Endgame Issues for the Global Polio Eradication Initiative
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1 VIEWPOINTS Endgame Issues for the Global Polio Eradication Initiative Technical Consultative Group to the World Health Organization on the Global Eradication of Poliomyelitis a The polio eradication initiative, created after the World Health Assembly resolved, in 1988, to eradicate poliomyelitis globally by 2000, has made remarkable progress. From 1988 through 2000, the number of countries where polio was endemic decreased from 1125 to 20, and the estimated number of polio cases decreased from 350,000 to!3500, for a percentage decrease of 199%. Wild-type 2 poliovirus has not been detected worldwide since October 1999, despite improving surveillance. The major focus of the eradication effort is to complete the task of stopping wild-type poliovirus transmission. Given the rapid progress made toward this goal, planning for the posteradication era has begun in earnest (1) to minimize the risk of reintroduction of virus into the population from laboratory stocks or long-term carriers, and (2) to prevent vaccine-derived polioviruses from circulating and causing outbreaks. This report summarizes the current thinking about these endgame issues, as put forth by the World Health Organization s technical advisory body for the initiative, the Technical Consultative Group on the Global Eradication of Poliomyelitis. The polio eradication initiative, which was created after the World Health Assembly resolved, in 1988, to eradicate poliomyelitis globally by 2000 [1], has made remarkable progress toward reaching the eradication target [2]. The major focus of the eradication effort has been, and continues to be, completing the task of stopping wild-type poliovirus transmission. Given the rapid progress made toward stopping wild-type poliovirus transmission, planning for the posteradication era has begun in earnest (1) to minimize the risk of reintroduction of virus into the Received 22 October 2001; electronically published 19 November a Members of the Technical Consultative Group on the Global Eradication of Poliomyelitis are listed after the text. Reprints or correspondence: Dr. Walter Orenstein, National Immunization Program (E05), Centers for Disease Control and Prevention, 12 Corporate Square Blvd. NE, Atlanta, Georgia (wao1@cdc.gov). Clinical Infectious Diseases 2002; 34: by the Infectious Diseases Society of America. All rights reserved /2002/ $03.00 population from laboratory stocks or long-term carriers, and (2) to prevent vaccine-derived polioviruses (VDPVs) from circulating and causing outbreaks. This report summarizes the current thinking about these endgame issues, as put forth by the World Health Organization s (WHO) technical advisory body for the initiative, the Technical Consultative Group (TCG) on the Global Eradication of Poliomyelitis. As long as oral poliovirus vaccine (OPV) is used, there is the potential for circulation of VDPVs and the potential that these viruses might acquire both the neurovirulence and transmission characteristics of wild-type polioviruses. With the possibility that immunization levels could decrease in future years as supplementary immunization activities cease in polio-free areas, there is a real threat of a resurgence of polio epidemics resulting from circulating VDPVs that express a wild-type virus phenotype. Therefore, the eradication of all poliomyelitis disease ultimately requires the cessation of OPV use. Ultimately, all vaccination against polio can be discontinued if it is safe to do so that is, only if the following criteria are met [3, 4]: (1) termination of wildtype poliovirus transmission, (2) containment of laboratory stocks of polioviruses, (3) demonstration that VDPVs will not circulate for a prolonged period after cessation of OPV vaccination, and (4) establishment of a global stockpile of, and a production capacity for, OPV for those instances in which wild-type polioviruses are detected in the postimmunization era. Until these criteria are met, high coverage with OPV will be necessary. CERTIFICATION OF ERADICATION In 1995, an independent 13-member Global Certification Commission was established to develop the criteria for, and oversee the process of, certification of eradication of wild-type poliovirus trans- 72 CID 2002:34 (1 January) TCG on Global Eradication of Poliomyelitis
