Foodborne illness poses significant health and economic challenges, costing billions annually. Pathogens in food products arise from various sources (ingredients, poor hygienic practices, environment) and the use of bacteriophages as biocontrol agents may offer promise in reducing bacterial levels in foods without the drawbacks of traditional chemical sanitizers. Thus, the study aimed to isolate bacterial strains from fresh shrimp, turkey, and beef products, and identify strains that are good bacteriophage hosts (using plaque assay), as well as conduct a microbiological safety assessment of the products using standard traditional (total viable bacterial and coliform counts, biochemical characterisation) and molecular (16S rRNA sequencing) methods. It assessed total bacterial and colony counts across the samples, revealing variations between them. Notably, Paenibacillus pectinilyticus emerged as the predominant strain, followed by Raoultella planticola, Klebsiella pneumonia, Neobacillus niacin, Enterobacter asburiae, and Serratia grimesii. Of the seven (7) bacterial strains identified using 16S rRNA molecular characterization, only four showed potential as good phage hosts. As another key finding, emerging pathogens like S. grimesii, E. asburiae and R. planticola were identified from the products for the first time. Again, over 57% of the time probable microbial identities from traditional techniques did not align with molecular identities (99.28-100% identity coverage). Hence, molecular methods cannot be overemphasized in ensuring the accuracy of microbial identities, and detecting emerging pathogens. The presence of emerging pathogens, high coliform and viable bacterial counts further indicated the unsafe nature of these fresh products. The screening for, and identification of food-based bacteriophages may hold promise as alternative bio-control tools against foodborne infections. However, further research is warranted to elucidate their characteristics and efficacy in enhancing food safety.
| [1] | Todd, E, “Food-borne disease prevention and risk assessment”. International Journal of Environmental Research and Public Health, 17 (14). 5129. 2020.View Article PubMed |
| [2] | Hoffmann, S. and Ahn, J.W, “Economic cost of major foodborne illnesses increased $2 billion from 2013 to 2018”, Amber waves: The Economics of Food, Farming, Natural Resources, and Rural America, 2021 (04). 2021. |
| [3] | Lin, P., Tsai, H. and Ho, T, “Food safety gaps between consumers’ expectations and perceptions: development and verification of a gap-assessment tool”, International Journal of Environmental Research and Public Health, 17 (17), 6328. 2020.View Article PubMed |
| [4] | Lianou, A., Panagou, E.Z. and Nychas, G.J.E, Meat safety—I foodborne pathogens and other biological issues. In Lawrie's meat science, Woodhead Publishing, 2023, 549-590.View Article |
| [5] | Sadiku, M.N., Ashaolu, T.J. and Musa, S.M, “Food contamination: A primer”, International Journal of Advance in Scientific Research and Engineering, 6 (03). 01-07. 2020.View Article |
| [6] | Gourama, H, Foodborne pathogens. Food safety engineering, Springer International Publishing, Cham, 2020, 25-49.View Article |
| [7] | Schirone, M., Visciano, P., Tofalo, R. and Suzzi, G, “Foodborne pathogens: Hygiene and safety. Frontiers in Microbiology, 10. 481870. 2019.View Article PubMed |
| [8] | Kamboj, S., Gupta, N., Bandral, J.D., Gandotra, G. and Anjum, N, “Food safety and hygiene: A review”, International Journal of Chemical Studies, 8 (2), 358-368. 2020.View Article |
| [9] | Farooq, U., Shafi, A., Shahbaz, M., Khan, M.Z., Hayat, K., Baqir, M. and Iqbal, M, Food Quality and Food Safety: An Introduction, In Sequencing Technologies in Microbial Food Safety and Quality, CRC Press, 2021, 3-24.View Article PubMed |
| [10] | Sehrawat, A. and Sindhu, S.S, “Potential of biocontrol agents in plant disease control for improving food safety”, Defence Life Science Journal, 4 (4). 220-225. 2019.View Article |
| [11] | Jongman, M., Carmichael, P., Loeto, D. and Gomba, A, “Advances in the use of biocontrol applications in preharvest and postharvest environments: A food safety milestone”, Journal of Food Safety, 42 (2). e12957. 2022.View Article |
