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Detection of Hepatitis E Virus in Sewage After an Outbreak on a French Island

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Abstract

A hepatitis E outbreak, which occurred on a small isolated island, provided an opportunity to evaluate the association between the number of hepatitis E cases in the community and the concentration of virus detected in sewage. Samples were collected from the different sewage treatment plants from the island and analyzed for the presence of hepatitis E (HEV) virus using real-time RT-PCR. We demonstrated that if 1–4 % of inhabitants connected to a WWTP were infected with HEV, raw sewage contained HEV at detectable levels. The finding that such a small number of infected people can contaminate municipal sewage works raises the potential of the further distribution of the virus. Indeed, investigating the routes of transmission of HEV, including the potential for sewage effluent to contain infectious HEV, may help us to better understand the epidemiology of this pathogen, which is considered to be an emerging concern in Europe.

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References

  • Abranavel, F., Lhomme, S., Dubois, M., Peron, J.-M., Alric, L., Rostaing, L., et al. (2013). Hepatitis E virus. Medecine et Maladies Infectieuses, 43, 263–270.

    Article  Google Scholar 

  • Abranavel, F., Sandres-Saune, K., Lhomme, S., Dubois, M., Mansuy, J.-M., & Izopet, J. (2012). Genotype 3 diversity and quantification of hepatitis E virus RNA. J Clin Microbiol, 50, 897–902.

    Article  Google Scholar 

  • Bibby, K., & Peccia, J. (2013). Identification of viral pathogen diversity in sewage sludge by metagenome analysis. Environ Sci Technol, 47, 1945–1951.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Boxman, I., Verhoef, L., Vennema, H., Ngui, S., Friesema, I. H., Whiteside, C., et al. (2016). International linkage of two food-borne hepatitis A clusters through traceback of mussels, the Netherlands, 2012. Euro Surveill. doi:10.2807/1560-7917.ES.2016.21.3.30113.

    PubMed  Google Scholar 

  • Cooper, K., Huang, F. F., Batista, L., Rayo, C. D., Beznilla, J. C., Toth, T. E., & Meng, X. J. (2005). Identification of genotype 3 hepatitis E virus (HEV) in serum and fecal samples from pigs in Thailand and Mexico, where genotype 1 and 2 HEV strains are prevalent in the respective human populations. J Clin Microbiol, 43, 1684–1688.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • EFSA. (2011). Scientifc opinion on an update on the present knowledge on the occurence and control of foodborne viruses. EFSA J, 9, 1–96.

    Google Scholar 

  • Gall, A., Marinas, B. J., Lu, Y., & Shisler, J. L. (2015). Waterborne viruses: a barrier to safe drinking water. PLoS Pathog, 11, e1004867.

    Article  PubMed  PubMed Central  Google Scholar 

  • Gibson, K. E. (2014). Viral pathogen in water: occurence, public health impact, and available control strategies. Curr Opin Virol, 4, 50–57.

    Article  PubMed  Google Scholar 

  • Grodzki, M., Schaeffer, J., Piquet, J.-C., Le Saux, J.-C., Chevé, J., Ollivier, J., et al. (2014). Bioaccumulation efficiency, tissue distribution, and environmental occurrence of hepatitis E virus in bivalve shellfish from France. Appl Environ Microbiol, 80, 4269–4276.

    Article  PubMed  PubMed Central  Google Scholar 

  • Guillois, Y., Abranavel, F., Miura, T., Pavio, N., Vaillant, V., Lhomme, S., et al. (2016). High proportion of asymptomatic infections in an outbreak of hepatitis E associated with a spit-roasted piglet, France, 2013. Clin Infect Dis, 62, 351–357.

    Article  PubMed  Google Scholar 

  • Ishii, S., Kitamura, G., Segawa, T., Kobayashi, A., Miura, T., & Okabe, S. (2014). Microfluidic quantitative PCR for simulteneous quantification of multiple viruses in environmental water samples. Appl Environ Microbiol, 80, 7505–7511.

