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Entomological terrorism: a tactic in asymmetrical warfare.

Historically, most US wartime casualties have been from disease and nonbattle injuries. If proper precautions are not taken, diseases like malaria, leishmaniasis, giardiasis, and botulism can have a detrimental impact on military personnel, their units, and their missions. Preventive medicine and public health personnel at all levels must remain vigilant during deployments to protect Soldiers from contracting food, water, and vector-borne diseases. The current operational environment, with insurgents using unconventional, indirect attacks against US forces, has caused the military to prepare for a wide array of enemy tactics. Improvised explosive devices (IEDs), vehicle-borne IEDs, snipers, and suicide bombers have all been used against military personnel, local security forces, and various local nationals in the Iraq and Afghanistan theaters. Another unconventional tactic that could be used by our nation's enemies is the use of biological terrorism, also known as bioterrorism.

Bioterrorism is defined as the deliberate release of viruses, bacteria, or other pathogens to cause illness or death in people, animals, or plants. (1) It should be noted that this definition excludes macrobiotic organisms, such as insects, which have been used to attack humans and agriculture. We would expand the Centers for Disease Control and Prevention definition to recognize the history and future of bioterrorism as including all living organisms. Insects have the potential to act as effective instruments for bioterrorism. This article will specifically address the threat posed to both the US civilian population and military personnel from entomological terrorism.

Entomological terrorism can be organized into 3 major categories: the use of insects as weapons of direct attacks, as agents of agroterrorism, and as disease vectors. (2) We would note that these categories are not mutually exclusive. For example, a plant disease vector could be an agent of agroterrorism.

Composite risk management (CRM) is the Army's primary decision-making process to identify hazards, reduce risk, and prevent both accidental and tactical loss. (3) The US Army Center for Health Promotion and Preventive Medicine Technical Guide 288, (4) used by preventive medicine personnel, applies the CRM concept to vector-borne disease threats encountered by military personnel. Risk management in the Army, regardless of what is being assessed, ultimately seeks to preserve the fighting force for future operations. Technical Guide 288 provides the framework to assess entomological hazards faced by military personnel, but was not intended to serve as a guide for analyzing entomological terrorist threats to our nation. The tactics used by our adversaries in overseas contingency operations have in many instances focused on targets other than military personnel. Unconventional strategies used by our enemies have included terrorist attacks to our nation on September 11, 2001, our international embassies, and our allies to include the Iraq and Afghan governments. Bioterrorism, including entomological terrorism, can instill fear in a society, devastate economies, and cause disease throughout a populace. Entomological threats should be further evaluated with considerations given to their potential use in attacks by our nation's enemies. Applying the Army's CRM and using Technical Guide 288 as a guide, examples of each form of entomological terrorism (direct attacks, agroterrorism, and disease vectors) are assessed in this article to illustrate their potential threat to the health of our nation's military, economy, and society.

DIRECT ATTACKS

Stinging insects were used for millennia in conflicts as a means of defending fortifications or routing enemies from entrenched positions. (2) It may appear that modern weapons have eliminated the need to conscript insects for such purposes, but such tactics were used by the Vietcong against US troops in Vietnam, (2) and their use by terrorists in a direct attack is not altogether improbable. More likely, military personnel will have natural exposures to biting, stinging, or toxic insects as part of military deployments in less sheltered conditions and unfamiliar environments.

According to Technical Guide 288:
   In addition to vector-borne and zoonotic disease,
   entomological hazards during deployment also include
   those hazards associated with biting and stinging
   arthropods, animals, poisonous plants, and pesticide
   exposure. Biting and stinging arthropods can degrade
   mission readiness and combat effectiveness even
   though they are relatively free of vector-borne disease.
   These arthropods can cause casualties from secondary
   infections and even death from allergic reactions to
   their venom. Annoyance from high populations of
   pests, itching bites, and loss of sleep can also reduce
   morale. (4) (p2)


One documented threat to military personnel that could be used in a direct attack or encountered in the environment is the Paederus beetle. (5) Paederus is a genus of rove beetles (family Staphylinidae) and are found in the Middle East and the Asian subcontinent. Most species are slender, about 7 mm to 13 mm long, and are distinctly colored with black heads, orange bodies, black abdominal tips, and metallic blue or green elytra (5) (Figure 1). A string of suppurating sores appears when someone brushes away a beetle and inadvertently smears the insect and the toxin, pederin, across the skin. Less than a hundred-thousandth of a gram of this chemical can cause festering lesions. (2) Intense pain and temporary blindness have been reported when pederin is introduced into the eyes. These sores, although not fatal, may result in lost duty time. (6) Ingestion of the beetle leads to severe and even deadly internal damage. Pederin is lethal if injected into the bloodstream. (2)

