Dataset Information

Horizontal Dissemination of Antimicrobial Resistance Determinants in Multiple Salmonella Serotypes following Isolation from the Commercial Swine Operation Environment after Manure Application.

ABSTRACT: The aim of this study was to characterize the plasmids carrying antimicrobial resistance (AMR) determinants in multiple Salmonella serotypes recovered from the commercial swine farm environment after manure application on land. Manure and soil samples were collected on day 0 before and after manure application on six farms in North Carolina, and sequential soil samples were recollected on days 7, 14, and 21 from the same plots. All environmental samples were processed for Salmonella, and their plasmid contents were further characterized. A total of 14 isolates including Salmonella enterica serotypes Johannesburg (n = 2), Ohio (n = 2), Rissen (n = 1), Typhimurium var5- (n = 5), Worthington (n = 3), and 4,12:i:- (n = 1), representing different farms, were selected for plasmid analysis. Antimicrobial susceptibility testing was done by broth microdilution against a panel of 14 antimicrobials on the 14 confirmed transconjugants after conjugation assays. The plasmids were isolated by modified alkaline lysis, and PCRs were performed on purified plasmid DNA to identify the AMR determinants and the plasmid replicon types. The plasmids were sequenced for further analysis and to compare profiles and create phylogenetic trees. A class 1 integron with an ANT(2?)-Ia-aadA2 cassette was detected in the 50-kb IncN plasmids identified in S Worthington isolates. We identified 100-kb and 90-kb IncI1 plasmids in S Johannesburg and S Rissen isolates carrying the blaCMY-2 and tet(A) genes, respectively. An identical 95-kb IncF plasmid was widely disseminated among the different serotypes and across different farms. Our study provides evidence on the importance of horizontal dissemination of resistance determinants through plasmids of multiple Salmonella serotypes distributed across commercial swine farms after manure application.IMPORTANCE The horizontal gene transfer of antimicrobial resistance (AMR) determinants located on plasmids is considered to be the main reason for the rapid proliferation and spread of drug resistance. The deposition of manure generated in swine production systems into the environment is identified as a potential source of AMR dissemination. In this study, AMR gene-carrying plasmids were detected in multiple Salmonella serotypes across different commercial swine farms in North Carolina. The plasmid profiles were characterized based on Salmonella serotype donors and incompatibility (Inc) groups. We found that different Inc plasmids showed evidence of AMR gene transfer in multiple Salmonella serotypes. We detected an identical 95-kb plasmid that was widely distributed across swine farms in North Carolina. These conjugable resistance plasmids were able to persist on land after swine manure application. Our study provides strong evidence of AMR determinant dissemination present in plasmids of multiple Salmonella serotypes in the environment after manure application.

SUBMITTER: Pornsukarom S

PROVIDER: S-EPMC5626988 | biostudies-literature | 2017 Oct

REPOSITORIES: biostudies-literature

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Horizontal Dissemination of Antimicrobial Resistance Determinants in Multiple Salmonella Serotypes following Isolation from the Commercial Swine Operation Environment after Manure Application.

Pornsukarom Suchawan S Thakur Siddhartha S

Applied and environmental microbiology 20170929 20

The aim of this study was to characterize the plasmids carrying antimicrobial resistance (AMR) determinants in multiple <i>Salmonella</i> serotypes recovered from the commercial swine farm environment after manure application on land. Manure and soil samples were collected on day 0 before and after manure application on six farms in North Carolina, and sequential soil samples were recollected on days 7, 14, and 21 from the same plots. All environmental samples were processed for <i>Salmonella</i ...[more]

PMID: 28802274

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Project description:Land application of swine manure in commercial hog farms is an integral part of their waste management system which recycles the nutrients back to the soil. However, manure application can lead to the dissemination of bacterial pathogens in the environment and pose a serious public health threat. The aim of this study was to determine the dissemination of antimicrobial resistant Salmonella in the environment due to manure application in commercial swine farms in North Carolina (n = 6) and Iowa (n = 7), two leading pork producing states in the US. We collected manure and soil samples twice on day 0 (before and after manure application) from four distinct plots of lands (5 soil samples/plot) located at 20 feet away from each other in the field. Subsequent soil samples were collected again on days 7, 14, 21 from the same plots. A total of 1,300 soil samples (NC = 600; IA = 700) and 130 manure samples (NC = 60; IA = 70) were collected and analyzed in this study. The overall Salmonella prevalence was 13.22% (189/1,430), represented by 10.69% and 38.46% prevalence in soil and manure, respectively. The prevalence in NC (25.45%) was significantly higher than in IA (2.73%) (P<0.001) and a consistent decrease in Salmonella prevalence was detected from Day 0-Day 21 in all the farms that tested positive. Salmonella serotypes detected in NC were not detected in IA, thereby highlighting serotype association based on manure storage and soil application method used in the two regions. Antimicrobial susceptibility testing was done by the broth microdilution method to a panel of 15 antimicrobial drugs. A high frequency of isolates (58.73%) were multidrug resistant (resistance to three or more class of antimicrobials) and the most frequent resistance was detected against streptomycin (88.36%), sulfisoxazole (67.2%), and tetracycline (57.67%). Genotypic characterization by pulse field gel electrophoresis revealed clonally related Salmonella in both manure and soil at multiple time points in the positive farms. Our study highlights the potential role of swine manure application in the dissemination and persistence of antimicrobial resistant Salmonella in the environment.

Project description:Antimicrobial resistance is an increasing problem worldwide, and Salmonella spp. resistance to quinolone was classified by WHO in the high priority list. Recent studies in Europe and in the US reported the presence of small plasmids carrying quinolone resistance in Enterobacteriaceae isolated from poultry and poultry products. The aims of this study were to identify and characterize plasmid-mediated quinolone resistance in Salmonella spp. and to investigate transduction as a possible mechanism associated to its dissemination. First, we assessed resistance to nalidixic acid and/or ciprofloxacin in 64 Salmonella spp. and detected resistance in eight of them. Genomic analyses determined that six isolates of different serotypes and sources carried an identical 2.7-kb plasmid containing the gene qnrB19 which confers quinolone resistance. The plasmid detected also has high identity with plasmids reported in the US, Europe, and South America. The presence of similar plasmids was later surveyed by PCR in a local Salmonella collection (n = 113) obtained from diverse sources: food (eggs), wild and domestic animals (pigs, horse, chicken), and human clinical cases. qnrB19-carrying plasmids were found in 8/113 Salmonella tested strains. A bioinformatics analysis including Chilean and previously described plasmids revealed over 95.0% of nucleotide identity among all the sequences obtained in this study. Furthermore, we found that a qnrB19-carrying plasmid can be transferred between Salmonella of different serotypes through a P22-mediated transduction. Altogether our results demonstrate that plasmid-mediated quinolone resistance (PMQR) is widespread in Salmonella enterica of different serotypes isolated from human clinical samples, wild and domestic animals, and food in Chile and suggest that transduction could be a plausible mechanism for its dissemination. The occurrence of these antimicrobial resistance elements in Salmonella in a widespread area is of public health and food safety concern, and it indicates the need for increased surveillance for the presence of these plasmids in Salmonella strains and to assess their actual impact in the rise and spread of quinolone resistance.

Dataset Information

Horizontal Dissemination of Antimicrobial Resistance Determinants in Multiple Salmonella Serotypes following Isolation from the Commercial Swine Operation Environment after Manure Application.

Publications

Horizontal Dissemination of Antimicrobial Resistance Determinants in Multiple Salmonella Serotypes following Isolation from the Commercial Swine Operation Environment after Manure Application.

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