1932

Abstract

Despite advances in modern technologies, the food industry is continuously challenged with the threat of microbial contamination. The overuse of antibiotics has further escalated this problem, resulting in the increasing emergence of antibiotic-resistant foodborne pathogens. Efforts to develop new methods for controlling microbial contamination in food and the food processing environment are extremely important. Accordingly, bacteriophages (phages) and their derivatives have emerged as novel, viable, and safe options for the prevention, treatment, and/or eradication of these contaminants in a range of foods and food processing environments. Whole phages, modified phages, and their derivatives are discussed in terms of current uses and future potential as antimicrobials in the traditional farm-to-fork context, encompassing areas such as primary production, postharvest processing, biosanitation, and biodetection. The review also presents some safety concerns to ensure safe and effective exploitation of bacteriophages in the future.

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2014-02-28
2024-06-20
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Literature Cited

  1. Abedon ST. 2011. Lysis from without. Bacteriophage 1:1–4 [Google Scholar]
  2. Adu-Bobie J, Trabulsi LR, Carneiro-Sampaio MMS, Dougan G, Frankel G. 1998. Identification of immunodominant regions within the C-terminal cell binding domain of intimin α and intimin β from enteropathogenic Escherichia coli. Infect. Immun. 66:5643–49 [Google Scholar]
  3. Allen HK, Levine UY, Looft T, Bandrick M, Casey TA. 2013. Treatment, promotion, commotion: antibiotic alternatives in food-producing animals. Trends Microbiol. 21:114–19 [Google Scholar]
  4. Anany H, Chen W, Pelton R, Griffiths MW. 2011. Biocontrol of Listeria monocytogenes and Escherichia coli O157:H7 in meat by using phages immobilized on modified cellulose membranes. Appl. Environ. Microbiol. 77:6379–87 [Google Scholar]
  5. Arya SK, Singh A, Naidoo R, Wu P, McDermott MT, Evoy S. 2011. Chemically immobilized T4-bacteriophage for specific Escherichia coli detection using surface plasmon resonance. Analyst 136:486–92 [Google Scholar]
  6. Atterbury RJ, Connerton PL, Dodd CE, Rees CE, Connerton IF. 2003. Application of host-specific bacteriophages to the surface of chicken skin leads to a reduction in recovery of Campylobacter jejuni. Appl. Environ. Microbiol. 69:6302–6 [Google Scholar]
  7. Bach SJ, Johnson RP, Stanford K, McAllister TA. 2009. Bacteriophages reduce Escherichia coli O157:H7 levels in experimentally inoculated sheep. Foodborne Pathog. Dis. 5:183–91 [Google Scholar]
  8. Bardina C, Spricigo DA, Cortes P, Llagostera M. 2012. Significance of the bacteriophage treatment schedule in reducing Salmonella colonization in poultry. Appl. Environ. Microbiol. 78:6600–7 [Google Scholar]
  9. Berchieri A Jr, Lovell MA, Barrow PA. 1991. The activity in the chicken alimentary tract of bacteriophages lytic for Salmonella Typhimurium. Res. Microbiol. 142:541–49 [Google Scholar]
  10. Bigot B, Lee WJ, McIntyre L, Wilson T, Hudson JA. et al. 2011. Control of Listeria monocytogenes growth in a ready-to-eat poultry product using a bacteriophage. Food Microbiol. 28:1448–52 [Google Scholar]
  11. Blasco R, Murphy MJ, Sanders MF, Squirrell DJ. 1998. Specific assays for bacteria using phage mediated release of adenylate kinase. J. Appl. Microbiol. 84:661–66 [Google Scholar]
  12. Borie C, Albala P, Sanchez P, Sanchez ML, Ramirez S. et al. 2008. Bacteriophage treatment reduces Salmonella colonization of infected chickens. Avian Dis. 52:64–67 [Google Scholar]
