Abstract

In order to evaluate whether seagulls living on the Lisbon coastline, Portugal, might be colonized and consequently represent potential spreaders of multidrug-resistant bacteria, a total of 88 gull fecal samples were screened for detection of extended-spectrum β-lactamase (ESBL)- or carbapenemase-producing Enterobacteriaceae for methicillin-resistant Staphylococcus aureus (MRSA) and for vancomycin-resistant Enterococci (VRE). A large proportion of samples yielded carbapenemase- or ESBL-producing Enterobacteriaceae (16% and 55%, respectively), while only two MRSA and two VRE were detected. Mating-out assays followed by PCR and whole-plasmid sequencing allowed to identify carbapenemase and ESBL encoding genes. Among 24 carbapenemase-producing isolates, there were mainly Klebsiella pneumoniae (50%) and Escherichia coli (33%). OXA-181 was the most common carbapenemase identified (54%), followed by OXA-48 (25%) and KPC-2 (17%). Ten different ESBLs were found among 62 ESBL-producing isolates, mainly being CTX-M-type enzymes (87%). Co-occurrence in single samples of multiple ESBL- and carbapenemase producers belonging to different bacterial species was observed in some cases. Seagulls constitute an important source for spreading multidrug-resistant bacteria in the environment and their gut microbiota a formidable microenvironment for transfer of resistance genes within bacterial species.

Highlights

  • Enterobacteriaceae producing extended-spectrum β-lactamases (ESBL) and/or carbapenemases are a major concern in the healthcare setting, and frequently recovered, mainly as colonizers, in the community, among livestock, and in the environment

  • Multidrug resistance is a major concern in Portuguese hospitals: (a) the prevalence of ESBL producers in invasive K. pneumoniae was estimated as 50% in 2018, considerably overcoming the European rate (31.7%); (b) in recent years, there has been a notorious increasing trend in carbapenem resistance among K. pneumoniae; (c) the prevalence of methicillin-resistant Staphylococcus aureus (MRSA) is still one of the highest in Europe (38.1%); (d) while a decreasing trend has been concomitantly observed with vancomycin-resistant Enterococci (VRE) and, in particular, Enterococcus faecium [11]

  • Our study revealed frequent occurrence of carbapenemase- and ESBL-producing Enterobacteriaceae (16% and 55%, respectively) colonizing gulls from the Lisbon coastline, Portugal

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Summary

Introduction

Enterobacteriaceae producing extended-spectrum β-lactamases (ESBL) and/or carbapenemases are a major concern in the healthcare setting (mostly Klebsiella pneumoniae), and frequently recovered, mainly as colonizers, in the community, among livestock, and in the environment (mostly Escherichia coli). Gulls have been reported as carriers of ESBL-producing E. coli in Europe, South America, North America, and Asia [2,3,4,5,6]. Multidrug resistance is a major concern in Portuguese hospitals: (a) the prevalence of ESBL producers in invasive K. pneumoniae was estimated as 50% in 2018, considerably overcoming the European rate (31.7%); (b) in recent years, there has been a notorious increasing trend in carbapenem resistance among K. pneumoniae (from 1.8% in 2014 to 11.7% in 2018); (c) the prevalence of methicillin-resistant Staphylococcus aureus (MRSA) is still one of the highest in Europe (38.1%); (d) while a decreasing trend has been concomitantly observed with vancomycin-resistant Enterococci (VRE) and, in particular, Enterococcus faecium (from 20.3% in 2015 to 4.4% in 2018) [11]

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