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Bacteriophage Applications for Food Safety

  • Ayman El-ShibinyEmail author
  • Alyaa Dawoud
Chapter
  • 75 Downloads

Abstract

Ingestion of food and water contaminated with pathogenic bacteria may cause serious diseases. Many of those pathogenic bacteria are considered normal microbiota of many animals and poultry and they usually infect human through cross contamination. With the increase resistance of bacteria to most available antibiotics, the development of an alternative and effective method to control bacterial infections is becoming an urgent solution. Bacteriophage therapy is considered an alternative to antibiotics to control bacterial contamination of food especially after the U.S. Food and Drug Administration (FDA) approval in 2006 to use phages as a safe food additive. It is very important to use virulent phages and to identify the best cocktail that shows the highest efficacy against their target bacterial host before biocontrol applications. In this chapter, we will discuss the successful applications of phages to decontaminate different types of food such as; meat, poultry, eggs, fish, fruits, vegetables, food animals and drinking water during processing stages to control bacterial infections. In addition, we will discuss the developments in phage delivery systems and the application of nano-based bio-packing material and edible anti-microbial coating to enhance the effectiveness of phages as a biocontrol agent.

References

  1. Abdelsattar AS, Abdelrahman F, Dawoud A, Connerton IF, El-Shibiny A (2019) Encapsulation of E. coli phage ZCEC5 in chitosan–alginate beads as a delivery system in phage therapy. AMB Express 9(1):87.  https://doi.org/10.1186/s13568-019-0810-9CrossRefPubMedPubMedCentralGoogle Scholar
  2. Abedon ST, Kuhl SJ, Blasdel BG, Kutter EM (2011) Phage treatment of human infections. Bacteriophage 1:66–85.  https://doi.org/10.4161/bact.1.2.15845CrossRefPubMedPubMedCentralGoogle Scholar
  3. Akinkunmi EO, Adesunkanmi AR, Lamikanra A (2014) Pattern of pathogens from surgical wound infections in a Nigerian hospital and their antimicrobial susceptibility profiles. Afr Health Sci 14.  https://doi.org/10.4314/ahs.v14i4.5
  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(18):6379–6387.  https://doi.org/10.1128/aem.05493-11CrossRefPubMedPubMedCentralGoogle Scholar
  5. 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(9):1904–1909CrossRefGoogle Scholar
  6. 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.  https://doi.org/10.1128/AEM.69.10.6302-6306.2003CrossRefPubMedPubMedCentralGoogle Scholar
  7. Attridge SR, Fazeli A, Manning PA, Stroeher UH (2001) Isolation and characterization of bacteriophage-resistant mutants of Vibrio cholerae O139. Microb Pathog 30:237–246.  https://doi.org/10.1006/mpat.2000.0426CrossRefPubMedGoogle Scholar
  8. Bai J, Kim YT, Ryu S, Lee JH (2016) Biocontrol and rapid detection of food-borne pathogens using bacteriophages and endolysins. Front Microbiol 7.  https://doi.org/10.3389/fmicb.2016.00474
  9. Belongia EA, MacDonald KL, Parham GL, White KE, Korlath JA, Lobato MN et al (1991) An outbreak of Escherichia coli O157:H7 colitis associated with consumption of precooked meat patties. J Infect Dis 164:338–343.  https://doi.org/10.1093/infdis/164.2.338CrossRefPubMedGoogle Scholar
  10. Bergmann CP, Stumpf A (2013) Dental ceramics: microstructure, properties and degradation. In Dental ceramics: microstructure, properties and degradation.  https://doi.org/10.1007/978-3-642-38224-6
