Decreasing prevalence of contamination with extended-spectrum beta-lactamase-producing Enterobacteriaceae (ESBL-E) in retail chicken meat in the Netherlands.

Pepijn Huizinga,Ina Willemsen,Alexander W Friedrich,Silvia García-Cobos,Carlo Verhulst,Marjolein Kluytmans-Van Den Bergh,John W Rossen,Jan Kluytmans,Paul H M Savelkoul,Timothy J Johnson

doi:10.1371/journal.pone.0226828

Abstract

Retail chicken meat is a potential source of extended-spectrum beta-lactamase-producing Enterobacteriaceae (ESBL-E). In the past decade, vast national efforts were undertaken to decrease the antibiotic use in the veterinary sector, resulting in a 58% decrease in antibiotic sales in the sector between 2009 and 2014. This decrease in antibiotic use was followed by a decrease in ESBL-E prevalence in broilers. The current study investigates the prevalence of contamination with ESBL-E in retail chicken meat purchased in the Netherlands between December 2013 and August 2015. It looks at associations between the prevalence of contamination with ESBL-E and sample characteristics such as method of farming (free-range or conventional), supermarket chain of purchase and year of purchase. In the current study, 352 chicken meat samples were investigated for the presence of ESBL-E using selective culture methods. Six samples were excluded due to missing isolates or problems obtaining a good quality sequence leaving 346 samples for further analyses. Of these 346 samples, 188 (54.3%) were positive for ESBL-E, yielding 216 ESBL-E isolates (Escherichia coli (n = 204), Klebsiella pneumoniae (n = 11) and Escherichia fergusonii (n = 1)). All ESBL-E isolates were analysed using whole-genome sequencing. The prevalence of contamination with ESBL-E in retail chicken meat decreased from 68.3% in 2014 to 44.6% in 2015, absolute risk difference 23.7% (95% confidence interval (CI): 12.6% - 34.1%). The ESBL-E prevalence was lower in free-range chicken meat (36.4%) compared with conventional chicken meat (61.5%), absolute risk difference 25.2% (95% CI: 12.9% - 36.5%). The prevalence of contamination with ESBL-E varied between supermarket chains, the highest prevalence of contamination was found in supermarket chain 4 (76.5%) and the lowest in supermarket chain 1 (37.8%). Pairwise isolate comparisons using whole-genome multilocus sequence typing (wgMLST) showed that clustering of isolates occurs more frequently within supermarket chains than between supermarket chains. In conclusion, the prevalence of contamination with ESBL-E in retail chicken in the Netherlands decreased over time; nevertheless, it remains substantial and as such a potential source for ESBL-E in humans.

Highlights

Infections with extended-spectrum beta-lactamase-producing Enterobacteriaceae (ESBL-E) are associated with substantial morbidity, mortality and increased costs compared to infections with their susceptible counterparts [1,2,3,4]
The prevalence of contamination with ESBL-E decreased from 68.3% in the period 2014 to 44.6% in the period 2015, absolute risk difference 23.7% or adjusted relative risk of 0.69 and is shown in more detail in S1 Fig. The prevalence of contamination with ESBL-E was lower in free-range chicken meat (36.4%) compared with conventional chicken meat (61.5%), absolute risk difference 25.2% or adjusted relative risk of 0.60, Table 1 and Fig 2
The method of farming was associated with the prevalence of contamination with ESBL-E; free-range chicken meat had a lower ESBL-E prevalence compared with conventional chicken meat

Summary

Introduction

Infections with extended-spectrum beta-lactamase-producing Enterobacteriaceae (ESBL-E) are associated with substantial morbidity, mortality and increased costs compared to infections with their susceptible counterparts [1,2,3,4]. In 2015, about 5% of invasive E. coli isolates (blood- and cerebrospinal-fluid cultures) were resistant to third generation cephalosporins in the Netherlands [8]. This is lower than the European population-weighted mean of 13%. ESBL-E infections were mainly a hospital-related problem with acquisition in hospitals or related to healthcare contact. This has changed in the past two decades with people that have had no healthcare contact being rectal carriers of ESBL-E [10,11]. Research efforts have focussed on uncovering routes of transmission and reservoirs of antimicrobial resistant microorganisms and resistance genes by using a one-health approach that includes humans, animals and the environment as an interconnected entity

Objectives

Methods

Results

Conclusion