Influence of Single Dose Enrofloxacin Injection on Development of Fluoroquinolone Resistance in <i>Campylobacter jejuni</i> in Calves

Fluoroquinolone (FQ) resistance in a major foodborne bacterial pathogen, <i>Campylobacter jejuni</i>, derived from cattle has recently become prevalent and poses a significant public health concern. However, the underlying factors for this increase are not entirely clear. To evaluate the...

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Main Authors: Debora Brito Goulart, Ashenafi Feyisa Beyi, Zuowei Wu, Mehmet Cemal Adiguzel, Samantha Wilson, Changyun Xu, Jinji Pang, Renee Dewell, Grant A. Dewell, Paul J. Plummer, Qijing Zhang, Orhan Sahin
Format: Article
Language:English
Published: MDPI AG 2022-10-01
Series:Antibiotics
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Online Access:https://www.mdpi.com/2079-6382/11/10/1407
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author Debora Brito Goulart
Ashenafi Feyisa Beyi
Zuowei Wu
Mehmet Cemal Adiguzel
Samantha Wilson
Changyun Xu
Jinji Pang
Renee Dewell
Grant A. Dewell
Paul J. Plummer
Qijing Zhang
Orhan Sahin
author_facet Debora Brito Goulart
Ashenafi Feyisa Beyi
Zuowei Wu
Mehmet Cemal Adiguzel
Samantha Wilson
Changyun Xu
Jinji Pang
Renee Dewell
Grant A. Dewell
Paul J. Plummer
Qijing Zhang
Orhan Sahin
author_sort Debora Brito Goulart
collection DOAJ
description Fluoroquinolone (FQ) resistance in a major foodborne bacterial pathogen, <i>Campylobacter jejuni</i>, derived from cattle has recently become prevalent and poses a significant public health concern. However, the underlying factors for this increase are not entirely clear. To evaluate the effect of enrofloxacin treatment on FQ-resistance development in <i>C. jejuni</i>, 35 commercial calves were equally divided into five groups (Groups 1–5) and were orally inoculated with FQ-susceptible (FQ-S) <i>C. jejuni</i>. Eight days later, Groups 4 and 5 were challenged with <i>Mannheimia haemolytica</i> via a transtracheal route to induce a respiratory disease; after 8 days, Groups 2, 3, 4, and 5 were injected subcutaneously with enrofloxacin (7.5 mg/kg for Groups 2 and 4, and 12.5 mg/kg for Groups 3 and 5). Colonization levels by FQ-resistant (FQ-R) and FQ-S <i>Campylobacter</i> in rectal feces were determined via differential culture throughout the experiment. Before oral inoculation with <i>C. jejuni</i>, only five calves were naturally colonized by <i>Campylobacter</i>, four of which were also colonized by FQ-R <i>C. jejuni</i> (three in Group 1 and one in Group 3). Soon after the oral inoculation, almost all calves in the groups became stably colonized by FQ-S <i>C. jejuni</i> (~3–6 log<sub>10</sub> CFU/g), except that the four calves that were pre-colonized before inoculation remained positive with both FQ-R and FQ-S <i>C. jejuni</i>. Following enrofloxacin administration, <i>C. jejuni</i> colonization declined sharply and rapidly in all treated groups to undetectable levels; however, the vast majority of the animals were recolonized by <i>C. jejuni</i> at comparable levels 72 h after the treatment. Notably, no FQ-R <i>C. jejuni</i> was detected in any of the calves that received enrofloxacin, regardless of the drug dose used or disease status of the animals. The lack of detection of FQ-R <i>C. jejuni</i> was likely due to the localized high concentration of the antibiotic in the intestine, which may have prevented the emergence of the FQ-R mutant. These findings indicate that single-dose enrofloxacin use in cattle poses a low risk for selection of de novo FQ-R mutants in <i>C. jejuni</i>.
