Abstract

Introduction
S
Materials and Methods
We reviewed investigation findings for Australian S. enterica outbreaks linked to eggs between 2001 and 2011, with our methods detailed elsewhere (Moffatt et al., 2016). Trace back data relating to outbreaks were obtained from records and correspondence with food safety regulators and investigators from state and territory primary industry departments (Moffatt et al., 2016). This included detail on the egg type and quality, extent of trace back, production systems, farm inspections, and Salmonella serovars recovered during sampling.
Results
Trace back and housing systems
Commercially produced eggs were implicated in 159 (96%) of 166 outbreaks with the remainder involving backyard (noncommercial) eggs. For outbreaks involving commercial production, housing system detail was only available for 70 (44%) events. Of these 36 (52%) were cage, 33 (47%) free range, and 1 (1%) barn laid. Trace back was conducted for 106 (64%) outbreaks, identifying a specific farm on 72 (68%) occasions. From the available data, no difference between the proportion of outbreaks linked to eggs produced in cage and free range housing systems was found.
Environmental sampling and egg testing
Of the 72 farms identified, 63 (88%) underwent environmental sampling and egg testing. Salmonella spp. were detected on 41 (63%) farms via environmental testing (including a Salmonella Enteritidis positive quality assurance isolate), with 30 of 41 (73%) farms having the outbreak strain. Among 49 farms where whole eggs were sampled, 16 (33%) had Salmonella spp. isolated, with 12 of 16 (75%) farms yielding the outbreak strain. While specific sampling details for on-farm investigations were incomplete, available data showed drag swabbing resulted more frequently in Salmonella spp. being isolated (40 farms), followed by fecal sampling (25 farms), equipment swabbing (22 farms), and feed sampling (21 farms).
Salmonella serovars
The Table 1 shows the recovery of Salmonella spp. from farms and processing environments following outbreak investigations. Salmonella Typhimurium was recovered from environmental samples and eggs sampled in response to 30 outbreaks, including 28 (93%) where the outbreak case isolates and farm-derived isolates matched. Non-Typhimurium serovars, including Salmonella Infantis, Salmonella Montevideo, and Salmonella Orion, were recovered on multiple occasions. However, on only four occasions did a farm-derived non-Typhimurium serovar match an outbreak strain, including Salmonella Singapore (twice), Salmonella Enteritidis, and Salmonella Livingstone.
Bold parts indicate a match between the outbreak agent and Salmonella spp recovered via environmental sampling or from sampled eggs.
MLVA, multiple-locus variable number tandem repeats analysis.
Discussion
Our report shows a high detection rate for outbreak associated Salmonella spp., particularly Salmonella Typhimurium, following microbiological investigation of layer farms and processing environments in Australia. The frequency of detection of this serovar over the study period highlights ongoing issues with environmental contamination and layer colonization, carrying significant implications for food safety in Australia.
Recovery of multiple Salmonella serovars from layer environments is not unusual. A state-wide survey of Australian farms revealed nearly half were positive for Salmonella spp. with 20% having Salmonella Typhimurium detected (New South Wales Food Authority [NSWFA], 2013). Prevalence between and within layer flocks also varies with Salmonella Typhimurium being shed for up to 15 weeks postinfection (Pande et al., 2016). Our data also show high detection rates for Salmonella spp., particularly Salmonella Typhimurium, reflecting the targeted nature of outbreak testing. Salmonella Typhimurium was not isolated from all investigated farms, which may reflect intermittent shedding of Salmonella Typhimurium (Pande et al., 2016) or differences in sampling strategies employed for outbreak events and between states.
In the European Union (EU), characteristics are assessed to aid in determining whether a Salmonella serovar is of public health significance. These include its frequency in causing human salmonellosis, its prevalence in an animal population, its ability to spread rapidly, and evidence of its increased virulence (European Commission [EC], 2003). Australian public health data have shown significant increases in Salmonella Typhimurium infections and outbreaks, and this serovar is responsible for the majority of human outbreak cases, with eggs the most important source of infection (Moffatt et al., 2016). Furthermore, the prevalence in the Australian population of serovars other than Salmonella Typhimurium is low, while the pathogenicity and virulence of Salmonella Typhimurium relative to these other serovars are demonstrated (McWhorter et al., 2015).
Layer farm contamination with Salmonella Typhimurium is a significant problem, with good agreement between the levels of environmental contamination, egg shell contamination, and human disease (Wales and Davies, 2011). From our data, of the 16 outbreaks where S. enterica was isolated from farm-sampled eggs, 14 (88%) had the same serovar(s) isolated from environmental samples. The presence of eggshell contamination without contamination of the internal contents, together with a low frequency of reproductive tract infection, suggests horizontal infection via feces is the major route for contamination with Salmonella Typhimurium (Pande et al., 2016).
In Australia most commercially produced eggs are washed to reduce microbial contamination (Gole et al., 2014). Considerable debate exists around egg washing with suggestions it may facilitate shell penetration by Salmonella Typhimurium (Gole et al., 2014), which may offer insight into its capacity for evading postcollection controls and causing outbreaks.
Salmonella contamination of flocks and shell eggs is multifactorial (Denagamage et al., 2015) with thorough outbreak investigation essential to understanding egg-associated disease and guiding mitigation strategies. Our effort to collate trace back findings in a uniform manner by retrospectively compiling investigative data from multiple sources outside of health departments was challenging. Data collection was not standardized across jurisdictions, with a lack of detail on sampling methods and the types of production systems implicated in outbreaks being notable limitations. However since 2011, guidelines for trace back investigation for egg-associated outbreaks have been developed (Biosecurity South Australia and New South Wales Food Authority [NSWFA], 2013), and we support their adoption and routine use. These should include the collection of a core data set to be shared with public health investigators. Notwithstanding, our evidence continues to highlight the need for a national regulatory response and review into the issue of Salmonella Typhimurium and eggs in Australia, with policy makers and stakeholders needing to consider international approaches in addressing egg-associated salmonellosis.
Conclusion
Egg-associated salmonellosis is an important public health issue in Australia, with the detection of Salmonella Typhimurium within layer environments and flocks representing a risk to human health. Reducing this risk will require ongoing and high level engagement between the human health sector, regulators, and industry.
Footnotes
Acknowledgments
OzFoodNet is funded by the Australian Government Department of Health. Cameron Moffatt receives funding from a National Health and Medical Research Council Public Health and Health Services Postgraduate Research Scholarship (APP1074790).
Disclosure Statement
No competing financial interests exist.
