Bacteriophages for Potential Food Safety Applications in Organic Meat Production

Organic Meat Production and Processing

Volumn , Issue , 2012, Pages 407-424

  Ricke, Steven C ^a   Hererra, Paul ^b   Biswas, Debabrata ^c  

^a UNIVERSITY OF ARKANSAS   (United States)

^b U S DEPARTMENT OF AGRICULTURE   (United States)

^c UNIVERSITY OF MARYLAND   (United States)

Author keywords

Bacteriophage; Escherichia coli; Food borne pathogens; Gastric compartment; Lysogenic; Lytic; Postharvest food safety; Preharvest food safety; Rumen; Salmonella; Temperate; Therapeutic; Virulent

Indexed keywords

EID: 84886496928     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1002/9781118229088.ch23     Document Type: Chapter

References (113)

1. 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. 74:6230-6238.
2. Ackerman, H. W. and M. S. Dubow. 1987. Viruses of Prokaryotes, vol. 1. CRC Press, Inc., Boca Raton, FL.
3. Alam, K. Y. and D. P. Clark. 1989. Anaerobic fermentation balance of Escherichia coli as observed by in vivo nuclear magnetic resonance spectroscopy. J. Bacteriol. 171:6213-6217.
4. Anany, H., W. Chen, R. Pelton, and M. W. Griffiths. 2011. Biocontrol of Listeria monocytogenes and E. coli O157:H7 in meat using phage immobilized on modified cellulose membranes. Appl. Environ. Microbiol. 77:6379-6387.
5. Atterbury, R. J., P. L. Connerton, C. E. R. Dodd, C. E .D. Rees, and I. F. Connerton. 2003a. Isolation and characterization of Campylobacter bacteriophages from retail poultry. Appl. Environ. Microbiol. 69:4511-4518.
6. Atterbury, R. J., P. L. Connerton, C. E. R. Dodd, C. E. D. Rees, and I. F. Connerton. 2003b. Application of hostspecific bacteriophages to the surface of chicken skin leads to a reduction in recovery of Campylobacter jejuni. Appl. Environ. Microbiol. 69: 6302-6306.
7. Bach, R. P. S. J., Johnson, K. Stanford, and T. A. McAllister. 2009. Bacteriophages reduce Escherichia coli O157:H7 levels in experimentally inoculated sheep. Can. J. Anim. Sci. 89:285-293.
8. Barrow, P., M. Lovell, and A. Berchjeri. 1998. Use of lytic bacteriophage for control of experimental Escherichia coli septicemia and meningitis in chickens and calves. Clin. Diagnost Lab. Immunol. 5:294-298.
9. Baucheron, S., C. Mouline, K. Praud, E. Chaslus-Dancla, and A. Cloeckaert. 2005. TolC but not AcrB is essential for multidrug-resistant Salmonella enterica serotype Typhimurium colonization of chicks. J. Antimicrob. Chemother. 55:707-712.
10. Berchieri, A., M. A. Lovell, and P. A. Barrow. 1991. The activity in the chicken alimentary tract of bacteriophage lytic for Salmonella typhimurium. Res. Microbiol. 142:541-549.
11. Bielke, L. R., S. E. Higgins, A. M. Donoghue, D. J. Donohue, B. M. Hargis, and G. Tellez. 2007a. Use of wide-host-range bacteriophages to reduce Salmonella on poultry products. Int. J. Poult. Sci. 6:754-757.
12. Bielke, L., S. Higgins, A. Donoghue, D. Donohue, and B. Hargis. 2007b. Salmonella host range of bacteriophages that infect multiple genera. Poult. Sci. 86:2536-7540.
13. Biswas, B., S. Adhya, P.Washart, B. Paul, A. N. Trostel, B. Powell, R. Carlton, and C. R. Merril. 2002. Bacteriophage therapy rescues mice bacteremic from a clinical isolate of vancomycin-resistant Enterococcus faecium. Infect. Immun. 70:204-210.