  13. Boyacioglu O, Sharma M, Sulakvelidze A, Goktepe I. 2013. Biocontrol of Escherichia coli O157:H7 on fresh-cut leafy greens: using a bacteriophage cocktail in combination with modified atmosphere packaging. Bacteriophage 3:e24620 [Google Scholar]
  14. Bren L. 2007. Bacteria-eating virus approved as food additive. FDA Consum. 41:20–22 [Google Scholar]
  15. Bruttin A, Brussow H. 2005. Human volunteers receiving Escherichia coli phage T4 orally: a safety test of phage therapy. Antimicrob. Agents Chemother. 49:2874–78 [Google Scholar]
  16. Callewaert L, Walmagh M, Michiels CW, Lavigne R. 2011. Food applications of bacterial cell wall hydrolases. Curr. Opin. Biotechnol. 22:164–71 [Google Scholar]
  17. Callaway TR, Edrington TS, Brabban A, Kutter B, Karriker L. et al. 2011. Evaluation of phage treatment as a strategy to reduce Salmonella populations in growing swine. Foodborne Pathog. Dis. 8:261–66 [Google Scholar]
  18. Carlton RM, Noordman WH, Biswas B, de Meester ED, Loessner MJ. 2005. Bacteriophage P100 for control of Listeria monocytogenes in foods: genome sequence, bioinformatic analyses, oral toxicity study, and application. Regul. Toxicol. Pharmacol. 43:301–12 [Google Scholar]
  19. Carrillo CL, Atterbury RJ, El-Shibiny A, Connerton PL, Dillon E. et al. 2005. Bacteriophage therapy to reduce Campylobacter jejuni colonization of broiler chickens. Appl. Environ. Microbiol. 71:6554–63 [Google Scholar]
  20. CDC 2011. 2011. estimates of foodborne illness in the United States: CDC estimates that each year roughly 1 in 6 Americans (or 48 million people) gets sick, 128,000 are hospitalized, and 3,000 die of foodborne diseases: CDC, Atlanta, updated April 15, 2011, accessed on May 4, 2013. http://www.cdc.gov/features/dsfoodborneestimates/
  21. Chen J, Novick RP. 2009. Phage-mediated intergeneric transfer of toxin genes. Science 323:139–41 [Google Scholar]
  22. Cherla RP, Lee SY, Tesh VL. 2003. Shiga toxins and apoptosis. FEMS Microbiol. Lett. 228:159–66 [Google Scholar]
  23. Clark JR, March JB. 2006. Bacteriophages and biotechnology: vaccines, gene therapy and antibacterials. Trends Biotechnol. 24:212–18 [Google Scholar]
  24. Coffey B, Mills S, Coffey A, McAuliffe O, Ross RP. 2010. Phage and their lysins as biocontrol agents for food safety applications. Annu. Rev. Food Sci. Technol. 1:499–68 [Google Scholar]
  25. Coffey B, Rivas L, Duffy G, Coffey A, Ross RP, McAuliffe O. 2011. Assessment of Escherichia coli O157:H7-specific bacteriophages e11/2 and e4/1c in model broth and hide environments. Int. J. Food Microbiol. 147:188–94 [Google Scholar]
  26. Connerton PL, Loc Carrillo CM, Swift C, Dillon E, Scott A. et al. 2004. Longitudinal study of Campylobacter jejuni bacteriophages and their hosts from broiler chickens. Appl. Environ. Microbiol. 70:3877–83 [Google Scholar]
  27. Cossart P, Lecuit M. 1998. Interactions of Listeria monocytogenes with mammalian cells during entry and actin-based movement: bacterial factors, cellular ligands and signalling. EMBO J. 17:3797–806 [Google Scholar]
  28. Cromwell GL. 2002. Why and how antibiotics are used in swine production. Anim. Biotechnol. 13:7–27 [Google Scholar]
  29. Deresinski S. 2009. Bacteriophage therapy: exploiting smaller fleas. Clin. Infect. Dis. 48:1096–101 [Google Scholar]
  30. Donaghy JA, Totton NL, Rowe MT. 2004. Persistence of Mycobacterium paratuberculosis during manufacturing and ripening of cheddar cheese. Appl. Environ. Microbiol. 70:4899–905 [Google Scholar]
