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The Foot-and-Mouth Disease Epidemic of 2001 in the UK: Implications for the USA and the “War on Terror”

Paul Gibbs

SUMMARYWhile there is no evidence to suggest that the recent epidemic of foot-and-mouth disease (FMD) in the UK and its subsequentspread to continental Europe were caused by bioterrorism, the extent of the epidemic shows that FMD could be a very powerfulweapon for a bioterrorist wishing to cause widespread disease in livestock and economic disruption for the targeted country.This paper describes the epidemic. It then examines the contentious issues that arose through the use of extensive slaughter tocontrol the epidemic and explores how, in turn, the concerns of society are being translated into a radical change in policywithin the European Union with respect to the control of FMD and other foreign animal diseases.

The crisis generated by the FMD epidemic in Europe in 2001 provides many lessons to be learned for the US and highlights theneed for creative thinking in research and teaching within Colleges of Veterinary Medicine to more effectively address the threatof epidemic diseases under the “new world order.” There is general agreement that the veterinary profession in the US plays aunique role in protecting the nation against epidemic livestock diseases, whether caused naturally or through bioterrorism. Theprofession also has a significant role in protecting the public’s health, since several epidemic diseases of animals, such as RiftValley fever, are zoonotic. However, improved financial support at the federal and state levels is urgently needed to support epi-demic-diseases research and teaching in Colleges of Veterinary Medicine.

INTRODUCTION

The terrorist attacks of Sept 11, 2001, led to the belated rec-ognition by the citizens of the US that al Qaeda is a globaland powerful terror organization. The anthrax bioterrorismthat soon followed hit first in Florida and then at the heartof government in Washington. Despite intensive detectivework, we do not currently know who initiated this bioter-rorism. These events have each, in their separate ways,revealed the vulnerability of the US to (1) physical acts ofdestruction on a scale never previously considered outsidenuclear war and (2) the intentional introduction of diseaseinto civilian populations. Distressingly, these events havealso exposed the limited ability of the nation to respondeffectively to such threats and the extent of the nationalneglect and intellectual impoverishment of the public healthsystem.

There is frequent mention in the media that the scale andurgency of the response by the US to the new tectonic platesof global politics, following the fall of communism and therise of international terrorism, must be akin to the Manhat-tan Project or to Kennedy’s challenge to “Put a man on themoon.” Under the rubric of the “war on terror,” the creationof the Department for Homeland Security is a step forwardin attempting to coordinate the many agencies of govern-ment in response to terrorism, a step forward that manyother nations, that are similarly threatened, have yet totake.1

Despite the hunt for al Qaeda, the wars in Afghanistan andIraq, and the heightened security in the US, we do not knowwhen or where or of what nature will be the next terroristattack in the US. There seems to be little doubt that furtherattacks will occur on American soil. Bioterrorisma is oftenregarded as the poor man’s nuclear bomb and many con-sider it is the major threat, even exceeding that of nuclearand chemical attacks. Biological agents are more readilyavailable and more difficult to monitor. Of the known bio-

logical agents possibly available to the terrorists, smallpoxvirus tops the list of fears, and the recent decision to beginvaccinating high-risk groups within the American popula-tion reflects the seriousness of this concern.

While the public’s health remains the first priority of thenation, the importance of protecting the food supplies hasnot been ignored. Prior to the events of the fall of 2001, therisk that food production would be targeted by bioterroristswas of concern only to those who had intimate knowledgeof animal and plant pathogens. Since then, a report by theNational Academies2 has highlighted the vulnerability ofthe nation’s food supply. Foot-and-mouth disease (FMD)was identified as the most important animal disease that theUS must be prepared for. I have identified in Table 1 thosecharacteristics that make FMD virus attractive to a bioter-rorist.

The potential use of FMD to physically cripple livestock andto economically cripple a country has been recognized (butnot openly discussed) for many years. Few know that in the1970s the Irish Republican Army threatened to release FMDvirus in the UK; in the 1980s Australia had to respond to anextortionist who similarly threatened to use FMD virus. Notsurprisingly, there are unsubstantiated reports that alQaeda has also studied the malevolent use of the virus.

So how effective might FMD virus be as a weapon in thehands of a terrorist? In 2001 the UK suffered an FMD out-break that was described as “one of the worst epidemics ofFMD the modern world has ever seen.”5 Although the pre-cise mechanism by which the virus entered the UK hasnever been determined, there is no reason to believe thatthis epidemic was caused by bioterrorism. However, sincethe only difference between a naturally occurring epidemicof disease and one initiated by terrorism is motive, such apossibility cannot be completely ruled out until thesequence of events leading to the establishment of the dis-ease in the UK is understood (if ever). The extent of this

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Table 1: An overview of the epidemiology of foot-and-mouth disease and those characteristics of the disease and the causal virus that make it attractive for bioterrorism.

Characteristic of FMD and the Causal Virus

Relevance to Disease Control Relevance as an Infectious Agent for Bioterrorism

Present in many parts of the developing world.

International trade and travelers unknowingly carrying infected meat represent risk to disease free countries.

Easily available from naturally infected animals in many countries around the world.

History of causing extensive outbreaks in the farming systems of Europe and South America.

Necessitates constant worldwide surveillance and preparedness by countries free of disease.

Importance of disease has led to most industrialized countries’ eradicating the disease. They do not use mass vaccination to protect their livestock, but rely upon complex import controls to avoid infection. This means that a virgin epidemic can be created. The high visibility of FMD and the knowledge of its impact leads to great potential economic concern = bioterror

Generally not infectious for people and, when infection has occurred, it is of little consequence (for example, no cases were confirmed in the 2001 epidemic).

The public needs to be informed that hand, foot, and mouth disease is relatively common in children but that it is caused by an unrelated human virus

Can be safely handled by terrorist (compare to anthrax and smallpox)

Pigs are amplifiers, cattle, indicators, and sheep are “silent spreaders.”

Pigs generally are the first species to become infected in a previously FMD free country by eating infected meat (in most cases imported illegally). They produce large quantities of virus as aerosol, which travels to neighboring farms to infect cattle and sheep. Whereas disease is easily recognized in cattle, FMD in sheep is generally mild and difficult to recognize.

Animals can be easily infected. The virus infects a wide range of livestock causing economic loss. Diagnosis is not always simple (as was illustrated in the 2001 crisis in Europe).

There are 7 seven serotypes and multiple strains.

Determining the serotype and the strain is important for epidemiological tracking of the origin of the virus, to determine its characteristics (for example, some are more capable of spreading by aerosol) and the need to evaluate vaccine effectiveness

Several serotypes could be used in an attack complicating the selection and availability of vaccines.

FMD can also represent “fast -moving disease.”

Generally, a short incubation period of to days, which leads to rapid dissemination.

Spreads rapidly, but terrorist can still be out of the country before any suspicion of the attack.

Transmission is by various routes. The virus is transmitted efficiently by contact with infected animals and their secretions and excretions (example e.g., in contaminated trucks) but also by aerosols over several miles and through ingestion of infected meat.

Multiple routes of transmission demand complex disease control responses and disruption of society.

