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An ‘insurance policy’ for smallpox eradication

April 15, 2011

Feature: The World Health Organization’s monkeypox surveillance programme, 1980–86 – by Robin Fawcett

In May 1980, the WHO certified the global eradication of smallpox. In recent years, historians have examined more closely the difference between the public and private, published and unpublished, accounts of the eradication, and the discrepancies can be revealing.

What is monkeypox?

  • First discovered in 1958 in monkeys (hence the name), but more common in rodents.
  • Part of the orthopoxvirus genus, like smallpox – the two have similar symptoms in humans.
  • Commonest in central and west Africa, but never a major killer.

Beneath the triumphant language of the historic declaration lies evidence of considerable scientific uncertainty and fear that variola virus might yet lurk in some remote corner of the globe, or that a closely related virus – monkeypox – might mutate into the very scourge the WHO had struggled to eliminate. With this in mind, the WHO Smallpox Eradication Unit conducted a broad and intensive monkeypox surveillance programme in central and western Africa from 1980 to 1986. An examination of unpublished papers in the WHO smallpox eradication programme archives in Geneva suggests that the WHO’s motives with regard to the monkeypox programme were more complex than generally acknowledged.

Years before the intensive monkeypox research programme, WHO researchers had acknowledged repeatedly that monkeypox virus, in and of itself, was unlikely ever to become a major public health threat. Instead, the WHO’s commitment to the research was a result of the virus’s clinical and laboratory similarities to variola virus; the interest in monkeypox naturally intensified as the smallpox eradication programme drew to a close.

Monkeypox virus and variola are both members of the genus orthopoxvirus, although their epidemiological features differ; it was generally accepted that, unlike smallpox, monkeypox had an animal (not human) reservoir. In humans, monkeypox was virtually indistinguishable from smallpox infection, with a similar clinical course of fever and pustular rash. And in the 1970s, Soviet scientists even suggested that a variant of monkeypox, dubbed ‘whitepox’, was identical to variola.

In contrast to the optimistic language of the smallpox eradication announcement, WHO scientific working papers from 1978–79 reveal fears that smallpox might return, from either an animal reservoir or the mutation of monkeypox. Just months before the 1980 declaration, the Global Commission for the Certification of Smallpox Eradication recommended that the WHO give urgent priority to the Soviet whitepox findings. This and the subsequent research and surveillance activities demonstrate the fears that monkeypox was a threat to the success of smallpox eradication. The need for an ‘insurance policy’ against unexpected poxvirus would be a familiar theme in WHO plans for a dedicated programme of monkeypox surveillance and research.

In 1979, the Smallpox Eradication Unit proposed monkeypox surveillance and research activities notable for their extraordinary depth and breadth. Objectives included: a more precise definition of human monkeypox frequency, transmissibility and geographic distribution; determination of the monkeypox virus reservoir and ecology; and ascertainment of whitepox virus prevalence as well as other animal orthopoxviruses that might cause human disease in west and central Africa. The proposed target countries included Zaire (as was), Nigeria, Cameroon, Ivory Coast, Liberia, Sudan and Malaysia.

Monkeypox coordination meeting in Zaire, 1981

Monkeypox coordination meeting in Zaire, 1981. The attendees hold diagnostic cards showing characteristic symptoms. WHO Photo

The scope of the monkeypox programme attracted private criticism from smallpox eradication veterans, including Dr Donald A Henderson, who was director of the smallpox eradication programme during the crucial years 1966–77. Medical and scientific researchers with experience in central Africa had reservations, too, about the complex technical and logistical challenges inherent in the proposed field activities. The participation of local health authorities, particularly in Zaire, was questioned, as was the conservative estimate of costs. Furthermore, an immense backlog of sera at the US CDC from suspected smallpox cases would mean long delays for the processing of animal sera and tissue samples from monkeypox ecological surveys, and the monkeypox-specific antibody testing available at that time was unreliable. Nevertheless, by May 1980, the monkeypox surveillance programme was well underway.

