The eradication of smallpox in Shanghai, China, October 1950—July 1951

Bulletin of the World Health Organization, 59 (6): 913-917 (1981) The eradication of smallpox in Shanghai, China, October 1950-July 1951 Xu Hui' & JIANG YUTU2 Smallpox (variola major) was endemic in China for thousands of years until it was finally eradicatedfrom the country in the early 1960s. The strategy and tactics of the eradi- cation campaign in Shanghai, the largest city and major communications centre in China, were typical of those employed throughout China, but had some additional features of interest. The decision to eradicate smallpox was made in 1950 and three preparatory steps were taken immediately: supplies ofpotent (liquid) vaccine were assured; popular support was enlisted by intensive propaganda; and teams of vaccinators were trained. In Shanghai, the mass vaccination campaign began in October 1950, at a time when a smallpox epidemic was raging in the city. The last case ofsmallpox in the city was recorded in July 1951. A special feature of the campaign in Shanghai was the introduction ofa national vaccination certifi- cate to prevent export ofsmallpoxfrom the city by the 2 800 000persons who moved in and out of Shanghai each week by rail, bus, or boat. Eradication wasfollowed up by aprogramme of vaccination ofall infants, with revac- cination at 6, 12, and 18 years ofage, and mass vaccination campaigns in 1963, 1968, 1972, and 1978. The number of adverse reactions to vaccination was small andfell progressively from an overallfigure of 8.4 per 100 000 in 1963 to 2.5 per 100 000 in 1978. Vaccination requirements were relaxed in 1978, but smallpox vaccination is still offered to children as part of the immunization programme. Smallpox (variola major) was introduced into China from the south-west in the first century A.D., and was endemic from that time until it was eradicated from the country in the early 1960s. Variolation had been practised in China since the Sung dynasty (1023 - 55), and vaccination was started on a limited scale in 1803, but until 1951 the disease continued to cause much illness and death. Immediately after the establishment of the People's Republic in 1949, vaccine production facilities were set up to cover the whole country, and in October 1950 the government announced its goal of eradicating smallpox by vacci- nation of the whole population. The present report describes the eradication of smallpox in Shanghai, the largest city and major communications centre of China. Vice-Director, Shanghai Municipal Health and Epidemio- logical Station, Shanghai, China. 2 Professor of Epidemiology, Institute of Epidemiology and Microbiology, Academy of Military Medical Sciences, Beijing, China. Requests for reprints should be addressed to this author. THE MUNICIPALITY OF SHANGHAI Shanghai, one of the three centrally administered cities of China, consists of 10 counties and 10 urban districts, with a total area of 6185 km2 and a current population (1980) of just over 11 million. It has long been the main port of China and was a major centre of conflict in the war against Japan and in the subsequent struggle against the Kuomintang between 1945 and 1949. When it was finally liberated in May 1949, its pre-war population of 1.2 million had grown to 5.4 million, largely because of the influx of refugees from surrounding districts. At the time of the smallpox eradication campaign, which took place from October 1950 to July 1951, the Shanghai municipality comprised 20 urban and 9 suburban districts. Although international shipping was restricted in the years immediately after 1949, there was a great deal of internal coastal and river boat movement through the port of Shanghai. In addition, the city had major rail and road links with other parts of the 4134 91 3- 914 H. XU & Y. T. JIANG country, centred on one railway station and a few long distance bus stations for the Shanghai - Nanjing and Shanghai - Hangchow highways. At the time of the eradication campaign, approximately 2 800 000 travellers entered or left Shanghai each week. THE SMALLPOX ERADICATION PROGRAMME Background As in other endemic areas, both mortality and morbidity from smallpox were grossly underreported, especially during the Japanese occupation of the city between 1942 and 1945. Nevertheless, the figures available for the period 1930- 51 indicate that, although the disease was always present, there were epidemic episodes