Calibration of multiple poliovirus molecular clocks covering an extended evolutionary range
Open accessAbstract
We have calibrated five different molecular clocks for circulating poliovirus based upon the rates of fixation of total substitutions (Kt), synonymous substitutions (Ks), synonymous transitions (As), synonymous transversions (Bs), and nonsynonymous substitutions (Ka) into the P1/capsid region (2,643 nucleotides). Rates were determined over a 10-year period by analysis of sequences of 31 wild poliovirus type 1 isolates representing a well-defined phylogeny derived from a common imported ancestor. Similar rates were obtained by linear regression, the maximum likelihood/single-rate dated-tip method, and Bayesian inference. The very rapid Kt[(1.03 ± 0.10) × 10−2 substitutions/site/year] and Ks[(1.00 ± 0.08) × 10−2] clocks were driven primarily by the Asclock [(0.96 ± 0.09) × 10−2], the Bsclock was ∼10-fold slower [(0.10 ± 0.03) × 10−2], and the more stochastic Kaclock was ∼30-fold slower [(0.03 ± 0.01) × 10−2]. Nonsynonymous substitutions at all P1/capsid sites, including the neutralizing antigenic sites, appeared to be constrained by purifying selection. Simulation of the evolution of third-codon positions suggested that saturation of synonymous transitions would be evident at 10 years and complete at ∼65 years of independent transmission. Saturation of synonymous transversions was predicted to be minimal at 20 years and incomplete at 100 years. The rapid evolution of the Kt,Ks, and Asclocks can be used to estimate the dates of divergence of closely related viruses, whereas the slower Bsand Kaclocks may be used to explore deeper evolutionary relationships within and across poliovirus genotypes.
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The capsid-encoding region of poliovirus, with a rate of fixation of total substitutions in the order of 10−2 substitutions/site/year, appears less genetically stable than the region encoding non-structural proteins.
“However, the capsid-encoding region, with a rate of fixation of total substitutions in the order of 10−2 substitutions/site/year, appears less genetically stable than the region encoding non-structural proteins [17,18].”
From Recombination between Poliovirus and Coxsackie A Viruses of Species C: A Model of Viral Genetic Plasticity and Emergence (2011) · cites this paper as [17]
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From Emergence to Eradication: The Epidemiology of Poliomyelitis Deconstructed
Nathanson, N., & Kew, O. M. (2010) · American Journal of Epidemiology · doi:10.1093/aje/kwq320 · Cited by 405 · see citing works
Self-citationBurns, C. C., Diop, O. M., Sutter, R. W., & Kew, O. M. (2014) · The Journal of Infectious Diseases · doi:10.1093/infdis/jiu295 · Cited by 310 · see citing works
Self-citationStatic and Evolving Norovirus Genotypes: Implications for Epidemiology and Immunity
Parra, G. I., Squires, R. B., Karangwa, C. K., Johnson, J. A., Lepore, C. J., Sosnovtsev, S. V., & Green, K. Y. (2017) · PLoS Pathogens · doi:10.1371/journal.ppat.1006136 · Cited by 275 · see citing works
Tee, K. K., Lam, T. T., Chan, Y. F., Bible, J. M., Kamarulzaman, A., Tong, C. Y. W., Takebe, Y., & Pybus, O. G. (2010) · Journal of Virology · doi:10.1128/jvi.01019-09 · Cited by 226 · see citing works
