Genes and expression of virulence factors in Escherichia coli isolated from production animals.
Abstract
The virulence factors of pathogens are expressed once they overcome the physiological mechanisms of immune response by the organism, Escherichia coli (E. coli) is a bacterium that is considered a public health problem worldwide due to the high prevalence of resistance and pathogenicity mechanisms expressed, it is mainly related to intestinal infections and is transmitted in the food chain; the genetic determinants encoding virulence factors are transferred between different species or the same, through the mechanism of horizontal gene transfer. The present review aims to describe virulence factors and genes encoding them in E. coli strains isolated from production animals and food products. The databases Medline, Lilacs, ScienceDirect, Scopus, SciELO, and Dialnet were searched using a combination of validated keywords in English (gene, virulence, virulence factor, infection, horizontal gene transfer, mutation, and production animals). Different virulence mechanisms were identified in different production environments, which vary according to the animal and bacterial species. The genes with the highest circulation were Stx1, Stx2 coding for toxins, Saa for adhesins, ehxA for enterohemolysin, eaeA for intimin, and IpfA for fimbriae. Microbiological surveillance and control in the food and animal production area are of great importance to avoid possible disease outbreaks in susceptible populations, due to the effect of virulence factors.
Keywords
Escherichia coli, Food Chain, Genes, Polymerase Chain Reaction, Virulence
References
- Akomoneh, E. A., Esemu, S. N & Kfusi, A. J. (2020). Prevalence and virulence gene profiles of Escherichia coli O157 from cattle slaughtered in Buea, Cameroon. PLoS ONE, 15(12 December), e0235583. https://doi.org/10.1371/journal.pone.0235583 DOI: https://doi.org/10.1371/journal.pone.0235583
- Al-Arfaj, A., Ali, S., Hessain, M., Zakri, M., Dawoud, M., Al-Maary, S., & Moussa, M. (2016). Phenotypic and genotypic analysis of pathogenic Escherichia coli virulence genes recovered from Riyadh, Saudi Arabia. Saudi Journal of Biological Sciences, 23(6), 713–717. https://doi.org/10.1016/J.SJBS.2015.11.011 DOI: https://doi.org/10.1016/j.sjbs.2015.11.011
- Alonso, M. Z., Krüger, A., Sanz, M. E., Padola, N. L., & Lucchesi, P. M. A. (2016). Serotypes, virulence profiles and stx subtypes of Shigatoxigenic Escherichia coli isolated from chicken derived products. Revista Argentina de Microbiologia, 48(4), 325–328. https://doi.org/10.1016/j.ram.2016.04.009 DOI: https://doi.org/10.1016/j.ram.2016.04.009
- Ateba, C. N., & Mbewe, M. (2016). Detection of Escherichia coli O157:H7 virulence genes in isolates from beef, pork, water, human and animal species in the northwest province, South Africa: Public health implications. Research in Microbiology, 162(3), 240–248. https://doi.org/10.1016/j.resmic.2010.11.008 DOI: https://doi.org/10.1016/j.resmic.2010.11.008
- Bag, M. A. S., Khan, M. S. R., Sami, M. D. H., Begum, F., Islam, M. S., Rahman, M. M., Rahman, M. T., & Hassan, J. (2021). Virulence determinants and antimicrobial resistance of E. coli isolated from bovine clinical mastitis in some selected dairy farms of Bangladesh. Saudi Journal of Biological Sciences. https://doi.org/10.1016/j.sjbs.2021.06.099 DOI: https://doi.org/10.1016/j.sjbs.2021.06.099
