Similar Levels of Antimicrobial Resistance in U.S. Food Service Ground Beef Products with and without a “Raised without Antibiotics” Claim

2018 ◽  
Vol 81 (12) ◽  
pp. 2007-2018 ◽  
Author(s):  
AMIT VIKRAM ◽  
ERIC MILLER ◽  
TERRANCE M. ARTHUR ◽  
JOSEPH M. BOSILEVAC ◽  
TOMMY L. WHEELER ◽  
...  
Keyword(s):  
Antimicrobial Resistance ◽  
Production System ◽  
Food Service ◽  
Ground Beef ◽  
Fold Change ◽  
Antimicrobial Use ◽  
Metagenomic Dna ◽  
E Coli ◽  
Log2 Fold Change ◽  
Enterococcus Spp

ABSTRACTU.S. ground beef with “raised without antibiotics” (RWA) label claims are perceived as harboring fewer bacteria with antimicrobial resistance (AMR) than are found in conventional (CONV) ground beef with no such label claim. A total of 370 ground beef samples from CONV (n = 191) and RWA (n = 179) production systems were collected over 13 months from three food service suppliers. The following bacteria were cultured: Escherichia coli, tetracycline-resistant (TETr) E. coli, third-generation cephalosporin-resistant (3GCr) E. coli, Salmonella enterica, TETr S. enterica, 3GCr S. enterica, nalidixic acid–resistant S. enterica, Enterococcus spp., erythromycin-resistant Enterococcus spp., TETr Enterococcus spp., Staphylococcus aureus, and methicillin-resistant S. aureus. TETr E. coli was more frequently detected in CONV ground beef (CONV, 54.2%; RWA, 35.2%; P < 0.01), but supplier (P < 0.01) and production system × suppler interaction (P < 0.01) effects were also significant. Metagenomic DNA was isolated from each sample, and equal amounts of metagenomic DNA were pooled by supplier, month, and production system for 75 pooled samples (38 CONV, 37 RWA). The abundance of aac(6′)-Ie-aph(2″)-Ia, aadA1, blaCMY-2, blaCTX-M, blaKPC-2, erm(B), mecA, tet(A), tet(B), and tet(M) genes was assessed by quantitative PCR. The tet(A) (2.9-log2-fold change, P = 0.04) and tet(B) (5.6-log2-fold change) (P = 0.03) genes were significantly more abundant in RWA ground beef. Phylogenetic analyses revealed that ground beef microbiomes differed more by supplier than by production system. These results were consistent with prior research suggesting antimicrobial use in U.S. beef cattle has minimal impact on the AMR of bacteria found in these products. These results should spur a reevaluation of assumptions regarding the impact of antimicrobial use during U.S. beef production on the AMR of bacteria in ground beef.

Food Service Pork Chops from Three U.S. Regions Harbor Similar Levels of Antimicrobial Resistance Regardless of Antibiotic Use Claims

2019 ◽  
Vol 82 (10) ◽  
pp. 1667-1676 ◽  
Author(s):  
AMIT VIKRAM ◽  
ERIC MILLER ◽  
TERRANCE M. ARTHUR ◽  
JOSEPH M. BOSILEVAC ◽  
TOMMY L. WHEELER ◽  
...  
Keyword(s):  
Antimicrobial Resistance ◽  
Production System ◽  
Antimicrobial Agents ◽  
Production Systems ◽  
Food Service ◽  
Antibiotic Use ◽  
Generation Cephalosporin ◽  
Metagenomic Dna ◽  
E Coli ◽  
Pork Products

ABSTRACT Pork products from animals “raised without antibiotics” (RWA) are assumed to harbor lower levels of antimicrobial resistance (AMR) than conventional (CONV) pork products with no claims regarding use of antimicrobial agents during production. A total of 372 pork chop samples from CONV (n = 190) and RWA (n = 182) production systems were collected over 13 months from three food service suppliers. The following bacteria were cultured: Escherichia coli, tetracycline-resistant (TETr) E. coli, third-generation cephalosporin-resistant (3GCr) E. coli, Salmonella enterica, TETr Salmonella, 3GCr Salmonella, nalidixic acid–resistant Salmonella, Enterococcus spp., TETr Enterococcus, erythromycin-resistant Enterococcus, Staphylococcus aureus, and methicillin-resistant S. aureus. Production system did not significantly impact the detection of cultured bacteria (P > 0.05). Metagenomic DNA was isolated from each sample, and equal amounts of metagenomic DNA were pooled by supplier, month, and production system for 75 pooled samples (38 CONV, 37 RWA). Quantitative PCR was used to assess the abundances of the following 10 AMR genes: aac(6′)-Ie-aph(2″)-Ia, aadA1, blaCMY-2, blaCTX-M, blaKPC-2, erm(B), mecA, tet(A), tet(B), and tet(M). For all 10 AMR genes, abundances did not differ significantly (P > 0.05) between production systems. These results suggest that use of antimicrobial agents during swine production minimally impacts the AMR of bacteria in pork chops.