14. Borie, C., I. Albala, P. Sànchez, M. L. Sánchez, S. Ramírez, C. Navarro, M. A. Morales, J. Retamales, and J. Robeson. 2008. Bacteriophage treatment reduces Salmonella colonization of infected chickens. Avian Dis. 52:64-67.
15. Borysowski, J. and A. Górski. 2008. Is phage therapy acceptable in immunocompromised host?. Int. J. Infect. Dis. 12:466-471.
16. Brüssow, H. 2005. Phage therapy: the Escherichia coli experience. Microbiol. 151:2133-2140.
17. Brüssow, H. and R. W. Hendrix. 2002. Phage genomics: small is beautiful. Cell 108:13-16.
18. Buckley, A. M., M. A. Webber, S. Cooles, L. P. Randall, R. M. La Ragione, M. J. Woodward, and L. J. V. Piddock. 2006. The AcrAB-TolC efflux system of Salmonella enterica serovar Typhimurium plays a role in pathogenesis. Cell. Microbiol. 8:847-856.
19. Bull, J. J., B. R. Levin, T. DeRouin, N. Walker, and C. A. Bloch. 2002. Dynamics of success and failure in phage and antibiotic therapy in experimental infections. BMC Microbiol. 35:1-10.
20. Callaway, T. R., J. A. Carroll, J. D. Arthington, C. Pratt, T. S. Edrington, R. C. Anderson, S. C. Ricke, P. Crandall, and D. J. Nisbet. 2008a. Citrus products decrease growth of E. coli O157:H7 and Salmonella Typhimurium in pure culture and in fermentation with mixed ruminal microorganism in vitro. Foodborne Pathog. Dis. 5:621-627.
21. 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. 2008b. Bacteriophage isolated from feedlot cattle can reduce Escherichia coli O157:H7 populations in ruminant gastrointestinal tracts. Foodborne Pathog. Dis. 5:183-191.
22. Callaway, T. R., J. A. Carroll, J. D. Arthington, T. S. Edrington, R. C. Anderson, M. L. Rossman, M. A. Carr, K. J. Genovese, S. C. Ricke, P. Crandall, and D. J. Nisbet. 2011a. Orange peel products can reduce Salmonella populations in ruminants. Foodborne Path. Dis. 8:1071-1075.
23. Callaway, T. R., J. A. Carroll, J. D. Arthington, T. S. Edrington, M. L. Rossman, M. A. Carr, N. A. Krueger, S. C. Ricke, P. Crandall, and D. J. Nisbet. 2011b. Escherichia coli O157:H7 populations in ruminants can be reduced by orange peel product feeding. J. Food Prot. 74:1917-1921.
24. Callaway, T. R., J. A. Carroll, J. D. Arthington, T. S. Edrington, R. C. Anderson, S. C. Ricke, P. Crandall, C. Collier, and D. J. Nisbet. 2011c. Chapter 17. Citrus products and their use against bacteria: Potential health and cost benefits. In: R. Watson, J. K. Gerald, and V. R. Preedy (eds). Nutrients, Dietary Supplements, and Nutriceuticals: Cost analysis versus clinical benefits. Humana Press, New York. pp. 277-286.
25. Chalova, V. I., P. G. Crandall, and S. C. Ricke. 2010. Microbial inhibitory and radical scavenging activities of cold-pressed terpeneless Valencia (Citrus sinensis) orange oil in different dispersing agents. J. Sci. Food Agric. 90:870-876.
26. Chaves, A. V., M. L. He., W. Z. Yang, A. N. Hristov, T. A. McAllister and C. Benchaar. 2008. Effects of essential oils on proteolytic, deaminative and methanogenic activities of mixed ruminal bacteria. Can. J. Anim. Sci. 88:117-122.
27. Coleman, M. E, D.W. Dreesen, and R. G.Wiegert. 1996. A simulation of microbial competition in the human colonic ecosystem. Appl. Environ. Microbiol. 62:3632-3639.
28. Connerton, P. L. and I. F. Connerton. 2005. Microbial treatments to reduce pathogens in poultry meat. In: G. C. Mead (ed) Food Safety Control in the Poultry Industry. Woodhead Publishing Ltd., Cambridge. pp. 414-432.
