Anthropogenic environmental drivers of antimicrobial resistance in wildlife

Benjamin M.C Swift,Malcolm Bennett,Katie Waller,Christine Dodd,Annie Murray,Rachel L Gomes,Bethan Humphreys,Jon L Hobman,Michael A Jones,Sophia E Whitlock,Lucy J Mitchell,Rosie J Lennon,Kathryn E Arnold

doi:10.1016/j.scitotenv.2018.08.180

Benjamin M.C Swift, Malcolm Bennett + Show 11 more

Open Access

https://doi.org/10.1016/j.scitotenv.2018.08.180

Copy DOI

Abstract

The isolation of antimicrobial resistant bacteria (ARB) from wildlife living adjacent to humans has led to the suggestion that such antimicrobial resistance (AMR) is anthropogenically driven by exposure to antimicrobials and ARB. However, ARB have also been detected in wildlife living in areas without interaction with humans. Here, we investigated patterns of resistance in Escherichia coli isolated from 408 wild bird and mammal faecal samples. AMR and multi-drug resistance (MDR) prevalence in wildlife samples differed significantly between a Sewage Treatment Plant (STP; wastes of antibiotic-treated humans) and a Farm site (antibiotic-treated livestock wastes) and Central site (no sources of wastes containing anthropogenic AMR or antimicrobials), but patterns of resistance also varied significantly over time and between mammals and birds. Over 30% of AMR isolates were resistant to colistin, a last-resort antibiotic, but resistance was not due to the mcr-1 gene. ESBL and AmpC activity were common in isolates from mammals. Wildlife were, therefore, harbouring resistance of clinical relevance. AMR E. coli, including MDR, were found in diverse wildlife species, and the patterns and prevalence of resistance were not consistently associated with site and therefore different exposure risks. We conclude that AMR in commensal bacteria of wildlife is not driven simply by anthropogenic factors, and, in practical terms, this may limit the utility of wildlife as sentinels of spatial variation in the transmission of environmental AMR.

Highlights

Antimicrobial resistance (AMR) has existed for millions of years, and is an inevitable evolutionary consequence of microbial competition in the environment (D'Costa et al, 2011; Davies and Davies, 2010; Martinez, 2009)
It is often assumed that antimicrobial-resistant bacteria (ARB) in wildlife result from contact with anthropogenic sources such as farms and human waste that pollute the environment with AMR bacteria and/or with antimicrobials (Allen et al, 2010; Clarke and Smith, 2011; Radhouani et al, 2011)
We addressed whether the spatial location where wild birds and mammals were sampled, including proximity to human and livestock wastes, explained variation in: 1) prevalence and genomic diversity of AMR E. coli in birds and mammals; 2) patterns of AMR and Multi-drug resistance (MDR) prevalence in E. coli isolates; and 3) prevalence of phenotypic resistance to medically important antimicrobials and the resistance genes responsible

Summary

Introduction

Antimicrobial resistance (AMR) has existed for millions of years, and is an inevitable evolutionary consequence of microbial competition in the environment (D'Costa et al, 2011; Davies and Davies, 2010; Martinez, 2009). It is often assumed that antimicrobial-resistant bacteria (ARB) in wildlife result from contact with anthropogenic sources such as farms and human waste that pollute the environment with AMR bacteria and/or with antimicrobials (Allen et al, 2010; Clarke and Smith, 2011; Radhouani et al, 2011). Farms on which manure and slurry can be contaminated with ARB, antibiotics (or their metabolites) and other selective drivers of AMR are important habitats for many small mammals and birds, as are sewage treatment plants (STPs) where some birds and mammals feed directly from the bioprocessers (reviewed in Arnold et al, 2016). It is unsurprising that ARB have been found in wild animals in close contact with humans (Allen et al, 2011; Bondo et al, 2016; Furness et al, 2017; Gilliver et al, 1999)

Objectives

Methods

Results

Discussion

Conclusion