Antimicrobial resistance in United States retail ground beef with and without label claims regarding antibiotic use

2020 ◽  
Author(s):  
John W. Schmidt ◽  
Amit Vikram ◽  
Enrique Doster ◽  
Kevin Thomas ◽  
Margaret D Weinroth ◽  
...  
Keyword(s):  
Antimicrobial Resistance ◽  
Production System ◽  
Ground Beef ◽  
Antibiotic Use ◽  
Resistant Bacteria ◽  
Antimicrobial Use ◽  
Food Animal ◽  
Antimicrobial Resistance Genes ◽  
Human Health Impacts ◽  
Beef Products

Antibiotics used during food-animal production account for approximately 77% of U.S. antimicrobial consumption by mass. Ground beef products labeled as raised without antibiotics (RWA) are perceived to harbor lower antimicrobial resistance (AMR) levels than conventional (CONV) products with no label claims regarding antimicrobial use. Retail ground beef samples were obtained from 6 U. S. cities. Samples with a RWA or USDA Organic claim ( N = 299) were assigned to the RWA production system. Samples lacking these claims ( N = 300) were assigned to the CONV production system. Each sample was cultured for the detection of five antimicrobial resistant bacteria. Genomic DNA was isolated from each sample and qPCR was used to determine the abundance of ten antimicrobial resistance genes (ARGs). Tetracycline-resistant Escherichia coli (CONV = 46.3%; RWA = 34.4%, P < 0.01) and erythromycin-resistant Enterococcus (CONV = 48.0%; RWA = 37.5%, P = 0.01) were more frequently detected in CONV. Salmonella were detected in 1.2% of samples. The ARG bla CTX-M (CONV = 4.1 log 10 normalized abundance, RWA = 3.8 log 10 normalized abundance, P < 0.01) was more abundant in CONV ground beef. The ARGs mecA (CONV = 4.4 log 10 normalized abundance, RWA = 4.9 log 10 normalized abundance, P = 0.05), tet (A) (CONV = 3.9 log 10 normalized abundance, RWA = 4.5 log 10 normalized abundance, P < 0.01), tet (B) (CONV = 3.9 log 10 normalized abundance, RWA = 4.5 log 10 normalized abundance, P < 0.01), and tet (M) (CONV = 5.4 log 10 normalized abundance, RWA = 5.8 log 10 normalized abundance, P < 0.01) were more abundant in RWA ground beef. Although these results suggest that antimicrobial use during U. S. cattle production does not increase human exposure to AMR via ground beef quantitative microbiological risk assessments are required for authoritative assessments regarding the human health impacts of antimicrobial uses during beef production.

scholarly journals Antimicrobial resistance in commensal Escherichia coli and Enterococcus spp. is influenced by production system, antimicrobial use, and biosecurity measures on Spanish pig farms

2021 ◽  
Vol 7 (1) ◽  
Author(s):  
Oscar Mencía-Ares ◽  
Héctor Argüello ◽  
Héctor Puente ◽  
Manuel Gómez-García ◽  
Edgar G. Manzanilla ◽  
...  
Keyword(s):  
Escherichia Coli ◽  
Antimicrobial Resistance ◽  
Production System ◽  
Production Systems ◽  
Multidrug Resistant ◽  
Antimicrobial Use ◽  
Global Public Health ◽  
E Coli ◽  
Pig Farms ◽  
Surveillance Programs

