Antimicrobial Resistance, Virulence, and Genetic Lineages of Staphylococci from Horses Destined for Human Consumption: High Detection of S. aureus Isolates of Lineage ST1640 and Those Carrying the lukPQ Gene

SIMPLE SUMMARY: Staphylococci are opportunistic pathogens which colonize humans and animals. Zoonotic transfer of staphylococcal species between domestic animals and humans is common and can occur through direct contact, the environment, and animal-derived food processing, implying a risk of the spread of antimicrobial resistance mechanisms and virulence factors into different ecosystems. Our work aimed at studying the diversity of staphylococcal species in nasal and faecal samples of healthy horses intended for human consumption and their resistance and virulence determinants. Staphylococci were detected in 90% and 66% of nasal and faecal samples tested, respectively. Eight staphylococcal species were detected, with the most prevalent ones being Staphylococcus aureus (all isolates were methicillin-susceptible), Staphylococcus delphini, and Staphylococcus sciuri. The predominant S. aureus lineage, ST1640, is associated with horses for the first time in this study. S. aureus isolates, except those of lineage ST1640, produced equid-adapted leukocidin (LukPQ) and blocker of equine complement system activation (eqSCIN). The toxic shock syndrome toxin-encoding gene was also detected in some S. aureus isolates. Multidrug resistance was observed among S. sciuri isolates, but not among S. aureus. Measures of hygiene and control should be implemented during horse slaughter and meat processing. ABSTRACT: This work aimed to determine the frequency and diversity of Staphylococcus species carriage in horses intended for human consumption, as well as their resistance and virulence determinants. Eighty samples (30 nasal; 50 faecal) were recovered from 73 healthy horses in a Spanish slaughterhouse. The samples were cultured for staphylococci and methicillin-resistant staphylococci (MRS) recovery. The phenotype/genotype of antimicrobial resistance was analysed for all isolates. The spa-type and sequence-type (ST) were determined in Staphylococcus aureus strains; moreover, the presence of virulence and host-adaptation genes (tst, eta, etb, pvl, lukPQ, scn-eq, and scn) was studied by PCR. Staphylococcus species were detected in 27/30 (90%) and 33/50 (66%) of nasal and faecal samples, respectively. Ninety isolates belonging to eight species were recovered, with predominance of S. aureus (n = 34), Staphylococcus delphini (n = 19), and Staphylococcus sciuri (n = 19). S. aureus strains were all methicillin-susceptible (MSSA), 28/34 were susceptible to all the antibiotics tested, and the remaining six showed resistance to (gene-detected) streptomycin (ant (6)-Ia), penicillin (blaZ), and trimetroprim/sulphametoxazole (SXT) (dfrA, dfrG). The lineage ST1640/t2559 was predominant (n = 21). The genes lukPQ and scn-eq were present in all but the ST1640 isolates. Three S. sciuri isolates were multidrug-resistant. Healthy horses in Spain seem to be a reservoir for virulent MSSA and the lineage ST1640, although the presence of the latter in horses is described for the first time in this study. Moreover, the equine-adapted leukocidin gene lukPQ is frequent among S. aureus strains. A large variety of staphylococcal species with low antibiotic resistance rate were also observed.