Modelling high pathogenic avian influenza outbreaks in the commercial poultry industry.

Highly pathogenic avian influenza (HPAI) outbreaks are devastating to poultry industries and pose a risk to human health. There is concern that demand for free-range poultry products could increase the number of HPAI outbreaks by increasing the potential for low pathogenic avian influenza (LPAI) introduction to commercial flocks. We formulate stochastic mathematical models to understand how poultry-housing (barn, free-range and caged) within the meat and layer sectors interacts with a continuous low-level risk of introduction from wild birds, heterogeneity in virus transmission rates and virus mutation probabilities, to affect the risk of HPAI emergence - at both the shed and industry scales. For H5 and H7 viruses, restricted mixing in caged systems, free-range outdoor access and, particularly, production cycle length significantly influence HPAI risk between sectors of the chicken production industry. Results demonstrate how delay between virus mutation and detection, ensuing from the short production cycle, large shed sizes and industry reporting requirements, could mean that HPAI emerges in meat-production sheds but is undetected with few birds affected. We also find that the Australian HPAI outbreak history appears to be better explained by low LPAI introduction rates and low mutation probabilities, rather than extremely rare introduction and relatively high mutation probabilities.

Emergence of Brucella suis in dogs in New South Wales, Australia: clinical findings and implications for zoonotic transmission.

BACKGROUND: Animal reservoirs of brucellosis constitute an ongoing threat to human health globally, with foodborne, occupational and recreational exposures creating opportunities for transmission. In Australia and the United States, hunting of feral pigs has been identified as the principal risk factor for human brucellosis due to Brucella suis. Following increased reports of canine B. suis infection, we undertook a review of case notification data and veterinary records to address knowledge gaps about transmission, clinical presentation, and zoonotic risks arising from infected dogs. RESULTS: Between 2011 and 2015, there was a 17-fold increase in the number of cases identified (74 in total) in New South Wales, Australia. Spatial distribution of cases largely overlapped with high feral pig densities in the north of the state. Ninety per cent of dogs had participated directly in pig hunting; feeding of raw feral pig meat and cohabitation with cases in the same household were other putative modes of transmission. Dogs with confirmed brucellosis presented with reproductive tract signs (33 %), back pain (13 %) or lameness (10 %); sub-clinical infection was also common (40 %). Opportunities for dog-to-human transmission in household and occupational environments were identified, highlighting potential public health risks associated with canine B. suis infection. CONCLUSIONS: Brucellosis due to B. suis is an emerging disease of dogs in Australia. Veterinarians should consider this diagnosis in any dog that presents with reproductive tract signs, back pain or lameness, particularly if the dog has a history of feral pig exposure. Moreover, all people in close contact with these dogs such as hunters, household contacts and veterinary personnel should take precautions to prevent zoonotic transmission.

Information delivery and the veterinarian-horse owner relationship in the context of Hendra virus in Australia.

Hendra virus (HeV) is an emerging bat-borne virus endemic in Australia that can be transmitted from horses to humans and has a high fatality rate for horses and people. Controversy surrounding HeV risk mitigation measures have strained the veterinarian-horse owner relationship. This study aimed to characterise the veterinarian-horse owner relationship in general and also in the context of HeV by analysing data derived from the 'Horse Owners and Hendra Virus: A Longitudinal Study to Evaluate Risk' (HHALTER) study. Australian horse owners were recruited via emails, social media and word-of-mouth for a series of five surveys that were administered online at six-monthly intervals over a two-year period to capture baseline knowledge, attitudes and practices of horse owners regarding HeV and any changes over time. In the current study, descriptive analyses of information sources were performed to understand the use of veterinarians as a HeV information source (Surveys 1 and 5; n = 1195 and n = 617). Ordinal logistic regression analyses were conducted to determine factors associated with the frequency of horse owner contact with a veterinarian (Survey 3; n = 636). This study found a relative increase over the study period in the proportion of horse owners who had used veterinarians as HeV information source in the last 12 months (from 51.9% to 88.3%). Owning more horses, being older, having a 'duty of care' for other people working with horses and deriving the main income from horse related business were factors associated with more frequent veterinary contact. Results suggest that traditional information sources such as workshops, information packs and risk training are likely to be used by horse owners. Smart phone applications should be considered for use in the future and require further investigation for horse health communication. The findings of this study may be helpful in optimising strategies for horse health information delivery.

