Combined treatment of Pseudomonas aeruginosa biofilms with bacteriophages and chlorine

Biotechnology and Bioengineering

Volumn 110, Issue 1, 2013, Pages 286-295

  Zhang, Yanyan ^a   Hu, Zhiqiang ^a  

^a University of Missouri   (United States)

Author keywords

Biofilm control and removal; Chlorination; Combined treatment; Phage; Pseudomonas aeruginosa

Indexed keywords

BACTERIA; BACTERIOPHAGES; CHLORINATION; CHLORINE; CONFOCAL MICROSCOPY; ELECTRON MICROSCOPY; RNA;

BACTERIAL BIOFILM; BIOFILM CONTROL; BIOFILM FORMATION; BIOFILM GROWTH; CELL DENSITY; COMBINATION TREATMENTS; COMBINED TREATMENT; CONTINUOUS-FLOW SYSTEM; LASER SCANNING CONFOCAL MICROSCOPY; MUNICIPAL WASTEWATERS; P.AERUGINOSA; PSEUDOMONAS AERUGINOSA; TIME DURATION; WATER-FLUSHING;

BIOFILMS;

CHLORINE;

ARTICLE; BACTERIOPHAGE; BIOFILM; CELL DENSITY; CELL VIABILITY; CHLORINATION; CONFOCAL MICROSCOPY; ELECTRON MICROSCOPY; LASER MICROSCOPY; NONHUMAN; PSEUDOMONAS AERUGINOSA; RNA PHAGE; WASTE WATER;

BACTERIA (MICROORGANISMS); PSEUDOMONAS AERUGINOSA;

EID: 84869872766     PISSN: 00063592     EISSN: 10970290     Source Type: Journal    
DOI: 10.1002/bit.24630     Document Type: Article

References (67)

