Similar levels of antimicrobial resistance in U.S. food service ground beef products with and without a "Raised Without Antibiotics" claim

Authors: Vikram, Amit; Miller, Eric; Arthur, Terrance; Bosilevac, Joseph - Mick; Wheeler, Tommy; Schmidt, John

Submitted to: Journal of Food Protection
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 8/22/2018
Publication Date: 11/26/2018
Citation: Vikram, A., Miller, E., Arthur, T.M., Bosilevac, J.M., Wheeler, T.L., Schmidt, J.W. 2018. Similar levels of antimicrobial resistance in U.S. food service ground beef products with and without a "Raised Without Antibiotics" claim. Journal of Food Protection. 81(12):2007-2018. https://doi.org/10.4315/0362-028X.JFP-18-299.
DOI: https://doi.org/10.4315/0362-028X.JFP-18-299

Interpretive Summary: Meat products, including ground beef, are thought to be routes of transmission for antibiotic resistance from animals to humans. Ground beef products produced from cattle "raised without antibiotics" (RWA) are perceived as harboring lower levels of antibiotic resistance than "conventional" (CONV) products which may contain meat from animals that received antibiotics. However, no study has examined antibiotic resistance levels in United States (U.S.) ground beef since a small study published in 2004. This study found that the microbial flora and antibiotic resistance levels of CONV and RWA ground beef were similar. These results demonstrate that RWA ground beef does not deliver its major perceived benefit, lower levels of antibiotic resistance than CONV ground beef. These results were consistent with prior research demonstrating that the long-term antibiotic resistance impacts of antibiotic uses during U.S. beef cattle production are minimal and indicate a need for reevaluation of the claims of the detrimental impact of antibiotic uses during U.S. beef cattle production on human health via ground beef.

Technical Abstract: U.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, thirdgeneration 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 x 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.