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      Association between antimicrobial drug class for treatment and retreatment of bovine respiratory disease (BRD) and frequency of resistant BRD pathogen isolation from veterinary diagnostic laboratory samples

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          Abstract

          Although 90% of BRD relapses are reported to receive retreatment with a different class of antimicrobial, studies examining the impact of antimicrobial selection (i.e. bactericidal or bacteriostatic) on retreatment outcomes and the emergence of antimicrobial resistance (AMR) are deficient in the published literature. This survey was conducted to determine the association between antimicrobial class selection for treatment and retreatment of BRD relapses on antimicrobial susceptibility of Mannheimia haemolytica, Pasteurella multocida, and Histophilus somni. Pathogens were isolated from samples submitted to the Iowa State University Veterinary Diagnostic Laboratory from January 2013 to December 2015. A total of 781 isolates with corresponding animal case histories, including treatment protocols, were included in the analysis. Original susceptibility testing of these isolates for ceftiofur, danofloxacin, enrofloxacin, florfenicol, oxytetracycline, spectinomycin, tilmicosin, and tulathromycin was performed using Clinical and Laboratory Standards Institute guidelines. Data were analyzed using a Bayesian approach to evaluate whether retreatment with antimicrobials of different mechanistic classes (bactericidal or bacteriostatic) increased the probability of resistant BRD pathogen isolation in calves. The posterior distribution we calculated suggests that an increased number of treatments is associated with a greater probability of isolates resistant to at least one antimicrobial. Furthermore, the frequency of resistant BRD bacterial isolates was greater with retreatment using antimicrobials of different mechanistic classes than retreatment with the same class. Specifically, treatment protocols using a bacteriostatic drug first followed by retreatment with a bactericidal drug were associated with a higher frequency of resistant BRD pathogen isolation. In particular, first treatment with tulathromycin (bacteriostatic) followed by ceftiofur (bactericidal) was associated with the highest probability of resistant M. haemolytica among all antimicrobial combinations. These observations suggest that consideration should be given to antimicrobial pharmacodynamics when selecting drugs for retreatment of BRD. However, prospective studies are needed to determine the clinical relevance to antimicrobial stewardship programs in livestock production systems.

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          Antibiotic interactions that select against resistance.

          Multidrug combinations are increasingly important in combating the spread of antibiotic-resistance in bacterial pathogens. On a broader scale, such combinations are also important in understanding microbial ecology and evolution. Although the effects of multidrug combinations on bacterial growth have been studied extensively, relatively little is known about their impact on the differential selection between sensitive and resistant bacterial populations. Normally, the presence of a drug confers an advantage on its resistant mutants in competition with the sensitive wild-type population. Here we show, by using a direct competition assay between doxycycline-resistant and doxycycline-sensitive Escherichia coli, that this differential selection can be inverted in a hyper-antagonistic class of drug combinations. Used in such a combination, a drug can render the combined treatment selective against the drug's own resistance allele. Further, this inversion of selection seems largely insensitive to the underlying resistance mechanism and occurs, at sublethal concentrations, while maintaining inhibition of the wild type. These seemingly paradoxical results can be rationalized in terms of a simple geometric argument. Our findings demonstrate a previously unappreciated feature of the fitness landscape for the evolution of resistance and point to a trade-off between the effect of drug interactions on absolute potency and the relative competitive selection that they impose on emerging resistant populations.
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            Drug interactions and the evolution of antibiotic resistance.

            Large-scale, systems biology approaches now allow us to systematically map synergistic and antagonistic interactions between drugs. Consequently, drug antagonism is emerging as a powerful tool to study biological function and relatedness between cellular components as well as to uncover mechanisms of drug action. Furthermore, theoretical models and new experiments suggest that antagonistic interactions between antibiotics can counteract the evolution of drug resistance.
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              Veterinary drug usage and antimicrobial resistance in bacteria of animal origin.

              In the production of food animals, large amounts of antimicrobial agents are used for therapy and prophylaxis of bacterial infections and in feed to promote growth. There are large variations in the amounts of antimicrobial agents used to produce the same amount of meat among the different European countries, which leaves room for considerable reductions in some countries. The emergence of resistant bacteria and resistance genes due to the use of antimicrobial agents are well documented. In Denmark it has been possible to reduce the usage of antimicrobial agents for food animals significantly and in general decreases in resistance have followed. Guidelines for prudent use of antimicrobial agents may help to slow down the selection for resistance and should be based on knowledge regarding the normal susceptibility patterns of the causative agents and take into account the potential problems for human health. Current knowledge regarding the occurrence of antimicrobial resistance in food animals, the quantitative impact of the use of different antimicrobial agents on selection of resistance and the most appropriate treatment regimes to limit the development of resistance is incomplete. Programmes monitoring the occurrence and development of resistance and consumption of antimicrobial agents are strongly desirable, as is research into the most appropriate ways to use antimicrobial agents in veterinary medicine.
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                Author and article information

