Methicillin-resistant Staphylococcus aureus CC22-MRSA-IV as an agent of dairy cow intramammary infections

Highlights

• Numerous subclinical intramammary infections of dairy cow caused by CC22-MRSA-IV.

• CC22-MRSA-IV isolated also from milker’s nose, volunteering in a nursing home.

• Minor molecular differences between human and cow isolates.

• S. aureus strains originally isolated in humans can switch host, adapting to cow.

• Monitoring S. aureus lineages, to reduce risks of spread in both herd and community.

Abstract

Methicillin-resistant S. aureus (MRSA) lineages have become major responsible of healthcare- and community-associated infections in human population. Bovine MRSA are sporadically detected in the dairy herd, but its presence enhances the risk of zoonosis. Some lineages are able to lose the specific host tropism, being easily transmitted from animals to humans and vice-versa. The present study aims at clarifying the epidemiology of MRSA intramammary infections in a closed dairy herd, which was running a mastitis control program since years. Quarter milk samples were collected from all lactating cows once a week for 9 weeks and bacteriologically tested. At the end of the follow-up period, also a self-taken nasal swab of the milker was analysed. Three cows (12.5%) were MRSA positive, a fourth showed a transient infection and MRSA was isolated also from the milker’s nose. Somatic cell counts of infected quarters fluctuated from 1000 to 1,800,000 cells/mL. The isolates were genotyped using DNA microarrays and identified as the epidemic UK-EMRSA-15 grouping in CC22. All strains carried the genes for β-lactam and macrolide resistance. The milker isolate differed from cow isolates mainly for the absence of the untruncated β-haemolysin and the presence of the immune evasion cluster. The milker had been volunteering in a nursing home since months, thus playing the role of MRSA vector into the herd. Our results showed the adaptive capacity of such MRSA to the bovine host. Therefore, we suggest that CC22-MRSA should be regarded as a potential cause of reverse zoonosis in dairy cattle herds.

Introduction

Staphylooccus aureus (S. aureus) is widely known as the major cause of contagious bovine mastitis and an important pathogen in different livestock species (Fitzgerald, 2012). The treatment with β-lactam antibiotics resulted in a selective pressure for resistance, and the acquisition of the mobile staphylococcal cassette chromosome (SCCmec), carrying the mecA or mecC gene, allows the bacteria to continue the cell wall biosynthesis, nullifying the antibiotic action. Methicillin-resistant S. aureus (MRSA) lineages are the result of this successful evolution, becoming a major responsible of healthcare- and community-associated human infections on a global scale (Köck et al., 2010). In contrast with some of the human-associated lineages, all bovine MRSA clones are occasionally detected in the dairy herds, being mostly associated with low prevalence of subclinical mastitis. Despite that, the persistence of MRSA clones in dairy herds enhances the risk of zoonosis (Luini et al., 2015). From the first bovine MRSA detected about 50 years ago (Devriese et al.,1972), understanding the risk of S. aureus cross-species transmission is still an interesting scientific field of research. The phylogenetic studies on MRSA demonstrated that bovine strains belong to a limited group of clonal complexes (CC; Enright et al., 2002; Holden et al., 2013). Human lineages of MRSA, such as CC5, CC8, CC22, CC30 and CC45 are rarely found in dairy animals, suggesting host range barriers (Enright et al., 2002; Sung et al., 2008). On the animal side, the most common livestock-associated MRSA (LA-MRSA) isolates belong to a small number of animal-associated clones: in particular bovine mastitis isolates group in few CCs, including CC9, CC97, CC130, CC133, CC398, CC522 and CC705 (Fitzgerald et al., 2012). Some of these have been demonstrating their ability to shift from animal to human hosts. This is the case of CC398 MRSA, that is considered the most important livestock-associated complex, affecting pig, poultry and ruminant farms, but can colonize and infect humans with direct or indirect livestock contact; moreover, it has been introduced in healthcare settings (van Alen et al., 2018). By contrast, CC8 MSSA originated in humans and emerged in the cow after ancient or recent host jumps (Sakwinska et al., 2011). The new bovine-adapted genotype loses the ability to colonize humans, lacking of a human-related mobile genetic element (Resch et al., 2013). As a result, some S. aureus clones can lose the specific host tropism and be easily transmitted from animals to humans (zoonotic threat) or vice-versa (concept of reverse zoonosis). This study aims at clarifying the epidemiological origin of a new MRSA intramammary infection in a closed dairy cow herd, which was running a mastitis control program since years.