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Suggested Citation:"4 Bioterrorism and the Food Supply." Institute of Medicine. 2006. Addressing Foodborne Threats to Health: Policies, Practices, and Global Coordination: Workshop Summary. Washington, DC: The National Academies Press. doi: 10.17226/11745.
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4
Bioterrorism and the Food Supply

OVERVIEW

Each of the three papers collected in this chapter address a different aspect of a single, highly publicized scenario for foodborne terrorism: the intentional contamination of the U.S. milk supply with botulinum toxin, as described in a May 2005 New York Times op-ed essay by Lawrence Wein (Wein, 2005). The article sparked an intense debate about the possible security risk it posed, a controversy that was fueled in subsequent weeks by the delayed publication of a peerreviewed paper by Wein and a coauthor (Wein and Liu, 2005) in the Proceedings of the National Academy of Sciences (Alberts, 2005).

These concerns are expressed in the first part of this chapter by Clay Detlefsen of the International Dairy Foods Association. “Disclosure of information that can be used to harm people needs to be limited except when necessary,” he argues, extending the definition of “harm” to include the needless scaring of consumers who might stop buying milk. Indeed, Detlefsen asserts, the dairy industry has been aware for years of the threats described by Wein and has been working with the U.S. government to safeguard its operations and products from bioterrorism. To prevent such efforts from being undermined by the release of sensitive information to potential terrorists and other malefactors, Detlefsen supports the creation of a vetting system as a means to fairly assess and, when appropriate, prohibit the publication of scientific findings that could be used to develop and launch an attack.

As workshop contributor Milton Leitenberg notes in the second contribution to this chapter, considerably less attention has been paid to the questionable va-

Suggested Citation:"4 Bioterrorism and the Food Supply." Institute of Medicine. 2006. Addressing Foodborne Threats to Health: Policies, Practices, and Global Coordination: Workshop Summary. Washington, DC: The National Academies Press. doi: 10.17226/11745.
×

lidity of Wein’s conclusion that milk represents “a uniquely valuable medium for a terrorist” than to its status as a threat to national security. Leitenberg, a senior research scholar at the University of Maryland’s Center for International Security Studies at Maryland (CISSM), offers detailed evidence that contradicts key assumptions upon which Wein based his model, most notably the ease by which terrorists could obtain botulinum toxin and use it to launch an attack. More generally, Leitenberg notes that several existing historical reviews of agricultural terrorism contain inaccuracies that serve to inflate the number of instances of actual attacks. As a result, he concludes, U.S. policy has been influenced by “gross exaggeration surrounding the potential for bioterrorism.”

Using the controversy over the Wein model as a jumping-off point, Dr. David Acheson, Director of the Food and Drug Administration (FDA) Office of Food Safety, Defense, and Outreach within the Center for Food Safety and Applied Nutrition, outlines the FDA’s multifaceted approach to protecting the U.S. food supply from attack in this chapter’s final paper. Acheson explains how the agency uses risk management and vulnerability assessment tools to determine which food/ agent combinations present the greatest threats to U.S. biosecurity, and in particular how these analyses have raised concerns about the potential consequences of the deliberate contamination of milk with botulinum toxin. He then describes how the FDA addresses such findings through the development of guidance documents and training programs to prevent and mitigate the effects of specific bioterrorism threats.

THE THREAT AGAINST MILK: JUST ONE OF MANY, WITH MORE TO COME

Clay Detlefsen, M.B.A., Esq.1

International Dairy Foods Association

After September 11, 2001, leaders in this country vowed that we would never be caught off guard again and began an extensive process by which every imaginable terrorist threat scenario is analyzed. The laudatory goal is to identify reasonable mitigation strategies for any threats within the realm of possibility of being perpetrated. More than four years later, that effort is continuing and expanding. Today, virtually every industry is working with the government to harden itself against a potential terrorist attack. The food industries are no exception, and the dairy industry, in particular, has been quite active and proactive.

I have worked with the government and various industries on food-specific scenarios involving terrorism, and I have participated in government and industry

1

Vice President for Regulatory Affairs.

Suggested Citation:"4 Bioterrorism and the Food Supply." Institute of Medicine. 2006. Addressing Foodborne Threats to Health: Policies, Practices, and Global Coordination: Workshop Summary. Washington, DC: The National Academies Press. doi: 10.17226/11745.
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exercises to plan for chemical and biological terrorist attacks that had little to do with the food supply. Further, I have brainstormed with government officials as to the private-sector response to a nuclear attack on U.S. soil. Due to the sensitive nature of the exercises and discussions, most of these activities take place with little fanfare or public acknowledgment. In some cases, participants such as myself are required to sign nondisclosure agreements. The bottom line is that the federal, state, and local government agencies and the private sector are working closely together to enhance the public’s safety. Being discrete about it is par for the course when dealing with a public safety or national security issue.

Secrecy or discretion is called for in these matters for fundamental reasons. For instance, the general public can scare easily and may then needlessly avoid the subject matter of the concern. This was exemplified by the dramatic downturn in commercial airline travel after 9-11, which lasted, as indicated in Figure 4-1 below, until nearly January 2004.

With respect to food, the 1980s, Alar/apple scare clearly establishes how consumers react when confronted with any implication that a food might present a risk or contain a deleterious substance. This is so even when the risk is only theoretical or otherwise unproven. As author Michael Fumento noted:

FIGURE 4-1 U.S. domestic airline passengers. These graphs present both actual data, and data that have been seasonally adjusted in order to clarify the trends over time. The data cited in the text represent actual (unadjusted) values.

SOURCE: Bureau of Transportation Statistics (2005).

Suggested Citation:"4 Bioterrorism and the Food Supply." Institute of Medicine. 2006. Addressing Foodborne Threats to Health: Policies, Practices, and Global Coordination: Workshop Summary. Washington, DC: The National Academies Press. doi: 10.17226/11745.
×

Nothing makes Greens—radical environmentalists—turn an angry red faster than invoking the word Alar to epitomize bogus environmental scares and imply that a current one is equally phony.

Manufactured by Uniroyal Chemical Co., Alar was commonly sprayed on apples to keep them on trees longer so that fewer would fall and rot before being harvested. The attack on it began in February 1989 when 60 Minutes reporter Ed Bradley called it “the most potent cancer-causing agent in our food supply.”

Bradley’s main source was the Natural Resources Defense Council (NRDC), which had decided to scapegoat a single substance to illustrate the horrors of all manmade chemicals. The NRDC had retained a radical environmentalist public relations firm, Fenton Communications, to create a front group called Mothers and Others for Pesticide Limits and place horrifying articles in newspapers and women’s magazines.

The result: Terrified mothers threw out their applesauce, poured out their apple juice, and swore off apples entirely for “healthier foods” such as Twinkies. Apple farmers across the nation suffered, and some went bankrupt. Subsequently, articles, monographs, and books peeled the wraps off one of the slickest, most cynical fear campaigns in recent American history (Fumento, 1999).

Although the harm in the above case is significant, it is largely one of economics and is overshadowed by a more significant type of harm—harm that results from a deliberate attack on people and loss of human lives. Disclosure of information that can be used to harm people needs to be limited except where necessary. Too often, the wrong people get their bad ideas from disclosures. The National Academies and many others in the scientific community are aware of the “dual use” problem of attempting to advance science while at the same time running the risk of assisting and aiding terrorists. Unfortunately, the debate seems to end with a statement along the lines “there is nothing new here that terrorists don’t already know, so there is no harm in publishing this article.” But, a “terrorist” needs to be thought of in a broader way—not just what would traditionally be thought of as a terrorist; but potentially our own misguided or mentally ill citizens, as well. Virtually every law enforcement agency in the nation is aware of, or concerned about, copycat criminal activity. The issue has been debated and discussed on a regular basis for decades. In recent years, a protracted period of carjacking was theorized to have escalated because of media attention:

Carjacking has always been around, especially in large metropolitan cities, we just rarely read about it. The crime of carjacking “took off” in the 1980s after the media published stories of bizarre situations and the violence associated with the crime. The media coined the phrase “carjacking,” and the crime of auto theft took on a new identity. After a rush of publicity, other criminals “copied” the crime of carjacking. These copycat criminals must have said, “Hey, I can steal any vehicle I want without damaging it, I get the car keys, and I can rob the owner too. What a concept!” (McGoey, 2006).

Suggested Citation:"4 Bioterrorism and the Food Supply." Institute of Medicine. 2006. Addressing Foodborne Threats to Health: Policies, Practices, and Global Coordination: Workshop Summary. Washington, DC: The National Academies Press. doi: 10.17226/11745.
×

In more recent times, carjacking has largely disappeared and the occurrence of a multitude of Columbine-like school shootings have been theorized to have stemmed from the media attention given to that unfortunate event. A Google internet search of the words copycat and Columbine yields 44,000 hits, which is a fairly clear indication that some association exists. Further, the mimicking of notorious events is by no means limited to our own domestic criminals. As Florida State University professor Cecil Greek noted in his paper on censorship, the issue is complex and may potentially link to terrorism:

Ray Surette has done extensive research on copycat crimes since the mid-1980s. He argues that copycat crime is a persistent social phenomenon, common enough to influence the total crime picture, but mainly by influencing crime techniques rather than the motivation to commit a crime or the development of criminal tendencies. A copycat criminal is likely to be a career criminal involved in property offenses rather than a first-time violent offender. The specific relationship between media coverage and the commission of copycat crime is currently unknown, and the social context factors influencing copycat crimes have not been identified….

Surette also noted that copycat crimes … seemed to fall into at least four groupings with some overlap. “Mode” copiers were those who already intended to commit a crime and who received a method from the media event. For example, a potential car thief copies the techniques seen on a television police drama for breaking into and hot-wiring a car. “Group” copiers were those who copied acts in groups. In 1995, a group of Tampa, Florida, teens bragged to police they stole cars and shot at robbery victims because earlier in the same week a 12-year-old repeat robber had been granted probation rather than prison. The case had been given major media attention. The other two categories were mentally ill or mentally deficient copiers, and terrorists. Since terrorism is partially driven by media attention, it is not surprising that terrorists choose to repeat methods that have produced high media ratings in the past. This has led concerned media executives to consider carefully how much attention they focus on terrorist acts (Greek, 1997).

Last summer, the dairy industry found itself in the middle of a media flurry over a paper that paints a terrorist scenario about botulinum toxin in milk. The paper, by Dr. Lawrence Wein of Stanford University, described a scenario by which terrorists could poison thousands of people through the U.S. milk supply (Wein and Liu, 2005). Wein’s paper was initially withheld at the government’s request over fears that it could aid attackers; later, the National Academy of Sciences (NAS) published the paper, insisting that it did not put any new information before terrorists.

