Food and Environmental Virology

, Volume 11, Issue 2, pp 198–203 | Cite as

Environmental Surveillance of Human Enteroviruses in Córdoba City, Argentina: Prevalence and Detection of Serotypes from 2009 to 2014

  • Adrian A. FaríasEmail author
  • Laura N. Mojsiejczuk
  • Fernando S. Flores
  • Juan J. Aguilar
  • Veronica E. Prez
  • Gisela Masachessi
  • Silvia V. Nates
Brief Communication


Environmental surveillance is an effective approach to investigate the circulation of human enteroviruses (EVs) in the population. EVs excreted by patients who present diverse clinical syndromes can remain infectious in the environment for several weeks, and limited data on circulating environmental EVs are available. A 6-year (2009–2014) surveillance study was conducted to detect non-polio enteroviruses (NPEVs) in the urban sewage of Cordoba city, Argentina. Echovirus 6 (E-6) was the most prevalent (28%), followed by E-14 (17%), E-16 (14%), Coxsackievirus (CV) A9 (11%), E-20 (9%), and CVA24 (6%). Other minority serotypes (E-7, E-13, E-21, E-25, and CVB4) were found, which together represented 14% of the total. In the absence of a systematic EV disease surveillance system, the detection and characterization of sewage-borne NPEVs will help us better understand the changes in EV disease trends and the epidemic background of circulating EVs, which could help interpret the EV trends and warn of future outbreaks in this area.


Enterovirus PCR Environmental surveillance Serotypes 


Author Contributions

AAF conceived and designed the experiments, LNM, FSF, and JJA, performed the experiments and analyzed the data. VEP, GM, and SVN contributed materials/analysis tools. AAF wrote the paper.


This work was supported by SECyT Cat B 1565/2014 and PICT-2016-2165.

Compliance with Ethical Standards

Conflict of interest

On behalf of all authors, the corresponding author (Dr Adrian A. Farias) states that there is no conflict of interest.

Ethical Approval

This article does not contain any studies with human participants or animals performed by any of the authors.