1. Abbaszadegan M, Mayer BK, Ryu H, Nwachuku N. 2007. Efficacy of removal of CCL viruses under enhanced coagulation conditions. Environ Sci Technol 41(3): 971-977.
2. Ackermann H, DuBow MS. 1987. Viruses of prokaryotes. Vol. 1. Boca Raton: CRC Press.
3. Adam MH. 1959. Bacteriophages. New York: Interscience Publishers.
4. Ahiwale S, Tamboli N, Thorat K, Kulkarni R, Ackermann H, Kapadnis B. 2011. In vitro management of hospital Pseudomonas aeruginosa biofilm using indigenous T7-like lytic phage. Curr Microbiol 62(2): 335-340.
5. Ammons MCB, Ward LS, Dowd S, James GA. 2011. Combined treatment of Pseudomonas aeruginosa biofilm with lactoferrin and xylitol inhibits the ability of bacteria to respond to damage resulting from lactoferrin iron chelation. Int J Antimicrob Agents 37(4): 316-323.
6. Anaissie EJ, Penzak SR, Dignani MC. 2002. The hospital water supply as a source of nosocomial infections: A plea for action. Arch Intern Med 162(13): 1483-1492.
7. Azeredo J, Sutherland IW. 2008. The use of phages for the removal of infectious biofilms. Curr Pharm Biotechnol 9(4): 261-266.
8. Barraud N, Storey MV, Moore ZP, Webb JS, Rice SA, Kjelleberg S. 2009. Nitric oxide-mediated dispersal in single- and multi-species biofilms of clinically and industrially relevant microorganisms. Microb Biotechnol 2(3): 370-378.
9. Brindle ER, Miller DA, Stewart PS. 2011. Hydrodynamic deformation and removal of Staphylococcus epidermidis biofilms treated with urea, chlorhexidine, iron chloride, or DispersinB. Biotechnol Bioeng 108(12): 2968-2977.
10. Caro A, Humblot V, Méthivier C, Minier M, Salmain M, Pradier CM. 2009. Grafting of lysozyme and/or poly(ethylene glycol) to prevent biofilm growth on stainless steel surfaces. J Phys Chem B 113(7): 2101-2109.
11. Carson L, Gorman SP, Gilmore BF. 2010. The use of lytic bacteriophages in the prevention and eradication of biofilms of Proteus mirabilis and Escherichia coli FEMS Immunol Med Microbiol 59(3): 447-455.
12. Ceyssens PJ, Lavigne R, Mattheus W, Chibeu A, Hertveldt K, Mast J, Robben J, Volckaert G. 2006. Genomic analysis of Pseudomonas aeruginosa phages LKD16 and LKA1: Establishment of the φKMV subgroup within the T7 supergroup. J Bacteriol 188(19): 6924-6931.
13. Chen X, Stewart PS. 1996. Chlorine penetration into artificial biofilm is limited by a reaction-diffusion interaction. Environ Sci Technol 30(6): 2078-2083.
14. Donlan RM. 2009. Preventing biofilms of clinically relevant organisms using bacteriophage. Trends Microbiol 17(2): 66-72.
15. Drenkard E, Ausubel FM. 2002. Pseudomonas biofilm formation and antibiotic resistance are linked to phenotypic variation. Nature 416(6882): 740-743.
16. Dunne WM, Jr. 2002. Bacterial adhesion: Seen any good biofilms lately? Clin Microbiol Rev 15(2): 155-166.
17. Fauquet CM, Mayo MA, Maniloff J, Desselberger U, Ball LA. 2005. Virus taxonomy: Classification and nomenclature of viruses: Eighth report of the International Committee on the Taxonomy of Viruses. San Diego: Elsevier Academic Press.
18. Flemming HC, Wingender J. 2001. Relevance of microbial extracellular polymeric substances (EPSs)-Part I: Structural and ecological aspects. Water Sci Technol 43(6): 1-8.
19. Flemming K, Klingenberg C, Cavanagh JP, Sletteng M, Stensen W, Svendsen JS, Flaegstad T. 2009. High in vitro antimicrobial activity of synthetic antimicrobial peptidomimetics against staphylococcal biofilms. J Antimicrob Chemother 63(1): 136-145.
20. Fu S, Fan H, Liu S, Liu Y, Liu Z. 2009. A bioaugmentation failure caused by phage infection and weak biofilm formation ability. J Environ Sci 21(8): 1153-1161.
21. Fu W, Forster T, Mayer O, Curtin JJ, Lehman SM, Donlan RM. 2010. Bacteriophage cocktail for the prevention of biofilm formation by Pseudomonas aeruginosa on catheters in an in vitro model system. Antimicrob Agents Chemother 54(1): 397-404.
22. Goldman G, Starosvetsky J, Armon R. 2009. Inhibition of biofilm formation on UF membrane by use of specific bacteriophages. J Membr Sci 342(1-2): 145-152.
