PEDIATRICS Vol. 118 No. 2 August 2006, pp. 611-618 (doi:10.1542/peds.2005-2358)
ARTICLE |
Decision Analysis in Planning for a Polio Outbreak in the United States
a Department of Pediatrics, Dartmouth Medical School, Hanover, New Hampshire
b Children's Hospital at Dartmouth, Lebanon, New Hampshire
| ABSTRACT |
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OBJECTIVE. Global eradication of poliomyelitis may soon be achieved, but circulating polioviruses could reemerge years after eradication by reversion of live attenuated oral vaccine virus to a virulent form, laboratory stock mishandling, or bioterrorism. If a poliomyelitis outbreak occurs in the United States, access to a vaccine stockpile to interrupt viral spread will be necessary. Options for the stockpile include the inactivated polio vaccine and the live-attenuated trivalent and monovalent oral poliovirus vaccines. With differences in immunogenicity, adverse effects, availability, and other issues, the optimal vaccine choice for the stockpile is not clear. We sought to compare vaccine interventions for poliomyelitis outbreak control.
DESIGN. We applied decision analysis to 8 strategies for outbreak control: no intervention, 1 or 2 inactivated polio vaccine doses, 1 or 2 trivalent oral poliovirus vaccine doses, 1 or 2 monovalent oral poliovirus vaccine doses, and sequential inactivated polio vaccine-monovalent oral poliovirus vaccine. Historical data from outbreaks in developed countries were used to estimate the risk of paralytic disease after a hypothetical reintroduction of circulating polioviruses. The outcome measure was cases of paralytic poliomyelitis.
RESULTS. Monovalent oral poliovirus vaccine provided optimal outbreak control in most scenarios because of high seroconversion rates with 1 dose. Control provided by trivalent oral poliovirus vaccine and inactivated polio vaccine was equivalent at high vaccine coverage rates. At low intervention rates, trivalent oral poliovirus vaccine produced fewer paralytic cases than inactivated polio vaccine in highly immune populations but more cases than inactivated polio vaccine in poorly immunized groups because of secondary transmission of oral poliovirus vaccine virus and vaccine-derived viruses.
CONCLUSIONS. This model suggests that monovalent oral poliovirus vaccine would be the most advantageous vaccine for outbreak control. If a monovalent oral poliovirus vaccine stockpile is impractical, the optimal vaccine choice depends on the previous immunity and the anticipated intervention rates.
Key Words: decision-making polio outcomes research outbreak control
Abbreviations: OPVoral poliovirus vaccine VDPVvaccine-derived poliovirus IPVinactivated poliovirus vaccine tOPVtrivalent oral poliovirus vaccine mOPVmonovalent oral poliovirus vaccine VAPPvaccine-associated paralytic polio VDPVvaccine-derived poliovirus
The World Health Organization Global Eradication Program hopes to eliminate paralytic poliomyelitis within the next 1 to 2 years.1,2 However, the recent spread of oral poliovirus vaccine (OPV)-derived live polioviruses in Minnesota3 is a nearby reminder that even after wild-type poliovirus is thought to be eradicated, poliomyelitis may reemerge in poorly immunized groups in any part of the world.4 The risk of reemergence arises from 4 sources5: (1) spread of virulent oral vaccine-derived poliovirus (VDPV) in areas with low population immunity6; (2) immunodeficient, long-term excretors of either wild-type or VDPV polioviruses; (3) release from an inactivated poliovirus vaccine (IPV) manufacturer or other facility that stores virulent polioviruses5; and (4) the unlikely use of preexisting or synthesized7 poliovirus as a bioterrorist weapon. Hence, preparation for an outbreak of virulent poliovirus is prudent. A polio vaccine stockpile must be available for emergency deployment should paralytic poliomyelitis reemerge.8,9
The ideal vaccine choice for the stockpile should be effective in any outbreak scenario, protect all vaccinees with 1 dose, spread to and protect the unvaccinated population, and have no detrimental effect. Although several polio vaccine types and formulations exist, each has advantages and disadvantages, and the best choice for the stockpile is uncertain. IPV is currently used for routine immunization in the United States. Its use precludes the rare occurrence of vaccine-associated paralytic polio that the live attenuated oral vaccines (OPV) can cause in nonimmune recipients,10 and it is the only polio vaccine licensed and distributed in the United States. However, experience with using IPV for outbreak control is limited. Furthermore, IPV requires 2 doses given after the first 6 months of life to generate a high level of immunity, confers little protection to nonimmune contacts, and, in the setting of a wild-type virus outbreak, could itself cause provocation poliomyelitis if given by intramuscular injection.11
