Chicken Meat-Associated Enterococci: Influence of Agricultural Antibiotic Use and Connection to the Clinic

Abstract

Industrial farms are unique, human-created ecosystems that provide the perfect setting for the development and dissemination of antibiotic resistance. Agricultural antibiotic use amplifies naturally occurring resistance mechanisms from soil ecologies, promoting their spread and sharing with other bacteria, including those poised to become endemic within hospital environments. To better understand the role of enterococci in the movement of antibiotic resistance from farm to table to clinic, we characterized over 300 isolates of Enterococcus cultured from raw chicken meat purchased at U.S. supermarkets by the Consumers Union in 2013. Enterococcus faecalis and Enterococcus faecium were the predominant species found, and antimicrobial susceptibility testing uncovered striking levels of resistance to medically important antibiotic classes, particularly from classes approved by the FDA for use in animal production. While nearly all isolates were resistant to at least one drug, bacteria from meat labeled as raised without antibiotics had fewer resistances, particularly for E. faecium. Whole-genome sequencing of 92 isolates revealed that both commensal- and clinical-isolate-like enterococcal strains were associated with chicken meat, including isolates bearing important resistance-conferring elements and virulence factors. The ability of enterococci to persist in the food system positions them as vehicles to move resistance genes from the industrial farm ecosystem into more human-proximal ecologies. IMPORTANCE Bacteria that contaminate food can serve as a conduit for moving drug resistance genes from farm to table to clinic. Our results show that chicken meat-associated isolates of Enterococcus are often multidrug resistant, closely related to pathogenic lineages, and harbor worrisome virulence factors. These drug-resistant agricultural isolates could thus represent important stepping stones in the evolution of enterococci into drug-resistant human pathogens. Although significant efforts have been made over the past few years to reduce the agricultural use of antibiotics, continued assessment of agricultural practices, including the roles of processing plants, shared breeding flocks, and probiotics as sources for resistance spread, is needed in order to slow the evolution of antibiotic resistance. Because antibiotic resistance is a global problem, global policies are needed to address this threat. Additional measures must be taken to mitigate the development and spread of antibiotic resistance elements from farms to clinics throughout the world.

Metagenomic characterization of bacterial community and antibiotic resistance genes in representative ready-to-eat food in southern China

“…The results from the VPA analysis showed that the joint effects of bacterial community shift and MGEs mainly explain the resistome alteration in the RTE food samples. It is known that MGEs alteration were found to affect the ARG profiles directly in commensal and/or potential pathogens found in the food, such as chicken and vegetable 57 , 58 . However, the role of the bacterial community shift for ARGs change in the food was few explored.…”

Prevalence of an Intestinal ST40 Enterococcus faecalis over Other E. faecalis Strains in the Gut Environment of Mice Fed Different High Fat Diets

“…However, in later years, studies on the recently isolated strains in Europe uncovered the epidemiological success of other CCs, displacing CC9 as a potentially risky lineage [20] and also reporting CC9 as a commensal isolated from porcine milk [21] or migrating birds [22]. Regarding ST40, which was previously described as the most frequent ST according to a large collection [17], it was defined as an emerging epidemic clone, probably the most prevalent in Central Europe [23], and its presence in epidemiological reports has been maintained across Europe [24,25] and elsewhere [26]. More recently, a comprehensive analysis of 42 ST40 isolates from different sources and geographical origins [27], including a D32 strain whose genome had been fully sequenced [28], gave new information about this sequence type.…”

“…E. faecalis population structures have repeatedly been studied using multilocus sequencing typing (MLST), and some clonal complexes have been found to be enriched among clinical strains, while commensal isolates are more frequently found in others [ 15 ]. Following this epidemiology-oriented investigation, much effort has been taken to evaluate the safety of the E. faecalis strains that can be found in different types of food [ 16 , 17 , 18 ]. However, to our knowledge, nothing has been done on how the intake of different foods may influence the safety of the prevalent E. faecalis strains in the host intestines, contributing to or preventing certain clinical isolates from spreading in the host community.…”

A Review of Antimicrobial Resistance in Poultry Farming within Low-Resource Settings

“…The connection between antimicrobial use (AMU) and selection for resistance has been extensively studied [ 4 , 5 , 6 ]. Studies have widely documented agricultural AMR emergence leading to resistance in clinical settings [ 7 , 8 , 9 , 10 , 11 , 12 , 13 ]. Within the United States, 80% of antimicrobial agents produced are applied to animal production; [ 14 ] and globally over 70% of global antimicrobials produced on Earth are used in food-animal production [ 7 , 15 , 16 ].…”