Antibiotic resistance and zoonotic potential of Escherichia coli strains isolated from poultry agro-industrial complex

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Resumo

Poultry is a source of antibiotic-resistant and potentially pathogenic Escherichia coli, which can circulate in enterprises and enter the environment through organic waste. The aim of the study was to analyze antimicrobial resistance profiles, pathogenicity genes and phylogroups of E. coli strains circulating in poultry farms in the Perm Region. The strains of three different groups were studied: those isolated from healthy birds (n = 16), chickens with colibacteriosis (n = 28) and organic waste (n = 19). PCR was used to detect antibiotic resistance and virulence-associated genes. In each of the groups, multidrug-resistant E. coli were found in 18.8 %, 75 % and 73.7 % of cases, respectively. Up to 6 antibiotic resistance genes were detected in E. coli genomes. The beta-lactamase blaTEM gene was found most often in all groups. More than half of the E. coli obtained from sick chickens carried blaCTX–M. A high proportion of E. coli encoding SHV type beta-lactamase (63.2 %) was found in the organic waste. Among them, the tetA efflux system gene was detected more often, and in this group more than 20 % of E. coli had the genes encoding QnrB and QnrS proteins responsible for plasmid-mediated resistance to fluoroquinolones. Most of the strains obtained from healthy birds belonged to phylogroup E, from sick birds – to B1, isolated from organic waste – to C or E. Avian pathogenic E. coli (APEC), including high-risk clones, were found with high frequency in the group of sick birds (75 %), were found in the group of healthy birds (6.3 %) and were preserved in organic waste (63.2 %). Most of the analyzed E. coli (54 %) carried combinations of marker genes both extraintestinal and intestinal E. coli, which indicates their high zoonotic potential.

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Sobre autores

M. Kuznetsova

Perm Federal Research Center of the Ural Branch of the Russian Academy of Sciences

Autor responsável pela correspondência
Email: mar19719@yandex.ru

Institute of Ecology and Genetics of Microorganisms of the Ural Branch of the Russian Academy of Sciences

Rússia, 614081, Perm, ul. Goleva, 13

Yu. Pospelova

Perm Federal Research Center of the Ural Branch of the Russian Academy of Sciences

Email: mar19719@yandex.ru

Institute of Ecology and Genetics of Microorganisms of the Ural Branch of the Russian Academy of Sciences

Rússia, 614081, Perm, ul. Goleva, 13

V. Mihailovskaya

Perm Federal Research Center of the Ural Branch of the Russian Academy of Sciences

Email: mar19719@yandex.ru

Institute of Ecology and Genetics of Microorganisms of the Ural Branch of the Russian Academy of Sciences

Rússia, 614081, Perm, ul. Goleva, 13

D. Kochergina

Perm Federal Research Center of the Ural Branch of the Russian Academy of Sciences

Email: mar19719@yandex.ru

Institute of Ecology and Genetics of Microorganisms of the Ural Branch of the Russian Academy of Sciences

