Enterococci in Meat: Understanding Consequences on Health and Food Safety
DOI:
https://doi.org/10.67601/njbls.v3i2c.75Keywords:
Antibiotics, resistance, Enterococci, animal, foodborne, healthAbstract
The focus of this review is the occurrence of Enterococci in meat and its consequence on health and food safety. Two species most commonly encountered in food as well as in hospital infections are Enterococcus faecalis and Enterococcus faecium. Members of the genus Enterococci are well known for their resistance to high temperatures, pH and salt concentrations. They are also known for their widespread resistance to a broad spectrum of antibiotics including some antibiotics of last resort such as vancomycin and linezolid. Antibiotic resistance is mostly mediated by genes borne on the chromosomes, plasmids or transposable elements. This also means they can acquire and transfer resistance easily. In addition, they possess a number of virulence determinants that aide invasion and colonization, as well as biofilm formation. Enterococci are found in different environments including soils, water, wastewater and slaughterhouses. Because of their widespread presence in different parts of the animal body, Enterococci easily find their way into foods of animal origin such as meat, poultry and milk. Strict personal and environmental hygiene must be observed while processing meat and other foods of animal origin to limit contamination with Enterococci and other foodborne pathogens. Prudent use of antibiotics both in healthcare and animal husbandry must be adopted to minimize the speed and scope of the development of resistace by Enterococci and other pathogens.
References
Abouelnaga, M., Lamas, A., Quintela-Baluja, M. et al. (2016). Evaluation of the extent of spreading of virulence factors and antibiotic resistance in Enterococci isolated from fermented and unfermented foods. Ann Microbiol 66, 577–585
Anderson, A.C., Jonas, D., Huber, I., Karygianni, L., Wölber, J., Hellwig, E., Arweiler, N., Vach, K., Wittmer, A., Al-Ahmad, A. (2016) Enterococcus faecalis from Food, Clinical Specimens, and Oral Sites: Prevalence of Virulence Factors in Association with Biofilm Formation. Front Microbiol.; 6:1534.
Araujo, A.J.G., Grassotti, T.T., and Frazzon, A.P.G. (2021). Characterization of Enterococcus spp. Isolated from a Fish Farming Environment in Southern Brazil. Brazilian Journal of Biology. 81(4): 954-961.
Aun, E., Kisand, V., Laht, M., Telling, K., Kalmus, P., Väli, Ü.,Brauer, A., Remm, M., and Tenson, T. (2021). Molecular Characterization of Enterococcus Isolates From Different Sources in Estonia Reveals Potential Transmission of Resistance Genes Among Different Reservoirs. Frontiers in microbiology, 12, 601490. https://doi.org/10.3389/fmicb.2021.601490.
Barel, M., Çelik, E., Gungor, G., Akcay, A., Güngör, C., Al, S., Hizlisoy, H., Ertas, N., Yildirim, Y. and Gonulalan, Z. (2022). Meta-Analysis of the Global Prevalence of Enterococcus spp. in Foods: Antibiotic Resistance Profile of Enterococcus faecalis and Enterococcus faecium. Annals of Animal Science. 23.
Ben Braïek, O. and Smaoui, S. (2019). Enterococci: Between Emerging Pathogens and Potential Probiotics. Biomed Research International, 5938210.
Bortolaia, V., Espinosa-Gongora C. and Guardabassi L. (2015). Human health risks associated with antimicrobial-resistant enterococci and Staphylococcus aureus on poultry meat. Clin Microbiol Infect. 22(2):130-140.
Chajęcka-Wierzchowska, W., Zadernowska, A., and García-Solache, M. (2020). Ready-to-eat dairy products as a source of multidrug-resistant Enterococcus strains: Phenotypic and genotypic characteristics. Journal of dairy science, 103(5), 4068–4077. https://doi.org/10.3168/jds.2019-17395.
Chen, M., Pan, H., Lou, Y., Wu, Z., Zhang, J., Huang, Y., Yu, W., & Qiu, Y. (2018). Epidemiological characteristics and genetic structure of linezolid-resistant Enterococcus faecalis. Infection and drug resistance, 11, 2397–2409. https://doi.org/10.2147/IDR.S181339.
Dapkevicius, M.L.E., Sgardioli, B., Câmara, S.P.A., Poeta, P. and Malcata, F.X. (2021). Current Trends of Enterococci in Dairy Products: A Comprehensive Review of Their Multiple Roles. Foods. ;10(4):821.
