Long-term maintenance of multidrug-resistant Escherichia coli carried by vampire bats and shared with livestock in Peru

Oumar O. Mahamat,Andrés Opazo-Capurro,Daniel G. Streicker,Julio A. Benavides,Carlos Shiva,Sylvain Godreuil,Nestor Falcon,Katarina Oravcova

doi:10.1016/j.scitotenv.2021.152045

Abstract

Extended-spectrum beta-lactamase-producing Escherichia coli (ESBL-E. coli) have been reported in wildlife worldwide. Whether wildlife is a transient host of ESBL-E. coli or comprises an independently maintained reservoir is unknown. We investigated this question by longitudinally monitoring ESBL-E. coli in common vampire bats and nearby livestock in Peru. Among 388 bats from five vampire bat colonies collected over three years, ESBL-E. coli were detected at a low prevalence (10% in 2015, 4% in 2017 and 2018) compared to a high prevalence (48%) from 134 livestock sampled in 2017. All ESBL-E. coli were multidrug-resistant, and whole genome sequencing of 33 randomly selected ESBL-E. coli isolates (18 recovered from bats) detected 46 genes conferring resistance to antibiotics including third-generation cephalosporins (e.g., blaCTX-M-55, blaCTX-M-15, blaCTX-M-65, blaCTX-M-3, blaCTX-M-14), aminoglycosides, fluoroquinolones, and colistin (mcr-1). The mcr-1 gene is reported for the first time on a wild bat in Latin America. ESBL-E. coli also carried 31 plasmid replicon types and 16 virulence genes. Twenty-three E. coli sequence types (STs) were detected, including STs involved in clinical infections worldwide (e.g., ST 167, ST 117, ST 10, ST 156 and ST 648). ESBL-E. coli with identical cgMLST (ST 167) were detected in the same bat roost in 2015 and 2017, and several ESBL-E. coli from different bat roosts clustered together in the cgMLST reconstruction, suggesting long-term maintenance of ESBL-E. coli within bats. Most antibiotic resistance and virulence genes were detected in E. coli from both host populations, while ESBL-E. coli ST 744 was found in a bat and a pig from the same locality, suggesting possible cross-species exchanges of genetic material and/or bacteria between bats and livestock. This study suggests that wild mammals can maintain multidrug-resistant bacteria and share them with livestock.

Highlights

The increase of antimicrobial resistance (AMR) is a major threat to human and animal health (FAO, 2016; WHO, 2017), responsible for thousands of human fatalities annually (WHO, 2014) and economic losses that could reduce global Gross Domestic Product by 1–4% in 2050 (World Bank, 2017)
Two bat colonies (Barranca and Huacho) had bats that carried ESBL-E. coli over two sampling years, while the bat colony in Mala had at least one bat carrying ESBL-E. coli in all three sampling years
This study shows that Multidrug resistance (MDR) ESBL-E. coli circulate in common vampire bat colonies, but occurred at a lower prevalence (5%) than observed in livestock (48%)

Summary

Introduction

The increase of antimicrobial resistance (AMR) is a major threat to human and animal health (FAO, 2016; WHO, 2017), responsible for thousands of human fatalities annually (WHO, 2014) and economic losses that could reduce global Gross Domestic Product by 1–4% in 2050 (World Bank, 2017). Despite frequent reports of AMR in clinically important bacterial species in domestic animals, there are still considerable gaps in our understanding of how AMR circulates between livestock and the remaining natural environment, including sympatric wildlife species (FAO, 2016; Benavides et al, 2018; Guenther et al, 2011). Since most wild animals are not treated with third-generation cephalosporins, ESBL-E. coli in wildlife is often attributed to contamination from humans or livestock (Arnold et al, 2016; Swift et al, 2019; Guenther et al, 2011). The extent that ESBL-E. coli circulates in wildlife is uncertain, its mere presence opens the worrying possibility that wildlife could act as a reservoir for future human or domestic animal infections (Dolejska and Literak, 2019; Poeta et al, 2009)

Methods

Results

Conclusion