High Prevalence of Cefotaxime Resistant Bacteria in Grazing Beef Cattle: A Cross Sectional Study

Although the over-use of antibiotics during food animal production is a potential driver of antimicrobial resistant microorganisms (ARMs), a high prevalence of cefotaxime resistant bacteria (CRB) has been observed in grazing animals raised without antibiotic supplementation. In this cross-sectional...

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Main Authors: Sarah Markland, Thomas A. Weppelmann, Zhengxin Ma, Shinyoung Lee, Raies A. Mir, Lin Teng, Amber Ginn, Choonghee Lee, Maria Ukhanova, Sebastian Galindo, Chad Carr, Nicolas DiLorenzo, Soohyoun Ahn, Jae-Hyung Mah, Hae-Yeong Kim, Volker Mai, Ray Mobley, J. Glenn Morris, KwangCheol Casey Jeong
Format: Article
Language:English
Published: Frontiers Media S.A. 2019-02-01
Series:Frontiers in Microbiology
Subjects:
Online Access:https://www.frontiersin.org/article/10.3389/fmicb.2019.00176/full
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author Sarah Markland
Sarah Markland
Thomas A. Weppelmann
Zhengxin Ma
Zhengxin Ma
Shinyoung Lee
Shinyoung Lee
Raies A. Mir
Raies A. Mir
Lin Teng
Lin Teng
Amber Ginn
Amber Ginn
Choonghee Lee
Choonghee Lee
Maria Ukhanova
Sebastian Galindo
Chad Carr
Nicolas DiLorenzo
Soohyoun Ahn
Jae-Hyung Mah
Jae-Hyung Mah
Hae-Yeong Kim
Volker Mai
Volker Mai
Ray Mobley
J. Glenn Morris
J. Glenn Morris
KwangCheol Casey Jeong
KwangCheol Casey Jeong
KwangCheol Casey Jeong
spellingShingle Sarah Markland
Sarah Markland
Thomas A. Weppelmann
Zhengxin Ma
Zhengxin Ma
Shinyoung Lee
Shinyoung Lee
Raies A. Mir
Raies A. Mir
Lin Teng
Lin Teng
Amber Ginn
Amber Ginn
Choonghee Lee
Choonghee Lee
Maria Ukhanova
Sebastian Galindo
Chad Carr
Nicolas DiLorenzo
Soohyoun Ahn
Jae-Hyung Mah
Jae-Hyung Mah
Hae-Yeong Kim
Volker Mai
Volker Mai
Ray Mobley
J. Glenn Morris
J. Glenn Morris
KwangCheol Casey Jeong
KwangCheol Casey Jeong
KwangCheol Casey Jeong
High Prevalence of Cefotaxime Resistant Bacteria in Grazing Beef Cattle: A Cross Sectional Study
Frontiers in Microbiology
cefotaxime
antibiotic resistance
beef cattle
cross sectional study
farm management survey
author_facet Sarah Markland
Sarah Markland
Thomas A. Weppelmann
Zhengxin Ma
Zhengxin Ma
Shinyoung Lee
Shinyoung Lee
Raies A. Mir
Raies A. Mir
Lin Teng
Lin Teng
Amber Ginn
Amber Ginn
Choonghee Lee
Choonghee Lee
Maria Ukhanova
Sebastian Galindo
Chad Carr
Nicolas DiLorenzo
Soohyoun Ahn
Jae-Hyung Mah
Jae-Hyung Mah
Hae-Yeong Kim
Volker Mai
Volker Mai
Ray Mobley
J. Glenn Morris
J. Glenn Morris
KwangCheol Casey Jeong
KwangCheol Casey Jeong
KwangCheol Casey Jeong
author_sort Sarah Markland
title High Prevalence of Cefotaxime Resistant Bacteria in Grazing Beef Cattle: A Cross Sectional Study
title_short High Prevalence of Cefotaxime Resistant Bacteria in Grazing Beef Cattle: A Cross Sectional Study
title_full High Prevalence of Cefotaxime Resistant Bacteria in Grazing Beef Cattle: A Cross Sectional Study
title_fullStr High Prevalence of Cefotaxime Resistant Bacteria in Grazing Beef Cattle: A Cross Sectional Study
title_full_unstemmed High Prevalence of Cefotaxime Resistant Bacteria in Grazing Beef Cattle: A Cross Sectional Study
title_sort high prevalence of cefotaxime resistant bacteria in grazing beef cattle: a cross sectional study
publisher Frontiers Media S.A.
