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Chapter 11 : Practical and Theoretical Considerations for the Use of Bacteriophages in Food Systems

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Practical and Theoretical Considerations for the Use of Bacteriophages in Food Systems, Page 1 of 2

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Abstract:

Bacteriophages represent a promising antibacterial technology that may be useful in the control of a wide variety of nuisance and pathogenic bacteria. One area that is garnering increasing interest is the use of phages for the control of bacteria—particularly food-borne pathogens—in food systems. This chapter discusses factors such as the stability of the phages, the state of the bacteria, or the ability of phages to access their hosts, in the context of theory, as well as empirical data from model phage-host systems and from trials of phage biocontrol in foods. The phage adsorption rate constant plays a major role in the rate at which phage adsorb to susceptible bacteria. In the case of the control of food-borne pathogens, phages present a viable option, as the diversity of pathogens requiring control is limited to relatively few bacterial species. In contrast, the use of phages as a general antimicrobial strategy in foods is severely restricted simply by the diversity of potential target bacteria in a given open environment. Biofilms are a topic of perennial concern in the food industry, as they can cause problems in food production facilities ranging from equipment fouling to the shedding of pathogenic microbes into food products. Minimally processed foods which are considered to be at risk from contamination by a narrow spectrum of food-borne pathogens, and which are also intrinsically conducive to bacterial and phage survival, could be the most promising initial candidates for phage-based biocontrol.

Citation: Gill J. 2010. Practical and Theoretical Considerations for the Use of Bacteriophages in Food Systems, p 217-235. In Sabour P, Griffiths M (ed), Bacteriophages in the Control of Food-and Waterborne Pathogens. ASM Press, Washington, DC. doi: 10.1128/9781555816629.ch11

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FIGURE 1

Proportion of a hypothetical phage population adsorbed to various concentrations of host bacteria over time, given an adsorption constant of 1 × 10 ml/min.

Citation: Gill J. 2010. Practical and Theoretical Considerations for the Use of Bacteriophages in Food Systems, p 217-235. In Sabour P, Griffiths M (ed), Bacteriophages in the Control of Food-and Waterborne Pathogens. ASM Press, Washington, DC. doi: 10.1128/9781555816629.ch11
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References

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1. Abedon, S. T. 1990. The ecology of bacteriophage T4. Ph.D. dissertation. University of Arizona, Tucson, AZ.
2. Abedon, S. T. 2009a. Kinetics of phage-mediated biocontrol of bacteria. Foodborne Pathog. Dis. 6: 807815.
3. Abedon, S. T. 2009b. Disambiguating bacteriophage pseudolysogeny: an historical analysis of lysogeny, pseudolysogeny, and the phage carrier state, p. 285307. In H. T. Adams (ed.), Contemporary Trends in Bacteriophage Research. Nova Science Publishers, Hauppauge, NY.
4. Abedon, S. T., and, J. Yin. 2009. Bacteriophage plaques: theory and analysis. Methods Mol. Biol. 501:161174.
5. Abuladze, T.,, M. Li,, M. Y. Menetrez,, T. Dean,, A. Senecal, and, A. Sulakvelidze. 2008. Bacteriophages reduce experimental contamination of hard surfaces, tomato, spinach, broccoli, and ground beef by Escherichia coli O157:H7. Appl. Environ. Microbiol. 74:62306238.
6. Adams, M. H. 1949. The stability of bacterial viruses in solutions of salts. J. Gen. Physiol. 32:579594.
7. Adams, M. H. 1959. Bacteriophages. Interscience Publishers, New York, NY.
8. Atterbury, R. J.,, M. A. Van Bergen,, F. Ortiz,, M. A. Lovell,, J. A. Harris,, A. De Boer,, J. A. Wagenaar,, V. M. Allen, and, P. A. Barrow. 2007. Bacteriophage therapy to reduce Salmonella colonization of broiler chickens. Appl. Environ. Microbiol. 73:45434549.
