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Abstract

Bacteriophages (phages) have traditionally been considered troublesome in food fermentations, as they are an important cause of starter-culture failure and trigger significant financial losses. In addition, from an evolutionary perspective, phages have contributed to the pathogenicity of many bacteria through transduction of virulence genes. In contrast, phages have played an important positive role in molecular biology. Moreover, these agents are increasingly being recognized as a potential solution to the detection and biocontrol of various undesirable bacteria, which cause either spoilage of food materials, decreased microbiological safety of foods, or infectious diseases in food animals and crops. The documented successful applications of phages and various phage-derived molecules are discussed in this review, as are many promising new uses that are currently under development.

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2019-03-25
2024-06-12
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Literature Cited

  1. Adamu Ahmad K, Sabo Mohammed A, Abas F 2016. Chitosan nanoparticles as carriers for the delivery of ΦKAZ14 bacteriophage for oral biological control of colibacillosis in chickens. Molecules 21:3256
    [Google Scholar]
  2. Ahmadi H, Anany H, Walkling-Ribeiro M, Griffiths MW 2015. Biocontrol of Shigella flexneri in ground beef and Vibrio cholerae in seafood with bacteriophage-assisted high hydrostatic pressure (HHP) treatment. Food Bioprocess Technol 8:51160–67
    [Google Scholar]
  3. Anany H, Chou Y, Cucic S, Derda R, Evoy S, Griffiths MW 2017. From bits and pieces to whole phage to nanomachines: pathogen detection using bacteriophages. Annu. Rev. Food Sci. Technol. 8:1305–29
    [Google Scholar]
  4. Argudín , Mendoza MC, Rodicio MR 2010. Food poisoning and Staphylococcus aureus enterotoxins. Toxins 2:71751–73
    [Google Scholar]
  5. Arthur TM, Kalchayanand N, Agga GE, Wheeler TL, Koohmaraie M 2017. Evaluation of bacteriophage application to cattle in Lairage at beef processing plants to reduce Escherichia coli O157:H7 prevalence on hides and carcasses. Foodborne Pathog. Dis. 14:117–22
    [Google Scholar]
  6. Back JP, Langford SA, Kroll RG 1993. Growth of Listeria monocytogenes in Camembert and other soft cheeses at refrigeration temperatures. J. Dairy Res. 60:3421–29
    [Google Scholar]
  7. Blaser MJ, LaForce FM, Wilson NA, Wang WL 1980. Reservoirs for human campylobacteriosis. J. Infect. Dis. 141:5665–69
    [Google Scholar]
  8. Bonilla N, Rojas MI, Netto Flores Cruz G, Hung S-H, Rohwer F, Barr JJ 2016. Phage on tap: a quick and efficient protocol for the preparation of bacteriophage laboratory stocks. PeerJ 4:e2261
    [Google Scholar]
  9. Botsaris G, Liapi M, Kakogiannis C, Dodd CER, Rees CED 2013. Detection of Mycobacterium avium subsp. paratuberculosis in bulk tank milk by combined phage-PCR assay: evidence that plaque number is a good predictor of MAP. Int. J. Food Microbiol. 164:176–80
    [Google Scholar]
  10. Botsaris G, Swift BMC, Slana I, Liapi M, Christodoulou M et al. 2016. Detection of viable Mycobacterium avium subspecies paratuberculosis in powdered infant formula by phage-PCR and confirmed by culture. Int. J. Food Microbiol. 216:91–94
    [Google Scholar]
  11. Boyd EF, Moyer KE, Shi L, Waldor MK 2000. Infectious CTXPhi and the vibrio pathogenicity island prophage in Vibrio mimicus: evidence for recent horizontal transfer between V. mimicus and V. cholerae. Infect. Immun 68:31507–13
    [Google Scholar]
  12. Breyne K, Honaker RW, Hobbs Z, Richter M, Żaczek M et al. 2017. Efficacy and safety of a bovine-associated Staphylococcus aureus phage cocktail in a murine model of mastitis. Front. Microbiol. 8:2348
    [Google Scholar]
  13. Buttimer C, McAuliffe O, Ross RP, Hill C, O'Mahony J, Coffey A 2017. Bacteriophages and bacterial plant diseases. Front. Microbiol. 8:34