series Frontiers in Microbiology
issn 1664-302X
publishDate 2019-02-01
description Although the over-use of antibiotics during food animal production is a potential driver of antimicrobial resistant microorganisms (ARMs), a high prevalence of cefotaxime resistant bacteria (CRB) has been observed in grazing animals raised without antibiotic supplementation. In this cross-sectional study, the prevalence and concentration of CRB in beef cattle on grazing farms were investigated. Fecal samples from the recto-anal junction of cattle (n = 840) and environmental samples (n = 258) were collected from 17 farms in North and Central Florida in the United States, and a survey of farm characteristics, animal husbandry practices, and antibiotic usage was conducted. CRB were detected in fecal samples from 47.4% of all cattle, with the prevalence ranging from 21.1 to 87.5% on farms, and significantly higher (P < 0.001) in calves compared to adult cows (54.1 vs. 41.8%). Environmental samples had a higher prevalence than fecal samples (P < 0.001), with CRB detected in 88.6% of water, 98.7% of soil, and 95.7% of forage samples. Compared to the concentration (log CFU/g) of CRB in fecal samples (2.95, 95% CI: 2.89, 3.02), the concentration of CRB was higher (P < 0.001) in soil and forage samples (5.37, 95% CI: 5.16, 5.57) and lower (P < 0.001) in water samples (1.08, 95% CI: 0.82, 1.36). Soil microbiota from farms with high prevalence of CRB clustered closer together and the proportion of Phylum Proteobacteria was higher on farms with high prevalence of CRB resistance. Large farming operations were associated with a 58% higher likelihood of CRB detection in fecal samples. Regular cleaning of drinking troughs and the addition of ionophores to feed were associated with CRB reduction in fecal samples. Taken together, the widespread of CRB into both cattle seldom treated with cephalosporin antibiotics and the surrounding environment suggests the environment is a natural source of antimicrobial resistance in beef cattle.
topic cefotaxime
antibiotic resistance
beef cattle
cross sectional study
farm management survey
url https://www.frontiersin.org/article/10.3389/fmicb.2019.00176/full
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spelling doaj-7e57d45f5093490b83da5ebcc7a5a3472020-11-24T21:45:48ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2019-02-011010.3389/fmicb.2019.00176408423High Prevalence of Cefotaxime Resistant Bacteria in Grazing Beef Cattle: A Cross Sectional StudySarah Markland0Sarah Markland1Thomas A. Weppelmann2Zhengxin Ma3Zhengxin Ma4Shinyoung Lee5Shinyoung Lee6Raies A. Mir7Raies A. Mir8Lin Teng9Lin Teng10Amber Ginn11Amber Ginn12Choonghee Lee13Choonghee Lee14Maria Ukhanova15Sebastian Galindo16Chad Carr17Nicolas DiLorenzo18Soohyoun Ahn19Jae-Hyung Mah20Jae-Hyung Mah21Hae-Yeong Kim22Volker Mai23Volker Mai24Ray Mobley25J. Glenn Morris26J. Glenn Morris27KwangCheol Casey Jeong28KwangCheol Casey Jeong29KwangCheol Casey Jeong30Department of Animal Sciences, University of Florida, Gainesville, FL, United StatesEmerging Pathogens Institute, University of Florida, Gainesville, FL, United StatesHerbert Wertheim College of Medicine, Florida International University, Miami, FL, United StatesDepartment of Animal Sciences, University of Florida, Gainesville, FL, United StatesEmerging Pathogens Institute, University of Florida, Gainesville, FL, United StatesDepartment of Animal Sciences, University of Florida, Gainesville, FL, United StatesEmerging Pathogens Institute, University of Florida, Gainesville, FL, United StatesDepartment of Animal Sciences, University of Florida, Gainesville, FL, United StatesEmerging Pathogens Institute, University of Florida, Gainesville, FL, United StatesDepartment of Animal Sciences, University of Florida, Gainesville, FL, United StatesEmerging Pathogens Institute, University of Florida, Gainesville, FL, United StatesDepartment of Animal Sciences, University of