This invited paper was presented at the CBMTS V, the fifth CBMTS plenary, Spiez Laboratory Switzerland, 25-30 April 2004 and is in the CBMTS V Proceedings.
Zoonotic Diseases, Bioterroism and Agroterrorism: Prevention by Preparedness
David H. Moore, D.V.M., Ph.D.
Battelle Memorial Institute
Introduction
Over the past several years, the scope of terrorist threats have expanded and as a result, it has become necessary to pay greater attention to the possibilities of bioterrorism and agroterrorism; potential events that could have a devastating impact to each of the countries represented at this CBMTS conference. The purpose of this presentation is to increase awareness of the relationships between zoonotic diseases, bioterrorism and agroterrorism and to raise the level of concern so as to increase the sharing of information in this area at future CBMTS meetings.
The motivations of terrorists and terrorist groups to launch attacks are many, e.g. economic, social, religious and/or political. The motivations of terrorists are not the subject, rater the potential methods and the impacts of their actions will be the focus.
Biological terrorism is defined as the use of microorganisms or toxins derived from living organisms, to cause death or disease in humans, animals, or plants in civilian settings.
Agricultural terrorism is the use, or threatened use, of biological, chemical, or radiological agents against some component of agriculture, in such a way as to adversely impact the agriculture industry or any component thereof, the economy, or the consuming public.|
Although difficult to detect, there are clues that suggest a biological agent may have been intentionally released. Healthcare providers, veterinarians and other public health professionals should be alert to illness patterns and diagnostic clues that might indicate an unusual infectious disease outbreak associated with intentional release of a biological agent. These include:
1) The unusual clustering of illness or mortality in a given geographic region or within a specific period of time for a large number of people or animals. This may also include abnormal or atypical unexplained symptoms.
2) Normally healthy individuals suddenly becoming ill.
3) Symptoms occurring in an area where a particular disease is extremely rare.
4) An unusual age distribution for common diseases.
5) A disease occurring outside its “typical” season.
Zoonoses and Agents of Concern
The United States Centers for Disease Control and Prevention (CDC) has categorized bioterrorism threat agents based on their transmissibility, mortality, public health impact and requirements for containment and response. Agents in the highest priority category are easily transmitted from person-to-person, have high mortality rates and have the potential to cause major public health impact. The agents and diseases in Category A are Anthrax, Botulism, Plague, and Smallpox, Tularemia, and Viral hemorrhagic fevers. The viral hemorrhagic fevers include Ebola and Marburg. In this group, Smallpox is the only infectious disease not considered to be zoonotic.
A zoonosis is a disease of animals that may be transmitted to man under natural conditions. In contrast, bioterrorism and agroterrorism require active (unnatural) initiation of the disease process. Both bioterrorism and agroterrorism agents can adversely impact animals, but of greater importance to public health is the fact that the majority of recognized bioterrorism and agroterrorism agents are zoonotic. Of the estimated 1,700 known pathogens affecting humans, 49% are zoonotic. Additionally, of the 156 pathogens associated with emerging diseases, 73% are zoonotic.
An example of one of the Category A zoonotic diseases is Tularemia, or “rabbit fever”, caused by the Gram negative bacterium Francisella tularensis. The disease can be transmitted by ingestion of infected, undercooked meat; bites from infected ticks, and deerflies; through direct contact with blood or tissues of infected animals; and inhalation of contaminated dust. Initial symptoms are flu-like and they include fever, chills, headache, and muscle aches. In humans there are six clinical forms of tularemia – glandular and ulceroglandular are the most common presentation of this disease. An ulcer may or may not be present at the site of infection and local lymph nodes are enlarged. Oculoglandular occurs when conjunctiva become infected by rubbing eyes with contaminated fingers or by splashing contaminated materials in the eyes. The oropharyngeal presentation is caused by ingestion of organism in contaminated food or water. Typhoidal and pneumonic forms usually occur following inhalation, or hematogenous spread of the organism. Both of these forms tend to present as atypical pneumonia and most fatalities occur with these forms and can be as high as 30-60% if untreated.
The next group is the Category B agents and diseases and has been given second priority by the CDC. In this category there are four bacterial diseases, Brucellosis, Glanders, Melioidosis, and Psittacosis and there are two rickettsial organisms causing Q fever and Typhus fever. There is also one group of viruses, the viral encephalitides, in addition to select toxins, and organisms that pose a threat to food and water.
An example of one of the Category B zoonotic diseases is Brucellosis or “undulant fever” caused by various species of Brucella, a Gram-negative bacterium. The organism can persist in the environment and in aborted fetuses or placentas. Transmission occurs via ingestion of infected food or consuming infected unpasturized milk or dairy products, via inhalation of infectious aerosols (a means of infection in slaughter facilities), or through contact with infected tissues through a break in the skin or mucous membranes. Brucellosis can involve any organ or organ system and has a very insidious onset with varying clinical signs. The one common sign in humans is an intermittent or irregular fever of variable duration, thus the term undulant fever. There are three forms of the disease in humans. In the acute form, symptomatic, nonspecific, and flu-like symptoms occur. Symptoms of the undulant form include undulant fevers, and arthritis. In the chronic form, symptoms may include chronic fatigue-like syndrome, and depressive episodes. Illness in people can be very protracted and painful and can result in an inability to work. In animals, the most common clinical signs involve abortions or infection of reproductive organs such as epididymitis, and orchitis.