Correction: Assessing the probability of introduction and spread of avian influenza (AI) virus in commercial Australian poultry operations using an expert opinion elicitation.

[This corrects the article DOI: 10.1371/journal.pone.0193730.].

Correction: Comparisons of management practices and farm design on Australian commercial layer and meat chicken farms: Cage, barn and free range.

[This corrects the article DOI: 10.1371/journal.pone.0188505.].

Low Pathogenic Avian Influenza Exposure Risk Assessment in Australian Commercial Chicken Farms.

This study investigated the pathways of exposure to low pathogenic avian influenza (LPAI) virus among Australian commercial chicken farms and estimated the likelihood of this exposure occurring using scenario trees and a stochastic modeling approach following the World Organization for Animal Health methodology for risk assessment. Input values for the models were sourced from scientific literature and an on-farm survey conducted during 2015 and 2016 among Australian commercial chicken farms located in New South Wales and Queensland. Outputs from the models revealed that the probability of a first LPAI virus exposure to a chicken in an Australian commercial chicken farms from one wild bird at any point in time is extremely low. A comparative assessment revealed that across the five farm types (non-free-range meat chicken, free-range meat chicken, cage layer, barn layer, and free range layer farms), free-range layer farms had the highest probability of exposure (7.5 × 10-4; 5% and 95%, 5.7 × 10-4-0.001). The results indicate that the presence of a large number of wild birds on farm is required for exposure to occur across all farm types. The median probability of direct exposure was highest in free-range farm types (5.6 × 10-4 and 1.6 × 10-4 for free-range layer and free-range meat chicken farms, respectively) and indirect exposure was highest in non-free-range farm types (2.7 × 10-4, 2.0 × 10-4, and 1.9 × 10-4 for non-free-range meat chicken, cage layer, and barn layer farms, respectively). The probability of exposure was found to be lowest in summer for all farm types. Sensitivity analysis revealed that the proportion of waterfowl among wild birds on the farm, the presence of waterfowl in the range and feed storage areas, and the prevalence of LPAI in wild birds are the most influential parameters for the probability of Australian commercial chicken farms being exposed to avian influenza (AI) virus. These results highlight the importance of ensuring good biosecurity on farms to minimize the risk of exposure to AI virus and the importance of continuous surveillance of LPAI prevalence including subtypes in wild bird populations.

Low- and High-Pathogenic Avian Influenza H5 and H7 Spread Risk Assessment Within and Between Australian Commercial Chicken Farms.

This study quantified and compared the probability of avian influenza (AI) spread within and between Australian commercial chicken farms via specified spread pathways using scenario tree mathematical modeling. Input values for the models were sourced from scientific literature, expert opinion, and a farm survey conducted during 2015 and 2016 on Australian commercial chicken farms located in New South Wales (NSW) and Queensland. Outputs from the models indicate that the probability of no establishment of infection in a shed is the most likely end-point after exposure and infection of low-pathogenic avian influenza (LPAI) in one chicken for all farm types (non-free range meat chicken, free range meat chicken, cage layer, barn layer, and free range layer farms). If LPAI infection is established in a shed, LPAI is more likely to spread to other sheds and beyond the index farm due to a relatively low probability of detection and reporting during LPAI infection compared to high-pathogenic avian influenza (HPAI) infection. Among farm types, the median probability for HPAI spread between sheds and between farms is higher for layer farms (0.0019, 0.0016, and 0.0031 for cage, barn, and free range layer, respectively) than meat chicken farms (0.00025 and 0.00043 for barn and free range meat chicken, respectively) due to a higher probability of mutation in layer birds, which relates to their longer production cycle. The pathway of LPAI spread between sheds with the highest average median probability was spread via equipment (0.015; 5-95%, 0.0058-0.036) and for HPAI spread between farms, the pathway with the highest average median probability was spread via egg trays (3.70 × 10-5; 5-95%, 1.47 × 10-6-0.00034). As the spread model did not explicitly consider volume and frequency of the spread pathways, these results provide a comparison of spread probabilities per pathway. These findings highlight the importance of performing biosecurity practices to limit spread of the AI virus. The models can be updated as new information on the mechanisms of the AI virus and on the volume and frequency of movements shed-to-shed and of movements between commercial chicken farms becomes available.