    Article  PubMed  PubMed Central  Google Scholar 

  • Jothikumar, N., Cromeans, T. L., Roberstib, B. H., Meng, X. J., & Hill, V. R. (2006). A broadly reactive one-step real-time RT-PCR assay for rapid and sensitive detection of hepatitis E virus. J Virol Methods, 131, 65–71.

    Article  CAS  PubMed  Google Scholar 

  • Kamar, N., Dalton, H. R., Abranavel, F., & Izopet, J. (2014). Hepatitis E virus infection. Clin Microbiol Rev, 27, 116–138.

    Article  PubMed  PubMed Central  Google Scholar 

  • Koopmans, M. (2013). Surveillance strategy for early detection of unusual infectious disease events. Curr Opin Virol, 3, 185–191.

    Article  PubMed  Google Scholar 

  • La Rosa, G., Pourshaban, M., Iaconelli, M., Vennarucci, V. S., & Muscillo, M. (2010). Molecular detection of hepatitis E virus in sewage samples. Appl Environ Microbiol, 76, 5870–5873.

    Article  PubMed  PubMed Central  Google Scholar 

  • Legrand-Abravanel, F., Mansuy, J.-M., Dubois, M., Kamar, N., Peron, J.-M., Rostaing, L., & Izopet, J. (2009). Hepatitis E virus genotype 3 diversity, France. Emerg Infect Dis, 15, 110–114.

    Article  PubMed  PubMed Central  Google Scholar 

  • Lhomme, S., Abranavel, F., Dubois, M., Chapuy-Regaud, S., Sandres-Saune, K., Mansuy, J.-M., et al. (2015). Temporal evolution of the distribution of hepatitis E virus genotypes in Southwestern France. Infect Genet Evol, 35, 50–55.

    Article  PubMed  Google Scholar 

  • Lodder, W. J., Buisman, A. M., Rutjes, S. A., Heijne, J. C., Teunis, P. F., & de Roda Husman, A. M. (2012). Feasability of quantitative environmental surveillance in poliovirus eradication strategies. Appl Environ Microbiol, 78, 3800–3805.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lodder, W. J., & de Roda Husman, A. M. (2005). Presence of noroviruses and other enteric viruses in sewage and surface waters in the Netherlands. Appl Environ Microbiol, 71, 1453–1461.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Masclaux, F. G., Hotz, P., Friedli, D., Savova-Bianchi, D., & Oppliger, A. (2013). High occurence of hepatitis E virus in samples from wastewater treatment plants in Switzerland and comparison with other enteric viruses. Water Res, 47, 5101–5109.

    Article  CAS  PubMed  Google Scholar 

  • Metcalf, T., Melnick, J. L., & Estes, M. K. (1995). Environmental Microbiology: from detection of virus in sewage and water by isolation to identification by molecular biology- a trip of over 50 years. Ann Rev Microbiol, 49, 461–487.

    Article  CAS  Google Scholar 

  • Myrmel, M., Lange, H., & Rimstad, E. (2015). A 1-year quantitiative survey of noro-, adeno-, human boca-, and hepatitis E viruses in raw and secondarily treated sewage from two plants in Norway. Food Environ Virol, 7, 213–223.

    Article  CAS  PubMed  Google Scholar 

  • Newton, R., McLellan, S. L., Dila, D. K., Vineis, J. H., Morrison, H. G., Eren, A. M., & Sogin, M. L. (2015). Sewage reflects the microbiomes of human populations. mBio, 6, e02574.

    Article  PubMed  PubMed Central  Google Scholar 

  • Pavio, N., Meng, X.-J., & Doceul, V. (2015). Zoonotic origin of hepatitis E. Curr Opin Virol, 10, 34–41.

    Article  PubMed  Google Scholar 

  • Ruggeri, F., 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. Appl Environ Microbiol, 81, 241–249.

