Oxford Textbook of Public Health
Frank Sorvillo, James R. Greenwood, and Roger Detels
Potential for bioterrorism
Elements of preparedness
Law enforcement and public health—forging new partnerships
Enhancing public health surveillance and laboratory capabilities
Informing the public
Modelling potential threats
Addressing the underlying causes of bioterrorism
The terrorist attacks against targets in the United States, including the World Trade Center and the Pentagon, on 11 September 2001, coupled with the subsequent intentional dispersal of anthrax spores through mailed envelopes in New York, Florida, and Washington, DC (CDC 2001a) focused renewed attention on the potential for biological organisms to be used as agents of war and weapons of terror. Bioterrorism has important public health implications and, unlike other acts of terrorism, it will be public health professionals who will serve as frontline ‘first responders’ to a bioterrorist act (Bryan and Fields 2000). This chapter is not meant to be an exhaustive treatise on bioterrorism but rather an overview of the issue from the critical perspective of public health.
Bioterrorism is the intentional use of micro-organisms, or their products, to cause harm, and may be used to target humans, animals or crops. There are several characteristics of biological agents that may make them appealing to terrorists (Table 1) (Hughes 1999). Biological weapons are relatively inexpensive compared with conventional, chemical, and nuclear weapons. Many biological agents are readily available in nature, from laboratories, or through the numerous microbiological repositories throughout the world. Some organisms, particularly bacteria and parasites, are relatively easy to make or acquire in quantity. Bioweapons occupy little space and are easily concealed. They have delayed effects, requiring hours to weeks to manifest symptoms, which allows a perpetrator to escape undetected. Bioweapons, if prepared and disseminated effectively, can cause widespread and serious illness and exact a significant economic toll. Finally, biological agents have the capacity to cause widespread fear and panic.
Table 1 Characteristics of candidate biological agents for use by bioterrorists
While apprehension about bioterrorism has accelerated recently, the use of bioweapons is not a new phenomenon, and concern about bioterrorism had been heightened for several years preceding the terrorist attacks on the United States in the autumn of 2001 (Henderson 1999). Despite the often repeated refrain that ‘It is not a question of if biological weapons will be used but when they will be used’, bioweapons have been employed repeatedly by nations, groups, and individuals over the course of history (Table 2) (Phills et al. 1972; Harris 1994; Karlen 1995; Torok et al. 1997; CBW Chronicle 1999; Henderson et al. 1999). The catapulting of plague corpses over the walls of Kaffa in 1346 (Karlen 1995) and the transfer of blankets from smallpox victims to Native Americans by British troops in the United States (Henderson et al. 1999) are often cited as early examples of biowarfare. It is generally accepted that the Japanese military used bioweapons in occupied Manchuria in the 1930s and early 1940s (Harris 1994). These activities allegedly employed such agents as plague, anthrax, cholera, typhoid, and typhus against prisoners of war and the Chinese population. Testimony to the Truth and Reconciliation Commission in South Africa has indicated that biological agents, including those causing anthrax and cholera, were used against anti-apartheid forces (CBW Chronicle 1999). More recently, in the United States in 1984, the Rajneeshee cult, in an effort to influence local elections, contaminated salad bars in several restaurants in Wasco County, Oregon, with Salmonella typhimurium (Torok et al. 1997). This act resulted in 751 confirmed or presumptive cases. Ascaris suum, a roundworm of pigs, was used intentionally to infect four university students in Toronto, Canada, in 1971 who required hospitalization after consuming a meal that had been deliberately contaminated with a massive dose of eggs (Phills et al. 1972). Other acts of bioterrorism have been well documented (Tucker 1999). However, it is conceivable, and perhaps likely, that additional bioterrorist attacks, both successful and unsuccessful, have gone unrecognized and undetected.
Table 2 Examples of bioterrorist attacksa
Potential for bioterrorism
Nearly every human microbial pathogen has the potential to be used as a bioweapon. However, the list of potential agents can be narrowed on such criteria as historical use, development by nations with extensive bioweapons programmes, availability of the agent, ease of preparation, dispersal requirements, and capacity for causing widespread and serious illness. The more sophisticated the terrorist or group, the greater the list of possible agents. The United States’ Centers for Disease Control and Prevention (CDC) has classified potential bioterrorism agents into three priority categories, labelled A, B, and C (Table 3) (CDC 2000). Included in Category A are pathogens with the potential for high mortality, ready dissemination or transmission from person to person, and the capacity to cause public panic. Category B includes those agents or products that are moderately easy to disseminate and can cause moderate levels of morbidity but low mortality. Category C lists those emerging pathogens that could possibly be used as bioweapons because of availability, relative ease of production, and the potential for high morbidity and mortality. Detailed information on specific agents is available from a variety of sources.