Rússia, 614081, Perm, ul. Goleva, 13

Bibliografia

  1. Hedman H. D., Vasco K. A., Zhang L. A. Review of antimicrobial resistance in poultry farming within low-resource settings // Animals. 2020. Vol. 10. Article 1264. URL: https://www.mdpi.com/2076–2615/10/8/1264 (дата обращения: 01.04.2024). doi: 10.3390/ani10081264.
  2. Влияние антибиотиков, использующихся в животноводстве, на распространение лекарственной устойчивости бактерий (обзор) / И. С. Сазыкин, Л. Е. Хмелевцова, Е. Ю. Селиверстова и др. // Прикладная биохимия и микробиология. 2021. Т. 57. № 1. С. 24–35.
  3. Use of antibiotics in broiler production: Global impacts and alternatives / Y. Mehdi, M. P. Létourneau-Montminy, M. L. Gaucher, et al. // Animal nutrition. 2018. Vol. 4. No. 2. P. 170–178 URL: https://pubmed.ncbi.nlm.nih.gov/30140756/ (дата обращения: 01.04.2024). doi: 10.1016/j.aninu.2018.03.002.
  4. Щепеткина С. В. Антибиотики в птицеводстве: запретить нельзя нормировать // Эффективное животноводство. 2019. № 4. С. 85–87.
  5. Antibiotic resistance and virulence factors among Escherichia coli isolates from avian organic fertilizer / J. M. A. Agostinho, M. V. Cardozo, M. M. Borzi, et al. // Ciência Rural. 2020. Vol. 50. No. 2. Article e20180849. URL: https://www.scielo.br/j/cr/a/GdwZcDsCbBKhXhhQ4VLRhSz/?lang=en (дата обращения: 01.04.2024). doi: 10.1590/0103-8478cr20180849.
  6. Prevalence of antibiotic resistant Escherichia coli strains isolated from farmed broilers and hens in Greece, based on phenotypic and molecular analyses / A. Xexaki, D. K. Papadopoulos, M. V. Alvanou, et al. // Sustainability. 2023. Vol. 15. Article 9421. URL: https://www.mdpi.com/2071-1050/15/12/9421 (дата обращения: 01.04.2024). doi.org/10.3390/su15129421.
  7. Antibiotic use in agriculture and its consequential resistance in environmental sources: potential public health implications / С. Manyi-Loh, S. Mamphweli, E. Meyer, et al. // Molecules. 2018. Vol. 23. No. 4. Article 795. URL: https://www.mdpi.com/1420-3049/23/4/795 (дата обращения: 01.04.2024). doi: 10.3390/molecules23040795.
  8. Escherichia coli from animal reservoirs as a potential source of human extraintestinal pathogenic E. coli / L. Bélanger, A. Garenaux, J. Harel, et al. // FEMS immunology and medical microbiology. 2011. Vol. 62. No. 1. P. 1–10. URL: https://academic.oup.com/femspd/article/62/1/1/519216?login=false (дата обращения: 14.04.2024). doi: 10.1111/j.1574-695X.2011.00797.x.
  9. Evaluation of Escherichia coli isolates from healthy chickens to determine their potential risk to poultry and human health / Z. R. Stromberg, J. R. Johnson, J. M. Fairbrother, et al. // PLoS One. 2017. Vol. 3. No. 12. Article e0180599. URL: https://journals.plos.org/plosone/article?id=10.1371/journal.pone.0180599 (дата обращения: 14.04.2024). doi: 10.1371/journal.pone.0180599.
  10. Zoonotic approach to Shiga toxin-producing Escherichia coli: integrated analysis of virulence and antimicrobial resistance in ruminants and humans / B. Oporto, M. Ocejo, M. Alkorta, et al. // Epidemiology and infection. 2019. Vol. 147. Article e164. URL: https://pubmed.ncbi.nlm.nih.gov/31063106/ (дата обращения: 14.04.2024). doi: 10.1017/S0950268819000566.
  11. Distribution of pathogenicity island (PAI) markers and phylogenetic groups in diarrheagenic and commensal Escherichia coli from young children / G. Naderi, F. Haghi, H. Zeighami, et al. // Gastroenterology and hepatology from bed to bench. 2016. Vol. 9. No. 4. P. 316–324.
  12. Kaper B., Nataro J. P., Mobley H. L. Pathogenic Escherichia coli // Nature reviews. Microbiology. 2004. Vol. 2. No. 2. P. 123–140. URL: https://www.nature.com/articles/nrmicro818 (дата обращения: 14.04.2024). doi: 10.1038/nrmicro818.
  13. Manges A. R., Johnson J. R., Food-borne origins of Escherichia coli causing extraintestinal infections // Clinical infectious diseases: an official publication of the Infectious Diseases Society of America. 2012. Vol. 55. No. 5. P. 712–719. URL: https://academic.oup.com/cid/article-abstract/55/5/712/351325?redirectedFrom=fulltext (дата обращения: 14.04.2024). doi: 10.1093/cid/cis502.
  14. Mellata M. Human and avian extraintestinal pathogenic Escherichia coli: infections, zoonotic risks, and antibiotic resistance trends // Foodborne pathogens and disease. 2013. Vol. 10. No. 11. P. 916–932. URL: https://www.liebertpub.com/doi/10.1089/fpd.2013.1533 (дата обращения: 17.04.2024). doi: 10.1089/fpd.2013.1533.
