Antimicrobial resistance profiles in Escherichia coli isolated from whole-chicken carcasses from conventional, antibiotic-free, and organic rearing systems
DOI:
https://doi.org/10.5433/1679-0359.2022v43n5p2093Keywords:
Alternative production system, Antibiotic restriction, Food-production animals, Public health.Abstract
Antimicrobial resistance (AMR) is a growing concern in human and animal health. Public discussions on these issues have contributed to an increased demand for antibiotic-free food. Studies comparing the antimicrobial resistance profiles of bacteria in foodstuffs originating from farming systems with restrictions on the use of antimicrobials are scarce. This study aimed to assess the antimicrobial resistance profiles of generic Escherichia coli isolated from whole chickens originating from farming systems with and without restrictions on the use of antimicrobials. For this purpose, three groups of E. coli strains were formed: (GC) from chickens reared in conventional production systems, without restriction on the use of antimicrobials (n=72); (GL) from chickens reared in farming systems certified as free of any antibiotic use (n=72); and (GO) from chickens from an organic farming system (n=72). Whole chicken units were individually rinsed as recommended by ISO 17604:2015, and E. coli was isolated from the rinse suspension. To evaluate the resistance profile, E. coli strains were tested against 12 antimicrobials using broth microdilution or disk diffusion tests. Eighty strains (40.7%) were found to be fully susceptible to the tested antimicrobials, and 23.6% were multidrug resistant. The highest frequencies of resistance were observed to tetracycline (GC=37,5%; GL=34,7%; GO=25%) and trimethoprim (GC=27,8%; GL=34,7%; GO=22,2%). In the case of multidrug resistant strains, GC presented 32% (n=23) of strains with multidrug resistance characteristics whereas the GL and GO groups presented 22% (n=16) and 17% (n=12), respectively. As for the totally susceptible strains, a frequency of 56% of Tsus strains was observed in the organic group, whereas this frequency was 33% in the GC and GL groups. Using GC as a reference, the Poisson regression model showed a higher occurrence of fully susceptible E. coli strains, as well as lower frequencies of multidrug resistance and resistance to ampicillin and nalidixic acid in GO. The GL group exhibited the lowest frequency of ampicillin resistance. These observations suggest that the lower selection pressure for antimicrobial use in the farming system may be reflected in the resistance profile of bacteria present in foodstuffs purchased by consumers.Downloads
References
Agyare, C., Boamah, V. E., Zumbi, C. N., & Osei, F. B. (2018). Antibiotic use in poultry production and its effects on bacterial resistance. In Y. Kumar (Ed.), Antimicrobial resistance - a global threat [Online]. London: IntechOpen. doi: 10.5772/intechopen.79371
Barbieri, N. L., Pimenta, R. L., Melo, D. A. de, Nolan, L. K., Souza, M. S. de, & Logue, C. M. (2021). mcr-1 Identified in fecal Escherichia coli and avian pathogenic E. coli (APEC) from Brazil. Frontiers in Microbiology, 12(659613). doi: 10.3389/fmicb.2021.659613
Bitrus, A. A., Chuanchuen, R., & Luangtongkum, T. (2018). Emergence of colistin resistance in extended-spectrum beta lactamase producing Enterobacteriaceae isolated from food animals and its public health implication: a review. Journal of Advanced Veterinary and Animal Research, 5(1), 1-11. doi: 10.5455/ javar.2018.e246
Cardoso, M. (2019). Antimicrobial use, resistance and economic benefits and costs to livestock producers in Brazil. OECD Food, Agriculture and Fisheries Papers, 135, 1-44. doi: 10.1787/27137b1e-en
Clinical and Laboratory Standards Institute (2018). Performance standards for antimicrobial susceptibility testing (28nd ed.). Clinical and Laboratory Standards Institute.
Clinical and Laboratory Standards Institute (2020). Performance standards for antimicrobial susceptibility testing (30nd ed.). Clinical and Laboratory Standards Institute.
