Bacteriophage and their lysins: A new era of biocontrol for inactivation of pathogenic bacteria in poultry processing and production—A review

Achtman, 2012, Insights from genomic comparisons of genetically monomorphic bacterial pathogens, Philosophical Transactions of the Royal Society B: Biological Sciences, 367, 860, 10.1098/rstb.2011.0303 Adhikari, 2017, Effect of dietary bacteriophage supplementation on internal organs, fecal excretion, and ileal immune response in laying hens challenged by Salmonella Enteritidis, Poultry Science, 96, 3264, 10.3382/ps/pex109 Ahmadi, 2016, Prophylactic bacteriophage administration more effective than post-infection administration in reducing Salmonella enterica serovar Enteritidis shedding in quail, Frontiers in Microbiology, 7, 10.3389/fmicb.2016.01253 Akinkunmi, 2014, Pattern of pathogens from surgical wound infections in a Nigerian hospital and their antimicrobial susceptibility profiles, African Health Sciences, 14, 802, 10.4314/ahs.v14i4.5 Alarcon-Rojo, 2015, Power ultrasound in meat processing, Meat Science, 107, 86, 10.1016/j.meatsci.2015.04.015 Alexandratos, 2012 Alter, 2011, Carry-over of thermophilic Campylobacter spp. between sequential and adjacent poultry flocks, Veterinary Microbiology, 147, 90, 10.1016/j.vetmic.2010.06.005 Atterbury, 2003, Application of host-specific bacteriophages to the surface of chicken skin leads to a reduction in recovery of Campylobacter jejuni, Applied and Environmental Microbiology, 69, 6302, 10.1128/AEM.69.10.6302-6306.2003 Atterbury, 2020, Reduction of Salmonella contamination on the surface of chicken skin using bacteriophage, Virology Journal, 17, 10.1186/s12985-020-01368-0 Berchieri, 1991, The activity in the chicken alimentary tract of bacteriophages lytic for Salmonella typhimurium, Research in Microbiology, 142, 541, 10.1016/0923-2508(91)90187-F Bigwood, 2008, Phage inactivation of foodborne pathogens on cooked and raw meat, Food Microbiology, 25, 400, 10.1016/j.fm.2007.11.003 Borie, 2008, Bacteriophage treatment reduces Salmonella colonization of infected chickens, Avian Diseases, 52, 64, 10.1637/8091-082007-Reg Brabban, 2005, Evolution of foodborne pathogens via temperate bacteriophage-mediated gene transfer, Foodborne Pathogen and Disease, 2, 287, 10.1089/fpd.2005.2.287 Bruhn, 2007, Enhancing consumer acceptance of new processing technologies, Innovative Food Science & Emerging Technologies, 8, 555, 10.1016/j.ifset.2007.04.006 Carvalho, 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 Microbiology, 10, 10.1186/1471-2180-10-232 Cassar, 2019, Decontamination of chicken thigh meat by pulsed ultraviolet light, Meat and Muscle Biology, 3, 479, 10.22175/mmb2019.08.0033 Chibeu, 2013, Efficacy of bacteriophage LISTEX™ P100 combined with chemical antimicrobials in reducing Listeria monocytogenes in cooked Turkey and roast beef, International Journal of Food Microbiology, 167, 208, 10.1016/j.ijfoodmicro.2013.08.018 Cieplak, 2018, A bacteriophage cocktail targeting Escherichia coli reduces E. coli in simulated gut conditions, while preserving a non-targeted representative commensal normal microbiota, Gut Microbes, 9, 391 Clavijo, 2019, Phage cocktail SalmoFREE® reduces Salmonella on a commercial broiler farm, Poultry Science, 98, 5054, 10.3382/ps/pez251 Coburn, 2007, Salmonella, the host and disease: A brief review, Immunology & Cell Biology, 85, 112, 10.1038/sj.icb.7100007 Colom, 2015, Liposome-encapsulated bacteriophages for enhanced oral phage therapy against Salmonella spp, Applied and Environmental Microbiology, 81, 4841, 10.1128/AEM.00812-15 D'Herelle, 1917, An invisible microbe that is antagonistic to the dysentery