# PROCEEDINGS OF THE INAUGURAL ISESSAH CONFERENCE

EDITED BY : Bouda Vosough Ahmadi, Jonathan Rushton, Barbara Häsler, George John Gunn and Henk Hogeveen PUBLISHED IN : Frontiers in Veterinary Science

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ISSN 1664-8714 ISBN 978-2-88963-224-4 DOI 10.3389/978-2-88963-224-4

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# PROCEEDINGS OF THE INAUGURAL ISESSAH CONFERENCE

Topic Editors:

Bouda Vosough Ahmadi, European Commission for the Control of Foot and Mouth Disease (EuFMD), Italy Jonathan Rushton, University of Liverpool, United Kingdom Barbara Häsler, Royal Veterinary College (RVC), United Kingdom George John Gunn, Scotland's Rural College, United Kingdom Henk Hogeveen, Wageningen University & Research, Netherlands

Citation: Vosough Ahmadi, B., Rushton, J., Häsler, B., Gunn, G. J., Hogeveen, H., eds. (2019). Proceedings of the Inaugural ISESSAH Conference. Lausanne: Frontiers Media SA. doi: 10.3389/978-2-88963-224-4

# Table of Contents

Trong Tung Tran, Van Trong Nguyen, Damian Tago, Pawin Padungtod, Scott H. Newman and Astrid Tripodi

*13 Market Impact of Foot-and-Mouth Disease Control Strategies: A UK Case Study*

Siyi Feng, Myles Patton and John Davis

Karin Alvåsen, Helena Hansson, Ulf Emanuelson and Rebecka Westin

Paolo Motta, Ian G. Handel, Gustaf Rydevik, Saidou M. Hamman, Victor Ngu Ngwa, Vincent N. Tanya, Kenton L. Morgan, Barend M. deC. Bronsvoort and Thibaud Porphyre

*108 Benefit–Cost Analysis of Foot-and-Mouth Disease Vaccination at the Farm-Level in South Vietnam*

Dinh Bao Truong, Flavie Luce Goutard, Stéphane Bertagnoli, Alexis Delabouglise, Vladimir Grosbois and Marisa Peyre

*119 Assessing Financial Impacts of Subclinical Mastitis on Colombian Dairy Farms*

Jaime Romero, Efraín Benavides and Carlos Meza

# Editorial: Proceedings of the Inaugural ISESSAH Conference

Bouda Vosough Ahmadi 1 \*, Jonathan Rushton2 , Barbara Häsler 3 , Henk Hogeveen4 and George John Gunn5

1 The European Commission for the Control of Foot-and-Mouth Disease (EuFMD), Food and Agriculture Organization of the United Nations (FAO), Rome, Italy, 2 Institute of Infection and Global Health, University of Liverpool, Liverpool, United Kingdom, 3 Royal Veterinary College (RVC), University of London, London, United Kingdom, 4 Business Economics Group, Wageningen University & Research, Wageningen, Netherlands, 5 Scotland's Rural College (SRUC), Edinburgh, United Kingdom

Keywords: economics of animal health, social sciences of animal health, ISESSAH, animal diseases, animal health policies

#### **Editorial on the Research Topic**

#### **Proceedings of the Inaugural ISESSAH Conference**

Tackling the challenge of supplying sufficient food for the increasing human population in an environmentally and ecologically sustainable manner is an important focus of public and private-sector policy makers. Livestock production chains play crucial roles in fulfilling the global sustainable development goals defined by the United Nations (1). Animal diseases and animal welfare problems are considered as major barriers in achieving optimized production and profit levels where ecological and environmental damages are minimized. Emerging and reemerging transboundary diseases that are often highly contagious [such as foot-and-mouth disease (FMD), peste des petits ruminants (PPR), African swine fever (ASF), and highly-pathogenic avian influenza (HPAI)] continue to threaten livestock industries in both developed and developing counties. Similarly, other infectious and non-infectious diseases continue to impose a socioeconomic burden on food production chains and on the wider social economy in many countries.

Edited and reviewed by: Mary M. Christopher, University of California, Davis, United States

\*Correspondence:

Bouda Vosough Ahmadi<EMAIL_ADDRESS>
#### Specialty section:

This article was submitted to Veterinary Humanities and Social Sciences, a section of the journal Frontiers in Veterinary Science

Received: 10 September 2019 Accepted: 04 October 2019 Published: 18 October 2019

#### Citation:

Vosough Ahmadi B, Rushton J, Häsler B, Hogeveen H and Gunn GJ (2019) Editorial: Proceedings of the Inaugural ISESSAH Conference. Front. Vet. Sci. 6:366. doi: 10.3389/fvets.2019.00366

To tackle animal diseases, resolve animal welfare problems, and mitigate their environmental and socioeconomic burden, continuously supplied quantitative and qualitative socioeconomic research is crucial to support policy-making process. To achieve this goal, the International Society for Economics and Social Sciences of Animal Health (ISESSAH) was established in 2017 and its inaugural conference was held in March 2017 in Avimore, Scotland. The current Research Topic is devoted to 11 papers from among those presented in the first ISESSAH conference. Papers presented in this Research Topic cover broad but relevant areas of focus that can be grouped into three main categories: (1) economic assessment and managerial decision analysis of production diseases; (2) economic and policy assessment of contagious transboundary animal diseases and zoonoses; and (3) human behavior in relation to animal health and market analysis.

# ECONOMIC ASSESSMENT AND MANAGERIAL DECISION ANALYSIS OF PRODUCTION DISEASES

Romero et al. assessed the financial impact of subclinical mastitis in dairy farms in Colombia. The authors showed that mastitis imposed a greater financial loss on small and medium-sized dairy farms than on larger farms, and they highlighted the gap in our understanding of the costs and effectiveness of on-farm intervention measures. Niemi et al. reported the costs of postpartum dysgalactia syndrome (PPDS) and locomotory disorders of sows due to their impacts on productivity and replacement rates in Finland. Using a stochastic dynamic programming model that maximized the return on sow space unit, they demonstrated that PPDS and locomotory disorders imposed financial losses of e29.1 and e11.5 per housed sow, respectively, during her lifetime.

**4**

By conducting a literature review, consulting experts, and using a partial budget model, Alvåsen et al. presented an analysis on animal welfare and the economic aspects of using nurse sows for equalizing the number of piglets per nursing sow in Sweden. They found that the lactation period of sows in Sweden is longer than in other countries, which can negatively affect sow body condition, damage teats and result in shoulder ulcers. Under nursing management practices, the piglet mortality rate could be reduced and higher financial returns generated, but the separating and mixing of piglets is stressful for piglets.

Hagerman et al. employed and assessed three estimation techniques for determining the value of replacement beef cows under data availability constraint, namely: hedonic pricing, vector error correction modeling, and cost of production. After analyzing the performance of each of these livestock valuation techniques, the authors concluded that the selection of a valuation method might need to vary based on data availability and characteristics of the livestock being valued, in terms of quality and age.

# ECONOMIC AND POLICY ASSESSMENT OF CONTAGIOUS TRANSBOUNDARY ANIMAL DISEASES AND ZOONOSES

A study by Truong et al. focused on assessing the economic impact of FMD outbreaks in beef and dairy farms in Long An and Tay Ninh provinces in South Vietnam. The authors also evaluated the economic justification of a biannual vaccination strategy to prevent and eradicate FMD. Results showed that FMD vaccination had a better net present value in large dairy farms than in small ones and had a 20-times higher net present value in dairy farms than in beef farms. They concluded that a biannual vaccination strategy is economically justifiable in dairy farms, but there was uncertainty about its justification in beef farms. Featuring FMD as a serious threat for international trade, Feng et al. assessed sectoral-level impacts of control measures on FMD outbreaks in FMD-free countries using a partial equilibrium model of the agricultural sector known as FAPRI-UK. By combining epidemiologic and economic modeling frameworks, the authors simulated and assessed the consequence of two control strategies of "stamping out" and "vaccinate-to-die" on commodity market prices in the UK. Given the assumptions used, their analyses showed that the price and value of output impacts were lower under the "vaccinate-to-die" strategy compared to the "stamping out" strategy.

Focusing on another highly contagious disease control policy, Thuy Nguyen et al. conducted a stakeholder survey of live bird markets and assessed the impact of closure of these markets as a mitigation measure for HPAI in Viet Nam. Their analysis demonstrated that it is very likely that trading outside of formal markets will occur in the event of a temporary live animal market closure. Hence, the authors concluded that strict enforcement, engagement with stakeholders, and adequate communication are important prerequisites before market closure policy is introduced. By merging value chain analysis and participatory approaches to developing innovative tools for analyzing constraints to information flow, Antoine-Moussiaux et al. proposed a field-based perspective on value chain applications to HPAI prevention and control as an example of animal health systems within a One Health framework.

Munsick et al. assessed the costs and benefits of vaccinating individual sheep flocks against bluetongue virus using a stochastic simulation modeling approach with a representative rangeland sheep operation in the Big Horn Basin of the state of Wyoming in the United States. They compared the costs, benefit, and net impacts of both a killed virus vaccine and a modified-live virus vaccine under various outbreak scenarios. Results showed that a killed virus vaccine was not economically justifiable for producers in areas with a low probability of outbreaks. A modified-live vaccine has not been manufactured in Wyoming and needs rigorous authorization before legal use can start.

# HUMAN BEHAVIOR IN RELATION TO ANIMAL HEALTH AND MARKET ANALYSIS

Under our third category of papers, by using exploratory and then face-to-face interviews, Ciaravino et al. investigated the perceptions, opinions, attitudes, and beliefs of farmers and veterinarians influencing the effectiveness of the bovine tuberculosis (bTB) eradication programme in Spain. The authors demonstrated the value of qualitative research for assessing the effectiveness of health interventions that are influenced by social and behavioral factors rather than biological ones. Focusing on market behavior and drivers of live cattle prices in Central Cameroon, Motta et al. used a quantitative framework, namely a generalized additive mixed-effect model, to identify the factors contributing to cattle price. Their findings indicated that the age and sex of the cattle traded were important drivers of price along with local human and bovine population densities.

Overall, the collection of papers in this Research Topic provides a good read on a number of important aspects of socioeconomics of animal health and welfare. This reflects a fraction of the many valuable efforts at the global level that are devoted to improving our knowledge and filling existing gaps in the literature of the economics of animal health and welfare. The authors of this Editorial and the board of the ISESSAH have great hope that the research being conducted and presented in future Research Topics of ISESSAH as well as in other related initiatives will contribute to further closure of these knowledge gaps and support animal health policies.

# AUTHOR CONTRIBUTIONS

BV drafted the editorial. BH had an advisory role and provided input at the designing stage of the Research Topic. JR, HH, and GG reviewed and revised the editorial and contributed to the reviewing and editing the papers published in the proceedings of the ISESSAH inaugural conference.

# REFERENCES

1. UN General Assembly. Transforming Our World: The 2030 Agenda for Sustainable Development. 21 October 2015, A/RES/70/1 (2015). Available online at: https://www.refworld.org/docid/57b6e3e44.html (accessed October 11, 2019).