Biosecurity practices on Australian commercial layer and meat chicken farms: Performance and perceptions of farmers.

This paper describes the level of adoption of biosecurity practices performed on Australian commercial chicken meat and layer farms and farmer-perceived importance of these practices. On-farm interviews were conducted on 25 free range layer farms, nine cage layer farms, nine barn layer farms, six free range meat chicken farms and 15 barn meat chicken farms in the Sydney basin bioregion and South East Queensland. There was a high level of treatment of drinking water across all farm types; town water was the most common source. In general, meat chicken farms had a higher level of adoption of biosecurity practices than layer farms. Cage layer farms had the shortest median distance between sheds (7.75m) and between sheds and waterbodies (30m). Equipment sharing between sheds was performed on 43% of free range meat chicken farms compared to 92% of free range layer farms. There was little disinfection of this shared equipment across all farm types. Footbaths and visitor recording books were used by the majority of farms for all farm types except cage layer farms (25%). Wild birds in sheds were most commonly reported in free range meat chicken farms (73%). Dogs and cats were kept across all farm types, from 56% of barn layer farms to 89% of cage layer farms, and they had access to the sheds in the majority (67%) of cage layer farms and on the range in some free range layer farms (44%). Most biosecurity practices were rated on average as 'very important' by farmers. A logistic regression analysis revealed that for most biosecurity practices, performing a practice was significantly associated with higher perceived farmer importance of that biosecurity practice. These findings help identify farm types and certain biosecurity practices with low adoption levels. This information can aid decision-making on efforts used to improve adoption levels.

Assessing the probability of introduction and spread of avian influenza (AI) virus in commercial Australian poultry operations using an expert opinion elicitation.

The objective of this study was to elicit experts' opinions and gather estimates on the perceived probability of introduction and spread of avian influenza (AI) virus in the Australian broiler and layer industry. Using a modified Delphi method and a 4-step elicitation process, 11 experts were asked to give initial individual estimates for the various pathways and practices in the presented scenarios using a questionnaire. Following this, a workshop was conducted to present group averages of estimates and discussion was facilitated to obtain final individual estimates. For each question, estimates for all experts were combined using a discrete distribution, with weights allocated representing the level of expertise. Indirect contact with wild birds either via a contaminated water source or fomites was considered the most likely pathway of introduction of low pathogenic avian influenza (LPAI) on poultry farms. Presence of a water body near the poultry farm was considered a potential pathway for introduction only when the operation type was free range and the water body was within 500m distance from the shed. The probability that LPAI will mutate to highly pathogenic avian influenza (HPAI) was considered to be higher in layer farms. Shared personnel, equipment and aerosol dispersion were the most likely pathways of shed to shed spread of the virus. For LPAI and HPAI spread from farm to farm, shared pick-up trucks for broiler and shared egg trays and egg pallets for layer farms were considered the most likely pathways. Findings from this study provide an insight on most influential practices on the introduction and spread of AI virus among commercial poultry farms in Australia, as elicited from opinions of experts. These findings will be used to support parameterization of a modelling study assessing the risk of AI introduction and spread among commercial poultry farms in Australia.

Australian horse owners and their biosecurity practices in the context of Hendra virus.

In recent years, outbreaks of exotic as well as newly emerging infectious diseases have highlighted the importance of biosecurity for the Australian horse industry. As the first potentially fatal zoonosis transmissible from horses to humans in Australia, Hendra virus has emphasised the need to incorporate sound hygiene and general biosecurity practices into day-to-day horse management. Recommended measures are widely publicised, but implementation is at the discretion of the individual owner. This cross-sectional study aimed to determine current levels of biosecurity of horse owners and to identify factors influencing the uptake of practices utilising data from an online survey. Level of biosecurity (low, medium, high), as determined by horse owners' responses to a set of questions on the frequency of various biosecurity practices performed around healthy (9 items) and sick horses (10 items), was used as a composite outcome variable in ordinal logistic regression analyses. The majority of horse owners surveyed were female (90%), from the states of Queensland (45%) or New South Wales (37%), and were involved in either mainly competitive/equestrian sports (37%) or recreational horse activities (35%). Seventy-five percent of owners indicated that they follow at least one-third of the recommended practices regularly when handling their horses, resulting in medium to high levels of biosecurity. Main factors associated with a higher level of biosecurity were high self-rated standard of biosecurity, access to personal protective equipment, absence of flying foxes in the local area, a good sense of control over Hendra virus risk, likelihood of discussing a sick horse with a veterinarian and likelihood of suspecting Hendra virus in a sick horse. Comparison of the outcome variable with the self-rated standard of biosecurity showed that over- as well as underestimation occurred. This highlights the need for continuous communication and education to enhance awareness and understanding of what biosecurity is and how it aligns with good horsemanship. Overall, strengthened biosecurity practices will help to improve animal as well as human health and increase preparedness for future disease outbreaks.

