A mini-review on the role of bacteriophages in food safety

References

• Ali, Y., Inusa, I., Sanghvi, G., Mandaliya, V. B., & Bishoyi, A. K. (2023). The current status of phage therapy and its advancement towards establishing standard antimicrobials for combating multi drug-resistant bacterial pathogens. Microbial Pathogenesis, 181, 106199. https://doi.org/10.1016/j.micpath.2023.106199
   PubMed Web of Science ®Google Scholar
• Batinovic, S., Wassef, F., Knowler, S. A., Rice, D. T., Stanton, C. R., Rose, J., Tucci, J., Nittami, T., Vinh, A., Drummond, G. R., Sobey, C. G., Chan, H. T., Seviour, R. J., Petrovski, S., & Franks, A. E. (2019). Bacteriophages in natural and artificial environments. Pathogens, 8(3), 100. https://doi.org/10.3390/pathogens8030100
   PubMed Web of Science ®Google Scholar
• Bhardwaj, N., Bhardwaj, S. K., Deep, A., Dahiya, S., & Kapoor, S. (2015). Lytic bacteriophages as biocontrol agents of foodborne pathogens. Asian Journal of Animal and Veterinary Advances, 10(11), 708–7. https://doi.org/10.3923/ajava.2015.708.723
   Google Scholar
• Bigwood, T., Hudson, J. A., Billington, C., Carey-Smith, G. V., & Heinemann, J. A. (2008). Phage inactivation of foodborne pathogens on cooked and raw meat. Food Microbiology, 25(2), 400–406. https://doi.org/10.1016/j.fm.2007.11.003
   PubMed Web of Science ®Google Scholar
• Braga, L. P., Spor, A., Kot, W., Breuil, M.-C., Hansen, L. H., Setubal, J. C., & Philippot, L. (2020). Impact of phages on soil bacterial communities and nitrogen availability under different assembly scenarios. Microbiome, 8(1), 1–14. https://doi.org/10.1186/s40168-020-00822-z
   PubMed Web of Science ®Google Scholar
• Carter, C. D., Parks, A., Abuladze, T., Li, M., Woolston, J., Magnone, J., Senecal, A., Kropinski, A. M., & Sulakvelidze, A. (2012). Bacteriophage cocktail significantly reduces Escherichia coli O157: H7 contamination of lettuce and beef, but does not protect against recontamination. Bacteriophage, 2(3), 178–185. https://doi.org/10.4161/bact.22825
   PubMedGoogle Scholar
• Chibeu, A., Agius, L., Gao, A., Sabour, P. M., Kropinski, A. M., & Balamurugan, S. (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(2), 208–214. https://doi.org/10.1016/j.ijfoodmicro.2013.08.018
   PubMed Web of Science ®Google Scholar
• Culot, A., Grosset, N., & Gautier, M. (2019). Overcoming the challenges of phage therapy for industrial aquaculture: A review. Aquaculture, 513, 734423. https://doi.org/10.1016/j.aquaculture.2019.734423
   Web of Science ®Google Scholar
• Ding, Y., Nan, Y., Qiu, Y., Niu, D., Stanford, K., Holley, R., Narváez‐Bravo, C., & McAllister, T. (2023). Use of a phage cocktail to reduce the numbers of seven Escherichia coli strains belonging to different STEC serogroups applied to fresh produce and seeds. Journal of Food Safety, 43(4), e13044. https://doi.org/10.1111/jfs.13044
   Web of Science ®Google Scholar
• Duc, H. M., Son, H. M., Yi, H. P. S., Sato, J., Ngan, P. H., Masuda, Y., Honjoh, K.-I., & Miyamoto, T. (2020). Isolation, characterization and application of a polyvalent phage capable of controlling Salmonella and Escherichia coli O157: H7 in different food matrices. Food Research International, 131, 108977. https://doi.org/10.1016/j.foodres.2020.108977
   PubMed Web of Science ®Google Scholar
• Fan, X., Niemira, B. A., Doona, C. J., Feeherry, F. E., & Gravani, R. B. (2009). Microbial safety of fresh produce (Vol. 41). John Wiley & Sons.
