Oral Poliovirus Vaccine Evolution and Insights Relevant to Modeling the Risks of Circulating Vaccine‐Derived Polioviruses (cVDPVs)

The live, attenuated oral poliovirus vaccine (OPV) provides a powerful tool for controlling and stopping the transmission of wild polioviruses (WPVs), although the risks of vaccine‐associated paralytic polio (VAPP) and circulating vaccine‐derived poliovirus (cVDPV) outbreaks exist as long as OPV remains in use. Understanding the dynamics of cVDPV emergence and outbreaks as a function of population immunity and other risk factors may help to improve risk management and the development of strategies to respond to possible outbreaks. We performed a comprehensive review of the literature related to the process of OPV evolution and information available from actual experiences with cVDPV outbreaks. Only a relatively small fraction of poliovirus infections cause symptoms, which makes direct observation of the trajectory of OPV evolution within a population impractical and leads to significant uncertainty. Despite a large global surveillance system, the existing genetic sequence data largely provide information about transmitted virulent polioviruses that caused acute flaccid paralysis, and essentially no data track the changes that occur in OPV sequences as the viruses transmit largely asymptomatically through real populations with suboptimal immunity. We updated estimates of cVDPV risks based on actual experiences and identified the many limitations in the existing data on poliovirus transmission and immunity and OPV virus evolution that complicate modeling. Modelers should explore the space of potential model formulations and inputs consistent with the available evidence and future studies should seek to improve our understanding of the OPV virus evolution process to provide better information for policymakers working to manage cVDPV risks.

[1]  R. Sutter,et al.  Vaccine-derived polioviruses. , 2014, The Journal of infectious diseases.

[2]  R. D. Tebbens,et al.  Modeling Population Immunity to Support Efforts to End the Transmission of Live Polioviruses , 2013, Risk analysis : an official publication of the Society for Risk Analysis.

[3]  M. Pallansch,et al.  Expert Review on Poliovirus Immunity and Transmission , 2013, Risk analysis : an official publication of the Society for Risk Analysis.

[4]  M. Pallansch,et al.  Characterizing Poliovirus Transmission and Evolution: Insights from Modeling Experiences with Wild and Vaccine‐Related Polioviruses , 2013, Risk analysis : an official publication of the Society for Risk Analysis.

[5]  F. Delpeyroux,et al.  Common and diverse features of cocirculating type 2 and 3 recombinant vaccine-derived polioviruses isolated from patients with poliomyelitis and healthy children. , 2012, The Journal of infectious diseases.

[6]  O. Kew Reaching the last one per cent: progress and challenges in global polio eradication. , 2012, Current opinion in virology.

[7]  Yong Zhang,et al.  [Analysis of genetic characteristics of type II non-wild poliovirus in mainland China, 2010]. , 2012, Bing du xue bao = Chinese journal of virology.

[8]  Z. Molnár,et al.  Paralytic poliomyelitis associated with Sabin monovalent and bivalent oral polio vaccines in Hungary. , 2011, American journal of epidemiology.

[9]  F. Delpeyroux,et al.  Recombination between Poliovirus and Coxsackie A Viruses of Species C: A Model of Viral Genetic Plasticity and Emergence , 2011, Viruses.

[10]  M. Pate,et al.  Outbreak of Type 2 Vaccine-Derived Poliovirus in Nigeria: Emergence and Widespread Circulation in an Underimmunized Population , 2011, The Journal of infectious diseases.

[11]  Wenbo Xu,et al.  Type 2 vaccine-derived poliovirus from patients with acute flaccid paralysis in china: current immunization strategy effectively prevented its sustained transmission. , 2010, The Journal of infectious diseases.

[12]  N. Nathanson,et al.  From Emergence to Eradication: The Epidemiology of Poliomyelitis Deconstructed , 2010, American journal of epidemiology.

[13]  W. Liu,et al.  Emergence and Localized Circulation of a Vaccine-Derived Poliovirus in an Isolated Mountain Community in Guangxi, China , 2010, Journal of Clinical Microbiology.

