Livestock Agroterrorism: The Deliberate Introduction of a Highly Infectious Animal Pathogen

Abstract

Agroterrorism refers to attacks with any of a variety of biological or chemical agents against commercial crops or livestock populations, either as targets in their own right or as vehicles to attack humans. An agroterrorism incident would generally involve bioterrorism, and potential agents include pathogens such as viruses, bacteria, or fungi. Within the context of agroterrorism, livestock agroterrorism is described as the intentional introduction of an animal-borne infectious disease with the goal of spreading fear, producing economic losses, and/or threatening social stability. Causing human illness or human casualties is another potential goal of livestock agroterrorism. Livestock agroterrorism is considered to be attractive to terrorists because biological agents that affect livestock or poultry are more readily available and more difficult to monitor than are agents that infect humans. In addition, a terrorist attack on animal husbandry may have huge economic consequences with no human casualties. Therefore, a biological attack that targets the animal husbandry sector should be regarded as both a “high-consequence” event and a grave national security risk. This review addresses the use of biological weapons that may be used to target livestock or poultry rather than agricultural inputs or equipment. It first defines livestock agroterrorism. Then, the common priority disease agents that may be used to target livestock or poultry in an agroterrorist attack and that are attractive to terrorists are outlined.

Introduction

A mong the types of biological terrorism, agroterrorism is defined as an attack in which viruses, bacteria, fungi, or toxins are applied to commercial crops or livestock populations, either as targets in their own right or as vehicles by which humans can be harmed. Agroterrorism has received little attention, possibly because of the misconception that it is as difficult to obtain, weaponize, and disseminate agricultural pathogens as it is to convert an anti-human biological weapon from bacteria into a bomb. Biological agents that target humans are extremely difficult to develop into weapons that would kill more individuals than would conventional explosives. Given that only a subset of terrorists would wish to kill thousands of individuals, this consideration has led policymakers to conclude that such catastrophic terrorism is a “high-consequence” event (Falkenrath et al., 1998).

One form of agricultural terrorism is the targeted introduction of a biological agent that is pathogenic to livestock. Compared with bioterrorism methods that employ biological agents to target humans, a major act of livestock agroterrorism causing over a billion dollars in damage with no human casualties could be conducted via a series of limited pathogenic infections that are induced using simple methods. Furthermore, depending on the chosen agent, biological attacks against livestock industries could appeal to (1) politically motivated terrorists, (2) criminal groups seeking financial gain, and (3) apocalyptic groups who seek to kill as many individuals as possible. Therefore, a biological attack that targets the animal husbandry sector should be regarded as both a “high-consequence” event and a grave national security risk (Casagrande, 2000).

Most significantly, livestock agrobioterrorism has captured the attention of policy makers in most countries and at all levels of government. Unfortunately, this type of bioterrorism remains a poorly understood subject. This review addresses the use of biological weapons that may be used to target livestock or poultry in attacks against plant or non-agricultural targets. This review first defines livestock agroterrorism. Then, the common priority disease agents that may be used to target livestock or poultry in an agroterrorist attack and that are attractive to terrorists are outlined.

Livestock Agroterrorism

Definition of livestock agroterrorism

“Terrorism” is defined as “the calculated use of violence, or the threat of violence, against civilians to attain goals that are political, religious, or ideological in nature; this is done through intimidation or coercion or instilling fear” (Webster's Online Dictionary, 2006b). There is no commonly accepted definition of bioterrorism, but it is generally defined as “terrorism by intentional release or dissemination of biological agents (bacteria, viruses, or toxins)” (Webster's Online Dictionary, 2006a). In contrast to the devices that are occasionally used in terrorist attacks, biological and agricultural weapons can continue to cause direct damage for days, weeks, or even months following their release (Clarke and Rinderknecht, 2011). These long-term effects are particularly likely when the disease becomes widely disseminated before its presence is recognized. The results of bioterrorism may be observed in the economic or biological effects of the introduction (or the perceived introduction) of diseases.

“Livestock agroterrorism” is a type of bioterrorism and is described as the intentional introduction of an animal infectious disease with the aim of instilling fear among the population, producing economic losses, and/or threatening social stability (Monke, 2007). Livestock agroterrorism is considered to be an attractive method for terrorists because biological agents that are effective against livestock or poultry are more readily available and more difficult to monitor than are biological agents that are used against humans. In addition, an attack on the animal husbandry sector could have enormous economic consequences with no human casualties.

