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Norovirus Detection at Oualidia Lagoon, a Moroccan Shellfish Harvesting Area, by Reverse Transcription PCR Analysis

  • N. El MoqriEmail author
  • F. El Mellouli
  • N. Hassou
  • M. Benhafid
  • N. Abouchoaib
  • S. Etahiri
Original Paper
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Abstract

Norovirus (NoV) is the leading cause of acute viral gastroenteritis outbreaks in the world. These outbreaks are frequently associated with bivalve shellfish consumption, particularly because these products are often eaten raw or only slightly cooked. In Morocco, regulations concerning the acceptable levels of enteric bacteria indicator organisms in these products have been put in place. However, these regulations do not take into account the risk of viral contamination, and many gastroenteritis outbreaks have been linked to the ingestion of bivalve shellfish from areas that comply with the current food safety criteria. The aim of this study was to investigate NoV presence in shellfish samples (n = 104) collected at four sites owcff Oualidia lagoon (Moroccan Atlantic coast) from November 2015 to February 2017. Samples were analysed using real-time RT-PCR in accordance with the ISO 15216-2 method. NoVs of the genogroup II were detected in 7% of samples that were all collected during the winter months. Moreover, 71% of NoV-positive samples were harvested at sites upstream of the lagoon. These results highlight the need of regularly monitoring viral contamination in bivalve shellfish to limit the risk of viral gastroenteritis outbreaks.