[14]  Z. Molnár,et al.  Molecular characterization of poliovirus isolates from children who contracted vaccine-associated paralytic poliomyelitis (VAPP) following administration of monovalent type 3 oral poliovirus vaccine in the 1960s in Hungary. , 2010, FEMS immunology and medical microbiology.

[15]  J. van de Kassteele,et al.  Shedding of Vaccine Viruses with Increased Antigenic and Genetic Divergence after Vaccination of Newborns with Monovalent Type 1 Oral Poliovirus Vaccine , 2009, Journal of Virology.

[16]  P. Minor Vaccine-derived poliovirus (VDPV): Impact on poliomyelitis eradication. , 2009, Vaccine.

[17]  Claire Blanchard,et al.  Recombination between Polioviruses and Co-Circulating Coxsackie A Viruses: Role in the Emergence of Pathogenic Vaccine-Derived Polioviruses , 2009, PLoS pathogens.

[18]  J. P. Davis,et al.  Transmission of imported vaccine-derived poliovirus in an undervaccinated community in Minnesota. , 2009, The Journal of infectious diseases.

[19]  P. Fine,et al.  Estimating the Extent of Vaccine-Derived Poliovirus Infection , 2008, PloS one.

[20]  Kimberly M Thompson,et al.  The risks, costs, and benefits of possible future global policies for managing polioviruses. , 2008, American journal of public health.

[21]  M. Birmingham,et al.  Reemergence of recombinant vaccine-derived poliovirus outbreak in Madagascar. , 2008, The Journal of infectious diseases.

[22]  O. Kew,et al.  Calibration of Multiple Poliovirus Molecular Clocks Covering an Extended Evolutionary Range , 2008, Journal of Virology.

[23]  M. Pallansch,et al.  A large vaccine-derived poliovirus outbreak on Madura Island--Indonesia, 2005. , 2008, The Journal of infectious diseases.

[24]  R. Sutter,et al.  Poliovirus vaccine-live , 2008 .

[25]  D. Earn,et al.  Circulating Vaccine Derived Polio Viruses and their Impact on Global Polio Eradication , 2008, Bulletin of mathematical biology.

[26]  Kimberly M Thompson,et al.  The case for cooperation in managing and maintaining the end of poliomyelitis: stockpile needs and coordinated OPV cessation. , 2008, Medscape journal of medicine.

[27]  E. Wimmer,et al.  Vaccination against polio should not be stopped , 2007, Nature Reviews Microbiology.

[28]  Javier Martin,et al.  Co-Circulation and Evolution of Polioviruses and Species C Enteroviruses in a District of Madagascar , 2007, PLoS pathogens.

[29]  M. Pallansch,et al.  Isolation of recombinant type 2 vaccine-derived poliovirus (VDPV) from a Nigerian child. , 2007, Virus research.

[30]  S. Guillot,et al.  Circulation of a type 1 recombinant vaccine-derived poliovirus strain in a limited area in Romania , 2007, Archives of Virology.

[31]  Kimberly M Thompson,et al.  Risks of Paralytic Disease Due to Wild or Vaccine‐Derived Poliovirus After Eradication , 2006, Risk analysis : an official publication of the Society for Risk Analysis.

[32]  Wenbo Xu,et al.  An outbreak of poliomyelitis caused by type 1 vaccine-derived poliovirus in China. , 2006, The Journal of infectious diseases.

[33]  V. Agol Vaccine-derived polioviruses. , 2006, Biologicals : journal of the International Association of Biological Standardization.

[34]  M. Rennels,et al.  Analysis of reversions in the 5'-untranslated region of attenuated poliovirus after sequential administration of inactivated and oral poliovirus vaccines. , 2006, The Journal of infectious diseases.

[35]  Julie K. Pfeiffer,et al.  Bottleneck-mediated quasispecies restriction during spread of an RNA virus from inoculation site to brain. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[36]  M. Vignuzzi,et al.  Quasispecies diversity determines pathogenesis through cooperative interactions in a viral population , 2006, Nature.

[37]  Update on vaccine-derived polioviruses. , 2006, MMWR. Morbidity and mortality weekly report.

[38]  V. Agol Molecular mechanisms of poliovirus variation and evolution. , 2006, Current topics in microbiology and immunology.