- Bolukaoto, J. Y., Kock, M. M., Strydom, K. A., Mbelle, N. M., & Ehlers, M. M. (2019). Molecular characteristics and genotypic diversity of enterohaemorrhagic Escherichia coli O157:H7 isolates in Gauteng region, South Africa. Science of the Total Environment, 692, 297–304. https://doi.org/10.1016/j.scitotenv.2019.07.119 DOI: https://doi.org/10.1016/j.scitotenv.2019.07.119
- Brusa, V., Costa, M., Padola, N. L., Etcheverría, A., Sampedro, F., Fernandez, P. S., Leotta, G. A., & Signorini, M. L. (2020). Quantitative risk assessment of haemolytic uremic syndrome associated with beef consumption in Argentina. PLoS ONE, 15(11 November), e0242317. https://doi.org/10.1371/journal.pone.0242317 DOI: https://doi.org/10.1371/journal.pone.0242317
- Cadona, J. S., Burgán, J., González, J., Bustamante, A. V., & Sanso, A. M. (2020). Differential expression of the virulence gene nleB among Shiga toxin-producing Escherichia coli strains. Heliyon, 6(6), e04277. https://doi.org/10.1016/j.heliyon.2020.e04277 DOI: https://doi.org/10.1016/j.heliyon.2020.e04277
- Carranza, C., León, R., Falcón, N., Neumann, A., & Kromm, C. (2016). Characterization and distribution of potentially avian pathogenic Escherichia coli isolates from broilers in Peru. Revista de Investigaciones Veterinarias Del Peru, 23(2), 209–219. https://doi.org/10.15381/rivep.v23i2.901 DOI: https://doi.org/10.15381/rivep.v23i2.901
- Carvajal, E., Rueda, E., Talavera, M., Torres, M., López, D., & Vásquez, M. C. (2021). Resistencia a antibióticos betalactámicos y quinolonas en Escherichia coli aislada de pollos broiler. Revista de Investigaciones Veterinarias del Perú, 32(2). http://dx.doi.org/10.15381/rivep.v32i2.20012 DOI: https://doi.org/10.15381/rivep.v32i2.20012
- Cruz-Soto, A. S., Toro-Castillo, V., Munguía-Magdaleno, C. O., Torres-Flores, J. E., Flores-Pantoja, L. E., Loeza-Lara, P. D., Jiménez-Mejía, R., Cruz-Soto, A. S., Toro-Castillo, V., Munguía-Magdaleno, C. O., Torres-Flores, J. E., Flores-Pantoja, L. E., Loeza-Lara, P. D., & Jiménez-Mejía, R. (2020). Relación genética, formación de biopelículas, movilidad y virulencia de Escherichia coli aislada de mastitis bovina. Revista Mexicana de Ciencias Pecuarias, 11(1), 167–182. https://doi.org/10.22319/RMCP.V11I1.4998 DOI: https://doi.org/10.22319/rmcp.v11i1.4998
- Cunha, M. P. V., De Oliveira, M. G. X., De Oliveira, M. C. V., Da Silva, K. C., Gomes, C. R., Moreno, A. M., & Knöbl, T. (2016). Virulence profiles, phylogenetic background, and antibiotic resistance of Escherichia coli isolated from turkeys with airsacculitis. Scientific World Journal, 2014. https://doi.org/10.1155/2014/289024 DOI: https://doi.org/10.1155/2014/289024
- Do, K. H., Park, H. E., Byun, J. W., & Lee, W. K. (2020). Virulence and antimicrobial resistance profiles of Escherichia coli encoding mcr gene from diarrhoeic weaned piglets in Korea during 2007–2016. Journal of Global Antimicrobial Resistance, 20, 324–327. https://doi.org/10.1016/j.jgar.2019.09.010 DOI: https://doi.org/10.1016/j.jgar.2019.09.010