Prodromal virus excretion. FMD virus is excreted as an aerosol and in milk up to 24 hours before clinical lesions appear.

Spread can occur from farm before suspicion of disease.

Virus titer in vesicular fluid can be as high as 10,000,000 infectious doses per ml as assessed in cell culture.

Cattle only require ~ 10 infectious doses as an aerosol to become infected.

A little virus can go a long way! Infection can be established by injection of virus.

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epidemic in the UK and its spread to other European coun-tries, the draconian response of the UK government (andindeed the governments of the other affected countries) toits control through stamping out,b and the consequent far-reaching, and often unforeseen, effect on the economy ofthese countries, illustrate what a powerful weapon FMDvirus could be to a potential bioterrorist. As a measure ofthe impact of the epidemic on everyday life in the UK, theepidemic caused a month’s postponement in the country’sgeneral election from May to June 2001, the first delay sinceWorld War II (Britain does not have a fixed schedule of elec-tions as the US does).

In the wake of the epidemic there have been many studiesthat provide lessons to be learned. Several of these studieswere commissioned by the UK government to address dif-ferent aspects of the epidemic. Since all the countriesdirectly affected with FMD in Europe in 2001 were membersof the European Union (EU) and received funds to offset thecost of eradication, the handling of the epidemic was thor-oughly reviewed by the European Parliament. The report tothe European Parliament3 was presented, and subsequentlyaccepted, in November 2002.c Most notably, these studiesrecognize the widespread public disgust at the extent of theslaughter associated with the stamping-out policy. Majorchanges are proposed in the way that extensive outbreaks ofFMD are handled in the EU in the future. The report to theEuropean Parliament favors the early use of emergency vac-cination when an epidemic appears to be out of control. Thereport emphatically states that mass culling of livestock onthe scale seen in the UK and the Netherlands will not bepublicly acceptable again and that alternative strategies aretherefore essential.

Were FMD to occur in the US, the initial federal and stateresponse would be identical to that used in the UK and con-tinental Europe to control the 2001 epidemic. A policy ofstamping out would be applied. Were FMD to occurthrough bioterrorism, it is probable that terrorists wouldtrigger several outbreaks in different parts of the country,possibly caused by several serotypes of the virus. The scaleof the stamping out could be extensive.

This article looks at control of the FMD epidemic of 2001 inthe EU (particularly in the UK) and examines its relevanceto the potential for FMD to cause a national emergency inthe US, whether resulting from an unintentional introduc-tion of the virus or from bioterrorism. Since this article iswritten for those involved in veterinary education, the dis-cussion on how the US should respond is restricted to therole of veterinary colleges. It should be read within the con-text of a previous article written for this journal by MarkThurmond and Corrie Brown on “Bio and Agroterror: Therole of the Veterinary Academy.”4

To place the analysis in context, it is first helpful to be awareof the history of FMD in Europe and North America.

THE RECENT HISTORY OF FMD IN EUROPE

Unlike the US, most countries in Europe battled FMD intheir livestock for most of the twentieth century. By the1990s however, the battle was believed to have been wonand the specter of FMD’s causing a major epidemic inEurope was considered most unlikely. With only minorincursions, which had been relatively easy to control, mostcountries had been free of disease for several years. Vaccina-tion had ceased throughout all countries of the EuropeanUnion (EU) by 1993. With the cessation of vaccination, noanimals had immunity to FMD, so it was considered that

Table 1 (continued)

Ruminants can become carriers. Probably not that important in industrialized nations as a reservoir of infection, but complicates use of vaccine and international recognition of a country as free from infection.

A small outbreak can have significant economic impact on export markets, even when the disease has been quickly eradicated.

Relatively hardy virus. Even though disinfectants are effective, contaminated areas may harbor virus for weeks and, under ideal circumstances, for several months.

Relatively easy to store prior to any proposed attack.

Wildlife can be infected. Many species of wildlife can become infected and develop clinical disease, but generally wildlife does not feature in transmitting the virus to livestock or acting as a reservoir. (The exception to this is the carrier state in the African Cape buffalo).

Infection of wildlife or feral animals (for example feral pigs or deer in the USA) could add an additional concern and complicate a response to a threat.

FMD vaccines are inactivated. For effective use, existing vaccines must be matched to the virus (es) causing the epidemic. High potency vaccines can induce protection as early as 4 four days, but this period and the logistics of arranging emergency vaccination can make it difficult to effectively use ring vaccination around infected farms to control an epidemic when dealing with a virus that spreads so rapidly.

While strategic vaccine banks are available, these do not necessarily contain adequate numbers of doses or types of vaccine to cover all permutations of possible use of FMD viruses by terrorists .

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any introduction of disease would be quickly detected.Thus protection of all of the EU’s livestock depended for thepreceding 10 years upon (1) restrictions on the importationof possible sources of virus and (2) quick recognition andreporting of disease, followed by (3) slaughter of affectedanimals and other susceptible animals on the farm. Thisstamping out policy is standard and is recognized by theOffice International des Epizooties (OIE)d as the mostappropriate way to break the chain of virus transmissionand thus control and eradicate the disease in industrializedcountries. Each country, within the EU, is required to haveits own national contingency plan for the control of FMD,based on criteria established by the European Commission.e

In February 2001 this complacency was abruptly shatteredwhen the United Kingdom experienced an epidemic thataffected most of the country. The disease also spread fromthe UK to three other European countries (Eire, France, andthe Netherlands). With remarkable speed but at a terriblefinancial and emotional cost to society, the disease waseradicated from all four countries by September 2001, usingstamping out as the initial policy. In 2002 Europe was againconsidered free of disease.

THE HISTORY OF FMD IN NORTH AMERICA

Foot-and-mouth disease has not been recorded in the USsince 1929. An outbreak occurred in Canada in 1952 andwas quickly controlled. The disease was endemic in Mexicountil eradicated in 1953 with help from the US government,and since that time the continent has been free of FMD.Within the US, prior to 1929, there had been several epidem-ics of the disease, often involving several states. The diseasewas eradicated on each occasion by slaughtering affectedanimals and animals in contact with disease. The origin ofthese epidemics was often traced to the importation ofinfected animals or animal products. This led, in 1929, tomajor restrictions being imposed on the importation of ani-mals and their products from infected countries. Theserestrictions, as suitably modified over time, are still in placetoday and have served the nation well. Vaccination wasused to control disease in Mexico but has never been used inthe US. The declared policy whereby FMD would be eradi-cated from the US were it to occur again, relies upon stamp-ing out as the preferred method, within the internationalconventions established by OIE.

THE EPIDEMIC OF FMD IN THE UK IN 2001 AND ITS SPREAD TO OTHER EUROPEAN COUNTRIES

The Statistics of the Epidemic

The epidemic of FMD in the United Kingdom was the mostextensive in living memory in that country. In contrast tothe last major epidemic in the UK in 1967–1968, the 2001epidemic was geographically widespread, affecting notonly England, but Scotland and Wales and, to a limitedextent, Northern Ireland. The disease also spread to Eire (1outbreak), France (2 outbreaks), and the Netherlands (26outbreaks), although only in the Netherlands was there sig-nificant secondary spread. The epidemic started in February2001 and the last recorded case was on September 30, 2001.Although FMD was first recognized as severe in pigs sentfor slaughter,f the epidemic was subsequently characterizedby extensive spread through the marketing and export of

infected sheep, in which the disease was often clinically dif-ficult to recognize.

