Overview of Agricultural Biosecurity

Historical Perspective
The Agricultural Biosecurity Threat
Potential Economic Impact in the United States
Potential Perpetrators
Potential Animal Pathogens
Potential Crop Pathogens
References

Historical Perspective

Past Incidents of Agroterrorism

Agricultural resources have been considered potential targets of biological warfare or terrorism since World War I. Examples include the following (see References: Cameron 2001; Casagrande 2000; Kohnen 2000; Monterey Institute of International Studies: Chronology of CBW attacks targeting crops and livestock 1915-2000; Pate 2001; Rogers 1999):

German operatives apparently infected horses that were being shipped to Europe with anthrax and glanders during World War I.
The Japanese allegedly used anthrax and rinderpest against Russia and Mongolia during World War II.
Britain accused Germany of dropping cartons of Colorado potato beetles in Southern England during World War II.
In 1952, the Mau Mau (members of the Kikuyu tribe) killed 33 head of cattle at a Kenyan mission station using African bush milk (a local plant toxin).
In 1978, the Arab Revolutionary Council used mercury to poison Israeli oranges to sabotage the Israeli economy; as a result of this contamination, Israeli orange exports were reduced by 40% and at least 12 people were injured from eating contaminated oranges.
In 1997, Israeli settlers from Gosh Etzion sprayed pesticides on grapevines in two Palestinian villages, destroying up to 17,000 metric tons of grapes.

Countries with Agricultural Bioweapons Programs

A number of countries have conducted bioweapons research on anti-livestock or anti-crop pathogens. Countries with documented programs are outlined in the table below.

Documented Agricultural Bioweapons Programs
Country*	Dates of Program	Diseases Studied
Canada	1940s-1960s	Anthrax, rinderpest
France	1939-1972	Potato beetle, rinderpest
Former Soviet Union	1935-1992 (current status unclear)	African swine fever, anthrax, avian influenza, brown grass mosaic, brucellosis, contagious bovine pleuropneumonia, contagious ecthyma (sheep), foot-and-mouth disease, glanders, maize rust, Newcastle disease, potato virus, psittacosis, rinderpest, rice blast, rye blast, tobacco mosaic, Venezuelan equine encephalitis, vesicular stomatitis, wheat stem rust, wheat and barley mosaic streak viruses
Germany	1915-1917, 1942-1945	Anthrax, foot-and-mouth disease, glanders, potato beetle, wheat fungus
Iraq	1980s-present (current status unclear)	Aflatoxin, anthrax, camelpox, foot-and-mouth disease, wheat stem rust, wheat smut
Japan	1937-1945	Anthrax, glanders
South Africa	1980s-1993	Anthrax
United Kingdom	1937-1960s	Anthrax
United States	1943-1969	Anthrax, brucellosis, Eastern and Western equine encephalitis, foot-and-mouth disease, glanders, late blight of potato, Newcastle disease, psittacosis, rice blast, rice brown spot disease, rinderpest, Venezuelan equine encephalitis, wheat blast fungus, wheat stem rust
In addition to the countries identified, the Rhodesian government was suspected of using anthrax to kill cattle owned by the rural black population in the 1970s. Adapted from Monterey Institute of International Studies. Agricultural biowarfare: state programs to develop offensive capabilities (see References).*

Several countries other than those noted in the table above are suspected of having agricultural bioweapons programs, although the status of these programs is unknown (see References: Monterey Institute of International Studies: Agricultural biowarfare). They include:

Egypt (anthrax, brucellosis, glanders, psittacosis, Eastern equine encephalitis)
North Korea (anthrax)
Syria (anthrax)

The Agricultural Biosecurity Threat

An agroterrorism attack could result in any of the following (see References: Chalk 2001; Wheelis: Agricultural biowarfare and bioterrorism):

