Prevalence of Escherichia coli and Salmonella spp. in mussels (Mytilus galloprovincialis) and serotyping of Salmonella spp. in Zenata and Mansouria regions of Morocco
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Abstract
Due to their immobile nature and filter-feeding habits, which enable biological particles to accumulate in their tissues, mussels are recognized as vectors of foodborne diseases. Consuming these shellfish uncooked or partly processed might result in food poisoning because of accumulated bacteria originating from the culture environment and unhygienic handling. The present study aimed to assess the presence of Salmonella and Escherichia coli as well as to biochemically and serotypically confirm Salmonella spp. in mussels (Mytilus galloprovincialis) taken from two locations in Morocco: Zenata and Mansouria. A total of 90 mussel samples were collected from October 2022 to August 2023. Two methods were employed in this study: AFNOR NF EN ISO 6579-1 (2017) for the detection of Salmonella spp., and the most probable number method (MPN) using Norm ISO/TS 16649–3 (2017) for E. coli. The number of E. coli varied between 0.2/100 g and 1.7 x 103/100 g of mussels. The percentage of Salmonella spp. detected in mussel samples was 4,4%. Further analysis revealed the identification of two distinct Salmonella serotypes, namely S. kentucky (1 isolate) and S. Typhimurium (3 isolates). This research highlights the potential risks to public health due to the presence of pathogenic bacteria in mussels from two regions of Morocco where shellfish farming and coastal tourism are significant contributors to the local economy.
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Keywords
Escherichia coli, Food Safety, Mussels, Mytilus galloprovincialis, Salmonella, Serotyping
References
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Boutaib, R., Marhraoui, M., Oulad Abdellah, M.K., & Bouchrif, B., (2011). Comparative Study on Faecal Contamination and Occurrence of Salmonella spp. and Vibrio parahaemolyticus in Two Species of Shellfish in Morocco. Open Environmental Sciences, 2011, 5, 30-37. DOI: 10.2174/1876325101105010030.
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Baudart, J., Lemarchand, K., Brisabois, A., &Lebaron, P. (2000). Diversity of Salmonella strains isolated from the aquatic environment as determined by serotyping and amplification of the ribosomal DNA spacer regions. Appl. Environ. Microbiol., 66, 1544–1552. DOI: 10.1128/aem.66.4.1544-1552.2000.
Baylis, C., Uyttendaele, M., Joosten, H., & Davies, A. (2011). The Enterobacteriaceae and their significance to the food industry. Available at: https://www.cabdirect.org/cabdirect/FullTextPDF/2014/20143006754.pdf , Accessed 11th Nov 2021. ISBN: 9789078637332.
Bingol, Baris, Colak, E., Hampikyan, H., &Muratoglu, K. (2008). "The microbiological quality of stuffed mussels (Midye Dolma) sold in Istanbul". British Food Journal, Vol. 110, No. 11, pp. 1079-1087. https://doi.org/10.1108/00070700810917992.
Bjørn, Tore Lunestad, Frantzen, Sylvia, Cecilie, Smith, Svanevik, Irja, Sunde, Roiha, & Arne, Duinker,. (2016). Time trends in the prevalence of Escherichia coli and enterococci in bivalves harvested in Norway during 2007–2012. Food Control., Volume 60, February 2016, Pages 289-295. https://doi.org/10.1016/j.foodcont.2015.08.001.
Boutaib, R., Marhraoui, M., Oulad Abdellah, M.K., & Bouchrif, B., (2011). Comparative Study on Faecal Contamination and Occurrence of Salmonella spp. and Vibrio parahaemolyticus in Two Species of Shellfish in Morocco. Open Environmental Sciences, 2011, 5, 30-37. DOI: 10.2174/1876325101105010030.
Butt, A.A., Aldridge, K.E., & Sanders, C.V. (2004). Infections related to the ingestion of seafood Part I: Viral and bacterial infections. The Lancet Infectious Diseases, 4 (4) (2004), pp. 201-212. https://doi.org/10.1016/S1473-3099(04)00969-79. Commission Implementing Regulation (EU) 2019/627. (2019). Official Journal of the European Union, Article 52: Classification of production and relaying areas for live bivalve molluscs, L 131/51, 15 March 2019.
Campos, C.J., Avant, J., Gustar, N., Lowther, J., Powell, A., Stockley, L., &N lees, D. (2015). Fate of human noroviruses in shellfish and water impacted by frequent sewage pollution events. Environmental Science & Technology, 49 (14) (2015), pp. 8377-8385. https://doi.org/10.1021/acs.est.5b0126811. Costa, R.A. (2013). Escherichia coli in seafood: A brief overview. Advances in Bioscience and Biotechnology, 4 (2013), 450-454. http://dx.doi.org/10.4236/abb.2013.43A060 P.