The scale of the epidemic can be assessed from the follow-ing thumbnail sketch of the eradication policy. There were2,030 premises where FMD was confirmed, 2026 in GreatBritain (England, Scotland, and Wales) and 4 in NorthernIreland.g Although a strategic stockpile of vaccine was avail-able to control FMD in the UK (indeed vaccine use was seri-ously considered, as discussed later), the eradication ofFMD relied upon the traditional policy of slaughtering allclinically affected and susceptible animals on infectedfarms. During previous epidemics of FMD this policy hadalso been applied to farms where there was suspicion of dis-ease and also to dangerous contact farms (for example, farmsreceiving livestock from affected farms shortly before therecognition of disease). In the 2001 epidemic this policy wasoften extended to include slaughter of all animals on farmsthat were considered contiguous premises; namely, farms thatgeographically bordered the affected farm. In one areastraddling the western border between England and Scot-land, where the number of infected farms was already high,this policy was extended to a 3 km zone.

Applying this policy of extended cull, all susceptible live-stock were slaughtered on 10,157 premises. When brokendown into different categories, there were 2,030 premiseswhere FMD was confirmed or animals were slaughtered onsuspicion; 4,762 premises designated as dangerous contacts(includes all premises where animals were slaughtered aspart of a 3-km cull); and 3,369 premises designated as con-tiguous. A total of 592,000 cattle (5.5% of the national herd),3,428,000 sheep and 2,500 goats (11.5% of the national herd),and 140,000 pigs (2.3% of the national herd) were slaugh-tered. Additionally, approximately 1,000 deer were alsoslaughtered.h In the Netherlands approximately 285,000 ani-mals were slaughtered, with smaller numbers in France(63,000) and Eire (53,000).

Because of length of the epidemic in the UK and the imposi-tion of restrictions on the free movement of animals,between farms, to market,i to slaughterhouses for meatsales, and even across public roads that cut through an indi-vidual farmer’s land, many farmers found that they wereshort of grazing or overstocked. The farming communitywas given the opportunity to have animals slaughtered onwelfare grounds. Under this system, 1,821,000 sheep,166,000 cattle and 306,000 pigs were slaughtered and com-pensation in excess of $200 million was paid to farmers.

The last case of FMD was recorded on September 30, 2001,and after a period of six months of surveillance, the OIEdeclared the UK free of FMD on 15 January, 2002—aremarkable achievement considering the complexity of thesituation at the height of the epidemic.

Why Was the Epidemic So Extensive?

As the epidemic progressed, several reasons emerged toexplain why the epidemic became so extensive.

Delay in Recognition That FMD Was in the Country -- The majorcause was a delay in recognizing that the disease waspresent in the country. The first line of defense lies withthose who own/work with livestock; it is their responsibil-ity to report suspicion of unusual disease and this failed.Only when infected pigs were sent to slaughter was FMD

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suspected by a veterinarian conducting antemortem inspec-tions. Backtracking to the index farm revealed that approxi-mately 90% of 570 pigs had lesions of FMD at varying stagesof healing, indicating that infection may have been presenton the farm for at least two weeks prior to detection. Duringthis time, the virus had been transmitted to a neighboringfarm with cattle and sheep. Sheep from this farm had thenbeen sold through a large market, through which more than20,000 sheep were moved before animal movement wasstopped throughout the UK because of FMD’s being presentin the country (see below). Clearly, many sheep becameinfected in this market. It is now believed that over 40 farms,mostly throughout the western part of the country, wereinfected through the direct or indirect movement of infectedsheep from this market before the disease had been confirmed inthe pigs at the slaughterhouse. This widespread disseminationof the virus through the marketing of sheep led to the dis-ease’s spreading to Northern Ireland and subsequently toFrance, from where it was exported to the Netherlands incalves that had been housed near sheep imported from theUK (i.e., before animal movement restrictions had beenimposed in the UK). This extensive seeding of the epidemic

had all occurred before the disease was recognized to be inthe country.

Delay in imposing a National Stop on All Animal Movement -- Oncethe disease had been confirmed at the slaughterhouse bylaboratory tests, an animal movement restriction wasimposed in the affected area, but it was a further 3 daysbefore a national ban on animal movement was imposed.Advanced notice of the ban and an allowance by the gov-ernment that animals in transit could continue to their desti-nation led to an unprecedented increase in animalmovements prior to the ban. It has been suggested that (1)had a national ban on all livestock been in place immedi-ately on confirmation of the disease in the pigs, the size ofthe outbreak could have been reduced by one half or more;and (2) had there not been a seven-hour delay between thesigning of an order for a national ban and that order’s goinginto effect, 19 farms would have escaped FMD.

Difficulty in Recognizing Clinical Disease in Sheep -- Relativelysevere disease was seen in some flocks with large numbersof periparturient ewes, but in general the clinical signs ofFMD in sheep were mild and easily confused with those ofother conditions, such as foot rot. The term silent spreaderseloquently describes the situation, and it is not surprisingthat the presence of infection in a flock was often revealedonly when cattle in contact showed clinical signs as an indi-cator host.

Dependency on Laboratory Confirmation of Diagnosis -- Theacronym FMD has often been said to represent fast movingdisease because of the ease of transmission and the generallyshort incubation period. One of the lessons learned from the1967 epidemic of FMD in the UK was the importance ofslaughtering infected animals and animals incubating dis-ease as soon as possible (within 24 hours) after diagnosis.Indeed, UK policy had been refined, prior to the 2001 epi-demic, to the extent that pigs should be slaughtered first,then cattle, and finally sheep, since this is the order in whichmost virus is excreted as an aerosol. Prompt slaughterreduces the time over which infectious virus is potentiallybeing spread to other farms, an essential prerequisite if astamping out policy is to be effective. It had, until 2001, alsobeen traditional policy, when FMD had already been con-firmed in the immediate area of a suspected case, to acceptclinical diagnosis as sufficient justification for slaughter of aherd or flock, always provided that the lesions were consis-tent with FMD. Laboratory diagnosis was sought only forequivocal cases and cases outside the established infectedareas. At the start of this epidemic, there was often confu-sion over whether laboratory diagnosis was needed. Staff atthe government headquarters were often not convinced bythe telephone reports and instructed the veterinarians onthe farm to take samples. The difficulty of diagnosing FMDin sheep, which did not show obvious clinical signs, and thelack of veterinary experience with FMD led to large demandon the diagnostic laboratory at Pirbright in Surrey.j Infectedanimals were often kept alive until the Pirbright laboratoryhad confirmed the diagnosis. At times, this dependency onlaboratory diagnosis caused a delay of up to four daysbefore infected animals were slaughtered and contributedto prolonged dissemination of virus from the farm. Therequirement to seek laboratory diagnosis before animalssuspected as having FMD could be slaughtered was lifted in

Figure 1: The areas of Great Britain affected with Foot--and-Mouth Disease in 2001.

