Skip to main content

Advertisement

Log in

Prevalence and Bayesian Phylogenetics of Enteroviruses Derived From Environmental Surveillance Around Polio Vaccine Switch Period in Shandong Province, China

  • Original Paper
  • Published:
Food and Environmental Virology Aims and scope Submit manuscript

Abstract

We present the results of environmental surveillance for poliovirus (PV) and non-poliovirus (NPEV) around the switch from trivalent to bivalent oral polio-vaccine (OPV) which occurred in China in May 2016. Sewage samples were collected in Jinan and Linyi city from 2015 to 2017. Enterovirus (EV) isolation, VP1 amplification, Sanger sequencing, and phylogenetic analyses were performed. Among105 sewage samples (36 in Jinan and 69 in Linyi), 101 were positive for EV, with 74.3% (78/105) PV-positive samples and 90.5% (95/105) NPEV-positive samples. A total of 893 EV isolates were obtained, including 326 (36.5%) PVs and 567 (63.5%) NPEVs. Echovirus (E) -11 was the most common serotype out of 18 detected NPEV types (120/567), followed by E-3 (75/567) and E-6 (74/567). PV2 vanished and PV3 came to be the ascendant PV type in sewage after May 2016. Eight PV isolates were judged as pre-vaccine-derived poliovirus (pre-VDPV) and no VDPV or wild PV isolates were monitored. Bayesian phylogenetics demonstrated global E-11 originated in 1876 and evolved with the estimated rate of 4.63 × 10–3 nucleotide substitutions per site per year (s/s/y). Multiple circulating clusters that originated at different times were coexisting in Shandong province. The most recently common ancestor of global coxsackievirus B5 could date back to 1867, at the evolutionary rate of 3.95 × 10–3 s/s/y. In conclusion, our study described the changes of PVs and NPEVs around the polio vaccine switch period and provided meaningful global molecular epidemiological data for further studies of EV-related diseases among the population.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Abedi, G. R., Watson, J. T., Nix, W. A., Oberste, M. S., & Gerber, S. I. (2018). Enterovirus and Parechovirus Surveillance-United States, 2014–2016. MMWR. Morbidity and Mortality Weekly Report, 67(18), 515–518.

    Article  PubMed  PubMed Central  Google Scholar 

  • Asghar, H., Diop, O. M., Weldegebriel, G., Malik, F., Shetty, S., El Bassioni, L., et al. (2014). Environmental surveillance for polioviruses in the Global Polio Eradication Initiative. Journal of Infectious Diseases, 210(Suppl 1), S294-303.

    Article  PubMed  Google Scholar 

  • Baele, G., Lemey, P., Bedford, T., Rambaut, A., Suchard, M. A., & Alekseyenko, A. V. (2012). Improving the accuracy of demographic and molecular clock model comparison while accommodating phylogenetic uncertainty. Molecular Biology and Evolution, 29(9), 2157–2167.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Baggen, J., Thibaut, H. J., Strating, J., & van Kuppeveld, F. J. M. (2018). The life cycle of non-polio enteroviruses and how to target it. Nature Reviews Microbiology, 16(6), 368–381.

    Article  CAS  PubMed  Google Scholar 

  • 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(2), 645–654.

    Article  CAS  PubMed  Google Scholar 

  • Chen, J. H., Chiu, N. C., Chang, J. H., Huang, F. Y., Wu, K. B., & Lin, T. L. (2005). A neonatal echovirus 11 outbreak in an obstetric clinic. Journal of Microbiology, Immunology, and Infection, 38(5), 332–337.

    PubMed  Google Scholar 

  • Chen, P., Lin, X., Liu, G., Wang, S., Song, L., Tao, Z., et al. (2018). Analysis of enterovirus types in patients with symptoms of aseptic meningitis in 2014 in Shandong, China. Virology, 516, 196–201.

    Article  CAS  PubMed  Google Scholar 

  • Chow, C. B., Tse, H. H., Chan, K. Y., Tam, A., Ho, L. C., Ho, W. Y., et al. (1987). Outbreak of Echo Virus Type 11 Infection in Newborn Infants in a Maternity Ward: Clinical Presentation. Journal of Tropical Pediatrics, 33(6), 305–308.

    Article  CAS  PubMed  Google Scholar 

  • Duintjer Tebbens, R. J., Zimmermann, M., Pallansch, M. A., & Thompson, K. M. (2017). Insights from a Systematic Search for Information on Designs, Costs, and Effectiveness of Poliovirus Environmental Surveillance Systems. Food Environ Virol, 9(4), 361–382.

    Article  PubMed  Google Scholar 

  • Hampton, L. M., Farrell, M., Ramirez-Gonzalez, A., Menning, L., Shendale, S., Lewis, I., et al. (2016). Cessation of Trivalent Oral Poliovirus Vaccine and Introduction of Inactivated Poliovirus Vaccine - Worldwide, 2016. MMWR. Morbidity and Mortality Weekly Report, 65(35), 934–938.

