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  • 1. Downloaded from on January 2, 2011 - Published by Epidemiological characteristics and financial costs of the 1997 foot-and-mouth disease epidemic in Taiwan P. C. Yang, R. M. Chu, W. B. Chung, et al. Veterinary Record 1999 145: 731-734 doi: 10.1136/vr.145.25.731 Updated information and services can be found at: These include: References Article cited in: Email alerting Receive free email alerts when new articles cite this article. Sign up in the service box at the top right corner of the online article. NotesTo request permissions go to: order reprints go to: subscribe to BMJ go to:
  • 2. Downloaded from on January 2, 2011 - Published by PAPERS & ARTICLES Africa, Stellenbosch University Printers UNITED STATES DEPARTMENT OF AGRICULTURE (1993) Supplement to SHAKESPEARE, A. S. (1996) Clinical cases illustrating causes of recumbent the draft environmental impact statement. Animal Damage Control ostriches. In Improving our Understanding of Ratites in a Farming Program. Washington DC, USDA Environment. Ed D. C. Deeming. Oxfordshire, Ratite Conference. pp 55-57 VAN PUTTEN, G. & ELSHOF, W. J. (1978) Observations on the effect of trans- SKADHAUGE, E., DAWSON, T. J., PRYS-JONES, R. & WARUI, C. N. (1996) port on the well-being and lean quality of slaughter pigs. Animal Regulation The role of the kidney and the gut in osmoregulation. In Improving our Studies 1, 247-271 Understanding of Ratites in a Farming Environment. Ed D. C. Deeming. WOTTON, S. B. & HEWITT, L. (1997) The humane destruction of large poul- Oxfordshire, Ratite Conference. pp 115-122 try flocks. Proceedings of the 5th Symposiumm of Poultry Welfare. SMITH, G. A. (1993) Ostrich chick survival presents challenge. Journal of the Wageningen, The Netherlands American Veterinary Medical Association 203, 5 YAGIL, R.,VAN CREVELD, C., MARKOWITZ, E. & LEVY,A. (1996) Urine pro- TARRANT, P.V., KENNY, E J., HARRINGTON, D. & MURPHY, M. (1992) Long duction and health status in ostriches. In Improving our Understanding of distance transportation of steers to slaughter; effect of stocking density on phys- Ratites in a Farming Environment. Ed D. C. Deeming. Oxfordshire, Ratite iology, behaviour and carcass quality. Livestock Production Science 30,223-238 Conference. p 59 Epidemiological characteristics and financial costs of the 1997 foot-and-mouth disease epidemic in Taiwan P. C. YANG, R. M. CHU, W. B. CHUNG, H. T. SUNG Between March and July 1997, a devastating outbreak of foot-and-mouth disease (FMD), serotype 0, occurred in pigs in Taiwan. A total of 6147 pig farms with more than 4 million pigs were infected, and 37-7 per cent of the pigs in Taiwan either died (0-18 million pigs) or were killed (3-85 million pigs). The epidemic reached its peak during the fifth week after it was first recognised. During the eighth and ninth weeks, a two-dose blanket vaccination programme was instituted which led to a large reduction in new outbreaks. Except for two cities, the whole of Taiwan was declared an FMD-infected zone. During the four months in which new farm outbreaks occurred, 21-7 per cent of the pigs on infected farms showed clinical signs, and there was an overall mortality of 3-95 per cent. During the early stages of the epidemic, the incubation period was as short as 24 hours and the case fatality rates for suckling piglets reached 100 per cent. The financial cost of the epidemic was estimated at usS 378-6 million, including indemnities, vaccines, carcase disposal plus environmental protection, miscellaneous expenses, and loss of market value. Owing to the ban on exports of pork to Japan, it is estimated that the total economic cost to Taiwans pig industry will be about us$ 1-6 billion.Veterinary Record (1999) FOOT-AND-MOUTH disease (FMD) is a highly contagious MATERIALS AND METHODS145, 731-734 viral disease affecting cattle, pigs, sheep, goats, and other cloven-hoofed domestic and wild animals (House and House Control strategiesP. C. Yang, DVM, PhD, 1992, Fenner and others 1993). Two previous epidemics of A policy of depopulating each infected farm and vaccinatingDepartment of FMD have occurred in Taiwan (Ryu 1984), the first between all the pigs on farms at high risk was adopted immediatelyComparative