The Centers for Disease Control and Prevention Advisory Committee on Immunization Practices prefers OPV for control of poliomyelitis outbreaks, because it confers intestinal immunity, because replication of the live vaccine virus in the intestine interferes with transmission of virulent polioviruses, and because transmission of vaccine viruses can protect nonimmune household contacts.10 Although no longer licensed in the United States, trivalent OPV (tOPV) is used in much of the world for poliomyelitis prevention. Trivalent OPV induces mucosal immunity and may spread from vaccinees to unimmunized contacts but requires several doses to confer complete immunity because of interference among the poliovirus serotypes in the vaccine. Separate monovalent OPVs (mOPVs) have recently become available for special use in the Global Poliomyelitis Eradication Program.12 Although less useful for routine immunization than IPV or tOPV, mOPV provides theoretical advantages for outbreak control: each monovalent vaccine is highly immunogenic in a single dose; it can spread to nonimmune contacts; and its use would avoid reintroduction of 2 unnecessary vaccine-serotype viruses into a posteradication environment.13 However, both mOPV and tOPV can potentially cause vaccine-associated paralytic polio (VAPP) in nonimmune vaccinees, and, if they circulate in a poorly immunized population, can eventually revert to virulence in the form of VDPVs. In addition, regulatory issues present a major barrier to the acquisition of tOPV or mOPV from either domestic or foreign manufacturers.
We sought to determine which vaccine would provide optimal protection from paralytic poliomyelitis once an outbreak in the United States is detected. We used decision analysis to incorporate available data on vaccine immunogenicity; transmission of wild virus, vaccine virus, and vaccine-derived virus; and susceptibility in the population, as well as unknown probabilities, such as the percentage of the population infected before the outbreak is detected, to compare the outcomes of the vaccine interventions. We also sought to assess how changing the probabilities for events and immunity levels would alter the optimal strategy.
| METHODS |
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Outcome Measure
We measured the predicted number of cases of paralytic poliomyelitis from virulent poliovirus, VAPP, provocation polio, or VDPV in the setting of a type 1 poliovirus outbreak.
Decision Tree
Decision analysis is a technique for modeling a complex problem that has risk-benefit trade-offs and incomplete information.14,15 It structures the problem into choices, events or consequences, and outcome measures. By comparing the outcomes of potential treatment strategies, we can determine which choice is best. Decision analysis can also identify the probabilities that influence the optimal strategy using sensitivity analysis.
A decision tree16 was constructed with 8 branches, each representing an intervention that might be adopted by public health officials in the event of an outbreak (Fig 1). We compared the outcome of 7 vaccine strategies with the modeled natural course of the outbreak in which there was no vaccination response (ie, "do nothing"). The model predicts the morbidity resulting from a hypothetical outbreak of poliomyelitis in the United States, using current information, as well as projections for future immunization rates. The decision tree incorporates the likelihood of immunity from previous vaccination or past exposure to OPV viruses; the likelihood of developing new immunity for each intervention; the risk of VAPP and paralysis from VDPV for nonimmune persons in the interventions using OPV and the risk of provocation poliomyelitis in the strategies using IPV; the risk of infection by the virulent poliovirus strain; and the chance of infected persons spreading virulent polioviruses. We used sensitivity analysis to explore the effects of changing: (1) the rates of immunity, (2) the population's acceptance of the intervention, (3) intestinal immunity for past OPV vaccines, (4) seroconversion rates for each vaccine, and (5) the extent of community infection before a case of paralytic polio is discovered.
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Probabilities
Baseline probabilities and sensitivity analysis ranges were obtained from the literature, as shown in Table 1. When no information was available, probabilities were imputed and tested with wide-range sensitivity analysis.
