Human enteric viruses’ detection in mussels (Mytilus galloprovincialis) farmed in the central Adriatic Sea

Submitted: 2 February 2024
Accepted: 18 April 2024
Published: 20 May 2024
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Human enteric viruses, such as hepatitis A virus (HAV), hepatitis E virus (HEV), and norovirus genogroups I and II (NoVGI and NoVGII), cause infections, and it has been largely demonstrated that mussels play an important role if consumed as raw or undercooked food matrices. This study aimed to investigate, through qualitative and quantitative biomolecular assays, the detection of partial genomic regions belonging to the most relevant enteropathogenic viruses for humans (HAV, HEV, NoVGI and NoVGII) in mussels (Mytilus galloprovincialis) farmed along the coasts of two Italian regions on the central Adriatic Sea: Abruzzo (Casalbordino, Chieti) and Molise (Termoli, Campobasso). A total of 425 animals were sampled, and the respective georeferentiations were registered. A total of 85 pools, each composed of five subjects/aliquots, were formed (22 from Abruzzo and 63 from Molise regions). This step was followed by homogenization and RNA extraction, and then the biomolecular assays [nested reverse transcription polymerase chain reaction (PCR) and real-time reverse transcription-quantitative PCR] were performed. 1.17% of the pool was positive for HAV RNA detection (102 copies/mL), 9.41% for HEV (102-103 copies/µL), 2.35% for NoVGI (101 copies/µL), and no pool was positive for NoVGII. This study demonstrated the human enteric viruses’ presence in mussels farmed in a low-investigated marine area. Based on a one-health point of view, this paper aims to enforce the importance of biomolecular and epidemiological screenings as surveillance systems to guarantee human, animal, and environmental health.

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Amoroso MG, Di Concilio D, Langellotti AL, Martello A, Cioffi B, Suffredini E, Cozzi L, Russo V, Mauriello G, Di Pasquale S, Galiero G, Fusco G, 2021. Quantitative real-time PCR and digital PCR to evaluate residual quantity of HAV in experimentally depurated mussels. Food Environ Virol 13:329-36.
Bazzoni AM, Mudadu AG, Esposito G, Urru R, Ortu S, Mara L, Uda MT, Arras I, Lorenzoni G, Sanna G, Bazzardi R, Marongiu E, Virgilio S, Meloni D, 2019. Bacterial and viral investigations combined with determination of phytoplankton and algal biotoxins in mussels and water from a mediterranean coastal lagoon (Sardinia, Italy). J Food Protect 82:1501-11.
Chahouri A, Yacoubi B, Moukrim A, Banaoui A, 2022. Integration assay of bacteriological risks in marine environment using Salmonella spp. and multimarker response in the bivalve Donax trunculus: Novel biomonitoring approach. Chemosphere 297:134149.
Choi C, Kingsley DH, 2016. Temperature-dependent persistence of human norovirus within oysters (Crassostrea virginica). Food Environ Virol 8:141-7.
Council of the European Communities, 1991. Council Directive 91/492/EEC of 15 July 1991 laying down the health conditions for the production and the placing on the market of live bivalve molluscs. In: Official Journal, L 268 , 24/09/1991.
Croci L, Losio MN, Suffredini E, Pavoni E, Di Pasquale S, Fallacara F, Arcangeli G, 2007. Assessment of human enteric viruses in shellfish from the northern Adriatic sea. Int J Food Microbiol 114:252-7.
da Silva VC, Elois M, Savi BP, Miotto M, De Dea Lindner J, Fongaro G, Souza DSM, 2023. Bioaccumulation dynamic by crassostrea gigas oysters of viruses that are proposed as surrogates for enteric virus contamination in environmental samples. Food Environ Virol 15:1-7.
Errani F, Ponti M, Volpe E, Ciulli S, 2021. Spatial and seasonal variability of human and fish viruses in mussels inside and offshore of Ravenna’s harbour (Adriatic Sea, Italy). J Appl Microbiol 130:994-1008.
European Commission, 2005. Commission Regulation (EC) No 2073/2005 of 15 November 2005 on microbiological criteria for foodstuffs. In: Official Journal, L 338/1, 22/12/2005.
European Commission, 2019a. Commission Implementing Regulation (EU) 2019/627 of 15 March 2019 laying down uniform practical arrangements for the performance of official controls on products of animal origin intended for human consumption in accordance with Regulation (EU) 2017/625 of the European Parliament and of the Council and amending Commission Regulation (EC) No 2074/2005 as regards official controls. In: Official Journal, L 131/51, 17/05/2019.
European Commission, 2019b. Commission Implementing Regulation (EU) 2019/626 of 5 March 2019 concerning lists of third countries or regions thereof authorised for the entry into the European Union of certain animals and goods intended for human consumption, amending Implementing Regulation (EU) 2016/759 as regards these lists. In: Official Journal: L 131/51, 17/05/2019.