**Conflict of Interest:** 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.

Copyright © 2019 Vosough Ahmadi, Rushton, Häsler, Hogeveen and Gunn. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

# A Stakeholder Survey on Live Bird Market Closures Policy for Controlling Highly Pathogenic Avian Influenza in Vietnam

*Thi Thanh Thuy Nguyen1 \*, Lyle Fearnley 2 , Xuan Tung Dinh3 , Thi Tram Anh Tran4 , Trong Tung Tran5 , Van Trong Nguyen5 , Damian Tago6 , Pawin Padungtod1 , Scott H. Newman1 and Astrid Tripodi7*

*1Emergency Center for Transboundary Animal Diseases, Food and Agriculture Organization of the United Nations, Ha Noi, Vietnam, 2Singapore University of Technology and Design, Singapore, Singapore, 3National Institute of Animal Sciences, Ha Noi, Vietnam, 4 Institute of Economics and Finance, Ha Noi, Vietnam, 5Department of Livestock Production, Ministry of Agriculture and Rural Development, Ha Noi, Vietnam, 6Emergency Center for Transboundary Animal Diseases, Food and Agriculture Organization of the United Nations, Regional Office for Asia and the Pacific, Bangkok, Thailand, 7Animal Health Service, Food and Agriculture Organization of the United Nations, Rome, Italy*

#### *Edited by:*

*Jonathan Rushton, University of Liverpool, United Kingdom*

#### *Reviewed by:*

*Howard H. Erickson, Kansas State University, United States Melissa M. Upjohn, Brooke, United Kingdom*

#### *\*Correspondence:*

*Thi Thanh Thuy Nguyen<EMAIL_ADDRESS>
#### *Specialty section:*

*This article was submitted to Veterinary Humanities and Social Sciences, a section of the journal Frontiers in Veterinary Science*

> *Received: 29 April 2017 Accepted: 07 August 2017 Published: 22 August 2017*

#### *Citation:*

*Nguyen TTT, Fearnley L, Dinh XT, Tran TTA, Tran TT, Nguyen VT, Tago D, Padungtod P, Newman SH and Tripodi A (2017) A Stakeholder Survey on Live Bird Market Closures Policy for Controlling Highly Pathogenic Avian Influenza in Vietnam. Front. Vet. Sci. 4:136. doi: 10.3389/fvets.2017.00136*

Extensive research in Vietnam and elsewhere has shown that live bird markets (LBMs) play a significant role in the ecology and zoonotic transmission of avian influenzas (AIs) including H5N1 and H7N9. Vietnam has a large number of LBMs reflecting the consumer preferences for live poultry. Under pressure to mitigate risks for H7N9 and other zoonotic AIs, Vietnam is considering, among other mitigation measures, temporary closures of LBMs as a policy to reduce risk of AI outbreaks. However, the efficacy of market closure is debated, particularly because little is known about how poultry traders may react, and whether trading may emerge outside formal marketplaces. Combining efforts of anthropologists, economists, sociologists, and veterinarians can be useful to elucidate the drivers behind poultry traders' reactions and better understanding the barriers to implementing risk mitigation measures. In this paper, we present results from a stakeholder survey of LBM stakeholders in Vietnam. Our qualitative data show that trading outside formal markets is very likely to occur in the event of a temporary LBM market closure. Our data show that the poultry value chain in Vietnam remains highly flexible, with traders willing and able to trade poultry in many possible locations. Our results indicate that simplification of the poultry value chain along with strict enforcement, engagement of stakeholders, and adequate communication would be a necessary prerequisite before market closure could be an effective policy.

Keywords: avian influenza, live bird market, market closure, trader opinion, poultry value chain, risk mitigation

# INTRODUCTION AND PURPOSE

A number of studies point to the significance of live bird markets (LBMs) in the maintenance, transmission, and spread of avian influenza (AI) viruses in poultry populations, and highlight the role of LBMs in transmission of zoonotic influenza viruses to human populations (1–7). Studies in Vietnam have shown that LBMs are at high risk for presence of AI viruses (8), and market practices were significantly associated with AI virus contamination (9–11). In China, epidemiological studies have indicated that exposure to live poultry or contaminated environments, especially markets where live birds are sold, were significant risk factors for influenza A (H7N9) infection in human (6, 12). In a number of Chinese cities, government authorities have closed live poultry markets as part of the effort to control the epidemic.1

Emerging subtypes or clades of highly pathogenic avian influenza (HPAI) viruses could be detected in Vietnam months or years after similar viruses were detected in China, e.g., H5N1 clade 1 and clade <IP_ADDRESS>a and H5N6. Cross-border trade in poultry is suspected to be an important mechanism for the introduction of new zoonotic and HPAI viruses into Vietnam (14). The government of Vietnam is considering closure of LBMs as a possible emergency intervention if H7N9 or other zoonotic influenza viruses are detected in the market or in a person who has visited the market. Besides reducing direct contact between poultry and people, temporary market closure would enable cleaning and disinfection aimed at reducing virus accumulation, amplification, and spread among poultry population and transmit to humans. Market closure would include culling and disposal of all poultry on the day of closure, and the prohibition of holding or selling poultry in the market for 7 days while cleaning and disinfection would be conducted [Vietnam Ministry of Agriculture and Rural Development Action Plan (2014) on Emergency Response to Dangerous Avian Influenza Virus Strains with Potential Infection on Humans].

Although scientific consensus exists about the role of LBMs in the ecology of AI, significant debate remains about whether closure of LBMs will effectively transform this viral ecology and reduce risk of AI transmission. Both qualitative and quantitative studies of China's 2013 LBM closures suggested that they were effective in reducing the number of human infections with H7N9 (15–16). Studies in Hong Kong, in particular, have shown that emergency closure can transform the ecology of AI and reduce risk of transmission (17, 18). However, Fournié and Pfeiffer (19) question whether market closure can be an effective long-term strategy or can be utilized in resource-poor settings. In particular, they suggest that closure may not be as effective in a future epidemic if informal marketing channels develop. Parallel informal trade routes could spread the virus to new locations, transform the structure of viral transmission networks, and worst of all, render existing targeted surveillance and risk management activities less effective (13). Fournié and Pfeiffer (19) highlight the importance of assessing the feasibility of closing markets and the likelihood of unintended adverse results, before implementing such a measure.

Although previous studies analyzed the natural ecology of poultry and AI viruses in LBMs, they left unanswered this fundamental question about the feasibility of market interventions: how will poultry traders and LBM market managers respond to market interventions, including temporary market closure? This study aims to answer this question through a qualitative, participatory survey of the perceptions and opinions of LBM stakeholders toward disease risk in LBMs and toward temporary market closure as part of government risk mitigation interventions.

Previous surveys in LBMs focused on hygiene practices and risk behaviors (20), quantifying trader scale, and analyzing market chains (9, 11, 21), but provided minimal information about the perceptions and motivations of traders or market managers. To date, a few studies have analyzed social and cultural factors impacting the ecology of AI, focusing on farmers (22, 23) or consumers (24). This study fills this remaining gap in the understanding of social and cultural factors that are relevant for the ecological dynamics of AI through an in-depth survey of the perceptions and opinions of poultry traders and market managers in LBMs, with a particular focus on their perceptions toward temporary market closures. The aim of this study is to provide policy makers with field evidence for developing adequate risk mitigation policies in response to new introductions or detection of zoonotic AI viruses.

# METHODOLOGY

# Prospective Participatory Stakeholder Research

The study employed a participatory stakeholder approach that investigates perceptions and opinions of stakeholders about problems and policies (25). Participatory research can be defined as "systematic inquiry, with the collaboration of those affected by the issue being studied, for the purposes of education and taking action or effecting change" (26). Previous research has shown that early stakeholder involvement in the response to an environment or health problem is more effective in terms of reducing negative impact and adverse reactions than *post hoc* surveys of stakeholder reactions to a policy intervention (25, 27). In this study, we adopted a prospective approach by surveying the opinions and perceptions of stakeholders in advance of policy implementation.

The study was designed by an interdisciplinary team of trained anthropologists and sociologists, including both Vietnamese and international researchers, and in consultation with experts in animal health and AI. Guiding questions were prepared and pretested in one of the LBMs in Ha Noi, which are similar in structure and trading operations with LBMs in survey areas. The piloting markets were excluded from the survey. The interviews conducted by a team of three researchers with in-depth experience in participatory survey methods. The interviewers exchanged information at the end of each interview day in the field to ensure consistency of the field interviews. Questions were addressing aspects related to market closures such as reaction of stakeholders, impact of market closure on the livelihoods, other trading options for poultry in case of market closure, reaction on compulsory culling of poultry, and willingness of stakeholders to collaborate and under which conditions traders would

1The strategy of live bird market closure is based in part on the earlier experiences of Hong Kong. The 1997 outbreak of H5N1 in Hong Kong continues to provide a standing example of the potential for reduction or even eradication of avian influenza viruses through closure of markets coupled with poultry culls. However, as the Hong Kong case also demonstrates, the ability to eradicate AI from one city or region does not ensure protection against the later reintroduction of the virus (13).

comply with government policy on market closure. Interviews were conducted from February to March 2014. In total, 91 faceto-face interviews were conducted with poultry wholesalers, middlemen, transporters, and retailers. The interviewees were selected randomly in the survey markets. Notes were taken by the interviewers, and data were subsequently analyzed by coding of interviews. Interviews were also conducted with market management boards in six of eight LBMs. Two markets did not have market management boards, as they were open street markets.

During interviews, stakeholders were presented with the possibility that markets would be closed by the government for a temporary period of time, either 7 or 21 days, based on the Vietnam action plan on emergency response to dangerous AI virus strains with potential infection on humans. Under this plan, the decision between 7 and 21 days closure should be based on the magnitude of the disease situation. While a closure of 7 days would apply as emergency control response in markets in a small geographic area, a 21-day closure would come into force in case of geographic spread of the disease and would include markets in a wider geographic area. These stakeholder groups were defined as follows: (1) a *market manager* appointed by local government to manage the market; (2) a *wholesaler* trades a *high* volume of poultry, primarily purchasing from farms and selling to other traders; (3) a *middleman* trades a *small to medium* volume of poultry, purchased from wholesalers and sold to other traders; (4) a *retailer* trades a *small* volume of poultry and sells directly to the end user (consumer); and (5) a *consumer* is a purchaser and end user of poultry.

# Research Setting: The LBMs

Interviews were conducted in eight LBMs in four provinces: Ha Vi and Bac Thang Long markets (Ha Noi), Re Market (Hai Phong), Dam Chieu (Hai Phong), Tuc Duyen (Thai Nguyen), Ba Hang (Thai Nguyen), Gieng Vuong (Lang Son), and That Khe (Lang Son). The markets were selected to represent diversity in scale, management, trading operations, and mode of construction, which would need to be considered by government interventions in case of HPAI outbreaks.

The term "traders" (**Table 1**) includes live poultry wholesalers, middlemen, and retailers. The number of live poultry traders in each market range from 10 to 190, with a mean of 62 and a median of 57. The largest market is Ha Vi market, with 190 wholesalers and middlemen trading over 30,000 birds per day.

All the surveyed markets operate 7 days per week. Three out of the eight markets are sheltered or roofed and enclosed. Traders with permanent stalls in the market pay a monthly hygiene fee of about 50,000 VND2 to the market management board, which hires cleaners to clean the market at the end of each day. In addition, investments have been made in two of these markets to improve the hygienic situation. For example, Ha Vi market was built during 2007–2011 with funds from the World Bank through the Vietnam Animal and Human Influenza Control and Preparedness (VAHIP) project. The VAHIP invested in a waste water treatment and drainage system. However, in all three of these markets, drainage systems remained clogged by solid wastes and therefore ineffective.

Four of the eight markets located on open streets. In these street markets, traders pay a daily market fee of about 3,000–5,000 VND3 per trader. Some of these street markets are nearby to official, enclosed marketplaces that do not sell live poultry. One market is neither indoors nor on a public street, but on an area of barren land. When it rains, the ground turns to mud.

# RESULTS

In response to the possible 7-day market closure, all stakeholders pointed to the likelihood that parallel trading outside the market would emerge. At the same time, responses to parallel trading diverged according to the scale of the traders' operations. The opinion of stakeholders on market closure for 7 days is summarized in **Table 2**.

However, in response to the possible 21-day market closure, the divergence of opinions shifted. In this case, middlemen and retailers joined wholesalers in declaring that they would halt trading of live poultry altogether. They stated that with such a long, and probably widespread closure of markets, the market demand for poultry would likely decline sharply. Many traders suggested they would temporarily shift to other jobs, such as agricultural work, or trading other products (vegetables, rice, pork, kittens, puppies, etc.). In addition, they would request for exemption or reduction of taxes and other charges (market fee and charges). Market managers remained consistent in declaring they would comply with regulations, and also noted that they would request remissions of taxes or revenue charges.

Although wholesalers had declared they would halt poultry operations during both 7- and 21-day market closures, further inquiry revealed that they disagreed with compulsory culling of poultry associated with market closures in case of market closures as specified in the Vietnam action plan. Wholesalers argued that their birds have been carefully selected and have farm origin and vaccination certificates issued by animal health authorities. Therefore, they believed the birds could not be responsible for any AI outbreaks, and therefore should not be culled. If the authorities forcibly cull poultry, wholesalers argue that they should be compensated according to the purchase (farm) price or at 50–70% of the birds' market value. In addition, they called for assistance, such as preferential loans, following the end of the outbreak and

3Equivalent to 0.12–0.22 USD.

TABLE 1 | Number of traders in survey markets.

2Equivalent to 2.2 USD.

the resumption of normal market activities. Middlemen and retailers also disagreed with the culling policy, in particular the culling of "healthy looking" birds. Both groups of stakeholders called on the government to compensate for any culled birds at market or farm price. Retailers also suggested that they might try to bring birds home to avoid being culled. The market managers worried that traders would protest against any culling of poultry. They suggested that any decision to cull poultry should combine strict enforcement with good communication and explanation. They noted that the government does have a mechanism for assistance and compensation in the case of poultry culls and suggested it should be used to enhance compliance of traders.