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Assumptions
First, probabilities derived from global outbreak and immunization literature can be used for baseline probabilities to model a potential US outbreak. Second, the "population-at-risk" is composed of all persons of any age potentially exposed to virulent poliovirus, including immune and nonimmune persons. The intervention rate is the percentage of the population at risk that receives a new vaccination. Third, virulent poliovirus spread continues until sufficient population immunity develops, by natural infection and vaccination, to interrupt transmission. Fourth, previous immunity does not prevent a new poliovirus infection, but does decrease its probability.17 IPV-induced immunity is less protective than OPV-induced immunity. The intestinal immunity of previous OPV recipients wanes18 but confers some protection against becoming infected with new poliovirus compared with previous IPV vaccination. Fifth, secondary OPV virus spread has a greater relative impact on population immunity at lower intervention rates19,20 and can be modeled as a second-order equation. The highest probability of secondary OPV spread is assumed to be 50%, as shown in Fig 2. Sixth, the potential to derive VDPV from intervention with any oral vaccine is limited to populations with low vaccination coverage21 and can be modeled as a
function, as shown in Fig 2. Seventh, the risk of paralytic poliomyelitis caused by wild-type poliovirus, VAPP, or VDPV for previously immune persons is 0. Only nonimmune persons are at risk for paralysis.22 Lastly, the type of vaccine and route of administration does not affect the acceptance of polio vaccination in an outbreak.23,24
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Sensitivity Analysis
One- and 2-way sensitivity analyses were performed for each probability in the decision tree, and the values at which the optimal strategy changed (threshold values) were identified.
Statistical Analysis
Decision analysis does not generate P values. Comparing 2 strategies for a statistically significant difference in the outcome depends on the number of patients in the trial, among other things. Because decision analysis produces the probability of an outcome in a hypothetical population, the size of the population could be 10 people or 10 million people, and significance would vary accordingly. Clinical judgment must determine whether the difference in outcomes between strategies in a decision analysis is important.
| RESULTS |
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Using baseline probabilities, a strategy of doing nothing to interrupt poliovirus transmission in a type 1 outbreak resulted in 36 cases of paralytic poliomyelitis per 100000 population at risk for poliovirus infection in a well-immunized population with only 8% susceptibility to paralysis. In a poorly immunized population, where 50% are susceptible to paralysis, the rate of paralytic poliomyelitis increased to 243 per 100000 at risk for infection.
Relative Effectiveness of Interventions Using Baseline Probabilities
Fig 3 shows the relative effectiveness of the intervention strategies compared with the do-nothing strategy for a well-immunized population. With an intervention rate of 70%, vaccination in response to an identified poliovirus infection prevented between 22% and 75% of these cases. mOPV was the most successful vaccination strategy, preventing 75% of the expected number of cases of paralytic polio with the first dose. The outcomes for the mOPV 1-dose and 2-dose strategies were almost identical because of the high seroconversion rate after the first dose of mOPV. mOPV was also the optimal choice when values for types 2 and 3 poliovirus outbreaks were used.
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The relative effectiveness of intervention with IPV versus tOPV becomes important if a mOPV stockpile is not feasible because of regulatory issues. Figure 3 shows that the 2-dose tOPV strategy was slightly more effective than the 2-dose IPV strategy, preventing 3 more cases of paralytic polio per 100000 at risk under baseline probabilities.
Sensitivity Analysis
We varied the probabilities of each factor in Table 1 throughout its stated range to determine whether changing any probabilities, especially those inferred or assumed, would alter the optimal strategy. One- and 2-way sensitivity analyses were performed for each factor. In most realistic sensitivity analyses, mOPV remained the optimal vaccine for outbreak control (Fig 4 A). Sensitivity analysis on the rate of VAPP as a complication of either mOPV or tOPV use had no measurable impact on the anticipated number of cases.
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However, mOPV was not the optimal choice in controlling a wild-type virus outbreak in a poorly immune population that may shun the control measure. At 50% exposure to poliovirus and <20% vaccine uptake (Fig 4B), IPV was preferable to the oral vaccines. If the virus had only 10% penetration in the population, IPV would be the optimal choice for an uptake of
40%. These results were because of the risk of VDPV in strategies using oral vaccine at low intervention rates.
Attack Rates
Case rates in a polio outbreak changed depending on the vaccination strategy and the intervention rate for a well-immunized population (Fig 4A) and for a poorly immunized population (Fig 4B). Higher intervention rates were more successful in protecting the population for every vaccine strategy. For previous immunity rates of 92%, as shown in Fig 4A, the greatest benefit of mOPV over other strategies occurred at intervention rates of
80%. At low anticipated rates of intervention, the advantage of mOPV over tOPV was very small.
