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Published in: Virology Journal 1/2016

Open Access 01-12-2016 | Research

Characterization of four vaccine-related polioviruses including two intertypic type 3/type 2 recombinants associated with aseptic encephalitis

Authors: Jiansheng Liu, Haihao Zhang, Yilin Zhao, Longhui Xia, Chen Guo, Huai Yang, Na Luo, Zhanlong He, Shaohui Ma

Published in: Virology Journal | Issue 1/2016

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Abstract

Background

Four vaccine-related polioviruses (VRPV) were isolated from aseptic encephalitis cases in Yunnan, China in 2010. The genomic sequences of these VRPVs were investigated to gain a better understanding of their molecular characteristics.

Methods

Molecular typing was performed by amplification and sequencing of the VP1 region. The genomic sequences of the four VRPV3 strains were compared to vaccine strain and wild strain sequences to study genetic drift and recombination.

Results

All four isolates could be entirely neutralized by polyclonal poliovirus 3 (PV3) antisera but not by PV1 and PV2 antisera and displayed a temperature-sensitive phenotype. The genomic sequences of all four isolates contained two Sabin 3-specific attenuating mutations at nucleotides 472(C → T) and 2034(C → T), but a third Sabin 3-specific attenuating mutation at position 2493 (T → C) had reverted back to a T. Recombination analyses showed RF108/YN/CHN/2010 and RF134/YN/CHN/2010 strain recombined with Sabin 2 at the 3′-end of the 2C to 3′-untranslated region (3′-UTR) and at the 5′-end of the 3D to 3′-UTR, respectively.