Coverage of this issue was widespread, including features in the New York Times, USA Today, the Washington Post, and on major television networks. The story ultimately appeared around the globe in more than 500 newspapers. Today,

Suggested Citation:"4 Bioterrorism and the Food Supply." Institute of Medicine. 2006. Addressing Foodborne Threats to Health: Policies, Practices, and Global Coordination: Workshop Summary. Washington, DC: The National Academies Press. doi: 10.17226/11745.
×

a Google search of the Internet using the search of the combined words Wein and milk yields 282,000 hits.

Unbeknownst to most though, the scenario was neither novel nor new. In fact, the industry had been working with the FDA for several years after the FDA brought the matter to industry’s attention in 2002. Long before that, the government had theorized about this particular scenario being perpetrated by communists. As early as the mid 1950s government scientists studied the possibility that a variety of beverages, including milk, could be contaminated with botulinum toxin. The report’s conclusion was that the threat to the milk supply was negligible because of the nullifying effects of pasteurization on the toxin. In fact, the report concluded that 99 percent of any toxin would be inactivated by pasteurization. This inactivation finding is not consistent with information obtained by Wein that indicated the temperature and time required for inactivation would be much greater. However, the research cited by Wein explored inactivation of toxin in creamed corn, tomato soup, tomato juice, string beans, and canned corn (Woodburn et al., 1979). The research did not include research using milk. The research of the 1950s and more recently conducted research did utilize milk, and those studies are consistent with each other. In fairness to Wein, neither of those studies are publicly available. Curiously, one of the researchers in the 1950s project is one of the researchers of a study cited by Wein.

In addition, what you did not see in the newspaper or on TV were the efforts the dairy industry made behind the scenes to correct the misperceptions we feared the Wein paper might raise, and—more broadly—the extensive work that has already been done to address security issues.

We knew that the Wein paper was flawed in the assumptions it made about the milk supply and about milk processing—I and others pointed those flaws out to Wein himself, who has admitted to shortcomings in his own research. Close scrutiny by a seasoned biosecurity expert—Milton Leitenberg—found that there is “an extraordinary degree of uncertainty associated with Wein’s estimates,” finding flaws with everything from his mathematical methodology to his assumptions on the production of the necessary toxin.

Moreover, pasteurization steps have been taken within processing plants that substantially eliminate the threat Wein presents. Although Wein was successful in publishing his paper, the International Dairy Foods Association (IDFA) and others have been successful in delivering the facts to government officials—many of whom we have built relationships with since the events of 9-11.

To be clear, the dairy industry welcomes scientific research that is aimed at helping our nation secure its vital systems, including the food supply. But the Wein paper does not fall into that category—and it remains a lesson on how important it is for researchers and security experts to work together with industry in assessing possible terrorist threats.

One area where cooperation is working well is in communication between industry and government. An impressive amount of work has been done coopera-

Suggested Citation:"4 Bioterrorism and the Food Supply." Institute of Medicine. 2006. Addressing Foodborne Threats to Health: Policies, Practices, and Global Coordination: Workshop Summary. Washington, DC: The National Academies Press. doi: 10.17226/11745.
×

tively on security since 9-11. I work closely with officials at the U.S. Department of Homeland Security (DHS), the FDA, the U.S. Department of Agriculture (USDA) and other federal and state government agencies on a daily basis to help evaluate situations and further safeguard the dairy industry. Other individuals in other sectors and industries fill similar roles.

A thorough government analysis of possible threats to the food and dairy supply was completed fairly soon after 9-11. Based on that analysis, the dairy industry has worked diligently, without fanfare, to implement a wide range of measures to secure facilities and the milk supply. For example, based on guidelines prepared by the National Milk Producers Federation and the IDFA, dairy farmers and processors have implemented new standards for sealing milk tankers. Using these new protocols, any unauthorized opening of a tanker before its delivery to a processing plant is immediately evident.

In addition, producers and processors have taken many proactive steps to increase awareness among employees about security measures at the farm and in processing facilities, including increased security of milk storage areas. Dairy plants have secured entry systems and employee screening programs, and have restricted access on the plant floor. And, of course, most packaging operations are already automated, enclosed, and secure.

There is always more we can do as an industry to be vigilant—and we encourage dairy facilities to make every reasonable effort along these lines. But it is also important to realize we have done quite a lot. I expect new challenges to continually emerge between government and industry on security issues. We will never be “done” when it comes to protecting our most valuable attribute—the safety of our products. The good news is that we have good working relationships and valuable new protocols in place.

Our efforts, though, should not be undermined by inappropriate publication of sensitive material that has a potential to be used by foreign or domestic terrorists or criminals. Instead, the scientific community needs to work collaboratively with industry and the government, and this may at times require self-censorship or restraint. The downside of not being cognizant or otherwise ignoring the possibility of harm being perpetrated on the U.S. citizenry can be the loss of human lives, which is clearly unacceptable. We are aware of the scientific community’s interest in addressing this important concern, as was recently described by Dr. Brian Gorman in his Yale journal article:

The open science dilemma has been recognized as a top priority in the scientific and national security communities since the terrorist attacks of 2001. It is undisputed that the fruits of scientific advancements may also be subject to harmful “dual use” by enemy combatants, terrorists, and any number of other malefactors with the necessary skills and resources. The dilemma over open science arises from the incompatibility of restricting access to scientific findings in the interests of public welfare with a notion of public welfare that is itself reliant upon the open exchange of findings and scientific data. Therefore, great care is

Suggested Citation:"4 Bioterrorism and the Food Supply." Institute of Medicine. 2006. Addressing Foodborne Threats to Health: Policies, Practices, and Global Coordination: Workshop Summary. Washington, DC: The National Academies Press. doi: 10.17226/11745.
×

needed to avoid remedies that unnecessarily impede the exchange of information between researchers and deter important lines of inquiry. Thus, a carefully crafted remedy is needed to cease “free ride” opportunities available to malefactors interested in misusing scientific advancements without impeding much needed advancements in science interests.

Surprisingly, the most draconian and potentially deleterious remedies to the open science dilemma, to date, come from the scientific community. As of January 2003, over 20 scientific journals adopted a policy calling for the censorship of articles that present unjustifiable risks (Journal Editors and Authors Group, 2003).2 However, many recognize that censorship is not a guarantee of protection. In October 2002, the former president of the American Society for Microbiology (ASM) warned that, “censorship of scientific communication would provide a false sense of protection” (Greenberg, 2002). Severe measures are of concern because, if carried out, they may discourage research in areas critical to biodefense efforts. Moreover, even if applied sparingly, censorship policies are destined to undermine academic freedom and compromise national security interests.

Unfortunately, there has been little discourse in the literature on specific methods to effectively remedy the problem. While the dilemma clearly calls for “an articulated and uniform practice” to identify and assess sensitive research, efforts to create formal procedures have been abandoned (Cozzarelli, 2003). For example, the journal Proceedings of the National Academy of Sciences, which published a sensitive article on the variola virus (Rosengard et al., 2002), abandoned its pursuit for uniform procedures after a self-congratulatory assessment of its ad hoc handling of the article (Cozzarelli, 2003). Despite satisfaction with the “natural” manner in which the article was vetted, flaws remain in the allegedly successful approach. For instance, the national security community was not consulted during a review of the article (Gorman, 2005).

Ultimately, Gorman describes a proposal to pursue a strategy for the creation of a due process vetting system (DPVS). Gorman has clearly given considerable thought to the problem and has proposed a complex, though fair and workable process:

2

On February 20, 2003, Nature published an editorial entitled “Statement on the consideration of biodefense and biosecurity” Nature 421(6925):771. The editorial described a one-day workshop at the National Academy of Sciences that was attended by representatives of editorial boards, societies (including ASM), and a select group of investigators. The workshop culminated in adoption of four statements pertaining to review and publication of manuscripts that might contain information that could be harmful in the context of bioterrorism. The fourth statement is as follows: “We recognize that on occasions an editor may conclude that the potential harm of publication outweighs the potential social benefits. Under such circumstances, the paper should be modified, or not be published.”

Suggested Citation:"4 Bioterrorism and the Food Supply." Institute of Medicine. 2006. Addressing Foodborne Threats to Health: Policies, Practices, and Global Coordination: Workshop Summary. Washington, DC: The National Academies Press. doi: 10.17226/11745.
×

The DPVS is a comprehensive system that enables immediate and informed communication between the scientific and national security communities on new research in line for publication and public release. The rapid communication on potentially sensitive research enables immediate cooperative vetting of flagged articles between the scientific community and the relevant government authority. The DPVS also provides temporary safe harbor for sensitive research by consensus rather than unilateral classification imposed by the government. In the rare occasion when the government needs to classify a research article absent consensus, the government will have notice of the article before it reaches the presses and the scientific community will have ample opportunity to be heard through a fair hearing on the matter if desired. As previously stated, for the purposes of this discussion, the administrative board charged with federal authority will be deemed a new federal agency called the Biologic Regulatory Commission (BRC)….

The stakes in this debate could not be higher. The potential showdown between the scientific community and the government on open science, absent goodwill and cooperation, would certainly yield a duel of mutual destruction.

If scientific journals can cooperate by accommodating the parameters of articles in LRC [Least Restrictive Classification] status, and if professional stakeholders agree on fair scaling procedures and joint vetting, the entire field of science can move forward in a safe and efficient manner. The DPVS could provide a superior alternative to the ASM model and ad hoc approaches undertaken by the majority of U.S. bioscience journals. But, the DPVS is just a proposal, and is by no means seen as a comprehensive solution to the debate on open science. It is hoped that the flaws and virtues of this proposal will help inspire a fair and comprehensive approach to sensitive and dual use science that will accommodate the needs of all of the stakeholders in this debate (Gorman, 2005).

Industry and government will continue to work together and we will, as we have in the past, involve the scientific community. It would be foolhardy to think we could cover our security bases without the scientific community. For the sake of the public’s safety, we will conduct our activities discretely and cautiously. We have already achieved considerable success with our endeavors and will undoubtedly achieve much more. It is hoped issues involving freedom of the press and censorship will not undermine the efforts that are so vital to the nation’s security and the public’s safety. I encourage readers in the scientific community not to overlook the dangers associated with our own domestic malefactors, and to, at the very least, read Gorman’s paper and consider that as a starting point. No one should ever be put in a position to regret their decision to publish after human lives were lost as a result of such a publication. A robust and systematic approach as outlined by Gorman could obviate such an occurrence.