during the periods 1930- 34, 1936 - 39, 1946 - 48, and in 1950 when the eradication campaign began. Smallpox was mainly a disease of childhood, with mortality rates highest in children less than five years old. There was a marked seasonal variation in the number of cases of smallpox, with a high incidence in winter and spring (December - May) and a low inci- dence in summer and autumn (August - November). During the period prior to the war with the Jap- anese, both vaccination and variolation were prac- tised in Shanghai (1), but both were expensive and few of the poorer people were inoculated. Variolation was banned long before 1949 and, until 1951, overall vaccination rates were low (Table 1). The decision to eradicate smallpox in China was promulgated in October 1950 by the state council of the central government, in a "Notice on the Cam- paigns for Smallpox Vaccination of Autumn 1950". The vaccination campaign itself was preceded by a massive propaganda campaign to enlist the support of the whole population, and the training of large numbers of vaccination teams. Table 1. Smallpox vaccination rates in Shanghai, 1946 - 51 No. of persons Vaccination Year Population vaccinated rate 1%) 1946 3 536 209 536 573 15.2 1947 3 925 621 2 251 096 57.3 1948 5 204 321 2 464 381 47.4 1949 5 406 644 1 447 609 26.8 1950 5 063 818 2 232 340 44.1 1951 5 333 036 6 925 363w 129.9a Includes visitors, travellers, and persons vaccinated more than once. The mass vaccination campaign of 1951 Throughout China, the Temple of Heaven strain of vaccinia, prepared in calves and glycerinated, was used as a liquid vaccine. Smallpox vaccination was free and compulsory for all except those with contra- indications. The aim of the campaign in Shanghai was to vac- cinate 95%1o of the population in the shortest possible time. In order to accomplish this, 6944 medical and paramedical personnel were organized into 1319 per- manent stations and 1836 mobile vaccination teams. The personnel, comprising 3173 traditional Chinese medical doctors, 2067 doctors of western medicine, 455 nurses and midwives, 1126 medical students, and 123 others, were given a short training in order to standardize the vaccination technique. The mass vaccination campaign began in March 1951, when an epidemic of smallpox was raging in Shanghai. As the number of vaccinations rose, the incidence of smallpox fell (Table 2), and the last case in Shanghai was reported on 26 July 1951. Table 2. The cumulative vaccination rate and the inci- dence of smallpox in Shanghai in 1951 Cumulative No. of reported Month vaccination rate 1%) smallpox cases January 11 .5 958 February 19.1 646 March 88.1 722 April 108.0 325 May 110.3 55 June 110.4 18 July 110.5 10 August 110.6 0 An important feature of the Shanghai campaign was the need to prevent the movement of persons suffering from smallpox into or out of the city. Special measures were adopted by the Health Bureau of the Shanghai Railway Offices and by the Quarantine Service of Shanghai Harbour to deal with all travellers and with boat dwellers on the Huangpu River. All travellers had to show a certificate ofvaccination or be vaccinated before they were allowed to board a boat, train, or long-distance bus. Ships' crews were mobil- ized as "health groups", and between January and July 1951, 35 smallpox cases were recognized among 355 986 boat passengers. Thus, in spite of the severe epidemic of smallpox in Shanghai in 1951, there were no outbreaks elsewhere in China originating from cases in Shanghai. ERADICATION OF SMALLPOX IN SHANGHAI 915 Table 3. Smallpox vaccination rates during mass vaccination campaigns in Shanghai No. of persons Vaccination rate (%) in whom vaccination was indicated No. of persons for whole forthose Year Population (age 1 - 55 years) vaccinated population indicated 1963 10 647 000 6 217 987 5 173 365 48.6 83.2 1972 10665050 8991 802 7580089 71.1 84.3 1978 10 923 759 8 458 607 6 376 908 58.4 75.4 Follow-up measures Various follow-up measures were applied in order to prevent the reappearance of smallpox. Beginning early in 1953, compulsory vaccination against small- pox was given to all infants at age two months, with revaccination at 6, 12, and 18 years of age. In addition, over the last 30 years, mass smallpox vacci- nation campaigns have been organized every 4-6 years, and were carried out in Shanghai in the years 1963, 1968, 1972, and 1978 (Table 3). Because of the global eradication