Spatial-temporal assessment of Norovirus contamination in mussels from Cherrat estuary, Morocco, by real-time Reverse Transcription-Polymerase Chain Reaction
Article Main
Abstract
Mussels filter large amounts of water to extract nutrients; therefore, they can concentrate and accumulate in their tissues infectious agents, and vectors of enteric diseases. The aim of this study was to assess mussel contamination by Norovirus genogroups I and II in the Cherrat estuary to determine the public health risk linked to their consumption. Mussels (Mytilus galloprovincialis) were collected (n=52 samples; 12 mussels/sample) at four sites (S1 and S2 located on the right rocky bank / S3 and S4, located on the rocky left bank) in the Cherrat estuary (Casa-Settat region), Morocco, during 13 months, from March 2019 to March 2020. Norovirus was detected and quantified by real-time Reverse Transcription-Polymerase Chain Reaction (RT-PCR). Norovirus genogroups I and II were detected in 17.30% and 94.23% of mussel samples, respectively. Contamination by Norovirus (genogroups I and II) was not correlated with seasonal factors (month and rainfall), and Norovirus prevalence was comparable among the four sampling sites. Consumption of raw or undercooked mussels contaminated with Norovirus can cause gastroenteritis, which represents a potential risk to human health. The present study would be helpful to control and manage the potential risk to the public health of the Moroccan population due to the degradation of water quality continuously impacted by runoff, the urban wastewater treatment system malfunctions, and overflows from nearby sewage systems.
Article Details
Article Details
Keywords
Cherrat estuary, mussels, Norovirus genogroups I and II, real-time RT-PCR, Viral contamination
References
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Bellou, M., Kokkinos, P. & Vantarakis, A. (2013). Shellfish-borne viral outbreaks: a systematic review. Food and Environmental Virology, 5, 13-23.https://doi.org/10.1007/s12560-012-9097-6
Benabbes, L., Ollivier, J., Schaeffer, J., Parnaudeau, S., Rhaissi, H., Nourlil, J. & Le Guyader, F. S. (2013). Norovirus and other human enteric viruses in Moroccan shellfish. Food and Environmental Virology, 5, 35-40.https://doi.org/10.1007/s12560-012-9095-8
Bonura, F., Urone, N., Bonura, C., Mangiaracina, L., Filizzolo, C., Sciortino, G. et al. (2021). Recombinant GII. P16 genotype challenges RT-PCR-based typing in region A of norovirus genome. Journal of Infection, 83(1), 69-75.https://doi.org/10.1016/j.jinf.2021.04.015
Cantelli, P., da Silva, M., Fumian, T., da Cunha, D., Andrade, J., Malta, F., da Silva, E., Mouta, S., Fialho, A., de Moraes, M., Brasil, P., Miagostovich, M., Leite, J. (2019). High genetic diversity of noroviruses in children from a community-based study in Rio de Janeiro, Brazil, 2014–2018. Archives of virology. 164 (5), 1427–1432. https://doi.org/10.1007/s00705-019-04195-z
Chhabra, P., de Graaf, M., Parra, G. I., Chan, M. C. W., Green, K., Martella, V., Wang, Q., White, P. A., Katayama, K., Vennema, H., Koopmans, M. P. G. & Vinjé, J. (2019). Updated classification of norovirus genogroups and genotypes. The Journal of general virology, 100:1393-1406. DOI 10.1099/jgv.0.001318
Da Silva, A. K., Le Saux, J. C., Parnaudeau, S., Pommepuy, M., Elimelech, M. & Le Guyader, F. S. (2007). Evaluation of removal of noroviruses during wastewater treatment, using real-time reverse transcription-PCR: different behaviors of genogroups I and II. Applied and environmental microbiology, 73, 7891-7897.https://doi.org/10.1128/AEM.01428-07
Das, O., Lekshmi, M., Kumar, S., Nayak, B. (2020). Incidence of norovirus in tropical seafood harbouring fecal indicator bacteria. Marine Pollution Bulletin. 150, 110777. https://doi.org/10.1016/j.marpolbul.2019.110777