Animal health policy has traditionally been determined by a Chief Veterinary Officer, with jurisdiction over the entire UK. In recent years, however, devolution of government to Scotland (Parliament) and Wales (Assembly) has occurred. This devolution, which equates roughly with state rights in the US, has led to complexity in the implementation of policy in Scotland and Wales. (Figure modi-fied from "Lessons to Be Learned" Inquiry).

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late March, once the extent of the outbreak became appar-ent.

Peak Time for Marketing and Movement of Sheep -- For variousreasons of sheep husbandry and marketing that are beyondthe purview of this review, February and March are monthswhen large numbers of sheep are being transported aroundthe UK and to continental Europe. Although a national ani-mal identification system exists for cattle and pigs in theUK, there was none established at the time of the epidemicfor sheep. By law, all livestock movements in the UK shouldbe recorded by the farmer and trucker. However, to qualifyfor the payment of quota-based farm subsidies through theEuropean Community, some sheep were also being movedillegally from farm to farm. This activity has also been collo-quially described as the “rent-a-sheep” program. The com-plexity and extent of the marketing channels and movementof sheep in the UK is said to have come as a major surpriseto those responsible for eradicating the disease and madebacktracking of sheep movements a major, and often impos-sible, task. Since February and March are also busy monthsfor lambing, the problem was complicated further by thelarge numbers of lambs in a sheep population that was esti-mated to be around 35 million, far more than the officiallyrecognized numbers.

Survival of the Virus -- When compared with viruses such assmallpox virus, FMD virus is relatively fragile, but underthe cool, moist, and often cloudy conditions (low ultravioletlight concentration) of winter and spring in the UK, it sur-vives for several days and often longer. Vesicular fluid, tis-sue from lesions, and most excretions and secretions ofanimals with early disease contain large amounts of virusthat contaminate vehicles used to transport livestock. Thesevehicles, if not disinfected adequately between loads, infectsusceptible animals. The weather conditions of the earlystages of the epidemic favored not only the fomite survivalof the virus in vehicles but also the survival of the virus asan aerosol over several kilometers. This is presumed to haveoccurred in the case of the transmission from the originalsource of the epidemic on the pig farm to the neighboringcattle and sheep farm. The cattle and sheep farm was 5 kmfrom the pig farm and presumably downwind for at leastpart of the extended time during which the pig herd wasproducing large aerosol concentrations of virus. However, itmust be noted that sheep and cattle produce far less aerosolvirus than pigs. Once the virus had transferred from the pigfarm and become established in sheep, it appears that inmost infected flocks relatively few sheep were ever excret-ing virus at one time. Transmission between flocks and tocattle was believed to have been by close contact or aero-solized virus over short distances. This feature of the epide-miology has great significance when analyzing the needand effectiveness of the contiguous cull.

Inadequate Veterinary Force, Inadequate Preparedness, and Stereotypic Thinking -- Thirty-five years ago, the veterinaryforce in the UK responsible for animal health was at itszenith, both in numbers and reputation. Paradoxically, suc-cess was its problem and, with the election of a Conserva-tive government led by Margaret Thatcher, dramatic cuts ingovernment spending precipitated a decline in numbersand, sadly, in reputation. In practical terms, the governmentveterinary force available to combat FMD in 2001 wasapproximately two thirds of the manpower available at the

time of the previous epidemic in 1967. But the veterinaryforce had other problems in 2001. There were continuingconcerns over bovine spongiform encephalopathy (BSE).The epidemic of BSE, which emerged quietly in 1985, hadpresented a challenge of profound biological complexity,one that no country could have predicted or handled withconfidence. The way in which the BSE epidemic, and mostparticularly its association with the emergence of variantCreutszfeld Jacob disease in young people, was presented tothe public, by both politicians and senior veterinarians, haddamaged the high esteem that regulatory veterinary medi-cine had previously enjoyed in the UK. Thus at the time thatthe FMD epidemic hit the UK in 2001, the veterinary author-ities responsible for its control were still reeling from theeffect of the BSE epidemic. While the incidence of BSE caseshad fallen, many of the problems stemming from the pre-sumed ability of the BSE prion to infect people had not beenresolved. Consumed by a heavy workload with BSE and, inconcert with the European perspective that FMD now pre-sented far less of a threat than a decade earlier, it is no sur-prise to find that no extensive exercises had been held in thepreceding years to test the country’s preparedness for FMD.

When the 2001 epidemic occurred, it appeared to many whowere involved in the epidemic that those principally con-cerned with determining policy for eradicating the diseasewere not aware of the most recent scientific advances inrapid laboratory diagnosis, modeling, and vaccination. Par-adoxically, these were often advances that had come fromstudies funded in the UK! While everyone from overseaswho was involved in the epidemic had high praise for thoseresponsible for the day-to-day hard work in the field, thecompetence of those in higher authority was questioned.Certainly the work load was heavy and no one doubtedthen, or since, the sincerity of those in senior management,but, as is so often seen when a group is presented with anew challenge, old patterns of behavior emerge rather thanrecognizing that new approaches are required. There was aculture, within the government department primarilyresponsible for the control of the epidemic, to favor decisionmaking through committee with an associated fear of per-sonal risk taking. As the epidemic continued into the secondmonth, the cumulative effect led to a breakdown in trustbetween the farming community and the government.

When this situation was realized, Tony Blair, the prime min-ister, took charge and a process was activated by which allthe resources of government (beyond a single department)could be mobilized to handle an emergency. This processwas coordinated through the Cabinet Briefing Room(COBR) and had a flexible design, but most importantly, itbrought an orderly flow of decisions, resources, and actions.When COBR takes a decision, the government as a whole,with all its departments, is committed to support it. Forexample, COBR quickly involved the military to assist in thelogistics and disposal problems.

Once COBR was activated, the prime minister called in thechief scientist (a surface chemist) and a team of epidemio-logical modelers renowned for their work on human immu-nodeficiency virus infections (but with little veterinaryexperience) to advise him. It was from this FMD ScienceGroup, with limited veterinary input, that the concept of thecontiguous cull emerged for the control of FMD. This fire-break policy was contentious when implemented in 2001

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and remains contentious as a means of controlling and erad-icating FMD in the modern era. The relevance of the contig-uous cull and how it created public concern will bediscussed in more detail later.

What Was the Economic and Social Impact of the Epidemic on the UK and Continental Europe?

Initially, the government saw the epidemic as an agricul-tural problem, but it was soon recognized that the economicimpact extended far beyond the farming community. Tour-ism has become an important component of the UK econ-omy; the beauty of the British countryside and itsaccessibility (through a network of public paths and bridle-ways) make it a popular destination for British and overseasvisitors. To minimize the risk of FMD virus being intro-duced to grazing fields by local residents and tourists, pub-lic paths in affected areas were closed. The governmentempowered local authorities to close paths in other areasand many did so. This well-meaning decision by govern-ment in support of the farming community conveyed a mes-sage that the countryside was closed across the UK. Thenews quickly spread to the US. The extensive impact of theclosures on everyday life rapidly became obvious, but onlyafter some weeks was a system of risk assessment estab-lished to selectively reopen paths. To some this was consid-ered the most costly decision of the epidemic.

