The Looming Threat of Bioterrorism

Donald A. Henderson, et al.

Science 283, 1279 (1999);
DOI: 10.1126/science.283.5406.1279

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 SCIENCES COMPASS REVIEW
REVIEW: BIOLOGICAL TERRORISM

The Looming Threat of Bioterrorism

Donald A. Henderson

Biological Incident Response Force and the

Biological weapons have recently attracted the attention and the resources of the Armys Technical Escort Unit. Additional re-
nation. Discerning the nature of the threat of bioweapons as well as appropriate sources have also been provided to the FBI to
responses to them requires greater attention to the biological characteristics of these permit additional agents to be hired, intelli-
instruments of war and terror. The dominant paradigm of a weapon as a nuclear gence efforts are being augmented, and DOD
device that explodes or a chemical cloud that is set adrift leaves us ill-equipped and the Department of Energy have mounted
conceptually and practically to assess and thus to prevent the potentially devastating greatly expanded research programs. Research
effects of bioterrorism. Strengthening the public health and infectious disease infra- areas include the development of environmen-
structure is an effective step toward averting the suffering that could be wrought by tal detection devices for chemical agents and
a terrorists use of a biological agent. some for biological agents, plus the develop-
ment of equipment such as masks and suits for
working in chemically contaminated areas.

T
he past 4 years have been marked by signed lead responsibility for crisis manage-
The Challenge of Biological Agents

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escalating concerns in the United ment, in implementing measures to resolve the
States about the threat of biological immediate emergency and to investigate the Of the weapons of mass destruction (nuclear,
weapons. At first, discussions about the im- scene with the goal of gathering evidence to chemical, and biological), the biological ones
plications of this threat and its possible sce- support criminal prosecution of a perpetrator. are the most greatly feared (4), but the coun-
narios were confined primarily to those in the The federal lead role in coordinating subse- try is least well prepared to deal with them.
military, diplomatic, law enforcement, and quent assistance, termed consequence manage- Virtually all federal efforts in strategic plan-
intelligence communities and to those con- ment, was delegated to the Federal Emergency ning and training have so far been directed
cerned with arms reduction issues. Only re- Management Agency. The Public Health Ser- toward crisis management after a chemical
cently have the civilian medical and public vices Office of Emergency Preparedness release or an explosion. Should such an event
health communities begun to be engaged in (OEP) was asked to coordinate all health and occur, fire, police, and emergency rescue
examining the practical challenges posed by medical assistance. However, OEP was given workers would proceed to the scene and, with
this threat. Professional societies for the first few funds with which to do this, and the De- the FBI assuming lead responsibility, stabi-
time have begun to incorporate discussions of partment of Health and Human Services lize the situation, deal with casualties, decon-
bioterrorism in national meetings. On the in- (HHS), in which OEP is housed, was itself taminate, and collect evidence for identifica-
ternational scene, in 1998 the World Health provided with virtually no new resources. The tion of a perpetrator. This exercise is not
Organization (WHO) decided to establish an dominant role and most of the funds were as- unfamiliar. Spills of hazardous materials, ex-
expert group to review and revise its 1970 signed to the Department of Defense (DOD) plosions, fires, and other civil emergencies
landmark document, Health Aspects of under the 1997 Defense Against Weapons of are not uncommon events.
Chemical and Biological Weapons (1). Mass Destruction Act. The act directed DOD to The expected scenario after release of an
Clearly, there is growing public aware- develop and implement a domestic prepared- aerosol cloud of a biological agent is entirely
ness of the threat of bioterrorism, and there is ness program to improve the ability of local, different (Table 1). The release could be si-
nascent concern among medical and public state, and federal agencies to cope with chem- lent and would almost certainly be undetec-
health professionals as well. This is important ical, biological, and nuclear threats and to con- ted. The cloud would be invisible, odorless,
because if real progress is to be made in duct exercises and preparedness tests. and tasteless. It would behave much like a gas
addressing this difficult problem, a substan- Metropolitan Medical Response Teams, in penetrating interior areas. No one would
tially greater input of good science, medicine, funded by OEP, are now being trained in a know until days or weeks later that anyone
and public health will be needed. program that will eventually reach 120 major had been infected (depending on the mi-
cities (3). These teams are to be composed of crobe). Then patients would begin appearing
Beginnings of a National Response first responders (fire fighting, law enforce- in emergency rooms and physicians offices
The threat of bioterrorism has not been ignored. ment, and emergency medical personnel) that with symptoms of a strange disease that few
Substantial national preparedness measures are already employed by their municipal gov- physicians had ever seen. Special measures
were taken in June 1995 with Presidential De- ernments. Limited funds are available for would be needed for patient care and hospi-
cision Directive 39 (PDD-39), which was fur- training and for the cities to lease equipment talization, obtaining laboratory confirmation
ther elaborated in May 1998 by PDD-62 and but not for operating costs. Meanwhile, 10 regarding the identity of microbes unknown
PDD-63, all classified documents. PDD-39 de- National Guard units of 22 full-time people to most laboratories, providing vaccine or
fined the broad responsibilities and coordina- each, called Rapid Assessment and Initial antibiotics to large portions of the population,
tion relationships among the federal agencies Detection Teams, are being trained. One unit and identifying and possibly quarantining pa-
involved (2). PDD-62 and PDD-63 sought to is planned for each federal region. Under con- tients. Trained epidemiologists would be
define a better organizational structure. The sideration is the possibility of providing one or needed to identify where and when infection
Federal Bureau of Investigation (FBI) was as- more such units for each state. The units will be had occurred, so as to identify how and by
on a standby basis, able to be mobilized quickly whom it may have been spread. Public health
should a chemical or biological substance be administrators would be challenged to under-
The author is at the Johns Hopkins Center for Civilian
Biodefense Studies, Johns Hopkins School of Public
released. Two other specialized units, each con- take emergency management of a problem
Health, Suite 850, Candler Building, 111 Market Place, sisting of several hundred people, have been alien to their experience and in a public en-
Baltimore, MD 21202, USA. establishedthe Marine Corps Chemical and vironment where pestilential disease, let

