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Chapter 29 : Bacteriophages for Biological Control of Foodborne Pathogens

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Abstract:

Novel trends in consumer demands and the global threat of antibiotic-resistant bacteria have generated the need for natural preservation techniques to reduce the use of preservatives in food production and to provide alternatives to aid safe food production. Bacteriophages, the natural killers of bacteria, provide alternative biological solutions for control of foodborne pathogens covering the entire food chain. Bacteriophages are obligate parasites that are specific to bacteria, thus being harmless to humans, animals, and plants. Phages are highly specific and leave the remaining microbiota untouched, another property that favors phages over conventional methods that may affect the beneficial microbiota of the food. Furthermore, phages have low inherent toxicity and are already present in foods as well as the human and animal gut. Finally, phages can be used along the entire food chain, including phage therapy for reduction of pathogen colonization of animals in primary production and phage biocontrol during food production. In this chapter, we explain the principles and mechanisms behind the use of phages for biological control of foodborne pathogens, as well as the rationale and outcome of using phages for therapy and biocontrol, including the challenges and limitations of such applications. In terms of future prospects, we discuss the technical and regulatory challenges of widespread industrial use of phages for biological control of foodborne pathogens.

Citation: Gencay Y, Brøndsted L. 2019. Bacteriophages for Biological Control of Foodborne Pathogens, p 755-786. In Doyle M, Diez-Gonzalez F, Hill C (ed), Food Microbiology: Fundamentals and Frontiers, 5th Edition. ASM Press, Washington, DC. doi: 10.1128/9781555819972.ch29
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Figure 29.1

Life cycles of phages.

Citation: Gencay Y, Brøndsted L. 2019. Bacteriophages for Biological Control of Foodborne Pathogens, p 755-786. In Doyle M, Diez-Gonzalez F, Hill C (ed), Food Microbiology: Fundamentals and Frontiers, 5th Edition. ASM Press, Washington, DC. doi: 10.1128/9781555819972.ch29
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Image of Figure 29.2
Figure 29.2

Plaque morphologies. (Left) Dilution of a wastewater sample that harbors phages showing different plaque morphologies. (Right) Ten-fold dilutions of purified phage stocks showing consistent plaque morphologies (right).

Citation: Gencay Y, Brøndsted L. 2019. Bacteriophages for Biological Control of Foodborne Pathogens, p 755-786. In Doyle M, Diez-Gonzalez F, Hill C (ed), Food Microbiology: Fundamentals and Frontiers, 5th Edition. ASM Press, Washington, DC. doi: 10.1128/9781555819972.ch29
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References

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1. Breitbart M, Hewson I, Felts B, Mahaffy JM, Nulton J, Salamon P, Rohwer F . 2003. Metagenomic analyses of an uncultured viral community from human feces. J Bacteriol 185 : 6220 6223.[CrossRef][PubMed]
2. Hsu FC, Shieh YSC, Sobsey MD . 2002. Enteric bacteriophages as potential fecal indicators in ground beef and poultry meat. J Food Prot 65 : 93 99.[CrossRef][PubMed]
3. Kennedy JE Jr, Wei CI, Oblinger JL . 1986. Distribution of coliphages in various foods. J Food Prot 49 : 944 951.[CrossRef].
4. Suárez VB, Quiberoni A, Binetti AG, Reinheimer JA . 2002. Thermophilic lactic acid bacteria phages isolated from Argentinian dairy industries. J Food Prot 65 : 1597 1604.[CrossRef][PubMed]
5. Croci L, De Medici D, Scalfaro C, Fiore A, Divizia M, Donia D, Cosentino AM, Moretti P, Costantini G . 2000. Determination of enteroviruses, hepatitis A virus, bacteriophages and Escherichia coli in Adriatic Sea mussels. J Appl Microbiol 88 : 293 298.[CrossRef][PubMed]
6. D'Herelle F Publications Service . 2007. On an invisible microbe antagonistic toward dysenteric bacilli: brief note by Mr. F. D'Herelle, presented by Mr. Roux. 1917. Res Microbiol 158 : 553 554.[CrossRef][PubMed]
7. Brüssow H, Hendrix RW . 2002. Phage genomics: small is beautiful. Cell 108 : 13 16.[CrossRef][PubMed]
8. Lavigne R, Seto D, Mahadevan P, Ackermann HW, Kropinski AM . 2008. Unifying classical and molecular taxonomic classification: analysis of the Podoviridae using BLASTP-based tools. Res Microbiol 159 : 406 414.[CrossRef][PubMed]
9. Lavigne R, Darius P, Summer EJ, Seto D, Mahadevan P, Nilsson AS, Ackermann HW, Kropinski AM . 2009. Classification of Myoviridae bacteriophages using protein sequence similarity. BMC Microbiol 9 : 224.[CrossRef][PubMed]