Goal of livestock agroterrorism

The use of biological weapons against humans could cause mass casualties on an unprecedented scale. The enormity of the decision to use biological weapons that could kill thousands of individuals increases the likelihood of dissention within a group that plans to employ such weapons. Many terrorist plots have been foiled by conspirators who succumbed to their conscience and informed on their partners (Casagrande, 2000). An agroterrorist attack may result in the loss of valuable animals, the incurring of costs related to the containment of outbreaks and the disposal of carcasses, lost trade, and other economic effects that involve suppliers, transporters, distributors, and restaurants.

The goal of livestock agroterrorism is not to kill cows, pigs, or chickens; rather, these deaths are a means to achieve the goal of social disorder that would potentially result from (1) a loss of confidence in the government and (2) economic crises in the food and agricultural industries (Monke, 2007). The goals of livestock agroterrorism include spreading fear among the populace, producing economic losses, and/or threatening social stability. Causing human illness or human casualties may be another goal of livestock agroterrorism. Human health may be jeopardized through either contaminated food or the release of an animal pathogen that is transmissible to humans (Monke, 2007). Although livestock may not be a terrorist's first choice of target because it lacks the “shock factor” of more conventional targets of terrorism, bioterrorism analysts increasingly consider livestock to be a viable secondary target (Chalk, 2005).

Terrorists wish to see a dramatic public response that attracts media attention. Such results can be only triggered by attacking a large target (i.e., one or more of the dairy, beef, swine, or poultry industries) with a foreign animal virus that leads to mass slaughter and costly international trade embargoes. A small amount of infected material could produce a significant effect in a livestock-targeted agroterrorist attack. Thus, livestock agroterrorism may be a low-cost but highly effective tool with which the perpetrator can achieve their goal of destroying the economy of the target country or sector.

Nature of livestock or poultry bioterrorism

Livestock may be easy targets for bioterrorists, and it has been suggested that the strategic infection of animals could cause damage that is far more severe than would be incurred by accidental contamination or natural outbreaks (Gyles, 2010). In fact, the potential use of animal pathogens that are both highly infectious and contagious (e.g., the foot-and-mouth disease [FMD] virus) to physically cripple livestock and economically cripple a country has been recognized for many years (Gibbs, 2003). Indeed, both the 2001 FMD epidemic in the United Kingdom and the 2010–2011 FMD epidemic in South Korea clearly illustrate how effective the FMD virus could be as a weapon in the hands of a terrorist. In 2001, the United Kingdom suffered an FMD outbreak that was described as “one of the worst epidemics of FMD the modern world has ever seen” (Gibbs, 2003). The 2010–2011 South Korean FMD epidemic resulted in the culling of more than 3.3 million animals, with losses estimated to have exceeded US$2.6 billion (ProMED-mail, 2011). The extent of these epidemics indicates that a highly virulent animal disease agent, such as the FMD virus, may be a very powerful weapon for a bioterrorist who wishes to cause widespread disease among livestock and economic disruption in the targeted country. These outbreaks can be seen as costly warnings, although the precise mechanisms by which the FMD virus entered the United Kingdom and South Korea were never determined.

Highly virulent diseases of livestock or poultry that are easily acquired and transported, non-hazardous to humans, and capable of causing catastrophic epidemics in countries with industrialized livestock production methods are common, and livestock products are distributed worldwide. Bioterrorist attacks that target livestock or poultry would not require access to weapons-grade disease strains or laboratory cultures; natural diseases that can cause catastrophic epidemics are common, dispersed globally, and easily acquired. Virulent contagious livestock diseases, such as highly pathogenic avian influenza, Newcastle disease, anthrax, and FMD are enzootic or even common in countries that are associated with highly organized, well-financed, and globally active terrorist organizations (Roeder, 1999; Tucker, 2000).

Elaborate delivery technologies or methods are unnecessary for clandestine, economically targeted bioweapon-based attacks on livestock or poultry. The only requirements are a willing actor or conspirator, careful planning, and access to an appropriate disease agent (OTA, 1993). The ease and rapidity of the international transport of potential human and animal vectors, coupled with the increasing virulence and variety of human-selected and human-engineered disease organisms, set the stage for epidemic scenarios that could equal or surpass the toll of any known historical incident.

