CNS Occasional Papers: #9

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Commentary

by

Dr. Jack Woodall
Director, Nucleus for the Investigation of Emerging Infectious Diseases
Department of Medical Biochemistry
Institute of Biomedical Sciences
Federal University of Rio de Janeiro, Brazil


In this commentary I analyze the four hypotheses proposed for the origin of the 1971 smallpox epidemic in Aralsk. Thus, the official 1971 USSR report proposed three alternative scenarios, and a 2001 report from Russia suggested a fourth.

1. Port Source

The first official scenario was that the index case, a fisheries researcher, became infected with smallpox when she went ashore at one of three port cities visited by the ship. But in 2002 the scientist said she never went ashore and that female passengers were in fact expressly prohibited from doing so (no explanation for the prohibition was provided). The official report further stated that she had bought a towel, some fabric, and a dress at the market in Muynak on August 4. Contaminated fabrics are well known to transmit smallpox viruses; viz. the contaminated blankets distributed to American Indians in the past. But although she remembers the port call at Muynak, she denies going ashore, let alone buying anything there. However, it is presumably possible that she asked somebody else to get those items for her, and she simply has forgotten that.

As the translators note, the official report contains many conflicting dates. The most important for purposes of analysis are those of the port calls and the arrival in Aralsk at the end of the voyage. To quote the official report (p. 26):

The expedition was conducting research at 20 stations in the Aral Sea from June 15 to August 8, 1971. Members of the crew and of the research team went ashore on July 29 in the town of Uyaly in the Kzyl-Orda region, on July 31 in the town of Komsomolsk-on-Ustyurt, and on August 4 in the town of Muynak in the Karakalpak ASSR... On August 11 upon her arrival in Aralsk ... the physician ... was called to the house, and he noted that the patient complained of the following: headache, cough, and a fever up to 39 degrees. He completed a form releasing her from work from August 11 to August 17.

Further on (p. 29):

Thus, consistent with the average incubation period, it is presumed that [Patient 2] contracted the disease sometime between August 10 and August 20, 1971, when his older sister came home from her trip... As has been mentioned before, she was sailing the Aral Sea from July 18 to August 8 and went ashore on July 29 and 31, 1971, and August 4, 1971. She became ill on August 6. It can be presumed that she became infected with smallpox in one of the two locations [where she went ashore]. Judging by the incubation period, these locations were Uyaly and Komsomolsk [-on Ustyurt]. This is confirmed by the absence of the illness among the other crewmembers of the vessel and among the researchers.

In fact, Patient 1 did state in her phone interview that no one on board the Lev Berg developed illness or fever. But the official report states on p. 29: "Patient 1 and her friend P., who fell ill a day earlier, associated their illness with the fact that they had felt very cold a few days prior, when they were casting nets from the boat." P.'s blood was tested but the results are not included in the report. It seems unlikely that P. would have been blood tested if she had not been ill.

Note that the port dates are consistent in the two sections of the report, but the arrival date varies between August 8 and 11, and the onset of illness between August 6 and 11.

Thus the official report excludes Muynak as the place where the index case contracted smallpox. Zelicoff also excludes Muynak on the grounds that the incubation time is too short, quoting a period of 11-15 days (95% CI). Based on their onset dates in relation to the earliest appearance of rash -- and therefore of infectivity -- in their contacts, Patients 6, 8, and 9 could have had incubation periods as short as eight days. Therefore, if Patient 1 fell ill on August 6, as stated in the official report, there was only enough time for her to have become infected during the port call on July 29, not at the one on July 31 or at Muynak on August 4. On the other hand, if her illness began on the day of her return home to Aralsk, as she recalls -- while not remembering the actual date -- whether that was August 8, 10, or 11, it brings the July 31 port call into contention (assuming that the port dates are correct). It seems unlikely that she would have forgotten being confined to her bunk for the last 5 days of the voyage, as the official report has it and which she denies.

Whatever the reality of the dates, it seems that the ship was visiting ports and sailing in waters south of the island test range during dates that would fit the incubation period of her illness.