   Google Scholar
• Firlieyanti, A. S., Connerton, P. L., & Connerton, I. F. (2016). Campylobacters and their bacteriophages from chicken liver: The prospect for phage biocontrol. International Journal of Food Microbiology, 237, 121–127. https://doi.org/10.1016/j.ijfoodmicro.2016.08.026
   PubMed Web of Science ®Google Scholar
• Fruciano, D. E., & Bourne, S. (2006). Phage as an antimicrobial agent: D’Herelle’s heretical theories and their role in the decline of phage prophylaxis in the west. The Canadian Journal of Infectious Diseases & Medical Microbiology, 18(1), 19–26. https://doi.org/10.1155/2007/976850
   Web of Science ®Google Scholar
• Garvey, M. (2020). Bacteriophages and the one health approach to combat multidrug resistance: Is this the way? Antibiotics, 9(7), 414. https://doi.org/10.3390/antibiotics9070414
   Google Scholar
• Garvey, M. (2022). Bacteriophages and food production: Biocontrol and bio-preservation options for food safety. Antibiotics, 11(10), 1324. https://doi.org/10.3390/antibiotics11101324
   Google Scholar
• Gencay, Y. E., Ayaz, N. D., Copuroglu, G., & Erol, I. (2016). Biocontrol of Shiga toxigenic Escherichia coli O157: H7 in Turkish raw meatball by bacteriophage. Journal of Food Safety, 36(1), 120–131. https://doi.org/10.1111/jfs.12219
   Web of Science ®Google Scholar
• Giau, V. V., Lee, H., An, S. S. A., & Hulme, J. (2019). Recent advances in the treatment of C. Difficile using biotherapeutic agents. 12, 1597–1615. https://doi.org/10.2147/IDR.S207572
   Google Scholar
• Greer, G. G. (2005). Bacteriophage control of foodborne bacteria. Journal of Food Protection, 68(5), 1102–1111. https://doi.org/10.4315/0362-028X-68.5.1102
   PubMed Web of Science ®Google Scholar
• Imran, A., Shehzadi, U., Islam, F., Afzaal, M., Ali, R., Ali, Y. A., Chauhan, A., Biswas, S., Khurshid, S., Usman, I., Hussain, G., Zahra, S. M., Shah, M. A., & Rasool, A. (2023). Bacteriophages and food safety: An updated overview. Food Science & Nutrition, 11(7), 3621–3630. https://doi.org/10.1002/fsn3.3360
   PubMed Web of Science ®Google Scholar
• Ishaq, A., Ebner, P. D., Syed, Q. A., & Ur Rahman, H. U. (2020). Employing list-shield bacteriophage as a bio-control intervention for Listeria monocytogenes from raw beef surface and maintain meat quality during refrigeration storage. LWT- Food Science Technology, 132, 109784. https://doi.org/10.1016/j.lwt.2020.109784
   Web of Science ®Google Scholar
• Islam, F., Saeed, F., Afzaal, M., Ahmad, A., Hussain, M., Khalid, M. A., Saewan, S. A., & Khashroum, A. O. (2022). Applications of green technologies-based approaches for food safety enhancement: A comprehensive review. Food Science & Nutrition, 10(9), 2855–2867. https://doi.org/10.1002/fsn3.2915
   PubMed Web of Science ®Google Scholar
• Lawpidet, P., Tengjaroenkul, B., Saksangawong, C., & Sukon, P. (2021). Global prevalence of vancomycin-resistant enterococci in food of animal origin: A meta-analysis. Foodborne Pathogens and Disease, 18(6), 405–412. https://doi.org/10.1089/fpd.2020.2892
   PubMed Web of Science ®Google Scholar
• Liu, S., Lu, H., Zhang, S., Shi, Y., & Chen, Q. (2022). Phages against pathogenic bacterial biofilms and biofilm-based infections: A review. Pharmaceutics, 14(2), 427. https://doi.org/10.3390/pharmaceutics14020427