  31. Doolittle MM, Cooney JJ, Caldwell DE. 1995. Lytic infection of Escherichia coli biofilms by bacteriophage T4. Can. J. Microbiol. 41:12–18 [Google Scholar]
  32. Doyle ME. 2007. Microbial Food Spoilage—Losses and Control Strategies: A Brief Review of the Literature Madison, WI: Food Res. Inst. Brief., Univ. Wisc. [Google Scholar]
  33. DuPont HL, Levine MM, Hornick RB, Formal SB. 1989. Inoculum size in shigellosis and implications for expected mode of transmission. J. Infect. Dis. 159:1126–28 [Google Scholar]
  34. Edgar R, McKinstry M, Hwang J, Oppenheim AB, Fekete RA. et al. 2006. High sensitivity bacterial detection using biotin-tagged phage and quantum-dot nano complexes. Proc. Natl. Acad. Sci. USA 103:4841–45 [Google Scholar]
  35. El-Shibiny A, Scott A, Timms A, Metawea Y, Connerton P, Connerton I. 2009. Application of a group II Campylobacter bacteriophages to reduce strains of Campylobacter jejuni and Campylobacter coli colonizing broiler chickens. J. Food Prot. 72:733–40 [Google Scholar]
  36. Endersen L, Coffey A, Neve H, McAuliffe O, Ross RP, O'Mahony JM. 2012. Isolation and characterisation of six novel mycobacteriophages and investigation of their antimicrobial potential in milk. Int. Dairy J. 28:8–14 [Google Scholar]
  37. Eugster MR, Haug MC, Huwiler SG, Loessner MJ. 2011. The cell wall binding domain of Listeria bacteriophage endolysin PlyP35 recognizes terminal GlcNAc residues in the cell wall teichoic acid. Mol. Microbiol. 81:1419–32 [Google Scholar]
  38. Everest PH, Cole AT, Hawkey CJ, Knutton S, Goossens H. et al. 1993. Roles of leukotriene B4, prostaglandin E2, and cyclic AMP in Campylobacter jejuni-induced intestinal fluid secretion. Infect. Immun. 61:4885–87 [Google Scholar]
  39. Feng Y, Joshua G, Yu H, Jin Y, Zhu J, Han Y. 2010. Identification of changes in the composition of ileal bacterial microbiota of broiler chickens infected with Clostridium perfringens. Vet. Mirobiol. 140:116–21 [Google Scholar]
  40. Fenton M, Keary R, McAuliffe O, Ross RP, O'Mahony J, Coffey A. 2013. Bacteriophage-derived peptidase CHAPk eliminates and prevents staphylococcal biofilms. Int. J. Microbiol. 2013:625341 [Google Scholar]
  41. Ferreira AA, Mendonca RCS, Hungaro HM, Carvalho MM, Pereira JAM. 2011. Bacteriophages actions on Salmonella Enteritidis biofilm. Science and Technology Against Microbial Pathogens—Research, Development and Evaluation: Proceedings of the International Conference on Antimicrobial Research (ICAR2010) Valladolid, Spain, 3–5 November 2010 A Mendez-Vilas 135 Hackensack, NJ: World Sci. Pub. Co. [Google Scholar]
  42. Fey PD, Safranek TJ, Rupp ME, Dunne EF, Ribot E. et al. 2000. Ceftriaxone-resistant Salmonella acquired by a child from cattle. N. Eng. J. Med. 342:1242–49 [Google Scholar]
  43. Flaherty JE, Jones JB, Harbaugh BK, Somodi GC, Jackson LE. 2000. Control of bacterial spot on tomato in the greenhouse and field with H-mutant bacteriophages. Hort. Sci. 35:882–84 [Google Scholar]
  44. Fruciano DE, Bourne S. 2007. Phage as an antimicrobial agent: d'Herelle's heretical theories and their role in the decline of phage prophylaxis in the West. Can. J. Infect. Dis. Med. Microbiol. 18:19–26 [Google Scholar]
  45. Gaeng S, Scherer S, Neve H, Loessner. 2000. Gene cloning and expression and secretion of Listeria monocytogenes bacteriophage-lytic enzymes in Lactococcus lactis. Appl. Environ. Microbiol. 66:2851–958 [Google Scholar]
  46. Garcia P, Rodriguez L, Rodriguez A, Martinez B. 2010. Food biopreservation: promising strategies using bacteriocins, bacteriophages and endolysins. Trends Food Sci. Technol. 21:373–82 [Google Scholar]
