CNS Occasional Papers: #9

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Dr. Zelicoff Responds to the Commentaries

by Alan P. Zelicoff, M.D.
Sandia National Laboratory


I am grateful to the Center for Nonproliferation Studies (CNS), Monterey Institute of International Studies, for soliciting commentary on my analysis of the 1971 Aralsk smallpox outbreak. For too many years, discussions about smallpox -- destruction of existing stocks, threat analysis, contingency planning -- have failed to take into account advances in molecular biology as well as the scope and accomplishments of the former Soviet Union's offensive biological warfare (BW) program. With this publication, the CNS has revitalized the debate over these difficult issues.

In reference to the commentaries, Dr. D.A. Henderson's critique of my article centers on the assertion that there is "nothing new" in the findings of my analysis of the Aralsk outbreak. Specifically, he states:

  • It has always been known that smallpox could be aerosolized and disseminated over long distances. Besides, Henderson argues, Dr. Ken Alibek made us (actually, only our intelligence community at that time) aware of Soviet smallpox biological weapons research shortly after he defected in 1992.
  • Former Soviet Vice-Minister of Health Pyotr Burgasov already had given an interview to a Moscow newspaper in November 2001 stating that the Aralsk smallpox outbreak was to the result of a biological weapons test.
  • Because hemorrhagic smallpox has occurred before in other epidemics, it is "not unexpected" that 3 out of the 10 victims of the Aralsk outbreak would have had the hemorrhagic form of the disease.
  • The apparent vaccine resistance of smallpox in Aralsk is consistent with other outbreaks in which, despite successful vaccination, immunity waned after 10 years.
  • The index case had a mild rash and was "well in four days," thus casting doubt on the diagnosis of virulent smallpox.

In response:

The knowledge in the West of the details of the Soviet "work" with smallpox virus are what are at issue here. It is one thing to grow variola virus in chick embryos, and quite another to deliver it as an aerosol over a distance of several kilometers while maintaining virulence. Alibek did not provide any information on the aerosol testing of a smallpox biological weapon on Vozrozhdeniye Island to the general public until after Burgasov was interviewed, which was nine years after his defection. This omission suggests that Alibek's knowledge of the Soviet Union's smallpox program was incomplete, consistent with its highly compartmentalized nature. Indeed, if Dr. Lev Sandakhchiev and Dr. Sergei Netesov (Director and Deputy Director, respectively, of Vektor, in Koltsovo, Siberia) are to be believed, even they were unaware of the test. This is significant because they, unlike Alibek, worked exclusively on viruses for the Soviet BW program, with a concentration on the smallpox virus.

Burgasov's interview was, indeed, the first public revelation of the Aralsk outbreak, but many people doubt Burgasov's credibility -- including commentator Dr. Jack Woodall. Burgasov is infamous for having lied to and successfully duped American scientists in the past and, besides, it turns out he was wrong on the details of the outbreak's effects (he stated, for example, that everyone on the research ship Lev Berg died). I think the scientific community deserves better than the isolated testimony of one ex-Soviet official in characterizing the scope of the threat of use of smallpox virus as a weapon.

The only data ever published on the aerosol survivability of an orthopox virus is found in an article by G.J. Harper, "Airborne micro-organisms: survival test with four viruses," Journal of Hygiene 59:479-486 (1961). The Soviet aerosol test did not take place until more than ten years after this article appeared, and given that they had a robust bioweapons development program, it is possible that the virus particles they weaponized were microencapsulated to, for example, harden them against ultraviolet radiation and other environmental stresses, which would have been a more effective protectant than the horse serum used in Harper's experiment. Thus, the Aralsk outbreak raises the question of how far virulent smallpox viruses can be disseminated as an aerosol plume. Harper's data suggest that high relative humidity destroys the virus (under a reasonable range of temperatures) in hours or less. Indeed, Henderson stated at the National Academy of Sciences (NAS) meeting on June 15, 2002, when I first presented the Aralsk data publicly, that it was not possible for an aerosol of variola viruses to have been transported in the open environment as far as allegedly occurred in 1971. Given that the Aralsk experiment took place in a very warm, high-humidity environment (August in Central Asia), relying on Harper's data alone would bolster Henderson's contention. But, the realization that infectious viruses did travel at least 15 kilometers (and perhaps even further) downwind from their point of release strongly suggests that there is indeed something new to be learned from an analysis of the Aralsk outbreak.

