Epidemiological events surrounding a paralytic case of poliomyelitis in Sweden

Bulletin of the World Health Organization, 57 (1): 99-103 (1979) Epidemiological events surrounding a paralytic case of poliomyelitis in Sweden M. BOTTIGER,1 P. MELLIN,2 V. ROMANUS,3 H. SODERSTROM,4 T. WESSLEN,5 & G. VON ZEIPEL6 A case of clinical poliomyelitis occurred in Sweden in January 1977; it was the first indigenous case in Sweden since 1962. This incident was ofparticular interest as it provided an opportunity to study the spread of virus in a cluster of unvaccinated persons and in individuals more or less fully vaccinated with inactivated vaccine. The patient excreted wild type 2 virus and the same type was isolated from 25 other individuals, all of whom were close contacts of virus excretors. Among the close contacts, 14 of 20 unvaccinated preschool children were found to excrete virus, but excretion was not found in any of the 7 vaccinated children examined. The first indigenous case of paralytic polimyelitis in Sweden since 1962 occurred in January 1977. A 2-year-old unvaccinated girl became paralysed on on 28 January; the diagnosis was confirmed on 9 February when poliovirus type 2 was isolated. The girl's family belonged to a sect whose members refrain from vaccination. The epidemiological consequences of this case were of particular interest since a generation of children had grown up in Sweden who had been vaccinated with killed vaccine only. This case also offered a unique opportunity to study the possible spread of virus among both parenterally vaccinated and unvaccinated persons. EPIDEMIOLOGICAL INVESTIGATIONS Family The family of the patient consisted of father, mother, and a 4-year-old brother. The father, who is Dutch, had spent 3 months in the Netherlands but had returned to Sweden on the 13 December 1976. Two German students had stayed with them until Christmas. The mother had been vaccinated against poliomyelitis with the Swedish killed vaccine; the father was probably not vaccinated and the two 1 National Epidemiologist, The National Bacteriological Laboratory, 105 21 Stockholm, Sweden. 'Physician, Delsbo, Sweden. 'National Bacteriological Laboratory, Stockholm, Sweden. 'Physician, Sodertalje, Sweden. Central Microbiological Laboratory, Stockholm, Sweden. children had not received any vaccination. The mother and the two children had had chills and diarrhoea in January. Index family contacts About 50 primary contacts were identified and stool samples were examined. On 13 February 1977 the brother of the index case was confirmed as a virus excretor. In addition to the patient and her brother, the investigation showed 3 adults and 7 children to be excretors of the virus. Among them there was one girl who on 11 February had been ill with fever, irritability, and ataxia lasting for about 2 days. A second round of investigations was undertaken of the contacts of the excretors revealed during the primary study. The members of one of the virus- excreting families ran the preschool kindergarten of the sect in their own house, a fact that widened the group of contacts. Two of the excretors were school- mates at a private school run by the sect. In view of the fact that 64 of the 130 schoolchildren were unvaccinated it was decided to include the school in the virological investigations. The majority of the contacts were followers of the sect. The social activities of the members were intense and the number of contacts was higher than among Swedes in general. The second investigation disclosed virus excretion by 3 adults and 3 children. They all lived in an isolated village in the central part of Sweden and none of them had been ill. A third group was also included in the investiga- tions, i.e., contacts, comprising children and students, 3778 - 99 M. BOTTIGER ET AL. in a neighbouring village. Well-baby clinic visitors, children's party visitors, and close contacts of the last detected excretors were also investigated. Among the close contacts, 2 adults and 5 children were found to excrete poliovirus type 2. Finally, an unvaccinated Danish lady became infected: she cared for the children of the family that ran the kindergarten after they had returned home from isolation in hospital. Measures to prevent spread of virus As the spread of virus in the community could not be predicted, measures were undertaken to limit the spread from excretors and suspected excretors. All virus-excreting families and suspected families (before the laboratory results were available) were recommended to restrict their movements. RESULTS Faecal investigations The number of persons investigated in relation to age and type of contact is shown in Table 1. The individuals were roughly divided into 3 groups according to their contact pattern with known virus excretors. Group I consists of close contacts of infected families. The families (or one