    [Google Scholar]
  14. Canchaya C, Proux C, Fournous G, Bruttin A, Brüssow H 2003. Prophage genomics. Microbiol. Mol. Biol. Rev. 67:2238–76
    [Google Scholar]
  15. Carvalho CM, Gannon BW, Halfhide DE, Santos SB, Hayes CM et al. 2010. The in vivo efficacy of two administration routes of a phage cocktail to reduce numbers of Campylobacter coli and Campylobacter jejuni in chickens. BMC Microbiol 10:1232
    [Google Scholar]
  16. Cent. Dis. Control. (CDC). 2018. Reports of selected E. coli outbreak investigationsFact Sheet, CDC, Atlanta, GA. https://www.cdc.gov/ecoli/outbreaks.html
    [Google Scholar]
  17. Chang Y, Kim M, Ryu S 2017.a Characterization of a novel endolysin LysSA11 and its utility as a potent biocontrol agent against Staphylococcus aureus on food and utensils. Food Microbiol 68:112–20
    [Google Scholar]
  18. Chang Y, Yoon H, Kang D-H, Chang P-S, Ryu S 2017.b Endolysin LysSA97 is synergistic with carvacrol in controlling Staphylococcus aureus in foods. Int. J. Food Microbiol. 244:19–26
    [Google Scholar]
  19. Channabasappa S, Durgaiah M, Chikkamadaiah R, Kumar S, Joshi A, Sriram B 2017. Efficacy of novel antistaphylococcal ectolysin P128 in a rat model of methicillin-resistant Staphylococcus aureus bacteremia. Antimicrob. Agents Chemother. 62:2e01358–17
    [Google Scholar]
  20. Chen J, Griffiths MW 1996. Salmonella detection in eggs using Lux+ bacteriophages. J. Food Prot. 59:9908–14
    [Google Scholar]
  21. ChiHsin H, ChongYi L, JongKang L, ChanShing L 2000. Control of the eel (Anguilla japonica) pathogens, Aeromonas hydrophila and Edwardsiella tarda, by bacteriophages. J. Fish. Soc. Taiwan 27:121–31
    [Google Scholar]
  22. Choi IY, Park JH, Gwak KM, Kim K-P, Oh J-H, Park M-K 2018. Studies on lytic, tailed Bacillus cereus–specific phage for use in a ferromagnetoelastic biosensor as a novel recognition element. J. Microbiol. Biotechnol. 28:187–94
    [Google Scholar]
  23. Coffey A, Ross RP 2002. Bacteriophage-resistance systems in dairy starter strains: molecular analysis to application. Antonie Van Leeuwenhoek 82:1–4303–21
    [Google Scholar]
  24. 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. 147:3188–94
    [Google Scholar]
  25. Colavecchio A, Cadieux B, Lo A, Goodridge LD 2017. Bacteriophages contribute to the spread of antibiotic resistance genes among foodborne pathogens of the Enterobacteriaceae family: a review. Front. Microbiol. 8:1108
    [Google Scholar]
  26. Colom J, Cano-Sarabia M, Otero J, Aríñez-Soriano J, Cortés P et al. 2017. Microencapsulation with alginate/CaCO3: a strategy for improved phage therapy. Sci. Rep. 7:41441
    [Google Scholar]
  27. Colom J, Cano-Sarabia M, Otero J, Cortés P, Maspoch D, Llagostera M 2015. Liposome-encapsulated bacteriophages for enhanced oral phage therapy against Salmonella spp. Appl. Environ. Microbiol. 81:144841–49
    [Google Scholar]
  28. Danelishvili L, Young LS, Bermudez LE 2006. In vivo efficacy of phage therapy for Mycobacterium avium infection as delivered by a nonvirulent mycobacterium. Microb. Drug Resist. 12:11–6
    [Google Scholar]
  29. Das M, Bhowmick TS, Ahern SJ, Young R, Gonzalez CF 2015. Control of Pierce's disease by phage. PLOS ONE 10:6e0128902
    [Google Scholar]
  30. Deasy T, Mahony J, Neve H, Heller KJ, van Sinderen D 2011. Isolation of a virulent Lactobacillus brevis phage and its application in the control of beer spoilage. J. Food Prot. 74:122157–61
    [Google Scholar]
  31. de Melo AG, Levesque S, Moineau S 2018. Phages as friends and enemies in food processing. Curr. Opin. Biotechnol. 49:185–90
    [Google Scholar]
  32. Denyes JM, Dunne M, Steiner S, Mittelviefhaus M, Weiss A et al. 2017. Modified bacteriophage S16 long tail fiber proteins for rapid and specific immobilization and detection of Salmonella cells. Appl. Environ. Microbiol. 83:e00277–17
    [Google Scholar]
