Edited by: Irene Iglesias, Instituto Nacional de Investigación y Tecnología Agraria y Alimentaria (INIA), Spain
Reviewed by: Marius Gilbert, Université libre de Bruxelles, Belgium; Fernanda Dorea, National Veterinary Institute, Sweden
Specialty section: This article was submitted to Veterinary Epidemiology and Economics, a section of the journal Frontiers in Veterinary Science
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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 pathogenic avian influenza (LPAI) viruses are naturally circulating in wild birds globally. Birds in the taxonomic orders Anseriformes (waterfowl including ducks and geese) and Charadriiformes (shorebirds including gulls, waders, and auks) constitute the major natural reservoir of LPAI with an approximate prevalence of 2.5 and 0.6%, respectively, in Australia (
Highly pathogenic avian influenza (AI) is classed as a category 2 emergency animal disease in Australia under the Emergency Animal Disease Response Agreement as it has the potential to cause severe production losses and impact the national economy, and potentially impact human health and/or the environment (
There is concern from experts within the Australian poultry industry about the change in probability of AI outbreak occurrence with the recent consumer driven expansion of free-range poultry farms. There are approximately 800 commercial contract meat chicken grower farms and 300 commercial chicken egg farms currently in Australia (
There are substantial differences in farm design, management, and biosecurity practices among the Australian commercial chicken enterprises, i.e., cage, barn, and free-range systems of both layer and meat chicken farms which can influence wild bird presence on farm (
The World Organisation of Animal Health provides a methodological framework for conducting animal health risk analysis (
Most of the input values used in this model were parameterized using data collected from a survey on commercial chicken farms in Australia (
A survey commenced in mid-2015 involving on-farm interviews with the farm manager or farm owner on 73 commercial chicken farms; 15 non-free-range meat, 15 free-range meat, nine cage layer, 9 barn layer, and 25 free-range layer farms. The farms were located in the Sydney basin region in NSW and in South East Queensland. The Sydney basin region was selected due to the high concentration of both layer and meat chicken farms in this area. However in this region, free-range meat chicken farms are all owned by one of two large privately owned meat chicken companies in Australia. Therefore, additional farm visits to South East Queensland were conducted to gain more representative data of privately owned meat chicken companies in Australia. The interviews involved a comprehensive questionnaire which asked questions to the farmers relating to biosecurity practices performed on farm, wild bird and animal presence, general farm information, and farm management. A greater proportion of layer farms and of free-range farms were surveyed due to the greater perceived risk of AI occurrence on these farm types. More details on the methodology of the survey, including the region and farm selection, questionnaire development, and conduct of the on-farm interviews, can be found in Scott et al. (
The statistical program JMP® was used (© 2012 SAS Institute Inc., Cary, NC, USA) to conduct one-way analysis of variance (ANOVA) to analyze differences between the outcome probabilities for each of the different farm types. The outcome probabilities compared using ANOVA were the outcome probability from 1,000 iterations of the exposure scenario tree model simulation for each farm type, with each iteration reflecting the situation for one farm at a point in time. A
The exposure assessment examines all potential pathways by which AI virus can be introduced from wild birds into a commercial layer or meat chicken farm and estimates the probability that a first exposure to a chicken occurs through each of these pathways. Five exposure assessments were performed, one for each farm type: non-free-range meat chicken farms, free-range meat chicken farms, cage layer farms, barn layer farms, and free-range layer farms. Only LPAI viruses were considered due to the fact that HPAI viruses have never been detected from Australian wild birds during surveillance activities (
In addition, the models considered differences depending on the season or time of the year, given virus prevalence in wild birds changes during different times of the year. The probability of chickens accessing outdoors in free-range farms also changes during different times of the year due to weather conditions. Therefore, three “seasons” were considered in the exposure assessments; winter (June–August), summer (December–February), and then autumn and spring (March–May and September–November) were combined as one season.
Parameters required in these exposure assessments included (1) the probability of wild bird presence in different areas of the commercial chicken farm; (2) the probability of wild birds being infected and excreting LPAI viruses; and (3) parameters in relation to the management and biosecurity practices performed on the farm that would increase or reduce the probability of exposure. The main pathways of exposure considered in these assessments were the following six pathways: (1) direct exposure in a shed; (2) direct exposure around feed storage areas; (3) indirect exposure through fomites or vectors; (4) indirect exposure through aerosol; (5) indirect exposure through contaminated water inside; (6) indirect exposure through contaminated water outside sheds; and (7) direct exposure on the range.
