Skip to main content

Advertisement

Log in

Norovirus and Other Human Enteric Viruses in Moroccan Shellfish

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

Abstract

The aim of this study was to evaluate the presence of human enteric viruses in shellfish collected along the Mediterranean Sea and Atlantic Coast of Morocco. A total of 77 samples were collected from areas potentially contaminated by human sewage. Noroviruses were detected in 30 % of samples, with an equal representation of GI and GII strains, but were much more frequently found in cockles or clams than in oysters. The method used, including extraction efficiency controls, allowed the quantification of virus concentration. As in previous reports, results showed levels of contamination between 100 and 1,000 copies/g of digestive tissues. Sapoviruses were detected in 13 % of samples mainly in oyster and clam samples. Hepatitis A virus was detected in two samples, with concentrations around 100 RNA copies/g of digestive tissues. Only two samples were contaminated with enterovirus and none with norovirus GIV or Aichi virus. This study highlights the interest of studying shellfish samples from different countries and different production areas. A better knowledge of shellfish contamination helps us to understand virus levels in shellfish and to improve shellfish safety, thus protecting consumers.

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

Similar content being viewed by others

References

  • Alfano-Sobsey, E., Sweat, D., Hall, A., Breedlove, F., Rodriguez, R., Greene, S., et al. (2012). Norovirus outbreak associated with undercooked oysters and secondary household transmission. Epidemiology and Infection, 140, 276–282.

    Article  PubMed  CAS  Google Scholar 

  • Atmar, R. L. (2010). Noroviruses: State of the art. Food and Environmental Virology, 2, 117–126.

    Article  PubMed  Google Scholar 

  • Atmar, R. L., Neill, F. H., Romalde, J. L., Le Guyader, F., Woodley, C. M., Metcalf, T. G., et al. (1995). Detection of Norwalk virus and hepatitis A virus in shellfish tissues with the PCR. Applied and Environmental Microbiology, 61, 3014–3018.

    PubMed  CAS  Google Scholar 

  • Bosch, A., Lucena, F., Girones, R., & Jofre, J. (1988). Occurence of enteroviruses in marine sediment along the coast of Barcelona, Spain. Canadian Journal of Microbiology, 34, 921–924.

    Article  PubMed  CAS  Google Scholar 

  • Boxman, I. L. A. (2010). Human enteric viruses occurence in shellfish from European markets. Food and Environmental Virology, 2, 156–168.

    Article  Google Scholar 

  • dePaola, A., Jones, J. L., Woods, J., Burkhardt, W., I. I. I., Calci, K. C., Krantz, J. A., et al. (2010). Bacterial and viral pathogens in live oysters: 2007 United States market survey. Applied and Environmental Microbiology, 76, 2754–2768.

    Article  PubMed  CAS  Google Scholar 

  • EFSA Panel on Biological Hazards (BIOHAZ). (2012). Norovirus (NoV) in oysters: Methods, limits and control options. EFSA Journal, 10, 2500.

    Google Scholar 

  • Elamri, D. E., Aouni, M., Parnaudeau, S., & Le Guyader, F. S. (2006). Detection of human enteric viruses in shellfish collected in Tunisia. Letters in Applied Microbiology, 43, 399–404.

    Article  PubMed  CAS  Google Scholar 

  • Gabrieli, R., Macaluso, A., Lanni, L., Saccares, S., di Giamberardino, F., Cencioni, B., et al. (2007). Enteric viruses in molluscan shellfish. New Microbiologica, 30, 471–475.

    PubMed  Google Scholar 

  • Gentry, J., Vinje, J., Guadagnoli, D., & Lipp, E. K. (2009). Norovirus distribution within an estuarine environment. Applied and Environmental Microbiology, 75, 5474–5480.

    Article  PubMed  CAS  Google Scholar 

  • Grangere, K., Menesguen, A., Lefebvre, S., Bacher, C., & Pouvreau, S. (2009). Modelling the influence of environmental factors on the physiological status of the Pacific oysters Crassostrea gigas in an estuarine embayment; the Baie des Veys (France). Journal of Sea Research, 62, 147–158.

    Article  Google Scholar 

  • Greening, G. E., & McCoubrey, D.-J. (2010). Enteric viruses and management of shellfish production in New Zealand. Food and Environmental Virology, 2, 167–175.

    Article  Google Scholar 

  • Karamoto, Y., Ibenyassine, K., Aitmhand, R., Idaomar, M., & Enmaji, M. M. (2005). Adenovirus detection in shellfish and urban sewage in Morocco (Casablanca region) by the polymerase chain reaction. Journal of Virological Methods, 126, 135–137.

    Article  Google Scholar 

  • Le Guyader, F. S., Atmar, R. L., & Le Pendu, J. (2012). Transmission of viruses through shellfish: When specific ligands come into play. Current Opinion in Virology, 2, 103–110.

    Article  PubMed  Google Scholar 

  • Le Guyader, F. S., Krol, J., Ambert-Balay, K., Ruvoen-Clouet, N., Desaubliaux, B., Parnaudeau, S., et al. (2010). Comprehensive analysis of a norovirus-associated gastroenteritis outbreak, from the environment to the consumer. Journal of Clinical Microbiology, 48, 915–920.