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 SCIENCES COMPASS
alone in epidemic form, has been unknown. the termination of all research on offensive 400-lb bombs had been outfitted with botuli-
The implicit assumption has frequently bioweapons and the destruction of existing num toxin and anthrax warheads, and drone
been that chemical and biological threats and stocks of agents. The Western countries com- aircraft had been equipped with aerosol dis-
the responses to them are so generically sim- plied but, as time passed, other countries took persal systems. Iraqs bioweapons capability
ilar that they can be readily handled by a an interest in developing their own capacities. remains intact.
single chembio expert, usually a chemist. There was no mechanism for verification of In 1995, the sarin gas attack on metropol-
This is a serious misapprehension (Table 1). this. In the United States during the 1970s and itan Tokyo by the Japanese religious cult
First responders to a biological weapons 1980s, there was a mood of complacency about Aum Shinrikyo came as an unexpected sur-
incident (in contrast to an explosion or chem- bioterrorism; funds for defensive activities all prise. This little known cult foresaw the com-
ical release) would be emergency room phy- but evaporated, and a highly regarded research ing of an apocalyptic war from which its
sicians and nurses, family physicians, infec- program and team were partially dismantled. followers would emerge to assume control
tious disease specialists, infection control That complacency has been shattered in first of Japan and then the world (9). To speed
practitioners, epidemiologists, hospital and recent years by events in Iraq and Japan, by this process, they sought to use weapons of
public health administrators, and laboratory revelations from Soviet defectors that docu- mass destruction to kill hundreds of thou-
experts. Surprisingly, to date there has been mented the extent of the program in Russia, sands, if not millions, and to spread panic.
little involvement of any of these groups in and by the disclosure that at least 10 nations Only in 1998 was it learned that the cult had
planning for appropriate responses or in train- now have a biological weapons capacity (7). actually sought to aerosolize anthrax and bot-
ing. One recent measure to address this def- Discoveries during and after the 1990 Gulf ulinum toxin throughout metropolitan Tokyo
icit is the convening, by the Hopkins Center, War brought new concerns about bioweapons on eight occasions between 1990 and 1995.
of a national Working Group on Civilian (8). Iraq used chemical weapons in the Iran- Although its leader has been imprisoned, the