The index case did not have a mild, atypical rash (as described in the Official Report); rather, she had a severe rash -- so severe that she was concerned she might miss her marriage date on August 30 (not August 14 as stated in the Official Report). I believe it is reasonable to assume that she is the more accurate source of information as to the date of her marriage.

Regarding the three hemorrhagic cases (33% of the Aralsk victims), the statistical analysis does not support Henderson's contention that the Aralsk outbreak was similar to other outbreaks in the percentage of hemorrhagic cases (particularly among infants, where it is decidedly rare) or in the ease with which the virus propagated in households where everyone was vaccinated.

One would not expect an aerosol cloud to necessarily penetrate into the interstices of the ship, especially at night (when, for technical reasons, it is most likely that the aerosol was dispersed in the Soviet field test). Two phenomena help to explain why this would be the case. First, at night metal surfaces are cooler than the surrounding air due to black-body radiation into the night sky (you can convince yourself of this by putting your hand on the hood of a car on a hot summer's night -- you'll be amazed how cool it is compared to the ground or wooden objects). Second, aerosol particles will impact and stick on cooler surfaces (that is, cooler relative to the air than carries them). This phenomenon is called themophilic attraction, and is manifested in our everyday experience as dust on windows (especially in the winter). Thus, a thin aerosol cloud of virus particles would be greatly diminished by thermophilic attraction as it approached a cool surface.

Finally, as Henderson knows, I presented my analysis to the NAS staff organizing the June 15th, 2002 public meeting and more than two dozen people at the Centers for Disease Control and Prevention (CDC) to solicit their opinion as to whether or not the Aralsk data warranted presentation (Henderson was invited to participate in the telephone conference, but chose not to). There was consensus (with only a few detractors) that the Advisory Committee on Vaccination Policy should learn about the outbreak and see my statistical analysis before the round of public hearings came to a close.

Dr. Ronald Atlas and Dr. Richard Clover make the following points in their critique:

  • The data in the report on the smallpox vaccination program indicated that there had been a low immunity -- only 31.6% of the residents of Aralsk had been vaccinated. Among first and second grade schoolchildren, 24% had not been vaccinated, and 31.6% showed a primary vaccination reaction when they were vaccinated again following the Aralsk outbreak, indicating a low immunity even among those who had been previously vaccinated. Hence, it seems more likely that there was inadequate immunity in those exposed than the possibility that the strain of smallpox virus was immune-resistant.
  • The viewpoint that proper vaccination would afford protection against the strain of smallpox virus that caused the Aralsk outbreak, even if it came from the Soviet biological weapons program, is supported by the fact that mass vaccination was used to contain the outbreak.

In response:

It is indeed difficult to ascertain the presence of successful vaccination (of those in whom vaccination was undertaken anytime before the outbreak) in most of the victims. The Official Report makes clear that the index case had a vaccination scar yet came down with a severe case of smallpox.

The Official Report refers to an older Report ("No. 86"), from which Atlas and Clover quote:

"During the years from 1966 to 1970, according to Report No. 86 of the epidemiological monitoring station, a total of 69.7% of the district's population and 31.6% of the residents of the city of Aralsk were vaccinated (vaccination and re-vaccination), which is obviously insufficient."

However, there may have been a vaccination effort in the interim, that is, between 1966 and the outbreak in 1971, that could have raised the number of vaccinated persons. This possibility is substantiated by the actual findings on examining individuals during the vaccination campaign in Aralsk (some 49,000 people were vaccinated in a little over two weeks), which revealed:

"As a result of an examination of 1,383 schoolchildren, carried out in order to determine their immunization status by randomly checking the nature of their skin reaction to revaccination, it was determined that 161 of these children (11.6%) did not have vaccination scars. Among the first- and second-grade students, 24% had not been vaccinated, while among the third- to tenth-grade students -- 15%. Of 370 adults examined, 37 (10%) did not have vaccination scars, i.e., had not been previously vaccinated. At the same time, a significant percentage (20.6%) had primary skin reactions, indicating an absence of immunity. A low-immunity segment was observed among first- and second-grade students, where the primary reaction percentage was 31.6%."