Abstract Background Antimicrobial resistance (AMR) is a global public health threat consequence of antimicrobial use (AMU) in human and animal medicine. In food-producing animals factors such as management, husbandry or biosecurity may impact AMU. Organic and extensive Iberian swine productions are based on a more sustainable and eco-friendly management system, providing an excellent opportunity to evaluate how sustained differences in AMU impact the AMR in indicator bacteria. Here, we evaluate the usefulness of commensal Escherichia coli and Enterococcus spp. isolates as AMR bioindicators when comparing 37 Spanish pig farms from both intensive and organic-extensive production systems, considering the effect of AMU and biosecurity measures, the last only on intensive farms. Results The production system was the main factor contributing to explain the AMR differences in E. coli and Enterococcus spp. In both bacteria, the pansusceptible phenotype was more common (p < 0.001) on organic-extensive farms when compared to intensive herds. The microbiological resistance in commensal E. coli was, for most of the antimicrobials evaluated, significantly higher (p < 0.05) on intensive farms. In enterococci, the lincosamides usage revealed the association between AMR and AMU, with an increase in the AMR for erythromycin (p < 0.01), quinupristin-dalfopristin (p < 0.01) and the multidrug-resistant (MDR) phenotype (p < 0.05). The biosecurity measures implemented on intensive farms influenced the AMR of these bioindicators, with a slightly lower resistance to sulfamethoxazole (p < 0.01) and the MDR phenotype (p < 0.05) in E. coli isolated from farms with better cleaning and disinfection protocols. On these intensive farms, we also observed that larger herds had a higher biosecurity when compared to smaller farms (p < 0.01), with no significant associations between AMU and the biosecurity scores. Conclusions Overall, this study evidences that the production system and, to a lesser extent, the biosecurity measures, contribute to the AMR development in commensal E. coli and Enterococcus spp., with antimicrobial usage as the main differential factor, and demonstrates the potential value of these bacteria as bioindicators on pig farms in AMR surveillance programs.

scholarly journals Antimicrobial Resistance in Retail Ground Beef with and Without a “Raised Without Antibiotics” Claim

2019 ◽  
Vol 3 (2) ◽  
Author(s):  
J. W. Schmidt ◽  
A. Vikram ◽  
K. Thomas ◽  
T. M. Arthur ◽  
M. Weinroth ◽  
...  
Keyword(s):  
Antimicrobial Resistance ◽  
Production System ◽  
Bacterial Infections ◽  
Meat Products ◽  
Ground Beef ◽  
Animal Production ◽  
Resistant Bacteria ◽  
Antimicrobial Use ◽  
Food Animal ◽  
Antimicrobial Resistance Genes

ObjectivesThe occurrences of human bacterial infections complicated by antimicrobial resistance (AMR) have increased in recent decades. Concerns have been raised that food-animal production practices that incorporate antimicrobials contribute significantly to human AMR exposures since food-animal production accounts for approximately 81% of U.S. antimicrobial consumption by mass. Although empirical studies comparing AMR levels in meat products, including ground beef, are scant ground beef products with Raised without Antibiotics (RWA) label claims are perceived to harbor less AMR than “conventional” (CONV) products with no label claims regarding antimicrobial use. The objective of this research was to determine AMR levels in retail ground beef with and without an RWA label claims.Materials and MethodsRetail ground beef samples were obtained from 6 U.S. cities. Samples were obtained on the following dates: 9/18/2017, 10/30/2017, 11/27/2017. 1/29/2018. 3/5/2018, and 6/11/2018. A total of 599 samples were obtained. Samples with a “Raised without Antibiotics” or USDA Organic claim (N = 299) were assigned to the RWA production system. Samples lacking a “Raised without Antibiotics” claim (N = 300) were assigned to the CONV production system. Each sample was cultured for the detection of five antimicrobial resistant bacteria (ARB). Genomic DNA was isolated from each sample and qPCR was used to determine the abundance of ten antimicrobial resistance genes (ARGs). The impacts of production system and city on ARB detection were assessed by the Likelihood-ratio chi-squared test. The impacts of production system and city on ARG abundance was assessed by two-way ANOVA.ResultsTetracycline-resistant Escherichia coli (CONV = 46.3%; RWA = 34.4%) and erythromycin-resistant Enterococcus (CONV = 48.0%; RWA = 37.5%) were more frequently (P < 0.01) detected in CONV. Detection of third generation cephalosporin-resistant E. coli (CONV = 5.7%; RWA = 1.0%), vancomycin-resistant Enterococcus (CONV = 0.0%; RWA = 0.0%) and methicillin-resistant Staphylococcus aureus (CONV = 1.3%; RWA = 0.7%) did not differ (P = 1.00). The blaCTX-M ARG was more abundant in CONV (2.4 vs. 2.1 log copies/gram, P = 0.01) but the tet(A) (2.4 vs. 2.5 log copies/gram, P = 0.02) and tet(M) (3.6 vs. 3.9 log copies/gram, P < 0.01) ARGs were more abundant in RWA. aadA1, blaCMY-2, mecA, erm(B), and tet(B) abundances did not differ significantly (Fig. 5) (P > 0.05). Abundances of aac (6’)-Ie-aph (2”)-Ia and blaKPC-2 were not analyzed since they were quantified in less than 5% of the samples.ConclusionU.S. retail CONV and RWA ground beef harbor generally similar levels of AMR since only 5 of 15 AMR measurements were statistically different between production systems. Three AMR measurements were higher in CONV, while 2 AMR measurements were higher in RWA. These results are in general agreement with a recently published study authored by our group that examined antimicrobial resistance in CONV and RWA ground beef obtained from U.S. foodservice suppliers (Vikram et al., J. Food Prot. 81:2007–2018. 2018.). Together these studies suggest that antimicrobial use during U.S. cattle production has minimal to no impact on human exposure to AMR via ground beef.Figure 5.