Davis, G. S., Waits, K., Nordstrom, L., Grande, H., Weaver, B., Papp, K., Horwinski, J., Koch, B., Hungate, B. A., Liu, C. M., & Price, L. B. (2018). Antibiotic-resistant Escherichia coli from retail poultry meat with different antibiotic use claims. BMC Microbiology, 18(174), 7. doi: 10.1186/s12866-018-1322-5
Demattê, L. C., Fº., & Pereira, G. V. (2017). O mercado de frangos e ovos orgânicos e caipira - potencial de mercado. Anais do Seminário Nordestino de Pecuária - PECNordeste, Fortaleza, CE, Brasil, 21. http:// www.cpmo.org.br/cms/publicacoes/1.pdf
Diaz-Sanchez, S., Moscoso, S., Santos, F. S., Andino, A., & Hanning, I. (2015). Antibiotic use in poultry: a driving force for organic poultry production. Food Protection Trends, 35(6), 440-447. https://www. researchgate.net/publication/282332674_Antibiotic_use_in_poultry_A_driving_force_for_organic_poultry_production
Elumba, Z. S., Allera, M. L. M., & Taganas, R. R. R. (2018). Occurrence and antibiotic sensitivity of Escherichia coli and Salmonella spp. in retail chicken meat at selected markets in Valencia City, Bukidnon, Philippines. Asian Journal of Biological and Life Sciences, 7(2), 53-58. doi: 10.5530/ajbls. 2018.7.4
European Centre for Disease Prevention and Control, European Food Safety Authority & Europe Medicines Agency (2017). ECDC, EFSA and EMA Joint Scientific Opinion on a list of outcome indicators as regards surveillance of antimicrobial resistance and antimicrobial consumption in humans and food‐producing animals. EFSA Journal, 15(10), 70. http://doi.wiley.com/10.2903/j.efsa.2017.5017
European Food Safety Authority & European Centre for Disease Prevention and Control (2018). The European Union summary report on antimicrobial resistance in zoonotic and indicator bacteria from humans, animals and food in 2016. EFSA Journal, 16(2), 270. doi: 10.2903/j.efsa.2018.5182
European Food Safety Authority & European Centre for Disease Prevention and Control (2019). The European Union summary report on antimicrobial resistance in zoonotic and indicator bacteria from humans, animals and food in 2017. EFSA Journal, 17(6), 278. doi: 10.2903/j.efsa.2019.5709
Guenther, S., Falgenhauer, L., Semmler, T., Imirzalioglu, C., Chakraborty, T., Röesler, U., & Roschanski, N. (2017). Environmental emission of multiresistant Escherichia coli carrying the colistin resistance gene mcr-1 from German swine farms. Journal of Antimicrobial Chemotherapy, 72(5), 1289-1292. doi: 10. 1093/jac/dkw585
Hofacre, C., Fricke, J., & Inglis, T. (2013). Antimicrobial use in poultry. In S. Giguère DVM, J. F. Prescott, & P. M. Dowling (Eds.), Antimicrobial therapy in veterinary medicine (pp. 569-588). Wiley Blackwell.
Irrgang, A., Roschanski, N., Tenhagen, B. A., Grobbel, M., Skladnikiewicz-Ziemer, T., Thomas, K., Resler, U., & Kasbohrer, A. (2016). Prevalence of mcr-1 in E. coli from livestock and food in Germany, 2010-2015. PLoS One, 11(17), e0159863. doi: 10.1371/journal.pone.0159863.
Jahantigh, M., Samadi, K., Dizaji, R. E., & Salari, S. (2020). Antimicrobial resistance and prevalence of tetracycline resistance genes in Escherichia coli isolated from lesions of colibacillosis in broiler chickens in Sistan, Iran. BMC Veterinary Research, 16(267), 1-6. doi: 10.1186/s12917-020-02488-z
Kampf, G. (2019). Antibiotic resistance can be enhanced in Gram-positive species by some biocidal agents used for disinfection. Antibiotics, 8(13), 15. doi: 10.3390/antibiotics8010013
Landoni, M. F., & Albarellos, G. (2015). The use of antimicrobial agents in broiler chickens. The Veterinary Journal, 205(2015), 21-27. doi: 10.1016/j.tvjl.2015.04.016
Lentz, S. A. M., Dalmolin, T. V., Barth, A. L., & Martins, A. F. (2021). mcr -1 Gene in Latin America: how is it disseminated among humans, animals, and the environment? Frontiers in Public Health, 9(648940). doi: 10.3389/fpubh.2021.648940
Literak, I., Dolejska, M., Rybarikova, J., Cizek, A., Strejckova, P., Vyskocilova, M., Friedman, M., & Klimes, J. (2009). Highly variable patterns of antimicrobial resistance in commensal Escherichia coli isolates from pigs, sympatric rodents, and flies. Veterinary Microbiology, 15(3), 229-237. doi: 10.1089/ mdr.2009.0913
Lopes, H. P., Costa, G. A., Pinto, A. C. L. Q., Machado, L. S., Cunha, N. C., Nascimento, E. R., Pereira, V. L. A., & Abreu, D. L. C. (2020). Detection of the mcr-1 gene in Enteropathogenic Escherichia coli (EPEC) and Shigatoxigenic E. coli (STEC) strains isolated from broilers. Pesquisa Veterinária Brasileira, 40(3), 165-169. doi: 10.1590/1678-5150-PVB-5983
Magiorakos, A. P., Srinvasan, A., Carey, R. B., Carmeli, Y., Falagas, M. E., Giske, C. G., Harbarth, S., Hindler, J. F., Kaahlmeter, G., Olsson-Liljequist, B., Paterson, D. L., Rice, L. B., Stelling, J., Struelens, M. J., Vatopoulos, A., Weber, J. T., & Monnet, D. L. (2012). Multidrug-resistant, extensively drug-resistant and pandrug-resistant bacteria: an international expert proposal for interim standard definitions for acquired resistance. Clinical Microbiology and Infectious Diseases, 18(3), 268-281. doi: 10.1111/j. 1469-0691.2011.03570.x
Millman, J. M., Waits, K., Grande, H., Marks, A. R., Marks, J. C., Price, L. B., & Hungate, B. A. (2013). Prevalence of antibiotic-resistant E. coli in retail chicken: comparing conventional, organic, kosher, and raised without antibiotics. F1000Research, 2(155), 13. doi: 10.12688/f1000research.2-155.v2
Ministério da Agricultura Pecuária e Abastecimento (2009). MAPA. Instrução Normativa n. 26, de 10 de julho de 2009. Diário Oficial da União, Brasília, DF, Brasil.