  47. Giannella RA. 1996. Chapter 21: Salmonella. Medical Microbiology S Baron 143–51 Galveston: Univ. Tex. Med. Branch, 4th. http://www.ncbi.nlm.nih.gov/books/NBK8435/ [Google Scholar]
  48. Gill JJ, Hyman P. 2010. Phage choice, isolation, and preparation for phage therapy. Curr. Pharm. Biotechnol. 11:2–14 [Google Scholar]
  49. Goodridge LD, Bisha B. 2011. Phage-based biocontrol strategies to reduce foodborne pathogens in foods. Bacteriophage 1:130–37 [Google Scholar]
  50. Gram L, Ravn L, Rasch M, Bruhn JB, Christensen AB, Givskov M. 2002. Food spoilage—interactions between food spoilage bacteria. Int. J. Food Microbiol. 78:79–97 [Google Scholar]
  51. Grant IR, Ball HJ, Rowe MT. 1998. Effect of high-temperature, short-time (HTST) pasteurization on milk containing low numbers of Mycobacterium paratuberculosis. Lett. Appl. Microbiol. 26:116–70 [Google Scholar]
  52. Grant IR, Ball HJ, Rowe MT. 2002. Incidence of Mycobacterium paratuberculosis in bulk raw and commercially pasteurized cows' milk from approved dairy processing establishments in the United Kingdom. Appl. Environ. Microbiol. 68:2428–35 [Google Scholar]
  53. Guenther S, Herzig O, Fieseler L, Klimpp J, Loessner MJ. 2012. Biocontrol of Salmonella typhimurium in RTE foods with the virulent bacteriophage FO1-E2. Int. J. Microbiol. 154:66–72 [Google Scholar]
  54. Guenther S, Huwyler D, Richard S, Loessner MJ. 2009. Virulent bacteriophage for efficient biocontrol of Listeria monocytogenes in ready-to-eat foods. Appl. Environ. Microbial. 75:93–100 [Google Scholar]
  55. Hagens S, Offerhaus ML. 2008. Bacteriophages—new weapons for food safety. Food Technol. 62:446–54 [Google Scholar]
  56. Harper DR, Morales S. 2012. Bacteriophage therapy: practicability and clinical need meet in the multidrug-resistance era. Future Microbiol. 7:797–99 [Google Scholar]
  57. Herold S, Karch H, Schmidt H. 2004. Shiga toxin-encoding bacteriophages—genomes in motion. Int. J. Med. Microbiol. 294:115–21 [Google Scholar]
  58. Higgins JP, Higgins SE, Guenther K, Huff W, Donoghue AM. et al. 2005. Use of specific bacteriophage treatment to reduce Salmonella in poultry products. Poult. Sci. 84:1141–45 [Google Scholar]
  59. Hodgson K. 2013. Bacteriophage therapy. Microbiol. Aust. 34:28–31 [Google Scholar]
  60. Hooten SPT, Atterbury RJ, Connerton IF. 2011. Application of a bacteriophage cocktail to reduce Salmonella Typhimurium U288 contamination on pig skin. Int. J. Food Microbiol. 151:157–63 [Google Scholar]
  61. Hungaro MH, Santos Mendonca RC, Gouvea DM, Danatas Vanetti MC, de Oliveira Pinto CL. 2013. Use of bacteriophages to reduce Salmonella in chicken skin in comparison with chemical agents. Food Res. Int. 52:75–81 [Google Scholar]
  62. Int. Messag. Access Protoc 2010. Food and Beverage Industry Global Report—2010. Barcelona, Sp: IMAP, Inc http://www.imap.com/imap/media/resources/IMAP_Food__Beverage_Report_WEB_AD6498A02CAF4.pdf [Google Scholar]
  63. Kaper JB. 1998. Enterohemorrhagic Escherichia coli. Curr. Opin. Microbiol. 1:103–8 [Google Scholar]
  64. Kelly D, McAuliffe O, Ross RP, Coffey A. 2012. Prevention of Staphylococcus aureus biofilm formation and reduction in established biofilm density using a combination of phage K and modified derivatives. Lett. Appl. Microbiol. 54:286–91 [Google Scholar]
  65. Kent TH. 1966. Staphylococcal enterotoxin gastroenteritis in rhesus monkeys. Am. J. Pathol. 48:387–407 [Google Scholar]
  66. Kim KP, Klumpp J, Loessner MJ. 2007. Enterobacter sakazakii bacteriophages can prevent bacterial growth in reconstituted infant formula. Int. J. Food. Microbiol. 115:195–203 [Google Scholar]
