Methicillin-resistant and methicillin-susceptible Staphylococcus aureus in dairy sheep and in-contact humans: An intra-farm study

Abstract

Staphylococcus aureus is involved in a wide variety of diseases in humans and animals, and it is considered one of the most significant etiological agents of intramammary infection in dairy ruminants, causing both clinical and subclinical infections. In this study, the intra-farm prevalence and circulation of methicillin-resistant S. aureus (MRSA) and methicillin-susceptible S. aureus (MSSA) were investigated on an Italian dairy sheep farm previously identified as MRSA-positive by testing bulk tank milk (first isolation in 2012). Human samples (nasal swabs, hand skin samples, and oropharyngeal swabs) from 3 persons working in close contact with the animals were also collected, and the genetic characteristics and relatedness of the MRSA isolates from human and animal sources within the farm were investigated. After 2yr from the first isolation, we confirmed the presence of the same multidrug-resistant strain of MRSA sequence type (ST)1, clonal complex (CC)1, spa type t127, staphylococcal cassette chromosome mec (SCCmec) type IVa, showing identical pulsed field gel electrophoresis (PFGE) and resistance profiles at the farm level in bulk tank milk. Methicillin-resistant S. aureus isolates were detected in 2 out of 556 (0.34%) individual milk samples, whereas MSSA isolates were detected in 10 samples (1.8%). The MRSA were further isolated from udder skin samples from the 2 animals that were MRSA-positive in milk and in 2 of the 3 examined farm personnel. All MRSA isolates from both ovine and human samples belonged to ST(CC)1, spa type t127, SCCmec type IVa, with some isolates from animals harboring genes considered markers of human adaptation. In contrast, all MSSA isolates belonged to ruminant-associated CC130, ST700, spa type t528. Analysis by PFGE performed on selected MRSA isolates of human and animal origin identified 2 closely related (96.3% similarity) pulsotypes, displaying only minimal differences in gene profiles (e.g., presence of the immune evasion cluster genes). Although we observed low MRSA intra-farm prevalence, our findings highlight the importance of considering the possible zoonotic potential of CC1 livestock-associated MRSA, in view of the ability to persist over years at the farm level. Biosecurity measures and good hygiene practices could be useful to prevent MRSA spread at the farm level and to minimize exposure in the community and in categories related to farm animal industry (e.g., veterinarians, farmers, and farm workers).

Prevalence and characterization of methicillin-resistant Staphylococcus aureus carrying mecA or mecC and methicillin-susceptible Staphylococcus aureus in dairy sheep farms in central Italy

“…In the last years, the emergence of livestock-associated (LA) methicillin-resistant Staphylococcus aureus (MRSA) has been increasingly reported worldwide, with a raising concern for the risks of zoonotic transmission, especially for people with occupational livestock exposure (Hanselman et al, 2006;Vanderhaeghen et al, 2010;Fessler et al, 2012;Guardabassi et al, 2013), but also for the possible introduction of these strains in the community through the food chain (Kluytmans, 2010). Clonal complex (CC)398 is the most prevalent LA-MRSA lineage in Europe, although in Italy other major LA-MRSA lineages, such as CC1 and CC97, have spread and have also been found to colonize and cause infections in livestock (Alba et al, 2015;Feltrin et al, 2015;Luini et al, 2015;Carfora et al, 2016). In the last decade, MRSA clones with a divergent mecA homolog, named mecC (formerly mecALGA251), have been detected in different animal species and human beings in different European countries, with isolates mainly belonging to CC130, CC1943, and CC425 (García-Álvarez et al, 2011;Paterson et al, 2014;Angen et al, 2017).…”

The recent emergence in hospitals of multidrug-resistant community-associated sequence type 1 and spa type t127 methicillin-resistant Staphylococcus aureus investigated by whole-genome sequencing: Implications for screening

“…Following its initial success as a CA clone [19, 28], ST1-MRSA-IV has been associated with HCA-colonization and infection in North and South America, Europe, the Middle East and Asia [21, 29–31]. More recently, ST1-MRSA-IV spa type (t) 127 has been recovered from companion animals, livestock and livestock produce in Italy, Austria and Hungary [32–36]. …”

Molecular Epidemiology of Methicillin-Resistant and Methicillin-Susceptible Staphylococcus aureus in the Ovine Dairy Chain and in Farm-Related Humans

“…In Italy, the community-acquired MRSA (CA-MRSA) ST(CC) 1 spa -type t127 is reported among the main lineages of MRSA isolated in livestock productions [15,16,17,18,19,20,21]. CA-MRSA clones often harbor the PVL virulence genes, more than CA-MSSA, suggesting that methicillin resistance has contributed to the success of pvl -positive S. aureus strains [22].…”

“…Although S. aureus is frequently isolated in ovine milk and dairy products [16,28,29], the occurrence of MRSA in the ovine dairy chain appears to be low [17,18,29,30,31]. The aim of this study was to investigate the genetic diversity, as determined by pulsed-field gel electrophoresis (PFGE) and spa -types, of MRSA and MSSA isolated from samples of udder milk, raw milk, cheeses, nasal swabs of workers, and skin swabs of ewes taken from dairy sheep farms with a history of MRSA in bulk tank milk, as documented in a previous survey.…”