scholarly journals Transcriptomic Analysis of Shiga Toxin-Producing Escherichia coli during Initial Contact with Cattle Colonic Explants

2020 ◽  
Vol 8 (11) ◽  
pp. 1662
Author(s):  
Zachary R. Stromberg ◽  
Rick E. Masonbrink ◽  
Melha Mellata
Keyword(s):  
Escherichia Coli ◽  
Shiga Toxin ◽  
Bacterial Colonization ◽  
Coli Strain ◽  
Fold Change ◽  
Initial Contact ◽  
Lon Protease ◽  
E Coli ◽  
Log2 Fold Change ◽  
Colonization Factors

Foodborne pathogens are a public health threat globally. Shiga toxin-producing Escherichia coli (STEC), particularly O26, O111, and O157 STEC, are often associated with foodborne illness in humans. To create effective preharvest interventions, it is critical to understand which factors STEC strains use to colonize the gastrointestinal tract of cattle, which serves as the reservoir for these pathogens. Several colonization factors are known, but little is understood about initial STEC colonization factors. Our objective was to identify these factors via contrasting gene expression between nonpathogenic E. coli and STEC. Colonic explants were inoculated with nonpathogenic E. coli strain MG1655 or STEC strains (O26, O111, or O157), bacterial colonization levels were determined, and RNA was isolated and sequenced. STEC strains adhered to colonic explants at numerically but not significantly higher levels compared to MG1655. After incubation with colonic explants, flagellin (fliC) was upregulated (log2 fold-change = 4.0, p < 0.0001) in O157 STEC, and collectively, Lon protease (lon) was upregulated (log2 fold-change = 3.6, p = 0.0009) in STEC strains compared to MG1655. These results demonstrate that H7 flagellum and Lon protease may play roles in early colonization and could be potential targets to reduce colonization in cattle.

scholarly journals Prevalence and Antimicrobial Susceptibility of Indicator Organisms Escherichia coli and Enterococcus spp. Isolated from U.S. Animal Food, 2005–2011

2020 ◽  
Vol 8 (7) ◽  
pp. 1048 ◽  
Author(s):  
Beilei Ge ◽  
Kelly J. Domesle ◽  
Stuart A. Gaines ◽  
Claudia Lam ◽  
Sonya M. Bodeis Jones ◽  
...  
Keyword(s):  
Escherichia Coli ◽  
Antimicrobial Resistance ◽  
Animal Feed ◽  
The United States ◽  
Resistant Bacteria ◽  
Indicator Organisms ◽  
Pet Food ◽  
Animal Food ◽  
E Coli ◽  
Enterococcus Spp

