Occurrence of methicillin-resistant Staphylococcus aureus in dairy cattle herds, related swine farms, and humans in contact with herds

Abstract

In this study we investigated the circulation of methicillin-resistant Staphylococcus aureus (MRSA) in 2 dairy cattle farms (farm A and B), previously identified as MRSA-positive in bulk tank milk samples, and epidemiologically related to swine farms. Collected specimens included quarter milk samples and nasal swabs from dairy cows, pig nasal swabs collected at both the farm and slaughterhouse level, environmental dust samples, and human nasal swabs from the farms' owners and workers. The prevalence of MRSA was estimated at the herd level by testing quarter milk samples. The prevalence of MRSA was 4.8% (3/63; 95% confidence interval=0-10.2%) and 60% (33/55; 95% confidence interval=47.05-72.95) in farm A and B, respectively. In farm A, MRSA was also isolated from humans, pigs sampled at both farm and slaughterhouse level, and from environmental samples collected at the pig facilities. The dairy cattle facilities of farm A tested negative for MRSA. In farm B, MRSA was isolated from environmental dust samples in both the cattle and pig facilities, whereas nasal swabs collected from cows and from humans tested negative. Sixty-three selected MRSA isolates obtained from different sources in farm A and B were genetically characterized by multilocus sequence typing, spa-typing, ribosomal spacer-PCR, and also tested for the presence of specific virulence genes and for their phenotypical antimicrobial susceptibility by broth microdilution method. Different clonal complex (CC) and spa-types were identified, including CC398, CC97, and CC1, CC already reported in livestock animals in Italy. The MRSA isolates from quarter milk of farm A and B mostly belonged to CC97 and CC398, respectively. Both lineages were also identified in humans in farm A. The CC97 and CC398 quarter milk isolates were also identified as genotype GTBE and GTAF by ribosomal spacer-PCR respectively, belonging to distinct clusters with specific virulence and resistance patterns. The GTBE and GTAF clusters also included swine, environmental, and human isolates from both farms. A high heterogeneity in the genetic and phenotypic profiles was observed in environmental isolates, in particular from farm B. These results demonstrate the possibility of a dynamic sharing and exchange of MRSA lineages or genotypes between different species and farm compartments in mixed-species farms. The risk of transmission between swine and related dairy cattle herds should be considered. Our findings also confirm the zoonotic potential of livestock-associated MRSA and underline the importance of applying biosecurity measures and good hygiene practices to prevent MRSA spread at the farm level and throughout the food production chain.

Epidemiology and Antimicrobial Susceptibility of Methicillin-Resistant Staphylococcus aureus in Cattle of Pothohar Region, Pakistan

“…The finding shows that overall prevalence of MRSA was 54% in the Pothohar region of Pakistan. Similar highlevel MRSA prevalence of 60%, was reported by Locatelli et al (2017). In contrast to our study lower MRSA prevalence (34%) in Pakistan (2017) was reported: while from other regions of the world a prevalence of 16.7%, and 9.2%, is reported from India (2011), Saudi Arabia (2018), respectively (Kumar et al, 2011;Aqib et al, 2017;El-Deeb et al, 2018).…”

Antimicrobial Resistance on Farms: A Review Including Biosecurity and the Potential Role of Disinfectants in Resistance Selection

“…Apparent spread between species was observed using molecular and resistance typing of LA-MRSA, showing colonization of broilers, rats, dogs, cats, and farmers by strains highly similar to those in pigs on the same premises (Pletinckx et al, 2013). In a pattern already established for other contagious mastitis pathogens, poor hygiene at milking was observed to be associated with LA-MRSA spread between dairy cows (Locatelli et al, 2017).…”

“…Several studies examining the detection and/or subtyping of AMR bacteria have yielded evidence of the physical transfer of AMR between premises and between generations. This has been documented for LA-MRSA in pigs and cattle (Grøntvedt et al, 2016;Locatelli et al, 2017;Pletinckx et al, 2013), for cephalosporin-resistant E. coli in broilers (with hatcheries appearing to act as source and/or conduit in many cases) (Baron et al, 2018;Dierikx et al, 2013), and for FQ-resistant Campylobacter coli in broilers (Idris et al, 2006). An alternative (metagenomic) approach has yielded evidence of associations between the frequencies of certain AMR genes in feces, comparing breeding sows and their derived finishing herds on separate premises (Birkegård et al, 2018).…”

“…Co‐selection by a heavy metal (zinc) is a possible mechanism for the maintenance of multidrug resistant E. coli in piglets around weaning, an association suggested by a recent experimental study (Ciesinski et al., ). Finally, a dairy farm study showed that a LA‐MRSA strain persisted on a unit for at least two years, albeit presumably under conditions of routine antimicrobial use (Locatelli et al., ).…”

Molecular epidemiology of methicillin-susceptible Staphylococcus aureus (MSSA) isolated from milk of cows with subclinical mastitis

“…As far as we know, this is the first report of the detection of spa type t321 isolates in milk samples from cows with subclinical mastitis. Previously, it has only been isolated from humans, and swine [35][36][37], showing that the host specificity of the pathogen may be questioned.…”