[39]  Pei-Jer Chen,et al.  Intratypic Recombination among Lineages of Type 1 Vaccine-Derived Poliovirus Emerging during Chronic Infection of an Immunodeficient Patient , 2005, Journal of Virology.

[40]  M. Pallansch,et al.  Vaccine-derived polioviruses and the endgame strategy for global polio eradication. , 2005, Annual review of microbiology.

[41]  Kimberly M Thompson,et al.  A dynamic model of poliomyelitis outbreaks: learning from the past to help inform the future. , 2005, American journal of epidemiology.

[42]  E. Wimmer,et al.  Poliovirus and poliomyelitis: a tale of guts, brains, and an accidental event. , 2005, Virus research.

[43]  G. Dunn,et al.  Effect of different immunisation schedules on the excretion and reversion of oral poliovaccine strains , 2005, Journal of medical virology.

[44]  T. Nomura,et al.  Genetic basis of the neurovirulence of type 1 polioviruses isolated from vaccine-associated paralytic patients , 2005, Archives of Virology.

[45]  W. Hall,et al.  Long-Term Excretion of Vaccine-Derived Poliovirus by a Healthy Child , 2004, Journal of Virology.

[46]  Lilly Yuen,et al.  Circulation of Type 1 Vaccine-Derived Poliovirus in the Philippines in 2001 , 2004, Journal of Virology.

[47]  M. Pallansch,et al.  Vaccine policy changes and epidemiology of poliomyelitis in the United States. , 2004, JAMA.

[48]  Global Polio Eradication Initiative, strategic plan 2004-2008. , 2004, Releve epidemiologique hebdomadaire.

[49]  Laboratory surveillance for wild and vaccine-derived polioviruses, January 2003-June 2004. , 2004, MMWR. Morbidity and mortality weekly report.

[50]  Francis Delpeyroux,et al.  Circulating vaccine-derived polioviruses: current state of knowledge. , 2004, Bulletin of the World Health Organization.

[51]  V. Agol,et al.  Retrospective Analysis of a Local Cessation of Vaccination against Poliomyelitis: a Possible Scenario for the Future , 2003, Journal of Virology.

[52]  M. Pallansch,et al.  Serial Recombination during Circulation of Type 1 Wild-Vaccine Recombinant Polioviruses in China , 2003, Journal of Virology.

[53]  M. Pallansch,et al.  Circulation of Endemic Type 2 Vaccine-Derived Poliovirus in Egypt from 1983 to 1993 , 2003, Journal of Virology.

[54]  D. Rousset,et al.  Recombinant Vaccine–Derived Poliovirus in Madagascar , 2003, Emerging infectious diseases.

[55]  A. Plebani,et al.  Nucleotide variation in Sabin type 2 poliovirus from an immunodeficient patient with poliomyelitis. , 2003, The Journal of general virology.

[56]  M. L. Yakovenko,et al.  Long-Term Circulation of Vaccine-Derived Poliovirus That Causes Paralytic Disease , 2002, Journal of Virology.

[57]  T. Kitamura,et al.  Prevalence of vaccine-derived polioviruses in the environment. , 2002, The Journal of general virology.

[58]  M. Pallansch,et al.  Outbreak of Poliomyelitis in Hispaniola Associated with Circulating Type 1 Vaccine-Derived Poliovirus , 2002, Science.

[59]  R. Sutter,et al.  Vaccine-associated paralytic poliomyelitis in India during 1999: decreased risk despite massive use of oral polio vaccine , 2002 .

[60]  R. Sutter,et al.  Sabin monovalent oral polio vaccines: review of past experiences and their potential use after polio eradication. , 2001, Clinical infectious diseases : an official publication of the Infectious Diseases Society of America.

[61]  S. Guillot,et al.  Genomic Features of Intertypic Recombinant Sabin Poliovirus Strains Excreted by Primary Vaccinees , 2001, Journal of Virology.

[62]  Transmission of wild poliovirus type 2--apparent global interruption. , 2001, Releve epidemiologique hebdomadaire.

[63]  Javier Martin,et al.  The vaccine origin of the 1968 epidemic of type 3 poliomyelitis in Poland. , 2000, Virology.

