Ecology of anti-biofilm agents II: Bacteriophage exploitation and biocontrol of biofilm bacteria

Pharmaceuticals

Volumn 8, Issue 3, 2015, Pages 559-589

  Abedon, Stephen T ^a  

^a OHIO STATE UNIVERSITY   (United States)

Author keywords

Bacteriophage ecology; Biocontrol; Biofilm control; Biofilm eradication; Biofilms; Ecology; Phage ecology; Phage therapy

Indexed keywords

ANTIBIOFILM AGENT; ANTIBIOTIC AGENT; ANTIINFECTIVE AGENT; UNCLASSIFIED DRUG;

BACTERIAL INFECTION; BACTERIOPHAGE; BIOFILM; CONCENTRATION (PARAMETERS); ECOLOGY; ECOSYSTEM; IMMUNE RESPONSE; NONHUMAN; POPULATION DYNAMICS; POPULATION GROWTH; REVIEW; STEADY STATE;

EID: 84941202270     PISSN: None     EISSN: 14248247     Source Type: Journal    
DOI: 10.3390/ph8030559     Document Type: Review

References (167)

1. Diaz-Munoz, S.L.; Koskella, B. Bacteria-phage interactions in natural environments. Adv. Appl. Microbiol. 2014, 89, 135–183.
2. Whitman, W.B.; Coleman, D.C.; Wiebe, W.J. Prokaryotes: The unseen majority. Proc. Natl. Acad. Sci. U.S.A. 1998, 95, 6578–6583.
3. Karner, M.B.; DeLong, E.F.; Karl, D.M. Archaeal dominance in the mesopelagic zone of the Pacific Ocean. Nature 2001, 409, 507–510.
4. Lipp, J.S.; Morono, Y.; Inagaki, F.; Hinrichs, K.U. Significant contribution of Archaea to extant biomass in marine subsurface sediments. Nature 2008, 454, 991–994.
5. Lloyd, K.G.; May, M.K.; Kevorkian, R.T.; Steen, A.D. Meta-analysis of quantification methods shows that archaea and bacteria have similar abundances in the subseafloor. Appl. Environ. Microbiol. 2013, 79, 7790–7799.
6. Hall, M.R.; McGillicuddy, E.; Kaplan, L.J. Biofilm: Basic principles, pathophysiology, and implications for clinicians. Surg. Infect. 2014, 15, 1–7.
7. Flemming, H.C.; Wingender, J. The biofilm matrix. Nat. Rev. Microbiol. 2010, 8, 623–633.
8. Bjarnsholt, T. The role of bacterial biofilms in chronic infections. APMIS, 2013, 121, 1–58.
9. Scali, C.; Kunimoto, B. An update on chronic wounds and the role of biofilms. J. Cutan. Med. Surg. 2013, 17, 371–376.
10. Cooper, R.A.; Bjarnsholt, T.; Alhede, M. Biofilms in wounds: A review of present knowledge. J. Wound Care 2014, 23, 570–580.
11. Macia, M.D.; Rojo-Molinero, E.; Oliver, A. Antimicrobial susceptibility testing in biofilm-growing bacteria. Clin. Microbiol. Infect. 2014, 20, 981–990.
12. Solheim, H.T.; Sekse, C.; Urdahl, A.M.; Wasteson, Y.; Nesse, L.L. Biofilm as an environment for dissemination of stx genes by transduction. Appl. Environ. Microbiol. 2013, 79, 896–900.
13. Costerton, J.; Stewart, P.; Greenberg, E. Bacterial biofilms: A common cause of persistent infections. Science 1999, 284, 1318–1322.
14. Matz, C. Biofilms as refuge against predation. In The Biofilm Mode of Life: Mechanisms and Adaptations; Kjelleberg, S., Givskov, M., Eds.; Horizon Bioscience: Norfolk, UK, 2007; pp. 195–213.
15. Abedon, S.T. Bacteriophages and Biofilms: Ecology, Phage Therapy, Plaques; Nova Science Publishers: New York, NY, USA, 2011.
16. Abedon, S.T. Spatial vulnerability: Bacterial arrangements, microcolonies, and biofilms as responses to low rather than high phage densities. Viruses 2012, 4, 663–687.
17. Abedon, S.T. Thinking about microcolonies as phage targets. Bacteriophage 2012, 2, 200–204.
18. Chan, B.K.; Abedon, S.T. Bacteriophages and their enzymes in biofilm control. Curr. Pharm. Des. 2015, 21, 85–99.
19. Abedon, S.T. Ecology of anti-biofilm agents I. Antibiotics versus bacteriophages. Pharmaceuticals, 2015, 8, 525–588.
20. Harper, D.R. Biological control by microorganisms. In The Encyclopedia of Life Sciences; John Wiley & Sons: Chichester, UK, 2006; pp. 1–10.
21. Abedon, S.T. Kinetics of phage-mediated biocontrol of bacteria. Foodborne Pathog. Dis. 2009, 6, 807–815.
22. Hyman, P.; Abedon, S.T. Bacteriophages in Health and Disease; CABI Press: Wallingford, UK, 2012.
23. Borysowski, J.; Miedzybrodzki, R.; Górski, A. Phage Therapy: Current Research and Applications; Caister Academic Press: Norfolk, UK, 2014.
