Evolution of Poliovirus Type I during 5.5 Years of Prolonged Enteral Replication in an Immunodeficient Patient
Open accessAbstract
Poliovirus type 1 was isolated from an immunodeficient patient 4 days after onset of paresis (IS1) and after 5.5 years of prolonged enteral virus replication (IS2). Antigenic characterization revealed that IS1 was Sabin 1-like, whereas IS2 reacted like poliovirus 1 Mahoney. Complete genomic sequencing demonstrated the phylogenetic relationship (94.9% identity) of IS1 and IS2, which differed from the most closely related Sabin 1 by 5.4 and 8.3%, respectively. Both isolates had revertant-like mutations at nucleotides 480 and 6203. Deduced amino acid sequences indicated significant changes between IS1 and IS2 at the neutralizing antigenic site 1. Prolonged enteral replication, evolution, and shedding of poliovirus by immunodeficient patients should be considered in the poliovirus eradication strategy.
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They also appear to be largely independent of immune selection, as evolution rates are similar during prolonged replication in immunodeficient patients and during widespread circulation.
“They also appear to be largely independent of immune selection, as evolution rates are similar during prolonged replication in immunodeficient patients (10, 88, 117, 223) and during widespread circulation (60, 84, 85, 108).”
From VACCINE-DERIVED POLIOVIRUSES AND THE ENDGAME STRATEGY FOR GLOBAL POLIO ERADICATION (2005) · cites this paper as [10]
Other CVID patients developed paralysis several years after receipt of the implicated OPV dose (typically the last dose).
“Other CVID patients developed paralysis several years after receipt of the implicated OPV dose (typically the last dose) (10, 88, 223).”
From VACCINE-DERIVED POLIOVIRUSES AND THE ENDGAME STRATEGY FOR GLOBAL POLIO ERADICATION (2005) · cites this paper as [10]
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“European Region 14/101 (14) 10/94 (11) 4/7 (57)”
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“The study population included 52 males and 30 females, ages 5 months to 33 years, diagnosed with 2 categories of PIDs: (i) humoral or combined immunodeficiencies (agammaglobulinemia, n 11; common variable immunodeficiency disorders [CVID], n 14; hyper-IgM syndrome, n 8; MHC class II deficiency, n 14) and (ii) other im…”
BackgroundInfluentialPoliovirus Vaccines: Molecular Biology and Immune Response
Minor, P. D., & Almond, J. (2014) · Molecular Biology of Picornavirus · doi:10.1128/9781555817916.ch30 · Cited by 33 · see citing works
Labadie, K., Pelletier, I., Saulnier, A., Martín, J. E.-S., & Colbère-Garapin, F. (2003) · Virology · doi:10.1016/j.virol.2003.09.005 · Cited by 33 · see citing works
“…hereditary antibody deficiencies, Sabin PV strains of each of the three serotypes can continue replicating for long periods of times, more than 10 years, sometimes causing chronic poliomyelitis (Bellmunt et al., 1999; Buttinelli et al., 2003; Kew et al., 1998; Minor, 2001; Yoneyama et al., 2001).”
BackgroundEnteroviruses and Parechoviruses
Dunn, J. J. (2016) · Microbiology Spectrum · doi:10.1128/microbiolspec.dmih2-0006-2015 · Cited by 33 · see citing works
de Silva, R., Gunasena, S., Ratnayake, D., Wickremesinghe, G. D., Kumarasiri, C., Pushpakumara, B. A. W., Deshpande, J. M., Kahn, A.-L., & Sutter, R. W. (2012) · Vaccine · doi:10.1016/j.vaccine.2012.10.035 · Cited by 32 · see citing works
Viral infection in primary antibody deficiency syndromes
Jones, T. P., Buckland, M. S., Breuer, J., & Lowe, D. M. (2019) · Reviews in Medical Virology · doi:10.1002/rmv.2049 · Cited by 32 · see citing works
Complete genomic characterization of an intertypic Sabin 3/Sabin 2 capsid recombinant
Dedepsidis, E., Pliaka, V., Kyriakopoulou, Z., Brakoulias, C., Levidiotou-Stefanou, S., Pratti, A., Mamuris, Z., & Markoulatos, P. (2008) · FEMS Immunology & Medical Microbiology · doi:10.1111/j.1574-695x.2008.00381.x · Cited by 32 · see citing works
“According to previous studies (Kew et al., 1998; Bellmunt et al., 1999; Gavrilin et al., 2000; Martin et al., 2000) the rate of accumulation of synonymous substitutions in naturally evolving polioviruses has a linear character.”