The previous immunity rate had an even larger effect on the number of cases than the intervention rate. Some past poliomyelitis outbreaks have occurred in underimmunized, culturally defined groups living within or among a larger well-immunized population. In the situation of an outbreak in a group in which 50% of the population was susceptible to paralytic poliomyelitis (Fig 4B), an almost sevenfold increase in the number of cases, totaling 243 cases per 100000 population at risk for infection, would be expected if no intervention occurred. A 2-dose intervention with mOPV reaching 70% of the population at risk would prevent 76%, or 184, cases of paralysis compared with doing nothing. Two doses of tOPV decreased the expected caseload by 158, and 2 doses of IPV lessened the expected caseload by 144. For a group that allowed only a 20% intervention rate for 2 doses of vaccine, intervention with IPV prevented
42 cases, and vaccination with tOPV prevented
31 cases of paralysis.
The sensitivity analyses in Fig 4 also showed how the optimal strategy would change if mOPV were not available. For an intervention rate of 20%, 2 doses of tOPV prevented 5 more cases of paralysis per 100000 in a highly immune population (Fig 4A) but allowed 11 more cases per 100000 in a poorly immunized population (Fig 4B) than did 2 doses of IPV. At high intervention rates, the protection provided by 2 doses of tOPV or IPV was comparable; the choice between tOPV and IPV was not as important as delivering 2 doses of either vaccine. The relative effectiveness of tOPV and IPV did not change in simulations of type 2 and type 3 outbreaks.
| DISCUSSION |
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In most polio outbreak scenarios tested, mOPV vaccine strategies resulted in the fewest cases of paralysis. The advantage of the monovalent polio vaccines is because of their superior immunogenicity. One dose of type 1, type 2, or type 3 mOPV induces neutralizing antibodies in 95%, 98%, and 94% of nonimmune recipients, respectively,13 substantially higher than the seroconversion rates after 1 dose of either tOPV or IPV.25,26
The predicted number of poliomyelitis cases varied with changes in the nonimmune proportion of the population and with the proportion vaccinated in the outbreak response (Fig 4). When the intervention reached the majority of the population, mOPV was the optimal choice, and tOPV was slightly more effective than IPV. IPV provided an advantage over OPV in situations of low vaccine acceptance, because live vaccine viruses may revert to virulence in poorly immunized populations.
Our decision tree model was designed to apply to a population of any size capable of sustained poliovirus transmission, including a relatively closed community or the general populace, in the United States or in any temperate-zone developed country. The attack rates of paralytic poliomyelitis generated by the model are consistent with outbreak data from the United States before the control of poliomyelitis and from other countries.27 Some information necessary for modeling a poliomyelitis outbreak is not known. Inferred and assumed values in Table 1 were tested using wide-range sensitivity analysis to determine whether the optimal strategy would change if our assumptions and baseline values were wrong. Although the optimal vaccine choice depended on a number of factors if the intervention rate was low, mOPV was the optimal choice for all scenarios with high intervention rates.
Public Health
Previously immune persons will not develop paralysis but may become infected with virulent polioviruses and transmit them to nonimmune contacts. If the population at risk is largely immune, the attack rate will be far lower than if the population is mostly nonimmune before the outbreak. A high intervention rate will also prevent many cases of paralytic polio that would occur if nothing were done. These parameters, previous immunity and acceptance of new vaccination in an outbreak, may be linked. The vaccination rate may improve in a poorly immunized population experiencing a poliovirus outbreak, but religious or cultural beliefs may restrict vaccine acceptance even when paralytic polio is identified, regardless of vaccine type.23,24 When outbreaks have occurred in developed countries, they have generally resulted from spread of virulent polioviruses within poorly vaccinated communities with a common religious or cultural heritage and have not spread more widely to the general population.28
The likelihood of a paralytic poliomyelitis outbreak in the United States is now very low, because the immunity level against poliomyelitis far exceeds the 80% level estimated for herd immunity.27 More than 90% of 2- to 3-year-old children have received 3 doses of polio vaccine since the mid-1990s, and school entry immunization requirements have increased immunization rates to >95% for children
6 years of age.29 Underimmunization among preschool children residing in disadvantaged communities remains a concern; however, recent data from a seroprevalence survey of inner city children are reassuring. This study, conducted in New York, NY; Detroit, MI; Denver, CO; and San Diego, CA, from 1997 to 2001, found that >90% of 2- to 3-year-old preschool children had neutralizing antibodies to all 3 of the poliovirus serotypes.30
Should the routine immunization rate fall to a level that enables transmission of the virulent strain, an outbreak of paralytic poliomyelitis could occur. A future outbreak could be caused by a single infected person who spreads virulent poliovirus to nonimmune contacts here in the United States. Conversely, a large exposure, such as a bioterrorist attack, could result in widespread infection. Although polio is a poor choice for bioterrorism, given its attack rate of only 1 case of paralysis per 100 nonimmune infected persons and the availability of an effective vaccine response, an appropriate stockpile strategy should be able to meet such a situation. mOPV was the optimal choice for both small-scale and large-scale exposures, if the majority of the susceptible population can be vaccinated.
