High prevalence and diversity of extended-spectrum β-lactamase and emergence of OXA-48 producing Enterobacterales in wildlife in Catalonia.

Laila Darwich,Alba Casado,Andreu Albamonte,Ferrán López,Rafael A Molina-López,Lourdes Migura-Garcia,Anna Vidal,Chiara Seminati,Monica Cartelle Gestal

doi:10.1371/journal.pone.0210686

Laila Darwich, Alba Casado + Show 7 more

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https://doi.org/10.1371/journal.pone.0210686

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Abstract

Most of the studies focused on antimicrobial resistance (AMR) performed in wildlife describe Escherichia coli as the principal indicator of the selective pressure. In the present study, several species of Enterobacterales with a large panel of cephalosporin resistant (CR) genes have been isolated from wildlife in Catalonia. A total of 307 wild animals were examined to determine the prevalence of CR enterobacteria, AMR phenotypes and the presence of common carbapenem and CR genes. The overall prevalence of CR-phenotype was 13% (40/307): 17.3% in wild mammals (18/104) and 11.5% in wild birds (22/191) (p<0.01). Hedgehogs showed the highest prevalence (13.5% of 104) of the mammal specimens, and raptors the highest in bird specimen (7.3% of 191). Although CR E. coli was the most frequently isolated (45%), other CR- Enterobacterales like Klebsiella pneumoniae (20%), Citrobacter freundii (15%), Enterobacter cloacae (5%), Proteus mirabilis (5%), Providencia spp (5%) and Serratia marcescens (2.5%) were also isolated. A high diversity of CR genes was identified among the isolates, with 50% yielding blaCMY-2, 23% blaSHV-12, 20% blaCMY-1 and 18% blaCTX-M-15. Additionally, resistance to carbapenems associated to OXA-48 gene was found. Most of the CR isolates, principally K. pneumoniae and C. freundii, were multi-resistant with co-resistance to fluoroquinolones, tetracycline, sulphonamides and aminoglycosides. This study reports high prevalence of Enterobacterales harbouring a variety of CR genes and OXA-48 mediated-carbapenem resistance, all of them frequently associated to nosocomial human infections, for the first time in wild mammals and wild birds. Implementation of control measures to reduce the impact of anthropogenic pressure in the environment is urgently needed.

Highlights

In the last decades, the prevalence of opportunistic and antimicrobial resistant (AMR) bacteria associated with nosocomial infections has increased in hospital settings
We report for the first time in Spain, the presence of diverse families of cephalosporin resistant (CR)-encoding genes in a large variety of Enterobacterales including E. coli, K. pneumoniae, Citrobacter freundii, Enterobacter cloacae, Serratia marcescens and Proteus mirabilis- in wild mammals and wild birds
We describe the presence of carbapemenase resistant E. coli and P. mirabilis associated with the presence of OXA-48 variant in isolates of wildlife origin

Summary

Introduction

The prevalence of opportunistic and antimicrobial resistant (AMR) bacteria associated with nosocomial infections has increased in hospital settings. Extended-spectrum β-lactamases (ESBLs) and AmpC-type β-lactamases (AmpC) are the most common enzymes that confer resistance to broad-spectrum cephalosporins among members of the family Enterobacterales. These β-lactamases have extensively diversified in response to the clinical use of new generation drugs: cephalosporins, carbapenems and monobactams [2]. The second classification, described by Bush and Jacoby (2010) is based on the functional activity of the enzymes Within this classification, the group 1 contains cephalosporinases encoded in the chromosome of many Enterobacterales, such as AmpC, CMY, ACT, FOX and MIR. The group 2 serine beta-lactamase represents the largest group with a broad spectrum against penicillins, cephalosporins, and carbapenems They include the TEM, SHV, CTX, OXA and KPC enzymes. The group 3 metallo-beta-lactamases (MBLs) are zinc dependent and include NDM, IMP, VIM and SPM enzymes [5]

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