According to the second scenario (below), teams from the Aralsk shipping company were sent to the port of Termez, where they transferred ship cargos from Afghanistan to trains, and one such team was en route back to Aralsk from Termez during August. Could a team (not necessarily the same one), northbound from Termez to Aralsk, have been in one of the ports at the same time that the ship called?

2. Trade Route Source

The second scenario was that the virus originated in Afghanistan, where smallpox was still endemic at the time, and reached Aralsk from the southern border regions of Kazakhstan by land or waterway. This scenario differs from the first in that it postulates direct infection of Aralsk from the south without involving other Aral Sea ports and land transit points.

Atshabar, in the Foreword, states that this hypothesis is less plausible because the disease could only have been transported from Afghanistan to Aralsk through Tajikistan and Uzbekistan. If people had become ill with smallpox in those republics, he says they certainly would have been detected, yet no such cases were reported. Zelicoff states: "In and of itself, the failure of the Soviet Union to notify the World Health Organization (WHO) of the 1971 outbreak suggests a sinister source for the epidemic." But non-reporting of infectious disease outbreaks in the USSR was routine at the time -- see the Introduction: "Epidemics in the Union of Soviet Socialist Republics (USSR) often went unreported because they undermined the propaganda image of the socialist workers' paradise." On Zelicoff's premise, every failure to report cholera to the WHO would suggest a sinister source.

The USSR reported importations of smallpox into the region from Afghanistan to the WHO in 1959 (one non-fatal case arrived by land at Termez in July) and 1961 (one non-fatal case arrived by land at Kirovabad in October), and none thereafter [1]. However, the big breakout of smallpox from Afghanistan to the west began in 1970, when the disease first reached Mashhad, which is located on Iran's northern border with the USSR, in October. From there it followed trade routes south to the Persian Gulf and west to Iraq, arriving in that nation by the end of 1971. Smallpox then spread through Turkey to Yugoslavia by 1972 [2]. It is logical that in the same time frame the disease would also have followed the road north from Mashhad, along the west coast of the Aral Sea to Komsomolsk-on-Ustyurt and Aralsk, and the Amu-Darya River from the Afghan border to Muynak on the Aral Sea and across it to Aralsk.

The official report states (p. 30):

According to World Health Organization reports, there were 1,030 cases of smallpox in Afghanistan in 1970, and 482 cases during the first eight months of 1971. The disease could have reached the territory of the Tajik and Uzbek Soviet Socialist Republics, which were economically linked to the city of Aralsk. Large quantities of cotton, melons, and other agricultural products from the Uzbek and Tajik republics were shipped north to Aralsk via the Amu-Darya River and the Aral Sea, whereas grain, coal, and other items were shipped south.

Workers from Aralsk and other cities and towns in the region serviced the Uch-Say transshipping facility. Periodically, teams from the Aralsk shipping company were sent to the port of Termez, where they transferred cargo from Afghanistan from ships to trains. Such a team arrived in Aralsk from Termez on August 29-30. Nevertheless, its members could not have been the source of infection for Patient 1 because of the time discrepancy.

Since Patient 1 was already ill before August 29, as was her brother, Patient 2, and all subsequent cases were linked to her household, this scenario is effectively ruled out.

3. Fomites in the Aralsk Market as a Possible Source

According to the third hypothesis presented on page 30 of the official report:

A scenario of infection via the open-air market has also been thoroughly checked. As a matter of fact, individuals bring to the city of Aralsk large quantities of produce from the Uzbek and Tajik republics. However, no evidence was established that people with smallpox arrived from those regions and visited the home of [the father of Patients 1 and 2] or the market's director [also the father], or that goods such as rugs and other wool artifacts were bought or sold there.

It would be entirely possible that the disease could reach the territory of the Tajik and Uzbek SSRs [Soviet Socialist Republics]. These regions are connected to the city of Aralsk economically, as large quantities of cargo are conveyed via the Amu-Darya River and the Aral Sea. Cotton, melons, etc. are shipped to the north, while grain, coal, and other items are shipped to the south."