  11. 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.  https://doi.org/10.1016/j.fm.2007.11.003CrossRefPubMedGoogle Scholar
  12. Bren L (2007) Bacteria-eating virus approved as food additive. FDA ConsumGoogle Scholar
  13. Brooks JD, Flint SH (2008) Biofilms in the food industry: problems and potential solutions. Int J Food Sci Technol 43(12):2163–2176.  https://doi.org/10.1111/j.1365-2621.2008.01839.xCrossRefGoogle Scholar
  14. Brown-Jaque M, Muniesa M, Navarro F (2016) Bacteriophages in clinical samples can interfere with microbiological diagnostic tools. Sci Rep 6(September):1–8.  https://doi.org/10.1038/srep33000CrossRefGoogle Scholar
  15. 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.  https://doi.org/10.1128/AAC.49.7.2874-2878.2005CrossRefPubMedPubMedCentralGoogle Scholar
  16. Campos J, Gil J, Mourão J, Peixe L, Antunes P (2015) Ready-to-eat street-vended food as a potential vehicle of bacterial pathogens and antimicrobial resistance: an exploratory study in Porto region, Portugal. Int J Food Microbiol 206:1–6.  https://doi.org/10.1016/j.ijfoodmicro.2015.04.016CrossRefPubMedGoogle Scholar
  17. 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.  https://doi.org/10.1016/j.yrtph.2005.08.005CrossRefPubMedGoogle Scholar
  18. Chang Y, Yoon H, Kang DH, Chang PS, Ryu S (2017) Endolysin LysSA97 is synergistic with carvacrol in controlling Staphylococcus aureus in foods. Int J Food Microbiol 244:19–26.  https://doi.org/10.1016/j.ijfoodmicro.2016.12.007CrossRefPubMedGoogle Scholar
  19. Cheetham BF, Katz ME (1995) A role for bacteriophages in the evolution and transfer of bacterial virulence determinants. Mol Microbiol 18(2):201–208.  https://doi.org/10.1111/j.1365-2958.1995.mmi_18020201.xCrossRefPubMedGoogle Scholar
  20. Choińska-Pulit A, Mituła P, Śliwka P, Łaba W, Skaradzińska A (2015) Bacteriophage encapsulation: trends and potential applications. Trends Food Sci Technol 45:212–221.  https://doi.org/10.1016/j.tifs.2015.07.001CrossRefGoogle Scholar
  21. 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(14):4841–4849.  https://doi.org/10.1128/AEM.00812-15CrossRefPubMedPubMedCentralGoogle Scholar
  22. d’Herelle F (1917) Sur un microbe invisible antagoniste des bacilles dysentériques. CR Acad.Sci, ParisGoogle Scholar
  23. Delbruck M (1940) The growth of bacteriophage and lysis of the host. J Gen Physiol 23:643–660.  https://doi.org/10.1085/jgp.23.5.643CrossRefPubMedPubMedCentralGoogle Scholar
  24. Dobrindt U, Janke B, Piechaczek K, Nagy G, Ziebuhr W, Fischer G et al (2000) Toxin genes on pathogenicity islands: impact for microbial evolution. Int J Med Microbiol 290(4–5):307–311.  https://doi.org/10.1016/S1438-4221(00)80028-4CrossRefPubMedGoogle Scholar
  25. 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(4):733–740.  https://doi.org/10.4315/0362-028X-72.4.733CrossRefPubMedGoogle Scholar
  26. El-Shibiny A, El-Sahhar S, Adel M (2017) Phage applications for improving food safety and infection control in Egypt. J Appl Microbiol 123:556–567.  https://doi.org/10.1111/jam.13500CrossRefPubMedGoogle Scholar
  27. 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(1):327–349.  https://doi.org/10.1146/annurev-food-030713-092415CrossRefPubMedGoogle Scholar
  28. Fagan RP, McLaughlin JB, Castrodale LJ, Gessner BD, Jenkerson SA, Funk EA et al (2011) Endemic foodborne botulism among Alaska native persons-Alaska, 1947-2007. Clin Infect Dis 52(5):585–592.  https://doi.org/10.1093/cid/ciq240CrossRefPubMedGoogle Scholar