- Douëllou, T., Delannoy, S., Ganet, S., Mariani-Kurkdjian, P., Fach, P., Loukiadis, E., Montel, M., & Thevenot-Sergentet, D. (2016). Shiga toxin-producing Escherichia coli strains isolated from dairy products — Genetic diversity and virulence gene profiles. International Journal of Food Microbiology, 232, 52–62. https://doi.org/10.1016/J.IJFOODMICRO.2016.04.032 DOI: https://doi.org/10.1016/j.ijfoodmicro.2016.04.032
- Farfán, A., Ariza, E., Vargas, S., & Vargas, L (2016). Virulence mechanisms of enteropathogenic Escherichia coli. Revista Chilena de Infectologia, 33(4), 438–450. https://doi.org/10.4067/S0716-10182016000400009 DOI: https://doi.org/10.4067/S0716-10182016000400009
- Fayemi, O. E., Akanni, G. B., Elegbeleye, J. A., Aboaba, O. O., & Njage, P. M. (2021). Prevalence, characterization and antibiotic resistance of Shiga toxigenic Escherichia coli serogroups isolated from fresh beef and locally processed ready-to-eat meat products in Lagos, Nigeria. International Journal of Food Microbiology, 347, 109191. https://doi.org/10.1016/J.IJFOODMICRO.2021.109191 DOI: https://doi.org/10.1016/j.ijfoodmicro.2021.109191
- Fu, Q., Su, Z., Cheng, Y., Wang, Z., Li, S., Wang, H., Sun, J., & Yan, Y. (2017). Clustered, regularly interspaced short palindromic repeat (CRISPR) diversity and virulence factor distribution in avian Escherichia coli. Research in Microbiology, 168(2), 147–156. https://doi.org/10.1016/J.RESMIC.2016.10.002 DOI: https://doi.org/10.1016/j.resmic.2016.10.002
- Gazal, L. E. S., Puno-Sarmiento, J. J., Medeiros, L. P., Cyoia, P. S., Da Silveira, W. D., Kobayashi, R. K. T., & Nakazato, G. (2016). Presence of pathogenicity islands and virulence genes of extraintestinal pathogenic Escherichia coli (ExPEC) in isolates from avian organic fertilizer. Poultry Science, 94(12), 3025–3033. https://doi.org/10.3382/PS/PEV278 DOI: https://doi.org/10.3382/ps/pev278
- He, L., Simpson, D. J., & Gänzle, M. G. (2020). Detection of enterohaemorrhagic Escherichia coli in food by droplet digital PCR to detect simultaneous virulence factors in a single genome. Food Microbiology, 90, 103466. https://doi.org/10.1016/j.fm.2020.103466 DOI: https://doi.org/10.1016/j.fm.2020.103466
- Herrera Arias, F., Santos Buelga, J., & Villamizar Gallardo, R. (2019). Primer reporte de Escherichia coli productora de toxina shiga no O157 que codifica el gen de la enterohemolisina en carne cruda en colombia. Arch. Latinoam. Nutr, 59–67. https://www.alanrevista.org/ediciones/2019/1/art-8/ DOI: https://doi.org/10.37527/2019.69.1.008
- Kaushik, P., Anjay, Kumari, S., Dayal, S., & Kumar, S. (2018). Antimicrobial resistance and molecular characterisation of E. coli from poultry in eastern India. Veterinaria Italiana, 54(3), 197–204. https://doi.org/10.12834/VetIt.330.1382.2
- Keane, O. M. (2016). Genetic diversity, the virulence gene profile and antimicrobial resistance of clinical mastitis-associated Escherichia coli. Research in Microbiology, 167(8), 678–684. https://doi.org/10.1016/J.RESMIC.2016.06.011 DOI: https://doi.org/10.1016/j.resmic.2016.06.011
- Le Strange, K., Markland, S. M., Hoover, D. G., Sharma, M., & Kniel, K. E. (2017). An evaluation of the virulence and adherence properties of avian pathogenic Escherichia coli. One Health, 4, 22–26. https://doi.org/10.1016/j.onehlt.2017.08.001 DOI: https://doi.org/10.1016/j.onehlt.2017.08.001