Table 3 US Centers for Disease Control and Prevention categorization of potential bioweapons
Many potential bioterrorism agents (e.g. Yersinia pestis, Bacillus anthracis, Salmonella species) can be readily acquired in nature, through laboratories, or by ordering from microbiological repositories. Alternatively, it may be possible for a terrorist organization to obtain a bioweapon product from a state-sponsored biological weapons programme either directly or from someone who may have access to the agents. In general, viral agents (e.g. Ebola virus) are more difficult to acquire and may require special laboratory capabilities that are beyond the capacity of most terrorist organizations. All of the known successful historical users of bioweapons have employed bacterial or parasitic agents. In nation-sponsored biological weapons programmes, agent-screening procedures to evaluate such factors as virulence and environmental stability are pursued prior to large-scale production (Alibek 1999). Such screening efforts are probably outside the capability of most existing terrorist groups.
In addition to naturally occurring biological agents there is the potential, through genetic engineering, to create new microbes that may be resistant to antibiotics and current vaccines, possess increased virulence, and demonstrate improved environmental stability. Russian scientists reportedly engineered a strain of Bacillus anthracis resistant to the tetracycline and penicillin classes of antibiotics (Stepanov et al. 1996). Recent bioengineering of the mousepox virus resulted in the production of a highly virulent strain (Norazmi 2001).
Once an agent is acquired, it must then be produced in sufficient quantity, and maintained in a viable state, to be effectively disseminated. In general, bacterial agents are easier to culture than viral pathogens which require living cells, either tissue culture or live animals, in which to grow. Many bacterial organisms (e.g. Bacillus anthracis) can grow on a variety of readily available culture media (Inglesby et al. 1999). Transmissible stages of parasitic agents cannot be cultured and must be obtained from infected animals. Manufacturing pathogenic organisms presents a risk to those producing them, and sufficient expertise and appropriate laboratory equipment is necessary to avoid laboratory-acquired infection.
A biological weapon can be disseminated by several different methods, including aerosols (airborne), water, food, injection, infected vectors, and, as recent events have demonstrated, mailed envelopes. Release of an infectious micro-organism through the airborne route is the method of greatest concern since it has the potential to expose large numbers of people and has the capacity to induce more severe disease manifestations (Franz et al. 1999). A bioweapon aerosol is likely to be invisible and odorless, and therefore undetectable when released. However, aerosol transmission is difficult and necessitates overcoming a number of technical obstacles. Effective airborne dissemination requires that the preparation be of very small particle size. In order to remain suspended in air and to be respired deep into the respiratory tract, the product must be less than 5 µm in size. Moreover, even if a preparation can be created in the required size, it must then be effectively dispersed. Such dispersal requires a device capable of dispensing sufficient product into the air in a manner that will expose the targeted population. Aum Shinrikyo, the Japanese cult that perpetrated the sarin gas attack in the Tokyo subway system in 1995, attempted to release anthrax spores and botulinim toxin via aerosols on several occasions but failed each time (Olsen 1999). The fact that this terrorist group, despite significant financial resources and the successful recruitment of Ph.D. level scientists and engineers as members, could not disperse bioweapons through the airborne route demonstrates the difficulty of such dissemination. Nevertheless, some nations have developed sophisticated bioweapons programmes that have included effective aerosol delivery capability (Alibek 1999).
Waterborne transmission is another possible mechanism of dispersal. However, most infectious agents would be inactivated or removed by the disinfection and filtration techniques employed by most municipal water systems (Khan et al. 2001). Consequently, such a method of dispersal would probably be limited to small water systems or sources.
Most of the successful bioterrorist events recognized to date have used food as a vehicle of dissemination, and, in all likelihood, foodborne transmission will remain the primary method of delivery. While it is possible for a contaminated food product to affect large numbers of people (Hennessy et al. 1996), most of the more virulent potential biological agents (e.g. smallpox virus, Yersinia pestis) cannot be effectively transmitted through foods. In addition, thorough heating will inactivate most agents or toxins and a contaminated food product is likely to be implicated rapidly in any large-scale epidemic.
