Risk Factors for Antimicrobial Resistance in Turkey Farms: A Cross-Sectional Study in Three European Countries

Food-producing animals are an important reservoir and potential source of transmission of antimicrobial resistance (AMR) to humans. However, research on AMR in turkey farms is limited. This study aimed to identify risk factors for AMR in turkey farms in three European countries (Germany, France, and...

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Main Authors: Mayu Horie, Dongsheng Yang, Philip Joosten, Patrick Munk, Katharina Wadepohl, Claire Chauvin, Gabriel Moyano, Magdalena Skarżyńska, Jeroen Dewulf, Frank M. Aarestrup, Thomas Blaha, Pascal Sanders, Bruno Gonzalez-Zorn, Dariusz Wasyl, Jaap A. Wagenaar, Dick Heederik, Dik Mevius, Heike Schmitt, Lidwien A. M. Smit, Liese Van Gompel
Format: Article
Language:English
Published: MDPI AG 2021-07-01
Series:Antibiotics
Subjects:
Online Access:https://www.mdpi.com/2079-6382/10/7/820
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language English
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author Mayu Horie
Dongsheng Yang
Philip Joosten
Patrick Munk
Katharina Wadepohl
Claire Chauvin
Gabriel Moyano
Magdalena Skarżyńska
Jeroen Dewulf
Frank M. Aarestrup
Thomas Blaha
Pascal Sanders
Bruno Gonzalez-Zorn
Dariusz Wasyl
Jaap A. Wagenaar
Dick Heederik
Dik Mevius
Heike Schmitt
Lidwien A. M. Smit
Liese Van Gompel
spellingShingle Mayu Horie
Dongsheng Yang
Philip Joosten
Patrick Munk
Katharina Wadepohl
Claire Chauvin
Gabriel Moyano
Magdalena Skarżyńska
Jeroen Dewulf
Frank M. Aarestrup
Thomas Blaha
Pascal Sanders
Bruno Gonzalez-Zorn
Dariusz Wasyl
Jaap A. Wagenaar
Dick Heederik
Dik Mevius
Heike Schmitt
Lidwien A. M. Smit
Liese Van Gompel
Risk Factors for Antimicrobial Resistance in Turkey Farms: A Cross-Sectional Study in Three European Countries
Antibiotics
antimicrobial use
antimicrobial resistance
turkeys
poultry
farm
antimicrobial resistance genes
author_facet Mayu Horie
Dongsheng Yang
Philip Joosten
Patrick Munk
Katharina Wadepohl
Claire Chauvin
Gabriel Moyano
Magdalena Skarżyńska
Jeroen Dewulf
Frank M. Aarestrup
Thomas Blaha
Pascal Sanders
Bruno Gonzalez-Zorn
Dariusz Wasyl
Jaap A. Wagenaar
Dick Heederik
Dik Mevius
Heike Schmitt
Lidwien A. M. Smit
Liese Van Gompel
author_sort Mayu Horie
title Risk Factors for Antimicrobial Resistance in Turkey Farms: A Cross-Sectional Study in Three European Countries
title_short Risk Factors for Antimicrobial Resistance in Turkey Farms: A Cross-Sectional Study in Three European Countries
title_full Risk Factors for Antimicrobial Resistance in Turkey Farms: A Cross-Sectional Study in Three European Countries
title_fullStr Risk Factors for Antimicrobial Resistance in Turkey Farms: A Cross-Sectional Study in Three European Countries
title_full_unstemmed Risk Factors for Antimicrobial Resistance in Turkey Farms: A Cross-Sectional Study in Three European Countries
title_sort risk factors for antimicrobial resistance in turkey farms: a cross-sectional study in three european countries
publisher MDPI AG
series Antibiotics
issn 2079-6382
publishDate 2021-07-01
description Food-producing animals are an important reservoir and potential source of transmission of antimicrobial resistance (AMR) to humans. However, research on AMR in turkey farms is limited. This study aimed to identify risk factors for AMR in turkey farms in three European countries (Germany, France, and Spain). Between 2014 and 2016, faecal samples, antimicrobial usage (AMU), and biosecurity information were collected from 60 farms. The level of AMR in faecal samples was quantified in three ways: By measuring the abundance of AMR genes through (i) shotgun metagenomics sequencing (<i>n</i> = 60), (ii) quantitative real-time polymerase chain reaction (qPCR) targeting <i>ermB</i>, <i>tetW</i>, <i>sul2</i>, and <i>aph3′-III</i>; (<i>n</i> = 304), and (iii) by identifying the phenotypic prevalence of AMR in <i>Escherichia coli</i> isolates by minimum inhibitory concentrations (MIC) (<i>n</i> = 600). The association between AMU or biosecurity and AMR was explored. Significant positive associations were detected between AMU and both genotypic and phenotypic AMR for specific antimicrobial classes. Beta-lactam and colistin resistance (metagenomics sequencing); ampicillin and ciprofloxacin resistance (MIC) were associated with AMU. However, no robust AMU-AMR association was detected by analyzing qPCR targets. In addition, no evidence was found that lower biosecurity increases AMR abundance. Using multiple complementary AMR detection methods added insights into AMU-AMR associations at turkey farms.