    Article  PubMed  Google Scholar 

  • Huang, B., Harrower, B., Burtonclay, P., Constantino, T., & Warrilow, D. (2017). Genome Sequences of Coxsackievirus B5 Isolates from Two Children with Meningitis in Australia. Genome Announc, 5(41), e01125-e1217.

    Article  PubMed  PubMed Central  Google Scholar 

  • Ivanova, O. E., Yarmolskaya, M. S., Eremeeva, T. P., Babkina, G. M., Baykova, O. Y., Akhmadishina, L. V., et al. (2019). Environmental Surveillance for Poliovirus and Other Enteroviruses: Long-Term Experience in Moscow, Russian Federation, 2004–2017. Viruses, 11(5), 424.

    Article  CAS  PubMed Central  Google Scholar 

  • Jacques, J., Moret, H., Minette, D., Leveque, N., Jovenin, N., Deslee, G., et al. (2008). Epidemiological, molecular, and clinical features of enterovirus respiratory infections in French children between 1999 and 2005. Journal of Clinical Microbiology, 46(1), 206–213.

    Article  PubMed  Google Scholar 

  • Ji, H., Fan, H., Lu, P. X., Zhang, X. F., Ai, J., Shi, C., et al. (2019). Surveillance for severe hand, foot, and mouth disease from 2009 to 2015 in Jiangsu province: epidemiology, etiology, and disease burden. BMC Infectious Diseases, 19(1), 79.

    Article  PubMed  PubMed Central  Google Scholar 

  • Jorba, J., Diop, O. M., Iber, J., Henderson, E., Zhao, K., Quddus, A., et al. (2019). Update on Vaccine-Derived Poliovirus Outbreaks - Worldwide, January 2018-June 2019. MMWR. Morbidity and Mortality Weekly Report, 68(45), 1024–1028.

    Article  PubMed  PubMed Central  Google Scholar 

  • Kroneman, A., Vennema, H., et al. (2011). An automated genotyping tool for enteroviruses and noroviruses. Journal of Clinical Virology, 51(2), 121–125.

    Article  CAS  PubMed  Google Scholar 

  • Kumthip, K., Khamrin, P., Ushijima, H., & Maneekarn, N. (2017). Multiple enterovirus genotypes circulating in children hospitalized with acute gastroenteritis in Thailand. Infect Genet Evol, 55, 324–331.

    Article  PubMed  Google Scholar 

  • Liu, D. P., Wang, T. A., Huang, W. T., Chang, L. Y., Wang, E. T., Cheng, S. H., et al. (2016). Disease burden of enterovirus infection in Taiwan: Implications for vaccination policy. Vaccine, 34(7), 974–980.

    Article  PubMed  Google Scholar 

  • Lu, J., Kang, M., Zeng, H., Zhong, Y., Fang, L., Zheng, X., et al. (2020). Tracking echovirus eleven outbreaks in Guangdong, China: a metatranscriptomic, phylogenetic, and epidemiological study. Virus Evol, 6(1), 029.

    Article  Google Scholar 

  • Matsuura, K., Hasegawa, S., Nakayama, T., Morita, O., & Uetake, H. (1984). Viral pollution of the rivers in Toyama City. Microbiology and Immunology, 28(5), 575–588.

    Article  CAS  PubMed  Google Scholar 

  • Oberste, M. S., Maher, K., Flemister, M. R., Marchetti, G., Kilpatrick, D. R., & Pallansch, M. A. (2000). Comparison of classic and molecular approaches for the identification of untypeable enteroviruses. Journal of Clinical Microbiology, 38(3), 1170–1174.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Oberste, M. S., Maher, K., Williams, A. J., Dybdahl-Sissoko, N., Brown, B. A., Gookin, M. S., et al. (2006). Species-specific RT-PCR amplification of human enteroviruses: a tool for rapid species identification of uncharacterized enteroviruses. Journal of General Virology, 87(Pt 1), 119–128.

    Article  CAS  PubMed  Google Scholar 

  • Posada, D. (2008). jModelTest: Phylogenetic Model Averaging. Molecular Biology and Evolution, 25(7), 1253–1256.

    Article  CAS  PubMed  Google Scholar 

  • Rotbart, H. A. (1995). Enteroviral Infections of the Central Nervous System. Clinical Infectious Diseases, 20(4), 971–981.

    Article  CAS  PubMed  Google Scholar 

  • Sedmak, G., Bina, D., & MacDonald, J. (2003). Assessment of an Enterovirus Sewage Surveillance System by Comparison of Clinical Isolates with Sewage Isolates from Milwaukee, Wisconsin, Collected August 1994 to December 2002. Applied and Environment Microbiology, 69(12), 7181.

