Tulathromycin metaphylaxis increases nasopharyngeal isolation of multidrug resistant Mannheimia haemolytica in stocker heifers

Bovine respiratory disease (BRD) is a leading cause of disease in feedlot and stocker calves with Mannheimia haemolytica (MH) as one of the most common etiologies. One of the most effective means of controlling BRD is through metaphylaxis, which involves administering antimicrobials to all animals a...

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Main Authors: William B. Crosby, Brandi B. Karisch, Lari M. Hiott, Lee J. Pinnell, Alexandra Pittman, Jonathan G. Frye, Charlene R. Jackson, John Dustin Loy, William B. Epperson, John Blanton, Sarah F. Capik, Paul S. Morley, Amelia R. Woolums
Format: Article
Language:English
Published: Frontiers Media S.A. 2023-11-01
Series:Frontiers in Veterinary Science
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Online Access:https://www.frontiersin.org/articles/10.3389/fvets.2023.1256997/full
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author William B. Crosby
Brandi B. Karisch
Lari M. Hiott
Lee J. Pinnell
Alexandra Pittman
Jonathan G. Frye
Charlene R. Jackson
John Dustin Loy
William B. Epperson
John Blanton
Sarah F. Capik
Paul S. Morley
Amelia R. Woolums
author_facet William B. Crosby
Brandi B. Karisch
Lari M. Hiott
Lee J. Pinnell
Alexandra Pittman
Jonathan G. Frye
Charlene R. Jackson
John Dustin Loy
William B. Epperson
John Blanton
Sarah F. Capik
Paul S. Morley
Amelia R. Woolums
author_sort William B. Crosby
collection DOAJ
description Bovine respiratory disease (BRD) is a leading cause of disease in feedlot and stocker calves with Mannheimia haemolytica (MH) as one of the most common etiologies. One of the most effective means of controlling BRD is through metaphylaxis, which involves administering antimicrobials to all animals at high risk of developing BRD. However, increasing prevalence of multidrug resistant (MDR) MH may reduce efficacy of metaphylaxis due to decreased susceptibility to drugs used for metaphylaxis. Primarily, this study aimed to determine the effect of tulathromycin metaphylaxis and subsequent BRD treatment on antimicrobial resistance (AMR) in MH isolated from stocker calves. Secondary objectives included evaluating the effect of metaphylaxis and treatment for BRD on animal health and comparing the genetic relationship of MH isolated. Crossbred beef heifers (n = 331, mean weight = 232, SD = 17.8 kg) at high risk for BRD were randomly assigned to receive tulathromycin metaphylaxis (META, n = 167) or not (NO META, n = 164). Nasopharyngeal swabs were collected for MH isolation, antimicrobial susceptibility testing and whole genome sequencing at arrival and 3 (WK3) and 10 (WK10) weeks later. Mixed-effects logistic regression was used to identify risk factors for isolation of MH and MDR MH (resistant to ≥3 antimicrobial drug classes) at 3 and 10 weeks, BRD morbidity, and crude mortality. Animals in the META group had higher odds of isolation of MDR MH at 3 weeks [OR (95% CI) = 13.08 (5–30.9), p < 0.0001] and 10 weeks [OR (95% CI) = 5.92 (1.34–26.14), p = 0.019] after arrival. There was no difference in risk of isolation of any MH (resistant or susceptible) between META and NO META groups at all timepoints. Animals in the NO META group had 3 times higher odds of being treated for BRD [WK3: OR (95% CI) = 3.07 (1.70–5.52), p = 0.0002; WK10: OR (95% CI) = 2.76 (1.59–4.80), p = 0.0002]. Antimicrobial resistance genes found within isolates were associated with integrative conjugative element (ICE) genes. Tulathromycin metaphylaxis increased risk of isolation of MDR MH and in this population, the increase in MDR MH appeared to be associated with ICE containing antimicrobial resistance genes for multiple antimicrobial classes. This may have important implications for future efficacy of antimicrobials for control and treatment of BRD.