Suggested Citation:"4 Bioterrorism and the Food Supply." Institute of Medicine. 2006. Addressing Foodborne Threats to Health: Policies, Practices, and Global Coordination: Workshop Summary. Washington, DC: The National Academies Press. doi: 10.17226/11745.
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BOTULINUM TOXIN: THE LINKAGE WITH BIOTERRORISM

Milton Leitenberg, M.S.3

University of Maryland

My task was to prepare a paper that brought three subjects together: the traditional biological weapons agent, botulinum toxin; its possible use by bioterrorists; and its dispersion by application to food as the mechanism of such use.

The very opening lines of the guidance document for this conference read as follows:

In December 2004, at a press conference called to announce his departure as Secretary of the Department of Health and Human Services, Tommy Thompson raised both concern and controversy when he remarked that he could not understand why terrorists had not yet attacked our food supply “because it is so easy to do” (Branigin et al., 2004).4

Secretary Thompson’s comment is a useful introduction to this paper. In contrast to the expectation that it suggests, one realizes immediately that in the entire period since 1945 there have been only two instances in which any individual or group deliberately added a pathogen or a toxin to the U.S. food supply. The more significant of these was the event in 1984 in The Dalles, Oregon, in which a prepared culture of Salmonella was placed on food in a salad bar, resulting in 751 recorded cases of illness (Carus, 2000).5 Many more people were probably affected, although there was no record of mortality.

In November 2000, Dr. William Fry, a plant pathologist at Cornell University, and an expert on potato late blight in particular (Phytophthora infestans), the fungus that caused the historic potato famine in Ireland in 1845–1848, gave an excellent presentation at a conference titled “Agro-Terrorism: What Is the Threat.” His assignment for the conference was “Think Like a Terrorist,” and he enjoined the conference attendees to do so. Yet his own detailed and thorough presentation repeatedly emphasized the difficulties in producing an artificially caused outbreak of potato blight, to the point of often frustrating the efforts of

3

Senior Fellow, Center for International and Security Studies at Maryland.

4

The original statement continued with the added words: “...and the fact that the United States imports a lot of food products form the Middle East.”

5

It is pertinent to note that the purpose of the Rajneesh use of the biological agent was not “terrorist”: It was done covertly and intended to remain covert, and its purpose was a trial run to test its subsequent use intended to cause large-scale public absenteeism from a local election.In his presentation to the Forum on Microbial Threats, Dr. Robert Tauxe noted that in 20 years there had been 20,000 outbreaks of disease due to food contamination, only two of which were caused by a deliberate act. The second event was the incident in which a laboratory worker in Texas placed Shigella into baked goods, which she gave to her colleagues. The organism was obtained from the laboratory in which she worked.

Suggested Citation:"4 Bioterrorism and the Food Supply." Institute of Medicine. 2006. Addressing Foodborne Threats to Health: Policies, Practices, and Global Coordination: Workshop Summary. Washington, DC: The National Academies Press. doi: 10.17226/11745.
×

academic researchers when they sought to do so for purposes of their research. He concluded that:

Devastating crop loss caused by anticrop terrorism is certainly within the realm of possibility, but there are many obstacles to successful implementation. While there are many examples of terrible crop destructions by plant pests, the manipulation of these agents as biological warfare agents to destroy crops on a wide scale by terrorist states or groups faces severe technical challenges. Even if an aggressive plant pathogen can be developed or found, its potential is severely limited by meteorological conditions. Thus, it is difficult to conceive that a biological warfare agent could be used “at will” by a terrorist group or even by a state (Fry, 2003).6

But perhaps even more to the point was that while he urged his audience to “think like a terrorist,” and many members of the academic and contract analytical community quickly identified ways they thought terrorists could make use of plants or animal pathogens, no real-world terrorist organization had ever done so.

Another guide, in a similar vein to Secretary Thompson’s remark, was to be found in the opening line of a report by the Congressional Research Service in August 2004, stating that “The potential of terrorist attacks against agricultural targets (agroterrorism) is increasingly recognized as a national security threat, especially after the events of September 11, 2001” (Congressional Research Service, 2004).7 At first thought, the statement seems logical: after 9-11, civil authorities looked at every sector of the nation’s infrastructure to identify vulnerabilities and points of access by which terrorists could wreck havoc or destruction or injure the public. Nevertheless, the statement is a non sequitur: nothing in the events of 9-11 suggested that any terrorist group intended to attack U.S. agricultural targets or had even considered doing so. The purpose of this study, however, is not to suggest another particular vulnerability. It is rather to attempt a classical threat assessment: an identification and evaluation of real-world entities, their parameters, performance, experiences, and capabilities as regards the potential for terrorist use of botulinum toxin.

Before doing that it would be useful to examine the more general subject of agroterrorism because it serves as an example of what quickly became evident as a major problem in the course of this work. Two tables dealing with historical

6

The last sentence in the quotation implicitly refers to plant pathogens only.

7

Other reports on agroterrorism that might be of use for the reader are:• Parker HS. 2002. Agricultural Bioterrorism: A Federal Strategy to Meet the Threat. McNair Paper 65. Washington, D.C.: Institute for National Strategic Studies, National Defense University.• GAO (Government Accountability Office). 2005. Homeland Security: Much Is Being Done to Protect Agriculture from a Terrorist Attack, but Important Challenges Remain. GAO-05-214. Washington, D.C.• GAO. 1999. Food Safety: Agencies Should Further Test Plans for Responding to Deliberate Contamination. GAO-RCED-00-3. Washington, D.C.

Suggested Citation:"4 Bioterrorism and the Food Supply." Institute of Medicine. 2006. Addressing Foodborne Threats to Health: Policies, Practices, and Global Coordination: Workshop Summary. Washington, DC: The National Academies Press. doi: 10.17226/11745.
×

aspects of agroterrorism prepared by the Center for Nonproliferation Studies of the Monterey Institute of International Studies are posted on their Web site. Both the center and the institute are well known, and their work would ordinarily be considered authoritative and of the highest quality. The first table is titled “Chronology of CBW Attacks Targeting Crops and Livestock 1915–2000” (CNS, 2001). It lists 18 events for the 85-year period. As the title of the table states, all 18 are characterized as “attacks.” However, an examination of the 18 entries demonstrates the following:

  • Three were false allegations;

  • Three others were “threats,” and as best as is known, more accurately described, they were bluffs;

  • One was an incident in which one man killed his neighbor’s animals;

  • One was unsubstantiated (Alabama);

  • One was a very low-scale “economic” event (Wisconsin);

  • Two, both in Israel, were low-scale economic sabotage that could perhaps qualify as “attacks”; and

  • One, the U.S. use of a herbicide in the DMZ (demilitarized zone) separating North and South Korea, was done for the purpose of impeding infiltration of North Korean military and security personnel into South Korea. It did not target “crops and livestock” at all.

In sum, 11 or 12 of the 18 events in the table—two-thirds of the entries—are not what they claim to be. They are not “attacks.” At a minimum, the title for the table should have read “Attacks, Incidents, False Allegations, and Bluffs.”

The second table is titled “Agricultural Bio-warfare: State Programs to Develop Offensive Capabilities” (CNS, 2000). It lists programs for 13 states. The entries for 8 of them need corrections of varying degree:

  • Egypt: The claim that Egypt has a dedicated antianimal biological weapons (BW) program is based on a paper that is unreliable and unsubstantiated. The Israeli author, Daniel Shoham, essentially listed any pathogen for which an Egyptian journal publication existed. If the same criterion were applied to Israel, the list of the pathogens would be five times longer than for Egypt. Nevertheless, Israel does not appear in the table at all, even though it maintains an extensive anthrax research program, for example.

  • Iraq: Anthrax in the Iraqi BW program was for antihuman purposes, not for use against animals. Studies on camel pox served as a research simulant for smallpox. Finally, contrary to the entry in the table, there was no evidence ever found by the UN Special Commission (UNSCOM), UN Monitoring, Verification, and Inspection Commission (UNMOVIC), or the U.S. postwar Iraq Survey Group to indicate that work on foot-and-mouth disease was ever part of the Iraqi BW program.

Suggested Citation:"4 Bioterrorism and the Food Supply." Institute of Medicine. 2006. Addressing Foodborne Threats to Health: Policies, Practices, and Global Coordination: Workshop Summary. Washington, DC: The National Academies Press. doi: 10.17226/11745.
×
  • Rhodesia: Regarding the allegation of anthrax use in 1979 during the civil war, the outbreak was almost certainly of natural origin, not due to government action.

  • South Africa: The anthrax produced was added to food and cigarettes to produce intestinal or pulmonary anthrax in people; there is no evidence that it was ever intended for or used against animals.

  • USSR (Russia, Kazakhstan, Uzbekistan): The facilities and the activities in what became those countries belonged to the Soviet-era BW program. There is no presumption that BW-relevant work continued in them once the two new states became independent in 1992, although the facilities continued to exist. Neither Kazakhstan nor Uzbekistan was an independent entity at the time of the USSR, so there is no justification for listing them.

  • North Korea: If North Korea has an offensive BW program, and if that program includes anthrax, it would in all likelihood be intended for antihuman use.

  • Syria: The source given is one of the large survey studies by Cordesman; it would have to be checked to evaluate the validity of Cordesman’s source.

  • UK: The year in which the offensive BW program was terminated is known.

Of the entries for 13 countries, 3 are totally incorrect, 5 others include varying degrees of inaccuracy, and only 5 can stand as the original entries were written.

Literature References to the Production of Botulinum Toxin by Terrorist Groups

References exist for the production of botulinum toxin by two terrorist groups. The first of these was the Red Army Faction, another name of the West German Baader-Meinhof Group.

A laboratory in a safe house of the Red Army Faction in Paris, France, was found to have made quantities of botulinum toxin; it is believed that none was used (Caudle, 1997).8

Allegedly, an Erlenmeyer flask containing the substance had been found in an apartment bathtub. The source for this claim, which allegedly had taken place in 1980, was given as Brad Roberts, Weapons of the Future? (Roberts, 1993). The German intelligence agency Bundesnachrichtendienst (BND) had always—privately—said that the story was apocryphal, that is, it was untrue. Nevertheless, numerous U.S. analysts and some U.S. government officials persisted in claiming

8

Douglas and Livingstone, and Kupperman, citing access to classified U.S. government sources, would frequently state the allegation as fact in various seminars in the Washington, D.C., area in the late 1980s and early 1990s.

Suggested Citation:"4 Bioterrorism and the Food Supply." Institute of Medicine. 2006. Addressing Foodborne Threats to Health: Policies, Practices, and Global Coordination: Workshop Summary. Washington, DC: The National Academies Press. doi: 10.17226/11745.
×

for two decades that this “event” had occurred. The claim was finally laid to rest in the book edited by Jonathan Tucker in 2000 (Taylor and Trevan, 2000).