    Article  CAS  Google Scholar 

  • Takahashi, S., Metcalf, C. J. E., Arima, Y., Fujimoto, T., Shimizu, H., Rogier van Doorn, H., et al. (2018). Epidemic dynamics, interactions and predictability of enteroviruses associated with hand, foot and mouth disease in Japan. Journal of the Royal Society, Interface, 15(146), 20180507.

    Article  PubMed  PubMed Central  Google Scholar 

  • Tao, Z., Wang, H., Li, Y., Xu, A., Zhang, Y., Song, L., et al. (2011). Cocirculation of two transmission lineages of echovirus 6 in jinan, china, as revealed by environmental surveillance and sequence analysis. Applied and Environment Microbiology, 77(11), 3786–3792.

    Article  CAS  Google Scholar 

  • Tao, Z., Wang, H., Liu, Y., Li, Y., Jiang, P., Liu, G., et al. (2014). Non-polio enteroviruses from acute flaccid paralysis surveillance in Shandong Province, China, 1988–2013. Sci Rep, 4, 6167.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tapparel, C., Siegrist, F., Petty, T. J., & Kaiser, L. (2013). Picornavirus and enterovirus diversity with associated human diseases. Infect Genet Evol, 14, 282–293.

    Article  PubMed  Google Scholar 

  • Tsuno, K., Miyatake, C., Nishijima, H., Hotta, C., Ogawa, T., & Asano, T. (2018). Coxsackievirus B5 Aseptic Meningitis in Infants in Chiba Prefecture, Japan, in 2016. J Nippon Med Sch, 85(3), 187–190.

    Article  PubMed  Google Scholar 

  • Vreugdenhil, G. R., Schloot, N. C., Hoorens, A., Rongen, C., Pipeleers, D. G., Melchers, W. J., et al. (2000). Acute onset of type I diabetes mellitus after severe echovirus 9 infection: putative pathogenic pathways. Clinical Infectious Diseases, 31(4), 1025–1031.

    Article  CAS  PubMed  Google Scholar 

  • Walker, P. J., Siddell, S. G., Lefkowitz, E. J., Mushegian, A. R., Dempsey, D. M., Dutilh, B. E., et al. (2019). Changes to virus taxonomy and the International Code of Virus Classification and Nomenclature ratified by the International Committee on Taxonomy of Viruses (2019). Archives of Virology, 164(9), 2417–2429.

    Article  CAS  PubMed  Google Scholar 

  • Wang, H., Tao, Z., Li, Y., Lin, X., Yoshida, H., Song, L., et al. (2014). Environmental surveillance of human enteroviruses in Shandong Province, China, 2008 to 2012: serotypes, temporal fluctuation, and molecular epidemiology. Applied and Environment Microbiology, 80(15), 4683–4691.

    Article  Google Scholar 

  • Wang, Q., Lin, X., Wang, H., Tao, Z., & Xu, A. (2017). Molecular epidemiology of Coxsackievirus B5 in Shandong province, China, in 2014. Bing Du Xue Bao, 33(4), 518–523.

    Google Scholar 

  • Xie, W., Lewis, P. O., Fan, Y., Kuo, L., & Chen, M. H. (2011). Improving marginal likelihood estimation for Bayesian phylogenetic model selection. Systematic Biology, 60(2), 150–160.

    Article  PubMed  Google Scholar 

  • Zheng, H., Lu, J., Zhang, Y., Yoshida, H., Guo, X., Liu, L., et al. (2013). Prevalence of nonpolio enteroviruses in the sewage of Guangzhou city, China, from 2009 to 2012. Applied and Environment Microbiology, 79(24), 7679–7683.

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This study was supported by the Taishan Scholar Program of Shandong Province (Grant Number ts201511105); the Taishan Scholar Program of Youth Experts; the National Natural Science Foundation of China (Grant Numbers 81573209, 82003510); the Natural Science Foundation of Shandong Province, China (Grant Number ZR2019BH085).

Author information

Authors and Affiliations

Authors

Contributions

Conceptualization: AX, ZT, PC, Formal analysis: CZ, Funding acquisition: AX, PC, ZT, Investigation: XL, FJ, SW, Methodology: AX, ZT, PC, Project administration: AX, ZT, Resources: PX, YL, QX, LZ, Supervision: AX, ZT, QX, LZ, Writing-original draft: CZ, Writing-review & editing: ZT, CZ.

Corresponding authors

Correspondence to Zexin Tao or Aiqiang Xu.

Ethics declarations

Conflict of interest

We declare that we have no known conflict of financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary file1 (PDF 135 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zhao, C., Lin, X., Ji, F. et al. Prevalence and Bayesian Phylogenetics of Enteroviruses Derived From Environmental Surveillance Around Polio Vaccine Switch Period in Shandong Province, China. Food Environ Virol 12, 321–332 (2020). https://doi.org/10.1007/s12560-020-09449-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12560-020-09449-7

Keywords

Navigation