Indications of disease symptoms and transmission route may be keys to distinguish between attacks that target livestock and naturally occurring endemic outbreaks

Any government or terrorist organization whose agents commit acts of agroterrorism against livestock and poultry may believe that it could evade blame for the act. Indeed, it may be difficult to unambiguously attribute an animal-disease outbreak to a biological attack as opposed to a natural occurrence. For a biological attack that involves human pathogens, there are generally two potential indicators that a disease outbreak resulted from an intentional attack: the kinetics of the outbreak and the route of infection. Explosive outbreaks, in which hundreds of individuals become ill at once, or outbreaks that occur simultaneously in geographically scattered areas, are unlikely to occur in the natural person-to-person spread of a disease. A high prevalence of respiratory infections may also be an indication of an attack, as mass-casualty biological weapons rely on the inhalation of the pathogen by the victims. For example, the few cases of anthrax infection that have occurred in the United States have nearly all been cutaneous (Guillemin, 2001). If cases of inhaled anthrax were to appear at hospitals, a biological attack would be suspected.

In contrast, biological attacks on livestock or poultry have fewer indications that could be used to distinguish them from natural outbreaks; the local, national, and international responses would generally be similar to those that are required for natural or accidental outbreaks. However, an intentional introduction could follow unpredictable patterns and may involve multiple locations or organisms, making it difficult to detect and contain an outbreak (Clarke and Rinderknecht, 2011). Although livestock agroterrorism could also cause explosive or multi-focal outbreaks, these infections may occur through the pathogen's natural route of entry into the host. A terrorist group that seeks to disguise an attack as a natural outbreak would have its agents spread the pathogen over a single area near a port of entry into the country, thereby mimicking the pattern of a natural outbreak.

Pathogens That Are More Attractive to Terrorists

The use of enzootic livestock diseases and emerging zoonotic diseases (i.e., diseases that can be transmitted between animal and human populations) by bioterrorists represents a potentially serious threat to livestock populations that were previously unexposed to these diseases. Several animal infectious diseases may be more attractive to terrorism perpetrators because certain diseases can be zoonotic, whereas other pathogens exclusively infect certain species. Approximately 60% of the pathogens that affect public health are zoonoses (CDC, 2009), which do not normally infect humans in the same manner as they do animals.

Once infected, the livestock can often act as the vector, continuing to spread the infectious disease and facilitating an outbreak, especially when live animals are transported (Monke, 2007). In the initial 2010–2011 South Korean FMD epidemic, for instance, the owner of a pig farm observed suspicious clinical signs of FMD in his herds and reported the incident to the local veterinary service. This service conducted tests on these animals on the same day using a pen-side antibody test kit and reported that the results were negative. Over the next several days, before FMD was finally confirmed, the farmers in the same village continued to transport the animals to and from livestock markets. Furthermore, feed company and manure transport vehicles frequently visited the farms. Thus, the live animals and vehicles may have been the vectors that facilitated the continuous transmission of the disease. Several days later, the owner of the same farm noticed blisters and ulcers in his herds as well as similar signs at the adjacent pig farm. The farmer then reported the incident to the National Veterinary Research & Quarantine Service. The national veterinary diagnostic laboratory confirmed the animals as FMD-positive using both antigen detection ELISA and RT-PCR tests the following day (OIE, 2010; ProMED-mail, 2010). This delay of the response for several days was responsible for the explosive nationwide epidemic that occurred over the next few weeks. In addition, the one-time use of a single test or the use of a single test early in the course of the disease is not as successful in detecting an outbreak as is the use of multiple tests over a period of time. For example, sera could be obtained at acute versus convalescent time points.

Diseases that are suitable for bioterrorist attacks on livestock and poultry

Of the many animal infectious agents that are available to agroterrorists, possibly fewer than two dozen have the potential to result in significant economic losses (Monke, 2007). The identification and prioritization of these agents require consideration of the organism involved, the consequences of the introduction of the disease, global surveillance, intelligence estimates, and the advice of panels of subject matter experts. Collectively, several different pathogens are suitable for use as animal bioterrorist agents. The agents of greatest concern are those with the following characteristics: (1) a high degree of contagion, morbidity, and mortality; (2) low levels of immunity to the agent in the target population; (3) a potential for rapid spread and simple routes of dissemination; (4) a potential to cause serious socioeconomic or public health consequences; (5) major importance to the international trade of animals and animal products; and (6) the influence of conducive climate and environmental conditions among bordering countries and that global warming will influence spread and that disease does not care about country borders (i.e., influence of migratory species and disease transmission). In most countries, the list of select agents that are currently of major concern in terms of bioterrorism that targets livestock and poultry generally mirrors the list of select agents that are relevant to the natural or accidental introduction of exotic animal diseases. In the case of the livestock industry sector, the emphasis is primarily placed on viral diseases that affect multiple species and that are both highly virulent and contagious.