bacillus, Comptes Rendus Academie Sciences Paris, 165, 373 Dibner, 2005, Antibiotic growth promoters in agriculture: History and mode of action, Poultry Science, 84, 634, 10.1093/ps/84.4.634 Duc, 2018, Isolation and application of bacteriophages to reduce Salmonella contamination in raw chicken meat, LWT, 91, 353, 10.1016/j.lwt.2018.01.072 El-Gohary, 2014, Environmental augmentation with bacteriophage prevents colibacillosis in broiler chickens, Poultry Science, 93, 2788, 10.3382/ps.2014-04282 El-Shibiny, 2005, Enumeration and diversity of campylobacters and bacteriophages isolated during the rearing cycles of free-range and organic chickens, Applied and Environmental Microbiology, 71, 1259, 10.1128/AEM.71.3.1259-1266.2005 El-Shibiny, 2017, Bacteriophages: The possible solution to treat infections caused by pathogenic bacteria, Canadian Journal of Microbiology, 63, 865, 10.1139/cjm-2017-0030 El-Shibiny, 2009, Application of a group II Campylobacter bacteriophage to reduce strains of Campylobacter jejuni and Campylobacter coli colonizing broiler chickens, Journal of Food Protection, 72, 733, 10.4315/0362-028X-72.4.733 Endersen, 2020, The use of bacteriophages for food safety, Current Opinion in Food Science, 36, 1, 10.1016/j.cofs.2020.10.006 Firlieyanti, 2016, Campylobacters and their bacteriophages from chicken liver: The prospect for phage biocontrol, International Journal of Food Microbiology, 237, 121, 10.1016/j.ijfoodmicro.2016.08.026 Fister, 2019, Part of the problem or the solution? Indiscriminate use of bacteriophages in the food industry can reduce their potential and impair growth-based detection methods, Trends in Food Science & Technology, 90, 170, 10.1016/j.tifs.2019.02.031 Garcia, 2008, Bacteriophages and their application in food safety, Letters in Applied Microbiology, 47, 479, 10.1111/j.1472-765X.2008.02458.x Gonçalves, 2014, Bacteriophage-induced reduction in Salmonella Enteritidis counts in the crop of broiler chickens undergoing preslaughter feed withdrawal, Poultry Science, 93, 216, 10.3382/ps.2013-03360 Goode, 2003, Reduction of experimental Salmonella and Campylobacter contamination of chicken skin by application of lytic bacteriophages, Applied and Environmental Microbiology, 69, 5032, 10.1128/AEM.69.8.5032-5036.2003 Grant, 2016, Salmonella and Campylobacter: Antimicrobial resistance and bacteriophage control in poultry, Food Microbiology, 53, 104, 10.1016/j.fm.2015.09.008 Guenther, 2012, Biocontrol of Salmonella Typhimurium in RTE foods with the virulent bacteriophage FO1-E2, International Journal of Food Microbiology, 154, 66, 10.1016/j.ijfoodmicro.2011.12.023 Guenther, 2009, Virulent bacteriophage for efficient biocontrol of Listeria monocytogenes in ready-to-eat foods, Food Microbiology, 75, 93 Guglielmi, 2017, Do bacteriophage guests protect human health?, Science, 358, 982, 10.1126/science.358.6366.982 Gutiérrez, 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, 10.1016/j.foodcont.2016.11.007 Gutiérrez, 2016, Bacteriophages as weapons against bacterial biofilms in the food industry, Frontiers in Microbiology, 7, 10.3389/fmicb.2016.00825 Hagens, 2010, Bacteriophage for biocontrol of foodborne pathogens: Calculations and considerations, Current Pharmaceutical Biotechnology, 11, 58, 10.2174/138920110790725429 Hassan, 2021, The age of phage: Friend or foe in the new dawn of therapeutic and biocontrol applications?, Pharmaceuticals, 14, 10.3390/ph14030199 Higgins, 2005, Use of a specific bacteriophage treatment to reduce Salmonella in poultry products, Poultry Science, 84, 1141, 10.1093/ps/84.7.1141 Hong, 2013, Therapeutic effects of bacteriophages against Salmonella gallinarum infection in