CHAPTER 23 SMALLPOX IN NON-ENDEMIC COUNTRIES Contents Page Introduction 1069 Criteria for defining non-endemic countries 1070 The significance of smallpox in non-endemic countries 1071 Actions taken by the non-endemic countries 1071 Actions taken by WHO 1073 Smallpox in Europe, 1959-1978 1073 Sources of importations 1073 Nature of index cases 1075 Delays in notification 1076 Transmission from imported cases 1076 Case studies of importations into Europe 1078 Importations into North America after 1959 1081 Importations into Japan 1081 Importations into recently endemic countries, 1959-1976 1082 Africa 1083 South America 1085 Southern Asia 1085 The 1970-1 972 outbreak in south-western Asia and Europe 1087 Iran 1088 Iraq 1090 Syrian Arab Republic 1090 Yugoslavia 1091 Laboratory-associated outbreaks in the United Kingdom 1095 The London outbreak, 1973 1095 The Birmingham outbreak, 1978 1097 Outbreak of variola minor in the Midlands and Wales, 1966 1098 Conclusions 1100 INTRODUCTION world in the 1960s and early 1970s, cases continued to be imported into smallpox-free In the preceding 11 chapters we have countries. The annual numbers of smallpox systematically reviewed the elimination of cases in most of the larger countries between smallpox from the 31 countries in which it 1920 and 1958 are tabulated in Chapter 8. The was endemic in 1967 and 2 other countries year in which smallpox was last endemic in (Botswana and the Sudan) in which endem- each of these countries is indicated in the icity was re-established after 1967. Because tables; cases occurring after that year were smallpox was endemic in many parts of the due to importations. This chapter is con- 1069 1070 SMALLPOX AND ITS ERADICATION Table 23. I. Annual numbers of importations of million air passengers in 1948, 46 million in smallpox into industrialized countries, 1966, and over 400 million in 1975) and the 1959-I978 much greater speed of travel by air than by sea. As the Intensified Smallpox Eradication EuroDea~~ -r ~ Proe-ramme" moceeded, more detailed infor- Year Source Canada Japan mation was collected about cases throughout country Source Laboratory- known uncertain associated Africa, South America and Asia, and as a result of this effort, many outbreaks were 1959 46 I 0 0 recognized which were due to transfers across 1960 I 0 0 0 1961 10 0 0 0 national boundaries in each of those contin- 1962 4 0 I 0 ents. Most of these importations were con- 1963 2 I 0 0 1964 0 0 0 0 tained, but some had serious consequences, 1965 I 0 0 0 leading to the re-establishment of endemic 1966 0 0 I 0 0 smallpox in the Sudan (1 968), Botswana 1967 4 0 0 0 0 1960 2 0 0 0 0 (1971), Bangladesh (1972) and Somalia 1969 I 0 0 0 0 (1976). An importation from Afghanistan 1970 I 0 0 0 0 into Iran in 1970 led to a large epidemic 1971 0 0 0 0 0 1972 I 0 0 0 which was not terminated until 1972, and 1973 I 0 0 I spread from Iran to Iraq, then to the Syrian 1974 0 0 0 I 1975 0 0 0 0 Arab Republic, and from Iraq to Yugoslavia. 1976 0 0 0 0 0 Excluding the laboratory-associated inci- 1977 0 0 0 0 0 dents, the 34 outbreaks in Europe produced 1978 0 0 I 0 0 573 cases, of which 90 were fatal. Although Total 32 2 3 I 2 the number of cases was extremely small a Thirteen countries; see Table 23.2. compared with the number occurring in the One outbreak in the Federal Republic of Germany started in endemic countries (perhaps some 50 million 1958 but continued into 1959. cases annually in the mid-l950s), health officers and the general public in the industri- alized countries feared smallpox more than cerned with a more detailed description and any other of the diseases then primarily analysis of outbreaks of smallpox that oc- indigenous to the developing countries. curred in industrialized non-endemic coun- Importations into Europe and Japan did tries after 1958, and in non-endemic countries not cease until 1974, when smallpox had been of Africa, South America and Asia after 1966, eliminated from most countries of Africa, when reasonably complete information first from Indonesia, and from large areas of India began to be compiled. and Pakistan, including most of the larger In the industrialized countries a total of 37 cities. outbreaks due to importations from endemic areas were reported between 1959 and 1974: 34 occurred in 13 countries of Europe, 1 in CRITERIA FOR DEFINING Canada, and 2 in Japan (Table 23.1). In NON-ENDEMIC COUNTRIES addition to importations by infected persons, there were 3 laboratory-associated outbreaks Apart from the industrialized countries, in in the United Kingdom between 1966 and which importations had been recognized as 1978. These are comparable to importations such from the 1940s or earlier, few efforts from endemic countries in that they were were made until 1967 to classify countries as introductions of smallpox infection into a having endemic smallpox or as being small- smallpox-free country ; they are described in pox-free. All countries, by international con- the last section