High Prevalence and Diversity Characteristics of blaNDM, mcr, and blaESBLs Harboring Multidrug-Resistant Escherichia coli From Chicken, Pig, and Cattle in China

Abstract

The objective of this study was to understand the diversity characteristics of ESBL-producing <i>Escherichia coli</i> (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 (<i>n</i> = 89), OXA (<i>n</i> = 59), SHV (<i>n</i> = 7), and TEM (<i>n</i> = 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 <i>bla</i>_NDM-1 or <i>bla</i>_NDM-5, especially, of which four ESBL-EC also contained the colistin resistance gene <i>mcr-1</i>, as confirmed by genomic analysis. More interestingly, two deletion events with a 500-bp deletion in ΔIS<i>Aba125</i> and a 180-bp deletion in <i>dsbC</i> were observed in three <i>bla</i>_NDM-5 IncX3 plasmids, which, as far as we know, is the first discovery. This showed the instability and horizontal transfer of <i>bla</i>_NDM genetic context, suggesting that <i>bla</i>_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 (<i>n</i> = 5), ST189 (<i>n</i> = 5), ST206 (<i>n</i> = 4), ST6396 (<i>n</i> = 3), ST10 (<i>n</i> = 3), and ST155 (<i>n</i> = 3), where ST48 ESBL-EC originated from three food animal species. The STs of all <i>bla</i>_NDM-positive ESBL-EC were attributed to three STs, namely, ST6396 (<i>n</i> = 2), ST206 (<i>n</i> = 2), and ST189 (<i>n</i> = 4), where ST189 was also the unique type for four <i>mcr-1</i>-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.