The regulatory issues associated with creating a polio vaccine stockpile are challenging. IPV is now the only polio vaccine licensed and distributed in the United States. The acquisition of a live vaccine stockpile from domestic manufacturers is not possible, but tOPV may be readily obtained on the international market, and mOPV is now being manufactured abroad. However, without licensing in the United States, the oral vaccines would be considered investigational medications, even in a public health emergency, such as a widespread poliomyelitis outbreak. The differences in the expected number of cases, depending on vaccine choice, were in some scenarios very small and may or may not be meaningful in a public health context. Whether preventing more cases of paralytic polio is worth the cost of developing and maintaining a stockpile of mOPV or tOPV is beyond the scope of this study.
Limitations
This decision analysis addressed the relative impact of strategies to limit virus spread after the discovery of an outbreak. It did not attempt to assess the spread of live polioviruses before a case of poliomyelitis emerges. Although a disease transmission model has been developed,31 the size and identification of the population at risk will not affect the optimal vaccine choice.
Our model addressed exposure to virulent VDPV by the distribution shown in Fig 2; however, the actual risk distribution for exposure to VDPV after OPV use is not known. This risk is likely quite small. Worldwide, only 82 persons developed paralytic disease from VDPV between January 2000 and January 2006 compared with 7092 cases of naturally occurring paralytic poliomyelitis.32 However, because the risk persists for a currently undefined number of years after OPV use,21 we emphasized this risk as opposed to minimizing it. Because we assumed that all virus transmission would occur in closed settings, such as households and day care centers, via fecal-oral transmission and not in the open community via respiratory transmission, the model retains a bias against IPV, which has little effect on fecal excretion, limiting transmission via the respiratory route.
| CONCLUSIONS |
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On detection of a first case of paralytic poliomyelitis, the federal government will deploy its stockpile vaccine to the population at risk for poliovirus infection. The success of this intervention in preventing paralytic poliomyelitis will depend on the new vaccination rate and on the effectiveness of the vaccine in halting the spread of virulent poliovirus in immunized and nonimmunized groups at risk for infection. This study addressed the effectiveness of potential vaccination strategies for preventing cases of paralytic poliomyelitis at several levels of preexisting immunity, inoculation size, vaccination rate, and virus spread to inform the choice of the stockpile vaccine for use in such an outbreak.
Our decision analysis shows that use of mOPV in response to an outbreak caused by any of the 3 polio vaccine serotypes generally resulted in fewer paralytic poliomyelitis cases than use of either tOPV or IPV. IPV would be preferable to the oral vaccines in some scenarios. Because no live vaccine is currently licensed or manufactured in the United States, the creation of a national polio vaccine stockpile of either mOPV or tOPV represents a special regulatory challenge that will require collaboration of the federal government with vaccine manufacturers, the World Health Organization, and other international health partners.9 Should mOPV become available as either a domestic or a global supply, it would be the vaccine of choice for outbreak control in the United States.
| ACKNOWLEDGMENTS |
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This research was supported by Mentored Clinical Scientist Development Awards to Dr Jenkins from the Doris Duke Charitable Foundation and the Agency for Healthcare Research and Quality.
We thank Victor Caceres, MD, Margaret Watkins, MPH, BSN, Trudy Murphy, MD, Lorraine Alexander, RN, MPH, and Charles LeBaron, MD, from the Centers for Disease Control and Prevention for reviewing the decision analysis and advising us on regulatory issues associated with the polio vaccine stockpile.
| FOOTNOTES |
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Accepted Mar 2, 2006.
Address correspondence to Pamela C. Jenkins, MD, PhD, Department of Pediatrics, Dartmouth Medical School, Hanover, NH 03756. E-mail: pcj{at}hitchcock.org
The authors have indicated they have no financial relationships relevant to this article to disclose.
| REFERENCES |
|---|
|
|
|---|
- Roberts L. Polio: the final assault?
