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      Staphylococcus aureus CC398: Host Adaptation and Emergence of Methicillin Resistance in Livestock


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          Since its discovery in the early 2000s, methicillin-resistant Staphylococcus aureus (MRSA) clonal complex 398 (CC398) has become a rapidly emerging cause of human infections, most often associated with livestock exposure. We applied whole-genome sequence typing to characterize a diverse collection of CC398 isolates ( n = 89), including MRSA and methicillin-susceptible Saureus (MSSA) from animals and humans spanning 19 countries and four continents. We identified 4,238 single nucleotide polymorphisms (SNPs) among the 89 core genomes. Minimal homoplasy (consistency index = 0.9591) was detected among parsimony-informative SNPs, allowing for the generation of a highly accurate phylogenetic reconstruction of the CC398 clonal lineage. Phylogenetic analyses revealed that MSSA from humans formed the most ancestral clades. The most derived lineages were composed predominantly of livestock-associated MRSA possessing three different staphylococcal cassette chromosome mec element (SCC mec) types (IV, V, and VII-like) including nine subtypes. The human-associated isolates from the basal clades carried phages encoding human innate immune modulators that were largely missing among the livestock-associated isolates. Our results strongly suggest that livestock-associated MRSA CC398 originated in humans as MSSA. The lineage appears to have undergone a rapid radiation in conjunction with the jump from humans to livestock, where it subsequently acquired tetracycline and methicillin resistance. Further analyses are required to estimate the number of independent genetic events leading to the methicillin-resistant sublineages, but the diversity of SCC mec subtypes is suggestive of strong and diverse antimicrobial selection associated with food animal production.


          Modern food animal production is characterized by densely concentrated animals and routine antibiotic use, which may facilitate the emergence of novel antibiotic-resistant zoonotic pathogens. Our findings strongly support the idea that livestock-associated MRSA CC398 originated as MSSA in humans. The jump of CC398 from humans to livestock was accompanied by the loss of phage-carried human virulence genes, which likely attenuated its zoonotic potential, but it was also accompanied by the acquisition of tetracycline and methicillin resistance. Our findings exemplify a bidirectional zoonotic exchange and underscore the potential public health risks of widespread antibiotic use in food animal production.

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          Most cited references18

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          Classification of staphylococcal cassette chromosome mec (SCCmec): guidelines for reporting novel SCCmec elements.

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            Recent human-to-poultry host jump, adaptation, and pandemic spread of Staphylococcus aureus.

            The impact of globalization on the emergence and spread of pathogens is an important veterinary and public health issue. Staphylococcus aureus is a notorious human pathogen associated with serious nosocomial and community-acquired infections. In addition, S. aureus is a major cause of animal diseases including skeletal infections of poultry, which are a large economic burden on the global broiler chicken industry. Here, we provide evidence that the majority of S. aureus isolates from broiler chickens are the descendants of a single human-to-poultry host jump that occurred approximately 38 years ago (range, 30 to 63 years ago) by a subtype of the worldwide human ST5 clonal lineage unique to Poland. In contrast to human subtypes of the ST5 radiation, which demonstrate strong geographic clustering, the poultry ST5 clade was distributed in different continents, consistent with wide dissemination via the global poultry industry distribution network. The poultry ST5 clade has undergone genetic diversification from its human progenitor strain by acquisition of novel mobile genetic elements from an avian-specific accessory gene pool, and by the inactivation of several proteins important for human disease pathogenesis. These genetic events have resulted in enhanced resistance to killing by chicken heterophils, reflecting avian host-adaptive evolution. Taken together, we have determined the evolutionary history of a major new animal pathogen that has undergone rapid avian host adaptation and intercontinental dissemination. These data provide a new paradigm for the impact of human activities on the emergence of animal pathogens.
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              Methicillin-Resistant Staphylococcus aureus (MRSA) Strain ST398 Is Present in Midwestern U.S. Swine and Swine Workers