  15. Refining the definition of the avian pathogenic Escherichia coli (APEC) pathotype through inclusion of high-risk clonal groups / T. J. Johnson, E. A. Miller, C. Flores-Figueroa, et al. // Poultry Science. 2022. Vol. 101. No. 10. Article 102009. URL: https://www.sciencedirect.com/science/article/pii/S0032579122003005?via%3Dihub (дата обращения: 17.04.2024). doi: 10.1016/j.psj.2022.102009.
  16. Diversity of hybrid- and hetero-pathogenic Escherichia coli and their potential implication in more severe diseases / A.C.M. Santos, F. F. Santos, R. M. Silva, et al. // Frontiers in cellular and infection microbiology. 2020. Vol. 10. Article 339. URL: https://www.frontiersin.org/journals/cellular-and-infection-microbiology/articles/10.3389/fcimb.2020.00339/full (дата обращения: 17.04.2024). doi: 10.3389/fcimb.2020.00339.
  17. Intensive poultry farming: A review of the impact on the environment and human health / G. Gržinić, A. Piotrowicz-Cieślak, A. Klimkowicz-Pawlas, et al. // The Science of the total environment. 2023. Vol. 1. Article 160014. URL: https://www.sciencedirect.com/science/article/pii/S0048969722071145?via%3Dihub (дата обращения: 17.04.2024). doi: 10.1016/j.scitotenv.2022.160014.
  18. Escherichia coli isolated from cases of colibacillosis in Russian poultry farms (Perm Krai): Sensitivity to antibiotics and bacteriocins / M. V. Kuznetsova, J. S. Gizatullina, L. Y. Nesterova, et al. // Microorganisms. 2020. Vol. 8. No. 5. Article 741. URL: https://www.mdpi.com/2076–2607/8/5/741 (дата обращения: 17.04.2024). doi: 10.3390/microorganisms8050741.
  19. Bacteriocin-producing Escherichia coli isolated from the gastrointestinal tract of farm animals: prevalence, molecular characterization and potential for application / M. V. Kuznetsova, V. S. Mihailovskaya, N. B. Remezovskaya, et al. // Microorganisms. 2022. Vol. 10. Article 1558. URL: https://www.mdpi.com/2076–2607/10/8/1558 (дата обращения: 17.04.2024). doi: 10.3390/microorganisms10081558.
  20. Multidrug-resistant, extensively drug-resistant and pandrug-resistant bacteria: an international expert proposal for interim standard definitions for acquired resistance / A. P. Magiorakos, A. Srinivasan, R. B. Carey, et al. // Clin. Microbiol. Infect. 2012. Vol. 18. P. 268–281. doi: 10.1111/j.1469-0691.2011.03570.x.
  21. Mihailovskaya V. S., Starčič Erjavec M., Kuznetsova M. V. Escherichia coli from healthy farm animals: antimicrobial resistance, resistance genes and mobile genetic elements // Acta Veterinaria Hungarica. 2024. Vol. 72. No. 4. P. 225–234. URL: https://akjournals.com/view/journals/004/72/4/article-p225.xml (дата обращения: 17.04.2024). doi: 10.1556/004.2024.01102.
  22. Comparison of extraintestinal pathogenic Escherichia coli strains from human and avian sources reveals a mixed subset representing potential zoonotic pathogens / T. J. Johnson, Y. Wannemuehler, S. J. Johnson, et al. // Applied and environmental microbiology. 2008. Vol. 74. No. 22. P. 7043–7050. doi: 10.1128/AEM.01395-08.
  23. The Clermont Escherichia coli phylo-typing method revisited: improvement of specificity and detection of new phylo-groups / O. Clermont, J. K. Christenson, E. Denamur, et al. // Environmental microbiology reports. 2013. Vol. 5. No. 1. P. 58–65. doi: 10.1111/1758-2229.12019.
  24. Olaimat A. N., Holley R. A. Factors influencing the microbial safety of fresh produce: a review // Food Microbiology. 2012. Vol. 32. No. 1. P. 1–19. URL: https://www.sciencedirect.com/science/article/abs/pii/S0740002012000986?via%3Dihub (дата обращения: 17.04.2024). doi: 10.1016/j.fm.2012.04.016.
  25. Distribution, numbers, and diversity of ESBL-producing E. coli in the poultry farm environment / H. Blaak, A. H. van Hoek, R. A. Hamidjaja, et al. // PLoS One. 2015. Vol. 10. No. 8. Article e0135402. URL: https://journals.plos.org/plosone/article?id=10.1371/journal.pone.0135402 (дата обращения: 20.04.2024). doi: 10.1371/journal.pone.0135402.
  26. Antimicrobial resistance of commensal Escherichia coli from food-producing animals in Russia / D. A. Makarov, O. E. Ivanova, S. Y. Karabanov, et al. // Veterinary world. 2020. Vol. 13. No. 10. P. 2053–2061. doi: 10.14202/vetworld.2020.2053-2061.
  27. Szmolka A., Nagy B. Multidrug resistant commensal Escherichia coli in animals and its impact for public health, Frontiers in microbiology, 2013, vol. 4, Article 258. URL: https://www.frontiersin.org/journals/microbiology/articles/10.3389/fmicb.2013.00258/full (дата обращения: 20.04.2024). doi: 10.3389/fmicb.2013.00258.