29. Dabrowska, K., K. Switala-Jelen, A. Opolski, B. Weber-Dabrowska, and A. Gorski. 2005. Bacteriophage penetration in vertebrates. J. Appl. Microbiol. 98:7-13.
30. Deresinski, S. 2009. Bacteriophage therapy: Exploiting smaller fleas. Clin. Infect. Dis. 48:1096-1101.
31. Dunkley, K. D., T. R. Callaway, C. O'Bryan, M. M. Kundinger, C. S. Dunkley, R. C. Anderson, D. J. Nisbet, P. G. Crandall, and S. C. Ricke. 2009a. Cell yields and fermentation responses of a Salmonella Typhimurium poultry isolate at different dilution rates in an anaerobic steady state continuous culture (CC). Antonie van Leeuwenhoek. J. Gen. Mol. Microbiol. 96:537-544.
32. Dunkley, K. D., T. R. Callaway, V. I. Chalova, J. L. McReynolds, M. E. Hume, C. S. Dunkley, L. F. Kubena, D. J. Nisbet, and S. C. Ricke. 2009b. Foodborne Salmonella ecology in the avian gastrointestinal tract. Anaerobe 15:26-35.
33. Durant, J. A., D. E. Corrier, J. A. Byrd, L. H. Stanker, and S. C. Ricke. 1999. Feed deprivation affects crop environment and modulates Salmonella enteritidis colonization and invasion of Leghorn hens. Appl. Environ. Microbiol. 65:1919-1923.
34. Felix, A. and B. R. Callow. 1943. Typing of paratyphoid bacilli by means of Vi bacteriophage. Br. Med. J. 2:127-130.
35. Fiorentin, L., N. D. Vieira and W. Barioni Jr. 2005. Oral treatment with bacteriophages reduces the concentration of Salmonella Enteritidis PT4 in caecal contents of broilers. Avian Pathology 34:258-263.
36. Freifelder, D. 1983. Molecular Biology-A Comprehensive Introduction to Prokaryotes and Eukaryotes. Jones and Bartlett Publishers, Inc., Boston, MA.
37. Friedly, E. C., P. G. Crandall, S. C. Ricke, M. Roman, C. A. O'Bryan and V. I. Chalova. 2009. In vitro anti-listerial effects of citrus oil fractions in combination with organic acids. J. Food Sci. 74:M67-M72.
38. Goode, D., V. M. Allen, and P. A. Barrow. 2003. Reduction of experimental Salmonella and Campylobacter contamination of chicken skin by application of lytic bacteriophages. Appl. Environ. Microbiol. 69:5032-5036.
39. Górski, A., E. Wazna, B.W. Dabrowska, K. Dabrowska, K. Switala-Jelen, and R. Miedzybrodzki. 2006. Bacteriophage translocation. FEMS Immunol. Med. Microbiol. 46:313-319.
40. 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. 75:93-100.
41. Guilfoyle, D. E., and I. N. Hirshfield. 1994. The molecular response of Escherichia coli to the short chain organic acid butyrate. Ann. N.Y. Acad. Sci. 730:246-248.
42. Guilfoyle, D. E., and I. N. Hirshfield. 1996. The survival benefit of short chain organic acids and the inducible arginine and lysine decarboxylase genes for Escherichia coli. Lett. Appl. Microbiol. 22:393-396.
43. Hayes, W. 1968. The Genetics of Bacteria and Their Viruses, 2nd edn. John Wiley & Sons. New York.
44. Higgins, J. P., R. L. Andreatti Filho, S. E. Higgins, A. D. Wolfenden, G. Tellez, and B. M. Hargis. 2008. Evaluation of Salmonella-lytic properties of bacteriophages isolated from commercial broiler houses. Avian Dis. 52:139-142.
45. Higgins, J. P., S. E. Higgins, K. L. Guenther, W. Huff, A. M. Donoghue, D. J. Donoghue, and B. M. Hargis. 2005. Use of a specific bacteriophage treatment to reduce Salmonella in poultry products. Poult. Sci. 84:1141-1145.
