A Shared Population of Epidemic Methicillin-Resistant <named-content content-type="genus-species">Staphylococcus aureus</named-content> 15 Circulates in Humans and Companion Animals

ABSTRACT Methicillin-resistant Staphylococcus aureus (MRSA) is a global human health problem causing infections in both hospitals and the community. Companion animals, such as cats, dogs, and horses, are also frequently colonized by MRSA and can become infected. We sequenced the genomes of 46 multil...

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Autores principales: Ewan M. Harrison, Lucy A. Weinert, Matthew T. G. Holden, John J. Welch, Katherine Wilson, Fiona J. E. Morgan, Simon R. Harris, Anette Loeffler, Amanda K. Boag, Sharon J. Peacock, Gavin K. Paterson, Andrew S. Waller, Julian Parkhill, Mark A. Holmes
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Publicado: American Society for Microbiology 2014
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spelling oai:doaj.org-article:23eef690f87e4e0495719494f04dd7582021-11-15T15:47:38ZA Shared Population of Epidemic Methicillin-Resistant <named-content content-type="genus-species">Staphylococcus aureus</named-content> 15 Circulates in Humans and Companion Animals10.1128/mBio.00985-132150-7511https://doaj.org/article/23eef690f87e4e0495719494f04dd7582014-07-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.00985-13https://doaj.org/toc/2150-7511ABSTRACT Methicillin-resistant Staphylococcus aureus (MRSA) is a global human health problem causing infections in both hospitals and the community. Companion animals, such as cats, dogs, and horses, are also frequently colonized by MRSA and can become infected. We sequenced the genomes of 46 multilocus sequence type (ST) 22 MRSA isolates from cats and dogs in the United Kingdom and compared these to an extensive population framework of human isolates from the same lineage. Phylogenomic analyses showed that all companion animal isolates were interspersed throughout the epidemic MRSA-15 (EMRSA-15) pandemic clade and clustered with human isolates from the United Kingdom, with human isolates basal to those from companion animals, suggesting a human source for isolates infecting companion animals. A number of isolates from the same veterinary hospital clustered together, suggesting that as in human hospitals, EMRSA-15 isolates are readily transmitted in the veterinary hospital setting. Genome-wide association analysis did not identify any host-specific single nucleotide polymorphisms (SNPs) or virulence factors. However, isolates from companion animals were significantly less likely to harbor a plasmid encoding erythromycin resistance. When this plasmid was present in animal-associated isolates, it was more likely to contain mutations mediating resistance to clindamycin. This finding is consistent with the low levels of erythromycin and high levels of clindamycin used in veterinary medicine in the United Kingdom. This study furthers the “one health” view of infectious diseases that the pathogen pool of human and animal populations are intrinsically linked and provides evidence that antibiotic usage in animal medicine is shaping the population of a major human pathogen.IMPORTANCE Methicillin-resistant Staphylococcus aureus (MRSA) is major problem in human medicine. Companion animals, such as cats, dogs, and horses, can also become colonized and infected by MRSA. Here, we demonstrate that a shared population of an important and globally disseminated lineage of MRSA can infect both humans and companion animals without undergoing host adaptation. This suggests that companion animals might act as a reservoir for human infections. We also show that the isolates from companion animals have differences in the presence of certain antibiotic resistance genes. This study furthers the “one health” view of infectious diseases by demonstrating that the pool of MRSA isolates in the human and animal populations are shared and highlights how different antibiotic usage patterns between human and veterinary medicine can shape the population of bacterial pathogens.Ewan M. HarrisonLucy A. WeinertMatthew T. G. HoldenJohn J. WelchKatherine WilsonFiona J. E. MorganSimon R. HarrisAnette LoefflerAmanda K. BoagSharon J. PeacockGavin K. PatersonAndrew S. WallerJulian ParkhillMark A. HolmesAmerican Society for MicrobiologyarticleMicrobiologyQR1-502ENmBio, Vol 5, Iss 3 (2014)
institution DOAJ
collection DOAJ
language EN
topic Microbiology
QR1-502
spellingShingle Microbiology
QR1-502
Ewan M. Harrison
Lucy A. Weinert
Matthew T. G. Holden
John J. Welch
Katherine Wilson
Fiona J. E. Morgan
Simon R. Harris
Anette Loeffler
Amanda K. Boag
Sharon J. Peacock
Gavin K. Paterson
Andrew S. Waller
Julian Parkhill
Mark A. Holmes