10. Kutter EM, d'Acci K, Drivdahl RH, Gleckler J, McKinney JC, Peterson S, Guttman BS . 1994. Identification of bacteriophage T4 prereplicative proteins on two-dimensional polyacrylamide gels. J Bacteriol 176 : 1647 1654.[CrossRef][PubMed]
11. Ceyssens PJ, Minakhin L, Van den Bossche A, Yakunina M, Klimuk E, Blasdel B, De Smet J, Noben JP, Bläsi U, Severinov K, Lavigne R . 2014. Development of giant bacteriophage φKZ is independent of the host transcription apparatus. J Virol 88 : 10501 10510.[CrossRef][PubMed]
12. Chevallereau A, Blasdel BG, De Smet J, Monot M, Zimmermann M, Kogadeeva M, Sauer U, Jorth P, Whiteley M, Debarbieux L, Lavigne R . 2016. Next-generation “-omics” approaches reveal a massive alteration of host RNA metabolism during bacteriophage infection of Pseudomonas aeruginosa. PLoS Genet 12 : e1006134.[CrossRef][PubMed]
13. De Smet J, Hendrix H, Blasdel BG, Danis-Wlodarczyk K, Lavigne R . 2017. Pseudomonas predators: understanding and exploiting phage-host interactions. Nat Rev Microbiol 15 : 517 530.[CrossRef][PubMed]
14. Keen EC, Bliskovsky VV, Malagon F, Baker JD, Prince JS, Klaus JS, Adhya SL . 2017. Novel “superspreader” bacteriophages promote horizontal gene transfer by transformation. mBio 8 :e02115-16.[CrossRef][PubMed]
15. Matilla MA, Fang X, Salmond GPC . 2014. Viunalikeviruses are environmentally common agents of horizontal gene transfer in pathogens and biocontrol bacteria. ISME J 8 : 2143 2147.[CrossRef][PubMed]
16. Bertozzi Silva J, Storms Z, Sauvageau D . 2016. Host receptors for bacteriophage adsorption. FEMS Microbiol Lett 363 : fnw002.[CrossRef][PubMed]
17. Letarov AV, Kulikov EE . 2017. Adsorption of bacteriophages on bacterial cells. Biochemistry (Mosc) 82 : 1632 1658.[CrossRef][PubMed]
18. Chaturongakul S, Ounjai P . 2014. Phage-host interplay: examples from tailed phages and Gram-negative bacterial pathogens. Front Microbiol 5 : 442.[CrossRef][PubMed]
19. Wendlinger G, Loessner MJ, Scherer S . 1996. Bacteriophage receptors on Listeria monocytogenes cells are the N-acetylglucosamine and rhamnose substituents of teichoic acids or the peptidoglycan itself. Microbiology 142 : 985 992.[CrossRef][PubMed]
20. Trojet SN, Caumont-Sarcos A, Perrody E, Comeau AM, Krisch HM . 2011. The gp38 adhesins of the T4 superfamily: a complex modular determinant of the phage's host specificity. Genome Biol Evol 3 : 674 686.[CrossRef][PubMed]
21. Sandmeler H . 1994. Acquisition and rearrangement of sequence motifs in the evolution of bacteriophage tail fibres. Mol Microbiol 12 : 343 350.[CrossRef][PubMed]
22. Drexler K, Dannull J, Hindennach I, Mutschler B, Henning U . 1991. Single mutations in a gene for a tail fiber component of an Escherichia coli phage can cause an extension from a protein to a carbohydrate as a receptor. J Mol Biol 219 : 655 663.[CrossRef][PubMed]
23. Hyman P, Abedon ST, . 2010. Bacteriophage host range and bacterial resistance, p 217 248. In Laskin AI, Sariaslani S, Gadd GM (ed), Advances in Applied Microbiology. Academic Press, San Diego, CA.
24. Roux S, Hallam SJ, Woyke T, Sullivan MB . 2015. Viral dark matter and virus-host interactions resolved from publicly available microbial genomes. eLife 4 :e08490.[CrossRef][PubMed]
25. Villarroel J, Kleinheinz KA, Jurtz VI, Zschach H, Lund O, Nielsen M, Larsen MV . 2016. HostPhinder: a phage host prediction tool. Viruses 8 : 116.[CrossRef][PubMed]
26. Sørensen MCH, van Alphen LB, Harboe A, Li J, Christensen BB, Szymanski CM, Brøndsted L . 2011. Bacteriophage F336 recognizes the capsular phosphoramidate modification of Campylobacter jejuni NCTC11168. J Bacteriol 193 : 6742 6749.[CrossRef][PubMed]
27. Holst Sørensen MC, van Alphen LB, Fodor C, Crowley SM, Christensen BB, Szymanski CM, Brøndsted L . 2012. Phase variable expression of capsular polysaccharide modifications allows Campylobacter jejuni to avoid bacteriophage infection in chickens. Front Cell Infect Microbiol 2 : 11.[PubMed]
28. Aidley J, Sørensen MCH, Bayliss CD, Brøndsted L . 2017. Phage exposure causes dynamic shifts in the expression states of specific phase-variable genes of Campylobacter jejuni. Microbiology 163 : 911 919.[CrossRef][PubMed]
29. Gencay YE, Sørensen MCH, Wenzel CQ, Szymanski CM, Brøndsted L . 2018. Phase variable expression of a single phage receptor in Campylobacter jejuni NCTC12662 influences sensitivity toward several diverse CPS-dependent phages. Front Microbiol 9 : 82.[CrossRef][PubMed]
30. Cota I, Sánchez-Romero MA, Hernández SB, Pucciarelli MG, García-Del Portillo F, Casadesús J . 2015. Epigenetic control of Salmonella enterica O-antigen chain length: A tradeoff between virulence and bacteriophage resistance. PLoS Genet 11 : e1005667.[CrossRef][PubMed]
31. Samson JE, Magadán AH, Sabri M, Moineau S . 2013. Revenge of the phages: defeating bacterial defences. Nat Rev Microbiol 11 : 675 687.[CrossRef][PubMed]
