Emergence of methicillin resistance predates the clinical use of antibiotics
Jesper Larsen (),
Claire L. Raisen,
Xiaoliang Ba,
Nicholas J. Sadgrove,
Guillermo F. Padilla-González,
Monique S. J. Simmonds,
Igor Loncaric,
Heidrun Kerschner,
Petra Apfalter,
Rainer Hartl,
Ariane Deplano,
Stien Vandendriessche,
Barbora Černá Bolfíková,
Pavel Hulva,
Maiken C. Arendrup,
Rasmus K. Hare,
Céline Barnadas,
Marc Stegger,
Raphael N. Sieber,
Robert L. Skov,
Andreas Petersen,
Øystein Angen,
Sophie L. Rasmussen,
Carmen Espinosa-Gongora,
Frank M. Aarestrup,
Laura J. Lindholm,
Suvi M. Nykäsenoja,
Frederic Laurent,
Karsten Becker,
Birgit Walther,
Corinna Kehrenberg,
Christiane Cuny,
Franziska Layer,
Guido Werner,
Wolfgang Witte,
Ivonne Stamm,
Paolo Moroni,
Hannah J. Jørgensen,
Hermínia Lencastre,
Emilia Cercenado,
Fernando García-Garrote,
Stefan Börjesson,
Sara Hæggman,
Vincent Perreten,
Christopher J. Teale,
Andrew S. Waller,
Bruno Pichon,
Martin D. Curran,
Matthew J. Ellington,
John J. Welch,
Sharon J. Peacock,
David J. Seilly,
Fiona J. E. Morgan,
Julian Parkhill,
Nazreen F. Hadjirin,
Jodi A. Lindsay,
Matthew T. G. Holden,
Giles F. Edwards,
Geoffrey Foster,
Gavin K. Paterson,
Xavier Didelot,
Mark A. Holmes,
Ewan M. Harrison and
Anders R. Larsen
Additional contact information
Jesper Larsen: Statens Serum Institut
Claire L. Raisen: University of Cambridge
Xiaoliang Ba: University of Cambridge
Nicholas J. Sadgrove: Royal Botanic Gardens, Kew
Guillermo F. Padilla-González: Royal Botanic Gardens, Kew
Monique S. J. Simmonds: Royal Botanic Gardens, Kew
Igor Loncaric: University of Veterinary Medicine
Heidrun Kerschner: Institute for Hygiene, Microbiology and Tropical Medicine, Ordensklinikum Linz Elisabethinen
Petra Apfalter: Institute for Hygiene, Microbiology and Tropical Medicine, Ordensklinikum Linz Elisabethinen
Rainer Hartl: Institute for Hygiene, Microbiology and Tropical Medicine, Ordensklinikum Linz Elisabethinen
Ariane Deplano: Hôpital Erasme, Université libre de Bruxelles
Stien Vandendriessche: Hôpital Erasme, Université libre de Bruxelles
Barbora Černá Bolfíková: Czech University of Life Sciences Prague
Pavel Hulva: Charles University
Maiken C. Arendrup: Statens Serum Institut
Rasmus K. Hare: Statens Serum Institut
Céline Barnadas: Statens Serum Institut
Marc Stegger: Statens Serum Institut
Raphael N. Sieber: Statens Serum Institut
Robert L. Skov: Statens Serum Institut
Andreas Petersen: Statens Serum Institut
Øystein Angen: Statens Serum Institut
Sophie L. Rasmussen: Aalborg University
Carmen Espinosa-Gongora: University of Copenhagen
Frank M. Aarestrup: Technical University of Denmark
Laura J. Lindholm: Finnish Institute for Health and Welfare
Suvi M. Nykäsenoja: Finnish Food Authority
Frederic Laurent: Hospices Civils de Lyon, University of Lyon
Karsten Becker: University Medicine Greifswald
Birgit Walther: Freie Universität Berlin
Corinna Kehrenberg: Justus-Liebig University Giessen
Christiane Cuny: Robert Koch Institute
Franziska Layer: Robert Koch Institute
Guido Werner: Robert Koch Institute
Wolfgang Witte: Robert Koch Institute
Ivonne Stamm: Vet Med Labor GmbH
Paolo Moroni: Università degli Studi di Milano
Hannah J. Jørgensen: Norwegian Veterinary Institute
Hermínia Lencastre: ITQB NOVA
Emilia Cercenado: Hospital Universitario Lucus Augusti
Fernando García-Garrote: Hospital Universitario Lucus Augusti
Stefan Börjesson: National Veterinary Institute (SVA)
Sara Hæggman: Public Health Agency of Sweden
Vincent Perreten: University of Bern
Christopher J. Teale: Animal and Plant Health Agency
Andrew S. Waller: Animal Health Trust
Bruno Pichon: UK Health Security Agency
Martin D. Curran: Addenbrooke’s Hospital
Matthew J. Ellington: Addenbrooke’s Hospital
John J. Welch: University of Cambridge
Sharon J. Peacock: University of Cambridge
David J. Seilly: University of Cambridge
Fiona J. E. Morgan: University of Cambridge
Julian Parkhill: University of Cambridge
Nazreen F. Hadjirin: University of Cambridge
Jodi A. Lindsay: St George’s, University of London
Matthew T. G. Holden: University of St Andrews
Giles F. Edwards: Stobhill Hospital
Geoffrey Foster: SRUC Veterinary Services
Gavin K. Paterson: University of Edinburgh
Xavier Didelot: University of Warwick
Mark A. Holmes: University of Cambridge
Ewan M. Harrison: University of Cambridge
Anders R. Larsen: Statens Serum Institut
Nature, 2022, vol. 602, issue 7895, 135-141
Abstract:
Abstract The discovery of antibiotics more than 80 years ago has led to considerable improvements in human and animal health. Although antibiotic resistance in environmental bacteria is ancient, resistance in human pathogens is thought to be a modern phenomenon that is driven by the clinical use of antibiotics1. Here we show that particular lineages of methicillin-resistant Staphylococcus aureus—a notorious human pathogen—appeared in European hedgehogs in the pre-antibiotic era. Subsequently, these lineages spread within the local hedgehog populations and between hedgehogs and secondary hosts, including livestock and humans. We also demonstrate that the hedgehog dermatophyte Trichophyton erinacei produces two β-lactam antibiotics that provide a natural selective environment in which methicillin-resistant S. aureus isolates have an advantage over susceptible isolates. Together, these results suggest that methicillin resistance emerged in the pre-antibiotic era as a co-evolutionary adaptation of S. aureus to the colonization of dermatophyte-infected hedgehogs. The evolution of clinically relevant antibiotic-resistance genes in wild animals and the connectivity of natural, agricultural and human ecosystems demonstrate that the use of a One Health approach is critical for our understanding and management of antibiotic resistance, which is one of the biggest threats to global health, food security and development.
Date: 2022
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DOI: 10.1038/s41586-021-04265-w
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