Keywords

Norovirus Detection Shellfish RT-PCR Oualidia lagoon 

Notes

References

  1. Ahmed, S. M., Hall, A. J., Robinson, A. E., Verhoef, L., Premkumar, P., Parashar, U. D., et al. (2014). Global prevalence of norovirus in cases of gastroenteritis: A systematic review and meta-analysis. The Lancet Infectious Diseases, 14, 725–730.CrossRefGoogle Scholar
  2. Ahmed, S. M., Lopman, B. A., & Levy, K. A. (2013). Systematic review and meta-analysis of the global seasonality of norovirus. PLoS ONE.  https://doi.org/10.1371/journal.0075922.Google Scholar
  3. Ang, L. H. (1998). An outbreak of viral gastroenteritis associated with eating raw oysters. Communicable Disease and Public Health, 1(1), 38–40.Google Scholar
  4. Atmar, R. L. (2010). Noroviruses: State of the art. Food and Environmental Virology, 2(3), 117–126.CrossRefGoogle Scholar
  5. Atmar, R. L., & Estes, M. K. (2006). The epidemiologic and clinical importance of norovirus infection. Gastroenterology Clinics of North America, 35(2), 275–290.CrossRefGoogle Scholar
  6. Baert, L., Mattison, K., Loisy-Hamon, F., Harlow, J., Martyres, A., Lebeau, B., et al. (2011). Review: Norovirus prevalence in Belgian, Canadian and French fresh produce: A threat to human health. International Journal of Food Microbiology, 151(3), 261–269.CrossRefGoogle Scholar
  7. Bartsch, S. M., Lopman, B. A., Ozawa, S., Aron, J. H., & Bruce, Y. L. (2016). Global economic burden of norovirus gastroenteritis. PLoS ONE, 11(4), e0151219.  https://doi.org/10.1371/journal.pone.0151219.CrossRefGoogle Scholar
  8. Beaubrun, P. C. (1976). Les huîtres au Maroc et l’ostréiculture dans la lagune de Oualidia. Bulletin de l’institut des Pêches Maritimes, 22, 13–143.Google Scholar
  9. Bellou, M., Kokkinos, P., & Vantarakis, A. (2013). Shellfish-borne viral outbreaks: A systematic review. Food and Environmental Virology, 5(1), 13–23.CrossRefGoogle Scholar
  10. Benabbes, L., Olivier, J., Schaeffer, J., Parnaudeau, S., Rhaissi, H., Nourlil, J., et al. (2013). Norovirus and other human enteric viruses in Moroccan shellfish. Food and Environmental Virology, 5(1), 35–40.CrossRefGoogle Scholar
  11. Brake, F., Ross, T., Holds, G., Andreas Kiermeier, A., & McLeod, C. (2014). A survey of Australian oysters for the presence of human noroviruses. Food Microbiology, 44, 264–270.CrossRefGoogle Scholar
  12. Carruesco, C., (1989). Genèse et évolution de trois lagunes du littoral atlantique depuis l’holocène: Oualidia, Moulay BouSalham (Maroc) et Arcachon (France). Thèse doctorat d’état Es science université de bordeaux.Google Scholar
  13. Chalmers, J. W., & McMillan, J. H. (1995). An outbreak of viral gastroenteritis associated with adequately prepared oysters. Epidemiology and Infection, 115(1), 163–167.CrossRefGoogle Scholar
  14. Da Silva, A. K., Le Saux, J. C., Parnaudeau, S., Pommepuy, M., Elimelech, M., & Le Guyader, F. S. (2007). Évaluation of removal of noroviruses during wastewater treatment, using real-time reverse transcription-PCR: different behavior of genogroups I and II. Applied and Environmental Microbiology, 73(24), 7891–7897.CrossRefGoogle Scholar
  15. Dowell, S. F., Graves, C., & Kirkland, K. B. (1995). A multistate outbreak of oyster associated gastroenteritis: implications for interstate tracing of contaminated shellfish. Journal of Infectious Diseases, 171, 1497–1503.CrossRefGoogle Scholar
  16. El Qazoui, M., Oumzil, H., Baassi, L., El Omari, N., Sadki, K., & Amzazi, S. (2014). Rotavirus and norovirus infections among acute gastroenteritis children in Morocco. BioMed Central Infectious Diseases, 14, 300.  https://doi.org/10.1186/1471-2334-14-300.CrossRefGoogle Scholar
  17. 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.CrossRefGoogle Scholar
  18. Formiga-Cruz, M., Tofini-Quesada, G., Bofill-Mas, S., Lees, D. N., Henshilwood, K., Allard, A. K., et al. (2002). Distribution of human virus contamination in shellfish from different growing areas in Greece, Spain, Sweden and the United Kingdom. Applied and Environmental Microbiology, 68(12), 5990–5998.CrossRefGoogle Scholar
  19. Glass, R. I., Parashar, U. D., & Estes, M. K. (2009). Norovirus gastroenteritis. The New England Journal Medicine, 361, 1776–1785.CrossRefGoogle Scholar
