Pigs have been recognised as a reservoir of livestock associated methicillin-resistant Staphylococcus aureus (LA-MRSA) in Europe, Asia and North America. However, little is known about the presence and distribution of MRSA in the Australian pig population and pig industry. This study describes the presence, distribution and molecular characteristics of the human adapted Australian CA-MRSA ST93 isolated from pigs, people, and the environment within a piggery. Isolates were subjected to antibiotic susceptibility testing, DNA microarray, whole genome sequencing, multi locus sequence typing, virulence and resistance gene characterization and phylogenetic analysis. MRSA were isolated from 60% (n = 52) of farm workers where 84% of isolates returned ST93 and the rest ST398. Of the thirty-one pig isolates tested further, an equal number of ST398 and ST93 (15 each) and one as ST30-V were identified. Four of six environmental isolates were identified as ST93 and two as ST398. This study has identified for the first time in Australia the occurrence of CA-MRSA ST93 and LA-MRSA ST398 amongst farm workers, pigs, and the farm environment. Comparative genome analysis indicates that ST398 is likely to have been introduced into Australia from Europe or North America. This study also reports the first linezolid resistant MRSA isolated in Australia.

In a structured survey of all major chicken-meat producers in Australia, we investigated the antimicrobial resistance (AMR) and genomic characteristics of Campylobacter jejuni (n = 108) and C. coli (n = 96) from cecal samples of chickens at slaughter (n = 200). The majority of the C. jejuni (63%) and C. coli (86.5%) samples were susceptible to all antimicrobials. Fluoroquinolone resistance was detected among both C. jejuni (14.8%) and C. coli (5.2%), although this only included three sequence types (STs) and one ST, respectively. Multidrug resistance among strains of C. jejuni (0.9%) and C. coli (4.1%) was rare, and fluoroquinolone resistance, when present, was never accompanied by resistance to any other agent. Comparative genome analysis demonstrated that Australian isolates were found dispersed on different branches/clusters within the international collection. The major fluoroquinolone-resistant STs of C. jejuni (ST7323, ST2083, and ST2343) and C. coli (ST860) present in Australian chickens were similar to those of international isolates and have been reported previously in humans and animals overseas. The detection of a subpopulation of Campylobacter isolates exclusively resistant to fluoroquinolone was unexpected since most critically important antimicrobials such as fluoroquinolones are excluded from use in Australian livestock. A number of factors, including the low level of resistance to other antimicrobials, the absence of fluoroquinolone use, the adoption of measures for preventing spread of contagion between flocks, and particularly the genomic identities of isolates, all point to humans, pest species, or wild birds as being the most plausible source of organisms. This study also demonstrates the need for vigilance in the form of surveillance for AMR based on robust sampling to manage AMR risks in the food chain. IMPORTANCE Campylobacter is one of the most common causes of gastroenteritis in humans, with infections frequently resulting from exposure to undercooked poultry products. Although human illness is typically self-limiting, a minority of cases do require antimicrobial therapy. Ensuring that Campylobacter originating from meat chickens does not acquire resistance to fluoroquinolones is therefore a valuable outcome for public health. Australia has never legalized the use of fluoroquinolones in commercial chickens and until now fluoroquinolone-resistant Campylobacter has not been detected in the Australian poultry. This structured survey of meat chickens derived from all major Australian producers describes the unexpected emergence of fluoroquinolone resistance in Campylobacter jejuni and C. coli. Genetic characterization suggests that these isolates may have evolved outside the Australian poultry sector and were introduced into poultry by humans, pest species, or wild birds. The findings dramatically underline the critical role of biosecurity in the overall fight against antimicrobial resistance.

The World Health Organisation has defined “highest priority critically important antimicrobials” (CIAs) as those requiring the greatest control during food production. Evidence demonstrating that restricted antimicrobial usage prevents the emergence of resistance to CIA’s amongst pathogenic and commensal organisms on a production system-wide scale would strengthen international efforts to control antimicrobial resistance (AMR). Therefore, in a designed survey of all major chicken-meat producers in Australia, we investigated the phenotypic AMR of E. coli (n = 206) and Salmonella (n = 53) from caecal samples of chickens at slaughter (n = 200). A large proportion of E. coli isolates (63.1%) were susceptible to all tested antimicrobials. With regards to CIA resistance, only two E.coli isolates demonstrated resistance to fluoroquinolones, attributed to mutations in the quinolone resistance-determining regions of gyrA. Antimicrobial resistance was observed for trimethoprim/sulfamethoxazole (8.7%), streptomycin (9.7%), ampicillin (14.1%), tetracycline (19.4%) and cefoxitin (0.5%). All Salmonella isolates were susceptible to ceftiofur, chloramphenicol, ciprofloxacin, colistin, florfenicol, gentamicin and tetracycline. A low frequency of Salmonella isolates exhibited resistance to streptomycin (1.9%), ampicillin (3.8%), and cefoxitin (11.3%). AMR was only observed among Salmonella Sofia serovars. None of the Salmonella isolates exhibited a multi-class-resistant phenotype. Whole genome sequencing did not identify any known resistance mechanisms for the Salmonella isolates demonstrating resistance to cefoxitin. The results provide strong evidence that resistance to highest priority CIA’s is absent in commensal E. coli and Salmonella isolated from Australian meat chickens, and demonstrates low levels of resistance to compounds with less critical ratings such as cefoxitin, trimethoprim/sulfamethoxazole, and tetracycline. Apart from regulated exclusion of CIAs from most aspects of livestock production, vaccination against key bacterial pathogens and stringent biosecurity are likely to have contributed to the favorable AMR status of the Australian chicken meat industry. Nevertheless, industry and government need to proactively monitor AMR and antimicrobial stewardship practices to ensure the long-term protection of both animal and human health.

Non-typhoidal Salmonella is a major zoonotic pathogen that plays a significant role in foodborne human salmonellosis worldwide through the consumption of contaminated foods, particularly those of animal origin. Despite a considerable reduction in human salmonellosis outbreaks in developed countries, Australia is experiencing a continuous rise of such outbreaks in humans. This review of the literature highlights the reported non-typhoidal Salmonella outbreaks in humans as well as the occurrence of the pathogen in foods from animal sources throughout Australia. Non-typhoidal Salmonella infections from food animals are more often associated with at-risk people, such as immunocompromised and aged people or children. Although several animal-sourced foods were recognised as the catalysts for salmonellosis outbreaks in Australia, egg and egg-based products remained the most implicated foods in the reported outbreaks. This review further highlights the antimicrobial resistance trends of non-typhoidal Salmonella isolates at the human–food interface, with a focus on clinically important antimicrobials in humans, by collating evidence from previous investigations in Australia. The rise in antimicrobial-resistant Salmonella, especially to antimicrobials commonly prescribed to treat human salmonellosis, has become a significant global public health concern. However, the overall prevalence of antimicrobial resistance in Australia is considerably lower than in other parts of the world, particularly in terms of critically important antimicrobials for the treatment of human salmonellosis. The present review adds to our understanding of the global epidemiology of non-typhoidal Salmonella with emphasis on the past few decades in Australia.

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