Possibilities of using mussels (Mytilus galloprovincialis) to predict rotavirus contamination in Albania

Lugaj, Arta; Korro, Kastriot; Tolomeo, Anna Maria; Bakiu, Rigers; Santovito, Gianfranco

doi:10.2478/jvetres-2023-0053

Abstract

Introduction

Rotaviruses are non-enveloped viruses that each consist of 11 double-stranded RNA molecules. These viruses are able to persist in the environment, and therefore play a fundamental role in the epidemiology of gastroenteritis and severe diarrhoea in children worldwide. While mussels have been primarily used as indicators of chemical pollution, they can also be used to monitor viral contamination. The purpose of this study was to demonstrate that the Mytilus galloprovincialis mussel can also be used to detect microbial contamination, owing to its tendency to naturally concentrate viruses and other pathogens.

Material and Methods

A total of 102 Mytilus galloprovincialis mussel samples from Albania were collected over a three-year period: 37 samples off the Cape of Stillo in 2015, 39 samples from Butrinti Lake in 2019 and 26 samples from Butrinti Lake in 2021.

Results

The presence of rotavirus in the Cape of Stillo samples in 2015 was noted in 47% of samples from site 1, 33% from site 2, and 52% from site 3. In Butrinti Lake the percentage of infected individuals in 2019 was 33% from site 1, 41% from site 2, and 33% from site 3, whereas in 2021, it was 50% from site 1, 19% from site 2, and 0% from site 3. In total the percentage of infected individuals off the Cape of Stillo in 2015 was 44%, in Butrinti Lake in 2019 it was 36%, and in Butrinti Lake in 2021 it was 23 %.

Conclusion

These results indicate the presence of rotavirus in the shellfish specimens tested, and further analysis is needed to assess the potential health risks associated with consuming these shellfish. This study also indicates that mussels can be used in marine virological surveillance programmes.

