Economic evaluation of low pathogenic avian influenza in northeastern US live bird markets

Economic evaluation of low pathogenic avian influenza in northeastern US live bird markets Abstract Avian influenza in domestic poultry can have varied impacts on the health and welfare of birds and an economic burden on producers, consumers, and animal health agencies including the cost to control and eradicate avian influenza. Low pathogenic avian influenza has historically been a recurring issue in U.S. live bird markets, but rarely studied. Live bird markets source various species of birds and mammals from a variety of wholesalers and sell either live animals or freshly harvested animals. Using cost estimates from the 2016 outbreak of low pathogenic avian influenza in northeastern U.S. live bird markets, estimates of the mean per market costs were calculated for responding government agencies ($804) and the market itself ($3,997), including traceback investigation, testing costs, and cleaning and disinfection. The economic impact also included market impacts which the majority are affected by income that the live bird markets forego during cleaning and disinfection ($3,998 per market) with an expected shutdown of 3–5d. Animal health agencies' responses to a disease depend on the established disease response and resources, such as labor and funding. Understanding the economic costs of disease management improves the decision-making process for these agencies and markets as a whole to limit disease introduction, spread, longevity, and market impacts through business disruptions and foregone income. DESCRIPTION OF PROBLEM Animal disease events can cause economic disruptions in production, marketing, and distribution of animal products depending on the pathogenicity of the strain and the type of bird affected [1]. These costs are born by the supply chain, including producers, wholesalers, and the final retail markets. Additionally, the cost to respond and manage a disease event is borne by government animal health agencies [2]. Relative to the size of the market, these costs can be substantial. There have been no recently published works that have estimated the costs of low pathogenic avian influenza (LPAI) outbreaks on a live bird market (LBM) in the United States. This work aims to provide market participants, policy makers, and responders with estimates of the cost of response and the economic impact on the affected markets. Low pathogenic avian influenza is a disease reportable to the World Organization for Animal Health for H5 and H7 virus subtypes [3]. Low pathogenic avian influenza may cause no, to relatively mild clinical signs, where these clinical signs can be more severe depending on additional, exacerbating infection and environmental conditions [3]. However, H5 and H7 virus subtyped LPAI can pose a risk of mutating into a highly pathogenic avian influenza, which spreads rapidly and causes mortality rates above 75% [3]. Low pathogenic avian influenza has historically been a recurring issue in LBMs in the United States [4]. US LBMs use a schedule of cleaning and disinfecting at the market level and continued testing protocols for disease surveillance in order to prove disease-free status and reduce risk of disease exposure and transmission as proscribed by their respective animal health agencies. Using cost estimates from state-level animal health officials for the 2016 LPAI event in New England LBMs, an estimate of the response cost of an outbreak of LPAI was calculated. Accounting for these costs allows for a deeper understanding of the value of preventative measures and the overall cost of response to government agencies and LBMs. Live Bird Markets in the United States Live bird markets are found in many areas around the United States for customers with diverse cultural, ethnic, and religious backgrounds. In states where it is legal, animals may be purchased to be slaughtered at home or be freshly slaughtered at these facilities. Markets may adhere to certain religious slaughter practices (e.g., halal or kosher) or may cater to customer demand for product freshness [5]. Live bird markets are less common in the United States than in many countries around the world and may be considered niche or nontraditional marketing channels for poultry, including chickens, turkeys, geese, and ducks. These markets must meet US Department of Agriculture–Food Safety and Inspection Service sanitation requirements to operate as well as oversight by other regulatory agencies, such as the local health department, State Department of Agriculture, and US Department of Agriculture–Veterinary Services [6]. These requirements include cleaning and disinfection schedules, potential down time periods, or other local, regional, or state level requirements. US Department of Agricultures’ National Animal Health Monitoring System surveyed LBMs in reference to their management practices. From this, we know that LBMs are typically open 6–7 d a week depending on regional market norms and demand [7]. Depending on geographic location of the market, LBMs can have different market sizes or operation practices. Northern LBMs, as defined by the USDA study, typically sell more than 1,000 birds per week, whereas more than half the southern LBMs sell fewer than 500 birds per week where northern markets are represented by New York, New Jersey, New England, Pennsylvania and southern markets by California, Florida, and Texas [7]. These markets are diverse in the types of poultry and other animals sold at the market. In addition to chickens, an overwhelming majority of the northern LBMs carry ducks and guinea fowl—89% and 91%, respectively as well as other poultry including quail, chukar partridges, turkeys, and other gamefowl [7]. These markets tend to also carry other animals such as rabbits (67% of markets), sheep (21%), goats (24%), and cattle (8%) [7]. These animals can be kept indoors, outdoors, or a combination of the 2. For further reading on practices in LBMs see the Poultry 2004 report on live-poultry markets in the United States [7]. Low Pathogenic Avian Influenza in US LBMs Live bird markets in the United States have a history of LPAI market disruptions [4,8,9]. In the early 2000s, LBMs in the northeast were plagued by persistent and increasing numbers of LPAI H5- and H7-positive markets [4]. Increased state regulatory efforts and coordination with market operators and the US Department of Agriculture led to system-wide closure of all LBMs in the northeast United States including New York, New Jersey, Pennsylvania, Massachusetts, Connecticut, and Rhode Island [4]. Intensive cleaning and disinfection of all markets was accomplished during a 3-day, poultry-free closure period. This coordinated market closure resulted in a drastic reduction in the presence of LPAI [10]. This success led to changes in coordinated efforts by