Abstract
Within the initiatives for poliomyelitis eradication by WHO, Italy activated an environmental surveillance (ES) in 2005. ES complements clinical Acute Flaccid Paralysis (AFP) surveillance for possible polio cases, detects poliovirus circulation in environmental sewage, and is used to monitor transmission in communities. In addition to polioviruses, the analyses comprised: (i) the monitoring of the presence of non-polio enteroviruses in sewage samples and (ii) the temporal and geographical distribution of the detected viruses. From 2009 to 2015, 2880 sewage samples were collected from eight cities participating in the surveillance. Overall, 1479 samples resulted positive for enteroviruses. No wild-type polioviruses were found, although four Sabin-like polioviruses were detected. The low degree of mutation found in the genomes of these four isolates suggests that these viruses have had a limited circulation in the population. All non-polio enteroviruses belonged to species B and the most frequent serotype was CV-B5, followed by CV-B4, E-11, E-6, E-7, CV-B3, and CV-B2. Variations in the frequency of different serotypes were also observed in different seasons and/or Italian areas. Environmental surveillance in Italy, as part of the ‘WHO global polio eradication program’, is a powerful tool to augment the polio surveillance and to investigate the silent circulation or the re-emergence of enteroviruses in the population.
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References
Adams, M. J., Lefkowitz, E. J., King, A. M., Harrach, B., Harrison, R. L., Knowles, N. J., et al. (2016). Ratification vote on taxonomic proposals to the International Committee on Taxonomy of Viruses. Archives of Virology, 161(10), 2921–2949. https://doi.org/10.1007/s00705-016-2977-6.
Amvrosieva, T. V., Titov, L. P., Mulders, M., Hovi, T., Dyakonova, O. V., Votyakov, V. I., et al. (2001). Viral water contamination as the cause of aseptic meningitis outbreak in Belarus. Central European Journal of Public Health, 9(3), 154–157.
Antona, D., Leveque, N., Chomel, J. J., Dubrou, S., Levy-Bruhl, D., & Lina, B. (2007). Surveillance of enteroviruses in France, 2000–2004. European journal of Clinical Microbiology & Infectious Diseases: Official Publication of the European Society of Clinical Microbiology, 26(6), 403–412. https://doi.org/10.1007/s10096-007-0306-4.
Aw, T. G., & Gin, K. Y. (2010). Environmental surveillance and molecular characterization of human enteric viruses in tropical urban wastewaters. Journal of Applied Microbiology, 109(2), 716–730. https://doi.org/10.1111/j.1365-2672.2010.04701.x.
Battistone, A., Buttinelli, G., Bonomo, P., Fiore, S., Amato, C., Mercurio, P., et al. (2014b). Detection of Enteroviruses in Influent and Effluent Flow Samples from Wastewater Treatment Plants in Italy. Food and Environmental Virology, 6(1), 13–22. https://doi.org/10.1007/s12560-013-9132-2.
Battistone, A., Buttinelli, G., Fiore, S., Amato, C., Bonomo, P., Patti, A. M., et al. (2014a). 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, 80(15), 4491–4501. https://doi.org/10.1128/AEM.00108-14.
Blomqvist, S., Bassioni, E., El Maamoon Nasr, L., Paananen, E. M., Kaijalainen, A., Asghar, S., H., et al (2012). Detection of imported wild polioviruses and of vaccine-derived polioviruses by environmental surveillance in Egypt. Applied and Environmental Microbiology, 78(15), 5406–5409. https://doi.org/10.1128/AEM.00491-12.
Cao, C. Y., Chen, Q. J., He, C. R., Luo, Z. F., He, Y., Liao, Y. H., et al. (2014). Analysis of genetic characteristics of ECHO6 virus isolated from an epidemic outbreak of encephalitis in Longyan, China. Bing du xue bao = Chinese Journal of Virology, 30(4), 412–416.
CDC (2015). Poliovirus ITD and VDPV 4.0 RT-PCR Training Manual.