2 mission. A formal process has now been established to focus on epidemiological blocks (i.e., groups of countries sharing similar epidemiological features of disease), length of time free of polio, and quality of surveillance [5]. The key criterion for global certification is the absence of wild-type poliovirus transmission throughout the world for 3 consecutive years in the presence of excellent surveillance [5]. Surveillance for cases of acute flaccid paralysis (AFP) provides the most important information for certification [6]. Detection and investigation of at least 1 case of nonpolio AFP per 100,000 children aged!15 years has proven to be the key indicator of whether a surveillance system would be able to detect polio if the virus was present. Other indicators deal with the collection and processing of stool specimens. Many countries, including countries affected by conflict (e.g., civil war and internal strife), have either reached and sustained or are approaching certification-standard AFP surveillance. Certification for the 6 WHO regions is done on a region-by-region basis, requiring every country to have achieved the aforementioned criteria. Experience in 2 WHO regions (regions of the Americas and Western Pacific [certified in 1994 and 2000, respectively]) has demonstrated that the process and criteria for certifying the eradication of indigenous wild-type poliovirus transmission are sound. The Global Certification Commission will review the work of the regional commissions and, with the completion of appropriate containment, eventually will certify the world as being polio free. Although individual regions can be certified as polio free, global certification is a precondition to ceasing OPV vaccination. CONTAINMENT OF LABORATORY STOCKS OF POLIOVIRUSES In 1997, the Global Certification Commission decided that containment of laboratory stocks of wild-type polioviruses would be a prerequisite before global certification could occur [7]. Many of the world s laboratories store samples that either are known to contain wild-type poliovirus or are suspected to contain wild-type poliovirus because they were collected at a time when, and in areas where, wild-type poliovirus was circulating. Although absolute containment is not possible, effective containment is a realistic goal. The risk of inadvertent transmission of poliovirus from the laboratory to the community is small, but it is not nonexistent. Transmission requires that 4 conditions be met: (1) poliovirus infectious materials must be present in the laboratory, (2) some operations must be performed with the materials that expose the worker to the virus, (3) the worker must be susceptible to an infection that results in poliovirus shedding and the exposure of others, and (4) persons in the community who are exposed to the virus must be susceptible to infection. Although blocking transmission by eliminating any one of these conditions may be questioned, the risks associated with all 4 conditions can be effectively reduced, collectively providing a high level of community protection [8]. The last case of smallpox, which occurred in Birmingham, England, in 1978 (1 year after the global eradication of smallpox), was the result of a laboratory containment failure [9], and it serves as an important reminder of the critical need for effective containment. A total of 110 countries have already appointed a national task force responsible for establishing a national plan of action and implementing laboratory containment. Seventy countries have already begun compiling exhaustive lists of biomedical laboratories to be surveyed, with 160,000 laboratories listed to date. A national survey has been started by the majority of these countries, including several large industrialized countries, such as Japan, Australia, Canada, and Spain. Extensive pilot surveys have been conducted in both the United States and the United Kingdom to prepare for national surveys scheduled for To date, 11 countries have completed the activities of the preeradication phase and have submitted national inventories for review [10]. In addition, WHO, in collaboration with manufacturers of inactivated poliovirus vaccine (IPV) and regulatory authorities, has produced guidelines for the safe production and quality control of IPV manufactured from wild-type polioviruses and is continuing to work with these groups. CIRCULATION OF VDPVS Poliomyelitis is caused by any one of 3 serotypes of poliovirus. After individuals are vaccinated with the live attenuated strains contained in the trivalent OPV, the VDPVs are excreted and may infect contacts of the vaccinees. Data from Hungary and Cuba suggest that, under conditions of mass administration of OPV, circulation of VDPVs is usually limited to a 2 3-month period after OPV use is stopped [11, 12]. However, new data now demonstrate that VDPVs also may acquire the neurovirulence and transmission characteristics of wild-type poliovirus. The rarity of this event is reflected in information from the polio eradication initiative. For example, an estimated 10 billion doses of OPV were administered from 1997 through 2001, with VDPVs isolated and analyzed in the global polio laboratory network during this period [13]. This work has detected 2 episodes of paralysis due to circulating VDPVs [13]. These VDPVs are estimated to have circulated for 2 years after an initial vaccination, before they acquired the characteristics capable of causing a polio outbreak. Circulating type 1 VDPVs were detected in Hispaniola during [14], and circulating type 1 VDPVs were detected in The Philippines in 2001 [15]. Circulating type 2 VDPVs detected in Egypt during 1988 Global Polio Eradication Initiative CID 2002:34 (1 January) 73