Florida, Gainesville, FL, United StatesEmerging Pathogens Institute, University of Florida, Gainesville, FL, United StatesDepartment of Animal Sciences, University of Florida, Gainesville, FL, United StatesEmerging Pathogens Institute, University of Florida, Gainesville, FL, United StatesEmerging Pathogens Institute, University of Florida, Gainesville, FL, United StatesDepartment of Agricultural Education and Communication, University of Florida, Gainesville, FL, United StatesDepartment of Animal Sciences, University of Florida, Gainesville, FL, United StatesNorth Florida Research and Education Center, University of Florida, Marianna, FL, United StatesDepartment of Food Science and Human Nutrition, University of Florida, Gainesville, FL, United StatesDepartment of Animal Sciences, University of Florida, Gainesville, FL, United StatesDepartment of Food and Biotechnology, Korea University, Sejong, South KoreaInstitute of Life Sciences and Resources and Department of Food Science and Biotechnology, Kyung Hee University, Yongin, South KoreaEmerging Pathogens Institute, University of Florida, Gainesville, FL, United StatesDepartment of Epidemiology, College of Public Health and Health Professions and College of Medicine, University of Florida, Gainesville, FL, United States0Department of Animal Science, Florida Agricultural and Mechanical University, Tallahassee, FL, United StatesEmerging Pathogens Institute, University of Florida, Gainesville, FL, United States1Department of Medicine, College of Medicine, University of Florida, Gainesville, FL, United StatesDepartment of Animal Sciences, University of Florida, Gainesville, FL, United StatesEmerging Pathogens Institute, University of Florida, Gainesville, FL, United StatesInstitute of Life Sciences and Resources and Department of Food Science and Biotechnology, Kyung Hee University, Yongin, South KoreaAlthough the over-use of antibiotics during food animal production is a potential driver of antimicrobial resistant microorganisms (ARMs), a high prevalence of cefotaxime resistant bacteria (CRB) has been observed in grazing animals raised without antibiotic supplementation. In this cross-sectional study, the prevalence and concentration of CRB in beef cattle on grazing farms were investigated. Fecal samples from the recto-anal junction of cattle (n = 840) and environmental samples (n = 258) were collected from 17 farms in North and Central Florida in the United States, and a survey of farm characteristics, animal husbandry practices, and antibiotic usage was conducted. CRB were detected in fecal samples from 47.4% of all cattle, with the prevalence ranging from 21.1 to 87.5% on farms, and significantly higher (P < 0.001) in calves compared to adult cows (54.1 vs. 41.8%). Environmental samples had a higher prevalence than fecal samples (P < 0.001), with CRB detected in 88.6% of water, 98.7% of soil, and 95.7% of forage samples. Compared to the concentration (log CFU/g) of CRB in fecal samples (2.95, 95% CI: 2.89, 3.02), the concentration of CRB was higher (P < 0.001) in soil and forage samples (5.37, 95% CI: 5.16, 5.57) and lower (P < 0.001) in water samples (1.08, 95% CI: 0.82, 1.36). Soil microbiota from farms with high prevalence of CRB clustered closer together and the proportion of Phylum Proteobacteria was higher on farms with high prevalence of CRB resistance. Large farming operations were associated with a 58% higher likelihood of CRB detection in fecal samples. Regular cleaning of drinking troughs and the addition of ionophores to feed were associated with CRB reduction in fecal samples. Taken together, the widespread of CRB into both cattle seldom treated with cephalosporin antibiotics and the surrounding environment suggests the environment is a natural source of antimicrobial resistance in beef cattle.https://www.frontiersin.org/article/10.3389/fmicb.2019.00176/fullcefotaximeantibiotic resistancebeef cattlecross sectional studyfarm management survey