Abstract
Human Enteroviruses (hEVs) are responsible for a wide variety of human diseases. During hEVs infection, virions are excreted in human feces and the fecal–oral route is the primary pathway for person-to-person transmission. Sewage surveillance could help in monitoring hEVs circulation and describing their diversity in a specific population. In this study, sewage samples collected in Buenos Aires Metropolitan Area (Argentina) were retrospectively studied through an amplicon-deep sequencing approach and phylogenetic analyses to characterize hEVs spread. We identified 17 different hEVs types belonging to A, B, and C species. To the best of our knowledge, this is the first report in Buenos Aires for 7 identified hEV-C types. Phylogenetic analyses suggest several introductions of coxsackievirus B4, echovirus 1, and echovirus 9 in the country, along with the national spread reached by some variants. Besides, well-supported monophyletic groups of Argentine, Uruguayan, and Brazilian strains unveiled regional circulation patterns for some variants. These results extend our knowledge about hEVs circulation in Buenos Aires and might exhort authorities to implement more active sewage surveillance in the region.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data Availability
Not applicable.
Code Availability
Not applicable.
References
Adeniji, J. A., Oragwa, A. O., George, U. E., Ibok, U. I., Faleye, T., & Adewumi, M. O. (2017). Preponderance of enterovirus C in RD-L20B-cell-culture-negative stool samples from children diagnosed with acute flaccid paralysis in Nigeria. Archives of virology. https://doi.org/10.1007/s00705-017-3466-2
Anisimova, M., & Gascuel, O. (2006). Approximate likelihood-ratio test for branches: A fast, accurate, and powerful alternative. Systematic biology. https://doi.org/10.1080/10635150600755453
Battistone, A., Buttinelli, G., Fiore, S., Amato, C., Bonomo, P., Patti, A. M., Vulcano, A., Barbi, M., Binda, S., Pellegrinelli, L., Tanzi, M. L., Affanni, P., Castiglia, P., Germinario, C., Mercurio, P., Cicala, A., Triassi, M., Pennino, F., & Fiore, L. (2014). Sporadic isolation of sabin-like polioviruses and high-level detection of non-polio enteroviruses during sewage surveillance in seven Italian cities, after several years of inactivated poliovirus vaccination. Applied and environmental microbiology. https://doi.org/10.1128/AEM.00108-14
Benschop, K., van der Avoort, H. G., Jusic, E., Vennema, H., van Binnendijk, R., & Duizer, E. (2017). Polio and Measles Down the Drain: Environmental Enterovirus Surveillance in the Netherlands, 2005 to 2015. Applied and environmental microbiology. https://doi.org/10.1128/AEM.00558-17
Bessaud, M., & Delpeyroux, F. (2020). Enteroviruses-the famous unknowns. The Lancet. Infectious diseases. https://doi.org/10.1016/S1473-3099(19)30636-X
Brinkman, N. E., Fout, G. S., & Keely, S. P. (2017). Retrospective Surveillance of Wastewater To Examine Seasonal Dynamics of Enterovirus Infections. mSphere. https://doi.org/10.1128/mSphere.00099-17
Carballo, C. M., Erro, M. G., Sordelli, N., Vazquez, G., Mistchenko, A. S., Cejas, C., Rodriguez, M., Cisterna, D. M., Freire, M. C., Contrini, M. M., & Lopez, E. L. (2019). Acute Flaccid Myelitis Associated with Enterovirus D68 in Children, Argentina, 2016. Emerging infectious diseases. https://doi.org/10.3201/eid2503.170897
Chaves, S. S., Lobo, S., Kennett, M., & Black, J. (2001). Coxsackie virus A24 infection presenting as acute flaccid paralysis. Lancet (London, England). https://doi.org/10.1016/s0140-6736(00)04066-6
Cisterna, D., Lema, C., Riviello Lopez, G., Freyre, L., Martinez, L., Torres, C., Mbayed, V., & Freire, M. C. (2008). Detección y caracterización de Enterovirus y Hepatitis A en el Riachuelo y Río de la Plata. IX Congreso Argentino de Virología. Revista Argentina de Microbiología, Supl. 1. (Unpublished).