De Andrade, J. D. S. R., Fumian, T. M., Leite, J. P. G., de Assis, M. R., Fialho, A.M., Mouta, S., Santiago, C. M. P. & Miagostovich, M. P. (2017). Norovirus GII. 17 associated with a foodborne acute gastroenteritis outbreak in Brazil, 2016. Food and environmental virology, 10, 212-216. https://doi.org/10.1007/s12560-017-9326-0
El Moqri, N., El Mellouli, F., Hassou, N., Benhafid, M., Abouchoaib, N. & Etahiri, S. (2019). Norovirus Detection at Oualidia Lagoon, a Moroccan Shellfish Harvesting Area, by Reverse Transcription PCR Analysis. Food Environ Virol, 11, 268–273.https://doi.org/10.1007/s12560-019-09386-0
Ferla, S., Varricchio, C., Knight, W., Ho, P. K., Saporito, F., Tropea, B., Fagan, G., Flude, B. M., Bevilacqua, F., Santos-Ferreira, N. et al. (2021). Structure–Activity Relationship Studies on Novel Antiviral Agents for Norovirus Infections. Microorganisms, 9, 1795.https://doi.org/10.3390/microorganisms9091795
Flannery, J., Keaveney, S., Rajko-Nenow, P., O’Flaherty, V. & Doré, W. (2013). Norovirus and FRNA bacteriophage determined by RT-qPCR and infectious FRNA bacteriophage in wastewater and oysters. Water Research, 47, 5222–5231. https://doi.org/10.1016/j.watres.2013.06.008
Fusco, G., Anastasio, A., Kingsley, D., Amoroso, M., Pepe, T., Fratamico, P., Cioffi, B., Rossi, R., La Rosa, G., Boccia, F. (2019). Detection of hepatitis A virus and other enteric viruses in shellfish collected in the Gulf of Naples, Italy. International Journal of Environmental Research and Public Health, 16 (14). 2588. https://doi.org/10.3390/ijerph16142588
Harsono, N. D. B. D., Ransangan, J., Denil, D. J. & Tan, K. S. (2017). Heavy metals in marsh clam (Polymesoda expansa) and green mussel (Perna viridis) along the northwest coast of Sabah, Malaysia. Borneo Journal of Marine Science and Aquaculture. https://doi.org/10.51200/bjomsa.v1i0.987
Hassard, F., Sharp, J. H., Taft, H., LeVay, L., Harris, J. P., McDonald, J. E. & Malham, S. K. (2017). Critical Review on the Public Health Impact of Norovirus Contamination in Shellfish and the Environment: A UK Perspective. Food and Environmental Virology, 9, 123–141. https://doi:10.1007/s12560-017-9279-3
Hewitt, J., Greening, G. E., Leonard, M. & Lewis, G. D. (2013). Evaluation of human adenovirus and human polyomavirus as indicators of human sewage contamination in the aquatic environment. Water Research, 47, 6750-6761. https://doi.org/10.1016/j.watres.2013.09.001
Kageyama, T., Kojima, S., Shinohara, M., Uchida, K., Fukushi, S., Hoshino, F. B., Takeda, N. & Katayama, K. (2003). Broadly reactive and highly sensitive assay for Norwalk-like viruses based on real-time quantitative reverse transcription-PCR. Journal of clinical microbiology, 41, 1548-1557.https://doi.org/10.1128/JCM.41.4.1548-1557.2003
Karangwa, C. K., Parra, G. I., Bok, K., Johnson, J. A., Levenson, E. A. & Green, K. Y. (2017). Sequential gastroenteritis outbreaks in a single year caused by norovirus genotypes GII. 2 and GII. 6 in an institutional setting. Open forum infectious diseases, 4, ofx236. https://doi.org/10.1093/ofid/ofx236
Knight, A., Haines, J., Stals, A., Li, D., Uyttendaele, M. & Jaykus, L. A. (2016). A systematic review of human norovirus survival reveals a greater persistence of human norovirus RT-qPCR signals compared to those of cultivable surrogate viruses. International journal of food microbiology, 216, 40-49.https://doi.org/10.1016/j.ijfoodmicro.2015.08.015
Kosek, M., Bern, C. & Guerrant, R. L. (2003). The global burden of diarrhoeal disease, as estimated from studies published between 1992 and 2000. Bulletin of the world health organization, 81, 197-204.
