Epidemiology and molecular characterisation of methicillin resistant Staphylococcus aureus in the Australian pig industry

Methicillin resistant Staphylococcus aureus (MRSA) is an opportunistic pathogen of humans and some livestock that causes skin and soft tissue infections with potential to progress to fatal bacteraemia. MRSA poses a potent threat to human and animal health because of its resistance to many common antibiotics. Pigs are a notable reservoir for MRSA due to their asymptomatic carriage of particular sequence types and a demonstrated capacity to transfer these to humans involved in pig farms. In the last decade, MRSA has emerged as a challenge in many pig-producing regions, especially across Europe and North America, and is traditionally known as livestock-associated MRSA (LA-MRSA). In Australia, LA-MRSA isolates appear to represent a smaller proportion of invasive S.aureus isolates obtained from humans than observed in Europe and this may explain why epidemiological aspects of LA-MRSA in the Australian pig industry have not been well described. However, in 2014, MRSA was implicated as the cause of an ongoing outbreak of staphylococcal disease amongst workers at a pig farm in New South Wales.
The overall goal of this research was to advance the understanding of MRSA in pigs in Australia. The first objective of this study was to explore a unique outbreak of MRSA in piggery workers and to elucidate the potential role of the pigs in this outbreak, including identification of the potential risk factors for MRSA carriage associated with the occupational activity. The second objective of this study was to determine the prevalence, distribution, and antibiotic susceptibility of MRSA in Australian pig herds
The outbreak investigation revealed occurrence of bidirectional transmission of MRSA between pigs and humans. A high prevalence of asymptomatic carriage was found in pigs (75.2%; 95% CI 71.8-78.6) and humans (59.6% CI 46.1- 71.8) with two distinct MRSA lineages present. One comprised ST93 - regarded as a highly-virulent form of community-associated (CA) MRSA in humans in Australia. The second was ST398 - a pig-adapted strain of LA-MRSA that is thought to have a global distribution. The odds of MRSA carriage for persons working in direct contact with pigs was 24 times that for persons with no pig contact and a dose-response relationship was found between carriage of workers and the number of hours of exposure to pigs. Moreover, this association was observed both for the LA-MRSA ST398 and the human-derived CA-MRSA ST93, therefore, reporting for the first time ST93 as a potential occupational-risk for piggery workers. In a subsequent national survey of commercial pig herds, MRSA was found on 54% (CI 35.5-71.2) of the 26 study farms, with pig-level prevalence ranging from 1.6% to 100% within infected farms. All MRSA collected in the national herd survey were identified as ST398. No ST93 or any other CA-MRSA were detected on any other farm. This study also indicates that MRSA carriage and infection in piggery workers could potentially cause a significant economic impact to the Australian pig industry, and the emergence of new MRSA strains like ST93 amongst piggery workers could pose a major economic challenge. The outcomes of these studies indicate that in Australia, and probably elsewhere, greater scrutiny of staphylococcal infections in humans and animals is warranted, in the form of coordinated investigation of outbreaks to identify the factors predisposing each host species to infection and emergence of virulent pathogens with novel resistance traits. The risk of MRSA carriage is greatest when working with direct pig contact; therefore, emphasis is required on personal protective equipment. Findings and recommendations outlined in this thesis could be used to develop relevant strategies and interventions to limit the MRSA spread among pigs and piggery workers.