Eradication of Wild Poliovirus from the Americas: Acute Flaccid Paralysis Surveillance,

Transcription

1 S37 Eradication of Wild Poliovirus from the Americas: Acute Flaccid Paralysis Surveillance, Ciro A. de Quadros, Bradley S. Hersh, Jean-Marc Olive, Jon K. Andrus, Claudio M. da Silveira, and Peter A. Carrasco Special Program for Vaccines and Immunization, Pan American Health Organization, Washington, DC; Global Programme for Vaccines and Immunization, World Health Organization, Geneva, Switzerland; Expanded Programme on Immunization. World Health Organization, New Delhi. India In May 1985, the Pan American Health Organization proposed the goal of interruption of wild poliovirus transmission in the Western Hemisphere. An important component of the polio eradication strategy was conducting surveillance for cases of acute flaccid paralysis. Reported cases were thoroughly investigated, including the collection of stool samples for testing for the presence of wild poliovirus. The last patient with poliomyelitis due to wild poliovirus in the Americas had onset of paralysis on 23 August 1991 in Peru. Since then, >9000 cases of acute flaccid paralysis have been reported and thoroughly investigated; none has been confirmed as paralytic poliomyelitis due to wild poliovirus. On 29 September 1994, the International Commission for the Certification of Poliomyelitis Eradication declared the Americas to be polio-free. In May 1985, the Pan American Health Organization proposed the goal of interruption of wild poliovirus transmission in the Western Hemisphere [1]. This proposal was promptly endorsed by all member governments and received strong support from several agencies and organizations including Rotary International, the US Agency for International Development, UNICEF, the Inter-American Development Bank, and the Canadian Public Health Association. In 1988, as a result of the progress achieved in the Americas, the World Health Assembly proposed the goal of global polio eradication [2]. The development of a surveillance system to monitor the incidence of paralytic poliomyelitis due to wild poliovirus was a critical component of the polio eradication strategy used in the Americas. Here we describe the surveillance system for persons with acute onset offlaccid paralysis (AFP) and review data obtained from this system for the years 1988 through Poliovirus Eradication Strategy in the Americas The major components ofthe strategy used to interrupt transmission of wild poliovirus in the Americas were the achievement and maintenance of high levels of vaccination coverage in children < 5 years of age, development of a surveillance system for the timely detection and investigation of persons with AFP (probable poliomyelitis cases), and creation of a Reprints or correspondence: Dr. Ciro A. de Quadros, Special Program for Vaccines and Immunization, Pan American Health Organization, rd St., NW, Washington, DC The Journal of Infectious Diseases 1997;175(Suppll):S by The University of Chicago. All rights reserved /97/75S $01.00 surveillance system for detection of wild poliovirus supported by a regional network of diagnostic virology laboratories [3]. To achieve and maintain high levels ofvaccination coverage in the population at risk, routine vaccination services have been supplemented by annual national immunization days (NIDs) in all countries ofthe region where wild poliovirus was circulating in Mass vaccination campaigns have been conducted twice a year over a short period of time (usually 1 or 2 days) in which one dose of oral polio vaccine (OPV) is administered to all children in the target age group (generally children 0-4 years of age), regardless of prior vaccination history. The annual NIDs are conducted with an interval of 4-6 weeks between campaigns. After completion ofthe NIDs, vaccine coverage and surveillance data identified areas either that had low coverage or in which wild poliovirus transmission persisted. These areas were targeted for "mop-up" activities in the form of house-to-house vaccination ofall children <5 years ofage, regardless of previous vaccination status. AFP Surveillance Methods Surveillance is a critical component ofthe poliovirus eradication strategy. The surveillance system used to monitor the incidence ofparalytic disease due to wild poliovirus in the Americas has evolved over time. The number of reporting units in the region has greatly increased since the beginning of the surveillance system and the definitions used to classify cases have been modified as the program evolved. The polio eradication program has attempted to include at least one reporting site (generally a health center or hospital) in every district or county throughout the region. Each reporting site submits a weekly report concerning the presence or absence