23. Gu J, Liu X, Li Y, Han W, Lei L, Yang Y, Zhao H, Gao Y, Song J, Lu R, Sun C, Feng X. 2012. A method for generation phage cocktail with great therapeutic potential. PLoS ONE 7(3): 1-8.
24. Hanlon GW, Denyer SP, Olliff CJ, Ibrahim LJ. 2001. Reduction in exopolysaccharide viscosity as an aid to bacteriophage penetration through Pseudomonas aeruginosa biofilms. Appl Environ Microbiol 67(6): 2746-2753.
25. Hantula J, Kurki A, Vuoriranta P, Bamford DH. 1991. Ecology of bacteriophages infecting activated sludge bacteria. Appl Environ Microbiol 57(8): 2147-2151.
26. Harper DR, Enright MC. 2011. Bacteriophages for the treatment of Pseudomonas aeruginosa infections. J Appl Microbiol 111(1): 1-7.
27. Harrison JJ, Turner RJ, Joo DA, Stan MA, Chan CS, Allan ND, Vrionis HA, Olson ME, Ceri H. 2008. Copper and quaternary ammonium cations exert synergistic bactericidal and antibiofilm activity against Pseudomonas aeruginosa Antimicrob Agents Chemother 52(8): 2870-2881.
28. Heringa SD, Kim J, Jiang X, Doyle MP, Erickson MC. 2010. Use of a mixture of bacteriophages for biological control of Salmonella enterica strains in compose. Appl Environ Microbiol 76(15): 5327-5332.
29. Hornstra LM, Smeets PWMH, Medema GJ. 2011. Inactivation of bacteriophage MS2 upon exposure to very low concentrations of chlorine dioxide. Water Res 45(4): 1847-1855.
30. Hyman P, Abedon ST. 2010. Bacteriophage host range and bacterial resistance. Adv Appl Microbiol 70: 217-248.
31. Ito A, Taniuchi A, May T, Kawata K, Okabe S. 2009. Increased antibiotic resistance of Escherichia coli in mature biofilms. Appl Environ Microbiol 75(12): 4093-4100.
32. Jensen EC, Schrader HS, Rieland B, Thompson TL, Lee KW, Nickerson KW, Kokjohn TA. 1998. Prevalence of broad-host-range lytic bacteriophages of Sphaerotilus natans, Escherichia coli, and Pseudomonas aeruginosa Appl Environ Microbiol 64(2): 575-580.
33. Khan MA, Satoh H, Katayama H, Kurisu F, Mino T. 2002. Bacteriophages isolated from activated sludge processes and their polyvalency. Water Res 36(13): 3364-3370.
34. Kim J, Pitts B, Stewart PS, Camper A, Yoon J. 2008. Comparison of the antimicrobial effects of chlorine, silver ion, and tobramycin on biofilm. Antimicrob Agents Chemother 52(4): 1446-1453.
35. Kim Y, Wang X, Ma Q, Zhang X-S, Wood TK. 2009. Toxin-antitoxin systems in Escherichia coli influence biofilm formation through YjgK (TabA) and fimbriae. J Bacteriol 191(4): 1258-1267.
36. Knezevic P, Petrovic O. 2008. A colorimetric microtiter plate method for assessment of phage effect on Pseudomonas aeruginosa biofilm. J Microbiol Methods 74(2-3): 114-118.
37. Kolter R, Greenberg EP. 2006. Microbial sciences: The superficial life of microbes. Nature 441(7091): 300-302.
38. Krylov VN. 2001. Phage therapy in terms of bacteriophage genetics: Hopes, prospects, safety, limitations. Russian J Genet 37(7): 715-730.
39. Kunisaki H, Tanji Y. 2010. Intercrossing of phage genomes in a phage cocktail and stable coexistence with Escherichia coli O157: H7 in anaerobic continuous culture. Appl Microbiol Biotechnol 85(5): 1533-1540.
40. Lacqua A, Wanner O, Colangelo T, Martinotti MG, Landini P. 2006. Emergence of biofilm-forming subpopulations upon exposure of Escherichia coli to environmental bacteriophages. Appl Environ Microbiol 72(1): 956-959.
41. LeChevallier MW, Cawthon CD, Lee RG. 1988. Inactivation of biofilm bacteria. Appl Environ Microbiol 54(10): 2492-2499.
42. Lenski RE. 1988. Dynamics of interactions between bacteria and virulent phage. Adv Microb Ecol 10: 1-44.
43. Leroy C, Delbarre C, Ghillebaert F, Compere C, Combes D. 2008. Effects of commercial enzymes on the adhesion of a marine biofilm-forming bacterium. Biofouling 24(1): 11-22.
44. Madigan MT, Martinko JM, Dunlap PV, Clark DP. 2009. Brock biology of microorganisms. San Francisco: Pearson Education, Inc.
45. Mah TF, Pitts B, Pellock B, Walker GC, Stewart PS, O'Toole GA. 2003. A genetic basis for Pseudomonas aeruginosa biofilm antibiotic resistance. Nature 426(6964): 306-310.