Military personnel currently conduct operations in environments throughout Iraq that support Paederus beetle populations. The entomological hazard assessment (4) for Paederus beetles in these areas of Iraq was evaluated based on the severity and probability of exposure. Paederus beetles pose a "marginal" hazard to military personnel and the probability of receiving an injury by these beetles would be "occasional," therefore, the risk estimate for this entomological threat is "moderate" in areas with Paederus beetle populations. Military personnel can reduce the risk of the typical method of exposure to these beetles by applying an indoor residual spray (permethrin) in tents (D. A. Strickman, PhD, oral communication, January 2010), not working or resting under bright lights during May through July, properly wearing uniforms, and using window screens to help prevent Paederus beetles and other insects from traveling toward light sources indoors. (6)

The stings and bites of insects and arthropods are one threat the US Army should be able to manage effectively. Since its adoption, the Geneva Protocol of 1925 (7) has prevented most nations from using chemical or biological weapons. The use of insects to vector pathogens is also prohibited under the Protocol. However, terrorists do not bind themselves to such protocols and could possibly employ biological weapons against the United States. The difficulty in the control of biological pathogens indicates that terrorists would probably use them at a location remote from their own territory (ie, against civilians residing in the United States). On the other hand, it is evident that terrorists are willing to both kill their countrymen and to die in attacks against US forces, which suggests that there are no places entirely safe from biological weapons. The 2 main entomological terrorism threats to the United States at home are agroterrorism and vector-borne disease threats.

[FIGURE 1 OMITTED] (6)

AGROTERRORISM

Agroterrorism is defined as:
   the deliberate introduction of an animal or plant disease
   as well as damage to crops and livestock with the goal
   of generating fear, causing economic losses, and/or
   undermining social stability. (8)


Insects can be agents of agroterrorism as they can vector plant or animal pathogens or directly damage economically important crops and livestock. Table 1 identifies plant pests of significant concern in terms of bioterrorist potential. Many insects that are problematic to agriculture are invasive species. Invasive species can be defined as species that have a demonstrable ecological or economic impact and that have become established in a region outside of their native range. (10) Insects that become invasive to the United States can arrive in various ways, including:

* Accidental introductions of a species by global travel or trade

* Species originally released for agricultural or economic gains that later became problematic pests

* Species released in an act of bioterrorism against our nation

Agriculture and livestock remain a vital part of the economic stability of the United States. Although farming employs less than 2% of the country's workforce, 16% of the workforce is involved in the food and fiber sector, ranging from farmers and input suppliers to processors, shippers, grocers, and restauranteurs. (11) The US produces and exports a large share of the world's grain. In 2003, the US share of world production was 42% for corn, 35% for soybeans, and 12% for wheat. Of global exports, the US accounted for 65% for corn, 40% for soybeans, and 32% for wheat. (12)

Economic losses from an agroterrorist incident could have the following effects:

* Value losses in terms of lost production, cost of destroying diseased animals or products, and cost of containment (drugs, diagnostics, pesticides, and veterinary services). (8)

* The imposition of trade restrictions on US exports by foreign nations to prevent the disease or pest from spreading.

* Damage to the US economy as tourism and agriculturally dependent businesses suffer.

* State and federal governments burdened by the significant costs associated with disease or pest eradication, containment efforts, and compensation to farmers for their losses.

The Mediterranean fruit fly (Ceratitis capitata Wiedemann), commonly known as the Medfly (Figure 2), is a possible entomological agent that could be used against the United States for the purposes of agroterrorism. The species is found in Hawaii, but is not established on the US mainland . The larvae of this fly eat a wide variety of plants, including avocados, coffee, olives, tomatoes, bananas, citrus, mangos, and peaches. (2) If Medflies were established in California, a total quarantine of California fruits, both nationally and internationally, would result in the loss of 132,000 jobs and $13.4 billion. (13)

Medflies played the central role in a relatively recent entomological threat faced by our nation's citrus growers. In 1989, an ecoterrorist group known as the "Breeders" threatened to release Medflies in California if the state did not stop its pesticide spraying program. The State of California was spraying pesticides, ironically, to remove Medflies that had appeared in the Los Angeles area. (2)

Applying the criteria of Technical Guide 288, the severity of damage caused by Medflies to the United States would be "critical" and the probability of this pest occurring and becoming established is "likely," therefore the risk assessment for this pest is "high." There are mechanical, cultural, biological, and chemical control measures that can be used to control and eliminate Medflies, however, preventing the Medfly from establishing itself on the mainland would be less expensive than control measures.

There are ways to mitigate the threat of agroterrorism to our nation. Monitoring, containment, and continued research will help prevent a terrorist event. The following are several suggestions to stop agroterrorism:

* Increase funding for research and eradication programs of invasive species present in the United States.

* Establish or continue monitoring programs for invasive species such as the Medfly, the Emerald Ash Borer (Agrilus planipennis Fairmaire) (monitoring in adjacent states that have not previously had this pest), and the Khapra beetle (Trogoderma granarium Everts), a grain and stored products pest.

* Ensure agencies responsible for monitoring trade and security threats to the United States are trained to identify entomological hazards and deter their entry to the United States. Possible participating agencies include the Food and Drug Administration, Food Safety and Inspection Service, and US Customs and Border Protection. The agency primarily responsible for this function is the US Department of Agriculture (USDA) Animal and Plant Health Inspection Service (APHIS).

