Antimicrobial Usages and Antimicrobial Resistance in Commensal Escherichia coli From Veal Calves in France: Evolution During the Fattening Process

Abstract

Extended-Spectrum-Cephalosporin (ESC)-resistant Enterobacteriaceae have widely spread in all settings worldwide. In animals, Extended-Spectrum Beta-Lactamase (ESBL) producers have been frequently identified in veal calves. The objectives of this study were to investigate the trends in the ESBL load and antimicrobial resistance (AMR) proportions, and antimicrobial usages (AMU) in veal calves during the fattening process. Ten fattening farms were selected and 50 animals per farm were sampled. AMR was assessed in bacteria from the dominant flora (collected on non-selective MacConckey agar) and in ESBL/AmpC-carrying bacteria from the subdominant flora (selected on ChromID ESBL selective plates) upon arrival and 5–6 months later before slaughter. The number and types of treatments during fattening were also collected. Rates of ESBL-producing E. coli from the subdominant flora significantly decreased in all farms (arrival: 67.7%; departure: 20.4%) whereas rates of multidrug-resistant E. coli from the dominant flora have significantly increased (arrival: 60.2%; departure: 67.2%; p = 0.025). CTX-M-1 was the most frequently identified ESBL enzyme (arrival: 59.3%; departure: 52.0%). The plasmid-mediated mcr-1 gene was also identified occasionally. In parallel, levels of resistances to non-critically important antimicrobials were already high upon arrival but have still further increased over time until slaughter. Our study also highlighted that if only ESBL-producing isolates were monitored, it might have led to a partial (and partly false) picture of AMR rates globally decreasing during the fattening period. The mean number of antimicrobial treatments per calf (NTPC) was 8.75 but no association between AMU and AMR was evidenced. Most ESBL producers were clonally unrelated suggesting multiple sources and not cross-contaminations among calves during transportation. Feeding milk containing antimicrobial residues to veal calves is hypothesized to explain the high ESBL loads in animals at the entrance on farms.

Farm animals and aquaculture: significant reservoirs of mobile colistin resistance genes

“…However, the prevalence of mcr-1 in bacteria from dairy cattle remains low, ranging from 0.5% to 0.8% in China (He et al, 2017;Bai et al, 2018;Zheng et al, 2019), 2.6% in Egypt (Khalifa et al, 2016), and 0% in Brazil (Palmeira et al, 2018). Overall, there is a greater number of studies in cattle from European countries, including the Netherlands (Veldman et al, 2016), Germany (Falgenhauer et al, 2016), France (Brennan et al, 2016;Haenni et al, 2016;Lupo et al, 2018;Gay et al, 2019), Italy (Alba et al, 2018), Belgium (Malhotra-Kumar et al, 2016), Spain (Hernandez et al, 2017), and Portugal (Clemente et al, 2019), compared with Asian countries, where the majority of such studies comes from China (Wang et al, 2018b) and Japan (Suzuki et al, 2016;Kawanishi et al, 2017). However, levels of colistin resistance are consistently low.…”

Temporal dynamics of the fecal microbiota in veal calves in a 6-month field trial

“…One of the main drivers of such a decrease was the decrease in abundance of the Enterobacteriaceae family, in which 90% of the members were classi ed as E. coli [28]. It is wellknown that commensal E. coli populations of veal calves harbor high levels of antibiotic-resistance genes [3,29], and that they are diverse. Antibiotic treatment may have promoted an increase in the number of speci c pre-existing E. coli strains at the beginning of fattening, as the extended treatments during the rst month did not result in marked depletion of the E. coli population.…”

“…Nevertheless, one of the aims of this study was to characterize the fecal microbiota of calves reared following common veal-farm practices. These three farms, in which eld studies had already been conducted [3], are representative of management practices in the veal-calf industry in France. Second, the calves were only sampled after spending seven days on the farms.…”

Drivers of ESBL-producing Escherichia coli dynamics in calf fattening farms: a modelling study

“…Second, we evaluated the effect of ESBL-EC prevalence on arrival at the fattening farm (on day 1). We extracted from the literature [21] the baseline value of 68% for this prevalence on arrival in France. We assumed that changes in practices on dairy farms where calves were born could decrease this prevalence on arrival, and simulated such reductions.…”

“…The drivers of AMR spread in livestock are not fully understood, although extensive antimicrobial use (AMU) is assumed to play a major role. Previous studies have investigated the relationship between variations in AMU and AMR in livestock at a scale ranging from an entire country [10][11][12] to specific farms [13][14][15][16][17], including cattle farms [18][19][20][21][22]. Some of these studies found an association between AMU and AMR, but not all of them.…”