Direct costs of five foot-and-mouth disease epidemics in the Republic of Korea, from 2000 to 2011

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1 pissn , eissn J. Prev. Vet. Med. Vol. 37, No. 4: , Decem ber Direct costs of five foot-and-mouth disease epidemics in the Republic of Korea, from 2000 to 2011 Han Kim 1, Hachung Yoon 1, Oun-Kyong Moon 1, Jun-Hee Han 1, Kyuyoung Lee 1, Wooseog Jeong 1, Jida Choi 1, Young-Mi Cho 1, Yong-Myeong Kang 1, Hyo-Young Ahn 1, Do-Soon Kim 1, Tim E Carpenter 2, 1 Veterinary Epidemiology Division, Animal and Plant Quarantine Agency, Anyang , Republic of Korea 2 EpiCentre, Massey University, Palmerston North, New Zealand Abstract: Foot-and-mouth disease (FMD) has great potential for causing huge economic loss and was the first disease identified by the World Organisation for Animal Health (OIE) in its official list of free countries and zones. This study examined the governmental expenditures for five FMD epidemics that occurred in the Republic of Korea between 2000 and The costs of an epidemic ranged from 26 billion Korean won (KRW, approximately 23.6 million US dollars, $) to a maximum of 2,044 billion KRW (US$ 1.9 billion). For two epidemics in which vaccinations were implemented, the costs were higher than those epidemics without vaccination. The mean cost for an outbreak ranged from 0.5 billion KRW (US$ 4.5 million) for the 2010/2011 epidemic to 18.2 billion KRW (US$ 16.5 million) for the 2000 epidemic. Mean costs per infected premises were 7.0 billion KRW for cattle farms (95% CI: ), 1.38 billion KRW for pig farms ( ), 0.11 billion KRW for deer farms ( ), and 0.10 billion KRW for goat farms ( ). The highest cost for an outbreak in cattle seemed associated with the number of outbreak cattle farms in two epidemics in which vaccination was implemented. Key words: Foot-and-mouth disease, cost, economic impact, epidemic INTRODUCTION Foot-and-mouth disease (FMD) is a highly contagious disease affecting cloven-hoofed animals, caused by the FMD virus belonging to the family Picornaviridae and genus Aphthovirus [15, 16]. FMD has great potential for causing huge economic losses and was the first disease identified by the World Organisation for Animal Health (OIE) in its official list of free countries and zones. Currently, FMD is present in more than 100 countries in the world, primarily in less developed countries, where it is often endemic [7]. When the disease is introduced into an FMD-free country, an outbreak may be more economically disruptive than in endemic countries. Susceptible animals on infected farms and surrounding areas are often culled to eradicate the disease, and international trade in animal products is suspended [12]. Therefore, FMD not only affects farms raising livestock but also damages a nation s livestock industry and economy. The components of the economic impact are divided into two categories, direct and indirect costs. The direct costs of an FMD outbreak include cost of disease management, immediate losses to animal production and livestock industry, while the indirect costs are mainly related to disruption of local economies and environmental impacts [5, 17]. The majority of the exotic disease control costs are spent by the government and are associated with compensation for slaughter, disposal, cleaning and disinfecting of premises and administration costs to implement control measures [18]. This study examined the governmental expenditures for five FMD epidemics that occurred in the Republic of Korea between 2000 and Prior to the 2000 FMD epidemic, Korea had been FMD-free, since Following the 2000 FMD epidemic, the FMD virus was reintroduced in 2002 [14] and on three separate occasions in The aim of the present study was to quantify the farm-level costs for an FMD outbreak, considering such factors as farm type, primary infected animal species, season and vaccination. Received 07 November 2013, Revised 03 December 2013, Accepted 18 December 2013 Corresponding author. Tim E Carpenter. EpiCentre, Massey University, Palmerston North, New Zealand. Tel: , Fax: , t.e.carpenter@ massey.ac.nz Copyright 2013 The Korean Society of Preventive Veterinary Medicine. The full text is freely available on the web at MATERIALS AND METHODS The information on outbreaks, control measures, and governmental expenses for the five epidemics of FMD in