46. Hoelzer, K., B. D. Sauders, M. D. Sanchez, P. T. Olsen, M. M. Pickett, K. J. Mangione, D. H. Rice, J. Corby, S. Stich, E. D. Fortes, S. E. Roof, Y. T. Grohn, M. Wiedmann, and H. F. Oliver. 2011. Prevalence, distribution, and diversity of Listeria monocytogenes in retail environments, focusing on small establishments and establishments with a history of failed inspections. J. Food Prot. 74:1083-1095.
47. Holck, A. and J. Berg. 2009. Inhibition of Listeria monocytogenes in cooked ham by virulent bacteriophages and protective cultures. Appl. Environ. Microbiol. 75:6944-6946.
48. Hudson, J. A., C. Billington, G. Carey-Smith, and G. Greening. 2005. Bacteriophages as biocontrol agents in food. J. Food Prot. 68:426-437.
49. Huff, W. E., G. R. Huff, N. C. Rath, and A. M. Donoghue. 2010. Immune interference of bacteriophage efficacy when treating colibacillosis in poultry. Poult. Sci. 89:895-900.
50. Huff, W. G., G. R. Huff, N. C. Rath, J. M. Balog, and A. M. Donoghue. 2005. Alternatives to antibiotics: Utilization of bacteriophage to treat colibacillosis and prevent foodborne pathogens. Poult. Sci. 84:655-659.
51. Huff, W. E., G. R. Huff, N. C. Rath, J. M. Balog, and A. M. Donoghue. 2004. Chapter 27-Bacteriophage: Potential role in food safety. In: R. C. Beier, S. D. Pillai, T. D. Phillips, and R. L. Ziprin (eds) Pre-Harvest and Post-Harvest Food Safety: Contemporary Issues and Future Directions. Blackwell Publishing Professional, Ames, IA. pp. 365-374.
52. Huff, W. E., G. R. Huff, N. C. Rath, J. M. Balog, and A. M. Donoghue. 2003. Evaluation of aerosol spray and intramuscular injection of bacteriophage to treat an Escherichia coli respiratory infection. Poult. Sci. 82:1108-1112.
53. Huff, W. E., G. R. Huff, N. C. Rath, J. M. Balog, and A. M. Donoghue. 2002. Prevention of Escherichia coli infection in broiler chickens with a bacteriophage aerosol spray. Poult. Sci. 81:1486-1491.
54. Hurley, A., J. J. Mauer, 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. 52:599-607.
55. Iuchi, S. and E. C. C. Lin. 1993. Adaptation of Escherichia coli to redox environments by gene expression. Mol. Microbiol. 9:9-15.
56. Joerger, R. D. 2003. Alternatives to anitobiotics: Bacteriocins, antimicrobial peptidies and bacteriophages. Poult. Sci. 82:640-647.
57. Johnson, R. P., C. L. Gyles, W. E. Huff, S. Ojha, G. R. Huff, N. C. Rath and A. M. Donoghue. 2008. Bacteriophages for prophylaxis and therapy in cattle, poultry and pigs. Anim. Health Res. Reviews 9:201-215.
58. Jones, B. D. and S. Falkow. 1994. Identification and characterization of a Salmonella typhimurium oxygenregulated gene required for bacterial internalization. Infect. Immun. 62:3745-3752.
59. Jones, F. T. and S. C. Ricke. 2003. Observations on the history of the development of antimicrobials and their use in poultry feeds. Poult. Sci. 82:613-617.
60. 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. 76:5557-5564.
61. Kim, K.P., J.D. Cha, E. H. Yang, J. Klumpp, S. Hagens, W. D. Hardt, K. Y. Lee, and M. J. Loessner. 2008. PEGlyation of bacteriophages increases blood circulation time and reduces T-helper type-1 immune response. Microb. Biotech. 1:247-257.
62. Kim, M. and S. Ryu. 2011. Characterization of a T5-like coliphage, SPC35, and differential development of resistance to SPC35 in Salmonella enterica serovar Typhimurium and Escherichia coli. Appl. Environ. Microbiol. 77:2042-2050.
