Abstract
A type 2 vaccine-related poliovirus (strain CHN3024), differing from the Sabin 2 strain by 0.44% in the VP1 coding region was isolated from a patient with vaccine-associated paralytic poliomyelitis. Sequences downstream of nucleotide position 6735 (3D pol coding region) were derived from an unidentified sequence; no close match for a potential parent was found, but it could be classified into a non-polio human enteroviruses species C (HEV-C) phylogeny. The virus differed antigenically from the parental Sabin strain, having an amino acid substitution in the neutralizing antigenic site 1. The similarity between CHN3024 and Sabin 2 sequences suggests that the recombination was recent; this is supported by the estimation that the initiating OPV dose was given only 36–75 days before sampling. The patient’s clinical manifestations, intratypic differentiation examination, and whole-genome sequencing showed that this recombinant exhibited characteristics of neurovirulent vaccine-derived polioviruses (VDPV), which may, thus, pose a potential threat to a polio-free world.
Similar content being viewed by others
References
Adu F, Iber J, Bukbuk D, Gumede N, Yang SJ, Jorba J, Campagnoli R, Sule WF, Yang CF, Burns C, Pallansch M, Harry T, Kew O (2007) Isolation of recombinant type 2 vaccine-derived poliovirus (VDPV) from a Nigerian child. Virus Res 127:17–25
Avellon A, Cabrerizo M, de Miguel T, Perez-Brena P, Tenorio A, Perez JL, de Aragon MV, Trallero G (2008) Paralysis case and contact spread of recombinant vaccine-derived poliovirus, Spain. Emerg Infect Dis 14:1807–1809
Balanant J, Guillot S, Candrea A, Delpeyroux F, Crainic R (1991) The natural genomic variability of poliovirus analyzed by a restriction fragment length polymorphism assay. Virology 184:645–654
Bouchard MJ, Lam DH, Racaniello VR (1995) Determinants of attenuation and temperature sensitivity in the type 1 poliovirus Sabin vaccine. J Virol 69:4972–4978
Brown B, Oberste MS, Maher K, Pallansch MA (2003) Complete genomic sequencing shows that polioviruses and members of human enterovirus species C are closely related in the noncapsid coding region. J Virol 77:8973–8984
Cuervo NS, Guillot S, Romanenkova N, Combiescu M, Aubert-Combiescu A, Seghier M, Caro V, Crainic R, Delpeyroux F (2001) Genomic features of intertypic recombinant sabin poliovirus strains excreted by primary vaccinees. J Virol 75:5740–5751
Dahourou G, Guillot S, Le Gall O, Crainic R (2002) Genetic recombination in wild-type poliovirus. J Gen Virol 83:3103–3110
de la Torre JC, Giachetti C, Semler BL, Holland JJ (1992) High frequency of single-base transitions and extreme frequency of precise multiple-base reversion mutations in poliovirus. Proc Natl Acad Sci USA 89:2531–2535
Dowdle WR, De Gourville E, Kew OM, Pallansch MA, Wood DJ (2003) Polio eradication: the OPV paradox. Rev Med Virol 13:277–291
Estivariz CF, Watkins MA, Handoko D, Rusipah R, Deshpande J, Rana BJ, Irawan E, Widhiastuti D, Pallansch MA, Thapa A, Imari S (2008) A large vaccine-derived poliovirus outbreak on Madura Island–Indonesia, 2005. J Infect Dis 197:347–354
Fine PE, Carneiro IA (1999) Transmissibility and persistence of oral polio vaccine viruses: implications for the global poliomyelitis eradication initiative. Am J Epidemiol 150:1001–1021
Freistadt MS, Vaccaro JA, Eberle KE (2007) Biochemical characterization of the fidelity of poliovirus RNA-dependent RNA polymerase. Virol J 4:44
Georgescu MM, Delpeyroux F, Tardy-Panit M, Balanant J, Combiescu M, Combiescu AA, Guillot S, Crainic R (1994) High diversity of poliovirus strains isolated from the central nervous system from patients with vaccine-associated paralytic poliomyelitis. J Virol 68:8089–8101
Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98
Heim A (2005) From poliovirus surveillance to enterovirus surveillance: a complete picture? J Med Microbiol 54:1–2
Huang SC, Hsu YW, Wang HC, Huang SW, Kiang D, Tsai HP, Wang SM, Liu CC, Lin KH, Su IJ, Wang JR (2008) Appearance of intratypic recombination of enterovirus 71 in Taiwan from 2002 to 2005. Virus Res 131:250–259