  33. Eur. Comm. (EC). 2011. Preparatory study on food waste across EU 27 Tech. Rep., BIO Intell. Serv. Paris:
    [Google Scholar]
  34. El-Shibiny A, Scott A, Timms A, Metawea Y, Connerton P, Connerton I 2009. Application of a group II Campylobacter bacteriophage to reduce strains of Campylobacter jejuni and Campylobacter coli colonizing broiler chickens. J. Food Prot. 72:4733–40
    [Google Scholar]
  35. Endersen L, Buttimer C, Nevin E, Coffey A, Neve H et al. 2017. Investigating the biocontrol and anti-biofilm potential of a three phage cocktail against Cronobacter sakazakii in different brands of infant formula. Int. J. Food Microbiol. 253:1–11
    [Google Scholar]
  36. Endersen L, O'Mahony J, Hill C, Ross RP, McAuliffe O, Coffey A 2014. Phage therapy in the food industry. Annu. Rev. Food Sci. Technol. 5:1327–49
    [Google Scholar]
  37. Fan J, Zeng Z, Mai K, Yang Y, Feng J et al. 2016. Preliminary treatment of bovine mastitis caused by Staphylococcus aureus, with trx-SA1, recombinant endolysin of S. aureus bacteriophage IME-SA1. Vet. Microbiol. 191:65–71
    [Google Scholar]
  38. Fischer S, Kittler S, Klein G, Glünder G 2013. Impact of a single phage and a phage cocktail application in broilers on reduction of Campylobacter jejuni and development of resistance. PLOS ONE 8:10e78543
    [Google Scholar]
  39. Food Drug Admin. (FDA). 2003. Quantitative assessment of the relative risk to public health from foodborne Listeria monocytogenes among selected categories of ready-to-eat foods Rep., U.S. Dep. Agric. Washington, DC:
    [Google Scholar]
  40. Foster DM, Smith GW 2009. Pathophysiology of diarrhea in calves. Vet. Clin. North Am. Food Anim. Pract. 25:113–36
    [Google Scholar]
  41. Fraise AP 2002. Biocide abuse and antimicrobial resistance: a cause for concern?. J. Antimicrob. Chemother. 49:111–12
    [Google Scholar]
  42. García P, Madera C, Martínez B, Rodríguez A 2007. Biocontrol of Staphylococcus aureus in curd manufacturing processes using bacteriophages. Int. Dairy J. 17:101232–39
    [Google Scholar]
  43. García P, Madera C, Martínez B, Rodríguez A, Evaristo Suárez J 2009. Prevalence of bacteriophages infecting Staphylococcus aureus in dairy samples and their potential as biocontrol agents. J. Dairy Sci. 92:73019–26
    [Google Scholar]
  44. García P, Martínez B, Rodríguez L, Rodríguez A 2010. Synergy between the phage endolysin LysH5 and nisin to kill Staphylococcus aureus in pasteurized milk. Int. J. Food Microbiol. 141:3151–55
    [Google Scholar]
  45. Garneau JE, Moineau S 2011. Bacteriophages of lactic acid bacteria and their impact on milk fermentations. Microb. Cell Fact. 10:Suppl. 1S20
    [Google Scholar]
  46. Gerstmans H, Rodriguez-Rubio L, Lavigne R, Briers Y 2016. From endolysins to Artilysin®s: novel enzyme-based approaches to kill drug-resistant bacteria. Biochem. Soc. Trans. 44:1123–28
    [Google Scholar]
  47. Gervasi T, Lo Curto R, Minniti E, Narbad A, Mayer MJ 2014. Application of Lactobacillus johnsonii expressing phage endolysin for control of Clostridium perfringens. Lett. Appl. Microbiol 59:4355–61
    [Google Scholar]
  48. Gómez-Torres N, Dunne M, Garde S, Meijers R, Narbad A et al. 2018. Development of a specific fluorescent phage endolysin for in situ detection of Clostridium species associated with cheese spoilage. Microb. Biotechnol. 11:2332–45
    [Google Scholar]
  49. Goode D, Allen VM, Barrow PA 2003. Reduction of experimental Salmonella and Campylobacter contamination of chicken skin by application of lytic bacteriophages. Appl. Environ. Microbiol. 69:85032–36
    [Google Scholar]
  50. Gouvêa DM, Mendonça RCS, Soto ML, Cruz RS 2015. Acetate cellulose film with bacteriophages for potential antimicrobial use in food packaging. LWT Food Sci. Technol. 63:185–91
    [Google Scholar]
  51. Greer GG, Dilts BD 2002. Control of Brochothrix thermosphacta spoilage of pork adipose tissue using bacteriophages. J. Food Prot. 65:5861–63