participating states in monitoring and testing for avian influenza. In 2016, New England LBMs were found to again be infected with LPAI [8]. Below is a summary of a report of the event by Fox [8]; for more detailed information see the full report. In total, the outbreak affected 105 LBMs in the northeast United States [8]. In late June and early July 2016, routine surveillance samples from an LBM in Pennsylvania were collected, tested, and found to be positive for LPAI H5 by the National Veterinary Services Laboratories [8]. During the same period, an LBM in New York was also found to be positive with LPAI H5. These 2 premises were linked by a common distributor [8]. Tracing shipments from the common distributor found movement of Muscovy ducks to markets in Pennsylvania, New York, and New Jersey [8]. The response to disease in these markets was managed by their respective state animal health agencies, and markets were cleared after each LBM was cleaned and disinfected and environmental samples tested negative. Below is a brief overview of each state's approach to LPAI management. In terms of international trade restrictions, there were market restrictions as a holdover from the 2015 HPAI outbreak in US commercial poultry. There were no additional negative trade impacts in LBMs due to this 2016 LPAI outbreak. Pennsylvania animal health officials depopulated the premises known to be infected, including chickens, guineas, and Muscovy ducks, and provided compensation to affected markets [8]. These carcasses were disposed of by commercial incineration [8]. Additional LBMs from the common distributor were quarantined and required to sell down stocks of birds within 3 d; no live birds were permitted to leave the market [8]. Each market was required to undergo cleaning and disinfecting before obtaining regulatory approval of all cleaning results and negative environmental sample test results for LPAI prior to being released from quarantine [8]. New York required all 58 LBMs that received products from the distributor (7 were confirmed positive for LPAI H5) to be cleaned and disinfected [8]. Positive markets were quarantined and had a 5-day period to sell down animals followed by depopulation of remaining animals and cleaning and disinfecting [8]. New Jersey tested all 37 LBMs whether they received animals from the common distributor or not [8]. Ten markets were confirmed positive with LPAI [8]. Animals were sold down through marketing channels [8]. New Jersey LBMs were quarantined and required to clean the facilities, after which New Jersey animal health personnel disinfected premises and collected environmental samples prior to granting approval to restock the market [8]. MATERIALS AND METHODS To estimate the economic costs for control and eradication of LPAI in LBMs, costs associated with disease response and management were accounted for using expenses associated with the 2016 LPAI event in New England LBMs, including the cost to monitor, test, clean, and disinfect facilities and any bird depopulation, and other associated management costs. Each of these costs was assigned to a payee. For this work, costs associated with government animal health officials were assigned as government costs. A separate estimate of the impact on market participants was provided and included additional cleaning and disinfecting costs as well as forgone income during an LPAI outbreak. Each state responds to LPAI uniquely, expending state-specific hours and labor costs. To maintain protection of proprietary data for participating states, these state-specific values were not reported in this work. These specific costs were used in differentiating and establishing the types of practices, the number of associated hours, and in calculating average cost per unit for disease management. Total costs were assessed based on assumed average inventory for an LBM. Assumptions There were several assumptions made to estimate the cost of LPAI in LBMs. These are presented below. The average number of birds in a northeastern LBM used in the analysis was a weighted mean of 650 birds, calculated from a range of 500–800 birds based on USDA reporting and elicited expert opinion [7]. Cleaning and disinfecting costs were borne by the LBM and were not included in the cost of government response. Some states required that disinfection of LBMs be performed by animal health officials, but for consistency with reported costs and uniformity in this work, the costs to clean and disinfect were considered costs associated with the markets. All values presented were calculated means reported by animal health agencies, as were the number of disease tests and labor hours. The reported tests included a mixture of poultry and environmental tests. The cost per test varied by type and by reporting state. These costs have been averaged for conformity of tests per market and for reporter anonymity. Market impacts were based on USDA–Animal and Plant Health Inspection Services appraisal values for specialty birds. While LBMs carried a mixture of types of poultry, the reported value was an average value of replacement adult specialty breed chickens. The cost of cleaning and disinfecting by the LBM was based on an expected cumulative 8-h work day by 2 employees with minimal cost of material. Government Cost Calculations To estimate the costs of a disease outbreak, the averaged costs and quantities were applied to a cost equation expressed as follows: \begin{eqnarray} {\rm{Average}}\ {\rm{Cost\ }} = \frac{1}{n}\ \mathop \sum \limits_{i\ = \ 1}^n \big( {\rm{Test}}{{\rm{s}}_i} + {\rm{Ve}}{{\rm{t}}_i}\nonumber\\ + {\rm{Inspec}}{{\rm{t}}_i} + {\rm{La}}{{\rm{b}}_i} + {\rm{Manag}}{{\rm{e}}_i} \big) \end{eqnarray} (1) where the average cost of disease management per LBM, i, was a function of the costs of all disease sampling/testing (Tests), veterinary services—services provided by state veterinarians—(Vet), animal health inspections (Inspect), laboratory services outside of testing including salary and processing of results (Lab), and additional labor and management (Manage) per LBM divided by the number of markets, n. The cost for a specific type of LBM and the respective management employed was dependent on location, type of animals sold, and the state animal health authority's management decisions. The values presented represent average costs and quantities across reported and elicited values and can be used in calculating an approximate cost for response. Market Impact Estimation A conservative estimate of the average impact to a LBM was calculated using the following: \begin{eqnarray} {\rm{Impact}}\ &=& \ \sum \big( {\rm{Income}} + {\rm{Cleaning}}\nonumber\\ && + {\rm{Disinfection}} + {\rm{Supplies}} \big)\end{eqnarray} (2) where the estimated economic impact of LPAI for an LBM, i, was a function of the average forgone income (Income), cost for cleaning labor (Cleaning), cost