BackgroundSamoilovich, E., Roivainen, M., Titov, L. P., & Hovi, T. (2003) · Journal of Medical Virology · doi:10.1002/jmv.10480 · Cited by 30 · see citing works
Prevalence of vaccine-derived polioviruses in sewage and river water in South Africa
Pavlov, D. N., van Zyl, W. B., Heerden, J. V., Grabow, W. O. K., & Ehlers, M. M. (2005) · Water Research · doi:10.1016/j.watres.2005.05.027 · Cited by 30 · see citing works
Tebbens, R. J. D., & Thompson, K. M. (2016) · Epidemiology and Infection · doi:10.1017/s0950268816002302 · Cited by 29 · see citing works
Search for poliovirus long-term excretors among patients affected by agammaglobulinemia
Fiore, L., Plebani, A., Buttinelli, G., Fiore, S., Donati, V., Marturano, J., Soresina, A., Martire, B., Azzari, C., Nigro, G., et al. (2004) · Clinical Immunology · doi:10.1016/j.clim.2003.11.011 · Cited by 29 · see citing works
Cassemiro, K. M. S. D. M., Burlandy, F. M., Barbosa, M. R. F., Chen, Q., Jorba, J. C., Hachich, E. M., Sato, M. I. Z., Burns, C. C., & da Silva, E. E. (2016) · PLoS ONE · doi:10.1371/journal.pone.0152251 · Cited by 27 · see citing works
Evolution of a rare vaccine-derived multirecombinant poliovirus
Karakasiliοtis, I., Paximadi, E., & Markoulatos, P. (2005) · Journal of General Virology · doi:10.1099/vir.0.80823-0 · Cited by 28 · see citing works
“The presence of vaccine-derived polioviruses in immunodeficient patients (Bellmunt et al., 1999; Khetsuriani et al., 2003; MacLennan et al., 2004), civil sewage (Blomqvist et al.”
BackgroundRetrospective Characterization of a Vaccine-Derived Poliovirus Type 1 Isolate from Sewage in Greece
Dedepsidis, E., Kyriakopoulou, Z., Pliaka, V., Kottaridi, C., Bolanaki, E., Levidiotou-Stefanou, S., Komiotis, D., & Markoulatos, P. (2007) · Applied and Environmental Microbiology · doi:10.1128/aem.00535-07 · Cited by 27 · see citing works
Hovi, T., Lindholm, N., Savolainen, C., Stenvik, M., & Burns, C. C. (2004) · Journal of General Virology · doi:10.1099/vir.0.19518-0 · Cited by 27 · see citing works
“A few reports have been published on the extensive genetic divergence generated during chronic infection with OPVderived strains lasting for several years (Yoneyama et al., 1982; Kew et al., 1998; Bellmunt et al., 1999; Gavrilin et al., 2000; Martı́n et al., 2000).”
BackgroundKorotkova, E. A., Gmyl, A. P., Yakovenko, M. L., Ivanova, O. E., Eremeeva, T. P., Kozlovskaya, L. I., Shakaryan, A. K., Lipskaya, G. Y., Parshina, I. L., Loginovskikh, N. V., et al. (2016) · Journal of Virology · doi:10.1128/jvi.00277-16 · Cited by 23 · see citing works
“This work was funded by Russian Science Foundation (RSF) (15-1500147).”
BackgroundMethodZhang, Y., Wang, H., Zhu, S., Li, Y., Li, S., Liu, Y., Liu, G., Nishimura, Y., Chen, L., Yan, D., et al. (2009) · Journal of General Virology · doi:10.1099/vir.0.014258-0 · Cited by 25 · see citing works
“According to the WHO program of global eradication of poliomyelitis (WHO, 2004a), this VDPV is undoubtedly an aVDPV, because it does not have the genetic characteristics of iVDPV, such as numerous amino acid changes in NAg sites (Bellmunt et al., 1999; Kew et al., 1998).”
BackgroundMethodFoiadelli, T., Savasta, S., Battistone, A., Kota, M., Passera, C., Fiore, S., Bino, S., Amato, C., Lozza, A., Marseglia, G. L., et al. (2016) · BMC Infectious Diseases · doi:10.1186/s12879-016-1587-y · Cited by 24 · see citing works
“subjects attenuated OPV viruses replicate in the gut and can persist for long periods [15, 33–35].”
