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Polio Eradication: Surveillance Implications for the United Kingdom

D. M. Salisbury, M. E. Ramsay, J. M. White, and D. W. Brown
Department of Health, Communicable Disease Surveillance Centre, Virus Reference Division, Public Health Laboratory Service, London, United Kingdom

The requirements for certification of elimination of wild virus poliomyelitis will pose particular problems for some industrialized countries, such as the United Kingdom, where there has been no case detected for at least a decade. Systems of surveillance of poliomyelitis have been reviewed and potential weaknesses identified. When oral polio vaccine is routinely used, the rate of vaccineassociated cases provides an indication of the likelihood that if they occurred, wild virus cases would be detected. Acute flaccid paralysis surveillance was done for 3 years, but rates were lower than reported elsewhere and were accepted for certification purposes. Alternative techniques, such as surveillance of polioviruses, either in clinical samples or from the environment, may be developed in such countries. The ability to identify enteroviruses and to distinguish between wild and vaccine strains of polioviruses will give assurance that silent transmission of wild viruses is unlikely.
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In 1988, the World Health Assembly announced the goal of the global eradication of poliomyelitis by the year 2000. This declaration took into account the experiences and benefits of the successful global eradication of smallpox, certified by an international commission in 1979, and was considered technically feasible: Polio has no known animal reservoir, the virus does not survive for long in the environment, and effective vaccines are readily available. The key to the eradication of smallpox was the use of surveillance to focus immunization activities; however, the requirements for surveillance for polio are even more demanding. Poliovirus infection may be inapparent. For each clinically recognized poliovirus paralytic case, there may be between 60 and 1000 inapparent infections [1, 2]. Smallpox immunization was stopped in 1971 in the United Kingdom (UK), 8 years before global eradication [3]. Because of the risk of large epidemics among unimmunized persons following an importation, polio immunization cannot be stopped in anyone country until all countries have convincingly eradicated the wild virus. The model for the global eradication of polio was developed in the Region of the Americas. There, in 1985, the Directing Council of the Pan American Health Organization (PAHa) committed the region to polio elimination by 1990 [4]. The strategy that was used depended on routine polio immunization activities, supplemented by annual national immunization days. All children under 5 years were given two doses of oral polio vaccine, a month apart, with "mop-up" immunization in the local populations following probable cases or in areas where cases were thought still to be occurring.

At the same time that augmented immunization activities were being implemented, new surveillance systems were being developed. In order to have the highest probability of detecting any cases of poliomyelitis, all cases of acute flaccid paralysis (AFP) in children < 15 years old (later reduced to children <6) were to be investigated and reported to PAHO. Two stool samples were required from each AFP case, as well as 1 stool sample from each of 5 childhood contacts of the case-patient. The samples were sent to accredited reference laboratories where they were tested for polioviruses. This process allowed the development of the following sensitive performance indicators for the surveillance [5]: At least 80% of reporting sites should report weekly; the rate of AFP cases reported should be ---1.0/100,000 population < 15 years of age; ~80% of all AFP cases reported should be investigated within 48 h of reporting; ~ 80% of all AFP cases reported should have 2 stool specimens taken for virus culture within 2 weeks of paralysis onset; and ~ 80% of all AFP cases reported should have stool investigations of at least 5 contacts. On 23 August 1991, a 2-year-old Peruvian boy, Luis Fermin Tenorio Cortez, was the last person reported to have poliomyelitis in the Americas. In September 1994, an international commission declared that there had been no single case of wild virus poliomyelitis in the Americas for 3 years and, based on the evidence of the surveillance from every country in the Americas, the commission was convinced that poliovirus transmission had been interrupted [6]. Despite the eradication of polio from the region, immunization activities must continue unabated until all countries worldwide have eliminated poliomyelitis.