Burns, C. C., Campagnoli, R., Shaw, J., Vincent, A., Jorba, J., & Kew, O. (2009) · Journal of Virology · doi:10.1128/jvi.00508-09 · Cited by 170 · see citing works
Self-citationSutter, R. W., Kew, O. M., & Cochi, S. L. (2008) · Elsevier eBooks · doi:10.1016/b978-1-4160-3611-1.50030-1 · Cited by 167 · see citing works
Self-citationBurns, C. C., Shaw, J., Jorba, J., Bukbuk, D., Adu, F., Gumede, N., Pate, M. A., Abanida, E. A., Gasasira, A., Iber, J., et al. (2013) · Journal of Virology · doi:10.1128/jvi.02954-12 · Cited by 153 · see citing works
Self-citationTan, X., Huang, X., Zhu, S., Chen, H., Yu, Q., Wang, H., Huo, X., Zhou, J., Wu, Y., Yan, D., et al. (2011) · PLoS ONE · doi:10.1371/journal.pone.0025662 · Cited by 162 · see citing works
The Evolutionary Pathway to Virulence of an RNA Virus
Stern, A., Yeh, M. T., Zinger, T., Smith, M., Wright, C., Ling, G., Nielsen, R., Macadam, A., & Andino, R. (2017) · Cell · doi:10.1016/j.cell.2017.03.013 · Cited by 127 · see citing works
Zhang, Y., Wang, D., Yan, D., Zhu, S., Liu, J., Wang, H., Zhao, S., Yu, D., Nan, L., An, J., et al. (2010) · Journal of Clinical Microbiology · doi:10.1128/jcm.02338-09 · Cited by 143 · see citing works
Klapsa, D., Wilton, T., Zealand, A. M., Bujáki, E., Saxentoff, E. V., Troman, C. M., Shaw, A., Tedcastle, A. B., Majumdar, M., Mate, R., et al. (2022) · The Lancet · doi:10.1016/s0140-6736(22)01804-9 · Cited by 142 · see citing works
Combelas, N., Holmblat, B., Joffret, M.-L., Colbère-Garapin, F., & Delpeyroux, F. (2011) · Viruses · doi:10.3390/v3081460 · Cited by 135 · see citing works
Dornburg, A., Brandley, M. C., McGowen, M. R., & Near, T. J. (2011) · Molecular Biology and Evolution · doi:10.1093/molbev/msr228 · Cited by 127 · see citing works
Wassilak, S., Pate, M. A., Wannemuehler, K., Jenks, J., Burns, C., Chenoweth, P., Abanida, E. A., Adu, F., Baba, M., Gasasira, A., et al. (2011) · The Journal of Infectious Diseases · doi:10.1093/infdis/jiq140 · Cited by 120 · see citing works
Self-citationChen, B., Lee, H.-C., Lee, K.-M., Gong, Y., & Shih, S. (2020) · Frontiers in Microbiology · doi:10.3389/fmicb.2020.00261 · Cited by 117 · see citing works
Dunn, G., Klapsa, D., Wilton, T., Stone, L., Minor, P. D., & Martín, J. E.-S. (2015) · PLoS Pathogens · doi:10.1371/journal.ppat.1005114 · Cited by 105 · see citing works
Tebbens, R. J. D., Pallansch, M. A., Kim, J., Burns, C. C., Kew, O. M., Oberste, M. S., Diop, O. M., Wassilak, S. G. F., Cochi, S. L., & Thompson, K. M. (2013) · Risk Analysis · doi:10.1111/risa.12022 · Cited by 101 · see citing works
Self-citationBrown, B. A., Maher, K., Flemister, M. R., Naraghi‐Arani, P., Uddin, M., Oberste, M. S., & Pallansch, M. A. (2009) · Journal of General Virology · doi:10.1099/vir.0.008540-0 · Cited by 99 · see citing works
Tebbens, R. J. D., Pallansch, M. A., Kalkowska, D. A., Wassilak, S. G. F., Cochi, S. L., & Thompson, K. M. (2013) · Risk Analysis · doi:10.1111/risa.12044 · Cited by 95 · see citing works
Vaccine-Derived Poliomyelitis 12 Years after Infection in Minnesota
DeVries, A., Harper, J. E., Murray, A., Lexau, C., Bahta, L., Christensen, J., Cebelinski, E. A., Fuller, S., Kline, S., Wallace, G. S., et al. (2011) · New England Journal of Medicine · doi:10.1056/nejmoa1008677 · Cited by 87 · see citing works