Reduce production of food (although unlikely to be an issue in a country such as the United States, starvation could occur in poor countries with limited resources)
Lead to dramatic economic loss within the affected agricultural sector or sectors (through direct loss of crops or animals, cost of containment activities, or reduced domestic demand)
Result in export embargoes that would remove agricultural products from the global market
Lead to destabilization of related economic markets (such as revenue losses to shippers, processors, exporters, and others)
Create social instability by causing the population to lose confidence in the safety of the food supply and by inciting fear and a sense of vulnerability

A bioterrorist attack on agricultural targets in the United States has been considered by some to be a "high consequence–high probability event" for the following reasons (see References: Casagrande 2000, Parker 2002, Wheelis 2002):

The technological barriers to obtaining and weaponizing agricultural pathogens are relatively minimal.
Many crop and animal pathogens can be isolated from the environment or obtained from laboratories without substantial difficulty.
An attack against crops or livestock could be carried out relatively easily without sophisticated equipment or expertise.
Only a small quantity of the affecting agent would be needed, since many of the agents of concern are highly transmissible between animals or, for plant diseases, via the air.
Crops are openly exposed and relatively vulnerable to an attack.
Livestock and poultry often are raised under conditions involving high concentrations of animals (eg, feedlots may hold up to 300,000 head of cattle, chicken farms may house up to several million birds).
Certain sectors of the food-production industry are geographically localized, so an attack on one sector could have a dramatic impact on a local, state, or regional economy.
Current animal husbandry methods have increased stress levels in livestock and poultry, increasing their vulnerability to infection.
Limited genetic diversity in US agriculture promotes susceptibility to specific pathogens.
Animals and animal products often are dispersed to many different locations over a short period of time, thereby enhancing the potential for spread of a communicable agent.
Damaging crops and livestock is not as morally serious as committing terrorist acts involving loss of human life; therefore, agroterrorism may be more acceptable to some potential perpetrators than other forms of terrorism.

In addition to a direct impact on producers, an attack on a sector of US agriculture would have a ripple effect on other industries. For example, an attack would affect shippers, wholesalers, distributors, exporters, retailers, and possibly other aspects of the economy, such as tourism.

Potential Economic Impact in the United States

Role of Agriculture in the US Economy

Agriculture continues to be a major aspect of the US economy (see References: NRC: Countering agricultural bioterrorism).

Agricultural products account for 8% of US exports.
The entire food and fiber system accounts for 16% of the gross domestic product and 17% of the domestic labor workforce, with an annual output of $1.5 trillion.
In 2001, the total value of exported US agricultural products was nearly $50 billion.

Economic Costs of Naturally Occurring Outbreaks

Deliberate introduction of animal or plant pathogens into the United States could cause billions of dollars of damage, depending on the agent(s) used and the sector(s) of the agricultural economy targeted. Naturally occurring outbreaks involving some of these agents, both in the United States and abroad, serve to illustrate this potential economic impact. Examples:

In 1971, an outbreak of velogenic viscerotopic Newcastle disease (VVND) occurred in Southern California. The disease spread rapidly to commercial poultry farms in the area. Containing the outbreak ultimately cost $56 million and led to the slaughter of 12 million birds (see References: Watson 1999). The outbreak severely disrupted the operations of poultry producers in the area and led to increases in the cost of poultry and poultry products in the area.
In 1983, an outbreak of pathogenic avian influenza in Pennsylvania led to the destruction of more than 17 million birds and cost nearly $65 million to control (see References: USDA: Highly pathogenic avian influenza).
In 1997, an outbreak of foot-and-mouth disease in pigs in Taiwan cost an estimated $19 billion to the Taiwanese economy ($4 billion to diagnose and eradicate the disease and $15 billion in indirect losses from trade embargoes) (see References: Parker 2002).
In 1997, an outbreak of hog cholera in the Netherlands led to the slaughter of 5 million pigs and 1.5 million piglets and cost an estimated $2 billion to control. In addition, the outbreak had a dramatic impact on Dutch pig exports during that time (see References: Pate 2001; NRC: Countering agricultural bioterrorism).
In 1996, identification of karnal bunt of wheat (caused by the fungus Tilletia indica) in the southwestern United States cost an estimated $250 in lost wheat exports (see References: Casagrande 2000). In addition, between 1996 and 1998, the US Department of Agriculture (USDA) spent over $60 million to contain the spread of karnal bunt (see References: Wheelis 2002).
In 1995, citrus canker was discovered in Florida, and since that time the disease has spread to 1,000 square miles of southern Florida and has cost over $200 million in control efforts (see References: Madden 2001).
In 2001, an outbreak of foot-and-mouth disease occurred in the United Kingdom; economic losses associated with the outbreak are estimated at $6 to $30 billion, and over 4 million animals were destroyed (see References: Ferguson 2001; NRC: Countering agricultural bioterrorism).