63. Koo, J., D. L. Marshall, and A. DePaola. 2001. Antacid increases survival of Vibrio vulnificus and Vibrio vulnificus phage in a gastrointestinal model. Appl. Environ. Microbiol. 67:2895-2902.
64. Kropinski, A. M. 2006. Phage therapy-Everything old is new again. Can. J. Dis. Med. Microbiol. 17:297-306.
65. Kudva, I. T., S. Jelacic, P. I. Tarr, P. Youderian, and C. J. Hovde. 1999. Biocontrol of Escherichia coli OI57 with O157 bacteriophages. Appl. Environ. Microbiol. 65:3767-3773.
66. Letarov, A. and E. Kulikov. 2009. The bacteriophages in human- and animal body-associated microbial communities. J. Appl. Microbiol. 107:1-13.
67. Leverentz, B., W. S. Conway, M. J. Camp, W. J. Janisiewicz, T. Abuladze, M. Yang, R. Saftner, A. Sulakvelidze. 2003. Biocontrol of Listeria monocytogenes on fresh-cut produce by treatment with lytic bacteriophages and a bacteriocin. Appl. Environ. Microbiol. 69:4519-4526.
68. Lianou, A. and J. N. Sofos. 2007. A review of the incidence and transmission of Listeria monocytogenes in ready-to-eat products in retail and food service environments. J. Food Prot. 70:2172-2198.
69. 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. 71:6554-6563.
70. Merril, C. R., B. Biswas, R. Carlton, N. C. Jensen, G. J. Creed, S. Zullo, S. Adhya. 1996. Long-circulationg bacteriophage as antibacterial agents. Prc. Natl. Acad. Sci. 93:3188-3192.
71. Miller, R. W., J. Skinner, A. Sulakvelidze, G. F. Mathis, and C. L. Hofacre. 2010. Bacteriophage therapy for control of necrotic enteritis of broiler chickens experimentally infected with Clostridium perfringens. Avian Dis. 54:33-40.
72. Nannapaneni, R., V. I. Chalova, P. G. Crandall, S. C. Ricke, M. G. Johnson, and C. A. O'Bryan. 2009b. Campylobacter and Arcobacter species sensitivity to commercial orange oil fractions. Int. J. Food Microbiol. 129:43-49.
73. Nannapaneni, R., V. I. Chalova, R. Story, K. C. Wiggins, P. G. Crandall, S. C. Ricke, and M. G. Johnson. 2009a. Ciprofloxacin-sensitive and ciprofloxacin-resistant Campylobacter jejuni are equally sensitive to natural orange oil-based antimicrobials. J. Environ. Sci. Health, Part B. 44:571-577.
74. Nannapaneni, R., A. Muthaiyan, P. G. Crandall, M. G. Johnson, C. A. O'Bryan, V. I. Chalova, T. R. Callaway, J. A. Carroll, J .D. Arthington, D. J. Nisbet, and S. C. Ricke. 2008. Antimicrobial activity of commercial citrus-based extracts against Escherichia coli O157:H7 isolates and mutant strains. Foodborne Path. Dis. 5:695-699.
75. Naylor, S. W., J. C. Low, T. E. Besser, A. Mahajan, G. J. Gunn, M. C. Pearce, I. J. McKendrick, D. G. E. Smith, and D. L. Gally. 2003. Lymphoid follicle dense mucosa at the terminal rectum is the principal site of colonization of enterohemorrhagic Escherichia coli O157:H7 in the bovine host. Infect. Immun. 71:1505-1512.
76. Nishino, K., T. Latifi, and E. A. Groisman. 2006. Virulence and drug resistance roles of multidrug efflux systems of Salmonella enterica serovar Typhimurium. Mol. Microbiol. 59:126-141.
77. Niu, Y. D., T. A. McAllister, Y. Xu, R. P. Johnson, T. P. Stephens, and K. Stanford. 2009. Prevalence and impact of bacteriophages on the presence of Escherichia coli O157:H7 in feedlot cattle and their environment. Appl. Environ. Microbiol. 75:1271-1278.