Priority pathogens that may be used to target livestock and poultry in agroterrorist attacks: OIE Disease List

The determinants of the threat level of an agent are its mortality, its morbidity, and its international status as a “reportable” disease (i.e., a disease that is subject to international animal [and animal product] quarantine) under the World Organization for Animal Health (OIE) regulations. The OIE is an intergovernmental organization that consists of 178 member countries as of 2011 (OIE, 2012). The World Trade Organization (WTO) recognizes the OIE as the international body that is responsible for setting the animal health standards on which international trade restrictions are based (Chillaud, 1996; Thiermann, 1997).

The diseases of concern with respect to livestock agroterrorism consist of diseases that are of concern to the OIE and those that require notification of occurrence (OIE, 2011). Implicit in the development of such lists is the recognition of the relative importance of the economic and animal/human health implications of outbreaks of the constituent diseases. The commonly accepted animal infectious diseases of concern include all of the OIE's “List A” diseases and certain “List B” diseases. List A diseases comprise 15 agents that the OIE has identified as being the most serious animal pathogens from a global perspective; these diseases are outlined in Table 1. List A diseases are transmissible animal infectious diseases for which there is a risk of rapid spread beyond national boundaries. List A diseases have serious socioeconomic and/or public health consequences and are of major concern with respect to international trade. All of these agents could pose severe threats to animal and human health (e.g., Rift Valley fever [RVF]) or to the safety of animal products. List B diseases are transmissible diseases that are considered to be of socioeconomic or public health concern within national borders and which have an important impact on international trade (Kohnen, 2000). In 2004, the OIE replaced Lists A and B with a single list that is more compatible with the Sanitary and Phytosanitary Agreement of the WTO. The new OIE list classifies diseases equally, giving each the same degree of importance in international trade (Vallat, 2004).

Table 1.

Summary of Basic Information About List A Diseases That Have the Potential to Be Used as Livestock-Targeted Biological Agents–List A Animal Diseases: From the Office International des Epizooties (OIE)