- Li, G; Mohamed, L; Zhao, G; Gao, Y; Kaidi, R; Mustapha, O; Wang, J & Oumouna, K. (2018). Virulence traits of avian pathogenic (APEC) and fecal (AFEC) E. coli isolated from broiler chickens in Algeria. Tropical Animal Health and Production, 50(3), 547–553. https://doi.org/10.1007/S11250-017-1467-5 DOI: https://doi.org/10.1007/s11250-017-1467-5
- Marazzato, M., Aleandri, M., Massaro, M. R., Vitanza, L., Conte, A. L., Conte, M. P., Nicoletti, M., Comanducci, A., Goldoni, P., Maurizi, L., Zagaglia, C., & Longhi, C. (2020). Escherichia coli strains of chicken and human origin: Characterization of antibiotic and heavy-metal resistance profiles, phylogenetic grouping, and presence of virulence genetic markers. Research in Veterinary Science, 132, 150–155. https://doi.org/10.1016/J.RVSC.2020.06.012 DOI: https://doi.org/10.1016/j.rvsc.2020.06.012
- Márquez, H., Quiroz, I., Miranda, P., Vidales, E., Sánchez, H., & López, A. (2018). Genes de virulencia y grupo filogenético en aislados de Escherichia coli patogénica aviar. Archivos de Medicina, ISSN-e 1698-9465, Vol. 14, No. 1, 2018, 14(1), 2. https://dialnet.unirioja.es/servlet/articulo?codigo=6373537&info=resumen&idioma=ENG
- Martín, C., Jimena, C., Sanso, S., & Mariel, A. (2018). Distribución de genes de virulencia en Escherichia coli verotoxigénico O91 de bovinos y alimentos cárnicos.14–34. https://www.ridaa.unicen.edu.ar/xmlui/bitstream/handle/123456789/2027/CHRISTENSEN%2C%20MARTIN.pdf?sequence=1&isAllowed=y
- Martínez-Vázquez, A. V., Rivera-Sánchez, G., Lira-Méndez, K., Reyes-López, M. Á., & Bocanegra-García, V. (2018). Prevalence, antimicrobial resistance and virulence genes of Escherichia coli isolated from retail meat in Tamaulipas, Mexico. Journal of Global Antimicrobial Resistance, 14, 266–272. https://doi.org/10.1016/J.JGAR.2018.02.016 DOI: https://doi.org/10.1016/j.jgar.2018.02.016
- Millán, Y., Méndez, A., Burguera, M., Pimentel, P., Araque, M., & Ramírez, A. (2018). Determinación de Enterobacterias y detección de genes de virulencia en Escherichia coli aislada en leche cruda. Revista de La Sociedad Venezolana de Microbiología, 38(2), 58–63. http://saber.ucv.ve/ojs/index.php/rev_vm/article/view/16260
- Moeinirad, M., Douraghi, M., Foroushani, A. R., Sanikhani, R., & Dallal, M. M. S. (2021). Molecular characterization and prevalence of virulence factor genes of Shiga toxin-producing Escherichia coli (STEC) isolated from diarrheic children. Gene Reports, 25, 101379. https://doi.org/10.1016/j.genrep.2021.101379 DOI: https://doi.org/10.1016/j.genrep.2021.101379
- Nüesch-Inderbinen, M., Stevens, M. J., Cernela, N., Müller, A., Biggel, M., & Stephan, R. (2021). Distribution of virulence factors, antimicrobial resistance genes and phylogenetic relatedness among Shiga toxin-producing Escherichia coli serogroup O91 from human infections. International Journal of Medical Microbiology, 311(8), 151541. https://doi.org/10.1016/j.ijmm.2021.151541 DOI: https://doi.org/10.1016/j.ijmm.2021.151541
- Pearson, J. S., Giogha, C., Wong Fok Lung, T., & Hartland, E. L. (2016). The Genetics of Enteropathogenic Escherichia coli Virulence. In Annual Review of Genetics (Vol. 50, pp. 493–513). Annual Reviews. https://doi.org/10.1146/annurev-genet-120215-035138 DOI: https://doi.org/10.1146/annurev-genet-120215-035138