[FIGURE 2 OMITTED]

DISEASE VECTORS

An intentional release of a vector-borne disease by adversaries of the United States is a realistic threat to our nation. Table 2 provides a list of arthropod-transmitted diseases that could be delivered in a terrorist act that pose significant risks to plant, animal, and human health. The adverse effects caused by the introduction of certain arthropod-vectored pathogens to the United States, whether accidental or intentional, could ultimately result in illness and death from disease or devastation of the economy. This could be compounded if the introduced pathogen became established within our nation's borders and persisted, despite control and eradication efforts. Engineering new strains of viruses would require resources that typical insurgent groups do not possess at present, but many naturally occurring pathogens do exist that would need minimal effort to develop into biological weapons. Furthermore, the delivery of these diseases by terrorists to US soil could be simple and leave little to no evidence of the attack.

Rift Valley fever is an excellent example of a disease that would require little effort to deliver to the United States, and could have devastating effects on the nation's public health and livestock industry. Rift Valley fever (RVF) is caused by a virus in the family Bunyaviridae and occurs in various regions of sub-Saharan Africa and Madagascar. (19) Recent outbreaks in the Arabian peninsula, the first reported cases outside the African continent, have raised concerns that the disease could extend into Asia and Europe (20) (Figure 3). Numerous mosquito species transmit the virus that causes RVF, including those inhabiting North America and the United States. (21) The virus can be passed to an infected mosquito's offspring via transovarial transmission, thus enabling its persistence and maintenance in the environment through long stretches of dry conditions. Eggs infected with the virus can lay dormant until rains arrive when they will then hatch, develop in the larval and pupal stages, and emerge as disease-carrying adults. The public health and economic impacts of a RVF outbreak in the US could far exceed anything experienced by recent West Nile virus events. (2,22) Although these diseases spread in much the same manner, both the infection rate and proportion of those exhibiting severe symptoms are vastly higher in RVF.

The intentional introduction of RVF through infected mosquitoes, humans, and/or livestock represents a serious threat to both our military and civilian populations, whether delivered by a terrorist or through accidental introduction. The RVF virus is transmitted to humans by the bite of an infected mosquito or through contact with animals/meat that are infected. The mild form of RVF observed in most human infection manifests itself in the form of flu-like symptoms. The more severe form of the disease appears in one of 3 syndromes: ocular disease, meningoencephalitis, or haemorrhagic fever. Using RVF's approximate case fatality rate of 1%, (19) the analysis of a hypothetical attack allows us to better understand the implications of such an outbreak. If a small community with a population of just 10,000 people experienced a 10% RVF attack rate, the results would overwhelm the local health care infrastructure. Approximately 1,000 cases of the disease would require medical attention, with approximately 10 people ultimately dying from debilitating symptoms. In this age of constant news streams from cable networks (ie, CNN, MSNBC, Fox News), word of even a small outbreak of RVF would make headlines.

The absence of human cases occurring in a RVF bioterrorist attack would not equate to failure for our adversaries. An intentional release of RVF would also be a form of agroterrorism, for the livestock losses this disease can cause could cripple a large part of our national economy. Cattle, sheep, dogs, and rodents are among the many animals susceptible to RVF. Outbreaks of RVF have been characterized by high attack rates in livestock, with 30% mortality and abortion rates approaching 100%. (23) Corrie Brown, an animal infectious disease specialist who supervised the pathology section of USDA's Plum Island Animal Disease Center in New York, contends that if an outbreak occurred in the United States, domestic beef exports would shut down. (2,24) This impact on the beef industry would result in a $3 billion ([10.sup.9]) loss to the economy. (2,24)

The composite risk assessment for the threat of RVF being delivered in an act of terrorism was estimated to be a "high" due to its "critical" severity and its probability occurrence "likely." (4) Control measures that can mitigate the risk of RVF include:

* Continue mosquito surveillance programs to both monitor various pathogen infection rates (ie, West Nile and Eastern Equine Encephalitis) in vector populations as well as maintain preparedness in the event of an RVF or other mosquito-borne disease outbreak.

* Monitor conditions suitable for RVF outbreaks (eg, regional flooding, hurricanes) to focus mosquito control and surveillance efforts.

* Develop and rehearse RVF outbreak response plans to be implemented by the Department of Homeland Security (DHS) and Federal Emergency Management Agency.

* Ensure RVF vaccine could be readily available for the public in the event of an outbreak. An inactivated vaccine has been developed for human use. However, this vaccine is not licensed and is not commercially available. It has been used experimentally to protect veterinary and laboratory personnel at high risk of exposure to RVF. Other candidate vaccines are under investigation. (20)

* Institute a mobile, federal vector control force that could respond to such emergencies.