The direct cost to the government to control the epidemichas been estimated to be US$4.5 billion, including $2 billionpaid to compensate farmers for their loss of livestock. How-ever, farms that were unaffected by disease but subject toprolonged movement restrictions received no compensationfor loss of sales. The financial costs of the epidemic mostlyfell on those outside the farming community, yet theyreceived no compensation. There were costs imposed on thefood chain, most markedly on auction markets, slaughter-houses, and food processors. These activities were dis-rupted by the movement and export bans. The indirect coststo tourism were more difficult to assess but were estimatedto be large—around $5 billion. As one small reflection, Brit-ish Airways reported a significant fall in the numbers oftransatlantic passengers and even gave FMD as a major rea-son for a quarterly decline in revenues.

The costs, in terms of human stress, were far more difficultto measure. In many areas, the fabric of rural society wasdisrupted. Farmers were isolated on their farms and unableto go about their usual lives. Some committed suicide. Insome areas, even schools were closed for short periods.

While a benefit-cost analysis of the control of the 1967–1968FMD epidemic in the UK had reported favorably on the useof the stamping out policy, now—some 30 years later—thestructure of the country’s economy and the lifestyles of itscitizens had both changed. The importance of tourism to theeconomy and more importantly, the value that society nowattached to animal welfare and the environment eachaltered the balance of the equations.

THE CONTENTIOUS ISSUES

The Extent of the Slaughter

Irrespective of the way in which the epidemic was con-trolled, the widespread seeding of the virus, such thatnearly 57 geographically dispersed premises were infected

before the disease was recognized to be present in the UK,almost certainly would have generated a large epidemic.The worst case scenario in the contingency plans prior to2001 had only ever envisaged 10 outbreaks being discov-ered at the beginning of an epidemic. Within a few days ofthe first case of FMD, the UK government’s veterinaryresources were fully utilized and were operating withoutadequate contingency planning for such a large-scale event.

Once FMD was confirmed in the pigs at the slaughterhouse,veterinary authorities immediately applied a control policy,one that had worked effectively in the past in the UK andone that was recognized by the OIE to be the preferredmethod for countries where FMD is not endemic and is notcontrolled by vaccination. While, in retrospect, movementcontrol on all farm livestock should have been appliedthroughout the country immediately upon the initial diag-nosis (there was a three-day delay before extending itnationally during which time additional spread of virusalmost certainly occurred), the initial approach of the veteri-nary authorities was correct. The contentious issues arosewhen it was becoming clear that the previously successfulmethod for controlling FMD in the UK was apparently notworking and COBR was activated. The contribution ofCOBR to improved logistics and manpower was significant,but the introduction of the contiguous cull and the vacilla-tion over the use of vaccines created great concern and mis-trust.

Official inquiries into the management of the epidemic inthe UK have not been able to identify the precise origins ofthe decision to pursue the 3-km pre-emptive cull in certainareas and the contiguous cull in others. The Lessons to BeLearned Inquiry5, 6 criticized the government for failing todocument key decisions. It concludes that the 3-km cull wasprobably first proposed informally by the Scottish Executiveto control FMD in the sheep population of the southwest ofScotland from spreading further north into valuable cattlepopulations. Since this area of Scotland borders England,the concept was then extended by the UK government toinclude sheep across the border in England (cattle wereexcluded, but this was not explicitly stated and initiallycaused confusion and then lingering resentment). It seemsthat this approach was attractive to the modelers advisingthe prime minister. They came to the conclusion, after run-ning several scenarios, that an extensive culling policythroughout the UK (not just in this border area betweenEngland and Scotland) was the only way to control the epi-demic. Thus for areas where FMD appeared to be out ofcontrol, a contiguous cull (to include all susceptible species)was adopted as a more practical approach than determininga specific zone. The modelers stressed that a parallel reduc-tion in the time-to-slaughter of infected herds to within 24hours of detection was of paramount importance. Culling ofcontiguous farms was to be complete within 48 hours ofdetection on the affected farm

The report of the Lessons to Be Learned Inquiry5 commentsas follows:

From some perspectives the rigorous applicationof a contiguous culling policy was a desperatemeasure. But the situation was desperate. Theepidemic was expanding out of control. FMDcould have become endemic. The pressure wasintense. Resources were stretched. There was no

128 JVME 30(2) © 2003 AAVMC

time to explore alternatives or carry out experi-ments. Here was a simple formula that both theChief Veterinary Officer and the Chief ScientificAdviser said would work. And that was theadvice that was followed.

The UK government now had a range of culling policies tobe implemented on the ground. While there was (and stillis) an argument as to whether there was legal authority tosupport this, it went into effect:

• culling of all susceptible animals on premises with clinically confirmed cases within 24 hours of report

• slaughter of all susceptible animals on a farm upon suspicion of disease

• culling of all susceptible animals on farms with known dangerous contacts

• culling of sheep, pigs, and goats within 3 km of infected premises in the affected region in the west between Scotland and England

• culling of all susceptible animals contiguous to infected premises within 48 hours

Contiguous was intended to designate those farms that had acommon border with an infected farm, but little local discre-tion was allowed. Accordingly, there were numerousappeals against the contiguous cull and many of these wereupheld. In several instances the farm in question was re-designated as not contiguous. A climate of confrontationand opposition to the cull was generated in many parts ofthe country. Many veterinarians were opposed to the cull.Similarly, many farmers did not understand or accept thestatistical basis for the pre-emptive cull policy.

Most contiguous premises were not infected and probablywould not have become infected. Some analysts have con-cluded that the traditional approach had already estab-lished control of the disease at the time that the contiguouscull was introduced. It is arguable that the extensive depop-ulation of farms in the UK was therefore not necessary andcould have been avoided.

Disposal

Traditionally, animals that are slaughtered with FMD or aresuspected to have FMD have been buried or incinerated onthe farm. The disposal of carcasses always creates problems,but the situation was exacerbated in the early part of the2001 epidemic because of the numbers of animals culled, theinadequacy of the logistics, and concerns for environmentalcontamination. At the peak of the epidemic, on one dayalone approximately 60,000 animals were culled. While clo-sure of footpaths may have been a major factor in keepinglocal tourists away from rural attractions, the images of themass pyres, televised around the globe, undoubtedly keptaway foreign visitors.

These problems were overcome by introducing militarylogistical support, creating mass burial sites, and using ren-dering plants, but not before public hostility and disgusthad been generated by the piles of decomposing animals lit-tering the countryside. In retrospect, commercial landfillcould, in theory, have accommodated all the stock slaugh-tered for disease-control purposes. However, because therewas no contingency planning ahead of the epidemic, whenlandfill capacity was successfully contracted, prices were up

to ten times those in normal circumstances. Table 2, as mod-ified from the report of the Lessons to Be Learned Inquiry,5gives further detail about the scale of the operation.

Table 2: The methods of disposal for animals slaughtered in the control of FMD in the UK in 2001.