46. McLennan SD, Peterson LA, Rose JB. 2009. Comparison of point-of-use technologies for emergency disinfection of sewage-contaminated drinking water. Appl Environ Microbiol 75(22): 7283-7286.
47. Mikuniya T, Kato Y, Ida T, Maebashi K, Monden K, Kariyama R, Kumon H. 2007. Treatment of Pseudomonas aeruginosa biofilms with a combination of fluoroquinolones and fosfomycin in a rat urinary tract infection model. J Infect Chemother 13(5): 285-290.
48. Niu YD, Johnson RP, Xu Y, McAllister TA, Sharma R, Louie M, Stanford K. 2009. Host range and lytic capability of four bacteriophages against bovine and clinical human isolates of Shiga toxin-producing Escherichia coli O157: H7. J Appl Microbiol 107(2): 646-656.
49. Otawa K, Lee SH, Yamazoe A, Onuki M, Satoh H, Mino T. 2007. Abundance, diversity, and dynamics of viruses on microorganisms in activated sludge processes. Microb Ecol 53(1): 143-152.
50. Patil JS, Jagadeesan V. 2011. Effect of chlorination on the development of marine biofilms dominated by diatoms. Biofouling 27(3): 241-254.
51. Payne RJH, Jansen VAA. 2001. Understanding bacteriophage therapy as a density-dependent kinetic process. J Theor Biol 208(1): 37-48.
52. Pires D, Sillankorva S, Faustino A, Azeredo J. 2011. Use of newly isolated phages for control of Pseudomonas aeruginosa PAO1 and ATCC 10145 biofilms. Res Microbiol 162(8): 798-806.
53. Richards JJ, Melander C. 2009. Controlling bacterial biofilms. Chem Bio Chem 10(14): 2287-2294.
54. Rutala WA, Weber DJ. 1997. Uses of inorganic hypochlorite (bleach) in health-care facilities. Clin Microbiol Rev 10(4): 597-610.
55. Sabbah S, Springthorpe S, Sattar SA. 2010. Use of a mixture of surrogates for infectious bioagents in a standard approach to assessing disinfection of environmental surfaces. Appl Environ Microbiol 76(17): 6020-6022.
56. Snead MC, Olivieri VP, Kawata K, Kruse CW. 1980. The effectiveness of chlorine residuals in inactivation of bacteria and viruses introduced by post-treatment contamination. Water Res 14(5): 403-408.
57. Srinivasan S, Harrington GW, Xagoraraki I, Goel R. 2008. Factors affecting bulk to total bacteria ratio in drinking water distribution systems. Water Res 42(13): 3393-3404.
58. Sulakvelidze A, Pasternack GR. Intralytix, Inc., assignee. 2007 Jun 18. Pseudomonas aeruginosa: Bacteriophage and uses thereof. US patent 7622293.
59. Tré-Hardy M, Nagant C, El Manssouri N, Vanderbist F, Traore H, Vaneechoutte M, Dehaye JP. 2010. Efficacy of the combination of tobramycin and a macrolide in an in vitro Pseudomonas aeruginosa mature biofilm model. Antimicrob Agents Chemother 54(10): 4409-4415.
60. Ueda T, Horan NJ. 2000. Fate of indigenous bacteriophage in a membrane bioreactor. Water Res 34(7): 2151-2159.
61. USEPA. 1992. Control of biofilm growth in drinking water distribution systems, EPA/625/R-92/01. Washington, DC: Office of Research and Development.
62. Weld RJ, Butts C, Heinemann JA. 2004. Models of phage growth and their applicability to phage therapy. J Theor Biol 227(1): 1-11.
63. Whiteley M, Bangera MG, Bumgarner RE, Parsek MR, Teitzel GM, Lory S, Greenberg EP. 2001. Gene expression in Pseudomonas aeruginosa biofilms. Nature 413(6858): 860-864.
64. Withey S, Cartmell E, Avery LM, Stephenson T. 2005. Bacteriophages-Potential for application in wastewater treatment processes. Sci Total Environ 339(1-3): 1-18.
65. Yasunori T, Katsunori M, Masatoshi Y, Masatomo M, Katsutoshi H, Hajime U. 2002. Fate of coliphage in a wastewater treatment process. J Biosci Bioeng 94(2): 172-174.
66. Yeon KM, Cheong WS, Oh HS, Lee WN, Hwang BK, Lee CH, Beyenal H, Lewandowski Z. 2009. Quorum sensing: A new biofouling control paradigm in a membrane bioreactor for advanced wastewater treatment. Environ Sci Technol 43(2): 380-385.
67. Yoichi M, Morita M, Mizoguchi K, Fischer CR, Unno H, Tanji Y. 2004. The criterion for selecting effective phage for Escherichia coli O157: H7 control. Biochem Eng J 19(3): 221-227.