Population dynamics of enteric Salmonella in response to antimicrobial use in beef feedlot cattle

Ohta, Naomi; Norman, Keri N.; Norby, Bo; Lawhon, Sara D.; Vinasco, Javier; Bakker, Henk D.; Loneragan, Guy H.; Scott, H. M.

doi:10.1038/s41598-017-14751-9

Cited by 20 publications

(30 citation statements)

References 61 publications

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“…These findings are consistent with previous reports describing development of multi-drug resistance developing in livestock treated with antimicrobials 10,12,14 . A number of mechanistic explanations exist for acquisition of multi-drug resistance, including conjugal transfer of multiple genes encoding resistance to different antimicrobials and multidrug efflux pumps 63 .…”

Section: Discussionsupporting

confidence: 93%

A Common Practice of Widespread Antimicrobial Use in Horse Production Promotes Multi-Drug Resistance

Álvarez‐Narváez

Berghaus

Morris

et al. 2020

Sci Rep

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the practice of prophylactic administration of a macrolide antimicrobial with rifampin (MaR) to apparently healthy foals with pulmonary lesions identified by thoracic ultrasonography (i.e., subclinically pneumonic foals) is common in the United States. the practice has been associated epidemiologically with emergence of R. equi resistant to MaR. Here, we report direct evidence of multidrug resistance among foals treated with MaR. In silico and in vitro analysis of the fecal microbiome and resistome of 38 subclinically pneumonic foals treated with either MaR (n = 19) or gallium maltolate (GaM; n = 19) and 19 untreated controls was performed. Treatment with MaR, but not GaM, significantly decreased fecal microbiota abundance and diversity, and expanded the abundance and diversity of antimicrobial resistance genes in feces. Soil plots experimentally infected with Rhodococcus equi (R. equi) and treated with MaR selected for MaR-resistant R. equi, whereas MaR-susceptible R. equi out-competed resistant isolates in GaM-treated or untreated plots. our results indicate that MaR use promotes multi-drug resistance in R. equi and commensals that are shed into their environment where they can persist and potentially infect or colonize horses and other animals. Despite their beneficial properties for treating infections, injudicious antimicrobial use can promote resistance in bacteria in both human and animal populations 1,2. The United States leads the list of high-income countries for antibiotic consumption, with ~80% of its annual antimicrobial consumption used for treating disease or promoting growth in animals 3,4. Furthermore, several studies suggest that the use of antibiotics in animals contributes to the crisis of antibiotic-resistant infections in humans 5-7. Although antimicrobial use in food animal production has received considerable attention 8-14 , antimicrobial resistance in equine medicine has received relatively limited attention. Pneumonia caused by Rhodococcus equi (R. equi) in foals is an important problem for the equine breeding industry worldwide 15-17. Foals are exposed to R. equi from birth 18,19 , and the disease generally progresses insidiously with onset of signs typically between ages 1 and 5 months 19,20. The combination of a macrolide with rifampin has been the standard of care for foals infected with R. equi in North America for over 30 years 21. Because of its insidious onset, many farms in North America have implemented serial thoracic ultrasonographic screening of foals to identify foals with pneumonia prior to the onset of clinical signs (i.e., subclinical pneumonia) and treatment of subclinical pneumonia 21-23. Evidence exists that most foals with subclinical pneumonia attributed to R. equi will not develop clinical signs of pneumonia 21,24,25. Consequently, thoracic ultrasonographic screening combined with antimicrobial treatment of foals with subclinical pneumonia results in overuse of antimicrobials. Resistance to MaR in R. equi has been increasing in prevalence over recent years in cent...

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Section: Discussionsupporting

confidence: 93%

A Common Practice of Widespread Antimicrobial Use in Horse Production Promotes Multi-Drug Resistance

Álvarez‐Narváez

Berghaus

Morris

et al. 2020

Sci Rep

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“…Commensal bacteria external to the animal and that are susceptible to AMD may outcompete within-host resistant bacteria after AMD treatment ends or mitigate an expansion of ex vivo resistant bacterial populations immediately posttreatment. While this was not observed in previously described culture studies ( 7 – 9 ), this repopulation is likely dependent on the availability of bacteria from the pen environment. In this study, higher group-level exposures to CCFA (an extended-duration formulation of ceftiofur) may have had a greater long-term suppressive effect on enteric bacteria and, thus, a lower measure of population diversity.…”

Section: Resultsmentioning

confidence: 47%

“…Research conducted using clinical trials to evaluate the impacts of AMD administration provides better opportunities to avoid bias, and these studies conducted by Kanwar et al ( 7 , 8 ) and Ohta et al ( 9 ) provide important information that is relevant to beef production and public health. However, they provide limited information about the entire microbiome and resistome, given their focus on either specific bacterial species (e.g., E. coli and Salmonella ) or a few AMR genes [e.g., tet (A), tet (B), bla CMY-2 , and bla CTX-M-32 ] using qPCR.…”