chickens, Journal of Microbiology and Biotechnology, 23, 1478, 10.4014/jmb.1304.04067 van Houte, 2016, Evolutionary ecology of prokaryotic immune mechanisms, Microbiology and Molecular Biology Reviews, 80, 745, 10.1128/MMBR.00011-16 Huang, 2018, Isolation, characterization, and application of bacteriophage LPSE1 against Salmonella enterica in ready to eat (RTE) foods, Frontiers in Microbiology, 9, 10.3389/fmicb.2018.01046 Huang, 2021, Phages and their lysins: Toolkits in the battle against foodborne pathogens in the postantibiotic era, Comprehensive Reviews in Food Science and Food Safety, 20, 3319, 10.1111/1541-4337.12757 Hudson, 2005, Bacteriophages as biocontrol agents in food, Journal of Food Protection, 68, 426, 10.4315/0362-028X-68.2.426 Hung, 2009, Emerging concepts of biofilms in infectious diseases, Missouri Medicine, 106, 292 Hyman, 2010, Bacteriophage host range and bacterial resistance, Advances in Applied Microbiology, 70, 217, 10.1016/S0065-2164(10)70007-1 Kang, 2013, Wksl3, a new biocontrol agent for Salmonella enterica serovars enteritidis and typhimurium in foods: Characterization, application, sequence analysis, and oral acute toxicity study, Applied and Environmental Microbiology, 79, 1956, 10.1128/AEM.02793-12 Kimminau, 2020, Bacteriophage in-feed application: A novel approach to preventing Salmonella enteritidis colonization in chicks fed experimentally contaminated feed, The Journal of Applied Poultry Research, 29, 930, 10.1016/j.japr.2020.09.003 Kittler, 2013, Effect of bacteriophage application on Campylobacter jejuni loads in commercial broiler flocks, Applied and Environmental Microbiology, 79, 7525, 10.1128/AEM.02703-13 Kortright, 2019, Phage therapy: A renewed approach to combat antibiotic-resistant bacteria, Cell Host & Microbe, 25, 219, 10.1016/j.chom.2019.01.014 Kutter, 2010, Phage therapy in clinical practice: Treatment of human infections, Current Pharmaceutical Biotechnology, 11, 69, 10.2174/138920110790725401 Lenski, 1988, Dynamics of interactions between bacteria and virulent bacteriophage, Advances in Microbial Ecology, 10, 1, 10.1007/978-1-4684-5409-3_1 Leung, 2018, Effect of storage temperature on the stability of spray dried bacteriophage powders, European Journal of Pharmaceutics and Biopharmaceutics, 127, 213, 10.1016/j.ejpb.2018.02.033 Li, 2020, Broad-host-range Salmonella bacteriophage STP4-a and its potential application evaluation in poultry industry, Poultry Science, 99, 3643, 10.1016/j.psj.2020.03.051 Lim, 2012, Use of bacteriophage for biological control of Salmonella Enteritidis infection in chicken, Research in Veterinary Science, 93, 1173, 10.1016/j.rvsc.2012.06.004 Lim, 2010, Evaluation of efficacy of bacteriophage CJø07 against Salmonella enteritidis infection in the SPF chicks, Korean Journal of Poultry Science, 37, 283, 10.5536/KJPS.2010.37.3.283 Lim, 2011, Efficacy of bacteriophage therapy on horizontal transmission of Salmonella Gallinarum on commercial layer chickens, Avian Diseases, 55, 435, 10.1637/9599-111210-Reg.1 Luong, 2020, Phage therapy in the resistance era: Where do we stand and where are we going?, Clinical Therapeutics, 42, 1659, 10.1016/j.clinthera.2020.07.014 Ly-Chatain, 2014, The factors affecting effectiveness of treatment in phages therapy, Frontiers in Microbiology, 5, 10.3389/fmicb.2014.00051 Merril, 2003, The prospect for bacteriophage therapy in Western medicine, Nature Reviews Drug Discovery, 2, 489, 10.1038/nrd1111 Milho, 2019, Escherichia coli and Salmonella enteritidis dual-species biofilms: Interspecies interactions and antibiofilm efficacy of phages, Scientific Reports, 9, 10.1038/s41598-019-54847-y Miller, 2010, Bacteriophage