3 1993 caused a third episode of paralysis and were identified after earlier poliovirus isolates from that country were examined [16]. Low vaccination coverage appears to be the common risk factor that allowed VDPVs to circulate among susceptible populations and acquire wildtype characteristics. There is additional concern that longterm poliovirus carriers identified among immunodeficient persons may pose a threat for the reseeding of an increasingly susceptible population with VDPVs in a postimmunization era. Twelve long-term carriers of poliovirus (i.e., persons who excreted virus for 16 months) have been identified worldwide; one of these carriers excreted poliovirus for 11 decade (median duration, 5.6 years from the last receipt of OPV and the last identification of a specimen yielding poliovirus, for the first 9 cases) [17]. All long-term carriers were detected among persons with rare cases of congenital immunodeficiency disorders that occur with a frequency of 1 case per 10, ,000 births. However, the risk posed by such long-term carriers is probably minimal for several reasons. First, the number of persons who excrete virus is very low, despite almost universal OPV use worldwide. On the basis of results of studies performed in the United States and the United Kingdom, the risk of becoming a long-term carrier of poliovirus among immunodeficient persons with hereditary disorders is low (estimated risk, 0.1% 1%; N. Halsey, personal communication, 2000). Second, no long-term carriers have been detected in the developing world, despite studies in Ethiopia, Pakistan, and Central America, and extensive data from the global AFP surveillance system. In addition, immunodeficient persons would not be expected to survive for long in these settings. All long-term carriers who were identified were detected in middle- or high-income industrialized countries. Third, only 4 (33%) of these long-term carriers are known to currently excrete poliovirus. Fourth, an increasing number of industrialized countries have shifted to IPV use (the most-recent chronic carrier was probably infected in 1992 [17]). None of these carriers are known to have transmitted their viruses to other persons in the community, although transmission could have been limited, because these individuals who excreted viruses lived in highly vaccinated communities. In addition, the therapeutic use of antiviral agents and high-dose immunoglobulin may help eliminate the carrier state in some of these cases. Neither research studies nor the AFP surveillance system, which investigates 125,000 cases each year, found an association between HIV infection (or AIDS) and either (1) an increased risk for poliomyelitis due to wildtype poliovirus or VDPV [18], or (2) long-term excretion of poliovirus. POLIO VACCINE STOCKPILE AND SURVEILLANCE As part of contingency planning for the posteradication era, both a stockpile of polio vaccine (e.g., OPV, monovalent type-specific OPVs, and/or IPV) and the production capacity for this vaccine under appropriate containment conditions will need to be maintained [19]. The size and composition of such a stockpile are topics of discussion, but a stockpile may need to include sufficient vaccine to vaccinate 3 5 global birth cohorts [20]. Surveillance systems to detect poliovirus circulation also will need to be maintained after cessation of OPV use. Finally, both a response plan for instances of poliovirus detection and the organizational capacity to respond must be in place before OPV use is discontinued. The TCG believes that these plans should be required before certification occurs. The polio vaccine stockpile would be available if poliovirus were released either unintentionally, through a laboratory accident, or intentionally, through biological warfare or an act of bioterrorism, into an increasingly or fully susceptible population in the post-opv era. Compared with smallpox and anthrax, polioviruses have been considered poor agents for use in biological warfare or acts of bioterrorism, because the vast majority of poliovirus infections (199%) would not result in paralytic manifestations, even in a susceptible population. However, release of poliovirus into a highly susceptible population could greatly enhance public anxiety. In light of the ongoing anthrax events, the threat that poliovirus could pose should be reassessed. Plans must be in place to control outbreaks should they occur. OPTIONS FOR STOPPING POLIO VACCINATION Leading immunization experts have expressed opposing views as to the implications of circulating VDPVs, with one group suggesting that OPV use must now continue