24. Brüssow, H. Bacteriophage-host interaction: From splendid isolation into a messy reality. Curr. Opin. Microbiol. 2013, 16, 500–506.
25. Fan, X.; Li, W.; Zheng, F.; Xie, J. Bacteriophage inspired antibiotics discovery against infection involved biofilm. Crit. Rev. Eukaryot. Gene Expr. 2013, 23, 317–326.
26. Harper, D.R.; Parracho, H.M. R.; Walker, J.; Sharp, R.; Hughes, G.; Werthrén, M.; Lehman, S.; Morales, S. Bacteriophages and biofilms. Antibiotics 2014, 3, 270–284.
27. Parasion, S.; Kwiatek, M.; Gryko, R.; Mizak, L.; Malm, A. Bacteriophages as an alternative strategy for fighting biofilm development. Pol. J. Microbiol. 2014, 63, 137–145.
28. Sillankorva, S.; Azeredo, J. Bacteriophage attack as an anti-biofilm strategy. Methods Mol. Biol. 2014, 1147, 277–285.
29. Sillankorva, S.; Azeredo, J. The use of bacteriophages and bacteriophage-derived enzymes for clinically relevant biofilm control. In Phage Therapy: Current Research and Applications; Borysowski, J., Miedzybrodzki, R., Górski, A., Eds.; Caister Academic Press: Norfolk, UK, 2014.
30. Abedon, S.T.; Thomas-Abedon, C. Phage therapy pharmacology. Curr. Pharm. Biotechnol. 2010, 11, 28–47.
31. Abedon, S. Phage therapy pharmacology: Calculating phage dosing. Adv. Appl. Microbiol. 2011, 77, 1–40.
32. Hyman, P.; Abedon, S.T. Bacteriophage host range and bacterial resistance. Adv. Appl. Microbiol. 2010, 70, 217–248.
33. Labrie, S.J.; Samson, J.E.; Moineau, S. Bacteriophage resistance mechanisms. Nat. Rev. Microbiol. 2010, 8, 317–327.
34. Friman, V.P.; Buckling, A. Phages can constrain protist predation-driven attenuation of Pseudomonas aeruginosa virulence in multienemy communities. ISME. J. 2014, 8, 1820–1830.
35. Ly, M.; Abeles, S.R.; Boehm, T.K.; Robles-Sikisaka, R.; Naidu, M.; Santiago-Rodriguez, T.; Pride, D.T. Altered oral viral ecology in association with periodontal disease. MBio. 2014, 5, doi: 10.1128/mBio.01133-14.
36. Zhang, J.; Ormala-Odegrip, A.M.; Mappes, J.; Laakso, J. Top-down effects of a lytic bacteriophage and protozoa on bacteria in aqueous and biofilm phases. Ecol. Evol. 2014, 4, 4444–4453.
37. Rodriguez-Brito, B.; Li, L.; Wegley, L.; Furlan, M.; Angly, F.; Breitbart, M.; Buchanan, J.; Desnues, C.; Dinsdale, E.; Edwards, R. et al. Viral and microbial community dynamics in four aquatic environments. ISME J. 2010, 4, 739–751.
38. Winter, C.; Bouvier, T.; Weinbauer, M.G.; Thingstad, T.F. Trade-offs between competition and defense specialists among unicellular planktonic organisms: The "killing the winner" hypothesis revisited. Microbiol. Mol. Biol. Rev. 2010, 74, 42–57.
39. Costerton, J.W.; Cheng, J.-J.; Geesey, G.G.; Ladd, T.I.; Nickel, J.C.; Dasgupta, M.; Marrie, T.J. Bacterial biofilms in nature and disease. Ann. Rev. Microbiol. 1987, 41, 435–464.
40. Costerton, J.W.; Lewandowski, Z.; Caldwell, D.E.; Korber, D.R.; Lappin-Scott, H.M. Microbial biofilms. Ann. Rev. Microbiol. 1995, 49, 711–745.
41. Tait, K.; Sutherland, I.W. Antagonistic interactions amongst bacteriocin-producing enteric bacteria in dual species biofilms. J. Appl. Microbiol. 2002, 93, 345–352.
42. Rao, D.; Webb, J.S.; Kjelleberg, S. Competitive interactions in mixed-species biofilms containing the marine bacterium Pseudoalteromonas tunicata. Appl. Environ. Microbiol. 2005, 71, 1729–1736.
43. Chan, B.K.; Abedon, S.T. Bacteriophage adaptation, with particular attention to issues of phage host range. In Bacteriophages in Dairy Processing; Quiberoni, A., Reinheimer, J., Eds.; Nova Science Publishers: New York, NY, USA, 2012; pp. 25–52.
44. Bohannan, B.J. M.; Lenski, R.E. Effect of resource enrichment on a chemostat community of bacteria and bacteriophage. Ecology 1997, 78, 2303–2315.
45. Pace, M.L.; Cole, J.J. Comparative and experimental approaches to top-down and bottom-up regulation of bacteria. Microb. Ecol. 1994, 28, 181–193.