32. Baba T, Ara T, Hasegawa M, Takai Y, Okumura Y, Baba M, Datsenko KA, Tomita M, Wanner BL, Mori H . 2006. Construction of Escherichia coli K-12 in-frame, single-gene knockout mutants: the Keio collection. Mol Syst Biol 2 : 2006.0008.[CrossRef][PubMed]
33. Labrie SJ, Samson JE, Moineau S . 2010. Bacteriophage resistance mechanisms. Nat Rev Microbiol 8 : 317 327.[CrossRef][PubMed]
34. Barrangou R, Fremaux C, Deveau H, Richards M, Boyaval P, Moineau S, Romero DA, Horvath P . 2007. CRISPR provides acquired resistance against viruses in prokaryotes. Science 315 : 1709 1712.[CrossRef][PubMed]
35. Makarova KS, Wolf YI, Alkhnbashi OS, Costa F, Shah SA, Saunders SJ, Barrangou R, Brouns SJJ, Charpentier E, Haft DH, Horvath P, Moineau S, Mojica FJM, Terns RM, Terns MP, White MF, Yakunin AF, Garrett RA, van der Oost J, Backofen R, Koonin EV . 2015. An updated evolutionary classification of CRISPR-Cas systems. Nat Rev Microbiol 13 : 722 736.[CrossRef][PubMed]
36. Bondy-Denomy J, Pawluk A, Maxwell KL, Davidson AR . 2013. Bacteriophage genes that inactivate the CRISPR/Cas bacterial immune system. Nature 493 : 429 432.[CrossRef][PubMed]
37. Makarova KS, Wolf YI, Snir S, Koonin EV . 2011. Defense islands in bacterial and archaeal genomes and prediction of novel defense systems. J Bacteriol 193 : 6039 6056.[CrossRef][PubMed]
38. Goldfarb T, Sberro H, Weinstock E, Cohen O, Doron S, Charpak-Amikam Y, Afik S, Ofir G, Sorek R . 2015. BREX is a novel phage resistance system widespread in microbial genomes. EMBO J 34 : 169 183.[CrossRef][PubMed]
39. Ofir G, Melamed S, Sberro H, Mukamel Z, Silverman S, Yaakov G, Doron S, Sorek R . 2018. DISARM is a widespread bacterial defence system with broad anti-phage activities. Nat Microbiol 3 : 90 98.[CrossRef][PubMed]
40. Doron S, Melamed S, Ofir G, Leavitt A, Lopatina A, Keren M, Amitai G, Sorek R . 2018. Systematic discovery of antiphage defense systems in the microbial pangenome. Science 359 :eaar4120.[CrossRef][PubMed]
41. Hagens S, Loessner MJ . 2010. Bacteriophage for biocontrol of foodborne pathogens: calculations and considerations. Curr Pharm Biotechnol 11 : 58 68.[CrossRef][PubMed]
42. Abedon ST . 2011. Lysis from without. Bacteriophage 1 : 46 49.[CrossRef][PubMed]
43. 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 : 301 312.[CrossRef][PubMed]
44. Chibani-Chennoufi S, Sidoti J, Bruttin A, Kutter E, Sarker S, Brüssow H . 2004. In vitro and in vivo bacteriolytic activities of Escherichia coli phages: implications for phage therapy. Antimicrob Agents Chemother 48 : 2558 2569.[CrossRef][PubMed]
45. Bruttin A, Brüssow H . 2005. Human volunteers receiving Escherichia coli phage T4 orally: a safety test of phage therapy. Antimicrob Agents Chemother 49 : 2874 2878.[CrossRef][PubMed]
46. Marti R, Zurfluh K, Hagens S, Pianezzi J, Klumpp J, Loessner MJ . 2013. Long tail fibres of the novel broad-host-range T-even bacteriophage S16 specifically recognize Salmonella OmpC. Mol Microbiol 87 : 818 834.[CrossRef][PubMed]
47. Flores CO, Meyer JR, Valverde S, Farr L, Weitz JS . 2011. Statistical structure of host-phage interactions. Proc Natl Acad Sci USA 108 : E288 E297.[CrossRef][PubMed]
48. Örmälä A-M, Jalasvuori M . 2013. Phage therapy: should bacterial resistance to phages be a concern, even in the long run? Bacteriophage 3 : e24219.[CrossRef][PubMed]
49. Havelaar AH, Mangen M-JJ, de Koeijer AA, Bogaardt M-J, Evers EG, Jacobs-Reitsma WF, van Pelt W, Wagenaar JA, de Wit GA, van der Zee H, Nauta MJ . 2007. Effectiveness and efficiency of controlling Campylobacter on broiler chicken meat. Risk Anal 27 : 831 844.[CrossRef][PubMed]
50. Barrow PA . 2001. The use of bacteriophages for treatment and prevention of bacterial disease in animals and animal models of human infection. J Chem Technol Biotechnol 76 : 677 682.[CrossRef].
51. Johnson RP, Gyles CL, Huff WE, Ojha S, Huff GR, Rath NC, Donoghue AM . 2008. Bacteriophages for prophylaxis and therapy in cattle, poultry and pigs. Anim Health Res Rev 9 : 201 215.[CrossRef][PubMed]
52. Wernicki A, Nowaczek A, Urban-Chmiel R . 2017. Bacteriophage therapy to combat bacterial infections in poultry. Virol J 14 : 179.[CrossRef][PubMed]
53. Nakai T, Sugimoto R, Park KH, Matsuoka S, Mori K, Nishioka T, Maruyama K . 1999. Protective effects of bacteriophage on experimental Lactococcus garvieae infection in yellowtail. Dis Aquat Organ 37 : 33 41.[CrossRef][PubMed]
54. Park SC, Nakai T . 2003. Bacteriophage control of Pseudomonas plecoglossicida infection in ayu Plecoglossus altivelis. Dis Aquat Organ 53 : 33 39.[CrossRef][PubMed]
55. Vinod MG, Shivu MM, Umesha KR, Rajeeva BC, Krohne G, Karunasagar I, Karunasagar I . 2006. Isolation of Vibrio harveyi bacteriophage with a potential for biocontrol of luminous vibriosis in hatchery environments. Aquaculture 255 : 117 124.[CrossRef].