The extensive briefing materials prepared in advance of the workshop included two published papers that referred to the production of botulinum toxin by the Japanese Aum Shinrikyo organization or by other unidentified “terrorist” groups. The first was by Sobel, Khan, and Swerdlow, who wrote in The Lancet in 2002, “Aum Shinrikyo … reportedly had produced stocks of botulinum toxin and other biological agents” (Sobel et al., 2002). Their source for this statement was the chapter by Kadlec, Zelicoff, and Vrtis in Joshua Lederberg’s 1999 book, Biological Weapons, Limiting the Threat (Kadlec et al., 1999). The source for these authors was in turn Kaplan and Marshall’s 1996 book on the Aum, which is inaccurate in virtually all its discussion of the Aum’s work on biological agents, except that such work was carried out and that numerous attempts were made by the group to distribute whatever “products” they had made (Kaplan and Marshall, 1996).

The crucial point is that all the biological materials produced by the Aum Shinrikyo group were innocuous, nonpathogenic, and nontoxic. The Aum produced no “stocks” of botulinum toxin. At first it appeared that either they had obtained a strain that produced no toxin, or that they had not succeeded in producing the toxin due to incompetence. It now appears certain that they never obtained a strain of Clostridium botulinum at all. This will be discussed further below. The Aum produced no “other biological agents,” specifically anthrax, because they only had the Sterne vaccine strain of anthrax, and in addition they did not work with it properly. The Aum had no other biological agents of any kind. By the end of 1999—and therefore certainly by 2002—three publications were available that explained the above as well as additional inaccuracies that by then had appeared in print in every reference to the Aum and BW and which continue to appear in print to this day.9

9

A detailed description of the efforts of the Aum group to produce biological agents became available in 1999 and 2000 in three publications by this author:• Leitenberg M. 1999. Aum Shinrikyo’s efforts to produce biological weapons: A case study in the serial propagation of misinformation. Terrorism and Political Violence (Special Issue on the Future of Terrorism) 11(4):149–158.• Leitenberg M. 2000. The experience of the Japanese Aum Shinrikyo group and biological agents. In: Roberts B, Ed. Hype or Reality: The “New Terrorism” and Mass Casualty Attacks. Alexandria, VA: Chemical and Biological Arms Control Institute.• Leitenberg M. 2000. Aum Shinrikyo’s efforts to produce biological weapons: A case study in the serial propagation of misinformation. In: Taylor M, Horgan J, Eds. The Future of Terrorism. London: Frank Cass.

Suggested Citation:"4 Bioterrorism and the Food Supply." Institute of Medicine. 2006. Addressing Foodborne Threats to Health: Policies, Practices, and Global Coordination: Workshop Summary. Washington, DC: The National Academies Press. doi: 10.17226/11745.
×

The second paper was by Arnon et al. in the Journal of the American Medical Association (JAMA) in 2001:

Terrorists have already attempted to use botulinum toxins as a bioweapon … by the Japanese cult Aum Shinrikyo. These attacks failed, apparently because of faulty microbiological technique, deficient aerosol generating equipment, or internal sabotage. The perpetrators obtained their C. botulinum from soil that they collected in northern Japan….

Four of the countries listed by the U.S. government as “state sponsors of terrorism” (Iran, Iraq, North Korea, and Syria) have developed, or are believed to be developing, botulinum toxin as a weapon (Arnon, 2001).10

Here, there are several important points to be made. In the statement on the Aum group, both sources used by the authors are not reliable regarding the information that they contain about the Aum and BW. As will be explained below, it appears that the Aum did not succeed in isolating C. botulinum from soil or obtaining it in any other way. As regards the other countries, except for Iraq, the U.S. government does not claim to know which specific BW agents the identified countries produced in the past or may be developing (Leitenberg, 1996, 2004). The Russian intelligence agency Federal’naya Sluzhba Bezopasnosti 1993 report, the only publicly available source that could be considered authoritative, does not list botulinum toxin among the four BW agents that it claimed North Korea was working with (Federal’naya Sluzhba Bezopasnosti, 1993). Finally, official U.S. government statements consider it highly unlikely that BW or chemical weapons (CW) would be included in state assistance to terrorist groups. It has never happened to date despite four decades of state assistance to terrorist groups by states which do, or may, possess both BW and CW capabilities and which have assisted terrorist groups in every other conceivable manner (Leitenberg, 2004). That includes funding, sanctuary, training, arms, explosives, embassy support, false documents, and other forms of assistance.

A third publication by Roger Shapiro of the Centers for Disease Control and Prevention (CDC), also published in the JAMA in 1997, contained the following statements (Shapiro, 1997):

  • “Reports that national governments and terrorist groups have stockpiled botulism toxin.” However, no “terrorist group” is known to have “stockpiled botulism toxin” to date.

  • “As many as 17 countries are suspected of either including or developing biological agents in their offensive weapons program; botulism toxin is frequently

10

The sources given in Arnon et al. for the first quotation are David Kaplan’s chapter in Toxic Terror, which repeats all the errors in his own book, as well as a New York Times article of 1998. The sources for the second quotation are papers by Anthony Cordesman in 1998 and Joseph Bermudez in 2001.

Suggested Citation:"4 Bioterrorism and the Food Supply." Institute of Medicine. 2006. Addressing Foodborne Threats to Health: Policies, Practices, and Global Coordination: Workshop Summary. Washington, DC: The National Academies Press. doi: 10.17226/11745.
×

one of these agents.” According to official U.S. government tallies, the number has never been alleged to exceed 13. As of mid-2005, it had been reduced by 3 or 4, again according to U.S. government statements. Only Iraq is known to have produced and stockpiled botulinum toxin (Leitenberg 2004, 2005).

  • “The Aum Shinrikyo cult in Japan also produced botulism toxin.” The Aum group produced no toxin, and they did not have the organism.

  • “Instructions for the production of botulism toxin have been broadcast on the Internet as well.” Virtually all the “instructions … on the Internet” are useless, excluding professional journal papers that may be available online. This will be discussed further below, and an example provided.

What then was the actual experience of the Aum Shinrikyo group and botulinum toxin, and why has misinformation been propagated for all these years? As early as May 24, 1996, the major Japanese daily newspaper, Asahi Shimbun, reporting on evidence presented by the Japanese prosecutor, wrote:

A group led by Seiichi Endo tried to culture botulinum, but failed in isolating the germ. Then … Hideo Murai installed a big tank in order to make a large-scale production of the germ. After all, the facility was not accomplished to produce germs.

The decision of the Public Security Commission of the Public Security Investigation Agency (Japan), January 31, 1997, stated that “The Aum had failed to isolate Clostridium botulinum.”11 In February 1998, the Chief Toxicologist of Chiba Prefecture, adjacent to Tokyo, told this author that “The group had not been sufficiently competent to succeed [in their effort] to produce biological agents,” a statement that referred to their efforts regarding both botulinum toxin and anthrax (personal communication, Chiba Prefecture, February 1998).12

In anticipation of this workshop, it nevertheless seemed desirable to revisit this question once again and to try to establish as definitive an answer as possible. I therefore sent a series of very explicit and specific questions to a Japanese academic, Masaaki Sugishima, who had examined the full Japanese prosecutorial record in the Aum Shinrikyo court trials. I asked if the Aum group had acquired a pathogenic strain of botulinum toxin by whatever means. All possible alternatives for acquisition of the organism were explicitly enumerated, and if it had been obtained, whether the group had been able to work with the organism to the point of obtaining the toxin. Box 4-1, below, provides Masaaki Sugishima’s response.

11

The full report of the Public Security Commission, Production of Biological (Bacteriological) Weapons by the Organization, is classified, but the decision is available.

12

Translation provided by a Japanese colleague, Dr. Minoru Ouchi, during the conversation.

Suggested Citation:"4 Bioterrorism and the Food Supply." Institute of Medicine. 2006. Addressing Foodborne Threats to Health: Policies, Practices, and Global Coordination: Workshop Summary. Washington, DC: The National Academies Press. doi: 10.17226/11745.
×

BOX 4-1

Date: 10/18/2005 8:25:54 AM EDT

Dear Milton,

As far as I know, there is NO publicly available information that the Aum had successfully obtained a strain of Clostridium botulinum. You might know, according to the prosecutors’ opening statement at Asahara’s trial (Tokyo District Court, May 23, 1996).

  1. Tomomasa Nakagawa taught Asahara about the toxicity of botulinum toxin.

  2. Asahara asked Sei-ichi Endo to isolate and cultivate Clostridium botulinum.

  3. Endo, together with Kiyohide Hayakawa and Tomomitsu Niimi, went to Hokkaido to collect soil for that purpose.

  4. But Endo FAILED [in] isolating Clostridium botulinum.

In this statement, prosecutors have NEVER said that the Aum had successfully obtained (bought, stolen, etc.) a strain of Clostridium botulinum.

Best regards,

Masaaki Sugishima

School of Law, Asahi University

In a chapter of his own in a book published early in 2006 Sugishima wrote:

Endo attempted to isolate C. botulinum from soil samples collected in Hokkaido, but there is no evidence that he was successful. Where the strain that was ultimately used came from is unknown, as are its identity and toxigenicity. The fact that multiple dissemination events led to no casualties suggests that the Aum was using an avirulent strain or was unable to cultivate C. botulinum properly. Nakagawa told another senior follower that the substance his team produced had proved ineffective in mice (Wheelis and Sugishima, 2006).

The third possibility was more definitively stated above in 1997 by the Japanese Public Security Commission, namely that the group had never isolated any C. botulinum at all. Sugishima adds:

Finally, about a week before the Tokyo sarin incident in 1995, the Aum tried to disseminate botulinum toxin from attaché cases with built-in spray devices. Three such cases were found abandoned at the Kasumigaseki subway station in Tokyo, but nothing harmful was found in them. Endo testified at Asahara’s trial

Suggested Citation:"4 Bioterrorism and the Food Supply." Institute of Medicine. 2006. Addressing Foodborne Threats to Health: Policies, Practices, and Global Coordination: Workshop Summary. Washington, DC: The National Academies Press. doi: 10.17226/11745.
×

that he had been unable to produce botulinum toxin and had filled the devices with harmless liquid (Wheelis and Sugishima, 2006).13

In contrast, the information in Kaplan and Marshall’s book on the Aum Shinrikyo and BW derives from three reports by the Japanese National Police Agency dating from 1995 and 1996. These would appear to be based on early statements made to the police by members of the Aum during interrogation rather than on forensic investigation. These were clearly not reliable. All subsequent references in the Western international media as well as in the scientific literature derive in one way or another from the original Kaplan and Marshall book. The information on the Aum and BW in a lengthy report by the two legal counsels to the U.S. Senate Committee on Governmental Affairs in October 1995 is similarly totally incorrect for the same reason (U.S. Senate Government Affairs Permanent Subcommittee on Investigations, 1995).