  67. Konkel ME, Hayes SF, Joens LA, Cieplak W Jr. 1992. Characteristics of the internalization of intracellular survival of Campylobacter jejuni in human epithelial cell cultures. Microb. Pathog. 13:357–70 [Google Scholar]
  68. Kretzer JW, Lehmann R, Schmelcher M, Banz M, Kim KP. et al. 2007. Use of high-affinity cell wall-binding domains of bacteriophage endolysins for immobilization and separation of bacterial cells. Appl. Environ. Microbiol. 73:1992–2000 [Google Scholar]
  69. Kropinski AM. 2006. Phage therapy—Everything old is new again. Can. J. Infect. Dis. Med. Microbiol. 17:297 [Google Scholar]
  70. Kuhn M, Goebel W. 1999. Pathogenesis of Listeria monocytogenes. Listeria, Listeriosis, and Food Safety ET Ryser, EH Marth 97–130 New York: CRC [Google Scholar]
  71. Kutter E, Sulakvelidze A. 2005. Bacteriophages—Biology and Applications Boca Raton, FL: CRC [Google Scholar]
  72. Leverentz B, Conway WS, Alavidze Z, Janisiewicz WJ, Fuchs Y. et al. 2001. Examination of bacteriophages as a biocontrol method for Salmonella on fresh-cut fruit. J. Food Prot. 64:1116–21 [Google Scholar]
  73. Leverentz B, Conway WS, Camp MJ, Janisiewicz WJ, Abuladze T. et al. 2003. Biocontrol of Listeria monocytogenes on fresh-cut produce by treatment with lytic bacteriophages and a bacteriocin. Appl. Environ. Microbiol. 69:4519–26 [Google Scholar]
  74. Li Q, Zhao WD, Zhang K, Fang WG, Hu Y. et al. 2010. PI3K-dependant host cell actin rearrangements are required for Cronobacter sakazakii invasion of human brain microvascular endothelial cells. Med. Microbiol. Immunol. 199:333–40 [Google Scholar]
  75. Lim TH, Kim MS, Lee DH, Lee YN, Park JK. et al. 2012. Use of bacteriophage for biological control of Salmonella enteritidis infection in chicken. Res. Vet. Sci. 93:1173–78 [Google Scholar]
  76. Loessner MJ, Rees CE, Stewart GS, Scherer S. 1996. Construction of luciferase reporter bacteriophage A511::luxAB for rapid and sensitive detection of viable Listeria cells. Appl. Environ. Microbiol. 62:1133–40 [Google Scholar]
  77. Loessner MJ, Kramer K, Ebel F, Scherer S. 2002. C-terminal domains of Listeria monocytogenes bacteriophage murein hydrolases determine specific recognition and high-affinity binding to bacterial cell wall carbohydrates. Mol. Microbiol. 44:335–49 [Google Scholar]
  78. Loessner MJ. 2005. Bacteriophage endolysins—current state of research and applications. Curr. Opin. Microbiol. 8:480–87 [Google Scholar]
  79. McKenna F, El-Tarabily KA, Hardy GEStJ, Dell B. 2001. Novel in vivo use of a polyvalent Streptomyces phage to disinfest Streptomyces scabies-infected seed potatoes. Plant Pathol. 50:666–75 [Google Scholar]
  80. Mills S, Shanahan F, Stanton C, Coffey A, Ross RP. 2013. Movers and shakers: influence of bacteriophages in shaping the mammalian gut microbiota. Gut Microbes 4:4–16 [Google Scholar]
  81. Modi R, Hirvi Y, Hill A, Griffiths MW. 2001. Effect of phage on survival of Salmonella enteritidis during the manufacture and storage of cheddar cheese made from raw and pasteurized milk. J. Food Prot. 64:927–33 [Google Scholar]
  82. Mohawk KL, Melton-Celsa AR, Zangari T, Carroll EE, O'Brien A. 2010. Pathogenesis of Escherichia coli O157:H7 strain 86–24 following oral infection of BALB/c mice with an intact commensal flora. Microb. Pathog. 48:131–42 [Google Scholar]
  83. Monk AB, Rees CD, Barrow P, Hagens S, Harper DR. 2010. Bacteriophage applications: Where are we now?. Lett. Appl. Microbiol. 51:363–69 [Google Scholar]
  84. Moran AP. 1996. Biological and serological characterization of Campylobacter jejuni lipopolysaccharides with deviating core and lipid A structures. FEMS Immunol. Med. Microbiol. 11:121–30 [Google Scholar]
