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

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.

A Livestock-Associated, Multidrug-Resistant, Methicillin-Resistant Staphylococcus aureus Clonal Complex 97 Lineage Spreading in Dairy Cattle and Pigs in Italy

“…This differs from what has been observed for CC1 LA-MRSA isolates from Italian dairy cattle, which are closely related and most likely derived from a human CC1 SCCmec IVa lineage (33). This may also indicate that the CC97 MRSA strains are unlikely to have originated from humanto-cattle spillback.…”

“…One MSSA isolate (ST97) from dairy cattle carried the LukM and LukF-PV(P83) genes encoding the highly active bicomponent leukocidin typical of S. aureus strains from cattle and ruminants (24). All isolates carried the hemolysin genes hlb, hl, and hlIII (hl and hlIII coding for a putative membrane protein [33]), and all but three cattle isolates were also positive for hla.…”

Livestock-Associated MRSA and Its Current Evolution

“…CC1/ST1 is one of the major clones circulating in Italy, where it first was reported in pigs [87,88] and dairy cows [43], and seems to be spreading to other countries. In 2009, one strain was detected in Denmark [89], and recently a few strains were discovered in veal calves and pigs in Belgium [29•].…”

“…Fortunately, to date and to our knowledge, PVL-positive MRSA CC1 isolates have not yet been isolated from animals; however, typically present are the IEC genes sak and scn, or the enterotoxine gene sea as in human strains, and they also may carry β-hemolysins, LukFLukS, LukD-LukE, LukX-LukY γ-hemolysin, enterotoxin H, and superantigen X [87,90]. The typical strain found in animals belongs to spa type t127 [43,[87][88][89]. MRSA CC1 also has been implicated in mastitis in cows in Italy [43,90].…”

Methicillin-Resistant Staphylococcus aureus (MRSA) in Food- Producing and Companion Animals and Food Products

“…Although some studies suggested that the MRSA present in catle is bovine-speciic, most of the reports indicated that MRSA found in catle were derived from humans [89,92,115,116]. Bovine, porcine, canine, feline, and equine MRSA isolates containing the pvl gene and other virulence factors, such as chp, scn, seb, sek, and seq, toxic shock syndrome toxin 1 (tsst1 or tst) gene [91,117], hemolysin, protease, superantigen-like protein, capsule, and bioilm-associated genes [118][119][120][121], may pose a potential threat to public health. …”