for disinfecting labor (Disinfecting), and the price of supplies used for cleaning and disinfecting (Supplies) on average per LBM. The values presented represented average costs and quantities across reported and elicited values and could be used in calculating an approximate cost for response. Labor values, which do not consider foregone income by employees, were assumed to be an average minimum wage—$8.46 for the tristate study region [11]. RESULTS AND DISCUSSION Costs associated with government LPAI management in LBMs and the economic impact to LBMs are presented in Table 1. Due to confidentiality, we are unable to provide ranges, medians, maximums, or minimums. The table provides the average cost per unit, average number of units, and total cost per LBM for response, where 650 birds were assumed per LBM. The reported economic impact also accounted for forgone income and the cost to the LBM for cleaning and disinfecting. This allowed for individualization of costs to be quickly estimated. The use of actual reported costs by individual state Departments of Agriculture provides realistic estimations and projected costs of future events which can be useful to markets and responding agencies in understanding the true economic impact of LPAI outbreak in LBMs. Table 1. Average costs associated with government LPAI management for affected live bird markets and economic impact to live bird markets. Units Price per unit Quantity Cost per live bird market Disease testing Samples $38.36 10.4 $399 Inspection Hours $34.91 4.9 $171 Laboratory services Hours $21.82 2.8 $61 Management Hours $37.31 2.7 $100 Veterinary services Hours $55.14 1.3 $73 Total government response per market $804 Forgone income Bird $9.65 650 $3,860 Cleaning and disinfecting Market $137.91 1 $137 Total impact per live bird market $3,997 Units Price per unit Quantity Cost per live bird market Disease testing Samples $38.36 10.4 $399 Inspection Hours $34.91 4.9 $171 Laboratory services Hours $21.82 2.8 $61 Management Hours $37.31 2.7 $100 Veterinary services Hours $55.14 1.3 $73 Total government response per market $804 Forgone income Bird $9.65 650 $3,860 Cleaning and disinfecting Market $137.91 1 $137 Total impact per live bird market $3,997 View Large Table 1. Average costs associated with government LPAI management for affected live bird markets and economic impact to live bird markets. Units Price per unit Quantity Cost per live bird market Disease testing Samples $38.36 10.4 $399 Inspection Hours $34.91 4.9 $171 Laboratory services Hours $21.82 2.8 $61 Management Hours $37.31 2.7 $100 Veterinary services Hours $55.14 1.3 $73 Total government response per market $804 Forgone income Bird $9.65 650 $3,860 Cleaning and disinfecting Market $137.91 1 $137 Total impact per live bird market $3,997 Units Price per unit Quantity Cost per live bird market Disease testing Samples $38.36 10.4 $399 Inspection Hours $34.91 4.9 $171 Laboratory services Hours $21.82 2.8 $61 Management Hours $37.31 2.7 $100 Veterinary services Hours $55.14 1.3 $73 Total government response per market $804 Forgone income Bird $9.65 650 $3,860 Cleaning and disinfecting Market $137.91 1 $137 Total impact per live bird market $3,997 View Large During an LPAI outbreak, there are several costs associated with containment and eradication, including testing, inspection, laboratory services, management, and veterinary services. The total per-market cost for government response was estimated to be $804, or $1.24 on a per-bird basis. Relative to the other associated costs, disease tests were by far the greatest, and most necessary expense to facilitate approval for markets to reopen. These tests included those run during the outbreak and 3 mo of follow-up testing. Testing for LPAI in a market involves several different types of bird and environmental tests. There were, on average, 10.4 disease tests per LBM with an average cost of $38.36 per test, or $399 per LBM over a 4-mo period. The other 4 categories included the increased labor and management in managing LPAI. In addition to the monetary costs, there are increased time demands for animal health inspectors and veterinarians which can be taxing on agencies during an outbreak and for follow-up testing. On average, animal health inspectors spend 4.9 additional hours and veterinary services spend 1.3 additional hours per LBM during an outbreak. Similarly, there is an increase in management needs which includes general disease management, reporting, travel, and other miscellaneous facets outside the direct categories. For a state with 10 LBMs, an outbreak of LPAI can lead to an average increase in labor demand of 117 h. The data collected for these estimates coincided with a relatively short time frame from detection to reopening markets, a period of time that was 2 wk or less. While the range in the increase in the number of personnel hours may fluctuate, using these estimates, an LPAI outbreak in an LBM requires the equivalent of a full-time employee over the course of 2 wk. This perspective may help agencies and markets understand the increased cost and labor demand associated with an outbreak. An estimate for the average forgone income for birds in an LBM was estimated to be $3,860, assuming normal daily sales of 100 birds per day and an average closure of 3–5 d. There are many factors that can affect this forgone market income, including reduced pricing to move birds during the sell down period, length of market closure, or time it takes to clean and disinfect the market. During an outbreak, these values are subject to change to reflect regional and other market prices, as well as to reflect a more accurate breakout of the types of poultry housed at the LBM. The range of forgone income estimated was between $2,895 and $4,825. There may be additional losses in markets that sell their inventory prior to shut down, potentially at reduced prices, as markets tend to be permitted to sell down inventory prior to cleaning and disinfecting. Markets may reduce prices to sell birds rather than depopulate their inventory and there may be changes in customer purchasing patterns due to availability of product. While there are no estimates of the effects of the changes in prices included in this analysis, it should be noted that this would mean additional forgone income to the LBMs, leading to greater impacts on the markets. Total Costs The costs and estimated losses above were presented at the market level. Using these market-level costs and economic impacts, an estimate for the total cost of an outbreak can be assessed. Below is an estimate for the June 2016 outbreak of LPAI in northeast LBMs. The total government cost and total market impacts are presented in Table 2, which was based on 105 affected markets (37 from New Jersey, 58 from New York, and 10 from Pennsylvania). Table 2. Total estimated cost breakout for 2016 low