- Randall, L., Wu, G., Phillips, N., Coldham, N., Mevius, D., & Teale, C. (2016). Virulence genes in bla CTX-M Escherichia coli isolates from chickens and humans. Research in Veterinary Science, 93(1), 23–27. https://doi.org/10.1016/j.rvsc.2016.06.016 DOI: https://doi.org/10.1016/j.rvsc.2011.06.016
- Ranjbar, R., Masoudimanesh, M., Dehkordi, F. S., Jonaidi-Jafari, N., & Rahimi, E. (2017). Shiga (Vero)-toxin producing Escherichia coli isolated from the hospital foods virulence factors, o-serogroups and antimicrobial resistance properties. Antimicrobial Resistance and Infection Control, 6(1), 1–11. https://doi.org/10.1186/s13756-016-0163-y DOI: https://doi.org/10.1186/s13756-016-0163-y
- Rípodas, A., Fernández, D., & Macho, M. (2017). Investigación de Escherichia Coli productor de toxinas Shiga (STEC) en carnes y derivados cárnicos. Sanidad Militar, 73(3), 147–152. https://doi.org/10.4321/s1887-85712017000300002
- Sanchez, A. (2019). Caracterizacion molecular de factores de virulencia y genotipos de Escherichia coli aislada en langostino (litopenaeus vannamei) y camarones de rio (cryphiops caementarius) en terminales pesqueros de Lima metropolitana. [Universidad Peruana Cayetano Heredia]. In Journal of Chemical Information and Modeling (Vol. 53, Issue 9). https://repositorio.upch.edu.pe/handle/20.500.12866/3680
- Sarowska, J., Futoma-Koloch, B., Jama-Kmiecik, A., Frej-Madrzak, M., Ksiazczyk, M., Bugla-Ploskonska, G., & Choroszy-Krol, I. (2019). Virulence factors, prevalence and potential transmission of extraintestinal pathogenic Escherichia coli isolated from different sources: Recent reports. In Gut Pathogens (Vol. 11, Issue 1, pp. 1–16). BioMed Central Ltd. https://doi.org/10.1186/s13099-019-0290-0 DOI: https://doi.org/10.1186/s13099-019-0290-0
- Soares, B. D., de Brito, K. C. T., Grassotti, T. T., Filho, H. C. K., de Camargo, T. C. L., Carvalho, D., Dorneles, I. C., Otutumi, L. K., Cavalli, L. S., & de Brito, B. G. (2021). Respiratory microbiota of healthy broilers can act as reservoirs for multidrug-resistant Escherichia coli. Comparative Immunology, Microbiology and Infectious Diseases, 101700. https://doi.org/10.1016/J.CIMID.2021.101700. DOI: https://doi.org/10.1016/j.cimid.2021.101700
- Sunde, M., Ramstad, S. N., Rudi, K., Porcellato, D., Ravi, A., Ludvigsen, J., ... & Telke, A. A. (2021). Plasmid-associated antimicrobial resistance and virulence genes in Escherichia coli in a high arctic reindeer subspecies. Journal of Global Antimicrobial Resistance, 26, 317-322. https://doi.org/10.1016/j.jgar.2021.06.003 DOI: https://doi.org/10.1016/j.jgar.2021.06.003
- Taha, Z. M., & Yassin, N. A. (2019). Prevalence of diarrheagenic Escherichia coli in animal products in Duhok province, Iraq. Iranian Journal of Veterinary Research, 20(4), 255–262. /pmc/articles/PMC6983314/. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6983314/pdf/ijvr-20-255.pdf
- Thierry, S. I. L., Gannon, J. E., Jaufeerally-Fakim, Y., & Santchurn, S. J. (2020). Shiga-toxigenic Escherichia coli from animal food sources in Mauritius: Prevalence, serogroup diversity and virulence profiles. International Journal of Food Microbiology, 324. https://doi.org/10.1016/J.IJFOODMICRO.2020.108589 DOI: https://doi.org/10.1016/j.ijfoodmicro.2020.108589