Thus, it appears, that in Aralsk, the rate of vaccination "take" before the re-vaccination (or primary vaccination) campaign was closer to 70 -- 75%.

Next, assuming that in other, earlier smallpox outbreaks (e.g., in India and Pakistan) the vaccination "take" among household contacts was similar, then all other things being equal, my statistical analysis shows that smallpox was more likely to spread within households in Aralsk where there was a high percentage of vaccinated people, thus indicating a propensity of the Aralsk strain to spread more easily than was "usual" in vaccinated hosts. That the number of smallpox victims is small does not negate this statistical conclusion.

Finally, Atlas and Clover make a mistake in assessing the effectiveness of vaccination in managing an outbreak when they say that "mass vaccination contained the outbreak," but make no mention of quarantine. I emphasized in my analysis that the Aralsk authorities imposed a quarantine that was massive in scope and duration: no movement in and out of the city for many weeks, hundreds of inhabitants formally hospitalized in observation units, and restriction on movement of inhabitants within the city. Therefore, in Aralsk it was the combination of vaccination and quarantine that was effective in stemming the outbreak.

Woodall opines that importation of smallpox from Afghanistan (or somewhere along the well-established trade routes into the Central Asian portion of the then-Soviet Union) could have accounted for the outbreak. But since the Soviet Union had reported importations in 1961 and 1962 into Moscow (after indigenous smallpox had been declared eradicated before World War II), why not report the Aralsk outbreak if it was imported? After all, it was the Soviet Union that initiated the global smallpox eradication campaign in the first place, and key to its final success was the reporting of all cases, imported or indigenous.

Alternatively, Woodall posits the possibility of fomites (objects contaminated with variola virus, such as imported fabrics) as the cause of the outbreak. But epidemiologists looked for other cases of smallpox in the Aral Sea region and found none. I find it difficult to believe that smallpox would behave in this way; i.e., to present a small cluster of cases in complete isolation. The more reasonable explanation for the Aralsk outbreak is that a secret biological weapons test on Vozrozhdeniye Island was the source of the outbreak.

Woodall also wonders why the Official Report was so riddled with inconsistencies, opining that this was as a result of an effort to cover-up the real source of the outbreak. He then likened this alleged cover-up to the clumsily "written U.S. response to the Cuban allegation that an American aircraft had sprayed Thrips palmi insects over their island, which was so full of contradictions that it looked suspiciously like a badly designed cover-up". Well, maybe so, but the difference is that the Cuban allegation has been authoritatively analyzed and found baseless[1] and, unlike the Soviet Union, the United States presented its version of how the Thrips episode occurred in an open, special session of states parties to the Biological Weapons Convention that was held in 1997. But, I agree with Woodall that there are puzzling aspects of the Official Report that require clarification. This is precisely why I, along with others[2], have called on our colleagues in Russia to provide answers to questions such as those posed by Woodall, as well as samples of the Aralsk smallpox strain. To date, they have not been forthcoming.

In summary, the statistical evidence strongly suggests that the strain of smallpox virus (or, perhaps, quasi-species) responsible for the Aralsk outbreak behaved differently than most strains recovered from earlier outbreaks in that the hemorrhagic manifestation was more common. Moreover, relative vaccine resistance may also have been in the nature of the Aralsk strain. The small numbers of cases involved in the outbreak are, of course, to be noted, but the statistical inferences are nonetheless robust. Given the epidemiology of the outbreak, the wind patterns, the likely infection of the index case on an ecological research vessel traveling down-wind of a secretive Soviet military bioweapons testing ground, and the absence of any other cases of smallpox in the region that could have provided a source for the epidemic, the origin of the Aralsk outbreak cannot be in doubt.

[1] Zilinskas R.A. "Cuban Allegations of Biological Warfare by the United States: Assessing the Evidence." Critical Reviews in Microbiology 25(3):173--227 (1999).

[2] Lederberg, J., Monath, T., Jahrling, P., and Zelicoff, A.P. Letter to Lev A. Sandakchiev, Director of the All Russian Institute of Virology and Biotechnology (Vektor), Koltsovo, Russia, July 15, 2002.


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