Bioterror game finds nations reticent to share smallpox vaccine post-attack

Grim aftermath: Nearly 90,000 dead, smallpox back in the wild

A coordinated smallpox attack on international transportation hubs quickly would divide the world into "the haves and the have nots," exerting extraordinary pressure on world leaders to withhold their vaccine stocks to protect their own populations, a bioterrorism war game revealed.

The Atlantic Storm exercise — which used former world leaders to play the roles of presidents and prime ministers — underscored that terrorists might be able to create massive chaos and divide the global community through a smallpox attack. Held recently in Washington, DC, the exercise was organized by the Center for Biosecurity of the University of Pittsburgh Medical Center (UPMC), the Center for Transatlantic Relations of Johns Hopkins University in Baltimore, and the Transatlantic Biosecurity Network.

As the mock smallpox attacks unfolded, Atlantic Storm world leaders debated the availability of vaccine in their countries and were surprised to learn there was wide disparity even among industrialized nations. Sufficient supplies to vaccinate their respective entire populations are held in the United States, the United Kingdom, France, Germany, and the Netherlands. However, Italy and Sweden, for example, have enough smallpox vaccine for only about 10% of their populations.

"There absolutely is not enough [smallpox vaccine]," says Bradley T. Smith, PhD, one of the organizers of the Atlantic Storm exercise and a fellow at the UPMC Center for Biosecurity.

"There are only about 700 million doses of smallpox vaccine in the world. That will cover about 10% of the global population. Even within Europe and North America, there are definite haves and have nots. The United States has about 100% coverage, but Canada has about 20%."

As a result, the leaders found themselves in a high-stakes game where their national and international priorities might be at cross-purposes. "One of the lessons here is when nations have a limited supply of a critical resource — be it smallpox vaccine, antibiotics, or some other drug — that severely limits their strategic options to share and work together," Smith says. "You have to start making these incredibly challenging decisions about who you’re going to help and who you can’t help."

Game outcome: Smallpox reintroduced

Though the distinguished players were courageous in their decisions, nearly 90,000 people died worldwide and wild smallpox was reintroduced into the undeveloped world in the aftermath.

"By the end of February 2005, we proposed, based on talking with experts, that it was likely that smallpox could be on its way to being re-established in the developing world," Smith tells Bioterrorism Watch. "That would have huge implications for global economy and trade. You would constantly be having new smallpox re-importations from travel and trade back to the developed world — even if they were all vaccinated."

Organizers plan to publish a complete analysis of the findings in the coming months, but drew some preliminary conclusion at game’s end.

The cast of players was extraordinary, with former U.S. Secretary of State Madeleine Albright playing the U.S. president. Many other distinguished international leaders assumed roles similar to the ones they held in real life. With a spectacularly successful terrorist attack under way as the game began, the leaders found themselves under intense pressure to both protect their national interest and aid a world on the brink of catastrophe.

"There are domestic political pressures that are going to very strongly impact national leaders," Smith says. "For a nation like the United States or Germany — that has all of the resources it needs — there is going to be very strong domestic pressure to make sure that it takes care of itself first before it starts helping even close allies.

"Regardless of whether it makes good public health sense or not. These pressures may be underappreciated in the public health community. We wanted to raise this issue to get people talking about it more and being more realistic about what might happen during a crisis like this," he adds.

A worst-case scenario

In the exercise, seed stocks of smallpox virus have been obtained by a terrorist group called Al-Jihad Al-Jadid from a bioweapons facility in the former Soviet Union. Though smallpox is known to be only in the hands of the United States and Russia, this aspect of the scenario has long been the subject of concern and speculation.

Based on reports from Russian scientists, smallpox stocks are believed to exist in at least two and possibly three of the former biological weapons laboratories in the former Soviet Union. Many of those who once worked in these laboratories now are working in other countries, but little information is available as to where they are or what they are doing.1

Returning to the Atlantic Storm scenario, the Al-Jadid terrorists received microbiological training at Indian and U.S. universities. The terrorist group combined this knowledge with publicly available technical information to develop dry powder preparations of the viruses. Then, with their own microbiology training, the terrorist group was able to acquire all the required laboratory equipment to grow and process the Variola major seed stock they had acquired into a relatively high-quality dry powder that then was used in the attacks. The attacks were carried out by vaccinated terrorists who walked throughout the target locations for several hours during periods of peak occupancy. A commercially available dry powder dispenser the size of a small fire extinguisher hidden in a backpack was used to disseminate the agent, the scenario states. Is such viral processing and delivery far-fetched?

"Unfortunately it is not," points out Smith, who holds a PhD in molecular biology from the Massachusetts Institute of Technology. "The technology for aerosol dispersion for both dry powders and wet flurries of biologic mixtures — be they viruses or bacteria — is actually a very common technology."