2 164 H Kim, H Yoon, O-K Moon, J-H Han, K Lee, W Jeong, J Choi, Y-M Cho, Y-M Kang, H-Y Ahn, D-S Kim, TE Carpenter Korea were referenced from a whitepaper on FMD epidemics published by the concerned governmental ministry [11] and from a source book for the surveillance committee of animal disease control in Korea [2]. For each epidemic, the number of outbreak farms was listed by animal species (e. g. cattle, pig, goats and deer) and costs for each species. Then, to find a representative value for costs by animal species, a data sheet with 31 records, for which the values of the variables were averages of the combinations for these five epidemics, was established. An equation including the number of outbreak farms and cost per outbreak by species was established with the weighted average by the inverse of the variance as follows: Mean cost per Outbreak = (number of outbreak farm i cost of outbreak per farm i) where, i means species. The most suitable values for the cost of each species were found with the solver function of Excel (Microsoft, USA). 95% confidence interval (95% CI) was estimated, with the deviation between the suitable value found by the solver function and each of the 31 records. RESULTS Table 1 presents the information on the five epidemics of FMD that occurred in Korea between 2000 and FMD virus type O was responsible for four epidemics and type A was responsible for one. The costs of the epidemics ranged from 26 billion Korean won (KRW) for the virus type A epidemic in 2010 to 2,044 billion KRW in the 2010/ 2011 epidemic for the type O virus. Vaccination was implemented in two epidemics in 2000 and 2010/2011. For the two epidemics, mean costs were higher than epidemics without vaccination. Mean cost per outbreak farms ranged from 0.5 billion KRW for the 2010/2011 epidemic to 18.2 billion KRW for the 2000 epidemic. The season and species of the index farm seemed to have nothing to do with determining the total cost of an epidemic (Table 1). The mean costs per one outbreak farm were 7.0 billion KRW for cattle farms (95% CI: ), 1.38 billion KRW for pig farms (95% CI: ), 0.11 billion KRW for deer farms (95% CI: ), and 0.10 billion KRW for goat farms (95% CI: ). The costs for an FMD outbreak in a cattle farm was five times higher than that of a pig farm, while the costs for a goat or deer farm were Table 1. Outbreak situation of foot-and-mouth disease epidemics and costs spent on five epidemics in the Republic of Korea between 2000 and 2011 Epidemic year (virus strain) 2000 (O 1) 2002 (O 1) 2010 (A) 2010 (SEA O) 2010/2011 (SEA O) Outbreak time (season) Mar. 24 Apr. 15 (spring) May. 2 Jun. 23 (spring) Jan. 2 Jan. 29 (winter) Apr. 8 May. 6 (spring) Nov. 28 Apr. 21 (winter) Number of outbreak farms (by species) 15 (Cattle 15) 16 (Cattle 1, Pig 15) 6 (Cattle 6) 11 (Cattle 7, Pig 4) 3,748 (Cattle 1,934, Pig 1,727, Goat 44, Deer 43) Vaccination Ring vaccination to slaughter No vaccination No vaccination No vaccination Vaccination to live Species of index farm Total cost (KRW)* Cost per outbreak farm (KRW) Cattle Pig Cattle Cattle Pig billion billion 26.2 billion billion 2,044.5 billion 18.2 billion 6.6 billion 4.4 billion 9.2 billion 0.5 billion * KRW : Korean Won Mean cost per outbreak farm = Total cost / Number of outbreak farms SEA : Southeast Asia

3 Direct costs of five foot-and-mouth disease epidemics in the republic of Korea, from 2000 to ten times lower than that of a pig farm (Fig. 1). DISCUSSION This study analyzed the economic impacts from five epidemics of FMD that occurred in Korea and found that the cost per one outbreak was the highest in cattle farms. In the case of foreign countries, the economic impacts of FMD were estimated using data analysis or simulation. FMD-free countries, such as Canada, USA, France and Australia [8 10, 13], simulated the economic impacts, while countries that suffered from FMD outbreaks, including Bhutan, Taiwan, Sudan and United Kingdom, used real outbreak data for the analysis [1, 4, 19, 20] summarized in Table 2. The lowest cost was reported in California, U.S.A. in 1929 with 0.11 million dollars spent for five outbreak herds [6]. The most expensive epidemic was associated with a detection delay. The simulated economic losses on national agriculture in the U.S.A. were billion dollars due to detection delays of 7 22 days in a dairy cattle farm located in California [5]. In