56. Richards GP . 2014. Bacteriophage remediation of bacterial pathogens in aquaculture: a review of the technology. Bacteriophage 4 : e975540.[CrossRef][PubMed]
57. Pal S . 2015. Phage therapy an alternate disease control in aquaculture: a review on recent advancements. IOSR J Agric Vet Sci Ver I 8 : 2319 2372.
58. Rohde C, Resch G, Pirnay JP, Blasdel BG, Debarbieux L, Gelman D, Górski A, Hazan R, Huys I, Kakabadze E, Łobocka M, Maestri A, Almeida GMF, Makalatia K, Malik DJ, Mašlaňová I, Merabishvili M, Pantucek R, Rose T, Štveráková D, Van Raemdonck H, Verbeken G, Chanishvili N . 2018. Expert opinion on three phage therapy related topics: bacterial phage resistance, phage training and prophages in bacterial production strains. Viruses 10 : 178.[CrossRef][PubMed]
59. Loc Carrillo C, Atterbury RJ, el-Shibiny A, Connerton PL, Dillon E, Scott A, Connerton IF . 2005. Bacteriophage therapy to reduce Campylobacter jejuni colonization of broiler chickens. Appl Environ Microbiol 71 : 6554 6563.[CrossRef][PubMed]
60. Atterbury RJ, Van Bergen MAP, Ortiz F, Lovell MA, Harris JA, De Boer A, Wagenaar JA, Allen VM, Barrow PA . 2007. Bacteriophage therapy to reduce Salmonella colonization of broiler chickens. Appl Environ Microbiol 73 : 4543 4549.[CrossRef][PubMed]
61. Jamalludeen N, Johnson RP, Shewen PE, Gyles CL . 2009. Evaluation of bacteriophages for prevention and treatment of diarrhea due to experimental enterotoxigenic Escherichia coli O149 infection of pigs. Vet Microbiol 136 : 135 141.[CrossRef][PubMed]
62. 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 : e78543.[CrossRef][PubMed]
63. Borie C, Albala I, Sánchez P, Sánchez ML, Ramírez S, Navarro C, Morales MA, Retamales AJ, Robeson J . 2008. Bacteriophage treatment reduces Salmonella colonization of infected chickens. Avian Dis 52 : 64 67.[CrossRef][PubMed]
64. Naylor SW, Low JC, Besser TE, Mahajan A, Gunn GJ, Pearce MC, McKendrick IJ, Smith DGE, Gally DL . 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.[CrossRef][PubMed]
65. Sheng H, Knecht HJ, Kudva IT, Hovde CJ . 2006. Application of bacteriophages to control intestinal Escherichia coli O157:H7 levels in ruminants. Appl Environ Microbiol 72 : 5359 5366.[CrossRef][PubMed]
66. Rozema EA, Stephens TP, Bach SJ, Okine EK, Johnson RP, Stanford K, McAllister TA . 2009. Oral and rectal administration of bacteriophages for control of Escherichia coli O157:H7 in feedlot cattle. J Food Prot 72 : 241 250.[CrossRef][PubMed]
67. Grauke LJ, Kudva IT, Yoon JW, Hunt CW, Williams CJ, Hovde CJ . 2002. Gastrointestinal tract location of Escherichia coli O157:H7 in ruminants. Appl Environ Microbiol 68 : 2269 2277.[CrossRef][PubMed]
68. Wilf A . 2017. Phage therapy in aquaculture, hopes and challenges. Oceanogr Fish 2 : 1 2.
69. Ma Y, Pacan JC, Wang Q, Xu Y, Huang X, Korenevsky A, Sabour PM . 2008. Microencapsulation of bacteriophage Felix O1 into chitosan-alginate microspheres for oral delivery. Appl Environ Microbiol 74 : 4799 4805.[CrossRef][PubMed]
70. Stanford K, McAllister TA, Niu YD, Stephens TP, Mazzocco A, Waddell TE, Johnson RP . 2010. Oral delivery systems for encapsulated bacteriophages targeted at Escherichia coli O157:H7 in feedlot cattle. J Food Prot 73 : 1304 1312.[CrossRef][PubMed]
71. Wall SK, Zhang J, Rostagno MH, Ebner PD . 2010. Phage therapy to reduce preprocessing Salmonella infections in market-weight swine. Appl Environ Microbiol 76 : 48 53.[CrossRef][PubMed]
72. 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 : 4841 4849.[CrossRef][PubMed]
73. Park SC, Shimamura I, Fukunaga M, Mori KI, Nakai T . 2000. Isolation of bacteriophages specific to a fish pathogen, Pseudomonas plecoglossicida, as a candidate for disease control. Appl Environ Microbiol 66 : 1416 1422.[CrossRef][PubMed]
74. Seed KD, Faruque SM, Mekalanos JJ, Calderwood SB, Qadri F, Camilli A . 2012. Phase variable O antigen biosynthetic genes control expression of the major protective antigen and bacteriophage receptor in Vibrio cholerae O1. PLoS Pathog 8 : e1002917.[CrossRef][PubMed]
75. 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 : 733 740.[CrossRef][PubMed]
76. Carvalho CM, Gannon BW, Halfhide DE, Santos SB, Hayes CM, Roe JM, Azeredo J . 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 : 232.[CrossRef][PubMed]
77. Kunisaki H, Tanji Y . 2010. Intercrossing of phage genomes in a phage cocktail and stable coexistence with Escherichia coli O157:H7 in anaerobic continuous culture. Appl Microbiol Biotechnol 85 : 1533 1540.[CrossRef][PubMed]
78. Oliveira J, Castilho F, Cunha A, Pereira MJ . 2012. Bacteriophage therapy as a bacterial control strategy in aquaculture. Aquacult Int 20 : 879 910.[CrossRef].