Cisterna, D. M., Palacios, G., Rivero, K., Girard, D., Lema, C., & Freire, M. C. (2007). Epidemiologia de los enterovirus asociados a enfermedades neurologicas [Epidemiology of enterovirus associated with neurologic diseases]. Medicina, 67(2), 113–119.
Coutinho, C., Siqueira, J., Machado, R. S., Bandeira, R., Ferreira, J. L., Alves, J., Gabbay, Y. B., & Tavares, F. N. (2020). Enterovirus detection and serotyping of fecal material collected from three children living on the outskirts of Belém city, Amazon region, Brazil, during the first 3 years of life (1983–1986). Journal of medical virology. https://doi.org/10.1002/jmv.25656
Dos Santos, G. P., Skraba, I., Oliveira, D., Lima, A. A., de Melo, M. M., Kmetzsch, C. I., da Costa, E. V., & da Silva, E. E. (2006). Enterovirus meningitis in Brazil, 1998–2003. Journal of medical virology. https://doi.org/10.1002/jmv.20509
Edgar, R. C. (2004). MUSCLE: a multiple sequence alignment method with reduced time and space complexity. BMC Bioinformatics. https://doi.org/10.1186/1471-2105-5-113
Fernandez-Garcia, M. D., Kebe, O., Fall, A. D., & Ndiaye, K. (2017). Identification and molecular characterization of non-polio enteroviruses from children with acute flaccid paralysis in West Africa, 2013–2014. Scientific reports. https://doi.org/10.1038/s41598-017-03835-1
Guindon, S., Dufayard, J. F., Lefort, V., Anisimova, M., Hordijk, W., & Gascuel, O. (2010). New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Systematic biology. https://doi.org/10.1093/sysbio/syq010
Hall, T. A. (1999). BioEdit: A User-Friendly Biological Sequence Alignment Editor and Analysis Program for Windows 95/98/NT. Nucleic Acids Symposium Series, 41, 95–98.
Harvala, H., Calvert, J., Van Nguyen, D., Clasper, L., Gadsby, N., Molyneaux, P., Templeton, K., McWilliams Leitch, C., & Simmonds, P. (2014). Comparison of diagnostic clinical samples and environmental sampling for enterovirus and parechovirus surveillance in Scotland, 2010 to 2012. Euro surveillance: bulletin Europeen sur les maladies transmissibles = European communicable disease bulletin. https://doi.org/10.2807/1560-7917.es2014.19.15.20772
Horner, L. M., Poulter, M. D., Brenton, J. N., & Turner, R. B. (2015). Acute Flaccid Paralysis Associated with Novel Enterovirus C105. Emerging infectious diseases. https://doi.org/10.3201/eid2110.150759
Hyypiä, T., Hovi, T., Knowles, N. J., & Stanway, G. (1997). Classification of enteroviruses based on molecular and biological properties. The Journal of general virology. https://doi.org/10.1099/0022-1317-78-1-1
Jegouic, S., Joffret, M. L., Blanchard, C., Riquet, F. B., Perret, C., Pelletier, I., Colbere-Garapin, F., Rakoto-Andrianarivelo, M., & Delpeyroux, F. (2009). Recombination between polioviruses and co-circulating Coxsackie A viruses: role in the emergence of pathogenic vaccine-derived polioviruses. PLoS Pathogens. https://doi.org/10.1371/journal.ppat.1000412
Jiang, P., Faase, J. A., Toyoda, H., Paul, A., Wimmer, E., & Gorbalenya, A. E. (2007). Evidence for emergence of diverse polioviruses from C-cluster coxsackie A viruses and implications for global poliovirus eradication. Proceedings of the National Academy of Sciences. https://doi.org/10.1073/pnas.0700451104
Kroneman, A., Vennema, H., Deforche, K., & v d Avoort, H., Peñaranda, S., Oberste, M. S., Vinjé, J., & Koopmans, M. . (2011). An automated genotyping tool for enteroviruses and noroviruses. Journal of clinical virology: the official publication of the Pan American Society for Clinical Virology. https://doi.org/10.1016/j.jcv.2011.03.006