The role animal food plays in the introduction of antimicrobial-resistant bacteria into the human food chain is not well understood. We conducted an analysis of 1025 samples (647 pet food and 378 animal feed) collected across the United States during 2005–2011 for two indicator organisms (Escherichia coli and Enterococcus spp.). The overall prevalence ranged from 12.5% for E. coli to 45.2% for Enterococcus spp., and 11.2% of samples harbored both organisms. Regardless of bacterial genus, animal feed had significantly higher prevalence than pet food (p < 0.001). A general downward trend in prevalence was observed from 2005 to 2009 followed by an upward trend thereafter. Among E. coli isolates (n = 241), resistance was highest to tetracycline (11.2%) and below 5% for fourteen other antimicrobials. Among Enterococcus spp. isolates (n = 1074), Enterococcus faecium (95.1%) was the predominant species. Resistance was most common to tetracycline (30.1%) and ciprofloxacin (10.7%), but below 10% for thirteen other antimicrobials. Multidrug-resistant organisms were observed among both E. coli and Enterococcus spp. isolates at 3.3%. Compared to National Antimicrobial Resistance Monitoring System (NARMS) 2011 retail meat and animal data, the overall resistance for both organisms was much lower in animal food. These findings help establish a historic baseline for the prevalence and antimicrobial resistance among U.S. animal food products and future efforts may be needed to monitor changes over time.

Influence of Housing Systems on Microbial Load and Antimicrobial Resistance Patterns of Escherichia coli Isolates from Eggs Produced for Human Consumption

2012 ◽  
Vol 75 (5) ◽  
pp. 847-853 ◽  
Author(s):  
ELENA ÁLVAREZ-FERNÁNDEZ ◽  
JESSICA DOMÍNGUEZ-RODRÍGUEZ ◽  
ROSA CAPITA ◽  
CARLOS ALONSO-CALLEJA
Keyword(s):  
Escherichia Coli ◽  
Antimicrobial Resistance ◽  
Housing System ◽  
Diffusion Method ◽  
Aerobic Bacteria ◽  
Human Consumption ◽  
E Coli ◽  
Free Range ◽  
Housing Systems ◽  
Enterococcus Spp

Microbial counts (aerobic bacteria, psychrotrophs, Enterobacteriaceae, coliforms, Pseudomonas spp., Enterococcus spp., Staphylococcus spp., and molds and yeasts) were obtained for the shells of 240 table eggs in northwestern Spain. Eggs from six sources (40 samples in each) were analyzed: chicken eggs from five different housing systems (conventional battery cages, barn, free range, organic, and domestic breeding) and quail eggs (cages). A total of 120 Escherichia coli strains (20 from each source) were tested by the disk diffusion method for resistance to 12 antimicrobial drugs of veterinary and human health significance. Aerobic plate counts ranged from 1.96 ± 1.0 (barn) to 3.69 ± 0.7 (domestic) log CFU/cm2. Counts for most microbial groups differed significantly between sources. Eggs from domestic production had the highest contamination loads (P &lt; 0.05) for aerobic bacteria, Enterococcus spp., and molds and yeasts and the highest prevalence of E. coli. Twenty-three E. coli isolates (19.17%) were susceptible to all antimicrobials tested, and 80.83% were resistant to one (22.50%) or more (58.33%) antimicrobials. The housing system had a significant influence (P &lt; 0.05) on the average resistance per strain, with the highest resistance in conventional cage (2.85) and barn (3.10) systems followed by free range (1.55) and quail (1.95). Eggs from organic (1.00) and domestic (0.75) production systems had the lowest resistance per strain. The highest prevalence of resistance was observed for the groups of antimicrobials more frequently used on poultry farms. Our results suggest that a relationship exists between the prevalence of antimicrobial resistance in E. coli strains and the more frequent use of antimicrobials in conventional (cage, barn, and free range) than in domestic and organic chicken housing systems. Education covering good sanitary practices for handling eggs to avoid cross-contamination or inadequate cooking is needed.

scholarly journals Effect of Antimicrobial Dosage Regimen on Salmonella and Escherichia coli Isolates from Feeder Swine

2008 ◽  
Vol 74 (6) ◽  
pp. 1731-1739 ◽  
Author(s):  
Bruce A. Wagner ◽  
Barbara E. Straw ◽  
Paula J. Fedorka-Cray ◽  
David A. Dargatz
Keyword(s):  
Escherichia Coli ◽  
Antimicrobial Resistance ◽  
Commensal Bacteria ◽  
Antimicrobial Use ◽  
Control Analysis ◽  
Fecal Samples ◽  
E Coli ◽  
The Impact ◽  
Susceptibility And Resistance ◽  
Continuous Pulse