Chen, Q., Cao, C., Zhang, Y., He, C., Luo, Z., He, Y., et al. (2015). Genetic analysis of Echovirus 11 isolated from patients with viral encephalitis in Longyan, China. Bing du xue bao = Chinese Journal of Virology, 31(1), 36–41.
Chikhi-Brachet, R., Bon, F., Toubiana, L., Pothier, P., Nicolas, J. C., Flahault, A., et al. (2002). Virus diversity in a winter epidemic of acute diarrhea in France. Journal of Clinical Microbiology, 40(11), 4266–4272.
Chomel, J. J., Antona, D., Thouvenot, D., & Lina, B. (2003). Three ECHOvirus serotypes responsible for outbreak of aseptic meningitis in Rhone-Alpes region, France. European Journal of Clinical Microbiology & Infectious Diseases: Official Publication of the European Society of Clinical Microbiology, 22(3), 191–193. https://doi.org/10.1007/s10096-003-0896-4.
Combelas, N., Holmblat, B., Joffret, M. L., Colbere-Garapin, F., & Delpeyroux, F. (2011). Recombination between poliovirus and coxsackie A viruses of species C: A model of viral genetic plasticity and emergence. Viruses, 3(8), 1460–1484. https://doi.org/10.3390/v3081460.
Costan-Longares, A., Moce-Llivina, L., Avellon, A., Jofre, J., & Lucena, F. (2008). Occurrence and distribution of culturable enteroviruses in wastewater and surface waters of north-eastern Spain. Journal of Applied Microbiology, 105(6), 1945–1955. https://doi.org/10.1111/j.1365-2672.2008.03954.x.
de Roda Husman, A. M., Lodder, W. J., Rutjes, S. A., Schijven, J. F., & Teunis, P. F. (2009). Long-term inactivation study of three enteroviruses in artificial surface and groundwaters, using PCR and cell culture. Applied and Environmental Microbiology, 75(4), 1050–1057. https://doi.org/10.1128/AEM.01750-08.
Di Bartolo, I., Pavoni, E., Tofani, S., Consoli, M., Galuppini, E., Losio, M. N., et al. (2015). Waterborne norovirus outbreak during a summer excursion in Northern Italy. The New Microbiologica, 38(1), 109–112.
Foiadelli, T., Savasta, S., Battistone, A., Kota, M., Passera, C., Fiore, S., et al. (2016). Nucleotide variation in Sabin type 3 poliovirus from an Albanian infant with agammaglobulinemia and vaccine associated poliomyelitis. BMC Infectious Diseases, 16, 277. https://doi.org/10.1186/s12879-016-1587-y.
Fontana, S., Buttinelli, G., Fiore, S., Mulaomerovic, M., Acimovic, J., Amato, C., et al. (2017). Acute Flaccid Paralysis surveillance in Bosnia and Herzegovina: Recent isolation of two Sabin like type 2 poliovirus. Journal of Medical Virology, 89(9), 1678–1681. https://doi.org/10.1002/jmv.24827.
Francy, D. S., Stelzer, E. A., Bushon, R. N., Brady, A. M., Williston, A. G., Riddell, K. R., et al. (2012). Comparative effectiveness of membrane bioreactors, conventional secondary treatment, and chlorine and UV disinfection to remove microorganisms from municipal wastewaters. Water Research, 46(13), 4164–4178. https://doi.org/10.1016/j.watres.2012.04.044.
GPEI (2015). Guidelines on environmental surveillance for detection of polioviruses. http://polioeradication.org/wpcontent/uploads/2016/07/GPLN/GuidelinesES_April2015.pdf.
Groneck, P., Jahn, P., Schuler-Luttmann, S., & Beyrer, K. (2011). Neonatal enterovirus meningitis: Transmission via parents during rooming-in and current epidemiology in Germany. Zeitschrift fur Geburtshilfe und Neonatologie, 215(1), 1–5. https://doi.org/10.1055/s-0030-1255024.