[64]  T. Kitamura,et al.  Assessment of Poliovirus Eradication in Japan: Genomic Analysis of Polioviruses Isolated from River Water and Sewage in Toyama Prefecture , 2000, Applied and Environmental Microbiology.

[65]  S. Guillot,et al.  Natural Genetic Exchanges between Vaccine and Wild Poliovirus Strains in Humans , 2000, Journal of Virology.

[66]  V. Agol,et al.  Evolution of Circulating Wild Poliovirus and of Vaccine-Derived Poliovirus in an Immunodeficient Patient: a Unifying Model , 2000, Journal of Virology.

[67]  Javier Martin,et al.  Evolution of the Sabin Strain of Type 3 Poliovirus in an Immunodeficient Patient during the Entire 637-Day Period of Virus Excretion , 2000, Journal of Virology.

[68]  A. Heim,et al.  Evolution of poliovirus type I during 5.5 years of prolonged enteral replication in an immunodeficient patient. , 1999, Virology.

[69]  P E Fine,et al.  Transmissibility and persistence of oral polio vaccine viruses: implications for the global poliomyelitis eradication initiative. , 1999, American journal of epidemiology.

[70]  P. McIntyre,et al.  Vaccine-associated paralytic poliomyelitis. , 1999, Communicable diseases intelligence.

[71]  Progress towards global poliomyelitis eradication. The approaching extinction of wild poliovirus type 2. , 1999, Releve epidemiologique hebdomadaire.

[72]  M. Pallansch,et al.  Prolonged Replication of a Type 1 Vaccine-Derived Poliovirus in an Immunodeficient Patient , 1998, Journal of Clinical Microbiology.

[73]  M. Georgescu,et al.  Evolution of the Sabin type 1 poliovirus in humans: characterization of strains isolated from patients with vaccine-associated paralytic poliomyelitis , 1997, Journal of virology.

[74]  R. Linkins,et al.  Sequential use of inactivated poliovirus vaccine followed by oral poliovirus vaccine in Oman. , 1997, The Journal of infectious diseases.

[75]  X. L. Zhang,et al.  Surveillance for polio eradication in the People's Republic of China. , 1997, The Journal of infectious diseases.

[76]  M. Pallansch,et al.  Seroprevalence of antibody against poliovirus in inner-city preschool children. Implications for vaccination policy in the United States. , 1996, JAMA.

[77]  S. Elena,et al.  Basic concepts in RNA virus evolution , 1996, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[78]  K. Chumakov,et al.  Limited genetic changes in the Sabin 1 strain of poliovirus occurring in the central nervous system of monkeys. , 1996, The Journal of general virology.

[79]  H. Schatzmayr,et al.  Poliovirus type 1 isolated from a vaccine-associated case of paralytic poliomyelitis in Brazil. , 1996, Brazilian journal of medical and biological research = Revista brasileira de pesquisas medicas e biologicas.

[80]  J. Meredith,et al.  Role of mutations G-480 and C-6203 in the attenuation phenotype of Sabin type 1 poliovirus , 1995, Journal of virology.

[81]  M. Georgescu,et al.  Tripartite genome organization of a natural type 2 vaccine/nonvaccine recombinant poliovirus. , 1995, The Journal of general virology.

[82]  M. Bouchard,et al.  Determinants of attenuation and temperature sensitivity in the type 1 poliovirus Sabin vaccine , 1995, Journal of virology.

[83]  H. Schatzmayr,et al.  Genomic characterization of type 1 Sabin-related polioviruses isolated in Brazil. , 1995, Acta virologica.

[84]  J. Modlin,et al.  Vaccine-Associated Paralytic Poliomyelitis , 1994, Journal of child neurology.

[85]  Z. Lu,et al.  Microevolution of Sabin 1 strain in vitro and genetic stability of oral poliovirus vaccine. , 1994, Virology.

[86]  S. Guillot,et al.  Point mutations involved in the attenuation/neurovirulence alternation in type 1 and 2 oral polio vaccine strains detected by site-specific polymerase chain reaction. , 1994, Vaccine.