If a zoonotic influenza virus is detected in a market, the veterinary authorities will also need to go beyond local market interventions and rapidly identify the source of the infection to focus control measures at the origin. When reporting about the willingness and ability to locate the farms of origin, responses varied according to the scale and structure of trader operations. Wholesalers claimed that tracing their poultry back to the farm of origin would be easy since their poultry typically have origin and vaccination certificates issued by animal health authorities. Wholesalers would be able and willing to provide the addresses of the farms of origin.

Middlemen claimed they purchased birds both directly from farms and from other markets or street vendors. Birds purchased directly from farms would be easy to trace, but it would be difficult or impossible to trace birds purchased at markets or on roads. Finally, retailers suggested that it would be difficult or impossible to trace the origin farm of their birds, because they purchase birds from different sources.

# DISCUSSION: VALUE CHAIN FLEXIBILITY AND THE ECOLOGY OF AI

Research in Vietnam indicates that markets connected through trade networks can contribute to large-scale epidemics, while providing opportunities for effective control as well. Targeting network hubs for surveillance, hygiene and biosecurity interventions at LBMs could reduce the transmission of virus through the network (11, 28) for China (4). The results of our study reveal that despite their position as hubs in trade networks, temporary "emergency" market closures of 7 days in case of new detection of AI viruses are unlikely to reduce the spread of AI viruses. Poultry traders, in particular middlemen and retailers, maintain a highly flexible practice of market transactions along the poultry value chain. The physical location of the LBM is only one among many possible transaction sites. Our results showed that temporary market closure for 7 days is likely to lead to establishment of parallel, informal, and uncontrolled live poultry trade, which could lead to virus introduction into non-affected areas (29). Our study concludes that given the structure of Vietnam's poultry value chain, which remains highly flexible with numerous middlemen between producer and consumer, closure of LBMs, unless implemented on a longer term and in a larger geographical area or nationwide, will be an ineffective strategy for reducing the risk of AI. However, decisions on longer term closures, would need to take into consideration the economic effects on the poultry sector (30). The importance of timely and appropriate compensation following simple procedures for culled birds appeared consistently among the responses of all the stakeholders. While current Vietnam government regulations do foresee financial compensation for compulsory culling of poultry at farms, there is at present no provision for compensation for poultry culled at markets. If stakeholders do not perceive culling as a justified measure, they will be more prone to disobey regulations and trade their poultry through unofficial channels. Proper communication of compensation schemes has shown to be crucial to improve compliance and avoid unintended effects (31, 32).

The results of our study demonstrated that poultry value chains in northern Vietnam contain a high degree of flexibility. In an agricultural value chain, "actors are connected along a chain producing, transforming, and bringing goods and services to end-consumers through a sequenced set of activities" (33). Value chain analysis has tended to provide formalistic accounts of market relationships, focusing on the vertical links that bring a product "from farm to fork." We propose the concept of the "flexibility" of the value chain to describe the capacity of a value chain to shift spatially, or to forge new transaction links, in the event that a particular site or relationship of exchange is eliminated (e.g., through market closure). Our study exposed the high degree of flexibility of the value chain in Vietnam. The flexibility of market transactions far exceeds the physical space of the marketplace, i.e., the LBM. If the LBM is closed for 7 days, trading would continue in other forms and locations. At the same time, this flexibility itself was not shared equally by all stakeholders. Wholesalers, due to the large scale of their operations, were more closely bound to the institutional setting and physical site of the formal LBM marketplace. Furthermore, they reported that they purchase poultry with official certification of farm of origin, indicating a relatively stable and traceable part of the value chain. Small retailers, by contrast, purchase birds from middlemen or wholesalers each day and sell them again, often on the side of small streets or by delivering them to small restaurants. Middlemen buy and sell poultry with the highest degree of flexibility: they report that they could easily shift operations to other markets in the event of market closure for 7 days. The restructuring and simplification of the poultry value chain as suggested by several poultry value chain studies conducted in Vietnam (FAO unpublished data), by reducing the number of middlemen and small-scale traders, could decrease the overall flexibility of trading and therefore improve the effectiveness of market closure. The flexibility of the poultry value chain explains why market closure may not be an effective strategy for reducing the spread of AI or AI incursion risk. The closure of the marketplace is intended to eliminate a key node in the network of AI transmission. But LBM traders do not necessarily confine their trading to the LBM. As traders exploit the flexibility of the value chain and shift transactions to parallel trading sites, live poultry trading networks may expand and fragment, increasing rather than reducing AI transmission and risk.

Finally, our results also revealed important limits to the flexibility of the poultry value chain. A minor limit exists in the length of market closure. During a 7-day closure, all stakeholders described how they would adapt by shifting market operations to other locations, but during closure of minimum 21 days, all stakeholders reported that they would halt trading operations. Rather than trading live poultry in alternate locations along the value chain, they reported that they would shift to other forms of economic activity: trading non-poultry products or even returning to farm work. However, prolonged market closures may result in high economic losses and impact livelihoods in the poultry production sector (34).

# CONCLUSION

The present study shows that analyzing perceptions of stakeholders regarding risk mitigation interventions, such as the temporary closures of markets, are crucial for the design of effective policies and to avoid adverse results.

To date, the implementation of market closures has been based on viral surveillance data relying on virus detection alone.

# REFERENCES

Neglecting the fact that LBMs are human, social and cultural institutions may render disease control policy ineffective. In fact, the role of LBMs in the chain of influenza transmission is conditioned by the practices and perceptions of LBM stakeholders. As a result, although market places may be closed, marketing practices and networks may continue to operate in a shifted form and facilitate AI virus spread. The position of LBMs in the poultry value chain in the North of Vietnam exemplify how the natural ecology of AI is shaped as a consequence of human perceptions and reflexive practices (35). In such cases, understanding the ecology of the virus and how to manage its risks relies on understanding the human stakeholders that construct, and can unexpectedly reconstruct, the links in the chains of viral transmission.

Stakeholder participation should be an integral part of the development of science-based policy interventions, not only for reasons of equity and ownership but also more importantly to provide accurate knowledge about natural ecology itself (25) and to ensure planning and implementation of more effective risk mitigation measures.

# ETHICS STATEMENT

The study was considered low risk as the main risks to study respondents were believed to be abreact of confidentiality and privacy. To mitigate these risks, the following safeguards were put in place. Verbal informed consent was received from study participants during the recruitment process. Another verbal informed consent was received from participants before each interview or group discussion after clear explanation about the objectives and content of the study. Each study participant was assigned a code to maintain confidentiality during data collection and analysis. No personal identifiers, including names, were collected at any time throughout the study.

# AUTHOR CONTRIBUTIONS

All the authors: substantial contributions to the design of the study, collecting data in the field, and analysis and interpretation of the data; drafting the report; approval of the version to be published; and agreement to be accountable for all aspects of the manuscript.

# FUNDING

This study was financially supported by the United States Agency for International Development (USAID) under grant number GHA-A-00-06-00001.

chains in South China: the value of social network analysis. *Prev Vet Med* (2011) 102(3):196–205. doi:10.1016/j.prevetmed.2011.07.007

**Conflict of Interest Statement:** 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.

*Copyright © 2017 Nguyen, Fearnley, Dinh, Tran, Tran, Nguyen, Tago, Padungtod, Newman and Tripodi. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.*

# Market impact of Foot-and-Mouth Disease control strategies: a UK case study

*Siyi Feng\*, Myles Patton and John Davis*

*Agri-Food and Biosciences Institute, Belfast, United Kingdom*

Foot-and-mouth disease (FMD) poses a serious threat to the agricultural sector due to its highly contagious nature. Outbreaks of FMD can lead to substantial disruptions to livestock markets due to loss of production and access to international markets. In a previously FMD-free country, the use of vaccination to augment control of an FMD outbreak is increasingly being recognized as an alternative control strategy to direct slaughtering [stamping-out (SO)]. The choice of control strategy has implications on production, trade, and hence prices of the sector. Specific choice of eradication strategies depends on their costs and benefits. Economic impact assessments are often based on benefit–cost framework, which provide detailed information on the changes in profit for a farm or budget implications for a government (1). However, this framework cannot capture price effects caused by changes in production due to culling of animals; access to international markets; and consumers' reaction. These three impacts combine to affect equilibrium within commodity markets (2). This paper provides assessment of sectoral level impacts of the eradication choices of FMD outbreaks, which are typically not available from benefit–cost framework, in the context of the UK. The FAPRI-UK model, a partial equilibrium model of the agricultural sector, is utilized to investigate market outcomes of different control strategies (namely SO and vaccinate-to-die) in the case of FMD outbreaks. The outputs from the simulations of the EXODIS epidemiological model (number of animals culled/vaccinated and duration of outbreak) are used as inputs within the economic model to capture the overall price impact of the animal destruction, export ban, and consumers' response.

#### *Edited by:*

*Jonathan Rushton, University of Liverpool, United Kingdom*

#### *Reviewed by:*

*Dustin L. Pendell, Kansas State University, United States Francois Frederick Maree, Agricultural Research Council of South Africa (ARC-SA), South-Africa*

> *\*Correspondence: Siyi Feng<EMAIL_ADDRESS>
#### *Specialty section:*

*This article was submitted to Veterinary Epidemiology and Economics, a section of the journal Frontiers in Veterinary Science*

*Received: 30 March 2017 Accepted: 26 July 2017 Published: 01 September 2017*

#### *Citation:*

*Feng S, Patton M and Davis J (2017) Market Impact of Foot-and-Mouth Disease Control Strategies: A UK Case Study. Front. Vet. Sci. 4:129. doi: 10.3389/fvets.2017.00129*

Keywords: foot-and-mouth disease, partial equilibrium model, disease control strategy, market impact, economics

# INTRODUCTION

Foot-and-mouth disease (FMD) poses a serious threat to the agricultural sector due to its highly contagious nature, which can lead to substantial disruptions to livestock markets. It is estimated that the outbreak in the UK in 2001 resulted in losses to agriculture and the food chain of approximately £3.1 billion, with further significant impacts on the wider economy (3). A *stamping-out (SO)* policy was implemented in 2001 to control the disease, whereby all infected stock and others exposed to infection (dangerous contact herds) were culled. Subsequent legislation included provisions for emergency vaccination as a control strategy. Vaccination was considered as an alternative control strategy during the 2007 outbreak, but ultimately was not deployed due to advice on the degree of risk of the disease spreading (4). There are two main vaccination strategies: *vaccinate-to-die (V-t-D)* and *vaccinate-to-live*. Under the *V-t-D* strategy, vaccinated animals are culled. Compared to the *SO* strategy, this may entail higher compensation spending, but shorten the duration of the outbreak by slowing the spread of the disease. Under the alternative *vaccinate-to-live* strategy, vaccinated animals remain in the population and may be slaughtered commercially, but this strategy entails delays in the reopening of international markets.

The market implications will vary across different control strategies due to, for example, differences in the duration of the outbreak, number of animals culled and closure of export markets. It is not straightforward to discern the market impact from previous outbreaks due to evolvement of contingency plans, country variations, dependency on export markets, other shocks to the market, etc. For example, when Argentina used vaccination to eradicate FMD in the early 2000s, the economy experienced severe downturns during this period, making it difficult to isolate the market impacts of the control strategy. FMD outbreaks are rare in countries, such as the UK, but will potentially have serious consequences if it occurs. It is, therefore, important to gain insights on disease management from not only historic experiences but also modeling exercises, which are built based on the logical abstraction of reality.

This paper investigates the market impacts of the strategies of *SO* versus *V-t-D* in FMD control in the case of the UK using a partial equilibrium modeling framework. The results are based on linking the FAPRI-UK partial equilibrium model and the EXODIS epidemiological model. Outputs from the simulations of the EXODIS model (number of animals culled/vaccinated and duration of outbreak) are used as inputs within the FAPRI-UK model to capture the price impact of the destruction of animals and restrictions to internal trade. The EXODIS model is stochastic, that is, the same virus can potentially result in a small- or a large-scale outbreak. Within this paper, market impacts are assessed for different scales of a potential outbreak. We begin with a review of the literature in Section "Literature Review." This is followed by descriptions of the economic partial equilibrium model, the FAPRI-UK model and alternative scenarios in Section "Model and Scenarios." The results are presented in Section "Results" and conclusions are drawn in Section "Summary and Discussion."