  29. Fister S, Robben C, Witte AK, Schoder D, Wagner M, Rossmanith P (2016) Influence of environmental factors on phage-bacteria interaction and on the efficacy and infectivity of phage P100. Frontiers Microbiol 7(JUL):1–13.  https://doi.org/10.3389/fmicb.2016.01152CrossRefGoogle Scholar
  30. Fortini D, Fashae K, García-Fernández A, Villa L, Carattoli A (2011) Plasmid-mediated quinolone resistance and β-lactamases in Escherichia coli from healthy animals from Nigeria. J Antimicrob Chemother 66:1269–1272.  https://doi.org/10.1093/jac/dkr085CrossRefPubMedGoogle Scholar
  31. García P, Martínez B, Obeso JM, Rodríguez A (2008) Bacteriophages and their application in food safety. Lett Appl Microbiol 47(6):479–485.  https://doi.org/10.1111/j.1472-765X.2008.02458.xCrossRefPubMedGoogle Scholar
  32. Gbassi GK, Vandamme T (2012) Probiotic encapsulation technology: from microencapsulation to release into the gut. Pharmaceutics 4(1):149–163.  https://doi.org/10.3390/pharmaceutics4010149CrossRefPubMedPubMedCentralGoogle Scholar
  33. 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.  https://doi.org/10.1128/AEM.69.8.5032-5036.2003CrossRefPubMedPubMedCentralGoogle Scholar
  34. Goodridge LD, Bisha B (2011) Phage-based biocontrol strategies to reduce foodborne pathogens in foods. Bacteriophage 1(3):130–137.  https://doi.org/10.4161/bact.1.3.17629CrossRefPubMedPubMedCentralGoogle Scholar
  35. Górski A, Wazna E, Daṃbrowska BW, Daṃbrowska K, Świtała-Jeleń K, Miȩdzybrodzki R (2006) Bacteriophage translocation. FEMS Immunol Med Microbiol 46(3):313–319.  https://doi.org/10.1111/j.1574-695X.2006.00044.xCrossRefPubMedGoogle Scholar
  36. Górski A, Miedzybrodzki R, Weber-Dabrowska B, Fortuna W, Letkiewicz S, Rogóz P et al (2016) Phage therapy: combating infections with potential for evolving from merely a treatment for complications to targeting diseases. Frontiers Microbiol 7(SEP):1–9.  https://doi.org/10.3389/fmicb.2016.01515CrossRefGoogle Scholar
  37. Gould LH, Nisler AL, Herman KM, Cole DJ, Williams IT, Mahon BE et al (2011) Surveillance for foodborne disease outbreaks — United States, 2008. Morb Mortal Wkly RepGoogle Scholar
  38. Greer GG, Dilts BD (1990) Inability of a bacteriophage pool to control beef spoilage. Int J Food Microbiol 10:331–342.  https://doi.org/10.1016/0168-1605(90)90080-OCrossRefPubMedGoogle Scholar
  39. 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.  https://doi.org/10.1016/j.ijfoodmicro.2011.12.023CrossRefPubMedGoogle Scholar
  40. Hacker J, Bender L, Ott M, Wingender J, Lund B, Marre R, Goebel W (1990) Deletions of chromosomal regions coding for fimbriae and hemolysins occur in vitro and in vivo in various extra intestinal Escherichia coli isolates. Microb Pathog 8(3):213–225.  https://doi.org/10.1016/0882-4010(90)90048-UCrossRefPubMedGoogle Scholar
  41. Hagens S, Loessner (2010) Bacteriophage for biocontrol of foodborne pathogens. Curr Pharm Biotechnol 11(1):58–68. Retrieved from http://e-citations.ethbib.ethz.ch/view/pub:29137CrossRefGoogle Scholar
  42. Harper DR, Parracho HMRT, Walker J, Sharp R, Hughes G, Werthén M et al (2014) Bacteriophages and biofilms. Antibiotics 3:270–284.  https://doi.org/10.3390/antibiotics3030270CrossRefPubMedCentralGoogle Scholar
  43. Hildebrand GJ, Wolochow H (1962) Translocation of bacteriophage across the intestinal wall of the rat. Proc Soc Exp Biol Med 109(1):183–185CrossRefGoogle Scholar
  44. Hoffmann M (1965) Animal Experiments on Mucosal Passage and Absorption Viraemia of T3 Phages after Oral, Trachéal and Rectal Administration. Zentralblatt Bakteriol Parasitenkd Infekt Hyg 198(4):371–390Google Scholar