Comparisons of management practices and farm design on Australian commercial layer and meat chicken farms: Cage, barn and free range.

There are few published studies describing the unique management practices, farm design and housing characteristics of commercial meat chicken and layer farms in Australia. In particular, there has been a large expansion of free range poultry production in Australia in recent years, but limited information about this enterprise exists. This study aimed to describe features of Australian commercial chicken farms, with particular interest in free range farms, by conducting on-farm interviews of 25 free range layer farms, nine cage layer farms, nine barn layer farms, six free range meat chicken farms and 15 barn meat chicken farms in the Sydney basin bioregion and South East Queensland. Comparisons between the different enterprises (cage, barn and free range) were explored, including stocking densities, depopulation procedures, environmental control methods and sources of information for farmers. Additional information collected for free range farms include range size, range characteristics and range access. The median number of chickens per shed was greatest in free range meat chicken farms (31,058), followed by barn meat chicken (20,817), free range layer (10,713), barn layer (9,300) and cage layer farms (9,000). Sheds had cooling pads and tunnel ventilation in just over half of both barn and free range meat chicken farms (53%, n = 8) and was least common in free range layer farms (16%, n = 4). Range access in free range meat chicken farms was from sunrise to dark in the majority (93%, n = 14) of free range meat chicken farms. Over half of free range layer farms (56%, n = 14) granted range access at a set time each morning; most commonly between 9:00 to 10.00am (86%, n = 12), and chickens were placed back inside sheds when it was dusk.

"We've learned to live with it"-A qualitative study of Australian horse owners' attitudes, perceptions and practices in response to Hendra virus.

Hendra virus causes sporadic zoonotic disease in Australia following spill over from flying foxes to horses and from horses to people. Prevention and risk mitigation strategies such as vaccination of horses or biosecurity and property management measures are widely publicised, but hinge on initiative and action taken by horse owners as they mediate management, care and treatment of their animals. Hence, underlying beliefs, values and attitudes of horse owners influence their uptake of recommended risk mitigation measures. We used a qualitative approach to investigate attitudes, perceptions and self-reported practices of horse owners in response to Hendra virus to gain a deeper understanding of their decision-making around prevention measures. Data presented here derive from a series of in-depth interviews with 27 horse owners from Hendra virus 'hot spot' areas in New South Wales and Queensland. Interviews explored previous experience, perceptions and resulting behaviour as well as communication around Hendra virus. All interviews were recorded, transcribed verbatim and analysed in NVivo using thematic analysis. Analysis revealed four major themes: perception of Hendra virus as a risk and factors influencing this perception, Hendra virus risk mitigation strategies implemented by horse owners, perceived motivators and barriers of these strategies, and interaction of perceived risk, motivators and barriers in the decision-making process. Although Hendra virus disease was perceived as a serious threat to the health of horses and humans, individual risk perception diverged among horse owners. Perceived severity, likelihood and unpredictability as well as awareness and knowledge of Hendra virus, trust in information obtained and information pathways, demographic characteristics and personal experience were the main factors influencing Hendra virus risk perceptions. Other key determinants of horse owners' decision-making process were attitudes towards Hendra virus risk mitigation measures as well as perceived motivators and barriers thereof. Horse owners' awareness of the necessity to consider individual Hendra virus risk and adequate risk management strategies was described as a learning process, which changed over time. However, different perceptions of risk, barriers and motivators in combination with a weighing up of advantages and disadvantages resulted in different behaviours. These findings demonstrate the multifactorial determinants of cognitive mediating processes and facilitate a better understanding of horse owners' perspectives on preventive horse health measures. Furthermore, they provide valuable feedback to industry and government stakeholders on how to improve effective risk communication and encourage uptake of recommended risk mitigation measures.

Redefining the Australian Anthrax Belt: Modeling the Ecological Niche and Predicting the Geographic Distribution of Bacillus anthracis.