| [12] | Zdolec, N., Lorenzo, J.M., and Ray, R.C, “Use of microbes for improving food safety and quality”, BioMed Research International, 2018. 3902698. 2018View Article PubMed |
| [13] | Acuff, J.C., Dickson, J.S., Farber, J.M., Grasso-Kelley, E.M., Hedberg, C., Lee, A. and Zhu, M.J, “Practice and Progress: updates on outbreaks, advances in research, and processing technologies for low-moisture food safety”, Journal of Food Protection, 86 (1). 100018. 2023.View Article PubMed |
| [14] | Sibisi, A.S, Food hygiene, safety, handling practices and knowledge of food handlers in a food retail company in Durban, KwaZulu-Natal, South Africa (Doctoral dissertation), 2019. |
| [15] | Suárez, V.B., Quiberoni, A., Binetti, A.G. and Reinheimer, J.A., 2002. Thermophilic lactic acid bacteria phages isolated from Argentinian dairy industries. Journal of Food Protection, 65(10), 1597-1604.View Article PubMed |
| [16] | Moye, Z.D., Woolston, J. and Sulakvelidze, A, “Bacteriophage applications for food production and processing”, Viruses, 10 (4). 205. 2018.View Article PubMed |
| [17] | Islam, M.S., Zhou, Y., Liang, L., Nime, I., Liu, K., Yan, T., Wang, X. and Li, J, “Application of a phage cocktail for control of Salmonella in foods and reducing biofilms”, Viruses, 11 (9). 841. 2019.View Article PubMed |
| [18] | Garvey, M, “Bacteriophages and food production: Biocontrol and bio-preservation options for food safety”, Antibiotics, 11 (10), 1324, 2022.View Article PubMed |
| [19] | Lavilla, M., Domingo-Calap, P., Sevilla-Navarro, S. and Lasagabaster, A, “Natural Killers: Opportunities and challenges for the use of bacteriophages in microbial food safety from the one health perspective”, Foods, 12 (3). 552. 2023.View Article PubMed |
| [20] | Aruwa, C.E., and Ogunlade, S.T, “Classical identification, 16S rDNA sequencing, and molecular characterization of Bacillus species from convenience foods”, British Journal of Applied Science & Technology, 15 (5). 1-11. 2016.View Article |
| [21] | Aruwa, C.E., Akindusoye, A.J. and Awala, S.I, “Socio-demographic characteristics and food hygiene level assessment of food handlers in cafeterias around a Federal University in Nigeria”, Journal of Scientific Research and Reports, 14 (4). 1-9. 2017.View Article |
| [22] | Martínez-Laorden, A., Arraiz-Fernández, C. and González-Fandos, E, “Microbiological quality and safety of fresh turkey meat at retail level, including the presence of ESBL-producing Enterobacteriaceae and methicillin-resistant S. aureus”, Foods, 12 (6), 1274. 2023.View Article PubMed |
| [23] | Anie, C.O., Jemikalajah, D.J. and Eke, C.N, “Determination of microbial load of selected smoked fish sold in Abraka markets delta state” Nigerian Journal of Pure and Applied Science, 32 (1). 3281-3288. 2019. |
| [24] | Fawole, M.O. and Oso, B.A, Characterization of bacteria: Laboratory manual of microbiology, Spectrum Publishers, Ibadan, 2004, 24. |
| [25] | Van Twest, R. and Kropinski, A.M, Bacteriophage enrichment from water and soil. Bacteriophages: Methods and Protocols - Isolation, Characterization, and Interactions, 1. 15-21. 2009.View Article PubMed |
| [26] | Cappuccino, J. G. and Sherman, N, Microbiology. A laboratory manual (5th ed.). Benjamin/Cummings Science Publishing, 1999. |
| [27] | Glonti, T. and Pirnay, J.P, “In vitro techniques and measurements of phage characteristics that are important for phage therapy success”, Viruses, 14 (7). 1490. 2022.View Article PubMed |
| [28] | Rijpens, N.P. and Herman, L.M, “Molecular methods for identification and detection of bacterial food pathogens”, Journal of AOAC International, 85 (4). 984-995. 2002.View Article PubMed |
| [29] | Shin, J.H, “Nucleic acid extraction techniques”, Advanced Techniques in Diagnostic Microbiology, 209-225. 2013.View Article PubMed |
| [30] | Nkere, C.K., Ibe, N.I. and Iroegbu, C.U, “Bacteriological quality of foods and water sold by vendors and in restaurants in Nsukka, Enugu State, Nigeria: A comparative study of three microbiological methods”, Journal of Health, Population, and Nutrition, 29 (6). 560. 2011.View Article PubMed |