# LITERATURE REVIEW

Due to the potential loss caused by FMD outbreaks, control strategies are constantly reviewed and evaluated, among which economic assessments are important. Economic assessments mostly concern the costs of alternative control strategies and/or value of certain responses, such as early detection, which help to reduce costs [e.g., Ref. (5, 6)]. These analyses are often based on the benefit–cost framework, which provide detailed information on the changes in profit for a farm or budget implications for a government (1). However, the benefit–cost framework cannot capture market price effects caused by changes in the following:

These three impacts combine to affect equilibrium within commodity markets (2). Reduced production as a result of the destruction of animals exerts a positive impact on price. Counteracting this, if exports are banned in response to the outbreak, additional production must be absorbed within the domestic market leading to an increase in supply. In addition, although FMD does not typically affect humans, there may be a negative consumption response to an outbreak due to consumer health concerns, even if these concerns are unfounded. Such concerns would lead to an inward shift in the demand curve and exert a downward impact on price. The ultimate impact on price depends on the weight of these individual effects and will vary across sectors depending on, for example, the importance of exports relative to domestic consumption. The partial equilibrium modeling framework models both the supply side and the demand side of a market and solves for a market clearance price. Thus, it is better suited to capture these effects. It enhances understanding of the market consequences for different commodities of different control strategies in response to an outbreak, complementing the benefit–cost analysis. There are assessments of FMD outbreaks and/or FMD control strategies using partial equilibrium models for the United States (7–10), Australia (11), Canada (12), and Mexico (13).

The economic impacts of vaccination as a control strategy are explicitly examined by Hagerman et al. (8), Schroeder et al. (9), Buetre et al. (11) and Tozer et al. (12), which reflect the rising recognition of this strategy in recent years. Both Hagerman et al. (8) and Buetre et al. (11) find that the desirability of vaccination depends on the scale of the outbreak. The cost of vaccination strategy cannot be justified when the outbreak is small. Also in the context of the US, Schroeder et al. (9) examines outbreaks at a larger scale compared to those in Hagerman et al. (8) and finds substantial benefits of using the vaccination strategy. Tozer et al. (12) is less informative in control strategy choices as it focuses on the dynamics of producer decisions using a discrete time optimal control model. The model assumes deterministic parameters that characterize the way in which FMD develops; in other words, there is no uncertainty with regard to the spread of the disease itself. To our knowledge, the market impacts of vaccination strategy for FMD control have not been examined in the UK. Following Hagerman et al. (8) and Buetre et al. (11), the control strategies will be assessed for potential outbreaks of different scales.

# MODEL AND SCENARIOS

# Model

The FAPRI-UK model is an annual partial equilibrium model of the agricultural sector of the UK. Commodities modeled include wheat, barley, rapeseed, oats, beef, lamb, pork, poultry, dairy, and biofuel. Final demand for the meats and dairy entail derived demand for animals for slaughter and dairy cows and derived demand for feed from the crop sector. The dynamics in breeding herd building and livestock production are captured through appropriate lags in the equations. Production of these commodities is modeled at the level of the four countries of the UK: England, Wales, Scotland, and Northern Ireland. Demand is modeled at the UK level. Under most analyses, the model is run in conjunction with the EU-GOLD model so that markets clear at the EU level as markets of the Member States within the EU are deeply integrated.1,2 This means that international trade, excess supply, and demand at the UK level feed into the EU for solving the equilibrium prices.

The FAPRI-UK modeling system produces Baseline projections over a 10-year period of key variables in the beef, sheep, pig, poultry, dairy, and crop sectors for each country in the UK under the assumption that current policies remain in place and specific macroeconomic assumptions hold. The Baseline provides a benchmark against which projections of the policy scenarios can be compared and interpreted (14).3 The Baseline used in this analysis was finalized in Spring 2016 and covers the projection period 2016–2025.

When an FMD outbreak occurs, export of animal products from the outbreak country will be banned until the disease is eradicated and a specified waiting period has passed. During this period, the UK markets will be temporarily disintegrated from the EU. New equations for import and export of beef, lamb, and pork are developed so that these markets clear at the UK level. Then the export ban is incorporated as a shock to the export equation. The size of the shock depends on the duration of the disease outbreak and the waiting period. The time taken to eradicating the disease obviously depends on the success of the control strategy used, while the waiting period also depends on the control strategy as specified in existing regulations. Details of the waiting period for each of the control strategies examined within this paper and the specification of the size of the shock to export are provided in the next section.

In addition, the FMD outbreak will cause a shock to the production of the meat and dairy products as infected (and perhaps vaccinated livestock) are culled. Given the biological dynamics in livestock sector, culled livestock have impacts on meat production beyond the outbreak year, particularly in the beef sector. In general, if commodities redirected from export outweigh the reduction in production following an FMD outbreak, this results in excess supply, which exerts a downward impact on price in the domestic market. Price falls may deepen, depending on whether the outbreak causes a food scare in consumption.4

The last route through which equilibrium is restored is import adjustment. Imports will reduce in response to lower prices in the UK as exports being redirected to the domestic market. Nevertheless, domestic prices would rarely be higher than EU prices during the year of outbreak as imports are always possible. For the markets to reach equilibrium following an FMD outbreak, the price elasticity of import is a particularly crucial parameter; that is, the extent of import changes relative to price change. It is important to acknowledge that there is considerable uncertainty regarding the extent to which imports are likely to be displaced by the rechanneling of exports to the domestic market. The rate of displacement is of particular concern as the export ban implies a sudden substantial increase in supply to the domestic market from the rechanneled exports. This has important implications on the price impact of an FMD outbreak. Imports may be slow to readjust due to contractual reasons and demand requirements, e.g., imports from the southern hemisphere may fulfill demand requirements during specific periods of the season. It is also possible that imports adjust quickly in response to the rechanneling of exports. As a result, sensitivity analyses regarding import adjustments are carried out in which changes in imports are exogenously imposed. Two extreme cases are examined: no displacement and substantial displacement. In the case of no displacement, it is assumed that imports remain unchanged compared to Baseline projections. This reflects the assumption that imports are slow to adjust and cannot be readily canceled. In the case of substantial displacement, it is assumed that imports are reduced by 90% of exports that are diverted to the domestic market due to the export ban, implying that imports adjust instantaneously in response to the imposition of an export ban. The sensitivity analysis provides a means to quantify the price impact of an FMD outbreak under different trade assumptions.

# Scenarios

Two FMD control strategies are examined in this paper.

### Stamping-Out

Under this scenario, numbers of animals culled from simulations of the epidemiological model are incorporated within the economic model, resulting in reductions in livestock numbers and animals available for slaughter. In addition to the number of culled animals, the epidemiological model provides data on the duration of the outbreak. Under the "SO" scenario, the waiting period for applying for disease-free status and resuming export is 90 days after the last case of FMD.

#### Vaccinate-to-Die

Similar to scenario (i), numbers of culled animals from the epidemiological model are entered as supply shocks in the economic model and exports resume 90 days after the last infected and vaccinated animals are culled.

The analysis undertaken in this paper is based on stochastic simulations of the EXODIS epidemiological model undertaken by the Animal and Plant Health Agency as an extension of Exercise Rowan.5 The epidemiological model simulations are based on an outbreak equivalent to the characteristics of the

1The EU-GOLD model is a partial equilibrium model of the agricultural sector at the EU level. It is developed and maintained by the Food and Agricultural Policy Research Institute (FAPRI) at the University of Missouri.

2This study was carried out before the UK referendum of exiting the EU.

3Project information on the AFBI website: https://www.afbini.gov.uk/analysisagricultural-commodity-markets-fapri-uk-project.

4Note the analysis in this paper focuses on the effect of shock to production and exports. We do not examine the implication of a shock in consumption as it is difficult to discern the size of such a shock from real data as the scale of the shock in the simulations is smaller than the 2001 outbreak.

5The initial phase of Exercise Rowan was undertaken in the latter part of 2015. During the exercise, the EXODIS model was used to test FMD response capability in the UK. See Roche et al. (15) for further information on the EXODIS model.

virus in the UK in 2001, but take into account up-to-date UK contingency plans. The stochastic output from the epidemiological model yielded 200 outcomes, which reflect alternative developments of the same FMD virus. In order to identify the market impact of these different outcomes, the median outputs from the epidemiological model are used as inputs within the economic model. In addition, we consider the tails of the distribution from the epidemiological model outcomes. In particular, the 95th percentile is used to represent the situation in which the virus develops into a particularly serious outbreak, as reflected in the number of livestock affected and the duration of the disease outbreak. The 5th percentile replicates a mild outbreak. As shown in the summary statistics in **Table 1**, the number of culled animals is higher under the V-t-D simulations compared to SO. However, the duration of the disease-free status period is lower under the former, particularly with regard to the 95th percentile. A matching procedure was used to identify individual simulations that approximate the median, 5th and 95th percentile statistics of all the relevant variables (numbers of livestock culled of different species and duration of disease outbreak).6

Animals culled under the *SO* scenario in the simulated outbreak of median scale (based on the epidemiological model) represent 1.8, 0.6, and 0.2% of the projected total number slaughtered of the year for the beef, sheep, and pig sector, respectively. The percentages rise to 4.8, 1.9, and 0.7% in the *V-t-D* scenario. However, it should be noted that while the breeding herd and animals at different life stages are not distinguished in the epidemiological model, they are modeled separately in the economic model.

6Rather than devising a rule to disaggregate UK epidemiology outputs at the regional level, individual simulations that approximate the median, 5th and 95th percentile statistics of all the relevant variables (numbers of livestock culled of different species and duration of disease outbreak) at the UK-level were identified. It is relatively straightforward to identify individual simulations that closely approximate the 5th percentile and median, but less so for the 95th percentile of all the sectors simultaneously. With regard to individual simulations, some sectors are not affected to the same extent compared to the statistics for the 95th percentile. More emphasis was placed on the beef and sheep sectors within the matching procedure. The relevant variables from the chosen individual simulations closely match the 95th statistics for these sectors, but slightly lower outcomes emerged for the pig sector. Nevertheless, the differences were sufficiently small such that qualitative differences between the scenarios for all the sectors, including the pig, still hold.

Therefore, total number culled by species are proportioned to the breeding herd and animal for meat purpose at different life stages based on historic census before they are incorporated into the economic model. This implies that the percentages mentioned earlier are greater than the production shock to the year of the outbreak while the culling will exert some effects for the year(s) following the outbreak.

The FMD outbreak in the UK in 2001 lasted for 221 days and the number of animals culled was over 4 million. By contrast, the 2007 outbreak lasted for 58 days and only 2,160 animals were culled (4). It appears that the 2001 outbreak is more serious than the case of 95th percentile presented in this study (**Table 1**). Although the epidemiological simulations are based on an outbreak equivalent to the characteristics of the virus in the UK in 2001, direct comparison is difficult because the model simulations take into account the up-to-date UK contingency plans, which have been significantly reviewed and updated following the outbreaks.

Underlying the *SO* and *V-t-D* scenarios, it is assumed that all exports of beef, sheep, and pig meat are halted for the duration of the outbreak plus 3 months after the detection of the last case, in line with World Animal Health Guidelines. Thus, it is assumed that there is no regionalization, i.e., exports from the whole country are banned. The reduction in exports as a result of the export ban is computed as a proportion of the length of the export ban:

> Export Reduction Export under the Baseline Days of Expo = × ( rt Ban/ ) 365 .

The length of the export ban is defined as the period of the last reported case plus the waiting period before it is possible to apply for disease-free status. This definition may be interpreted as the most optimistic estimation of the duration of the export ban as it implies no delay in approval. In the past two FMD outbreaks in the UK (2001 and 2007), both outbreaks ended in around September of the year and the UK regained disease-free status in the beginning of the following year. This suggests that the waiting period in these two cases were not much longer than the minimum required (i.e., 3 months). However, it should be noted that in both cases, the UK used the *SO* strategy only. A summary of the scenarios (including sensitivity analysis of import adjustments) is presented in **Table 2**.

# RESULTS

# Impact during the Year of Outbreak

**Table 3** reports the impacts of the SO and V-t-D strategies for outbreaks of difference scales with various assumptions on import adjustment during the year of outbreak.

Starting with the "*SO—endogenous displacement*" scenario, UK prices fall by 7.9, 24.7 and 17.3%, respectively, in the beef, sheep, and pig sectors in 2017 for an outbreak of median scale. The negative price impact is attributable to the additional production absorbed onto the domestic market due to the export ban, which leads to an increase in domestic supply. The limited decline in production is insufficient to offset the rechanneling of

TABLE 2 | Foot-and-mouth disease (FMD) control scenarios.

exports and, hence, commodity prices decline. The sheepmeat sector experiences the greatest price decline due to the high level of self-sufficiency. The projected value of output in the sheepmeat sector falls by 25.1% and primarily reflects the drop in price.