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Biodefense, which is composed of govern- Iraq war; it was known to be developing a cult remains intact and legal today; it operates
ment and nongovernment experts. The prin- nuclear capability; and there were signs that it electronic, computer, and other stores with a
cipal goal of this group has been to identify had been engaged in developing anthrax as a net revenue of $30 million annually. It is said
which biological agents require priority atten- weapon. Concerns about anthrax arose too to have about 5000 adherents in Japan and to
tion and what should be the most appropriate late, however, for enough vaccine to be pro- have branches in Russia, Ukraine, Belarus,
response to each. duced to vaccinate more than a small propor- and Kazakhstan (10).
tion of the allied forces. After the war, it was Perhaps of greatest concern is the status of
Emergence of the Bioweapons Threat learned that Iraqs bioweapons program was Russias bioweapons establishment. The
Bioweapons programs began to receive sub- substantially larger and more advanced than scope of the Soviet program and details of its
stantial attention during World War II. An in- had been appreciated. In 1995, with the de- operation have become increasingly available
famous Japanese program ceased with the end fection of the Presidents son-in-law Hussein during the 1990s as a result of defections by
of the war, but programs in the United States, Karnel Hassan, Iraqi documents were ob- senior officials of its bioweapons program.
Canada, the Soviet Union, and the United King- tained that portrayed an operation of previ- The signing of the BWC in 1972 is reported
dom expanded steadily until 1972 (5). At that ously unknown scope and sophistication. The to have been seen by the Soviet Union as an
time, the Biological and Toxin Weapons Con- acknowledged production included 20,000 li- opportunity to gain an advantage over its
vention (BWC) was opened for signature and ters of botulinum toxin and 8000 liters of Cold War adversaries. Accordingly, a mas-
was eventually ratified by 140 nations, includ- anthrax spore suspension. SCUD missiles sive expansion of its bioweapons program
ing the Soviet Union and Iraq (6). It called for with a range of 300 to 600 km and carrying was begun (11). The eradication of smallpox
and the cessation of vaccination in 1980 were
considered another opportunity to be exploit-
Table 1. Important distinctions between chemical and biological terrorism. ed. A program was begun to produce small-
pox virus on a very large scale and to weap-
Chemical terrorism Biological terrorism onize it. By 1989, this had been achieved
Speed at which attack results in illness with a production capacity of dozens of tons
Rapid usually minutes to hours after Delayed usually days to weeks after attack of smallpox virus annually. Ken Alibek, a
attack former first deputy chief of research and pro-
Distribution of affected patients duction for the Russian biological weapons
Downwind area near point of release Widely spread through city or region; major program, has reported that smallpox virus
international epidemic in worst-case scenario had been mounted in intercontinental ballistic
First responders missiles and in bombs for strategic use.
Paramedics, firefighters, police, emergency Emergency department physicians and nurses, The biological weapons R&D programs in
rescue workers, and law enforcement infectious disease physicians, infection control
the former Soviet Union were funded and
practitioners, epidemiologists, public health
officials, hospital administrators, and laboratory managed by at least two different entities: the
experts first, called Biopreparat, was in the Ministry
Release site of weapon of Medical and Microbiological Industry; the
Quickly discovered; possible and useful to Difficult to identify; probably not possible or useful second was in the Ministry of Defense. Still
cordon off area of attack to cordon off area of attack operative is a significant proportion of a mul-
Decontamination of patients and environment tilaboratory complex (the vestiges of Bio-
Critically important in most cases Not necessary in most cases preparat) extending across at least eight dif-
Medical interventions ferent cities, which once employed 60,000
Chemical antidotes Vaccines and/or antibiotics workers. One of these laboratories, the Russia
Patient isolation/quarantine State Research Center of Virology and Bio-
After decontamination there is no need Crucial if easily communicable disease is involved technology, is located in Koltsovo, No-
(such as smallpox); advance hospital planning for
isolating large numbers of patients is critical vosibirsk Region (12). It houses one of the
two WHO-sanctioned repositories of small-