Science. 2004;303
:1960
1968
[Abstract/Free Full Text] - World Health Organization. Progress towards interruption of wild poliovirus transmission, January 2004 to March 2005. Week Epidemiol Rec. 2005;80 :149 156
- Centers for Disease Control and Prevention. Poliovirus infections in four unvaccinated children Minnesota, AugustOctober 2005. MMWR Morb Mortal Wkly Rep. 2005;54 :1053 1055[Medline]
- World Health Organization. Wild poliovirus, 22 Feb 2005 to 21 Feb 2006. 21 February 2006. Available at: www.polioeradication.org/content/fixed/casemap.shtml. Accessed February 27, 2006
- Aylward R, Cochi S. Framework for evaluating the risks of paralytic poliomyelitis after global interruption of wild poliovirus transmission. Bull WHO. 2004;82 :40 46[Web of Science][Medline]
- Modlin J. Poliomyelitis in the United States: the final chapter?
JAMA. 2004;292
:1749
1751
[Free Full Text] - Cello J, Paul A, Wimmer E. Chemical synthesis of poliovirus cDNA: generation of infectious virus in the absence of natural template.
Science. 2002;297
:1016
1018
[Abstract/Free Full Text] - Technical Consultative Group to the World Health Organization on the Global Eradication of Poliomyelitis. "Endgame" issues for the global polio eradication initiative. Clin Infect Dis. 2002;34 :72 77[CrossRef][Web of Science][Medline]
- NVAC-ACIP Joint Working Group and Centers for Disease Control and Prevention. Ensuring preparedness for potential poliomyelitis outbreaks. Recommendations for the US Poliovirus Vaccine Stockpile from the National Vaccine Advisory Committee (NVAC) and the Advisory Committee on Immunization Practices (ACIP).
Arch Ped Adol Med. 2004;158
:1106
1112
[Abstract/Free Full Text] - Centers for Disease Control and Prevention. Poliomyelitis prevention in the United States. MMWR Morb Mort Wkly Rep. 2000;49 :1 22[Medline]
- Sutter R, Patriarca P, Suleiman A, et al. Attributable risk of DTP (diphtheria and tetanux toxoids and pertussis vaccine) injection in provoking paralytic poliomyelitis during a large outbreak in Oman. J Infect Dis. 1992;165 :444 449[Web of Science][Medline]
- World Health Organization. Polio Outbreak Spreads Across Yemen. Available at: www.who.int/mediacentre/news/releases/2005/pr19/en/index.html. Accessed May 6, 2005.
- Caceres V, Sutter R. Sabin monovalent oral polio vaccines: review of past experiences and their potential use after polio eradication. Clin Infect Dis. 2001;33 :531 541[CrossRef][Web of Science][Medline]
- Detsky A, Naigle G, Krahn M, Naimark D, Redelmeier DA. Primer on medical decision analysis: Part 1 getting started.
Med Decis Making. 1997;17
:123
125
[Abstract/Free Full Text] - Weinstein M, Fineberg H. Clinical Decision Analysis. Philadelphia, PA: WB Saunders; 1980
- TreeAge Pro [computer program]. Williamstown, MA: TreeAge Software, Inc; 2005
- Oronato I, Modlin J, McBean A, et al. Mucosal immunity induced by enhanced-potency inactivated and oral polio vaccines. J Infect Dis. 1991;163 :1 6[Web of Science][Medline]
- Nishio O, Ishihara Y, Sakae K, Thoms ML, Losonsky GA, Bernier RH. The trend of acquired immunity with live poliovirus vaccine and the effect of revaccination: follow-up of vaccinees for ten years. J Biol Stand. 1984;12 :1 10[Web of Science][Medline]
- Kimball A, Barr R, Bauer H, Kleinman H, Johnson EA, Cooney MK. Community spread of orally administered attenuated poliovirus vaccine strains. Pub Health Rep. 1961;76 :903 914[Web of Science][Medline]
- Gelfand H, LeBlanc D, Potash L, Clemmer DI, Fox JP. The spread of living attenuated strains of polioviruses in 2 communities in southern Louisiana.
