Abstract

The objective of this study was to understand the diversity characteristics of ESBL-producing Escherichia coli (ESBL-EC) in chicken, pig, and cattle. A high prevalence of ESBL-EC (260/344) was observed in all food animals with prevalence rates of 78.6% (110/140) for chicken, 70.7% (58/82) for cattle, and 75.4% (92/122) for swine. However, the resistance rates presented significant differences in different animal origin ESBL-EC, where resistance to CTX, GEN, IMP, NEO, and OFL was the highest in chicken ESBL-EC, then in cattle, and the lowest in swine. Seriously, most ESBL-EC harbor multidrug resistance to antibiotics (MDR, ≥3 antibiotic categories), and the MDR rates of ESBL-EC were the highest in chicken (98.18%), followed by swine (93.48%), and the lowest in cow (58.62%), while the same trend also was observed in MDR of ≥5 antibiotic categories. This high prevalence and resistance can be partly interpreted by the high carriage rates of the β-lactamases CTX-M (n = 89), OXA (n = 59), SHV (n = 7), and TEM (n = 259). A significant difference of β-lactamase genes also presented in different animal species isolates, where the chicken origin ESBL-EC possessed higher carriage rates of almost all genes tested than cattle and swine. Notably, eight chicken origin ESBL-EC carried transferable plasmid-mediated bla NDM-1 or bla NDM-5, especially, of which four ESBL-EC also contained the colistin resistance gene mcr-1, as confirmed by genomic analysis. More interestingly, two deletion events with a 500-bp deletion in ΔISAba125 and a 180-bp deletion in dsbC were observed in three bla NDM-5 IncX3 plasmids, which, as far as we know, is the first discovery. This showed the instability and horizontal transfer of bla NDM genetic context, suggesting that bla NDM is evolving to “pack light” to facilitate rapid and stable horizontal transfer. Sequence types (STs) and PFGE showed diversity patterns. The most prevalent STs were ST48 (n = 5), ST189 (n = 5), ST206 (n = 4), ST6396 (n = 3), ST10 (n = 3), and ST155 (n = 3), where ST48 ESBL-EC originated from three food animal species. The STs of all bla NDM-positive ESBL-EC were attributed to three STs, namely, ST6396 (n = 2), ST206 (n = 2), and ST189 (n = 4), where ST189 was also the unique type for four mcr-1-carrying ESBL-EC. In conclusion, we suggest that the three animal species ESBL-EC show similar high prevalence, diversity in isolate lineages, and significant discrepancies in antibiotic resistance and resistance genes. This suggests that monitoring and anti-infection of different food animal origin ESBL-EC need different designs, which deserves more attention and further surveillance.

Highlights

  • Antimicrobial resistance (AMR) is a serious threat to public health

  • We identified 260 extended-spectrum blactamase (ESBL)-EC isolates from the 344 fecal samples, including 110 (78.6%, 110/140) from chicken, 58 (70.7%, 58/82) from cattle, and 92 (75.4%, 92/122) from swine

  • BlaTEM-1 was the predominant b-lactamase gene among the animal species screened in this study, and the blaCTX-M-55 gene was the major ESBL gene found in chicken

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Summary

Introduction

Antimicrobial resistance (AMR) is a serious threat to public health. The annual human deaths will rise from the current 0.7 million to 10 million with an estimated $100 trillion in economic losses by 2050 due to AMR (O’Neill, 2016; Friedrich, 2019). The important ARGs in animals are bla, mcr, cfr, and tet genes and their variants (de Alcântara Rodrigues et al, 2020; Ling et al, 2020), where bla (blaKPC, blaNDM, blaVIM, and blaOXA-48/23), mcr, and tet gene-mediated AMR are closely associated to the last resort antibiotics in the human clinic (Guerra et al, 2014). All those ARB and ARGs can transfer to human through the consumption of products of animal origin (de Alcântara Rodrigues et al, 2020). AMR and ARGs in food animals need more attention

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