Loisy, F., Atmar, R. L., Guillon, P., Le 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.https://doi.org/10.1016/j.jviromet.2004.08.023
Lowther, J.A., Gustar, N. E., Powell, A. L., O’Brien, S. & Lees, D. N. (2018). A one-year survey of norovirus in UK oysters collected at the point of sale. Food and Environmental Virology, 10, 278-287.https://doi.org/10.1007/s12560-018-9338-4
Ministry of Energy, Mines, Water and of the Environment in charge of the environment / Ministry of Equipment, Transport and Logistics (2016). National report -Monitoring of the quality of bathing water, Morocco, p 41.
Ministry of Territorial Development, Water and the Environment/Secretariat of State for the Environment (2003). Thematic report on protected areas in Morocco, p 27.
Oliveira, J., Cunha, A., Castilho, F., Romalde, J. L. & Pereira, M. J. (2011). Microbial contamination and purification of bivalve shellfish: Crucial aspects in monitoring and future perspectives–A mini-review. Food Control, 22, 805-816.https://doi.org/10.1016/j.foodcont.2010.11.032
Reymão, T., Fumian, T., Justino, M., Hernandez, J., Bandeira, R., Lucena, M., Teixeira, D., Farias, F., Silva, L., Linhares, A., Gabbay, Y. (2018). Norovirus RNA in serum associated with increased fecal viral load in children: detection, quantification and molecular analysis. PLoS One 13 (7), e0199763. https://doi.org/10.1371/journal.pone.0199763
Schaeffer, J., Le Saux, J. C., Lora, M., Atmar, R. L., Le Guyader, F. S. (2013). Norovirus contamination on French marketed oysters. International journal of food microbiology, 166, 244-248. https://doi.org/10.1016/j.ijfoodmicro.2013.07.022
Schaeffer, J., Treguier, C., Piquet, J. C., Gachelin, S., Cochennec-Laureau, N., Le Saux, J. C. et al. (2018). Improving the efficacy of sewage treatment decreases norovirus contamination in oysters. International journal of food microbiology, 286, 1-5.https://doi.org/10.1016/j.ijfoodmicro.2018.07.016
Svraka, S., Duizer, E., Vennema, H., de Bruin, E., van der Veer, B., Dorresteijn, B. & Koopmans, M. (2007). Etiological role of viruses in outbreaks of acute gastroenteritis in The Netherlands from 1994 through 2005. Journal of clinical microbiology, 45, 1389-1394.https://doi.org/10.1128/JCM.02305-06
Tarek, F., Benani, A., Hassou, N., Bessi, H. & Ennaji, M.M. (2019). Investigating of Norovirus genogroups I and II using bivalve mollusks biomarkers from the wild lagoon. Ecology, Environment and Conservation, 25 (4), 1885-1890.
Tatusov, R. L., Chhabra, P., Diez-Valcarce, M., Barclay, L., Cannon, J. L. & Vinjé, J. (2021). Human Calicivirus Typing tool: A web-based tool for genotyping human norovirus and sapovirus sequences. Journal of Clinical Virology, 134, 104718.https://doi.org/10.1016/j.jcv.2020.10 4718
Victoria, M., Guimarães, F. R., Fumian, T. M., Ferreira, F. F., Vieira, C. B. et al. (2010a). One year monitoring of norovirus in a sewage treatment plant in Rio de Janeiro, Brazil. Journal of Water Health, 8, 158–165.https://doi.org/10.2166/wh.2009.012
Victoria, M., Rigotto, C., Moresco, V., de Abreu Corrêa, A., Kolesnikovas, C. et al. (2010b). Assessment of norovirus contamination in environmental samples from Florianópolis City, Southern Brazil. Journal of Applied Microbiology, 109, 231–238.https://doi.org/10.1111/j.1365-2672.2009.04646.x
Winterbourn, J. B., Clements, K., Lowther, J. A., Malham, S. K., McDonald, J. E. et al. (2016). Use of Mytilus edulis biosentinels to investigate spatial patterns of norovirus and faecal indicator organism contamination around coastal sewage discharges. Water Research, 105, 241–250.https://doi.org/10.1016/j.watres.2016.09.002