Leendertse, M., van Vugt, M., Benschop, K. S., van Dijk, K., Minnaar, R. P., van Eijk, H. W., Hodiamont, C. J., & Wolthers, K. C. (2013). Pleurodynia caused by an echovirus 1 brought back from the tropics. Journal of clinical virology: the official publication of the Pan American Society for Clinical Virology. https://doi.org/10.1016/j.jcv.2013.06.039
Lefort, V., Longueville, J. E., & Gascuel, O. (2017). SMS: Smart Model Selection in PhyML. Molecular biology and evolution. https://doi.org/10.1093/molbev/msx149
Lema, C., Torres, C., Van der Sanden, S., Cisterna, D., Freire, M. C., & Gómez, R. M. (2019). Global phylodynamics of Echovirus 30 revealed differential behavior among viral lineages. Virology. https://doi.org/10.1016/j.virol.2019.02.012
Lizasoain, A., Mir, D., Masachessi, G., Farías, A., Rodríguez-Osorio, N., Victoria, M., Nates, S., & Colina, R. (2021). Environmental Surveillance through Next-Generation Sequencing to Unveil the Diversity of Human Enteroviruses beyond the Reported Clinical Cases. Viruses. https://doi.org/10.3390/v13010120
Mach, O., Verma, H., Khandait, D. W., Sutter, R. W., O’Connor, P. M., Pallansch, M. A., Cochi, S. L., Linkins, R. W., Chu, S. Y., Wolff, C., & Jafari, H. S. (2014). Prevalence of asymptomatic poliovirus infection in older children and adults in northern India: analysis of contact and enhanced community surveillance, 2009. The Journal of infectious diseases. https://doi.org/10.1093/infdis/jit234
Majumdar, M., & Martin, J. (2018). Detection by Direct Next Generation Sequencing Analysis of Emerging Enterovirus D68 and C109 Strains in an Environmental Sample From Scotland. Frontiers in microbiology. https://doi.org/10.3389/fmicb.2018.01956
Mistchenko, A. S., Viegas, M., Latta, M. P., & Barrero, P. R. (2006). Molecular and epidemiologic analysis of enterovirus B neurological infection in Argentine children. Journal of clinical virology: the official publication of the Pan American Society for Clinical Virology. https://doi.org/10.1016/j.jcv.2006.08.009
Nix, W. A., Oberste, M. S., & Pallansch, M. A. (2006). Sensitive, seminested PCR amplification of VP1 sequences for direct identification of all enterovirus serotypes from original clinical specimens. Journal of clinical microbiology. https://doi.org/10.1128/JCM.00542-06
Oberste, M. S., Maher, K., Kilpatrick, D. R., & Pallansch, M. A. (1999). Molecular evolution of the human enteroviruses: correlation of serotype with VP1 sequence and application to picornavirus classification. Journal of virology. https://doi.org/10.1128/JVI.73.3.1941-1948.1999
Ohman, T., King, S. L., Krithivas, A., Cunningham, J., Dickeson, S. K., Santoro, S. A., & Bergelson, J. M. (2001). Echoviruses 1 and 8 are closely related genetically, and bind to similar determinants within the VLA-2 I domain. Virus Research. https://doi.org/10.1016/s0168-1702(01)00226-x
Palacios, G., Casas, I., Cisterna, D., Trallero, G., Tenorio, A., & Freire, C. (2002). Molecular epidemiology of echovirus 30: temporal circulation and prevalence of single lineages. Journal of virology. https://doi.org/10.1128/jvi.76.10.4940-4949.2002
Pallansch, M. A., Oberste, M. S., & Whitton, J. L., et al. (2013). Enteroviruses: Polioviruses, Coxsackieviruses, Echoviruses and Newer Enteroviruses. In D. M. Knipe & P. M. Howley (Eds.), Fields virology (pp. 490–530). Lippincott Williams & Wilkins.