Holmes, C. W., Koo, S. S., Osman, H., Wilson, S., Xerry, J., Gallimore, C. I., et al. (2016). Predominance of enterovirus B and echovirus 30 as cause of viral meningitis in a UK population. Journal of Clinical Virology: The Official Publication of the Pan American Society for Clinical Virology, 81, 90–93. https://doi.org/10.1016/j.jcv.2016.06.007.
Hovi, T., Shulman, L. M., van der Avoort, H., Deshpande, J., Roivainen, M., & EM, D. E. G (2012). Role of environmental poliovirus surveillance in global polio eradication and beyond. Epidemiology and Infection, 140(1), 1–13. https://doi.org/10.1017/S095026881000316X.
Hughes, M. S., Coyle, P. V., & Connolly, J. H. (1992). Enteroviruses in recreational waters of Northern Ireland. Epidemiology and infection, 108(3), 529–536.
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 of the United States of America, 104(22), 9457–9462. https://doi.org/10.1073/pnas.0700451104.
Khetsuriani, N., Lamonte, A., Oberste, M. S., & Pallansch, M. (2006b). Neonatal enterovirus infections reported to the national enterovirus surveillance system in the United States, 1983–2003. The Pediatric infectious disease journal, 25(10), 889–893. https://doi.org/10.1097/01.inf.0000237798.07462.32.
Khetsuriani, N., Lamonte-Fowlkes, A., Oberst, S., & Pallansch, M. A. (2006a). Enterovirus surveillance–United States, 1970–2005. MMWR Surveill Summ, 55(8), 1–20.
Khetsuriani, N., Perehinets, I., Nitzan, D., Popovic, D., Moran, T., Allahverdiyeva, V., et al. (2017). Responding to a cVDPV1 outbreak in Ukraine: Implications, challenges and opportunities. Vaccine, 35(36), 4769–4776. https://doi.org/10.1016/j.vaccine.2017.04.036.
LaBelle, R. L., & Gerba, C. P. (1979). Influence of pH, salinity, and organic matter on the adsorption of enteric viruses to estuarine sediment. Applied and Environmental Microbiology, 38(1), 93–101.
Lee, S. H., Lee, C., Lee, K. W., Cho, H. B., & Kim, S. J. (2005). The simultaneous detection of both enteroviruses and adenoviruses in environmental water samples including tap water with an integrated cell culture-multiplex-nested PCR procedure. Journal of Applied Microbiology, 98(5), 1020–1029. https://doi.org/10.1111/j.1365-2672.2004.02496.x.
Leveque, N., Jacques, J., Renois, F., Antona, D., Abely, M., Chomel, J. J., et al. (2010). Phylogenetic analysis of Echovirus 30 isolated during the 2005 outbreak in France reveals existence of multiple lineages and suggests frequent recombination events. Journal of Clinical Virology: The Official Publication of the Pan American Society for Clinical Virology, 48(2), 137–141. https://doi.org/10.1016/j.jcv.2010.03.011.
Lodder, W. J., van den Berg, H. H., Rutjes, S. A., & de Roda Husman, A. M. (2010). Presence of enteric viruses in source waters for drinking water production in The Netherlands. Applied and Environmental Microbiology, 76(17), 5965–5971. https://doi.org/10.1128/AEM.00245-10.
Lopalco, P. L. (2017). Wild and vaccine-derived poliovirus circulation, and implications for polio eradication. Epidemiology and Infection, 145(3), 413–419. https://doi.org/10.1017/S0950268816002569.
Manor, Y., Shulman, L. M., Kaliner, E., Hindiyeh, M., Ram, D., Sofer, D., et al. (2014). Intensified environmental surveillance supporting the response to wild poliovirus type 1 silent circulation in Israel, 2013. Euro Surveillance: Bulletin Europeen sur les Maladies Transmissibles = European Communicable Disease Bulletin, 19(7), 20708.