Dabrowski, T., Doré, W.J., Lyons, K., & Nolan, G.D. (2014). Numerical modelling of blue mussel (Mytilus edulis) bacterial contamination. J. Sea Res., 89 (2014), 52-63. https://doi.org/10.1016/j.seares.2014.02.005.
Donovan, T. J., Gallacher, S., Andrews, N., Greenwood, M., Graham, J., Russell, J., Roberts, S., &Lee, R. (1998). Modification of the standard method used in the United Kingdom for counting Escherichia coli in live bivalve molluscs. Commun. Dis. Publ. Health, 1 (3), 188–196. PMID: 9782634.
Ghaichat, S., Mahari, I., Zekhnini, H., El, Mellouli, F., & Lakhiari, H. (2023). Molecular analysis and prevalence of Hepatitis A and Norovirus GI and GII of mussels by real-time reverse transcription in the Zenata area, Morocco. Teikyo Medical Journal, Volume 46, Issue 6, June, 2023. ISSN: 03875547.
Grimont, P., Une, D., &Weill, F.X. (2007). Antigenic formulae of the Salmonella serovars. Institut du Pasteur (9th edition).
Gyawali, P., & Hewitt. J. (2020). Fecal contamination in bivalve molluscan shellfish: Can the application of the microbial source tracking method minimize public health risks? Current Opinion in Environmental Science & Health, 16 (2020), pp. 14-21. DOI: 10.1016/j.coesh.2020.02.005.
Hackney, C.R., &Potter, M.E. (1994). Animal-associated and terrestrial bacteria pathogens. In Hackney C.R., and Pierson (ed.) M. D., Environmental indicators and shellfish safety, Chap- man & Hall, New York, p. 172–209.
Huss, H.H., (1994). Assurance of seafood quality. FAO Fisheries Technical Paper, 334 (1994), p. 169. ISBN 92-5-103446-X.
ISO 16649-3, 2017 (2017). Food chain microbiology – Horizontal method for the enumeration of beta-glucuronidase positive Escherichia coli – Part 3: Most probable number investigation and technique using bromo-5-chloro-4-indolyl-3 β-D-glucuronate. International Organization for Standardization, Geneva.
20. ISO 6579-1, 2017 (2017). Microbiology of the food chain – Horizontal method for the detection, enumeration and serotyping of Salmonella – Part 1: Detection of Salmonella spp. International Organization for Standardization, Geneva.
Jang, J., Hur, H.G., Sadowsky, M.J., Byappanahalli, M.N., Yan, T., & Ishii, S. (2017). Environmental Escherichia coli: Ecology and public health implications—a review. Journal of Applied Microbiology, 123 (3) (2017), pp. 570-581. DOI: 10.1111/jam.13468.
Kaper, J.B., Nataro, J.P., & Mobley, H.L.T. (2004). Pathogenic Escherichia coli. Nature Reviews Microbiology, 2 (2004), pp. 123-140. DOI: 10.1038/nrmicro818.
Kauffman, G. (1974). Kauffman white scheme. WHO. Pd 172, 1, rev. 1. Acta Pathol. Microbiol. Scand., A - B, 61 (1974), p. 385.
Lamon, S., Piras, F., Meloni, D., Agus, V., Porcheddu, G., Pes, M., Giovanna, M., Giuseppe, C., Federica, E., Simonetta, F., Consolati, G., & Mureddu, A. (2020). Enumeration of Escherichia coli and determination of Salmonella spp. and verotoxigenic Escherichia coli in shellfish (Mytilus galloprovincialis and Ruditapes decussatus) harvested in Sardinia, Italy. Ital. J. Food Saf., 2020 Dec 3, 9(4), 8625. DOI: 10.4081/ijfs.2020.8625.
Lorenzoni, G., Tedde, G., Mara, L., Bazzoni, A.M., Esposito, G., Salza, S., &Piras, G., Tiziana, T., Bazzardi, R., Arras, I., Uda, M.T., Virgilio, S., Meloni, D., & Mudadu, A.G. (2021). Presence seasonal distribution and biomolecular characterization of Vibrio parahaemolyticus and Vibrio vulnificus in shellfish harvested and marketed in Sardinia (Italy) between 2017 and 2018. Journal of Food Protection, 84 (9) (2021), pp. 1549-1554. DOI: 10.4315/JFP-21-059.
Lozano-Leon, A., Garcia-Omil, C., Dalama, J., Rodriguez-Souto, R., Martinez-Urtaza, J., & Gonzalez-Escalona, N. (2019). Detection of colistin resistance mcr-1 gene in Salmonella enterica serovar Rissen isolated from mussels, Spain, 2012 to 2016. Eurosurveillance 2019, 24 (16), 1900200. DOI: 10.2807/1560-7917.ES.2019.24.16.1900200.
