Prevalence of antimicrobial resistant and extended-spectrum beta-lactamase-producing Escherichia coli in dairy cattle farms in east Tennessee

Authors: GELALCHA, BENTI - University Of Tennessee; ENSERMU, D - University Of Tennessee; Agga, Getahun; VANCUREN, M - University Of Tennessee; GILLESPIE, B - University Of Tennessee; D'SOUZA, D - University Of Tennessee; OKAFOR, C - University Of Tennessee; DEGO, O - University Of Tennessee

Submitted to: Foodborne Pathogens and Disease
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 3/15/2022
Publication Date: 4/22/2022
Citation: Gelalcha, B.D., Ensermu, D.B., Agga, G.E., Vancuren, M., Gillespie, B.E., D'Souza, D.H., Okafor, C., Dego, O.K. 2022. Prevalence of antimicrobial resistant and extended-spectrum beta-lactamase-producing Escherichia coli in dairy cattle farms in east Tennessee. Foodborne Pathogens and Disease. 19(6). https://doi.org/10.1089/fpd.2021.0101.
DOI: https://doi.org/10.1089/fpd.2021.0101

Interpretive Summary: Dairy cattle production is highly dependent on the use of large amounts of antibiotics for the purposes of treatment or prevention of various bacterial infections. Largescale use of antibiotics undoubtedly increases the occurrence of antibiotic resistant bacteria which may spread to the natural environments through dairy manure or infect humans through the food chain. We investigated Escherichia coli resistant to innocuous antibiotic tetracycline on one hand, and to the critically important antibiotics, third generation cephalosporins and nalidixic acid, for human use on the other. Enteric bacteria such as E. coli that produce a group of enzymes called extended spectrum beta-lactamases (ESBLs) can make most antibiotics such as penicillin ineffective are particularly worrisome. They became widespread through genes that can easily disseminate to bacterial populations. As a result, CDC considers infections caused by ESBLs producing enteric bacteria as serious threats. Our results show that up to three in four tetracycline resistant E. coli, one in five third generation cephalosporin resistant E. coli, and one in 12 nalidixic acid resistant E. coli isolates could be found in dairy farms. Almost all third-generation cephalosporin resistant E. coli isolates carried ESBLs gene that can make them resistant to so many drugs related to penicillin. Furthermore, these strains are multidrug resistant suggesting that not only beta-lactam classes of antibiotics, but also other unrelated drugs are ineffective for the treatment of serious infections caused by these bacteria. There was a significant variation between the farms with respect to the level of antibiotic resistance suggesting the presence of farm specific factors that could be targeted to mitigate antimicrobial resistance. The presence of ESBLs producing E. coli in the raw milk emphasizes the importance of milk pasteurization before it is consumed or used for the production of milk products.

Technical Abstract: Antimicrobials are widely used in dairy farms for the prevention and control of diseases of dairy cattle since the 1960s. This led to widespread occurrence of antimicrobial resistant bacteria (ARB) and antimicrobial resistance genes (ARGs) that can spread from dairy farms to humans. Therefore, regular antimicrobial resistance (AMR) monitoring is important to implement proper mitigation measures. The objective of this study was to determine the prevalence of AMR- and extended-spectrum beta-lactamase (ESBLs)-producing- E. coli in dairy cattle. A cross-sectional study was conducted in four dairy cattle farms (A - D) in East Tennessee. Eighty samples consisting of twenty samples each of bulk tank milk, feces, dairy cattle manure amended soil (Agsoil), and prairie soil adjacent to the farms were collected and cultured for the isolation of E. coli. Tetracycline (TETr)-, third-generation cephalosporin (TGCr)- and nalidixic acid (NALr)-resistant E. coli (n=88) were isolated and identified on agar media supplemented with tetracycline, cefotaxime, and nalidixic acid, respectively. TGCr E. coli were tested for ESBLs and other co-selected ARGs. TETr (74%, n=88) was the most common, followed by TGCr (20%) and NALr (8%). Farm had a significant (P<0.001) effect: the highest prevalence of TGCr (55%) and TETr (100%) were observed in farm D, while all NALr isolates were from farm C. Over 83% of TGCr isolates (n=18) harbored ESBLs gene blaCTX-M. Majority (78%) of them were multidrug-resistant (MDR) being positive for beta-lactams (blaCTX-M), tetracyclines (tet(A), tet(B), tet(M)), sulphonamides (sul2), aminoglycosides (strA), and phenicols (floR). This study indicates the widespread occurrence of MDR ESBLs-E. coli in dairy cattle farms. AMR surveillance of more dairy farms and identification of farm-level risk factors are important to mitigate the occurrence and spread of ARB of significant public health importance, such as ESBLs E. coli.