The ecology and distribution of B. anthracis in Australia is not well understood, despite the continued occurrence of anthrax outbreaks in the eastern states of the country. Efforts to estimate the spatial extent of the risk of disease have been limited to a qualitative definition of an anthrax belt extending from southeast Queensland through the centre of New South Wales and into northern Victoria. This definition of the anthrax belt does not consider the role of environmental conditions in the distribution of B. anthracis. Here, we used the genetic algorithm for rule-set prediction model system (GARP), historical anthrax outbreaks and environmental data to model the ecological niche of B. anthracis and predict its potential geographic distribution in Australia. Our models reveal the niche of B. anthracis in Australia is characterized by a narrow range of ecological conditions concentrated in two disjunct corridors. The most dominant corridor, used to redefine a new anthrax belt, parallels the Eastern Highlands and runs from north Victoria to central east Queensland through the centre of New South Wales. This study has redefined the anthrax belt in eastern Australia and provides insights about the ecological factors that limit the distribution of B. anthracis at the continental scale for Australia. The geographic distributions identified can help inform anthrax surveillance strategies by public and veterinary health agencies.

Hendra virus and horse owners--risk perception and management.

Hendra virus is a highly pathogenic novel paramyxovirus causing sporadic fatal infection in horses and humans in Australia. Species of fruit-bats (genus Pteropus), commonly known as flying-foxes, are the natural host of the virus. We undertook a survey of horse owners in the states of Queensland and New South Wales, Australia to assess the level of adoption of recommended risk management strategies and to identify impediments to adoption. Survey questionnaires were completed by 1431 respondents from the target states, and from a spectrum of industry sectors. Hendra virus knowledge varied with sector, but was generally limited, with only 13% of respondents rating their level of knowledge as high or very high. The majority of respondents (63%) had seen their state's Hendra virus information for horse owners, and a similar proportion found the information useful. Fifty-six percent of respondents thought it moderately, very or extremely likely that a Hendra virus case could occur in their area, yet only 37% said they would consider Hendra virus if their horse was sick. Only 13% of respondents stabled their horses overnight, although another 24% said it would be easy or very easy to do so, but hadn't done so. Only 13% and 15% of respondents respectively had horse feed bins and water points under solid cover. Responses varied significantly with state, likely reflecting different Hendra virus history. The survey identified inconsistent awareness and/or adoption of available knowledge, confusion in relation to Hendra virus risk perception, with both over-and under-estimation of true risk, and lag in the uptake of recommended risk minimisation strategies, even when these were readily implementable. However, we also identified frustration and potential alienation by horse owners who found the recommended strategies impractical, onerous and prohibitively expensive. The insights gained from this survey have broader application to other complex risk-management scenarios.

The influence of meteorology on the spread of influenza: survival analysis of an equine influenza (A/H3N8) outbreak.

The influences of relative humidity and ambient temperature on the transmission of influenza A viruses have recently been established under controlled laboratory conditions. The interplay of meteorological factors during an actual influenza epidemic is less clear, and research into the contribution of wind to epidemic spread is scarce. By applying geostatistics and survival analysis to data from a large outbreak of equine influenza (A/H3N8), we quantified the association between hazard of infection and air temperature, relative humidity, rainfall, and wind velocity, whilst controlling for premises-level covariates. The pattern of disease spread in space and time was described using extraction mapping and instantaneous hazard curves. Meteorological conditions at each premises location were estimated by kriging daily meteorological data and analysed as time-lagged time-varying predictors using generalised Cox regression. Meteorological covariates time-lagged by three days were strongly associated with hazard of influenza infection, corresponding closely with the incubation period of equine influenza. Hazard of equine influenza infection was higher when relative humidity was <60% and lowest on days when daily maximum air temperature was 20-25°C. Wind speeds >30 km hour(-1) from the direction of nearby infected premises were associated with increased hazard of infection. Through combining detailed influenza outbreak and meteorological data, we provide empirical evidence for the underlying environmental mechanisms that influenced the local spread of an outbreak of influenza A. Our analysis supports, and extends, the findings of studies into influenza A transmission conducted under laboratory conditions. The relationships described are of direct importance for managing disease risk during influenza outbreaks in horses, and more generally, advance our understanding of the transmission of influenza A viruses under field conditions.