[87]  S. Koike,et al.  Transgenic mice carrying the human poliovirus receptor: new animal models for study of poliovirus neurovirulence , 1994, Journal of virology.

[88]  J. Andrus,et al.  Lessons from Cuba: mass campaign administration of trivalent oral poliovirus vaccine and seroprevalence of poliovirus neutralizing antibodies. , 1994, Bulletin of the World Health Organization.

[89]  M. Furione,et al.  Polioviruses with natural recombinant genomes isolated from vaccine-associated paralytic poliomyelitis. , 1993, Virology.

[90]  F. Tekaia,et al.  A mutation in the RNA polymerase of poliovirus type 1 contributes to attenuation in mice , 1993, Journal of virology.

[91]  M. Furione,et al.  Genomic modifications in naturally occurring neurovirulent revertants of Sabin 1 polioviruses. , 1993, Developments in biological standardization.

[92]  S. R. Pollard,et al.  Genetic basis of attenuation of the Sabin type 2 vaccine strain of poliovirus in primates. , 1993, Virology.

[93]  P. Minor The molecular biology of poliovaccines. , 1992, The Journal of general virology.

[94]  G. Schild,et al.  A mutation present in the amino terminus of Sabin 3 poliovirus VP1 protein is attenuating , 1992, Journal of virology.

[95]  K. Dimock,et al.  Genetic characterization of Sabin types 1 and 3 poliovaccine virus following serial passage in the human intestinal tract. , 1992, Biologicals : journal of the International Association of Biological Standardization.

[96]  M. Pallansch,et al.  Epidemiology of poliomyelitis in the United States one decade after the last reported case of indigenous wild virus-associated disease. , 1992, Clinical infectious diseases : an official publication of the Infectious Diseases Society of America.

[97]  V. Agol,et al.  Frequent isolation of intertypic poliovirus recombinants with serotype 2 specificity from vaccine‐associated polio cases , 1991, Journal of medical virology.

[98]  C. Weeks-Levy,et al.  Identification and characterization of a new base substitution in the vaccine strain of Sabin 3 poliovirus. , 1991, Virology.

[99]  V. Agol,et al.  Coupled mutations in the 5'-untranslated region of the Sabin poliovirus strains during in vivo passages: structural and functional implications. , 1991, Virus research.

[100]  L. M. Onotato MUCOSAL IMMUNITY INDUCED BY ENHANCED POTENCY INACTIVATED AND ORAL POLIO VACCINES , 1991 .

[101]  L. Fiore,et al.  Identification of a consistent pattern of mutations in neurovirulent variants derived from the sabin vaccine strain of poliovirus type 2 , 1991, Journal of virology.

[102]  S. R. Pollard,et al.  The 5' noncoding region of the type 2 poliovirus vaccine strain contains determinants of attenuation and temperature sensitivity. , 1991, Virology.

[103]  R. Ren,et al.  Identification of two determinants that attenuate vaccine-related type 2 poliovirus , 1991, Journal of virology.

[104]  C. Wychowski,et al.  Use of type 1/type 2 chimeric polioviruses to study determinants of poliovirus type 1 neurovirulence in a mouse model. , 1991, Virology.

[105]  I. Onorato,et al.  Mucosal immunity induced by enhance-potency inactivated and oral polio vaccines. , 1991, The Journal of infectious diseases.

[106]  G. Dunn,et al.  Virus excretion and mutation by infants following primary vaccination with live oral poliovaccine from two sources , 1990, Journal of medical virology.

[107]  C. Christodoulou,et al.  Mapping of mutations associated with neurovirulence in monkeys infected with Sabin 1 poliovirus revertants selected at high temperature , 1990, Journal of virology.

[108]  S. R. Pollard,et al.  Nucleotide sequence of a neurovirulent variant of the type 2 oral poliovirus vaccine , 1989, Journal of virology.

[109]  J. Almond,et al.  Reversion of the attenuated and temperature-sensitive phenotypes of the Sabin type 3 strain of poliovirus in vaccinees. , 1989, Virology.

[110]  A. Nomoto,et al.  Determinants in the 5' noncoding region of poliovirus Sabin 1 RNA that influence the attenuation phenotype , 1989, Journal of virology.