therapy for control of necrotic enteritis of broiler chickens experimentally infected with Clostridium perfringens, Avian Diseases, 54, 33, 10.1637/8953-060509-Reg.1 Moye, 2018, Bacteriophage applications for food production and processing, Viruses, 10, 10.3390/v10040205 Nabil, 2018, Assessing the impact of bacteriophages in the treatment of Salmonella in broiler chickens, Infection Ecology & Epidemiology, 8, 10.1080/20008686.2018.1539056 2016 2016 Oh, 2017, Recent trends in Salmonella outbreaks and emerging technology for biocontrol of Salmonella using phages in foods: A review, Journal of Microbiology and Biotechnology, 27, 2075, 10.4014/jmb.1710.10049 Oliveira, 2010, In vivo efficiency evaluation of a phage cocktail in controlling severe colibacillosis in confined conditions and experimental poultry houses, Veterinary Microbiology, 146, 303, 10.1016/j.vetmic.2010.05.015 de Ornellas Dutka Garcia, 2017, Bacteriophage use to control Salmonella biofilm on surfaces present in chicken slaughterhouses, Poultry Science, 96, 3392, 10.3382/ps/pex124 Orquera, 2012, Control of Campylobacter spp. and Yersinia enterocolitica by virulent bacteriophages, Journal of Molecular and Genetic Medicine, 6, 273, 10.4172/1747-0862.1000049 Pearson, 2013, Phage-bacterium war on polymeric surfaces: Can surface-anchored bacteriophages eliminate microbial infections?, Biomacromolecules, 14, 1257, 10.1021/bm400290u Perera, 2015, Bacteriophage cocktail significantly reduces or eliminates Listeria monocytogenes contamination on lettuce, apples, cheese, smoked salmon and frozen foods, Food Microbiology, 52, 42, 10.1016/j.fm.2015.06.006 Pulido, 2016, Application of bacteriophages in post-harvest control of human pathogenic and food spoiling bacteria, Critical Reviews in Biotechnology, 36, 851, 10.3109/07388551.2015.1049935 Richards, 2019, Phage biocontrol of Campylobacter jejuni in chickens does not produce collateral effects on the gut microbiota, Frontiers in Microbiology, 10, 10.3389/fmicb.2019.00476 Ricke, 2005, Alternatives to antibiotics: Chemical and physical antimicrobial interventions and foodborne pathogen response, Poultry Science, 84, 667, 10.1093/ps/84.4.667 Shabbir, 2016, Bacteria vs. bacteriophages: Parallel evolution of immune arsenals, Frontiers in Microbiology, 7, 1292, 10.3389/fmicb.2016.01292 Sillankorva, 2012, Bacteriophages and their role in food safety, International Journal of Microbiology, 10.1155/2012/863945 Siringan, 2011, Bacteriophage-mediated dispersal of Campylobacter jejuni biofilms, Applied and Environmental Microbiology, 77, 3320, 10.1128/AEM.02704-10 Skarp, 2016, Campylobacteriosis: The role of poultry meat, Clinical Microbiology and Infection, 22, 103, 10.1016/j.cmi.2015.11.019 Soffer, 2017, Bacteriophage preparation lytic for Shigella significantly reduces Shigella sonnei contamination in various foods, PLoS One, 12, 10.1371/journal.pone.0175256 Sommer, 2019, Don't shut the stable door after the phage has bolted—the importance of bacteriophage inactivation in food environments, Viruses, 11, 10.3390/v11050468 Spricigo, 2013, Use of a bacteriophage cocktail to control Salmonella in food and the food industry, International Journal of Food Microbiology, 165, 169, 10.1016/j.ijfoodmicro.2013.05.009 Sukumaran, 2015, Reduction of Salmonella on chicken meat and chicken skin by combined or sequential application of lytic bacteriophage with chemical antimicrobials, International Journal of Food Microbiology, 207, 8, 10.1016/j.ijfoodmicro.2015.04.025 Sukumaran, 2016, Reduction of Salmonella on chicken breast fillets stored under aerobic or modified atmosphere packaging by the application of lytic bacteriophage preparation