9. Bayer, M. E.,, H. Thurow, and, M. H. Bayer. 1979. Penetration of the polysaccharide capsule of Escherichia coli (Bi161/42) by bacteriophage K29. Virology 94:95118.
10. Bremer, H., and, P. P. Dennis. 1996. Modulation of chemical composition and other parameters of the cell by growth rate, p. 15531569. In F. C. Neidhardt (ed.), Escherichia coli and Salmonella, 2nd ed., vol. 2. ASM Press, Washington, DC.
11. Briandet, R.,, P. Lacroix-Gueu,, M. Renault,, S. Lecart,, T. Meylheuc,, E. Bidnenko,, K. Steenkeste,, M. N. Bellon-Fontaine, and, M. P. Fontaine-Aupart. 2008. Fluorescence correlation spectroscopy to study diffusion and reaction of bacteriophages inside biofilms. Appl. Environ. Microbiol. 74:21352143.
12. Bruttin, A., and, H. Brüssow. 2005. Human volunteers receiving Escherichia coli phage T4 orally: a safety test of phage therapy. Antimicrob. Agents Chemother. 49:28742878.
13. Callaway, T. R.,, T. S. Edrington,, A. D. Brabban,, R. C. Anderson,, M. L. Rossman,, M. J. Engler,, M. A. Carr,, K. J. Genovese,, J. E. Keen,, M. L. Looper,, E. M. Kutter, and, D. J. Nisbet. 2008. Bacteriophage isolated from feedlot cattle can reduce Escherichia coli O157:H7 populations in ruminant gastrointestinal tracts. Foodborne Pathog. Dis. 5:183191.
14. Clark, W. A. 1962. Comparison of several methods for preserving bacteriophages. Appl. Microbiol. 10:466471.
15. Clark, W. A.,, W. Horneland, and, A. G. Klein. 1962. Attempts to freeze some bacteriophages to ultralow temperatures. Appl. Microbiol. 10:463465.
16. Corbin, B. D.,, R. J. McLean, and, G. M. Aron. 2001. Bacteriophage T4 multiplication in a glucose-limited Escherichia coli biofilm. Can. J. Microbiol. 47:680684.
17. Costerton, J. W.,, K. J. Cheng,, G. G. Geesey,, T. I. Ladd,, J. C. Nickel,, M. Dasgupta, and, T. J. Marrie. 1987. Bacterial biofilms in nature and disease. Annu. Rev. Microbiol. 41:435464.
18. Dassy, B., and, J. M. Fournier. 1996. Respiratory activity is essential for post-exponential-phase production of type 5 capsular polysaccharide by Staphylococcus aureus. Infect. Immun. 64:24082414.
19. Delbruck, M. 1940. Adsorption of bacteriophage under various physiological conditions of the host. J. Gen. Physiol. 23:631642.
20. De Paepe, M., and, F. Taddei. 2006. Viruses’ life history: towards a mechanistic basis of a trade-off between survival and reproduction among phages. PLoS Biol. 4:e193.
21. de Siqueira, R. S.,, C. E. Dodd, and, C. E. Rees. 2006. Evaluation of the natural virucidal activity of teas for use in the phage amplification assay. Int. J. Food Microbiol. 111:259262.
22. d’Herelle, F. 1926. The Bacteriophage and Its Behavior. Williams & Wilkins, Baltimore, MD.
23. Doolittle, M. M.,, J. J. Cooney, and, D. E. Caldwell. 1995. Lytic infection of Escherichia coli biofilms by bacteriophage T4. Can. J. Microbiol. 41:1218.
24. Doolittle, M. M.,, J. J. Cooney, and, D. E. Caldwell. 1996. Tracing the interaction of bacteriophage with bacterial biofilms using fluorescent and chromogenic probes. J. Ind. Microbiol. 16:331341.
25. Dykes, G. A., and, S. M. Moorhead. 2002. Combined antimicrobial effect of nisin and a listeriophage against Listeria monocytogenes in broth but not in buffer or on raw beef. Int. J. Food Microbiol. 73:7181.