[FIGURE 3 OMITTED]

Various state, federal, and international entities have recognized the threat of RVF and have implemented some of the above control measures. Contingency planning, predictive disease modeling, and outbreak response exercises represent some of the recent developments to combat RVF threats in both endemic and potentially exposed geographic regions. The Food and Agriculture Organization (FAO) of the United Nations is just one of the international agencies providing guidelines for development of RVF contingency plans. (25) The FAO provides vital information for animal and human health authorities of individual countries by specifying RVF details regarding risk analysis, prevention strategies, early warning signs, forecasting, and control strategies.

Weather patterns and anomalies have been used recently to model and predict RVF outbreaks. In Africa, outbreaks of RVF are integrally tied to widespread elevated rainfall, and the subsequent flooding and increase in vegetation. (26) Risk mapping using climate and normalized difference vegetation index data led to the first prediction of an RVF outbreak from December 2006 to May 2007. (27) The predicted RVF occurrence provided a warning period of 2 to 6 weeks that facilitated response and mitigation activities. The outbreak that subsequently occurred validated the utilization of risk mapping models to predict future RVF events.

While contingency plans and outbreak predictions provide the logistical framework and science needed, rehearsing the execution of epidemic disease scenarios, with all responding agencies involved, ultimately provides the best gauge of response preparedness. In November 2008, Paul Gibbs, PhD, from the College of Veterinary Medicine at the University of Florida supervised a multiagency test of Florida's response to a hypothetical introduction of RVF (http://www.flsart.org/rvf/index.htm). Incorporating various state and federal participants, including the DHS, the Federal Bureau of Investigation, and the USDA, the exercise trained major stakeholders to collaborate in response to an introduction of RVF virus into Florida. In light of the original event's success, 2 additional RVF exercises were planned and conducted in Puerto Rico and the Virgin Islands by Dr Gibbs and Dana McDaniel, DVM, in 2010 (Dr McDaniel, oral communication, March 2010).

The control measures discussed could reduce the impact from an RVF outbreak, whether the virus is delivered by terrorists or arrives by accident. Without further scientific advances in RVF forecasting, vaccine development, vector control, and diagnostic capabilities, it may be unrealistic to expect to attain the necessary resources required to build and maintain comprehensive control measures to eliminate the threat to our nation of RVF and similar vector-borne diseases. We conclude that the residual risk associated with the threat of RVF, and other vector-borne diseases, remains "high."

DISCUSSION

Entomological terrorism, regardless of its form, is a current and future threat faced by the United States. The estimated risks of the threats outlined in this article are speculative, however, it would be difficult to argue that the hazards associated with entomological terrorism are negligible. The US government has long recognized the consequences of biological warfare. The federal agencies conducting research and development on vector-borne diseases and crop pests include, but are not limited to the following:

* DHS: National Center for Foreign Animal and Zoonotic Disease Defense, and US Customs and Border Protection

* US Army Medical Research Institute of Infectious Disease (USAMRIID)

* Walter Reed Army Institute of Research

* USDA-Agricultural Research Service (ARS) and Animal and Plant Health Inspection Service

Additionally, some local abatement districts, a few state governments (ie, Florida, California), and numerous universities have also made significant contributions to research on vector-borne infectious diseases.

Merely studying the biology of a disease does not prepare us for response to an actual outbreak. Many aspects of an appropriate response to an entomological emergency still must be addressed, including:

* Is the pest management community prepared for an outbreak with the necessary equipment and knowledge to implement control techniques?

* Can pest management resources be quickly consolidated, mobilized, and deployed to outbreak locations?

* Are emergency organizations prepared with individual response plans for specific entomological threats, especially those posing high risk?

Accidental introductions of invasive arthropod species have a higher likelihood of occurring than intentional deliveries through terroristic plots. Military personnel moving to and from forward deployed environments can do their part in preventing the introduction of invasive species by thoroughly inspecting cargo transported by military transportation vehicles and by conducting retrograde washdowns of vehicles and equipment after a deployment. (28) The importance of preventing invasive species is illustrated by the costs currently incurred by these species in the United States. Damage caused by invasive species currently in the United States is estimated at $120 billion to $138 billion each year. (29) Crop losses and control costs due to invasive insects and pathogens were estimated at $25 billion in 2005.29 There are approximately 500 invasive insect and mite species in crops and an estimated 20,000 species of microbes, including introduced plant pathogens, that have invaded the United States thus far. (29) Additional invasive species would only compound the problem and costs caused by these pests.

Even with proper systems and technological advances in place to prevent attacks or mitigate the effects of disasters, the United States still faces a deficiency in the number of trained, qualified healthcare professionals. A large portion of the healthcare workforce (including public health professionals, clinicians, and related healthcare fields) in the United States is approaching retirement age. (30) Health professionals are not being trained at a rate needed to fill the loss of retirees. (30) Federal (including the US Army) and state agencies responsible for emergency preparedness and response will soon face personnel challenges requiring additional efforts to educate, train, and retain such public health professionals. A terrorist attack, especially with a biological weapon, would be more devastating if the medical infrastructure is poorly prepared, staffed, and funded.