of smallpox, the vaccination regu- lations were changed late in 1978. Primary vacci- nation is still required for one-year-old children, but further vaccination at 6 and 18 years of age is no longer compulsory.' Vaccinators were specially trained for each of the mass vaccination campaigns, and the take rates and vaccination reactions were examined regularly in groups of vaccinees of different ages and occupations. Vaccination reactions were examined on the third and the seventh days (Table 4). Over one quarter of those tested in 1951 gave a primary reaction, but the level fell substantially in a In August 1981, China officially informed WHO that routine smallpox vaccination was no longer obligatory. However, vacci- nation will be ended completely only after widespread health education activities. subsequent years because of the high vaccination rate that had been established. In 1963 and 1978, there was no take in very few unvaccinated individuals (0.1 07o and 0.20o) and in a slightly higher proportion of those previously vaccinated (2.30o and 1.40%o) (Table 5). About 30%o of those previously vaccinated had an immediate reaction. Surveillance for possible cases of smallpox was maintained through a system of reporting notifiable diseases including smallpox, chickenpox, and measles. All cases of suspected smallpox, of which there were about five each year in Shanghai between 1951 and 1966, were subjected to intensive epidemio- logical and virological investigation, but none of these was confirmed after 1951. Adverse reactions to vaccination Few adverse reactions were noted, in agreement with results from other areas (2). Table 6 sets out the adverse reactions observed during the mass vacci- nation campaigns carried out in 1963, 1972, and 1978. Post-vaccinial encephalitis was extremely rare, there being only 5 cases in nearly 18 million vaccinations. The complications observed after primary and follow-up vaccination were recorded for 1978, but not for other years. All complications except purpura Table 4. Vaccination reactions determined on selected samples of the population Successful vaccination' No take No. of persons Primary Year examined No. % reaction % No. % 1951 312 319 293 536 94.0 79 690 25.5 18 783 6.0 1955 4 797 4 647 96.9 298 6.3 150 3.1 1959 13688 12464 91.1 851 6.2 1 224 8.9 1963 13 863 13 526 97.6 572 4.1 337 2.4 1972 9 822 9 723 99.0 310 3.2 99 1.0 1978 16911 16629 98.3 1 022 6.2 282 1.7 a Includes primary, accelerated, and immediate reactions. 916 H. XU & Y. T. JIANG Table 5. Reactions after primary and follow-up vaccination, 1963 and 1978 Primary or accelerated No. of reaction Immediate reaction No take persons Year examined No. % No. % No. % 1963 13 863 Primary vaccination 119 0.9 0 - 20 0.1 Revaccination 9 126 65.8 4281 30.9 317 2.3 1978 16 911 Primary vaccination 217 1.3 0 - 37 0.2 Revaccination 11 416 67.5 4996 29.5 245 1.4 were much more common after primary vaccination, was sufficiently intensive and effective to break the the overall rates being 39.84 and 2.11 per 100 000 chains of transmission. Subsequently the immune primary and follow-up vaccinations respectively. status of the population was maintained by regular primary vaccination of newborn children, with revac- cinations at 6, 12, and 18 years, allied with periodical DISCUSSION mass vaccination campaigns covering the entire popu-lation. During recent years, the requirement for vacci- nation has been considerably relaxed, and exemption Smallpox was eliminated in most formerly endemic has been given on the grounds of eczema, intercurrent countries by mass vaccination followed by surveil- infection, etc. However, mothers still request vacci- lance and containment, the last being regarded as the nation of newborn children and this is provided, even most important component (3). This report indicates though there is now no risk of smallpox infection. that mass vaccination was successful in eliminating A novel feature of the campaign in Shanghai was smallpox from Shanghai. Elsewhere in China, surveil- the need to prevent spread of the disease from this lance and containment were important only in the major communication centre to other parts of the border regions of Yunnan and Tibet; for the country country, which was achieved by requiring vaccination as a whole, mass vaccination, using liquid vaccine, certificates for all travellers moving outside the city. Table 6. Complications of smallpox vaccination 