2 S38 de Quadros et al. lid 1997; 175 (Suppl 1) (i.e., negative notification) of AFP cases in the area under their jurisdiction. Epidemiologists attempt to investigate every case of AFP within 48 h ofnotification to confirm the clinical diagnosis and to obtain appropriate laboratory specimens. A "probable" case of poliomyelitis is considered any case of AFP in a person < 15 years of age or paralytic illness in a person of any age in whom a diagnosis of paralytic poliomyelitis is suspected. As part of the clinical case investigation, epidemiologists attempted to collect 2 stool specimens, ifat all possible, within 2 weeks after onset of paralysis. This is because the likelihood of wild poliovirus isolation decreases when stool specimens are collected later [4]. To increase the probability of detecting wild poliovirus, if present, in a community, investigators also attempted to collect stool specimens from at least 5 children (contacts) living in the same house or neighborhood as the index AFP case [5]. To increase the sensitivity of laboratory testing, stool specimens obtained from persons with AFP in whom there was a strong clinical suspicion of poliomyelitis were tested for virus isolation in two or more reference laboratories of the Pan American Health Organization (PAHO) Poliomyelitis Laboratory Network. In the early years of the polio eradication efforts (1985 ), when wild poliovirus was circulating freely in many countries of the region, a sensitive but nonspecific case definition was used to classify AFP cases as "confirmed." Cases of AFP were considered confirmed if there was anyone of the following criteria: laboratory confirmation (wild poliovirus isolated from stools obtained from cases or their contacts), epidemiologic linkage to another case of AFP or to a confirmed case of poliomyelitis, residual paralysis 60 days after onset of symptoms, death, or lack of appropriate investigation of a reported AFP case. As the polio eradication program progressed with increasing vaccine coverage and an increase in the number of AFP cases reported and investigated, it became increasingly clear to program managers, epidemiologists, and clinicians alike that there were a myriad of etiologies besides wild poliovirus that could result in AFP and that the above case definition resulted in the false "confirmation" of many AFP cases. Cases were frequently classified as "confirmed," even though the actual likelihood ofthe case being due to wild poliovirus was negligible. To be able to accurately monitor progress of the program, a more specific case definition was needed. In 1990, the case definition of a "confirmed" case was modified. An AFP case was confirmed only if it was associated with wild type poliovirus isolation from either the patient's stool or a specimen obtained from a contact of the patient. Cases of AFP that resulted in residual paralysis or death or that for a variety of reasons could not be fully investigated or could neither be confirmed nor discarded were now classified as "compatible with poliomyelitis." "Compatible" cases are considered failures of the surveillance system. After complete investigation, "probable" polio cases are reclassified as either "discarded," "compatible," or "confirmed. " A discarded case is a case that has been properly investigated, including the collection of adequate stool specimens, in which another cause of paralysis has been identified or laboratory testing has failed to detect the presence of wild poliovirus (or both). To assist in the collection and analysis ofafp and poliovirus surveillance data, PAHO developed a standardized polio surveillance database (Polio Elimination Surveillance System [PESS]). After the investigation of an AFP case, data are entered into PESS at the national level. Similarly, laboratory data are entered into a separate but linked module of PESS. Data are sent from the national level from national epidemiology units and laboratories to PAHO's headquarters in Washington, DC, on a weekly basis. Regional AFP and poliovirus surveillance data are summarized and reported back to countries in the form of PAHO's weekly polio bulletin. Surveillance Indicators To monitor the adequacy of regional AFP surveillance, a series of specific surveillance indicators were established [6]. These indicators are as follows: At least 80% of reporting units should report weekly on the presence or absence ofafp cases, the annual AFP rate per 100,000 population < 15 years of age should be ~ 1, at least 80% of reported AFP cases should be investigated within 48 h of being reported, at least 80% of reported AFP cases should have 2 adequate stool specimens collected within 14 days of paralysis onset, and at least 80% of AFP cases should have adequate stool specimens collected from 5 or more neighborhood contacts. The minimum annual rate of at least 1 case of AFP per 100,000 population < 15 years of age was based on the fact that in the absence of wild poliovirus transmission, cases of AFP due to other causes (e.g., Guillain-Barre syndrome, transverse myelitis, or tumors) will continue to occur [7]. Therefore, a sensitive AFP surveillance system would be expected to detect these "background" cases, even when wild poliovirus is not circulating in a country. Results In 1995, vaccination coverage through routine services among children at 1 year of age with at least three doses of oral poliovirus vaccine was 85% in the region (figure 1); these coverage rates have been supplemented by NIDs in several Latin American countries. Over the years, the negative notificationsystem has markedly expanded; by mid-1991, > 20,000 sites were reporting regularly on a weekly basis on the presence or absence of persons with AFP in their jurisdiction. The increase in reporting units helped to improve the timeliness of case reports. During the period