excreting fami- ly member) had lived in one another's homes from one to several days. Group II includes other contacts, such as nurses in the hospital, kindergarten compan- ions, members contacted at courses, short-term visitors, etc. Group III comprises all persons who had had no certain contact with excretors, including most of the schoolchildren, a number of students at the college, and employees and inmates at a number of homes run by members of the sect. Excretors were found only among the very close contacts (Group I). The approximate age of the individuals included in Group I is shown in Table 2, Table 1. Age distribution of 676 persons investigated for virus excretion, by degree of contact Age group (years) Group Total <1 1-2 3-6 7-14 >15 I. Close contacts 5 11 12 6 37 71 II. Other contacts 24 1 2 44 18 i11 209 Ill. No known contact 10 30 44 134 178 396 Age. Febr. | March | April >15 7-14 3-6 <3 Fig. 1. Periods during which individuals of different ages (years) excreted poliovirus. Solid lines = un- vaccinated persons; dashed lines = persons who claimed to have received one or more injection of poliomyelitis vaccine. which also gives the number of verified excretors and the vaccination histories. Virus excretors were found in 10 of 17 families with close connexions. All infected families had unvaccinated children 3 years old or younger. Among the 7 families without excretors, 3 consisted only of adults but the other 4 included young unvaccinated children. Enterovirus other than poliovirus type 2 was isolated from only 1 child who had recently received oral poliomyelitis vaccine in Norway. Relation between virus excretion, age, and vaccination history The periods during which virus was isolated from the faeces are illustrated in Fig. 1. Samples were collected weekly. After 1 or usually 2 negative tests the sampling was discontinued. The results indicate that the younger children excreted virus for longer periods than the adults. Six unvaccinated children excreted virus for several months. - _ _l ll * - - - | w 1 |~~~~I T | l l | 100 -4 1) -4 __ -4 -4 I.. -.4 .__ -.4 -0 i ------------ -4 PARALYTIC CASE OF POLIOMYELITIS IN SWEDEN Table 2. Number of persons of Group 1 (close contacts) positive and negative for virus excretion according to age, vaccination status, and type of family (with or without excretors) Age group Unvaccinated Vaccinated (years) Pos. Neg. Pos. Neg. Infected families <3 9 2 0 1 3-6 5 1 0 2 7-14 1 0 2a 3 > 15 3 1 6a 12 Noninfected families <3 0 2 0 2 3-6 0 2 0 2 7-14 0 0 0 0 >15 0 4 0 11 a Two vaccinated adult excretors had probably received 4 or 5 injections; the other vaccinated excretors had not received the recommended number of injections. The data in Table 2 show that none of the 14 younger excretors (<7 years) was vaccinated. The 7 vaccinated youngsters were all negative. Among the 12 older excretors (>7 years) 2 claimed to be vaccinated according to the recommended schedule, 6 were incompletely vaccinated, and 4 unvaccinated. Vaccination histories of others in the community Vaccination histories were taken from schoolmates both in the sect's private school and the ordinary municipal schools. As mentioned above, 64 of 130 investigated pupils of the private school had not received any vaccination. In the municipal schools 4 out of 1400 pupils were found to be unvaccinated. Among the preschool sect children, 7 of 20 had not been vaccinated. Antibody titrations on sera collected from school- children The sera of vaccinated and unvaccinated school- children and some of their families were tested for antibodies against all three types of poliovirus at a serum dilution of 1: 4 by means of a conventional neutralization test (1). The results showed that all except 10 of the 74 unvaccinated children tested lacked antibodies to all three types of poliovirus. The 42 vaccinated children tested were all triple- positive. Virus isolation tests of sewage Poliovirus type 2 was readily isolated from several sewage plants and sewage outlets by means of a selective isolation method (2). Virus was isolated from sewage systems that served areas further afield where no known excretors lived (Table 3). In March, the same type of virus was isolated also from one of the main sewage plants of Stockholm. Genetic studies of isolates Ten isolates from 6 excretors, including the patient, and 4 sewage samples were tested at the Center for Disease Control, Atlanta, GA, USA.a a By Dr A. Hatch. Table 3. Results of virological investigations in different sewers Sampling place February March April May Centre of village Poliovirus 2 Poliovirus 2 - Poliovirus 2 Eastern part of village Poliovirus 2 Negative - CPA,a not poliovirus Seminary Negative Poliovirus 2 - Poliovirus 2 Teachers' residential area Poliovirus 2 Poliovirus 2 - Poliovirus 2 School Negative Poliovirus 2 - Poliovirus 2 Western part of village Coxsackievirus - Nearest town CPA,a not poliovirus - Poliovirus 3 Northern part of village - Poliovirus 2 North-east Stockholm - Poliovirus 2 - Poliovirus 2 a CPA = cythopathic agent. 