- Umpiérrez, A., Ernst, D., Fernández, M., Oliver, M., Casaux, M. L., Caffarena, R. D., Schild, C., Giannitti, F., Fraga, M., & Zunino, P. (2021). Virulence genes of Escherichia coli in diarrheic and healthy calves. Revista Argentina de Microbiología, 53(1), 34–38. https://doi.org/10.1016/J.RAM.2020.04.004 DOI: https://doi.org/10.1016/j.ram.2020.04.004
- Varga, C., Brash, M. L., Slavic, D., Boerlin, P., Ouckama, R., Weis, A., Petrik, M., Philippe, C., Barham, M., & Guerin, M. T. (2018). Evaluating Virulence-Associated Genes and Antimicrobial Resistance of Avian Pathogenic Escherichia coli Isolates from Broiler and Broiler Breeder Chickens in Ontario, Canada. Avian Diseases, 62(3), 291–299. https://doi.org/10.1637/11834-032818-Reg.1 DOI: https://doi.org/10.1637/11834-032818-Reg.1
- Vidal, R. M., Chamorro, N. L., & Girón, J. A. (2016). Animal Enterotoxigenic Escherichia coli. In M. S. Donnenberg (Ed.), Escherichia Coli in the Americas (Vol. 7, Issue 1, pp. 1–26). ASM PressWashington, DC. https://doi.org/10.1007/978-3-319-45092-6_1 DOI: https://doi.org/10.1007/978-3-319-45092-6_1
- Wu, B., Duan, H., Qi, Q., Cai, Y., Zhong, Z., & Chai, T. (2018). Identifying virulence factor genes in E. coli in animal houses and their transmission to outside environments. Journal of Aerosol Science, 117, 189–199. https://doi.org/10.1016/j.jaerosci.2017.11.009 DOI: https://doi.org/10.1016/j.jaerosci.2017.11.009
- Yin, L., Li, Q., Wang, Z., Shen, X., Tu, J., Shao, Y., ... & Pan, X. (2021). The Escherichia coli type III secretion system 2 Is involved in the biofilm formation and virulence of avian Pathogenic Escherichia coli. Comparative Immunology, Microbiology and Infectious Diseases, 79, 101722. https://doi.org/10.1016/j.cimid.2021.101722 DOI: https://doi.org/10.1016/j.cimid.2021.101722
- Zhang, D., Zhang, Z., Huang, C., Gao, X., Wang, Z., Liu, Y., Tian, C., Hong, W., Niu, S., & Liu, M. (2018). The phylogenetic group, antimicrobial susceptibility, and virulence genes of Escherichia coli from clinical bovine mastitis. Journal of Dairy Science, 101(1), 572–580. https://doi.org/10.3168/jds.2017-13159 DOI: https://doi.org/10.3168/jds.2017-13159
- Zhang, S., Chen, S., Rehman, M. U., Yang, H., Yang, Z., Wang, M., Jia, R., Chen, S., Liu, M., Zhu, D., Zhao, X., Wu, Y., Yang, Q., Huan, J., Ou, X., Mao, S., Gao, Q., Sun, D., Tian, B., & Cheng, A. (2021). Distribution and association of antimicrobial resistance and virulence traits in Escherichia coli isolates from healthy waterfowls in Hainan, China. Ecotoxicology and Environmental Safety, 220, 112317. https://doi.org/10.1016/J.ECOENV.2021.112317 DOI: https://doi.org/10.1016/j.ecoenv.2021.112317
- Zotta, C. M., Lavayén, S., Nario, F., & Piquín, A. (2016). Detección de Escherichia coli productor de toxina Shiga en vísceras e animales bovinos y pollos destinadas para el consumo humano. Journal of the Selva Andina Research Society, 7(1), 2–9. https://doi.org/10.36610/j.jsars.2016.070100002 DOI: https://doi.org/10.36610/j.jsars.2016.070100002
- Zhuge, X., Jiang, M., Tang, F., Sun, Y., Ji, Y., Xue, F., ... & Dai, J. (2019). Avian-source mcr-1-positive Escherichia coli is phylogenetically diverse and shares virulence characteristics with E. coli causing human extra-intestinal infections. Veterinary microbiology, 239, 108483. 10.1016/j.vetmic.2019.108483 DOI: https://doi.org/10.1016/j.vetmic.2019.108483