But an artifact does not have to be made of wool to carry smallpox virus -- clothing and laundry have frequently been incriminated in the past as carriers of the virus. Imported raw cotton was suspected of causing some outbreaks in England [3]. But in any case, no smallpox case was recognized in Aralsk before Patient 1's arrival there, and all subsequent cases could be traced back to her household.

4. The Biological Weapons Field Test Site on Vozrozhdeniye Island as a Possible Source

This scenario is based on information derived from an interview with Burgasov's published in 2001. Burgasov's spreading of the disinformation that the source of the 1979 Sverdlovsk anthrax outbreak was contaminated meat had earlier destroyed his credibility. Is he trying to re-establish it now by claiming that this outbreak was the result of a biological weapons test? Zelicoff points out there are inconsistencies in Burgasov's account of the Aralsk incident, as he remembered it 30 years later; for example, his assertion that all the smallpox victims died. Another is his statement that the researcher was collecting plankton, when both the official 1971 report and the researcher interviewed by Zelicoff agree that she was collecting fish. So why should we now believe his statement that the research ship sailed inside the 40 km exclusion zone?

Although D.A. Henderson recently has stated that it is possible to dry the smallpox virus and add stabilizers so it can persist a long time in the air like anthrax [4], it is improbable that the technology to do so had been invented by 1971. The state of the art at the time was published in a 1970 WHO report; airborne viruses could not be expected to retain their lethality for aerosol transmission of more than 1 km -- in contrast to Bacillus anthracis spores with a range of more than 20 km [5]. So even if the ship did come as close as 15 km to the island, as stated by Burgasov, it is unlikely that airborne infection could have occurred after the virus had traveled that distance.

Referring to the virulence of the virus that caused the 1971 outbreak, I quote from the official report:

According to a September 29 report from Guryev and Alma Ata (where both Patient 1 and friend P. had gone -- JW), neither woman had any traces of smallpox on their skin. They were completely healthy. Both had vaccination scars. However, blood-serum tests on Patient 1, conducted in Moscow, showed high antibody levels, indicating recent exposure to the smallpox virus. Obviously, she had been sick with the mild form of the disease -- varioloid.

Alternatively, it could have been that her previous vaccination protected her, as well as the three other mild cases that had previous vaccinations. Further, "The source of the infection was [Patients 1 and 2's] family, from which the infectious agent spread to four households. By September 27 (i.e., within 5 days), the outbreak was contained." Taken together, this does not suggest that a laboratory-produced strain with enhanced virulence caused the Aralsk outbreak.

Summary

I start from the premise that, when interviewed in 2002, Patient 1 had no reason to falsify her recollection of events in 1971, whereas if the outbreak was suspected of being linked to secret experiments, the writers of the 1971 reports had every reason to alter events to fit a version that excluded the possibility of airborne infection at sea.

There are major discrepancies between the 2002 recollections of Patient 1 and the 1971 official report. If the official report was an attempt at a cover-up, the authors went to extraordinary lengths. According to Patient 1, they fabricated a story that she went ashore at all three ports, bought textiles at the August 4 port call -- even though, by their own calculations, that was already too late to have been the day of infection (so why invent it? To give an air of verisimilitude?) -- that she and a female friend called P. both fell ill on board, and that she was bunk-ridden for five days before the ship's arrival back in Aralsk. Was this all false, designed to bolster the hypothesis that the infection was contracted on July 29 or 31 at one of those port calls rather than at sea?

The translators noticed that dates in the original reports are inconsistent. Was this the result of alterations designed to place the ship at a port within the supposed incubation period, or was it simply bureaucratic sloppiness? I recall that the written U.S. response to the Cuban allegation that an American aircraft had sprayed Thrips palmi insects over their island was so full of contradictions that it looked suspiciously like a badly designed cover-up [6].

If Patient 1 had contracted smallpox in a year when there was no smallpox activity in any neighboring country, it would have been reasonably conclusive of an unnatural origin. But smallpox was spreading in the region, and the absence of any reporting from the USSR was not unusual.