For the purpose of this model, direct exposure is defined as physical contact between a wild bird and a commercial chicken or direct contact between a commercial chicken and wild bird feces. By contrast, indirect exposure is defined as a commercial chicken coming into contact with the virus through a medium, i.e., through water, fomites, or vectors. Fomites include boots and equipment contaminated with wild bird feces and are subsequently in contact with chickens through movement. Biological vectors may become infected with the virus, most notably insects, mice, and rats, and may shed the virus in the presence of chickens or be consumed by chickens. Mechanical vectors, such as dogs and cats, can also present the virus to chickens through movement only.
The overall probability of exposure represents the probability of a first exposure to a domestic chicken by one wild bird in each farm type, irrespective of the pathway of exposure. This probability was calculated by summing the outcome probability of all the pathways that lead to exposure for each farm type. In addition, the overall probability of direct and indirect exposure was calculated by summing the outcome probabilities of the direct (pathways 1, 2, and 7) and indirect (pathways 3, 4, 5, and 6) pathways, respectively, which lead to exposure for each farm type.
The models estimate the probability of exposure posed by a single wild bird at any point in time. This outcome probability of exposure is then used to estimate the expected number of exposures considering a range of the number of wild birds that could visit a property at any point in time and using binomial distributions. The standard prevalence of LPAI, at approximately 2.5, 0.6, and 0.5% for waterfowl, shorebirds, and other bird types, respectively, of which a subset are H5 and H7 subtypes, was used for these binomial distributions (
Tables
Nodes, parameter estimates, and input values used for the exposure assessment estimating the probability of exposure of commercial chickens on non-free-range meat chicken farms in Australia (specifically in the Sydney basin region and South East Queensland) to low pathogenic avian influenza (LPAI) from wild birds.
Node | Branch of node | Parameter estimates | Input values | Data sources |
---|---|---|---|---|
1. Type of wild bird on farm property | Waterfowl |
Proportion of answers from farmers that reported the respective wild bird type on their property ( |
Beta ( |
Scott et al. ( |
2. Prevalence of LPAI in wild birds | Yes |
Probability of the different wild bird types; waterfowl, shorebirds, or other, being infected with LPAI of H5 or H7 subtype in winter, summer, and autumn/spring ( |
Beta ( |
Grillo et al. ( |
3. Respective wild bird type has been reported inside chicken sheds | Yes |
Proportion of farms that witnessed the respective wild bird type inside chicken sheds on the farm. The data suggest the probability for waterfowl and shorebirds inside sheds is close to 0 and, therefore, a Pert distribution is used for these wild bird types ( |
Scott et al. ( |
|
4. Respective wild bird type has been reported in other locations on the farm | Waterbodies |
Proportion of answers from farmers that witnessed the respective wild bird type in the respective areas ( |
Beta ( |
Scott et al. ( |
5. Aerial transmission of LPAI from wild birds to domestic chickens | Yes |
Probability of LPAI introduction |
Beta ( |
Jonges et al. ( |
6. Surface water is used for chickens | Yes |
Proportion of farms that use surface water for the chicken farm ( |
Beta ( |
Scott et al. ( |
7. Water inside chicken sheds is treated | Yes |
Proportion of answers from farmers that treat water inside the chicken sheds ( |
Beta ( |
Scott et al. ( |
8. Chickens have escaped the shed | Yes |
Proportion of farms that have reported chickens unintentionally outside of the shed ( |
Beta ( |
Scott et al. ( |
9. Other indirect routes that can lead to LPAI introduction | Yes |
Probability that chickens will be exposed to LPAI virus |
Scott et al. ( |
Nodes, parameter estimates, and input values used for the exposure assessment estimating the probability of exposure of commercial chickens on free-range meat chicken farms in Australia (specifically in the Sydney basin region and South East Queensland) to low pathogenic avian influenza (LPAI) from wild birds.