Milia, M. G., Cerutti, F., Gregori, G., Burdino, E., Allice, T., Ruggiero, T., et al. (2013). Recent outbreak of aseptic meningitis in Italy due to Echovirus 30 and phylogenetic relationship with other European circulating strains. Journal of Clinical Virology: The Official Publication of the Pan American Society for Clinical Virology, 58(3), 579–583. https://doi.org/10.1016/j.jcv.2013.08.023.
Mirand, A., Henquell, C., Archimbaud, C., Ughetto, S., Antona, D., Bailly, J. L., et al. (2012). Outbreak of hand, foot and mouth disease/herpangina associated with coxsackievirus A6 and A10 infections in 2010, France: A large citywide, prospective observational study. Clinical Microbiology and Infection: The Official Publication of the European Society of Clinical Microbiology and Infectious Diseases, 18(5), E110-118. https://doi.org/10.1111/j.1469-0691.2012.03789.x.
Mirand, A., le Sage, F. V., Pereira, B., Cohen, R., Levy, C., Archimbaud, C., et al. (2016). Ambulatory pediatric surveillance of hand, foot and mouth disease as signal of an outbreak of Coxsackievirus A6 infections, France, 2014–2015. Emerging Infectious Diseases, 22(11), 1884–1893. https://doi.org/10.3201/eid2211.160590.
Moazeni, M., Nikaeen, M., Hadi, M., Moghim, S., Mouhebat, L., Hatamzadeh, M., et al. (2017). Estimation of health risks caused by exposure to enteroviruses from agricultural application of wastewater effluents. Water Research, 125, 104–113. https://doi.org/10.1016/j.watres.2017.08.028.
Molet, L., Saloum, K., Marque-Juillet, S., Garbarg-Chenon, A., Henquell, C., Schuffenecker, I., et al. (2016). Enterovirus infections in hospitals of Ile de France region over 2013. Journal of Clinical Virology: The Official Publication of the Pan American Society for Clinical Virology, 74, 37–42. https://doi.org/10.1016/j.jcv.2015.11.024.
Munoz, I., Tomas, N., Mas, J., Garcia-Reyes, J. F., Molina-Diaz, A., & Fernandez-Alba, A. R. (2010). Potential chemical and microbiological risks on human health from urban wastewater reuse in agriculture. Case study of wastewater effluents in Spain. Journal of Environmental Science and Health. Part. B, Pesticides, Food Contaminants, and Agricultural Wastes, 45(4), 300–309. https://doi.org/10.1080/03601231003704648.
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, 44(8), 2698–2704. https://doi.org/10.1128/JCM.00542-06.
Pellegrinelli, L., Bubba, L., Primache, V., Pariani, E., Battistone, A., Delogu, R., et al. (2017). Surveillance of poliomyelitis in Northern Italy: Results of acute flaccid paralysis surveillance and environmental surveillance, 2012–2015. Human Vaccines & Immunotherapeutics, 13(2), 332–338. https://doi.org/10.1080/21645515.2017.1264726.
Pennino, F., Nardone, A., Montuori, P., Aurino, S., Torre, I., Battistone, A., et al. (2018). Large-scale survey of human enteroviruses in wastewater treatment plants of a metropolitan area of Southern Italy. Food and Environmental Virology, 10(2), 187–192. https://doi.org/10.1007/s12560-017-9331-3.
Petrinca, A. R., Donia, D., Pierangeli, A., Gabrieli, R., Degener, A. M., Bonanni, E., et al. (2009). Presence and environmental circulation of enteric viruses in three different wastewater treatment plants. Journal of Applied Microbiology, 106(5), 1608–1617. https://doi.org/10.1111/j.1365-2672.2008.04128.x.
Pianetti, A., Baffone, W., Citterio, B., Casaroli, A., Bruscolini, F., & Salvaggio, L. (2000). Presence of enteroviruses and reoviruses in the waters of the Italian coast of the Adriatic Sea. Epidemiology and Infection, 125(2), 455–462.