Disease	Agent	Primary animal hosts	Transmission	Clinical signs	Mortality	Distribution
African horse sickness (AHS)	AHS virus (reovirus, genus Orbivirus)	Horses, mules, donkeys, zebras	Predominantly mosquito-borne (Culicoides species are the primary vectors; other vectors include Culex, Anopheles, Aedes); may be tick-borne	Cardiac and pulmonary forms occur	Mortality rate in horses is 70–95%	Enzootic in central Africa, occurs in other parts of Africa, the Middle East, Spain, and Portugal
African swine fever (ASF)	ASF virus (not yet classified)	Pigs, warthogs	Directly communicable between animals	May be acute, subacute, or chronic Acute form: fever, vomiting, diarrhea, death	Mortality may approach 100%	Enzootic in Sub-Saharan Africa Recently observed in Russia
Bluetongue (BT)	BT virus (reovirus, genus Orbivirus)	Sheep, cattle, goats	Mosquito-borne (Culicoides species)	Fever; ulceration and necrosis of the oral mucosa; pneumonia; myositis; abortion in pregnant animals	Mortality as high as 10% in sheep; infection is generally not apparent in other animals	Occurs globally between 40° N and 35° S
Classic swine fever (hog cholera [HC])	HC virus (flavivirus, genus Pestivirus)	Pigs, wild boars	Directly communicable between animals	Fever; hemorrhagic lesions of the skin and conjunctivae; cyanosis of the extremities; diarrhea	Mortality rate approaches 100% in young pigs	Occurs in Asia, Central and South America, Africa, and parts of Europe
Contagious bovine pleuropneumonia	Mycoplasma mycoides subsp. mycoides SC (bovine biotype)	Cattle, zebu, water buffalo	Directly communicable between animals (droplet spread) May be transmitted via an airborne route	Fever; respiratory symptoms; infected calves may present with joint swelling	Mortality may be as high as 50%	Occurs in Africa, Asia, the Middle East, and Southern Europe
Foot-and-mouth disease (FMD)	FMD virus (picornavirus, genus Aphthovirus)	Cloven-hooved animals (cattle, sheep, goats, pigs, wild ruminants)	Directly communicable between animals May be transmitted by both animate (e.g., human) and inanimate vectors Airborne transmission possible Highly contagious	Fever; vesicles on buccal and nasal mucous membranes, muzzle, teats, udders, and feet	High mortality in young animals	Occurs in Asia, Africa, the Middle East, and South America
Highly pathogenic avian influenza	Orthomyxovirus, influenza A virus subtypes H5 and H7, to date	Chickens, turkeys	Directly communicable between birds via respiratory secretions, feces	Decline in egg production Facial edema; swelling and cyanosis of combs and wattles	Mortality rate may approach 100%	Global
Lumpy skin disease (LSD)	LSD virus (poxvirus, genus Capripoxvirus)	Cattle, wild ruminants	Directly communicable between animals (via infected saliva); spread via mosquito vectors	Fever; swellings or nodules in the skin; nodules are painful and may become necrotic; enlargement of the lymph nodes	Mortality rate variable	Predominantly Sub-Saharan Africa; disease has also occurred in Egypt and Israel
Newcastle disease	Newcastle disease viruses (Paramyxoviruses)	Domestic and wild birds (chickens are the most susceptible)	Directly communicable between birds (predominantly via respiratory secretions and feces)	Partial or complete cessation of egg production; respiratory and neurologic symptoms; watery diarrhea	Mortality rate depends on strain, immunity of flock, environmental conditions	Enzootic in many areas of the world
Peste des petits ruminants (PPR)	PPR virus (paramyxovirus, genus Morbillivirus)	Goats and sheep	Directly communicable between animals via contact with feces and ocular, nasal, and oral secretions	Fever; nasal discharge; bronchopneumonia with respiratory distress; necrotic stomatitis; conjunctivitis; diarrhea (may be hemorrhagic)	Mortality rate may approach 100%	Occurs in Africa, the Middle East, and the Indian subcontinent
Rinderpest	Rinderpest virus (paramyxovirus, genus Morbillivirus)	Cattle, water buffalo, wild ruminants, sheep and goats, certain pig species	Directly communicable between animals via contaminated secretions and excretions	Fever; hemorrhagic diarrhea; areas of erosion and necrosis in the mouth, intestines, and upper respiratory tract	Mortality rate may be high	Global eradication program is underway; foci of disease still remain in East Africa and the Indian subcontinent
Rift Valley fever (RVF)	RFV virus (bunyavirus, genus Phlebovirus)	Cattle, sheep, goats, wild ruminants	Mosquito-borne (Aedes species are the primary vectors)	Febrile illness with high case-fatality rate in calves and lambs Also causes illness in humans (e.g., retinitis, meningoencephalitis, hemorrhagic fever)	Mortality and abortion rates vary from 5% to nearly 100%	Occurs in Sub-Saharan and East Africa, Egypt, Yemen, and Saudi Arabia
Sheep and goat pox (SGP)	SGP virus (poxvirus, genus Capripoxvirus)	Sheep, goats	Directly communicable between animals May be transmitted by the airborne route May be transmitted by inanimate vectors	Fever; cutaneous eruption (erythematous lesions that evolve into papules; papules may evolve into vesicles that rupture and crust over or may develop into nodules); pox lesions may occur on mucous membranes, muzzle, nares, udders, teats, testicles; pulmonary involvement may occur	Occasionally fatal; invariably high mortality in unprotected imported breeds	Endemic in Africa and the Middle East
Swine vesicular disease (SVD)	SVD virus (picornavirus, genus Enterovirus)	Pigs	Directly communicable between animals	Fever; vesicles on the snout, interdigital spaces of the feet, buccal mucosa, tongue, and teats	Mortality is rare	Disease has been recognized in Hong Kong, Japan, and Europe
Vesicular stomatitis (VS)	VS virus (rhabdovirus, genus Vesiculovirus)	Horses, cattle, pigs, deer, other wild animals	Directly communicable between animals Arthropod transmission possible	Vesicles in mouth, around nostrils, muzzle, on the snout (pigs); excessive salivation; foot lesions may occur (particularly in pigs); mastitis and teat lesions in dairy herds	Morbidity may be as high as 90%	Endemic in the Americas

Adapted from information available on the OIE website and in the 2008 OIE Terrestrial Manual (Manual of Diagnostic Tests and Vaccines for Terrestrial Animals) (OIE, 2008).