Compared to the median, the negative price impact is greater following a more serious outbreak (the 95th percentile version of the scenario). The prices of beef, sheep meat, and pig meat fall by 9.3, 31.4, and 22.2%, respectively. Despite the more serious nature of the outbreak, the prices are lower under the 95th simulations compared the median. The negative production impact from the larger number of animals culled is more than offset by the longer duration of the outbreak, which results in an extended export ban and more produce being absorbed on the domestic market. By contrast, the milder outbreak experienced under the 5th percentile version of the scenario results in smaller price impacts compared to the median.

Under the "*endogenous displacement*" simulations the absorption of exports onto the domestic market is partially counteracted by a fall in imports. When it is assumed that imports do not adjust to the export ban ("no displacement" scenario), price drops are more severe. In the case of the median outbreak, beef, sheep meat, and pig meat prices fall by 11.2, 43.2, and 22.1%, respectively. Within this scenario, the absorption of exports onto the domestic market is not counteracted by a fall in imports, leading to a greater negative supply shock. While this "*no displacement*" scenario is extreme it sheds light on situations in which imports adjust slowly to an export ban. It thereby provides an indication of the implications of this assumption.

The price impact is significantly less marked when imports almost fully readjust in response to the rechanneling of exports. Under the median version of the "*SO—substantial displacement*" in which it is assumed that imports are reduced by 90% of exports, the sheepmeat price is 4.4% lower than the Baseline. This contrasts with 43.2% in the no displacement scenario.

Compared to "*SO*", "*V-t-D*" leads to the culling of more animals and, hence, lower production. In addition, the "*V-t-D*" control strategy also significantly curtails the time-span of the outbreak and, as a consequence, the duration of the export ban. As a result, fewer exports are absorbed onto the domestic market. As a consequence of both these effects, the price impacts are less marked under the "*V-t-D*" scenarios compared to "*SO*." For example, the sheep meat price falls by 18.6% under the median "*V-t-D—endogenous displacement*" scenario, compared to 24.7% under the equivalent "*SO—endogenous displacement*" scenario. The projected value of output falls by a greater amount than price in percentage terms (20.2 versus 18.6%) due to the fall in production.

Comparing the results of the outbreaks at the same quantile under the *V-t-D* and *SO* scenarios, it is apparent that the projected price and value of output differences between these strategies are more marked for severe outbreaks. With regard to the sheepmeat price the difference between the two control strategies under the 95th percentile versions of these scenarios is 9.3% as the price fall under *V-t-D* is 22.1 and 31.4% under SO. This compares to 6.1% under the median. This result supports the hypothesis that the benefits of vaccination are clearer for more severe outbreaks.

Similar to the "*SO*" results, the price impacts are significantly greater when it is assumed that imports remain unchanged compared to the endogenous versions of the scenario, which entail partial adjustments in imports. For example, under the median version of the "*V-t-D—no displacement*" scenario, the sheepmeat price falls by 35%. Again, the benefits of vaccination are greater under the 95th percentile compared to the median.

In general, across the scenarios the longer the duration of the export ban the greater the price fall (**Figure 1**). One exception is the "*V-t-D*" 95th percentile scenario. Under the "*V-t-D*" 95th percentile scenario, the export ban is 176 days, compared to 171 under the "*SO*" median scenario. Despite this, the price decline is less marked under the former. The number of livestock culled under the "*V-t-D*" 95th percentile is greater than the "SO" median case and, consequently, the rechanneling of exports to the domestic market leads to smaller excess supply.

# Impact over the Whole Projection Period

While commodity prices in the livestock sector are negatively affected by an FMD outbreak, this impact generally lasts for less than a year even under a serious outbreak (the longest among all the scenarios is 224 days in the case of the 95% percentile under the SO strategy). An outbreak will result in a smaller herd for the following year; breeding herd and animals for meat production numbers are smaller. To rebuild the breeding herd, some animals that would have been designated for meat production will be kept for breeding instead. As a result, meat production will be lower and prices will be higher compared to the Baseline. Among the three sectors, the restocking process is the longest for the beef sector and, therefore, beef price is the slowest to return to baseline level (**Figure 2**).7 Beef prices do not return to the

7Note: the intertemporal results discussed in this section draw on the main analysis, i.e., the "Endogenous Displacement" scenario.

TABLE 3 | Foot-and-mouth disease control strategy results—comparison between baseline projections and scenario in year of outbreak (2017).

Market Impact FMD Control UK

Feng et al.

baseline level until the year 2023, while in the pig sector there is no discernible impact from the year 2019 onward. The paths of output values, defined as production multiplied by price, are similar to the price paths, suggesting that the increases in prices outweigh the smaller production (**Figure 2**).

To further compare the impact of the disease on the output value of the livestock sectors, output values are summed over the period of 2017–2025. All values are discounted to the 2017 value before the summation is carried out, using a discount rate of 3.5%.8 Results are presented in **Table 4**. Over the period of 2017–2025, there are some small reductions in the total output values in the livestock sector; furthermore, the more severe the outbreak, the greater impact on total output value. Taking the longer term impact into account, the main conclusion from the previous section is still valid: the vaccination-to-die strategy helps to mitigate the market impact compared to the SO strategy.

# SUMMARY AND DISCUSSION

This study is made possible following a new component developed in the partial equilibrium model that enables the UK markets to deviate from the EU. In the two most recent FMD outbreaks in the UK (very serious in 2001 versus mild in 2007), emergency vaccination was never used. The effectiveness of vaccination is shown in the experiences of other countries (for example, the Netherlands and Uruguay). The Netherlands had used emergency vaccination combined with the *V-t-D* strategy in 2001. The culling of large number of vaccinated healthy animals was not without controversy. Since then, there is ongoing exploration of the *vaccinate-to-live* strategy. However, the use of *vaccinate-to-live* strategy entails a longer export ban, which raises concerns with the industry. There could also be other issues such as logistics. Therefore, better understanding of the trade-offs of the different strategies is needed to assist decision making, which is the main purpose of our study. In a future study, we will cover the strategy of *vaccinate-to-live*.

By combining epidemiology and partial equilibrium modeling frameworks the analysis undertaken in this study demonstrates the potential market consequences of alternative FMD control strategies. It is projected that an FMD outbreak has a negative impact on market prices and value of output, regardless of the control strategy. Although the analysis is based on a virus similar to the characteristics of the 2001 outbreak, unlike this previous outbreak, the number of animals culled and, hence, the production impact is relatively modest. This reflects the evolvement of contingency plans, with co-ordination measures helping to reduce the spread of disease. While the projected decline in production under both the *SO* and *V-t-D* scenarios results in lower value of output, the largest impact on value of output stems from the drop in price due to the closure of export markets. Similarly, studies in other geographical areas have shown that the export ban exerts

Baseline

TABLE 3 | Continued

Endogenous displacement

Stamping-out

5th

*Changes in*

*percent*

Production Consumption

Price Output

−0.6%

5.0%

−15.5% −16.0%

−17.9%

−22.8%

−13.6%

−14.6%

−17.8%

−20.5%

−22.7%

−28.5%

−17.6%

−18.6%

−22.4%

−2.1%

−2.3%

−3.2%

−1.4%

−1.1%

−1.2%

−17.3%

−22.2%

−12.9%

−13.5%

−16.5%

−19.9%

−22.1%

−27.8%

−16.8%

−17.6%

−21.1%

−1.7%

−2.0%

−2.8%

−0.9%

−0.1%

 0.1%

 5.7%

 7.5%

 4.1%

 4.3%

 5.4%

 6.3%

 7.1%

 9.4%

 5.2%

 5.5%

 6.8%

 0.5%

 0.5%

 0.7%

 0.2%

 0.0%

 0.0%

−0.7%

−0.9%

−0.8%

−1.2%

−1.5%

−0.7%

−0.8%

−1.0%

−0.9%

−1.3%

−1.6%

−0.4%

−0.4%

−0.5%

−0.5%

−0.9%

−1.2%

 Median

95th

 5th Median

 95th

 5th

 Median

 95th

 5th

 Median

 95th

 5th

 Median

 95th

 5th Median 95th

Vaccinate-to-die

Stamping-out

No displacement

Vaccinate-to-die

Stamping-out

Vaccinate-to-die

Substantial displacement

8The choice of discount rate is based on Treasury Guidance of the UK government [the Greenbook by Treasury (16)].

the larger impact on farm revenue compared with production changes [e.g., Ref. (2, 7)].

The more severe the disease outbreak, the greater the negative price impact, as demonstrated by comparing the median and 95% percentile versions of the scenarios. While the latter results in the culling of more animals compared to the former, which exerts an upward impact on price, this is more than offset by the market impacts of the longer duration of the export ban.

It is important to acknowledge that underlying this analysis it is assumed that exports are halted for the full duration of the outbreak plus 90 days after the last case or the last vaccinated animal is culled. The price and value of output impact would be diminished if export markets were to reopen sooner. Potentially, governments could pursue regionalization, whereby trade is allowed to resume from non-infected regions, providing it is possible to demonstrate the disease is contained (2).

In addition, the feasibility of readjusting imports is crucial. The sensitivity scenarios indicate the extent to which readjustments in imports diminish the price and revenue impacts of an FMD outbreak. If it is not possible to reduce imports swiftly the price impact could be substantial, as demonstrated under the *no displacement* scenarios. This case represents the most marked potential impact. Exporters to the UK may choose to re-channel exports to other markets if prices were to decline significantly. However, the response is unlikely to be instantaneous.

Finally, the results of this analysis indicate that the price and value of output impacts are lower under *V-t-D* compared to *SO*. This conclusion holds when longer term impacts are taken into account. This primarily reflects the effectiveness of *V-t-D* in slowing the spread of the disease and, hence, curtailing the duration of the export ban. This comparison is based on the assumption that there are no delays in gaining the approval of reopening export markets. In reality, this may be more difficult with regard to vaccination due to logistical reasons, e.g., additional surveillance requirements for proof of freedom status and delays in removing vaccinated animals following the outbreak (15). The finding that vaccination is favored compared to SO is greater, the

TABLE 4 | Change in total output values of the livestock sectors of 2017–2025.

displacement" scenario (SO, stamping-out; V-t-D, vaccinate-to-die).

more severe the outbreak. However, it should be noted that this analysis focuses on the market impact of the disease outbreak. To make the final choice among the control strategies, other costs such as on farm and administrative costs should also be taken into account.

# AUTHOR CONTRIBUTIONS

Substantial contributions to the conception or design of the work: SF, MP, and JD. Acquisition, analysis, or interpretation of data for the work: SF and MP. Drafting the work or revising it critically for important intellectual content: SF, MP, and JD. Final approval of the version to be published: SF, MP, and JD. Agreement to be accountable for all aspects of the work in ensuring the questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved: SF, MP, and JD.

# ACKNOWLEDGMENTS

Special thanks to Charlotte Cook and Ruth Moir at Animal and Plant Health Agency, Weybridge for provision of results from the EXODIS epidemiology model.

# FUNDING

Research funded by the Department for Environment Food & Rural Affairs, the Scottish government, the Welsh government and the Department of Agriculture, Environment and Rural Affairs.