Shulman, L. M., Gavrilin, E., Jorba, J. C., Martín, J. E.-S., Burns, C. C., Manor, Y., Moran‐Gilad, J., Sofer, D., Hindiyeh, M. Y., Gamzu, R., et al. (2014) · Eurosurveillance · doi:10.2807/1560-7917.es2014.19.7.20709 · Cited by 80 · see citing works
Self-citationPoliovirus serotype-specific VP1 sequencing primers
Kilpatrick, D. R., Iber, J. C., Chen, Q., Ching, K., Yang, S.-J., De, L., Mandelbaum, M., Emery, B. D., Campagnoli, R. P., Burns, C. C., et al. (2011) · Journal of Virological Methods · doi:10.1016/j.jviromet.2011.03.020 · Cited by 73 · see citing works
Self-citationThe final stages of the global eradication of poliomyelitis
Grassly, N. C. (2013) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2012.0140 · Cited by 74 · see citing works
The polio-eradication programme and issues of the end game
Minor, P. D. (2011) · Journal of General Virology · doi:10.1099/vir.0.036988-0 · Cited by 71 · see citing works
Famulare, M., Chang, S. T., Iber, J. C., Zhao, K., Adeniji, J. A., Bukbuk, D. N., Baba, M., Behrend, M. R., Burns, C. C., & Oberste, M. S. (2015) · Journal of Virology · doi:10.1128/jvi.01532-15 · Cited by 72 · see citing works
Diagnostic Assay Development for Poliovirus Eradication
Gerloff, N., Sun, H., Mandelbaum, M., Maher, C., Nix, W. A., Zaidi, S., Shaukat, S., Seakamela, L., Nalavade, U. P., Sharma, D. K., et al. (2018) · Journal of Clinical Microbiology · doi:10.1128/jcm.01624-17 · Cited by 72 · see citing works
Mechanisms of genetic variation in polioviruses
Savolainen‐Kopra, C., & Blomqvist, S. (2010) · Reviews in Medical Virology · doi:10.1002/rmv.663 · Cited by 67 · see citing works
Estimating the Extent of Vaccine-Derived Poliovirus Infection
Wringe, A., Fine, P., Sutter, R. W., & Kew, O. M. (2008) · PLoS ONE · doi:10.1371/journal.pone.0003433 · Cited by 68 · see citing works
Self-citationHigh-Throughput Next-Generation Sequencing of Polioviruses
Montmayeur, A. M., Ng, T. F. F., Schmidt, A., Zhao, K., Magaña, L. C., Iber, J. C., Castro, C. J., Chen, Q., Henderson, E., Ramos, E., et al. (2016) · Journal of Clinical Microbiology · doi:10.1128/jcm.02121-16 · Cited by 66 · see citing works
Reaching the last one per cent: progress and challenges in global polio eradication
Kew, O. M. (2012) · Current Opinion in Virology · doi:10.1016/j.coviro.2012.02.006 · Cited by 63 · see citing works
Self-citationStatus of Global Virologic Surveillance for Rubella Viruses
Abernathy, E. S., Hübschen, J. M., Muller, C. P., Jin, L., Brown, D., Komase, K., Mori, Y., Xu, W., Zhu, Z. H., Siqueira, M. M., et al. (2011) · The Journal of Infectious Diseases · doi:10.1093/infdis/jir099 · Cited by 61 · see citing works
Ivanova, O. E., Yarmolskaya, M. S., Eremeeva, T. P., Gm, B., Baykova, O. Y., Akhmadishina, L. V., Krasota, A. Y., Kozlovskaya, L. I., & Lukashev, A. N. (2019) · Viruses · doi:10.3390/v11050424 · Cited by 58 · see citing works
Phylogeography of Crimean Congo Hemorrhagic Fever Virus
Lukashev, A. N., Klimentov, A. S., Smirnova, S. E., Dzagurova, T. K., Drexler, J. F., & Gmyl, A. P. (2016) · PLoS ONE · doi:10.1371/journal.pone.0166744 · Cited by 59 · see citing works
The 2010 outbreak of poliomyelitis in Tajikistan: epidemiology and lessons learnt
Yakovenko, M. L., Gmyl, A. P., Ivanova, O. E., Eremeeva, T. P., Ap, I., Prostova, M. A., Baykova, O. Y., Isaeva, O. V., Lipskaya, G. Y., Shakaryan, A. K., et al. (2014) · Eurosurveillance · doi:10.2807/1560-7917.es2014.19.7.20706 · Cited by 55 · see citing works