Node | Branch of node | Parameter estimates | Input values | Data sources |
---|---|---|---|---|
1. Type of wild bird on farm property | Waterfowl |
Proportion of answers from farmers that reported the respective wild bird type on their property ( |
Beta ( |
Scott et al. ( |
2. Prevalence of LPAI in wild birds | Yes |
Probability of the different wild bird types; waterfowl, shorebirds, or other, being infected with LPAI of H5 or H7 subtype in winter, summer, and autumn/spring ( |
Beta ( |
Grillo et al. ( |
3. Respective wild bird type has been reported inside chicken sheds | Yes |
Proportion of farms that witnessed the respective wild bird type inside chicken sheds on the farm. The data suggest the probability for waterfowl and shorebirds inside sheds is close to 0 and, therefore, a Pert distribution is used for these wild bird types ( |
Scott et al. ( |
|
4. Respective wild bird type has been reported in other locations on the farm | Waterbodies |
Proportion of answers from farmers that witnessed the respective wild bird type in the respective areas ( |
Beta ( |
Scott et al. ( |
5. Suitable weather conditions for range access | Yes |
Probability that the weather conditions for seasons winter, summer, and autumn/spring are suitable for farmers to allow chickens on the range; when conditions are dry, between 17 and 28 C and there is no severe weather ( |
Beta ( |
Bureau of Meterology ( |
6. Birds are a suitable age for range access | Yes |
Proportion of the chicken’ |
Beta ( |
Scott et al. ( |
7. Birds actually go onto the range | Yes |
Proportion of flock that actually leave shed and use the range as reported by farmers ( |
Average of 15 Beta functions ( |
Scott et al. ( |
8. Aerial transmission of LPAI from wild birds to domestic chickens | Yes |
Probability of LPAI introduction |
Beta ( |
Jonges et al. ( |
9. Surface water is used for chickens | Yes |
Proportion of answers from farmers that use surface water for the chicken farm ( |
Beta ( |
Scott et al. ( |
10. Locations surface water is used for | Inside shed |
Proportion of answers from farmers that use surface water for inside the shed versus outside the shed ( |
Beta ( |
Scott et al. ( |
11. Water inside chicken sheds is treated | Yes |
Proportion of answers from farmers that treat water inside the chicken sheds ( |
Beta ( |
Scott et al. ( |
12. Water outside chicken sheds is treated | Yes |
Proportion of answers from farmers that treat water used outside the shed ( |
Beta ( |
Scott et al. ( |
13. Chickens have escaped the shed or range area | Yes |
Proportion of farms that have reported chickens unintentionally outside of the shed or range area ( |
Beta ( |
Scott et al. ( |
14. Other indirect routes that can lead to LPAI introduction | Yes |
Probability that chickens will be exposed to LPAI virus via other indirect methods; boots, mice/rats, insects and pets combined into one probability ( |
Scott et al. ( |
Nodes, parameter estimates and input values used for the exposure assessment estimating the probability of exposure of commercial chickens on cage layer farms in Australia (specifically in the Sydney basin region and South East Queensland) to low pathogenic avian influenza (LPAI) from wild birds.
Node | Branch of node | Parameter estimates | Input values | Data sources |
---|---|---|---|---|
1. Type of wild bird on farm property | Waterfowl |
Proportion of answers from farmers that reported the respective wild bird type on their property ( |
Beta ( |
Scott et al. ( |
2. Prevalence of LPAI in wild birds | Yes |
Probability of the different wild bird types; waterfowl, shorebirds or other, being infected with LPAI of H5 or H7 subtype in winter, summer and autumn/spring ( |
Beta ( |
Grillo et al. ( |
3. Respective wild bird type has been reported inside chicken sheds | Yes |
Proportion of farms that witnessed the respective wild bird type inside chicken sheds on the farm. The data suggests the probability for waterfowl and shorebirds inside sheds is close to 0 and, therefore, a Pert distribution is used for these wild bird types ( |
Scott et al. ( |
|
4. Respective wild bird type has been reported in other locations on the farm | Waterbodies |
Proportion of answers from farmers that witnessed the respective wild bird type in the respective areas ( |
Beta ( |
Scott et al. ( |
5. Aerial transmission of LPAI from wild birds to domestic chickens | Yes |
Probability of LPAI introduction via aerial dispersion from wild birds on waterbodies to chickens on farm ( |
Beta ( |
Jonges et al. ( |
6. Surface water is used for chickens | Yes |
Proportion of farms that use surface water for the chicken farm ( |
Beta ( |
Scott et al. ( |
7. Locations surface water is used for | Inside shed |
Proportion of answers from farmers that use surface water for inside the shed versus outside the shed ( |
Beta ( |
Scott et al. ( |
8. Water inside chicken sheds is treated | Yes |
Proportion of answers from farmers that treat water inside the chicken sheds ( |
Beta ( |
Scott et al. ( |
9. Water outside chicken sheds is treated | Yes |
Proportion of answers from farmers that treat water used outside the shed ( |
Beta ( |
Scott et al. ( |
10. Chickens have escaped the shed | Yes |
Proportion of farms that have reported chickens unintentionally outside of the shed ( |
Beta ( |
Scott et al. ( |
11. Other indirect routes that can lead to LPAI introduction | Yes |
Probability that chickens will be exposed to LPAI virus via other indirect methods; boots, mice/rats, insects and pets combined into one probability ( |
Scott et al. ( |
Nodes, parameter estimates, and input values used for the exposure assessment estimating the probability of exposure of commercial chickens on barn layer farms in Australia (specifically in the Sydney basin region and South East Queensland) to low pathogenic avian influenza (LPAI) from wild birds.