Zakhour, M., Maalouf, H., Di Bartolo, I., Haugarreau, L., Le Guyader, F. S. et al. (2010). Bovine norovirus: Carbohydrate ligand, environmental contamination, and potential cross-species transmission via oysters. Applied and Environmental Microbiology, 76, 6404–6411.https://doi.org/10.1128/AEM.00671-10
Zormati, S., Kallel, I., Sellami, H. & Gdoura, R. (2018). Influence of environmental and seasonal factors on microbial contamination levels in clam production areas in southern Tunisia: Escherichia coli, Salmonella spp., hepatitis A virus and norovirus. Scientific and technical review (International Office of Epizootics), 37, 1061-1070. https://doi: 10.20506/rst.37.3.2906
Bazzardi, R., Fattaccio, M. C., Salza, S., Canu, A., Marongiu, E. & Pisanu, M. (2014). Preliminary study on Norovirus, hepatitis A virus, Escherichia coli and their potential seasonality in shellfish from different growing and harvesting areas in Sardinia region. Italian Journal of Food Safety, 3, 1601. https://doi:10.4081/ijfs.2014.1601
Bellou, M., Kokkinos, P. & Vantarakis, A. (2013). Shellfish-borne viral outbreaks: a systematic review. Food and Environmental Virology, 5, 13-23.https://doi.org/10.1007/s12560-012-9097-6
Benabbes, L., Ollivier, J., Schaeffer, J., Parnaudeau, S., Rhaissi, H., Nourlil, J. & Le Guyader, F. S. (2013). Norovirus and other human enteric viruses in Moroccan shellfish. Food and Environmental Virology, 5, 35-40.https://doi.org/10.1007/s12560-012-9095-8
Bonura, F., Urone, N., Bonura, C., Mangiaracina, L., Filizzolo, C., Sciortino, G. et al. (2021). Recombinant GII. P16 genotype challenges RT-PCR-based typing in region A of norovirus genome. Journal of Infection, 83(1), 69-75.https://doi.org/10.1016/j.jinf.2021.04.015
Cantelli, P., da Silva, M., Fumian, T., da Cunha, D., Andrade, J., Malta, F., da Silva, E., Mouta, S., Fialho, A., de Moraes, M., Brasil, P., Miagostovich, M., Leite, J. (2019). High genetic diversity of noroviruses in children from a community-based study in Rio de Janeiro, Brazil, 2014–2018. Archives of virology. 164 (5), 1427–1432. https://doi.org/10.1007/s00705-019-04195-z
Chhabra, P., de Graaf, M., Parra, G. I., Chan, M. C. W., Green, K., Martella, V., Wang, Q., White, P. A., Katayama, K., Vennema, H., Koopmans, M. P. G. & Vinjé, J. (2019). Updated classification of norovirus genogroups and genotypes. The Journal of general virology, 100:1393-1406. DOI 10.1099/jgv.0.001318
Da Silva, A. K., Le Saux, J. C., Parnaudeau, S., Pommepuy, M., Elimelech, M. & Le Guyader, F. S. (2007). Evaluation of removal of noroviruses during wastewater treatment, using real-time reverse transcription-PCR: different behaviors of genogroups I and II. Applied and environmental microbiology, 73, 7891-7897.https://doi.org/10.1128/AEM.01428-07
Das, O., Lekshmi, M., Kumar, S., Nayak, B. (2020). Incidence of norovirus in tropical seafood harbouring fecal indicator bacteria. Marine Pollution Bulletin. 150, 110777. https://doi.org/10.1016/j.marpolbul.2019.110777
De Andrade, J. D. S. R., Fumian, T. M., Leite, J. P. G., de Assis, M. R., Fialho, A.M., Mouta, S., Santiago, C. M. P. & Miagostovich, M. P. (2017). Norovirus GII. 17 associated with a foodborne acute gastroenteritis outbreak in Brazil, 2016. Food and environmental virology, 10, 212-216. https://doi.org/10.1007/s12560-017-9326-0
El Moqri, N., El Mellouli, F., Hassou, N., Benhafid, M., Abouchoaib, N. & Etahiri, S. (2019). Norovirus Detection at Oualidia Lagoon, a Moroccan Shellfish Harvesting Area, by Reverse Transcription PCR Analysis. Food Environ Virol, 11, 268–273.https://doi.org/10.1007/s12560-019-09386-0
