Resistance to critically important antimicrobials in Australian silver gulls (Chroicocephalus novaehollandiae) and evidence of anthropogenic origins

Abstract

Objectives Antimicrobial resistance (AMR) to critically important antimicrobials (CIAs) amongst Gram-negative bacteria can feasibly be transferred amongst wildlife, humans and domestic animals. This study investigated the ecology, epidemiology and origins of CIA-resistant Escherichia coli carried by Australian silver gulls (Chroicocephalus novaehollandiae), a gregarious avian wildlife species that is a common inhabitant of coastal areas with high levels of human contact. Methods Sampling locations were widely dispersed around the perimeter of the Australian continent, with sites separated by up to 3500 km. WGS was used to study the diversity and molecular characteristics of resistant isolates to ascertain their epidemiological origin. Results Investigation of 562 faecal samples revealed widespread occurrence of extended-spectrum cephalosporin-resistant (21.7%) and fluoroquinolone-resistant (23.8%) E. coli. Genome sequencing revealed that CIA-resistant E. coli isolates (n = 284) from gulls predominantly belonged to human-associated extra-intestinal pathogenic E. coli (ExPEC) clones, including ST131 (17%), ST10 (8%), ST1193 (6%), ST69 (5%) and ST38 (4%). Genomic analysis revealed that gulls carry pandemic ExPEC-ST131 clades (O25:H4 H30-R and H30-Rx) and globally emerging fluoroquinolone-resistant ST1193 identified among humans worldwide. Comparative analysis revealed that ST131 and ST1193 isolates from gulls overlapped extensively with human clinical isolates from Australia and overseas. The present study also detected single isolates of carbapenem-resistant E. coli (ST410-blaOXA-48) and colistin-resistant E. coli (ST345-mcr-1). Conclusions The carriage of diverse CIA-resistant E. coli clones that strongly resemble pathogenic clones from humans suggests that gulls can act as ecological sponges indiscriminately accumulating and disseminating CIA-resistant bacteria over vast distances.

Gulls as Sources of Environmental Contamination by Colistin-resistant Bacteria

“…Because the mcr-1 gene is typically located on mobile genetic elements, it may be transferred among bacteria through horizontal gene transfer 4 ; some bacterial infections could become difficult or impossible to treat if colistin resistance spreads to bacteria resistant to other antimicrobials 5 . Since 2015, mcr-1 has been detected in at least 31 countries on six continents, including in the U.S. 5,6 , where it has been detected in human and domestic swine isolates from 21 states 7 .…”

Think before you prescribe: how dentistry contributes to antibiotic resistance

“…The role of resident ARGs in commensal bacteria in the development and transmission of resistance is not fully understood. Transmission of ARGs need to be considered beyond interactions amongst humans, as recent evidence indicates that wildlife and domestic animals act as ‘ecological sponges’ of ARGs . A number of resistance strains have been identified in diverse animal populations from companion animals, livestock, to wild boar and seagulls.…”

“…Genome sequencing has revealed that strains belonging to human‐associated pathogenic clones, such as Escherichia coli , have been found in Australian silver gulls. Further study is required to understand the effects of dissemination of ARGs of these animal populations, particularly those that can travel significant distances …”

“…Transmission of ARGs need to be considered beyond interactions amongst humans, as recent evidence indicates that wildlife and domestic animals act as 'ecological sponges' of ARGs. 16 A number of resistance strains have been identified in diverse animal populations from companion animals, livestock, to wild boar and seagulls. Genome sequencing has revealed that strains belonging to human-associated pathogenic clones, such as Escherichia coli, have been found in Australian silver gulls.…”

“…Further study is required to understand the effects of dissemination of ARGs of these animal populations, particularly those that can travel significant distances. 16 More recent definitions of resistance have moved away from a species-centric to a gene-based definition, which considers the basic ecological function of ARGs in all environments and focuses on how the use of antibiotics by humans has resulted in altering the ecological function of resistance genes (see Fig. 1).…”