pathogenic avian influenza in live bird markets. Estimated costs Percent of estimated total costs Disease testing $41,886 50% Inspection $17,904 21% Management $10,535 12% Veterinary services $7,669 9% Laboratory services $6,376 8% Total government costs $84,370 100% Forgone income $4,05,300 97% Cleaning and disinfecting $14,481 3% Total live bird market costs $4,19,781 100% Estimated costs Percent of estimated total costs Disease testing $41,886 50% Inspection $17,904 21% Management $10,535 12% Veterinary services $7,669 9% Laboratory services $6,376 8% Total government costs $84,370 100% Forgone income $4,05,300 97% Cleaning and disinfecting $14,481 3% Total live bird market costs $4,19,781 100% View Large Table 2. Total estimated cost breakout for 2016 low pathogenic avian influenza in live bird markets. Estimated costs Percent of estimated total costs Disease testing $41,886 50% Inspection $17,904 21% Management $10,535 12% Veterinary services $7,669 9% Laboratory services $6,376 8% Total government costs $84,370 100% Forgone income $4,05,300 97% Cleaning and disinfecting $14,481 3% Total live bird market costs $4,19,781 100% Estimated costs Percent of estimated total costs Disease testing $41,886 50% Inspection $17,904 21% Management $10,535 12% Veterinary services $7,669 9% Laboratory services $6,376 8% Total government costs $84,370 100% Forgone income $4,05,300 97% Cleaning and disinfecting $14,481 3% Total live bird market costs $4,19,781 100% View Large Total government costs were estimated to be $84,370. Disease testing accounted for the largest percentage (50%) of government expenses and the greatest contribution ($41,886) to the government's total. The number of tests for all markets was based on the average number of samples collected at each LBM as a proxy for the actual number of tests and samples taken per market. The remaining 50% of the government costs were broken down into inspection (21%), management (12%), veterinary services (9%), and laboratory services time (8%), totaling $42,485. For an extended or persistent outbreak, that estimate could substantially increase, emphasizing the importance of early detection and thorough cleaning and disinfecting. The total market impact, in terms of forgone income and direct cleaning and disinfecting costs, was estimated to be $4,19,781. The overwhelming majority (97%) was forgone income with only 3% coming from cleaning and disinfecting. This foregone income represented lost revenue from closing the market for cleaning and disinfecting prior to clearance by state animal health officials. For these markets, this loss represented financial incentives to reduce the incidence of LPAI, to maintain biosecurity measures to mitigate risk of contracting disease, and to efficiently clean and disinfect as quickly as possible to reduce the time of forced closure. Understanding the costs associated with an outbreak can help provide context for changes in the decision-making of normal business to reduce disease introduction and management of LBMs during an outbreak to shorten the market closures and limit foregone income. CONCLUSIONS AND APPLICATIONS Using reported and elicited values for the 2016 outbreak of LPAI H5 in New Jersey, New York, and Pennsylvania LBMs, the estimated cost of LPAI was $84,370. The LBMs were also affected by business disruptions due to cleaning and disinfecting protocols that forced closure of the market, and the economic loss was estimated to be $4,19,781 for all affected markets, or $3,998 per market. While prevention of a disease outbreak is favorable, these estimates provide an understanding of the costs associated with an outbreak in both value and additional labor demands. Footnotes Primary Audience: Poultry Health Researchers, Poultry Veterinarians, Public Health Officials, Economists REFERENCES 1. Alexander D. J. 2000 . A review of avian influenza in different bird species . Vet. Microbiol. 74 : 3 – 13 . Google Scholar CrossRef Search ADS PubMed 2. Johansson R. C. , Preston W. P. , Seitzinger A. H. . 2016 . Government spending to control highly pathogenic avian influenza . Choices 31 . 3. World Organisation for Animal Health (OIE) . 2015 . Avian Influenza (Infection with Avian Influenza Viruses) . OIE Terrestrial Manual 2015, chapter 2.3.4 . World Organisation for Animal Health , Paris, France . 4. Mullaney R. 2003 . Live-bird market closure activities in the northeastern United States . Avian Dis. 47 ( s3 ): 1096 – 1098 . Google Scholar CrossRef Search ADS PubMed 5. Croghan L. , Lee P. . Farm's freshest: New York's live markets sell chickens, goats and rabbits . NY Daily News. Accessed 5 Apr. 2017. http://www.nydailynews.com/life-style/eats/new-york-live-markets-sell-chickens-goats-rabbits-customers-freshest-article-1.132070 . 6. Centers for Disease Control and Prevention (CDC) . 2016 . Live Animal & Bird Markets . Centers for Disease Control and Prevention . Accessed 6 June 2017. http://www.cdc.gov/features/liveanimalbird/index.html . 7. U. S. Department of Agriculture . 2004 . Part III: Reference of Management Practices in Live-Poultry Markets in the United States . National Animal Health Monitoring System , Fort Collins, CO . 8. Fox P. 2016 . Live Bird Marketing System Working Group Report Update . Accessed 5 Apr. 2016. http://www.usaha.org/transmissible-diseases-of-poultry-avian-species . 9. Yee K. S. , Carpenter T. E. , Mize S. , Cardona C.J. . 2008 . The live bird market system and low-pathogenic avian influenza prevention in Southern California . Avian Dis. 52 : 348 – 352 . Google Scholar CrossRef Search ADS PubMed 10. Senne D. A. , Pedersen J. C. , Panigrahy B. . 2003 . Live-bird markets in the Northeastern United States: a source of avian influenza in commercial poultry . Pages 19–24 in Proc. of the Frontis Workshop on Avian Influenza: Prevention and Control . Springer , Netherlands . Google Scholar CrossRef Search ADS 11. U. S. Department of Labor . 2017 . Minimum Wage Laws in the States . Wage and Hour Division . Accessed 5 Jan. 2017. https://www.dol.gov/whd/minwage/america.htm . PubMed PubMed Acknowledgments This work would not have been possible without the support and collaboration of state animal health officials in New Jersey, New York, and Pennsylvania. A special acknowledgment goes to Nicole Lewis for her dedication to the project and for organizing the group communications. The authors would also like to thank Lindsey Garber and all the other reviewers for their helpful comments and insights. Funding support was provided by the US Department of Agriculture under Cooperative Agreement 16-9220-0455-CA. Published by Oxford University Press on behalf of Poultry Science Association 2018. This work is written by (a) US Government employee(s) and is in the public domain in the US. http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Journal of Applied Poultry Research Oxford University Press