Ducková, V., Čanigová, M. and Kročko, M. (2014). Enterococci and their Resistance to Antibiotics and Thyme Essential Oil : J Microbiol Biotech Food Sci 3 (special issue 1) 1-4.
Ezeh, G., Nwanta, J. and Ogugua, A. (2023). Occurrence, Antimicrobial Resistance and Pathogenic Factors. Animal Research International. 20. 4791-4816.
Fahmy, N., Abdel-Gawad, A., Rezk, G., and Mahmoud, E. (2021). Characterization of Enterococci isolated from intensive care unit (ICU); Distribution of virulence markers, virulence genes and antibiotic resistance pattern. Microbes and Infectious Diseases, 2(4), 725-735.
Fang, S. (2020). Enterococci and food safety – Are all probiotics beneficial? Pediatrics & Neonatology, 61.
Fiore, E., Van Tyne, D. and Gilmore, M.S. (2019). Pathogenicity of Enterococci. Microbiol Spectrum 7(4):GPP3 0053-2018.
Foulquié Moreno, M. R., Sarantinopoulos, P., Tsakalidou, E., & De Vuyst, L. (2006). The role and application of enterococci in food and health. International Journal of Food Microbiology, 106(1), 1–24. doi.org
Franz, C., Muscholl-Silberhorn, A., Yousif, N., Vancanneyt, M., Swings, J. and Holzapfel, W. (2001). Incidence of virulence factors and antibiotic resistance among enterococci isolated from food. Appl Environ Microbiol 67:4385–4389.
García-Solache, M. and Rice, L.B. (2019). The enterococcus: a model of adaptability to its environment. Clin Microbiol Rev 32:e00058-18. https://doi.org/10.1128/CMR.00058-18.
Ghosh, A. and Zurek, L. (2015). Chapter 9 - Antibiotic Resistance in Enterococci: A Food Safety Perspective, Editor(s): Chin-Yi Chen, Xianghe Yan, Charlene R. Jackson, Antimicrobial Resistance and Food Safety, Academic Press, Pages 155-180, ISBN 9780128012147. https://doi.org/10.1016/B978-0-12-801214-7.00009-0.
Giraffa, G. (2002). Enterococci from foods. FEMS Microbiol Rev. 26(2):163-71.
Goh, H.M.S., Yong, M.H.A., Chong, K.K.L., Kline, K.A. (2017). Model systems for the study of Enterococcal colonization and infection. Virulence. 8(8):1525-1562.
Gökmen, M., Önen, A. Ektik Sezen, N., Kara, R. Torlak, E. and Metli, M. (2017). Detection of Prevalence, Antibiotic Resistance and Virulence Factors of Enterococcus spp. Isolated From Ready to Eat Foods. Kocatape Veterinary Journal 76-82. 10.5578/kvj.54067.
Graham, K., Stack, H. and Rea, R. (2020). Safety, beneficial and technological properties of enterococci for use in functional food applications - a review. Crit Rev Food Sci Nutr. 60(22):3836-3861.
Gwida, M., Zakaria, A., El-Sherbiny, H., Elkenany, R. and Elsayed, M. (2019). Prevalence of Campylobacter, Enterococcus and Staphylococcus aureus in slaughtered camels. Veterinární Medicína. 64. 521-530. 10.17221/104/2019-VETMED.
Hammerum, A.M., Lester, C.H., and Heuer, O.E. (2010). Antimicrobial-resistant enterococci in animals and meat: a human health hazard? Foodborne Pathog Dis. 7(10):1137-46.
Hanchi, H., Mottawea, W., Sebei, K. and Hammami, R. (2018). The Genus Enterococcus: Between Probiotic Potential and Safety Concerns-An Update. Front Microbiol. 9:1791.
Holman, D., Klima, C., Gzyl, K., Zaheer, R., Service, C., Jones, T. and McAllister, T. (2021). Antimicrobial Resistance in Enterococcus Spp. Isolated from a Beef Processing Plant and Retail Ground Beef. Microbiology Spectrum. 9. 10.1128/Spectrum.01980-21.
Igbinosa, I. H. and Raje, O. (2020). Characterization of Enterococcus species isolated from abattoir environment in Benin city, Nigeria. Ife Journal of Science. 21. 81. 10.4314/ijs.v21i3.8.