    [Google Scholar]
  52. Guabiraba R, Schouler C 2015. Avian colibacillosis: still many black holes. FEMS Microbiol. Lett. 362:15fnv118
    [Google Scholar]
  53. Gutiérrez D, Rodríguez-Rubio L, Fernández L, Martínez B, Rodríguez A, García P 2017. Applicability of commercial phage-based products against Listeria monocytogenes for improvement of food safety in Spanish dry-cured ham and food contact surfaces. Food Control 73:1474–82
    [Google Scholar]
  54. Gutiérrez D, Ruas-Madiedo P, Martínez B, Rodríguez A, García P 2014. Effective removal of staphylococcal biofilms by the endolysin LysH5. PLOS ONE 9:9e107307
    [Google Scholar]
  55. Hammerl JA, Jäckel C, Alter T, Janzcyk P, Stingl K et al. 2014. Reduction of Campylobacter jejuni in broiler chicken by successive application of group II and group III phages. PLOS ONE 9:12e114785
    [Google Scholar]
  56. Han J-H, Han S-J, Oh Y, Young Lee C 2016. Efficacy of dietary supplementation of bacteriophages in treatment of concurrent infections with enterotoxigenic Escherichia coli K88 and K99 in postweaning pigs. J Swine Heal. Prod. 24:5259–63
    [Google Scholar]
  57. Harper D, Parracho H, Walker J, Sharp R, Hughes G et al. 2014. Bacteriophages and biofilms. Antibiotics 3:4270–84
    [Google Scholar]
  58. Hartard C, Leclerc M, Rivet R, Maul A, Loutreul J et al. 2018. F-specific RNA bacteriophages, especially members of subgroup II, should be reconsidered as good indicators of viral pollution of oysters. Appl. Environ. Microbiol. 84:1e01866–17
    [Google Scholar]
  59. Hendrix RW 2003. Bacteriophage genomics. Curr. Opin. Microbiol. 6:5506–11
    [Google Scholar]
  60. Hernández I 2017. Bacteriophages against Serratia as fish spoilage control technology. Front. Microbiol. 8:449
    [Google Scholar]
  61. Hostetter J, Steadham E, Haynes J, Bailey T, Cheville N 2003. Phagosomal maturation and intracellular survival of Mycobacterium avium subspecies paratuberculosis in J774 cells. Comp. Immunol. Microbiol. Infect. Dis. 26:4269–83
    [Google Scholar]
  62. Hsu FC, Shieh YS, Sobsey MD 2002. Enteric bacteriophages as potential fecal indicators in ground beef and poultry meat. J. Food Prot. 65:193–99
    [Google Scholar]
  63. Hu Z, Meng X-C, Liu F 2016. Isolation and characterisation of lytic bacteriophages against Pseudomonas spp., a novel biological intervention for preventing spoilage of raw milk. Int. Dairy J. 55:72–78
    [Google Scholar]
  64. Huff WE, Huff GR, Rath NC, Balog JM, Donoghue AM 2003. Evaluation of aerosol spray and intramuscular injection of bacteriophage to treat an Escherichia coli respiratory infection. Poult. Sci. 82:71108–12
    [Google Scholar]
  65. Huff WE, Huff GR, Rath NC, Balog JM, Xie H et al. 2002. Prevention of Escherichia coli respiratory infection in broiler chickens with bacteriophage (SPR02). Poult. Sci. 81:4437–41
    [Google Scholar]
  66. Hughes JM, Wilson ME, Johnson KE, Thorpe CM, Sears CL 2006. The emerging clinical importance of non-O157 Shiga toxin–producing Escherichia coli. Clin. Infect. Dis 43:121587–95
    [Google Scholar]
  67. Ibarra-Sánchez LA, Van Tassell ML, Miller MJ 2018. Antimicrobial behavior of phage endolysin PlyP100 and its synergy with nisin to control Listeria monocytogenes in queso fresco. Food Microbiol 72:128–34
    [Google Scholar]
  68. Iversen C, Forsythe S 2003. Risk profile of Enterobacter sakazakii, an emergent pathogen associated with infant milk formula. Trends Food Sci. Technol. 14:11443–54
    [Google Scholar]
  69. Jackson BR, Griffin PM, Cole D, Walsh KA, Chai SJ 2013. Outbreak-associated Salmonella enterica serotypes and food commodities, United States, 1998–2008. Emerg. Infect. Dis. 19:81239–44
    [Google Scholar]
  70. Jones JB, Vallad GE, Iriarte FB, Obradović A, Wernsing MH et al. 2012. Considerations for using bacteriophages for plant disease control. Bacteriophage 2:4e23857