3 JID 1997; 175 (Suppl 1) AFP Surveillance in Region of the Americas 539 Conflrm.d c... (thou nd.) OPV3 cov.rege 8 100% 8 : 80% 4 : : : : 80% 40% 2 20% *:Ca.e. 0 Coverage Figure 1. Coverage with 3 doses of oral polio vaccine (OPV3) through routine vaccination services among children 12 months of age and reported confirmed paralytic poliomyelitis cases, Region of the Americas, Vaccination coverage has been augmented by national immunization days in several countries. Source: Pan American Health Organization , ",,2000 AFP cases were reported and investigated annually in the Region of the Americas (table 1). Each year the regional AFP notification rate exceeded 1 case/l00,000 population < 15 years ofage. The proportion ofcases investigated within 48 h of notification has been > 80% since The proportion ofreported cases with adequate stool specimens collected increased over time (table 2). As the number of stool specimens collected and tested increased, the number of wild poliovirus isolates decreased. The last wild poliovirus isolate from an AFP patient was obtained in Of the 453 confirmed polio cases reported in the period , 79 (17.4%) had wild poliovirus isolated from a stool specimen. Of these, 64 (83.5%) occurred in persons <6 years of age. Type 2 wild poliovirus was the first subtype to disappear from the Americas; the last reported type 2 poliovirus case occurred in Colombia in The last reported type 3 poliovirus case occurred in Mexico in 1990, and the last case associated with type 1 poliovirus isolation had paralysis onset in August On 23 May 1996, 4 years and 9 months had elapsed since a 2-year-old boy living in Junin, Peru, was diagnosed with poliomyelitis; this was the last case of poliomyelitis associated with wild poliovirus isolation (type 1) in the Americas [8]. Since this last confirmed case was reported, >9000 AFP cases have been thoroughly investigated and none has been confirmed as paralytic poliomyelitis due to wild poliovirus. Furthermore, > 36,000 stool specimens obtained in connection with these cases and their contacts were tested and found to be negative for wild poliovirus. The year ofonset oflast confirmed paralytic poliomyelitis cases due to indigenous wild poliovirus for countries of the Americas is summarized in table 3. During the period , a total of 15,789 AFP cases were completely investigated and were ultimately discarded (paralysis not due to wild poliovirus). Of the discarded cases, 8245 (52.2%) were diagnosed finally as Guillain-Barre syndrome, 380 (2.4%) as transverse myelitis, 277 (1.8%) as tumor, and 126 (0.8%) as trauma. The final diagnosis for the remaining discarded cases was reported as being other (28.9%) or unknown (13.8%). Discussion Information obtained from the PAHO AFP surveillance system has allowed program managers to regularly monitor progress toward polio eradication and to target resources to areas with greatest need. Moreover, these data have helped to refine and revise the regional polio eradication strategy, as needed. Finally, the availability of high-quality surveillance data has

4 S40 de Quadros et at. JID 1997; 175 (Suppl I) Table 1. Number ofacute flaccid paralysis (AFP) cases reported, AFP reporting rate, and final classification of reported cases, by year of paralysis onset, Region of the Americas, Total AFP % investigated No. ofcases cases AFP reporting within 48 h of Year reported rate AFP onset Discarded Compatible Confirmed * NOTE. Data are as of 31 May * 246 cases remain under investigation from allowed national and international certification commissions to evaluate progress toward the goal of polio eradication from the Americas. Several important examples demonstrate how surveillance data were used to further the cause of polio eradication. In 1986, despite high vaccination coverage, an outbreak of type 3 wild poliovirus with >350 cases occurred in the northeast region of Brazil [9]. A thorough investigation of this outbreak determined a contributing factor to be the relatively low effectiveness of the type 3 component of polio vaccine used in Brazil at the time. After this outbreak, a randomized trial of alternative formulations of OPV in Brazil demonstrated a significantly higher seroconversion rate for children vaccinated with OPV containing twice the titer of the type 3 component (600,000 compared with 300,000 TCID so ) [10]. Based on these findings, PAHO immediately recommended that the standard OPV formulation used in the region should be changed from 1,000,000:100,000:300,000 TCID so (10:1:3) for types 1, 2, and 3, respectively, to 1,000,000:100,000:600,000 TCID so (10:1:6) [11]. In,an outbreak oftype 3 poliomyelitis occurred in Mexico and was thought to be at least partially due to the late introduction of the OPV with higher-potency type 3 component [12]. A detailed analysis of AFP surveillance data in 1992 for risk factors for wild poliovirus isolation among reported AFP cases provided important information. Children < 6 years of age, with either the presence of fever at the onset of paralysis or the development ofcomplete paralysis in <4 days after onset, were significantly more likely to have wild poliovirus isolated from stool specimens than were other reported patients with AFP [13]. Information from this analysis helped epidemiologists to establish priorities in conducting case investigations. A careful review of laboratory surveillance data (see [14]) revealed that a single stool specimen, appropriately collected within 2 weeks of paralysis onset, would have been sufficient Table 2. Laboratory results for stool specimens from acute flaccid paralysis (AFP) cases and contacts by year of paralysis onset, Region of the Americas, No. ofwild Total no. of No. ofwild No. of AFP % ofafp cases % ofafp cases Total no. of poliovirus % ofafp cases contact poliovirus cases with ~ 1 stool with ~2 stool patient isolates among with ~5 contact stools isolates among Year investigated specimen" specimens" stools tested patients stool specimens tested contacts t NOTE. Data are as of 31 May * Collected within 14 days of AFP onset. t 246 cases remain under investigation from 1995.