# REFERENCES

**Conflict of Interest Statement:** 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.

*Copyright © 2017 Feng, Patton and Davis. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.*

*Tristram R. Munsick1 , Dannele E. Peck1 \*† , John P. Ritten1 , Randall Jones2 , Michelle Jones2 and Myrna M. Miller 3*

#### *Edited by:*

*Bouda Vosough Ahmadi, Scotland's Rural College, United Kingdom*

#### *Reviewed by:*

*Hans-Hermann Thulke, Helmholtz-Zentrum für Umweltforschung (UFZ), Germany Kaare Græsbøll, Technical University of Denmark, Denmark*

*\*Correspondence:*

*Dannele E. Peck<EMAIL_ADDRESS>
#### *†Present address:*

*Dannele E. Peck, Northern Plains Climate Hub, USDA Agricultural Research Service, Fort Collins, CO, United States*

#### *Specialty section:*

*This article was submitted to Veterinary Epidemiology and Economics, a section of the journal Frontiers in Veterinary Science*

*Received: 25 March 2017 Accepted: 22 September 2017 Published: 11 October 2017*

#### *Citation:*

*Munsick TR, Peck DE, Ritten JP, Jones R, Jones M and Miller MM (2017) Expected Net Benefit of Vaccinating Rangeland Sheep against Bluetongue Virus Using a Modified-Live versus Killed Virus Vaccine. Front. Vet. Sci. 4:166. doi: 10.3389/fvets.2017.00166*

*1Department of Agricultural & Applied Economics, University of Wyoming, Laramie, WY, United States, 2Agricultural Producer, Big Horn Basin, WY, United States, 3Department of Veterinary Sciences, University of Wyoming, Laramie, WY, United States*

Recurring outbreaks of bluetongue virus in domestic sheep of the US Intermountain West have prompted questions about the economic benefits and costs of vaccinating individual flocks against bluetongue (BT) disease. We estimate the cost of a BT outbreak on a representative rangeland sheep operation in the Big Horn Basin of the state of Wyoming using enterprise budgets and stochastic simulation. The latter accounts for variability in disease severity and lamb price, as well as uncertainty about when an outbreak will occur. We then estimate the cost of purchasing and administering a BT vaccine. Finally, we calculate expected annual net benefit of vaccinating under various outbreak intervals. Expected annual net benefit is calculated for both a killed virus (KV) vaccine and modified-live virus vaccine, using an observed price of \$0.32 per dose for modified-live and an estimated price of \$1.20 per dose for KV. The modified-live vaccine's expected annual net benefit has a 100% chance of being positive for an outbreak interval of 5, 10, or 20 years, and a 77% chance of being positive for a 50-year interval. The KV vaccine's expected annual net benefit has a 97% chance of being positive for a 5-year outbreak interval, and a 42% chance of being positive for a 10-year interval. A KV vaccine is, therefore, unlikely to be economically attractive to producers in areas exposed less frequently to BT disease. A modified-live vaccine, however, requires rigorous authorization before legal use can occur in Wyoming. To date, no company has requested to manufacture a modified-live vaccine for commercial use in Wyoming. The KV vaccine poses less risk to sheep reproduction and less risk of unintentional spread, both of which facilitate approval for commercial production. Yet, our results show an economically consequential tradeoff between a KV vaccine's relative safety and higher cost. Unless the purchase price is reduced below our assumed \$1.20 per dose, producer adoption of a KV vaccine for BT is likely to be low in the study area. This tradeoff between cost and safety should be considered when policymakers regulate commercial use of the two vaccine types.

Keywords: domestic sheep, economics, intermountain west, Monte Carlo simulation, private cost, uncertainty, variability, Wyoming

# INTRODUCTION

Bluetongue (BT) is an insect-borne, hemorrhagic, viral disease that affects domestic sheep and other ruminants throughout much of the world, including the US (1). Clinical signs of bluetongue virus (BTV) infection in sheep (*Ovis aries*) can range from mild to severe or fatal; they include widespread edema, internal hemorrhaging, nasal discharge, weight loss, and oral ulcerations. The risk of BT disease can be reduced through vector control (e.g., insecticide application) or vaccination of susceptible flocks. Vector control has been helpful in Europe and Asia (2). However, vaccination has been the most effective method for preventing and controlling BT in Europe (3).

Virus serotypes, vaccine regulations, and day-to-day management practices on rangeland sheep operations in the US Intermountain West are sufficiently different from those in Europe that they may alter the economic effectiveness of vaccination. Costs and benefits of vaccination against BT in the US Intermountain West have not previously been estimated. This is due, in part, to a lack of research on the economic consequences of BT outbreaks in this region. We, therefore, estimate the costs of a BT outbreak in a representative rangeland sheep flock in the state of Wyoming, as well as the costs and expected benefits of vaccinating against BTV. Wyoming is an important sheep-producing state, currently ranking fourth in the US for lamb output, and accounting for 6.7% of the total US sheep inventory (4). The Big Horn Basin of north-central Wyoming (roughly 8,000 km2 ; **Figure 1**), in particular, experienced a severe BT outbreak in 2007, which provides a case-study on which to base many of our model parameters and assumptions.

We analyze the economic costs and benefits of two different vaccine types: killed virus (KV) and modified-live virus (MLV). A sheep producer in Wyoming can currently obtain a KV vaccine legally for commercial use, but it involves custom-manufacturing and is, therefore, not readily available and thought to be more expensive. An MLV vaccine, in contrast, cannot be legally obtained for use in Wyoming—due to vaccine safety concerns yet, is thought to be less expensive and hence more likely to be adopted. These tradeoffs between vaccine safety and vaccine cost (thus adoption) have piqued the interest of animal health policymakers in Wyoming. Unfortunately, the epidemiological data necessary for quantifying the economic value of vaccine safety are not currently available in our study area. But we lay the groundwork for future research and policy debate by determining if either vaccine generates enough benefits to outweigh the private costs of purchasing and administering it. If both vaccines are too costly to justify private investment by sheep producers, then future research and policy debate may be unnecessary. But if an MLV vaccine proves economically attractive for producers, while a KV vaccine does not because of its higher cost, then further research and policy debate may be justified.

# BTV and Disease

Bluetongue is a non-contagious, insect-borne viral disease that afflicts sheep, cattle, and other ruminant species (5). BTV is transmitted between susceptible animals by particular biting-midge species of the genus *Culicoides* (*C. sonorensis* in Wyoming). The disease's distribution depends on the range of the relevant midge species, but has historically circumnavigated the globe in temperate and semi-arid climates, between approximately 40° North and 35° South (6). Although BTV has a wide global distribution, symptomatic occurrence of BT disease is most common at the northern and southern boundaries of the virus' range. Virulence is significantly lower in areas where BTV is endemic (i.e., chronically prevalent). This may be due to increased population immunity and co-evolution of the virus and its susceptible hosts (7).

Bluetongue virus, the etiological agent of BT disease, is a member of the *Orbivirus* genus within the *Reovirideae* family. Evolution of BTV is driven by genetic drift, shift, and intragenic recombination (8). Over time, this has led to the establishment of at least 27 known viral serotypes worldwide. In the US, five serotypes were historically identified (BTV 2, 10, 11, 13, and 17), and 10 additional BTV serotypes were recently identified in the southeastern US (7). Viral serotypes vary from each other in characteristics such as virulence and transmission potential (9–11). This may help explain the highly variable morbidity and mortality rates experienced during outbreaks of different viral strains around the globe.

Clinical signs of BT vary in severity depending on the strain of virus and host species affected. Sheep, deer, and antelope (wild or domestic) are relatively more susceptible and affected, whereas cattle and goats are less affected (12–15). In severe cases, the infected ruminant's tongue becomes swollen and discolored and may protrude from the mouth, hence the name "bluetongue." Gross legions on the heart, liver, spleen, kidneys, lungs, and gastrointestinal tract may have extensive hemorrhaging. The course of the disease ranges from 2–15 days, with the majority of symptoms usually appearing within 7 days of infection (16). In mild cases, recovery is swift with costs consisting primarily of weight loss and supportive care. In more severe cases, often in previously unexposed (i.e., naïve) populations, recovery may be prolonged and generate much higher losses. Mortality rates under typical Intermountain West field conditions vary between 4 and 20% of the total exposed population. Death typically occurs 1–8 days after the appearance of symptoms (16).

# Economic Costs of BT Outbreaks

Most recent economic studies of BT disease have been conducted in Europe, where several outbreaks of BTV-8 (BTV, serotype 8) have had severe effects on the sheep and cattle industries (17). Most notably, epidemics in the Netherlands during 2006 and 2007 caused large economic losses to sheep and cattle producers. The 2006 outbreak affected 460 farms in the Netherlands, with additional outbreaks occurring in neighboring Belgium, France, Germany, and Luxemburg. The epidemic of 2007 affected more than 6,000 farms in the Netherlands alone. Economic losses totaled 32 million Euros in 2006 and 175 million Euros in 2007 (17). Although the majority of losses occurred within the cattle industry, the sheep industry was also impacted. Within the sheep sector, breeding farms suffered the greatest losses (58% of total sheep morbidity and mortality losses for 2006; 72% of losses for 2007) (17). Velthuis et al. (3) show that vaccination of all adult sheep and cattle is the

best strategy for BT disease control and prevention in Europe, based on benefit–cost ratios.

Although studies estimating the economic consequences of BT outbreaks in Europe offer useful insights, they focus on virus serotypes that do not exist in the US Intermountain West (9). Furthermore, the regulatory and physical environment, scale, and management practices of European sheep operations differ enough from the Intermountain West's extensively managed rangeland sheep flocks to necessitate a separate study.

# Recent BT Outbreaks in the US Intermountain West

In 2007, a regional outbreak of BTV-17 (BTV, serotype 17) was first identified in several sheep flocks in the southeastern region of the state of Montana. The disease was subsequently reported in northern regions of the state of Wyoming; first in pronghorn, white-tailed deer, and mule deer in early fall of 2007, and finally in domestic sheep in the Big Horn Basin of northern Wyoming in late fall of 2007 (16). Quarantines were placed on sheep flocks in 17 Montana counties and 3 Wyoming ranches, preventing any off-farm movement.

Bluetongue virus-17 outbreaks had previously occurred in other parts of Wyoming and Montana; however, ranchers and veterinarians reported that Big Horn Basin flocks had not been previously exposed (16). This may be due, in part, to the region's surrounding mountain ranges, which act as a natural barrier to foreign vector populations (16). Outbreaks occur more regularly in other regions of Wyoming that are less geographically protected. In such regions, previously exposed sheep populations seem to experience less severe symptoms than those sheep affected during the Big Horn Basin epidemic. These anecdotal observations provide grounds for further investigation of some veterinarians' hypothesis that sheep populations can build immunity over time if exposed to the virus regularly (16).

The BTV-17 outbreak in Big Horn Basin during 2007 had severe consequences on regional sheep operations. One flock suffered 36% morbidity (500 out of 1,404 sheep) and 20% flock mortality (275 out of 1,404 sheep) (Personal communication with Ranch A operator in 2015). A neighboring ranch was also affected, but fared slightly better: 14% morbidity (233 out of 1,679 sheep) and 0.2% flock mortality (7 out of 1,679 sheep) (16). Recovery from an epidemic of this magnitude can be challenging, given that western US livestock ranches typically have net returns averaging 2–4% per year (18). This thin profit margin can quickly disappear during an unexpected disease epidemic.

# BT Prevention Using Vaccines

Vaccination has been used effectively in some regions of the US to control BT in livestock. But because of the region-specific diversity of BT strains, there is limited demand for a vaccine against any one strain. Limited demand has prevented broadscale commercialization of BT vaccines. Exceptions include a live-attenuated (or modified-live) vaccine against BTV-10, which is approved for use throughout the US, and live-attenuated vaccines against BTV-10, 11, and 17 that are approved for use only in California (19).

Another reason for limited availability and approval of BT vaccines in the US is safety concerns, which differ for the two vaccine types we analyze here. The first vaccine type, live-attenuated or MLV, are relatively cheap to produce and are routinely used in domestic sheep flocks throughout Israel, South Africa, and some US states (limited to certain strains) (20). But use of MLV vaccines is prohibited in some US states because of their potential to revert to virulent type, as well as their ability to infect and be transmitted by insect vectors, thereafter circulating as a field strain. MLV viruses also have the ability to reassort gene segments with field viruses and create novel progeny (7). Finally, if given during pregnancy, MLV vaccines may cause unintended abortions, deformities, and other pregnancy complications (7).

The second type of vaccine is an inactivated autogenous, or KV vaccine. These are typically more expensive to produce than MLV vaccines and require a follow-up dose to attain a protective level of antibodies (19). However, they do not suffer the safety risks associated with MLV vaccines. Specifically, KV vaccines do not revert to virulence, do not reassort genes with field viruses, and do not cause reproductive damage to pregnant females (7).

Speiser et al. (21) tested the ability of two different custommade BTV-17 vaccines—KV and MLV—to trigger a humoral response in ewes from seven commercial sheep operations in Wyoming. Both vaccines induced protective levels of antibodies, which lasted for at least 1 year and provided passive immunity for lambs. In light of the equal effectiveness of both vaccine types, the next step is to evaluate and compare the vaccines' economic performance.

Our study evaluates the economic costs and expected benefits of vaccinating Wyoming domestic sheep flocks against BTV-17, using either a KV or MLV vaccine. Our results can help inform discussions between sheep producers, vaccine manufacturers, the State Veterinarian, and Livestock Board about potential approval and commercial sale of a BTV-17 vaccine for Wyoming. Currently, Wyoming producers can customorder a KV vaccine manufactured from a recent isolate taken from an outbreak occurring in their region. An MLV vaccine for BTV-17 is not currently available for producer use outside of California, but the potential exists to legalize its importation into western sheep-producing states such as Wyoming (Personal communication with Dr. Jim Logan, Wyoming State Veterinarian in 2016). Before engaging in a debate about MLV vaccine legalization, animal health policymakers need to know if either vaccine would generate positive economic net benefits for producers.