Node | Branch of node | Parameter estimates | Input values | Data sources |
---|---|---|---|---|
1. Type of wild bird on farm property | Waterfowl |
Proportion of answers from farmers that reported the respective wild bird type on their property ( |
Beta ( |
Scott et al. ( |
2. Prevalence of LPAI in wild birds | Yes |
Probability of the different wild bird types; waterfowl, shorebirds or other, being infected with LPAI of H5 or H7 subtype in winter, summer, and autumn/spring ( |
Beta ( |
Grillo et al. ( |
3. Respective wild bird type has been reported inside chicken sheds | Yes |
Proportion of farms that witnessed the respective wild bird type inside chicken sheds on the farm. The data suggests the probability for waterfowl and shorebirds inside sheds is close to 0 and, therefore, a Pert distribution is used for these wild bird types ( |
Scott et al. ( |
|
4. Respective wild bird type has been reported in other locations on the farm | Waterbodies |
Proportion of answers from farmers that witnessed the respective wild bird type in the respective areas ( |
Beta ( |
Scott et al. ( |
5. Aerial transmission of LPAI from wild birds to domestic chickens | Yes |
Probability of LPAI introduction via aerial dispersion from wild birds on waterbodies to chickens on farm ( |
Beta ( |
Jonges et al. ( |
6. Surface water is used for chickens | Yes |
Proportion of farms that use surface water for the chicken farm ( |
Beta ( |
Scott et al. ( |
7. Locations surface water is used for | Inside shed |
Proportion of answers from farmers that use surface water for inside the shed versus outside the shed ( |
Beta ( |
Scott et al. ( |
8. Water inside chicken sheds is treated | Yes |
Proportion of answers from farmers that treat water inside the chicken sheds ( |
Beta ( |
Scott et al. ( |
9. Water outside chicken sheds is treated | Yes |
Proportion of answers from farmers that treat water used outside the shed ( |
Beta ( |
Scott et al. ( |
10. Chickens have escaped the shed | Yes |
Proportion of farms that have reported chickens unintentionally outside of the shed ( |
Beta ( |
Scott et al. ( |
11. Other indirect routes that can lead to LPAI introduction | Yes |
Probability that chickens will be exposed to LPAI virus via other indirect methods; boots, mice/rats, insects and pets combined into one probability ( |
Scott et al. ( |
Nodes, parameter estimates and input values used for the exposure assessment estimating the probability of exposure of commercial chickens on free-range layer farms (specifically in the Sydney basin region and South East Queensland) in Australia to low pathogenic avian influenza (LPAI) from wild birds.
Node | Branch of node | Parameter estimates | Input values | Data sources |
---|---|---|---|---|
1. Type of wild bird on farm property | Waterfowl |
Proportion of answers from farmers that reported the respective wild bird type on their property ( |
Beta ( |
Scott et al. ( |
2. Prevalence of LPAI in wild birds | Yes |
Probability of the different wild bird types; waterfowl, shorebirds or other, being infected with LPAI of H5 or H7 subtype in winter, summer, and autumn/spring ( |
Beta ( |
Grillo et al. ( |
3. Respective wild bird type has been reported inside chicken sheds | Yes |
Proportion of farms that witnessed the respective wild bird type inside chicken sheds on the farm. The data suggests the probability for waterfowl and shorebirds inside sheds is close to 0 and, therefore, a Pert distribution is used for these wild bird types ( |
Scott et al. ( |
|
4. Respective wild bird type has been reported in other locations on the farm | Waterbodies |
Proportion of answers from farmers that witnessed the respective wild bird type in the respective areas ( |
Beta ( |
Scott et al. ( |
5. Suitable weather conditions for range access | Yes |
Probability that the weather conditions for seasons winter, summer, and autumn/spring are suitable for farmers to allow chickens on the range; when conditions are dry, between 17 and 28 C and there is no severe weather ( |
Beta ( |
Bureau of Meterology ( |
6. Birds are a suitable age for range access | Yes |
Proportion of the chicken’ |
Beta ( |
Scott et al. ( |
7. Birds actually go onto the range | Yes |
Proportion of flock that actually leave shed and use the range as reported by farmers ( |
Average of 25 Beta functions ( |
Scott et al. ( |
8. Aerial transmission of LPAI from wild birds to domestic chickens | Yes |