Johnston, L. M., and Jaykus, L. A. (2004). Antimicrobial resistance of Enterococcus species isolated from produce. Applied and Environmental Microbiology, 70(5), 3133–3137. https://doi.org/10.1128/AEM.70.5.3133-3137.2004.
Kayaoglu, G., and Ørstavik, D. (2004). Virulence factors of Enterococcus faecalis: relationship to endodontic disease. Critical reviews in oral biology and medicine : an official publication of the American Association of Oral Biologists, 15(5), 308–320. https://doi.org/10.1177/154411130401500506.
Kim, M.C., Cha, M.H., Ryu, J.G. and Woo, G.J. (2017). Characterization of Vancomycin-Resistant Enterococcus faecalis and Enterococcus faecium Isolated from Fresh Produces and Human Fecal Samples. Foodborne Pathog Dis. 14(4):195-201.
Klein, G. (2003). Taxonomy, ecology and antibiotic resistance of enterococci from food and the gastro-intestinal tract. International journal of food microbiology, 88(2-3), 123-131.
Klibi, N., Aouini, R., Borgo, F. et al. (2015). Antibiotic resistance and virulence of faecal enterococci isolated from food-producing animals in Tunisia. Ann Microbiol 65, 695–702 https://doi.org/10.1007/s13213-014-0908-x.
Krocko, M., Čanigová, M. and Ducková, V. (2008). Occurrence of enterococci in raw pork and beef and their antibiotics multiresistance. Acta Universitatis Agriculturae et Silviculturae Mendelianae Brunensis. 56. 101-106.
Ławniczek-Wałczyk, A., Cyprowski, M. and Górny, R. (2022). Distribution of Selected Drug-resistant Enterococcus Species in Meat Plants in Poland. RocznikOchronaŚrodowiska, 24, 345-359. https://doi.org/10.54740/ros.2022.024.
Makarov, D.A., Ivanova, O.E., Pomazkova, A.V., Egoreva, M.A., Prasolova, O.V., Lenev, S.V., Gergel, M.A., Bukova, N.K. and Karabanov, S.Y. (2022). Antimicrobial resistance of commensal Enterococcus faecalis and Enterococcus faecium from food-producing animals in Russia. Vet World. 15(3):611-621.
Manson, A.L., Van Tyne, D., Straub, T.J., Clock, S., Crupain, M., Rangan, U., Gilmore, M.S. and Earl, A.M. (2019). Chicken Meat-Associated Enterococci: Influence of Agricultural Antibiotic Use and Connection to the Clinic. Appl Environ Microbiol. 85(22):e01559-19.
Mariam, S. H. (2021). A sampling survey of enterococci within pasteurized, fermented dairy products and their virulence and antibiotic resistance properties. PloS one, 16(7), e0254390. https://doi.org/10.1371/journal.pone.0254390.
Medeiros, A. W., Pereira, R. I., Oliveira, D. V., Martins, P. D., d'Azevedo, P. A., Van der Sand, S., Frazzon, J. and Frazzon, A. P. (2014). Molecular detection of virulence factors among food and clinical Enterococcus faecalis strains in South Brazil. Brazilian journal of microbiology: [publication of the Brazilian Society for Microbiology], 45(1), 327–332. https://doi.org/10.1590/S1517-83822014005000031
Naas, H., Almajdoubi, Z., Garbaj, A., Azwai, S., Gammoudi, F., Abolghait, S., Moawad, A., Barbieri, I., Eshamah, H. and Eldaghayes, I. (2017). Molecular identification and antibiogram of Enterococcus spp. isolated on Enterococcus Selective Differential (ESD) media from meat, meat products and seafood in Libya. Journal of Microbiology, Biotechnology and Food Sciences. 6. 1264-1268.
Nagarajan, V., Wahab, A., Shivraj, S., et al. (2018). Study of bacterial contamination of raw meat in Hyderabad. MOJ Proteomics Bioinform, 7(1):46-51.
O'Dea, M., Sahibzada, S., Jordan, D., Laird, T., Lee, T., Hewson, K., Pang, S., Abraham, R., Coombs, G.W., Harris, T., Pavic, A. and Abraham, S. (2019). Genomic, Antimicrobial Resistance, and Public Health Insights into Enterococcus spp. from Australian Chickens. J Clin Microbiol. 57(8):e00319-19.