A recent report estimated that an outbreak of foot-and-mouth disease in California would incur the following costs (see References: Ekboir 1999):

Cleaning, disinfection, depopulation, and quarantine: $1.4 to $2.8 billion
Direct, indirect, and induced losses: $0.9 to $2.6 billion
Trade losses to both California and the United States at large: over $6 billion

Geographic and Regional Considerations

Agricultural resources are somewhat concentrated in the United States, with 34% of overall production coming from five states (California, Texas, Iowa, Nebraska, and Illinois); however, in 1997, 27 states had agricultural products valued at $3 billion or more (see References: Pate 2001). Thus, broad-scale agroterrorism attacks could have a dramatic impact across multiple states.

Some agricultural commodities are more geographically concentrated than others and therefore may be more vulnerable to a localized attack. Examples include the following:

Cattle (16% in Texas)
Hogs (22% in Iowa)
Grapes (92% in California)
Oranges (66% in Florida)
Cotton (23% in Texas)
Lettuce (78% in California)
Broiler chickens (16% in Georgia)

Certain commodities are concentrated regionally as well. For example, poultry production is centered in the Southeast, whereas cattle, hog, and corn production are centered in the Midwest (see References: Watson 1999).

Potential Perpetrators

Examples of potential perpetrators of agroterrorism include the following (see References: Wheelis 2002):

State-sponsored terrorist groups (ie, sponsored by rogue nations such as Iraq)
Independent terrorist organizations that have political motivations (eg, al Qaeda or other extremist groups)
Independent groups that have other ideological motivations (eg, groups against the use of genetically modified crops, radical animal rights groups)
Offenders motivated by economic factors (eg, a person or group that could profit from sabotaging certain market sectors or specific competitors)

Potential Animal Pathogens

A number of different pathogens are suitable as animal bioterrorist agents. The agents of greatest concern are those with the following characteristics (see References: USDA: Agricultural Bioterrorism Protection Act of 2002):

High morbidity and mortality
Potential for rapid spread
Potential to cause serious socioeconomic or public health consequences
Of major importance in the international trade of animals and animal products

The Office International des Epizooties (OIE), also known as the Animal World Health Organization, has identified 15 agents that are considered the most serious animal pathogens globally (ie, "List A" diseases). These are outlined in the table below; for more information on each agent, see the section: Animal Pathogens.

Many of the List A diseases from OIE do not currently occur in the United States and US animals are not routinely vaccinated against them; therefore, US livestock and poultry populations are generally susceptible to these diseases.