There are an estimated 250 pathogens causing an estimated 70 million cases of foodborne related illnesses each year in the U.S. alone. The most commonly recognized foodborne infections are caused by Campylobacter, Salmonella and E. coli O157:H7. Viruses, toxins, parasites, and natural or manufactured chemicals can also cause foodborne disease. Most agents cause gastrointestinal upset that is self-limiting in 1-5 days. However, some agents cause severe disease complications if left untreated. Campylobacter is considered the leading bacterial cause of foodborne related diarrhea. Common sources include raw or undercooked poultry, raw milk or items contaminated with infected animal or human feces. Animal sources include poultry, cattle, puppies, kittens and pet birds. E. coli O157:H7 is another major foodborne pathogen. Common sources include undercooked or raw hamburger, salami, lettuce and alfalfa sprouts. It has also been associated with unpasteurized milk, apple juice or cider as well as contaminated well water. Cattle are the most common animal source although other mammals can serve as a source.
In 1984, the Bagwan Shree Rajneesh cult in The Dalles, Oregon deliberately contaminated salad bars with Salmonella typhimurium in an attempt to incapacitate voters for an upcoming local election. At least 10 restaurants were affected and possibly one supermarket. Additionally, coffee creamers in some restaurants were also contaminated. The incident resulted in 751 people becoming ill. It wasn’t until one of the cultists broke a vow of silence and came forth one year later that the details of the “attack” became known. Plans were being made to contaminate the water also. This incident was meant to be a trial run before a full scale biological crime.
Throughout the years in the U.S., several cult groups have planned or implemented attempts to contaminate water sources. There are a number of biological organisms and chemicals that could be used to threaten the safety of water supplies. One organism in the Category B list of water safety threats is the zoonotic organism Cryptosporidium parvum. In Milwaukee, a Cryptosporidium parvum outbreak in 1993 was caused by the contamination of the municipal water supply. Over 400,000 people were affected and 40,000 became ill. In 1997, a decorative water fountain at the Minnesota Zoo became contaminated with the same organism and there were 369 cases of disease.
The organisms or diseases of third highest priority are on the CDC Category C agent list. Nipah virus and Hantavirus are both Category C agents and emerging zoonotic infectious diseases. These viruses, like three other zoonotic viral diseases that are not on the list, SARS, avian influenza and monkeypox, are predicted to pose threats to both agriculture and human health in the future.
Agroterrorism
In the case of agricultural terrorism, fear is one of the components causing the primary impact- severe economic losses. For the U.S., export revenues accounted for 20-30% of farm revenues over the last 30 years and are expected to continue at this level for the foreseeable future. In 2003, $56.2 billion in U.S. agricultural commodities were exported; $12.2 billion were animal and animal products.
In 1999 the U.S. food and fiber system added $1.5 trillion to the economy, accounting for 16.4% of the total national gross domestic product (GDP). Furthermore, approximately 17% of the total U.S. workforce was involved in the food and fiber system. Agriculture is also heavily tied to other industries, such as equipment manufacturers, feed suppliers, transportation, food retailers, restaurants, hotels, and tourism, to name just a few. A healthy agriculture economy is vital to most national economies. Any significant disturbance in this system has the potential to: create higher prices domestically and abroad, increase unemployment, reduce trade, and result in a concurrent negative impact on other sectors of the economy.
Terrorism targeting agriculture has the potential to cause mass disruption, and to destabilize a government. The reality is that terrorism does not need to infect any nations’ entire soybean crop or all of its beef cattle to create economic hardship, loss of consumer confidence, or panic. The impact and consequences from an animal disease such as Foot and Mouth Disease (FMD) in the U.S. could be severe. Harsh restrictions on movement would be enacted. There would be road closures, quarantined farms, and animal movement would stop. Access to campsites, state parks, wilderness areas, lakes, city parks, and zoos may be denied. The public could be shocked by some of the images the outbreak produces and lose confidence in food products as consumers. Depending on the extent of the outbreak, meat prices could skyrocket in some areas and drop in others. It is unlikely that a terrorist attack would create mass food shortages; but movement restrictions could complicate availability temporarily. Restaurants, grocery retailers, food processors and distributors would be affected, as would transporters. The direct costs of eradication and control involve disease surveillance, diagnostic testing, trace back of animal movements, implementing and maintaining quarantines, depopulation costs, indemnity paid to the farmer….the list goes on and so do the costs. Losses due to such an animal disease may take years to fully realize.
Estimates of the FMD impact on the U.K. put overall economic losses over £10 billion due to the total economic strain placed on agriculture and related industries. Indeed, while it is known that six million animals were slaughtered in the U.K. to control this disease, resulting in them reaching FMD free status in less than one year, the true costs will likely never be known. The public witnessed something few had ever seen. Mass slaughter was called into question, as were animal welfare and animal rights. Those involved found themselves having to justify nearly everything they did, but their actions were viewed by some as barbaric and unnecessary. Pollution from pyres of burning carcasses was intense in some areas and also impacted public health.