    Article  PubMed  Google Scholar 

  • Sano, D. U., Perez-Sautu, U., Guix, S., Pinto, R. M., Miura, T., Okabe, S., & Bosch, A. (2011). Quantification and genotyping of human sapoviruses in the Llobregat river catchment, Spain. Appl Environ Microbiol, 77, 111–114.

    Article  Google Scholar 

  • Sima, L. C., Schaeffer, J., Le Saux, J.-C., Parnaudeau, S., Elimelech, M., & Le Guyader, F. S. (2011). Calicivirus removal in a membrane bioreactor wastewater treatment plant. Appl Environ Microbiol, 77, 5170–5177.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Smith, D., Paddy, J. O., & Simmonds, P. (2016). The use of human sewage screening for community surveillance of hepatitis E virus in the UK. J Med Virol, 88(5), 915–918.

    Article  PubMed  Google Scholar 

  • Takahashi, M., Tanaka, T., Azuma, M., Kusano, E., Aikawa, T., Shibayama, T., et al. (2007). Prolonged fecal shedding of hepatitis E virus (HEV) during sporadic acute hepatitis E: evaluation of infectivity of HEV in fecal specimens in a cell culture system. J Clin Microbiol, 45, 3671–3679.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Uyttendaele, M., Jaykus, L.-A., Amoah, P., Chiodini, A., Cunliffe, D., Jacxsens, L., et al. (2015). Microbial hazards in irrigation water: standards, norms, and testing to manage use of water in fresh produce primary production. Compr Rev Food Sci Food Saf, 14, 336–356.

    Article  Google Scholar 

  • van der Poel, W. H. M. (2014). Food and environmental routes of hepatitis E virus transmission. Curr Opin Virol, 4, 91–96.

    Article  PubMed  Google Scholar 

  • Yugo, D. M., & Meng, X.-J. (2013). Hepatitis E virus: foodborne, waterborne and zoonotic transmission. Int J Environ Res Public Health, 10, 4507–4533.

    Article  PubMed  PubMed Central  Google Scholar 

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Acknowledgments

This study was supported by the Japan Society for the Promotion of Science (JSPS) through JSPS Research Fellowships for Young Scientists (23-4434) (TM), by Grant 2010 CESA 01003 ‘Hevecodyn’ from the Agence Nationale pour la recherche (ANR), and by the EU-H2020 Grant N°643476 Compare. We acknowledge the help of the SAUR technicians for sampling. We are grateful to Catherine McLeod (Seafood Safety Assessment) for a critical review of the manuscript.

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Author notes

  1. Takayuki Miura

    Present address: New Industry Creation Hatchery Center (NICHe), Tohoku University, 6-6-04 Aoba, Aramaki, Aoba-Ku, Sendai, 980-8579, Japan

Authors and Affiliations

  1. Laboratoire de Microbiologie, LSEM-SG2M, IFREMER, BP 21105, 44311, Nantes Cedex 03, France

    Takayuki Miura, Jean-Claude Le Saux & Françoise S. Le Guyader

  2. National Reference Center for HEV, Centre Hospitalier Universitaire, Toulouse, France

    Sébastien Lhomme, Jacques Izopet & Florence Abranavel

  3. SAUR, Direction générale Ouest, Vannes, France

    Philippe Le Mehaute

  4. Regional Epidemiology Unit for the Brittany region, Institut de veille sanitaire, Rennes, France

    Yvonnick Guillois

  5. Department of Infectious Diseases, Institut de Veille Sanitaire, Saint-Maurice, France

    Elizabeth Couturier

Authors
  1. Takayuki Miura
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  2. Sébastien Lhomme
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  3. Jean-Claude Le Saux
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  9. Françoise S. Le Guyader
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Correspondence to Françoise S. Le Guyader.

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Miura, T., Lhomme, S., Le Saux, JC. et al. Detection of Hepatitis E Virus in Sewage After an Outbreak on a French Island. Food Environ Virol 8, 194–199 (2016). https://doi.org/10.1007/s12560-016-9241-9

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  • DOI: https://doi.org/10.1007/s12560-016-9241-9

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