Recall that examination of autopsy specimens from the 1979 Sverdlovsk epidemic revealed multiple strains of anthrax in the same patient, an unnatural finding [7]. In that case, the location downwind of a military laboratory was definitive. On the other hand, after a hitherto unknown strain of hantavirus appeared in humans in 1993 in the region of several military proving grounds in western U.S.A., field research demonstrated that the strain was widespread in humans and wild rodents nationwide, and had been so for years previously [8], thus reducing the likelihood that it was an escapee from a military test. The location of the outbreak therefore appears to have been coincidental to the virus' natural range. Likewise, the location of the 1971 smallpox outbreak in Aralsk could have been coincidental to the presence of the smallpox virus in Afghanistan and other nearby countries.

In spite of the two deaths from hemorrhagic smallpox, there is evidence for the strain involved not having been exceptionally virulent. Unless nucleic acid sequences can be obtained from the autopsy specimens, it will be impossible to say whether the smallpox strain involved was the Afghanistan 1970-71 strain or a laboratory strain. Of course, if an isolate from the Aralsk outbreak still exists in a deep freeze somewhere, and can be shown to be significantly different from the contemporary Afghan strain, then all would be clear.

To conclude, my opinion is that there is at present insufficient evidence to decide between scenarios 1 and 4. Suggestions follow as to how the issue might be clarified.

Further questions to Patient 1:

  1. Does she remember hearing about an exclusion zone? If so, how big was it? Did the ship enter it? If so, why? How near did it approach the island? To the north, south, east or west?
  2. If not, how near did the ship approach to the south end of the island while sailing between Uyaly and Komsomolsk?
  3. Why were female passengers not allowed ashore at ports?
  4. Did she receive on board a towel, clothing or fabric from one of the ports -- perhaps obtained for her by someone who went ashore?
  5. Does she remember a female passenger named P. and, if so, was P. sick on board? If P. was sick, how long before the ship's return to Aralsk did symptoms appear?

Suggestions for further research:

  1. Try to obtain the ship's log to verify dates; failing that, check harbormaster logs at the three ports visited by the Lev Berg.
  2. Try to locate the Lev Berg's laboratory journal at its home fisheries institute.
  3. Try to obtain the reports of the contemporary epidemiological investigations mentioned by Sarynov as in process in the three port cities.
  4. Obtain wind force and direction data from Aralsk airport for the relevant dates, through the International Meteorological Organization, Geneva, Switzerland.
  5. Try to obtain autopsy material, or better, the strains isolated during the outbreak, for nucleic acid sequencing of the causative virus.

References

[1] Fenner, F., Henderson, D.A., Arita, L., Jezek, Z., and Ladnyi, I.D. Smallpox and Its Eradication (Geneva: World Health Organization, 1988), Table 23.2.
[2] Ibid. Fig. 23.5.
[3] Ibid. p. 1343.
[4] Rowland, R. Panel: Smallpox vaccine not for everyone; CNN.com/Health, <http://www.cnn.com/2002/HEALTH/conditions/06/20/smallpox.vaccine/index.html>. Accessed July 11, 2002.
[5] World Health Organization, Health Aspects of Chemical and Biological Weapons (Geneva: World Health Organization, 1970), Table 10.
[6] United States, Documents in Support of United States Presentation Regarding Cuban BW Allegations, Geneva, Switzerland, 25 August 1997 (Geneva: United States Delegation, 1997).
[7] Jackson, Paul J.; Hugh-Jones, Martin E.; Adair, Debra M., et al., "PCR analysis of tissue samples from the 1979 Sverdlovsk anthrax victims: The presence of multiple Bacillus anthracis strains in different victims." Proceedings of the National Academy of Sciences, USA, vol. 95, pp. 1224-1229 (1998).
[8] Nichol, S.T.; Spiropoulo, C.F.; Morzunov, S., et al., "Genetic identification of a Hantavirus associated with an outbreak of an acute respiratory illness." Science vol. 262, pp. 914-917 (1993).


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