  85. Nat. Res. Counc. Agric. Board 1956. Proceedings, First International Conference on the Use of Antibiotics in Agriculture. Washington, DC: Nat. Acad. Press [Google Scholar]
  86. Nat. Res. Counc. Food Nutr. Board 1985. An Evaluation of the Role of Microbiological Criteria for Foods and Food Ingredients. Washington, DC: Nat. Acad. Press [Google Scholar]
  87. Obeso M, Martinez B, Rodrigeuz A, Garcia P. 2008. Lytic activity of the recombinant staphylococcal bacteriophage ΦH5 endolysin active against Staphylococcus aureus in milk. Int. J. Food Microbiol. 128:212–18 [Google Scholar]
  88. Obradovic A, Jones JB, Momol MT. 2004. Management of tomato bacterial spot in the field by foliar applications of bacteriophages and SAR inducers. Plant Dis. 88:736–40 [Google Scholar]
  89. O'Flaherty S, Ross RP, Coffey A. 2009. Bacteriophages and their lysins for elimination of infectious bacteria. FEMS Microbiol. Rev. 33:801–19 [Google Scholar]
  90. O'Flynn G, Ross RP, Fitzgerald GF, Coffey A. 2004. Evaluation of a cocktail of three bacteriophages for biocontrol of Escherischia coli O157:H7. Appl Environ. Microbiol. 70:3417–24 [Google Scholar]
  91. Oliver SP, Jayarao BM, Almeida RA. 2005. Foodborne pathogens in milk and the dairy farm environment: food safety and public health implications. Foodborne Pathog. Dis. 2:115–29 [Google Scholar]
  92. O'Mahony J, Fenton M, Henry M, Sleator RD, Coffey A. 2011a. Lysins to kill—a tale of viral weapons of mass destruction. Bioeng. Bugs 2:306–8 [Google Scholar]
  93. O'Mahony J, McAuliffe O, Ross RP, van Sinderen D. 2011b. Bacteriophages as biocontrol agents of food pathogens. Curr. Opin. Biotech. 22:157–63 [Google Scholar]
  94. Oyaski M, Hatfull GF. 1992. The cohesive ends of mycobacteriophage L5 DNA. Nuc. Acids Res. 20:123251 [Google Scholar]
  95. Pagotto FJ, Farber JM, Lenati R. 2008. Pathogenicity of Enterobacter sakazakii Washington, DC: ASM [Google Scholar]
  96. Plym LF, Wierup M. 2006. Salmonella contamination: a significant challenge to the global marketing of animal food products. Rev. Sci. Tech. 25:541–54 [Google Scholar]
  97. Raya RR, Oot RA, Moore-Maley B, Wieland S, Callaway TR. et al. 2011. Naturally resident and exogenously applied T4-like and T5-like bacteriophages can reduce Escherichia coli O157:H7 levels in sheep guts. Bacteriophage 1:15–24 [Google Scholar]
  98. Razzaghi-Abyaneh M, Shams-Ghahfarokhi M. 2011. 13 natural inhibitors of food-borne fungi from plants and microorganisms. Natural Antimicrobials in Food Safety and Quality M Rai 182–203 Wallingford, UK: CABI Publ. [Google Scholar]
  99. Renzoni A, Cossart P, Dramsi S. 1999. PrfA, the transcriptional activator of virulence genes, is unregulated during interaction of Listeria monocytogenes with mammalian cell extracts. Mol. Microbiol. 34:552–61 [Google Scholar]
  100. Rivas L, Coffey B, McAuliffe O, McDonnell MJ, Burgess CM. et al. 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. 76:7210–16 [Google Scholar]
  101. Rodríguez-Rubio L, Martinez B, Donovan DM, Garcia P, Rodriguez A. 2013. Potential of the virion-associated peptidoglycan hydrolase HydH5 and its derivative fusion proteins in milk biopreservation. PLoS ONE 8:e54828 [Google Scholar]
  102. Rozema EA, Stephens TP, Bach SJ, Okine EK, Johnson RP. et al. 2009. Oral and rectal administration of bacteriophages for control of Escherichia coli O157:H7 in feedlot cattle. J. Food Prot. 72:241–50 [Google Scholar]