46. Abedon, S.T.; Culler, R.R. Optimizing bacteriophage plaque fecundity. J. Theor. Biol. 2007, 249, 582–592.
47. Anderson, T.F. Bacteriophages and their action on host cells. In Research in Medical Science; Green, D.E., Knox, W.E., Eds.; Macmillan: New York, 1950; pp. 1–16.
48. Bjarnsholt, T.; Alhede, M.; Alhede, M.; Eickhardt-Sorensen, S.R.; Moser, C.; Kuhl, M.; Jensen, P.O.; Hoiby, N. The in vivo biofilm. Trends Microbiol. 2013, 21, 466–474.
49. Barr, J.J.; Auro, R.; Furlan, M.; Whiteson, K.L.; Erb, M.L.; Pogliano, J.; Stotland, A.; Wolkowicz, R.; Cutting, A.S.; Doran, K.S. et al. Bacteriophage adhering to mucus provide a non-host-derived immunity. Proc. Natl. Acad. Sci. U.S.A. 2013, 110, 10771–10776.
50. Barr, J.J.; Youle, M.; Rohwer, F. Innate and acquired bacteriophage-mediated immunity. Bacteriophage 2013, 3, e25857.
51. Gorski, A.; Dabrowska, K.; Hodyra-Stefaniak, K.; Borysowski, J.; Miedzybrodzki, R.; Weber-Dabrowska, B. Phages targeting infected tissues: novel approach to phage therapy. Future Microbiol. 2015, 10, 199–204.
52. Abedon, S.T. Bacteriophage secondary infection. Virol. Sin. 2015, 30, 3–10.
53. Stewart, P.S.; Franklin, M.J. Physiological heterogeneity in biofilms. Nat. Rev. Microbiol. 2008, 6, 199–210.
54. Abedon, S.T. Disambiguating bacteriophage pseudolysogeny: An historical analysis of lysogeny, pseudolysogeny, and the phage carrier state. In Contemporary Trends in Bacteriophage Research; Adams, H.T., Ed.; Nova Science Publishers: Hauppauge, New York, NY, USA, 2009; pp. 285–307.
55. Moons, P.; Faster, D.; Aertsen, A. Lysogenic conversion and phage resistance development in phage exposed Escherichia coli biofilms. Viruses 2013, 5, 150–161.
56. Weitz, J.S.; Mileyko, Y.; Joh, R.I.; Voit, E.O. Collective decision making in bacterial viruses. Biophys. J. 2008, 95, 2673–2680.
57. Abedon, S.T.; Yin, J. Impact of spatial structure on phage population growth. In Bacteriophage Ecology; Abedon, S.T., Ed.; Cambridge University Press: Cambridge, UK, 2008; pp. 94–113.
58. Abedon, S.T. Communication among phages, bacteria, and soil environments. In Biocommunication of Soil Microorganisms; Witzany, G., Ed.; Springer: New York, NY, USA, 2011; pp. 37–65.
59. Kutter, E.; Kellenberger, E.; Carlson, K.; Eddy, S.; Neitzel, J.; Messinger, L.; North, J.; Guttman, B. Effects of bacterial growth conditions and physiology on T4 infection. In The Molecular Biology of Bacteriophage T4; Karam, J.D., Kutter, E., Carlson, K.; Guttman, B., Eds.; ASM Press: Washington, DC, USA, 1994; pp. 406–418.
60. Miller, R.V.; Day, M. Contribution of lysogeny, pseudolysogeny, and starvation to phage ecology. In Bacteriophage Ecology; Abedon, S.T., Ed.; Cambridge University Press: Cambridge, UK, 2008; pp. 114–143.
61. Golec, P.; Karczewska-Golec, J.; Łoś, M.; Węgrzyn, G. Bacteriophage T4 can produce progeny virions in extremely slowly growing Escherichia coli host: Comparison of a mathematical model with the experimental data. FEMS Microbiol. Lett. 2014, 351, 156–161.
62. Heilmann, S.; Sneppen, K.; Krishna, S. Coexistence of phage and bacteria on the boundary of self-organized refuges. Proc. Natl. Acad. Sci. U.S.A. 2012, 109, 12828–12833.
63. Borer, E.T.; Halpern, B.S.; Seabloom, E.W. Asymmetry in community regulation: Effects of predators and productivity. Ecology 2006, 87, 2813–2820.
64. Kutter, E.; De Vos, D.; Gvasalia, G.; Alavidze, Z.; Gogokhia, L.; Kuhl, S.; Abedon, S.T. Phage therapy in clinical practice: Treatment of human infections. Curr. Pharm. Biotechnol. 2010, 11, 69–86.
65. Abedon, S.T.; Kuhl, S.J.; Blasdel, B.G.; Kutter, E.M. Phage treatment of human infections. Bacteriophage 2011, 1, 66–85.
66. Abedon, S.T. Phage therapy of pulmonary infections. Bacteriophage 2015, 5, e1020260-1–e1020260-13.
67. Ślopek, S.; Weber-Dąbrowska, B.; Dąbrowski, M.; Kucharewicz-Krukowska, A. Results of bacteriophage treatment of suppurative bacterial infections in the years 1981–1986. Arch. Immunol. Ther. Exp. 1987, 35, 569–583.