BackgroundMolecular Mechanisms of Poliovirus Variation and Evolution
Agol, V. I. (2006) · Current Topics in Microbiology and Immunology · doi:10.1007/3-540-26397-7_8 · Cited by 73 · see citing works
Sutter, R. W., Tangermann, R. H., Aylward, R. B., & Cochi, S. L. (2001) · Infectious Disease Clinics of North America · doi:10.1016/s0891-5520(05)70267-1 · Cited by 23 · see citing works
Immunodeficiency-associated Vaccine-Derived Poliovirus Type 3 in Infant, South Africa, 2011
Gumede, N., Muthambi, V., & Schoub, B. D. (2012) · Emerging infectious diseases · doi:10.3201/eid1806.120037 · Cited by 21 · see citing works
Highly Divergent Type 2 and 3 Vaccine-Derived Polioviruses Isolated from Sewage in Tallinn, Estonia
Al‐Hello, H., Jorba, J. C., Blomqvist, S., Raud, R., Kew, O. M., & Roivainen, M. (2013) · Journal of Virology · doi:10.1128/jvi.01174-13 · Cited by 21 · see citing works
“Unlike most individuals with iVDPV infections who either clear their infections or die within a year from complications of their immunodeficiency (8, 33), infected individuals with CVID may excrete iVDPVs for 5 years (13, 15, 16, 22).”
BackgroundInfluentialSutter, R. W., Kew, O. M., Cochi, S. L., & Aylward, R. B. (2017) · Elsevier eBooks · doi:10.1016/b978-0-323-35761-6.00048-1 · Cited by 22 · see citing works
No evidence of prolonged enterovirus excretion in HIV‐seropositive patients
Gouandjika‐Vasilache, I., Akoua-Koffi, C. G., Bégaud, É., & Dosseh, A. R. G. A. (2005) · Tropical Medicine & International Health · doi:10.1111/j.1365-3156.2005.01454.x · Cited by 18 · see citing works
“One study reported that poliovirus was excreted for up to 637 days and another for up to 5.5 years (Hara et al. 1981; Misbah et al. 1991; WHO 1993; Bellmunt et al. 1999; Martin et al. 2000).”
BackgroundInfluentialPoliovirus vaccine strains detected in stool specimens of immunodeficient children in South Africa
Pavlov, D. N., van Zyl, W. B., Kruger, M., Blignaut, L., Grabow, W. O. K., & Ehlers, M. M. (2005) · Diagnostic Microbiology and Infectious Disease · doi:10.1016/j.diagmicrobio.2005.08.011 · Cited by 18 · see citing works
“Reversion of the OPV strains to increased neurovirulence is one key factor for the occurrence of vaccine-associated paralytic poliomyelitis (VAPP) (Sutter and Prevots, 1994; Bellmunt et al., 1999; Shulman et al., 2000; Hovi et al., 2004).”
BackgroundInfluentialPrevalence of vaccine-derived polioviruses in stools of immunodeficient children in South Africa
Pavlov, D. N., van Zyl, W. B., Heerden, J. V., Kruger, M., Blignaut, L., Grabow, W. O. K., & Ehlers, M. M. (2006) · Journal of Applied Microbiology · doi:10.1111/j.1365-2672.2006.03020.x · Cited by 18 · see citing works
“…common variable immunodeficiency or X-linked agammaglobulinemia) are highly divergent ( 90% VP1 sequence identity to the parental OPV strain), suggesting that the chronic PV infections had persisted for 10 years or more (Kew et al. 1998; Bellmunt et al. 1999; Wood et al. 2000; Yang et al. 2003).”
BackgroundGenome Instability in Picornaviruses
Agol, V. I. (2002) · Molecular Biology · doi:10.1023/a:1015317922221 · Cited by 18 · see citing works
Limited and Localized Outbreak of Newly Emergent Type 2 Vaccine-Derived Poliovirus in Sichuan, China
Yan, D., Zhang, Y., Zhu, S., Chen, N., Li, X., Wang, D., Ma, X., Zhu, H., Tong, W., & Xu, W. (2014) · Clinical and Vaccine Immunology · doi:10.1128/cvi.00196-14 · Cited by 17 · see citing works
“For polio eradication programs, the derivatives of the OPVrelated polioviruses have been classified into 4 categories (2, 3): (i) vaccine-related polioviruses, which exhibit the closest sequence relationships to the ancestral Sabin OPV strains and include most of the polioviruses isolated from acute flaccid paralysis…”
BackgroundMogotsi, M. T., Mwangi, P. N., Bester, P. A., Mphahlele, M. J., Seheri, M. L., O’Neill, H. G., & Nyaga, M. M. (2020) · Viruses · doi:10.3390/v12111260 · Cited by 17 · see citing works
“To the contrary, several immuno-deficient OPV recipients have been reported to excrete polioviruses for several years [25,27,28].”