Economic evaluation of low pathogenic avian influenza in northeastern US live bird markets

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Abstract

Abstract Avian influenza in domestic poultry can have varied impacts on the health and welfare of birds and an economic burden on producers, consumers, and animal health agencies including the cost to control and eradicate avian influenza. Low pathogenic avian influenza has historically been a recurring issue in U.S. live bird markets, but rarely studied. Live bird markets source various species of birds and mammals from a variety of wholesalers and sell either live animals or freshly harvested animals. Using cost estimates from the 2016 outbreak of low pathogenic avian influenza in northeastern U.S. live bird markets, estimates of the mean per market costs were calculated for responding government agencies ($804) and the market itself ($3,997), including traceback investigation, testing costs, and cleaning and disinfection. The economic impact also included market impacts which the majority are affected by income that the live bird markets forego during cleaning and disinfection ($3,998 per market) with an expected shutdown of 3–5d. Animal health agencies' responses to a disease depend on the established disease response and resources, such as labor and funding. Understanding the economic costs of disease management improves the decision-making process for these agencies and markets as a whole to limit disease introduction, spread, longevity, and market impacts through business disruptions and foregone income. DESCRIPTION OF PROBLEM Animal disease events can cause economic disruptions in production, marketing, and distribution of animal products depending on the pathogenicity of the strain and the type of bird affected [1]. These costs are born by the supply chain, including producers, wholesalers, and the final retail markets. Additionally, the cost to respond and manage a disease event is borne by government animal health agencies [2]. Relative to the size of the market, these costs can be substantial. There have been no recently published works that have estimated the costs of low pathogenic avian influenza (LPAI) outbreaks on a live bird market (LBM) in the United States. This work aims to provide market participants, policy makers, and responders with estimates of the cost of response and the economic impact on the affected markets. Low pathogenic avian influenza is a disease reportable to the World Organization for Animal Health for H5 and H7 virus subtypes [3]. Low pathogenic avian influenza may cause no, to relatively mild clinical signs, where these clinical signs can be more severe depending on additional, exacerbating infection and environmental conditions [3]. However, H5 and H7 virus subtyped LPAI can pose a risk of mutating into a highly pathogenic avian influenza, which spreads rapidly and causes mortality rates above 75% [3]. Low pathogenic avian influenza has historically been a recurring issue in LBMs in the United States [4]. US LBMs use a schedule of cleaning and disinfecting at the market level and continued testing protocols for disease surveillance in order to prove disease-free status and reduce risk of disease exposure and transmission as proscribed by their respective animal health agencies. Using cost estimates from state-level animal health officials for the 2016 LPAI event in New England LBMs, an estimate of the response cost of an outbreak of LPAI was calculated. Accounting for these costs allows for a deeper understanding of the value of preventative measures and the overall cost of response to government agencies and LBMs. Live Bird Markets in the United States Live bird markets are found in many areas around the United States for customers with diverse cultural, ethnic, and religious backgrounds. In states where it is legal, animals may be purchased to be slaughtered at home or be freshly slaughtered at these facilities. Markets may adhere to certain religious slaughter practices (e.g., halal or kosher) or may cater to customer demand for product freshness [5]. Live bird markets are less common in the United States than in many countries around the world and may be considered niche or nontraditional marketing channels for poultry, including chickens, turkeys, geese, and ducks. These markets must meet US Department of Agriculture–Food Safety and Inspection Service sanitation requirements to operate as well as oversight by other regulatory agencies, such as the local health department, State Department of Agriculture, and US Department of Agriculture–Veterinary Services [6]. These requirements include cleaning and disinfection schedules, potential down time periods, or other local, regional, or state level requirements. US Department of Agricultures’ National Animal Health Monitoring System surveyed LBMs in reference to their management practices. From this, we know that LBMs are typically open 6–7 d a week depending on regional market norms and demand [7]. Depending on geographic location of the market, LBMs can have different market sizes or operation practices. Northern LBMs, as defined by the USDA study, typically sell more than 1,000 birds per week, whereas more than half the southern LBMs sell fewer than 500 birds per week where northern markets are represented by New York, New Jersey, New England, Pennsylvania and southern markets by California, Florida, and Texas [7]. These markets are diverse in the types of poultry and other animals sold at the market. In addition to chickens, an overwhelming majority of the northern LBMs carry ducks and guinea fowl—89% and 91%, respectively as well as other poultry including quail, chukar partridges, turkeys, and other gamefowl [7]. These markets tend to also carry other animals such as rabbits (67% of markets), sheep (21%), goats (24%), and cattle (8%) [7]. These animals can be kept indoors, outdoors, or a combination of the 2. For further reading on practices in LBMs see the Poultry 2004 report on live-poultry markets in the United States [7]. Low Pathogenic Avian Influenza in US LBMs Live bird markets in the United States have a history of LPAI market disruptions [4,8,9]. In the early 2000s, LBMs in the northeast were plagued by persistent and increasing numbers of LPAI H5- and H7-positive markets [4]. Increased state regulatory efforts and coordination with market operators and the US Department of Agriculture led to system-wide closure of all LBMs in the northeast United States including New York, New Jersey, Pennsylvania, Massachusetts, Connecticut, and Rhode Island [4]. Intensive cleaning and disinfection of all markets was accomplished during a 3-day, poultry-free closure period. This coordinated market closure resulted in a drastic reduction in the presence of LPAI [10]. This success led to changes in coordinated efforts by participating states in monitoring