Isolation and application of bacteriophages as an antimicrobial alternative against beef-borne pathogens
Keywords:
Bacteriophages, Antimicrobials, Escherichia coli, Salmonella entericaAbstract
Meat products are widely consumed worldwide. During their production chain, they can be contaminated by pathogens such as Salmonella enterica subsp. enterica serovar Typhimurium and Escherichia coli, which cause serious and, in some cases, fatal infections. The limitations of conventional disinfection methods, together with the increasing resistance to antibiotics, underline the need for effective and economical alternatives. In this context, the use of phages as antimicrobial agents emerges as a promising solution. In this study, phages specific against strains of E. coli (ATCC 25922, 15597, 35401, O157:H7 ATCC 43888) and Salmonella Typhimurium (ATCC 13311) were obtained from water samples from a local wastewater treatment plant. Nineteen bacteriophages were isolated for E. coli strains, of which the E. coli strain ATCC 25922 showed higher susceptibility to the action of phages present in the water samples, while the strain ATCC 43888 showed high resistance. In the case of S. Typhimurium, only one phage (φ101) was isolated and evaluated against 30 clinical isolates of Salmonella spp., in which it showed lytic activity in 16. This same phage was used to reduce the bacterial load on a stainless-steel surface contaminated by S. Typhimurium, achieving a significant decrease after 24 hours. The results of this study highlight the potential antimicrobial activity of bacteriophages against antibiotic-susceptible and antibiotic-resistant strains, as well as their use as surface disinfectants. These findings suggest that the use of phages could represent an effective alternative for the treatment of pathogens transmitted by meat products.
References
1. SADER. Secretaria de Agricultura y Desarrollo Rural. (2022). Escenario mensual de productos agroalimentarios. Servicio de Informacion Agroalimentaria Y Pesquera. Mexico. https://www.gob.mx/siap/prensa/reporte-mensual-de-escenarios-de-13-productos-agroalimentarios?idiom=es
2. CDC. Centers for Disease Control and Prevention. (2023). Foodborne Germs and Illnesses. National Center for Emerging and Zoonotic Infectious Diseases (NCEZID), Division of Foodborne, Waterborne, and Environmental Diseases (DFWED). https://www.cdc.gov/ncezid/divisions-offices/about-dfwed.html
3. Cruz-Galvez, A. M., Gómez-Aldapa, C. A., Villagómez-Ibarra, J. R., Chavarría-Hernández, N., Rodríguez-Baños, J., Rangel-Vargas, E., & Castro-Rosas, J. (2013). Antibacterial effect against foodborne bacteria of plants used in traditional medicine in central Mexico: Studies in vitro and in raw beef. Food Control ;32(1):289-295. DOI: https://doi.org/10.1016/j.foodcont.2012.12.018
4. Stanley, P. L., Winslow, T. A. & Pillay, I. (2017). Detection of Presumptive Pathogens in Ground Beef from Supermarket and Farmers’ Market Sources. Georgia Journal of Science 2017;75(2):2. https://digitalcommons.gaacademy.org/gjs/vol75/iss2/2
5. Obaidat, M. M. (2020). Prevalence and antimicrobial resistance of Listeria monocytogenes, Salmonella enterica and Escherichia coli O157: H7 in imported beef cattle in Jordan. Comparative Immunology, Microbiology and Infectious Diseases, 70:101447. DOI: https://doi.org/10.1016/j.cimid.2020.101447
6. Garza-García, J. A. D. L., Rubio Lozano, M. S., Wacher-Rodarte, M. D. C., Navarro Ocaña, A., Hernández-Castro, R., Xicohtencatl-Cortes, J., & Delgado Suárez, E. J. (2020). Frecuencia de contaminación y de serotipos de Salmonella enterica y Escherichia coli en una operación integrada de matanza y deshuese de bovinos. Revista mexicana de ciencias pecuarias. 11(4):971-990. DOI: https://doi.org/10.22319/rmcp.v11i4.5111
7. Delgado-Suárez, E. J., Palós-Guitérrez, T., Ruíz-López, F. A., Hernández Pérez, C. F., Ballesteros-Nova, N. E., Soberanis-Ramos, O., Méndez-Medina, R. D., Allard, M. W., & Rubio-Lozano, M. S. (2021). Genomic surveillance of antimicrobial resistance shows cattle and poultry are a moderate source of multi-drug resistant non-typhoidal Salmonella in Mexico. PLoS One. 16(5):e0243681. DOI: https://doi.org/10.1371/journal.pone.0243681
8. WHO. World Health Organization. (2023). Estimates of the global burden of foodborne diseases. Foodborne disease burden epidemiology reference group 2007-2015. https://www.who.int/publications/i/item/9789241565165
9. Geletu, U. S., Usmael, M. A., & Ibrahim, A. M. (2022). Isolation, identification, and susceptibility profile of E. coli, Salmonella, and S. aureus in dairy farm and their public health implication in Central Ethiopia. Veterinary Medicine International. 2022(1), 1887977. https://doi.org/10.1155/2022/1887977
10. Richardson, S. D. (2003). Disinfection by-products and other emerging contaminants in drinking water. TrAC Trends in Analytical Chemistry. 22(10):666-684. DOI: https://doi.org/10.1016/S0165-9936(03)01003-3