BackgroundDriss, N., Mellouli, F., Yahia, A. B., Touzi, H., Barbouche, M., Triki, H., & Béjaoui, M. (2014) · Journal of Clinical Microbiology · doi:10.1128/jcm.01122-14 · Cited by 16 · see citing works
Romanenkova, N. I., Guillot, S., Rozaeva, N. R., Crainic, R., Александровна, Б. М., & Delpeyroux, F. (2006) · Journal of Clinical Microbiology · doi:10.1128/jcm.00017-06 · Cited by 16 · see citing works
“5%) remains high (5%), indicating that several strains have circulated for 6 to 16 months according to the molecular clock of poliovirus strains, with about 1% nucleotide substitutions per year (3, 13, 24).”
BackgroundCommunity-Acquired Poliovirus Infection in Children with Primary Immunodeficiencies in Tunisia
Triki, H., Barbouche, M., Bahri, O., Béjaoui, M., & Dellagi, K. (2003) · Journal of Clinical Microbiology · doi:10.1128/jcm.41.3.1203-1211.2003 · Cited by 16 · see citing works
“Previous studies reported immunodeficient patients who converted to long-term viral excretors shortly after receiving OPV vaccine, thus corresponding to massive infecting doses ( 5 , 19, 23).”
BackgroundInfluentialDedepsidis, E., Karakasiliοtis, I., Paximadi, E., Kyriakopoulou, Z., Komiotis, D., & Markoulatos, P. (2006) · Virus Genes · doi:10.1007/s11262-005-0055-3 · Cited by 16 · see citing works
McDonald, S. L., Weldon, W. C., Wei, L., Chen, Q., Shaw, J., Zhao, K., Jorba, J. C., Kew, O. M., Pallansch, M. A., Burns, C. C., et al. (2020) · Vaccine · doi:10.1016/j.vaccine.2020.02.035 · Cited by 13 · see citing works
Error Frequencies of Picornavirus RNA Polymerases: Evolutionary Implications for Virus Populations
Domingo, E., Baranowski, É., Escarmı́s, C., Sobrino, F., & Holland, J. J. (2014) · ASM Press eBooks · doi:10.1128/9781555817916.ch23 · Cited by 12 · see citing works
The Mechanism of Poliovirus Eradication
Kew, O. M., & Pallansch, M. A. (2014) · ASM Press eBooks · doi:10.1128/9781555817916.ch39 · Cited by 12 · see citing works
Sharif, S., Abbasi, B. H., Khurshid, A., Alam, M. M., Shaukat, S., Angez, M., Rana, M. S., & Zaidi, S. S. Z. (2014) · PLoS ONE · doi:10.1371/journal.pone.0088442 · Cited by 11 · see citing works
Virus Evolution in Prolonged Infections of Immunocompromised Individuals
Raglow, Z., & Lauring, A. S. (2024) · Clinical Chemistry · doi:10.1093/clinchem/hvae150 · Cited by 10 · see citing works
Hsieh, M.-S., Hsu, C.-W., Tu, L.-L., Chai, K. M., Yu, L.-L., Wu, C.-C., Chen, M., Chiang, C.-Y., Liu, S., Liao, C., et al. (2021) · Frontiers in Immunology · doi:10.3389/fimmu.2021.751883 · Cited by 10 · see citing works
The future of polio eradication
Hull, H. F. (2001) · The Lancet Infectious Diseases · doi:10.1016/s1473-3099(01)00143-8 · Cited by 10 · see citing works
van de Ven, A., van Konijnenburg, D. P. H., Wensing, A. M. J., & van Montfrans, J. M. (2011) · Clinical Reviews in Allergy & Immunology · doi:10.1007/s12016-011-8292-9 · Cited by 10 · see citing works
“Extended VDPV excretion particularly occurs in antibody deficiency syndromes [72], ranging from 21 months to 22 years in CVID and related hypogammaglobulinemias [25, 73–76].”