    Article  PubMed  Google Scholar 

  • Le Guyader, F. S., Le Saux, J.-C., Ambert-Balay, K., Krol, J., Serais, O., Parnaudeau, S., et al. (2008). Aichi virus, norovirus, astrovirus, enterovirus and rotavirus involved in clinical cases from a French oyster-related gastroenteritis outbreak. Journal of Clinical Microbiology, 46, 4011–4017.

    Article  PubMed  Google Scholar 

  • Le Guyader, F. S., Parnaudeau, S., Schaeffer, J., Bosch, A., Loisy, F., Pommepuy, M., et al. (2009). Detection and quantification of noroviruses in shellfish. Applied and Environmental Microbiology, 74, 618–624.

    Article  Google Scholar 

  • Lopman, B., Gastanaduy, P., Park, G. W., Hall, A. J., Parashar, U. D., & Vinje, J. (2012). Environmental transmission of norovirus gastroenteritis. Current Opinion in Virology, 2, 96–102.

    Article  PubMed  Google Scholar 

  • Lowther, J. A., Gustar, N. E., Hartnell, R. E., & Lees, D. N. (2012). Comparison of norovirus RNA levels in outbreak-related oysters with background environmental levels. Journal of Food Protection, 75, 389–393.

    Article  PubMed  CAS  Google Scholar 

  • Maalouf, H., Pommepuy, M., & Le Guyader, F. S. (2010a). Environmental conditions leading to shellfish contamination and related outbreaks. Food and Environmental Virology, 2, 136–145.

    Article  Google Scholar 

  • Maalouf, H., Schaeffer, J., Parnaudeau, S., Le Pendu, J., Atmar, R. L., Crawford, S. E., et al. (2011). Strain-dependent norovirus bioaccumulation in oysters. Applied and Environmental Microbiology, 77, 3189–3196.

    Article  PubMed  CAS  Google Scholar 

  • Maalouf, H., Zakhour, M., Le Pendu, J., Le Saux, J.-C., Atmar, R. L., & Le Guyader, F. S. (2010b). Norovirus genogroup I and II ligands in oysters: tissue distribution and seasonal variations. Applied and Environmental Microbiology, 76, 5621–5630.

    Article  PubMed  CAS  Google Scholar 

  • Metcalf, T. G. (1982). Viruses in shellfish growing waters. Environmental International, 7, 21–27.

    Article  Google Scholar 

  • Miura, T., Masago, Y., Sano, D., & Omura, T. (2011). Development of an effective method for recovery of viral genomic RNA from environmental silty sediment for quantitative molecular detection. Applied and Environmental Microbiology, 77, 3975–3981.

    Article  PubMed  CAS  Google Scholar 

  • Myrmel, M., Berg, E. M. M., Rimstad, E., & Grinde, B. (2004). Detection of enteric viruses in shellfish from the Norwegian coast. Applied and Environmental Microbiology, 70, 2678–2684.

    Article  PubMed  CAS  Google Scholar 

  • Nakagawa-Okamoto, R., Arita-Nishida, T., Toda, S., Kato, H., Iwata, H., Akiyama, M., et al. (2009). Detection of multiple sapovirus genotypes and genogroups in oyster-associated outbreaks. Japanese Journal of Infectious Disease, 62, 63–66.

    CAS  Google Scholar 

  • Nishida, T., Nishio, O., Kato, M., Chuma, T., Kato, H., Iwata, H., et al. (2007). Genotyping and quantitation of norovirus in oysters from two distinct sea areas in Japan. Microbiology and Immunology, 51, 177–184.

    PubMed  CAS  Google Scholar 

  • Oka, T., Katayama, K., Hansman, G. S., Kageyama, T., Ogawa, S., Wu, F.-T., et al. (2006). Detection of human sapovirus by real-time reverse transcription polymerase chain reaction. Journal of Medical Virology, 78, 1347–1353.

    Article  PubMed  CAS  Google Scholar 

  • Pepe, T., Ventrone, I., Suffredini, E., Ceruso, M., Croci, L., Anastasio, A., et al. (2012). Norovirus monitoring in bivalve molluscs harvested and commercialized in Southern Italy. Journal of Food Protection, 75, 976–981.

    Article  PubMed  CAS  Google Scholar 

  • Phillips, G., Tam, C. C., Rodrigues, L. C., & Lopman, B. (2010). Risk factor for symptomatic and asymptomatic norovirus infection in the community. Epidemiology and Infection, 10, 1–11.

    Google Scholar 

  • Pinto, R. M., Costafreda, M. I., & Bosch, A. (2009). Risk assessment in shellfish-borne outbreaks of hepatitis A. Applied and Environmental Microbiology, 75, 7350–7355.

    Article  PubMed  CAS  Google Scholar 

  • Rao, V. C., Seidel, K. M., Goyal, S. M., Metcalf, T. G., & Melnick, J. L. (1984). Isolation of enteroviruses from water, suspended solids and sediments from Galveston Bay: Survival of poliovirus and rotavirus adsorbed to sediments. Applied and Environmental Microbiology, 48, 404–409.