indefinitely and another group asserting that OPV use should stop soon after global certification occurs [21, 22]. Similar discussions took place during the smallpox eradication effort, with some experts advocating for continuing vaccination indefinitely and others wanting to discontinue smallpox vaccination as early as possible. In the end, individual countries decided if and when to stop vaccination. The United States, for example, recommended that vaccination be ended in 1971, long before the eradication goal was accomplished. In contrast, India established a special commission after the virus had been eradicated. Unfortunately, this country-by-country approach cannot be used for cessation of OPV use, because of the potential for the emergence of VDPVs. There are compelling reasons for discontinuing OPV use as soon as possible. The humanitarian and epidemiological reasons for discontinuation of OPV use are as follows: (1) continued OPV use risks reestablishment of polio disease through circulation of VDPVs, and (2) continued OPV use causes sporadic cases 74 CID 2002:34 (1 January) TCG on Global Eradication of Poliomyelitis
4 of vaccine-associated paralytic poliomyelitis (VAPP). Considering that the risk of VAPP is approximately 1 case per million initial doses of OPV administered [23], a global birth cohort of 120 million children would give rise to 120 cases of VAPP each year for as long as OPV is used. Such a scenario would require that communities and leaders agree to bear this burden of disability in the absence of any naturally occurring polio. However, public tolerance is invariably extremely low in the absence of disease [24]. There are also economic arguments, especially with regard to the potential elimination of vaccine distribution and administration costs, as well as decreased costs for vaccine production once the stockpile is established. The options for discontinuation of OPV in the postcertification era have been described elsewhere [17]. These options include (1) discontinuing OPV use after carrying out a mass campaign with OPV, to maximize population immunity and minimize circulation of VDPVs; (2) switching to vaccination with IPV; and (3) developing, for the posteradication era, new vaccines that would not cause VAPP and would not be transmissible. 1. Coordinated discontinuation of OPV use worldwide after polio eradication has been certified by the Global Certification Commission. With this scenario, mass campaigns for vaccination with OPV (to maximize population immunity) would be followed by coordinated discontinuation of OPV use. The major advantage of this option would be the cessation of OPV use at a time when population immunity is likely to be at the highest levels, thus minimizing the risk that VDPVs will circulate. Countries would have the option of continuing vaccination with IPV, since IPV is not associated with a risk for emergence of circulating VDPV. This option may raise ethical concerns that IPV would not be available for children living in countries that elect not to use this vaccine. Continued use of IPV in industrialized countries (as some experts advocate) would (1) provide further assurance that virus would not escape from IPV manufacturing sites, all of which are located in industrialized countries; (2) maintain population immunity against polio and thereby deter the use of poliovirus as a biological weapon in the most-likely target countries; (3) provide additional assurance that wild-type poliovirus will not be transmitted from laboratory stocks in industrialized countries; and (4) further minimize the risk of emergence of circulating VDPV (and possible outbreaks) from long-term carriers. 2. Replacement of OPV with IPV. The major advantage of replacing OPV with IPV in all countries would be that populations would have at least some level of protection against polio, including circulating VDPVs, for the foreseeable future. This scenario would reduce the likelihood of polio outbreaks should virus be introduced, and it might decrease the odds of poliovirus being considered as an agent for use in acts of bioterrorism. Two major disadvantages would be low population immunity, if coverage levels are not high, and low seroconversion rates for IPV (for type 1, 60%; type 2, 60%; and type 3, 90%) when it is given to individuals in developing countries at the usual immunization contact ages of 6, 10, and 14 weeks [24]. These disadvantages may be further aggravated by low routine coverage in many megacities and densely populated areas, where the risk of emergence of circulating VDPVs is greatest. In addition, manufacturers of IPV would need to increase production capacity greatly to permit implementation of this option. The greatest disadvantage of such a policy would be its cost, which could potentially place further financial burden on low-income countries that had already borne the majority of the costs for implementation of the eradication strategies. 