The opinions expressed herein are those of the authors, rather than the Department of Health and the Public Health Laboratory Service. Reprints or correspondence: Dr. D. M. Salisbury, Department of Health, 707 Wellington House, 133-155 Waterloo Rd., London SE1 8UG, UK.
The Journal of Infectious Diseases 1997; 175(8uppl 1):8156-9 1997 by The University of Chicago. All rights reserved. 0022-1899/97/7581-0027$01.00

Poliomyelitis in England and Wales

After the introduction of inactivated poliovirus vaccine in the late 1950s and oral polio vaccine shortly thereafter, poliomyelitis in the UK has remained under excellent control. There

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has been no single confirmed case of indigenous wild virus polio for more than a decade (figure 1). Under the Public Health Regulations (1984), suspected cases of acute polio in England and Wales should be reported by the clinician responsible for the case to the local Medical Officer for Environmental Health or Consultant in Communicable Disease Control who should immediately inform the Communicable Disease Surveillance Centre (CDSC). Consultants in Communicable Disease Control make weekly returns of all statutory notifiable diseases to the Office for National Statistics (ONS). ONS provides a weekly summary of these statutory notifiable cases to the Department of Health, and in addition, any death certificate in which there is mention of poliomyelitis contributing to the cause of death is brought to the attention of the Department ofHealth. Similar statutory reporting arrangements exist in Scotland and Northern Ireland. All cases of suspected poliomyelitis, whether officially notified or informally brought to the attention of CDSC, are followed up and classified as wild virus (indigenous), wild virus (imported), vaccine-associated!recipient, or vaccine-associated! contact or are discarded. Since 1985, there have been 28 cases of polio, notified or identified through laboratory reports or other means. There was no apparent difference between notified cases and those detected from other sources. All have been categorized according to the above criteria (table 1). There has been only 1 case of unknown etiology (probably caused by Coxsackie virus infection) since 1987, and only 1 imported case since 1989-a child returning from India who had been diagnosed as having acute polio 6 weeks before returning to the UK. The index case was no longer excreting wild virus when admitted to hospital for confirmation of diagnosis; neither were any of the UK contacts. It is therefore debatable if this case should be categorized as an importation. In a review of UK polio cases, Joce et al. [7] found that not all clinically suspected cases were being notified, and even

Table 1. Cases of poliomyelitis from all sources, according to diagnostic criteria, 1985-1994.
Vaccine/ recipient Vaccine/ contact Acquired abroad

Year

Unknown

Total

1985 1986 1987 1988 1989 1990 1991 1992 1993 1994

1 4 0 1 1 4 0 1
2 0

0 1 0 1 1 0 1
1 0 0

2 2 0 1 0 0
0 0

0 1 1
0

3 8 1 3
2

0 0 1
0 0

4
2

1
0

2 3
0

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some confirmed cases had not been notified. However, the rate of vaccine-associated paralytic poliomyelitis was estimated at 1.46 per million administered first doses, 0.49 for the second, o for the third and fourth doses, and 0.33 for the fifth. The risk to contacts was 0.98 per million immunizations for the first dose and 0 for subsequent doses. These estimates are comparable with those in other reports [8, 9]. Because reporting of polio would be scrutinized for the certification of eradication and also because of the surveillance that was being implemented in the Americas, it was evident that statutory notification alone would not suffice when the UK was to be considered for certification for eradication. Proof of absence of poliomyelitis would be needed, and additional evidence would be required to augment notification data.

AFP Surveillance in the UK

In 1991, AFP surveillance was instituted throughout the UK. Data were collected from July 1991 to June 1994, using the stimulated reporting system of the British Paediatric Association Surveillance Unit (BPASU). Each month, Consultant Paediatricians and members of the British Paediatric Association receive a card that lists 12 rare conditions presently under surveillance. Previous evaluation of the compliance with reporting has suggested that monthly returns of ;;:::90% of negative and positive reports are received [10]. In May 1991, all pediatricians were alerted to the addition of AFP surveillance to the BPASU scheme. A detailed protocol identified the reasons for the study and asked for telephone reporting of cases to CDSC in addition to monthly returns of cards. At least 1 and ideally 2 acute stool specimens were to be taken for viral culture. Any polioviruses were to be sent for typing to the Virus Reference Division of the Public Health Laboratory Service (PHLS). Children under the age of 16 years, presenting with AFP of any etiology, were included. Over the 3-year period, pediatricians Were reminded in regular newsletters from BPASU of the need to report; they received an annual report of the progress with the study.

numbers
10,000

8,000

6,000

4,000

2,000

1950

1960

1970

1980

1990

years

Figure 1. Notifications of acute poliomyelitis, 1940-1994, England and Wales (Office for National Statistics data).