Conclusion

Four VRPV3 strains including two type 3/type 2 intertypic recombinants were identified. The recombination of Sabin vaccine strains with other Sabin serotypes or human enterovirus C species could be a critical factor in the potential of emerging viruses and related disease outbreaks. Therefore, it is essential to be persistent in the surveillance of EVs (including PV).
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Literature
2.
go back to reference Arita M, Zhu SL, Yoshida H, Yoneyama T, Miyamura T, Shimizu H. A Sabin 3-derived poliovirus recombinant contained a sequence homologous with indigenous human enterovirus species C in the viral polymerase coding region. J Virol. 2005;79(20):12650–7.CrossRefPubMedPubMedCentral Arita M, Zhu SL, Yoshida H, Yoneyama T, Miyamura T, Shimizu H. A Sabin 3-derived poliovirus recombinant contained a sequence homologous with indigenous human enterovirus species C in the viral polymerase coding region. J Virol. 2005;79(20):12650–7.CrossRefPubMedPubMedCentral
3.
go back to reference Burns CC, Shaw J, Jorba J, Bukbuk D, Adu F, Gumede N, Pate MA, Abanida EA, Gasasira A, Iber J, et al. Multiple independent emergences of type 2 vaccine-derived polioviruses during a large outbreak in northern Nigeria. J Virol. 2013;87(9):4907–22.CrossRefPubMedPubMedCentral Burns CC, Shaw J, Jorba J, Bukbuk D, Adu F, Gumede N, Pate MA, Abanida EA, Gasasira A, Iber J, et al. Multiple independent emergences of type 2 vaccine-derived polioviruses during a large outbreak in northern Nigeria. J Virol. 2013;87(9):4907–22.CrossRefPubMedPubMedCentral
4.
go back to reference Rakoto-Andrianarivelo M, Gumede N, Jegouic S, Balanant J, Andriamamonjy SN, Rabemanantsoa S, Birmingham M, Randriamanalina B, Nkolomoni L, Venter M, et al. Reemergence of recombinant vaccine-derived poliovirus outbreak in Madagascar. J Infect Dis. 2008;197(10):1427–35.CrossRefPubMed Rakoto-Andrianarivelo M, Gumede N, Jegouic S, Balanant J, Andriamamonjy SN, Rabemanantsoa S, Birmingham M, Randriamanalina B, Nkolomoni L, Venter M, et al. Reemergence of recombinant vaccine-derived poliovirus outbreak in Madagascar. J Infect Dis. 2008;197(10):1427–35.CrossRefPubMed
5.
go back to reference Razafindratsimandresy R, Joffret ML, Rabemanantsoa S, Andriamamonjy S, Heraud JM, Delpeyroux F. Reemergence of recombinant vaccine-derived polioviruses in healthy children, Madagascar. Emerg Infect Dis. 2013;19(6):1008–10.CrossRefPubMedPubMedCentral Razafindratsimandresy R, Joffret ML, Rabemanantsoa S, Andriamamonjy S, Heraud JM, Delpeyroux F. Reemergence of recombinant vaccine-derived polioviruses in healthy children, Madagascar. Emerg Infect Dis. 2013;19(6):1008–10.CrossRefPubMedPubMedCentral
6.
go back to reference Wang HB, Fang G, Yu WZ, Du F, Fan CX, Liu QL, Hao LX, Liu Y, Zheng JS, Qin ZY, et al. An outbreak of type pi vaccine-derived poliovirus in Sichuan province, China: emergence and circulation in an under-immunized population. PLoS One. 2014;9(12):e113880.CrossRefPubMedPubMedCentral Wang HB, Fang G, Yu WZ, Du F, Fan CX, Liu QL, Hao LX, Liu Y, Zheng JS, Qin ZY, et al. An outbreak of type pi vaccine-derived poliovirus in Sichuan province, China: emergence and circulation in an under-immunized population. PLoS One. 2014;9(12):e113880.CrossRefPubMedPubMedCentral
7.
go back to reference Rakoto-Andrianarivelo M, Guillot S, Iber J, Balanant J, Blondel B, Riquet F, Martin J, Kew O, Randriamanalina B, Razafinimpiasa L, et al. Co-circulation and evolution of polioviruses and species C enteroviruses in a district of Madagascar. PLoS Pathog. 2007;3(12):e191.CrossRefPubMedPubMedCentral Rakoto-Andrianarivelo M, Guillot S, Iber J, Balanant J, Blondel B, Riquet F, Martin J, Kew O, Randriamanalina B, Razafinimpiasa L, et al. Co-circulation and evolution of polioviruses and species C enteroviruses in a district of Madagascar. PLoS Pathog. 2007;3(12):e191.CrossRefPubMedPubMedCentral
8.