68. Weber-Dąbrowska, B.; Mulczyk, M.; Górski, A. Bacteriophage therapy of bacterial infections: An update of our institute’s experience. Arch. Immunol. Ther. Exp. 2000, 48, 547–551.
69. Thawal, N.D.; Yele, A.B.; Sahu, P.K.; Chopade, B.A. Effect of a novel podophage AB7-IBB2 on Acinetobacter baumannii biofilm. Curr. Microbiol. 2012, 65, 66–72.
70. Mendes, J.J.; Leandro, C.; Mottola, C.; Barbosa, R.; Silva, F.A.; Oliveira, M.; Vilela, C.L.; Melo-Cristino, J.; Gorski, A.; Pimentel, M.; Sao-Jose, C.; Cavaco-Silva, P.; Garcia, M. In vitro design of a novel lytic bacteriophage cocktail with therapeutic potential against organisms causing diabetic foot infections. J. Med. Microbiol. 2014, 63, 1055–1065.
71. Goldman, G.; Starosvetsky, J.; Armon, R. Inhibition of biofilm formation on UF membrane by use of specific bacteriophages. J. Membr. Sci. 2009, 342, 145–152.
72. Castillo-Ruiz, M.; Vines, E.D.; Montt, C.; Fernandez, J.; Delgado, J.M.; Hormazabal, J.C.; Bittner, M. Isolation of a novel Aggregatibacter actinomycetemcomitans serotype b bacteriophage capable of lysing bacteria within a biofilm. Appl. Environ. Microbiol. 2011, 77, 3157–3159.
73. Belgini, D.R.; Dias, R.S.; Siqueira, V.M.; Valadares, L.A.; Albanese, J.M.; Souza, R.S.; Torres, A.P.; Sousa, M.P.; Silva, C.C.; De Paula, S.O. et al. Culturable bacterial diversity from a feed water of a reverse osmosis system, evaluation of biofilm formation and biocontrol using phages. World J. Microbiol. Biotechnol. 2014, 30, 2689–2700.
74. Siringan, P.; Connerton, P.L.; Payne, R.J.; Connerton, I.F. Bacteriophage-mediated dispersal of Campylobacter jejuni biofilms. Appl. Environ. Microbiol. 2011, 77, 3320–3326.
75. Gong, C.; Jiang, X. Application of bacteriophages to reduce biofilms formed by hydrogen sulfide producing bacteria on surfaces in a rendering plant. Can. J. Microbiol. 2015, 61, 539–544.
76. Bhattacharjee, A.S.; Choi, J.D.; Motlagh, A.M.; Mukherji, S.T.; Goel, R. Bacteriophage therapy for membrane biofouling in membrane bioreactors and antibiotic-resistant bacterial biofilms. Biotech. Bioeng. 2015, 112, 1644–1654.
77. Hughes, K.A.; Sutherland, I.W.; Jones, M.V. Biofilm susceptibility to bacteriophage attack: The role of phage-borne polysaccharide depolymerase. Microbiology 1998, 144, 3039–3047.
78. Tait, K.; Skilman, L.C.; Sutherland, I.W. The efficacy of bacteriophage as a method of biofilm eradication. Biofouling 2002, 18, 305–311.
79. Khalifa, L.; Brosh, Y.; Gelman, D.; Coppenhagen-Glazer, S.; Beyth, S.; Poraduso-Cohen, R.; Que, Y.A.; Beyth, N.; Hazan, R. Targeting Enterococcus faecalis biofilm using phage therapy. Appl. Environ. Microbiol. 2015, 81, 2696–2705.
80. Doolittle, M.M.; Cooney, J.J.; Caldwell, D.E. Lytic infection of Escherichia coli biofilms by bacteriophage T 4. Can. J. Microbiol. 1995, 41, 12–18.
81. Doolittle, M.M.; Cooney, J.J.; Caldwell, D.E. Tracing the interaction of bacteriophage with bacterial biofilms using fluorescent and chromogenic probes. J. Indust. Microbiol. 1996, 16, 331–341.
82. Corbin, B.D.; McLean, R.J. C.; Aron, G.M. Bacteriophage T4 multiplication in a glucose-limited Escherichia coli biofilm. Can. J. Microbiol. 2001, 47, 680–684.
83. Sharma, M.; Ryu, J.H.; Beuchat, L.R. Inactivation of Escherichia coli O157:H7 in biofilm on stainless steel by treatment with an alkaline cleaner and a bacteriophage. J. Appl. Microbiol. 2005, 99, 449–459.
84. Moons, P.; Werckx, W.; van Houdt, R.; Aertsen, A.; Michiels, C.W. Resistance development of bacterial biofilms against bacteriophage attack. Commun. Agric. Appl. Biol. Sci. 2006, 71, 297–300.
85. Lu, T.K.; Collins, J.J. Dispersing biofilms with engineered enzymatic bacteriophage. Proc. Natl. Acad. Sci. U.S.A. 2007, 104, 11197–11202.
86. Lu, T.K.; Collins, J.J. Engineered bacteriophage targeting gene networks as adjuvants for antibiotic therapy. Proc. Natl. Acad. Sci. U.S.A. 2009, 106, 4629–4634.