Self-citationSutter, R. W., Kew, O. M., Cochi, S. L., & Aylward, R. B. (2013) · Elsevier eBooks · doi:10.1016/b978-1-4557-0090-5.00035-5 · Cited by 55 · see citing works
Self-citationPreventing Vaccine-Derived Poliovirus Emergence during the Polio Endgame
Pons-Salort, M., Burns, C. C., Lyons, H. M., Blake, I. M., Jafari, H. S., Oberste, M. S., Kew, O. M., & Grassly, N. C. (2016) · PLoS Pathogens · doi:10.1371/journal.ppat.1005728 · Cited by 55 · see citing works
Self-citationRooting human parechovirus evolution in time
Faria, N. R., de Vries, M., van Hemert, F. J., Benschop, K., & van der Hoek, L. (2009) · BMC Evolutionary Biology · doi:10.1186/1471-2148-9-164 · Cited by 53 · see citing works
Evolution of Porcine Kobuvirus Infection, Hungary
Reuter, G., Kecskeméti, S., & Pankovics, P. (2010) · Emerging infectious diseases · doi:10.3201/eid1604.090937 · Cited by 50 · see citing works
Wassilak, S. G. F., Oberste, M. S., Tangermann, R. H., Diop, O. M., Jafari, H. S., & Armstrong, G. L. (2014) · The Journal of Infectious Diseases · doi:10.1093/infdis/jiu456 · Cited by 49 · see citing works
Broccolo, F., Drago, F., Ciccarese, G., Genoni, A. P., Puggioni, A., Rosa, G. M., Parodi, A., Manukyan, H., Laassri, M., Chumakov, K., et al. (2018) · Journal of Clinical Virology · doi:10.1016/j.jcv.2018.11.003 · Cited by 48 · see citing works
Macklin, G., Liao, Y., Takane, M., Dooling, K., Gilmour, S., Mach, O., Kew, O. M., Sutter, R. W., & The iVDPV Working Group (2017) · Frontiers in Immunology · doi:10.3389/fimmu.2017.01103 · Cited by 47 · see citing works
Self-citationMolecular epidemiology and phylogenetics of human enteroviruses: Is there a forest behind the trees?
Lukashev, A. N., Vakulenko, Y. A., Turbabina, N. A., Deviatkin, A. A., & Drexler, J. F. (2018) · Reviews in Medical Virology · doi:10.1002/rmv.2002 · Cited by 48 · see citing works
Identification of vaccine-derived polioviruses using dual-stage real-time RT-PCR
Kilpatrick, D. R., Ching, K., Iber, J., Chen, Q., Yang, S.-J., De, L., Williams, A. J., Mandelbaum, M., Sun, H., Oberste, M. S., et al. (2014) · Journal of Virological Methods · doi:10.1016/j.jviromet.2013.11.017 · Cited by 45 · see citing works
Self-citationYip, C. C., Lau, S. K. P., Lo, J. Y., Chan, K., Woo, P. C. Y., & Yuen, K. (2013) · Virology Journal · doi:10.1186/1743-422x-10-222 · Cited by 45 · see citing works
Shahmahmoodi, S., Parvaneh, N., Burns, C. C., Asghar, H., Mamishi, S., Tabatabaie, H., Chen, Q., Teimourian, S., Gooya, M. M., Esteghamati, A., et al. (2008) · Virus Research · doi:10.1016/j.virusres.2008.07.006 · Cited by 44 · see citing works
Self-citationCowger, T. L., Burns, C. C., Sharif, S., Gary, H. E., Iber, J. C., Henderson, E., Malik, F., Zaidi, S. S. Z., Shaukat, S., Rehman, L., et al. (2017) · PLoS ONE · doi:10.1371/journal.pone.0180608 · Cited by 43 · see citing works
Kew, O. M., & Pallansch, M. A. (2018) · Annual Review of Virology · doi:10.1146/annurev-virology-101416-041749 · Cited by 44 · see citing works
Self-citationA large Finnish echovirus 30 outbreak was preceded by silent circulation of the same genotype
Savolainen‐Kopra, C., Paananen, A., Blomqvist, S., Klemola, P., Simonen, M.-L., Lappalainen, M., Vuorinen, T., Kuusi, M., Lemey, P., & Roivainen, M. (2010) · Virus Genes · doi:10.1007/s11262-010-0536-x · Cited by 43 · see citing works