go back to reference Cuervo NS, Guillot S, Romanenkova N, Combiescu M, Aubert-Combiescu A, Seghier M, Caro V, Crainic R, Delpeyroux F. Genomic features of intertypic recombinant sabin poliovirus strains excreted by primary vaccinees. J Virol. 2001;75(13):5740–51.CrossRefPubMedPubMedCentral Cuervo NS, Guillot S, Romanenkova N, Combiescu M, Aubert-Combiescu A, Seghier M, Caro V, Crainic R, Delpeyroux F. Genomic features of intertypic recombinant sabin poliovirus strains excreted by primary vaccinees. J Virol. 2001;75(13):5740–51.CrossRefPubMedPubMedCentral
9.
go back to reference Guillot S, Caro V, Cuervo N, Korotkova E, Combiescu M, Persu A, Aubert-Combiescu A, Delpeyroux F, Crainic R. Natural genetic exchanges between vaccine and wild poliovirus strains in humans. J Virol. 2000;74(18):8434–43.CrossRefPubMedPubMedCentral Guillot S, Caro V, Cuervo N, Korotkova E, Combiescu M, Persu A, Aubert-Combiescu A, Delpeyroux F, Crainic R. Natural genetic exchanges between vaccine and wild poliovirus strains in humans. J Virol. 2000;74(18):8434–43.CrossRefPubMedPubMedCentral
10.
go back to reference Joffret ML, Jegouic S, Bessaud M, Balanant J, Tran C, Caro V, Holmblat B, Razafindratsimandresy R, Reynes JM, Rakoto-Andrianarivelo M, Delpeyroux F. Common and diverse features of cocirculating type 2 and 3 recombinant vaccine-derived polioviruses isolated from patients with poliomyelitis and healthy children. J Infect Dis. 2012;205(9):1363–73.CrossRefPubMed Joffret ML, Jegouic S, Bessaud M, Balanant J, Tran C, Caro V, Holmblat B, Razafindratsimandresy R, Reynes JM, Rakoto-Andrianarivelo M, Delpeyroux F. Common and diverse features of cocirculating type 2 and 3 recombinant vaccine-derived polioviruses isolated from patients with poliomyelitis and healthy children. J Infect Dis. 2012;205(9):1363–73.CrossRefPubMed
11.
go back to reference Zhang Y, Wang H, Zhu S, Li Y, Song L, Liu Y, Liu G, Nishimura Y, Chen L, Yan D, et al. Characterization of a rare natural intertypic type 2/type 3 penta-recombinant vaccine-derived poliovirus isolated from a child with acute flaccid paralysis. J Gen Virol. 2010;91(Pt2):421–9.CrossRefPubMed Zhang Y, Wang H, Zhu S, Li Y, Song L, Liu Y, Liu G, Nishimura Y, Chen L, Yan D, et al. Characterization of a rare natural intertypic type 2/type 3 penta-recombinant vaccine-derived poliovirus isolated from a child with acute flaccid paralysis. J Gen Virol. 2010;91(Pt2):421–9.CrossRefPubMed
12.
go back to reference Zhang Y, Zhu S, Yan D, Liu G, Bai R, Wang D, Chen L, Zhu H, An H, Kew O, Xu W. Natural type 3/type 2 intertypic vaccine-related poliovirus recombinants with the first crossover sites within the VP1 capsid coding region. PLoS One. 2010;5(12):e15300.CrossRefPubMedPubMedCentral Zhang Y, Zhu S, Yan D, Liu G, Bai R, Wang D, Chen L, Zhu H, An H, Kew O, Xu W. Natural type 3/type 2 intertypic vaccine-related poliovirus recombinants with the first crossover sites within the VP1 capsid coding region. PLoS One. 2010;5(12):e15300.CrossRefPubMedPubMedCentral
13.
go back to reference Furione M, Guillot S, Otelea D, Balanant J, Candrea A, Crainic R. Polioviruses with natural recombinant genomes isolated from vaccine-associated paralytic poliomyelitis. Virology. 1993;196(1):199–208.CrossRefPubMed Furione M, Guillot S, Otelea D, Balanant J, Candrea A, Crainic R. Polioviruses with natural recombinant genomes isolated from vaccine-associated paralytic poliomyelitis. Virology. 1993;196(1):199–208.CrossRefPubMed
14.
go back to reference Previsani N, Tangermann RH, Tallis G, Jafari HS. World Health Organization Guidelines for Containment of Poliovirus Following Type-Specific Polio Eradication - Worldwide, 2015. MMWR Morb Mortal Wkly Rep. 2015;64(33):913–7.CrossRefPubMed Previsani N, Tangermann RH, Tallis G, Jafari HS. World Health Organization Guidelines for Containment of Poliovirus Following Type-Specific Polio Eradication - Worldwide, 2015. MMWR Morb Mortal Wkly Rep. 2015;64(33):913–7.CrossRefPubMed
15.
go back to reference Weeks-Levy C, Tatem JM, DiMichele SJ, Waterfield W, Georgiu AF, Mento SJ. Identification and characterization of a new base substitution in the vaccine strain of Sabin 3 poliovirus. Virology. 1991;185(2):934–7.CrossRefPubMed Weeks-Levy C, Tatem JM, DiMichele SJ, Waterfield W, Georgiu AF, Mento SJ. Identification and characterization of a new base substitution in the vaccine strain of Sabin 3 poliovirus. Virology. 1991;185(2):934–7.CrossRefPubMed
16.