101 M. BOTTIGER ET AL. It was confirmed that they behaved like a wild strain when tested for the rct-marker and the McBride sero-marker (3, 4). DISCUSSION The epidemiological consequences of the first indigenous case of poliomyelitis in Sweden since 1962 are of special interest. A generation of children have grown up since vaccination against polio- myelitis started in this country and they rely entirely upon the immunity induced by killed vaccine. This case also offered a unique opportunity to study the possible spread of virus among both parenterally vaccinated and unvaccinated persons. When evaluating the results of these investigations it should be borne in mind that the case was caused by poliovirus type 2. Wild strains of this type have been shown to be less neurovirulent than the other two types of poliovirus (5). Also it is the type that is the most immunogenic in the Swedish polio- myelitis vaccine (1, 6). It never fails to induce anti- bodies. The results showed that both age and vaccination status were factors influencing the spread of virus. All infected families had small unvaccinated children. It was remarkable that none of the vaccinated children less than 7 years of age excreted the virus. This stands in contrast to the adult excretors among whom there were both vaccinated and unvaccinated individuals. This suggests that the vaccine-induced immunity prevents the transmission of virus at least during the first years of life, when children are very apt to spread infections, and thus might explain the interruption of poliovirus circulation in Sweden following the introduction of vaccination. Another aspect of the mechanism of spread of polioviruses and several other enteroviruses has also been discussed during the last years. In countries where the hygienic conditions are comparatively high it has been suggested that polioviruses and several other enteroviruses are spread via the oral- oral route and not the faecal-oral route (7). Little is known, however, about the resistance to polioviruses in the different parts of the intestinal tract after parenteral immunization. It is well known that much higher serum antibody levels are induced by killed than by live vaccine (8, 9). Possibly the serum antibodies penetrate the mucous tissue of the pharynx better than that of the gut; also the enzymes are dif- erent in the two sites. Investigations have thus shown that after challenge with live poliomyelitis vaccine, children previously parenterally immunized excrete much less virus in saliva than in faeces (10, 11). The studies of virus in sewage indicated that the virus was probably circulating widely in the com- munity and not restricted to the excretors detected in these studies. In the village where the patient lived, there was frequent exchange of students and teachers from all over Europe and viruses could have been introduced in this way. It was also discovered that several members of the sect believed in " live " vaccine, rather than something " killed ", and had recently been immunized orally abroad. The strains isolated, however, were not " vaccine- like " and thus were probably not derived from these vaccinees. Having in mind the tragedies caused by poliovirus type 1 in unvaccinated population clusters in Stap- horst, Netherlands (12), and in a Christian Science school in Connecticut, USA (13), the measures taken in the present incident to prevent the spread of virus were fairly rigorous. No further paralytic case occurred-probably because the type 2 strain was of comparatively low neurovirulence and the immunity in the surrounding population, was in general good. This incident, however, underlines the risks of unvaccinated " pockets " in an otherwise well- vaccinated population, in which natural circulation of virus has ceased and no " so-called " natural immunization takes place. The longer the un- vaccinated group persists the more dangerous will the situation be for them in view of the increasing risks of paralytic forms of poliomyelitis at older age (14). SUMt OBSERVATIONS EPIDEMIOLOGIQUES FAITES A L OCCASION D UN CAS DE POLIOMYELITE PARALYTIQUE EN SUtDE Un cas indigene de poliomy6lite, le premier a etre enregistr6 officiellement depuis 1962, est survenu en Suede en janvier 1977. Le virus a l'origine de ce cas a e identifi6 comme etant le poliovirus du type 2. La maladie a frappe une fillette de 2 ans non vaccinee dont les parents faisaient partie d'une secte hostile aux vaccinations. 