The monkeypox programme occupied an important place in the WHO agenda for more than five years, led by some of the Smallpox Eradication Unit’s most experienced officers. The activities covered a large swathe of territory, with a population of more than 5 million people. Nearly 300 cases of human monkeypox were detected, mostly in Zaire, where the programme was most active. Surveillance there was mainly hospital-based, targeted in rainforest regions. Serological surveillance was also conducted in Zaire in areas with the highest incidence of human monkeypox, mostly by collecting sera from children who had not received smallpox vaccine. These field studies, in combination with serological analysis and epidemiological research, were conducted at great length and expense, despite considerable administrative, logistical and political challenges. The campaign itself was characterised by frequent changes in research priorities and tactics, as the efficacy of particular strategies, and their implementation in different localities, was much debated.

The response of Zaire’s citizens, local health officials and government officers to the growing WHO presence is not well documented in the Geneva archives. The WHO did make an effort in 1980–81 to personalise the country-specific surveillance programmes in western Africa. In Zaire, however, in keeping with the WHO system established in the days of smallpox eradication, the leadership and organisation of the monkeypox programme were kept separate from the Zairian public health programmes that provided both financial and personnel support. This caused operational challenges. The WHO surveillance protocols were criticised by the Zaire public health service, for example, because they were incompatible with long-established national health maintenance systems and contained highly technical language unsuitable for the Zairian nursing staff to whom the protocol was distributed.

Operational complexities in Zaire abounded, and there was conflict at times between WHO administrators in Geneva and the research teams in the field. Cooperation from villagers and hunters was essential for the animal serology surveys, but the Zairian currency frequently experienced massive devaluation and was therefore not useful for compensation. By 1985, WHO field teams had adopted a form of currency that was both practical and highly effective: they paid villagers with shotgun cartridges. As correspondence between the field teams and WHO headquarters reveals, administrators were shocked and disturbed to discover their researchers dealing in such controversial material. The WHO field officers were immediately instructed to use only local currency, much to the dismay of the research team.

While field research in central and west Africa struggled to get underway, scientific fears about whitepox virus were being laid to rest. In late 1982, a breakthrough paper by Dr Keith Dumbell, a British authority on variola virus, discredited the Soviet whitepox research. Dumbell compared key biological markers of variola strains and demonstrated that cross- contamination of variola isolates in the Soviet lab had been responsible for the controversial findings. WHO scientists have more recently suggested that Soviet interest in variola virus and monkeypox research may have been prompted in part by Soviet efforts to weaponise orthopoxviruses, and the whitepox findings may have been deliberately fabricated.

Dumbell’s conclusions and the scientific community’s subsequent dismissal of the whitepox threat mark a major turning-point in the language used by the WHO to justify the monkeypox surveillance programme’s activities. By 1983, WHO committee working papers referred not to the threat of smallpox recurrence but to helping African nations manage outbreaks of human monkeypox. Tragically, it would be a different viral infection that would cause Africa’s next public health crisis. In 1986, the WHO Committee on Orthopoxvirus Infections decided that the human monkeypox programme should be discontinued in light of the new research priority in central and west Africa: HIV/AIDS.

Sporadic cases of human monkeypox infection continued in central and west Africa after the conclusion of the active surveillance programme. Significant outbreaks occurred in Zaire in 1996–97 and again in 2001; extended inter- human transmission was noted in an outbreak in the Republic of the Congo in 2005. A cluster of monkeypox infections occurred in the midwestern USA in 2003, associated with exposure to infected prairie dogs; the outbreak was traced to the importation of small mammals from Africa. Today, many epidemiologists and scientists consider monkeypox a potential bioterrorism threat.

The six-year mandate granted to the WHO monkeypox surveillance programme following the global eradication of smallpox provides a basis on which the confident rhetoric of the eradication declaration can – and should – be questioned. Three decades later, as we celebrate this monumental achievement, the medical world remains wary of smallpox, both as a disease and as a weapon. The history of smallpox eradication, and its research politics and methods, remains contemporary and relevant.

Robin Fawcett MD MA was a postgraduate student at the Wellcome Trust Centre for the History of Medicine at UCL and is now practising medicine in Reston, Virginia, USA.

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