[111]  G. Schild,et al.  Genetic basis of attenuation of the Sabin type 3 oral poliovirus vaccine , 1989, Journal of virology.

[112]  G. Dunn,et al.  The effect of sequences in the 5' non-coding region on the replication of polioviruses in the human gut. , 1988, The Journal of general virology.

[113]  L. Schonberger,et al.  Vaccine-associated paralytic poliomyelitis. United States: 1973 through 1984. , 1987, JAMA.

[114]  A. Kameda,et al.  Genetic analysis of the attenuation phenotype of poliovirus type 1 , 1986, Journal of virology.

[115]  J. Icenogle,et al.  Antigenic and molecular evolution of the vaccine strain of type 3 poliovirus during the period of excretion by a primary vaccinee. , 1986, The Journal of general virology.

[116]  J. Maizel,et al.  Increased neurovirulence associated with a single nucleotide change in a noncoding region of the Sabin type 3 poliovaccine genome , 1985, Nature.

[117]  M. Mulders,et al.  Molecular epidemiology of polioviruses. , 1995, Reviews of infectious diseases.

[118]  A. Cann,et al.  Reversion to neurovirulence of the live-attenuated Sabin type 3 oral poliovirus vaccine. , 1984, Nucleic acids research.

[119]  R. Bernier Some observations on poliomyelitis lameness surveys. , 1984, Reviews of infectious diseases.

[120]  I. Dömök Experiences associated with the use of live poliovirus vaccine in Hungary, 1959-1982. , 1984, Reviews of infectious diseases.

[121]  R. Mountford,et al.  Comparison of the complete nucleotide sequences of the genomes of the neurovirulent poliovirus P3/Leon/37 and its attenuated Sabin vaccine derivative P3/Leon 12a1b. , 1984, Proceedings of the National Academy of Sciences of the United States of America.

[122]  S. Kuge,et al.  Complete nucleotide sequence of the attenuated poliovirus Sabin 1 strain genome. , 1982, Proceedings of the National Academy of Sciences of the United States of America.

[123]  The relation between acute persisting spinal paralysis and poliomyelitis vaccine--results of a ten-year enquiry. WHO Consultative Group. , 1982, Bulletin of the World Health Organization.

[124]  O. Kew,et al.  Multiple genetic changes can occur in the oral poliovaccines upon replication in humans. , 1981, The Journal of general virology.

[125]  A. Kulesza,et al.  The epidemic of type 3 poliomyelitis in Poland in 1968. , 1970 .

[126]  J. Melnick,et al.  Studies of the immunogenicity, communicability and genetic stability of oral poliovaccine administered during the winter. , 1967, American journal of epidemiology.

[127]  A. Beale,et al.  A study of polio vaccination in infancy: excretion following challenge with live virus by children given killed or living poliovaccine , 1966, Journal of Hygiene.

[128]  V. Pavilanis,et al.  A STUDY OF SABIN TYPE 1 ORAL VACCINE VIRUS DURING FIVE HUMAN PASSAGES. , 1964, Revue canadienne de biologie.

[129]  G. Dick,et al.  Vaccination Against Poliomyelitis with Live Virus Vaccines—6* , 1961, British medical journal.

[130]  Y. Ghendon,et al.  Comparison of the Resistance of the Intestinal Tract to Poliomyelitis virus (Sabin's Strains) in Persons after Naturally and Experimentally Acquired Immunity. , 1961 .

[131]  E. Ludwig,et al.  Possible protective effect of previous type 2 infection against paralytic poliomyelitis due to type 1 virus. , 1957, American journal of hygiene.

[132]  J. Salk REQUIREMENTS FOR PERSISTENT IMMUNITY TO POLIOMYELITIS , 1956, Transactions of the Association of American Physicians.

[133]  A. Shelokov,et al.  RELATION OF POLIOMYELITIS VIRUS TYPES TO CLINICAL DISEASE AND GEOGRAPHIC DISTRIBUTION: A PRELIMINARY REPORT , 1955, Annals of the New York Academy of Sciences.

[134]  L. Reed,et al.  A SIMPLE METHOD OF ESTIMATING FIFTY PER CENT ENDPOINTS , 1938 .