79. 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 : 188 194.[CrossRef][PubMed]
80. 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 : 17 22.[CrossRef][PubMed]
81. O'Flynn G, Ross RP, Fitzgerald GF, Coffey A . 2004. Evaluation of a cocktail of three bacteriophages for biocontrol of Escherichia coli O157:H7. Appl Environ Microbiol 70 : 3417 3424.[CrossRef][PubMed]
82. Carter CD, Parks A, Abuladze T, Li M, Woolston J, Magnone J, Senecal A, Kropinski AM, Sulakvelidze A . 2012. Bacteriophage cocktail significantly reduces Escherichia coli O157: H7 contamination of lettuce and beef, but does not protect against recontamination. Bacteriophage 2 : 178 185.[CrossRef][PubMed]
83. Bigwood T, Hudson JA, Billington C, Carey-Smith GV, Heinemann JA . 2008. Phage inactivation of foodborne pathogens on cooked and raw meat. Food Microbiol 25 : 400 406.[CrossRef][PubMed]
84. Tomat D, Mercanti D, Balagué C, Quiberoni A . 2013. Phage biocontrol of enteropathogenic and Shiga toxin-producing Escherichia coli during milk fermentation. Lett Appl Microbiol 57 : 3 10.[CrossRef][PubMed]
85. Zampara A, Sørensen MCH, Elsser-Gravesen A, Brøndsted L . 2017. Significance of phage-host interactions for biocontrol of Campylobacter jejuni in food. Food Control 73 : 1169 1175.[CrossRef].
86. Hooton 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 : 157 163.[CrossRef][PubMed]
87. Atterbury RJ, Connerton PL, Dodd CER, Rees CED, 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 6306.[CrossRef][PubMed]
88. 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 : e0175256.[CrossRef][PubMed]
89. Guenther S, Huwyler D, Richard S, Loessner MJ . 2009. Virulent bacteriophage for efficient biocontrol of Listeria monocytogenes in ready-to-eat foods. Appl Environ Microbiol 75 : 93 100.[CrossRef][PubMed]
90. Perera MN, Abuladze T, Li M, Woolston J, Sulakvelidze A . 2015. Bacteriophage cocktail significantly reduces or eliminates Listeria monocytogenes contamination on lettuce, apples, cheese, smoked salmon and frozen foods. Food Microbiol 52 : 42 48.[CrossRef][PubMed]
91. Zinno P, Devirgiliis C, Ercolini D, Ongeng D, Mauriello G . 2014. Bacteriophage P22 to challenge Salmonella in foods. Int J Food Microbiol 191 : 69 74.[CrossRef][PubMed]
92. Hong Y, Pan Y, Ebner PD . 2014. Meat Science and Muscle Biology Symposium: development of bacteriophage treatments to reduce Escherichia coli O157:H7 contamination of beef products and produce. J Anim Sci 92 : 1366 1377.[CrossRef][PubMed]
93. Hong Y, Schmidt K, Marks D, Hatter S, Marshall A, Albino L, Ebner P . 2016. Treatment of Salmonella-contaminated eggs and pork with a broad-spectrum, single bacteriophage: assessment of efficacy and resistance development. Foodborne Pathog Dis 13 : 679 688.[CrossRef][PubMed]
94. 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.[CrossRef][PubMed]
95. Gencay YE, Ayaz ND, Copuroglu G, Erol I . 2016. Biocontrol of Shiga toxigenic Escherichia coli O157:H7 in Turkish raw meatball by bacteriophage. J Food Saf 36 : 120 131.[CrossRef].
96. Guenther S, Herzig O, Fieseler L, Klumpp J, Loessner MJ . 2012. Biocontrol of Salmonella Typhimurium in RTE foods with the virulent bacteriophage FO1-E2. Int J Food Microbiol 154 : 66 72.[CrossRef][PubMed]
97. 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 : 3019 3026.[CrossRef][PubMed]
98. 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 : 274 279.[CrossRef][PubMed]
99. Bao H, Zhang P, Zhang H, Zhou Y, Zhang L, Wang R . 2015. Bio-control of Salmonella Enteritidis in foods using bacteriophages. Viruses 7 : 4836 4853.[CrossRef][PubMed]
100. García P, Madera C, Martínez B, Rodríguez A . 2007. Biocontrol of Staphylococcus aureus in curd manufacturing processes using bacteriophages. Int Dairy J 17 : 1232 1239.[CrossRef].