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 SCIENCES COMPASS
pox virus [the other being the U.S. Centers effectively alone at the top of the list among Comprehensive reviews of these two dis-
for Disease Control (CDC)]. It has extensive potential agents. eases and consensus views as to appropriate
biosafety level 4 containment facilities, per- medical and public health responses have
mitting it to work with the most virulent Likely Perpetrators already been completed by the working group
pathogens, and is currently utilizing small- Some argue that almost anyone with intent convened by the Hopkins Center (22).
pox, Marburg, and hemorrhagic fever viruses can produce and dispense a biological weap- Smallpox poses an unusually serious
in recombinant research studies. Like other on. It is unlikely, however, that more than a threat; in part, because virtually everyone is
laboratories in Russia, it is experiencing fi- few would be successful in obtaining any of now susceptible, vaccination having stopped
nancial difficulties; substantial numbers of the top-rated agents in a form suitable to be worldwide 20 or more years ago as a result of
scientists have departed and security is more dispensed as an aerosol. Naturally occurring the eradication of the disease. Because of
lax. Where the scientists have gone is un- cases of plague, anthrax, and botulism do waning immunity, it is probable that no more
known, but Libya, Iran, Syria, Iraq, and occur on almost every continent and so pro- than 20% of the population is protected.
North Korea have actively been recruiting vide a potential source for strains. However, Among the unprotected, case fatality rates
such expertise (13). Relative to Biopreparat, there is considerable variation in the viru- after infection with smallpox are 30%. There
far less is known about the activities of the lence of different strains, and a high level of is no treatment. Virus, in aerosol form, can
biological weapons programs centered in the expertise, which is much less obtainable than survive for 24 hours or more and is highly
Ministry of Defense (14). the agents themselves, is needed to identify infectious even at low dosages (23).
A mixture of rogue states and well-fi- an especially pathogenic one. Moreover, pro- An outbreak in which as few as 100 peo-
nanced religious cults with scientists desper- ducing these particular organisms in large ple were infected would quickly tax the re-
ately seeking funds creates a volatile situation quantity and in the ultra-small particle form sources of any community. There would be

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with potentially serious consequences. needed for aerosolization is beyond the aver- both actual cases and people with a fever and
age laboratory. rash for whom the diagnosis was uncertain. In
Probable Agents Soviet laboratories had the sophistication all, 200 or more patients would probably
Any one of thousands of biological agents and capacity to produce all of the most patho- have to be treated in the first wave of cases.
that are capable of causing human infection genic organisms in large quantities. It is as- Most of the patients would be extremely ill
could be considered a potential biological sumed that a number of other countries now with severe aching pains and high fever and
weapon. Realistically, only a few pose seri- also possess this capacity because the costs of would normally be hospitalized. Hospitaliza-
ous problems. The NATO handbook dealing equipping and staffing a bioweapons labora- tion poses problems, however. Because of the
with potential biological warfare agents lists tory are modest when compared to those risk of widespread transmission of the virus,
31 infectious agents (15). Only a very small required for a nuclear or chemical facility. patients would have to be confined to rooms
number of these, however, can be cultivated Any group with sufficient resources could under negative pressure that were equipped
and dispersed effectively so as to cause cases purchase prepared supplies of aerosolizable with special filters to prevent the escape of
and deaths in numbers that would threaten the organisms and could transport them easily, the virus. Hospitals have few rooms so ven-
functioning of a large community. Other fac- because only small quantities are needed to tilated; there would, for example, probably be
tors also determine which microbes are of inflict casualties over a very wide area. No less than 100 in the Washington, D.C., met-
priority concern: specifically, the possibility mechanisms currently exist for screening to ropolitan area.
of further human-to-human spread, the envi- intercept such materials at state or national A vaccination program would have to be
ronmental stability of the organism, the size borders. undertaken rapidly to protect as many as pos-
of the infectious dose, and the availability of Discrete outbreaks of less virulent organ- sible of those who had been in contact with the
prophylactic or therapeutic measures. isms could certainly be propagated by dissi- patients. Vaccination given within 3 to 4 days
A Russian panel of bioweapons experts dent groups with less access to resources and after exposure can protect most people against a
reviewed the microbial agents and concluded sophisticated laboratories. One such outbreak fatal outcome and may prevent the disease en-
that there were 11 that were very likely to be occurred in 1984, when members of the Ra- tirely. It is unlikely, however, that smallpox
used. The top four were smallpox, plague, jneeshi religious sect introduced Salmonella would be diagnosed early enough and vaccina-
anthrax, and botulism (16). Lower on their typhimurium into salad bars in Dallas, Ore- tion programs launched rapidly enough to pre-
list were tularemia, glanders, typhus, Q fever, gon (18). In all, some 750 people became ill; vent infection of many of the people exposed
Venezuelan equine encephalitis, and Mar- none died or were hospitalized. Other epi- during the first wave. Few physicians have ever
burg and influenza viruses. Each of the four sodes of this type could occur but would be seen smallpox and few, if any, have ever re-
top-rated agents is associated with high case unlikely to panic or cripple a city as would an ceived training in its diagnosis. Moreover,
fatality rates when dispersed as an aerosol. outbreak of smallpox or anthrax. mounting a vaccination campaign requires time
The rates range upward from 30% for small- unless there has been advance planning, and no
pox to more than 80% for anthrax. Smallpox Greatest Threats: Smallpox and Anthrax city has yet done such planning. The human
and anthrax have other advantages in that Of the potential biological weapons, small- immunodeficiency virus epidemic and the more
they can be grown reasonably easily and in pox and anthrax pose by far the greatest general issue of vaccine complications among
large quantities and are sturdy organisms that threats, albeit because of different clinical immunosuppressed populations introduce add-
are resistant to destruction. They are thus and epidemiological properties. So far there ed complexity to decision-making regarding
especially suited to aerosol dissemination to have been no examples of the potential dev- smallpox vaccination administration.
reach large areas and numbers of people. astation of biological weapons like those pro- A second wave of cases would be almost
Plague and botulinum toxin are less likely vided by nuclear weapons during World War inevitable. From experiences with smallpox
prospects. From experience in the now de- II. Epidemics of smallpox in Yugoslavia imported into Europe over the past 40 years,
funct U.S. bioweapons development pro- (1972) (19) and of anthrax in the Soviet it is estimated that there would be at least 10
gram, producing and dispensing substantial Union (1979) (20) after an accidental release secondary cases for every case in the first
quantities of plague organisms or botulinum from the Sverdlosk bioweapons production wave (21), or 1000 cases in all, appearing
toxin (17) pose virtually insurmountable facility provide some sense of the magnitude some 14 days after the first wave. Vaccina-
problems. Thus, smallpox and anthrax are and nature of the problems posed (21). tion would initially be needed for health