Probability of LPAI introduction via aerial dispersion from wild birds on waterbodies to chickens on farm ( |
Beta ( |
Jonges et al. ( |
9. Surface water is used for chickens | Yes |
Proportion of answers from farmers that use surface water for the chicken farm ( |
Beta ( |
Scott et al. ( |
10. Locations surface water is used for | Inside shed |
Proportion of answers from farmers that use surface water for inside the shed versus outside the shed ( |
Beta ( |
Scott et al. ( |
11. Water inside chicken sheds is treated | Yes |
Proportion of answers from farmers that treat water inside the chicken sheds ( |
Beta ( |
Scott et al. ( |
12. Water outside chicken sheds is treated | Yes |
Proportion of answers from farmers that treat water used outside the shed ( |
Beta ( |
Scott et al. ( |
13. Chickens have escaped the shed or range area | Yes |
Proportion of farms that have reported chickens unintentionally outside of the shed or range area ( |
Beta ( |
Scott et al. ( |
14. Other indirect routes that can lead to LPAI introduction | Yes |
Probability that chickens will be exposed to LPAI virus via other indirect methods; boots, mice/rats, insects and pets combined into one probability ( |
Scott et al. ( |
Scenario tree representing the exposure of chickens on non-free-range layer farms to low pathogenic avian influenza (LPAI) viruses from wild birds in Australia (
Scenario tree representing the exposure of chickens on non-free-range meat chicken farms to low pathogenic avian influenza (LPAI) viruses from wild birds in Australia (
Scenario tree representing the exposure of chickens on free-range layer and meat chicken farms to low pathogenic avian influenza (LPAI) viruses from wild birds in Australia (
The Advanced Sensitivity Analysis tool of the program @RISK 7.0 (Palisade Corporation, USA) was used to determine the impact of changes in the input parameters on the model outputs.
The effect of the following inputs on exposure were investigated: (1) proportion of waterfowl on property (
The values for the input parameters included in the sensitivity analysis were varied from 0 to 1 in thirds (0, 0.3, 0.6, 1), with 1,000 iterations used for each of the values included, while all other input values were fixed to their base value. The model outputs assessed were the overall probability of exposure to LPAI across the three seasons per farm type.
The probability of a first LPAI exposure to a chicken on a commercial chicken farm being exposed from a wild bird present on the farm at any point in time through the pathways considered in this assessment was estimated to be extremely low for all farm types (Table
Median (5 and 95 percentiles) probabilities of direct and indirect exposure of a chicken on the commercial chicken farm types (non-free-range meat chicken, free-range meat chicken, cage layer, barn layer, free-range layer) to low pathogenic avian influenza (LPAI) viruses for the first time at any point in time from wild birds in Australia (specifically in the Sydney basin bioregion and South East Queensland).
Exposure and farm type | Median | 5% | 95% | |
---|---|---|---|---|
Non-free-range meat chicken | 0.00037 | 0.00020 | 0.00064 | |
Free-range meat chicken | 0.00032 | 0.00018 | 0.00057 | |
Cage layer | 0.00032 | 0.00015 | 0.00063 | |
Barn layer | 0.00030 | 0.00014 | 0.00058 | |
Free-range layer | 0.00075 | 0.00057 | 0.00010 | |
Non-free-range meat chicken | 8.68 × 10−5 | 3.153 × 10−5 | 0.00019 | |
Free-range meat chicken | 0.00016 | 8.45 × 10−5 | 0.00030 | |
Cage layer | 0.00011 | 3.81 × 10−5 | 0.00025 | |
Barn layer | 8.82 × 10−5 | 3.00 × 10−5 | 0.00022 | |
Free-range layer | 0.00056 | 0.00043 | 0.00073 | |
Non-free-range meat chicken | 0.00027 | 0.00014 | 0.00053 | |
Free-range meat chicken | 0.00016 | 5.72 × 10−5 | 0.00036 | |
Cage layer | 0.00020 | 7.76 × 10−5 | 0.00047 | |
Barn layer | 0.00019 | 7.46 × 10−5 | 0.00045 | |
Free-range layer | 0.00017 | 9.38 × 10−5 | 0.00036 | |
Non-free-range meat chicken | 0.00185 | 0.001 | 0.0032 | |
Free-range meat chicken | 0.0016 | 0.0009 | 0.00285 | |
Cage layer | 0.0016 | 0.00075 | 0.00315 | |
Barn layer | 0.0015 | 0.0007 | 0.0029 | |
Free-range layer | 0.00375 | 0.00285 | 0.0005 | |
Non-free-range meat chicken | 0.0037 | 0.002 | 0.0064 | |
Free-range meat chicken | 0.0032 | 0.0018 | 0.0057 | |
Cage layer | 0.0032 | 0.0015 | 0.0063 | |
Barn layer | 0.003 | 0.0014 | 0.0058 | |
Free-range layer | 0.0075 | 0.0057 | 0.001 |
