A shared population of epidemic methicillin-resistant Staphylococcus aureus 15 circulates in humans and companion animals.
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.


OBJECTIVE
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.
Department of Veterinary Medicine, University of Cambridge, Cambridge, United Kingdom.
Ewan M
EM
Harrison
Department of Veterinary Medicine, University of Cambridge, Cambridge, United Kingdom.
Lucy A
LA
Weinert
Wellcome Trust Sanger Institute, Hinxton, United Kingdom.
Matthew T G
MT
Holden
Department of Genetics, University of Cambridge, Cambridge, United Kingdom.
John J
JJ
Welch
Department of Veterinary Medicine, University of Cambridge, Cambridge, United Kingdom.
Katherine
K
Wilson
Department of Veterinary Medicine, University of Cambridge, Cambridge, United Kingdom.
Fiona J E
FJ
Morgan
Wellcome Trust Sanger Institute, Hinxton, United Kingdom.
Simon R
SR
Harris
Royal Veterinary College, University of London, North Mymms, Hertfordshire, England.
Anette
A
Loeffler
Royal Veterinary College, University of London, North Mymms, Hertfordshire, England.
Amanda K
AK
Boag
Sharon J
SJ
Peacock
School of Biological, Biomedical and Environmental Sciences, University of Hull, Hull, United Kingdom.
Gavin K
GK
Paterson
Centre for Preventive Medicine, Animal Health Trust, Kentford, Newmarket, Suffolk, United Kingdom.
Andrew S
AS
Waller
Wellcome Trust Sanger Institute, Hinxton, United Kingdom.
Julian
http://orcid.org/0000-0002-7069-5958
J
Parkhill
Department of Veterinary Medicine, University of Cambridge, Cambridge, United Kingdom mah1@cam.ac.uk.
Mark A
MA
Holmes
D000220:Adaptation, Biological; D000820:Animal Diseases / Q000453:epidemiology* / Q000382:microbiology*; D000818:Animals; D024881:Drug Resistance, Bacterial / Q000235:genetics; D019143:Evolution, Molecular; D016680:Genome, Bacterial; D055106:Genome-Wide Association Study; D006801:Humans; D055624:Methicillin-Resistant Staphylococcus aureus / Q000145:classification* / Q000235:genetics / Q000302:isolation & purification; D058885:Multilocus Sequence Typing; D010802:Phylogeny; D020641:Polymorphism, Single Nucleotide; D013203:Staphylococcal Infections / Q000453:epidemiology*; D037521:Virulence Factors / Q000235:genetics
D037521:Virulence Factors