go back to reference Mento SJ, Weeks-Levy C, Tatem JM, Gorgacz EJ, Waterfield WF. Significance of a newly identified attenuating mutation in Sabin 3 oral poliovirus vaccine. Dev Biol Stand. 1993;78:93–9. 99-100.PubMed Mento SJ, Weeks-Levy C, Tatem JM, Gorgacz EJ, Waterfield WF. Significance of a newly identified attenuating mutation in Sabin 3 oral poliovirus vaccine. Dev Biol Stand. 1993;78:93–9. 99-100.PubMed
17.
go back to reference Savolainen-Kopra C, Samoilovich E, Kahelin H, Hiekka AK, Hovi T, Roivainen M. Comparison of poliovirus recombinants: accumulation of point mutations provides further advantages. J Gen Virol. 2009;90(Pt8):1859–68.CrossRefPubMed Savolainen-Kopra C, Samoilovich E, Kahelin H, Hiekka AK, Hovi T, Roivainen M. Comparison of poliovirus recombinants: accumulation of point mutations provides further advantages. J Gen Virol. 2009;90(Pt8):1859–68.CrossRefPubMed
18.
go back to reference Simonen ML, Roivainen M, Iber J, Burns C, Hovi T. Outbreak of poliomyelitis in Finland in 1984-85 - Re-analysis of viral sequences using the current standard approach. Virus Res. 2010;147(1):91–7.CrossRefPubMed Simonen ML, Roivainen M, Iber J, Burns C, Hovi T. Outbreak of poliomyelitis in Finland in 1984-85 - Re-analysis of viral sequences using the current standard approach. Virus Res. 2010;147(1):91–7.CrossRefPubMed
19.
go back to reference McCarthy M. Eradication of wild poliovirus type 3 may be within reach, say CDC and WHO. BMJ. 2014;349:g6817.CrossRefPubMed McCarthy M. Eradication of wild poliovirus type 3 may be within reach, say CDC and WHO. BMJ. 2014;349:g6817.CrossRefPubMed
20.
go back to reference Diop OM, Burns CC, Sutter RW, Wassilak SG, Kew OM. Update on Vaccine-Derived Polioviruses - Worldwide, January 2014-March 2015. MMWR Morb Mortal Wkly Rep. 2015;64(23):640–6.PubMed Diop OM, Burns CC, Sutter RW, Wassilak SG, Kew OM. Update on Vaccine-Derived Polioviruses - Worldwide, January 2014-March 2015. MMWR Morb Mortal Wkly Rep. 2015;64(23):640–6.PubMed
21.
go back to reference Diop OM, Burns CC, Wassilak SG, Kew OM. Update on vaccine-derived polioviruses - worldwide, July 2012-December 2013. MMWR Morb Mortal Wkly Rep. 2014;63(11):242–8.PubMed Diop OM, Burns CC, Wassilak SG, Kew OM. Update on vaccine-derived polioviruses - worldwide, July 2012-December 2013. MMWR Morb Mortal Wkly Rep. 2014;63(11):242–8.PubMed
22.
go back to reference Centers for Disease Control and Prevention (CDC). Update on vaccine-derived polioviruses--worldwide, April 2011-June 2012. MMWR Morb Mortal Wkly Rep. 2012;61:741–6. Centers for Disease Control and Prevention (CDC). Update on vaccine-derived polioviruses--worldwide, April 2011-June 2012. MMWR Morb Mortal Wkly Rep. 2012;61:741–6.
23.
go back to reference Minor PD, Dunn G, Evans DM, Magrath DI, John A, Howlett J, Phillips A, Westrop G, Wareham K, Almond JW, Et A. The temperature sensitivity of the Sabin type 3 vaccine strain of poliovirus: molecular and structural effects of a mutation in the capsid protein VP3. J Gen Virol. 1989;70(Pt 5):1117–23.CrossRefPubMed Minor PD, Dunn G, Evans DM, Magrath DI, John A, Howlett J, Phillips A, Westrop G, Wareham K, Almond JW, Et A. The temperature sensitivity of the Sabin type 3 vaccine strain of poliovirus: molecular and structural effects of a mutation in the capsid protein VP3. J Gen Virol. 1989;70(Pt 5):1117–23.CrossRefPubMed
24.
go back to reference Blomqvist S, Bruu AL, Stenvik M, Hovi T. Characterization of a recombinant type 3/type 2 poliovirus isolated from a healthy vaccinee and containing a chimeric capsid protein VP1. J Gen Virol. 2003;84(Pt3):573–80.CrossRefPubMed Blomqvist S, Bruu AL, Stenvik M, Hovi T. Characterization of a recombinant type 3/type 2 poliovirus isolated from a healthy vaccinee and containing a chimeric capsid protein VP1. J Gen Virol. 2003;84(Pt3):573–80.CrossRefPubMed
25.
go back to reference Dedepsidis E, Pliaka V, Kyriakopoulou Z, Brakoulias C, Levidiotou-Stefanou S, Pratti A, Mamuris Z, Markoulatos P. Complete genomic characterization of an intertypic Sabin 3/Sabin 2 capsid recombinant. FEMS Immunol Med Microbiol. 2008;52(3):343–51.CrossRefPubMed Dedepsidis E, Pliaka V, Kyriakopoulou Z, Brakoulias C, Levidiotou-Stefanou S, Pratti A, Mamuris Z, Markoulatos P. Complete genomic characterization of an intertypic Sabin 3/Sabin 2 capsid recombinant. FEMS Immunol Med Microbiol. 2008;52(3):343–51.CrossRefPubMed