Diseases that are attractive or unattractive to terrorists

The OIE includes the majority of highly infectious, contagious, and pathogenic animal diseases that have serious socioeconomic or public health consequences and that are of major concern with respect to the international trade of animals and animal products (Kohnen, 2000). FMD is likely the most frequently discussed disease with respect to livestock agroterrorism due to the ease with which infection can be induced, its ability to spread rapidly, and its potential to cause great economic damage (Monke, 2007). Although all of the OIE-listed animal diseases may be attractive to livestock-targeting terrorists, not all are potential terrorist weapons. For example, it is inconceivable that camelpox virus, an infection that is confined to camels, would be used to terrorize every nation, as camels do not contribute to the economies of most countries. Similarly, certain countries would not be threatened by terrorist attacks on sheep or goats. Such attacks would be likely to have minor consequences and thus be economically insignificant. Another example of a disease agent that is unlikely to be chosen by agroterrorists is bovine spongiform encephalopathy (BSE). The causative agent of BSE is considered to be a dangerous agent, although BSE is less likely than other diseases to be chosen by a terrorist. Brucella species cause disease in cattle, swine, and sheep, and can also infect humans. Terrorists can threaten humans with Brucella (via aerosol release) but cannot threaten a nation's livestock industry given that such livestock infections do not trigger mass slaughter or international trade embargoes; thus, such attacks would be economically insignificant. Similarly, the infection of livestock with Brucella would not threaten human health; for decades, the public has been protected from Brucella by the pasteurization of milk and cheese. This protection was clearly demonstrated in 1999, when Brucella melitensis was identified in goats and cattle in Texas, likely following introduction from Mexico. The disease was eliminated without an economic ripple (Breeze, 2004). Widespread animal infectious diseases such as brucellosis, influenza, and tuberculosis receive relatively less attention than do FMD, hog cholera, and Newcastle disease. However, emerging diseases, such as the Nipah and Hendra viruses and the H5N1 strain of the highly pathogenic avian influenza (zoonotic diseases that have infected humans, primarily in Asia), can be lethal given that vaccines are in short supply or have not been developed (Monke, 2007).

Transmission modes of biological agents that target livestock or poultry

Once a potential perpetrator obtains a biological weapon against livestock or poultry, the challenge remains to disseminate the agent to a sufficient extent to damage an industry that occupies much of the target country's territory. All of the former OIE List A diseases, which are highly virulent and are the most important diseases with respect to the protection of industrial sector livestock, are viral. An exception is contagious bovine pleuropneumonia, which is caused by mycoplasma. However, the List A diseases are transmitted via different routes. Most viruses can spread through direct contact, and others can be transmitted over great distances in an aerosol form (Kohnen, 2000). Other diseases, such as bluetongue and African swine fever, are transmitted by “vectors” (i.e., intermediary organisms that are capable of spreading the disease, such as mosquitoes and ticks). The three primary transmission modes of these animal infectious diseases are described below (Kohnen, 2000).

Airborne transmission

Normally, the air is not a suitable or favorable environment for viruses, and the presence of viruses in the air is generally due to contamination from infected materials. Airborne infectious viruses are associated with two types of particles: droplet nuclei and dust particles (Falk and Hunt, 1980). FMD, Newcastle disease, and avian influenza can all be transmitted via airborne aerosols over long distances (Kohnen, 2000). In 1981, three days after an FMD outbreak in Brittany, France, single cases appeared across the English Channel on the Isle of Wight. The prevailing wind patterns corroborate the hypothesis that the virus traveled 175 miles as an airborne aerosol (Murphy et al., 1999). Recently, Sanson et al. (2011) statistically reassessed the likelihood that the windborne spread of the FMD virus occurred at the beginning of the 1967–1968 United Kingdom FMD epidemic in Oswestry, Shropshire. This group provided strong statistical support to the hypothesis that airborne spread had indeed occurred (Sanson et al., 2011). Tsukamoto et al. (2007) demonstrated that the airborne transmission of highly pathogenic avian influenza was dependent on the number of infected chickens. However, Spekreijse et al. (2011) recently reported that the rate of airborne transmission between chickens over short distances is low. With respect to Newcastle disease, much information regarding airborne transmission is available in recent peer-reviewed publications (Hugh-Jones et al., 1973; Li et al., 2009a,b; Mitchell and King, 1994). Airborne infectious diseases are relatively difficult to contain and thus would present an enormous challenge to emergency responders if an outbreak occurred (Kohnen, 2000). Most of the diseases that are included in this category can also be transmitted by direct contact.