Medicine, 1913 and 1916, and the second between 1924 and 1929. after each farm outbreak of FMD was confirmed. As the dis-Pig Research Institute Following the eradication of FMD after the second epidemic ease continued to spread, it was decided during late April toTaiwan, Chunan Miaoli Taiwan remained free of the disease for over 68 years. vaccinate every pig in Taiwan. Vaccines made from strains of35046, Taiwan The latest epidemic of FMD was identified in pigs in March 0 4174, O, Campos and O-Manisa were recommended byR. M. Chu, DVM, PhD, 1997 (Donaldson 1997) and within four months had spread the wRL on the basis of the evaluation of r, values (KitchingDepartment of Veterinary over the entire island, leading to the immediate closure of the and others 1989). When every pig in Taiwan had received atMedicine, National export market and heavy economic losses (Shieh 1997). least one dose of the FMD vaccine, the eradication policy wasTaiwan University, Taipei The first suspected case of FMD was observed on a pig farm changed from the complete depopulation of infected farms106, Taiwan on March 14,1997. Samples of vesicular fluid, epithelium, and to destroying only clinically ill pigs (Shieh 1997).W. B. Chung, DVM, PhD, serum from clinically sick pigs were sent to the Taiwan Animal Restrictions on the movement of pigs from infected farmsDepartment of Veterinary Health Research Institute for diagnosis (Shieh 1997) and FMD were implemented on March 20, to halt the spread of the dis-Medicine, National was confirmed on March 19. Samples ofvesicular epithelium ease. In addition, on March 22, the central governmentPingtung University of were promptly dispatched to the World Reference Laboratory announced a shipping ban on all cloven-hoofed animals andScience and Technology, (wRL) for FMD at Pirbright, UK, for further confirmation, and their meat products to the three counties along the easternPingtung 912, Taiwan serotype 0, referred to as 0 Taiwan, was confirmed and coast of Taiwan and to all the offshore islands.H. T. Sung, DVM, PhD, reported on March 25 (Donaldson 1997). To minimise the spread of FMD in the eastern part ofBureau of Animal and Outbreaks due to the same strain of FMD virus continued Taiwan, a protection zone with a radius of 3 km and a sur-Plant Health Inspection and the epidemic lasted about four months, with the last new veillance zone with an additional radius of 3 km were declaredand Quarantine, Council outbreak being reported on July 15. This paper describes the around each infected premises. Owing to the shortage of vac-of Agriculture, Taipei 100, epidemiological characteristics and financial cost of this epi- cine between late April and early May, it was decided to vac-Taiwan demic of FMD. cinate all animals in the surveillance zone first. When more The Veterinary Record, December 18/25, 1999 731
  • 3. Downloaded from on January 2, 2011 - Published by group.bmj.comPAPERS & ARTICLESC, 1200 O. o Ia).Gc. 1000 zDca) 3800cE0 600 a) a)M0 400n 200 - Cumulation of infected herdsE 4215 5Z Q 0 1 0 0- 2 1 0 0 2000. - Cumulation of depopulated herds o co N. , LO 0) cm co 0 CO CN 0 7- C~ r C~ r C~ t cm (D o _ Api c 0) cM C) CD cm 1000* March April May July JuneFIG 1: Epidemic curve of the outbreaks of foot-and-mouth 6 12disease in Taiwan in 1997. * March 29, started massvaccination, t May 3, started blanket vaccination March April May June July 1997vaccines became available, the order of priority for vaccina- FIG 2: Cumulative numbers of FMD-infected herds and herds being depopulatedtion in the protection zone was first, the sows and piglets, thenthe nearly finished fattening pigs, and finally the weanling pigsand animals of other susceptible species. cloven-hoofed animals and their meat products from Taiwan proper successfully protected the offshore islands of Penghu,Data analysis Green Island, Orchid Island, Kinman and Matzu, and theyThe analysis is based on data obtained from agricultural sta- have remained free of FMD.tistics (Taiwan Agricultural Yearbook 1997), the daily records The number of newly infected farms decreased signifi-of outbreaks of FMD, an epidemiological questionnaire, and cantly five weeks after the initial recognition of the reports from government agencies. The