When the type of LPAI exposure was considered, direct exposure had the highest probability of causing first exposure to a domestic chicken among free-range farm types, with the lowest being reported for barn layer farms (Table
To assess the influence of flock size of the farm on the probability of exposure, the overall probability of exposure of each farm type was multiplied by hypothetical numbers of sheds on the property, as each shed can be considered independent in the exposure models. Five and 10 sheds were used, and results are shown in Table
Results from the binomial distributions are shown in Table
Number of low pathogenic avian influenza (LPAI) virus exposures that would occur given a number of wild birds (
Waterfowl proportion | Standard | 100% | 80% | 100% | 50% | 50% | |||||||||||||
---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|
Waterfowl LPAI prevalence | Standard | Standard | 20% | 10% | 20% | 10% | |||||||||||||
Farm type | Number of wild birds | Median | 5% | 95% | Median | 5% | 95% | Median | 5% | 95% | Median | 5% | 95% | Median | 5% | 95% | Median | 5% | 95% |
Non-free-range meat chicken | 10 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 |
50 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 1 | 0 | 0 | 1 | 0 | 0 | 1 | 0 | 0 | 1 | |
100 | 0 | 0 | 0 | 0 | 0 | 1 | 0 | 0 | 1 | 0 | 0 | 1 | 0 | 0 | 1 | 0 | 0 | 1 | |
1,000 | 0 | 0 | 2 | 1 | 0 | 3 | 3 | 0 | 7 | 2 | 0 | 5 | 2 | 0 | 5 | 1 | 0 | 3 | |
Free-range meat chicken | 10 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 |
50 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 1 | 0 | 0 | 1 | 0 | 0 | 1 | 0 | 0 | 0 | |
100 | 0 | 0 | 0 | 0 | 0 | 1 | 0 | 0 | 1 | 0 | 0 | 1 | 0 | 0 | 1 | 0 | 0 | 1 | |
1,000 | 0 | 0 | 1 | 1 | 0 | 3 | 2 | 0 | 7 | 1 | 0 | 5 | 2 | 0 | 5 | 1 | 0 | 3 | |
Cage layer | 10 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 |
50 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 1 | 0 | 0 | 1 | 0 | 0 | 1 | 0 | 0 | 0 | |
100 | 0 | 0 | 0 | 0 | 0 | 1 | 0 | 0 | 1 | 0 | 0 | 1 | 0 | 0 | 1 | 0 | 0 | 1 | |
1,000 | 0 | 0 | 2 | 1 | 0 | 3 | 2 | 0 | 7 | 1 | 0 | 5 | 2 | 0 | 5 | 1 | 0 | 3 | |
Barn layer | 10 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 |
50 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 1 | 0 | 0 | 1 | 0 | 0 | 1 | 0 | 0 | 0 | |
100 | 0 | 0 | 0 | 0 | 0 | 1 | 0 | 0 | 1 | 0 | 0 | 1 | 0 | 0 | 1 | 0 | 0 | 1 | |
1,000 | 0 | 0 | 1 | 1 | 0 | 3 | 2 | 0 | 7 | 1 | 0 | 5 | 1 | 0 | 5 | 1 | 0 | 3 | |
Free-range layer | 10 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 1 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 |
50 | 0 | 0 | 0 | 0 | 0 | 1 | 0 | 0 | 1 | 0 | 0 | 1 | 0 | 0 | 1 | 0 | 0 | 1 | |
100 | 0 | 0 | 1 | 0 | 0 | 1 | 0 | 0 | 2 | 0 | 0 | 2 | 0 | 0 | 2 | 0 | 0 | 1 | |
1,000 | 1 | 0 | 2 | 2 | 0 | 5 | 6 | 2 | 11 | 4 | 1 | 8 | 4 | 1 | 8 | 2 | 0 | 5 |
Number of low pathogenic avian influenza (LPAI) virus exposures that would occur given a number of wild birds (
The number of exposures was assessed by changing the proportion of wild birds that are waterfowl and the LPAI prevalence of waterfowl, with some scenarios representing worst-case scenarios (with high proportion of waterfowl present among the wild birds on farm and with elevated LPAI prevalence among the wild birds on farm). Waterfowl may make up a considerable proportion of wild birds on the property during specific events such as drought and, similarly, the prevalence of LPAI in waterfowl may increase with population dynamics, such as an increase in immune-naive juvenile birds. The impact of these scenarios on the number of expected exposures is shown in Table
The estimated probabilities of a chicken on commercial chicken farms being exposed to LPAI virus from wild birds at any point in time during the three seasons previously defined (winter, autumn/spring, and summer) are summarized in Table
Median (5 and 95 percentiles) overall probabilities of exposure (direct and indirect) of a chicken on the commercial chicken farm types (non-free-range meat chicken, free-range meat chicken, cage layer, barn layer, free-range layer) to low pathogenic avian influenza (LPAI) viruses for the first time at any point in time during the three defined seasons; winter (June–August); summer (December–February); and autumn and spring (March–May and September–November); from wild birds in Australia (specifically in the Sydney basin bioregion and South East Queensland).