Jarvis TC, Kirkegaard K (1992) Poliovirus RNA recombination: mechanistic studies in the absence of selection. EMBO J 11:3135–3145
John TJ (2004) A developing country perspective on vaccine-associated paralytic poliomyelitis. Bull World Health Organ 82:53–57 discussion 57–58
Jorba J, Campagnoli R, De L, Kew O (2008) Calibration of multiple poliovirus molecular clocks covering an extended evolutionary range. J Virol 82:4429–4440
Kawamura N, Kohara M, Abe S, Komatsu T, Tago K, Arita M, Nomoto A (1989) Determinants in the 5′ noncoding region of poliovirus Sabin 1 RNA that influence the attenuation phenotype. J Virol 63:1302–1309
Kew O, Morris-Glasgow V, Landaverde M, Burns C, Shaw J, Garib Z, Andre J, Blackman E, Freeman CJ, Jorba J, Sutter R, Tambini G, Venczel L, Pedreira C, Laender F, Shimizu H, Yoneyama T, Miyamura T, van Der Avoort H, Oberste MS, Kilpatrick D, Cochi S, Pallansch M, de Quadros C (2002) Outbreak of poliomyelitis in Hispaniola associated with circulating type 1 vaccine-derived poliovirus. Science 296:356–359
Kew OM, Nottay BK, Hatch MH, Nakano JH, Obijeski JF (1981) Multiple genetic changes can occur in the oral poliovaccines upon replication in humans. J Gen Virol 56:337–347
Kew OM, Sutter RW, Nottay BK, McDonough MJ, Prevots DR, Quick L, Pallansch MA (1998) Prolonged replication of a type 1 vaccine-derived poliovirus in an immunodeficient patient. J Clin Microbiol 36:2893–2899
Kew OM, Wright PF, Agol VI, Delpeyroux F, Shimizu H, Nathanson N, Pallansch MA (2004) Circulating vaccine-derived polioviruses: current state of knowledge. Bull World Health Organ 82:16–23
Kew OM, Sutter RW, de Gourville EM, Dowdle WR, Pallansch MA (2005) Vaccine-derived polioviruses and the endgame strategy for global polio eradication. Annu Rev Microbiol 59:587–635
Liang X, Zhang Y, Xu W, Wen N, Zuo S, Lee LA, Yu J (2006) An outbreak of poliomyelitis caused by type 1 vaccine-derived poliovirus in China. J Infect Dis 194:545–551
Liu HM, Zheng DP, Zhang LB, Oberste MS, Pallansch MA, Kew OM (2000) Molecular evolution of a type 1 wild-vaccine poliovirus recombinant during widespread circulation in China. J Virol 74:11153–11161
Macadam AJ, Pollard SR, Ferguson G, Skuce R, Wood D, Almond JW, Minor PD (1993) Genetic basis of attenuation of the Sabin type 2 vaccine strain of poliovirus in primates. Virology 192:18–26
Martin J, Dunn G, Hull R, Patel V, Minor PD (2000) Evolution of the Sabin strain of type 3 poliovirus in an immunodeficient patient during the entire 637-day period of virus excretion. J Virol 74:3001–3010
Martin J, Odoom K, Tuite G, Dunn G, Hopewell N, Cooper G, Fitzharris C, Butler K, Hall WW, Minor PD (2004) Long-term excretion of vaccine-derived poliovirus by a healthy child. J Virol 78:13839–13847
Minor PD, Dunn G (1988) The effect of sequences in the 5′ non-coding region on the replication of polioviruses in the human gut. J Gen Virol 69(Pt 5):1091–1096
Minor PD (1990) Antigenic structure of picornaviruses. Curr Top Microbiol Immunol 161:121–154
Minor PD, Macadam AJ, Stone DM, Almond JW (1993) Genetic basis of attenuation of the Sabin oral poliovirus vaccines. Biologicals 21:357–363
Nomoto A, Omata T, Toyoda H, Kuge S, Horie H, Kataoka Y, Genba Y, Nakano Y, Imura N (1982) Complete nucleotide sequence of the attenuated poliovirus Sabin 1 strain genome. Proc Natl Acad Sci USA 79:5793–5797
Oberste MS, Maher K, Kilpatrick DR, Pallansch MA (1999) Molecular evolution of the human enteroviruses: correlation of serotype with VP1 sequence and application to picornavirus classification. J Virol 73:1941–1948
Oberste MS, Penaranda S, Pallansch MA (2004) RNA recombination plays a major role in genomic change during circulation of coxsackie B viruses. J Virol 78:2948–2955
Oberste MS, Maher K, Williams AJ, Dybdahl-Sissoko N, Brown BA, Gookin MS, Penaranda S, Mishrik N, Uddin M, Pallansch MA (2006) Species-specific RT-PCR amplification of human enteroviruses: a tool for rapid species identification of uncharacterized enteroviruses. J Gen Virol 87:119–128
Paximadi E, Karakasiliotis I, Bolanaki E, Krikelis A, Markoulatos P (2007) Vaccine derived bi- and multi-recombinant Sabin strains. Virus Genes 35:541–548