# MATERIALS AND METHODS

# Expected Profit Maximization

The theoretical framework for this study is expected profit maximization. We assume a sheep producer's expected profit depends on their decision to vaccinate (or not vaccinate) their flock against BT. When combined with two possible states of nature (BT affects their flock, or it does not), there are four possible outcomes: (1) vaccinate and sheep contract BT anyway; (2) vaccinate and sheep do not contract BT; (3) do not vaccinate and sheep contract BT; (4) do not vaccinate and sheep do not contract BT. The producer organizes these four possible outcomes into two different expected profit functions: one for the decision to vaccinate, and one for the decision not to vaccinate. They then compare the two expected profits to decide whether or not to vaccinate.

The first step in identifying the expected profit maximizing decision is to determine the probability of occurrence for each of the four possible outcomes. Our chosen probabilities are based on historical data of the disease (16) and first-hand producer knowledge for the Intermountain West (Personal communication with Ranch A operator in 2016). To represent differences in disease prevalence throughout Wyoming, we calculated the expected net benefit associated with outbreaks occurring every 5, 10, 20, or 50 years.

# Rangeland Sheep Production Budgets

The next step of our analysis is updating an existing sheep enterprise budget, for a representative operation with 640 breeding ewes (1,404 sheep in total) (22), to US\$2014 prices using indices of prices paid by Wyoming farmers and ranchers from 2010 to 2014 (23). Prices assumed in our analysis are reported in Table S1 in Supplementary Material. The updated budget provides an outline of management activities, costs, and revenues for a 1-year production calendar. It provides baseline estimates of profit, which we later adjust to reflect the costs of vaccinating sheep against BT, and the cost of a BT outbreak itself. A summary of the baseline budget is available in Table S2 in Supplementary Material. Munsick (24) provides a more detailed version of the baseline budget.

# BT Outbreak Costs

To estimate the cost of a BT outbreak, we reconstruct the series of events experienced by an anonymous producer during the 2007 BT outbreak in the Big Horn Basin of Wyoming. The dates they report imply a particular subset of production activities being disrupted. If the outbreak's timing had differed substantially from this, an alternative subset of activities would be disrupted, resulting in different outbreak costs. The anonymous producer's outbreak unfolded as follows. BT symptoms were detected September 1st and ended October 15th, encompassing 45 days of symptomatic disease within the flock. An on-site flock quarantine was imposed throughout the duration of the outbreak. The end of vector season occurred on the first hard freeze (29°F or below) on October 15th (23). An additional asymptomatic quarantine period of 14 days commenced on October 16th and extended to October 30th. This lengthened the total BT outbreak quarantine period to 59 days (Personal communication with Ranch A operator in 2015).

Tangible costs that a producer incurs during an outbreak include death loss, supportive care, pharmaceuticals, loss of condition, labor, and veterinarian fees. Intangible costs, such as stress and other emotional impacts, are not quantified here but are no less impactful. To calculate lamb death loss, we multiply the number of lambs lost to BT by a 25-year mean market value, \$130/cwt, which we derive from a distribution of real historical lamb prices (1990–2014) from the Centennial Livestock Auction near Fort Collins, CO, USA (25). We assume that our representative operation markets 90-pound feeder lambs.

Ewe death loss is calculated by multiplying the number of ewes lost to BT by the economic value of an average-aged ewe in the flock. Based on conversations with regional producers (Personal communication with Peter John Camino, former President Wyoming Woolgrowers Association and with Ranch A operator in 2015), our representative flock's replacement ewes are developed from within the operation. Therefore, the loss of an adult ewe due to BT is considered a capital loss. Specifically, it is equal to the cost of developing an identical replacement minus the cull value. This capital loss is then added to the discounted cull value lost to determine overall economic value lost when a ewe dies from BT. Details of the cost to develop a replacement ewe can be found in Munsick [(24), p. 16]. We use a similar method to calculate costs associated with ram death loss from BT [(24), p. 17]. Throughout our analysis, we use a 7% rate to discount the operation's future costs and benefits to the present. This rate is commonly used for agricultural investments; it accounts for a 4% real rate of return on investment plus a 3% risk premium (18).

Another factor in the cost of a BT outbreak is providing supportive care to infected sheep. Substantial swelling in the face and throat of infected sheep requires a producer to provide a source of nourishment other than forage or hay. Ranch A accomplished this by mixing creep feed with water and administering the mixture directly to infected animals *via* feeding tube. Infected sheep that eventually recover begin to show signs of improvement after 7 days of creep-feeding. Those that eventually die do so after 10 days of creep-feeding (Personal communication with Ranch A operator in 2015). Infected lambs consume 2 lbs of creep feed (before adding water) per day while ewes and rams consume 3 lbs per day.

Pharmaceuticals needed during an outbreak are also included in supportive care costs. Direct vector control, for example, is beneficial when used to supplement vaccination in preventing further BT infections once an outbreak is detected [(2); Personal communication with Dr. Jim Logan, Wyoming State Veterinarian in 2016]. Permethrin is an affordable, widely available insecticide approved for direct use on livestock, including sheep. It is helpful in the control of the BT vector, *Culicoides* spp. (2). However, application is labor intensive [(2); Personal communication with Ranch A operator in 2015], and its effectiveness as a sole control measure (which we do not quantify in this analysis) is incomplete (26). We assume the treatment is repeated every 2 weeks throughout the course of the outbreak, totaling three treatments from September 1st to October 15th.

A significant portion of BT mortality is caused by secondary respiratory infections (16). Nuflor is an example of a synthetic, broad-spectrum antibiotic that aids in prevention and treatment of bacterial pathogens (e.g., pneumonia) that commonly occur during a BT outbreak (Personal communication with Dr. Matt Cherni, practicing large animal veterinarian in 2015). Nuflor label instructions call for a two-dose treatment, the second being administered 48 h after the first. Dexamethasone is used as an anti-inflammatory and may be administered simultaneously with Nuflor to the entire flock. The drug is relatively affordable and is effective in treating inflammatory symptoms common for BT, such as fever, pain, and swelling.

Due to a lack of data, we assume no loss in ewes' reproductive efficiency or condition during a BT outbreak. However, we do account for a loss of condition in market lambs during the year of the outbreak. We assume a 10% live-weight loss (i.e., 90 lb lamb × (1 − 0.10) = 81 lb live weight, or a 9 lb loss per lamb) in surviving infected lambs which are marketed soon after recovery (Personal communication with Ranch A operator in 2015).

Labor costs include additional hired labor required to manage a BT outbreak. Many operations will fulfill additional labor requirements with longer hours for themselves and their families, but we assume additional owner labor is unavailable and, therefore, hired labor must be increased. The amount of additional labor necessary to cope with an outbreak is estimated based on Ranch A operator's experience in 2007.

A BT outbreak generally does not involve extensive veterinarian resources. However, some visits from State and Federal officials may be necessary. The use of these public resources represents a social cost (as opposed to private cost) of the disease, and should not be overlooked. Similarly, research funded with public dollars to better understand BT represents an additional social cost (and social benefit). Our study focuses on private costs to sheep producers and, therefore, does not attempt to estimate the public cost of State or Federal veterinarians' visits, BT research, or other public resources used during an outbreak.

## BT Vaccination Costs

The cost of purchasing and administering a BT vaccine is based on pharmaceutical companies' recommendation that producers annually vaccinate their entire flock. To improve efficiency and decrease vaccination labor costs, we assume that a producer vaccinates their entire flock at the same time as deworming, on June 1st. This also allows for passive immunity to begin to wane in the newborn lamb crop (Expert opinion of co-author, Miller). Since the entire flock is already being handled and run through the chute for deworming, we assume it takes only 10 additional seconds to vaccinate for BT. The follow-up dose, required only if using the KV vaccine, can be given at any point after a minimum of 3 weeks has passed since the first dose. However, for the vaccine to produce desired levels of antibodies, the second dose must be given at least 7 days prior to flock exposure to the disease. For many producers, this amounts to vaccinating their flock twice before moving to summer range, or possibly administering the follow-up dose at some point during summer. If producers decide to vaccinate their flock separately from any existing handling sessions, the cost of labor will increase beyond what is reported in our analysis. Total vaccination costs are calculated by summing the cost of purchasing the vaccine and the cost of labor needed to administer it during existing handling sessions.

#### MLV Vaccination Cost

An MLV vaccine contains whole viruses that are able to grow and multiply within a host body. They stimulate the host immune system to create antibodies, yet do not typically cause actual disease in the host. Because the vaccine contains live active viruses, only one annual injection is needed (27).

A major side-effect of the MLV BT vaccine is the potential to cause abortions in pregnant ewes or malformations in their lambs. We do not include risk of abortions in our cost estimate, because we assume that producers administer the vaccine properly, i.e., not during pregnancy. There is also a risk that the modified virus will revert to virulent type, causing the vaccinated animal to become sick, or to infect and be transmitted further by the vector midges (28). This "escape" risk represents an external or social cost and is not borne by producers directly. Therefore, it is outside the scope of this analysis, which focuses solely on producer's private costs. These two risks limit the use of an MLV vaccine to between March 31 and June 1 (i.e., after lambing and before the height of vector season).

The only available MLV vaccine for BTV-17 is approved for use strictly in California. For use in Wyoming, the producing company would need to seek USDA approval for distribution and use in other states, and then solicit a formal request from the State Veterinarian. To do this they must provide adequate documentation of efficacy, product safety, and USDA licensure (Personal communication with Dr. Jim Logan, Wyoming State Veterinarian in 2015). We assume a retail purchase price for such an MLV vaccine of \$0.32 per dose, based on the price advertised for a similar vaccine on the California Wool Growers Association's website (http://cawoolgrowers.org/vaccines/bluetongue.html).

#### KV Vaccination Cost

An autogenous or KV vaccine is produced using virus strains isolated from infected tissue samples using a cell culture system (29). As a USDA-licensed, restricted-use product, KV vaccines against BT are available for use only under veterinarian supervision. However, they involve no seasonal restrictions on its use, no risk of vector transmission, and no risk of abortion if used in pregnant ewes. The vaccine can be made as a monovalent (single antigen), bivalent (double antigen), or trivalent (triple antigen) vaccine. However, our analysis focuses on a monovalent vaccine for BTV-17.

Production of a KV vaccine takes approximately 12 weeks. Therefore, production and field-deployment of this type of vaccine might be infeasible if begun after the onset of an outbreak. However, virus isolates taken from a specific site may be used for up to 15 months from the date of isolation from tissue (30). An additional 24 months of use may be granted if vaccine efficacy has been shown and a viable threat of disease still exists. The use of a KV vaccine is also restricted to the BTV isolate's source flock. However, permission for use in other flocks may be granted by the State Veterinarian (30). Retail pricing for a KV vaccine is assumed to be approximately \$1.20/dose, which includes a 20% markup by a private veterinarian (Personal communication with Newport Laboratories, Worthington, MN, USA, in 2012).

## BT Vaccination Benefits and Net Benefits

Recent studies have found the efficacy of both MLV and KV vaccines under controlled conditions to range from 84 to 100% (21). We assume a conservative 84% effectiveness for both vaccines. Vaccine effectiveness is modeled by reducing the number of infected sheep by 84%, which propagates through the enterprise budget by reducing the number of sheep experiencing morbidity or mortality and the total hours of supportive care required.

The next step in our analysis is to calculate expected annual net benefit of vaccinating. We calculate this for both the MLV and KV vaccine, and for outbreak intervals of 5, 10, 20, and 50 years. To calculate expected annual net benefit, we first determine the expected benefit of vaccinating in a given year, accounting for time value of money and uncertainty in outbreak timing. Even if a producer knows the outbreak interval for their area (e.g., 10 years), they cannot predict the exact year in which an outbreak will occur. Therefore, we calculate the present value (PV) of benefit for each possible year in which the outbreak could occur (e.g., 1–50). We then annualize each of these PVs. Next, we multiply each annualized benefit by the probability of an outbreak occurring in a given year (e.g., 0.02). This generates a weighted annualized benefit for each year. Finally, we sum the weighted annualized benefits for each year to obtain an average or expected annual benefit over the given outbreak interval. This approach accounts for time value of money as well as uncertainty about an outbreak's timing within a given interval. From this expected annual benefit, we then subtract the annual cost of vaccination to obtain expected annual net benefit of vaccination. This four-step calculation is summarized in Eq. 1:

$$\text{Expected Annual Net Bonefit} = \sum\_{i=0}^{N-1} \left\lfloor \frac{\text{Benefit}}{\left(1+i\right)^{i}} \star \frac{i}{1-\left(1+i\right)^{-N}} \star \frac{1}{N} \right\rfloor$$

$$\text{-Annual Cost},\tag{1}$$

where *N* is the outbreak interval (e.g., *N* = 5, 10, 20, or 50); *t* is the year in which an outbreak occurs (e.g., *t* = 0 indicates it occurs in the current year); *Benefit* is the undiscounted benefit of having a vaccinated flock when an outbreak does occur; *i* is the discount rate; and *Annual Cost* is the real cost incurred per year to vaccinate a flock against BT disease. In summary, the first term inside the brackets discounts the benefit of vaccinating based on the year in which the outbreak occurs. This adjusts for a producer's time value of money (i.e., \$1 of benefit received today tends to be valued more highly than \$1 of benefit received in a future year). Next, the middle term inside the brackets annualizes the PV of benefit, spreading it evenly across the entire outbreak interval after accounting for the discount rate. The third and final term inside the brackets weights the annualized benefit by its probability of occurring (i.e., by the probability of an outbreak occurring in year, *t*). This three-step process is repeated for every *t* (i.e., for every possible year in which the outbreak could occur, given a particular outbreak interval). The resulting set of weighted annualized benefits is then summed to give the expected annual benefit. Finally, annual cost of vaccinating a flock is subtracted from expected annual benefit, resulting in expected annual net benefit of vaccination.