In addition to the bioterrorism agents categorized by the CDC, the U.S. Department of Agriculture (USDA) has developed a list of high consequence livestock pathogens and toxins. Of particular interest is the large number of agents that appear on both the CDC bioterrorism list and the USDA list and the fact that most of these agents are zoonotic.
When one considers a terrorist attack, one tends to expect the targeting of people, not animals or plants. The attack on plants and animals evokes less emotion than an attack on humans would, resulting in there being less likelihood of retaliation. An attack on a crop or herd may go undetected for many days, or even weeks, allowing the perpetrator ample time to escape. The use of pathogens also carries with it the ability of a terrorist organization to deny involvement and point toward natural circumstances.
Clues generated by the outbreak of an animal disease might point toward an intentional introduction. These clues might include: trace back of animals yielding a dead-end with no evidence of exposure to other infected animals or common feed; animals that have not passed through a common sale barn or farm; the occurrence of several, smaller outbreaks at different locations at one time; the manifestation of signs not typically seen with a particular disease that suggest an atypical route of exposure; overwhelming mortality; or unusual season of occurrence. These taken separately might not alert the investigator to agroterrorism, but the combination of two or three, plus other history or suspicions, might be all that is needed to make the connection.
Any species of economic importance can be a target for an agroterrorism event. High concentration of animals (feedlots, swine confinement units, poultry houses) could aid in the distribution of an agent. Auction markets mix animals which are then loaded and transported, sometimes over long distances where they are mixed with other animals. Another concern is a centralized feed supply. As feed can be an ideal vehicle in which to distribute an agent or compound, one feed manufacturer can supply hundreds or thousands of farms, unknowingly distributing an infectious disease agent throughout a country. Free trade leave borders open, making many countries vulnerable to agents or contaminated equipment being smuggled in. Another concern is the lack of bio-security on the farm.
Bio-security entails the efforts and measures employed in keeping out unwanted microbial agents and in minimizing the spread and risk of disease agents to livestock, crops, and food supplies. Bio-security can be applied to a farm, a county, a state, and a country. One key component and concern in agricultural bio-security is the movement of animals, plants, people, and food. Bio-security entails limiting access of visitors and wildlife, making visitors wear clean boots and leaving them on the premises, disinfecting boots and supplies brought onto a farm, wearing clean coveralls and removing them before leaving the farm, and keeping workers or visitors free from contact with livestock outside of the farm for a given length of time before returning. Bio-security also means restricting the movement of vehicles such as feed trucks, as well as personal vehicles, to defined areas on the premises. Quarantining new animals is very important to high quality bio-security. Finally, there is also a great need to improve animal disease awareness and education among public health professionals, producers and the general public. We all must be able to recognize the signs and know how to report them in order to decrease our vulnerability to the spread of these infectious diseases.
Summary
• Bioterrorism and agroterrorism are threats that must be taken seriously.
• Many bioterrorism and agroterrorism agents and diseases are zoonotic.
• Awareness is an important component of preparedness and protection.
• Public health and agricultural security programs and infrastructure must be strengthened.
• Prevention, recognition and response involve everyone and medical professionals from around the world must play a critical role in prevention through awareness and preparedness.
Acknowledgment
I acknowledge the valuable contributions of the faculty and staff of Iowa State University’s Center for Food Security and Public Health (Drs Glenda Dvorak, Gayle Brown, Radford Davis and Danelle Bickett-Weddle) for much of the material used in the preparation of this lecture. Under a grant from the U.S. Centers for Disease Control and Prevention, Iowa State University has developed an outreach and training program for veterinarians and other health care professionals. I have benefited greatly from the excellent training and materials they have provided.
References:
- Huxsoll D, Patrick W, Parrott C. Veterinary services in biological disasters. JAVMA 1987; 190: 714-722.
Noah, D. Biological terrorism against animals and humans: a brief review and primer for action. JAVMA 2002; 221: 40-43.
- Davis, RG. Agroterrorism: Need for awareness. In: Scanes C, ed. Perspectives in world food and agriculture: 2003. Ames, IA: ISU Press, 2003
- Chemical and Biological Terrorism: Research and Development to Improve Civilian Medical Response. The Institute of Medicine, National Research Council, National Academies Press, Washington, DC, 1999.
- Chalk, P., Hitting Americas Soft Underbelly: The Potential Threat of Deliberate Biological Attacks Against the U.S. Agriculture and Food Industry. The National Defense Research Institute, Rand Corporation Press, Washington, DC, 2004
- Countering Agricultural Bioterrorism. The National Research Council, National Academies Press. Washington, DC. 2003
- USDA Outlook Report, Nov 25, 2003 http://usda.mannlib.cornell.edu/reports/erssor/trade/aes-bb/2003/aes40.pdf
- USDA-APHIS website www.aphis.usda.gov; OIE website www.oie.int
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