Rakoto-Andrianarivelo M, Guillot S, Iber J, Balanant J, Blondel B, Riquet F, Martin J, Kew O, Randriamanalina B, Razafinimpiasa L, Rousset D, Delpeyroux F (2007) Co-circulation and evolution of polioviruses and species C enteroviruses in a district of Madagascar. PLoS Pathog 3:e191
Rakoto-Andrianarivelo M, Gumede N, Jegouic S, Balanant J, Andriamamonjy SN, Rabemanantsoa S, Birmingham M, Randriamanalina B, Nkolomoni L, Venter M, Schoub BD, Delpeyroux F, Reynes JM (2008) Reemergence of recombinant vaccine-derived poliovirus outbreak in Madagascar. J Infect Dis 197:1427–1435
Ren RB, Moss EG, Racaniello VR (1991) Identification of two determinants that attenuate vaccine-related type 2 poliovirus. J Virol 65:1377–1382
Rousset D, Rakoto-Andrianarivelo M, Razafindratsimandresy R, Randriamanalina B, Guillot S, Balanant J, Mauclere P, Delpeyroux F (2003) Recombinant vaccine-derived poliovirus in Madagascar. Emerg Infect Dis 9:885–887
Shimizu H, Thorley B, Paladin FJ, Brussen KA, Stambos V, Yuen L, Utama A, Tano Y, Arita M, Yoshida H, Yoneyama T, Benegas A, Roesel S, Pallansch M, Kew O, Miyamura T (2004) Circulation of type 1 vaccine-derived poliovirus in the Philippines in 2001. J Virol 78:13512–13521
Smura T, Blomqvist S, Paananen A, Vuorinen T, Sobotova Z, Bubovica V, Ivanova O, Hovi T, Roivainen M (2007) Enterovirus surveillance reveals proposed new serotypes and provides new insight into enterovirus 5′-untranslated region evolution. J Gen Virol 88:2520–2526
Stanway G, Brown F, Christian P, Hovi T, Hyypiä T, King AMQ, Knowles NJ, Lemon SM, Minor PD, Pallansch MA, Palmenberg AC, Skern T (2005) Family Picornaviridae. In: Fauquet CM, Mayo MA, Maniloff J, Desselberger U, Ball LA (eds) Virus taxonomy. Eighth Report of the International Committee on Taxonomy of viruses. Elsevier/Academic Press, London, pp 757–778
Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599
Toyoda H, Kohara M, Kataoka Y, Suganuma T, Omata T, Imura N, Nomoto A (1984) Complete nucleotide sequences of all three poliovirus serotype genomes. Implication for genetic relationship, gene function and antigenic determinants. J Mol Biol 174:561–585
van der Avoort HG, Hull BP, Hovi T, Pallansch MA, Kew OM, Crainic R, Wood DJ, Mulders MN, van Loon AM (1995) Comparative study of five methods for intratypic differentiation of polioviruses. J Clin Microbiol 33:2562–2566
Wang K, Zhang LB, Otten MW Jr, Zhang XL, Yasuo C, Zhang RZ, Xu T, Liu X, Liu M, Li QL, Yu JJ, Wang Z (1997) Status of the eradication of indigenous wild poliomyelitis in the People’s Republic of China. J Infect Dis 175(Suppl 1):S105–S112
Westrop GD, Wareham KA, Evans DM, Dunn G, Minor PD, Magrath DI, Taffs F, Marsden S, Skinner MA, Schild GC et al (1989) Genetic basis of attenuation of the Sabin type 3 oral poliovirus vaccine. J Virol 63:1338–1344
WHO (2004) Polio laboratory manual, 4th edn. Document World Health Organization/IVB/04.10. Geneva, Switzerland
Yang CF, Naguib T, Yang SJ, Nasr E, Jorba J, Ahmed N, Campagnoli R, van der Avoort H, Shimizu H, Yoneyama T, Miyamura T, Pallansch M, Kew O (2003) Circulation of endemic type 2 vaccine-derived poliovirus in Egypt from 1983 to 1993. J Virol 77:8366–8377
Yoshida H, Horie H, Matsuura K, Kitamura T, Hashizume S, Miyamura T (2002) Prevalence of vaccine-derived polioviruses in the environment. J Gen Virol 83:1107–1111
Acknowledgments
This study was supported by National Key Technology R&D Program of China (Project No.2008BAI56B00), National Key Science and Technology Projects of China (Project No.2008ZX10004-008), and a grant I8/181/978 from the World Health Organization.
Conflict of interest statement
The authors declare that they have no conflict of interest.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Zhang, Y., Zhang, F., Zhu, S. et al. A Sabin 2-related poliovirus recombinant contains a homologous sequence of human enterovirus species C in the viral polymerase coding region. Arch Virol 155, 197–205 (2010). https://doi.org/10.1007/s00705-009-0564-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00705-009-0564-9