Detection and Characterization of Staphylococcus aureus and Methicillin-Resistant S. aureus in Foods Confiscated in EU Borders

Abstract

The aim of the study was to evaluate the potential role of the illegal entry of food in UE in the Methicillin-resistant S. aureus (MRSA) spread. We studied the prevalence and characteristics of Staphylococcus aureus and MRSA isolated from foods of animal origin confiscated from passengers on flights from 45 non-EU countries from 2012 to 2015 by the Border Authorities at Bilbao International Airport (Spain) and Vienna International Airport (Austria), as well as foods from open markets close to EU land borders. Of 868 food samples tested (diverse meat samples including antelope, duck, guinea pig, pork, rodents, turkey, dairy products, and eggs), 136 (15.7%) were positive for S. aureus and 26 (3.0%) for MRSA. All MRSA strains were mecA-positive. The prevalence of S. aureus-positive dairy samples among food confiscated at Bilbao International Airport was 64.6%, and this airport also had the highest value (11.8%) for MRSA-positive samples. The predominant sequence type was ST5 (30.8%), followed by ST8, ST1649, ST1, and other lineages were found to a lesser extent (ST7, ST22, ST72, ST97, and ST398). Six isolates tested positive for luk-PVL genes (SCCmec IV subtypes IVc and IVe). Enterotoxin profiling revealed that 19 MRSA strains were enterotoxigenic, harboring one or more se genes. The MRSA isolates positive for luk-PVL genes were not enterotoxigenic, and none of the isolates tested positive for enterotoxin E. We found 14 resistance profiles, and more than 69% of the MRSA isolates were resistant to three or more types of antimicrobial agents. This finding reveals both the wide diversity of the antimicrobial resistance found in the strains and the capacity to resist not only to beta-lactam drugs. One MRSA strain showed unusual characteristics: it was oxacillin-susceptible, harbored SCCmec V, and was positive for sed, seg, and sej but negative for PVL virulence factors. This study shows the presence of enterotoxigenic HA-, CA-, and LA-MRSA in foods illegally entering the EU, and highlights illegal importation of food as route of enterotoxigenic MRSA spread. Uncontrolled entry of food stuffs into the EU can be a relevant neglected route of MRSA dissemination.

High occurrence of enterotoxigenic isolates and low antibiotic resistance rates of Staphylococcus aureus isolated from raw milk from cows and ewes

“…Owing to many limitations we were unable to study the genetic-relatedness of our isolates. However, many studies have reported the clonal spread of food-borne S. aureus isolates containing multienterotoxin genes (Aydin et al 2011;Rodr ıguez-L azaro et al 2017). Taken together, our findings highlight the emergence of enterotoxigenic S. aureus producing SE-like as reported by many studies describing the roles of both SE-like and classical SE in staphylococcal food poisoning (Bianchi et al 2013;Emilie et al 2018).…”

“…; Rodríguez‐Lázaro et al . ). The staphylococcal enterotoxin D (SED) was previously reported as the most frequent toxin type, after SEA, in staphylococcal food poisoning in dairy products (Bianchi et al .…”

“…; Rodríguez‐Lázaro et al . ). Taken together, our findings highlight the emergence of enterotoxigenic S. aureus producing SE‐like as reported by many studies describing the roles of both SE‐like and classical SE in staphylococcal food poisoning (Bianchi et al .…”

The Genomic Context for the Evolution and Transmission of Community-Associated Staphylococcus aureus ST59 Through the Food Chain

“…However, most of these transmission pathways lack regularity, making it difficult to determine the origin of the MRSA clone, especially when clones have spread across the country. As a traceable vector, the food chain poses a significant risk for MRSA transmission across geographic regions, as it has been demonstrated by the illegal introduction and commerce of MRSA-contaminated food (Oniciuc et al, 2015;Rodriguez-Lazaro et al, 2017). Thus, the aim of this study was to characterize the evolutionary dynamic and transmission potential of MRSA through the food chain.…”

Listeria monocytogenes and enterotoxigenic Staphylococcus aureus in dry fermented sausages belonging to “Traditional Agri‐Food Product” produced in Southern Italy

“…Although no strain of S. aureus was found to carry the mecA gene, the presence of MRSA strains has been detected in different foodstuffs including raw bovine milk and cheese (Normanno et al, 2007;Papadopoulos et al, 2018), meat products (de Boer et al, 2009;Rodríguez-Lázaro et al, 2017;Van Loo et al, 2007), and raw chicken meat (Kitai et al, 2005;Kwon et al, 2006). Therefore, the presence of MRSA and antibiotic resistant strains in food of animal origin should be systematically monitored to protect public health.…”