European Parliament, Council of the European Union, 2004. Regulation (EC) No 853/2004 of the European Parliament and of the Council of 29 April 2004 laying down specific hygiene rules for food of animal origin. In: Official Journal, L 139/55, 30/04/2004.
European Parliament, Council of the European Union, 2017. Regulation (EU) 2017/625 of the European Parliament and of the Council of 15 March 2017 on official controls and other official activities performed to ensure the application of food and feed law, rules on animal health and welfare, plant health and plant protection products, amending Regulations (EC) No 999/2001, (EC) No 396/2005, (EC) No 1069/2009, (EC) No 1107/2009, (EU) No 1151/2012, (EU) No 652/2014, (EU) 2016/429 and (EU) 2016/2031 of the European Parliament and of the Council, Council Regulations (EC) No 1/2005 and (EC) No 1099/2009 and Council Directives 98/58/EC, 1999/74/EC, 2007/43/EC, 2008/119/EC and 2008/120/EC, and repealing Regulations (EC) No 854/2004 and (EC) No 882/2004 of the European Parliament and of the Council, Council Directives 89/608/EEC, 89/662/EEC, 90/425/EEC, 91/496/EEC, 96/23/EC, 96/93/EC and 97/78/EC and Council Decision 92/438/EEC (Official Controls Regulation). In: Official Journal, L 95/1, 7/04/2017.
Farkas K, Green E, Rigby D, Cross P, Tyrrel S, Malham SK, Jones DL, 2021. Investigating awareness, fear and control associated with norovirus and other pathogens and pollutants using best-worst scaling. Sci Rep 11:11194.
Fenaux H, Chassaing M, Berger S, Gantzer C, Bertrand I, Schvoerer E, 2019. Transmission of hepatitis E virus by water: an issue still pending in industrialized countries. Water Res 151:144-57.
Ferri G, Giantomassi G, Piccinini A, Olivastri A, Vergara A, 2023. Hepatitis E virus RNA detection from hunted wild boars in central Italy: an epidemiological investigation. Food Environ Virol 15:158-66.
Fiorito F, Amoroso MG, Lambiase S, Serpe FP, Bruno T, Scaramuzzo A, Maglio P, Fusco G, Esposito M, 2019. A relationship between environmental pollutants and enteric viruses in mussels (Mytilus galloprovincialis). Environ Res 169:156-62.
Fusco G, Anastasio A, Kingsley DH, Amoroso MG, Pepe T, Fratamico PM, 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. Int J Environ Res Public Health 16:2588.
ISO, 2017. Microbiology of the food chain - horizontal method for determination of hepatitis A virus and norovirus using real-time RT-PCR. ISO Norm 15216-1:2017. International Standardization Organization ed., Geneva, Switzerland.
Johne R, Plenge-Bönig A, Hess M, Ulrich RG, Reetz J, Schielke A, 2010. Detection of a novel hepatitis E-like virus in faeces of wild rats using a nested broad-spectrum RT-PCR. J Gen Virol 91:750-8.
La Bella G, Martella V, Basanisi MG, Nobili G, Terio V, La Salandra G, 2017. Food-borne viruses in shellfish: investigation on norovirus and HAV presence in Apulia (SE Italy). Food Environ Virol 9:179-86.
La Bella G, Basanisi MG, Nobili G, Terio V, Suffredin E, La Salandra G, 2021. First report of hepatitis E virus in shellfish in southeast Italy. Appl Sci 11:43.
La Rosa G, Mancini P, Bonanno Ferraro G, Iaconelli M, Veneri C, Paradiso R, De Medici D, Vicenza T, Proroga YTR, Di Maro O, Ciccaglione AR, Bruni R, Della Rotonda M, Suffredini E, 2020. Hepatitis A virus strains circulating in the Campania region (2015-2018) assessed through bivalve biomonitoring and environmental surveillance. Viruses 13:16.
La Rosa G, Proroga YTR, De Medici D, Capuano F, Iaconelli M, Della Libera S, Suffredini E, 2018. First detection of hepatitis E virus in shellfish and in seawater from production areas in southern Italy. Food Environ Virol 10:127-31.
Macaluso G, Guercio A, Gucciardi F, Di Bella S, La Rosa G, Suffredini E, Randazzo W, Purpari G, 2021. Occurrence of human enteric viruses in shellfish along the production and distribution chain in Sicily, Italy. Foods 10:1384.
Mangeri L, Righi F, Benevenia R, Galuppini E, Tilola M, Bertasi B, Tranquillo V, Rubini S, Losio MN, Filipello V, 2024. Monitoring and genotyping of norovirus in bivalve molluscan shellfish from northern Italian seas (2018-2020). Foodborne Pathog Dis 21:27-35.
