Long-term carriage and rapid transmission of extended spectrum beta-lactamase-producing E. coli within a flock of Mallards in the absence of antibiotic selection.

Linus Sandegren,Dan I Andersson,Josef D Järhult,Ulrika Lustig,Johan Stedt,Jonas Bonnedahl

doi:10.1111/1758-2229.12681

Abstract

Wild birds have been suggested as transmitters and reservoirs for antibiotic resistant bacteria. We performed an experimental study investigating carriage time and interindividual transmission of extended spectrum beta-lactamase- (ESBL-)producing Escherichia coli in Mallards (Anas platyrhynchos) to assess if the birds carry the bacteria long enough to transfer them geographically during migration. Mallards were inoculated intraoesophageally with four different strains of ESBL-producing E. coli and kept together in a flock. The ESBL-strains belonged to sequence types previously shown to spread between birds and humans. Culturing from faecal samples showed presence of ESBL-producing E. coli the entire 29 day experimental period. An extensive and rapid transmission of the different ESBL-strains between individuals (including non-inoculated controls) was observed. In necropsy samples, we detected ESBL-strains in the cecum even in faeces-negative birds, indicating that this part of the intestine could function as a reservoir of resistant bacteria. We demonstrate that birds can carry ESBL-producing E. coli for long enough times to travel far during migration and the extensive interindividual transmission suggests spread between individuals in a dense bird population as a mechanism that allow persistence of resistant bacteria.

Highlights

Antibiotic resistance is a large and growing threat to the health care and Enterobacteriaceae resistant to the common therapy option cephalosporins through production of Extended Spectrum Beta-Lactamases (ESBLs) represent a continuous clinical problem (Coque et al, 2008)
The mallard is an especially interesting species as it often forages in waterways downstream of sewage treatment plants, where it can be exposed to both antibiotic resistant bacteria and antibiotic residues originating from the sewage water; and it has been shown that 47% of faecal samples from Swedish urban Mallards grew extended spectrum beta-lactamase- (ESBL-)producing E. coli (Hessman et al, 2018)
To assess the carriage time and spread of ESBLproducing E. coli strains among Mallards in a flock, we inoculated four groups of three Mallards each with one of four different ESBL-producing E. coli strains originally isolated from gulls and kept three birds as uninoculated controls (Fig. 1)

Summary

Introduction

Antibiotic resistance is a large and growing threat to the health care and Enterobacteriaceae resistant to the common therapy option cephalosporins through production of Extended Spectrum Beta-Lactamases (ESBLs) represent a continuous clinical problem (Coque et al, 2008). Birds are interesting environmental indicators as they often live close to human settings and are exposed to our bacteria and antibiotic residues through, for example, garbage dumps, sewage treatment plants and agricultural areas. In several bird species living close to humans or feeding from human related products, resistant E. coli have been found, for example, in Mallards Anas platyrhynchos (Literak et al, 2010b), Canada geese Branta canadensis (Cole et al, 2005; Middleton and Ambrose, 2005), feral pigeons Columba livia (Radimersky et al, 2010) and red-billed choughs Pyrrhocorax pyrrhocorax (Blanco et al, 2009). The mallard is an especially interesting species as it often forages in waterways downstream of sewage treatment plants, where it can be exposed to both antibiotic resistant bacteria and antibiotic residues originating from the sewage water; and it has been shown that 47% of faecal samples from Swedish urban Mallards grew ESBL-producing E. coli (Hessman et al, 2018). A recent Polish study demonstrates that mallards can migrate up to 382 km in 1 day (Smietanka et al, 2016), and ring and recovery data show that the mallard can migrate about 1700 km in 1 month [birds reported to the Swedish Bird Ringing Centre (http://www.nrm.se/ english/researchandcollections/environmentalresearchand monitoring/birdringingcentre.214_en.html, data from personal communication, Thord Fransson)]

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