    PubMed  CAS  Google Scholar 

  • Rohayem, J. (2009). Norovirus seasonality and the potential impact of climate change. Clinical and Microbiology Infection, 15, 524–527.

    Article  CAS  Google Scholar 

  • Simmons, G., Garbutt, C., Hewitt, J., & Greening, G. (2007). A New Zealand outbreak of norovirus gastroenteritis linked to the consumption of imported raw Korean oysters. New Zealand Medical Journal, 120, 1–7.

    Google Scholar 

  • Suffredini, E. C. C., Arcangeli, G., Fasolato, L., Manfrin, A., Rosseti, E., Biazzi, E., et al. (2008). Occurence of enteric viruses in shellfish and relation to climatic-environmental factors. Letters in Applied Microbiology, 47, 467–474.

    Article  PubMed  CAS  Google Scholar 

  • Tan, M., & Jiang, X. (2011). Norovirus–host interaction: multi-selections by human histo-blood group antigens. Trends in Microbiology, 19, 382–388.

    Article  PubMed  CAS  Google Scholar 

  • Terio, V., Martella, V., Moschidou, P., Di Pinto, P., Tantillo, G., & Buanavoglia, C. (2010). Norovirus in retail shellfish. Food Microbiology, 27, 29–32.

    Article  PubMed  CAS  Google Scholar 

  • Tian, P., Bates, A. H., Jensen, H. M., & Mandrell, R. E. (2006). Norovirus binds to blood group A-like antigens in oyster gastrointestinal cells. Letters in Applied Microbiology, 43, 645–651.

    Article  PubMed  CAS  Google Scholar 

  • Tian, P., Engelbrektson, A. L., Jiang, X., Zhong, W., & Mandrell, R. E. (2007). Norovirus recognizes histo-blood group antigens on gastrointestinal cells of clams, mussels, and oysters: a possible mechanism of bioaccumulation. Journal of Food Protection, 70, 2140–2147.

    PubMed  Google Scholar 

  • Trujilo, A. A., McCaustland, K. A., Zheng, D.-P., Hadley, L. A., Vaughn, G., Adams, S. M., et al. (2006). Use of Taq-Man real-time reverse transcription PCR for rapid detection, quantification and typing of norovirus. Journal of Clinical Microbiology, 44, 1405–1412.

    Article  Google Scholar 

  • Ueki, Y., Shoji, M., Okimura, Y., Miyota, Y., Masago, Y., Oka, T., et al. (2010). Detection of sapovirus in oysters. Microbiology and Immunology, 54, 483–486.

    Article  PubMed  CAS  Google Scholar 

  • Vilarino, M. L., Le Guyader, F. S., Polo, D., Schaeffer, J., Krol, J., & Romalde, J. L. (2009). Assessment of human enteric viruses in cultured and wild bivalve molluscs. International Microbiology, 12, 145–151.

    PubMed  CAS  Google Scholar 

  • Webby, R. J., Carville, K. S., Kirk, M. D., Greening, G., Ratcliff, R. M., Crerar, S. K., et al. (2007). Internationally distributed frozen oyster meat causing multiple outbreaks of norovirus infection in Australia. Clinical and Infectious Disease, 44, 1026–1031.

    Article  CAS  Google Scholar 

  • Wobus, C., & Nguyen, T. H. (2012). Viruses are everywhere—what do we do? Current Opinion in Virology, 2, 60–62.

    Article  PubMed  Google Scholar 

  • Woods, J. W., & Burkhardt, W., I. I. I. (2010). Occurence of norovirus and hepatitis A virus in US oysters. Food and Environmental Virology, 2, 176–182.

    Article  Google Scholar 

  • Yamashita, T., Sugiyama, M., Tsuzuki, H., Sakae, K., Suzuki, Y., & Miyazaki, Y. (2000). Application of a reverse transcription-PCR for identification and differentiation of Aichi virus, a new member of the picornavirus family associated with gastroenteritis in humans. Journal of Clinical Microbiology, 38, 2955–2961.

    PubMed  CAS  Google Scholar 

  • Zakhour, M., Maalouf, H., diBartolo, I., Haugarreau, L., Le Guyader, F. S., Ruvoen-Clouet, N., et al. (2010). Bovine norovirus ligand, environmental contamination and potential cross-species transmission via oyster. Applied and Environmental Microbiology, 76, 6404–6411.

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This work was funded by IFREMER (France) and DGAl (French Ministry of Agriculture and Food) and Pasteur Institute International network through a graduate research fellowship for Laila Benabbes. We thank Jacques Le Pendu (INSERM UMR-U892, CNRS UMR 6299, Université de Nantes) for critical review of the manuscript and helpful discussion, and Helen McCombie-Boudry for English correction.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Françoise S. Le Guyader.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Benabbes, L., Ollivier, J., Schaeffer, J. et al. Norovirus and Other Human Enteric Viruses in Moroccan Shellfish. Food Environ Virol 5, 35–40 (2013). https://doi.org/10.1007/s12560-012-9095-8

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12560-012-9095-8

Keywords

Navigation