Pisano MB, Giadans CG, Flichman DM, Ré VE, Preciado MV, Valva P, 2021. Viral hepatitis update: Progress and perspectives. World J Gastroenterol 27:4018-44.
Polo D, Álvarez C, Longa Á, Romalde JL, 2014. Effectiveness of depuration for hepatitis A virus removal from mussels (Mytilus galloprovincialis). Int J Food Microbiol 180:24-9.
Purdy MA, Harrison TJ, Jameel S, Meng XJ, Okamoto H, Van der Poel WHM, Smith DB, 2017. ICTV Virus Taxonomy Profile: Hepeviridae. J Gen Virol 98:2645-6.
Purpari G, Macaluso G, Di Bella S, Gucciardi F, Mira F, Di Marco P, Lastra A, Petersen E, La Rosa G, Guercio A, 2019. Molecular characterization of human enteric viruses in food, water samples, and surface swabs in Sicily. Int J Infect Dis 80:66-72.
Razafimahefa RM, Ludwig-Begall LF, Thiry E, 2020. Cockles and mussels, alive, alive, oh-The role of bivalve molluscs as transmission vehicles for human norovirus infections. Transbound Emerg Dis 67:9-25.
Rowan NJ, 2023. Current decontamination challenges and potentially complementary solutions to safeguard the vulnerable seafood industry from recalcitrant human norovirus in live shellfish: Quo Vadis?. Sci Total Environ 874:162380.
Savini G, Casaccia C, Barile NB, Paoletti M, Pinoni C, 2009. Norovirus in bivalve molluscs: a study of the efficacy of the depuration system. Vet Ital 45:535-9.
Scarponi D, Nawrot R, Azzarone M, Pellegrini C, Gamberi F, Trincardi F, Kowalewski M, 2022. Resilient biotic response to long-term climate change in the Adriatic Sea. Global Change Biol 28:4041-53.
Stagličić N, Bojanić Varezić D, Kurtović Mrčelić J, Pavičić M, Tutman P, 2021. Marine litter on the shallow seafloor at Natura 2000 sites of the Central Eastern Adriatic Sea. Mar Pollut Bull 168:112432.
Suffredini E, Lanni L, Arcangeli G, Pepe T, Mazzette R, Ciccaglioni G, Croci L, 2014. Qualitative and quantitative assessment of viral contamination in bivalve molluscs harvested in Italy. Int J Food Microbiol 184:21-6.
Szabo K, Trojnar E, Anheyer-Behmenburg H, Binder A, Schotte U, Ellerbroek L, Klein G, Johne R, 2015. Detection of hepatitis E virus RNA in raw sausages and liver sausages from retail in Germany using an optimized method. Int J Food Microbiol 149-56.
Taffon S, Bidini G, Vichi F, Corti G, Genovese D, Kondili LA, Bindi R, Armellini F, Leoncini F, Bartoloni A, Mazzotta F, Rapicetta M, 2011. A unique HAV strain circulated in patients with acute HAV infection with different risk exposures in Tuscany, Italy. J Clin Virol 50:142-7.
Tan MTH, Ho SX, Chu JJH, Li D, 2021. Application of virome capture sequencing in shellfish sold at retail level in Singapore. Lett Appl Microbiol 73:486-94.
Van der Poel WHM, Dalton HR, Johne R, Pavio N, Bouwknegt M, Wu T, Cook N, Meng XJ, 2018. Knowledge gaps and research priorities in the prevention and control of hepatitis E virus infection. Transbound Emerg Dis 65:22-9.
Wang Y, Ling R, Erker JC, Zhang H, Li H, Desai S, Mushahwar IK, Harrison TJ, 1999. A divergent genotype of hepatitis E virus in Chinese patients with acute hepatitis. J Gen Virol 80:169-77.
Xu L, Cai J, Gao T, Ma A, 2022. Shellfish consumption and health: a comprehensive review of human studies and recommendations for enhanced public policy. Crit Rev Food Sci Nutr 62:4656-68.
Yan H, Yagyu F, Okitsu S, Nishio O, Ushijima H, 2003. Detection of norovirus (GI, GII), Sapovirus and astrovirus in fecal samples using reverse transcription single-round multiplex PCR. J Virol Methods 114:37-44.

How to Cite

1.
Ferri G, Olivieri V, Vergara A. Human enteric viruses’ detection in mussels (<i>Mytilus galloprovincialis</i>) farmed in the central Adriatic Sea. Ital J Food Safety [Internet]. 2024 May 20 [cited 2024 Dec. 22];13(3). Available from: https://www.pagepressjournals.org/ijfs/article/view/12349