Botulinum Toxin: A Brief Description

Botulinum toxin is produced by a gram negative spore-forming anaerobe, Clostridium botulinum. There are seven distinct serotypes, A through H, and roughly 100 or more available isolates for each serotype.14 Many of the isolates produce little or no toxin at all. Only serotypes A, B, E, and F are involved in human poisoning and of these, primarily A. The toxin is a single protein with a molecular weight of around 150,000 that acts presynaptically, blocking the release of acetyl choline, and possibly other neurotransmitters, producing a flaccid paralysis (Middlebrook and Franz, 1997).

During the years of the U.S. offensive biological weapons program stretching from 1943 to 1969, hundreds of isolates of C. botulinum were tested for toxin production. From these, about a dozen were selected for further research. Those

13

Sugishima supplies the following Japanese-language sources for the material quoted in the text, as well as the paragraph below.• Police newly identified Aum’s microbiological laboratory. 1995 (May 5). Yomiuri Shinbun.• Aum’s two scientists were addicted to scientific experiments. 1995 (May 30). Mainichi Shinbun.• Testimony of Endo, January 10, 2005, in Ken-ichi Furihata, Aum Hotei [Court Trials of the Aum], vol. 12, Tokyo: Asahi Shinbun, 2005, P. 292.The Aum Shinrikyo group did not lack for financial resources. When Japanese police finally raided the Aum’s facility for the first time after the release of sarin by the group in the Tokyo subway, they reportedly found “… a glove box, incubator, centrifuge, drier, DNA/RNA synthesizer, electron microscope, two fermenters each having about a 2,000-liter capacity, and an extensive scientific library.” Yet the group was not able to obtain or produce any pathogenic agent, demonstrating the point that although equipment is certainly desirable, the key requirements are a culture and competence.

14

These individual isolates located in various culture collections have at times been referred to as “strains.” However, as genomic identification is not available for nearly all of them, it would be better to refer to them as isolates.

Suggested Citation:"4 Bioterrorism and the Food Supply." Institute of Medicine. 2006. Addressing Foodborne Threats to Health: Policies, Practices, and Global Coordination: Workshop Summary. Washington, DC: The National Academies Press. doi: 10.17226/11745.
×

in turn were reduced to two, one of which was finally selected for production on the basis of its stability of toxin production, yield, and hardiness of the organism under the condition of large-scale culture (personal communication, Dr. William Patrick, 1988). It took many person-years of work to achieve that result. In 1997 at a NATO Advanced Research Workshop in Budapest, Hungary, Dr. Jerzy Mierzykowski, at that time director of the Polish biodefense laboratory at Pulawy, made an unusual appeal to the researchers present. He was about to retire after a lifetime’s work with C. botulinum. Nevertheless, he explained, he was unable to obtain repeatable levels of toxin production. He asked the American and the British scientists present to advise him on how one obtained reproducible toxin production.15 In some months his cultures produced toxin, and in other months they did not. The reason for this is that the structural gene for the toxin appears to vary between chromosomal and extrachromosomal locations in the seven C. botulinum serotypes. Some are located in a plasmid, some in a bacteriophage, and some apparently are chromosomally located.

Botulinum toxin—or the group of botulinal toxins—are frequently referred to as the most toxic substances known, with an LD50 of 1 nanogram per kilo of body weight. Although unrelated to botulinum toxin poisoning via ingestion by food, two of the scientific publications referred to earlier, Arnon et al. (2001) and Shapiro (1997), state that one gram of botulinum toxin if distributed as an aerosol would result in the death of “more than one million people,” and “at least 1.5 million” people, respectively. All such estimates made on the basis of mathematical extrapolations from LD50 values assume perfect distribution. They are many orders of magnitude from possible realization in the real world. In fact both the United States and later the Soviet offensive BW programs discovered that botulinum toxin did not perform well under aerosol distribution, and both programs lost interest in weaponizing the agent.16

Botulinum Toxin Poisoning and the U.S. Milk Supply

On May 25, 2005, the Proceedings of the National Academy of Sciences (PNAS) announced that it would publish a paper that presented a mathematical model of the possible consequences of deliberate botulinum toxin contamination of the U.S. milk supply. The paper was written by Dr. Lawrence Wein of the Stanford University Graduate School of Business, and Yifan Liu, a graduate stu-

15

The author was present and contributed a chapter to the book that resulted from the conference. See Geissler E, et al. 1998. Conversion of Former BTW Facilities. Dordrecht, The Netherlands: Kluwer Academic Publishers.

16

Among other problems, the neurotoxin protein must first cross the air-blood barrier in the lungs and then the blood-brain barrier. Other toxins are more effective when delivered by aerosol because they act directly on cells in the lungs.

Suggested Citation:"4 Bioterrorism and the Food Supply." Institute of Medicine. 2006. Addressing Foodborne Threats to Health: Policies, Practices, and Global Coordination: Workshop Summary. Washington, DC: The National Academies Press. doi: 10.17226/11745.
×

dent. Stewart Simonson, Assistant Secretary for Public Health Emergency Preparedness at the Department of Health and Human Services requested that the paper not be published on the grounds that it served as a “road map for terrorists,” supplied “very detailed information on vulnerability nodes in the cow-to-consumer chain,” and that “publication is not in the interests of the United States” (Carr, 2005a,b).17 PNAS editors agreed to a delay in publication. However, a preprint of the paper had been released in advance to journalists, and it was possible to obtain a copy within a day or two.

On May 30, Wein (alone) published an op-ed in the New York Times titled “Got Toxic Milk.” It presented the conclusions of the unpublished manuscript. This short version included one crucial aspect not contained in the PNAS paper: It stated that “a terrorist, using a 28-page manual called Preparation of Botulinum Toxin that has been published on several jihadist Web sites and buying toxin from an overseas black market laboratory,” could produce “a few grams of botulin” (Wein, 2005). It took a few additional days to obtain a copy of the jihadi manual in question, and to query appropriately informed professional colleagues in Europe as to whether any “overseas black market laboratory”—or overseas black market—for botulinum toxin existed. With these, plus an extensive search of the professional literature dealing with the isolation and purification of botulinum toxin, one was able to try to make sense of the mathematical model in question.18 PNAS duly published the original paper without modification at the end of June 2005 (Wein and Liu, 2005). Comment by the general media as well as editorials and news section reports in journals such as Nature and Science commented only on the fact that publication of the PNAS article had been delayed. None took issue with any aspect of the model itself (Editorial, 2005; Shane, 2005; Weiss, 2005).

Wien’s model postulated that contamination of milk with less than one gram of botulinum toxin would cause 100,000 poisoned individuals, and that mortality could be in the range of 400,000 or 500,000 people—“the great majority of 568,000 consumers”—if 10 grams were used. In early seminar presentations of his model at Stanford University, Wien had even posited that the terrorists could have 1 kilogram or more of the toxin (personal communication). His New York Times article postulated that a single “terrorist” could achieve such levels of toxin production. Some 15 years ago scientists at the Center for Applied Microbiological Research in the United Kingdom had made a few grams of toxin, which served to supply the entire European and U.S. commercial market for a decade. Producing 10 grams—down two orders of magnitude from a kilo—would be a feat for professional scientists.

17

Assistant Secretary Simonson’s letter was sent to the head of the National Academy of Sciences, Dr. Bruce Alberts, on May 27, 2005.

18

Research and part of the writing for this section of the paper were done together with Dr. George Smith. I would also like to thank Dr. Mark Gorwitz and three other anonymous colleagues for assistance in supplying references to relevant literature and other information.

Suggested Citation:"4 Bioterrorism and the Food Supply." Institute of Medicine. 2006. Addressing Foodborne Threats to Health: Policies, Practices, and Global Coordination: Workshop Summary. Washington, DC: The National Academies Press. doi: 10.17226/11745.
×

To begin with, the terrorist or terrorists would have to obtain a good producing strain of C. botulinum. The jihadi manual begins by extraction from soil. The deus ex machina that Wein invoked as an alternative, an “overseas black market lab,” apparently does not exist to anyone’s knowledge. The 25-page jihadi manual that Wein refers to is in fact a good one: it was composed by splicing together the “Methods” sections of several professional scientific papers. However, applying its directions requires a very long list of reagents and equipment, including a walk-in cold room, a refrigerated vacuum centrifuge, a substantial number of highly specialized reagents, a mouse colony (since the testing for various steps in the isolation of the toxin requires repeated in vivo assays), and, not least substantial, technical skill and experience. Without such knowledge, the manual is useless. None of these are likely to be available in any jihadi terrorist camp, and none of them have ever been found to date in any such location. Annex 4-1 contains excerpts from a far more typical jihadi manual concerning botulinum toxin. They provide an indication of what the knowledge base of such a group is more likely to be.

Alternatively, if the terrorist group obtained the services of a competent trained scientist, or if the terrorist himself had such qualifications as well as access to equipment and facilities (as was apparently the case for the individuals who produced the anthrax used in the United States in October and November 2001), then there is no need to invoke a “jihadi manual.” Such an individual would be likely to already have a culture of the organism or to know how to obtain it from nature, know how to produce and purify the toxin, and how to perform the in vivo mouse assays.

Fortuitously, we have the rudiments of a real-world example to measure against. In December 2001, the United States and allied forces overran an al-Qaeda facility in Afghanistan that contained documentary material relating to their program to attempt to produce biological agents. This author obtained the declassification of these materials. They demonstrated that botulinum toxin was one of the agents in which the group was interested (Leitenberg, 2005). A Ph.D.-level Pakistani scientist working in a Pakistani government facility had provided the group with photocopies of papers from the journal literature that Dr. Zawahiri, a senior al-Qaeda official, had requested. However he was not willing to do any laboratory work himself, and as best as is publicly known, he had not provided them with a culture of C. botulinum. In addition to journal papers on anthrax, plague, and hepatitis A, the following were the publications that the group possessed that dealt with botulinum toxin:

  • Roberts TA. 1965. Sporulation of Clostridium botulinum type E in different culture media. Journal of Applied Bacteriology 28(1):142–146.

  • Hobbs C, Roberts TA, Walker PD. 1965. Some observations on OS variants of Clostridium botulinum type E. Journal of Applied Bacteriology 28(1):147–152.