The recent anthrax attacks on the east coast of the United States have demonstrated that mailed packages, such as envelopes, can be used as a method of dissemination. However, anthrax is the only significant agent with sufficient environmental stability to allow dispersal in such a fashion. Moreover, despite the occurrence of 18 cases and five deaths, the American anthrax cases had relatively limited casualties, and, coupled with existing data, this demonstates the relative inefficiency of such a method of dispersal.
Dissemination of a bioweapon via injection or through the use of vectors has limited utility.
The capacity of infectious agents to cause significant morbidity and mortality should not be underestimated. Infectious diseases remain the most important cause of mortality globally, accounting for an estimated 17 million deaths annually (Hinman 1998). Major infectious disease epidemics continue to occur even in industrialized countries. An outbreak of cryptosporidiosis in Milwaukee, Wisconsin, in 1993, linked to contaminated municipal water, affected an estimated 400 000 residents of the city (MacKenzie et al. 1994), and a multistate epidemic of salmonellosis caused by contaminated ice cream resulted in an estimated 250 000 cases in 1994 (Hennessy et al. 1996). Clearly, there exists the potential for a bioterrorist act to have considerable impact. However, while it is impossible to predict the nature and extent of future acts of bioterrorism, past events would suggest that such acts perpetrated by individuals or groups are likely to remain sporadic and result in limited outbreaks. Nevertheless, either a state-sponsored biological weapons attack or a bioweapon release by terrorist groups who have overcome the significant obstacles that currently exist, however implausible such an event may be, could inflict major casualties that might stretch or overload public health and medical capabilities. An estimate by a World Health Organization expert committee suggested that an aerosol release of 50 kg of anthrax spores upwind of a population of five million would infect 250 000 people with an estimated 100 000 deaths (WHO 1970; Alibek 1999). An attack of this extent is well beyond the scope of individuals or terrorist groups and could only be perpetrated by a nation with a sophisticated bioweapons programme. Such extreme scenarios, while improbable, nevertheless provide a sense of the potential magnitude of an intentional release of a bioweapon and its capacity to cause casualties. Depending on the agent employed, even a modest bioterrorist event would require rapid determination of persons at risk, effective distribution of appropriate prophylaxis, including antibiotics or vaccine when indicated, possible isolation and quarantine measures, co-ordination of medical support, and identification of sufficient hospital capacity.
While the biological impact of a bioterrorist event alone may be considerable, the use of infectious agents has the capacity to cause significant fear to the point of panic (DiGiovanni 1999; Holloway et al. 1999). The idea of being attacked by something invisible can induce considerable and, in some, uncontrollable anxiety. Such panic by the ‘worried well’ has the potential to overwhelm existing resources in demands for medical attention and therapeutic agents. Allaying public anxiety in the midst of a bioterrorist attack requires good communication, accurate information, co-ordination of all involved agencies, and a media that that will resist the impulse to sensationalize events.
A bioterrorist event, unlike a conventional, nuclear, or chemical attack, will unfold over time, probably over a period of days to weeks, and will be insidious in nature. Sporadic cases may occur over a wide geographic area and initially appear to be unrelated. The first to recognize and respond to such an occurrence will not be the traditional first responders but rather the medical and public health communities.
Elements of preparedness
Law enforcement and public health—forging new partnerships
Since the recent mail-related anthrax bioterrorism events in the United States, it has become increasingly clear that any response to bioterrorism, and consequently any preparedness effort, needs to be multifaceted and include organizations not traditionally related to public health disease control efforts. Public health and general law enforcement agencies now have a substantial area of overlap, particularly in the area of disease surveillance and the collection and analysis of evidence. Public health workers are not trained to treat infectious disease samples as evidence and have the potential to ‘contaminate’ these samples, from a law enforcement perspective, in the course of a routine investigation. Consequently, with the new possibility of bioterrorism, the larger issue becomes: When does a routine disease control investigation develop into a potential crime scene? Should public health and law enforcement collaborate every time there is an outbreak of a disease that starts with fever, malaise, and cough? It is now necessary to evaluate disease control efforts with this new world view in mind.
Partnerships of law enforcement and public health should be developed at all working levels, not just national and state agencies, but local jurisdictions as well. Inclusion of local public health is necessary because bioterrorist attacks involve biological material and control efforts usually must begin at the local level. Developing working relationships using standardized response protocols should ensure that future collaborative criminal and disease control investigations compliment rather than hinder the efforts of both groups.
Schools of public health also have a role in this new paradigm. Infectious disease epidemiology courses should be revised to include some aspects of law enforcement investigations as part of course offerings.