Ministério da Agricultura Pecuária e Abastecimento (2016). MAPA. Instrução Normativa n. 45, de 22 de novembro de 2016. Diário Oficial da União, Brasília, DF.
Ministério da Saúde (2019a). MS. Instrução Normativa n. 60, de 23 de dezembro de 2019. Diário Oficial da União, Brasil.
Ministério da Saúde (2019b). MS. RESOLUÇÃO - RDC n. 331, de 23 de dezembro 2019. Diário Oficial da União, Brasil.
Monte, D. F., Mem, A., Fernandes, M. R., Cerdeira, L., Esposito, F., Galvão, J. A., Franco, B. D. G. M., Lincopan, N., & Landgraf, M. (2017). Chicken meat as a reservoir of colistin-resistant Escherichia coli strains carrying mcr-1 genes in South America. Antimicrobial Agents and Chemotherapy, 61(5), e02718 -16. doi: 10.1128/AAC.02718-16
Much, P., Sun, H., Lassnig, H., Koeberl-Jelovcan, S., Schliessnig, H., & Stueger, H. P. (2019). Differences in antimicrobial resistance of commensal Escherichia coli isolated from caecal contents of organically and conventionally raised broilers in Austria, 2010-2014 and 2016. Preventive Veterinary Medicine, 171(2019), 104755. doi: 10.1016/j.prevetmed.2019.104755
Musa, L., Proietti, P. C., Branciari, R., Menchetti, L., Bellucci, S., Ranucci, D., Marenzoni, M. L., & Franciosini, M. P. (2020). Antimicrobial susceptibility of Escherichia coli and ESBL-producing Escherichia coli diffusion in conventional, organic and antibiotic-free meat chickens at slaughter. Animals, 10(1215), 12. doi: 10.3390/ani10071215
Musa, L., Proietti, P. C., Marenzoni, M. L., Stefanetti, V., Kika, T. S., Blasi, F., Magistrali, C. F., Toppi, V., Ranucci, D., Branciari, R., & Franciosini, M. P. (2021). Susceptibility of commensal E. coli isolated from conventional, antibiotic-free, and organic meat chickens on farms and at slaughter toward antimicrobials with public health relevance. Antibiotics, 10(11), 1321. doi: 10.3390/antibiotics10111321
Organisation for Economic Cooperation and Development (2020). Meat consumption (indicator). https:// data.oecd.org/agroutput/meat-consumption.htm
Osman, K. M., Kappell, A. D., Elhadidy, M., ElMougy, F., El-Ghany, W. A. A., Orabi, A., Mubarak, A. S., Dawoud, T. M., Hemeg, H. A., Moussa, I. M. I., Hessain, A. M., & Yousef, H. M. Y. (2018). Poultry hatcheries as potential reservoirs for antimicrobial-resistant Escherichia coli: a risk to public health and food safety. Scientific Reports, 8(5859), 14. doi: 10.1038/s41598-018-23962-7
Perrin-Guyomard, A., Bruneau, M., Houée, P., Deleurme, K., Legrandois, P., Poirier, C., Soumet, C., & Sanders, P. (2016). Prevalence of mcr-1 in commensal Escherichia coli from French livestock, 2007 to 2014. Eurosurveillance, European Centre for Diesease Prevention and Control, 21(6), 1-3. doi: 10. 2807/1560-7917.ES.2016.21.6.30135
Pesciaroli, M., Magistrali, C. F., Filippini, G., Epifanio, E. M., Lovito, C., Marchi, L., Maresca, C., Massacci, F. R., Orsini, S., Scoccia, E., Tofani, S., & Pezzotti, G. (2020). Antibiotic-resistant commensal Escherichia coli are less frequently isolated from poultry raised using non-conventional management systems than from conventional broiler. International Journal of Food Microbiology, 314(2020), 108391. doi: 10.1016/j.ijfoodmicro.2019.108391
Puangseree, J., Jeamsripong, S., Prathan, R., Pungpian, C., & Chuanchuen, R. (2021). Resistance to widely-used disinfectants and heavy metals and cross resistance to antibiotics in Escherichia coli isolated from pigs, pork and pig carcass. Food Control, 124(107892), 11. doi: 10.1016/j.foodcont.2021.107892
Quinn, J. P., Markey, B. K., Leonard, F. C., Hartigan, P., Fanning, S., & Fitzpatrick, E. S. (2011). Veterinary microbiology and microbial disease (2nd ed.). John Wiley and Sons.