Direct transmission

Highly virulent diseases such as rinderpest, FMD, highly pathogenic avian influenza, Newcastle disease, and classical swine fever can be spread by both direct contact between animals and by contact with contaminated objects (Kohnen, 2000). For instance, the feed and water troughs and the milking machines that are used by an infected animal can transmit a virus to other animals. In addition, these viruses can travel on clothes, shoes, and equipment. This potential for disease transmission illustrates the necessity of biosecurity measures, including the cleaning of animal facilities and the restriction of human and vehicle traffic around animals.

Vector transmission

Certain diseases are transmitted by insect vectors. A tick or a mosquito acquires a pathogen from one animal and subsequently transmits it to another via a bite. Diseases such as RVF, African swine fever, bluetongue, Japanese encephalitis, and West Nile fever can be spread by arthropods, such as mosquitoes, midges, or ticks. In these cases, disease control depends on insect control. However, many developing countries cannot afford insecticides; therefore, these diseases tend to persist (Kohnen, 2000).

With respect to vector-borne disease, from August through September 2000, an overwhelming outbreak of Rift Valley fever struck southwestern Saudi Arabia and the adjoining Yemeni territories (CDC, 2000a,b,c). During this outbreak, approximately 40,000 animals, primarily sheep and goats, died or were spotaneously aborted by pregnant females (CDC, 2000b), and 883 human cases, including 124 deaths, were recorded in Saudi Arabia (Balkhy and Memish, 2002). An additional 1,328 human cases, including 166 deaths, were concurrently recorded in northwestern Yemen (Al-Afaleq and Hussein, 2011). Vector studies in Saudi Arabia established Aedes vexans arabiensis and Culex triteniorynchus as the biological vectors of the RVF virus in the region (Jup et al., 2002). Both of these species and several other potential Rift Valley fever vectors can be found throughout the region (Jup et al., 2002). Rigorous control measures were implemented in Saudi Arabia, which succeeded in curtailing the infection and preventing its spread to other parts of the country; however, the virus persisted in a cryptic form in the original area of infection, resulting in the intermittent diagnosis of several cases over the past 10 years (Al-Afaleq and Hussein, 2011). This case is an example of an animal infectious disease that is transmitted by both mosquito vectors and direct contact.

Conclusion

A biological attack on livestock or poultry should be regarded as both a potentially high-consequence event and a grave national security risk. The robust livestock industries of countries with industrialized production methods are currently vulnerable to terrorists; an act of livestock agroterrorism would affect the economies of the targeted country, those of geospatially and environmentally similar territories, and the respective global economies that depend on the affected resources. Such an attack could undermine consumer confidence in the government's ability to regulate and maintain the nation's food supply. Furthermore, the safety of a nation's food supply is a matter of great psychological, social, political, and economic importance.

It is important to be prepared for a possible future attack on livestock or poultry. Steps can be taken to prevent livestock agroterrorism, for example, by sharing information among government agencies, educating more veterinarians, strengthening laws, increasing public awareness, and supporting research to identify new methods to combat this threat. To further prepare a defense against livestock agroterrorism, it will be necessary to continue to devote national attention and government funding to continued research. The creation of animal vaccine stockpiles will also be necessary. Systemic education and training are required to familiarize veterinarians with the epidemiology of animal diseases and to instruct them in the reporting of suspicious cases. Government and private industry field personnel now access and create information at speeds and across distances that were unheard of only a decade ago. The establishment of a global tracking system using a digital database could enable the tracking of worldwide outbreaks. The overall objective of these activities would be to prevent or minimize the capability of terrorists to either take or threaten the lives of animals and civilians and to damage livestock property. Prevention is best accomplished through preparation, and biosecurity is a major part of an effective prevention strategy, with benefits extending well beyond livestock agroterrorism.

Footnotes

Acknowledgments

We would like to acknowledge the following individuals, without whose help, guidance, direction, mentorship, and assistance, this manuscript would not exist: Min-Ae Ahn and Ji-Eun Seo. We also thank two anonymous reviewers for helpful comments on preliminary drafts. This work was supported by Animal, Plant, and Fisheries Quarantine and Inspection Agency, Republic of Korea (grant 6235-320-210-13).

Disclosure Statement

No competing financial interests exist.

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