Farm type | Median | 5% | 95% | |
---|---|---|---|---|
Non-free-range meat chicken | 0.00044 | 0.00024 | 0.00079 | |
Free-range meat chicken | 0.00039 | 0.00022 | 0.00068 | |
Cage layer | 0.00038 | 0.00017 | 0.00077 | |
Barn layer | 0.00035 | 0.00016 | 0.00070 | |
Free-range layer | 0.00102 | 0.00076 | 0.0014 | |
Non-free-range meat chicken | 0.00019 | 0.00010 | 0.00034 | |
Free-range meat chicken | 0.00018 | 9.06 × 10−5 | 0.00035 | |
Cage layer | 0.00018 | 8.09 × 10−5 | 0.00036 | |
Barn layer | 0.00017 | 7.56 × 10−5 | 0.00033 | |
Free-range layer | 0.00030 | 0.00020 | 0.00049 | |
Non-free-range meat chicken | 0.00046 | 0.00026 | 0.00082 | |
Free-range meat chicken | 0.00039 | 0.00023 | 0.00069 | |
Cage layer | 0.00040 | 0.00018 | 0.00079 | |
Barn layer | 0.00036 | 0.00017 | 0.00072 | |
Free-range layer | 0.00093 | 0.00069 | 0.0012 |
According to the exposure sensitivity analysis, the most influential parameters were the proportion of waterfowl among wild birds on the property and the probability of waterfowl being on the feed storage areas (Figure
Results of the sensitivity analysis on the exposure assessment depicting the change in probability (
Sensitivity analysis on the prevalence of LPAI in waterfowl was also conducted separately as this parameter has a profound influence on the probability of LPAI exposure. It was found from the sensitivity analysis there is an approximate threefold to fourfold increase in the probability of LPAI exposure across the farm types when the LPAI prevalence in wild waterfowl is increased to 20%.
This study comparatively estimates the probability of a first exposure of a chicken to LPAI viruses from wild birds present on different types of commercial chicken enterprises in Australia. The probabilities estimated in this study can be considered representative for the Sydney basin region as weather information and the majority of on-farm surveys conducted are specific to this region. In addition, all of the LPAI wild bird prevalence data used in this study was from the Sydney basin region, where most samples were collected from the Lower Hunter region which was considered part of the Sydney basin region in the survey by Scott et al. (
The probabilities of exposure estimated in this study apply to commercial chicken farms according to the definition implemented in the on-farm survey conducted by Scott et al. (
Overall, the probability of a first exposure to LPAI from wild birds at any point in time is extremely low for all farm types; however, the highest probability of exposure is seen among free-range layer farms, with this probability being over two times higher than for the other farm types. These results are in agreement with a study conducted by Gonzales et al. (
There have been a total of 15 confirmed LPAI cases in Australian poultry since 1976 (
To best validate these models, routine sampling of Australian commercial chicken farms for LPAI should be conducted. According to the Australian Veterinary Emergency Plan for AI (
The differences in the probability of direct and indirect exposure between free-range and non-free-range farms are likely due to the definitions of exposures types used in this model. Direct exposure is more likely to occur when chickens have access to the outdoors and, as such, exposure to the virus in non-free-range farms is more likely to occur through indirect pathways. Biosecurity refers to actions to prevent the introduction and spread of infectious agents. In relation to poultry enterprises this refers to practices, such as the use of foot baths, treatment of water, disinfection of equipment between sheds, and vermin control (
Another major introduction route implicated for LPAI is the contamination of drinking water for chickens with infective wild bird feces. At least half of all Australian HPAI outbreaks so far are likely to have been associated with the introduction of LPAI
The exposure sensitivity analysis revealed that the most influential parameters were related to waterfowl presence on the farm; particularly the proportion of waterfowl among wild birds on the property, waterfowl around feed storage areas, and waterfowl on the range. Waterfowl on waterbodies was not a highly influential parameter due to the high proportion of farms that treat surface water, as previously mentioned, and the low probability of aerosol transmission of LPAI from wild waterfowl on waterbodies to commercial chickens (
In addition to the presence of waterfowl in different areas of the farm, the actual number of waterfowl present as well as the prevalence of LPAI in waterfowl are highly influential on the potential number of exposures occurring. The 1994 H7N2 outbreak in Lowood, Queensland is a classic example of both Australian waterfowl movements and the impact of the number of waterfowl in a property. The outbreak occurred during severe drought and a river that constituted one border for the farm as well as a small dam near the entrance of the chicken sheds had attracted a large population of wild birds prior to the subsequent outbreak. LPAI was speculated to be introduced to the flock through contaminated drinking water (