   PubMed Web of Science ®Google Scholar
• Lu, Y. T., Ma, Y., Wong, C. W., & Wang, S. (2022). Characterization and application of bacteriophages for the biocontrol of Shiga-toxin producing Escherichia coli in romaine lettuce. Food Control, 140, 109109. https://doi.org/10.1016/j.foodcont.2022.109109
   Web of Science ®Google Scholar
• Mahajan, P. V., Caleb, O. J., Singh, Z., Watkins, C. B., & Geyer, M. (2014). Postharvest treatments of fresh produce. Philosophical Transactions Series A, Mathematical, Physical, and Engineering Sciences, 372(2017), 20130309. https://doi.org/10.1098/rsta.2013.0309
   PubMed Web of Science ®Google Scholar
• McCallin, S., Sarker, S. A., Barretto, C., Sultana, S., Berger, B., Huq, S., Krause, L., Bibiloni, R., Schmitt, B., Reuteler, G., & Reuteler, G. (2013). Safety analysis of a Russian phage cocktail: From MetaGenomic analysis to oral application in healthy human subjects. Virology, 443(2), 187–196. https://doi.org/10.1016/j.virol.2013.05.022
   PubMed Web of Science ®Google Scholar
• Moye, Z. D., Woolston, J., & Sulakvelidze, A. (2018). Bacteriophage applications for food production and processing. Viruses, 10(4), 205. https://doi.org/10.3390/v10040205
   PubMed Web of Science ®Google Scholar
• Murray, K., Wu, F., Shi, J., Jun Xue, S., & Warriner, K. (2017). Challenges in the microbiological food safety of fresh produce: Limitations of post-harvest washing and the need for alternative interventions. Food Quality and Safety, 1(4), 289–301. https://doi.org/10.1093/fqsafe/fyx027
   Web of Science ®Google Scholar
• Orquera, S., Gölz, G., Hertwig, S., Hammerl, J., Sparborth, D., Joldic, A., & Alter, T. (2012). Control of Campylobacter spp. And Yersinia enterocolitica by virulent bacteriophages. Journal of Molecular and Genetic Medicine: An International Journal of Biomedical Research, 6(1), 273. https://doi.org/10.4172/1747-0862.1000049
   PubMedGoogle Scholar
• O’Sullivan, L., Bolton, D., McAuliffe, O., & Coffey, A. (2019). Bacteriophages in food applications: From foe to friend. Annual Review of Food Science and Technology, 10(1), 151–172. https://doi.org/10.1146/annurev-food-032818-121747
   PubMedGoogle Scholar
• Ranveer, S. A., Dasriya, V., Ahmad, M. F., Dhillon, H. S., Samtiya, M., Shama, E., Anand, T., Dhewa, T., Chaudhary, V., Chaudhary, P., Behare, P., Ram, C., Puniya, D. V., Khedkar, G. D., Raposo, A., Han, H., & Puniya, A. K. (2024). Positive and negative aspects of bacteriophages and their immense role in the food chain. Npj Science of Food, 8(1), 1–13. https://doi.org/10.1038/s41538-023-00245-8
   PubMedGoogle Scholar
• Rashida, H., Sean, B., Douglas, N., Carlota, M., Alida, S., Jessica, L., Rotstein, D., Schlater, L., Freiman, J., Douris, A., Simmons, M., Donovan, D., Henderson, J., Tewell, M., Snyder, K., Oni, O., Von Stein, D., Dassie, K. … Gieraltowski, L. (2019). Multistate outbreak of salmonella infections linked to raw turkey products — United States, 2017–2019. MMWR Morbidity & Mortality Weekly, 68(46), 1045–1049. https://doi.org/10.15585/mmwr.mm6846a1
   PubMed Web of Science ®Google Scholar
• Rawat, S. (2015). Food spoilage: Microorganisms and their prevention. Asian Journal of Plant Science and Research, 5(4), 47–56.