CONCLUSION

Vector-borne diseases are a current threat because of the self-perpetuating capabilities and delayed morbidity and mortality following exposure or infection. (31) Most disease causing organisms used as biological weapons, particularly the zoonoses, can be delivered to a target population without risk of immediate detection. (31) This article illustrates that insects and other arthropods can be used by an enemy to attack US military personnel and civilians. Some recommendations on how to mitigate the specific threats given (ie, Paederus beetles, Medfly, Rift Valley fever) were presented, however, all military personnel can mitigate vector-borne disease threats by taking relatively simple actions.

* Deploying Soldiers and DoD personnel should practice operational risk management (ORM) for infectious diseases. Excellent resources for understanding and following ORM are Technical Guide 288, (4) as well as the website for the National Center for Medical Intelligence (http:// www.phsource.us/PH/MI/index.htm).

* Personal Protective Measures should be implemented when training within the United States and when deploying outside the country. Treating uniforms with permethrin, or purchasing uniforms that are pretreated with permethrin, as well as using N,N-diethyl-3-methylbenzamide (deet) on exposed skin can reduce the likelihood of contracting mosquito--or tick-borne diseases during field training. The use of personal protective measures will not only help protect the individual from a new emerging vector-borne disease like RVF, but also prevent Soldiers from contracting Rocky Mountain spotted fever, Lyme disease, West Nile virus, Ehrlichiosis, and other vector-borne diseases present in the United States.

* Military personnel conducting food and water vulnerability assessments (32) or retrograde operations are critical players in security by helping protect food and water from exposure to biological agents and by preventing them, including vectors and invasive species, from entering the country.

Invasive pests and the diseases they may carry represent a threat that is magnified when terrorism is involved. The research conducted by academic institutions, a host of federal agencies (eg, USDA-ARS) and the US military (eg, USAMRIID), coupled with entities capable of organizing emergency response activities (eg, DHS, Federal Emergency Management Agency, state and local authorities), provide the critical framework needed to address the entomological threats we face. It would be ideal to provide a definitive countermeasure to entomological terrorism, however, this may be unfeasible due to the financial and logistical challenges involved. The most critical countermeasure to entomological terrorism is the same for any form of terrorism--vigilance by the US military, government agencies, citizens, and our allies. (31)

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ACKNOWLEDGEMENTS

We thank Dan Strickman, PhD, Alex Gerry, PhD, LTC Mark Carder, LTC Timothy Bosetti, LTC Robert Richards, MAJ Robert Lowen, CPT Wes McCardle, and Jim Harrison for constructive comments and review of this article.

REFERENCES

(1.) CDC (Centers for Disease Control and Prevention). Bioterrorism Overview Page. Available at: http:// www.bt.cdc.gov/bioterrorism/overview.asp. Updated February 12, 2007. Accessed December 26, 2009.

(2.) Lockwood JA. Six-legged Soldiers: Using Insects as Weapons of War. New York, NY: Oxford University Press, Inc.; 2009.

(3.) Field Manual 5-19: Composite Risk Management. Washington, DC: Dept of the Army. August 2006.

(4.) Technical Guide 288: Entomological Operational Risk Management. Aberdeen Proving Ground, MD: US Army Public Health Command (Provisional). September 2003. Available at: http://chppmwww.apgea.army.mil/documents/TG/TECHGUID/ TG288.pdf. Accessed April 15, 2010.

(5.) Davidson SA, Norton SA, Carder MC, Debboun M. Outbreak of dermatitis linearis caused by Paederus ilsae and Paederus iliensis (Coleoptera: Staphylinidae) at a military base in Iraq. Army Med Dept J. July-September 2009:6-15.

(6.) Just the Facts ... Paederus Beetles 18-071-1108. Aberdeen Proving Ground, MD: US Army Public Health Command (Provisional). November 2008. Available at: http://usachppm.apgea.army.mil/ Documents/FACT/PaederusBeetleFactSheet.pdf. Accessed December 28, 2009.

(7.) Protocol for the Prohibition of the Use of Asphyxiating, Poisonous or Other Gasses, and of Bacteriological Methods of Warfare. Geneva, Switzerland: Conference for the Supervision of the International Trade in Arms and Ammunition; June 17, 1925. Available at: http://www.icrc.org/IHL.NSF/ FULL/280?OpenDocument. Accessed December 26, 2009.

(8.) Monke J. Agroterrorism: Threats and Preparedness. Washington, DC: Congressional Research Service; March 12, 2007:1. CRS Report for Congress Order Code RL 32521. Available at: http://www.fas.org/ sgp/crs/terror/RL32521.pdf. Accessed December 27, 2009.

(9.) Mini Pest Risk Assessments page. USDA Animal and Plant Health Inspection Service Website. Available at: http://www.aphis.usda.gov/plant_health/ plant_pest_info/pest_detection/mini-pra.shtml. Accessed March 12, 2010.

(10.) Lockwood JL, Hoopes MF, Marchetti MP. Invasion Ecology. Malden, MA: Blackwell Publishing Ltd; 2007.