  103. Saez AC, Zhang J, Rostagno MH, Ebner PD. 2011. Direct feeding of microencapsulated bacteriophages to reduce Salmonella colonization in pigs. Foodborne Pathog. Dis. 8:1269–74 [Google Scholar]
  104. Sansonetti PJ, Arondel JJ, Cantey R, Prevost MC, Huerre M. 1996. Infection of rabbit Peyer's patches by Shigella flexneri: effect of adhesive or invasion bacterial phenotypes on follicle-associated epithelium. Infect. Immun. 64:2752–64 [Google Scholar]
  105. Scallan E, Hoekstra RM, Angulo FJ, Tauxe RV, Widdowson MA. et al. 2011. Foodborne illness acquired in the United States—major pathogens. Emerg. Infect. Dis. 17:1–15 [Google Scholar]
  106. Scanlan PD, Buckling A. 2011. Co-evolution with lytic phage selects for the mucoid phenotype of Pseudomonas fluorescens SBW25. ISME J. 6:1148–58 [Google Scholar]
  107. Schlundt J. 2002. New directions in foodborne disease prevention. Int. J. Food Microbiol. 78:3–17 [Google Scholar]
  108. Schmidt H. 2001. Shiga-toxin-converting bacteriophages. Res. Microbiol. 152:687–95 [Google Scholar]
  109. Shakeeba W, Hanifi-Moghaddam P, Coleman, Masotti M, Ryan S. et al. 2010. Orally administered P22 phage tailspike protein reduces Salmonella colonization in chickens: prospects of novel therapy against bacterial infections. PLoS ONE 5:e13904 [Google Scholar]
  110. Shimizu T, Ohtani K, Hirakawa H, Yamashita A, Shiba T. et al. 2001. Complete genome sequence of Clostridium perfringens, an anaerobic flesh-eater. Proc. Natl. Acad. Sci. USA 99:996–1001 [Google Scholar]
  111. Shupp JW, Jett M, Pontzer CH. 2002. Identification of a transcytosis epitope on staphylococcal enterotoxins. Infect. Immun. 70:2178–86 [Google Scholar]
  112. Sillankorva S, Oliveira DR, Vieira MJ, Sutherland IW, Azeredo J. 2004. Bacteriophage ΦS1 infection of Pseudomonas flurescens planktonic cells versus biofilms. Biofouling 20:133–38 [Google Scholar]
  113. Sillankorva S, Pleteneva E, Shaburova O, Santos S, Carvaiho C. et al. 2010. Salmonella enteritidis bacteriophage candidates for phage therapy of poultry. J. Appl. Microbiol. 108:1175–86 [Google Scholar]
  114. Sillankorva SM, Oliverira H, Azeredo J. 2012. Bacteriophages and their role in food safety. Int. J. Microbiol 2012:863945 [Google Scholar]
  115. Simoes M, Simoes LC, Vieira MJ. 2008. A review of current and emergent biofilm control strategies. Food Sci. Tech. 43:573–83 [Google Scholar]
  116. Singh A, Poshtiban S, Evoy S. 2013. Recent advances in bacteriophages based biosensors for foodborne pathogen detection. Sensors 13:1763–86 [Google Scholar]
  117. Slopek S, Weber-Dabrowska B, Dabrowski M, Kucharewicz-Krukowska A. 1987. Results of bacteriophage treatment of suppurative bacterial infections in the years 1981–1986. Arch. Immunol. Ther. Exp. (Warsz.) 35:569–83 [Google Scholar]
  118. Soni KA, Nannapaneni R. 2010. Removal of Listeria monocytogenes biofilms with bacteriophage p100. J. Food Prot. 78:1519–24 [Google Scholar]
  119. Stanford K, McAllister TA, Niu YD, Stephens TP, Mazzocco A. et al. 2010. Oral delivery systems for encapsulated bacteriophages targeted at Escherichia coli O157:H7 in feedlot cattle. J. Food Prot. 73:1304–12 [Google Scholar]
  120. Stanley D, Keyburn AL, Denman SE, Moore RJ. 2012. Changes in the caecal microflora of chickens following Clostridium perfringens challenge to induce necrotic enteritis. Vet. Microbiol. 159:155–62 [Google Scholar]
  121. Stella EJ, De La Iglesia AI, Morbidoni HR. 2009. Mycobacteriophages as versatile tools for genetic manipulation of mycobacteria and development of simple methods for diagnosis of mycobacterial diseases. Rev. Argent. Microbiol. 41:45–55 [Google Scholar]