  20. Greening, G. E. (2006). Human and animal viruses in food (including taxonomy of enteric viruses). Food Microbiology and Food Safety, 5–42.Google Scholar
  21. Hassou, N., Maanan, M., Hennani, M., Zourarah, B., & Assobhei, O. (2014). Spatial and temporal variation of faecal pollution indicators (Escherichia coli and Faecal streptococci) and physico-chemical parameters at the Oualidia lagoon and its watershed (Morocco). International Journal of Current Microbiology and Applied Science, 3(3), 675–694.Google Scholar
  22. Hilmi, K., Orbi, A., Lakhdar, J. L., (2009). Hydrodynamisme de la lagune de Oualidia (Maroc) Durant l’été et l’automne 2005. Bulletin de l’Institut Scientifique, Section Sciences de la Terre. Rabat, N°31.Google Scholar
  23. ISO/TS 15216-2. (2013). Microbiology of food and animal feed: Horizontal method for detection of hepatitis A virus and norovirus in food using real-time RT-PCR—Part 2: Method for qualitative detection. Geneva: International Organization for Standardization.Google Scholar
  24. Kabue, J. P., Meader, E., Hunter, P. R., & Potgieter, N. (2016). Human Norovirus prevalence in Africa: A review of studies from 1990 to 2013. Tropical Medicine & International Health, 21(1), 2–17.CrossRefGoogle Scholar
  25. Kageyama, T., Kojima, S., Shinohara, M., Uchida, K., Fukushi, S., Hoshino, F. B., et al. (2003). Broadly reactive and highly sensitive assay for Norwalk-like viruses based on real-time quantitative reverse transcription-PCR. Journal of Clinical Microbiology, 41(4), 1548–1557.CrossRefGoogle Scholar
  26. Koutitansky, V. G., Ouabi, M., Ibrahimi. I. (2007). L’étude du comportement hydrosédimentaire du système lagunaire Oualidia par la modélisation mathématique. Phase 2: Modélisation hydro-sédimentaire de l’état actuel et de scenarios d’aménagement. Direction des ports et du domaine public maritime. Ministère de l’Equipement et du Transport. Royaume du Maroc. 204p+Annexes.Google Scholar
  27. Kreidieh, K., Charide, R., Dbaibo, G., & Melhem, N. D. (2017). The epidemiology of norovirus in the Middle East and North Africa (MENA) region: a systematic review. Virology Journal, 14, 220.CrossRefGoogle Scholar
  28. La Bella, G., Martella, V., Basanisi, M. G., Nobili, G., Terio, V., & La Salandra, G. (2017). Food-borne viruses in shellfish: Investigation on norovirus and HAV presence in Apulia (SE Italy). Food Environmental Virology, 9, 179–186.CrossRefGoogle Scholar
  29. Le Guyader, F. S., Haugarreau, L., Miossec, L., Dubois, E., & Pommepuy, M. (2000). Three-year study to assess human enteric viruses in shellfish. Applied and Environmental Microbiology, 66(8), 3241–3248.CrossRefGoogle Scholar
  30. Lees, D. N. (2000). Viruses and bivalve shellfish. International Journal Food of Microbiology., 59, 81–116.CrossRefGoogle Scholar
  31. Loisy, F., Atmar, R. L., Guillon, P., Cann, P., Pommepuy, M., & Le Guyader, F. S. (2005). Real-time RT-PCR for norovirus screening in shellfish. Journal of Virological Methods, 123, 1–7.CrossRefGoogle Scholar
  32. Lopman, B. A., Reacher, M. H., Van Duijnhoven, Y., Hanon, F. X., Brown, D., & Koopmans, M. (2003). Viral gastroenteritis outbreaks in Europe, 1995–2000. Emerging Infectious Diseases Jounal., 9(1), 90–96.CrossRefGoogle Scholar
  33. Lowther, J. A., Gustar, N. E., Powell, A. L., Hartnell, R. E., & Lees, D. N. (2012). Two-year systematic study to assess norovirus contamination in oysters from commercial harvesting areas in the United Kingdom. Applied and Environmental Microbiology, 78(16), 5812–5817.  https://doi.org/10.1128/AEM.01046-12.CrossRefGoogle Scholar
  34. Lowther, J. A., Henshilwood, K., & Lees, D. N. (2008). Determination of norovirus contamination in oysters from two commercial harvesting areas over an extended period, using semi-quantitative real-time reverse transcription PCR. Journal of Food Protection, 71(7), 1427–1433.CrossRefGoogle Scholar
  35. 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.CrossRefGoogle Scholar
  36. Maalouf, H., Zakhour, M., Le Pendu, J., Le Saux, J. C., Atmar, R. L., & Le Guyader, F. S. (2010). Distribution in tissue and seasonal variation of norovirus genogroup I and II ligands in oysters. Applied an Environmental Microbiology., 76(16), 5621–5630.CrossRefGoogle Scholar
