Role of the Environment in the Transmission of Antimicrobial Resistance to Humans: A Review

Abstract

To establish a possible role for the natural environment in the transmission of clinically relevant AMR bacteria to humans, a literature review was conducted to systematically collect and categorize evidence for human exposure to extended-spectrum β-lactamase-producing Enterobacteriaceae, methicillin-resistant Staphylococcus aureus, and vancomycin-resistant Enterococcus spp. in the environment. In total, 239 datasets adhered to inclusion criteria. AMR bacteria were detected at exposure-relevant sites (35/38), including recreational areas, drinking water, ambient air, and shellfish, and in fresh produce (8/16). More datasets were available for environmental compartments (139/157), including wildlife, water, soil, and air/dust. Quantitative data from exposure-relevant sites (6/35) and environmental compartments (11/139) were scarce. AMR bacteria were detected in the contamination sources (66/66) wastewater and manure, and molecular data supporting their transmission from wastewater to the environment (1/66) were found. The abundance of AMR bacteria at exposure-relevant sites suggests risk for human exposure. Of publications pertaining to both environmental and human isolates, however, only one compared isolates from samples that had a clear spatial and temporal relationship, and no direct evidence was found for transmission to humans through the environment. To what extent the environment, compared to the clinical and veterinary domains, contributes to human exposure needs to be quantified. AMR bacteria in the environment, including sites relevant for human exposure, originate from contamination sources. Intervention strategies targeted at these sources could therefore limit emission of AMR bacteria to the environment.

‘Disperse abroad in the land’: the role of wildlife in the dissemination of antimicrobial resistance

“…While some progress has been made in understanding the epidemiology of multi-host infections involving wildlife [2], less attention has been paid to the role of wild animals in the ecology and evolution of antimicrobial resistance (AMR) [3,4]. Although AMR is considered one of the greatest challenges to global health security [5], to date, most AMR research has been based in clinical settings [6].…”

“…Although AMR is considered one of the greatest challenges to global health security [5], to date, most AMR research has been based in clinical settings [6]. Relatively little is known about the flow and fate of AMR in the natural environment [7], particularly in highly mobile species that could act as efficient AMR dispersers [3,4] (figure 1). In this review, we discuss the possible role of wildlife in the dissemination of AMR, specifically how wildlife might acquire and transport AMR and the potential for them to transmit AMR to humans and livestock.…”

Extended-spectrum β-lactamase- and pAmpC-producing Enterobacteriaceae among the general population in a livestock-dense area

“…Potential routes of transmission of ESBL/pAmpC-E to humans are via the food chain [2,3], by direct contact with animals [4] or indirectly via the environment [11,14].…”

“…Enteric bacteria are introduced into the environment with human and animal faeces and residents of rural areas may be exposed to ESBL/pAmpC-E through the air, through contact with contaminated surface water or soil, or through consumption of home grown fresh produce [14]. Usually, people working on a farm have a higher carriage rate of ESBL/pAmpC-E than the general population [4,6].…”

“…Usually, people working on a farm have a higher carriage rate of ESBL/pAmpC-E than the general population [4,6]. Although several studies hypothesize that exposure to ESBL/ pAmpC-E is elevated in close proximity around animal farms [17,18], the risk of this exposure is not clear [14].…”