Pina, S., Jofre, J., Emerson, S. U., Purcell, R. H., & Girones, R. (1998). Characterization of a strain of infectious hepatitis E virus isolated from sewage in an area where hepatitis E is not endemic. Applied and environmental microbiology. https://doi.org/10.1128/AEM.64.11.4485-4488.1998
Rao, C. D., Yergolkar, P., & Shankarappa, K. S. (2012). Antigenic diversity of enteroviruses associated with nonpolio acute flaccid paralysis, India, 2007–2009. Emerging infectious diseases. https://doi.org/10.3201/eid1811.111457
Rao, D. C., Ananda Babu, M., Raghavendra, A., Dhananjaya, D., Kumar, S., & Maiya, P. P. (2013). Non-polio enteroviruses and their association with acute diarrhea in children in India. Infection, genetics and evolution: journal of molecular epidemiology and evolutionary genetics in infectious diseases,. https://doi.org/10.1016/j.meegid.2013.04.011
Rognes, T., Flouri, T., Nichols, B., Quince, C., & Mahé, F. (2016). VSEARCH: a versatile open source tool for metagenomics. PeerJ. https://doi.org/10.7717/peerj.2584
Ruggieri, V., Paz, M. I., Peretti, M. G., Rugilo, C., Bologna, R., Freire, C., Vergel, S., & Savransky, A. (2017). Enterovirus D68 infection in a cluster of children with acute flaccid myelitis, Buenos Aires, Argentina, 2016. European journal of paediatric neurology: EJPN: official journal of the European Paediatric Neurology Society. https://doi.org/10.1016/j.ejpn.2017.07.008
Sadeuh-Mba, S. A., Kavunga-Membo, H., Joffret, M. L., Yogolelo, R., Endegue-Zanga, M. C., Bessaud, M., Njouom, R., Muyembe-Tamfu, J. J., & Delpeyroux, F. (2019). Genetic landscape and macro-evolution of co-circulating Coxsackieviruses A and Vaccine-derived Polioviruses in the Democratic Republic of Congo, 2008–2013. PLoS Neglected Tropical Diseases. https://doi.org/10.1371/journal.pntd.0007335
Sapia, E. Y., Maroni, C., Groisman, C., Kromer, H., Lihue Rojo, G., Dastugue, M., & Valinotto, L. (2020). Genotipificación del virus de la enfermedad mano-pie-boca atípica en un hospital pediátrico de la Ciudad de Buenos Aires, Argentina [Atypical hand-foot-mouth disease virus genotyping in a pediatric hospital in Buenos Aires city, Argentina]. Archivos argentinos de pediatria. https://doi.org/10.5546/aap.2020.e199
Tapparel, C., Siegrist, F., Petty, T. J., & Kaiser, L. (2013). Picornavirus and enterovirus diversity with associated human diseases. Infection, genetics and evolution: journal of molecular epidemiology and evolutionary genetics in infectious diseases,. https://doi.org/10.1016/j.meegid.2012.10.016
van der Linden, L., Wolthers, K. C., & van Kuppeveld, F. J. (2015). Replication and Inhibitors of Enteroviruses and Parechoviruses. Viruses. https://doi.org/10.3390/v7082832
Zell, R., Delwart, E., Gorbalenya, A. E., Hovi, T., King, A., Knowles, N. J., Lindberg, A. M., Pallansch, M. A., Palmenberg, A. C., Reuter, G., Simmonds, P., Skern, T., Stanway, G., Yamashita, T., & Ictv Report Consortium. (2017). ICTV Virus Taxonomy Profile: Picornaviridae. The Journal of general virology. https://doi.org/10.1099/jgv.0.000911
Zou, L., Yi, L., Song, Y., Zhang, X., Liang, L., Ni, H., Ke, C., Wu, J., & Lu, J. (2017). A cluster of coxsackievirus A21 associated acute respiratory illness: the evidence of efficient transmission of CVA21. Archives of virology. https://doi.org/10.1007/s00705-016-3201-4
Funding
This study was supported by Programa Polos de Desarrollo Universitario, from the Comisión Coordinadora del Interior, Universidad de la República, Uruguay. Andrés Lizasoain received a PhD scholarship from the Comisión Académica de Posgrados, Universidad de la República, Uruguay.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
Nothing to disclose.
Ethical Approval
Not applicable.
Consent to Participate
Not applicable.
Consent for Publication
Not applicable.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Lizasoain, A., Mir, D., Victoria, M. et al. Human Enterovirus Diversity by Next-Generation Sequencing Analysis in Urban Sewage Samples From Buenos Aires Metropolitan Area, Argentina: A Retrospective Study. Food Environ Virol 13, 259–269 (2021). https://doi.org/10.1007/s12560-021-09468-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12560-021-09468-y