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 SCIENCES COMPASS
workers, essential service personnel, and con- In May, Assistant Secretary Margaret Feasibility studies suggest that substantially
tacts of patients at home and at work. With Hamburg was assigned responsibility for de- improved second-generation vaccines can be
mounting numbers of cases, contacts, and veloping a strategic plan for HHS. Formerly developed quickly.
involved areas, mass vaccination would soon New York City Commissioner of Health, she Finally, there is a need both now and in
be the only practical approach. That would guided the nations most advanced counter- the longer term to pursue measures that will
not be possible, however, because present terrorist planning effort from the perspective prevent acts of terrorism. Whatever can be
vaccine supplies are too limited, there being of public health and medical consequence done to strengthen the provisions of the BWC
approximately 5 to 7 million doses currently management. At the request of the president deserves all possible support. The strength-
available. To put this number in perspective, and with bipartisan support from Congress, ening of our intelligence capabilities so as to
in New York City in 1947, 6 million people $133 million was appropriated to HHS for anticipate and perhaps interdict terrorists is of
were vaccinated over approximately 1 week fiscal 1999 for countering biological and the highest priority. The fostering of interna-
in response to a total of eight cases of small- chemical threats, $51 million of which is for tional cooperative research programs to en-
pox. Moreover, there are no longer any man- an emergency stockpile of antibiotics and courage openness and dialogue as is now
ufacturers of smallpox vaccine. Best esti- vaccines. Most of the funds are allocated to being done with Russian laboratories is also
mates indicate that substantial additional sup- the CDC, primarily for the strengthening of important.
plies could not be ensured sooner than 36 the infectious disease surveillance network Once the medical community rallied to
months from the initial outbreak. and for enhancing the capacity of federal and support Lown and Chazov (24) in educating
A scenario for an inhalation anthrax epi- state laboratories. This is not a large sum of peoples and policymakers everywhere about
demic is of no less concern. Like smallpox, the money, considering the needs of a fragile the dread realities of a nuclear winter. Per-
aerosol would almost certainly be unobtrusive- public health infrastructure extending over 50 haps the same should now be done with

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ly released and would drift throughout a build- states and at least 120 major cities, but it is a respect to the realities of biological weapons,
ing or even a city without being noticed. After beginning. which are now considered to be a more seri-
2 to 3 days, infected individuals would appear The provision of funds to HHS is conso- ous threat than the nuclear ones.
in emergency rooms and doctors offices with a nant with the general belief that the most
variety of nonspecific symptoms such as fever, effective step now is to strengthen the public References
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within 24 to 72 hours. It is doubtful that anti- als at the state and local level would repre- 3. House Government Reform and Oversight Commit-
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1282 26 FEBRUARY 1999 VOL 283 SCIENCE www.sciencemag.org