List A Animal Diseases: From the Office International des Epizooties (OIE)
Disease	Agent	Primary Animal Hosts	Comments
African horse sickness (AHS)	AHS virus (reovirus, genus Orbivirus)	Horses Mules Donkeys Zebras	—Predominantly mosquitoborne (Culicoides species are primary vector; other vectors include Culex, Anopheles, Aedes); may be tickborne —Mortality rate in horses is 70%-95% —Cardiac and pulmonary forms occur —Enzootic in central Africa, occurs in other parts of Africa, 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
Bluetongue (BT)	BT virus (reovirus, genus Orbivirus)	Sheep Cattle Goats	—Mosquitoborne (Culicoides species) —Fever; ulceration, necrosis of oral mucosa; pneumonia; myositis; abortion in pregnant animals —Mortality up to 10% in sheep; infection usually inapparent in other animals —Occurs globally between 40° N and 35° S
Classic swine fever (hog cholera [HC])	HC virus (flavivirus, genus Pestivirus)	Pigs Wild boar	—Directly communicable between animals —Fever; hemorrhagic lesions of skin, conjunctivae; cyanosis of 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 airborne route —Fever; respiratory symptoms; infected calves may present with joint swelling —Occurs in Africa, Asia, Middle East, and southern Europe
Foot-and-mouth disease (FMD)	FMD virus (picornavirus, genus Apthovirus)	Cattle Sheep Goats Pigs Wild ruminants	—Directly communicable between animals —May be transmitted by animate (eg, human) and inanimate vectors —Airborne transmission possible —Highly contagious —Fever; vesicles on buccal and nasal mucous membranes, muzzle, teats, udders, feet —High mortality in young animals —Occurs in Asia, Africa, 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 may approach 100% —Global occurrence
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 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 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, Middle East, and Indian subcontinent
Rinderpest	Rinderpest virus (paramyxovirus, genus Morbillivirus)	Cattle Water buffalo Wild ruminants Sheep and goats Some pig species	—Directly communicable between animals via contaminated secretions and excretions —Fever; hemorrhagic diarrhea; areas of erosion, necrosis in mouth, intestines, and upper respiratory tract —Mortality rate may be high —Global eradication program is under way; 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	—Mosquitoborne (Aedes species are the primary vectors) —Febrile illness with high case-fatality rate in calves and lambs —Also causes illness in humans (eg, retinitis, meningoencephalitis, hemorrhagic fever) —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 inanimate vectors —May be transmitted by the airborne route —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, udder, teats, testicles; pulmonary involvement may occur —Endemic in Africa, Middle East
Swine vesicular disease (SVD)	SVD virus (picornavirus, genus Enterovirus)	Pigs	—Directly communicable between animals —Fever; vesicles on snout, interdigital spaces of feet, buccal mucosa, tongue, and teats —Disease has been recognized in Hong Kong, Japan, and Europe
Vesicular stomatitis (VS)	VS virus (rhabovirus, genus Vesiculovirus)	Horses Cattle Pigs Deer and other wild animals	—Directly communicable between animals —Arthropod transmission may occur —Vesicles in mouth, around nostrils, muzzle, 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 Web site (see References).

All of these agents are identified in the Agricultural Bioterrorism Act of 2002 as agents that could pose a severe threat to animal health, animal and human health (ie, Rift Valley fever), or animal products in the United States. In addition to the OIE List A diseases, the Agricultural Bioterrorism Act includes the following diseases:

Akabane virus
Bovine spongiform encephalopathy
Camelpox virus
Contagious caprine pleuropneumonia
Cowdria ruminantium (heartwater)
Japanese encephalitis
Malignant catarrhal fever
Menangle virus
Nipah virus

Potential Crop Pathogens

Microorganisms

A number of microorganisms could disrupt crop production and lead to substantial economic loss if spread deliberately through a bioterrorist act. Recently, the USDA identified a list of pathogens considered to pose a severe threat to plant health, production, or marketability in the United States (see References: USDA: Agricultural Bioterrorism Act of 2002). These are outlined in the table below.

Crop Diseases Considered to Pose a Severe Threat to Plant Health, Production, or Marketability in the United States*
Disease	Agent	Crops Affected
Rice bacterial leaf streak (or blight)	Xanthomonas oryzae pv oryzicola	Rice
Bacterial wilt	Ralstonia solanacearum race 3, biovar 2	Soybeans, potatoes
Brown stripe downy mildew	Sclerophthora rayssiae var zeae	Corn
Huanglongbing (citrus greening)	Liberobacter africanus Liberobacter asiaticus	Citrus fruit
Potato wart	Synchytrium endobioticum	Potatoes
Plum pox	Plum pox potyvirus	Stone fruit
Philippine downy mildew	Peronosclerospora philippinensis	Corn
Soybean rust	Phakopsora pachyrhizi	Soybeans
Citrus variegated chlorosis	Xylella fastidiosa	Citrus fruit
*According to the USDA Agricultural Bioterrorism Act of 2002.