11. Ahn, D. U., & Lee, E. J. (2012). Mechanisms and prevention of quality changes in meat by irradiation. Food irradiation research and technology. 58:209-226. DOI: https://doi.org/10.1002/9781118422557.ch12
12. Chen, J. H., Ren, Y., Seow, J., Liu, T., Bang, W. S., & Yuk, H. G. (2012). Intervention technologies for ensuring microbiological safety of meat: current and future trends. Comprehensive Reviews in Food Science and Food Safety. 11(2):119-132. DOI: https://doi.org/10.1111/j.1541-4337.2011.00177.x
13. Maherani, B., Hossain, F., Criado, P., Ben-Fadhel, Y., Salmieri, S., & Lacroix, M. (2016). World market development and consumer acceptance of irradiation technology. Foods. 5(4):79. DOI: https://doi.org/10.3390/foods5040079
14. Mittendorfer, J. (2016). Food irradiation facilities: Requirements and technical aspects. Radiation Physics and Chemistry. 129:61-63. DOI: https://doi.org/10.1016/j.radphyschem.2016.08.007
15. Pereira, C., Costa, P., Duarte, J., Balcão, V. M., & Almeida, A. (2021). Phage therapy as a potential approach in the biocontrol of pathogenic bacteria associated with shellfish consumption. International Journal of Food Microbiology. 338:108995. DOI: https://doi.org/10.1016/j.ijfoodmicro.2020.108995
16. Minh, D. H., Minh, S. H., Honjoh, K. I., & Miyamoto, T. (2016). Isolation and biocontrol of Extended Spectrum Beta-Lactamase (ESBL)-producing Escherichia coli contamination in raw chicken meat by using lytic bacteriophages. LWT-Food Science and Technology, 71:339-346. DOI: https://doi.org/10.1016/j.lwt.2016.04.013
17. Jamalludeen, N., Johnson, R. P., Friendship, R., Kropinski, A. M., Lingohr, E. J., & Gyles, C. L. (2007). Isolation and characterization of nine bacteriophages that lyse O149 enterotoxigenic Escherichia coli. Veterinary microbiology. 124(1-2):47-57. DOI: https://doi.org/10.1016/j.vetmic.2007.03.028
18. Gaviria, G., & Castaño, J. (2012). Técnica para aislamiento de bacteriófagos específicos para Escherichia coli DH5α a partir de aguas residuales. Revista MVZ Córdoba. 17(1):2852-2860. DOI: https://doi.org/10.21897/rmvz.253
19. Kang, Y., Wang, J., Zhu, C., & Li, Z. (2024). Unveiling the Genomic Diversity and Ecological Impact of Phage Communities in Hospital Wastewater. Journal of Hazardous Materials, 135353. DOI: https://doi.org/10.1016/j.jhazmat.2024.135353
20. Wang, D., Liu, L., Xu, X., Wang, C., Wang, Y., Deng, Y., y Zhang, T. (2024). Distributions, interactions, and dynamics of prokaryotes and phages in a hybrid biological wastewater treatment system. Microbiome. 12 (1), 134. DOI: https://doi.org/10.1186/s40168-024-01853-6
21. Azzam, M. I., ElSayed, E. E., Gado, M. M., & Korayem, A. S. (2024). New phage-based wastewater pollution control solution with safe reuse. Environmental Nanotechnology, Monitoring & Management. 21, 100951. DOI: https://doi.org/10.1016/j.enmm.2024.100951
22. Choi, Y., Kwak, M. J., Kang, M. G., Kang, A. N., Lee, W., Mun, D., Choi, H., Jeongkuk, P., Eor, J. Y., Song, M., Kim, J. N., Oh, S., & Kim, Y. (2024). Molecular characterization and environmental impact of newly isolated lytic phage SLAM_phiST1N3 in the Cornellvirus genus for biocontrol of a multidrug-resistant Salmonella typhimurium in the swine industry chain. Science of The Total Environment, 922, 171208. DOI: https://doi.org/10.1016/j.scitotenv.2024.171208
23. Elbahnasawy, M. A., ElSayed, E. E., & Azzam, M. I. (2021). Newly isolated coliphages for bio-controlling multidrug-resistant Escherichia coli strains. Environmental Nanotechnology, Monitoring & Management. 16:100542. DOI: https://doi.org/10.1016/j.enmm.2021.100542
24. Costa, P., Pereira, C., Gomes, A. T., & Almeida, A. (2019). Efficiency of single phage suspensions and phage cocktail in the inactivation of Escherichia coli and Salmonella Typhimurium: An in vitro preliminary study. Microorganisms. 7(4):94. DOI: https://doi.org/10.3390/microorganisms7040094
25. Petsong, K., Benjakul, S., Chaturongakul, S., Switt, A. I. M., & Vongkamjan, K. (2024). Lysis profiles of Salmonella phages on Salmonella isolates from various sources and efficiency of a phage cocktail against S. enteritidis and S. typhimurium. Microorganisms. 7(4):100. DOI: https://doi.org/10.3390/microorganisms7040100
26. Chen, Z., Yang, Y., Li, G., Huang, Y., Luo, Y., & Le, S. (2024). Effective elimination of bacteria on hard surfaces by the combined use of bacteriophages and chemical disinfectants. Microbiology Spectrum. 12(4), e03797-23. DOI: https://doi.org/10.1128/spectrum.03797-23
27. Brás, A., Braz, M., Martinho, I., Duarte, J., Pereira, C., & Almeida, A. (2024). Effect of bacteriophages against Escherichia coli biofilms on food processing surfaces. Microorganisms, 12 (2), 366. DOI: https://doi.org/10.3390/microorganisms12020366
28. Byun, K. H., Han, S. H., Choi, M. W., Kim, B. H., & Ha, S. D. (2024). Efficacy of disinfectant and bacteriophage mixture against planktonic and biofilm state of Listeria monocytogenes to control in the food industry. International Journal of Food Microbiology, 413, 110587. DOI: https://doi.org/10.1016/j.ijfoodmicro.2024.110587