and testing for avian influenza. In 2016, New England LBMs were found to again be infected with LPAI [8]. Below is a summary of a report of the event by Fox [8]; for more detailed information see the full report. In total, the outbreak affected 105 LBMs in the northeast United States [8]. In late June and early July 2016, routine surveillance samples from an LBM in Pennsylvania were collected, tested, and found to be positive for LPAI H5 by the National Veterinary Services Laboratories [8]. During the same period, an LBM in New York was also found to be positive with LPAI H5. These 2 premises were linked by a common distributor [8]. Tracing shipments from the common distributor found movement of Muscovy ducks to markets in Pennsylvania, New York, and New Jersey [8]. The response to disease in these markets was managed by their respective state animal health agencies, and markets were cleared after each LBM was cleaned and disinfected and environmental samples tested negative. Below is a brief overview of each state's approach to LPAI management. In terms of international trade restrictions, there were market restrictions as a holdover from the 2015 HPAI outbreak in US commercial poultry. There were no additional negative trade impacts in LBMs due to this 2016 LPAI outbreak. Pennsylvania animal health officials depopulated the premises known to be infected, including chickens, guineas, and Muscovy ducks, and provided compensation to affected markets [8]. These carcasses were disposed of by commercial incineration [8]. Additional LBMs from the common distributor were quarantined and required to sell down stocks of birds within 3 d; no live birds were permitted to leave the market [8]. Each market was required to undergo cleaning and disinfecting before obtaining regulatory approval of all cleaning results and negative environmental sample test results for LPAI prior to being released from quarantine [8]. New York required all 58 LBMs that received products from the distributor (7 were confirmed positive for LPAI H5) to be cleaned and disinfected [8]. Positive markets were quarantined and had a 5-day period to sell down animals followed by depopulation of remaining animals and cleaning and disinfecting [8]. New Jersey tested all 37 LBMs whether they received animals from the common distributor or not [8]. Ten markets were confirmed positive with LPAI [8]. Animals were sold down through marketing channels [8]. New Jersey LBMs were quarantined and required to clean the facilities, after which New Jersey animal health personnel disinfected premises and collected environmental samples prior to granting approval to restock the market [8]. MATERIALS AND METHODS To estimate the economic costs for control and eradication of LPAI in LBMs, costs associated with disease response and management were accounted for using expenses associated with the 2016 LPAI event in New England LBMs, including the cost to monitor, test, clean, and disinfect facilities and any bird depopulation, and other associated management costs. Each of these costs was assigned to a payee. For this work, costs associated with government animal health officials were assigned as government costs. A separate estimate of the impact on market participants was provided and included additional cleaning and disinfecting costs as well as forgone income during an LPAI outbreak. Each state responds to LPAI uniquely, expending state-specific hours and labor costs. To maintain protection of proprietary data for participating states, these state-specific values were not reported in this work. These specific costs were used in differentiating and establishing the types of practices, the number of associated hours, and in calculating average cost per unit for disease management. Total costs were assessed based on assumed average inventory for an LBM. Assumptions There were several assumptions made to estimate the cost of LPAI in LBMs. These are presented below. The average number of birds in a northeastern LBM used in the analysis was a weighted mean of 650 birds, calculated from a range of 500–800 birds based on USDA reporting and elicited expert opinion [7]. Cleaning and disinfecting costs were borne by the LBM and were not included in the cost of government response. Some states required that disinfection of LBMs be performed by animal health officials, but for consistency with reported costs and uniformity in this work, the costs to clean and disinfect were considered costs associated with the markets. All values presented were calculated means reported by animal health agencies, as were the number of disease tests and labor hours. The reported tests included a mixture of poultry and environmental tests. The cost per test varied by type and by reporting state. These costs have been averaged for conformity of tests per market and for reporter anonymity. Market impacts were based on USDA–Animal and Plant Health Inspection Services appraisal values for specialty birds. While LBMs carried a mixture of types of poultry, the reported value was an average value of replacement adult specialty breed chickens. The cost of cleaning and disinfecting by the LBM was based on an expected cumulative 8-h work day by 2 employees with minimal cost of material. Government Cost Calculations To estimate the costs of a disease outbreak, the averaged costs and quantities were applied to a cost equation expressed as follows: \begin{eqnarray} {\rm{Average}}\ {\rm{Cost\ }} = \frac{1}{n}\ \mathop \sum \limits_{i\ = \ 1}^n \big( {\rm{Test}}{{\rm{s}}_i} + {\rm{Ve}}{{\rm{t}}_i}\nonumber\\ + {\rm{Inspec}}{{\rm{t}}_i} + {\rm{La}}{{\rm{b}}_i} + {\rm{Manag}}{{\rm{e}}_i} \big) \end{eqnarray} (1) where the average cost of disease management per LBM, i, was a function of the costs of all disease sampling/testing (Tests), veterinary services—services provided by state veterinarians—(Vet), animal health inspections (Inspect), laboratory services outside of testing including salary and processing of results (Lab), and additional labor and management (Manage) per LBM divided by the number of markets, n. The cost for a specific type of LBM and the respective management employed was dependent on location, type of animals sold, and the state animal health authority's management decisions. The values presented represent average costs and quantities across reported and elicited values and can be used in calculating an approximate cost for response. Market Impact Estimation A conservative estimate of the average impact to a LBM was calculated using the following: \begin{eqnarray} {\rm{Impact}}\ &=& \ \sum \big( {\rm{Income}} + {\rm{Cleaning}}\nonumber\\ && + {\rm{Disinfection}} + {\rm{Supplies}} \big)\end{eqnarray} (2) where the estimated economic impact of LPAI for an LBM, i, was a function of the average forgone income (Income), cost for cleaning labor (Cleaning), cost for disinfecting labor (Disinfecting), and the price of supplies used for cleaning and disinfecting (Supplies) on average per LBM. The values presented represented average costs and quantities across reported and elicited values and could be used in calculating an approximate cost for response. Labor values, which do not consider foregone income by employees, were assumed to be an average minimum wage—$8.46 for the tristate study region [11]. RESULTS AND DISCUSSION Costs associated with government LPAI management in LBMs and the economic impact to LBMs are presented in Table 1. Due to confidentiality, we are unable to provide ranges, medians, maximums, or minimums. The table provides the average cost per unit, average number of units, and total cost per LBM for response, where 650 birds were assumed per LBM. The reported economic impact also accounted for forgone income and the cost to the LBM for cleaning and disinfecting. This allowed for individualization of costs to be quickly estimated. The use of actual reported costs by individual state Departments of Agriculture provides realistic estimations and projected costs of future events which can be useful to markets and responding agencies in understanding the true economic impact of LPAI outbreak in LBMs. Table 1. Average costs associated with government LPAI management for affected live bird markets and economic impact to live bird markets. Units Price per unit Quantity Cost per live bird market Disease testing Samples $38.36 10.4 $399 Inspection Hours $34.91 4.9 $171 Laboratory services Hours $21.82 2.8 $61 Management Hours $37.31 2.7 $100 Veterinary services Hours $55.14 1.3 $73 Total government response per market $804 Forgone income Bird $9.65 650 $3,860 Cleaning and disinfecting Market $137.91 1 $137 Total impact per live bird market $3,997 Units Price per unit Quantity Cost per live bird market Disease testing Samples $38.36 10.4 $399 Inspection Hours $34.91 4.9 $171 Laboratory services Hours $21.82 2.8 $61 Management Hours $37.31 2.7 $100 Veterinary services Hours $55.14 1.3 $73 Total government response per market $804 Forgone income Bird $9.65 650 $3,860 Cleaning and disinfecting Market $137.91 1 $137 Total impact per live bird market $3,997 View Large Table 1. Average costs associated with government LPAI management for affected live bird markets and economic impact to live bird markets. Units Price per unit Quantity Cost per live bird market Disease testing Samples $38.36 10.4 $399 Inspection Hours $34.91 4.9 $171 Laboratory services Hours $21.82 2.8 $61 Management Hours $37.31 2.7 $100 Veterinary services Hours $55.14 1.3 $73 Total government response per market $804 Forgone income Bird $9.65 650 $3,860 Cleaning and disinfecting Market $137.91 1 $137 Total impact per live bird market $3,997 Units Price per unit Quantity Cost per live bird market Disease testing Samples $38.36 10.4 $399 Inspection Hours $34.91 4.9 $171 Laboratory services Hours $21.82 2.8 $61 Management Hours $37.31 2.7 $100 Veterinary services Hours $55.14 1.3 $73 Total government response per market $804 Forgone income Bird $9.65 650 $3,860 Cleaning and disinfecting Market $137.91 1 $137 Total impact per live bird market $3,997 View Large During an LPAI outbreak, there are several costs associated with containment and eradication, including testing, inspection, laboratory services, management, and veterinary services. The total per-market cost for government response was estimated to be $804, or $1.24 on a per-bird basis. Relative to the other associated costs, disease tests were by far the greatest, and most necessary expense to facilitate approval for markets to reopen. These tests included those run during the outbreak and 3 mo of follow-up testing. Testing for LPAI in a market involves several different types of bird and environmental tests. There were, on average, 10.4 disease tests per LBM with an average cost of $38.36 per test, or $399 per LBM over a 4-mo period. The other 4 categories included the increased labor and management in managing LPAI. In addition to the monetary costs, there are increased time demands for animal health inspectors and veterinarians which can be taxing on agencies during an outbreak and for follow-up testing. On average, animal health inspectors spend 4.9 additional hours and veterinary services spend 1.3 additional hours per LBM during an outbreak. Similarly, there is an increase in management needs which includes general disease management, reporting, travel, and other miscellaneous facets outside the direct categories. For a state with 10 LBMs, an outbreak of LPAI can lead to an average increase in labor demand of 117 h. The data collected for these estimates coincided with a relatively short time frame from detection to reopening markets, a period of time that was 2 wk or less. While the range in the increase in the number of personnel hours may fluctuate, using these estimates, an LPAI outbreak in an LBM requires the equivalent of a full-time employee over the course of 2 wk. This perspective may help agencies and markets understand the increased cost and labor demand associated with an outbreak. An estimate for the average forgone income for birds in an LBM was estimated to be $3,860, assuming normal daily sales of 100 birds per day and an average closure of 3–5 d. There are many factors that can affect this forgone market income, including reduced pricing to move birds during the sell down period, length of market closure, or time it takes to clean and disinfect the market. During an outbreak, these values are subject to change to reflect regional and other market prices, as well as to reflect a more accurate breakout of the types of poultry housed at the LBM. The range of forgone income estimated was between $2,895 and $4,825. There may be additional losses in markets that sell their inventory prior to shut down, potentially at reduced prices, as markets tend to be permitted to sell down inventory prior to cleaning and disinfecting. Markets may reduce prices to sell birds rather than depopulate their inventory and there may be changes in customer purchasing patterns due to availability of product. While there are no estimates of the effects of the changes in prices included in this analysis, it should be noted that this would mean additional forgone income to the LBMs, leading to greater impacts on the markets. Total Costs The costs and estimated losses above were presented at the market level. Using these market-level costs and economic impacts, an estimate for the total cost of an outbreak can be assessed. Below is an estimate for the June 2016 outbreak of LPAI in northeast LBMs. The total government cost and total market impacts are presented in Table 2, which was based on 105 affected markets (37 from New Jersey, 58 from New York, and 10 from Pennsylvania). Table 2. Total estimated cost breakout for 2016 low pathogenic avian influenza