Agriculture includes an entire subindustry of sprayers and foggers and other devices to make slurries and mixtures that can be sprayed over acres of land, he added. The scenario’s use of a powder medium is similarly grounded in reality. "There is a whole industry in the biotechnology world that is developing dry powders for measles vaccine, other viral vaccines and drug delivery."

Though the lessons of bioterrorism certainly caution against underestimating any enemies, the next phase of Atlantic Storm certainly is a worst-case scenario. Presumably to force global involvement in the game, the scenario calls for multiple smallpox attacks in the same day.

The exercise begins with simultaneous outbreaks of smallpox in Istanbul, Frankfurt, and Rotterdam, with attacks in the United States surfacing later in the day. The attack sites all are among the busiest airports and public transportation centers in the world, including Los Angeles International Airport and New York City’s Penn Station.

While the sheer scale of such an attack may be unlikely, the transmission ratio selected for the scenario actually was a relatively conservative 1-3. The Centers for Disease Control and Prevention (CDC) has criticized media depictions and movies where one smallpox case may infect as many as 20 other people.

"We tried very hard to be conservative in our estimates, making sure that these were things that a broad array of CDC and public health officials would agree with," Smith says. "Frankly, it’s a big enough problem as it is — with conservative estimates."

Ring strategy, mass vaccination considered

The Atlantic Storm leaders debated the issue of surrounding first cases with ring vaccination or opting for mass vaccination of whole populations. This led to discussions of which countries would be willing or politically able to share vaccine.

"We wanted to see what that conversation was about," he adds. "In reality, there is going to be a tipping point. At what point is it still feasible to do ring vaccination vs. switching to mass vaccination? All of these countries plans on paper at least say they are going to do ring vaccination, but if it gets very difficult or some unspecified trigger is met, they have the option of going to mass vaccination."

Acting as the U.S. president, Madeleine Albright expressed doubts as to whether the American people would be willing to give away a portion of the U.S. stockpile to European countries whose governments had been less than supportive of U.S. policies in the recent past. As the day went on, the number of reported smallpox cases grew rapidly, and the number of countries whose populations were affected also increased.

Cases were reported in Canada and Mexico, as well as in countries throughout Europe. A debate ensued about the advisability of closing borders, quarantining cities, and limiting the movement of people and goods.

Participants wanted the World Health Organization (WHO) to manage the distribution of available smallpox vaccine. Providing the reality check was former WHO Director-General Gro Harlem Brundtland. Playing that role in the game, she told participants the WHO has a budget "about as big as that of a middle-sized English hospital."

The WHO consists of 172 member nations but is dependent on them for its resources.

"All of the leaders in this scenario were looking to WHO as an honest broker," Smith says. "That was something they immediately gravitated toward. I think what that means is that WHO should maybe get more resources and authority than it currently has. I think many people would agree it does not have the resources to manage a global distribution campaign of smallpox vaccine."

In reality, the WHO continues to move forward on establishing a global smallpox vaccine reserve. With smallpox eradicated in the wild, the consequences of an intentional release of smallpox must be considered, according to a report presented recently to the executive board of the WHO.

"Population immunity following mass vaccination during the eradication era has waned, leaving much of the world’s population vulnerable," the WHO report states. "The greatest fear is that, in the absence of global capacity to contain an outbreak rapidly, smallpox might re-establish endemicity, undoing one of public health’s greatest achievements."

The WHO report notes that such a vaccine reserve would be a logical way to enhance international response capacity, as most countries are not in a position to build and maintain their own supplies of smallpox vaccine.

The WHO is considering doubling its current stock of 2.5 million doses in Geneva and is asking world member nations to provide another 200 million doses. The United States has pledged 20 million doses of smallpox vaccine to the WHO global stockpile.

The Atlantic Storm exercise certainly underscored the need for a global smallpox vaccine stock, but it raised larger questions that would remain unanswered by that specific remedy. It is easy to imagine similar scenarios involving vaccine and resources for pandemic flu or another biological agent.

"The bigger lesson is regardless of whether [the question is] smallpox vaccine, ventilators, doctors, nurses, or antibiotics, there are no preexisting systems in place for nations to work together and share limited and valuable medical resources," Smith notes. "Unfortunately, there are just none in place."

Indeed, despite the existence of treaties and alliances, no clear partnerships exist when it comes to bioterrorism. The European Union has considered creating stockpiles of smallpox vaccine and other critical supplies but has not reached agreement on the distribution process.

"It was too difficult politically to develop a decision-making process that could be used in a crisis," Smith adds. "For example, could the UK actually agree to share with Germany or France or whatever. They just shelved the whole concept. And this is a union, countries that have the same currency and have no border controls. Yet on this critical security issue, they could not come to agreement."


1. Alibek K, Handelman S. Biohazard: The Chilling True Story of the Largest Covert Biological Weapons Program in the World — Told from Inside by the Man Who Ran It. New York City: Random House; 1999.