Mancini, M.E., Alessiani, A., Donatiello, A., Didonna, A., D’Attoli, L., Faleo, S., Occhiochiuso, G., Carella, F., Di Taranto, P., Pace, L., Rondinone, V., Damato, A.M., Coppola, R., Pedarra, C., & Goffredo, E. (2023). Systematic Survey of Vibrio spp. and Salmonella spp. in Bivalve Shellfish in Apulia Region (Italy): Prevalence and Antimicrobial Resistance. Microorganisms. 11(2), 450. https://doi.org/10.3390/microorganisms11020450.
Mannas, H., Mimouni, R., Chaouqy, N., Hamadi, F., & Martinez-Urtaza, J. (2014). Occurrence of Vibrio and Salmonella species in mussels (Mytilus galloprovincialis) collected along the Moroccan Atlantic coast. SpringerPlus, 3, 265 (2014). https://doi.org/10.1186/2193-1801-3-265.
29. Marceddu, M., Lamon, S., Consolati, S.G., Ciulli, S., Mazza, R., Mureddu, A., & Meloni, D. (2017). Determination of Salmonella spp., E. coli VTEC, Vibrio spp., and norovirus GI-GII in bivalve molluscs collected from growing natural beds in Sardinia (Italy). Foods, 6 (10) (2017), p. 88. DOI: 10.3390/foods6100088.
Martinez-Urtaza, J., Saco, M., de Novoa, J., Perez-Piñeiro, P., Peiteado, J., Lozano-León, A., &Garcia-Martin, O. (2004). Influence of environmental factors and human activity on the presence of Salmonella serovars in a marine environment. Appl. Environ. Microbiol., 70, 2089-2097. DOI: 10.1128/AEM.70.4.2089-2097.2004.
Mudado, A.G., Spanu, C., Pantoja, J.C.F., Dos Santos, M.C., De Oliveira, C.D., Salza, S., Piras, G., Uda, M.T., Virgilio, S., Giagnoni, L., Pereira, J.G., & Tedde, T. (2022). Association between Escherichia coli and Salmonella spp. food safety criteria in live bivalve molluscs from wholesale and retail markets. Food Control., Volume 137, July 2022, 108942. https://doi.org/10.1016/j.foodcont.2022.108942.
Mudadu, A.G., Salza, S., Melillo, R., Mara, L., Piras, G., Spanu, C., Giovanni, Terrosu, Fadda, A., Virgilio, S., & Tedde, T. (2021). Prevalence and pathogenic potential of Arcobacter spp. isolated from edible bivalve molluscs in Sardinia. Food Control, 127 (4), 108139. DOI: 10.1016/j.foodcont.2021.108139.
OMS. (2015). OMS estimates of the global burden of foodborne disease Foodborne diseases burden epidemiology reference group 2007–2015.http://apps.who.int/iris/handle/10665/199350〉 (accessed 29 November 2023).
Polo, D., Varela, M.F., & Romalde, J.L. (2015). Detection and quantification of hepatitis A virus and norovirus in Spanish authorized shellfish harvesting areas. International Journal of Food Microbiology, 193 (2015), pp. 43-50. DOI: 10.1016/j.ijfoodmicro.2014.10.007.
Potasman, I., Paz, A., & Odeh, M. (2002). Infectious outbreaks associated with bivalve shellfish consumption: a worldwide perspective. Clin. Infect. Dis., 35 (8), pp. 921-928. DOI: 10.1086/342330.
Roszak, D.B., Grimes, D. J., &Colwell, R.R. (1984). Viable but nonrecoverable stage of Salmonella enteritidis in aquatic systems. Can. J. Microbiol., 30 (3), 334–338. DOI: 10.1139/m84-049.
Rubini, S., Giorgio, G., D’Incau, M., Govoni, G., Boschetti, L., Berardelli, C., Barbieri, S., Merialdi, G., Formaglio, A., Guidi, E., Bergamini, M., Piva, S., Serraino, A., & Giacometti, F. (2018). Occurrence of Salmonella enterica subsp. enterica in bivalve molluscs and associations with Escherichia coli in molluscs and faecal coliforms in seawater. Food Control, Volume 84, February 2018, Pages 429-435. https://doi.org/10.1016/j.foodcont.2017.08.035.
Sanjee, S.A., & Karim, M.E. (2016). Microbiological quality assessment of frozen fish and fish processing materials from Bangladesh. International Journal of Food Science, 8605689 (2016), pp. 1-6. DOI: 10.1155/2016/8605689.
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Prevalence of Escherichia coli and Salmonella spp. in mussels (Mytilus galloprovincialis) and serotyping of Salmonella spp. in Zenata and Mansouria regions of Morocco. (2024). Journal of Applied and Natural Science, 16(3), 1115-1122. https://doi.org/10.31018/jans.v16i3.5721