5 JID 1997;175 (Suppll) AFP Surveillance in Region of the Americas S4l Table 3. Year of last confirmed case of paralytic poliomyelitis due to indigenous wild poliovirus, by country, Region of the Americas. Country North America Canada United States Mexico English-speaking Caribbean Antigua and Barbuda Bahamas Barbados Belize Cayman Islands Grenada Guyana Saint Kitts-Nevis Saint Vincent Saint Lucia Jamaica Suriname Trinidad/Tobago Latin Caribbean Cuba Dominican Republic Haiti Central America Costa Rica EI Salvador Guatemala Nicaragua Panama Andean countries Bolivia Colombia Ecuador Peru Venezuela Brazil Southern cone Argentina Chile Paraguay Uruguay Year 1991 (April) (August) to detect the majority ofareas where wild poliovirus was circulating. Moreover, the collection of specimens from contacts had only a negligible contribution in detecting the presence of wild poliovirus in a community. These data strongly suggest that countries in which polio is still endemic should consider the collection of only 1 stool specimen from AFP patients and only in special circumstances collect stool from contacts of AFP patients. This measure should greatly simplify case investigations and at the same time reduce laboratory work load and increase efficiency [15]. After carefully reviewing detailed national surveillance data in early 1994, all national certification commissions recommended that their countries be certified as being polio-free. On 29 September 1994, during the quadrennial meeting of the Pan American Sanitary Conference, the president of the International Commission for the Certification ofpoliomyelitis Eradication (ICCPE), Frederick C. Robbins, stated that, based on recommendations ofthe national certification commissions and after thoroughly reviewing regional polio vaccination coverage, AFP, and wild poliovirus surveillance laboratory data, the IC CPE had concluded that wild poliovirus transmission had been interrupted in the Americas. Wild poliovirus transmission, however, continues to occur in other regions ofthe world, and with the availability of rapid transportation between continents, it is clear that the Americas will remain at risk for the importations ofwild poliovirus [16]. If importations occur, the potential exists for polio outbreaks in the Americas, especially in areas with low vaccine coverage and poor sanitation. Indeed, poliovirus has demonstrated the ability to locate and infect pockets of susceptible persons, even in countries with high levels of vaccination coverage. In mid-1978, an outbreak of 80 cases ofparalytic poliomyelitis due to type 1 poliovirus occurred in the Netherlands [17]. All affected persons were unvaccinated because of religious objections to vaccination. In late 1978, in Canada, 11 cases of paralytic poliomyelitis due to type 1 virus occurred among unvaccinated persons from a community with religious objections to vaccination. Characterization of the virus isolates from this outbreak revealed that the Canadian isolates were very similar to those obtained from patients during the Netherlands outbreak [18]. The last outbreak of wild poliovirus in the United States occurred in 1979, when 10 paralytic cases were reported from four states [19]. In this outbreak, clinical cases ofpoliomyelitis occurred almost exclusively among persons belonging to religious groups with objections to vaccination. Virus obtained from this outbreak was similar to isolates obtained during 1978 in the Netherlands and Canada [20]. From September 1992 through February 1993, a large outbreak of paralytic poliomyelitis due to type 3 poliovirus occurred in the Netherlands [21]. A total of 68 cases were reported, including 2 deaths. All cases except 1 occurred in persons with religious objection to vaccination. After notification of the outbreak from the Netherlands Ministry of Health, especially in light ofthe 1978 outbreak, the Canadian Ministry of Health enhanced their polio surveillance activities. Stool surveys were conducted in several religious communities with objections to vaccination that were known to have had recent contact with travelers from the Netherlands. In early 1993, an investigation was begun in a small community near Lethbridge, Alberta, Canada [22]. A case of paralytic poliomyelitis had been reported from this area during the 1978 outbreak. There were unvaccinated members of a religious group living in this community. No cases of suspected polio had been reported. Type 3 poliovirus was isolated from stool samples obtained from unvaccinated children. In an epide-