other simulation study reported an estimated potential revenue impact of an FMD outbreak in the U.S.A. for a similar outbreak in the United Kingdom during In reference to the financial situation of the U.S.A. in year 1999, the estimated appraised cost was 14.0 billion dollars for control measures [13]. The smallest estimation was less, while the largest was more than the costs spent for the five FMD epidemics in Korea, where the lowest cost was 23.8 million dollars (exchange rate, 1,100 KRW to 1 USD) and the highest was 1.9 billion dollars. The economic losses varied extremely according to a country s own situation and control measures implemented. For example, in Taiwan, the costs estimated were different for two different Fig. 1. Cost of foot-and-mouth disease for one outbreak farm by animal species; estimated costs based on the expenses of five epidemics in the Republic of Korea between 2000 and Table 2. Estimated economic impacts for the outbreak of foot-and-disease in the world by data analysis or simulation Continent Outbreak country Analysis Outbreak year Infected herds (heads) Type of species Control measures Appraised cost Reference Bhutan Data analysis Endemic ( ) 111 outbreaks Cattle, yak, pig, goat, sheep Average vaccination 71,000 dose $0.15 million per year [19] Asia Taiwan Data analysis ,000 6,147 (> 4 Million) Pig Slaughter 4 million Slaughter 4 million, vaccine $379 million $1.6 billion [20] Africa South Sudan Data analysis Prevalence acute (15.8%), chronic (2.6%) Cattle Vaccination $2.5 million + vaccine $0.2 million [3]

4 166 H Kim, H Yoon, O-K Moon, J-H Han, K Lee, W Jeong, J Choi, Y-M Cho, Y-M Kang, H-Y Ahn, D-S Kim, TE Carpenter Table 2. Continued Continent North America Europe Outbreak country Canada USA, California USA France, Brittany Analysis Simulated (scenario 1) Simulated (scenario 2) Outbreak year (use data) Infected herds (heads) Outbreak in herds Large scale outbreak (eastern Canada) Type of species Control measures Quick slaughter (1,500 2,000 heads) Slaughter (6 month program) Appraised cost $2.0 billion $2.8 billion Data analysis (109,855) - $4.35 million Data analysis (3,591) goat, sheep - $0.11 million Simulation Simulation 2006 (Survey data) 1999 (use data) Simulated United Kingdom Data analysis (2030) Australia Australia Simulated (3 month - 1 year) $ : US dollar, F. : France franc, : British pound, AUD : Australian dollar. This table was reconstructed based on Knight-Jones & Rushton [9]. - goat, sheep lamb, sheep goat, sheep sheep sheep Diagnostic delay 7 22 days $ billion Reference [8] [6] [5] - $14.0 billon [13] Stamping out of affected herds (SO) SO and dangerous contact herds SO + early vaccination Slaughter 7 million F.243 million F.211 million F.944 million $ billion [9] [1] Slaughter 3.1 billion [18] Slaughter + export loss AUD billion [10] situations: with and without vaccination. Although the number of outbreak farms in the 1997 epidemic in Taiwan (6,000 farms) were higher than that of the 2010/2011 epidemic in Korea (3,748 farms), the estimated value without vaccination (slaughter policy) was four times lower than that of the Korean epidemic [2, 11]. However, when vaccination was added to the control measures, the cost increased to a comparable level to the Korean outbreak [20]. Adopting emergency vaccination may sometimes cause problems in regaining an FMD free status as well as increasing economic losses as in the Netherlands [3]. In contrast to a study performed on FMD endemic Pakistani dairy cattle in which inhibiting the appearance of clinical symptoms of FMD by implementing a strain-matched high quality vaccine reducing the damage associated with decreased milk production under the condition that all animals at all study farms were vaccinated, economic analyses done either in Korea or in other countries referenced in this study consistently showed that the cost of an epidemic was higher when vaccinations were implemented [4, 5, 9, 11, 20]. The highest cost for an outbreak in cattle, estimated in the present study for epidemics in Korea, seemed associated with the number of outbreak cattle farms in two epidemics in which vaccinations were implemented. Economic impacts varied throughout the world because the environment and circumstances resulted in different outbreak situations. The actions of farmers also affected the risk of FMD outbreak in other farms. The range of economic effects included in the cost analysis studies de-