  45. Hubbell JA, Chilkoti A (2012) Chemistry. Nanomaterials for drug delivery. Science 337(6092):303–305.  https://doi.org/10.1126/science.1219657CrossRefPubMedGoogle Scholar
  46. Huff WE, Huff GR, Rath NC, Balog JM, Donoghue AM (2002) Prevention of Escherichia coli infection in broiler chickens with a bacteriophage aerosol spray. Poult Sci 81:1486–1491.  https://doi.org/10.1093/ps/81.10.1486CrossRefPubMedGoogle Scholar
  47. Ishani D, Tina S (2015) Bacteriophages as twenty-first century antibacterial tools for food and medicine. J Interdisciplinary Multidisciplinary Res 2(9):92–97.  https://doi.org/10.1007/s00253-011-3227-1CrossRefGoogle Scholar
  48. Jain RK, Stylianopoulos T (2010) Delivering nanomedicine to solid tumors. Nat Rev Clin Oncol 7:653–664.  https://doi.org/10.1038/nrclinonc.2010.139CrossRefPubMedPubMedCentralGoogle Scholar
  49. Keller R, Engley FB (2013) Fate of bacteriophage particles introduced into mice by various routes. Exp Biol Med 98:577–580.  https://doi.org/10.3181/00379727-98-24112CrossRefGoogle Scholar
  50. 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.  https://doi.org/10.1016/j.ijfoodmicro.2008.10.014CrossRefPubMedGoogle Scholar
  51. Koo J, DePaola A, Marshall DL (2000) Effect of simulated gastric fluid and bile on survival of Vibrio vulnificus and Vibrio vulnificus phage†. J Food Prot 63:1665–1669.  https://doi.org/10.4315/0362-028X-63.12.1665CrossRefPubMedGoogle Scholar
  52. Koutsoumanis KP, Sofos JN (2005) Effect of inoculum size on the combined temperature, pH and a w limits for growth of Listeria monocytogenes. Int J Food Microbiol 104:83–91.  https://doi.org/10.1016/j.ijfoodmicro.2005.01.010CrossRefPubMedGoogle Scholar
  53. Kutateladze M, Adamia R (2010) Bacteriophages as potential new therapeutics to replace or supplement antibiotics. Trends Biotechnol 28:591–595.  https://doi.org/10.1016/j.tibtech.2010.08.001CrossRefPubMedGoogle Scholar
  54. Labrie SJ, Samson JE, Moineau S (2010) Bacteriophage resistance mechanisms. Nat Rev Microbiol 8:317–327.  https://doi.org/10.1038/nrmicro2315CrossRefPubMedGoogle Scholar
  55. León M, Bastías R (2015) Virulence reduction in bacteriophage resistant bacteria. Front Microbiol 6(APR):1–7.  https://doi.org/10.3389/fmicb.2015.00343CrossRefGoogle Scholar
  56. Leverentz B, Conway WS, Alavidze Z, Janisiewicz WJ, Fuchs Y, Camp MJ et al (2001) Examination of bacteriophage as a biocontrol method for Salmonella on fresh-cut fruit: A model study. J Food Prot 64:1116–1121.  https://doi.org/10.4315/0362-028X-64.8.1116CrossRefPubMedGoogle Scholar
  57. Leverentz B, Conway WS, Camp MJ, Janisiewicz WJ, Abuladze T, Yang M et al (2003) Biocontrol of Listeria monocytogenes on fresh-cut produce by treatment with lytic bacteriophages and a bacteriocin. Appl Environ Microbiol 69(8):4519–4526CrossRefGoogle Scholar
  58. Loc Carrillo CM, Connerton PL, Pearson T, Connerton IF (2007) Free-range layer chickens as a source of campylobacter bacteriophage. Anton Leeuw Int J Gen Mol Microbiol 92:275–284.  https://doi.org/10.1007/s10482-007-9156-4CrossRefGoogle Scholar
  59. Loretz M, Stephan R, Zweifel C (2010) Antimicrobial activity of decontamination treatments for poultry carcasses: A literature survey. Food Control 21:791–804.  https://doi.org/10.1016/j.foodcont.2009.11.007CrossRefGoogle Scholar
  60. Lourens-Hattingh A, Viljoen BC (2001) Yogurt as probiotic carrier food. Int Dairy J 11(1–2):1–17.  https://doi.org/10.1016/S0958-6946(01)00036-XCrossRefGoogle Scholar
  61. Ly-Chatain MH (2014) The factors affecting effectiveness of treatment in phages therapy. Front Microbiol 5.  https://doi.org/10.3389/fmicb.2014.00051