    [Google Scholar]
  71. Jun JW, Park SC, Wicklund A, Skurnik M 2018. Bacteriophages reduce Yersinia enterocolitica contamination of food and kitchenware. Int. J. Food Microbiol. 271:33–47
    [Google Scholar]
  72. Kaclíková E, Kuchta TV, Kay H, Gray D 2001. Separation of Listeria from cheese and enrichment media using antibody-coated microbeads and centrifugation. J. Microbiol. Methods. 46:163–67
    [Google Scholar]
  73. Kadariya J, Smith TC, Thapaliya D 2014. Staphylococcus aureus and staphylococcal food-borne disease: an ongoing challenge in public health. BioMed Res. Int. 2014:827965
    [Google Scholar]
  74. Kannan P, Yong HY, Reiman L, Cleaver C, Patel P, Bhagwat AA 2010. Bacteriophage-based rapid and sensitive detection of Escherichia coli O157:H7 isolates from ground beef. Foodborne Pathog. Dis. 7:121551–58
    [Google Scholar]
  75. Kenzaka T, Tani K, Sakotani A, Yamaguchi N, Nasu M 2007. High-frequency phage-mediated gene transfer among Escherichia coli cells, determined at the single-cell level. Appl. Environ. Microbiol. 73:103291–99
    [Google Scholar]
  76. Kerry JP, O'Grady MN, Hogan SA 2006. Past, current and potential utilisation of active and intelligent packaging systems for meat and muscle-based products: a review. Meat Sci 74:1113–30
    [Google Scholar]
  77. Kim KH, Ingale SL, Kim JS, Lee SH, Lee JH et al. 2014. Bacteriophage and probiotics both enhance the performance of growing pigs but bacteriophage are more effective. Anim. Feed Sci. Technol. 196:88–95
    [Google Scholar]
  78. Kong M, Ryu S 2015. Bacteriophage PBC1 and its endolysin as an antimicrobial agent against Bacillus cereus. Appl. Environ. Microbiol 81:72274–83
    [Google Scholar]
  79. Krüger A, Lucchesi PMA 2015. Shiga toxins and stx phages: highly diverse entities. Microbiology 161:3451–62
    [Google Scholar]
  80. Kuchment A 2012. The Fading of Phage Therapy. The Forgotten Cure: The Past and Future of Phage Therapy35–42 New York: Springer
    [Google Scholar]
  81. Laanto E, Bamford JKH, Ravantti JJ, Sundberg L-R 2015. The use of phage FCL-2 as an alternative to chemotherapy against columnaris disease in aquaculture. Front. Microbiol. 6:829
    [Google Scholar]
  82. Labrie SJ, Samson JE, Moineau S 2010. Bacteriophage resistance mechanisms. Nat. Rev. Microbiol. 8:5317–27
    [Google Scholar]
  83. Ladero V, Gómez-Sordo C, Sánchez-Llana E, Del Rio B, Redruello B et al. 2016. Q69 (an E. faecalis–infecting bacteriophage) as a biocontrol agent for reducing tyramine in dairy products. Front. Microbiol. 7:445
    [Google Scholar]
  84. Larpin Y, Oechslin F, Moreillon P, Resch G, Entenza JM, Mancini S 2018. In vitro characterization of PlyE146, a novel phage lysin that targets Gram-negative bacteria. PLOS ONE 13:2e0192507
    [Google Scholar]
  85. Lee S, Hosseindoust A, Goel A, Choi Y, Kwon IK, Chae B 2016. Effects of dietary supplementation of bacteriophage with or without zinc oxide on the performance and gut development of weanling pigs. Italian J. Anim. Sci. 15:3412–18
    [Google Scholar]
  86. Lehman SM 2007. Development of a bacteriophage-based biopesticide for fire blight PhD Thesis Brock Univ. St. Catharines, Ont.:
    [Google Scholar]
  87. Liana AE, Marquis CP, Gunawan C, Gooding JJ, Amal R 2018. Antimicrobial activity of T4 bacteriophage conjugated indium tin oxide surfaces. J. Colloid Interface Sci. 514:227–33
    [Google Scholar]
  88. Loc Carrillo C, 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. 71:116554–63
    [Google Scholar]
  89. Loeffler JM, Djurkovic S, Fischetti VA 2003. Phage lytic enzyme Cpl-1 as a novel antimicrobial for pneumococcal bacteremia. Infect. Immun. 71:116199–204
    [Google Scholar]
  90. Loessner MJ, Rudolf M, Scherer S 1997. Evaluation of luciferase reporter bacteriophage A511::luxAB for detection of Listeria monocytogenes in contaminated foods. Appl. Environ. Microbiol. 63:82961–65
    [Google Scholar]