References

Annarita P., Grassi T., Donia D., De Donno A., Idolo A., Alfio C., Alessandri C., Alberto S., Divizia M.: Detection and molecular characterization of human rotaviruses isolated in Italy and Albania. J Med Virol 2010, 82, 510–518, doi: 10.1002/jmv.21700.
Open DOI Search in Google Scholar Back to article
Armah G.E., Sow S.O., Breiman R.F., Dallas M.J., Tapia M.D., Feikin D.R., Binka F.N., Steele A.D., Laserson K.F., Ansah N.A., Levine M.M., Lewis K., Coia M.L., Attah-Poku M., Ojwando J., Rivers S.B., Victor J.C., Nyambane G., Hodgson A., Schödel F., Cialet M., Neuzil K.M.: Efficacy of pentavalent rotavirus vaccine against severe rotavirus gastroenteritis in infants in developing countries in sub-Saharan Africa: a randomised, double-blind, placebo-controlled trial. Lancet 2010, 376, 606–614, doi: 10.1016/S0140-6736(10)60889-6.
Open DOI Search in Google Scholar Back to article
Bakiu R., Korro K., Santovito G., Tolomeo A.: Rotavirus presence in Mediterranean mussels (Mytilus galloprovincialis) from Southwestern Albanian Coasts. Front Vet Sci Conf Abstr AquaEpi I 2016, doi: 10.3389/conf.FVETS.2016.02.00022.
Open DOI Search in Google Scholar Back to article
Bigliardi L., Cesari C., Zoni R., Sansebastiano G.E.: The concentration of viruses in water using the tangential flow ultrafiltration. Recovery effectiveness in experimental conditions. Ann Ig Med Prev Comunita 2004, 16, 281–289.
Search in Google Scholar Back to article
Black R.E., Cousens S., Johnson H.L., Lawn J.E., Rudan I., Bassani D.G., Jha P., Campbell H., Walker C.F., Cibulskis R., Eisele Th., Liu L., Mathers C.: Global, regional, and national causes of child mortality in 2008: a systematic analysis. Lancet 2010, 375, 1969–1987, doi: 10.1016/S0140-6736(10)60549-1.
Open DOI Search in Google Scholar Back to article
Bosch A., Pinto R.M., Le Guyader F.S.: Part 2 Improving molluscan shellfish safety and quality: Viral contaminants of molluscan shellfish: Detection and characterisation, in: Shellfish Safety and Quality, edited by S.E. Shumway, Woodhead Publishing/Elsevier, Cambridge, 2009, 83–107, doi: 10.1533/9781845695576.2.83.
Open DOI Search in Google Scholar Back to article
Bosch A., Sánchez G., Abbaszadegan M., Carducci A., Guix S., Guyader F.S.L., Netshikweta R., Pinto R., Poel V.H.M., Rutjes S., Sano D., Taylor M.B., Zyl W.B., Lázaro D.R., Kovač K., Sellwood J.: Analytical Methods for Virus Detection in Water and Food. Food Anal Methods 2011, 4, 4–12, doi: 10.1007/s12161-010-9161-5.
Open DOI Search in Google Scholar Back to article
Bowen M., Mijatovic-Rustempasic S., Esona M.: Rotavirus strain trends during the postlicensure vaccine era: United States, 2008–2013. J Infect Dis 2016, 214, 732, doi: 10.1093/infdis/jiw233.
Open DOI Search in Google Scholar Back to article
Cullaj A., Hasko A., Miho A., Schanz F., Brandl H., Bachofen R.: The quality of Albanian natural waters and the human impact. Environ Int 2005, 31, 133–146, doi: 10.1016/j.envint.2004.06.008.
Open DOI Search in Google Scholar Back to article
De Donno A., Liaci D., Bagordo F., Lugoli F., Gabutti G.: Mytilus galloprovincialis as a bioindicator of microbiological pollution of coastal waters: a study conducted in the Salento peninsula (Italy). J Coast Res 2008, 216–221, doi: 10.2112/05-0463.1.
Open DOI Search in Google Scholar Back to article
Denis L., Alliot E., Grzebyk D.: Clearance rate responses of Mediterranean mussels, Mytilus galloprovincialis, to variations in the flow, water temperature, food quality and quantity. Aquat Living Resour 1999, 12, 279–288, doi: 10.1016/S0990-7440(00)86639-5.
Open DOI Search in Google Scholar Back to article
Donia D., Dell’Amico M.C., Petrinca A.R., Martinucci I., Mazzei M., Tolari F., Divizia M.: Presence of hepatitis E RNA in mussels used as bio-monitors of viral marine pollution. J Virol Methods 2012, 186, 198–202, doi: 10.1016/j.jviromet.2012.06.007.
Open DOI Search in Google Scholar Back to article
Ferro D., Bakiu R., De Pittà C., Boldrin F., Cattalini F., Pucciarelli S., Miceli C., Santovito G.: Cu, Zn superoxide dismutases from Tetrahymena thermophila: molecular evolution and gene expression of the first line of antioxidant defenses. Protist 2015, 166, 131–145, doi: 10.1016/j.protis.2014.12.003.
Open DOI Search in Google Scholar Back to article
Fong T.T., Lipp E.K.: Enteric viruses of human and animals in aquatic environments: health risks, detection, and potential water quality assessment tools. Microbiol Mol Biol Rev 2005, 69, 357–371, doi: 10.1128/MMBR.69.2.357-371.2005.
Open DOI Search in Google Scholar Back to article
Formiga-Cruz M., Allard A.K., Conden-Hansson A.C., Henshilwood K., Hernroth B.E., Jofre J., Lees D.N., Lucena F., Papapetropoulou M., Rangdale R.E., Tsibouxi A., Vantarakis A., Girones R.: Evaluation of Potential Indicators of Viral Contamination in Shellfish and Their Applicability to Diverse Geographical Areas. Appl Environ Microbiol 2003, 69, 1556–1563, doi: 10.1128/AEM.69.3.1556-1563.2003.