1978 Primary Diagnosis 1963 1972 vaccination Revaccination Total Total Rate per Rate per Rate per Rate per Rate per Rate per No. 100 000 No. 100 000 No. 100 000 No. 100 000 No. 100 000 No. 100 000 Postvaccinial encephalitis 3 0.08 2 0.03 0 0 0 0 0 0 5 0.03 Vaccinia necrosum 7 0.18 2 0.03 0 0 0 0 0 0 9 0.05 Eczema vaccinatum 2 0.05 7 0.10 4 4.31 2 0.03 6 0.09 15 0.08 Generalized vaccinia 17 0.43 12 0.17 1 1.08 0 0 1 0.01 30 0.17 Vaccinia multiforme° 243 6.19 91 1.29 15 16.15 88 1.36 103 1.57 437 2.45 Vesicular multi- forme rashb No data 48 0.68 5 5.30 2 0.03 7 0.11 55 0.40 Purpura 3 0.08 8 0.11 0 0 3 0.05 3 0.05 14 0.08 Accidental infection 54 1.38 73 1.04 12 12.92 41 0.63 53 0.81 178 1.00 Total 329 8.41 243 3.44 37 39.84 136 2.11 173 2.52 743 4.17 a Mild generalized vaccinia. b Mild generalized vaccinia with vesicular rash. ERADICATION OF SMALLPOX IN SHANGHAI 917 ACKNOWLEDGEMENTS The authors are indebted to Professor F. Fenner, John Curtin School of Medical Research, Canberra, Australia, Dr I. Arita, Smallpox Eradication Unit, World Health Organization, Geneva, Switzerland, and Dr J. Breman, Centers for Disease Control, Atlanta, GA, USA, for their encouragement and advice in the writing of this paper. RESUME ERADICATION DE LA VARIOLE A SHANGHAI, CHINE, OCTOBRE 1950- JUILLET 1951 La variole a e endemique en Chine pendant des mille- naires jusqu'a ce qu'elle soit finalement eradiquee dans l'ensemble du pays au debut des annees 1960. Le present rapport decrit la strategie et la tactique de la campagne d'eradication qui a et menee a Shanghai, la plus grande ville et le principal centre de communications de la Chine. C'est en 1950 qu'il a e decide d'eradiquer la variole et trois mesures pr6paratoires ont e imm6diatement prises: des approvisionnements en vaccin actif (liquide) ont e assures, le soutien populaire a e obtenu par une propa- gande intensive et des equipes de vaccinateurs ont e formees. A Shanghai, la campagne de vaccination de masse a commence en octobre 1950, a un moment oui une epidemie de variole faisait rage dans la ville. Le dernier cas de variole a et enregistre en juillet 1951. La vaccination a e effectuee par un total de 6944 vacci- nateurs, organises en 1319 equipes fixes et 1836 equipes mobiles. Au cours de l'annee 1951, 6 925 363 personnes ont et vaccinees, chiffre qui depassait celui de la population de la ville a ce moment parce qu'il comprenait de nombreux voyageurs. Un caractere particulier de la campagne realis6e a Shanghai a et 1'1aboration d'une procedure de ocertificat national de vaccination>> destinee a empecher que la variole ne soit exportee par les 2 800 000 personnes qui penetraient A Shanghai ou en sortaient chaque semaine par le rail, la route ou l'eau. Trente-cinq cas de variole ont et diagnosti- ques durant la premiere moitie de 1951 parmi les 356 986 personnes qui ont voyage par bateau au cours de cette annee. 11 y a eu environ cinq cas suspects de variole par an pendant les quelques annees qui ont suivi la vaccination. Chacun a e soumis A un examen epidemiologique et viro- logique approfondi et tous se sont reveles negatifs. L'eradication a et suivie par un programme assurant la vaccination de tous les nourrissons, la revaccination des enfants aux Ages de 6, 12 et 18 ans et des campagnes de vacci- nation de masse en 1963, 1968, 1972 et 1978. Le nombre de reactions adverses A la vaccination a e faible et en general s'est abaisse progressivement d'un taux global de 8,4 pour 100 000 en 1963 A 2,5 pour 100 000 en 1978. Les reactions vaccinales etaient beaucoup plus frequentes apres la vacci- nation primaire (40,91 pour 100 000) qu'apres revaccination (2,18 pour 100 000). Les exigences relatives A la vaccination ont e encore assouplies vers la fin de 1978, mais la vacci- nation antivariolique reste encore offerte aux enfants dans le cadre du programme de vaccination. REFERENCES 1. TAO, C. S. A study of the smallpox prevalence and inoculation data in some districts of Kiangsu Province. In: Transactions of the Ninth Congress of the Far East Association of Tropical Medicine, Nanjing, 1934, Nanjing, 1935, pp. 499 - 501. 2. LANE, J. M. ET AL. Complications of smallpox vacci- nation, 1968. National surveillance in the United States. New England journal of medicine, 281: 1201 - 1208 (1969). 3. The global eradication ofsmallpox. Final report of the Global Commission for the Certification of Smallpox Eradication. Geneva, World Health Organization, 1980.