101. Bueno E, García P, Martínez B, Rodríguez A . 2012. Phage inactivation of Staphylococcus aureus in fresh and hard-type cheeses. Int J Food Microbiol 158 : 23 27.[CrossRef][PubMed]
102. Modi R, Hirvi Y, Hill A, Griffiths MW . 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 : 927 933.[CrossRef][PubMed]
103. Soni KA, Desai M, Oladunjoye A, Skrobot F, Nannapaneni R . 2012. Reduction of Listeria monocytogenes in queso fresco cheese by a combination of listericidal and listeriostatic GRAS antimicrobials. Int J Food Microbiol 155 : 82 88.[CrossRef][PubMed]
104. 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.[CrossRef][PubMed]
105. Endersen L, Buttimer C, Nevin E, Coffey A, Neve H, Oliveira H, Lavigne R, O'Mahony J . 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.[CrossRef][PubMed]
106. Sharma M, Patel JR, Conway WS, Ferguson S, Sulakvelidze A . 2009. Effectiveness of bacteriophages in reducing Escherichia coli O157:H7 on fresh-cut cantaloupes and lettucet. J Food Prot 72 : 1481 1485.[CrossRef][PubMed]
107. Boyacioglu O, Sharma M, Sulakvelidze A, Goktepe I . 2013. Biocontrol of Escherichia coli O157: H7 on fresh-cut leafy greens. Bacteriophage 3 : e24620.[CrossRef][PubMed]
108. Spricigo DA, Bardina C, Cortés P, Llagostera M . 2013. Use of a bacteriophage cocktail to control Salmonella in food and the food industry. Int J Food Microbiol 165 : 169 174.[CrossRef][PubMed]
109. Sharma M, Dashiell G, Handy ET, East C, Reynnells R, White C, Nyarko E, Micallef S, Hashem F, Millner PD . 2017. Survival of Salmonella Newport on whole and fresh-cut cucumbers treated with lytic bacteriophages. J Food Prot 80 : 668 673.[CrossRef][PubMed]
110. Fong K, LaBossiere B, Switt AIM, Delaquis P, Goodridge L, Levesque RC, Danyluk MD, Wang S . 2017. Characterization of four novel bacteriophages isolated from British Columbia for control of non-typhoidal Salmonella in vitro and on sprouting alfalfa seeds. Front Microbiol 8 : 2193.[CrossRef][PubMed]
111. Ye J, Kostrzynska M, Dunfield K, Warriner K . 2010. Control of Salmonella on sprouting mung bean and alfalfa seeds by using a biocontrol preparation based on antagonistic bacteria and lytic bacteriophages. J Food Prot 73 : 9 17.[CrossRef][PubMed]
112. Leverentz B, Conway WS, Camp MJ, Janisiewicz WJ, Abuladze T, Yang M, Saftner R, Sulakvelidze A . 2003. Biocontrol of Listeria monocytogenes on fresh-cut produce by treatment with lytic bacteriophages and a bacteriocin. Appl Environ Microbiol 69 : 4519 4526.[CrossRef][PubMed]
113. Moye ZD, Woolston J, Sulakvelidze A . 2018. Bacteriophage applications for food production and processing. Viruses 10 : 205.[CrossRef][PubMed]
114. Betts A, Vasse M, Kaltz O, Hochberg ME . 2013. Back to the future: evolving bacteriophages to increase their effectiveness against the pathogen Pseudomonas aeruginosa PAO1. Evol Appl 6 : 1054 1063.[PubMed]
115. EFSA Panel on Biological Hazards (BIOHAZ) . 2012. Scientific opinion on the evaluation of the safety and efficacy of Listex TM P100 for the removal of Listeria monocytogenes surface contamination of raw fish. EFSA J 10 : 2615.[CrossRef].
116. Lukacik P, Barnard TJ, Keller PW, Chaturvedi KS, Seddiki N, Fairman JW, Noinaj N, Kirby TL, Henderson JP, Steven AC, Hinnebusch BJ, Buchanan SK . 2012. Structural engineering of a phage lysin that targets gram-negative pathogens. Proc Natl Acad Sci USA 109 : 9857 9862.[CrossRef][PubMed]
117. Briers Y, Walmagh M, Van Puyenbroeck V, Cornelissen A, Cenens W, Aertsen A, Oliveira H, Azeredo J, Verween G, Pirnay JP, Miller S, Volckaert G, Lavigne R . 2014. Engineered endolysin-based “Artilysins” to combat multidrug-resistant gram-negative pathogens. mBio 5 : e01379-14.[CrossRef][PubMed]
118. Nobrega FL, Costa AR, Kluskens LD, Azeredo J . 2015. Revisiting phage therapy: new applications for old resources. Trends Microbiol 23 : 185 191.[CrossRef][PubMed]
119. Citorik RJ, Mimee M, Lu TK . 2014. Sequence-specific antimicrobials using efficiently delivered RNA-guided nucleases. Nat Biotechnol 32 : 1141 1145.[CrossRef][PubMed]
120. García P, Martínez B, Obeso JM, Rodríguez A . 2008. Bacteriophages and their application in food safety. Lett Appl Microbiol 47 : 479 485.[CrossRef][PubMed]
121. Shin H, Lee JH, Kim H, Choi Y, Heu S, Ryu S . 2012. Receptor diversity and host interaction of bacteriophages infecting Salmonella enterica serovar Typhimurium. PLoS One 7 : e43392.[CrossRef][PubMed]
122. Choi Y, Shin H, Lee JH, Ryu S . 2013. Identification and characterization of a novel flagellum-dependent Salmonella-infecting bacteriophage, iEPS5. Appl Environ Microbiol 79 : 4829 4837.[CrossRef][PubMed]
123. Kim M, Ryu S . 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.[CrossRef][PubMed]
124. Ricci V, Piddock LJV . 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.[CrossRef][PubMed]
125. Killmann H, Braun M, Herrmann C, Braun V . 2001. FhuA barrel-cork hybrids are active transporters and receptors. J Bacteriol 183 : 3476 3487.[CrossRef][PubMed]
126. Kim M, Kim S, Park B, Ryu S . 2014. Core lipopolysaccharide-specific phage SSU5 as an auxiliary component of a phage cocktail for Salmonella biocontrol. Appl Environ Microbiol 80 : 1026 1034.[CrossRef][PubMed]
127. Waddell TE, Poppe C . 2000. Construction of mini-Tn10luxABcam/Ptac-ATS and its use for developing a bacteriophage that transduces bioluminescence to Escherichia coli O157:H7. FEMS Microbiol Lett 182 : 285 289.[CrossRef][PubMed]
128. Sørensen MCH, Gencay YE, Birk T, Baldvinsson SB, Jäckel C, Hammerl JA, Vegge CS, Neve H, Brøndsted L . 2015. Primary isolation strain determines both phage type and receptors recognised by Campylobacter jejuni bacteriophages. PLoS One 10 : e0116287.[CrossRef][PubMed]
129. Bach SJ, McAllister TA, Veira DM, Gannon VPJ, Holley RA . 2003. Effect of bacteriophage DC22 on Escherichia coli O157:H7 in an artificial rumen system (Rusitec) and inoculated sheep. Anim Res 52 : 89 101.[CrossRef].