Prim, N., Rodriguez, G., Margall, N., Del Cuerpo, M., Trallero, G., & Rabella, N. (2013). Combining cell lines to optimize isolation of human enterovirus from clinical specimens: Report of 25 years of experience. Journal of Medical Virology, 85(1), 116–120. https://doi.org/10.1002/jmv.23426.
Rajtar, B., Majek, M., Polanski, L., & Polz-Dacewicz, M. (2008). Enteroviruses in water environment–a potential threat to public health. Annals of Agricultural and Environmental Medicine: AAEM, 15(2), 199–203.
Ramelli, G. P., Simonetti, G. D., Gorgievski-Hrisoho, M., Aebi, C., & Bianchetti, M. G. (2004). Outbreak of coxsackie B5 virus meningitis in a Scout camp. The Pediatric Infectious Disease Journal, 23(1), 86–87. https://doi.org/10.1097/01.inf.0000107294.96717.d5.
Richter, J., Koptides, D., Tryfonos, C., & Christodoulou, C. (2006). Molecular typing of enteroviruses associated with viral meningitis in Cyprus, 2000–2002. Journal of Medical Microbiology, 55(Pt 8), 1035–1041. https://doi.org/10.1099/jmm.0.46447-0.
Richter, J., Tryfonos, C., & Christodoulou, C. (2011). Circulation of enteroviruses in Cyprus assessed by molecular analysis of clinical specimens and sewage isolates. Journal of Applied Microbiology, 111(2), 491–498. https://doi.org/10.1111/j.1365-2672.2011.05061.x.
Roivainen, M., Blomqvist, S., Al-Hello, H., Paananen, A., Delpeyroux, F., Kuusi, M., et al. (2010). Highly divergent neurovirulent vaccine-derived polioviruses of all three serotypes are recurrently detected in Finnish sewage. Euro Surveillance: Bulletin Europeen sur les Maladies Transmissibles = European Communicable Disease Bulletin, 15(19), pii/19566.
Rudolph, H., Prieto Dernbach, R., Walka, M., Rey-Hinterkopf, P., Melichar, V., Muschiol, E., et al. (2017). Comparison of clinical and laboratory characteristics during two major paediatric meningitis outbreaks of echovirus 30 and other non-polio enteroviruses in Germany in 2008 and 2013. European Journal of Clinical Microbiology & Infectious Diseases: Official Publication of the European Society of Clinical Microbiology, 1–10, https://doi.org/10.1007/s10096-017-2979-7.
Ruggeri, F. M., Bonomo, P., Ianiro, G., Battistone, A., Delogu, R., Germinario, C., et al. (2015). Rotavirus genotypes in sewage treatment plants and in children hospitalized with acute diarrhea in Italy in 2010 and 2011. Applied and Environmental Microbiology, 81(1), 241–249. https://doi.org/10.1128/AEM.02695-14.
Ruggeri, F. M., & Fiore, L. (2012). Vaccine preventable viral diseases and risks associated with waterborne transmission. Annali dell’Istituto superiore di sanita, 48(4), 460–472. https://doi.org/10.4415/ANN_12_04_12. doi.
Scarcella, C., Carasi, S., Cadoria, F., Macchi, L., Pavan, A., Salamana, M., et al. (2009). An outbreak of viral gastroenteritis linked to municipal water supply, Lombardy, Italy, June 2009. Euro Surveillance: Bulletin Europeen sur les Maladies Transmissibles = European Communicable Disease Bulletin, 14(29).
Simmons, F. J., & Xagoraraki, I. (2011). Release of infectious human enteric viruses by full-scale wastewater utilities. Water Research, 45(12), 3590–3598. https://doi.org/10.1016/j.watres.2011.04.001.
Steele, M., & Odumeru, J. (2004). Irrigation water as source of foodborne pathogens on fruit and vegetables. Journal of Food Protection, 67(12), 2839–2849.
Tapparel, C., Siegrist, F., Petty, T. J., & Kaiser, L. (2013). Picornavirus and enterovirus diversity with associated human diseases. Infection, Genetics and Evolution, 14, 282–293. https://doi.org/10.1016/j.meegid.2012.10.016.