Suggested Citation:"4 Bioterrorism and the Food Supply." Institute of Medicine. 2006. Addressing Foodborne Threats to Health: Policies, Practices, and Global Coordination: Workshop Summary. Washington, DC: The National Academies Press. doi: 10.17226/11745.
×
  • Roberts TA, Ingram M, Skulberg A. 1965. The resistance of Clostridium botulinum type E to heat and radiation. Journal of Applied Bacteriology 28(1): 125–141.

  • A one-page extract of a handbook of gram-positive bacteria, on Clostridium tetani.

  • A four-page extract of a medical or microbiological handbook on Clostridium tetani and Clostridium botulinum.

There was no indication that the group had obtained a culture of C. botulinum from any source, and there was no indication that it had initiated any laboratory work.

If we return to examining Wein’s model, it appears that it was constructed with little knowledge of the relevant literature concerning botulinum toxin. The few sources referenced are of poor quality, inappropriate, or inaccurate. As indicated, the mathematical model is built upon a thin supposition regarding what terrorists can do. Wein starts with the assumption that terrorists can make gram quantities of botulinum toxin. For the PNAS publication, the reasoning for this was delivered in a little over a paragraph and based on three citations. The first is an article published in the Journal of Bacteriology in 1971. Although it deals with the production of botulinum toxin, it more specifically concerns the preliminary characterization of another protein from the microbe that activates the toxin.

The second citation that Wein used to posit terrorist capability was not from another scientific journal at all but, surprisingly, from a short news piece published by the New York Times on April 27, 2003, written by Judith Miller, then embedded with the U.S. Army’s Mobile Exploitation Team Alpha in Iraq. It is a very brief interview with a scientist who worked in Iraq’s bioweapons program, and it delivers one brief and contextually meaningless claim about the degree of toxin concentration achieved in that country’s production of botulinum toxin. It was a simple task to determine that neither UNSCOM, UNMOVIC, nor the Iraq Survey Group inspectors were ever able to verify his statement or find documentary verification for it in any internal Iraqi government report. Even if accurate, the claim could not be expected to reflect an achievement level that a terrorist group might reach. The Iraqi biological weapons program was a national program with access to unlimited resources. Late in 1985, botulinum toxin and anthrax were one of the first two pathogens selected as candidate agents for the Iraqi BW program. Initial production began in 1988, and early in 1989 full-scale production began (United Nations Security Council, 2005). Approximately three full years were thus taken up by Iraqi scientists and technicians in preparatory work, and although UNSCOM inspectors never obtained any of the prepared material to evaluate, they assumed it to have been a relatively crude preparation. Given that this was a state program—in contrast to “a” single terrorist postulated by Wein’s model—it perhaps offers a more realistic estimate of what might be required.

The third citation was used by Wein to bolster an argument for possible

Suggested Citation:"4 Bioterrorism and the Food Supply." Institute of Medicine. 2006. Addressing Foodborne Threats to Health: Policies, Practices, and Global Coordination: Workshop Summary. Washington, DC: The National Academies Press. doi: 10.17226/11745.
×

advanced production methods in the hands of terrorists. It too is not from a scientific publication, but is a reference to a “paper for discussion” attributed to Richard Danzig, a former U.S. Secretary of the Navy, which includes the single sentence saying that there are such advanced methods. Of course there are advanced methods for botulinum toxin production; the question is whether they are within the capabilities of terrorists. Finally, the data point used in the model for toxin survival during thermal processing was out of date, and was for canned corn rather than for milk.

But the most critical assessment of the model results from several lines at the very end of Wein’s PNAS paper:

In closing, it is important to stress that several elements of the model contain enough irreducible uncertainty to preclude estimating the impact of the attack to within several orders of magnitude….

The dose-response curve, pasteurization inactivation rate, and terrorists’ release size capabilities each contain several orders of magnitude of uncertainty…. Taken together, we have reasonably accurate estimate of the number of people who could be poisoned, but a very poor estimate of how much toxin is required to cause a large outbreak (Wein and Liu, 2005).

As it turns out, there apparently is variability of three or more orders of magnitude in each of the three variables. Taken together, this could result in a possible difference of nine orders of magnitude from the numbers presented by Wein. The mortality result could be one billionth of Wein’s estimate. Instead of the predicted mortality of half a million people, there might not have been a single death. By definition, Wein could not have had “a reasonably accurate estimate” if the results could vary anywhere over a range of nine orders of magnitude. The first and last lines in the quotation above are contradictory, and the last lines appear to be internally contradictory. The model builder apparently knew little or nothing of the relevant literature on botulinum toxin and nothing at all about the real-world capabilities of would-be bioterrorists and bioterrorism. Intelligence analysis and mathematical modeling share the same classic limitation: faulty assumptions lead to faulty conclusions. A mountain of mathematics, formulas, and curves cannot remedy flawed basic assumptions and inputs. It is difficult to understand how the PNAS reviewers and editors let this pass. Finally, Wein had given presentations of his model to public groups and government officials in Washington, D.C., long before the manuscript was submitted to PNAS for publication. During both the private and public presentations he had been informed that remedial measures had already been taken by the U.S. milk industry to raise both the temperature and duration of heating during the pasteurization process (personal communication, June 2005). This sharply increased the level of toxin inactivation reached during pasteurization—one of the three variables in question—and concomitantly reduced the amount of inactivated toxin that might remain. Thus one of the two recommendations that Wein suggested at the end of his paper had essentially already been carried out, although not mandated by law.

Suggested Citation:"4 Bioterrorism and the Food Supply." Institute of Medicine. 2006. Addressing Foodborne Threats to Health: Policies, Practices, and Global Coordination: Workshop Summary. Washington, DC: The National Academies Press. doi: 10.17226/11745.
×

Although all of the public discussion surrounding the model concerned issues related to the delay in its publication, the far more germane issue appears to be that the model was wrong. At the same time, the episode served as yet another example of the gross exaggeration surrounding the potential for bioterrorism. The most likely outcome of such exaggeration is to prompt would-be terrorists who might not otherwise consider or pursue the development of biological agents to do so because a fictitious simplicity and a fictitious effectiveness was touted. Documentation captured in Afghanistan demonstrated that precisely that occurred in the case of al-Qaeda. On April 15, 1999, the Egyptian-born physician, Dr. Ayman al Zawahiri, deputy to Osama bin Laden, wrote in a message to one of his colleagues:

We only became aware of them [biological weapons] when the enemy drew our attention to them by repeatedly expressing concerns that they can be produced simply with easily available materials (Leitenberg, 2005).

There was a final coda to the PNAS publication, which ironically also concerns publication restrictions. When PNAS published the Wein-Liu model, it printed an accompanying lengthy commentary by Dr. Bruce Alberts, then the president of the NAS. In it he noted:

The Wein and Liu article has been widely circulated in preprint form, generating a great deal of discussion. For this reason, we are already aware of scientists who plan to publish challenges to some of its conclusions. This type of give-and-take lies at the heart of scientific progress and is precisely why scientific analyses are made available in the open literature (Alberts, 2005).

Alberts’ reference to “scientists who plan to publish challenges” referred specifically to a very brief critique of the Wein model by this author and Dr. George Smith. It had been submitted to PNAS asking if it could be published together with the model. However, Dr. Nicholas Cozzarelli, the PNAS editor, had already rejected that suggestion by June 2, a full six weeks earlier, saying “We do not have a letters to the editor section in our journal for what you propose. You are of course free to send in an article that will be subject to our customary peer review.”19 The catch-22 however was that we did not write a scientific paper, only a brief three-page critique very similar to the material presented here. We then submitted the same critique to the New York Times. The editor who had published the Wein op-ed replied, “Thank you for your submission. As a matter of policy, we do not publish rebuttals on the op-ed page—that is the job of the letters page. I have taken the liberty of forwarding your article to them.”20 We never heard

19

Dr. Nicholas Cozzarelli, Editor, Proceedings of the National Academy of Sciences, e-mail to the author on June 2, 2005.

20

David Shipley, op-ed page editor, New York Times, e-mail to the author, June 8, 2005. Shipley’s statement is factually incorrect, since responses that are functionally “rebuttals” appear relatively frequently on the New York Times op-ed page.

Suggested Citation:"4 Bioterrorism and the Food Supply." Institute of Medicine. 2006. Addressing Foodborne Threats to Health: Policies, Practices, and Global Coordination: Workshop Summary. Washington, DC: The National Academies Press. doi: 10.17226/11745.
×

from the letter editor. Nature had editorialized about the PNAS publication delay, and the Washington Post had also carried an op-ed on the same aspect. The critique was submitted to both. The Washington Post declined to publish it either as an op-ed or as a letter. There was no reply from Nature. Despite Albert’s generous anticipation, no scientific “give and take” ever appeared in print.

Alberts also claimed that when:

NAS and PNAS representatives met with government representatives to discuss their specific concerns about the Wien and Liu article on June 7 … we learned in our discussion with government representatives that a great deal has been done to improve the pasteurization of milk since 9/11 … we appear to be considerably safer from an attack than they [Wein and Liu] have calculated (Alberts, 2005).

Although the NAS officials and PNAS editors professed not to have previously known what nearly everyone acquainted with the model apparently had heard about, they suggested no revisions in the manuscript as a result of their new knowledge, and it was printed exactly as it had been submitted with its original projections.

A Brief Conclusion

The degree of inaccuracy in information published by members of the scientific community regarding the past record and feasibility of bioterrorism by essentially untrained true terrorist organizations is unbelievably bad. That is a situation that the scientific community should consider impermissible. Any scientist that includes information concerning the record of terrorist interest and experience with biological agents in his papers is responsible to apply the same standards for accuracy to such passages as he does in reporting his own research work.

Much of that same information continues to grossly exaggerate, to misinform, and by suggesting the relative ease and feasibility of producing biological weapon agents, provokes interest among potential actors, state and nonstate, to investigate BW, which they might not otherwise have considered. As was indicated, the al-Qaeda experience is a case in point: it was explicitly provoked by the bioterrorism furor in the United States in 1996–1998. It is legitimate to explore vulnerabilities and to improve defenses, but there is no justification for imputing capabilities to real-world terrorists that they do not possess.