130. Raya RR, Varey P, Oot RA, Dyen MR, Callaway TR, Edrington TS, Kutter EM, Brabban AD . 2006. Isolation and characterization of a new T-even bacteriophage, CEV1, and determination of its potential to reduce Escherichia coli O157:H7 levels in sheep. Appl Environ Microbiol 72 : 6405 6410.[CrossRef][PubMed]
131. Callaway TR, Edrington TS, Brabban AD, Anderson RC, Rossman ML, Engler MJ, Carr MA, Genovese KJ, Keen JE, Looper ML, Kutter EM, Nisbet DJ . 2008. Bacteriophage isolated from feedlot cattle can reduce Escherichia coli O157:H7 populations in ruminant gastrointestinal tracts. Foodborne Pathog Dis 5 : 183 191.[CrossRef][PubMed]
132. Niu YD, Xu Y, McAllister TA, Rozema EA, Stephens TP, Bach SJ, Johnson RP, Stanford K . 2008. Comparison of fecal versus rectoanal mucosal swab sampling for detecting Escherichia coli O157:H7 in experimentally inoculated cattle used in assessing bacteriophage as a mitigation strategy. J Food Prot 71 : 691 698.[CrossRef][PubMed]
133. Rivas L, Coffey B, McAuliffe O, McDonnell MJ, Burgess CM, Coffey A, Ross RP, Duffy G . 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.[CrossRef][PubMed]
134. Raya RR, Oot RA, Moore-Maley B, Wieland S, Callaway TR, Kutter EM, Brabban AD . 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.[CrossRef][PubMed]
135. Berchieri A Jr, Lovell MA, Barrow PA . 1991. The activity in the chicken alimentary tract of bacteriophages lytic for Salmonella Typhimurium. Res Microbiol 142 : 541 549.[CrossRef][PubMed]
136. Sklar IB, Joerger RD . 2001. Attempts to utilize bacteriophage to combat Salmonella enterica serovar Enteritidis [ sic] infection in chickens. J Food Saf 21 : 15 29.[CrossRef].
137. Lee N, Harris D . 2001. The effect of bacteriophage treatment to reduce the rapid dissemination of Salmonella Typhimurium in pigs. Swine Res Rep 50 : 196 197.
138. Fiorentin L, Vieira ND, Barioni W Jr . 2005. Oral treatment with bacteriophages reduces the concentration of Salmonella Enteritidis PT4 in caecal contents of broilers. Avian Pathol 34 : 258 263.[CrossRef][PubMed]
139. Toro H, Price SB, McKee AS, Hoerr FJ, Krehling J, Perdue M, Bauermeister L . 2005. Use of bacteriophages in combination with competitive exclusion to reduce Salmonella from infected chickens. Avian Dis 49 : 118 124.[CrossRef][PubMed]
140. Andreatti Filho RL, Higgins JP, Higgins SE, Gaona G, Wolfenden AD, Tellez G, Hargis BM . 2007. Ability of bacteriophages isolated from different sources to reduce Salmonella enterica serovar enteritidis in vitro and in vivo. Poult Sci 86 : 1904 1909.[CrossRef][PubMed]
141. 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 1274.[CrossRef][PubMed]
142. Albino LAA, Rostagno MH, Húngaro HM, Mendonça RCS . 2014. Isolation, characterization, and application of bacteriophages for Salmonella spp. biocontrol in pigs. Foodborne Pathog Dis 11 : 602 609.[CrossRef][PubMed]
143. Wagenaar JA, Van Bergen MA, Mueller MA, Wassenaar TM, Carlton RM . 2005. Phage therapy reduces Campylobacter jejuni colonization in broilers. Vet Microbiol 109 : 275 283.[CrossRef][PubMed]
144. Kittler S, Fischer S, Abdulmawjood A, Glünder G, Klein G . 2013. Effect of bacteriophage application on Campylobacter jejuni loads in commercial broiler flocks. Appl Environ Microbiol 79 : 7525 7533.[CrossRef][PubMed]
145. Hammerl JA, Jäckel C, Alter T, Janzcyk P, Stingl K, Knüver MT, Hertwig S . 2014. Reduction of Campylobacter jejuni in broiler chicken by successive application of group II and group III phages. PLoS One 9 : e114785.[CrossRef][PubMed]
146. Martínez-Díaz SF, Hipólito-Morales A . 2013. Efficacy of phage therapy to prevent mortality during the vibriosis of brine shrimp. Aquaculture 400–401 : 120 124.[CrossRef].