topic antimicrobial use
antimicrobial resistance
turkeys
poultry
farm
antimicrobial resistance genes
url https://www.mdpi.com/2079-6382/10/7/820
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spelling doaj-f3387eb0391b498eb338bc7d628e3a1e2021-07-23T13:28:10ZengMDPI AGAntibiotics2079-63822021-07-011082082010.3390/antibiotics10070820Risk Factors for Antimicrobial Resistance in Turkey Farms: A Cross-Sectional Study in Three European CountriesMayu Horie0Dongsheng Yang1Philip Joosten2Patrick Munk3Katharina Wadepohl4Claire Chauvin5Gabriel Moyano6Magdalena Skarżyńska7Jeroen Dewulf8Frank M. Aarestrup9Thomas Blaha10Pascal Sanders11Bruno Gonzalez-Zorn12Dariusz Wasyl13Jaap A. Wagenaar14Dick Heederik15Dik Mevius16Heike Schmitt17Lidwien A. M. Smit18Liese Van Gompel19Institute for Risk Assessment Sciences, Utrecht University, Yalelaan 2, 3584 CM Utrecht, The NetherlandsInstitute for Risk Assessment Sciences, Utrecht University, Yalelaan 2, 3584 CM Utrecht, The NetherlandsVeterinary Epidemiology Unit, Department of Obstetrics, Reproduction and Herd Health, Faculty of Veterinary Medicine, Ghent University, Salisburylaan 133, 9820 Merelbeke, BelgiumResearch Group for Genomic Epidemiology, The National Food Institute, Technical University of Denmark, Kemitorvet, 2800 Kgs. Lyngby, DenmarkField Station for Epidemiology, University of Veterinary Medicine Hannover, Büscheler Straße 9, 49456 Bakum, GermanyEpidemiology, Health and Welfare Unit, The French Agency for Food, Environmental and Occupational Health & Safety (ANSES), 22440 Ploufragan, FranceAntimicrobial Resistance Unit (ARU), Animal Health Departement, Faculty of Veterinary Medicine and VISAVET Health Surveillance Centre, Complutense University of Madrid, 28040 Madrid, SpainDepartment of Microbiology, National Veterinary Research Institute (PIWet), Partyzantów Avenue 57, 24-100 Puławy, PolandVeterinary Epidemiology Unit, Department of Obstetrics, Reproduction and Herd Health, Faculty of Veterinary Medicine, Ghent University, Salisburylaan 133, 9820 Merelbeke, BelgiumResearch Group for Genomic Epidemiology, The National Food Institute, Technical University of Denmark, Kemitorvet, 2800 Kgs. Lyngby, DenmarkField Station for Epidemiology, University of Veterinary Medicine Hannover, Büscheler Straße 9, 49456 Bakum, GermanyEpidemiology, Health and Welfare Unit, The French Agency for Food, Environmental and Occupational Health & Safety (ANSES), 22440 Ploufragan, FranceAntimicrobial Resistance Unit (ARU), Animal Health Departement, Faculty of Veterinary Medicine and VISAVET Health Surveillance Centre, Complutense University of Madrid, 28040 Madrid, SpainDepartment of Microbiology, National Veterinary Research Institute (PIWet), Partyzantów Avenue 57, 24-100 Puławy, PolandDepartment of Infectious Diseases and Immunology, Faculty of Veterinary Medicine, Utrecht University, Yalelaan 1, 3584 CL Utrecht, The NetherlandsInstitute for Risk Assessment Sciences, Utrecht University, Yalelaan 2, 3584 CM Utrecht, The NetherlandsDepartment of Infectious Diseases and Immunology, Faculty of Veterinary Medicine, Utrecht University, Yalelaan 1, 3584 CL Utrecht, The NetherlandsInstitute for Risk Assessment Sciences, Utrecht University, Yalelaan 2, 3584 CM Utrecht, The NetherlandsInstitute for Risk Assessment Sciences, Utrecht University, Yalelaan 2, 3584 CM Utrecht, The NetherlandsInstitute for Risk Assessment Sciences, Utrecht University, Yalelaan 2, 3584 CM Utrecht, The NetherlandsFood-producing animals are an important reservoir and potential source of transmission of antimicrobial resistance (AMR) to humans. However, research on AMR in turkey farms is limited. This study aimed to identify risk factors for AMR in turkey farms in three European countries (Germany, France, and Spain). Between 2014 and 2016, faecal samples, antimicrobial usage (AMU), and biosecurity information were collected from 60 farms. The level of AMR in faecal samples was quantified in three ways: By measuring the abundance of AMR genes through (i) shotgun metagenomics sequencing (<i>n</i> = 60), (ii) quantitative real-time polymerase chain reaction (qPCR) targeting <i>ermB</i>, <i>tetW</i>, <i>sul2</i>, and <i>aph3′-III</i>; (<i>n</i> = 304), and (iii) by identifying the phenotypic prevalence of AMR in <i>Escherichia coli</i> isolates by minimum inhibitory concentrations (MIC) (<i>n</i> = 600). The association between AMU or biosecurity and AMR was explored. Significant positive associations were detected between AMU and both genotypic and phenotypic AMR for specific antimicrobial classes. Beta-lactam and colistin resistance (metagenomics sequencing); ampicillin and ciprofloxacin resistance (MIC) were associated with AMU. However, no robust AMU-AMR association was detected by analyzing qPCR targets. In addition, no evidence was found that lower biosecurity increases AMR abundance. Using multiple complementary AMR detection methods added insights into AMU-AMR associations at turkey farms.https://www.mdpi.com/2079-6382/10/7/820antimicrobial useantimicrobial resistanceturkeyspoultryfarmantimicrobial resistance genes