A Shared Population of Epidemic Methicillin-Resistant <named-content content-type="genus-species">Staphylococcus aureus</named-content> 15 Circulates in Humans and Companion Animals
description ABSTRACT Methicillin-resistant Staphylococcus aureus (MRSA) is a global human health problem causing infections in both hospitals and the community. Companion animals, such as cats, dogs, and horses, are also frequently colonized by MRSA and can become infected. We sequenced the genomes of 46 multilocus sequence type (ST) 22 MRSA isolates from cats and dogs in the United Kingdom and compared these to an extensive population framework of human isolates from the same lineage. Phylogenomic analyses showed that all companion animal isolates were interspersed throughout the epidemic MRSA-15 (EMRSA-15) pandemic clade and clustered with human isolates from the United Kingdom, with human isolates basal to those from companion animals, suggesting a human source for isolates infecting companion animals. A number of isolates from the same veterinary hospital clustered together, suggesting that as in human hospitals, EMRSA-15 isolates are readily transmitted in the veterinary hospital setting. Genome-wide association analysis did not identify any host-specific single nucleotide polymorphisms (SNPs) or virulence factors. However, isolates from companion animals were significantly less likely to harbor a plasmid encoding erythromycin resistance. When this plasmid was present in animal-associated isolates, it was more likely to contain mutations mediating resistance to clindamycin. This finding is consistent with the low levels of erythromycin and high levels of clindamycin used in veterinary medicine in the United Kingdom. This study furthers the “one health” view of infectious diseases that the pathogen pool of human and animal populations are intrinsically linked and provides evidence that antibiotic usage in animal medicine is shaping the population of a major human pathogen.IMPORTANCE Methicillin-resistant Staphylococcus aureus (MRSA) is major problem in human medicine. Companion animals, such as cats, dogs, and horses, can also become colonized and infected by MRSA. Here, we demonstrate that a shared population of an important and globally disseminated lineage of MRSA can infect both humans and companion animals without undergoing host adaptation. This suggests that companion animals might act as a reservoir for human infections. We also show that the isolates from companion animals have differences in the presence of certain antibiotic resistance genes. This study furthers the “one health” view of infectious diseases by demonstrating that the pool of MRSA isolates in the human and animal populations are shared and highlights how different antibiotic usage patterns between human and veterinary medicine can shape the population of bacterial pathogens.
format article
author Ewan M. Harrison
Lucy A. Weinert
Matthew T. G. Holden
John J. Welch
Katherine Wilson
Fiona J. E. Morgan
Simon R. Harris
Anette Loeffler
Amanda K. Boag
Sharon J. Peacock
Gavin K. Paterson
Andrew S. Waller
Julian Parkhill
Mark A. Holmes
author_facet Ewan M. Harrison
Lucy A. Weinert
Matthew T. G. Holden
John J. Welch
Katherine Wilson
Fiona J. E. Morgan
Simon R. Harris
Anette Loeffler
Amanda K. Boag
Sharon J. Peacock
Gavin K. Paterson
Andrew S. Waller
Julian Parkhill
Mark A. Holmes
author_sort Ewan M. Harrison
title A Shared Population of Epidemic Methicillin-Resistant <named-content content-type="genus-species">Staphylococcus aureus</named-content> 15 Circulates in Humans and Companion Animals
title_short A Shared Population of Epidemic Methicillin-Resistant <named-content content-type="genus-species">Staphylococcus aureus</named-content> 15 Circulates in Humans and Companion Animals
title_full A Shared Population of Epidemic Methicillin-Resistant <named-content content-type="genus-species">Staphylococcus aureus</named-content> 15 Circulates in Humans and Companion Animals
title_fullStr A Shared Population of Epidemic Methicillin-Resistant <named-content content-type="genus-species">Staphylococcus aureus</named-content> 15 Circulates in Humans and Companion Animals
title_full_unstemmed A Shared Population of Epidemic Methicillin-Resistant <named-content content-type="genus-species">Staphylococcus aureus</named-content> 15 Circulates in Humans and Companion Animals
title_sort shared population of epidemic methicillin-resistant <named-content content-type="genus-species">staphylococcus aureus</named-content> 15 circulates in humans and companion animals
publisher American Society for Microbiology
publishDate 2014
url https://doaj.org/article/23eef690f87e4e0495719494f04dd758
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