26.
go back to reference Tao Z, Wang H, Xu A, Zhang Y, Song L, Zhu S, Li Y, Yan D, Liu G, Yoshida H, et al. Isolation of a recombinant type 3/type 2 poliovirus with a chimeric capsid VP1 from sewage in Shandong, China. Virus Res. 2010;150(1-2):56–60.CrossRefPubMed Tao Z, Wang H, Xu A, Zhang Y, Song L, Zhu S, Li Y, Yan D, Liu G, Yoshida H, et al. Isolation of a recombinant type 3/type 2 poliovirus with a chimeric capsid VP1 from sewage in Shandong, China. Virus Res. 2010;150(1-2):56–60.CrossRefPubMed
27.
go back to reference Shahmahmoodi S, Parvaneh N, Burns C, Asghar H, Mamishi S, Tabatabaie H, Chen Q, Teimourian S, Gooya MM, Esteghamati AR, et al. Isolation of a type 3 vaccine-derived poliovirus (VDPV) from an Iranian child with X-linked agammaglobulinemia. Virus Res. 2008;137(1):168–72.CrossRefPubMed Shahmahmoodi S, Parvaneh N, Burns C, Asghar H, Mamishi S, Tabatabaie H, Chen Q, Teimourian S, Gooya MM, Esteghamati AR, et al. Isolation of a type 3 vaccine-derived poliovirus (VDPV) from an Iranian child with X-linked agammaglobulinemia. Virus Res. 2008;137(1):168–72.CrossRefPubMed
28.
go back to reference Martin J, Samoilovich E, Dunn G, Lackenby A, Feldman E, Heath A, Svirchevskaya E, Cooper G, Yermalovich M, Minor PD. Isolation of an intertypic poliovirus capsid recombinant from a child with vaccine-associated paralytic poliomyelitis. J Virol. 2002;76(21):10921–8.CrossRefPubMedPubMedCentral Martin J, Samoilovich E, Dunn G, Lackenby A, Feldman E, Heath A, Svirchevskaya E, Cooper G, Yermalovich M, Minor PD. Isolation of an intertypic poliovirus capsid recombinant from a child with vaccine-associated paralytic poliomyelitis. J Virol. 2002;76(21):10921–8.CrossRefPubMedPubMedCentral
29.
go back to reference Chan YF, Sam IC, AbuBakar S. Phylogenetic designation of enterovirus 71 genotypes and subgenotypes using complete genome sequences. Infect Genet Evol. 2010;10(3):404–12.CrossRefPubMed Chan YF, Sam IC, AbuBakar S. Phylogenetic designation of enterovirus 71 genotypes and subgenotypes using complete genome sequences. Infect Genet Evol. 2010;10(3):404–12.CrossRefPubMed
30.
go back to reference Famulare M, Chang S, Iber J, Zhao K, Adeniji JA, Bukbuk D, Baba M, Behrend M, Burns CC, Oberste MS. Sabin Vaccine Reversion in the Field: a Comprehensive Analysis of Sabin-Like Poliovirus Isolates in Nigeria. J Virol. 2016;90(1):317–31.CrossRef Famulare M, Chang S, Iber J, Zhao K, Adeniji JA, Bukbuk D, Baba M, Behrend M, Burns CC, Oberste MS. Sabin Vaccine Reversion in the Field: a Comprehensive Analysis of Sabin-Like Poliovirus Isolates in Nigeria. J Virol. 2016;90(1):317–31.CrossRef
31.
go back to reference Liu J, Zhu Y, Pan Y, Liu Z, Guo C, Ma S. Complete genome sequence analysis of two human coxsackievirus A9 strains isolated in Yunnan, China, in 2009. Virus Genes. 2015;50(3):358–64.CrossRefPubMed Liu J, Zhu Y, Pan Y, Liu Z, Guo C, Ma S. Complete genome sequence analysis of two human coxsackievirus A9 strains isolated in Yunnan, China, in 2009. Virus Genes. 2015;50(3):358–64.CrossRefPubMed
32.
go back to reference Nix WA, Oberste MS, Pallansch MA. Sensitive, seminested PCR amplification of VP1 sequences for direct identification of all enterovirus serotypes from original clinical specimens. J Clin Microbiol. 2006;44(8):2698–704.CrossRefPubMedPubMedCentral Nix WA, Oberste MS, Pallansch MA. Sensitive, seminested PCR amplification of VP1 sequences for direct identification of all enterovirus serotypes from original clinical specimens. J Clin Microbiol. 2006;44(8):2698–704.CrossRefPubMedPubMedCentral
Metadata
Title
Characterization of four vaccine-related polioviruses including two intertypic type 3/type 2 recombinants associated with aseptic encephalitis
Authors
Jiansheng Liu
Haihao Zhang
Yilin Zhao
Longhui Xia
Chen Guo
Huai Yang
Na Luo
Zhanlong He
Shaohui Ma
Publication date
01-12-2016
Publisher
BioMed Central
Published in
Virology Journal / Issue 1/2016
Electronic ISSN: 1743-422X
DOI
https://doi.org/10.1186/s12985-016-0615-2

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