in live bird markets. Estimated costs Percent of estimated total costs Disease testing $41,886 50% Inspection $17,904 21% Management $10,535 12% Veterinary services $7,669 9% Laboratory services $6,376 8% Total government costs $84,370 100% Forgone income $4,05,300 97% Cleaning and disinfecting $14,481 3% Total live bird market costs $4,19,781 100% Estimated costs Percent of estimated total costs Disease testing $41,886 50% Inspection $17,904 21% Management $10,535 12% Veterinary services $7,669 9% Laboratory services $6,376 8% Total government costs $84,370 100% Forgone income $4,05,300 97% Cleaning and disinfecting $14,481 3% Total live bird market costs $4,19,781 100% View Large Table 2. Total estimated cost breakout for 2016 low pathogenic avian influenza in live bird markets. Estimated costs Percent of estimated total costs Disease testing $41,886 50% Inspection $17,904 21% Management $10,535 12% Veterinary services $7,669 9% Laboratory services $6,376 8% Total government costs $84,370 100% Forgone income $4,05,300 97% Cleaning and disinfecting $14,481 3% Total live bird market costs $4,19,781 100% Estimated costs Percent of estimated total costs Disease testing $41,886 50% Inspection $17,904 21% Management $10,535 12% Veterinary services $7,669 9% Laboratory services $6,376 8% Total government costs $84,370 100% Forgone income $4,05,300 97% Cleaning and disinfecting $14,481 3% Total live bird market costs $4,19,781 100% View Large Total government costs were estimated to be $84,370. Disease testing accounted for the largest percentage (50%) of government expenses and the greatest contribution ($41,886) to the government's total. The number of tests for all markets was based on the average number of samples collected at each LBM as a proxy for the actual number of tests and samples taken per market. The remaining 50% of the government costs were broken down into inspection (21%), management (12%), veterinary services (9%), and laboratory services time (8%), totaling $42,485. For an extended or persistent outbreak, that estimate could substantially increase, emphasizing the importance of early detection and thorough cleaning and disinfecting. The total market impact, in terms of forgone income and direct cleaning and disinfecting costs, was estimated to be $4,19,781. The overwhelming majority (97%) was forgone income with only 3% coming from cleaning and disinfecting. This foregone income represented lost revenue from closing the market for cleaning and disinfecting prior to clearance by state animal health officials. For these markets, this loss represented financial incentives to reduce the incidence of LPAI, to maintain biosecurity measures to mitigate risk of contracting disease, and to efficiently clean and disinfect as quickly as possible to reduce the time of forced closure. Understanding the costs associated with an outbreak can help provide context for changes in the decision-making of normal business to reduce disease introduction and management of LBMs during an outbreak to shorten the market closures and limit foregone income. CONCLUSIONS AND APPLICATIONS Using reported and elicited values for the 2016 outbreak of LPAI H5 in New Jersey, New York, and Pennsylvania LBMs, the estimated cost of LPAI was $84,370. The LBMs were also affected by business disruptions due to cleaning and disinfecting protocols that forced closure of the market, and the economic loss was estimated to be $4,19,781 for all affected markets, or $3,998 per market. While prevention of a disease outbreak is favorable, these estimates provide an understanding of the costs associated with an outbreak in both value and additional labor demands. Footnotes Primary Audience: Poultry Health Researchers, Poultry Veterinarians, Public Health Officials, Economists REFERENCES 1. Alexander D. J. 2000 . A review of avian influenza in different bird species . Vet. Microbiol. 74 : 3 – 13 . Google Scholar CrossRef Search ADS PubMed 2. Johansson R. C. , Preston W. P. , Seitzinger A. H. . 2016 . Government spending to control highly pathogenic avian influenza . Choices 31 . 3. World Organisation for Animal Health (OIE) . 2015 . Avian Influenza (Infection with Avian Influenza Viruses) . OIE Terrestrial Manual 2015, chapter 2.3.4 . World Organisation for Animal Health , Paris, France . 4. Mullaney R. 2003 . Live-bird market closure activities in the northeastern United States . Avian Dis. 47 ( s3 ): 1096 – 1098 . Google Scholar CrossRef Search ADS PubMed 5. Croghan L. , Lee P. . Farm's freshest: New York's live markets sell chickens, goats and rabbits . NY Daily News. Accessed 5 Apr. 2017. http://www.nydailynews.com/life-style/eats/new-york-live-markets-sell-chickens-goats-rabbits-customers-freshest-article-1.132070 . 6. Centers for Disease Control and Prevention (CDC) . 2016 . Live Animal & Bird Markets . Centers for Disease Control and Prevention . Accessed 6 June 2017. http://www.cdc.gov/features/liveanimalbird/index.html . 7. U. S. Department of Agriculture . 2004 . Part III: Reference of Management Practices in Live-Poultry Markets in the United States . National Animal Health Monitoring System , Fort Collins, CO . 8. Fox P. 2016 . Live Bird Marketing System Working Group Report Update . Accessed 5 Apr. 2016. http://www.usaha.org/transmissible-diseases-of-poultry-avian-species . 9. Yee K. S. , Carpenter T. E. , Mize S. , Cardona C.J. . 2008 . The live bird market system and low-pathogenic avian influenza prevention in Southern California . Avian Dis. 52 : 348 – 352 . Google Scholar CrossRef Search ADS PubMed 10. Senne D. A. , Pedersen J. C. , Panigrahy B. . 2003 . Live-bird markets in the Northeastern United States: a source of avian influenza in commercial poultry . Pages 19–24 in Proc. of the Frontis Workshop on Avian Influenza: Prevention and Control . Springer , Netherlands . Google Scholar CrossRef Search ADS 11. U. S. Department of Labor . 2017 . Minimum Wage Laws in the States . Wage and Hour Division . Accessed 5 Jan. 2017. https://www.dol.gov/whd/minwage/america.htm . PubMed PubMed Acknowledgments This work would not have been possible without the support and collaboration of state animal health officials in New Jersey, New York, and Pennsylvania. A special acknowledgment goes to Nicole Lewis for her dedication to the project and for organizing the group communications. The authors would also like to thank Lindsey Garber and all the other reviewers for their helpful comments and insights. Funding support was provided by the US Department of Agriculture under Cooperative Agreement 16-9220-0455-CA. Published by Oxford University Press on behalf of Poultry Science Association 2018. This work is written by (a) US Government employee(s) and is in the public domain in the US.

Journal

Journal of Applied Poultry ResearchOxford University Press

Published: May 14, 2018

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