A Single Recommendation

The United States has appropriated $30 billion since FY 2002—in four years—towards bioterrorism prevention. Fiscal year 2005 and 2006 expenditure will amount to $12.7 billion. All further funding for “select agent” programs should be cancelled. Future funding should be split between public health programs such as described in the presentation by Dr. Robert Tauxe to the Forum on

Suggested Citation:"4 Bioterrorism and the Food Supply." Institute of Medicine. 2006. Addressing Foodborne Threats to Health: Policies, Practices, and Global Coordination: Workshop Summary. Washington, DC: The National Academies Press. doi: 10.17226/11745.
×

Microbial Threats and to preparations to anticipate an H5N1 pandemic influenza outbreak. The former should include increased earmarked funding for state and county public health agencies to enable them to carry out the specified programs. The latter should include the construction of a National Influenza Vaccine Facility as well as a dedicated national pharmaceutical facility for the production of anti-influenza pharmaceuticals. These two dedicated facilities could be rented to commercial entities in the same way that production facilities for weapon systems were built by the federal government and rented to manufacturers during World War II, and for a very large portion of the post-WWII period. The vaccine facility should be prepared to produce an H5N1 vaccine. In all other years of operation, it could produce the required U.S. quota of influenza vaccine to cover annual needs, so that no shortfalls would continue to occur (annual flu mortality in the United States ranges from 22,000 to more than 80,000) (GAO, 2005a,b). Funds freed up by cancellation of existing and proposed Bioshield legislation for “select agents,” as well as the massive spending on infrastructure targeted to work on the same agents would more than suffice for this purpose.

ANNEX 4-1

The Microbe Clostridium

The word clostridium comes from the Greek word meaning “little spindle.” Among its characteristics is the ease with which it can be obtained. It is widely available in the environment, found in water and in soil, especially in areas fertile with the dung of grass-eating animals.

These microbes can have within them organisms, microbes, or bacteria which have potential in nonideal climatic circumstances. At this stage, they are latent and inactive until they get into the right circumstances. At that point, the walls of the bacteria are shed and they become active as deadly microbes. They are freed of the glucose that creates an acidic substance. They are active in the absence of oxygen (anaerobic).

As mentioned these kinds of poisons are of the Clostridium botulinum type. They are considered among the most destructive poisons because they act immediately on the nervous system and cause the muscles and respiratory organs to fail. These poisons resist fever to an extent, as well as gastric acid. Their effects are similar to food poisoning. The Clostridium microbe multiplies in fresh meat and causes it to rot (the strength of the poison is limited in the presence of heat, which invites the question of how it could survive the heat of an explosion. It might be possible to position the poison somehow away from the heat of the explosion, and transfer the poison onto, for example, legs or shoes in the case of a suicide operation). There may also be a way to specially design something to spit the poison out of the exhaust pipe of a car as an alternative to an aerosol.

Suggested Citation:"4 Bioterrorism and the Food Supply." Institute of Medicine. 2006. Addressing Foodborne Threats to Health: Policies, Practices, and Global Coordination: Workshop Summary. Washington, DC: The National Academies Press. doi: 10.17226/11745.
×

Clostridium Bacteria

The bacteria of this microbe is killed in the presence of dry heat above 120 degrees Celsius. Its poison emerges from the cell into the environment. It might work to capture these contents on some of the plants on which the bacteria grows. It might be possible to obtain a lot of the poison available in the cell, after it has been released. These poisons have a protein nature such that they lose their poisonous quality if they are exposed to acid (in spite of the fact that they can stand up to gastric acid) or to heat. This microbe is rarely transmitted on tissue, living or dead, but it can be grown inside some cans of food, discharging its lethal poisons. These poisons can lose their effectiveness in temperatures between 61 and 80 degrees Celsius. They causes [sic] food poisoning when food is contaminated with the poisons. However, in observing cases of sickness by the same illness (botulism) occurring as a result of contamination with the microbe, it is my opinion that its usefulness would double in suicide operations. The microbe grows well in regular laboratory cultures under intense anaerobic conditions (meaning its worth as a lethal biological weapon could double.) The ideal temperature for growth is 25 degrees Celsius, but it can grow in temperatures between 20 and 30 degrees Celsius. The bacteria of this microbe are active in anaerobic conditions. The activity causes the microbe to release the poisons.

Properties of the Poisons

They are released after [exposure to] a temperature of 80 degrees Celsius for a period of 30 minutes, or a temperature of 100 degrees Celsius for 10–15 minutes. They are released in acid, but the exception to that is stomach acid. The poisons are divided into six kinds: A, B, C, D, E, F (A, B, and E cause sickness in people, and C and D cause sickness in animals. The sickness in people is also caused by F, which is found in water environments and produces poison symptoms in people and fish). In English: [it is a] “globulin of high molecular weight.” The weight of the A part is between 6,000 and 9,000 B. These weights are beneficial in the electronic separation of poisons.

How to Cultivate the Specimen

These bacteria are cultivated in normal cultures in the complete absence of oxygen. This requirement can be met simply by lighting a candle inside the flask containing the microbe after either a rubber stopper or a piece of cotton has closed off the opening. This means: place the specimen contaminated with the microbe—which is a piece of dirt—....

Suggested Citation:"4 Bioterrorism and the Food Supply." Institute of Medicine. 2006. Addressing Foodborne Threats to Health: Policies, Practices, and Global Coordination: Workshop Summary. Washington, DC: The National Academies Press. doi: 10.17226/11745.
×

From Where to Obtain the Specimen

From dry dirt. Place some of the dung of grass-eating animals in the dirt. Take the specimens after some days.

The nature of the specimen, as mentioned, is simply dirt. Leave it in anaerobic conditions for a number of days; it will become liquid.

A Section on Poisons

Seeing as bacterial culture contain a number of substances, it is important to use electricity on the poisons. These [processes] are known as electrophoresis and affinity column chromatography. They separate the different materials depending on the differences in their weights (references prior). Admittedly, I do not have details on this point, nor the topics of the concentration and preservation of poisons, may God forgive me.

THE FOOD AND DRUG ADMINISTRATION’S APPROACH TO FOOD DEFENSE

David W. K. Acheson, M.D.21

Food and Drug Administration

A Risk-Based Approach to Food Defense

The FDA is pursuing a multipronged approach to food defense. It includes increasing the awareness of the food industry and other stakeholders to critical opportunities for safeguarding the U.S. food supply, developing prevention strategies and building capacity to implement them, and planning for response to and recovery from an intentional food contamination event. There are many foods that could be intentionally contaminated, and one food that has attracted a lot of attention of late is milk and its potential to be deliberately contaminated with Clostridium botulinum neurotoxin. Although this scenario is discussed in more detail below, it is important to recognize that this is only one food-agent combination amongst the many that the FDA has focused on.

Finding the Risks

The FDA has adopted a risk-based approach to determine where food defense resources should be applied. Following September 11, 2001, the FDA utilized an approach known as operational risk management (ORM). ORM involves

21

Chief Medical Officer and Director, Office of Food Safety, Defense and Outreach, Center for Food Safety and Applied Nutrition.

Suggested Citation:"4 Bioterrorism and the Food Supply." Institute of Medicine. 2006. Addressing Foodborne Threats to Health: Policies, Practices, and Global Coordination: Workshop Summary. Washington, DC: The National Academies Press. doi: 10.17226/11745.
×

a determination of which combinations of foods and agents, and where on the farm-to-table continuum, constitute the highest risks. The FDA began this process with a list of potential terrorism agents that was developed by the CDC in 2000. The FDA modified the agents’ rankings according to a variety of criteria such as the stability of the agent in a food matrix; the effect of the agent on the odor, flavor, or color in a food matrix; the severity of public health outcomes associated with the agent; its oral infective or toxic dose; its availability; and perhaps most important, existing threat intelligence on the use of this agent for foodborne bioterrorism. We then evaluated combinations of these agents with a wide range of foods and food ingredients considered to represent possible targets for foodborne attacks.

The ORM evaluations revealed the probability of contaminating a specific point in the food chain with a specific agent. That information was further enhanced by combining it, in matrix format, with an assessment of the likely severity of outcome, as measured by estimated mortality. The construction of these matrices involved the application of basic science, knowledge of food processing, the food industry, transportation, and logic, but the availability of credible intelligence of a food threat trumped all other factors. We recognize that any food could potentially be contaminated by a determined person or group, thus zero-risk foods do not exist. Higher-risk foods do, however, share several common vulnerability factors: large batch size, which implies a large number of servings; short shelf life, which implies rapid turnaround at retail and rapid consumption; uniform mixing, which would maximize the number of people exposed to an agent; and accessibility of a so-called critical node, defined as a process or activity in the farm-to-table chain during which the agent could be added, undetected, in effective quantities.

Based on this information, the FDA developed guidance documents and training for its staff, state and local regulatory colleagues, and the food industry. This knowledge has also contributed to shaping the agency’s considerations of preventive measures, its emergency response planning, and the setting of its research priorities. Because the FDA does not have authority to regulate the security or defense of the food supply, we use this information as we work cooperatively with state and local regulatory officials, the food industry, and other stakeholders in food defense. A For Official Use Only (FOUO) version of the FDA ORM evaluations was prepared and distributed to both industry and states to facilitate a better understanding of where the risks lie.

Following the ORM approach described above, which gave a broad overview of the relative risks, the FDA has also employed a more sophisticated vulnerability assessment tool called CARVER + Shock. CARVER is an acronym for the following factors by which it assesses the vulnerability of a potential food-agent combination as a target for terrorism:

Suggested Citation:"4 Bioterrorism and the Food Supply." Institute of Medicine. 2006. Addressing Foodborne Threats to Health: Policies, Practices, and Global Coordination: Workshop Summary. Washington, DC: The National Academies Press. doi: 10.17226/11745.
×
  • Criticality (public health and economic impacts)

  • Accessibility (physical access to the targeted food)

  • Recuperability (ability of the affected system/population to recover from the attack)

  • Vulnerability (ease of accomplishing the attack)

  • Effect (losses directly attributable to attack)

  • Recognizability (ease of identifying a target)

An additional measure called “shock,” which combines the physical, psychological, and economic effects, was also evaluated. This framework allows a far more detailed assessment of the farm-to-table continuum than is possible with operational risk management. For example, we might perform a CARVER + Shock vulnerability assessment of a specific beverage product, having already recognized that the uniform mixing of large volumes of this beverage from different suppliers raises the vulnerability of that commodity to terrorism. For example, for fruit juice production a flow diagram is developed, starting with the fruit on a tree in a growing area in the United States or abroad, and continuing with the worker who picks that fruit, the fruit storage facilities on the farm, transport to the dock, shipping and transport from the docks to the warehouse, every processing step through blending and pasteurization, packaging, distribution, and retail. Initially the FDA undertook CARVER + Shock determinations within the federal government only. The results of this process were classified documents that could not be readily shared and thus had the distinct disadvantage of not being readily available to the industry. To address this shortcoming the FDA worked with a number of industries to train them in CARVER + Shock methodology so they could perform their own assessments. With that information, food industries can make the best use of limited resources for food defense.