Mombo, I. M., Berthet, N., Lukashev, A. N., Bleicker, T., Brünink, S., Léger, L., Atencia, R., Cox, D., Bouchier, C., Durand, P., et al. (2015) · PLoS ONE · doi:10.1371/journal.pone.0136700 · Cited by 42 · see citing works
African Non-Human Primates Host Diverse Enteroviruses
Mombo, I. M., Lukashev, A. N., Bleicker, T., Brünink, S., Berthet, N., Maganga, G. D., Durand, P., Arnathau, C., Boundenga, L., Ngoubangoye, B., et al. (2017) · PLoS ONE · doi:10.1371/journal.pone.0169067 · Cited by 40 · see citing works
Molecular evolution of types in non-polio enteroviruses
Lukashev, A. N., & Vakulenko, Y. A. (2017) · Journal of General Virology · doi:10.1099/jgv.0.000966 · Cited by 39 · see citing works
Quantifying Transmission Heterogeneity Using Both Pathogen Phylogenies and Incidence Time Series
Li, L. M., Grassly, N. C., & Fraser, C. (2017) · Molecular Biology and Evolution · doi:10.1093/molbev/msx195 · Cited by 38 · see citing works
Wang, H., Tao, Z., Li, Y., Lin, X., Yoshida, H., Song, L., Zhang, Y., Wang, S., Cui, N., Xu, W., et al. (2014) · Applied and Environmental Microbiology · doi:10.1128/aem.00851-14 · Cited by 38 · see citing works
Hassel, C., Mirand, A., Farkas, A., Diedrich, S., Huemer, H. P., Peigue‐Lafeuille, H., Archimbaud, C., Henquell, C., Bailly, J., & the HFMD French Study Network (2017) · Journal of Virology · doi:10.1128/jvi.00630-17 · Cited by 37 · see citing works
Duchêne, S., Giallonardo, F. D., & Holmes, E. C. (2015) · Molecular Biology and Evolution · doi:10.1093/molbev/msv207 · Cited by 36 · see citing works
Emergency Services of Viral RNAs: Repair and Remodeling
Agol, V. I., & Gmyl, A. P. (2018) · Microbiology and Molecular Biology Reviews · doi:10.1128/mmbr.00067-17 · Cited by 34 · see citing works
Genus-Specific Substitution Rate Variability among Picornaviruses
Hicks, A. L., & Duffy, S. (2011) · Journal of Virology · doi:10.1128/jvi.02535-10 · Cited by 35 · see citing works
Zhang, Y., Yan, D., Zhu, S., Wen, N., Li, L., Wang, H., Liu, J., Ye, X., Ding, Z., Wang, D., et al. (2010) · The Journal of Infectious Diseases · doi:10.1086/657410 · Cited by 34 · see citing works
Self-citationTao, Z., Wang, H., Xu, A., Zhang, Y., Song, L., Zhu, S., Li, Y., Yan, D., Liu, G., Yoshida, H., et al. (2010) · Virus Research · doi:10.1016/j.virusres.2010.02.014 · 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
Shulman, L. M., Mendelson, E., Anis, E., Bassal, R., Gdalevich, M., Hindiyeh, M. Y., Kaliner, E., Kopel, E., Manor, Y., Moran‐Gilad, J., et al. (2014) · The Journal of Infectious Diseases · doi:10.1093/infdis/jiu294 · Cited by 32 · see citing works
Culture-Independent Detection of Poliovirus in Stool Samples by Direct RNA Extraction
Harrington, C., Sun, H., Jeffries-Miles, S., Gerloff, N., Mandelbaum, M., Pang, H., Collins, N., Burns, C. C., & Vega, E. (2021) · Microbiology Spectrum · doi:10.1128/spectrum.00668-21 · Cited by 25 · see citing works
The role of genetic sequencing and analysis in the polio eradication programme
Jorgensen, D., Pons-Salort, M., Shaw, A. G., & Grassly, N. C. (2020) · Virus Evolution · doi:10.1093/ve/veaa040 · Cited by 31 · see citing works
The Challenge of Global Poliomyelitis Eradication
Garon, J. R., Cochi, S. L., & Orenstein, W. A. (2015) · Infectious Disease Clinics of North America · doi:10.1016/j.idc.2015.07.003 · Cited by 32 · see citing works