Enhancing public health surveillance and laboratory capabilities
The early recognition of a bioterrorist event is essential in ensuring effective containment and reduction of casualties (Kaufmann et al. 1997). Given the historically poor record of passive surveillance systems for most infectious diseases (Marier 1977), the rapid detection of a bioterrorist act will require enhanced disease surveillance activities using active surveillance methods. Active surveillance can include such measures as the use of sentinel primary care providers and emergency room physicians, assigning ‘public health liaisons’ to be stationed at selected health-care facilities, establishing collaborations with veterinarians for animal-based surveillance, employment of real-time Internet-based reporting, and conducting targeted surveillance activities during selected events such as political conventions or the Olympic Games. Other possible useful, albeit less timely, measures include accessing pharmaceutical databases and evaluation of medical examiner and mortality data for the occurrence of selected syndromes. Education of and close collaboration with local health-care providers and emergency medical system staff are essential to the success of any augmented surveillance system.
Early detection of bioterrorism also requires development of enhanced laboratory capabilities to ensure rapid diagnosis of bioterrorist agents. One example of this is the CDC multilevel laboratory response network in the United States which includes providing reagents, protocols, and training to local laboratory staff, typically public health laboratories (CDC 2000). Information is Internet-based and the system assigns a hierarchy of laboratories for the diagnosis of specific agents.
The World Health Organization (WHO) established a WHO Office in Lyon, France, in February 2001 to provide training and support of laboratory capabilities to enhance global security. The first group of international laboratory workers was trained in April 2001. The establishment of this office should improve the quality of public health laboratories which are essential for the establishment and continuing operation of effective surveillance programmes in all countries.
Once detected, effective response and mitigation of events requires epidemiological capability to conduct well-designed studies to implicate a source of infection quickly and to determine populations at risk. Such a capacity, which is lacking in many local jurisdictions, is essential to successfully direct implementation of control measures including provision of prophylactic antibiotics and vaccines as needed. Other control efforts may necessitate isolation and quarantine of patients and, to a lesser extent, disinfection and decontamination activities.
Enhancement of the existing public health infrastructure will require a commitment of funds and resources. However, any augmentation of public health systems for the purpose of responding to bioterrorism will have the added benefit of improving the quality of standard surveillance and response activities to naturally occurring infectious diseases.
Training physicians to recognize and treat disease caused by bioterrorist agents
Before the recent bioterrorism attack in the United States, anthrax would not have been part of the differential diagnosis in a 46-year-old urban letter carrier presenting with fever, malaise, cough for 2 days, and the abrupt onset of severe dyspnoea. Now, however, the need for quick and accurate diagnosis of disease caused by bioterrorism agents has become part of the new reality facing physicians. Unfortunately, relatively few physicians have had experience with some of the agents listed earlier in this chapter (e.g. Yersinia pestis, Clostridium botulinum, Coxiella burnetti). Compounding this problem is the realization that many of the initial clinical manifestations of bioterrorism diseases overlap with common illnesses, and clustering of cases, which might raise the index of suspicion, might not occur because of delayed onset from exposure to a bioterrorism event and multiple sources of health care for exposed individuals.
Lack of case recognition is only one part of the problem. Treatment information for many bioterrorism agents is anecdotal at best and incorrect at worst. Many of the present medications and treatment modalities, while now considered standard treatment for many infectious diseases, have never been rigorously evaluated for the majority of bioterrorism agents. This also has obvious implications for the stockpiling of effective antimicrobial agents and vaccines, as will be outlined later in this chapter.
Key to an appropriate medical response is a trained cadre of emergency room physicians and primary care providers. These individuals would often be the first health-care providers to see individuals infected with bioterrorism agents. Consequently, they should be the primary recipients of medical education programmes to prepare them to recognize cases of infectious diseases most likely due to a bioterrorist attack. Although the list of potential agents is rather daunting, training should focus on those agents that most likely would be used and at a minimum should include the diagnosis and treatment of anthrax, smallpox, plague, botulism, tularemia, and the viral haemorrhagic fevers. Secondary training should include hospital infection control staff and ancillary staff. This training should be incorporated into medical center emergency response plans.