Section: Introductionmentioning

confidence: 99%

Effects of Ceftiofur and Chlortetracycline on the Resistomes of Feedlot Cattle

Weinroth

Scott

Norby

et al. 2018

Appl Environ Microbiol

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Treatment of food-producing animals with antimicrobial drugs (AMD) is controversial because of concerns regarding promotion of antimicrobial resistance (AMR). To investigate this concern, resistance genes in metagenomic bovine fecal samples during a clinical trial were analyzed to assess the impacts of treatment on beef feedlot cattle resistomes. Four groups of cattle were exposed, using a 2-by-2 factorial design, to different regimens of antimicrobial treatment. Injections of ceftiofur crystalline-free acid (a third-generation cephalosporin) were used to treat all cattle in treatment pens or only a single animal, and either chlortetracycline was included in the feed of all cattle in a pen or the feed was untreated. On days 0 and 26, respectively, pre- and posttrial fecal samples were collected, and resistance genes were characterized using shotgun metagenomics. Treatment with ceftiofur was not associated with changes to β-lactam resistance genes. However, cattle fed chlortetracycline had a significant increase in relative abundance of tetracycline resistance genes. There was also an increase of an AMR class not administered during the study, which is a possible indicator of coselection of resistance genes. Samples analyzed in this study had previously been evaluated by culture characterization (Escherichia coli and Salmonella) and quantitative PCR (qPCR) of metagenomic fecal DNA, which allowed comparison of results with this study. In the majority of samples, genes that were selectively enriched through culture and qPCR were not identified through shotgun metagenomic sequencing in this study, suggesting that changes previously documented did not reflect changes affecting the majority of bacterial genetic elements found in the predominant fecal resistome.IMPORTANCE Despite significant concerns about public health implications of AMR in relation to use of AMD in food animals, there are many unknowns about the long- and short-term impact of common uses of AMD for treatment, control, and prevention of disease. Additionally, questions commonly arise regarding how to best measure and quantify AMR genes in relation to public health risks and how to determine which genes are most important. These data provide an introductory view of the utility of using shotgun metagenomic sequencing data as an outcome for clinical trials evaluating the impact of using AMD in food animals.

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“…With that said, S. Reading has been shown to have enhanced ability to form biofilms under stress conditions (18) and has been isolated from produce (19). Multidrug resistance phenotypes, including resistance towards third-generation cephalosporins, also appear to be common in S. Reading strains, including those in dairy cows and beef feedlot cattle (20)(21)(22).…”

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confidence: 99%

Emergence of a Novel Salmonella enterica Serotype Reading Clonal Group Is Linked to Its Expansion in Commercial Turkey Production, Resulting in Unanticipated Human Illness in North America

Miller

Elnekave

Flores-Figueroa

et al. 2020

mSphere

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Two separate human outbreaks of Salmonella enterica serotype Reading occurred between 2017 and 2019 in the United States and Canada, and both outbreaks were linked to the consumption of raw turkey products. In this study, a comprehensive genomic investigation was conducted to reconstruct the evolutionary history of S. Reading from turkeys and to determine the genomic context of outbreaks involving this infrequently isolated Salmonella serotype. A total of 988 isolates of U.S. origin were examined using whole-genome-based approaches, including current and historical isolates from humans, meat, and live food animals. Broadly, isolates clustered into three major clades, with one apparently highly adapted turkey clade. Within the turkey clade, isolates clustered into three subclades, including an “emergent” clade that contained only isolates dated 2016 or later, with many of the isolates from these outbreaks. Genomic differences were identified between emergent and other turkey subclades, suggesting that the apparent success of currently circulating subclades is, in part, attributable to plasmid acquisitions conferring antimicrobial resistance, gain of phage-like sequences with cargo virulence factors, and mutations in systems that may be involved in beta-glucuronidase activity and resistance towards colicins. U.S. and Canadian outbreak isolates were found interspersed throughout the emergent subclade and the other circulating subclade. The emergence of a novel S. Reading turkey subclade, coinciding temporally with expansion in commercial turkey production and with U.S. and Canadian human outbreaks, indicates that emergent strains with higher potential for niche success were likely vertically transferred and rapidly disseminated from a common source. IMPORTANCE Increasingly, outbreak investigations involving foodborne pathogens are difficult due to the interconnectedness of food animal production and distribution, and homogeneous nature of industry integration, necessitating high-resolution genomic investigations to determine their basis. Fortunately, surveillance and whole-genome sequencing, combined with the public availability of these data, enable comprehensive queries to determine underlying causes of such outbreaks. Utilizing this pipeline, it was determined that a novel clone of Salmonella Reading has emerged that coincided with increased abundance in raw turkey products and two outbreaks of human illness in North America. The rapid dissemination of this highly adapted and conserved clone indicates that it was likely obtained from a common source and rapidly disseminated across turkey production. Key genomic changes may have contributed to its apparent continued success in commercial turkeys and ability to cause illness in humans.

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Population dynamics of enteric Salmonella in response to antimicrobial use in beef feedlot cattle

Cited by 20 publications

References 61 publications

A Common Practice of Widespread Antimicrobial Use in Horse Production Promotes Multi-Drug Resistance

A Common Practice of Widespread Antimicrobial Use in Horse Production Promotes Multi-Drug Resistance

Effects of Ceftiofur and Chlortetracycline on the Resistomes of Feedlot Cattle

Emergence of a Novel Salmonella enterica Serotype Reading Clonal Group Is Linked to Its Expansion in Commercial Turkey Production, Resulting in Unanticipated Human Illness in North America

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