daily records The effectiveness of the control measures became especiallyof the outbreak identified the number of newly infected marked by the ninth week (May 9 to May 15), one week afterfarms, the number of pigs on each farm, the number of pigs a second dose of vaccine had been administered to all cloven-with clinical signs, their mortality, and the number ofinfected hoofed animals in the country. The number of new outbreaksfarms being depopulated. In late May, an epidemiological sur- continued to decrease, with only five newly infected farmsvey was conducted by sending questionnaires to 41 pig pro- being identified during June and two during the first week ofducers. Sixteen of them reported being affected by FMD, and July. On July 15, Taichung County reported the last newlythe epidemiological data were collected and analysed. The infected farm, and the epidemic came to an end. It wasfinancial costs of the outbreak were analysed by using expense remarkable that no clinical cases of FMD were reported inaccounts for the purchase of vaccines, indemnity payments todepopulated farms, the cost of the disposal of carcases, and Taipei Countymiscellaneous payments.RESULTSThe first suspected case of FMD was reported on a pig farmin Hsinchu County on March 14, 1997, the second wasreported on another pig farm in the same county on March17, and the third in Taoyuan County on March 18. By the timethe Council of Agriculture announced the confirmation ofoutbreaks of FMD in Taiwan on March 20, the disease hadbeen identified on 28 farms in 10 counties or cities, and byMarch 27 it had been identified on 217 pig farms alongTaiwans western coast. The epidemic curve (Fig 1) peakedduring the fifth week, April 11 to April 17, with 1113 newlyinfected farms identified. By the end of March, among the 19counties and cities on the western coast, 17 were classified asFMD-infected zones, the two cities, Taipei and Keelung, beingthe only exceptions. The disease was restricted to the west-ern coast until April 21, when an outbreak of FMD occurredin Ilan County, in north-east Taiwan. Epidemiological inves-tigations showed that the possible source of infection was thefeeding of uncooked swill from uncertain sources. Two dayslater, on April 23, another outbreak occurred in TaitungCounty, in south-east Taiwan. On May 3, Hwalien County on FIG 3: Distribution ofthe eastern coast of Taiwan became the last area to be infected outbreaks of foot-and-by FMD. mouth disease in As shown in Fig 3, the whole of Taiwan except Taipei and Taiwan in 1997. Each dotKeelung cities was eventually classified as an FMD-infected represents an FMDV-zone. The blanket vaccination and a shipping ban on all infected farm732 The Veterinary Record, December 18/25, 1999
  • 4. Downloaded from on January 2, 2011 - Published by PAPERS & ARTICLES Million % of total Carcase disposal method (%) Expenses (million us$) (%) Items us$ costs Burying 80 8.0 32-5 Indemnity of pigs slaughtered 187.5 49.5 Rendering 15 64 26.1 Cost of vaccines 13-6 3-6 Burming or incinerating 5 10-2 41.4 Carcase disposal and environmental protection 24-6 6-5 Total 100 24-6 100-0 Miscellaneous expenses 27.9 7-4 Loss of market value 125-0 33.0 Total costs 378-6 100-0 during the four-month epidemic was estimated at try us$125-0 million, 33 per cent of the total financial cost. The total financial cost of the 1997 FMD epidemic in Taiwan wasruminant animals throughout the epidemic, despite the fact estimated at us$378-6 million (Table 1).that on some of the infected pig farms there were cattle or After negotiations between the government and the piggoats on the premises or in close proximity. producers association, the indemnity price for non-diseased During the four months of the epidemic, 6147 farms were pigs destroyed on infected farms was set at us$85-7 for a 100identified as infected; the farm incidence rate was 24-2 per kg pig and us$12*5 for pigs less than 25 kg. For pigs of inter-cent. The total number of pigs on the infected farms was mediate weight the indemnity price was adjusted according4,658,515, of which 1,011,674 (21.7 per cent) showed clini- to their actual weight. For registered breeding stock, thecal signs and 184,231 (3.95 per cent) died; the overall case indemnity price