Vaccination

The UK considered the use of emergency vaccination dur-ing 2001, but in contrast to the approach used to control ofthe epidemic in the Netherlands, vaccination was neverused in the UK. The report to the European Parliament iscritical of the internationally agreed framework that existedin 2001 for the control of FMD. The OIE regulations penal-ized countries for using vaccination by unnecessarily pro-longing the period between freedom from disease and theopening of international markets. Freedom from disease, asestablished through stamping out, allowed exports to openin 3 months, compared with 12 months when vaccine wasused.k While the Netherlands used emergency vaccinationto control the epidemic, it subsequently culled all vacci-nated animals to allow its markets to open early. With theknowledge that vaccination could significantly delayresumption of the UK export market, the question ofwhether or not to vaccinate created considerable contro-versy during the epidemic.

FMD virus can cause a carrier state in ruminants, which canbe masked by vaccination. Serological tests are available todifferentiate vaccinated from naturally infected animals, butare currently best used only at the herd level. The issueswere complex, even for professionals with relevant clinicalexperience. Surprisingly, since the UK had considered useof vaccines in the previous epidemic in 1967–1968, nodetailed policy for using emergency vaccination existed,despite the fact that high potency vaccine was available.Further, there was confusion in the farming community asto the consequences; for example, a survey of consumersindicated that many would be reluctant to purchase prod-ucts from vaccinated animals. All the inquiries into the epi-demic recognized the complexity of the issue, but all calledfor the use of suppressive vaccination in support of an ini-tial stamping out policy.

COMMUNICATIONS

One recurrent theme in the various inquiries was communi-cations. A government has a clear responsibility in times ofcrisis to communicate clearly within its organization andwith the public. From the very first suspicion of FMD in thepigs in the slaughterhouse, small mistakes in communica-tion were often made that had major repercussions. Forexample, samples for laboratory confirmation were col-lected from the pigs at the slaughterhouse where FMD was

Disposal Method Provisional Statistics

Burning (on -farm) Over 950 sites

Burial (on -farm) 900 sites

Mass burial 61,000 tonnes at 4 sites

Commercial landfill 95,000 tonnes at 29 sites

Rendering 131,000 tonnes at seven plants

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first suspected and were quickly dispatched, in the anticipa-tion that the samples would be examined overnight at thePirbright laboratory. However, the laboratory was unawarethat they would be arriving that evening because this infor-mation was sent by e-mail and not telephoned. It was notuntil the following morning that the laboratory was madeaware of the situation.

As control of the epidemic began to call for resourcesbeyond the major government agency involved, centralizedcoordination was needed. This was belatedly recognized bythe activation of COBR. Where a local coordinated emer-gency response system was present (such as in Scotland,which had established one following the Lockerbie airdisaster involving Pan Am Flight 103) the control of the epi-demic was more effective.

To its credit, once FMD had been confirmed, the govern-ment acted quickly to establish telephone hotlines and aWeb site to provide information. While there was criticismof the number of lines available, the competency of thoseanswering, and the accuracy of the information, theseattempts freely to provide up-to-date information were gen-erally well received. The Chief Veterinary Officer and theMinister for Agriculture gave daily briefings to the press.These briefings gave details of the disease and its spread ina straightforward way. They were welcomed by journalists,and the ensuing coverage in the popular media was posi-tive. There was an understanding that under the pressure ofan epidemic, information changes rapidly and is not alwaysaccurate. However, a few weeks later, when the epidemicappeared to be out of control and policy was being decidedthrough the prime minister’s office, these daily briefingsthrough the agriculture department were discontinued andwere replaced by twice daily briefings from the prime min-ister’s office. The press attending these meetings at Number10 were largely political journalists; those specialist journal-ists who normally served the farming and rural communi-ties felt excluded. This change occurred at the time that thecontiguous cull was being introduced, which further fueledmistrust of the government.

From this point on the national media began to be more hos-tile. The media focused on the impact of the eradication pol-icy on the country as a whole, it questioned the legitimacyof the contiguous cull by championing the cause of individ-ual farmers who resisted it, and it drew attention to the useof emergency vaccination in other countries. With such con-cerns over the mistrust of information coming from the cen-tral government, the local and regional media, particularlyin the form of local radio, were seen to play a positive role inkeeping communities aware of what was happening to con-trol the epidemic and how it was affecting them.

The Web sites established by the national media were wellconstructed and an excellent source of detailed informationfor those following the epidemic from overseas. Web sitesdevoted to the epidemic were also established by manyinterested groups, from individual farmers to large industrygroups. In concert with the media these groups created con-stant pressure for greater accountability and responsivenessfrom central government—democracy in action.

The international press focused on the “killing fields” andthe impact on tourism and the rural economy. CNN and themajor networks ran daily reports and sent news anchors to

the UK to report. Even magazines in the US that one wouldnot expect to run stories on FMD, such as GQ, publishedincisive articles on the way in which the epidemic wasaffecting the country and remarked on the stoicism of coun-try people. The international press, focusing as it did on thepyres and mass burial pits, probably dissuaded manypotential tourists from traveling to the UK and to a lesserextent Europe. There was a common belief that the whole ofthe UK was ablaze and that the food was unsafe to eat,because of confusion between FMD and BSE. On a positivenote, veterinary authorities of countries around the worldbenefited from this extensive coverage because it sensitizedinternational travelers to the risks of importing animalpathogens through animal products and fomites.

THE IMMEDIATE RESPONSE OF THE USA TO THE EUROPEAN EPIDEMIC OF FMD IN 2001

The response of the US government to the European crisiswas both quick and appropriate.7 Immediately the UKreported FMD, the importation of animal products from theUK and then the EU was prohibited. As the extent of theepidemic became known, the Federal and State govern-ments supplied veterinarians to assist the UK authorities.Not only did they provide valuable assistance, but they alsohad the opportunity to gain both clinical and managementexperience. The Public Health Service of the USA sent ateam to evaluate the psychological impact of the epidemicon rural communities affected by FMD. USDA teams evalu-ated the logistics and environmental issues associated withthe disposal of the culled animals. Expertise in the area ofrapid diagnostics was offered.

Within the US, federal and state authorities increased surveil-lance at international air- and seaports for illegal animalproducts. Travelers arriving from overseas, particularly theUK, were subject to more attention. USDA and state veteri-narians of probably all states reviewed their contingencyplans. The lessons learned from FMD exercises during recentyears were reviewed, particularly the tripartite exercise of theUS, Canada, and Mexico, conducted in the fall of 2000. Whileno one expects that an epidemic of FMD in the US would par-allel the 2001 epidemic in Europe and involve large numbersof sheep, previous exercises have shown that an explosiveepidemic in cattle across the US is possible, because of a simi-larly extensive system of dealers and markets.

While it was reassuring to wildlife conservationists thatfree-living deer did not apparently become involved in theEuropean epidemic (even though they are known to be sus-ceptible), the much larger numbers of deer and other spe-cies of ruminant wildlife, such as pronghorn antelope andbison, prompted USDA and wildlife agencies to examinestrategies for controlling FMD.