  1. Barril, P. A., Fumian, T. M., Prez, V. E., Gil, P. I., Martínez, L. C., Giordano, M. O.,et al (2015). Rotavirus seasonality in urban sewage from Argentina: Effect of meteorological variables on the viral load and the genetic diversity. Environmental Research, 138, 409–415.CrossRefGoogle Scholar
  2. Casas, I., Palacios, G. F., Trallero, G., Cisterna, D., Freire, M. C., & Tenorio, A. (2001). Molecular characterization ofhumanenteroviruses in clinical samples: Comparison between VP2, VP1, and RNA polymerase regions using RT nested PCR assays and direct sequencing of products. Journal of Medical Virology, 65, 138–148.CrossRefGoogle Scholar
  3. Casas, I., Tenorio, A., Echevarria, J. M., Klapper, P. E., & Cleator, G. M. (1997). Detection of enteroviral RNA and specific DNA of herpesviruses by multiplex genome amplification. Journal of Virological Methods, 66, 39–50.CrossRefGoogle Scholar
  4. Chen, P., Li, Y., Tao, Z., Wang, H., Lin, X., Liu, Y., Wang, S., Zhou, N., Wang, P., & Xu, A. (2017). Evolutionary phylogeography and transmission pattern of echovirus 14: An exploration of spatiotemporal dynamics based on the 26-year acute flaccid paralysis surveillance in Shandong, China. BMC Genomics. 7, 18(1), 48. Scholar
  5. Farías, A., Cabrerizo, M., Ré, V., Glatstein, N., Pisano, B., Spinsanti, L., et al. (2011). Molecular identification of human enteroviruses in children with neurological infections from the central region of Argentina. Archives of Virology, 156(1), 129–133.CrossRefGoogle Scholar
  6. Farías, A. A., Mojsiejczuk, L. N., Pisano, M. B., Flores, F. S., Aguilar, J. J., Jean, A. N., Yanes, L. A., Masachessi, G., Prez, V. E., Isa, M. B., Campos, R. H., Ré, V. E., & Nates, S. V. (2018). Environmental surveillance of enteroviruses in Central Argentina: First detection and evolutionary analyses of E14. Food and Environmental Virology, 10(1), 121–126. Scholar
  7. Kargar, M., Sadeghipour, S., & Nategh, R. (2009). Environmental surveillance of non-polio enteroviruses in Iran. Virology Journal, 6, 149.CrossRefGoogle Scholar
  8. 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, 51(2), 121–125. Scholar
  9. Kyriakopoulou, Z., Bletsa, M., Tsakogiannis, D., Dimitriou, T. G., Amoutzias, G. D., Gartzonika, C., et al. (2015). Molecular epidemiology and evolutionary dynamics of Echovirus 3 serotype. Infection, Genetics and Evolution, 32, 305–312. Scholar
  10. Medina, N. H., Haro-Muñoz, E., Pellini, A. C., Machado, B. C., Russo, D. H., Timenetsky, M. D., & Carmona, R. C. (2016). Acute hemorrhagic conjunctivitis epidemic in São Paulo State, Brazil, 2011. Revista Panamericana de Salud Pública., 39(2), 137–141.Google Scholar
  11. Pallansch, M., & Roos, R. (2007). Enteroviruses: Polioviruses, coxsackieviruses, echoviruses, and newer enteroviruses. In D. M. Knipe, P. M. Howley, D. E. Griffin, R. A. Lamb, M. A. Martin, B. Roizman & S. E. Straus (Eds.), Fields virology (5th edn., pp. 839–893). Philadelphia: Lippincott Williams & Wilkins.Google Scholar
  12. Pellegrinelli, L., Binda, S., Chiaramonte, I., Primache, V., Fiore, L., Battistone, A., Fiore, S., Gambino, M., Bubba, L., & Barbi, M. (2013). Detection and distribution of culturable Human Enteroviruses through environmental surveillance in Milan, Italy. Journal of Applied Microbiology, 115(5), 1231–1239. Scholar
  13. Pérez, M. G., Rosanova, M. T., Freire, M. C., et al. (2017). Aumento inusual de casos de mielitis en un hospital pediátrico en Argentina. Archivos Argentinos de Pediatria, 1;115(4), 364–369. Scholar
  14. Pinto, R., Alegre, D., Dominguez, A., El-Senousy, W., Sanchez, G., Villena, C., et al. (2007). Hepatitis A virus in urban sewage from two Mediterranean countries. Epidemiology & Infection, 135, 270–273.CrossRefGoogle Scholar
  15. Prado, T., Gaspar, A. M., & Miagostovich, M. P. (2014). Detection of enteric viruses in activated sludge by feasible concentration methods. Brazilian Journal of Microbiology, 19, 45(1), 343–349.CrossRefGoogle Scholar
  16. 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, 7181.CrossRefGoogle Scholar
  17. Vecchia, A. D., Fleck, J. D., Kluge, M., Comerlato, J., Bergamaschi, B., Luz, R. B., Arantes, T. S., Silva, J. V., Thewes, M. R., & Spilki, F. R. (2012). Assessment of enteric viruses in a sewage treatment plant located in Porto Alegre, southern Brazil. Brazilian Journal of Biology, 72(4), 839–846.CrossRefGoogle Scholar
  18. WHO. (2003). Guidelines for environmental surveillance of poliovirus circulation. Geneva: World Health Organization. Accessed 18 Nov 2015.
  19. Zhang, T., Du, J., Xue, Y., Su, H., Yang, F., & Jin, Q. (2013). Epidemics and frequent recombination within species in outbreaks of human enterovirus B-associated hand, foot and mouth disease in Shandong China in 2010 and 2011. PLoS ONE, 8, e67157. Scholar
  20. Zheng, H., Jing Lu, J., Yong Zhang, Y., Hiromu Yoshida, H., Xue Guo, X., et al. (2013). Prevalence of nonpolio enteroviruses in the sewage of Guangzhou city, China, from 2009 to 2012. Applied and Environmental Microbiology. 79(24): 7679–7683. Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Facultad de Ciencias Médicas, Instituto de Virología “Dr. J. M. Vanella”Universidad Nacional de CórdobaCórdobaArgentina
  2. 2.Consejo Nacional de Investigaciones Científicas y Técnicas, CONICETBuenos AiresArgentina
  3. 3.Departamento de Microbiología, Inmunología y Biotecnología, Cátedra de Virología, Facultad de Farmacia y BioquímicaUniversidad de Buenos AiresBuenos AiresArgentina

Personalised recommendations