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Over the 3 years, 120 children were reported through the scheme. The overall rate of reports has been 0.38/100,000 children < 16 years old/year. The rate was 0.48/100,000 during the first year of the scheme, 0.34 during the second year, and 0.34 during the third year, suggesting that reporting rates declined after the start of the surveillance (figure 2). Overall, 54% of cases were known to have had at least 1 stool specimen taken for virology; 15% had 2 stool samples sent. There did not appear to be any identifiable trends in compliance for collection of stool samples during the surveillance period. Sixty-nine (58%) of 120 AFP cases were diagnosed as Guillain-Barre syndrome. In 11 cases (9.1%), no diagnosis has yet been allocated, although follow-up of outstanding reports continues (table 2). Evidence of acute infection was found in several cases of Guillain-Barre syndrome, including 2 boys (3 and 6 years) with adenovirus infection, a 2-year-old boy with reovirus infection, a l2-year-old girl with nonpolio enterovirus infection, 2 with Mycoplasma infection, 2 with Campylobacter infection, 1 each with respiratory syncytial virus, cytomegalovirus, Epstein-Barr virus, influenza virus, and adenovirus infections, and 1 who was Paul-Bunnell test-positive. Other cases of AFP, not classified as Guillain-Barre syndrome, were reported to have been caused by Coxsackie B virus (2), Mycoplasma species (2), glandular fever, and rubella vaccine (lgG- and IgM-positive with immunization 16 days previously). There were 3 polio vaccine-associated/recipient cases (type 2 in a boy at 2 months, type 1 in a boy at 3 months and another at 6 months). All of these cases were also notified to ONS. The rate of reporting of AFP in the UK study was lower than that from any country in the Americas undertaking such surveillance [6]. The low UK AFP rates, along with the progressive decline of reporting through the study period, suggest that there has been considerable failure of reporting. However,

Table 2. Diagnoses of acute flaccid paralysis cases reported to British Paediatric Association Surveillance Unit.
No. of cases (%)

Diagnosis Poliomyelitis Guillain-Barre syndrome Transverse myelitis, radiculitis Other identified conditions Paralysis of uncertain origin, not polio* No follow-up Total * 5 of 6 cases had stools negative for polioviruses.

4 (3) 69 (58) 12 (10) 21 (18) 6 (5) 8 (7) 120

as AFP is a presenting feature of many different conditions, some of which may be enterovirus-related, the rates of these contributing causes to AFP may vary according to local sanitation and hygiene. Despite this possibility, however, the results of AFP surveillance in the UK would probably not be sufficient to convince an independent certification commission (using the criteria developed in the Americas) that eradication was accomplished.

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Further Surveillance Initiatives

numbers
12

10

6
4

1991

1992

1993

1994

years

Figure 2. Nos. of monthly reports of acute flaccid paralysis cases to British Paediatric Association Surveillance Unit, July 1991 to June 1994.

The purpose of AFP surveillance is to show convincingly that if there were any polio cases occurring, they would be detected. A bonus of this surveillance is a form of environmental surveillance for polioviruses. Over 3 years, >25,000 stool samples from paralyzed persons and their childhood contacts were examined in the Americas, and no wild polioviruses were detected. It would be expected that if wild poliovirus was in circulation, such samples would detect the viruses. Currently, laboratories in England and Wales report all confirmed poliovirus isolates to the PHLS CDSC. Most viruses are isolated in the stools of young children with gastroenteritis who have samples taken shortly after vaccination with oral polio vaccine. During 1993-1994, as part of a pilot scheme to enhance surveillance, isolates from several laboratories were submitted to the PHLS Enteric and Respiratory Virus Laboratory to be characterized as Sabin-like or wild strains by immunologic and molecular tests. During 1994, 200 poliovirus strains were received: 70 type 1, 63 type 2, and 67 type 3. All 183 isolates thus far characterized have proved to be Sabin vaccine-like strains. To ensure that imported strains of wild poliovirus are not circulating in the community, it is now proposed to extend this surveillance to all poliovirus strains isolated in England and Wales. Because it is known that most poliovirus infection is subclinical, it has been suggested that the detection and characterization of polioviruses in the environment would provide useful surveillance data. Routine environmental surveillance for poliovirus through sewage monitoring is unlikely to be practical