(11.) USDA Economic Research Service. Table 1: Key Statistical Indicators of the Food & Fiber Sector, April 2005. Available at: http://www.ers.usda.gov/ publications/agoutlook/aotables/2005/04apr/. Accessed April 19, 2010.

(12.) US Bureau of the Census. Statistical Abstract of the United States: 2004-2005. 124th ed. Washington, DC: US Bureau of the Census Agriculture; 2005. Available at: http://www.census.gov/prod/2004 pubs/04statab/agricult.pdf. Accessed April 19, 2010.

(13.) Root-Bernstein RS. Infectious terrorism. Atlantic Monthly. 1991; May: 44-50.

(14.) Frazier TW, Richardson DC, eds. Food and agricultural security: guarding against natural threats and terrorist attacks affecting health, national food supplies, and agricultural economics. Ann New York Acad Sci. 1999;894:1-232. Theme issue.

(15.) Geissler E, ed. Biological and Toxin Weapons Today. New York, NY: Oxford University Press; 1986.

(16.) Pelzel AM. Cattle fever tick surveillance in Texas. NAHSS Outlook [serial online]. August 2005. Available at: http://www.aphis.usda.gov/vs/ceah/ ncahs/nsu/outlook/issue7/cattle_fever_tick_surveillance.pdf. Accessed April 12, 2010.

(17.) Wilson TM, Logan-Henfrey L, Weller R, Kellman B. 2000. Agroterrorism, biological crimes, and biological warfare targeting animal agriculture. In: Brown C, Bolin C, eds. Emerging Diseases of Animals. Washington, DC: ASM Press; 2000:23-57.

(18.) World Health Organization. Global early warning system for major animal diseases, including zoonoses. Available at: http://www.who.int/zoonoses/ outbreaks/glews/en/index2.html. Accessed March 24, 2010.

(19.) Center for Disease Control and Prevention. Rift Valley Fever Fact Sheet. Available at: http:// www.cdc.gov/ncidod/dvrd/spb/mnpages/dispages/rvf/ rvf_qa.htm. Updated January 2, 2007. Accessed January 17, 2010.

(20.) World Health Organization. Rift Valley fever. Available at: http://www.who.int/mediacentre/ factsheets/fs207/en/. Updated September 2007. Accessed January 18, 2010.

(21.) Gargan TP, Clark CG, Dohm DJ, Turell MJ, Bailey CL. Vector potential of selected North American mosquito species for Rift Valley fever virus. Am J Trop Med Hyg. 1988;38:440-446.

(22.) Selim J. Virus code red. Discover Mag. March 2005:14.

(23.) Patrick KW, ed. Military Preventive Medicine: Mobilization and Deployment. Vol 2. Washington, DC: Office of The Surgeon General, Dept of the Army; 2005:825.

(24.) McGinnis D. Looking for loopholes. Beef Mag. July 2004. Available at: beefmagazine.com/mag/beef_looking_loopholes/. Accessed April 19, 2010.

(25.) FAO Animal Health Manual No. 15: Preparation of Rift Valley fever (RVF) contingency plans. Rome, Italy: Food and Agriculture Organization of the United Nations; 2002. Available at: ftp://ftp.fao.org/ docrep/fao/005/y4140e/y4140e00.pdf. Accessed February 18, 2010.

(26.) Davies FG, Linthicum KJ, James AD. Rainfall and epizootic Rift Valley fever. Bull World Health Organ. 1985;63:941-943.

(27.) Anyamba A, Chretien J, Small J, et al. The first prediction of a Rift Valley fever outbreak. PNAS: Proc Natl Acad Sci USA. 106.3 2009:955-959.

(28.) Technical Guide 31: Retrograde Washdowns: Cleaning and Inspection Procedures. Washington, DC: Armed Forces Pest Management Board. March 2008.

(29.) Pimentel D, Zuniga R, Morrison D. Update on the environmental and economic costs associated with alien species in the United States. Eco Econ. 2005;52:273-288.

(30.) American Association for the Advancement of Science. Center for Science, Technology and Security Policy Page. Available at: http://cstsp.aaas.org/ content.html?contentid=2215. Accessed February 17, 2010.

(31.) Kendall RJ, Presley SM, Austin GP, Smith PN, eds. Advances in Biological and Chemical Terrorism Countermeasures. Boca Raton, FL: CRC Press; 2008.

(32.) Technical Guide 188: US Army Food and Water Vulnerability Assessment Guide. Aberdeen Proving Ground, MD: US Army Public Health Command (Provisional). July 2008.

CPT Derek Monthei, MS, USA

CPT Scott Mueller, MS, USA

Jeffrey Lockwood, PhD

COL Mustapha Debboun, MS, USA

CPT Monthei is a Medical Entomologist, Entomological Sciences Division, US Army Public Health Command (Provisional) Public Health Region-West, Joint Base Lewis-McChord, Washington.

CPT Mueller is a Medical Entomologist, Entomological Sciences Division, US Army Public Health Command (Provisional) Public Health Region-North, Fort Meade, Maryland.