Tsao, K. C., Huang, C. G., Huang, Y. L., Chen, F. C., Huang, P. N., Huang, Y. C., et al. (2010). Epidemiologic features and virus isolation of enteroviruses in Northern Taiwan during 2000–2008. Journal of Virological Methods, 165(2), 330–332. https://doi.org/10.1016/j.jviromet.2010.03.001.
van der Sanden, S. M., Koopmans, M. P., & van der Avoort, H. G. (2013). Detection of human enteroviruses and parechoviruses as part of the national enterovirus surveillance in the Netherlands, 1996–2011. European Journal of Clinical Microbiology & Infectious Diseases: Official Publication of the European Society of Clinical Microbiology, 32(12), 1525–1531. https://doi.org/10.1007/s10096-013-1906-9.
Viau, E., Bibby, K., Paez-Rubio, T., & Peccia, J. (2011). Toward a consensus view on the infectious risks associated with land application of sewage sludge. Environmental Science & Technology, 45(13), 5459–5469. https://doi.org/10.1021/es200566f.
Vieira, C. B., Mendes, A. C., Guimaraes, F. R., Fumian, T. M., Leite, J. P., Gaspar, A. M., et al. (2012). Detection of enteric viruses in recreational waters of an urban lagoon in the city of Rio de Janeiro, Brazil. Memorias do Instituto Oswaldo Cruz, 107(6), 778–784.
Werber, D., Lausevic, D., Mugosa, B., Vratnica, Z., Ivanovic-Nikolic, L., Zizic, L., et al. (2009). Massive outbreak of viral gastroenteritis associated with consumption of municipal drinking water in a European capital city. Epidemiology and Infection, 137(12), 1713–1720. https://doi.org/10.1017/S095026880999015X.
WHO (2002). Certification of poliomyelitis eradication: European Region declared ‘polio-free’. fifteenth meeting of European regional. Certification Commission. Copenhagen, 19–21 June 2002.
WHO (2003). Guidelines for environmental surveillance of poliovirus circulation. WHO/V&B/03.03.WHO, Geneva, Switzerland.
WHO (2004). Polio Laboratory Manual. WHO/IVB/04.10. Geneva, Switzerland: World Health Organization. Retrieved November, from http://polioeradication.org/wp-content/uploads/2017/05/Polio_Lab_Manual04.pdf.
WHO (2014). Supplement to the WHO Polio Laboratory Manual. Retrieved January, from http://polioeradication.org/wp-content/uploads/2017/05/NewAlgorithmForPoliovirusIsolationSupplement1.pdf.
Wikswo, M. E., Khetsuriani, N., Fowlkes, A. L., Zheng, X., Penaranda, S., Verma, N., et al. (2009). Increased activity of Coxsackievirus B1 strains associated with severe disease among young infants in the United States, 2007–2008. Clinical Infectious Diseases: An Official Publication of the Infectious Diseases Society of America, 49(5), e44-51. https://doi.org/10.1086/605090.
Zurbriggen, S., Tobler, K., Abril, C., Diedrich, S., Ackermann, M., Pallansch, M. A., et al. (2008). Isolation of sabin-like polioviruses from wastewater in a country using inactivated polio vaccine. Applied and Environmental Microbiology, 74(18), 5608–5614. https://doi.org/10.1128/AEM.02764-07.
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The authors wish to thank the workers of the wastewater-treatment plants in charge of collecting samples for the environmental surveillance.
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This work was partially supported by grants from the Italian Ministry of Health, CCM, “AFP surveillance in Italy. Research of Poliovirus and other enteroviruses in immunodeficient patients and in the environment”.
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Delogu, R., Battistone, A., Buttinelli, G. et al. Poliovirus and Other Enteroviruses from Environmental Surveillance in Italy, 2009–2015. Food Environ Virol 10, 333–342 (2018). https://doi.org/10.1007/s12560-018-9350-8
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DOI: https://doi.org/10.1007/s12560-018-9350-8