Livestock-Associated Methicillin Resistant and Methicillin Susceptible Staphylococcus aureus Sequence Type (CC)1 in European Farmed Animals: High Genetic Relatedness of Isolates from Italian Cattle Herds and Humans.

Patricia Alba,Monica Monaco,Alessia Franco,María Concepción Porrero,Frank M Aarestrup,Gessica Cordaro,Suvi Nykäsenoja,María Angeles Argudín,Patrick Butaye,Antonio Battisti,Fabiola Feltrin,Britta Kraushaar,Marc Stegger

doi:10.1371/journal.pone.0137143

Abstract

Methicillin-resistant Staphylococcus aureus (MRSA) Sequence Type (ST)1, Clonal Complex(CC)1, SCCmec V is one of the major Livestock-Associated (LA-) lineages in pig farming industry in Italy and is associated with pigs in other European countries. Recently, it has been increasingly detected in Italian dairy cattle herds. The aim of this study was to analyse the differences between ST1 MRSA and methicillin-susceptible S. aureus (MSSA) from cattle and pig herds in Italy and Europe and human isolates. Sixty-tree animal isolates from different holdings and 20 human isolates were characterized by pulsed-field gel electrophoresis (PFGE), spa-typing, SCCmec typing, and by micro-array analysis for several virulence, antimicrobial resistance, and strain/host-specific marker genes. Three major PFGE clusters were detected. The bovine isolates shared a high (≥90% to 100%) similarity with human isolates and carried the same SCCmec type IVa. They often showed genetic features typical of human adaptation or present in human-associated CC1: Immune evasion cluster (IEC) genes sak and scn, or sea; sat and aphA3-mediated aminoglycoside resistance. Contrary, typical markers of porcine origin in Italy and Spain, like erm(A) mediated macrolide-lincosamide-streptograminB, and of vga(A)-mediated pleuromutilin resistance were always absent in human and bovine isolates. Most of ST(CC)1 MRSA from dairy cattle were multidrug-resistant and contained virulence and immunomodulatory genes associated with full capability of colonizing humans. As such, these strains may represent a greater human hazard than the porcine strains. The zoonotic capacity of CC1 LA-MRSA from livestock must be taken seriously and measures should be implemented at farm-level to prevent spill-over.

Highlights

Methicillin-resistant Staphylococcus aureus (MRSA) spa-type t127, Sequence Type (ST) 1, was first reported as one of the three most prevalent MRSA lineages in Italian pig industry, present in 6% of the holdings surveyed in Italy in 2008 [1]
ST1 belongs to Clonal Complex (CC)1, a successful lineage associated with human infections, which includes Panton-Valentine (PVL)-positive CA-MRSA known as USA400 [2]
Macrorestriction-pulse field gel electrophoresis (PFGE) clusters showed an impressive concordance with host of isolation and a series of other genetic markers that are often carried by mobile genetic elements (MGEs), bacteriophages, and subject to loss or acquisition in relation to host adaptation process, useful for molecular epidemiology (Fig 1)

Summary

Introduction

Methicillin-resistant Staphylococcus aureus (MRSA) spa-type t127, Sequence Type (ST) 1, was first reported as one of the three most prevalent MRSA lineages in Italian pig industry, present in 6% of the holdings surveyed in Italy in 2008 [1]. ST1 spa-type t127 isolates have been reported as the sixth most prevalent clone, both MSSA and MRSA, isolated from human invasive infections in Europe [7,8]. As previously reported [9] spa-type t127 ST1 isolates of porcine origin shared a 75% similarity when tested by pulse field gel electrophoresis (PFGE) with isolates of human origin. They showed mainly differences in the SCCmec cassette and in some virulence and antimicrobial resistance marker genes

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