R Core Team (2013). R: A language and environment for statistical computing. http://www.r-project.org/
Rabello, R. F., Bonelli, R. R., Penna, B. A., Albuquerque, J. P., Souza, R. M., & Cerqueira, A. M. F. (2020). Antimicrobial resistance in farm animals in Brazil: an update overview. Animals, 10(552), 43. doi: 10. 3390/ani10040552
Roth, N., Kasbohrer, A., Mayrhofer, S., Zitz, U., Hofacre, C., & Domig, K. J. (2019). The application of antibiotics in broiler production and the resulting antibiotic resistance in Escherichia coli: a global overview. Poultry Science, 98(4), 1791-1804. doi: 10.3382/ps/pey539
Sanchez, H. M., Whitener, V. A., Thulsiraj, V., Amundson, A., Collins, C., Duran-Gonzalez, M., Giragossian, E., Hornstra, A., Kamel, S., Maben, A., Reynolds, A., Roswell, E., Schmidt, B., Sevigny, L., Xiong, C., & Jay, J. A. (2020). Antibiotic resistance of Escherichia coli isolated from conventional, no antibiotics, and humane family owned retail broiler chicken meat. Animals, 10(2217), 17. doi: 10. 3390/ani10122217
Schwaiger, K., Schmied, E. V., & Bauer, J. (2008). Comparative analysis of antibiotic resistance characteristics of Gram-negative bacteria isolated from laying hens and eggs in conventional and organic keeping systems in Bavaria, Germany. Zoonoses and Public Health, 55(7), 331-341. doi: 10. 1111/j.1863-2378.2008.01151.x
Varga, C., Guerin, M. T., Brash, M. L., Slavic, D., Boerlin, P., & Susta, L. (2019). Antimicrobial resistance in fecal Escherichia coli and Salmonella enterica isolates: a two-year prospective study of small poultry flocks in Ontario, Canada. BMC Veterinary Research, 15(464), 10. doi: 10.1186/s12917-019-2187-z
Wang, L. Y. R., Jokinen, C. C., Laing, C. R., Johnson, R. P., Ziebell, K., & Gannon, V. P. J. (2020). Assessing the genomic relatedness and evolutionary rates of persistent verotoxigenic Escherichia coli serotypes within a closed beef herd in Canada. Microbial Genomics, 6(6), e000376. doi: 10.1099/mgen. 0.000376
World Health Organization (2015). Global action plan on antimicrobial resistance. World Health Organization.
World Health Organization (2019). Critically important antimicrobials for human medicine (6nd Revision). World Health Organization.
Xiong, W., Sun, Y., & Zeng, Z. (2018). Antimicrobial use and antimicrobial resistance in food animals. Environmental Science and Pollution Research, 25(19), 18377-18384. doi: 10.1007/s11356-018-1852-2
Yassin, A. K., Zhang, J., Wang, J., Chen, L., Kelly, P., Butaye, P., Lu, G., Gong, J., Li, M., Wei, L., Wang, Y., Qi, K., Han, X., Price, S., Hathcock, T., & Wang, C. (2017). Identification and characterization of mcr mediated colistin resistance in extraintestinal Escherichia coli from poultry and livestock in China. Federation of European Microbiological Societies - Microbiology Letters, 364(24), 6. doi: 10.1093/femsle/fnx242
Zhang, J., Chen, L., Wang, J., Yassin, A. K., Butaye, P., Kelly, P., Gong, J., Guo, W., Li, J., Li, M., Yang, F., Feng, Z., Jiang, P., Song, C., Wang, Y., You, J., Yang, Y., Price, S., Qi, K., Wang, C. (2018). Molecular detection of colistin resistance genes (mcr-1, mcr-2 and mcr-3) in nasal/oropharyngeal and anal/cloacal swabs from pigs and poultry. Scientific Reports, 8(1), 3705. doi: 10.1038/s41598-018-22084-4
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