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spelling doaj.art-97bbda0bcf6a463f9f6185358df750f52023-11-23T22:35:58ZengMDPI AGAntibiotics2079-63822022-10-011110140710.3390/antibiotics11101407Influence of Single Dose Enrofloxacin Injection on Development of Fluoroquinolone Resistance in <i>Campylobacter jejuni</i> in CalvesDebora Brito Goulart0Ashenafi Feyisa Beyi1Zuowei Wu2Mehmet Cemal Adiguzel3Samantha Wilson4Changyun Xu5Jinji Pang6Renee Dewell7Grant A. Dewell8Paul J. Plummer9Qijing Zhang10Orhan Sahin11Department of Veterinary Microbiology and Preventive Medicine, College of Veterinary Medicine, Iowa State University, Ames, IA 50011, USADepartment of Veterinary Microbiology and Preventive Medicine, College of Veterinary Medicine, Iowa State University, Ames, IA 50011, USADepartment of Veterinary Microbiology and Preventive Medicine, College of Veterinary Medicine, Iowa State University, Ames, IA 50011, USADepartment of Veterinary Microbiology and Preventive Medicine, College of Veterinary Medicine, Iowa State University, Ames, IA 50011, USADepartment of Veterinary Microbiology and Preventive Medicine, College of Veterinary Medicine, Iowa State University, Ames, IA 50011, USADepartment of Veterinary Microbiology and Preventive Medicine, College of Veterinary Medicine, Iowa State University, Ames, IA 50011, USADepartment of Veterinary Microbiology and Preventive Medicine, College of Veterinary Medicine, Iowa State University, Ames, IA 50011, USACenter for Food Security and Public Health, College of Veterinary Medicine, Iowa State University, Ames, IA 50011, USADepartment of Veterinary Diagnostic and Production Animal Medicine, College of Veterinary Medicine, Iowa State University, Ames, IA 50011, USADepartment of Veterinary Microbiology and Preventive Medicine, College of Veterinary Medicine, Iowa State University, Ames, IA 50011, USADepartment of Veterinary Microbiology and Preventive Medicine, College of Veterinary Medicine, Iowa State University, Ames, IA 50011, USADepartment of Veterinary Diagnostic and Production Animal Medicine, College of Veterinary Medicine, Iowa State University, Ames, IA 50011, USAFluoroquinolone (FQ) resistance in a major foodborne bacterial pathogen, <i>Campylobacter jejuni</i>, derived from cattle has recently become prevalent and poses a significant public health concern. However, the underlying factors for this increase are not entirely clear. To evaluate the effect of enrofloxacin treatment on FQ-resistance development in <i>C. jejuni</i>, 35 commercial calves were equally divided into five groups (Groups 1–5) and were orally inoculated with FQ-susceptible (FQ-S) <i>C. jejuni</i>. Eight days later, Groups 4 and 5 were challenged with <i>Mannheimia haemolytica</i> via a transtracheal route to induce a respiratory disease; after 8 days, Groups 2, 3, 4, and 5 were injected subcutaneously with enrofloxacin (7.5 mg/kg for Groups 2 and 4, and 12.5 mg/kg for Groups 3 and 5). Colonization levels by FQ-resistant (FQ-R) and FQ-S <i>Campylobacter</i> in rectal feces were determined via differential culture throughout the experiment. Before oral inoculation with <i>C. jejuni</i>, only five calves were naturally colonized by <i>Campylobacter</i>, four of which were also colonized by FQ-R <i>C. jejuni</i> (three in Group 1 and one in Group 3). Soon after the oral inoculation, almost all calves in the groups became stably colonized by FQ-S <i>C. jejuni</i> (~3–6 log<sub>10</sub> CFU/g), except that the four calves that were pre-colonized before inoculation remained positive with both FQ-R and FQ-S <i>C. jejuni</i>. Following enrofloxacin administration, <i>C. jejuni</i> colonization declined sharply and rapidly in all treated groups to undetectable levels; however, the vast majority of the animals were recolonized by <i>C. jejuni</i> at comparable levels 72 h after the treatment. Notably, no FQ-R <i>C. jejuni</i> was detected in any of the calves that received enrofloxacin, regardless of the drug dose used or disease status of the animals. The lack of detection of FQ-R <i>C. jejuni</i> was likely due to the localized high concentration of the antibiotic in the intestine, which may have prevented the emergence of the FQ-R mutant. These findings indicate that single-dose enrofloxacin use in cattle poses a low risk for selection of de novo FQ-R mutants in <i>C. jejuni</i>.https://www.mdpi.com/2079-6382/11/10/1407<i>Campylobacter</i>antimicrobial resistancecattleintestinal colonizationfecesbovine respiratory disease (BRD)
spellingShingle Debora Brito Goulart
Ashenafi Feyisa Beyi
Zuowei Wu
Mehmet Cemal Adiguzel
Samantha Wilson
Changyun Xu
Jinji Pang
Renee Dewell
Grant A. Dewell
Paul J. Plummer
Qijing Zhang
Orhan Sahin
Influence of Single Dose Enrofloxacin Injection on Development of Fluoroquinolone Resistance in <i>Campylobacter jejuni</i> in Calves
Antibiotics
<i>Campylobacter</i>
antimicrobial resistance
cattle
intestinal colonization
feces
bovine respiratory disease (BRD)
title Influence of Single Dose Enrofloxacin Injection on Development of Fluoroquinolone Resistance in <i>Campylobacter jejuni</i> in Calves
title_full Influence of Single Dose Enrofloxacin Injection on Development of Fluoroquinolone Resistance in <i>Campylobacter jejuni</i> in Calves
title_fullStr Influence of Single Dose Enrofloxacin Injection on Development of Fluoroquinolone Resistance in <i>Campylobacter jejuni</i> in Calves
title_full_unstemmed Influence of Single Dose Enrofloxacin Injection on Development of Fluoroquinolone Resistance in <i>Campylobacter jejuni</i> in Calves
title_short Influence of Single Dose Enrofloxacin Injection on Development of Fluoroquinolone Resistance in <i>Campylobacter jejuni</i> in Calves
title_sort influence of single dose enrofloxacin injection on development of fluoroquinolone resistance in i campylobacter jejuni i in calves
topic <i>Campylobacter</i>
antimicrobial resistance
cattle
intestinal colonization
feces
bovine respiratory disease (BRD)
url https://www.mdpi.com/2079-6382/11/10/1407
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