Not surprisingly, the extensive media coverage given to theepidemic in Europe prompted many livestock industries toevaluate biosecurity and seek assistance from veterinary col-leges for updates on disease recognition and prevention. Theextent of the national coverage prompted many local news-papers and radio stations to run stories on biosecurity.

The extent of this media coverage and the economic analy-ses that indicated an epidemic of FMD in the US could becatastrophic were recognized by Congress. The GeneralAccounting Office was asked to review both the prepared-

130 JVME 30(2) © 2003 AAVMC

ness of the US and the government’s response to the Euro-pean crisis. The report concluded that, with minorexceptions, principally in the area of communications withCustoms, the response had been well timed and proactive.

In the UK the absence of a nationwide cohesive emergencyresponse system had hampered the eradication of FMDuntil the activation of COBR. It is noteworthy, therefore,that at the federal level in the US 26 federal agencies and theAmerican Red Cross signed the federal response plan inApril 1999, which is intended to guide the federal responseto national emergencies and augment state response efforts.Under this plan the Federal Emergency ManagementAgency (FEMA) is designated as the coordinating agencyand is responsible for providing expertise in emergencycommunications, command and control, and public affairs.In the event of a natural outbreak of FMD, FEMA woulddesignate USDA as the lead agency and work closely withthe department to coordinate the support of other federalagencies to respond to the outbreak. For example, under theplan, Customs would lock down ports of entry; the Depart-ment of Defense would provide personnel, equipment, andtransport; the Environmental Protection Agency would pro-vide technical support on the disposal of animal carcasses;the National Park Service would guide the response if wild-life became infected; and other agencies would provideadditional support. FEMA is now integrated into theDepartment of Homeland Security.

THE WAY AHEAD IN EUROPE AND THE USA

In looking to the future, our focus on FMD should beextended to consider other diseases that may have a similar,possibly even more severe, impact on livestock and publichealth.

With regard to FMD there are many recommendations thathave emerged from the various inquiries into the 2001 epi-demic. Some are specific to the bureaucracy of the UK gov-ernment and the European Union, but many are generic andrelevant to the US in its contingency planning for FMD,whether by accidental or intentional introduction. In look-ing ahead and planning appropriately, we must recognizethat this epidemic probably reflects the last time that mas-sive culling will ever be acceptable to the citizens of anydemocratic country for combating a disease that has nopublic health significance. The change in society’s valuesregarding animal welfare, conservation, and the environ-ment demands new thinking by those responsible for safe-guarding the nation’s livestock. The societal values ofEurope and the US are very close. Democracy and freedomof the press are just two values that affect the course of dis-ease eradication. Were an outbreak of FMD to occur in theUS and be approached with a stamping out policy associ-ated with mass slaughter, it seems likely that many of thecontentious issues seen in Europe in 2001 would arise.

It should not be forgotten that the veterinary services of acountry serve the people. Society, once educated, thereforeexpects its values and opinions to be respected and itswishes to be followed. The epidemic of FMD in 2001 inEurope painfully educated the electorate, which thenexpected a quick response. Accordingly, the report to theEuropean Parliament commented as follows:

The EU’s policy in the event of an FMD outbreakhas accordingly hitherto been geared to cullinglivestock from infected herds and FMD-suscepti-ble animals which had come into contact with thesource of infection or infected vectors or whichwere shown to have become infected in any otherway (a “stamping-out” policy). As a general rule,emergency vaccinations were to be avoided andperformed only at the request of the Member Stateconcerned, by way of exception in the event of amajor epidemic. In light of experience of FMD in2001, this policy cannot continue in its present form.l

The 2001 FMD crisis was a traumatic experiencein the areas affected. For the purpose of deter-mining control strategies and methods, the policyof the EU and the Member States must therefore infuture take account of the social and psychologicalimpact on the public and effects on non-agricul-tural sectors of the economy, such as tourism, inthe areas affected by a major FMD outbreak.Hitherto the basic “non-vaccination” policy hasassigned undue priority to trade-policy aspects(emphasis added).3

In line with this radical rethinking of policy, the report ofthe European Parliament calls upon the European Commis-sion and its Member States to adopt no less than 65 mea-sures to assist in the future control of FMD and otherdiseases that might occur in the EU. The 80 recommenda-tions of the Lessons to Be Learned Inquiry5, 6 as they applyto the UK as a member of the EU were similar. They weregrouped under three major headings and provide a conve-nient yardstick by which to measure the US’s policy onFMD and other foreign animal diseases.m

Detailed discussion of these recommendations is beyondthe scope of this article. However, both the Lessons to BeLearned Inquiry5 and the report to the EuropeanParliament3 comment that training and research areregarded as key to the prevention and control of disease.Colleges of Veterinary Medicine are seen as critically impor-tant for professional training and research. With regard tothe broader perspective of disease control, the report of theRoyal Society of the UK8 (equivalent to the National Acade-mies in the US), in addressing its role of examining the sci-entific questions relating to the transmission, prevention,and control of epidemic outbreaks of infectious disease inlivestock in Great Britain (not just FMD), highlighted theimportance of teaching and research. It emphasized in itsrecommendations the importance of better surveillance, epi-demiological modeling, biosecurity, diagnostic techniques,vaccination, research and development, and education andtraining. The report went as far as to recommend specificfunding levels for research and teaching in animal diseaseand support for Colleges of Veterinary Medicine. Indeed,support for Colleges has already been forthcoming from theUK government in conjunction with the Wellcome Trust.

The situation for long-term support of similar activities inVeterinary Colleges in the US has not been so encouraging.While one would have expected through the “war on ter-ror” that specific and substantial support for teaching andresearch on those foreign animal diseases that have thepotential to cause epidemics would have been a priority,

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this has not been the case. Money has flowed into medicalresearch and into preparedness through the health depart-ments of all states, but, in general, little has been directed toa long-term commitment to research on animal diseases.Similarly, there has been only limited national support forthe teaching of veterinary students, veterinarians, and live-stock owners to prepare the nation for such natural and ter-rorist induced threats.

The case for greater support has been made repeatedly. TheForeign and Emerging Animal Disease Committee of theUnited States Animal Health Association has been active inpetitioning greater support for better research and trainingin epidemic diseases for many years (see annual proceed-ings) and has intensified its efforts since 2001. Articles bymembers of this committee have been published. The Soci-ety of Tropical Veterinary Medicine held a conference inKey West in 1999 on disease control and prevention in thecontext of the “new world order,” which, among otherissues, highlighted the threat of future bioterrorism and theneed for regulatory veterinary medicine to adapt to thechanging expectations of society.9 The National Academies,in its report Countering Agricultural Bioterrorism, remarkedthat, in order to increase awareness of pests and pathogensnew to US agriculture, the Animal Plant Health InspectionService—together with cooperative extension, academicinstitutions, scientific professional societies, state animaland plant health agencies, and representatives of US plantand animal commodities industries—should develop acomprehensive educational plan.2 The Association of Amer-ican Veterinary Medical Colleges conference in Washingtonin November 2002, the report of which is the theme of thisissue of the Journal, highlights the contributions of Veteri-nary Colleges to the “war on terror” and how they can helpprepare the US against epidemic diseases. While wellattended by the colleges themselves, it was significant thatthere was poor attendance by senior personnel from gov-ernment agencies that could effect change. As discussedextensively elsewhere in this issue, the meeting identified aneed for changes to the veterinary curriculum in most, if notall, colleges, to develop a cadre of veterinarians and alliedscientists well trained in animal and public health. Collabo-ration among colleges would be necessary in developingfocused research and training programs.