was set at us$171-4 per pig. Within a weekfatality rate was 18 2 per cent. Suckling piglets had the high- of the official announcement of the FMD outbreak by theest mortality, reaching 100 per cent during the first stage of Council of Agriculture, pig prices decreased by nearly 70 perthe epidemic when the entire population had no immunity cent, from us$200 to us$60 per 100 kg liveweight. With pigagainst the FMD virus. Older pigs generally had a much lower production costs estimated at us$140 per 100 kg liveweight;mortality, ranging between 5 and 20 per cent. Observations even uninfected farms were severely affected. The pig pricemade on the infected farms indicated that the course of the returned to us$140 briefly during mid and late May when theclinical disease might range from a minimum of 10 days up epidemic was under control, but fell again to us$1 10 per 100to 38 days (average 22 days) with a very short incubation kg liveweight during the remainder of 1997.period of 24 to 48 hours. The first animals to show clinical Of the 4-03 million pig carcases disposed of under gov-signs were usually larger pigs, either finishers or sows, fol- ernment supervision, 80 per cent were buried, 15 per centlowed by younger pigs. Once a lactating sow developed vesic- were rendered, and 5 per cent were incinerated or burned inular lesions on its mammary glands and teats, the entire litter open fields (Table 2). An analysis of the cost effectiveness ofof suckling pigs would often die overnight. these three disposal methods showed that burying was the The total number of pigs destroyed was 4-03 million, cheapest and easiest way to handle large quantities of deadroughly 37-7 per cent of Taiwans entire population of pigs; animals, with 32-5 per cent of the total disposal costs cover-3-85 million pigs (95-5 per cent) were destroyed in the erad- ing 80 per cent of the carcases. Rendering was more expen-ication programme and only 184,231 (4-5 per cent) died of sive, with 26.1 per cent of the total expense being used toFMD. During the first month of the epidemic the eradication dispose of 15 per cent of the carcases, and burning or incin-campaign lagged far behind the rate of confirmation of new erating was the most expensive, with 41-4 per cent of the totalFMD-infected farms and it was unable to catch up until mid- expense being used to dispose of only 5 per cent of the car-May (Fig 2). Many infected farms had to be put on a waiting cases. The method of carcase disposal was selected on thelist for one to four weeks before the herd could be slaughtered, basis of the following considerations: the availability of land-owing to the lack of skilled and unskilled manpower, equip- fill sites (either private or public), the level of the water table,ment and experience in destroying large numbers of animals, proximity to human residence, the availability of incinerators,in addition to the difficulties of carcase disposal. The short- and other environmental factors.age of manpower was alleviated by drafting in military per- In addition to the direct economic losses, the pig andsonnel during April and May, enabling the programme to related industries continue to suffer severe financial losses. Aseliminate up to 200,000 pigs per day during mid-April, and a result of the ban on the export of pork to Japan, an esti-allowing the eradication operation to catch up with the recog- mated loss of us$1-6 billion will be incurred by the Taiwan pignition of newly infected farms by mid-May. industry. Among other businesses affected, feed mills, the Among the 6147 infected farms, 5674 (92-3 per cent) were pharmaceutical industry, meat packers for exportation, farmlocated in the top five pig-producing counties, all situated on equipment manufacturers and suppliers, livestock markets,the western coast, and accounting for about 78-1 per cent of and the transportation industry were the hardest hit. Overthe total pig population. The overall prevalence of FMD infec- 65,000 jobs have been lost in these affected businesses dur-tions on the western coast was 24-3 per cent (6144 of 25,288 ing or after the epidemic.pig farms), whereas on the eastern coast it was only 0-2 percent (three of 1398 pig farms). The intensity of the epidemicis illustrated