Prevalence, serotypes, and antimicrobial resistance of Salmonella from mink feces and feed in the United States

Authors: Agga, Getahun; Silva, Philip - Phil; MARTIN, RANDAL - Utah State University

Submitted to: Foodborne Pathogens and Disease
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 7/28/2021
Publication Date: 9/14/2021
Citation: Agga, G.E., Silva, P.J., Martin, R.S. 2021. Prevalence, serotypes, and antimicrobial resistance of Salmonella from mink feces and feed in the United States. Foodborne Pathogens and Disease. 19(1):45-55. https://doi.org/10.1089/fpd.2021.0037.
DOI: https://doi.org/10.1089/fpd.2021.0037

Interpretive Summary: Non-typhoidal Salmonella is a second leading cause of foodborne infections. Although it results in mild intestinal problems, it can lead to severe infections requiring hospitalizations and antibiotic treatments. The U.S. Centers for Disease Control (CDC) considers drug resistant non-typhoidal Salmonella as serious public health threats. The United States monitors antimicrobial resistant bacteria in humans, food animals and retail meat. The U.S. is one of the leading mink producers in the world. Concentrated mink production can be a reservoir for pathogenic bacteria that can escape the production farms and spread to the environment which may eventually reach people through contaminated water and vegetables when mink manure is land applied. We investigated the level of Salmonella in the fecal and feed samples obtained from a mink farm. Non-typhoidal Salmonella was detected from 26% of fecal and one feed samples. Four serotypes including Salmonella Heidelberg, a common serotype associated with contaminated poultry, and Salmonella Reading, a multi-drug resistant serotype associated with turkey consumption, were identified. These two Salmonella serotypes are among the CDC’s top 30 serotypes reported from human infections. Salmonella Reading caused a large-scale multistate turkey associated outbreaks between 2017-2019 in the US. The Salmonella Reading isolates identified from mink feces belonged to the same sequence type with similar antibiotic resistance profiles as the US outbreak strains. This study indicates that foodborne pathogens such as Salmonella including multidrug resistant and outbreak strains can be maintained in commercial mink production system. Antimicrobial resistance monitoring programs need to incorporate mink farming in to a one health approach for combating antimicrobial resistant pathogens. Since mink are carnivores and that their feed is derived from food animals, ensuring the safety of mink feed is also essential to prevent the entry of pathogenic bacteria into the mink farms.

Technical Abstract: Nontyphoidal Salmonella is a leading cause of foodborne illnesses, and concentrated animal production such as commercial mink farming can be a reservoir. The objective of this study was to determine the prevalence, serotypes, antimicrobial resistance, virulence genes and mobile genetic elements, and phylogenetic characterization of Salmonella from mink fecal (n = 42) and feed (n = 8) samples at a commercial mink farm in the United States. Salmonella was detected from 11 (26.2%) fecal and 1 (12.5%) feed samples. Twelve fecal isolates obtained from the positive samples were identified into four serotypes: Salmonella Uganda (eight isolates; two isolates were obtained from one sample), Salmonella Reading (two isolates), Salmonella Heidelberg (one isolate), and Salmonella Orion (one isolate). Two isolates from the positive feed sample were identified as Salmonella Cerro. Twelve isolates, one isolate per positive sample, were whole genome sequenced for further characterization. The two Salmonella Reading isolates were multidrug resistant (MDR) with the classical ASSuT (ampicillin, streptomycin, sulfisoxazole, and tetracycline) phenotype. Genotypically, the isolates were correspondingly positive, both by polymerase chain reaction and by whole-genome sequencing (WGS), for blaTEM-1, aph(3†)-Ib and aph(6)-Id, sul2, and tet(A). WGS additionally identified trimethoprim resistance gene dfrA8 in Salmonella Reading, and fosfomycin resistance gene fosA7 in Salmonella Heidelberg. All isolates carried Salmonella-specific multidrug resistance (mdsA/B), gold resistance, and intimin-like virulence genes. In addition, Salmonella Orion carried copper and silver resistance gene clusters. The two Salmonella Reading isolates also carried a cytolethal distension toxin (cdtB) gene. Salmonella Reading isolates belonged to ST412, a predominant sequence type among turkey and human isolates obtained in relation to recent salmonellosis outbreaks in North America. Phylogenetically, Salmonella Uganda, Salmonella Heidelberg, and Salmonella Reading were mostly associated with historic human/clinical, and poultry and swine source isolates. This study indicates that mink production can be a reservoir for foodborne pathogens such as Salmonella with MDR serovars commonly associated with human illnesses.