  91. Madonna AJ, Van Cuyk S, Voorhees KJ 2003. Detection of Escherichia coli using immunomagnetic separation and bacteriophage amplification coupled with matrix-assisted laser desorption/ionization time-of-flight mass spectrometry. Rapid Commun. Mass Spectrom. 17:3257–63
    [Google Scholar]
  92. Mallmann WL, Hemstreet C 1924. Isolation of an inhibitory substance from plants. J. Agric. Res. 28:6599–602
    [Google Scholar]
  93. Matsuoka S, Hashizume T, Kanzaki H, Iwamoto E, Se Chang P et al. 2007. Phage therapy against β-hemolytic streptococcicosis of Japanese flounder Paralichthys olivaceus. Fish Pathol 42:4181–89
    [Google Scholar]
  94. Meyer A, Greene M, Kimmelshue C, Cademartiri R 2017. Stabilization of T4 bacteriophage at acidic and basic pH by adsorption on paper. Colloids Surfaces B 160:169–76
    [Google Scholar]
  95. Miller RW, Skinner J, Sulakvelidze A, Mathis GF, Hofacre CL 2010. Bacteriophage therapy for control of necrotic enteritis of broiler chickens experimentally infected with Clostridium perfringens. Avian Dis 54:133–40
    [Google Scholar]
  96. Misiou O, van Nassau TJ, Lenz CA, Vogel RF 2018. The preservation of Listeria-critical foods by a combination of endolysin and high hydrostatic pressure. Int. J. Food Microbiol. 266:355–62
    [Google Scholar]
  97. Muldoon MT, Teaney G, Li J, Onisk DV, Stave JW 2007. Bacteriophage-based enrichment coupled to immunochromatographic strip-based detection for the determination of Salmonella in meat and poultry. J. Food Prot. 70:102235–42
    [Google Scholar]
  98. Muytjens HL, Roelofs-Willemse H, Jaspar GH 1988. Quality of powdered substitutes for breast milk with regard to members of the family Enterobacteriaceae. J. Clin. Microbiol. 26:4743–46
    [Google Scholar]
  99. Nakai T, Sugimoto R, Park K, Matsuoka S, Mori K et al. 1999. Protective effects of bacteriophage on experimental Lactococcus garvieae infection in yellowtail. Dis. Aquat. Org. 37:133–41
    [Google Scholar]
  100. Nanda AM, Thormann K, Frunzke J 2015. Impact of spontaneous prophage induction on the fitness of bacterial populations and host-microbe interactions. J. Bacteriol. 197:3410–19
    [Google Scholar]
  101. Nieth A, Verseux C, Barnert S, Süss R, Römer W 2015. A first step toward liposome-mediated intracellular bacteriophage therapy. Expert Opin. Drug Deliv. 12:91411–24
    [Google Scholar]
  102. Obeso JM, Martínez B, Rodríguez A, García P 2008. Lytic activity of the recombinant staphylococcal bacteriophage ΦH5 endolysin active against Staphylococcus aureus in milk. Int. J. Food Microbiol. 128:2212–18
    [Google Scholar]
  103. Obrig TG 2010. Escherichia coli Shiga toxin mechanisms of action in renal disease. Toxins 2:122769–94
    [Google Scholar]
  104. O'Flaherty S, Coffey A, Meaney WJ, Fitzgerald GF, Ross RP 2005. Inhibition of bacteriophage K proliferation on Staphylococcus aureus in raw bovine milk. Lett. Appl. Microbiol. 41:3274–79
    [Google Scholar]
  105. Oliveira H, Melo LDR, Santos SB, Nóbrega FL, Ferreira EC et al. 2013. Molecular aspects and comparative genomics of bacteriophage endolysins. J. Virol. 87:84558–70
    [Google Scholar]
  106. O'Sullivan D, Ross RP, Fitzgerald GF, Coffey A 2000. Investigation of the relationship between lysogeny and lysis of Lactococcus lactis in cheese using prophage-targeted PCR. Appl. Environ. Microbiol. 66:52192–98
    [Google Scholar]
  107. Park M-K, Weerakoon KA, Oh J-H, Chin BA 2013. The analytical comparison of phage-based magneto-elastic biosensor with TaqMan-based quantitative PCR method to detect Salmonella Typhimurium on cantaloupes. Food Control 33:2330–36
    [Google Scholar]
  108. Petsong K, Vongkamjan K 2015. Applications of Salmonella bacteriophages in the food production chain. The Battle Against Microbial Pathogens: Basic Science, Technological Advances and Educational Programs 1 A. Méndez-Vilas 275–83 Badajoz, Spain: Formatex Res. Cent.