Am J Public Health. 1960;50
:767
778
[Free Full Text] - Kew O, Wright P, Agol V, et al. Circulating vaccine-derived polioviruses: current state of knowledge. Bull WHO. 2004;82 :16 23[Web of Science][Medline]
- Nkowane B, Wassilak S, Orenstein W, et al. Vaccine-associated paralytic poliomyelitis. United States: 1973 through 1984.
JAMA. 1987;257
:1335
1340
[Abstract/Free Full Text] - Bijkerk H. Poliomyelitis epidemic in the Netherlands, 1978. Dev Biol Stand. 1979;43 :195 206[Medline]
- Van Wijngaarden J, van Loon A. The polio epidemic in The Netherlands, 1992/1993. Public Health Rev. 1994;21 :107 116
- McBean A, Thoms M, Albrecht P, et al. The serologic response to oral polio vaccine and enhanced potency inactivated polio vaccines.
Am J Epidemiol. 1988;128
:615
628
[Abstract/Free Full Text] - Cohen-Abbo A, Culley B, Reed G, et al. Seroresponse to trivalent oral poliovirus vaccine as a function of dosage interval. Ped Infect Dis J. 1995;14 :100 106[Web of Science]
- Patriarca P, Sutter R, Oostvogel P. Outbreaks of paralytic poliomyelitis, 19761995. J Infect Dis. 1997;175 :S165 S172[Web of Science][Medline]
- Schaap G, Bijkerk H, Coutinho R, et al. The spread of wild poliovirus in the well-vaccinated Netherlands in connection with the 1978 epidemic. Prog Med Virol. 1984;29 :124 140[Web of Science][Medline]
- Centers for Disease Control and Prevention. National Immunization Program. Immunization coverage in the US. Available at: www.cdc.gov/nip/coverage/default.htm#chart. Accessed September 15, 2004.
- Prevots D, Pascual F, Angellili M, et al. Population immunity to polioviruses among preschool children from four urban low-income communities, United States, 19972001. Ped Infect Dis J. 2004;23 :1130 1136[Web of Science]
- Tebbens R, Pallansch M, Kew O, et al. A dynamic model of poliomyelitis outbreaks: learning from the past to help inform the future.
Am J Epidemiol. 2005;162
:358
372
[Abstract/Free Full Text] - World Health Organization. Polio Case Count. 16 February 2006. Available at: www.who.int/vaccines/immunization_monitoring/en/diseases/poliomyelitis/case_count.cfm. Accessed February 27, 2006
- Chen R, Hausinger S, Dajani A, et al. Seroprevalence of antibody against poliovirus in inner-city preschool children.
JAMA. 1996;275
:1639
1645
[Abstract/Free Full Text] - Modlin J, Halsey N, Thoms M, et al. Humoral and mucosal immunity in infants induced by three sequential IPV-OPV immunization schedules. J Infect Dis. 1997;75 :S228 S234
- Gelfand H, Fox J, LeBlanc D. Observations on natural poliovirus infection in immunized children.
Am J Public Health. 1957;47
:421
431
[Free Full Text] - Gelfand H, LeBlanc D, Potash L, et al. Studies on the development of natural immunity to poliomyelitis in Louisiana. IV. Natural infections with polioviruses following immunization with a formalin-inactivated vaccine. Am J Hyg. 1959;70 :312 327[Web of Science][Medline]
- Gelfand H, LeBlanc D, Fox J, et al. Studies on the development of natural immunity to poliomyelitis in Louisiana. II. Description and analysis of episodes of infection observed in study group households. Am J Hyg. 1957;65 :367 385[Web of Science][Medline]
- Melnick J, Ledinko N. Social serology: antibody levels in a normal young population during an epidemic of poliomyelitis. Am J Hyg. 1951;54 :354 382[Web of Science][Medline]
- Horstmann D. Clinical aspects of acute poliomyelitis. Am J Med. 1949;6 :592[CrossRef][Web of Science][Medline]
- Prevots D, Sutter R, Strebel P, et al. Completeness of reporting for paralytic poliomyelitis, United States, 1980 through 1991.
Arch Ped Adol Med. 1994;148
:479
485
[Abstract/Free Full Text] - Alexander L, Seward J, Santibanez T, et al. Vaccine policy changes and epidemiology of poliomyelitis in the United States.
JAMA. 2004;292
:1696
1701
[Abstract/Free Full Text] - Domok I. Experiences associated with the use of live poliovirus vaccine in Hungary, 19591982. Rev Infect Dis. 1984;6 (suppl 2):S413S418
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