Ferla, S., Varricchio, C., Knight, W., Ho, P. K., Saporito, F., Tropea, B., Fagan, G., Flude, B. M., Bevilacqua, F., Santos-Ferreira, N. et al. (2021). Structure–Activity Relationship Studies on Novel Antiviral Agents for Norovirus Infections. Microorganisms, 9, 1795.https://doi.org/10.3390/microorganisms9091795
Flannery, J., Keaveney, S., Rajko-Nenow, P., O’Flaherty, V. & Doré, W. (2013). Norovirus and FRNA bacteriophage determined by RT-qPCR and infectious FRNA bacteriophage in wastewater and oysters. Water Research, 47, 5222–5231. https://doi.org/10.1016/j.watres.2013.06.008
Fusco, G., Anastasio, A., Kingsley, D., Amoroso, M., Pepe, T., Fratamico, P., Cioffi, B., Rossi, R., La Rosa, G., Boccia, F. (2019). Detection of hepatitis A virus and other enteric viruses in shellfish collected in the Gulf of Naples, Italy. International Journal of Environmental Research and Public Health, 16 (14). 2588. https://doi.org/10.3390/ijerph16142588
Harsono, N. D. B. D., Ransangan, J., Denil, D. J. & Tan, K. S. (2017). Heavy metals in marsh clam (Polymesoda expansa) and green mussel (Perna viridis) along the northwest coast of Sabah, Malaysia. Borneo Journal of Marine Science and Aquaculture. https://doi.org/10.51200/bjomsa.v1i0.987
Hassard, F., Sharp, J. H., Taft, H., LeVay, L., Harris, J. P., McDonald, J. E. & Malham, S. K. (2017). Critical Review on the Public Health Impact of Norovirus Contamination in Shellfish and the Environment: A UK Perspective. Food and Environmental Virology, 9, 123–141. https://doi:10.1007/s12560-017-9279-3
Hewitt, J., Greening, G. E., Leonard, M. & Lewis, G. D. (2013). Evaluation of human adenovirus and human polyomavirus as indicators of human sewage contamination in the aquatic environment. Water Research, 47, 6750-6761. https://doi.org/10.1016/j.watres.2013.09.001
Kageyama, T., Kojima, S., Shinohara, M., Uchida, K., Fukushi, S., Hoshino, F. B., Takeda, N. & Katayama, K. (2003). Broadly reactive and highly sensitive assay for Norwalk-like viruses based on real-time quantitative reverse transcription-PCR. Journal of clinical microbiology, 41, 1548-1557.https://doi.org/10.1128/JCM.41.4.1548-1557.2003
Karangwa, C. K., Parra, G. I., Bok, K., Johnson, J. A., Levenson, E. A. & Green, K. Y. (2017). Sequential gastroenteritis outbreaks in a single year caused by norovirus genotypes GII. 2 and GII. 6 in an institutional setting. Open forum infectious diseases, 4, ofx236. https://doi.org/10.1093/ofid/ofx236
Knight, A., Haines, J., Stals, A., Li, D., Uyttendaele, M. & Jaykus, L. A. (2016). A systematic review of human norovirus survival reveals a greater persistence of human norovirus RT-qPCR signals compared to those of cultivable surrogate viruses. International journal of food microbiology, 216, 40-49.https://doi.org/10.1016/j.ijfoodmicro.2015.08.015
Kosek, M., Bern, C. & Guerrant, R. L. (2003). The global burden of diarrhoeal disease, as estimated from studies published between 1992 and 2000. Bulletin of the world health organization, 81, 197-204.
Loisy, F., Atmar, R. L., Guillon, P., Le 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.https://doi.org/10.1016/j.jviromet.2004.08.023
Lowther, J.A., Gustar, N. E., Powell, A. L., O’Brien, S. & Lees, D. N. (2018). A one-year survey of norovirus in UK oysters collected at the point of sale. Food and Environmental Virology, 10, 278-287.https://doi.org/10.1007/s12560-018-9338-4
Ministry of Energy, Mines, Water and of the Environment in charge of the environment / Ministry of Equipment, Transport and Logistics (2016). National report -Monitoring of the quality of bathing water, Morocco, p 41.
Ministry of Territorial Development, Water and the Environment/Secretariat of State for the Environment (2003). Thematic report on protected areas in Morocco, p 27.