26. Federal Register. 2006. Food additives permitted for direct addition to food for human consumption; bacteriophage preparation. Fed. Regist. 71:4772947732.
27. Fortier, L. C., and, S. Moineau. 2009. Phage production and maintenance of stocks, including expected stock lifetimes. Methods Mol. Biol. 501:203219.
28. Garcia, P.,, C. Madera,, B. Martinez,, A. Rodriguez, and, J. Evaristo Suarez. 2009. Prevalence of bacteriophages infecting Staphylococcus aureus in dairy samples and their potential as biocontrol agents. J. Dairy Sci. 92:30193026.
29. Gerba, C. P. 1984. Applied and theoretical aspects of virus adsorption to surfaces. Adv. Appl. Microbiol. 30:133168.
30. Gill, J. J. 2008. Modeling of bacteriophage therapy, p. 439464. In S. T. Abedon (ed.), Bacteriophage Ecology: Population Growth, Evolution, and Impact of Bacterial Viruses. Cambridge University Press, Cambridge, United Kingdom.
31. Gill, J. J.,, P. M. Sabour,, K. E. Leslie, and, M. W. Griffiths. 2006. Bovine whey proteins inhibit the interaction of Staphylococcus aureus and bacteriophage K. J. Appl. Microbiol. 101:377386.
32. Greer, G. G. 1982. Psychrotrophic bacteriophages for beef spoilage pseudomonads. J. Food Prot. 45:13181325.
33. Greer, G. G. 1983. Psychrotrophic Brocothrix thermosphacta bacteriophages isolated from beef. Appl. Environ. Microbiol. 46:245251.
34. Greer, G. G., and, B. D. Dilts. 1990. Inability of a bacteriophage pool to control beef spoilage. Int. J. Food Microbiol. 10:331342.
35. Greer, G. G., and, B. D. Dilts. 2002. Control of Brochothrix thermosphacta spoilage of pork adipose tissue using bacteriophages. J. Food Prot. 65:861863.
36. Groman, N. B., and, G. Suzuki. 1962. Temperature and lambda phage reproduction. J. Bacteriol. 84:431437.
37. Guenther, S.,, D. Huwyler,, S. Richard, and, M. J. Loessner. 2009. Virulent bacteriophage for efficient biocontrol of Listeria monocytogenes in ready-to-eat foods. Appl. Environ. Microbiol. 75:93100.
38. Hadas, H.,, M. Einav,, I. Fishov, and, A. Zaritsky. 1997. Bacteriophage T4 development depends on the physiology of its host Escherichia coli. Microbiology 143:179185.
39. Hanlon, G. W.,, S. P. Denyer,, C. J. Olliff, and, L. J. Ibrahim. 2001. Reduction in exopolysaccharide viscosity as an aid to bacteriophage penetration through Pseudomonas aeruginosa biofilms. Appl. Environ. Microbiol. 67:27462753.
40. Hantke, K., and, V. Braun. 1978. Functional interaction of the tonA/tonB receptor system in Escherichia coli. J. Bacteriol. 135:190197.
41. Herbert, S.,, S. W. Newell,, C. Lee,, K. P. Wieland,, B. Dassy,, J. M. Fournier,, C. Wolz, and, G. Doring. 2001. Regulation of Staphylococcus aureus type 5 and type 8 capsular polysaccharides by CO2. J. Bacteriol. 183:46094613.
42. Hershey, A. D. 1957. Bacteriophages as genetic and biochemical systems. Adv. Virus Res. 4:2561.
43. Hughes, K. A.,, I. W. Sutherland, and, M. V. Jones. 1998. Biofilm susceptibility to bacteriophage attack: the role of phage-borne polysaccharide depolymerase. Microbiology 144:30393047.
44. Huisman, G. W.,, D. A. Siegele,, M. M. Zambrano, and, R. M. Kolter. 1996. Morphological and physiological changes during stationary phase, p. 16721682. In F. C. Neidhardt (ed.), Escherichia coli and Salmonella, 2nd ed., vol. 2. ASM Press, Washington, DC.