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or scientifically meaningful in the UK, in contrast to countries with less centralized sewage systems. Two programs are planned, however, that will give information about the origin of any polioviruses circulating in the environment. To assess the threat to public health posed by possible importation, a protocol is being developed to investigate all contacts of suspected importation and to use environmental monitoring to establish the scale of transmission that takes place following an imported case. To complement this, it is planned that a representative sample of the enteroviruses already being detected as part of the statutory drinking and seawater bathing water testing will be further characterized to try to identify the presence or absence of any wild polioviruses. A small proportion of poliovirus infections are associated with aseptic meningitis. It is planned to investigate cases of aseptic meningitis by testing cerebrospinal fluid and fecal samples with a sensitive nested polymerase chain reaction with poliovirus. Using this approach in a number of sentinellaboratories should provide additional information on the presence or absence of circulation of wild poliovirus in the UK. Conclusions The UK, along with many other European countries, has reported an absence of poliomyelitis for a decade or even longer. Computer simulations of poliovirus transmission [11] in developing countries suggest that even after 5 years without paralytic cases, the probability of silent transmission can still be in the range of 0.1%-1.0%. After a decade without paralytic cases, the UK is even more likely to be free of transmission. Because routine surveillance has not detected any cases of paralysis, this evidence would not prove the absence of circulation of wild polioviruses. From all sources, the rate of detection of vaccine-associated cases is as high as reported from other similar countries. Independent indicators of surveillance (such as AFP) are unlikely to reach the quality demonstrated in the Region of the Americas, where many countries had polio cases

until relatively recently. The standards for surveillance applied to industrialized countries, however, will need to be as rigorous as those met by less developed countries. In the UK, several new surveillance initiatives are proposed to demonstrate the absence of wild polioviruses that may be sufficient to satisfy certification procedures. Every country will gain considerably from the ability to abandon polio immunization. Countries will not benefit until there is convincing evidence worldwide that no wild polioviruses are in circulation, and the standards of evidence needed will be rigorous. The UK will need to rise to this challenge.
References 1. Nathanson N, Martin JR. The epidemiology of poliomyelitis: enigmas surrounding its appearance, periodicity, and disappearance. Am J Epidemiol 1979; 110:672-92. 2. Melnick JL, Ledinko N. Social serology: antibody levels in a normal young population during an epidemic of poliomyelitis. Am J Hyg 1951; 54:354-82. 3. Chief Medical Officer/Chief Nursing Officer Letter. Vaccination against smallpox. London: Department of Health, 1980; publication nos. CMO(80)12, CNO(80)8. 4. De Quadros CA, Andrus JA, Olive lM, et al. Eradication of poliomyelitis: progress in the Americas. Pediatr Infect Dis J 1991; 10:222-9. 5. De Quadros CA, Henderson DA. Disease eradication and control in the Americas. Biologicals 1993;21:335-43. 6. Pan American Health Organization. Final report of the third meeting of the International Commission for the Certification of Poliomyelitis Eradication in the Americas. Washington, DC: PARO, 1994. 7. Joce R, Wood D, Brown D, Begg NT. Paralytic poliomyelitis in England and Wales, 1985-91. BMJ 1992;305:79-82. 8. Esteves K. Safety of oral poliomyelitis vaccine: results of a WHO enquiry. Bull WHO 1988; 66:739-46. 9. Strebel PM, Sutter RW, Cochi SL, et al. Epidemiology of poliomyelitis in the United States one decade after the last reported case of indigenous wild virus-associated disease. Clin Infect Dis 1992; 14:568-79. 10. British Paediatric Surveillance Unit. 8th annual report. London, UK: British Paediatric Association, 1993. 11. Eichner M, Dietz K. Eradication of poliomyelitis: when can one be sure that polio virus transmission has been terminated? Am J Epidemiol 1996; 143:816-22.

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