in Fig 3. DISCUSSION The Taiwan government bore approximately 49-5 per centof the total financial cost of the epidemic, providing us$187-5 Four major factors were responsible for the rapid spread ofmillion. The total cost of 21 million doses of vaccine was this epidemic of FMD in Taiwan: the inability of the govern-us$13-6 million, 3-6 per cent of the total financial cost. The ment to shut down the livestock auction markets; the longexpenses for carcase disposal and environmental protection delays before infected farms could be depopulated in the erad-were estimated at us$24-6 million, 6-5 per cent of the total ication programme; the high density of pig farms; and thefinancial cost. Other miscellaneous expenses such as disin- inadequate quantity of vaccines available during the emer-fectants, disposable coveralls, boots, gloves, syringes, electro- gency.cution devices, lime, rent for bulldozers, transportation, and First, the livestock auction markets were found to haveso forth were estimated at us$27-9 million, 7-4 per cent of the been a source of transmission of the FMD virus. Although thetotal financial cost. The loss of market value to the pig indus- government implemented health requirements for market-The Veterinary Record, December 18/25, 1999 Veterinary Record, 18/25,1999 733
  • 5. Downloaded from on January 2, 2011 - Published by group.bmj.comPAPERS & ARTICLESweight hogs entering auction markets immediately after the licity about the epidemic. Fear that FMD might be a zoonoticoutbreak, infected pigs which were showing no clinical signs disease and that pork might not be safe, and ethical concernsled to the transmission and dissemination of the virus by the about the methods of destroying healthy pigs, were majormovement of pigs between farms. A complete shutdown of all consumer concerns. A decrease of 28 per cent in the domes-auction markets was not feasible because Taiwanese people tic demand for pork was observed during the first month ofare used to consuming fresh pork obtained through the daily the epidemic, but the market gradually recovered and wasmovement of live market-weight pigs from production areas, back to normal byAugust 1997, five months after the first out-mainly in the southern part of the island, through the 21 auc- break was announced.tion markets throughout Taiwan. An attempt early in the epi- When the direct economic losses due to this FMD epidemicdemic to shut down the auction markets for five days, in an were analysed, it became obvious that mass vaccination wasattempt to stabilise the plummeting prices, did not achieve the cheapest way to control the spread of the disease. The vac-this goal. cine costs accounted for only 3-6 per cent compared with 49 5 Secondly, the infected farms waiting to be depopulated per cent for indemnity of the direct economic losses.during the early stages of the epidemic continued to be However, in the long run, since vaccination was and contin-sources of transmission of the virus. Infected pigs may each ues to be so widely practised, Taiwan will have difficulty inshed 108 6 TCID50 of virus per day (Donaldson and others regaining its status as an FMD-free country without vaccina-1982). The entry of FMD into new herds was reported repeat- tion. Continuing cost-benefit analyses are needed to evalu-edly during the first month of the epidemic in spite of strict ate whether vaccination and limited depopulation or totalbiosecurity measures. depopulation may have more beneficial long-term economic Thirdly, the population density of pigs in Taiwan is effects on pig producers.extremely high. Eighty-three per cent of the entire pig popu-lation was concentrated in the south western region of Taiwanwhich contained approximately 1922 pigs per km2 of culti- ACKNOWLEDGEMENTSvated land. This region was the hardest hit by the epidemic(Fig 3). The authors wish to thank Dr George Beran at the Veterinary Finally, the quantity of vaccines imported was not suffi- College of Iowa State University for modifying this manu-cient to create an immune blanket during the first month of script. The Council of Agriculture funded the work throughthe epidemic. On most farms only a partial vaccination pro- theHog Cholera and FMD Eradication Programmesgramme could be