45. Hurley, A.,, J. J. Maurer, and, M. D. Lee. 2008. Using bacteriophages to modulate Salmonella colonization of the chicken’s gastrointestinal tract: lessons learned from in silico and in vivo modeling. Avian Dis. 52:599607.
46. Jepson, C. D., and, J. B. March. 2004. Bacteriophage lambda is a highly stable DNA vaccine delivery vehicle. Vaccine 22:24132419.
47. Joh, D.,, E. R. Wann,, B. Kreikemeyer,, P. Speziale, and, M. Hook. 1999. Role of fibronectin-binding MSCRAMMs in bacterial adherence and entry into mammalian cells. Matrix Biol. 18:211223.
48. Kasman, L. M.,, A. Kasman,, C. Westwater,, J. Dolan,, M. G. Schmidt, and, J. S. Norris. 2002. Overcoming the phage replication threshold: a mathematical model with implications for phage therapy. J. Virol. 76:55575564.
49. Klein, W., and, W. Boos. 1993. Induction of the λ receptor is essential for effective uptake of trehalose in Escherichia coli. J. Bacteriol. 175:16821686.
50. Koch, A. L. 1960. Encounter efficiency of coliphage-bacterial interaction. Biochim. Biophys. Acta 39:311318.
51. Kolter, R.,, D. A. Siegele, and, A. Tormo. 1993. The stationary phase of the bacterial life cycle. Annu. Rev. Microbiol. 47:855874.
52. Krueger, D. H.,, W. Presber,, S. Hansen, and, H. A. Rosenthal. 1975. Biological functions of the bacteriophage T3 SAMase gene. J. Virol. 16:453455.
53. Kumar, C. G., and, S. K. Anand. 1998. Significance of microbial biofilms in food industry: a review. Int. J. Food Microbiol. 42:927.
54. Kutter, E.,, E. Kellenberger,, K. Carlson,, S. Eddy,, J. Neitzel,, L. Messinger,, J. North, and, B. Guttman. 1994. Effects of bacterial growth conditions and physiology on T4 infection, p. 406418. In J. D. Karam (ed.), Molecular Biology of Bacteriophage T4. ASM Press, Washington, DC.
55. Lavigne, R.,, P.J. Ceyssens, and, J. Robben. 2009. Phage proteomics: applications of mass spectrometry. Methods Mol. Biol. 502:239251.
56. Leiman, P. G.,, A. J. Battisti,, V. D. Bowman,, K. Stummeyer,, M. Muhlenhoff,, R. Gerardy-Schahn,, D. Scholl, and, I. J. Molineux. 2007. The structures of bacteriophages K1E and K1-5 explain processive degradation of polysaccharide capsules and evolution of new host specificities. J. Mol. Biol. 371:836849.
57. Leverentz, B.,, W. S. Conway,, M. J. Camp,, W. J. Janisiewicz,, T. Abuladze,, M. Yang,, R. Saftner, and, A. Sulakvelidze. 2003. Biocontrol of Listeria monocytogenes on fresh-cut produce by treatment with lytic bacteriophages and a bacteriocin. Appl. Environ. Microbiol. 69:45194526.
58. Leverentz, B.,, W. S. Conway,, W. Janisiewicz, and, M. J. Camp. 2004. Optimizing concentration and timing of a phage spray application to reduce Listeria monocytogenes on honeydew melon tissue. J. Food Prot. 67:16821686.
59. Lillford, P. J., and, C. B. Holt. 2002. In vitro uses of biological cryoprotectants. Philos. Trans. R. Soc. Lond. B Biol. Sci. 357:945951.
60. Lindberg, A. A. 1973. Bacteriophage receptors. Annu. Rev. Microbiol. 27:205241.
61. Lindberg, A. A., and, T. Holme. 1969. Influence of O side chains on the attachment of the Felix O-1 bacteriophage to Salmonella bacteria. J. Bacteriol. 99:513519.