3. Development of new live vaccines for the posteradication period (i.e., vaccines that would not cause VAPP and that are not transmissible) appears to be a formidable task one that may not be feasible on the basis of current scientific knowledge and regulatory concerns. The costs associated with developing, testing, and seeking regulatory approval for a new vaccine would be enormous. Since OPV causes 1 case of VAPP per million doses administered, any field trial testing a new vaccine would need to be very large. The molecular basis of transmissibility is unknown, thus hampering efforts at the rational design of less-transmissible strains. In addition, such a vaccine might be used for only a short period, thereby further reducing manufacturers financial incentives to develop, test, and produce such a product. For these reasons, it appears unlikely that a new vaccine could be available during the expected time frame of the polio eradication initiative or, even, ever in the posteradication era, unless huge public-sector investments were made [20]. The first option described above currently appears to be the most-attractive option in terms of programmatic feasibility and costs. After global eradication of poliovirus has been achieved, many countries will be ready and, indeed, anxious to stop vaccination against a disease that no longer exists. Individual decisions by countries to stop OPV use could, however, place populations that no longer benefit from vaccination at risk of exposure to circulating VDPVs imported from countries that elect to continue using that vaccine. For this reason, stopping OPV use would require a coordinated approach. However, it would be premature to endorse any strategy until (1) the risk of reintroduction of circulating VDPVs is better understood, (2) the costs and benefits of alternate strategies have been assessed, and (3) the potential use of poliovirus for acts of bioterrorism is reassessed, given recent events related to terrorism. Finally, the implications of all options for developing countries must be carefully considered. Whichever option is ultimately adopted, OPV will be required Global Polio Eradication Initiative CID 2002:34 (1 January) 75
5 as part of the global immunization program for the foreseeable future. DISCUSSION AND NEXT STEPS Several expert consultations have played a critical role in identifying gaps in knowledge, outlining possible scenarios for stopping OPV use, defining the infrastructure and the surveillance systems that need to be in place before OPV use could be stopped, and determining additional research to answer important questions that affect the feasibility of each possible scenario for stopping vaccination [3 5, 20, 25 28]. This series of meetings, with an even broader representation, needs to continue to augment the knowledge base for decision making and then to build a global consensus about the safest and most-effective strategy for stopping polio immunization. WHO and its partners are coordinating and implementing a 3-part agenda for the polio endgame that encompasses the programmatic work (to be completed by the end of 2002), new scientific research (to be completed by the end of 2003), and policy development and communication (to be completed by the end of 2004). Recognizing the need for critical oversight of the scientific research agenda, WHO constituted a Steering Committee for Research on Stopping Polio Vaccines that began its work in The Steering Committee will identify and prioritize key research questions and, using available collaborative and contracting means, obtain answers that will broaden the scientific knowledge base for decision making. The highest priority of the polio eradication initiative is its primary objective of interrupting transmission of wild-type poliovirus and certifying that achievement in At the same time, a great deal of work needs to be completed before a final decision can be made as to the feasibility of the most-appropriate strategy for eventually stopping polio immunization. WHO has put in place a structure and process that includes advisory committees, informal meetings, formal consultations, and a comprehensive system of review and decision making by the World Health Assembly, which, in May 2002, will begin consideration of this issue for the first time. The TCG will continue to assist in the process of identifying a safe and scientifically sound strategy that will allow for OPV discontinuation (if prudent), one that will find broad endorsement by both the scientific community and political bodies, one that ensures that polio eradication will be permanent, and one that can realize the expected economic savings after OPV use is discontinued. Ultimately, the final decision regarding cessation of polio immunization will rest with WHO member states represented at their annual meeting, the World Health Assembly. TCG MEMBERS The members of the TCG are as follows: Walter A. Orenstein (Centers for Disease Control and Prevention, Atlanta), J. Peter Figueroa (Ministry of Health, Kingston, Jamaica), Isao Arita (Agency for Cooperation in International Health, Kumamoto City, Japan), Ali J. Mohammad (Ministry of Health, Muscat, Oman), R. Nath Basu (formerly with the National Institute of Communicable Diseases, New Delhi, India), and Francis K. Nkrumah (Noguchi Memorial Institute for Medical Research, Legon, Ghana). References 1. World Health Assembly. Global eradication of poliomyelitis by the year Geneva: World Health Organization, 1988 (resolution 41.28). 