The current approach for vulnerability assessments is a joint approach led by FDA, USDA, DHS, and the Federal Bureau of Investigation (FBI), and is known as the Strategic Partnership Program Agroterrorism (SPPA) initiative. The SPPA was launched in July 2005 and solicits industry and state volunteers to undertake locally based vulnerability assessments on a variety of food commodities. By being locally based these assessments not only address a specific food commodity but also facilitate local interactions between the very federal, state, and local officials that would have to deal with a deliberate attack on the food supply.

Deliberate Contamination of Milk with Botulinum Toxin

Vulnerability assessments such as the ORM and CARVER + Shock methods discussed above indicate certain foods of higher concern. One of these foods is fluid milk and the specific example of botulinum toxin in milk is frequently raised, since milk production is a significant industry, both in terms of the volume of product consumed and its importance to the U.S. economy.

Suggested Citation:"4 Bioterrorism and the Food Supply." Institute of Medicine. 2006. Addressing Foodborne Threats to Health: Policies, Practices, and Global Coordination: Workshop Summary. Washington, DC: The National Academies Press. doi: 10.17226/11745.
×

After the milking process, milk is typically stored in a tank on the farm that may hold up to 500 gallons until it is transported to the dairy in a 5,000-gallon tanker. At the dairy, milk received from several such tankers is held in bulk tanks of up to 60,000 gallons before it is pasteurized and packaged. Packaged milk is distributed first to a warehouse and then to a retail outlet. Milk has many of the common vulnerability factors mentioned above. The same conclusion was reached in an FOUO report prepared by the U.S. Department of Transportation’s Volpe National Transportation Systems Center in 2004, which was intended to inform the dairy industry about vulnerabilities in the milk supply and ways to address them.

In response to the results of this report, and continuing discussions with the dairy industry, changes have been made by individual milk producers and the dairy industry as a whole that have improved the security of the U.S. milk supply.

There are multiple points along the farm-to-table continuum where food may be vulnerable, and it is critical that the approach to this problem be multifaceted. To this end, the FDA has produced a series of guidance documents, one of which is targeted at the dairy industry and outlines an array of possible steps that can be taken to minimize the chance of a deliberate attack on the food supply (CFSAN, 2003).

Fluid milk is not the only food commodity that may be subject to a deliberate attack, and to that end the FDA produced guidance documents directed toward a variety of other industries. These include the following:

Each one of these documents provides general guidance as well as more focused messages directed toward the specific industry groups.

Research Questions

During the vulnerability assessment process, whether it be ORM or CARVER + Shock, a number of questions typically arise that require research. FDA has undertaken a food defense research strategy that is focused on a number of areas. These include work on the behavior of select agents in certain food matrices, the value of specific mitigation approaches, sensitive and specific detection methods that are rapid, and dose-response relationships with select agents that may be added to food.

Suggested Citation:"4 Bioterrorism and the Food Supply." Institute of Medicine. 2006. Addressing Foodborne Threats to Health: Policies, Practices, and Global Coordination: Workshop Summary. Washington, DC: The National Academies Press. doi: 10.17226/11745.
×
Mitigation of Botulinum Toxin in Milk

Specific steps to mitigate the intentional contamination of milk with botulinum toxin are also being researched. The toxin is sensitive to the effects of heat, and thermal destruction of the toxin occurs in foods that are heated to certain temperatures for long enough times. Milk that is shipped in interstate commerce has to be pasteurized using a minimum temperature of 161° Fahrenheit for 15 seconds. Consideration was therefore given to the impact of pasteurization of milk at higher temperatures and/or for longer times. Basic research was undertaken to address this question and the results shared with the milk industry. However, a number of other issues have to be taken into account if higher pasteurization temperatures or longer times are considered. Such things include the economic impact of heating, then cooling the milk, the increase in plate fouling that occurs at higher temperatures, as well as any possible affect to milk’s taste and color, and potential reductions in its nutritional value.

Another research question that has arisen is whether testing for botulinum toxin in milk provides an alternative to raising pasteurization temperatures. Testing could potentially be performed at various points from farm to table, and depending on a variety of factors such as the sensitivity, specificity, cost, and assay speed it could be a useful addition to other mitigation strategies. Issues such as sensitivity are critical as approximately one million milk tanker trips occur annually in the United States, a test yielding a one percent false positive rate (e.g., an Enzyme Immuno Assay) would falsely identify 10,000 positive tankers holding a total of 500,000 gallons of milk each year. Dealing with such false positives in a timely way could become complex and time consuming.

Although tests for botulinum toxin currently exist, they are not necessarily appropriate for mass testing because of cost or time required to conduct the assay and so on. Toward the goal of a rapid, sensitive, specific, and cost effective assay, a DHS initiative is currently funding the first phase of a program for a rapid (less than 20 minute turnaround), sensitive, specific (less than one per million false positives), simple (could be performed by someone with a high school education), and cost-effective test for botulinum toxin in food. The eventual objective of this project is to develop a platform that could be adapted to detect multiple agents in different food matrices.

At the end of the day, the most important message regarding mitigation strategies is not to rely on a single strategy alone to produce adequate protection. Rather put in place as many different strategies at different points on the farm-to-table continuum that will, overall, minimize the chances of a successful attack on the food supply.

Preparatory Measures

Being prepared for an attack on the food supply is a very important aspect of the FDA’s work. To that end, in 2004 the FDA initiated a series of assignments

Suggested Citation:"4 Bioterrorism and the Food Supply." Institute of Medicine. 2006. Addressing Foodborne Threats to Health: Policies, Practices, and Global Coordination: Workshop Summary. Washington, DC: The National Academies Press. doi: 10.17226/11745.
×

that were associated with special security events and focused on ensuring the safety and defense of the nation’s food supply. These assignments involved activities associated with the G8-Summit, as well as the Democratic and Republican National Conventions. These special event assignments were, however, regional and limited in scope. Based on heightened security during the national election in November 2004, the FDA determined that it was appropriate to issue a broader nationwide food defense assignment. The first assignment of this nature was issued in 2003 during Operation Iraqi Freedom under Operation Liberty Shield. In October 2004, the FDA initiated a new assignment (FDA Security Surveillance Assignment [FSSA]) that, while similar to the Liberty Shield assignment, was designed to involve federal, state, local, and industry partners to a greater extent than was done in Operation Liberty Shield and to better evaluate our national preparedness capabilities. The primary goals of this national assignment are as follows:

  1. Deter intentional contamination of food through heightened and targeted preventive activities at various points in the chain of supply; and

  2. Exercise the planning and implementation of the system for responding to a period of increased food security risk to identify and address gaps in the system.

The food items selected to be part of the assignment were based on the ORM vulnerability assessments undertaken previously by the FDA. This process allowed the FSSA to focus the limited federal, state, and local public health resources on those food commodities with the highest potential for intentional contamination (CFSAN, 2005). The FSSA was designed to test the FDA’s ability to respond to a threat to the food supply, and as such FDA inspectors entered the premises of domestic firms that produced certain foods to discuss food security and food defense issues with their managers. They also took samples of foods in the above categories, which were tested for a variety of chemical (e.g., cyanide) and microbiological (e.g., botulinum toxin) agents using the Food Emergency Response Network (FERN) laboratories. In addition, the FDA conducted an electronic vulnerability analysis of registrations for imported foods in the above categories; it identified 38 “suspicious” products that were subsequently tested using the FERN laboratories.

Response and Recovery

It is likely that a successful attack on the food supply would be detected first at a local level, most likely due to the detection of a sick animal or a sick human, so an effective response requires close coordination with local public health officials. Key aspects of such a response is containment of the threat and communication with the public. Achieving recovery from such an attack requires the means to demonstrate that the food supply is safe, as well as to decontaminate

Suggested Citation:"4 Bioterrorism and the Food Supply." Institute of Medicine. 2006. Addressing Foodborne Threats to Health: Policies, Practices, and Global Coordination: Workshop Summary. Washington, DC: The National Academies Press. doi: 10.17226/11745.
×

and dispose of potentially large amounts of tainted food—including food in the homes of consumers—and processing equipment. Once again, good communication with consumers is critical to the success of a recovery program to reassure the public of when a particular food is safe to consume.

Food Safety vs. Food Defense

Although the discussion in this chapter has been focused on food defense, it is imperative that we do not lose sight of the importance of food safety. A deliberate attack on the food supply is plausible and potentially catastrophic both economically as well as in loss of life. However, foodborne illness due to unintentional events is an ongoing and real everyday event resulting in sickness and death. As we continue to move forward in meeting our food defense goals by increasing preparedness, developing response plans and ensuring we have the tools to facilitate recovery, we must also integrate these approaches into our ongoing food safety work. In this context, we are talking about the same foods in the same farms, manufacturers, warehouses, and so on, as well as the same set of inspectors at the local, state, and federal level, and in some instances even the same agents. The overlap is huge and obvious, and the same resources are used for both. Food safety and food defense are here to stay, and it is critical they be integrated to the maximum extent possible to ensure the most efficient use of resources as well as optimizing response to an event.

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In December 2004, at a press conference called to announce his departure as Secretary of the Department of Health and Human Services (HHS), Tommy Thompson raised both concern and controversy when he remarked that he could not understand why the terrorists had not yet attacked our food supply "because it is so easy to do." Although to date the United States has been spared such a disaster, the many documented examples of unintentional outbreaks of foodborne disease—some of which have sickened hundreds of thousands of people, and killed hundreds—provide a grim basis for estimating the impact of deliberate food adulteration. Due to the wide variety of potential chemical and biological agents that could be introduced at many vulnerable points along the food supply continuum, contaminating food is considered an especially simple, yet effective, means to threaten large populations.

To explore the nature and extent of such threats, possibilities for reducing their impact, and obstacles to this goal, the Forum on Microbial Threats of the Institute of Medicine (IOM) convened the workshop Foodborne Threats to Health: The Policies and Practice of Surveillance, Prevention, Outbreak Investigations, and International Coordination on October 25 and 26, 2005. Workshop participants discussed the threat spectrum and burden of disease associated with foodborne illness and the role that increasing globalization of food production and distribution plays in the transmission of foodborne disease. Participants also reviewed existing research, policies, and practices concerning foodborne threats in order to identify unmet needs, challenges, and opportunities for improving food safety systems, surveillance, and emergency response.

Although this workshop summary provides an account of the individual presentations, it also reflects an important aspect of the Forum philosophy. The workshop functions as a dialogue among representatives from different sectors and presents their beliefs on which areas may merit further attention. However, the reader should be aware that the material presented here expresses the views and opinions of the individuals participating in the workshop and not the deliberations of a formally constituted IOM study committee. These proceedings summarize only what participants stated in the workshop and are not intended to be an exhaustive exploration of the subject matter or a representation of consensus evaluation.

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