Additional plant pathogens are considered to pose a major threat by some experts (see References: Kohnen 2000, Madden 2001, Parker 2002). Examples include:

Cereals (wheat, barley, rye)

Wheat stem rust (Puccinia graminis)
Wheat smut (Fusarium graminearum)
Stripe rust of cereals (Puccinia glumarum)
Powdery mildew of cereals (Erysiphe graminis)
Wheat dwarf geminivirus

Rice

Rice blast (Pyricularia oryzae)
Rice brown-spot disease (Helminthosporium oryzae)

Corn

Corn blight (Pseudomonas alboprecipitans)

Potatoes

Late blight of potato (Phytophthora infestans)

Other fruits and vegetables

Sweet orange scab (Elsinoe australis) (affects citrus fruit)
Black spot (Guignardia citricarpa) (affects citrus fruit)
Apple proliferation (Phytoplasma) (affects apples)
Tomato yellow leaf curl (TYLCV virus) (affects tomatoes)
Citrus canker (Xanthomonas axonopodis pv. citri) (affects citrus fruit)

Pests

In addition to microorganisms, certain insects could pose an important economic threat to some crops. Examples include the following (see References: Parker 2002):

Asian longhorn beetle
Boll weevil
Grape louse
Whitefly
Wheat aphid

References

Cameron G, Pate J, Vogel KM. Planting fear: how real is the threat of agricultural terrorism? Bull At Sci 2001;57(5):38-44 [Full text]

Casagrande R. Biological terrorism targeted at agriculture: the threat to US national security. Nonproliferation Review; 2000 Fall/Winter;7.3 [Full text]

Chalk P. The US agricultural sector: a new target for terrorism? Jane's Intelligence Review 2001 Feb 9 [Full text]

Ekboir JM. Potential impact of foot-and-mouth disease in California: the role and contribution of animal health surveillance and monitoring services. 1999 University of California, Davis, Agricultural Issues Center [Full text]

Ferguson NM, Donnelly CA, Anderson RM. Transmission intensity and impact of control policies on the foot-and-mouth epidemic in Great Britain. (Letter) Nature 2001;413:542-8 [Full text]

Kohnen AS. Responding to the threat of agroterrorism: specific recommendations for the United States Department of Agriculture. BCSIA Discussion Paper 2000-29, ESDP Discussion Paper ESDP-2000-04, John F. Kennedy School of Government, Harvard University, Oct 2000 [Full text—click on pdf link near bottom].

Madden LV. What are the nonindigenous plant pathogens that threaten US Crops and forests? St Paul, MN: American Phytopathological Society, Oct 31, 2001 [Full text]

MIIS (Monterey Institute of International Studies). Agricultural biowarfare: state programs to develop offensive capabilities [Web page]

MIIS (Monterey Institute of International Studies). Chronology of CBW attacks targeting crops and livestock 1915-2000 [Web page]

NRC (National Research Council). Countering agricultural bioterrorism. 2002 [Ordering instructions]

Parker HS. Agricultural bioterrorism: a federal strategy to meet the threat. Institute for National Strategic Studies, National Defense University. McNair paper. Mar 2002 [Full text]

Pate J, Cameron G. Covert biological weapons attacks against agricultural targets: assessing the impact against US agriculture. BCSIA Discussion Paper 2001-9, ESDP Discussion Paper ESDP-2001-05; John F. Kennedy School of Government, Harvard University, Aug 2001 [Full text]

Rogers P, Whitby S, Dando M. Biological warfare against crops. Sci American 1999 Jun;280(6):70-5

USDA. Agricultural Bioterrorism Protection Act of 2002. [Full text]

USDA/APHIS. Highly pathogenic avian influenza. Feb 2002 [Full text]

Watson SA. The changing biological warfare threat. Anti-crop and anti-animal agents. Ann NY Acad Sci 1999;894:168-80

Wheelis M. Agricultural biowarfare and bioterrorism. Federation of American Scientists, Chemical & Biological Arms Control Program. 2002 [Web page]


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