   Google Scholar
• Romero-Calle, D., Guimarães Benevides, R., Góes-Neto, A., & Billington, C. J. A. (2019). Bacteriophages as alternatives to antibiotics in clinical care. Antibiotics (Basel), 8(3), 138. https://doi.org/10.3390/antibiotics8030138
   PubMed Web of Science ®Google Scholar
• Sadekuzzaman, M., Mizan, M. F. R., Yang, S., Kim, H. S., & Ha, S. D. (2018). Application of bacteriophages for the inactivation of Salmonella spp. In biofilms. Food Science and Technology International, 24(5), 424–433. https://doi.org/10.1177/1082013218763424
   PubMed Web of Science ®Google Scholar
• Salmond, G. P., & Fineran, P. C. (2015). A century of the phage: Past, present and future. Nature Reviews Microbiology, 13(12), 777–786. https://doi.org/10.1038/nrmicro3564
   PubMed Web of Science ®Google Scholar
• Sarno, E., Pezzutto, D., Rossi, M., Liebana, E., & Rizzi, V. (2021). A review of significant European foodborne outbreaks in the last decade. Journal of Food Protection, 84(12), 2059–2070. https://doi.org/10.4315/JFP-21-096
   PubMed Web of Science ®Google Scholar
• Scallan, E., Hoekstra, R. M., Angulo, F. J., Tauxe, R. V., Widdowson, A., Roy, S. L., Jones, J. L., & Griffin, P. M. (2010). Foodborne illness acquired in the United States—major pathogens. Emerging Infectious Diseases, 17(1), 7–15. https://doi.org/10.3201/eid1701.P11101
   Web of Science ®Google Scholar
• Selle, K., Fletcher, J. R., Tuson, H., Schmitt, D. S., McMillan, L., Vridhambal, G. S., Rivera, A. J., Montgomery, S. A., Fortier, C., Barrangou, R., Theriot, C. M., Ousterout, D. G., & Ballard, J. D. (2020). In vivo targeting of clostridioides difficile using phage-delivered CRISPR-Cas3 antimicrobials. MBio, 11(2). https://doi.org/10.1128/mBio.00019-20
   PubMed Web of Science ®Google Scholar
• Shebs-Maurine, E. L., Giotto, F. M., Laidler, S. T., & de Mello, A. S. (2021). Effects of bacteriophages and peroxyacetic acid applications on beef contaminated with Salmonella during different grinding stages. Meat Science, 173, 108407. https://doi.org/10.1016/j.meatsci.2020.108407
   PubMed Web of Science ®Google Scholar
• Sillankorva, S. M., Oliveira, H., & Azeredo, J. (2012). Bacteriophages and their role in food safety. International Journal of Microbiology, 2012, 1–13. https://doi.org/10.1155/2012/863945
   Google Scholar
• Sisakhtpour, B., Mirzaei, A., Karbasizadeh, V., Hosseini, N., Shabani, M., & Moghim, S. (2022). The characteristic and potential therapeutic effect of isolated multidrug-resistant Acinetobacter baumannii lytic phage. Annals of Clinical Microbiology and Antimicrobials, 21(1), 1–11. https://doi.org/10.1186/s12941-022-00492-9
   PubMed Web of Science ®Google Scholar
• Sukumaran, A. T., Nannapaneni, R., Kiess, A., & Sharma, C. S. (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, 8–15. https://doi.org/10.1016/j.ijfoodmicro.2015.04.025
   PubMed Web of Science ®Google Scholar
• Tang, S., Biswas, S. K., Tan, W. S., Saha, A. K., & Leo, F. (2019). Efficacy and potential of phage therapy against multidrug resistant shigella spp. PeerJ, 7, 7. https://doi.org/10.7717/peerj.6225
   Web of Science ®Google Scholar
• Thanki, A. M., Hooton, S., Gigante, A. M., Atterbury, R. J., & Clokie, M. R. (2021). Potential roles for bacteriophages in reducing Salmonella from poultry and swine. Salmonella spp-a global challenge, IntechOpen.
   Google Scholar
• Vikram, A., Woolston, J., & Sulakvelidze, A. (2021). Phage biocontrol applications in food production and processing. Current Issues in Molecular Biology, 40(1), 267–302. https://doi.org/10.21775/cimb.040.267
   PubMedGoogle Scholar
• Villa, T. G., Feijoo-Siota, L., Rama, J. R., Sánchez-Pérez, A., & Viñas, M. (2019). Horizontal gene transfer between bacteriophages and bacteria: Antibiotic resistances and toxin production. Horizontal Gene Transfer: Breaking Borders Between Living Kingdoms, 97–142 https://link.springer.com/chapter/10.1007/978-3-030-21862-1_3.