  37. Makaoui, A., Idrissi, M., Agouzouk, A., Larissi, J., Baibai, T., El Ouehabi, Z., et al. (2018). Etat océanographique de la lagune de Oualidia, Maroc (2011–2012). European Scientific Journal, 14, 96–107.Google Scholar
  38. Marks, P. J., Vipond, I. B., Regan, F. M., Wedgwood, K., Fey, R. E., & Caul, E. O. (2003). A school outbreak of Norwalk-like virus: Evidence for airborne transmission. Epidemiology and Infection, 131, 727–736.CrossRefGoogle Scholar
  39. Mead, P. S., Slutsker, L., Dietz, V., McCaig, L. F., Bresee, J. S., Shapiro, C., et al. (1999). Food-related illness and death in the United States. Emerging Infectious Diseases Journal, 5, 607–625.CrossRefGoogle Scholar
  40. Mesquita, J. R., Vaz, L., Cerqueira, S., Castilho, F., Santos, R., Monteiro, S., et al. (2011). Norovirus, hepatitis A virus and enterovirus presence in shellfish from high quality harvesting areas in Portugal. Food Microbiology, 28, 936–941.CrossRefGoogle Scholar
  41. Neish, A. (2013). (CEFAS) Investigative trials on the purification of oysters to identify ways of reducing norovirus. CEFAS contract report C5224.Google Scholar
  42. Nenonen, N. P., Hannoun, C., Laesson, C. U., & Bergström, T. (2012). Marked genomic diversity of norovirus genogroup I strain in a waterborne outbreak. Applied Environmental Microbiology, 78(6), 1846–1852.CrossRefGoogle Scholar
  43. Nguyen, G. T., Phan, K., Teng, I., Pu, J., & Watanabe, T. (2017). A systematic review and meta-analysis of the prevalence of norovirus in cases of gastroenteritis in developing countries. Medicine, 96, e8139.  https://doi.org/10.1097/MD.00000000008139.CrossRefGoogle Scholar
  44. Nishida, T., Nishio, O., Kato, M., Chuma, T., Kato, H., Iwata, H., et al. (2007). Genotyping and quantitation of noroviruses in oysters from two distinct sea areas in Japan. Microbiology Immunology, 51(2), 177–184.CrossRefGoogle Scholar
  45. Patel, M. M., Widdowson, M. A., Glass, R. I., Akazawa, K., Vinje, J., & Parashar, U. D. (2008). Systematic literature review of role of noroviruses in sporadic gastroenteritis. Emerging Infectious Diseases Journal, 14, 1224–1231.CrossRefGoogle Scholar
  46. Polo, D., Alvarez, C., Diez, J., Darriba, S., Longa, A., & Romalde, J. L. (2014). Viral elimination during commercial depuration of shellfish. Food Control, 43, 206–212.CrossRefGoogle Scholar
  47. Svraka, S., Duizer, E., Vennema, H., De Bruin, E., Van Der Veer, B., Dorresteijn, B., et al. (2007). Etiological role of viruses in outbreaks of acute gastroenteritis in The Netherlands from 1994 through 2005. Journal of Clinical Microbiology, 45(5), 1389–1394.CrossRefGoogle Scholar
  48. Ueki, Y., Shoji, M., & Suto, A. (2007). Persistence of caliciviruses in artificially contaminated oysters during depuration. Applied and Environmental Microbiology, 73(17), 5698–5701.CrossRefGoogle Scholar
  49. Vega, E., Barclay, L., Gregoricus, N., Hannah Shirley, S., David, L. D., & Vinjéa, J. (2014). Genotypic and epidemiologic trends of norovirus outbreaks in the United States, 2009 to 2013. Journal of Clinical Microbiology, 52(1), 147–155.CrossRefGoogle Scholar
  50. Vega, E., Barclay, L., Gregoricus, N., Williams, K., Lee, D., & Vinjé, J. (2011). Novel surveillance network for norovirus gastroenteritis outbreaks, United States. Emerging Infectious Diseases, 17, 1389–1395.Google Scholar
  51. Vilariňo, M. L., Le Guyader, F. S., Polo, D., Schaeffer, J., Kröl, J., & Romalde, J. L. (2009). Assessment of human enteric viruses in cultured and wild bivalve molluscs. International Microbiology., 12(3), 145–151.Google Scholar
  52. Vinjé, J. (2015). Advances in laboratory methods for detection and typing of norovirus. Journal of Clinical Microbiology, 53(2), 373–381.CrossRefGoogle Scholar

Copyright information

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

Authors and Affiliations

  • N. El Moqri
    • 1
    Email author
  • F. El Mellouli
    • 2
  • N. Hassou
    • 1
  • M. Benhafid
    • 3
  • N. Abouchoaib
    • 2
  • S. Etahiri
    • 1
  1. 1.Marine Biotechnology and Environment Laboratory, Faculty of SciencesUniversity Chouaib DoukkaliEl JadidaMorocco
  2. 2.Casablanca Regional Research and Analysis Laboratory of National Office of Sanitary Safety and Food Products (ONSSA)CasablancaMorocco
  3. 3.Virology LaboratoryNational Institute of HygieneRabatMorocco

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