The probability of the first exposure to LPAI virus for a chicken on an Australian commercial chicken farm was found to be lowest in summer for all farm types. The highest probability was estimated to be in winter for chickens on free-range layer farms and autumn/spring for the rest of the farms, except for free-range meat chicken farms which reported no difference between winter and autumn/spring. However, there were minor differences in the probabilities of exposure for all farm types between winter and autumn/spring overall. Among previous HPAI outbreaks in Australia, one occurred in winter (July), four in autumn and spring (May, October, and November), and two in summer (December and January). The three latest outbreaks that occurred in Tamworth (1997), Maitland (2012), and Young (2013) occurred in October or November (
The seasonal variations in the probability of exposure are influenced by the wild bird LPAI prevalence data and the guidelines on outside weather conditions that determine whether or not chickens are provided access to the range. The overall prevalence of LPAI in Australian wild waterfowl at any point in time is approximately 2.5%. Seasonal effects on the prevalence of LPAI in wild birds within NSW do not appear to fluctuate as greatly as in the northern hemisphere (
Birds in the families Scolopacidae and Charadriidae (shorebirds and waders) do undergo annual migrations over long distances and visit Australasia (
There are still many uncertainties related to the mechanisms of the LPAI virus introduction and exposure, particularly in Australian commercial chicken farm settings. However, the results of this study have used the best data available at this time. The results suggest that chickens on commercial free-range layer farms have approximately double the risk of LPAI exposure compared to other farm types. The probability of direct exposure is also more likely in both free-range layer and meat chicken farms compared to the other farm types. Moreover, the probability of LPAI exposure seems to be lower in summer compared to all other seasons and this is influenced by the prevalence of LPAI in wild birds and the weather conditions in which free-range chickens are allowed to go on the range. The proportion of waterfowl on the farm and the presence of waterfowl on the range and feed storage areas are the most influential parameters on the probability of exposure. These results highlight the importance of good biosecurity on farms, providing insight regarding the on-farm actions that can reduce the risk of LPAI exposure such as those related to waterfowl deterrence. In addition, the importance of continuous surveillance of Australian wild bird populations to monitor LPAI prevalence and subtypes is highlighted, as this can help predict future introductions and outbreaks. The need of further research in AI virus properties, particularly in an Australian context is also highlighted.
This study was carried out in accordance with the recommendations of the Human Ethics Committee of the University of Sydney, Australia with written informed consent from all subjects. The protocol was approved by the Human Ethics Committee of the University of Sydney, Australia (ethics reference number: 2015/252).
The first author ABS was involved in investigation, methodology, writing of the original draft, and reviewing and editing. J-AT formed initial conceptualization of the study, and was involved in formal analysis, methodology, project administration, supervision of ABS, and reviewing and editing the manuscript. MS was also involved in investigation, methodology, project administration, supervision of ABS, and reviewing and editing the manuscript. BB and KG were also involved in initial conceptualization of the study, formal analysis, methodology, and provided reviewing and editing. BM, AB, and PG were involved in conceptualization and project administration funding/support of the study. PG also provided methodology and supervision. BM provided reviewing and editing. MH-J was heavily involved in formal analysis of the results, conceptualization of the study, methodology, project administration, supervision of ABS, and reviewing and editing the manuscript.
The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
The authors extend thanks to the New South Wales Department of Primary Industries, the University of Newcastle and the National Avian Influenza Wild Birds Surveillance Program, which is funded by the Australian Government Department of Agriculture and Water Resources and is administered by Wildlife Health Australia, for their collaboration in providing wild bird LPAI virus prevalence data that were used in the exposure model. Egg and chicken meat companies and producers are also appreciated by the authors for their participation in the farm survey. This research was conducted within the Poultry Cooperative Research Centre (CRC) with support from the CRC and Woolworths Limited. The first author is also a recipient of a Post-graduate Scholarship from the Poultry CRC.
The Supplementary Material for this article can be found online at