2. Centers for Disease Control and Prevention. Progress toward global poliomyelitis eradication, MMWR Morb Mortal Wkly Rep 2001; 50:320 2, Expanded Program on Immunization. Report of the meeting on the scientific basis for stopping polio immunization, Geneva, March Geneva: World Health Organization, 1998 (WHO/EPI/GEN/98.12). 4. Vaccines & Biologicals Department. Sixth Meeting of the Technical Consultative Group (TCG) on the Global Eradication of Poliomyelitis, Geneva, 7 10 May Geneva: World Health Organization, 2001 (WHO/ V&B/01.32). 5. Expanded Program on Immunization. Report of the 1st Meeting of the Global Commission for the Certification of Poliomyelitis. Geneva: World Health Organization, 1995 (WHO/EPI/GEN/95.6). 6. World Health Organization. Acute flaccid paralysis (AFP) surveillance: the strategy for poliomyelitis eradication. Wkly Epidemiol Rec 1998; 73: Vaccines & Biologicals. WHO global action plan for laboratory containment of wild polioviruses. Geneva: World Health Organization, 1999 (WHO/V&B/99.32). 8. Dowdle WR. Polio eradication: turning the dream into reality. ASM News 2001; 67: Fenner F, Henderson DA, Arita I, Jezek Z, Ladnyi ID. Smallpox and its eradication. Geneva: World Health Organization, 1988; 23: Centers for Disease Control and Prevention. Global progress toward laboratory containment of wild polioviruses, June MMWR Morb Mortal Wkly Rep 2001; 50: Domok I, Molnar E, Jancso A, Daniel M. Enterovirus survey in children after mass vaccination with live attenuated polioviruses. BMJ 1962; i: Mas Lago P, Caceres VM, Galindo MA, et al. Persistence of vaccine-derived poliovirus following a mass vaccination campaign in Cuba: a population-based survey among unvaccinated infants. Int J Epidemiol 2001; 20: Centers for Disease Control and Prevention. Developing and expanding contributions of the Global Laboratory Network for Poliomyelitis Eradication, MMWR Morb Mortal Wkly Rep 2000; 49: Centers for Disease Control and Prevention. Outbreak of poliomyelitis Dominican Republic and Haiti, MMWR Morb Mortal Wkly Rep 2001; 50: Centers for Disease Control and Prevention. Paralytic poliomyelitis due to circulating vaccine-derived poliovirus Philippines, MMWR Morb Mortal Wkly Rep 2001; 50: Centers for Disease Control and Prevention. Circulation of a type 2 vaccine derived poliovirus Egypt, MMWR Morb Mortal Wkly Rep 2001; 50:41 2, Wood DJ, Sutter RW, Dowdle WR. Stopping poliovirus vaccination after eradication: issues and challenges. Bull World Health Organ 2001; 78: Sutter RW, Cochi SL, Melnick JL. Live attenuated poliovirus vaccines. In: Plotkin SA, Orenstein WA, eds. Vaccines. Philadelphia: WB Saunders, 1999: Fine P, Sutter RW, Orenstein WA. 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6 In: Brown F, ed. Progress in polio eradication: vaccine strategies for the end game. Basel, Switzerland: S. Karger (in press). 20. Vaccines & Biologicals. New Polio Vaccines for the Post-Eradication Era, Geneva, January Geneva: World Health Organization, 2000 (WHO/V&B/00.20). 21. Dove AW, Racaniello VR. The polio eradication effort: should vaccine eradication be next? Science 1997; 277: Henderson DA. Countering the posteradication threat of smallpox and polio. Clin Infect Dis 2001; 33:79 83 (in this issue). 23. 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: Chen RT. Safety of vaccines. In: Plotkin SA, Orenstein WA, eds. Vaccines. 3d ed. Philadelphia: WB Saunders, 1999: WHO Collaborative Study Group on Oral and Inactivated Poliovirus Vaccines. Combined immunization of infants with oral and inactivated poliovirus vaccines: results of a randomized trial in the Gambia, Oman, and Thailand. J Infect Dis 1997; 175(Suppl 1): S Expanded Program of Immunization. Second Meeting of the Technical Consultative Group (TCG) on the Global Eradication of Poliomyelitis, 28 April Geneva: World Health Organization, 1998 (WHO/EPI/ GEN/98.04). 27. Brown F, ed. Progress in polio eradication: vaccine strategies for the end game. Basel, Switzerland: S. Karger (in press). 28. Vaccine & Biologicals. Polio vaccines for the post-eradication era: regulatory and biosafety issues, September Geneva: World Health Organization (in press). Global Polio Eradication Initiative CID 2002:34 (1 January) 77
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