SalmoFresh, Poultry Science, 95, 668, 10.3382/ps/pev332 Sulakvelidze, 2001, Bacteriophage therapy, Antimicrobial Agents and Chemotherapy, 45, 649, 10.1128/AAC.45.3.649-659.2001 Tawakol, 2019, Evaluation of bacteriophage efficacy in reducing the impact of single and mixed infections with Escherichia coli and infectious bronchitis in chickens, Infection Ecology & Epidemiology, 9, 10.1080/20008686.2019.1686822 Threlfall, 2000, The emergence and spread of antibiotic resistance in food-borne bacteria, International Journal of Food Microbiology, 62, 1, 10.1016/S0168-1605(00)00351-2 Thung, 2020, Partial characterization and in vitro evaluation of a lytic bacteriophage for biocontrol of Campylobacter jejuni in mutton and chicken meat, Journal of Food Safety, 40, 10.1111/jfs.12770 Torres‐Acosta, 2019, Economic evaluation of the development of a phage therapy product for the control of Salmonella in poultry, Biotechnology Progress, 35, 10.1002/btpr.2852 Twort, 1915, An investigation on the nature of ultra-microscopic viruses, The Lancet, 186, 1241, 10.1016/S0140-6736(01)20383-3 2019 Vaz, 2020, Effect of time of therapy with wild-type lytic bacteriophages on the reduction of Salmonella Enteritidis in broiler chickens, Veterinary Microbiology, 240, 10.1016/j.vetmic.2019.108527 Vikram, 2021, Phage biocontrol applications in food production and processing, Current Issues in Molecular Biology, 40, 267, 10.21775/cimb.040.267 Vongkamjan, 2013, Persistent Listeria monocytogenes subtypes isolated from a smoked fish processing facility included both phage susceptible and resistant isolates, Food Microbiology, 35, 38, 10.1016/j.fm.2013.02.012 Wagenaar, 2005, Phage therapy reduces Campylobacter jejuni colonization in broilers, Veterinary Microbiology, 109, 275, 10.1016/j.vetmic.2005.06.002 Waseh, 2010, Orally administered P22 phage tailspike protein reduces Salmonella colonization in chickens: Prospects of a novel therapy against bacterial infections, PLoS One, 5, 10.1371/journal.pone.0013904 Whichard, 2003, Suppression of Salmonella growth by wild-type and large-plaque variants of bacteriophage Felix O1 in liquid culture and on chicken frankfurters, Journal of Food Protection, 66, 220, 10.4315/0362-028X-66.2.220 2014 Wittebole, 2014, A historical overview of bacteriophage therapy as an alternative to antibiotics for the treatment of bacterial pathogens, Virulence, 5, 226, 10.4161/viru.25991 Wójcik, 2020, Comprehensive evaluation of the safety and efficacy of BAFASAL® bacteriophage preparation for the reduction of Salmonella in the food chain, Viruses, 12, 10.3390/v12070742 Wong, 2014, Evaluation of a lytic bacteriophage, Φ st1, for biocontrol of Salmonella enterica serovar Typhimurium in chickens, International Journal of Food Microbiology, 172, 92, 10.1016/j.ijfoodmicro.2013.11.034 Xu, 2021, Phage and phage lysins: New era of bio-preservatives and food safety agents, Journal of Food Science, 86, 3349, 10.1111/1750-3841.15843 Yang, 2017, Treatment with lauric arginate ethyl ester and commercial bacteriophage, alone or in combination, inhibits Listeria monocytogenes in chicken breast tissue, Food Control, 78, 57, 10.1016/j.foodcont.2017.02.021 Yeh, 2018, Effect of ultraviolet light, organic acids, and bacteriophage on Salmonella populations in ground beef, Meat Science, 139, 44, 10.1016/j.meatsci.2018.01.007 Yeh, 2017, Bacteriophage application on red meats and poultry: Effects on Salmonella population in final ground products, Meat Science, 127, 30, 10.1016/j.meatsci.2017.01.001 Zinno, 2014, Bacteriophage P22 to challenge Salmonella in foods, International Journal of Food Microbiology, 191, 69, 10.1016/j.ijfoodmicro.2014.08.037