Dr Lockwood is Professor of Natural Sciences and Humanities at the University of Wyoming, Laramie, WY. He is the author of Six-Legged Soldiers: Using Insects as Weapons of War (2009, Oxford University Press).

COL Debboun is Program Manager, Medical Education Training Campus Transition, and Chairman of the AMEDD Journal Editorial Review Board, US Army Medical Department Center & School, Fort Sam Houston, Texas.
Table 1. Exotic plant pests of greatest risk. (a)

Pest                    Expected Range         Ecological
Common Name(s):                                Suitability (b)
Scientific Name

Japanese wax scale:     67% US (eastern and    High
Ceroplastes             western states)
japonicas

Metallic beetle, Oak    67% US (eastern and    High
spl endo r be et le:    western states)
Agrilus biguttatus

Rice cutworm, Cotton    67% US (eastern and    High
leafworm: Spodoptera    western states)
litura

Silvery moth:           50% US (eastern and    High
Autographa gamma        parts of western
                        states)

Egyptian cotton         67% US (eastern and    High
leafworm: Spodoptera    western states)
littoralis

Passionvine             67% US (western and    Medium
mealybug:               mid-western states)
Planococcus minor

Light brown apple       90% US                 High
moth: Epiphyas
postvittana

Khapra beetle:          67% US (eastern and    High
Trogoderma granarium    western states)

Arrowheadscale:         33% US (eastern,       Medium
Unaspis yanonensis      portions of midwest
                        and California)

Siberian silk moth:     80% US (except parts   High
Den drol imus           of western states)
superans

Ambrosia beetle:        33% US (eastern        Medium
Platypus quercivorus    states and Oregon)

Summer fruit tortrix    25% US (eastern        Medium
moth: Adoxophyes        states and Oregon)
orana

Pink gypsy moth:        50% US (eastern and    Medium
Lymantria Mathura       parts of western
                        states)

Pest                    Survey           Taxonomic
Common Name(s):         Difficulty (c)   Difficulty (d)
Scientific Name

Japanese wax scale:     High             Medium
Ceroplastes
japonicas

Metallic beetle, Oak    High             Medium
spl endo r be et le:
Agrilus biguttatus

Rice cutworm, Cotton    Medium           High
leafworm: Spodoptera
litura

Silvery moth:           Medium           High
Autographa gamma

Egyptian cotton         Medium           High
leafworm: Spodoptera
littoralis

Passionvine             High             Medium
mealybug:
Planococcus minor

Light brown apple       Medium           High
moth: Epiphyas
postvittana

Khapra beetle:          Low              High
Trogoderma granarium

Arrowheadscale:         High             Medium
Unaspis yanonensis

Siberian silk moth:     Low              Medium-Low
Den drol imus
superans

Ambrosia beetle:        Medium           Medium
Platypus quercivorus

Summer fruit tortrix    Low              Medium
moth: Adoxophyes
orana

Pink gypsy moth:        Low              Low
Lymantria Mathura

Pest                    Primary                Potential
Common Name(s):         Damage                 Economic
Scientific Name                                Risk

Japanese wax scale:     Ornamentals Fruits     High
Ceroplastes
japonicas

Metallic beetle, Oak    Oak                    High
spl endo r be et le:    Beech Chestnut
Agrilus biguttatus

Rice cutworm, Cotton    Vegetables Field       High
leafworm: Spodoptera    crops
litura

Silvery moth:           Vegetables Field       High
Autographa gamma        Crops Greenhouses

Egyptian cotton         Cotton Vegetables      High
leafworm: Spodoptera    Ornamentals Forages
littoralis

Passionvine             Many crops             High
mealybug:
Planococcus minor

Light brown apple       Ornamentals Fruits     High
moth: Epiphyas
postvittana

Khapra beetle:          Stored grain           High
Trogoderma granarium

Arrowheadscale:         Citrus Vegetables      High
Unaspis yanonensis      Trees

Siberian silk moth:     Conifers               High
Den drol imus
superans

Ambrosia beetle:        Oak Chestnut           High
Platypus quercivorus

Summer fruit tortrix    Fruit                  High
moth: Adoxophyes
orana

Pink gypsy moth:        Fruit crops Forests    High
Lymantria Mathura

Pest                    Potential        Potential
Common Name(s):         Environmental    for
Scientific Name         Impact           Establishment

Japanese wax scale:     High             High
Ceroplastes
japonicas

Metallic beetle, Oak    High             High
spl endo r be et le:
Agrilus biguttatus

Rice cutworm, Cotton    (Low)            High
leafworm: Spodoptera
litura

Silvery moth:           (Low)            High
Autographa gamma

Egyptian cotton         (High)           Medium- High
leafworm: Spodoptera
littoralis

