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.
Similar content being viewed by others
References
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.
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.
Ang, L. H. (1998). An outbreak of viral gastroenteritis associated with eating raw oysters. Communicable Disease and Public Health, 1(1), 38–40.
Atmar, R. L. (2010). Noroviruses: State of the art. Food and Environmental Virology, 2(3), 117–126.
Atmar, R. L., & Estes, M. K. (2006). The epidemiologic and clinical importance of norovirus infection. Gastroenterology Clinics of North America, 35(2), 275–290.
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.
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.
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.
Bellou, M., Kokkinos, P., & Vantarakis, A. (2013). Shellfish-borne viral outbreaks: A systematic review. Food and Environmental Virology, 5(1), 13–23.
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.
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.
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.
Chalmers, J. W., & McMillan, J. H. (1995). An outbreak of viral gastroenteritis associated with adequately prepared oysters. Epidemiology and Infection, 115(1), 163–167.
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.
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.
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.
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.
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.
Glass, R. I., Parashar, U. D., & Estes, M. K. (2009). Norovirus gastroenteritis. The New England Journal Medicine, 361, 1776–1785.
Greening, G. E. (2006). Human and animal viruses in food (including taxonomy of enteric viruses). Food Microbiology and Food Safety, 5–42.
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.
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.
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.
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.
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.
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.
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.
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.
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.
Lees, D. N. (2000). Viruses and bivalve shellfish. International Journal Food of Microbiology., 59, 81–116.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
Neish, A. (2013). (CEFAS) Investigative trials on the purification of oysters to identify ways of reducing norovirus. CEFAS contract report C5224.
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.
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.
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.
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.
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.
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.
Ueki, Y., Shoji, M., & Suto, A. (2007). Persistence of caliciviruses in artificially contaminated oysters during depuration. Applied and Environmental Microbiology, 73(17), 5698–5701.
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.
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.
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.
Vinjé, J. (2015). Advances in laboratory methods for detection and typing of norovirus. Journal of Clinical Microbiology, 53(2), 373–381.
Author information
Authors and Affiliations
Corresponding author
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
El Moqri, N., El Mellouli, F., Hassou, N. et al. Norovirus Detection at Oualidia Lagoon, a Moroccan Shellfish Harvesting Area, by Reverse Transcription PCR Analysis. Food Environ Virol 11, 268–273 (2019). https://doi.org/10.1007/s12560-019-09386-0
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12560-019-09386-0