applied until early May. As a result, manypartially vaccinated farms became infected. A supply of 15million doses of 01 Campos vaccine which arrived between Referenceslate April and early May made it possible to halt the further DONALDSON, A. I. (1997) Foot-and-mouth disease in Taiwan. Veterinarytransmission of the virus. Record 140, 407 Pig farms in the three eastern coastal counties were the DONALDSON, A. I., FERRIS, N. P. & GLOSTER, J. (1982) Air sampling of pigsleast affected. In addition to the relatively low density of the infected with foot-and-mouth disease virus: comparison of Litton andpig population in these areas, there were other factors which DUNN, C.samplers. Research in Veterinary Science 33, 384-385 to pigs of a cyclone S. & DONALDSON, A. I. (1997) Natural adaptationhelped to reduce the spread of infection; they included the rel- Taiwanese isolate of foot-and-mouth disease virus. Veterinary Record 141,ative geographical isolation of the area, the placing of road- 174-175blocks with quarantine stations on the three major highways FENNER, F. J., GIBBS, E. P. J., MURPHY, E A., ROTT, R., STEDDERT, M. J. &connecting the west and east of the country, and the estab- WHITE, D. 0. (1993) Picornaviridae. In Veterinary Virology. 2nd edn. Sanlishment of protection and surveillance zones around infected Diego, Academic Press. pp 403-423premises. HOUSE, J. A. & HOUSE, C. A. (1992) Vesicular Diseases. In Diseases of Swine. It has been suggested that the reason why the clinical 7th edn. Eds A. D. Leman, B. E. Straw, W. L. Mengeling, S. DAllaire, D. J. Taylor. Ames, Iowa Statedisease appeared initially in larger pigs, mainly in sows and KITCHING, R. P. (1998) AUniversity Press. pp 387-398 recent history of foot-and-mouth disease. Journalfinishing pigs, and only later in younger pigs, may be related of Comparative Pathology 118, 89-108to the higher air intake rate of larger pigs and their resulting KITCHING, R P., KNOWLES, N. J., SAMUEL, A. R. & DONALDSON,.A. I.exposure to larger doses of aerosolised virus (Donaldson (1989) Development offoot-and-mouth disease virus strain characterization1997). - a review. Tropical Animal Health and Production 21, 153-166 The 0 Taiwan virus showed natural adaptation to pigs by RYU, E. (1984) Picornavirus. In Veterinary Microbiology. Taipei, Yihsienexperimental exposure (Dunn and Donaldson 1997), and was Publishing. p 1279shown to be closely related genetically to strains in Hong SHIEH, H. K. (1997) The FMD situation in Taiwan. Journal of the Chinese SocietyKong and the Phillipines in recent years (Kitching 1998). of Veterinary Science 23, 395-402During the epidemic in Taiwan, field observations of the lack TAIWAN AGRICULTURAL YEARBOOK (1997) Department of Agriculture and Forestry, Taiwan Provincial Governmentof spread of the virus from infected pigs to ruminant animalsin close proximity support this finding, and no clinical caseshave been reported from cattle, buffalo, or goats. A routinemonitoring programme including clinical examinations plusprobang sampling of oesophagopharyngeal fluid for the iso-lation of FMD virus, has been implemented since late 1997 invaccinated cattle, buffalo, and goats. BHK-21 cells were usedto try to isolate FMD virus from the samples of oesophago- Notices and divisional eventspharyngeal fluid but no cases of FMD have been identified inany vaccinated ruminant species. The monitoring should be Divisions of the BVA are entitled to a free notice in Thecontinued to verify the specific affinity of this FMD type 0 Veterinary Record for each meeting that they organise.virus to pigs. Notices should contain the date, time, venue and town of the The sharp decline in the market value of pigs was due to meeting, details ofthe subject, any speakers and sponsors andtwo major factors. The first was the loss of the export market, the address and telephone number of the person from whomwhich led to an immediate 40 per cent oversupply on the details can be obtained. They should be addressed to:domestic market. The second factor was the temporary rejec- Kathryn Clark, The Veterinary Record, 7 Mansfield Street,tion of pork by consumers, caused by the overwhelming pub- London WiM OAT, fax 020 7637 0620.734 The Veterinary Record, December 18/25, 1999