              Background Recent research has demonstrated that many swine and swine farmers in the Netherlands and Canada are colonized with MRSA. However, no studies to date have investigated carriage of MRSA among swine and swine farmers in the United States (U.S.). Methods We sampled the nares of 299 swine and 20 workers from two different production systems in Iowa and Illinois, comprising approximately 87,000 live animals. MRSA isolates were typed by pulsed field gel electrophoresis (PFGE) using SmaI and EagI restriction enzymes, and by multi locus sequence typing (MLST). PCR was used to determine SCCmec type and presence of the pvl gene. Results In this pilot study, overall MRSA prevalence in swine was 49% (147/299) and 45% (9/20) in workers. The prevalence of MRSA carriage among production system A's swine varied by age, ranging from 36% (11/30) in adult swine to 100% (60/60) of animals aged 9 and 12 weeks. The prevalence among production system A's workers was 64% (9/14). MRSA was not isolated from production system B's swine or workers. Isolates examined were not typeable by PFGE when SmaI was used, but digestion with EagI revealed that the isolates were clonal and were not related to common human types in Iowa (USA100, USA300, and USA400). MLST documented that the isolates were ST398. Conclusions These results show that colonization of swine by MRSA was very common on one swine production system in the midwestern U.S., suggesting that agricultural animals could become an important reservoir for this bacterium. MRSA strain ST398 was the only strain documented on this farm. Further studies are examining carriage rates on additional farms.

                Author and article information

                American Society of Microbiology (1752 N St., N.W., Washington, DC )
                21 February 2012
                Jan-Feb 2012
                : 3
                : 1
                Translational Genomics Research Institute (TGen), Pathogen Genomics Division, Flagstaff, Arizona, USA [ a ];
                Department of Microbiological Surveillance and Research, Statens Serum Institut, Copenhagen, Denmark [ b ];
                National Food Institute, Technical University of Denmark, Lyngby, Denmark [ c ];
                Center for Microbial Genetics and Genomics, Northern Arizona University, Flagstaff, Arizona, USA [ d ];
                Österreichische Agentur für Gesundheit und Ernährungssicherheit GmbH, Bereich Humanmedizin, Institut für Medizinische Mikrobiologie und Hygiene, Graz, Austria [ e ];
                Veterinary Faculty, Institute of Microbiology and Parasitology, University of Ljubljana, Ljubljana, Slovenia [ f ];
                Istituto Zooprofilattico Sperimentale delle Regioni Lazio e Toscana, Rome, Italy [ g ];
                Department of Swine Diseases, National Veterinary Research Institute, Pulawy, Poland [ h ];
                Institute of Farm Animal Genetics, Friedrich-Loeffler-Institut, Neustadt-Mariensee, Germany [ i ];
                Department of Pathology, Bacteriology, and Poultry Diseases, Faculty of Veterinary Medicine, University of Ghent, Merelbeke, Belgium [ j ];
                Unit of General Bacteriology, Veterinary and Agrochemical Research Centre, Brussels, Belgium [ k ];
                Anses, Ploufragan Plouzané Laboratory, Ploufragan, France [ l ];
                Interdisciplinary Centre of Research in Animal Health, Faculty of Veterinary Medicine, Lisbon, Portugal [ m ];
                Centro de Vigilancia Sanitaria Veterinaria, Universidad Complutense de Madrid, Madrid, Spain [ n ];
                University Paris-Diderot and National Reference Center, Bacterial Resistance in the Commensal Flora, Hôpital Bichat-Claude Bernard, Paris, France [ o ];
                Center for Emerging Infectious Diseases, University of Iowa, Coralville, Iowa, USA [ p ];
                Department of Microbiology, University of Mississippi Medical Center, Jackson, Mississippi, USA [ q ];
                Ontario Veterinary College, University of Guelph, Guelph, Ontario, Canada [ r ];
                Department of Preventive Veterinary Medicine, San Marcos Major National University, Lima, Peru [ s ];
                Department of Laboratory Medicine, First Affiliated Hospital of Wenzhou Medical College, Wenzhou, China [ t ]; and
                Laboratory of Bacteriology, Hôpital de la Croix Rousse, National Reference Center for Staphylococci, Lyon, France [ u ]
                Author notes
                Address correspondence to Lance B. Price, lprice@ 123456tgen.org .

                Editor Fernando Baquero, Ramón y Cajal University Hospital

                Copyright © 2012 Price et al.

                This is an open-access article distributed under the terms of the Creative Commons Attribution-Noncommercial-Share Alike 3.0 Unported License, which permits unrestricted noncommercial use, distribution, and reproduction in any medium, provided the original author and source are credited.

                : 19 December 2011
                : 3 January 2012
                Page count
                Pages: 6
                Research Article
                Custom metadata
                January/February 2012

                Life sciences
                Life sciences


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