Upgrading hospital and quarantine capacities
Most experts in the field of bioterrorism feel that anthrax and/or smallpox would be the most likely agents used by terrorists. Of the two, smallpox has significant ramifications for hospital capacity. Because smallpox is highly contagious and most of the population has little or no immunity, even a small event could rapidly tax hospital capacity for handling infected patients. Infected patients must be confined to rooms with negative pressure and have exhaust air systems that are filtered to prevent the smallpox virus from exiting and then re-entering the air-handling system. Unfortunately, even in large metropolitan areas such as Washington, DC, there are probably less than 100 such isolation rooms available (Henderson 1999). Thus one of the first areas to receive serious review should be the capacity to isolate and treat smallpox-infected patients.
Concomitant with the review of isolation units should be an evaluation of the quarantine capacity in individual health jurisdictions. In addition to considering hospitals for primary quarantine areas, non-hospital sites, such as abandoned schools or old hotels should be considered as potential triage and quarantine locations. Public health quarantine laws and regulations need to be reviewed and updated as necessary so that little ambiguity will exist and restricting the mobility of exposed segments of the population can be implemented rapidly, if indicated. The concept of quarantine for containment of infectious diseases also needs to be reconsidered in the context of the feasibility of restricting movement in a highly mobile population, the nature of the disease threat, including the infectious characteristics of the agent (which may have been modified), the magnitude of the outbreak, and the nature of the outbreak. In conjunction with quarantine, the feasibility of post-exposure vaccination needs to be considered if an effective vaccine to the agent is available and the length of the incubation period is sufficient to permit artificial development of immunity post-exposure. For example, Meltzer et al. (2001) have suggested that a combination of quarantine and post-exposure vaccination is the most effective strategy to control a bioterrorist outbreak due to smallpox.
Another potentially useful tool for assessing capacity has been developed by the American Hospital Association (2001). This document presents a series of self-assessment questions that allow hospital managements to assess their own capacity for dealing with chemical and bioterrorism events. In addition to capacity, other major areas that are evaluated include communications and public affairs, access to care, business continuity plans, pharmaceuticals and equipment, medical treatment procedures, training and personnel, facility management/security, psychiatric services and crisis counselling, and diagnostic capabilities.
Stockpiling vaccines and antibiotics
One of the hallmarks of a good public health response to a man-made or natural disaster is preparedness. As an example, at the individual level, the public health message is for people who live in earthquake country to prepare for a disaster by storing food and water in case these supplies are not available for a few days after a major earthquake. At the community level, preparation might involve developing a disaster response plan and stockpiling supplies and tents to shelter, feed, and house people whose homes have been lost as a result of a disaster. Taken in this light, stockpiling of vaccines and appropriate antibiotics is good public health policy. However, in contrast to a natural disaster, the difficulty is knowing what and how much to stockpile. This is especially true if one is concerned about state-sponsored terrorism. For example, an announcement that ciprofloxacin is being stockpiled could lead a terrorist organization to develop ciprofloxacin-resistant strains, or at least to announce that they had done so in an attempt to further terrorize a population. Although it might be prudent not to publicize the details of what is being stockpiled, this is not feasible in an open society where the circle of those who need to know would be quite wide. Having sufficient antibiotics and vaccines on hand to control or limit outbreaks while calming the public is consistent with good public health policy.
Informing the public
The recent anthrax events in the United States have demonstrated how important it is for the public health community to provide accurate and timely information to the general public and news media about bioterrorism events. It was clear during the initial stages of the 2001 anthrax incidents in the United States that, in the absence of a strong, clear, and consistent message from the public health community, the news media and other less credible sources were eager to fill the information void. This resulted in inappropriate usage of antibiotics by large segments of the population who were not at risk of exposure to anthrax and the purchase of useless ‘gas masks’ to prevent anthrax inhalation.
The conflicting messages initially delivered by government health officials also undermined the confidence of the public and led to further feelings of insecurity. Therefore, to avoid confusion if there are more bioterrorism events, the public health community needs to develop ‘consensus papers’ on each of the potential agents that might be used. This information should be developed in a non-crisis mode and then distributed to state and local health departments and the media for use as specific situations develop. Part of this process should also be ongoing evaluation of treatment and prophylaxis for these agents. This information could then be sent to the local health-care community when necessary.
The mail system has now been shown to provide a method for the delivery of anthrax spores. While it is not possible at this point to determine how efficient this mechanism is, there is no doubt that anthrax in letters has been responsible for widespread concern about the threat of anthrax and other forms of bioterrorism by the population of the United States. Based on the biology of most bioterrorism agents, it is extremely unlikely that the majority of them could be transmitted through contaminated letters. Bacillus anthracis, because it is a spore former, may be one of the few bioterrorism agents that has the potential to be transmitted through the mail.