| [31] | Cooke. E.M., and Gibson, G.L, Essential clinical microbiology. John Wiley and Sons, New York, 1990, 16-21. |
| [32] | Merlin, S.B, “Food contamination and gastroenteritis”, Annual Reviews in Public Health, 6. 12-14. 1969. |
| [33] | World Health Organization Food Safety Unit. Contaminated food: a major cause of diarrhoea and associated malnutrition among infants and young children. Facts Infant Feed, 1-4, 1993. |
| [34] | Ling, H., Lou, X., Luo, Q., He, Z., Sun, M. and Sun, J, “Recent advances in bacteriophage-based therapeutics: Insight into the post-antibiotic era”, Acta Pharmaceutica Sinica B, 12 (12), 4348-4364. 2022.View Article PubMed |
| [35] | Huang, C., Shi, J., Ma, W., Li, Z., Wang, J., Li, J. and Wang, X, “Isolation, characterization, and application of a novel specific Salmonella bacteriophage in different food matrices”, Food Research International, 111. 631-641. 2018.View Article PubMed |
| [36] | Abebe, E., Gugsa, G. and Ahmed, M, “Review on major food-borne zoonotic bacterial pathogens”, Journal of Tropical Medicine, 2020 (4674235). 1-19. June 2020.View Article PubMed |
| [37] | Yang, Q., Ding, Y., Nie, R., Yao, L., Wang, X., Zhou, M., Wang, J. and Wang, X, “Characterization of a novel T7-like Salmonella typhimurium (ATCC13311) bacteriophage LPST144 and its endolysin”, LWT, 123. 109034. 2020.View Article |
| [38] | El-Shibiny, A. and El-Sahhar, S, “Bacteriophages: the possible solution to treat infections caused by pathogenic bacteria”, Canadian Journal of Microbiology, 63 (11). 865-879. 2017.View Article PubMed |
| [39] | Suja, E. and Gummadi, S.N., 2023. Advances in the applications of bacteriophages and phage products against food-contaminating bacteria. Critical Reviews in Microbiology, 1-26.View Article PubMed |
| [40] | Vecchia, I.D., Fasan, D., Pegoraro, M. and Benedetti, P, “Febrile sepsis: First report of human disease due to Paenibacillus sylvae”, Access Microbiology, 5 (6). 000580-v3. 2023.View Article PubMed |
| [41] | Szaniawski, M.A. and Spivak, A.M, “Recurrent Paenibacillus infection”, Oxford Medical Case Reports, 2019 (5). p.omz034. 2019. |
| [42] | Moreno, S.A.I., Andrus, A.D., Ranieri, M.L., Orsi, R.H., Ivy, R, “Genomic comparison of spore forming bacilli isolated from milk”, BMC Genomics, 15. 26. 2014.View Article PubMed |
| [43] | Mihu, A.G., Susan, M.M., Strauti, C.N., Mot, M.D., Muresanu, H.D., Balta, C. and Nesiu, A, “First Case of Raoultella planticola urinary tract infection reported in western Romania”, Medicina, 59 (3). 506. 2023.View Article PubMed |
| [44] | Vittoria, M.M., Angela, K., Aurora, P., Stefano, G., Cristina, M., Mariangela, S., Patrizia, C., Roberta, M. and Fausto, B, “Enterobacter asburiae ST229: an emerging carbapenemases producer”, Scientific Reports, 14 (1). p.6220. 2024.View Article PubMed |
| [45] | Shousha, A., Awaiwanont, N., Sofka, D., Smulders, F.J., Paulsen, P., Szostak, M.P., Humphrey, T. and Hilbert, F, “Bacteriophages isolated from chicken meat and the horizontal transfer of antimicrobial resistance genes”, Applied and Environmental Microbiology, 81 (14). 4600-4606. 2015.View Article PubMed |
| [46] | Bozhokina, E., Kever, L. and Khaitlina, S., “The Serratia grimesii outer membrane vesicles‐associated grimelysin triggers bacterial invasion of eukaryotic cells”, Cell Biology International, 44 (11). 2275-2283. 2020.View Article PubMed |
| [47] | Stenholm, A.R., Dalsgaard, I. and Middelboe, M, “Isolation and characterization of bacteriophages infecting the fish pathogen Flavobacterium psychrophilum”, Applied and Environmental Microbiology, 74 (13). 4070-4078. 2008.View Article PubMed |
| [48] | Pavlopoulos, G.A., Soldatos, T.G., Barbosa-Silva, A., and Schneider, R, “A reference guide for tree analysis and visualization”, BioData mining, 3 (1). 1. 2010.View Article PubMed |
| [49] | Mirzaei, M.K. and Pourmand, M.R, “Applications of molecular methods for identification and characterization of microbial communities in contaminated sites”, Journal of Applied Microbiology, 121 (3). 655-670. 2023. |