Onaran, B., Goncuoglu, M. and Bilir, F. (2019). Antibiotic resistance profiles of vancomycin resistant enterococci in chicken meat samples. Ankara Üniversitesi Veteriner Fakültesi Dergisi. 66. 10.33988/auvfd.451328.
Rabah, I., Mansour, M., Mohamed, A., Soliman, F, and Saleh, N. (2022). Detection of Enterococcus faecalis as an indicator organism in abattoirs´ environment as well as meat. Matrouh Journal of Veterinary Medicine.
Ramos, S., Silva, V., Dapkevicius, M. L. E., Igrejas, G., & Poeta, P. (2020). Enterococci, from Harmless Bacteria to a Pathogen. Microorganisms, 8(8), 1118. https://doi.org/10.3390/microorganisms8081118.
Samad, M. A., Sagor, M. S., Hossain, M. S., Karim, M. R., Mahmud, M. A., Sarker, M. S., Shownaw, F. A., Mia, Z., Card, R. M., Agunos, A., and Johanna, L. (2022). High prevalence of vancomycin non-susceptible and multi-drug resistant enterococci in farmed animals and fresh retail meats in Bangladesh. Veterinary Research Communications, 46(3), 811–822. https://doi.org/10.1007/s11259-022-09906-7
Sanlibaba, P., Tezel, B. U., and Senturk, E. (2018). Antimicrobial Resistance of Enterococcus Species Isolated from Chicken in Turkey. Korean journal for food science of animal resources, 38(2), 391–402.
Sigirci, B.D., Celik, B., Halaç, B., Kahraman, B.B., Bagcigil, A.F. and Ak, S. (2021). Characterization of Faecal Enterococci from Wild Birds in Turkey and Its Importance in Antimicrobial Resistance. Journal of the Hellenic Veterinary Medical Society. 72(3), 3015-3022 3015. 10.12681/jhvms.28482.
Soni, M., Nayak, J.B., Anjaria, P., Bhavsar, P., Chaudhary, J. and Brahmbhatt, M.N. (2022). Isolation and molecular detection of biofilm producing and multiple drug resistant Enterococcus faecalis from the buffalo meat. Buffalo Bulletin. 41. 537-546.
Sustacková, A., Nápravníková, E., and Schlegelová, J. (2004). Antimicrobial resistance of Enterococcus spp. isolates from raw beef and meat products. Folia microbiologica, 49(4), 411–417. https://doi.org/10.1007/BF02931602
Tansuphasiri, U., Khaminthakul, D., and Pandii, W. (2006). Antibiotic resistance of enterococci isolated from frozen foods and environmental water. The Southeast Asian journal of tropical medicine and public health, 37(1), 162–170.
Tuncay, R. and Sancak, Y. (2022). The Prevalence of Enterococcus spp., Resistance Profiles, the Presence of the VanA and VanB Resistance Genes in Chicken Meats. Kocatepe Veterinary Journal, 15(4), 381 - 389.
Venkateswaran, P., Lakshmanan, P. M., Muthukrishnan, S., Bhagavathi, H., Vasudevan, S., Neelakantan, P., and Solomon, A. P. (2022). Hidden agenda of Enterococcus faecalis lifestyle transition: planktonic to sessile state. Future microbiology, 17, 1051–1069. https://doi.org/10.2217/fmb-2021-0212.
Výrostková, J., Regecová, I., Dudriková, E., Marcinˇcák, S., Vargová, M., Kováˇcová, M. and Mal’ová, J. (2021). Antimicrobial Resistance of Enterococcus sp. Isolated from Sheep and Goat Cheeses. Foods, 10, 1844. https://doi.org/10.3390/foods10081844.
Zaheer, R., Cook, S. R., Barbieri, R., Goji, N., Cameron, A., Petkau, A., Polo, R. O., Tymensen, L., Stamm, C., Song, J., Hannon, S., Jones, T., Church, D., Booker, C. W., Amoako, K., Van Domselaar, G., Read, R. R., and McAllister, T. A. (2020). Surveillance of Enterococcus spp. reveals distinct species and antimicrobial resistance diversity across a One-Health continuum. Scientific reports, 10(1), 3937. https://doi.org/10.1038/s41598-020-61002-5

