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      Effects of Ceftiofur and Chlortetracycline on the Resistomes of Feedlot Cattle

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          ABSTRACT

          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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          Most cited references23

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          Call of the wild: antibiotic resistance genes in natural environments.

          Antibiotic-resistant pathogens are profoundly important to human health, but the environmental reservoirs of resistance determinants are poorly understood. The origins of antibiotic resistance in the environment is relevant to human health because of the increasing importance of zoonotic diseases as well as the need for predicting emerging resistant pathogens. This Review explores the presence and spread of antibiotic resistance in non-agricultural, non-clinical environments and demonstrates the need for more intensive investigation on this subject.
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            CTX-M Enzymes: Origin and Diffusion

            CTX-M β-lactamases are considered a paradigm in the evolution of a resistance mechanism. Incorporation of different chromosomal bla CTX-M related genes from different species of Kluyvera has derived in different CTX-M clusters. In silico analyses have shown that this event has occurred at least nine times; in CTX-M-1 cluster (3), CTX-M-2 and CTX-M-9 clusters (2 each), and CTX-M-8 and CTX-M-25 clusters (1 each). This has been mainly produced by the participation of genetic mobilization units such as insertion sequences (ISEcp1 or ISCR1) and the later incorporation in hierarchical structures associated with multifaceted genetic structures including complex class 1 integrons and transposons. The capture of these bla CTX-M genes from the environment by highly mobilizable structures could have been a random event. Moreover, after incorporation within these structures, β-lactam selective force such as that exerted by cefotaxime and ceftazidime has fueled mutational events underscoring diversification of different clusters. Nevertheless, more variants of CTX-M enzymes, including those not inhibited by β-lactamase inhibitors such as clavulanic acid (IR-CTX-M variants), only obtained under in in vitro experiments, are still waiting to emerge in the clinical setting. Penetration and the later global spread of CTX-M producing organisms have been produced with the participation of the so-called “epidemic resistance plasmids” often carried in multi-drug resistant and virulent high-risk clones. All these facts but also the incorporation and co-selection of emerging resistance determinants within CTX-M producing bacteria, such as those encoding carbapenemases, depict the currently complex pandemic scenario of multi-drug resistant isolates.
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              Metagenomic and network analysis reveal wide distribution and co-occurrence of environmental antibiotic resistance genes.

              A metagenomic approach and network analysis was used to investigate the wide-spectrum profiles of antibiotic resistance genes (ARGs) and their co-occurrence patterns in 50 samples from 10 typical environments. In total, 260 ARG subtypes belonging to 18 ARG types were detected with an abundance range of 5.4 × 10(-6)-2.2 × 10(-1) copy of ARG per copy of 16S-rRNA gene. The trend of the total ARG abundances in environments matched well with the levels of anthropogenic impacts on these environments. From the less impacted environments to the seriously impacted environments, the total ARG abundances increased up to three orders of magnitude, that is, from 3.2 × 10(-3) to 3.1 × 10(0) copy of ARG per copy of 16S-rRNA gene. The abundant ARGs were associated with aminoglycoside, bacitracin, β-lactam, chloramphenicol, macrolide-lincosamide-streptogramin, quinolone, sulphonamide and tetracycline, in agreement with the antibiotics extensively used in human medicine or veterinary medicine/promoters. The widespread occurrences and abundance variation trend of vancomycin resistance genes in different environments might imply the spread of vancomycin resistance genes because of the selective pressure resulting from vancomycin use. The simultaneous enrichment of 12 ARG types in adult chicken faeces suggests the coselection of multiple ARGs in this production system. Non-metric multidimensional scaling analysis revealed that samples belonging to the same environment generally possessed similar ARG compositions. Based on the co-occurrence pattern revealed by network analysis, tetM and aminoglycoside resistance protein, the hubs of the ARG network, are proposed to be indicators to quantitatively estimate the abundance of 23 other co-occurring ARG subtypes by power functions.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                Appl Environ Microbiol
                Appl. Environ. Microbiol
                aem
                aem
                AEM
                Applied and Environmental Microbiology
                American Society for Microbiology (1752 N St., N.W., Washington, DC )
                0099-2240
                1098-5336
                4 May 2018
                18 June 2018
                1 July 2018
                18 June 2018
                : 84
                : 13
                : e00610-18
                Affiliations
                [a ]Department of Animal Sciences, Colorado State University, Fort Collins, Colorado, USA
                [b ]Department of Veterinary Pathobiology, Texas A&M University, College Station, Texas, USA
                [c ]Department of Large Animal Clinical Sciences, Michigan State University, East Lansing, Michigan, USA
                [d ]Department of Animal and Food Sciences, Texas Tech University, Lubbock, Texas, USA
                [e ]Department of Clinical Sciences, Colorado State University, Fort Collins, Colorado, USA
                [f ]Instituto Nacional de Investigacion Agropecuaria, Treinta y Tres, Uruguay
                [g ]Department of Animal Sciences, University of California—Davis, Davis, California, USA
                INRS—Institut Armand-Frappier
                Author notes
                Address correspondence to Keith E. Belk, keith.belk@ 123456colostate.edu .

                P.S.M. and K.E.B. contributed equally to this article.

                Citation Weinroth MD, Scott HM, Norby B, Loneragan GH, Noyes NR, Rovira P, Doster E, Yang X, Woerner DR, Morley PS, Belk KE. 2018. Effects of ceftiofur and chlortetracycline on the resistomes of feedlot cattle. Appl Environ Microbiol 84:e00610-18. https://doi.org/10.1128/AEM.00610-18.

                Author information
                https://orcid.org/0000-0001-6149-1008
                Article
                00610-18
                10.1128/AEM.00610-18
                6007121
                29728379
                62f14059-69f5-48d9-baa6-cc283122d778
                Copyright © 2018 Weinroth et al.

                This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license.

                History
                : 15 March 2018
                : 24 April 2018
                Page count
                supplementary-material: 2, Figures: 3, Tables: 3, Equations: 1, References: 37, Pages: 12, Words: 7883
                Funding
                Funded by: USDA | National Institute of Food and Agriculture (NIFA), https://doi.org/10.13039/100005825;
                Award ID: 2010-51110-21083
                Award Recipient : Award Recipient : Award Recipient : Award Recipient :
                Funded by: USDA | National Institute of Food and Agriculture (NIFA), https://doi.org/10.13039/100005825;
                Award ID: 2008-35201-04682
                Award Recipient : Award Recipient : Award Recipient :
                Funded by: USDA | National Institute of Food and Agriculture (NIFA), https://doi.org/10.13039/100005825;
                Award ID: 2008-35210-30235
                Award Recipient : Award Recipient : Award Recipient :
                Funded by: USDA | National Institute of Food and Agriculture (NIFA), https://doi.org/10.13039/100005825;
                Award ID: 2015-68003-23048
                Award Recipient : Award Recipient : Award Recipient : Award Recipient : Award Recipient :
                Categories
                Microbial Ecology
                Custom metadata
                July 2018

                Microbiology & Virology
                antibiotic resistance,antimicrobial agents,cattle,feedlot,metagenomics,postantibiotic effect

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