The CDC has developed guidelines (CDC 2001b) to prevent the possible exposure of mail handlers to bioterrorism agents. Recommendations include the use of vinyl gloves when handling mail, particulate respirators (which would be difficult to implement), and other methods of avoiding contact with airborne particles. Longer-term disease control solutions have focused on the irradiation of mail to inactivate infectious materials that might be present within packages and letters.
There is no question that exposed air intakes make major buildings vulnerable to the deliberate introduction of biological and chemical agents. However, from a practical standpoint, most buildings do not have secured entries and the introduction of bioterrorism and chemical agents through the air-handling system is not the only way to contaminate a building that uses recirculated air. Consequently, the cost of any major alterations in air intakes, such as securing their location or raising ducts above ground level to avoid easy access to openings, needs to be balanced against potential threats to a building and its occupants versus other security provisions for limiting access. An alternative approach is to develop very efficient and affordable air-filtration systems capable of removing spores and biological agents.
One potentially promising approach for protecting higher-risk buildings or other essential facilities is the continuous air-sampling device. As envisaged, the quality of air entering or circulating within a building would be continuously tested for the presence of biological and chemical agents. If detected, the sensors would then be programmed to shut off intake air supplies or internal fan systems. To date these systems have had difficulty discriminating between dust particles and biological agents, but at some point technological advances should obviate this difficulty.
Water supplies to major cities and towns in the industrialized world are generally considered to be safe and secure from being used as a mechanism for the mass distribution of infectious agents. Because public health has had a historical role in developing drinking water that is free from infectious agents, treatment and monitoring systems are already in place to prevent such an occurrence. Most surface water supplies are presumed to be contaminated with infectious agents (e.g. Cryptosporidium or giardia) and are extensively filtered and chlorinated before water is distributed to individual users.
Preformed toxins, such as botulinum toxin, have been discussed as potential bioterrorism agents which could be distributed through a water system. However, because of the massive dilution of most metropolitan water supply systems, it is unlikely that sufficient quantities of toxin could be added to cause harm after dilution and treatment effects are taken into account. However, there is certainly a possibility that a determined terrorist could contaminate a small segment of a water-supply system by deliberately introducing infectious agents downstream from a water-treatment facility or by contaminating water to an individual building or group of buildings served by a single water main. In this case, if the attack were covert, it would be necessary for public health disease surveillance programmes to determine that an attack had taken place after non-deliberate modes of infection had been eliminated.
Food supplies are vulnerable to bioterrorism at multiple levels. The first of these is at the basic farm or production level where it is known that disease agents have been developed into weapons to infect growing crops and food animal production. Both the United States and the Soviet Union developed and experimented with smuts, rusts, and animal pathogens such as Burkholderia mallei, the causative agent of glanders in cattle (Alibek 1998; Carus 1998). It was the intention of these programmes to starve potential enemies and shift resources away from the production of military hardware to food. Delivery of such agents over a large area in the industrialized world, while possible, is still unlikely unless it is related to state-sponsored terrorism. Consequently, bioterrorism at the food-production level, if it is to take place at all, will more likely be limited to events designed to disrupt commerce and terrorize the population, rather than starving a military target.
Governmental surveillance systems and quarantine mechanisms are presently in place to monitor crop and animal health and to prevent the transportation of contaminated products. Many of these systems, especially as they relate to animal diseases, have recently been strengthened in many areas of the world in response to outbreaks of foot-and-mouth disease occurring in the late 1990s. However, it is obvious that these systems should now be re-evaluated to determine if they have the potential to detect and control the deliberate introduction of crop and animal diseases.
The next level of potential vulnerability in the food-supply system is related to modern commerce and the mass distribution of food. Multiple outbreaks (Tucker 1999) have demonstrated that foods contaminated with Salmonella or E. coli 0157, for example, can be widely distributed throughout a large geographical area by centralized food commissaries or other commercial food distribution networks. Thus it is entirely possible that food products at the commercial distribution level could be used deliberately to spread disease and cause terror among a population. Several obstacles prevent food at this level from becoming a major source of disease transmission. Multiple sources of similar foods are available to consumers and many of them are only distributed within local or regional areas. Thus it would be next to impossible to contaminate an entire regional milk supply. Also, many of the pathogens that could conceivably be used to contaminate foods are already considered to be part of the ‘normal flora’ of raw foods. Since these foods are cooked before they are consumed, the addition of more Salmonella to chicken or raw meat, for example, would be of little consequence. Nonetheless, many cases could be caused this way. Thus distribution procedures should be reviewed and strategies to protect against terrorist introductions of agents considered.