Song, Y., Gorbatsevych, O., Liu, Y., Mugavero, J., Shen, S. H., Ward, C. B., Asare, E., Jiang, P., Paul, A. V., Mueller, S., et al. (2017) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1714385114 · Cited by 30 · see citing works
Valesano, A. L., Taniuchi, M., Fitzsimmons, W. J., Islam, M. O., Ahmed, T., Zaman, K., Haque, R., Wong, W., Famulare, M., & Lauring, A. S. (2020) · Cell Host & Microbe · doi:10.1016/j.chom.2020.10.011 · Cited by 30 · see citing works
Tao, Z., Song, Y., Wang, H., Zhang, Y., Yoshida, H., Ji, S., Xu, A., Song, L., Liu, Y., Cui, N., et al. (2012) · Applied and Environmental Microbiology · doi:10.1128/aem.01861-12 · Cited by 29 · see citing works
Yan, D., Li, L., Zhu, S., Zhang, Y., An, J., Wang, D., Wen, N., Jorba, J. C., Liu, W. Y., Zhong, G., et al. (2010) · Journal of Clinical Microbiology · doi:10.1128/jcm.00712-10 · Cited by 28 · see citing works
Self-citationZhang, Y., Zhu, S., Yan, D., Liu, G., Bai, R., Wang, D., Chen, L., Zhu, H., An, H., Kew, O. M., et al. (2010) · PLoS ONE · doi:10.1371/journal.pone.0015300 · Cited by 29 · see citing works
Self-citationKorotkova, 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
Zhang, 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
Zhang, Y., Yan, D., Zhu, S., Nishimura, Y., Ye, X., Wang, D., Jorba, J. C., Zhu, H., An, H., Shimizu, H., et al. (2015) · Scientific Reports · doi:10.1038/srep17291 · Cited by 25 · see citing works
Self-citationDetection of Vaccine-Derived Polioviruses in Mexico Using Environmental Surveillance
Esteves-Jaramillo, A., Estívariz, C. F., Peñaranda, S., Richardson, V., Reyna, J., Coronel, D. L., Carrion, V., Landaverde, M., Wassilak, S. G. F., Pérez-Sánchez, E. E., et al. (2014) · The Journal of Infectious Diseases · doi:10.1093/infdis/jiu183 · Cited by 25 · see citing works
Burns, C. C., Kilpatrick, D. R., Iber, J. C., Chen, Q., & Kew, O. M. (2016) · Methods in molecular biology · doi:10.1007/978-1-4939-3292-4_9 · Cited by 24 · see citing works
Self-citationvan der Sanden, S., Pallansch, M. A., van de Kassteele, J., El-Sayed, N., Sutter, R. W., Koopmans, M., & van der Avoort, H. (2009) · Journal of Virology · doi:10.1128/jvi.02388-08 · Cited by 24 · see citing works
Faleye, T. O. C., Bowes, D. A., Driver, E. M., Adhikari, S., Adams, D., Varsani, A., Halden, R. U., & Scotch, M. (2021) · Viruses · doi:10.3390/v13091803 · Cited by 22 · see citing works
Tao, Z., Zhang, Y., Liu, Y. Z., Xu, A., Lin, X., Yoshida, H., Xiong, P., Zhu, S., Wang, S., Yan, D., et al. (2013) · PLoS ONE · doi:10.1371/journal.pone.0083975 · Cited by 22 · see citing works
Molecular evolution and epidemiology of echovirus 6 in Finland
Smura, T., Kakkola, L., Blomqvist, S., Klemola, P., Parsons, A., Kallio‐Kokko, H., Savolainen‐Kopra, C., Kainov, D. E., & Roivainen, M. (2013) · Infection Genetics and Evolution · doi:10.1016/j.meegid.2013.02.011 · Cited by 23 · see citing works
Selective Factors Associated with the Evolution of Codon Usage in Natural Populations of Arboviruses
Velázquez-Salinas, L., Zárate, S., Eschbaumer, M., Lobo, F. P., Gladue, D. P., Arzt, J., Novella, I. S., & Rodrı́guez, L. L. (2016) · PLoS ONE · doi:10.1371/journal.pone.0159943 · Cited by 23 · see citing works
Snider, C. J., Boualam, L., Tallis, G. F., Takashima, Y., Abeyasinghe, R. R., Lo, Y.-R. J., Grabovac, V., Avagyan, T., Aslam, S. K., Eltayeb, A. O., et al. (2022) · Vaccine · doi:10.1016/j.vaccine.2022.02.022 · Cited by 24 · see citing works