87. Carson, L.; Gorman, S.P.; Gilmore, B.F. 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.
88. Kay, M.K.; Erwin, T.C.; McLean, R.J.; Aron, G.M. Bacteriophage ecology in Escherichia coli and Pseudomonas aeruginosa mixed biofilm communities. Appl. Environ. Microbiol. 2011, 77, 821–829.
89. Chibeu, A.; Lingohr, E.J.; Masson, L.; Manges, A.; Harel, J.; Ackermann, H.W.; Kropinski, A.M.; Boerlin, P. Bacteriophages with the ability to degrade uropathogenic Escherichia coli biofilms. Viruses 2012, 4, 471–487.
90. Ryan, E.M.; Alkawareek, M.Y.; Donnelly, R.F.; Gilmore, B.F. Synergistic phage-antibiotic combinations for the control of Escherichia coli biofilms in vitro. FEMS Immunol. Med. Microbiol. 2012, 65, 395–398.
91. Hosseinidoust, Z.; Tufenkji, N.; van de Ven, T.G. Formation of biofilms under phage predation: Considerations concerning a biofilm increase. Biofouling 2013, 29, 457–468.
92. Coulter, L.B.; McLean, R.J.; Rohde, R.E.; Aron, G.M. Effect of bacteriophage infection in combination with tobramycin on the emergence of resistance in Escherichia coli and Pseudomonas aeruginosa biofilms. Viruses 2014, 6, 3778–3786.
93. Pei, R.; Lamas-Samanamud, G.R. Inhibition of biofilm formation by T7 bacteriophages producing quorum quenching enzymes. Appl. Environ. Microbiol. 2014, 80, 5340–5348.
94. Schmerer, M.; Molineux, I.J.; Ally, D.; Tyerman, J.; Cecchini, N.; Bull, J.J. Challenges in predicting the evolutionary maintenance of a phage transgene. J. Biol. Eng. 2014, 8, 21.
95. Bedi, M.S.; Verma, V.; Chhibber, S. Amoxicillin and specific bacteriophage can be used together for eradication of biofilm of Klebsiella pneumoniae B 5055. World J. Microbiol. Biotechnol. 2009, 25, 1145–1151.
96. Verma, V.; Harjai, K.; Chhibber, S. Restricting ciprofloxacin-induced resistant variant formation in biofilm of Klebsiella pneumoniae B5055 by complementary bacteriophage treatment. J. Antimicrob. Chemother. 2009, 64, 1212–1218.
97. Verma, V.; Harjai, K.; Chhibber, S. Structural changes induced by a lytic bacteriophage make ciprofloxacin effective against older biofilm of Klebsiella pneumoniae. Biofouling 2010, 26, 729–737.
98. Chhibber, S.; Nag, D.; Bansal, S. Inhibiting biofilm formation by Klebsiella pneumoniae B5055 using an iron antagonizing molecule and a bacteriophage. Bmc Microbiol. 2013, 13, 174.
99. Chhibber, S.; Bansal, S.; Kaur, S. Disrupting the mixed species biofilm of Klebsiella pneumoniae B5055 and Pseudomonas aeruginosa PAO using bacteriophages alone or in combination with xylitol. Microbiology 2015, 161, 1369–1377.
100. Jamal, M.; Hussain, T.; Das, C.R.; Andleeb, S. Characterization of Siphoviridae phage Z and studying its efficacy against multidrug-resistant Klebsiella pneumoniae planktonic cells and biofilm. J. Med. Microbiol. 2015, 64, 454–462.
101. Roy, B.; Ackermann, H.-W.; Pandian, S.; Picard, G.; Goulet, J. Biological inactivation of adhering Listeria monocytogenes by listeriaphages and a quaternary ammonium compound. Appl. Environ. Microbiol. 1993, 59, 2914–2917.
102. Hibma, A.M.; Jassim, S.A.; Griffiths, M.W. Infection and removal of L-forms of Listeria monocytogenes with bred bacteriophage. Int. J. Food Microbiol. 1997, 34, 197–207.
103. Soni, K.A.; Nannapaneni, R. Removal of Listeria monocytogenes biofilms with bacteriophage P 100. J. Food Prot. 2010, 73, 1519–1524.
104. Montanez-Izquierdo, V.Y.; Salas-Vazquez, D.I.; Rodriguez-Jerez, J.J. Use of epifluorescence microscopy to assess the effectiveness of phage P100 in controlling Listeria monocytogenes biofilms on stainless steel surfaces. Food Control 2012, 23, 470–477.
105. Ganegama Arachchi, G.J.; Cridge, A.G.; Dias-Wanigasekera, B.M.; Cruz, C.D.; McIntyre, L.; Liu, R.; Flint, S.H.; Mutukumira, A.N. Effectiveness of phages in the decontamination of Listeria monocytogenes adhered to clean stainless steel, stainless steel coated with fish protein, and as a biofilm. J. Ind. Microbiol. Biotechnol. 2013, 40, 1105–1116.
106. Chaitiemwong, N.; Hazeleger, W.C.; Beumer, R.R. Inactivation of Listeria monocytogenes by disinfectants and bacteriophages in suspension and stainless steel carrier tests. J. Food Prot. 2014, 77, 2012–2020.