  62. Lynch MF, Tauxe RV, Hedberg CW (2009) The growing burden of foodborne outbreaks due to contaminated fresh produce: risks and opportunities. Epidemiol Infect 137:307–315.  https://doi.org/10.1017/S0950268808001969CrossRefPubMedGoogle Scholar
  63. Majewska J, Beta W, Lecion D, Hodyra-Stefaniak K, Kłopot A, Kazmiercźak Z et al (2015) Oral application of T4 phage induces weak antibody production in the gut and in the blood. Viruses 7(8):4783–4799.  https://doi.org/10.3390/v7082845CrossRefPubMedPubMedCentralGoogle Scholar
  64. Manrique P, Dills M, Young MJ (2017) The human gut phage community and its implications for health and disease. 9–11.  https://doi.org/10.3390/v9060141
  65. McVay CS, Velásquez M, Fralick JA (2007) Phage therapy of Pseudomonas aeruginosa infection in a mouse burn wound model. Antimicrob Agents Chemother 51:1934–1938.  https://doi.org/10.1128/AAC.01028-06CrossRefPubMedPubMedCentralGoogle Scholar
  66. 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.  https://doi.org/10.4315/0362-028X-64.7.927CrossRefPubMedGoogle Scholar
  67. Modi SR, Lee HH, Spina CS, Collins JJ (2014) Ecological network of the phage metagenome. Nature 499(7457):219–222.  https://doi.org/10.1038/nature12212.AntibioticCrossRefGoogle Scholar
  68. Monk AB, Rees CD, Barrow P, Hagens S, Harper DR (2010) Bacteriophage applications: where are we now? Lett Appl Microbiol 51:363–369.  https://doi.org/10.1111/j.1472-765X.2010.02916.xCrossRefPubMedGoogle Scholar
  69. Morozova VV, Vlassov VV, Tikunova NV (2018) Applications of bacteriophages in the treatment of localized infections in humans. Front Microbiol 9(AUG).  https://doi.org/10.3389/fmicb.2018.01696
  70. Mousavi, S. L., Rasooli, I., Nazarian, S., & Amani, J. (2009). Simultaneous detection of Escherichia coli O157:H7, toxigenic Vibrio cholerae, and Salmonella typhimurium by multiplex PCR. Iran J Clin Infect Dis. 4(2): 97-103Google Scholar
  71. Nagel TE, Chan BK, De Vos D, El-Shibiny A, Kang’ethe EK, Makumi A, Pirnay JP (2016) The developing world urgently needs phages to combat pathogenic bacteria. Front Microbiol 7.  https://doi.org/10.3389/fmicb.2016.00882
  72. Navarro F, Muniesa M (2017) Phages in the human body. Front Microbiol 8(APR):1–7.  https://doi.org/10.3389/fmicb.2017.00566CrossRefGoogle Scholar
  73. 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.  https://doi.org/10.1128/AEM.70.6.3417-3424.2004CrossRefPubMedPubMedCentralGoogle Scholar
  74. Oliveira M, Viñas I, Colàs P, Anguera M, Usall J, Abadias M (2014) Effectiveness of a bacteriophage in reducing Listeria monocytogenes on fresh-cut fruits and fruit juices. Food Microbiol 38:137–142.  https://doi.org/10.1016/j.fm.2013.08.018CrossRefPubMedGoogle Scholar
  75. Pao S, Rolph SP, Westbrook EW, Shen H (2006) Use of bacteriophages to control Salmonella in experimentally contaminated sprout seeds. J Food Sci 69:M127–M130.  https://doi.org/10.1111/j.1365-2621.2004.tb10720.xCrossRefGoogle Scholar
  76. Pavlickova S, Dolezalova M, Holko I (2015) Resistance and virulence factors of Escherichia coli isolated from chicken. J Environ Sci Health, Part B Pestic Food Contam Agric Wastes 50:417–421.  https://doi.org/10.1080/03601234.2015.1011959CrossRefGoogle Scholar
  77. Payne RJH, Jansen VAA (2001) Understanding bacteriophage therapy as a density-dependent kinetic process. J Theor Biol 208:37–48.  https://doi.org/10.1006/jtbi.2000.2198CrossRefPubMedGoogle Scholar
  78. Pelaz B, Alexiou C, Alvarez-Puebla RA, Alves F, Andrews AM, Ashraf S et al (2017) Diverse applications of nanomedicine. ACS Nano 11(3):2313–2381.  https://doi.org/10.1021/acsnano.6b06040CrossRefPubMedPubMedCentralGoogle Scholar