78. O'Bryan, C. A., P. G. Crandall, V. I. Chalova, and S. C. Ricke. 2008a. Orange essential oils antimicrobial activities against Salmonella spp. J. Food Sci. 73:M264.
79. O'Bryan, C. A., P. G. Crandall and S. C. Ricke. 2008b. Organic poultry pathogen control from farm to fork. Foodborne Path. Dis. 5:709-720.
80. O'Flynn, G., R. P. Ross, G. F. Fitzgerald, andA. Coffey. 2004. Evaluation of a cocktail of three bacteriophages for biocontrol of Escherichia coli O157:H7. Appl. Environ. Microbiol. 69:4519-4526.
81. Payne, R. J. H. and V. A. A. Jansen. 2001. Understanding bacteriophage therapy as a density-dependent kinetic process. J. Theor. Biol. 208:37-48.
82. Ramesh, V., J. A. Fralick, and R. D. Rolfe. 1999. Prevention of Clostridium difficile-induced ileocecitis with bacteriophage. Anaerobe. 5:69-78.
83. Ricci, V. and L. J. V. Piddock. 2010. Exploiting the role of TolC in pathogenicity: identification of a bacteriophage for eradication of Salmonella serovars from poultry. Appl. Environ. Microbiol. 76:1704-1706.
84. Ricke, S. C. 2003a. Perspectives on the use of organic acids and short chain fatty acids as antimicrobials. Poultry Sci. 82:632-639.
85. Ricke, S. C. 2003b. The gastrointestinal tract ecology of Salmonella Enteritidis colonization in molting hens. Poultry Sci. 82:1003-1007.
86. Ricke, S. C.,M.M. Kundinger, D. R. Miller and J. T. Keeton. 2005. Alternatives to antibiotics: chemical and physical antimicrobial interventions and foodborne pathogen response. Poult. Sci. 84:667-675.
87. Rivas, L., B. Coffey, O. McAuliffe, M. J. McDonnell, C. M. Burgess, A. Coffey, R. P. Ross, and G. Duffy. 2010. In vivo and ex vivo evaluations of bacteriophages e11/2 and e4/1c for use in the control of Escherichia coli O157:H7. Appl. Environ. Microbiol. 76:7210-7216.
88. Rowbury, R. J. 1995. An assessment of environmental factors influencing acid tolerance and sensitivity in Escherichia coli, Salmonella spp. and other enterobacteria. Lett. Appl. Microbiol. 20:333-337.
89. Rozema, E. A., T. P. Stephens, S. J. Bach, E. K. Okine, R. P. Johnson, K. Stanford, and T. A. McAllister. 2009. Oral and rectal administration of bacteriophages for control of Escherichia coli O157:H7 in feedlot cattle. J. Food Prot. 72:241-250.
90. Russell, J. B. 1992. Another explanation for the toxicity of fermentation acids at lowpH-anion accumulation versus uncoupling. J. Appl. Bacteriol. 73:363-370.
91. Santos, S. B., E. Fernandes, C. M. Carvalho, S. Sillankorva, V. N. Krylov, E. A. Pleteneva, O. V. Shaburova, A. Nicolau, E. C. Ferreira, and J. Azeredo. 2010. Selection and characterization of a multivalent Salmonella phage and its production in a nonpathogenic Escherichia coli strain. Appl. Environ. Microbiol. 76:7338-7342.
92. Schiemann, D. A. and S. R. Shope. 1991. Anaerobic growth of Salmonella typhimurium results in increased uptake by Henle 407 epithelial and mouse peritoneal cells in vitro and repression of a major outer membrane protein. Infect. Immun. 59:437-440.
93. 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. 43:1157-1163.
94. Shannon, E., S. R. Milillo, M. G. Johnson, and S. C. Ricke. 2011. Efficacy of cold pressed terpeneless valencia oil and its primary components on inhibition of Listeria species by direct contact and exposure to vapors. J. Food Sci. 76:M500-M503.