62. Loc Carrillo, C.,, R. J. Atterbury,, A. El-Shibiny,, P. L. Connerton,, E. Dillon,, A. Scott, and, I. F. Connerton. 2005. Bacteriophage therapy to reduce Campylobacter jejuni colonization of broiler chickens. Appl. Environ. Microbiol. 71:65546563.
63. Łoś, M.,, P. Golec,, J. M. Łoś,, A. Weglewska-Jurkiewicz,, A. Czyz,, A. Węgrzyn,, G. Węgrzyn, and, P. Neubauer. 2007. Effective inhibition of lytic development of bacteriophages X, P1 and T4 by starvation of their host, Escherichia coli. BMC Biotechnol. 7:13.
64. Lu, T. K., and, J. J. Collins. 2007. Dispersing biofilms with engineered enzymatic bacteriophage. Proc. Natl. Acad. Sci. USA 104:1119711202.
65. Maaloe, O. 1950. Some effects of changes of temperature on intracellular growth of the bacterial virus T4r. Acta Pathol. Microbiol. Scand. 27:680694.
66. Markoishvili, K.,, G. Tsitlanadze,, R. Katsarava,, J. G. Morris, Jr., and, A. Sulakvelidze. 2002. 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. 41:453458.
67. McConnell, M., and, A. Wright. 1979. Variation in the structure and bacteriophage-inactivating capacity of Salmonella anatum lipopolysaccharide as a function of growth temperature. J. Bacteriol. 137:746751.
68. McGrath, S.,, G. F. Fitzgerald, and, D. van Sinderen. 2007. Bacteriophages in dairy products: pros and cons. Biotechnol. J. 2:450455.
69. Modi, R.,, Y. Hirvi,, A. Hill, and, M. W. Griffiths. 2001. Effect of phage on survival of Salmonella enteritidis during manufacture and storage of cheddar cheese made from raw and pasteurized milk. J. Food Prot. 64:927933.
70. O’Flaherty, S.,, A. Coffey,, W. J. Meaney,, G. F. Fitzgerald, and, R. P. Ross. 2005. Inhibition of bacteriophage K proliferation on Staphylococcus aureus in raw bovine milk. Lett. Appl. Microbiol. 41:274279.
71. O’Flynn, G.,, R. P. Ross,, G. F. Fitzgerald, and, A. Coffey. 2004. Evaluation of a cocktail of three bacteriophages for biocontrol of Escherichia coli O157:H7. Appl. Environ. Microbiol. 70:34173424.
72. Olsen, R. H. 1967. Isolation and growth of psychrophilic bacteriophage. Appl. Microbiol. 15:198.
73. Olsen, R. H.,, E. S. Metcalf, and, J. K. Todd. 1968. Characteristics of bacteriophages attacking psychrophilic and mesophilic pseudomonads. J. Virol. 2:357364.
74. Payne, R. J., and, V. A. Jansen. 2001. Understanding bacteriophage therapy as a density-dependent kinetic process. J. Theor. Biol. 208:3748.
75. Payne, R. J., and, V. A. Jansen. 2003. Pharmacokinetic principles of bacteriophage therapy. Clin. Pharmacokinet. 42:315325.
76. Poutrel, B.,, P. Rainard, and, P. Sarradin. 1997. Heterogeneity of cell-associated CP5 expression on Staphylococcus aureus strains demonstrated by flow cytometry. Clin. Diagn. Lab. Immunol. 4:275278.
77. Randall-Hazelbauer, L., and, M. Schwartz. 1973. Isolation of the bacteriophage lambda receptor from Escherichia coli. J. Bacteriol. 116:14361446.
78. Ripp, S., and, R. V. Miller. 1997. The role of pseudolysogeny in bacteriophage-host interactions in a natural freshwater environment. Microbiology 143:20652070.
79. Ripp, S., and, R. V. Miller. 1998. Dynamics of the pseudolysogenic response in slowly growing cells of Pseudomonas aeruginosa. Microbiology 144:22252232.