  79. Pennington H (2010) Escherichia coli O157. Lancet 376(9750):1428–1435.  https://doi.org/10.1016/S0140-6736(10)60963-4CrossRefPubMedGoogle Scholar
  80. Ramesh V, Fralick JA, Rolfe RD (1999) Prevention of Clostridium difficile-induced ileocecitis with bacteriophage. Anaerobe 5:69–78.  https://doi.org/10.1006/anae.1999.0192CrossRefGoogle Scholar
  81. Ranadheera RDCS, Baines SK, Adams MC (2010) Importance of food in probiotic efficacy. Food Res Int 43:1–7.  https://doi.org/10.1016/j.foodres.2009.09.009CrossRefGoogle Scholar
  82. Rao VB, Black LW (2010) Structure and assembly of bacteriophage T4 head. Virol J 7:1–14.  https://doi.org/10.1186/1743-422X-7-356CrossRefGoogle Scholar
  83. 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. Bacteriophage 1(1):15–24.  https://doi.org/10.4161/bact.1.1.14175CrossRefPubMedPubMedCentralGoogle Scholar
  84. Reynaud A, Cloastre L, Bernard J, Laveran H, Ackermann HW, Licois D, Joly B (1992) Characteristics and diffusion in the rabbit of a phage for Escherichia coli 0103. Attempts to use this phage for therapy. Vet Microbiol 30:203–212.  https://doi.org/10.1016/0378-1135(92)90114-9CrossRefPubMedGoogle Scholar
  85. Rosenquist H, Nielsen NL, Sommer HM, Nørrung B, Christensen BB (2003) Quantitative risk assessment of human campylobacteriosis associated with thermophilic Campylobacter species in chickens. Int J Food Microbiol 83:87–103.  https://doi.org/10.1016/S0168-1605(02)00317-3CrossRefPubMedGoogle Scholar
  86. Rozema EA, Stephens TP, Bach SJ, Okine EK, Johnson RP, Stanford KIM, Mcallister TA (2009) Oral and rectal administration of bacteriophages for control of escherichia coli O157.-H7 in feedlot cattle. J Food Prot 72(2):241–250.  https://doi.org/10.4315/0362-028X-72.2.241CrossRefPubMedGoogle Scholar
  87. Ryan EM, Alkawareek MY, Donnelly RF, Gilmore BF (2012) Synergistic phage-antibiotic combinations for the control of Escherichia coli biofilms in vitro. FEMS Immunol Med Microbiol 65(2):395–398.  https://doi.org/10.1111/j.1574-695X.2012.00977.xCrossRefPubMedGoogle Scholar
  88. Sanders ME (2008) Probiotics: definition, sources, selection, and uses. Clin Infect Dis 46(s2):S58–S61.  https://doi.org/10.1086/523341CrossRefPubMedGoogle Scholar
  89. Sarhan WA, Azzazy HME (2015) Phage approved in food, why not as a therapeutic? Expert Rev Anti-Infect Ther 13(1):91–101.  https://doi.org/10.1586/14787210.2015.990383CrossRefPubMedGoogle Scholar
  90. Scallan E, Hoekstra RM, Angulo FJ, Tauxe RV, Widdowson M, Roy SL, Jones JL, Griffin PM (2011) Foodborne illness acquired in the United States- major pathogens. Emerg Infect Dis 17:7–15.  https://doi.org/10.3201/eid1701.P11101CrossRefPubMedPubMedCentralGoogle Scholar
  91. Schellekens MM, Woutersi J, Hagens S, Hugenholtz J (2007) Bacteriophage P100 application to control Listeria monocytogenes on smeared cheese. MilchwissenschaftGoogle Scholar
  92. Schubbert R, Lettmann C, Doerfler W (1994) Ingested foreign (phage M13) DNA survives transiently in the gastrointestinal tract and enters the bloodstream of mice. MGG Mol Gen Genet 242(5):495–504.  https://doi.org/10.1007/BF00285273CrossRefPubMedGoogle Scholar
  93. Smith DL, Harris AD, Johnson JA, Silbergeld EK, Morris JG (2002) Animal antibiotic use has an early but important impact on the emergence of antibiotic resistance in human commensal bacteria. Proc Natl Acad Sci U S A 99:6434–6439.  https://doi.org/10.1073/pnas.082188899CrossRefPubMedPubMedCentralGoogle Scholar
