title: A Livestock-Associated, Multidrug-Resistant, Methicillin-Resistant Staphylococcus aureus Clonal Complex 97 Lineage Spreading in Dairy Cattle and Pigs in Italy.
abstract: Pandemic methicillin-resistant Staphylococcus aureus (MRSA) clonal complex 97 (CC97) lineages originated from livestock-to-human host jumps. In recent years, CC97 has become one of the major MRSA lineages detected in Italian farmed animals. The aim of this study was to characterize and analyze differences in MRSA and methicillin-susceptible S. aureus (MSSA) mainly of swine and bovine origins. Forty-seven CC97 isolates, 35 MRSA isolates, and 6 MSSA isolates from different Italian pig and cattle holdings; 5 pig MRSA isolates from Germany; and 1 human MSSA isolate from Spain were characterized by macrorestriction pulsed-field gel electrophoresis (PFGE) analysis, multilocus sequence typing (MLST), spa typing, staphylococcal cassette chromosome mec (SCCmec) typing, and antimicrobial resistance pattern analysis. Virulence and resistance genes were investigated by PCR and microarray analysis. Most of the isolates were of SCCmec type V (SCCmec V), except for two German MRSA isolates (SCCmec III). Five main clusters were identified by PFGE, with the German isolates (clusters I and II) showing 60.5% similarity with the Italian isolates, most of which (68.1%) grouped into cluster V. All CC97 isolates were Panton-Valentine leukocidin (PVL) negative, and a few (n = 7) tested positive for sak or scn. All MRSA isolates were multidrug resistant (MDR), and the main features were erm(B)- or erm(C)-mediated (n = 18) macrolide-lincosamide-streptogramin B resistance, vga(A)-mediated (n = 37) pleuromutilin resistance, fluoroquinolone resistance (n = 33), tet(K) in 32/37 tet(M)-positive isolates, and blaZ in almost all MRSA isolates. Few host-associated differences were detected among CC97 MRSA isolates: their extensive MDR nature in both pigs and dairy cattle may be a consequence of a spillback from pigs of a MRSA lineage that originated in cattle as MSSA and needs further investigation. Measures should be implemented at the farm level to prevent spillover to humans in intensive farming areas.
authors.affiliation: Istituto Zooprofilattico Sperimentale del Lazio e della Toscana M. Aleandri, Diagnostic Department, Rome, Italy.
authors.forename: Fabiola
authors.initials: F
authors.lastname: Feltrin
authors.affiliation: Istituto Zooprofilattico Sperimentale del Lazio e della Toscana M. Aleandri, Diagnostic Department, Rome, Italy.
authors.forename: Patricia
authors.initials: P
authors.lastname: Alba
authors.affiliation: Federal Institute for Risk Assessment (BfR), Berlin, Germany.
authors.forename: Britta
authors.initials: B
authors.lastname: Kraushaar
authors.affiliation: Istituto Zooprofilattico Sperimentale del Lazio e della Toscana M. Aleandri, Diagnostic Department, Rome, Italy.
authors.forename: Angela
authors.initials: A
authors.lastname: Ianzano
authors.affiliation: Veterinary and Agrochemical Research Centre (VAR-CODA-CERVA), Brussels, Belgium National Reference Centre-Staphylococcus aureus, Department of Microbiology, Hôpital Erasme, Université Libre de Bruxelles, Brussels, Belgium.
authors.forename: María Angeles
authors.initials: MA
authors.lastname: Argudín
authors.affiliation: Istituto Zooprofilattico Sperimentale del Lazio e della Toscana M. Aleandri, Diagnostic Department, Rome, Italy.
authors.forename: Paola
authors.initials: P
authors.lastname: Di Matteo
authors.affiliation: VISAVET Health Surveillance Centre, Universidad Complutense Madrid, Madrid, Spain.
authors.forename: María Concepción
authors.initials: MC
authors.lastname: Porrero
authors.affiliation: National Food Institute, Technical University of Denmark, Kongens Lyngby, Denmark.
authors.forename: Frank M
authors.initials: FM
authors.lastname: Aarestrup
authors.affiliation: Veterinary and Agrochemical Research Centre (VAR-CODA-CERVA), Brussels, Belgium Ross University School of Veterinary Medicine, Department of Biosciences, Basseterre, St. Kitts and Nevis, West Indies Ghent University, Faculty of Veterinary Medicine, Department of Pathology, Bacteriology and Poultry Diseases, Merelbeke, Belgium.
authors.forename: Patrick
authors.initials: P
authors.lastname: Butaye
authors.affiliation: Istituto Zooprofilattico Sperimentale del Lazio e della Toscana M. Aleandri, Diagnostic Department, Rome, Italy.
authors.forename: Alessia
authors.initials: A
authors.lastname: Franco
authors.affiliation: Istituto Zooprofilattico Sperimentale del Lazio e della Toscana M. Aleandri, Diagnostic Department, Rome, Italy antonio.battisti@izslt.it.
authors.forename: Antonio
authors.initials: A
authors.lastname: Battisti
mesh_terms: D000818:Animals; D001427:Bacterial Toxins; D015373:Bacterial Typing Techniques; D002417:Cattle; D002418:Cattle Diseases / Q000382:microbiology*; D024881:Drug Resistance, Bacterial / Q000235:genetics*; D016521:Electrophoresis, Gel, Pulsed-Field; D005098:Exotoxins; D005838:Genotype; D005858:Germany; D006801:Humans; D007558:Italy / Q000453:epidemiology; D007956:Leukocidins; D058751:Livestock / Q000382:microbiology; D055624:Methicillin-Resistant Staphylococcus aureus / Q000235:genetics* / Q000302:isolation & purification* / Q000472:pathogenicity; D046228:Microarray Analysis; D008826:Microbial Sensitivity Tests; D058885:Multilocus Sequence Typing; D013030:Spain; D013203:Staphylococcal Infections / Q000382:microbiology / Q000517:prevention & control / Q000635:transmission / Q000662:veterinary*; D013211:Staphylococcus aureus / Q000187:drug effects / Q000235:genetics / Q000302:isolation & purification / Q000472:pathogenicity; D013552:Swine; D013553:Swine Diseases / Q000382:microbiology*; D014774:Virulence / Q000235:genetics
chemical_list: D001427:Bacterial Toxins; D005098:Exotoxins; D007956:Leukocidins; C078284:Panton-Valentine leukocidin