of this chapter. vention, were supposed to report the occur- A notable feature of this period, compared rence of cases of smallpox promptly to WHO, with earlier times (see Chapters 5 and 8), was but not all did so, nor were the reports that the absence of transfers of smallpox between were received investigated to determine their the Eastern and Western Hemispheres, and validity. With the establishment of the Inten- the rarity of intercontinental importations sified Smallpox Eradication Programme, a other than from the Indian subcontinent to deliberate attempt was made to distinguish Europe (Fig. 23.1). This is surprising, in view countries in which smallpox was endemic of the vast volume of international traffic (4 from those that were free of the disease. Many 23. SMALLPOX IN NOS-ENDEMIC COUNTRIES 1071 errors in reporting the existence of smallpox, except for international travellers, and only and many instances of failure to report the about 60°& of the population were disease, were discovered. After considerable vaccinated. inquiry, 31 countries or territories were eventually categorized as harbouring endemic Vaccination certij'icdtes smallpox in 1967 (see Chapter 10). Between 1959, when the global smallpox Many countries placed considerable reli- eradication programme began, and 1967, a ance on the examination of certificates of number of countries of Africa, South America vaccination, spending much money on and Asia which were thought to be non- checking them and complaining about falsi- endemic reported a few cases each year-too fied certificates. However, there were several few to represent accurately an endemic situa- deficiencies in the certification system. For tion with continuing transmission. Before example, vaccination certificates were regu- 1967 few of these outbreaks had been further larly examined at most-but not all-Euro- investigated, and it was impossible to deter- pean airports. This was less of a problem in mine whether they were due to occasional Canada and the USA, in which airport health importations or represented underreported officials were rather more rigorous in asking endemic smallpox, or, indeed, whether they all arriving passengers where they had been in were fictitious events reported as a result of the preceding 14 days and requiring a valid clerical or diagnostic error. vaccination certificate from all those who had Because of uncertainty as to whether coun- been in a smallpox-endemic country during tries in Africa, South America and Asia were this period. indeed free of smallpox, and because report- With regard to vaccination certificates, ing had been unsatisfactory and importations there was much discussion of the need to had rarely been fully documented, discussion examine the results of vaccinations 7-9 days of importations into these countries will be later to confirm whether these had been brief, and restricted, for the most part, to the successful, and to require a repeat vaccination period after 1967. if they had not. Few appreciated that much of the vaccine used, especially in endemic coun- tries, was of low potency, and that the failure THE SIGNIFICANCE OF SMALLPOX of a first attempt often resulted in a second IN NON-ENDEMIC COUNTRIES vaccination with equally poor vaccine. How- ever, certificates did not require that the Two aspects of smallpox in non-endemic results of a second primary vaccination should countries were relevant to the global strategy be examined. of smallpox eradication : the actions taken by The principal value of vaccination certifi- the countries themselves and those taken by cates probably lay in encouraging most tra- WHO. vellers to be vaccinated before they left their own country. Most intercontinental travellers were from non-endemic countries, and al- Actions Taken by the Non-endemic though they were in fact responsible for the Countries majority of importations into European countries (see the next section), the number of Before about 1970, almost all industrialized incidents might have been much higher had countries regularly vaccinated a large propor- there been no requirement for vaccination tion o€ their population and enforced the certificates. requirement stipulated in the International Health Regulations that international trav- Control of outbreaks ellers should hold valid certificates of vacci- nation. These measures were pursued with In accordance with the philosophy of varying degrees of diligence in different smallpox control then prevalent (see Chapter countries. In the USA, for example, most 9), industrialized countries in the 1950s and children were required to show evidence of early 1960s usually responded to the discovery vaccination at school entry and the vaccina- of an importation of smallpox by mounting a tion rate in the population as a whole large vaccination campaign, in parallel with exceeded 95O& In the United Kingdom efforts to identify contacts and vaccinate and vaccination was encouraged but not enforced, isolate them.