Age-associated distribution of antimicrobial-resistant Salmonella enterica and Escherichia coli isolated from dairy herds in Pennsylvania, 2013-2015

Authors: CAO, HUILIN - University Of Maryland; PRADHAN, ABANI - University Of Maryland; Karns, Jeffrey; WOLFGANG, DAVE - Pennsylvania State University; HOVINGH, ERNEST - Pennsylvania State University; Van Kessel, Jo Ann; Vinyard, Bryan; KIM, SEON-WOO - US Department Of Agriculture (USDA)

Submitted to: Foodborne Pathogens and Disease
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 3/26/2016
Publication Date: 1/23/2019
Citation: Cao, H., Pradhan, A.K., Karns, J.S., Wolfgang, D.R., Hovingh, E., Van Kessel, J.S., Vinyard, B.T., Kim, S. 2019. Age-associated distribution of antimicrobial-resistant Salmonella enterica and Escherichia coli isolated from dairy herds in Pennsylvania, 2013-2015. Foodborne Pathogens and Disease. 16:60-67. https://doi.org/10.1089/fpd.2018.2519.
DOI: https://doi.org/10.1089/fpd.2018.2519

Interpretive Summary: Antimicrobial resistance has become a major public health concern; resistant bacterial pathogens limit treatment options and can lead to failure of treatment, prolonged hospital stays, higher health care expenditures, and increased morbidity and mortality. While development of antibiotic resistance has been attributed to use and misuse of antibiotics in clinical settings, antimicrobial use in the production of food producing animals has also been implicated as a source of antimicrobial resistance. Antibiotic use in dairy animals is regulated in the US and antibiotics are commonly used to prevent and to treat diseases in calves and cows. The prevalence of resistant bacteria on dairy farms has not been well described. The objective of this study was to examine antimicrobial resistance in Salmonella and E. coli from different animal age groups on Pennsylvania dairy herds. Manure composite samples were collected from pre-weaned calves, post-weaned calves, dry cows, and lactating cows on 80 dairy farms. E. coli and Salmonella, when present, were pre-screened for resistance to a panel of 8 antimicrobials and isolates with unique resistance profiles in the pre-screening were further tested against a panel of 14 antibiotics. Salmonella, a pathogen that is often detected in dairy animals, was isolated from at least one composite sample from 51 farms (67%) and was associated mostly with older animals. The predominant Salmonella serotypes were Montevideo, Cerro, and Kentucky. Most Salmonella isolates (n=1095) were pan-susceptible and grew in the presence of all 14 antibiotics on the panel. Among E. coli isolates (n=2370) the most common resistance detected in pre-screening was to tetracycline, streptomycin, ampicillin, and/or kanamycin. Resistant isolates were more common in calves than in adult cows. Multi-drug resistant (MDR) (resistant to =3 antimicrobial classes) E. coli isolates were observed in 66 (83%) farms, primarily among young animal groups. Resistance was observed to as many as 8 classes of antibiotics, including resistance attributable to extended spectrum ß-lactamase (ESBL), enzymes that affect cephalosporin antibiotics important in treating infections in humans. Ciprofloxacin is an important antibiotic for human medicine and resistance was observed in only 1% of E. coli isolates from young animal samples and was not found in adult animal samples. ESBL blaCTX-M genes were detected in isolates from 4 (5%) farms. The blaCMY gene was detected in isolates from 35% of the farms and 8.4% of all the samples, with the majority being pre-weaned calf samples. This study indicates that antimicrobial resistance is low in common dairy-associated Salmonella enterica but that resistant E. coli are prevalent on Pennsylvania dairy farms, primarily in calf samples. Resistance to 3rd generation cephalosporins was appreciable in E. coli, but the prevalence of blaCTX-M, conferring resistance to ceftriaxone, an increasing concern in human medicine, was very low. Dairy animals do harbor MDR E. coli and have the potential to pose risks to human health. This information will be of interest to other scientists, the dairy industry and regulatory agencies.

Technical Abstract: Antimicrobial resistance has become a major public health concern and animal agriculture is often implicated as a source of bacteria that are resistant to antibiotics. The objective of this study was to examine antimicrobial resistance in Salmonella and E. coli from different animal age groups on Pennsylvania dairy herds. Manure composite samples were collected from pre-weaned calves, post-weaned calves, dry cows, and lactating cows. E. coli and Salmonella, when present, were screened for resistance using Mueller Hinton agar supplemented with 8 antimicrobials. Isolates with unique resistance profiles in the pre-screening were tested via an automated broth micro-dilution susceptibility assay against 14 antimicrobials on a NARMS Gram-negative Panel. A total of 444 composite manure samples were collected from 80 herds in Pennsylvania. Salmonella was isolated from at least one composite sample from 51 farms (67%), and was associated mostly with older animals. The predominant Salmonella serotypes were Montevideo, Cerro, and Kentucky. Most Salmonella isolates (n=1095) were pan-susceptible. Among E. coli isolates (n=2370) the most common resistance detected in pre-screening was to tetracycline, streptomycin, ampicillin, and/or kanamycin. Resistant strains were more common in calves than in adult cows. Multi-drug resistant (MDR) (resistant to =3 antimicrobial classes) E. coli isolates were observed in 66 (83%) farms, primarily among young animal groups. Resistance to up to 8 classes of antibiotics, including the types associated with extended spectrum ß-lactamases (ESBL), was observed. Fluoroquinolone resistance was observed in 1% of E. coli isolates from young animal samples and was not found in adult animal samples. Among E. coli isolates displaying (ESBL) phenotypes, blaCTX-M genes were detected in isolates from 4 (5%) farms. The blaCMY gene was detected in isolates from 35% of the farms with the majority being from pre-weaned calf samples. This study indicates that antimicrobial resistance is low in common dairy-associated Salmonella enterica but that resistant E. coli are prevalent on Pennsylvania dairy farms, primarily in calf samples. Resistance to 3rd generation cephalosporins was appreciable in E. coli, but the prevalence of blaCTX-M, an increasing concern in human medicine, was very low. Dairy animals do harbor MDR E. coli and have the potential to pose risks to human health.