BackgroundSazzad, H. M. S., Rainey, J. J., Mach, O., Sutter, R. W., Diordista, S., Kawser, C. A., Mobarak, R., Alam, D., Chowdhury, M. A., Hossain, J., et al. (2012) · Vaccine · doi:10.1016/j.vaccine.2012.06.017 · Cited by 10 · see citing works
Vaccine derived bi- and multi-recombinant Sabin strains
Paximadi, E., Karakasiliοtis, I., Bolanaki, E., Krikelis, A., & Markoulatos, P. (2007) · Virus Genes · doi:10.1007/s11262-007-0146-4 · Cited by 10 · see citing works
Estívariz, C. F., Krow‐Lucal, E., & Mach, O. (2024) · Pathogens · doi:10.3390/pathogens13121128 · Cited by 9 · see citing works
Sazzad, H. M. S., Rainey, J. J., Kahn, A.-L., Mach, O., Liyanage, J. B. L., Alam, A. N., Kawser, C. A., Hossain, A., Sutter, R. W., & Luby, S. P. (2014) · The Journal of Infectious Diseases · doi:10.1093/infdis/jiu221 · Cited by 9 · see citing works
Adu, F., Iber, J. C., Harry, T. O., Burns, C. C., Oyedele, O. I., Adeniji, J. A., Mubarak, O. T., & Kew, O. M. (2003) · AFRICAN JOURNAL OF BIOTECHNOLOGY · doi:10.5897/ajb2003.000-1092 · Cited by 10 · see citing works
“The poliovirus is among the most rapidly evolving viruses known, about 10-2 nt substitution/site/yr (Bellmunt et al., 1999; Kew et al., 1995; Kew et al., 1998 Martin et al., 2000).”
BackgroundPersistent Infections by Picornaviruses
Colbère-Garapin, F., Pelletier, I., & Ouzilou, L. (2014) · ASM Press eBooks · doi:10.1128/9781555817916.ch35 · Cited by 9 · see citing works
Weil, M., Rahav, G., Somech, R., Stauber, T., Alfandari, J., Weiss, L., Silberstein, I., Indenbaum, V., Or, I. B., Mendelson, E., et al. (2019) · International Journal of Infectious Diseases · doi:10.1016/j.ijid.2019.03.037 · Cited by 8 · see citing works
Kew, O. M. (2014) · Springer eBooks · doi:10.1007/978-1-4899-7448-8_13 · Cited by 8 · see citing works
Use of mutational pattern in 5′-NCR and VP1 regions of polioviruses for molecular diagnosis
Pliaka, V., Dedepsidis, E., Kyriakopoulou, Z., Papadopoulou, I., Levidiotou, S., & Markoulatos, P. (2007) · Molecular and Cellular Probes · doi:10.1016/j.mcp.2007.01.004 · Cited by 8 · see citing works
“The VP1 mutational pattern of these isolates comes in contradiction with mutational patterns observed in previous studies where synonymous mutations outnumbered the nonsynonymous ones in VP1 region [23,34–36].”
ResultShulman, L. M. (2012) · Springer eBooks · doi:10.1007/978-1-4614-5719-0_10 · Cited by 7 · see citing works
- Authors
- Bellmunt, A., May, G., Zell, R., Pring-Åkerblom, P., Verhagen, W., & Heim, A.
- Affiliations
- Medizinische Hochschule Hannover (DE)
- University of Münster (DE)
- Friedrich Schiller University Jena (DE)
- Corresponding author
- Heim, Albert
- Venue
- Virology
- Publisher
- Elsevier BV
- Published
- 1999-12
- Volume
- 265
- Issue
- 2
- Pages
- 178-184
- ISSN
- 0042-6822 (ISSN-L)
- OpenAlex
- W2041302422
- Cited by
- 128
- References
- 18
- Citations by year
- 2024: 2 · 2023: 3 · 2021: 1 · 2020: 4 · 2019: 2 · 2018: 1 · 2017: 2 · 2016: 6 · 2015: 3 · 2014: 13 · 2013: 4 · 2012: 10
- FWCI
- 2.18
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Virology (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Health Sciences › Medicine › Cardiology and Cardiovascular Medicine › Viral Infections and Immunology Research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Evolution and Genetic Dynamics
- Health Sciences › Medicine › Epidemiology › Virology and Viral Diseases
- Keywords
- poliovirus type 1, viral evolution, Mahoney strain, antigen characterization, revertant mutations, viral shedding, polio eradication, long-term viral persistence
- MeSH terms
- Amino Acid Sequence, Base Sequence, Humans, Molecular Sequence Data, Nucleic Acid Conformation, Phylogeny, Poliomyelitis, RNA, Viral, Time Factors, Virus Replication, Sequence Alignment, Immunocompromised Host, Virus Shedding, Sequence Homology, Amino Acid, Poliovirus, Evolution, Molecular, 5' Untranslated Regions
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