107. Lehman, S.M.; Donlan, R.M. Bacteriophage-mediated control of a two-species biofilm formed by microorganisms causing catheter-associated urinary tract infections in an in vitro urinary catheter model. Antimicrob. Agents Chemother. 2015, 59, 1127–1137.
108. Hanlon, G.W.; Denyer, S.P.; Olliff, C.J.; Ibrahim, L.J. Reduction in exopolysaccharide viscosity as an aid to bacteriophage penetration through Pseudomonas aeruginosa biofilms. Appl. Environ. Microbiol. 2001, 67, 2746–2753.
109. Knezevic, P.; Petrovic, O. A colorimetric microtiter plate method for assessment of phage effect on Pseudomonas aeruginosa biofilm. J. Microbiol. Meth. 2008, 74, 114–118.
110. Fu, W.; Forster, T.; Mayer, O.; Curtin, J.J.; Lehman, S.M.; Donlan, R.M. 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.
111. Ahiwale, S.; Tamboli, N.; Thorat, K.; Kulkarni, R.; Ackermann, H.; Kapadnis, B. In vitro management of hospital Pseudomonas aeruginosa biofilm using indigenous T7-like lytic phage. Curr. Microbiol. 2011, 62, 335–340.
112. Knezevic, P.; Obreht, D.; Curcin, S.; Petrusic, M.; Aleksic, V.; Kostanjsek, R.; Petrovic, O. Phages of Pseudomonas aeruginosa: Response to environmental factors and in vitro ability to inhibit bacterial growth and biofilm formation. J. Appl. Microbiol. 2011, 111, 245–254.
113. Pires, D.; Sillankorva, S.; Faustino, A.; Azeredo, J. Use of newly isolated phages for control of Pseudomonas aeruginosa PAO1 and ATCC 10145 biofilms. Res. Microbiol. 2011, 162, 798–806.
114. Alemayehu, D.; Casey, P.G.; McAuliffe, O.; Guinane, C.M.; Martin, J.G.; Shanahan, F.; Coffey, A.; Ross, R.P.; Hill, C. Bacteriophages ϕMR299-2 and ϕNH-4 can eliminate Pseudomonas aeruginosa in the murine lung and on cystic fibrosis lung airway cells. MBio 2012, 3, e00029-12.
115. Liao, K.S.; Lehman, S.M.; Tweardy, D.J.; Donlan, R.M.; Trautner, B.W. Bacteriophages are synergistic with bacterial interference for the prevention of Pseudomonas aeruginosa biofilm formation on urinary catheters. J. Appl. Microbiol. 2012, 113, 1530–1539.
116. Phee, A.; Bondy-Denomy, J.; Kishen, A.; Basrani, B.; Azarpazhooh, A.; Maxwell, K. Efficacy of bacteriophage treatment on Pseudomonas aeruginosa biofilms. J Endod. 2013, 39, 364–369.
117. Yilmaz, C.; Colak, M.; Yilmaz, B.C.; Ersoz, G.; Kutateladze, M.; Gozlugol, M. Bacteriophage therapy in implant-related infections: an experimental study. J. Bone Joint Surg. Am. 2013, 95, 117–125.
118. Zhang, Y.; Hu, Z. Combined treatment of Pseudomonas aeruginosa biofilms with bacteriophages and chlorine. Biotechnol. Bioeng. 2013, 110, 286–295.
119. Zhang, Y.; Hunt, H.K.; Hu, Z. Application of bacteriophages to selectively remove Pseudomonas aeruginosa in water and wastewater filtration systems. Water Res. 2013, 47, 4507–4518.
120. Danis-Wlodarczyk, K.; Olszak, T.; Arabski, M.; Wasik, S.; Majkowska-Skrobek, G.; Augustyniak, D.; Gula, G.; Briers, Y.; Jang, H.B.; Vandenheuvel, D. et al. Characterization of the newly isolated lytic bacteriophages KTN6 and KT28 and their efficacy against Pseudomonas aeruginosa biofilm. PLoS ONE 2015, 10, e0127603, doi: 10.1371/journal.pone.0127603.
121. Sillankorva, S.; Oliveira, R.; Vieira, M.J.; Sutherland, I.W.; Azeredo, J. Bacteriophage Φ S1 infection of Pseudomonas fluorescens planktonic cells versus biofilms. Biofouling 2004, 20, 133–138.
122. Sillankorva, S.; Oliveira, R.; Vieira, M.J.; Azeredo, J. Real-time quantification of Pseudomonas fluorescens cell removal from glass surfaces due to bacteriophage φS1 application. J. Appl. Microbiol. 2008, 105, 196–202.
123. Sillankorva, S.; Neubauer, P.; Azeredo, J. Pseudomonas fluorescens biofilms subjected to phage phiIBB-PF7A. Bmc Biotechnol. 2008, 8, 79.
124. Sillankorva, S.; Neubauer, P.; Azeredo, J. Phage control of dual species biofilms of Pseudomonas fluorescens and Staphylococcus lentus. Biofouling 2010, 26, 567–575.