102 PARALYTIC CASE OF POLIOMYELITIS IN SWEDEN 103 L'enfant etait donc entouree d'un groupe de personnes non vaccinees. On a examine au total 676 personnes en vue de deceler toute excretion de virus, et les eaux usees ont egalement ete soumises a des epreuves d'isolement de virus. En outre, des titrages d'anticorps ont ete operes sur un certain nombre d'enfants d'age scolaire et pr6- scolaire. Les personnes soumises 'a 1'enquete ont et6 divis&es en trois groupes: les contacts familiaux imme- diats des sujets excr6teurs de virus (groupe I), les autres contacts de ces excreteurs (groupe II) et les individus n'ayant pas eu avec eux de contacts etablis de maniere precise (groupe II1). Le groupe I comprenait 71 personnes appartenant a 17 familles. Des excr6teurs, au nombre de 26, ont 6te trouv6s dans 10 familles et celles-ci comptaient toutes des enfants d'age prescolaire. Deux excreteurs adultes ont declare avoir requ 1'ensemble des injections prescrites pour la vaccination. Parmi les enfants d'age prescolaire appartenant au groupe I, 14 excreteurs ont ete d6tectes sur les 21 enfants non vaccines alors qu'aucun des 7 enfants vaccin6s n'a ete trouve positif (tableau 2). On n'a pas decele d'excr6tion de virus chez les 209 contacts du groupe II ni chez les 396 individus (principalement des enfants et des etudiants) du groupe III. Nombre des epreuves pratiquees sur les eaux usees ont donn6 des resultats positifs, meme lorsque celles-ci provenaient de regions voisines oiu l'on n'avait pas depist6 d'excreteurs. Le virus du type 2 isole chez les excreteurs et dans les echantillons d'eaux us6es a ete identifie comme appartenant a une souche * sauvage *. L'examen serologique effectue chez les enfants d'age pr6scolaire et scolaire a montre qu'aucun des 74 enfants non vaccines soumis A 1'epreuve ne possedait d'anticorps contre les poliovirus des types 1 et 2. Des anticorps contre le poliovirus du type 3 ont toutefois ete deceles chez 10 de ces enfants. Quant aux 42 enfants vaccines qui ont ete examines, ils possedaient tous des anticorps contre les virus des trois types. II a paru particuliere- ment interessant d'avoir pu constater que tous les enfants d'age prescolaire qui avaient ete vaccines par voie parent6rale etaient, sur la foi de ces epreuves, immunises contre l'infection virale. La pr6sente etude met en lumiere le danger que repre- sente tout groupe non vaccine au sein d'une population bien protegee dans son ensemble. Si le risque d'infection peut etre considere comme tres limite, les consequences d'une telle infection peuvent etre desastreuses. REFERENCES 1. BbTTIGER, M. ET AL. The immune response to vaccina- tion with inactivated poliovirus vaccine in Sweden. Acta pathologica et microbiologica scandinavica, 66: 239-256 (1966). 2. BbTrIGER, M. Isolation of viruses from sewage, with special regard to poliovirus: an evaluation of the sensitivity of three tissue culture methods. Bulletin ofthe World Health Organization, 56: 937-943 (1978). 3. SABIN, A. B. Reproductive capacity of polioviruses of diverse origins at various temperatures. Perspec- tives in virology II, p. 90, 1960. 4. McBRIDE, W. D. Antigenic analysis of polioviruses by kinetic studies of serum neutralization. Virology, 7: 45-58 (1959). 5. HORSFALL, F. L. & TAMM, I., ED., Viral and rickettsial infections of man. London, Pitman Medical, 1965, p. 452. 6. BOTrIGER, M. Follow-up studies after vaccination with inactivated poliovaccines. In: Proceedings of the IXth Symposium of the European Association Against Poliomyelitis and Allied Diseases, Stockholm, 1962, Brussels, European Association Against Poliomyelitis and Allied Diseases, 1963, pp. 156- 158. 7. SALK, J. & SALK, D. Control of influenza and polio- myelitis with killed virus vaccines. Science, 195: 834-847 (1977). 8. B6TrIGER, M. Studies on immunization with inactived and live poliovirus vaccines. Acta paediatrica scandi- navica, Suppl. 164, p. 14, 1966. 9. BEALE, A. J. Discussion following paper presented by M. Bottiger & L. Aro. In: Proceedings of the XIth Symposium of the European Association Against Poliomyelitis and Allied Diseases, Rome, October 1966, Brussels, European Association Against Polio- myelitis and Allied Diseases Vol. XI, 1967, p. 141. 10. B6TTIGER, M. ET AL. Vaccination with attenuated Type 1 poliovirus, the Chat strain. II. Transmission of virus in relation to age. Acta paediatrica scandi- navica, 55: 416-421 (1966). 11. GALBRAITH, N. S. A survey of poliovirus excretion in normal children in England and Wales 1961-62. In: Proceedings ofthe Xth Symposium ofthe European Association Against Poliomyelitis and Allied Diseases, Warsaw, October 1964., Brussels, European Associa- tion Against Poliomyelitis and Allied Diseases, pp. 119-127. 12. Poliomyelitis in 1971. Weekly Epidemiological Record, 47: 293-299 (1972). 13. Neurotropic viral diseases surveillance. Poliomyelitis, Annual summary-1972, Atlanta, GA, USA, Center for Disease Control, US Department of Health, Education, and Welfare, 1974, p. 9. 14. OLIN, G. & WESSLEN, T. Seroimmune patterns for poliomyelitis in Sweden. Archiv far die gesainte Virusforschung, 7: 191-205 (1957).