6 S42 de Quadros et al. JID 1997;175 (Supp11) miologic analysis, contact with visitors from the Netherlands and travel to the Netherlands were found to be risk factors for isolatjon of wild poliovirus from a stool specimen. To prevent the reintroduction of wild poliovirus, the countries of the Americas will need to maintain high levels of population immunity. The challenge now for the Americas is to maintain the interruption ofpoliovirus circulation over time. In addition to maintaining high vaccination coverage, ongoing surveillance for cases of AFP and for wild poliovirus will be absolutely necessary to ensure that the Americas remain polio-. free. International communication and collaboration are necessary to ensure the rapid detection and timely implementation of control efforts for importations of wild poliovirus. Only the global eradication of poliomyelitis will ensure that poliovirus infection will not cause paralytic disease again in the Americas. References 1. Pan American Health Organization. Director announces campaign to eradicate poliomyelitis from the Americas by Bull Pan Am Health Organ 1985; 19: World Health Assembly. Global eradication of poliomyelitis by the year Geneva: World Health Organization, 1988; resolution WHA de Quadros CA, Andrus JK, Olive 1M, et al. Eradication of poliomyelitis: progress in the Americas. Pediatr Infect Dis J 1991; 10: Alexander JP Jr., Gary HE Jr., Pallansch MA. Duration of poliovirus excretion and its implications for acute flaccid paralysis surveillance: a review of the literature. J Infect Dis 1997; 175(supp1 1):S Andrus JK, de Quadros CA, Olive JM. The surveillance challenge: final stages of eradication of poliomyelitis in the Americas. MMWR CDC Surveill Summ 1992;41(SS-1): Pan American Health Organization. Strategies for the certification of the eradication of wild poliovirus transmission in the Americas. Bull Pan Am Health Organ 1993;27: Alter M. The epidemiology ofguillain-barre syndrome. Ann Neuro11990; 27(suppl):S Pan American Health Organization. No polio in the Americas for two years. PAHO/EPI Newsletter 1993; 15(4): Pan American Health Organization. Polio in northeast Brazil. PAHO/EPI Newsletter 1986;8(4): Patriarca PA, Laender F, Palmeira G, et al. Randomised trial of alternative formulations of oral poliovaccine in Brazil. Lancet 1988; 1: Pan American Health Organization. Final report, seventh meeting of the Technical Advisory Group on EPI and the Eradication of Poliomyelitis in the Americas, Lima, Peru. Washington, DC: PAHO, Pan American Health Organization. Poliovirus surveillance in the Americas. PAHO/EPI Newsletter ; 11(6): Andrus JK, de Quadros CA, Olive 1M, et al. Screening of cases of acute flaccid paralysis for poliomyelitis eradication: ways to improve specificity. Bull World Health Organ 1992; 70: Pinheiro FP, Kew OM, Hatch MH, da Silveira CM, de Quadros CA. Eradication of wild poliovirus from the Americas: wild poliovirus surveillance-laboratory issues. J Infect Dis 1997; 175(suppl 1):S Silveira CM, de Quadros CA, Hersh BS, et al. Polio diagnosis: one or two samples? PAHO/EPI Newsletter 1995; 17(5): Hull HF, Ward NA, Hull BP, et al. Paralytic poliomyelitis: seasoned strategies, disappearing disease. Lancet 1994;343: Bijkerk H. Poliomyelitis epidemic in the Netherlands, Dev Biol Stand 1979;43: Furesz J, Armstrong RE, Contreras G. Viral and epidemiological links between poliomyelitis outbreaks in unprotected communities in Canada and the Netherlands [letter]. Lancet 1978;2: Schonberger LB, Kaplan J, Kim-Farley R, et al. Control of paralytic poliomyelitis in the United States. Rev Infect Dis 1984;6(suppl 2):S Hatch MH, Marchetti GE, Nottay BK. Strain characterization studies of poliovirus type 1 isolates from poliomyelitis cases in the United States in Dev BioI Stand 1981;47: Oostvogel PM, van Wijngaarden JK, van der Avoort HGAM, et al. Poliomyelitis outbreak in an unvaccinated community in the Netherlands, Lancet 1994;344: Centers for Disease Control and Prevention. Isolation of wild poliovirus type 3 among members of a religious community objecting to vaccination-alberta, Canada, MMWR Morb Mortal Wkly Rep 1993; 42:337-9.