There is general agreement that the veterinary professionplays a unique role in protecting the nation against epi-demic livestock diseases, whether caused naturally orthrough bioterrorism. The profession also has a significantrole in protecting the public’s health, since several epidemicdiseases of animals, such as Rift Valley fever, are zoonotic.However, improved financial support at the federal andstate levels is urgently needed to support research andteaching in the Colleges of Veterinary Medicine.

The crisis generated by the FMD epidemic in Europe in 2001provides many lessons to be learned, one of which is theneed for creative thinking within the Colleges of VeterinaryMedicine of the US to effectively address the threat of epi-demic diseases in light of the new world order.

NOTESa. Bioterrorism is a relatively new word to denote the use

of a biological agent or its toxin to create terror. Since the events of 2001 the media sometimes restrict its use

to describe the criminal use of a biological agent to cause disease in human populations and add the prefix agro (hence agro-bioterrorism) when animal or plants are the potential target. Agro-terror has also become popu-lar when describing attacks against livestock and crops, but this term has a wider meaning, as it can also include attacks using chemicals and explosives. In this article, the term bioterrorism will be used to refer to actions using biological agents or their toxins as directed against both animals and humans.

b. Stamping out: a control strategy that involves slaughter-ing infected animals and those thought to have been exposed to the disease, as soon as possible.

c. This report is a valuable resource for further study of the epidemic, as it lists all the major reports and their Web sites, as available in Nov 2002. Details on how to access the Web site are listed in the references

d. OIE serves as the world animal-health organization. OIE was founded in 1924 and has 158 member coun-tries. Its main objectives are to inform governments of the occurrence and course of animal diseases through-out the world and of ways to control them; to coordi-nate, at the international level, studies devoted to the surveillance and control of animal diseases; and to har-monize regulations for trade in animals and animal products among member countries

e. In 1993 the Food and Veterinary Office (FVO) of the European Commission had approved the contingency plans of the UK (last amended in 2000). Its effective operation had not been checked by the FVO prior to the 2001 crisis. However, prior to the epidemic, the ability of the UK to respond to an epidemic of FMD was con-sidered amongst the best in the EU.

f. The virus was probably introduced to the pig farm from overseas in the form of infected garbage, as indeed happened in California in 1929. The popular press and Web traffic have often raised the question of possible bioterrorism.

g. Northern Ireland and Great Britain, together with the Isle of Man and Channel Islands, constitute the United Kingdom.

h. In the early stages of the epidemic there was serious concern that free-living and farmed deer might be play-ing a role in the transmission of FMD, but FMD virus was never detected in either farmed or free-living deer. No accurate populations of deer are available, but it is believed that there are approximately 1 million free-liv-ing deer in the UK. Those slaughtered were mainly farmed deer. The population of farmed deer is about 250,000.

i. All markets for the sale of livestock within the UK were closed for approximately 6 months.

j. The pedigree of the UK in the diagnosis and research of FMD can be assessed by the OIE recognizing the Pir-bright laboratory as the World Reference Laboratory for the disease. This laboratory is credited with giving excellent diagnostic service throughout the epidemic. It coordinated the testing of over 3 million sera during the

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surveillance period (see later), before OIE recognized the country to be free of FMD virus.

k. These restrictions have since been revised by OIE to facilitate earlier opening of export markets when emer-gency vaccination is used. The period is now 6 months, subject to satisfactory serological surveillance.

1. Please note that the EU is not advocating that a stamp-ing out policy should not be pursued, just that emer-gency vaccination (vaccinate-to-live policy) should be considered a complementary tool to eradication.

m. Developing and maintaining a national strategy for disease avoidance and control: strategy; legislation; vaccination; farming practices; veterinary matters; bio-security; training; and import controls.

Developing and maintaining appropriate contin-gency plans and ensuring effective preparedness: con-tingency planning; scientific advice; information; public health; slaughter and disposal; animal welfare; and human resources

Managing an outbreak of disease: crisis management; speed of response; diagnosis; role of the military; com-munications; management; and controls.

REFERENCES1. The spores of war. Economist Nov. 30, 2002 p20–24 <http://www.economist.com>. Accessed 04/07/03.

2. Committee on Biological Threats to Agricultural Plants and Animals, National Research Council. Countering Agri-cultural Bioterrorism. Washington, DC: National Academies [forthcoming]. See Moon et al. J Vet Med Educ 30(2): 96–104, 2003 (current issue) for Executive Summary.

3. European Parliament Resolution on Measures to Con-trol Foot-and-Mouth Disease in the European Union in 2001 and Future Measures to Prevent and Control Animal Dis-eases in the European Union. 2002/2153(INI) <http://

www.europarl.eu.int/committees/fiap_home.htm> (click on Resolution en for English text). Accessed 04/07/03.

4. Thurmond M, Brown C. Bio and agroterror: the role of the veterinary academy. J Vet Med Educ 29: 1–4, 2002.

5. Lessons to Be Learned Inquiry. Anderson Report on Foot-and-Mouth Disease 2001. HC888 <http://www.fmd-lessonslearned.org.uk/>. Accessed 04/07/03.

6. Editorial—a year of inquiries (Wellcome Funding). Vet Rec 151: 745–747, 2002.

7. Government Accounting Office (USA). Foot-and-Mouth Disease: To Protect U.S. Livestock, USDA Must Remain Vigilant and Resolve Outstanding Issues. Report to the Honorable Tom Daschle, US Senate, July 2002 <http://www.gao.gov>. Accessed 04/07/03.

8. Royal Society. Infectious Diseases in Livestock. <http://www.royalsoc.ac.uk/inquiry/>. Accessed 04/07/03.

9. House JA, Kocan KM, Gibbs EPJ, eds. Tropical Veteri-nary Medicine: Disease Control and Prevention in the Con-text of the New World Order. Proceedings of the Fifth Biennial Conference of the Society for Tropical Veterinary Medicine, June 12–16, 1999, Key West, FL. New York: New York Academy of Sciences, 2001. <http://www.nyas.org/books/vols/toc916.html>. Accessed 04/07/03.

AUTHOR INFORMATION

Paul Gibbs, BVSc, PhD, FRCVS, is Professor of Virology at the College of Veterinary Medicine, University of Florida, Gaines-ville, FL, where his responsibilities have included teaching and research on foreign animal diseases. Prior to joining the fac-ulty in Florida in 1979, he was involved in the FMD outbreak in the UK in 1967–1968 and subsequently conducted research on FMD in deer at the Pirbright laboratory in the UK. He was in the UK several times during the recent epidemic. Contact Information: Tel 352–392–4700 Ext 5882. E-mail pgibbs@ufl.edu