Oliveira, J., Cunha, A., Castilho, F., Romalde, J. L. & Pereira, M. J. (2011). Microbial contamination and purification of bivalve shellfish: Crucial aspects in monitoring and future perspectives–A mini-review. Food Control, 22, 805-816.https://doi.org/10.1016/j.foodcont.2010.11.032
Reymão, T., Fumian, T., Justino, M., Hernandez, J., Bandeira, R., Lucena, M., Teixeira, D., Farias, F., Silva, L., Linhares, A., Gabbay, Y. (2018). Norovirus RNA in serum associated with increased fecal viral load in children: detection, quantification and molecular analysis. PLoS One 13 (7), e0199763. https://doi.org/10.1371/journal.pone.0199763
Schaeffer, J., Le Saux, J. C., Lora, M., Atmar, R. L., Le Guyader, F. S. (2013). Norovirus contamination on French marketed oysters. International journal of food microbiology, 166, 244-248. https://doi.org/10.1016/j.ijfoodmicro.2013.07.022
Schaeffer, J., Treguier, C., Piquet, J. C., Gachelin, S., Cochennec-Laureau, N., Le Saux, J. C. et al. (2018). Improving the efficacy of sewage treatment decreases norovirus contamination in oysters. International journal of food microbiology, 286, 1-5.https://doi.org/10.1016/j.ijfoodmicro.2018.07.016
Svraka, S., Duizer, E., Vennema, H., de Bruin, E., van der Veer, B., Dorresteijn, B. & Koopmans, M. (2007). Etiological role of viruses in outbreaks of acute gastroenteritis in The Netherlands from 1994 through 2005. Journal of clinical microbiology, 45, 1389-1394.https://doi.org/10.1128/JCM.02305-06
Tarek, F., Benani, A., Hassou, N., Bessi, H. & Ennaji, M.M. (2019). Investigating of Norovirus genogroups I and II using bivalve mollusks biomarkers from the wild lagoon. Ecology, Environment and Conservation, 25 (4), 1885-1890.
Tatusov, R. L., Chhabra, P., Diez-Valcarce, M., Barclay, L., Cannon, J. L. & Vinjé, J. (2021). Human Calicivirus Typing tool: A web-based tool for genotyping human norovirus and sapovirus sequences. Journal of Clinical Virology, 134, 104718.https://doi.org/10.1016/j.jcv.2020.10 4718
Victoria, M., Guimarães, F. R., Fumian, T. M., Ferreira, F. F., Vieira, C. B. et al. (2010a). One year monitoring of norovirus in a sewage treatment plant in Rio de Janeiro, Brazil. Journal of Water Health, 8, 158–165.https://doi.org/10.2166/wh.2009.012
Victoria, M., Rigotto, C., Moresco, V., de Abreu Corrêa, A., Kolesnikovas, C. et al. (2010b). Assessment of norovirus contamination in environmental samples from Florianópolis City, Southern Brazil. Journal of Applied Microbiology, 109, 231–238.https://doi.org/10.1111/j.1365-2672.2009.04646.x
Winterbourn, J. B., Clements, K., Lowther, J. A., Malham, S. K., McDonald, J. E. et al. (2016). Use of Mytilus edulis biosentinels to investigate spatial patterns of norovirus and faecal indicator organism contamination around coastal sewage discharges. Water Research, 105, 241–250.https://doi.org/10.1016/j.watres.2016.09.002
Zakhour, M., Maalouf, H., Di Bartolo, I., Haugarreau, L., Le Guyader, F. S. et al. (2010). Bovine norovirus: Carbohydrate ligand, environmental contamination, and potential cross-species transmission via oysters. Applied and Environmental Microbiology, 76, 6404–6411.https://doi.org/10.1128/AEM.00671-10
Zormati, S., Kallel, I., Sellami, H. & Gdoura, R. (2018). Influence of environmental and seasonal factors on microbial contamination levels in clam production areas in southern Tunisia: Escherichia coli, Salmonella spp., hepatitis A virus and norovirus. Scientific and technical review (International Office of Epizootics), 37, 1061-1070. https://doi: 10.20506/rst.37.3.2906
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Spatial-temporal assessment of Norovirus contamination in mussels from Cherrat estuary, Morocco, by real-time Reverse Transcription-Polymerase Chain Reaction . (2023). Journal of Applied and Natural Science, 15(1), 155-161. https://doi.org/10.31018/jans.v15i1.4176
