Impact of "raised without antibiotics" beef cattle production practices on occurrences of antimicrobial resistance

Authors: Vikram, Amit; ROVIRA, PABLO - Colorado State University; Agga, Getahun; Arthur, Terrance; Bosilevac, Joseph - Mick; Wheeler, Tommy; MORLEY, PAUL - Colorad0 State University; BELK, KEITH - Colorado State University; Schmidt, John

Submitted to: Applied and Environmental Microbiology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 9/5/2017
Publication Date: 11/1/2017
Citation: Vikram, A., Rovira, P., Agga, G.E., Arthur, T.M., Bosilevac, J.M., Wheeler, T.L., Morley, P., Belk, K., Schmidt, J.W. 2017. Impact of "raised without antibiotics" beef cattle production practices on occurrences of antimicrobial resistance. Applied and Environmental Microbiology. 83:e01682-17. https://doi.org/10.1128/AEM.01682-17.

Interpretive Summary: Although the recently implemented (January 2017) regulations are expected to reduce their use, the majority of antimicrobials used in the United States (U.S.) are for food-animal production. Thus, there remains a concern that typical antimicrobial use patterns for food-animal production contribute greatly to the occurrence of antimicrobial resistance (AMR). Fecal AMR levels for U.S. beef cattle produced "conventionally" (no restrictions on antibiotic use other than regulatory compliance) and "raised without antibiotics" (no antimicrobial use including ionophores) were assessed over a 12-month period using cultural and genetic methods. Individual AMR levels were either similar between production systems or slightly elevated in conventional animals. Since the scale of AMR reductions in feces from raised without antibiotics cattle were small or nonexistent, further restrictions on antimicrobial use in U.S. beef production are unlikely to reduce the occurrence of antimicrobial-resistant human infections. However, to ensure judicious antimicrobial use, the animal health, economic, and AMR impacts of shorter duration in-feed antimicrobial administration should be examined.

Technical Abstract: The specific antimicrobial resistance (AMR) decreases that can be expected from reducing antimicrobial (AM) use in U.S. beef production have not been defined. To address this data gap, feces were recovered from 36 lots of “raised without antibiotics” (RWA) and 36 lots of “conventional” (CONV) beef cattle. Samples (n = 719) were collected during harvest and distributed over a year. AMR was assessed by (i) the culture of six AM-resistant bacteria (ARB), (ii) quantitative PCR (qPCR) for 10 AMR genes (ARGs), (iii) a qPCR array of 84 ARGs, and (iv) metagenomic sequencing. Generally, AMR levels were similar, but some were higher in CONV beef cattle. The prevalence of third-generation cephalosporin-resistant (3GCr) Escherichia coli was marginally different between production systems (CONV, 47.5%; RWA, 34.8%; P = 0.04), but the seasonal effect (summer, 92.8%; winter, 48.3%; P < 0.01) was greater. Erythromycin-resistant (ERYr) Enterococcus sp. concentrations significantly differed between production systems (CONV, 1.91 log10 CFU/g; RWA, 0.73 log10 CFU/g; P < 0.01). Levels of aadA1, ant(6)-I, blaACI, erm(A), erm(B), erm(C), erm(F), erm(Q), tet(A), tet(B), tet(M), and tet(X) ARGs were higher (P < 0.05) in the CONV system. Aggregate abundances of all 43 ARGs detected by metagenomic sequencing and the aggregate abundances of ARGs in the aminoglycoside, ß-lactam, macrolide-lincosamidestreptogramin B (MLS), and tetracycline AM classes did not differ (log2 fold change < 1.0) between CONV and RWA systems. These results suggest that further reductions of AM use in U.S. beef cattle production may not yield significant AMR reductions beyond MLS and tetracycline resistance.