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spelling doaj.art-f2cfdf9c8f38486884ba75bd31913bc32023-11-20T08:24:53ZengFrontiers Media S.A.Frontiers in Veterinary Science2297-17692023-11-011010.3389/fvets.2023.12569971256997Tulathromycin metaphylaxis increases nasopharyngeal isolation of multidrug resistant Mannheimia haemolytica in stocker heifersWilliam B. Crosby0Brandi B. Karisch1Lari M. Hiott2Lee J. Pinnell3Alexandra Pittman4Jonathan G. Frye5Charlene R. Jackson6John Dustin Loy7William B. Epperson8John Blanton9Sarah F. Capik10Paul S. Morley11Amelia R. Woolums12Department of Pathobiology and Population Medicine, College of Veterinary Medicine, Mississippi State University, Mississippi State, MS, United StatesDepartment of Animal and Dairy Sciences, College of Agriculture and Life Sciences, Mississippi State University, Mississippi State, MS, United StatesPoultry Microbiological Safety and Processing Research Unit, U.S. National Poultry Research Center, United States Department of Agriculture-Agricultural Research Service, Athens, GA, United StatesVERO Program, School of Veterinary Medicine and Biomedical Sciences, Texas A&M University, Canyon, TX, United StatesDepartment of Animal and Dairy Sciences, College of Agriculture and Life Sciences, Mississippi State University, Mississippi State, MS, United StatesPoultry Microbiological Safety and Processing Research Unit, U.S. National Poultry Research Center, United States Department of Agriculture-Agricultural Research Service, Athens, GA, United StatesPoultry Microbiological Safety and Processing Research Unit, U.S. National Poultry Research Center, United States Department of Agriculture-Agricultural Research Service, Athens, GA, United StatesNebraska Veterinary Diagnostic Center, School of Veterinary Medicine and Biomedical Sciences, University of Nebraska-Lincoln, Lincoln, NE, United StatesDepartment of Pathobiology and Population Medicine, College of Veterinary Medicine, Mississippi State University, Mississippi State, MS, United StatesDepartment of Animal Sciences, College of Agriculture, Purdue University, West Lafayette, IN, United StatesTumbleweed Veterinary Services, PLLC, Amarillo, TX, United StatesVERO Program, School of Veterinary Medicine and Biomedical Sciences, Texas A&M University, Canyon, TX, United StatesDepartment of Pathobiology and Population Medicine, College of Veterinary Medicine, Mississippi State University, Mississippi State, MS, United StatesBovine respiratory disease (BRD) is a leading cause of disease in feedlot and stocker calves with Mannheimia haemolytica (MH) as one of the most common etiologies. One of the most effective means of controlling BRD is through metaphylaxis, which involves administering antimicrobials to all animals at high risk of developing BRD. However, increasing prevalence of multidrug resistant (MDR) MH may reduce efficacy of metaphylaxis due to decreased susceptibility to drugs used for metaphylaxis. Primarily, this study aimed to determine the effect of tulathromycin metaphylaxis and subsequent BRD treatment on antimicrobial resistance (AMR) in MH isolated from stocker calves. Secondary objectives included evaluating the effect of metaphylaxis and treatment for BRD on animal health and comparing the genetic relationship of MH isolated. Crossbred beef heifers (n = 331, mean weight = 232, SD = 17.8 kg) at high risk for BRD were randomly assigned to receive tulathromycin metaphylaxis (META, n = 167) or not (NO META, n = 164). Nasopharyngeal swabs were collected for MH isolation, antimicrobial susceptibility testing and whole genome sequencing at arrival and 3 (WK3) and 10 (WK10) weeks later. Mixed-effects logistic regression was used to identify risk factors for isolation of MH and MDR MH (resistant to ≥3 antimicrobial drug classes) at 3 and 10 weeks, BRD morbidity, and crude mortality. Animals in the META group had higher odds of isolation of MDR MH at 3 weeks [OR (95% CI) = 13.08 (5–30.9), p < 0.0001] and 10 weeks [OR (95% CI) = 5.92 (1.34–26.14), p = 0.019] after arrival. There was no difference in risk of isolation of any MH (resistant or susceptible) between META and NO META groups at all timepoints. Animals in the NO META group had 3 times higher odds of being treated for BRD [WK3: OR (95% CI) = 3.07 (1.70–5.52), p = 0.0002; WK10: OR (95% CI) = 2.76 (1.59–4.80), p = 0.0002]. Antimicrobial resistance genes found within isolates were associated with integrative conjugative element (ICE) genes. Tulathromycin metaphylaxis increased risk of isolation of MDR MH and in this population, the increase in MDR MH appeared to be associated with ICE containing antimicrobial resistance genes for multiple antimicrobial classes. This may have important implications for future efficacy of antimicrobials for control and treatment of BRD.https://www.frontiersin.org/articles/10.3389/fvets.2023.1256997/fullantimicrobial resistancewhole genome sequencingantimicrobial susceptibilitybovine respiratory diseasebeef productionbacterial culture
spellingShingle William B. Crosby
Brandi B. Karisch
Lari M. Hiott
Lee J. Pinnell
Alexandra Pittman
Jonathan G. Frye
Charlene R. Jackson
John Dustin Loy
William B. Epperson
John Blanton
Sarah F. Capik
Paul S. Morley
Amelia R. Woolums
Tulathromycin metaphylaxis increases nasopharyngeal isolation of multidrug resistant Mannheimia haemolytica in stocker heifers
Frontiers in Veterinary Science
antimicrobial resistance
whole genome sequencing
antimicrobial susceptibility
bovine respiratory disease
beef production
bacterial culture
title Tulathromycin metaphylaxis increases nasopharyngeal isolation of multidrug resistant Mannheimia haemolytica in stocker heifers
title_full Tulathromycin metaphylaxis increases nasopharyngeal isolation of multidrug resistant Mannheimia haemolytica in stocker heifers
title_fullStr Tulathromycin metaphylaxis increases nasopharyngeal isolation of multidrug resistant Mannheimia haemolytica in stocker heifers
title_full_unstemmed Tulathromycin metaphylaxis increases nasopharyngeal isolation of multidrug resistant Mannheimia haemolytica in stocker heifers
title_short Tulathromycin metaphylaxis increases nasopharyngeal isolation of multidrug resistant Mannheimia haemolytica in stocker heifers
title_sort tulathromycin metaphylaxis increases nasopharyngeal isolation of multidrug resistant mannheimia haemolytica in stocker heifers
topic antimicrobial resistance
whole genome sequencing
antimicrobial susceptibility
bovine respiratory disease
beef production
bacterial culture
url https://www.frontiersin.org/articles/10.3389/fvets.2023.1256997/full
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