80. Ryter, A.,, H. Shuman, and, M. Schwartz. 1975. Integration of the receptor for bacteriophage lambda in the outer membrane of Escherichia coli: coupling with cell division. J. Bacteriol. 122:295301.
81. Schaechter, M.,, O. Maaloe, and, N. O. Kjeldgaard. 1958. Dependency on medium and temperature of cell size and chemical composition during balanced growth of Salmonella typhimurium. J. Gen. Microbiol. 19:592606.
82. Scholl, D.,, S. Adhya, and, C. Merril. 2005. Escherichia coli K1’s capsule is a barrier to bacteriophage T7. Appl. Environ. Microbiol. 71:48724874.
83. Schrader, H. S.,, J. O. Schrader,, J. J. Walker,, T. A. Wolf,, K. W. Nickerson, and, T. A. Kokjohn. 1997. Bacteriophage infection and multiplication occur in Pseudomonas aeruginosa starved for 5 years. Can. J. Microbiol. 43:11571163.
84. Schwartz, M. 1976. The adsorption of coliphage lambda to its host: effect of variations in the surface density of receptor and in phage-receptor affinity. J. Mol. Biol. 103:521536.
85. Smith, H. W.,, M. B. Huggins, and, K. M. Shaw. 1987. Factors influencing the survival and multiplication of bacteriophages in calves and in their environment. J. Gen. Microbiol. 133:11271135.
86. Stent, G. S. 1963. Molecular Biology of Bacterial Viruses. W. H. Freeman & Co., San Francisco, CA.
87. Sternberg, C.,, B. B. Christensen,, T. Johansen,, A. Toftgaard Nielsen,, J. B. Andersen,, M. Givskov, and, S. Molin. 1999. Distribution of bacterial growth activity in flow-chamber biofilms. Appl. Environ. Microbiol. 65:41084117.
88. Stopar, D., and, S. T. Abedon. 2008. Modeling bacteriophage population growth, p. 389414. In S. T. Abedon (ed.), Bacteriophage Ecology: Population Growth, Evolution, and Impact of Bacterial Viruses. Cambridge University Press, Cambridge, United Kingdom.
89. Sutra, L.,, P. Rainard, and, B. Poutrel. 1990. Phagocytosis of mastitis isolates of Staphylococcus aureus and expression of type 5 capsular polysaccharide are influenced by growth in the presence of milk. J. Clin. Microbiol. 28:22532258.
90. Tolmach, L. J. 1957. Attachment and penetration of cells by viruses. Adv. Virus Res. 4:63110.
91. Wann, E. R.,, S. Gurusiddappa, and, M. Hook. 2000. The fibronectin-binding MSCRAMM FnbpA of Staphylococcus aureus is a bifunctional protein that also binds to fibrinogen. J. Biol. Chem. 275:1386313871.
92. Wesche, A. M.,, J. B. Gurtler,, B. P. Marks, and, E. T. Ryser. 2009. Stress, sublethal injury, resuscitation, and virulence of bacterial foodborne pathogens. J. Food Prot. 72:11211138.
93. Whitman, P. A., and, R. T. Marshall. 1971. Characterization of two psychrophilic Pseudomonas bacteriophages isolated from ground beef. Appl. Microbiol. 22:463468.
94. Wilkinson, B. J., and, K. M. Holmes. 1979. Staphylococcus aureus cell surface: capsule as a barrier to bacteriophage adsorption. Infect. Immun. 23:549552.
95. Wilkinson, M. H. 2001. Predation in the presence of decoys: an inhibitory factor on pathogen control by bacteriophages or bdellovibrios in dense and diverse ecosystems. J. Theor. Biol. 208:2736.
96. Wong, A. C. 1998. Biofilms in food processing environments. J. Dairy Sci. 81:27652770.
97. Yanagida, M.,, Y. Suzuki, and, T. Toda. 1984. Molecular organization of the head of bacteriophage Teven: underlying design principles. Adv. Biophys. 17:97146.
98. Yin, J. 1991. A quantifiable phenotype of viral propagation. Biochem. Biophys. Res. Commun. 174:10091014.

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