                Contributors
                Role: ConceptualizationRole: Formal analysisRole: InvestigationRole: Project administrationRole: Writing – original draftRole: Writing – review & editing
                Role: ConceptualizationRole: Data curationRole: SupervisionRole: Writing – review & editing
                Role: Formal analysisRole: Writing – original draftRole: Writing – review & editing
                Role: Data curationRole: Formal analysisRole: Writing – review & editing
                Role: Data curationRole: Writing – review & editing
                Role: Data curationRole: Formal analysisRole: InvestigationRole: MethodologyRole: Writing – review & editing
                Role: Data curationRole: MethodologyRole: Writing – review & editing
                Role: Data curationRole: InvestigationRole: MethodologyRole: Writing – review & editing
                Role: Writing – review & editing
                Role: ConceptualizationRole: Formal analysisRole: Writing – review & editing
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, CA USA )
                1932-6203
                13 December 2019
                2019
                : 14
                : 12
                : e0219104
                Affiliations
                [1 ] Department of Veterinary Diagnostic and Production Animal Medicine, College of Veterinary Medicine, Iowa State University, Ames, IA, United States of America
                [2 ] Department of Anatomy and Physiology, College of Veterinary Medicine, Kansas State University, Manhattan, KS, United States of America
                [3 ] Department of Information Management and Business Analytics, College of Business and Public Administration, Drake University, Des Moines, IA, United States of America
                [4 ] Department of Clinical Sciences, College of Veterinary Medicine, Kansas State University, Manhattan, KS, United States of America
                University of Minnesota, UNITED STATES
                Author notes

                Competing Interests: JFC has been a consultant for Intervet-Schering Plough Animal Health (now Merck Animal Health), Bayer Animal Health, Boehringer-Ingelheim Vetmedica, Zoetis Animal Health, Midwest Veterinary Services, and Norbrook Laboratories Ltd. Author JFC is supported by the Agriculture and Food Research Initiative Competitive Grants no. 2017-67015-27124 and 2019-04991 from the USDA National Institute of Food and Agriculture and served as USDA NIFA Grant Panel Manager from 2017- 2018. AOC has been a consultant for Bayer Animal Health. This does not alter our adherence to all the PLOS ONE policies on sharing data and materials. There are no patents, products in development, or marketed products to declare.

                Author information
                http://orcid.org/0000-0003-1802-3991
                http://orcid.org/0000-0003-3784-5982
                Article
                PONE-D-19-16691
                10.1371/journal.pone.0219104
                6910856
                31835273
                0c95fd78-28ec-46b7-bab8-0991cddb9f95
                © 2019 Coetzee et al

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                : 12 June 2019
                : 19 November 2019
                Page count
                Figures: 9, Tables: 8, Pages: 24
                Funding
                Author JFC received consulting fees from Intervet-Schering Plough Animal Health (now Merck Animal Health), Bayer Animal Health, Boehringer-Ingelheim Vetmedica, Zoetis Animal Health, Midwest Veterinary Services, and Norbrook Laboratories Ltd. Author JFC is supported by the Agriculture and Food Research Initiative Competitive Grants no. 2017-67015-27124 and 2019-04991 from the USDA National Institute of Food and Agriculture and served as USDA NIFA Grant Panel Manager from 2017- 2018. AOC has received consulting fees from Bayer Animal Health. The specific roles of these authors are articulated in the 'author contributions' section. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Medicine and Health Sciences
                Pharmacology
                Drugs
                Antimicrobials
                Biology and Life Sciences
                Microbiology
                Microbial Control
                Antimicrobials
                Biology and Life Sciences
                Microbiology
                Microbial Control
                Antimicrobial Resistance
                Medicine and Health Sciences
                Pharmacology
                Antimicrobial Resistance
                Biology and Life Sciences
                Veterinary Science
                Veterinary Medicine
                Livestock Care
                Medicine and Health Sciences
                Pharmaceutics
                Drug Therapy
                Physical Sciences
                Mathematics
                Probability Theory
                Probability Distribution
                Biology and Life Sciences
                Microbiology
                Medical Microbiology
                Microbial Pathogens
                Bacterial Pathogens
                Pasteurella Multocida
                Medicine and Health Sciences
                Pathology and Laboratory Medicine
                Pathogens
                Microbial Pathogens
                Bacterial Pathogens
                Pasteurella Multocida
                Biology and Life Sciences
                Organisms
                Eukaryota
                Animals
                Vertebrates
                Amniotes
                Mammals
                Bovines
                Cattle
                Biology and Life Sciences
                Organisms
                Eukaryota
                Animals
                Vertebrates
                Amniotes
                Mammals
                Ruminants
                Cattle
                Biology and Life Sciences
                Microbiology
                Medical Microbiology
                Microbial Pathogens
                Bacterial Pathogens
                Medicine and Health Sciences
                Pathology and Laboratory Medicine
                Pathogens
                Microbial Pathogens
                Bacterial Pathogens
                Custom metadata
                This study used retrospective epidemiological data collected at Iowa State Veterinary Diagnostic Laboratory. Data contain private information that cannot be disclosed without individual agreement of each of the veterinarians and producers that submitted samples to the veterinary diagnostic laboratory at Iowa State University. Explicit permission was not obtained from animal owners to make this data publicly available. These restrictions prohibit authors from making the data set publicly available. Data may be available from Iowa State University's Office of Research Compliance for researchers who meet the criteria for access to confidential data. Interested researchers may contact Sarah Kaatz, Director of the Office for Responsible Research ( skaatz@ 123456iastate.edu ) or the corresponding author with data requests.

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