). Experimental phage therapy of burn wound infection: Difficult first steps. Int. J. Burns Trauma 4, 66-73.
54. Sader, H. S., Farrell, D. J., Flamm, R. K., and Jones, R. N. (2014). Antimicrobial susceptibility of Gram-negative organisms isolated from patients hospitalised with pneumonia in US and European hospitals: results from the SENTRY Antimicrobial Surveillance Program, 2009-2012. Int. J. Antimicrob. Agents 43, 328-334. doi: 10.1016/j.ijantimicag.2014.01.007
55. Sader, H. S., Huband, M. D., Castanheira, M., and Flamm, R. K. (2017). Pseudomonas aeruginosa antimicrobial susceptibility results from four years (2012 to 2015) of the international network for optimal resistance monitoring program in the United States. Antimicrob. Agents Chemother. 61:e02252-16. doi: 10.1128/AAC.02252-16
56. Sasikala, S., and Sundararaj, T. (2012). Characterization of Pseudomonas strains from sinusitis patients. BMC Infect. Dis. 12:P64. doi: 10.1186/1471-2334-12-S.1-P.64
57. Sulakvelidze, A., Alavidze, Z., and Morris, J. G. (2001). Bacteriophage Therapy. Antimicrob. Agents Chemother. 45, 649-659. doi: 10.1128/AAC.45.3.649-659.2001
58. Tamura, K., Nei, M., and Kumar, S. (2004). Prospects for inferring very large phylogenies by using the neighbor-joining method. Proc. Natl. Acad. Sci. U.S.A 101, 11030-11035. doi: 10.1073/pnas.0404206101
59. Tamura, K., Stecher, G., Peterson, D., Filipski, A., and Kumar, S. (2013). MEGA6: molecular evolutionary genetics analysis version 6.0. Mol. Biol. Evol. 30, 2725-2729. doi: 10.1093/molbev/mst197
60. Vilas Boas, D., Almeida, C., Sillankorva, S., Nicolau, A., Azeredo, J., and Azevedo, N. F. (2016). Discrimination of bacteriophage infected cells using locked nucleic acid fluorescent in situ hybridization (LNA-FISH). Biofouling 32, 179-190. doi: 10.1080/08927014.2015.1131821
61. Wiegand, I., Hilpert, K., and Hancock, R. E. W. (2008). Agar and broth dilution methods to determine the minimal inhibitory concentration (MIC) of antimicrobial substances. Nat. Protocols 3, 163-175. doi: 10.1038/nprot.2007.521
62. Worley-Morse, T. O., Zhang, L., and Gunsch, C. K. (2014). The long-term effects of phage concentration on the inhibition of planktonic bacterial cultures. Env. Sci. Process. Impacts 16, 81-87. doi: 10.1039/C3EM00427A
63. Wright, A., Hawkins, C. H., Anggard, E. E., and Harper, D. R. (2009). 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. 34, 349-357. doi: 10.1111/j.1749-4486.2009.01973.x