  94. Soni KA, Nannapaneni R (2010) Removal of listeria monocytogenes biofilms with bacteriophage P100. J Food Prot 73:1519–1524.  https://doi.org/10.4315/0362-028X-73.8.1519CrossRefPubMedGoogle Scholar
  95. 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(2):169–174.  https://doi.org/10.1016/j.ijfoodmicro.2013.05.009CrossRefPubMedGoogle Scholar
  96. Stone R (2002) Bacteriophage therapy. Food and agriculture: testing grounds for phage therapy. Science 298:730.  https://doi.org/10.1126/science.298.5594.730CrossRefPubMedGoogle Scholar
  97. Summers WC (1999) Bacteriophage discovered. In Félix d’Herelle and the origins of molecular biology. (p. 230). Retrieved from https://yalebooks.yale.edu/book/9780300071276/felix-dherelle-and-origins-molecular-biology
  98. Swaminathan B, Gerner-Smidt P (2007) The epidemiology of human listeriosis. Microbes Infect 9:1236–1243.  https://doi.org/10.1016/j.micinf.2007.05.011CrossRefPubMedGoogle Scholar
  99. Tanji Y, Shimada T, Yoichi M, Miyanaga K, Hori K, Unno H (2004) Toward rational control of Escherichia coli O157:H7 by a phage cocktail. Appl Microbiol Biotechnol 64(2):270–274.  https://doi.org/10.1007/s00253-003-1438-9CrossRefPubMedGoogle Scholar
  100. Tanji Y, Shimada T, Fukudomi H, Miyanaga K, Nakai Y, Unno H (2005) Therapeutic use of phage cocktail for controlling Escherichia coli O157:H7 in gastrointestinal tract of mice. J Biosci Bioeng 100:280–287.  https://doi.org/10.1263/jbb.100.280CrossRefPubMedGoogle Scholar
  101. Translocation of Bacteriophage Across the Intestinal Wall of the Rat (1962) Proceedings of the Society for Experimental Biology and Medicine.  https://doi.org/10.3181/00379727-109-27146
  102. Turki Y, Ouzari H, Mehri I, Ammar AB, Hassen A (2012) Evaluation of a cocktail of three bacteriophages for the biocontrol of Salmonella of wastewater. Food Res Int 45:1099–1105.  https://doi.org/10.1016/j.foodres.2011.05.041CrossRefGoogle Scholar
  103. 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.  https://doi.org/10.1016/j.fm.2010.09.009CrossRefPubMedGoogle Scholar
  104. Waddell TE, Mazzocco A, Pacan J, Ahmed R, Johnson R, Poppe C, Khakhria R (2002) U.S. Patent No. 6,485,902. U.S. Patent and Trademark Office, Washington, DCGoogle Scholar
  105. Wilczewska AZ, Niemirowicz K, Markiewicz KH (2012) Review Nanoparticles as drug delivery systemsGoogle Scholar
  106. Wills QF, Kerrigan C, Soothill JS (2005) Experimental bacteriophage protection against Staphylococcus aureus abscesses in a rabbit model. Antimicrob Agents Chemother 49:1220–1221.  https://doi.org/10.1128/AAC.49.3.1220-1221.2005CrossRefPubMedPubMedCentralGoogle Scholar
  107. World Health Organization (2014) Antimicrobial resistance: global report on surveillance 2014. World Health Organization. doi: 9789241564748Google Scholar
  108. Yang ZQ, Tao XY, Zhang H, Rao SQ, Gao L, Pan ZM, Jiao XA (2019) Isolation and characterization of virulent phages infecting Shewanella baltica and Shewanella putrefaciens, and their application for biopreservation of chilled channel catfish (Ictalurus punctatus). Int J Food Microbiol 292:107–117.  https://doi.org/10.1016/j.ijfoodmicro.2018.12.020CrossRefPubMedGoogle Scholar
  109. Zinno P, Devirgiliis C, Ercolini D, Ongeng D, Mauriello G (2014) Bacteriophage P22 to challsenge Salmonella in foods. Int J Food Microbiol 191:69–74.  https://doi.org/10.1016/j.ijfoodmicro.2014.08.037CrossRefPubMedGoogle Scholar

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© Springer Nature Switzerland AG 2020

Authors and Affiliations

  1. 1.Center for Microbiology and Phage TherapyZewail City of Science and TechnologyGizaEgypt

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