   Google Scholar
• Wittebole, X., De Roock, S., & Opal, S. M. (2014). A historical overview of bacteriophage therapy as an alternative to antibiotics for the treatment of bacterial pathogens. Virulence, 5(1), 226–235. https://doi.org/10.4161/viru.25991
   PubMed Web of Science ®Google Scholar
• Witte, S., Huijboom, L., Klamert, S., van de Straat, L., Hagens, S., Fieseler, L., de Vegt, B. T., & van Mierlo, J. T. (2022). Application of bacteriophages EP75 and EP335 efficiently reduces viable cell counts of Escherichia coli O157 on beef and vegetables. Food Microbiology, 104, 103978. https://doi.org/10.1016/j.fm.2022.103978
   PubMed Web of Science ®Google Scholar
• Woźnica, W. M., Bigos, J., & Łobocka, M. B. (2015). Liza komórek bakteryjnych w procesie uwalniania bakteriofagów–kanoniczne i nowo poznane mechanizmy. Postępy Higieny i Medycyny Doświadczalnej, 69, 114–126.
   Google Scholar
• Yang, S., Sadekuzzaman, M., & Ha, S. D. (2017). Reduction of Listeria monocytogenes on chicken breasts by combined treatment with UV-C light and bacteriophage ListShield. Lwt, 86, 193–200. https://doi.org/10.1016/j.lwt.2017.07.060
   Web of Science ®Google Scholar
• Yeh, Y., Purushothaman, P., Gupta, N., Ragnone, M., Verma, S. C., & De Mello, A. S. (2017). Bacteriophage application on red meats and poultry: Effects on Salmonella population in final ground products. Meat Science, 127, 30–34. https://doi.org/10.1016/j.meatsci.2017.01.001
   PubMed Web of Science ®Google Scholar
• Yu, H., Elbediwi, M., Zhou, X., Shuai, H., Lou, X., Wang, H., Li, Y., & Yue, M. (2020). Epidemiological and genomic characterization of campylobacter jejuni isolates from a foodborne outbreak at Hangzhou, China. International Journal of Molecular Sciences, 21(8), 3001. https://doi.org/10.3390/ijms21083001
   PubMed Web of Science ®Google Scholar
• Żaczek, M., Weber-Dąbrowska, B., & Górski, A. (2015). Phages in the global fruit and vegetable industry. Journal of Applied Microbiology, 118(3), 537–556. https://doi.org/10.1111/jam.12700
   PubMed Web of Science ®Google Scholar
• Zampara, A., Sørensen, M. C. H., Elsser-Gravesen, A., & Brøndsted, L. (2017). Significance of phage-host interactions for biocontrol of campylobacter jejuni in food. Food Control, 73, 1169–1175. https://doi.org/10.1016/j.foodcont.2016.10.033
   Web of Science ®Google Scholar
• Zeng, D., Zhang, X., Xue, F., Wang, Y., Jiang, L., & Jiang, Y. (2016). Phenotypic characters and molecular epidemiology of Campylobacter jejuni in East China. Journal of Food Science, 81(1), M106–M113. https://doi.org/10.1111/1750-3841.13146
   PubMed Web of Science ®Google Scholar
• Zhang, X., Niu, Y. D., Nan, Y., Stanford, K., Holley, R., McAllister, T., & Narváez-Bravo, C. (2019). SalmoFresh™ effectiveness in controlling Salmonella on romaine lettuce, mung bean sprouts and seeds. International Journal of Food Microbiology, 305, 108250. https://doi.org/10.1016/j.ijfoodmicro.2019.108250
   PubMed Web of Science ®Google Scholar
• Zhou, C., Zhu, M., Wang, Y., Yang, Z., Ye, M., Wu, L., Bao, H., Pang, M., Zhou, Y., Wang, R., Sun, L., Wang, H., Zheng, C., & Zhang, H. (2020). Broad host range phage vB-LmoM-SH3-3 reduces the risk of Listeria contamination in two types of ready-to-eat food. Food Control, 108, 106830. https://doi.org/10.1016/j.foodcont.2019.106830
   Web of Science ®Google Scholar