Detection of food-related bioterrorism events will require increased co-ordination between local, state, and federal regulatory and public health agencies. More active surveillance systems need to be developed and used to replace traditional passive reporting systems. Most importantly, public health will be required to adopt a new mindset in which the potential of terrorism will be one additional factor considered in any food-related disease outbreak.
Modelling potential threats
One of the major problems which the world must confront is the absence of knowledge. The pathogenicity and virulence of the naturally occurring potential organisms which would be used for bioterrorism are known, but these agents may be altered for use as a bioterrorist agent. For example, Russian scientists were able to develop anthrax strains that were resistant to penicillin and tetracycline and to increase the virulence of mousepox (Stepanov et al. 1996; Norazmi 2001). Further, their impact is dependent, in part, on the susceptibility of the population which depends on the prior exposure of the population to the organism, migration of susceptibles, and the proportion of individuals who have been immunized if, indeed, a vaccine exists for the particular organism. For example, some of the population who were alive prior to the eradication of smallpox in 1977 may have been vaccinated. But, in the absence of subsequent challenges to boost the level of artificial immunity, it is not know what proportion of even this population is immune. Those born since eradication will have no immunity to smallpox and the majority of the population will not have immunity to other potential bioterrorist agents.
A second problem is that several countries, and perhaps individuals, have conducted research to alter the basic properties of the agents to make them more pathogenic/virulent and to improve their potential for widespread transmission. An example of this is the attempt to reduce the size and electrostatic properties of the anthrax preparation to increase its ability to be aerosolized, thus enhancing its ability to infect a large number of individuals, especially in crowded congested situations such as a major subway station. Aerosolization of anthrax from letters has already been demonstrated in the bioterrorist episodes in Miami, Washington, DC, Connecticut, and New York in 2001, and involved transmission of spores at levels sufficient to cause infection of individuals who never came into direct contact with the originally infected letter, although relatively few cases occurred.
Given the variability of strains, the meteorological conditions existing when agents would be released (e.g. wind, temperature, and light conditions), the range of potential transporting media (e.g., water, air, food), the availability of treatment and vaccines, and the susceptibility of the population, how can responsible national and international agencies anticipate the magnitude of the threat and thus respond effectively? One approach is to model the potential episodes. Mathematical modelling has been used for a variety of infectious diseases, including estimates of the future of the HIV/AIDS epidemics in many countries and the impact of smallpox epidemics (see Chapter 6.14). Meltzer et al. (2001), from the CDC, developed a model to estimate the attack rate for smallpox following the deliberate release of the virus in a crowded situation. Not only were they able to estimate the number of secondary and subsequent cases that would occur, but they were also able to evaluate the relative contributions of a rapid vaccination response and quarantine on reducing the spread of the virus. The fact that the infectiousness of smallpox has already been established helped them in the development of their model. However, the relative infectiousness of many of the other potential bioterrorist agents, including those that have been altered, is not known. In this situation mathematical modelling can still be useful. Multiple models can be developed using different levels of infectiousness and different scenarios. The use of multiple models often reveals key determinants of rapid transmission.
Development of complex models is limited by the quality of the assumptions which may be incomplete or invalid. Moreover, it is difficult for any mathematical model to accommodate every possible contingency. Thus model predictions must be interpreted cautiously. Nonetheless, models can provide valuable information about the potential behaviour of agents in populations. The use of mathematical models can assist national and international agencies to prepare for potential bioterrorist episodes in the future. Although their accuracy will be difficult to evaluate in the absence of a real episode, the early stages of an episode will provide validation (or no validation) of each of the models which have been developed, providing an opportunity to select the most appropriate model.
Addressing the underlying causes of bioterrorism
When faced with a bioterrorist threat the tendency, even by governments, is to concentrate on the problem at hand and to ignore the underlying causes of bioterrorism. Yet, if we are to reduce the threat of bioterrorism effectively we must address its underlying causes. Terrorism may be the result of national policy, religious or political convictions, or a sense of unchangeable economic inequities, but may also be caused by a sense of alienation by a single individual. Perhaps a common thread among all these groups is the feeling of being disenfranchised by society. The terrorists feel that their only recourse when outnumbered and shunned by society is to engage in activities which can be implemented by only a few dedicated individuals but which will have a large impact. Examples include the Palestinians in Israel, the Catholics in Northern Ireland, and the al-Q’aida Muslims in Afghanistan. This perception on the part of nations, religious and political groups, and individuals may be due to psychological factors, political policies, economic disparities, and/or ‘fanaticism’. However, fanaticism may also be the expression of or response to the feeling of being disenfranchised. Of course, there may well be other root causes of bioterrorism, as yet unknown, but which must be understood if we are to address the issue successfully.