147. Stalin N, Srinivasan P . 2017. Efficacy of potential phage cocktails against Vibrio harveyi and closely related Vibrio species isolated from shrimp aquaculture environment in the south east coast of India. Vet Microbiol 207 : 83 96.[CrossRef][PubMed]
148. Abuladze T, Li M, Menetrez MY, Dean T, Senecal A, Sulakvelidze A . 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.[CrossRef][PubMed]
149. Viazis S, Akhtar M, Feirtag J, Diez-Gonzalez F . 2011. Reduction of Escherichia coli O157:H7 viability on leafy green vegetables by treatment with a bacteriophage mixture and trans-cinnamaldehyde. Food Microbiol 28 : 149 157.[CrossRef][PubMed]
150. Hudson JA, Billington C, Cornelius AJ, Wilson T, On SLW, Premaratne A, King NJ . 2013. Use of a bacteriophage to inactivate Escherichia coli O157:H7 on beef. Food Microbiol 36 : 14 21.[CrossRef][PubMed]
151. Hudson JA, Billington C, Wilson T, On SL . 2015. Effect of phage and host concentration on the inactivation of Escherichia coli O157:H7 on cooked and raw beef. Food Sci Technol Int 21 : 104 109.[CrossRef][PubMed]
152. Ferguson S, Roberts C, Handy E, Sharma M . 2013. Lytic bacteriophages reduce Escherichia coli O157: H7 on fresh cut lettuce introduced through cross-contamination. Bacteriophage 3 : e24323.[CrossRef][PubMed]
153. Shahrbabak SS, Khodabandehlou Z, Shahverdi AR, Skurnik M, Ackermann HW, Varjosalo M, Yazdi MT, Sepehrizadeh Z . 2013. Isolation, characterization and complete genome sequence of PhaxI: a phage of Escherichia coli O157: H7. Microbiology 159 : 1629 1638.[CrossRef][PubMed]
154. Lee H, Ku HJ, Lee DH, Kim YT, Shin H, Ryu S, Lee JH . 2016. Characterization and genomic study of the novel bacteriophage HY01 infecting both Escherichia coli O157:H7 and Shigella flexneri: potential as a biocontrol agent in food. PLoS One 11 : e0168985.[CrossRef][PubMed]
155. Snyder AB, Perry JJ, Yousef AE . 2016. Developing and optimizing bacteriophage treatment to control enterohemorrhagic Escherichia coli on fresh produce. Int J Food Microbiol 236 : 90 97.[CrossRef][PubMed]
156. Seo J, Seo DJ, Oh H, Jeon SB, Oh MH, Choi C . 2016. Inhibiting the growth of Escherichia coli O157:H7 in beef, pork, and chicken meat using a bacteriophage. Han-gug Chugsan Sigpum Hag-hoeji 36 : 186 193.[CrossRef][PubMed]
157. Cui H, Yuan L, Lin L . 2017. Novel chitosan film embedded with liposome-encapsulated phage for biocontrol of Escherichia coli O157:H7 in beef. Carbohydr Polym 177 : 156 164.[CrossRef][PubMed]
158. Leverentz B, Conway WS, Alavidze Z, Janisiewicz WJ, Fuchs Y, Camp MJ, Chighladze E, Sulakvelidze A . 2001. Examination of bacteriophage as a biocontrol method for Salmonella on fresh-cut fruit: a model study. J Food Prot 64 : 1116 1121.[CrossRef][PubMed]
159. Whichard JM, Sriranganathan N, Pierson FW . 2003. Suppression of Salmonella growth by wild-type and large-plaque variants of bacteriophage Felix O1 in liquid culture and on chicken frankfurters. J Food Prot 66 : 220 225.[CrossRef][PubMed]
160. 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 : 5032 5036.[CrossRef][PubMed]
161. Pao S, Rolph SP, Westbrook EW, Shen H . 2004. Use of bacteriophages to control Salmonella in experimentally contaminated sprout seeds. J Food Sci 69 :M 127–M 130.[CrossRef].
162. Higgins JP, Higgins SE, Guenther KL, Huff W, Donoghue AM, Donoghue DJ, Hargis BM . 2005. Use of a specific bacteriophage treatment to reduce Salmonella in poultry products. Poult Sci 84 : 1141 1145.[CrossRef][PubMed]
163. Donoghue AM, Bielke LR, Higgins SE, Donoghue DJ, Hargis BM, Tellez G . 2007. Use of wide-host-range bacteriophages to reduce Salmonella on poultry products. Int J Poult Sci 6 : 754 757.[CrossRef].
164. Kocharunchitt C, Ross T, McNeil DL . 2009. Use of bacteriophages as biocontrol agents to control Salmonella associated with seed sprouts. Int J Food Microbiol 128 : 453 459.[CrossRef][PubMed]
165. Ye J, Kostrzynska M, Dunfield K, Warriner K . 2009. Evaluation of a biocontrol preparation consisting of Enterobacter asburiae JX1 and a lytic bacteriophage cocktail to suppress the growth of Salmonella Javiana associated with tomatoes. J Food Prot 72 : 2284 2292.[CrossRef][PubMed]
166. Kang HW, Kim JW, Jung TS, Woo GJ . 2013. wksl3, a new biocontrol agent for Salmonella enterica serovars Enteritidis and Typhimurium in foods: characterization, application, sequence analysis, and oral acute toxicity study. Appl Environ Microbiol 79 : 1956 1968.[CrossRef][PubMed]
167. Augustine J, Bhat SG . 2015. Biocontrol of Salmonella Enteritidis in spiked chicken cuts by lytic bacteriophages φSP-1 and φSP-3. J Basic Microbiol 55 : 500 503.[CrossRef][PubMed]
168. Sukumaran AT, Nannapaneni R, Kiess A, Sharma CS . 2015. Reduction of Salmonella on chicken meat and chicken skin by combined or sequential application of lytic bacteriophage with chemical antimicrobials. Int J Food Microbiol 207 : 8 15.[CrossRef][PubMed]
169. Oliveira M, Abadias M, Colás-Medà P, Usall J, Viñas I . 2015. Biopreservative methods to control the growth of foodborne pathogens on fresh-cut lettuce. Int J Food Microbiol 214 : 4 11.[CrossRef][PubMed]
170. Pereira C, Moreirinha C, Rocha RJM, Calado R, Romalde JL, Nunes ML, Almeida A . 2016. Application