5 Direct costs of five foot-and-mouth disease epidemics in the republic of Korea, from 2000 to pended on the authors points of view about the economic impacts of the epidemic. The facts imply that an FMD epidemic can only affect farmers and the regional economy of an outbreak area, and also affect a whole country according to the impression of the people associated with the outbreak. Raising public awareness with economic impacts on the society may help educate the general public on not doing risky behaviors such as visiting farms in FMD outbreak countries and bringing animal products home from overseas trips. ACKNOWLEDGMENTS This study was funded by the Research and Development program of the Animal and Plant Quarantine Agency [Project No. I ]. REFERENCES 1. Anderson I. Foot and mouth disease: lessons to be learned. Inquiry Report HC888. House of commons papers London, Great Britain Department for Environment, Food and Rural Affairs, Animal and Plant Quarantine Agency (QIA). Analysis of FMD outbreak status and management of risk factors. In: Source Book for Surveillance Committee of Animal Disease Control, Anyang, Republic of Korea, Backer JA, Hagenaars TJ, Nodelijk G, van Roermund HJ. Vaccination against foot-and-mouth disease I: epidemiological consequences. Prev Vet Med. 2012, 107(1-2): Barasa M, Catley A, Machuchu D, Laqua H, Puot E, Tap Kot D, Ikiror D. Foot-and-mouth disease vaccination in South Sudan: benefit-cost analysis and livelihoods impact. Transbound Emerg Dis. 2008, 55(8): Carpenter TE, O'Brien JM, Hagerman AD, McCarl BA. Epidemic and economic impacts of delayed detection of foot-and-mouth disease: a case study of a simulated outbreak in California. J Vet Diagn Invest. 2011, 23(1): Ekboir JM. Potential impact of foot and mouth disease in California : The role and contribution of animal health surveillance and monitoring services. Agricultural Issues Center, Division of Agriculture and Natural Resources, University of California, Jamal SM, Belsham GJ. Foot-and-mouth disease: past, present and future. Vet Res. 2013, 44(1): Krystynak RH, Charlebois PA. The potential economic impact of an outbreak of foot-and-mouth disease in Canada. Can Vet J. 1987, 28(8): Mahul O, Durand B. Simulated economic consequences of foot-and-mouth disease epidemics and their public control in France. Prev Vet Med. 1999, 47(1-2): Matthews K. A review of Australia s preparedness for the threat of foot-and-mouth disease. pp , Australian Government Department of Agriculture, Fisheries and Forestry, Ministry for Food, Agriculture, Forestry and Fisheries (MIFAFF). White paper on the Foot and Mouth Disease. Gwacheon, Republic of Korea, Muroga N, Kobayashi S, Nishida T, Hayama Y, Kawano T, Yamamoto T, Tsutsui T. Risk factors for the transmission of foot-and-mouth disease during the 2010 outbreak in Japan: a case-control study. BMC Vet Res. 2013, 9: Paarlberg PL, Lee JG, Seitzinger AH. Potential revenue impact of an outbreak of foot-and-mouth disease in the United States. J Am Vet Med Assoc. 2002, 220(7): Park JH, Ko YJ, Kim SM, Lee HS, Heo EJ, Lee KN, Cho IS. Surveillance of foot-and-mouth disease in Korea. Kor J Vet Publ Hlth. 2009, 33(3): Park JH, Lee KN, Kim SM, Ko YJ, Lee HS, Heo HJ, Kweon CH, Yang CB. The condition for air-borne transmission of foot-and-mouth disease. Kor J Vet Publ Hlth. 2008, 32(3): Park JH, Lee KN, Ko YJ, Kim SM, Lee HS, Shin YK, Sohn HJ, Park JY, Yeh JY, Lee YH, Kim MJ, Joo YS, Yoon H, Yoon SS, Cho IS, Kim B. Control of foot-and-mouth disease during epidemic, South Korea. Emerg Infect Dis. 2013, 19(4): Roigen L, Koo[manschap MA, Rutten FFH, Maas PJ. Indirect costs of diseases; an international comparison. Health Policy. 1995, 33: Thompson D, Muriel P, Russell D, Osborne P, Bromley A, Rowland M, Creigh-Tyte S, Brown C. Economic costs of the foot and mouth disease outbreak in the United Kingdom in Rev Sci Tech. 2002, 21(3): Tshering P. An economic evaluation of the impact of foot and mouth disease and its control in Bhutan. VEERU, University of Reading, UK, Yang PC, Chu RM, Chung WB, Sung HT. Epidemiological

6 168 H Kim, H Yoon, O-K Moon, J-H Han, K Lee, W Jeong, J Choi, Y-M Cho, Y-M Kang, H-Y Ahn, D-S Kim, TE Carpenter characteristics and financial costs of the 1997 foot-andmouth disease epidemic in Taiwan. Vet Rec. 1999, 145 (25):