125. Cornelissen, A.; Ceyssens, P.J.; T'Syen, J.; Van, P.H.; Noben, J.P.; Shaburova, O.V.; Krylov, V.N.; Volckaert, G.; Lavigne, R. The T7-related Pseudomonas putida phage φ15 displays virion-associated biofilm degradation properties. PLoS ONE 2011, 6, e18597, doi: 10.1371/journal.pone.0018597.
126. Gino, E.; Starosvetsky, J.; Kurzbaum, E.; Armon, R. Combined chemical-biological treatment for prevention/rehabilitation of clogged wells by an iron-oxidizing bacterium. Environ. Sci. Technol. 2010, 44, 3123–3129.
127. Del Pozo, J.L.; Alonso, M.; Arciola, C.R.; Gonzalez, R.; Leiva, J.; Lasa, I.; Penades, J. Biotechnological war against biofilms. Could phages mean the end of device-related infections? Int. J. Artif. Organs 2007, 30, 805–812.
128. Son, J.S.; Lee, S.J.; Jun, S.Y.; Yoon, S.J.; Kang, S.H.; Paik, H.R.; Kang, J.O.; Choi, Y.J. Antibacterial and biofilm removal activity of a podoviridae Staphylococcus aureus bacteriophage SAP-2 and a derived recombinant cell-wall-degrading enzyme. Appl. Microbiol. Biotechnol. 2010, 86, 1439–1449.
129. Rahman, M.; Kim, S.; Kim, S.M.; Seol, S.Y.; Kim, J. Characterization of induced Staphylococcus aureus bacteriophage SAP-26 and its anti-biofilm activity with rifampicin. Biofouling 2011, 27, 1087–1093.
130. Kelly, D.; McAuliffe, O.; Ross, R.P.; 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.
131. Seth, A.K.; Geringer, M.R.; Nguyen, K.T.; Agnew, S.P.; Dumanian, Z.; Galiano, R.D.; Leung, K.P.; Mustoe, T.A.; Hong, S.J. Bacteriophage therapy for Staphylococcus aureus biofilm-infected wounds: a new approach to chronic wound care. Plast. Reconstr. Surg. 2013, 131, 225–234.
132. Lungren, M.P.; Christensen, D.; Kankotia, R.; Falk, I.; Paxton, B.E.; Kim, C.Y. Bacteriophage K for reduction of Staphylococcus aureus biofilm on central venous catheter material. Bacteriophage 2013, 3, e26825.
133. Alves, D.R.; Gaudion, A.; Bean, J.E.; Perez-Esteban, P.; Arnot, T.; Harper, D.R.; Kot, W.; Hansen, L.H.; Enright, M.C.; Jenkins, A.T. Combined use of bacteriophage K and a novel bacteriophage to reduce Staphylococcus aureus biofilm. Appl. Environ. Microbiol. 2014, 80, 6694–6703.
134. Drilling, A.; Morales, S.; Boase, S.; Jervis-Bardy, J.; James, C.; Jardeleza, C.; Tan, N.C.; Cleland, E.; Speck, P.; Vreugde, S. et al. Safety and efficacy of topical bacteriophage and ethylenediaminetetraacetic acid treatment of Staphylococcus aureus infection in a sheep model of sinusitis. Int. Forum Allergy Rhinol. 2014, 4, 176–186.
135. Drilling, A.; Morales, S.; Jardeleza, C.; Vreugde, S.; Speck, P.; Wormald, P.J. Bacteriophage reduces biofilm of Staphylococcus aureus ex vivo isolates from chronic rhinosinusitis patients. Am. J. Rhinol. Allergy 2014, 28, 3–11.
136. Lungren, M.P.; Donlan, R.M.; Kankotia, R.; Paxton, B.E.; Falk, I.; Christensen, D.; Kim, C.Y. Bacteriophage K antimicrobial-lock technique for treatment of Staphylococcus aureus central venous catheter-related infection: a leporine model efficacy analysis. J. Vasc. Interv. Radiol. 2014, 25, 1627–1632.
137. Gutierrez, D.; Vandenheuvel, D.; Martinez, B.; Rodriguez, A.; Lavigne, R.; Garcia, P. Two phages, phiIPLA-RODI and phiIPLA-C1C, lyse mono- and dual-species staphylococcal biofilms. Appl. Environ. Microbiol. 2015, 81, 3336–3348.
138. Wood, H.L.; Holden, S.R.; Bayston, R. Susceptibility of Staphylococcus epidermidis biofilm in CSF shunts to bacteriophage attack. Eur. J. Ped. Surgery 2001, 11, S56–S57.
139. Curtin, J.J.; Donlan, R.M. Using bacteriophages to reduce formation of catheter-associated biofilms by Staphylococcus epidermidis. Antimicrob. Agents Chemother. 2006, 50, 1268–1275.
140. Cerca, N.; Oliveria, 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.
141. Tan, D.; Dahl, A.; Middelboe, M. Vibriophages differentially influence biofilm formation by Vibrio anguillarum strains. Appl. Environ. Microbiol. 2015, 81, 4489–4497.
142. Abedon, S.T. Phage therapy best practices. In Bacteriophages in Health and Disease; Hyman, P., Abedon, S.T., Eds.; CABI Press: Wallingford, UK, 2012; pp. 256–272.