# Incorporating Variability: @Risk Simulation

For the final step of our analysis, we use the software program @Risk to conduct a Monte Carlo simulation, which allows three parameters in our model to vary (26): lamb price, morbidity rate, and mortality rate. Monte Carlo simulation is a technique that randomly draws a set of parameter values (where each set represents an "iteration") from a probability distribution (29), and then uses those values in all calculations involving the three parameters. Each simulation involves running 50,000 iterations.

By simulating variability in lamb price, morbidity rate, and mortality rate, we are able to account for the inherent variability of outbreaks occurring in different years and at different geographic locations. Producers are generally well-aware of changing market and disease conditions and, therefore, desire information about vaccine performance during worst-case and best-case scenarios, not just on average. The distributional information generated through Monte Carlo simulation helps producers identify strategies that are robust to a range of possible outcomes.

We first simulate a distribution for outbreak cost (**Figure 2**), which then serves as an intermediate input to the simulation of distributions for expected annual net benefit, one each for the KV and MLV vaccines. Each of these three distributions is influenced by the input distributions chosen for lamb price, morbidity rate, and mortality rate. We fit a log-logistic distribution to observed lamb prices (28) from the Fort Collins auction barn during November 1990 to November 2014 (adjusted to US\$2014; see Figures S1 and S2 in Supplementary Material). Its parameters are set to the following values: γ = 0.58805, β = 128.31, α = 7.0474, minimum = 46.53, maximum = 229. Truncation at the minimum and maximum values allows the lamb price to fall one SD (\$0.31/ pound) below or above the historical price range.

We model the morbidity rate as a uniform distribution with a minimum = 0.06 and maximum = 0.36. Similarly, we model the mortality rate as a uniform distribution with a minimum = 0.046 and maximum = 0.20. Parameter values for the mortality and morbidity rates are based on observations from a previously naïve flock in the Big Horn Basin (for maximum values), and from a routinely exposed flock in Johnson County, Wyoming (for minimum values). More details of the rationale behind the distributions chosen are presented in Munsick [(24), p. 32–36]. Table S3 in Supplementary Material provides @Risk formulas for the three input distributions.

# RESULTS AND DISCUSSION

# BT Outbreak Costs

**Table 1** provides outbreak costs assuming mean values for morbidity rate (21%), mortality rate (12.3%), and lamb price (\$1.30 per pound). **Figure 2** depicts the distribution of simulated outbreak costs for the operation, accounting for variability in lamb price, morbidity, and mortality. Costs associated with a BT outbreak can be disaggregated into several categories.

Total death loss is the combined loss of ewes, rams, and lambs due strictly to a BT outbreak. Although ram death loss is static, ewe death loss is a function of the variable lamb price and is,

therefore, a distribution. After all, the death of a ewe triggers retention of an extra replacement lamb, which would have otherwise been sold at the variable lamb price. Lamb death loss is also a function of the variable lamb price, as well as morbidity and mortality rates.

Supportive care costs include tubing infected animals with a creep feed/water mixture and administering necessary pharmaceuticals as needed. Creep feed costs are driven by the variable morbidity and mortality rates. Pharmaceutical costs include direct application of permethrin insecticide spray, administration of Nuflor for all clinically infected cases, and administration of dexamethasone as needed. Additional costs include weight loss on surviving infected lambs, labor, and veterinarian costs (only those paid by the producer).

# BT Vaccination Costs

The cost of vaccination includes both the cost of purchasing vaccine and the labor to administer it. Cost of hired labor is assumed to be \$10.64/h (31) adjusted by a producer price index of 1.091. Purchase price of the vaccine is estimated at \$0.32/dose for the MLV vaccine and \$1.20/dose for the KV vaccine. **Table 2** shows the vaccine and labor costs for vaccinating the entire flock, using the MLV versus KV vaccine. Costs reported for the KV vaccine include both the first dose and the required follow-up dose.

# BT Vaccination Benefits

The benefit of vaccinating sheep against BT is a reduction in the proportion of the flock affected when the virus strikes. In a 640-ewe flock that has been vaccinated, the average number of morbidities and mortalities is reduced from 285 and 167 (without

*Reported costs are calculated using the mean morbidity rate (21%), mean mortality rate (12.3%), and mean lamb price (\$1.30/pound).*

Table 2 | Cost of annual bluetongue vaccination for a 640-breeding-ewe operation (entire flock at time of vaccination is 1,423 sheep) using a modified-live virus (MLV) versus killed virus (KV) vaccine (US\$2014).

vaccination), respectively, to just 46 and 27 (with vaccination). This reduces the cost of an outbreak from an average of \$36,207 (without vaccination) to \$5,243 (with vaccination). Thus, on average, the benefit of vaccinating is \$30,964 per outbreak. This benefit ranges, however, from as little as \$11,325 to as much as \$63,183, depending on the outbreak's severity and the lamb price. Because the benefit of vaccinating depends so heavily on outbreak cost, their distributions are shaped similarly (compare **Figure 2** to Figure S3 in Supplementary Material).

Of the three random variables in our analysis, BT mortality rate has the greatest influence on outbreak cost and hence vaccination benefit. Lamb price has the second greatest influence, followed by BT morbidity rate. **Figure 3** shows a tornado graph (using the "regression coefficients" option in @Risk) of relative influence of the three random variables on vaccination benefit. Regression coefficients indicate the amount of change that will occur in a dependent variable due to a change in an independent variable. For example, increasing the lamb price by 1 unit will result in a 0.35 unit increase in the benefit of vaccination.

The total benefit of administering a BT vaccine, over a producer's career, depends on how often their flock is exposed to the virus.  Unfortunately, society's ability to predict an outbreak is currently limited, so producers must decide ahead of the risk season each year whether to vaccinate. Before making the vaccination decision, producers should compare the annual cost of vaccinating against its expected annual benefit, to determine expected annual net benefit.

# BT Vaccination Net Benefits

To calculate expected annual net benefit of vaccination, we must assume how frequently the virus will strike. **Table 3** reports the mean value of expected annual net benefit for outbreak intervals of 5, 10, 20, and 50 years. Expected annual net benefit of vaccination tends to be higher for MLV than for the KV vaccine (**Table 3**; **Figure 4**). This is because the MLV vaccine is cheaper to purchase and requires only one dose per year, whereas the KV vaccine has a higher assumed purchase price and requires a follow-up dose. The higher expected annual net benefit for MLV than for KV holds true across all outbreak intervals (**Table 3**). More specifically, MLV yields positive expected annual net benefit (based on its median) up to 69 years between outbreaks (**Figure 5**). KV vaccine, in contrast, yields positive expected annual net benefit up to just 9 years between outbreaks (**Figure 5**).

**Figure 5** also reveals that, as outbreak interval lengthens, expected annual benefit decreases. This is because benefit is assumed to occur just once during a given interval. Thus, as outbreak interval lengthens, the annualized benefit of vaccination gets smaller and smaller, whereas the annual vaccination cost remains the same. This causes the expected annual net benefit to decrease as outbreak interval lengthens (**Table 3**).

Turning to variability, the distributions of expected annual net benefit for MLV versus KV are shown in **Figure 4**, for a 10-year outbreak interval. The shape of these distributions is similar to those for 5, 20, and 50-year outbreak intervals (not shown). Note that the two distributions in **Figure 4** are identically shaped and differ only in their mean values. This is because they both derive

Table 3 | Mean value of expected annual net benefit (US\$2014) for two different vaccine types [modified-live virus (MLV), killed virus (KV)], administered annually, under different outbreak intervals (5, 10, 20, and 50 years).

from the same outbreak cost distribution (**Figure 2**), which is based on a log-logistic lamb price distribution (Figure S1 in Supplementary Material) and uniform morbidity and mortality distributions (Table S3 in Supplementary Material). The identical distribution of expected annual net benefit for MLV versus KV (**Figure 4**) also reflects our assumption that both vaccines are equally effective. Given their many similarities, the two distributions differ only because the MLV vaccine is assumed to be \$3,003 cheaper than KV (precisely the difference between the two distributions' means). The purpose of **Figure 4** is to illustrate the dramatic implication this cost difference has on the probability of MLV versus KV generating positive expected annual net benefit. For a 10-year outbreak interval, MLV has a 100% chance of generating positive expected annual net benefit, whereas KV has only a 42% chance. This cost-driven reduction in the probability of breaking even, on average, will reduce producers' willingness to adopt KV as compared to MLV.

**Table 4** reports, for various outbreak intervals, the percent of simulation iterations in which vaccination enjoys positive expected annual net benefit. The KV vaccine's probability of yielding positive expected net benefit falls sharply from 97 to 42% as outbreak interval lengthens from 5 to 10 years. And for producers facing a 20-year or longer outbreak interval, there is zero probability that a KV vaccine will generate positive expected net benefit. For the MLV vaccine, in contrast, there is a 100% chance of positive expected net benefit for outbreak intervals of 5, 10, and 20 years. Only at an outbreak interval of 50 years does this probability fall to 77%. This reflects, again, the MLV vaccine's lower assumed cost, and highlights its important economic implications.

# Epizootic versus Endemic Outbreaks

A sheep operation's location and history of disease play an important role in the expected net benefit of vaccinating. Producers in high-frequency, low-virulence areas, who face regular but mild outbreaks, may face a different risk than producers in lowfrequency areas with no recent history of the disease and thus naïve sheep flocks and severe outbreaks.

**Table 5** reports two iterations from the @Risk simulation to put expected annual net benefit of vaccination (using an MLV vaccine) into a geographic context. We have hand-selected two iterations that share the same historical mean lamb price, \$130.36 (25), but exhibit different outbreak characteristics. One iteration represents conditions typical of the Big Horn Basin, where sheep flocks have experienced outbreaks relatively infrequently (e.g., roughly every 10 years) and relatively severely (e.g., 22% morbidity, 20% mortality). The other iteration represents conditions typical of eastern Wyoming, where flocks have experienced outbreaks more frequently (e.g., roughly every 5 years) yet less severely (e.g., 6% morbidity, 7% mortality). The Big Horn Basin iteration is chosen from among the 50,000 MLV iterations underlying **Figure 4** (i.e., a 10-year outbreak interval). The eastern Wyoming iteration is chosen from among 50,000 MLV iterations underlying a similar (unpublished) figure for a 5-year outbreak interval.

Vaccination is less beneficial for producers located in a "lower" risk (i.e., more frequent thus less severe outbreaks) area compared

Bluetongue (BT) morbidity rate, and BT mortality rate. MLV's net benefit exceeds the maximum net benefit of KV in 33.6% of the 50,000 iterations.

to those in a "higher" risk (i.e., less frequent thus more severe outbreaks) area (**Table 5**). Ironically, producers that experience outbreaks less frequently may also be less likely to administer the vaccine (32). For producers in areas with shorter outbreak intervals and lower risk of high-severity outbreaks (e.g., eastern Wyoming), lamb prices may be a significant factor in their decision to vaccinate or not. Vaccination might not be profitable in years with unusually low lamb prices. Increased BT forecasting would give producers in low-risk areas the ability to vaccinate only in years when lamb prices are high enough to make vaccination profitable, thereby decreasing vaccination costs. This is a promising area for future research.

Table 4 | Percentage of iterations in which vaccination with modified-live virus (MLV) versus killed virus (KV) has positive expected annual net benefit, for various outbreak intervals, on a 640-ewe operation.