    [Google Scholar]
  109. Pirnay J-P, Merabishvili M, Van Raemdonck H, De Vos D, Verbeken G 2018. Bacteriophage production in compliance with regulatory requirements. Methods in Molecular Biology JM Walker 233–52 New York: Humana Press
    [Google Scholar]
  110. Prajapati A, Ramchandran D, Verma H, Abbas M, Rawat M 2014. Therapeutic efficacy of Brucella phage against Brucella abortus in mice model. Vet. World 7:34–37
    [Google Scholar]
  111. Radford D, Guild B, Strange P, Ahmed R, Lim L-T, Balamurugan S 2017. Characterization of antimicrobial properties of Salmonella phage Felix O1 and Listeria phage A511 embedded in xanthan coatings on poly(lactic acid) films. Food Microbiol 66:117–28
    [Google Scholar]
  112. 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. 76:217210–16
    [Google Scholar]
  113. Sabouri S, Sepehrizadeh Z, Amirpour-Rostami S, Skurnik M 2017. A minireview on the in vitro and in vivo experiments with anti–Escherichia coli O157:H7 phages as potential biocontrol and phage therapy agents. Int. J. Food Microbiol. 243:52–57
    [Google Scholar]
  114. Sanders ME, Leonhard PJ, Sing WD, Klaenhammer TR 1986. Conjugal strategy for construction of fast acid-producing, bacteriophage-resistant lactic streptococci for use in dairy fermentations. Appl. Environ. Microbiol. 52:51001–7
    [Google Scholar]
  115. Schmelcher M, Powell AM, Becker SC, Camp MJ, Donovan DM 2012. Chimeric phage lysins act synergistically with lysostaphin to kill mastitis-causing Staphylococcus aureus in murine mammary glands. Appl. Environ. Microbiol. 78:72297–305
    [Google Scholar]
  116. Schmelcher M, Powell AM, Camp MJ, Pohl CS, Donovan DM 2015. Synergistic streptococcal phage λSA2 and B30 endolysins kill streptococci in cow milk and in a mouse model of mastitis. Appl. Microbiol. Biotechnol. 99:208475–86
    [Google Scholar]
  117. Schmelcher M, Shabarova T, Eugster MR, Eichenseher F, Tchang VS et al. 2010. Rapid multiplex detection and differentiation of Listeria cells by use of fluorescent phage endolysin cell wall binding domains. Appl. Environ. Microbiol. 76:175745–56
    [Google Scholar]
  118. Schmieger H, Schicklmaier P 1999. Transduction of multiple drug resistance of Salmonella enterica serovar typhimurium DT104. FEMS Microbiol. Lett. 170:1251–56
    [Google Scholar]
  119. Smith HW, Huggins MB 1983. Effectiveness of phages in treating experimental Escherichia coli diarrhoea in calves, piglets and lambs. J. Gen. Microbiol. 129:2659–75
    [Google Scholar]
  120. Soffer N, Woolston J, Li M, Das C, Sulakvelidze A 2017. Bacteriophage preparation lytic for Shigella significantly reduces Shigella sonnei contamination in various foods. PLOS ONE 12:3e0175256
    [Google Scholar]
  121. Stambach NR, Carr SA, Cox CR, Voorhees KJ 2015. Rapid detection of Listeria by bacteriophage amplification and SERS-lateral flow immunochromatography. Viruses 7:126631–41
    [Google Scholar]
  122. Swift SM, Seal BS, Garrish JK, Oakley BB, Hiett K et al. 2015. A thermophilic phage endolysin fusion to a Clostridium perfringens–specific cell wall binding domain creates an anti-Clostridium antimicrobial with improved thermostability. Viruses 7:63019–34
    [Google Scholar]
  123. Szermer-Olearnik B, Boratyński J 2015. Removal of endotoxins from bacteriophage preparations by extraction with organic solvents. PLOS ONE 10:3e0122672
    [Google Scholar]
  124. Tabla R, Martínez B, Rebollo JE, González J, Ramírez MR et al. 2012. Bacteriophage performance against Staphylococcus aureus in milk is improved by high hydrostatic pressure treatments. Int. J. Food Microbiol. 156:3209–13
    [Google Scholar]