Blomqvist, S., Savolainen‐Kopra, C., Paananen, A., Bassioni, L. E., Nasr, E. M. E. M., Firstova, L., Zamiatina, N. A., Kutateladze, T., & Roivainen, M. (2010) · Virus Research · doi:10.1016/j.virusres.2010.05.006 · Cited by 22 · 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
Self-citationAngez, M., Shaukat, S., Alam, M. M., Sharif, S., Khurshid, A., & Zaidi, S. S. Z. (2012) · Virology Journal · doi:10.1186/1743-422x-9-51 · Cited by 21 · see citing works
Shaw, A., Mampuela, T. K., Lokilo, E., Pratt, C. B., Troman, C. M., Bujáki, E., O’Toole, A. N., Akello, J. O., Amuri-Aziza, A., Kinganda-Lusamaki, E., et al. (2023) · Nature Microbiology · doi:10.1038/s41564-023-01453-4 · Cited by 20 · see citing works
Sutter, 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
Self-citationZhao, K., Jorba, J. C., Shaw, J., Iber, J. C., Chen, Q., Bullard, K., Kew, O. M., & Burns, C. C. (2017) · Computational and Structural Biotechnology Journal · doi:10.1016/j.csbj.2017.09.004 · Cited by 18 · see citing works
Self-citationShaw, J., Jorba, J. C., Zhao, K., Iber, J. C., Chen, Q., Adu, F., Adeniji, J. A., Bukbuk, D. N., Baba, M., Henderson, E., et al. (2018) · Journal of Virology · doi:10.1128/jvi.01949-17 · Cited by 18 · see citing works
Self-citationSmura, T., Blomqvist, S., Vuorinen, T., Ivanova, O. E., Samoilovich, E., Al‐Hello, H., Savolainen‐Kopra, C., Hovi, T., & Roivainen, M. (2014) · PLoS ONE · doi:10.1371/journal.pone.0093737 · Cited by 17 · 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
Cui, A., Zhu, Z. H., Mao, N., Si, Y., Ma, Y., Hu, Y., Deng, X., Wang, L., Zeng, L., Zhang, Y., et al. (2018) · Vaccine · doi:10.1016/j.vaccine.2018.08.028 · Cited by 17 · see citing works
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- Authors
- Jorba, J., Campagnoli, R., De, L., & Kew, O.
- Affiliations
- Centers for Disease Control and Prevention (US)
- Division of Viral Diseases, National Center for Immunization and Respiratory Diseases, Centers for Disease Control and Prevention, Atlanta, Georgia 30333
- Corresponding author
- Jorba, Jaume
- ORCID
- Jorba, Jaume
- Venue
- Journal of Virology
- Publisher
- American Society for Microbiology
- Published
- 2008-05
- Volume
- 82
- Issue
- 9
- Pages
- 4429-4440
- ISSN
- 0022-538X (ISSN-L)
- 1098-5514
- PMC
- PMC2293050
- OpenAlex
- W1981598477
- Cited by
- 177
- References
- 94
- Citations by year
- 2026: 1 · 2025: 6 · 2024: 9 · 2023: 11 · 2022: 10 · 2021: 8 · 2020: 6 · 2019: 3 · 2018: 12 · 2017: 16 · 2016: 16 · 2015: 9 · 2014: 17 · 2013: 12 · 2012: 8
- FWCI
- 6.27
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Journal of Virology (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Evolution and Genetic Dynamics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Phylogenetic Studies
- Health Sciences › Medicine › Cardiology and Cardiovascular Medicine › Viral Infections and Immunology Research
- Keywords
- poliovirus type 1, molecular clock calibration, synonymous substitution rate, nonsynonymous substitution rate, purifying selection, substitution saturation, divergence time estimation, viral evolution
- MeSH terms
- Calibration, Biological Evolution, Kinetics, Models, Genetic, Phylogeny, Point Mutation, Poliovirus, Capsid Proteins
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