95. Sheng, H., H. J. Knecht, I. T. Kudva, and C. J. Hovde. 2006. Application of bacteriophages to control intestinal Escherichia coli O157:H7 levels in ruminants. Appl. Environ. Microbiol. 72:5359-5366.
96. Sirsat, S. A., A. Muthaiyan, and S. C. Ricke. 2009. Antimicrobials for pathogen reduction in organic and natural poultry production. J. Appl. Poultry Res. 18:379-388.
97. Sklar, I. B., and R. D. Joerger. 2001. Attempts to utilize bacteriophage to combat Salmonella enterica serovar enteritidis infection in chickens. J. Food Safety. 21:15-29.
98. Stent, G. S. and R. Calendar. 1978. Molecular Genetics-An Introductory Narrative, 2nd edn.W.H. Freeman and Company, San Francisco, CA.
99. Stone, R. 2002. Stalin's forgotten cure. Science 298:728-731.
100. Sulakvelidze, A. 2011. Safety by nature: potential bacteriophage applications. Microbe. 6:122-126.
101. Sulakvelidze, A., Z. Alavidze, and J. G. Morris. 2001. Bacteriophage therapy. Antimicrob. Agents Chemother. 45:649-659.
102. Summers, W. C. 2001. I. Bacteriophage Therapy. Annu. Rev. Microbiol. 55:437-51.
103. Tanji, Y., T. Shimada, M. Yoichi, K. Miyanaga, K. Hori, and H. Unno. 2004. Toward rational control of Escherichia coli O157:H7 by a phage cocktail. Appl. Microbiol. Biotechnol. 64:270-274.
104. Toro, H., S. B. Price, S. McKee, F. J. Hoerr, A. J. Krehling, M. Perdue, and L. Bauermeister. 2005. Use of bacteriophages in combination with competitive exclusion to reduce Salmonella from infected chickens. Avian Dis. 49:118-124.
105. USDA National Organic Program. 2008. Agricultural Marketing Service 7, Code of Federal Regulations (CFR), Part 205: the National Organic Program.
106. Wang, J., B. Hu, M. Xu, Q. Yan, S. Liu, X. Zu, Z. Sun, E. Reed, L. Ding, J. Gong, Q. Q. Li, and J. Hu. 2006. Use of bacteriophage in the experimental treatment of bacteremia from imipenem-resistant Pseudomonas aeruginosa. Int. J. Mol. Med. 17:309-317.
107. Waseh, S., P. Hanifi-Moghaddam, R. Coleman, M. Masotti, S. Ryan S, M. Foss, R. MacKenzie1, M. Henry, C. M. Szymanski, and J. Tanha. 2010. Orally administered P22 phage tailspike protein reduces Salmonella colonization in chickens: Prospects of a novel therapy against bacterial infections. PLoS One. 5:e13904.
108. Weiss, M., E. Denou, A. Bruttin, R. Serra-Moreno, M.-L. Dillmann, and H. Brüssow. 2009. In vivo replication of T4 and T7 bacteriophages in germ-free mice colonized with Escherichia coli. Virology 393:16-23.
109. Weld, R. J., C. Butts, and J. A. Heinemmann. 2004. Models of phage growth and their applicability to phage therapy. J. Theoretical Biol. 227:1-11.
110. Whichard, J. M., N. Sriranganathan, and F.W. Pierson. 2003. Supression of Salmonella growth by wild-type large-plaque variants of bacteriophage Felix Olin liquid culture and on chicken frankfurters. J. Food Prot. 66:220-225.
111. Williams Smith, H. and M. B. Huggins. 1983. Effectiveness of phages in treating experimental Escherichia coli diarrhoea in calves, piglets and lambs. J. Gen. Microbiol. 129:2659-2675.
112. Williams Smith, H., M. B. Huggins, K. M. Shaw. 1987a. The control of experimental Escherichia coli diarrhoea in calves by means of bacteriophages. J. Gen. Microbiol. 133:1111-1126.
113. Williams Smith, H., M. B. Huggins, K. M. Shaw. 1987b. Factors influencing the survival and multiplication of bacteriophages in calves and in their environment. J. Gen. Microbiol. 133:1127-1135.