ABSTRACT A body of evidence exists that suggests that antimicrobial use in food animals leads to resistance in both pathogenic and commensal bacteria. This study focused on the impact of three different antimicrobial regimes (low-level continuous, pulse, and no antimicrobial) for two antimicrobials (chlortetracycline and tylosin) on the presence of Salmonella spp. and on the prevalence of antimicrobial resistance of both Salmonella spp. and nonspecific Escherichia coli in fecal samples from feeder swine. The prevalence of fecal samples positive for Salmonella spp. significantly decreased between the samples taken at feeder placement compared to samples taken when the animals were close to market weight. Differences in resistance of Salmonella spp. did not appear to be influenced by dosing treatment including the control. Analysis of antimicrobial resistance examining both susceptibility and resistance, as well as MIC outcomes, demonstrated that only resistance to cephalothin increased in E. coli under the pulse chlortetracycline treatment. These results suggest that the dosing regimes examined in this study did not lead to an increase in either the prevalence of Salmonella spp. or the prevalence of antimicrobial resistance in isolates of Salmonella spp. or E. coli.

scholarly journals Antimicrobial Resistance in Enterococcus Spp. Isolated from a Beef Processing Plant and Retail Ground Beef

2021 ◽  
Author(s):  
Devin B. Holman ◽  
Cassidy L. Klima ◽  
Katherine E. Gzyl ◽  
Rahat Zaheer ◽  
Cara Service ◽  
...  
Keyword(s):  
Antimicrobial Resistance ◽  
Ground Beef ◽  
Fabrication Process ◽  
Resistant Bacteria ◽  
Processing Plant ◽  
Agricultural Industry ◽  
Beef Processing ◽  
Enterococcus Spp

Antimicrobial resistance (AMR) is a serious challenge facing the agricultural industry. Understanding the flow of antimicrobial-resistant bacteria through the beef fabrication process and into ground beef is an important step in identifying intervention points for reducing AMR.

Antimicrobial Resistance and Genetic Profiling of Escherichia coli from a Commercial Beef Packing Plant†

2006 ◽  
Vol 69 (7) ◽  
pp. 1508-1513 ◽  
Author(s):  
MUEEN ASLAM ◽  
CARA SERVICE
Keyword(s):  
Escherichia Coli ◽  
Antimicrobial Resistance ◽  
Membrane Filtration ◽  
Antimicrobial Agents ◽  
Random Amplified Polymorphic Dna ◽  
Ground Beef ◽  
Resistant Bacteria ◽  
Filtration Method ◽  
E Coli ◽  
Beef Processing

The objective of this study was to investigate the extent of antimicrobial resistance and to genetically characterize resistant Escherichia coli recovered from a commercial beef packing plant. E. coli isolates were recovered by a hydrophobic grid membrane filtration method by direct plating on SD-39 medium. A total of 284 isolates comprising 71, 36, 55, 52, and 70 isolates from animal hides, washed carcasses, conveyers, beef trimmings, and ground beef, respectively, were analyzed. The susceptibility of E. coli isolates to 15 antimicrobial agents was evaluated with an automated broth microdilution system, and the genetic characterization of these isolates was performed by the random amplified polymorphic DNA (RAPD) method. Of the 284 E. coli isolates, 56% were sensitive to all 15 antimicrobial agents. Resistance to tetracycline, ampicillin, and streptomycin was observed in 38, 9, and 6% of the isolates, respectively. Resistance to one or more antimicrobial agents was observed in 51% of the E. coli isolates recovered from the hides but in only 25% of the E. coli from the washed carcasses. Resistance to one or more antimicrobial agents was observed in 49, 50, and 37% of the isolates recovered from conveyers, beef trimmings, and ground beef, respectively. The RAPD pattern data showed that the majority of resistant E. coli isolates were genetically diverse. Only a few RAPD types of resistant strains were shared among various sample sources. The results of this study suggest that antimicrobial-resistant E. coli isolates were prevalent during all stages of commercial beef processing and that considerably higher numbers of resistant E. coli were present on conveyers, beef trimmings, and ground beef than on dressed carcasses. This stresses the need for improving hygienic conditions during all stages of commercial beef processing and meatpacking to avoid the risks of transfer of antimicrobial-resistant bacteria to humans.

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