143. Abedon, S.T. Bacteriophages as drugs: The pharmacology of phage therapy. In Phage Therapy: Current Research and Applications; Borysowski, J., Miedzybrodzki, R.; Górski, A., Eds.; Caister Academic Press: Norfolk, UK, 2014; pp. 69–100.
144. Abedon, S.T. Phage therapy: Eco-physiological pharmacology. Scientifica 2014, 2014, 581639.
145. Wright, A.; Hawkins, C.H.; Änggård, E.E.; Harper, D.R. A controlled clinical trial of a therapeutic bacteriophage preparation in chronic otitis due to antibiotic-resistant Pseudomonas aeruginosa; a preliminary report of efficacy. Clin. Otolaryng. 2009, 34, 349–357.
146. Hawkins, C.; Harper, D.; Burch, D.; Anggard, E.; Soothill, J. Topical treatment of Pseudomonas aeruginosa otitis of dogs with a bacteriophage mixture: A before/after clinical trial. Vet. Microbiol. 2010, 145, 309–313.
147. Pirnay, J.P.; De, V.D.; Verbeken, G.; Merabishvili, M.; Chanishvili, N.; Vaneechoutte, M.; Zizi, M.; Laire, G.; Lavigne, R.; Huys, I. et al. The phage therapy paradigm: prêt-à-porter or sur-mesure? Pharm. Res. 2011, 28, 934–937.
148. Chan, B.K.; Abedon, S.T. Phage therapy pharmacology: Phage cocktails. Adv. Appl. Microbiol. 2012, 78, 1–23.
149. Chan, B.K.; Abedon, S.T.; Loc-Carrillo, C. Phage cocktails and the future of phage therapy. Future Microbiol. 2013, 8, 769–783.
150. Schmerer, M.; Molineux, I.J.; Bull, J.J. Synergy as a rationale for phage therapy using phage cocktails. PeerJ 2014, 2, e590.
151. Abedon, S.T. Lysis from without. Bacteriophage 2011, 1, 46–49.
152. Blackledge, M.S.; Worthington, R.J.; Melander, C. Biologically inspired strategies for combating bacterial biofilms. Curr. Opin. Pharmacol. 2013, 13, 699–706.
153. Thallinger, B.; Prasetyo, E.N.; Nyanhongo, G.S.; Guebitz, G.M. Antimicrobial enzymes: An emerging strategy to fight microbes and microbial biofilms. Biotechnol. J. 2013, 8, 97–109.
154. Shen, Y.; Mitchell, M.S.; Donovan, D.M.; Nelson, D.C. Phage-based enzybiotics. In Bacteriophages in Health and Disease; Hyman, P.; Abedon, S.T., Eds.; CABI Press: Wallingford, UK, 2012; pp. 217–239.
155. Yan, J.; Mao, J.; Xie, J. Bacteriophage polysaccharide depolymerases and biomedical applications. BioDrugs 2014, 28, 265–274.
156. Hwang, I.Y.; Tan, M.H.; Koh, E.; Ho, C.L.; Poh, C.L.; Chang, M.W. Reprogramming microbes to be pathogen-seeking killers. ACS Synth. Biol. 2014, 3, 228–237.
157. Curtright, A.J.; Abedon, S.T. Phage therapy: Emergent property pharmacology. J. Bioanal. Biomed. 2011, S6, doi:10.4172/1948-593X.S6-002.
158. Loc-Carrillo, C.; Abedon, S.T. Pros and cons of phage therapy. Bacteriophage 2011, 1, 111–114.
159. Viruses vs. Superbugs, Available online: http://www.bacteriophagetherapy.info/ECF40946- 8E2F-4890-9CA6-D390A26E39C1/Pros and cons of phage therapy.html (accessed on 6 September 2015).
160. Phage Therapy, Available online: phage-therapy.org (accessed on 6 September 2015).
161. Kutter, E.M.; Kuhl, S.J.; Abedon, S.T. Re-establishing a place for phage therapy in western medicine. Future Microbiol. 2015, 10, 685–688.
162. Hargreaves, K.R.; Clokie, M.R. Clostridium difficile phages: Still difficult? Front Microbiol. 2014, 5, 184, doi: 10.3389/fmicb.2014.00184.
163. Balogh, B.; Jones, J.B.; Iriarte, F.B.; Momol, M.T. Phage therapy for plant disease control. Curr. Pharm. Biotechnol. 2010, 11, 48–57.
164. Bull, J.J.; Otto, G.; Molineux, I.J. In vivo growth rates are poorly correlated with phage therapy success in a mouse infection model. Antimicrob. Agents Chemother. 2012, 56, 949–954.
165. Henry, M.; Lavigne, R.; Debarbieux, L. Predicting in vivo efficacy of therapeutic bacteriophages used to treat pulmonary infections. Antimicrob. Agents Chemother. 2013, 57, 5961–5968.
166. Bull, J.J.; Gill, J.J. The habits of highly effective phages: Population dynamics as a framework for identifying therapeutic phages. Front Microbiol. 2014, 5, 61, doi: 10.3389/fmicb.2014.00618.
167. Lindberg, H.M.; McKean, K.A.; Wang, I.-N. Phage fitness may help predict phage therapy efficacy. Bacteriophage 2014, 4, e964081, doi:10.4161/21597073.2014.964081.