  122. Sulakvelidze A. 2001. Bacteriophage therapy. Antimicrob. Agents Chemother. 45:649–59 [Google Scholar]
  123. Sulakvelidze A. 2011. Safety by nature: potential bacteriophage applications. Microbe 6:122–26 [Google Scholar]
  124. Townsend SM, Hurrell E, Gonzalez-Gomez I, Lowe J, Frye JG. et al. 2007. Enterobacter sakazakii invades brain capillary endothelial cells, persists in human macrophages influencing cytokine secretion and induces severe brain pathology in the neonatal rat. Microbiology 153:3538–47 [Google Scholar]
  125. US Environ. Prot. Agency 2005. Xanthomonas campestris pv. vesicatoria and Pseudomonas syringae pv. tomato specific bacteriophages; exemption from the requirement of a tolerance. Fed. Regist. 7016700–4 http://www.epa.gov/EPA-PEST/2005/December/Day-28/p24540.pdf [Google Scholar]
  126. Viazis S, Akhtar M, Feirtag J, Diez-Gonzalez F. 2010. Reduction of Escherichia coli O157:H7 viability on leafy green vegetables by treatment with a bacteriophage mixture and trans-cinnamaldehyde. Food Microbiol. 28:149–57 [Google Scholar]
  127. Wagenaar JA, Van Bergen MAP, Mueller MA, Wassenaar TM, Carlton RM. 2005. Phage therapy reduces Campylobacter jejuni colonization in broilers. Vet. Med. 109:275–83 [Google Scholar]
  128. Wagner PL, Waldor MK. 2002. Bacteriophages control of bacterial virulence. Infect. Immun. 70:3985–93 [Google Scholar]
  129. Walcher G, Stessl B, Wagner M, Eichenseher F, Loessner MJ, Hein I. 2010. Evaluation of paramagnetic beads coated with recombinant Listeria phage endolysin-derived cell-wall-binding domain proteins for separation of Listeria monocytogenes from raw milk in combination with culture-based and real-time polymerase chain reaction-based quantification. Foodborne Pathog. Dis. 7:1019–24 [Google Scholar]
  130. Wall SK, Zhang J, Rostagno MH, Ebner PD. 2010. Phage therapy to reduce preprocessing Salmonella infections in market-weight swine. Appl. Environ. Mircobiol. 76:48–53 [Google Scholar]
  131. Walsh MC, Sholly DM, Hinson RB, Saddoris KL, Sutton AL. et al. 2007. Effect of water and diet acidification with and without weaning pig growth and microbial shedding. J. Anim. Sci. 85:1799–808 [Google Scholar]
  132. Waseh S, Hanifi-Moghaddam P, Coleman R, Masotti M, Ryan S. et al. 2010. Orally administered P22 phage tailspike protein reduces Salmonella colonization in chickens: prospects of a novel therapy against bacterial infections. PLoS ONE 5:e13904 [Google Scholar]
  133. Young R. 1992. Bacteriophage lysis: mechanism and regulation. Microbiol. Rev. 56:430–81 [Google Scholar]
  134. Young R, Blasi U. 1995. Holins: form and function in bacteriophage lysis. FEMS Microbiol. Rev. 17:191–205 [Google Scholar]
  135. Zhang H, Bao H, Billington C, Hudson JA, Wang R. 2012. Isolation and lytic activity of the Listeria bacteriophage endolysin LysZ5 against Listeria monocytogenes in soya milk. Food Microbiol. 31:133–36 [Google Scholar]
  136. Zhang H, Wang R, Hongduo B. 2013. Phage inactivation of foodborne Shigella on ready-to-eat spiced chicken. Poult. Sci. 92:211–17 [Google Scholar]
  137. Zimmer M, Vukov N, Scherer S, Loessner MJ. 2002. The murein hydrolase of the bacteriophage Φ3626 dual lysis system is active against all tested Clostridium perfringens strains. Appl. Environ. Microbiol. 68:5311–17 [Google Scholar]
  138. Zuber S, Boissin-Delaporte C, Michot L, Iversen C, Diep B. et al. 2008. Decreasing Enterobacter sakazakii (Cronobacter spp.) food contamination level with bacteriophages: prospects and problems. Microbiol. Biotechnol. 1:532–43 [Google Scholar]
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