The immediate response among individual victims, groups, and nations suffering the consequences of bioterrorism is usually to seek immediate revenge. But if bioterrorism is to be reduced it is also essential to step back from the immediacy of the problem to consider the underlying causes and how to address them. Addressing these root causes provides the best promise of a lasting strategy to reduce bioterrorism. Thus it is important, even in the midst of the terror and confusion caused by a bioterrorist incident, to study and identify the causes of the act by the nation, group, or individual perpetrating it. If we know the causes, we can attempt to address them and thereby reduce the likelihood of future incidents. It is important to realize that making the necessary changes may not be easy or popular, but it is the responsibility of national and international leaders to understand what needs to be done and to convince the public of the need.
The effort to prevent the threat of bioterrorism must be international. The threat of bioterrorism is not confined to one country. Bioterrorist attempts have been made in many countries, including the United States, Iran, and Japan. Although some bioterrorists act within their own country, others implement their activities in other countries. As observed by Horton (2001), terrorism is a consequence of wider political and social change and thrives in those countries undergoing state failure such as Afghanistan, Colombia, Northern Ireland, Sudan, and Iraq. But the activities are often directed at other countries. Thus international co-operation is essential to prevent these international bioterrorist activities. Further, a combined approach by many nations is more likely to be successful than uncoordinated attempts by individual countries. Joint antiterrorism efforts must include sharing of intelligence, co-ordinated diplomatic and financial pressures when indicated, close co-operation between national health authorities, including heightened surveillance for the rapid identification and communication of possible bioterrorist acts, and efforts to prevent terrorist groups acquiring biological agents from the numerous microbiological repositories and laboratories throughout the world.
The WHO publishes the Weekly Epidemiologic Record which reports disease outbreaks in member states. In order to upgrade the quality of the reports, the WHO has developed a manual for recommended surveillance standards in the field of communicable diseases. The WHO Recommended Surveillance Standards manual (WHO 1999) includes recommendations for diagnostic methods, case definitions, types of surveillance, minimum data elements, data analysis methods, principal uses of data for decision-making, and standardization of reporting and international data exchange based on the International Classification of Disease (10th revision) codes.
The Weekly Epidemiologic Record will be very helpful for identifying outbreaks of disease which may be caused by bioterrorism, but the utility of the system will depend on the quality of the surveillance in the various countries, the speed of reporting the outbreak, the honesty of the countries in both reporting the disease and providing an accurate estimate of the magnitude of the outbreak, and the ability of WHO to respond appropriately.
The member states of the United Nations recognized this need several decades ago by establishing a new instrument in 1972 to supplement the 1925 Geneva Protocol, the ‘Convention on the Prohibition of the Development, Production and Stockpiling of Bacteriological (Biological) and Toxin Weapons and on their Destruction’ (BWC) (United Nations 2001). Unfortunately, the absence of any formal verification protocol to monitor compliance severely limited its effectiveness. Recognizing this shortcoming, a group of governmental experts (VEREX) was established at the Third Review Conference of the BWC to identify and examine potential verification measures from a scientific and technical standpoint. Despite subsequent Review Conferences in 1996 and 2001, a system of verification that is acceptable to the signees has yet to be adopted by the signees (United Nations 2001).
The events of the latter half of 2001 have brought into sharper focus the need to adopt an international protocol which incorporates an effective verification strategy. At least equally important, however, is the need to address the underlying causes of bioterrorism. Thus an effort has to be made by the nations of the world to act together to reduce the feeling of alienation and disenfranchisement felt by some countries, especially smaller developing nations, and by groups both within individual countries and spanning many countries. It is clear that attempts of individual nations, even large powerful nations such as the United States, acting independently of other nations will fail. Thus the nations of the world must co-operate if the threat of bioterrorism is to be reduced and ultimately controlled. A united and co-ordinated antiterrorist strategy by the nations of the world may discourage rogue nations, groups, and individuals against using bioterrorism to achieve their goals.
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