Open DOI Search in Google Scholar Back to article
Hunt C.D., Slone E.: Long-term monitoring using resident and caged mussels in Boston Harbor yield similar spatial and temporal trends in chemical contamination. Mar Environ Res 2010, 70, 5, 343–357, doi: 10.1016/j.marenvres.2010.07.002.
Open DOI Search in Google Scholar Back to article
Kittigul L., Ekchaloemkiet S., Utrarachkij F., Siripanichgon K., Sujirarat D., Pungchitton S., Boonthum A.: An efficient virus concentration method and RT-nested PCR for detection of rotaviruses in environmental water samples. J Virol Methods 2005, 124, 117–122, doi: 10.1016/j.jviromet.2004.11.013.
Open DOI Search in Google Scholar Back to article
Kota M., Bino S., Delogu R., Simaku A., Neza B., Ruggeri F.M., Fiore L.: Epidemiology of rotavirus diarrhoea in Albania. Arch Virol 2014, 159, 2491–2495, doi: 10.1007/s00705-014-2093-4.
Open DOI Search in Google Scholar Back to article
Le Guyader F.S., Atmar R.L.: Binding and inactivation of viruses on and in food, with a focus on the role of the matrix. In: Food-borne viruses: progress and challenges, edited by M.P.G. Koopmans, D.O. Cliver, A. Bosch, ASM Press, Washington, DC, 2009, pp. 189–208, doi: 10.1128/9781555815738.
Open DOI Search in Google Scholar Back to article
Lowther J.A., Henshilwood K., Lees D.N.: Determination of norovirus contamination in oysters from two commercial harvesting areas over an extended period, using semiquantitative real-time reverse transcription PCR. J Food Prot 2008, 71, 1427–1433, doi: 10.4315/0362-028X-71.7.1427.
Open DOI Search in Google Scholar Back to article
Mohan V., Rawat S., Lokesh K.M., Mohan H.V., Avinash Reddy D., Kumar A., Bhilegaonkar K.N.: Prevalence of Rotavirus in shellfish from Southern Kerala. Vet World 2014, 7, 821–824, doi: 10.14202/vetworld.2014.821-824.
Open DOI Search in Google Scholar Back to article
Pereira M.A., Nunes M.M., Nuernberg L., Schulz D., Batista C.R.V.: Microbiological quality of oysters (Crassostrea gigas) produced and commercialized in the coastal region of Florianópolis-Brazil. Braz J Microbiol 2006, 37, 159–163, doi: 10.1590/S1517-83822006000200012.
Open DOI Search in Google Scholar Back to article
Richards G.P.: Chapter 7, Shellfish-Associated Enteric Virus Illness: Virus Localization, Disease Outbreaks and Prevention. In: Viruses in Foods, edited by S.M. Goyal, J.L. Cannon, Springer Nature, Cham, 2016, pp. 185–207, doi: 10.1007/978-3-319-30723-7.
Open DOI Search in Google Scholar Back to article
Ripabelli G., Sammarco M.L., Grasso G.M., Fanelli I., Caprioli A., Luzzi I.: Occurrence of Vibrio and other pathogenic bacteria in Mytilus galloprovincialis (mussels) harvested from Adriatic Sea, Italy. Int J Food Microbiol 1999, 49, 43–48, doi: 10.1016/s0168-1605(99)00056-2.
Open DOI Search in Google Scholar Back to article
Ruiz-Palacios G.M., Pérez-Schael I., Velázquez F.R, Abate H., Breuer Th., Clemens S.C., Cheuvart B., Espinoza F., Gillard P., Innis B.L., Cervantes Y., Linhares A.C., López P., Macías-Parra M., Ortega-Barría E., Richardson V., Rivera-Medina D.M., Rivera L., Salinas B., Pavía-Ruz N., Salmerón J., Rüttimann R., Tinoco J.C., Rubio P., Nuñez E., Guerrero M.L., Yarzábal J.P., Damaso S., Tornieporth N., Sáez-Llorens X., Vergara R.F., Vesikari T., Bouckenooghe A., Clemens R., De Vos B., O’Ryan M.: Safety and efficacy of an attenuated vaccine against severe rotavirus gastroenteritis. N Engl J Med 2006, 354, 11–22, doi: 10.1056/NEJMoa052434.
Open DOI Search in Google Scholar Back to article
Shieh Y.C., Baric R.S., Woods J.W., Calci K.R.: Molecular Surveillance of Enterovirus and Norwalk-Like Virus in Oysters Relocated to a Municipal-Sewage-Impacted Gulf Estuary. Appl Environ Microbiol 2003, 69, 7130–7136, doi: 10.1128/AEM.69.12.7130-7136.2003.
Open DOI Search in Google Scholar Back to article
Silva A.I.M., Vieira R.H.S.F., Menezes F.G.R., Fonteles-Filho A.A., Torres R.C.O., Sant’Anna E.S.: Bacteria of fecal origin in mangrove oysters (Crassostrea rhizophorae) in the Cocó River estuary, Ceará State, Brazil. Braz J Microbiol 2003, 34, 126–130, doi: 10.1590/S1517-83822004000100021.
Open DOI Search in Google Scholar Back to article
Topi T., Bani A., Malltezi J., Sulce S.: Heavy metals in soil, sediments, mussels, and water from Butrinti Lagoon (Albania). Fresenius Environ Bull 2012, 21, 3042–3051.
Search in Google Scholar Back to article
Van Heerden J., Ehlers M.M., Van Zyl W.B., Grabow W.O.K.: Incidence of adenoviruses in raw and treated water. Water Res 2003, 37, 3704–3708, doi: 10.1016/S0043-1354(03)00245-8.
Open DOI Search in Google Scholar Back to article