  125. Tadeo JL 2008. Analysis of Pesticides in Food and Environmental Samples Boca Raton, FL: CRC Press
    [Google Scholar]
  126. Tay L-L, Huang P-J, Tanha J, Ryan S, Wu X et al. 2012. Silica encapsulated SERS nanoprobe conjugated to the bacteriophage tailspike protein for targeted detection of Salmonella. Chem. Commun 48:71024–26
    [Google Scholar]
  127. Thiele-Bruhn S 2003. Pharmaceutical antibiotic compounds in soils: a review. J. Plant Nutr. Soil Sci. 166:2145–67
    [Google Scholar]
  128. Tolba M, Ahmed MU, Tlili C, Eichenseher F, Loessner MJ, Zourob M 2012. A bacteriophage endolysin-based electrochemical impedance biosensor for the rapid detection of Listeria cells. Analyst 137:245749–56
    [Google Scholar]
  129. Verreault D, Gendron L, Rousseau GM, Veillette M, Massé D et al. 2011. Detection of airborne lactococcal bacteriophages in cheese manufacturing plants. Appl. Environ. Microbiol. 77:2491–97
    [Google Scholar]
  130. Vinay M, Franche N, Grégori G, Fantino J-R, Pouillot F, Ansaldi M 2015. Phage-based fluorescent biosensor prototypes to specifically detect enteric bacteria such as E. coli and Salmonella enterica Typhimurium. PLOS ONE 10:7e0131466
    [Google Scholar]
  131. Vinod MG, Shivu MM, Umesha KR, Rajeeva BC, Krohne G et al. 2006. Isolation of Vibrio harveyi bacteriophage with a potential for biocontrol of luminous vibriosis in hatchery environments. Aquaculture 255:1–4117–24
    [Google Scholar]
  132. Wagenaar JA, Van Bergen MAP, Mueller MA, Wassenaar TM, Carlton RM 2005. Phage therapy reduces Campylobacter jejuni colonization in broilers. Vet. Microbiol. 109:3–4275–83
    [Google Scholar]
  133. Wang Y, Barton M, Elliott L, Li X, Abraham S et al. 2017. Bacteriophage therapy for the control of Vibrio harveyi in greenlip abalone (Haliotis laevigata). Aquaculture 473:251–58
    [Google Scholar]
  134. Warren BR, Parish ME, Schneider KR 2006. Shigella as a foodborne pathogen and current methods for detection in food. Crit. Rev. Food Sci. Nutr. 46:7551–67
    [Google Scholar]
  135. Whitman W, Coleman D, Wiebe W 1998. Prokaryotes: the unseen majority. PNAS 95:126578–83
    [Google Scholar]
  136. Willford JD, Bisha B, Bolenbaugh KE, Goodridge LD 2011. Luminescence based enzyme-labeled phage (Phazyme) assays for rapid detection of Shiga toxin producing Escherichia coli serogroups. Bacteriophage 1:2101–10
    [Google Scholar]
  137. Wittmann J, Brancato C, Berendzen KW, Dreiseikelmann B 2015. Development of a tomato plant resistant to Clavibacter michiganensis using the endolysin gene of bacteriophage CMP1 as a transgene. Plant Pathol 65:3496–502
    [Google Scholar]
  138. World Health Org. (WHO). 2015. WHO estimates of the global burden of foodborne diseases Rep., WHO, Geneva Switz.:
    [Google Scholar]
  139. World Health Org. (WHO). 2017. WHO guidelines on use of medically important antimicrobials in food-producing animals Rep., WHO, Geneva Switz.:
    [Google Scholar]
  140. Yan J, Mao J, Xie J 2014. Bacteriophage polysaccharide depolymerases and biomedical applications. BioDrugs 28:3265–74
    [Google Scholar]
  141. Zhang D, Coronel-Aguilera CP, Romero PL, Perry L, Minocha U et al. 2016. The use of a novel NanoLuc-based reporter phage for the detection of Escherichia coli O157:H7. Sci. Rep. 6:133235
    [Google Scholar]
  142. Zhang H, Wang R, Bao H 2013. Phage inactivation of foodborne Shigella on ready-to-eat spiced chicken. Poult. Sci. 92:1211–17
    [Google Scholar]
  143. Zhang J, Li Z, Cao Z, Wang L, Li X et al. 2015. Bacteriophages as antimicrobial agents against major pathogens in swine: a review. J. Anim. Sci. Biotechnol. 6:139
    [Google Scholar]
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