  28. Prevalence and molecular characterization of extended-spectrum β-lactamases and AmpC β-lactamase-producing Enterobacteriaceae among human, cattle, and poultry / M. A. Nossair, F. A. Abd El Baqy, M. S. Y. Rizk, et al. // Pathogens. 2022. Vol. 11. No. 8. Article 852. URL: https://www.mdpi.com/2076–0817/11/8/852 (дата обращения: 20.04.2024). doi: 10.3390/pathogens11080852.
  29. Davin-Regli A., Pages J.-M., Ferrand A. Clinical status of efflux resistance mechanisms in gram-negative bacteria // Antibiotics. 2021. Vol. 10. Article 1117. URL: https://www.mdpi.com/2079–6382/10/9/1117 (дата обращения: 20.04.2024). doi.org/10.3390/antibiotics10091117.
  30. Plasmid-mediated quinolone resistance: a multifaceted threat / J. Strahilevitz, G. A. Jacoby, D. C. Hooper, et al. // Clinical microbiology reviews. 2009. Vol. 22. No. 4. P. 664–689. doi: 10.1128/CMR.00016-09.
  31. Характеристика вирулентных штаммов Escherichia coli, выделенных от пациентов с урологической инфекцией / П. В. Слукин, Е. И. Асташкин, Е. М. Асланян и др. // Журнал микробиологии, эпидемиологии и иммунобиологии. 2021. Т. 98. № 6. С. 671–684. doi: 10.36233/0372-9311-134.
  32. Molecular screening of virulence genes in extraintestinal pathogenic Escherichia coli isolated from human blood culture in Brazil / V. L. Koga, G. Tomazetto, P. S. Cyoia, et al. // BioMed Research International. 2014. Article 465054. URL: https://onlinelibrary.wiley.com/doi/10.1155/2014/465054 (дата обращения: 20.04.2024). doi: 10.1155/2014/465054.
  33. Avian-pathogenic Escherichia coli strains are similar to neonatal meningitis E. coli strains and are able to cause meningitis in the rat model of human disease / K. A. Tivendale, C. M. Logue, S. Kariyawasam, et al. // Infection and Immunity. 2010. Vol. 78. P. 3412–3419. doi: 10.1128/IAI.00347-10.
  34. Genome evolution and the emergence of pathogenicity in avian Escherichia coli / L. Mageiros, G. Méric, S. C. Bayliss, et al. // Nature Communications. 2021. Vol. 12. No. 1. Article 765. URL: https://www.nature.com/articles/s41467–021–20988-w (дата обращения: 20.04.2024). doi: 10.1038/s41467-021-20988-w.
  35. Phylogenetic group and virulence profile classification in Escherichia coli from distinct isolation sources in Mexico / J. R. Aguirre-Sánchez, J. B. Valdez-Torres, N. C. Del Campo, et al. // Infection, genetics and evolution. 2022. Vol. 106. Article 105380. URL: https://www.sciencedirect.com/science/article/pii/S1567134822001770?via%3Dihub (дата обращения: 20.04.2024). doi: 10.1016/j.meegid.2022.105380.
  36. Comparative characteristics and pathogenic potential of Escherichia coli isolates originating from poultry farms, retail meat, and human urinary tract infection / J. Sarowska, T. Olszak, A. Jama-Kmiecik, et al. // Life. 2022. Vol. 12. No. 6. Article 845. URL: https://www.mdpi.com/2075–1729/12/6/845 (дата обращения: 20.04.2024). doi: 10.3390/life12060845.
  37. An integrated perspective on virulence-associated genes (VAGs), antimicrobial resistance (AMR), and phylogenetic clusters of pathogenic and non-pathogenic avian Escherichia coli / S. E. Rezatofighi, A. Najafifar, M. Askari Badouei, et al. // Frontiers Veterinary Science. 2021. Vol. 24. No. 8. Article 758124. URL: https://www.frontiersin.org/journals/veterinary-science/articles/10.3389/fvets.2021.758124/full (дата обращения: 20.04.2024). doi: 10.3389/fvets.2021.758124.

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2. Fig. 1. The number of detected antibiotic resistance genes (a) and their distribution between the three groups of E. coli (b).

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3. Fig. 2. The number of detected genes associated with virulence (a) and their distribution between the three groups of E. coli (b).

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4. Fig. 3. Distribution of genes associated with the InPEC, ExPEC and APEC pathotypes in E. coli strains isolated from healthy birds (a), birds with signs of colibacillosis (b), and from organic waste (c). The number on the abscissa axis reflects the number of detected genes.

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5. Fig. 4. Radar plots showing the number of E. coli strains of different phylogroups isolated from healthy birds (a), birds with signs of colibacillosis (b), and from organic waste (c).

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