Passionvine             High             High
mealybug:
Planococcus minor

Light brown apple       (Low)            Medium
moth: Epiphyas
postvittana

Khapra beetle:          Medium           High
Trogoderma granarium

Arrowheadscale:         Medium           High
Unaspis yanonensis

Siberian silk moth:     High             High
Den drol imus
superans

Ambrosia beetle:        High             Medium
Platypus quercivorus

Summer fruit tortrix    High             High
moth: Adoxophyes
orana

Pink gypsy moth:        High             Medium
Lymantria Mathura

(a) Data adapted from the USDA Animal and Plant Health Inspection
Service Mini Pest Risk Assessments. (9) There is no comprehensive
summary of agricultural threats, although these pests are
representative of the agents that could be used for bioterrorism. The
ratings of risk presume that each of the listed categories is of equal
weight. The qualitative assessments were converted into scores and
summed, such that "high" = 3, "medium" = 2; "low" = 1 (in all columns
"high" is associated with a quality favorable for bioterrorism).
Because potential environmental impact was not explicitly listed for
all species, this category was not included in the summed risk score
(the authors' estimates for this assessment, based on the USDA
descriptions, are shown in parentheses). When totaled scores yielded a
tie, potential environmental impact and expected range were used.

(b) Ecological suitability concerns whether the pest's life history
accords with climates, soils, and host plants in the United States and
the extent to which these ecological conditions are available.

(c) Survey difficulty addresses whether the United States has methods
to readily detect the pest (eg, pheromone traps and sampling
methodologies) and the extent to which the pest and its damage remain
cryptic.

(d) Taxonomic difficulty reflects the ease with which the pest can be
differentiated from native insects, the variability of the pest across
its life stages, and the availability of supporting materials (eg,
taxonomic keys).

(e) Species evaluated in the "mini pest risk assessments" representing
lower threats and not included in this table are (in alphabetic order
by common name): Chestnut weevil, Curculio elephas; European grape
vine moth or Grape berry moth, Lobesia botrana; False codling moth,
Thaumatotibia leucotreta Fruit piercing moth, Eudocima fullonia; Giant
woodwasp, Urocerus gigas; Old World bollworm, Helicoverpa armigera;
Soft wax scale, Ceroplastes destructor

Table 2. Arthropod-transmitted exotic diseases of potentially
significant risk to plant, animal, and human health. (a)

Disease                    Vector(s)           Pathogen

Chikungunya                Mosquitoes          Virus
Yellow fever               Mosquitoes          Virus
Japanese encephalitis      Mosquitoes          Virus
Rift Valley fever          Mosquitoes          Virus
Lumpy skin                 Mosquitoes and      Virus
                             other flies
African horse sickness     Biting midges       Virus
Russian spring-summer
  encephalitis             Ticks               Virus
Crimean-Congo
  hemorrhagic fever        Ticks               Virus
Cattle tick lever          Ticks               Virus
Africanswine fever         Ticks               Virus
New World screwworm        Adult screwworms    NA
                             flies
Tomato yellow leaf curl    Whiteflies          Virus
Citrus chlorotic dwarf     Whiteflies          Virus
Citrus variegated          Leafhoppers         Virus
  chlorosis
Lime witches' broom        Leaf hoppers        Phytoplasma
Pierce's disease           Leaf hoppers        Bacterium
Potato wilt or brown rot   Leaf hoppers,       Bacterium
                             beetles, aphids
Citrus greening            Psyllids            Bacterium

Disease                    Host(s)

Chikungunya                Humans (b)
Yellow fever               Humans (c)
Japanese encephalitis      Humans, pigs, birds
Rift Valley fever          Humans, livestock, birds
Lumpy skin                 Cattle (d)
African horse sickness     Horses
Russian spring-summer
  encephalitis             Humans (e)
Crimean-Congo
  hemorrhagic fever        Humans (f)
Cattle tick lever          Cattle
Africanswine fever         Pigs
New World screwworm        Mammalian
                           livestock (g)
Tomato yellow leaf curl    Tomatoes (h)
Citrus chlorotic dwarf     Citrus
Citrus variegated          Citrus
  chlorosis
Lime witches' broom        Lime
Pierce's disease           Grapes
Potato wilt or brown rot   Potatoes (i)

Citrus greening            Citrus

(a) Data sources: USDA, (9) Frazier and Richardson, (14) Geissler,
(15) Pelzel, (16) Wilson et al, (17) and World Health
Organization. (18)

(b) Various nonhuman animas can serve as reservoirs.

(c) Other primates can serve as reservoirs.

(d) Insect vectors are highly suspected but have not been specifically
identified.

(e) Small mammals can serve as reservoirs.

(f) Small mammals and domestic livestock can serve as reservoirs.

(g) Infestations of screwworms are not a disease in the classic sense
but share many important commonalities with pathogenic infections.

(h) Localized infections have been found in California, but the
disease is not yet established.

(i) Insect vectors are highly suspected based on experiments with
closey related diseases but have not been specifically identified.
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Article Details
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Author:Monthei, Derek; Mueller, Scott; Lockwood, Jeffrey; Debboun, Mustapha
Publication:U.S. Army Medical Department Journal
Geographic Code:1USA
Date:Apr 1, 2010
Words:6377
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