Risk Factors for Antimicrobial Resistance in Turkey Farms: A Cross-Sectional Study in Three European Countries
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
Affiliations
Mayu Horie
Institute for Risk Assessment Sciences, Utrecht University, Yalelaan 2, 3584 CM Utrecht, The Netherlands
Dongsheng Yang
Institute for Risk Assessment Sciences, Utrecht University, Yalelaan 2, 3584 CM Utrecht, The Netherlands
Philip Joosten
Veterinary Epidemiology Unit, Department of Obstetrics, Reproduction and Herd Health, Faculty of Veterinary Medicine, Ghent University, Salisburylaan 133, 9820 Merelbeke, Belgium
Patrick Munk
Research Group for Genomic Epidemiology, The National Food Institute, Technical University of Denmark, Kemitorvet, 2800 Kgs. Lyngby, Denmark
Katharina Wadepohl
Field Station for Epidemiology, University of Veterinary Medicine Hannover, Büscheler Straße 9, 49456 Bakum, Germany
Claire Chauvin
Epidemiology, Health and Welfare Unit, The French Agency for Food, Environmental and Occupational Health & Safety (ANSES), 22440 Ploufragan, France
Gabriel Moyano
Antimicrobial Resistance Unit (ARU), Animal Health Departement, Faculty of Veterinary Medicine and VISAVET Health Surveillance Centre, Complutense University of Madrid, 28040 Madrid, Spain
Magdalena Skarżyńska
Department of Microbiology, National Veterinary Research Institute (PIWet), Partyzantów Avenue 57, 24-100 Puławy, Poland
Jeroen Dewulf
Veterinary Epidemiology Unit, Department of Obstetrics, Reproduction and Herd Health, Faculty of Veterinary Medicine, Ghent University, Salisburylaan 133, 9820 Merelbeke, Belgium
Frank M. Aarestrup
Research Group for Genomic Epidemiology, The National Food Institute, Technical University of Denmark, Kemitorvet, 2800 Kgs. Lyngby, Denmark
Thomas Blaha
Field Station for Epidemiology, University of Veterinary Medicine Hannover, Büscheler Straße 9, 49456 Bakum, Germany
Pascal Sanders
Epidemiology, Health and Welfare Unit, The French Agency for Food, Environmental and Occupational Health & Safety (ANSES), 22440 Ploufragan, France
Bruno Gonzalez-Zorn
Antimicrobial Resistance Unit (ARU), Animal Health Departement, Faculty of Veterinary Medicine and VISAVET Health Surveillance Centre, Complutense University of Madrid, 28040 Madrid, Spain
Dariusz Wasyl
Department of Microbiology, National Veterinary Research Institute (PIWet), Partyzantów Avenue 57, 24-100 Puławy, Poland
Jaap A. Wagenaar
Department of Infectious Diseases and Immunology, Faculty of Veterinary Medicine, Utrecht University, Yalelaan 1, 3584 CL Utrecht, The Netherlands
Dick Heederik
Institute for Risk Assessment Sciences, Utrecht University, Yalelaan 2, 3584 CM Utrecht, The Netherlands
Dik Mevius
Department of Infectious Diseases and Immunology, Faculty of Veterinary Medicine, Utrecht University, Yalelaan 1, 3584 CL Utrecht, The Netherlands
Heike Schmitt
Institute for Risk Assessment Sciences, Utrecht University, Yalelaan 2, 3584 CM Utrecht, The Netherlands
Lidwien A. M. Smit
Institute for Risk Assessment Sciences, Utrecht University, Yalelaan 2, 3584 CM Utrecht, The Netherlands
Liese Van Gompel
Institute for Risk Assessment Sciences, Utrecht University, Yalelaan 2, 3584 CM Utrecht, The Netherlands
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 (n = 60), (ii) quantitative real-time polymerase chain reaction (qPCR) targeting ermB, tetW, sul2, and aph3′-III; (n = 304), and (iii) by identifying the phenotypic prevalence of AMR in Escherichia coli isolates by minimum inhibitory concentrations (MIC) (n = 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.